Sports Med 2009; 39 (11): 889-901 0112-1642/09/0011-0889/$49.95/0
LEADING ARTICLE
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Design of the iPlay Study Systematic Development of a Physical Activity Injury Prevention Programme for Primary School Children Dorine C.M. Collard,1 Mai J.M. Chinapaw,1,2 Willem van Mechelen1,2 and Evert A.L.M. Verhagen1 1 EMGO Institute for Health and Care Research and Department of Public and Occupational Health, VU University Medical Center, Amsterdam, the Netherlands 2 Research Centre Body@Work TNO VUmc, Amsterdam, the Netherlands
Abstract
Health benefits of physical activity in children are well known. However, a drawback is the risk of physical activity-related injuries. Children are at particular risk for these injuries, because of a high level of exposure. Because of the high prevalence of physical activity injuries and the negative short- and long-term consequences, prevention of these injuries in children is important. This article describes how we systematically developed a school-based physical activity injury prevention programme using the intervention mapping (IM) protocol. IM describes a process for developing theory- and evidence-based health promotion programmes. The development can be described in six steps: (i) perform a needs assessment; (ii) identify programme and performance objectives; (iii) select methods and strategies; (iv) develop programme; (v) adopt and implement; and (vi) evaluate. First, the results of the needs assessment showed the injury problem in children and the different risk factors for physical activity injuries. Based on the results of the needs assessment the main focus of the injury prevention programme was described. Second, the overall programme objective of the injury prevention programme was defined as reducing the incidence of lower extremity physical activity injuries. Third, theoretical methods and practical strategies were selected to accomplish a decrease in injury incidence. The theoretical methods used were active learning, providing cues and scenariobased risk information, and active processing of information. The practical strategy of the injury prevention programme was an 8-month course about injury prevention to be used in physical education classes in primary schools. Fourth, programme materials that were used in the injury prevention programme were developed, including newsletters for children and parents, posters, exercises to improve motor fitness, and an information website. Fifth, an implementation plan was designed in order to ensure that the prevention programme would be implemented, adopted and sustained over time. Finally, an evaluation plan was designed. The injury prevention programme is being evaluated in a cluster randomized controlled trial with more than 2200 children from 40 primary schools throughout the Netherlands.
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The IM process is a useful process for developing an injury prevention programme. Based on the steps of the IM we developed an 8-month injury prevention programme to be used in physical education classes of primary schools.
Regular physical activity (PA) has many health benefits, for example it lowers the risk of obesity, coronary heart disease and osteoporosis.[1-3] A drawback of increased PA levels is the risk of PA-related injuries. Sports are the leading cause of injury and hospital emergency room visits in adolescents.[4-5] The high prevalence of PA injuries in children and the negative short- and long-term consequences confirm its importance as a health problem. Although most PA injuries are not life threatening, the occurrence of PA injury can result in pain, disability, school absence, absence from PAs and sometimes in dysfunction in the short and long term. Therefore, prevention of PA-related injuries is essential. Emery[6] showed in a review that injury prevention strategies in children can reduce the risk of PA injuries. However, the literature has some limitations and is based primarily on observational studies for specific injuries and specific sports.[7] Few studies on school-based PA injury prevention strategies have been published. Of these, only one study was a randomized controlled trial.[8] Measures to prevent PA injuries should generally be based on knowledge about the incidence and severity of the PA injury problem, aetiological risk factors, and mechanisms contributing to the risk of sustaining such injuries.[9] Because a proper school-based PA injury prevention programme in children does not exist and evidence on effectiveness is lacking, development and evaluation of such a programme is necessary. An injury prevention programme can be developed using the intervention mapping (IM) protocol.[10,11] IM describes a process for developing theory- and evidence-based health promotion programmes, and involves a systematic process that prescribes a series of six steps: (i) performing a needs assessment; (ii) defining suitable programme objectives; (iii) selecting theory-based intervention methods and practical strategies; (iv) producing ª 2009 Adis Data Information BV. All rights reserved.
programme components and materials; (v) designing an implementation plan; and (vi) designing an evaluation plan (see figure 1). Collaboration between the developers, the users of the intervention and the target population is a basic assumption in the IM process.[12] This article describes in detail the development of a PA injury prevention programme for children by using the steps of the IM process. Step 6 of the process descibes in detail how to evaluate the effectiveness of such a programme. 1. Step 1: Perform a Needs Assessment Prior to the development of a PA injury prevention programme for children, the injury problem and the risk factors for PA injuries in children should be assessed. In order to gain insight into the needs of the target population, a focus group interview with 23 physical education (PE) teachers from 12 secondary schools was carried out. 1.1 The Injury Problem
Injuries cause children unnecessary suffering and pain in the short term.[1,8,13] Individuals who have experienced macro trauma or PA injuries to joints may be at risk of accelerated development of (secondary) osteoarthritis in later life.[14] Moreover, it is suggested that PA injuries sustained Step 1: Needs assessment Step 2: Define suitable programme objectives Step 3: Select theory-based intervention methods and practical strategies Step 4: Produce programme components and materials Step 5: Design an implementation plan Step 6: Design an evaluation plan Fig. 1. Steps of the intervention mapping process.
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Table I. Risk factors for physical activity injuries in children[5] Extrinsic risk factors non-modifiable
potentially modifiable
Intrinsic risk factors non-modifiable potentially modifiable
Sport played (contact/no contact)
Rules
Previous injury
(Aerobic) fitness level
Level of play (recreational/elite)
Playing time
Age
Pre-participation in sport-specific training
Position played
Playing surface (type/condition)
Sex
Flexibility
Weather
Equipment (protective/footwear)
Time of season/time of day
Strength Joint stability Biomechanics Balance/proprioception Psychological/social factors
at a young age have a negative influence on participation in PAs and sports.[15,16] Data from the period 2000–2004 revealed that in the Netherlands 1.5 million acute PA injuries are reported each year and 51% of these injuries are medically treated. The PA injury incidence in children aged 0–17 years is 1.3 (95% CI 1.2, 1.4).[17] The absolute number of PA injuries in the Netherlands increases for both sexes until the age of 12 years. Above this age, injuries in boys increase considerably until the age of 16 years. The highest number of PA injuries in girls is registered at 14 years of age. The most frequently injured body parts are the lower extremities. The ankle is the most affected part of the body (20%), followed by the knee (18%).[17] Although sport participation in children has increased (children aged 6–11 years: 88% in 1991 to 93% in 2003; children aged 12–19 years: 84% in 1991 to 93% in 2003), membership of sports clubs has decreased (children aged 6–11 years: 76% in 1991 to 74% in 2003; children aged 12–19 years: 77% in 1991 to 71% in 2003).[18] There are a large number of children who participate in organized team sports, but a growing number of children are attracted to non-organized sports activities and individual sports. There seems to be a trend for individualization, and children nowadays are attracted to sports other than traditional sports in a sport club.[19] The literature shows that most PA injuries occur during non-organized sports activities and leisure time.[20-22] Data from a nationwide survey in the Netherlands showed that school absence occurs ª 2009 Adis Data Information BV. All rights reserved.
in 7% of the children who sustained a sports injury, and the mean duration of school missed by these children was 8 days. This means that 0.02% of the total population who visit school and participate in sports are absent from school one or more days. With a mean duration of 8 days, the total school absence due to sports injuries can be calculated at 794 000 days a year. In addition, 22% of the people who sustained a PA injury were also absent from PAs.[17] The economic consequences of PA injuries in children are not known, but direct medical costs, for example medical treatments as a result of all PA injuries, were estimated at h170 and indirect medical costs, for example work or school absence, were estimated at h420 million (year of costing 2003).[23] Risk factors for PA injuries are factors that increase the potential risk for injury and include extrinsic risk factors (i.e. weather, field conditions) and intrinsic risk factors (i.e. age, conditioning). Identification of risk factors can be used as a leading guide for preventive measures. However, it is clear that injuries are caused mostly by a combination of factors. Table I shows the most important risk factors for PA injuries in children.[5] Based on these data, the aim our injury prevention programme should be to prevent lower extremity PA injuries in school children. A prevention programme to prevent PA injuries embedded in PE classes in schools will reach all the children who are physically active – not only children in sport clubs. PA injuries are defined as injuries occurring during organized sports activities, leisure time activities and PE class. Sports Med 2009; 39 (11)
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1.2 Focus Group Interviews
In order to gain insight into the needs of the target population and in order to be able to design a feasible intervention programme, focus group interviews were held. Five individual interviews and two focus group interviews were performed with 23 PE teachers from 12 secondary schools. In the Netherlands, children go to primary school until the age of 12 years, followed by attendance at secondary school. The interviewed secondary school PE teachers generally agreed there is a great diversity in physical fitness and motor performance in children in the first grade of secondary schools. Their common opinion was that these interindividual differences are an important contributing factor to PA injuries in children. Asking the interviewed PE teachers about the causes of the noted diversity in physical fitness and motor control, and particularly about possible solutions, they argued that an intervention programme should focus on primary school children. In primary schools, children receive regular PE classes. Unfortunately, these regular PE classes are not always supervised by certified PE teachers (due to economic reasons, the child’s regular teacher often provides the PE classes). However, the regular teachers usually do not incorporate injury prevention aspects in their PE classes; as general injury prevention lessons are not given in primary schools, it is likely that a preventive intervention in this setting can lead to maximum improvement. In addition, the PE teachers in secondary schools said they were hesitant and not motivated to incorporate our preventive intervention in their PE classes, because they already incorporated their own injury prevention in their PE classes. Because the PE teachers in secondary schools argued that the intervention programme should focus on primary schools since injury prevention lessons are already given in secondary schools, a shift from secondary school children to primary school children was made. From the focus group interviews with the PE teachers we also learned that, in general, the PE teachers were rarely confronted with injuries, and they were unaware of a sports injury problem ª 2009 Adis Data Information BV. All rights reserved.
among their pupils. From the interviews it became clear that raising injury knowledge in children, teachers and parents should be an important objective for our intervention programme. 2. Step 2: Define Suitable Programme Objectives This step provides the foundation for the programme by specifying who and what will change as a result of the intervention. The overall objective of our intervention programme was to reduce the incidence of lower extremity PA injuries. In order to achieve this overall objective, several risk-reduction behavioural and interpersonal environment ‘sub-objectives’ were defined that focus on children, parents and PE teachers. The underlying assumption of the risk-reduction behavioural sub-objectives is that if an intervention reduces the prevalence of risk factors, it will reduce the prevalence of PA injuries. Furthermore, the presence or absence of support from important others (e.g. parents, PE teachers) within the individual’s immediate interpersonal environment may have an influence on the performance of the injury-preventing behaviour.[24] The subobjectives used in our preventive measure are: (i) children take fewer injury-related risks; (ii) parents create a safe PA environment for their children outside PE classes; (iii) and teachers include injury prevention into their usual teaching routine. Performance objectives were defined on the basis of the programme objectives and describe what the participants in this programme need to do to perform the desired injury-preventing behaviour. The performance objectives for each programme objective are presented in table II. 3. Step 3: Select Theory-Based Intervention Methods and Practical Strategies The third step of the IM process is the selection of theory-based intervention methods and practical strategies to effect changes in the health behaviour of individuals, and to change organizational and societal factors to alter the environment. Sports Med 2009; 39 (11)
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Table II. Performance objectives for the four different programme objectives Performance objective
Programme objective 1: children will take fewer injuryrelated risks
Programme objective 2: parents will create a safe physical activity environment outside PE classes
Programme objective 3: PE teachers will include injury prevention into their usual teaching routine
1
Children learn the consequences of an injury
Parents learn the consequences of an injury
PE teachers learn the consequences of an injury
2
Children learn which risk factors cause injuries
Parents learn which risk factors cause injuries
PE teachers learn which risk factors cause injuries
3
Children gain insight into their own injury risk behaviour
Parents gain insight into the injury risks during the child’s leisure time physical activities
PE teachers gain insight into the pupils’ risk behaviour
4
Children form strategies to reduce their injury risk
Parents form strategies to reduce the injury risk during the child’s leisure time physical activities
PE teachers form strategies to reduce the pupils’ risk behaviour
5
Parents gain insight into the child’s risk behaviour
6
Parents form strategies to reduce the child’s risk behaviour
PE = physical education.
A ‘method’ can be described as a theoretically derived technique used to influence (determinants of) injury-preventing behaviour, and a ‘strategy’ as a practical way of organizing and delivering the intervention method.[12,25] 3.1 Theory-Based Intervention Methods
Preventive measures should target one or more of the risk factors mentioned earlier (table I). A potentially modifiable risk factor for PA injuries in children is wearing appropriate protective equipment and footwear during PAs. To decrease this risk factor, injury-preventing behaviour should be addressed. Injury-preventing behaviour is an indirect causal factor for PA injuries.[26] Therefore, improving this behaviour could be a method to decrease PA injury incidence and PA injury severity. To change injury-preventing behaviour, knowledge of determinants of behaviour is necessary.[27] We applied the attitude, social influence and self-efficacy (ASE) model for behaviour change. The ASE model is based on the theory of planned behaviour[28] and the social learning theory.[29] This model[30,31] postulates that intention, the most proximal determinant of behaviour, is determined by three conceptually independent constructs: attitude, social influence and self-efficacy. To change injury-preventing behaviour and finally decrease injury incidence, our programme ª 2009 Adis Data Information BV. All rights reserved.
tries to improve attitude, social influence, selfefficacy and intention towards wearing appropriate protective equipment and footwear during organized PAs, leisure time activities and PE classes (see figure 2). In addition, a second potentially modifiable risk factor for PA injuries in children is dimensions of motor fitness (e.g. flexibility, strength and balance/proprioception). Motor fitness and sport-specific skills have an impact on sports injuries.[32] There is some evidence that improving certain dimensions of motor fitness can decrease PA injuries. However, this evidence is found in sport-specific studies[33-38] (see figure 2). Theoretical methods are general techniques for influencing changes in determinants of behaviour. In our programme the following methods will be used: active learning, providing cues and scenario-based risk information, and active processing of information.[24] The related theories for the adopted methods are the persuasion communication matrix, elaboration likelihood, social cognitive theory, theories of information processing, and a precaution adoption process model.[24] 3.2 Practical Strategies
The next step is to translate the methods into practical strategies that can be used in a preventive measure. Knowledge is a basis for many different determinants of behaviour, but giving Sports Med 2009; 39 (11)
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Attitude The degree to which performance of injurypreventing behaviour is positively or negatively valued Social influence Consists of three components: - Subjective norms - Social support - Pressure and modelling
Intention
Injury-preventing behaviour
Decrease PA injury incidence rates Decrease severity of PA injuries
Self-efficacy The subjective probability that a person is capable of executing injury-preventing behaviour Motor fitness Dimensions of motor fitness are strength, flexibility, speed, power and balance/coordination Fig. 2. A conceptual model of injury prevention. PA = physical activity.
children information will not lead directly to behavioural change. However, behavioural determinants like attitude are based partly on knowledge.[39] The practical strategy that is used to deliver information in order to increase attitude, social influence, self-efficacy and motor fitness is an 8-month course about injury prevention. The communication channels are a course manual for teachers, newsletters for children and parents, posters for children, an exercise programme during PE lessons for children, and an interactive website. The newsletters can be made especially for children or parents, and the willingness to receive a newsletter is usually good.[24] In addition, posters can be effective in calling attention to a campaign and they provide continuous exposure to the children.[24] Table III gives an overview of the determinants, methods, theories and strategies to reach the programme objectives. 3.3 Interpersonal Environment
Changing determinants of behaviour is almost always embedded in one or more environmental levels. A child participating in PAs is in an environment with parents and PE teachers, thereª 2009 Adis Data Information BV. All rights reserved.
fore parents and PE teachers should also be involved in the intervention programme.[24] Parents are very important in creating a safe PA environment outside PE classes. They should encourage their children to play safe,[40] and they are important as role models for their children. The influence of parental rules and pressure has been found to have a strong effect on the use of protective equipment.[41-43] PE teachers are very important in creating a safe PA environment during PE classes. In order to prevent injuries in PE classes it is important that teachers include injury prevention into their usual teaching routine. If PE teachers include injury prevention into their teaching routines, they will teach children how to prevent injuries during PAs, not only during PE classes, but also outside school. 4. Step 4: Produce Programme Components and Materials The task in this step of the IM process is to translate methods and practical strategies into programme components and materials. Our injury prevention programme as a whole is not Sports Med 2009; 39 (11)
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specified for any specific type of sport. It addresses the most common injuries and preventive measures in general and includes the programme components and materials outlined below. 4.1 Newsletters
Monthly newsletters are produced for both children and parents. The aim of the newsletters is to increase knowledge and awareness about injury prevention. The monthly newsletters consist of information about injury prevention, selfevaluation tests and puzzles on a specific topic. By providing a monthly newsletter, new information will be given each month in a motivational way. It is believed that this will remind all involved each month of the task of preventing PA injuries.
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speed, balance/coordination and flexibility). The exercises are developed on the basis of exercises from ‘active childhood-healthy life’,[44] exercises from ‘Basisdocument Bewegingsonderwijs’,[45] and exercises from a programme to prevent lower limb injuries in youth sports.[37] Table IV gives examples of the exercises that are done during the PE classes. 4.4 Website
The website (www.iplaystudy.nl) contains general information about injury prevention for children, parents and PE teachers, who can view the newsletters online, and children can check their solutions to the newsletter puzzles. Additionally, various instruction videos and photos are displayed to illustrate for PE teachers how to teach the exercises.
4.2 Posters
Eight different posters (A1 size, i.e. 594 · 840 mm) show the highlights of the content of the newsletters. The posters contain important and clear messages about injury prevention and are very colourful and have humorous cartoon images in order to make the posters attractive to children. They are displayed in the classroom, so that the children are able to see the posters continuously. 4.3 Exercises to Improve Motor Fitness
A short training circuit is performed at the beginning and the end of each PE class, twice a week. This circuit consists of exercises aimed at the improvement of motor fitness (i.e. strength,
4.5 Pretesting and Revising
Pilot testing of programme strategies and materials with intended implementers and recipients is an important part of step 4. 4.5.1 Pretesting the 8-Month Course
Teachers and children of six primary schools were informed about the programme in full detail. Teachers were asked for their comments on the topics and timing of the different modules of the 8-month course via a focus group interview. With the exception of a few minor comments, all interviewed primary school teachers were positive about the programme and believed the programme to be feasible and effective. Children
Table III. Theoretical methods and practical strategies to reach programme objective Determinants
Methods
Theory
Strategies
Attitude
Active learning
Persuasion communication matrix
Newsletter delivered to children and parents to improve knowledge
Social influence
Cues
Elaboration likelihood
Posters exposed to children in the classroom to improve knowledge
Self-efficacy
Scenario-based risk information
Social cognitive theory
Course manual for teachers
Motor fitness
Active processing of information
Theories of information processing
Short circuit training to improve motor fitness during physical education classes
Precaution adoption process model
Website accessible for children, parents and teachers
ª 2009 Adis Data Information BV. All rights reserved.
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Table IV. Examples of the iPlay-programme of exercises used to prevent injuries Strength
Coordination
Speed
Forward jumps
Passing the ball (one leg stance)
Shuttle run
Flexibility of hamstring
Squats to 80 of knee flexion
Skate jumps
Race course
Flexibility of calf muscle
Hand wrestling in push-up stand
Pushing each other off balance (one leg stance)
Spurts from different start positions
Flexibility of biceps femoris
responded in a comparable way and were very enthusiastic about the monthly newsletters and posters. Although the programme also targets parents, for practical reasons they were not asked for their comments about the 8-month course. However, the positive response of teachers and children led us to believe that the programme will be widely accepted in its current form. 4.5.2 Pretesting Exercise Programme
The exercise programme to improve motor fitness was pretested in two different primary schools, involving three PE teachers. Teachers were asked specifically for their comments on the feasibility of the exercises, the level of intensity, the degree of difficulty of the exercises and the clarity of the manual. Some exercises were perceived as too difficult or taking too much time. Additionally, the teachers advised delivery of the exercises in a more competitive and playful way. Exercises were adapted as suggested by the PE teachers. The teacher’s manual was considered to be very clear. 5. Step 5: Design an Implementation Plan This step focuses on the design of an implementation plan, in order to ensure that an injury prevention programme will be implemented, adopted and sustained over time. The intervention programme is a ‘ready to use’ preventive measure so it can be implemented directly in PE lessons, if proven effective. The Royal Association of Teachers of Physical Education (KVLO) and the Academy for PE Teachers’ Education will then play an important role in the implementation. The KVLO controls the standards and continuity of physical education in the Netherlands, and has a wide array of implementation channels. Thereby, the KVLO will ª 2009 Adis Data Information BV. All rights reserved.
Flexibility
be an important channel through which the preventive programme can be implemented not only by today’s PE teachers, but also by the PE teachers of the future. Another channel that plays an important role in successful implementation is the academic school where PE teachers are educated. The KVLO and the Academy for PE Teachers’ Education have been involved in the study from the very beginning and have participated in the IM process. By using IM, the programme was tailored to the wishes of the end users. In doing so, the practical and logistical issues of implementation have been minimized. 6. Step 6: Design an Evaluation Plan Through effect and process evaluation, IM planners can determine whether decisions were correct at each mapping step. To evaluate the effect of the intervention, the decrease in injury incidence will be analysed in a cluster randomized controlled trial. The primary research questions addressed are: ‘‘What is the effect of the injury prevention programme on lower extremity PA injury incidence and severity?’’ and ‘‘What is the cost effectiveness of this programme?’’ The secondary research question is: ‘‘What is the effect of the injury prevention programme on the improvement of knowledge, (determinants of) injury-preventing behaviour and motor fitness?’’ 6.1 Sample Size
A difference in the incidence of acute lower extremity injuries of 7% between the intervention and control group after 8 months is considered clinically relevant. To detect a difference of 7% in the incidence of lower extremity PA injures with a power of 90% and an a of 5%, 500 children per group (intervention/control) are needed in an Sports Med 2009; 39 (11)
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evaluation study. However, in order to perform multi-level analyses taking into account a cluster randomization design (schools as randomization level) – with an intra-cluster correlation coefficient of 10% and a dropout rate of 20% – a total of 2280 children from 40 schools are required at baseline. 6.2 Recruitment 6.2.1 Recruitment of Primary Schools
The evaluation will be carried out in Dutch primary schools. From the 7000 primary schools throughout the Netherlands, 520 primary schools are randomly selected from a database and invited by means of an information flyer. Inclusion criteria for the primary schools are: (i) being a regular primary school; (ii) giving PE lessons twice a week; and (iii) being willing to appoint a contact person for the duration of the study. A flowchart of the recruitment of primary schools is given in figure 3. 6.2.2 Recruitment of Children and their Parents
The children and parents from the participating schools receive an information letter about the study design. All children are eligible for inclusion in the study. The parents receive a passive informed consent request: this consent procedure assumes that the parents consent, unless the
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researcher is contacted by means of a telephone call or by sending an email. 6.3 Randomization
Schools serve as randomization units to avoid spillover of the intervention within schools. A stratified randomization is performed based on geographic location (urban/suburban) and professional status of the PE teacher (certified/ uncertified), resulting in four strata. From each stratum, schools are randomly allocated to the intervention or control group by a computerized random number generator. Before the school year starts, the primary schools are informed about the group (intervention/control) they are assigned to. 6.4 Primary Outcome Measures 6.4.1 Injury Definition and Registration
Throughout the school year, PA injuries are recorded continuously by PE teachers. They are instructed to question children explicitly every week about whether they have been injured as a result of PAs (including non-organized events) in the past week. The injury definition, as described by van Mechelen et al.,[9] is used where a PA injury is any injury as a result of participation in PE class, sport activities or leisure time PAs
520 primary schools 370 primary schools did not respond at all
105 primary schools not willing to participate
45 primary schools willing to participate
40 primary schools participate in the iPlay study (n = 2210)
Reasons: - No time (n = 58) - Missing value (n = 15) - Not relevant (n = 10) - Already participating in other project (n = 8) - No interest (n = 8) - Change in teacher (n = 5)
Five primary schools were excluded: - Only once-a-week PE class (n = 3) - Change in teacher at the beginning of the school year (n = 1) - Already participates in the study with another primary school (n = 1) Control group = 20 schools (n = 1093) Randomization Intervention group = 20 schools (n = 1117)
Fig. 3. Flowchart of recruitment in primary schools. PE = physical education.
ª 2009 Adis Data Information BV. All rights reserved.
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with one or more of the following consequences: the child (i) has to stop the physical activity and/or (ii) cannot (fully) participate in the next planned PA (applies also to planned leisure time PAs) and/or (iii) cannot go to school the next day and/or (iv) needs medical attention ranging from onsite care (e.g. first-aid personnel) to personal care (e.g. physiotherapist or sports physician). In case of an injury, the child is asked to complete an injury registration form. The injury registration form collects information on injury type, injury location, direct cause of the injury and activity performed at the time of injury. Injury incidence refers to the number of new PA injuries during a particular period of time (e.g. 1 year). One method to express incidence rates is to calculate the incidence of PA injuries in relation to exposure (in days, hours or sport event). To determine time at risk for PA injuries, all children complete a questionnaire in the classroom twice a year. This questionnaire collects information on exposure time (sports and leisure-time PA participation). 6.4.2 Cost Effectiveness
In order to evaluate the cost effectiveness of the preventive measure, all parents from children who sustain a PA injury receive a cost diary. The cost diary is a log in which parents register all (para-) medical treatment (including use of medication), absence from school and sport activities, and other discomfort from the moment of injury onwards, until full recovery. From these cost diaries, direct and indirect costs resulting from the sustained injury can be calculated for use in the economic evaluation. 6.5 Secondary Outcome Measures
Knowledge, injury-preventing behaviour, behavioural determinants and motor fitness are measured at baseline (start of the school year) and follow-up (end of the school year). 6.5.1 Questionnaires
Children are requested to complete a questionnaire in the classroom. The children take home the questionnaire to their parents, who are asked to complete their questionnaire and return ª 2009 Adis Data Information BV. All rights reserved.
it to the research team in a pre-stamped reply envelope. Knowledge about injury prevention is measured with one question on self-reported improvement in knowledge of how to prevent PA injuries, as well as a knowledge test including nine multiple-choice questions about injury prevention in general. Behavioural determinants are assessed with the following constructs: attitude, social influence, self-efficacy and intention. The injurypreventing behaviour is defined as wearing appropriate protective equipment and footwear during organized PAs, leisure time and PE class. Attitude towards the injury-preventing behaviours is assessed with three questions. Social influence is assessed with questions regarding social norm, modelling of friends, and modelling of parents. Self-efficacy is assessed with two questions relating to the child’s perception of their ability to perform injury-preventing behaviour. Intention and behaviour towards wearing protective equipment and appropriate shoes during organized PAs, leisure time and PE class are assessed with one question. All answers on the questions are given on a five-point Likert scale varying from always (1) to never (5) or totally agree (1) to totally do not agree (5). All questions are positively formulated. We pretested the questionnaires on comprehensibility, (lack of) clarity and practical applicability in 54 children and their parents. Based on the results of the pretest, we changed some questions to increase comprehensibility, deleted excessive text messages and shortened the questionnaire to decrease completion time. 6.5.2 MOPER Fitness Test
Motor fitness is assessed with the MOtor PERformance (MOPER) fitness test. Supervised by a research assistant, groups of three to four children perform seven test items of the MOPER fitness test (bent arm hang test, 10 · 5 m run test, plate tapping test, leg lift test, sit and reach test, arm pull test and standing high jump test), and they are asked to perform all test elements as well as possible. For practical reasons, we decided to exclude the 6-minute endurance run. For an Sports Med 2009; 39 (11)
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extensive description of the MOPER fitness test items, see Leyten et al.[46] In addition, children perform the flamingo balance test, which has been described in the EUROFIT test.[47] To be able to complete all tests during one PE class we shortened the flamingo balance test to 30 seconds instead of 1 minute as the original flamingo balance test protocol indicates. All test items are performed barefoot to rule out the effect of footwear on the test results. Body height and weight are also measured. Body height is measured in metres to the nearest centimetre with a portable stadiometer (Seca 214, Leicester Height Measure; Seca GmbH & Co, Hamburg, Germany). Asking the subject to stand straight, with the heels together and looking straight ahead, standardizes positioning of the body. Body weight is measured to the nearest 0.1 kg with a digital scale (Seca 770; Seca GmbH & Co, Hamburg, Germany). During the body height and weight measurements, children wear only underwear. 6.6 Statistical Analysis
The effects of the intervention will be assessed using multilevel regression analysis. This statistical technique takes into account the dependency of observations of different children from the same class and school. Analyses will be adjusted for baseline values and, if necessary, for other confounders. The economic evaluation will be assessed using mean direct (i.e. medical costs), indirect (i.e. costs for absence from school/work) and total costs from the cost diaries. Because costs are generally not normally distributed, 95% confidence intervals for the differences in mean costs will be obtained by bias-corrected and accelerated bootstrapping. Differences in costs and differences in injury incidence will be included in a cost-effectiveness ratio, which estimates the additional costs to prevent one PA injury. 6.7 Process Evaluation
A process evaluation is included to monitor programme implementation, which will gain insight into the relationship between specific proª 2009 Adis Data Information BV. All rights reserved.
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gramme elements and programme outcomes.[48] The injury prevention programme will be evaluated with the use of the RE-AIM (reach, efficacy/ effectiveness, adoption, implementation and maintenance) framework.[49] All PE teachers, children and parents assigned to the intervention group are asked to complete the process evaluation questionnaire.
7. Discussion and Conclusions Regular PA has many health benefits, but also increases the risk of PA injuries. This paper describes how to develop and evaluate a preventive measure using the IM protocol. To our knowledge, this is the first time this has been done in the injury prevention field. Although this strategy has never been used before in this field, the underlying systematic ‘evidence-based’ process and the contribution of the field of practice make the IM method likely superior to any other method for developing an injury prevention programme. The IM protocol provides a valuable checklist for the development of an intervention programme. However, it is a rather time-consuming process. The research on determinants, definition of suitable performance objectives, moving back and forth between the IM steps, and the pretesting of materials required much time. This makes it sometimes difficult to apply the IM process according to the full instructions. The results of the evaluation study will be published elsewhere. Preliminary analysis clearly indicates that the iPlay study resulted in a significant decrease in injury incidence in the intervention group. Moreover, the results of the evaluation study will help to gain more insight into the effects of school-based injury prevention programmes. Acknowledgements The iPlay study is supported by a grant from the Netherlands organization for health research and development (ZONMW), grant number 62200033. The authors have no conflicts of interest that are directly relevant to the content of this review.
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Authors’ contribution: EV was involved in developing the concept and the design of the study. DC, MC and EV were involved in further developing the idea and the protocol for carrying out the study. DC was responsible for the data collection and she drafted the manuscript. All authors contributed to the final manuscript by reading and correcting draft versions.
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18. SCP. Rapportage Sport 2006. The Hague: 2006 19. SCP. Rapportage jeugd 2002. Sociaal en Cultureel Planbureau, Den Haag, 2003 20. Kahl H, Dortschy R, Ellsasser G. Injuries among children and adolescents (1-17 years) and implementation of safety measures: results of the nationwide German Health Interview and Examination Survey for Children and Adolescents (KiGGS). Bundesgesundheitsblatt Gesundheits forsch Gesundheitsschutz 2007 May; 50 (5-6): 718-27 21. Schneiders W, Rollow A, Rammelt S, et al. Risk-inducing activities leading to injuries in a child and adolescent population of Germany. J Trauma 2007 Apr; 62 (4): 996-1003 22. Sundblad G, Saartok T, Engstrom LM, et al. Injuries during physical activity in school children. Scand J Med Sci Sports 2005 Oct; 15 (5): 313-23 23. Toet H, Schoots W, den Hertog PC, et al. Kosten van sportblessures in Nederland. Amsterdam: Consument en Veiligheid, 2005 24. Bartholomew LK, Parcel GS, Kok G, et al. Planning health promotion programs, an intervention mapping approach. San Fransico (CA): Jossey-Bass, 2006 25. Caine D, Caine C, Maffulli N. Incidence and distribution of pediatric sport-related injuries. Clin J Sport Med 2006 Nov; 16 (6): 500-13 26. Klassen TP, MacKay JM, Moher D, et al. Communitybased injury prevention interventions. Future Child 2000; 10 (1): 83-110 27. Machenbach J, van der Maas PJ. Volksgezondheid en gezondheidszorg. Maarsen: Elsevier Gezondheidszorg, 1999 28. Fishbein M, Ajzen I. Belief, attitude, intention and behavior: an introduction to theory and research. New York (NY): Wiley, 1975 29. Bandura A. Social foundations of thought and action: a social cognitive theory. Englewood Cliffs (NY): Prentice Hall, 1986 30. de Vries H, Dijkstra M, Kuhlman P. Self-efficacy: the third factor besides attitude and subjective norm as a predictor of behavioural intentions. Health Educ Res 1988; 3: 273-82 31. Kok G, de Vries H, Mudde A, et al. Planned health education and role of self-efficacy: Dutch research. Health Educ Res 1991; 6: 231-8 32. Verstappen FT, Twellaar M, Hartgens F, et al. Physical fitness and sports skills in relation to sports injuries: a fouryear prospective investigation of sports injuries among physical education students. Int J Sports Med 1998 Nov; 19 (8): 586-91 33. Emery CA, Cassidy D, Klassen TP. The effectiveness of a proprioceptive balance-training program in healthy adolescents: a cluster randomized controlled trial. Am J Epidemiol 2004; 159: 749-54 34. Heidt Jr RS, Sweeterman LM, Carlonas RL, et al. Avoidance of soccer injuries with preseason conditioning. Am J Sports Med 2000 Sep; 28 (5): 659-62 35. Hewett TE, Lindenfeld TN, Riccobene JV, et al. The effect of neuromuscular training on the incidence of knee injury in female athletes: a prospective study. Am J Sports Med 1999 Nov; 27 (6): 699-706 36. Junge A, Rosch D, Peterson L, et al. Prevention of soccer injuries: a prospective intervention study in youth amateur players. Am J Sports Med 2002 Sep; 30 (5): 652-9
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37. Olsen OE, Myklebust G, Engebretsen L, et al. Exercises to prevent lower limb injuries in youth sports: cluster randomised controlled trial. BMJ 2005 Feb 26; 330 (7489): 449 38. Verhagen E, van der BA, Twisk J, et al. The effect of a proprioceptive balance board training program for the prevention of ankle sprains: a prospective controlled trial. Am J Sports Med 2004 Sep; 32 (6): 1385-93 39. Brug J, Schaalma H, Kok G, et al. Gezondheidsvoorlichting en gedragsverandering, een planmatige aanpak. Assen: Van Gorcum, 2001 40. Otis J, Lesage D, Godin G, et al. Predicting and reinforcing children’s intentions to wear protective helmets while bicycling. Public Health Rep 1992 May; 107 (3): 283-9 41. Berg P, Westerling R. Bicycle helmet use among schoolchildren: the influence of parental involvement and children’s attitudes. Inj Prev 2001 Sep; 7 (3): 218-22 42. Finch CF. Teenagers’ attitudes towards bicycle helmets three years after the introduction of mandatory wearing. Inj Prev 1996 Jun; 2 (2): 126-30 43. Miller PA, Binns HJ, Christoffel KK. Children’s bicycle helmet attitudes and use: association with parental rules. The Pediatric Practice Research Group. Arch Pediatr Adolesc Med 1996 Dec; 150 (12): 1259-64 44. Zahler L, Puhse U, Stussi C, et al. Active childhood-healthy life. Basle: Swiss Federal Office of Sports Magglinger
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(FOSPO); Institute for Exercise and Health Science, University of Basle, 2004 van Berkel M, Consten A, Danes H, et al. Basisdocument; bewegingsonderwijs. Zeist: Jan Luiting Fonds, 2004 Leyten C, Kemper H, Verschuur R. de MOPER hitheidstest: handleiding en prestatieschalen 9 t/m 11 jarigen. Haarlem: De Vrieseborch, 1982 Adam C, Klissouras V, Ravazzolo M, et al. Handbook for the EUROFIT test of Physical Fitness. Brussels: Council of Europe committee for the development of sport, 1988 Saunders RP, Evans MH, Joshi P. Developing a processevaluation plan for assessing health promotion program implementation: a how-to guide. Health Promot Pract 2005 Apr; 6 (2): 134-47 Dzewaltowski DA, Glasgow RE, Klesges LM, et al. RE-AIM: evidence-based standards and a Web resource to improve translation of research into practice. Ann Behav Med 2004 Oct; 28 (2): 75-80
Correspondence: Dr Mai J.M. Chinapaw, EMGO Institute and Department of Public and Occupational Health, VU University Medical Center, Van der Boechorststraat 7, 1081 BT Amsterdam, the Netherlands. E-mail:
[email protected]
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Sports Med 2009; 39 (11): 903-921 0112-1642/09/0011-0903/$49.95/0
REVIEW ARTICLE
ª 2009 Adis Data Information BV. All rights reserved.
Neuromuscular Adaptations to Training, Injury and Passive Interventions Implications for Running Economy Jason Bonacci,1,2 Andrew Chapman,1,3,4,5 Peter Blanch2 and Bill Vicenzino1 1 Musculoskeletal Pain and Injury Research Unit, University of Queensland, Brisbane, Queensland, Australia 2 Department of Physical Therapies, Australian Institute of Sport, Canberra, Australian Capital Territory, Australia 3 School of Kinesiology, Simon Fraser University, Vancouver, British Columbia, Canada 4 Applied Research Centre, Australian Institute of Sport, Canberra, Australian Capital Territory, Australia 5 Department of Kinesiology and Physical Education, McGill University, Montreal, Quebec, Canada
Contents Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Literature Search . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Adaptations of Muscle Recruitment to Single-Discipline Endurance Training . . . . . . . . . . . . . . . . . . . . 3. Adaptation of Muscle Recruitment to Multidiscipline Endurance Training . . . . . . . . . . . . . . . . . . . . . . . 4. Neuromuscular Characteristics and Running Economy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. Training, Shoes, In-Shoe Orthoses, Musculoskeletal Injury and Running Economy. . . . . . . . . . . . . . . . . 5.1 Resistance Training . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2 Plyometric Training . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.3 Stretching . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.4 Multidiscipline Sports and Training . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.5 Shoes and In-Shoe Orthoses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.6 Musculoskeletal Injury. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7. Future Directions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Abstract
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Performance in endurance sports such as running, cycling and triathlon has long been investigated from a physiological perspective. A strong relationship between running economy and distance running performance is well established in the literature. From this established base, improvements in running economy have traditionally been achieved through endurance training. More recently, research has demonstrated short-term resistance and plyometric training has resulted in enhanced running economy. This improvement in running economy has been hypothesized to be a result of enhanced neuromuscular characteristics such as improved muscle power development and more efficient use of stored elastic energy during running. Changes in indirect measures of neuromuscular control (i.e. stance phase contact times, maximal forward jumps) have been used to support this hypothesis. These results suggest that neuromuscular adaptations in response
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to training (i.e. neuromuscular learning effects) are an important contributor to enhancements in running economy. However, there is no direct evidence to suggest that these adaptations translate into more efficient muscle recruitment patterns during running. Optimization of training and run performance may be facilitated through direct investigation of muscle recruitment patterns before and after training interventions. There is emerging evidence that demonstrates neuromuscular adaptations during running and cycling vary with training status. Highly trained runners and cyclists display more refined patterns of muscle recruitment than their novice counterparts. In contrast, interference with motor learning and neuromuscular adaptation may occur as a result of ongoing multidiscipline training (e.g. triathlon). In the sport of triathlon, impairments in running economy are frequently observed after cycling. This impairment is related mainly to physiological stress, but an alteration in lower limb muscle coordination during running after cycling has also been observed. Muscle activity during running after cycling has yet to be fully investigated, and to date, the effect of alterations in muscle coordination on running economy is largely unknown. Stretching, which is another mode of training, may induce acute neuromuscular effects but does not appear to alter running economy. There are also factors other than training structure that may influence running economy and neuromuscular adaptations. For example, passive interventions such as shoes and in-shoe orthoses, as well as the presence of musculoskeletal injury, may be considered important modulators of neuromuscular control and run performance. Alterations in muscle activity and running economy have been reported with different shoes and in-shoe orthoses; however, these changes appear to be subject-specific and nonsystematic. Musculoskeletal injury has been associated with modifications in lower limb neuromuscular control, which may persist well after an athlete has returned to activity. The influence of changes in neuromuscular control as a result of injury on running economy has yet to be examined thoroughly, and should be considered in future experimental design and training analysis.
Endurance sports such as running, cycling and triathlon are performed by many people at the recreational and competitive levels. At competition level, each of these sports requires extensive training. Triathlon is unique in that it is a multidiscipline sport requiring athletes to balance the training demands of three separate disciplines (i.e. swimming, cycling, running). The physiological and metabolic adaptations that occur in response to training have been extensively investigated. Oxygen consumption, blood lactate threshold, heart rate intensity, respiratory exchange ratio and the pulmonary ventilation threshold are common measures used to reflect endurance performance or adaptation to training.[1] ª 2009 Adis Data Information BV. All rights reserved.
The steady-state oxygen consumption at a given running velocity is defined as running economy,[2,3] and reflects the metabolic cost or metabolic demand of running. A strong relationship has been demonstrated between running economy and endurance running performance.[2,4-7] These measures highlight the relationship between the cardiorespiratory system and performance; however, they do not reflect the contribution of the neural system, which controls and coordinates human movement. The interaction between the neural and muscle systems (i.e. neuromuscular system) is fundamental to all movement, and effectively translates cardiorespiratory capacity into efficient movement and therefore into performance. Sports Med 2009; 39 (11)
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The neuromuscular system has the capability to adapt to training, not unlike the cardiorespiratory system. Studies over the past two decades have provided strong evidence that continued practice of a task (i.e. training) facilitates neuromuscular adaptations, which are characterized by more skilled control of movement and muscle recruitment patterns.[8-11] Traininginduced adaptations of descending motor commands reflect learning within the CNS and can be represented by changes in muscle electromyography (EMG) function (i.e. motor recruitment).[11] Like training, musculoskeletal pain and injury[12,13] – and passive interventions such as shoes and in-shoe orthoses[14-17] (which are often prescribed for pain and/or injury) – have been shown to induce acute adaptations in motor recruitment. Musculoskeletal overuse injury is a significant adverse effect of training that constitutes a major impediment to training and ultimately performance, through missed training and/or diminished training quality. The prevalence of lower extremity injury in recreational and competitive athletes ranges from 19.4% to 79.3% in running athletes[18] and 37–91% in athletes participating in triathlons.[19] An injuryinduced restriction in training can result in detraining, which may negatively affect performance, cardiorespiratory health and neuromuscular control.[20,21] It is apparent within the literature that training can induce positive changes in running economy.[22,23] Training also appears to induce adaptations in motor recruitment.[8,9,11] Less well known are the neuromuscular adaptations that occur with different modes of training (i.e. running, cycling, multidiscipline training, resistance training) and how these changes in neuromuscular control can be coupled with running economy. It has recently been hypothesized that improvements in running economy following strength and resistance training were due to neuromuscular adaptations.[24-26] Inferences have also been made that optimal lower limb muscle recruitment is critical for superior running economy.[27] However, these hypotheses have been based on indirect measures of neuromuscular control such as stance phase ground contact ª 2009 Adis Data Information BV. All rights reserved.
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times and leg strength during isolated tasks as evidence for neuromuscular adaptations. If neuromuscular adaptations are responsible for the changes in running economy then it would be reasonable to suggest that there would be alterations in motor recruitment during running following training. It is important to appreciate that adaptations in motor recruitment as a result of training represent a learning effect. Positive adaptations infer that an individual learns to produce specific patterns of muscle recruitment that are associated with optimal performance of the task. This is inherently different to the alterations in neuromuscular function that occur with fatigue during prolonged exercise.[28] Fatigue in itself is a complex phenomenon and much attention has already been directed toward better understanding the mechanisms of fatigue and regulation of output during endurance exercise.[29-32] Accordingly, the intent of this review is not to revisit this information nor discount the importance of fatigue in modulating exercise performance but rather to discuss the adaptations in motor recruitment (i.e. learning effects) that occur with different modes of training, injury and passive interventions and the implications this may have for running economy. Therefore, the aims of this review are to: (i) examine the adaptations of lower limb muscle recruitment (i.e. neuromuscular adaptations) to different modes of training (i.e. running, cycling, multidiscipline); (ii) examine what aspects of neuromuscular control are associated with running economy; and (iii) investigate whether neuromuscular adaptations induced by training, passive interventions and injury can be coupled with changes in running economy.
1. Literature Search The databases Cinahl, MEDLINE, PubMed, SportDiscus and Web of Science were searched using the following combination of terms: (‘running economy‘ or ‘oxygen consumption’ or . ‘VO2’) and (‘EMG’ or ‘muscle activity’ or ‘neuromuscular’) or (‘EMG’ or ‘neuromuscular’ or Sports Med 2009; 39 (11)
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‘running economy’ or ‘oxygen consumption’) and (‘orthoses’ or ‘orthotics’ or ‘shoes’ or ‘resistance training’ or ‘plyometrics’ or ‘injury’ or ‘cycling’ or ‘triathlon’). The reference lists of the articles obtained were searched manually to obtain further studies not identified electronically. All relevant studies in the English language were included.
2. Adaptations of Muscle Recruitment to Single-Discipline Endurance Training Motor learning studies have demonstrated that continued practice of a task results in more skilled control of movement, characterized by decreased amplitude and duration of muscle activity,[8-10] decreased muscle co-activation[9,11,33] and less variability of movement.[9,11,34] However, these studies examined novel hand and arm movements over a short training period (e.g. 1–2 days), and their results provide little insight into the adaptations of muscle recruitment that may occur in response to years of continued training by athletes. Furthermore, there is very little research that has directly measured the neuromuscular adaptations that occur in response to endurance training such as cycling and running, which involve repetitive, rhythmical actions. Initial studies comparing muscle recruitment patterns of trained cyclists to their novice counterparts presented conflicting findings and are limited by small sample sizes, EMG methodological limitations, and inadequate regard for kinematics (i.e. kinematics were not controlled or measured and any difference in EMG activity may have been due to kinematic changes).[35,36] Similarly, running studies[37,38] are hindered by the heterogeneity of participants and inadequate inclusion criteria, making it difficult to determine the specific training status of included athletes. Only recently has evidence emerged that trained cyclists and runners display different patterns of muscle recruitment to their novice counterparts. Novice cyclists with 1.4 – 0.4 years of cycling experience, who cycled 36.1 – 10.3 km/wk, exhibited greater individual variance (i.e. variability of muscle activity between pedal ª 2009 Adis Data Information BV. All rights reserved.
strokes for individual cyclists), greater population variance (i.e. variability of muscle recruitment between athletes), more extensive and more variable muscle co-activation and longer durations of muscle activity than highly trained cyclists with 10.2 – 1.4 years’ experience, cycling 393.9 – 32.5 km/wk[39] (figure 1[40]). A similar finding emerged when moderately trained runners (6.6 – 1.3 years’ experience, 61.4 – 8.8 km/wk) were compared with novice runners (3.4 – 2.8 km/wk).[41] Specifically, novice runners were characterized by greater individual variance (i.e. variability between strides) and greater population variance. These findings are consistent with previous short-term training studies of arm and hand movements,[8,9,33] suggesting that ongoing neuromuscular adaptations occur as a result of continued training. The cross-sectional nature of the cycling and running studies is a clear limitation. However, given the limitations of the aforementioned studies, and the difficulties of tracking athletes over many years of training, this is the strongest evidence of continuing neuromuscular adaptations to endurance training available at present. Trained triathlete
Trained cyclist
Novice cyclist
TA
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PL
GL
SOL 0°
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Fig. 1. Rectified electromyogram (EMG) of tibialis anterior (TA), tibialis posterior (TP), peroneus longus (PL), lateral gastrocnemius (GL), and soleus (SOL) muscles during cycling at 77.5 rpm. Data for ten non-contiguous pedal strokes from a representative highly trained triathlete, highly trained cyclist and novice cyclist are shown. EMG amplitude is shown as a percentage of the maximum measured amplitude (0–100%). Muscle activity is plotted for each complete pedal stroke from upper vertical position of the crank (0) through to a range of 360 (reproduced from Chapman et al.,[40] with permission).
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3. Adaptation of Muscle Recruitment to Multidiscipline Endurance Training Multidiscipline endurance sports such as triathlon carry high training demands and are likely to provide an immense challenge to the human motor control system. Triathlon comprises sequential swimming, cycling and running, and triathletes often practice two or more of these disciplines in the one training session or practice each discipline separately with only short recovery periods (i.e. 2–4 hours). Short-term motor learning studies (i.e. 1–7 days of training) provide strong evidence that interference with acquisition of a new skill occurs when another task is practiced in sequence or within short interim periods.[42-45] Specifically, when multiple tasks are practiced in sequence or within short interim periods (i.e. <6 hours), learning of the second movement task was biased by the previous task in the sequence, and with each change of task, training adaptations were overwritten.[42-44,46] These studies provide evidence of interference with motor learning in the initial stages of training. However, the nature of triathlon training (i.e. athletes who practice multiple disciplines with no recovery periods or only short recovery periods) may provide an appropriate model to investigate the ability of the neuromuscular system to adapt (i.e. adaptations of muscle recruitment) to ongoing multidiscipline training. Evidence suggests that running and cycling performance of triathletes is less than that for cycling and running athletes who train for the single discipline (i.e. those who only train for running or who only train for cycling).[47] It could be argued that the decrement in performance is due to less time spent training the single discipline despite similar total training times. However, Chapman et al.[40] have shown that patterns of leg muscle activity in highly trained triathletes are less developed than in cyclists matched for cycling training loads. Specifically, triathletes show greater variation between pedal strokes, more extensive and variable muscle co-activity, less modulation of muscle activity (i.e. greater amplitude of muscle activity in periods between primary bursts), and display patterns of muscle ª 2009 Adis Data Information BV. All rights reserved.
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activity similar to that of novice cyclists (figure 1). The authors suggested that the similarity of leg muscle recruitment during cycling between highly trained triathletes and novice cyclists may reflect ongoing interference with motor learning and neuromuscular adaptation as a result of multidiscipline training.[40] Unlike cycling, multidiscipline training does not appear to adversely affect adaptation of running muscle activity in highly trained triathletes.[41] The difference in leg muscle recruitment during cycling between triathletes and cyclists only highlights a disparity between groups at a point in time. However, in order to provide stronger evidence that ongoing multidiscipline training interferes with adaptations of muscle recruitment, researchers would have to use a longitudinal motor learning paradigm. This would require strict control of training structure and continued re-assessment over years of training, and would be especially difficult to undertake. 4. Neuromuscular Characteristics and Running Economy In the late 1980s, Noakes[48] suggested that endurance performance may be limited not only by aerobic power but also by ‘muscle power’ factors related to force and velocity characteristics of the neuromuscular system. Later investigations used a battery of tests to determine the influence of neuromuscular characteristics on performance. In a homogenous group of. highly trained endurance runners with similar VO2max values, those athletes with faster 10 km and 5 km run times displayed shorter stance phase contact times and higher relative muscle pre-activation (i.e. prior to touchdown), accompanied with lower relative electromyographic (iEMG) activity during the propulsion phase than those athletes with slower run times.[49,50] Furthermore, there was a significant correlation between running economy and mean stance phase contact times during constant velocity running.[49] The authors speculated that in addition to aerobic power and running economy, the ability of the neuromuscular system to repeatedly produce rapid force during maximal and submaximal running Sports Med 2009; 39 (11)
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plays an important role in determining distance running performance in highly trained athletes. It has been suggested that shorter stance phase contact times and greater muscle pre-activation may represent enhanced leg muscle stiffness, leading to a faster transition from the braking to propulsive phase of ground contact.[50,51] Dalleau et al.[52] highlighted the importance of neuromuscular factors by demonstrating that running economy was related to the stiffness of the propulsive leg, with greater stiffness eliciting the best running economy.[52] Leg stiffness is modulated by neuromuscular activation, and changes in stiffness have been shown to occur as a result of neuromuscular adaptation to training (i.e. learning of more efficient or more skilled patterns of motor recruitment).[53] In support of the association between motor recruitment and leg stiffness, a reduction in EMG pre-activation was shown to be significantly related to a decrease in post-landing leg stiffness following fatiguing exercise.[54] Greater duration of muscle co-activation of bi-articular leg muscles during stance has also been significantly associated with better running economy.[55] Muscle co-activation modulates leg stiffness during running and may alter running economy through utilization of stored elastic energy, which has no additional metabolic cost. Kyrolainen et al.[56] found that as running speed increased so did EMG preactivation and ground reaction forces, along with their rate of force production (figure 2). Preparatory muscle function is an important function of the stretch shortening cycle (SSC). The SSC is a combination of a high velocity eccentric muscle contraction followed immediately with a concentric contraction. SSC muscle function enhances performance during the final phase (concentric action),[57] and the increase in preparatory muscle activity with higher running speeds was suggested to be a mechanism to tolerate higher impact loads, regulate landing stiffness[58] and improve running economy.[56] However, in that study, the increase in EMG activity may also be explained by the associated change in running kinematics with higher running speeds. A more recent study showed that a greater ratio of eccentric to
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200 ms Fig. 2. Muscle activity patterns of five muscles from the slowest speed of 3.25 m/s (thin line; mean of 170 contacts) up to the maximal speed (thick line; mean of 34 contacts). Data are the mean rectified electromyogram (EMG) measurements from a representative subject. The dashed lines indicate the respective EMG curves at the three medium running speeds and the vertical lines indicate the beginning of the contact phase. Note the greater EMG activity prior to contact (i.e. preactivation) with higher running speeds (reproduced from Kyrolainen et al.,[56] with permission).
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concentric vastus lateralis muscle activity was associated with a lower metabolic demand during running (i.e. better running economy).[59] Taken together, the findings from these studies suggest that neuromuscular characteristics may play an important role in running economy, especially in athletes with similar physiological attributes. The timing and amplitude of muscle activity has shown the most consistent association with running economy. Greater muscle activity prior to and in the initial phase of ground contact may enhance running economy by increasing leg stiffness and maximizing exploitation of stored elastic energy. 5. Training, Shoes, In-Shoe Orthoses, Musculoskeletal Injury and Running Economy Trained runners have a superior running economy to lesser trained or untrained runners,[22,23,60] indicating positive adaptations in response to training programmes. Training programmes can potentially improve running economy through physiological, biomechanical and neuromuscular adaptations. Interventions such as altitude training and training in the heat are aimed at improving cardiorespiratory function, and have previously been reviewed in this journal.[3] Resistance training, plyometrics, stretching and multidiscipline training are training interventions that feasibly have the potential to alter running economy through neuromuscular adaptations. Passive physical interventions such as use of shoes and in-shoe orthoses may also have the potential to elicit similar effects on neuromuscular control and running economy. Musculoskeletal pain and injury can result in a loss of training time and impaired neuromuscular control,[61-64] with potential consequential alterations in running economy. In order to evaluate the effect of injury and training interventions on running economy it is first useful to understand the typical intraindividual variation in this measure. Well controlled studies using moderate to highly trained subjects report intraindividual variations in running economy of between 1.5% and 5%.[65-71] Further to this, Saunders et al.[70] ª 2009 Adis Data Information BV. All rights reserved.
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have recommended that alterations in running economy in highly trained distance runners must exceed 2.4% to be confident a practically worthwhile change has occurred. 5.1 Resistance Training
It is well documented that initial performance gains following resistance training are a result of neuromuscular adaptations rather than withinmuscle adaptations (i.e. hypertrophy).[72,73] These adaptations include increased motor unit recruitment and motor unit synchronization.[72-74] Resistance training may improve running economy through improved leg muscle coordination and co-activation and decreasing stance phase contact times, thereby allowing a faster transition from the braking to the propulsive phase through elastic recoil.[26,50,56,72] For resistance training to improve running economy, a positive ‘transfer of learning’ would need to occur. Transfer occurs when the training for one task affects the performance or learning of a subsequent task. As a general principle, a positive transfer would require that a specific pattern of muscle recruitment associated with optimal performance of a resistance training task enhances running economy if it was expressed during running.[75] EMG analysis may allow for the identification of the transfer of learning from resistance or plyometric training to running. In a group of . moderately trained female distance runners (VO2max = 51 mL/kg/min), 10 weeks of traditional weight training combined with endurance training significantly improved . running economy (4%) without any changes in VO2max.[24] In further support of this training modality, two further studies have reported a 7%[76] and 5%[77] improvement in running economy with heavy resistance training (table I). Improvements in maximal strength were reported in all experimental groups, indicating positive neuromuscular adaptations occurred. However, resistance training was performed in addition to normal endurance training volumes, therefore the improvements in running economy may be related to the increased volume of training rather than the resistance training itself. Støren et al.[77] Sports Med 2009; 39 (11)
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Table I. Comparison of the effect of resistance and plyometric training programmes on running economy Study (year)
Subjects
Volume
Frequency and duration
Control
Results strength/force (%)
RE (%)
Johnston et al.[24] (1997)
12 moderately trained runners
2–3 sets of 6–20 RM in addition to endurance training
3 d/wk for 10 wk
Endurance running
› 24.4–33.8
› 4
Millet et al.[76] (2002)
15 highly trained triathletes
3–5 sets of 3–5 RM in addition to endurance training
2 d/wk for 14 wk
Endurance training (swim, cycle, run)
› 17–25
› 5.6–7
Støren et al.[77] (2008)
17 moderately trained runners
4 sets of 4 RM in addition to endurance training
8 wk
Endurance running
› 33.2
› 5
Paavolainen et al.[26] (1999)
22 moderately trained crosscountry runners
15–90 min/session
9 wk
Endurance running and circuit training
› 24.4–33.8
› 8.1
Turner et al.[78] (2003)
18 recreational distance runners
1 set of 5–25 reps in addition to endurance training
3 d/wk for 6 wk
Endurance running
2
› 2–3
Spurrs et al.[79] (2003)
17 moderately trained runners
2–3 sets of 8–15 reps in addition to endurance training
2–3 d/wk for 6 wk
Endurance running
› 11.4–13.6
› 4.1–6.7
Saunders et al.[80] (2006)
15 highly trained runners
30 min/session in addition to endurance training
3 d/wk for 9 wk
Endurance running
2
› 4
highly trained = national/international level and maximal oxygen consumption >65 mL/min/kg; moderately trained = weekly running volume >30 km/wk; RE = run economy; recreational = weekly running volume <30 km/wk; reps = repetitions; RM = repetition maximum; › indicates increase; 2 indicates no change.
suggested the main training response from the heavy resistance training was a change in muscle recruitment patterns, yet no direct measurement of muscle recruitment (i.e. EMG) was provided to support this notion. 5.2 Plyometric Training
Explosive resistance training or plyometrics is a specific form of strength training that aims to enhance the ability of muscles to generate power through the SSC by use of explosive activities such as jumping, hopping and bounding.[78] The SSC utilizes the ability of soft tissues to store and return elastic energy, thus reducing energy expenditure.[81-83] It has been speculated that stiffness of the musculotendinous system may determine the body’s ability to use such energy,[84] and that plyometric training has the potential to increase musculotendinous stiffness.[79] Paavolainen ª 2009 Adis Data Information BV. All rights reserved.
et al.[26] examined the effects of substituting 32% of endurance training hours with explosive strength training over 9 weeks on selected neuromuscular characteristics and performance measures in moderately trained runners. Velocity of a maximal 20 m sprint, distance of a series of five continual forward jumps and stance phase contact times during constant velocity running were used as indirect measures of neuromuscular characteristics. These variables are thought to represent the ability of the neuromuscular system to repeatedly produce rapid force during intense exercise, and the capability to store and utilize elastic energy.[26,49,50] A significant improvement in 5 km run performance (3.1%), running economy (8.1%), five-jump distance (4.6%), and velocity over a 20 m sprint (3.4%) was found, along with a concurrent decrease in stance phase contact times.[26] The authors suggested that the improved performance was a result of enhanced Sports Med 2009; 39 (11)
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neuromuscular characteristics that were transferred into improved muscle power and running economy. Three further studies have provided support that simultaneous plyometric and endurance training improves running economy in moderately and highly trained athletes[78-80] (table I). Proposed explanations for the improvement include increased lower body musculotendinous stiffness, and enhanced muscle power development and elastic energy return. Turner et al.,[78] however, reported no change in four indirect measures of the ability of the muscles to store and return elastic energy following plyometric training, despite an improved running economy. Countermovement jumps and static jumps on an inclined sled were used as measures of elastic energy return as opposed to the running-specific measures described by Paavolainen et al.[26] The mechanics of jumping on a sled are different to the mechanics of running at speed and it is likely that the measures used were insufficient to detect any change in elastic energy return during running. A direct method to quantify elastic energy utilization has yet to be developed, yet there is a consensus that this phenomenon contributes to economy of movement.[27,82,83,85] It has been proposed that more efficient motor recruitment patterns as a result of training, whether at the neural or muscular level, may decrease the oxygen cost at a given running velocity.[24] If the rate of force development and peak force is enhanced, a longer recovery period between muscle contractions is possible, leading to improved muscle blood perfusion and thereby improving economy.[86,87] In support of this, a recent investigation found 8 weeks of concurrent endurance and explosive strength training significantly improved leg extensor rapid force production and activation, along with a significant improvement in work economy (7% – 6%) during a constant velocity double-poling action in moderately trained cross-county skiing athletes.[88] Despite the different mode of testing, the weightbearing nature of the double-poling test could indicate these results are applicable to running economy. While it is difficult to determine the exact mechanisms responsible for the improved ª 2009 Adis Data Information BV. All rights reserved.
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economy following resistance training, these findings add some weight to the model of endurance performance described by Paavolainen et al.[49,50] whereby endurance performance is influenced by neuromuscular characteristics along with aerobic power, and that endurance performance may be improved through enhanced neuromuscular function. However, this premise is based on indirect measures of neuromuscular function and elastic energy return such as contact times and vertical jump height. Enhancements in strength and power development during isolated tasks may reflect neuromuscular adaptations but this has not been confirmed by more direct measurements of muscle recruitment, such as EMG. Thus, it is not possible to infer that these adaptations translate into more efficient muscle recruitment patterns during running, or that they are responsible for the enhanced running economy following resistance and plyometric training. 5.3 Stretching
There are two diametrically opposed hypotheses for the effect of stretching on energy requirements. It has been suggested that if stretching decreases the visco-elastic properties of muscle and tendon,[89,90] then less energy may be required to move the limb. Alternatively, the decreased compliance may reduce the storage of elastic energy, increasing energy requirements.[91,92] Stretching has indeed been shown to alter the compliance of human tendons in vivo.[93,94] There is also evidence to suggest that stretching induces acute neuromuscular effects. Numerous studies have demonstrated a decrease in a muscle’s ability to produce force immediately after passive stretching,[95-99] along with decreases in EMG amplitude during isometric[95,98,99] and concentric[97] muscle actions. In contrast, an acute bout of assisted and unassisted static quadriceps stretches did not alter peak torque or EMG amplitude of the quadriceps muscle group during an eccentric muscle action.[100] A further study found that four sets of three different dynamic stretches did not alter peak torque, but increased EMG amplitude of the biceps femoris muscle during maximal Sports Med 2009; 39 (11)
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isometric contractions at 81 and 101 knee flexion.[101] Methodological differences in the mode (i.e. static vs dynamic) and duration of stretching may explain the inconsistent findings between the various studies. It is likely the observed neuromuscular effects are specific to the mode of stretching and the subsequent muscle activity (i.e. isometric vs isokinetic). Further research is required to understand the differential effects of various modes of stretching on acute neuromuscular control during exercise. Early studies examined the relationship between flexibility and running economy. Gleim et al.[102] found that untrained subjects with the least flexibility on a number of active and passive measures about the trunk and lower extremity were more economical during walking and running. Similarly, Craib et al.[103] reported reduced active hip external rotation and passive ankle dorsiflexion range of motion was associated with better running economy in moderately trained distance runners. Both investigators attributed the superior economy to increased storage and return of elastic energy and a reduction in energyexpensive stabilizing muscle activity, though they did not provide evidence for these assumptions. Most importantly, both these investigations were correlative studies and neither study provides evidence that altering flexibility through various interventions will result in an enhanced running economy. To date, three studies have examined the effects of stretching programmes on running economy in recreationally active athletes. Two of these found stretching over a period of 3 weeks[104] or 10 weeks[105] had no impact on running economy despite significantly improving flexibility. Conversely, Godges et al.[106] found that an acute bout of end-range stretching resulted in an immediate, significant reduction (4–7%) in oxygen consumption at. workloads equivalent to 40%, 60% and 80% VO2max. The discrepancies reported may relate to different methodological procedures. The study by Godges et al.[106] was limited to seven subjects with tight hip flexor or extensor muscles. In addition, running economy was only measured immediately post-stretching and follow-up meaª 2009 Adis Data Information BV. All rights reserved.
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sures were not performed. In their subsequent investigation with a larger population over a 3-week period, Godges et al.[104] found no effect of stretching on running economy. Furthermore, the technique employed in their original study involved passive stretching at end of range with restraints and suspended weights, a technique that neither recreational nor elite athletes are likely to employ. A recent systematic review concluded that an acute bout of stretching preexercise may improve running economy, but regular stretching over time has no effect on economy.[91] These findings do not suggest stretching should be discounted as a training modality, because stretching exercises are commonly prescribed to running athletes for the maintenance and promotion of range of motion,[107] especially after injury. 5.4 Multidiscipline Sports and Training
Impairments in overground[108,109] and treadmill[110-113] running economy have frequently been observed in moderately trained athletes following cycling (i.e. when running ‘offthe-bike’) compared with an isolated control run. Further investigation in the same area found that running economy after maximal cycling is not increased compared with a control run in elite level triathletes.[114] The increase in oxygen consumption during running after cycling varies from 1.6% to 11.6% and is thought to be a reflection of ability level, with more experienced athletes displaying less impairment in running economy.[115] Proposed explanations for the increased oxygen consumption during running after cycling include glycogen depletion,[108,109,113,115] ventilatory muscle fatigue,[113] dehydration[108,109,112] and leg muscle fatigue.[111,112] Hausswirth et al.[112] attributed the increased metabolic cost of running at the end of a triathlon to biomechanical variables such as stride length and trunk gradient. In contrast, several others have reported no change in running kinematics following cycling.[109,113,116,117] A recent review suggested that if the consequence of previous exercise is to reduce subsequent running economy, Sports Med 2009; 39 (11)
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then it is more likely to be through physiological rather than biomechanical factors.[3] While this seems the most logical rationale, it fails to consider the influence of the neuromuscular system, and the possibility that movement patterns may be preserved but muscle activity altered.[116] The transition from bike to run involves a switch from a predominantly concentric type of muscle activity to a combined eccentric-concentric action.[114,115] This requires rapid neuromuscular adjustments to be made in order to effectively utilize stored elastic energy. The quantity of elastic energy stored and re-used is influenced by leg stiffness, and lower limb stiffness has been shown to be correlated to running economy.[52] Only neuromuscular activation is able to modulate leg stiffness.[52] Initial EMG studies of the cycle-run transition report small and sometimes only transient changes in muscle activation that may be attributed to alterations in kinematics, running speed or fatigue.[118,119] More recently, Chapman et al.[116] used a new paradigm to discriminate the influence of fatigue and altered running speed on leg kinematics and muscle activation. They found that a select proportion of highly trained triathletes (30%) exhibited muscle activity in the postcycling run leg that more closely resembled that used during cycling rather than the muscle activity used during the control pre-bike run. The altered muscle activity was evident as soon as running commenced and persisted for the duration of the 30-minute run off-the-bike. Moreover, despite the altered muscle activity, no changes in running kinematics were observed. As only the tibialis anterior muscle was investigated, further work is required to determine if similar alterations in activation exist in the other leg and thigh muscles. Interference with execution of optimal patterns of muscle recruitment when switching from cycling to running may alter muscle stiffness regulation and hinder the athlete’s ability to effectively utilize elastic energy during running.[120] Recovery of elastic energy is known to reduce energy expenditure.[81-83] Certainly, physiological stress appears to be the primary reason for the increased cost of running after ª 2009 Adis Data Information BV. All rights reserved.
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cycling.[3] However, it is probable that alterations in patterns of muscle recruitment after cycling may also be a contributing factor to the increased metabolic cost of running in some athletes.[120] Two recent studies have indeed shown that alterations in run performance after variable cycling compared with steady-state cycling may occur in the absence of physiological changes. Run time to exhaustion was found to be significantly greater following a variable cycling intensity (–20% of 90% lactate threshold) compared with a constant intensity (90% of lactate threshold).[121] Conversely, a 5 km run time trial was significantly better (4.4%) following a 20 km constant intensity cycle compared with a variable intensity cycle.[122] Although these are conflicting findings, both protocols that reported improvements in run performance completed the final stages of the cycle leg as a low intensity segment. Hence it appears that completing the final stages of the cycling phase at a high intensity is detrimental to subsequent run performance. Interestingly, despite considerable within-subject changes .in run performance, no differences in average VO2, ventilation, heart rate or rating of perceived exertion were detected between the controlled or variable conditions during both the cycle and the subsequent run leg. While cycling at a lower intensity in the final portion of the cycle leg may allow for a greater metabolic recovery,[121] it is also possible that alterations in neuromuscular control may be responsible for the difference in run performance. A recent study with a small sample size of triathletes demonstrated a similar magnitude of neuromuscular fatigue following constant-versus variable-intensity cycling.[123] The authors concluded that in the field of triathlon, variations in run performance cannot be attributed to different levels of neuromuscular fatigue following constant-versus-variable cycling. Perhaps then it is the change in lower limb muscle coordination during running after cycling,[116] independent of neuromuscular fatigue, that contributes to the difference in run performance. Further work examining lower limb muscle coordination during running after cycling is required to explore this supposition. Sports Med 2009; 39 (11)
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5.5 Shoes and In-Shoe Orthoses
With every ground contact during running, energy is transferred between the athlete and supporting surface. The interaction between the athlete and surface is coupled by the shoe and insert or orthoses. Theoretically, performance can be influenced by the shoe and shoe insert or orthosis through its mass, its potential to change movement patterns and alter muscle activity, and by minimizing the energy that is lost by the athlete.[124,125] In a landmark review paper, Nigg et al.[126] proposed a new concept for use of shoes, inserts and orthoses in sport: (i) the skeleton has a preferred path for a given movement task; (ii) if an intervention (shoe, insert, orthoses) supports the preferred path, muscle activity can be reduced; (iii) an optimal shoe, insert or orthosis feels comfortable because it reduces muscle activity and the resulting fatigue; and (iv) performance should increase with an optimal shoe, insert or orthosis since muscle activity is minimized and thus energy expenditure is reduced. Early work has indeed shown that orthoses elicit shortterm effects on lower limb muscle activity during walking and running.[14-16,127] The demonstrated changes in muscle activity have shown high intersubject variability,[14-16,127] indicating the individual nature of neuromuscular responses to orthoses. Shoe mass is an example of how manipulation of footwear can affect energy requirements. When different types of footwear were compared it was found that wearing heavier models significantly elevated oxygen consumption in trained runners without concomitant changes in stride length.[128] When identical shoe types are modified only with respect to their mass, oxygen consumption is significantly greater with the heavier shoes during walking and running.[129,130] Modifying shoe material properties can also influence economy of locomotion. The use of airsoled shoes elicited a superior running economy compared with regular ethylene vinyl acetate (EVA), midsoles in trained distance runners.[131] Nigg et al.[17] attempted to verify their concept of an optimal shoe by examining the effect of shoe materials on lower limb EMG and running ª 2009 Adis Data Information BV. All rights reserved.
economy. Oxygen consumption and EMG activity during running were compared between a medium hardness elastic shoe and a softer viscous shoe. They found that running economy responses to the shoes were highly individual, i.e. some athletes consumed less oxygen for the elastic shoe condition while others consumed less for the viscous shoe condition. The EMG data also showed muscle- and subject-specific responses to the shoes. An interesting finding was that all runners who consumed more oxygen in the viscous shoe showed higher vastus medialis pre-activation in that shoe; similarly, the runners who consumed more oxygen in the elastic shoe demonstrated higher vastus medialis preactivation in that shoe. This seems counterintuitive, given that EMG pre-activation is thought to modulate leg stiffness and enhance elastic energy return, which has been shown to be metabolically more efficient.[52,54,58] However, all changes in running economy were £2.0% and the running economy and EMG measurements were not made simultaneously, so it is difficult to draw any solid conclusions from this study other than that changes in running economy and muscle activity with different shoes are subject specific. Surprisingly, the effect of orthoses on running economy has received very little attention, despite being commonly prescribed to running athletes. Furthermore, no studies have simultaneously measured running economy and EMG activity of the leg muscles. The studies that have investigated the effect of orthoses on muscle activity have shown high intersubject variability in the EMG responses to orthoses.[14-16,127] Whether the changes in muscle activity associated with orthosis prescription correspond to an alteration in running economy has yet to be determined. Three studies have investigated the direct effect of orthoses on running economy. Two of the studies found that running economy was not altered with orthosis use in recreational[132] and moderately trained runners.[133] In contrast, the other study found that both flexible and semi-rigid orthoses significantly increased oxygen consumption in runners who had a history of runningrelated injuries.[134] This is the only investigation that included a symptomatic population, to whom Sports Med 2009; 39 (11)
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orthoses are commonly prescribed as a tool for symptomatic relief. However, no detail was given as to the type or site of injury, the mechanism of injury or current state of symptoms. Furthermore, analysis of data reveals the increase in oxygen consumption when running in rigid and flexible orthoses was only 2.0% and 1.7%, respectively, which is within intraindividual variation[66,68,70,71] and may not be a practically worthwhile change.[70] Taken collectively, it is likely that orthoses elicit subject-specific short-term effects on neuromuscular control during running, but there is insufficient evidence to date to support the concept proposed by Nigg et al.[126] that an optimal orthosis reduces muscle activity, minimizes energy expenditure and improves run performance. 5.6 Musculoskeletal Injury
Musculoskeletal overuse injury is arguably the most significant adverse effect of participation in endurance exercise and constitutes a major impediment to participation in physical activity. The knee and shin are the most common sites of injury in endurance athletes,[135-137] and the majority (50–75%) of all running injuries are reported to be overuse in nature.[135,137,138] Alterations in neuromuscular control – including muscle imbalances, altered muscle timing, muscle fatigue and muscle weakness – have been associated with musculoskeletal injury and pain in numerous independent reports.[61-64,139,140] Unfortunately, much of the research has been retrospective, and our understanding of overuse injury causation is limited. Moreover, knowledge of the direct effect of musculoskeletal injury and neuromuscular impairments on running economy is limited. While it is presumed that injury and subsequent pain and functional impairments hinder performance through loss of training hours and competition, many athletes may continue to participate with sequelae of injury (e.g. pain, swelling, proprioceptive deficits). Furthermore, alterations in muscle recruitment that occur with injury and ensuing pain have been exhibited up to 66 months post-injury.[141,142] It is possible that without ª 2009 Adis Data Information BV. All rights reserved.
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targeted interventions, the specific neuromuscular impairments that occur following injury[61-64,139] may persist well after the athlete has returned to training and competition. The literature to date fails to provide any insight into the possible effect that any injury in an endurance athlete may have on running economy. Therefore, to explore this area we present some available evidence from a wider model. There is some evidence that walking gait economy is decreased in those with knee joint osteoarthritis – a progressive form of musculoskeletal injury and pain.[143-146] Anterior cruciatedeficient patients have also demonstrated an 8% decrement in running economy compared with healthy controls,[147] and anterior cruciate ligament deficiency has been associated with increased hamstring muscle activity during running and cutting manoeuvres.[141,142] Whilst these injuries and the activities used to test economy (e.g. walking economy) only partially resemble the routine laboratory test intensity, and injuries sustained by endurance athletes, they provide a snapshot of how musculoskeletal injury may affect running economy in endurance athletes. Exercise-induced muscle damage (EIMD) is a further paradigm with which to investigate the effect of musculoskeletal pain and injury on performance. EIMD occurs after performing unaccustomed exercise or exercise of increased intensity or duration; it results in muscle stiffness, swelling, impairment of muscle function and delayed-onset muscle soreness.[148] For a comprehensive review of the alterations in neuromuscular function that follow EIMD the reader is directed to a recent review in this journal.[148] In short, documented outcomes of EIMD include reflex inhibition of muscle activity, decreased strength and power-generating ability, and a decrease in the force to electromyographic (iEMG) activity ratio.[148] In relation to performance, EIMD from a bout of isokinetic resistance exercises[149,150] and downhill running[151] did not alter running economy in recreationally active subjects.[149-151] In contrast, a 3.2% reduction in running economy and stride length was found 48 hours after performing a single bout of downhill running (resulting in considerable Sports Med 2009; 39 (11)
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muscle soreness) in moderately trained triathletes and distance runners.[152] Perhaps changes in running economy and kinematics due to EIMD are less sensitive in untrained subjects because of their less refined movement and muscle activity patterns. A similar protocol using trained and untrained subjects may provide further support for this idea. 6. Conclusions The purposes of this review were to: (i) examine the adaptations of lower limb muscle recruitment (i.e. neuromuscular adaptations) to different modes of training (i.e. running, cycling, multidiscipline); (ii) examine what aspects of neuromuscular control are associated with running economy; and (iii) examine whether neuromuscular adaptations induced by training, passive interventions and injury can be coupled with changes in running economy. It had previously been assumed that superior cycling and running performance was evidence for greater neuromuscular adaptation in trained athletes. Recent scientific knowledge supports this belief, with evidence that ongoing single-discipline training leads to more refined patterning of leg muscle recruitment. This is thought to be a positive neuromuscular adaptation to endurance training, which may reduce metabolic demand and enhance performance. A difference in leg muscle recruitment during cycling has been demonstrated between multi- and single-discipline athletes. This highlights a difference in neuromuscular adaptation to single- and multidiscipline training. However, it is uncertain whether these specific neuromuscular adaptations are beneficial or detrimental to sport-specific endurance performance. Available evidence suggests that in athletes with similar physiological attributes, neuromuscular characteristics play an important role in endurance running performance. The consistent finding from studies of improvements in running economy following strength and plyometric training appears related to neuromuscular adaptations (e.g. improvements in strength, force production). Whether these adaptations alter ª 2009 Adis Data Information BV. All rights reserved.
leg muscle recruitment during running remains unknown. The adverse effect of cycling on subsequent running economy in triathletes is most likely due to physiological stress, although alterations in muscle recruitment patterns should not be discounted as a potential contributor. There is insufficient evidence for the alteration of running economy through stretching, shoe material modifications, in-shoe orthoses and musculoskeletal injury in endurance athletes. Exerciseinduced muscle damage reduces running economy in moderately trained athletes through alterations in kinematics, which may be associated with changes in neuromuscular control. 7. Future Directions Future sport performance research needs to consider the role of the neuromuscular system in endurance activities. The available evidence suggests that adaptations of leg muscle recruitment do occur in response to ongoing endurance training. Research is yet to establish the optimal duration and intensity of training to promote these adaptations and whether further improvements can be achieved through training interventions once at the elite level. These questions warrant future investigation. Further knowledge of the relationship between leg muscle recruitment and running economy may divulge information about optimal patterns of muscle recruitment for economical running. Measurement of leg muscle recruitment pre- and post-training interventions would help explain whether running economy is altered through adaptations in leg muscle recruitment. In recent times, investigators have directed their attention to the neuromuscular effects of shoes and in-shoe orthoses. The available evidence suggests that changes in leg muscle activity with various shoe materials and orthoses may be specific to an individual, and thus an optimal shoe or orthosis for performance would also require individual consideration. However, the relationship between shoes, in-shoe orthoses, muscle activity and performance remains unclear and requires further investigation. Sports Med 2009; 39 (11)
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More knowledge of the effect that cycling has on subsequent leg muscle activation during running in triathletes is required, along with its relationship to running economy. Similarly, knowledge of how various cycling intensities affect leg muscle activation and subsequent run performance may help to structure triathlete training and race day performance. As evidenced in the literature, cycling affects leg muscle recruitment during running in some athletes, but not others. Therefore, researchers should consider the impact of various cycle intensities on the individual in addition to the group. It is likely that a strategy effective for one athlete may not be effective for another. Running and triathlon training are associated with high occurrences of musculoskeletal injury. There is preliminary evidence that ongoing multidiscipline training may interfere with neuromuscular adaptation. Numerous reports have associated alterations in neuromuscular control with musculoskeletal injury. However, the effect of any training-induced interference in neuromuscular adaptation on injury manifestation is yet to be determined. Furthermore, the effect of the sequelae of injury (e.g. pain, swelling, muscle weakness) on running economy remains unknown. Future work aimed at investigating the effect of training structure on muscle activity, musculoskeletal injury and running economy will improve our understanding of the relationship between training, musculoskeletal injury, neuromuscular control and performance. Acknowledgements Jason Bonacci and Andrew Chapman are supported by the Australian Research Council. No sources of funding were used to assist in the preparation of this review. The authors have no conflicts of interest that are directly relevant to the content of this review.
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133. Clement D, Taunton J, Wiley JP, et al. The effect of corrective orthotic devices on oxygen uptake during running. In: Bachl N, Prokop L, Suckert, R, editors. Current topics in sports medicine. Proceedings of the World Congress of Sports Medicine; 1982; Vienna: 648-55 134. Hayes J, Smith L, Santopietro F. The effects of orthotics on the aerobic demands of running [abstract]. Med Sci Sports Exerc 1983; 15: 169 135. Egermann M, Brocai D, Lill CA, et al. Analysis of injuries in long-distance triathletes. Int J Sports Med 2003; 271-6 136. Rauh MJ, Margherita AJ, Rice SG, et al. High school cross country running injuries: a longitudinal study. Clin J Sport Med 2000; 10: 110-6 137. Vanmechelen W. Running injuries: a review of the epidemiologic literature. Sports Med 1992; 14: 320-35 138. Hoeberigs JH. Factors related to the incidence of running injuries. Sports Med 1992; 13: 408-22 139. Ireland ML, Willson JD, Ballantyne BT, et al. Hip strength in females with and without patellofemoral pain. J Orthop Sports Phys Ther 2003; 33: 671-6 140. Madeley LT, Munteanu SE, Bonanno DR. Endurance of the ankle joint plantar flexor muscles in athletes with medial tibial stress syndrome: a case-control study. J Sci Med Sport 2007; 10: 356-62 141. Branch TP, Hunter R, Donath M. Dynamic EMG analysis of anterior cruciate deficient legs with and without bracing during cutting. Am J Sports Med 1989; 17: 35-41 142. Swanik CB, Lephart SM, Giraldo JL, et al. Reactive muscle firing of anterior cruciate ligament-injured females during functional activities. J Athl Train 1999; 34: 121-9 143. Gussoni M, Margonato V, Ventura R, et al. Energy cost of walking with hip joint impairment. Phys Ther 1990; 70: 295-301 144. McBeath AA, Bahrke MS, Balke B. Walking efficiency before and after total hip replacement as determined
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Correspondence: Prof. Bill Vicenzino, Division of Physiotherapy, School of Health and Rehabilitation Sciences, University of Queensland, Brisbane, QLD 4072, Australia. E-mail:
[email protected]
Sports Med 2009; 39 (11)
Sports Med 2009; 39 (11): 923-935 0112-1642/09/0011-0923/$49.95/0
REVIEW ARTICLE
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Exercise Preconditioning of the Myocardium Andreas N. Kavazis Department of Applied Physiology and Kinesiology, University of Florida, Gainesville, Florida, USA
Contents Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Characteristics of Endurance Exercise Training to Obtain and Maintain Cardioprotection . . . . . . . . 1.1 Long- and Short-Term Exercise Provide Cardioprotection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2 Exercise-Induced Cardioprotection: Role of Exercise Intensity. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.3 Time-Course of Loss of Cardioprotection after the Cessation of Exercise. . . . . . . . . . . . . . . . . . . . 2. Adaptations to the Myocardium following Exercise Training . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1 Extrinsic and Intrinsic Adaptations to Exercise Training . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2 Increased Antioxidant Capacity Provides Cardioprotection. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3 Exercise Training and Cardiac Mitochondria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Summary and Future Directions in the Area of Exercise-Induced Cardioprotection . . . . . . . . . . . . . .
Abstract
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Diseases of the heart (e.g. myocardial ischaemia reperfusion injury) remain the major cause of death in the industrialized world. Therefore, developing a pragmatic countermeasure to reduce myocardial ischaemia reperfusion injury is vital. In this regard, a plethora of evidence indicates that regular exercise can protect the heart during an ischaemia reperfusion insult (i.e. cardioprotection). This review summarizes studies indicating that both short-term (i.e. 1–5 days) and long-term (i.e. weeks to months) endurance exercise provides cardioprotection. Data are presented showing that exercise duration and exercise intensity are both important factors in achieving a cardioprotective phenotype. Importantly, it appears that the exercise duration of a single exercise session should last for 60 minutes and should be performed at about 75% maximum oxygen consumption in order to achieve exercise-induced cardioprotection. Furthermore, data are presented showing that exercise-induced cardioprotection against myocardial stunning can persist for at least 9 days after the cessation of exercise training, but is lost 18 days after exercise. This review also summarizes the exercise-induced adaptations that occur to the myocardium. In particular, extrinsic changes observed in human and animal models include neural, hormonal, humoral, vascular and reduced body fat. Other anatomical and biochemical/molecular changes that have been studied as putative mechanisms in exercise-induced cardioprotection include alterations in anatomic coronary arteries, induction of myocardial heat shock proteins, increased myocardial cyclooxygenase-2 activity, elevated endoplasmic reticulum stress proteins, nitric oxide production, improved function of sarcolemmal and/or mitochondrial adenosine
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triphosphate (ATP)-sensitive potassium channels and increased myocardial antioxidant capacity. However, the most compelling evidence for exerciseinduced cardioprotection is the fact that exercise training upregulates key antioxidant enzymes that have been shown to promote cardioprotection. Moreover, data are presented showing that exercise training induces cardiac mitochondrial changes that result in reduced oxidant production. In addition, recently our laboratory has shown that exercise training evokes changes in mitochondrial phenotype that are protective against apoptotic stimuli. Specifically, data are presented showing that several mitochondrial proteins are altered following repeated bouts of endurance exercise and several of these differentially expressed proteins are potential important cardioprotective mediators. Finally, in hopes of stimulating debate and future research, this review concludes with a discussion of unanswered questions related to exercise-induced cardioprotection.
Cardiovascular diseases (e.g. ischaemia reperfusion injury) are the major cause of death in the industrialized world. Over the years, investigators have studied many approaches to protect the heart against ischaemia reperfusion injury (cardioprotection). Specifically, cardioprotection (preconditioning) was originally described as an immediate adaptation of the heart to brief sublethal ischaemia.[1] It is now well recognized that preconditioning consists of two chronologically and pathophysiologically distinct phases: an early phase and a late phase of protection.[2-5] The early phase occurs immediately after a stimulus and induces robust protection, but it is short-lived (i.e. it lasts for only 2–3 hours).[4] However, the late phase of preconditioning develops 12–24 hours after the initial stimulus and can last several days.[5] In this regard, several procedures have been identified and are known to stimulate cardioprotection. These approaches include exercise, ischaemic preconditioning, heat stress, oxidative stress, stretch and certain pharmacological interventions.[6] However, endurance exercise is the only practical and sustainable countermeasure capable of providing cardioprotection.[7-29] Importantly, several studies indicate that endurance exercise training improves myocardial tolerance to ischaemia reperfusion injury (e.g. heart attack) in both young and old animals of both sexes (i.e. males and females).[7,8,10-15,17-25,27,29-34] Specifically, studies reveal that exercise training protects the heart against arrhythmias, oxidative injury, mitochonª 2009 Adis Data Information BV. All rights reserved.
drial damage and cell death.[10,15] Interestingly, several investigators have shown that shortterm exercise training (i.e. 3–5 consecutive days) provides the same cardioprotection as that observed following long-term training (i.e. 10 weeks).[7,11,13,15,17,18,23,24,35,36] Remarkably, the mediators responsible for exercise-induced cardioprotection have not yet been fully explained. Importantly, at least eight primary mechanisms could contribute to exerciseinduced cardioprotection. However, a plethora of data show that exercise-induced upregulation of antioxidant enzymes plays a critical role in protecting the myocardium against ischaemia reperfusion injury.[13-15,19,23,29,37] Therefore, the goal of this review is to provide an up-to-date synopsis describing the effects of exercise on the myocardium with emphasis on antioxidant enzymes. In writing this review, two search engines (i.e. PubMed and ISI Web of Knowledge) were used to find papers discussing the topic of exercise-induced cardioprotection. The search limits included the dates of 1960 to the present, and several keywords including: ‘antioxidants’, ‘cardiac muscle’, ‘cardioprotection’, ‘coronary arteries’, ‘cyclo-oxygenase-2’, ‘endoplasmic reticulum stress proteins’, ‘exercise’, ‘heat shock proteins’, ‘ischaemia reperfusion injury’, ‘mitochondria’, ‘adenosine triphosphate (ATP)-sensitive potassium channels’, ‘myocardium’, ‘nitric oxide’, ‘oxidants’ and ‘preconditioning’. This review is written so that a critical discussion of several key papers in this area is Sports Med 2009; 39 (11)
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provided. In addition, the final segment of this paper identifies research gaps in our knowledge of exercise-induced cardioprotection in hopes of stimulating future work in this field. 1. Characteristics of Endurance Exercise Training to Obtain and Maintain Cardioprotection 1.1 Long- and Short-Term Exercise Provide Cardioprotection
It is well documented that endurance exercise training improves myocardial tolerance to ischaemia reperfusion injury. Several of the pioneering studies showing that both short- and long-term endurance exercise training is cardioprotective are summarized below. In this regard, Bowles and Starnes[8] published one of the earliest animal studies describing how exercise training results in myocardial adaptations. Specifically, the authors used the in vitro working heart model and reported that hearts isolated from exercise-trained animals (5 days per week for 11–16 weeks) had a greater recovery of cardiac function after global ischaemia compared with hearts obtained from sedentary animals.[8] In the late 1990s, Powers and collaborators[23] completed an in vivo ischaemia reperfusion animal study showing that exercise training provides cardioprotection. In this study, animals were trained 4 days per week for 10 weeks on a motor-driven treadmill.[23] Following training, animals were subjected to an in vivo ischaemia reperfusion protocol and the results indicated that long-term endurance exercise training results in improved myocardial performance during both ischaemia and reperfusion.[23] Interestingly, studies performed in the 1990s suggest that as few as 3–5 consecutive days of endurance exercise are sufficient to promote a cardioprotective phenotype. One of these studies compared animals from three groups: (i) control, (ii) three consecutive days of treadmill exercise for 60 minutes per day, and (iii) five consecutive days of treadmill exercise for 60 minutes per day.[11] Hearts from the three groups were subjected to in an in vivo ischaemia reperfusion protocol. The results revealed that compared with untrained controls, exercised animals from ª 2009 Adis Data Information BV. All rights reserved.
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both groups maintained higher left ventricular developed pressure, maximum rate of left ventricular pressure development and maximum rate of left ventricular pressure decline at all measurement periods during both ischaemia and reperfusion.[11] Moreover, other investigators have also reported that short-term endurance exercise training can provide myocardial protection during ischaemia and reperfusion.[27,38] In summary, several well designed and implemented studies have repeatedly shown that both short-term (i.e. 3–5 days) and long-term (i.e. weeks to months) endurance exercise training decreases ischaemia reperfusion-induced cardiac injury. 1.2 Exercise-Induced Cardioprotection: Role of Exercise Intensity
Low-intensity exercise programmes are known to be effective in reducing the risk factors of cardiovascular disease in humans and other animals. However, until recently, it was not clear whether low-intensity exercise programmes were sufficient to improve intrinsic myocardial tolerance to ischaemia reperfusion injury. To address this issue, Starnes and collaborators[26] investigated the effect of exercise intensity in providing cardioprotection in an ischaemic attack. Starnes et al.[26] exercised rats on a treadmill at an intensity of 55–60% maximum oxygen consumption, 40 minutes per day, 5 days per week for 16 weeks. Hearts were then isolated from exercised and sedentary rats and were exposed to global ischaemia followed by reperfusion. Surprisingly, the study results indicate that exercise training at 55–60% maximum oxygen consumption is below the threshold intensity necessary to induce intrinsic cardioprotection against ischaemia reperfusion injury.[26] However, at the same time, a similar experiment was performed in Scott Powers’ laboratory at the University of Florida. In the study by Lennon et al.,[18] rats were exercised at a moderate exercise intensity (60 minutes at 55% maximum oxygen consumption) or at a high exercise intensity (60 minutes at 75% maximum oxygen consumption) on the treadmill. Hearts were then isolated from a sedentary control group, moderate-intensity exercise group and high-intensity Sports Med 2009; 39 (11)
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exercise group. Subsequently, hearts were exposed to an in vitro ischaemia reperfusion protocol. The results show that compared with sedentary animals, both moderate- and high-intensity exercised animals maintained a significantly higher percentage of pre-ischaemic cardiac output and cardiac work (cardiac output · systolic blood pressure) during reperfusion. In addition, no differences in the percent recovery of cardiac output and heart work existed between the two exercise groups. Based on these results, the authors concluded that both moderate- and high-intensity exercise training provides equivalent protection against ischaemia reperfusion injury.[18] It is important to draw attention to one main difference between the two aforementioned studies. In the study by Starnes et al.,[26] the exercise duration was 40 minutes. However, Lennon et al.[18] exercised the animals for 60 consecutive minutes. Therefore, it appears that exercise duration and exercise intensity are both important factors in achieving a cardioprotective phenotype. 1.3 Time-Course of Loss of Cardioprotection after the Cessation of Exercise
As already discussed, a plethora of data indicate that endurance exercise is cardioprotective. However, until recently it was unknown how long the heart retains its cardioprotective phenotype after the cessation of exercise. To investigate the loss of cardioprotection following cessation of exercise, Lennon et al.[17] assigned rats into one of five groups: (i) sedentary control, (ii) exercise followed by 1 day of rest, (iii) exercise followed by 3 days of rest, (iv) exercise followed by 9 days of
rest, and (v) exercise followed by 18 days of rest. The authors used an isolated working heart preparation and reported that exercise-induced cardioprotection against myocardial stunning persisted for at least 9 days after the cessation of exercise training. However, exercise-induced cardioprotection was absent 18 days after exercise (table I). The authors also investigated several putative mechanisms for cardioprotection. Specifically, they report that both heat shock protein 72 (HSP72) and catalase were elevated 1 and 3 days after the cessation of exercise, but returned to baseline values 9 days after the cessation of exercise. Therefore, Lennon and collaborators reported that the results indicate that cardioprotection persisted in the absence of elevated myocardial levels of HSP72 and catalase 9 days after exercise.[17] Importantly, the authors concluded that mechanisms other than HSP72 and catalase upregulation are involved in exerciserelated protection against ischaemia reperfusioninduced myocardial stunning. The following section summarizes several putative cardioprotective mechanisms, but focuses on the role of antioxidant enzymes in protecting the myocardium during an ischaemic attack. 2. Adaptations to the Myocardium following Exercise Training 2.1 Extrinsic and Intrinsic Adaptations to Exercise Training
Regular bouts of endurance exercise promote numerous cardiovascular benefits and epidemiological studies show that exercise is associated
Table I. Persistence of cardioprotection, levels of antioxidant enzymes and heat shock protein 72 (HSP72) after the cessation of exercise Variable
1 day after exercise
3 days after exercise
9 days after exercise
Cardioprotection
Present
Present
Present
Absent
2
2
2
2
GPX
18 days after exercise
catalase
›
›
2
2
MnSOD
2
2
2
2
CuZnSOD
2
2
2
2
HSP72
›
›
2
Not reported
CuZnSOD = copper zinc superoxide dismutase; GPX = glutathione peroxidase; MnSOD = manganese superoxide dismutase; › indicates increase; 2 indicates no change.
ª 2009 Adis Data Information BV. All rights reserved.
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with a reduced risk of coronary heart disease and cardiovascular mortality.[36,39] These benefits arise from changes, both intrinsic and extrinsic, to the heart. Extrinsic changes observed in human and animal models include neural, hormonal, humoral, vascular and reduced body fat.[40] Specifically, exercise can modify several cardiovascular risk factors (e.g. hypertension, diabetes mellitus, obesity, lipoprotein metabolism, risk of thrombosis and endothelial dysfunction). Therefore, it is possible that the link between exercise and reduced cardiovascular mortality rates is associated with one or more of these risk factors. For example, studies indicate that exercise prevents the development of hypertension[41,42] and lowers blood pressure.[43] Furthermore, physical activity has beneficial effects on both glucose metabolism and insulin sensitivity.[44] Exercise also induces changes in blood lipid levels (e.g. total cholesterol, low-density lipoproteins and high-density lipoproteins).[45] In addition to improvements in the blood lipid profile, exercise is also associated with improvement of endothelial function, as regular exercise increases the ability of the endothelium to release vasoactive factors,[46,47] which improve the intrinsic control of coronary vascular resistance.[48] However, endurance exercise training promotes several intrinsic adaptations to the myocardium; these adaptations are discussed in the following sections. At present, the molecular mechanisms responsible for exercise-induced cardioprotection are not well established. At least eight primary mechanisms could contribute to the cardioprotective effect of exercise (for a comprehensive review see Powers et al.[36]). In summary, researchers have focused on changes in anatomic coronary arteries, induction of myocardial heat shock proteins, increased myocardial cyclooxygenase-2 activity, elevated endoplasmic reticulum stress proteins, nitric oxide production, improved function of sarcolemmal and/or mitochondrial ATP-sensitive potassium channels and increased myocardial antioxidant capacity. However, published reports indicate that no significant development of collateral coronary arteries occurs during short-term exercise.[49] Furthermore, exercise training does not elevate myocardial levels of ª 2009 Adis Data Information BV. All rights reserved.
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cyclo-oxygenase-2[50] or endoplasmic reticulum stress proteins[51] in the rat heart. In addition, three independent studies conclude that induction of heat shock proteins is not a prerequisite for exercise-induced cardioprotection.[13,27,52] Nitric oxide has been shown to induce cardioprotection. Specifically, nitric oxide appears to play a dual role as a trigger and as a mediator of cardioprotection.[53-56] Although several studies have shown that increased nitric oxide availability is cardioprotective, only two studies have studied the protective contribution of nitric oxide to exercise-induced cardioprotection.[57,58] The results from these two studies are in disagreement. Babai et al.[57] utilized an in vivo ischaemia reperfusion protocol and reported that exercise elevated the inducible nitric oxide synthase activity, which may have contributed to the reduction in the severity of arrhythmias that occurred soon after the onset of ischaemia. However, the exercise-induced cardioprotection was abolished by a nitric oxide inhibitor. Therefore, the authors concluded that exercise-induced cardioprotection is mediated by nitric oxide.[57] However, Taylor at al.[58] used an in vitro working heart preparation model and reported that exercise induced cardioprotection against ischaemia reperfusion injury, even when nitric oxide production was blocked. The authors concluded that elevated nitric oxide production is not required for exercise-induced cardioprotection.[58] The results from these two studies[57,58] indicate that elevated nitric oxide production may not offer direct protection to the cardiomyocyte, but greater nitric oxide bioavailability in the vasculature may be an important factor that can contribute to cardioprotection. It is important to note distinct experimental differences between the two studies. Specifically, the two studies utilized different ischaemia reperfusion models.[57,58] Furthermore, the animal model (e.g. different species) may account for differences observed between studies. For example, Babai et al.[57] utilized an in vivo dog model of ischaemia reperfusion whereas Taylor et al.[58] utilized an in vitro rat model of ischaemia reperfusion. The disparity in the experimental approach may account for the different results. Therefore, additional research is required in this Sports Med 2009; 39 (11)
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area to fully elucidate the role of nitric oxide in exercise-induced cardioprotection. Furthermore, sarcolemmal and/or mitochondrial ATP-sensitive potassium channels have been proposed as important mediators in exerciseinduced cardioprotection. Specifically, Brown et al.[7] and Chicco et al.[59] reported that exercise training increases the expression of sarcolemmal ATP-sensitive potassium channels in the cardiac myocyte and that pharmacological blockage of these channels in the heart impairs cardioprotection. Another interesting finding is that female animals have higher sarcolemmal ATP-sensitive potassium channel density than male animals.[60,61] Importantly, studies have shown that estrogen can upregulate sarcolemmal ATP-sensitive potassium channel expression.[62] In this regard, Chicco et al.[59] and Johnson et al.[63] reported that the sexspecific cardioprotection is mediated by the higher expression of the sarcolemmal ATP-sensitive potassium channels. Furthermore, Brown et al.[7] also reported that mitochondrial ATP-sensitive potassium channels are not an essential mediator of exercise-induced protection against ischaemia reperfusion-induced myocardial infarction. However, Domenech et al.[64] showed that the early effect of exercise-induced cardioprotection is mediated through mitochondrial ATP-sensitive potassium channels. It is important to note that the molecular identity of the mitochondrial ATPsensitive potassium channels remains elusive. Therefore, studies examining the effect of the mitochondrial ATP-sensitive potassium channels have used 5-hydroxydecanoic acid as a specific inhibitor of the mitochondrial ATP-sensitive potassium channels. However, several investigators have questioned the specificity of this compound and have raised concerns for the conclusions drawn from these studies.[65] This is another example where additional research is warranted using a variety of molecular, cellular and biochemical tools before definitive conclusions can be drawn. 2.2 Increased Antioxidant Capacity Provides Cardioprotection
Researchers hypothesize that the cardioprotective benefits of exercise may be at least partially ª 2009 Adis Data Information BV. All rights reserved.
due to a reduction in oxidant production and increased myocardial antioxidant capacity. Both adaptations could reduce ischaemia reperfusioninduced oxidative damage.[9-11,14,15,17,18,21,24,29,31-33] Overexpression of myocardial antioxidants or the use of mitochondrial-targeted antioxidant minimizes ischaemia reperfusion-induced myocardial infarction.[66,67] Furthermore, research has shown that dietary supplementation with antioxidants lowers ischaemia reperfusion-induced myocardial oxidative injury and the magnitude of infarction in rats.[15,68] The most compelling evidence for exercise-induced cardioprotection is the fact that exercise training upregulates key antioxidant enzymes that have been shown to promote cardioprotection.[13-15,19,23,29,37] In this regard, both short- and long-term exercise training promotes an increase in myocardial antioxidant capacity, which is essential to achieve exercise-induced cardioprotection.[13-15,19,23,29,37] Importantly, data show that increased antioxidant activity is vital in providing protection against both myocardial necrosis and apoptosis.[14,19,31,33] Cardiac myocytes contain a network of antioxidant systems that provide protection from reactive oxygen species injury. Primary enzymatic antioxidant defences include superoxide dismutase (SOD), glutathione peroxidase and catalase. Importantly, each of these antioxidants is capable of combining with reactive oxygen species to produce other less reactive species. SOD exists in two isoforms (i.e. manganese superoxide dismutase [MnSOD] and copper zinc superoxide dismutase [CuZnSOD]). Both SOD isoforms promote the dismutation of the superoxide radical to form hydrogen peroxide and oxygen. Furthermore, catalase can then exert protection against oxidative injury by converting hydrogen peroxide to water and oxygen. Similarly, glutathione peroxidase utilizes reduced glutathione as a reducing equivalent to reduce hydrogen peroxide to form oxidized glutathione and water. Several investigators have studied the effects of endurance exercise training on the endogenous antioxidant enzymes. These studies reveal that endurance exercise training results in increased Sports Med 2009; 39 (11)
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myocardial antioxidant capacity. However, some researchers have reported no changes or even decreases in antioxidant enzymes following endurance exercise training. The ambiguity of these findings may be due to a variety of factors including methodological differences in the assay of the antioxidant activity, variations in the exercise training paradigm or improper handling of the tissue. Table II summarizes the exercise-induced response of three of the major antioxidants found in cardiac muscle (i.e. SOD, catalase and glutathione peroxidase). Importantly, to investigate the role that exercise-induced increases in MnSOD plays in cardioprotection, three innovative studies used an antisense oligonucleotide against MnSOD to prevent the exercise-induced increases in myocardial MnSOD activity.[14,29,92] All three studies concluded that increased MnSOD activity is essential to achieve optimal exercise-induced protection against both ischaemia reperfusion-induced cardiac arrhythmias and infarction.[14,29,92] In contrast, Lennon and collaborators reported that the exercise-induced increase in cardiac MnSOD is not required to achieve exercise-induced cardioprotection against myocardial stunning.[19] Therefore, based on these reports it is possible that the mechanisms responsible for exercise-induced protection against myocardial stunning differ from the mechanisms responsible for protecting the heart against myocardial arrhythmias and infarction. Additional research is warranted to delineate differences between differing levels of injury to the myocardium. In addition to primary antioxidant enzymes, cardiac cells possess other antioxidant enzymes (e.g. thioredoxin, glutaredoxin and peroxiredoxin antioxidant enzyme systems). The thioredoxin antioxidant system is composed of thioredoxin and thioredoxin reductase,[93-96] while glutar-
929
edoxin is a thiodisulfide oxidoreductase that is involved in the protection and repair of protein and non-protein thiols during periods of oxidative stress.[94,97] In addition, peroxiredoxin is involved in the reduction of both hydroperoxides and peroxynitrate with the use of electrons provided by a physiological thiol like thioredoxin.[98-100] Therefore, cardiac myocytes contain an elaborate antioxidant defence system. However, the effects of exercise training on thioredoxin, glutaredoxin and peroxiredoxin antioxidant enzyme systems in the myocardium remain unknown. This remains an interesting area for future work since it is conceivable that exercise-induced changes in one or all of these antioxidant systems could contribute to exercise-induced cardioprotection. 2.3 Exercise Training and Cardiac Mitochondria
Research performed by several laboratories indicates that mitochondria play a critical role in the heart during ischaemia reperfusion. Specifically, several laboratories have reported that exercise training results in cardiac mitochondrial adaptations that result in reduced reactive oxygen species production.[101,79,80] For example, Starnes et al.[79] reported that exercise training reduces reactive oxygen species production in myocardial mitochondria, which may result in less calcium influx on reperfusion. A similar study by Marcil et al.[101] reported that mitochondria isolated from trained hearts are more resistant to calcium-induced mitochondrial permeability transition pore opening. In addition to exercise-induced reduction in reactive oxygen species production, it appears that several exercise-induced adaptations occur in the cardiac mitochondria. Ascensa˜o et al.[9] challenged isolated cardiac mitochondria by using an in vitro anoxiareoxygenation model. The authors reported that
Table II. Published studies on the effect of endurance exercise training on three key antioxidant enzymes found in cardiac muscle Enzyme
Increase
No change
Decrease
GPX
69-78
10,11,13-15,17,18,23,24,37,79-85
86,87
Catalase
12,16-18,25,71,74,75,79,88,89
11,13-15,23,24,37,58,70,72,76,80-84
82,86,90
SOD
11-16,18,24,25,37,70-73,76,77,82,86
10,17,25,58,60,79-82,84,90,91
80
GPX = glutathione peroxidase; SOD = superoxide dismutase.
ª 2009 Adis Data Information BV. All rights reserved.
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following the anoxia-reoxygenation challenge, the drop in the mitochondrial respiratory control ratio and the adenosine diphosphate/oxygen (ADP/O) ratio were significantly attenuated in the exercise group.[9] Furthermore, Kwak and collaborators[102] were one of the first groups to report that endurance exercise training can protect against elevated apoptosis and remodelling in the aging heart. In this regard, a recent study by our group has shown that exercise training evokes a mitochondrial phenotype that is protective against apoptotic stimuli.[103] Specifically, our data indicate that both subsarcolemmal and intermyofibrillar cardiac mitochondria undergo biochemical adaptations in response to endurance exercise leading to decreased apoptotic susceptibility. Importantly, data indicate that intermyofibrillar and subsarcolemmal mitochondria exhibit a lower maximal rate of pore opening (Vmax) after endurance exercise training compared with sedentary animals. Furthermore, subsarcolemmal mitochondria obtained from hearts of endurance exercise-trained animals exhibited a longer time to Vmax compared with subsarcolemmal mitochondria isolated from sedentary animals. In addition, endurance exercise training resulted in a reduced cytochrome c release from isolated cardiac mitochondria after an in vitro reactive oxygen species challenge. These findings reveal that endurance exercise promotes biochemical alterations in cardiac subsarcolemmal and intermyofibrillar mitochondria resulting in a phenotype that resists apoptotic stimuli. Furthermore, these results are consistent with the concept that exercise-induced mitochondrial adaptations contribute to exercise-induced cardioprotection. In view of the above findings, our laboratory has investigated any exercise-induced changes in mitochondrial proteins by utilizing isobaric tags for relative and absolute quantitation. A total of 222 cardiac mitochondrial proteins were identified.[104] Specifically, repeated bouts of endurance exercise resulted in significant alterations within intermyofibrillar and subsarcolemmal mitochondria. Differentially expressed proteins could be classified into seven functional groups ª 2009 Adis Data Information BV. All rights reserved.
Kavazis
(i.e. b-oxidation of fatty acids, mitochondrial respiratory chain, the tricarboxylic acid [TCA] cycle, amino acid metabolism, apoptosis, redox regulation and receptor protein signalling pathway). Importantly, following endurance exercise training, several novel and potentially important cardioprotective mediators (e.g. monoamine oxidase A [MAO-A]) were changed. Monoamine oxidases are mitochondrial enzymes involved in the oxidative deamination of biogenic amines. Specifically, MAO-A catalyzes the oxidative deamination of several monoamines (i.e. serotonin, noradrenaline [norepinephrine], dopamine) resulting in reactive oxygen species (e.g. H2O2) production.[105] Published data indicate that during post-ischaemic myocardial injury, oxidative stress induced by MAO-A is responsible for myocardial apoptosis.[105,106] Specifically, MAO-A knockout (KO) animals are protected from ischaemia reperfusion-induced cardiac damage.[105] Notably, the protection of MAO-A KO was related to significantly lower reactive oxygen species generation following ischaemia reperfusion injury.[105] Also, several investigators have reported an increase in cardiac MAO-A activity with age.[107,108] Importantly, MAO-A protein levels and MAO-A-dependent H2O2 production strongly increases in the senescent heart, and the authors proposed that MAOA was a key factor involved in cardiac oxidative stress during aging.[109] Our laboratory has shown that MAO-A protein levels were significantly reduced in cardiac mitochondria following endurance exercise training. In view of the results discussed here, it is possible that downregulation of MAO-A protein expression following endurance exercise is one of the mechanisms for exercise-induced cardioprotection. Therefore, it is conceivable that the downregulation of MAO by endurance exercise represents a physiological and practical approach to prevent cardiac oxidative stress and subsequent cell death and apoptosis, especially in situations where the production of reactive oxygen species increases (i.e. ischaemia reperfusion). Furthermore, the quantity of other mitochondrial proteins was also altered following repeated bouts of endurance exercise. Specifically, Sports Med 2009; 39 (11)
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the abundance of several cardiac mitochondrial proteins involved in bioenergetics was changed following endurance exercise training.[104] Importantly, mitochondria are highly dynamic organelles that continuously adjust the amount of ATP produced to match changing bioenergetic demands of cells. Therefore, regulation of proteins/enzymes involved in energy production may help to satisfy the increased energy demands during exercise, and maintain and/or enhance cardiac function in the resting condition. Under physiological conditions, the myocardium obtains most of its energy supply by the oxidation of fatty acids. However, during the development of heart disease, the myocardial energy source switches from fatty acid b-oxidation to glycolysis. In addition, data indicate that reduced capacity for fatty acid utilization may lead to heart failure and cardiac rhythm disturbances. For example, acyl-CoA dehydrogenase is downregulated in a rodent model of heart failure and the level of acyl-CoA dehydrogenase was reduced in human cardiomyopathic hearts.[110] Our laboratory has shown that the protein levels of several proteins involved in b-oxidation of fatty acids [e.g. acyl-CoA dehydrogenase, hydroxyacyl-CoA dehydrogenase, d(3,5)- d(2,4)-dienoyl-CoA isomerase] were increased following repeated bouts of endurance exercise. Moreover, the levels of two proteins (methylmalonate-semialdehyde dehydrogenase and aspartate aminotransferase) involved in amino acid metabolism were increased following endurance exercise. Specifically, aminotransferases can convert some amino acids into other amino acids, and amino acid transamination may be an important adaptive process in the immature heart, improving its resistance to ischaemic damage.[111]
3. Summary and Future Directions in the Area of Exercise-Induced Cardioprotection Diseases of the heart remain the major cause of morbidity and mortality in industrialized nations. Therefore, given the impact of this problem worldwide on public health, developing a pragmatic countermeasure to provide cardioprotecª 2009 Adis Data Information BV. All rights reserved.
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tion against cardiac injury is important. Currently, the only practical method of providing sustainable cardioprotection against myocardial injury is endurance exercise training. Indeed, regular bouts of exercise have been shown to protect the heart against all levels of cardiac injury including myocardial arrhythmias, stunning and infarction. Importantly, given the growing incidence of cardiovascular disease in many countries around the world, it is important to continue to research factors leading to cardioprotection. Furthermore, the number of elderly individuals in the industrialized world is increasing, which further highlights the importance of developing countermeasures that can prevent/ minimize cardiovascular disease. Interestingly, several investigators have shown that short-term exercise training (i.e. 3–5 consecutive days) provides the same cardioprotection as that observed following long-term training (i.e. 10 weeks). Therefore, endurance exercise training may provide a pragmatic countermeasure in preventing/ minimizing cardiovascular disease that can benefit most people around the world. In recent years, substantial progress has been made in delineating the mechanisms responsible for cardioprotection that results from exercise training. However, numerous unanswered questions still remain. In order to advance our progress, additional basic research is needed in several areas. Describing the specific pathways and mechanisms that are involved in exerciseinduced cardioprotection is critical for therapeutic intervention. For example, it is important to continue to investigate the role that sarcolemmal and/or mitochondrial ATP-sensitive potassium channels play in exercise-induced cardioprotection. Currently, only a few studies are available in this area, but it appears that potassium channels may be important contributors to exerciseinduced cardioprotection. Importantly, several studies have shown that mitochondria play an important role when the cardiac muscle is challenged (e.g. ischaemia reperfusion injury). Although several sources for production of reactive oxygen species exist in cells, it is clear that mitochondrial production of reactive oxygen species occurs during both Sports Med 2009; 39 (11)
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ischaemia and reperfusion, and mitochondria are an important source of reactive oxygen species during an ischaemia and reperfusion insult.[112,113] Specifically, research reveals that exercise training protects against anoxia reoxygenation-induced damage in mitochondria isolated from the hearts of exercise-training animals.[9] In addition, a recently published paper shows that mitochondria undergo exerciseinduced adaptations that result in a phenotype that is less susceptible to reactive oxygen speciesinduced apoptosis.[103] These studies indicate that exercise training promotes changes in the mitochondria that may contribute to the exercise-induced cardioprotection. However, the mechanisms by which exercise training induces mitochondrial changes remain unknown and warrant future investigation. In summary, it is important to delineate the mechanisms responsible for exercise-induced cardioprotection; data from these studies should lead to the development of pharmacological or molecular approaches to the prevention of myocardial injury. Acknowledgements This article was supported by an award from the American Heart Association awarded to Andreas N. Kavazis and NIH grant R01HL067855 awarded to Scott K. Powers. The author wishes to acknowledge with thanks the advice and critical reviews provided by Scott K. Powers. The author has no conflicts of interest that are directly relevant to the content of this review.
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6. Taylor RP, Starnes JW. Age, cell signalling and cardioprotection. Acta Physiol Scand 2003 Jun; 178 (2): 107-16 7. Brown DA, Chicco AJ, Jew KN, et al. Cardioprotection afforded by chronic exercise is mediated by the sarcolemmal, and not the mitochondrial, isoform of the KATP channel in the rat. J Physiol 2005 Dec 15; 569 (Pt 3): 913-24 8. Bowles DK, Starnes JW. Exercise training improves metabolic response after ischemia in isolated working rat heart. J Appl Physiol 1994 Apr; 76 (4): 1608-14 9. Ascensa˜o A, Magalhaes J, Soares JM, et al. Endurance training limits the functional alterations of rat heart mitochondria submitted to in vitro anoxia-reoxygenation. Int J Cardiol 2006 May 10; 109 (2): 169-78 10. Demirel HA, Powers SK, Caillaud C, et al. Exercise training reduces myocardial lipid peroxidation following short-term ischemia-reperfusion. Med Sci Sports Exerc 1998 Aug; 30 (8): 1211-6 11. Demirel HA, Powers SK, Zergeroglu MA, et al. Short-term exercise improves myocardial tolerance to in vivo ischemia-reperfusion in the rat. J Appl Physiol 2001 Nov; 91 (5): 2205-12 12. French JP, Quindry JC, Falk DJ, et al. Ischemia-reperfusion-induced calpain activation and SERCA2a degradation are attenuated by exercise training and calpain inhibition. Am J Physiol Heart Circ Physiol 2006 Jan; 290 (1): H128-36 13. Hamilton KL, Powers SK, Sugiura T, et al. Short-term exercise training can improve myocardial tolerance to I/R without elevation in heat shock proteins. Am J Physiol Heart Circ Physiol 2001 Sep; 281 (3): H1346-52 14. Hamilton KL, Quindry JC, French JP, et al. MnSOD antisense treatment and exercise-induced protection against arrhythmias. Free Radic Biol Med 2004 Nov 1; 37 (9): 1360-8 15. Hamilton KL, Staib JL, Phillips T, et al. Exercise, antioxidants, and HSP72: protection against myocardial ischemia/reperfusion. Free Radic Biol Med 2003 Apr 1; 34 (7): 800-9 16. Harris MB, Starnes JW. Effects of body temperature during exercise training on myocardial adaptations. Am J Physiol Heart Circ Physiol 2001 May; 280 (5): H2271-80 17. Lennon SL, Quindry J, Hamilton KL, et al. Loss of exercise-induced cardioprotection after cessation of exercise. J Appl Physiol 2004 Apr; 96 (4): 1299-305 18. Lennon SL, Quindry JC, French JP, et al. Exercise and myocardial tolerance to ischaemia-reperfusion. Acta Physiol Scand 2004 Oct; 182 (2): 161-9 19. Lennon SL, Quindry JC, Hamilton KL, et al. Elevated MnSOD is not required for exercise-induced cardioprotection against myocardial stunning. Am J Physiol Heart Circ Physiol 2004 Aug; 287 (2): H975-80 20. Libonati JR. Exercise training improves left ventricular isovolumic relaxation. Med Sci Sports Exerc 2000 Aug; 32 (8): 1399-405 21. Libonati JR, Gaughan JP, Hefner CA, et al. Reduced ischemia and reperfusion injury following exercise training. Med Sci Sports Exerc 1997 Apr; 29 (4): 509-16
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22. Libonati JR, Kendrick ZV, Houser SR. Sprint training improves postischemic, left ventricular diastolic performance. J Appl Physiol 2005 Dec; 99 (6): 2121-7 23. Powers SK, Demirel HA, Vincent HK, et al. Exercise training improves myocardial tolerance to in vivo ischemia-reperfusion in the rat. Am J Physiol 1998 Nov; 275 (5 Pt 2): R1468-77 24. Quindry J, French J, Hamilton K, et al. Exercise training provides cardioprotection against ischemia-reperfusion induced apoptosis in young and old animals. Exp Gerontol 2005 May; 40 (5): 416-25 25. Starnes JW, Taylor RP, Park Y. Exercise improves postischemic function in aging hearts. Am J Physiol Heart Circ Physiol 2003 Jul; 285 (1): H347-51 26. Starnes JW, Taylor RP, Ciccolo JT. Habitual low-intensity exercise does not protect against myocardial dysfunction after ischemia in rats. Eur J Cardiovasc Prev Rehabil 2005 Apr; 12 (2): 169-74 27. Taylor RP, Harris MB, Starnes JW. Acute exercise can improve cardioprotection without increasing heat shock protein content. Am J Physiol 1999 Mar; 276 (3 Pt 2): H1098-102 28. Taylor RP, Olsen ME, Starnes JW. Improved postischemic function following acute exercise is not mediated by nitric oxide synthase in the rat heart. Am J Physiol Heart Circ Physiol 2007 Jan; 292 (1): H601-7 29. Yamashita N, Hoshida S, Otsu K, et al. Exercise provides direct biphasic cardioprotection via manganese superoxide dismutase activation. J Exp Med 1999 Jun 7; 189 (11): 1699-706 30. Hoshida S, Yamashita N, Otsu K, et al. Repeated physiologic stresses provide persistent cardioprotection against ischemia-reperfusion injury in rats. J Am Coll Cardiol 2002 Aug 21; 40 (4): 826-31 31. Powers SK, Lennon SL, Quindry J, et al. Exercise and cardioprotection. Curr Opin Cardiol 2002 Sep; 17 (5): 495-502 32. Powers SK, Locke AM, Demirel HA. Exercise, heat shock proteins, and myocardial protection from I-R injury. Med Sci Sports Exerc 2001 Mar; 33 (3): 386-92 33. Powers SK, Quindry J, Hamilton K. Aging, exercise, and cardioprotection. Ann N Y Acad Sci 2004 Jun; 1019: 462-70 34. Zhang LQ, Zhang XQ, Ng YC, et al. Sprint training normalizes Ca(2+) transients and SR function in postinfarction rat myocytes. J Appl Physiol 2000 Jul; 89 (1): 38-46 35. Ascensao A, Ferreira R, Magalhaes J. Exercise-induced cardioprotection: biochemical, morphological and functional evidence in whole tissue and isolated mitochondria. Int J Cardiol 2007 Apr 12; 117 (1): 16-30 36. Powers SK, Quindry JC, Kavazis AN. Exercise-induced cardioprotection against myocardial ischemia-reperfusion injury. Free Radic Biol Med 2008 Jan 15; 44 (2): 193-201 37. Powers SK, Criswell D, Lawler J, et al. Rigorous exercise training increases superoxide dismutase activity in ventricular myocardium. Am J Physiol 1993 Dec; 265 (6 Pt 2): H2094-8 38. Locke M, Tanguay RM, Klabunde RE, et al. Enhanced postischemic myocardial recovery following exercise
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induction of HSP 72. Am J Physiol 1995 Jul; 269 (1 Pt 2): H320-5 Ignarro LJ, Balestrieri ML, Napoli C. Nutrition, physical activity, and cardiovascular disease: an update. Cardiovasc Res 2007 Jan 15; 73 (2): 326-40 Thompson PD, Buchner D, Pina IL, et al. Exercise and physical activity in the prevention and treatment of atherosclerotic cardiovascular disease: a statement from the Council on Clinical Cardiology (Subcommittee on Exercise, Rehabilitation, and Prevention) and the Council on Nutrition, Physical Activity, and Metabolism (Subcommittee on Physical Activity). Circulation 2003 Jun 24; 107 (24): 3109-16 Blair SN, Goodyear NN, Gibbons LW, et al. Physical fitness and incidence of hypertension in healthy normotensive men and women. JAMA 1984 Jul 27; 252 (4): 487-90 Paffenbarger Jr RS, Wing AL, Hyde RT, et al. Physical activity and incidence of hypertension in college alumni. Am J Epidemiol 1983 Mar; 117 (3): 245-57 Kokkinos PF, Narayan P, Colleran JA, et al. Effects of regular exercise on blood pressure and left ventricular hypertrophy in African-American men with severe hypertension. N Engl J Med 1995 Nov 30; 333 (22): 1462-7 Shephard RJ, Balady GJ. Exercise as cardiovascular therapy. Circulation 1999 Feb 23; 99 (7): 963-72 Tran ZV, Weltman A. Differential effects of exercise on serum lipid and lipoprotein levels seen with changes in body weight: a meta-analysis. JAMA 1985 Aug 16; 254 (7): 919-24 Bowles DK, Woodman CR, Laughlin MH. Coronary smooth muscle and endothelial adaptations to exercise training. Exerc Sport Sci Rev 2000 Apr; 28 (2): 57-62 Laughlin MH, Korzick DH. Vascular smooth muscle: integrator of vasoactive signals during exercise hyperemia. Med Sci Sports Exerc 2001 Jan; 33 (1): 81-91 Moncada S, Palmer RM, Higgs EA. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 1991 Jun; 43 (2): 109-42 Laughlin MH, Oltman CL, Bowles DK. Exercise traininginduced adaptations in the coronary circulation. Med Sci Sports Exerc 1998 Mar; 30 (3): 352-60 Quindry JC, French J, Hamilton KL, et al. Cyclooxygenase-2 is unaltered by exercise in the young and old heart [abstract]. Med Sci Sports Exerc 2006; 38 (5): S416 Murlasits Z, Lee Y, Powers SK. Short-term exercise does not increase ER stress protein expression in cardiac muscle. Med Sci Sports Exerc 2007 Sep; 39 (9): 1522-8 Quindry JC, Hamilton KL, French JP, et al. Exerciseinduced HSP-72 elevation and cardioprotection against infarct and apoptosis. J Appl Physiol 2007 Sep; 103: 1056-62 Bell RM, Smith CC, Yellon DM. Nitric oxide as a mediator of delayed pharmacological (A (1) receptor triggered) preconditioning: is eNOS masquerading as iNOS? Cardiovasc Res 2002 Feb 1; 53 (2): 405-13 Di Napoli P, Taccardi AA, Grilli A, et al. Chronic treatment with rosuvastatin modulates nitric oxide synthase expression and reduces ischemia-reperfusion injury in rat hearts. Cardiovasc Res 2005 Jun 1; 66 (3): 462-71 Hattori R, Otani H, Maulik N, et al. Pharmacological preconditioning with resveratrol: role of nitric oxide. Am J Physiol Heart Circ Physiol 2002 Jun; 282 (6): H1988-95
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56. Bolli R. Cardioprotective function of inducible nitric oxide synthase and role of nitric oxide in myocardial ischemia and preconditioning: an overview of a decade of research. J Mol Cell Cardiol 2001 Nov; 33 (11): 1897-918 57. Babai L, Szigeti Z, Parratt JR, et al. Delayed cardioprotective effects of exercise in dogs are aminoguanidine sensitive: possible involvement of nitric oxide. Clin Sci (Lond) 2002 Apr; 102 (4): 435-45 58. Taylor RP, Olsen ME, Starnes JW. Improved postischemic function following acute exercise is not mediated by nitric oxide synthase in the rat heart. Am J Physiol Heart Circ Physiol 2007 Jan; 292 (1): H601-7 59. Chicco AJ, Johnson MS, Armstrong CJ, et al. Sex-specific and exercise-acquired cardioprotection is abolished by sarcolemmal KATP channel blockade in the rat heart. Am J Physiol Heart Circ Physiol 2007 May; 292 (5): H2432-7 60. Brown DA, Lynch JM, Armstrong CJ, et al. Susceptibility of the heart to ischaemia-reperfusion injury and exerciseinduced cardioprotection are sex-dependent in the rat. J Physiol 2005 Apr 15; 564 (Pt 2): 619-30 61. Ranki HJ, Budas GR, Crawford RM, et al. Gender-specific difference in cardiac ATP-sensitive K(+) channels. J Am Coll Cardiol 2001 Sep; 38 (3): 906-15 62. Ranki HJ, Budas GR, Crawford RM, et al. 17Beta-estradiol regulates expression of K (ATP) channels in heart-derived H9c2 cells. J Am Coll Cardiol 2002 Jul 17; 40 (2): 367-74 63. Johnson MS, Moore RL, Brown DA. Sex differences in myocardial infarct size are abolished by sarcolemmal KATP channel blockade in rat. Am J Physiol Heart Circ Physiol 2006 Jun; 290 (6): H2644-7 64. Domenech R, Macho P, Schwarze H, et al. Exercise induces early and late myocardial preconditioning in dogs. Cardiovasc Res 2002 Aug 15; 55 (3): 561-6 65. Brown DA, Moore RL. Perspectives in innate and acquired cardioprotection: cardioprotection acquired through exercise. J Appl Physiol 2007 Nov; 103 (5): 1894-9 66. Chen Z, Siu B, Ho YS, et al. Overexpression of MnSOD protects against myocardial ischemia/reperfusion injury in transgenic mice. J Mol Cell Cardiol 1998 Nov; 30 (11): 2281-9 67. Adlam VJ, Harrison JC, Porteous CM, et al. Targeting an antioxidant to mitochondria decreases cardiac ischemiareperfusion injury. FASEB J 2005 Jul; 19 (9): 1088-95 68. Coombes JS, Powers SK, Hamilton KL, et al. Improved cardiac performance after ischemia in aged rats supplemented with vitamin E and alpha-lipoic acid. Am J Physiol Regul Integr Comp Physiol 2000 Dec; 279 (6): R2149-55 69. Aydin C, Ince E, Koparan S, et al. Protective effects of long term dietary restriction on swimming exercise-induced oxidative stress in the liver, heart and kidney of rat. Cell Biochem Funct 2007 Mar-Apr; 25 (2): 129-37 70. Gunduz F, Senturk UK, Kuru O, et al. The effect of one year’s swimming exercise on oxidant stress and antioxidant capacity in aged rats. Physiol Res 2004; 53 (2): 171-6 71. Husain K, Hazelrigg SR. Oxidative injury due to chronic nitric oxide synthase inhibition in rat: effect of regular
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87. Ji LL, Fu RG, Mitchell EW, et al. Cardiac hypertrophy alters myocardial response to ischaemia and reperfusion in vivo. Acta Physiol Scand 1994 Jul; 151 (3): 279-90 88. Husain K. Interaction of physical training and chronic nitroglycerin treatment on blood pressure, nitric oxide, and oxidants/antioxidants in the rat heart. Pharmacol Res 2003 Sep; 48 (3): 253-61 89. Kim JD, Yu BP, McCarter RJ, et al. Exercise and diet modulate cardiac lipid peroxidation and antioxidant defenses. Free Radic Biol Med 1996; 20 (1): 83-8 90. Kihlstrom M. Protection effect of endurance training against reoxygenation-induced injuries in rat heart. J Appl Physiol 1990 Apr; 68 (4): 1672-8 91. Chicco AJ, Hydock DS, Schneider CM, et al. Low-intensity exercise training during doxorubicin treatment protects against cardiotoxicity. J Appl Physiol 2006 Feb; 100 (2): 519-27 92. French JP, Hamilton KL, Quindry JC, et al. Exercise-induced protection against myocardial apoptosis and necrosis: MnSOD, calcium-handling proteins, and calpain. FASEB J 2008 Aug; 22 (8): 2862-71 93. Yoshioka J, Schreiter ER, Lee RT. Role of thioredoxin in cell growth through interactions with signaling molecules. Antioxid Redox Signal 2006 Nov-Dec; 8 (11-12): 2143-51 94. Berndt C, Lillig CH, Holmgren A. Thiol-based mechanisms of the thioredoxin and glutaredoxin systems: implications for diseases in the cardiovascular system. Am J Physiol Heart Circ Physiol 2007 Mar; 292 (3): H1227-36 95. Arner ES, Holmgren A. Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 2000 Oct; 267 (20): 6102-9 96. Holmgren A, Johansson C, Berndt C, et al. Thiol redox control via thioredoxin and glutaredoxin systems. Biochem Soc Trans 2005 Dec; 33 (Pt 6): 1375-7 97. Holmgren A. Hydrogen donor system for Escherichia coli ribonucleoside-diphosphate reductase dependent upon glutathione. Proc Natl Acad Sci U S A 1976 Jul; 73 (7): 2275-9 98. Kim K, Kim IH, Lee KY, et al. The isolation and purification of a specific ‘‘protector’’ protein which inhibits enzyme inactivation by a thiol/Fe (III)/O2 mixedfunction oxidation system. J Biol Chem 1988 Apr 5; 263 (10): 4704-11 99. Rhee SG, Chae HZ, Kim K. Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radic Biol Med 2005 Jun 15; 38 (12): 1543-52 100. Kim K, Rhee SG, Stadtman ER. Nonenzymatic cleavage of proteins by reactive oxygen species generated by dithiothreitol and iron. J Biol Chem 1985 Dec 15; 260 (29): 15394-7 101. Marcil M, Bourduas K, Ascah A, et al. Exercise training induces respiratory substrate-specific decrease in Ca2+induced permeability transition pore opening in heart
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mitochondria. Am J Physiol Heart Circ Physiol 2006 Apr; 290 (4): H1549-57 Kwak HB, Song W, Lawler JM. Exercise training attenuates age-induced elevation in Bax/Bcl-2 ratio, apoptosis, and remodeling in the rat heart. FASEB J 2006 Apr; 20 (6): 791-3 Kavazis AN, McClung JM, Hood DA, et al. Exercise induces a cardiac mitochondrial phenotype that resists apoptotic stimuli. Am J Physiol Heart Circ Physiol 2008 Feb; 294 (2): H928-35 Kavazis AN, Alvarez S, Talbert E, et al. Exercise training induces a cardioprotective phenotype and alterations in cardiac subsarcolemmal and intermyofibrillar mitochondrial proteins. Am J Physiol Heart Circ Physiol 2009 Jul; 297 (1): H144-52 Pchejetski D, Kunduzova O, Dayon A, et al. Oxidative stress-dependent sphingosine kinase-1 inhibition mediates monoamine oxidase A-associated cardiac cell apoptosis. Circ Res 2007 Jan 5; 100 (1): 41-9 Bianchi P, Kunduzova O, Masini E, et al. Oxidative stress by monoamine oxidase mediates receptor-independent cardiomyocyte apoptosis by serotonin and postischemic myocardial injury. Circulation 2005 Nov 22; 112 (21): 3297-305 Cao Danh H, Strolin Benedetti M, Dostert P, et al. Agerelated changes in benzylamine oxidase activity in rat tissues. J Pharm Pharmacol 1984 Sep; 36 (9): 592-6 Meco M, Bonifati V, Collier WL, et al. Enzyme histochemistry of monoamine oxidase in the heart of aged rats. Mech Ageing Dev 1987 Apr; 38 (2): 145-55 Maurel A, Hernandez C, Kunduzova O, et al. Age-dependent increase in hydrogen peroxide production by cardiac monoamine oxidase A in rats. Am J Physiol Heart Circ Physiol 2003 Apr; 284 (4): H1460-7 Barger PM, Kelly DP. Fatty acid utilization in the hypertrophied and failing heart: molecular regulatory mechanisms. Am J Med Sci 1999 Jul; 318 (1): 36-42 Julia P, Young HH, Buckberg GD, et al. Studies of myocardial protection in the immature heart. II. Evidence for importance of amino acid metabolism in tolerance to ischemia. J Thorac Cardiovasc Surg 1990 Dec; 100 (6): 888-95 Downey JM. Free radicals and their involvement during long-term myocardial ischemia and reperfusion. Annu Rev Physiol 1990; 52: 487-504 Li C, Jackson RM. Reactive species mechanisms of cellular hypoxia-reoxygenation injury. Am J Physiol Cell Physiol 2002 Feb; 282 (2): C227-41
Correspondence: Dr Andreas N. Kavazis, Department of Applied Physiology and Kinesiology, University of Florida, Gainesville, FL 32611, USA. E-mail:
[email protected]
Sports Med 2009; 39 (11)
REVIEW ARTICLE
Sports Med 2009; 39 (11): 937-960 0112-1642/09/0011-0937/$49.95/0
ª 2009 Adis Data Information BV. All rights reserved.
The Potential Role of Prophylactic/ Functional Knee Bracing in Preventing Knee Ligament Injury Neetu Rishiraj,1,2,3 Jack E. Taunton,4,5 Robert Lloyd-Smith,5 Robert Woollard,6 William Regan7 and D.B. Clement5 * 1 2 3 4 5
School of Physiotherapy, University of Otago, Dunedin, New Zealand ACTIN Health & Rehabilitation Inc., Vancouver, British Columbia, Canada School of Human Kinetics, University of British Columbia, Vancouver, British Columbia, Canada Chief Medical Officer, 2010 Winter Olympics, Vancouver, British Columbia, Canada Primary Care, Allan McGavin Sports Medicine Centre, University of British Columbia, Vancouver, British Columbia, Canada 6 Department of Family Practice, University of British Columbia, Vancouver, British Columbia, Canada 7 Orthopaedics Department, Allan McGavin Sports Medicine Centre, University of British Columbia, Vancouver, British Columbia, Canada
Contents Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Knee Bracing: 1970 to Mid-1990s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.1 Bracing Effectiveness Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2 Cadaver and Surrogate Model Studies. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.3 Functional Knee Brace Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.3.1 Subjective and Clinical Assessments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.3.2 Kinematic Testing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.3.3 Ground Reaction Force Testing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.3.4 Sport-Related Performance Testing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.4 Summary of Knee Bracing: 1970 to Mid-1990s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Knee Bracing: Mid-1990s to Present . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1 Knee Bracing Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2 Functional Knee Bracing and Game-Related Performance Testing . . . . . . . . . . . . . . . . . . . . . . . . 2.3 Summary of Knee Bracing: Mid-1990s to Present . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Conclusions and Recommendations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Abstract
* Now Emeritus.
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It is estimated that knee injuries account for up to 60% of all sport injuries, with the anterior cruciate ligament (ACL) accounting for almost half of these knee injuries. These knee injuries can result in high healthcare costs, as an ACL injury is often associated with surgery, long and costly rehabilitation, differing degrees of impairment and potential long-term consequences such
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as osteoarthritis. The interest in ACL injury prevention has been extensive for the past decade. Over this period, many ACL (intrinsic and extrinsic) injury risk factors have been identified and investigated by numerous researchers. Although prevention programmes have shown potential in decreasing knee ligament injuries, several researchers have suggested that no conclusive evidence has been presented in reducing the rate and/or severity of ACL injuries during sporting competition. Knee braces have been available for the last 30 years and have been used to assist individuals with ACL-deficient and ACL-reconstructed knees. However, research is limited on the use of knee braces (prophylactic and functional) to potentially prevent knee ligament injury in the non-injured population. One possible explanation for the limited research could be that the use of these devices has raised concerns of decreased or impaired athletic performance. In summary, the review of subjective and some objective publications suggests that a functional knee brace may offer stability to an ACL-deficient knee joint; however, research is limited on the use of a knee brace for prophylactic use in non-injured athletes. The limited research could be a result of fear of performance hindrance that has led to poor knee brace compliance.
The risk of knee injury varies between sports, ranging between 13% and 71% of all sport injuries.[1-5] However, knee injuries, via contact and non-contact, are recognized as being particularly high in collision and contact sports.[6-8] It is estimated 81% of North American football (hereafter referred to as football) players sustain an injury. Of these injuries, 13–71% are concentrated at the knee joint.[9-13] In ice hockey, injuries concerning the knee joint range between 13.5% and 42% of all the injuries sustained by participants.[4,14-17] In soccer, 11–49% of all reported injuries are localized to the knee joint.[18-23] Of these knee injuries, up to 64% involve the anterior cruciate ligament (ACL).[1,5,12,14,18,19] In Australia, the private medical system has documented 52 446 knee injuries involving the ACL between 1994 and 2003.[24] In New Zealand, available data from three sports (soccer, netball, rugby) showed 2381 claims for knee injury totalling $US10.3 million ($NZ13.6 million) in 2006, with the mean cost per ACL surgery being approximately $US11 500 ($NZ15 000).[25] In 2002–3, the New Zealand Accident Compensation Corporation (ACC) spent almost $US7.2 million
($NZ9.5 million) on ACL injuries sustained while participating in the three sports listed above.[25] In 2000, conservative estimated costs for an ACL surgery and rehabilitation in the US was up to $US25 000 per athlete,[1,26,27] with the total cost reaching $US2.0 billion per annum.[26,28-32] This total price did not include the cost of initial evaluation and treatment of those injured individuals requiring conservative/nonsurgical care, or the cost of future for healthcare and employment (estimated to be $US3.4 billion in 1997)[33] for those who develop post-traumatic osteoarthritis1 (OA).[1,26,29,31,34,35] Roos[36] and Von Porat et al.[37] have identified that individuals (females and males) who sustained an ACL injury while playing soccer had 51% higher radiographic changes related to OA 12–14 years post-injury. Furthermore, Ford et al.,[38] Freedman et al.[39] and Deacon et al.[40] stated that the risk of being diagnosed with OA increased 100 times in athletes who have sustained a knee injury. These figures are of concern, as >50% of ACL injuries occur in young athletes aged 15–25 years.[27,41-43] Knee injury prevention should be of even greater concern when it is considered that statistics on
1 These costs include both males and females with OA aged ‡30 years. OA data (incidence and costs) exclusive to sports knee injuries were not available even though an extensive database search was completed.[33]
ª 2009 Adis Data Information BV. All rights reserved.
Sports Med 2009; 39 (11)
Knee Bracing in Preventing Knee Ligament Injury
return to sport post-injury, with conservative management and/or ACL reconstruction, illustrate a decreased level of participation, earlier forced retirement and/or continued knee joint discomfort. Following reconstruction, not all individuals return to their pre-injury level of competition, and those that do can expect up to 33% performance decrement compared with preinjury levels.[44,45] Roos et al.[46] found that only 30% of the ACL injured soccer players were active 3 years post-injury compared with 80% in an uninjured control population. The reason for this early departure from sport participation may be attributed to the fact that athletes who return to sport experience significant knee joint instability and a reduced range of motion and/or pain. As Myklebust and Bahr[47] stated, ‘‘It seems fair to conclude that, although the initial return rate is high, regardless of the treatment, previously injured athletes retire at a higher rate than athletes without previous ACL injury.’’ Furthermore, the above-listed medical costs and challenges do not account for the discomfort associated with long-term debilitating OA, which can affect the injured person’s professional, academic and/or private life.[23,38-40,48-52] Recently, the elevated risk of ACL injury in women, coupled with a 10-fold increase in US high school and a 5-fold increase in US collegiate sport participation in the past 30 years, has led to a rapid rise in the number of ACL injuries in female sports.[53,54] This increase in ACL injury in the female sports population has fuelled intensive research to identify the possible mechanism(s) responsible for high incidences of female knee injuries. However, despite the increased concern regarding the excessive number of ACL injuries in women, most orthopaedic literature on ACL reconstruction cites that more men than women experience an ACL injury and require ACL reconstructive surgery.[55] This ‘epidemic’ has prompted investigations aimed at identifying factors that will decrease knee injury severity and/or rates.[11,32] The initial ACL injuryprevention strategy had concentrated on enhancing the protection offered by the hamstring muscle group.[56-59] However, research has illustrated that this muscle group may be ineffective ª 2009 Adis Data Information BV. All rights reserved.
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in protecting the knee joint ligaments because of a delayed neuromuscular response.[60-65] In addition, the role of numerous other intrinsic and extrinsic risk factors as potential contributors to an ACL injury has been addressed by many researchers[26,29,32,61-63,66-108] and has led to the publication of more than 2000 scientific articles on ACL injuries in the past two decades.[109] Researchers agree that the findings on intrinsic risk factors improve our understanding of the mechanism(s) involved in ACL injury; however, widespread disagreement still remains regarding the effectiveness of prevention programmes aimed at both extrinsic and intrinsic ACL injury risk factors.[79,110-116] Thirty-six programme published papers were reviewed;[27,79,110-125] 24 studies reported a decrease in the rate of knee injuries in the intervention group[27,70,74,101,110,111,118-121,126-139] and 12 papers reported no effect of the respective intervention.[115-117,124,140-147] Hewett et al.[30] performed a meta-analysis of six randomized controlled trails or prospective cohort study prevention programmes[27,79,110,115,116,118] and concluded, ‘‘There is evidence that neuromuscular training decreases potential biomechanical risk factors for ACL injury and decreases ACL injury incidence in female athletes. However, we do not know which components [agility, balance, flexibility, plyometrics, proprioception, strengthening, training rate/intensity] are most effective or where their effects are combinatorial.’’ Nevertheless, as Griffin et al.[32] stated, ‘‘yone must appreciate that if anatomical [intrinsic] factors are found to be definitely associated with an increased risk of injury, they may be more difficult to modify than are environment, hormonal, and/or neuromuscular factors.’’ Griffin et al.[32] further stated, ‘‘The impact of ACL prevention programs is still largely unknown. More randomized controlled trails are needed between institutions, between various geographic areas of the country, across all age groups, and across both sexes for all high-risk sports, followed by a careful analysis of the effects of these prevention programs on influencing dynamic knee stability, sport performance, and overall injury rates.’’ It should also be noted that most prevention programmes have concentrated Sports Med 2009; 39 (11)
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on female athletes and have not addressed the high number of basketball non-contact ACL injuries for male athletes (60.3% for males vs 63.8% for females),[148,149] the high risk of contact ACL injuries in soccer for both sexes (46% for females and 58.7% for males),[18,19] and the high percentage of contact ACL injuries in collision sports such as football[13] and ice hockey.[4] In 1973, a paper on the first ‘functional knee brace’ (FKB) called the Anderson Knee Stabler (Omni Scientific Inc., Lafayette, IL, USA) to be worn in a sporting domain was published.[150] It was not until 1985 that the American Association of Orthopaedics Surgeons (AAOS)[151] sponsored a seminar to discuss the effectiveness of knee braces. From this seminar, three distinct brace classifications (rehabilitation, prophylactic and FKBs) were established;[150,151] these classifications are still used today (see figures 1–3). Rehabilitation braces are designed to allow a protected range of motion of injured knees post-surgery.
a
b
Fig. 1. Rehabilitation knee braces: (a) DonJoy, TROM Advance ¨ ssur, Innovator Rehab Knee Brace (permission to Cool and (b) O reprint kindly provided by DJO Inc., Vista, CA, USA and Ossur Americas, Orthopedics, Foothill Ranch, CA, USA).
ª 2009 Adis Data Information BV. All rights reserved.
Prophylactic knee braces (PKBs) are ‘off-the-shelf’ knee braces designed to prevent or reduce the severity of knee injuries. FKBs are custom-made braces that are designed to provide stability for unstable knees.[151,152] Despite much research having been conducted in the area of FKBs, the efficacy of these knee braces remains in question. Almost 20 years after their first meeting on knee bracing, the AAOS Position Statement was adjusted to reflect current research.[153] The AAOS[153] now stated ‘‘ywell-designed experimental studies have shown that currently available off-the-shelf prophylactic knee braces can provide at least 20% to 30% greater resistance to a lateral blow to the knee of sufficient magnitude to cause medial joint line opening. At least one well-designed clinical trial has revealed a statistically significant reduction in medical collateral ligament injuries with the use of a prophylactic knee brace.’’ The AAOS further stated that ‘‘ystudies designed to test whether FKBs protect against the knee ‘giving way’ have demonstrated some beneficial effect of the brace.’’[153] Despite the apparent preventive benefit(s), athletes remain reluctant to use a knee brace because of perceived impediment to performance.[52,153-157] The purpose of this literature review was twofold. First, to provide a synopsis of the current understanding of knee bracing, and second, to provide published evidence as to whether FKBing in non-injured individuals hinders performance. The following Internet search databases were employed to detect relevant articles: Evidence-Based Medicine Reviews, PubMed, SportDiscus, Ovid, MEDLINE and Proquest 5000. The search reference terms ‘knee injuries’, ‘bracing’, ‘knee bracing’, ‘functional knee bracing’ and ‘prophylactic knee bracing’ were used. In order to maintain the scientific integrity of the review process, the criteria for inclusion were that articles were originally published in peerreviewed scientific journals (n = 193), National Governing Body Reports (n = 6), and/or Clinical Symposia/Meeting Reports (n = 6). One submitted article, one article (with editor’s consent) that was not available on search databases, information from texts (n = 4), and one unpublished thesis were also cited. Sports Med 2009; 39 (11)
Knee Bracing in Preventing Knee Ligament Injury
a
b
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d
e
f
Fig. 2. Prophylactic knee braces: (a) and (b) DonJoy, with unilateral hinged bar; (c) and (d) DonJoy, ACL Everyday, with bilateral hinged ¨ ssur, Paradigm with bilateral hinged bars; (f) O ¨ ssur, Trainer with unilateral hinged bar and strap (permission to reprint kindly bars; (e) O provided by DJO Inc., Vista, CA, USA and Ossur Americas, Orthopedics, Foothill Ranch, CA, USA).
1. Knee Bracing: 1970 to Mid-1990s During the 1970s, knee braces were used primarily for rehabilitation purposes. Devices such as the Lenox Hill brace (Lenox Hill Hospital Brace Shop, New York, NY, USA) were viewed as too bulky and restrictive during competition. Between 1979 and 1985, over 30 brace manufacturers introduced various knee braces that claimed to prevent medial collateral ligament (MCL) and ACL knee ligament injuries. Before 1985, accounts of the successes or failures of these devices were largely anecdotal.[158] After 1985, several studies focused on bracing effectiveness studies, cadaveric/surrogate model and subjective/objective study design. Research involving epidemiological and cadaveric/surrogate model study design tested the efficacy of PKBs in preventing knee ligament injuries. Studies involving subjective/objective methodology evaluated the PKB and the FKB effectiveness in preventing a MCL and/or ACL injury. The data obtained during the first 17 years allowed the AAOS to publish their first position paper on knee bracing.[151] This publication also fuelled knee bracing research, leading to 17 papers being published on this topic over the next 8 years. In the mid-1990s, with an increase in non-contact ACL injuries in female sports, researchers shifted their attention specifically to preventing noncontact ACL injuries and the role of knee bracing post-injury/surgery. ª 2009 Adis Data Information BV. All rights reserved.
1.1 Bracing Effectiveness Studies
Thirteen studies were reviewed, with ten studies[52,157,159-166] concentrating solely on MCL injury and the remaining three studies[9,167,168] on both MCL and ACL injury rates (see table I). Four studies reported no significant change in MCL knee injury rates,[163,164,166-167] whereas two studies a
b
¨ ssur, ExtremeLigament Fig. 3. Functional knee braces: (a) O Knee Brace, hinge, post, shell design, and (b) DonJoy, 4TITUDE, hinge, post, strap design (permission to reprint kindly provided by DJO Inc., Vista, CA, USA and Ossur Americas, Orthopedics, Foothill Ranch, CA, USA).
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Table I. Summary of bracing effectiveness studies using prophylactic knee braces Study (year)
Subjects
Brace type
Result(s)
Anderson et al.[160] (1979)
Nine professional American football players with knee injuries
Anderson Knee Stabler
Subjects played 29 games over two seasons without re-injury to the knee
Hansen et al.[161] (1985)
University of South California. 329 non-braced players and 148 braced players
Anderson Knee Stabler
Injury rate for non-braced players was 11% vs 5% for braced players
Schriner[162] (1985)
1246 high school players from 25 schools in Michigan
DonJoy, Cutter Anderson, Omni, McDavid Knee Stablizer
45 injuries from lateral blows in non-braced group vs 0 injuries from lateral blows in braced group
Hewson et al.[163] (1986)
University of Arizona. Non-braced (1977–1981): 28 191 IEs Braced (1981–1985): 29 293 IEs
Anderson Knee Stabler
No statistical difference in MCL injuries between the non-braced and braced periods
Rovere et al.[164] (1987)
Wake Forest University (1981–1984)
Anderson Knee Stabler
6.1% knee injuries during non-braced period and 7.5% knee injuries during braced period; data not statistically significant
Teitz et al.[159] (1987)
NCAA division 1 1984: 6307 players from 71 schools 1985: 5445 players from 61 schools
McDavid, Omni, Anderson Knee Stabler, Stabilizer, Don Joy, American Prostheses, others not specified
1984: 6.0% injury rate for non-braced vs 11% for braced players 1985: 6.4% injury rate for non-braced vs 9.4% for braced players. Significantly more MCL injuries for braced players
Grace et al.[165] (1988)
Albuquerque and Santa Fe high school players. 250 non-braced control group matched with 247 with single-hinge braces and 83 with double-hinged braces
Primarily McDavid Knee Stablizer and Stromgern
Knee injury rates: 1) non-braced = 4% 2) single-hinge = 15% significant › 3) double-hinged = 6%, statistically nonsignificant
Taft et al.[167] (1989)
University of North Carolina. (1980–1982) non-braced group (1983–1985) braced group
Anderson Knee Stabler and McDavid Knee Stablizer
No statistical difference in MCL, ACL or meniscal injuries between the non-braced and the braced periods
Sitler et al.[168] (1990)
1396 West Point Cadets playing intramural American Football
DonJoy Orthopaedics, Protector Knee Guard
Significant fl in total number of knee injuries and MCL injury in braced subjects Significant fl only noted in players playing a defensive position No significant fl in severity of MCL and ACL
Zemper[166] (1990)
Representation of NCAA and NAIA football teams/players: (1986) 32 teams with 3431 players (1987) 27 teams with 2798 players
Omni Anderson Knee Stabler (used by 37.5% of the subjects), DonJoy (20.5%), McDavid Knee Guard (20.6%), other unnamed braces (21.4%)
Total number of knee injuries observed: braced = 185 non-braced = 336 MCL injuries (based on 1987 data): braced = 32 non-braced = 69 severity of MCL injuries (based on 1987 data): MCL 1: braced = 21; non-braced = 41 MCL 2: braced = 8 non-braced = 22 MCL 3: braced = 3 non-braced = 6 Author concluded braces have no significant effect in reducing the severity of all knee injuries and specifically of MCL injuries Continued next page
ª 2009 Adis Data Information BV. All rights reserved.
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Table I. Contd Study (year)
Subjects
Brace type
Result(s)
Jackson et al.[9] (1991)
Professional Canadian Football League team (American Football): (1977–1983) non-braced group (1984–1988) braced group
McDavid Knee Stabilizer, Depuy, and Anderson Knee Stabler
No significant difference in number of injuries 17% significant fl in severity (>21-days lost) of knee injuries, 20% statistical fl in MCL injuries. No significant difference in ACL injuries
Albright et al.[52,157] (1994)
987 NCAA division 1 college football players, 50% braced
Unspecified
Found statistically significant lower rate of injury for braced vs non-braced players playing in ‘non-skilled’ positions
ACL = anterior cruciate ligament; IE = injury exposure; MCL = medial collateral ligament; NCAA = National Collegiate Athletic Association; › indicates increase; fl indicates decrease.
showed a significant increase in incidence of MCL knee injuries while using a PKB.[159,165] The remaining seven studies supported the use of a PKB for preventing MCL injures.[9,52,157,160-162,168] However, only four studies found a statistically significant reduction in MCL injury rates while using a PKB.[9,52,157,168] Of these four studies, Sitler et al.[168] and Albright et al.[52,157] stated that the statistically significant lower MCL injury rates pertained only to players playing in a defensive or in a ‘non-skilled’ position. All three studies concentrating on ACL injuries found no statistically significant difference between braced and nonbraced subjects.[9,167,168] 1.2 Cadaver and Surrogate Model Studies
Several studies have examined knee bracing from a biomechanical perspective using cadavers and surrogate models (see table II).[169-173] Paulos et al.[169,171] and France et al.[170] applied strain gauges to the bone of cadaver knees at attachment sites to determine the forces and joint openings necessary to disrupt the valgum, evaluating the restraining properties of ligaments in braced and unbraced knees. Forces were applied with a hydraulic apparatus and joint openings were measured with a single-axis electropotentiometer. Tests performed on the four braces showed that the mechanical stiffness (ability of a brace to absorb, distribute and transmit the input force and energy) varied 3-fold among the braces. The average stiffness of the unbraced knees at the point of ligament failure was equivalent to 105.8 kN/m ª 2009 Adis Data Information BV. All rights reserved.
compared with 25.1 kN/m for the braces alone. The resting tension in the MCL was increased in 60% of the braced knees, which was attributed to preloading of the ligament. Knees with a slight to moderate varus demonstrated as much as a 160% increase in ligament tension when braces were in place.[170,171] Hoffman et al.[172] reported that PKBs provided increased stability compared with unbraced knees with sectioned ACL and MCL. Baker et al.[173] presented similar data but only when FKBs were applied to the cadaver knee joint. 1.3 Functional Knee Brace Studies
In the 1984 AAOS seminar on knee braces, Paulos and colleagues[174] introduced a classification system for FKBs that included two basic types. The first consisted of the hinge, post and shell, while the second brace type consisted of the hinge, post and straps (see figure 3). The AAOS[151] used this classification for their position statement in defining available brace types. Research on FKB use concentrated on ACL-deficient and non-injured subjects in the following domains: subjective and clinical testing; kinematic testing; ground reaction force (GRF) testing; functional/game-related performance testing. 1.3.1 Subjective and Clinical Assessments
Subjective and clinical reports by brace users were another method employed by researchers to evaluate the efficacy of functional braces. Clinical-based assessments were the first to Sports Med 2009; 39 (11)
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Table II. Summary of cadaver and surrogate models using prophylactic knee braces Study (year)
Brace type
Evaluation
Findings
Paulos et al.[169] (1976)
Four unnamed braces
Applied strain gauges to cadaver knees to determine forces required for MCL disruption
› in resting ligament tension in braced knees, resulting in possible preloading of the MCL
Hofmann et al.[172] (1984)
3D 3-Way, 3D 2-Way, Bledsoe, Universal, ‘Anatomic’ Universal, Knee-Trol
Measurements (displacement) taken by using half pins and an external fixator to the tibia and femur. Tested for anterior, valgus, and rotational stability
All braces provided › in stability compared with non-braced knees with a sectioned ACL and MCL, but did not duplicate natural ligamentous stability
Baker et al.[173] (1987)
2 PKB: Anderson Knee Stabler, McDavid Knee Guard Also tested 5 FKB, results presented in table III
Force transducers applied to the MCL and ACL. Abduction forces (0–30 N) were applied. Data collected at 0, 15 and 30 of knee flexion
No reduction in knee abduction angle with PKB use. With unstable MCL, different braces offered varied protection
Paulos et al.[171] (1987)
McDavid Knee Guard and Omni Anderson Knee Stabler
Conducted static non-destructive (1 mm/sec) and low-rate destructive (76–90 mm/sec) valgus loading. Medial joint opening and ligament injury mechanisms in cadaver knees measured
MCL disruption at higher tensions than ACL and PCL. MCL provided 80% medial restrain, ACL 11%, PCL 9%. Braces tested did not offer protection. Four potential adverse effects reported: (1) MCL preloading, (2) centre axis shift, (3) premature joint line contact, (4) brace slippage
France et al.[170] (1987)
McDavid Knee Guard, Omni Anderson Knee Stabler, DonJoy Knee Guard, Stromgren brace, Mueller brace, and the True-Fit Renegade
Using a surrogate knee model, performed 500 impact tests with and without a knee brace. Knee joint was in full extension or flexed to 30. Limb was in constrained or unconstrained position. Used two valgus impact loads that caused 7 mm (start of MCL damage) and 15 mm (MCL disruption) joint opening. Lateral impact loads of to evaluate: (1) pre-loading, (2) brace performance, (3) ideal brace characteristics
(1) MCL preloading negated by joint compressive forces; (2) one brace exceeded the minimum impact safety factor; (3) ‘ideal’ brace should › lateral absorption rate by 80%
ACL = anterior cruciate ligament; FKB = functional knee brace; MCL = medial collateral ligament; PCL = posterior cruciate ligament; PKB = prophylactic knee brace; › indicates increase.
illustrate statistically significant reduction in anterior tibial displacement and rotatory instability in braced ACL-deficient subjects.[175-177] However, all studies were conducted using low forces and concerns were raised regarding the efficacy of FKBing during application of higher forces to the braced ACL-deficient knee joint. The subjective studies (usually a collection of responses to set questions) gave insight into the capability and the acceptability of the brace(s) being tested by the wearer. Whether these subjective reports were reflective of decreased knee laxity or of performance remain inconclusive, as indicated in table III. 1.3.2 Kinematic Testing
The earliest kinematic studies on ACLdeficient subjects concentrated analysis on three rotations about the knee joint with the use of a ª 2009 Adis Data Information BV. All rights reserved.
3-degrees-of-freedom electrogoniometer. However, the electrogoniometer had inherent restrictions imposed by the electronic cable, the ‘umbilical cord’ between the device and recording unit.[179-183] Three studies used an electrogoniometer to measure three rotations between ACL-deficient and healthy control subjects during running.[181-183] All three studies reported flexion and total varus/valgus motion to be greater in the ACLdeficient group, while internal-external rotation was less. However, none of the differences were found to be statistically significant.[181-183] In an unnamed study identified in Branch and Hunter’s paper,[179] walking analysis was completed on 20 ACL-deficient and 30 control (non-injured) subjects using a goniometric technique whereby 6 degrees of freedom were measured. The results showed no statistical difference between the three Sports Med 2009; 39 (11)
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groups in flexion-extension, varus-valgus, internalexternal rotation, medial-lateral shear or joint compression-distraction. However, statistically significant increases in anterior translation were noted (mean difference of 4.7 mm). Unfortunately, the authors did not provide KT-1000 (MEDmetric Corporation, San Diego, USA) arthrometer measurements (knee joint laxity) or make clear at which walking and/or running phase(s) the increase occurred. This study was replicated using high-speed cinematography and focused on walking, running and stair climbing.[184] Tibone and colleagues[184] reported that the results failed to show any statistical differences. Branch and others[185] (mentioned in Branch and Hunter[179]) using a 3-dimensional tracking system measured compensatory kinematic changes between ACL-deficient subjects and healthy subjects during a side-step manoeuvre. The ACL-deficient subjects kinematics were also analysed using the strap-type DonJoy brace and the shell-type CTi brace. The authors reported that the ACLdeficient group exhibited greater anterior shift of their pelvis, kept their hips less abducted and were more externally rotated during the stance phase compared with non-injured control subjects.[179] Furthermore, the ACL-deficient subjects planted side knee was in greater varus and externally rotated while the ankle was also more externally rotated than the control group. Branch and Hunter[179] concluded that the cumulative external rotation of the hip, knee and ankle in the ACLdeficient group translates to a compensatory early turning of the body towards the cut. However, the data were not statistically significant. As a result, the authors suggested that persons with ACLdeficiency employ a complex set of kinematic adjustments to compensate for knee laxity and thus the above measures may be statistically significant as a set but not individually. Even though the above data were not statistically significant, the authors illustrated that knee brace during running produced statistically significant decreases in knee flexion (22% in the sagittal plane) during the swing phase and 13% during the stance phase. Further-
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more, a 24% reduction in mediolateral/varus-valgus movements as well as a 35% reduction in total tibial rotation was reported. DeVita et al.[186] assessed the biomechanical effects of an FKB2 on kinematics, GRFs and joint moments during the stance phase of running. Two groups were tested, non-injured subjects and ACL-deficient subjects. The latter group was tested with and without an FKB while the non-injured subjects were only tested without the brace. Kinematics analysis exhibited the following results: Bracing did not alter knee kinematics. In comparison with ACL-deficient subjects, non-injured subjects flexed about 8 and 11 more at the hip and knee, respectively, throughout the stance phase. The ACL-deficient group adopted a more erect running style. Vailas and Pink[187] compared performance levels using an unnamed FKB and a placebo knee sleeve on non-injured and ACL-deficient subjects. Statistically significant decreases in torque were found in braced non-injured subjects. Braced ACL-deficient subjects exhibited less torque on the involved limb than on the uninvolved limb. However, no statistical differences were found when the placebo knee sleeve was used by either group and between the braced and unbraced ACL-deficient limb. The authors suggested FKB provided some mechanical restraint to the entire lower extremity instead of just the knee joint. In light of these findings, the authors stated that an FKB should be considered for persons with significant functional ACL deficiency. 1.3.3 Ground Reaction Force Testing
Tibone and colleagues[184] tested 20 subjects with a minimum grade 1+ ACL knee joint laxity (as defined by Arnheim[188]) identified by positive Lachman, anterior drawer, pivot shift and KT1000 testing. Significantly greater vertical GRFs were reported for the involved limb during fast walking and a significantly higher roll-off vertical GRF were noted in the uninvolved limb during
2 Specific knee brace name and manufacturer was not provided. The brace was a strap design and had bilateral posts. The mean weight of the braces was 8.0 N (800 g).
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Table III. Summary of subjective and clinical assessment using functional knee braces Study (year)
Brace type
Evaluation
Findings
Nicholas[150] (1973)
Lenox Hill
52 ACL-deficient subjects
65% of brace users reported instability and not able to return to pre-injury sport
Bassett and Fleming[175] (1983)
Lenox Hill
36 ACL-deficient subjects evaluated anterior drawer and ALRI/AMRI. Subjects also provided subjective feedback
Brace use improved anterior drawer by minimum 1 grade in 81% of the subjects, ALRI improved in 50% of the subjects. Subjectively, 70% of the subjects reported episodes of giving way while wearing the brace; 5% in daily living activities, 8% in recreational sports
Colville et al.[176] (1986)
Lenox Hill
45 ACL-deficient subjects completed clinical tests and provided subjective feedback
Brace failed to significantly fl maximal anterior tibial subluxation. Rotatory instability improved 1 grade with brace use, while varus/valgus laxity remained unchanged. Subjectively, brace use significantly fl episodes of giving way and 69% of subjects reported improved athletic performance. Overall, 91% described the brace as being beneficial
Baker et al.[173] (1987)
DonJoy, Generation II PoliAxial, Lenox Hill, PRO-AM, CTi. Also tested 2 PKBs, results presented in table II
Force transducers applied to the MCL and ACL. Abduction forces (0–30 N) were applied. Data collected at 0, 15 and 30 of knee flexion
A reduction in knee abduction angle with FKB use
Mishra et al.[178] (1989)
Don-Joy Four-Point, RSK, Lenox Hill, and CTi
42 ACL-deficient subjects evaluated by clinical exam and KT-1000 testing. Subjects had used a brace for 1 month
Subjects reported brace migration greatest concern; fl in pain and swelling episodes with brace use. Authors found subjects continued same pre-injury sport participation but for shorter duration
Rink et al.[177] (1989)
CTi, OTi, and Omni TS7
14 subjects arthroscopically proven and conservatively managed ACL. Subjects used each brace for 180–240 hours over 1 month
Subjects reported statistically significant fl in knee instability and pain level with improved activity level; each subject preferring a different brace. Low force KT-1000 tested in significant reduction in anterior tibial displacement
ACL = anterior cruciate ligament; ALRI = anterolateral rotatory instability; AMRI = anteromedial rotatory instability; FKB = functional knee brace; MCL = medial collateral ligament; PKB = prophylactic knee brace; fl indicates decrease.
running. The authors suggested that the increased force during fast walking was an attempt to minimize forces across the ACL-deficient knee joint. The decreased force on the involved knee joint was thought to be related to a midstance subluxation episode. During both the cross-cut and the side-step cut/open cut3 manoeuvres, decreased lateral shear was noted in the injured limb. In addition, vertical force was significantly lower during the side-step test, whereas the antero-
posterior shear was statistically lower during the cross-cut movement. Tibone and colleagues[184] attempted to factor the multiple techniques used to negotiate a cut without subluxing the knee joint by employing a non-dimensional parameter called the ‘cutting index’4 and found significant differences between ACL-deficient and healthy knee joints. The authors suggested that subjects with ACL deficiency utilize a slower approach to the cut, spend more time in the stance (plant)
3 Side-step/open cut involves planting with the reference limb (i.e. the injured limb) and cutting away from the planted limb. ðYÞ ðZ FORCESÞ ðAPPROACH ANGLEÞ 4 Cutting index defined:[184] ðTIMEðXÞ ON FORCE PLATFORMÞ ðAPPROACH TIMEÞ ª 2009 Adis Data Information BV. All rights reserved.
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Knee Bracing in Preventing Knee Ligament Injury
phase of the cut, reduce the angle of the cut and exert less force on the planted leg during the cut. Replicating the study using a custom fitting shelltype FKB (CTi), Cook and colleagues[189] reported the braced ACL-deficient limb had significantly greater shear forces when compared with the same limb unbraced. Furthermore, running velocity increased while wearing an FKB for most athletes, but this result was not statistically significant. As a result, Cook et al.[189] suggested that FKBs allow for significantly better running and cutting performances for athletes with an injured ACL. DeVita et al.[186] reported that an FKB did not affect the GRFs of ACL-deficient subjects running on a flat surface. Persons with ACL deficiency had greater maximum impact force in both conditions (braced and unbraced) than noninjured runners; however, the differences were not statistically significant.
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Five studies reported no significant differences between braced and non-braced groups,[177,178,185,194-195] whereas four studies reported statistically inferior performance measures.[196,197,200-201] Marans et al.[198] found ACLdeficient braced subjects had statistically inferior performance levels in the 40 m sprint but statistically superior performance in the figure-of-eight test. Veldhuizen et al.[199] described that braced subjects had statistically inferior performance levels on the first day of testing, but by day 28, performance was no different between the two testing conditions. However, the continued notion that knee brace use during athletic activity may impair performance by disrupting normal neuromuscular control[179] may be alleviated by the suggestion that brace accommodation is required in order to circumvent neuromuscular disruption and facilitate relearning; otherwise, the brace wearer may risk injury.[3]
1.3.4 Sport-Related Performance Testing
An alternative method to evaluate functional bracing is to examine its impact on athletic performance. Of the first studies to investigate the effect of bracing on motor performance, Corcoran et al.[190] and Reed[191] reported an improvement in walking speed. Both studies, however, were performed with hemiparetic and arthritic subjects, which is only remotely related to athletics and bracing. To date, objective measurement of knee function during athletic performance has been limited to oxygen consumption/expenditure, timed tasks and/or distances during isolated athletic activity (see table IV). Performance assessment has been divided into two categories: either specific running5[179,202] or jumping6[179,202,203] activities. Thirteen studies were examined. The first study used 6 kg weights on each foot while walking at 5.49 km/h and reported a 420% increase in energy expenditure,[192] while Houston and Goenans[193] reported no differences in lower extremity isometric and dynamic strength. However, no statistical analyses were performed in either study.
1.4 Summary of Knee Bracing: 1970 to Mid-1990s
Many brace-effectiveness studies lacked an adequate subject pool to obtain statistically significant results. Other studies had high variance, as the large subject pool had no control population, and were designed to diagnose and/or treat injuries. Furthermore, many studies did not calculate exposure and injury rates and most did not measure knee laxity and/or account for previous injury prior to knee bracing, which could result in higher risk of injury or re-injury. Lastly, some studies did not perform statistical analysis. Although cadaver and surrogate studies provide us with excellent information, the results cannot be equated to on-field performance. There are many other factors (proprioception, reflexes, muscular stability and the athlete’s anticipation to contact) that may help an athlete to avoid serious injury. One study raises the issue regarding validity. Paulos et al.[171] suggested that the
5 Category 1 specific tests include 40-yard dash, shuttle run, figure-of-eight run, stair climb, slalom circuit and cross-cut manoeuvre.[179,202] 6 Category 2 specific tests include one-leg long (horizontal) jump and vertical jump.[179,202,203]
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Table IV. Summary of sport-related performance testing using various knee braces Study (year)
Brace type
Evaluation
Findings
Soule and Goldman[192] (1969)
6 kg weight on each foot
Walked at speeds of 5.49 km/h
420% › in energy expenditure compared to non-weighted walking
Houston and Goenans[193] (1982)
PKB: Lenox Hill, Toronto 2191 and The Kelly
Seven subjects: three with MCL instability, one ACL-deficient, and three with combined ACL and MCL injury. Performed four functional tests (isometric, isokinetic, and maximal knee extension strength tests, stationary bicycle endurance test) over 4 weeks
Isometric strength test, no difference. Dynamic strength testing at 30/sec, braced limb slower; at 300/sec and maximum angular velocity 12–30% slower. Authors concluded that braced subjects were slower, produced less power and produced 41% more lactic acid
Iglehart[194] (1985)
FKB: CTi
Ten non-injured subjects. Three tests performed and three testing sessions; day 1, brace provided, after 280–420 hours of use, after 420–630 hours of brace use
Authors suggested CTi brace use led to no statistical effect on strength and/or motor performance
Tegner and Lysholm[195] (1985)
PBK: ECKO
26 subjects with ACL deficiency and 16 subject post-ACL reconstruction
No significant difference between two groups. › in hop index reported in braced ACL-deficient group; authors suggested was due to › in confidence
Zetterlund[196] (1986)
FBK: Lenox Hill
Ten arthroscopically confirmed ACLdeficient subjects. Subjects used an FKB an average of 23.9 months. Performed treadmill running
After 6 minutes of treadmill running, braced subjects had significantly › levels of oxygen consumption (5.3%) and heart rate (4.3%). No significant difference in ventilation or stride length between the two conditions
Mishra et al.[178] (1989)
4 FKBs used (Don-Joy FourPoint, RSK, Lenox Hill, and CTi)
42 ACL-deficient subjects evaluated by clinical exam and KT-1000 testing. Subjects had used a brace for at least 1 month. Performed 1-legged hop jump and 40-yard shuttle run
Brace use led to fl in the measured pathologic anterior displacement. Improved performance in hop jump only, but not statistically significant
Rink et al.[177] (1989)
2 FKBs (CTi and Omni TS7)
14 arthroscopically proven ACLdeficient subjects performed a figureof-eight test
No significant difference in timed performances in 20-yard and figureof-eight between the two conditions. Authors reported five subluxation episodes with brace use and concluded that there was no advantage to bracing
Unpublished study reported by Branch and Hunter[185] (1990)
FKB: CTi
Ten non-injured subjects used brace for 336 to 420 hours and performed 5 tests.
No statistically significant difference between braced and non-braced conditions
Highgenboten et al.[197] (1991)
4 FKBs (Generation II PoliAxial, Orthotech Performer, CTi, and Lenox Hill Derotation)
14 asymptomatic subjects performed six treadmill runs, at speeds of 9.5 to 12.8 km/h, over 2 weeks.
Significant › in oxygen consumption, heart rate, ventilation between 3% and 8% and › in RPE by 9% and 13%. No data on accommodation over the 2-week testing period
Marans et al.[198] (1991)
6 FKBs (DonJoy Four Point, DonJoy Rotational, Generation II Poly-Axial, Lenox Hill Derotation, McDavid Knee Guard, and Zimmer Double Hinged)
Ten subjects with arthroscopically proven ACL-deficient knee joints. Subjects performed six functional tests
Braced performance level was significantly slower during in the 40 m sprint but faster during figure-of-eight and acute-angle cutting (slalom) tests. Results were brace dependent
Continued next page
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Table IV. Contd Study (year)
Brace type
Evaluation
Findings
Veldhuizen et al.[199] (1991)
PKB: Push Brace Heavy
Eight healthy subjects performed four tests over four durations: (1) 3 days pre-brace application; (2) day 1 of brace use; (3) 28 days after first day of brace use; (4) 1 day post-brace use
Statistically lower performance levels on day 1 of brace use for all tests and no difference after using the brace for 28 days. 1 day after brace removal all test parameters were statistically similar to base values
Styf et al.[200,201] (1992 and 1999)
DonJoy Hinged Neoprene Knee Support, Omni II, and Bell-Horn Knee Sleeve
Eight non-injured subjects used to evaluate brace use and intramuscular pressure
Statistically significant › in intramuscular pressure with use of all three braces
ACL = anterior cruciate ligament; FKB = functional knee brace; MCL = medial collateral ligament; PKB = prophylactic knee brace; RPE = rate of perceived exertion; › indicates increase; fl indicates decrease.
ACL and the posterior cruciate ligament (PCL) disrupt prior to the MCL being torn during valgus loading. However, if this were true, during valgus loading the MCL should never sustain an isolated injury. Also, since the medial meniscus is attached to the MCL, it should not sustain injury during isolated valgus loading. As such, the testing conducted by Paulos and colleagues must have had some limb rotation. All presented studies based on subjective reporting had similar findings. Furthermore, all studies were conducted with high reliability. All performance dynamic/game-like testing research, except that done by Cocorran et al.[190] and Reed,[191] has been conducted with high validity. Of these studies, three provided the greatest insight into how a functional brace may perform during competition.[197,198,201] The one criticism of these studies is that they focused on product testing (of available braces) rather than strictly on athletic performance. Kinematic data has been very valuable as it has allowed researchers to visualize how body segments behave in a particular segment of time. As with kinematic research, force platform studies have also provided excellent visual information on the GRF encountered by the injured or non-injured and the braced and non-braced limbs. Over the last 25 years, the evidence from the review of the literature suggests that FKBs for ACL deficiency may mediate improvements in knee stability and mobility when performing activities of daily living and during certain sporting activities. However, the efficacy of FKBs in preventing knee joint ligament injury remains ª 2009 Adis Data Information BV. All rights reserved.
inconclusive. Few studies have investigated whether apprehension about wearing a brace during athletic activity impairs performance and consequently leads to non-compliance, and this warrants further investigation. 2. Knee Bracing: Mid-1990s to Present By the mid-1990s, female participation in US collegiate and high school athletics experienced a respective 5- to 10-fold increase, with concomitant increases in ACL injuries.[53,54] During the same time period, a rapid rise in ACL injuries in female sports was noted.[53,54] This fuelled intense ACL research in three specific areas: 1. identifying the mechanisms responsible for the high incidences of non-contact knee ligament injuries; 2. investigating the potential benefit of FKBing for ACL deficiency; 3. investigating whether FKBs are beneficial post-ACL reconstruction. In a survey of brace prescription patterns, 97% of orthopaedic surgeons reported that they prescribe braces to their ACL-deficient and ACLreconstructed patients,[204,205] many of whom continue to report positive subjective feedback with their use.[155,177,178,198,206-208] The lack of supportive scientific evidence that FKBs may be beneficial during athletic participation[155,206-211] or prevent knee ligament injuries remains contentious.[32,204,208,210-213] Moreover, the biomechanical evidence on the effects of PKBs on preventing MCL injury remains ambiguous.[156,214] Sports Med 2009; 39 (11)
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2.1 Knee Bracing Studies
Of the 15 studies analysed, seven evaluated knee brace use on subjects with ACL deficiency,[104,215-220] three assessed brace performance after ACL reconstruction,[221-223] and the remaining five tested brace use on non-injured subjects[212,224-227] (table V). These five studies used non-injured subjects; one used a ‘sleeve-type brace’,[224] the second study did not perform functional/dynamic testing,[212] the third used an unnamed PKB,[226] the fourth study evaluated a newly designed functional brace,[227] and the fifth screened over 9000 professional skiers to evaluate the potential benefit of bracing.[225] However, none addressed the effectiveness of an FKB to possibly prevent a ligament injury and/or the impact on performance hindrance. Of the seven studies involving braced ACL-deficient subjects, five reported statistically improved performance levels,[217-220,228] whereas two reported no performance differences between nonbraced and braced ACL-deficient groups.[215,216] Performance differences were no different between ACL-reconstructed braced and non-braced groups.[221,223] Wu et al.[222] suggested that both FKB- and placebo-braced subjects may have improved static knee joint proprioception but not muscle functioning. Of the five studies that examined braced non-injured subjects’ performance levels, one recorded an 11% improvement in joint proprioception[224] and one found that braced subjects exhibited significantly reduced anterior shear loads.[212] Kocher et al.[225] found that a significantly higher proportion of non-braced skiers sustained an ACL injury and they had a higher risk of re-injury post-ACL surgery when not wearing a brace. Culp et al.[226] observed that although PKBs have no proprioceptive benefits, they may assist in absorbing externally applied forces. The study by Yu et al.[227] found a newly designed FKB had no effect on peak ground reaction forces during the stop-jump task. 2.2 Functional Knee Bracing and Game-Related Performance Testing
Three studies investigated FKBing on noninjured subjects (see table VI). ª 2009 Adis Data Information BV. All rights reserved.
Stephens[229] found no statistical differences in straight line and successive turning running activities among collegiate basketball players using two different FKBs. Two studies evaluated athletes’ speed and agility,[154,215] and one study measured brace tendency to migrate (brace movement in the horizontal and/or vertical planes) in dynamic/game-like settings.[154] Testing six FKBs during the 40-yard dash (speed) and the fourcone drill (agility) tests, the authors[154] reported that performance levels were statistically hindered while using two of the six FKBs in the speed test. During the agility drill, performance levels decreased only when wearing one of the six FKBs, leading Greene et al.[154] to suggest that FKBs do not significantly reduce speed and agility. However, all braces tended to migrate, potentially affecting protective function and athletic performance. To investigate whether braces worn during athletic activity hindered performance, 30 non-injured subjects performed five functional tests with and without an FKB.[215] During the brace accommodation phase, the braced group demonstrated statistically inferior performances during the 10 m dash, figure-of-eight and slalom tests, and a statistically superior performance in the horizontal hop test. When running down stairs, no statistical differences were noted between conditions. However, once subjects had accommodated to the brace (best performance measures), no significant differences were noted between the braced and non-braced conditions for any of the tests.[215] 2.3 Summary of Knee Bracing: Mid-1990s to Present
According to Marans et al.,[198] the degree of objective instability found by clinical testing has never been correlated to the degree of functional instability (instability during daily and sporting activities) that one experiences as a result of an ACL injury. While many studies have concentrated their research on the effectiveness of one type of brace or on a comparison between available braces,[198] or have focused on ACLdeficient subjects or subjects with surgically reconstructed ACLs,[230] these studies have Sports Med 2009; 39 (11)
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Table V. Summary of knee brace studies, mid-1990s to present Study (year)
Brace type
Evaluation
Findings
McNair et al.[224] (1996)
Knee sleeve type brace
20 subjects with no musculoskeletal or neurological deficit performed tracking task on Kin-Com. Angle and force data sampled using electrogoniometers
Improvement of 11% in tracking while using the knee sleeve
Wojtys et al.[228] (1996)
Six FKBs (Bledsoe Proshifter, Generation II, Poli-Axial, Lenox Hill Spectralite, Townsend, Sutter Telon, CTi)
Five arthroscopically confirmed ACL-deficient subjects. Assessed effects of FKBs on anterior tibial translation, isokinetic performance and neuromuscular function
Braced subjects had significantly fl anterior tibial translation with and without muscle activation. Also, spinal level reaction time improved for quadriceps but not for hamstrings
Risberg et al.[221] (1999)
DonJoy rehabilitation brace followed by FKB, DonJoy Gold Point
60 subjects post-ACL reconstruction followed for 2 years. 30 subjects per braced and non-braced group. Measured knee laxity, Cincinnati knee score, ROM, thigh atrophy, isokinetic testing, three functional knee tests, and visual analog scale to evaluate pain
No significant disparity in knee joint laxity, ROM, muscle strength, functional knee testing, or pain between groups. Cincinnati score showed significantly › functioning at knee function at 3-month follow-up even with significant thigh atrophy
Fleming et al.[212] (2000)
FKB: DonJoy Legend
15 non-injured subjects with arthroscopically proven intact ACL. Evaluated the ACL strain response in braced and unbraced knees during nonand weightbearing in combination with (1) anterior-posterior shear forces, (2) internal-external torques, and (3) varusvalgus moments external applied loads.
1) A-P forces: Brace significantly fl strain on anterior shear loads up to 130 N during non- and weightbearing 2) I-E torques: Braced knee had statistically fl strain (up to 9 Nm) in nonweightbearing 3) Brace did not significantly fl external (up to 9 Nm) and varus-valgus (up to 10 Nm) moments
Rishiraj et al.[215] (2000)
FKB: Generation II PoliAxial
30 ACL-deficient (grade 2, KT-1000 evaluated) subjects. Subjects performed five functional tasks
Braced group performance › by 1.1–6.5% in speed and agility events and 1.8–4.4% in the hop test. Results were statistically non-significant
Wu et al.[222] (2001)
FKB: DonJoy Legend and a mechanical placebo brace
31 subjects post-ACL reconstruction, minimum 5 months post-surgery. Evaluated subjects’ ability to accurately reproduce specified knee joint angles and knee joint isokinetic performance at 60 and 180/sec
Compared with non-braced, braced and placebo braced subjects may improve static knee joint proprioception but not muscle functioning.
Ramsey et al.[216] (2001)
FKB: DonJoy Legend
Six ACL-deficient subjects evaluated with grade 2 Lachman test and KT-1000 testing results of 4.5–9.0 mm. Assessed knee kinematics during horizontal hop jump using Steinmann traction pins
Bracing produced minor and inconsistent reduction in anterior tibial translations during hop jump
Beynnon et al.[217,218] (2002 and 2003)
Two FKBs: DonJoy Legend, SofTec Genu and Townsend Rebel
Nine subjects with chronic ACL-deficient knees. A-P shear and compressive loads applied to the knee, and tibial translation measured in nonweightbearing, throughout the transition to weightbearing, and during weightbearing
Bracing resulted in a significant fl of A-P laxity values, to within limits of the normal knee during non-weightbearing and weightbearing postures, but not during transition from nonweightbearing to weightbearing. Latter anterior translation › 3.5 times more than in the normal knee
Kocher et al.[225] (2003)
Various knee braces, specific names not identified
9410 professional skiers screened (1991–1997) and 180 ACL injuries reported. ACL-deficient knee was defined by an abnormal Lachman or
Significantly higher proportion of non-braced skiers sustained ACL injury. Risk ratio of 6.4 (13% and 2%, respectively) for subsequent knee Continued next page
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Table V. Contd Study (year)
Brace type
Evaluation
Findings
pivot-shift and a 5 mm or greater KT-1000 manual maximum laxity
injury between non-braced and braced skiers. Univariate analysis revealed no significant effects of the other covariates Significant › in rectus femoris activity on landing only one subject demonstrated › anterior drawer. Authors suggested joint stability may result from proprioceptive feedback rather than the mechanical stabilizing effect of the brace
Ramsey et al.[219] (2003)
FKB: DonJoy Legend
Four ACL-deficient subjects with +2 Lachman performed horizontal hop jump. Recorded EMG and simultaneous tibiofemoral kinematics data to investigate the effect of the brace
Smith et al.[220] (2003)
FKB: CTi
Ten individuals with chronic ACL-deficient knee performed three single-leg hop manoeuvres on their ACL-deficient knee with and without a knee brace. Recorded EMG data
Brace significantly delayed average vastus lateralis onset before landing. Non-braced, 5 of the 10 subjects activated hamstrings or gastrocnemius muscles first. Braced, 7 of 10 activated same muscles first. Authors suggested multiple strategies may exist to stabilize the braced ACL-deficient knee
Culp et al.[226] (2004)
PKB: unnamed
20 non-injured males performed repeated double leg squats, held position for 10 sec and repeated movement to failure
Prophylactic knee bracing had no proprioceptive affect on the knee. Authors concluded, bracing may absorb external loads
McDevitt et al.[223] (2004)
FKB: DonJoy IROM
100 subjects post-ACL reconstruction followed for 2 years. Braced group used brace post-surgery. Non-braced and braced data collected during cutting, pivoting, jumping and strength test activities
No significant difference in knee stability between groups in single-leg hop test, Lysholm scores, knee ROM or isokinetic strength testing. Two braced and three non-braced subjects reinjured ACL
Yu et al.[227] (2004)
FKB: Newly designed DonJoy 4titude
20 non-injured subjects. Performed non-braced and braced stop-jump task
New knee brace fl knee flexion by 5 but did not significantly affect peak ground reaction forces while performing a stop-jump task
ACL = anterior cruciate ligament; A-P = anterior-posterior; EMG = electromyogram; FKB = functional knee brace; MCL = medial collateral ligament; PKB = prophylactic knee brace; ROM = range of motion; › indicates increase; fl indicates decrease.
provided insight into the potential stabilizing effects that FKBs may offer the ACL-deficient population, and the potential stabilizing/injury protection they may offer to non-injured individuals. Given the limited amount of research involving braced non-injured subjects, it appears that familiarization/accommodation may be required before performance equals that of nonbraced non-injured subjects.
3. Conclusions and Recommendations An extensive review of the literature on ACL injury yielded more than 2000 papers published over the last decade.[109] Much of the research has ª 2009 Adis Data Information BV. All rights reserved.
concentrated on injury mechanisms as identified by Bahr and Krosshaug,[231] McIntosh[232] and Meeuwisse,[233] and thus far, although promising, no conclusive information or preventative strategies have been identified to decrease the rate and/ or severity of ACL injury; several authors have suggested that further research is necessary.[30,32] Also, no research has been conducted on the high percentage of basketball non-contact ACL injuries experienced by males,[148] and there should be concern regarding the high number of contact ACL injuries associated with soccer (for both men and women),[18,19] ice hockey[4] and football.[13] The recent AAOS[153] position paper and several studies have illustrated that knee braces generally provide 20–30% greater knee ligament Sports Med 2009; 39 (11)
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Table VI. Summary of functional knee brace (FKB) studies on non-injured subjects performing game-related activities mid-1990s to present Author(s)
FKB type
Evaluation
Findings
Stephens[229] (1995)
DonJoy GoldPoint and Omni OS-five knee braces
25 non-injured basketball players completed 2 days of running trials
No significant difference in straight line or successive turning running times between non-braced and braced testing conditions
Greene et al.[154] (2000)
Air Armor, Knee and Thigh Protection System, Berg Tradition, DonJoy Legend, McDavid Knee Guard, OMNI-ASK 101 W
30 Phoenix Junior College football players with no history of knee injury
Performance statistically not hindered while using two of six knee braces in the 40-yard dash and five of six braces during agility test. All braces had M/L and D/P had migration concerns, with only some data being statistically significant
Rishiraj et al.[215] (2000)
Generation II Poli-Axial brace
30 university athletes with no known history of knee injury. Knee joint laxity quantified using KT-1000. Performed five functional tests
Day 1 of testing: braced subjects had statistically inferior performance levels in three of five tests, enhanced performance in horizontal hop-test, and no significant difference in running down the stairs test. After brace accommodation, no significant difference between the two testing conditions in all tests
D/P = distal/proximal; M/L = medial/lateral.
protection.[9,52,82,156,157,168] In light of information presented in this paper, the application of an FKB may help to disperse GRF and/or forces from direct impact and/or to stabilize the knee joint complex. If a brace is able to offer ‘protection’, then we may not only see a reduction in knee injury severity, but possibly also a decrease in the rate of knee injuries. All injury prevention mechanisms that protect knee joint ligaments need to be investigated.[231] In particular, FKBs worn during sport competition warrant further study. Compliance, however, is an issue among non-injured athletes; when braces are worn during competitive activity, they have been shown to be related to fear of performance hindrance.[52,153-157] The results of brace accommodation are encouraging,[154,215,229] but further research is needed before performance hindrance fears are alleviated. Once this is addressed, only then can the efficacy of FKBs in preventing knee injuries during athletic performance be evaluated. Acknowledgements No funding was received for this review. The authors have no potential conflicts of interest directly relevant to the content of this review. The authors would like to thank K. (Janey) Hoover for helping with the earlier versions of this manuscript.
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Correspondence: Neetu Rishiraj, ACTIN Health & Rehabilitation Inc., 5767 Oak Street, Vancouver, BC, Canada. Email:
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Sports Med 2009; 39 (11)
Sports Med 2009; 39 (11): 961-975 0112-1642/09/0011-0961/$49.95/0
REVIEW ARTICLE
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Physical Activity and Preterm Birth A Literature Review Marlos Rodrigues Domingues, Alicia Matijasevich and Aluı´sio J.D. Barros Post-Graduate Program in Epidemiology, Federal University of Pelotas, Pelotas, Brazil
Contents Abstract. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Reviewing Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Recommendations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Physical Activity Studies and Preterm Birth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1 Occupational Physical Activities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2 Fatigue and Job Satisfaction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3 Leisure-Time Physical Activities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4 All-Domain or Other Physical Activities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Limitations Found in the Reviewed Literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. Physiological Aspects of Physical Activities in Pregnancy. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6. Physical Activity and Preterm Birth: Considerations. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Abstract
961 962 962 963 963 966 967 969 970 970 971 972
Preterm birth is a major reason for infant mortality and morbidity, representing a public health concern worldwide. Regular and voluntary physical activity is healthy behaviour that should be incorporated by everyone, including pregnant women. On the other hand, some women are exposed to highly demanding occupational physical activities during pregnancy that might represent a threat to the fetus and to their own health. This paper is a literature review of studies (1987–2007) on physical activity during pregnancy and its relationship to preterm birth. Although the effects measured by the studies are not strong and the evidence is impaired by many methodological flaws, it seems that recreational or leisure-time physical activities performed regularly provide protection against prematurity. Studies on occupational physical activities, especially standing for long periods, present contrasting results – some presenting standing as a risk factor, but most showing no association. Housework and other daily activities do not seem to be associated with preterm birth. Regardless of the methodological aspects of the studies reviewed, there is a chance that the real effect of occupational physical activity is being blurred by some underlying factors not easily measured in epidemiological investigations. Our conclusions do not reject the idea that working conditions might represent danger for the pregnancy outcome, but only raise the question that maybe the mechanisms through which employment-related physical activities have been considered up till now could be better and more thoroughly studied. Future studies should pay additional attention to psychological and socioeconomic characteristics, without neglecting biological plausibility.
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Gestational age is known to be one of the most important predictors of an infant’s subsequent health and survival.[1] The incidence of preterm birth (birth before 37 weeks of gestation) ranges from 5% to 7% of live births in most developed countries and up to 25% in developing nation settings.[2] There is also evidence that preterm birth rates have been rising fairly steadily in the past few years in many countries, and therefore it represents a major public health concern.[3-6] Information available on risk factors associated with preterm birth considers individual-level behavioural and psychosocial factors, environmental exposures, medical conditions, infertility treatments, biological factors and genetics.[6-9] Even though in a high percentage of preterm births the aetiology cannot be positively defined, several maternal aspects have been thought to contribute to preterm birth. Poor socioeconomic status, maternal malnutrition, illiteracy, extremes of maternal age and cigarette smoking are the main non-obstetric risk factors identified.[10-12] In addition, cervical incompetence, multiple gestations, short birth intervals, premature membrane rupture and previous preterm birth are some of the obstetric risk factors that have been associated with preterm birth.[7-9] Other medical conditions such as urinary and genital tract infections and history of adverse pregnancy outcome have also been associated with preterm delivery.[13,14] Another factor to consider is that the higher medicalization of pregnancy and childbirth may increase the chance of iatrogenic preterm deliveries.[15] Maternal psychological profile plays a role in preterm birth determination: stress, anxiety and depression are frequently associated with prematurity.[16-18] Moutquin suggests that infection is mostly responsible for extreme preterm birth, while stress and lifestyle influence mild preterm birth, and a mixture of both conditions contributes to extreme preterm birth.[19] The preterm birth rates seem to be on the rise as there are more nearterm babies (34–36 weeks).[20] These deliveries often are preceded by labour induction in women with conditions such as hypertension and diabetes mellitus.[21] ª 2009 Adis Data Information BV. All rights reserved.
Over the last decades an increasing interest in physical activity during pregnancy resulted in several studies evaluating the impact of active lifestyles and occupational physical tasks on pregnancy outcomes such as birthweight and prematurity. The aim of this paper is, based on a literature review, to explore potential relationships between physical activity and preterm birth. Special attention is devoted to the contrasting physiological aspects regarding occupational and leisuretime physical activities. 1. Reviewing Methods We conducted a search for papers published between 1987 and November 2007 in English, Portuguese or Spanish that studied preterm birth as the main or secondary outcome and considered some kind of physical activity as an exposure. The databases searched were: MEDLINE, Lilacs, MedCarib, CiteBase, Paho, Cybertesis, ProQuest Dissertation Library, Syracuse University Library, Popline and EMBASE. Main search terms (or a combination of terms) were ‘Preterm’, ‘Premature’, ‘Prematurity’, ‘Physical Activity’, ‘Exercise’, ‘Occupation’, ‘Work’, ‘Occupational’, ‘Birth’ and ‘Delivery’. References from retrieved papers were searched to identify additional references. In addition, we contacted several authors to obtain reprints and information about unpublished material. Four studies published before 1987 were also included due to their frequent citation in studies within the time range of this review. Some review papers were reference sources during our search and reviewers’ commentaries were evaluated. 2. Recommendations Currently there is no guideline concerning the most appropriate physical activity to be performed throughout gestation: only some precautions are advocated. Pregnant women and physicians must consider the same precautions taken with nonpregnant populations besides relying on common sense and bearing in mind past activities Sports Med 2009; 39 (11)
Physical Activity and Preterm Birth
performed. Women should avoid activities with potential risk of trauma, like horseback riding and contact sports.[22] Scuba diving is another activity to be avoided since there is a chance of adverse outcome because the fetus is not protected from decompression problems and is at risk of malformation and gas embolism after decompression disease.[23] When exercising lying on the ground, women must be advised to avoid the supine position, especially during the second and third trimesters. Because of the increased uterus weight, this posture might result in vena cava compression, compromising venous return and possibly decreasing cardiac output and blood pressure – a situation known as supine hypotensive syndrome.[24] 3. Physical Activity Studies and Preterm Birth We reviewed 47 papers on this subject, besides complementary literature, to help us understand the relationship between physical activity and preterm birth. Basically, three study types were available discussing physical activity and preterm birth: (i) occupational physical activity; (ii) leisure-time physical activity; and (iii) all-domain physical activity (or a mixture of several activities). We could identify 25 papers dealing exclusively with occupational exposures (table I), six limited to leisure-time physical activity (table II), and 16 studies that evaluated both occupational and leisuretime activities or all-domain physical activity assessments (table III), including housework and other daily activities. 3.1 Occupational Physical Activities
Prolonged standing is by far the most investigated occupational activity regarding preterm birth. From the 41 studies assessing occupational exposures, 27 evaluated standing postures. Five studies found that standing at work was a risk factor for preterm birth, showing results varying from odds ratio (OR) = 1.26 (95% CI 1.1, 1.5) in a multicentre case-control study by Saurel-Cubizolles et al.[47] that defined standing as >6 daily hours to OR = 4.10 (95% CI 1.29, 13.10) in ª 2009 Adis Data Information BV. All rights reserved.
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Ritsmitchai et al.,[66] a case-control study with lowschooling Thai women that considered standing when women stand for at least 3 hours per day. Small numbers in the Ritsmitchai et al. study may have hindered the adjusted analysis, for example, from the 223 cases; only 32 women were exposed to standing during pregnancy and only five women belonged to the higher schooling category. The remaining 22 studies found no significant associations between prematurity and standing at work. Lifting activities have been assessed and discussed in prematurity, fetal growth and birthweight studies.[30,58,62-65,67,71] With respect to lifting weights and prematurity specifically, Ahlborg et al.[58] found that lifting (‡12 kg) more than 50 times a week increased the chance of preterm birth only among women who stopped working before the 32nd week of gestation. The same was found by McDonald et al.,[30] who reported that lifting heavy weights more than 15 times a day was only a risk factor for women who stopped working before the 28th week of gestation. This relationship could be an example of reverse causality often left out in the discussion of several such papers. Ahlborg et al.[58] argued that perhaps cervical insufficiency could be triggered by lifting weights among susceptible women and that such women could leave work earlier because of symptoms or a previous preterm delivery experience. Leaving out these subgroup analyses, we did not find evidence that lifting heavy weights per se would provoke any kind of adaptation known to be highly related to prematurity. Berkowitz et al.,[56] Fortier et al.[65] and Koemeester et al.[64] studied both leisure-time physical activity and occupational physical activity, finding no association between occupational activities and preterm birth. Different results might be due to contrasting definitions. In terms of exposure definition, the main occupational exposure – standing – is categorized by some papers as yes/no,[36] below or above 3 hours,[66] below or above 8 hours,[30] or in three,[47] four[59] or five categories.[68] Some use weekly exposure[68,71] while most use daily measures. These disparities reinforce the difficulty in Sports Med 2009; 39 (11)
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ª 2009 Adis Data Information BV. All rights reserved.
Table I. Studies evaluating exclusively occupational physical activities (PA) and preterm birth (PB) Study design (no. of subjects)
Physical activity
Effect/conclusions (OR; 95% CI)
Limitations
Mamelle et al.[25] (1984)
Retro (1928)
Fatigue scorea
Physical exertion increases the risk of prematurity (1.7; 1.1, 2.0). Mental stress was associated with PB (1.8; 1.1, 2.2)
Saurel-Cubizolles et al.[26] (1985)
Retro (621)
Standing, carrying heavy loads and heavy cleaning tasks
Zuckerman et al.[27] (1986)
Retro (1507)
Standing
Higher PB rate among cleaners, cooks, etc. and in the presence of at least two of the arduous conditions: standing, carrying heavy loads and heavy cleaning No association
Fatigue score is not specific for PA, as it considers mental stress and many different aspects of the environment such as cold, noise, gases, chemical manipulation and wet atmosphere Poor statistics
Saurel-Cubizolles and Kaminski[28] (1987)
Retro (2387)
Standing, heavy load carrying and physical effort
Mamelle and Munoz[29] (1987)
CC (600)
Fatigue scorea
McDonald et al.[30] (1988)
Retro (22761)
Standing, lifting, physical efforts and fatigue scorea
Hartikainen-Sorri and Sorri[31] (1989)
CC (568)
Homer et al.[32] (1990)
Pro (773)
Heavy physical load, standing and an industrial classification based on job type Physical exertion based on job title
Teitelman et al.[33] (1990)
Pro (1206)
Job classification in three groups: standing, active or sedentary
Standing jobs associated with PB (2.72; 1.24, 5.95)
Ramirez et al.[34] (1990)
CC (6674)
Low, medium, moderately heavy, heavy or very heavy according to woman’s military occupation
Women employed in the highest levels of physical effort were at higher risk of PB (1.75; 1.12, 2.75)
PB was more common among women who stand, carry heavy loads and had considerable physical effort Work on machines (1.7; 1.01, 2.90) and mental stress (1.5; 1.03, 2.30) associated with PB. Physical exertion and posture not associated with PB Lifting associated with PB only among women who stopped working before the 28th week of gestation No association
High exertion jobs associated with PB (RR = 2.0; 1.2, 3.9)
Standing measurement based only on job title, gestational age evaluated as a mean value (no evaluation of PB as a dichotomous outcome) No control for confounders and poor statistics No control for confounding. Fatigue score is not appropriate for PA measurement
Misleading writing and analysis
Long period between delivery and interview (1 year), voluntary participation
Selection bias (sample comprised young minority women socioeconomically disadvantaged). PB estimated as birth >3 wk earlier than expected date Voluntary participation, selection bias, not every woman was interviewed at the same time, some in the first trimester and the rest were interviewed by the 20th week of gestation Some known confounders were not considered, representativeness of the sample, PA measurement, missing data
Continued next page
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Sports Med 2009; 39 (11)
Study (year)
Study design (no. of subjects)
Physical activity
Effect/conclusions (OR; 95% CI)
Limitations
Klebanoff et al.[35] (1990)
Retro (2227)
Residency (female physicians, and wives of male physicians) occupation compared with other occupations
No association
Saurel-Cubizolles et al.[36] (1991)
Retro (875)
Occupational group (skilled or unskilled) was associated with PB, but not working conditions
Magann and Nolan[37] (1991)
CC (1549)
Peoples-Sheps et al.[38] (1991)
Retro (2711)
Luke et al.[39] (1995)
CC (1470)
Standing, lifting, other arduous positions and a combination of the three factors Occupational routine activities of the military Based on job title, classified into sedentary, light, medium, heavy or very heavy Physical exertion at work, standing and fatigue scorea
Long recall time, voluntary participation. The authors were unaware of the exposures among physicians’ wives. Authors discuss potential harms of OPA based on other studies (with no direct measurement) None
Savitz et al.[40] (1996)
Retro (7903)
Based only on job title
No association
Cero´n-Mireles et al.[41] (1996)
Retro (2663)
Standing and job’s physical effort
No association
Tuntiseranee et al.[42] (1998)
Pro (1797)
No association
Tuntiseranee et al.[43] (1999)
Pro (1797)
No association
Selection bias, poor measurement of PA
Escriba`-Agu¨ir et al.[44] (2001)
CC (576)
Physical job demand (low, moderate or high) Physical job demand (low, moderate or high) Standing, bending, kneeling, squatting, holding arms above shoulders and load carrying
Voluntary participation, high refusal rate. No adjusted data for standing and physical exertion High nonresponse rate (35%), long period (>1 y) between delivery and interview Women who stopped working due to medical problems were excluded, physical effort variables not well defined PA poorly measured
High physical exertion associated with PB (2.31; 1.43–3.73)
Newman et al.[45] (2001)
Pro (2929)
Fatigue scorea
Small sample size for the subgroup analysis might have biased results, women with some condition that excluded them from work were not included Fatigue score is not specific for studying PA
Henrich et al.[46] (2003)
CC (707)
Standing, turning, bending, kneeling, holding arms above shoulders and load carrying
No association No association
Fatigue score (above 3) associated with PB (OR = 1.4)
Spontaneous PB was associated with fatigue score only among nulliparous women No association
No direct measurement of activities, no control for confounding One year between deliveries and interviews, voluntary participation, PA measured indirectly
No control for confounders, inappropriate statistics and misleading writing
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Study (year)
Physical Activity and Preterm Birth
ª 2009 Adis Data Information BV. All rights reserved.
Table I. Contd
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ª 2009 Adis Data Information BV. All rights reserved.
Based on standing, work on industrial machines, physical exertion, mental stress and environmental conditions.
CC = case-control; OPA = occupational physical activities; OR = odds ratio; Pro = prospective; Retro = retrospective; RR = relative risk.
a
Small sample size, unclear and unusual definition of variables Anxiety (2.16; 1.28, 3.64) and manual work (1.70; 1.02, 2.84) associated with PB Manual work (heavy or usual) CC (400) Al-Dabbagh and Al-Taee[49] (2006)
Poor measurement of PA, representativeness of the sample Farm workers (4.2; 2.8, 6.4) and women with physical work (2.4; 1.8, 3.3) were at higher risk for PB Occupation divided into: farmers; officials or private business or students; housewives Retro (1709) Nguyen et al.[48] (2004)
None Risk factors for PB: stand >6 h/day (1.26; 1.1, 1.5), low job satisfaction (1.27; 1.1, 1.5), work >42 h/wk (1.33; 1.1, 1.6) Standing, bending, twisting, kneeling, squatting, holding arms above shoulder level and carrying heavy loads CC (6467)
Limitations
Saurel-Cubizolles et al.[47] (2004)
Table I. Contd
Physical activity Study design (no. of subjects) Study (year)
Effect/conclusions (OR; 95% CI)
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comparing the results from such a pool of information. In a multicentre study[47] countries with better health conditions presented higher associations between job satisfaction and preterm birth. Conversely, as the health condition of the country decreased, the associations weakened. The same study showed that, although standing was associated with preterm birth, job dissatisfaction and long working hours presented higher odds ratios. The authors concluded that conflicting results from studies on this topic are probably due to social and legislative issues, and while a multicentre study is a unique chance to evaluate different working conditions, they also believe that contrasting work-related policies (i.e. ‘workleaves’ – when a pregnant woman stops working due to a health problem) play a role in the determination of pregnancy outcomes.
3.2 Fatigue and Job Satisfaction
Studies that evaluated pregnancy work-leaves have shown a protective association with preterm birth,[72] although it is not clear whether occupational physical activity or psychological aspects of work are making the difference. Long working hours[25,30,39,47] and shift working[71] have also been linked to preterm birth as job dissatisfaction.[46,47] Women who did not want to remain in the workforce also presented higher risks of prematurity,[73] suggesting that psychological aspects and personal fulfilment probably influence preterm birth occurrence. One of the first studies on the subject, by Mamelle et al.,[72] evaluated women from factories working under strenuous conditions, and found that work-leaves conceded, especially for fatigue (without any pathological reason), were protective against preterm birth. The protective effect of work-leaves on preterm birth seen in these studies may be an underestimate, since work-leaves may indicate pregnancy illness highly related to adverse late pregnancy outcomes. Cero´n-Mireles et al.,[41] studying Mexican women, showed that workleave was a risk factor for preterm birth, while the Sports Med 2009; 39 (11)
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Table II. Studies evaluating exclusively leisure-time physical activities (PA) and preterm birth (PB) Study (year)
Study design (no. of subjects)
Physical activity
Effect/conclusions (OR; 95% CI)
Limitations
Hall and Kaufmann[50] (1987)
Pro (845)
Categories based on frequency of exercise (treadmill, cycling and resisted training)
No association
Small sample size, no control for confounders, self-selection bias
Clapp[51] (1990)
Pro (131)
Running and aerobics classes
No association
Small sample size, selection bias
Hatch et al.[52] (1998)
Pro (557)
Intensity codes (kcal/min) and classified as no exercise, low-moderate exercise or heavy exercise
Heavy exercise reduced PB risk (0.11; 0.02, 0.81). Less intense exercise did not affect gestational length
Voluntary participation
Hanson[53] (2001)
Pro (922)
Four categories: no exercise, strenuous exercise, nonstrenuous exercise and non-strenuous and strenuous exercise
No association
Selection bias
Evenson et al.[54] (2002)
Pro (1699)
Vigorous leisure activities performed before and during pregnancy (1st and 2nd trimester), frequency and duration for each period
Vigorous leisure activities in the 1st and even more in the 2nd trimester was associated with a reduced (but nonsignificant) risk of PB and spontaneous PB
No assessment of lightto-moderate physical activities, self-selection (to engage in vigorous activities)
Leiferman and Evenson[55] (2003)
Retro (9089)
Exercise or sports at least 3 times a week during pregnancy (yes/no)
No association
Poor assessment of PA, long interval between interview and birth (average of 17 months), voluntary participation
OR = odds ratio; Pro = prospective; Retro = retrospective.
ability to rest in the antenatal period was protective for preterm birth. 3.3 Leisure-Time Physical Activities
Studies that evaluate leisure-time physical activities typically collect information about the usual patterns (frequency, duration and intensity) and type of activity performed. Most of these studies were performed among voluntary women. The most common modalities assessed were: walking, swimming, cycling, running, weight-training, water exercises, dancing and aerobics classes. Clapp[51] found that, after 37 weeks of gestational age, active women deliver on average 6 days earlier if exercise is continued throughout ª 2009 Adis Data Information BV. All rights reserved.
late pregnancy, but no association with preterm birth was found. Hatch et al.[52] divided exercisers into low-moderate exercisers and heavy exercisers, finding that heavy exercise (above 1000 kcal/week of energy expenditure) reduced preterm birth risk, while less intense exercise did not affect gestational length. Evenson et al.[54] evaluated the role of vigorous recreational activities during the first and second trimester and preterm birth, finding nonsignificant protective effects (OR 0.80 and 95% CI 0.48, 1.35; OR 0.52 and 95% CI 0.24, 1.11, respectively). In one of the earliest studies to consider leisure-time physical activity, Berkowitz et al.[56] analysed sports activities during pregnancy and reported a protective effect of sports/exercise for Sports Med 2009; 39 (11)
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Table III. Studies evaluating simultaneously occupational, leisure-time or other physical activities (PA) and preterm birth (PB) Study design (no. of subjects)
Physical activity
Effect/conclusions (OR; 95% CI)
Limitations
Berkowitz et al.[56] (1983)
CC (488)
Standing, carrying, lifting, housework, daily use of stairs and sports/exercises
Small sample size. Standing or moving around combined
Launer et al.[57] (1990)
Pro (15786)
Ahlborg et al.[58] (1990)
Pro (3906)
Household chores, type of work (office or manual) and position at work (standing, sitting or walking) Lifting
Sports/exercises decreased the chance for spontaneous PB (0.53; 0.36, 0.78). No association for other activities Standing (compared with sitting) was a risk for PB (1.56; 1.04, 2.60)
Klebanoff et al.[59] (1990)
Pro (7101)
Standing, heavy work/exercise and light work/exercise
Barnes et al.[60] (1991)
Pro (2741)
Household work and paid work (time and energy expenditure)
Hickey et al.[61] (1995)
Pro (1368)
Housework, recreational activities and fatigue scorea
No association
Florack et al.[62] (1995)
Pro (128)
No association
Henriksen et al.[63] (1995)
Pro (4259)
Standing, walking, bending, lifting, housekeeping and fatigue scorea Lifting, standing, walking at work and LTPA
Koemeester et al.[64] (1995)
Pro (116)
Walking, lifting, standing, bending, squatting, number of sports activities
Fortier et al.[65] (1995)
Retro (4390)
Ritsmitchai et al.[66] (1997)
CC (446)
Standing, lifting and perception of physical effort, housework and LTPA (energy expenditure) Lifting, carrying loads, standing, walking, sitting and physical exercise
Alderman et al.[67] (1998)
Retro (291)
Sports, housework and job vigorous activities (lifting, digging, carrying)
Lifting associated with PB only among women who stopped working before the 32nd week of gestation Standing associated with PB (1.31; 1.01, 1.71), heavy work/exercise not associated and light work/exercise was protective (0.59; 0.38, 0.93) Standing and higher physical stress shortened gestational age, not PB
Only crude analysis was done for LTPA. PB rate decreased as LTPA increased. For OPA, after adjustment, the combination of walking/standing at workplace presented an OR = 3.3 (1.4, 8.0) No association
No association
Physical exertion (2.91; 1.29, 6.58) and standing (4.10; 1.29, 13.10) are risk factors for PB. Physical exercise is protective (0.34; 0.16, 0.73) No association
Selection bias (women or husband had to be formally employed to have access to the clinic) None
Recreational and occupational activities combined
Unclear definition of PA, PB was not a binary outcome, only mean values of gestational age were reported Selection bias, PA at home combined standing and strenuous recreational activity Small sample size, voluntary participation Voluntary participation, exposure data collected only at the 16th week of gestation, exclusion of women with morbidities, PB rate higher among refusals Voluntary participation, gestational age evaluated as a continuous variable, convenience sample, small sample Misleading writing (variables definition) and voluntary participation Small sample size, recruitment in a single maternity hospital
Small sample size, only 2nd trimester PA was considered. All PAs combined Continued next page
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Study (year)
Based on standing, work on industrial machines, physical exertion, mental stress and environmental conditions.
CC = case-control; LTPA = leisure-time physical activities; OPA = occupational physical activities; OR = odds ratio; Pro = prospective; Retro = retrospective.
a
High nonresponse rate (39%). Data only on 1st and 2nd trimester LTPA protects against PB (only crude analysis). No association for standing and lifting
ª 2009 Adis Data Information BV. All rights reserved.
Vigorous LTPA, standing and lifting CC (1908) Pompeii et al.[71] (2005)
Voluntary participation, high refusal rate LTPA not associated with PB. OPA is a risk factor for the whole sample (1.94; 1.13, 3.35) and among nulliparous (4.16; 1.59, 10.83). Among multiparous, housework protects against PB OPA, LTPA, school activities and housework Retro (1714) Cavalli and Tanaka[70] (2001)
Small sample size, poor PA measurement Extreme prematurity is inversely associated with regular LTPA Regular LTPA and physical exertion CC (245) Petridou et al.[69] (2001)
Standing combined with moving on the job, selection bias, only data from 1st and 2nd trimester were analysed Stair climbing (1.60; 1.05, 2.46) and walking for a purpose (2.10; 1.38, 2.20) were risks, while LTPA was protective for PB (0.51; 0.27, 0.95) LTPA, job and housework activities (lifting, standing, climbing stairs and walking for a purpose) Pro (1166) Misra et al.[68] (1998)
Limitations Physical activity Study design (no. of subjects) Study (year)
Table III. Contd
969
Effect/conclusions (OR; 95% CI)
Physical Activity and Preterm Birth
spontaneous preterm birth. Four other studies[59,63,66,68] also found that recreational activities were associated with a reduced incidence of preterm birth. Pompeii et al.[71] found similar protective effects for leisure-time physical activity, but only a crude analysis was carried out. From the papers reviewed, not a single study showed a detrimental effect of recreational activities concerning preterm birth. Overall, studies show that either recreational activities are associated with less chance of preterm birth[52,54,56,63,66,68] or at least do not affect this outcome.[50,51,53,55,64,65,70] 3.4 All-Domain or Other Physical Activities
One way to measure physical activity when assessing more than one kind of activity is through total energy expenditure. This method has been used in pregnant[60,74-76] and nonpregnant samples.[77] Energy expenditure can be assessed by accelerometers, double-labelled water or questionnaires.[78,79] However, all these procedures share the same characteristic of not explaining how the energy was used. Another type of study evaluates physical activities as a single measure, usually a score of activity. Instruments like the International Physical Activity Questionnaire (IPAQ)[80] or the Physical Activity Recall (PAR)[81] are designed to measure physical activity based on the amount of activity performed during specific periods (e.g. for a week) and to consider all domains of physical activity: occupational, commuting, household and leisure time. This type of instrument could be used during pregnancy as long as the interview is repeated several times during gestation to capture changes in activity patterns from conception to delivery. If one decides to interview women during pregnancy and to measure physical activity based on 7-day recall information, the stage of gestation would influence the results, and the information from a single moment would underestimate or overestimate physical activity levels for the whole pregnancy. Four of the studies evaluated[60-62,67] considered physical activity as energy expenditure or as a single score, including occupational physical activity, leisure-time physical activity and housework. Sports Med 2009; 39 (11)
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No association between physical activity and preterm birth was reported in these studies. Household activities were also not associated with prematurity. Contrary to previous studies,[59-61,67] physical activity questionnaires that combine all domains of physical activity in a single score do not seem suitable to study some pregnancy outcomes. Clearly, occupational, household and leisure activities may have different effects. Therefore, we cannot see physical activity as a whole, unless we are studying outcomes that are influenced primarily by energy expenditure balance, which may be appropriate to study, for example, maternal weight gain, fetal growth or birthweight. However, this does not seem to be the case for preterm birth. 4. Limitations Found in the Reviewed Literature Sampling was a weakness in many studies. Convenience samples obtained from a single maternity ward,[25,27,69] from the private sector[33] or from women voluntarily responding to a mailed questionnaire[39,40,52,55] may not be representative of a population. Although we identified papers that explored large datasets[30,34,40,47,55,57,59] with thousands of women, only one study[39] provided a sample size calculation and another[41] provided an estimate of statistical power. Without a sample size or power calculation it is not possible to adequately interpret a lack of association – it may simply be due to lack of statistical power and not evidence against an association. There is no need for a representative sample to be used to study biological outcomes, but, as discussed by Marbury,[82] some papers base their conclusions on risk calculations using very small and selected groups[26,28,30] (e.g. developed-country studies dividing women into job-demand categories and high-demand categories are usually very small) resulting in comparisons between categories that are flawed or applicable only to specific populations. Different working conditions worldwide might lead us to conflicting conclusions, regardless of study quality, methodology or real effects being evaluated. Living conditions and culture may reª 2009 Adis Data Information BV. All rights reserved.
sult in women rating the physical effort they perform differently in a way that epidemiological effects may not be directly comparable: what is seen as a strenuous effort to an American woman might be considered a usual task to another woman living in Thailand, for instance. Another point is that a woman whose colleagues’ working conditions are strenuous may consider her tasks less tiring than if we compared the same job among women working in less physically demanding jobs.[29] A woman who usually works under high physical demands and suddenly changes her job tasks to less demanding ones may classify herself in the low-effort category, although she still experiences high efforts. In addition, when reviewing studies written over a long timespan we must consider that working conditions may be changing and what was considered strenuous in 1995 may not be in 2005 or in 1985.[36] In addition, there may be a self-selection bias in occupational studies where women who keep on working standing for long periods during the third trimester are less likely to have experienced medical problems and therefore present lower risk for adverse outcomes. The best way to assess the potential ‘healthy worker effect’ would be to follow up women who gave up working in the same manner as the working women, and to evaluate whether the reasons for preterm birth differ between both groups.
5. Physiological Aspects of Physical Activities in Pregnancy During prolonged standing, pregnant women experience circulation adaptations: the relaxed uterus inhibits venous flow to the right ventricle by compression and fetal heart rate seems to increase.[83] Little evidence is available about lifting weights, and epidemiological studies do not discuss the issue deeply. However, unless a woman stops breathing during lifting extremely heavy weights (valsalva manoeuvre[84]), there is no reason to believe that daily activities of lifting could result in any adaptation or blood flow alteration that could be related to an increase in the likelihood of preterm birth. Sports Med 2009; 39 (11)
Physical Activity and Preterm Birth
The literature describes many benefits of recreational physical activity during pregnancy:[85,86] more adequate weight gains, improvements in mood and self-esteem,[87] better body image, less anxiety and depressive symptoms among exercising women,[88-90] faster labour, better blood circulation (including blood perfusion to the placenta[91] and venous return from lower limbs, preventing swelling of the extremities), less constipation, better muscular support to the pelvis (leading to less chance of urinary incontinence[92]), better diabetes and hypertension control[93] and less low back pain complaints,[94] among others. Most of the potential effects of leisure-time physical activity on preterm birth prevention are thought to be indirect, as some known risk factors for preterm birth are preventable or reduced by regular exercise, such as excessive weight gain, depression and arterial hypertension.[86] With regard to pre-eclampsia, decreases in proinflammatory cytokines and leptin, lower oxidative stress and improved lipoprotein concentrations are also potential effects of exercise in pregnancy.[86] 6. Physical Activity and Preterm Birth: Considerations Physical activity is a complex factor to assess in epidemiological studies with pregnant or nonpregnant populations, and even the same activity (type, frequency and duration) can result in distinct physiological effects depending on several factors such as environment, intensity, nutrition status, willingness to exercise, period of gestation and previous training.[95] To illustrate the adaptation principle, a 5 km run may be unthinkable for most women (pregnant or not) but for a few well-conditioned people it might be an ordinary exercise session, easily carried out in the fifth month of pregnancy. On an occupational level, if a woman usually works standing 8 hours a day and suddenly reduces her shifts to 4 hours, her effort level will probably not be the same as that experienced by another woman who recently moved from a sedentary job to one where she works standing 4 hours; although, if we interview both, the exposure will be the same – 4 hours daily of standing work. ª 2009 Adis Data Information BV. All rights reserved.
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Most leisure-time physical activity studies rely on information from voluntary women or select groups of women.[50,51,96,97] We cannot rule out the chance that there might be a tendency for healthier women to exercise more than high-risk women,[60] which may affect the results. Leisure-time physical activity might protect against preterm birth because recreationally active women might have a favourable psychological profile and be more concerned about their overall health and other factors not easily controlled in an epidemiological study. Moreover, causation of preterm birth is multifactorial, with many of its determinants still unknown.[6] Underlying risk factors for preterm birth may be those psychological aspects of occupations where women are under constant stress and/or socioeconomic factors not completely assessed by researchers.[59,82] Usually, jobs that are physically demanding are also the ones with less control over decisions and with the lowest levels of satisfaction. There is no clear evidence in the literature that the standing position is harmful to pregnant women as regards preterm labour. The transitory physiological changes of the upright posture are unlikely to have a significant impact on premature rupture of the membranes or birth. When dealing specifically with leisure-time physical activity, some aspects of reverse causality must be considered, especially concerning psychological features. It is reasonable to suppose that depression might lead to isolation and inactivity, an idea supported by a recent literature review.[89] In addition, depressed women present with a higher incidence of preterm birth.[18,98] Barnes et al.[60] suggested that healthier women tend to exercise more than high-risk women, another association that could lead to reverse causality when studying pregnancy adverse outcomes, although other researchers[66] have found a protective effect of leisure-time physical activity independent of pregnancy complications. Many papers have discussed the benefits of physical activity regarding hypertension prevention.[86,99,100] When considering preterm birth it is reasonable to believe that hypertension prevention indirectly prevents preterm birth, since active lifestyles are thought to be beneficial for blood Sports Med 2009; 39 (11)
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pressure and arterial hypertension, and it is a well known risk factor for prematurity. According to a recent roundtable held by the American College of Sports Medicine, physical activity may reduce the risk of pre-eclampsia through several physiological and metabolic pathways. Data reviewed by the group provided evidence to support the biological plausibility of using recreational physical activity to prevent pre-eclampsia in pregnant women.[86] Other researchers have reached similar conclusions.[101,102] Another consideration regarding leisure-time physical activity is that women with a preterm history might avoid physical effort (whether advised by health personnel or not). Regardless of physical activity status, these are women at higher risk of preterm birth, because preterm birth history and other past obstetric risk factors are strong predictors for prematurity. This does not apply to occupational activities, depending on working conditions; to change occupational tasks might not be an option. Although many countries’ legislation assure special treatment for pregnant women, we know that poor working conditions do not allow for changes, especially in developing countries where women must work throughout gestation to survive. If occupational exposures do affect preterm birth it is probably through physiological and biomechanical mechanisms working during the second and third trimesters, when fetal size becomes a physical load and circulation adaptations discussed previously begin. If that is true, results from studies that evaluated only activities at the beginning of gestation[67,33] should be taken cautiously. With regard to leisure activities, the possible effects are not immediate, since the idea we support here is that the exercise acts mainly by improving women’s overall health. Physical activity assessment would be better classified if some in loco observation was carried out, especially to evaluate occupational activities. This strategy would help to avoid recall bias and bias from a woman’s self-perception of physical effort. Stress sources, although difficult to measure, should be investigated to isolate harmful effects of psychological aspects and not to mix them with other aspects of poor working conditions. ª 2009 Adis Data Information BV. All rights reserved.
With respect to control of confounding factors, at least the following variables must be considered: age, race, parity, socioeconomic characteristics, obstetric history and pregnancy-related illnesses such as infections and hypertension. 7. Conclusions Given the evidence provided by the reviewed literature concerning leisure-time physical activity and prematurity, it is safe to assume there is no risk involved for normal pregnancies. Pregnant active women should not be advised to stop exercising, and intensity reduction should be according to the woman’s perception, assuming that the gestational development is normal. Sedentary women should be encouraged to start a physical activity programme compatible with their fitness levels and clinical status. Adequate leisure-time physical activity during pregnancy is also indicated to prevent excessive weight gain, and to control risk factors such as hypertension and diabetes.[99,100] Regarding occupational physical activities, although there is a high variation of exposure among the occupations studied, it seems that, if working conditions are adequate, the negative effect of working during pregnancy is due to psychological features and not physical workload. Thus, pregnant women do not need to be systematically taken away from physically demanding activities fearing that this would increase their risk of premature deliveries. In any case, pregnant women should enrol in high quality antenatal care early on, and the advice from the health team, based on the particular characteristics of each woman and pregnancy, must be followed at all times. The well-being of the future mother is also a priority during working hours. Finally, it is essential that the many methodological issues raised in the present review are dealt with in the planning of future studies so that they can provide us with more conclusive results regarding physical activity and pregnancy outcomes. Acknowledgements No sources of funding were used to assist in the preparation of this review. The authors have no conflicts of interest
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that are directly relevant to the content of this review. During the preparation of the paper, MRD received a fellowship from the CNPq (Brazilian National Council for Scientific and Technological Development).
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Correspondence: Marlos Rodrigues Domingues, PhD, Rua Pedro Armando Gatti, 158-Jardim do Sol., CEP 96216-080, Rio Grande/RS, Brazil. E-mail:
[email protected]
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