Weaning The Pig: Concepts and Consequences

Weaning the pig Concepts and consequences

Edited by: J.R. Pluske J. Le Dividich M.W.A. Verstegen

Weaning the pig – concepts and consequences

Weaning the pig concepts and consequences

Edited by: J.R. Pluske J. Le Dividich M.W.A. Verstegen

Wageningen Academic P u b l i s h e r s

ISBN: 978-90-76998-17-6 e-ISBN: 978-90-8686-513-0 DOI: 10.3920/978-90-8686-513-0

Subject headings: Growth Digestive physiology Fertility

First published, 2003

Photo cover: J. Chevalier (INRA)

© Wageningen Academic Publishers The Netherlands, 2003

This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned. Nothing from this publication may be translated, reproduced, stored in a computerised system or published in any form or in any manner, including electronic, ­mechanical, reprographic or photographic, without prior written permission from the publisher, Wageningen Academic Publishers, P.O. Box 220, 6700 AE Wageningen, the Netherlands, www.WageningenAcademic.com The individual contributions in this publication and any liabilities arising from them remain the responsibility of the authors. The publisher is not responsible for possible damages, which could be a result of content derived from this publication.

Contents 1

Introduction J.R. Pluske, J. Le Dividich and M.W.A. Verstegen

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Growth of the weaned pig I.H. Williams 2.1 Introduction 2.2 The potential growth of weaned pigs 2.3 Description of growth 2.4 The growth check at weaning 2.5 Bodyweight at weaning - its importance for post-weaning growth 2.6 Can weaning weight be increased by supplementary feeding? 2.7 Do pigs stimulated to reach higher weaning weights grow faster to slaughter? 2.8 Do pigs exhibit compensatory growth? 2.9 The importance of weight gain in the first week after weaning 2.10 Minimising the growth check at weaning 2.11 Does minimising the growth check have long-term benefits? 2.12 Conclusions References

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Nutritional management of the pig in preparation for weaning R.H. King and J.R. Pluske 3.1 Introduction 3.2 The importance of weaning weight to subsequent growth 3.3 Nutrient intake before weaning 3.3.1 Supplying creep food in lactation 3.3.2 Dry creep feed intake 3.3.3 Liquid diets to enhance feed intake 3.3.4 The effects of gender on nutrient intake of neonatal pigs 3.4 The composition of diets offered during lactation 3.4.1 Dietary formulation of creep diets 3.4.2 Use of flavours in creep/starter diets 3.4.3 Presentation of the creep diet 3.5 Water for suckling pigs 3.6 Conclusions References Behavioural changes and adaptations associated with weaning P. Mormède and M. Hay Summary 4.1 Introduction

Concepts and consequences

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4.2 Neuroendocrine consequences of weaning 4.3 The critical role of food 4.4 Behaviour 4.5 Conclusion References

54 54 57 57 58

Metabolic and endocrine changes around weaning F.R. Dunshea 5.1 Introduction 5.2 The post-weaning check 5.3 Effect of weaning on metabolism 5.3.1 Lipid and carbohydrate metabolism 5.3.2 Protein metabolism 5.4 Hormonal status 5.4.1 Somatotropin and insulin-like growth factor-I 5.4.2 Insulin 5.4.3 Hypothalamic-pituitary axis 5.5 Conclusions References

61 61 61 65 65 67 68 68 72 72 74 74

Factors affecting the voluntary feed intake of the weaned pig P.H. Brooks and C.A. Tsourgiannis 6.1 Introduction 6.2 Feeding behaviour of piglets kept under ‘natural’ or ‘semi-natural’ conditions 6.3 Commercial weaning practice - an event rather than a process 6.4 Pre-weaning feed and water intake 6.5 Relationship between pre-weaning food consumption and post-weaning growth 6.6 Feeding behaviour of the post-weaned pig 6.7 Feed and water intake of weaned pigs 6.8 The significance of maintaining continuity of food intake after weaning 6.9 The interaction between water and feed intake post weaning 6.10 Liquid feeding post-weaning 6.11 Conclusions References Digestive physiology of the weaned pig H.M. Miller and R.D. Slade Summary 7.1 Introduction 7.2 Strategies for adaptation to enteral nutrition in the neonatal pig

81 81 81 86 87 91 94 96 99 102 106 108 109 117 117 117 118

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7.2.1 Preparation 7.2.2 Implementation I 7.2.3 Perspective 1 7.3 The weaned pig 7.3.1 Commercial weaning 7.3.2 Gastrointestinal, pancreatic and hepatic response 7.3.3 Small intestine morphological response 7.3.4 Small intestine carbohydrase and transporter response 7.3.5 Amino acid transport 7.3.6 Perspective 2 7.4 Regulation of post-weaning adaptation 7.4.1 Milk withdrawal 7.4.2 Weaning stress 7.4.3 Direct dietary effects 7.4.4 Indirect dietary effects 7.4.5 Perspective 3 References 8

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Diet-mediated modulation of small intestinal integrity in weaned piglets M.A.M. Vente-Spreeuwenberg and A.C. Beynen Summary 8.1 Introduction 8.2 Small intestinal integrity 8.2.1 Small intestinal morphology 8.2.2 Mucus production 8.2.3 Transepithelial permeability 8.2.4 Inflammation 8.2.5 Brush border enzyme activity 8.2.6 Animal performance 8.3 Modulation of small intestinal integrity by luminal nutrition 8.3.1 Modulation by route of administration 8.3.2 Modulation by level of energy intake 8.3.3 Modulation by dietary components 8.4 Concluding remarks References Interactions between the intestinal microflora, diet and diarrhoea, and their influences on piglet health in the immediate post-weaning period D.E. Hopwood and D.J. Hampson Summary 9.1 Changes in intestinal microflora at weaning

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145 145 145 147 148 149 149 150 150 151 151 152 155 159 185 186

199 199 199

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9.2 Major enteric diseases at weaning 9.3 Post-weaning colibacillosis (PWC) 9.4 Factors predisposing to post-weaning colibacillosis at weaning 9.4.1 The role of the small intestine 9.4.2 The role of the large intestine 9.4.3 The specific role of diet 9.4.4 The specific role of dietary non-starch polysaccharides in PWC 9.5 Conclusions Acknowledgements References 10 Aspects of intestinal immunity in the pig around weaning M.R. King, D. Kelly, P.C.H. Morel and J.R. Pluske 10.1 Introduction 10.2 Overview of immune systems 10.2.1 Active immunity 10.2.2 Passive immunity 10.3 The intestinal immune system 10.3.1 Intestinal inflammation 10.3.2 Oral tolerance 10.3.3 Development of intestinal immunity 10.4 The effect of weaning on the intestinal immune system 10.4.1 Overview of the weaning process 10.4.2 Alteration of intestinal morphology 10.4.3 Activation of the intestinal immune system 10.5 Conclusion References 11 Nutritional requirements of the weaned pig M.D. Tokach, S.S. Dritz, R.D. Goodband and J.L. Nelssen Summary 11.1 Introduction 11.2 Importance of pig weight and age 11.3 Basis of nutrient specifications for weaner pigs 11.3.1 Ingredient selection based on digestive capacity 11.4 Nutrient requirements of the weaned pig 11.4.1 Energy 11.4.2 Amino acids 11.4.3 Other approaches to determining a requirement estimate 11.4.4 Vitamins 11.4.5 Minerals 11.4.6 Post-weaning diarrhea and zinc oxide. 11.4.7 Organic trace minerals

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201 202 204 204 205 205 206 211 212 212 219 219 220 220 223 224 227 228 231 233 233 234 236 244 244 259 259 259 259 262 263 264 264 264 265 268 269 270 271

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11.5 11.5.1 11.5.2 11.5.3

Selection of ingredients for the weaned pig Energy sources Protein sources Non-nutritive Feed additives (eg., antibiotics, enzymes, organic acids, etc.) 11.6 Example of phase feeding program for early weaned pigs 11.6.1 SEW diet - weaning to 5 kg 11.6.2 Transition diet - 5 to 7 kg 11.6.3 Phase 2 - 7 to 11 kg 11.6.4 Phase 3 - 11.5 to 23 kg 11.7 Importance of management in the success of the nutritional program 11.7.1 Management to encourage feed intake 11.7.2 Adjust feeders frequently to minimize feed wastage References 12 Intestinal nutrient requirements in weanling pigs D. Burrin and B. Stoll 12.1 Introduction 12.2 Changes in gut physiology during weaning 12.2.1 Acute phase 12.2.2 Adaptive phase 12.3 Intestinal nutrient utilization in young pigs 12.3.1 Physiological and cellular basis of gut metabolism 12.3.2 Major oxidative fuels 12.3.3 Essential amino acid utilization 12.3.4 Interactions between nutrition and enteric health and function 12.4 Summary and perspectives Acknowledgments References 13 Environmental requirements and housing of the weaned pig F. Madec, J. Le Dividich, J.R. Pluske and M.W.A. Verstegen 13.1 Introduction 13.2 Environmental requirements of the weaned pig 13.2.1 Events related to weaning that affect thermal requirements 13.2.2 Ambient temperature 13.2.3 Relative humidity and ventilation 13.2.4 Lighting 13.2.5 Effects of non-optimal climate on performance 13.3 Pen structure 13.3.1 Flooring materials 13.3.2 Feeders and waterers

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13.3.3 13.3.4 13.4 13.4.1

Stocking densities Group size Housing as a cause of poor health of weaned pigs Evidence that housing conditions predispose pigs to digestive disorders 13.4.2 Impact of non-optimal indoor climate on the pig’s health status 13.4.3 Multifactorial nature of post-weaning disorders: risk factors associated with housing and management 13.4.4 Integrating the risk factors to improve health 13.5 Conclusion References 14 Saving and rearing underprivileged and supernumerary piglets, and improving their health at weaning J. Le Dividich, G.P. Martineau, F. Madec and P. Orgeur 14.1 Introduction 14.2 What are underprivileged and supernumeraries? 14.3 Reasons accounting for variation in birthweight and weaning weight 14.3.1 Variation in birth weight 14.3.2 Variation in weaning weight 14.4 Differences between underprivileged and “normal” piglets 14.4.1 Body composition 14.4.2 Performance of underprivileged pigs 14.5 Management practices to improve survival and growth of the underprivileged pigs 14.5.1 Providing assistance to the underprivileged piglets at birth 14.5.2 Cross fostering 14.5.3 Split weaning 14.5.4 Feeding strategy 14.6 Growth potential of underprivileged piglets 14.7 Supernumerary piglets 14.7.1 Weaning at day 1-3 14.7.2 Fostering onto a nurse sow 14.7.3 Weaning at one week of age 14.8 Management to improve the health of piglets 14.8.1 All-in / All-out management system 14.8.2 Segregation 14.9 Conclusion: the need for research References

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347 348 349 349 350 351 353 353 355

361 361 362 363 363 364 365 365 366 367 368 369 370 370 371 371 372 372 372 373 373 374 376 377

Weaning the pig

Contents

15 Productivity and longevity of weaned sows A. Prunier, N. Soede, H. Quesnel and B. Kemp 15.1 Introduction 15.2 Reproductive causes of culling 15.3 Consequences of lactation and weaning on the reproductive axis 15.3.1 Postpartum inhibition 15.3.2 Removal of the inhibition of the hypothalamic-pituitaryovarian axis at weaning 15.4 Variation in reproductive performance: extent and sources of variation 15.4.1 Components of fertility and prolificacy 15.4.2 Influence of nutritional factors 15.4.3 Influence of lactational characteristics 15.4.4 Influence of the physical and social environment 15.4.5 Relationships between WEI, litter size and farrowing rate 15.5 Conclusion References

385 385 385 388 388 392 394 394 394 402 404 406 408 409

Conclusions

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List of authors

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Index

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Concepts and consequences

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1

Introduction

The weaning age of pigs has been reduced from about 8 weeks of age in the 1950s and 1960s down to a current average weaning age of 22-26 days of age that is practiced in many pig-producing countries, although even earlier weaning ages (< 21 days) are adopted with some systems. The reduction in weaning age occurred largely because of the productivity increases, both in the growing and breeding herds, which were achievable. However, the inevitable shift to earlier weaning ages presented many problems concerning the nutrition, housing, health, behavioural and environmental requirements of the young pig, as well as having consequences for the fertility of the sow. These are especially pertinent in systems where pigs are weaned at less than 21 days of age, such as segregated early weaning practices. Much research, combined with field experience, has minimized the stressors encountered at weaning so that good levels of production can be achieved after weaning. Nevertheless, changes in the global business of pig production continue to occur and must be dealt with. Of recent interest, particularly in Europe, has been the increasing awareness in society with respect to animal welfare, food safety, the environment, and the ‘quality’ of production, especially with respect to antibiotics as growth promoters. These (relatively) recent events have instigated a flood of new research into fields concerning, for example, optimum gut ‘health’ and immune function that, until recently, have largely been ignored in weaner pig production. Consequently, issues such as enteric diseases, welfare and the intestinal nutritional requirements of the weaned pig are under increased scrutiny and attention as producers, feed manufacturers, scientists and managers attempt to resolve these new issues. It is also increasingly evident that the events surrounding weaning can have profound and life-long consequences in both the growing and breeding herds. Collectively, the process of ‘weaning’ has never been considered as more important as it is nowadays. In light of these changes and developments, “Weaning the Pig: Concepts and Consequences” is timely and has been compiled to provide the reader with an up to date account of all facets related to the weaning process, including the fate of the weaned sow. The material in the book covers the following areas associated with the weaning process: growth of the weaned pig, nutritional management in preparation for weaning, behavioural changes and adaptations around weaning, voluntary feed intake, digestive physiology, modulation of small intestinal integrity, the intestinal microflora and diarrhoeal diseases after weaning, intestinal immunity, nutritional requirements and intestinal requirements of the weaned pig, environmental and housing issues after weaning, saving and rearing supernumery and underprivileged piglets, and productivity and longevity of the weaned sow.

Concepts and consequences

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Pluske, Le Dividich and Verstegen

World-renowned experts and specialists from numerous countries have written the chapters, and are applicable to all people involved in pig production, health and disease, research, management and extension throughout the world. The information contained can be used to modify and (or) develop nutritional, environmental, housing, disease, welfare and management strategies to best handle the weaning process. Developments in our knowledge may also help to update courses in the field of pig science and to interest those who teach animal production principles. John Pluske Jean Le Dividich Martin Verstegen

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2

Growth of the weaned pig I.H. Williams

2.1

Introduction

Pigs are capable of extremely rapid growth after weaning but there are a host of factors that limit the extent to which this potential is expressed. The weight of the pig at weaning, its nutrition and growth rate in the immediate post-weaning period, and the physical, microbiological and psychological environment are all factors that interact to determine food intake and subsequent growth. The age at weaning is variable and so weight at weaning can vary two or three fold. In most countries it is common practice to wean at 3 to 4 weeks when pigs weigh in excess of 6 kg but, in other countries, particularly North America, weaning pigs before three weeks of age of age is common. The main reason for early weaning is to reduce the transfer of disease from the sow but younger, lighter piglets require a higher standard of management and require better nutrition and more stringent environmental conditions. This chapter begins by outlining the young pig’s potential for growth followed by a simple description of growth and its principles. This is followed by a consideration of how bodyweight and nutrition impinge on growth. Other factors that limit growth will be considered in subsequent chapters.

2.2

The potential growth of weaned pigs

Growth rates of 100, 200 and 400 g/d in the first, second and third weeks after weaning at 21 days have been suggested by Whittemore and Green (2001) as commercially acceptable targets in the absence of observed clinical disease and overt stress. However, these growth rates represent substantial underperformance. The same authors suggest that a healthy pig at 3 weeks of age weighing 5 kg and given unrestricted food intake in the experimental facility at Edinburgh will grow at 500 g/d, twice the commercial performance. Yet even this rapid growth may not represent the true growth potential of the young pig. If piglets are weaned very early in life (1 to 2 days) and given liquid diets based on cow’s milk, growth rates in excess of 500 g/d can be achieved. For example, Hodge (1974) removed piglets from the sow when they were 2 days old and fed them ad libitum on reconstituted cow’s whole milk. Between 10 and 30 days of age his pigs grew at 571 g/d and between 30 and 50 days of age they grew at 832 g/d. Similar growth rates for piglets removed from sow at 2 days of age and fed milk have been demonstrated by Williams (1976) and by Harrell et al. (1993). If similar

Concepts and consequences

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Williams

experiments to those of Hodge (1974) were conducted with modern-day genotypes, piglets might grow even faster on milk and demonstrate a higher potential. There can be no doubt that the potential for growth of the young pig is extremely high and is between two and three times that which is commonly observed under the best commercial conditions. The question is, why is this potential rarely if ever reached and what can be done to lift performance closer to potential?

2.3

Description of growth

There has been much debate in recent years about the best way to describe growth because of the interest in modelling growth (Black, 1995). Most models are based on a prediction of the protein mass and its incrementation, and some defined relationship between the gain in protein and lipid. Gains in protein and lipid are summed to give gain in liveweight. If the liveweights of animals that have been fed ad libitum on high-quality diets throughout life are plotted against time they produce an “S-shaped” curve, termed a sigmoidal growth curve (Lawrence and Fowler, 1997). Whittemore and Green (2001) have put forward a compelling argument that the sigmoid growth in pigs from birth to maturity can best be described by a Gompertz function: Daily gain = liveweight * B * ln(weight at maturity/liveweight), where B is a growth coefficient. Sigmoidal growth has two main phases. The first is early in life where growth increases. The second is where growth decreases and finally ceases when animals reach maturity. These phases are linked at the point of inflection where growth is linear and this generally occurs at approximately one third of mature body size (Lawrence and Fowler, 1997). The weaned pig fits into phase one, that of increasing or accelerating growth. The Gompertz function requires two parameters, an asymptote or description of maturity and a growth coefficient, which are not independent of each other. An increase in one will be accompanied by an increase in the other. This has some important ramifications for the growth of animals. It means that animals have predetermined growth paths and that there are large, fast growing animals and smaller, slower growing animals. It means that a larger genotype or a pig with a greater propensity for growth will, at any age, be bigger and grow faster than a smaller genotype.

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Growth of the weaned pig

What the Gompertz function does not describe is the growth check that usually occurs at weaning and the recovery phase that follows. At weaning it is common for piglets to lose weight and display negative growth for several days and not recover their pre-weaning weight for perhaps 7 or even 10 days (Pluske et al., 1995). When they do begin their recovery phase, do they exhibit any signs of compensation? That is, do they grow faster than their contemporaries at the same weight who have not experienced the same check in growth or do they grow at the same rate and simply take longer to market weight. This will be addressed later in this chapter.

2.4

The growth check at weaning

At weaning the piglet faces three challenges. First, there are major changes to its food supply. Not only does the piglet have to find its own food from a creep feeder but the new food is more bulky, is often composed of ingredients that the piglet has not previously encountered, and it is 88% dry. By contrast, sow’s milk is 80% water and the dry matter (20%) is composed of protein (30%), fat (40%) and lactose (25%), but no starch. True digestibilities of fat and lactose are close to 100% and ileal digestibilities of amino acids are also very high at 92% (Mavromichalis et al., 2001). Creep feed is less digestible (80 to 90%), often contains a mixture of plant and animal proteins, contains mostly starch instead of lactose, and has very little fat relative to sow’s milk. As a consequence the digestive tract of the piglet has to make a major shift away from digesting fat towards digesting complex carbohydrates. In addition, it has to cope with a very large increase in dry matter intake if the growth of the newly-weaned piglet is to be maintained. For example, a piglet growing at 250 g/d would need to eat about 200 g of dry matter per day from sow’s milk while consumption of a high-density creep would need to reach at least 300 g/d, a 50% increase, and even more if lower-quality creep diets are used. Associated with these changes in the supply of food are alterations of the digestive tract that may have long-term (one or more weeks) ramifications. When the milk supply ceases abruptly the structure and function of the digestive tract begins to change immediately within hours. Villous height reduces, crypt depth increases, and there is a reduction in the absorptive capacity because the specific activity of the digestive enzymes, lactase and sucrase, decreases. Poor absorption of nutrients in the small intestine is often associated with proliferation of enterotoxigenic bacteria (mainly Escherichia coli) and/or fermentation of less digestible nutrients in the large intestine (McCracken and Kelly, 1993). Either way, this may lead to diarrhoea. The second major challenge at weaning for the piglet is to cope with the change in the physical environment. At weaning litters are generally mixed together into weaner pools. Having learnt to live in the farrowing pen with its mother and littermates it now has to learn to live without its mother and face competition with many more pigs, up to 250. The problem is to design a weaner pen that allows

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individual piglets to find their own comfort zone. Because of the great variation in food intake it is almost impossible to design an environment where all piglets will be within their thermoneutral zone. For example, when a piglet increases its food intake from maintenance to twice maintenance its lower critical temperature is reduced by 3°C (Close and Stanier, 1984). So there could be a difference of 12°C in lower critical temperature between a piglet that is not eating compared with one that is eating at maximum, say 4 times maintenance. If room temperatures are set to keep the pigs that are eating within their thermoneutral zone then the piglets not eating will be severely cold stressed. If room temperatures are raised so that piglets not eating are within their comfort zone, other piglets that are eating are likely to be heat stressed. The third challenge at weaning is the psychological stress that accompanies moving and mixing. Although many workers believe that this depresses growth the extent of this influence is unknown, but will be considered in a subsequent chapter. When all these changes are taken into account it is little wonder that the rate of growth of the piglet falls after weaning, and the extent of the depression in growth depends on how rapidly the piglet can adjust to its new circumstances and regain homeostasis.

2.5

Bodyweight at weaning - its importance for post-weaning growth

The Gompertz description of growth predicts that a pig of large mature body size will be larger and grow faster at any given age than a pig of smaller size. Producers have always known that heavier pigs at birth are heavier at weaning and that heavier pigs at weaning grow faster after weaning than smaller pigs and, in most instances, are also heavier at slaughter. So the difference in weight at weaning is not just maintained but it is magnified as the pig grows because the heavier pigs grow faster than their lighter counterparts at all ages. There are several studies that substantiate this view. Birth weight is positively correlated with weight at weaning (McBride et al., 1965; McConnell et al., 1987; Cranwell et al., 1995; Dunshea et al., 2003), weight at one week of age is highly correlated with weaning weight (Miller et al., 1999) and weight at weaning is highly correlated with post-weaning performance (Miller et al., 1999; Lawler et al., 2002). There are also several studies where bodyweights at various ages have been quantified for their influence on subsequent growth to slaughter. Campbell (1989) analysed the weaning records from a large piggery in Australia and found that a difference of 1.8 kg between pigs weaned at 25 to 29 days of age (6.14 verses 7.95 kg) increased to 5 kg at 78 days and 10 kg at 150 days. Mahan and Lepine

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Growth of the weaned pig

(1991) found that pigs with weaning weights of 4.1 to 5.0 kg required 11 to 20 days longer to reach slaughter at 105 kg than piglets with weaning weights of 7.3 to 8.6 kg. More recently, Wolter and Ellis (2001) reached a similar conclusion after they found that a difference of 1.5 kg (3.9 versus 5.4 kg) in pigs weaned at 3 weeks of age was translated into a growth difference of 8.6 days at slaughter. In a most comprehensive study on lifetime and post-weaning determinants of performance indices of pigs Dunshea et al. (2003) found that a difference in birthweight of 0.37 kg (1.86 vs 1.39 kg) had increased to 1.9 kg (5.22 vs 3.21 kg) by two weeks of age and 13 kg (107.1 vs 94.3 kg) by 23 weeks of age. Because of the great importance of bodyweight at weaning, research has focused on two questions. Can the growth of piglets during lactation be stimulated so that they are heavier at weaning and, if so, will this larger pig at weaning outperform a lighter counterpart in growth after weaning?

2.6

Can weaning weight be increased by supplementary feeding?

The main argument for offering sucking piglets supplementary food from a creep feeder is that it can satisfy the ever-widening energy gap between the piglet’s energy requirements and the dwindling supply of milk. Since Harrell et al. (1993) have calculated that the supply of sows’s milk probably begins to limit growth at about 10 days of age, piglets offered creep should be heavier at weaning and be better able to withstand the stresses at weaning. In the 1950s and 1960s when it was common to wean piglets at 8 weeks of age, Lucas and Lodge (1961) demonstrated the importance of offering creep feed before weaning. They raised weaning weight from 12 to 20 kg but found that significant consumption of creep did not begin until the piglets were four weeks or older. As the age of weaning was reduced to as little as two or three weeks it was thought that creep feeding might become even more important because of the susceptibility of smaller pigs to adverse environmental conditions. However, despite a large number of studies conducted in many parts of the world the magic formula that encourages creep consumption before the piglets were 3 weeks of age has eluded research workers and producers. Pluske et al. (1995) analysed the results of several experiments and reached two conclusions. First, that consumption of creep feed before weaning is highly variable and at best might contribute approximately 17% of energy intake and, at worst, zero. Perhaps more baffling is the relatively poor relationship between the amount of creep consumed and the weight at weaning suggesting that creep feed might be a substitute for rather than a supplement to sow’s milk. This is exemplified by the work of Toplis et al. (1999) who introduced creep at 14 days and then weaned the piglets at 24 days. Piglets receiving no creep weighed 6.9 kg at weaning, those that were offered creep

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in dry form consumed 91 g over the 10 days and were 6.5 kg at weaning, and piglets offered creep as a gruel (1:2 meal to water) ate 374 g/piglet over the 10 days and weighed 6.7 kg. So despite consuming sufficient gruel that should have, by calculation, increased weaning weight by about 5%, no increase could be measured. A similar example comes from the work of Brown et al. (1999). They coaxed sucking piglets to drink cow’s whole milk at 12 days of age and measured a mean dry matter intake of 332 g dry matter/week between 12 and 19 days, an intake that should have been sufficient to stimulate growth by about 0.4 kg. Yet they found that the piglets that drank milk were the same bodyweight as the controls at weaning at 19 days. Growth of piglets during lactation can be stimulated if food is offered in a liquid form early enough in life, and Reale (1987) was one of the first to demonstrate this. He offered milk to piglets when they were a week old and, by the time they had reached a weaning age of four weeks, they weighed 9.6 kg and had grown an extra 1.8 kg (24% increase in weight) over piglets not receiving supplementary milk. Similar results have been obtained by Dunshea et al. (1997b), who offered supplemental milk to piglets at 10 days of age and measured a 10% stimulation in growth by the time the pigs were 20 days old. As suggested above, the success of stimulating growth by offering supplementary milk during lactation probably depends on the age that piglets are offered the milk. For example, Armstrong and Clawson (1980) offered milk to piglets at three weeks of age but failed to stimulate growth suggesting perhaps that piglets were too settled in suckling behaviour to take in extra milk. Another way to increase weight at weaning is to split wean the litter, a practice where half the litter is weaned at say 20 days (generally the heavier pigs) leaving the lighter pigs to remain suckling for an extra week to obtain more milk per piglet. Several workers have shown that the light piglets that remain with the sow grow faster than their counterparts that have to compete with their larger littermates (Cox et al., 1983; Edwards et al., 1985; English et al., 1987; Pluske and Williams, 1996). For example, Pluske and Williams (1996) split weaned litters at 22 days of age and demonstrated that the growth rate of light pigs could be increased by 60% in the following week. When the light piglets in the split-weaned litters were weaned at 29 days they weighed 15% more than their counterparts in the full litters. This stimulation of growth was brought about by a 50% increase in milk consumption because the piglets learned to suck multiple teats and there was a longer duration of sucking during letdown. More milk per piglet and better growth of piglets might also be achieved by increasing the milk output of the sow through better nutrition (see a later chapter by R.H. King and J.R. Pluske) or by infusing sows with insulin (see McCauley et al., 1999).

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Growth of the weaned pig

The conclusion is that supplementary feeding during lactation can increase weaning weight if the food is offered early in life in a liquid form. If the supply of sow’s milk can be increased then weaning weights are likely to be greater. However dry diets are unlikely to be effective if offered early in life and are only likely to be of value in situations where piglets are weaned late, for example, at four or five weeks of age. Supplementary or creep feeding has been practised for reasons other than simply increasing the weight at weaning. It has been suggested that exposure to dry food would allow piglets to learn how to source dry food from a feeder, drink water, accustom the digestive tract to dry food, induce the necessary enzymes for its digestion and help prepare the piglet to cope better with many of the potential allergens contained in plant foods. Evidence that any of these benefits might accrue if creep feed is offered is also scarce. Pluske et al. (1995) concluded that there was a modest but non-significant relationship between gain after weaning and creep intake during suckling. They questioned the value of creep feeding particularly for early-weaned pigs but suggested that creep feed may still be of some value for pigs weaned after 3 weeks of age. However, if piglets can be stimulated to eat a reasonable quantity of creep feed in lactation it may pay dividends after weaning. By feeding gruel, Toplis et al. (1999) stimulated piglets to eat 374g of creep over 10 days and, although this did not increase weaning weight, it did stimulate performance after weaning. Piglets fed gruel grew 150% faster (49 vs 125 g/d) than piglets that ate no creep in the first week after weaning and 30% faster (317 vs 416 g/d) for 5 weeks after weaning.

2.7

Do pigs stimulated to reach higher weaning weights grow faster to slaughter?

The philosophy for stimulating piglets to reach a higher weaning weight is that they will behave in a similar way to piglets that are naturally heavier at weaning and grow faster than piglets not stimulated during lactation. Put another way, can supplementary nutrition during lactation be used to raise a piglet from a lower to a higher growth curve? If food intake is genetically determined to drive growth that is also genetically programmed, as it must be, it is most unlikely that a transient period of higher-than-normal nutrition will alter a long-term food setting in the hypothalamus. If this is correct the expectation would be that any increase in weight brought about an increase in growth would, at best, be maintained and, at worst, disappear with time. There have been many attempts to increase weaning weight but relatively few attempts to measure the long-term benefits. Offering piglets dry food from a creep has mostly been unsuccessful in stimulating growth during lactation but increasing

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the milk available to each piglet by split weaning or offering it as a supplement has consistently stimulated growth. Pluske and Williams (1996) increased the growth of light piglets by split weaning litters at 3 weeks of age. These piglets grew faster than their contemporaries left as whole litters and weighed 1 kg more at full weaning at 4 weeks (7.7 vs 6.7 kg). However by nine weeks of age the difference in weight had vanished (19.3 vs 19.3 kg). Edwards et al. (1985) achieved a weight difference of 0.4 kg by split weaning and noted that post-weaning growth rate was no different between the heavy and light pigs. Wolter et al. (2002) stimulated the growth of piglets by offering supplementary milk at 3 days of age. By 3 weeks the supplemented piglets weighed 0.9 kg more (6.6 vs 5.7 kg) than the unsupplemented piglets. This increase in weight was not translated into a significant increase in post-weaning growth and overall growth from weaning to 110 kg was almost identical for the supplemented versus the unsupplemented pigs (827 vs 820 g/d). By contrast Dunshea et al. (1997a) found that increasing growth rate during suckling had longer-term benefits. They found that skim milk fed to piglets at 10 days of age increased weaning weight by 0.7 kg of (7.3 vs 6.6 kg) and that this extra growth was still evident at 42 days (14.7 vs 12.2 kg) and 120 days (64.5 vs 60.6 kg). Do the data of Dunshea et al. (1997a) suggest that supplementary feeding has stimulated piglets to a higher growth path? The answer is uncertain but recent data from Wolter et al. (2002) are helpful in addressing this question. In an elegant experiment and, to my knowledge the only one of its kind, Wolter et al. (2002) investigated how weaning weight affected growth to slaughter. They attempted to measure the importance of weaning weight as a measure of the growth curve versus weaning weight as consequence of previous nutrition. They separated piglets into light and heavy at birth and supplemented half the piglets with a milk replacer beginning at three days of age (Table 2.1). By separating pigs at birth into light

Table 2.1. How birth weight (Heavy vs Light), weaning weight and supplementary milk in lactation (Milk vs No milk) influence food intake and growth to slaughter (from Wolter et al., 2002).

Weight (kg) Birth Weaning (20d) Weaning to 110 kg liveweight Food intake (g/d) Growth rate (g/d)

24

Heavy

Light

Milk

No milk

1.83 6.6

1.38 5.7

1.58 6.6

1.58 5.7

1866 851

1783 796

1841 827

1808 820

Weaning the pig

Growth of the weaned pig

and heavy they achieved a weight difference at weaning of 0.9 kg. The same difference in weight was induced at 20 days by feeding half the piglets supplementary milk. The pigs that were heavier at weaning because of their birth-weight advantage ate more food and grew faster (7%) after weaning than their lighter counterparts. By contrast, the pigs that were heavier at weaning because they were offered supplementary milk during lactation failed to maintain the advantage and consumed similar amounts of food as their lighter counterparts. Wolter et al. (2002) concluded that supplemental milk replacer is unlikely to be an effective strategy for increasing post-weaning performance. However, the work of Dunshea et al. (1997a) cannot be ignored and a possible explanation of their results is that they provided a supplement that allowed pigs to exhibit compensation, a topic discussed in the next section.

2.8

Do pigs exhibit compensatory growth?

Compensatory or catch-up growth is the growth of an animal fed ad libitum after a period of nutritional stress, and it is higher than the growth of a genetically-identical animal in the same environment at the same body weight during normal growth (Hogg, 1991). Interest in compensatory growth began initially with grazing animals because in most temperate parts of the world there is an abundance of food at one time of the year and a scarcity at another. This leads to rapid growth at one time of the year followed by weight loss at another. Whether animals exhibit compensatory gain after a period of restriction depends on several factors including the severity of restriction, the duration of the restriction and the stage of maturity when the restriction is applied; the younger the animal, the less likely it is to exhibit compensatory growth. For example, sheep less than 3 months old (Ryan, 1990) and cattle below 4 months old (Morgan, 1972) do not show compensatory growth. Pigs might be different. McCance (1960) weaned piglets at 10 days of age and severely restricted their food intake so that they gained only 2 kg in a year. When allowed to rehabilitate with food offered ad libitum they grew at high rates and, according to Widdowson and Lister (1991), showed some signs of compensatory growth despite the young age at which their gross nutritional insult was imposed. Despite an exhaustive literature on compensatory growth (see reviews by O’Donovan, 1984; Ryan, 1990; Hogg, 1991; Lawrence and Fowler, 1997) the underlying mechanisms remain elusive. The most consistent observations in compensating animals are that they are more efficient in the initial stages of rehabilitation and that this may be followed by a higher-than-normal food intake. The common explanation for increased efficiency involves changes in size and possibly metabolic activity of the internal organs such as the liver, kidney, and gastro-

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intestinal tract. In a well-nourished animal these organs make up 10 to 15% of the liveweight and make a disproportionately high contribution to the fasting heat of production, about 40% (Koong et al., 1983). When nutrition is restricted these organs reduce in size and possibly metabolic rate and this allows the animal to conserve energy and function on less. When rehabilitation begins and food becomes available, these organs take time to build up their size and metabolic rate and, in the meantime, there is extra energy available for the animal to deposit in body tissues. Pigs reared under intensive conditions are in a very different situation from grazing animals and are rarely short of food or specific nutrients except in the early stages of their growth, that is, before weaning and just after. At weaning the stresses are often sufficient to reduce food intake to very low levels and growth is often zero or negative, a situation where compensatory growth might apply. Sow’s milk has low protein relative to its energy content and is deficient in protein for maximum lean gain (Campbell and Dunkin, 1982; Williams, 1995). After about 10 days of lactation the potential intake of milk by the piglets begins to exceed the production from the sow so growth of the piglets starts to fall below their potential (Harrell et al., 1993). So the relative deficiency of protein plus the restriction in quantity of milk that together limit growth represent another situation that might invoke compensation. Several workers have demonstrated compensatory growth in young pigs but the most comprehensive experiments are those of Campbell and Dunkin (1983a, b and c) who have clearly demonstrated that very young pigs will compensate when deprived of protein or energy or both, and will do so even when given fixed intakes of food. In the previous section reference was made to work of Dunshea et al. (1997a) who supplemented piglets at 10 days of age with skim milk and measured a 0.7 kg increase in weaning weight which was still evident at 60 kg liveweight. Could it be that the skim milk allowed the piglets to compensate and return to their preprogrammed growth curve? Since sow’s milk is known to be deficient in protein for maximum lean gain, skim milk with its high protein content would make an excellent supplement to sow’s milk.

2.9

The importance of weight gain in the first week after weaning

The aim of producers is to encourage piglets to make a smooth transition between drinking milk from the sow and eating solid feed after weaning with minimal interruption to growth. The importance of the rate of growth in the first week after weaning in determining growth to slaughter is shown in calculations made by Pluske et al. (1995). They analysed data from Pollman (1993) showing that if pigs maintained weight during the first week after weaning they reached slaughter weight in 178 days but, if pigs grew at 115 g/d or better in the first week, age at slaughter

26

Weaning the pig

Growth of the weaned pig

was reduced by 15 days to 163 days. This means that a 0.9 kg weight difference one week after weaning becomes a 12 kg difference in weight at slaughter. Similarly, Tokach et al. (1992) showed that pigs gaining 225 g/d were 1.6 kg heavier at the end of the first week after weaning than pigs that maintained weight and were 8 kg heavier at slaughter at 156 days.

2.10

Minimising the growth check at weaning

The extent and duration of the interruption or growth check is highly variable. Pluske et al. (1995) concluded that it often takes pigs two or even three weeks to recover their energy intake and grow at the same rate as they did before weaning, let alone grow faster to begin to reach their potential. Minimising the growth check at weaning depends on the amount of food the piglet can eat. Fowler and Gill (1989) calculated that if a weaned pig at 21 days of age was to grow at 280 g/d, a growth akin to growth on the sow, it would need to eat 7.8 MJ of DE. Hence, it would need to eat 500 g of a starter diet containing 15.5 MJ of DE, an intake that is never seen under experimental conditions let alone in commercial practice. Campbell (1989) believes that practical nutrition of the young pig at weaning is more of an art than a science and has suggested that a dietary regime that is highly successful and repeatable at a research station may not stand up to the rigours of commercial practice. Such a comment simply reflects the number of factors that impinge and interact on the animal at weaning. However there are some general nutritional principles that have been established as far as nutrition of the young pig is concerned. High food intake and hence high growth rates with minimal digestive disturbances can only be achieved consistently when high-density, highly-digestible diets are used. Starter diets are generally required to ease the transition from milk (high fat, high lactose) to plant based diets that are much lower in fat, and contain high non-starch polysaccharides. Such diets generally need to contain high-quality animal products of milk origin and/or products derived from blood. The younger the pig is at weaning the more important this becomes and this is nicely demonstrated in recent data from Dunshea et al. (2002a). They offered piglets a traditional weaner diet containing wheat (55%), lupins (5%), soybean meal (5%) meatmeal (6.6%), fish meal (8.3%) skim milk (2%) and blood meal (2.6%) and whey powder (10%) and weaned them at either 14 or 24 days of age. The older pigs at weaning coped much better than the younger pigs (Table 2.2) with this sort of diet and gained weight during the first week after weaning while the younger pigs lost weight. In the 1970s it was generally regarded that the most profitable time to wean pigs was between 3 and 5 weeks. During the 1980s this changed and interest was rekindled in weaning pigs earlier largely because of two findings. The first was the realisation that sow’s milk begins to impose a limit on the growth of piglets at about

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Table 2.2. Age at weaning and its effect on growth (g/d) after weaning (from Dunshea et al., 2002a). Age at weaning (d) Days after weaning

14

24

0-7 7 - 14 14 - 21

-16 187 333

162 340 460

day 10 of age and, by 3 weeks, the limitation becomes severe enough to reduce piglet growth. Second, piglets at two weeks of age are relatively free of disease and, the longer they stay with the sow, the more disease organisms they are likely to acquire. So early weaning was thought to be a way of reducing and controlling disease and overcoming the limitation of milk imposed by the sow. Successful early weaning requires specialised diets if the growth check at weaning is to be minimised. In the early 1990s, nutritionists at Kansas State University began to develop a dietary program for early weaning to ease the transition from sow’s milk to solid food (see chapter by M. Tokach et al.). The program was based on feeding piglets as soon as they were weaned with milk products and animal plasma proteins. Products from porcine blood, particularly porcine plasma, have now been tested in many studies and seem to be mandatory for diets in North America. It seems that an inclusion rate of 6% is likely to stimulate food intake of young pigs, particularly in situations where enteric disease is more prevalent (Coffey and Cromwell, 2001). The most favoured explanation of the stimulation of food intake is that it is due to the presence of immunoglobulins and presumably immunoglobulins of pig origin might be more effective than those derived from cow’s milk. But, because of the concern about feeding animal proteins to the same species, there is now interest in looking at other sources of immunoglobulins. Products from cows are also effective in stimulating food intake and growth. Pluske et al. (1999) weaned pigs at 4 weeks and found that 5% spray-dried colostrum stimulated food intake by 12% in the first week after weaning. They increased the amount to 10% and stimulated food intake by 25%. This extra food intake boosted growth by 40% and 80% respectively so that pigs on the highest level of colostrum grew in excess of 200 g/d in the first week after weaning, a very acceptable rate of growth. King et al. (2001) have also found a 25% stimulation to food intake in the first week after weaning by adding 6% bovine colostrum. They found a lesser,

28

Weaning the pig

Growth of the weaned pig

non-significant stimulation with spray-dried bovine plasma. Dunshea et al. (2002b) have recently compared a number of animal products containing immunoglobulins and, rather than using spray-dried products from commercial sources, they freeze-dried their own products to preserve the potency of the immunoglobulins. They compared porcine and bovine plasma, bovine colostrum and commercially produced skim milk and found relatively little difference between the protein sources in the performance of pigs weaned at 14 days. However, they did point out that their studies were conducted in a ‘clean’ research environment. There is little doubt that high-quality animal proteins are far superior at stimulating growth in early-weaned pigs and even small amounts of plant protein will depress performance (see Dunshea et al., 2002b; Liu et al., 2001). Advances in technology have allowed liquid feeding systems to be a viable commercial option and, as a consequence, there is now interest in using liquid milk to stimulate food intake and growth. Pluske et al. (1996a) demonstrated that, given a similar intake, fresh milk obtained from sheep maintained villous height better than a dry diet based on skim milk powder and fish meal. They found that villous height could also be maintained with fresh cow’s milk and the more milk consumed the greater the height of the villi or, alternatively, less villous atrophy (Pluske et al., 1996b). Maintenance of gut architecture after weaning seems a prerequisite for high food intake and good growth, particularly for pigs weaned early in life at two to three weeks of age. So feeding liquid milk or milk replacer at weaning is perhaps the best way of minimising the growth check. Heo et al. (1999) almost eliminated the growth check by feeding a liquid milk replacer at weaning, and they achieved a growth rate of 470 g/d for the first 7 days after weaning pigs at 14. The pigs were held at 24°C in this experiment. When pigs were kept at 17°C, and presumably cold stressed, growth was reduced to 340 g/d and, when kept at 32°C and possibly heat stressed, growth was also reduced to 360 g/d. Kim et al. (2001) have also recorded extremely high growth rates with very young pigs weaned at 11 days of age and fed diets based on whey proteins (70%), lard (12%) and plasma proteins (5%) fed either in liquid form or as a dry pellet. Pigs fed the liquid grew at 380g/d while those fed the pellets grew at 260 g/d for the first 14 days after weaning.

2.11

Does minimising the growth check have longterm benefits?

Minimising the growth check at weaning has obvious short-term benefits of faster turnover in the weaner rooms and reductions in mortality and morbidity but there are very few studies where long-term benefits for growth have been quantified. Dunshea et al. (1997a) found that skim milk fed to pigs for one week after weaning

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Williams

at 20 days of age increased liveweight by 0.6 kg compared with control animals offered a dry, conventional starter diet. By the time the pigs had reached 120 days of age the difference in weight had increased to 3 kg (59 vs 62 kg). Pluske et al. (1999) fed spray-dried bovine colostrum to pigs and, 14 days after weaning at 4 weeks of age, the weight advantage of the pigs fed colostrum was 1.1 kg. This growth difference was still evident at slaughter at 83 kg. Kim et al. (2001) induced a difference in weight of 1.6 kg 14 days after weaning by feeding pigs a milk replacer diet in a liquid rather than a dry pellet. This difference doubled to 3.3 kg by the time the pigs reached 150 days of age and about 110 kg. So it seems from the few reports available that stimulation of growth in the immediate post-weaning period by highquality animal proteins has a small but beneficial effect on long-term growth. There has been some suggestion that stimulating post-weaning growth and minimising the check is unnecessary because pigs will display compensatory growth and catch up to their contemporaries who have suffered less of a check. Whang et al. (2000) addressed this by comparing a 3-phase starter regimen containing highquality animal products (skim milk, whey, and plasma protein) with a traditional starter diet based on corn and soybean with minimal fish meal. Pigs fed animal protein gained liveweight at 175 g/d while the pigs fed the corn/soybean diet lost 38 g/d, and this gave a difference in liveweight of 1.5 kg at the end of the first week after weaning. Animal protein allowed the pigs to gain substantial amounts of body protein and keep fat losses to a minimum, while the pigs fed plant proteins could only maintain their body protein and they lost substantial amounts of fat (Table 2.3).

Table 2.3. Change in liveweight, body protein and body fat (g/d) in the first 7 days after weaning (from Whang et al., 2000). Diet

Liveweight

Protein

Fat

Animal protein Corn/soybean

175 -38

30 5

-7 -30

Despite these differences created in the first week after weaning the pigs fed the traditional starter diet compensated and reached the same mass of body protein (15.4 vs 15.1 kg) as the pigs fed animal protein at 152 days of age although they did not compensate completely in body fat (25.5 vs 28.1 kg) and were leaner. If body protein had been lost in the first week after weaning rather than just maintained it would be interesting to know whether there would have been complete compensation. Young pigs, particularly after weaning, protect their body protein and appear to preferentially metabolise fat in times of nutritional shortage. Whittemore et al. (1978) showed that for the first week after weaning piglets lost

30

Weaning the pig

Growth of the weaned pig

a modest 6 g/d of bodyweight and this consisted of a large loss of fat (46 g/d) and gains in both protein (4 g/d) and water (36 g/d). They suggested that young pigs probably needed to grow at rates of about 200 g/d before they started to accumulate body fat. Allowing pigs to exhibit compensatory growth might be one way reducing the cost of starter diets and increasing the efficiency of growth.

2.12

Conclusions

It is suggested that growth and its driver, food intake, are pre-programmed and that bigger animals at birth are bigger at weaning and bigger at maturity. The consequence of this is that a larger animal will grow faster than a smaller animal at any stage of its life. Hence pigs that are heavier at weaning will grow faster than lighter ones and any weight differences at weaning will be magnified during postweaning growth. It seems from most of the evidence that stimulating growth of piglets during lactation to reach a greater weaning weight is rarely rewarded by a higher post-weaning growth. Simple observations on growth rate in the first week after weaning, like the genetically programmed weight at weaning, suggest that this is also an important determinant of post-weaning growth, that is, the more rapid the growth the faster the pig reaches market weight. The normal check in growth that follows weaning can be minimised and reduced to only a few days by feeding high-quality diets based on animal proteins. This circumvents the need for the normal mechanisms of compensatory growth that would otherwise operate and allow animals to catch up to their normal growth path.

References Armstrong, W.D. and A.J. Clawson, 1980. Nutrition and management of early weaned pigs: effects of increased nutrient concentrations and/or supplemental liquid feeding. Journal of Animal Science 50, 377-384. Black, J.L., 1995. Modelling energy metabolism in the pig - critical evaluation of a simple reference model. In: P.J. Moughan, M.W.A. Verstegen, and M.I. Visser-Reneveld (editors), Modelling Growth in the Pig. EAAP Publication No. 78. Wageningen Pers, Wageningen, The Netherlands, pp. 87102. Brown, L.J., G.L. Krebs and B.P. Mullan, 1999. Feeding of liquid milk supplements to pigs preand post-weaning improves live weight gain. In: P.D. Cranwell (editor), Manipulating Pig Production VII. Australasian Pig Science Association, Werribee, Victoria, pp. 273. Campbell, R.G., 1989. The nutritional management of weaner pigs. In: J.L. Barnett and D.P. Hennesy (editors), Manipulating Pig Production II. Australasian Pig Science Association: Werribee, pp. 170-175. Campbell, R.G. and A.C. Dunkin, 1982. The effect of birth weight on the estimated milk intake, growth and body composition of sow-reared piglets. Animal Production 335, 193-197.

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Harrell, R.J., M.J. Thomas and R.D. Boyd, 1993. Limitations of sow milk yield on baby pig growth. In: Proceedings of the 1993 Cornell Nutrition Conference for Feed Manufacturers. New York State College of Agriculture and Life Sciences, Cornell University, Ithaca, pp. 156-164. Heo, K.N., J. Odle, W. Oliver, J.H. Kim, I.K. Han and E. Jones, 1999. Effects of milk replacer and ambient temperature on growth performance of 14-day-old early-weaned pigs. AsianAustralasian Journal of Animal Science 12, 908-913. Hodge, R.M.W., 1974. Efficiency of food conversion and body composition of the preruminant lamb and the young pig. British Journal of Nutrition 32, 113-126. Hogg, B.W., 1991. Compensatory growth in ruminants. In: A.M. Pearson and T.D. Dutson (editors), Growth Regulation in Farm Animals. Advances in Meat Research 7. Elsevier Applied Science, London and New York, pp. 104. Kim, J.H., K.N. Heo, J. Odle, I.K. Han and R.J. Harrell, 2001. Liquid diets accelerate the growth of early-weaned pigs and the effects are maintained to market weight. Journal of Animal Science 79, 427-434. King, M.R., P.C.H. Morel, E.A.C. James, W.H. Hendriks, J.R. Pluske, R. Skilton and G. Skilton, 2001. Inclusion of colostrum powder and bovine plasma in starter diets increases voluntary feed intake. In: P.D. Cranwell (editor), Manipulating Pig Production VIII. Australasian Pig Science Association: Werribee, pp. 213. Koong, L.J., J.A. Nienaber and H.J. Mersmann, 1983. Effects of plane of nutrition on organ size and fasting heat production in genetically obese and lean pigs. Journal of Nutrition 113, 16261631. Lawrence, T.L.J. and V.R. Fowler, 1997. Growth of Farm Animals. CAB International, Wallingford Oxon. Lawlor, P.G., P.B. Lynch, P.J. Caffrey and J.V. O’Doherty, 2002. Effect of pre- and post-weaning management on subsequent pig performance to slaughter and carcass quality. Animal Science 75, 245-256. Lucas, I.A.M. and G.A. Lodge, 1961. The Nutrition of the Young Pig - A Review. Commonwealth Agricultural Bureaux, Slough, UK. Lui, H., L.H. Kim, K.J. Touchette, M.D. Newcomb and G.L. Allee, 2001. The effect of spray dried plasma, lactose and soybean protein sources on the performance of weaned pigs. AsianAustralasian Journal of Animal Science 14, 1290-1298. Mahan, D.C. and A.J. Lepine, 1991. Effect of pig weaning weight and associated nursery feeding programs on subsequent performance to 105 kg body weight. Journal of Animal Science 69, 1370-1378. Mavromichalis, I., T.M. Parr, V.M. Gabert and D.H. Baker, 2001. True ileal digestibility of amino acids in sow’s milk for 17-day-old pigs. Journal of Animal Science 79, 707-713. McBride, C., J.W. James and G.S. Wyeth, 1965. Social behaviour of domestic animals. VII. Variation in weaning weight in pigs. Animal Production 7, 67-74. McCance, R.A., 1960. Severe undernutrition in growing and adult animals. 1. Production and general effects. British Journal of Nutrition 14, 59-73. McCauley, I., E.A. Nugent, D.E. Bauman and F.R. Dunshea, 1999. Insulin infusion and high protein diets can increase sow milk yield and piglet growth. In: P.D. Cranwell (editor), Manipulating Pig Production VII. Australasian Pig Science Association: Werribee, pp. 175.

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McConnell, J.C., J.C. Eargle and R.C. Waldorf, 1987. Effects of weaning weight, co-mingling, group size and room temperature on pig performance. Journal of Animal Science 65, 1202-1206. McCracken, K.J. and D. Kelly, 1993. Development of digestive function and nutrition/disease interactions in the weaned pig. In: D. J. Farrell (editor), Recent Advances in Animal Nutrition in Australia 1993. Department of Biochemistry, Microbiology and nutrition, University of New England, Armidale, Australia, pp. 182-192. Miller, H.M., P. Toplis and R.D. Slade, 1999. Weaning weight and daily live weight gain in the week after weaning predict piglet performance. In: P.D. Cranwell (editor), Manipulating Pig Production VII. Australasian Pig Science Association: Werribee, pp. 130. Morgan, J.H.L., 1972. Effect of plane of nutrition in early life on subsequent live-weight gain, carcass and muscle characteristics, and eating quality of meat in cattle. Journal of Agricultural Science 78, 417-423. O’Donovan, P.B., 1984. Compensatory growth in cattle and sheep. Nutrition Abstracts and Reviews (Series B) Livestock Feeds and Feeding 54, 389-410. Pluske, J.R., G. Pearson, P.C.H. Morel, M.R. King, G. Skilton and R. Skilton, 1999. A bovine colostrum product in a weaner diet increases growth and reduces days to slaughter. In: P.D. Cranwell (editor), Manipulating Pig Production VII. Australasian Pig Science Association: Werribee, pp. 256. Pluske, J.R., I.H. Williams and F.X. Aherne, 1995. Nutrition of the neonatal pig. In: M.A. Varley (editor), The Neonatal Pig Development and Survival. CAB International, Wallingford, Oxon., pp. 187-235. Pluske, J.R. and I.H. Williams, 1996. Split weaning increases the growth of light piglets during lactation. Australian Journal of Agricultural Research 47, 513-523. Pluske, J.R., I.H. Williams and F.X. Aherne, 1996a. Maintenance of villous height and crypt depth in piglets by providing continuous nutrition after weaning. Animal Science 62, 131-144. Pluske, J.R., I.H. Williams and F.X. Aherne, 1996b. Villous height and crypt depth in piglets in response to increases in the intake of cow’s milk after weaning. Animal Science 62, 145-158. Pollmann, D.S., 1993. Effects of nursery feeding programs on subsequent grower-finisher pig performance. In: J. Martin (editor), Proceedings of the Fourteenth Western Nutrition Conference. University of Alberta, Edmonton, pp. 243-254. Reale, T.A., 1987. Supplemental liquid diets and feed flavours for young pigs. Master of Agricultural Science thesis: University of Melbourne. Ryan, W.J., 1990. Compensatory growth in cattle and sheep. Nutrition Abstracts and Reviews (Series B) Livestock Feeds and Feeding 60, 653-664. Tokach, M.D., R.D. Goodband, J.L. Nelssen and D.R. Keesecker, 1992. Influence of weaning weight and growth during the first week postweaning on subsequent pig performance. In: Proceedings of the American Association of Swine Practitioners University of Minnesota, pp. 409. Toplis, P., P.J. Blanchard and H.M. Miller, 1999. Creep feed offered as a gruel prior to weaning enhances performance of weaned piglets. In: P.D. Cranwell (editor), Manipulating Pig Production VII. Australasian Pig Science Association: Werribee, pp. 129. Whang, K.Y., F.K. McKeith, S.W. Kim and R.A. Easter, 2000. Effect of starter feeding program on growth performance and gains of body components from weaning to market weight in swine. Journal of Animal Science 78, 2885-2895.

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Growth of the weaned pig

Whittemore, C.T. and D.M. Green, 2001. Growth of the young weaned pig. In: M.A. Varley and J. Wiseman (editors), The weaner pig: Nutrition and Management. CAB International, pp. 115. Whittemore, C.T., A. Aumaitre and I.H. Williams, 1978. Growth and body composition in young weaned pigs. Journal of Agricultural Science (Cambridge) 91, 681-692. Widdowson, E.M., and D. Lister, 1991. Nutritional control of growth. In: A.M. Pearson and T.D. Dutson (editors), Growth Regulation in Farm Animals. Advances in Meat Research 7. Elsevier Applied Science, London and New York, pp. 67-101. Williams, I.H., 1976. Nutrition of the young pig in relation to body composition. PhD thesis, University of Melbourne. Williams, I.H., 1995. Sow’s milk as a major nutrient source before weaning. In: D.P. Hennessy and P.D. Cranwell (editors), Manipulating Pig production V. Australasian Pig Science Association: Werribee, pp. 107-113. Wolter, B.F. and M. Ellis, 2001. The effects of weaning weight and rate of growth immediately after weaning on subsequent pig growth performance and carcass characteristics. Canadian Journal of Animal Science 81, 361-369. Wolter, B.F., M. Ellis, B.P. Corrigan and J.M. DeBecker, 2002. The effect of birth weight and feeding of supplemental milk replacer to piglets during lactation on preweaning and postweaning growth performance and carcass characteristics. Journal of Animal Science 80, 301-308.

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3

Nutritional management of the pig in preparation for weaning R.H. King and J.R. Pluske

3.1

Introduction

The average weaning age in many of the major pork-producing countries in the world has declined progressively over the last 20 years owing to the continued pressure on the pig industry to improve the efficiency of pork production. Reducing the age at weaning to 18 to 24 days of age, which is the average weaning age in many countries, has the potential of improving efficiency. This is because the farrowing interval of sows is reduced (thereby increasing the number of pigs produced per sow per year) and the risk of disease transfer between sows and piglets (segregated early weaning systems) is reduced, thereby increasing growth rate and efficiency in subsequent growth phases. Removing piglets from the sow at an earlier age also provides opportunities to exploit the enormous growth potential of the young pig, because it is well established that the sucking piglet, because of limitations on sow milk yield and milk composition, does not grow to its full genetic potential. Weaning can be regarded as one of the most critical periods in the modern-day pork production cycle because it represents a period of adaptation and stress in response to the simultaneous stressors imposed on pigs at weaning. Pigs are removed from their mothers, usually mixed with others and moved to a different environment, and are fed an alien diet that is presented and offered very differently to sows’ milk that was received during lactation. Consequently, pigs usually suffer a post-weaning “growth check” for 7-14 days following weaning that is characterised by low and variable feed intake, poor and variable growth rate, increased maintenance requirements and increased susceptibility to enteric pathogens to cause diseases such as post-weaning colibacillosis. There is now realisation that the weight of the pig at weaning, and indeed at birth, bears a strong, positive relationship to subsequent growth and weight at some point in the future. A key performance target in pork production should be maximisation of weaning weight, because this will have an overall influence on subsequent growth in the growing and finishing stages. Also of importance is the variation in weaning weight, and weight in the nursery, grower and finisher phases. Increases in litter size cause an increase in variation in piglet size, and this includes more piglets in the less viable category. Limiting weight variation is important for improving a facility’s utilisation of all-in, all-out systems, and this needs to be balanced against management strategies aimed at improving piglet growth rate during lactation.

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The influences of sow-and piglet-related characteristics to milk production by the sow have been the subject of many reviews (eg, Hartmann and Holmes, 1989; Pettigrew, 1995; Williams, 1995; Le Dividich, 1999), and will not be discussed in this chapter. To help satisfy the requirements of the piglet to achieve maximum growth potential and maximum weaning weight, nutrients additional to those supplied by sow’s milk are often provided to the sucking pig. In addition, the supply of additional nutrients may also prepare the digestive system of the sucking pigs to cereal-based solid diets after weaning. The purpose of this chapter is to discuss some of the management options available before weaning to ensure that the liveweight of the pig, and perhaps the efficiency of the gastrointestinal tract, is maximised/optimised at weaning so that the stressors imposed around weaning will have less impact upon overall efficiency in the production system.

3.2

The importance of weaning weight to subsequent growth

The weight of piglets at weaning is one of the most critical factors determining the subsequent growth performance of pigs, and has been reviewed in chapter 14 (Le Dividich et al., 2003). Research by Campbell (1990), for example, showed a strong inverse relationship between weight of pigs at weaning at 28 days of age (W) and the length of time taken to grow to 20 kg live weight (T), as follows: T = 52.1 (± 1.69) - 3.39 (± 0.224) W (R2 = 0.85, P < 0.001). Based upon this equation, pigs that are 1 kg heavier at weaning reach 20 kg over 3 days earlier. Other research using younger pigs (eg, Dritz et al. 1996; Miller et al. 1999) confirms this general relationship. Heavier pigs at weaning seem to continue their weaning weight advantage to slaughter weight (Mahan and Lepine, 1991; Le Dividich et al. 2003), and the age at slaughter could be reduced even further by at least 10 days for a pig that is 1 kg heavier at weaning (Cole and Close, 2001). Because of the positive relationship between weaning weight and post-weaning growth performance, any factor that increases piglet weight at weaning should reduce slaughter age. Interestingly, data from both commercial and research trials shows consistently that there is a highly significant (30 to 60% of the total variance) effect of litter from which the piglet is derived on weaning weight and subsequent post-weaning performance (Slade and Miller, 1999). This indicates that one or more factors that occurs prior to weaning is/are having a major influence on both weaning weight and subsequent growth rate, with both pre-natal and post-natal components having an effect. Rooke et al. (1998) reported that the relative importance of these events

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was 3:1 in favour of the pre-natal effects, begging the question of just where exactly does one begin to investigate the phenomenon of variation in pig weights. Some authors (Bate, 1991; Braastad, 1998) have presented evidence of in utero effects on subsequent post-natal behaviour. Nevertheless, maximisation of weaning weight should remain a goal in pig production because of its relationship to the number of days it takes a given pig to reach slaughter weight.

3.3

Nutrient intake before weaning

The piglet places an enormous reliance on the sow for its nutritional needs before weaning, first consuming colostrum in the first 24-36 hours after parturition and then consuming milk at regular intervals during the day and night until weaning (Pluske and Dong, 1998). The intake of an ‘adequate’ amount of colostrum before closure of the small intestine to immunoglobulins is of crucial importance to both the subsequent survival and performance of the young pig (Le Dividich and Noblet, 1981; Varley, 1992). Coalson and Lecce (1971) considered an intake of 40-60 g colostrum was necessary for piglets to have normal serum immunoglobulin concentrations. The provision of colostrum to weaker piglets, or to litters where the sow is suffering agalactia, is generally used as a key management technique to increase survival rates, increase weaning weight, and possibly reduce the variation in weaning weight. Alternatively, practices such as split weaning immediately after farrowing offer potential to allow a more equitable transfer of colostral immunoglobulins across the spectrum of weights within a litter (Donovan and Dritz, 1997). Many studies espouse the benefits of colostrum for gut development, as an energy source for thermoregulation of the newborn piglet, a substrate for protein synthesis, and as a passive supply of protection against enteric pathogens. Collectively, these functions are important in establishing the pig during lactation and, ultimately, after weaning. 3.3.1

Supplying creep food in lactation

Amongst the many pre-weaning influences that can affect the growth and survival of pigs after weaning, most attention has been directed towards the nutrition of the young pig. A plethora of studies have examined, and reviewed, the effects of creep feeding (ie, offering a solid diet) during lactation on weaning weight and performance thereafter (eg, Pluske et al., 1995). This is based largely on the premise that offering solid feed before weaning will familiarise, both behaviourally and physiologically, the young pig to the changes imposed on it simultaneously at weaning. Traditionally, the sucking piglet has been supplied with creep food for two main reasons. First, creep food supplies supplemental nutrients that are required to maintain satisfactory growth rates and achieve heavier weaning weights. Second, the consumption of creep food is believed to prepare the digestive system of the

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piglet for digestion of complex carbohydrates and protein that will be supplied as the sole source of nutrients after weaning. However, some research, such as that of Chapple et al. (1989), found that the variation in amylolytic activity in the pancreas of piglets was more a function of sow (litter of origin) than of the intake of solid feed during lactation and immediately after weaning. Similarly, it has been reported that pepsin and maltase activities could not be related to weaning weight or creep feeding time (Lindemann et al. 1986; de Passille et al. 1989). 3.3.2

Dry creep feed intake

Evidence to support the notion that supplying pigs with dry creep food during lactation will improve pre-weaning growth performance is equivocal. Pluske et al. (1995) reviewed a large number of studies presented in the literature and found an enormous variation in feed intake of creep-fed piglets, with the contribution of creep feed to daily energy intake prior to weaning at 21-35 days of age ranging from 1.2 to 17.4%. Thus the data from the literature demonstrate that intake of dry creep food during lactation is generally small and variable and unlikely to significantly influence weaning weight, particularly in piglets weaned at 3 weeks of age or younger. Furthermore, growth rate in the immediate period following weaning is often poorly related to pre-weaning creep food intake (Barnett et al. 1989, Pajor et al. 1991; Fraser et al. 1994), suggesting that causal links between creep feeding and weight gain after weaning remain to be demonstrated. Two of the reasons for this are because creep feed consumption varies so much within litters and between litters. Fraser et al. (1994), for example, estimated that creep feed intake (associated with creep feeding behaviour) accounted for only 1-4% of the variation in liveweight gain in piglets in their first 14 days following a 28-day weaning, even though there were significant litter effects on the intake of dry feed during lactation. Nevertheless, some pork producers, especially those weaning later than 21 days of age, often offer high-quality expensive creep diets to sucking pigs, despite minimal responses in pre-weaning growth rate, to assist the adaptation to starter diets as the sole source of nutrients immediately after weaning. In some European countries such as Sweden and Denmark where weaning age is now 28 days of age or greater, and the use of growth-promoting antibiotics and antimicrobial agents such as zinc oxide are banned or strictly regulated, the importance of enhancing the intake of solid feed before weaning is receiving renewed attention. This is to take advantage of both a heavier weaning weight and to modulate the gastrointestinal tract, especially the microflora, to the dietary challenges after weaning. Numerous recent studies, such as those reported by Toplis et al. (1999) and Blanchard et al. (2000), show that offering creep feed as a gruel/slurry (1:2 meal to water) may enhance the consumption of dry matter before weaning.

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3.3.3

Liquid diets to enhance feed intake

In contrast to the equivocal results reported with dry creep feed supplementation (Pluske et al. 1995), providing sucking piglets with liquid diets would appear to offer more potential to provide a significant boost to pre-weaning growth rate and weaning weight (Reale, 1987; Azain et al. 1996), and also performance after weaning (see Odle and Harrell, 1998, for review). Reale (1987) offered cows’ whole milk to piglets from 10.00 h each day, adding fresh milk every two hours until 23.00 h, from day 7 to day 28 of lactation. Growth was stimulated by 151 g/day (71%) in the fourth week of lactation and, from days 7 to 28, by 87 g/day, an amount that increased weaning weight by 1.8 kg in comparison to controls that were offered a dry creep feed. Similarly, King et al. (1998) found that piglets offered cows’ liquid milk from day five of lactation were 1.6 kg heavier at weaning at 28 days of age than piglets which received no supplemental nutrients. In addition, piglets appeared to still prefer milk from the sow, as the supply of supplemental milk did not reduce the amount of milk that the piglet obtained directly from the sow. The results of a number of studies where sucking piglets were offered milk liquid diets are shown in Table 3.1. Significant increases in the intakes of nutrients have been observed when sucking pigs have been offered liquid milk diets compared to dry creep intakes (Table 3.1). As a result, pre-weaning growth rates are increased by 11 to 35% (Table 3.1). These results demonstrate the potential benefit of additional nutrients on weaning weight and a clear benefit of supplemental milk replacer to increase weaning weight. Although pre-weaning growth rates were increased to almost 300 g/day, there is still enormous potential for these piglets to grow faster up until weaning at 21-28 days of age (Hodge, 1974) if further nutrients are consumed. The use of a liquid milk replacer not only before weaning, but the supply of liquid diets during the immediate period after weaning, can further reduce the growth check and improve the subsequent growth performance of pigs. Kim et a1. (2001) showed that feeding a starter diet as a liquid rather than in the dry form for the first 14 days after weaning significantly increased weight at 28 days of age by 1.62 kg. In this study, pigs were weaned at 14 days of age. This growth advantage was maintained to market weight with no evidence of compensatory gain in the dryfed control pigs. However, and in contrast, Lawlor et al. (2002) showed no positive effects whatsoever on post-weaning gain when a number of dietary interventions based on liquid feeding were implemented after weaning. Dunshea et al. (1997) attempted to alleviate the post-weaning growth check by providing extra milk around the time of weaning. Pigs provided with liquid milk replacer, in addition to access to dry starter feed, gained 1.2 kg during the first week after weaning whereas pigs that received only dry starter feed gained 0.4 kg in the

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Table 3.1. Consumption of liquid milk replacer by piglets during lactation and consequent growth response. Reference

Treatment duration of feeding (days)

Azain et al. (1996) Cool season No replacer 21 Replacer 21 Warm season No replacer 21 Replacer 21 King et al. (1998) No replacer 24 Replacer 24 Dunshea et al. (1997b) No replacer 10 Replacer 10 Campbell (1990) No replacer 10 Replacer 10 Pluske et al. (1995)1 15.3 1Means

Lactation length (days)

Average Pre-weaning Increase in supplemental growth rate growth rate intake over (g/day) (%) lactation (g DM/pig/day)

21 21

20.9

222 247

11

21 21

66.2

166 224

35

28 28

58.5

238 297

25

20 20

48.5

223 291

30

28 28 28.1

29.3 11.8

214 264 213.6

23

figures for dry creep intake in studies reviewed by Pluske et al. (1995).

first week after weaning (Dunshea et al. 1997). Supply of a liquid milk replacer to piglets both prior to weaning and in the first week after weaning had an additive effect; pigs that received liquid milk replacer before and after weaning were 10% heavier at 120 days of age than pigs that were suckled by the sow only and weaned onto dry starter feed (Dunshea et al. 1997). Much of this improvement was due to the extra nutrient intake from supplemental milk replacer prior to and immediately after weaning. The development of liquid feeds and feeding systems offers the potential to markedly improve the growth performance of piglets both before weaning and during the immediate period after weaning.

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3.3.4

The effects of gender on nutrient intake of neonatal pigs

An interesting observation by King et al. (1998) was that female piglets grew faster than their male counterparts prior to weaning when litters were offered supplemental milk. This was most likely related to greater nutrient intake in the female pigs. Similar observations of greater growth rates amongst female piglets have been made in the immediate post-weaning period when pigs were offered either liquid diets (Dunshea et al. 1997) or dry diets (Bruininx et al. 2001; Dunshea et al. 2001). In a retrospective analysis of 58 studies conducted at the University of Kentucky, Cromwell et al. (1996) showed that gilts grew more rapidly over the first few weeks after weaning. Thus, there does appear to be more sexual dimorphism in young pigs, and this is often manifested in the immediate post-weaning period if nutrient intake is high or when supplemental nutrients are provided before weaning.

3.4

The composition of diets offered during lactation

During the first two or three weeks of life, the piglet’s digestive tract is best suited to digest lactose, fat and the milk proteins, casein and whey (Pluske and Dong, 1998). The digestive enzymes necessary for the digestion of starch, sugar and nonmilk proteins are present at relatively low levels. Therefore, dry and liquid creep feeds must be palatable, concentrated and contain ingredients compatible with the digestive system of the young sucking pig. Complete creep diets containing cooked or flaked cereals, oils, various milk products and other highly digestible feedstuffs are often used to stimulate food intake of piglets prior to weaning to achieve heavier weaning weights and to prepare the piglet for weaning. Fraser et al. (1994) compared a standard creep diet based primarily on corn and soybean meal with a complex commercial creep diet containing no soybean meal, and found that piglets consumed more of the complex creep diet and were 0.3 kg heavier at weaning at four weeks of age. However, Fraser et al. (1994) found that these piglets only tended to gain more weight in the week before, and the two weeks following, weaning. In other studies with 4- or 5-week weaning, performance of pigs after weaning that have been raised with or without creep feeding has generally shown small or negligible effects (Okai et al. 1976; Barnett et al. 1989; Tokach et al. 1990), although English et al. (1980) showed large effects of pre-weaning creep feed intake on post-weaning performance. One of the contentious issues associated with creep feeding is to do with the inclusion of antigenic compounds, such as glycinin and β-conglycinin from soybean products, in the diet. It has been hypothesised by some researchers that a short-term exposure to creep feed and low feed consumption may sensitise the

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pig to antigens in certain feed ingredients, eg, soybean meal, beans, such that exposure of the sensitised pigs to an increased intake of the same dietary antigens after weaning gives rise to a hypersensitivity response. This, in turn, is believed to cause post-weaning diarrhoea (eg, Miller et al. 1984; Newby et al. 1985). It is outside the scope of this chapter to discuss this issue in detail, however numerous authors have subsequently failed to endorse this hypothesis. For example, Barnett et al. (1989) examined the effects of feeding a common corn-soybean meal-whey creepdiet on the immune response and post-weaning performance of pigs weaned at 4 weeks of age. Although creep-fed pigs tended to have higher immune responses and slightly more severe scouring, both pre-weaning and post-weaning growth performance of piglets were unaffected by the provision of the creep diet containing soybean meal. Similarly, Kelly et al. (1990) found that offering creep feed before weaning failed to affect the prevalence or severity of diarrhoea induced experimentally by exposure to an enteropathogenic strain of Escherichia coli, and Sarimento et al. (1990) reported that restricted feeding of a creep diet failed to affect the incidence of induced diarrhoea and did not induce any morphological changes characteristic of an allergic reaction in the small intestine. McCracken et al. (1999) postulated that any effects of soybean antigens on the structure and function of the small intestine might occur secondarily to the period of starvation that occurs after weaning. The reader is directed towards reviews by Dreaù and Lallès (1999) and Bailey et al. (2001) for further information on this topic. Nevertheless, withholding soybean meal from the diet of a young pig after weaning, to allow for the negative effects on gut structure and function that occur post-weaning, and then re-including it two weeks after weaning, causes the same histological and performance setback as if the antigens were present in the diet all along (Dritz et al., 1996). In this regard, commercial practice dictates that soybean meal is included in diets for young pigs despite the documented physiological, immunological and morphological changes that occur. 3.4.1

Dietary formulation of creep diets

There is a dearth of data relating to the protein and amino acid requirements of pigs before 3-4 weeks of age (ARC, 1981). Data from milk-fed pigs have provided estimates of 0.87 to 0.95 g lysine/MJ gross energy as the nutrient requirements for pigs averaging 4 kg live weight (Williams, 1976, Auldist et al. 1997). There is little data on which to base nutrient requirements for solid diets for weaned pigs. NRC (1998) estimated the minimum dietary requirements of weaned pigs from 3 to 5 kg were 14.2 MJ DE/kg, 18.3g CP/MJ DE and 1.06 g lysine/MJ DE. Similarly, ARC (1981) provided tentative recommendations of 16 g CP/MJ DE and 1.12 g lysine/MJ DE for the nutrient requirements of weaned pigs between birth and three weeks of age.

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These dietary requirements are often used as a guide to develop diet specifications for supplemental creep diets. However, the emphasis on dietary formulation of creep diets is more specifically on the choice of palatable and highly digestible protein and energy sources that promote high feed intake rather than meeting the nutrient specifications on a least cost basis. Examples of the composition of creep diets suitable for suckling pigs up until 3-4 weeks of age are shown in Table 3.2 (A.C. Edwards, personal communication). 3.4.2

Use of flavours in creep/starter diets

Attempts have been made to increase weaning weight and reduce the growth check of pigs after weaning by using various sweeteners and aromatic compounds to increase feed consumption, particularly during the first week or two after weaning (Campbell, 1976; Kornegay, 1977). Gatel and Guion (1990) found that diets containing monosodium glutamate significantly increased creep food intake, although the increase was not sufficient to improve weaning weight. However, Clarke and Batterham (1989) found that creep food intake was low and unaffected by the supplementation of a creep diet with monosodium glutamate. Campbell (1976) found that incorporation of a feed flavour into a creep diet failed to increase creep food consumption or weaning weight. However, Campbell (1976) also found that pigs that had been weaned from sows given a flavoured diet and had also been given a flavoured diet after weaning consumed more feed, particularly in the first two weeks after weaning. King (1979) later confirmed this interaction for feed intake after weaning, and also demonstrated that when the flavour was added to the sow diet, it was detected in milk samples collected from those sows. Madsen (1977) indicated that feed preferences could be transferred from lactating sows to their litter by incorporating a non-metabolisable substance into both the lactating sow diet and the diet offered to piglets after weaning. Any positive effects of feed flavours observed in young pigs are more likely to be due to this transference of feed preferences via flavours incorporated in sows milk or masking unacceptable tastes to improve the palatability in the creep diet. 3.4.3

Presentation of the creep diet

One of the most important factors stimulating piglets to eat creep feed is the freshness of the feed. Piglets should be offered small amounts of feed, at least on a daily basis, as not only does this ensure that the feed is fresh, but the frequent arrival of fresh feed stimulates the inherent curiosity of the piglets, thereby encouraging consumption of creep feed (Pajor et al. 1991). Creep feed is usually offered to pigs when they are at least one week of age because they usually show no interest in supplemental dry feed during the first week of

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Table 3.2. Composition of creep diets (g/ kg air dry diet)1. Weaning age

2 weeks

3-4 weeks

Duration of Feeding

2-4 weeks of age

3-6 weeks of age

Diet

1

2

3

4

5

6

Wheat Dehulled oats Extruded corn Soyabean meal Sugar Full fat soyabean meal Meat and bone meal Fish Meal Blood Meal Skim milk powder Whey powder

390 30 30 60 30 50 15 200 150

464 30 40 25 50 20 200 150

352 35 30 119 30 60 200 150

592 80 20 45 55 70 20 100

616 80 20 45 50 60 20 100

579 80 20 79 42 50 20 100

Vegetable oil Dicalcium phosphate Limestone Lysine -HCL D, L-methionine Threonine Tryptophan Mineral/ vitamin premix Salt Digestible energy (MJ/ kg) Crude protein Lysine Methionine Threonine Calcium Phosphorus

38 2 0.5 1.0 0.7 0.2 2.0 -

15 2 0.6 0.6 0.8 0.2 2.0 -

20 0.2 1.0 0.4 0.2 2.0 -

10 2.6 0.8 1.0 0.2 2.0 1.0

2 2 0.6 0.9 0.1 2.0 1.0

5 1.9 1.0 0.4 0.1 2.0 2.0

16.0 233 15.9 5.5 10.1 9.4 7.9

16.1 225 16.1 5.1 10.2 9.1 7.8

16.1 236 16.2 5.8 10.2 9.1 7.6

15.3 229 15.0 4.8 9.5 9.2 7.7

15.6 228 15.3 4.6 9.7 9.4 7.6

15.6 230 15.3 4.9 9.7 9.1 7.3

1Use

of cooked cereals and extruded feed ingredients may improve digestibility. In addition, use of supplements such as organic acids, enzymes and flavours might also improve digestibility, feed intake and (or) piglet health.

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life. Initially, feed should be offered on the floor of the farrowing crate or in shallow trays (English et al. 1977). When the litter is obviously consuming the feed, a small feeder allowing room for several piglets to feed at the same time can be used to supply the creep diet to the suckling pigs. Appleby et al. (1991) observed that although provision of fresh food daily compared to three times per day had no effect on creep food consumption, increasing the number of feeding spaces enhanced overall creep intake in both the third and fourth week of lactation. It seems that provision of sufficient feeder space to allow several pigs to feed at once may assist imitation of feeding behaviour, which is an important factor in the establishment of feeding behaviour in pigs (Appleby et al. 1991).

3.5

Water for suckling pigs

Water intake by pigs is often taken for granted but is one of the more critical nutrients, particularly for the sucking pig. Apart from water required to support the growth of muscle tissue and to clear wastes from the body, young pigs require water to replace that lost by evaporation and respiration. Under most circumstances the amount of water consumed via sows’ milk would be more than enough to satisfy the requirements for tissue deposition and evaporative moisture loss (Fraser et al. 1993). Supplemental water is often available to piglets in farrowing crates, but B. Jennings (personal communication) showed that deprivation of supplemental water to suckling piglets had no significant effect on their growth performance to weaning or in the immediate post-weaning period. Water availability is likely to be only important for an underfed piglet in a very warm environment or in a piglet suffering diarrhoea (Fraser et al. 1993).

3.6

Conclusions

The first weeks after weaning are regarded as some of the most crucial in the pork production cycle because they represent a period of adaptation and stress on the young pig. There are nutritional strategies that can be implemented before, and around, weaning to reduce the amount of stress and severity of the growth check in the immediate post-weaning period. Adequate intake of supplemental nutrients before weaning can assist in preparing the digestive system of the pig for the digestion of complex carbohydrates and proteins, and promote greater weight gain and weaning weight. Responses to this strategy, however, tend to be variable and depend to a degree on the weaning age. Supplementation of piglets before and around weaning with liquid milk diets offers the greatest potential to stimulate pre-weaning growth rate and to eliminate the post-weaning check than usually occurs in commercial pork production. The development of liquid feeds and feeding systems offers the potential to prepare the piglet for the weaning process and markedly improve the performance of the young pig.

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References Agricultural Research Council, 1981. The Nutrient Requirements of Pigs. Commonwealth Agricultural Bureau, Slough, UK. Appleby M.C., E.A. Pajor and D. Fraser, 1991. Effects of management options on creep feeding by piglets. Animal Production 53, 361-366. Auldist, D.E., F.L. Stevenson, M.G. Kerr, P. Eason and R.H. King, 1997. Lysine requirements of pigs from 2 to 7kg live weight. Animal Science 65, 501-507. Azain, M.J., T. Tomkins, J.S. Sowinski, R.A. Arentson and D.E. Jewell, 1996. Effect of supplemental pig milk replacer on litter performance: Seasonal variation in response. Journal of Animal Science 74, 2195-2202. Bailey, M., M.A. Vega-Lopez, H.-J. Rothkötter, K. Haverson, P.W. Bland, B.G. Miller and C.R. Stokes, 2001. Enteric immunity and gut health. In: M.A. Varley and J. Wiseman (editors), The Weaner Pig Nutrition and Management. CABBI Publishing, Wallingford, UK, pp. 207-222. Barnett, K.L., E.T. Kornegay, C.R. Risley, M.D. Lindemann and C.R. Schurig, 1989. Characterisation of creep feed consumption and its subsequent effects on immune response, scouring index and performance of weaning pigs. Journal of Animal Science 67, 2698-2708. Bate, L.A., 1991. Modifications in the aggressive and ingestive behaviour of the neonatal piglet as a result of prenatal elevation of cortisol in the dam. Applied Animal Behavioural Science 30, 299-306. Blanchard, P.J., P. Toplis, L. Taylor and H.M. Miller, 2000. Liquid diets fed prior to weaning enhance performance of weaned piglets. In: Proceedings of the British Society of Animal Science, p. 119. Braastad, B.O., 1998. Effects of prenatal stress on behaviour of offspring of laboratory and farmed mammals. Applied Animal Behavioural Science 61, 159-180. Bruininx, E.M.A.M., C.M.C. van der Peet-Schwering, J.W. Schrama, P.F.G. Vereijken, P.C. Vesseur, H. Everts, L.A. den Hartog and A.C. Beynen, 2001. Individually measured feed intake characteristics and growth performance of group-housed weanling pigs. Effects of sex, initial body weight and body weight distribution within groups. Journal of Animal Science 79, 301308. Campbell, R.G. 1976. A note on the use of a feed flavour to stimulate feed intake of weaner pigs. Animal Production 23, 417-419. Campbell, R.G., 1990. The nutrition and management of pigs to 20 kg liveweight. In: Pig Rations: Assessment and Formulation, Proceedings of the Refresher Course for Veterinarians. 132. Post Graduate Committee in Veterinary Science, University of Sydney, pp 123-126. Chapple, R.P., J.A. Cuaron and R.A. Easter, 1989. Effect of glucocorticoids and limited nursing on the carbohydrate digestive capacity and growth rate of piglets. Journal of Animal Science 67, 2956-2973. Clarke, W.A. and E.S. Batterham, 1989. Monosodium glutamate as a flavour enhancer in creepweaner diets for piglets. In: J.L. Barnett and D.P. Hennsessy (editors), Manipulating Pig Production. Australasian Pig Science Association: Werribee, p.184. Coalson, J.A. and J.G. Lecce, 1973. Influence of nursing intervals on changes in serum protein (immunoglobulin) in neonatal pigs. Journal of Animal Science 36, 381-385.

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Cole, D.J.A. and W.H. Close W.H., 2001. The modern pig setting performance targets. Animal Talk 8, 3. Cromwell, G.J., R.D. Coffey, D.K. Aaron, M.D. Lindemann, J.L. Pierce, H.J. Monegue, V.M. Rupard, D.E. Cowen, M.B. Parido and T.M. Clayton, 1996. Differences in growth rate of weaning barrows and gilts. Journal of Animal Science 74 (Suppl. 1), 320. de Passille, A.M.B., G. Pelletier, J. Menard and J. Morrisset, 1989. Relationships of weight gain and behavior to digestive organ weight and enzyme activities in piglets. Journal of Animal Science 67, 2921-2929. Donovan, T.S. and S.S. Dritz, 1997. Effects of split nursing management on growth performance in nursing pigs. American Association of Swine Practitioners, 255-259. Dréau, D. and J.P. Lallès, 1999. Contribution to the study of gut hypersensitivity reactions to soybean proteins in preruminant calves and early-weaned piglets. Livestock Production Science 60, 209218. Dritz, S.S., R.D. Goodband, M.D. Tokach and J.L. Nelssen, 19996. Nutrition programs for segregated early-weaned pigs. Compendium on Continuing Education for the Practicing Veterinarian 18 (Suppl.), S222-S234. Dunshea, F.R., 2001. Sexual dimorphism in growth of sucking and growing pigs. Asian-Australasian Journal of Animal Science 14, 1610-1615. Dunshea, F.R., P.J. Eason, D.J. Kerton, L. Morrish, M.L. Cox and R.H. King, 1997. Supplemental milk around weaning can increase live weight at 120 days of age. In: P.D. Cranwell (editor), Manipulating Pig Production VI. Australasian Pig Science Association: Werribee, p.68. English, P.R., C.M. Robb and M.F.M. Dias, 1980. Evaluation of creep feeding using a highly-digestible diet for litters weaned at 4 weeks of age. Animal Production 30, 496 (Abstr.). English, P.R., W.J. Smith and A. MacLean, 1977. The sow: improving her efficiency. Farming Press, Ipswich. Fraser, D., J.F.Patience, P.A. Phillips and J.M. McLeese, 1993. Water for piglets and lactating sows: Quantity, quality and quandaries. In: D.J.A. Cole, W. Haresign and P.C. Gainsworthy (editors), Recent Developments in Pig Nutrition 2. Nottingham University Press, Loughborough, UK, pp.201-224. Fraser, D., J.J.R. Feddes and E.A. Pajor, 1994. The relationship between creep feeding behaviour of piglets and adaptation to weaning. Effect of diet quality. Canadian Journal of Animal Science 74, 1-6. Gatel, F. and P. Guion, 1990. Effect of monosodium L glutamate on diet palatability and piglet performance during suckling and weaning periods. Animal Production 50, 365-372. Hartmann, P.E. and M.A. Holmes, 1989. Sow lactation. In: J.L. Barnett and D.P. Hennessy (editors), Manipulating Pig Production VI. Australasian Pig Science Association, Werribee, Victoria, pp. 72-97. Hodge, R.W., 1974. Efficiency of food conversion and body composition of the pre-ruminant lamb and young pig. British Journal of Nutrition 32, 113-126. Kim, J.H., K.N. Heo, J. Odle, I.K. Han and R.J. Harrell, 2001. Liquid diets accelerate the growth of easily weaned pigs and the effects are maintained to market weight. Journal of Animal Science 79, 427-434.

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King, R.H., 1979. The effect of adding a feed flavour to diets of young pigs before and after weaning. Australian Journal of Experimental Agriculture and Husbandry 19, 695-697. King, R.H., J.M. Boyce and F.R. Dunshea, 1998. The effect of supplemental nutrients on the growth performance of suckling pigs. Australian Journal of Agricultural Science. 49, 1-5. Kornegay, E.T., 1977. Artificial sugar replacers whey intensifier, aromatic attractants for swine starter rations. Feedstuffs 49 (48), 24. Kelly, D., J.J. O’Brien and K.J. McCracken, 1990. Effect of creep feeding on the incidence, duration and severity of post-weaning diarrhoea in pigs. Research in Veterinary Science 49, 223-228. Lawlor, P.G., Lynch, P.B., Gardiner, G.E., Caffrey, P.J., O’Doherty, J.V., 2002. Effect of liquid feeding weaned pigs on growth performance to harvest. Journal of Animal Science 80, 1725-1735. Le Dividich, J., 1999. Neonatal and weaner pig: Management to reduce variation. In: P.D. Cranwell (editor), Manipulating Pig Production VII. Australasian Pig Science Association, Werribee, Victoria, pp. 135-156. Le Dividich, J. and J. Noblet, 1981. Colostrum intake and thermoregulation in the neonatal pig in relation to environmental temperature. Biology of the Neonate 40, 167-174. Lindemann, M.D., S.G. Cornelius, S.M. El Kandelgy, R.L. Moser and J.E. Pettigrew, 1986. Effect of age, weaning and diet on digestive enzyme levels in the piglet. Journal of Animal Science 62, 1298-1307. Madsen, F.C., 1977. Development of feed preference in young swine. Feedstuffs 49 (5), 25. Mahan, D.C. and A.J. Lepine, 1991. Effect of pig weaning weight and associated nursery feeding programs on subsequent performance to 105 kilograms body weight. Journal of Animal Science 69, 1370-1378. McCracken, B.A., M.E. Spurlock, M.A. Roos, F.A. Zuckerman and H.R. Gaskins, 1999. Weaning anorexia may contribute to local inflammation in the piglet small intestine. Journal of Nutrition 129, 613-619. Miller, B.G., A.D. Phillips, T.J. Newby, C.R. Stokes and F.J. Bourne, 1984. Immune hypersensitivity and post-weaning diarrhoea in the pig. Proceedings of the Nutrition Society 43, 116A. Miller, H.M., P. Toplis and R.D. Slade, 1999. Weaning weight and daily live weight gain in the week after weaning predict piglet performance. In: P.D. Cranwell (editor), Manipulating Pig Production VII. Australasian Pig Science Association, Werribee, Victoria, p. 130. National Research Council. 1998. Nutrient Requirements of Swine. 10th Edition. National Academy Press, Washington, DC. Newby, T.J., B.G. Miller, D,J. Hampson and F.J. Bourke, 1985. Local hypersensitivity response to dietary antigens in early weaned pigs. In: D.J.A. Cole and W. Haresign (editors), Recent Developments in Pig Nutrition. Butterworths, London. Odle, J. and R.J. Harrell, 1998. Nutritional approaches for improving neonatal piglet performance: Is there a place for liquid diets in commercial production? A review. Asian-Australasian Journal of Animal Science 11, 774-780. Okai, D.B., F.X. Aherne and R.T. Hardin, 1976. Effects of creep and starter composition on feed intake and performance of young pigs. Canadian Journal of Animal Science 56, 573-586. Pajor, E.A., D. Fraser and D.L. Kramer, 1991. Individual variation in the consumption of solid food by suckling pigs and its relationship to post-weaning performance. Applied Animal Behaviour Science 32, 139-155.

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Pettigrew, J.E., 1995. The influence of substrate supply on milk production in the sow. In: D.P. Hennessy and P.D. Cranwell (editors), Manipulating Pig Production V. Australasian Pig Science Association, Werribee, Victoria, pp. 101-106. Pluske, J.R. and G.Z. Dong, 1998. Factors influencing the utilisation of colostrum and milk. In: M.W.A. Verstegen, P.J. Moughan and J.W. Schrama (editors), The Lactating Sow. Wageningen Pers, Wageningen, pp. 45-70. Pluske, J.R., I.H. Williams and F.X. Aherne (1995). Nutrition of the neonatal pig. In: M.A.Varley (editor), The Neonatal pig - Development and Survival. CAB International, Wallingford, UK, pp. 187-235. Reale, J.A., 1987. Supplemental liquid diets and feed flavours for young pigs. M. Agr. Sc. Thesis, University of Melbourne. Rooke, J.A., M. Shanks and S.A. Edwards, 1998. Maternal and dietary influences on post-weaning piglet growth. In: Proceedings of the British Society of Animal Science, p. 156. Sarimento, J.I., P.L. Reinnels and H.W. Moon, 1990. Effects of pre-weaning exposure to a starter diet on enterotoxigenic Escherichia coli - induced post weaning diarrhoea in swine. American Journal of Veterinary Research 51, 1180-1183. Slade, R.D. and H.M. Miller, 1999. Influences of litter origin and weaning weight on post-weaning piglet growth. In: P.D. Cranwell (editor), Manipulating Pig Production VII. Australasian Pig Science Association, Werribee, Victoria, p. 131. Tokach, M.D., J.E. Pettigrew, L.J. Johnston and S.G. Cornelius, 1990. Overall performance to market weight is improved by adding milk products, but not fat to the starter diet. Journal of Animal Science 68 (Suppl. 1), 377. Toplis, P., P.J. Blanchard and H.M. Miller, 1999. Creep feed offered as a gruel prior to weaning enhances performance of weaned piglets. In: P.D. Cranwell (editor), Manipulating Pig Production VII. Australasian Pig Science Association, Werribee, Victoria, p. 129. Varley, M.A., 1992. Neonatal survival: an overview. In: Proceedings of the British Society of Animal Science, Occasional Publication No. 15, pp. 1-7. Williams, I.H., 1976. Nutrition of the young sow in relation to body composition. PhD thesis, The University of Melbourne. Williams, I.H., 1995. Sow milk as a major nutrient source before weaning. In: D.P. Hennessy and P.D. Cranwell (editors), Manipulating Pig Production V. Australasian Pig Science Association, Werribee, Victoria, pp. 107-113.

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4

Behavioural changes and adaptations associated with weaning P. Mormède and M. Hay

Summary In modern husbandry, weaning is an abrupt transition between two extremely different conditions and imposes numerous challenges to piglets: nutritional (from milk diet to solid food), environmental (temperature, characteristics of the lodging system), social (separation from the dam, interactions with unknown mates), and physical (transportation). Therefore, weaning leads to intense taxation of adaptive processes, both at the behavioural and at the neuroendocrine level. The consequences of weaning are more intense with earlier ages, although detailed biological data are still scarce. Several behavioural and biological indices indicate that the welfare of the piglets may be compromised during this period of intense adaptation. Experimental data clearly show that the anorexia or, at least, the nutritional deficit due to the abrupt transition from milk to solid food plays a major role in these alterations. New experimental approaches have been developed, allowing a detailed investigation of neuroendocrine changes in urinary excretion of stress hormones (cortisol and catecholamines), together with the monitoring of behavioural changes and production traits. Those new approaches should allow more comprehensive studies of the different factors impinging upon piglets at weaning when nutritional needs are covered, as well as a better appraisal of the influence of age at weaning. This knowledge is necessary to adjust weaning procedures to ensure an optimal production rate without compromising the welfare of the animals.

4.1

Introduction

In natural or seminatural conditions, weaning in the pig is a progressive process taking place around 12 to 17 weeks (Jensen, 1986; Newberry and Wood-Gush, 1988; Stolba and Wood-Gush, 1989; Boe, 1991). In modern husbandry, piglets are usually weaned abruptly at the age of 3-4 weeks. It can occur even earlier with the practice of segregated early weaning, which allows a better control of some diseases, and with the use of hyperprolific sows, which leads to an excessive number of piglets to be raised by the sows (Worobec and Duncan, 1997). Weaning is a period of important and numerous changes for the young piglets, including: separation from the dam, reallocation involving mixing with strangers, introduction in a novel environment and eventually transportation to a distant place in the case of segregated weaning, the radical change from a milk diet to solid food, and various other changes in the physical environment (e.g. ambient temperature, nature of the floor, air quality). Therefore, weaning leads to intense taxation of adaptive processes, both

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at the level of behavioural adjustments and neuroendocrine and other biological systems (Dantzer and Mormède, 1983).

4.2

Neuroendocrine consequences of weaning

Most available neuroendocrine data concern the variation of cortisol in plasma. Cortisol is a secretion product of the adrenal gland released under stimulation by the anterior pituitary hormone ACTH that, itself, is under hypothalamic control (Mormède, 1995). Circulating cortisol levels are very high at delivery, and decrease sharply immediately after birth and then more slowly during the first weeks of life, to increase thereafter (Kattesh et al., 1990; Carroll et al., 1998). Adrenal reactivity to ACTH also decreases during the first post natal weeks (Kanitz et al., 1999). A transient increase of cortisol levels at weaning has been described in a number of studies, whatever the age of the piglets, although the change tends to be higher when the animals are weaned at a younger age (Worsaae and Schmidt, 1980; Dantzer and Mormède, 1981; Rantzer et al., 1995, 1997; Carroll et al., 1998). Glucocorticoid receptor levels in the hippocampus were also reduced after weaning, alike after snaring stress in adults (Kanitz et al., 1998). Although the changes of cortisol level are widely used as an index of stress, they are not stimulus-specific. It is thus difficult to dissociate the respective contribution of the various changes associated with weaning in the activation of the hypothalamic-pituitary-adrenal (HPA) axis. A number of single factors like fasting (Farmer et al., 1992), maternal deprivation (Klemcke and Pond, 1991), exposure to novel environments (Mormède and Dantzer, 1978; Désautés et al., 1999), simulated or real transportation (Mormède and Dantzer, 1978; Lamboij and Van Putten, 1993, Perremans et al., 2001), and mixing of animals (Bradshaw et al., 1996) can all activate the HPA axis and may therefore play a role in the increase of cortisol levels measured at weaning.

4.3

The critical role of food

One critical change associated with weaning is the shift from sow’s milk to a dry feed, which induces a period of fasting during the first few days following weaning. This weaning anorexia has a negative impact on growth and leads to mobilisation of fat stores, as shown by the sharp increase of circulating free fatty acid levels (Bark et al., 1996). It may also be involved in the digestive problems that are frequently encountered after weaning (McCracken et al., 1999). Experimental data indicate that this period of under-nutrition markedly alters the functioning of several neuroendocrine systems during the post-weaning period. For instance, the changes measured in the somatotrophic axis (increased GH and reduced IGF levels) and in the autonomic nervous system (reduced catecholamine excretion in urine) are similar to those measured in fasting animals (Carroll et al., 1998; Hay et al., 2001). These changes may be long lasting, as in the case of weaning at 6 days of age for instance (Hay et al., 2001) (figure 4.1). Some of the metabolic responses

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b

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Figure 4.1. Consequences of early weaning (EW) on post-natal day 6 (C = control piglets raised by their dam). EW induced an early and persistent reduction in growth rate, that did not reach control values until the fourth post-natal week (panel a). EW transiently increased cortisol excretion in urine (panel c). EW induced an early and profound reduction in urinary levels of noradrenaline (panel b), that may be a consequence of starvation, in order to save calories via a reduction of heat production. This interpretation is supported by the change in thermoregulatory behavior of EW piglets that spend more time under the infrared lamp (panel e shows the proportion of piglets located under the infrared lamp, as recorded by scan sampling for 4 h/day). The reduction of adrenaline excretion in urine was postponed by a few days after EW, but was longlasting, as compared to noradrenaline (d), since adrenaline has a major role in the mobilisation of energy stores. The differential influence of EW on adrenaline and noradrenaline excretion is better illustrated by the ratio of the urinary content in both catecholamines (panel f). From Hay et al. (2001), with permission of Elsevier Science.

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to weaning can be corrected by milk feeding, which improves the growth rate of the animals as compared to dry feed (McCracken et al., 1995; Kim et al., 2001). Indeed, piglets weaned at 2-3 days of age and subsequently fed with a milk replacer display greater growth rates by day 7-8 of lactation than piglets raised by their dam, showing that sow milk yield is a limiting factor to piglet growth (Harrell et al., 1993). The increase of voluntary food intake after weaning by using whole cow’s milk also improves the mucosal architecture of the small intestine (Pluske et al., 1996). However, in commercial settings, weanling piglets are usually offered dry food, for economical reasons. Such a food is not accepted as well as a liquid milk replacer, and weaning alters average daily feed intake and average daily weight gain, the magnitude of which is larger with earlier weaning ages. As an example, Leibbrandt and collaborators showed that increasing weaning age (2, 3 and 4 weeks) resulted in reduced weight gain depression. All the animals nevertheless reached the same body weight at 6 weeks of age (Leibbrandt et al., 1975). Consumption of solid food by suckling piglets increases slowly and becomes significant only during the fourth week of age. Moreover, large differences among animals have been reported, and many piglets show no evidence of eating creep feed at the weaning age of 4 weeks (Barnett et al., 1989; Pajor et al., 1991; Fraser et al., 1994; Bruininx et al., 2002a). For instance, Bruininx and collaborators (2001) observed in 4-week piglets that the mean time to initiate feeding after weaning was 15.4 hours, with very large variation among individual piglets, ranging from a very short time up to four days after weaning. The initial feed intake was only slightly affected by sex or initial body weight, but occured sooner in animals eating significant amount of creep feed before weaning. Additionally, the daily weight gain was improved in those animals during the first weeks after weaning as compared to their littermates (Bruininx et al., 2002a). Much effort has been devoted to the development of highly palatable and easily digestible diet for nursing and weanling piglets, with mixed success. For instance, in an experiment with piglets weaned at 14-18 days of age, Gardner and collaborators (2001) compared the efficiency of two diets (a low-quality diet with a relatively high content of soybean meal and a high-quality diet enriched with blood plasma and fish meal) with and without addition of milk products. The low quality - no milk diet was slightly less consumed, but only during the first week after weaning, and the difference between diets disappeared thereafter. In accordance with the latter experiment, Lawlor et al. (2002) did not find any significant difference of feeding postweaning diets as dry pelleted feed, fresh liquid feed, acidified liquid feed and fermented liquid feed on pig performance from weaning (26 days) to harvest. Another attempt to increase food intake was made by increasing day length to 23 h (instead of 8 h). Although this lighting regimen was efficient to increase

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food intake and weight gain during the second week after weaning, no change could be observed during the first week (Bruininx et al., 2002b).

4.4

Behaviour

The behaviour of early weaned (6-day) piglets, as compared to animals raised by the dam, is characterised by an increase of vocalisations emitted during the first few days after weaning, increased restlessness, more aggressive behaviours and bellynosing, increased litter cohesion and increased time spent under the heating lamp (Orgeur et al., 2001). Most of these changes are still visible on day 20, i.e. 2 weeks after weaning, like some of the neuroendocrine changes (Hay et al., 2001). They have also been observed at various intensities in piglets weaned at older ages. For instance, belly-nosing, which consists of reciprocal massages, butting and sucking bouts, has been repeatedly described in weaned piglets, and its frequency increases when the age at weaning decreases (Boe, 1993; Worobec et al., 1999). Belly-nosing has been suggested to be a form of massaging that piglets would normally direct toward the udder both before and after a bout of suckling (Worobec and Duncan, 1997). However, the fact that it develops progressively over days after weaning and remains stable thereafter suggests that it may have its own psychobiological mechanisms and several authors have suggested that it reflects reduced welfare. As with belly-nosing, the increase of aggressive behaviours after weaning was found to be more intense when weaning occurred at a younger age (Worsaae and Schmidt, 1980; Orgeur et al., 2001). Aggressive behaviours are normal components of the behaviour of weaned pigs, but their high level of expression after early weaning may be part of the same general psychobiological syndrome indicative of altered welfare, together with belly-nosing and other behavioural changes.

4.5

Conclusion

There is no doubt that weaning is a period of intense stress for piglets, with profound consequences on growth, physiology, and disease outbursts, which reveal severe welfare problems. Experimental data clearly show that the anorexia or, at least, the nutritional deficit due to the abrupt transition between milk and solid food, induces severe taxation of the adaptive mechanisms of piglets and may be of special relevance from a welfare point of view. Most of the problem comes from the fact that during lactation spontaneous intake of dry food remains very low up to 3 weeks of age and does not become significant until the 4th week, indicating that the appetite for dry food is very low in younger piglets. The large individual variation suggests that this trait may be influenced by genetic factors and could therefore respond to genetic selection. It would be valuable to gain more information on the physiological changes induced by weaning at different ages. Indeed, most studies have focused solely on growth performance and behaviour up to now. Recent experiments showed however that measures of physiological stress, like urinary levels of catecholamines

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provide sensitive indications on the adaptation processes occurring at weaning and on the nature of the constraints imposed to piglets (Hay et al., 2001). Additionally, it would be interesting to design experiments where nutritional needs are covered, in order to assess the respective contribution of the other components involved in the stress of weaning (e.g. separation from the dam, transportation to remote places, change of the environment, mixing with unknown congeners).

References Bark, L.J., T.D. Crenshaw and V.D. Leibbrandt, 1986. The effect of meal intervals and weaning on free intake of early weaned pigs. Journal of Animal Science 62, 1233-1239. Barnett, K.L., E.T. Kornegay, C.R. Risley, M.D. Lindemann and G.G. Schurig, 1989. Characterization of creep feed consumption and its subsequent effects on immune response, scouring index and performance of weanling pigs. Journal of Animal Science 67, 2698-2708. Boe, K. 1991, The process of weaning in pigs: when the sow decides. Applied Animal Behavioural Science 30, 47-59. Boe, K. 1993. The effect of age at weaning and post-weaning environment on the behaviour of pigs. Acta Agriculturae Scandanavica 43, 173-180. Bradshaw, R.H., R.F. Parrott, J.A. Goode, D.M .Lloyd, R.G. Rodway and D.M. Broom, 1996. Behavioural and hormonal responses of pigs during transport: effect of mixing and duration of the journey. Animal Science 62, 547-554. Bruininx, E.M.A.M., C.M.C. Peet-Schwering, J.W. Schrama, P.F.G. Vereijken, P.C. Vesseur, H. Everts, L.A. Den Hartog and Beynen, A.C., 2001. Individually measured feed intake characteristics and growth performance of group-housed weanling pigs: effects of sex, initial body weight, and body weight distribution within groups. Journal of Animal Science 79, 301-308. Bruininx, E.M.A.M., G.P. Binnendijk, C.M.C. Peet-Schwering, J.W. Schrama, L.A. Den Hartog, H. Everts and A.C. Beynen, 2002a. Effect of creep feed consumption on individual feed intake characteristics and performance of group-housed weanling pigs. Journal of Animal Science 80, 1413-1418. Bruininx, E.M.A.M., M. J. W. Heetkamp, D. van der Bogaart, C. M. C. Peet-Schwering, A.C. Beynen, H. Everts, L. A. Den Hartog and J.W Schrama, 2002b. A prolonged photoperiod improves feed intake and energy metabolism of weanling pigs. Journal of Animal Science 80, 1736-1745. Carroll, J.A., T.L. Veum and R.L. Matteri, 1998. Endocrine responses to weaning and changes in post-weaning diet in the young pig. Domestic Animal Endocrinology 15, 183-198. Dantzer, R. and P. Mormède, 1981. Influence du mode d’élevage sur le comportement et l’activité hypophyso-corticosurrénalienne du porcelet. Reproduction, Nutrition, Development 21, 661670. Dantzer, R. and P. Mormède, 1983. Stress in farm animals: a need for reevaluation. Journal of Animal Science 57, 6-18. Désautés, C., A. Sarrieau, J.C. Caritez and P Mormède, 1999. Behaviour and pituitary-adrenal function in Large White and Meishan pigs. Domestic Animal Endocrinology 16, 193-205.

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Farmer, C., D. Petitclerc, G. Pelletier, P. Gaudreau and P. Brazeau, 1992. Carcass composition and resistance to fasting in neonatal piglets born of sows immunized against somatostatin and/or receiving growth hormone-releasing factor injections during gestation. Biology of the Neonate 61, 110-117. Fraser, D., J.J.R. Feddes, and E.A. Pajor, 1994. The relationship between creep feeding behavior of piglets and adaptation to weaning: effect of diet quality. Canadian Journal of Animal Science 74, 1-6. Gardner, J.M., C.F.M. de Lange and T.M. Widowski, 2001. Belly-nosing in early-weaned piglets is not influenced by diet quality or the presence of milk in the diet. Journal of Animal Science 79, 73-80. Harrell, R. J., M. J. Thomas and R. D Boyd, 1993. Limitations of sow milk yield on baby pig growth. Proc. Cornell Nutr. Conf., Ithaca, NY, 156-164. Hay, M., P. Orgeur, F. Lévy, J. Le Dividich, D. Condorcet, R. Nowak, B. Schaal and P. Mormède, 2001. Neuroendocrine consequences of very early weaning in swine. Physiology and Behaviour 72, 263-269. Jensen, P., 1986. Observations on the maternal behaviour of free-ranging domestic pigs. Applied Animal Behavioural Science 16, 131-142. Kanitz, E., G. Manteuffel and W. Otten, 1998. Effects of weaning and restraint stress on glucocorticoid receptor binding capacity in limbic areas of domestic pigs. Brain Research 804, 311-315. Kanitz, E., W. Otten, G. Nürnberg and K.P. Brüssow, 1999. Effects of age and maternal reactivity on the stress response of the pituitary-adrenocortical axis and the sympathetic nervous system in neonatal pigs. Animal Science 68, 519-526. Kattesh, H.G., S.F. Charles, G.A. Baumbach and B.E. Gillespie, 1990. Plasma cortisol distribution in the pig from birth to six weeks of age. Biology of the Neonate 58, 220-226. Kim, J.H., K.N. Heo, J. Odle, I.K. Han and R.J Harrell, 2001. Liquid diets accelerate the growth of early-weaned pigs and the effects are maintained to market weight. Journal of Animal Science 79, 427-434. Klemcke, H.G. and W.G. Pond, 1991. Porcine adrenal adrenocorticotropic hormone receptors; characterization, changes during neonatal development, and response to a stressor. Endocrinology 128, 2476-2488. Lambooij, E. and G. Van Putten, 1993. Transport of pigs. In: T. Grandin (editor), Livestock Handling and Transport. CAB International, Wallingford, UK, pp. 213-231. Lawlor, P.G., P.P. Lynch, G.E. Gardiner, P.J. Caffrey and J.V. O’Doherty, 2002. Effect of liquid feeding weaning pigs on growth performance to harvest. Journal of Animal Science 80, 1725-1735. Leibbrandt, V.D., R.C. Ewan, V.C. Speer and D.R. Zimmerman, 1975. Effect of weaning and age at weaning on baby pigs performance. Journal of Animal Science 40, 1077-1080. McCracken, B.A., H.R. Gaskins, P.J. Ruwe-Kaiser, K.C. Klasing and D.E. Jewell, 1995. Dietdependent and diet independent metabolic responses underlie growth stasis of pigs at weaning. Journal of Nutrition 125, 2838-2845. McCracken, B.A., M.E. Spurlock, M.A. Roos, F.A. Zuckermann and H. R. Gaskins, 1999. Weaning anorexia may contribute to local inflammation in the piglet small intestine. Journal of Nutrition 129, 613-619.

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Mormède, P. 1995. Le stress : interaction animal-homme-environnement, Cahiers Agricultures 4, 275-286. Mormède, P. and R. Dantzer, 1978. Behavioural and pituitary-adrenal characteristics of pigs differing by their susceptibility to the malignant hyperthermia syndrome induced by halothane anesthesia. 2 - Pituitary-adrenal function. Annales Recherches Veterinaires 9, 569-576. Newberry, R C. and D.G.M. Wood-Gush, 1988. Development of some behaviour pattern in piglets under semi-natural conditions. Animal Production 46, 103-109. Orgeur, P., M. Hay, P. Mormède, H. Salmon, J. Le Dividich, R. Nowak, B. Schaal and F Lévy, 2001. Behavioural, growth and immune consequences of early weaning in one-week-old Large White piglets. Reproduction, Nutrition, Development 41, 321-332. Pajor, E.A., D. Fraser and D.L. Kramer, 1991. Consumption of solid food by suckling pigs: individual variation and relation to weight gain. Applied Animal Behavioural Science 32, 139-155. Perremans, S., J.M. Randall, G. Rombouts, E. Decuypere and R. Geers, 2001. Effect of whole-body vibration in the vertical axis on cortisol and adrenocorticotropic hormone levels in piglets. Journal of Animal Science 79, 975-981. Pluske, J. R., I.H. Williams and F.X. Aherne, 1996. Villous height and crypt depth in piglets in response to increases in the intake of cow’s milk after weaning. Animal Science 62, 145-158. Rantzer, D., J. Svendsen and B. Weström, 1995. Weaning of pigs raised in sow-controlled and in conventional housing systems. 2. Behaviour studies and cortisol levels. Swedish Journal of Agricultural Research 25, 61-71. Rantzer, D., J. Svendsen and B. Weström, 1997. Weaning of pigs in group housing and in conventional housing systems for lactating sows. Swedish Journal of Agricultural Research 27, 23-31. Stolba, A. and D.G.M. Wood-Gush, 1989. The behaviour of pigs in a semi-natural environment. Animal Production 48, 419-425. Worobec, E. and I.J.H. Duncan, 1997. Early weaning in swine: a behavioural review. Compendium of Continueng Education for the Practising Veterinariun 9, S271-S277. Worobec, E., I.J.H. Duncan and T.M. Widowski, 1999. The effect of weaning at 7,14 and 28 days on piglet behaviour. Applied Animal Behavioural Science 62, 173-182. Worsaae, H. and M. Schmidt, 1980. Plasma cortisol and behaviour in early weaned piglets, Acta Veterinaria Scandanavica 21, 640-657.

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5

Metabolic and endocrine changes around weaning F.R. Dunshea

5.1

Introduction

One of the major stressors for the weaning pig is the rapid change from a liquid milk based diet to a solid pelleted cereal-based diet. All this occurs at the same time as the pigs are introduced into a new environment, mixed with other pigs and removed from the sow. The combined effect of this transition and these stressors is that newly weaned pigs often lose considerable weight (up to 10% of live weight) over the first 2 days post-weaning and may not regain this weight for up to 7 days post-weaning. These effects are more pronounced in young and small-for-age pigs (Power et al. 1996). The metabolic and endocrine changes that occur at this time are equally profound. In this chapter I will discuss the metabolic and endocrine events that occur after weaning and some of the interventions that have been tried to reduce this growth check.

5.2

The post-weaning check

Between birth and weaning, sucking pigs grow at approximately 220 g/day (King et al. 1993), but this growth rate is far below the biological potential of the artificiallyreared pig (Hodge, 1974). For example, pigs weaned at 2-3 days of age and fed cow’s milk or milk replacer alone until 21 days of age, can achieve growth rates in excess of 400 g/day (Harrell et al. 1993; Dunshea et al. 2002a). Since the sow increases milk production over the first two weeks of lactation before reaching a plateau (Toner et al. 1995), the extent to which milk yield limits piglet growth rate is exacerbated as lactation advances. For example, from d 21 of lactation, suckling piglet growth rate decreases, particularly in large litters (Cranwell et al. 1995a; Dunshea and Walton, 1995). That milk yield constrains piglet growth was demonstrated by Cranwell et al. (1995). Except for the period immediately after weaning (27-35 days) pigs exhibited considerably faster growth rate in all postweaning periods than they did while on the sow. To accommodate this decline in nutrient supply, suckling piglets may commence to eat creep feed, or sows feed, from about three weeks of age. However, the intakes of dry creep feeds are generally low and unlikely to significantly increase pre-weaning growth rate of pigs (Pluske et al. 1995). Also, given that in many parts of the world weaning typically occurs now at 21 d or younger, most piglets have had little opportunity to consume solid feed. It is little wonder then, that newly-weaned piglets consume very little feed over the first few days post weaning. The post-weaning check in body weight occurs in pigs that are heavy- or light-for-age (Figure 5.1; Dunshea et al. 2000a, 2002a,b)

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Figure 5.1. Effect of sex, weaning age and weaning weight on growth in pigs weaned onto solid diets. Animals were either weaned at between 12 and 17 days (Figure 5.1a) or 20 and 28 days (Figure 5.1b). Boars are depicted as open symbols and gilts as closed symbols. Light-, average- and heavy-for age pigs are depicted as triangles, squares or circles, respectively. Data are collated from a number of studies conducted by the author (Power et al. 1996; Dunshea, 2001; Dunshea et al 1.999a;2000a,b;2002b,c).

and is greater and lasts longer in early-weaned pigs (Power et al. 1996; Dunshea et al. 2002b). Collation of data from a number of studies conducted by the author demonstrate that pigs weaned at greater than 20 days of age take approximately 4 days to return to weaning weight, whereas pigs weaned at less than 17 days of age may not return to weaning weight until after 7 days post-weaning (Figure 5.1). The post-weaning check is also greater in boars and barrows than in gilt piglets (Power et al. 1996; Dunshea et al. 1999a; Dunshea, 2001; Bruininx et al. 2002) although this difference is only transient in nature. The reason for the reduction in live weight is the failure of weaned pigs to consume dry feed. Le Dividich and Seve (2000) collated data from 7 studies on feed intake

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immediately before and after weaning. Average milk energy intake prior to weaning was approximately 1250 kJ/kg0.75/day. On the day after weaning, solid feed intake was approximately 25% that achieved before weaning. By 1 week postweaning solid feed intake had increased but was still only 60-70% of that consumed prior to weaning. In a very comprehensive study, Bruininx et al. (2001) investigated the effect of weaning weight on time taken to first consume feed and found that on average it took approximately 15 h until pigs first consumed dry food. However, over half (53%) of the pigs had consumed food in the first 4 h after weaning when the lights were turned off for 12 h. Over the next 12 h of darkness only a further 3% of pigs commenced feeding. During the following 12 of light a further 32% of the pigs commenced feeding. These data suggest that although it can take some considerable time before weaned pigs consume feed there may be some potential to influence this by changing light patterns (Bruininx et al. 2002). The low feed intake and growth check immediately after weaning are consistent with a large number of observations in our laboratory (Power et al. 1996; Dunshea, 2001; Dunshea et al. 1999a,b; 2000a, b;2002a,b,c). The low feed intake, and poor or even negative growth rates, can be largely overcome by feeding the weaned pigs liquid instead of dry diets (Lecce et al. 1979; Odle and Harrell, 1998). Liquid diets (skim milk) have also been used to supplement dry post-weaning diets with considerable success especially if the pigs received the same liquid diet as a supplement prior to weaning (Dunshea et al. 1999a). Growth rates and DM intakes of up to 240 g/day and 260 g/day respectively, in the 7 days after weaning, were recorded in pigs supplemented with a liquid diet before and after weaning compared with growth rates of <30 g/day and DM intakes of up to 88 g/day in pigs that were not supplemented before weaning and then fed a dry diet. The critical importance of feed intake in the immediate post-weaning period has been demonstrated recently by Geary and Brooks (1998), who found that there was a highly significant (P<0.001) relationship between DM intake in the first 7 days post-weaning and 28-day post-weaning weight. For every 10 g/d of extra DM that a pigs eats in the 7 days post weaning, 174 g of extra body weight will be accumulated by 28 days post-weaning. Irrespective of the physical form of the diet another problem that can occur at weaning, especially in early-weaned pigs, is disease associated with enterotoxigenic bacterial infection of the gastrointestinal tract. Lecce (1986), a pioneer of artificial rearing of pigs, observed that while early-weaned pigs can be raised on liquid milk, “diarrhoea was the nemesis of the artificially reared pig” and remained the greatest barrier to adoption of these systems on farm. One method of overcoming this is to use liquid diets that have been fermented by lactic acid bacteria (or acidified) to reduce the pH of the diet to that which is inhibitory to pathogenic organisms (Azain et al. 1996; Geary and Brooks, 1998; Dunshea et al. 2000b). Liquid feeding systems for weaners, however, need not be based on milk or milk replacers

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but rather take the form of water and mash meal as is the case for grower-finishers. For example, Russell et al. (1996) fed weaner pigs either dry commercial pellets or the same diet as a liquid feed and observed an increase in daily gain, particularly over the first week after weaning. Thus, daily gain was increased by 110 and 25% over the first 1 and 4 weeks after weaning, respectively. However, under many pig production systems there is no opportunity to liquid feed the weaner pig and the metabolic events that occur at weaning are obligatory. Despite the fact that there is only a modest change in live weight over the first week post-weaning, there are quite dramatic changes in the weights of the visceral organs. In particular, there is an enormous increase in the weight of the large intestine as this becomes a major site of digestion of the solid feed. Initially, there is a decrease in the weight of the small intestine (Kelly et al. 1991; Spreeuwenberg et al. 2001) while the weight of the large intestine increases rapidly (Kelly et al. 1991; Pluske et al. 2003). For example, Kelly et al. (1991) found that by 3 days post weaning the small intestine and large intestine were 80 and 141%, of pre-weaning weights in pigs intragastrically-infused with cereal-based weaner feed. The weight of the small intestine subsequently increases in mass after the short period of weight loss and alteration in morphology (Cera et al. 1988). Similarly, we have found that in both early (14 d) and late (28 d) weaned pigs there is a considerable increase in the various intestinal components, both in total and relative mass, particularly in the early-weaned pigs (Pluske et al. 2003, Figure 5.2). There are also quite dramatic changes in small intestinal histology over this period. For example, McCracken et al. (1999) found that while there was no effect of weaning on the villous height on the first day post-weaning, by the second day post-weaning there

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Figure 5.2. Effect of weaning age (14 and 28 d of age) and time post -weaning on the body weight and weight of visceral organs. Data are expressed as a percentage of the respective weights at weaning. Data are from Pluske et al. 2003.

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was a 65% reduction in villus height. There subsequently follows a period of rapid hyper-regenerative villus repair (Cera et al. 1988; McCracken et al. 1999; Spreeuwenberg et al. 2001). In addition to these morphological changes in the gut there are also quite profound changes in the composition of the carcass as the piglet’s metabolism adjusts to meet the energetic deficit that occurs at weaning, as well as the change in substrates that the piglet receives.

5.3

Effect of weaning on metabolism

Prior to weaning, the piglet consumes a liquid milk diet with a high ratio of fat to protein and with lactose as the predominant source of carbohydrate. The neonatal pig is born with very little in the way of fat reserves, but because of the high fat content of sow’s milk, it incorporates much of the pre-formed fat from milk into body lipid (Mellor and Cockburn, 1986). In addition, the piglet obtains these nutrients every 45-60 minutes (Ellendorff et al. 1982; Auldist et al. 1998; 2000) and so tissues are receiving substrates at a relatively steady rate and are in an anabolic state. However, the newly weaned pig suddenly has this source of nutrients removed and unless it can consume some food, moves into a negative energy balance. This energy deficit can be exacerbated by the stress of being removed from the sow, mixing, transportation and change in temperature. All of these factors combine to alter metabolism and increase energy expenditure in the immediate post-weaning period. 5.3.1

Lipid and carbohydrate metabolism

The weaning-induced fasting results in mobilisation of fat, and to a much lesser extent glycogen, to provide energy to support life. Classical calorimetry studies demonstrate that pigs generally mobilise lipid while conserving or even deposit protein, with the mobilisation of body lipid being exacerbated at temperatures below the piglets ’lower critical body temperature (Le Dividich et al. 1980; Close and Le Dividich, 1984; Bruininx et al. 2002). Although not typically measured or reported, the amount of fat mobilised must be greatest over the first 2-3 days post-weaning, once the animals have absorbed the nutrients from sow’s milk and before they consume solid feed. For example, over the period between 1 and 6 days post-weaning feed intake increased from approximately 50 to 250 g/d while the average rate of fat mobilisation over the entire period was 20 g fat/d (Bruininx et al. 2002). Total heat production per day was relatively constant between 1 and 6 d post-weaning suggesting that most of the fat mobilisation occurred in the immediate couple of days post-weaning (Bruininx et al. 2002). Indeed, using slaughter balance techniques, Whittemore et al. (1981) found that over the first 2 d post-weaning pigs weaned at 21 d of age lost approximately 80 g fat/day, but that this fat loss progressively decreased over the next 6 d (Figure 5.3). These findings are supported by other slaughter balance data that show that both the proportionate and absolute body lipid contents are reduced over at least the first 7 d post-weaning.

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Figure 5.3. Effect of time post -weaning on body fat (open symbols) and protein (closed symbols) tissue gain. Data are from Whittemore et al. (1981).

Thus, in the study by Zijlstra et al. (1996) total body lipid decreased from approximately 11.2 to 8.5% of body weight in pigs weaned at 18 d of age. On the other hand, pigs that remained nursing the sow or were given milk replacer increased fat deposition by approximately 40 and 60 g/d, thus maintaining a similar proportionate lipid composition as at weaning at 18 d. Indeed, after weaning pigs of modern genotypes may not return to the same proportionate body lipid composition until 17 weeks of age (Dunshea et al. 2001). Plasma NEFA concentrations, which are directly related to the rate of fatty acid mobilisation from adipose tissue (Dunshea et al. 1992a), are elevated immediately after weaning (Bark et al. 1986; Funderburke and Seerley, 1990). Regression analyses of the mean data of Bark et al. (1986) demonstrate a strong inverse relationship between feed intake and plasma NEFA (Feed intake (g/d) = -4.2 + 234.9 * 0.998NEFA (µmol/L), n=20, R2 = 0.86, P<0.001) in weaned pigs, as is the case in ruminants (Dunshea et al. 1988). Thus, in response to the low feed intake that occurs immediately post-weaning, the newly weaned pig mobilises body fat as NEFA. This is clearly demonstrated when feed intake and plasma NEFA from the ad libitumfed pigs in their study are graphed against days post-weaning (Figure 5.4). In addition, the rate of lipogenesis in adipose tissue explants obtained from weaned pigs is very low suggesting that adipose tissue is in a net catabolic state at this time (Fenton et al. 1990). Interestingly, even though there is a dramatic reduction in energy intake over the first few days post-weaning, plasma glucose is reduced only transiently and slightly (Funderburke and Seerley, 1990) before returning to similar levels to those observed in suckled animals (Rantzer et al. 1997). These data suggest that there must be increased glycogen breakdown and/or increased gluconeogenesis in order to maintain glycemia after weaning. However, liver glycogen stores are relatively low at weaning (ca. 10 g/pig) and are relatively resistant to depletion after

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Figure 5.4. Effect of time post -weaning on feed intake (open symbols) and plasma non-esterified fatty acid (NEFA) concentrations (closed symbols). Data are from Bark et al. (1986).

weaning (Stanton and Mueller, 1976; Funderburke and Seerley, 1990) suggesting that gluconeogenesis must be the major source of glucose. Mobilised glycerol is the most likely source of gluconeogenic substrates rather than amino acids since whole body protein accretion is maintained in the post-weaning period (see next section) and plasma urea nitrogen is low in newly-weaned pigs (Pluske, 1995; McCracken et al. 1995). Plasma glycerol concentrations are not high in the weaned piglet (Pluske, 1995) possibly because the glycerol is rapidly cleared from the liver and converted to glucose. As we shall see later, some of the hormonal changes that occur around weaning orchestrate these necessary adaptations in metabolism. 5.3.2

Protein metabolism

The concept of homeorhesis, as defined as “the partitioning of nutrients towards a tissue of priority for a particular physiological state” by Bauman and Currie (1980), is possibly no better illustrated as by the conservation or increase in whole body protein, particularly in the gut, during the weaning-induced fast and subsequent undernutrition. In the case of the newly-weaned pig, the tissues of priority are gut and skeletal muscle protein. Thus, the neonatal pig has an enormous capacity to deposit protein and the whole-body fractional protein synthesis rate is at its highest in the first few weeks of life (Young, 1970). In the face of undernutrition the weaned pig attempts to conserve protein in the gut and to a lesser extent in skeletal muscle tissue. For example, Ebner et al. (1994) found that during periods of both protein and energy restriction, the decrease in protein deposition was less in the gastrointestinal tract than it was in skeletal muscle. Also, calorimetric studies indicate that whole-body protein balance is positive over the first week after weaning despite the animals being in negative energy balance (Bruininx et al. 2002). Nevertheless,

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the newly weaned pig must be in negative protein balance for at least the first 2 days after weaning since they consume so little food over this period of time. Extrapolation of the relationship between protein intake and protein balance suggests that the weaned pig needs to consume 3.1 g protein/kg0.75 (Le Dividich et al. 1980), or approximately 60 g/d of a typical weaner diet, to remain in zero protein balance. Using the slaughter balance technique, Whittemore et al. (1981) found that newlyweaned pigs were in a slight negative protein balance for the first 4 days after weaning (Figure 5.3). However, there is no doubt that very soon after commencing to consume solid food the newly-weaned piglet is in positive protein balance and there is a rapid expansion of the gut and other visceral organs. It is also interesting that the rate at which protein deposition increases with increasing feed intake is greater at low as compared to high levels of energy consumption (Close and Stanier, 1984). Feeding stimulates the fractional rate of protein synthesis and protein accretion in the small intestine and skeletal muscle of young pigs (Davis et al. 1996; 1997). While the post-prandial increase in insulin stimulates protein synthesis in skeletal muscle, insulin does not appear to be the mediator of the increase in intestinal protein synthesis that occurs after feeding (Davis et al. 2001). Likewise, systemic elevations of amino acid concentrations, achieved through intravenous infusion, have little effect on intestinal protein synthesis stimulation (Davis et al. 2002). Therefore, it appears that the feeding-induced increase in protein synthesis is due to an increase in amino acid supply via the intestinal lumen rather than via increased arterial supply of insulin or amino acids. In this context, dietary amino acids make a greater contribution to small intestinal protein synthesis than circulating amino acids in fed neonatal pigs (Stoll et al. 1999). As the weaned pig moves from a liquid milk diet to a period of limited feed consumption followed by a gradual increased ingestion of a dry complex diet, there are some dramatic changes to intestinal growth and histology (see above). It is likely that some of the hormonal changes that occur post-weaning help to conserve gut and body protein.

5.4

Hormonal status

The onset of weaning results in some quite profound hormonal changes, although it is difficult to separate cause and effect. No doubt many of the changes are in response to the social and nutritional stress associated with weaning but there are also overlying developmental changes that likely occur independent of the weaning process. 5.4.1

Somatotropin and insulin-like growth factor-I

Although porcine somatotropin (pST) increases lean tissue growth and decreases fat growth in grower and finisher pigs, the response to pST is much less in younger pigs (Campbell et al. 1991). For example, young weaned pigs (ca. 10.0 kg, age not

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given) did not exhibit any growth response to pST until after at least 10 d of treatment and even then the response was inconsistent (Harrell et al. 1997). This was despite elevated plasma IGF-I and insulin levels and reduced plasma urea as a result of only 5 d with pST treatment (Harrell et al. 1997). Also, pST administration at the doses used in finisher pigs (0.06 mg/kg) failed to increase plasma IGF-I or growth in neonatal sucking pigs although there was limited evidence of subsequent growth responses (Dunshea et al. 1999b). In contrast, Wester et al. (1998) found that a relatively high dose of exogenous pST (1 mg/kg) increased plasma IGF-I and growth over the first 7 days of life in artificially-reared pigs. Likewise, Dunshea et al. (2001) found that relatively high doses of pST could increase lean tissue and decrease fat deposition in neonatal pigs. The ontogeny of somatotropin and its receptors in the neonate has been well studied in a variety of species although data specific to the pig are relatively scarce. In the young pig plasma ST is very high around parturition, declines rapidly over the first week of birth, then remains constant until the second week of life before gradually increasing again over the next 5 weeks and declining once again (Buonomo and Klindt, 1993; Matteri and Carroll, 1997). ST then gradually declines up to at least 30 weeks of age (Harrell et al. 1997; Klindt and Stone, 1984; Owens et al. 1991). These patterns of plasma ST concentrations are essentially the same as in vitro basal and growth hormone releasing hormone-stimulated ST release from cultured pituitary cells (Matteri and Carroll, 1997). ST receptor mRNA has been found in the liver of the fetal (Duchamp et al. 1996) and neonatal (Brameld et al. 1995) pig and it increases over at least the first 20 d of life (Owens et al. 1990). Therefore it appears that the ST receptor gene is being transcribed but there may be only a limited number of functional receptors being produced or alternatively, there may be some functional receptors that are resistant to ST but that may respond to high doses of exogenous pST. Either of these scenarios would explain why there was little response to moderate doses of exogenous pST (Dunshea et al. 1999b) whereas there was modest response to high doses of pST (Wester et al. 1998; Dunshea et al. 2001) in neonatal pigs. Weaning itself results in a decrease in plasma IGF-I and a simultaneous increase in plasma ST (White et al. 1991; Tang et al. 1995; Carroll et al. 1998; Matteri et al. 2000). The study of Matteri et al. (2000) quite clearly demonstrated that the decrease in IGF-I concentrations was related to the onset of weaning rather than being a developmental response since animals that remained nursing the sow had much higher levels of IGF-I than weaned pigs. Also, the decrease in plasma IGF-I occurs regardless of weaning age, at least between 14 and 35 days (White et al. 1991; Matteri et al. 2000). Circulating IGF-I does not return to pre-weaning values until 1 to 2 weeks post-weaning at a similar time to when pre-weaning energy intakes are achieved (Le Dividich and Seve, 2000). Exogenous IGF-I and analogues inhibit pST secretion in 60 kg growing pigs (Dunaiski et al. 1997), and it is possible that the

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increase in pST after weaning is in response to the profound decrease in IGF-I and subsequent diminution in the inhibitory effects of IGF-I upon pST secretion. The increase in pST in response to the reduction in feed intake at weaning may occur in an attempt to conserve gut and skeletal muscle protein. Indeed, the proteins in the gastrointestinal tract have an enormous turnover and without some conservation of these organs the gut would reduce in size to a greater extent than it does immediately after weaning. Interestingly, in weaned pigs fed either a high or low feed intake, the hepatic ST receptor mRNA was down-regulated whereas it was upregulated by a low feed intake in the four muscles examined (longissimus, rhomboideus, soleus, and cardiac) (Katsumata et al. 2000). In contrast, at 2 d postweaning Matteri et al. (2000) did not see any effect of weaning on either skeletal muscle, adipose tissue or hepatic ST receptor mRNA. However, there were differences between different weight classes. These adaptations to underfeeding may explain how skeletal muscle is spared during the weaning-induced negative energy balance via muscle ST receptor up-regulation and/or elevated circulating pST. Indeed, the effects of pST on protein metabolism differ between the fed and the fasted state with pST increasing protein deposition in the fed state via increasing protein synthesis and decreasing protein degradation and amino acid oxidation (Vann et al. 2000a), whereas protein loss is minimised during the fasted state via an increase in protein synthesis and a decrease in amino acid oxidation (Vann et al. 2000b). Therefore, a number of workers have investigated whether somatotropin or IGF-I treatment of neonatal and/or weaned pigs can ameliorate the weaning-induced depression in feed intake and weight gain. Dunshea et al. (1999b) treated nursing pig with daily pST injections (0.06 mg/kg) from day 4 until weaning on day 31 and found little effect of pST on daily gain until the final 3 days of lactation. However, immediate post-weaning growth was not studied. In a subsequent study, Dunshea et al. (2001) found that pre-weaning fat and immediate post-weaning lean tissue deposition were decreased with much higher doses of pST (1.0 mg/kg per day) given from day 1 until weaning on day 21. Previous pST treatment of finisher pigs causes a large (ca. 50%) reduction in the amount of pST contained in the pituitary (Campbell et al. 1989). Therefore, it may be possible that pST treatment of neonatal pigs may decrease pituitary pST production and/or delay the development of somatotrophic activity in the pituitary (Matteri et al. 1997). A decrease in endogenous pST production in the immediate post-weaning period may be the cause of the reduced lean tissue deposition in weaner pigs previously treated with pST and this may limit the applicability of neonatal pST treatment to improve immediate post-weaning performance. Despite these findings, it may be worth investigating pST treatment during the weaning process since daily pST injection partially reversed a dexamethasone-induced catabolic state in weaned piglets, although the combined pST/IGF-I therapy was even more efficacious (Ward and Atkinson, 1999). Also, exogenous pST partially ameliorated fasting induced protein catabolism in older pigs (Vann et al. 2000b).

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Exogenous IGF-I, the putative mediator of pST’s action on lean tissue growth, has also been investigated as a means of increasing growth of weaned pigs. Acute IGF-I treatment increases protein synthesis in neonatal pigs consuming milk replacer in a variety of tissues, but this response is markedly lower in 26-d-old as compared to 7-d-old pigs (Davis et al. 2002). Schoknecht et al. (1997) found that chronic IGF-I infusion (4 µg/h) for 7 d increased growth rate of suckling normal and intra-uterine growth retarded (IUGR) piglets. However, similar doses (2, 4 and 8 µg/h for 8 d) of IGF-I or the potent analogue LR3IGF-I had little effect upon growth rate in artificially-reared pigs that were restrictively-fed to grow at similar rates to those observed in pigs suckling the sow (ca. 200 g/d) (Dunshea et al. 2002a). In a study in the same series, IGF-I or LR3IGF-1 were infused into neonatal pigs (from ca. 4 d of age) that were consuming cow’s milk ad libitum. While neither IGF-I nor LR3IGF-1 infusion (8 µg/h) had any effect upon feed intake or growth rate over the first 9 d of Experiment 2, when the infusion rates were doubled (16 µg/h), there was an increase in feed intake and growth rate over the second 9 d, particularly in pigs infused with LR3IGF-I (Dunshea et al. 2002a). Although there were few significant effects of IGFs on visceral organs, the liver and small intestinal weights tended to be greater in pigs infused with LR3IGF-I. In a subsequent experiment, the interactions between nutrient intake (manipulated through establishing litter sizes of 6 and 12 piglets) and LR3IGF-I infusion in suckling piglets were investigated (Table 5.1). Again, although there was an increase in growth during LR3IGF-I treatment, this did not become manifest until the latter stages of the experiment. Also, growth responses to LR3IGF-I were greater in the piglets from litters of 12. LR3IGF-I infusion increased visceral organ size and, as for growth rate, the responses were greatest in the piglets under the greater nutritional stress. Therefore, it could be hypothesised that neonatal treatment with IGF-I or analogues either before and/or after weaning may help piglets withstand the weaning check. However, subsequent studies directed at ameliorating the post-

Table 5.1. Effect of LR3IGF-I infusion on growth performance and organ size in suckling piglets from litters of 6 or 12 piglets (Dunshea and Walton, 1995). Growth factor (GF)

Control

Litter size (L)

6

12

6

12

sed

L

GF

ADG (0-27 d), g/d ADG (18-27d), g/d Small intestine, g Liver, g Spleen, g

299 294 359 263 29

187 114 247 168 16

304 325 373 312 53

199 167 311 221 40

19.0 32.0 34.0 23.0 6.3

0.001 0.001 0.011 0.001 0.033

0.43 0.036 0.047 0.003 0.001

Concepts and consequences

LR3IGF-I

P value

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weaning check in pigs infused with LR3IGF-I both before and after weaning and in piglets that did or didn’t receive supplemental milk failed to show any benefits of LR3IGF-I on growth performance although increases in the mass of some visceral organs were observed (Tomas, 1996). 5.4.2

Insulin

Insulin plays a key role in the regulation of growth and tissue deposition in the young pig. Insulin stimulates the partitioning of amino acids to protein deposition and away from oxidation and gluconeogenesis while also stimulating glucose incorporation into fat (Dunshea et al. 1992b; Wray-Cahen et al. 1998; Davis et al. 2001). In the sucking pig, insulin increases skeletal muscle protein synthesis although this response declines between 7 and 26 d of age (Davis et al. 2001;2002). However, insulin has no effect upon protein synthesis in visceral and intestinal tissues nor is there a decline in protein synthesis over this age range (Davis et al. 2001;2002). Insulin decreases during fasting in neonatal pigs (Davis et al. 1996), and although there are little supporting data, it is reasonable to assume that insulin decreases immediately post-weaning. For example, plasma insulin decreases precipitiously on the day following weaning (Rantzer et al. 1997) but returns to pre-weaning values within 2-3 days. Similarly, plasma insulin was comparable 5-7 days after weaning as in pigs that had been maintained on liquid cow’s milk (Pluske, 1995, Zijsltra et al. 1996). Also, plasma insulin was higher in pigs weaned onto a liquid milk replacer diet than in those weaned onto a cereal diet on d2 after weaning but not subsequently (McCracken et al. 1995). Thus, a decrease in insulin immediately after weaning would result in a mobilisation of fat and glycogen to meet the energy demands of the young pig. A decrease in insulin would also favour an increase in gluconeogenesis since elevated insulin inhibits gluconeogenesis (Dunshea et al. 1992b). Presumably, weaning would cause a decrease in protein synthesis in skeletal muscle but not necessarily in visceral and intestinal tissues. This may partially explain how total and relative intestinal masses are maintained, or even increased, during the immediate post-weaning period (see Figure 5.2). In addition, refeeding stimulates protein synthesis in visceral and intestinal tissues via a mechanism independent of insulin and post-hepatic amino acid supply (Davis et al. 2002). The inference is that once pigs do commence feeding after weaning then visceral mass will be stimulated, in part because of first-pass utilization of nutrients from the gut lumen (Stoll et al. 1999). On the other hand, the increase in skeletal muscle protein synthesis is due to the post-prandial increase in insulin rather than directly to an increase in nutrients (Davis et al. 2002). 5.4.3

Hypothalamic-pituitary axis

The stress associated with weaning generally results in a rapid, but transient, increase in plasma and urinary cortisol concentrations that lasts for 1-2 d (Carroll et al. 1998;

72

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Metabolic and endocrine changes around weaning

Kanitz et al. 1998; 2002; Hay et al. 2001). By 5 d post-weaning, plasma and urinary cortisol concentrations have decreased to pre-weaning or suckled control values (Pluske, 1995; Hay et al. 2001). Funderburke and Seerley (1990) attempted to partition the immediate post-weaning plasma cortisol responses into psychological, climatic and nutritional effects. While they found none of the treatments resulted in average plasma cortisol concentrations over the 48 h post-weaning that were significantly different from those of pigs that remained nursing, plasma cortisol were highest in pigs that faced the nutritional stress. Also, in samples that were obtained via venipuncture (as compared to bleeding via a catheter), plasma cortisol was significantly higher in pigs that were subject to a nutritional as compared to psychological or cold stress (Funderburke and Seerley, 1990). Cortisol stimulates gluconeogenesis and has been implicated in the development of gluconeogenic capacity in the fetal pig (Martin et al. 1980; Fowden et al. 1995). Indeed, the latter authors speculated that the prepartum rise in endogenous cortisol may be responsible for the increase in fetal gluconeogenic capacity observed towards term. It is possible that the post-weaning surge in cortisol may be involved in the next developmental increment in gluconeogenic capacity. Although there may be a transient decrease in circulating glucose concentrations immediately post-weaning, plasma glucose quickly returns to pre-weaning levels before pigs really commence to consume feed (Stanton and Mueller, 1976; Rantzer et al. 1997; Funderburke and Seerley, 1990) suggesting an increase in gluconeogenesis. Plasma catecholamine concentrations in the pig are very sensitive to acute stress. For example, the concentrations of both epinephrine and norepinephrine can increase many-fold (>25-fold) within a minute of the application of stressor such as restraint (Neubert et al. 1996). Exogenous catecholamine injection increases fat and glycogen mobilisation (Dunshea and King, 1995; Dunshea et al. 1998) and so it may be anticipated that weaning would increase circulating catecholamines to favour the mobilisation of energy stores during the early post-weaning period. However, the effects of weaning on the catecholamine system are equivocal. Stanton and Mueller (1973) found that the adrenal glands of weaned pigs were larger and tended to contain more norepinephrine than those of pigs that remained with the sow. Likewise the activities of some of the adrenal gland enzymes involved in catecholamine synthesis, including tyrosine hydroxylase, were higher in weaned pigs. Adrenal epinephrine was not altered by weaning. Mann and Sharman (1983) found that that while there was a decrease in the amount of tyrosine hydroxylase in the adrenal gland of early weaned pigs there was an increase in the activity of the enzyme, and suggested that this indicates a mechanism compensating for the decreased amount of enzyme. In contrast, Hay et al. (2001) found that urinary norepinephrine was lower on d 7, 11 and 14 of age in pigs that were weaned at 6 d of age compared to their suckled contemporaries. Urinary epinephrine concentrations were lower at 14 and 19 d of age in the early-weaned pigs. Therefore, given these contrasting observations the actual role of the catecholamine system

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in adrenergic system in the regulation of metabolism of the weaned pig is still unclear.

5.5

Conclusions

One of the major stressors for the weaning pig is the rapid change from a liquid milk based diet to a solid pelleted cereal-based diet. All this occurs at the same time as the pigs are introduced into a new environment, mixed with other pigs and removed from the sow. The combined effect of this transition and these stressors is that newly weaned pigs do not eat for up to 2 d and often lose considerable weight which may not be regained until up to 7 d post-weaning. Most of the tissue loss is fat that is mobilised to meet the energy deficit that occurs as a result of the low feed intake. On the other hand, carcass and particularly visceral protein is not as labile, although there are certainly morphological changes in the gut. These metabolic adaptations are favoured by the hormonal milieu that exists immediately post-weaning and beyond.

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Owens, P.C., M.A. Conlon, R.G. Campbell, R.J. Johnson, R. King and F.J. Ballard, 1991. Developmental changes in growth hormone, insulin-like growth factors (IGF-I and IGF-II) and IGF-binding proteins in plasma of young growing pigs. Journal of Endocrinology 128, 439447. Pluske, J.R., 1995. Psychological and nutritional stress in pigs at weaning: Production parameters, the stress response, and histology and biochemistry of the small intestine. PhD Thesis, The University of Western Australia. Pluske, J.R., I.H. Williams and F.X. Aherne, 1995. Nutrition of the piglet. In ‘The Neonatal Pig. Development and Survival’. (Ed. M.A. Varley) pp. 187-235. (CAB International: Wallingford, UK). Pluske, J.R., D.J. Kerton, P.D. Cranwell, R.G. Campbell, B.P. Mullan, R.H. King, G.N. Power, S.G. Pierzynowski, B. Westrom, C. Rippe, O. Peulen and F.R. Dunshea, 2003. Age, sex and weight at weaning influence the physiological and gastrointestinal development of weanling pigs. Australian Journal of Agricultural Research (manuscript submitted). Power, G.N., J.R. Pluske, R.G. Campbell, P.D. Cranwell, D.J. Kerton, R.H. King and F.R. Dunshea, 1996. Effect of sex, weight and age on post-weaning growth of pigs. Proceedings Nutrition Society of Australia 20, 137 (Abstr.). Rantzer, D., P. Kiela, M.J. Thaela, J. Svendsen, B. Ahren, S. Karlsson and S.G. Pierzynowski, 1997. Pancreatic exocrine secretion during the first days after weaning in pigs. Journal of Animal Science 75, 1324-31. Russell, P.J., T.M. Geary, P.H. Brooks and A. Campbell, 1996. Performance, water use and effluent output of weaner pigs fed ad libitum with either dry pellets or liquid feed and the role of microbial activity in the liquid feed. Journal of the Science of Food and Agriculture 72, 8-16. Schoknecht, P.A., S. Ebner, A. Skottner, D.G. Burrin, T.A. Davis, K. Ellis and W.G. Pond, 1997. Exogenous insulin-like growth factor-I increases weight gain in intrauterine growth-retarded neonatal pigs. Pediatric Research 42, 201-207. Spreeuwenberg, M.A., J.M. Verdonk, H.R. Gaskins and M.W.A. Verstegen, 2001. Small intestine epithelial barrier function is compromised in pigs with low feed intake at weaning. Journal of Nutrition 131, 1520-1527. Stanton, H.C. and R.L. Mueller, 1976. Sympathoadrenal neurochemistry and early weaning of swine. American Journal of Veterinary Research 37, 779-83. Stoll, B., D.G. Burrin, J.F. Henry, F. Jahoor and P.J. Reeds, 1999. Dietary and systemic phenylalanine utilization for mucosal and hepatic constitutive protein synthesis in pigs. American Journal Physiology 276, 49-57. Tang, M., A.G. van Kessel and B. Laavel, 1995. Ontogeny of insulin-like growth factor I in pigs from birth to 65d of age. Annual Research Report. Prairie Swine Centre (Saskatoon) 61-62. Tomas, F.M., 1996. Promotion of lean and efficient growth by treatment of sucking pigs with growth factor. Final report CSN5/0998, Pig Research and Development Corporation, Canberra, Australia. Toner, M.S., R.H. King, F.R. Dunshea, H. Dove, C.S. Atwood, 1996. The effect of exogenous somatotropin on lactation performance of first-litter sows. Journal of Animal Science 74, 167-172. Vann, R.C., H.V. Nguyen, P.J. Reeds, D.G. Burrin, M.L. Fiorotto, N.C. Steele, D.R. Deaver and T.A. Davis, 2000a. Somatotropin increases protein balance by lowering body protein degradation in fed, growing pigs. American Journal of Physiology 278, E477-483.

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Vann, R.C., H.V. Nguyen, P.J. Reeds, N.C. Steele, D.R. Deaver and T.A. Davis, 2000b. Somatotropin increases protein balance independent of insulin’s effects on protein metabolism in growing pigs. American Journal of Physiology 279, E1-10. Ward, W.E. and S.A. Atkinson, 1999. Growth hormone and insulin-like growth factor-I therapy promote protein deposition and growth in dexamethasone-treated piglets Journal of Pediatric and Gastroenterology Nutrition 28, 404-410. Wester, T.J., T.A. Davis, M.L. Fioretto and D.G. Burrin, 1998. Exogenous growth hormone stimulates somatotropic axis function and growth in neonatal pigs. American Journal of Physiology 274, E29-37. White, M.E., T.G. Ramsay, J.M. Osborne, K.A. Kampman and D.W. Leaman, 1991. Effect of weaning at different ages on serum insulin-like growth factor I (IGF-I), IGF binding proteins and serum in vito mitogenic activity in swine. Journal of Animal Science 69, 134-145. Whittemore, C.T., H.M. Taylor, R. Henderson, J.D. Wood and D.C. Brack, 1981. Chemical and dissected composition changes in weaned pigs. Animal Production 32, 203-210. Wray-Cahen, D., H.V. Nguyen, D.G. Burrin, P.R. Beckett, M.L. Fiorotto, P.J. Reeds, T.J. Wester and T.A. Davis, 1998. Response of skeletal muscle protein synthesis to insulin in suckling pigs decreases with development. American Journal of Physiology 275, E602-609. Young, V.R., 1970. The role of skeletal and cardiac muscle in the regulation of protein metabolism. In: Mammalian Protein Metabolism, pp 585-674, ed. H.N. Munro, Academic Press, New York. Zijlstra, R.T., K.Y. Whang, R.A. Easter and J. Odle, 1996. Effect of feeding a milk replacer to earlyweaned pigs on growth, body composition, and small intestinal morphology, compared with suckled littermates. Journal of Animal Science 74, 2948-59.

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6

Factors affecting the voluntary feed intake of the weaned pig P.H. Brooks and C.A. Tsourgiannis

6.1

Introduction

For the wild pig, or the domestic pig kept under natural conditions, weaning represents a slow transition from reliance totally on sows milk to a situation where the pig has become an independent forager no longer reliant on nutrients supplied by its mother. For the domesticated piglet, weaning is an event, an abrupt separation from the sow and a sudden denial of maternal support. The response of the piglet to this separation depends upon the experience that it has gained before this event, and the age at which the event takes place. Typically, domestic piglets are removed from the sow, between 12 and 28 days of age; much earlier than they would be denied maternal support in natural conditions. Consequently, they have to develop new feeding strategies in hours rather than weeks. Their inability to make this transition quickly frequently results in a reduction in growth rate immediately following weaning. Pigs that may have been growing at around 200-300 grams per day before weaning, experience a period of very low or even negative growth immediately following weaning. This has usually been treated as a nutritional problem. Nutritionists have attempted to compensate for the low feed intake of weaned piglets by increasing the nutrient density of the diets and have responded to the enteric problems that ensue by the addition of antimicrobial products to the diet. However, this chapter will propose that the problems facing the newly weaned domestic pig are behavioural rather than nutritional. By attempting to understand the evolutionary advantages that the pig would gain from certain natural patterns of behaviour, we may be able to appreciate the extent to which commercial weaning practices for domestic pigs have subverted these behaviour patterns. By understanding the changes that the pig has to make to its behaviour following weaning, we can explain why some management practices may adversely affect feed intake. Conversely, an improved understanding of behaviour may allow us to develop management practices that will enable the young pig to maintain its pre-weaning growth in the post-weaning period.

6.2

Feeding behaviour of piglets kept under ‘natural’ or ‘semi-natural’ conditions

In order to understand the problems that the domestic piglet faces in confinement housing systems, it is important to refer to our knowledge of behavioural development in wild pigs and domestic pigs kept under conditions that are more natural. In nature, weaning is not an event, but a process that takes place over a

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several weeks. This process has three different but interrelated developmental strands, namely, behavioural, nutritional and immunological. The appropriate development of each strand influences the health of the pig and its ability to function independently from of its mother and from its littermates. The piglet has to adapt from a situation in which it obtains all its food by suckling the sow, which is an instinctive behaviour, to foraging / independent feeding, which has significant learned components. Initially, the piglet relies totally on its mother’s milk. Sows milk provides not only nutrients, but also immunoglobulins, bioactive proteins and peptides, which stimulate and modulate the development of the gut (Zabielski, 1998). The sow is the most important factor influencing the microbial environment into which the piglet is born (Conway, 1966). The first bacteria that the piglet encounters are organisms colonising the sow’s vagina and teats and emanating from her faeces. These organisms are ingested during the birth process, and from the sow’s teats when the piglet subsequent suckles, and have a profound influence on the structure and biochemistry of the gut, the gut ecosystem, and on immunological development (Kelly and King, 2001). Under natural conditions, the pre-weaning lactation period can be divided into four phases (Table 6.1). For the first 10 days of lactation (range 3-16d), the piglets remain in, or in very close proximity to, a nest prepared by their mother (hiding phase) (Jensen and Redbo, 1987). When the piglets leave the nest their mother takes them to rejoin the matriarchal group. From this point on the piglets will accompany the sow on her foraging trips (following phase) (Jensen, 1986). The piglets do not necessarily forage, but will rest close by the sow as she forages. As the piglets grow, their fat reserves increase; they gain strength, and will spend increasing amounts of time in the close proximity of the sow and will watch her foraging. They will sample the feed that the sow eats. This sampling of food and non-food substrates (e.g. soil) exposes the gut to novel food sources, antigens and microorganisms. In turn, this exposure to novel substrates stimulates the development of the piglet’s gut enzyme system (Kidder and Manners, 1978) and contributes to the development of active immunity. The period around three weeks of lactation can be considered an immunological low point. Passive (colostrum derived) immunity has declined to a low level and active immunity is only just starting to develop. The sow initially determines the pattern of food acquisition by the piglet. Sows initiate nursing on a cyclical basis (Lewis and Hurnik, 1986). Pigs are drawn to the sow by her vocalisations regardless of how hungry they may be (Lewis and Hurnik, 1985). This response maintains the contiguity of the litter and synchronises behaviour (Castren et al., 1989). Although piglets generally suckle from the same teat throughout lactation (de Passille and Rushen, 1989; Fraser and Morley-Jones, 1975; McBride, 1963), the pattern is not constant (Puppe et al., 1993). There is considerable

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Table 6.1. Schematic outline of the development of piglets under natural conditions. Week Phase

Behavioural features

Influence on piglet development

1

Hiding

Piglets initially isolated in nest built by mother. Limited excursions beyond the nest.

2-3

Following Piglets leave nest and follow (Familiarizing) sow. Sow and litter rejoin matriarchal group. Piglets remain in litter group with little or no integration with other piglets. Piglets start rooting. Integration Piglets increase foraging (Learning?) (grazing) behaviour. Piglets start to integrate with others. Sow leaves piglets for increasing periods. Interval between nursing events increases. Sows increasingly terminate nursing events. Piglet become fully integrated with other members of the social group.

Nutrients provided entirely by mother. Development of GI tract determined by nutrients and bioactive molecules in sow’s milk. Initial microbial colonisation of GIT dominated by flora from sow. Passive immunity provided by immunoglobulins in sow’s milk. Milk still dominates nutrition. Bioactive molecules in milk continue to influence GIT development. Limited sampling of environment exposes GIT to other microbes. Active immunity develops in response to sampling of environment.

4-7

8-17 Independent

Nutritional demand of piglets starts to outstrip supply by sow stimulating pigs to forage for themselves, usually in proximity of sow. Reduced suckling opportunities and limitations of nutrient supply by sow encourage piglets to forage independently. New food sources stimulate development of GIT and immune system. Milk still contributes to gut health and development. Passive immunity is no longer effective. Piglets engage in agonistic behaviour, resolve conflicts and develop new social structure. Nursing by the sow becomes Piglets become increasingly less frequent and at some independent of both the sow and point ceases (pigs weaned). their litter group. Piglets function independently as Piglets develop independent feeding part of extended social group. strategies (meal size/ meal interval). Piglets may still sleep in family Removal of milk represents the final group with sow. stage in GIT development.

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variation in milk production from different teats (Algers and Jensen, 1991; Fraser, 1980; Fraser and Thompson, 1986). It is generally presumed that the anterior teats are the most productive and are claimed by the stronger more vigorous piglets. Recent studies on domestic pigs would suggest that this is correct and that teat order becomes more rigid as the lactation progresses (Puppe and Tuchscherer, 1999). The formation of a teat order may promote orderly feeding and eliminate competition between piglets when feeding (Fraser, 1980; McBride, 1963). This may be important for the piglet’s survival, as milk is only available for 10-20 seconds at each nursing event (Barber et al., 1955; Fraser, 1980; Whittemore and Fraser, 1974). There is considerable variation in the interval between nursing events (Table 6.2), but it averages approximately 50 minutes in the first week of lactation. The intrasuckling interval increases to around 90 minutes after 2-4 weeks (Horrell, 1997) and over 300 minutes by ten weeks of lactation (Bøe, 1991). It also becomes increasingly variable (30->200 minutes) between 6 and 10 weeks of lactation (Newberry and Wood-Gush, 1985). Similar intra-suckling intervals occur in wildtype and domestic sows in the first week post farrowing (Gustafsson et al., 1999). However, in the second week of lactation the intra-suckling interval tended to be longer in domestic sows.

Table 6.2. Estimates of intra-suckling intervals. Interval (minutes)

Day of lactation

Reference

40 to 45 40 to 60 29 to 78 76 51and 63 (range 26-96) 44 range (21 to 92) 48 to 52 52 (range 42 to 68) 53± 9.7 42± 2.4 91± 6.7 86± 21.3 64 72 102 182 334

1 to 13 1 to 14 1 to 42 3 6 to 51 7 to 28 10 to 24 14 to 5 First 48 h 6 to 8 14-28 42-49 14 28 42 56 70

(Arey and Sancha, 1996) (Gustafsson et al., 1999) (Newberry and Wood-Gush, 1984) (Spinka et al., 1997) (Barber et al., 1955) (Ellendorff et al., 1982) (Auldist and King, 1995) (Wechsler and Brodmann, 1996) (Horrell, 1997)

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(Bøe, 1991)

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The extension of the interval between nursing events coincides with the increasing nutrient demand of the piglets and the reduction in nutrient supply by the sow, which occurs from 3-4 weeks onwards (Mackenzie and Revell, 1998). The sow increasingly terminates suckling bouts and by the fourth week of lactation sows terminate them all (Jensen and Recen, 1989). Sows have been observed to nurse their pigs while standing from 4 weeks of lactation (Bøe, 1991). This encourages the piglets to find alternative sources of nutrients. Despite this, some sows continue to suckle their piglets intermittently for up to 20 weeks. Bøe (1991) observed that although the number of sucklings per day gradually decreased there was no drop in daily weight gain as the piglets increased their intake of solid food to compensate for the reduced intake of sow’s milk. The period from around four to around eight weeks of age can be regarded as an integration and learning phase in the piglet’s behavioural development. Despite being part of the group, there is little mixing or interaction with other pigs before four weeks of age (Jensen, 1986). The family affiliations loosen between six and eight weeks, with piglets increasingly associating with pigs in the group that are not littermates (Jensen, 1995). There is considerable variation in the relationship between sows and individual pigs in their litter. The proportion of sucklings at which one or more of the litter was missing increased up to 12 weeks post-partum. The pigs that missed sucklings were within the lighter half of litters and, although near the sow, did not seem to take any interest in suckling. The average age for complete weaning of litters appears to be around 17 weeks of age (Jensen and Recen, 1989; Petersen, 1994). However, there were large variations between pigs within litters (range 15.6 to 19.5 weeks). This implies that piglets suckling less productive teats invest less time and effort in trying to obtain nutrients from their dam and increasingly adopt an independent foraging strategy. From around four weeks onwards, piglets become members of a larger matriarchal group and will forage alongside the adults within that group (integration/learning phase). The piglets learn foraging behaviour by following their mother and by copying her behaviour patterns. It is likely that they learn from her example which sources are suitable food materials and which are not. Although piglets have been observed to root from the first week of life onwards, grazing behaviour appears to commence at around three weeks of age and, between 4 and 11 weeks of age, piglets increased the proportion of time spent grazing from 7 to 56% (Petersen, 1994). The pig is an opportunistic feeder and is primarily herbivorous (Baber and Coblenz, 1987). Ninety percent of the diet of the wild pig is vegetable matter, of which 50% comprises seeds and fruits (Spitz, 1986). The remaining 10% of the diet comprises ground-dwelling insects, molluscs and earthworms. Consequently, when the wild piglet starts taking solid food, that food will have a dry matter content of between 15 and 30%. In nature, this gradual transition from a milk diet, through a mixed diet, to a diet devoid of milk, provides the stimulus, and allows time for, the enzyme and immune

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systems of the immature gastrointestinal tract (GIT) to develop and for adaptation of the microbial population in the gastrointestinal tract. We can summarise the key features of the weaning process under natural or seminatural conditions as follows: -

• Weaning is not a single event, but an extended process of gradual adjustment that occurs over a period of three or more months.

• Sow milk continues to be available to the piglet while it samples novel foods • • • •

and while its gut adapts microbiologically and immunologically to these new food sources. The slow changeover from total dependence on sow’s milk to total dependence on solid food maintains continuity of nutrient input and prevents transient starvation. The piglet integrates into the larger social group over a period of time and with a minimum of aggression. Initially, the sow determines the feeding strategy of the piglet and sow vocalisations and the behaviour of littermates reinforces group-feeding behaviour. Independent foraging starts at different ages for different pigs, prompted by an inadequate supply of sow milk to the individual. However, for the majority of pigs within a litter, group-feeding (suckling) behaviour is still a significant component through to 8-10 weeks of age.

6.3

Commercial weaning practice - an event rather than a process

For practical reasons weaning on commercial pig units has little in common with weaning in natural conditions. Some of the key differences between natural and commercial weaning are summarised in Table 6.3. Sows and their litters are normally housed individually prior to weaning, so there is no opportunity for the pigs to socialise with non-littermates. In order to maximize sow reproductive output piglets are removed from their dams before they have achieved behavioural independence. In recent years, there has been a trend towards very early weaning in North America (12-18 days) while in the EU weaning below 21 days is not permitted. The EU plans to increase the minimum age at weaning to 28 days and in some European countries, such as Sweden, where the use of antibiotic growth promoters has been banned, weaning age is often increased to 35 or even 42 days. At weaning pigs are moved to a new environment and frequently new and larger social groups are formed by mixing unfamiliar pigs. Solid feed and water is provided for them from unfamiliar dispensers. The age at which weaning takes place, and the amount of experience that the piglet has had of alternative feed sources, influence its ability to cope with these changes. In addition, the environment into which the pig is weaned and the

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Table 6.3. Key differences between natural and commercial weaning. Natural weaning

Commercial weaning

Piglets integrate with other members of an extended group before and during the weaning process. Weaning is an extended process occurring over a period of around three months.

Piglets generally have no opportunity to integrate with non-littermates before weaning. Weaning is a single event, taking place on a specific day (generally varies between 14 and 35 days). Sow milk (and its bioactive constituents) is not available to support the transition to dry feed.

Sow milk continues to be available to the piglet while it samples novel foods and while its gut adapts microbiologically and immunologically to these new food sources. The slow changeover from total dependence on sow’s milk to total dependence on solid food maintains continuity of nutrient input and prevents transient starvation. Solid food contains around 200 g DM per kg No change of environment at weaning

Piglets continue to sleep with sow(s) in the matriarchal group even after weaning. The piglet integrates into the larger social group over a period of time and with a minimum of aggression.

Sudden removal of sow milk results in transient starvation, adverse effects on the gut architecture and limited, zero, or negative growth for a period immediately post weaning Solid food contains around 800-850 g DM per kg. Piglets usually moved to a new environment and have to adapt to different feeding and drinking equipment. Piglets removed from the sow. Piglets frequently regrouped and mixed unfamiliar pigs at weaning, resulting in considerable aggression and potential physical damage.

way the pig is managed following weaning contribute to the success or failure of the transition. The following sections consider the ways in which pre- and postweaning management influence feed intake and contribute to the success or failure of the weaning process.

6.4

Pre-weaning feed and water intake

The young pig has little control over its food intake. While the young of any species are being suckled, there is no evolutionary value in them having their intake limited. It is beneficial for them to consume all the nutrients that the dam can provide.

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Consequently, the mother is the factor determining feed intake, not the physiology of the animal being suckled. Despite selection to produce large quantities of milk, modern sows are still unable to satisfy the demands of their growing litter from a relatively early stage of lactation. Over the years a number of authors have shown that piglets can achieve greater growth on milk based diets than they can if left to suckle the sow (Benevenga et al., 1990; Braude et al., 1970; Harrell et al., 1993; Zijlstra et al., 1996). Harrell et al. (1993) have calculated that the milk production of modern sow genotypes becomes limiting to the growth of their litters at around 8-10 days of lactation. They also calculate that by 21 days of age the sow would need to produce in excess of 18 kg milk per day (approximately twice the milk yield of modern sows) in order to support growth rates equivalent to those achieved by artificially reared pigs. As the sow’s milk output is inadequate to meet the piglet’s demands, and in order to prepare pigs for weaning, piglets may be offered solid (creep) feed before weaning. However, as discussed earlier, in natural conditions piglets take little in the way of solid food in the first three weeks after birth. Domestic pigs in confinement housing show the same pattern. Consequently, piglets weaned at 21 days or less will have consumed little or no solid food. For example, Metz and Gonyou (1990), reported that piglets weaned at two weeks of age consumed only 7 g food per day in the two days before weaning, whereas piglets weaned at four weeks of age consumed 127 g. Pajor et al. (1991) found that although confined piglets began sampling feed at around day 12 (ranging between day 10 and 28), intake was generally less than 5 g per pig per day up until day 20 of lactation. Between day 20 and 28 piglets consumed an average of 63 g/d, but there was great variation between individual piglets (2-205 g/d). The total intake before weaning varied from 13-1911 g/pig. Similarly, Delumeau and Meunier-Salaün (1995) found that feeding activity started around 21 days and, in weeks 3 and 4, creep feed intake was very variable between litters (range 0-2382 g). It would appear that while the sow is available as a provider of nutrients, the piglet concentrates its efforts on stimulating the sow to suckle more frequently and provide more milk, rather than utilising other available sources of nutrients to maximise its feed intake. This is demonstrated by the data of Bøe and Jensen (1995) (Figure 6.1). In their study, piglets continued to suckle sows for eight weeks. The intake of creep feed by individual pigs ranged between 0-437 g/d at four weeks of age and 0-1571 g/d at eight weeks of age. The range in weight of piglets at eight weeks of age (range 6.326.6; mean 17.7) reflected the wide difference in nutrient intake. It would seem reasonable to expect that the pigs suckling less productive teats would compensate for their limited nutrient supply by taking more creep feed, and this has been confirmed in some studies (Algers et al., 1990). Fraser et al.(1994) reported that, in piglets weaned at 28 days, creep feed consumption varied greatly between littermates, but that pigs consuming more creep feed than their littermates tended to be those that had the lowest weight gains up to three weeks of age. However, other authors have reported that larger piglets, occupying the more productive teats,

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2000

20

1600

16

1200

12

800

8

400

4

0

Mean piglet weight (kg)

Creep feed intake (g/d)

Factors affecting the voluntary feed intake of the weaned pig

0 4

5

6 7 Week of lactation

Creep feed intake (mean and range)

8 Piglet weight

Figure 6.1. Variation in the creep feed intake of individual pigs during weeks 4-8 of lactation. (After Bøe and Jensen, 1995). N.B. the bars represent the range of individual pig intake at each sampling point.

also consumed more creep feed (Bøe, 1991; Bøe and Jensen, 1995). The variability in feeding behaviour and feed intake by individuals before weaning has important implications for weight at weaning and for the development of the gastrointestinal tract (Nabuurs et al., 1996). Therefore, it is important to try to understand the reasons for these wide variations in pre-weaning feed intake. In recent years, researchers have attempted to classify piglets based on individual behaviour traits. Hessing et al. (1993) classified piglets as ‘aggressive’ and ‘nonaggressive’ based on them displaying an active or passive coping strategy. However, other researchers have robustly refuted this classification (Forkman et al., 1995; Jensen et al., 1995a). Forkman et al. (1995) identified three personality traits that explained 60% of the total variation, namely, aggression (25%), sociability (20%) and exploration (15%), whereas Jensen et al.(1995b) found no evidence of consistent individual behaviour strategies similar to those displayed by rodents. However, individual ‘personality’ was not related to performance in any of these studies. To date the only evidence for a link between individual behaviour traits and growth performance comes from studies undertaken using 17-day-old, weaned pigs (Giroux et al., 2000). In their study, they found a relationship between rank order and growth in piglets. However, the social rank of the piglets accounted for only 9% of the variation among individuals. It is our contention, that the strongly reinforced group feeding behaviour of suckling pigs provides the explanation for the observed differences. We have noted that piglets with a less productive teat will often take creep feed while littermates with productive teats suckle the sow. This is consistent with the findings of Appleby et al. (1991; 1992), who compared creep feed intake of piglets provided with 2 or 8 creep feeding spaces (Figure 6.2).

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Creep food intake per piglet (g)

140 120 100

Gain 21-28d=261g

80 60 Gain 21-28d=248g

40 20 2 feeding spaces

8 feeding spaces

0 21

22

23

24

25

26

27

Day of lactation Figure 6.2. Consumption of creep feed by piglets provided with 2 or 8 creep feeding places (After Appleby et al., 1992).

On average, 4.1 piglets per litter consumed very little on the day before weaning when only two feeding spaces were provided. These tended to be piglets that had a high birth weight, and high growth rates on days 0 to 21, but low growth rates from day 28 (weaning) to day 42. Conversely, piglets that ate the most creep feed were often those that had gained least on days 0-21. Providing eight feeding spaces increased the average intake on the three days before weaning and reduced the number of pigs eating very little on the day before weaning to 0.6 pigs per litter. Usually, creep feed is supplied as a meal or a pellet; however, there have been some notable improvements in performance when piglets have been offered supplementary nutrients in liquid form. In a very large study, Azain et al. (1996), offered piglets a liquid milk replacer from birth to weaning at 21 days and found that they consumed 0.375 and 1.49 kg DM during the cool and warm season respectively, resulting in a significant increase in weaning weight. However, as with solid feed intake there was great variation in consumption between and within litters. Significant increases in weaning weight resulting from feeding liquid diets have been reported in other studies (Kavanagh et al., 1995). Not only food intake but also water intake varies considerably in the pre-weaning period. The type of drinker provided also affects water intake (Gill, 1989). In the humid tropics, piglets began to drink water between 3 and 5 hr after birth (Kabuga and Annor, 1992; Nagai et al., 1994). Nagai et al. (1994) found that water consumption per pig increased from 36 ml/day at day 1 of lactation to 403 ml/day

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at day 28. Interestingly, water consumption per kg body weight remained constant at 51 to 62 ml, regardless of age. Over a 7-week lactation, piglets provided with water ate more creep food (3215 g/pig) than control piglets that had no water provided (2166 g/pig) (Friend and Cunningham, 1966). However, up to 3 weeks of age, there were no treatment differences and the piglets consumed only 62 g creep food per pig. Gill et al. (1991) found that up to 3 weeks of age piglets consumed only 34.7 ± 3.4 g creep feed per pig, and that the provision of water did not increase creep feed consumption.

6.5

Relationship between pre-weaning food consumption and post-weaning growth

It might be anticipated that familiarity with food and water before weaning would be an advantage to the pig and would result in improved feed intake and live weight gain thereafter. However, there is no compelling evidence that this is the case when pigs are weaned at 21 days or less as they will have had little experience of feed. Piglets that ate more solid food before weaning gained more weight in the two weeks following weaning (Appleby et al., 1991). However, the pigs with the higher creep feed intakes also had higher birth weights so the apparent response may merely reflect greater developmental maturity in these pigs. Subsequently, Appelby et al. (1992) characterised pigs based on their individual creep feeding behaviour (Table 6.4). They found an inverse relationship between birth weight and creep feeding behaviour, and that increasing creep feed intake did not result in any increase in growth rate in the post-weaning period. By 42 day of age, there was no significant difference between the pigs classified in the different groups.

Table 6.4. Weights and performance of piglets according to their creep feeding category (based on the proportion of time they were seen at the creep feeder) (After Appleby et al., 1992). Creep feeding category Body weight (g)

Very low

Low

Medium

High

Birth 42 days

1572 10939

1509 11308

1471 10774

1280 10601

218 240 224

198 267 271

170 244 284

177 254 257

Gain (g/d) Day 0-21 Days 21-28 Days 28-42

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In the case of pigs weaned at 28 days or later, there is some evidence of beneficial effects of creep feeding. Pajor et al.(1991) found that litters with the greatest average feed intake had the highest post-weaning gains. However, there was little evidence of a similar relationship within litters. Post-weaning feed intake tended to be higher in piglets with an estimated creep feed intake above 100g between days 14 and 27 (Delumeau and Meunier-Salaün, 1995). Friend et al. (1966) found that pigs that consumed more creep feed than their littermates tended to be those with low gains in the first three weeks after birth. They found that creep feed intake accounted for only 4% of individual variation in post-weaning gain. In another study, pigs weaned at 27 days were fed creep feed either as dry pelleted feed or as fermented liquid feed (Brooks and van Zuylen, 1998). Piglets were divided into two weight groups at weaning, 5.5-7.5 kg (Low) and 7.5-9.5 kg (High) and were all fed fermented liquid feed for three weeks post weaning. Dry feed was offered in addition from 14 days post weaning. There were no significant differences in post weaning growth rate, although pigs that had low weaning weights, and pigs that had received fermented liquid creep feed, tended to have higher growth rates (Table 6.5). Examination of the growth rate data on a weekly basis revealed a significant difference in growth rate between the two weaning weight groups during the first week post weaning (Table 6.6). Pigs with a low weaning weight had a growth rate more than double that of their heavier littermates. However, the higher growth rate was not sufficient for them to catch up with the initially heavier pigs by three weeks post weaning. In practical situations, producers often attempt to encourage intake by providing continuity of feed pre- and post-weaning. However, this is of little assistance if the pre-weaning pig has not sampled the feed. A different approach was attempted by Campbell (1976) who fed a flavouring agent to sows that would expressed in their

Table 6.5. Post-weaning performance of pigs with low or high weights at weaning offered fermented liquid feed (FLF) or dry pelleted feed (DPF) during the suckling period (After Brooks and van Zuylen, 1998).

Dry matter feed intake (g/d) Daily gain (g) Dry matter FCR

92

Weaning weight (kg)

Pre-weaning feed regime

5.5-7.5

7.5-9.5

FLF

DPF

427 372 1.15

402 353 1.13

422 373 1.14

406 351 1.14

Weaning the pig

Factors affecting the voluntary feed intake of the weaned pig

Table 6.6. Post-weaning growth rate (g/d) of pigs with low or high weights at weaning offered fermented liquid feed (FLF) or dry pelleted feed (DPF) during the suckling period (After Brooks and van Zuylen, 1998).

Week 1 Week 2 Week 3 Overall a

Weaning weight (kg)

Pre-weaning feed regime

5.5-7.5

7.5-9.5

FLF

DPF

204a 333 577 427

97a 411 552 402

156 378 585 422

144 366 544 406

SED

37 41 37 82

means with the same superscript differ significantly P<0.05.

milk and then added the same flavour to the post-weaning diet of the piglets, which were weaned at 30 days of age. The aim was to encourage consumption feed intake by association with a familiar flavour. In this study, the provision of flavour in both the sow feed and the weaner diet the pigs significantly increased feed intake and daily gain. These studies do not appear to have been repeated in pigs, although a similar approach has been investigated in human infants (Mennella and Beauchamp, 1991; 1993; Mennella et al., 2001). In summary: • Piglets weaned at 21 days or less, and previously offered creep feed, are unlikely to have consumed more than a few grams. Therefore, they will be unfamiliar with the concept of consuming solid food. • In litters weaned at 28 or more days piglets will have a very variable experience of solid food consumption. Some will have become familiar with solid food; others will have little or no experience of solid food. • The balance of evidence would suggest that in pigs weaned at 28-35 days the larger pigs in the litter, which have suckled the most productive teats, would have least experience of eating solid food. • Providing more feeding spaces is likely to improve creep food consumption. • Liquid feed supplements may be consumed more readily than dry feed. • Irrespective of the form in which creep feed is presented the differences in intake between litters and between pigs within litter are extremely large. • Experience of obtaining water and water intake will be very variable within and between litters.

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6.6

Feeding behaviour of the post-weaned pig

Following abrupt weaning the piglet has to adapt its feeding and drinking behaviour very rapidly to take account of its new environment. Generally, it fails to do this and as a result, there is a dramatic reduction in its dry matter intake (Figure 6.3) following weaning. Dry matter intake does not recover to the preweaning level until the second week post weaning.

Average dry matter intake (g/pig)

As described earlier, in natural conditions, weaning is a gradual transition from sow’s milk (circa 20% dry matter), to a solid diet containing 15-30% dry matter, over a number of weeks. This is in marked contrast to the situation on commercial units. The confinement-reared piglet is weaned abruptly and expected to make an instant transition from a liquid diet, of around 20% dry matter, to a compound diet containing 80-90% dry matter, usually presented in pelleted form. Before weaning the stimulus provided by the sow has two important effects on feeding behaviour. First, the sow calling her piglets to feed conditions them to suckle at regular intervals and, second, it programmes the litter to feed as a group (Brooks and Burke, 1998). Abrupt weaning removes the stimulus to eat at regular intervals that was previously provided by the sow. If litter groups are separated, the stimulus of group (litter) behaviour is also disrupted.

700 600 500 400

Weaning 300 200 100 0 1

2

3

Week of Lactation*

Day Day Day Day Day Day Day 1 2 3 4 5 6 7 Day following weaning (Week 4 of age)

5

6

7

8

Week of age

Figure 6.3. Typical (mean) feed intake pattern of pigs weaned at 21 days. * Dry matter intake in lactation is the sum of sow milk and creep feed.

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Attempts have been made to stimulate feeding behaviour in pigs by playing recorded sow feeding calls. Playing recorded sow nursing chants in a farrowing house at regular intervals improved piglet growth by around 8% in one study (Cronin et al., 2001) but had not noticeable effect on performance in another (Kasanen and Algers, 2002). Similarly, playing recorded nursing chants to weaned piglets had some effect on feeding behaviour (Csermely and Woodgush, 1981; Petrie and Gonyou, 1988). The latter authors found that playing nursing chants to pigs increased feeding time from 104 to 127 minutes on the second day after weaning, with inconclusive effects on growth performance. Keeling and Hurnik (1996) hypothesized that familiar individuals would spend more time at the feeder and be more synchronized than unfamiliar individuals. They found that this was correct in the case of females but not males. Familiar males were more synchronized in their feeding but unfamiliar males spent more time at the feeder and ate most feed. We might expect that piglets that were unfamiliar with food would learn to eat from watching their experienced pen mates. However, this is not necessarily the case. Nicol and Pope (1994) allowed piglets to observe either untrained-sibling, or trained-sibling, demonstrator pigs press one of two panels for food reward during 10 daily sessions. In subsequent tests there were no significant effects of observation experience on rewarded panel pressing. However, pigs that had observed demonstrators spent significantly more time facing the operant panels and directed more non-rewarded presses at the operant panels than did controls. A recent study (Morgan et al., 2001) attempted to investigate the extent to which experienced weaners transferred information about solid food to inexperienced weaners. There was some indication that the presence of an experienced piglet stimulated earlier feeding behaviour by inexperienced piglets. However, variation among the experimental animals was such that none of the differences reached statistical significance. Our observations on commercial units would be consistent with these findings. We have observed pigs that have suckled together approaching a feeder together, but this did not ensure that they all ate. If not all the pigs were able to eat at the same time the dominant pigs fed and the subservient pigs stood behind and observed. When the dominant pigs were satisfied, they left the feeder and returned to the resting area. Subservient pigs either took very small meals and then rejoined the group or did not feed and returned to the resting area with siblings that had eaten (Brooks, unpublished data). The observed phenomena could indicate a deficiency in the learning mechanism of some pigs, i.e. they are slow learners or lack the confidence to act independently. Alternatively, it could indicate an overriding influence of social behaviour (group synchrony). In nature, synchronous, group behaviour would benefit the population even if it did not necessarily work in the best interest of the individual. However, in commercial production, such group behaviour could (and apparently does) disadvantage some individuals.

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6.7

Feed and water intake of weaned pigs

When weaning occurs as a gradual process, piglets have the opportunity to learn by experience about food and water, without interruption of nutrient intake from the sow. In contrast, domestic pigs weaned at 21 days or less will have been used to having both their hunger and their thirst satisfied by the sow’s milk. When weaned, these piglets have to learn to distinguish between the physiological drives of hunger and thirst. They also have to learn how to satisfy these drives by consuming water and solid food. Lack of familiarity with food and water means that it may take some time for the pig to learn how to satisfy its requirements and maintain its homeostatic balance. Some years ago we reported a study demonstrating that in the immediate post-weaning period, piglets consumed water rather than eating food (Figure 6.4). Only when they learned to recognise food did they develop a more normal water to feed ratio (Table 6.7). Recent studies have demonstrated that not only is there great variation in the feeding behaviour of pigs pre-weaning, but also there is great variation immediately postweaning. Using a computerized weighing station, Bruininx et al.(2001b) measured the intake of individual pigs in a group-housing situation immediately post-weaning. Their data (Figure 6.5) illustrated two important points. First, there was considerable variation in the interval from weaning to the first feed, with around 10% of pigs taking more than 40 hours to take their first feed and some taking almost 100 h.

2.2 2.0

Water intake (I)

1.8 1.6 1.4 1.2 1.0 0.8 0.6 0.4 0.2 0.0 1 2 3

4 5

6 7 8

9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24

Day post weaning Figure 6.4. Water intake (litres per pig per day) of piglets weaned at 21 days of age (After Brooks et al., 1984).

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Table 6.7. Ratio of water consumed (g) to food consumed (g) by pigs weaned at 21(1 days of age and fed on two commercial diets (After Brooks et al., 1984). Week post weaning

Water:Feed ratio

1 2 3 4

Commercial diet A

Commercial diet B

4.3:1 3.2:1 2.9:1 2.8:1

4.0:1 3.5:1 3.6:1 3.7:1

Second, the number of pigs that had started to eat increased very little during the dark phase. As the performance of the pigs fed using a computerised station was similar to that of pigs fed using single space feeders (Bruininx et al., 2001a), it may be assumed that the pattern of feed intake was similar to that pertaining in this type of feeding system. However, such systems prevent social facilitation and prevent the type of synchronous feeding behaviour that would be more normal in pigs of this age.

100 Fasting pigs, % of total

90 80 70 60 50 40 30 20 10 0 0

10

20 30 40

50 60 70 80 90 100

Post-weaning interval, h

Figure 6.5. Percentage of pigs not having fed at different intervals post-weaning. Lines represent pigs in different weaning weight categories. Shaded bands correspond with dark periods (After Bruininx et al., 2001a).

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We have recently studied the latency to first feed in pigs offered liquid feed in a situation where 50% of the pigs could eat simultaneously (Brooks and Brice, unpublished data). The results (Figure 6.6) show a similar pattern to the data of Bruininx et al. (2001b). While a majority of pigs had taken their first meal within 3 minutes of weaning, some pigs were took a very long time (up to 54 h) before eating their first meal, even though their pen mates had already found and were consuming feed. We have been unable to find any data on the feeding behaviour of pigs in situations where the entire litter group have the opportunity to eat together. In recent years, there has been a trend to house weaners in larger and larger groups (from 100 to 1000 pigs in a group). However, there has been little attempt to determine the effect that this has on the individual or the extent to which large group size affects variability. One advantage of large groups is that littermates are generally kept together. Subjective observations of pigs in very large groups (100+ pigs) suggest that litters tend to retain an identity and continue to show synchronised feeding behaviour. In such settings, generally there are insufficient feeding places for the entire pen group to indulge in synchronous feeding. However, there may be less disturbance of feeding behaviour than in small groups, as litter groups can still feed together and independently of other litter groups in the pen.

23 21 19

Pig number

17 15 13 11 9 7 5 3 1 0

10

20

30

40

50

60

Interval from weaning to first feed (h)

Figure 6.6. Interval from weaning to first feed for group housed piglets weaned at 21 days and offered liquid fermented feed (Brooks and Brice, unpublished data).

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These observations have important implications both for practical management and for experimental design. Stockpersons need to recognise that even if some pigs are observed to use the feed and water provided in the pen this does not mean that all the pigs are. Thus, management strategies must have the aim of ensuring that feed and water acquisition by all pigs in the group takes place as soon after weaning as possible. Because experiments usually consider the mean performance of groups of pigs, treatment differences may result either from a change in the behaviour of some pigs in the group or from a change in the biological response of the whole population. The period for which the pig does not eat post-weaning is particularly important but so is the pattern of feeding that the pig adopts once it has started to eat. Bark et al. (1986) allowed pigs weaned at 21 days to feed ad libitum or, for 15 minutes at 2-, 4-, or 6-hourly intervals. Even the pigs fed ad libitum failed to consume enough feed during the 3 days post-weaning to satisfy their maintenance requirements, and feed intake was less in the pigs fed at increasing intervals (Figure 6.7). Consequently, pigs fed at 4-, or 6-hourly intervals had not regained their weaning weight seven days post weaning (Figure 6.8).

6.8

The significance of maintaining continuity of food intake after weaning

Average daily feed intake (g/pig)

It is easy to forget that the epithelial lining of the gut is the most rapidly growing tissue in the body and that many of the nutrients required for gut growth are absorbed direct from the gut lumen. The work of Pluske and his co-workers (Pluske

250 200 150 100 50 0 1 ad lib

2

3 4 5 Day post weaning 2-hourly

4-hourly

6

7 6-hourly

Figure 6.7. Feed intake of pigs weaned at 21 days of age and fed ad lib. or for 15 minutes at 2-, 4-, or 6-hourly intervals (After Bark et al., 1986).

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Liveweight (g)

7000

6800 Weaning weight 6600

6400

6200 1 ad lib

2 3 4 5 Day post weaning 2-hourly

4-hourly

6

7

6-hourly

Figure 6.8. Live weight change in pigs weaned at 21 days of age and fed ad lib. or for 15 minutes at 2-, 4-, or 6-hourly intervals (After Bark et al., 1986).

et al., 1996a; 1996b; Pluske et al., 1997), showed that a continuous supply of nutrients is essential in order to maintain the villous architecture of the gut postweaning. Previous studies suggested that villus height was greater when pigs were fed a liquid diet rather than a dry diet (Deprez et al., 1987). It was assumed that the physical form of the food was responsible for this effect. However, the studies undertaken by Pluske and his co-workers demonstrated that the change in villus height was not a function of diet form, but of nutrient intake. In their study, feeding liquid diets at a maintenance energy level still resulted in a reduction in villus height five days post weaning. However, when pigs were fed an allowance equivalent to three times the requirement for maintenance, villus height was actually greater than that immediately pre-weaning. A recent study, using a larger data set (Ward and Moran unpublished data), has again demonstrated the positive relationship between dry matter intake and villus height (Figure 6.9). Conversely, there is good evidence, from rats, that transient starvation can result in atrophy of the villi (Rudo et al., 1976; Steiner et al., 1968). A reduction in villus height reduces absorption and leaves more nutrients escaping digestion and entering the lower gut. This promotes the development of an inappropriate gut microflora that in turn can result in enteric disease. The practical implication of these findings is that every effort must be made to maintain continuity of food and water intake following weaning.

100

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Mean villous height (µm)

800 700 600 500 400 300 200 100 0 0

500

1000

1500

2000

2500

3000

3500

4000

4500

Total dry matter intake (g)

Figure 6.9. Relationship between total dry matter feed intake (days 5-13 post weaning) and villus height in piglets fed liquid diets for 14 days post weaning (Ward and Moran unpublished data).

It appears that the short inter-meal intervals entrained by the suckling pattern of the sow are important in maintaining the integrity and effectiveness of the piglet’s gut. The behavioural imposition by the sow of short inter-meal intervals may be necessary because of the relative immaturity of the piglet at birth. As discussed previously, when the interval between feeds was increased piglets were unable to consume sufficient nutrients to satisfy their maintenance requirements (Bark et al., 1986). More recently, Thorpe et al.(1998) found that the digestibility of nutrients was dramatically reduced as the interval between feeds increases. Nitrogen digestibility in pigs fed at hourly intervals was double that of pigs fed 2-hourly and five times greater than that of pigs fed 3- or 4-hourly. They also noted that a steady state flow of digesta occurred only when pigs were fed on an hourly basis. In a recent study, Miller (2002 personal communication) recorded the individual feeding patterns of group-housed pigs following weaning at 21 days of age. Analysis of the data demonstrates how misleading conventional statistical treatment of the data can be. The combined data from 48 pigs indicated a smooth transition to solid food following weaning albeit with a large standard deviation (Figure 6.10). The temptation is to assume that the standard deviation represents a range in performance and that individuals within the population behave in a consistent manner. However, a more detailed analysis reveals a very different picture. The postweaning behaviour of one pen of pigs is presented in Figure 6.11. The results are separated into two parts for clarity. These data demonstrate that the apparent smooth transition in Figure 6.10 is actually a statistical artefact, and that there were very large variations in the feeding patterns of individual pigs. Half the pigs in the group (Figure 6.11A) had a peak of intake on Day 2 and then a fall, which had not recovered

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700

Feed intake (g/d)

600 500 400 300 200 100 0

1

3

5

7

9 11 13 15 Days post weaning

17

19

21

Figure 6.10. Feed intake of pigs housed in groups but individually fed using a computerised feeding system (After B Miller 2002, personal communication; with acknowledgement to Parnutt Feeds).

by the end of the first week. Almost half had erratic feed intakes (Figure 6.11B) with peak intakes occurring on days 4, 5 or 6. In this pen of pigs only one pig (broken line) showed the steady increase in feed intake over the first week following weaning that the data in Figure 6.10 might suggest. Given the results of Thorpe et al.(1998), we hypothesize that such large differences in feed intake pattern will have profound effects on the villous architecture, the ecophysiology of the gut and the development of the immune system. A retrospective analysis of data collected in a number of studies at our centre demonstrated a highly significant (P<0.001) effect of dry matter feed intake in the first week post-weaning on the weight of pigs 28 days post-weaning (Geary and Brooks, 1998). The results of this analysis suggest that each 50g per day increase in DM feed intake in the week following weaning increased 28-day post-weaning weight by 870g. Dry matter feed intake in the week post weaning accounted for as much variation in the 28 day post weaning weight as any combination of weaning weight, weaning age, sex and dietary treatment.

6.9

The interaction between water and feed intake post weaning

Voluntary or involuntary deprivation of water post-weaning has serious consequences for the piglet. Gill (1989) showed that it could take more than a week for the weaned piglet to restore its daily fluid intake to the equivalent of that on the day before weaning. Piglets experiencing such reduced fluid intakes can become seriously dehydrated. The resulting disturbance of the pig’s homeostatic balance has

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Factors affecting the voluntary feed intake of the weaned pig

500

A

450 Feed intake (g/d)

400 350 300 250 200 150 100 50 0 1

2

3

4

5

6

7

500 B

Feed intake (g/d)

450 400 350 300 250 200 150 100 50 0 1

2

3

4 5 Days post weaning

6

7

Figure 6.11. The pattern of feed intake in individual pigs, weaned at 21 days of age, housed in a group and fed using a computerised feeding system (After B Miller 2002, personal communication; with acknowledgement to Parnutt Feeds).

important repercussions on its physiology, as does any subsequent, rapid, rehydration that occurs when the pig finally starts drinking. Therefore, it is important to encourage pigs to maintain fluid intake following weaning. Water consumption levels in the five days post-weaning appear to have little relationship with presumed physiological need (Brooks et al., 1984; McLeese et al., 1992). Both overand under-consumption of water will reduce feed intake in the weaned pig; overconsumption by producing physical feelings of satiety, and under-consumption through disruption of the homeostatic balance. There are important behavioural components to post-weaning water intake that must not be underestimated. Pigs that have learned to eat and drink will minimise

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their intake of water per unit of feed (water to feed ratio) when fed ad libitum and, when they are restrict fed, will take additional water to produce feelings of satiety (Yang et al., 1981; Yang et al., 1984). Suckling pigs have been conditioned to consume milk to satisfy their needs for total volumetric fill, and in the early post-weaning period may fail to discriminate between the separate drives of hunger and thirst. Consequently, they consume water to provide gut fill. Having been used to a liquid diet they may mistakenly believe that water is also a source of nutrients. The weaned pig also has to learn to locate water. Piglets may find some difficulty identifying nipple drinkers as a supply of water. However, there is little evidence that providing water drinkers that drip encourages water consumption (Ogunbameru et al., 1991). Providing readily available water in a bowl has been shown to encourage water consumption and increase feed intake (English et al., 1981). If bowls are used, their management is critical, as fouling may reduce the palatability and consumption of water (Brooks and Carpenter, 1990; Phillips and Phillips, 1999; Sorensen et al., 1994). Some UK producers are now using bell-shaped turkey drinkers to water newly weaned pigs. They claim that these drinkers encourage water consumption because the suspended drinker attracts the attention of the piglet and the free water surface encourages exploration and subsequent consumption. Although there appears to be no research data to support these claims, performance on commercial units has been improved by the use of this type of drinker in the immediate post-weaning period. Drinker design and positioning can influence the acquisition of water post-weaning and can affect both piglet performance and water use (Table 6.8). It is most important to position nipple drinkers correctly. Drinkers placed at the incorrect height and angle or in an appropriate part of the pen will inhibit intake. Building designs that provide a warm kennelled area for sleeping and a cooler (cold) area where the pigs feed, drink and eliminate are particularly problematic. The necessity to leave a warm

Table 6.8. Water use by weaned piglets from 3 to 6 weeks of age, provided with water from five different drinker types (After Gill, 1989). Drinker type

Daily gain (g)

Water to feed ratio (l/kg)

Water to weight ratio (l/kg LW)

Mono-flo nipple Arato 76 nipple Lubing bite type I Lubing bite type II Alvin bowl

199b 260a 213b 221b 224ab

5.32 3.23 3.68 2.90 3.49

0.23 0.13 0.12 0.13 0.14

a, b Means

104

with the same superscript are not significantly different (P>0.05)

Weaning the pig

Factors affecting the voluntary feed intake of the weaned pig

environment and go to a colder area to feed or drink will inhibit these behaviours. The limited data available on the effects of water temperature on consumption indicates that, as might be expected, warm water encourages consumption in cold environmental conditions and cold water encourages consumption at high ambient temperatures (Standing Committee on Agriculture; Pig Subcommittee). In the weaned pig, the rate and velocity of the water delivered by the drinker affects feed intake and performance (Table 6.9). Nipple drinkers with a restricted flow rate significantly affected both water and food intake with consequent effects on the performance of pigs weaned at 21 days of age (Barber et al., 1989). The interesting observation in this study was that pigs given drinkers with low flow rates would not increase the amount of time that they spent drinking in order to optimise their intake. In a study involving somewhat older pigs, drinking times were extended, but they still did not increase the time spent drinking sufficiently to compensate for the restricted intake (Nienaber and Hahn, 1984). In another study, increasing water flow rate from 70 to 700 ml/min did not increase the performance of pigs weaned at 28 days of age (Celis, 1996). In the study of Barber et al. (1989), pigs provided with water at the lowest flow rate spent only 268 seconds per day drinking. This is similar to the 290 seconds1 per day that they would have spent actively drinking milk when suckled by the sow. These results suggest a degree of activity scheduling by the pig, once again conditioned by the behavioural patterns imposed by the sow during suckling. This becomes less stringent as the pig increases in age and becomes more familiar with food and water. 1

Calculated on the basis that at in the third week of lactation sows would nurse their piglets 25-29

times per day and the milk ejection per suckling event lasts for 10-20 seconds.

Table 6.9. The effects of water delivery rate on the voluntary food intake and water use of weaned pigs (After Barber et al., 1989). Water delivery rate (ml/ minute)

Daily feed intake (g) Daily gain (g) FCR Daily water used (l) Time spent drinking (sec./d) a, b, c, d Means

175

350

450

700

SEd

303c 210c 1.48 0.78d 268b

323b 235b 1.39 1.04c 176a

341a 250a 1.37 1.32b 175a

347a 247a 1.42 1.63a 139a

3.68 5.57 0.03 0.01 14.4

with the same superscript are not significantly different (P>0.05)

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It is clear from the above that the amount of food that the piglet will eat is determined by the amount of water that it consumes and not the reverse. Therefore, strategies that increase water consumption may have a positive effect on feed intake. Responses may be variable. For example, Maenz et al. (1993) found no improvement in water intake when a commercial sweetener was added to water. However, if water has a poor taste, the addition of flavourings or sweeteners may encourage greater water consumption and hence food intake. Perversely, if the water has good taste characteristics, the addition of a flavour or sweetener may encourage over-consumption of water to the detriment of feed intake (Table 6.10). Barber (1992) offered weaned pigs water containing two sweetener/flavour products from nipple drinkers for the first three days post-weaning and found that it increased the average number of visits to the drinker in the first hour post weaning from 4 to 10 but did not significantly affect the number of visits made subsequently. Where facilities exist to make additions to the water it may be desirable to use a product of this type on the day of weaning to help the pigs locate and start using the water supply. Because water flavour is so variable, it will be necessary to experiment on the individual farm to determine whether promoting water intake increases feed intake or results in the pig over-consuming water at the expense of feed intake.

Table 6.10. Effect on water and feed intake of including a sweetener in the drinking water of 21 day old weaners for the first three days after weaning (After Barber, 1992). Control

Palasweet™

Palasweet Plus™

SEM

Water intake (L/pig) Days 1-3 Days 4-7 Days 8-16

1.23a 1.99a 6.99

1.63b 2.25ab 7.30

1.65b 2.62b 7.51

0.09 0.12 0.39

Feed intake (g/pig) Days 1-3 Days 4-7 Days 8-16

414a 721 2580

314b 728 2214

283b 691 2434

21 34 112

a, b

Means with the same superscript are not significantly different (P>0.05)

6.10

Liquid feeding post-weaning

The case for liquid feeding young pigs has been reviewed recently (Brooks et al., 2001) so only a brief summary is included here, focussing on the behavioural aspects of this method of feeding.

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In view of the problems that the piglet has in discriminating hunger and thirst it might be anticipated that post-weaning performance would be improved by offering a liquid diet. Liquid feeding has potential advantages because: -

• It provides a diet with a dry matter concentration more like that of sow milk and more like the solid food that the pig would encounter in the wild. This might encourage intake and maintain continuity of nutrient supply. • It provides a diet that more closely meets the piglet’s need for both nutrients and water. • It overcomes some of the problems posed by the piglets having to learn to satisfy their drives of hunger and thirst separately. Until relatively recently, liquid feeding was confined to the use of milk replacer for the artificial rearing of pigs or for pigs weaned at very young ages. In this context, and with good hygiene, it has been demonstrated that pigs will grow faster on liquid diets than they will on the sow (Odle and Harrell, 1998) Liquid feeding has been limited in application because of the problems in maintaining the feed in a wholesome and palatable form. However, developments in delivery systems had resulted in renewed interest in the approach. If feed hygiene can be maintained, feed intake and growth of weaners is increased by feeding liquid diets and further improved by feeding fermented liquid diets (Table 6.11). The greatest benefits were obtained in the week immediately following weaning where dry matter intake and growth rate are improved by 20-30% (Kim et al., 2001; Russell et al., 1996). Importantly, the acceleration of early growth is maintained to market weight (Kim et al., 2001). Pig producers have been encouraged to offer pigs a liquid ‘porridge’ or ‘gruel’ in addition to dry feed in the immediate post weaning period. Experimental data on this is sparse and contradictory. In one study (Beattie et al., 1999), feed intake in

Table 6.11. Improvement (%) in growth rate and food conversion ratio in experiments in which the performance of pigs fed dry feed (DF), liquid feed (LF) or fermented liquid feed (FLF) was compared (From the review of Jensen and Mikkelsen, 1998). No. of trials

LF v. DF 10 FLF v. DF 4 FLF v. LF 3

Improved daily weight gain

Improved food conversion ratio

Mean ± SD

Range

Mean ± SD

Range

12.3 ± 9.4 22.3 ± 13.2 13.4 ± 7.1

-7.5 - 34.2 9.2 - 43.8 5.7 - 22.9

-4.1 ± 11.8 -10.9 ± 19.7 -1.4 ± 2.4

-32.6 - 10.1 -44.3 - 5.8 -4.8 - 0.6

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the 2 days following weaning was improved by offering additional wet feed in an easily accessible trough increased, but growth performance was not improved over the 3 week post-weaning period. In another study, Dunshea et al. (2000) provided weaned pigs with supplemental fermented milk for 8 days after weaning and reported significantly increased growth rates and pigs that were 20% heavier at 42 days of age. In our own studies, the growth rate of pigs offered fermented liquid feed in addition to dry feed was intermediate between that of pigs offered either a dry or a liquid diets (Brooks et al., 2001). An important observation in this study was that, compared with the pigs offered liquid or dry diets, more of the pigs offered a choice of diets engaged in antisocial behaviours such as belly-nosing. Given the previous discussion it is clear that it may not be a sensible approach to offer both dry and liquid diets. The weaned pig already has the challenge of learning to differentiate between hunger and thirst and recognising that food and water will satisfy these needs. Providing it with water, food and a third option of wet feed is likely to hamper this learning process not accelerate it.

6.11

Conclusions

From the discussion above, it is clear that a wide range of different factors affect the behaviour of the newly weaned pig and many of these impact directly or indirectly on its ability to find feed and water (see summary Table 6.12). In addition, either through lack of experience, or because its homeostatic control mechanisms have not matured, the piglet can fail to satisfy its physiological requirements for water and/or nutrients. Thus, the theoretical models of voluntary food intake that we would employ to describe the control of intake of food and water in pigs with mature homeostatic mechanisms have no value when trying to explain the phenomena observed in the period immediately post-weaning when pigs are weaning at 5 weeks of age or less. Our attempts to improve performance of the newly weaned pig need to focus on the development of management strategies that will increase the independence of the weaned pig from its dam and increase its exploratory behaviour. In this context we may need to concentrate on the effects that pre-weaning environment can have on equipping the pig to cope with the changes it faces at weaning. Recent reports have shown that the housing experienced by sows may affect the behaviour of their piglets (Beattie et al., 1996), that enriched environments increase piglet activity (Beattie et al., 1994), and that piglets from outdoor farrowing systems feed more frequently than pigs from confinement systems (Cox and Cooper, 2001; Webster and Dawkins, 2000). These findings may point the way forward, suggesting as they do that more diverse and stimulating environments encourage the development of exploratory skills that may assist the piglet in making the transition to independence.

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Factors affecting the voluntary feed intake of the weaned pig

Table 6.12. Summary of factors affecting feed and water intake in weaned pigs (2128 days of age). Factors adversely affecting feed intake in the newly-weaned pig

Factors adversely affecting water intake in the newly-weaned pig

Lack of previous experience of eating solid food and/or drinking. (Underdeveloped feeding, drinking and exploratory behaviour). Inability to discriminate between hunger and thirst. Inability to find food or water (unfamiliar feed and water presentation). Cold conditions (pigs huddle rather than actively seeking food or water). Hot conditions (pigs rest rather than actively seeking food or water). Agonistic behaviour (fighting in mixed pigs displaces other behaviours). Lack of feeding stimulus . (no sow vocalisations)

Water quality (flavour, mineral content, microbiology).

Palatability (taste, smell, texture, freshness, nutrient balance).

Water temperature (cold water reduces intake in cold conditions, hot water reduces intake in hot conditions).

Feed availability (accessibility of feeding places).

Water availability (accessibility of drinkers, flow rate).

Inadequate or excessive water intake

What is not clear from the literature is whether we should be encouraging the weaned pig to develop individual foraging behaviour, or reinforcing synchronous group feeding as a way of ensuring that all piglets in a cohort make a successful transition to solid food. The answer to this question may differ according to the weaning age and hence the ease with which modifications can be made to entrained behaviour. This fundamental question needs answering. Without a satisfactory answer, it is not possible to specify feeding and watering equipment or to devise management systems that will optimise the performance of all the individuals within a group.

References Algers, B. and P. Jensen, 1991. Teat stimulation and milk-production during early lactation in sows - effects of continuous noise. Canadian Journal of Animal Science 71, 51-60. Algers, B., P. Jensen and L. Steinwall, 1990. Behaviour and weight changes at weaning and regrouping of pigs in relation to teat quality. Applied Animal Behavioural Science 26, 143-155.

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Appleby, M.C., E.A. Pajor and D. Fraser, 1991. Effects of management options on creep feeding by piglets. Animal Production 53, 361-366. Appleby, M.C., E.A. Pajor and D. Fraser, 1992. Individual variation in feeding and growth of piglets - effects of increased access to creep food. Animal Production 55, 147-152. Arey, D.S. and E.S. Sancha, 1996. Behaviour and productivity of sows and piglets in a family system and in farrowing pens. Applied Animal Behavioural Science 50, 135-145. Auldist, D.E. and R.H. King, 1995. Piglets’ role in determining milk production in the sow. In: 5th Biennial Conference of the Australasian Pig Science Association. Australasian Pig Science Association, Werribee, Australia. pp. 114-118. Azain, M.J., T. Tomkins, J.S. Sowinski, R.A. Arentson and D.E. Jewell, 1996. Effect of supplemental pig milk replacer on litter performance: Seasonal variation in response. Journal of Animal Science 74, 2195-2202. Baber, D.W. and B.E. Coblenz, 1987. Diet, nutrition and conception in feral pigs on Santa Catalina island. Journal of Wildlife Management 51, 306-317. Barber, J., 1992. The rationalisation of drinking water supplies for pig housing. PhD, University of Plymouth, UK. Barber, J., P.H. Brooks and J.L. Carpenter, 1989. The effects of water delivery rate on the voluntary food intake, water use and performance of early-weaned pigs from 3 to 6 weeks of age. In: J.M. Forbes, M.A. Varley, T.L.J. Lawrence, H. Davies and M.C. Pitkethly, (eds). The voluntary feed intake of pigs. pp. 103-104. British Society of Animal Production, Edinburgh. Barber, R.S., R. Braude and K.G. Mitchell, 1955. Studies on milk production of Large White pigs. Journal of Agricultural Science 46, 97-118. Bark, L.J., T.D. Crenshaw and V.D. Leibbrandt, 1986. The effect of meal intervals and weaning on feed-intake of early weaned pigs. Journal of Animal Science 62, 1233-1239. Beattie, V.E., N. Walker and I.A. Sneddon, 1994. Effects of early environment on the behaviour of the pig. Animal Production 58, 476 (Abstr.). Beattie, V.E., N. Walker and I.A. Sneddon, 1996. Influence of maternal experience on pig behaviour. Applied Animal Behavioural Science 46, 159-166. Beattie, V.E., R.N. Weatherup and D.J. Kilpatrick, 1999. The effect of providing additional feed in a highly accessible trough on feeding behaviour and growth performance of weaned pigs. Irish Journal of Agricultural and Food Research 38, 209-216. Benevenga, N.J., F.R. Greer and T.D. Crenshaw, 1990. What is the growth potential of the runt pig? Wisconsin Swine Day Report. pp. 4-6. Bøe, K., 1991. The process of weaning in pigs - when the Sow decides. Applied Animal Behavioural Science 30, 47-59. Bøe, K. and P. Jensen, 1995. Individual-differences in suckling and solid food-intake by piglets. Applied Animal Behavioural Science 42, 183-192. Braude, R., K.G. Mitchell, M.J. Newport and J.W.G. Porter, 1970. Artificial rearing of pigs: 1. Effect of frequency and level of feeding on performance and digestion of milk proteins. British Journal of Nutrition 24, 501-516. Brooks, P.H. and J.L. Carpenter, 1990. The water requirement of growing-finishing pigs - theoretical and practical considerations. In: W. Haresign and D.J.A. Cole, (eds). Recent Advances in Animal Nutrition. pp. 115-136. Butterworths, London.

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Brooks, P.H. and J. Burke, 1998. Behaviour of sows and piglets during lactation. In: M. Verstegen, J. Schrama and P. Moughan, (eds). The Lactating Sow. pp. 299-336. Wageningen Pers, Wageningen. Brooks, P.H. and B. van Zuylen, 1998. The effect of feeding a fermented liquid diet to suckling pigs on their pre- and post-weaning performance and the effect of weaning weight on post weaning performance. In: J.A.M. van Arendonk, V. Ducrocq, Y. van der Honing, F. Madec, T. van der Lende, D. Puller, J. Folch, E.W. Fernandez and E.W. Bruns, (eds). Book of Abstracts of the 49th meeting of the European Association of Animal Production. Warsaw 24th-29th August. pp. 268 (abs). Wageningen Pers, Wageningen. Brooks, P.H., S.J. Russell and J.L. Carpenter, 1984. Water intake of weaned piglets from three to seven weeks old. Veterinary Record 115, 513-515. Brooks, P.H., C.A. Moran, J.D. Beal, V. Demeckova and A. Campbell, 2001. Liquid feeding for the young pig. In: M.A. Varley and J. Wiseman, (eds). The weaner pig; Nutrition and management. CABI Publishing, Wallingford. Bruininx, E.M.A.M., C.M.C. van der Peet-Schering, J.W. Schrama, L.A. den Hartog, H. Everts and A.C. Beynen, 2001a. The IVOG feeding station: A tool for monitoring the individual feed intake of group-housed weaniling pigs. Journal of Animal Physiology and Animal Nutrition 85, 8187. Bruininx, E.M.A.M., C.M.C. van der Peet-Schering, J.W. Schrama, P.F.G. Vereijken, P.C. Vesseur, H. Everts, L.A. den Hartog and A.C. Beynen, 2001b. Individually measured feed intake characteristics and growth performance of group-housed weanling pigs: Effects of sex, initial body weight, and body weight distribution within groups. Journal of Animal Science 79, 301-308. Campbell, R.G., 1976. A note on the use of a feed flavour to stimulate the feed intake of weaner pigs. Animal Production 23, 417 - 419. Castren, H., B. Algers, P. Jensen and H. Saloniemi, 1989. Suckling behaviour and milk consumption in new born piglets as a response to sow grunting. Applied Animal Behavioural Science 24, 227-238. Celis, J.E., 1996. Effect of water restriction on performance of nursery pigs. Agribiological Research-Z. Agrarbiol. Agrik.chem. Okol. 49, 150-156. Conway, P.L., 1966. Development of intestinal microbiota. In: R.E. Isaacson, (ed.) Gastointestinal microbiology. Volume 2. Gastrointestinal microbes and host interactions. pp. 3-39, Vol. 2. Chapman and Hall, London. Cox, L.N. and J.J. Cooper, 2001. Observations on the pre- and post-weaning behaviour of piglets reared in commercial indoor and outdoor environments. Animal Science 72, 75-86. Cronin, G.M., E. Leeson, J.G. Cronin and J.L. Barnett, 2001. The effect of broadcasting sow suckling grunts in the lactation shed on piglet growth. Asian-Australasian Journal of Animal Science 14, 1019-1023. Csermely, D. and D.G.M. Woodgush, 1981. Artificial stimulation of ingestive behavior in earlyweaned piglets. Biology of Behaviour 6, 159-165. de Passille, A.M.B. and J. Rushen, 1989. Suckling and teat disputes by neonatal piglets. Applied Animal Behavioural Science 22, 23-38. Delumeau, O. and M.C. Meunier-Salaün, 1995. Effect of early trough familiarity on the creep feeding behaviour in suckling piglets and after weaning. Behavioural Processes 34, 185-196.

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Deprez, P., P. Deroose, C. van den Hende, E. Muylle and W. Oyaert, 1987. Liquid versus dry feeding in weaned piglets: The influence on small intestinal morphology. Journal of Veterinary Medicine 34, 254-249. Dunshea, F.R., D.J. Kerton, P.J. Eason and R.H. King, 2000. Supplemental fermented milk increases growth performance of early-weaned pigs. Asian-Australasian Journal of Animal Science 13, 511-515. Ellendorff, F., M.I. Forsling and D.A. Poulain, 1982. The milk ejection reflex in the pig. Journal of Physiology-London 333, 577-594. English, P.R., P.M. Anderson, F.M. Davidson and M.F.M. Dias, 1981. A study of the value of readily available liquid supplements for early-weaned pigs. Animal Production 32, 395-396. Forkman, B., I.L. Furuhaug and P. Jensen, 1995. Personality, coping patterns and aggression in piglets. Applied Animal Behavioural Science 45, 31-42. Fraser, D., 1980. A review of the behavioural mechanism of milk ejection of the domestic pig. Applied Animal Ethology 6, 247-255. Fraser, D. and R. Morley-Jones, 1975. The ‘teat-order’ of suckling pigs. 1. Relation to birth weight and subsequent growth. Journal of Agricultural Science 84, 387-391. Fraser, D. and B.K. Thompson, 1986. Variation in piglet weights - relationship to suckling behavior, parity number and farrowing crate design. Canadian Journal of Animal Science 66, 31-46. Fraser, D., J.J.R. Feddes and E.A. Pajor, 1994. The relationship between creep feeding-behaviour of piglets and adaptation to weaning - effect of diet quality. Canadian Journal of Animal Science 74, 1-6. Friend, D.W. and H.M. Cunningham, 1966. The effect of water consumption on the growth, feed intake, and carcass composition of suckling pigs. Canadian Journal of Animal Science 46, 203209. Geary, T.M. and P.H. Brooks, 1998. The effect of weaning weight and age on the post-weaning growth performance of piglets fed fermented liquid diets. Pig Journal 42, 10-23. Gill, B.P., 1989. Water use by pigs managed under various conditions of housing, feeding and nutrition. Ph.D. Thesis, University of Plymouth. Gill, B.P., P.H. Brooks and J.L. Carpenter, 1991. The effects of water and creep food provision on the performance of sucking piglets. Animal Production 52, 599 (Abstr.). Giroux, S., G.P. Martineau and S. Robert, 2000. Relationships between individual behavioural traits and post- weaning growth in segregated early-weaned piglets. Applied Animal Behavioural Science 70, 41-48. Gustafsson, M., P. Jensen, F.H. de Jonge, G. Illmann and M. Spinka, 1999. Maternal behaviour of domestic sows and crosses between domestic sows and wild boar. Applied Animal Behavioural Science 65, 29-42. Harrell, R.J., M.J. Thomas and R.D. Boyd, 1993. Limitations of sow milk yield on baby pig growth. In: Proceedings of the Cornell Nutrition Conference for Feed Manufacturers, Ithaca New York U.S.A. Department of Animal Science, Cornell University. pp. 156-164. Hessing, M.J.C., A.M. Hagelso, J.A.M. Vanbeek, P.R. Wiepkema, W.G.P. Schouten and R. Krukow, 1993. Individual behavioral-characteristics in pigs. Applied Animal Behavioural Science 37, 285-295.

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Horrell, I., 1997. The characterisation of suckling in wild boar. Applied Animal Behavioural Science 53, 271-277. Jensen, B.B. and L.L. Mikkelsen, 1998. Feeding liquid diets to pigs. In: P.C. Garnsworthy and J. Wiseman, (eds). Recent Advances in Animal Nutrition 1998. pp. 107-126. Nottingham University Press, Thrumpton, Nottingham. Jensen, P., 1986. Observations on the maternal-behavior of free-ranging domestic pigs. Applied Animal Behavioural Science 16, 131-142. Jensen, P., 1995. The weaning process of free-ranging domestic pigs: Within- and between-litter variations. Ethology 100, 14-25. Jensen, P. and I. Redbo, 1987. Behavior during nest leaving in free-ranging domestic pigs. Applied Animal Behavioural Science 18, 355-362. Jensen, P. and B. Recen, 1989. When to wean - observations from free-ranging domestic pigs. Applied Animal Behavioural Science 23, 49-60. Jensen, P., J. Rushen and B. Forkman, 1995a. Behavioral strategies or just individual variation in behavior - a lack of evidence for active and passive piglets. Applied Animal Behavioural Science 43, 135-139. Jensen, P., B. Forkman, K. Thodberg and E. Koster, 1995b. Individual variation and consistency in piglet behavior. Applied Animal Behavioural Science 45, 43-52. Kabuga, J.D. and S.Y. Annor, 1992. A note on the development of behaviour of intensively managed piglets in the humid tropics. Animal Production 54, 157-159. Kasanen, S. and B. Algers, 2002. A note on the effects of additional sow gruntings on suckling behaviour in piglets. Applied Animal Behavioural Science 75, 93-101. Kavanagh, S., P.B. Lynch, P.J. Caffrey and W.D. Henry, 1995. Creep-feed intake by suckling pigs. Irish Journal of Agricultural and Food Research 34, 87 (Abstr.). Keeling, L.J. and J.F. Hurnik, 1996. Social facilitiation and synchronization of eating between familiar and unfamiliar newly weaned piglets. Acta Agriculturae Scandinavica 46, 54-60. Kelly, D. and T.P. King, 2001. Luminal bacteria: Regulation of gut function and immunity. In: A. Piva, K.E. Bach Knudsen and J.E. Lindberg, (eds). Gut environment of the pig. pp. 113-131. Nottingham University Press, Nottingham. Kidder, D.E. and M.J. Manners, 1978. Digestion in the pig. Scientechnia, Bristol. Kim, J.H., K.N. Heo, J. Odle, I.K. Han and R.J. Harrell, 2001. Liquid diets accelerate the growth of early-weaned pigs and the effects are maintained to market weight. Journal of Animal Science 79, 427-434. Lewis, N.J. and J.F. Hurnik, 1985. The development of nursing behaviour in swine. Applied Animal Behavioural Science 14, 225-232. Lewis, N.J. and J.F. Hurnik, 1986. An approach response of piglets to the sows nursing vocalisations. Canadian Journal of Animal Science 66, 537-539. Mackenzie, D.D.S. and D.K. Revell, 1998. Genetic influences on milk quality. In: M. Verstegen, J. Schrama and P. Moughan, (eds). The Lactating Sow. pp. 97-112. Wageningen Pers, Wageningen. Maenz, D.D., J.F. Patience and M.S. Wolynetz, 1993. Effect of water sweetener on the performance of newly weaned pigs offered medicated and unmedicated feed. Canadian Journal of Animal Science 73, 669-672.

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McBride, G., 1963. The ‘teat order’ and communication in young pigs. Animal Behaviour 11, 5356. McLeese, J.M., M.L. Tremblay, J.F. Patience and G.I. Christison, 1992. Water-intake patterns in the weanling pig - effect of water-quality, antibiotics and probiotics. Animal Production 54, 135142. Mennella, J.A. and G.K. Beauchamp, 1991. Maternal diet alters the sensory qualities of humanmilk and the nurslings behavior. Pediatrics 88, 737-744. Mennella, J.A. and G.K. Beauchamp, 1993. The effects of repeated exposure to garlic-flavored milk on the nurslings behavior. Pediatric Research 34, 805-808. Mennella, J.A., C.P. Jagnow and G.K. Beauchamp, 2001. Prenatal and postnatal flavor learning by human infants. Pediatrics 107, U11-U16. Metz, J.H.M. and H.W. Gonyou, 1990. Effect of age and housing conditions on the behavioural and haemolytic reaction piglets to weaning. Applied Animal Behavioural Science 27, 299-309. Morgan, C.A., A.B. Lawrence, J. Chirnside and L.A. Deans, 2001. Can information about solid food be transmitted from one piglet to another? Animal Science 73, 471-478. Nabuurs, M.J.A., A. Hoogendoorn and A. VanZijderveldVanBemmel, 1996. Effect of supplementary feeding during the sucking period on net absorption from the small intestine of weaned pigs. Research in Veterinary Science 61, 72-77. Nagai, M., K. Hachimura and K. Takahashi, 1994. Water-consumption in suckling pigs. Journal of Veterinary Medicine Science 56, 181-183. Newberry, R.C. and D.G.M. Wood-Gush, 1984. The suckling behaviour of domestic pigs in a seminatural environment. Behaviour 95, 11-25. Newberry, R.C. and D.G.M. Wood-Gush, 1985. The suckling behaviour of domestic pigs in a seminatural environment. Behaviour 95, 11-25. Nicol, C.J. and S.J. Pope, 1994. Social-learning in sibling pigs. Applied Animal Behavioural Science 40, 31-43. Nienaber, J.A. and G.L. Hahn, 1984. Effects of water-flow restriction and environmental-factors on performance of nursery-age pigs. Journal of Animal Science 59, 1423-1429. Odle, J. and R.J. Harrell, 1998. Nutritional approaches for improving neonatal piglet performance: Is there a place for liquid diets in commercial production? Review. Asian-Australasian Journal of Animal Science 11, 774-780. Ogunbameru, B.O., E.T. Kornegay and C.M. Wood, 1991. A comparison of drip and non-drip nipple waterers used by weanling pigs. Canadian Journal of Animal Science 71, 581-583. Pajor, E.A., D. Fraser and D.L. Kramer, 1991. Consumption of solid food by suckling pigs - individual variation and relation to weight-gain. Applied Animal Behavioural Science 32, 139-155. Petersen, V., 1994. The development of feeding and investigatory behavior in free- ranging domestic pigs during their first 18 weeks of life. Applied Animal Behavioural Science 42, 87-98. Petrie, C.L. and H.W. Gonyou, 1988. Effects of auditory, visual and chemical stimuli on the ingestive behavior of newly weaned piglets. Journal of Animal Science 66, 661-668. Phillips, P.A. and M.H. Phillips, 1999. Effect of dispenser on water intake of pigs at weaning. Transactions of the ASAE 42, 1471-1473. Pluske, J.R., I.H. Williams and F.X. Aherne, 1996a. Villous height and crypt depth in piglets in response to increases in the intake of cows’ milk after weaning. Animal Science 62, 145-158.

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Pluske, J.R., I.H. Williams and F.X. Aherne, 1996b. Maintenance of villous height and crypt depth in piglets by providing continuous nutrition after weaning. Animal Science 62, 131-144. Pluske, J.R., D.J. Hampson and I.H. Williams, 1997. Factors influencing the structure and function of the small intestine in the weaned pig: A review. Livestock Production Science 51, 215-236. Puppe, B. and A. Tuchscherer, 1999. Developmental and territorial aspects of suckling behaviour in the domestic pig (sus scrofa f. Domestica). Journal of Zoology 249, 307-313. Puppe, B., M. Tuchscherer, S. Hoy and A. Tuchscherer, 1993. Social-organization structures in intensively kept pigs .1. Ethological investigations on the sucking order. Archiv fur TierzuchtArchives of Animal Breeding 36, 539-550. Rudo, N.D., I.H. Rosenberg and R.W. Wissler, 1976. The effect of partial starvation and glucagon treatment on intestinal villus morphology and cell migration. Proceedings of the Society for Experimental Biology and Medicine 152, 277-280. Russell, P.J., T.M. Geary, P.H. Brooks and A. Campbell, 1996. Performance, water use and effluent output of weaner pigs fed ad libitum with either dry pellets or liquid feed and the role of microbial activity in the liquid feed. Journal of the Science of Food and Agriculture 72, 8-16. Sorensen, M.T., B.B. Jensen and H.D. Poulsen, 1994. Nitrate and pig manure in drinking-water to early weaned piglets and growing pigs. Livestock Production Science 39, 223-227. Spinka, M., G. Illmann, B. Algers and Z. Stetkova, 1997. The role of nursing frequency in milk production in domestic pigs. Journal of Animal Science 75, 197-212. Spitz, F., 1986. Current state of knowledge of wild boar biology. Pig News and Information 7, 171175. Standing Committee on Agriculture; Pig Subcommittee, 1987. Feeding standards for Australian livestock. Pigs. CSIRO, East Melbourne, Victoria, Australia. Steiner, M., H.R. Bourges, L.S. Freedman and S.J. Gray, 1968. Effect of starvation on the tissue composition of the small intestine in the rat. American Journal of Physiology 215, 75-77. Thorpe, J., B.G. Miller and H. Schulze, 1998. The effect of liquid feeding at different feed intervals on ileal digestibility in the early weaned pig. In: J.A.M. van Arendonk, V. Ducrocq, Y. van der Honing, F. Madec, T. van der Lende, D. Puller, J. Folch, E.W. Fernandez and E.W. Bruns, (eds). Book of Abstracts of the 49th meeting of the European Association of Animal Production. Warsaw, Poland. 24th-29th August. pp. 264 (abs). Wageningen Pers, Wageningen. Webster, S. and M. Dawkins, 2000. The post-weaning behaviour of indoor-bred and outdoor-bred pigs. Animal Science 71, 265-271. Wechsler, B. and N. Brodmann, 1996. The synchronisation of nursing bouts in group housed sows. Applied Animal Behavioural Science 47, 191-199. Whittemore, C.T. and D. Fraser, 1974. The nursing and suckling behaviour of pigs. Ii. Vocalisation of the sow in relation to suckling behaviour and milk ejection. British Veterinary Journal 130, 346-356. Yang, T.S., B. Howard and W.V. McFarlane, 1981. Effects of food on drinking behaviour of growing pigs. Applied Animal Ethology 7, 259-270. Yang, T.S., M.A. Price and F.X. Aherne, 1984. The effect of level of feeding on water turnover in growing pigs. Applied Animal Behavioural Science 12, 103-109. Zabielski, R., 1998. Regulatory peptides in milk, food and in the gastrointestinal lumen of young animals and children. Journal of Animal and Feed Sciences 7, 65-78.

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Zijlstra, R.T., K.Y. Whang, R.A. Easter and J. Odle, 1996. Effect of feeding a milk replacer to earlyweaned pigs on growth, body composition, and small intestinal morphology, compared with suckled littermates. Journal of Animal Science 74, 2948-2959.

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7

Digestive physiology of the weaned pig H.M. Miller and R.D. Slade

Summary Descriptions of the changes in piglet digestive physiology following weaning abound in the literature to such an extent that review of the subject is suited more to a dedicated book than just this one chapter. Accordingly we have attempted to draw the literature together into a brief yet cohesive analysis of intestinal events pre and post-weaning. In doing so we have encapsulated conventional opinion whilst endeavouring to introduce novel or poorly documented perspectives. We hope that this review will help to provoke thought and stimulate continuing innovative research in this fascinating area.

7.1

Introduction

Profound changes in piglet digestive physiology occur following weaning as the piglet gut adapts to the change in feed type. In wild pigs these changes would occur progressively over time as the piglet made a gradual transition from a wholly milk diet to a wholly non-milk diet, the piglets finally achieving nutritional independence from the sow at about 8 to 12 weeks of age. However in the commercial situation piglets are weaned suddenly and uncompromisingly by removal from the sow and her milk supply at 14 to 28 days of age. Although highly digestible diets are supplied to the newly weaned piglet, such weaning practice is invariably associated with a dramatic reduction in feed intake, which in turn is associated with rapid changes in gut structure and function and reduced overall growth rate. Whilst traditionally the effects of sudden early weaning have been compared with delayed weaning (35 to 42 days) or gradual weaning in the continuing presence of the sow, such a dramatic change in piglet diet is not without precedent. At birth the piglet must face a symphony of changes in which the successful switch from placental to enteral nutrition plays a key role. Although the gut has had the whole of gestation to develop a structure suitable for enteral nutrition, extensive functional changes have to occur within hours of birth to enable adequate digestion and absorption. This adaptation to enteral nutrition at birth is accomplished with an alacrity that is markedly absent in the commercial weaning situation. In this review we will discuss the changes in gut structure and function that occur with current commercial weaning practice. In addition to describing how these changes may be affected by age at weaning we have also compared them with the developmental strategies of the neonatal pig. We hope that this may help us to understand regulation of postweaning events and thereby improve our ability to counteract the characteristic post-weaning check in piglet growth. Where appropriate

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we have also made comparisons with digestive development in other species, however distinctive differences in gestational, post-natal and post-weaning development between the pig (precocial) and altrical species (eg. rat, mouse and rabbit) prohibit generalised comparisons of their digestive physiology. In addition, the pig has frequently been used as a model for human research because of the homogeneity of anatomy, physiology, nutrition and metabolism across the two species (Moughan et al., 1992; Wykes et al., 1993; Ball et al., 1995). Just as the pig is regarded as a good model for the human we likewise consider the human to be a good model for the pig and therefore, where research progress in human infant digestive physiology exceeds that made in the pig, a cautious paralleling of developmental aspects of the two species has been made.

7.2

Strategies for adaptation to enteral nutrition in the neonatal pig

The rapid changes in the structure and function of the digestive tract that are triggered by weaning undoubtedly result in a transient period of sub optimal digestive competence. Let us first consider how similar problems are resolved in the neonate. 7.2.1

Preparation

During gestation the complex multicellular systems required for postnatal nutrition develop progressively (Zabielski et al., 1999) so that by the time of birth the architecture and mechanisms required for extra-uterine life are already established. Differentiation of the gut into individual recognisable organs is complete early in gestation. Thereafter refinement of the structure and development of digestive and absorptive systems must take place. Fetal and neonatal gastric development in pigs are described in recent reviews by Sangild et al. (2000) and Xu et al. (2000). Prenatal growth of the stomach is similar to whole body growth. Gastric fluid pH (important for bacterial suppression and activation of gastric zymogens) gradually reduces during gestation to reach 2-4 at birth. These reductions are paralleled by increases in both intrinsic factor in the gastric fundus, and gastrin. Development of proteolytic capability coincides with birth and is evidenced initially by activity of milk clotting chymosins and, with increasing age, by the general proteolytic activity of pepsins. Immediately post-partum, growth of the stomach exceeds that of the whole body, its mass increasing approximately two-fold from birth to 7 days of age (doa). Gastric acid secretory capacity doubles during the 24 hours following birth (presumably secretagogue stimulated) and again between 1 and 3 doa. This reflects augmentation of the gastric tissue and increased gastric gland oxyntic cell volume density and

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HCl secretory capacity per unit of tissue mass. Gastric proteolytic competence also develops rapidly after birth with protease secretory capacity enhanced 9-fold by 7 doa. Structural development and cytodifferentiation of the fetal intestinal mucosa follow a highly organised temporal pattern. Briefly, villi forming from the presumptive small intestine mucosa are separated one from another by distinct regions of proliferating cells termed primordial crypts. Subsequently, primordial crypt cells invade the underlying mesenchyme to form crypt cell regions. Cells produced in the crypt regions differentiate and mature as they migrate along the crypt to villus axis. Thus, villus form and function emerge during fetal development. For example, mechanisms for amino acid transport have been detected in porcine fetal villus enterocytes as early as 40% gestation (Buddington and Malo, 1996). Rate of amino acid absorption increases as gestation progresses and rapidly immediately prior to birth (Buddington et al., 2001), suggesting that the transport mechanisms continue to be upregulated as gestation proceeds. Similarly, capacities for carbohydrate digestion and absorption are already established at birth (Manners and Stevens, 1972; Puchal and Buddington, 1992). Following resolution of villus structure and enterocyte differentiation, ingestion of amniotic fluid is thought to contribute significantly toward gastro intestinal growth (Buddington, 1993; Buddington et al., 2001) and may have positive priming effects on post-partum enterocyte competence. Thus fundamental mucosal characteristics associated with enteral nutrition are fully developed prior to birth. Prenatal development of enzyme activities is not limited to intestinal tissues alone. Pancreatic enzyme activities increase as gestation progresses (Westrom et al., 1987) and appear to be maximal by the end of gestation, as demonstrated for elastase II (Gestin et al., 1997a) and chymotrypsin (Gestin et al., 1997b). There is little discussion of prenatal development of the porcine colon in the literature. The colon functions to absorb water and electrolytes, and this function appears developed in the neonate. Conservation of dietary carbohydrate (CHO) through the action of colonic bacteria relies on inoculation with the appropriate microbial population since the intestinal tract will be sterile at birth. In early life, bacteria whose substrate is lactose would be necessary for this function, although efficient digestion and absorption in the upper gastrointestinal tract (GIT) may significantly limit the necessity for such bacterial activity. Measurements in the human neonate indicate the small intestine (SI) is incapable of hydrolyzing and absorbing all dietary lactose, thus the colon may play a role in CHO conservation. Murray et al. (1991) studied conceivable routes of colonic energy retrieval from bypass dietary lactose, including mucosal metabolism and absorption as well as bacterial degradation to SCFA and subsequent absorption. Their studies indicate that in the neonatal pig lactose may be directly absorbed by colonocytes in the

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disaccharide form. The peri-natal colon is able to absorb electrolytes and amino acids (see for example Henin and Smith, 1976; Sepulveda and Smith, 1979). However we were unable to find any information describing prenatal development or activity of these functions. It is apparent that at birth the young piglet potentially has all the digestive equipment to start extra-uterine life but the system now requires activation and fine-tuning. Colostrum intake provides the activation signal required. 7.2.2

Implementation I

Colostrum stimulates intensive growth of the neonatal pig’s stomach, pancreas and small intestine within 24 hours of intake (Zabielski et al., 1999). Mucosal growth is characterised by increased DNA synthesis, an increase in protein content (Zhang et al., 1997), and a decrease in cell turnover (Moon and Joel, 1975). This is accompanied by marked expansion of villi and microvilli surface areas (Xu et al., 1992). These changes are thought to be initiated and regulated by intrinsic growth factors and hormones in the colostrum (Kelly et al., 1992; Buddington, 1993; Pacha, 2000). Cells produced by the crypts during the perinatal period rapidly replace the fetal villus enterocyte population and this coincides with the onset of changes in villus structural configuration. The finger-like villi gradually shorten and thicken throughout the suckled period (Cera et al., 1988), a process paralleled by reshuffling of hydrolase and nutrient transport activities. After birth there is a decline in amino acid absorption and monosaccharide uptake relative to tissue protein content of the enterocytes. However this is compensated for by rapid mucosal growth (Puchal and Buddington, 1992; Zhang et al., 1998; Buddington et al., 2001), such that overall capacity for nutrient uptake is unaffected or increased slightly (Zhang et al., 1997). Colostrum mediates rapid changes in intestinal hydrolase activity. Zhang et al. (1997, 1998) demonstrated colostrum-induced regional (proximal, mid and distal small intestine) and compartmental (brush border membrane vesicles and mucosal homogenate) modification of the specific activities of hydrolases within 24 hours of birth (Table 7.1). Total intestinal activities of lactase, sucrase, maltase and aminooligopeptidase are higher 24 hours post-partum than at birth, although their activities per unit of intestinal protein decrease (Zhang et al., 1997). Pre-partum endogenous secretion of cortisol is positively implicated in stimulation of these brush-border hydrolases (Sangild et al., 1995; Sangild et al., 2000). Amplification of absolute maltase and sucrase activities within 24 hours of birth is paralleled by increases in fructose transport capacity relative to glucose (Puchal and Buddington, 1992). This may seem surprising for an animal which is receiving an entirely milk

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Table 7.1. Changes from birth in specific (µmol/[min/g protein]) and total hydrolase activities in small intestine mucosa homogenate and brush-border membrane vesicles (BBMV) during the initial 24 hours post-partum. (Adapted from Zhang et al. 1997) Small intestine homogenate

Small intestine BBMV

Region

Proximal

Mid

Distal

Proximal

Mid

Distal

Specific activity Lactase Sucrase Maltase Aminoligopeptidase (AOP)

= = ↓ 6hrs ↓ 6hrs

= ↓ 6hrs ↓ 6hrs ↓ 6hrs

= = ↓ 6hrs =

↓ 6hrs* = = =

= = = =

= = = =

Hours post-partum

6

12

24

6

12

24

Total activity Lactase Sucrase Maltase Aminoligopeptidase (AOP)

↑ = ↑ =

↑ ↑ ↑ =

↑ ↑ ↑ ↑

= = = =

↑ = ↑ ↑

↑ = ↑ ↑

= no significant change in activity ↓↑ significant decrease or increase in activity * decreased at 6 hours, = at 12 hours, decreased at 24 hours

diet, but indicates that the piglet is evolutionally equipped to digest and absorb non-milk as well as milk foods almost immediately after birth. The nascent capacity to digest sucrose and maltose apparently develops independently of luminal exposure to these compounds, but is influenced by feed intake and composition. Zhang et al. (1998) examined intestinal structure and function in piglets 6 hours after birth in response to feed deprivation (FD) or gastric intubation with similar volumes of colostrum (C), milk replacer (MR) or an oral electrolyte solution (OES). In this study, total intestinal maltase activity in mucosal homogenate was elevated in C compared to FD pigs; MR and OES were intermediate but tended to be lower than in C contemporaries. Brush-border membrane vesicle (BBMV) total maltase and aminooligopeptidase activities were greater for C than OES with MR measurements falling between the two: FD values were comparable with MR and OES treatments. Treatment effects on gut morphology were not reported, however intestinal length and nominal surface area (intestinal

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circumference x length) declined in the order C/MR >OES/FD and C > MR/OES > FD respectively. Therefore it appears that intestinal hydrolase activities and intestinal enlargement are stimulated by the physical presence of material in the intestine and that such stimulation is differentially enhanced by the material’s nutritional and/or bioactive composition. Furthermore, the compositional qualities of colostrum appear to initiate development of intestinal characteristics associated with weaned pig digestive physiology. In addition to their role in promoting structural and functional development of the GIT, colostrum and milk provide the piglet with an arsenal of specific and nonspecific biologically active proteins and peptides. These factors mediate interaction between the contents of the intestinal tract and it’s epithelial surface and, subsequent to transmission across the gut wall, provide initial systemic immune protection. Comment on the immunological benefits this confers to the piglet is beyond the scope of this chapter but is addressed elsewhere in this publication. 7.2.3

Perspective 1

The transition from placental to enteral nutrition is immediate and abrupt. For it to be achieved successfully the neonate requires a competent digestive physiology within hours of birth. Three major factors ensure success. First, preliminary morphological adaptation of the tissues necessary for enteral nutrition occurs before birth. Second, development of enzyme and transport systems is pre-emptively targeted toward arrival of a known substrate package (colostrum/milk) within a given timeframe. Third, arrival of the substrate package activates up-regulation of the system and induces changes that fine-tune digestive physiology to the enteral diet. In addition, the substrate package has evolved to meet the nutritional requirement of the neonate completely. The neonate rapidly and effectively resolves the problems of adaptation to the extrauterine diet. However, commercial weaning enforces a second immediate and abrupt change to piglet diet. What are the consequences of this change, and does the piglet contend with this second transition as successfully?

7.3

The weaned pig

Natural weaning is a gradual process rather than the single episode we impose on the piglet commercially. The development of adult digestive physiology initiated by colostrum intake continues progressively during suckling and is more advanced when weaning is delayed (Hampson,1986; Miller et al., 1986; Cera et al., 1988; Kelly et al., 1991). Buddington (1993) suggested that normal progression of postweaning intestinal maturation was regulated by intrinsic timing mechanisms but was also dependent upon transition to the adult diet. This agreed with the

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comment by Kelly et al. (1992) that luminal nutrition has a profound influence on intestinal morphology at all developmental ages but is unlikely to be the ultimate cue for intestinal differentiation. 7.3.1

Commercial weaning

Intestinal maturation of the commercial piglet, weaned at 3 to 4 weeks of age, is compromised on two counts. First, the transition from lactation to adult diets is abrupt rather than progressive. The sudden and vastly different functional requirement this imposes on the intestine often results in profound reduction in nutrient intake (Rantzer et al., 1997; Le Dividich and Seve, 2000) and a transitory (5 d) failure of the piglet to meet its maintenance energy requirement (Pluske et al., 1997). Second, at commercial weaning age the developmental demands placed on the intestine by the change in dietary input generally precede the temporally induced adaptations observed in unweaned piglets by between 2 and 4 weeks. Thus, commercial weaning superimposes our own timetable of events over the natural maturation of the piglet’s digestive physiology instigating severe acceleration of the weaning process and launching the developmental program into a frantic ‘catch-up’ state. To confound this problem further, the piglet simultaneously elects not to eat and therefore becomes severely energy deficient. 7.3.2

Gastrointestinal, pancreatic and hepatic response

Differential growth of the various compartments of the gastrointestinal tract occurs following weaning. Makkink et al. (1994) reported a gradual increase in relative stomach mass (g/kg liveweight) over the 10 days after weaning but a decrease in that of the small intestine during the first three days that was not recovered until day 10. Similar small intestinal responses have been demonstrated by other workers (Cera et al., 1988; Kelly et al., 1991; Jiang et al., 2000) and appear positively related to feed intake (Makkink et al., 1994). In contrast, the relative mass of the large intestine increases rapidly during the early post-weaning period (van Beers-Schreurs et al., 1998), an effect that is independent of age of weaning (Kelly et al., 1991). The growth rates of organs associated with the GIT also change differentially relative to overall body mass following weaning. For example, relative liver mass increases significantly during the second week post-weaning, indicating increased hepatic metabolic activity (Slade and Miller, 2000). Following a period of accelerated growth during the perinatal period, pancreatic weight relative to whole bodyweight stabilises from about 13 doa (Gestin et al., 1997b). However, following weaning, and independent of age, pancreatic growth and protein accretion again become positively allometric (Peng et al., 1996). This second hypertrophic phase of pancreatic development is paralleled by enzyme

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specific changes in biosynthetic function of the organ. Briefly, the activities of chymotrypsin and elastase II relative to body weight decline dramatically, lipase increases slightly and trypsin, amylase and elastase I increase to dominate pancreatic contribution to the digestive process (Gestin et al., 1997a; Gestin et al., 1997b). Pancreatic response to weaning is inconsistent. For example, Rantzer et al. (1997) reported that adult exocrine volume, and protein and trypsin levels, were achieved within 5 days of weaning pigs at 30 doa. Conversely Cranwell (1995) reported that pancreatic enzymes were significantly depressed during the first week after weaning. Biosynthesis of specific enzymes appears to be an adaptive response to age at weaning (Gestin et al., 1997a), fat and dry matter intake (Gestin et al., 1997b), and dietary protein content (Zebrowska et al., 1983; Makkink et al., 1994). The source of protein in the diet also influences expression of pancreatic enzymes. For example, Makkink et al. (1994) found that pancreatic tissue enzyme activity was enhanced in pigs fed milk protein as opposed to soya. However, this result contrasts directly with the earlier findings of Newport and Keal (1982) comparing response to the same two proteins, but with different diets and methods of analysis. Further clarification of dietary effects on pancreatic development and enzyme expression is required. 7.3.3

Small intestine morphological response

The effects of weaning on intestinal morphology are acute. Over the last 30 years there have been numerous observations of post weaning villus atrophy and crypt hyperplasia. To summarise, reductions in the ratio of villus height to crypt depth ratio (V:C) are evident within 24 hours of weaning and are most pronounced by 3 to 5 days (Hampson, 1986; Miller et al., 1986; Cera et al., 1988). Significant increases in crypt depth may not be observed until 5 days post-weaning (Hampson, 1986) after which time V:C ratio stabilises between 1.5 and 2.0 (Hampson, 1983). The decline in V:C ratio immediately following weaning is thus primarily the result of villus shortening, an effect that is less pronounced proximal to distal along the small intestine. Figure 7.1 presents plots of least squares mean values for proximal jejunum crypt depth, villus height and V:C ratio data extracted from seven different trials reported during a period of 15 years (Hampson, 1986; Miller et al., 1986; Kelly et al., 1991; Pluske et al., 1991; Makkink et al., 1994; Pluske et al., 1996b; Jiang et al., 2000). Weaning ages, diets and days post-weaning of sampling are detailed for each reference in Table 7.2. Analysis of the data used to generate Figure 7.1 indicates the decline in villus height from d 0 (suckled) becomes significant on d 4 (P<0.05) at which point villus height is reduced by approximately 50%. Hampson (1986) reported that such villus atrophy is due to a reduction in enterocyte number rather than a contraction of the villus structure. Villus height gradually recovers to d 8 and thereafter stabilises at approximately 70% of suckled height.

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1000

Crypt depth

Villous height

7

V:C ratio

Crypt villous axis

800

6

600

5 *

** **

400

4

200

3 Villous crypt interface

0 - 200

**

**

*

*

1

16

0 18

- 400 0

2

4

6

8 10 12 Days post weaning

14

2

Villous height to crypt depth ratio

Digestive physiology of the weaned pig

Figure 7.1. Changes in villus and crypt morphology following weaning.

Table 7.2. Sources of data used for analysis of post-weaning gut morphology. Reference

Weaning age Diet type

Hampson 1986

21 days

Miller et al. 1986

21 days 35 days Kelly et al. 1991 14 days Pluske et al.1996a 28 days Makkink et al. 1994 28 days Pluske et al.1996b 29 days Jiang et al. 2000 14 days

Sampling age

Commercial creep feed 21, 22, 23, 24, 25, 26, 29, 32 days Soya flour 21, 28 days Soya flour 35, 42 days Skim milk powder 14, 17, 19, 22 days Whole milk 28, 33 days Skim milk powder 34 days Whole milk 34 days Soyprotein 14, 16, 18, 22, 30 days

Crypt depth varies little to d 6 post-weaning and then rapidly and significantly increases (P<0.01) to a stable depth in the region of twice the d 0 level. Elongation of the crypts is initiated by the weaning event and is not influenced by age at weaning (14, 21, 28 or 35 doa). The enterocyte migration distance (EMD: the distance from crypt basin to villus apex along which the enterocyte migrates), does not alter with age and is reduced significantly only on day 5 following weaning (P<0.1). Similar EMD to that of the data presented here for day 16 is still in evidence 28 days following weaning (calculated from Salgado et al., 2001). It appears from this data, that the mechanisms that regulate post-weaning structural change are targeted toward re-establishment of the suckled EMD. Pre-weaning EMD is re-established in the weaned pig primarily through elongation of the crypts. It is generally accepted that this phenomena is indicative of increased

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crypt cell production of enterocytes and this appears confirmed by concomitant increases in villus height. In light of the frequent associations made between enterocyte migration, differentiation and post-weaning functional competence there are startlingly few studies in which crypt cell proliferation rate (CCPR) has been measured before and after weaning. Combination of EMD and CCPR data enable calculation of proportional estimates of enterocyte migration rate: Suckled (EMD / CCPR %) Weaned (EMD / CCPR % For example, substituting the data means of Jiang et al. (2000) into this equation indicates that enterocyte migration from crypt basin to villus apex was proportionately 1.86, 3.42, 2.60 and 2.13 faster on d 2, 4, 8 and 16 postweaning than on d 0 (suckled). Villus height, crypt depth and epithelial cell numbers reported by Hampson (1986a) for creep fed pigs weaned at 21 doa indicate enterocyte size is unaffected by weaning. Thus, relative to EMD, accelerated migration of cells from crypt basin to villus apex following weaning would seem likely to result in a reciprocal reduction in enterocyte lifespan. Reduced functionality of individual enterocytes will occur only if there is insufficient time for complete differentiation as they migrate up the villus. There is evidence that this does occur (see section 7.4). The increase in villus diameter observed in parallel with villus shortening during suckling (Cera et al., 1988) continues post-weaning and ultimately results in acquisition of the leaf-shape, thickened development characteristic of the adult intestine (Cera et al., 1988; Kelly et al., 1992). The maturing crypt-villus structure is essentially a geometric tube of height EMD and increasing diameter. The negative effect of post-weaning villus atrophy on enterocyte migration is thus to some degree compensated for by a temporal program of crypt extension (maintenance of EMD) and increasing villus diameter. However, restructuring of the villus after weaning results in a marked loss of the apical surface and is consequently associated with a reduction in enterocyte maturity and functionality. Strikingly obvious from the data presented in Figure 7.1 is the inadequacy of V:C ratio as a satisfactory indicator of the individual dynamics of villus and crypt restructuring or their additive effects on EMD and enterocyte maturation. We propose the expression of villus height, crypt depth and crypt basin to villus apex measurements as a proportion of their absolute values in control animals to be more worthwhile. This would facilitate rapid and informative comparison of data between studies.

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7.3.4

Small intestine carbohydrase and transporter response

At birth, nutrient uptake occurs along the entire crypt to villus axis but during the suckling period this capability gradually becomes concentrated in the apical enterocytes. Miller et al. (1986) elegantly demonstrated the negative that effect apical enterocyte loss has on lactase and β-glucosidase activities, and on Na-dependent uptake of alanine in pigs 5 d post-weaning. In this study, functional capacity of the post-weaning villi remnant was greatly reduced, indicating immaturity of the apical enterocytes. In contrast, Kelly et al. (1991) reported significant increases in maltase and glucoamylase activities (absolute and per unit of protein) in 21-day old pigs (weaned 14 doa) that were greater than age-related increases observed in unweaned siblings at 22 d of age. In fact, significant increases in both enzymes were apparent 3 days following the switch from milk to the gastric-intubated weaner ration. Rapid carbohydrase induction post-weaning is therefore possible in response to luminal substrate presence. Interestingly however, in this study, weaning at 14 doa significantly compromised the chronological increase in total sucrase activity evident at 22 doa in suckled pigs despite 5% inclusion of sucrose in the diet of the weaned piglets.

Activity per unit mucosa

Regional differences in carbohydrase activities (Figure 7.2) and rates of monosaccharide transport (Figure 7.3) are evident following weaning and consumption of solid food. During suckling, lactose is the predominant dietary carbohydrate (CHO), and lactase the most active of the disaccharidases. Unlike the complex CHO fed post-weaning, lactose is readily hydrolysed in the proximal small intestine and its component monosaccharides, glucose and galactose, rapidly taken up by enterocyte aldohexose transporters. In contrast, digestion of the more complex CHO in weaner diets is protracted, requiring the breakdown of macromolecules to their component disaccharides before these can be hydrolysed by brush-border enzymes and absorbed. Consequently, post-weaning intestinal

Lactase

Sucrase

Maltase 10%

30%

50%

70%

90%

Figure 7.2. Mucosa normalised proximal to distal disaccharidase activity profiles in 21 day old pigs weaned at 7 days (Adapted from Kelly et al. (1991)).

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Day 10 (suckled)

Proximal

Medial

Distal

Day 30 (weaned d 21)

Proximal

Medial

Distal

Galactose transport

Glucose transport

Fructose transport

Figure 7.3. Mucosa normalised proximal to distal monosaccharide absorption profiles in pigs 10 days post-partum and 9 days after weaning at 21 days (Adapted from Puchal and Buddington (1992)).

carbohydrase activities extend further along the small intestine (Manners and Stevens, 1972; Kelly et al., 1991), and are supported by appropriate regional distribution of monosaccharide transporters (Puchal and Buddington, 1992). 7.3.5

Amino acid transport

Developmental aspects of amino acid absorption in the pig appear to have received little attention to date apart from a recent contribution from Buddington and colleagues (Buddington et al., 2001). These workers investigated apical amino acid absorption in intact tissues excised from the small intestine of pigs at developmental stages ranging from late gestation (11 days prior to birth) through to 42 doa (12 days post-weaning). Sample tissues were collected at proximal, medial and distal sites along the intestine. Rates of absorption per unit tissue mass (‘rate’) declined sharply during the first 3 hours post-partum for all 5 free amino acids studied: aspartate, leucine, lysine, methionine and proline (Asp, Leu, Lys, Met and Pro). Pro rate then increased significantly to 7 doa. From day 7 to 28 specific rates declined and thereafter remained stable. Relative to bodyweight, intestinal absorptive capacity for Leu doubled to 7 doa and then stabilised. Absorption of the other amino acids studied increased gradually to 28 doa after which uptake increased markedly for Asp and Met and to a lesser extent for Lys. Absorption rates for Pro and Asp were significantly and permanently reduced in the distal intestine 24 hours after birth. No other age-related regional differences in rate or capacity were reported. Affinity constants and carrier mediated maximum rates of absorption reduced for

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all amino acids except Lys from 28 to 42 doa (12 days post-weaning), and were paralleled by a universal increase (average 49%) in their apparent rates of diffusion. Buddington et al. (2001) concluded that as a consequence of rapid intestinal growth, increasing from 15 g wet mass at birth to 862 g at 42 doa, overall capacities for amino acid absorption increased faster than did metabolic liveweight. Weaning therefore does not compromise intestinal capacity for uptake of amino acids, however, there may be a transient decline in amino acid uptake capability corresponding with the period of villus shortening immediately after weaning. This has yet to be investigated. The majority of amino acids in the weaner diet comprise complex proteins. These must be broken down enzymatically before amino acid absorption can occur, thus the simultaneous development of appropriate gastric, pancreatic and mucosal enzyme systems is necessary. Di- and tri-peptides are also generated during protein breakdown and many of these can be absorbed directly from the intestinal lumen. In older pigs peptide absorption can be of equal importance to amino acid uptake, however, we have been unable to find any literature describing the development of peptide absorption in the weaned pig. 7.3.6

Perspective 2

The digestive infrastructure necessary for neonatal enteral nutrition is established during fetal development and includes nascent ability to digest non-milk dietary components. Commencement of enteral nutrition amplifies the intestinal capacity to process solid food whilst simultaneously instigating progressive changes in villus structure. Thus gradual intestinal preparation for post-weaning nutritional input continues throughout the suckling period. Just as fetal digestive development may be primed/stimulated by ingestion of amniotic fluids, so the gradual luminal introduction of novel nutrients in the natural situation generates appropriate changes in gut growth and functionality. Parallels therefore exist between neonatal and natural weaning digestive development; however, commercial early weaning practices introduce fundamental differences between the two processes. We previously identified three principal factors influencing digestive physiology and the successful transition from placental to enteral nutrition in the neonate. How do these factors differ between the neonate and the commercially weaned pig? First, the neonate has been evolutionally pre-equipped with the digestive apparatus requisite for the switch in nutrient intake. In contrast, intestinal development in preparation for the transition from milk to solid diets is far from complete in the commercially weaned piglet. Second, the neonate is provided with a highly digestible, high fat, low fibre, tailor-made nutritional package temporally matched to its stage of digestive development. Despite our best efforts, the weaner is not. Third, the neonate receives dietary agents that direct appropriate changes

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in intestinal physiology to fine-tune the digestive and absorptive processes. Although intestinal adaptation in the commercially weaned piglet is primarily substrate driven, the components of the weaner diet demand, rather than direct, digestive development, and result in coarse adjustment rather than fine-tuning of the digestive apparatus. We have described how these deficiencies are characterised in the commercially weaned pig by rapid and severe alteration of intestinal form and function, but how are such responses mediated by the piglet?

7.4

Regulation of post-weaning adaptation

Delayed or natural weaning extends the opportunity for piglet adaptation to the adult intestinal format thereby reducing, or eliminating entirely, the digestive traumas associated with transition to the adult diet (Hampson, 1986; Miller et al., 1986; Kelly et al., 1991). The rapid intestinal modification which occurs in commercially weaned pigs is therefore a consequence of differences between weaning scenarios, ie. weaning stress and abrupt substitution of the milk diet with a weaner ration resulting in a pronounced reduction in feed intake. 7.4.1

Milk withdrawal

It has been argued that the whole weaning process - removal of dam, change of housing, mixing with other pigs, change of feed type and source etc. - is incredibly stressful to the piglet. However the importance of milk removal per se and its replacement by an alternative food cannot be overstated. The digestive physiology of the suckled pig is focussed on digestion and absorption of milk components and, in consequence, is transiently compromised by the sudden substitution of a more complex diet at weaning. Nutritionally, milk is a source of protein, fat and carbohydrate that can be further described in terms of essential amino acids, carbohydrate moieties and different chain-length fatty acids. However, concealed within this nutritional profile are a vast array of physiological, immunological, biochemical and bacteriological mediators of gut health, efficiency and growth (Fox and Flynn, 1993). Removal from the sow thus simultaneously deprives the piglet of a readily digestible food source and potent regulators of intestinal structure and function. The importance of milk is demonstrated by studies in which weaning onto milk diets prevented the typical post-weaning change in crypt and villus architecture (Pluske et al., 1996a and b). An increasing awareness of the primary (non-nutritional) functions of lactation products and their capacities to regulate intestinal health and adaptation is apparent from the literature (see Xu et al., 2000). At least 16 distinct growth factors have been detected in mammary secretions (Fox and Flynn, 1993). In addition, a number of bioactive peptides are released by the hydrolysis of casein and whey proteins (Meisel et al., 1989, Maubois and Lenoil, 1989: cited by Fox and Flynn,

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1993). Intestinal receptors and modes of action have yet to be characterised for many of these substances. In addition, the majority of studies in swine have concentrated on neonatal response to factors in colostrum; considerably less information is available regarding the effects of factors in milk on pig digestive physiology (see Pluske et al., 1997). The consequences of individual bioactive milk component withdrawal on intestinal stability are not well understood, and require comprehensive investigation in order to further our comprehension of weaning associated events. 7.4.2

Weaning stress

We have considered the physical and functional consequences of commercial early weaning on piglet digestive physiology. However, separation from the sow, handling, mixing and adaptation to new behavioural and nutritional situations subjects the piglet to considerable physiological stress. Weaning is therefore associated with significant increases in plasma cortisol concentration (Carroll et al., 1998; Wu et al., 2000). Intestinal sensitivity to cortisol is generally thought to be lost by the time of natural weaning, however, commercial early weaning practices may well precede development of cortisol insensitivity. A recent review of factors influencing small intestinal structure and function in the weaned pig (Pluske et al., 1997), exposed the lack of evidence linking cortisol levels at weaning with the subsequent growth check and intestinal ‘maladaptation’. However, there is considerable support in the literature for a more benevolent role of cortisol in intestinal adaptation. For example, pre-term pigs (82 - 96 days of gestation) administered cortisol in utero exhibited significantly increased lactase, maltase and aminopeptidase A and N activities six days later (Sangild et al., 1995). Similar benefits on carbohydrase activities have been reported in suckled pigs at 26 doa (Chappel et al., 1989: cited by Flynn and Wu, 1997). Furthermore, intramuscular injection of glucocorticoid given to weaned pigs infected with transmissible gastroenteritis virus prevented villus atrophy and increased electrolyte retention through improved glucose-facilitated Na absorption (Rhoads et al., 1988). More relevant to weaning physiology is the role of endogenous cortisol in regulation of mucosal amino acid metabolism. Post-weaning redevelopment of intestinal structure and function involves considerable increase in mucosal protein synthesis with consequent high enterocyte demand for amino acids, both as energy substrates (e.g. glutamine, glutamate, aspartate) and as building blocks for protein synthesis (e.g. arginine). In theory, cells of the intestinal mucosal can obtain these substrates from either the intestinal lumen or the mesenteric arterial circulation. However in practice, with the notable exception of glutamine, uptake of circulatory substrates/precursors is negligible. This is apparent from the mucosal atrophy which occurs with total parenteral nutrition (TPN) (eg. Remillard et al., 1998a; Bertolo

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et al., 2000). Enterocyte metabolism of dietary amino acids is always necessary for intestinal homeostasis but becomes critical during post-weaning maturation of the small intestine. Increased circulating cortisol concentrations appear to facilitate appropriate amino acid metabolism by the small intestine post weaning. For example, Flynn and Wu (1997) reported that blocking glucocorticoid receptors abolished weaning-enhanced enterocyte production of ornithine, citrulline and CO2 from glutamine, and proline and CO2 from arginine. Similarly, Wu et al. (2000) reported that enterocyte synthesis of citrulline from glutamine in pigs 8 days after weaning was 10-fold greater than in unweaned contemporaries. Inhibition of adrenal cortisol production during the immediate post-weaning period completely eliminated this increase. In both studies the authors offered evidence of cortisol involvement in the enhanced expression or activity of enterocyte enzymes catalysing specific stages of glutamine and arginine metabolism. Therefore it appears that cortisol release in response to the stress of weaning actually enhances the piglet’s ability to react appropriately, at least in terms of its digestive physiology. 7.4.3

Direct dietary effects

The punitive effects of low feed intake on gut morphology are well documented (Goldstein et al., 1985; Remillard et al., 1998a; Remillard et al., 1998b; Lopez-Pedrosa et al., 1999). However, the weaned piglet undergoes a relatively short period of sub-maintenance feed intake, with maintenance energy intake re-established within 5 days of weaning (Le Dividich and Herpin, 1994, cited by Pluske et al., 1997). In the interim, the significant mobilisation of lipid reserves post-weaning (Whittemore et al., 1978) is likely to fund deficits in energy intake. Transient depression in energy intake would therefore seem unlikely to reduce whole body energy availability. However, we have already noted that the contribution of circulatory energy substrates to metabolism and structural maintenance of the mucosa is negligible, thus enteral nutrition would seem pivotal to gut maintenance. Pluske et al. (1996b) clearly demonstrated that in piglets fed cows’ milk after weaning, energy intake strongly influenced villus height. Similar effects of energy intake on gut morphology were reported by van Beers-Schreurs et al. (1998). Interestingly, data from Pluske et al. (1996b) also indicated that, independent of dry matter and energy intake, mean villus height was maintained and crypt depths less increased when pigs were weaned onto cows’ milk rather than a starter ration. This response might reflect physical differences in the form of the diet or, alternatively, the complementary effects of milk nutritional composition and availability on enterocyte metabolism and hence intestinal homeostasis. It is apparent from consideration of enterocyte metabolism that the amino acid profile of the weaning diet is a key factor in the success of rapid post-weaning intestinal development. However, as a consequence of mucosal metabolism, the pattern of amino acids available for peripheral tissue metabolism will differ markedly

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from that provided in the diet (Stoll et al., 1998). This effect is comprehensively detailed for glutamate (eg Windmueller and Spaeth, 1980; Reeds et al., 1996; Reeds et al., 2000), but with a few notable exceptions (Yu et al., 1990; Stoll et al., 1998; Wu, 1998) is less well characterised for the essential amino acids (EAA). This questions the ability of weaner diets to adequately support the nutritional requirements for intestinal development or, following mucosal metabolism, to effectively promote whole animal growth. The extent of EAA intestinal catabolism is of obvious importance to both perspectives and as such requires further elucidation. Physical qualities of the post-weaning diet may contribute to villus atrophy. Pelleting (see Pluske et al., 1997) and increased fibre content of the diet (Tasman-Jones et al., 1982) may lead to mechanical erosion of apical enterocytes during digesta flow along the small intestine. There is little direct evidence in the literature to support this theory, indeed scanning electron microscopy failed to detect villus damage in intestinal sections prepared from pigs fed pelleted cereal diets (Hampson, 1986). However, villus atrophy to day 5 post-weaning followed by emergence of the more compact, lower profile, leaf-shaped villus configuration may indicate an abrasioninduced response. Similarly, the changes in digesta mucin noted after weaning (Pestova et al., 2000) may be in response to the increased abrasive qualities of digesta. Studies in our laboratory indicate goblet cell numbers per villi reduced post-weaning (d 5) but increased per unit of villus height (unpublished data). Thus the capacity for epithelial protection by mucin secretion increases after weaning. Miller et al. (1986) speculated that the post-weaning changes in enterocyte carbohydrase expression could not be completely reconciled with aetiological theories implicating changes in diet, hormone levels and CCPR. These authors hypothesised that enterocyte ontogenic development might instead be influenced by interactions with the immune system following epithelial exposure to food antigens. Hypersensitive responses to dietary antigens and their immunological implications have been discussed extensively in the literature (see for example Miller et al., 1991; Newby et al., 1994; Dreau and Lalles, 1999) and lie beyond the scope of this chapter. However, in view of the implicit connection between immunemediated intestinal hypersensitivity and modification of weaned pig digestive physiology, brief comment is justified. Hypersensitivity (Types I and IV) requires previous exposure or ‘sensitisation’ of the immune system to the antigen. Induction of hypersensitivity depends on the extent of initial antigenic exposure. Very low or high exposure promotes ‘oral tolerance’ of the antigen, whereas an intermediate antigen dose sensitises (primes) the immune system. The dilemma is that division between priming and tolerising antigen doses is not readily quantifiable. Furthermore, sensitisation varies depending on individual antigenic, environmental and genetic determinants.

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Sensitisation results in the production of antigen specific IgE and B memory cells (Type I) or T memory cells (Type IV) that, on subsequent exposure to the antigen, elicit particular immune responses. Simply, Type I responses (termed ‘immediate’) are mediated primarily by antigen specific IgE attached to mast cell surface receptors; cross-linking of IgE by the antigen results in rapid degranulation of mast cells. Type IV responses (termed ‘delayed’) involve T cell activation and macrophage recruitment to the site of antigen presence, mast cell degranulation and cytokine release. Both responses elicit acute inflammatory effects and damage to antigen-associated tissues, in this case the gut epithelium. Thereafter their Type I and IV responses are suppressed by T helper 1 cells (Th1), and keratinocyte and macrophage-produced prostaglandin E (PGE) respectively. What is clear is that piglets weaned at between 21 and 28 doa which have had access to creep feed during the nursing period are unlikely to have consumed the correct antigen dose to elicit immune tolerance on subsequent exposure (Newby et al., 1994). In humans Type I and IV responses peak approximately 12 and 72 hours following re-exposure to the antigen (Roitt et al., 1998). Therefore it is likely that in piglets, diet-induced immunological enteropathy contributes to the adverse changes in villus architecture observed in the first 5 days post-weaning. In the commercial situation the piglet’s first significant exposure to dietary antigens often occurs at weaning. However, unless access to the sow’s diet is prevented, exposure to sensitising doses of antigenic material may occur during the nursing period. In a recent study, McCracken et al. (1999) determined jejunal expression of proinflammatory immune system components in villus and crypt tissue of pigs weaned onto milk or soy-based diets. These authors reported significant reductions in villus height from 2 days post-weaning that were paralleled by marked increases in villus CD4+ T cell numbers and preceded by significant depression in MHC class I RNA expression. However, these effects were similar in both treatment groups. Likewise, crypt and villus CD8+ T cell numbers and MHC class II determinations were unaffected by dietary protein source whilst PGE concentrations, maximal at 48 hours plus in Type IV scenarios, were highest on day 1 for both treatments. McCracken et al. (1999) reasoned that the temporal pattern of immune events elicited in this experiment did not completely satisfy the hypersensitivity hypothesis. Feed intake of piglets over the 2 days following weaning was typically low, less than 100 g per pig in total. This prompted the authors to suggest that weaning anorexia itself might compromise epithelial integrity, thus initiating inflammatory response through direct interaction of the antigen with the lamina propria. 7.4.4

Indirect dietary effects

Inadequate nutrient intake is a consistent feature of piglet response to weaning and has clear effects on gut morphology. The expression or secretion of a variety of somatotropic hormones is also strongly influenced by nutritional status

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(Buonomo and Baile, 1991) and therefore is significantly altered at weaning (Carroll et al., 1998; Le Dividich and Seve, 2000). Insulin-like growth factor I (IGF-I) and growth hormone (GH) have been implicated in intestinotrophic events (see Burrin, 1997; Baksheev and Fuller, 2000), and are affected by nutrient intake. In fact, White et al. (1991) reported similar significant reductions in circulating IGF-I in pigs that were weaned to those that were fasted for 36 hours! However, it is the nutrient responsive gut peptides that appear most strongly influenced by, and regulatory of, weaning digestive events. The effects of several of these peptides on gastrointestinal motility, adaptation and growth are summarised in Table 7.3. The list of enteroendocrine factors already identified is extensive, and our understanding of their actions and interactions is far from definitive. Changes in the endocrine and metabolic status of the pig at weaning are discussed elsewhere in this book. Comment here will therefore be restricted to a brief consideration of weaning-elicited gut hormone secretion. Using the example of the proglucagon derived peptides (PGDPs), particularly glucagon-like peptide 1 and 2 (GLP-1 and GLP-2), we will discuss the enteroendocrine regulation of post-weaning digestive development. Nutrient responsive secretion of gut peptides is suppressed by a reduction in feed intake (van Goudoever et al., 2001) and may also be influenced by diet composition (eg. fibre, complex carbohydrates, short-chain fatty acids: Burrin et al., 2001). Endocrine response to re-feeding is equally pronounced. Van Goudoever et al. (2001) reported that piglet arterial concentrations of glucose dependent insulinotropic polypeptide (GIP) and GLP-2 increased 4 to 8-fold within 1 hour of feeding after a fast of 13 hours. GLP-2 is a member of a group of 5 peptides derived from post-translational processing of intestinal proglucagon in the L cells of the colon and distal small intestine. The other members of the group are GLP-1, glicentin, glicentin-related pancreatic peptide (GRPP) and oxyntomodulin. Direct contact with luminal nutrients stimulates L cell secretion of these peptides into the villus capillary system. Glicentin promotes intestinal cell growth in vitro but immunoneutralisation demonstrated that it has little effect on bowel growth in vivo (Bloom and Polak, 1982: cited by Drucker, 1997). Oxyntomodulin has no detectable intestinotrophic effect but does stimulate intestinal glucose uptake, particularly in the ileum (Collie et al., 1997). Nutrient intake also stimulates secretion of GIP from duodenal K cells. Both GIP and GLP-1 function as incretin hormones, ie. their secretion in response to nutrient intake stimulates insulin secretion that is disproportionately larger than would otherwise be elicited by ingested nutrients. As such, both hormones play a major role in extra-intestinal metabolism and growth. GIP stimulation of GLP secretion in vivo was first demonstrated in rats by Roberge and Brubaker (1993) for GLP-1 and has since been implicated in GLP-2 expression in pigs (van Goudoever et al., 2001).

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Table 7.3. Nutrient responsive enteroendocrine mediators of intestinal response to weaning. Peptide Site of secretion

‘Ileal brake’

Enterotropic

References

EGF 1

Submandibular glands Brunner’s glands Paneth cells

Yes

Yes

Peng et al. 1996 Cuber 1997 Drucker 1997 Baksheev and Fuller 2000

GIP 2

K cells

Yes

Insulinotropic

Roberge and Brubaker 1993 Knapper et al. 1995 van Goudoever et al. 2001

GLP-1 3 L cells

Yes

Insulinotropic

Roberge and Brubaker 1993 Knapper et al. 1995 Hansen et al. 1999 Holst 2000

GLP-2 4 L cells

Yes

Yes

Drucker 1997 Drucker et al. 1997 Holst 2000 van Goudoever et al. 2001

PYY 5

L cells

Yes

Yes

Drucker 1997 van Goudoever et al. 2001

CCK 6

I cells

Yes

Pancreatropic

Cuber 1997

NT 7

N cells

Yes

Drucker 1997

1Epidermal

growth factor dependent insulinotropic polypeptide 3Glucagon-like peptide 1 4Glucagon-like peptide 2 5Peptide YY 6Cholecystokinin 7Neurotensin 2Glucose

GLP-1 is one of the gut peptides involved in the ‘ileal brake’ phenomenon (Read et al., 1994). This is the mechanism by which ileal presence of unabsorbed nutrients inhibits upper gastrointestinal activity. Thus nutrient responsive GLP-1 release

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inhibits gastric acid secretion and stomach emptying, depresses pancreatic exocrine activity and reduces intestinal motility. Deactivation of GLP-1 is extraordinarily rapid. Hansen et al. (1999) reported that 50 to 75% of GLP-1 is metabolised to an inactive form before leaving the villus capillaries. More recently, one of the co-authors of this study reasoned that GLP-1 intestinal effects might be mediated through interaction with sensory afferent neurones terminating in the lamina propria (see Holst, 2000). In summary, in response to unabsorbed lipid and carbohydrate in the distal ileum and colon, GLP-1 prolongs nutrient exposure to upper GIT digestive and absorptive processes. It is clearly possible that the nutrient complexity of postweaning diets in combination with reduced villus functionality might result in physiological malabsorption with resulting GLP-1 secretion. This in turn would down-regulate intestinal dynamics and consequently reduce feed intake. Intravenous infusion of GLP-1 has been shown to depress appetite and food intake in man (Flint et al., 1998; cited by Holst, 2000). GLP-2 secretion parallels that of GLP-1 in that both are stimulated by direct exposure of the L cell to intraluminal nutrients. Although to a lesser extent, gastrointestinal motility is also inhibited by GLP-2, however the primary action of this peptide appears to be stimulation of intestinal growth. Infusion of GLP-2 has been shown to increase intestinal tissue mass, mucosal thickness, villus height and crypt depth and has also been reported to increase hydrolase expression and hexose and amino acid transport in several species (see reviews by Baksheev and Fuller, 2000; Drucker, 1997; Holst, 2000; Burrin et al., 2001). In addition, in pigs receiving total parenteral nutrition, GLP-2 infusion maintained intestinal growth by suppressing proteolysis and apoptosis (Burrin et al., 2000). These responses were generated following administration of supraphysiological levels of GLP-2. However, Fischer et al. (1997) reported that an increase of approximately 50% in endogenous GLP2 secretion was sufficient to promote significant intestinal growth and villus and crypt extension in rats. Arterial concentration of GLP-2 increased 4-fold in weaning age pigs following re-alimentation after a 13 hour fast (van Goudoever et al., 2001). The voluntary feed intake of the just-weaned pig is typically very low (see for example Bark et al., 1986), and the duration of ‘non-eating’ invariably in excess of 24 hours. We are unaware of any investigations in which the effects of weaning on GLP-2 concentrations in pigs have been reported. However, it would appear from the studies presented here that a GLP-2 surge following significant ingestion of the weaning diet is likely and, if so, would undoubtedly contribute to intestinal adaptation. The combined action of GLPs thus presents a coherent response to villus atrophy and subsequent physiological malabsorption that is supported by the actions of other gut hormones, the mechanism effectively retarding nutrient transit whilst adaptive growth of the intestine is instigated. Outwardly such events would be characterised by a feed intake plateau or reduction as observed in our own studies (Figure 7.4) and those of other workers (see for example Bark et al., 1986;

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Feed intake (g/pig/day)

Miller and Slade

1000 800 600 400 200 0 0

2

4

6

8

10

12

14

16

18

20

Day post-weaning

Figure 7.4. Post-weaning feed intake of piglets weaned at 26 days of age and offered diets containing skim milk.

McCracken, 1989). Inwardly, reduced nutrient intake would be paralleled by an increase in intestinotrophic events as demonstrated in Figure 7.1. 7.4.5

Perspective 3

The changes in digestive physiology after weaning can be separated into 2 phases: the decline of infant intestinal structure and function (phase I) and the development of mature intestinal parameters (phase II). The transition from one phase to the other is initiated by enteral nutrition and is subject to inherent developmental drives. Ingestion of colostrum and subsequently milk stimulates elemental changes in gut morphology and growth that are paralleled by reshuffling of intestinal secretory and absorptive capacities. In the natural situation the developmental phases merge seamlessly: the piglet continues to receive nutritional and immunological support from the sow whilst luminal exposure to new dietary components increases; improved intestinal capacity to process non-milk products is both developmentally and adaptively generated; and tolerance of novel nutrients is mediated by lactation components. The process continues until between 9 and 12 weeks after birth when the milk component of the diet diminishes to nothing and the pig is weaned. Commercial weaning effectively condenses the latter two thirds of the natural weaning process into a period of days rather than weeks. As a consequence the development phases become quite distinct. Phase I culminates 3 to 5 days following weaning and is characterised by marked reductions in villus surface area, enterocyte population, enterocyte maturity and secretory and absorptive function. Initiation of phase II precedes or coincides with conclusion of phase I. Developmental progression of intestinal maturation evident pre-weaning is dominated and overtaken by adaptive responses to nutrient luminal presence. Crypt cell proliferation is induced and villus height partially restored with consequent

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re-establishment of the crypt-villus axis dimension. Intense growth of the digestive tract maintains or increases total digestive and absorptive function whilst gastric motility is transiently reduced and exposure of ingested nutrients to digestive secretions increased. Pancreatic and intestinal hydrolase activities adapt responsively to dietary input and are complemented by regionalised increases in nutrient transporter capacities. Ultimately, equilibrium between cell production and cell loss is achieved, enzyme expression and activities are optimised to diet intake and composition, and nutrients are absorbed with maximum efficiency. The digestive physiology of the weaned pig is thus established.

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van Goudoever, J.B., B. Stoll, B. Hartmann, J.J. Holst, P.J. Reeds and D.G. Burrin. 2001. Secretion of trophic gut peptides is not different in bolus- and continuously fed piglets. Journal of Nutrition 131, 729-732. Westrom, B.R., B. Ohlsson and B.W. Karlsson. 1987. Development of porcine pancreatic hydrolases and their isozymes from the foetal period to adulthood. Pancreas 2, 589-596. White, M.E., T.G. Ramsay, J.M. Osborne, K.A. Kampman and D.W. Leaman. 1991. Effect of weaning at different ages on serum insulin-like growth factor I (IGF-I), IGF-binding proteins and serum in vitro mitogenic activity in swine.” Journal of Animal Science 69, 134-145. Whittemore, C.T., A. Aumaitre and I.H. Williams. 1978. Growth of body components in young weaned pigs. Journal of Agricultural Science, Cambridge 91, 681-692. Windmueller, H.G. and A.E. Spaeth. 1980. Respiratory fuels and nitrogen metabolism in vivo in the small intestine of fed rats. Quantitative importance of glutamine, glutamate and aspartate. Journal of Biological Chemistry 255, 107-112. Wu, G. 1998. Intestinal mucosal amino acid metabolism. Journal of Nutrition 128, 1249-1252. Wu, G., C.J. Meininger, K. Kelly, M. Watford and S.M. Morris Jnr. 2000. A cortisol surge mediates the enhanced expression of pig intestinal pyrroline-5-carboxylate synthase during weaning. Journal of Nutrition 130, 1914-1919. Wykes, L.J., R.O. Ball and P.B. Pencharz. 1993. The development and validation of a total parenteral nutrition model in the neonatal pig. Journal of Nutrition 123, 1248-1259. Xu, R.J., D.J. Mellor, P. Tungthanathanich, M.J. Birtles, G.W. Reynolds and H.V. Simpson. 1992. Growth and morphological changes in the small and large intestine in piglets during the first three days after birth. Journal of Developmental Physiology 18, 161-172. Xu, R.J., F. Wang and S.H. Zhang. 2000. Postnatal adaptation of the gastrointestinal tract in neonatal pigs: a possible role of milk-borne growth factors. Livestock Production Science 66, 95-107. Yu, Y-M., D.A. Wagner, E.E. Tredget, J.A. Walaszewski, J.F. Burke and V.R. Young. 1990. Quantitative role of splanchnic region in leucine metabolism: L-[1-13C 15N] leucine and substrate balance studies. American Journal of Physiology 259, E36-E51. Zabielski, R., I. Le Hueron-Luron and P. Guilloteau. 1999. Development of gastrointestinal and pancreatic functions in mammalians (mainly bovine and porcine species): influence of age and ingested food. Reproduction Nutrition Development 39, 5-26. Zebrowska, T., A.G. Low and H. Zebrowska. 1983. Studies on gastric digestion of protein and carbohydrate, gastric secretion and exocrine pancreatic secretion in growing pigs. British Journal of Nutrition 49, 401-410. Zhang, H., C. Malo, C.R. Boyle and R.K. Buddington. 1998. Diet influences development of the pig (Sus scrofa) intestine during the 6 hours after birth. Journal of Nutrition 128, 1302-1310. Zhang, H., C. Malo and R.K. Buddington. 1997. Suckling induces rapid intestinal growth and changes in brush border digestive functions in newborn pigs. Journal of Nutrition 127, 418-426.

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8

Diet-mediated modulation of small intestinal integrity in weaned piglets M.A.M. Vente-Spreeuwenberg and A.C. Beynen

Summary Piglets are faced with multiple changes around the weaning transition. This generally results in low voluntary feed intake, sub-optimal growth rate and diarrhoea may occur frequently. The small intestine not only digests and absorbs nutrients, but also excludes pathogens, toxins and allergic compounds. Small intestinal function depends on its integrity, which can be assessed on the basis of indicators such as villous length, crypt depth, number of goblet cells, transepithelial permeability, brush border enzyme activity and growth performance. Weaning of piglets negatively affects small intestinal integrity as indicated by a decrease in villous length, an increase in paracellular permeability and a decrease in total brush border enzyme activities. This review focuses on dietary modulation of the weaning-induced impairment of small intestinal integrity. It is concluded that the level of feed intake is the most important determinant of mucosal function and integrity. Thus, the temporal low feed intake immediately after weaning is the main cause of the decrease in small intestinal integrity. Furthermore, the actual amount of feed consumed is positively correlated with the development of the small intestine. Studies reviewed are those dealing with potential functional feed ingredients, including protein source, specific amino acids, fatty acids, fibres, non-digestible oligosaccharides, growth factors, polyamines and nucleotides. It is concluded that the individual feed constituents have only marginal effects on small intestinal integrity of the weaned pig. Possibly, combinations of functional feed ingredients will be more successful. Further research should involve identification of determinants of feed intake immediately after weaning and functional feed ingredients to stimulate epithelial cell proliferation and differentiation, enhance immune function and promote growth of beneficial bacteria.

8.1

Introduction

At weaning, piglets are faced with changes of various nature. Under commercial conditions, weaning at 24-28 days of age usually involves complex social changes for the piglets, including their separation from the mother, separation from littermates and exposure to unfamiliar counterparts (Fraser et al., 1998). The composition of the piglets’ diet changes drastically at weaning; the liquid milk from the sow is replaced by pelleted dry feed with starch instead of fat as the main energy source. The transition from suckling to eating solid food is associated with a critical period of underfeeding during which the pig is adapting itself to the dry food (Le Dividich

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and Herpin, 1994). The low feed intake during the first two days after weaning, which essentially is independent of diet composition (McCracken et al., 1995), causes growth stasis (Leibrandt et al.,1975; McCracken et al., 1995; 1999). Diarrhoea frequently occurs after the weaning transition (Nabuurs, 1991). The gastrointestinal tract not only allows for the digestion and absorption of nutrients, but also acts as a barrier for bacteria, toxins and allergic compounds that otherwise may reach the systemic organs and tissues. For the small intestine, the level of feed intake is a critical determinant of its digestive and absorptive capacity (Pekas, 1991) and also of its barrier function (Bishop et al., 1992). The low feed intake caused by weaning often leads to maldigestion and malabsorption and also to reduced small intestinal barrier function. When feed intake increases, diarrhoea may occur. Enterotoxemic bacteria proliferate and release their toxins. An integrated concept of the response to weaning is given in Figure 8.1. The problems associated with weaning are mainly a consequence of the commercial conditions. Weaning of piglets at an age as young as possible increases the number of piglets per sow per year. Under natural conditions, piglets gradually develop the capability to digest solid food and voluntary reduce their intake of milk. Thus, the piglets themselves control the weaning process. Some nursing may still continue until the piglets are 12-16 weeks of age, this being considered the natural age of weaning (Jensen and Recén, 1989; Fraser et al., 1998). Based on general knowledge of the influence of nutrition on gut function and health, diets may be formulated that alleviate or prevent the adverse effects of weaning at 4 weeks of age. The objective of this chapter is to highlight the nutritional

Pathogenesis of the post-weaning syndrome Social and diet changes Low feed intake Lack of enteral nutrition Impairment of mucosal function Uptake of antigens, toxins and translocation of bacteria Inflammation

Maldigestion, Malabsorption Poor performance Diarrhoea Infections

Figure 8.1. An integrated concept of the effect of weaning on mucosal barrier function, performance and health in piglets.

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opportunities to modulate the intestinal barrier function after weaning, thus resulting in increased piglet performance. It is beyond the scope of this chapter to review the effect of hormones on small intestinal integrity. Prior to describing the effects of diet composition, the indicators of small intestinal integrity will be discussed briefly.

8.2

Small intestinal integrity

One important function of the gastrointestinal tract is to transform ingested food so that absorbable nutrients become available for the body. Morphologically, the small intestine represents a maximum absorptive surface. The presence of Kerckring’s folds, villi and microvilli in the small intestine produces a large surface area compared with that of a cylindrical tube (Junqueira and Cerneiro, 1980; Caspary, 1987, 1992; Dyce et al., 1987). The small intestinal villi of healthy piglets are predominantly finger-shaped with few tongue-shaped villi (Mouwen, 1972). A 10-day old, 3-kg piglet has a relatively small intestine with a total absorptive surface area of 114 m2 (Buddle and Bolton, 1992). The epithelial cells lining of the gastrointestinal tract renew rapidly. The small intestinal villus epithelium in 1-dayold pigs is replaced in 7-10 days, whereas this process in 3-week-old pigs takes 24 days (Moon, 1971). The epithelial cells have apical 0.5-2 µm intercellular attachment zones or junctional complexes, which join them together. These tight junctions regulate epithelial permeability by influencing para-cellular flow of fluid and constituents. In general, the complexity, strand number and depth of the tight junction correlate inversely with the permeability of epithelia (Trier and Madara, 1981). The gastrointestinal tract provides an extensive surface area with intimate contact between the host organism and dietary substances, microorganisms, parasites and exogenous toxins. The intestine permits the uptake of dietary substances into the systemic circulation, but at the same time excludes pathogenic compounds (Gaskins, 1997). The gastrointestinal tract has multiple non-specific and immunological defence mechanisms. The non-specific defence includes gastric acid production, peristaltis, mucus layer, tight junctions, epithelial desquamation, proteolysis, resistance against colonisation of pathogenic bacteria and the gut-liver axis. The immunological defence of the small intestine includes the production of secretory immunoglobulins, M-cells and lymphocytes (Madara et al. 1990; Walker and Owen, 1990; Deitch, 1993; Wang, 1995). Components of the intestinal barrier are shown in Figure 8.2. Concurrent absorption of nutrients and exclusion of pathogenic compounds is achieved through concerted actions of the small intestine. For example, tight junctions are crucial for baseline intestinal barrier function, but regulation adapts them to the uptake of nutrients (Madara, 1989). That the small intestine has two

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Epithelial barrier function Luminal factors

transcellular

paracellular Phospholipid layer Mucus layer Tight junction M-cell Enterocyte

Epithelial factors

Goblet cell

Macrophage

Mast cell

Lymphocyte Leukocyte

Submucosal factors

Lymph tube

Capillary

Lymph node

Reticuloendothelial system

Spleen

Liver Other organs

Figure 8.2. Schematic presentation of the gastrointestinal defence barrier and effector factors (After Wang, 1995).

functions is reflected in the difficulty to interpretate numerical values as to small intestinal integrity. Commonly used indicators of small intestinal integrity are villus length, crypt depth, number of goblet cells, mucus production, transepithelial permeability, inflammation, brush border enzyme activity and animal performance. These indicators and their relation to the process of weaning are discussed briefly below. 8.2.1

Small intestinal morphology

The depth and shape of the crypts of Lieberkühn, the shape and height of the villi and the number of goblet cells are indicators of intestinal integrity. The villus orientation and shape has been classified by Mouwen (1972), with classes including tongue-shaped, finger shaped, leaf-shaped, ridged-shaped and convoluted villi. Small intestinal integrity is most commonly assessed by histologic measurements of villus height and crypt dept. Weaning causes a reduction in villus height and an increase in crypt depth (Hampson, 1986; Miller et al., 1986; Cera et al., 1988; Dunsfort et al., 1989; Hall and Byrne, 1989; Kelly et al., 1991a; Nabuurs et al., 1993; Pluske et al., 1996a; 1996b). Villous atrophy after weaning is caused by a combination of increased rate of cell loss and reduced rate of cell renewal (Pluske et al., 1997a). The histological changes are smaller with higher post-weaning feed intakes (Kelly et al., 1991b; McCracken et al., 1995; Van Beers-Schreurs, 1996;

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Pluske 1996b). Ideally, specific diet formulations for weanling piglets should ameliorate the weaning-induced decrease in villus height. 8.2.2

Mucus production

The mucus protects the mucosa against digestive secretions, pathogens and physico-chemical damage (Mantle and Allen, 1989; Stokes and Bourne, 1989; Forstner and Forstner, 1994). Binding of pathogens to mucins rather than to epithelial cells is generally regarded as an important host defence mechanism (Forstner and Forstner, 1994). Mucus gel is stored in the intestinal goblet cells and secreted by baseline or accelerated secretion (Lamont, 1992). Baseline secretion is continuous and provides renewal of the mucus coat that is lost due to erosion, digestion and luminal digesta flow. Accelerated secretion is characterised by rapid, massive goblet discharge in response to physiological or pathological stimuli (Lamont, 1992, Epple et al., 1997), including inflammatory mediators (Specian and Neutra, 1982; Cohen et al., 1991; Plaisancié et al., 1998) and bacterial toxins (Roomi et al., 1984; Cohen et al., 1991, Epple et al., 1997). The actual amount of mucus secreted cannot be measured. An increase in the number of goblet cells might point to increased mucus production. Weaning of piglets has been shown to result in either unchanged (Dunsford et al., 1991; McCracken et al., 1999) or decreased (McCracken et al., 1995) numbers of goblet cells in the villi, and unchanged (McCracken et al., 1995; Spreeuwenberg et al. 2001) or decreased (Dunsford et al., 1991) numbers of goblet cells in the crypts. The importance of the number of goblet cells as an indicator of intestinal integrity seems limited due to the inconsistent response to weaning. 8.2.3

Transepithelial permeability

Small intestinal integrity can be estimated on the basis of intestinal permeability for macromolecules, which can be measured as passive diffusion of a marker compound. Ideal markers cross the intestinal epithelium by non-mediated diffusion, are recovered quantitatively after oral administration, and can be reliably measured in blood or urine by a convenient technique (Uil et al., 1997). Various probe molecules have been used to measure intestinal permeability, including the sugars lactulose and mannitol (Uil et al., 1997), horseradish peroxidase, ova-albumin and chromium-labeled ethylene diamine tetra-acetate (51CrEDTA) (Vellenga, 1989; Bjarnason et al., 1995). Transepithelial transport can also be measured with the use of Ussing chambers. An intestinal biopsy is placed in an Ussing chamber separating the mucosal and serosal site of the tissue. The marker is added at the mucosal site. At given time points the serosal fluid is sampled to measure the amount of marker that has crossed the epithelium. The transepithelial electrical resistance (TEER) and short circuit current (Isc) may also be measured. The TEER has been suggested to reflect tight junction function (Wirén

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et al., 1999), whereas the Isc reflects ion pump activity (Wirén et al., 1999). With increased paracellular transport of markers it is anticipated that mucosal integrity is diminished and that pathogens and toxins may cross the epithelial barrier. Weaning results in increased paracellular transport for mannitol in transport chambers (Verdonk et al., 2001). Plasma xylose concentration after oral administration was similar in weaned and unweaned piglets (Pluske et al., 1996b). Thus, the formulation of diets for weanling piglets may aim at reducing the paracellular transport of an appropriate marker in an intestinal biopsy placed in a transport chamber. 8.2.4

Inflammation

If and when bacteria or other deleterious agents cross the first line of defence and reach the connective tissue of the lamina propria, their metabolites or mediators liberated from epithelial cells may evoke an inflammatory response (Gaskins, 1997). The different T-cell subsets or major histocompatibility complex (MHC) classes indicate the status of small intestinal immunity. Class I MHC molecules interact with CD8-positive T cells which usually have a cytotoxic function. Class II MHC molecules interact with CD4-positive T cells which provide help to the antigenic peptide recognition (Shanahan, 1994). The measurement of pro-inflammatory cytokines provides information as to local inflammation. The production of interleukin-1 (Il-1), Il-6 and tumor necrosis factor (TNF) occurs rapidly following infection, tissue injury and trauma. The cytokines activate receptors on different target cells, leading to a wide range of effects, including anorexia, fever and acute phase protein production (Gruys et al., 1999), and also inhibition of growth (Johnson, 1997). Weaning results in an inflammatory response as measured by an increased production of Il-1 at day 1 and 2 post weaning (McCracken et al., 1995). However, the production of TNF is unchanged when compared to the production rates at the day of weaning (McCracken et al., 1995). With an average digestible energy intake of 1575 kJ during the first four days after weaning, the ratio of CD4 to CD8 positive T cell subsets decreased compared to the ratio at the day of weaning, which might point to an inflammatory response (Spreeuwenberg et al., 2001). Thus, the formulation of diets for weanling piglets may aim at reducing inflammation. Interleukins are indicators, which measure an inflammatory response directly. Decreased ratios of CD4 to CD8 positive T cells or MHC II to MHC I classes are indirect indicators of an inflammatory response. 8.2.5

Brush border enzyme activity

The enzyme activity of the brush border and pancreas may also serve as indicators of small intestinal function. The maturing enterocytes embedded in the apical membrane of the small intestine synthesise enzymes to hydrolyse disaccharides and small peptides (Caspary, 1992). Enzyme production of enterocytes during the

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weaning transition of piglets is determined by villus height and maturity of the enterocytes (Smith et al., 1985; Miller et al., 1986). In general, the brush border enzyme activity increases markedly when going from the bottom of the crypt to the tip of the villus (Miller et al., 1986; Fan et al., 2001). The increased enzyme activity at the villus tip is consistent with enterocyte differentiation (Fan et al., 2001). Enzyme activity may be expressed in units produced per time interval (total enzyme activity), in units per gram of brush border membrane protein (specific activity) or units per cm of small intestine. Weaned piglets have low specific activity of sucrase, lactase (Hampson, 1986; Miller et al., 1986; Kelly et al., 1991a) and isomaltase (Miller et al., 1986) when compared to unweaned piglets of the same age. The effect of weaning on disaccharidase activity is less pronounced when the pigs are weaned at an older age (Miller et al., 1986). Activities of maltase II and maltase III increase in response to weaning at six weeks of age when compared to unweaned piglets of the same age, but show no change in four-week-old pigs (Miller et al., 1986). Pluske and colleagues (1997b) showed that maltase and glucoamylase activities increased with age (2 versus 4 weeks of age) and with day postweaning. Kelly and co-workers (1991a) reported increases in specific activities of maltase and glucoamylase at 7 days post weaning when compared to sow-reared piglets of the same age. The discrepancy in response of various disaccharidases specific activities compared to weaning might be explained by substrate induction through the weaner diet. Efird and colleagues (1982) found an increased amount of trypsin and chymotrypsin in the intestinal contents (g / kg body weight) and a decreased amount of pancreatic trypsin and chymotrypsin (g / kg body weight). The sum of trypsin and chymotrypsin activities tended to be lower in weaned piglets compared to sowreared piglets (Efird et al., 1982). Thus, the formulation of diets for weanling piglets may aim at stimulating the production of disaccharidase and pancreatic enzyme activity in order to maintain the digestive capacity. 8.2.6

Animal performance

The length and weight of the small intestine, the weight of the digestive organs, the average daily gain (ADG) and the health status are indicators of digestive development and capacity, and thus of intestinal integrity. These indicators are positively influenced by feed intake, which is the most important determinant. As mentioned above, high feed intakes after weaning counteract the weaning-induced negative changes in indicators of gut integrity. A major goal of formulating diets for weanling piglets is to stimulate feed intake.

8.3

Modulation of small intestinal integrity by luminal nutrition

During periods of stress, such as weaning, the nutrients that are required for cell turnover and maintenance of barrier function are critically important. These nutrients

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can be supplied via the intestinal lumen or via the splanchnic blood flow. Factors in response to ingestion and digestion of food acting on mucosal growth include cell loss, local nutrients, bulk properties and pH. Additionally, gastrointestinal hormones and nerves also act on mucosal growth (Johnson and McCormack, 1994), but are outside the scope of this review. The effect on intestinal integrity of route of nutrient supplementation, energy intake level and specific dietary components will be discussed below. 8.3.1

Modulation by route of administration

Exposure of the gastrointestinal tract to nutrients is essential for maintaining its integrity (Goldstein et al., 1985; Bishop et al., 1992; Park et al., 1998; Bertolo et al., 1999; Ganessunker et al., 1999; Burrin et al., 2000). The importance of the presence of food in the lumen of the gastrointestinal tract (luminal nutrition) on mucosal integrity can be assessed by intravenous (parenteral) feeding as the sole source of nutrition. Table 8.1 summarises studies comparing the effects of total parenteral nutrition (TPN) versus enteral nutrition (EN). Despite similar body-weight gain in all studies, total intestinal mass, mucosal mass, villus height and villus surface area were all markedly reduced in piglets receiving TPN compared to their conterparts receiving EN (Goldstein et al., 1985; Park et al., 1998; Bertolo et al., 1999; Ganessunker et al., 1999; Burrin et al., 2000). This observation indicates that TPN can supply adequate nutrients to sustain somatic growth, but for intestinal integrity nutrients have to be provided from the luminal site. Interestingly, the intestinal length was not affected by TPN, pointing at selective inhibition of mucosal growth (Park et al., 1998). The lack of enteral stimulation associated with the administration of TPN may alter the intestinal immune cells as shown by an increased number of CD4+ and CD8+ T lymphocytes (Ganessunker et al., 1999). Total mucosal dissacharidase activity was also decreased by TPN (Park et al., 1998). Park and co-workers (1998) showed that provision of enteral nutrition at 1% of normal intake was not sufficient for improvement of intestinal integrity compared to non-supplemented piglets. Total parenteral nutrition with enteral IGF-I (1000 µg/l) had no effect on intestinal development relative to TPN alone, but the dosage of IGF-I could have been too low (Park et al., 1998). Burrin and colleagues (2000) showed, in an elegant study, that the minimal enteral nutrient intake necessary for efficacy depends on the measure chosen. Piglets were fed by both intravenous and enteral nutrition, the contribution of the two routes to total feed intake being variable. Irrespective of the intestinal region studied, the amount of enteral nutrition required to increase mass and protein content was less than that required to stimulate proliferative activity as based on measurements of DNA content, crypt depth and BrdU (5-bromodeoxyuridine) incorporation. The protein mass of the proximal region of the intestine was more responsive to a

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• • • •

• EN (TPN solution) • TPN-IV • TPN- IP

II

III

EN (MR) TPN-IP + water TPN-IP + EN (MR) TPN-IP + EN (MR + IGF-I)

• weaned piglets, 6 weeks of age,

• EN (TPN solution) • EN (starter diet) • TPN-IV

I

Comparing TPN (IV and IP) vs. EN

postweaning

• similar intake • n=5 / treatment

crypt depth TPN-IP

• 0 intestinal length • ↓ villus height, ↓ crypt depth for TPN-IV, 0

(41%)

• 0 ADG • ↓ intestinal weight (60%), ↓ mucosal weight

• piglets, 2-4 d postpartum • duration experiment: 8 d

post weaning • similar energy and protein intake for all treatments • n=4, 5 or 6 / treatment

Comparing mean of TPN-IP across treatments vs. EN: • 0 ADG • ↓ in intestinal weight (47%), ↓ mucosal weight (49%), ↓ mucosal protein content (17%) • 0 intestinal length • ↓ villus height (24%), ↓ crypt depth (16%) • ↓ lactase and sucrase total activity

Comparing TPN-IV vs. EN (TPN solution): • 0 ADG • ↓ intestinal weight • ↓ villus height, 0 crypt depth, ↓ number of epithelial cells • similar lactase, maltase and sucrase specific activity

Observations c

• piglets, 1 d postpartum • duration experiment: 0, 7 d

10 kg • duration experiment: 0, 21 d • similar energy intake for all treatments: ± 711 kJ/kg/d • n=3 / treatment

Design

Treatments b

Ref. a

Table 8.1. Effect of route of feed administration on small intestinal integrity of weanling piglets.

sucrase specific activity for EN (starter diet) when compared to EN (TPN solution)

↑ lactase, maltase and

(MR) or TPN-IP+EN (MR+IGF-I) vs. TPN-IP

• no effect of TPN-IP+EN

•

Remarks

Diet-mediated modulation of small intestinal integrity in weaned piglets

153

154 Comparing increasing percentages of EN • proximal small intestine more sensitive to amount of EN then distal segment • 0 ADG • ↑ in wet weight and protein content in jejunum with from 40% EN onwards, in ileum from 60% EN onwards, ↑ in DNA content from 60% EN onwards • ↑ in villus height from 40% EN onwards, ↑ in crypt depth from 60% EN onwards • ↑ in lactase activity from 80% EN onwards

• piglets 7 d postpartum, 3.1 kg • duration experiment: 0, 7 d

Of diet supplied: • 100% TPN-IV • 10% EN + 90% TPN-IV • 20% EN + 80% TPN-IV • 40% EN + 60% TPN-IV • 60% EN + 40% TPN-IV • 80% EN + 20% TPN-IV • 100% EN

V post weaning

energy intake for all treatments: 900 kJ/kg/dag

• balanced for nutrient intake,

TPN-IV or via EN

• n=5 / treatment • TPN solution either fed via

• for EN

↑ energy and protein intake

Remarks

b

reference: I: Goldstein et al., 1985; II: Park et al., 1998; III: Bertolo et al., 1999; IV: Ganessunker et al., 1999; V: Burrin et al., 2000 Abbreviations: ADG: average daily gain; d: day; CD: cell differentiation molecutes, surface markers of leukocyte subsets; EN: enteral nutrition; IGF-I: insulin like growth factor; MHC: major histocompatibility complex; MR: milk replacer; TPN-IP: total parenteral nutrition fed intraportally; TPN-IV: total parenteral nutrition fed intravenously c 0: similar, ↑: increased, ↓: decreased, #: number

a

Comparing TPN-IP vs. EN • 0 ADG • ↓ in intestinal weight (50%) • 0 intestinal length • 0 villus height, ↓ in crypt depth (30%) • ↑ # goblet cells in villi (147%), 0 in crypts • ↑ # CD4+ and CD8+ T lymphocytes • ↓ in MHC-I (57%), 0 MHC-II in jejunum, ↑ in MHC-II in ileum (455%)

• piglets, 1 d postpartum • duration experiment: 0, 7 d

• EN (MR) • TPN-IP

IV post weaning • n=6

Observations c

Design

Treatments b

Ref. a

Table 8.1. Continued.

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Diet-mediated modulation of small intestinal integrity in weaned piglets

decrease in enteral nutrition than that of the distal region. In contrast, the proportion of enteral nutrition needed to increase cell proliferation showed much less regional variation along the gastrointestinal tract. The daily feed intake in the study was approximately 900 kJ⋅kg-1⋅d-1, corresponding with 2800 kJ for piglets of 3.1 kg (Burrin et al., 2000). Maintenance requirement for these piglets is approximately 1040 kJ ME⋅d-1 (NRC, 1998) so that they were fed at ≈ 2.7 × maintenance. Sixty percent of total feed intake in the form of enteral nutrition was necessary to sustain normal mucosal proliferation and growth, which corresponds to 1.6 × maintenance requirement. The piglets used in the experiments comparing the effects of TPN and EN were generally weaned at a very young age, i.e. 1 to 7 days postpartum. The young age relates to the fact that the piglets were used as a model for low birth-weight infants with low nutrient stores, high metabolic rate and immature gastrointestinal development. In piglets weaned at an older age (Goldstein et al., 1985) the results were comparable to those weaned at a younger age. Total parenteral nutrition is also used for critically injured patients (McCauley et al., 1996). The effect of early EN, in addition to TPN, on post-surgery infectious complications or bacterial translocation is not consistent. Some experiments show a reduction in infectious complications (Kudsk, 1994), but others show no effect on bacterial translocation (McCauley et al., 1996). A decreased mucosal integrity through lack of nutrients in the small intestine might reduce its immunological defence mechanisms. So, although TPN is generally used as a model for low birth weight infants or critically ill patients, it can very well be used to study the effect of enteral nutrition on small intestinal integrity. The effect of short-term starvation immediately after hatching in chickens has been investigated. Under commercial conditions, newly hatched pullets are usually refrained from feed up to a maximum of 48 hours. The delay in access to feed results in decreased body weight when compared to immediate access (Pinchasov and Noy, 1993; Uni et al., 1998; Noy and Sklan 1999), and also leads to decreased villus height and shallower crypts (Uni et al., 1998). Access to a non-nutritious bulk material in the form of sawdust to provide gut fill overcame the loss of body weight during short-term starvation to a similar extent as did access to dry or liquid feed (Noy and Sklan, 1999). This outcome indicates that mechanical stimulation by non-nutritious gut fill is important in the early feeding process. It is not known whether mechanical stimulation per se has positive effects on intestinal integrity in weanling piglets. 8.3.2

Modulation by level of energy intake

Table 8.2 summarises studies comparing the effect of level of feed intake on small intestinal integrity in early-weaned piglets. Underfed piglets show decreased daily

Concepts and consequences

155

156 • newly weaned piglets, 5 d

• ad lib MR • 60% restriction of ad lib

• • • •

• sow milk semi ad lib d • PD • sow milk pair fed with PD

II

III

IV

PD MR at Ma MR at 2.5 × Ma MR ad lib

postpartum • duration experiment: 5 d post weaning • n=18 / treatment

g/pig/d) • 75% restricted PD (± 50 g/piglet/d)

postpartum • duration experiment 0, 4, 7 d post weaning • n=6 / treatment

• newly weaned piglets, 28 d

pospartum • duration experiment: 0, 5 d post weanig • n=8 /treatment

• newly weaned piglets, 29 d

piglets were gavaged fed

Remarks

Comparing PD and sow milk pair fed with PD vs. sow milk semi ad lib • ↓ in ADG • ↓ in villus height, 0 crypt depth

Comparing MR fed at Ma vs. 2.5×Ma and ad lib • ↓ in ADG • ↓ mucosal protein content (21%) • ↓ villus height (29%), ↑ crypt depth (18%) • 0 plasma xylose concentration

•

↑ crypt depth for PD when compared to sow milk pair fed with PD at d 4

Comparing restricted vs. ad lib • energy intake not given • ↓ in ADG (42%) • ↓in small intestinal weight (51%), ↓ mucosal weight (56%), ↓ mucosal protein content 72%) • ↓ villus height (47%), ↑ crypt depth (7%) • ↓ # goblet cells in villi (34%) • ↑ # infiltrated cells in lamina propria (51%)

Comparing restricted vs. continuous PD • ↓ in ADG • ↓ in small intestinal weight (51%), 0 mucosal protein content • ↓ villus height (10%), ↓ crypt depth (15%) • 0 plasma xylose concentration

• newly weaned piglets, 14 d

• continuous PD (± 200

I

postpartum • duration experiment: 0, 30 d post weaning • n= 6 or 7 / treatment

Observations c

Design

Treatments b

Ref. a

Table 8.2. Effect of level of feed intake on small intestinal integrity of weanling piglets.

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Concepts and consequences • symposium paper

Remarks

reference: I: Kelly et al., 1991b; II: Núñez et al., 1996; III: Pluske et al., 1996b; IV: Van Beers- Schreurs, 1996; V: Lopez-Pedrosa et al., 1998; VI: Verdonk et al. 2001 b Abbreviations: ADG: average daily gain; d: day; Ma: maintenance; MR: milk replacer; PD: pelleted starter diet; c 0: similar, ↑: increased, ↓: decreased, #: number d semi ad lib: according to formula describing voluntary feed intake of piglets (NRC, 1998)

a

lib d

Comparing restricted vs. semi ad lib ↓ in villus height in proximal small intestine (19%), 0 crypt depth • ↑ in paracellular transport (48%), 0 transcellular transport

postpartum • duration experiment 0, 1, 2, or 4 d post weaning • n=6 / treatment

•

• newly weaned piglets, 26 d

• semi ad lib MR • 67% restriction of semi ad

VI

• n=6 / treatment

weaning

Comparing restricted vs. ad lib • ↓ weight /cm of the intestine, ↓ DNA, protein, triglyceride, cholesterol and phospholipid content in mucosa • ↓ villus height, ↑ in enterocyte losses • ↓ mucin levels in goblet cells

• weaned piglets, 7 d postpartum • duration experiment: 30 d post

• ad lib MR • 80% restriction of ad lib

V

Observations c

Design

Treatments b

Ref. a

Table 8.2 Continued.

Diet-mediated modulation of small intestinal integrity in weaned piglets

157

Vente-Spreeuwenberg and Beynen

gain, decreased intestinal and mucosal mass and decreased villus height (Kelly et al., 1991b; Núñez et al., 1996; Pluske et al., 1996b; Van Beers-Schreurs, 1996; LopezPedrosa et al., 1998; Verdonk et al., 2001). These piglets also have lower numbers of goblet cells in the villi (Núñez et al., 1996) with low levels of mucin (LopezPedrosa et al., 1998). The effect of low feed intake on crypt depth is inconsistent. Crypt depth was either increased (Núñez et al., 1996, Pluske et al., 1996b), similar (Van Beers-Schreurs, 1996; Verdonk et al., 2001), or decreased (Kelly et al., 1991b) for low versus high feed intake. Shallower crypts are thought to be associated with decreased cell renewal in the crypt and deeper crypts with increased cell proliferation (Pluske et al., 1997a). The reason for the differences between studies as to the response of crypt cells to underfeeding is not known. In general (Table 8.3), total enzyme activities were decreased and specific activities were increased in malnourished piglets. The increase in enzyme activity when expressed per gram of mucosal protein implies that the relative effect of malnutrition on total protein content of the small intestine is larger than that on enzyme activity. Alternatively, underfeeding leads to an increase in enzyme capacity per enterocyte.

Table 8.3. Comparing restricted versus unrestricted feed intake on small intestinal brush border dissacharidase activity. Reference a

I

unit

µmol/min/ mol/d µmol/min/ µmol/ µmol/min/ µmol/min/ µmol/ g protein g protein min/cm g protein g protein min/cm

Lactase Sucrase Maltase Isomaltase Glucoamylase Aminopeptidase protein content

0b ↑ 25% 0 nd 0 nd 0 (mg/g)

a

b

158

II

0 0 ↓ 55% nd ↓ 47% nd

↑ 83% ↑ 46% ↑ 22% ↑ 182% nd ↑ 31% ↓ 72% (mg/cm)

III

↓ 51% ↓ 56% ↓ 60% ↓ 22% nd ↓ 60%

0 0 nd nd nd ↓ 21% (mg/g)

IV

↑ 22% ↑ 37% ↑ 39% nd nd nd ↓ 113% (mg/cm)

↓ 123% ↓ 46% ↓ 38% nd nd nd

I: Kelly et al., 1991; II: Núñez et al., 1991; III: Pluske et al., 1996; IV: Lopez-Pedrosa et al., 1998 0: similar enzyme activity; ↑: increased enzyme activity in restricted versus unrestricted-fed piglets; ↑: decreased enzyme activity in restricted versus unrestricted-fed piglets; nd: not determined

Weaning the pig

Diet-mediated modulation of small intestinal integrity in weaned piglets

Because underfeeding is associated with a negative nitrogen balance it is likely that the increase in specific activity of digestive enzymes is caused by protein depletion of the intestine. Verdonk et al. (2001) showed increased paracellular transport of mannitol across the small intestinal epithelium in underfed piglets. Wirén and colleagues (1999) investigated the influence of starvation, anesthesia and surgical trauma in rats. Starvation only caused a decrease in villous height in the jejunum and an increase in paracellular permeability in the ileum and jejunum (Wirén et al., 1999). Yang and coworkers (1999) found an inverse relation between the ATP levels in jejunal mucosa and permeability in rats, indicating that low ATP levels are associated with increased permeability. Starvation lowers the TEER, which also points at impaired tight junction function being associated with increased permeability. Starvation also produced a decrease in short-circuit current, indicating a decrease in the ion pump activity (Wirén et al., 1999). So, underfeeding leads to increased paracellular permeability, which is associated with diminished mucosal integrity, so that pathogens and toxins may cross the epithelial barrier. It is possible to improve feed intake at weaning by the use of liquid feeding. In general, improvements in postweaning growth rates have been reported in most of the studies with piglets fed liquid feed versus dry feed. However, the efficiency of the feed utilisation is in general lower in piglets receiving liquid feed compared to those receiving dry feed, as reviewed by Jensen and Mikkelsen (1998). Water consumption also increased by supplying liquid feed (Russell et al., 1996; Schellingerhout et al., 2002b). Water and feed intake are positively correlated (Barber et al., 1989; Schellingerhout et al., 2002b ). Deprez and colleagues (1987) observed smaller morphological change in the distal jejunum and in the ileum when a liquid diet (water: feed = 2: 1; w/w) instead of a dry feed was offered to weaned piglets. Blanchard and colleagues (2000) studied in a 2 × 2 factorial design the effect of liquid or dry feed fed before and/or after weaning on villus architecture at 25, 50 or 75% along the small intestinal tract. Piglets fed liquid feed before and after weaning showed increased villus height at 25% of the small intestine when compared to the other treatments. Crypt depth and number of goblet cells were not affected by dietary treatment. However, in both studies investigating the effect of liquid versus dry feed on gut morphology, no information was given on actual dry matter intakes of the experimental groups. Therefore it is not clear whether the observed increased villus height is due to the liquid feed itself or due to the increased feed intake. 8.3.3

Modulation by dietary components

It is clear that luminal nutrition and level of feed intake per se affect gut structure and function. Functional feed ingredients may indirectly, through enhanced feed

Concepts and consequences

159

Vente-Spreeuwenberg and Beynen

intake, and / or directly, through specific effects, improve small intestinal integrity. In the following sections, the effects of specific nutrients on gut integrity are discussed with special attention given to actual feed intake as a possible confounder. 8.3.3.1

Protein

As to the effect of dietary protein on small intestinal integrity, there is ample work on comparing the effect of soy proteins with that of treated soy proteins or milk proteins. Table 8.4 summarises the reported effects of protein source on small intestinal integrity in early-weaned piglets. The inclusion in the diet of soybean meal instead of milk protein results in similar (Makkink, 1993; Makinde et al.,1996) or decreased ADG (Efird et al., 1982; Owsley et al., 1986; Dunsford et al., 1989; Li et al., 1991). Villus height after feeding soybean meal was either similar (Makkink, 1993; McCracken et al., 1999) or decreased (Dunsford et al., 1989; Li et al., 1991; Makinde et al., 1996). Zarkadas and Wiseman (2000a; 2000b) showed that the intake level of trypsin inhibitor as a component of soybean meal was negatively correlated to body-weight gain and villus height in weaned piglets. Feed conversion ratio (feed intake : weight gain) was positively correlated to the level of trypsin inhibitor intake (Zarkadas and Wiseman, 2000a). Crypt depth responded inconsistently and is either increased (Dunsford et al., 1989; Li et al., 1991), similar (McCracken et al., 1998; 1999; Makkink, 1993) or decreased (Makinde et al., 1996) by inclusion of soybean meal. The number of goblet cells was not affected by dietary soybean meal (Dunsford et al., 1991; McCracken et al., 1999). Makkink (1993) compared, skimmed milk powder, soy protein concentrate, soybean meal and fish meal with regard to small intestinal morphology. In the proximal and distal jejunum, the type of protein source in the diet did not affect villus length, crypt dept and intestinal weight. Within the experimental treatments, the level of feed intake affected villus architecture. To assess the effect of protein source per se, feed intake should be comparable as may be achieved by a pair-feeding or restricted-feeding regimen. Newport and Keal (1983) reported a decrease in ADG when milk protein was replaced by fish protein in the diet. However, the piglets were weaned as young as 2 d of age and were fed a liquid milk replacer. The piglets might have been too young to tolerate high levels of fish meal and the practical relevance of this trial can be questioned. We have compared the effect of protein from feather meal and skimmed milk powder, which both are low in anti-nutritional factors (ANFs). The piglets fed the two protein sources and used for measurements were selected on the basis of comparable feed intake. Villus architecture and growth were measured at 4, 7 and 14 days post weaning. ADG was increased by 72% during first two weeks post weaning when comparing piglets receiving the skimmed milk powder diet to those fed the feather meal diet. Across days, skimmed milk powder increased villus height (14%) and crypt depth (10%) compared to feather meal (Spreeuwenberg, 2002).

160

Weaning the pig

• newly weaned piglets, 21 d

Experiment 1 (dry feed) • MP • SBM Experiment 2 • MP (dry feed ) • MP (liquid feed) • CSBM (dry feed)

• CSBM • CSBM + 20 % DW • CSBM + 5% lard

I

II

Concepts and consequences pospartum • duration experiment: 1, 3, 14, 16, 28d post weaning • n=6 /treatment

• newly weaned piglets, 28 d

postpartum • duration experiment 1: 7, 14 d post weaning (n=6 / treatment) • duration experiment 2: 7, 14, 21 d post weaning (n=5 / treatment) • balanced diets for protein delivered by test component (re = 24%)

Design

Dietary variables b

Ref. a Remarks

Comparing CSBM vs. CSBM + DW • ↓ ADG (6%) • ↓ total trypsin units in intestine (32%), 0 total trypsin units in pancreas, ↑ chymotrypsin in intestine (31%), 0 total chymotrypsin in pancreas

protein content (re = 23.82 vs. 21.45 vs. 22.64) or lysine (1.21 vs. 1.09 vs. 1.22) • no data on feed intake

• diets not balanced on

Experiment 1: Comparing SBM vs. MP • no data on feed intake • ↓ ADG (50%) • 0 intestinal weight / cm, ↑ pancreas weight (19%), ↑ intestinal length (28%) • ↑ trypsin in intestine (63%), 0 trypsin in pancreas, 0 chymotrypsin in intestine, ↓ chymotrypsin in pancreas (29%) Experiment 2 Comparing CSBM vs. MP (dry feed) • ↓ ADG (49%) • ↑ intestinal weight (15%) and length (20%), 0 intestinal weight / length, ↑ pancreas weight (31%) • ↑ total trypsin in intestine (341%), 0 total trypsin in pancreas, ↑ total chymotrypsin in intestine (95%), ↓ total chymotrypsin in pancreas (61%)

Observations b, c

Table 8.4. Effect of protein source in the diet on small intestinal integrity of weanling piglets.

Diet-mediated modulation of small intestinal integrity in weaned piglets

161

162

• • • • •

• • • •

IV

V

MP 15.5% SBM 31.5% SBM Cowpea meal

MP SBM SPC extruded SPC SPI

Comparing SBM and CSBM vs. casein • ↓ ADG for SBM (30%) and CSBM (70%), ↓ FI for SBM (8%) and CSBM (51%) • ↓ in villus height for SBM (14%) and CSBM (9%), ↑ crypt dept for SBM (16%) and 0 for casein • 0 areas of Peyer’s patches, 0 # goblet cells in villi and crypts

• newly weaned piglets, 21 d

• casein • SBM • CSBM

III

pospartum • duration experiment: 0, 7, 14, 21 d post weaning • before weaning, half of piglets received creep feed • n=5 / treatment

• newly weaned piglets, 28 d

• •

•

•

• duration experiment: 7 d

and cowpea diet compared to control at d 7. ↑ villus height and similar crypt depth for SBM diets at d 21. ↓ villus height for cowpea diet at d 21

• ↓ ADG Cowpea compared to other diets. • ↓ villus height, ↓ crypt depth for SBM diets

• ↓ ADG at week 1 and 2 for SBM and SPC postweaning compared to MP, ↓ FI for SBM vs. SPC in newly weaned piglets, 21 d week 1, ↓ FI for MP vs. extruded SPC postpartum • ↓ villus height of all diets compared to MP, pigs were sensitised with the ↑ crypt dept for SBM compared to other respective protein source from d diets 7 to 12 of age • ↑ lymphocyte density for SBM compared to n=8 / treatment other diets balanced diets for protein and • ↑ IgG titers to soy proteins for SBM energy compared to other diets • ↓ xylose concentration in plasma for SBM and extruded SPC compared to SPI or MP

postpartum • duration experiment: 0, 3, 6, 9, 12, 15 post weaning • n=5 / treatment • balanced diets for protein delivered by test component (re = 20%)

Observations b, c

Design

Dietary variables b

Ref. a

Table 8.4. Continued.

• no data on feed intake

raw material

• cowpea was fed as a single

materials

• diets not balanced for raw

Remarks

Vente-Spreeuwenberg and Beynen

Weaning the pig

Concepts and consequences

• • • •

of protein in diet: • 0% FM + 100% MP • 35% FM + 65% MP • 52.5% FM + 47.5% MP • 70% FM + 30% MP

• SMP • feather meal

VII

VIII

IX

SMP SPC SBM FM

• newly weaned piglets, 21 d

• MP • SBM + SPC

VI

SMP from d 0-3, 0 FI from d 3-10. • ↑ pancreatic weights for SMP and SPC • 0 villus length, 0 crypt depth at d 6

postpartum • duration experiment: 0, 4, 7, or 14 d post weaning • n=6 / treatment • balanced diet for protein and lactose

• newly weaned piglets, 27 d

postpartum • duration experiment: 0, 5, 26 • n=7 / treatment • balanced diets for protein

depth were affected by level of feed intake

• villus height and crypt

Comparing feather meal with SMP • ↓ ADG (46%), ↓ feed efficiency (50%) • ↓ in villus height (12%), ↓ in crypt depth (9%)

comparable feed intake to avoid entanglement between protein source and feed intake

• piglets were selected for

Comparing different ratios of FM and MP in diets • diets fed as milk replacer • ↓ ADG and ↑ feed : gain with increasing FM content • ↓ pH, DM and total N in the stomach with increasing FM content, 0 total N in small intestine • 0 chymotrypsin and trypsin activity

• 0 ADG, ↑ FI for FM and SBM compared to

postpartum • duration experiment: 0, 3, 6, or 10 days post weaning • n=5 / treatment • balanced diets for protein

• newly weaned piglets, 2 d

Remarks

Comparing SBM + SPC vs. MP • weaning itself resulted in villus atrophy and • 0 FI d 0-4, ↑ FI d 4-7 intestinal inflammation • 0 villus height and crypt depth • 0 # goblet cells • 0 # CD8+ and CD4+ T cells, 0 concentration of prostaglandin 2

Observations b, c

• newly weaned piglets, 28 d

postpartum • duration experiment: 0, 0.5, 1, 2, 4, 7 d • n=10 / treatment • balanced diets for protein delivered by test component (re=20%)

Design

Dietary variables b

Ref. a

Table 8.4. Continued.

Diet-mediated modulation of small intestinal integrity in weaned piglets

163

164

XII

XI

• • • •

MP hydrolysed MP SPI hydrolysed SPI

• control • SDAP

SBM

• •

• •

intake • ↑ small intestinal weight per kg of body weight for piglets receiving SPI • ↓ specific activities of trypsin and chymotrypsin in the duodenum and pancreas by hydrolysis

• ↓ ADG with SPI, 0 with hydrolysis, 0 feed

• newly weaned piglets, 4 d pospartum adaptation in groups for 3 d duration experiment: 21 d after adaptation n=8 / treatment balanced diets for protein and lactose

Comparing SDAP vs. control: • ↑ ADG (26.8%), ↑ FI (24.5%), ↓ feed efficiency (3.2%)

• weaned piglets

• diets fed as milk replacer

published studies with SDAP

• review combining 15

Comparing SDAP and pair fed SDAP to • diets not balanced for DW+SBM vs. DW+SBM: protein (re=24 vs. 22) • ↑ ADG d 0-16 for SDAP, ↑ FI d 0-16 SDP, 0 • feed intake of pair fed ADG and FI for d 0-4 and 0-8 animals is lower than feed intake of control • ↓ small intestine weight / kg of body weight at day 16, ↓ DNA and protein content at day 16 • 0 villus height, crypt depth, mucosal thickness • 0 5-bromo-2’-deoxyuridine labeling • ↓ intravillus lamina propria cell density in the proximal jejeunum at d 4, 8 and 16

postpartum • duration experiment: 0, 2, 4, 8, 16 d post weaning • n=8 / treatment

• newly weaned piglets, 14 d

• DW + SBM • SDAP • SDAP pair fed to DW +

X

Remarks

Observations b, c

Design

Dietary variables b

Ref. a

Table 8.4. Continued.

Vente-Spreeuwenberg and Beynen

Weaning the pig

Concepts and consequences

• • • • •

untreated SBM acid treated SBM acid hydrolysed SBM MP SPC

• newly weaned piglets, 29 d

Comparing vs. untreated SBM postpartum • ↑ ADG (0-7d) for hydrolysed SBM (63%) and MP (48%), 0 ADG 0-14, 0-21d., ↑ FI (0-21d) for • duration experiment 8-11 d post weaning hydrolysed (12%) and acid treated (13%) SBM • n=24 / treatment, growth • 0 villus height, crypt depth, villus area performance • 0 aminopeptidase, lactase, maltase, ↑ sucrase for hydrolysed SBM (100%) and SPI (92%) • n=4 / treatment, intestinal integrity (specific activity) • 0 antibody titres • 0 plasma xylose

for hydrolysed and normal SPI. 0 villus height at day 5 and 10 at proximal jejunum, 0 villus height at all days at mid and distal jejunum, ↑ crypt depth at mid small intesinte at d 2 for hydrolysed and normal SPI, 0 crypt depth other days and segments • 0 # CD8+ T cells and prostaglandin concentration

• ↓ diarrhoea with hydrolysed SPI at d 2 • ↓ villus height at proximal jejunum at d 2

compared to normal SPI, 0 FI

• tendency for ↑ ADG for hydrolysed

Observations b, c Remarks

reference: I: Efird et al., 1982; II: Owsley et al., 1986; III: Dunsford et al., 1989; 1991; IV: Li et al., 1991; V: Makinde et al., 1996; VI: McCracken et al., 1999; VII: Makkink, 1993; VIII: Newport and Keal, 1983; IX: Spreeuwenberg, 2002; X: Jiang et al., 2000; XI: Van Dijk et al., 2001; XII: Leibholz, 1981; XIII: McCracken et al., 1998; XIV: Rooke et al., 1998 b Abbreviations: ADG: average daily gain; CD: cell differentiation molecutes, surface markers of leukocyte subsets; CSBM: corn + soybean meal, DW: dried whey, FI: feed intake; FM: fish meal, MP: milk protein, SBM: soybean meal, SDAP: spray dried plasma protein, SMP: skimmed milk powder, SPC: soya protein concentrate, SPI: soya protein isolate c 0: similar, ↑: increased, ↓: decreased, #: number

a

XIV

• newly weaned piglets, 2 d.

• casein • SPI • hydrolysed SPI

XIII pospartum • duration experiment: 0, 2, 5 and 10 d after adaptation for 5 d • n=4 / treatment • balanced diets for protein

Design

Dietary variables b

Ref. a

Table 8.4. Continued.

Diet-mediated modulation of small intestinal integrity in weaned piglets

165

Vente-Spreeuwenberg and Beynen

Van Dijk and colleagues (2001) conducted a multiple regression analysis and concluded that dietary sprayed dried animal plasma (SDAP) levels up to 6% in the diet increase both average daily gain and feed intake in the first 2 weeks after weaning in a dose-dependent fashion. The positive effect of SDAP was more pronounced in the first than in the second week after weaning. It is suggested that the positive effect of SDAP can be explained by increased feed intake, and possibly also by specific bioactive components preventing attachment of pathogenic E. coli to the intestine (Van Dijk et al., 2002). Villus height, crypt depth and cell proliferation were unaffected by SDAP (Jiang et al., 2000; Van Dijk et al., 2001). Due to health risks associated with the use of non-sterilised products of animal origin as feed ingredients, SDAP may be banned as an ingredient for animal feed. Unravelling the mechanism underlying the positive effect of SDAP would be important for further developing functional feeds. However, the positive effect of SDAP seems mainly to occur via stimulation of feed intake. The early-weaned piglet has limited capacity to digest dietary proteins. By enzymatic hydrolysis of feed proteins, protein digestibility and availability for earlyweaned piglets might be improved. It is difficult to draw general conclusions about the efficacy of hydrolysed proteins because the conditions of processing and enzymes used are variable, leading to different hydrolysis products. Treatment of soy proteins has been shown to ameliorate effects of ANFs and to decrease the serum antibody immunoglobulin G titers (Li et al., 1991). Rooke and co-workers (1998) showed lower antigenic protein contents in hydrolysed soybean meal, but no effect on antibody titers. When comparing soybean meal with hydrolysed soybean meal, ADG was either similar (Leibholz, 1981) or increased (McCracken et al., 1998; Rooke et al., 1998), and gut wall architecture was not different (McCracken et al., 1998; Rooke et al., 1998). McCracken and colleagues (1998) showed less postweaning diarrhoea after feeding diets with hydrolysed soy protein isolate instead of either soy protein isolate or milk protein. However, there was no diet effect on intestinal numbers of goblet cells, mast cells, T cells, local production of prostaglandins and local expression of MHC genes, demonstrating that the type of protein did not influence inflammation when fed to piglets weaned 2 d post partum (McCracken et al., 1998). Poullain and colleagues (1989) compared the effects of alimentary whole whey protein, whey protein oligopeptides and an amino acid mixture in rats. Growth and nitrogen retention after starvation followed by realimentation was highest for rats receiving the oligopeptides. Weanling rats recovering from severe starvation by feeding either a casein hydrolysate or the native protein had similar weight gain. However, intestinal permeability for ovalbumin remained increased only in the group refed with the casein diet (Boza et al., 1995). Possibly, the feeding of hydrolysed protein more effectively counteracts the weaning-induced impairment of gut integrity than does feeding of the intact protein.

166

Weaning the pig

Diet-mediated modulation of small intestinal integrity in weaned piglets

8.3.3.2

Amino Acids

Amino acids taken up by the intestinal mucosa are derived from the blood and from the intestinal lumen. Stoll and colleagues (1998) conducted tracer balance studies with radioactive amino acids and measured amino acid incorporation into mucosal protein in piglets. The authors concluded that 60% of the essential amino acids taken up from the intestinal lumen were catabolised by the intestine. The amount of catabolised amino acid was equivalent to at least 20% of the essential amino acids consumed and was directly related to the mucosal mass (Stoll et al., 1998). This not only implies intestinal mass determines the efficiency of dietary protein utilization, but also that the availability of luminal amino acids is important for maintaining the mucosal mass and thus mucosal integrity. Individual amino acids may have a specific role in regulating intestinal integrity and function (Wu, 1998). Glutamine, glutamate and aspartate are major fuels for small intestinal mucosa and support ATP-dependent metabolic processes such as active nutrient transport and high rates of intracellular protein turnover. Ornithine, which is derived from arginine, glutamine and proline, is the immediate precursor for polyamine synthesis, which is essential for proliferation, differentiation and repair of intestinal epithelial cells. Arginine is the physiological precursor of nitric oxide (NO), which plays an important role in processes such as vasodilation, immune responses, neurotransmission and adhesion of platelets and leucocytes (Wu and Morris, 1998). Glutamate, glycine and cysteine are precursors for the synthesis of glutathione, a tripeptide critical for defending the intestinal mucosa against toxic and peroxidative damage (Wu, 1998). Thus dietary glutamine is involved in the energy supply of the intestine, while the other amino acids through conversion have regulatory properties. We are not aware of studies on the effect of dietary supplementation of aspartate, glycine, cysteine or proline on small intestinal integrity of the weaned pig as measured by histology, specific enzyme activity and permeability. Supplementation to the diet of either 0.6% or 0.93% arginine did not affect growth performance and villus height (Touchette et al., 2000; Ewtushik et al., 2000). The effects of glutamine have been repeatedly studied. Whilst not considered to be an essential amino acid, L-glutamine is an abundant free amino acid in the plasma of animals (Wu et al., 1996) and in sow’s milk (Wu and Knabe, 1994). As mentioned above, glutamine is a major energy source for the gut and supports nucleotide biosynthesis, but it also serves as an ammonia scavenger and preserves the immunological function during total parenteral nutrition (Windmueller, 1982; Alverdy, 1990; Souba 1993; Salway, 1995). Glutamine can be taken up with feed, but it can also be formed from glutamate and NH4+ in an ATP-requiring reaction catalysed by glutamate synthetase. Hydrolysis of the terminal amide group of glutamine by glutaminase results in formation of glutamate and ammonia. As an energy source, glutamate

Concepts and consequences

167

Vente-Spreeuwenberg and Beynen

readily enters the Krebs cycle following oxidative deamination by glutamate dehydrogenase into α-ketoglutarate. Complete oxidation of 1 molecule of glutamate generates 12 molecules of ATP. A study by Houdijk and colleagues (1994) showed that feeding a glutamine-enriched diet increased the splanchnic blood flow in the rat. Thus extra glutamine provides energy in itself and indirectly by increasing the blood flow to the intestine. Glutamine, but not glutamate, plays a role in nucleotide metabolism as it donates the nitrogen atoms which form N-9 and N3 of the purine ring (Salway, 1995). Depending on the activity of glutamine synthetase, glutamate can substitute for glutamine in purine metabolism. A disadvantage of glutamine for dietary supplementation is its instability. Degradation of glutamine can be minimised by the addition of L-glutamine shortly before administration or by the use of a more stable form, e.g. L-alanyl-L glutamine or L-glycyl-L-glutamine. Dipeptides are rapidly hydrolyzed to their respective amino acids (Lacey and Wilmore, 1990), but are relatively expensive. Table 8.5 summarises the reported effects of glutamine on the small intestine. In newly-weaned piglets plasma concentrations of glutamine are reduced when compared to unweaned, suckling piglets (Ayonrinde et al., 1995a). Some experiments with weaned piglets showed no effect on villus height with either 1% (Kitt et al., 2001) or 1.2% glutamine in the diet (Touchette et al., 2000). Some showed that 1% glutamine (Wu et al., 1996) or 6.5% glutamate (Ewtushik et al., 2000) had an effect on one site of the proximal small intestine but not further along the intestine. One study showed that 4% glutamine increased villus height in both the duodenum and ileum (Ayonrinde et al., 1995b). Wu and colleagues (1996) showed improved feed efficiency but similar growth during the second week postweaning when 1% glutamine was fed. In other studies, growth was either similar (Ewtushik et al., 2000) or increased by the addition of glutamine to the diet (Kitt et al., 2001). Lackeyram and colleagues (2001) noted increased growth with 0.8% glutamine, but no effect with either 1.6% or 2.4%. It may be concluded that the effects of glutamine supplementation on villus architecture and growth performance are equivocal. Perfusion of the epithelium of the ileum of weaned piglets with L-glutamine increased tissue viability as indicated by an increase in transmembrane potential difference (Smith et al., 1992). However, glutamine administration had no effect on tissue integrity as based on the TEER (Smith et al., 1992). Bacterial translocation of orally administered E. coli did not occur in either control or glutamine supplemented weanling piglets (Smith et al., 1992). Dugan and McBurney (1995) indicated that luminal glutamine is beneficial for the maintenance of normal mucosal permeability during endotoxicosis. Ileal perfusion with a glutaminecontaining solution effectively abolished endotoxin-induced increases in mucosal permeability in intestinal loops. In endotoxemic rats, glutamine-supplemented parenteral nutrition improved the morphology of the jejunal mucosa as based on

168

Weaning the pig

• newly weaned piglets, 21 d

Enteral nutrition • 4% gln • 4% gly

Enteral nutrition • 0% gln • 0.2% gln • 0.6% gln • 1.0% gln

• 0% glu, arg • 6.51% glu • 0.93% arg

I

II

Concepts and consequences

III postpartum • duration experiment: 0, 10 post weaning • n=7 / treatment

• newly weaned piglets, 12 d

postpartum • duration experiment: 0, 7, 14 post weaning • n=5 / treatment

• newly weaned piglets, 21 d

postpartum • duration experiment: 5 days • n=10 / treatment

Design

Dietary variables b

Ref. a

Comparing the addition of 0 vs. 6.51% glu • 0 ADG and FI • 0 organ weights • 0 sucrase, lactase, maltase specific and total activity • ↑ villus height duodenum, 0 villus height proximal and mid jejunum and ileum. 0 crypt depth

Comparing 1.0% vs. 0 % gln • 0 ADG and FI during week 1 and 2, ↑ ADG and feed efficiency during week 2 • ↑ villus height at 7 d post weaning at jejunum, 0 villus height at 7 d post weaning in duodenum and at 14 d post weaning in duodenum and jejunum, ↓ crypt dept at 14 d post weaning at jejunum, 0 crypt depth at 14 d post weaning in duodenum and at 7 d post weaning in duodenum and jejunum

Comparing addition of gln vs. gly • 0 ADG, 0 FI • 0 protein content (mg/cm gut),↑ DNA content (µg/cm gut) • ↑ villus height and crypt depth in ileum and jejunum. • ↑ jejunal glutaminase (µmol/h/cm)

Observations b, c

Table 8.5. Effect of glutamine on small intestinal integrity of early weaned piglets.

did not differ from control group

• Piglets receiving arginine

intake for piglets with morphology measurements • In growth trial piglets receiving 1% gln had numeric lower feed intake

• no information on feed

symposium paper

Remarks

Diet-mediated modulation of small intestinal integrity in weaned piglets

169

170 • newly weaned piglets, 18 d

• 0% gln • 1.0% gln

• 0% gln, arg • 1.2% gln • 0.6% arg

TPN: • 0% gln + 0% glu • 0.35% gln + 0% glu • 0% gln + 0.35% glu

IV

V

VI

0 ADG 0 plasma and jejunal mucosa concentration of gln and glu 0 intestinal weight, protein , DNA content or protein / DNA ratios • similar lactase, sucrase or maltase specific activities

Comparing the addition of 0 vs. 1.2% gln: • 0 ADG and FI • 0 villus height, ↑ crypt depth at d 14

adaptation

showed either 0 and ↓ crypt depth

• arg vs. control and gln

from 0-7 and 14-28

• arg vs. gln showed ↓ ADG

growth performance or villus height were not the same

• Piglets used to measure

• 0 ADG and FI from 0-14, ↑ ADG and FI from 14-21 • 0 villus height

Remarks

Observations b, c

• newly weaned miniature piglets, • 2 d postpartum • • adaptation period: 5 d • • duration experiment: 7 d post

postpartum • duration experiment (postweaning): 0, 7, 14 for histologic sampling. 0, 7, 14, 28 for growth performance • n=6 / treatment

• newly weaned piglets, 17 d

postpartum • duration experiment (postweaning): 0, 4 for histologic sampling. 0, 4, 7, 14, 21 for growth performance • n=4 / treatment

Design

Dietary variables b

Ref. a

Table 8.5. Continued.

Vente-Spreeuwenberg and Beynen

Weaning the pig

Concepts and consequences

perfused intestinal loops: • Ringer’s lactate solution • Ringer’s lactate solution + 2% gln • oxygen-purged Ringer’s lactate solution + 2% gln

VIII of clearance of 51Cr-EDTA and urea • administration of bacterial endotoxin • n=4 / treatment

• piglets 21 d postpartum • permeability estimated by ratio

administration for gln perfused loops, ↑ permeability for loops perfused with only Ringer’s lactate solution

• 0 permeability after endotoxin

Comparing weanling with gln vs. without • ↑ potential difference (=tissue viability) • 0 resistance (= tissue integrity) • no bacterial translocation

Observations b, c Remarks

reference: I: Ayonrinde et al., 1995b; II: Wu et al., 1996; III: Ewtushik et al., 2000; IV: Kitt et al., 2001; V: Touchette et al., 2000; VI Burrin et al., 1991; VII: Smith et al., 1992; VIII: Dugan and McBurney, 1995 b abbreviations: ADG: average daily gain; FI: average daily feed; glutamic acid: glu; glutamine: gln; glycine: gly; HBBS: Hanks Balanced Salt Solution; TPN: total parenteral nutrition c 0: similar, ↑: increased, ↓: decreased

a

• newborn piglets, 1 to 4 d

Using chambers perfused with: • newborn + HBBS (A) • weanling + HBBS (B) • A + 0.29% gln (C) • B + 0.29% gln (D) • C + E. coli • D + E. coli

VII postpartum • weanling piglets, 21 d postpartum • permeability measured with Using chamber • n=4-8 / treatment

Design

Dietary variables b

Ref. a

Table 8.5. Continued.

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increased villus height, crypt depth and wall thickness. In the glutamine group, the arterio - portal venous endotoxin difference after intravenous infusion of a lipopolysaccharide of E. coli was less negative, suggesting that the absorption of endotoxin across the gut was diminished through improved mucosal barrier function (Chen et al., 1994). Yoo and colleagues (1997) studied the proliferative response of lymphocytes to concanavalin A, which specifically activates T cells via binding to specific membrane receptors (CD3). The proliferative response in lymphocytes from pigs infected with E. coli and fed a diet without glutamine was depressed, whereas lymphocytes from infected pigs fed a diet with 4% glutamine responded similarly to those isolated from non-infected pigs. Both the control diet and the diet with extra glutamine contained 4.4% glutamate. It may be concluded that glutamine supplementation supports immune function during critical states, but has no clear effect in non-challanged weanling piglets. 8.3.3.3

Fat and poly-unsaturated fatty acids

The addition of fat at the expense of corn to pig starter diets does not consistently enhance growth rates and feed / energy conversion during the initial weeks post weaning (Li et al., 1990; Cera et al., 1990b, Mahan, 1991). However, during the second phase of the nursery period, the addition of extra fat improves daily gain and feed efficiency (Li et al., 1990; Cera et al., 1990b; Mahan, 1991), but energy conversion is not or slightly improved. The most pronounced effects of added fat on daily gain during the second period are seen with coconut, soybean and corn oil (Li et al., 1990; Cera et al., 1990b; Mahan, 1991). Cera and co-workers (1990a) showed that luminal lipase activity is low during the initial post-weaning period, but subsequently increases again. This observation confirms the increase in growth and feed efficiency with post-weaning age. Table 8.6 summarises the outcome of two studies on the influence of the fat source in the weaner diet on small intestinal morphology. Cera and colleagues (1988) showed that supplementation of the diet with 6% corn oil at the expense of corn reduced villus height in the small intestine of weaned piglets. However, feed intake data were not shown. However, body weight was similar in the low and high fat diet. Li and colleagues (1990) compared diets supplemented with either soy oil, coconut fat or a 50/50 mixture of these two fat sources. The piglets that received either coconut or soybean oil had shorter villi than did the piglets that received the fat mixture, but when compared to the control diet, fat supplementation did not affect villus height. Fat supplementation at the expense of corn resulted in deeper crypts, irrespective of the type of fat (Li et al., 1990). Likewise, in rats, the addition of 8% instead of 4% corn oil to the diet increased crypt cell proliferation resulting in deeper crypts (Pell et al., 1992). It may be concluded that the addition of extra fat to the diet increases crypt depth and may lower villus height in weanling piglets without affecting growth performance.

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• • • •

4 trials with: • control • white grease • soybean oil • coconut oil • soybean oil + coconut oil

II

III

0% DW + 0% corn oil 25% DW + 0% corn oil 0% DW + 6% corn oil 25% DW + 6% corn oil

• newly weaned piglets, 28 d

• CSBM • CSBM + DW • CSBM + 5% lard

I

18 and 21 d • diets balanced for lysine / energy ratio

• newly weaned piglets, between

postpartum • duration experiment 3, 7, 14, 21, and 28 d • n=6 / treatment • diets balanced on kcal ME / g lysine, increased ME content for diets with oil

• newly weaned piglets, 21 d

pospartum • duration experiment: 0, 14, 27, 29, 31, 42, 44, 56 postpartum • n=6 / treatment

Design

Dietary variables b

Ref. a

during first 2 weeks, ↑ ADG with addition of fat from week 3-5 post weaning, especially with combination of soybean and coconut oil • ↓ ileal DM digestibility with addition of fat • ↑ villus height with combination of soybean and coconut oil compared to soybean or coconut oil alone, 0 villus height with addition of fat compared to control, ↑ crypt depth with addition of fat compared to control

• 0 ADG, FE and ↓ FI with addition of 10% fat

Comparing 6% vs. 0% corn oil • 0 ADG and intestinal weight, ↑ pancreas weight at d 28 • ↓ villus height • ↑ total lipase in pancreas, 0 lipase / g pancreas, 0 lipase in intestine

• ↓ lipase activity after weaning

Comparing CSBM+ 5% lard vs. CSBM • ↓ ADG (10%) • 0 trypsin in intestine and in pancreas, ↑ trypsin per kg of pancreas (77%), 0 chymotrypsin in the intestinal contents and pancreas

Observations b, c

Table 8.6. Effect of fat source in the diet on small intestinal integrity of weanling piglets.

• no data on feed intake

content (ether extract (%) = 1.34 vs. 2.38 vs. 8.68) • no data on feed intake

• diets not balanced on fat

Remarks

Diet-mediated modulation of small intestinal integrity in weaned piglets

173

174

• • • •

Control Control + PUFA Malnourished Malnourished + PUFA

malnourished piglets during 30 days followed by 10 d refeeding with or without fatty • ↑ recovery in the morphology in malnourished piglets acids • 0 disachharidase and alkaline phosphatase activities • ↑ DNA, protein, cholesterol, phospholipid and triglyceride content in jujunal but 0 in ileal mucosa of malnourished piglets

• weaned piglets, 7 d post partum Comparing PUFA vs. no PUFA • malnutrition (20% of control) • ↑ weight per length ratio of the intestine for

• no data on feed intake and

Comparing oil vs. control • 0 # leukocytes and lymphocyts, 0 migration index of lymphocytes,. • 0 CD4+, ↑ CD8+, 0 CD2+ lympocytes • ↓ level of archidonic acid (ω6),↑ docosahexaenoic acid (ω6), ↑gammalinolenic acid (ω3), eicosapentaenoic acid (ω3) and docosahexaenoic acid (ω3) • ↑ growth factors • ↑ IgM (43%)

diet was supplemented with a phospholipid concentrate of ω-6 and ω-3 long chain fatty acids also containing cholesterol.

growth

Remarks

Observations b, c

b

reference: I: Owsley et al., 1986; II: Cera et al., 1988; 1990; III: Li et al., 1990; IV: Kastel et al., 1999; V: Lopez-Pedrosa et al. 1999 abbreviations: ADG: average daily gain; DM: dry matter; DW: dried whey; FE: feed efficiency; IgM: immunoglobulin M; PUFA: poly unsatturated fatty acids c 0: similar, ↑: increased, ↓: decreased, #: number

a

V

• suckling piglets, 4 d post

• control • oil: ω3:ω6 = 10:1

IV partum • n= 5 or 6 / treatment

Design

Dietary variables b

Ref. a

Table 8.6. Continued.

Vente-Spreeuwenberg and Beynen

Weaning the pig

Diet-mediated modulation of small intestinal integrity in weaned piglets

Polyunsaturated fatty acids can belong to either the omega-3 (ω-3) or omega-6 (ω-6) family of fatty acids. Soybean, corn and sunflower oil are fat sources rich in the ω-6 fatty acids. Linseed and fish oil are rich in the ω-3 fatty acids α-linolenic and eicosapentanoeic acid, respectively. The ω-3 polyunsaturated fatty acids have been investigated for use in the treatment of inflammatory diseases (Blok et al., 1996; Calder, 1998). Calder (1998) reviewed the effect of dietary fatty acids on the immune system and indicated that high-fat diets generally lower T-lymphocyte proliferation and natural killer cell activation when compared with low-fat diets. Among the fat sources in high-fat diets the order of potency was found to be: saturated fat (e.g. palm oil, coconut fat) < n-6 polyunsaturated rich oils (e.g. corn oil, soybean oil, sunflower seed oil) < olive oil < linseed oil < fish oil. Studies with experimental animals indicate that diets rich in ω-3 polyunsaturated fatty acids are anti-inflammatory and immunosuppressive in vivo (Calder, 1998). The effect of ω-3 and ω-6 polyunsaturated fatty acids has not been extensively investigated in piglets (Table 8.6). Kastel and colleagues (1999) found that oral administration of ω-3 polyunsaturated fatty acids to piglets affected the immune response. The production of ω-3 derived docosahexanoeic acid was significantly increased in the blood at the expense of ω-6 derived arachidonic acid. The production of IgM by B lymphocytes and growth factor (somatomedin C) was increased after ω-3 supplementation, but so was the production of cytotoxic T lymphocytes (Kastel et al., 1999). Lopez-Pedrosa and co-workers (1999) investigated the effect of feed restriction and combined ω-6 and ω-3 polyunsaturated fatty acid supplementation in a 2×2 factorial design. Extra fatty acids enhanced small intestinal recovery after feed restriction, but had only limited effect in well-nourished piglets. In weanling piglets, offering a diet containing linseed oil, which is rich in α-linolenic acid, visually improved assessed body condition but not growth performance when compared with a diet containing corn oil, which is rich in linoleic acid (Schellingerhout et al., 2002a). It may be concluded that the addition of ω-3 fatty acids to the diet of weanling piglets might have beneficial effects, especially when feed intake is low and hygiene status is suboptimal. 8.3.3.4

Fibres and non-digestible oligosaccharides

The term dietary fibre refers to plant carbohydrates, including pectins that resist hydrolysis by alimentary enzymes but can be fermented by the gastrointestinal flora. Dietary fibres cover a wide variety of substances with different physical properties and physiological effects. Some components are soluble, whereas others are insoluble; some have a high water-holding capacity, whereas others have a low or no water-holding capacity (Roberfroid, 1993). Soluble fibers may delay, whereas insoluble fibers may accelerate, small intestinal transit time, influencing contact time between digesta, enzymes and microbes. The major effect of soluble fibre is

Concepts and consequences

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Vente-Spreeuwenberg and Beynen

a reduction in starch hydrolysis and carbohydrate absorption, leading to a reduced and flattened glycemic response as well as reduced insulinemia (Bueno et al., 1981; Silk, 1989; Scheppach et al., 1990; Roberfroid, 1993; Mosenthin and Hambrecht, 1998). Soluble fibers may increase the thickness of the unstirred water layer covering the epithelial cells in the small intestine and thereby create a diffusion barrier that limits contact between intestinal enzymes and their substrates, and consequently reduces apparent enzyme activity. The increased unstirred layer may protect the mucosa against damage from particles. The reported effects of dietary fibres on small intestinal integrity in weaned piglets are shown in Table 8.7. In general, inclusion of fiber in the diet did not affect growth (Moore et al., 1988; Jin et al., 1994; Longland et al., 1994; Lizardo et al., 1997; Hambrecht, 1998; Gill et al., 2000). Small intestinal weight was either unchanged (Jin et al., 1994, Lizardo et al., 1997) or increased after fibre consumption (Hambrecht, 1998). Hambrecht (1998) reported an increased incidence of diarrhoea during the first 2 weeks after weaning with the inclusion of wheat bran in the diet, however over a 5-week period, there was no effect on the incidence of diarrhoea. Extra intake of fibre by weaned piglets increased total tract apparent digestibility of non-starch polysaccharides, but had no effect on total tract apparent digestibility of protein, dry matter and energy (Longland et al., 1994; Lizardo et al., 1997; Gill et al., 2000). Lizardo and colleagues (1997) showed in weanling piglets that faecal nutrient digestibility was similar for fibrous diets versus fibrefree diets, but apparent ileal nutrient digestibility was decreased. Jin and colleagues (1994) investigated the effect of 10% wheat straw in the diet on small intestinal architecture in weaned piglets. Villus height was not affected by dietary fibre, but the width of the villi and crypt depth were increased. Because the crypts are the principal site of cell proliferation in the intestinal mucosa, these data, in conjunction with the observed increase in cell proliferation and cell death, support the hypothesis that high fibre intake increases the rate of turnover of intestinal mucosal cells (Jin et al., 1994). Moore and coworkers (1988) showed no effect of dietary fibre on microscopic morphology. The effects seen in weaned piglets agree with those found in rats. In rats, supplementation of the diet with 10% guar gum also increased crypt cell proliferation, resulting in deeper crypts. However insoluble wood cellulose had no effect on crypt cell proliferation, which may be due to its poor fermentability (Pell et al., 1992). In rats, dietary supplementation with either guar gum or pectin increased crypt depth, crypt cell proliferation and the migration rate of cells along the crypt villus axis when compared to either a fibre free diet or diets supplemented with either cellulose or retrograded starch. The effects of the soluble fibres were more pronounced in the proximal and mid small intestine than in the distal small intestine. Villus height was not affected by the type and amount of dietary fibre (Brunsgaard and Eggum, 1995).

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Concepts and consequences

II

• • • •

CSBM OH SBH AM start of trial • n=3 / treatment • diets balanced for protein and energy

• piglets, 9.7 kg • duration growth trial 34 d post

• 0 morphology (shape of villi)

compared to others, 0 FI

• ADG and FE tended to be lower for AM diet

intestine, caecum and colon Comparing all three diets during 5 weeks: • ↓ FI in week 3, 4/5 for CWR. ↑ FE for CWR in week 4/5 • 0 in diarrhoea • ↑ weight of distal and similar weight of proximal small intestine for W / B • ↑ total VFA production in distal small intestine for W / B and CWR/WB and similar total VFA production in caecum and colon

• 0 total VFA production in distal small

intestine

• newly weaned piglets, 24 d post Comparing W and B vs CWR during 2 weeks: partum • 0 ADG, FI and FE • duration experiment: 14 or 35 d • ↑ incidence of diarrhoea post weaning • ↑ weight of proximal and distal small

• CWR • W and B • CWR, W and B

I

Observations b, c

Design

Dietary variables b

Ref. a

Table 8.7. Effect of fibers in the diet on small intestinal integrity of piglets. Remarks

Diet-mediated modulation of small intestinal integrity in weaned piglets

177

178 • weaned boars, 21 d post partum Comparing 15% with 0% SBP • 0 ADG, ADFI and FE • n=6 / treatment • ↑ TTAD of NSP (39%), 0 TTAD of N and • diets balanced for protein and

• 0% SBP • 15% SBP

Diet composition • 0 ADG, FI, FE • weaned piglets, 28 d post partum • 0 TTAD of N, DM, GE, ↑ TTAD of NSP • W • B • growth trial (n=6 / treatment), duration experiment 4 weeks • SBP Diet with or without enzymes post weaning • digestibility trial (n=4 / treatment), duration experiment 11 days post weaning

V

energy

energy

Comparing 10 vs. 0 % WS • 0 ADG, FI and FE • 0 weight of small intestine • 0 villus height, ↑ width of intestinal villi, ↑ crypt depth • ↑ rates of cell proliferation (5-bromo-2deoxy-uridine) in jejunum and colon • ↑ rate of programmed cell death in jejunum and ileum

IV

barrows, 14.3 kg n=4 / treatment duration experiment: 14 d diets balanced for protein and energy

• • • •

• 0% WS • 10% WS

Observations b, c

III

Design

Dietary variables b

Ref. a

Table 8.7. Continued. Remarks

Vente-Spreeuwenberg and Beynen

Weaning the pig

Concepts and consequences

• • • •

SBM SBM + SBP (12%) SFPC SFPC + SBP (12%)

Dietary variables b

partum • duration experiment 31 days • n=7 / treatment • diets are balanced for energy, protein and total lysin

• weaned piglets, 25 d post

Design Comparing 12% with 0% SBP: • 0 ADG and FI • 0 small intestinal weight and protein content.• ↑ TTAD of fibrous components, similar for other nutrients • ↓ ileal nutrient apparent digestibility • ↓ ileal N retention, ↑ faecal N retention, • ↑ dipeptidyl peptidase, N-aminopeptidase, alkaline phosphatase and similar maltase and γ-glutamyl transferase in the ileum, 0 enzyme activities in jejunum, 0 α-amylase, trypsin, chymotrypsin activity, ↑ lipase activity

Observations b, c

by ileo-rectal anastomosis

• ileal digestibilty measured

piglets were 56 days of age

• for enzyme activities,

Remarks

b

reference: I: Hambrecht, 1998; II: Moore et al., 1988; III: Jin et al., 1994; IV: Longland et al., 1994; V: Gill et al., 2000; VI: Lizardo et al., 1997 abbreviations: ADG: average daily gain, AM: Alfalfa meal; B: barley; CSBM: corn soybean meal; CWR: cooked white rice; FE: feed efficiency; FI: feed intake; NSP: non starch polysaccharides; OH: oat hulls; SBH: soya bean hulls; SBM: soybean meal; SBP: sugar beet pulp; SFPC: soluble fish protein concentrate; TTAD: total tract apperent digestibility; W: wheat, WB: wheat bran; WS: wheat straw c 0: similar, ↑: increased, ↓: decreased

a

VI

Ref. a

Table 8.7. Continued.

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Short chain fatty acids (SCFA) may be involved in increased proliferation of crypt cells caused by soluble fiber. In fistulated rats, SCFA infusion at a physiological dose increased the crypt cell production rate in the small and large intestine in a dose-dependent manner, the effectiveness being in the order n-butyric > propionic > acetic acid (Sakata, 1987). Fermentation of dietary soluble fibres by microbes leads to the generation of SCFA. The number of bacteria and SCFA production in the different segments of the small intestine are indicators of fermentative capacity. The stomach and proximal small intestine of the pig contain relatively low numbers of microbes (103-105 bacteria per ml of digesta). The distal small intestine (ileum), however, maintains a more diverse microbiota and higher bacterial numbers (108 per ml of digesta) than the upper intestine. The large intestine is a major site of microbial colonization and is characterised by large numbers of bacteria (10101011per ml of digesta) (Gaskins, 2000). In piglets weaned at 5 1/2 weeks of age, SCFA production (µmol/ g dry matter of digesta) in the distal small intestine was only 2 and 3% of SCFA production in the caecum and proximal large intestine, respectively (Hambrecht, 1998). Although the number of bacteria and SCFA production indicate that only limited fermentation occurs in the small intestine, Houdijk (1998) showed that of the fructooligosaccharides (FOS) added to a weaner diet at a level of 40 g / kg feed more than 90% was degraded pre-caecally. This observation indicates that fermentation takes place in the small intestine. Thus, it is feasible that the observed effects of soluble fibres on small intestinal integrity are mediated by SCFA. Non-digestible oligosaccharides (NDO) resist the hydrolysis by the alimentary enzymes. The pH of the ileal digesta decreased after addition to the diet of 4% FOS when compared to a negative control. An effect on pH was not detected with 1% FOS or either 1 or 4% transgalacto oligosaccharide in the diet. Short chain fatty acid production and number of bacteria in the ileal digesta did not differ between piglets fed diets with or without dietary oligosaccharides (Houdijk, 1998). The inclusion in the diet of 0.2% transgalactosylated oligosaccharide, 0.2% glucooligosaccharide, 0.2% lactitol (Gabert et al., 1995), 0.5% galactosyl lactose (Mathew et al., 1997), either 1 or 2% sucrose thermal oligosaccharide caramel (Orban et al., 1996) and 0.1% mannooligosaccharide (Kim et al., 2000) had no effect on the composition and activity of the microflora, the pH and the concentrations of SCFA and NH3 in the small intestinal digesta of weaned piglets. The incidence of diarrhoea was not affected either. It follows that NDO’s have no effect on small intestinal integrity in contrast to soluble fibres. The lack of effect of NDO consumption on SCFA concentration in the digesta may be explained by rapid absorption of SCFA. It could be suggested that soluble fibres not only act through generation of SCFA. Fibres and SCFA have accessory effects in relation to the small intestine. The inclusion of fibre in orally or intravenously supplied TPN prevented bacterial translocation

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to the mesenteric lymph nodes even in the absence of oral nutrients (Spaeth et al., 1990). Dietary soluble fibre may enhance the faecal excretion of bile acids and render them unavailable for the formation of intra-luminal micelles so that fat and cholesterol absorption be reduced (Roberfroid, 1993). SCFAs are avidly absorbed and at the same time stimulate colonic sodium and water absorption, thereby acting as anti-diarrhoeal agents (Silk, 1989; Scheppach et al., 1990). SCFAs, especially butyric acid, are preferred energy sources for colonocytes (Roediger, 1982). 8.3.3.5

Probiotics and lactic acid

It is reasonable to suggest that dietary measures which enhance colonisation resistance and / or translocation resistance against enteropathogenic E. coli will have a positive effect on the performance of weanling piglets. Colonisation and translocation resitance may be influenced by the feeding of antibiotics, probiotics, prebiotics and / or other ingredients that affect microbial ecology of the small intestine. In weanling piglets, antibiotics may be used therapeutically, but in the European Union most antibiotics have been banned for preventive use. In the weanling pig, the effect of feeding probiotics, i.e. live microorganisms with beneficial activity on the host, has been studied. The feeding of either 106 or 107 viable spores of B. licheniformis or 106 viable spores of B. toyoi when compared to a negative control improved growth performance in piglets with 31, 99, or 28 % respectively from 0 to 28 days postweaning (Kyriakis et al., 1999). However, the extremely high morbidity and mortality in the negative control group may caused the lower growth performance in the negative control group. Mortality was 44% in the negative control and on average 20% in the probiotic treated groups. The administration of commercial preparations of probiotics to weanling piglets either showed no effect (Jost and Bracher-Jakob, 1998), or increased growth performance by 4% when compared to a negative control (Inamoto and Waltanabe, 1998). Prebiotics such as fructooligosaccharides have been shown to specifically stimulate the growth of lactobacilli and bifidobacteria in the intestine, but as mentioned previously there is no evidence that these probiotics influence gut integrity in weanling piglets. Lactobacilli produce lactic acid, which is known to have antibacterial activity. In weanling piglets dietary lactic acid concentrations of 0.82.4% have been shown to stimulate feed intake and growth (Roth et al., 1993; Smolders et al., 2000). Likewise, the feeding of fermented feed, which is rich in lactic acid, also stimulated growth in weanling piglets (Jensen and Mikkeelsen, 1998; Scholten, 2001) and increased villus height (Scholten, 2001). Thus probiotics, lactic acid and fermented feed might be beneficial to weanling piglets, but it is not known whether there is a direct effect on gut integrity or that these compounds act through enhanced feed intake.

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8.3.3.6

Growth factors

Growth factors, especially epidermal growth factor (EGF) and insulin-like growth factors I and II (IGF-I and IGF-II), are present in the colostrum and milk of the sow. The concentration of EGF per ml colostrum or milk is 1.5 µ and 0.15 - 0.25 µg, respectively (Xu, 1996). The concentration of IGF-I per ml colostrum or milk is 0.07 - 0.35 µg and 0.004 - 0.014 µg, respectively (Xu, 1996). The growth factors stimulate growth, maturation and / or functional development of the intestinal tract (Kelly, 1994; Xu, 1996; Odle et al., 1996). Epidermal growth factor is a trophic peptide for the gastrointestinal mucosa and acts both from the lumen and the blood. Playford and colleagues (1993) showed that luminally-supplied EGF is rapidly hydrolysed by proteases in the small intestine of human subjects while in the fasting state. Hydrolysis was blocked by the presence of casein or a soybean trypsin inhibitor. It was hypothesised that EGF is digested by pancreatic enzymes in the fasting state, but is preserved when food proteins act as competitive substrates and / or block the active sites of these enzymes (Playford et al., 1993). Oral supplementation of 372 µg/day EGF, but not 124 µg/day, to weanling piglets partly counteracted the weaning-induce decrease in lactase specific activity. Small intestinal sucrase specific activity was increased at day 3 after weaning by a supplementation with the high dose of EGF. However, supplementation of EGF did not affect on the mucosal protein content and the villus : crypt ratio in the small intestine (Jaeger et al., 1990). Zijlstra and colleagues (1994) examined the effects of EGF given with a milk replacer (0, 500, or 1000 µg/l) on the recovery of piglets that were infected at 4 days of age with rotavirus enteritis. EGF increased villus length and lactase specific activity in a dose-dependent fashion. At the dose of 500 µg/l, effects were seen only in the proximal portion of the small intestine, whereas with the higher EGF level there also were effects further down the tract (Zijlstra et al., 1994). Houle and colleagues (1997) looked at the effect of oral IGF-I administration (500 µg/l milk replacer) in neonatal piglets until 7 and 14 days postpartum. Circulating concentrations of IGF-I did not change and growth, organ weights, mucosal RNA, mucosal DNA and mucosal protein content were not affected. Mean villus height in the proximal ileum tended to be higher and that in the terminal ileum was significantly higher in IGFI-treated piglets. In other regions of the intestine, no effect of IGF-I on villus architecture was detected. By day 14 after birth, sucrase and lactase specific activities were increased throughout the jejunum and ileum in IGF-I-treated piglets. On day 7, enzyme specific activity was not affected by IGF-I administration (Houle et al., 1997). The addition of IGF-I to sow’s milk so as to double the concentration of that present in sows’ colostrum was found to increase the length of the tight junctions by 23% in 36-hour old piglets. However, sows’ milk with a IGF-I concentration similar to that in sows’ colostrum did not affect tight junction structure. Thus at high intake levels IGF-I can modulate the tight junction structure and thereby influence intestinal permeability (Zarrinkalam et al., 1999). In rabbits intestinal transport of electrolytes and nutrients was measured with Ussing chambres. EGF

182

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supplementation to the perfusate up-regulated intestinal transport (Opleta-Madsen et al., 1991). In may be concluded that dietary supplementation of IGF-I and EGF has only limited effects on body or organ weight. Within the intestine, IGF-I and EGF increased sucrase and lactase activities without significantly increasing intestinal weight, length, villus architecture, protein or DNA content. Thus, IGF-I and EGF may regulate disaccharidase activities through modifying the function or differentiation of individual enterocytes. The action of orally administered IGF-I and EGF seems to be limited to the intestine without exerting systemic effects. So far the role of growth factors on intestinal development has been studied in neonatal and not in weanling piglets. Applications might be restricted to prophylactic administration of growth factors to enhance recovery from gastrointestinal trauma. 8.3.3.7

Polyamines

Polyamines are characterised by multiple NH2 groups in the molecule, representatives being putrescine, spermidine and spermine (Halász and Baráth, 1998). Polyamines have been shown to play a role in regulating growth of the gastrointestinal mucosa and also post-natal maturation, turnover of intestinal mucosa, binding of the vitamin D receptor to DNA, postprandial intestinal motility, transport of D-glucose and mucosal hyperplasia during lactation (Johnson and McCormack, 1994; Blachier, 1997; Halász and Baráth, 1998). Polyamines are present in sow milk (Kelly et al., 1991c). For the biosynthesis of the polyamines in animal tissue the precursors ornithine, which is not found in proteins but is synthesised from arginine, or L-methionine, are required (McCormack and Johnson, 1991). Polyamines are synthesised from L-arginine in absorptive cells, secreted by exocrine pancreas and provided by extruded enterocytes at the top of villi (Blachier, 1997). Polyamines are also produced by intestinal flora (Blachier, 1997). Wu and colleagues (2000a) showed that intestinal polyamine synthesis is enhanced after weaning of piglets at 21 days of age. Grant and colleagues (1990) studied the effect of polyamine supplementation to a liquid milk replacer fed to piglets weaned at 2 d of age. An all-milk-protein milk replacer was compared with the same milk replacer in which 20% of the protein was replaced with soy protein isolate without or with 25 g/l of either putriscine dihydrochloride or ethylamine hydrochloride. Daily gain, villus height and the kinetics of xylose absorption did not differ between dietary treatments. Crypt depth tended to be lowest in the milksoy diet without polyamines, but mitotic index was altered. Specific and total activities of sucrase in the brush border were highest for the piglets fed the all-milk diet. Specific activity of cytosolic dipeptidase was lowest for piglets fed the milk replacer with putrescine. Total dipeptidase activity was lower in piglets fed the diets with putrescine or ethulamine when compared to the milk diet. Grant and colleagues (1989) applied the same dietary treatments to 3-day old preruminant calves as well.

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The plasma xylose concentration was highest in calves receiving the milk diet. Enterocyte proliferation was decreased in calves fed the soy-milk diet without added polyamines when compared to the other diets. Thus supplementation of the milksoy protein diet with either putrescine or ethylamine enhanced enterocyte proliferation. Villus architecture was not affected by any dietary treatment (Grant et al., 1989). Oral daily supplementation of rats with 6 µmol spermine or 10 µ mol spermidine in rats increased sucrase and maltase specific activity and decreased lactase specific activity. Ileal villus enterocytes were maturer in either spermine or spermidine treated rats, when compared to control animals, as based on changes in enterocytes structure and dissacharase activities (Dufour et al., 1988). Osman and colleagues (1998) investigated the effect of spermine on intestinal permeability in rats by Ussing diffusion chambers. High spermine concentrations (10-50 mM) enhanced transcellular permeability, whereas low concentrations (0.5-1 mM) either had no effect or produced a decrease. Thus, spermine concentration has no straightforward action on epithelial barrier function. It is clear that administration of polyamines to rats induces intestinal maturation and increases proliferation. We are not aware of any studies on polyamine supplementation in piglets weaned at 3 weeks of age. However, polyamines added to a liquid milk replacer for either neonatal piglets or calves, did neither affect performance nor intestinal integrity. 8.3.3.8

Nucleotides

Nucleotides are building blocks of RNA and DNA, which can be either purine or pyrimidine nucleosides. Nucleotides may also function as energy source in cellular metabolism, influence lipid metabolism and serve as intermediates in biosynthetic and oxidative pathways. Nucleotides are important for immunity and gut development and repair (Boza et al., 1992; Carver and Walker, 1995; LeLeiko and Walsh, 1996; Nagafuchi et al., 1997). Cellular proliferation requires nucleotides derived either from glutamine, glycine and ribosylphosphates or from reuse of digested desquamated mucosal cells (LeLeiko et al., 1996). Bueno and colleagues (1994) fed weanling rats diets containing either corn starch or lactose for two weeks, followed by a 4-week period during which the corn starch diet with or without a nucleotide mixture was given. The lactose diet was used to induce diarrhoea. Rats that recovered from diarrhoea and received the diet with nucleotides showed increased villus height when compared to the rats not supplemented with nucleotides. However, rats that received the corn starch diet throughout did not benefit from nucleotide supplementation. This observation suggests that dietary nucleotides may improve intestinal healing after injury as induced by chronic diarrhoea. Adjei and colleagues (1996) fed mice either a casein diet, a protein-free diet, the protein-free diet with individual components of nucleotides / nucleosides or the protein-free diet with a nucleotide / nucleosides mixture to investigate the effect of diet on endotoxin-induced (E. coli O26:B6) bacterial translocation and small intestinal injury. Compared to the protein-deficient mice, dietary

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supplementation of a mixture of nucleotides and nucleosides or the individual component cytidine increased villus height and reduced the incidence of bacterial translocation. However, preventing protein malnutrition by feeding the casein diet resulted in higher villi and less bacterial translocation than did protein-free diet with a mixture of nucleotides and nucleosides (Adjei et al., 1996). The authors do not know published studies on dietary supplementation with nucleotides of weaner diets for piglets. However, in specific rodent models nucleotide supplementation may improve intestinal recovery after chronic diarrhoea or malnutrition.

8.4

Concluding remarks

Weaning is a stressful event as indicated by an increase of plasma cortisol concentration and behavioral changes (Worsaae and Schmidt, 1980). Plasma cortisol concentrations were more than 2.5 times higher in weanling pigs on day 2 postweaning when compared to unweaned pigs (Wu et al., 2000a; 2000b). Inappetance and low feed intake, lethargy, reduced activity and fever are prevalent during many types of stress (Elsasser et al., 2000). The transition from suckling to eating solid food is typically associated with a critical period of underfeeding (Leibrandt et al., 1975, Okai et al., 1976, Le Dividich and Herpin, 1994). Le Dividich and Herpin (1994) and Pluske and colleagues (1995) used various data sets and concluded that the daily metabolisable energy (ME) intake necessary for maintenance was not met until the fifth day after weaning. The level of preweaning ME intake was not attained until the end of the second week following weaning. Clearly, the weaning transition of piglets causes underfeeding. The low feed intake after weaning and the associated decreased mucosal integrity both negatively affect growth performance and health of the early-weaned pig. There generally is a high incidence of diarrhoea after weaning (Nabuurs, 1991). With early weaning being fundamental, nutritional interventions to counteract the weaninginduced decrease in mucosal barrier function should aim at increasing feed intake and / or the formulation of specific diet compositions. Experiments indeed confirm that feed intake level is critically important. Low feed intake is associated with decreased absorptive and digestive capacity as indicated by the decreased mucosal surface area and often low total brush border enzyme activities. Permeability of macromolecues, an indicator of small intestinal integrity, is increased by low feed intake. In contrast to feed intake level, dietary constituents studied thus far only have marginal effects on small intestinal integrity in the weaned piglet. The effect of dietary constituents generally is more pronounced in malnourished / diseased piglets when compared to apparently healthy weanling piglets. There are potential functional ingredients to improve the mucosal integrity, but data for weanling pigs are relatively scarce, even though the weaned piglet is a good model for human infants (Reeds et al., 1997). Most studies on potential functional dietary ingredients have been conducted with rodents or neonatal piglets

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instead of piglets weaned at 3 weeks of age. In the nutrition of monogastric farm animals, emphasis has been on anti-nutritional factors (Van Weerden and Huisman, 1989) and only recently researchers have started to explore the functional properties of certain feed contituents. Regarding the diet of weanling piglets, research should focus on critical determinants of feed intake immediately after weaning and functional feed ingredients to stimulate epithelial cell proliferation and differentiation, enhance immune function, and promote growth of beneficial bacteria. Combinations of functional feed ingredients may be more successful than the use of single ingredients. The cost-efficiency of the ingredients will determine their application in practice.

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9

Interactions between the intestinal microflora, diet and diarrhoea, and their influences on piglet health in the immediate post-weaning period D.E. Hopwood and D.J. Hampson

Summary The piglet is subjected to many environmental, behavioural and dietary stresses immediately after weaning, and the intestinal microenvironment of the newly weaned pig is particularly precarious. With weaning comes a major change in diet that requires and induces significant changes in the types and numbers of microorganisms residing in the gastrointestinal tract, as well as in the physiology and functionality of the tract. Given these circumstances, it is not surprising that the newly weaned pig is highly susceptible to enteric disease. The balance between development of a “healthy” intestinal microflora or the establishment of bacterial intestinal disease can be easily tipped toward disease expression (Aumaitre et al., 1995; Nabuurs, 1995). This chapter briefly describes the basic intestinal microflora present during the post-weaning period, specific enteric diseases that can occur at this time, and some potential precipitating dietary factors. Particular emphasis is placed on Escherichia coli and its involvement in the condition known as postweaning colibacillosis (PWC), since this is the most common cause of intestinal disease in the newly-weaned pig. The role of dietary fibre in altering susceptibility to PWC receives special attention.

9.1

Changes in intestinal microflora at weaning

During and shortly after birth, piglets are exposed to micro-organisms within their immediate environment. Ingestion of the sow’s faeces at this time introduces bacteria that colonise the gastrointestinal tract. These bacteria then localise to suitable niches where they compete and interact, and ultimately form a relatively stable and complex population that represents the normal intestinal microflora. Following initial establishment, the intestinal microbiota remains relatively stable except for times of major dietary and environmental change, such as occurs following weaning (Radecki and Yokoyama, 1991; Conway, 1994; Jensen, 1998). Pigs generally have a relatively large number of bacteria both in the stomach and the distal small intestine compared to other species. Consistent with this, considerable microbial fermentation occurs in the stomach and the small intestine, particularly in the ileum where the rate of passage of digesta slows and bacterial numbers are high (Jensen,

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1998). Whilst the piglet is suckling, the dominant bacteria within the stomach and small intestine tend to be lactobacilli and streptococci, both of which are welladapted to utilise substrate from the milk diet. The large intestinal microbiota that develops shortly after birth comes to contain a large and diverse selection of mainly obligate anaerobic bacteria, including Bacteroides, Eubacterium, Bifidobacterium, Propionibacterium, Fusobacterium, and Clostridium species (Radecki and Yokoyama, 1991). The metabolic activity and physical presence of this complex and stable microflora provides a “colonisation resistance”, preventing or reducing colonisation by other more transient bacteria, including potentially pathogenic species (Nurmi and Rantala, 1973). Following weaning, particularly if this occurs abruptly, a brief period of starvation and then consumption of the new solid diet results in altered availability of specific microbial substrate at sites all along the tract. The amount and type of substrate available at the different sites is influenced by the type and amount of food consumed after weaning, as well as by the relative functional capacity of the pig’s gastrointestinal tract after weaning. The process of abrupt weaning induces quite profound changes in intestinal structure, with associated disrupted functional capacity, and it can take several weeks for full, efficient and appropriate functionality to be restored (Hampson, 1986; van Beers-Schreurs, 1996; Pluske et al., 1997). Concurrently, these intestinal changes result in changes to the mass, composition and complexity of the intestinal microflora. Jensen (1998) quantified changes in bacterial populations that occur in the small and large intestine of pigs following weaning at 28 days of age. In the small intestine the previously predominant lactobacilli decreased in number during the first week after weaning, whilst the total number of bacteria and the proportion of coliforms, Escherichia coli in particular, increased. Immediately after weaning, most of the cultivable bacteria from the lumen of the large intestine are Gram-negative. In the study by Jensen (1998), microbial activity in the large intestine was not significantly increased until 20 days after weaning, whilst in the small intestine it took only a week for the bacterial population to establish and undergo maximum fermentation. Following this period of perturbation to the intestinal microflora, it subsequently re-stabilises. For more detailed review of the porcine intestinal microflora, and traditional culturebased and modern molecular methodology for their detection and enumeration, the reader is referred to articles by Conway (1994), Stewart (1997), Mackie et al (1999), Jensen (2001), Gaskins (2001), Leser et al. (2002), and Pluske et al., (2002). Few of these studies have specifically focused on changes in the microflora of healthy pigs immediately after weaning, because this represents a dynamic and variable process which is difficult to monitor without using large numbers of pigs killed sequentially to obtain intestinal samples. For example, different microflora effects

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may be seen in pigs weaned at different ages (Franklin et al., 2002). The main message from this section of the chapter is that both the composition and stability of this microflora undergo disruption in the period immediately following weaning, thus leaving the piglet more susceptible to overgrowth with potentially disease-causing pathogenic bacteria.

9.2

Major enteric diseases at weaning

Diseases of the gastrointestinal tract in weaner piglets generally result in diarrhoea of one form or another. Such diseases may be associated with the colonisation and overgrowth of bacteria, viruses or intestinal parasites, or a nutritional imbalance causing irritation and/or increased luminal osmotic forces. Diarrhoea occurs as a result of inflammation of the intestinal tract, or from a disruption to the absorptive or secretory processes of cells lining the epithelium of the intestinal tract (LieblerTenorio et al., 1999), as well as from disorders of intestinal motility. Diarrhoea is manifest as an increase in the water content of the faeces, and (or) as an increased daily passage of faeces. Diarrhoea becomes visually apparent once the faecal water content exceeds about 80%. Diarrhoea that is caused by the activity of bacterial enterotoxins in the small intestine is alkaline and watery (eg E. coli “secretory” diarrhoea), whilst that associated with damage and/or loss of function of the epithelium and its brush border tends to be acidic and bulky (eg rotavirus or enteropathogenic E. coli “osmotic” diarrhoea). Where the seat of infection is in the large intestine, mucus is often present in the faeces, and if there is tissue damage then fresh blood may be present (eg swine dysentery). Bleeding from further up the tract usually results in dark tar-like faeces (eg following gastric ulceration). Viruses are not a major cause of diarrhoea immediately after weaning. Rotaviruses (rotavirus diarrhoea) and Coronaviruses (transmissible gastroenteritis, porcine epidemic diarrhoea) may proliferate in the small intestine after weaning, but are more usually a problem in younger suckling pigs (Fu and Hampson, 1987; Will et al., 1994). Where they do occur after weaning, they may predispose to or exacerbate problems rather than being the initial cause of the diarrhoea (Hampson et al., 1985; Cox et al., 1988). Swine fever can cause severe intestinal lesions and diarrhoea, but there are also systemic manifestations, and the disease is not just focused on newly weaned pigs. Infestation with the large intestinal parasite Trichuris suis can result in mucoid diarrhoea, and typically results when piglets are weaned onto a dirt floor, but this disease is not usually seen until later in the postweaning period. On the other hand, infection with coccidia usually occurs in the sucking period, where it causes a white diarrhoea. Bacteria that have been associated with diarrhoeal diseases after weaning include Escherichia coli (post-weaning colibacillosis/post-weaning diarrhoea, oedema disease) and Salmonella species, particularly S. enterica Serovar Typhimurium, and

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similar serovars (salmonellosis). Pigs usually become infected with salmonella after consumption of contaminated protein sources, or exposure to infected faeces from rodents or wild birds. Salmonellosis is most commonly seen in older weaner pigs, as is infection with the intestinal spirochaetes Brachyspira hyodysenteriae (swine dysentery: SD), and Brachyspira pilosicoli (porcine intestinal spirochaetosis: PIS), and with the intracellular bacterium Lawsonia intracellularis (porcine proliferative enteropathy: PPE). PPE and PIS are particularly common causes of generally mild but chronic diarrhoea, whilst salmonellosis and SD can cause severe illness, with dysentery (blood in the faeces), systemic signs, and sometimes death. Of all these bacterial diseases, post-weaning colibacillosis, caused by enterotoxigenic E. coli, is the one that is the most common and widespread in the immediate post-weaning period, and is the main focus of this chapter.

9.3

Post-weaning colibacillosis (PWC)

Post-weaning colibacillosis (PWC) is a major cause of post-weaning morbidity and mortality worldwide, resulting in large economic losses (Cutler, 1981; Cutler and Gardner, 1988). The anterior small intestine is the main focus of the infection, and is the site of the underlying fluid and electrolyte loss into the intestinal lumen, although the bacterium is present throughout the small and large intestine. It is common for Escherichia coli (a coliform bacteria) to appear in the faeces of pigs in increased numbers in the first week after weaning (Mathew et al., 1993). This can happen in both healthy and diarrhoeic pigs, although the number and proportion of potentially pathogenic strains of E. coli in the faeces of diarrhoeic pigs is higher (Kenworthy and Crabb, 1963; Svendsen et al 1977; Hampson et al., 1985; Hinton et al., 1985; Gyles, 1993). Most strains of E. coli are harmless, but those that cause diarrhoea after weaning are often distinguished by their capacity to lyse red blood cells, and are known as beta-haemolytic E. coli. This haemolytic activity is not considered to be a virulence factor in itself. Pigs displaying postweaning diarrhoea harbour massive numbers (up to 109 colony forming units [CFU] and higher) of such haemolytic E. coli in the small intestine, whilst there is minimal change in the populations of other bacteria in the tract (Smith and Jones, 1963). Although digesta flows relatively quickly through the small intestine, pathogenic E. coli possess surface structures called fimbriae, or pili, that attach to the enterocytes lining the small intestinal villi, or to the mucus covering the villi. Attachment prevents the bacteria from being flushed through to the large intestine, where there would be far greater competition for survival. The most common adhesins present in the E. coli strains causing PWC are known as K88 (or F4), and F18 (formerly F107), both of which display several antigenic variants (Francis, 2002). After attaching to and colonising the small intestine, haemolytic enterotoxigenic E. coli (ETEC) provoke hypersecretory diarrhoea through the release of specific enterotoxins. Secretion of chloride ions, sodium ions, bicarbonate ions, and water

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into the lumen is induced by the actions of a heat labile toxin (LT) binding irreversibly to the mucosal cells and activating the adenyl cyclase-cyclic AMP system (Argenzio, 1992). A second heat stable toxin (ST; variants STa and STb) inhibits the absorption of sodium and chloride ions from the lumen into the epithelial cell via the guanyl cyclase-cyclic GMP system (Gyles, 1993). The resultant excess volume of fluid and electrolyte in the gut lumen can be reabsorbed in the large intestine only if it is free from disease, has a well-developed microflora, and its physical capacity is not overloaded (Argenzio, 1992). Other less common virulence determinants possessed by certain strains of E. coli involved in some cases of PWC include production of the enteroaggregative E. coli heat-stable enterotoxin 1, whose function remains uncertain (Choi et al., 2001), and the presence of the attaching and effacing genes (Eae) encoding intimins in enteropathogenic E. coli (Higgins et al., 1997). These outer membrane proteins are involved in attachment of the bacteria to colonic enterocytes, preceding effacement of their microvilli and rearrangement of the enterocyte cytoskeleton (Nataro and Kaper, 1998). Other E. coli strains which proliferate in the intestinal tract of weaned pigs produce a verotoxin, which is involved in the production of oedema disease, a predominantly neurological condition sometimes accompanied by diarrhoea (Osek, 1999). The association between excessive proliferation of haemolytic ETEC in the intestines of weaned pigs and the development of diarrhoea was first noticed in the 1960s, and was subsequently confirmed in many studies (Richards and Fraser, 1961; Palmer and Hulland, 1965; Hill and Kenworthy, 1970; Armstrong and Cline, 1976; Okai et al., 1976; Bertschinger and Eggenberger, 1978; Thomlinson and Lawrence, 1981; Ball and Aherne, 1982; Hampson, 1983; Cooke, 1985). The disease was called post-weaning colibacillosis (PWC) and is characterised by diarrhoea, dehydration, weight loss, metabolic acidosis, changes in the hair coat and shivering (Hampson, 1994; MacKinnon, 1998; Bertschinger, 1999). In severe cases, and in the absence of specific treatment with antibiotics and/or electrolyte solutions, death results. Immunity to one strain of pathogenic E. coli does not protect from others, and successive infections can pass through herds. No effective vaccines are currently available to control the disease, and many strains show resistance to multiple antibiotics (Amezcua et al., 2002). Infections usually last between 4 and 14 days, and are spread between animals primarily by the faecal-oral route, but also by aerosols and probably fomites (Bertschinger, 1999). Research over the years has shown that most E. coli associated with post-weaning diarrhoea are enterotoxin producing, haemolytic strains. Disease-inducing haemolytic E. coli are usually restricted to a small number of serotypes, in particular O8, O9, O71, O115, O138, O139, O141, O147, O149, O157 and NT (Hampson, 1994; MacKinnon, 1998).

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9.4

Factors predisposing to post-weaning colibacillosis at weaning

9.4.1

The role of the small intestine

Although haemolytic ETEC have been identified as the primary infectious agent in PWC, there is abundant evidence to suggest that other factors are necessary for this disease to take hold (Madec et al., 2000). The act of weaning is an essential precipitating factor for the development of post-weaning colibacillosis, regardless of the age at weaning. Factors involved with the weaning process create an environment suitable for the proliferation of ETEC and other pathogens in the small intestine. Slower intestinal transit time and relative intestinal stasis immediately after weaning allow bacteria the opportunity to attach to the intestinal epithelium and time to multiply. Undigested food particles in the lumen of the small intestine supply substrate for bacterial growth, and there is no longer any protective passive immunity provided by sows’ milk. An inability to thermoregulate adequately often results in cold stress, which alters intestinal motility and is thought to be an important predisposing factor in the pathogenesis of PWC (Wathes et al., 1989). Social stresses from mixing, fighting and crowding trigger blood cortisol release, depressing the immune response to bacterial infection. Moving to a new pen environment causes increased antigenic exposure to microbes residing in fresh or dried faecal matter. The presence of other organisms such as rotavirus in the environment increases the likelihood and severity of disease occurring (Lecce, 1983; Tzipori et al., 1983), whilst poorer pen hygiene will also result in a greater antigenic load, as a result of faecal-oral cycling (Madec et al., 1998). Morphological changes and reduced functional capacity within the small intestine associated with weaning may contribute to the development of PWC. Small intestinal villous atrophy and a reduced ability of the small intestine to absorb water and electrolytes at weaning are magnified when the small intestine is infected with haemolytic E. coli, thereby contributing to more severe diarrhoea (Nabuurs, 1998). The role of villus atrophy as a predisposing factor for PWC remains unclear, however, a reduced ability of enterotoxigenic E. coli to colonise has been found in pigs with experimentally-induced villus atrophy (Cox et al., 1988). Lack of familiarity with the new food source at weaning frequently results in anorexia followed by overeating, which starves the enterocytes lining the small intestine, and then overloads the digestive process. Overeating by individual pigs has been linked to an increased occurrence of PWC in these animals (Hampson and Smith, 1986). In the small intestine, E. coli fimbriae attach to glycoprotein receptors expressed in the brush border cells lining the intestinal villi. Receptors for F4 and F18 are not expressed in neonatal animals, but develop subsequently. Although receptors

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for F4 and F18 are still present in adult pigs, susceptibility to ETEC infection decreases with age (Erickson et al., 1992). Some pigs are resistant to PWC because they do not express the receptors at all, and some have receptors that are only weakly adhesive (Chandler et al., 1994). The presence of receptors varies between pig breeds (Baker et al., 1997), as well between individuals within a litter. Overall, this distribution has a strong influence on whether or not PWC will eventuate (Madec et al., 2000). 9.4.2

The role of the large intestine

There is growing evidence that the weaner pig’s immature large intestine influences the pathogenesis of nutritional and infectious diarrhoea (Bolduan et al., 1988; van Beers-Schreurs et al., 1992; Aumaitre et al., 1995; Hambrecht, 1998; Nabuurs, 1998; van Beers-Schreurs et al., 1998a; van Beers-Schreurs et al., 1998b). The large intestine is often viewed as a “salvage” organ. The populations of microbes residing there degrade and utilise undigested food and sloughed cells, whilst the epithelial cells reabsorb significant amounts of water and electrolytes along with volatile fatty acids (VFA) produced from microbial fermentation. The three-week old pig can absorb considerable water and electrolyte from its large intestine (Hamilton and Roe, 1977), even in the face of small intestinal villous atrophy (Argenzio et al., 1984). The capacity for intestinal resorption of water and VFA is similar in weaned or unweaned piglets, however, the pig’s absorptive capacity becomes greater within approximately two weeks after weaning. In the few days after weaning, the absorption of VFA does not augment the absorption of water (van Beers-Schreurs et al.,1998a), as it does in adult pigs (Argenzio, 1992), and these few days are a vulnerable time for the piglet. There is evidence that the reduced large intestinal absorption during this period may exacerbate the effects of enterotoxins in the small intestine (Nabuurs, 1998). Some authors recommend providing a weaning diet that results in higher VFA concentrations, especially butyrate, in the large intestine to maximise the absorptive function of the epithelial cells (van Beers-Schreurs et al., 1998b). This can be achieved by inclusion of fibrous ingredients in the diet. Dietary fibre is not digested in the small intestine, but subsequently is fermented in the large intestine to produce VFA. 9.4.3

The specific role of diet

The composition of the weaning diet has a central role in the pathogenesis of enteric disease, as it influences intestinal morphology, digestive and absorptive ability, intestinal motility and transit time, and selective growth of the microflora and their resultant fermentation patterns. Whether changes in the microflora at weaning will culminate in disease depends on the nature, number and activity of the specific bacteria present. Expression of PWC in particular depends on the existence of a

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range of dietary and other predisposing factors, with a greater number of risk factors acting in concert carrying a greater risk of disease occurring (Madec et al., 1998). It has been known for a long time that it is possible to influence the development of PWC by changing the composition of the weaner diet (see review by Hampson, 1987). Some highly digestible and milk-based diets have been associated with reduced clinical evidence of post-weaning diarrhoea, although the presence of E. coli has not always been monitored (English, 1981). Conversely, there is evidence that diets high in dietary fibre provide some protection from this disease (Bertschinger and Eggenberger, 1978; Bolduan et al., 1988; Aumaitre et al., 1995). In addition, components of some feed, such as soybean, are considered harmful in weaner pigs as they have been implicated in invoking intestinal mucosal damage (Li et al., 1990; Li et al., 1991), and intestinal fluid accumulation (Nabuurs et al., 1996). High levels of dietary protein have been suggested to predispose to PWC due to their high acid-binding capacity in the stomach, which then allows ETEC to escape the less-acidic environment of the stomach and colonise the small intestine (Prohaszka and Baron, 1980). The source of dietary protein used in feed formulation also has received some attention with regard to PWC. Diets containing complex or large number of protein sources may increase severity of diarrhoea compared to diets with few sources of protein (Okai et al., 1976; Ball and Aherne, 1982; Etheridge et al., 1984). Excess protein within the intestines is degraded by microbes, and may contribute to a proteolytic diarrhoea irrespective of E. coli presence, producing harmful amine by-products which irritate the mucosa and induce diarrhoea (Nollet et al., 1999). Plasma protein, however, is popular in some countries, particularly the US, as a spray-on additive for weaner feeds, and has shown to markedly improve the growth performance and robustness of pigs after weaning (Ermer et al., 1994). 9.4.4

The specific role of dietary non-starch polysaccharides in PWC

As previously mentioned, dietary fibre has been shown to influence intestinal physiology and the microflora in weaner pigs. Recently we have been investigating the influence of the type and level of dietary fibre on the expression of PWC (McDonald et al., 2000; McDonald, 2001; McDonald et al., 2001; Hopwood et al., 2002), and some concepts arising from this work are presented here. In this work, newly-weaned pigs were offered diets containing different levels of dietary fibre in the form of non-starch polysaccharide (NSP). Pigs fed these diets were either monitored for the development of natural infection with PWC, or experimentally infected with a pathogenic haemolytic ETEC strain. In these experiments a highly digestible diet, the main ingredient of which was cooked white rice, was used as a control diet because it is very low in dietary NSP (less than 1% of the diet). In the other test diets, sources of NSP replaced the cooked rice

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component so that the chosen NSP source comprised the major carbohydrate source in these diets (greater than 50% inclusion). The protein and energy contents of the different test diets remained essentially unchanged. The foods providing the sources of NSP were selected according to the type of NSP they contained. They were comprised of the following: mixed, approximately equal amounts of low viscosity soluble (easily fermented) and insoluble (slow to ferment) NSP (hammermilled wheat and extruded wheat diets), primarily soluble NSP of a moderate viscosity (pearl barley diets), and a highly viscous soluble synthetic NSP that resists large intestinal fermentation (carboxymethylcellulose diet: CMC). As added variables, a diet based on a hydrolysed form of rice was also offered to pigs as a comparison with the control cooked white rice diet, and exogenous digestive enzymes were added to the pearl barley diet to determine whether they could reverse any effects induced by the presence of soluble NSP. For all experiments, Large White x Landrace pigs from a specific pathogen free piggery were weaned at 21 days of age and transported to a research facility, where they were allocated to an experimental diet in a manner that ensured the average pig weight was the same for all experimental groups. From the day of weaning until the end of each experiment, faecal swabs were collected and cultured daily for the presence of haemolytic ETEC. An estimate of the proportion of faecal ETEC that grew from these swabs was recorded. Pigs that became naturally infected with PWC harboured ETEC of serotype O149;K91;K88 (enterotoxins LT, STa, STb). Where experimental infection was carried out, pigs were orally inoculated 48-72 hours post-weaning with 5-50mls of a broth containing an average of 108.5 haemolytic ETEC/ml of serotype O8;K88;K87 (enterotoxins LT, STb, STab) or O149;K91;K88 (enterotoxins LT, STa, STb), the latter being the same serotype cultured from the natural infection which occurred in pigs from this source. Pigs experimentally infected with ETEC began excreting the bacteria in their faeces within 24 hours of inoculation, and the severe watery diarrhoea that followed soon after was associated with a heavy, almost pure growth of haemolytic ETEC in their faeces. Pigs that naturally developed PWC began excreting heavy growths of haemolytic ETEC within a day of developing diarrhoea, usually 4-5 days after weaning. As the numbers of haemolytic ETEC cultured from faecal swabs can reflect the growth of E. coli within the large intestine, rather than in the small intestine where they stimulate diarrhoea (Armstrong and Cline, 1977; Sarmiento, 1988), growth from faecal swabs was not taken as the only indication of colonisation and proliferation of haemolytic E. coli. A more accurate method of determining the site of proliferation was by making viable counts of the bacteria from the intestinal contents. Counts from the small intestine of experimentally infected pigs have been reported to range from 2.7 to 9.7 CFU/g (log 10) (Smith and Halls, 1968), and similar counts

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were obtained in the current series of experiments. Scrapings from the small intestinal wall were collected from pigs killed 7-8 days post-weaning, 3-4 days after the commencement of diarrhoea. The viable counts obtained in these experiments allowed quantitative comparison between pigs fed different sources of NSP, and allowed an insight into the effect of infection on intestinal development. A summary of the viable counts of haemolytic ETEC from the mid-small intestine of all dietary groups with PWC is shown in Figure 9.1.

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The number of ETEC in the mid-small intestine and the expression of PWC increased as the amount of soluble NSP in the feed increased. In addition, all the natural sources of NSP that exacerbated PWC were soluble, readily fermented by intestinal bacteria, and tended to be viscous in nature, with greater viscosity being associated with higher ETEC numbers (Figure 9.2). The greatest proliferation of ETEC occurred as part of a natural infection, and was precipitated by the presence in the diet and in the intestinal digesta of the synthetic soluble viscous compound CMC. The distinguishing features of the diet containing CMC were its high water-holding capacity, highly viscous nature, high solubility and resistance to intestinal

a 2

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Figure 9.1. Viable counts of enterotoxigenic E. coli in the small intestine of pigs fed different diets. Effect of diet (vertical bars, P= 0.0001) on enterotoxigenic haemolytic E. coli numbers in the mid-small intestine of pigs with experimental or naturally-occurring PWC, and the corresponding % soluble NSP in the diet (line). Bars without the same letters represent diets that differ significantly. Rice = cooked rice/animal protein diet, HR = hydrolysed rice, Wheat = raw wheat diet, EW = extruded wheat, Barley +E = pearl barley with enzyme added, Barley = pearl barley diet, CMC cooked rice +4% carboxymethylcellulose (medium viscosity).

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0 Rice

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Figure 9.2. Comparison of intestinal enterotoxigenic E. coli numbers with intestinal viscosity of weaner pigs fed diets differing in soluble NSP content. Mean (±sem) enterotoxigenic haemolytic E. coli numbers in the mid-small intestine (vertical bars) and the corresponding mean viscosity of small intestinal contents (line) in groups of pigs with experimental or naturally-occurring PWC that were fed different diets. All diets contained cooked rice. The Barley and Barley+E (included enzyme) diets contained 50% of the diet as barley, and CMC was added to the cooked rice diet at 4% of the diet.

fermentation. The increased intestinal proliferation of haemolytic ETEC in pigs fed the non-fermentable, viscous CMC infers that low fermentability (which is also a feature of consuming the cooked white rice diet) is not a protective feature per se. Viscosity can in itself have a significant influence on the complex interaction between intestinal microflora, diet and enteric disease. This is a concept which is well accepted in poultry science (Choct and Annison, 1992; Langhout, 1998). The most significant and consistent result in all PWC infection experiments was the low level of intestinal proliferation of haemolytic ETEC in pigs fed the cooked rice diet. Although an occasional pig had moderate numbers of the bacteria in its intestinal tract, many of the pigs fed the cooked rice diet had minimal ETEC colonisation. Although not fully protective, the diet seemed to reduce the impact of the disease, and inhibit the ability of the bacteria to establish within the small intestine. The prominent features of the cooked rice diet were its highly digestible nature, low bulking properties, low viscosity and lack of fermentable substrates (i.e. dietary fibre). Highly digestible diets such as this provide energy to the

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individual, generally reducing both the impact of disease on the body and the duration of diarrhoea. This is the principle behind many oral rehydration solutions used to treat diarrhoea in humans. The cooked rice diet left little residue within the intestinal tract, and this is likely to have inhibited the growth of small intestinal pathogens by reducing the amount of available substrate. The piglet is unable to fully digest solid food immediately after weaning, resulting in food residues entering the large intestine (regardless of diet), where they undergo fermentation. This presence increases the osmolality of intestinal contents (Etheridge et al., 1984) and contributes to an influx of water into the lumen, potentially predisposing to diarrhoea (Etheridge et al., 1984). The presence of NSP, or any substance with strong water-holding capacity, is most likely to exacerbate this problem. Consistent with this principle, the cooked rice diet would have minimised this occurrence. The ability to significantly minimise the establishment of haemolytic ETEC was confined to the low-fibre cooked rice diet. In the last few years, research using guinea pigs has identified a substance in boiled rice that inhibits one of the mechanisms by which enterotoxins induce secretory diarrhoea (Mathews et al., 1999). It is possible that this substance contributed to the protective effect of cooked white rice seen in the experiments described here. Unexpectedly, consumption of the hydrolysed rice diet, which was of flour-like consistency, did not prevent the proliferation of ETEC. This lack of a protective effect may have been the result of the presence of an excess of easily-available starch in the small intestine, which acted as a substrate for bacterial growth. Addition of exogenous enzymes to the pearl barley diet also was not protective, perhaps because it increased the digestibility of the diet, so providing excess substrate for the bacteria in a similar way to the hydrolysed rice-based diet. Consistent with this idea of substrate in the small intestine being important in regulating E. coli numbers, diets that are high in insoluble NSP previously have been shown to reduce colonisation by haemolytic E. coli (Bertschinger and Eggenberger, 1978). In this case the insoluble fibre may physically trap substrate, preventing ETEC from gaining access to it in the small intestine. In addition to the abovementioned aspects of the experiments, all pigs with experimental or natural PWC had reduced whole body growth, and had less microbial fermentation within their large intestines than their healthy counterparts. All infected pigs fed any of the diets containing more than 1% dietary NSP lost weight post-inoculation. Subjectively, infected pigs eating the cooked rice diet (containing less than 1% NSP) were more alert and had a better appetite than pigs fed other diets, although this simply may have been a result of them remaining healthy whilst their littermates developed diarrhoea.

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Whether an invading pathogen will establish and proliferate in the intestinal tract depends upon the rate of its adhesion to the intestinal wall and the ability of normal regulatory factors to suppress the pathogen. These regulatory mechanisms include competitive exclusion (competition for nutrients or attachment sites) and the production of toxic metabolites that directly suppress pathogens or create adverse environmental conditions (Hentges, 1992). There are four habitats in which the bacteria can proliferate: the epithelial cell surface, within the mucus layer of the intestinal crypts, in the mucus lining the epithelium, and in the lumen of the intestines (Freter, 1974). Mucus can be beneficial or detrimental to the health of the animal, depending on whether it is used as an attachment site or whether it inhibits bacteria accessing the epithelial sites. The mucus layer lining the tract is thickened by the presence of viscous substances in the digesta (such as CMC), and increasing the amount of fibre in the diet also increases production of mucus. Not only does this increased thickness increase the distance for nutrients to move across prior to absorption (Blackburn and Johnson, 1981; Blackburn et al., 1984), but also it provides an attachment site for the haemolytic E. coli that is full of degraded nutrients required for bacterial growth. Escherichia coli have the ability to attach to mucins, which would reduce their initial establishment time by decreasing the distance required to access attachment sites. In fact, thicker mucus or more volume may allow more rapid establishment because there are, in effect, more attachment sites available. The primary bacteriostatic mechanism in the lumen of the intestines is that of mechanical forces. Slowing of mixing will allow bacterial proliferation, and it is feasible that both the presence of viscous and non-viscous fibre may interfere with mixing patterns and transit times. Interestingly, in older weaned pigs, the presence of fermentable and nonfermentable soluble, viscous NSP also can increase and hasten the onset of shedding of intestinal spirochaetes from the large intestine (Siba et al., 1996; Pluske et al., 1998; Hampson et al., 2000; Hopwood et al., 2002). Similarly, the highly digestible cooked white rice diet used in the PWC experiments described here has been the most successful diet for reducing or preventing the expression of experimental intestinal spirochaetal diseases (SD and PIS). These observations emphasise the need for further study on the underlying effects of viscous NSP on facilitating colonisation and proliferation of pathogenic enteric bacterial species in pigs.

9.5

Conclusions

Given that enteric diseases after weaning have a multifactorial origin, prevention should be aimed at reducing the number of predisposing risk factors present (Hampson, 1994; Madec et al., 1998; Bertschinger and Fairbrother, 1999). Three main means of manipulating the development of enteric disease stand out as being options that are easily implementable:

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1. Optimising the weaning environment (socially, thermally and hygienically), 2. Reducing the impact of weaning on the gut environment by optimising diet (composition, form, intake or additives), and 3. Manipulating the development and stability of the intestinal microflora through the judicial use of medication or diet (composition and specific antibacterial additives). In particular, diets that are easily digestible, and contain low concentrations of soluble NSP, are recommended for use in the control PWC.

Acknowledgements Parts of the work described in this chapter were undertaken with the financial support of Australian Pork Limited (the former Australian Pig Research and Development Corporation). At the time of conducting the work described, Dr Hopwood (née McDonald) was in receipt of a postgraduate scholarship from the former Corporation.

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Ermer, P. M., P. S. Miller and A.J. Lewis, 1994. Diet preference and meal patterns of weanling pigs offered diets containing either spray-dried porcine plasma or dried skim milk. Journal of Animal Science 72, 1548-1554. Etheridge, R.D., R.W. Seerley and T.L. Huber, 1984. The effect of diet on fecal moisture, osmolarity of fecal extracts, products of bacterial fermentation and loss of minerals in feces of weaned pigs. Journal of Animal Science 58, 1403-1411. Francis, D.H., 2002. Enterotoxigenic Escherichia coli infections in pigs and its diagnosis. Journal of Swine Health and Production 10, 171-175. Franklin, M.A., A.G. Mathew, J.R. Vickers and R.A. Clift, 2002. Characterization of microbial populations and volatile fatty acid concentrations in the jejunum, ileum, and cecum of pigs weaned at 17 vs 24 days of age. Journal of Animal Science 80, 2904-2910. Freter, R., 1974. Interactions between mechanisms controlling the intestinal microflora. American Journal of Clinical Nutrition 27, 1409-1416. Fu, Z.F. and D.J. Hampson, 1987. Group A rotavirus excretion patterns in naturally infected pigs. Research in Veterinary Science 43, 297-300. Gaskins, H.R., 2001. Intestinal bacteria and their influence on swine growth. In: A.J Lewis and L.L. Southern (editors). Swine Nutrition, 2nd ed. CRC Press LLC, Florida, pp. 585-608. Gyles, C.L., 1993. Escherichia coli. In: C.L Gyles and C. O. Thoen (editors). Pathogenesis of Bacterial Infections in Animals. Iowa State University Press, Ames, Iowa. pp. 164-187. Hambrecht, E., 1998. Effect of non-starch polysaccharides on performance, incidence of diarrhoea and gut growth in weaned pigs. Masters thesis, Hohenheim University, Stuttgart-Hohenheim, Germany. Hamilton, D.L. and W.E. Roe, 1977. Electrolyte levels and net fluid and electrolyte movements in the gastrointestinal tract of weanling swine. Canadian Journal of Comparative Median 41, 241250. Hampson, D.J., 1983. Post-weaning changes in the piglet small intestine in relation to growth checks and diarrhoea. PhD thesis, University of Bristol, Bristol, UK. Hampson, D.J., 1986. Alterations in piglet small intestinal structure at weaning. Research in Veterinary Science 40, 32-40. Hampson, D.J., 1987. Dietary influences on porcine post-weaning diarrhoea. In: J.L Barnett, E.S. Batterham, G.M. Cronin, C. Hansen, P.H. Hemsworth, D.P. Hennessy, P.E. Hughes, N.E. Johnston and R.H. King (editors). Manipulating Pig Production. Australasian Pig Science Association, Werribee, Victoria, Australia. pp. 202-214. Hampson, D.J., 1994. Postweaning Escherichia coli diarrhoea in pigs. In: C.L. Gyles (editor). Escherichia coli in Domestic Animals and Humans. CAB International, Wallingford, England. pp. 171-191. Hampson, D.J. and W.C. Smith, 1986. Influence of creep feeding and dietary intake after weaning on malabsorption and occurrence of diarrhoea in the newly-weaned pig. Research in Veterinary Science 41, 63-69. Hampson, D.J., M.H. Hinton, and D.E. Kidder, 1985. Coliform numbers in the stomach and small intestine of healthy pigs following weaning at three weeks of age. Journal of Comparative Pathology 95, 353-362.

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Hampson, D.J., I.D. Robertson, T. La, S.L. Oxberry and D.W. Pethick, 2000. Influences of diet and vaccination on colonisation of pigs with the intestinal spirochaete Brachyspira (Serpulina) pilosicoli. Veterinary Microbiology 73, 75-84. Hentges, D.J., 1992. Gut flora and disease resistance. In: R. Fuller (editor). Probiotics. The scientific basis. Chapman and Hall, London, pp. 87-110. Higgins, R.J., G.R. Pearson and C. Wray, 1997. Attaching and effacing E. coli. Microscopic and ultrastructural observations of intestinal infections in pigs. Advances in Experimental Medicine and Biology 412, 59-62. Hill, I.R. and R. Kenworthy, 1970. Microbiology of pigs and their environment in relation to weaning. Journal of Applied Bacteriology 33, 299-316. Hinton, M., D.J. Hampson, E.M. Hampson and A.H. Linton, 1985. A comparison of the ecology of Escherichia coli in the intestines of healthy unweaned pigs and pigs following weaning. Journal of Applied Bacteriology 58, 471-478. Hopwood, D.E, Pethick, D.W. and D.J. Hampson, 2002. Increasing the viscosity of the intestinal contents stimulates proliferation of enterotoxigenic Escherichia coli and Brachyspira pilosicoli in weaner pigs. British Journal of Nutrition 88, 523-532. Jensen, B.B. 1998. The impact of feed additives on the microbial ecology of the gut in young pigs. Journal of Animal and Feed Sciences 7, 45-64. Jensen, B.B., 2001. Possible ways of modifying type and amount of products from microbial fermentation in the gut. In: A. Piva, K.E. Bach Knudsen and J-E. Lindberg (editors). Gut Environment of Pigs. Nottingham University Press, Loughborough, England, pp.181-200. Kenworthy, R. and W.E. Crabb, 1963. The intestinal flora of young pigs, with reference to early weaning Escherichia coli and scours. Journal of Comparative Pathology 73, 215-228. Langhout, D.J., 1998. The role of the intestinal flora as affected by non-starch polysaccharides in broiler chicks. PhD thesis, Wageningen Agricultural University, Wageningen, The Netherlands. Lecce, J.G., 1983. Dietary regimen, rotavirus, and hemolytic enteropathogenic Escherichia coli in weanling diarrhea of pigs. Annales Recherches Veterinaires 14, 463-8. Leser, T.D., J.Z. Amenuvor, T.K. Jensen, R.H. Lindecrona, M. Boye and K. Moller, 2002. Cultureindependent analysis of gut bacteria: The pig gastrointestinal tract microbiota revisited. Applied Environmental Microbiology 66, 673-690. Li, D.F., J.L. Nelssen, P.G. Reddy, F. Blecha, J.D. Hancock, G.L. Allee, R.D. Goodband and R.D. Klemm, 1990. Transient hypersensitivity to soybean meal in the early-weaned pig. Journal of Animal Science 68, 1790-1799. Li, D.F., J.L. Nelssen, P.G. Reddy, F. Blecha, R. Klemm and R.D. Goodband, 1991. Interrelationship between hypersensitivity to soybean proteins and growth performance in early-weaned pigs. Journal of Animal Science 69, 4062-4069. Liebler-Tenorio, E. M., J. F. Pohlenz and S.C. Whipp, 1999. Diseases of the digestive system. In: B.E. Straw, S. D’Allaire, W.L. Mengeling and D.J. Taylor (editors). Diseases of Swine. Iowa State University Press, Ames, Iowa, USA. pp. 821-831. Mackie, R.I., A. Sghir and H.R. Gaskins, 1999. Developmental microbial ecology of the neonatal gastrointestinal tract. American Journal of Clinical Nutrition. 69, 1035S-1045S. MacKinnon, J.D., 1998. Enteritis in the young pig caused by Escherichia coli. The Pig Journal 41, 227-255.

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Madec, F., N. Bridoux, S. Bounaix and A. Jestin, 1998. Measurement of digestive disorders in the piglet at weaning and related risk factors. Preventative Veterinary Medicine 35, 53-72. Madec, F., N. Bridoux, S. Bounaix, R. Cariolet, Y. Duval-Iflah, D.J. Hampson and A. Jestin, 2000. Experimental models of porcine postweaning colibacillosis and their relationship to postweaning diarrhoea and digestive disorders as encountered in the field. Veterinary Microbiology 72, 295-310. Mathew, A.G., A.L. Sutton, A.B. Scheidt, J.A. Patterson, D.T. Kelly and K.A. Meyerholtz, 1993. Effect of galactan on selected microbial populations and pH and volatile fatty acids in the ileum of the weanling pig. Journal of Animal Science 71, 1503-1509. Mathews, C.J., R.J. MacLeod, S-X. Zheng, J.W. Hanrahan, H.P.J. Bennett and J.R. Hamilton, 1999. Characterization of the inhibitory effect of boiled rice on intestinal chloride secretion in guinea pig crypt cells. Gastroenterology 116, 1342-1347. McDonald, D.E. 2001. Dietary fibre for the newly weaned pig; influence on pig performance, intestinal development and expression of post-weaning colibacillosis and intestinal spirochaetosis. PhD thesis, Murdoch University, Perth, Western Australia. McDonald, D.E., D.W. Pethick, B.P. Mullan, J.R. Pluske and D.J. Hampson, 2000. Soluble nonstarch polysaccharides from pearl barley exacerbate experimental post-weaning colibacillosis. In: J.E. Lindberg and B. Ogle (editors). Digestive Physiology of Pigs. CABI Publishing, Wallingford, England. pp. 280-282. McDonald, D.E., D.W. Pethick, B.P. Mullan and D.J. Hampson, 2001. Increasing the viscosity of the intestinal contents alters small intestinal structure and intestinal growth, and stimulates proliferation of enterotoxigenic Escherichia coli in newly weaned pigs. British Journal of Nutrition 86, 487-498. Nabuurs, M.J.A., 1995. Microbiological, structural and functional changes of the small intestine of pigs at weaning. Pig News and Information 16, 93N-97N. Nabuurs, M.J.A., 1998. Weaning piglets as a model for studying pathophysiology of diarrhea. Veterinary Quarterly 20, S42-S45. Nabuurs, M.J.A., A. Hoogendoorn and van Zijderveld-van Bemmel, 1996. Effect of supplementary feeding during the sucking period on net absorption from the small intestine of weaned pigs. Research in Veterinary Science 61, 72-77. Nataro, J.P. and J.B. Kaper, 1998. Diarrheagenic Escherichia coli. Clinical Microbiological Reviews 11, 142-201. Nollet, H., P. Deprez, E. Van Driessche and E. Muylle, 1999. Protection of just weaned pigs against infection with F18+ Escherichia coli by non-immune plasma powder. Veterinary Microbiology 65, 37-45. Nurmi, E. and M. Rantala, 1973. New aspects of Salmonella infection in broiler production. Nature 241, 210-211. Okai, D.B., F.X. Aherne and R.T. Hardin, 1976. Effects of creep and starter composition on feed intake and performance of young pigs. Canadian Journal of Animal Science 56, 573-586. Osek, J., 1999. Prevalence of virulence factors of Escherichia coli strains isolated from diarrheic and healthy piglets after weaning. Veterinary Microbiology 68, 209-217. Palmer, N.C. and T.J. Hulland, 1965. Factors predisposing to the development of coliform gastroenteritis in weaned pigs. Canadian Veterinary Journal 6, 310-316.

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Pluske, J.R., D.J. Hampson and I.H. Williams, 1997. Factors influencing the structure and function of the small intestine in the weaned pig: a review. Livestock Production Science 51, 215-236. Pluske, J.R., Z. Durmic, D.W. Pethick, B.P. Mullan and D.J. Hampson, 1998. Confirmation of the role of non-starch polysaccharides and resistant starch in the expression of swine dysentery in pigs following experimental infection. Journal of Nutrition 128, 1737-1744. Pluske, J.R., D.W. Pethick D.E. Hopwood and D.J. Hampson, 2002. Nutritional influences on some major enteric bacterial diseases of pigs. Nutritional Research Reviews 15, 333-371. Prohaszka, L. and F. Baron, 1980. The predisposing role of high dietary protein supplies in enteropathogenic Escherichia coli infections in weaned pigs. Zbl Veterinary Medicine B, 27, 222232. Radecki, S.V. and M.T. Yokoyama, 1991. Intestinal bacteria and their influence on swine nutrition. In: E.R. Miller, D. E. Ullrey and A. J. Lewis (editors). Swine Nutrition. Butterworth Heinemann, Boston, USA, pp. 439-447. Richards, W.P.C. and C.M. Fraser, 1961. Coliform enteritis of weaned pigs. A description of the disease and its association with haemolytic Escherichia coli. Cornell Veterinarian 51, 245-257. Sarmiento, J.I., 1988. Postweaning diarrhea in swine: Experimental model of enterotoxigenic Escherichia coli infection. American Journal of Veterinary Research 49, 1154-1159. Siba, P.M., D.W. Pethick and D.J. Hampson, 1996. Pigs experimentally infected with Serpulina hyodysenteriae can be protected from developing swine dysentery by feeding them a highly digestible diet. Epidemiology and Infection 116, 207-216. Smith, H.W. and S. Halls, 1968. The production of oedema disease and diarrhoea in weaned pigs by the oral administration of Escherichia coli: Factors that influence the course of the experimental disease. Journal of Medical Microbiology 1, 45-59. Smith, H.W. and J.E.T. Jones, 1963. Observations on the alimentary tract and its bacterial flora in healthy and diseased pigs. Journal of Pathology and Bacteriology 86, 387-412. Stewart, C.S., 1997. Microorganisms in hindgut fermenters. In: R.I. Mackie, B.A. White and R.E. Isaacson (editors). Gastrointestinal Microbiology. Chapman and Hall, New York, USA, pp. 142186. Svendsen, J., H.J. Riising and S. Christensen, 1977. Studies of the pathogenesis of enteric E. coli infections in weaned pigs: bacteriological and immunofluorescent studies. Nordisk Veterinary Medicine 29, 212-20. Thomlinson, J.R. and T.L. Lawrence, 1981. Dietary manipulation of gastric pH in the prophylaxis of enteric disease in weaned pigs: Some field observations. Veterinary Record 109, 120-122. Tzipori, S., D. Chandler and M. Smith, 1983. The clinical manifestation and pathogenesis of enteritis associated with rotavirus and enterotoxigenic Escherichia coli infections in domestic animals. Progress in Food Nutrition and Science 7, 193-205. van Beers-Schreurs, H.M.G., 1996. The changes in the function of the large intestine of weaned pigs. PhD thesis, University of Utrecht, Utrecht, The Netherlands. van Beers-Schreurs, H.M.G., L. Vellenga, T. Wensing and H.J. Breukink 1992. The pathogenesis of the post-weaning syndrome in weaned piglets; a review. Veterinary Quarterly 14, 29-34. van Beers-Schreurs, H.M.G., M.J.A. Nabuurs, L. Vellenga, H.J. Kalsbeek-van der Valk, T. Wensing and H.U. Breukink, 1998a. Weaning piglets, microbial fermentation, short chain fatty acids and diarrhoea. Veterinary Quarterly 20, S64-S69.

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van Beers-Schreurs, H.M.G., M.J.A. Nabuurs, L. Vellenga, T. Wensing and H.J. Breukink, 1998b. Role of the large intestine in the pathogenesis of diarrhoea in weaned pigs. American Journal of Veterinary Research 59, 696-703. Wathes, C.M., B.G. Miller and F.J. Bourne, 1989. Cold stress and post-weaning diarrhoea in piglets inoculated orally or by aerosol. Animal Production 49, 483-496. Will, L.A., P.S. Paul, T.A. Proescholdt, S.N. Aktar, K.P. Flaming, B.H. Janke, J. Sacks, Y.S. Lyoo, H.T. Hill and L.J. Hoffman, 1994. Evaluation of rotavirus infection and diarrhea in Iowa commercial pigs based on an epidemiologic study of a population represented by diagnostic laboratory cases. Journal of Veterinary Diagnostic Investigation 6, 416-422.

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10 Aspects of intestinal immunity in the pig around weaning M.R. King, D. Kelly, P.C.H. Morel and J.R. Pluske

10.1

Introduction

Two equally important functions performed by the small intestine are the digestion and absorption of dietary nutrients, and the defence of the body from infection via the gastrointestinal mucosa. Some antagonism exists between these tasks, since any increase in the digestive and absorptive area of the intestine also enlarges the area that must be protected by the intestinal immune system. From a teleological perspective, the intestine has sought to perform its functions by providing a physical barrier to most luminal antigens while areas which specialise in sampling of antigen enable controlled induction of immune responses, and by providing a vast area for nutrient absorption which necessitates an equally vast immune system to effectively protect it from infection. The intestinal immune system is constantly exposed to a barrage of antigenic material, ranging from dangerous antigens associated with pathogenic bacteria and viruses to harmless antigens present in a normal diet. This has led to the development of a sophisticated system enabling the induction of active immune responses against harmful antigens and tolerance towards those that are innocuous. Because the pig is born with an immature gastrointestinal immune system, the early postnatal period is of particular developmental significance. The modern practice of abrupt weaning at an early age is highly unnatural for the piglet, which would, under normal circumstances, be gradually weaned at a much greater age and level of developmental maturity. Modern weaning practices abruptly remove the passive protection of maternal milk-derived immunoglobulins and other protective immune factors exposing the piglet to a plethora of novel dietary and environmental antigens. Along with these changes, the piglet is required to rapidly adapt to differences in diet presentation and composition, and social environment, while maintaining a high level of growth and productive efficiency. Given theses psychological and physiological hurdles, the weaning period is, unsurprisingly, often accompanied by poor performance. Weaning is also accompanied by significant alterations in intestinal immunity (Vega-López et al., 1995; McCracken et al., 1999; Pluske et al., 1999; Solano-Aguilar et al., 2001) and intestinal immune responses, in particular inflammatory responses directed against dietary and bacterial antigens, which have been implicated in the pathogenesis of the post-weaning ‘growth check’ (Li et al., 1990; Pluske et al., 1997).

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10.2

Overview of immune systems

10.2.1

Active immunity

10.2.1.1 Innate immunity During their evolutionary development, vertebrates and invertebrates were subjected to selection pressure conveyed by infectious pathogens, which resulted in the early development of the non-specific, or innate immune system (Mushegian and Medzhitov, 2001). Functioning independent to prior exposure to bacterial pathogens, innate immunity can respond to bacterial invasion extremely quickly, and may be considered the ‘first line of defence’ against bacterial infection. The predominant leukocytes that mediate the actions of the innate immune system are natural killer cells, mast cells, macrophages and neutrophils, which are derived from the myeloid descendants of the hematopoietic stem cells that reside in bone marrow. Constituting approximately 50% of the leukocytes found in blood, neutrophils are considered the most active of the cells involved in innate responses, and circulate constantly in the blood. In the gut, epithelial cells provide the first point of contact for both bacterial and dietary antigens. These cells play a pivotal role in initiating inflammatory immune responses by secreting chemokines and cytokines that promote the activation and recruitment of myelolymphoid effector cells to sites of infection or damage. An important feature of the epithelial cell is its ability to discriminate between harmful and innocuous antigens; with respect to antigens associated with gut bacteria, various receptor recognition systems expressed on apical and basolateral surfaces fulfil this function. An important receptor class in bacterial recognition is the toll-like receptor (TLR) (Cario et al. 2000); these receptors recognise pathogen-associated molecule patterns (PAMPS) such as gram negative lipopolysaccharide and gram positive peptidoglycan and trigger downstream signalling cascades that activate epithelial transcription factors which drive inflammatory gene expression. Gene products including IL-8 and MIP-2α are chemotactic for neutrophils and macrophages (McCormick et al. 1993; Hang et al. 1999). Epithelial cells also produce antimicrobial peptides referred to as beta-defensins, an important constituent of the innate immune system, that kill bacteria thus limiting their translocation across the epithelial barrier during infection and invasion (O’Neil et al. 1999). Intestinal inflammation leads to expression of adhesion molecules on endothelial cells lining the tissue capillaries, to which blood-borne neutrophils bind by virtue of complimentary cell-surface receptors that they express (Osborne, 1990; Butcher, 1991). Bound neutrophils infiltrate the tissue via the capillary wall by a process known as diapedesis, which allows the cell to fit through a pore much smaller than its size. After entering the infected tissue, neutrophils also recognise PAMPs via

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specific cell-surface pattern recognition receptors including TLRs (Kelly and King, 2001). Neutrophils migrate towards the source of these antigens by a process known as ‘chemotaxis’ and non-specifically engulf the invading bacteria. Recognition of bacterial antigens activates the neutrophil, resulting in an ‘effector’ phase characterised by activation of the complement system, and secretion of inflammatory agents such as such as chemokines and cytokines including interleukin (IL) -1, IL6, interferon (IFN) -γ, tumor necrosis factor (TNF) -α and reactive oxygen metabolites, all of which have direct or indirect anti-bacterial actions (Sandborg and Smolen, 1998; Zhang et al., 2000; Morein and Hu, 2001). However although present in low numbers at birth, blood-borne neutrophils do not reach adult levels until 21 days after weaning (McCauley and Hartmann, 1984), also the chemotactic mechanism of neutrophils (and macrophages) is reported to be impaired in young pigs, and the complement system may not reach adult concentrations until 4 weeks of age (Stokes et al., 1992). Another component of the innate immune system is the mast cell. Mast cells are present in the lamina propria of the intestine and respond to antigen and nonantigen-dependent stimulation, releasing a broad range of bioactive mediators which serve to recruit further leukocytes such as neutrophils, and promote the development of the intestinal inflammatory response (Befus et al., 1988; Malaviya and Abraham, 2001; Yu and Perdue, 2001). Mast cells are of particular importance in the pathogenesis of allergic reactions, in which they play a central role (Befus et al., 1988; Malaviya and Abraham, 2001; Yu and Perdue, 2001). In addition to the innate immune system, which provides a generic response to repeated bacterial invasion, there exists the adaptive immune system, providing what is known as ‘acquired’ immunity. This comprises two arms of the immune system, which are primed by initial exposure to antigens, allowing an antigen-specific immune response that provides long-term immunity. These immune systems are functionally distinct, and their activation is dependent on the nature of the antigen involved. In the case of viral infection, in which a mammalian ‘host cell’ and its machinery is exploited to enable viral replication, the infected cell must be destroyed in order to eliminate the viral pathogen. These actions are performed by the cellular arm of the immune system. In the case of bacteria, which replicate independently in most environments, such cytotoxic responses alone are largely ineffectual and the antibody-mediated response of the ‘humoral’ arm of the immune system is engendered. These systems will now be discussed. 10.2.1.2 Adaptive immunity Humoral immunity Activation of the adaptive immune response begins with the processing and presentation of intracellular antigens to either the humoral or cellular arm of the

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immune system. In the case of humoral immunity, bacterial or other soluble antigens are taken up by specialised antigen-presenting cells (APCs) such as tissue macrophages and dendritic cells (Kagnoff, 1987), which use proteolytic enzymes to degrade (process) the antigen into immunogenic peptides. These peptides are presented on the surface of the APC, associated with specialised antigen-receptor molecules referred to as major histocompatibility complex (MHC) class II molecules. The MHC class II-antigen complex is subsequently recognised by antigenspecific helper T cells. T cells are commonly identified by specific ‘cluster of differentiation’ (CD) molecules which are expressed on their cell surfaces - in the case of helper T cells this is CD4, and on this basis helper T cells are often referred to as CD4+ T cells. Antigen recognition by helper T cells causes them to secrete specific lymphokines. These lymphokines stimulate antigen-specific B cells to undergo clonal expansion (multiplication) and differentiation, producing large numbers of antibody-secreting plasma cells (Gaskins and Kelley, 1995). The immunoglobulins (antibodies) secreted by plasma cells recognise and bind specific antigens associated with the pathogenic agent that initiated the immune response, and effect removal of the agent through such processes as opsonisation and complement-mediated direct cytotoxicity (Gaskins and Kelley, 1995). The humoral immune system therefore provides a potent, antigen-specific response to extracellular infection. Cellular immunity Viral infection, which subverts the cellular machinery of host cells to enable viral replication, necessitates the destruction of the infected cell, using the cytotoxic actions of the so-called ‘cellular’ immune response. Most somatic cells are susceptible to viral infection, and most are therefore also able to process and present viral antigen to the cellular arm of the immune system. The process of antigen presentation begins with the intracellular processing of a subset of viral antigens into immunogenic peptides, which are then presented on the cell surface as MHC class I-antigen complexes (Jackson and Peterson, 1993). In contrast to the humoral immune system, the cellular immune system employs MHC class I molecules in antigen presentation, which mediate recognition of antigen by antigen-specific cytotoxic T lymphocytes. Cytotoxic T lymphocytes express the CD8 surface molecule, and are therefore often referred to as CD8+ T cells. Recognition of the antigen-MHC class I complex ‘activates’ the cytotoxic T lymphocyte, causing it to multiply by clonal expansion, and to synthesise and secrete bioactive factors that destroy the infected cell (Gaskins and Kelley, 1995). As in the case of humoral B lymphocytes, once activated, the cytotoxic action of the T cell is antigen-specific, meaning it will only kill cells expressing the stimulating antigen in conjunction with the same MHC class I molecules involved in induction of the immune response (Kagnoff, 1987). The cell-mediated immune response therefore specifically targets and destroys only the infected cells that are the source of viral replication, effectively removing the intracellular pathogenic threat while leaving healthy cells unperturbed.

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10.2.2

Passive immunity

The use of preformed antibodies derived from an individual to provide temporary protection against infection in another individual, is termed ‘passive’ immunity. The acquisition of passive immunity is crucial to the survival of the neonatal pig for several reasons. First, the epitheliochorial placentation of the pig foetus prevents the transfer of maternal antibodies during gestation (Sterzl and Silverstein, 1967) resulting in a pig that is agammaglobulinemic at birth (Salmon, 1984). Second, although the cellular components of the immune system are qualitatively represented at birth (Binns, 1973), they are quantitatively and functionally immature (Stokes and Bourne, 1989; Stokes et al., 1992). The acquisition of passive immunity therefore provides crucial protection from pathogens while the cellular components of the immune system mature. Passive immunity is provided by maternal immunoglobulins, which are selectively concentrated in the mammary gland towards the end of gestation and absorbed intact across the ‘open’ small intestine of the neonatal pig upon the initiation of suckling (Holland, 1990). The open gut of the piglet can endocytose macromolecules such as immunoglobulins in massive quantities within the first forty-eight hours after birth, resulting in serum antibody titres similar to those of sow (Holland, 1990), and a spectrum of antibodies indistinguishable from that of the sow (Bourne, 1977). The absorbed antibodies circulate in the serum, providing short-term passive systemic protection from infectious agents. However, the passively acquired antibody repertoire of the neonate is necessarily restricted to those antigens to which the sow has been exposed, and developed memory B cells (Porter, 1986). The predominant immunoglobulin isotype in colostrum reflects that of the serum from which it is derived - immunoglobulin-G (IgG) (Jensen and Pedersen, 1979; Butler and Brown, 1994). Immunoglobulins A (IgA) and M (IgM) are present in colostrum in much smaller concentrations than IgG (Jensen and Pedersen, 1979; Butler and Brown, 1994), and are derived from both serum and local synthesis within the mammary gland (Bourne and Curtis, 1973). The macromolecular endocytosis of the open gut is non-selective, and its gradual cessation (referred to as ‘gut closure’) is complete by 48 hours after birth (Murata and Namioka, 1977; Weström et al., 1984). This prevents further large-scale absorption of immunoglobulins, but has the benefit of also preventing further absorption of macromolecules that might be antigenic or pathogenic in nature. After colostrum formation, established lactation proceeds and the character of immunoglobulins present in mammary secretions changes, reflecting a change in the site of their synthesis with most immunoglobulins in milk derived from local synthesis within the mammary gland (Stokes et al. 1992; Salmon, 1999). This is associated with a decrease in total immunoglobulin concentration in milk, and an alteration in the relative concentration of milk immunoglobulins, with IgA

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predominating (Jensen and Pedersen, 1979; Stokes et al., 1992; Butler and Brown, 1994; Salmon, 1999). These changes coincide with gut closure, and mark a change in the major function of maternally-derived immunoglobulin for the piglet. Prior to gut closure, a secondary function of unabsorbed maternal immunoglobulin is the provision of local passive protection against the many pathogenic agents encountered at the intestinal mucosa; after gut closure this becomes the predominant function of maternal immunoglobulins. However, IgG antibodies are relatively ineffective at mucosal surfaces (Gaskins and Kelley, 1995; Gaskins, 1998), whereas IgA is largely resistant to the action of digestive and bacterial proteolytic enzymes and binds to mucous components (Kerr, 1990) where it functions largely to bind antigens, prevent bacterial and viral colonisation and invasion at mucosal surfaces, and neutralise bacterial enterotoxins (Porter, 1986; Kagnoff, 1993; Salmon, 1999). Although a minor component of the immunoglobulins present in colostrum and milk, maternal IgM antibodies nonetheless bolster local passive protection by virtue of a lower adherence to the mucous lining of epithelial surfaces, making IgM particularly suitable for opsonizing pathogens in the gut lumen (Salmon, 1999). As with passive systemic immunity, the protection afforded by passive local immunity only extends to antigens to which the sow has been exposed and developed active immunity. Other protective factors present in milk and colostrum, such as lactoferrin and lactoperoxidase, perform non-specific antimicrobial functions, however a discussion of these factors falls outside of the scope of this review, and the reader is directed to recent reviews of the topic (Chierici, 2001; van der Strate et al., 2001; van Hooijdonk et al., 2000; Wagstrom et al., 2000). Both forms of passive immune protection extend for the entirety of the lactation period, and their removal at weaning marks a significant breach in the immune protection of the piglet, which will be discussed later in this review.

10.3

The intestinal immune system

The intestinal epithelium provides an extensive and complex interface between the piglet’s immune system and its environment, which must function simultaneously to absorb digested nutrients and provide a barrier against a vast array of ingested antigens. The barrier is composed of the basement membrane underlying epithelial cells, the epithelial cells themselves, the tight junctions that join adjacent cells, and the cell glycocalyx (Kagnoff, 1987; Perdue 1999; Podolsky, 1999). In addition to its barrier function the epithelium also functions in surveillence, communicating information regarding the contents of the intestinal lumen to the underlying mucosal immune system through the production of cytokines (Gaskins 1998; Perdue 1999; Lu and Walker, 2001; Sanderson, 2001). Innate defense is provided by epithelial goblet cells, which secrete mucin and trefoil peptides that form a visoelastic gel which covers the mucosal surface, providing a barrier which protects the mucosa

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from luminal bacteria and antigens (Kindon et al., 1995; Podolsky, 1999; Deplanke and Gaskins, 2001). Trefoil peptides have also been implicated in mucosal repair as well as prevention of injury (Babyatsky et al., 1996; Playford, 1997; Podolsky, 1999). A further innate defense mechanism is performed by epithelial Paneth cells, which secrete antimicrobial peptides into the gut lumen, contributing to a biochemical barrier against colonisation (Ouellette, 1999; Zhang et al., 2000). The continual and rapid migration of epithelial cells from the crypts of Lieberkühn, culminating in their extrusion from the villous tip into the gut lumen, removes damaged or infected cells and also provides a mechanism for rapid epithelial restitution after mucosal injury (Podolsky, 1999). Further protection is provided by the intestinal immune system, which is the largest immune organ in vertebrate species (Gaskins, 1998; Kraehenbuhl and Neutra, 1992). Approximately 25% of the intestinal mucosa consists of lymphoid tissue (Kagnoff, 1987), which in turn constitutes approximately 50% of the total body lymphoid tissue (James, 1993). The gut-associated lymphoid tissue, commonly abbreviated as GALT, contains three major lymphoid compartments consisting of (1) dispersed or non-organised cells residing in the lamina propria and epithelium (lamina propria leukocytes and intraepithelial T lymphocytes); (2) collections of highly organised lymphoid follicles, such as Peyer’s patches and lymph nodes; and (3) scattered individual or small aggregates of lymphoid follicles (Kagnoff, 1987; Gaskins, 1998). Approximately 20-30 discrete Peyer’s patches exist in the jejunum and upper ileum of the pig, which increase only slightly in number but significantly in size and cellularity, during the post-natal period (Pabst et al., 1988; Stokes et al., 1994). One continuous patch, which can extend for 2.5 metres, exists in the distal ileum, but this involutes at approximately 1 year of age (Pabst et al., 1988; Stokes et al., 1994). Antigen transport function is performed by specialised antigen-transporting cells known as M-cells, which are expressed in the epithelium overlying organised lymphoid follicles such as Peyer’s patches (Neutra et al., 1980; Neutra, 1999; Kraehenbuhl and Neutra, 2000). M-cells efficiently endocytose and transcytose luminal antigens, bacteria and viruses, which then interact with APCs in the underlying lymphoid follicle, which acts as an antigen ‘sampling site’ (Neutra et al. 1980; Neutra, 1999; Kraehenbuhl and Neutra, 2000). APCs process the antigen into immunogenic peptides, which are then presented in association with class II MHC molecules to helper T lymphocytes. Antigen presentation causes T lymphocytes to secrete lymphokines that induce B lymphocytes to undergo immunoglobulin class-specific switching within the lymphoid follicle, dedicating themselves to production of a single class of antibody. Class-switching of B-cells in Peyer’s patches favours the IgA+ phenotype, due to unknown factors within the follicular microenvironment (Kagnoff, 1987, 1993).

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A proportion of the activated T and B lymphocytes then migrate from the Peyer’s patch through the lymphatic system before entering the systemic circulation, thereupon ‘homing’ to the lamina propria and intraepithelial region of the small intestine (Kagnoff, 1987; Thiele, 1991; Gaskins and Kelley, 1995; Corthesy and Kraehenbuhl, 1999). Upon reaching the lamina propria, activated B lymphocytes differentiate into plasma cells, capable of secreting large quantities of IgA antibody, a process controlled by cytokines (such as TGF-β, IL4, IL-5 and IL-6) which are produced by helper T lymphocytes in response to reintroduction of antigen (Corthesy and Kraehenbuhl, 1999). The dimeric IgA produced by plasma cells in the lamina propria interacts with a specialised receptor on the basal surface of intestinal epithelial cells, and the bound IgA is then endocytosed and trancytosed across the cell to be released into the lumen, retaining a cleaved portion of the receptor known as the secretory component (Solari and Kraehenbuhl, 1985; Kerr, 1990; James, 1993). The presence of the secretory component stabilises the structure of the antibody, known as secretory IgA, and increases its resistance to proteolysis (Lindh, 1975; James, 1993), making it particularly suitable for activity in the gut lumen. The main action of secretory IgA is at the mucosal surface, where it binds antigens and prevents viral and bacterial invasion of epithelial surfaces (Williams and Gibbons, 1972; Kagnoff, 1987, 1993; Kraehenbuhl and Neutra, 1992). There is also evidence that secretory IgA can act on antigens within the lamina propria, causing them to be expelled into the gut lumen via the IgA secretory pathway described previously (Kaetzel et al., 1991; Mazanec et al., 1993). A further feature of dimeric IgA is that it is relatively nonphlogistic compared to other immunoglobulins, participating in neither complement activation nor antibody-directed cytotoxic responses (Kagnoff, 1987, 1993). Since a vast number of the antigens commonly present in the gut lumen are likely to be harmless and non-pathogenic, from a teleological perspective it is sensible that the predominant immunoglobulin at mucosal surfaces functions through antigen binding and exclusion rather than induction of mucosal inflammation (Kagnoff, 1987, 1993). In addition to professional APCs, processing and presentation of luminal antigens to the immune system has been postulated to occur via small intestine epithelial cells expressing class II MHC (Bland and Warren, 1986a, b; Hoyne, et al. 1993; Kaiserlian, 1999). Although epithelial cells have been shown to display class I and II MHC antigens (Olivier et al., 1994), their role in antigen presentation remains contentious (Dvorak et al., 1987; Vega-López et al. 1993, 1995; Chianini et al., 2001).

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10.3.1

Intestinal inflammation

Despite the protection afforded by the aforementioned mechanical barriers and secretory IgA, enterocytes can transport a small proportion of luminal antigenic material to the underlying tissues by transcytosis (Wheeler et al. 1993; Heyman, 2001). Similarly, enteric pathogens and antigenic material can invade the intestinal epithelium and the underlying lamina propria via paracellular routes, particularly during times of compromised mucosal integrity such as intestinal infection and inflammation (Heyman, 2001). The epithelial monolayer is interspersed with a heterogenous population of intraepithelial T lymphocytes, which are predominantly cytotoxic, although so-called double-negative T cells (which express neither the CD4+ nor CD8+ surface antigen) are also present, particularly in the neonate (Vega-López et al., 1993, 2001). Intraepithelial T cells, which represent around 50% of all intestinal lymphocytes in the mature pig (Vega-López et al., 2001), are capable of mediating antibody dependent and direct cytotoxic activity (see Stokes et al., 1994; MacDonald, 1999) and, because of their proximity to the intestinal lumen, are ideally positioned to potentially effect and regulate immune responses (Vega-López et al., 2001). The function of intraepithelial T cells is not well established, although it is hypothesised that they may maintain epithelial integrity by destroying damaged, virally infected or parasitised epithelial cells (Kraehenbuhl and Neutra, 1992; MacDonald, 1999), or promote epithelial growth and renewal through the production of cytokines during active immune responses (Mowat and Viney, 1997). The lamina propria is populated by a wide range of diffuse immune cells, such as T lymphocytes, antibody-forming B lymphocytes and plasma cells, macrophages, dendritic cells, mast cells, eosinophils, neutrophils, and biologically active fibroblasts (Kagnoff, 1987; Gaskins and Kelley, 1995; Gaskins 1997). The distribution of T cells in lamina propria of the pig appears to be distinctly compartmentalised by 6 months of age (Vega-López et al., 1993; Olivier et al., 1994), with cytotoxic (CD8+) T cells generally positioned in and around the epithelium, and helper (CD4+) T cells generally situated deeper in the lamina propria. The ontogenesis and functional significance of this distribution is yet to be established. Antigenic material that is present in the lamina propria as a result of disruption of the epithelial barrier is processed by lamina propria APCs such as dendritic cells and macrophages (Stokes et al., 1992, 1996; Iwasaki and Kelsall, 1999; Haverson et al., 2000). Antigen is then presented as immunogenic peptides in the context of class II MHC and co-stimulatory molecules to helper T lymphocytes either in the lamina propria or, in the case of mature dendritic cells, after the APC has migrated to the mesenteric lymph nodes, (Haverson et al., 2000; Guermonprez et al., 2001). Antigen recognition by helper T lymphocytes causes activation and secretion of a

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range of cytokines (Murtaugh, 1994; Wood and Seow, 1996). Activated T lymphocytes in the mesenteric lymph nodes proliferate in response to inflammatory signals and migrate to the mucosa to interact with antigen-specific B-cells (Jenkins et al., 2001). The cytokines released by activated T lymphocytes recruit and activate further lymphocytes and the cellular components of the innate immune system, such as eosinophils, neutrophils and lamina propria mast cells, which in turn produce pro-inflammatory cytokines (such as IL-1, IL-4, IL-8, IFN-γ, TNF-α, and granulocyte-monocyte colony stimulating factor), neurotransmitters, and other inflammatory mediators such as complement, nitric oxide and granulocyte proteins which perform or aid antimicrobial functions (Murtaugh, 1994; Elwood and Garden, 1999; Miller and Sandoval, 1999; Zhang et al., 2000). Proinflammatory cytokines and other mediators produce an array of enteropathic effects in the mucosa: induction of matrix metalloproteinase expression in macrophages, which destroys supporting elements in the mucosa; induction of MHC class II expression in APCs; increased ion secretion into the gut lumen; increased epithelial permeability; and induction of goblet cell differentiation and crypt cell mitosis (MacDonald and Spencer, 1988; Goetzl et al., 1996; Elwood and Garden, 1999; Ferreira et al., 1990, Pender et al., 1997; MacDondald et al., 1999; Monteleone et al., 1999). A detailed discussion of the nature of the inflammatory process in intestinal mucosa is outside the scope of this review, and the previous explanation represents an extreme simplification. Physiological and immunological processes in the intestine represent a complex interaction between immune and non-immune cells and the extracellular matrix, and pathological inflammation may result from dysfunction of one or more of these components, resulting in a homeorhetic response involving all constituents (see Fiocchi, 1997). Evidence of intestinal inflammation has been observed in pigs after weaning (McCracken et al., 1999), and this will be explored later in this review. 10.3.2

Oral tolerance

The gastrointestinal immune system is constantly sampling antigenic material from the intestinal lumen, a large proportion of which is dietary protein. It is essential for the gastrointestinal immune system to be able to discriminate between antigens of dietary origin, to which immunological tolerance must be induced, and those derived from pathogenic bacteria, against which an active immune response must be mounted. Failure of this discriminatory system results in inappropriate immune responses to innocuous antigens, which can take the form of allergic reactions to dietary components. There is also evidence that a similar state of tolerance exists with regard to harmless commensal gut bacteria (Duchmann et al., 1995, 1996), and perturbations of this state may be crucial for the development and maintenance of chronic intestinal inflammation (Duchmann et al., 1997).

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The most common example of the induction of oral tolerance is the feeding of a novel protein antigen to an animal, which results in systemic immunological hyporesponsiveness when the animals are subsequently challenged with the same antigen (Challacombe and Tomasi, 1980). The mechanisms by which oral tolerance is induced are the subject of active research, and are not yet fully understood; in particular, the specific cellular and molecular interactions which generate mucosal tolerance, and their localisation, have yet to be fully identified, and the mechanisms which allow the mucosal immune system to accurately discriminate between innocuous and hazardous antigen are unclear (Bailey et al., 2001a). For detailed discussions of current concepts of oral tolerance, the reader is directed to recent reviews of the topic (Strobel and Mowat, 1998; Weiner, 2000; Garside and Mowat, 2001). Mucosal exposure to antigen from living and multiplying pathogens generally leads to priming of the local or systemic immune system, whereas exposure to soluble antigen most commonly results in the development of oral tolerance (Kagnoff, 1993; Strobel and Mowat, 1998; Strobel, 2001). The current understanding of the development of oral tolerance implicates several possible mechanisms of induction: clonal anergy, clonal suppression or regulation, and clonal deletion (Strobel and Mowat, 1998; Czerkinsky et al., 1999; Strobel, 2001; Bailey et al., 2001a). Apoptosis of T lymphocytes has also been suggested as a mechanism by which mucosal unresponsiveness may be maintained (Bu et al., 2001). It is thought that multiple mechanisms are likely to be involved in induction and maintenance of oral tolerance, many of which may not necessarily be mutually exclusive (Strobel and Mowat, 1998; Weiner, 2000; Garside and Mowat, 2001; Strobel, 2001). Antigen processing and presentation may be a central determinant of whether active immunity or tolerance to an antigen is induced. Soluble antigens may be processed and presented to helper T lymphocytes by APCs which express class II MHC, but not the full range of co-stimulatory molecules (such as B7-1 (CD80) or B7-2 (CD86)) which are normally required for induction of an active immune response, resulting in clonal anergy and oral tolerance (Strobel, 2001; Strobel and Mowat, 1998). Alternatively, the MHC class II+ APC may express a specialised inhibitory receptor (such as cytotoxic T lymphocyte-associated antigen-4), which may be required to induce tolerance (Bluestone, 1997; Frauwirth and Thomson, 2002), possibly through interaction with regulatory T cells (Toms and Powrie, 2001). At low doses of antigen, tolerance may also be induced through non-professional APCs that express class I MHC or possibly non-classical class I restriction elements, which present immunogenic peptides to suppressor T lymphocytes, producing a dosedependent induction of T lymphocyte-mediated clonal suppression (Strobel and Mowat, 1998; Strobel, 2001).

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T lymphocyte-mediated regulation or suppression of immune responses is likely to be effected by production of transforming growth factor (TGF) -β, and other immunosuppressive cytokines such as IL-4 and IL-10 (Khoury et al. 1992; Chen et al., 1994; Friedman and Weiner, 1994). Interestingly, these cytokines are also implicated in the class switching of B lymphocytes to the IgA+ phenotype (Murray et al., 1987; Defrance et al., 1992; van Vlasselaer et al., 1992), which is compatible with the observation that systemic tolerance and humoral secretory immune responses can develop concurrently (Challacombe and Tomasi, 1980). There is significant evidence that the intestinal immune system of the pig is highly regulated, and perhaps biased in favour of the induction of mucosal tolerance rather than active immune responses to antigen. Activation of porcine T cells in vitro has been shown to induce secretion of the immunosuppressive lymphokines IL-4 and IL-10, and only low levels of IL-2, which implies preferential induction of tolerance and secretory immune responses rather than cellular immunity (Bailey et al., 1994, 1998; Whary et al., 1995). There is also some evidence that isolated pig lamina propria lymphocytes undergo increased apoptosis in response to activation compared to similarly isolated splenic lymphocytes (Stokes et al., 2001). Increased susceptibility to apoptosis is consistent with the observation that lamina propria T cells are generally in an advanced state of differentiation indicating memory or recent activation status (Haverson et al., 1999), which may predispose T cells to apoptosis after activation (Salmon et al., 1994). Furthermore, many of the MHC class II+ cells in the pig lamina propria are non-professional APCs, such as endothelial cells and eosinophils, which may induce anergy by presenting antigen in the absence of appropriate co-stimulatory molecules (Haverson et al., 1994; Stokes et al., 1996; Wilson et al., 1996; Haverson et al., 2000). The induction of oral tolerance is likely to result from a complex interaction of many immunological factors, many of which are only partially understood at present. Failure of the mucosal immune system to develop oral tolerance towards innocuous antigen leads to induction of an active immune response in the lamina propria, resulting in pathological inflammation of the intestine, as described previously. An example of this condition is gluten intolerance resulting in coeliac disease in humans (Ferguson et al., 1984). In the pig, it has been suggested that the induction of oral tolerance is perturbed by the process of early-weaning, resulting in hypersensitivity reactions to dietary proteins including soy protein (Miller and Stokes, 1994; Bailey et al., 2001a, b), which will be discussed later. Supporting this hypothesis, weaning has been reported to be associated with reduced ease of oral tolerance induction in mice (see Strobel, 1996).

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10.3.3

Development of intestinal immunity

The neonatal pig may be considered essentially immunoincompetent at birth, due to low numbers of intestinal MHC class II+ cells that are required for the presentation of antigen, and CD4+ and CD8+ T cells, which are necessary for the induction of active immune responses (Bianchi et al., 1992; Vega-López et al., 1995, 2001; Pabst and Rothkötter, 1999; Rothkötter et al., 1999). However T cells (which express the characteristic CD2 surface antigen and are therefore classified as CD2+ cells) are present in the intestine, but these cells express neither the CD4 or CD8 surface antigen, and are therefore predominantly of the double-negative phenotype CD2+CD4-CD8- (Rothkötter et al. 1991, Vega-López et al., 1995, 2001; Whary et al., 1995). The presence of this double-negative population of T cells in pigs has been reported elsewhere (Pescovitz et al., 1985; Saalmuller et al., 1989; Binns et al., 1992, Vega-López et al., 1993), as has a double-positive (CD2+CD4+CD8+) population of T cells (Whary et al. 1995; Zuckermann and Gaskins, 1996; Zuckermann, 1999; Solano-Aguilar et al., 2001), however currently their function is unclear. Intraepithelial T cells are present at birth, accounting for around 40% of all intestinal T cells, and are also predominantly of the double-negative phenotype (Chu et al. 1979; Vega-López et al., 2001). A small number of IgM+ and IgA+ cells are present in the intestine at birth (Bianchi et al. 1992). Components of the innate immune system are present at birth, with low numbers of macrophage and granulocyte cells present in an even distribution throughout the villous and crypt regions (Vega-López et al., 1995), however they may not yet be functionally mature (Stokes et al., 1992). As previously described, jejunal and upper ileal Peyer’s patches are present at birth in approximately the same number and positions as adult animals, although the single continuous Peyer’s patch present in the distal ileum involutes at around 1 year of age. During the postnatal period the intestinal immune system undergoes extensive change, as the pig is exposed to a plethora of environmental antigens, both injurious and innocuous in nature. The presence of macrophages and polymorphonuclear cells increases after birth, becoming more concentrated in the crypt rather than villous region of the lamina propria and reaches adult levels at five weeks of age (Vega-López et al., 1995). The number of dendritic cells likewise increases after birth although, in contrast to macrophages, dendritic cells become prevalent in the villous lamina propria rather than the crypt (Stokes et al., 1992). This is confirmed by the development of MHC class II+ cells, which are about twice as abundant in the villus compared to the crypt area of lamina propria by one week of age (although significant numbers are still present in crypt area), and reach adult levels at 5 weeks after birth (Vega-López et al., 1995). At present it is unclear what may be the functional significance this apparent compartmentalisation of APCs in the lamina propria.

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The lymphocyte profile of the intestinal mucosa alters dramatically after birth, with the number of lamina propria T lymphocytes doubling in the first four weeks after birth (Rothkötter et al., 1991; Stokes et al., 1992). This process is driven largely by exposure to microbial antigens, with gnotobiotic pigs displaying only minor increases in intestinal lymphocytes despite being exposed to nutritional antigens (Rothkötter et al., 1991, 1994, 1999; Pabst and Rothkötter, 1999). Immature lamina propria T lymphocytes begin to differentiate into CD4+ and CD8+ subsets by the fifth day of age, with their collective number equalling that of CD2+ T cells by 12 days of age (Rothkötter et al., 1994). However the CD4+ and CD8+ T cell subsets display different developmental patterns, with the presence of CD4+ T cells rapidly increasing immediately after birth, while CD8+ T cell numbers increase in a comparatively sedate fashion in the first 5-7 weeks after birth (Rothkötter et al., 1991; Bianchi et al., 1992; Stokes et al., 1992; Vega-López et al., 1995, 2001). By 6 months of age, lamina propria CD4+ and CD8+ T cells display distinct patterns of localisation within the lamina propria, as previously described, and are four times more concentrated in the villous area of the lamina propria than the crypt area (Vega-López et al., 1993). The number of intraepithelial T lymphocytes increases significantly with age and exposure to microbial antigen, and intraepithelial lymphocytes represent around 50% of all intestinal lymphocytes by 5 weeks of age (Rothkötter et al., 1999; Whary et al., 1999; Vega-López et al., 2001). Lymphocytes accumulating in the epithelium in early life are predominantly CD2+, with significant numbers of CD8+ T cells only detectable later in life (Vega-López et al., 1995, 2001). The number of intraepithelial T cells remains comparatively low during the first 5 weeks of life which, combined with the paucity of CD8+ T cells, may predispose the young pig to enteric infection (Vega-López et al., 2001). Adult numbers of intraepithelial T cells are not reached until around 24 weeks of age, at which time approximately half are CD8+ T cells and half double-negative T cells, with some granular lymphocytes also present (Vega-López et al., 2001). B lymphocytes in the lamina propria respond to antigenic stimulation during the post-natal period, with IgA+ plasma cells increasing rapidly in number from 6 to 28 days of age, around which time adult levels are reached (Brown and Bourne, 1976). The presence of IgM+ plasma cells is also significant, outnumbering IgA+ cells until around 4 weeks of age, after which time IgA+ cells predominate (Brown and Bourne, 1976; Allen and Porter, 1977; Butler et al., 1981; Rothkötter et al., 1991; Bianchi and van der Heijden, 1994; Pabst and Rothkötter, 1999). In contrast to T cells, plasma cells are more concentrated in the crypt rather than villus area of the lamina propria (Brown and Bourne, 1976; Rothkötter et al., 1991; Pabst and Rothkötter, 1999).

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Peyer’s patches undergo enlargement during the postnatal period, with their length increasing around three times in the first 38 days after birth (Pabst et al., 1988). The enlargement and lymphocyte composition of Peyer’s patches is at least partially determined by environmental conditions such as disease load. Germ-free pigs display a smaller increase in size of the ileal Peyer’s patch in the first 38 days after birth, whereas jejunal patches showed no change (Pabst et al., 1988). Similarly at 6 weeks of age the vast majority of lymphocytes present in Peyer’s patches of conventional pigs are B cells, whereas in germ-free pigs, T cells predominate (Rothkötter and Pabst, 1989; Pabst and Rothkötter, 1999). The swift and extensive accumulation of MHC class II+ APCs and both the CD4+ and CD8+ subsets of T lymphocytes in the postnatal period indicates that the piglet rapidly develops the potential for direct antigen recognition and subsequent induction of active immune responses in the lamina propria of the small intestine. However, the components of the intestinal immune system do not resemble that of the adult pig by three weeks of age, the time when weaning usually occurs. In particular, the ratio of CD4+ to CD8+ T cells at this time is the reverse of that which is observed in the adult pig. In adult pigs this ratio is less than 1, whereas in younger pigs the disparity in the relative proliferation of these T cell subsets produces a ratio greater than 1, which could potentially influence the capacity of the piglet to regulate normal intestinal immune responses (Miller and Stokes, 1994). Furthermore, absolute levels of lymphocytes in the lamina propria and intraepithelial compartments are far below adult levels at weaning, which may compromise immunological defence against enteric infections in the intestine (Vega-López et al., 1995, 2001). Withdrawal of the maternal supply of immunoglobulins at this time at this time eliminates their passive immunological function in the intestinal lumen, leaving the mucosa vulnerable to opportunistic infections such as haemolytic E. coli and rotavirus (see van Beers-Scheurs et al., 1992; Pluske et al., 1997). Weaning is associated with numerous other sources of stress for the young pig, throughout which the animal must attempt to maintain homeostasis. It is therefore unsurprising that weaning has a significant effect on intestinal immunity, which will now be explored.

10.4

The effect of weaning on the intestinal immune system

10.4.1

Overview of the weaning process

In modern pig production systems weaning generally occurs at 2 to 4 weeks of age. Common characteristics of the weaning process are: separation of the sow and piglets, ensuring immediate and complete cessation of piglet access to sow’s milk; relocation of the piglets to a nursery facility, which is recommended to be thoroughly cleaned and disinfected prior to piglet entry and maintained at

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thermoneutral temperature; mixing of different litters of piglets in nursery pens, which may be random or based on common liveweight or sex within a pen; provision of a high nutrient density compound diet, which may be offered in dry (pelleted or meal) or liquid form from easily accessed feeders; water is provided ad libitum from specialised drinkers or water-nipples, and an electrolyte solution may also be provided. This weaning system provides a stark contrast to that which occurs under ‘natural’ conditions, where piglets, after a gradual decline in intake, generally cease consumption of sow’s milk between 15 and 22 weeks of age (Jensen and Stangel, 1992), during which time they have learned foraging behaviour to provide nutrition to supplement and eventually replace the declining maternal supply of nutrition. Weaning under the majority of commercial conditions currently practiced worldwide generally results in a ‘growth check’, which is characterised by low voluntary feed intake, poor weight gain or weight loss and occasionally diarrhoea, morbidity and death (see Pluske et al. 1995). The impaired growth performance may persist for up to 14 days after weaning, with growth during this time reduced by 25-40% compared to that observed in unweaned piglets of the same age (Musgrave et al. 1991; Pajor et al., 1991). This phenomenon is variously attributed to nutritional stress, due to removal of sow’s milk and provision of a novel replacement diet; psychological stress, caused by removal of the sow, relocation and mixing, and unfamiliarity with the nature of the weaning diet; and environmental stress, caused by fluctuations in ambient temperature, air-borne dust, and the presence of environmental antigens. A further cause of the post-weaning growth check may be postulated to be that of immunological ‘stress’. Since the immunological state of the animal is affected by alterations in nutritional, psychological, and environmental factors (Kelley, 1980), immunological stress may be considered to interpenetrate the effects of all of these variables, forming a potential secondary cause of growth stasis at weaning. The notion that immunological stress can inhibit animal growth is well established, with pro-inflammatory cytokines such as IL-1, IL-6 and TNF-α implicated as primary mediators of this effect, through their modulation of intermediary metabolism of fat, protein and carbohydrate, inhibition of voluntary feed intake, stimulation of hepatic acute-phase protein synthesis, and other physiological and behavioural effects (Kelley et al., 1994; Johnson, 1997). 10.4.2

Alteration of intestinal morphology

The post-weaning period is usually characterised by villous atrophy and crypt hyperplasia in the small intestine (see Kelly et al., 1992; Pluske et al., 1997). Villous height has been shown to decrease rapidly to around 75% of pre-weaning values within 24 hours of weaning in pigs weaned at 21 days, and this villous atrophy

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was observed to continue, albeit at a slower rate, until 5 days after weaning (Figure 10.1; Hampson, 1986). Crypt elongation was observed to occur at a slower rate over the first 11 days of the weaning period, indicating an increase in epithelial cell mitosis (Hampson, 1986). Similarly, reductions in the length of microvilli have been reported after weaning (Cera et al., 1988). After the small intestine has recovered from the weaning process, the long thin villi that are typical of the neonate have been remodelled into the shorter tongue or leaf-shaped villi characteristic of the adult intestine. In more natural conditions, this transition is likely to have occurred slowly over the course of a gradual weaning process, however the abrupt weaning system employed in modern pig farming induces more precipitous morphological restructuring.

a 800 700 600 um

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Figure 10.1. Comparison of villous height (a) and crypt depth (b) at 2% along the small intestine, between unweaned pigs and pigs weaned at 21 days of age. * Significant difference between values for weaned vs. unweaned pigs (P<0.001) (from Hampson, 1986).

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The deleterious effects of weaning on gut architecture have been associated with a reduction in the specific activities of brush-border enzymes such as lactase isomaltase and sucrase, within 4 to 5 days after weaning (Hampson and Kidder, 1986; Miller et al., 1986). The combined effect of reductions in brush-border enzyme activity and small intestinal absorptive area are likely to impair the absorptive function of the intestine after weaning. This has been confirmed in several studies, measuring absorption of a standard dose of D-xylose (Miller et al., 1984a, b; Hampson and Smith 1986), alanine (Smith, 1984; Miller et al., 1986), and a solution containing glucose and electrolytes (Nabuurs et al., 1994). However, contrary to these results, Kelly et al. (1990, 1991a) and Pluske et al. (1996c) observed no reduction in the ability of villi to absorb xylose after weaning. Nevertheless, decreases in the absorptive capacity of the intestine may be a central determinant of the severity of post-weaning growth stasis. Supporting this notion, several authors have reported a high correlation between post-weaning growth rate and small intestine villous height (Li et al., 1991b; Pluske et al., 1995, 1996b). 10.4.3

Activation of the intestinal immune system

Activation of the gastrointestinal immune system during weaning has been described in various animal species, including the rat (Cummins et al., 1988a, b, 1991; Thompson et al., 1996; Masjedi et al., 1999) human (Machado et al. 1994; Cummins and Thompson, 1997), and pig (Vega-López et al., 1995; McCracken et al., 1999; Pluske et al., 1999; Solano-Aguilar et al., 2001). Using values derived at weaning (day 0) as a comparison, McCracken et al. (1999) observed that weaning in the pig at 21 days of age is associated with an increase in jejunal lamina propria CD4+ and CD8+ T lymphocytes within 2 and 7 days after weaning, respectively. These authors also reported increased expression of the active form of the matrix metalloproteinase stromelysin in jejunal explants during the initial 7 days after weaning, and a decrease in jejunal expression of MHC class I and II mRNA (McCracken et al., 1999). Similarly, Pluske et al. (1999) observed an increase in jejunal lamina propria CD4+ T cells within 24 hours of weaning at 21 days of age, but no change in CD8+ T cells, compared to values obtained at weaning. In contrast to these results, Vega-López et al. (1995) reported that by 4 days after weaning, piglets weaned at 21 days of age displayed an increase in lamina propria T cells (CD2+) compared to unweaned control piglets, but no increase in CD4+ or CD8+ T cells, indicating that the infiltrating cells were of the CD2+CD4-CD8phenotype. Vega-López et al. (1995) also observed an increase in granulocyte/macrophage cells in the crypt and villous regions of proximal small intestine lamina propria, and an increase in MHC class II+ APCs, after weaning. Somewhat paradoxically, despite the observed influx of immunocytes into the

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mucosa of piglets in this study, there was no evidence of increased activation of T cells or macrophages after weaning, as determined by IL-2 receptor expression. Similar results to Vega-López et al. (1995) were reported by Solano-Aguilar et al. (2001), who observed gradual changes in CD4+ and CD8+ T cells, monocytes granulocytes and macrophages (cells expressing the SWC3 surface antigen), and expression of the SLA-DQ surface antigen in the month after weaning at 17 days of age. However the study of Solano-Aguilar et al. (2001) did not provide an unweaned control for comparison, and sampling occurred somewhat erratically due to animal and/or lymphocyte yield limitations, making discrimination between age and weaning related changes problematic. Similarly determination of the time-course of immunological activity in the immediate post-weaning period (i.e. 1-7 days after weaning) is difficult due to long intervals between sampling and, in many cases, the absence data taken at the point of weaning. In this study the final pre-weaning sample was taken 6 days prior to weaning, and the first postweaning sample was taken 1 day after weaning. Since significant changes in immunological variables, such as T lymphocytes and MHC mRNA expression, have been observed in the first 24 hours after weaning (McCracken et al., 1999; Pluske et al., 1999), rigorous temporal sampling is required to illustrate the dynamic alterations in intestinal immunity in the immediate post-weaning period. However the study of Solano-Aguilar et al. (2001) provides useful and extensive data characterising relatively long-term alterations in mucosal lymphocyte subsets in the first month after weaning. Linking activation of the intestinal immune system at weaning with metabolic inflammatory responses on a systemic level, McCracken et al. (1995) observed that the decreasing ratio of villous height to crypt depth immediately after weaning is accompanied by an increase in plasma concentrations of the proinflammatory cytokine IL-1, the acute-phase protein fibrinogen, and glucagon, as well as increased liver weight, which is associated with acute-phase responses. Determining the causes of immune system activation at weaning has become a major focus in the pursuit of methods to ameliorate the physiological responses of piglets to the weaning process. In this context, two main hypotheses have emerged: (1) that anorexia of the piglet during the weaning period compromises the integrity of the intestine, allowing luminal antigens to penetrate the epithelial barrier initiating an active immune response in the underlying lamina propria; and (2) that the intestinal immune system is in an immature state at weaning, which impairs its ability to discriminate between harmful and innocuous antigen, and to generate appropriate active immune responses These hypotheses will now be discussed.

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10.4.3.1 Compromised epithelial barrier function Transient anorexia during the immediate post-weaning period is common in modern pig production. Voluntary feed intake after weaning is also extremely variable; grouphoused pigs weaned at 27 days of age have been reported to take an average of around 15 hours to start eating, although the interval between weaning and eating varied from close to zero to around four days after weaning (Bruininx et al., 2001). In a summary of several data sets, Le Dividich and Herpin (1994) concluded that the intake of piglets weaned at 21 days of age does not meet the daily metabolisable energy requirement for maintenance until the fifth day after weaning, and that the daily metabolisable energy intake achieved by the piglet during the pre-weaning period is not reached until two weeks after weaning. Increasing evidence supports the notion that luminal nutrition plays a pivotal role in determining the structure and function of the small intestine. For example, exclusion of luminal nutrients by total parenteral nutrition in piglets results in small intestinal villous atrophy and reduced crypt depth (Park et al., 1998; Ganessunker et al., 1999; Burrin et al., 2000); increased jejunal and ileal lamina propria CD4+ and CD8+ T cells, ileal MHC class II mRNA expression, and jejunal goblet cell numbers (Ganessunker et al., 1999); reduced epithelial cell mitosis (Burrin et al., 2000); reduced specific activity of mucosal sucrase and lactase (Park et al., 1998); and a negative protein accretion rate in the intestine (Stoll et al., 2000), compared to piglets offered luminal nutrition. Similar studies using rats have demonstrated that total parenteral nutrition increases epithelial permeability and bacterial translocation across the epithelial barrier, an effect that can be prevented through provision of luminal nutrition (Omura et al., 2000; Mosenthal et al., 2002). Similar symptoms are observed in piglets after weaning, from which it was inferred that the level of luminal nutrition received over the post-weaning period may play a key role in determining the structure and function of the piglet intestine during this time, as initially proposed by Kelly et al. (1984) and McCracken and Kelly (1984). The effect of feed intake on the pig intestinal mucosa has been illustrated in numerous studies (Kelly et al., 1984, 1991a, b; McCracken and Kelly, 1984; Pluske and Williams, 1995; Núñez et al., 1996; Pluske et al., 1996a, b, c; McCracken et al., 1999; Spreeuwenberg et al., 2001; Verdonk et al., 2001a, b). Taken together, these studies show that a reduction in luminal nutrition produces atrophy of the intestinal mucosa, and that mucosal atrophy over weaning can be ameliorated by maintaining a continuous supply of luminal nutrition during this time. Furthermore, it is hypothesised that transient anorexia over the weaning period compromises intestinal barrier function, allowing luminal antigens to penetrate the lamina propria, inducing intestinal inflammation which exacerbates the adverse morphology (McCracken et al., 1999).

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Supporting this hypothesis, Verdonk et al. (2001a) observed an increase in paracellular, but not transcellular, transport within 2 days of weaning at approximately 26 days of age, which continued until at least 4 days after weaning, when measurement was ceased. This was accompanied by the characteristic postweaning reduction in villous height, and increase in crypt depth. Furthermore, Verdonk et al. (2001a) showed that piglets maintained on a low level of nutrient intake after weaning had significantly increased paracellular, but not transcellular, transport, and reduced villous height in the proximal small intestine, compared to piglets maintained on a high level of nutrient intake. Similar results were reported by Spreeuwenburg et al. (2001), who concluded that diminished enteral stimulation and stress at weaning compromise small intestinal barrier function in pigs within 2 days of weaning at 26 days of age. Commensurate with the increase in paracellular transport observed in this study was a numerical increase in crypt lamina propria CD8+ T cells, which was positively correlated to both paracellular and transcellular transport (as measured by transport of GlySar and mannitol, respectively), and a numerical decrease in CD4+ T cells, leading to a significantly reduced ratio of CD4+:CD8+ T cells (Table 10.1). Spreeuwenburg et al. (2001) observed that these changes were accompanied by atrophy of intestinal villi, with villous height and ratio of villous height to crypt depth negatively correlated with lamina propria CD8+ T cell numbers and tending to be negatively correlated with lamina propria CD4+ T cell numbers. Collectively, these results suggest that low nutrient intake after weaning impairs the integrity of the tight junctions between epithelial cells lining the small intestine, increasing paracellular permeability, and

Table 10.1. Transepithelial transport and T lymphocyte subsets in the small intestine of pigs fed a liquid milk replacer after weaning (from Spreeuwenburg et al., 2001). Days

Trans-epithelial transport

T lymphocyte subsets

n

n

post-weaning GlySar

Mannitol

12 12 12 12

16.6 15.6 16.8 19.8 152 NS

CD8+

CD4+:CD8+

n/106 mm2 crypt lamina propria

10-6 cm/s 0 1 2 4 SEM P-value of model

CD4+

6.6b 8.1b 12.2a 11.9a 0.88 0.01

12 18 18 18

216 125 195 226 30.7 NS

117 116 168 167 28.9 NS

2.2a 1.1c 1.4bc 2.0ab 0.26 0.05

a,b,c

Means within a column with different superscripts are significantly different at the Pvalue designated by the model. NS, non-significant (P>0.05).

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potentially allowing luminal antigens into the underlying lamina propria where an active immune response may be initiated. Similar results were reported by McCracken et al. (1999), who observed expansion of lamina propria CD4+ and CD8+ T cells within 2 days of weaning at 21 days of age (Figure 10.2), which coincided with a reduction in villous height of around 65% compared to that observed at the point of weaning. This was accompanied

A

A

B

B

Figure 10.2. Enumeration of CD4+ (i) and CD8+ (ii) T cells in jejunal villous (A) and crypt (B) lamina propria of pigs offered either a milk (M)- or soy (S)-based diet after weaning. * Values differ significantly (P<0.05) from those at Day 0; Different letters (a,b) indicate a significant difference (P<0.05) between groups M and S (from McCracken et al., 1999).

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by increased expression of the matrix metalloproteinase stromelysin, which peaked at 4 days after weaning, suggesting a link between expression of inflammatory matrix metalloproteinases and intestinal atrophy in the weaner piglet. McCracken et al. (1999) also observed reduced expression of MHC class I mRNA in the day after weaning, which was attributed to an effect of increased plasma cortisol levels caused by weaning stress, as observed by Wu et al. (2000). In the study by McCracken et al. (1999), increased expression of MHC class I mRNA, which generally occurs during inflammatory responses, did not occur in the first 7 days after weaning, however they suggest this may also reflect cortisol-induced inhibition of the AP1 family of transcription factors which activate MHC class I gene expression, since the post-weaning cortisol surge may not decline until between 2 and 8 days after weaning (Wu et al., 2000). Expansion of T cell subsets in the lamina propria after weaning reported by Spreeuwenburg et al. (2001) and McCracken et al. (1999) was also reported by Pluske et al. (1999), who observed an increase in lamina propria CD4+ T cells within 24 hours after weaning at 28 days of age, although CD8+ T cell numbers were unchanged compared to that observed at the point of weaning. Expansion and activation of CD8+ T cells can indicate induction of a cellular immune response, which promotes secretion of various proinflammatory cytokines, such as INF-γ and TNF-α, which bolster the inflammatory response and cause injury to the gut tissue (MacDonald, 1999). T cell activation in this manner has been shown to induce crypt hyperplasia, villous atrophy and matrix metalloproteinases that degrade extracellular matrix proteins (MacDonald and Spencer, 1988; Ferreira et al., 1990, Pender et al., 1997; MacDondald et al., 1999; Monteleone, 1999). The data of Spreeuwenburg et al. (2001), in which CD8+ and to a lesser degree CD4+ T cell numbers were negatively correlated to intestinal villous height, implicate anorexiainduced expansion of T cell subsets in the pathology of mucosal atrophy at weaning. Furthermore, the observation by McCracken et al. (1999) that weaning anorexia is associated with increased expression of matrix metalloproteinases elucidates a mechanism through which the observed tissue remodelling could be mediated in pigs. The decreased expression of MHC class I mRNA observed by McCracken et al. (1999) may also suggest a reduction in presentation of viral antigens and the associated cytotoxic T lymphocyte recognition and destruction of host cells, resulting in an increased susceptibility to viral disease during the post-weaning period. 10.4.3.2 Hypersensitivity to dietary antigen Villous atrophy and crypt hyperplasia similar to that observed at weaning has been documented in cases of human dietary allergies, such as coeliac disease (Ferguson et al., 1984), where inappropriate active mucosal immune responses are mounted against dietary antigens. Immune responses to dietary proteins have often been

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observed after weaning in the pig, where weaning onto a soy protein-based diet has been shown to result in appearance of serum IgG antibodies specific for glycinin and β-conglycinin, which are major storage proteins of the soybean (Wilson et al., 1989; Li et al., 1990, 1991a, b; Dréau et al., 1994). Consumption of soy protein containing glycinin and β-conglycinin after weaning has also been associated with increased density of intestinal CD2+, CD4+ and CD8+ T cells (Figure 10.3) and plasma cells (Dréau et al., 1995), as well as villous atrophy and crypt hyperplasia (Dréau et al., 1994; Li et al., 1990, 1991a, b). This immune response has been linked to depressed growth rate after weaning, with a significant amount of the variation in weight gain after weaning explained by systemic immune responses to soybean meal, as indicated by delayed-type skin hypersensitivity reactions and serum antibodies (Li et al., 1990). In this study, weight gain after weaning was negatively correlated with delayed-type hypersensitivity reactions to intradermal soybean protein, which is consistent with the hypothesis that cellular immune responses after weaning impair performance. Immune response to dietary soybean protein appears to be most evident in younger pigs, with antibody responses decreasing with age (Wilson et al., 1989). This suggests that the immune system of the young pig is particularly prone to mounting inappropriate immune responses to dietary antigen. Soy protein-induced primary immune responses appear to be followed by immunological tolerance rather than

1400

**

No. cells per mm 2

1200 1000 800

ETSP HTSP

**

600

*

400 200 0

CD2+

CD4+

CD8+

T lymphocyte subset

Figure 10.3. Lamina propria lymphocyte subsets of pig offered diets containing low and high levels of conglycinin and (-conglycinin (ethanol-treated soy protein (ETSP) and heat-treated soy protein (HTSP), respectively), for 7-9 days after weaning at 21 days of age. *, ** Significantly different from ETSP group P<0.05 and P<0.01, respectively (from Dréau et al., 1995).

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priming, with pigs injected with soy protein after primary exposure displaying minimal immune responses compared to those that are naïve to soy protein (Bailey et al., 1993). This suggests that the primary immune mechanism controlling soybean hypersensitivity is classical ‘oral tolerance’ (Bailey et al., 2001a), as previously described. For more comprehensive reviews of this area of research the reader is directed to the work of Stokes et al. (1987), Miller et al. (1994) and Bailey et al. (2001a, b). Exactly what immunological factors may predispose the weaner pig to development of dietary hypersensitivity is currently unknown. However, it has been suggested that weaning, which is associated with depression of humoral immune responses (Blecha et al., 1983; Wattrang et al., 1998); mixing and housing changes, which have been reported to alter parameters of immunity and immune response (Hicks et al., 1998; Kelly et al., 2000); weaning stressors such as low temperatures or draughts, which have been shown to influence T cell responses to non-specific mitogens (Blecha and Kelley, 1981; Scheepens et al., 1994); and stress-induced cortisol release, which has been observed to suppressive effect on immune function (Westly and Kelley, 1984; Brown-Borg et al., 1993), may disturb the development of the intestinal immune system, impairing its ability to discriminate between harmful and innocuous antigen (Bailey et al., 2001). Although the hypothesis that soybean hypersensitivity is a common cause of growth stasis after weaning has generally gained acceptance in pig science, evidence of mucosal mast cell involvement in its pathogenesis has yet to be shown (Gaskins, 1997). Mucosal mast cells are an integral component of classical hypersensitivity reactions, producing a wide array of inflammatory mediators in response to antigenic stimulation, resulting in increased ion secretion into the gut lumen and increased epithelial and vascular permeability (Befus et al., 1988; Malaviya and Abraham, 2001; Yu and Perdue et al., 2001). Also, dietary and non-dietary factors have been implicated in post-weaning growth stasis of pigs offered a soy-containing diet, implying that, if present, hypersensitivity to soy protein may be one of several factors involved in poor performance after weaning (McCracken et al., 1995). Indeed, the observations of McCracken et al. (1999) led them to suggest that soy-hypersensitivity reactions at weaning may occur subsequent to inflammation induced by postweaning anorexia, since expansion of T cell subsets occurred immediately after weaning regardless of whether soy or milk-based diets were consumed at this time (Figure 10.2). Given the apparently pivotal role of feed intake on intestinal morphology and immunity, the absence of individual feed intake measurements in many studies reporting immunological and morphological effects of soy hypersensitivity (Dréau et al., 1994; Li et al., 1990, 1991a, b) suggests that these two variables are often confounded.

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To minimise or alleviate post-weaning inappetence through strategies that promote food intake is obviously an important target in pig production, however understanding the inputs required to stimulate functional maturity of the developing pig immune system, in relation to handling both dietary and bacterial antigens, is equally important. In this regard, factors that promote the regulatory systems governing tolerance, inflammation and active immunity require further investigation.

10.5

Conclusion

The modern practice of abrupt early weaning represents a formidable challenge for the intestinal immune system, a fact that is exemplified by the alterations in intestinal immunity that weaning causes. However, in a multi-factorial situation such as weaning, determination of the relative importance of different factors is inevitably difficult, and results are likely to vary due to subtle, and perhaps unpredictable, factors. This renders problematic the goal of establishing, with a high degree of certitude, the predominant cause of poor and variable postweaning performance. Significant evidence exists supporting both the luminal nutrition and soybean hypersensitivity hypotheses, in some cases in the same experiment (McCracken et al., 1995; McCracken et al., 1999). This serves to emphasise that neither hypothesis precludes the other, and both problems are likely to significantly affect post-weaning growth performance. In the absence of irrefutable evidence contradicting either hypothesis, it is therefore prudent to make every effort to maintain a constant level of luminal nutrition over the weaning period, and to defer the inclusion of soybean protein in weaner diets until a greater level of maturity has been reached. Weaning at a greater age, and hence level of developmental maturity, can diminish weaning-induced immune responses (Wilson et al., 1989; Bianchi et al., 1992). Given the extensive physiological and behavioural effects of pro-inflammatory cytokines, which hinder growth during active immune responses (Kelley et al., 1994; Johnson, 1997; Stahly, 2001), control of the post-weaning immune response is a valuable objective in pig production.

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van Hooijdonk, A.C., K.D. Kussendrager and J.M. Steijns, 2000. In vivo antimicrobial and antiviral activity of components in bovine milk and colostrum involved in non-specific defence. British Journal of Nutrition 84 (Supplement 1), S127-S134. van Vlasselaer, P., J. Punnonen and J.E. de Vries, 1992. Transforming growth factor β directs IgA switching in human B cells. The Journal of Immunology 148, 2062-2067. Vega-López, M.A., G. Arenas-Contreras, M. Bailey, S. González-Pozos, C.R. Stokes, M.G. Ortega and R. Mondragón-Flores, 2001. Development of intraepithelial cells in the porcine small intestine. Developmental Immunology 8, 147-158. Vega-López, M.A., M. Bailey, E. Telemo and C.R. Stokes, 1995. Effect of early weaning on the development of immune cells in the pig small intestine. Veterinary Immunology and Immunopathology 44, 319-327. Vega-López, M.A., E. Telemo, M. Bailey, K. Stevens and C.R. Stokes, 1993. Immune cell distribution in the small intestine of the pig: immunohistological evidence for an organized compartmentalization in the lamina propria. Veterinary Immunology and Immunopathology 37, 49-60. Verdonk, J.M.A.J., M.A.M. Spreeuwenberg, G.C.M. Bakker and M.W.A. Verstegen, 2001a. Nutrient intake level affects histology and permeability of the small intestine in newly weaned piglets. In: Lindberg, J.E. and B. Ogle (editors), Digestive Physiology of Pigs: Proceedings of the 8th Symposium. CABI Publishing, UK, pp. 332-334. Verdonk, J.M.A.J., M.A.M. Spreeuwenberg, G.C.M. Bakker and M.W.A. Verstegen, 2001b. Effect of protein source and feed intake level on histology of the small intestine in newly weaned piglets. In: Lindberg, J.E. and B. Ogle (editors), Digestive Physiology of Pigs: Proceedings of the 8th Symposium. CABI Publishing, UK, pp. 347-349. Wagstrom, E.A., K.J. Yoon and J.J. Zimmerman, 2000. Immune components in porcine mammary secretions. Viral Immunology 13, 383-397. Wattrang, E., P. Wallgren, A. Lindberg and C. Fossum, 1998. Signs of infections and reduced immune functions at weaning of conventionally reared and specific pathogen free pigs. Journal of Veterinary Medicine Series B 45, 7-17. Weiner, H.L. 2000. Oral tolerance, an active immunologic process mediated by multiple mechanisms. The Journal of Clinical Investigation 106, 935-937. Westly, H.J. and K.W. Kelley, 1984. Physiologic concentrations of cortisol suppress cell-mediated events in the domestic pig. Proceedings of the Society for Experimental Biology and Medicine 177, 156-164. Weström, B.R., J. Svendsen, B.G. Ohlsson, C. Tagesson and B.W. Karlsson, 1984. Intestinal transmission of macromolecules (BSA and FITC-labelled dextrans) in the neonatal pig: influence of age of piglet and molecular weight of markers. Biology of the Neonate 46, 20-26. Whary, M.T., A. Zarkower, F.L. Confer and F.G. Ferguson, 1995. Age-related differences in subset composition and activation responses of intestinal intraepithelial and mesenteric lymph node lymphocytes from neonatal swine. Cellular Immunology 163, 215-221. Wheeler, E.E., D.N. Challacombe, P.J. Kerry and E.C. Pearson, 1993. A morphological study of betalactoglobulin absorption by cultured explants of the human duodenal mucosa using immunocytochemical and cytochemical techniques. Journal of Pediatric Gastroenterology and Nutrition 16, 157-164.

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Williams, R. and R. Gibbons, 1972. Inhibition of bacterial adherence by secretory immunoglobulin A: a mechanism of antigen disposal. Science 177, 697. Wilson, A.D., K. Haverson, K. Southgate, P.W. Bland, C.R. Stokes and M. Bailey, 1996. Expression of major histocompatibility complex class II antigens on normal porcine intestinal endothelium. Immunology 88, 98-103. Wilson, A.D., C.R. Stokes and F.J. Bourne, 1989. Effect of age on absorption and immune responses to weaning or introduction of novel dietary antigens in pigs. Research in Veterinary Science 46, 180-186. Wood, P.R. and H.-F. Seow, 1996. T cell cytokines and disease prevention. Veterinary Immunology and Immunopathology 54, 33-44. Wu, G., C.J. Meininger, K. Kelly, M. Watford and S.M. Morris, 2000. A cortisol surge mediates the enhanced expression of pig intestinal pyrroline-5-carboxylate synthase during weaning. Journal of Nutrition 130, 1914-1919. Yu, L.C.H. and M.H. Perdue, 2001. Role of mast cells in intestinal mucosal function: studies in models of hypersensitivity and stress. Immunological Reviews 179, 61-73. Zhang, G., C.R. Ross and F. Blecha, 2000. Porcine antimicrobial peptides: new prospects for ancient molecules of host defense. Veterinary Research 31, 277-296. Zuckermann, F.A. 1999. Extrathymic CD4/CD8 double positive T cells. Veterinary Immunology and Immunopathology 72, 55-66. Zuckermann, F.A. and H.R. Gaskins, 1996. Distribution of porcine CD4/CD8 double positive T lymphocytes in mucosa-associated lymphoid tissues. Immunology 87, 493-499.

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11 Nutritional requirements of the weaned pig M.D. Tokach, S.S. Dritz, R.D. Goodband and J.L. Nelssen

Summary The challenges for feeding early-weaned pigs extend beyond diet formulation and nutrient requirements. Recognizing that many of these challenges are interrelated and addressing areas will lead to successful early-weaned pig feeding programs.

11.1

Introduction

The basic rules for a successful nutritional program for the weaner pig can be summarized as follows: 1) start with as heavy a pig as possible; 2) feed as simple of diets (low cost) as possible, and 3) focus on nursery management. In this chapter, we will discuss these three points and their importance in designing nutrition programs for the weaner pig. Most of the chapter will focus on nutrient requirements and diet formulation. However, we cannot overlook the importance of initial pig weight and age and quality of husbandry, and their influence on pig performance and the diet formulation strategy.

11.2

Importance of pig weight and age

The optimal feeding patterns for lactating sows continue to be debated. However, the research results in this area are clear. Restricting feed, protein, or energy intake during any period of lactation will reduce milk production, decrease litterweaning weight, and impair subsequent reproductive performance (King and Martin, 1989; Koketsu et al., 1997, Koketsu and Dial, 1998; Tokach et al., 1992). With the implementation of early weaning strategies (< 21 days), the importance of litter weaning weight has increased. Pigs weaned at heavier weights and older ages are simply easier to manage in the nursery and have a lower risk of developing enteric disease (Cranwell et al., 1995; Madec et al., 1998). Other data indicate that pigs with lighter weights at weaning are at a higher risk of death (Deen et al., 1998). Unfortunately, management-induced energy deficiency during lactation leading to failure to achieve potential weaning weights is a major problem on many commercial swine farms. In a recent experiment, we characterized the importance of weaning age on growth performance in the first 28 d after weaning. We grouped pigs by age (12 to 15 d, 16 to 18 d, and 19 to 21 d old) and weight (light or heavy) within each age category (Table 11.1). We found a weaning age by growth performance interaction (P < .07). Note that the difference in average weight between the heavy and lightweight categories was approximately 1 kg (Figure 11.1). Thus, the heavy 12 to 15-d and

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Table 11.1. Influence of weaning age (d) and weaning weight (lb) on nursery performance. (Dritz, 2002). Age

12 to 15

Item Wt d 0 to 28 ADG, g ADFI, g Feed/gain

Light Heavy Light Heavy Light Heavy SEM

Weight

Age

213 309 1.46

0.05 0.04 0.83

0.01 0.07 0.01 0.79 0.10 0.04

241 331 1.38

16 to 18

286 381 1.35

286 395 1.39

19 to 21

309 395 1.37

295 409 1.39

P Value

5 9 0.02

Wt x Age

*Each number is the mean of 12 pens (21 pigs/pen), and pigs averaged 5.3 kg at weaning.

7 L1215

Weig ht , k g

6

H1215

5

L1618

4

H1618

3

L1921

2

H1921

1 0 0

7

14

21

28

35

42

Days after weaning

Figure 11.1. Influence of weaning weight and age on weight difference between groups (Dritz, 2002).

the light 16 to 18-d old categories averaged similar weights at weaning. The heavy 16 to 18-d and light 19 to 21-d old categories also averaged similar weights at weaning. The youngest pigs at weaning gained the least from day 0 to 42 after weaning. The data clearly show that weaning weight is important with all ages of pigs; however, the impact of weaning weight was not as important as weaning age. When comparing pigs that were 16 days or older at weaning, the weight differences at weaning were only slightly increased by day 42 after weaning. Weaning weight was also important for pigs weaned at less than 16 days; however, age also becomes a critical factor as pigs with heavier weaning weights within the 12 to 15 d old category were not able to compensate for their young age. The heavy 12 to 15 day old pigs had the same weaning weight as the light 16 to 18 day old pigs; however, they were 2 kg lighter at day 42 after weaning. Weaning weight differences also become magnified

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with young pigs. Note that while the light 12 to 15 d old pigs were 1 kg lighter at weaning than the light 16 to 18 d old pigs, the difference had magnified to 4 kg by 42 d after weaning. Average age at weaning or lactation length calculated at weaning is based on the date of the last recorded wean event for the sow in most record keeping systems. In many farms where pigs are weaned multiple times per week, the heaviest pigs in a litter are weaned before the remainder of the litter. Thus, the actual average weaning age of the pigs will be lower than that stated on the summary report. We have observed actual weaning age as much as 1 day younger than that reported from average lactation length calculated from the sow wean event. Another common practice, even on farms that have strict policies about movement of pigs among rooms, is to hold back older lightweight pigs to wean them at an older age. This is another phenomena that will not be highlighted in records because the average age at weaning will be calculated based on the wean event of the sow. Actual data from an experiment by Donavan and Dritz (2000) indicated that, on a farm with a 21 d maximum weaning age policy, 7.8% (83/1,062) of pigs were actually greater than the desired 21 d maximum age (Figure 11.2) and 1.4% (15/1,062) were weaned at greater than 26 d of age. Also, note that 12% (128/1,062) of the pigs were weaned at 15 d of age or less. Examination of 1,800 pigs from another production system in which piglets are tattooed with date of birth indicated that 17% were greater than 21 d of age at weaning when the policy of maximum weaning age was 21 days.

26 M or e

25

24

23

22

21

20

19

18

17

16

15

14

200 180 160 140 120 100 80 60 40 20 0 13

Frequency

Strict adherence to maximum weaning age has been advocated to minimize transfer of infectious disease. Also, a narrow spread of weaning age has been indicated as desirable for success of isowean programs with a maximum of 20 d of age suggested

Age, d

Figure 11.2. Histogram of ages at weaning (Dritz, 2002).

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for the elimination or control of most swine pathogens (Harris, 2000). Our experience indicates that the actual weaning age of groups of pigs is highly variable based on farrowing house management practices. Therefore, even though most weaner pig nutritional programs are based on pig weight, we believe understanding the mean and variation in age are important for successful nutrition programs.

11.3

Basis of nutrient specifications for weaner pigs

We adhere to three key concepts when formulating diets for the weaner pig. First, the economics of today’s swine industry dictate that we must adjust pigs to the simplest and relatively lowest cost diets (i.e., grain and soybean meal) as quickly as possible after weaning. Second, we must remember that the newly weaned pig is in an extremely energy dependent stage of growth and that maximizing feed (energy) intake is essential. Third, we must remember the digestive physiology of the weaner pig and formulate the initial diets with highly digestible ingredients that complement the pattern of digestive enzymes secreted at weaning. One example emphasizing all three of these concepts is the practice of using soybean meal in diets fed immediately after weaning. Some nutritionists believe that weanling pigs should be fed diets with no or very little soybean meal immediately after weaning and that the level should be steadily increased over time. This slow and very gradual introduction of soybean meal into the pig’s diet will minimize the potential for delayed-type hypersensitivity to the soy proteins, conglycinin and betaconglycinin (Li et al., 1990a,b; 1991a,b) and, thus, generally results in excellent growth performance initially after weaning. However, it also leads to very high nursery feed cost. A second option is to feed a diet with a moderate level (10 to 15% of the diet for pigs weaned between 15 and 21 days of age) of soybean meal as a partial replacement for more expensive specialty protein sources (Friesen et al., 1993a). This approach is a compromise between feeding extremely expensive all milk- and animal specialty protein-based diets and simple grain-soybean mealbased diets. As a result, the pig’s feed intake is stimulated by the lactose and specialty protein sources, which are highly digestible and palatable and, thus, increase energy intake. At the same time, the pig becomes exposed to the moderate amount of soybean meal protein, minimizing the negative effects of a delayed-type hypersensitivity response. As a result the amount of soybean meal in the diet can be quickly increased in a phase feeding program to decrease the need for the more expensive specialty protein sources. The net result of using soybean meal in this fashion is that we can still provide a highly digestible complex diet that stimulates feed intake immediately after weaning, and then quickly reduce diet complexity by increasing the amount of soybean meal protein (Dritz et al., 1996a). This strategy takes advantage of the fact that the impact of diet complexity on feed intake and pig performance decreases

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rapidly after weaning, especially in high health pigs. Thus, a feeding program can be developed that nutritionally allows for maximum growth performance and yet will be economically competitive. 11.3.1

Ingredient selection based on digestive capacity

Selection of different types and amounts of other feed ingredients also should be based on the three primary criteria of quickly reducing diet complexity to lower feed cost, maximizing feed (energy) intake, and physiology of the digestive system. Indeed, ingredient selection in addition to cost should be based on factors including nutrient digestibility, amino acid density, lactose concentration, and stimulatory affects on feed intake and(or) growth. Another consideration is how an ingredient or combination of ingredients will react under various feed processing methods. The use of added fat is an example of this latter consideration. Although added fat is not well utilized by the pig as an energy source immediately after weaning, its inclusion is essential if diets containing high levels of milk and other specialty protein sources are to be pelleted. The newly weaned pig’s digestive system is relatively immature but, at the age of weaning, well adapted to digest the proteins, lactose, and lipids secreted in sow’s milk. It has been well established that inclusion of lactose containing ingredients assists in the transition at weaning from sow’s milk to a dry diet (Tokach et al., 1989; Mahan, 1992; Nessmith et al., 1997). However, evidence may suggest that despite our best attempts to mimic the nutrient composition of sow’s milk in a dry diet, there are dramatic changes that take place in the size, shape, and functioning of the villi in the small intestine (Cera et al., 1988a; Li et al., 1990a, 1991a,b; Jiang et al., 2000). The anatomical changes in the villi after weaning may be a possible cause for poor utilization of some ingredients. For example, the anatomical changes in the villi may cause the reduction in secretion of fatty acid binding protein, which correlates with poor fat utilization by pigs for approximately 10 to 14 days after weaning (Reinhart et al., 1990). Ingredient selection also can change the degree to which these changes in the structure and functioning of the villi take place. An example is the shearing of villi caused by the delayed-type hypersensitivity reaction to excessive soybean meal fed immediately after weaning (Figure 11.3; Li et al. 1990a,b). Certain ingredients, such as spray-dried animal plasma, also may have a positive effect on intestinal development (Jiang et al., 2000). Although our understanding of the influence of ingredient selection on structure and functioning of the villi has improved, the rapid change in function of the villi at weaning still seems to be a primary challenge in weanling pig nutrition. Despite the changes in digestive physiology at the time of weaning, protein source solubility within the intestine appears to be the primary limitation to digestion in the early-weaned pig (Asche et al., 1989a,b).

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Figure 11.3. Villi of small intestine after being fed high levels of soybean meal (left panel) or a milk-based diet for two weeks after weaning (right panel).

11.4

Nutrient requirements of the weaned pig

11.4.1

Energy

Weanling pigs simply do not eat enough feed to maximize their potential for protein deposition. Thus, any increase in feed (energy) intake will result in a further increase in growth rate provided proper nutrient to calorie ratios are maintained. In order to maximize energy intake, ingredients must be highly palatable to stimulate feed intake, highly digestible, and contain a high net energy concentration. When selecting protein and energy sources, their impact on feed intake must be carefully considered. Individual feed ingredients will be discussed later in this chapter, together with the importance of management decisions to increase feed intake. 11.4.2

Amino acids

Because of dramatic improvements in our understanding of the environmental requirements of weanling pigs as well as management and pig flow practices that result in minimizing exposure to disease antigens, protein deposition and, thus, amino acid requirements have increased over the past 10 years. Although the lysine requirement estimate for the weanling pig has increased in recent publications (NRC, 1998), many would argue that these requirement estimates may still be too low for the high-health, high lean growth potential pigs in commercial production systems.

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Data from Owen et al. (1995d,e), Chung et al. (1996), and Williams et al. (1997b) all estimate a similar lysine requirement of the weanling pig of approximately 1.60% total lysine, or approximately 1.40% apparent digestible lysine for the first 14 days after weaning at 14 to 22 days of age. Because weaner pigs are in an energy dependent phase of growth, diets should be formulated on amino acid to calorie ratios, rather than percentages of the diet. Using the energy content of the diets of Owen et al. (1995d), Chung et al. (1996) and Williams et al. (1997b), a lysine to calorie ratio of approximately 4.1 to 4.2 g apparent digestible lysine/Mcal ME is suggested. Because of the limited utilization of added fat by the weanling pig immediately after weaning, the actual lysine to calorie ratio may be underestimated in this age pig. As the pig becomes older and heavier, the optimum lysine to calorie ratio decreases to approximately 3.3 g apparent digestible lysine/Mcal ME for the 22 kg pig (Nam and Aherne, 1994; Smith et al., 1999b). Information on the requirement estimates of other amino acids, particularly on a ratio relative to lysine, is less abundant. However, it would appear that the optimum minimum ratios of other amino acids relative to lysine on a true digestible basis are: methionine, 30% of lysine (Chung and Baker, 1992; Owen et al., 1995a,b); methionine and cysteine, 55% of lysine; isoleucine, 55% of lysine (Kerr, 1999; James et al., 2001a); tryptophan 16% of lysine (Han et al., 1993); valine 60% of lysine (James et al., 2001c). However, results of titration studies evaluating threonine requirements are less definitive. Threonine estimates range from approximately 60% to 68% relative to lysine (Johnston et al., 2000; James, et al., 2001b). Because of the relatively low concentration of threonine in many specialty protein sources fed to weanling pigs and the cost of crystalline threonine, the variation in requirement estimates has a potentially large economic burden. Listed in Table 11.2 are suggested lysine to calorie ratios and ratios of other amino acids to lysine for pigs from 3 to 22 kg. 11.4.3

Other approaches to determining a requirement estimate

One reason for the disparity between requirement estimates derived from typical titration studies and levels used in commercial production may be related to our method of defining a requirement. In academia, we often titrate an increasing concentration of an amino acid and record the response in daily gain and feed efficiency. We then fit the data to a broken-line model, where we have an increasing response up to a point (the requirement), after which there is a plateau with no further improvement in performance. Full economic evaluation of a requirement is not usually conducted in academia, but there might be an estimate of feed cost per unit gain. Unfortunately, the fitting of most data to a “broken line” is more the result of our inability to have as many treatments and replications as what would be ideal because of the physical constraints of many research facilities. From a biological standpoint, because there are frequently continued, albeit diminishing, improvements in a response criterion beyond the estimated requirement, fitting data to a broken line to establish a requirement will have its

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Table 11.2. Amino acid recommendations for pigs from 3 to 22 kg. Weight range, kg Item

3 to 5

5 to 7

7 to 11

11 to 23

Total lysine:calorie ratio, g/Mcal ME Apparent digestible lysine:calorie ratio True digestible lysine:calorie ratio Approximate total lysine, % Approximate true digestible lysine, %

4.7 4.0 4.2 1.65 1.50

4.5 3.9 4.1 1.55 1.40

4.0 3.4 3.5 1.35 1.22

3.8 3.2 3.3 1.30 1.16

Ratios relative to lysine on true digestible basis Isoleucine, % Methionine, % Total sulfur amino acids, % Threonine, % Tryptophan, % Valine, %

55 27.5 55 62 16 60

limitations and almost in all cases derive a conservative (low) requirement estimate. For example, using the broken line method on the data in Table 11.3, we would derive a requirement of approximately 1.10% lysine for ADG (James et al., 2000). However, F/G continued to improve slightly through 1.40% lysine. The interesting aspect of this case is trying to determine the optimal lysine level to feed in this production system. To answer this question, we used a ten-year historical price series for corn, soybean meal, choice white grease and market hogs. We then determined which diet provided the lowest feed cost per pound of gain and the greatest margin over feed cost in each month according to procedures of De La Llata et al. (2001). The average value from the ten-year period (120 months) is shown in Table 11.3. The diet containing 0.95% lysine provided the lowest feed cost per lb of gain in 100 of the 120 months, or 83% of the time. The diets containing 1.10% lysine or 1.40% lysine had the lowest feed cost per pound of gain in 5 (4%) and 15 (13%) of the 120 months, respectively. However, a slightly different answer results when a value is placed on the extra weight gain of pigs fed the higher lysine diets. On average, diets formulated to 1.10, 1.25 or 1.40% lysine provide an extra $1.27 to $1.63 return over feed cost compared to the diet formulated to 0.95% lysine. An additional $2.57 to $2.93 return over feed cost was captured compared to the diet formulated to 0.80% lysine. In 118

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Table 11.3. Economic value (in U.S. $) of increasing the dietary lysine level for pigs from 40 to 80 lb. (James et al., 2000). Total dietary lysine, % Economic calculations

0.80

0.95

1.10

1.25

1.40

Diet cost, $/ton Feed cost, $/pig

147.52 4.65

154.53 4.67

161.55 5.18

168.82 5.27

176.05 5.40

Wt gain in 28 d, lb Feed cost, $/kg gain Value of gain at $1.025/kg, $/pig Return over feed cost, $/pig Extra return over 0.8% lysine ($)

15.7 0.295 16.13 13.58

16.9 0.276 17.30 14.88 1.30

18.6 0.280 18.99 16.28 2.70

18.5 0.287 18.86 16.05 2.57

18.9 0.284 19.38 16.51 2.93

of the 120 months (98%), the diet containing 1.40% lysine provided the greatest return over feed cost. The diet containing 1.10% lysine provided the greatest return in the other 2 months. The results of this analysis indicate that diets for pigs weighing 18 to 35 kg can be formulated from 1.10 to 1.40% lysine with similar economic results. The slight improvement in F/G at higher lysine levels offsets the increase in diet cost to result in similar return over feed cost. It is important to note that the optimal lysine level (1.10 to 1.40% lysine) would rarely have minimized feed cost per pound of gain, but almost always maximized margin over feed costs. Clearly this type of analysis can lead to different requirement estimate than more conventional procedures, thus explaining a portion of the possible variation in nutrient concentrations used in diets. Another method to evaluate the same data set is shown with regression analysis. Regression analysis was applied to the data from the growth trial to generate regression equations. The regression equations allow us to predict the response in ADG and F/G to each incremental increase in lysine in the diet. The regression equations also allow us to predict which lysine level would provide the greatest margin over feed cost for month in the 120-month price series (Figure 11.4). This analysis indicates that, with the exception of late 1998 when the pig price dropped significantly, the optimal lysine level for this period was always between 1.25 and 1.3%.

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1.4

Lysine, %

1.3 1.2 1.1

1998

1997

1996

1995

1994

1993

1992

1991

1990

1989

1988

1

Figure 11.4. Dietery lysine level that would have provided the greatest return over feed cost for each month (Adapted from James et al., 2000).

11.4.4

Vitamins

Conducting research evaluating vitamin requirements of weanling pigs is frustrating because of the tremendous variation in response between trials. These oftenconflicting results appear to be somewhat characteristic of studies conducted on vitamin requirement estimates. It is likely that factors such as age, health, environment, lean growth potential, and diet may influence responses to added vitamins. While it seems there is tremendous trial-to-trial variation in pigs’ responses to vitamin supplementation, one observation is certain: current NRC (1998) vitamin requirement estimates are too low for pigs in commercial production. Vitamins that should be routinely supplemented in weaner diets include the fat soluble vitamins A, D, E, and K and the water soluble vitamins B12, niacin, pantothenic acid, and riboflavin. Of the fat-soluble vitamins, the majority of research has been conducted on vitamin E because it is generally one of the most expensive vitamins to add to a diet. Data would indicate that if the sow has adequate supplemental vitamin E and selenium in gestation and lactation diets (44 IU/kg and 0.3 ppm, respectively; Mahan, 1994), supplementing nursery diets to 44 IU/kg of added vitamin E should be adequate. However, if breeding herd diets contain less than 44 IU/kg, greater than 44 IU/kg of feed added in nursery diets may be needed in some herds to minimize the incidence of mulberry heart occurrence post weaning. Wilson et al. (1991, 1993), in a series of studies, observed that multiple B-vitamin supplementation to concentrations 3 to 4 times NRC estimates resulted in improved growth performance of weanling pigs. For the most part, the feed industry typically fortifies diets for weanling pigs at a rate similar to this (BASF, 1997). However, recently Stahly et al. (1996) observed increased growth performance of high-health and high lean growth potential pigs when fed up to 6 times NRC

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estimates for the major B-vitamins. Application of these results, however, is limited because several vitamins were added at increasing concentrations. Therefore, it is impossible to determine if the response is due to one specific vitamin or a combination of several vitamins. Another factor that may be biasing the response to vitamin supplementation is that pigs were fed a vitamin deficient diet before the experiment began. However, a study recently conducted by a vitamin manufacturer reported similar improvement in growth performance with vitamin supplementation up to 16 times NRC (1998) requirement estimates (Coelho et al., 2001). Additional research is needed in this area to confirm pig responses to these “supra-nutritional” concentrations. Currently, there is justification for vitamin supplementation at 3 to 4 times NRC (1998) requirements under field conditions. There is also data suggesting that some vitamins previously considered not necessary to add to weanling pig diets, such as pyridoxine (Woodworth et al., 2000), vitamin C (de Rodas et al., 1998) and carnitine (Real et al. 2001) may increase growth performance of weanling pigs. The response to pyridoxine and vitamin C appears to be greatest initially after weaning. The response to carnitine appears greatest from 2 to 4 weeks after weaning. Economics dictate that the decision to add pyridoxine to diets immediately after weaning is easier than the decision to add either vitamin C or carnitine. Further research is needed with vitamin C and carnitine before definitive conclusions can be made. 11.4.5

Minerals

Weaner pig diets should be supplemented with the macro minerals calcium, phosphorus, sodium and chloride and the trace minerals copper, iodine, iron, manganese, selenium, and zinc. As for the macro minerals, because of their relative abundance and availability in milk and other specialty protein sources, providing a wide margin of safety above the pig’s actual requirements is neither difficult nor costly. Because of the importance of bone growth early in the pig’s life, calcium and available phosphorus concentrations should range from 0.90 to 0.75 and 0.48 to 0.40 from weaning to 20 kg, respectively. The other macro minerals that appear to improve pig growth performance are sodium and chloride (Mahan et al., 1996). Despite the relatively high concentrations of sodium and chloride in dried whey and spray-dried animal plasma, studies show improved growth performance when salt is supplemented to diets containing high levels of these ingredients (Mahan et al., 1996). The sodium and chloride requirement of weaner pigs initially after weaning is clearly higher than recommendations of NRC (1998). Copper and zinc are the two trace minerals that have received the most attention due to their potential as growth promoters. The basal requirement for copper and zinc is approximately 10 and 100 ppm, respectively. Data on the addition of high

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levels of copper (100 to 250 ppm) to starter diets as a growth promoter was summarized well by NRC (1998). In recent years, numerous experiments have demonstrated that adding high levels of zinc oxide (3,000 ppm) to nursery diets improves pig performance (Hahn and Baker, 1993; Carlson et al., 1999; Woodworth et al., 1999a,b,d) immediately after weaning and to a greater extent than copper sulfate (Smith et al., 1997). In a series of experiments, Woodworth, et al. (1999a) confirmed earlier work of Hahn and Baker (1993) and McCully et al. (1995) showing that the oxide form of zinc was more effective in producing the growth-promotion response than zinc sulfate or a zinc amino acid complex. Woodworth et al. (1999b) also discovered that the source of zinc oxide, although important for bioavailability (Edwards and Baker, 1999), did not influence the pharmacologic growth-promotion response. Most commercial diets now use 2,000 to 3,000 ppm of zinc oxide as a growth promoter immediately after weaning and 100 to 250 ppm of copper sulfate, or no supplemental copper or zinc in the late nursery diets. 11.4.6

Post-weaning diarrhea and zinc oxide.

Post weaning diarrhea associated with hemolytic Escherichi-coli is a common problem in early wean pigs. Supplementing nursery diets with 3000 ppm zinc from zinc oxide (ZnO) post-weaning has also been observed to have beneficial effects in helping control post-weaning E. coli associated challenges under field conditions (Holm and Poulsen, 1996, Tokach et al., 2000). A case study by Tokach et al. (2000) clearly illustrated the clinical and economic impact ZnO can have in controlling post-weaning diarrhea. Piglets were being weaned from a 1400-sow unit and sent to three different producers in loads of 600 pigs per week. Production records indicated poorer performance and a greater problem with E. coli associated diarrhea in one herd compared to pigs from the other two [394 g vs. 436 g of average daily gain (ADG) and 8.0% vs. 0.96% mortality for the case herd and other two herds, respectively]. No environment and management differences on the sow farm of origin were found to explain the performance differences in these three groups of pigs. When diet formulations were reviewed, it was discovered that the first two diets fed to the weaned pigs in the case herd contained 612 ppm zinc from ZnO, instead of the specified 3,000 ppm. Comparable diets for the pigs in the other two locations contained 3,000 ppm zinc. The diet formulation error was corrected, and performance of the next groups of pigs improved. This case study demonstrated the value of closeout records in determining the economic impact of the diet formulation error, which was calculated to be a loss of $3.13 to $5.88 per weaned pig. In a challenge study, Jensen-Waern et al. (1998) found that adding 2500 ppm of zinc from ZnO to the diet prevented postweaning diarrhea without affecting the numbers of E. coli excreted in the feces. In another challenge study (Mores et al.,

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1998), high concentrations of zinc from any of four ZnO sources reduced the occurrence of E. coli diarrhea without affecting fecal shedding of the E. coli. In these experiments, a high prevalence of diarrhea occurred in pigs that did not receive high concentrations of ZnO when challenged. Another recent study demonstrated that pigs supplemented with ZnO at 3,000 ppm had a reduced translocation of bacteria to the ileal-mesenteric lymph node (Huang et al., 1999). The potential mechanism for this finding, as well as the other beneficial effects demonstrated above, is not clearly understood. Zinc has been demonstrated to have an effect on cells undergoing rapid turnover, as it is needed for DNA and protein synthesis. Zinc also seems to play a role in stabilizing cell membranes and modifying membrane functions (Bray and Bettger, 1990). Zinc is also a powerful anti-inflammatory agent and the gut often suffers an non-specific inflammatory response after weaning. Therefore, zinc’s beneficial impact may be in part due to a direct supportive or protective role of intestinal epithelial cells (Huang et al., 1999). Managing post-weaning E. coli challenges is increasingly becoming more complex. These challenges need an ongoing effort for improved prevention or intervention techniques. Utilizing excess supplemental zinc early in the nursery phase is one option available to help minimize these challenges and promote growth. The environmental concerns associated with feeding zinc are significant. This concern reemphasizes the desire to restrict the 3,000 ppm ZnO inclusion in the first two weeks after weaning when feed intake is the lowest and the benefit the greatest. 11.4.7

Organic trace minerals

The chemical form of trace minerals also has received considerable attention in recent years. Organic sources of copper appear to provide growth promotion similar to copper sulfate (Coffey et al., 1994; Apgar and Kornegay, 1996). Numerous organic forms of zinc (zinc-lysine, zinc-methionine, zinc-amino acid complexes) also are available for use in swine diets. However, supplementing diets with the organic forms of zinc does not consistently improve pig performance to the same extent as growth promoting levels of zinc oxide (Hahn and Baker, 1993; Woodworth et al., 1999a,c). Environmental issues with trace mineral accumulation in swine waste will force continued evaluation of different mineral sources for pigs in an attempt to reduce zinc and copper excretion.

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11.5

Selection of ingredients for the weaned pig

11.5.1

Energy sources

11.5.1.1 Lactose Research with high quality lactose sources has demonstrated linear improvements in pig performance as levels of lactose increase in the diet, even through levels as high as 45% (Mahan, 1990). Most diets used in commercial application fed immediately after weaning contain more modest and economical levels of 15 to 20% lactose. Lactose additions to the diet continue to improve growth performance until approximately 21 to 28 days after weaning, or 10 to 13 kg (Crow et al., 1995). After this time, lactose can be replaced with other, more economical carbohydrate sources, such as cereal grains. A high quality, edible-grade, dried whey is the predominant lactose source used in starter diets. Recent research with lactose has focused on evaluating less expensive lactose sources to replace dried whey in the diet. Several lactose sources have emerged including L-lactose, deproteinized whey, and whey permeates. The value of these sources was questionable in the past; however, processors have improved their knowledge of the drying conditions required to maintain a high quality product. Additionally, the quantity of these products has increased due to the desire for whey proteins in human food products. Nutritionists’ understanding of the use of whey replacements also has improved. Initial tests attempted to replace dried whey on a lactose basis without substituting another high quality protein source for the whey protein removed from the diet when substituting a lactose product for dried whey. Recent trials have proven that other lactose sources can replace whey in the diet (Nessmith et al., 1997; Touchette et al., 1995) with two stipulations: 1) the spray drying must be well controlled, and 2) a high quality protein source must be used to replace the whey protein fraction. Recently, other non-lactose carbohydrates have been touted as replacements for lactose or dried whey. These carbohydrates include dextrose, sucrose, or byproducts of candy manufacturers. The research generally shows that these sources can replace a portion of the whey in the diet, but they should not replace the entire lactose fraction (Stephas and Miller, 1998). Incremental replacements of whey or high quality proteins, such as animal plasma, must be viewed with some skepticism. If the protein or carbohydrate source cannot replace whey or plasma directly, care must be taken with an incremental replacement approach. As an example, trials have shown that reducing the lactose level from 15 to 10% will not reduce performance significantly (Owen et al., 1993). Similarly, reducing the plasma level from 7 to 5% may not demonstrate a

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significant response in a given experiment. However, if sufficient replication was conducted or the plasma and lactose levels were reduced at the same time, significant differences will often be found. Research results must be viewed with care when evaluating ingredient replacements. These trials can be easily designed to find the desired and potentially biased results. 11.5.1.2 Fat The original high nutrient density diets for weanling pigs contained 8 to 10% supplemental fat to provide levels similar to that of sows milk (Nelssen, 1986). Since the introduction of these diets, numerous trials have been conducted to examine the young pig’s ability to utilize fat. Nelssen (1990) explained that fat was added to the diets for two reasons: 1) to increase dietary energy density, and 2) to improve pellet quality and efficiency in the pellet mill. However, early research examining the response to supplemental fat in diets containing high levels of milk products failed to consider the importance of fat in maintaining pellet quality. Diets containing high levels of milk products without supplemental fat are extremely difficult to pellet with low passage rate through the pellet mill. The diet will, thus, have a longer residence time in the die and may be scorched, lowering lysine availability and milk product quality. Adding high levels of fat to the diet prevents the scorching. Thus, a response that was attributed to added fat in early research may have been due to an improvement in pellet quality rather than a response to fat per se. When carefully monitoring pellet quality, researchers (Li et al., 1989; Tokach et al., 1995) have failed to show an improvement in performance when adding up to 10% fat to weaner diets fed immediately after weaning. However, the “pellet quality factor” must be considered when adding fat to a diet containing high levels of milk products. The ideal fat level for the pelleting process depends on the level of milk products, thickness of the die, and skill of the pellet mill operator (Leaver, 1988). Levels of 3 to 6% supplemental fat may be warranted in diets containing high levels of milk products to improve pelleting efficiency; however, higher levels of fat addition to the diet appear unjustified. The reason that fat utilization is limited in the pig before 35 d of age is not well understood. The lower digestibility of fat by weanling pigs during the initial period after weaning may be part of the problem (Leibbrandt et al., 1975; Cera et al., 1988a,b). The lower digestibility may be due to myriad of reasons. Dietary fat causes the sloughing of intestinal villi cells impairing digestion immediately after weaning (Cera et al., 1988a). The young pig also has decreased levels of fatty acid binding protein during the first 2 wk after weaning (Reinhart et al., 1990). Furthermore, enzyme secretion and(or) activity may be limited immediately after weaning at an early age. Several researchers (Scherer et al., 1973; Corring et al., 1978;

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Lindemann et al., 1986; Cera et al., 1990) have reported that lipase activity and secretion in pancreatic tissue increased with increasing age postweaning. Quantities of calcium and copper in the diet also have been implicated as influencing fat digestibility. High levels of calcium in the small intestine may depress fat absorption by increasing the formation of fatty acid soaps (Atteh and Leeson, 1983). Conversely, Dove and Haydon (1992) and Dove (1993) demonstrated high levels of copper sulfate in the diet improve fat utilization in the young pig. The lower apparent digestibility may not fully explain the young pig’s poorer utilization of energy from fat than that of older pigs. Part of the problem with fat utilization also appears to occur at the tissue level. Cera et al. (1988c) found that supplemental fat decreased nitrogen retention and increased serum urea concentration during the initial 2 wk after weaning. Supplemental fat also increased carcass fat (Endres et al., 1988) and decreased protein gain (Leibbrandt et al., 1975) during this period. These results indicate that the young pig digests and absorbs a large portion of the dietary fat and stores it as carcass fat. However, during the initial weeks after weaning, the pig may not be able to efficiently catabolize the fat for use as energy. Thus, an energy deficit may occur requiring the pig to utilize dietary protein as an energy source. This would explain the decreased nitrogen retention and increased serum urea concentration found by Cera et al. (1988c). If a limitation in fat metabolism exists, further research is needed to determine whether the limitation occurs in lipolysis, transport, or beta-oxidation. Research in the human nutrition field suggests babies are born with limited ability to synthesize the carnitine-acyl transferase enzyme needed to transport the fatty acid into the mitochondria for beta-oxidation. Adding L-carnitine to diets immediately after weaning has improved pig performance in some experiments (Rincker et al., 2001); however, it does not appear to solve the entire problem associated with fat utilization. With increasing age after weaning, the ability of the pig to efficiently utilize fat improves. Increasing the energy density of the diet by adding fat consistently improves feed efficiency and growth rate for pigs greater than 42 days of age. After this age, dietary fat decisions should be based on economics, as the ability of the pigs to utilize the fat is not a concern. Considerable research has been conducted in recent years to determine the appropriate fat source for the early-weaned pig. Cera et al. (1988b) found corn oil to be more digestible than lard or tallow, but differences among fat sources narrowed from week 1 to 4 after weaning. Tokach et al. (1995) found no difference in performance when comparing corn oil and soybean oil. Li et al. (1989) found that a combination of soybean oil and coconut oil was superior to diets containing soybean oil, choice white grease or a combination of coconut oil and choice white grease. However, the high cost of refined coconut oil usually limits its use in swine

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diets. Tallow and restaurant grease have consistently been found to be the least desirable fat sources for nursery diets. Whenever fat is added to the starter diet, a high quality, stabilized fat source must be used. Also, a constant ratio of nutrients to energy must be maintained when adding fat to the diet. The importance of fat in maintaining pellet quality in high milk, dry diet should not be underestimated. 11.5.1.3 Grain sources Several grain sources have been used successfully in diets immediately after weaning. In diets containing relatively high levels of specialty protein or lactose sources, corn can be substituted as the main cereal source with tapioca, sorghum, or rice (Rantanen et al., 1995a), oat groats (Mahan and Newton, 1993), whole oats, oat groats or oat flour (Rantanen et al., 1995b), naked oats (Landblom and Poland, 1998), potato starch (Dritz et al., 1994a; Kerr et al., 1998b) or wheat. In none of these trials, however, was performance improved by replacing corn with these alternative grain sources. In the later nursery stages, pigs respond as expected with grains containing higher energy concentrations providing improved pig performance. 11.5.2

Protein sources

11.5.2.1 Spray-dried animal plasma Although animal plasma is expensive, it is necessary to encourage maximum feed intake in the period immediately after weaning (Gatnau et al., 1991; Hansen et al., 1993; Kats et al., 1994c) with very young pigs. Increasing the level of animal plasma from 5 to 15% in the diet for SEW pigs results in a linear increase in pig performance (Dritz et al., 1994b). However, the greatest portion of the response is evident with the first 5% inclusion of plasma (Hansen et al. 1993). Thus, most nutritionists include plasma in the SEW diet at 5 to 7%, depending on price and other combinations of protein sources included in the diet. Plasma contains high levels of cysteine, but low methionine levels, making it necessary to formulate for methionine in addition to total sulfur amino acids. When comparing various plasma sources, solubility and bacterial levels should be considered. Higher solubility indicates less heat denaturing during the spray-drying process. Lower bacterial levels are an indication of quality of the raw material. Recently, DeRouchey et al. (2001a,b) found that lowering the bacterial levels in plasma with irradiation or by applying a formaldehyde-based product improved pig performance. The main response to adding plasma to the diet is an increase in feed intake. Numerous researchers have tried to find the mechanism for this feed intake response. Owen et al. (1995c) and Peirce et al. (1995) demonstrated that the immunoglobulin

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fraction of plasma appears to provide the greatest benefit in feed intake, as compared to the albumin fraction or the remaining portions of plasma. Plasma normally contains about 15 to 18% immunoglobulin. Because of the feed intake response, plasma rapidly became the dominant protein source in starter pig diets. Due to the high cost of plasma, research quickly shifted to experiments to determine the optimal level of plasma in the diet and whether other protein sources or combinations of protein and carbohydrate sources could replace a portion of the plasma. Other protein sources, such as high quality fish meal, spray-dried blood meal, and spray-dried whole egg, have been able to replace a portion of the plasma in the starter diet; however, none of these protein sources is a viable replacement for the entire plasma fraction of the diet. One other peculiarity to plasma is the carryover effect after removing pigs from a diet containing a high level of plasma. Many trials have fed high levels of plasma (5 to 10%) for 1 to 2 weeks after weaning. After feeding these high levels, the pigs were switched to diets without plasma. When this is done, most of the growth advantage is lost within the next week or two. To overcome this problem, we advocate a step-wise approach to removing plasma from the diet. If the first diet fed contains 5% plasma or greater, a second diet containing 1 to 2.5% plasma should be fed before removing all the plasma from the diet (Dritz et al., 1996b; Bergstrom et al., 1997). Because plasma is expensive, this strategy results in considerable cost savings compared to maintaining the high level in the diet. Reducing the plasma level with diet changes after weaning is an example of managing the inclusion rate of an expensive ingredient to match the biology of the pig to derive maximum economic benefit. Because the response to plasma is due to an increase in feed intake, there also is an interaction with the health level of the pigs on the response to plasma. If the pigs are very high health and, thus, have a high level of feed intake without plasma, plasma does not provide as much benefit as in a low health situation or more challenging environment (Coffey and Cromwell, 1995). In some European countries, animal proteins (other than milk products) can not be fed to pigs due to concerns with Bovine Spongiform Encephalitis (BSE). Thus, it is not legal to use spray-dried plasma in swine diets in these countries. Because of this ban, diets must be formulated using many of the alternative protein sources listed below. 11.5.2.2 Whey protein concentrate Whey protein concentrate is a very high quality protein source. Recent research (Grinstead et al., 2000) indicate that high protein (78%) whey protein concentrate

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may be one of the few protein sources that consistently provides pig performance similar to animal plasma. High protein, whey protein concentrate has a similar amino acid profile to plasma. Grinstead et al. (2000) tested this product at levels of 3 to 7% of the diet and found excellent similar ADG and feed efficiency in comparison to plasma. Unfortunately, access to high protein, whey protein concentrate is limited due to the high demand for use in non-fat foods by the human food industry. Price may limit the application in the United States, but its economic competitiveness should be watched closely around the world. 11.5.2.3 High quality fish meal Several fish meal sources are available for starter diets. The highest quality fish meals from various United States (Select Menhaden Fishmeal), European (Low temperature Norwegian fish meals), and Chilean (low amine products) sources all have proven to be excellent protein sources for young pigs. Researchers have found little difference in feeding value between these high quality sources. However, none of these sources can directly replace plasma in the starter diet. High quality fish meal is used at 3 to 6% in most starter diets to increase the amino acid content and increase feed intake without dramatically increasing cost. When a high quality fish meal is available and economical, weaner diets can contain as much as 12% Select Menhaden Fishmeal without compromising performance (Stoner et al., 1990). Similar to other protein sources that rely on high quality raw materials and correct drying, the quality of fish meal can deteriorate quickly when not handled properly. 11.5.2.4 Dried skim milk In the past, most diets fed immediately after weaning routinely contained 10 to 25% dried skim milk. The use of animal plasma quickly eliminated skim milk as a protein source in most diets. Skim milk has two problems: 1) expense, and 2) the casein fraction decreases feed intake. Dritz et al. (1994c) found no benefit to having skim milk in the diet, when the diet contains adequate plasma and lactose. If fact, feed intake improved when skim milk was removed from the diet. Dried skim milk still is being used in weaner diets in some instances because pigs look cleaner and drier when fed a diet containing skim milk. The problem is that they do not grow faster. However, when marketing to unsophisticated producers that rely on their eyes instead of performance data to make decisions, ingredients like skim milk and oat groat products increase in value. Because of the high biological value, pigs fed diets containing dried skim milk often have better feed efficiency than pigs fed diets containing plasma; however, feed intake and average daily gain will be lower. Nevertheless, in addition to being more expensive than other protein sources, our findings indicate that the skim milk can be replaced with lower cost protein sources without sacrificing performance.

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11.5.2.5 Spray-dried blood meal or red blood cells Spray-dried blood cells are a byproduct of plasma manufacturing. Spray-dried blood meal has the advantage of not having the plasma removed during processing. Spraydried blood meal and cells have high protein contents (85 to 95%) and, thus, can be used in the weaner diets in small quantities as concentrated amino acid sources. When fed to pigs weighing 5 to 15 kg, blood products increased feed intake and growth rate (Hansen et al., 1993; Kats et al., 1994b). These products need to be used with caution with pigs weighing less than 5 kg. Levels greater than 2% can depress feed intake. Blood meal or blood cells should not be used at levels higher than 3% in most diets due to the isoleucine deficiency that occurs in most practical diets after this point. Spray-dried blood products also are deficient in methionine. Methionine becomes the limiting amino acid when greater than approximately 5% spray-dried blood products (plasma and/or blood cells or meal) are included in the diet (Kats et al., 1994b). It is critical that synthetic methionine is added to the weaner diets containing plasma and other blood products for optimal performance (Owen et al., 1995b). Processing method for the spray-dried blood meal also appears to be critical to maintain the quality of protein sources. Kats et al. (1994b) demonstrated that pigs fed spray-dried blood meal performed better than pigs fed flash-dried blood meal. 11.5.2.6 Dried porcine solubles Dried porcine solubles is a product that originates from the processing of porcine mucosa and small intestines. Porcine solubles are available in various concentrations with protein content ranging from 30 to 55%. These products have a high ash content (approximately 32%). The fiber content varies whether soyhulls are added to the product (18%) as a carrier in the drying process or not. The product is extremely high in sodium (3.5%) and iron (500 ppm). The amino acid profile is good, but the lysine level is relatively low (2.0 to 3.8% depending on the protein content). The difficulty with using porcine solubles in research trials is determining the method of substitution for other ingredients. The first research compared porcine solubles to dried whey. Cost and nutrient profile led many researchers to question whether this was a worthwhile comparison. Subsequent research attempting to compare porcine solubles to plasma has had difficulty comparing them directly as protein sources due to the large difference in protein and amino acid content. Because porcine solubles has improved feed intake when being fed and has improved subsequent intake after they have been removed from the diet, this protein source may be a viable option for weaner pig diets (Zimmerman et al., 1997), however, the database to determine optimum usage is still sparse.

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11.5.2.7 Soybean meal Soybean protein in the form of soybean meal has long been the predominant protein source in swine diets. Unfortunately, soybeans contain many anti-nutritional factors such as trypsin inhibitors, lectins, and complex carbohydrates and proteins that impair the pigs’ ability to utilize them. Heat treatment of the soybeans in the process of making soybean meal removes much of the trypsin inhibitor; however, complex proteins and carbohydrates are not removed. Complex proteins in soybean meal have been suggested as the cause of a transient hypersensitivity response in the earlyweaned pig. Before weaning, pigs can consume soybean proteins by eating small quantities of sow feed or creep feed and become exposed or “sensitized” to the soy proteins. Bourne (1984) explains that prior to building up a tolerance to an antigen such as those in soybean proteins, the pig goes through a period of heightened responsiveness. Feeding the soybean protein during this period can result in damaging hypersensitivity responses, such as increased crypt cell division and the appearance of immature enterocytes on the villus, resulting in reduced digestive and absorptive capacity and an increased susceptibility to enterotoxins. This response appeared to be caused by antigenic proteins present in soybeans, such as glycinin and beta-conglycinin. The transient hypersensitivity is measured experimentally as higher immunoglobulin G titers to soybean protein resulting from the pig’s attempt to mount an immune response against the antigenic proteins. However, the end result is that digestive abnormalities, including disorders in digestive movement and inflammatory responses in the intestinal mucosa, can occur. Villi are sloughed from the small intestinal mucosa and absorptive capabilities are reduced. The source and percentage of soy protein in diets for early-weaned pigs have been controversial subjects among swine nutritionists because of the implication that soybean protein causes an immune-mediated pathology leading to decreased growth performance (Li et al., 1990). Engle (1994) reviewed the role of soybean meal in causing immune-mediated delayed-type hypersensitivity (DTH) allergic reaction. Some nutritionists believe soybean meal should not be included in the first diet after weaning to prevent the DTH allergic reaction to the protein antigens it contains. Most researchers agree that the ideal time to establish oral immune tolerance to soy protein antigens is before weaning (Engle, 1994). However, with early weaning ages, it is difficult for the pigs to consume enough soybean protein during the lactation period to establish oral tolerance. Nutritionists that advocate not including soybean meal in the first diet postweaning typically will replace it with a further refined soy protein, such as soy protein concentrate, isolated soy protein, or extruded soy protein concentrate. If a refined soy product is used in the diet, several research trials have demonstrated an advantage to moist-extruded soy products compared to those that have not been moist-extruded (Friesen et al., 1993b).

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Other researchers and nutritionists take a different approach. They believe that exposing young pigs to increasing levels of soybean meal in each diet will allow them to overcome the hypersensitivity to soy protein more quickly, without causing a long-term reduction in performance. This approach also is substantially less expensive than delaying acclimation to soybean meal. Friesen et al. (1993a) indicated that delaying exposure to soybean meal until d 14 postweaning only delayed the effects of DTH. In fact, overall growth performance from d 0 to 35 postweaning was better for pigs exposed to soybean meal immediately postweaning than for pigs whose diet did not contain soybean meal until d 14 postweaning. Thus, formulations of diets for SEW pigs must consider the relationship with performance in subsequent phases. Pigs are born with an immature immune system. Over the first few weeks of life, the immune system progressively develops a greater ability to distinguish between native and foreign proteins. If exposed to foreign proteins, such as soy protein, at a very young age, the immune system will be primed to recognize them as native. The early exposure permits inclusion of soybean meal at higher levels in subsequent diets without reducing growth performance. The appropriate level and source of soy protein for the SEW pig are not well researched. We recommend a low level (10 to 15%) of soybean meal in the initial diet after weaning as a means of acclimating the young pig to soy protein (Dritz et al., 1994c, 1996b). Research of Friesen et al. (1993a) and Dritz et al. (1994c) has indicated that early exposure to soy protein may be beneficial. 11.5.2.8 Further processed soy products Several experiments have been conducted to determine if further processing of soybean products would improve the value of soy proteins for the young pig. Several soy products are available including soybean meal (44 or 48% protein), soy flour (50% protein), soy protein concentrate (70% protein) or isolated soy protein (90% protein). Research indicates that these products are only superior to soybean meal if they have been moist extruded (Li et al. 1990a,b). These experiments revealed that further processing of soy proteins decreases transient hypersensitivity and increases villus height, nutrient digestibility, and growth performance as compared to pigs fed diets containing high levels of soybean meal. However, pigs fed milkbased diets still had longer villi and higher nutrient digestibility than pigs fed the further processed soy proteins. This research reveals that processing method significantly affects the utilization of soy proteins by nursery pigs. Further research (Friesen et al., 1993b) has suggested that moist extrusion of soybean meal greatly improves its nutritive value for weanling pigs. In fact, pigs fed diets containing moist extruded soybean meal performed as well as pigs fed diets containing moist extruded soy protein concentrate. Moist extrusion appears to be

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an effective means of improving the value of less expensive soy protein products. Similar advantages of extrusion processing have been seen in a subsequent trial comparing pigs fed an all-milk protein based diet to those fed either soybean meal, moist extruded soybean meal, or dry extruded soybean meal. If further processed soy products such as soy protein concentrate or isolated soy protein are used in weaner diets, they should be extruded prior to use. Research consistently demonstrates that the non-extruded products are similar to soybean meal in feeding value at a much higher cost. However, once extruded, products like extruded soy protein concentrate are excellent protein sources to use in combination with other proteins in the starter pig diet. If a nutritionist has a goal of not using any soybean meal in the diets immediately after weaning, extruded soy protein concentrate as an excellent protein source. 11.5.2.9 Potato protein Kerr et al. (1998a) conducted a series of trials with various potato proteins. These refined products contain approximately 85% protein. The major problem with some of these products is the level of alkaloids. Further processed potato proteins that have the alkaloids removed appear to be excellent protein sources. Although potato protein does not appear to be able to totally replace plasma in the diet, it may be used in combination with other protein sources in the starter diet. Economics limit their use in the United States; however, they are more appropriate in economic situations presented in other parts of the world. Potato protein is a protein source to watch for further improvement and utilization in the future. The greatest limitation to use is the cost of removing alkaloids from the product. 11.5.2.10 Spray-dried egg protein The high immunoglobulin content of whole eggs makes them a logical protein source to use as a partial replacement to plasma. Egg products still hold promise in starter diets, but there are still questions about their use. Trials to date demonstrate inconsistent responses (Nessmith et al., 1995). There are several potential reasons for the difference in responses in various trials, including: 1) the purity of the raw material, 2) the level of egg whites and yolk in the product, 3) the spray drying temperature, 4) post-processing handling of the product, or 5) the avidin content all of which could limit performance. Similar to potato protein, egg products hold promise as a protein source for starter pigs, but further work must be done to determine the required quality parameters and changes in diet formulation to fully utilize the eggs. The relatively low price of spray dried eggs has led to renewed interest in egg products as a protein source for young pigs.

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11.5.2.11 Spray-dried wheat gluten Similar to egg protein, spray-dried wheat gluten is an interesting protein source. Initial trials are quite variable in results (Richert et al., 1993). Spray-dried wheat gluten is a high protein, extremely lysine-deficient protein source. When used in the diet, high levels of synthetic lysine can be added before any other amino acids will be limiting. Thus, wheat gluten can serve in combination with other high lysine protein sources to improve the amino acid ratio of the diet. A unique result of the wheat gluten trials appears to be an improvement in subsequent performance after pigs have been fed a diet containing wheat gluten. Similar to most dried products, processing conditions are extremely important in determining the quality of the final product. Wheat gluten must be spray dried to maintain protein quality (Richert et al., 1993). Wheat gluten is another protein source that has not been utilized to the full extent of possibilities due to our lack of understanding of the reasons that the responses have not been consistent in various experiments. 11.5.3

Non-nutritive Feed additives (eg., antibiotics, enzymes, organic acids, etc.)

The NRC (1998) provided excellent background information on many of the nonnutritive feed additives that have been used in weaner diets including antimicrobial agents, microbial supplements, oligosaccharides, enzymes, acidifiers, flavors, and pellet binders. Guidelines for selecting growth-promoting antimicrobials were reviewed by Straw (1994), who also established guidelines for determining growth-promoting antibiotic usage in swine herds. Growth promoting antimicrobials have a greater response in young versus older pigs, in “dirty” versus “clean” environments, and in low-health versus high-health animals (NRC, 1998). Recent evidence indicates that the growth responses to including growth promoting antimicrobials in swine diets are much lower in modern multi-site swine production systems compared to previous summaries (Dritz et al., 2002). Also, there is increased concern that agricultural use of antimicrobials can lead to transmission of resistant pathogens to humans (Witte, 1998). Without a doubt, development of resistance is reduced in the face of less selection pressure from lower usage of antimicrobials (Levy, 1998; Dunlop et al., 1998). Therefore, we advocate implementation of production practices that improve health status and decrease reliance on continuous use of feed antimicrobials. Although microbial supplements or probiotics have been reported to improve performance under some field conditions, most controlled experiments have failed to show consistent, beneficial responses (NRC, 1998). Oligosaccharides, such as fructooligosaccharide and monooligosaccharide, also have been reported to improve pig performance in some experiments. More research is needed to determine the conditions (diet, environment, pathogen load, etc) necessary to

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demonstrate a consistent benefit to including oligosaccharides in the diet. Other additives include various plant extracts and spices (Turner et al., 2001). Many of these additives are being advocated as replacements for antimicrobials. However, the supporting data for their usage is limited and inconsistent. Therefore, we believe implementation of sound production practices such as improved hygiene is a more cost effective investment than many of these types of additives. Phytase is an example of an effective enzyme that can be beneficial for the swine industry. Adding phytase to the diet improves the utilization of phytate phosphorus and decreases phosphorus excretion into the environment. Unfortunately, many of the other enzymes on the market, including proteases, cellulases and hemicellulases, have not shown the same consistency of response. As reviewed by Gabert and Sauer (1994), supplementing weaner diets with organic acids has been shown to improve pig performance. The response is greater with simple diet formulations than with more complex diets (Giesting and Easter, 1985). Inorganic acids, phosphoric or propionic acid, also have been shown to improve pig performance during the first couple of weeks after weaning (Bergstrom et al., 1995). The response to acidification of the diet declines rapidly as the pigs become older after weaning. Flavors are often added to swine diets in an attempt to improve palatability and increase feed intake. When given a choice, pigs will consume more of a diet containing a flavor; however, when pigs are not given a choice, most research shows little benefit to flavors (NRC, 1998). Pellet binders are often used to improve pellet quality of nursery diets. Because high levels of milk products are often used in the first couple of diets after weaning, pellet binders should not be required to make a high quality pellet. Pellet binders may have more use in the later nursery stages because diet formulas in this period make the diet more difficult to pellet. Unless needed for improved pellet quality, non-nutritive binders should not be routinely added to swine diets.

11.6

Example of phase feeding program for early weaned pigs

11.6.1

SEW diet - weaning to 5 kg

Maximizing feed intake after weaning reduces stress and increases growth rate by decreasing the mobilization of lipid stores to provide energy for protein deposition (Whittemore et al., 1978). Consequently, the major objectives when formulating an SEW diet, in order of importance are to: 1) select ingredients that stimulate feed intake, 2) provide a substantial amount of highly-available amino acids in the proper proportions, and 3) prepare pigs to utilize less expensive diets in subsequent phases. The high amino acid fortification of the SEW diet necessitates multiple protein sources to meet the young pig’s nutritional needs (Table 11.4). Several of the

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Table 11.4. Recommended sequences and composition of SEW nutritional programs. SEW Diet for pigs weighing less than 5 kg Grain-based 1.6 to 1.7% Lysine 0.44 to 0.47% Methionine 18 to 25% Lactose equivalent 5 to 7% Spray-dried animal plasma 10 to 15% Soybean meal 3 to 6% Added fat 0 to 2% Spray-dried blood meal 3 to 7.5% High quality fish meal 3,000 ppm Zinc oxide Pelleted

Transition Diet for pigs weighing 5 to 7 kg Grain-soybean meal-based 1.5 to 1.6% Lysine 0.38 to 0.43 Methionine 15 to 20% Lactose equivalent 2 to 3% Spray-dried porcine plasma 2 to 3% Spray-dried blood meal and (or) Select menhaden fish meal 3 to 5% Added fat 3,000 ppm Zinc oxide Pellet or meal form

Phase 2 for pigs weighing 7 to 11 kg Grain-soybean meal-based 1.30 to 1.40% Lysine .36 to .38% Methionine 6 to 8 % Lactose equivalent 2 to 3% Spray-dried blood meal or 3 to 5% High quality fish meal 0 to 3% Added fat 2,000 ppm Zinc oxide Pellet or meal form

Phase 3 for pigs weighing 11 to 25 kg Grain-soybean meal-based 1.15 to 1.30% Lysine .32 to .36% Methionine No added specialty ingredients 0 to 6% Added fat 100 to 250 ppm Copper sulfate Pellet or meal form

following protein sources often are used in combination in the SEW diet to meet the amino acid requirements and to stimulate feed intake: spray-dried plasma protein, fish meal, skim milk, whey-protein concentrate, spray-dried egg protein, spray-dried blood meal, soybean meal, and further processed soy products. At the present time, the only protein source considered somewhat essential in this diet is spray-dried animal plasma because of its influence on feed intake. The SEW diet often contains 5 to 7% plasma. Other protein sources used in the SEW diet will depend on the availability and pricing in a particular location in relation to growth performance benefits. The controversy surrounding the level of soybean protein to include in this diet is discussed in the protein source section. We recommend adding 10 to 15% soybean meal to the SEW diet in order to prepare the pig to handle much higher levels of soybean meal in the next diets. The high cost of plasma and detrimental effects of high levels of soybean meal limit their inclusion in the SEW diet. Thus, other protein sources are required to increase the amino acid content of the diet. Spray-dried blood meal (up to 2.5%) and/or a high quality fish meal (up to 7.5%) are often the most economical protein sources other than soybean

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meal that can increase feed intake immediately after weaning. Thus, they are often used in SEW diets. The SEW diet should contain 18 to 25% lactose. High levels of lactose are beneficial for stimulating feed intake and increasing growth performance; however, care must be taken during processing because high levels of milk products increase the difficulty of pelleting the diet (Leaver, 1988). The appropriate added fat level in the SEW diet depends on the level of milk products and the skill of the pellet mill operator (Leaver, 1988). Typically, 3 to 6 % fat is added to the diet to lubricate the pellet die. Diets containing plasma and high levels of milk products should be conditioned at less than 77° C during pelleting (Steidinger et al., 2000). Even though the SEW diet contains a high level of lactose, the grain source serves as an important energy source. Further processed oat products (oat groats, oat flour) improve diet appearance and can improve stool consistency and pig appearance. However, research showed no differences in pig performance with diets containing oat flour or corn ground to 600 microns (Dritz et al., 1994a). Additionally, refined oat products are often 2 to 3 times the expense of other grain sources (corn, sorghum, wheat, etc) and, thus, their inclusion in the diet must be carefully considered. Growth-promoting levels of antibiotics normally are included in the SEW diet. As discussed earlier in this chapter, research has demonstrated that ZnO at 3,000 ppm is a better growth promotant for early-weaned pigs than copper sulfate. Addition of high levels of ZnO is not legal in all countries; however, it provides an excellent growth promotion response when available for commercial use. Other potential additives in the SEW diet include dietary acids, such as propionic, fumaric, or other acids at low levels. Research by Bergstrom et al. (1995) indicated that a buffered propionic acid can improve growth performance and be a cost effective addition to the SEW diet for pigs weaned at 14 d of age. 11.6.2

Transition diet - 5 to 7 kg

The transition diet is a natural extension of the SEW diet and contains many of the same ingredients. However, feed intake increases rapidly in high-health-status pigs that are free from immune challenge. Minimizing immune challenge limits cytokine production, which leads to increased feed intake (Klasing, 1988; Williams et al., 1997a). Consequently, the primary objectives when formulating a transition diet are to provide a substantial amount of highly available amino acids in the proper proportions and to prepare pigs to utilize less expensive diets in subsequent phases. Selecting ingredients that stimulate feed intake is still an important but secondary objective. The importance of maximizing growth performance and optimizing economic performance by using a transition diet between the first diet postweaning and the phase 2 diet was demonstrated by Dritz et al. (1996a).

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The main difference between a conventional phase 1 diet and the transition diet is the level of spray-dried animal plasma, which is added to the diet primarily to increase feed intake. Because pigs receiving the transition diet are adjusted to feed, the diet typically contains only 2 to 3% spray-dried plasma protein compared to 5 to 7% in the SEW diet. In addition, the response to adding spray-dried animal plasma in the transition diet has not been as consistent as the response in the SEW diet. In one experiment, pigs failed to exhibit increased growth performance when plasma protein and (or) select menhaden fish meal were added to diets containing 2.5% spray-dried blood meal and 20% edible-grade dried whey (Bergstrom et al., 1997). This experiment used pigs from a high-health-status herd and was conducted in a facility operated all in-all out by site. In a subsequent experiment by the same authors, growth performance of 5- to 7-kg pigs was improved by feeding a transition diet containing 2.5% spray-dried plasma protein, 2.5% spray-dried blood meal, and 20% edible-grade dried whey compared to a transition diet without spray-dried plasma protein. The major difference was that the second trial was conducted on a farm in which the nursery was operated on an all in-all out basis by room and multiple rooms were in the same nursery complex. Until further research is conducted, we support a standard recommendation of including 2.5% spray-dried plasma protein in the transition diet, but recognize that the level may need to be customized to a particular herd depending on health status. Spray-dried blood meal and (or) a high quality fish meal also are used commonly in the transition diet as major protein sources. However, as with the SEW diet, inclusion level and source of proteins will depend up the balance between quality and price. Because the pigs were acclimated to soybean meal while being fed the SEW diet, the transition diet can contain higher levels of soybean meal (20 to 25%) without risk of hypersensitivity. The addition of soybean meal also further prepares the pig to efficiently utilize the less expensive diets in the successive phases. The lactose level in the transition diet often is decreased compared to the SEW diet. However, it is still critical that the transition diet contain at least 15% lactose for optimal pig performance. A high quality fat source (3 to 6%) is added to the transition diet for the same reason as the SEW diet (improved pellet quality). As in the SEW diet, antibiotics, ZnO (3,000 ppm), and acidifiers should be maintained in the transition diet as growth promoters. 11.6.3

Phase 2 - 7 to 11 kg

By the time the pigs in an SEW system weigh 11 kg, they already will have consumed 3 to 5 kg of feed. With feed intake rapidly increasing in these high-health-status pigs, stimulating feed intake is less of a concern in this phase. Moreover, the major concern when formulating this diet is to provide high levels of amino acids to maximize protein deposition. The specialty products are needed only at minimal

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levels to maximize growth performance, minimize cost, and efficiently shift pigs to simple grain-protein source diets in the subsequent phases. Feeding behavior is well adjusted and, thus, lower cost, less complex diets can be fed. Therefore, in order to reduce total feed cost, that spray-dried plasma protein should not be included in this diet. The phase 2 diet is typically a grain-soybean meal-based diet with a high quality source of lactose and a small amount of a specialty protein source; common choices include spray-dried blood meal or high quality fish meal. Research has shown consistently that these two protein sources result in similar performance for the phase 2 diet (Kats et al., 1994b). Therefore, the choice of protein source will depend on economics. Other specialty protein sources may be used in this diet depending on economic considerations of a particular producer or location. Research has shown an interaction between the inclusions of high quality fish meal, such as select menhaden fish meal, and dried whey in the phase 2 diet (Stoner et al., 1990). Those researchers found that when 4% select menhaden fish meal and 10% dried whey were added to the phase 2 diet, pig growth performance was similar to that of pigs fed 20% dried whey and no fish meal. Other research indicated that, when 2.5% spray-dried blood meal was used, approximately 10% dried whey in the phase 2 diet resulted in the optimum balance between economics and pig growth performance (Dritz et al., 1993). Additional research indicated that edible-grade lactose is an acceptable substitute for dried whey in the phase 2 diet (Crow et al., 1995). Therefore, we recommend supplementing the phase 2 diet with edible-grade dried whey or another high quality lactose source. If an economical fat source is available, the phase 2 diet should contain 3 to 5% added fat. As with the SEW and transition diets, growth-promoting antibiotics and ZnO are added to the phase 2 diet. However, research indicated that a lower level (2,000 ppm) of ZnO results in optimum growth performance (Smith et al., 1999a). Many producers make the phase 2 diet on their farms and feed it in a meal form. Research has shown an approximately 14% improvement in feed efficiency by feeding this phase in pellet form (Stark et al., 1994). The improvement in feed efficiency will depend on diet formulation, pellet quality, and feeder adjustment. However, the advantage of improvement in feed efficiency must offset the disadvantage of the increased cost to obtain the diet in the pellet form. 11.6.4

Phase 3 - 11.5 to 23 kg

The strategic intent of the SEW, transition, and phase 2 diets using the various combinations of specialty protein and carbohydrate sources is to efficiently prepare the pig to use a low cost, simple phase 3 diet. Thus, the objective when

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formulating the phase 3 diet for SEW pigs is to provide a simple grain-protein source diet formulated to provide high levels of amino acids. The later are needed to maximize lean tissue deposition. With proper dietary transition in the previous phases, a simple grain, protein source diet can be fed by this stage. The phase 3 diet is the lowest cost diet in the SEW nursery-feeding program. However, because consumption of the phase 3 diet is the greatest (Table 11.5), it usually accounts for 50% of the total feed cost from weaning to 23 kg. Thus, cost of this diet is critical to minimize total feed cost while maximizing performance in the nursery. Specialty ingredients, such as spray-dried blood meal, fish meal or dried whey are cost prohibitive, because research has failed to indicate improved growth performance from feeding such ingredients in phase 3 (Kats et al., 1994a). The fat level of the diet will depend on the ability of the producer to economically purchase fat. Pigs will show improved average daily gain and feed efficiency with increasing levels of fat in the phase 3 diet. Thus, 3 to 6% added fat is a common recommendation based on economics. As with the SEW and transition diets, growth-promoting antibiotics are added to the phase 3 diet. Because there is no advantage in growth performance and high levels of excretion can occur, high levels of ZnO should not be fed during this phase. Many nutritionists add copper sulfate (125 to 250 ppm) to this diet as a growth promoter.

11.7

Importance of management in the success of the nutritional program

A successful nutritional program is not measured by projected cost of feed delivered to the barn. Properly designed diets and feed budget are not enough to ensure success. Several management factors are critical to the success of the feeding program. The two biggest keys in management of the feed program in the barn are a) proper management to encourage feed intake, and b) adjusting feeders to minimize feed wastage.

Table 11.5. Example feed budget (amount, kg, of each diet that should be fed per pig; Dritz et al., 1996b). Weaning Age and Initial Weight

Diet

Pig weight, kg

14 d 4 kg

SEW Transition Phase 2 Phase 3

< 5 kg 5 to 7 kg 7 to 11 kg 11 to 25 kg

0.9 2.3 6 23

288

21 d 5.9 kg

24 d 6.8 kg

0.4 0.9 6 23

--0.9 5 23

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Nutritional requirements of the weaned pig

11.7.1

Management to encourage feed intake

Numerous management procedures are critical to maximizing feed (energy) intake and improving performance in the nursery. The factors necessary to maximize feed intake include a warm draft-free environment and an overall herd health program and pig flow that minimizes exposure to antigens. Providing easily accessible drinking water fixtures and unlimited water supply is essential as there is a linear relationship between water intake and feed intake in weaner pigs (Brooks et al., 1984). An often overlooked but critical need, is a dedicated workforce that can identify the signs of a “starve” out pig (Table 11.6) and then gently “teach” the pig where and how to eat (Dritz et al., 1996b), with either mat or individual feeding. Some pigs simply don’t start eating readily after weaning. Teaching these “starve” out pigs to eat, rather than treating them with an antibiotic, will save more pigs. Lastly, one of the most important factors in maximizing feed intake is allowing ad libitum access to feed. Many times when pigs exhibit post-weaning diarrhea or loose stools, producers will begin to limit-feed pigs thinking that this will minimize the severity of the post weaning scours. However, failure to investigate causative agents like improper air temperature or ventilation, poor sanitation, or inappropriate ingredient selection or quality can lead to failure to solve the primary problem. Limit feeding in the nursery results in reduced nursery exit weights. This is demonstrated by the exit weight of nursery groups in a large production system (Figure 11.5). Exit weights typically averaged 18 to 22 kg when nursery managers limit fed pigs the initial week after weaning. However, when management switched to ad libitum feeding by always having feed present in the trough throughout the entire nursery phase (8 weeks), feed intake and exit weights increased dramatically.

Table 11.6. Conditions to Identify “Starve-out” Pigs. • • • • • •

Mental status - alert or depressed Body condition - normal or thin Abdominal shape - round or gaunt Skin - sleek appearance vs fuzzy Appetite -feeding at the feeder or huddled Signs of dehydration - normal or sunken eyes

11.7.2

Adjust feeders frequently to minimize feed wastage

Proper and frequent feeder adjustment is the key to excellent feed efficiency and low feed cost in the nursery. Proper feeder adjustment starts with the first additions of feed to the feeder. Regardless of whether the first diet after weaning is in bags or bulk, the feed gate in all feeders should be closed before the first pellets are placed

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850

32 Feed intake Exit wt, kg

Exit wt

24

650

ADFI, g

750

28

550

20 Management change

450

16 1

2

3

4

5

6

7

8

Grou p

Figure 11.5. Changes in nursery exit weight and feed intake as a result of switching from limited- to ad libitum nursery feed intake (Dritz, 2002).

in them. The feed gate then should be opened so that a small amount of feed if visible in the feed pan. Placing pelleted feed into an empty feeder with the agitation gate open will result in large amounts of feed filling the trough leading to feed wastage and difficulty in achieving the proper feeder adjustment. Although adequate amounts of feed must be present in the feeder at all times after weaning, too much feed present in the pan of the feeder also can decrease growth rate. In an attempt to stimulate feeding behavior, some producers place large amounts of the first diet in the feeding pan. Although the intention is correct, the outcome is negative. Energy deficiency can result from pigs “sorting” the diet and a buildup of fines in the feeding pan. These fines then lodge in the feed agitator mechanism, making it difficult for new feed to flow from the feeder. This problem can be corrected by managing the amount of feed flow in the pan to stimulate development of feeding behavior. Approximately 50% of the feeding pan should be visible in the first few days after weaning. As the pigs become more accustomed to the location of the feed and adjust feeding behavior, the amount of the feed in the feeding pan should be decreased rapidly to less than 25% coverage. Also, feed agitators need to be tested frequently to ensure that the buildup of fines does not prevent them from working freely.

References Apgar, G.A., and E.T. Kornegay, 1996. Mineral balance of finishing pigs fed copper sulfate or a copper lysine complex at growth promoting levels. Journal of Animal Science 74, 1594. Asche, G.L., A.J. Lewis, and E.R. Peo Jr, 1989a. Protein digestion in weanling pigs: effect of feeding regimen and endogenous protein secretion. J Nutr 119, 1083-1092. Asche, G.L., A.J. Lewis, and E.R. Peo Jr, 1989b. Protein digestion in weanling pigs: effect of dietary protein source. J Nutr 119, 1093-1099.

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Atteh, J.O. and S. Leeson, 1983. Effect of increasing dietary fat, calcium and phosphorus levels on performance and mineral metabolism of weaner pigs. Canadian Journal of Animal Science 63, 699. BASF, 1997. Vitamin supplementation rates for U. S. Commercial Poultry, Swine, and Dairy Cattle. BASF Keeping Current KC 9305. BASF Corporation, Mt. Olive, NJ. Bergstrom, J.R., J.L. Nelssen, M.D. Tokach, R.D. Goodband, S.S. Dritz, K.Q. Owen, and W.B. Nessmith Jr, 1997. Evaluation of spray-dried animal plasma and select menhaden fish meal in transition diets fed to pigs weaned at 12 to 14 days of age and reared in different production systems. Journal of Animal Science 75, 3004-3009. Bergstrom, J.R., M.D. Tokach, R.D. Goodband, J.L. Nelssen, T.L. Signer, and G. Lynch, 1995. Influence of buffered propionic and fumaric acid on starter pig performance. Journal of Animal Science (Suppl. 2) 73 (Abstr.). Bourne, F.J., 1984. Gut immunity in the pig - Hypersensitivity responses to dietary antigens. Animal Production 38, 526(Abstr.). Bray, T.M. and W.J. Bettger, 1990. The physiologic role of zinc as an antioxidant. Free Radicals Biology Medicine 8, 281. Brooks, P.H., S.J. Russel, and J.L. Carpenter, 1984. Water intake of weaned piglets from three to seven weeks old. Veterinary Record 115, 513-515. Carlson, M.S., G.M. Hill, and J.E. Link, 1999. Early and traditional weaned nursery pigs benefit from phase-feeding pharmacological concentrations of zinc oxide. Journal of Animal Science 77, 1199. Cera, K.R., D.C. Mahan, R.F. Cross, G.A. Reinhart, and R.E. Whitmoyer, 1988a. Effect of age and postweaning diet on small intestinal growth and jejunal morphology in young swine. Journal of Animal Science 66, 574-584. Cera, K. R., D. C. Mahan and G. A. Reinhart, 1988b. Weekly digestibilities of diets supplemented with corn oil, lard or tallow by weanling swine. Journal of Animal Science 66, 1430. Cera, K.R., D.C. Mahan, and G.A. Reinhart, 1988c. Effects of dietary dried whey and corn oil on weanling pig performance, fat digestibility and nitrogen utilization. Journal of Animal Science 66, 1438. Cera, K.R., D.C. Mahan, and G.A. Reinhart, 1990. Effect of weaning, week postweaning and diet composition on pancreatic and small intestinal luminal lipase response in young swine. Journal of Animal Science 68, 384. Chung, J., B.Z. deRodas, C.V. Maxwell, and M.E. Davis, 1996. The effect of increasing whey protein concentrate as a lysine source on performance of segregated early weaned pigs. Journal of Animal Science 74(Suppl.1), 195 (Abstr.). Chung, T.K. and D.H. Baker, 1992. Methionine requirement of pigs between 5 and 10 kilograms body weight. Journal of Animal Science70, 1857-1863. Coelho, M., B. Cousins, and W. McKnight, 2001. Impact of a targeted B-vitamin regimen on rate and efficiency of growth on lean growth genotype pigs from 6 to 110 kilograms of body weight. Journal of Animal Science 79(Suppl. 1), 68 (Abstr.). Coffey, R.D., G.L Cromwell, H.J. Monegue, 1994. Efficacy of a Copper-Lysine Complex as a Growth Promotant for Weanling Pigs. Journal of Animal Science 72, 2880.

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Coffey, R.D., and G.L. Cromwell, 1995. The impact of environment and antimicrobial agents on growth response of early-weaned pigs to spray-dried porcine plasma. Journal of Animal Science 73, 2532. Corring, T., A. Aumaitre, and G. Durand, 1978. Development of digestive enzymes in the piglet from birth to 8 weeks. I. Pancreas and pancreatic enzymes. Nutrition and Metabolism 22, 231. Cranwell, P.D., Ma.L. Tarvid I, and R.G. Harrison, 1995. Weight at weaning, causes and consequences. In: D.P. Hennesey and P.D. Cranwell (editors), Manipulating Pig Production V. Proceedings of the Australasian Pig Science Association, Werrribee, Victoria, p. 119. Crow, S.D., K.J. Touchette, G.L. Allee, and M.D. Newcomb, 1995. Late nursery pigs respond to lactose (d 7 to 21 postweaning). Journal of Animal Science (Suppl. 2), 73 (Abstr.). De La Llata, S.S. Dritz, M., M. Langemeier, M.D. Tokach, R.D. Goodband, and J.L. Nelssen, 2001. Economics of increasing lysine: calorie ratio and dietary fat addition for growing-finishing pigs reared in a commercial environment. Journal of Swine Health and Production 9, 215-223. de Rodas, B.Z., C.V. Maxwell, M.E. Davis, S. Mandali, E. Broekman, and B.J. Stoecker, 1998. L-ascorbyl2-polyphosphate as a vitamin C source for segregated and conventionally weaned pigs. Journal of Animal Science 76, 1636-1643. Deen, J., S. Dritz, L.E. Watkins, and W.C. Weldon, 1998. The effect of weaning weights on the survivability, growth and carcass characteristics of pigs in a commercial facility. In: Proceedings of the 15th International Veterinary Pig Society Congress, Birmingham, England, p. 172. DeRouchey, J.M., M.D. Tokach, J.L. Nelssen, R.D. Goodband, S.S. Dritz, J.C. Woodworth, M.J. Webster, B.J. James, and D.E. Real, 2001a. Effects of irradiation processing of specialty protein products on nursery pig performance. Journal of Animal Science 79(Suppl. 1), (Abstract). DeRouchey, J.M., M.D. Tokach, J.L. Nelssen, R.D. Goodband, S.S. Dritz, and R.E. Musser, 2001b. Evaluation of Termin-8 addition to spray-dried animal plasma or base mix on growth performance of nursery pigs. Journal of Animal Science 79(Suppl. 1), (Abstract). Donovan, T.S. and S.S. Dritz, 2000. Effect of split nursing on variation in pig growth from birth to weaning. Journal of the American Veterinary Medical Assocciation 217, 79-81. Dove, C.R., 1993. The effect of adding copper and various fat sources to the diets of weanling swine on growth performance and serum fatty acid profiles. Journal of Animal Science 71, 2187. Dove, C.R., and K.D. Haydon, 1992. The effect of copper and fat addition to the diets of weanling swine on growth performance and serum fatty acids. Journal of Animal Science 70, 805. Dritz, S.S., M.D. Tokach, J.L. Nelssen, R.D. Goodband, and L.J. Kats, 1993. Optimal dried whey level in starter pig diets containing spray-dried blood meal and comparison of avian and bovine spray-dried blood meals. Journal of Animal Science (Suppl. 1)71, 57 (Abstr.). Dritz, S.S., R.D. Goodband, J.L. Nelssen, M.D. Tokach, and C.A. Kerr, 1994a. Comparison of carbohydrate sources for the early weaned pig. Journal of Animal Science (Suppl. 2)72, 69 (Abstr.). Dritz, S.S., M.D. Tokach, R.D. Goodband, J.L. Nelssen, and K.Q. Owen, 1994b. Optimum level of spray-dried porcine plasma for early-weaned (10.5 d of age) starter pigs. Journal of Animal Science (Suppl. 2)72, 69 (Abstr.). Dritz, S.S., M.D. Tokach, R.D. Goodband, J.L. Nelssen, and K.Q. Owen, 1994c. Optimum level of soybean meal for early-weaned (12 d of age) starter pigs. Journal of Animal Science (Suppl. 2)72, 70, (Abstr.).

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Dritz, S.S., K.Q. Owen, J.L. Nelssen, R.D. Goodband, and M.D. Tokach, 1996a. Influence of weaning age and nursery diet complexity on growth performance and carcass characteristics and composition of high health status pigs from weaning to 109 kilograms. Journal of Animal Science 74, 2975. Dritz, S.S., M.D. Tokach, R.D. Goodband, and J.L. Nelssen, 1996b. Nutritional programs for segregated early-weaned pigs: Part I. Management procedures and nutritional principles. Compendium of Continuing Education for Practicing Veterinariansacticing Veterinarians 18, S222. Dritz, S.S. Personal communications. Dritz, S.S., M.D. Tokach, R.D. Goodband, and J.L. Nelssen, 2002. An Evaluation of In-Feed Antimicrobial Regimens in Multi-Site Pig Production Systems. Journal of the American Veterinary Medical Assocciation 220, 1690-1695. Dunlop, R.H., S.A. McEwen, A.H. Meek, R.C. Clarke, W.D. Black, and R.M. Friendship, 1998. Associations among antimicrobial drug treatments and antimicrobial resistance of fecal Escherichia coli of swine on 34 farrow-to-finish farms in Ontario, Canada. Preventative Veterinary Medicine 34, 283-305. Edwards, H.M., and D.H. Baker, 1999. Bioavailability of zinc in several sources of zinc oxide, zinc sulfate, and zinc metal. Journal of Animal Science. 77, 2730-2735. Endres, B., F.X. Aherne, L. Ozimek, and H. Spicer, 1988. The effects of fat supplementation on ileal versus fecal fat digestibilities, performance and body composition of weaned pigs. Canadian Journal of Animal Science 68, 225. Engle, M.J., 1994. The role of soybean meal hypersensitivity in postweaning lag and diarrhea in piglets. Swine Health and Production 4, 7. Friesen, K.G., R.D. Goodband, J.L. Nelssen, F. Blecha, D.N. Reddy, P.G. Reddy, and L.J. Kats, 1993a. The effect of pre- and post weaning exposure to soybean meal on growth performance in the early-weaned pig. Journal of Animal Science 71, 2089. Friesen, K. G., J. L. Nelssen, R. D. Goodband, K. C. Behnke, and L. J. Kats, 1993b. The effect of moist extrusion of soy products on growth performance and nutrient utilization in the early weaned pig. Journal of Animal Science 71, 2099. Gabert, V.M., and W.C. Sauer, 1994. The effects of supplementing diets for weanling pigs with organic acids. A review. Journal of Animal and Feed Sciences 3, 73-87. Gatnau, R., D. R. Zimmerman, T. Diaz and J. Johns, 1991. Determination of optimal levels of spraydried porcine plasma (SDPP) in diets for weanling pigs. Journal of Animal Science 69(Suppl.1), 369(Abstr.). Giesting, D.W., and R.A. Easter, 1985. Response of starter pigs to supplementing corn-soybean meal diets with organic acids. Journal of Animal Science 60, 1288-1294. Grinstead, G.S., R.D. Goodband, S.S. Dritz, M.D. Tokach, J.L. Nelssen, J.C. Woodworth and M. Molitor, 2000. Effects of a whey protein product and spray-dried animal plasma on growth performance of weanling pigs. Journal of Animal Science 78, 647-657. Hahn, J.D. and Baker D.H, 1993. Growth and plasma zinc response of young pigs fed pharmacological levels of zinc. Journal of Animal Science 71, 3020. Han, Y., T.K. Chung, and D.H. Baker, 1993. Tryptophan requirement of pigs in the weight category 10 to 20 kilograms. Journal of Animal Science 71, 139.

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Hansen, J.A., J.L. Nelssen, R.D. Goodband, and T.L. Weeden, 1993. Evaluation of animal protein supplements in diets of early-weaned pigs. Journal of Animal Science 71, 1853. Harris, D.L., 2000. Multi-site pig production. Iowa State Press, Ames IA. Holm, A. and H.D. Poulsen, 1996. Zinc oxide in treating E. coli diarrhea in pigs after weaning. Compendium of Continuing Education for Practicing Veterinariansacticing Veterinarians (Supplement18), S26. Huang, S.X., M. McFall, A.C. Cegielski, and R.N. Kirkwood, 1999. Effect of dietary zinc supplementation on Escherichia coli septicemia in weaned pigs. Swine Health and Production 7.3, 109. James, B.W., S.S. Dritz, M.D. Tokach, R.D. Goodband, and J.L. Nelssen, 2000. Effects of lysine level fed from 19 to 36 kg on growth performance and backfat of barrows and gilts. Journal of Animal Science 78(Suppl. 1), 67 (Abstr.). James, B.W., R.D. Goodband, M.D. Tokach, J.L. Nelssen, J.M. DeRouchey, and J.C. Woodworth, 2001a. The optimum isoleucine: lysine ratio to maximize growth performance of the earlyweaned pig. Journal of Animal Science 79(Suppl. 1), (Abstr.). James, B.W., R.D. Goodband, M.D. Tokach, J.L. Nelssen, J.M. DeRouchey, and J.C. Woodworth, 2001b. The optimum threonine: lysine ratio to maximize growth performance of weanling pigs. Journal of Animal Science 79(Suppl. 1), 148 (Abstr.). James, B.W., R.D. Goodband, M.D. Tokach, J.L. Nelssen, J.M. DeRouchey, and J.C. Woodworth, 2001c. The optimum valine: lysine ratio in nursery diets to maximize growth performance in weanling pigs. Journal of Animal Science 79(Suppl. 1), (Abstr.). Jensen-Waern, M., L. Melin, R. Lingerg, R. Johannisson, A. Petersson, and P. Wallgren, 1998. Dietary zinc oxide in weaned pigs-effects on performance, tissue concentrations, morphology, neutrophil functions, and faecal microflora. Research in Veterinary Science 64, 225-231. Jiang, R., X. Chang, B. Stoll, M.Z. Fan, J. Arthington, E. Weaver, J. Campbell, and D.G. Burrin, 2000. Dietary plasma protein reduces small intestinal growth and lamina propria cell density in early weaned pigs. Journal of Nutrition 130, 21-26. Johnston, M.E., D.R. Cook, R.D. Boyd, K.D. Haydon, and J.L. Usry, 2000. Optimum threonine: lysine ratio in a corn-soybean meal diet for pigs in the late nursery phase (12-23 kg). Journal of Animal Science 78(Suppl. 2), 148 (Abstr.). Kats, L.J., J.L. Nelssen, M.D. Tokach, R.D. Goodband, J.A. Hansen, and J.L. Laurin, 1994a. The effect of spray-dried porcine plasma on growth performance in the early-weaned pig. Journal of Animal Science 72, 2075. Kats, L.J., J.L. Nelssen, M.D. Tokach, R.D. Goodband, J.A. Hansen, K.G. Friesen, and S.S. Dritz, 1994b. Influence of spray-dried blood meal on growth performance of the early-weaned starter pig. Journal of Animal Science 72, 2860. Kats, L.J., R.D. Goodband, J.L. Nelssen, M.D. Tokach, K.G. Friesen, S.S. Dritz, and K.Q. Owen, 1994c. The effect of spray-dried blood meal in the phase III (d 21 to 42 postweaning) diet. Journal of Animal Science (Suppl. 2) 72 (Abstr.). Kerr, B.J., 1999. Isoleucine nutrition in starting swine. Eleventh BioKyowa Amino Acid Conference. pp 1-16. Nutri-Quest, Inc. Chesterfield, MO.

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Kerr, C.A., R.D. Goodband, J.W. Smith, II, R.E. Musser, J.R. Bergstrom, W.B. Nessmith, Jr., M.D. Tokach, and J.L. Nelssen, 1998a. Evaluation of potato proteins on growth performance of earlyweanling pigs. Journal of Animal Science 76, 3024-3033. Kerr, C.A., R.D. Goodband, M.D. Tokach, J.L. Nelssen, S.S. Dritz, B.T. Richert, and J.R. Bergstrom, 1998b. Evaluation of enzymatically modified potato starches in diets for weanling pigs. Journal of Animal Science 76, 2838-2844. King, R.H. and G.B. Martin, 1989. Relationships between protein intake during lactation, LH levels and oestrus activity in first-litter sows. Animal Reproduction Science 19, 283-292. Klasing, K.C., 1988. Nutritional aspects of leukocytic cytokines. Journal of Nutrition 118, 14361446. Koketsu, Y. and G.D. Dial, 1998. Factors associated with average pig weight at weaning on farms using early weaning. Journal of Animal Science 66, 247-253. Koketsu, Y., G.D. Dial, and V.L. King, 1997. Influence of factors on farrowing rate on farms using early weaning. Journal of Animal Science 75, 2580-2587. Landblom, D.G., and W. Poland, 1998. Weanling pig response when naked oat and extruded field pea replace corn and soybean meal in pig starter diets. Journal of Animal Science 76(Suppl. 2), 63. Leaver, R., 1988. The Pelleting Process (2nd Ed.). Sprout-Bauer, Mucy, PA. Leibbrandt, V.D., R.C. Ewan, V.C. Speer, and D.R. Zimmerman, 1975. Effect of age and calorie:protein ratio on performance and body composition of baby pigs. Journal of Animal Science 40, 1070-1079. Levy, S.B., 1998. The challenge of antibiotic resistance. Scientific American 278, 46-53. Li, D.F., R.C. Thaler, J.L. Nelssen, D. Harmon, G.L. Allee, T. Weeden, G. Stoner, G. Fitzner, R. Hines and D. Nichols, 1989. Effect of fat source and fat combinations on starter pigs. Journal of Animal Science 67(Suppl.1), 230(Abstr.). Li, D.F., J.L. Nelssen, P.G. Reddy, F. Blecha, J.D. Hancock, G.L. Allee, R.D. Goodband, and R.D. Klemm, 1990a. Transient hypersensitivity to soybean meal in the early-weaned pig. Journal of Animal Science 68, 1790. Li, D.F., J.L. Nelssen, P.G. Reddy, F. Blecha, R. Klemm, and R.D. Goodband, 1990b. Interrelationship between hypersensitivity to soybean proteins and growth performance in early-weaned pigs. Journal of Animal Science 69, 4062. Li, D.F., J.L. Nelssen, P.G. Reddy, F. Blecha, R.D. Klemm, D.W. Geisting, J.D. Hancock, G.L. Allee, and R.D. Goodband, 1991a. Measuring the suitability of soybean products for early-weaned pigs with immunological criteria. Journal of Animal Science 69, 3299. Li, D.F., J.L. Nelssen, P.G. Reddy, F. Blecha, R.D. Klemm, and R.D. Goodband, 1991b. Interrelationship between hypersensitivity to soybean proteins and growth performance in early-weaned pigs. Journal of Animal Science 69, 4062. Lindemann, M.D., S.G. Cornelius, S.M. El Kandelgy, R.L. Moser, and J.E. Pettigrew, 1986. Effect of age, weaning and diet on digestive enzyme levels in the piglet. Journal of Animal Science 62, 1298. Madec, F., F. Bridoux, S. Bounaix, and A. Jestin, 1998. Measurement of digestive disorders in the piglet at weaning and related risk factors. Preventative Veterinary Medicine 35, 53-72.

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Mahan, D.C., 1992. Efficacy of dried whey and its lactalbumin and lactose components at two dietary lysine levels on postweaning pig performance and nitrogen balance. Journal of Animal Science 70, 2182-2187. Mahan, D.C., 1994. Effects of dietary vitamin E on sow reproductive performance over a five-parity period. Journal of Animal Science 72, 2870-2879. Mahan, D.C., 1990. Carbohydrate - The limiting nutrient in a corn-soybean meal diet for weanling pigs. Journal of Animal Science 69(Suppl.1), 102(Abstr.). Mahan, D.C., and E.A. Newton, 1993. Evaluation of feed grains with dried skim milk and added carbohydrate sources on weanling pig performance. Journal of Animal Science 71, 3376-3382. Mahan, D.C., E.M. Weaver, and L.E. Russell, 1996. Improved postweaning performance responses by adding NaCl or HCl to diets containing animal plasma. Journal of Animal Science 74(Suppl. 1), 58(Abstr.). McCully, G.A., G.M. Hill, J.E. Link, R.L. Weavers, M.S. Carlson, and S.W. Rozeboom, 1995. Evaluation of zinc sources for the newly weaned pig. Journal of Animal Science (Suppl. 2) 73 (Abstr.). Mores, N., J. Cristani, I.A. Piffer, W. Barioni Jr., and G.M.M. Lima, 1998. Effects of zinc oxide on postweaning diarrhea control in pigs experimentally infected with E. coli. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 50, 513-523. NRC, 1998. Nutrient Requirements of Swine. (10th Ed.) National Academy Press, Washington, D.C. NRC, 1988. Nutrient Requirements of Swine (9th Revised Ed.). National Academy Press, Washington, D.C. Nam, D.S. and F.X. Ahern, 1994. The effects of lysine:energy ratio on performance of weanling pigs. Journal of Animal Science 72, 1247-1256. Nelssen, J.L., 1986. High nutrient density diets for weanling pigs. Proceedings 47th Minnesota Nutrition Conference pp 132-154. Minneapolis, MN. Nelssen, J.L., 1990. Recent advances in high nutrient density starter diet research. Proceedings 51st Minnesota Nutrition Conference pp 217-230. Minneapolis, MN. Nessmith Jr., W.B., M.D. Tokach, R.D. Goodband, and J.L. Nelssen, 1997. Defining quality of lactose sources used in swine diets. Swine Health and Production 5, 145-149. Nessmith Jr., W.B., M.D. Tokach, R.D. Goodband, J.L. Nelssen, J.R. Bergstrom, J.W. Smith II, K.Q. Owen, and S.S. Dritz, 1995. The effects of substituting spray-dried whole egg from grading plants only for spray-dried animal plasma in phase I diets. Journal of Animal Science (Suppl. 1) 73 (Abstr.). Owen, K.Q., J.L. Nelssen, M.D. Tokach, R.D. Goodband, S.S. Dritz and L.J. Kats, 1993. The effect of increasing level of lactose in a porcine plasma-based diet for the early weaned pig. Journal of Animal Science 71(Suppl. 1), 175(Abstr.). Owen, K.Q., J.L. Nelssen, R.D. Goodband, M.D. Tokach, L.J. Kats, and K.G. Friesen, 1995a. Added dietary methionine in starter pigs diets containing spray-dried blood co-products. Journal of Animal Science 73, 2647. Owen, K.Q., R.D. Goodband, J.L. Nelssen, M.D. Tokach, and S.S. Dritz, 1995b. The effect of dietary methionine and its relationship to lysine on growth performance of the segregated early-weaned pig. Journal of Animal Science 73, 3666.

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Owen, K.Q., J.L. Nelssen, R.D. Goodband, M.D. Tokach, K.G. Friesen, B.T. Richert, J.W. Smith, and L.E, Russell, 1995c. The influence of various plasma fractions on starter pig performance. Journal of Animal Science 73(Suppl. 1), 81(Abstr.). Owen, K.Q., J.L. Nelssen, R.D. Goodband, M.D. Tokach, B.T. Richert, K.G. Friesen, J.W. Smith, J.R. Bergstrom, and S.S. Dritz, 1995d. Dietary lysine requirements of segregated early-weaned pigs. Journal of Animal Science, 73(Suppl. 1), 68 (Abstr.). Owen, K.Q., R.D. Goodband, J.L. Nelssen, M.D. Tokach, J.R. Bergstrom, K.G. Friesen, J.W. Smith, and B.T. Richert, 1995e The effects of increasing digestible lysine from 18 to 34 kg on growth performance of segregated early weaned pigs. Journal of Animal Science 73(Suppl. 1), 69 (Abstr.). Pierce, J.L., G.L. Cromwell, M.D. Lindemann, and R.D. Coffey, 1995. Assessment of three fractions of spray-dried porcine plasma on performane of early-weaned pigs. Journal of Animal Science 73(Suppl. 1), 81(Abstr.). Rantanen, M.M., R.H. Hines, J.D. Hancock, K.C. Behnke, M.R. Cabrera, and I.H. Kim, 1995a. Effects of novel carbohydrates on growth performance of nursery pigs. Journal of Animal Science 73(Suppl. 1), 179 (Abstr.). Rantanen, M.M., R.H. Hines, J.D. Hancock, M.R. Cabrera, and L.L. Burham, 1995b. Influence of oat products on growth performance of weanling pigs. Journal of Animal Science 73(Suppl. 1), 78 (Abstr.). Real, D.E., M.U. Steidinger, J.L. Nelssen, M.D. Tokach, R.D. Goodband, S.S. Dritz, J.M. DeRouchey, J.C. Woodworth, and K.Q. Owen, 2001. Effects of dietary L-carnitine on growth performance of nursery pigs. Journal of Animal Science 79(Suppl. 1), (Abstract). Reinhart, G.A., F.A. Simmen, D.C. Mahan, C.M. Simmen, and M.E. White, 1990. Isolation, characterization, and developmental expression of pig intestinal fatty acid binding proteins. Journal of Nutritional Biochemistry 1, 592-598. Richert, B.T.; J.D. Hancock, J.L. Morrill, 1994. Effects of replacing milk and soybean products with wheat glutens on digestibility of nutrients and growth performance in nursery pigs. Journal of Animal Science 72, 151-159. Rincker, M.J. S.D. Carter, R.W. Senne, and K.Q. Owen, 2001. Effects of L-carnitine and soybean oil on growth performance in weanling pigs. Journal of Animal Science 79(Suppl. 1), 149 (Abstr.). Scherer, C.W., V.W. Hayes, G.L. Cromwell, and D.D. Kratzer, 1973. Effects of diet and age on pancreatic lipase activity and fat utilization in pigs. Journal of Animal Science 37(Suppl. 1), 290 (Abstr.). Smith II, J.W., M.D. Tokach, R.D. Goodband, J.L. Nelssen, and B.T. Richert, 1997. Effects of the interrelationship between zinc oxide and copper sulfate on growth performance of early-weaned pigs. Journal of Animal Science 75, 1851. Smith II, J.W., M.D. Tokach, R.D. Goodband, S.S. Dritz, and J.L. Nelssen, 1999a. The effects of increasing zinc oxide on growth performance of weanling pigs. Professional Animal Science 14, 197. Smith II, J.W., M.D. Tokach, J.L. Nelssen, and R.D. Goodband, 1999b. Effects of lysine:calorie ratio on growth performance of 10- to 25-kilogram pigs. Journal of Animal Science 77, 3000.

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Stahly, T.S., S.G. Swenson, and R.C. Ewan, 1996. Dietary B vitamin needs of high and moderate lean growth pigs fed from 20 to 62 pounds body weight, 1995 Swine Research Report. Iowa State Univ. Ext., AS-633. Ames, IA. Stark, C.R., K.C. Behnke, J.D. Hancock, and R.H. Hines, 1993. Pellet quality affects growth performance of nursery and finishing pigs. Kansas Agricultural Experiment Station Report of Progress 695. p 67. Stephas, E.L., and B.L. Miller, 1998. Evaluatioin of dextrose as a replacement for crystalline lactose in phase I and phase II nursery diets. Journal of Animal Science 76(Suppl. 1), 66(Abstr.). Steidinger, M.U., R.D. Goodband, M.D. Tokach, S.S. Dritz, J.L. Nelssen, L.J. McKinney, B.S. Borg, and J.M. Campbell, 2000. Effects of pelleting and pellet conditioning temperatures on weanling pig performance. Journal of Animal Science 78, 3014-3018. Stoner, G.R., G.L. Allee, J.L. Nelssen, M.E. Johnston, and R.D. Goodband, 1990. Effect of select menhaden fish meal in starter diets for pigs. Journal of Animal Science 68, 2729. Straw, B., 1994. Selection and use of antibiotics for swine. In: Proc. George A. Young Swine Conf Ann Nebraska SPF Swine Conf, Lincoln, NE, p.33. Tokach, L.M., S.S. Dritz, and M.D. Tokach, 2000. Diagnosis and calculation of economic impact of incorrect pharmacologic dosage of zinc oxide supplementation aided by record analysis of nursery performance. Swine Health and Production 8.5, 229. Tokach, M.D., J.L. Nelssen, and G.L. Allee, 1989. Effect of protein and/or carbohydrate fractions of dried whey on performance and nutrient digestibility of early weaned pigs. Journal of Animal Science 67, 1307. Tokach, M.D., J.E. Pettigrew, G.D. Dial, et al., 1992. Characterization of luteinizing hormone secretion in the primiparous, lactation sow: relationship to blood metabolites and return-to-estrus interval. Journal of Animal Science 70, 2195-2201. Tokach, M.D., J.E. Pettigrew, L.J. Johnston, M. Overland, J.W. Rust, and S.G. Cornelius, 1995. Effect of adding fat and (or) milk products to the weanling pig diet on performance in the nursery and subsequent grow-finish stages. Journal of Animal Science 73, 3341. Touchette, K.J., S.D. Crow, G.L. Allee, and M.D. Newcomb, 1995. Weaned pigs respond to lactose (d 0 to 14 postweaning ). Journal of Animal Science (Suppl. 2)73 (Abstr.). Turner, J.L., S.S. Dritz, and J.E. Minton, 2001. A review of natural alternatives to conventional antimicrobials in swine diets. Professional Animal Science In Press. Whittemore, C.T., A. Aumaitre, and I.H. Williams, 1978. Growth of body components in young weaned pigs. Journal of Agricultural Science (Cambridge), 91, 681-691. Williams, N. H., T. S. Stahly, and D. R. Zimmerman, 1997a. Effect of chronic immune system activation on the rate, efficiency, and composition of growth and lysine needs of pigs fed from 6 to 27 Kg. Journal of Animal Science 75, 2463-2471. Williams, N.H., T.S. Stahly, and D.R. Zimmerman, 1997b. Effect of level of chronic immune system activation on the growth and dietary lysine needs of pigs fed from 6 to 112 kg. Journal of Animal Science 75, 2481-2496. Wilson, M.E., M.D. Tokach, R.W. Walker, J.L. Nelssen, R.D. Goodband, and J.E. Pettigrew, 1993. Influence of high levels of individual B vitamins on starter pig performance. Journal of Animal Science 71 (Suppl. 1), 56 (Abstr.).

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Wilson, M.E., J.E. Pettigrew, L.J. Johnston, J.D. Hawton, J.W. Rust, and H. Chester-Jones, 1991. Provision of additional B vitamins improves growth rate of weanling pigs. Journal of Animal Science 69 (Suppl. 1), 106 (Abstr.). Witte, W., 1998. Medical consequences of antibiotic use in agriculture. Science 279, 996-997. Woodworth, J.C., M.D. Tokach, J.L. Nelssen. R.D. Goodband, P.R. O’Quinn, and T.M. Falker, 1999a. The effects of added zinc from an organic zinc complex or inorganic sources on weanling pig growth performance. Journal of Animal Science (Supplement 1) 77, 61. Woodworth, J.C., M.D. Tokach, J.L. Nelssen, R.D. Goodband, P.R. O’Quinn, and T.M. Falker, 1999b. The effects of different zinc sources on weanling pig growth performance. Journal of Animal Science (Supplement 1) 77, 177. Woodworth, J.C., M.D. Tokach, J.L. Nelssen, R.D. Goodband, P.R. O’Quinn, and T.M. Fakler, 1999c. The effects of added zinc from organic and inorganic zinc sources on weanling pig growth performance. Journal of Animal Science 77(Suppl. 1), 61(Abstr.). Woodworth, J.C., M.D. Tokach, J.L. Nelssen, R.D. Goodband, P.R. O’Quinn, and T.M. Fakler, 1999d. The effects of added zinc from zinc sulfate or zinc sulfate/zinc oxide combinations on weanling pig growth performance. Journal of Animal Science 77(Suppl. 1), 61(Abstr.). Woodworth, J.C., R.D. Goodband, J.L. Nelssen, M.D. Tokach, and R.E. Musser, 2000. Pyridoxine, but not thiamin improves weanling pig growth performance. Journal of Animal Science 78, 88-93. Zimmerman, D.R., J.C. Sparks, and C.M. Cain, 1997. Carry-over response to an intestinal hydrolysate in weanling pig diets. Journal of Animal Science 75(Suppl. 1), 71(Abstr.).

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12 Intestinal nutrient requirements in weanling pigs D. Burrin and B. Stoll

12.1

Introduction

In the postnatal life of the pig, the period of weaning is marked by significant changes in nutrition and the environment. The extent to which the young pig can adapt physiologically to these changes determines its survival, health and subsequent growth rate. Of particular importance to this adaptation process is the functional development of the gastrointestinal tract, particularly digestive, absorptive and immune function. In the past few years, there has been considerable progress in our understanding of intestinal nutrient metabolism, particularly in young pigs. However, despite its overall importance to the pig’s health and adaptation the impact of weaning on the rate and pattern of intestinal nutrient utilization remains a poorly understood, yet critical, nutritional issue. The aim of this chapter is to first briefly review the underlying changes in the gastrointestinal physiology of the weanling pig and then to describe how these changes impact the nutrient needs of the gastrointestinal tract and the animal as a whole. Although this chapter will focus mainly on the small intestine, the nutrient requirements necessary to support physiological functions in other components of the gastrointestinal tract during weaning are also mentioned, including the stomach, large intestine and pancreas.

12.2

Changes in gut physiology during weaning

During the process of weaning, there are several key nutritional and environmental factors that contribute to significant changes in structure and function of the gastrointestinal tract; many of these factors are reviewed in detail in this book and elsewhere (Maxwell and Stewart 1995; Pluske et al. 1995; Pluske et al. 1997; Fraser et al. 1998; Gaskins 1998; Dreau and Lalles 1999; Le Dividich and Seve 2000; Stokes et al. 2001). These factors are as follows, 1) the change in mode of nutrient ingestion, namely from suckling milk from the dams udder to ingestion of feed from a feeder, 2) the change in the physical and chemical composition from a liquid to a dry diet, 3) the psychological and behavioral stress associated with the change in mode of nutrient ingestion, withdraw from the sow and mixing with unfamiliar pigs, and 4) the qualitative and quantitative changes in the gut microflora. During the process of weaning, these factors simultaneously interact with each other to produce temporal changes in gastrointestinal structure and function. For the purpose of this discussion, these temporal changes are divided into the acute phase observed within the first five to seven days after weaning and the adaptive phase that occurs subsequently (Figure 12.1). The distinction between acute and adaptive phases is

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-50 15

Figure 12.1. Changes in energy intake and weight gain in young pigs before and after weaning. Pigs were weaned from the sow at 14 days of age and fed a corn-based diet containing soy or whey protein (24% crude protein and 14.8 MJ energy). Adapted from Jiang et al. 2000.

based primarily on the changes in feed intake, since it takes about seven days for weaned pigs to learn how to eat out of a feeder and resume an intake that is comparable to that during the pre-weaning period (Pluske et al. 1997; Le Dividich and Seve, 2000). 12.2.1

Acute phase

The dominant factor affecting gut structure and function during the acute phase after weaning is the reduction in feed intake (Figure 12.1). Although the underlying cause of the loss of appetite has not been clearly established, it is likely due to the psychological and behavioral stress associated with the change in mode of nutrient ingestion, withdraw from the sow and mixing with unfamiliar pigs. However, the impact of reduced feed intake on the gut is clearly evident in the diminished overall mass and mucosal structure of the small intestine (Figure 12.2). The reduced feed intake appears to have a limited effect on stomach weight, however, the weight of the colon is increased approximately threefold within seven days after weaning (McCracken et al. 1995; Jiang et al. 2000). During the acute phase, there is a significant reduction in protein and DNA mass, as well as villus height, in the small intestine. In general, studies show that villus height is reduced approximately 50% within the first three to five days after weaning (Pluske et al. 1997). Despite the overall reduction in DNA content and villus height during the acute phase, the depth and rate of proliferation in the crypt compartment increases substantially, indicative of crypt hyperplasia. In addition, there is also an increased cell density in the lamina

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200 Protei n mass DNA mass

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300

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15

Figure 12.2. Changes in intestinal morphology, cell proliferation and mass in young pigs before and after weaning. Pigs were weaned from the sow at 14 days of age and fed a corn-based diet containing soy or whey protein (24% crude protein and 14.8 MJ energy). Adapted from Jiang et al. 2000.

propria of the villus region, indicative of increased infiltration and proliferation of lymphoid cells (Jiang et al. 2000). The reduction in gut mass and mucosal thickness in response to reduced feed intake is a well known phenomenon (Bragg et al. 1991). In young pigs, the absence of nutrients in the intestinal lumen, as a result of either reduced feed intake or parenteral nutrition, leads to reduced cell proliferation, protein synthesis and villus atrophy (Davis et al. 1996; Burrin et al. 2000; Stoll et al. 2000). The underlying factors that mediate the loss of gut mass are multifactorial, but include deprivation of lumen substrates for mucosal epithelial cell growth and reduced secretion and expression of humoral gut growth factors, such as glucagon-like peptide 2 and IGFI (Carroll et al. 1998; Burrin, 2001; Stoll and Burrin, 2001). The crypt hyperplasia that occurs despite the reduction in feed intake, however, is somewhat unexpected and may be linked to several factors. One of the most important factors in hyperplasia of both the crypt epithelium and lamina propria region is believed to be gut hypersensitivity reactions in response to components in the weaning diet, namely plant proteins, such as soy glycinins and lectins, and fiber (Jin et al. 1994; Dreau and Lalle 1999; Jordinson et al. 1999). However, an additional factor that contributes to increase in lymphoid cell density within the intestinal mucosa is the normal development of adaptive immune function (Gaskins 1998; Kelly and Coutts, 2000). During the acute phase of weaning, the pig is especially vulnerable to pathogenic infection in part because of the abrupt withdraw of sow’s milk, which contains numerous factors that bolster the intestinal immune defense. In addition, however, the changes in the diet composition and the environment lead to a shift

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in the colonization of commensal gut microorganisms, providing a situation for growth of opportunistic pathogenic organisms. Pathogenic infection results in an activation of the mucosal immune system and release of proinflammatory cytokines (e.g. tumor necrosis factor α and interleukins) that have been shown to increase crypt cell proliferation and villus enterocyte apoptosis (Rafferty et al. 1994; Piguet et al. 1999). Infection, the presence of bacteria and proinflammatory cytokines also have been shown to increase the synthesis of intestinal acute phase proteins and mucins (Higashiguchi et al. 1994; Breuille et al. 1998; Wang et al. 1998; Mack et al. 1999). Thus, there would appear to be a general increase in protein metabolic activity associated with activation of the mucosal immune system, yet this is in contrast to the observed loss of intestinal protein mass during the acute phase of weaning (Figure 12.2). This loss of intestinal protein indicates a relative increase in the balance of proteolysis versus protein synthesis. A plausible explanation for the acute phase loss in intestinal protein mass is the apoptotic death and proteolytic degradation of villus enterocytes. However, there is very little published information about the temporal changes in gut protein metabolism during the acute phase of weaning. 12.2.2

Adaptive phase

During the adaptive phase of weaning, the pig has regained its appetite and feed intake is and comparable to, or in excess of, the preweaning intake (Figure 12.1). The resumption of relatively normal feed intake is marked by significant increases in the masses of the small intestinal, stomach and large intestine; however the levels attained are in excess of those observed during preweaning (Figure 12.2) (Kelly et al. 1991b; Jiang et al. 2000; McCracken et al. 1995). Within the small intestinal mucosa the villus height increases to a small degree, but does not return to the preweaning levels. The depth of the crypt compartment continues to increase, yet the rates of proliferation appear to plateau. Based on the few reported studies with weaned pigs, it would appear that the increase in intestinal protein mass after weaning is accompanied by a significant increase in the protein synthesis rate (Table 12.1) (Seve et al. 1986; Seve et al. 1993; Nyachoti et al. 2000). This relative increase in small intestinal protein synthesis rate after weaning may stem from the higher dry matter intake, but also could be linked to presence of fiber and plant proteins, such as lectins (Southon et al. 1985; Palmer et al. 1987). Moreover, there is evidence that the rates of protein synthesis are also higher in the large intestine in young pigs fed a higher fiber (69%) cereal-based diet than in those fed a low fiber (21%) diet containing casein and starch (Nyachoti et al. 2000). These observations, coupled with the marked increase in mass of the small and large intestines, suggest that the amino acid requirement necessary to support gastrointestinal tissues are substantially higher during the adaptive period of weaning.

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Table 12.1. Fractional protein synthesis rates in tissues of young, milk-fed piglets and weaned, growing pigs1.

Pancreas Stomach Jejunum Ileum Cecum Colon Liver Muscle Skin Kidney Spleen

Young-Milk-fed2

Weaned-growing3

60 -103 32 39 - 79 53 nd nd 56 - 72 6-8 13 25 14

162 nd 98 - 119 104 123 138 52 - 68 3 - 33 nd nd nd

1

Values are expressed as %/d based on the bolus-dose phenylalanine method. Values obtained from Davis et al. 2001; Burrin et al. 1999b; and Davis et al. 1996. 3 Values obtained from Nyachoti et al. 2000 and Seve et al. 1993. 2

The increased dry matter intake not only stimulates growth of the small and large intestine, but the increase in fiber content and decreased digestibility of weaning diets have further implications. First, there is an increase in the number of the colonic microflora that translates into increased fermentation and production of short-chain fatty acids (SCFA) (Risley et al. 1992; Maxwell and Stewart 1995). It is noteworthy that the SCFA concentrations have been reported to increase not only in the lower colon, but also increase several-fold in the stomach and jejunal fluid (Risley et al. 1992). Studies with colonocytes have demonstrated that SCFA may be used both as oxidative substrates and as a stimulus of cell proliferation (Darcy-Vrillon et al. 1993; Darcy-Vrillon et al. 1996; Sakata and Inagaki, 2001), yet the capacity for SCFA oxidation in enterocytes in the small intestine is lower than colonocytes (Fleming et al.1991). A second potentially important consequence of increased SCFA production in the lower intestine and colon is the stimulus of intestinal blood flow (Kvietys and Granger, 1981). Furthermore, increased colonic SCFA stimulate gut hormone secretion, in particular glucagon-like peptide 2 (GLP-2). GLP-2 is a potent nutrient-dependent gut growth factor (Burrin et al. 2001). Studies in rats show that feeding fiber and infusion of SCFA upregulates the expression of proglucagon in the distal bowel and this is associated with increased circulating concentrations of GLP-2 (Reimer and McBurney, 1996; Tappenden et al. 1998). The increased circulating GLP-2 may serve as an indirect gut trophic signal that mediates the increase in cell proliferation that is observed under these two conditions. These

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observations suggest that, in the weaned pig, the increased production of SCFA may trigger increased secretion of GLP-2 and explain the increase in crypt cell proliferation. The adaptive phase of weaning is also characterized by substantial increases in digestive enzyme capacity, particularly gastric proteases and pancreatic proteases and α-amylase activity (Lindemann et al. 1986; Kelly et al. 1991c;Cranwell, 1995; Bach Knudsen and Jorgensen, 2001). In addition, there is a significant increase in the activity and capacity of maltase and glucoamylase in the small intestine. The increase in these carbohydrate digestive enzymes is diet-induced and a function of the increased starch content found in most cereal-based weaning diets. Furthermore, the increased pancreatic digestive enzyme production is associated not only with increased specific activity, but also increased volume of pancreatic enzyme output (Pierzynowski et al. 1990; Pierzynowski et al. 1993). The proteins secreted from the pancreas, as well as the stomach, small and large intestine and gallbladder, are collectively referred to as endogenous proteins. An important nutritional consideration with respect to endogenous protein secretion is the extent to which these endogenous proteins are digested and the amino acids reutilized by the intestine. In particular, the mucin glycoproteins are a class of proteins present in endogenous secretions that play an important role in the innate barrier function throughout the gastrointestinal tract (Deplancke and Gaskins 2001). Given their role in gut barrier function, one could predict that goblet cell density and mucin secretion might increase after weaning, and there is some evidence to support this in pigs (Brown et al. 1988). The production of mucins may be nutritionally significant, in that, because they are relatively resistant to digestion within the small intestine, the amino acids present in the mucin glycoproteins are not reabsorbed, but instead are catabolized by microbial fermentation in the large intestine. There is very little quantitative information as to the extent to which mucins and other gastrointestinal secretions are digested, and their constituent amino acids and hexose molecules are reabsorbed or fermented in the colon.

12.3

Intestinal nutrient utilization in young pigs

In the past five years, there have been significant advancements in the our understanding of intestinal nutrient metabolism in young pigs. Quantitative estimates of intestinal nutrient utilization and their impact on whole animal nutrient requirements have been determined from in vivo studies in pigs using isotopic tracers and measurements of trans-organ balance of substrates, such as glucose and amino acids (Ebner et al. 1994; Reeds et al. 1996; Bertolo et al. 1998; Stoll et al. 1998; Stoll et al. 1999; Van Goudoever et al. 2000; Van der Schoor et al. 2001). These and other studies with cultured porcine intestinal enterocytes have revealed important qualitative characteristics of the metabolic fate of key substrates and the underlying cellular basis for intestinal nutrient utilization (Blachier et al. 1991;

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Blachier et al. 1992; Blachier et al. 1993; Darcy-Vrillon et al. 1994; Blachier et al. 1995; Wu, 1998; Wu and Morris, 1998; Rhoads,1999). The recent advances in our understanding of intestinal nutrient metabolism in young pigs fed milk-based diets compliment the earlier pioneering studies with adult (50 to 70 kg body weight) pigs published over the past twenty years (Rerat et al. 1984; Rerat et al. 1987; Rerat and Simoes-Nunes, 1988; Rerat et al. 1988; Rerat and Simoes-Nunes 1988; Rerat et al. 1992; Yen et al. 1997). However, despite the breadth in our current knowledge, there is still a significant gap in our understanding of the intestinal nutrient metabolism in young weanling pigs consuming conventional cereal-based diets. 12.3.1

Physiological and cellular basis of gut metabolism

12.3.1.1 Relative metabolic rate Much of what we know about intestinal nutrient utilization is derived from studies that have measured the metabolic exchange of nutrients across the portal-drained visceral (PDV) tissues. The PDV tissues are comprised largely of gastrointestinal tissues, including the stomach, pancreas, small and large intestine, but also includes the spleen. In pigs, the PDV tissues contribute approximately 5% of body weight, yet they account for 20% to 35% of whole-body protein turnover and energy expenditure (Yen et al., 1997; Stoll et al., 1999a; Van Goudoever et al. 2000). The disproportionate impact of gastrointestinal tissues on whole-body metabolism is a function of their relatively high fractional rates of protein synthesis and oxygen consumption. Studies in pigs have demonstrated that the fractional protein synthesis rates in the gastrointestinal tissues are substantially higher than that in peripheral tissues, especially skeletal muscle (Table 12.1) (Simon et al. 1982; Seve et al. 1986; Burrin et al. 1992; Davis et al. 1996). However, there are also differences within the tissues of the gastrointestinal tract, where protein synthesis rates are higher in the small intestine than in the stomach and large intestine (Attaix and Arnal, 1987; Attaix et al., 1992; Burrin et al., 1999a; Burrin et al. 1999b; Stoll et al. 2000). The high rates of metabolism and nutrient utilization in the gut are directly linked to the high rates of proliferation, protein secretion, cell death and desquamation of various epithelial and lymphoid cells within the mucosa. In young pigs, epithelial cells have a life span of about three to ten days (Fan et al., 2001). Within the small intestinal epithelium, the proliferative crypt compartment contains pluripotent stem cells which undergo mitosis and differentiation into four cell lineages: absorptive enterocytes, mucin-producing goblet cells, antibacterial peptide-producing Paneth cells, and enteroendocrine cells. In addition, present in the lamina propria region beneath the epithelium are lymphoid and other cell types including, T and B lymphocytes, macrophages, neutrophils, mast cells, dendritic cells and fibroblasts.

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Studies in vitro show that these epithelial (Higashiguchi et al. 1993; Wu 1998) and lymphoid (Szondy and Newsholme, 1990; Wu et al. 1991; Dugan et al., 1994) cell types exhibit high rates of protein synthesis and glutamine metabolism. In the case of goblet cells, there is a substantial utilization of nutrients for mucin secretion, which make up a large component of endogenous secretions that are fermented in the colon (Lien et al., 1997). 12.3.1.2 Luminal versus arterial nutrient utilization

Tissu e Free Isotopic en richment % plasma enrichmen t

Another critical anatomical consideration with respect to the metabolism of intestinal epithelial cells is that they derive nutrients from two separate sources: the luminal route via the diet and from the blood via the arterial circulation. Estimates derived from studies in piglets fed a milk-based formula indicate that the absolute rate of nutrient input to the PDV tissues from the arterial circulation is significantly greater than from the diet (Figure 12.3) (Stoll et al. 1998). The diet represents less than 30% of the total nutrient input to the PDV tissues, with the exception of aspartate. However, there is a preferential utilization of some amino acids from the luminal route, namely glutamate and glutamine (Table 12.2). When expressed as a percentage of the inputs, the uptakes of glutamate and glutamine are 96% and 67% from the lumen and 11% and 21% from the arterial circulation, respectively. Interestingly, the uptake of luminal glucose, both on a relative and absolute basis, is considerably less than that of amino acids. Instead the use of glucose by the PDV tissues is preferentially derived from the arterial circulation. Although the relative rate of extraction from the arterial input is nearly equal to

100 Prox ima l Jejunum Distal Ileu m

80 60 40 20 0

P < 0.05 vs 0%

0

20 40 60 80 Enteral intake, % total intake

100

Figure 12.3. Rates of amino acid input into the PDV tissues from the diet and arterial circulation in young piglets. Dietary inputs were based on intake of sow’s milk replacer fed at 12 g protein/kg per day. Arterial inputs were calculated from measurements of arterial amino acid concentration and portal blood flow rate; this assumed arterial and portal blood flow to be equal. Adapted from Stoll et al. 1998.

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Table 12.2. Relative portal utilization of glucose, glutamate and glutamine from the luminal and arterial sources in piglets fed a milk-based formula.1

Luminal Input Uptake % Arterial Input Uptake %

Glucose

Glutamate

Glutamine

3,400 217 6.4

585 562 96

219 147 67

18,874 1227 6.5

731 80 11

934 191 21

1Data

are expressed as µmol•kg-1•h-1 , unless otherwise indicated. Calculated from Stoll et al. (1999a).

that from the diet, the absolute rate of arterial glucose utilization is substantially greater than the combined uptake of both glutamate and glutamine. Thus, the utilization of glucose by PDV tissues is derived largely from the arterial circulation (85% total), with only a small contribution from the diet (15%). The general preference for arterial nutrients is perhaps not surprising if one considers how nutrients are normally presented to the PDV tissues. Under normal conditions, when animals are fed diets with polymeric forms of carbohydrate and protein, the level of free glucose and amino acids in the lumen is relatively low in the stomach and large intestine. Because the digestive environment in the stomach and large intestine limits the luminal availability of glucose and amino acids, the nutrient needs of these tissues must be met by the arterial circulation. This idea should also hold for the proximal versus distal small intestine, if one assumes that most of the dietary carbohydrate and protein is digested and the resulting monosaccharides and amino acids are absorbed efficiently in the proximal intestine. To demonstrate this, we studied neonatal piglets infused intravenously with 3H-leucine and then administered increasing amounts of their total nutrient intake intragastrically, while maintaining a constant total nutrient intake via intravenous nutrient infusion (Stoll et al. 2000). The results showed that in piglets receiving 100% of their nutrient intake via the enteral route, the proportion of systemically-derived labeled leucine in the mucosal free amino acid pool is significantly greater in the distal ileum than the proximal jejunum (Figure 12.4). The results also show that as increasing amounts of nutrients were infused via the enteral or luminal route, there was a marked decrease in the isotopic enrichment in the proximal jejunum due to increased absorption and dilution by unlabeled enteral leucine. Additional evidence

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Net portal nutrient utilization % of dietary intake

100

GL

N

P U A S GL

80

TH 60

40

R ME

T

Y GL L YS U R L E SE HE AL RO P V P

20

IL E

UC GL

E OS

0

Figure 12.4. Changes in the tissue isotopic enrichment of 2H-leucine in the proximal jejunum and distal ileum of neonatal pig fed varying proportions of their total nutrient intake via the enteral versus parenteral route. Seven day-old piglets were fed an elemental diet either intragastrically or intravenously for seven days, then infused intravenously with 2H-leucine for six hours prior to sampling. Adapted from Stoll et al. 2000.

consistent with this idea can be found in pigs studied during acute-phase of weaning, where atrophy occurs primarily in the small intestine, while the mass of the stomach and large intestine is preserved (McCracken et al. 1995; Jiang et al. 2000). 12.3.1.3 Crypt versus villus enterocytes Another important factor that affects the extent to which epithelial cells derive their nutrients from the luminal or vascular input is their stage of differentiation and physical location along the crypt-villus axis. Early studies (Alpers 1972) showed that crypt cells are more highly labeled with isotopic tracers derived from the blood, whereas villus cells are more highly labeled with tracers given luminally. These results implied that crypt cells derive their nutrients predominantly from the arterial circulation, whereas villus cells rely on nutrients absorbed luminally from the diet. If this phenomenon is true, it may explain the reduced villus length seen during the acute-phase of weaning, because luminal nutrient supply is significantly reduced. However, studies with animals fed via total parenteral nutrition have shown that intestinal mucosal growth and villus height can be maintained, even in the absence of luminal nutrients, by providing intravenous gut growth factors, such as GLP-2, IGF-I, EGF, or SCFA (Koruda et al. 1990; Goodlad et al. 1992; Peterson et al. 1996; Burrin et al. 2001). These studies suggest that, if an appropriate intestinal growth stimulus is provided, villus enterocytes are not strictly dependent on luminal nutrients and have the capacity to extract sufficient nutrients from the arterial

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circulation necessary for survival. Further studies using simultaneous systemic and luminal isotope labeling coupled with isolation of crypt and villus enterocytes are warranted to characterize how stage of differentiation and spatial localization affects the source of nutrients for epithelial cells. 12.3.2

Major oxidative fuels

12.3.2.1 Glutamine, glutamate, aspartate A significant proportion of the dietary nutrients are metabolized by gastrointestinal tissues, due to their relatively high metabolic rate. However, the pattern of nutrient utilization by the PDV tissues is not uniform and some nutrients are preferentially metabolized. A number of studies in pigs have shown that there is substantial utilization of dietary glutamine, glutamate and aspartate by PDV tissues (Reeds et al. 1996; Rerat et al. 1992; Van der Muelen et al. 1997; Stoll et al. 1998; Reeds et al. 2000). Results from young piglets fed a high protein, milk-based formula indicated that more than 95% of the dietary glutamine, glutamate and aspartate is utilized by the gut (Figure 12.5) (Stoll et al. 1998). These results are consistent with the seminal studies of Windmueller and Spaeth (1974, 1975, 1976, 1978, 1980), which first showed evidence of extensive metabolism of these three substrates in in situ intestinal perfusions in fasted, anaesthetized rats. These studies have since spawned literally hundreds of studies that have tended to focus on the role of glutamine as the major oxidative fuel in the gut. However, it is important to note that both glutamate and aspartate are of perhaps equal

3500

L Y AL A

G

PDV amino acid input (µmol • kg-1 • h-1)

3000 2500 2000

R TH

Diet Arterial LN G

LE

U VA

1500

L

O PR

S LY

LU G IL

E

1000 P AS

500

E PH

AR

G

ET M

0

Figure 12.5. Rates of net portal nutrient utilization in young piglets. Dietary inputs were based on intake of sow’s milk replacer fed at 12 g protein/kg per day. Adapted from Stoll et al. 1998.

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importance as intestinal oxidative fuels. Recent studies in young pigs and humans confirm the extensive intestinal oxidation of dietary 13C-labeled glutamate and glutamine (Battezati et al. 1995; Stoll et al. 1999a; Haisch et al. 2000). The metabolism of glutamine is accomplished first by the catalysis via phosphatedependent glutaminase and subsequently by glutamate dehydrogenase (GDH) enzymes, both of which are present in the stomach, small intestine and colon of the young pig (Madej et al. 1999). Interestingly, the activity of GDH is increased approximately threefold in the small intestine after weaning. The resulting keto-acid product of GDH is α-ketoglutarate, which is then metabolized yielding CO2 via the tricarboxylic acid cycle. It is important to note that, although there is extensive uptake and metabolism of these three amino acids, their carbon skeletons are not completely oxidized to CO2 and they do not account for all of the CO2 released by the gut. The in situ studies with perfused rat intestine and those in vivo with piglets and humans indicate that most of the glutamine (55% to 70%), glutamate (52% to 64%) and aspartate (52%) are oxidized to CO2 (Windmueller and Spaeth 1976; Windmueller and Spaeth 1978; Stoll et al. 1999a). The remaining carbon atoms from these three substrates, that are not oxidized to CO2 , are converted to lactate, alanine, proline, citrulline, ornithine and arginine and then released into the portal circulation (Windmueller and Spaeth 1975; Stoll et al. 1999a). The metabolic fate of nitrogen from these amino acids is not fully understood. However, evidence suggests that a portion of the nitrogen derived from glutamine and glutamate metabolism is transferred to ammonia and other amino acids, including citrulline, ornithine, proline and arginine. Other potentially important biosynthetic products of glutamine metabolism are nucleotides used for RNA and DNA synthesis (Gate et al. 1999). 12.3.2.2 Glucose Glucose is another important oxidative fuel for the gut, although less significant quantitatively than glutamate, glutamine, and aspartate. Glucose is often considered as a “primal” oxidative fuel for most mammalian tissues, yet studies by Windmueller and Spaeth (1978) showed that the uptake of arterial glutamine and glucose are roughly equal in the postabsorptive rodent intestine. However, we are only beginning to understand the quantitative significance of intestinal glucose metabolism in growing pigs fed conventional diets. Early studies in finishing pigs reported that only 57% to 70% of a dietary glucose load was absorbed into the portal circulation, implying that 43% to 30% is metabolized by the intestine (Rerat et al.1984). More recent studies in piglets fed a lactose-containing, milk-replacer have reported higher rates of glucose absorption ranging from 85% to 92%, suggesting that only 8% to 15% of the glucose is metabolized by the gut (Stoll et al. 1999a; Van der Schoor et al. 2001). Thus, it appears that the proportion of intestinal utilization of dietary glucose increases with age, yet its unclear whether this is due to age, per se, or a variety of other factors.

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Of the glucose utilized by the gut tissues, a relatively small fraction is completely oxidized to CO2. In the perfused rat intestine, oxidation of arterial glucose was about 10% to 15%, whereas 29% of luminal glucose is converted to CO2 (Windmueller and Spaeth, 1980). In contrast, in vivo measurements of PDV glucose metabolism in piglets indicate a higher fractional oxidation of arterial (28%) than of dietary glucose (3%) (Stoll et al. 1999a). Studies with isolated porcine enterocytes confirm the relatively low oxidation rate of glucose (~10-15%) and also demonstrated a significant decline in both the cellular uptake and oxidation of glucose between birth and weaning (Darcy-Vrillon et al. 1994; Wu et al. 1995). The ontogeny of intestinal glucose oxidation in the neonatal rat appears to differ from the pig, and studies have shown that glucose oxidation increases markedly during and shortly after weaning (Kimura, 1996). Interestingly, however, in porcine intraepithelial lymphocytes isolated at 21, 29 and 56 days of age, glucose oxidation was highest after weaning at 29 days (Dugan et al. 1994). Studies in enterocytes also show that glucose oxidation is inhibited in the presence of glutamine, but glutamine oxidation is not altered by addition of glucose (Wu et al. 1995). Taken together, the results indicate that intestinal tissues preferentially derive much more energy from glutamine and glutamate than glucose. However, given the evidence in rodents, more studies are warranted to examine the impact of weaning on intestinal substrate utilization and whether glucose perhaps becomes a quantitatively more significant fuel source. A majority of the glucose carbon utilized by gut tissues is either metabolized to lactate and alanine or used for biosynthetic purposes. In the perfused rat intestine, 43% to 58% of arterial glucose is metabolized to lactate, 13% to 19% is converted to alanine, and approximately 25% is incorporated into intestinal tissue and mesenteric lipid (Windmueller and Spaeth 1978; Windmueller and Spaeth 1980). Similarly, in vivo studies with pigs demonstrate that of the relatively small fraction of dietary glucose utilized by the PDV tissues, 45% and 37% is metabolized to lactate and alanine, respectively (Stoll et al. 1999a). However, considerably less of the arterial glucose (approximately 10%) is metabolized to lactate and alanine. This implies that a large proportion of the intestinal glucose requirement, which is derived largely from the arterial circulation, may be used for biosynthesis of structural and functional molecules, such as mucin glycoproteins, fatty acids and lipids. 12.3.2.3 Ketones and short-chain fatty acids In the categories of ketones and short-chain fatty acids, there are several substrates that have been shown to be metabolized by the gut, including acetoacetate, βhydroxybutyrate, acetate, propionate, and butyrate. The early studies by Windmueller and Spaeth (1978) showed that in the perfused rat intestine approximately 50% of CO2 production was derived from oxidation of β-hydroxybutyrate (26%) and acetoacetate (24%). Although the total utilization of ketones was only 40% of that

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observed with glutamine and glucose, the fractional oxidation of ketones to CO2 was high (64%). There is very limited information on intestinal ketone utilization in pigs. In general, ketogenesis is relatively low in newborn piglets and increases with age (Adams and Odle, 1993; Tetrick et al., 1995). However, studies in rats indicate that β-hydroxybutyrate oxidation is relatively low in suckling rats and increases significantly after weaning (Kimura, 1996). These studies indicate the potentially significant metabolic role of ketones as an intestinal fuel, especially under fasting conditions during the acute-phase of weaning, when ketones may be elevated in the blood. Short-chain fatty acids or volatile fatty acids are also potentially important oxidative substrates. The total concentration of SCFA in luminal contents of postweaned pigs are relatively high (~500-4000 mM) not only in the cecum, but also in the stomach and jejunum (Risley et al. 1992). The most abundant SCFA in the stomach and jejunum is acetate with negligible concentrations of propionate and butyrate. In the cecum, acetate is also the most abundant SCFA, but there are significant concentrations of propionate and butyrate; the molar proportion of acetate, propionate and butyrate is 54%, 28% and 18%, respectively. In finishing pigs fed a corn-fish meal diet, the rate of portal SCFA absorption is approximately 1000 µmol•kg-1•h-1 with the relative proportions of acetate, propionate and butyrate being 52%, 38% and 10% (Rerat et al. 1987). In vivo studies in fasted dogs indicate that the fractional extraction of circulating acetate by the PDV is high (~70%) and represents approximately 5% of whole body acetate utilization (Pouteau et al. 1998). Studies in finishing pigs indicate that SCFA can represent up to 25% of whole body energy expenditure (Yen et al. 1991), yet we know little about the extent of SCFA metabolism specifically by gut tissues in pigs. Studies in rodents and ruminants indicate that there is significant metabolism of all three of the major SCFA by intestinal tissues (Bergman, 1990; Fitch and Fleming, 1999). The recent study using the luminally-perfused rat colon indicates that approximately 10% to 20% of the acetate and butyrate are oxidized to CO2 and substantial amounts of butyrate are metabolized to β-hydroxybutyrate and lactate (Fitch and Fleming, 1999). Moreover, when a complete mixture of substrates was perfused, as much as 40% of the butyrate was preferentially metabolized relative to acetate (20%). 12.3.3

Essential amino acid utilization

12.3.3.1 Metabolic fate The metabolic fate of dietary essential amino acids utilized by the intestinal tissues has a critical influence on their availability for growth. Essential amino acids can be used for three major metabolic purposes: (1) incorporation into protein; (2)

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conversion via transamination into other amino acids, metabolic substrates and biosynthetic intermediates; and (3) complete oxidation to CO2. Amino acids incorporated into cellular protein can be degraded within the mucosal cells and released into the portal circulation. In addition, amino acids incorporated into cellular protein also can be secreted or sloughed into the gut lumen and then be degraded and reabsorbed into the portal circulation. In either of the latter two scenarios, the amino acids are “recycled” back into the body and are available for lean tissue growth. However, when amino acids are metabolized irreversibly to either non-amino acid intermediates or completely into CO2 , they become unavailable for lean tissue growth. The following discussion will highlight the importance of various essential amino acids for gut function and how this may impact their dietary requirement in the weanling pig. 12.3.3.2 Intake level, chemical form, and digestibility Studies of net portal amino acid balance in pigs suggest that the intestinal utilization of essential amino acids is significant, ranging from 30% to 85% of the dietary intake (Figure 12.6) (Rerat et al. 1988; Van Der Meulen et al. 1997; Stoll et al. 1998; Van Goudoever et al. 2000; Van Der Schoor et al. 2001). Among the studies with pigs using the portal A-V balance approach, a number of factors have been shown to affect net absorption and utilization of dietary essential amino acids, including the level of intake and chemical form. Recent studies in young pigs fed cow’s milk-based liquid diets, demonstrated that the PDV utilization of essential amino acids, expressed as a proportion of the dietary intake, is significantly higher in pigs fed a low- (10%) versus high-protein (25%) diet (Van Goudoever et al. 2000;

Portal amino acid utilization % intake

125

High protein Low protein

100

75 50

25

0 THR

LYS

ILE

PHE

LEU

Figure 12.6. Net rates of portal essential amino acid utilization in young pigs fed either a high (25%) or low (10%) protein diet for seven days. Adapted from Van Goudoever et al. 2000.

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Van Der Schoor et al. 2001). These and other previous (Ebner et al. 1994) studies found that gut growth was preserved despite a reduced rate of whole body growth when pigs are fed a low-protein diet. The critical implication from these studies in that there is a preferential utilization of amino acids by the gut such that, when the dietary intake is markedly reduced, it limits the net absorption and availability of dietary amino acids for peripheral lean tissue growth. Another factor that appears to affect the intestinal utilization of dietary essential amino acids is the chemical form in which they are fed. Studies with finishing pigs, found that the portal absorption of amino acids was significantly lower when fed as free amino acids than as peptides (Rerat et al. 1988). These findings have implications for feeding crystalline amino acids in weanling pig diets and suggest that there is preferential intestinal utilization of supplemented free amino acids compared to those fed as intact proteins. This preferential intestinal utilization of crystalline amino acids may contribute to the reduced availability and increased catabolism reported for free versus protein-bound lysine (Batterham and Bailey 1989; Daenzer et al. 2001). Although the intestinal absorption of crystalline free amino acids is assumed to be 100%, further studies are warranted to establish their “portal availability” in pig diets. Other studies in grower pigs (40 kg), demonstrated that net portal uptake of essential amino acids was higher in pigs fed maize versus pea starch (Van Der Meulen et al. 1997), implying an interaction between dietary carbohydrate source and amino acid availability. In pigs fed diets where the protein source is less than 95% to 100% digestible, the ileal amino acid availability is a critically important consideration, when interpreting the relative intestinal amino acid utilization rate. If the net portal utilization rate of an amino acid is expressed relative to the dietary intake, and the digestibility of the amino acid is not 100%, then the intestinal utilization rate will be incorrectly overestimated. This concern is negligible in pigs fed diets containing highly digestible, milk proteins, but is important with many other plant and animal protein sources. On the other hand, however, if the intent is to determine the availability of dietary amino acids for lean tissue growth, then it could be argued that the net “portal availability” of an amino acid is perhaps a more valid, biologically relevant estimate than the ileal availability. Moreover, because net portal availability reflects the balance between the gut and the rest of the body, it avoids the uncertainties of determining endogenous losses. 12.3.3.3 Threonine, methionine, and cysteine Threonine utilization by the gut is higher than any other essential amino acid. Most studies of net portal balance in pigs, indicate that approximately 40% to 60% of the dietary threonine intake is utilized by the PDV tissues (Rerat et al. 1988; Van der Meulen et al. 1997; Stoll et al. 1998). However, a recent report in young pigs

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fed a high-protein, milk-based diet, indicated that as much as 85% of the dietary threonine is used by the gut (Figure 12.6) (Van der Schoor et al. 2001). The utilization of sulphur amino acids (methionine and cysteine) is also substantial, with various estimates ranging from 30% to 58% of the dietary intake (Rerat et al. 1988; Van der Meulen et al. 1997; Stoll et al. 1998). Estimates based on whole body amino acids requirements demonstrated that the requirements for threonine and methionine in parenterally fed neonatal piglets were 40% and 70%, respectively, of that observed in enterally fed piglets (Bertolo et al. 1998; Shoveller et al. 2000). These latter studies imply that intestinal uptake and metabolism account for 60% and 30%, respectively, of the whole body threonine and methionine requirements in neonatal pigs. Moreover, cysteine can be synthesized from methionine, and thus represents a possible end-product of intestinal methionine utilization. Studies in neonatal pigs also have shown that supplemental cysteine reduces the whole body methionine requirement, when fed either enterally or parenterally (Shoveller et al. 2000). Thus, the extent to which the intestine can convert methionine to cysteine warrants further study. Two potentially important uses for threonine and cysteine in the gut are for the synthesis of mucins and glutathione. The secretory mucins play a key role in the innate immune defense of the mucosa, and the core protein of the major intestinal mucins contains a large amount of threonine and cysteine (Fogg et al. 1996; van Klinken et al. 1997). In addition, cysteine is a component of the tripeptide antioxidant glutathione, which is critical for the maintenance of the structural integrity and barrier function of the intestinal mucosa (Martensson et al. 1991). The mucosal synthesis and secretion of mucins and glutathione are likely to be quantitatively significant, and thus the needs for dietary threonine and cysteine may be increased during the weaning process where there is gut hypersensitivity or inflammation. A recent study demonstrated that feeding a threonine-deficient diet to piglets significantly reduces intestinal mass and goblet cell numbers, and this suppression of intestinal growth cannot be fully restored by providing threonine parenterally (Ball et al. 1999). Besides incorporation into mucin and other mucosal proteins, the extent to which threonine is further metabolized within the intestine is poorly understood. There is some debate as to which metabolic pathway is most important in the catabolism of threonine in mammals (House et al. 2001). The two predominant pathways of threonine catabolism in the pig are believed to be catalyzed by either threonine aldolase/dehydrogenase or threonine dehydratase (Ballevre et al. 1990; Le Floc’h et al. 1996; Le Floc’h et al. 1997). Studies in pigs suggest that conversion to glycine via threonine aldolase/dehydrogenase is the predominant pathway of irreversible threonine catabolism. Moreover, threonine dehydrogenase activity was localized to both the liver and pancreas, but not other gut tissues, implicating the PDV as a possible site of threonine catabolism. Despite this evidence, there is negligible 13C-threonine oxidation to CO2 by the PDV when given either enterally or systemically to young

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piglets (Van Goudoever and Reeds unpublished results). However, this does not preclude the possibility that metabolism of threonine to glycine is nutritionally significant and warrants further study. 12.3.3.4 Lysine, phenylalanine and branched-chain amino acids The intestinal utilization and net portal availability of dietary lysine are particularly important, given that lysine is the first limiting amino acid in weanling pigs. Studies in young piglets fed milk-replacer indicate that only about 55% of the dietary lysine intake is absorbed, suggesting that the gut utilizes 45% (Figure 12.6) (Stoll et al. 1998; Van Goudoever et al. 2001). The net portal lysine utilization in grower-finishing pigs fed cereal-based diets was similar (50% of intake) in one report (Rerat et al. 1988), but substantially lower (27.5% of intake) in another (Van Der Meulen et al. 1997). Similar to lysine, the net portal utilization of phenylalanine and branched-chain amino acids (BCAA) is also high, with the gut consuming on average approximately 50% of the dietary intake (Stoll et al. 1998b; Stoll et al. 1999b; Van Goudoever et al. 2001). In older pigs, estimates of net portal utilization rates of BCAA are slightly greater (~60% of intake) (Rerat et al. 1988), whereas others found much lower (~28%) rates (Van Der Meulen et al. 1997). The explanation for the discrepancy between results of Rerat et al. (1988) and Van Der Meulen et al. (1997) is probably due to the fact that the latter study expressed the portal fluxes relative to the amount of the ileal digested amino acid rather than the intake, a point mentioned previously. In general, the catabolism of essential amino acids by the gut has been considered to be negligible, based on the assumption that the liver is the main site of oxidation (Wu, 1998). However, recent studies based on isotopic tracer kinetics in PDV tissues suggest that dietary essential amino acids are oxidized within the gut, particularly lysine and leucine. Studies in young pigs showed that intestinal oxidation of dietary lysine accounted for about one-third of whole-body lysine oxidation and was completely suppressed by feeding a low-protein diet (Van Goudoever et al. 2000). Interestingly, although arterial lysine was taken up by the PDV, none of this was oxidized, suggesting a preferential oxidation of dietary lysine (Van Goudoever et al. 2000). As with lysine, there is significant leucine metabolism by the gut via both transamination to α-ketoisocaproic acid (KIC) and complete oxidation to CO2. Studies in young pigs and dogs have demonstrated that approximately 5-10 % of whole-body leucine flux is oxidized by the PDV (Yu et al. 1995; Van Der Schoor et al. 2001). Although approximately 40% of the leucine taken up by the gut was converted to KIC, nearly all of this is transaminated back to leucine, thus, the net KIC release is negligible (Yu et al. 1995). Studies in young, grower pigs (15-20 kg) suggest that approximately 15% of the whole- body phenylalanine flux is oxidized by the PDV tissues (Bush et al. 2001). The oxidation of phenylalanine implies that phenylalanine hydroxylation occurs in the gut and is consistent with previous

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observations suggesting net portal tyrosine production in excess of dietary intake. Given that hydroxylation rather than complete oxidation to CO2 represents the point of irreversible loss of phenylalanine, further studies are warranted to quantify the proportion of whole body phenylalanine flux metabolize to tyrosine by the gut. Additional studies are also needed to establish the localization of essential amino acid catabolic enzymes within the different mucosal cell phenotypes, i.e. enterocytes versus lymphoid cells. 12.3.3.5 Arginine and proline In suckling pigs, arginine is considered to be essential in the diet. Studies have shown that the small intestine is an important site of arginine and proline synthesis (Murphy et al., 1996; Wu, 1998; Stoll et al. 1999a). In the healthy suckling pig, the intestinal synthesis of arginine provides only about half of the animal’s needs for growth and the arginine concentration in sow’s milk is also limiting (Davis et al. 1994). Moreover, the net intestinal synthesis of arginine declines substantially during the late suckling period (Wu and Morris 1998). These observations raise the possibility that both the endogenous (via gut synthesis) and dietary arginine supply may be limiting for maximal growth of suckling piglets. Studies with enterocytes from newborn pigs (Blaicher et al. 1993; Wu and Knabe 1995) have shown developmental changes in arginine-metabolizing enzymes. At birth, the enterocytes are the major site of arginine synthesis, but gradually become the major site of net citrulline production as intestinal arginase expression increases via a glucocorticoid-dependent mechanism. In weanling pigs, intestinal citrulline synthesis from glutamine, glutamate and proline is the main source for circulating citrulline, which plays a critical role in whole body arginine homeostasis (Dugan et al. 1995). This transition is compensated by the gradually increasing capacity of the kidney to use citrulline for arginine synthesis. Thus, following the transition from suckling to weanling, the intestine probably becomes a site of net arginine degradation rather than synthesis (Wu and Morris 1998). The limited arginine degradation by enterocytes from newborn pigs ensures a maximum output of arginine (synthesized from glutamine or derived from milk) into the portal circulation for utilization by extraintestinal tissues. The induction of type II arginase in enterocytes after weaning possibly regulates the availability of arginine for the synthesis of nitric oxide (NO), ornithine and thus, polyamines, proline, and glutamate by the small intestinal mucosa. Major end-products of arginine metabolism by intestinal enterocytes from weaned pigs are proline and ornithine. Proline, required for collagen synthesis, is one of the most abundant amino acids in human milk (Davis et al. 1994). Providing proline in the diet can ameliorate the hyperammonemia associated with dietary arginine deficiency in neonatal pigs (Brunton et al. 1999). Thus, while proline is not considered an absolute dietary essential nutrient, it may be conditionally essential for maintaining

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arginine synthesis in neonates. It is apparent from a number of studies that a normally functioning gut is important for maintenance of whole-body arginine and proline status, especially in neonates. Furthermore, these amino acids become conditionally essential under conditions that markedly reduce gut mass or compromise function, such as massive small bowel resection (Wakabayashi et al. 1995). Recent studies in cultured intestinal cells have shown that ornithine derived from arginine metabolism is converted to polyamines (Blaicher et al. 1995). Polyamines (putrescine, spermidine, spermine, cadaverine) are ubiquitous cationic amines involved in cell proliferation and differentiation in many tissues, including the gastrointestinal tract. Ornithine decarboxylase (ODC) and S-adenosyl-methionine decarboxylase (SAMDC), converting ornithine to putrescine and putrescine to spermine, respectively, are the rate-limiting enzymes in polyamine synthesis. The synthesis of polyamines from arginine is negligible in enterocytes of newborn and suckling animals (Blaicher et al. 1991; Blaicher et al. 1992), but increases in enterocytes of postweaning animals, concurrent with the induction of both arginase and ODC (Wu and Morris 1998). Polyamines are present in porcine milk and luminal administration of polyamines increases intestinal growth in adult rats and enhances intestinal maturation and cell proliferation in developing rats (Dufour et al. 1988; Grant et al. 1990; Kelly et al. 1991a). Thus, when the ingestion of milkborne polyamines by the suckling pig ceases after weaning, the induction of intestinal polyamine synthesis from ornithine, arginine and proline may become physiologically significant for the maintenance of normal intestinal growth and function (Wu et al. 2000a; Wu et al. 2000b). Furthermore, the weaning-induced cortisol surge has been shown to be a key signal in the induction of intestinal polyamine synthesis. 12.3.4

Interactions between nutrition and enteric health and function

12.3.4.1 Gut specific nutrients In the past, weanling pig diets have been manipulated largely to overcome the limitations or immaturity in digestive function in order to maximize growth of the whole animal. However, given our increased understanding of intestinal nutrient utilization, it is possible to now formulate weanling pig diets with the specific goal of optimizing the growth, function and health of the gut. From the foregoing discussion of intestinal nutrient utilization some of the most promising candidates are glutamine, glutamate and threonine. A survey of the numerous literature reports of dietary glutamine supplementation indicate that the effects on intestinal growth are equivocal (Reeds and Burrin 2001). However, surprisingly few studies have been done in weanling pigs, yet these studies suggest dietary glutamine supplementation may be beneficial. Studies in weanling pigs by Ayonrinde et al.

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(1995) and Wu et al. (1996) showed that supplementing the diet with crystalline glutamine at either 4% or 1%, respectively, increased intestinal villus height. In addition, Wu et al. (1996) and Kitt et al. (2001) found 1% dietary glutamine supplementation to increase weight gain in weanling pigs. Another report found that weanling pigs fed diets supplemented with 4% glutamine had increased muscle glutamine concentrations and improved lymphocyte function (Yoo et al. 1997). A more recent study with early-weaned pig diets showed that dietary supplementation (% dry matter) with either glutamate (6.5%) or arginine (0.93%) modestly increased intestinal mass and villus height, whereas neither citrulline (0.94%), or ornithine (0.90%) had any effect and polyamines (0.39%) were detrimental (Ewtushik et al. 2000). Interestingly, the latter study also showed that glutamate supplementation markedly increased (200%) the plasma glutamine concentration, implying that glutamate had a glutamine-sparing effect or perhaps served as a precursor for glutamine synthesis. In the case of threonine, the studies of Ball et al. (1999) suggest that dietary threonine is particularly essential for intestinal growth and mucus production in young pigs. Another recent study showed a dose-dependent increase in weight gain and feed efficiency in early-weaned pigs fed a basal corn-soybean meal diets supplemented with crystalline threonine (0.250.50 % diet dry matter), despite the fact that the basal diet was formulated to meet the dietary threonine requirement (Lackeyram et al. 2001). Taken together, these studies suggest that further studies are warranted to examine the dose efficacy of dietary supplementation with these particular amino acids on enteric health and post-weaning growth in pigs. In addition to amino acids, there are other nutrients that have been shown to improve intestinal growth and function in rodents, but have yet to be examined in weanling pig diets. Among these are long-chain polyunsaturated fatty acids and nucleotides. The interest in dietary long-chain fatty acids (LCFAs) stems from the idea that n-3 long-chain, polyunsaturated fatty acids (LC-PUFAs) have been shown to improve the health and development of infants. The concentrations of several n-3 LC-PUFAs are higher in breast milk than in formulas and have prompted the recent move to include the fatty acids in infant formulas. It is well established that the n-3 LC-PUFAs or omega-3 fatty acids, particularly docosahexanoic acid (DHA), eicosapentaenoic acid (EPA) and arachidonic acid (AA), have pleiotropic biological effects on immune function, inflammation, hemodynamics, and bone metabolism (Calder 1999). The interest in adding n-3 LC-PUFAs to infant formula has been heightened by recent studies showing that supplementing these fatty acids can lower the incidence and inflammatory effects of necrotizing enterocolitis in neonatal infants and rats (Akisu et al. 1998; Carlson et al. 1998; Caplan et al. 2001). There is limited information regarding the intestinal trophic effects of either n-3 LC-PUFA or other LCFA in developing animals. However, a series of studies by Vanderhoof et al. (Vanderhoof et al. 1984; Vanderhoof et al. 1994; Kollman et al. 1999) have demonstrated that n-3 LC-PUFAs enhance

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intestinal adaptation after small- bowel resection, and their effects were greater than those of less saturated oils; they also found that medium-chain triglycerides are less trophic than long-chain triglycerides. Another LC-PUFA of interest is the isomer of n-6 linoleic acid, conjugated linoleic acid (CLA), which has been shown to enhance lean tissue growth in pigs (Ostrowska et al. 1999; Bassanganya-Riera et al. 2001a). The impact of CLA on the weanling pig intestine is unknown, but it has been shown to increase colonocyte apoptosis (Park et al. 2001) and enhance the cytotoxic function of lymphocytes (Bassanganya-Riera et al. 2001b). Nucleotides are ubiquitous, low-molecular-weight, intracellular compounds that are integral to numerous biochemical processes, and are especially important as precursors for nucleic acid synthesis in rapidly dividing cells, such as epithelial and lymphoid cells in the mucosa (Cosgrove, 1998). Nucleotides consist of a purine or pyrimidine base, which can be synthesized within cells de novo from glutamine, aspartic acid, glycine, formate, and carbon dioxide as precursors, or they can be salvaged from the degradation of nucleic acids and nucleotides. The relative significance of de novo synthesis versus the salvage pathway for intestinal nucleotide requirements is not clear; however, the evidence suggests that dietary sources of purine and pyrimidine bases are necessary (Uauy et al. 1994; Boza et al. 1996). Numerous reports have demonstrated that dietary supplementation with nucleosides, nucleotides, or nucleic acids supports small intestinal mucosal immune function, growth and morphology in vivo and in vitro (Uauy et al. 1994; Lopez-Navarro et al. 1996; Cosgrove 1998; Carver, 1999). 12.3.4.2 Impact of antimicrobials and infection A critical factor influencing the growth of weanling pigs is the degree of infestation with pathogenic microbes. Studies with growing animals indicate that exposure to these organisms and their toxins can adversely affect intestinal structure and function (Figure 12.7) (Von Allmen et al., 1992; Higashiguchi et al. 1994; Breuille et al., 1998; Wang et al., 1998; Mack et al., 1999). The studies demonstrate that the pro-inflammatory stimulus induced by bacteria, endotoxin and cytokines significantly increases the intestinal protein synthesis rate. Recent work in sheep demonstrated that parasitic infection increases the rate of leucine utilization and oxidation by PDV tissues, thereby reducing the systemic availability of dietary amino acids by 20-30% (Yu et al., 2000). In addition, most of the increased PDV leucine utilization is either oxidized or lost as endogenous protein secretion; together, these losses account for most of the reduced nitrogen retention associated with infection (Yu et al., 2000). Thus, it is likely that enteric infection increases the intestinal nutrient requirements, which in turn limits the availability of dietary nutrients for growth of weanling pig. This raises two critical questions for future studies 1) how does infection alter the pattern of intestinal nutrient utilization? and 2) what are the key nutrients that may become limiting for either intestinal function or whole body

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Dietary Amino Acids

An timicrobials Bacteria

Villus Ce lls

NH4 Toxins

Proliferating Cry pt Cells

Blood

Increased Mucosal Amino A cid Util ization

Increased Proinf lammator y Cytokines

Decrea sed Amino Acid Ab sorption

Figure 12.7. Schematic illustration of the relationship between intestinal amino acid metabolism and the luminal bacteria.

growth in infected pigs? It is likely that threonine will be a key nutrient under these conditions, given its importance for intestinal metabolism and that it is one of the first limiting amino acids for growth in swine. Antimicrobial compounds are fed to weanling pigs in order to suppress the activity of the gut microflora and enhance growth; although the exact mechanism for this effect is unknown. However, it is generally held that by suppressing microbial activity, antimicrobials reduce the luminal concentration and associated toxic insult of ammonia, and thereby diminish the thickness and mass of the intestinal mucosa and associated lymphoid tissue (Visek 1978). Studies in pigs and chickens show that feeding antimicrobial compounds significantly reduces small intestinal mass, cell proliferation and intestinal ammonia absorption (Yen et al. 1987; Yen and Pond 1990; Krinke and Jamroz 1996). Additional evidence indicates that the luminal ammonia arises from bacterial hydrolysis of urea and deamination of dietary amino acids. Thus, a critical mechanistic question regarding the site of dietary amino acid utilization in the gastrointestinal tract is whether this activity is associated with the luminal microbes or the cell populations of the mucosa.

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12.4

Summary and perspectives

Three important themes of this chapter are 1) that the gut undergoes significant morphological and functional adaptation during weaning, 2) that under normal conditions, the gut consumes a substantial proportion of the dietary nutrients, and 3) that the gut preferentially uses specific nutrients. As young pigs transition from suckling sow’s milk to consumption of cereal-based weaning diets there is an increase in gastrointestinal growth, marked by increased proliferation of epithelial cells and the synthesis and secretion of proteins within the stomach, intestine and pancreas. Some of the important factors contributing to this increased growth are related to increased voluntary dry matter intake and digestive enzyme production, as well as, immune hypersensitive and inflammatory responses to noxious compounds arising from the diet and microflora. This stimulation of gut growth likely translates into increased intestinal nutrient requirements, yet further study is needed to establish how the weaning processes alters the quantity and pattern of gut nutrient utilization. Some of the key nutrients that are preferentially used by the gut include glucose and nonessential amino acids, glutamate, glutamine and aspartate, but also essential amino acids that are limiting for lean tissue growth, namely threonine. It remains to be seen whether the increased intestinal utilization of these key nutrients limits their availability for maximal growth of the weanling pig. If so, then perhaps these “gut specific” nutrients should be supplemented or their dietary requirements increased to improve growth. An alternate approach to enhancing growth is to limit those factors which stimulate intestinal growth during weaning. For example feeding antimicrobials or employing segregated weaning practices will reduce the microbial pathogen load and the nutritional cost associated with immune stimulation. A final point of consideration is that while the maintenance of enteric health and intestinal function is key for supporting maximum growth of the weaned pig, it’s clear that this imparts a nutritional cost. Thus, the aim of future research should be to identify novel nutritional management approaches that optimize intestinal function while minimizing the nutritional cost associated with increased intestinal metabolism.

Acknowledgments The authors would like to thank Jane Schoppe for her assistance in the preparation of this manuscript. This work is a publication of the USDA/ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine and Texas Children’s Hospital, Houston, TX. The work was supported in part by federal funds from the U.S. Department of Agriculture Agricultural Research Service, Cooperative Agreement No. 58-6258-6001, by the National Institutes of Health R01 HD33920. The contents of this publication do not necessarily reflect the views or policies of the U.S. Department of Agriculture, nor does mention of trade names, commercial products, or organizations imply endorsement by the U.S. Government.

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Grant, A.L., J.W. Thomas, K.J. King and J.S. Liesman, 1990. Effects of dietary amines on small intestinal variables in neonatal pigs fed soy protein isolate. Journal of Animal Science 68, 363371. Haisch, M., N.K. Fukagawa and D.E. Matthews, 2000. Oxidation of glutamine by the splanchnic bed in humans. American Journal of Physiology 278, E593-E602. Higashiguchi, T., P-O. Hasselgren, K. Wagner and J.E. Fischer, 1993. Effect of glutamine on protein synthesis in isolated intestinal epithelial cells. Journal of Parenteral and Enteral Nutrition 17, 307-314. Higashiguchi, T., Y. Noguchi, W. O’Brien, K. Wagner, J.E. Fischer, and P.O. Hasselgren, 1994. Effect of sepsis on mucosal protein synthesis in different parts of the gastrointestinal tract in rats. Clinical Science 87, 207-211. House, J.D., B.N. Hall and J.T. Brosnan, 2001. Threonine metabolism in isolated rat hepatocytes. American Journal of Physiology 281, E1300-E1307. Jiang, R., X. Chang, B. Stoll, M.Z. Fan and D.G. Burrin, 2000. Dietary plasma protein reduces small intestinal growth and lamina propria cell density in early weaned pigs. Journal of Nutrition 130, 21-26. Jin, L., L.P. Reynolds, D.A. Redmer, J.S. Caton, J.S. and J.D. Crenshaw, 1994. Effects of dietary fiber on intestinal growth, cell proliferation, and morphology in growing pigs. Journal of Animal Science 72, 2270-2278. Jordinson, M., R.A. Goodlad, A. Brynes, P. Bliss, M.A. Ghatei, S.R. Bloom, A. Fitzgerald, G. Grant, S. Bardocz, A. Pusztai, M. Pignatelli, and J. Calam, 1999. Gastrointestinal responses to a panel of lectins in rats maintained on total parenteral nutrition. American Journal of Physiology 276, G1235-G1242. Kelly, D. and A.G.P. Coutts, 2000. Early nutrition and the development of immune function in the neonate. Proceedings of the Nutrition Society 59, 177-185. Kelly, D., T.P. King, D.S. Brown and M. McFadyen, 1991a. Polyamide profiles of porcine milk and of intestinal tissue of pigs during suckling. Reproduction, Nutrition, Development 31, 73-80. Kelly, D., J.A. Smyth and K.J. McCracken, 1991b. Digestive development of the early-weaned pig. 1. Effect of continuous nutrient supply on the development of the digestive tract and on changes in digestive enzyme activity during the first week post-weaning. British Journal of Nutrition 65, 169-180. Kelly, D., J.A. Smyth and K.J. McCracken, 1991c. Digestive development of the early-weanted pig. 2. Effect of level of food intake on digestive enzyme activity during the immediate post-weaning period. British Journal of Nutrition 65, 181-188. Kimura, R.E. 1996. Neonatal intestinal metabolism. Clinical Perinatology 23, 245-263. Kitt, S.J., P.S. Miller, A.J. Lewis and R.L. Fischer, 2001. Effects of diet and crystalline glutamine supplementation on growth performance and small intestinal morphology in weanling pigs. Journal of Animal Science 79, 148 (Abstr). Kollman K.A., E.L. Lien and J.A. Vanderhoof, 1999. Dietary lipids influence intestinal adaptation after massive bowel resection. Journal of Pediatric Gastroenterology and Nutrition 28, 41-45. Koruda, M.J., R.H. Rolandelli, D.Z. Bliss, J. Hastings, J.L. Rombeau and R.G. Settle, 1990. Parenteral nutrition supplemented with short-chain fatty acids: effect on the small-bowel mucosa in normal rats. American Journal of Clinical Nutrition 51, 685-689.

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Wu, G., N.E. Flynn, D.A. Knabe and L.A. Jaeger, 2000b. A cortisol surge mediates the enhanced polyamine synthesis in porcine enterocytes during weaning. American Journal of Physiology 279, R554-R559. Yen, J.T., J.A. Nienaber and W.G. Pond, 1987. Effect of neomycin, carbadox and length of adaptation to calorimeter on performance, fasting metabolism and gastrointestinal tract of young pigs. Journal of Animal Science 65, 1243-1248. Yen, J.T. and W.G. Pond, 1990. Effect of carbadox on net absorption of ammonia and glucose into hepatic protal vein of growing pigs. Journal of Animal Science 68, 4236-4242. Yen, J.T., J.A. Nienaber, D.A. Hill and W.G. Pond, 1991. Potential contribution of absorbed volatile fatty acids to whole-animal energy requirement in conscious swine. Journal of Animal Science 69, 2001-2012. Yoo, S.S., C.J. Field and M.I. McBurney, 1997. Glutamine supplementation maintains intramuscular glutamine concentrations and normalizes lymphocyte function in infected early weaned pigs. Journal of Nutrition 127, 2253-2259. Yu, F., L.A. Bruce, A.G. Calder, E. Milne, R.L. Coop, F. Jackson, G.W. Horgan and J.C. MacRae, 2000. Subclinical infection with the nematode Trichostrongylus colubriformis increases gastrointestinal tract leucine metabolism and reduces availability of leucine for other tissues. Journal of Animal Science 78, 380-390. Yu, Y-M., V.R. Young, R.G. Tompkins and J.F. Burke, 1995. Comparative evaluation of the quantitative utilization of parenterally and enterally administered leucine and L-[1-13C,15] leucine within the whole body and the splanchic region. Journal of Parenteral and Enteral Nutrition 19, 209215.

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13 Environmental requirements and housing of the weaned pig F. Madec, J. Le Dividich, J.R. Pluske and M.W.A. Verstegen

13.1

Introduction

In most pig producing countries, piglets are weaned between 17 and 30 days of age in specialised nurseries (Hendriks et al., 1998) at an age when most of their nutrient intake is still obtained from milk. Most of these nurseries are temperaturecontrolled and have pens with perforated floors (Hendriks et al., 1998). Weaning is commonly associated with mixing of piglets from different litters and sometimes with transportation from breeding to nursery units and, with in an abrupt change in both the pattern and the type of diet. The transition from nursery to consumption of solid feed usually results in a critical period of underfeeding during which piglets learn to eat and adapt to digest the solid feed (Le Dividich and Herpin, 1994). It follows that weaning imposes simultaneous social, nutritional and environmental stressors that affect the energy metabolism indeed the thermal requirements of piglets. The health of the weaned pig is very fragile. Weaning implies the withdrawal of milk protection at an age when the immune system of the pig is not yet fully developed (Dyrendhal, 1964). Diarrhoea leading to growth retardation and sometimes to mortality is a major clinical problem encountered at weaning. Various factors account for this complex disease. They include mainly nutrition (for details, see chapters 9 and 12) and housing through its environmental and hygienic conditions (van Beers-Schreurs et al., 1992; Madec et al., 1998). Because of the great number of piglets kept together in the same unit, non-optimal indoor climate and hygienic conditions and pen structure may lead to important economic losses. The objective of this chapter is to consider the housing requirements of the pig weaned between 3 and 4 weeks of age in the light of improving pig performance and health. We first assess the environmental requirements and factors accounting for changes associated with weaning. The second section focuses on the pen structure including flooring material, feeders and waterers, stocking rate and group size, which may influence piglet performance. Housing and management as causes of poor health of the pig are considered in the last section. Unless specified, in this chapter, piglets are weaned at 3-4 weeks of age and reared in groups on perforated flooring.

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13.2

Environmental requirements of the weaned pig

Ambient temperature (Ta) is the predominant component of the climatic environment. Requirement for temperature depends on several factors among which the amount of feed consumed and body thermal insulation is the most important. It is therefore relevant to assess the effects of weaning on feed consumption and its ensuing consequences on fat accretion and body thermal insulation. 13.2.1

Events related to weaning that affect thermal requirements

13.2.1.1 Feed intake At weaning between 3 and 4 weeks, most piglets have consumed very little solid feed and hence they are unfamiliar with the weaning diet. It follows that feed intake of piglets abruptly deprived of liquid milk provided by their dam pre-weaning and offered a pelleted solid feed post-weaning is often very limited. Both the extent and the duration of underfeeding vary enormously (Le Dividich and Sève, 2001). However, the level of metabolizable energy (ME) intake attained at the end of the 1st post-weaning week approximates 70% of the pre-weaning milk ME intake. In fact, the pre-weaning ME intake is only attained by about 2 weeks after weaning. Attempts to reduce both the extent and duration of the underfeeding period can be achieved by providing the piglets with liquid feed (for details, see Chapter 6). Provision of liquid feed certainly attenuates the extent of underfeeding, but not completely. However, this practice induces feed wastage, needs to be carefully monitored for hygiene reasons, and requires sophisticated dispensers. Together, these would suggest that a period of underfeeding following weaning is practically unavoidable. 13.2.1.2 Fat metabolism and effects on body thermal insulation Fat is a good insulating material. Its heat conductivity is three times lower than that of water. Subcutaneous fat provides thermal insulation to the pig. At weaning, body composition changes markedly towards a temporary decrease in fat content. At least two factors account for this decrease in body fatness. First, mixing of unfamiliar pigs at weaning results in vigorous fighting associated with the formation of a new social order and, in a transient increase in heat production (Heetkamp et al., 1995). When the effects of mixing and transportation are combined, a slight increase in heat production is measurable for up to 5-7d post transportation (del Barrio et al., 1993). Second, and most importantly, due to low feed intake, most of the newly-weaned pigs are in negative energy balance during a period of 4-7 days following weaning. However the nitrogen balance remains positive and is less dependent on the environmental conditions (Le Dividich et al., 1980; Close and Stanier, 1984b; Bruininx et al., 2002). It follows that the energy required for maintenance, physical

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activity and for protein synthesis involves a mobilisation of body fat (Whittemore et al., 1978). The rate of mobilisation depends on both level of feeding and environmental temperature, it being more pronounced at low feed intake (Close and Le Dividich, 1984) and at low environmental temperature (Le Dividich et al., 1980). The extent to which this loss of body fat affects the decrease in body thermal insulation is therefore variable, but depends on the available body fat stores at weaning. In pigs of low weaning weight (4.55 kg at 21d of age), the rate of fat mobilisation can be as high as 32% during the first week following weaning (Sloat et al., 1985). According to Fenton et al. (1985), the decline in backfat thickness can be as high as 33% in the 1st week following weaning at 2 weeks of age. These data provide evidence that the body thermal insulation is reduced and leads to an increased susceptibility of the weaned pig to cold. This is illustrated by the amount of extra heat produced in the cold, i.e., 18kJ/kg 0.75 .°C-1, which is 50% higher than in a 60-kg pig (Le Dividich et al., 1998). With the low feed intake, this has major impacts on the thermal requirement of the piglet at weaning. 13.2.2

Ambient temperature

Because of the transient effect of weaning of feed intake, two periods are examined (Le Dividich and Herpin, 1994) (i) the critical period of 1 to 2 weeks following weaning, representing the period of underfeeding and corresponding to the time required to attain the pre-weaning level of ME intake, and (ii) the post-critical period, i.e., when regular feed intake is established. 13.2.2.1 The critical period The lower critical temperature (LCT) is defined as the ambient temperature at which, for a given ME intake, energy retention is maximal. LCT corresponds to the optimum temperature at weaning inasmuch as the main goal is to minimise heat loss to avoid excessive loss of body fat and hence minimise the decrease in thermal insulation. At weaning, the combination of a low feed intake and a reduced body thermal insulation (Figure 13.1) results in a temporary increase in LCT from 22-23°C at weaning to 26 to 28°C during the first post-weaning week (Le Dividich et al., 1980; McCracken and Caldwell, 1980), decreasing thereafter to 23 to 24°C in the second post-weaning week (Close and Stanier, 1984b; McCracken and Gray, 1984). In addition, it should be noted that maintaining the ambient temperature at or above the LCT during the critical period of weaning helps to prevent a possible overconsumption occurring sometimes after piglets start to eat solid feed, thus limiting the consequences of post-weaning digestive and (or) enteric disease disturbances.

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Critical temperature, °C

30 28 26 24 22 20 18 2000 1500

12 10

1000

8 500

6 4

Pre-weaning week

2 Birth 1

2

ME intake, kJ/kg 0,75/d

Body fat content, %

14

0 1

3 5

Weaning at 21 d of age

7

14

21

28

Days post-weaning

Figure 13.1. Diagrammatic representation of the effects of the abrupt decline in feed intake and of the reduction of body fat content occuring at weaning on the lower critical temperature of piglets raised on perforated floor.

13.2.2.2 The post-critical period Once regular feed intake is well established and inasmuch as there is no health problem, the air temperature of the nursery can be rapidly reduced in relation to the increase in feed intake (Figure 13.1). Most studies suggest a progressive decrease in ambient temperature by 2 to 3°C/week until the temperature to be maintained in the finishing house is reached (Le Dividich, 1981; Close and Stanier, 1984a; Feenstra, 1985). In addition, the weaned pig is to some extent able to compensate for a sub-optimal environment by increasing its voluntary feed intake. The adjustment in feed intake is rapid since being stabilised within 6d after exposure to “cold” (Verhagen et al. 1988). This is in agreement with the fact that within the 25 to 18-19°C temperature interval, growth rate remains practically constant, with however an increase in feed to gain ratio (Fuller, 1965; Hata et al., 1986; Rinaldo and Le Dividich, 1991). However, an abrupt reduction in the nursery temperature after the critical period appears to be detrimental. For example, an abrupt 5°C

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decrease of ambient temperature on d7 post-weaning is found to depress overall growth rate by 21% and feed efficiency by 10% (McConnell et al., 1987). 13.2.2.3 Ways to reduce heating costs Because of the relatively high ambient temperature considered essential for optimal performance, the weaning house requires considerable heating. Consequently, several ways of reducing the heating requirement while maintaining pig performance at an acceptable level have been investigated. These include the provision of a microenvironment, bedding and, reduction in nocturnal air temperature. Provision of a microenvironment A simple way to save energy is to create a microenvironment for the pig within the weaning house. Use of covers is an alternative that offers the possibility to reduce the heating cost. Pigs provided with hovers or covers at moderate air temperatures (18 to 20°C) had performance similar to those maintained at recommended temperatures (Shelton and Brumm, 1983). Similar results are recorded in Denmark (Feenstra, 1985) where systems with a covered area and two-thirds solid floor have become increasingly popular. The hovers reduce draughts and, to some extent, trap the heat produced by the pigs. Provision of bedding Provision of bedding (straw, sawdust, wood shavings) lowers LCT. Verstegen and van der Hel (1974) calculated the LCT of groups of 40-kg pigs to be 7-8°C lower on straw than on concrete slats. From preference studies, Morrison et al. (1987) calculated that, compared to perforated metal, weaned piglets on bedded solid floor required 5.8 °C less Ta (Table 13.1). Similar performance is reported when comparing weaned pigs on solid bedded floors (temperature initially 23°C gradually decreasing to 16°C by the end of the weaner period) to those on metal slatted floor with temperature initially 27°C decreasing gradually to 18°C) (Kelly et al., 2000), while improving the welfare of piglets. In practise, pigs on solid bedded

Table 13.1. Difference in effective ambient temperature of various floors compared to solid bedded floor. Type of floor

Difference in effective environmental temperature (°C)

Bare solid floor Perforated metal Raised rubber-coated floor

+ 2.8 + 5.8 + 3.0

(After Morrison et al., 1987)

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floors require 4 to 6 °C less than those on perforated floor. However, the extra cost associated with bedding (bedding, extra labour) must be compared to that of extra heating. Reduction of the nocturnal temperature Another alternative is based on the fact that the pig displays a marked circadian variation in metabolic rate, which is lower during the nighttime than during the daytime. This variation in metabolic rate results in a variation of the LCT, being lower during the night than during the day (van der Hel et al., 1985). Compared with a constant temperature, a 4 to 9°C reduction in nocturnal temperature (RNT) does not affect the pig’s performance (Table 13.2) while decreasing markedly heating cost (Shelton and Brumm, 1988). No adverse consequence during the finishing phase is reported. However, pigs on a RNT treatment tended to have a greater incidence and severity of scouring (Swinkels et al., 1988). Similarly, data obtained by Rinaldo et al. (1989) also indicated that within the 12 to 30 kg body weight interval, pigs subjected to a 8°C reduction in nocturnal temperature (22 → 14°C) had similar average daily gain (ADG) than those maintained at a constant temperature of 22°C. However, the RNT treatment was associated with an overall increase in average daily feed intake (ADFI) with a greater proportion (38 vs 32%) being consumed during the nighttime. Also, pigs on the RNT treatment huddled more during the nighttime, indicating an activation of the thermoregulatory behaviour. In practise, environmental conditions are not constant. It is usually assumed that performance of pigs exposed to daily air temperature fluctuation is equivalent to the average of that fluctuation. Data of Kurihara et al. (1996) obtained in pigs aged 53 to 62d suggest that a diurnal range of ±3°C around the mean is acceptable (Table 13.3). A higher range (± 7°C) results in a significant decrease in performance.

Table 13.2. Effect of reduced nocturnal temperature (RNT) during the nursery phase on the pig performance1. Treatment

Control (°C)

RNT (°C)

ADG, g ADFI, g Feed:gain (kg/kg)

340 530 1.57

360 570 1.61

1There

were 256 pigs per treatment, initial body weight = 6.7Kg. They were exposed to either a constant regime (30°C for the first week and then decreased by 2°C per week for four weeks) or a cycling daily temperature regime (the same temperature as the control during the first week, but night temperature lowering to 22°C on week 2 and further by 2°C per subsequent week. (After Shelton and Brumm, 1988)

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Table 13.3. Effect of diurnal variation in ambient temperature on piglets performance (initial age, 53-62 days). Ambient temperature (°C)

21

21±31

21±62

ADG Feed intake, g Feed: gain (kg/kg)

682 1330 1.95

660 1300 1.97

602 1150 1.95

1

12h at 18°C and 12h at 24°C 12h at 15°C and 12h at 27°C (After Kurihara et al, 1996)

2

13.2.3

Relative humidity and ventilation

Little attention has been paid to the effect of relative humidity (RH) and air velocity on the performance of the weaned pig. However, relative humidity is expected to have little influence on the performance of the weaned pig maintained within thermal neutrality. For example, at 24°C, similar performance is obtained at 60 and 90% RH (Bresk and Stolpe, 1988). In contrast, in growing pigs, a 10% change in RH, between 45 and 90% induced a 24 g/d reduction in feed intake with no change in feed efficiency (Massabie et al., 1997). Ventilation serves two major functions: (i) removal of air humidity and noxious gases, and (2) assist with the control of the temperature of the animal house. Ventilation determines air velocity at the pig level. As such, it plays an important role in the rate of heat loss. Using the operant conditioning technique, Verstegen et al. (1987) found that increasing the air velocity from 8 to 40cm/s resulted in a 3.8°C increase in the preferred temperature (Table 13.4). Results of Hacker et al. (1979) indicate that below the LCT, an increase in air velocity from 0 (still air) to 50 cm/s resulted in a 15% decrease in ADG and a 23% decrease in gain to feed

Table 13.4. Effect of air velocity on preferred temperature by the 14-20kg pig. Air velocity(cm s-1)

Preferred temperature (°C)

8 25 40

17.9 20.5 21.7

(After Verstegen, et al., 1987)

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ratio in pigs weaned at 21 to 25 d of age. Similarly, Riskowski and Bundy (1990) calculated that during the second post-weaning week within the temperature range of 24 to 35°C, each 10 cm/s increase in air velocity was associated with a 25 g/d decrease in growth rate. Because ventilation accounts for most (80 to 90%) of the heat loss of the weaning house, the current recommendation during cold weather is “as low ventilation as possible”. Studies conducted at the University of Minnesota (Boedicker et al. 1984; Jacobson et al., 1985-86), indicated that ventilation rate lower that the recommended minimum had no detrimental effect on performance and health despite 2-3 times higher concentrations of ammonia and carbon dioxide. In practice (Ritz, 1971), recommendations for ventilation rate during winter are 0.35-0.40 m3 h-1 kg-1 body weight (BW). During summer, to remove heat and water vapour produced by the pigs and hence to avoid excessive rise in temperature and humidity, recommendations for ventilation are 1.60 - 2.10 m3 h-1 Kg-1 bodyweight. Effects of noxious gases on performance have been the subject of an excellent review by Wathes (2001) and will not be discussed here. 13.2.4

Lighting

Lighting as an environmental factor has received little attention. Bears et al. (1974) suggested that complete darkness reduces the agonistic interactions at weaning. However, constant illumination of 5 or 100lx has no effect on the behaviour (included the feeding behaviour) of the newly weaned pig (Christison, 1996). In contrast, photoperiod may have effects on performance. Bruininx et al. (2002) reported that ADFI is 16 and 38% enhanced during the 1st and the 2nd postweaning week, respectively, in pigs subjected to a 23:1h lighting schedule compared to 8:16 schedule. However, more data are necessary to substantiate these results. The EU regulation mentions that pigs should be exposed to daily 8 h lighting of at least 40lx. 13.2.5

Effects of non-optimal climate on performance

The effects of cold and high ambient temperature on performance are shown in Figure 13.2. Low ambient temperature during the critical period of weaning is the most detrimental to performance mainly because feed intake is not increased. Pigs maintained at 21°C during the first 10 post-weaning days are found to grow 33% less on 53% more feed than those at 29°C (Maenz et al.,1994). Once regular feed intake is established, the weaned pig is able, to some extent, to increase its feed intake to compensate for a low temperature. However, maximum intake capacity is reached at 18-19°C (Collin et al., 2001). It follows that at lower temperature, ADG decreases by about 13g °C-1 coldness, and feed conversion ratio increases by 0.04 unit °C-1 coldness (Le Dividich and Noblet, 1982; Close and Stanier, 1984a).

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In addition, draughty conditions markedly affect performance. Draughts have enormous effects on the behaviour of the piglets (Scheepens et al., 1991), resulting mainly in an increased activity and therefore in an increase in the activity-related heat production (Verhagen, 1987). Negative effects of draughts are the most detrimental in the immediate post-weaning period. During this period, a 106 g/d decrease in growth rate was found by Scheepens et al. (1991) due to draught, the decrease amounting to 155 g/d when draughts were superimposed on fluctuating temperature (25/15°C) (Verhagen, 1987).

700

ADG, g/d

600 500 400 2.5 2

FCR, kg/kg

1.5 0

1 0

10 20 30 Temperature, °C

40

Fuller, 1965 Rinaldo and Le Dividich, 1991 Hata et al, 1986

Figure 13.2. Effect of environmental temperature on the performance of weaned piglets.

At high ambient temperature, performance declines as a result of a decrease in feed intake. During the overall post-weaning period, feed intake starts to decline markedly at Ta higher than 25°C (Collin et al., 2001), the decline being dependent on the pig body weight. For a 20-kg pig, ADFI decrease is in the range of 28-33 g. °C-1, between 25 and 32-35°C, but may be as high as 42g.°C-1 (Sugahara et al., 1970). This reduction in ADFI, leads to a decrease in ADG of 15-21% between 25 and 3133°C (Rinaldo and Le Dividich, 1991; Collin et al., 2001), with, however, no detrimental effect on feed conversion ratio.

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13.3

Pen structure

The major features of the pen structure that are likely to influence the environmental and housing conditions of the weaner pig include flooring material, feeders and waterers, stocking density and group size. 13.3.1

Flooring materials

There are many types of flooring materials available for nurseries, with fully or partly slatted (or perforated) floors providing maximum manure throughput being the most common types (Hendriks et al., 1998). Potential advantages are easiness of clean, reduced labour and improved hygienic condition. Slatted or perforated floors must be designed to minimise foot and claw injuries while facilitating cleaning. Based on the morphology of the pig foot (Mitchell and Smith, 1978) and on the occurrence of injuries (Vellenga et al., 1983), a slot width of 10-15 mm is acceptable for pigs over 5-6 kg. Similar performance is usually reported on bedded solid floors and slatted or perforated floors (Schneider and Bronsch, 1974; Danielsen and Nielsen, 1978; Kelly et al., 2000) when ambient conditions are appropriate. However, there is a trend toward a reduced performance for pigs on aluminium floors (Wilson et al., 1977; Orr et al., 1978). On the basis of preference studies (Farmer and Christison, 1982; Pouteaux et al., 1983/84) and of the occurrence of foot lesions, plastic-coated expanded metals are superior to other perforated flooring materials. 13.3.2

Feeders and waterers

Ideally, nursery pigs should be equipped with feeder space that allows at least half of the pigs in the pen to eat at any one time, however this scenario is not always attained and the issue of the ‘correct’ number of pigs per feeding space is always a topic of discussion and contention. Feeding space is dictated by a number of factors, one of which is the width of the pig; the relationship between feeding space per pig and the pig’s physical conformation has led to the development of equations to describe the minimum width needed in a feeder for a pig to eat. Baxter (1989) described the equation: W = 61 x BW0.33, where W = width of the pig at the shoulder (in mm) and BW is bodyweight (kg), that represents the minimum feeding space. Practically, a margin of 10% to address individual pig variation should be used. Using these calculations, therefore, a pig weighing 10 kg requires a minimum feeder space of 130 mm. Weanling pigs are commonly offered their feed from a partitioned linear (trough) feeder that has a feeding pan in the front, and in which the rate of feed flow from the hopper can be adjusted to prevent feed wastage. Single-space or wet/dry feeders

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are generally not recommended for weanling pigs due to perceived problems of access and excessive feed wastage, however Pluske and Williams (1996) reported no difference in production indices in pigs fed from a linear (trough) feeder or a single-space feeder between 28 and 56 days of age. However, pigs offered a singlespace feeder with a nipple waterer enclosed (‘wet/dry’ feeder) grew slower and wasted more feed than pigs offered feed from the linear feeder or the ‘dry’ single-space feeder. Adequate water intake is essential in the immediate post-weaning period (see Chapter 6 by Brooks and Tsourgiannis), so waterers (drinkers) need to be accessible, working, kept clean and have the correct flow rates. Adjustable-height nipple drinkers are generally preferred over cup waterers (bowls), at least in the initial period after weaning. One nipple drinker should be provided for every 1015 pigs, however extensive pens (eg, straw-based shelters) can have 1 watering point per 20-25 pigs seemingly without effects on production. The height of the waterer should be adjusted to that of the pig’s back, and water pressure at the nipple (drinker) should be limited to 20 pounds per square inch and 500-600 ml per minute. 13.3.3

Stocking densities

Floor space per pig is usually based on the space required for sternum and fully recumbent resting positions. For a fully recumbent position, the relationship between space allowance (A, m2) and BW (kg) is expressed as A = 0.047 x BW 2/3 (Petherick and Baxter, 1982). According to these authors, adequate space allowance for a 6.8kg pig is 0.17m2 increasing to 0.44m2 for a 27-kg pig. From literature data, the effects of space allowance (S, m2) on ADG and ADFI can be predicted from the following equations (Kornegay and Notter, 1984): ADG (kg) = 0.261 + 0.800 S - 1.051 S2 (R2 = 0.97) ADFI (kg) = 0.533 + 1.125S - 1.383 S2 (R2 = 0.97) In practise, within the body weight range of 5-6 to 25-30 kg, current recommendations are 0.25 to 0.30 m2 per pig on perforated floors. A reduced space area leads to a reduced feed intake and hence growth rate. During the overall postweaning period (from 21 to 63d of age), reducing the space allowance from 0.24 to 0.18 m2 results in a 13% reduction in both ADFI and ADG (Le Dividich, 1979). However, feed conversion ratio is not usually affected. Less information exists on the possible interaction between the type of flooring (bedded solid vs perforated floors) and the space requirement. However, it is assumed that pigs on bedded solid floors require some 20-25% more space.

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13.3.4

Group size

There is a strong evidence that group penning of pigs may have a detrimental effect on feed intake and performance. During the overall post-weaning period, increasing the number of pigs from 8 to 24 per pen at constant space area of 0.21m2 reduced ADFI and ADG by 13 and 12% respectively (McConnell, et al., 1987). Large group sizes (100 or more per pen) are an increasingly feature in production, especially in the USA and Australia. In Australia, pigs are sometimes weaned directly into straw-based shelters (‘hoops’) in groups of up to 400. However, within the body weight range of 5 to 15 kg, Wolter and Ellis (2002) consistently reported a small, negative effect of increasing group size from 20 to 100 pigs per pen on growth rate after weaning, with the extent of depression in ADG and ADFI ranging from 4.3 to 6.6% and from 5.1 to 6.6%, respectively. Using the prediction equations of Kornegay and Notter (1984) obtained at constant floor area per pig, ADG and ADFI decrease by 3.7 and 9.2 g, respectively, per each additional pig. However, in their data set, only data from 4 studies were used and the range of group size (from 3 to 15) was rather narrow. In contrast, McConnell et al. (2001), in an experiment using 1,280 pigs held in groups of 10, 20, 30, 40 and 60 from weaning at 28 days of age to 10 weeks of age, reported no significant differences between treatments in performance indices. Recently. Turner et al. (2003), using larger group sizes (3120), re-calculated Kornegay and Notter’s prediction equations. They are (N = number of pigs per pen): ADG (g) = 416 - 0.36N (R2 = 0.968) ADFI (g) = 681 - 0.51N (R2 = 0.978), indicating that the extent of decrease in both ADG and ADFI is much lower, amounting to 0.36 and 0.51 g, respectively, per each additional pig. Of importance is to notice that group size has no effect on both feed conversion ratio and on the within-group variation in ADG (Giles et al., 2001; Turner, et al., 2003). Furthermore, many other factors influence the relationships between group size and performance post-weaning, of which feeder space, feeder design and water supply are influential. Because mixing of litter is common at weaning, the question that arises is how should pigs be grouped? Grouping by weight has been assumed to be beneficial to the uniformity of the group. However, the effects of grouping pigs by weight on performance are still unclear as illustrated by data of Francis et al. (1996) and Bruininx et al. (2001), which failed to exhibit any difference in performance of uniform and heterogeneous groups. From an economic standpoint, in deciding the group size, the extra cost of housing must be compared to that of the reduction of performance.

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13.4

Housing as a cause of poor health of weaned pigs

Enteric disease is the most common clinical problem encountered at weaning. Usually, it peaks around 10d post-weaning, but its occurrence is closely dependent on the herd. In some herds, piglets exhibit diarrhoea immediately post-weaning, in others, on week 3 or 4 after weaning corresponding to a change in feed (Madec and Leon, 1999). Feed additives including antibiotics, pro-or pre-biotics, and trace elements (eg, Zn, Cu) to some extent, control it. In all cases, diarrhoea results in a loss of ADG, as illustrated by the negative relationship between diarrhoea score and ADG (r= -0.47 and -0.39 in the 1st and 2nd post-weaning week, respectively (Madec et al., 1998)). Various factors account for this complex disease among which both nutrition (for details, see Chapter 9) and housing conditions are the most important. 13.4.1 Evidence that housing conditions predispose pigs to digestive disorders Evidence for the implication of the environment and housing in the development of enteric disease is provided by experiments described by Madec and Leon (1999). In brief, from 5 pig farms exhibiting high occurrence of diarrhoea, a sample of 2830 piglets from each herd was moved on the day of weaning to experimental facilities at the Pig Veterinary Research Institute (Ploufragan). In these facilities, hygienic and climatic conditions were of a very high standard (all-in / all out management, no bacterial growth on Agar plates after cleaning operations, air filtration). In both farms and experimental facilities, pigs were reared on perforated floors and fed ad libitum the same diet. Enterotoxigenic E coli were found in pigs of both locations, however, no mortality occurred in the experimental facilities whereas a rate of 2.1 to 4.5% was recorded in pigs weaned in farms (Table 13.5). Also, pigs weaned on farms grew on average 30% less and exhibited a higher occurrence of diarrhoea. In another study, using a similar protocol (Kerebel et al., 2000), feeding and drinking behaviour of piglets were video-recorded during the first post-weaning week. Again, the occurrence of diarrhoea was much higher in pigs weaned on farms. In addition, both feeding and drinking frequencies were higher in pigs moved to the experimental facilities. To some extent, similar results are also obtained when comparing all-in/all-out nursery to a continuous flow nursery, in that overall performance and health are markedly improved in the former facility (Schneider and Bronsch, 1973) Together, these demonstrate the role of housing (in a broad sense) on the occurrence of diarrhoea and suggest that (i) highly hygienic and climatic conditions of the nursery and that (ii) early and high feed and water intake, do not allow the expression of the most common pathogens.

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Table 13.5. ADG, diarrhoea incidence and mortality of piglets selected at random on farms severely affected with post-weaning diarrhoea and weaned either on farm or in experimental facilities. Number of pigs

Diarrhoea (% of pigs)3

ADG (g)

Mortality (%)

Farm Farm1

Exp. F2

Farm

Exp. F

Farm

Exp. F

Farm

Exp. F

A B C D E

30 28 30 30 30

44.2 47.5 60.0 31.4 42.6

3.3 0 6.6 0 3.3

326 320 284 346 351

430 445 429 515 510

4.2 2.6 4.5 2.1 3.0

0 0 0 0 0

120 116 155 142 198

1Piglets 2Piglets

weaned on farm from the corresponding farm that were transferred to experimental facilities

(Exp. F) 3Piglets

were daily examined for diarrhoea score ranging from 1 to 5. Faeces scored at 4 and 5 were considered diarrhoeic. (After Madec and Leon 1999)

13.4.2

Impact of non-optimal indoor climate on the pig’s health status

Post-weaning gastrointestinal disturbances can be triggered or at least accentuated by adverse climatic conditions. An increased incidence of diarrhoea at chronic moderate cold temperatures (18-20 °C) has been observed by Le Dividich et al. (1980), Close and Stanier (1984a) and Feenstra (1985). More importantly, acute cold exposure (12 increasing to 18°C or 18 decreasing to 12°C) results in an unacceptable 14-15% rate of mortality (Feenstra, 1984). Acute and continuous changes in ambient temperature may also be detrimental to the health of piglets. Le Dividich (1981) observed a greater incidence of post-weaning diarrhoea in piglets kept in a continuous (hourly) fluctuating temperature (23.5±3°C) compared to a constant temperature (23.5±0.5°C). In addition, the detrimental effect of a continuous fluctuating temperature is particularly high during the 1st postweaning week. Also, reduced nighttime temperature appears to impose an additional stress on sick pigs (Brumm et al., 1985). Intermittent exposure to draught results in more coughing, sneezing and diarrhoea while decreasing growth rate (Scheepens et al., 1991). Compared with constant temperature, fluctuating temperatures have no effect on antibody level of 30-kg pigs challenged with Haemophilus pleuropneumoniae. However, it is increased when draughts superimpose fluctuating temperatures (Kreukniet et al., 1990).

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Whereas it is clear that adverse climatic conditions are detrimental to the health state of the weaned piglet, the accounting mechanisms are, however, less obvious. For example, severe cold stress increases the susceptibility of the new-born (Sarmiento, 1983) and the newly weaned piglet (Armstrong and Cline, 1977) to enterotoxigenic E. coli diarrhoea. However, when piglets challenged with enterotoxigenic E. coli are exposed to moderate cold stress, only those fed ad libitum suffer postweaning diarrhoea (Wathes et al., 1989). The literature review of Kelley (1980) indicated that inadequate environment can affect the immune function of the pig. Blecha and Kelley (1981) reported that exposure to severe cold (0 vs 25°C) for 4 days caused an increase in circulating γ globulin and in antibody titer in the weaned pig. However, Crenshaw et al. (1986) and Bonnette et al. (1990) failed to demonstrate any effect of moderate cold exposure (18-19 vs 25-30 °C) on the systemic immunological state. Nevertheless, in field studies, air quality (temperature, humidity, ventilation) at entry in the nursery is an important risk factor associated with post-weaning digestive disorders (Madec et al., 1998), suggesting that it is difficult to explain the post-weaning diarrhoea by a single environmental factor. 13.4.3 Multifactorial nature of post-weaning disorders: risk factors associated with housing and management From the above, it is clear that several factors interact in the onset of diarrhoea. In an attempt to identify the risk factors associated with housing, Madec et al. (1998) conducted a survey involving 106 commercial herds and more than 12,000 pigs. At least 13 risk factors were identified, among which the most important (expressed as Odds-Ratios) were: feed intake during the 1st post-weaning week, hygiene of the nursery, air quality, age and body weight at weaning. In this survey, environmental temperature does not appear to be a risk factor as recorded data were close to recommended values. Other factors have been identified. For example, a perforated floor in the dung area is less risky than a solid floor (Rantzer and Svendsen, 2001). However, it is out of the scope of this single chapter to discuss all risk factors. They are listed in Table 13.6 together with the corresponding preventive measures. It is, however, relevant to notice that a high feed intake before and immediately after weaning is a major factor that minimises the risk of diarrhoea. As mentioned in Chapter 8, early post-weaning feed intake is considered to be an important factor in the pathogenesis of the post-weaning diarrhoea that is associated with villous atrophy (Pluske et al., 1997). A high creep feed intake before weaning is, to some extent, consistent with both a higher weaning weight and a higher feed intake post-weaning (Bruininx et al., 2002). Both weaning weight and ADG (and hence feed intake) during the 1st week post-weaning are also the best predictors of subsequent performance, accounting for about 80% of body weight on day 20 after weaning (Miller et al., 1999). Conversely, post-weaning diarrhoea is usually attenuated by feed restriction (Rantzer et al., 1995). Again, this demonstrates how complex the aetiology of post-weaning enteric disease is.

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Table 13.6. Risk factors to post-weaning digestive disorders and corresponding preventive measures. Risk factors

Less risky value of the factor

Relation with the disorders1

• Hygiene status in the nursery at the arrival of the piglets.

All-in/all-out; cleaning; empty pit below

↓

slatted floor; disinfection; dry floor; warm (24°).

• Creep-feed intake/piglet last week

> 470 g.

↓

NH3: < 10 ppm; CO2: < 0,15% + average

↓

prior to weaning (g).

• Air quality all along the postweaning period

air speed: < 0.10 m/sec; no draught; no turbulence of the flow; no air flowing out of the slatted floor; RH: < 85%.

• Temperature (2) • 1st wk PW • 2nd wk PW • Water supply (2)

28°C (weaning at 4 weeks)

Not determ.

27°C

Not determ.

Waterers: easy access, to operate, to

↓

maintain clean, potable water. > 1700 g

↓

≥ 28 days

↓

≥ 9 kg

↓

<4

↑

Number of piglets/pen.

< 13

↑

Space available at the feeder

≥ 8 cm per pig

↓

Stocking density (pigs/m2)

≤3

↓

Level of concurrent respiratory

absence of cough

↑

disorders.

average sneezing counts: n < 2 (for 100

• Feed intake/piglet during the 1st post weaning week.

• Age at weaning (days). • Live weight at weaning (kg). • Number of litters origin per pen (post-weaning room).

• • • •

pigs, mean of 3 counts of 2 min.)

• Sow / person • Overall farm health level (PW digestive disorders excluded)

≤ 80

↓

Score calculated on the basis of annual

↓

mortality rate in growing-finishing pigs and in sows, occurrence of influenza-like syndromes and PRRS infection in growing-finishing pigs, diarrhoea prior to weaning, and diarrhoea during growingfinishing phase.

1Arrows

indicate the relation between the factors and the risk of disease onset (e.g.; the risk of disease

onset increases with decreasing level of hygiene or decreases with the increase in stocking density etc...). (After Madec et al., 1998).

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13.4.4

Integrating the risk factors to improve health

It is evident that the occurrence of post-weaning diarrhoea is the result of the cumulative effects of several risk factors. Therefore the approach first implies the identification of these risk factors. The situation is then improved step-by-step in an attempt to move towards a less risky profile and a subsequent reduction in digestive disorders. An example of a simulation conducted in a severely affected herd is provided in Figure 13.3. An initial follow-up observation of the batch of piglets to ascertain the situation regarding health provides the initial risk factors profile of the herd (to be simple, only 8 categories of risk factors are considered). The initial profile (left column of Figure 13.3) indicates several major failures (level 1) regarding hygiene, air quality, etc. Multivariate analysis of the risk factors profile gives the position (ie, in the ‘at risk’ or ‘secure’ zone) of the herd on the map of correspondence analysis, as shown in the left part of Figure 13.3. Different technical solutions can be proposed to attenuate the risks. For example, adoption of a strict all-in/all out management system with other components of hygiene, including cleaning and disinfection remaining unchanged, might be sufficient to attain level 2 for the hygiene risk factor, which moves the herd in position 1 on the map of correspondence. However, despite a great management effort, migration towards the target secure area is not significant. Improving the overall category of factors associated with hygiene moves the farm on position 2 on the map, still far from the target area. Assuming now that two risk factors, ie, hygiene and air quality, are simultaneously improved, this allows the producer to attain the secure level of 4 for both. Because the weight of these two factors is high (as attested by their Odd-Ratios), the herd position migrates to position 4 on the map and, a significant improvement of health should be expected. In fact, any change in one risk factor is dependent on values of other risk factors. When all risk factors are at their most secure level, the herd is moved to the position 6 on the map. In practice, it is difficult to attain this situation, however good results are obtained before attaining this ideal stage. Together, these indicate that because of post-weaning diarrhoea is multifactorial in nature, simultaneous reduction in risk factors associated with housing and management is necessary to improve the pig health.

13.5

Conclusion

The period following weaning between 3 and 4 weeks of age is characterised by rapid changes in environmental requirements of the piglets caused by changes in feed intake, metabolism and tissue thermal insulation. During the first 10-14 days after weaning climatic conditions are very important for a successful weaning and a stable ambient temperature of 26-28°C is recommended for piglets penned on perforated floors. Once regular feed intake is established the ambient temperature

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“secure” area

“at risk” area

=Target area

6

4 5

2 3 1 The different farm profiles 1 Risk factors

I : initial

1

2

3

4

5

62

Hygiene Air quality Creep feed intake Feed intake 1st wk PW Weaning age Man power/sow Respiratory. diseases Overall farm health state

1 1 1 1 2 1 1 2

2 1 1 1 2 1 1 2

4 1 1 1 2 1 1 2

1 4 1 1 2 1 1 2

4 4 1 1 2 1 1 2

4 4 3 3 2 1 1 2

4 4 4 4 3 3 1 4

1

Categorial risk factors with levels ranging from 1 to 4 (i.e;, creep feed intake < 190g/pig during the week preceding weaning corresponds to level 1; level 4 corresponds to creep feed intake >490g/pig. Respiratory diseases is assumed to remain unchanged for the six simulations 2 Profile 6 on the right side of the table corresponds to the less risky levels for all the risk factors Figure 13.3. Diagrammatic illustration of the multifactorial efforts needed to reduce the post-weaning digestive disorders (simulation based on the map of correspondence analysis described by Madec et al., 1998).

can be gradually decreased by 2-3°C per week until the temperature of the finishing house is attained. Effects of the pen structure, including flooring materials, feeders and waterers, stocking density and group size, on performance have been assessed. Finally effects of climatic and hygienic conditions and management of the nursery on the onset of digestive disorders are considered. It is suggested that disease prevention should be directed towards provision of zootechnical profiles that reduce risk factors. Attention to optimal hygiene, feed intake immediately post-weaning,

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strategic animal movement, thermal environment and air quality all contribute to reduce the risk of disease.

References Amstrong, W.D. and T.R. Cline, 1977. Effect of various nutrient levels and environmental temperatures on the incidence of coli bacillary diarrhea in pigs: Intestinal fistulisation and titration studies. Journal of Animal Science 45, 10421-1050. Baxter, S.H., 1989. Designing the pig pen. In: J.L. Barnett and D.P. Hennessy (editors), Manipulating Pig Production II. Australasian Pig Science Association, Werribee, Australia, pp. 191-206. Bears, W.H., R.R. Hacker and T.R. Batra, 1974. Some effects of complete darkness on. young piglets. Journal of Animal Science 39, 153 (Abstr.). Beers-Scheurs, van H.M.G., L. Vellenga, Th. Wensing and H.J. Breukink, 1992. The pathogenesis of the post-weaning syndrome in weaned piglets. A review. Veterinary Quarterly 14, 29-34. Blecha, F. and K.W. Kelley, 1981. Effects of cold and weaning stressors on the antibody-mediated immune response of pigs. Journal of Animal Science 56, 396-400. Boedicker, J.J., L.D. Jacobson, J.W. Rust and J.M. Roach, 1984. Animal performance and environment related effects of ventilation rate and temperature for a swine nursery. ASAE Paper N° 84-504. ASAE, St Joseph, MI. Bonnette, J.J., E.T. Kornegay, M.D. Lindeman and C. Hammerberg, 1990. Hormonal and cellmediated immune response and performance of weaned pigs fed four supplemental vitamin E and housed at two nursery temperatures. Journal of Animal Science 68, 1337-1345. Bresk, B. and J. Stolpe, 1988. Effect of high and medium relatives humidities on live weight gain of weaned piglets exposed to different temperatures. Monatshefte für Veterinärmedizin 48, 191193. Bruininx, E.M.A.M., C.M.C. van der Peet-Schering, J.W. Schrama, P.F.G. Vereijken, P.C. Vesseur, H. Everts, L.A. den Artog and A.C. Beynen, 2001. Individually measured feed intake characteristics and growth performance of group housed weanling pigs: effects of sex, initial body weight, and body weight distribution within groups. Journal of Animal Science 79, 301-308. Bruininx, E.M.A.M., M.J.W. Heetkamp, D. van den Bogart, C.M.C. van der Peet-Schering, A.C. Beynen, H. Everts, L.A. den Hartog and J.W. Schrama, 2002. A prolonged photoperiod improves feed intake and energy metabolism of weanling pigs. Journal of Animal Science 80, 1736-1745. Brumm, M.C, D.P. Shelton and R.K. Johnson, 1985. Reduced nocturnal temperature for early weaned pigs. Journal of Animal Science 61, 552-558. Christison, G.I., 1996. Dim light does not reduce fighting or wounding of newly mixed pigs at weaning. Canadian Journal of Animal Science 76, 141-143. Close, W.H.C and J. Le Dividich, 1984. The influence of environmental temperature, level of feeding and age of weaning on the growth and metabolism of the young pig. Animal Production 38, 550 (Abstr.). Close, W.H.C and M. Stanier, 1984a. Effects of plane of nutrition and environmental temperature on the growth and development of early-weaned piglets. 1-Growth and body composition. Animal Production 38, 211-220.

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Close, W.H.C and M. Stanier, 1984b Effects of plane of nutrition and environmental temperature on the growth and development of early-weaned piglets. 2- Energy metabolism. Animal Production 38, 221-231. Collin, A., J. van Milgen and J. Le Dividich, 2001. Modelling the effect of high, constant temperature on food intake in young growing pigs. Animal Science 72, 519-527. Crenshaw, T.D., M.E. Cook, J. Odle and R.E. Martin, 1986. Effect of nutritional status, age at weaning and room temperature on growth and systemic immune response of weanling pigs. Journal of Animal Science 63, 1845-1853. Danielsen V and H.E. Nielsen, 1978. Rearing of early weaned piglets on flat decks or on concrete floors. Paper presented at the 29th Annual Meeting of the EAAP (6pp). Stockholm. DK. del Barrio, A.S., J.W. Schrama, W. van der Hel, H.M. Beltman and M.W.A. Verstegen, 1993. Energy metabolism of growing pigs after transportation, regrouping, and exposure to new housing conditions as affected by feeding level. Journal of Animal Science 71, 1754-1760. Dyrendhal, S., 1964. Suitable age and weight for early weaning of piglets. In: E Salmon Legagneur and A Aumaître (editors), Physiologie nutritionnelle et sevrage des porcelets, INRA, Paris, pp. 129-136. Farmer, C and G.I. Christison, 1982. Selection of perforated floors by newborn and weanling pigs. Canadian Journal of Animal Science 62, 1229-1236. Feenstra, A., 1984. Environmental experiments with weaned pigglets: air temperature. Danish Building Research Institute. SBI Landrugsbyggeri., 62. Feenstra, A., 1985. Effects of air temperature on weaned piglets. Pigs News and Information 6, 295-299. Fenton, J.P., K.L. Roehrig, D.C. Mahan and J.R. Corley, 1985. Effect of swine weaning age on body fat and lipogenic activity in liver and adipose tissue. Journal of Animal Science 60, 190-199. Francis, D.A., G.I. Christison and N.F. Cymbaluk, 1996. Uniform or heterogeneous weight groups as factors in mixing weanling pigs. Canadian Journal of Animal Science 76, 171-176. Fuller, M.F., 1965. The effect of environmental temperature on the nitrogen metabolism and growth in the young pig. British Journal of Nutrition 19, 531-546. Giles, L.R., D.T. Harrison, D.P. Collins and P.J. Nichols, 2001. Effect of group size on weaner pig performance. In: P.D. Cranwell, (editor), Manipulating Pig Production VIII. Australasian Pig Science Association, Werribee, Australia, pp. 39. Hacker, P.R., G.S. Wogar and J.R. Ogilvie, 1979. Environment indices for weaned pigs. ASAE Paper N° 79-4017. ASE; St Joseph, MI. Hata, H., T. Koizumi, H. Miyazaki, H. Abe, N. Sugimoto and T. Fujita, 1986. Behavioural and growth responses to environmental temperature in weaned piglets kept in groups. Japonese Journal of Zootechnical Science 73, 796-800. Heetkamp, M.J.W., J.W. Schrama, L. de Jong, J.W.G.M. Swinkels, W.G.P. Schouten and M.W. Bosch, 1995. Energy metabolism in young pigs as affected by mixing. Journal of Animal Science 73, 3562-3569. Hel, van der , W., M.W.A. Verstegen, W. Baltussen and H. Brandsma, 1985. The effect of ambient temperature on diurnal rhythm in heat production and activity in pigs kept in groups. International Journal of Biometeorology 28, 303-316.

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Hendriks, H.J.M., B.K. Pedersen, H.M. Vermeer and M. Wittman, 1998. Pig housing systems in Europe: current distributions and trends. Pigs News and Information 19, 97N-104N. Jacobson, L.D., E. Noyes, C. Pijuan, J.J. Boedicker and K.A. Jenni, 1985. Effects of below normal ventilation rates on early weaned piglets. ASAE Paper N° 85-4021. ASAE, St Joseph, MI. Jacobson, L.D., J.J. Boedicker and K.A. Jenni, 1986. Air quality in a swine industry. ASAE Paper N° 86-4036. ASAE St Joseph, MI. Kelley, K.W., 1980. Stress and immune function. A bibliographic review. Annales de Recherches Vétérinaires 11, 445-478. Kelly, H.R.C., J.M. Bruce, S.A. Edwards, P.R. English and V.R. Fowler, 2000. Limb injuries, immune response and growth of early weaned pigs in different housing conditions. Animal Science 70, 73-83. Kérébel, C., P. Gérault, E. Eveno, R. Cariolet, D. Huonnic and F. Madec, 2000. Le comportement alimentaire du porcelet au moment du sevrage. Journées de Recherche Porcine en France 32, 151-156. Kornegay, E.T and D.R. Notter, 1984. Effects of floor space and number of pigs per pen on performance. Pig News and Information 5, 23-33. Kreukniet, M.B., W. Visser, J.M.F. Verhagen and M.W.A. Verstegen, 1990. Influence of climatic treatments on systemic immunological parameters in pigs. Livestock Production Science 24, 249-258. Kurihura, Y., S. Ikeda, S. Suzuki, S. Sukemori and S. Ito, 1996. Effect of daily variation of environmental temperature on the growth and digestibility in piglets. Japenese Journal of Swine Science 33, 25-29. Le Dividich, J., 1979. Le bâtiment de sevrage des porcelets: importance des conditions climatiques et de l’aménagement intérieur sur les perfoirmances. Journées de la Recherche Porcine en France 11, 133-152. Le Dividich, J., M. Vermorel, J. Noblet, J.C. Bouvier and A. Aumaître, A., 1980. Effects of environmental temperature on heat production, energy retention, protein and fat gain in early weaned piglets. British Journal of Nutrition 44, 313-323. Le Dividich, J., 1981. Effects of environmental temperature on the growth rates of early weaned piglets. Livestock Production Science 8, 45-86. Le Dividich, J. and J. Noblet, 1982. Growth rate and protein and fat gain in early weaned pig housed below thermal neutrality. Livestock Production Science 9, 731-742. Le Dividich, J. and P. Herpin, 1994. Effects of climatic conditions on the performance, metabolism and health status of weaned piglets: a review. Livestock Production Science 38, 79-90. Le Dividich, J., J. Noblet, P. Herpin, J. van Milgen and N. Quiniou, 1998. Thermoregulation. In: J. Wiseman, M.A. Varley and J.P. Charlick (editors), Progress in Pig Science. Nottingham University Press, Nottingham, UK, pp. 229-263. Le Dividich, J. and B. Sève, 2001. Energy requirements of the young pig. In: M.A. Varley and J Wiseman (editors), The Weaner Pig. Nutrition and Management. CABI Publishing International, Wallingford, UK, pp 17-44. Madec, F. and E. Leon, 1999. The role of management and husbandry in the pig health with emphasis on the post-weaning enteric disorders. In: P.D. Cranwell (editor), Manipulating Pig Production VII. Australasian Pig Science Association, Werribee, Australia, pp. 200-209.

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Madec, F., N. Bridoux, S. Bounaix and A. Jestin, 1998. Measurements of digestive disorders in the piglet a weaning and related risk factors. Preventive Veterinary Medicine 35, 53-71. Maenz, D.D., J.F. Patience and M.S. Wolynetz, 1994. The influence of the mineral level in drinking water and the thermal environment on the performance and intestinal fluid flux of newlyweaned pigs. Journal of Animal Science 71, 300-308. Massabie, P., R. Granier and J. Le Dividich, 1997. Effects of environmental conditions on the performance of growing-finishing pigs. Proceedings of the 5th International Livestock Environment Symposium, Bloomington, Minnesota. pp. 1010-1016. McConnell, J.C., J.C. Eargle, and R.C. Waldorf, 1987. Effects of weaning weight, co-mingling, group size and room temperature on pig performance. Journal of Animal Science 65, 1201-1206. McCracken, K.J. and B.J. Caldwell, 1980. Studies of diurnal variations of heat production and the effective lower critical temperature of early-weaned pigs under commercial conditions of feeding and management. British Journal of Nutrition 43, 321-328. McCracken, K.J. and R. Gray, 1984. Further studies on the heat production and effective lower critical temperature of early weaned pigs under commercial conditions of feeding and management. Animal Production 39, 283-290. Miller, H.M., P. Toplis, and R.D. Slade, 1999. Weaning weight and daily live weight gain in the week after weaning predict piglet performance. In: P.D. Cranwell (editor), Manipulating Pig Production VII. Australasian Pig Science Association, Werribee, Australia, p. 130. Mitchell, C.D. and W.J. Smith, 1978., Piglet foot dimensions for design of slotted floors. Farm Building Progress 51, 7. Morrison, W.D., L.A. Bate, I. McMillan and E. Amyot, 1987. Operant heat demand for piglets housed on four different floors. Canadian Journal of Animal Science 67, 337-341. O’Connell, N.E., V.E. Beattie and R.N. Weatherup, 2001. Influence of group size on the performance and behaviour of 4 to 10 week old pigs. Animal Science 69, 481-489. Orr, D.E., F.E. Moudy, L.F. Tribble and W. Grub, 1978. Interactive effect of temperature and floor material on nursery pig performance. Proceedings of the 26th Ann. Swine Short Course. Texas Tech. University. Tech. Rept. N° t-5-138. Petherick, C. and S. Baxter, 1982. Space requirement for pigs. Pig Farming (Suppl.) Dec., 93. Pluske, J.R. and I.H. Williams, 1996. The influence of feeder type and the method of group allocation at weaning on voluntary food intake and growth in piglets. Animal Science 62, 115-120. Pluske, J.R., D.J. Hampson and I.J. Williams, 1997. Factors influencing the structure and function of the small intestine in the weaned pig: a review. Livestock Production Science 51, 216-236. Pouteaux, V.A., G.I. Christison and W.R. Stricklin, 1983/84. Perforated floor preferences of weanling pigs. Applied Animal Ethology 11, 19-23. Rantzer, D., J. Svendsen and B. Westrom, 1995. Effects of strategies restriction on pig performance and health during the post-weaning period. Acta Agriculturae Scandinavica 46, 219-225. Rantzer, D. and J. Svendsen, 2001. Slatted versus solid floors in the dung area: comparison of pig production system (moved versus not moved) and effects on hygiene and pig performance, weaning to 4 weeks after weaning. Acta Agriculturae Scandinavica 51, 175-183. Rinaldo, D., M.C. Salaün and J. Le Dividich, 1989. Influence d’une réduction de la température ambiante ou d’ un abaissement nocturne de la température ambiante sur les performances du porcelet sevré. Journées de la Recherche Porcine en France 21, 239-244.

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Rinaldo, D. and J. Le Dividich, 1991. Assessment of optimal temperature for performance and chemical body composition of growing pigs. Livestock Production Science 29, 61-75. Riskowski, G.L. and D.S. Bundy, 1990. Effect of air velocity and temperature on growth performance of weanling pigs. Transactions of the ASAE 33, 1669-1675. Ritz, M. 1971. CIGR Conference. Piacenza, 239A-245A. Sarmiento, J.I., 1983. Enviromental temperature: a predisposing facxtor in the enterotoxigenic escherichia Coli- induced diarrhea in the newborn pig. MSc, Dissertation. University of Guelph. 123pp. Scheepens, C.J.M., M.J.L. Tielen and M.J.C. Hessing, 1991. Influence of daily intermittent draught on the health of weaned pigs. Livestock Production Science 29, 241-254. Schneider, D. and K. Bronsch, 1973. Einfluss der stallbelegung nach der sog. Fleissbaud und Rein Raus Methode auf die Frekelaufzucht. Züchtungskunde 45, 53-60. Schneider, D. and K. Bronsch, 1974. The effect of carbadox on the rearing of early weaned piglets kept on the floor or in batteries. Züchtungskunde 46, 366-375. Shelton, D.P. and M.C. Brumm, 1983. Hovers in flat-deck swine nursery pens. ASAE Paper N° 834010. ASAE, St Joseph, MI. Shelton, D.P. and M.C. Brumm, 1988. Reduced nocturnal temperatures in a swine nursery. A modified regimen. Transactions of the ASAE 31, 888-891;. Sloat, D.A., D.G. Mahan and K.L. Roehrig, 1985. Effect of weaning weight on postweaning body composition and digestive enzyme development. Nutrition Reports International 31, 627-635. Sugahara, M., D.H. Baker, B.G. Harmon and A.H. Jensen, 1970. Effect of ambient temperature on performance and carcass development in young swine. Journal of Animal Science 31, 59-62. Swinkels, J.W.G.M., E.T. Kornegay and M.W.A. Verstegen, 1988. The effect of reduced nocturnal air temperature and feed additives on the performance, the immune response and scouring indexes of weanling pigs. Journal of Animal Physiology and Animal Nutrition 60, 137-145. Turner, S.P., D.J. Allcroft and S.A. Edwards, 2003. Housing pigs in large social groups: a review of implications for performance and other economic traits. Livestock Production Science. (In press). Vellenga, L., H.M.van Veen and A. Hoogerbrugge, 1983. Mortality, morbidity and external injuries in piglets housed in two different housing systems. Veterinary Quarterly 5, 101-106. Verhagen, J.M.F., 1987. Acclimation of growing pigs to climatic environment. PhD Thesis, 128 pp., Wageningen, The Netherlands. Verhagen, J.M.F., R. Geers and M.W.A. Verstegen, 1988. Time taken for growing pigs to acclimate to change in ambient temperature. Netherlands Journal of Agricultural Science 36, 1-10. Verstegen, M.W.A. and W. van der Hel, 1974. The effects of temperature and type of floor on metabolic rate and effective critical temperature in groups of growing pigs. Animal Production 18, 1-11. Verstegen M.W.A., A. Siegerink, W. van der Hel, R. Geers and C. Brandsma, 1987. Operant supplementary heating in groups of growing pigs in relation to air velocity. Journal of Thermal Biology 12, 257-261. Wathes, C.M., B.G. Miller and F.J. Bourne, 1989. Cold stress and post-weaning diarrhoea in piglets inoculated orally or by aerosol. Animal Production 49, 483-496. Wathes, C.M., 2001. Air polluants from weaner production. In: M.A. Varley and J Wiseman (editors),The Weaner Pig. Nutrition and Management, CABI Publishing International, Wallingford, UK, pp. 259-271.

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Whittemore, C.T., A. Aumaître and I.H. Williams, 1978. Growth of body components in young weaned piglets. Journal of Agricultural Science (Cambridge) 91, 681-692. Wilson, R.D., D.E. Orr, L.F. Trible and W. Grub, 1977. Floor material and temperature effect on nursery pig performance. In: Proceedings of the 25th Annual Swine Short Course, Texas Tech. University. pp 35-39. Wolter, B.F. and M. Ellis, 2002. Impact of large group sizes on growth performance in pigs in the USA. Pig News and Information 23, 17N-20N.

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14 Saving and rearing underprivileged and supernumerary piglets, and improving their health at weaning J. Le Dividich, G.P. Martineau, F. Madec and P. Orgeur

14.1

Introduction

Variation in weight is a trait relevant to pig production. However, variations in weight within groups of pigs under commercial conditions can have a high associated cost to swine producers, particularly when the all-in, all-out concept of raising pigs is followed. Within a litter, a two- to three- fold difference in birthweights and in weaning weights are very common in commercial herds. This variation in birth weight is associated with a high level of mortality among the lightest piglets, termed as underprivileged. When surviving, these piglets perform worse than their heavier littermates causing high variation in days to market weight. Birth weight and growth of the suckling piglets are dependent on several factors, among which, litter size has the largest influence. During the past decade, pig production has been characterised by a major improvement in litter size (see review by Legault , 1998). However, this has resulted in a higher proportion of undersized piglets, whereas the rearing capacity of- these more prolific sows has not been usually increased proportionally so that, in a batch-farrowing system, the total pigs born alive can exceed the rearing capacity of the batch. Disease control both prior to and at weaning is another major problem encountered in piglet rearing. Prior to weaning, piglets can be contaminated by the sow. In addition, the weaned pig is highly susceptible to digestive disorders because of the relatively immature defence mechanisms of its digestive tract to cope with the proliferation of toxin-producing microorganisms (Mezoff et al., 1991). As a result, diarrhoea is the most common clinical problem encountered in the first one or two weeks after weaning, and this leads to a temporarily impaired growth rate and sometimes to death. Therefore, saving these supernumerary and light piglets while helping the latter to catch up in growth their heavier littermates and improving the health status are major concerns for the pig producer. Reviews on the nutrition of the weaned piglets are available (see Chapter 11) and in Veum and Odle (2001).

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14.2

What are underprivileged and supernumeraries?

The term underprivileged is applied to piglets weighing 65-70% of the mean birth weight of the litter. Compared to their heavier littermates, these piglets have less body energy stores, are more susceptible to cold, took longer to achieve their first suckling, and are less competitive at the udder and hence consume less colostrum (see review by Le Dividich et al., 1998). On the basis that they have a higher risk of dying both during and/or soon after parturition and before weaning (Figure 14.1), piglets from modern genotype weighing approximately 1.00 kg at birth can be classified as underprivileged (Rydhmer, 1992; Léon and Madec, 1992; Herpin et al., 1996). This body weight is close to the 1.10 kg below which the thermogenic capacities of the newborn are also impaired (Herpin et al., 2001). Within a litter, the term supernumerary is applied to piglets in excess of the number of available functional teats. However, these piglets are usually saved by fostering. More specifically, in batch - farrowing systems, the term supernumerary refers to piglets in excess of the number of functional available teats of the batch. In this chapter, the term supernumerary is referred to those piglets. Occurrence of these underprivileged and supernumerary piglets is dependent on several factors including litter size. Litter size is dependent on genotype, and within a genotype, on the sow parity. However, during the last decades, selection of sows for litter size at birth has been introduced successfully in many breeding programmes (Bidanel et al., 1994; Estany and Sorensen, 1995; Legault et al., 1998). In France, for example, total piglets born per litter has increased from 11.4 to 12.8 over the past decade, with the increase reaching 1 piglet over the last 5 years. This

1500 Stillborn piglets Birthweight (g)

1200 900

Liveborn piglets dying before weaning

600 Surviving piglets

300 0 Rydhmer (1992)

Léon and Madec (1992)

Figure 14.1. Birthweight of stillborn piglets, liveborn piglets dying before weaning and piglets surviving to weaning.

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Percentage

increase in litter size has resulted in both a decrease in absolute mean birthweight amounting to 35-40 g for every additional pig born, and an increased proportion of low birthweight piglets. Surveys by Le Dividich (1999) and Quiniou et al. (2001) showed that the increase in litter size from 12-13 to (16 increases the proportion of weak piglets (< 1.0 kg) from 9 to 23%. In addition, the proportion of high litter size (≥ 15 total born) has dramatically increased (Figure 14.2), while in most cases the rearing capacity of these sows has not been increased proportionally unless some components of the Chinese Meishan breed have been incorporated into these more prolific sows (Tribout et al., 2002). It follows that selection for litter size has resulted in an increased proportion of disadvantaged animals while creating supernumerary piglets.

25

30

20

25 20

15

15

10

10

5

5

0

0

< 11

12 - 13 14 - 15

> 16

Litter size

1971

1981

1991 1995/96 2000

Year

Figure 14.2. Percentage of small piglets (< 1.0 kg) per litter in relation to litter size (a) and percentage of high litter size (≥ 15 total born) throughout the three last decades in France (b). (Adapted from Quiniou et al, 2002 (a) and J. Dagorn, 2002 (Personal communication)(b).

14.3

Reasons accounting for variation in birthweight and weaning weight

Piglets are not equal at birth at least with respect to body weight. In addition, variations in growth rate can occur at any stage of pig life, but particularly during the suckling phase due to nutritional / environmental influences. 14.3.1

Variation in birth weight

Foetal growth and hence birth weight is determined by the amount of nutrients transferred from the mother to her foetuses and ultimately the genetic endowment of the foetus. The transfer of nutrients from the mother to her foetuses depends

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on both the size of placenta, uterine blood flow and, to a much lesser extent, on sow nutrition. However, piglet birthweight is less dependent on level of feeding of the pregnant sow because it increases by only 4 to 8 g for each additional megajoule of daily digestible energy intake (Henry and Etienne, 1978). Small piglets have a lower placental weight and a reduced placental blood flow when compared with their larger littermates (DeRoth and Bisaillon, 1980; Wootton et al., 1977). On the other hand, uterine blood flow per foetus decreases with the increase in the number of foetuses present in the uterine horn (Père and Etienne, 2000), and this explains why piglets from a large litter size are lighter at birth. These small placentas are identified as early as 30 days of gestation (Wise et al., 1997), while the within-litter variation in birthweight is established at 35 days of pregnancy (van der Lende et al.,1990). Heritability of the within-litter standard deviation in birthweight is low, ranging from 0.08 to 0.11 (Högberg and Rydhmer, 2000; Damgaard et al., 2001), but significantly different from zero, thus offering some premise for genetic selection of sows to give birth to more homogeneous litters. 14.3.2

Variation in weaning weight

During the suckling phase, growth rate of piglets is closely dependent on milk intake (Noblet and Etienne, 1987) which, in turn, is dependent on both nursing position of the piglet and its ability to extract milk from the teats. In addition, the mammary glands are not equal in terms of functionality. The most anterior pairs have more wet and dry weights, more protein and DNA contents, and, are more functional than the most posterior pairs of glands (Kim et al., 2000). It follows that, even if litters are uniform at birth, those piglets adopting the most posterior teats exhibit a lower growth rate (Figure 14.3). However, heavier pigs at birth usually nurse anterior mammary glands (Hartsock et al., 1977), which leaves the small pigs to nurse the posterior glands. Further, there is a strong positive relationship between piglet body weight, milk consumption and sow milk production (King et al., 1997) indicating that piglet body weight itself contributes to differences in milk intake. For example, through d17 to 24 of lactation, lighter piglets are reported to consume 25% less milk per sucking than do heavier ones (Pluske and Williams, 1996). In summary, pigs are not equal at birth with respect to birthweight. Also the functionality of the mammary glands is not uniform. These, combined with the lower ability of the small pigs to compete at the udder and to extract milk from the teats, may accentuate the disadvantage of the small pigs.

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ADG 170 Birth weight

160

ADG

150 140 130 120

Birth weight, kg

110

1.6 1.4

100

1.2

90

1 1

2

3

4

5

6

52

56

50

45

29

34

7 16

80 8 Teat position 2

n piglets

Figure 14.3. Effect of teat position (1 = anterior) on the average daily gain of nursering pigs in relation to birth weight (weaning age = 21 d) (Adapted from Kim et al., 2000).

14.4

Differences between underprivileged and “normal” piglets

14.4.1

Body composition

Is the difference between an underprivileged and a “normal” piglet only a difference in weight? Within a large range of birth weights (0.5-1.86 kg), Curtis et al. (1967) and de Passillé and Hartsock (1979) did not observe any differences in gross chemical composition in piglets. Liver and muscle glycogen concentrations are only marginally affected (Ojamaa et al.., 1980). Because muscle fibre number is a major determinant of muscle mass and hence of growth potential, it is important to examine to what extent the number of muscle fibres is affected by birthweight. A reduced number of muscle fibres is usually reported in small piglets when comparing pairs of littermates differing extremely in body weight (Powell and Aberle, 1980; Wigmore and Stickland, 1983; Handel and Stickland, 1987), but not always (Dwyer et al. 1993). Comparing small (0.80-1.00 kg) to large (1.90-2.10 kg) littermates Gondret et al. (2003) found that total myofibre number was 13 and 20% reduced in semitendinosus (P < 0.09) and rhomboideus (P < 0.08) muscles, respectively, in small piglets at slaughter. There is a strong, positive within-litter correlation between circulating concentrations of insulin-like growth factor I (IGF1) and birthweight (Herpin et al., 1992; Wise et al., 1997). IGF-1 and analogues are reported to stimulate growth in normal and intra-uterine growth-retarded piglets

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(Schoknecht et al., 1997; Dunshea et al., 2002). In contrast, Ritacco et al. (1997) failed to find any stimulatory effect of IGF-1 on the postnatal growth of low-birth weight piglets. Body weight does influence body composition at weaning. Small piglets at weaning are leaner (Sloat et al., 1985) and are suggested to have a less functional digestive tract (de Passillé et al., 1989; Cranwell et al., 1997). Together, these observations suggest a lower ability of light piglets to withstand the period of underfeeding following weaning and to cope with the transition to the postweaning diet. 14.4.2

Performance of underprivileged pigs

Weight at a given age is important in terms of subsequent growth. This is illustrated by the fact that 21 to 45% of the variation in weaning weight is explained by the variation in birthweight (McBride et al., 1965; McConnell et al., 1987; Caugant and Gueblez, 1993), and that 28 to 49 % of the variation in piglet bodyweight at the end of the post-weaning phase is explained by the variation in weaning weight (Miller et al., 1999; Lawlor et al., 2002). The relationships between birthweight and weight at weaning and at the end of the post-weaning phase are shown in Figure 14.4. Based on these data, each 0.1 kg decrease in birth weight ranging from 0.7

Body weight, kg

Body weight at the end of the post-weaning phase

35 30 25 20 15

Body weight at weaning

10 5

2.3-2.4

2.2-2.3

2.1-2.2

2.0-2.1

1.9-2.0

1.8-1.9

1.7-1.8

1.6-1.7

1.5-1.6

1.4-1.5

1.3-1.4

1.2-1.3

1.1-1.2

1.0-1.1

0.9-1.0

0.8-0.9

0.7-0.8

0

Birthweight class, kg Figure 14.4. Effects of piglets birthweight on the mean body weight at weaning and at the end of the post-weaning phase (age at weaning = 27 d; duration of the postweaning phase = 36 d; total number of piglets = 4208). (Adapted from Quiniou et al., 2001).

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to 2.3 kg, translates into approximately 0.35 and 0.76 kg decrease in the weight at weaning and at the end of the post-weaning phase, respectively. Overall (Table 14.1), every 0.1 kg decrease in birthweight increases days from birth to slaughter by approximately 2.3 days. However, an important point is to notice that within the range of 0.8 to 2.0 kg, birthweight has no marked effect on carcass lean meat content and on feed efficiency. From these observations and on the basis of the ability of the piglet to survive, it is suggested that a birthweight of ≈ 0.9-0.95 kg represents a limit above which saving of piglets from modern genotypes is not questionable.

Table 14.1. Effects of birth-weight on days to slaughter and carcass lean meat content. Birthweight (kg) Days to slaughter

kg feed : kg gain content (%)

Lean meat

References

• 1.57

3.28 3.34 2.94 3.06 2.83 2.82 2.70 2.70 2.19 2.23 -

54.7 55.6 56.2 56.5 55.6 55.2 52.9 51.7 54.9 55.1 60.9 59.9

Hegarthy and Allen (1978) Powell and Aberle (1980) Caugant and Guéblez (1993) Azain (1993) Mahan (1993) Wolter et al., (2001) Wolter et al., (2002) Gondret et al. (2003, Pers.com.)

• •

• • • • •

0.81 1.76 1.06 1.87 1.18 1.5 - 2.0 < 1.0 > 1.35 < 0.9 1.71 1.45 1.70 1.40 1.83 1.32 1.9 - 2.1 0.8 - 1.0

14.5

182 205 160 174 170 179 173 184 167 182 169 179 162 170 141 148 154 166

Management practices to improve survival and growth of the underprivileged pigs

Management practices aimed at improving the survival and performance of the disadvantaged pig are directed towards providing assistance to the neonatal pig, reducing competition among littermates by grouping piglets of similar bodyweight

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together within litters (cross-fostering), split weaning, that is, a permanent removal of part (the heaviest piglets) of the litter a few days before complete weaning, and appropriate feeding strategies. 14.5.1

Providing assistance to the underprivileged piglets at birth

This includes supervision of farrowing, provision of energy and immunoglobulins to the pigs and cross-fostering. 14.5.1.1 Supervision of farrowing Piglets of low birthweight have a high risk of dying during or soon after parturition (see review in Le Dividich, 1999). These piglets are more susceptible to a higher degree of asphyxia during parturition than their heavier littermates, and therefore are less viable at the time of birth as they are less able to maintain their body temperature, take longer to achieve the first sucking and are less competitive at the udder (Herpin et al., 1996). Attending farrowing and providing assistance to the piglets consist mainly in the removal of placenta envelopes around the pig to prevent suffocation, providing the weak pigs with a source of energy, guiding them to nipples and positioning them in the heated area. These practices improve survival as illustrated by the reduction in the number of stillbirths from 0.6- 0.7 to 0.2- 0.3 per litter (Holyoake et al.,1995; White et al.,1996). Although the practices need to be evaluated against the cost of the extra labour and the benefits derived from raising extra pigs, it is clear that the economic benefits of the procedures would be maximised when several litters are being born simultaneously as in the case in operations which use batch farrowing. 14.5.1.2 Provision of energy and immunoglobulins The requirement for energy is maximum at birth mainly because of the high rate of heat loss associated with thermoregulation. Therefore, provision of an adequate thermal environment and hence minimising heat loss from the piglet is a major goal during the first postnatal days (see review in Le Dividich and Herpin, 1999). Sow colostrum is certainly the best food for the newborn pig, providing passive immunity, energy and growth factors for the developing digestive tract. Colostrum consumption averages 315-340g/kg BW in the first day of life (Le Dividich et al.,1998) but can be very variable as suggested by changes in body weight gain ranging from -136 to + 233 g during the first postnatal day (Thompson and Fraser, 1988). In addition, because of an increased competition at the udder or sometimes, an insufficient number of teats or insufficient colostrum production by the sow, there is a risk that consumption of colostrum will be insufficient with an increasing number of piglets from a large litter size. Insufficient nutrient (colostrum) intake

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is primarily implicated in deaths due to undernutrition and hypothermia. However, a sub-optimal intake of colostrum may result in an inadequate transfer of maternal immunoglobulins (Ig) to the new-born animal and therefore increase susceptibility to infection, not only in the immediate post-natal period, but also during late lactation as suggested by the positive relationship between the concentrations of IgG in the plasma of piglets shortly after birth and survival rate (Blecha and Kelley, 1981; Hendrix et al., 1978). In the case of litter size exceeding the number of available teats, if no alternative exists, cross nursing (Donovan and Dritz, 2000) can be efficiently used. Similarly, a number of pig producers collect colostrum during parturition, and then tube feed colostrum (40-50g, twice daily). This is becoming a common practice to provide supplemental energy and immunoglobulins (Ig) to the weak piglets. Freezing of colostrum is a suitable means of creating a colostrum bank with intact nutritional and immunological qualities (Klobasa et al., 1998). Several commercial colostrum substitutes are available with most of them containing Ig derived from cow’s or ewe’s colostrum. It is assumed that these Ig provide some local protection within the digestive tract. However, IgG derived from these species is not specific for pathogens affecting swine and are poorly absorbed by the neonatal pig intestine (Gomez et al., 1998). More recently, purified porcine Ig has become commercially available. However, porcine IgG is also poorly absorbed by the piglet (Gomez et al. 1998; Jensen et al., 2001). Nonetheless, piglets deprived of sow colostrum and fed artificial milk containing purified porcine IgG for two days are reported to survive and perform similarly to those fed sow’s colostrum (Gomez et al., 1998). 14.5.2

Cross fostering

Fostering of piglets from one litter to another is used to avoid an excessive number of piglets in a given litter while creating litters of light and heavy pigs to reduce competition among littermates. Practised within a few hours after birth, cross-fostering reduces mortality among the small pigs. English and Bampton (1982) found that cross-fostered litters had a 40% improvement in piglet survival to weaning. Crossfostering is sometimes continuously practised up to weaning so that individuals that fall back are transferred to a smaller litter. This practice reduces the variation of body weight at weaning thus producing more uniform litters at weaning (Straw et al.,1998). However, repeated mixings have detrimental effects on the behaviour of sows and piglets, resulting in disruption of suckling patterns (Price et al., 1994), increased non-productive milk letdowns and enhanced aggressive behaviour of sows towards alien piglets. Compared with fostering limited to the first two days of life, repeated fostering causes a 13 to 20% reduction in weight gain of the fostered piglets (Straw et al., 1998; Robert and Martineau, 2001) and sometimes of the resident piglets. In these conditions, it is doubtful that the reduced variation in weight at weaning is desirable if it is associated with a reduction in growth rate.

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An important point is to recognise that cross-fostering can have negative effects on the health status of piglets. Extensive cross-fostering maintains a continuous cycle of PRRSv (Porcine Reproductive and Respiratory Syndrome virus) transmission (McCaw et al.. 1996). Similarly, Madec et al.. (1999) provide some evidence that both the sow and contact between piglets are involved in the transmission of the PCV2 (Porcine Circovirus type 2) which is involved in the Post-Weaning Multisystemic Wasting Syndrome (PMWS). Reduced mixing of litters is therefore strongly recommended to minimise the impact of these diseases in affected herds. 14.5.3

Split weaning

Selective weaning of the heaviest piglets of the litter some days before normal weaning improves the growth of the lightest piglets left with the sow allowing, to some extent, for these piglets to catch up in growth to their heavier littermates at normal weaning. This practice reduces the competitive pressure at the udder at an age when the supply of milk by the sow does not fulfil the energy needs of the piglets, and results in an enhanced milk intake in the light piglets. Pluske and Williams (1996) showed that when litters were reduced from 10 to 5 pigs per sow for 7 days before weaning at 29 days, milk intake per pig increased by 49%. This was related to multiple teat swapping and a longer duration of suckling during milk let down. Most authors (Wu et al., 1985; Mahan, 1993; Pluske and Williams, 1996; Vesseur et al., 1997) reported an improved growth rate ranging from 27 to 61%. Kavanagh et al. (2002) showed that pig weaning weight improved by up to 0.23 kg for each 1 pig reduction in litter size. However, this weight advantage disappears in the early post-weaning period (Pluske and Williams, 1996; Vesseur et al., 1997). It is suggested (Pluske and Williams, 1996) that pigs that are left to suckle after the reduction in litter size suffer a greater setback after weaning than their counterparts in control litters. In summary, this practise temporarily promotes the growth of small pigs but offers little in the way of improving their lifetime performance. 14.5.4

Feeding strategy

14.5.4.1 Suckling phase Providing litters with supplemental liquid milk replacer during lactation can increase piglet weaning weights by 10 to 38% (Le Dividich and Sève, 2001). However, to what extent this practice could promote the growth of litters of light piglets grouped on a sow remains to be determined. Sometimes, piglets which do not keep up with their littermates are weaned and reared with EMMA (Electronic Mother Milk Application). However, to date there is only evidence from the popular farming press in relation to this practise.

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14.5.4.2 Weaning phase Daily weight gain in the week after weaning is a significant predictor of subsequent performance (Miller et al., 1999). However, provision of a complex diet high in energy and dairy milk products to litters of small piglets (Himmelberg et al., 1985; Mahan and Lepine, 1991; Mahan, 1993; Dritz et al., 1996a), or supplemental milk replacer (Wolter and Ellis, 2001) or by increasing the duration of the phase 1 postweaning diet (Himmelberg, et al., 1985; Mahan et al., 1998), have only relatively modest improvements in piglets performance in the overall post weaning phase. Further, this advantage disappears gradually in the growing-finishing period (Dritz et al., 1996a; Whang et al., 2000).

14.6

Growth potential of underprivileged piglets

From the above discussions, it is clear that most of the attempts failed to substantially improve the life-long performance of underprivileged piglets. Now the question is, to what extent can these piglets catch up in growth to the large piglets? Neither intra-uterine growth retardation induced by protein restriction of the sow (Davis et al., 1997) nor birthweight ranging from 0.85 to 1.40 kg (Campbell and Dunkin, 1982) have effects on the potential for protein synthesis and growth performance of the piglet. Milk intake (i.e., g milk/kg BW) is not affected by birth weight (Campbell and Dunkin, 1982), however, absolute milk intake is lower in light piglets. Similarly, in the growing-finishing period, absolute feed intake is also consistently reported to be lower in lighter pigs, while feed efficiency is little or not affected. Thompson and Fraser (1986) showed that piglets’ weight gain in a given week tends to be a fixed percentage of the body weight at the beginning of the week. Together, this suggests that the lower performance achieved by light piglets is, to some extent, determined by their lower ingestive capacity and hence by their body weight.

14.7

Supernumerary piglets

Because of the increased competition at the udder, a litter size higher than the number of available functional teats results in delayed first colostrum ingestion and formation of the nursing order, lower teat fidelity, higher rate of mortality, more nursing failure and reduced growth of the litter (P. Orgeur, Personal Communication). Ways to save and to rear the supernumeraries include (i) weaning at d 1-3, or (ii) grouping on d 1 the piglets in excess of the available teats to form a new litter. This new litter is fostered onto a dam of the previous batch whose litter is weaned. In all cases, piglets are allowed to receive colostrum from their dam.

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14.7.1

Weaning at day 1-3

Piglets artificially fed a liquid diet high in dairy products can exhibit growth rates as high as 400-550g / d (Hodge, 1974; Harrell et al., 1993). More usually, satisfactory growth rates of ≈ 200 g/d are reported (Pettigrew and Harmon, 1977; Pettigrew et al., 1977). Reduced performance was found by Huysman et al. (1994) in piglets reared from d 3 to d 28 with EMMA compared with that obtained using fostersow nursing (122 vs 206g). In fact, this practice requires specialised nurseries, sophisticated milk dispensers, and because of the high occurrence of diarrhoea, a high level of sanitation. 14.7.2

Fostering onto a nurse sow

In a batch-farrowing system, the practice implies the choice of a nurse sow from the previous batch so that, at the time of fostering, the older litter can be easily weaned. The size of the new litter is similar to that of the nurse sow and, in practice, is composed of large pigs which have more opportunity to ingest enough colostrum from their dam. As mentioned above, fostering of piglets practised after the nursing order has been established, i.e., after 2-3 days, has detrimental effects on the behaviour of sows and piglets. However, supplying a nurse sow with a new litter aged 24-36 hours has only minor effects on the nursing behaviour of the sow. In a study involving 18 nurse sows (Orgeur et al., 2000), all piglets survived and only one sow displayed aggressive behaviour towards the new litter and refused to nurse. On average, sows nursed the new litter within 5h (range 1.35 to 8.15 h) following the piglets introduction. The growth rate of the new litter during the first postnatal week is acceptable, albeit lower (170 vs 205 g/pig/d) than that of the control pigs. The new litter is then weaned at one week of age or sometimes at the normal weaning age. 14.7.3

Weaning at one week of age

Weaning at 7-14 d of age is usually associated with a severe growth check caused by the low dry food intake (Leibbrandt et al., 1975; Zijlstra et al., 1996; Heo et al., 1999; Kim et al., 2001). In the study by Orgeur et al. (2000) involving weaning at 7 d of age, pigs at 21 days of age were 40% lighter than their counterparts (sow reared). However, the difference decreased to 7.5% at d 74 and to 3.7% at slaughter weight. Other studies (Hohenshell et al., 2000) reported similar performance in early (8-13d) and late weaned pigs (27-34 d). However, the severity of the growth check can be markedly overcame by providing the piglets with a liquid feed (Lecce et al., 1979; Zijlstra et al., 1996; Heo et al., 1999; Kim et al., 2001). An important point to recognise is that early weaning has little effect on body composition at slaughter weight (Pluske et al., 1995; Dritz et al., 1996a; Kim et al., 2001; Le Dividich et al., Pers. Communication).

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In summary, advantages of the use of a foster sow associated with early weaning are (i) no disturbance in the batch farrowing system, (ii) minimal mortality among the fostered pigs while growing reasonably well, (iii) no marked digestive disturbance at weaning and (iv) no effect on carcass composition. The weak point of the practice is the low level of performance in the immediate period following weaning, but this can be improved by feeding liquid diets.

14.8

Management to improve the health of piglets

One of the major problems in the pig industry is the postweaning syndrome (PWS), which occurs mainly through diarrhoea mainly caused by E. coli, leading to poor performance during a period of about 10 days following weaning (for details, see Chapter 9 and the review of van Beers-Schreurs et al., 1992). Weaning at about 3 weeks of age, as practised in the major pig producing countries, implies the withdrawal of milk resulting in the loss of milk immunoglobulins protection at an age when maternal antibodies are at the lowest levels and active humoral and mucosal immunity are still impaired. At weaning, the piglet is exposed to novel antigens associated with food and to changes in microbial flora while the low feed intake immediately postweaning induces marked morphological changes in the intestine. Although the aetiology of diarrhoea is multifactorial, it is to some extent, controlled by feed additives, including acidifiers, antibiotics and antimicrobial growth promoters such as copper sulphate and zinc oxide and pre-and probiotics. However, there is currently pressure to reduce the use of antibiotics, copper sulfate and zinc oxide. In addition, dependent on the immune state of the piglet, the sow also may be a source of contamination for her litter. Production systems such as all-in / all-out (AIAO) production and weaning at an age when the immune protection of the litter is still adequate have the potential to improve both the health of the piglet and production efficiency. 14.8.1

All-in / All-out management system

The AIAO procedure has become an essential part of successful management of the nursery. The procedure includes simultaneous weaning of pigs and simultaneous emptying of the nursery, and involves cleaning and disinfection between batches, and a delay of at least 3-4 days between two batches, thus limiting the disease transmission between batches. The procedure is shown to improve the air quality (Cargil and Banhazi, 1997). Advantages of the AIAO were first described by Schneider and Bronsch (1973). Compared with continuous flow (CF), an AIAO system resulted in a 26% and 8% improvement of ADG and feed efficiency, respectively (Table 14.2), and this was due to reduced incidence of diarrhoea. More recently, Dewey et al. (2002) assessed the health status for PRRS, Mycoplasma hyopneumoniae, Brachyspira hyodysenteriae and Actinobacillus pleuropneumoniae of 3000 pigs from 8 commercial herds in Ontario. Pigs were ear tagged and weighed at birth, weaning, 7, 14 and

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Table 14.2. Continuous flow vs all-in, all-out management system on the performance of piglets weaned at 3 weeks of age and on air quality.

Avg daily gain1 Feed/gain1 Total particles (mg/m3) 2 Airborne bacteria (103 cfu/m3) 2 1 From 2 Data

Continuous flow

All-in, all-out

References

400 1.89 1.549 124.6

503 1.74 0.937 94.2

Schneider and Bronsch, (1973) Cargill et al. (1997)

d 21 to d 63 obtained in growing-finishing houses

21 weeks, and managed in AIAO or CF. Farms using a CF management system were more positive for disease-causing agents than those using the AIAO production system. In addition, at 21 weeks of age, pigs on the AIAO system were 26 kg heavier (100 vs 76 kg) than those on the CF system. Together, these highlighted that, when applied correctly, the AIAO management system is effective in controlling a number of diseases, while improving production. Yet, its efficiency is enhanced when it is associated with segregation. 14.8.2

Segregation

Major progress in the control of the transmission of infectious agents from the sow to her litter is associated with early weaning procedures. Early weaning is designed to eliminate, or at least reduce, the effective risk of transfer of many diseases from sows to piglets while the passive immunity that the piglet has derived from colostrum intake is still at a high protective level. The original method (Medicated Early Weaning, MEW) was first described in the UK by Alexander et al. (1980). The procedure includes medication of the sow during late gestation and during lactation, farrowing in sites physically isolated from the rest of the herd, weaning of piglets at 5 days of age and moving them to off-site facilities (Off-site segregated early weaning, OFSSEW). Subsequently the procedure has been modified towards weaning between 10-12 and 15-18 days of age and a reduced medication (non-medicated early weaning). These include mainly ONSSEW (On Site Segregated Early Weaning, i.e., nursery physically isolated from the breeding herd), ISOWEAN® (Isolated Weaning), or SEW (Segregated Early Weaning) with nurseries strictly isolated from older groups of pigs (MSP, MultiSite Production). All these methods are largely related to the management of the piglets’ passive immunity. The half life of IgG, IgA and IgM is approximately 10, 3 and 2 days, respectively, (Koblasa et al., 1981). However, both the level and duration of passive immunity are quite variable (Figure 14.5) as they are dependent on the

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amount of colostrum intake and on its quality which, in turn, is dependent on the immune status of the sow, with all being variable. Strategies aiming at eliminating pathogens are based on weaning age together with a medicated protocol (Table 14.3). However, the practice fails to eliminate Streptococcus suis and PRRSv. Vaginal secretions are assumed to be the source of transmission of Streptococcus suis to piglets during parturition (Amass, et al., 1996). Further, disease caused by Streptococcus suis is even suggested to be exacerbated in some inappropriately managed SEW (Moore, 1995). However, the SEW / MSP system does minimise the effects of disease outbreaks, as illustrated by the consistently reported improvement in piglet performance (Coffey and Cromwell, 1995; Patience et al., 1997; Fangman et al., 1996) (Table 14.4) but is not a panacea for disease control. However, early weaning may reduce sow productivity because short lactation lengths are sometimes associated with an increased weaning-to-service interval, reduced farrowing rate and subsequent litter size (for review, see Cosgrove et al., 1997). Nonetheless, the SEW / MSP System has proven to be efficient to improve piglets health and performance which, to some extent, can offset the extra cost associated with the system and the possible reduced sow productivity.

50 45

Ig conc entration (mg/mL)

40 35 30

IgG IgM

25

IgA

20 15 10 5 0 0

5

10

15

20

25

30

35

Post natal day

Figure 14.5. IgG, IgA and IgM levels in the sera of suckling piglets (Adapted from Klobasa et al., 1981).

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Table 14.3. Weaning age allowing to prevent spread of disease. Disease

Weaning age (days)

Mycoplasma hyponeumoniae Pasteurella multicoda PRRSv Salmonella choleraesuis Haemophilus parasuis Aujesky’s disease Actinobacillus pleuropneumoniae

< 10 < 10 < 10 < 12 < 14 < 21 < 21

(After Harris, 1993)

Table 14.4. Effects of of site segregated early weaning on piglets performance1. ADG

Feed conversion ratio (kg feed / kg gain)

Period (d)

Control

ONSSEW

OFSSEW

Control

ONSSEW

OFSSEW

12-21 21-26 21 56

250 140 425

109 190 439

188 215 511

1.13 1.36

1.50 1.18 1.39

0.99 1.47 1.34

1 O SSEW, N

on site; OFSSEW, off site. Piglets were weaned at 21 ±3 days of age (Control) or at 12 ± 2 days of age (ONSSEW, OFSSEW). Adapted from Patience et al. (1997).

14.9

Conclusion: the need for research

In this chapter we attempted to provide information regarding the extent and the occurrence of underprivileged and supernumerary piglets and ways of improving their survival and performance. A major point to notice is that the occurrence of small and supernumerary piglets is markedly increased in hyperprolific sows. As a whole, saving small piglets (0.90 - 0.95 kg) at birth is not questionable, however a long-term improvement of their performance is still questionable. The basic question that arises is to what extent the growth potential of underprivileged piglets is lower than that of their heavier littermates. However, because bodyweight at weaning and growth rate during the week following weaning are major determinants for subsequent performance, we suggest that more research should be focused on specific strategies helping these piglets to realise their growth potential during the

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suckling period and on feeding strategies making the suckling-weaning transition smoother. Ultimately, in the light of reducing the extent of both supernumerary and small piglets, it should be relevant to select sows having more available uniform teats while giving birth to more uniform litters. The all-in/all-out management system and, early weaning associated with off-site nursery, have proven to be efficient in improving the health of the weaned piglet. But weaning at an age lower than 21 days is not allowed in certain countries (i.e., in the EU), while segregation can be costly. However, adequate management of the immune status of the sow and piglets appears promising in improving piglets health.

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Huysman, C.N., P.F.M.M. Roelefs, J.G. Plagge and A.I.J. Hoofs, 1994. Motherless rearing or extension of suckling of piglets using “EMMA”. Research Report No 1.113. Rosmalen The Netherlands, pp. 36. Jensen, A.R., J. Elnif, D.G. Burrin and P.T.Sangild, 2001. Development of intestinal immunoglobulin absorption and enzyme activities in neonatal pigs is diet dependent. Journal of Nutrition 131, 3259-3265. Kavanagh, S., P.B. Lynch, P.J. Caffrey and W. Henry, 2002. Creep feed consumption by suckling pigs and its effect on pre- and post-weaning performance. Irish Journal of Agricultural and Food Research In Press. Kim, S.W., W.L. Hurley, I.K. Han and R.A. Easter, 2000. Growth of nursing pigs related to the characteristics of the nursed mammary glands. Journal of Animal Science 78, 1313-1318. Kim, J.H., J.N. Heo, J. Odle, I.K. Han and R.J. Harrell, 2001. Liquid diets accelerate the growth of early weaned pigs and the effects are maintained to market weight. Journal of Animal Science 79, 427-434. King, R.H., B.P. Mullan, F.R. Dunshea and H. Dove, 1997. The influence of piglet body weight on milk production of sow. Livestock Production Science 47, 169-174. Klobasa, F., E. Werhahn and J.E. Butler, 1981. Regulation of humoral immunity in the piglet by immunoglobulins of maternal origin. Research in Veterinary Science 31, 195-206. Klobasa, F., M.C. Goel and E. Werhlam, 1998. Comparison of freezing and lyophilizing for preservation of colostrum as a source of immunoglobulins for calves. Journal of Animal Science 76, 923-926. Lawlor, P.G., P.B. Lynch, P.J. Caffrey and J.V. O’Doherty, 2002. Effect of pre- and post-weaning management on subsequent pig performance to slaughter and carcass quality. Animal Science 75, 245-256. Lecce, J.G., W.D Armstrong, P.C. Crawford and G.A. Ducharne, 1979. Nutrition and management of early weaned piglets: Liquid vs. dry feeding. Journal of Animal Science 48, 427-434. Le Dividich, J., 1999. Neonatal and Weaner Pig. Management to reduce Variation. In: P.D. Cranwell (editor), Manipulating Pig Production VII, Australasian Pig Science Association, Werribee, Australia, p.135-155. Le Dividich, J., J. Noblet, P. Herpin, J. van Milgen and N. Quiniou, 1998 Thermoregulation. In: J. Wiseman, M.A. Varley and J.P. Charlick (editors), Progress in Pig Science, Nottingham University Press, U.K., pp.229-263. Le Dividich, J. and P. Herpin, 1999. Perinatal Mortality in the Pig. Seminar on “Physiological and Genetic Aspects of Perinatal Mortality in Livestock”. Wageningen Institute of Animal Sciences. Wageningen, The Netherlands, 20p. Le Dividich, J. and B. Sève, 2001. Energy requirement of the young piglet. In: M.A. Varley and J Wiseman (editors), The Weaner Pig, Nutrition and Management, CAB International, pp. 1744. Legault, Ch., 1998. Génétique et prolificité chez la truie: la voie hyperprolifique et la voie sinoeuropéenne. INRA Production Animals 11, 214-218. Leibbrandt, V.D., R.C. Ewan, V.C. Speer and D. Zimmerman, 1975. Effect of age at weaning on baby pigs performance Journal of Animal Science 40, 1077-1080.

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Pettigrew, J.E. and B.G. Harmon, 1977. Milk proteins for artificially reared piglets. I. Comparison of egg white protein and effect of added immunoglobulins. Journal of Animal Science 44, 374382. Pettigrew, J.E., B.G. Harmon, S.E. Curtis, S.G. Cornelius, H.W. Norton and A.H. Jensen, 1977. Milk protein for artificially reared piglets. III. Efficacy of sodium caseinate and sweet dried whey. Journal of Animal Science 45, 261-268. Pluske, J.R., I.H. Williams and F.X. Aherne, 1995. Nutrition of the neonatal pig. In: M.A. Varley (editor), The Neonatal Pig. Development and Survival, CAB International Wallingford, U.K., pp. 187-235. Pluske, J.R. and I.H. Williams, 1996. Split weaning increases the growth of light piglets during lactation. Australian Journal of Agricultural Research 47, 513-523. Powell, S.E., and D.E. Aberle, 1980. Effects of birth weight on growth and carcass composition of swine. Journal of Animal Science, 50, 860-868. Price, E.O., G.D. Hutson, M.I. Price and R. Borwardt, 1994. Fostering in swine as affected by age of offspring. Journal of Animal Science, 72, 1697-1701. Quiniou, N., J. Dagorn and D. Gaudré, 2001. Variation du poids des porcelets à la naissance et incidence sur les performances zootechniques ultérieures. Technicine Porcine 24, 11-17. Quiniou, N., J. Dagorn and D. Gaudré, 2002. Variation of piglets’ birth weight and consequences on subsequent performance. Livestock Production Science (Special issue) 78, 63-70. Ritacco, G., S.V. Radecki and P.A. Schokneht, 1997. Compensatory growth in runt pigs is not mediated by insulin-like growth factor 1. Journal of Animal Science, 75, 1237-1243. Robert, S. and G.P. Martineau, 2001. Effects of repeated cross-fostering on preweaning behavior and growth performance of piglets and on maternal behavior of sows. Journal of Animal Science, 79, 88-93. Rydhmer, L., 1992. Relation between piglet weights and survival. In: M.A. Varley, P.E.V. Williams and T.L.J. Lawrence (editors), Neonatal Survival and Growth, Occasional Publication of the British Society of Animal Production, 15, 183-184. Schneider, D. and K. Bronsch, 1973. Einfluss der stallbelegung nach der sog. Fleissbaud und Rein Raus Methode auf die Frekelaufzucht. Züchtungskunde, 50, 53-60. Schoknecht, P.A., S. Ebner, A. Skottner, D.G. Burrin, T.A. Davis, K. Ellis and W.G. Pong, 1997. Exogenous insulin-like growth factor-1 increases weight gain in intrauterine growth-retarded neonatal pigs. Pediatric Research, 42, 201-207. Sloat, D.A., D.C. Mahan and K.L. Roehrig, 1985. Effect of pig weaning weight on postweaning body composition. Nutrition Reports International 31, 627-634. Straw, B.E., E.J. Burgi, C.E. Dewey and C.O. Duran, 1998. Effects of extensive crossfostering on performance of pigs on a farm . Journal of the American Veterinary Medical Association 212, 855-856. Thompson, B.K. and D. Fraser, 1986. Variation in piglets weights: development of within-litter variation over a 5-week lactation and effect of farrowing crate design. Canadian Journal of Animal Science, 66, 361-372. Thompson, B.K. and D. Fraser, 1988. Variation in piglets weights: weight gains in the first days after birth and their relationship with later performance. Canadian Journal of Animal Science, 68, 581-590.

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Tribout, Th., J.C. Caritez, J. Cogué, J. Gruand, Y. Billon, J. Le Dividich, H. Quesnel and J.P. Bidanel, 2002. Estimation of realised genetic trends in french Large White pigs from 1997 to 1998 for male and female reproduction traits using stored frozen semen. Paper presented at 7th World Congress of Genetics Applied to Livestock Production. Montpellier, France. van Beers-Schreurs, H.M.G., L.L. Vellenga, Th. Wensing, and H.J. Breukink, 1992. The pathogenesis of the post-weaning syndrome in weaned piglets: A review. Veterinary Quarterly 14, 29-34. van der Lende, T., W. Hazelegen and D. de Jager, 1990. Weight distribution within litters at early fœtal age and at birth in relation to embryonic mortality in the pig. Livestock Production Science 26, 53-65. Vesseur, P.C., B. Kemp, L.A. den Hartog and J.P.T.M. Noodhuizen, 1997. Effect of split-weaning in first and second parity sows on sow and piglet performance. Livestock Production Science 49, 277-285. Veum, L. and J. Odle, 2001. Feeding neonatal pigs. In: A.J. Lewis and L.L. Southern (editors), Swine nutrition, CRC Press, pp. 671-690. Whang, K.Y., F.K. McKeith, S.W. Kim and R.A. Easter, 2000. Effect of starter feeding program on growth performance and gains of body components from weaning to market weight in swine. Journal of Animal Science 78, 2885-2895. White, K.R., D.M. Anderson and L.A. Bate, 1996. Increasing piglet survival thruogh an improved farrowing management protocol. Canadian Journal of Animal Science 76, 491-495. Wigmore, P.M.C. and N.C. Stickland, 1983. Muscle development in large and small fetuses. Journal of Anatomy 137, 235-245. Wise,T., R.T. Roberts and R.K. Christenson, 1997. Relationship of light and heavy fetuses to uterine position, placental weight, gestational age and fetal cholesterol concentrations. Journal of Animal Science 72, 2197-2207. Wolter, B.F. and M. Ellis, 2001. The effects of weaning and rate of growth immediately after weaning on subsequent pig growth performance and carcass characteristics. Canadian Journal of Animal Science 81, 363-369. Wolter, B.F., M. Ellis, B.P. Corrigan and J.M. Dedecker, 2002. The effect of birth weight and feeding supplemental milk replacer to piglets during lactation and postweaning growth performance and carcass characteristics. Journal of Animal Science 80, 301-308. Wootton, R., I.R. McFayden, and J.E. Cooper, 1977. Measurement of placental blood flow in the pig and its relation to placental and fetal weight. Biology of the Neonate 31, 333-339. Wu, M.C., S.Y. Chen, T.P. Yeh and T.C. Hsieh, 1985. Improvement of the baby pig performance and sow productivity by fractional early weaning. Taiwan Sugar 32, 13-15. Zijlstra, R.T., K.Y. Wang, R.A. Easter and J. Odle, 1996. Effect of feeding milk replacer to early-weaned pigs on growth, body composition, and small intestinal morphology, compared with suckled littermates. Journal of Animal Science 74, 2948-2959.

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15 Productivity and longevity of weaned sows A. Prunier, N. Soede, H. Quesnel and B. Kemp

15.1

Introduction

In modern pig producing systems, the reproductive life span of sows is close to 5 litters: 4.2 in the USA (Lucia et al., 1999), 4.7 in France (GTTT, 2000) and 5.4 in Great Britain (MLC, 1999). This average of 4 to 5 litters is well below the suggested optimum of about 7 to 8 litters (review: Gill, 2000). Interestingly enough, this figure does not seem to have changed in the last decades: Dagorn and Aumaître in 1979 reported an average sow life span of 4.2 litters in France and, Kroes and Male, also in 1979, reported an average of 4.6 litters per sow in The Netherlands. Therefore, the increase of on average 4.5 piglets weaned/sow/year over the last 20 years (GTTT, 1980 and 2000) does not seem to have resulted in a shorter reproductive life span. A proportion part of the females in a pig herd is culled for reproductive reasons, such as no estrus, failure to conceive, abortions, and small litters. These culls are of great economic importance for pig producers for many reasons. Females culled for reproductive reasons achieved a lower parity number, have a higher proportion of non-productive days and produce fewer weaned pigs, both per year of herd life and during their total herd life compared to females culled for any other reason (Dijkhuizen et al., 1989; Lucia et al., 2000). First-litter sows are well known for their reproductive problems. Field data show that these sows have the highest risk of a prolonged weaning-to-estrus interval and of low pregnancy rate after insemination (Vesseur et al., 1994a, b; Tummaruk et al., 2000), resulting in a high culling rate (Dijkhuizen et al., 1989). In second-litter sows, a relatively low litter size is frequent (the so-called ‘second-litter syndrome’; Morrow et al., 1992), which is also attributed to the reduced reproductive functioning of the sows after weaning their first litter. In this paper, an overview will be given of the reproductive causes of culling. Thereafter, the physiological consequences of lactation and weaning on the reproductive axis will be discussed. Subsequently, the major reproductive parameters for reproductive performance will be discussed, including the influence of internal and external factors on underlying reproductive parameters, such as ovulation rate and embryo survival.

15.2

Reproductive causes of culling

Reasons of sow culling have been analysed in numerous retrospective studies based on producer records in databases such as GTTT in France (Dagorn and Aumaître, 1979), VAMPP in the Netherlands (Dijkhuizen et al., 1989), NSRS in Norway (Sehested and Schjerve, 1996) and PigCHAMP in the USA (Koketsu et al., 1997a; Lucia et al., 2000). These studies have shown that a large proportion of culled sows is removed from herds for reproductive reasons, such as anestrus, failure to farrow

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385

386 39.2 36.4 34.2 33.0 33.7 28.7 31.2 33.8

Source

Dagorn & Aumaître, 1979 Zivkovic et al., 1986 Dijkhuizen et al., 1989 Bhatia, 1989 Lucia et al., 20001 Sehested & Schjerve, 1996 Heinonen et al., 1998

Mean

8.8

4.6 15.9 6.2 ? 14.1 4.0 7.9

Low litter size

4.5

6.3 ? ? ? 3.4 4.0 4.3

2Including

7.2

6.1 12.1 13.9 ? 4.9 4.8 3.4

Peripartum Low milk disorders3 production4

gilts anestrus, failure to conceive and abortion 3Including farrowing difficulties such as matritis and mastitis... 4Including poor litter growth, abnormal teat

1Including

Reproductive failure2

10.4

8.8 9.1 10.5 8.7 13.2 10.2 12.6

Locomotion

6.0

6.5 ? ? 8.0 7.4 4.2 3.9

Death

13.7

27.2 ? 11.0 8.4 8.7 11.3 15.5

Age

23.2

1.3 26.5 24.2 41.9 14.6 32.8 21.2

Other reasons

Table 15.1. Reasons for culling sows in commercial herds from different countries (percentage of culled sows).

France, 1975-1976 Yugoslavia, 1984 NL, 1985-1986 India USA, 1992 Norway, 1992-1994 Finland, 1992/1993

Country and year

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Productivity and longevity of weaned sows

and small litters. These reproductive reasons account for 33 to 52% of the total culls, and even add up to 43-64% if mothering ability (peripartum disorders, agalactia or low milk production) is added (Table 15.1). When looking more carefully at the reproductive reasons of culling, data show that failure to conceive or to farrow are the main causes accounting each for nearly one third of the culls (Table 15.2). Anestrus (including silent ovulation) is another important reason which represents nearly 25% of the culls for reproductive failure. Besides culling for reproduction, other main causes for culling are: old age (8-27% of total culls), locomotion disorders (8-13% of total culls) and death (4-8% of total culls) (Table 15.1).

Table 15.2. Reasons for culling sows in commercial herds within the reproductive failure category (percentage of sows).

Source

Failure to Anestrus conceive2

Failure to farrow3 Abortion Country and year

Koketsu et al., 1997a Sehested & Schjerve, 1996 Lucia et al., 20001 Heinonen et al., 1998

25.2 23.4 27.0 22.3

30.4 36.8 33.34

37.1 31.7 39.7 77.75

7.4 8.0

USA, 1991 Norway, 1992-1994 USA, 1992 Finland, 1992/1993

1Including

gilts return to heat (18-25 days after service) 3Abnormal return to heat (>25 days after service) 4Including abortion 5Including failure to farrow and abortion 2Normal

As could be expected, reasons for culling vary with parity of the females. “True” reproductive disorders (anestrus + failure to conceive/farrow + low litter size at birth) account for nearly 40% of total culls in young sows (parities 1 and 2) and only for 17% in old ones (parity > 7); (Figure 15.1). However, when sows that are culled because of their age are excluded from the analyses, the difference in the reasons for culling between young and old sows is much smaller. For instance, it can be calculated from Norwegian data that nearly 40% of first-parity sows are culled for “true” reproductive disorders versus 34% of sows whose parity is higher than 7, when the age reason is excluded (Sehested and Schjerve, 1996). A potential limitation of studies from database analyses is the fact that definitions of removal reasons are not standardised and, very often, sows are not culled for a single reason but for several reasons. For instance, an old sow with low productivity and lameness may be culled for low mothering ability, for lameness and for its

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Figure 15.1. Influence of the parity on the reasons of culling in Landrace x Yorkshire sows (based on Sehested and Schjerve, 1996).

age. However, the producer has to choose only one reason. This may underestimate one parameter and overestimate the other. Moreover, producers may falsely diagnose reproductive failures. Geudeke (1992), for example, examined genital tracts of 5969 sows. Of the 13.7% sows that were culled for anestrus, almost 60% had normal ovaries, 16.9% had inactive ovaries and 25.3% had cystic ovaries.

15.3

Consequences of lactation and weaning on the reproductive axis

Lactation normally almost completely inhibits the activity of the reproductive axis. Weaning removes this inhibition and thus results in estrus behaviour and ovulation (reviews: Britt et al., 1985; Varley and Foxcroft, 1990; Quesnel and Prunier, 1995). Under specific conditions, lactational estrus and ovulation may occur (see further). 15.3.1

Postpartum inhibition

15.3.1.1 Long-term effects of pregnancy and farrowing Weaning piglets at birth, instead of at 3 to 5 weeks of age, results in a higher incidence of anestrus and cystic ovaries, a longer weaning-to-estrus (weaning-to-service) interval, or a reduced litter size (Peters et al., 1969; Elliot et al., 1980; Varley and Atkinson, 1985). This suggests that physiological events associated with pregnancy and farrowing have an inhibitory influence on the reproductive axis.

388

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During the last month of pregnancy, LH secretion is inhibited by the high concentrations of progesterone synthesized by corpora lutea and probably also by the high levels of estrogens originating from the feto-placental units. Farrowing is accompanied by a drop in progesterone and estrogen concentrations and is followed by an immediate increase in gonadotropin secretion in suckled sows and in sows weaned immediately after farrowing (zero-weaned sows; Smith et al., 1992; De Rensis et al., 1993a). Therefore, postpartum anestrus in zero-weaned sows is not related to an impaired secretion of gonadotropins just after farrowing, as observed in domestic ruminants. Anestrus and cystic follicles can be due to the lack of a preovulatory LH-surge resulting from either the high levels of corticosteroids observed in early-weaned sows (Ryan and Raeside, 1991) or an impaired responsiveness to positive feedback effects of estradiol-17β at the hypothalamicpituitary level (Elsaesser and Parvizi 1980; Cox et al. 1988; Sesti and Britt 1993). This responsiveness is partially recovered between the third and the fourth weeks of lactation. Decreased responsiveness of the pituitary in early lactation may be partly related to LH stores in the pituitary gland, that are depleted just after farrowing and progressively restored during lactation (Crighton and Lamming 1969; Bevers et al. 1981). However, the pituitary answer to the positive feedback of estrogens has not been investigated in zero-weaned sows. Another long-term effect of gestation on the reproductive axis involves the uterus, which was submitted to considerable changes during gestation. The uterine involution is rapid during the first week postpartum (p.p.) but is completely achieved only within 21 to 28 days p.p. in lactating sows (Palmer et al., 1965a, b; Smidt et al., 1969). In early-weaned sows (4 days p.p.), the involution is still slower (Smidt et al., 1969). Therefore, the morphology and physiology of the genital tract may not be optimal for fertilization and blastocyst implantation in sows weaned at farrowing or shortly after, resulting in a reduced rate of gestation (and a longer weaning-to-service interval) or a reduced litter size. 15.3.1.2 Influence of suckling Mean concentrations of circulating LH are high during the two or three days following parturition and then decrease in lactating sows (Tokach et al., 1992; De Rensis et al., 1993a, b). These concentrations and the number of LH pulses remain low during early lactation, from about day 4 to 14, and gradually increase thereafter (Stevenson et al., 1981; Shaw and Foxcroft, 1985; De Rensis et al., 1993b). There is consistent evidence that suckling (stimulation of the teats by the piglets) and piglet proximity provide physical and behavioural stimuli to the sow that induce the release of neurotransmitters and opioid peptides, through neuroendocrine reflexes (review: Kraeling and Barb 1990). These factors stimulate the secretion of pituitary hormones involved in milk ejection and production (e.g. oxytocin,

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prolactin, growth hormone, cortisol) and suppress LH secretion by inhibiting the GnRH pulse generator. The suckling-induced inhibition of LH begins only within two or three days p.p. (De Rensis et al., 1993a). It is mainly due to endogenous opioids during established lactation, whereas its development during the early p.p. period appears to be opioid-independent (De Rensis et al., 1993b, 1998a). In addition to the opioidergic system, a dopaminergic regulation of LH secretion exists during the fourth week of lactation as shown by De Rensis et al. (1998b). However, these authors provided evidence that prolactin itself was not involved in the control of the GnRH/LH secretion during lactation. This is in contradiction with the prevailing hypothesis suggesting that prolactin may partly inhibit LH release during lactation (reviews: Van de Wiel et al., 1985; Dusza and Tilton, 1990). The progressive decrease in the inhibition of LH secretion could be related to a decrease in suckling frequency and intensity over the four weeks of lactation (Pederson et al., 1998; Jensen et Recén 1989) and could be related to the increase in the pituitary LH response to GnRH as lactation progresses (Bevers et al., 1981; Rojanasthien et al., 1987a). Data on the variation in FSH secretion during lactation are less consistent. Within the three days following parturition, FSH concentrations do not vary with time and are similar in suckled and zero-weaned sows (De Rensis et al., 1993a). From the second week of lactation onwards, a continuous increase in plasma FSH has been observed by Stevenson et al. (1981) and De Rensis et al. (1993b). Ovariectomy during lactation is accompanied by an increase in FSH concentrations without affecting LH secretion (Stevenson et al., 1981), demonstrating that FSH secretion is more controlled by the ovarian negative feedback (presumably by inhibin) than by suckling. In suckled sows, large follicles (> 5 mm) are present in the ovaries during the first week p.p. and are replaced by small and medium-sized follicles (3-4 mm) during the second week (Crighton and Lamming, 1969; Kunavongkrit et al., 1982; Rojanasthien et al., 1987b). During the third and fourth weeks of lactation, follicular growth resumes as a consequence of the progressive increase in LH pulse frequency but most follicles are < 5 mm in diameter (review: Britt et al., 1985). Because of the inhibition of follicular growth, circulating estrogens are generally low (Baldwin and Stabenfeldt, 1975; Kirkwood et al., 1984; Prunier et al., 1993). Beside this general pattern of follicular growth during lactation, Lucy et al. (2001) reported differences in follicular development between sows before weaning using ultrasonography. Sows can have relatively inactive ovaries (follicles less than 2 mm in diameter) or have large follicles present.

390

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Ovulation can be induced during lactation by administration of exogenous gonadotropins (review: Britt et al., 1985). Reduced follicular growth during lactation is thus primarily due to low gonadotrophic signal. However, other factors can act directly at the ovarian level for instance, by modulating the follicular responsiveness to gonadotropins. 15.3.1.3 Influence of the metabolic status During lactation, sows are usually fed ad libitum or close to ad libitum and their voluntary feed intake increases during the first three weeks postpartum (review: Dourmad, 1988). Energy requirements for milk production simultaneously increase and peak during the third week of lactation (Noblet and Etienne 1986). Voluntary feed intake depends on numerous endogenous and environmental factors (review: Dourmad, 1988; Eissen et al., 2000) and is often not sufficient to meet the high energy and nutrient requirements for milk production. This appears to be particularly true in high-yielding multiparous sows and in most first-litter sows, that have a lower feed intake than multiparous sows but a relatively high milk production (> 7-8 kg/day). The energy balance of these sows is thus negative throughout lactation. A slight catabolic state does not affect gonadotropin secretion, even in first-litter sows, as evidenced in lactating sows that consume between 80 and 90% of the metabolic energy requirements for maintenance and milk production (review: Prunier and Quesnel, 2000). Moreover, making sows anabolic during lactation, by superalimentation via a stomach cannula, did not alleviate the negative impact of suckling on LH secretion around weaning and did not improve reproductive performance after weaning, as shown by Zak et al. (1998). In their experiment, however, the control sows already had a good reproductive performance. In contrast, a strong catabolic condition during lactation has been clearly demonstrated to inhibit the activity of the hypothalamo-pituitary complex in primiparous sows. Indeed, restriction of feed (Reese et al., 1982; Zak et al., 1997a; Quesnel et al., 1998a), energy (Armstrong et al., 1986a; Koketsu et al., 1996a) or protein (King and Martin, 1989; Jones and Stahly, 1999a; Yang et al., 2000a) generally inhibit the secretion of LH during lactation and delay estrus after weaning. Lactation induces metabolic adaptations that favour the preferential drive of nutrients towards mammary glands. Concentrations of prolactin, growth hormone (GH), insulin-like growth factor-I (IGF-I) and insulin are relatively high during lactation due to suckling and high feed consumption. During the course of lactation, prolactin, GH and IGF-I decline slowly, possibly due to attenuated intensity of suckling stimuli (Rojkittikhun et al., 1993; Schams et al., 1994). Plasma glucose, insulin, IGF-I and leptin also decrease throughout lactation in those sows with increasing nutritional deficit and body reserve mobilization (Prunier et al., 1993; Messias de Bragança and Prunier, 1999; Van den Brand et al., 2001; Prunier et al., 2001). Metabolic adaptations have been extensively described in primiparous sows submitted to a

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severe level of nutritional restriction during lactation. Compared with well-fed sows, feed-restricted sows have lower plasma insulin, IGF-I and leptin but higher plasma NEFA and GH (Koketsu et al., 1996a; Zak et al., 1997a; Quesnel et al., 1998a; Mao et al., 1999). Obviously, the GH-IGF-I axis becomes uncoupled. Together with low insulin, this favors maternal catabolism. There is increasing evidence that these changes in metabolites and metabolic hormones signal to the reproductive axis the changes in metabolic state (reviews: Booth, 1990; Pettigrew and Tokach, 1993; Prunier and Quesnel, 2000). Amongst these potential mediators, glucose, insulin and IGF-I could play a preferential role. A strong reduction in glucose and/or insulin has been associated with inhibited secretion of LH in prepuberal gilts submitted to severe feed-restriction or to experimentally-induced glucose restriction (Booth, 1990; Barb, 1999) and in diabetic gilts (Angell et al., 1996). In lactating sows, LH pulsatility around weaning has been positively related either to insulin (Quesnel et al., 1998b) or IGF-I (Van den Brand et al., 2001). Feeding a carbohydrate-rich diet increases LH pulsatility during early lactation (day 7) but not later in lactation (days 14 or 21) despite higher post-feeding insulin levels at both stages (Kemp et al., 1995; Van den Brand et al., 2000a). Evidence is still lacking that reduced insulin alters LH pulses in catabolic lactating sows. At the ovarian level, consistent evidence exists that insulin and IGF-I stimulate follicular responsiveness to gonadotropins and folliculogenesis (Adashi et al., 1992). Therefore, reduced concentrations of insulin and IGF-I in plasma and/or follicles observed in feedrestricted lactating sows (Quesnel et al., 1998a, b) may reduce the ovarian response to the gonadotropic stimulation at weaning and alter subsequent follicular development. Indeed, Quesnel et al. (1998a, b) have observed that feed restriction during lactation induces a reduction in insulin, IGF-I and LH concentrations at day 27 of lactation. This results in a concomitant decrease in the number of follicles measuring at least 4 mm in diameter and in the proportion of healthy 1-3 mm follicles at weaning (day 28). Similarly, Clowes et al. (1999) have shown that protein restriction of primiparous sows has a negative influence on the number of large follicles (4 to 6 mm) on day 23 of lactation. Moreover, follicular fluid from these sows has a lower potential to support in vitro nuclear maturation of oocytes. 15.3.2

Removal of the inhibition of the hypothalamic-pituitary-ovarian axis at weaning

Weaning piglets suppresses the inhibitions originating from the suckling stimuli and from the potential catabolic status. This results in an immediate and transient increase in mean concentrations of LH and LH pulse frequency ovulation (reviews: Britt et al., 1985; Varley and Foxcroft, 1990; Quesnel and Prunier, 1995). Increased secretion of FSH in response to weaning has been observed in some experiments (Cox and Britt, 1982; Shaw and Foxcroft, 1985) but not in others (Stevenson et al., 1981; Edwards and Foxcroft, 1983; Foxcroft et al., 1987). This divergence between

392

Weaning the pig

Productivity and longevity of weaned sows

LH and FSH profiles around weaning supports the existence of different controls of gonadotropin secretion: LH secretion mainly depends on suckling and lactation influences, whereas FSH mainly depends on ovarian negative feedback. The increase in gonadotropin secretion at weaning stimulates follicular growth and maturation, as evidenced by the immediate increase in the number and size of large follicles (diameter > 5 mm) after weaning (Palmer et al., 1965a; Cox and Britt, 1982; Armstrong et al., 1986b). Relatively high concentrations of estradiol-17β and testosterone are measured in follicles 24-48 hours after weaning (Foxcroft et al., 1987; Killen et al., 1992). Plasma estradiol-17β rises significantly within 24-48 hours after weaning in sows with a normal return to estrus (Rojanasthien, 1988; Tsuma et al., 1995). Similarly, concentrations of inhibin in both plasma and follicular fluid progressively rise during the first two days after weaning (Trout et al., 1992). As during the follicular phase of the estrous cycle, high circulating concentrations of estradiol-17β induce estrous behaviour, the preovulatory surge of gonadotropins and then ovulation. However, a marked variability between sows is observed in post-weaning follicular development (Foxcroft et al., 1987). It is likely that this is related to the variation in the weaning-to-estrus interval and/or in the ovulation rate. Stimulation of LH secretion at weaning occurs in most sows, even when they were strongly catabolic during lactation (Zak et al., 1997a; Quesnel et al., 1998a). The amplitude of the increase is not necessarily related to the degree of inhibition of LH during lactation (Zak et al., 1997a). The interval between weaning and estrus was mainly related to mean or episodic secretion of LH during mid-lactation or just before weaning in several experiments in which primiparous sows belonged to a single population (Shaw and Foxcroft, 1985; Tokach et al., 1992) and in which LH secretion during lactation was altered by nutritional treatments (Armstrong et al., 1986a; Koketsu et al., 1996a; Zak et al., 1997a). This suggests that the degree of inhibition of LH during lactation influences the resumption of ovarian activity after weaning. However, several papers also describe a positive relationship between postweaning LH and subsequent WEI. For example, Van den Brand et al. (2000a) found that this relation was linear for sows with a low number of LH pulses (< 8 pulses/12 h) whereas sows with a higher number of LH pulses had the same short WEI. Postweaning ovarian activity could also be modulated by the concentrations of metabolic hormones during lactation (see 15.3.1) per se. Supporting that, alterations in post-weaning ovulation rate and/or embryo survival were reported regardless of variations in LH secretion around weaning (feed restriction: Zak et al., 1997a, b; lysine/protein restriction: Mejia-Guadarrama et al., 2001). Based on the kinetic and hormonal regulation of follicular growth, it is likely that FSH and LH induce follicle recruitment immediately after piglet removal. These follicles that ovulate 4 to 7 days later are healthy follicles measuring 2-3 mm at weaning. It is probable that their number will influence the ovulation rate at first post-weaning estrus and that their

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characteristics (‘quality’) could have consequences on the oocyte development and/or on the luteinization process of the follicular cells, thus modulating fertilization rate and embryo survival. In addition, the hormonal background existing after weaning may influence the process of recruitment and maturation of the preovulatory follicles. Therefore, both lactational and post-weaning events may act on the reproductive performance of primiparous and multiparous sows. However, if the lactation period does not have profound negative effects on LH secretion or follicle development, no detrimental effects of lactation on post-weaning performance are expected and effects of post-weaning events will be limited.

15.4

Variation in reproductive performance: extent and sources of variation

15.4.1

Components of fertility and prolificacy

Fertility and prolificacy of sows can be influenced by many factors, including internal (e.g. genetic factors, parity, body reserves, milk production) or environmental factors (e.g. stress, light, ambient temperature, light, housing) as well as management decisions (e.g. length of lactation, level of feeding). Field data give information especially on the effects of parity, genotype, litter size, length of lactation and season on the weaning-to-estrus interval, litter size and farrowing rate or longevity of sows (e.g. Koketsu et al., 1997a, b; Le Cozler et al., 1997; Lucia et al., 2000). Information on the influence of internal or environmental factors acting during lactation on the underlying components of farrowing rate and litter size, that is ovulation rate, fertilization rate, embryo survival and fetal survival comes from experimental herds. In the following paragraphs, effects of factors acting either during lactation or after weaning on the reproductive function will be summarised. However, it should be noticed that most of field or experimental data concern factors acting during lactation. 15.4.2

Influence of nutritional factors

15.4.2.1 Influence of nutrient supply Feed supply during lactation has often been found to affect WEI, and also ovulation rate and embryo survival, resulting in effects on pregnancy (farrowing) rate and litter size but the effects can be very variable from study to study (Table 15.3). A low feeding level during lactation increased WEI in most studies, but significantly in only 4 out of 8. It significantly decreased ovulation rate in only one study, embryo survival in three studies and pregnancy rate in two studies. Therefore, effects of low feeding levels on WEI are more consistent than their effects on ovulation rate, embryo survival and pregnancy rate. Even in modern crossbred primiparous sows (studies

394

Weaning the pig

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in Table 15.3 from 1997 onwards) very different effects can be found: no effects (Quesnel and Prunier, 1998); effects on WEI only (Zak et al., 1998); effects on ovulation rate and embryo survival (Zak et al., 1997a), or effects on ovulation rate only (Van den Brand et al., 2000a). It is not easy to verify the causes of this variability.

Table 15.3. Influence of feed supply during lactation or after weaning on liveweight at weaning (LW, kg), subsequent weaning-to-estrus interval (WEI, days), ovulation rate, embryo survival at day 25 to 35 of pregnancy (ES) or litter size (LS) in brackets and, pregnancy rate (PR) or farrowing rate (FR) in brackets. Feed sup.(%)a LW at weaning WEI

Ovulation rate ESb (LS)

PR (FR)

Low

High Low High

Low

High Low High

Low Sourcec

During lactation 85 40 135 85 45 ~200 80 40 ~177 80 45 199 80 45d 179 d 45 90 60 210 85 50 163 79 67 152

108 ~180 ~164 176 162 172 194 137 145

7.6 4.3 6.0 5.9 3.7

(9.7) 83 83 85 88

5.7 4.2 5.1

13.5 18.6 17.7 16.7 15.4* 15.4* 20.7 15.6 16.2†

(89) 69* 77† 62* 100 100 100 -

After weaning 285 115 122 245 155 199

121 199

9.1 8.2 15.2 13.4 14.1 14.6 6.0 5.9 16.6

High

Low

High

19.9* 14.4 5.8* 18.1 8.9* 17.6 7.5 16.2 5.6 19.9 5.1 5.9 19.2 6.3* 14.4 5.7 18.1

83 68

(9.7) 68† 72* 64* 87 64* 72 68

(79) 90 89 82 100 100 -

14.8 13.2* (10.0) (9.5) (76) 16.2 78 85 87

(1) (2) (3) (4)d (5) (5) (6) (7) (8)

(9) (92) (1) 82 (4)d

a

For effects of feed supply during lactation, animals were restricted after lactation. For effects of feed supply after lactation, animals were full fed during lactation. Feed supply (%) is the estimated ratio between metabolic energy intake and requirements for maintenance in weaned sows and for maintenance + milk production in lactating sows (see Prunier and Quesnel, 2000). b (1) King and Williams, 1984 (2) Kirkwood et al., 1987 (3) Kirkwood et al., 1990 (4) Baidoo et al., 1992 (5) Zak et al., 1997a (6) Quesnel and Prunier, 1998 (7) Zak et al., 1998 (8) Van den Brand et al., 2000a (9) Den Hartog and van der Steen, 1981. c Percentage of viable embryos to number of corpora lutea. d Low feed intake (5% of ME requirements) was imposed during the first three weeks of lactation (first line of data) or last (4th) week of lactation (second line of data). * P < 0.05, † P < 0.05.

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It is dependent on the reproductive performance of the control group (which is quite different from experiment to experiment), and may be related to factors such as body condition at farrowing, litter size, litter gain, lactation length, degree of feed restriction, weight loss during lactation etc. It seems reasonable to suggest that a more severe energy deficit during lactation will have larger effects on WEI, ovulation rate and embryo survival. Data from King and Dunkin (1986a) corroborate this relationship between the degree of feed restriction and the effect on WEI. They compared 6 levels of feed consumption during lactation of first-litter sows, and observed that the proportion of sows exhibiting estrus within 8 days of weaning was 83% at the highest feeding level and decreased linearly with daily feed intake to only 8%. Contrarily, they did not find any influence of the feed intake on ovulation rate. This may be due to the fact that the WEI was relatively long in all their experimental groups. Data from Table 15.3 show that the decrease in the ovulation rate in restricted sows was significant or close to significance only when weaning-to-estrus interval was short (Zak et al., 1997a; Van den Brand et al., 2000a). Therefore, factors imposed during lactation have decreasing effects on the postweaning ovulation rate when the WEI increases. Such a conclusion can not be drawn regarding the effects of feed restriction on embryo survival and pregnancy rate. The effects of lactational feed intake on ovulation rate seem to be associated with altered follicular development at the time of weaning, which itself may depend on the hormonal background at that time (see 15.3.2). Data obtained in gilts by Soede et al. (2000) corroborate this hypothesis. These authors found that a feed restriction of 60% of ad libitum feed intake during the last week of progesterone dominance (Regumate®) resulted in fewer large follicles at the last day of treatment (follicles larger than 4.5 mm/ovary: 4.2 vs. 9.5) and in lower subsequent ovulation rate (14.8 vs. 17.2) without any influence on the interval between Regumate® cessation and ovulation. Almeida et al. (2000) restricted feed intake during the second week of the luteal phase and did not find effects on ovulation rate, but found significant effects on progesterone rise during early pregnancy and subsequent embryo survival rate (68% vs 83%). Similarly, the hormonal background existing during lactation may influence quality of the oocytes and hence the subsequent embryo survival and pregnancy rate. Analyses of farm data have shown that the feed intake pattern during lactation is another important factor influencing subsequent reproductive processes. Farm data on feed intake patterns were analyzed by Koketsu et al. (1996b, c) who distinguished 6 feed intake patterns: Rapid (rapid increase in feed intake after farrowing, 23% of lactating sows); Major (major drop in feed intake during lactation, 33% of sows); Minor (minor drop, 28% of sows); LLL (low feed intake throughout lactation, 1% of sows); LHH (low feed intake during the first week then increasing for the remainder of lactation, (1% of sows); and Gradual (gradual increase in feed intake throughout lactation, 15% of sows). Analyses of subsequent reproductive

396

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performance revealed that sows showing either a rapid or gradual increase in feed intake with no drop (or either a minor drop in feed intake) during the course of lactation had the lowest weaning-to-conception interval and had a lower risk to be culled due to anestrus. In sows that show a marked drop in feed intake at any time during lactation, reproductive output was decreased. The authors concluded that both the average daily feed intake and the feed intake pattern influenced reproductive performance. Experimental data also show that restricted feeding during different parts of lactation differentially affect reproductive performance. In first-litter sows, Koketsu et al. (1996a) restricted energy intake during the whole lactation or during either the first, second or third week of lactation (diets were adjusted to ensure that energy intake was restricted by 60%, but lysine intake was not restricted). The rather severe restriction of energy intake during the second, third or whole lactation significantly increased WEI (from on average 9 days to 18 to 23 days), whereas restriction in the first week of lactation resulted in an intermediate WEI of on average 14 days. No other parameters for reproductive performance were assessed. Zak et al. (1997a) also varied the timing of feed restriction in primiparous sows weaned at 4 weeks of lactation. Sows were fed to appetite (= “control” group) or were submitted to feed restriction (about 50% of ad libitum intake) either between parturition and day 21 (= group “refed”) or between day 22 and day 28 (group “restricted”). In this experiment, “refed” sows showed a significant increase in WEI (from 3.7 to 5.6 days) and a decrease in ovulation rate (from 19.9 to 15.4) but embryo survival was not affected (from 88 to 86), whereas “restricted” sows showed an increase in WEI (to 5.1 days), and decreases in ovulation rate (to 15.4) and embryo survival (to 64 %). In a second experiment using a similar protocol, Zak et al. (1997b) compared the ability of the oocytes of the 15 largest follicles to mature in vitro as well as the ability of the follicles > 3 mm to support oocyte nuclear maturation. Sows in the “restricted” group had fewer oocytes to mature in the Metaphase II stage of meiosis than “refed” sows. Further, control oocytes matured less well in the follicular fluid obtained from the ovarian follicles of the “restricted” sows than of the “refed” sows. However, data showing that the ability of the ovocytes to mature in vitro is closely linked to their ability to mature in vivo are still missing. Data concerning the effects of feed supply after weaning on the subsequent reproductive performance are scarce. The only significant effect observed was a lower ovulation rate in restricted sows in one study (Table 15.3). This effect may be related to an influence of the hormonal background existing after weaning on the recruitment process (see 15.3.2). Indeed, ovulation rate can be increased by insulin treatment after weaning which reduces the rate of atresia of selected follicles (for review: Cox, 1997).

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15.4.2.2 Influence of the composition of the diet Proteins Protein demand during lactation is high because of the protein demand for milk production. The first limiting essential amino acid in most diets is lysine, and daily lysine intake is therefore often taken as a primary determinant of lactation performance. Low protein intake during lactation results in mobilization of significant amounts of maternal body protein and in decreased milk production (Jones and Stahly, 1999b). Numerous experiments have shown that a low protein intake during first lactation (but with high energy intake) increases the subsequent WEI (20 vs. 11 days in King and Williams, 1984; 13.9 vs. 8.4 in Jones and Stahly, 1999a) and decreases the percentage of sows expressing estrus within 8 days from weaning (41 vs. 59% in King and Dunkin, 1986b; 33 vs. 83 % in King and Martin, 1989) or within 7 days from weaning (60 vs. 88 % in Brendemuhl et al., 1987) without clear effect on ovulation rate or litter size. In contrast, in two more recent experiments, protein/lysine restriction had no clear influence on the interval between weaning and prestrus (Yang et al., 2000b) or estrus (Mejia-Guadarrama et al., 2001), but affected follicular development and/or ovulation rate. Indeed, ovulation rate was lower at the postweaning estrus in restricted compared to control sows (20.0 vs. 23.4, Mejia-Guadarrama et al., 2001). Moreover, protein/lysine restriction during lactation retarded growth of preovulatory follicles collected at the postweaning prestrus and reduced their ability to support oocyte maturation (Yang et al., 2000c). Long term effects of protein/lysine deficiency during lactation have been tested by Yang et al. (2000b). They compared five levels of lysine (0.60, 0.85, 1.10, 1.35 and 1.60%) over three successive parities. Increasing dietary lysine/protein linearly decreased voluntary feed intake; e.g. in the first-litter sows from 5.4 to 4.6 kg. In their study, dietary lysine did not affect WEI (which was on average 5.8, 4.7 and 4.1 days for parity 1, 2 and 3, respectively) or farrowing rate (75.2%, 74.8% and 84.4% for parity 1, 2 and 3, respectively). However, lysine levels during lactation affected subsequent litter size, the effect depending on parity: second litter size decreased linearly with the increase in dietary lysine during first lactation whereas, third and fourth litter sizes were lowest in sows receiving 0.85 g of lysine/day. Numerous authors have used two-factorial designs in order to test whether the effects of protein and energy intakes during lactation on reproductive performance may interact (King and Williams, 1984, King and Dunkin, 1986b; Brendemuhl et al., 1987). Results show that the effects of protein intake on reproduction were rather similar at the high and low level of energy intake suggesting that there was no interaction between energy and proteins. It has been suggested that increasing lysine/protein intake in lactating sows above the nutritional requirements could improve the reproductive performance after

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weaning. Some experiments support this hypothesis (reduced WEI: Wilson et al., 1996; increased litter size: Tritton et al., 1996) but not others (littersize: Touchette et al., 1998; Yang et al., 2000b; hormone profiles during lactation: Yang et al., 2000a; follicular maturation at proestrus: Yang et al. 2000c; WEI: Yang et al., 2000b). Therefore, no or only little improvement can be expected from high protein/lysine regimen during lactation. Starch/Fat Increasing the energy content of sow lactational diets may reduce mobilization of body stores during lactation even though a decrease in feed intake is often observed. Indeed, high fat diets allowed total ME intake to increase by 3 to 32% (12% as a mean) in high-parity sows (Drochner, 1989) and by on average 4.4 MJ (less than 10% fat added) to 6.5 MJ (more than 10% added fat) (Pettigrew and Moser, 1991). Van den Brand et al. (2000c) measured energy and protein balances in primiparous, isocalorically fed sows with diets containing 13.5% fat as compared to diets with 3.4% fat at two different feeding levels. At high feeding levels, the fat-rich diet resulted in higher body fat loss without any clear effect on reproductive performance (Table 15.4). Therefore, fat-rich diets do not reduce mobilization of body stores, but in fact increase the mobilization of body stores and thus are not expected to improve reproductive performance in practice. However, it is conceivable that in circumstances where the voluntary feed intake is very low (e.g. high ambient temperatures), the extra uptake of energy when using fat-rich diets will be beneficial for the sows.

Table 15.4. Effect of feeding level and fat level of the diet on partitioning of energy in first-litter sows during a 21 day lactation period (based on Van den Brand et al., 2000a, b, c). Energy intake/day

62.8 MJ ME

Diet

Fat

Starch

Fat

Starch

Sow losses during lactation Protein (g/d) Fat (g/d) WEI (h) Ovulation rate Embryo survival (%)

50 584a 123 17.9u 75

31 401b 122 18.2u 66

69 511a 152 15.5v 65

75 521a 130 16.9v 70

ab uv

47.1 MJ ME

P < 0.05 P < 0.10

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In the experiment of Van den Brand et al. (2000c), a starch-rich diet was expected to be beneficial for reproductive performance since one of the important mediators between nutrition and reproduction could be insulin (see 15.3.1.3.). The starchrich diet was found to result in a higher and more prolonged insulin release (Van den Brand et al., 1998). However, neither weaning-to-estrus interval, nor ovulation rate, nor peri-estrus hormone profiles, nor embryo survival during subsequent pregnancy were influenced by the diet (Table 15.4). 15.4.2.3 Influence of body stores As has been discussed in 15.4.2.1., the level of feed intake during lactation has important consequences for subsequent reproductive performance. An important question is whether these effects are influenced by the levels of body stores, either at the onset of lactation or at the end of lactation. Several studies have been performed trying to reveal the relative importance of factors such as body stores of protein and/or fat at farrowing, body stores of protein and/or fat at weaning, protein losses during lactation and fat losses during lactation for post-weaning reproductive performance. Effects of body condition at farrowing have mostly been studied in relation to weaning-to-estrus interval and in first-litter sows. Results are ambiguous: Mullan and Williams (1989), Weldon et al. (1994), Le Cozler et al. (1998 and 1999) found no effect of body condition on WEI; Prunier et al. (2001) did not observe alteration in gonadotropin release and ovarian development at the end of lactation; Yang et al. (1989) and Dourmad (1991) found a longer WEI in thin sows, whereas Xue et al. (1997) found a longer WEI in fat sows. In fact, there is a negative relationship between fatness at farrowing and appetite during lactation. Therefore, it is likely that the influence of body stores at farrowing on the post-weaning performance depends on their negative impact during lactation, being inhibitory only when this effect is very marked as illustrated by the following experiments. Firstly, Xue et al. (1997) compared two levels of feeding during gestation (46 vs. 27.2 MJ ME/day) which produced backfat depth at farrowing of 30.5 and 25.5 mm in average. During lactation, spontaneous feed intake was highly reduced in fatter sows (-29 %) and resulted in a similar body weight at weaning at day 21 (approximately 163 kg), but backfat was still higher in sows which were fatter at farrowing (23 vs. 17.5 mm). At day 15 of lactation, basal and peak levels of insulin after glucose infusion were lower in fatter sows. At days 7 and 14 of lactation, LH release was impaired in the fatter sows and the WEI tended to be longer (8.0 vs. 6.4 days). The authors suggest that the increase in WEI in the sows with high gestational energy intake was a result of the low feed intake during lactation through an interaction of insulin with LH-secretion. Secondly, Le Cozler et al. (1998, 1999) compared two levels of feeding during rearing which resulted in two levels of backfat at farrowing (23.7 vs. 17.4 mm in 1998; 22.4 vs. 20.7 mm in 1999). They observed

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that feed intake was only slightly reduced during lactation (- 8% in Le Cozler et al., 1998; -3 % in Le Cozler et al., 1999) in fatter sows and did not show any influence of fatness on the WEI and subsequent litter size. Yang et al. (1989) tried to determine the respective effects of body stores at parturition and at weaning on reproductive performance in sows over four parities. To achieve this, two levels of feeding were used during gestation in order to reach 12 or 20 mm of backfat (P2) at farrowing. These levels were combined with two levels of feeding (ad libitum or restricted at 3 kg/day) during lactation and two sizes of sucking litters (6 vs. 10 piglets). All three factors significantly influenced backfat at subsequent weaning, changes in backfat during lactation, sow live weight at weaning and changes in sow live weight during lactation. Sows which were fatter at farrowing had a lower ad libitum feed intake during lactation over the 4 parities (-23%) but this difference was much lower in first-litter sows (-7%). In these latter sows, WEI was influenced by fatness at parturition and by feed intake during lactation but not by litter size. A significant relationship was also found between fatness at weaning (P2 in mm) and WEI (WEI = 26.6 (s.e. 4.7) - 1.28 (s.e. 0.39) x P2 (r.s.d. 3.5)). No other relationships of body stores with WEI were presented. When looking at the percentage of primiparous sows in estrus within 8 days after weaning, there was a strong interaction between fatness at farrowing and feed intake during lactation: this percentage was highly reduced only in sows which were thin at farrowing and were restricted during lactation (30 vs. 83% in average for the three other groups). In later parities, only litter size during lactation influenced WEI (6.0 vs. 8.0 days for 6 vs. 10 piglets). In summary, reproductive performance of sows after weaning may be influenced by fatness at farrowing in interaction with feed intake during lactation. Extremely fat and extremely thin primiparous sows should both be avoided. 15.4.2.4 Conclusion In most studies, return-to-estrus after weaning is delayed by low feed intake and by low energy or protein intakes. For ovulation rate, the effects are less clear: in older studies, no effects on ovulation rate were found and in recent studies, ovulation rate was frequently decreased by both feed and protein restriction. For oocyte maturation and embryonic survival, data are scarce and comes only from studies published in the last five years. Both feed and protein deficiency during lactation can have negative effects on these parameters.

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15.4.3

Influence of lactational characteristics

15.4.3.1 Litter size Reducing litter size decreases the suckling intensity and lowers the risk of nutritional deficit and hence may improve the reproductive performance of sows after weaning. Indeed, in their experimental farm, Vesseur et al. (1994b) observed that sows with a larger litter size at weaning had a longer WEI (8.3 days vs. 7.5 days for sows weaning 11-12 vs. 7-8 pigs respectively). However, the percentage of anestrous sows which were treated with gonadotropins to induce heat was not influenced by the litter size at weaning. Similarly, in a retrospective study based on farm data, Koketsu et al. (1997a) observed that neither the percentage of anestrous sows nor the percentage of sows with return to heat after service were influenced by litter size at weaning. On the overall, the effect of litter size during lactation on reproductive performance after weaning seems to be weak. However, it should be noted that sows with larger litter size at weaning have probably larger litter size at farrowing and hence higher breeding values and a better potential for reproduction. Suckling intensity during lactation can be manipulated by removal of the heaviest piglets a few days before full weaning (= split-weaning) or by separating the whole litter from the sow during a part of each day for the last days of lactation (= interrupted suckling). It generally results in a shorter weaning-to-estrus interval (review: Matte et al., 1992). The reduction is more marked with the interrupted suckling but this latter method is more laborious and time-consuming. Moreover, estrus may occur during lactation that will complicate management of the sows. Therefore, in recent years, only the effect of split-weaning on reproductive performance has been evaluated. Data from Vesseur et al. (1997) did not show any clear effect of split-weaning (4-5 piglets out of 10-12 during the 4th week p.p.) on the WEI, nor on the farrowing rate and subsequent litter size in parity-1 sows. However, they observed a shorter WEI (4.6 vs. 5.4 days for sows returning to estrus within 15 days) and a higher farrowing rate (97.2 vs. 86.3%) in parity-2 sows submitted to split-weaning compared to control sows. 15.4.3.2 Length of lactation Increasing the length of lactation from about 10 to 30 days results in a decrease in the weaning-to-estrus interval and a raise in subsequent litter size and farrowing rate in both primiparous and multiparous sows. The effect on litter size is more marked in multiparous sows (Figures 15.2A and 2B). As a consequence, the weaningto-conception interval is reduced but this reduction is not sufficient to compensate for the increase in the lactation length and the farrowing-to-conception interval increases (Figure 15.3). The positive effect of the duration of lactation on fecundity and prolificacy can be explained by several phenomena. Firstly, it may be assumed

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Litter size (total born)

Weaning-to-estrus interval (days)

Productivity and longevity of weaned sows

Primiparous Multiparous

A

12

Primiparous Multiparous

10 8 6 4 10

15

20

25

30

15

20

25

30

B

13 12 11 10 10

Duration of lactation (days)

Figure 15.2. Influence of the length of lactation on the weaning-to-estrus interval (A) and on the farrowing-to-conception interval (B) in primiparous and in multiparous sows (redrawn from Le Cozler et al., 1997: ; Koketsu and Dial, 1998: ).

Farrowing-to-conception interval (days)

45

Primiparous

Multiparous

40 35 30 25 10

15

20

25

30

Duration of lactation (days)

Figure 15.3. Influence of the length of lactation on the subsequent farrowing-toconception interval after weaning (adapted from Le Cozler et al., 1997).

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that the recovery of the uterus from the previous gestation is more advanced at the new conception which will allow a better fertilization rate and embryo survival (see 15.3.1.1). Secondly, it seems that the percentage of sows that does not ovulate at first estrus is abnormally high in case of short lactations (Table 15.5). Thirdly, the reduction in the WEI associated with the increase in the length of lactation itself has positive effects on litter size (see 15.4.5). Surprisingly, in sows with very short lactation (7 to 10 days), litter size is higher than in sows with short lactation (11 to 16 days) as shown by Marois et al. (2000). This can be explained by a longer farrowing-to-conception interval and hence a better uterine recovery at mating.

Table 15.5. Effect of the length of lactation on the percentage of sows ovulating within 8 days after weaning and on the percentage of these sows that ovulate (based on Knox et al., 2001). Length of lactation (days)

Sows in estrus (%) Sows ovulating (%) ab

< 17

17-24

25-31

> 31

35a 78a

94b 92b

98b 98b

96b 96b

P < 0.05

15.4.4

Influence of the physical and social environment

15.4.4.1 Climatic environment Even though the domestic pig is not a true seasonal breeder, it manifests variations in reproductive performance throughout the year. Prolonged intervals between weaning and subsequent estrus, ovulation and fertilization have been reported during summer and early fall, the influence of season being more pronounced in primiparous compared to multiparous sows (review: Prunier et al., 1996). The highest remating rate and lowest farrowing rate are also observed for sows served in summer whereas season has no clear effect on litter size (Koketsu et al., 1997a, b; Hughes, 1998; Tummaruk et al., 2000). Lower feed intake during lactation in summer is not sufficient to explain the delayed return to estrus after weaning: in their retrospective analysis of farm data, Koketsu et al. (1997b) observed that the weaning-to-mating interval was still prolonged during summer after adjusting data for feed intake.

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Long photoperiod and high ambient temperatures are the main environmental cues, which may influence the reproductive activity. Results concerning the influence of photoperiod variation using abrupt variations of light duration around farrowing or weaning are controversial. In contrast, when progressive patterns of variation are applied during gestation and lactation, it is clear that increasing light duration has a detrimental influence on the return to estrus after weaning compared to decreasing light duration (review: Prunier et al., 1996). Numerous experiments have shown that high ambient temperatures increase the WEI and its variability especially in first-parity sows (review: Prunier et al., 1996). Reduction in appetite and subsequent increase in the nutritional deficit during lactation explains only partly this negative effect of high ambient temperatures on the reproductive function (Prunier et al., 1997; Messias de Bragança et al., 1998). Nutritionally-independent variations in the secretion of hormones implied in the control of thermoregulation (for example thyroid hormones and cortisol) and able to act on the hypothalamopituitary-ovarian axis are probably involved. 15.4.4.2 Housing environment Data related to the influence of the housing system during lactation or around weaning on the subsequent reproductive performance of sows are scarce and relatively old. Grouping sows during lactation induces fertile estrus during lactation which is not desirable (Bryant et al., 1983). Penning sows in groups at weaning has no or a positive effect on the weaning-to-estrus interval and on litter size (Hemsworth et al., 1982; Lynch et al., 1984; Schmidt et al., 1985). It has no effect (Hemsworth et al., 1982; Schmidt et al., 1985) or a negative effect (Lynch et al., 1984) on the farrowing rate. However, more data are necessary to conclude definitively whether grouping sows at weaning will improve or deteriorate reproductive performance. 15.4.4.3 Boar effect The boar is well known to have stimulatory effects on the reproductive function of female pigs. Indeed, boar exposure of sows daily during the last 7/8 days of lactation reduces the weaning-to-estrus interval (Walton, 1986; Newton et al., 1987), but the effect seems to be more marked in multiparous than in primiparous sows (Walton, 1986). Similarly it has been observed that in sows with daily boar contact after weaning, estrus and ovulation occur earlier (Hemsworth et al., 1982; Walton, 1986; Pearce and Pearce, 1992) and in a higher proportion of sows (Langendijk et al., 2000). However, some discrepancy exists. Hughes (1998), for example, did not observe any effect of boar contact(s) but in his study the return to estrus after weaning occurred very early even in sows without any boar contact (5.5 days). When farrowing rate and litter size were measured, these parameters were not influenced by boar exposure (Hemsworth et al., 1982; Hughes, 1998).

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15.4.5

Relationships between WEI, litter size and farrowing rate

Several analyses of field data have related the WEI to subsequent litter size and farrowing rate (Leman, 1990; Vesseur et al., 1994a; Le Cozler et al., 1997; Steverink et al., 1999; Tummaruk et al., 2000; Figure 15.4). The analyses show that an increase in WEI from 3 to about 8 days is associated with a decline in subsequent litter size and farrowing rate. From about day 10 onwards, an increase in WEI is associated with an increase in these reproductive parameters. This observation agrees well with data from Clowes et al. (1994) and Vesseur (1997) who found that insemination of sows during the second estrus after weaning compared to the first one resulted in an increased pregnancy rate (+ 15 %) and subsequent litter size (+ 1.3 to 2.5 piglets). Therefore, it seems that some sows have a high genetic potential for reproduction which includes rapid return-to-estrus after weaning, fertility and prolificacy, whereas some other sows with delayed return-to-estrus after weaning take advantage of this delay to recover from the negative effects of factors acting during lactation, especially the nutritional deficit. An important question is to determine whether the WEI related variations in fertility and prolificacy are due to effects on ovulation rate, fertilization rate and/or embryo survival rate? Ovulation rate Little is known about variation in ovulation rate in association with variation in WEI. Data from three experiments with more than 350 multiparous sows (Soede et al., 1995a, b; Steverink et al., 1997) show an average ovulation rate of 21.6, 21.4, 20.5 and 19.5 at days 3 to 6 after weaning, respectively (significant linear decrease). Recently, Patterson et al. (2001) also found a negative correlation between WEI (varying between 3.0 and 5.3 days) and ovulation rate (varying between 13 and 31) in multiparous sows (r = -0.54). In contrast, in primiparous sows, Van den Brand and Langendijk (unpublished results) did not find a relation between

Total born

100 90 80 70

13 12,5 12 11,5 11 10,5 10 9,5 9

60 50 40 30 0

5

10

15

20

Total born

Farrowing rate

Farrowing rate

25

Weanin g to service interval in days (1-30)

Figure 15.4. Association of Weaning-to-estrus interval (WEI) with subsequent farrowing rate and litter size (based on Leman, 1990).

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the weaning-to-ovulation interval (varying between 4.6 and 8.9 days) and ovulation rate (varying between 12 and 30), but they did find a relation with embryo survival (Table 15.6). Although ovulation rate is normally quite high and not the first limiting factor for litter size and farrowing rate, a role of the decrease in ovulation rate can not be ruled out, especially if the decline in number of ovulations is associated with a reduced quality of the corpora lutea, as has been suggested (Zak et al., 1997b; Almeida et al., 2000). In these sows with a short WEI, ovulation rate is probably closely related to the number of selectable follicles present at weaning.

Table 15.6. Reproductive characteristics of primiparous sows with variable weaningto-ovulation intervals (ovulation was assessed at 8-hour intervals) (Van den Brand and Langendijk, unpublished results). Weaning-to-ovulation interval (hours)

Pregnancy rate at day 35 (%) Ovulation rate Normal of embryos at day 35 Embryo survival at day 35 (%) 1 Luteal weight (g) Number of sows

110 - 145

150 - 158

166 - 214

91 19.7 ± 4.0 13.1 ± 3.1 67 ± 12 7.0 ± 1.2 23

96 19.0 ± 4.5 11.7 ± 3.7 62 ± 18 6.1 ± 1.1 26

86 19.9 ± 3.5 11.4 ± 3.2 57 ± 14 6.5 ± 1.1 29

1

Correlation between weaning-to-ovulation interval and embryo survival rate: r = -0.26, P < 0.05

For sows with a WEI of more than 10 days, it is not clear if the increase in reproductive performance is associated with an increased ovulation rate. However, an extended WEI which resulted from a three day treatment with altrenogest from weaning onwards, also resulted in an increase in ovulation rate (Koutsotheodoros et al., 1998). Fertilization rate In sows, fertilization results are very much dependent on the interval between insemination and ovulation (Waberski et al., 1994; Soede et al., 1995a), subsequently affecting litter size and farrowing rate (Nissen et al., 1997; Terqui et al., 2000). Kemp and Soede (1996) showed that, if sows with a WEI varying between 3 and 7 days were inseminated at an optimal time relative to ovulation (in the period of 24 hours before ovulation), fertilization results were not affected by WEI. In many experimental data, an increase in WEI (between 3 and 6 days) has found to be associated with a decrease in the duration of estrus and, consequently, a shorter

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interval between onset of estrus and ovulation (review: Soede and Kemp, 1997). A similar relation between WEI and estrus duration was found on farms (Steverink et al., 1999). If the insemination strategy on farms is not adjusted to WEI, the number of sows in which the first insemination takes place after ovulation will be increased in sows with a longer WEI and hence the risk of a low fertilization rate (review: Kemp and Soede, 1997). It is not clear to what extent these phenomena are responsible for the reduction in farrowing rate and litter size as found for sows with a WEI from 3 up to 8-10 days. For sows with a WEI of more than 10 days, the duration of estrus remains as short as found for sows with a WEI of 6 days and beyond (Steverink et al., 1999). It therefore does not seem likely that the increase in reproductive performance found for these sows is associated with a better timing of insemination and therefore with higher fertilization rates. Embryonic mortality No clear information is available for the relationship between the weaning-to-estrus interval and the subsequent embryo survival. However, Van den Brand and Langendijk (unpublished results) found that, in primiparous sows, an increase in the weaning-to-ovulation interval was indeed associated with a decrease in subsequent embryo survival (Table 15.6). In these sows, ovulation rate was not associated with the weaning-to-ovulation interval. There is some circumstantial evidence suggesting that WEI is associated with subsequent embryo survival, based on experiments in which feed restriction during lactation results not only in an increase in WEI, but also in a decrease in embryo survival (Table 15.3). However, as discussed earlier (see 15.4.2.1.), this association does not seem to be very strong and it is not clear which factors are of influence. In summary, associations between WEI and subsequent reproductive performance (both farrowing rate and litter size) seem to be a combined result of effects on ovulation rate, fertilization rate and embryo survival. The relative importance of these effects is not known.

15.5

Conclusion

During lactation, suckling-neuroendocrine reflexes are the main factors inhibiting LH secretion and ovarian activity. Negative metabolic state due to high milk production creates a hormonal milieu, which may have additional inhibitory effects. In commercial farms, the timing of weaning is the decision of the producer. It generally occurs when milk production is still very high and is not progressive as in “natural” conditions. As a consequence, weaned sows are submitted to rapid changes in the nutritional balance and the hormonal secretions that generally induce estrus behavior and ovulation some days later. Internal (i.e. genetic factors, parity, body reserves) and environmental factors (i.e. light, ambient temperature, housing)

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may influence the nature and the amplitude of these changes as well as the ability of the ovaries to respond to these changes. Therefore, both factors acting during lactation and after weaning may influence reproductive performance of weaned sows. Evidence from this review suggest that reproductive problems of sows, especially primiparous sows, are related for a large part to lactational events and less to post-weaning events. In order to improve reproductive performance and longevity, lactational sources of inhibition should be decreased, especially in first and-second litter sows. This can be done by reducing suckling stimulation and/or nutritional deficit (e.g. split-weaning, interruped suckling). Moreover, short lactations (< 21 days) should be avoided in order to allow the gonadotropic axis and the uterus to recover from the previous gestation and farrowing.

References Adashi, E.Y., C.E. Resnick, A. Hurwitz, E. Ricciarellie, E.R. Hernandez, C.T. Roberts, D. LeRoith and R. Rosenfeld, 1992. The intra-ovarian IGF system. Growth Regulation 2, 10-15. Almeida, F.R.C.L., Kirkwood, R.N., Aherne, F.X. and G.R. Foxcroft, 2000. Consequences of different patterns of feed intake during the estrous cycle in gilts on subsequent fertility. Journal of Animal Science 78, 1556-1563. Angell, C. A., R. C. Tubbs, A. B. Moore, C. R. Barb and N. M. Cox, 1996. Depressed luteinizing hormone response to estradiol in vivo and gonadotropin-releasing hormone in vitro in experimentally diabetic swine. Domestic Animal Endocrinology 13, 453-463. Armstrong, J.D., J.H. Britt and N.M. Cox, 1986a. Effect of energy during lactation on body condition, energy metabolism, endocrine changes and reproductive performance in primiparous sows. Journal of Animal Science 63, 1915-1925. Armstrong, J.D., J.H. Britt and N.M. Cox, 1986b. Seasonal differences in function of the hypothalamic-hypophysial-ovarian axis in weaned primiparous sows. Journal of Reproduction and Fertility 78, 11-20. Baidoo, S.K., F.X. Aherne, R.N. Kirkwood and G.R Foxcroft, 1992. Effect of feed intake during lactation and after weaning on sow reproductive performance. Canadian Journal of Animal Science 72, 911-917. Baldwin, D.M. and G.H. Stabenfeld, 1975. Endocrine changes in the pig during late pregnancy, parturition and lactation. Biology of Reproduction 12, 508-515. Barb, C.R., 1999. The brain-pituitary-adipocyte axis: role of leptin in modulating neuroendocrine function. Journal of Animal Science 77, 1249-1257. Bevers, M.M., A.H. Willemse, Th.A.M. Kruip and D.F.M. Van De Wiel, 1981. Prolactin levels and the LH-response to synthetic LH-RH in the lactating sow. Animal Reproduction Science 4, 155163. Bhatia, S.S., 1989. Studies on lifetime productivity in Large White sows. Indian Journal of Animal Production and Management 5, 30-32. Booth, P.J., 1990. Metabolic influences on hypothalamic-pituitary-ovarian function in the pig. Journal of Reproduction and Fertility Suppl. 40, 89-100.

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Varley, M.A. and G.R. Foxcroft, 1990. Endocrinology of the lactating sows. Journal of Reproduction and Fertility, Suppl. 40, 47-61. Vesseur, P.C., B. Kemp and L.A. Den Hartog, 1994a. The effect of weaning to estrus interval on litter size, live born piglets and farrowing rate in sows. Journal of Animal Physiology and Animal Nutrition 71, 30-38. Vesseur, P.C., B. Kemp and L.A. Den Hartog, 1994b. Factors affecting the weaning to estrus interval in the sow. Journal of Animal Physiology and Animal Nutrition 72, 225-233. Vesseur, P.C., B. Kemp, L.A., Den Hartog and J.P.T.M. Noordhuizen, 1997. Effect of split-weaning in first and second parity sows on sow and piglet performance. Livestock Production Science 49, 277-285. Waberski, D., K.F. Weitze, C. Lietmann, W. Lubbert zur Lage, F.P. Bortolozzo, T. Willmen and R. Petzoldt, 1994. The initial fertilizing capacity of longterm stored liquid semen following preand postovulatory insemination. Theriogenology 41, 1367-1377. Walton, J. S., 1986. Effect of boar presence before and after weaning on estrus and ovulation in sows. Journal of Animal Science 62, 9-15. Weldon, W.C., A.J. Lewis, G.F. Louis, J.L. Kovar and P.S. Miller, 1994. Postpartum hypophagia in primiparous sows: II. Effects of feeding level during gestation and exogenous insulin on lactation feed intake, glucose tolerance, and epinephrine-stimulated release of nonesterified fatty acids and glucose. Journal of Animal Science 72, 395-403. Wilson, M.E., H. Stein, N.L. Trottier, D.D. Hall, R.L. Moser, D.E. Orr and R.A. Easter, 1996. Effects of lysine intake on reproductive performance in first parity sows. Journal of Animal Science 74 (Suppl. 1), 63 (Abstract). Xue, J., Y. Koketsu, G.D. Dial, J. Pettigrew and A. Sower, 1997. Glucose tolerance, luteinizing hormone release, and reproductive performance of first-litter sows fed two levels of energy during gestation. Journal of Animal Science 75, 1845-1852. Yang, H., P.R., Eastham P. Phillips and C.T. Whittemore, 1989. Reproductive performance, body weight and body condition of breeding sows with differing body fatness at parturition, differing nutrition during lactation and differing litter size. Animal Production 48, 181-201. Yang, H., J.E. Pettigrew, L.J. Johnston, G.C. Shurson, J.E. Wheaton, M.E. White, Y. Koketsu, A.F. Sower and J.A. Rathmacher, 2000a. Impact of dietary lysine intake during lactation on blood metabolites, hormones, and reproductive performance in primiparous sows. Journal of Animal Science 78, 1001-1009. Yang, H., J.E. Pettigrew, L.J. Johnston, , G.C. Shurson and R.D. Walker, 2000b. Lactational and subsequent reproductive responses of lactating sows to dietary lysine (protein) concentration. Journal of Animal Science 78, 348-357. Yang, H., G.R. Foxcroft, J.E. Pettigrew, L.J. Johnston, G.C. Shurson, A.N. Costa and L.J. Zak, 2000c. Impact of dietary lysine intake during lactation on follicular development and oocyte maturation after weaning in primiparous sows. Journal of Animal Science 78, 993-1000. Zak, L.J., J.R. Cosgrove, F.X. Aherne, G.R. Foxcroft, 1997a. Pattern of feed intake and associated metabolic and endocrine changes differentially affect postweaning fertility in primiparous lactating sows. Journal of Animal Science 75, 208-216.

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Productivity and longevity of weaned sows

Zak, L.J., X. Xu,. R.T. Hardinand and G.R. Foxcroft, 1997b. Impact of different patterns of feed intake during lactation in the primiparous sow on follicular development and oocyte maturation. Journal of Reproduction and Fertility 110, 99-106. Zak, L.J., I.H. Williams, G.R. Foxcroft, J.R. Pluske, A.C. Cegielski, E.J. Clowes and F.X. Aherne, 1998. Feeding lactating primiparous sows to establish three divergent metabolic states: I. Associated endocrine changes and postweaning reproductive performance. Journal of Animal Science 76, 1145-1153. Zivkovic, M., M. Teodorovic and S. Kovcin, 1986. Longevity of sows according to the management in large units. World Review of Animal Production 22, 11-15.

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Conclusions The chapters in this book have presented the most up-to-date information, data and background philosophy related to the various events associated with ‘weaning’. Weaning is a stressful period for both the young pig and the sow, and the act of ‘weaning’ is an unusual event in the pig production cycle because of the many changes that are simultaneously imposed on the system, eg, change of nutrition, change of environment, change of social structure, and so on. Consequently, the risks to the producer of decreased production, increased mortality and morbidity, and deteriorated health status are high at weaning, and careful management is required to ameliorate the weaning process so that any losses associated with weaning are minimized. The large array of influences can cause enormous variation in the response of piglets to the transition from the sow to the next phase. This can cause big differences in development between animals, both within and between litters. The chapters give insight how this occurs, and offer ways to avoid the negative effects of weaning A recent comment in the magazine ‘Pig International’ stated that pork remains the most consumed meat in Europe, with an average of 43.7 kg per head eaten in 2002. This compares to 23 kg for poultry and 19.4 kg for beef/veal. To maintain, and increase, this level of consumption requires due diligence to all aspects of the pig production and the supply chain, as well as improving practices and adopting new technologies to achieve higher levels of production and consumption. Weaning is an integral component of the overall pig production cycle, predominately because of the impact weaning weight and post-weaning performance can have on finisher pig performance and profitability. Fertility of the weaned sow is also an important determinant of profitability in the system. However, new challenges are continually being faced by the pig Industry, such as the increasing awareness of society with respect to animal welfare, food safety, the environment, and the ‘quality’ of production, especially with respect to antibiotics and some minerals as growth promoters. Many of these challenges concern weaning and, on balance, the process of ‘weaning’ and its effects has never been considered more important. To this end, we believe that the material contained within “Weaning the Pig: Concepts and Consequences”, is both timely and pertinent to many of the issues being faced around the world today regarding weaning. We trust that you have enjoyed the chapters in this book and believe that the diversity of topics covered, including the fate of the weaned sow, will assist with your business or line of expertise in the pig Industry. John Pluske Jean Le Dividich Martin Verstegen

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421

List of authors A.C. Beynen, Department of Nutrition, Faculty of Veterinary Medicine, Utrecht University, P.O. Box 80152, 3508 TD Utrecht, The Netherlands P.H. Brooks, University of Plymouth, Faculty of Land, Food and Leisure, Seale-Hayne Campus, Newton Abbot, Devon, TQ12 6NQ, United Kingdom D. Burrin, USDA/ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, 1100 Bates Street, Houston, Texas 77030, USA S.S. Dritz, Department of Animal Sciences and Industry, Kansas State University, Manhattan KS 66506-0201, USA F.R. Dunshea, Natural Resources and Environment, Sneydes Road, Werribee Victoria 3030, Australia R.D. Goodband, Department of Animal Sciences and Industry, Kansas State University, Manhattan KS 66506-0201, USA D.J. Hampson, School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, Western Australia 6150, Australia. M. Hay, Ecole Nationale Vétérinaire de Toulouse, 23 Chemin des Capelles, 31076 Toulouse, France D.E. Hopwood, Animal Resources Centre, Murdoch Drive, Murdoch, WA 6150, Australia D. Kelly, Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen, AB2 9SB, Scotland B. Kemp, Animal Husbandry Group, Wageningen University, P.O. Box 338, 6700 AH Wageningen, The Netherlands M.R. King, Institute of Food, Nutrition and Human Health, Massey University, Private Bag 11-222, Palmerston North, New Zealand R.H. King, Agriculture Victoria, Sneydes Road, Werribee Victoria 3030, Australia J. Le Dividich, INRA-UMRVP, 35590 St-Gilles, France F. Madec, Agence Française de Sécurité Sanitaire des Aliments, BP 53, Zoopôle Les Croix, 22440 Ploufragan, France G.P. Martineau, Ecole Nationale Vétérinaire de Toulouse, 31076 Toulouse, France

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H.M. Miller, The , Centre for Animal Sciences, LIBA, School of Biology, Leeds LS2 9JT, United Kingdom P.C.H. Morel, Institute of Food, Nutrition and Human Health, Massey University, Private Bag 11-222, Palmerston North, New Zealand P. Mormède, Neurogénétique et Stress, INSERM U471, INRA, Université Victor Segalen Bordeaux 2, Institut François Magendie, 33077 Bordeaux, France J.L. Nelssen, Department of Animal Sciences and Industry, Kansas State University, Manhattan KS 66506-0201, USA P. Orgeur, INRA- PRMD, 37380 Tours, France J.R. Pluske, School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch WA 6150, Australia A. Prunier, INRA, Unite Mixte de Recherches sur le Veau et le Porc, Saint-Gilles, France H. Quesnel, INRA, Unite Mixte de Recherches sur le Veau et le Porc, Saint-Gilles, France R.D. Slade, The , Centre for Animal Sciences, LIBA, School of Biology, Leeds LS2 9JT, United Kingdom N.M. Soede, Animal Husbandry Group, Wageningen University, P.O. Box 338, 6700 AH Wageningen, The Netherlands B. Stoll, USDA/ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, 1100 Bates Street, Houston, Texas 77030, USA M.D. Tokach, Department of Animal Sciences and Industry, Kansas State University, Manhattan KS 66506-0201, USA C.A.Tsourgiannis, University of Plymouth, Faculty of Land, Food and Leisure, SealeHayne Campus, Newton Abbot, Devon, TQ12 6NQ, United Kingdom M.A.M. Vente-Spreeuwenberg, Nutreco Swine Research Centre, P.O. Box 240, 5830 AE Boxmeer, The Netherlands M.W.A. Verstegen, Animal Nutrition Group, Wageningen University, P.O. Box 338, 6700 AH Wageningen, The Netherlands I.H. Williams, School of Animal Biology, Faculty of Natural and Agricultural Sciences, University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia

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423

Index A

B

α-linolenic acid 175 accumulate body fat 31 active immunity 220, 224 active or passive coping strategy 89 acute IGF-I treatment 71 acute phase protein production 150 ad libitum 25 adaptations to underfeeding 70 adaptive immunity 221 adrenal reactivity to ACTH 54 affinity constants 128 aggressive behaviours 57 AIAO see all-in / all out (AIAO) air velocity 343 all-in / all out (AIAO) 349, 353, 373-374, 377 ambient temperature 338-340, 353 amino acid transport 128 amino acid utilization 314 ammonia 167 amylase 124 amylolytic activity 40 anestrus 385-388, 397 anorexia 204, 237 anterior teats 84 antigen-presenting cell (APC) 222, 225-231, 236 antigenic compounds 43 antimicrobials 322-323 APC see antigen-presenting cell (APC) apical 127 arginine 319, 320-321 aromatic compounds 45 arterial nutrient utilization 308 aspartate 167, 311-312 ATP levels in jejunal mucosa 159

bacterial translocation 180, 184 bedding 341-342 belly-nosing 57 biochemistry of the gut 82 birth-weight 20, 25, 91, 363-364, 366-367, 371 blood plasma 56 boar 405 body – lipid 66 – protein 68 – stores 399-401 – thermal insulation 338-339 butyric acid 181, 314

Concepts and consequences

C calcium 269, 274 carbohydrase induction 127 carboxymethylcellulose (CMC) 207 carnitine 269, 274 catecholamine excretion 54 CD4+ T cells 150 CD8+ T cells 134 cell proliferation 303, 305-306, 320 cellular immunity 230 cereals, cooked 43 cereals, flaked 43 CF see continuous flow (CF) changing light patterns 63 chymotrypsin 124 circulating cortisol 54 circulating free fatty acid levels 54 citrulline 312 climatic environment 404 CMC see carboxymethylcellulose (CMC) cold stress 73 colonocytes 181 colostrum 362, 368-369, 371 commercial

425

Index

– pellets 64 – weaning 138 – weaning age 123 compensatory growth 25 complex carbohydrates 40 concanavalin A 172 confinement-reared piglet 94 conserve gut 68 conserve protein 67 continuity of food intake 99 continuous flow (CF) 373-374 copper 269-271, 274, 288 corn starch 184 cortisol insensitivity 131 cortisol release 132 creep feed 21 creep feed consumption 42, 61, 88 creep feeding 91 cross nursing 369 crypt depth 19, 124, 125 crypt enterocytes 310 culling 385, 387 cysteine 265, 275, 316-317 cytokines 220-221, 224, 226-228, 230, 234, 237, 241, 244, 304, 322 cytosolic dipeptidase 183

D daily fluid intake 102 diarrhoea 146, 199, 201, 203, 205-208, 210, 337, 349, 351, 353, 372 diet – complexity 262-263 – formulation 259, 270, 287 – low-quality 56 dietary antigen 241 dietary interventions 41 different chain-length fatty acids 130 digestive – enzymes 43 – physiology 117, 301 – problems 54 dipeptides 168

426

dominant pigs 95 draughts 345, 350 dried porcine solubles 278 dried skim milk 277 dry pelleted feed 56

E early weaning 28, 372 easily digestible diet 56 ecophysiology 102 effects of gender 43 EGF see epidermal growth factor (EGF) elastase I 124 elastase II 124 embryo survival 385, 393-397, 400, 404, 408 endocrine changes 61 endotoxicosis 168 energy 264, 289, 368-369, 391 – deficit 65 – sources 264, 272, 285 enteral nutrition 132 enteric disease 199, 201, 211, 339, 349, 351 enterocyte 127, 184, 310 – aldohexose transporters 127 – differentiation 151 – migration distance 125 enteropathogenic E. coli 203 enterotoxigenic 202 enterotoxigenic E. coli 202, 204 enterotoxins 203, 205, 207, 210, 224 enzyme activities 119 epidermal growth factor (EGF) 182 epithelial barrier 99, 237, 238 epithelial integrity 134 epithelial lining of the gut 99 Escherichia coli 199-204, 206, 210-211 essential amino acids 133 estradiol-17β 389, 393 estrus 385, 388, 393-396, 398, 404-405, 408 ETEC 202, 204-205, 208-210 exogenous catecholamine 73

Weaning the pig

Index

F family affiliations 85 farrowing rate 394, 398, 405-408 fasting heat 26 fat 273-274, 286-288, 399, 400 – reserves 65, 70 – supplementation 172 fatness 400-401 feed – flavour 45 – intake pattern 396 – preferences 45 feeder 289, 337, 346, 354 feeding – activity 88 – behaviour 47, 81 – patterns 101 – spaces 47, 90 – strategy 368, 370 – systems 42 fermentation 199, 200, 205, 207, 209 fermented liquid feed 56 fertility 394, 406 fertilization rate 394, 404, 407-408 fetal gluconeogenic capacity 73 fetal villus enterocyte 120 fibre 205-206, 210-211 fish meal 56, 276-277, 284, 286-288 flooring material 337, 346, 354 follicle 389-390, 392-397, 407 foraging behaviour 85 fostering 362, 368-369, 372 fresh liquid feed 56 FSH 390, 392-393 functional feed ingredients 145, 185

G galactose 127 GALT 225 gastric development 118 gastric motility 139 gastrointestinal – hormones 152

Concepts and consequences

– tract 40 – trauma 183 genotypes, modern 66 GLP-1 135, 137 GLP-2 135, 137, 305-306, 310 glucagon-like peptide 2 (GLP-2) 135, 137, 305-306, 310 glucoamylase 127, 151 glucocorticoid receptor levels 54 glucocorticoid receptors 132 gluconeogenesis 66, 72 glucose 127, 312, 313 glutamate 167, 308-309, 311-313, 319-320 glutamine 167, 308-309, 31-313, 319-321 glutamine administration 168 glutathione 167 glycerol, mobilised 67 glycogen breakdown 66 goblet cells 133, 149 Gompertz function 18 grain sources 275, 285 group size 337, 348, 354 growth – factors 130 – potential 17, 365, 371, 376 – rates of organs 123 – to slaughter 20 gruel 22 gut – development 39 – ecosystem 82 – metabolism 307 – physiology 117, 301

H haemolytic E. coli 202, 207, 210-211 haemolytic ETEC 203-204, 206-210 health 353, 361, 373 hepatic ST receptor mRNA 70 high ambient temperature 344, 405 highly palatable 56 homeorhesis 67 homeostatsis 103

427

Index

housing system 337, 405 HPA see hypothalamic-pituitary-adrenal (HPA) axis humoral immunity 221-222 hydrolase activities 122 hygiene 351, 353-354 hypersensitivity 133, 230, 241-244, 279-280, 286 hypothalamic-pituitary axis 72 hypothalamic-pituitary-adrenal (HPA) axis 54 hypothalamic-pituitary-ovarian axis 392, 405

I IgA 223-224, 226 – cells 232 IGF-I 69, 391, 392 IgG 223-224, 242 IgM 223-224 – cells 232 immediate post-weaning period 63 immune system 44, 102, 219-224, 226, 228, 230, 233, 242, 244 immunoglobulin 29, 39, 219, 222-224, 226, 233, 368-369 immunological low point 82 inappropriate gut microflora 100 increased rate of cell loss 148 incretin hormones 135 individual variation 57 infection 322 inflammation 243-244 ingestion of amniotic fluid 119 ingredient selection 263 initial feed intake 56 innate immunity 220 insulin 69, 72, 391-392, 397, 400 insulin-like growth factors 182 interleukin-1 (Il-1) 150 interleukin-6 Il-6 150 interval between nursing events 84 intestinal

428

– absorptive capacity 128 – barrier function 147 – enlargement 122 – immune system 224, 230-231, 233, 236-237, 243 – immunity 219, 231, 233, 237, 243-244 – inflammation 220, 228 – microflora 199 – morphology 124, 234 – nutrient requirements 301 – nutrient utilization 301, 306 – permeability 149 intestine – large 200, 202, 205, 207, 211 – small 199-210 intestinotrophic events 138 intraluminal nutrients 137 intravenous infusion 68 intravenously supplied TPN 180 inverse relationship 91 isoleucine 265

K ketones 313

L L-arginine 183 lack of – enteral stimulation 152 – familiarity 96 – nutrients 155 lactation length 394, 396, 402 lactic acid 181 – bacteria 63 lactose 262-263, 272-273, 285-287 lamina propria 221, 225-228, 230-233, 236, 238-241 larger matriarchal group 85 LC-PUFA see long-chain, polyunsaturated fatty acid (LC-PUFA) LCFA see long-chain fatty acid (LCFA) LCT see lower critical temperature (LCT) lean tissue 69

Weaning the pig

Index

learning phase 85 LH 389-393, 400 lighting 344 lipase 124 lipase activity 172 liquid diets 41, 90 liquid feeding 107 litter cohesion 57 litter size 37, 362-364, 388-389, 394, 398399, 401-402, 405-407 long-chain fatty acid (LCFA) 321 long-chain, polyunsaturated fatty acid (LCPUFA) 321-322 long-term benefits 23 longevity 385, 394 lower critical temperature (LCT) 20, 339, 341-343 LR3IGF-I infusion in suckling piglets 71 luminal nutrient utilization 308 lymphocyte 147, 222, 226-230, 232-233, 236-237, 241 lysine 264-267, 278, 282, 318, 398

M M-cells 147 macrophage 220, 227, 231, 236-237 major histocompatibility complex (MHC) 222, 225-231, 236-238, 241 malnutrition 158 maltase 127, 151 – activities 40 maltose 121 management options 38 management strategies 108 maternal catabolism 392 meal or a pellet 90 mechanical stimulation 155 medicated early weaning (MEW) 374 metabolic status 391 methionine 265, 275, 278, 316-317 MEW see medicated early weaning (MEW) MHC see major histocompatibility complex (MHC)

Concepts and consequences

microbial environment 82 microenvironment 341 microflora 199-201, 203, 205-206, 209 microscopic morphology 176 milk energy intake 63 milk products 273, 283, 285 minerals 269 minimising the growth check 27 mixing of animals 53-54 mobilisation of body lipid 65 monosaccharides 127 morbidity 29 mortality 29 mucin 211, 224, 306, 317 mucosal function 145 mucosal integrity 167 mucus 202, 211 muscle fibres 365

N NDO see non-digestible oligosaccharides (NDO) NEFA concentrations 66 negative protein balance 68 neonatal enteral nutrition 129 neuroendocrine changes 53, 57 non-digestible oligosaccharides (NDO) 175, 180 non-optimal indoor climate 350 non-starch polysaccharide (NSP) 206-212 norepinephrine 73 novel environment 53 noxious gases 344 NSP see non-starch polysaccharide (NSP) nucleosides 185 nucleotides 184, 322 nutritional deficit 57 nutritional management 37 nutritional program 259, 262, 288 oedema 203

429

Index

O oils 43 oligosaccharides 282-283 ontogeny of somatotropin 69 operant panels 95 oral tolerance 228-229, 243 organic acids 283 ornithine 312, 320 ovalbumin 166 ovulation 385 ovulation rate 393-398, 400-401, 406-408 oxidative fuels 311-312

P pair-feeding 160 pancreatic enzyme activities 119 Paneth cells 225 paracellular permeability 159 paracellular transport 150 passive immunity 223, 374 PDV see portal-drained visceral (PDV) pen structure 337, 346, 354 pepsin 40 peptide absorption 129 peri-natal colon 120 permeability 166 Peyer’s patches 225-226, 233 phenylalanine 318-319 phosphorus 269 photoperiod 405 phytase 283 pituitary hormones 389 plant proteins 30 plasma – catecholamine 73 – cortisol 73 – glucose 66 – glycerol concentrations 67 – IGF-I 69 – insulin 72 – ST 69 poly-unsaturated fatty acids 172 polyamines 183, 320-321

430

portal-drained visceral (PDV) 307-309, 311, 313-315, 318, 322 post-hepatic amino acid supply 72 post-weaning 92 – colibacillosis (PWC) 199, 201-212 – diarrhoea 44 – growth check 37 – growth rate 92 – intestinal maturation 122 – lean tissue deposition 70 potato protein 281 pre-natal effects 39 pre-weaning creep food intake 39-40, 43 prebiotics 181 probiotics 181-282 production cycle 37 proglucagon derived peptides 135 proinflammatory immune system components 134 prolificacy 394, 402, 406 proline 312, 319, 320 protein intake 398, 401 protein sources 30, 262-263, 275-278, 281282, 284, 287-288 putriscine dihydrochloride 183 PWC see post-weaning colibacillosis (PWC)

R rapid intestinal growth 129 rate of lipogenesis 66 reduced functionality 126 reduced welfare 57 reduction in nocturnal temperature (RNT) 341-342 relative humidity 343 reproductive axis 385, 388-389 reproductive performance 385, 394, 396, 398, 400-401, 408 restricted feeding 44, 160 retrograded starch 176 ribosylphosphates 184 rice 206, 209-211 risk factors 351, 353-354

Weaning the pig

Index

RNT see reduction in nocturnal temperature (RNT)

S salmonellosis 202 satiety 103 SCFA see short-chain fatty acids (SCFA) secretory IgA 226, 227 secretory immunoglobulins 147 segregation 374, 377 serotype 203, 207 SEW 53, 275, 280, 283-288, 375 sexual dimorphism 43 short-chain fatty acids (SCFA) 180, 305-306, 310, 313-314 sigmoidal growth 18 similar intra-suckling intervals 84 skeletal muscle protein synthesis 72 skim milk 63, 277, 284 small intestinal histology 64 small intestinal integrity 149 social facilitation 97 social rank 89 soluble fibre 175 somatotrophic activity 70 somatotrophic axis 54 somatotropin 68 sow – genotypes 88 – milk 21, 86 – milk yield 56 – vocalisations 86 soybean meal 262, 279-281, 284, 286-287 soybean, hydrolysed 166 spermine concentration 184 split weaning 22, 368, 370 spray-dried – animal plasma 263, 269, 275, 284, 286 – blood meal 276, 278, 284, 286-288 – bovine colostrum 28, 30 – egg protein 281, 284 – wheat gluten 282

Concepts and consequences

– whole egg 276 ST receptor gene 69 starch 399 starter diets 27 stimulation of food intake 28 stocking densities 347, 354 stocking rate 337 stomach mass 123 stress hormones 53 suckling 389, 402 sucrose 121 supernumerary 361, 362-363, 371, 376-377 supervision of farrowing 368 supplemental water 47 supplementary feeding 23 supplementary milk 22 supplemented piglets 24 survival 367, 376 sweetener 45, 106 synchronous feeding 97-98

T T cells 222 taxation of the adaptive mechanisms 57 temperature fluctuation 342, 344-345, 350 thermal requirement 337-339 thermoregulation 39 threonine 265, 316-318, 320-321, 323 tight junctions 182, 224, 239 tissue thermal insulation 353 TNF see tumor necrosis factor (TNF) total heat production 65 trace minerals 269, 271 transient starvation 100 transportation 53 true digestibilities 19 trypsin 124 tryptophan 265 tumor necrosis factor (TNF) 150 tyrosine 319

431

Index

U underfed piglet 47 underfeeding 185 undernutrition 67 underprivileged 361-362, 365-367, 371, 376 urinary excretion 53 urinary norepinephrine 73

whole-body fractional protein 67 withholding soybean meal 44

Z zinc 269, 271 – oxide 270-271, 285-288

V valine 265 ventilation 343-344, 351 VFA see volatile fatty acids (VFA) villous architecture 19, 100, 120, 126, 147 villus enterocytes 310 villus surface 138 viscosity 208-209 vitamins 268-269 volatile fatty acids (VFA) 205 volumetric fill 104

W ω-3 polyunsaturated 175 ω-6 polyunsaturated 175 water – availability 47 – intake 47, 87 – temperature 105 – holding capacity 208, 210 waterer 337, 346, 354 weaning – age 28, 37, 259-261 – anorexia 54 – of piglets 149 – weight 260, 364, 366 – weight advantage 38 – elicited gut hormone secretion 135 – induced impairment 145 – to-estrus interval (WEI) 385, 393-395, 397-398, 400-402, 405-408 WEI see weaning-to-estrus interval (WEI) weight of the small intestine 64 whey 272, 276-278, 284, 286-288 – protein 166

432

Weaning the pig