VIEWPOINT ▼
Defining BIOAVAILABILITY and Bioaccessibility of Contaminated Soil and Sediment is Complicated K I R K . T. S E M P L E KIERON J. DOICK KEVIN C. JONES LANCASTER UNIVERSITY (U.K.) PETER BURAUEL FORSCHUNGSZENTRUM JÜLICH (GERMANY ) A N D R E W C R AV E N PE S T I C I D E S S A F E T Y D I R E C T O R AT E ( U . K . ) HAUKE HARMS UFZ CENTRE FOR ENVIRONMENTAL RESEARCH (GERMANY )
L
aura Ehlers
Different interpretations create
and Richard Luthy
more than a semantic
recently published an impor-
stumbling block.
tant A-page feature in ES&T in which they persuasively make the case that improving
risk assessment and remediation rests on better understanding of bioavailability (1). Their article provided a concise summary of a major U.S.
National Research Council (NRC) report called Bioavailability of Contaminants in Soils and Sediments: Processes, Tools and Applications (2). Despite consensus by scientists that bioavailability is indeed critical to the risk assessment process, Ehlers and Luthy note that “the NRC report contains no explicit definition of bioavailability.” Rather, the report defines “bioavailability processes as the individual physical, chemical, and biological interactions that determine the expo-
PHOTODISC/RHONDA SAUNDERS
sure of organisms to chemicals associated with soils and sediments.” Researchers have struggled for decades with concepts and definitions of bioavailability, but it seems remarkable that such an important report lacks a working definition of the term. Given the legal and regulatory implications of the bioavailability concept as part of the risk assessment framework, the term must be clearly understood. For example, the United Kingdom’s Contaminated Land Regulations under Part IIA of the Environmental Protection Act of 1990 defines contaminated land as “land that appears to the local authority to be in such a condition, by reason of substances in, on, or under the land, that significant harm is being caused, or there is significant possibility that harm is being caused” (3). Thus, just the presence of substances of concern is not sufficient; harmful interaction with a receptor must be a possibility. Because toxic effects require that an organism takes up the contaminant, the extent to which substances are bound to soil particles or are available to cause harm needs to be considered. We therefore offer this Viewpoint to stimulate further discussion about bioavailability and—perhaps— offer a clearer working definition of the term.
Ruling out related usages With several different definitions in related disciplines, environmental scientists discussing the term bioavail© 2004 American Chemical Society
ability are bound to experience confusion. In pharmacology and toxicology, the term relates to the systemic availability of a xenobiotic after intravenous or oral dosing (4). Environmental scientists have tried to adapt this usage when considering human exposure to soil-borne contaminants. For example, Ruby et al. (5) and Kramer and Ryan (6) suggested that the bioavailable portion is the amount of compound that is removed from soil through desorption processes under physiological conditions, which is transferred to the circulatory system. Kramer and Ryan used the term bioaccessibility to define the total amount of contaminant that is desorbed from the soil, which is available for uptake into the circulatory system (6). Although these concepts are useful, making direct parallels from the pharmacological usage to contaminants in soil and sediment biota can be problematic. For example, microorganisms do not have a digestive tract, target organs, or a circulatory system. Toxicologists also refer to the importance of the peak plasma concentration (Cmax) and the time to peak plasma concentration (tmax) as important parameters in characterizing availability in the body. These concepts may also not be appropriate because contaminants in soil or aquatic environments are often continuously supplied to organisms and controlled by, for example, the rate of desorption from solid phases rather than an acute dose. In addition, when a conJUNE 15, 2004 / ENVIRONMENTAL SCIENCE & TECHNOLOGY ■ 229A
taminant is present in a target organ, not only was absorption or uptake efficiency involved but also physiological or metabolic factors. For example, a child eats contaminated soil. After a persistent and bioaccumulatory organic chemical transfers from the soil into the child’s bloodstream, it may partition into body fat and be stored there for decades, rather than reach organs like the liver or brain. Therefore, we would argue that the pharmacological approach to defining bioavailability of soiland sediment-borne contaminants is inappropriate. Inconsistency and imprecision are also apparent when the term bioavailability is applied to contaminants in soil and aquatic systems. The following definitions are compiled in a Technical Report published by the European Centre for Ecotoxicology and Toxicology of Chemicals (7): (i) “The ability of a substance to interact with the biosystem of an organism” (8); (ii) “the portion of the total quantity or concentration of a chemical in the environment or a portion of it that is potentially available for biological action” (9); (iii) “the amount/percentage of a compound that is actually taken up by an organism as the outcome of a dynamic equilibrium of organism-bound uptake processes, and soil particle-related exchange processes, all in relation to a dynamic set of environmental conditions” (10). More recently, the NRC report also noted numerous definitions: [B]ioavailability may represent the fraction of a chemical accessible to an organism for absorption, the rate at which a substance is absorbed into a living sys-
FIGURE 1
Bioavailable and bioaccessible in soil This conceptual diagram illustrates the bioavailable and bioaccessible fractions of a contaminant in soil as defined by physical location. It also describes the relationship of soil-associated contaminant molecules in relation to bioaccessible fraction. Sorbed compound (rapidly reversible) (Bioavailable or bioaccessible: Temporally constrained) Plant root
Sorbed compound (slowly/very slowly reversible) (Bioaccessible: Temporally constrained)
Microbes
Bioavailable compound
Occluded compound (Non-bioaccessible)
Bioaccessible compound (Physically constrained) Earthworm
230A ■ ENVIRONMENTAL SCIENCE & TECHNOLOGY / JUNE 15, 2004
tem, or a measure of the potential to cause a toxic effect. Often, environmental scientists consider bioavailability to represent the accessibility of a soil-bound chemical for assimilation and possible toxicity (11), while toxicologists consider bioavailability as the fraction of chemical absorbed and able to reach systemic circulation in an organism. Another view of bioavailability is represented by a chemical crossing a cell membrane, entering a cell, and becoming available at a site of biological activity. Others might think of bioavailability more specifically in terms of contaminant binding to or release from a solid phase. The different viewpoints of bioavailability create a semantic stumbling block that can confound the use of the term across multiple disciplines— hence the reason that “bioavailability processes” is used in this report (2).
Proposed definitions Obviously, having so many definitions creates confusion for environmental scientists, and this ambiguity is undesirable given current regulatory contexts. Therefore, we would like to offer the following definitions, mindful of the literal usages of the words available and accessible. Bioavailable. The Oxford Dictionary of English defines available as “capable of being employed; at one’s disposal; at hand” (12). This term has an implied immediacy; what is available is available now. Hence, we define the bioavailable compound as that which is freely available to cross an organism’s cellular membrane from the medium the organism inhabits at a given time (Figure 1). Once transfer across the membrane has occurred, storage, transformation, assimilation, or degradation can take place within the organism; however, these processes are obviously distinct from the transfer between the medium (e.g., soil) and the organism. Bioaccessible. The same dictionary defines accessible as “capable of being approached or reached; approachable, attainable” (12). The definition implies that some of what is accessible can be reached but is often not quite within reach from a given place or at a given time. In our context, a constraint is implied in time and/or space, preventing the organism from gaining access to the chemical now. Hence, we define the bioaccessible compound as that which is available to cross an organism’s cellular membrane from the environment, if the organism has access to the chemical. However, the chemical may be either physically removed from the organism or only bioavailable after a period of time. In this context, physically removed may refer to a chemical that is occluded in soil organic matter and hence is not available at a given time or that occupies a different spatial range of the environment than the organism (Figure 1). Contaminants can become available within the order of seconds from these locations (and hence are bioavailable), following release from labile or reversible pools; or, the organism can move into contact with the contami-
nant. Alternatively, release may occur over much longer timescales (e.g., years or decades) and render the chemical bioaccessible. To sum up, bioaccessibility encompasses what is actually bioavailable now plus what is potentially bioavailable. We can link these definitions to the bioavailability processes described in the NRC report (2). Figure 2 describes the bioavailability processes (A–D). A represents the release of a bound or recalcitrant chemical to a more accessible form, B and C describe the transport of chemicals to a cellular membrane, and D represents the uptake of a chemical across a cellular membrane. Our definition of bioavailability addresses process D, whereas bioaccessibility encompasses processes A–D.
Advantages and implications It is well known that the portion of a chemical that is either bioavailable or bioaccessible in a given soil or sediment environment can differ substantially between organisms. One clear advantage of our definitions is their multi-functionality, as these definitions can apply to contaminants being available or accessible to microorganisms, fungi, plants, invertebrates, and higher animals, by simply addressing supply across the membrane of the organism in question. This would be the cellular membrane of a bacterium; in earthworms, for example, it encompasses uptake via the skin and the gastrointestinal tract together. Rather than addressing adverse effects, the definitions we offer account for the supply, or potential supply, of contaminants to organisms (usually microorganisms or plants) for uptake, transformation, or degradation. Distinguishing between bioavailability and bioaccessibility forces practitioners to consider what they actually measure with biological and chemical assays, which are purportedly developed to determine the ambiguously defined bioavailable fraction. According to our offered terminology, routine chemical techniques described in the literature, for example, actually estimate the bioaccessible rather than the bioavailable fraction. In truth, remediation scientists are probably more interested in what is bioaccessible over time at a given site than what is bioavailable. Moreover, our proposed definitions raise a fundamental methodological question: Can the bioavailable portion of substance x to species y actually be measured, and if so, how?
Acknowledgments The authors would like to thank Richard Burns, Jose Julio Ortega Calvo, Bill Davison, Alwyn Hart, Ken Killham, Graeme Paton, Simon Pollard, Brian Reid, and Ian Thompson for their constructive comments in drafting this paper.
Kirk T. Semple is a senior lecturer of environmental microbiology and ecotoxicology, Kieron J. Doick is a doctoral student investigating the bioavailability of organic contaminants in soil, and Kevin C. Jones is a professor of environmental chemistry at Lancaster University in the United Kingdom. Peter Burauel is the Deputy Director of the Agrosphere Unit at the Forschungszentrum Jülich in Germany, and Andrew Craven is a principal scientist
FIGURE 2
Differing definitions FIGURE 2
In both soil and sediment, processes that determine exposure to contamination includeprocesses release of a solid-bound contaminant (A) and Bioavailability subsequent transport (B), transport of bound contaminants (C), uptake In both soil and sediment, processes that determine exposure to conacross a physiological membrane (D), and incorporation into a living tamination include release of a solid-bound contaminant (A) and subsesystem (E). Note that A, B, and C can occur internal to an organism, quent transport (B), transport of bound contaminants (C), uptake across such as in the lumen of the gut. The NRC report defines A, B, C, and D a physiological membrane (D), and incorporation into a living system to be bioavailability processes, but not E, because soil and sediment (E). Note that A, B, and C can occur internal to an organism, such as in no longer play a role. In contrast, we define A, B, C, and D as processthe lumen of the gut. The NRC report defines A, B, C, and D to be bioes governing bioaccessibility, whereas D relates to bioavailability. availability processes, but not E, because soil and sediment no longer play a role. Biological membrane Bound contaminant Association
A
C
Dissociation
Released contaminant
D
Absorbed contaminant in organism
E
Site of biological response
B
Source: Ref. 1.
at the Pesticides Safety Directorate in the United Kingdom. Hauke Harms is a professor of environmental microbiology at the UFZ Centre for Environmental Research in Germany. Address correspondence to Semple at
[email protected].
References (1) Ehlers, L. J.; Luthy, R. G. Contaminant bioavailability in soil and sediment. Environ. Sci. Technol. 2003, 37, 295A– 302A. (2) National Research Council. Bioavailability of Contaminants in Soils and Sediments: Processes, Tools and Applications. National Academies Press: Washington, DC, 2002. (3) DETR Circular 2/2000. Contaminated Land: Implementation of Part IIA of the Environmental Protection Act 1990; DETR: London, 2000; ISBN: 0 11 753544 3. (4) Klaassen, C.D. Chapter 3. In Casarett and Doull’s Toxicology, 3rd Edition. Klaassen, C. D., Amdur, M. O., Doull, J., Eds.; Macmillian Publishing Co.: New York, 1986; pp 33–63. (5) Ruby, M. V.; et al. Estimation of lead and arsenic bioavailability using a physiologically based extraction test. Environ. Sci. Technol. 1996, 30, 422–430. (6) Kramer, B. K.; Ryan, P. B. Soxhlet and microwave extraction in determining the bioaccessibility of pesticides from soil and model solids. Proceedings of the 2000 Conference on Hazardous Waste Research, pp 196–210. (7) European Centre for Ecotoxicology and Toxicology of Chemicals (ECETOC). Scientific Principles of Soil Hazard Assessment of Substances; Technical Report No. 84; 2002; pp 24–26; ISSN-0773-6347-84. (8) Van Leeuwen, C. J.; Hermens, J. L. M. Terrestrial toxicity. In Risk Assessment of Chemicals, An Introduction; Kluwer Academic: Dordrecht, The Netherlands, 1995; pp 211–216. (9) Spacie, A.; Hamelink, J. L. Bioaccumulation. In Fundamentals of Aquatic Toxicology, Effects, Environmental Fate and Risk Assessment, 2nd ed.; Rand, G. M., Ed.; Taylor & Francis: Washington, DC, 1995. (10) Herrchen, M.; Debus, R.; Pramanik-Strehlow, R. Bioavailability as a key property in terrestrial ecotoxicity assessment and evaluation; Fraunhofer IRB Verlag: Stuttgart, Germany, 1997. (11) Alexander, M. Aging, bioavailability, and overestimation of risk from environmental pollutants. Environ. Sci. Technol. 1982, 34, 4259–4265. (12) The Oxford Dictionary of English, 2nd Ed. Oxford University Press: Oxford, U.K., 2003. JUNE 15, 2004 / ENVIRONMENTAL SCIENCE & TECHNOLOGY ■ 231A
