Biosorption and Bioaccumulation in Practice

BIOSORPTION AND BIOACCUMULATION IN PRACTICE

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BIOSORPTION AND BIOACCUMULATION IN PRACTICE

KATARZYNA CHOJNACKA

Nova Science Publishers, Inc. New York

Copyright © 2009 by Nova Science Publishers, Inc. All rights reserved. No part of this book may be reproduced, stored in a retrieval system or transmitted in any form or by any means: electronic, electrostatic, magnetic, tape, mechanical photocopying, recording or otherwise without the written permission of the Publisher. For permission to use material from this book please contact us: Telephone 631-231-7269; Fax 631-231-8175 Web Site: http://www.novapublishers.com NOTICE TO THE READER The Publisher has taken reasonable care in the preparation of this book, but makes no expressed or implied warranty of any kind and assumes no responsibility for any errors or omissions. No liability is assumed for incidental or consequential damages in connection with or arising out of information contained in this book. The Publisher shall not be liable for any special, consequential, or exemplary damages resulting, in whole or in part, from the readers’ use of, or reliance upon, this material. Independent verification should be sought for any data, advice or recommendations contained in this book. In addition, no responsibility is assumed by the publisher for any injury and/or damage to persons or property arising from any methods, products, instructions, ideas or otherwise contained in this publication. This publication is designed to provide accurate and authoritative information with regard to the subject matter covered herein. It is sold with the clear understanding that the Publisher is not engaged in rendering legal or any other professional services. If legal or any other expert assistance is required, the services of a competent person should be sought. FROM A DECLARATION OF PARTICIPANTS JOINTLY ADOPTED BY A COMMITTEE OF THE AMERICAN BAR ASSOCIATION AND A COMMITTEE OF PUBLISHERS. LIBRARY OF CONGRESS CATALOGING-IN-PUBLICATION DATA

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CONTENTS Preface

vii

Abstract

ix

Chapter 1

Introduction

1

Chapter 2

Biosorption and Bioaccumulation of Toxic Metals: The Fundamentals of the Processes

3

New Research in Biosorption and Bioaccumulation of Toxic Metals

21

Similarities and Differences between Biosorption and Bioaccumulation Processes

25

Brief Information on Analytical Techniques in Determination of Fate of Toxic Metals in Biosorption and Bioaccumulation

29

Using Bioaccumulation in Biomonitoring of Environmental Pollution

31

Using Biosorption and Bioaccumulation Processes in Wastewater Treatment

61

Using Biosorption and Bioaccumulation in Integrated Processes

71

Using Biosorption and Bioaccumulation to Treat Microelement Hunger

75

Conclusion

95

Chapter 3 Chapter 4 Chapter 5

Chapter 6 Chapter 7 Chapter 8 Chapter 9 Chapter 10 References Index

99 123

PREFACE In the present book, various practical aspects related with new applications of biosorption and bioaccumulation are discussed. These natural processes, which concern every living organism and biomass on the Earth, can find an application in pollution control and also in industry. Environmental applications include biomonitoring as the tool of the assessment of not only concentration, but first of all bioavailability of pollutants in the environment. On the other hand, biosorption and bioaccumulation can be used in the treatment of industrial wastewaters containing toxic metal ions. Biosorption and bioaccumulation can be useful in the manufacture of new kind of products – biofortified food. Plant food can be enriched with micronutrients by the excessive fertilization. The content of micronutrients in animal food can be increased by the supplementation of livestock diet with new preparations, consisting of the biomass enriched with microelements by either biosorption or bioaccumulation. This highly bioavailble and non-toxic form of microelements leads to fortification of animal food. The consumption of biofortified plant or animal food in the future should enable substitutition of mineral inorganic diet supplements with natural products. In order to make a practical use of biosorption and bioaccumulation, it is necessary to thouroughly investigate the processes. Since the biomass is involved here, together with complex mechanisms and multiplicity of interactions of metals with the biomass, it is necessary to carry out a thorough research to get to know the process mechanism and also to be able to model it. These aspects were discussed here. This work was financially supported by Polish Ministry of Science and Higher Education (grant No. R05 014 01 and N N204 019135).

ABSTRACT Natural and controlled processes of biosorption and bioaccumulation may be efficiently used in the assessment of environmental pollution as well as in pollution prevention and cleaning the polluted environment. The property that is used in such pollution control processes is the ability of all types of biomasses to bind toxic metals, in different extent though, depending on morphology and physiology of an organism. If the processes are performed at controlled conditions, the efficiency can be greatly improved. If we would like natural processes to work for us, it would be indispensable to understand their mechanism, rules that govern them, we should know how to model their kinetics and equilibrium. Basically, we should be able to predict the course of the processes at given process parameters in order to design a complete technique and to make a practical use of it. Biosorption and bioaccumulation differ when considering the mechanism and for this reason the potential applications will also be diverse. While in the process of biosorption, pollutants are bound to the surface of cellular wall of the biomass, in bioaccumulation contaminants are also transferred into cellular interiors. The latter can affect the metabolic functions of an organism. Biosorption can be performed by non-living biomass (materials of biological origin), but the essential condition for bioaccumulation to occur is that an organism should be metabolically-active. The present work discusses practical aspects of biosorption and bioaccumulation. The processes have the potential to find environmental applications but also in the manufacture of new high value products. Environmental applications include biomonitoring performed by living organisms. The property that is used here is that the level of a given contaminant in biological tissues is related to the concentration of this substance in the environment. This is expressed by the assessment of bioaccumulation factors. This book reports examples of the application of human hair and consumable

x

Abstract

tissues of animals, and various parts of plants (green parts as well as wood) in environmental pollution monitoring. Biosorption as well as bioaccumulation can find an application in removal of contaminants from aqueous solutions. Biosorption by different materials of plant (microalgal biomass, aquatic plants, plant leaves, straw, grass) and animal origin (eggshells, bones) can be applied in industrial wastewater treatment processes. Also, bioaccumulation by aquatic organisms: microalgae, macroalgae and aquatic plants in metal ions removal from effluents can be used to bind metal ions simultaneously with nutrients. Biosorption and bioaccumulation have the potential to be used in the production of plant and animal food biofortified with microelements, which would be used to treat mineral deficiencies in food and feed. Various aspects related with excessive bioaccumulation of micronutrients by plants were discussed. Biofortification of animal food can be achieved by the proper supplementation of livestock diet. A new preparation consisting of the biomass enriched with microelements by biosorption was elaborated. An attempt to make the processes predictable is discussed here, including screening for good biosorbents/bioaccumulators, determining biosorption and bioaccumulation capacity as well as bioavailability as the function of the concentration of metals in the environment in which an organism is present, together with growth requirements, mathematical modeling, carrying out processes at different operational conditions. This should constitute the basis for the assessment of standardized procedures, in the design of biosorption or bioaccumulation treatment plants and for environmental biomonitoring.

Chapter 1

INTRODUCTION Biosorption and bioaccumulation are processes instantaneously performed by all biomasses either living or dead. It is a natural property and the processes are carried out either by purpose or by mistake (toxic metal ions are taken up instead of essential ions). Capacity of the biomass to bind and concentrate toxic metals from solutions may create the fundamentals for a cost-effective technology for detoxification of industrial effluents [1], mainly from mining and electroplating industry or to recover precious metals from processing solutions [2]. The potential uses and mechanisms of biosorption and bioaccumulation for toxic metals control are shown in Figure 1. Biosorption and bioaccumulation are significant stages of toxic elements cycles in the environment. Thanks to these processes, metals can be transferred from e.g., aquatic environment and become concentrated in bottom sediments.

Figure 1. Binding of metal ions by the biomass.

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These phenomena have been used for decades in conventional biological wastewater treatment plants in which scattered soluble impurities (nutrients, toxic metals and organic compounds) are transferred from dilute soluble form into concentrated, condensed several fold in the biomass of activated sludge with the simultaneous use of processes of biosorption, bioaccumulation and biodegradation. While organic pollutants can be processed by the biomass with the use of all three processes, metal ions can only be utilized with biosorption and bioaccumulation – biodegradation is not possible. The advantage of activated sludge method is that the impurities become concentrated and transferred into solid state that facilitates their utilization. The other practical aspect of the discussed processes is environmental pollution monitoring which bases on known bioaccumulation behavior of metals and organisms [3]. It has been observed that the concentration of toxic metals in biological tissues reflects their concentration in the environment over extended period of time. This theory created the fundamentals for biological monitoring – a technique that determines not only the degree of environmental pollution but also investigates bioavailability of toxic elements from the surrounding environment to living organisms and assessment of the risk posed by these contaminants.

Chapter 2

BIOSORPTION AND BIOACCUMULATION OF TOXIC METALS: THE FUNDAMENTALS OF THE PROCESSES 2.1. TOXIC METALS A term “heavy metal” is commonly used to describe metals that are toxic. However, the term is rather used in causal language and has never been defined by any authority i.e., IUPAC [4]. There are numerous definitions of “heavy metals” classifying according to certain physical, chemical or biological properties, including density (specific gravity), atomic weight and number, other chemical properties, definitions without a clear basis other than toxicity or nonchemical definitions [4]. The majority of definitions have no relation with toxicity of these metals to living organisms since in fact no relation between density and atomic/molecular weight and toxicity has been observed [4]. In the present chapter, toxic metals are understood to be elements (not only metals) commonly used in industry and generally toxic to living organisms even at low concentrations [1], including As, Cd, Cr, Cu, Pb, Hg, Ni, Se, Zn [5]. Se and As are frequently named with a term “heavy metal” although these elements are not metallic [6]. However, when considering toxic properties, they are classified to the same group, similarly as the remaining toxic elements, and are named toxic metals [6]. It is always questionable whether a given element should be considered as toxic. There are metals that play only harmful role in living organisms, through enzyme inhibition or activation, damage of subcellular organelles, carcinogenicity, and effects on kidneys, nervous system, endocrine system, reproduction, and respiratory system [7]. They do not play any positive function

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in living organisms. This is so-called toxic trio that includes Hg, Pb and Cd – the mostly toxic elements used by the industry [8]. Another group includes metals that are needed for the proper functioning of an organism, in low quantities, but simultaneously at elevated levels are toxic [9]. In some cases the difference between essential and harmful concentration is very narrow (such as in the case of selenium). Sometimes, oxidation degree determines toxicity and essentiality of a given metal, e.g., Cr(III) is considered to be microelement, but Cr(VI) is toxic (carcinogenic) [6]. The presence of toxic metals in the scattered and bioavailable form in the environment is highly undesirable. Metals occur in nature in rocks, ores, soil, water, air in naturally low levels and in dispersed form [7]. We should bear in mind though that the total amount of toxic metals such as the majority of other elements present on the Earth has remained and will remain constant. The problem that arose with the industrialization was that metals were mobilized from their deposits (the forms that were not available to living organisms) by anthropogenic activity (making utensils and machinery, mining, smelting, welding, grinding, soldering and printing [7, 9]) and were transferred into bioavailable form and redistributed in such form in the environment [7]. Metals have been mainly mobilized by the branches of industry such as mining and metallurgy [10] and are generally commonly used by industry, agriculture and medicine [7]. The result was that toxic metals began to cycle in ecosystem at elevated concentrations between its biotic and abiotic components and also in the trophic chain becoming concentrated on the top of it in organisms of final consumers, frequently in human body [1]. Because it is impossible to degrade toxic metals, the only method of utilization is safe disposal – immobilization in a solid state and concentration into the form that will not undergo biological cycles and will be basically not available to living organisms [1]. Since the presence of toxic metals in the environment is not desired, their emission by the industry is regulated by law. Recently, environmental law has become more stringent (Table 1) [11]. It is difficult to employ conventional methods to remove metal ions below the level of “ppm’s” since these methods if applied at such low concentrations cause that the methods become expensive and highly energy consuming [11]. These disadvantages of conventional technologies created the need to elaborate a new generation of efficient methods of environmental prevention (intervening at the impact source, in advance of pollutant event), protection (elimination of the effects of pollutant actions or minimization of these effects) and restoration (removing damages caused by previous actions) [12], as well as monitoring [9].

Biosorption and Bioaccumulation of Toxic Metals

5

Table 1. The levels of contaminants in raw effluents, maximum admissible concentration of contaminants in effluents and drinking water (American and European regulations) [mg/L] Metal ion Ag Al As Ba Be Cd Co Cr (total) Cr(VI) Cu Fe Hg Mn Ni Pb Sb Se Sn Th Zn

Domestic wastewater1 0.003-0.01 0.25-1 0.001-0.005

0.001-0.004 0.0005-0.002 0.01-0.004 0.03-0.1 0.4-1.5 0.001-0.003 0.04-0.15 0.01-0.04 0.025-0.08

Wastewater discharge limits European2 American3 0.1 1

Drinking water standards European4 American5

0.1 2

2

0.05 0.05

0.1-0.2 1 0.5 0.1 0.5

1

0.005

0.05 2 0.004 0.005

2

0.05

0.1

0.05

5 100 0.05

0.5 0.5

5 2

1 2

1.3 0.001

0.002

0.05 0.05 0.01 0.01

0.1 0.015 0.006 0.05 0.0005

0.08-0.3

2

5

1

Typical content of metals in domestic wastewater [13]. German requirements for the effluent concentrations in direct discharge into receiving water and indirect discharge into municipal sewers considered dangerous [14]. 3 Wastewater discharge limits (U.S., EPA); pretreatment standards [15]. 4 NPDW (national primary drinking water) regulations for inorganic chemicals MCLG (maximum contaminant level goal) [16]. 5 European Economic Community Standards (maximum admissible concentration) [17]. 2

2.2. BIOSORPTION Biosorption is defined as the ability of materials of biological origin to bind e.g., toxic metals to the surface of cellular wall or membrane in the equilibrium process (Figure 2). More recently, it has been discovered that biosorption is the interaction between metal ions and functional groups present on the cell wall biopolymers of dead organisms [18].

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Figure 2. Biosorption of metal ions.

That is why, biosorption can be classified as a typical adsorption process. There are various classes of biosorbents: by-products or waste materials (with an intermediate sorption capacity), naturally grown and collected biomass [10, 19] (that is practically of no cost) and especially propagated biomass (with high sorption capacity and a possibility to become recovered [19] (e.g. Spirulina [20])). Biosorbents are materials of biological origin that can bind metals and organic compounds. Biosorbents can be of microbial, fungal, seaweed, plant or animal origin [21]. Practically, each type of biomass possesses metal-binding properties. This is determined by the chemical structure of biomolecules that all expose similar functional groups. Of course, there are differences in metal-binding capacities and binding mechanisms between sorbents. Fundamental for the complete design of the process is investigation of the mechanism. The reported mechanism of biosorption is very complex (a combination of ion-exchange, physical adsorption, surface complexation and surface microprecipitation [10, 21-23]), such as diverse is the structure of biological materials [10]. In the past, physical adsorption was thought to be the dominating mechanism. However, recent studies [2, 24-45] showed that the mechanism is similar to ion-exchange process with the functional groups (amino, carboxyl, phosphate, sulfate, hydroxyl groups) exposed by the cellular wall, which is composed mainly of polysaccharides, proteins and lipids [46], and for this reason biosorbents can be considered as weak acidic cation-exchangers [47-48]. Protons and metal cations are released from the biomass, and cations of other metal ions become bound by cellular surface [49]. Therefore, the biomass acts as organic polyelectrolyte. In the process, metal ions compete with protons for the binding sites [46] and hence pH is probably the mostly important process

Biosorption and Bioaccumulation of Toxic Metals

7

parameter. Since the biomass is not uniform and chemically defined material, there are some difficulties in modelling the process in terms of ion-exchange [18]. Recent literature reports that biomaterials can be characterized in terms of acidbase and metal based potentiometric titrations, used in studies of organo-metallic complexes [18]. Biosorption is a metabolically-passive process [2], which means that there is no need for the biosorbent to carry out metabolic functions during biosorption. For this reason, non-living biomasses are used. Process involving toxic metals and non-living biomass is much easier and cheaper since keeping biomass alive requires expenditures of nutrients and energy. Also, toxic effects that might be potentially posed by these metals can be avoided. The mostly important process parameters include concentration of metal ions and the biomass, temperature, contact time, agitation and pH. The latter influences three significant parameters, such as speciation of metal ions and their solubility, as well as surface properties of the biomass [11]. The process may find a practical application only if its mechanism, process parameters, kinetics and equilibrium are known. Only then it will be reliable, predictable and possible to design and control [2]. In modeling of biosorption and bioaccumulation processes similar simplifications are used as in the case of microbial growth modelling (which is simplified to single enzymatic reaction). Biosorption is a quick process. The equilibrium is usually reached within few minutes. Since the rate of the process is high, in some cases it is even difficult to select and fit the proper equation and to determine the order of the reaction due to errors related with quick sampling. The process is usually described with either first- [50], second- [51], pseudo-first- [52] or pseudo-second [52-53] order kinetic equation. The reaction order is related with the mechanism of biosorption, which is the most frequently ion exchange or surface precipitation (metal hydroxide, sulfide or carbonate) [54]. Literature reports that the rate limiting step is chemisorption which involves valent forces by sharing or exchange of electrons between sorbent and sorbate [54-55]. In kinetics modeling, Lagergren pseudo-first order and pseudo-second order models are used [56]:

ln

qeq − qt qeq

= − k1t , k1 (1/min)

t t 1 , k2 (g/(mg min)) = + 2 qt k 2 qeq qeq

- assumes that metal cation binds only to one sorption site on the sorbent surface: R(s)+ Me2+(aq)=RMe2+(ads) - metal cations are bound to two binding sites on the sorbent surface 2R(s)+ Me2+(aq)=R2Me2+(ads)

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Katarzyna Chojnacka

The equilibrium of biosorption can be described with either Langmuir [26, 57-98] or Freundlich [57-59] model (Figure 3). In studies on sorption behavior, both capacity and affinity of a given sorbent to sorbate are investigated [2]. If the dominating mechanism is ion-exchange, which means that a biosorbent possesses a finite number of cations binding sites, we can observe a plateau on isotherm graph. The equilibrium can be described with Langmuir equation, since it is more suitable for description of chemisorption process. It was observed that biosorption is usually a reversible process. It is possible to remove bound metal ions with weakly acidic solutions or with strong brine and thus to recover the biomass such as in classical cation-exchange process. Through the selection of the proper eluents, it is possible to restore biosorption properties of biosorbent and reuse it another biosorption cycle [60-61].

Freundlich

qeq

Langmuir

Ceq Figure 3. A comparison of Langmuir and Freundlich models.

Multi-component biosorption Biosorption is influenced by both: surface properties of the biomass and physicochemical parameters of the solution (pH, ionic strength, temperature, biomass concentration, presence of organic and inorganic ligands in the solution

Biosorption and Bioaccumulation of Toxic Metals

9

[62]. The majority of works devoted to biosorption is carried out in single-metal system and single-metal isotherms are plotted. This is, of course, idealistic approach. In real systems, if real effluents are treated, a multiplicity of various ions is present in the solution. Under those conditions, predicted biosorption performance in single metal experiments does not comply with the performance in real systems, due to the presence of competitive phenomena and multiplicity of interactions. Competition between metal ions hinders observed sorption capacity. Usually, the biomass binds cations selectively – some ions are preferred over the other [63]. A lot of further research needs to be done in order to elaborate a uniform approach to multi-metallic biosorption. Only then the process will find an application in practice. In biosorption process, the following equilibrium reactions take place in the solution [54]:

R 2− + M 2+ ⇔ MeR at low pH protons compete for the binding sites:

R 2− + 2 H + ⇔ H 2 R A possible approach in modeling is to measure the ratio between the maximum biosorption capacity in multi-metal system to single metal system at different pH [54]. In multi-metal systems, interaction between particular cations for the binding sites is observed [64]. Also, internal competition (competition between cations of the same type) occurs as well as competition between metal cations and protons [54]. Biosorption performance in multi-metal systems depends on variety of factors: the number and the type of competing metal ions for the binding sites, metals combination, concentration, the type of biosorbent. Also, the type of interactions vary and can be either synergistic, antagonistic or none [64]. The biomass possesses different selectivity towards various metal cations. This selectivity depends on the type of the biomass, the composition of the solution, physicochemical conditions [62]. This makes it difficult to elaborate a universal model describing multi-ion biosorption. Generally, it is impossible to predict biosorption performance in multi-metal system theoretically. Although, some attempts in the literature have been made to forecast biosorption on the basis of known Langmuir isotherms determined in single-metal system [64]. In the majority of cases an approach includes the use of isotherm model parameters determined in single-metal system and correction factors evaluated in multi-metal system experiments, which are characteristic for a given cation and depend on the concentrations of other species in the solution [62].

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Modeling biosorption in multi-metal system Recently, many efforts have been made in the literature to elaborate a universal model which would describe multi-component biosorption well. This is required to transfer the process into industrial scale, to be able to design and predict a continuous process, adsorbent selectivity in multi-metal systems, to carry out the process in continuous fixed bed columns after immobilization in a polymeric matrix [65]. Usually, simple extensions of classical isotherms are used. However, it is necessary to take into consideration that these models do not predict, but only correlate the model with the experimental data [66]. Generally, competitive isotherms describing multi-component biosorption are classified according to their relationships with single component isotherms [67]: 1. competitive Langmuir/Freundlich models are related only with individual parameters of isotherm 2. modified competitive Langmuir/Freundlich models are related with both: individual parameters of isotherm and correction factors A model better fits experimental data if coefficients from experimental competitive isotherms were included [67]. The model parameters can be determined by nonlinear least-squares regression. Multi-metal isotherms found in the literature are presented in Table 2. The constants qmax and b are derived from individual isotherms, η is multicomponent Langmuir constant; Qmax and B determined from multicomponent experiments; N- total number of metals in the system. Predictive models do not require fitting to data from multi-component systems. All parameters are determined from single-metal isotherms [69]. Consequently, these models frequently fail to describe multi-metal biosorption data well. The assumption of multi-sorbate Langmuir model is that sorption does not involve competition. Competitive models, though assume the presence of other metals in the solution which affect only the apparent affinity for the active site. The shape of the isotherm changes if other metal ions are present in the solution. However, the maximum biosorption capacity does not change [70]. In this case, the model proposed by Jain and Snoeyink [70] is used.

Table 2. Different Langmuir and Freundlich-type equations used in modeling multi-metal biosorption Model

qi ,eq =

qmax,i bi Ci ,eq N

1 + ∑ b j C j ,eq j =1

qmax,i bi qi ,eq =

qi ,eq =

Ci ,eq

ηi

N

C j ,eq

j =1

ηj

1 + ∑ bj

Qmax,i Bi Ci ,eq N

1 + ∑ B j C j ,eq j =1

Name

Decription Equations based on Langmuir model the predictive derived from corresponding individual Lanmguir isotherms; assumes competitive the same selectivity, uniform surface and that all cations compete for Langmuir the same binding sites without interaction nor competition between model ions; qmax is determined from single metal system and theoretically should be the same for all metal cations; if qmax differs, this means that binding sites are not homogeneous and are specific towards metal cations; but this is not consistent with the basic assumption of Langmuir equation; if sorbent shows heterogeneity, then affinity should differ empirical beside mono-component coefficients, additional competition extension coefficients are determined from experimental multi-metal data; nonLangmuir ideal competition between sorbates is assumed; the model is more model flexible and represents complexity of multi-metal system; qmax is general for various multi-component systems Langmuir model

all parameters are determined by fitting to multi-component equilibrium data

Ref. [65, 68-69]

[62, 65, 69]

[65]

Table 2. (Continued) Model

qi ,eq =

Name Langmuir model with general total binding capacity

qmax,Total bi Ci ,eq N

1 + ∑η j b j C j ,eq j =1

qi ,eq =

qmax,i bi Ci ,eq N

extension LangmuirFreundlich model

ni

1 + ∑ b j C j ,eq

nj

j =1

qi ,eq =

(qmax,i − q max, j )bi Ci ,eq 1 + bi Ci ,eq

+

q max, j bi Ci ,eq N

1 + ∑ bjC j ,eq j =1

qi ,eq =

K F Ci ,eq N

n

nj

j =1

K F ,i Ci ,eq

qi ,eq = Ci ,eq

ni 1

N

ni0 + ni 1

+ ∑ K F , ij C j ,eq j =1

(qmax,i − qmax, j ) -

the fraction of ions which adsorb without

nij

empirical extension Freundlich model

Ref. [69]

[66]

[70]

competition

qmax, j - the fraction of ions which adsorbs with competition

Equations based on Freundlich model the predictive KF,i and ni are determined from individual Freundlich isotherms; competitive Freundlich model

ni + n1

Ci ,eq 1 + ∑ b j C j ,eq

Decription general total binding capacity (qmax,Total) and additional correction coefficients (η) are used in this isotherm; the total binding capacity is the same for all the cations and can be determined by potentiometric titration (total active site concentration or total cation exchange capacity); total metal uptake at given pH is constant for all the cations; if pH decreases, binding capacity also decreases; all the cations compete for the same binding sites artificial neural networks were used to solve this equation

KF,ij, nij are correction coefficients determined in multi-metal system

[62]

[62]

Biosorption and Bioaccumulation of Toxic Metals

13

According to the literature [69] the best model for the description of multimetal biosorption is simple competitive Langmuir equation with additional correction coefficients. This makes the model flexible. There was also found a completely different approach to modeling biosorption in multi-metal systems. Ma and Tobin [71] suggested that oxygen containing functional groups act as metal binding sites. Ion exchange and surface complexation were the dominating mechanisms. This can be understood as the explanation of selectivity order. Selectivity should differ as the affinity constants of metal cations to the binding sites differ. Biosorption followed the following reactions and equilibria [71]:

R − + H + ⇔ RH

KH =

αR − + M 1α + ⇔ Rα M 1

[ R − ][ H + ] [ RH ] α+

βR − + M 2 β + ⇔ Rβ M 2

K M1 =

[ R − ]α [ M 1 ] [ Rα M 1 ]α

K M2 =

[ R − ]β [ M 2 ] [ Rβ M 2 ] β

β+

χR − + M 3 χ + ⇔ R χ M 3

χ+

K M3

[ R − ]χ [ M 3 ] = [ Rχ M 3 ] χ

The total number of sites can be expressed with the following equation:

[R ] = [R ]+ [RH ] + α1 [R M ] + β1 [R M ]+ χ1 [R M ] −

T

−

α

1

β

2

χ

3

The above set of equations can be used to model multi-model biosorption. The uptake of metal ions is related with its hydrolytic properties:

HO − H + M n+ ⇔ M ( OH )( n−1 )+ + H + and also with interaction among metal cations and the protonated site:

R − H + M n+ ⇔ R( M )( n−1 )+ + H + If metal is very acidic (which can be evaluated by determination of the ratio

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Katarzyna Chojnacka

charge:mass), then the metal cation binds more easily with a protonated site, when related to weaker acidic metal cation [69]. For this reason, the most acidic ion is less affected by the presence of other less acidic ions and influences their binding the mostly. Consequently, the values of hydrolysis constants describe the following selectivity order: Pb(II)>Cu(II)>Zn(II)>Cd(II) [69].

State-of-the-art in research on multi-metal biosorption Ma and Tobin [71] carried out biosorption of Cr(III), Cu(II) and Cd(II) cations onto peat moss. It was found that the selectivity order was as follows: Cr(III)>Cu(II)>Cd(II). Mohapatra nad Gupta [72] investigated concurrent biosorption of Zn, Co and Cu by Oscillatoria angustissima in binary and ternary system. In single metal system, the following selectivity order was identified: Zn>Co>Cu. In binary system: Cu(II)>Zn(II), Cu(II)>Co(II), Zn(II)≈Co(II). The domination of Cu(II) was found. In ternary system, Co(II) protection against inhibitory effect of Cu(II) on Zn(II) was found. Inhibitory effect of Zn(II) and Cu(II) on Co(II) was additive. While it was achievable to model binary system, the problems were encountered in modeling ternary system [72]. Mehta and Gaur (2001) proposed the use of two-dimensional contour plots. But those were confined only to binary systems. It is also possible to propose triangular graph, which would be useful in modeling biosorption in ternary system. Such equilibrium diagrams were proposed by Sag et al. [73]. In biosorption in ternary system at equal initial molar concentrations of metal ions in the solution, the relative surface coverage of the biomass was 45-55 % for Cr(VI), 36-41 % for Fe(III) and 8-14 % for Cu(II). Sag and Kutsal [64] studied competitive biosorption of Cr(VI) and Fe(III) in binary system by a filamentous fungus Rhizopus arrhizus. This was investigated as the potential method of wastewater treatment. The results were described with competitive Langmuir model. Sag et al. [67] carried out work on biosorption of Cu(II) and Zn(II) in binary metal mixtures by the same fungus. The results were described with competitive Freundlich model. Pagnanelli et al. [62] investigated selectivity of the biomass towards Cu(II) and Cd(II) in binary solution. The biomass was more selective towards Cu(II) and the selectivity changed with pH. The same authors [69] found that low pH masks the competition between metal ions for the binding sites, which is another proof that biosorption phenomenon is related with ion exchange. In this work biosorption by Sphaerotilus natans in various binary systems (Cu-Cd, Cu-Pb, Cu-Zn) at different pH was investigated. Cu(II) uptake was strongly influenced by increasing Pb(II) concentration, while the influence of Cd(II) was much weaker. In another study, where the experiments

Biosorption and Bioaccumulation of Toxic Metals

15

were carried out in ternary system, Pagnanelli et al. [65] identified a typical selectivity order for ternary system: Pb>Cu>Cd. Sun et al. [54] carried out biosorption in binary solutions containing Co(II) and Zn(II) ions on aerobic granules. Biosorption of Co(II) was quicker than of Zn(II). The mechanism of biosorption investigated in this study was binding to the functional groups (carboxylate, alcoholic). The groups were identified by using FTIR and XPS techniques. Chen and Wang [74] used also instrumental techniques: FTIR (Fourier Transformed Infrared Spectroscopy), SEM (Scanning Electron Microscopy), TEM (Transmission Electron Microscopy) to identify the mechanism of biosorption. Resulting, the possible mechanism was ion exchange, chelation and microprecipitation [75-76]. Chen and Wang [74] studied how ionic characteristics of various cations influence their biosorption properties. A quantitative structure activity model for biosorption of 10 metal cations to Saccharomyces cerevisiae was proposed. Physicochemical parameters (22) were correlated with the maximum biosorption capacity of a given cation. The mostly important parameter was covalent index: the higher index, the higher potential to form covalent bonds with biological ligands (thiol, amino, carboxyl, hydroxyl groups). However in the study of Tobin et al. [77] the most significant physicochemical parameter which influenced biosorption capacity was ionic radius. The following selectivity order of maximum biosorption capacities were proposed (expressed as meq/g): Pb(II)>Ag(I)>Cr(III)>Cu(II)>Zn(II)>Cd(II)>Co(II)>Sr(II)>Ni(II)>Cs(I) [74]. Saeed et al. [78] investigated removal of Cd, Cu, Ni and Zn by a crop milling agro-waste (black gram husk) in single, binary and ternary systems. Selectivity order determined in this study was similar and was as follows: Pb(II)>Cd(II)>Zn(II)>Cu(II)>Ni(II). The presence of Pb(II) did not significantly affect sorption of other metal cations. The authors also managed to completely desorb metal cations from the biomass by 0.1 M HCl [78].

2.3. BIOACCUMULATION Bioaccumulation is the process in which toxic metals or organic compounds become bound within the inner cellular structures. According to the definition [79], bioaccumulation is the process by which living organisms absorb and retain chemicals or elements from their surrounding environment. Other definitions say that bioaccumulation is the accumulation of a chemical either from a medium (usually water) directly or from the consumption of food containing the chemical

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[9]. Bioaccumulants are substances the concentration of which in living organisms increases as they are taken up from contaminated air, water or food [79]. The critical condition for bioaccumulation to occur is that the biomass should be alive. Bioaccumulation can be performed only by metabolically active cells [2] and therefore the process is metabolically controlled [79-81]. All living organisms throughout their lives accumulate essential, non-essential and toxic substances. All living beings developed pathways that protect them either from an excessive bioaccumulation (e.g. routes through which bioaccumulant enters an organism is blocked or bioaccumulant is excreted outside of an organism) or bioaccumulant is safely deposited within the cell to prevent incorporation into metabolic reactions (e.g. metal ions are bound by special chelating proteins that are rich in thiol groups, so-called phytochelatins in algae or metallothioneins [82]). For simplification, bioaccumulation can also be described as absorption of metal ions by whole cells (not only by cellular surface as in biosorption). The route through which a bioaccumulant enters an organism is usually the same through which it takes up nutrients or food. In unicellular organisms, toxic metals enter through the transport channels, usually erroneously with essential elements (e.g. Ca(II) or Mg(II)). In plants, some toxic metals are transported from water and soil through the root system, some are acquainted foliarly (from atmospheric deposition) [83]. The route of transfer also depends on which environment is the mostly polluted with a given metal: water, soil or air. In animals, the routes through which toxic metals are bioaccumulated are mainly alimentary tract (food and water contaminated with toxic metals), but also from respiratory system (from polluted air) and through skin (contact exposure) [84]. In some cases the route of bioaccumulation determines toxic effect and protective response that is activated. Bioaccumulation can find a dual application in pollution control. It can be used to monitor environmental pollution, since there is a correlation between bioaccumulation capacity (the concentration of metal in the biomass) and the concentration in the environment in pollution prevention (wastewater treatment) [85-90] and in cleaning the environment (soil remediation by bioaccumulating plants – so-called hyperaccumulators) [91]. If a method of environmental monitoring is elaborated, it is necessary to screen for good bioaccumulators – biomonitors [92-93]. The analysis of such biomass on the basis of known correlation between the level in the environment and biological material, enables to measure the concentration of a given pollutant in the environment (Figure 4). The mostly advantageous would be to find such biomonitors, the analysis of which would be non invasive nor painful to sample and would not cause any damage to an organism. An example of such biomonitor is human hair or fingernails.

Cbiological tissue

Biosorption and Bioaccumulation of Toxic Metals

17

bioaccumulation factor

Cenvironment Figure 4. Correlation between the level of contaminant in environment and in biological tissues.

The use of cosmopolitan organisms to monitor bioavailability of a given contaminant enables comparison of contaminants levels in different geographical regions. There are two types of bioaccumulating organisms distinguished: bioindicators that are used for identification and qualitative determination of environmental pollution and biomonitors that are used for quantitative analysis of contaminants. In the latter group, sensitive (optical type - morphological changes are observed) and accumulative biomonitors (ability to store contaminants is assessed) are distinguished. Also, the route of absorption may influence the subsequent distribution of the metal within the body [3, 12]. For instance in human, bioaccumulation occurs through inhalation, oral ingestion and dermal exposure [3]. Bioaccumulation itself is the result of the equilibrium of biota intake and discharges from and into the surrounding environment [12]. The process depends on many factors: availability of elements, characteristics of an organism (species, age, state of health etc.) and parameters, such as temperature, available moisture, substrate characteristics, climatic factors, frequently being also parameters that influence metabolic functions of an organism [12]. Therefore, there are difficulties to elaborate standardized procedures and obtain reference values.

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Quantitative biomarkers are used to identify toxic responses in populations exposed to very low concentrations in the environment [94]. Monitoring is the repetitive observation for defined purposes using comparable and standardized methods [95]. Thus, it is very important to elaborate standardized procedures that would enable to monitor environmental pollution on the basis of analysis of contaminants levels in biological tissues. Recently evolved, so-called bioaccumulation monitoring is the exposure assessment by measuring contaminant level in biota [95]. Since living organisms bioaccumulate toxic metals from the environment, their concentration in biological tissues is related with the concentration of a given pollutant in the environment in which they live and with the length of their life. The concentration of bioaccumulant in the biomass, when related to its concentration in the environment (bioaccumulation factor) (Figure 4) [96-97], is the measure of bioavailability of a given metal from the polluted environment in an organism of a given species. It was observed that the higher organization level an organism possesses, the more perfect protective system preventing bioaccumulation or excreting bioaccumulant it would have. E.g. in human body metals become concentrated in keratinous materials: hair or fingernails that are indicators of longterm exposure [3]. Basically, the lower organism is, the higher bioaccumulation capacity it possesses. Therefore, if we would like to employ bioaccumulation process as a method of toxic metals removal from the environment, it would be the mostly advantageous to employ the smallest and the mostly primitive organisms – microorganisms since they have the highest bioaccumulation capacity [19]. In bioaccumulation, two distinctive processes can be distinguished (Figure 5). In the first step, metal ions are bound to the surface of cells – the process is metabolically passive, it is identical with biosorption. In the second stage, metal ions are transported into the cellular interior. In order to perform this stage, cells must be metabolically active. In another stage, if nutrients are available, the concentration of the biomass increases. More metal binding sites and cellular interiors are available to metal ions. This enables to bind more metal ions when comparing with biosorption.

Biosorption and Bioaccumulation of Toxic Metals

Figure 5. The stages of bioaccumulation of metal ions.

19

Chapter 3

NEW RESEARCH IN BIOSORPTION AND BIOACCUMULATION OF TOXIC METALS The recent research on biosorption focuses mainly on removal of toxic metals commonly used in industrial processes, such as Cu [48, 85, 88, 98-102], Cd [18, 48, 100, 103-106], Pb [18, 48, 100, 103, 107-109], Cr [53-54, 57, 81], Zn [52, 99], Ni [110] (Figure 6). There are few studies devoted Hg [104], Al [57] and Co, As, Th. In bioaccumulation literature concentrates mainly on Cd [97, 109, 111-112], Cu [80, 109], Hg [109], Pb [109], Cr [109], Zn [111], As and Ni (Figure 6). Currently studied sorbents include: aerobic [8, 50] and anaerobic [110] granular biomass, bacteria (Sphaerotilus natans [12, 21, 82], Pseudomonas putida [99]), microalgae (Chlorella vulgaris [98], Microcystis aeruginosa [104]), macroalgae ((Gelidium) and algal waste [101, 103], Sargassum muticum [106]) fungi (Cephalosporium aphidicola [108], Rhizopus arrhizus [46, 58], Neurospora crassa [100]), biological products (extracellular polysaccharide (Pestan) produced by fungus Pestalotiopsis [107] and other fungal by-products (Botrytis cinerea) [105], cellulose/chitin bed [113], chaff [114]). Trends in current research include studies on kinetics [50, 52, 108] and equilibrium [12, 21, 51, 53, 102-104, 108], influence of pH [8, 38, 101], ionic strength [12, 21, 101-102] and temperature [101], including modelling [12, 21, 24, 51, 102-103]. Reports contain investigation of biosorption in single- and multi-metal systems [98]. A particular attention is paid to identification of the mechanism of the process [113], including i.e., metal-based potentiometric titration [19, 46]. Also, some modifications (pretreatments) of the biomass are tested [80], i.e., protonation [106]. The new process configurations are also studied extensively, including carrying out the process in membrane bioreactors [12]. Bioaccumulators that are currently studied include: bacteria (genetically engineered Escherichia coli [86]), yeasts (Kluyveromyces marxianus [88]),

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microalgae (Chlorella kessleri [114]), plants (grass Dactylis glomerata [115]), aquatic plants (Lemna minor) [85], aquatic animals (Baikal seal (Phoca sibirica) [116], scleractinian coral (Stylophora pistillata) [117], tube worm Riftia pachyptila [109], soft tissues of mollusks Patella aspera [118] and zebra mussel (Dreissena polymorpha) [119], mangrove oysters (Crassostrea rhizophorae) [92], amphibian larvae [120], marine fish [89, 111], freshwater fish (European eel Anguilla anguilla [121]), multispecies monitoring of muscle tissue of fish [122]), terrestrial animals (earthworm Lumbricus terrestris [123-124], animals (rats [125126]). Th 0.3% As 0.3% Co 0.4% Al 1% Hg 3% Ni 9%

Cu 25%

Zn 12%

Cr 14%

Cd 18% Pb 17%

As 5%

a)

Ni 3% Cd 23%

Zn 10% Cr 10%

Cu 18% Pb 14% Hg 16%

Figure 6. Current trends in research in biosorption (a) and bioaccumulation (b).

b)

New Research in Biosorption and Bioaccumulation of Toxic Metals

23

The majority of studies concern environmental monitoring of aquatic environment with the use of bioaccumulating aquatic animals: invertebrates and vertebrates. Recently appeared also reports on monitoring by terrestrial plants and animals, including human (assessment of exposure by the analysis of hair and fingernails) [6]. Toxicity tests using metals bioaccumulation usually are performed on rats. New research on bioaccumulation focuses on: monitoring of pollution of aquatic environment through the analysis of levels of toxic metals in tissues of aquatic organisms [109, 111, 120, 121-122], wastewater treatment [85-86, 88-89], bioaccumulation by plants grown on contaminated soils [115], bioaccumulation of metals from wastes by earthworms [124], inhalation toxicity tests by rats [125], effect of the presence of one metal on the accumulation of other toxic metals [111], the effect of solubility of toxic metals salts on their bioavailability [124], the assessment of relationship between bioaccumulation of toxic metals with environmental conditions and genetic variability [82], analytical studies on bioaccumulation of toxic metals in biological tissues [126].

Chapter 4

SIMILARITIES AND DIFFERENCES BETWEEN BIOSORPTION AND BIOACCUMULATION PROCESSES When comparing biosorption and bioaccumulation processes, bioaccumulation although performed in simpler installations, requires troublesome cultivation of the biomass in the presence of contaminants that may pose toxic effects to the biomass itself. The difference between the equilibrium of biosorption and bioaccumulation process is shown in Figure 7.

qmax

Bioaccumulation

q

external

(mg/g)

Biosorption

C0

Ceq (mg/kg)

Figure 7. Equilibrium shift towards lower values of Ceq in bioaccumulation process when comparing with biosorption.

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Biosorption itself is the first stage of bioaccumulation. In the second stage, ions are furtherly transferred into cellular interior that results in the equilibrium shift towards lower concentration of metal ions. Table 3 discusses the differences between biosorption and bioaccumulation processes. Table 3. The comparison between biosorption and bioaccumulation process Biosorption Passive process Metals are bound with cellular surface Adsorption Reversible process Biomass is not alive Nutrients are not required Single-stage process The rate is quick Not controlled by metabolism No danger of toxic effect No cellular growth Intermediate equilibrium concentration of metal ions

Bioaccumulation Active process Metals are bound with cellular surface and interior Absorption Partially reversible process Biomass is alive Nutrients are required Double-stage process The rate is slow Controlled by metabolism Danger of toxic effects caused by contaminants Cellular growth occurs Very low equilibrium concentration of metal ions

Biosorption is an equilibrium process. The efficiency of biosorption is expressed in terms of biosorption capacity, which is the mass or molar equivalent of metal bound by the unit mass of a biosorbent [mg/g or meq/g]. The basic characterization of a biosorbent includes evaluation of maximum sorption capacity (qmax) and affinity (b parameter in the case of Langmuir equation). The mostly advantageous in the case of both bioremoval and biobinding would be for a sorbent to have simultaneously high sorption capacity and affinity. In Figure 8 there are shown sorbents with different characteristics. Sorbent 1 possesses high affinity and high maximum binding capacity. This is the best sorbent. Sorbent 2 possesses high maximum sorption capacity but low affinity. Sorbent 3 – high sorption affinity but low maximum sorption capacity and sorbent 4 – low affinity and low maximum sorption capacity. The latter sorbent possesses the worse characteristics. In bioremoval processes of particular importance is affinity of a biosorbent. This is related with the potential applications of this process as polishing treatment in order to reduce the concentration of pollutants below the acceptable limits.

Similarities and Differences Between Biosorption and Bioaccumulation... 27

1

qeq

2 3 4

Ceq

Figure 8. Isotherms for different types of sorbents.

For this reason the mostly desired characteristic would be high affinity of sorbent to sorbate, which is low equilibrium concentration of pollutant reached even at low equilibrium sorption capacities. Therefore, it is recommended to use sorbent possessing characteristics such as material 1 and 3 (Figure 8). If we are interested in other than bioremoval applications – biobinding (e.g. production of bioavailable feed supplements), of the primary importance would be the highest maximum sorption capacity since the goal is to bind possibly high quantities of metal ions by a unit of the biosorbent biomass. In this case it is recommended to use either sorbent 1 or 2.

Chapter 5

BRIEF INFORMATION ON ANALYTICAL TECHNIQUES IN THE DETERMINATION OF FATE OF TOXIC METALS IN BIOSORPTION AND BIOACCUMULATION Analytical techniques used in studies on biosorption and bioaccumulation processes should be very sensitive in determination of elements on the level of even ng/kg and should minimize interferences and matrix effects. These include modern instrumental techniques, such as atomic absorption spectrometry, atomic emission spectrometry, inductively coupled plasma emission spectrometry: ICP Optical Emission Spectrometry (ICP-OES) and ICP – Mass Spectrometry (ICPMS). It is very significant to use methods with very low detection limit, since in the majority of cases the concentration of elements is below 1 mg/kg. Prior the analysis, the studied materials are digested with mineral acids, preferably in microwave oven in closed vessels. This generates 50-100 times dilution. For this reason, it is advantageous to use methods with detection limit below μg/L, such as ICP-OES with ultrasonic nebulization or ICP with mass detector [127]. The analytical process should be controlled by the use of certified reference materials that have similar matrix as the analyzed material. E.g. in the analysis of human hair, Reference Material Human Hair was used [128]. It is recommended to perform semi-quantitative analysis of samples prior the quantitative analysis in order to evaluate the expected levels of analytes and to determine the main components. The knowledge of the levels of the main components is used in the preparation of calibration solutions. The mostly advantageous is to add the main components into the calibration solution. Such an approach minimizes matrix effects and also in some extent, interferences.

Chapter 6

USING BIOACCUMULATION IN BIOMONITORING OF ENVIRONMENTAL POLLUTION The processes of biosorption and bioaccumulation have found or will find in the nearest future an application in various areas related with environmental protection (Figure 9). Among these processes, two types of methods can be distinguished, which have common mechanisms, but the goals are different – bioremoval and biobinding. In the case of bioremoval, the goal is to achieve the highest possible removal of toxic metal ions via either biosorption or bioaccumulation processes.

Figure 9. Biosorption and bioaccumulation understood as bioremoval and biobinding.

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The objective is first of all to remove metal ions to the concentration below the level required by obligatory law, which is usually ca. 1 mg/L from large volume diluted solutions. This use of biosorption and bioaccumulation methods is recommended as the final, polishing step, before the final discharge of effluents. Biobinding processes that can be applied in environmental protection include biomonitoring. In this case, the aim would be not to bind the highest amounts of metals but to assess the concentration and bioavailability of pollutant in the environment. Biobinding processes can also find another application – in the production of highly bioavailable mineral feed additives. In this case the goal would be to bind the highest quantities of metals via either biosorption or bioaccumulation. The content of toxic metals in tissues or in the biomass of each organism reflects the level of a given contaminant in the environment. But, on the other hand, not every organism has the potential to be a good biomonitor or biondicator. First of all, biomonitoring should be ethically correct. Sampling of biomonitor tissues should not be invasive, nor should not pose destruction or deterioration of an organism, nor pain. Another issue is that the concentration factor of a pollutant in the studied material should be high enough to be possible to determine after digestion and dilution of a sample. Criteria of good biomonitor fulfill particularly non-living tissues, such as human hair [128-130], animal fear or birds feather, as well as animal products, advantageously consumable, such as eggs and milk [132142]. Also, plant tissues are good biomonitors of soil pollution [143-147]. The analysis of human hair provides the information on pollution of environment in which an organism lives, as well as contamination of food and drinks [128-129]. The level of soil pollution can be determined by the analysis of plant tissues [143]. It was also found that it is possible, through the use of specially elaborated extraction procedures to determine content of bioavailable forms of metals and on this basis (knowing so-called transfer factor) to predict the composition of plants that are to be cultivated on a given soil [143-147].

6.1. HUMAN HAIR AS BIOMONITOR OF ENVIRONMENTAL POLLUTION AND NUTRITIONAL STATUS OF INDIVIDUALS It is well known that the concentration of metals in biological tissues reflects their level in the environment. The property that is used in biomonitoring is that a mechanism that protects an organism from the excessive accumulation and toxic effects posed by a given contaminant is excretion outside an organism via

Using Bioaccumulation in Biomonitoring of Environmental Pollution

33

different routes: urine and feces, sweat and also transfer to external non-living tissues, such as hair and nail or birds feather. Elements enter living organism via different routes: are transferred from air, water, foods, drugs, through skin, respiratory tract and gastro-intestinal tract. Metals are transported by blood and deposited in organs [129]. The elements are distributed in an organism by blood and deposited in organs and tissues [129]. The elements that are present in hair can be divided into macroelements and trace elements. The latter group consists of toxic trace elements and essential trace elements (microelements) that comprises of major essential trace elements (Fe, Zn and Cu) and minor essential trace elements (Mn, Se, Cr, Co, Ni, Si, F, I) [128-130]. Table 4 presents the composition of hair from a population living in urban and industrialized area [129]. Table 4. Concentration of elements in human hair: reference values reported by commercial laboratories and scientific literature Reference values

Average values in populations

Commercial laboratories

Literature data

Element Doctor’s Data, Inc. Ag Al As B Ba Be Ca Cd Co Cr Cu Fe Hg K Mg Mn Mo Na

< 0.13 <8 < 0.08 0.5-3.5 0.19-1.6 < 0.02 160-500 < 0.15 0.013-0.035 0.23-0.50 9-30 6-17 < 0.4 10-40 12-50 0.18-0.60 0.04-0.089 12-90

Hair Analysis Lab

0.2-1.5 < 0.23

72-188 < 0.15 0.04-0.35 1.5-3.4 0.9-3 < 0.2 8-20 7.5-22.5 0.04-0.35 10-32

[152]

< 0.7 < 12 <7 1-3 0.3-3.5 350-860 <1 0.26-0.47 0.78-1 13-35 6-15 < 1.2 8-38 40-110 0.26-0.75 0.21-0.44 18-87

USA (Trace Elements Inc.) [181]

Rio de Janeiro [152]

9-18 0.1-0.2

1.19 8.3 <0.04

0-2.60

6.9

220-970 0.07-0.14 0.01-0.03 0.20-0.80 9-39 5-16 0.09-0.18 20-240 20-110 0.10-1.30 0.03-0.08 40-360

802 0.59 0.13 < 0.3 44.1 20.8 0.62 4.9 43.9 5 0.05 87.7

Sweden [182]

Poland, Wrocław [128-130]

0.231 8.2 0.085 0.670 0.64 0.0013 750 0.058 0.013 0.167 25 9.6 0.261 83 46 0.560 0.042 147

0.395 14.9 0.044 2.04 2.02 0.055 1088 0.114 0.034 0.568 12.4 15 0.5 210 67 0.6 0.017 217

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Table 4. Concentration of elements in human hair: reference values reported by commercial laboratories and scientific literature (continued) Reference values

Average values in populations

Commercial laboratories

Literature data

Element Doctor’s Data, Inc. < 0.4 160-250 <1 < 0.005 < 0.066 0.95-1.7

USA (Trace Elements Inc.) [181]

Hair Analysis Lab

[152]

Rio de Janeiro [152]

0.13-0.37 9-18 < 1.5

< 1.6 120-180 <6

110-200 1.5-3

0.7 119 12.5

0.03-0.2

< 1.8 0.38-0.7

0.30-1.80

0.02 129

Ni P Pb Pt Sb Se Si Sn Sr Ti U V W Zn Zr

110-190 0.06-0.70

14-24

125-165

100-210 0.155

156

Ca/Mg Ca/P Na/K Zn/Cu Zn/Cd

4-30 0.8-8 0.5-10 4-20 >800

3-25 4-21 0.5-4 4-16 > 93

3-22 2-7 0.5-11 4-13 > 125

2-48 1-9 0.17-18 2.6-23 714

16 6 2 6 2450

< 0.3 0.21-2.7 <1 < 0.06 0.025-0.1

<3 1-7.6

0.35-0.8

0.13 5.1 0.09-0.17 0.02-0.14

0.07

Sweden [182]

Poland, Wrocław [128-130]

0.430 133 0.960 0.00015 0.022 0.830 33 0.320 1.20 0.830 0.057 0.027 0.0053 142 0.155

0.84 132 1.05 0.0004 0.455 0.679 57.5 1.2 2.88 1.5 0.21 0.09 0.002 156 0.57

18 7 18 3.5 264

16 8 1 13 1370

The elaboration of commonly used methods of environmental pollution monitoring through the analysis of biological tissues should preferably include studying materials that are sampled easily and painlessly and reflect an exposure history of a given organism. Human hair, for instance, fulfills these criteria. Although human hair can be theoretically considered as reliable and convenient biological indicator of environmental pollution, there have been some problems encountered in the elaboration of reference values for the concentration of metals in human hair, in particular some problems with the standardization of the method occurred. It was found that the level of elements in hair is the function of age, sex, and hair color, as well as hair treatments, including hair coloring and undulation as well as other treatments that affect the structure of hair. Also sex,

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35

nutritional habits and smoking [130] influence the composition of hair. In studying the composition of hair it is also necessary to consider inter-elementinteractions: antagonisms and synergisms [129]. It is also significant to distinguish between internal (originating from the body) and external deposition. There exist elaborated washing procedures (i.e. with water and acetone) [129] that enable to distinguish between the metal that entered an organism (was bioaccumulated) and was simply adsorbed by the external surface of hair. Hair mineral analysis supplies information which could be used in environmental sciences as well as in medicine. Beside the potential of using hair as reliable and convenient biomonitor of environmental pollution, it was found that some problems with elaboration of reference values for elements concentration in human hair and interpretation problems were encountered. Elements in hair are incorporated into its keratin structure. Affinity for metals is due to the presence of cystine in keratin, follicular melanin, which binds cations to its carboxyl groups [148]. Melanin is the main pigment of hair. Blond hair contain lower concentration of melanin when compared with black hair. Therefore, blond hair contain less cations binding agent and typically tend to contain less cations. This is needed to take into consideration while interpreting results of hair mineral analyses. Many studies proved that the composition of hair reflects elemental status of an organism. Hair mineral analysis, if correctly interpreted, could show a multiplicity of information – not only on environmental pollution, but also on food status of human and diseases. Beside that this technique is known for ca. 30 years, it has found so far no practical application in medical analytics, because there are problems with interpretation. Since the concentration of elements in hair is very low (on the level of ppm, ppb or even ppt), over years the reference values changed along with the development of more sensitive and more advanced analytical techniques. Probably because of this, in the literature many confusing information are found. Reference values reported in the literature for healthy people which were not exposed to environmental pollution, show contradictory information (Table 4). In the past years, it was discovered that multielemental composition of human hair is strongly correlated with personal characteristics, such as age, sex, hair color, cosmetic treatments (hair coloring, perm, shampoos), structure of hair and its growth rate, human race and even geographical location. It was hypothesized that the content of trace elements in hair is the consequence of adaptation of the population to environmental factors (climate, geographical and geochemical factors, eating habits) [149]. Available reference values did not take into consideration these characteristics, beside that recent literature information

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showed that these parameters should be considered in interpretation of results of hair mineral analysis. Only then it would be possible to state whether a given person was exposed to toxic metals, or suffers for deficiency of a microelement. The results of hair mineral analysis should not be interpreted as the results of blood tests. In contrast with the results of blood analysis, the content of elements in hair is not related with homeostatic mechanisms. Differences in the concentration of elements from the reference values are frequently observed before the appearance of symptoms. This is a very good tool in forecasting physiological disorders. The concentration of trace elements in hair is, as literature reports, 10-50 times higher than in blood, 100-500 times higher than in urine [150]. Additionally the results of hair mineral analysis are the picture of chronic, not temporary exposure (as in blood or urine) of elemental status of an organism and reflect an average exposure of a given subject [151]. While analysis of the composition of hair gives a good description of status of toxic elements (Hg, As, Pb, Cd) [152], there are problems with interpretation of status of nutritional elements. Elevated concentration of nutritional elements in hair does not necessarily reflects its elevated concentration in the whole organism, but could mean higher excretion of this element to hair tissue and consequently lower concentration of this element in other tissues and organs, showing thus its poor absorption. Literature review clearly shows that more epidemiological studies are needed to make hair analysis a useful tool in the assessment of environment exposure and health of human. Table 5 lists advantages and disadvantages of hair mineral analysis. Problems which arise in hair mineral analysis are mainly related with either analytical procedures (different analytical techniques yield different results) or with problems with interpretation of results. Human hair is excretory, not functional tissue. During the growth of hair, elements become permanently incorporated into its structure. The process is irreversible and non-equilibrium. The elemental composition of hair is the record of history of elemental metabolism and exposure to toxic elements. The results of hair analysis could be the basis of diagnosis of physiological disorders related with malfunction of metabolism of nutritional and toxic elements. Hair is important in terms of mechanism of elimination of toxic elements from an organism [151]. The growth rate of hair is ca. 0.4 mm/d (1 cm/month) [155]. The analyses of fragments which are 1 cm long enable to recall the history of exposure of a given person in the previous months. When a given person is not exposed anymore, after a period of time, the concentration in hair gradually approaches the normal value [156]. Factors influencing response of a given person include age, sex, bodyweight, nutritional, genetic and immunological status. The possibility of

Using Bioaccumulation in Biomonitoring of Environmental Pollution

37

excretion of substances to hair tissue is related with a tolerance towards a given toxin. This creates the lack of symptoms beside the presence of a toxin in an organism [156]. Table 5. Advantages and disadvantages of hair mineral analysis [148, 153-154] Advantages Marker of metals exposure at workplace and environment The measure of total and average body intake over extended periods of time (body fluids are the measure of only momentary status) Higher concentration of analytes than in body fluids Easy, painless and non-invasive sampling Stable during storage

Disadvantages Exogenous contamination (sebum, sweat, air deposition, cosmetic and pharmaceutical products) Lack of correlation between the content of hair and other organs (in some cases)

Lack of knowledge on kinetics of elements incorporation into hair structure Insufficient epidemiological data to predict health effects The source of controversial findings: sampling and sample preparation procedures, exogenous contamination, geographical origin, lifestyle, differences between various analytical methods

Good screening tool Less affected by natural excretion

Literature describes that the concentration of elements in hair which are cofactors of enzymes: Mg, Cr, Zn, Cu, Se, is significantly correlated with their concentration in organs and tissues. American Environmental Protection Agency recommends using hair mineral analysis for the assessment of environmental pollution with toxic elements (U.S.E.P.A. 600/4-79-049) [157]. The existence of statistically significant correlations between the content of elements in hair and internal organs on the basis of tests carried out on persons which died in accidents was confirmed [156]. Literature describes many examples of diseases related with malfunction of biological balance between the concentrations of elements in hair in eg. patients suffering for arthritis or cancer when compared with healthy people [151]. Also, examples of correlation of various diseases with deficiency/excess of nutritional (Co, Zn, Se, Cu, Cr) or toxic (Cd, Pb, Hg) elements are reported [152]. Hair of alcoholics contain elevated level of Ca, P, Na and low content of K [156, 158].

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It was found that in the case of many elements, their concentration in hair was proportional to the concentration in an organism. But there are exceptions. The analysis of hair also shows problems with absorption of minerals: − −

−

Impairment of excretion of metals, eg. in autism, the concentration of Hg in hair is low and in tissues is high. After treatment, the aim of which was detoxification of an organism from Cu by using Cu antagonists (Zn and vitamin C), the concentration of Cu in hair increases. The ratio Cu/Zn is used in diagnosis of ADHD and behavioral disorders.

Below, literature examples of diseases identification in relation to the content of elements in human hair, are listed: Historical examples: − Mineral analysis of Napoleon Bonaparte hair showed that the cause of his death was not gastric carcinoma, as was supposed on the basis of postmortem, but chronic poisoning with inorganic form of arsenic [159]. The concentration of arsenic exceeded the reference values 100 times [157, 160]. − Ludwig van Beethoven suffered for deafness and many neurological and gastric disorders. Many years after his death, basing on hair mineral analysis it was proved that these were the symptoms of plumbism. The standardized values were exceeded 100 times. Searching for the source of Pb exposure revealed that the composer sweetened wine with the salts of Pb and used utensils painted with Pb [156, 161]. Children – age and sex: − The concentration of trace elements in children depends on age and sex. In hair of boys, the concentration of Cu and Mn was higher than in girls. The level of Cu, Mn and Zn was low in children below 14 years of age and increased up to 20 years. It was thus hypothesized that requirements of growing children for trace elements was higher than children which do not grow [162]. Lekouch et al., [150] found differences in the level of Pb and Cd in hair of children of various sexes and age. Generally, the concentration of these elements was higher in girls than in boys and decreased with age. Correlations between living environment, the composition of drinking water and the content of these elements in hair were denoted [150]. − Senofonte et al. [154] determined reference values for the concentration of

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elements in hair of schoolboys from cities from various age groups and both sexes. − Low concentration of Cu is the consequence of malnutrition, according to Ali et al., [163]. Other sources report than in malnourished children, the content of Zn in hair was low, and the content of Cu and Fe was high. Therefore it was hypothesized that the content of Zn was the indicator of malnutrition [156]. − On the basis of hair analysis it was hypothesized that age, sex and profession of mother influenced the concentration of Pb in infants in the age 0-12 months [164]. Children – diseases: − In children suffering for enteritis, statistically significant lower level of Ca, Cu, K, Mn and V in hair was determined when compared with the control (children of the same age, living in the same geographical region) [165]. − In children with autism, higher level of Mg and Zn in hair was recorded. These elements play a significant role in neurochemical processes [156, 166]. Heart diseases, diabetes: − In subjects with hypertension, coronary heart disease and diabetes, lower level of Cr, Cu and Zn was found. The content of Cd in hair was significantly higher than in the control group [167]. − It is thought that too low level of Cu is responsible for coronary heart disease. Hence, low concentration of Cu in hair or elevated value of ratio Zn/Cu (low concentration of Cu and high Zn) indicates hypercholesterolemia, ischemic heart disease, arterial hypertension or excessive weight. In women, in the hair of which higher content of Cu and lower level of Zn was determined, insulinindependent diabetes could be expected, before the first symptoms are observed [156, 168]. − In subjects after myocardial infarction, higher content of Zn and lower Cu was determined. Other studies report that in 90 % subjects after myocardial infarction, low level of Ca in hair was found [156, 169]. − Afridi et al. [170] showed that pathogenesis of heart diseases is related with imbalance of trace elements. In hair of patients with myocardial infarction, lower content of Fe and Zn was recorded in all the age groups, in both sexes. The concentration of Pb, Cd and Ni was elevated. Also, imbalance of proportions between trace elements was recorded, in particular low values of ratios: Zn/Cu and Zn/Cd. The authors hypothesized that toxic metals might decrease absorption of nutritional elements. Recently, a significant attention was paid to the role of Cu, Fe, Cr and Zn in ischemic heart disease, eg. Cu is essential in blood forming processes. Cu is the component of superoxide dismutase, which also requires the presence of Mn and Zn. Deficiency of any of these elements decreases the activity of this enzyme and as the consequence the number of free radicals increases. This causes

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arteriosclerosis, lungs diseases, in particular in elderly people. Also, the consequence of the excessive accumulation of Pb and Cd are heart diseases, cancer, infertility, arteriosclerosis through the occurrence of oxidative stress [170]. − Hair of people suffering for diabetes contain less Cr when compared with healthy people, however in women with gestational diabetes mellitus, higher level of Cr in hair was determined [156, 171]. − Syndrome X, caused by insulin resistance, causes hyperinsulinism (glucose intolerance and type II diabetes). The consequence is the loss of Zn from an organism and excessive excretion to hair tissue. It was found that in nephritic syndrome, Zn is lost with urine beside its presence in the diet. Consequently, the content of Zn in hair is low. Similarly in celiac disease, the concentration of Zn in hair is low [156]. Diseases of women: − In women sensitive to Ni, significantly higher levels of this element were found in hair [156, 172]. − Shamberger [173] investigated the concentration of various elements in blood and hair of women suffering for premenstrual syndrome. The author showed that in hair of these women, the content of Hg, Zn/Cu in hair was higher and Fe, K and Mg/Ca was lower than in the control group. The author hypothesized that premenstrual syndrome could be related with Ca deficiency or Ca metabolic defect. He also observed that Ca supplementation weakened the symptoms. In women suffering for fibromyalgia – rheumatic diseases of 2 % women, higher level of Ca and Mg in hair was found. Etiology of this disease is too low level of these elements in blood, since they are excreted in excess to hair tissues. In this case, Ca and Mg supplementation is recommended [173]. − Osteoporosis in women, resulting in lower mineral density of bones is the result of excessive excretion of Mg to hair tissue and that an important indicator of this disease is the ratio of Ca/Mg in hair [174]. Cancer: − The composition of hair of women with breast cancer and hypertrophy of the mammary gland was determined and was compared with the group of healthy subjects. In hair of women with breast pathology, lower levels of Se and Zn and higher of Cr were denoted. The lowest concentration of Se was in hair of women suffering for cancer when compared with suffering for hypertrophy of the mammary gland. The possible explanation was the role of free radicals [175]. It was proved that the concentration of Se in hair was proportional to the concentration in internal organs. Se is antagonist of Hg and is supplied in preparations for Hg detoxification [156]. − Analysis of hair composition of patients suffering for nasopharyngeal carcinoma showed lower level of Sr and higher of As, Fe, V when compared

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with the control group, while the concentration of V was 3 times higher than in healthy people [151]. Nervous system diseases: − In patients with epilepsy the value of the ratio Mg/Zn was lower than 1 and in healthy people was higher than 1. Literature also reports that the basis for diagnosis of epilepsy could be low level of Cu, Mg and Zn [156, 176]. − In hair of mentally retarded children, elevated concentration of Pb and Cd was observed. It was found that both toxic metals cause mental retardation, lower intelligence, difficulties in learning and concentrating [177]. − Hair of prisoners guilty of aggressive crimes contained higher levels of manganese. Many studies showed that hair of aggressive people contain elevated level of Cd and Pb in hair [156, 178]. − In hair of patients suffering for dyskinesia, with parenteral nutrition, lower concentration of Cu, Se and Mo was observed when compared with the control group of persons of the same age. This shows reduced uptake of these elements [179]. − Etiology of Parkinson’s disease is thought to be related with imbalances in the body level of Ca, Cu, Fe, Mg, Si and Zn. Forte et al. [148] found that hair of patients suffering on this disease contained statistically significant lower levels of Fe, Ca, Mg and higher levels of Zn. The concentration of elements however did not correlate with the duration and the severity of sickness [148]. In Parkinson’s disease metals (Fe) are accumulated in some regions of brains. This was confirmed by the post-mortem analysis of the Substantia Nigra. Cu is the cofactor of detoxifying enzymes which reduce oxidative stress in brain. Zn is the component of superoxide dismutase and Zn-thioneine enzymes which also reduce oxidative stress. On the other hand, neurotoxicity of Ca is related with promoting free generation of free radicals generation [148]. Occupational diseases: − Hair mineral analysis is also a tool for the assessment of occupational risk. For instance, hair of workers of glass-works contained higher levels of Mg, Zn, Al, Na, Mn and As [155]. Biomonitoring: − Hair is very useful in identification of elevated levels of Hg in an organism. The studies showed that persons, which consume marine fish once a week, the content of Hg in hair is 2 times higher than in persons which do not eat fish [156]. − Hair content of Pb in people living in rural area was lower than in people living in cities. Only in the case of the content of Cr, Cu, Ni and Zn, statistically significant influence of age, sex or diet was not recorded [167]. − Human hair was used as biomonitor of pollution emitted by electric power plant [175]. − Hair was used in the assessment of heavy metals exposure by cupric pyrite

42

Katarzyna Chojnacka mine in Portugal [153]. It was found that hair of subjects living in the proximity of the mine contained significantly higher levels of Cd, Cu and As. Drinking water was probably not the source of trace elements to human. The toxic elements entered human organism probably through dairy products. Therefore animal foodstuffs were the most probable source of exposure [153].

Table 4 presents the comparison of reference values reported by commercial laboratories, scientific literature as well as the average values for the population of Poland (Wroclaw city) [126-128], Sweden and Brazil. The concentration of various elements in hair was compared with the reference values. Several divergences between standardized concentrations reported by various sources were found. For example, according to commercial laboratories, the content of Cr in the population of Wrocław, Poland was elevated, according to Park et al. [181] was normal, and according to Miekeley et al. [152] was deficient. Similarly in the case of Se. According to the values reported by Hair Analysis Lab, hair of subjects from Poland contained excessive levels of Se, according to Miekeley [152] and Park et al. [181], the content lied within a normal range, and according to the laboratory Doctor’s Data – was deficient in Se. Unique interpretation was possible only in the case of Ca (excess in the population of Wrocław), Mo (deficient), Ca, As, Cd and Pb (concentration within a normal range). The majority of reference values (3 lof 4) pointed out on the excess of Al, K and Na and the normal content of Cu, Fe, Mn and Zn. The population of Wrocław, Poland, when compared with the majority of the reference values showed significant differences in the level of Na, K, Ca, which could result from differences in nutritional habits (food, water). The above information point out the existence of inconsistencies and many problems in the assessment of elemental status – interpretation of results or diagnosis of deficiencies or excessive levels of elements with the use of currently available reference values and show the needs for further investigations in order to elaborate new reference values, which are specific for a given ethnical, geographical characteristics, eating habits etc. However, surprising is conformity of results of proportions between various elements. Interpretation of proportions between them by using different reference values gave very consistent results. For ratios of elements, all the results were within the normal range. Perhaps this points out on the course in the interpretation of the results of hair mineral analysis. In the future, more significant will probably be not concentrations of a given element, but rather ratios between elements. This should give the information on anomalies in metabolism of various elements and point out imbalance problems.

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Studies of inter-element interactions between elements in human hair were performed on the population living in an urban and industrialized region [129] in order to assess if a concentration of a given element is somehow related with the concentration of another. This approach enabled to point out on common occurrence of elements related with i.e., environmental exposure or dietary habits. Synergisms and antagonisms between elements were studied through determination of statistically significant linear correlation coefficients and also by linear multiple regression analysis [129]. On the basis of multielemental determination of 33 elements in human hair, the elements were grouped according to their concentration in hair (in decreasing order): Ca < Na < Zn < P < Mg < Si < Fe < Al < Cu < Sr < B < Ba < Ti < Sn < Pb < Ni < Se < Mn < Zr < Cr < Hg < Sb < Ag < U < Cd < V < Be < Au < As < Co < Mo < W < Pt. The concentration of Ca was above 1000 mg/kg. The concentration of Na, Zn and P was in the range 100-200 mg/kg. The level of Mg, Si, Fe, Al and Cu was above 10 mg/kg. The concentration of Sr, B, Ba, Ti, Sn and Pb was 1-2 mg/kg. The level of other metals was below 1 mg/kg [129]. The concentration of elements in hair of the studied population was compared with other studies. The differences in the level of Ag, Al, Ca and Na were encountered [129]. Studies on inter-element interactions showed the existence of the following statistically significant correlations, mainly of synergistic character: Mg-Ca, MnCa, Sr-Ca,Sr-Mg, U-Na, Ni-Zn, Cd-Ni, Sb-Pt. There exist stronger interactions between industrially related elements when comparing with essential elements, i.e.: Cu-V, U-Ba, Fe-Mn and Al, Mn-Al and Sr, Mo-Au, Au-Pt, Be-Pt, Ba-Sb, AgSb, Sr-Sb and W and W-Sb. It was possible to distinguish groups of elements that are mutually correlated, such as a group of (Sr, Sb, W) – the elements that are emitted by industry, including metallurgical works. Another group of (Ca, Mg, Mn, Sr) was negatively correlated with (Pt, W) [129]. Linear multiple regression analysis confirmed the following inter-element dependencies: Al=f(U, P, Mn), As=f(Zn, Fe) (Zn is an antagonist), Cu=f(V), Fe=f(Mn, As), Mg=f(Ca), Ca=f(Mg, Ba), Ni=f(Zn, Cd), Sb=f(Pt, Sn, W), Ti=f(Fe, Co) [129]. It was found that age of individuals has strong influence on elements concentration in human hair. The studied population was divided into four age groups: children (0-15 years old individuals), young people (15-25 years old), adults (25-45 years old), middle-aged people (45-65) (Table 6). The level of some elements did not depend on age of an individual: Ti, Se, Mn, Ni, Hg, Cd, As, Co. This group (except Co) was found to be related rather with environmental exposure or originated from food and drinking water. Hair of children (< 15 years) has a tendency to contain more Na, K, P, Al, B, Pb, Fe, Cr, Au, Pt, Sb, Be,

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W and less Ca, Cu, V, Sn, Be, Ag, Zr than hair of older people. Hair of individuals in the age 15-25 years (young people) has higher levels of Ca, Zn, Si, Mg, Sr and lower levels of Na and K than people from other age groups. Hair of adults in the age 25-45 years has higher level of Ca, Ag, Zr and lower level of Na and K. People from the oldest group (45-65 years) have higher level of Na, K, Cu, V, Sn and lower level of: Ca, Zn, Si, Mg, Sr, Ag, Zr in their hair [130]. Also, the concentration of elements of females’ hair was compared with the level in males hair. The study showed that hair of females contained significantly more Ag, W, Sr, Ca and more Mg, Si, Be, Cr, P and Mn. Hair of males contained higher concentrations of Sn, V, Au, Sb, Pb, Zr, K, B, As, Na, Mo, Hg. It was found that the level of Al, Cd and Co did not depend on sex of an individual [130]. Table 6. The effect of age on the level of elements in hair [130] Elements Ca Na, K P, Al, B, Pb, Fe, Cr, Au, Pt, Sb, Be, W Cu, V, Sn Zn, Si, Mg, Sr Ag, Zr Ba Ti, Se, Mn, Ni, Hg, Cd, As, Co

Age group 0-15 15-25 25-45 45-65 ↓ ↑ ↑ ↓ ↑ ↓ ↓ ↑ ↑ ↓ ↓ ↓ ↓ ↓ ↓ ↑ ↓ ↑ ↓ ↓ ↓ ↓ ↑ ↓ ↓ ↓ ↑ ↑ the level does not depend on age

↑ - higher concentration when compared with other age groups. ↓ - lower concentration when compared with other age groups.

The composition of hair of tobacco-smokers was compared with hair of nonsmokers. Surprisingly, results showed that hair of non-smokers did not contain higher levels of toxic metals, such as Cd. It was found that hair of non-smokers contained higher level of V, Se, P, Sr, Si, Ba, Na, Cr and hair of smokers contained more Zr, Mo and As. The level of the following elements was similar: Cd, K, Ag, Ca, Co and Be. Generally, hair of non-smokers contained more metals (both essential and non-essential). Literature reports that smokers, blood and urine contain elevated levels of toxic metals and this is the main route of detoxification of an organism [130]. The effect of hair treatments (e.g. coloring) and hair color on the elemental composition of hair was investigated. Colored hair contained more Sr, Ba, Ca,

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Mg, W, Mo, Ag, Mn, but less V, Zr, Sb, Pb, As, Si, K and Hg. Colored hair contained almost twenty times higher level of metals than natural hair. Also, the level of elements in hair of different color (among naturally colored hair) was investigated. The highest concentration of Si was found in dark blond hair, Co – in blond hair, Au, Cd, Sb, Ni, Ag, Pb, Co, Cu – in dark hair, V, Pt – in auburn hair. Generally, the concentration of Ca was higher in dark hair than in fair hair. The level of Mn, Fe and Na was not the function of hair color [130]. The concentration of metals in hair of a given individual changes significantly along with the change of living habits. The elemental composition of hair of individuals that either lived together or were family related was investigated over extended period of time. The content of metals of the studied individuals was compared with the average composition of hair of people living in the studied urban area. The differences concerned mainly different living habits (Na, Si, Co, Fe, Mn, Zn) and local exposure or personal ability to accumulate a given metal (Pb, Cd, Ba). The concentration of the following elements did not depend on local exposure nor personal predispositions: Ag, Al, As, B, Cr, Pt, Se. Time profile from a given individual showed that the concentration of a given element changed several fold over the years with the change of living habits and environmental exposure. There were found similar tendencies in the accumulation of the majority of elements by people that lived together. It was found that the effect of living habits was stronger than the influence of either sex or family relationship. The concentration of the majority of elements was similar in people that lived together and thus consume similar food and drinks and live in the same environment. Of course, lifestyle of a particular subject is always individual. Also, inter-element interactions were observed between the elements that occur together: Ca-Mg, FeMn, Na-K, Co-K, Au-Pt, Cd-Pb. Linear multiple regression analysis confirmed the existence of the following dependencies: Ca=f(Mn, Sr), Na=f(K, Mn), K=f(V, Ti). Groups of mutual statistically significant correlations were distinguished: (Fe, Mn, V), (As, Au, Pt, Zr), (Co, Pb, Sb) that resulted either from the common occurrence of these elements or synergistic effects between them [128]. Hair of females contained more Ag, Sr, Ca, Mg, Cu, TI, P, Mn, but hair of males Mo, B, Co, Sn, Zr, Si, V, K, Pt, Au, As, Pb and Fe. No differences in the concentration of Ba, Cd, Zn, Ni, Hg, Cr, Se, Na, Al were observed. The level of the following elements was a function of living habits: Zr, Sn, Ag, Ti, As, Se, Co, Sb, Si, Sr, Ni, Ba, Mn, Cu, Mg, Cd, Pb, Ca, Na, Fe, P, V, B, Cr. No differences in the level of Mo, Zn, K, Hg, Al was denoted. Generally, it was found that hair of females contained more macroelements (Ca, Mg, P) and hair of males more microelements (Mo, B, Co). The level of toxic elements was similar and it was concluded that their level was rather related with local exposure and living habits.

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The study showed that people that lived together have practically identical level of Hg, Al, Mo and Zn. When comparing with the whole population, the level of As and Al was similar. It was found that the whole population was exposed to As and Al and the level of these elements in hair was elevated when comparing with other populations. Generally, the strongest influence on elements level in hair was not posed by personal ability nor sex, but first of all by living habits and environmental exposure [128].

6.2. BIOAVAILABILITY OF TOXIC METALS FROM SOILS TO PLANTS Of particular concern is food contamination with toxic metals, such as As, Cd, Hg and Pb. Legal directives define the permissible content of elements in plants used for consumption purposes. Toxic metals are taken up by plants from air, water and soil. The presence of toxic metals, such as As, Cd, Hg and Pb in these environments results in their accumulation throughout the trophic chain. Also, some micronutrients, such as Cu, Cr, Ni, Zn are toxic at higher concentrations. Bioavailability of toxic elements to plants is affected by many factors, including soil and climatic conditions, plant species, agronomic management, active/passive transfer processes, sequestration and speciation, redox state, the type of plant root system and the response of plants to elements in relation to seasonal cycles [143]. Knowledge of bioavailability of toxic metals from soils to plants can be used in ecological risk assessment that relies on site-specific exposure models for the estimation of uptake of contaminants. There is the need to elaborate standardized procedures that would enable to predict before sowing, whether it is recommended to cultivate plants for consumption purposes on a given field. It is therefore necessary to assess techniques that would enable to estimate bioavailability of metals to plants. This would make it possible to predict the composition of plants before sowing, on the basis of the analysis of extractable fraction of metals in soil that is bioavailable to plants along with the assessment of soil-plant correlation coefficients. For many years, there have been attempts to obtain statistically significant soil-plant correlation coefficients, however without success, since the concentration of metals in plant was related with the total concentration in soil. This means that the presence of a given metal in soil at high concentrations would not necessarily mean that the level in plant would be exceeded. Extraction procedures were proposed as a method of simulation of

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transfer of metal ions from soil to plants. The proposed extraction tests were verified in field experiments on contaminated soils. The efficiency was confirmed by germination tests. In order to precisely determine the concentration of elements in soil, soil extracts and plants, it was necessary to use analytical techniques with a very low detection limits, such as inductively coupled plasma optical emission spectroscopy (ICP-OES) with ultrasonic nebulizer or inductively coupled plasma mass spectroscopy (ICP-MS). These experiments enabled to assess uptake and bioavailability of metals from soil and to investigate inter-element interactions [143, 183]. It was found that through the application of the proper extraction procedures it was possible to assess the portion of a given element that was soluble in the soil solution and thus was available to plants. It was shown that the highest soil-plant correlation coefficient was found in the case of extraction with 2 % w/v ammonium citrate and 0.1 M sodium nitrate solution. This means that extraction of soil with the use of such eluents and the analysis of the concentration of metals in the post-extraction solution would provide us with the information on bioavailability of metals from soil to plant [143]. The quantity of metal accumulated by plants from soil is defined as transfer factor (bioaccumulation coefficient) (TF):

TF =

C Plant C Soil

(1)

where CPlant is the concentration in plant and CSoil is the concentration of metal in soil. However, the equation can only be applied if there exists a statistically significant correlation between the concentration of metal in plant and soil (Figure 10). For this reason, CSoil would rather represent bioavailable concentration of metal in soil. In some cases, the dependence CPlant=f(CSoil) does not intercepts at (0, 0). The equation should be expressed with the use of the following equation:

TF = a +

C Plant C Soil

(2)

If a≠0, a metal does not originate only from soil, but can be bioaccumulated by a plant from i.e., air deposition. If a=0, the metal was bioaccumulated by plant only from soil as illustrated by Figure 10 [143].

Katarzyna Chojnacka

CPlant

48

___

a=0 a>0

CSoil

Figure 10. Soil-plant transfer of metal ions.

Soil-plant transfer factors were determined for various metals. Statistically significant dependencies between bioavailable soil fraction (extracted with sodium citrate) and the concentration in plant was detected in the case of As, Cd, Cr, Cu, Hg, Mn, Pb, and Zn. Only in the case of Ni no correlation was observed. Statistically significant correlation between total concentration in soil and plant was observed only for Cu. Also, transfer factors were calculated for elements that showed statistically significant correlations. The knowledge of TF enables to predict the composition of plants before sowing, on the basis of the analysis of concentration of bioavailable form of elements in soil [143]. Solubility (and thus concentration of bioavailable forms) of metals is not necessarily directly proportional to its total concentration in soil. It depends first of all on factors that affect solubility, such as pH and the concentration of P2O5 as well as on the presence of other elements (synergistic and antagonistic effects). Statistically significant correlations between the total content in soil and in plants were encountered only for potassium, the metal that forms soluble salts with almost all anions. Also, the experimental results showed that elevated pH and high concentration of P2O5 resulted in decreased bioavailability.

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Transfer Factor is the measure of the extent to which a plant concentrates a given element in its biomass, as related to bioavailable fraction in soil. The highest TF was found for Zn (4000), afterwards Cu (120), Mn (44), Pb (33), Cd (31), As (17), Hg (4.5). Also, it was checked whether a given element was accumulated by plants only from soil (model parameter a=0). The following elements were taken up only from soil: As, Cd, Cu. In the case of Hg and Ni a>0, which meant that these elements were bioaccumulated also by air deposition. This is the explanation of low (although statistically significant) correlation coefficient for Hg and no statistical significance for Ni.

6.3. WOOD ASH AS BIOMONITOR OF ENVIRONMENTAL POLLUTION AND MATERIAL THAT DECREASES BIOAVAILABILITY OF POLLUTANTS IN CONTAMINATED SOILS Wood ash constitutes ca. 5 % of burnt wood. Thus, wood ash can be considered as the concentrate of metals that were bioaccumulated by wood that became concentrated 20 times. In the combustion process, organic matter, nitrogen, sulfur, mercury and cadmium volatilize. The remaining macroelements (i.e., Ca), microelements and toxic metals become concentrated. For this reason, since the material is the concentrate, it is easier to determine the presence of trace elements in wood biomass. Wood ash is strongly alkaline material that can find an application as the substitute of lime, as soil deacidifying agent. Wood ash contains 35 % CaO, 9 % K2O, 2 % P2O5 and 1.6 % MgO. These can be considered as macroelements of fertilizer significance. Wood ash contains also high levels of micronutrients that were bioaccumulated by wood and are of fertilizer value, such as Fe (0.5 %), Mn (0.1 %), B (350 mg/kg), Zn (230 mg/kg), Cu (170 mg/kg), Co (8 mg/kg), Mo (3 mg/kg). Also, wood ash contains toxic metals on the level related with the environmental pollution, such as Pb (30 mg/kg), Cd (8 mg/kg), As (20 mg/kg) [144]. The elemental composition of wood ash from different tree species was determined (Table 7) [184] and compared with soil. If used as soil amendment, wood ash should contain similar or lower level of toxic metals when compared with soil. The composition of wood ash from various trees (oak, birch, acacia, ash tree and apple tree, coniferous tree) was analyzed in order to investigate which wood

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species bioaccumulated the highest quantity of a given metal. The concentration of various elements (macroelements, microelements and trace elements vary depending on tree species. The lowest concentration of both microelements and toxic metals (with the exception of Zn and B) was found in ash from fruit tree. Probably these elements are partially excreted to fruits. Wood ash from deciduous trees contained high level of Pb, As and Cu. It was found that wood ash from coniferous trees contained significantly higher levels of Pb (430 mg/kg) when compared with deciduous trees: birch (63 mg/kg), acacia (57 mg/kg), oak (39 mg/kg). The lowest level was found to be present in ash tree and apple tree (25 mg/kg). The level of As was similar in each species of tree and was on the level 25 mg/kg. Significant differences were observed in the concentration of Cd. The highest content of this metal was observed in the case of oak (29 mg/kg), afterwards in birch (13 mg/kg), coniferous tree (9 mg/kg). Significantly lower level was determined in acacia, ash tree and apple tree (2 mg/kg). The concentration of Hg was low in each wood ash – this element volatilized during combustion process. Also, the level of micronutrients was compared (Table 8). The highest level of Fe contained coniferous trees (1.5 %), lower level was present in deciduous tree (0.40.6 %). The highest level of Mn was found in birch and acacia (1.6 %) as well as in oak (1.1 %). Lower level (0.2-0.4 %) was found in ash and apple tree as well as in coniferous tree. Ash and apple tree contained significantly higher levels of Zn (4800 and 5600 mg/kg, respectively). Coniferous tree and birch contained 3000 mg/kg. Oak and acacia 500 mg/kg. Very high level of Cu was found in coniferous tree (500 mg/kg). Deciduous trees, including oak, birch, acacia and ash tree contained 170 mg/kg. Significantly lower level was present in apple tree. The highest level of B was found in apple tree (800 mg/kg). The level of this element in wood ash from other trees was similar – on the level of 500 mg/kg. Birch ash was the richest in cobalt (24 m/kg), afterwards ash from coniferous tree (13 mg/kg), oak, acacia and ash tree (7 mg/kg). The concentration in apple tree was below 5 mg/kg. The highest concentrations of Mo was present in wood ash from oak, acacia and coniferous tree (above 3 mg/kg), lower levels were found in birch, ash tree and apple tree (below 2 mg/kg) [145].

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Table 7. The elemental composition of ashes from various tree species and soil [184] Element

Unit

Al As B Be Bi Co Ca Cd Ce Cr Cu Fe Ga Ge Hg K La Mo Mg Mn Na Nb Ni P Pb Pd Rb Rh Sb Sn Th Ti Tl U V Zn Zr

% mgkg-1 mgkg-1 µgkg-1 mgkg-1 mgkg-1 % mgkg-1 mgkg-1 mgkg-1 mgkg-1 % mgkg-1 mgkg-1 µgkg-1 % mgkg-1 mgkg-1 % % % µgkg-1 mgkg-1 % mgkg-1 µgkg-1 mgkg-1 µgkg-1 mgkg-1 mgkg-1 µgkg-1 mgkg-1 µgkg-1 µgkg-1 mgkg-1 mgkg-1 mgkg-1

Oak

Birch

Apple tree 0.849 0.233 0.147 21.94 19.12 19.80 344.87 510.65 257.36 535.08 382.72 254.72 1.37 60.26 ≤0.0005 7.29 13.34 4.79 31.14 29.36 35.11 7.82 23.27 1.674 1.78 2.397 0.909 75.90 16.30 5.79 111.37 143.13 96.81 0.58 0.53 0.56 7.75 84.77 66.26 1.60 24.08 24.52 6.30 0.01 ≤0.0001 4.85 6.25 5.16 1.11 2.31 0.666 2.807 0.960 1.280 0.96 2.51 5.16 0.999 1.691 0.191 0.21 0.16 0.19 521.49 419.38 362.32 87.66 37.80 46.98 0.85 1.97 1.15 32.09 103.07 25.190 653.23 448.54 580.49 478.20 141.30 37.17 20.44 ≤0.0006 29.19 2.63 0.516 1.02 1.76 0.351 0.346 ≤0.0006 ≤0.0006 ≤0.0006 258.92 293.85 236.93 75.60 0.05 0.00 28.80 15.51 6.45 0.00 ≤0.03 ≤0.03 227.70 4903 756.30 1.08 1.208 0.770

Ash

Coniferous tree 1.76 0.717 23.61 23.15 520.88 274.27 473.03 601.18 ≤0.0005 177.40 7.230 15.23 24.30 19.82 3.23 16.03 2.917 4.874 5.69 82.82 175.52 123.09 0.48 2.36 87.89 84.62 20.73 43.41 ≤0.0001 ≤0.0001 12.26 3.43 1.99 10.39 0.419 1.95 2.77 1.35 0.236 0.775 0.24 0.86 315.65 8107.00 102.47 53.11 2.19 2.11 42.62 690.14 718.64 538.22 157.60 177.46 12.05 11.49 0.49 14.61 0.230 2.321 ≤0.0006 ≤0.0006 255.98 2941.45 0.06 118.89 17.97 39.98 ≤0.03 20.26 577.60 5020 0.769 7.54

Soil 0.635 63.88 24.27 468.63 4.213 4.897 2.32 0.266 6.491 25.33 24.23 0.970 77.37 30.18 95.29 0.454 3.1956 1.741 0.251 0.0471.34 0.122 1396.65 10.84 0.169 15.17 566.67 22.34 ≤0.0006 4.626 1.37 0.0015 675.02 15.17 47.48 5.124 117.22 6.532

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Also, among wood ashes originating from different geographical regions differences in the elemental composition were encountered. For instance, the concentration of Pb in oak varied from 14 mg/kg (Silesia, Poland) to 87 mg/kg (Lower Silesia). The level of Cd from 1.4 mg/kg (Lesser Poland) to 52 mg/kg (Silesia). The concentration of As from 21 mg/kg in Lower Silesia and Central Poland to 40 mg/kg in Silesia. The level of Cr varied from 3 mg/kg (Greater Poland) to 76 mg/kg (Central Poland), Sn from 0.3 (Lower Silesia) to 75 mg/kg (Lesser Poland). It could be stated out that wood ash is a good indicator of environmental pollution. It is possible to elaborate a map of environmental pollution on the basis of analysis of wood ash from the same tree species from geographically different regions [146]. Agricultural studies showed that wood ash can be also used as soil amendment and deacidifying agent. It can be used as the source of potassium and also neutralizing agent in the production of fertilizers. The fertilizer components present in wood ash have relatively low solubility due to alkaline pH and it could be stated out that it can act as slow release fertilizer. All the components are released slowly: macronutrients, micronutrients and also toxic metals. Toxic metals present in wood ash possess low solubility and thus low bioavailability. Moreover, wood ash can also be used to decrease bioavailability of toxic metals present in soil due to alkalization properties and thus will reduce the effects of environmental pollution [143, 147, 183-186]. Bioavailability of nutrients and toxic elements was assessed. It was found that bioavailability of all metals, except potassium was very low i.e., Cd <2 %, Pb<1 %. The supplementation of ash into soil raises pH and this greatly reduces bioavailability. That is why, ash can be considered as slow release fertilizer. The other advantage is that supplementation of wood ash reduces solubility of macronutrients, micronutrients and toxic metals and this reduces elution of these elements to ground waters (Table 8). The applicability of wood ash as soil supplement was confirmed by germination tests. Study showed that the mostly advantageous is to supplement 5 % wood ash to soil [184]. The effect of supplementation with ash is increase of pH and this causes retention (immobilization) of macronutrients, micronutrients as well as toxic metals in soil and this reduces the intensity of their cycling in the environment and thus causes less damage [184].

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Table 8. The comparison of the composition of wood ash and soil (a), extraction efficiency (b) and bioavailability (c) of elements from ash, soil and soil supplemented with ash [184]

Macronutrients and micronutrients the level of which was higher in wood ash when comparing with soil Macronutrients: K (15 times higher content in ash than in soil), Ca (13 times), Mg (11 times), P (10 times), Na (2.5 times) Micronutrients: Cd, Pb, Bi, Ni, Tl.

The extraction efficiency of the following elements increased after addition of wood ash to soil K, Sb, Mo, Rb, Ge, B, V, Ga, Na, Cr, U

Availability of the following, elements increased with the increase of the level of ash supplementation Co, Zr, U, Sb, V, Cu, Ce, La, Ge, Ti, Nb, Fe, Sn, Ga, As, Pb, Cd, Pd, Ni, Mn, Zn

(a) Elements the level of which was similar in ash and in soil Cr, Nb, La, Ti, Al, Pd, Ga Fe, Be, V, Sb, Ge, Sn, Mo

(b) The extraction efficiency of the following elements reached maximum at intermediate level of ash supplementation (5-10 %) Al, Cd, Zr, Ni, Nb, Co, Zn, Mn, Pb, La, Ce, Be, Rh

Availability of the following, elements decreased with the increase of the level of ash supplementation Rb, Ti, Cr, Al, Ca, P, Mg, Bi

Toxic elements the level of which was lower in ash when comparing with soil Hg (91 times), Zr (3 times), As (3 times), Ag (3 times), Ce (2.5 times), U (2 times)

The extraction of the following elements decreased with increase of ash supplementation Ca, Mg, P, Tl

(c) Availability of the following, elements did not changed with the increase of the level of ash supplementation Mo, K, B

The extraction efficiency of the following elements did not change after addition of wood ash to soil As, Cu, Fe, Ti, Bi, Sn

The following elements were available from soil (extraction efficiency was higher than 5 %) Mo, K, Sb, V, Ti, Rb, Cr

The following elements were available from ash (the level of supplemen tation 5 %) Mo, K, Rb

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6.4. IDENTIFICATION OF METAL CYCLES IN TROPHIC CHAIN The aim of studies that included balances of metals cycles in animal breeding was the assessment of bioavailability of elements supplemented in livestock feeds in order to assess distribution of microelements as well as to point out sites of potential accumulation of toxic metals in animals’ organs and products. The level of macroelements, microelements and ultratrace elements was determined in feeds, physiological fluids, droppings, muscles, liver, kidneys, lungs and skin, as well as in livestock products, such as milk and eggs. Also, the composition of animal hair and feather was analyzed [132]. Bioindicative value posses cow milk, poultry eggs, some tissues and organs of livestock. Ducks, geese and hens are housed in many countries in extensive (free range) system. These animals are omnivorous and for this reason can be considered as a good biomonitor of environmental pollution [132]. The content of microelements and trace elements has recently been more widely studied, in particular in industrialized and polluted regions, milk is considered as a good biomonitor of pollution of agricultural environment. The concentration of the major mineral components in milk (Ca, P, K, Na, Mg,Cl, S) does not fluctuate. The total concentration of these elements in milk is 0.6 %. Also, the concentration of some trace elements is relatively constant, including Ni (0.03 mg/L), Fe (0.5 mg/L), Si (1.4 mg/L). The level of As, Cd, Hg and Pb strongly depends on environmental pollution and the level of these toxic metals should be monitored in milk [136] (Table 9). Table 9. Permissible levels of toxic metals in some animal products [mg/kg or mg/L] [136] Animal product Milk and milk products Meat of mammals and poultry Animal fat Liver Kidney Hen eggs

Pb 0.02 0.10 0.10 0.50 0.50 0.30

Cd 0.01 0.05 0.02 0.5 1.00 0.05

Hg 0.01 0.02 0.01 0.05 0.05 0.02

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The concentration of 38 microelements and trace elements in milk from cows kept in farms located in industrialized region was compared with milk from an ecological farm. The differences in the concentration of the following microelements and trace elements were encountered: I, Al, Rb, Ti, Mn, Ga, Se, Ge, Co, Cs, W, Th [136]. Animal products from industrialized region influenced by the activity of copper smelter and refinery were analyzed for the content of toxic metals and their concentration was compared with the permissible limits. It was found that the concentration of Pb in milk exceeded the allowed standards. Average reported value was 0.03 mg/kg and the maximum value was 0.08 mg/kg. The concentration of Pb in blood was 0.04 mg/kg (maximally 0.2 mg/kg). Positive statistically significant correlation between the concentration of Pb in milk and blood was denoted. Also the content of Hg in milk was significantly and positively correlated with Hg level in blood. The highest concentration of Hg was denoted in liver (0.005 mg/kg), lungs (0.04 mg/kg) and muscles (0.003 mg/kg). The concentration of Hg in eggs from laying hens housed in a farm was 8 times lower when compared with the free range system [139]. The concentration of 37 trace elements in 25 samples of raw milk and full blood of cow milk was investigated with the use of ICP-MS technique (Table 10). Correlation coefficients between 18 elements in milk and blood were determined. Statistically significant correlation between the concentration of a given element in blood and milk were observed for the following metals: Rb, Ti, Mn, Ga, Ni, Ge, Mo, Sb. No statistically significant correlation between Cr, As and Se level in blood and milk was denoted. The concentration of the following elements was significantly higher in blood when compared to milk: Cu, Ga, Ge, Ti. Lower concentration of Ag, Th and Be was found in blood. The concentration of Cr, Se and Sb was similar in blood as it was in milk. Among the studied microelements and trace elements, milk contained the highest level of Zn (3.3 mg/L), afterwards I (0.6 mg/L), Rb (0.6 mg/L), Al (0.3 mg/L) and Ba (0.2 mg/L). Full blood contained Zn (2.6 mg/L), Cu (0.6 mg/L), I (0.4 mg/L) and Rb (0.16 mg/L). In milk, high variability of Cr, Cu, Ge, Mo, Rb and Se was observed. Similarly in blood: Al, Be, Cr, Mn, Mo, Ni and Rb. Microelements and trace elements that were found in milk and blood originated from soil, feed, water and air. Of course, the concentration of a given element in animal tissues depends on its bioavailability and on inter-element interactions, including synergisms and antagonisms. However, the mechanism of transport of minerals to milk has not been well understood yet. It is thought to be complex, consisting of simple diffusion, active or facilitated transport [134].

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Eggs, similarly as milk, muscles and organs of animals, are indicator of environmental pollution. In particular, in the case of eggs from waterfowl birds (Table 10), it can be an indicator of water pollution. Not only the content of a given metal in the whole egg is considered, but also eggshell itself, as well as egg albumen and yolk possess bioindicatory values. Eggshells can be used first of all in biomonitoring of As and Cu, egg yolk to assess environmental pollution with As and Cd and egg albumen to bioindicate Cd, Hg, Pb and Cu. This theory was confirmed in industrialized regions and in eggs from so-called ecological farms. Eggs from industrialized area contained significantly more As, Hg and Cd and more Pb and Cu when compared with non-industrialized regions [132]. Physical and chemical eggs quality parameters from industrialized and nonindustrialized regions from young (< 1 year old) ducks and geese from several farms were investigated. It was found that morphological characteristics were similar, including average mass, share of shell, albumen and yolk that were typical. Toxicological studies however showed diversified concentration of metals in various morphological parts as well as in whole eggs. Statistically significant differences were observed between polluted and ecological region. The highest concentration of As was present in geese eggshell (2.4 mg/kg) and the lowest in ducks egg albumen (0.003 mg/kg). The concentration of As in duck and geese eggs (whole eggs and in its elements) was up to 8 times higher in industrialized region. Geese eggs contained 25 % more As than ducks. Arsenic is easily absorbed by geese but is also easily and quickly excreted in droppings. The acceptable concentration of As in egg content (egg yolk and albumen) is 0.20 mg/kg. In industrialized regions was evaluated as 0.13 mg/kg and eggs from an ecological farm contained 0.07 mg/kg [132]. Waterfowl eggs are also good biomonitors of cadmium pollution. Similarly as in the case of As, geese eggshell contained the highest levels of this element (0.045 mg/kg) and the lowest level was present in albumen of ducks eggs. It was found that the concentration of Cd in eggs from industrialized region was up to 13 times higher when compared with ecological. Geese eggs contained averagely 5 times higher levels of Cd when compared with duck eggs. Similar dependencies were found in the case of Pb, Cu and Zn. Eggshells were found to be better biomonitor of environmental pollution than egg content, since the level of metals is several times higher [132]. Moreover, it was found that the level of toxic metals was higher in animals and their products kept in free range system when compared with battery system.

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Table 10. The average content of trace elements in cows milk and blood (μg/l) [145] and in eggs of waterfowl birds (μg/kg) [131] Waterfowl birds Geese Ducks Industrialized Agricultural Industrialized Agricultural Raw milk Full blood region region region region 276.5 66.8 32.8 24.6 14.6 8.2 75.1 32 217.2 69.8 1413 737 602 804 4.5 4.9 26.7 4.4 10.5 2.6 6.5 4.6 84.9 77.6 23 4 5 8 79.6 620.8 596 510 797 653 64.5 104.3 28.2 70.8 1.56 2.03 55.1 10.5 137 39.7 559.6 387.9 74.3 27.7 240 122 308 223 11.5 5.4 61.0 13.0 17.4 31.2 113 20.6 75.1 42.9 579.0 163.7 5.5 5.3 60.5 51.8 91 57 47 52 78.8 156.2 84.5 70.6 3307 2575 8280 9230 9777 8993 Cows

Element Al As Ba Cd Co Cr Cu Ga Ge Hg I Mn Mo Ni Pb Rb Sb Se Ti V Zn

One issue is to measure the level of toxic metals in biological tissues as in biomonitors and the other is to elaborate methods that will reduce accumulation of these pollutants. A method that would enable to reduce bioaccumulation of toxic metals (including Pb, Cd and Hg) in body tissues and animal products was elaborated. The preventive detoxification preparation can be applied in cows and poultry breeding. Feeding animals with the prepared supplements inhibited transfer of toxic metals to animal products, including meat, eggs and milk.

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Katarzyna Chojnacka Table 11. The elemental composition of hens bones and feather [185] a) macroelements, %

Macroelement N P2O5 K2O

Bones 4,07 18,5 0,911

Feather 10,4 0,457 0,331

b) microelements and toxic elements, mg/kg

Element Al As B Be Cd Co Cr Cu Fe Hg Mg Mn Mo Ni Pb Ti Tl V Zn

Bones 28,4 1,06 0,720 0,333 0,100 0,005 3,31 ≤ 0, 37 62,4 0,0064 1048 1,73 0,26 ≤ 0,004 0,286 2,41 ≤ 0,0009 ≤ 0,02 53,5

Feather 119 0,68 ≤ 0, 15 ≤ 0,002 ≤ 0,009 0,0009 0,78 6,65 227 0,0204 182 10,2 ≤ 0, 01 ≤ 0, 04 4,08 3,38 ≤ 0,0009 0,48 105

The supplement consisted of humic materials and aluminosilicates that have complexing, sorptive and ion-exchange properties and are capable to bind cations, such as Cd, Hg and Pb. The supplement consisted mainly of humic materials (humodetrynite – brown coal) and aluminosilicates (bentonite, baidelite). The preparation was also supplemented with selenium yeasts, plant oil, mineral additives (including chalk, phosphates and dolomites). The preparation is intended to be used in poultry and cows feeding. Feeding livestock with humicaluminosilicate preparation resulted in 23 % decrease Cd concentration and 33 % decrease of Hg concentration in milk and 13 % and 10 %, respectively, in whole

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blood of cows. In poultry, 29 % reduction of Cd concentration in muscles was observed, 50 % in liver and Pb decreased 34 % and 70 %, respectively. Also, the concentration of Pb and Cd in eggs was significantly lower [139]. Methods of animals detoxification should be based on either metal-binding properties of feed supplements or on antagonistic interactions between elements. Such an example of an antagonism is selenium and mercury. Mercury is present in milk products in the following concentrations: in milk 1.7 μg/L, muscles 1.5 μg/kg and in eggs 2.0 μg/kg. Selenium is present in the concentration 34 μg/L, 43 g/kg and 22 μg/kg, respectively. In an organism of animals and human selenides of toxic metals are formed and this is one of the method of their rendering harmless. Mercury selenide is insoluble and therefore if this compound is formed, mercury does not become incorporated into metabolic processes [135]. Also, hens feather can be considered as a good bioindicator of environmental pollution, similarly as human hair. Toxic metals are also deposited in bones. The composition of bones is also related with the level of environmental pollution, but the method of determination is invasive. Table 11 presents the elemental composition of hens heather and bones [185].

Chapter 7

USING BIOSORPTION AND BIOACCUMULATION PROCESSES IN WASTEWATER TREATMENT There are different classes of biosorbents (Figure 11). Low-cost sorbents include wastes, by-products and useless materials as well as naturally collected biomass. Sorption capacity of such sorbents is not high, but since the materials are practically of no cost, it is possible to work at high concentration of sorbent. Lowcost sorbents include use-less materials of plant and animal origin. The class of biosorbents of plant origin includes the biomass of terrestrial plants (leaves [186], grass and straw [187]) that are easy to harvest and are abundant in the environment and the biomass of aquatic plants (duckweed [188-189] and crystalworth [189-190]) and macroalgae (including Cladophora [191-192]). Biosorbents of animal origin are i.e., grinded waste eggshells [193] or animal bones [194]. High cost sorbents are materials specially propagated for sorption purposes. Since the costs are high, there will be also special requirements towards these materials. High-cost sorbents should simultaneously possess high sorption affinity and capacity (sorbent 1 on Figure 8), so very low concentrations of these materials will bind high quantities of metals yielding simultaneously very low final concentration of metal ions (below 1 mg/L). Hence, high-cost sorbent should simultaneously possess very high sorption capacity and affinity. The subsequent desired characteristic is regenerability of the sorbent, so the material can be used in several biosorption cycles. These criteria fulfill, e.g., microalgae Spirulina sp. that can incorporate up to 20 % mass metal ions at very low residual concentration of metal ions in solution [195].

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Figure 11. Low-cost and high-cost biosorbents.

Biosorption can be performed in an ordinary continuous stirred tank reactor (Figure 12). Since the rate of the process is quick, the residence time can be short (0.5-1 h). This enables to treat large volumes of wastewater in a reactor of small dimensions. It is advantageous to simultaneously recover and recycle the biomass. Biosorption can also be carried out similarly as typical ion-exchange, in columns. Biosorbent can be either directly packed or immobilized in a matrix. Working on at least two columns enables to switch between sorption and desorption (sorbent regeneration) process without the necessity of stopping the process. The possibility of sorbent regeneration is an economic solution. Very significant is to select the proper filtration device that enables to work at high fluxes over long period of time. Biosorption can be performed by immobilized biosorbents. Disadvantages include additional costs, higher mechanical diffusion resistance, lower capacity, interaction of carrier with active sites [10]. An alternative solution would be a membrane reactor which assures confined space for free cells and enables continuous separation of the biomass from the solution [105].

Biosorption and Bioaccumulation Processes in Wastewater Treatment

Figure 12. Schematic diagram of biosorption process.

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Figure 13. Schematic diagram of bioaccumulation process.

The efficiency of the overall biosorption process can be examined through the evaluation of concentration factor between the metal concentrated in the biomass related to effluent or by the level of metal in eluent stream related to the concentration in raw wastewater. If we consider the first definition of concentration factor, the values reached are 10-1000, if we relate to the second definition the values would be 1-100. This means that starting i.e., with the initial concentration of metal ions 21 mg/L in raw wastewater, by using the quantity of sorbent 1 g/L, and with the concentration of metal ions in treated effluent 1 mg/L the metal would be concentrated almost 1000 times in the biomass. If we would like to furtherly regenerate the biomass, with e.g., acidic solution using 10 ml of eluent to wash 1 g biomass (assuming 100 % elution efficiency), we obtain solution containing 2000 mg/L metal ions, which means that the metal was concentrated almost 100 times when comparing it with raw wastewater. The solution of eluent containing metal ions can be furtherly treated with a conventional method, such as precipitation, ion exchange, electrodialysis, membrane separations. If bioaccumulation is used as a method of wastewater treatment, it requires simpler installation when compared with biosorption, since both growth of cells and binding of metal ions occur simultaneously: in the same place and time, in a single bioreactor (Figure 13). In bioaccumulation it is possible to partially recover the biomass – metal ions bound passively with the cellular surface can be

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desorbed from the biomass, similarly as in biosorption. The disadvantage of the process is that the residence time in bioaccumulation is longer than in biosorption and that nutrients are required to sustain metabolic processes and cellular growth. A problem that might occur is that the presence of pollutants can inhibit cellular growth and thus biomass productivity.

7.1. WASTEWATER TREATMENT BY LOW-COST BIOSORBENTS Eggshells Recent findings showed that eggshells can be considered as low cost biological sorbent. Waste eggshells are significant environmental problem and it would be advantageous to find an application for this material. Only in USA, 120 000 Mg of waste eggshells is annually generated and disposed to landfills. Eggshells mainly consist of calcium carbonate (85-95 %), magnesium carbonate (1.4 %), phosphorus (0.8 %) and organic matter. This material contains also traces of Na, K, Zn, Mn, Fe and Cu. It has been postulated that, similarly as calcite and calcareous soil, which are of similar chemical nature, eggshells should be good biosorbents with the dominating mechanism of biosorption as ion-exchange. It was found that in fact biosorption capacity of eggshells was high: 20-160 mg/g depending on conditions. The effect of process parameters: temperature (20-60 o C), pH (3-5) and sorbate concentration (100-300 mg/L) on process kinetics was investigated. The equilibrium of the process was reached after 1 hour. Increase of pH resulted in increased sorption capacity and sorption rate. The highest differences were observed between pH 3 and 4. At temperature 20-40 oC sorption capacity was not influenced by temperature, at higher temperature the efficiency decreased. The effect of temperature on sorption rate was adverse. On the basis of kinetic study, the proposed parameters for sorption were pH 5, temperature 20 oC, sorbate concentration 300 mg/L. This yields biosorbent capacity 56 mg/g at sorbent concentration 5 g/L. Also, the effect of pH, temperature and sorbent concentration on biosorption equilibrium was investigated. Similar dependencies as in kinetic experiments when considering process efficiency were determined. Increased sorbent concentration favored decreased sorption capacity. It was found that the best process parameters for biosorption by eggshells are pH 5 and 20 oC [193].

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The experimental results were described with pseudo-second order kinetic equation, the model that is the most frequently used in modeling of biosorption kinetics. The process equilibrium strongly depends on sorbent concentration. A new mathematical model being a modification of Langmuir equation was proposed:

⎛ bCeq qeq (Ceq , C S ) = q m ⎜ ⎜ 1 + bC eq ⎝

⎞⎛ ⎟⎜1 − C S ⎟⎜ d + C S ⎠⎝

⎞ ⎟⎟ ⎠

(3)

The first part of the equation is typical Langmuir equation, the second is an

⎛ bC eq ⎞ ⎞ ⎟ . At ⎟⎟ →1 and qeq→ q m ⎜ ⎜ 1 + bC ⎟ eq ⎠ ⎝ ⎠ ⎝ ⎛ CS ⎞ ⎟⎟ will be low, as well as the high sorbent concentration, the value of ⎜⎜1 − ⎝ d + CS ⎠ ⎛

empirical dependence. If CS→0, ⎜⎜1 −

CS d + CS

value of the overall sorption capacity. At a given sorbent concentration, the model would be alike Langmuir equation. Model parameters at various process conditions were determined. The model fitted the experimental data reasonably well [193]. On the basis of performed experiments it was concluded that it is possible to remove high quantities of metal ions with eggshells. It was possible to decrease the concentration of Cr(III) ions below the acceptable level (0.5 mg/L) at pH 5, 40 o C, initial concentration of Cr(III) ions 100 mg/L and sorbent concentration 15 g/L [193]. Since ion-exchange was hypothesized to be the mechanism of biosorption by eggshells, cation exchange capacity was determined by potentiometric titration and evaluated as 4.4 meq/g. It was found that cations are bound to carbonate groups. The value of sorption capacity was two times higher than of activated carbon, similar as of animal bones [194] and two times lower than for especially propagated biosorbent (Spirulina sp.) [195]. The problem however that should be resolved is sterilization of eggshells. But, since the mechanism is ion-exchange, it should be possible to recover the sorbent and use it several times [193].

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Animal Bones Animal bones are another waste product that requires utilization. The material consists of 65-70 % inorganic substances including mainly hydroxyapatite Ca10(PO4)6(OH)2 and organic matter, mainly fibrous protein collagen. The postulated mechanism of sorption by hydroxyapatite was ion-exchange with Ca2+ ions. The effect of sorption parameters on biosorption rate and efficiency was investigated. At initial concentration of Cr(III) ions 200 mg/L and sorbent concentration 1-15 g/L, it was possible to remove 40-99 % of Cr(III) ions from the solution. It was found that increasing pH and temperature resulted in increase of sorption capacity. pH was found to be a very important process parameter since influenced protonation of metal binding sites, affected calcium sulphate solubility and metal speciation in the solution. Sorbent concentration had the influence on equilibrium pH and phosphates solubility. But this effect is not so strong as in the case of eggshells. Sorption capacity strongly increases with pH increase. Also, increasing temperature results in higher efficiency of the process up to 50 oC. Above this temperature, sorbent denaturation occurs. The rate of biosorption by animal bones is slightly slower than by eggshells. The equilibrium is reached after 2.5 h. The highest efficiency of the process was reached at pH and 50 oC (over 190 mg/g). At 20 oC sorption capacity was 60 mg/g [194].

Biomass of Terrestrial Plants – Leaves, Grass and Wheat Straw Sorption of Cr(III) ions by dry leaves of Forsythia intermediata [186] grass and wheat straw [187] was investigated. The maximum experimentally determined biosorption capacity of all the sorbents was similar, within the range 5.5-25 mg/g depending on the process parameters (pH and temperature). The values of sorption capacity were not high, but since these materials are commonly abundant and practically of no cost, it is possible to improve wastewater treatment efficiency by increasing the concentration of the sorbent. The equilibrium was reached after 40-60 min. Similarly as in the case of other sorbents, sorption capacity depended on temperature and pH. The best performance of this sorbent was reached at 50 oC, pH 5. Pseudo-second order model was used to describe kinetics of the process carried out by all the sorbents of plant origin. Langmuir equation was used in equilibrium modelling of leaves and grass and Freundlich equation in the case of wheat straw. The dominating mechanism of all the sorbents was mainly physical adsorption with maximum 20 % contribution of ionexchange. Since the sorbents possess high heating value (20 kJ/g) and low ash

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content (7-9 %), after the combustion of metal-laden biomass it is possible to obtain both energy and ash being a concentration of metal [186-187].

7.2. WASTEWATER TREATMENT WITH HIGH-COST BIOSORBENTS Algae Spirulina sp. Microalgae Spirulina sp. were found to have very high sorption capacity – up to 200 mg/g. The kinetics of the process was described with reversible first-order kinetic equation and the process equilibrium with Langmuir model. It was found that cells cultivated at various process conditions had different sorption capacity [196]. The highest metal ions binding capacity possessed cells grown photoautotrophically (7 meq/g), afterwards heterotrophically and the lowest cells grown mixotrophically. Biosorption of three toxic metals to the biomass of this algae was carried out. Cells bound the highest quantities of Cr(III) ions, afterwards Cu(II) and Cd(II). Adsorptive surface area of cells was low 0.3-1 m2/g, however cation-exchange capacity of cells was very high (9 meq/g). For this reason, the mechanism of the process was identified as ion-exchange. It was found that cation-exchange capacity determined by potentiometric titration and biosorption capacity was directly proportional. Three groups capable of cationexchange were identified on the cellular surface: carboxyl, phosphoryl and amino or hydroxyl group. The contribution of each group in biosorption was confirmed by chemical modification. Cells with blocked groups exhibited lower biosorption capacity corresponding with the cellular concentration of the blocked group. Also, the possibility of desorption of bound ions from the biomass and subsequent reuse in another sorption cycle was investigated. The efficient sorbent that was identified was 0.1 M nitric acid. The application of 0.1 M acid solution assured almost complete desorption of bound cations from the biomass with the simultaneous restoration of sorption properties. Also, the effect of pH on biosorption performance was studied. This furtherly confirmed the participation of cation-exchange with functional groups in the biosorption process [195].

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7.3. THE APPLICATION OF BIOACCUMULATION IN WASTEWATER TREATMENT Bioaccumulation is the property that can also be used in the removal of toxic metals from solutions. The method can find an application in treatment of industrial effluents. It is particularly advantageous to employ this treatment as the final, polishing step, since frequently the application of traditional methods does not make it possible to lower concentration of toxic metals below limits permissible by law. Since industrial effluents generally do not contain organic carbon source, it would be advantageous to employ photosynthetic organisms that can incorporate carbon to the biomass from carbon dioxide or carbonates. Bioaccumulation understood as wastewater treatment technique is the method of cultivation of cells in the presence of substance that is to be bioaccumulated. Therefore, only aquatic organisms can be employed in bioaccumulation-based wastewater treatment processes. The potential application in such methods can find microalgae – photosynthetic and aquatic organisms that posses high metal binding capacities, such as Spirulina sp. [197]. The alga was used in the treatment of effluents from copper smelter and refinery that contained toxic metal ions in trace concentrations (however in concentrations slightly exceeding the acceptable levels), contained ammonia nitrogen and phosphorus and carbon only in the form of carbonates. The studies showed that the treatment of this effluent via bioaccumulation by Spirulina was efficient and yielded effluent with the desired concentration of toxic elements (including Hg from 760 to 216 μg/L, cadmium from 3810 μg/L to 917 μg/L at initial concentration of cells 0.4 g/L. Also, the concentration of ammonia nitrogen (from 66 mg/L to 0.6 mg/L) and phosphorus was lowered [197]. The same effluent was also treated with natural zeolites [198]. Similar performance was achieved towards Hg ions, but the concentration of ammonia nitrogen has not decreased significantly in the process [198]. Concluding, bioaccumulation assures simultaneous removal of various pollutants, including toxic metal ions and nutrients (compounds of nitrogen and phosphorus).

Chapter 8

USING BIOSORPTION AND BIOACCUMULATION IN INTEGRATED PROCESSES It is advantageous to combine biosorption and bioaccumulation into integrated production processes. It is possible to perform wastewater treatment with the simultaneous production of biological feed additives, if wastewaters do not contain high levels of toxic metals, such as Hg, Pb and Cd (Figure 14). Such an approach enables to manage waste sludges, which is metals-laden biomass, from wastewater treatment. Recently it was found that livestock feeds should be supplemented with deficient microelements. Therefore there is the need to elaborate a method of production of cheap and highly bioavailable mineral feed additives. Such a possibility offers the application of biological sludges from treatment of wastewater by biosorption and bioaccumulation techniques. Such an approach can solve several problems: wastewater treatment, utilization of waste biomass, production of commercially valuable product (mineral feed supplement) (Figure 14 a). If the treated wastewater contains toxic ions that are not microelements (Hg, Pb, Cd), the metals removed can be concentrated either in liquid-state form with the regeneration of the biomass (Figure 14 b) by elution or in solid-state form as the result of biomass ashing. The obtained biomass concentrates (either liquid or solid) can be used in the production processes of a given metal if it is possible (metal recovery) or can be utilized with conventional methods.

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Biosorbent or bioaccumulator

Metal-laden biomass of sorbent Wastewater treatment Treated effluent

Wastewater To surface water or soil

(a) Liquid-state concentrate of metal ions Elution Biosorbent or bioaccumulator

Conventional methods of wastewater treatment

Metal-laden biomass of sorbent

Ashing

Treated effluent

Solid-state concentrate of metal ions

Wastewater treatment Wastewater To surface water or soil

(b) Figure 14. Integrated processes using biosorption or bioaccumulation processes; a) low level of Cd, Hg and Pb in treated wastewater, b) high levels of Cd, Hg and Pb in treated wastewater.

8.1. ENVIRONMENTAL BIOTECHNOLOGY OF MICROALGAE Environmental biotechnology of microalgae is a new discipline that proposes integrated processes with the use of microalgae, including methods associated with environmental protection. In integrated processes, the biomass is cultivated in effluents containing biogenic compounds (C, N, P) with the use of CO2 (e.g. from flue gases) and the energy of sun (Figure 15). The biomass produced can be used as animal feed, biosorbent, biofertilizer and in the production of chemicals (i.e. colorants). This enables to combine the processes of wastewater and flue gases treatment with the simultaneous production of low-cost product of commercial value [199].

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Flue gases containing CO2

Effluents containing biogenic compounds (C, N, P)

Microalgal biomass

feeds biosorbents pharmaceuticals colorants bio-fertilizers

Light Figure 15. The concept of Environmental Biotechnology of Microalgae – integrated process of biomass culture and wastewater and flue gases treatment [199].

When designing such an integrated process, it is necessary to investigate the growth of microalgae and the effect of pollutants on growth kinetics and statics. Microalgae are organisms that are capable of using various sources of carbon (either inorganic or organic) and energy (either sunlight energy or energy stored in organic compounds). If algae use carbon dioxide and the energy of sun they grow photoautotrophically, if utilize organic compounds as the source of both carbon and energy – grow heterotrophically, if the observed growth is the sum of both processes – grow mixotrophically. A growth model in each metabolic mode was proposed [200] that consisted of the part that described the effect of organic carbon source (i.e. glucose) with typical Monod equation and the effect of light intensity with linear discontinuous model. The contribution of each constituting metabolism on the overall observed growth was investigated [201]. The possibility of microalgae to grow with the use of various metabolisms and different growth substrates makes their growth very flexible and enables them to adjust growth requirements to growth conditions. Also, the method of cells cultivation is significant since, as it was found, affects biosorption properties of cells [196]. The effect of growth parameters (light intensity, initial concentration of glucose) on metal ions binding capacity was investigated. Cells cultivated at high light intensity and at low concentration of organic carbon source showed the highest metal binding capacity. Biomass cultivated with a single metabolism showed higher sorption capacity when compared with mixed metabolism, e.g., autotrophically grown cells possess two times higher capacity than mixotrophic biomass. It was found that with the increase of glucose in the growth medium, sorption capacity decreased in heterotrophic and mixotrophic metabolism.

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Increased light intensity favors synthesis of cells with higher biosorption capacity, however does not affect biosorption capacity of mixotrophically grown biomass. However, each type of Spirulina biomass possessed very high metal binding capacity (200 mg/g of Cr(III) ions for photoautotrophic cells). Since biosorption properties depend on growth conditions, when designing biosorption unit, significant would be not only high biomass productivity, but also high biosorptive quality of the produced biomass. It is necessary to take into consideration that at high glucose concentration, productivity of the biomass is higher, but sorption capacity would be lower and also biomass yield from substrate would be low [196]. There are some problems associated with photosynthetic cultivation of the biomass for biosorption purposes. While many classical physiological studies focus on the response of an organism to a single parameter, physical, chemical and biological parameters interact and vary independently in nature, thereby producing non-linear effects. Optimal conditions seldom occur in nature and thus physical factors, such as temperature, light or availability of nutrients and water regulate performance of species. Adaptation resulted in that populations tend to evolve characteristics that make them well suited to the particular conditions experienced over extended period of time [202]. In natural lakes, if the concentration of cells is high (exceeds ca. 1 g/L) the energy of sun would be available only to cells present in the top layer of the lake surface. The remaining biomass would experience deficiency of sun energy. Thus, cells tend to achieve low, but constant cells concentration, so the species can survive generations. In this case, self-control of cells concentration would be an adaptation strategy. While this characteristic is highly advantageous in the natural environment, it would cause severe problems in large scale biomass cultivation on commercial scale [202].

Chapter 9

USING BIOSORPTION AND BIOACCUMULATION TO TREAT MICROELEMENT HUNGER Deficiency of microelements in the diet of human and animals, similarly as deficiency of micronutrients in plants causes the problem of so-called hidden hunger. This is the global problem of over 2 billion people [203-204]. A traditional method to overcome this was the use of microelement mineral diet supplements (for animals and human) and mineral fertilizers (for plants). A landmark in microelement supplementation may turn out the processes of biosorption and bioaccumulation which enable to produce food biofortified with microelements, either of plant or of animal origin. It is well known that biologically bound form of microelements is the healthiest and the safest form, in particular when comparing with mineral salts. Recently in the literature there were found information that food biofortified with microelements can be produced by: 1. Excessive bioaccumulation of micronutrients by plants by either excessive soil or foliar fertilization or by the selection or creation of genotypes which are able to accumulate high levels of microelements in edible parts of crops, or by using biofertilizers which enable to access soil pools of micronutrients which are normally not available to plant. 2. Supplementation of livestock diet with biological forms of microelements, obtained be enrichment of various types of biomass (eg. yeasts or algae) with these constituents. Biological form is more available than mineral. Resulting, the obtained meat or dairy (eggs, milk) products would contain higher density of microelements. Among microelements, malnutrition with first of all iron, iodine and zinc is the most serious problem [205]. The aim of biofortification is supplementation of deficiency of these microelements in diet through the production of biofortified

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plant and animal food. The task of biofortification is to solve the problem of microelement hunger, which is related rather with bioavailability of microelements, but not with their general concentration. Biofortification should be particularly used if biodiversity of food in human diet is poor [206]. The problem of microelement hunger occurred due to reduced variety of food products as well as due to environmental changes related with erosion of biodiversity [205]. This is also the problem of highly developed countries where increase of cases of diabetes, obesity and heart diseases was recently observed [207-208]. The World Summit for Children, 1990 [209] elaborated a strategy concerning the reduction of deficiency of various components of diet, in particular of iron, iodine and vitamin A. An important element of this strategy was biofortification of food – elaboration of techniques enabling producing biofortified grocery products, the issues related with its supply and selling [210]. Recently some studies were carried out on enrichment of plant or animal food with microelements to improve their nutritional values. Biofortification is a new term describing novel approach towards the production of agricultural products with increased content of mineral components. Biofortified food contains more microelements. In the case of consumption of such food there is no need to supplement diet with microelement supplements. Such a method was used in the enrichment of rice in iron and zinc and also to supplement the diet of laying hens with the preparation consisting of edible algae enriched with microelements by biosorption [211]. By using this new preparation it was possible to improve the content of microelements in eggs content and also in meat. The additional advantage was that hens and eggs were larger [211]. Another approach is to identify genes potentially responsible for the possibilities of increasing microelements concentration in edible parts of plants. Such a possibility should offer transgenic plants in the future [212]. Increased bioaccumulation of micronutrients could be also achieved by the application of biofertilizers which facilitates availability of minerals present in soil by eg. increasing the size of roots, extending it by mycorrhizae or by the activity of microbes in the root zone which transfers micronutrients into more soluble forms by symbiotic relationships.

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9.1. USING BIOSORPTION AND BIOACCUMULATION IN THE PRODUCTION OF FEED SUPPLEMENTS WITH MICROELEMENTS FOR LIVESTOCK TO PRODUCE BIOFORTIFIED ANIMAL FOOD Literature [213-215] reports that livestock feeds should contain 21 elements: Ca, P, Na, Mg, K, Cl, S, Se, Mo, Fe, I, Mn, Cu, Co, Zn, I, Ni, V, Cr, Sn. The goal in rational feeding of livestock in intensive breeding systems is the coverage of not only the basic nutrients and energy rations. Recently, a particular attention is paid to mineral constituents. As far as conventional feeds cover requirements for the basic nutrients and energy, they are deficient in macro- and microelements. These minerals need to be additionally supplemented. The content of microelements in natural feeds frequently does not cover requirements of animals for these constituents (Table 12). Such a situation takes place in particular in the case of cultivation of plants on soils deficient in micronutrients. Microelement deficiencies in feed are corrected by using mineral feed additives, frequently in the form of mineral salts, since such preparations are the cheapest. This has been practiced for years. However, recent studies showed their poor availability and adverse health effects. The problem of conventionally used inorganic feed additives is low bioavailability, possibility of toxic effects, the problem of uniform mixing of this very concentrated form of microelements. So, there is a high probability of posing either deficiency or overdosing. Microelements in such form are of transit character – are excreted and only a small quantity is absorbed by the organism. Recently, also environmental consequences of using inorganic feed supplements were detected. Elevated content of microelements (which are also classified to the group of toxic metals) in manure was detected. The problem of transit character concerns first of all such microelements as Cu, Fe and Zn (excreted with feces) as well as Mn and Se (excreted with feces and urine) [216], bioavailability of which from inorganic formulations is very low.

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Table 12. Recommended level of microelements in feed for swine and laying hens [213, 217-218] Microelement

Animal

Iron (Fe) Zinc (Zn)

swine swine laying hens swine laying hens swine swine laying hens swine laying hens swine

Manganese (Mn) Copper ( Cu) Iodine (I) Selenium (Se) Cobalt (Co)

Recommended level (mg/kg d.m feed) 50-60 50-60 30-40 20-30 40-50 4-5 0.15 0.35 0.2 0.08 0.0-0.5

Farm and industrial feeds do not meet livestock demands for minerals, in particular for microelements. Impoverishment of cultivated land in mineral components as a result of intense agricultural production, caused that plants became deficient in micronutrients. This yielded mineral deficiencies in livestock that were manifested by decreased growth rate and health problems in particular in intense breeding systems. Currently, minerals are supplied to livestock diet in the cheapest form – as inorganic salts. This can cause health problems to animals. Also, supplying minerals to livestock as inorganic salts is of environmental concern, since this form is characterized with low bioavailability and such minerals are rather of transit character. Thus, we could expect uncontrolled, elevated discharge of microelements (such as Zn, Cr, Cu) that are also considered as water pollutants, into manure. For this reason, there is a need to search for a new generation of mineral feed supplements that would be highly bioavailable and that would show no toxic effects and that would be economically advantageous [219]. Since all biological materials possess metal binding properties (characteristics that has been used so far in wastewater treatment and bomonitoring), theoretically, all biomaterials can be used as microelements carriers in supplying minerals to livestock diet. This would greatly improve bioavailability since biologically bound minerals would be similar to the natural form in which they are present in feeds. Also, biological materials to which microelements are bound possess additional nutritional value (vitamins, polyunsaturated fatty acids, high protein contents). It was found that supplementing i.e., algae in livestock diet would improve egg yolk color [219].

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On the market, two types of food and feed supplements are available: inorganic forms and the forms bound with an organic carrier: vitamin (eg. niacin in polynicotinate) or an amino acid derivative (eg. picolinic acid, a derivative of tryptophan, in picolinate) [220]. The latter is thought to be better absorbed by the body. Literature also reports that organically bound metals show better biological activity and are less toxic at higher concentrations when compared with inorganic salts [221]. There are market needs for modern mineral feed supplements for livestock which would supply microelements in highly bioavailable form, would not pose toxic effects and would be cheap. Such criteria are fulfilled by biological materials, which are good sorbents and accumulators of minerals. It would be also advantageous to control proportions between particular elements in livestock diet. Due to its ability to incorporate metals by biosorption and bioaccumulation, the biomass can be used as a delivery vehicle in metal supplements. Literature reports that bioavailability of microelements could be increased by supplementation in the form the mostly similar to natural, since absorption by animals from natural sources is the highest [222]. Therefore, it is necessary to search for new feed additives among the materials of biological origin. The elaboration of new mineral feed supplements for livestock and implementation of the product to industrial practice is much easier than pharmaceutical products for human, since nutritional supplements adhere to far fewer and significantly less stringent regulations [220]. New chances offer the processes of biosorption and bioaccumulation of microelements to biological materials. These methods have already found an application in the processes of wastewater treatment as well as for reclamation of precious metals (eg. gold from sea water). These processes use natural properties of organisms, under controlled conditions and enable to increase their intensity and efficiency [224]. Metal binding processes by the biomass is complex and depends on metal ions chemistry, surface properties of the biomass, physiology and physico-chemical effects of the environment [225]. The processes would enable to enrich the biomass with microelements. Another issue is to select the biomass which would be the carrier of microelements. The properties of the biomass which is a good candidate to become mineral feed supplements include: 1) good nutritional value 2) good biosorption/bioaccumulation properties – the biomass should bind microelement cations quickly and efficiently 3) availability and common occurrence in nature.

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The above criteria are fulfilled by the biomass of algae, which possesses good properties of binding metal cations (as reported in literature on wastewater treatment), it would be possible to enrich the biomass in microelement cations. Important is that algae are approved by international law as the components of animal (and also human) diet [226]. Another class of organisms which are candidates to be used as biological feed supplements are yeasts.

The role of microelements in livestock breeding In the past century it was confirmed that many microelements are essential to animals and that their deficiency could be considered as a global problem. Since then, microelements (zinc, copper, manganese, iron, cobalt) are routinely supplemented to livestock diet [227]. In the past, many mistakes have been made in microelement nutrition of animals [223]. Microelements are essential but can also be toxic, depending on the dose and form. The majority of metals, such as Fe, Cu, Co, Mn, Zn and Cr are essential for the proper development of animals. Their deficiency causes severe diseases. However essential elements at higher doses are frequently toxic [228].

Mineral feed supplements In the previous years it was found that it is the mostly advantageous to supplement microelements in biologically or organically bound form [229]. Increased interest in chelated or organic forms (complexes, chelates, proteinates), which are characterized with higher bioavailability and are non-toxic to animals is observed [223]. Literature shows an example of shells of mollusks Conchifera [230]. On the market, there are also available chelates and amino acid complexes, proteinates and polysaccharide complexes of microelements [222]. However, the cost of these additives is 10 times higher than of inorganic preparations (mineral salts) [229]. Microelements bound with organic carriers, such as different macromolecules of biological materials should have better absorbability and should be less toxic [231]. Natural products – of plant or animal origin are the basic feeds in feeding livestock. A serious problem is a variable content of mineral substances in plant feeds. It depends on livestock species, agrotechnical factors (fertilization) and geochemical characteristics. The problem of deficiency of micronutrients in

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fertilization of plants was belittled for many years. The consequence was deficiency of these components in soil and also in the biomass of plants which are used as the components of feed. As the result, deficiency of microelements in animals caused decrease of the growth rate and diseases. Imbalances in the level of microelements are related with significant health risks [220]. Mineral salts – this is currently the main source of microelements (inorganic salts: chlorides, sulfates, carbonates etc.) and their organic compounds with low molecular acids: formic, lactic, propionic etc. [230]. Inorganic preparations were found to have poor availability and toxic side effects [232]. Mineral complex compounds – complexes of microelements with organic components, amino acids, proteins, starches etc. Organic forms of microelements - There is a possibility of using chelates or complexes as feed supplements with microelements. Trace elements supplied in the form of protein, amino acids (with lysine or methionine) or polysaccharide complexes offer significantly higher bioavailability, stability and solubility when compared with inorganic form. On the market, there are currently available 4 groups of organic forms of microelements (according to AAFCO (Association of American Feed Control Officials) [233]: complex of microelement with amino acid, chelate of metal ion with amino acid, metal proteinate, complex of metal with polysaccharide. The above compounds differ with strength and the type of bonds between metal and organic compounds. Chelates are specific complexes of metal ions with amino acids with strong, double covalent bonds [234]. An advantage of using these compounds is high stability and fastness under variable conditions (intestine, stomach), as well as easiness in overcoming intestine barrier. It is important that into tissues they are transferred in unchanged form. Amino acids chelates can be used with the following microelement cations: Cu, Zn, Mn, Fe. The advantages of using such form instead of mineral salts include: better homogeneity of the feed, lower tendency for segregation, better durability of amino acids (absorbability from chelates is ca 65 % while from inorganic sources 4-22 % [234]). Chelates bind easily with digestive enzymes containing mineral components and facilitate absorption and utilization of amino acids on cellular basis [235-236]. Complex of protein and microelements contains a single covalent bond and therefore these products are less stable.

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Living organisms as mineral feed supplements enriched with microelements by biosorption and bioaccumulation Living organisms (algae, yeasts) can bind high quantities of microelement cations. This ability depends on the type of an organism and bound cation (Table 13). Beside that properties of metal ions binding from solutions by the biomass are well known, the processes are mainly used in industrial wastewater treatment [224]. Literature reports only few examples of binding microelements to cells to be used as mineral feed supplements. In elaboration of new technologies, efficient solutions can be found by observation of naturally occurring processes. By carrying out natural reactions in closed and fully controlled system, it is possible to use biomolecules and their natural properties of metal cations binding in industrial processes of removal of heavy metal ions from effluents or in the production of bio-preparations (mineral feed supplements). Table 13. Microelement cations binding capacity by living organisms [224] a) Biosorption capacity of microorganisms

Metal ion

Cr3+

Cu2+

Microorganism

Type of the biomass

Bacillus- biomass Rhizopus arrhizus Candida tropicalis Streptomyces nouresei Penicillium chrysogenum Candida tropicalis Cladosporium resinae Rhizopus arrhizus Saccharomyces cerevisiae

bacteria fungi yeasts filamentous bacteria fungi yeasts fungi fungi yeasts

Maximum biosorption capacity (mg Me/g d.m. cells) 118.04 31.03 4.59 1.80 0.33 80.01 18.00 16.00 20.00

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Table 13. (Continued) b) Biomass and biosorbents – the comparison of cation-exchange capacity Species Ascophyllum sp. Eclonia radiata Rhizopus arrhizus Sargassum sp. Peat moss Spirulina sp. Cation-exchange resins

Type of the biomass brown algae brown algae filamentous fungi brown algae peat moss microalgae

Biosorption capacity [meq/g] 2-2.5 1.8-2.4 1.1 2-2.3 4.5-5.0 2.0-11.4 0.35-5.0

Yeast as feed additive Yeasts can be used as feed additives in the form of: - Dead cells as easily absorbed source of vitamins and minerals and oligosaccharides which play important role in stimulation of immunological system [237]. - Living cells which through biological control of digestive system improve health condition of animals. In feeding livestock, Candida and Saccharomyces yeasts are used. They are cultivated especially for livestock feeding purposes, by using various industrial wastes as the components of growth media [238]. Literature reports examples of using fractions of inactive cell walls from yeasts as sorbent, the source of nutrients (sacchcarides, amino acids, B group vitamins). Organic compounds produced by yeasts (selenium-yeasts) are good and available source of selenium [238]. Stabnikova et al. [239] used yeasts in biotransformation of selenium. Under appropriate conditions, yeasts accumulated large quantities of this element by incorporation into organic selenium-containing compounds (eg. selenomethionine), which is the best source of selenium for living organisms. Literature reports that the biomass of yeast enriched with microelements is a new and safer solution of prevention of microelement deficiencies in animals, since microelements supplied in biological form are less toxic and have better absorbability in organisms [240-241]. Yeast enriched with eg. selenium can be used as a supplement for humans [242] and animals [243]. The biomass serves also as the additional source of proteins, essential amino acids and vitamins [241]. The production of metal enriched biomass of yeast includes disolving salt of a given metal in the growth medium, followed by heat treatment to stop yeast

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growth and inhibit enzymatic activity. Metal becomes incorporated into cells of yeast by the production of metal-binding proteins (metallothioneins), mineralization and sequestration to vacuoles [220]. Pan et al. [240] investigated enrichment of yeast Saccharomyces cerevisiae, Candida intermediata and Kluyveromyces marxianus with iron. The maximum ion binding capacity was 13, 20 and 34 mg Fe/g dry wt., respectively. Hossain et al. carried out studies on the assessment of influence of yeasts enriched with chromium (1 g/kg) on the growth of broilers. Feed was supplemented with Cr-enriched yeasts on the level 0-600 μg/kg. Supplementation of 300-400 μg/kg, increased the ratio of feed consumption to body weight increase was observed [244]. However, in the case of using yeasts as biological carrier of microelements in livestock feed. Although, it was necessary to kill the cells, due to the possibility of causing mycosis in livestock.

Algae and aquatic plants as feed additive Algae and aquatic plants as primary producers and also as very efficient biosorbent and bioaccumulators in their natural living environment are able to concentrate metal cations in their biomass. Enriched algae (microalgae: Spirulina sp. [224], Chlorella sp. [245], and macroalgae Enteromorpha sp. and Cladophora sp. [211] and aquatic plants (Lemna minor [188] and Riccia fluitans [189]) have the potential to be used as condensed form of biologically bound microelements, because: 1. posses very good cations binding properties (biosorption and bioaccumulation) 2. are approved as the component of diet of human as well as livestock [222]. 3. beside microelements, contain other nutritionally valuable components which have advantageous influence on the health of animals and human The biomass of algae consists 2/3 of the biomass on the Earth. Algae embrace over 40,000 species and carry out 50 % of global photosynthesis. Algae were one of the most important components of diet in ancient civilizations and are still being consumed by human. Algae are classified into two categories: macroalgae (seaweeds, eg. Sargassum) and microalgae (cyanobacteria, eg. Chlorella sp., Spirulina sp.). Both groups of algae are used in feeding livestock

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and human, as fertilizers, as raw materials in the production of biochemicals and pharmaceuticals. Microalgae are considered as good feeding materials due to high content of protein (500-700 g CP/kg), poly-unsaturated fatty acids (LA, GLA), vitamins, pigments (eg. C-PC, APC, carotenoids) and minerals [246-247]. Among microalgae and other materials of plant origin, Spirulina sp., contains the highest level of protein. It is produced on commercial scale and is used as the supplement in the diet of human. The content of minerals in the biomass of algae is significantly higher than in the products of plant or animal origin. The concentration of microelements in the biomass can be controlled through the selection of environmental conditions [248]. The biomass can be enriched in microelements via biosorption or bioaccumulation processes and then the content of microelements in the biomass can increase up to 6-10 % (w/w) [245]. The biomass of algae for many years has been used as the component of diet of human and animals due to high content of protein and minerals. The content of protein changes depending on species and environmental conditions [249]. Microalgae which are the most frequently used in livestock feeding include Spirulina sp. and Chlorella vulgaris [250]. Forecasts predict that in the nearest future using algae in diet would become more popular. Many works are devoted to the assessment of the possibilities of feeding livestock and the assessment of the possible toxicity of algae. These studies pointed out on the possibility of using algae as the components of valuable feeding materials, since algae have high nutritional value. The most frequently are used as a substitute of protein (eg. fish meal) [251]. Many strains of algae are cultivated on industrial scale. It is thought that their production is cheap, since use sunlight as the source of energy and CO2 as the source of carbon. Some of them can also use organic carbon source, which makes it possible to cultivate algae in either heterotrophic or mixotrophic mode, under sterile conditions. Elastic metabolism enables algae to live in various environments. Both macro- and microalgae can be also cultivated under fully controlled conditions – in artificially illuminated photobioreactors. Biomass productivity can be furtherly increased by using additional organic carbon source. Disadvantageous effects of algae as the component of livestock diet have not been found. However, it is necessary to mention two groups of animals: monogastric and ruminants. Monogastric are not able to digest cellulose plant materials (eg. cell wall of Cholorophyceae contains cellulose, but blue-green alga Spirulina – does not). Ruminants (cattle, sheeps) can digest cellulose materials due to the presence of an enzyme cellulase [252]. Particularly advantageous when considering the potential to be used as feed additives is Spirulina sp.

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Literature reports examples of using algae as feed supplements. The objective of the majority of works concerned the assessment of the maximum supplementation level. It was found that adding the biomass of Chlorella vulgaris [250], Spirulina, Scenedesmus and Spongiococcum [252] to the diet of chicks in the quantity of 0.2 % resulted in 10 % increased body weight [250]. Chickens fed on diet containing algae were healthier. Those animals had 16 % lower level of cholesterol. It was also shown that chicken can be fed with diet containing up to 20 % of macroalgae in their diet. In the case of feeding laying hens, it was found that egg yolks contained more pigments, in particular β-carotene and xanthophylls [250]. Planes et al. [248] carried out studies on bioavailability of magnesium from microalgae Spirulina, containing higher concentration of this element. The results were promising. Microalgae were also successfully used in feeding of Pacific oysters, shrimps [253], fish [254] and swine [255] in order to intensify livestock breeding [253]. Huang et al. [247] enriched the cells of Spirulina platensis with selenium as nutritional and potentially therapeutic additive. Inorganic selenite was bio-transformed by this alga into organic forms by adding sodium selenite to the growth medium. Selenium was bound to proteins, lipids, polysaccharides and other cell components. S. platensis was a very good Se-carrier [247]. Nutritional requirements of algae are small. In their cultivation, inorganic growth media are used – solutions containing macro- and microelements. Algae, similarly as plants, use sun light as the source of energy and carbon dioxide serves as the main building material for algal cells. However, in order to reach satisfactory growth rate, the proper temperature is required. Optimal temperature, the most frequently lies within the range 15-35 ºC. Since algae are cultivated in aqueous solutions, it is necessary to construct the proper cultivation pond which should be shallow, so light energy would be used efficiently by algae. The cultivation systems should be constructed in the way that the maximum ratio of illuminated surface per volume would be reached. In warm climate, algae can be cultivated in open systems, while in colder climate it is advantageous to cover the pond with a glasshouse. Such a solution would assure higher temperatures (the system would be less susceptible to low temperatures at night) and would lower the risk of contamination [224]. The main cost in the production of mineral feed supplements would be biomass cultivation. In the case of microalgae, the biomass can be cultivated in so-called algae farms, where in shallow ponds, occupying large surfaces, algae are cultivated on industrial scale. One of algae producers is an American company Cyanotech [224].

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The biomass of macroalgae could be obtained directly from water reservoirs (seas or lakes), using the natural sites of their occurrence. Realistic seems separation of a given space of sea and fishing algae. It is also possible to use similar fishing techniques, as in fish fishing. There have also been constructed special algae harvesters [224]. Also, aquatic plants enriched with microelements by biosorption and bioaccumulation can be used as mineral feed supplement. Microelements important in livestock feeding (Mn, Zn, Cu, Cr) were bound to the biomass of commonly worldwide available freshwater floating aquatic plant Lemna minor (duckweed) [188] and Riccia fluitans (liverworth) [189]. The plants are commonly used as valuable feed and possess capability to concentrate metal ions from solutions several fold (1000-100000 times). These plants are also used in hydrobotanical wastewater treatment plants. It is also possible to combine treatment of wastewaters containing i.e., Cu or Zn ions with either algae or aquatic plants with the simultaneous production of mineral feed supplements. Such an approach enables to simultaneously solve environmental problem (wastewaters) and to produce commercially valuable product. Since photosynthetic organisms are used, there is no need for effluents to contain organic carbon source [188-189]. Biosorption and bioaccumulation in single- and multi-metal system was compared. It was found that aquatic plants can bind up to 8 % microelements in their biomass. The equilibrium was described with Langmuir equation. The mechanism was found to be ion-exchange mainly with K, Ca, Mg. The highest performance was reached in single-ion system [188-189]. Table 14 lists model parameters for equilibrium of biosorption and bioaccumulation in single- and multi-metal system [188]. In another study [211], feeding experiments were performed with the new preparation, consisting of the biomass of an edible marine algae Enteromorpha prolifera and Cladophora sp. fortified with microelements (Cu(II), Zn(II), Co(II), Mn(II) and Cr(III)) by biosorption. The biomass enriched with Cu(II) contained 35.2 g/kg of Cu(II), with Zn(II) - 18.1 g/kg, with Co(II) - 21.2 g/kg, with Mn(II) 17.3 g/kg, with Cr(III) - 54.8 g/kg. The applicability of the preparation was tested in feeding experiments on laying hens, which were conducted on 5 experimental groups and 1 control group. In the control group, microelements were supplemented in the inorganic form, whereas in experimental groups Cu(II), Zn(II), Co(II), Mn(II) and Cr(III) were replaced by macroalgae enriched with a given microelement. Supplementation of bio-metallic feed additive to the diet of laying hens resulted in higher microelement transfer to eggs. The new preparation improved eggs weight, eggshell thickness as well as body weight of hens. The

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preparation was found to have very good properties because it not only increased the content of microelements in edible products, but also had advantageous effect on health condition and production yield of both egg and meat. It was concluded that the new preparation can be used in biofortification of eggs or meat with microelements. This kind of biofortified products could be applied as a new type of functional food, which would supplement microelements deficiencies in human diet as food instead of mineral salts [211]. Table 14. Langmuir Parameters for biosorption and bioaccumulation by both non-growing and growing cells of L. minor [188]

qmax (meqg-1) b (lmeq-1) R2 qmax (meqg-1) b (Lmeq-1) R2 qmax (meqg-1) b (lmeq-1) R2

Single-ion system Multi-ion system Cr Cr Cu Mn Biosorption 3.40 1.40 0.738 0.364 0. 298 4.98 1.33 3.2 0.983 0.977 0.964 0.991 Bioaccumulation by non-growing cells 2.46 0.773 0.0869 0.287 0.267 5.11 37.6 2.53 0.932 0.977 0.948 0.964 Bioaccumulation by growing cells 1.72 1.26 0.116 0.321 0.287 1.84 26.9 0.605 0.937 0.952 0.958 0.967

Zn 0.514 2.66 0.992 0.301 6.55 0.972 0.326 2.22 0.982

9.2. USING TECHNIQUES LEADING TO EXCESSIVE BIOACCUMULATION OF MICROELEMENTS IN THE PRODUCTION OF BIOFORTIFIED PLANT FOODS Bioaccumulation of micronutrients by terrestrial plants – a method of food biofortification Biofortification is the process of production of food which is rich in bioavailable microelements through the use of either conventional techniques of selection of plant varieties or through genetic modifications [206]. Not every plant can be enriched by biofortification. Good candidates are grains, rooted vegetables, rhizomes and bananas. Those are considered as cheap, common and available foods. This is of particular importance if biofortification of

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stable foods is used in developing countries [206]. The main factors which determine bioaccumulation of ions by plants are complex and involve not only absorption by roots from soil solution, but also their chemical form in soil, as well as physical and chemical interactions between roots of plants and soil [256]. Various works show that regulation of bioaccumulation of micronutrients of edible parts of plants varies and depends on the plant species and micronutrient itself [257-258]. It was found that there exist three distinctive mechanisms of micronutrients absorption by plants. The first is transport by carrier molecules present in external membranes of cells. Two subsequent include: mechanism of low selectivity, activated at high concentration of ions and highly selective transport which occurs at low level of ions in soil solution [259-260]. The existence of both high affinity and highly selective carrier proteins was confirmed, as well as non specific channels enabling quick and passive transport of ions through the membrane [256]. In micronutrients bioaccumulation a dominating role plaid by complexation with soil clay was underlined [261]. Si, B and Mo are strongly bound with hydroxides of Fe and Al of various charge by the mechanism of exchange of oxyanion ligands of their weak acids with hydroxyl groups present on their surface [262]. This concept was widened by specific binding with oxycations of hydrated micronutrient cations in soil [263-264].

Interaction of roots with soil Physical as well as chemical properties of roots of plants influence bioaccumulative properties of micronutrients from soil [256]. Some plants show better bioaccumulation properties. This concerns first of all Fe and Mn. Many soils contain sufficient levels of these micronutrients in the form available to many plants. Calcareous soils however tend to immobilize Fe and Mn and in this case it is indispensable to supply these constituents by foliar fertilizers, to supplement micronutrients and do not cause their deficiencies. Mn, Zn and also other micronutrients are not readily transported from shoots or between particular parts of roots, probably causing malfunction of an organism of plant a whole on soils deficient with micronutrients [265]. This probably causes higher susceptibility to diseases [266]. Additionally all the metallic micronutrients strongly react with soils. In the case of their supplementation to the surface layer of soil, they might become not available in the period of drought. The problem specifically concerns Cu and wheat [267].

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Biofortification of plants with micronutrients – a strategy against malnutrition Currently research is carried out on agronomic techniques increasing the concentration of microelements. Recently, non-transgenic rice biofortified with iron was produced and is currently tested as the component of human diet in order to check the efficiency in anemia treatment [212]. Increased concentration of microelements in grain to be consumed by human can significantly reduce the problem of microelements (Fe, Zn, Cu, I) deficiencies in diet. Literature reports that by fertilization of plants with inorganic or organic forms of micronutrients, it is possible to greatly increase their concentration in grains. It was shown that the mostly efficient form of biofortificaton was soil fertilization (for Zn and Cu), foliar (for Fe) and by addition of fertilizer components to irrigation water (I) [258]. It is necessary to pay special attention, that over-fertilization does not take place. This may cause toxic effect and decrease the quantity and the quality of crops. The efficiency of various agricultural treatments, the aim of which is to increase the concentration of microelements depends on the type of soil, the cultivated plant, the method of cultivation, crop rotation and other environmental factors [258]. An important issue is to asses how increased level of fertilization with micronutrients influences both micronutrients bioaccumulation by plant, but also crop yields. In many cases the optimum fertilization rate with micronutrients in order to reach the optimum crop yield is significantly lower than the level which assures higher density of micronutrients in plant. Consequently many studies are needed in the future to assess optimal conditions for both plants growth and bioaccumulation. Of concern here are also environmental factors, since micronutrient cations are also considered as toxic metals. Perhaps the future in microelement biofortification of plant food lies in hydroponic culture, which can be totally isolated from the environment and would not cause environmental pollution. At present increased attention is being paid to enrichment of eg. grains with microelements, for the consumption mainly for human. In the future, valuable would be biofortified plant feeds for animals which would yield animal food biofortified with microelements. There is a need to elaborate new agronomic measures (quantity, time, the site of dosing, the form of fertilizer, crop rotation etc.) as well as the method of cultivation. An important issue is the proper selection of concentration (the density, the quantity of fertilizer component per unit of eg. grain) in the case of cultivation of grain for human consumption, related to the content of microelements (the total quantity of fertilizer component per grain or plant) [258].

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The aim of the majority of agronomical techniques is reaching efficiency closed to the theoretically possible under given environmental conditions. Increased doses of micronutrient fertilizers in soils deficient in these components should yield high crop efficiency. Contrary to this, the concentrations of Zn and Fe in grains increase along with the increase of Zn and Fe application rates. For this reason, the quantities of Zn or Fe used in fertilizers when compared to the quantities required by plant to reach 90 % (or even 100 %) of the optimum growth may lead to increased concentrations of micronutrients in grain [258]. This is a new approach. Until now, the only aim of micronutrient fertilization was not to increase the density of these constituents in crops, but to increase the crop yield [268]. In micronutrient bioaccumulation, important is the stage of plant development. As grain develops, the concentration of micronutrients in seed depends on the type of soil, availability of elements, plant species and in the lower extent on the time of season and the method of cultivation [268].

Changing micronutrients density by fertilization with macronutrients Global fertilization is dominated by the coverage of plants requirements for fertilizer macronutrients N, P, and K [269]. These nutrients improve the growth rate of root system and shoots, increase binding of all the nutrients by plant, also micronutrients. Additionally, common use of macronutrient fertilizers in order to increase crop efficiency, causes that micronutrients are better absorbed [258]. Beside this, nowadays it is a common practice to supplement macronutrient multicomponent fertilizers with micronutrients [270-271]. Purposeful enrichment of multicomponent fertilizers with micronutrients can be used to increase the content of micronutrients in human diet. In Finland, the concentration of selenium in soil is low and so food crops cultivated on these soils do not cover requirements of human for this element, causing increased risk of diseases of cardiovascular system and some types of cancer. Consumption of selenium by human was increased by the addition of sodium selenate to fertilizers [272]. Higher concentration of macronutrients in grains is related with increased level of micronutrients. Correlations between the density of micronutrients and the concentration of phosphorus, as well as between the concentration of micronutrients and the level of protein in grains of T. aestivum, O. sativa and G. max were detected. In T. aestivum, correlations between the density of Fe and Zn in grains and the level of protein were statistically significant [273-274]. In G. max these correlations were smaller and weaker [275]. The domination of positive

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correlation coefficients suggest that fertilization the aim of which is to reduce deficiency of the content of micronutrients has weak but positive influence on the density of micronutrients in plants.

The role of micronutrient fertilizers in increase of the density of micronutrients in edible parts of consumption plants Micronutrient deficiencies influence disadvantageously the crop yield and are difficult to be eliminated, because [258]: 1. 2. 3. 4.

There exist high periodical and spatial variability in availability of micronutrients. The majority of micronutrients introduced to soil is quickly transformed into forms which are not available to plants. Nutrients which are added to soil do not readily enter the soil profile. The majority of micronutrients supplemented in the form of foliar fertilizers is not efficiently transported in the direction of roots. Therefore, deficiencies might occur.

Soil fertilizers The application of soil fertilizers with Zn caused 2-3 times increase of the concentration of Zn in various grains depending on species and genotype [276278]. Also, the type of soil influences the increase of Zn level in grain as the consequence of soil fertilization. Soils rich in organic matter, fertilized with Zn did not cause increased bioaccumulation of this micronutrient, because of adsorptive properties of organic matter in soil. Hence, Zn was not readily bioavailable to plants. Differently in the case of sandy soils which are poor in organic matter. Here soil constituents did not adsorb Zn. The micronutrient was thus present in the soil solution and available to plants [279-280]. In contrast to Zn, soil application of inorganic forms of Fe on soils deficient in Fe is the most frequently not effective, due to rapid transformation of Fe(II) into Fe(III). The latter is not available to plants. On the other hand, using synthetic chelates of Fe for the correction of deficiency of this element appeared to be efficient, but also costly [281]. Long-term fertilization with CuSO4 and ZnSO4 (cumulative application) did not result in increased level of Cu in grains of corn, while the level of Zn

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increased only at high rate of application of this element [282]. In studies on alkaline soils, high pH reduced phytoavailability of Zn, as well as Cu. However, above a certain supplementation level, further increase of supplementation caused decrease of crop yield, but also reduced micronutrients density in grains [283]. Even in the case of application to soil below the toxic dose, micronutrient fertilizer does not cause linear increase of the density of micronutrients in grain.

Foliar fertilizers Plants may accumulate soluble compounds and gases by leaves [258]. This phenomenon is based on fertilization by leaves spraying [284]. In foliar fertilization, it is assumed that supplied nutrients will be bioaccumulated and exported from the site of application (leaf) to the site of use (usually growing tissues). Cuticle of leaf is the first main barrier in micronutrient bioaccumulation by plants. In the case of Fe, Zn and Mn, used in chelated form or in the form of sulfates, efficient binding by cuticle in the site of dosage was proved [285]. Absorption of these three components by leaves was lower from chelates than from inorganic salts, but translocation in an organism of plants was better if chelated forms were used. Export of micronutrients from leaves, but also transport down the stem occurs mainly in phloem, but the transport up of stem may take place in either phloem or in xylem. For instance, Zn applied foliarly accumulated in roots of T. aestivum, suggesting good transport downwards [286]. Foliar fertilization with ZnSO4, Zn-EDTA (or other chelates) was applied in the cultivation of fruits and vegetables, as well as in field culture. Chelates are generally less efficient than sulfate salts [281], but relative efficiency from these two sources may depend on the stage of growth of plant [287]. Important is to take into consideration that Zn deficiency in an early stage of plant development (eg. before development of leaves to the stage when foliar fertilizer can be applied). This may cause decrease in the efficiency of grain production [288]. Soil application of Zn during sowing is the mostly preferred option, at least for T. aestivum [287]. On the other hand, foliar application of ZnSO4 in the cultivation of barley and T. aestivum at the end of vegetation season may significantly increase the content of Zn in grains [268]. It is indispensable to carry out further investigation on relation between micronutrients fertilization, micronutrients density in plant and environmental pollution [258]. While Zn bioaccumulation from the nutrients solution was more efficient than from soil [289], foliar application of Zn was even more efficient than soil supplementation, since enabled Zn transport to grain [289]. This shows that foliar

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spraying with Zn in field culture may become an efficient technique which would increase the content of Zn in grain [287].

Chapter 10

CONCLUSION Living organisms are known to interact with metals by a number of mechanisms, including binding of metal ions to cell wall and intracellular accumulation. In environmental pollution control, biosorption (by non living organisms) as well as bioaccumulation processes (by living organisms) can be used. Biosorption and bioaccumulation - based techniques and technologies can provide an alternative to conventional methods for removal of metal ions. The environmental applications of these processes include pollution prevention (wastewater treatment), pollution control (biomonitoring), decrease of damages caused by pollution through the purposeful reduction of availability of pollutants to living organisms (e.g. remediation of contaminated soils, deacidification of soils by the supplementation of wood ash, detoxification preparation for animals) with the use of knowledge on ionic synergisms and antagonisms. It is important to understand the mechanism and rules governing biosorption and bioaccumulation in order to propose and implement useful techniques and technologies. In bioaccumulation of particular significance are studies on synergistic and antagonistic effects between elements. This should enable to elaborate techniques that would reduce bioavailability of toxic metals and would result in their excretion from an organism. The analysis of the content of toxic elements in biomonitors, including animal products, such as eggs and milk, from so-called ecological agriculture and from industrial and urbanized regions showed that eggs and milk are good monitors of environmental pollution with toxic metals. It was found that these products originating from ecological agriculture contain significantly lower levels of pollutants. The analysis of animal products was shown to possess not only biomonitoring value but first of all enables to assess consumption usability of these products.

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Both processes, biosorption and bioaccumulation, can be used in wastewater treatment [290-291]. In the case of biosorption, the process is analogical to conventional sorption or ion-exchange process. In bioaccumulation, also metabolic processes occur that involve transport of metal ions into cellular interior. The first step of bioaccumulation is identical with biosorption, but here also nutrients are removed (biogenic compounds, including compounds of carbon, nitrogen and phosphorus). Also, bioaccumulation enables to reduce the level of contaminants to lower concentrations than in biosorption. Biosorption enables to solve significant environmental problem. The use of materials that require disposal or utilization (such as powdered eggshells or animal bones) in wastewater treatment, makes it doubly advantageous. If the level of toxic elements classified as toxic trio (Cd, Pb, Hg) in treated wastewater is low, metal-laden biomass containing toxic metals that are also microelements, such as Cu, Zn, Cr etc. can be used as highly bioavailable mineral feed additive with microelements. Depending on the application, different characteristics of biosorbents and bioaccumulating organisms are important. In wastewater treatment processes the aim is to remove ions from solutions down to possibly low level, below the concentration required by law. The sorbents can be classified as high-cost (especially propagated biomass) and low-cost sorbents (waste or commonly available biomass, such as plant and animal materials). If applied in wastewater treatment processes, if sorbent material is cheap or possesses no value, it is possible to lower the concentration of pollutant by the introduction of high concentration of the sorbent. In this case the mostly important would be sorbent affinity to sorbent, not necessarily very high sorbent capacity. Different objectives are desired if a material is to be used as mineral feed supplement. In this case the mostly important will be high biosorption capacity. Of course, in both cases, it would be advantageous if a biosorbent possesses simultaneously high biosorption affinity and capacity. Another practical aspect of biosorption and bioaccumulation is the production of food biofortified with microelements. This can become a milestone in the treatment of microelement hunger. Biofortified can be both: plant and animal food. The first can be achieved through the proper fertilization of plants with micronutrients (by soil or foliar fertilizers), grown either in field culture or in hydroponic system. If the goal is to bioaccumulate high level of micronutrients, it is important to set the dose of fertilizer which is higher than the optimal for the growth of plant, but is lower than the dose which causes toxic effects and hinders crop yield. The production of biofortified animal food bases on the supplementation of livestock diet with biologically bound forms of

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microelements. These new feed supplements are based on the biomass (algae, aquatic plants, yeast) which was enriched with microelements by either biosorption or bioaccumulation. The supplementation of livestock diet with microelements bound with biological carrier assures higher availability and lower toxicity, and enables to increase the content of these constituents in animal products (meat, eggs, milk). Using the possibilities offered by biosorption and bioaccumulation, it should be possible in the nearest future to substitute inorganic diet supplements with food biofortified with microelements. Biosorption and bioaccumulation can be used in integrated production processes in which it would be possible to simultaneously perform wastewater treatment, utilization of a waste product that requires disposal (waste biomass, i.e., eggshells or animal bones) and use it as sorbent of pollutants from wastewater and furtherly to use metal-laden biomass as cheap and highly bioavailability mineral feed supplement for livestock with microelements. There can be proposed various variants of the process depending on the composition of effluents. The methods proposed are consistent with the sustainable development policy [292]. The problem is of interdisciplinary character on the boundary of environmental biotechnology, chemistry, chemical technology, earth sciences, bioprocess engineering and agriculture, addressing problems such as bioremoval of contaminants from waters and for this reason, the elaboration of complete technologies requires cooperation of specialists from various disciplines.

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INDEX

A abiotic, 4 absorption, 16, 17, 29, 36, 38, 39, 79, 81, 89, 108, 119, 121 access, 75 accidents, 37 accumulation, 15, 23, 32, 45, 46, 54, 57, 95, 109 acetone, 35 acid, 7, 68, 79, 80, 81, 105 acidic, 6, 8, 13, 64 activated carbon, 66 activation, 3, 111 active site, 10, 12, 62 adaptation, 35, 74 additives, 32, 58, 71, 77, 79, 80, 83, 85, 114, 115 ADHD, 38 adsorption, 6, 67, 102, 103, 107, 116, 119 adults, 43 aerobic, 15, 21, 99, 102 aerobic granules, 15, 102 affect, ix, 34, 48, 74 Africa, 99 Ag, 5, 15, 33, 43, 44, 45, 53, 55 agar, 102, 106 age, 17, 34, 35, 36, 38, 39, 41, 43, 44, 109 agent, 35, 49, 52, 110

agricultural, 54, 76, 78, 90, 109 agriculture, 4, 95, 97, 109, 115 agrochemicals, 109, 110, 111, 114, 121 air, ix, 4, 16, 29, 32, 33, 34, 35, 37, 38, 43, 44, 45, 46, 47, 49, 55, 59, 99, 108, 111, 112, 113 air pollution, 99 alcoholics, 37, 111 algae, 16, 68, 73, 75, 76, 78, 80, 82, 83, 84, 85, 86, 87, 97, 99, 101, 106, 114, 118 algal, 21, 86, 101, 102, 106 alkaline, 49, 52, 93 alternative, 62, 95, 101 aluminosilicate, 58, 109, 110 aluminosilicates, 58 aluminum, 103 amino, 6, 15, 68, 79, 80, 81, 83 amino acid, 79, 80, 81, 83 amino acids, 81, 83 ammonia, 69 ammonium, 47 amphibia, 22, 108 anaerobic, 21, 107 analytical techniques, 35, 36, 47 anemia, 90 animal tissues, 55 animals, x, 16, 22, 23, 54, 56, 57, 59, 75, 77, 78, 79, 80, 81, 83, 84, 85, 86, 90, 95, 110

124

Index

anions, 48 antagonism, 59 antagonist, 40, 43 antagonistic, 9, 48, 59, 95 antagonists, 38 anthropogenic, 4 APC, 85 application, vii, ix, x, 7, 9, 16, 31, 32, 35, 47, 49, 65, 68, 69, 71, 76, 79, 91, 92, 93, 96, 103, 104, 105, 108, 109, 113, 114, 121 aquatic, x, 1, 22, 23, 61, 69, 84, 87, 97, 106, 114 aqueous solution, x, 86, 100, 101, 106, 107 aqueous solutions, x, 86, 101, 106, 107 arsenic, 38 arterial hypertension, 39 arteriosclerosis, 40 arthritis, 37 artificial, 12 ash, 49, 50, 52, 53, 67, 95, 111, 113 Asia, 115, 119 Aspergillus niger, 101 assessment, vii, ix, x, 2, 18, 23, 36, 37, 41, 42, 46, 54, 84, 85, 86, 99, 106 atmospheric deposition, 16 atomic absorption spectrometry, 29, 108 atomic emission spectrometry, 29 attention, 21, 39, 77, 90 Australia, 119, 121 authority, 3 autism, 38, 39 availability, 17, 74, 76, 77, 79, 81, 91, 92, 95, 97, 120

B Bacillus, 82 bacteria, 21, 82, 104 Baikal, 22, 107 bananas, 88 Bangladesh, 112 barley, 93, 119 barrier, 81, 93 battery, 56 behavior, 2, 8

behavioral disorders, 38 binding, 6, 7, 8, 9, 11, 12, 13, 14, 15, 18, 26, 35, 59, 64, 67, 68, 69, 73, 78, 79, 80, 82, 84, 89, 91, 93, 95, 100, 104, 108, 116 bioaccumulation, vii, ix, x, 1, 2, 7, 15, 16, 17, 18, 19, 21, 22, 23, 25, 26, 29, 31, 32, 47, 57, 64, 69, 71, 72, 75, 76, 79, 82, 84, 85, 87, 88, 89, 90, 91, 92, 93, 95, 96, 97, 100, 104, 105, 106, 107, 108, 114 bioavailability, vii, x, 2, 17, 18, 23, 32, 46, 48, 52, 53, 54, 55, 76, 77, 78, 79, 80, 81, 86, 95, 97, 116, 118 biochemical, 118 biochemistry, 99 biodegradation, 2 biodiversity, 76, 115 bioindicators, 17, 99 biological, ix, 2, 3, 4, 5, 6, 15, 16, 17, 18, 21, 23, 32, 34, 37, 57, 65, 71, 74, 75, 78, 79, 80, 83, 97, 114 biological activity, 79 biological control, 83 biological form, 75, 83 biologically, 75, 78, 80, 84, 96 biomarkers, 18, 106 biomass, vii, ix, x, 1, 2, 6, 7, 8, 9, 14, 15, 16, 18, 21, 25, 27, 32, 49, 61, 62, 64, 68, 69, 71, 72, 73, 74, 75, 79, 80, 81, 82, 83, 84, 85, 86, 87, 96, 97, 101, 102, 103, 104, 106, 107, 114, 117 biomaterials, 7, 78 biomolecules, 6, 82 biomonitoring, vii, ix, x, 32, 56, 95 biopolymers, 5 bioreactor, 64 bioreactors, 21 biosorption, vii, ix, x, 1, 2, 5, 6, 7, 8, 9, 10, 11, 13, 14, 15, 16, 18, 21, 22, 25, 26, 29, 31, 32, 61, 63, 64, 65, 66, 67, 68, 71, 72, 73, 74, 75, 76, 79, 82, 84, 85, 87, 88, 95, 96, 99, 100, 101, 102, 103, 104, 106, 107, 114, 117 biosorption rate, 67 biota, 17, 18 biotechnology, 72, 97, 114, 117

Index biotic, 4 biotransformation, 83 Biotransformation, 117 birds, 32, 33, 56, 57 black, 15, 35, 104 blood, 33, 36, 39, 40, 44, 55, 57, 59, 109 body, 4, 17, 18, 35, 57, 106, 108 body fluid, 37 body weight, 84, 86, 87 bonds, 15, 81 bone, 103, 112 bone density, 112 bowel, 112 boys, 38 BP, 104 brain, 41 Brazil, 42 breast, 40, 113 breast cancer, 40, 113 breeding, 54, 57, 77, 78, 80, 86 broilers, 84, 117 Brussels, 109, 110, 111, 114, 121 by-products, 6, 21, 61, 106

C Ca2+, 67 cadmium, 49, 56, 69, 102, 103, 106, 107, 109, 110 calcium, 65, 67 calcium carbonate, 65 calibration, 29 California, 107, 120 cancer, 37, 40, 91, 113 Cancer, 40 Candida, 82, 83, 84 candidates, 80, 88 capacity, x, 6, 8, 9, 10, 12, 15, 16, 18, 26, 27, 61, 62, 65, 66, 67, 68, 73, 82, 83, 84, 96, 104, 114 Capacity, 1 Cape Town, 99 carbon, 66, 69, 73, 85, 86, 87, 96, 104, 115 carbon dioxide, 69, 73, 86 carbonates, 69, 81

125

carboxyl, 6, 15, 35, 68 carboxyl groups, 35 carcinogenic, 4 carcinogenicity, 3 carcinoma, 38, 40, 111 cardiovascular, 91 cardiovascular system, 91 carotene, 86 carotenoids, 85 carrier, 62, 79, 84, 86, 89, 97 catalytic, 108 cation, 6, 7, 8, 9, 12, 14, 15, 66, 68, 82, 83 cations, 6, 7, 8, 9, 11, 12, 13, 14, 15, 35, 58, 66, 68, 79, 80, 81, 82, 84, 89, 90 cattle, 85, 116 CD, 110 cell, 5, 16, 83, 85, 86, 95 cellulose, 21, 85, 107 channels, 16, 89 chelates, 80, 81, 92, 93 chemical, 3, 6, 15, 56, 65, 68, 74, 79, 89, 97, 107, 113 chemical interaction, 89 chemical properties, 3, 89 chemicals, 5, 15, 72, 102 chemisorption, 7, 8 chemistry, 79, 97, 119 chicken, 86 chicks, 86 children, 38, 39, 41, 43, 111, 112, 113 chitin, 21, 107 cholesterol, 86 chromatography, 103 chromium, 84, 102, 103, 112, 114, 117 Chromium, 103, 104, 116 chronic, 36, 38 classes, 6, 61 classical, 8, 10, 74 classified, 3, 6, 10, 77, 84, 96 clay, 89 cleaning, ix, 16 climatic factors, 17 Co, 5, 14, 15, 21, 33, 37, 43, 44, 45, 49, 51, 53, 55, 57, 58, 77, 78, 80, 87, 104, 107 CO2, 72, 85

126

Index

coal, 58 cobalt, 50, 80, 102 collagen, 67 combustion, 49, 50, 68 commercial, 33, 34, 42, 72, 74, 85 competition, 9, 10, 11, 12, 14 complementary, 115 complexity, 11 components, 4, 29, 52, 54, 76, 78, 80, 81, 83, 84, 85, 86, 90, 91, 93 composition, 9, 32, 33, 35, 36, 38, 40, 44, 45, 46, 48, 49, 51, 52, 53, 54, 58, 59, 97, 109, 112, 117, 120 compounds, 2, 6, 15, 69, 72, 73, 81, 83, 93, 96, 108 concentrates, 21, 49, 71 concentration, vii, ix, x, 2, 4, 5, 7, 8, 9, 12, 14, 16, 18, 26, 27, 29, 32, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 48, 50, 52, 54, 55, 56, 58, 59, 61, 64, 65, 66, 67, 68, 69, 73, 74, 76, 85, 86, 89, 90, 91, 92, 96, 108, 112, 115, 117, 119 conformity, 42 Congress, iv, 110 coniferous, 49, 50 consumers, 4, 113 consumption, vii, 15, 46, 76, 84, 90, 92, 95 contact time, 7 contaminant, ix, 5, 17, 18, 32 contaminants, ix, x, 2, 5, 17, 18, 25, 26, 46, 96, 97 contaminated soils, 23, 47, 95 contamination, 32, 37, 46, 86 control, vii, ix, 1, 7, 16, 39, 40, 41, 74, 79, 83, 87, 95, 108, 112, 115 control group, 39, 40, 41, 87 controlled, ix, 16, 26, 29, 79, 82, 85 copper, 55, 69, 80, 100, 101, 104, 105, 106, 107, 110, 111, 112, 114, 119, 120 coral, 22, 107 corn, 92 coronary heart disease, 39 correction factors, 9, 10 correlation, 16, 37, 43, 46, 47, 48, 49, 55, 92 correlation coefficient, 43, 46, 49, 92

correlations, 37, 43, 45, 48, 91 cost-effective, 1 costs, 61, 62 covalent, 15, 81 covalent bond, 15, 81 coverage, 14, 77, 91 cow milk, 54, 55, 109 cows, 55, 57, 58, 109, 117 CP, 47, 85 Crassostrea gigas, 118 CRC, 99, 100, 102, 104, 118, 121 crimes, 41 crops, 75, 90, 91, 115, 118, 120 CS, 66 cultivation, 25, 69, 73, 74, 77, 86, 90, 91, 93 culture, 73, 90, 93, 94, 96, 115, 118 culture media, 118 cuticle, 93 cyanobacteria, 84 cycles, 1, 4, 46, 54, 61 cycling, 52 cystine, 35 Czech Republic, 108

D dairy, 42, 75, 116 dairy products, 42 damage, 3, 16, 52 danger, 26 deafness, 38 death, 38, 111 deciduous, 50 deficiency, 36, 37, 40, 74, 75, 76, 77, 80, 92, 93, 121 definition, 15, 64 degree, 2, 4 delivery, 79 demand, 119 denaturation, 67 density, 3, 40, 75, 90, 91, 92, 93, 112, 115, 118 Department of Agriculture, 119 deposition, 16, 35, 37, 47, 49 deposits, 4

Index dermal, 17 desorption, 62, 68 destruction, 32 detection, 29, 47 detoxification, 1, 38, 40, 44, 57, 59, 95 detoxifying, 41 developed countries, 76 developing countries, 89 development policy, 97 diabetes, 39, 40, 76, 112 diabetes mellitus, 40 diet, vii, x, 40, 41, 75, 76, 78, 79, 80, 84, 85, 86, 87, 88, 90, 91, 96, 112, 113, 115, 118 dietary, 43, 109, 110, 117 dietary habits, 43 diets, 118 diffusion, 55, 62 digestion, 32 digestive enzymes, 81 directives, 46 discharges, 17 discipline, 72 diseases, 37, 38, 39, 40, 76, 89, 91, 115 distribution, 17, 54 dosage, 93 dosing, 90 drainage, 105 dressings, 119 drinking water, 5, 38, 43 drought, 89 drugs, 33 dry, 67, 84 durability, 81 duration, 41 dyskinesia, 41

E earth, 97 earthworm, 22, 108 earthworms, 23, 108 eating, 35, 42 ecological, 46, 55, 56, 95, 110 ecology, 111 economic, 62

127

ecosystem, 4 ecotoxicology, 108 Education, vii effluent, 5, 64, 69 effluents, x, 1, 5, 9, 32, 69, 72, 82, 87, 97, 103, 114 egg, 56, 78, 86, 88 eggs, 32, 54, 55, 56, 57, 59, 75, 76, 87, 88, 95, 97, 109, 110, 115 elaboration, 34, 35, 76, 79, 82, 97, 108, 114 elderly, 40 electric power, 41 electrochemical, 100 electronic, iv electrons, 7 electroplating, 1 electrostatic, iv emission, 4, 29, 47, 100, 108 endocrine, 3 endocrine system, 3 energy, 4, 7, 68, 72, 73, 74, 77, 85, 86, 115 engineering, 97 enteritis, 39 environment, vii, ix, x, 1, 2, 4, 15, 16, 17, 18, 23, 32, 36, 37, 38, 45, 52, 54, 61, 74, 79, 84, 90, 105, 109, 110, 112, 114, 120 environmental, ix, x, 2, 4, 16, 17, 18, 23, 31, 32, 34, 35, 37, 43, 45, 46, 49, 52, 54, 56, 59, 65, 72, 76, 77, 78, 85, 87, 90, 91, 93, 95, 96, 97, 105, 106 environmental change, 76 environmental conditions, 23, 85, 91 environmental factors, 35, 90 environmental protection, 31, 32, 72 Environmental Protection Agency (EPA), 5, 37 enzymatic, 7, 84 enzymatic activity, 84 enzyme, 3, 39, 85 enzymes, 37, 41, 81 epidemiological, 36, 37 epilepsy, 41, 113 equilibrium, ix, 5, 7, 8, 9, 11, 14, 17, 21, 25, 26, 27, 36, 65, 66, 67, 68, 87, 100, 103, 106, 114

128

Index

equilibrium sorption, 27 erosion, 76 Escherichia coli, 21, 105 estrogens, 106 Europe, 117 European, 5, 22, 108, 110, 113 evidence, 119 evolutionary, 108 excretion, 32, 36, 37, 38, 40, 95 exogenous, 37 expenditures, 7 expert, iv exposure, 16, 17, 18, 23, 34, 36, 37, 38, 41, 43, 45, 46, 107, 108, 111, 116 extracellular, 21, 107 extraction, 32, 47, 53, 102, 106

F family, 45, 108 family relationships, 108 farm, 55, 56, 110 farms, 55, 56, 86 fat, 54 fatty acid, 78, 85 fatty acids, 78, 85 fear, 32 feces, 33, 77 feed additives, 32, 71, 77, 79, 83, 85, 114, 115 feeding, 58, 77, 80, 83, 84, 85, 86, 87, 105, 114, 116 females, 44, 45 fertilization, vii, 75, 80, 90, 91, 92, 93, 96, 110, 113, 120 fertilizer, 49, 52, 90, 91, 93, 96, 110, 119 fertilizers, 52, 75, 85, 89, 91, 92, 93, 96, 110, 113, 120 fibromyalgia, 40 filtration, 62 Finland, 91, 120 fish, 22, 41, 85, 86, 87, 105, 107, 108, 113, 118 fish meal, 85, 118 fishing, 87 FL, 118

floating, 87 flood, 121 flow, 100 flue gas, 72, 73 fluorine, 110 focusing, 113 follicular, 35 food, vii, x, 15, 16, 32, 35, 42, 43, 45, 46, 75, 76, 79, 88, 90, 91, 96, 112, 115, 118, 120 food products, 76 foodstuffs, 42 forecasting, 36 fortification, vii, 115 Fourier, 15 Fox, 120 free radical, 39, 40, 41 free radicals, 39, 40, 41 freshwater, 22, 87, 105, 108 Freundlich isotherm, 12 fruits, 50, 93 FTIR, 15 fungal, 6, 21, 101, 104, 106 fungi, 21, 82, 83, 103 fungus, 14, 21

G gases, 72, 73, 93 gastric, 38 geese, 54, 56 generation, 4, 41, 78 genes, 76 genetic, 23, 36, 88, 108 Geneva, 115 genotype, 92 genotypes, 75, 120 geochemical, 35, 80 germination, 47, 52 gestational diabetes, 40, 112 girls, 38 gland, 40 glass, 41 glucose, 40, 73 goals, 31, 115 gold, 79

Index grain, 90, 91, 92, 93, 120 grains, 88, 90, 91, 92, 93, 118 granules, 15, 102 graph, 8, 14 grass, x, 22, 61, 67, 114 gravity, 3 grazing, 116 ground water, 52 groups, 5, 6, 13, 15, 16, 35, 39, 43, 44, 66, 68, 81, 84, 85, 87, 89 growth, x, 7, 26, 35, 36, 64, 73, 78, 81, 83, 86, 90, 91, 93, 96, 105, 114, 118, 119, 120 growth rate, 35, 36, 78, 81, 86, 91 guilty, 41

H harmful, 3 harvest, 61 health, 17, 36, 37, 77, 78, 81, 83, 84, 88, 109, 110, 111, 114, 115 health effects, 37, 77 health problems, 78 heart, 39, 76, 112 Heart, 39 heart disease, 39, 76, 112 heat, 83 heating, 67 heavy metal, 3, 41, 82, 99, 100, 101, 102, 103, 104, 105, 107, 108, 110, 111, 116 heavy metals, 3, 41, 101, 102, 104, 105, 107, 110, 111, 116 heterogeneity, 11 heterotrophic, 73, 85, 114 homeostasis, 107 homogeneity, 81 homogeneous, 11 Hong Kong, 117 House, 111 housing, 110 human, ix, 4, 16, 17, 18, 23, 29, 32, 33, 34, 35, 36, 38, 42, 43, 59, 75, 76, 79, 80, 84, 85, 88, 90, 91, 108, 111, 113, 118 human exposure, 111 humans, 83

129

hydrolysis, 14 Hydrometallurgy, 99, 101, 102, 103, 114 hydroxide, 7 hydroxides, 89 hydroxyapatite, 67 hydroxyl, 6, 15, 68, 89 hydroxyl groups, 6, 15, 89 hypercholesterolemia, 39 hyperinsulinism, 40 hyperplasia, 113 hypersensitive, 112 hypertension, 39 hypertrophy, 40 hypothesis, 112

I id, 35, 44, 92 identification, 17, 21, 38, 41 imbalances, 41 immobilization, 4, 10, 52 immunological, 36, 83 implementation, 79 impurities, 2 inactive, 83 incineration, 105 Indian, 112 indicators, 18 indices, 107 indigenous, 103 industrial, vii, x, 1, 10, 21, 69, 78, 79, 82, 83, 85, 86, 95, 109, 114 industrial wastes, 83 industrialization, 4 industry, vii, 1, 3, 4, 43, 100, 110 infants, 39 infarction, 39, 112 infertility, 40 inflammatory, 112 inflammatory bowel disease, 112 influence, 17, 21, 35, 43, 45, 46, 67, 108, 114 ingestion, 17 inhalation, 17, 23 inhibition, 3 inhibitory, 14

130

Index

inhibitory effect, 14 injury, iv inorganic, vii, 5, 8, 38, 67, 73, 77, 78, 79, 80, 81, 86, 87, 90, 92, 93, 97, 121 inorganic growth, 86 inorganic salts, 78, 79, 81, 93 insulin, 39, 40 insulin resistance, 40 intelligence, 41 intensity, 52, 73, 79 interaction, 5, 9, 11, 13, 62 Interaction, 89, 101 interactions, vii, 9, 35, 43, 45, 47, 55, 59, 89, 108 interdisciplinary, 97 interference, 103 international, 80 international law, 80 interpretation, 35, 36, 42, 104 intestinal tract, 33 intestine, 81 invasive, 16, 32, 37, 59 invertebrates, 23 iodine, 75, 76, 118 Iodine, 78 ionic, 8, 15, 21, 95, 104, 106 ions, vii, x, 1, 2, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 18, 19, 26, 27, 31, 32, 47, 48, 61, 64, 66, 67, 68, 69, 71, 73, 79, 81, 82, 87, 89, 95, 96, 100, 102, 103, 104, 106, 114 iron, 75, 76, 80, 84, 90, 103, 111, 121 irrigation, 90 ischemic, 39, 112 ischemic heart disease, 39, 112 isotherms, 9, 10, 11, 12, 102, 107

K keratin, 35 kidneys, 3, 54 kinetic model, 102, 106, 114 kinetics, ix, 7, 21, 37, 65, 66, 67, 68, 73, 102, 107, 114 knowledge, 29, 48, 95 Kolmogorov, 113

Korean, 113

L LA, 85 lagoon, 107 lakes, 74, 87 land, 78 landfills, 65 Langmuir, 8, 9, 10, 11, 12, 13, 14, 26, 66, 67, 68, 87, 88, 103 language, 3 lanthanum, 99, 101 larvae, 22, 108 law, 4, 32, 69, 80, 96 lead, 91, 101, 103, 104, 106, 107, 108, 109, 110 learning, 41 lifestyle, 37, 45 ligands, 8, 15, 89 linear, 43, 73, 74, 93 lipids, 6, 86 liquid chromatography, 103 literature, 7, 9, 10, 13, 21, 33, 34, 35, 36, 38, 42, 75, 80 liver, 54, 55, 59, 110 livestock, vii, x, 54, 58, 71, 75, 77, 78, 79, 80, 83, 84, 85, 86, 87, 96, 97, 114 Livestock, 77, 117 living environment, 38, 84 location, 35 London, 99, 102, 115 long period, 62 long-term, 18, 120 low temperatures, 86 lungs, 40, 54, 55 lysine, 81

M machinery, 4 macroalgae, x, 21, 61, 84, 86, 87, 102, 114 macromolecules, 80 macronutrients, 52, 91, 110

Index Madison, 119 magnesium, 65, 86, 111, 118, 120 magnetic, iv males, 44, 45 malnutrition, 39, 75, 90, 112, 115 mammals, 54 management, 46 manganese, 41, 80, 118, 121 Manganese, 78 manure, 77, 78 market, 79, 80, 81 mass, 26, 29, 47, 56, 61, 108 mathematical, x, 66, 112 matrix, 10, 29, 62 maximum sorption, 26, 27 measures, 90 meat, 57, 75, 76, 88, 97, 118 mechanical, iv, 62 media, 83, 86, 118 medicine, 4, 35 melanin, 35 melter, 55, 69, 114 membranes, 89 mental retardation, 41 mercury, 49, 59, 105, 106, 108, 109, 113, 114 metabolic, ix, 7, 16, 17, 40, 59, 65, 73, 96 metabolism, 26, 36, 42, 73, 85, 115, 117 metal ions, vii, x, 1, 2, 4, 5, 6, 7, 8, 9, 10, 13, 14, 16, 18, 19, 26, 27, 31, 32, 47, 48, 61, 64, 66, 68, 69, 73, 79, 81, 82, 87, 95, 96, 100, 104 metal recovery, 71 Metallothionein, 104 metallothioneins, 16, 84 metallurgy, 4 metals, vii, ix, x, 1, 2, 3, 4, 5, 6, 7, 9, 10, 15, 16, 18, 21, 23, 32, 34, 35, 36, 37, 38, 39, 41, 43, 44, 45, 46, 48, 49, 50, 52, 54, 55, 56, 57, 59, 61, 68, 69, 71, 77, 79, 80, 90, 95, 96, 99, 101, 102, 104, 105, 107, 108, 110, 111, 116, 120 methionine, 81, 83 Mexico, 119 microalgae, x, 21, 22, 61, 69, 72, 73, 83, 84, 85, 86, 114, 115, 118

131

microbes, 76 microbial, 6, 7, 100, 116 Microbial, 102, 114, 117 micronutrients, vii, x, 46, 49, 50, 52, 53, 75, 76, 77, 78, 80, 88, 89, 90, 91, 92, 93, 96, 110, 113 microorganisms, 18, 82 microwave, 29 middle-aged, 43 milk, 32, 54, 55, 56, 57, 58, 59, 75, 95, 97, 109, 117 mineralization, 84 minerals, 38, 55, 76, 77, 78, 79, 83, 85, 111, 114, 116, 120 mining, 1, 4, 102 mixing, 77 mobility, 121 mode, 73 modeling, x, 7, 9, 11, 13, 14, 66, 102, 103 models, 7, 8, 10, 46, 103 moisture, 17 molasses, 105 molecular weight, 3 molecules, 89 mollusks, 22, 80 monitoring, 2, 4, 16, 18, 22, 23, 34, 99, 105, 108 Moon, 107 Morocco, 111 morphological, 17, 56 morphology, ix MS, 29, 47, 55, 113 multi-component systems, 10, 11 multiple regression, 43, 45 multiple regression analysis, 43, 45 multiplicity, vii, 9, 35 muscle, 22, 108, 110 muscle tissue, 22, 108 muscles, 54, 55, 56, 59 myocardial infarction, 39, 112

N nasopharyngeal carcinoma, 40, 111 national, 5

132

Index

National Academy of Sciences, 119 natural, vii, ix, 1, 37, 45, 69, 74, 77, 78, 79, 82, 84, 87, 106, 114 natural environment, 74 Nb, 51, 53 nebulizer, 47 nephritic syndrome, 40 nervous system, 3 Netherlands, 110 neural networks, 12 neurotoxicity, 41 New York, iii, iv, 99, 100, 111, 115 Ni, 3, 5, 15, 21, 33, 34, 39, 40, 41, 43, 44, 45, 46, 48, 49, 51, 53, 54, 55, 57, 58, 77, 104, 107 niacin, 79 nickel, 99, 101, 107, 112 nitrate, 47 nitric acid, 68 nitrogen, 49, 69, 96 non invasive, 16 non-invasive, 37 nonlinear, 10 non-linear, 74 non-smokers, 44 normal, 36, 42, 112 nutrient, 116, 119, 120 nutrients, x, 2, 7, 16, 18, 52, 65, 69, 74, 77, 83, 91, 93, 96, 111 nutrition, 41, 80, 113, 115, 116, 117, 118, 120, 121 nutritional supplements, 79

O obesity, 76 occupational, 41, 105 Ohio, 118 oil, 58, 75, 120 older people, 44 oligosaccharides, 83 optical, 17, 47 oral, 17 ores, 4 organelles, 3

organic, 2, 6, 8, 15, 49, 65, 67, 69, 73, 79, 80, 81, 83, 85, 86, 87, 90, 92, 105, 108, 121 organic compounds, 2, 6, 15, 73, 81 organic matter, 49, 65, 67, 92 organism, vii, ix, x, 4, 16, 17, 18, 32, 34, 35, 36, 37, 38, 40, 41, 42, 44, 59, 74, 77, 82, 89, 93, 95 organization, 18 oxidation, 4 oxidative, 40, 41 oxidative stress, 40, 41 oxygen, 13 oysters, 22, 86, 107, 118

P Pacific, 86, 115, 118 pain, 32 Pakistani, 112 PAN, 116 Paper, 115, 119 parameter, 7, 15, 26, 49, 67, 74 parenteral, 41 Parkinson, 41, 111 particles, 119 passive, 7, 18, 46, 89 pasture, 116 pathogenesis, 39 pathology, 40 pathways, 16 patients, 37, 39, 40, 41, 111, 112, 113 Pb, 3, 4, 5, 14, 15, 21, 34, 36, 37, 38, 39, 41, 42, 43, 44, 45, 46, 48, 49, 50, 51, 52, 53, 54, 55, 56, 57, 58, 71, 72, 96, 106, 107 PCR, 104 peat, 14, 83, 104 perception, 120 performance, 9, 67, 68, 69, 74, 87, 106, 117, 118 personal, 35, 45, 46 Perth, 119 pesticides, 101 pH, 6, 7, 8, 9, 12, 14, 21, 48, 52, 65, 66, 67, 68, 93, 99, 101, 104, 106 pharmaceutical, 37, 79

Index pharmaceuticals, 85 phloem, 93 phosphate, 6, 119, 120 phosphates, 58, 67 phosphorus, 65, 69, 91, 96, 120, 121 photobioreactors, 85 photosynthesis, 84 photosynthetic, 69, 74, 87 physical activity, 115 physical factors, 74 physicochemical, 8, 9, 15 physiological, 36, 54, 74, 117 physiology, ix, 79 pigments, 85, 86 pigs, 118 plants, x, 2, 16, 22, 23, 32, 46, 47, 48, 49, 61, 75, 76, 77, 78, 81, 84, 86, 87, 88, 89, 90, 91, 92, 93, 96, 105, 110, 111, 114, 119, 121 plasma, 29, 47, 108, 112 platinum, 108 play, 3, 39, 83 plumbism, 38 poisoning, 38 Poland, 33, 34, 42, 52 pollutant, 4, 16, 18, 27, 32, 96 pollutants, vii, ix, 2, 26, 57, 65, 69, 73, 78, 95, 97, 105 pollution, vii, ix, x, 2, 16, 17, 18, 23, 32, 34, 35, 37, 41, 49, 52, 54, 56, 59, 90, 93, 95, 99, 108, 109, 113 polysaccharide, 21, 80, 81, 107 polysaccharides, 6, 86 polyunsaturated fat, 78 polyunsaturated fatty acid, 78 polyunsaturated fatty acids, 78 pond, 86 pools, 75 poor, 36, 76, 77, 81, 92 population, 33, 35, 42, 43, 46, 112 Portugal, 42, 111 positive correlation, 92 potassium, 48, 52, 119 poultry, 54, 57, 58 poverty, 115 poverty reduction, 115

133

power, 41, 113 power plant, 41, 113 precipitation, 7, 64, 102 pregnant, 112 pregnant women, 112 premenstrual syndrome, 40 preparation, iv, x, 29, 37, 57, 58, 76, 87, 88, 95, 109, 110 prevention, ix, 4, 16, 83, 95, 115 preventive, 57, 110 printing, 4 prisoners, 41 probability, 77 procedures, x, 17, 18, 32, 35, 36, 37, 46 producers, 84, 86 production, x, 27, 32, 52, 71, 72, 75, 76, 78, 82, 83, 85, 86, 87, 88, 93, 96, 97, 109, 111, 113, 114, 121 productivity, 65, 74, 85 profession, 39 property, iv, ix, 1, 32, 69 protection, 4, 14, 31, 32, 72 protein, 67, 78, 81, 85, 91, 120 proteins, 6, 16, 81, 83, 86, 89, 116, 118 protons, 6, 9, 101 pseudo, 7, 66 Pseudomonas, 21, 101, 106 pyrite, 41

R race, 35 radius, 15 range, 42, 43, 54, 55, 56, 67, 86, 110 rat, 108 rats, 22, 23, 108 raw material, 85, 110 raw materials, 85 RC, 118 reaction order, 7 recall, 36 reclamation, 79 Reclamation, 105 recovery, 71, 101, 104 redox, 46

134

Index

reduction, 59, 76, 95, 109, 115 regenerate, 64 regeneration, 62, 71 regression, 10, 43, 45 regression analysis, 43, 45 regulation, 89 regulations, 5, 79 relationship, 23, 45, 112 relationships, 10, 76, 108, 115 remediation, 16, 95, 105 reparation, 58 reproduction, 3 research, vii, 9, 14, 21, 22, 23, 90 reservoirs, 87 resins, 83 resistance, 40, 62, 119 resolution, 100 respiratory, 3, 16, 33 restoration, 4, 68 retardation, 41 retention, 52, 116, 121 rheumatic, 40 rheumatic diseases, 40 rice, 76, 90 Rio de Janeiro, 33, 34 risk, 2, 41, 46, 86, 91, 106, 110, 112, 116 risk assessment, 46, 106 risk factors, 112 risks, 81 river systems, 106 ruminant, 116 rural, 41, 109

S SA, 119 Saccharomyces cerevisiae, 15, 82, 84, 104 salt, 83 salts, 23, 38, 48, 75, 77, 78, 79, 80, 81, 88, 93 sample, 16, 32, 37 sampling, 7, 37 scalp, 112, 113 Scanning Electron Microscopy (SEM), 15 scientific, 33, 34, 42 search, 78, 79, 115

seaweed, 6, 101 sebum, 37 sediments, 1, 2 seed, 91, 119, 120 segregation, 81 selectivity, 9, 10, 11, 13, 14, 15, 89 selenium, 4, 58, 59, 83, 86, 91, 109, 117 self, 74, 115 self-control, 74, 115 separation, 62, 87 series, 118 services, iv severity, 41 sewage, 107 sex, 34, 35, 36, 38, 39, 41, 44, 45, 46, 109 shape, 10 sharing, 7 side effects, 81 silicon, 111 simulation, 46, 102, 103 simulations, 103 sites, 6, 7, 8, 9, 11, 12, 13, 14, 18, 54, 62, 67, 87, 100, 101 skin, 16, 33, 54 sludge, 2, 99, 102, 103, 107 smelting, 4 smokers, 44 smoking, 35, 109 sodium, 47, 48, 86, 91, 117 soil, 4, 16, 32, 46, 47, 48, 49, 51, 52, 53, 55, 65, 75, 76, 81, 89, 90, 91, 92, 93, 96, 105, 107, 108, 110, 111, 113, 119, 120 soil particles, 119 soil pollution, 32 soils, 23, 46, 77, 89, 91, 92, 93, 95, 110, 113, 119, 120, 121 solid state, 2, 4 solid-state, 71 solubility, 7, 23, 48, 52, 67, 81, 108 solutions, x, 1, 8, 15, 29, 32, 69, 82, 86, 87, 96, 101, 104, 106, 107 sorbents, 6, 21, 26, 27, 61, 67, 79, 96 sorption, 6, 7, 8, 9, 10, 15, 26, 27, 61, 62, 65, 66, 67, 68, 73, 96, 104, 113, 114 South Africa, 99

Index soybeans, 120 spatial, 92 specialists, 97 speciation, 7, 46, 67, 111 species, 9, 17, 18, 46, 49, 50, 51, 52, 74, 80, 84, 85, 89, 91, 92, 105, 107 specific gravity, 3 spectroscopy, 47 stability, 81 stages, 1, 19 standardization, 34 standards, 5, 55, 116 Standards, 5 starches, 81 sterile, 85 sterilization, 66 stomach, 81 storage, 37 strains, 85 strength, 8, 21, 81, 100, 106 Streptomyces, 82 stress, 40, 41 substances, 16, 37, 67, 80, 105 substrates, 73 suffering, 37, 39, 40, 41 sulfate, 6, 93, 120, 121 sulfur, 49 sulphate, 67, 119 Sun, 15, 102 sunlight, 73, 85 superoxide, 39, 41 superoxide dismutase, 39, 41 supplemental, 117 supplements, vii, 27, 57, 59, 75, 76, 77, 78, 79, 80, 81, 82, 86, 87, 97, 114, 118 supply, 76, 79, 89, 119 surface area, 68 surface layer, 89 surface properties, 7, 8, 79 susceptibility, 89 sustainable development, 97 sweat, 33, 37 Sweden, 33, 34, 42, 113 symbiotic, 76 symptoms, 36, 37, 38, 39, 40

135

syndrome, 40 synergistic, 9, 43, 45, 48, 95 synergistic effect, 45 synthesis, 74 synthetic, 92, 106, 118 systematic, 114 systems, 9, 10, 11, 13, 14, 15, 21, 77, 78, 86, 102, 103, 104, 106

T Taiwan, 105 technological, 121 technology, 1, 97, 110, 114 temperature, 7, 8, 17, 21, 65, 67, 74, 86, 106 TF, 47, 48, 49 theory, 2, 56 therapeutic, 86 therapy, 113 thermolysis, 108 Ti, 34, 43, 44, 45, 51, 53, 55, 57, 58 TI, 45 time, 2, 7, 36, 37, 45, 62, 64, 74, 90, 91 tissue, 22, 36, 37, 40, 107, 108 titration, 12, 21, 66, 68, 100, 102 tobacco, 44 tolerance, 37, 119 toxic, vii, ix, 1, 2, 3, 4, 5, 7, 15, 16, 18, 21, 23, 25, 26, 31, 32, 36, 37, 39, 41, 42, 44, 45, 46, 49, 50, 52, 54, 55, 56, 57, 58, 59, 68, 69, 71, 77, 78, 79, 80, 81, 83, 90, 93, 95, 96, 110 toxic effect, 7, 16, 25, 26, 32, 77, 78, 79, 90, 96 toxic metals, ix, 1, 2, 3, 4, 5, 7, 15, 16, 18, 21, 23, 32, 36, 39, 41, 44, 46, 49, 50, 52, 54, 55, 56, 57, 59, 68, 69, 71, 77, 90, 95, 96 toxic side effect, 81 toxic substances, 16 toxicity, 3, 4, 23, 85, 97, 117 toxicology, 99, 105 toxin, 37 trace elements, 33, 35, 36, 38, 39, 42, 49, 50, 54, 55, 57, 109, 111, 112, 113, 116 trade, 119

136

Index

transfer, 10, 16, 32, 33, 46, 47, 48, 57, 87, 105 transformation, 92 transgenic, 76, 90 transgenic plants, 76 transition, 115 translocation, 93, 121 Transmission Electron Microscopy (TEM), 15 transport, 16, 55, 89, 93, 96 trees, 49, 50 tryptophan, 79 two-dimensional, 14 type II diabetes, 40

U UK, 119 UNICEF, 115 uniform, 7, 9, 11, 77 United Kingdom, 113 uranium, 102, 105, 108 urban, 33, 43, 45, 111 urbanized, 95 urine, 33, 36, 40, 44, 77, 116

V values, 14, 17, 25, 33, 34, 35, 36, 38, 39, 42, 56, 64, 67, 76, 111 variability, 23, 55, 92, 108 variable, 80, 81, 119 variation, 120 vegetables, 88, 93 vegetation, 93 vertebrates, 23 vessels, 29 vitamin A, 76 vitamin C, 38 vitamins, 78, 83, 85

waste, 6, 15, 21, 61, 65, 67, 71, 96, 97, 102, 103, 104, 105, 106 waste incineration, 105 wastes, 23, 83, 108, 117 wastewater, x, 2, 5, 14, 16, 23, 62, 64, 67, 69, 71, 72, 73, 78, 79, 80, 82, 87, 95, 96, 97, 100, 101, 105, 111, 115 wastewater treatment, x, 2, 14, 16, 23, 64, 67, 69, 71, 78, 79, 80, 82, 87, 95, 96, 97, 100, 115 wastewaters, vii, 71, 87, 101, 105 water, 4, 5, 15, 16, 33, 35, 38, 42, 43, 46, 55, 56, 74, 78, 79, 87, 90, 105 waterfowl, 56, 57, 109 welding, 4 wetlands, 108 wheat, 67, 89, 114, 118, 119, 120, 121 wine, 38 Wisconsin, 119 women, 39, 40, 112 wood, x, 49, 50, 52, 53, 95, 110, 111, 113 wood species, 50 work, vii, ix, 61, 62 workers, 41, 105 workplace, 37 World Bank, 119 World Health Organisation (WHO), 115 worm, 22, 107

X XPS, 15 xylem, 93

Y yeast, 83, 97, 116, 117 yield, 36, 74, 88, 90, 91, 92, 93, 96, 120 yolk, 56, 78

W Z Warsaw, 110 washing procedures, 35 Washington, 115, 119

zeolites, 69, 114

Index zinc, 75, 76, 80, 101, 102, 106, 107, 108, 111, 112, 118, 119, 120, 121 Zinc, 78, 120 zinc sulfate, 120, 121

137

Zn, 3, 5, 14, 15, 21, 33, 34, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 48, 49, 50, 51, 53, 55, 56, 57, 58, 65, 77, 78, 80, 81, 87, 88, 89, 90, 91, 92, 93, 96, 103, 104, 107, 108, 112, 120