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 )
 aura Ehlers Different interpretations create

L and Richard Luthy

recently published an impor-
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
more than a semantic

bioavailability (1). Their article provided a concise summary of a major U.S.

National Research Council (NRC) report called Bioavailability of Contaminants
stumbling block.

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 indi-
vidual physical, chemical, and biological interactions that determine the expo-
sure of organisms to chemicals associated with soils and sediments.”
Researchers have struggled for decades with con- ability are bound to experience confusion.
cepts and definitions of bioavailability, but it seems In pharmacology and toxicology, the term relates to
remarkable that such an important report lacks a the systemic availability of a xenobiotic after intra-
working definition of the term. Given the legal and venous or oral dosing (4). Environmental scientists
regulatory implications of the bioavailability concept have tried to adapt this usage when considering human
as part of the risk assessment framework, the term exposure to soil-borne contaminants. For example,
must be clearly understood. Ruby et al. (5) and Kramer and Ryan (6) suggested that
For example, the United Kingdom’s Contaminated the bioavailable portion is the amount of compound
Land Regulations under Part IIA of the Environmental that is removed from soil through desorption process-
Protection Act of 1990 defines contaminated land as es under physiological conditions, which is transferred
“land that appears to the local authority to be in such to the circulatory system. Kramer and Ryan used the
a condition, by reason of substances in, on, or under term bioaccessibility to define the total amount of con-
the land, that significant harm is being caused, or taminant that is desorbed from the soil, which is avail-
there is significant possibility that harm is being able for uptake into the circulatory system (6). Although
caused” (3). Thus, just the presence of substances of these concepts are useful, making direct parallels from
concern is not sufficient; harmful interaction with a the pharmacological usage to contaminants in soil and
receptor must be a possibility. Because toxic effects sediment biota can be problematic. For example, mi-
require that an organism takes up the contaminant, croorganisms do not have a digestive tract, target or-
the extent to which substances are bound to soil par- gans, or a circulatory system.
ticles or are available to cause harm needs to be Toxicologists also refer to the importance of the
considered. peak plasma concentration (Cmax) and the time to
PHOTODISC/RHONDA SAUNDERS

We therefore offer this Viewpoint to stimulate fur-
ther 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-
peak plasma concentration (tmax) as important para-
meters in characterizing availability in the body. These
concepts may also not be appropriate because con-
taminants in soil or aquatic environments are often
continuously supplied to organisms and controlled by,
for example, the rate of desorption from solid phas-
es rather than an acute dose. In addition, when a con-

© 2004 American Chemical Society JUNE 15, 2004 / ENVIRONMENTAL SCIENCE & TECHNOLOGY ■ 229A
 taminant is present in a target organ, not only was ab-
sorption or uptake efficiency involved but also phys-
iological 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 pharma-
cological approach to defining bioavailability of soil-
and sediment-borne contaminants is inappropriate.
Inconsistency and imprecision are also apparent
when the term bioavailability is applied to contami-
nants in soil and aquatic systems. The following de-
finitions are compiled in a Technical Report published
by the European Centre for Ecotoxicology and Tox-
icology 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 ac-
tually taken up by an organism as the outcome of a
dynamic equilibrium of organism-bound uptake
processes, and soil particle-related exchange process-
es, 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 frac-
tion of a chemical accessible to an or-
ganism 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 mole-
cules in relation to bioaccessible fraction.
Sorbed compound
(rapidly reversible)
(Bioavailable or bioaccessible: Sorbed compound
Temporally constrained) (slowly/very slowly reversible)
Plant root (Bioaccessible:
Temporally constrained)
Microbes
Bioavailable
compound
Bioaccessible
compound
(Physically constrained)
Occluded compound
(Non-bioaccessible) Earthworm
230A ■ ENVIRONMENTAL SCIENCE & TECHNOLOGY / JUNE 15, 2004
tem, or a measure of the potential to
cause a toxic effect. Often, environmen-
tal 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 cir-
culation in an organism. Another view of
bioavailability is represented by a chem-
ical 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 stum-
bling 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 con-
fusion for environmental scientists, and this ambi-
guity is undesirable given current regulatory contexts.
Therefore, we would like to offer the following defin-
itions, mindful of the literal usages of the words avail-
able and accessible.
Bioavailable. The Oxford Dictionary of English de-
fines available as “capable of being employed; at one’s
disposal; at hand” (12). This term has an implied im-
mediacy; what is available is available now. Hence, we
define the bioavailable compound as that which is
freely available to cross an organism’s cellular mem-
brane from the medium the organism inhabits at a
given time (Figure 1). Once transfer across the mem-
brane has occurred, storage, transformation, assim-
ilation, or degradation can take place within the
organism; however, these processes are obviously dis-
tinct from the transfer between the medium (e.g., soil)
and the organism.
Bioaccessible. The same dictionary defines acces-
sible as “capable of being approached or reached; ap-
proachable, 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 en-
vironment, if the organism has access to the chemi-
cal. 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 envi-
ronment than the organism (Figure 1). Contaminants
can become available within the order of seconds
from these locations (and hence are bioavailable), fol-
lowing 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, bioaccessi-
bility encompasses what is actually bioavailable now
plus what is potentially bioavailable.
We can link these definitions to the bioavailabili-
ty processes described in the NRC report (2). Figure
2 describes the bioavailability processes (A–D). A rep-
resents the release of a bound or recalcitrant chemi-
cal 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 cellu-
lar membrane. Our definition of bioavailability
addresses process D, whereas bioaccessibility encom-
passes 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 be-
tween organisms. One clear advantage of our defin-
itions is their multi-functionality, as these definitions
can apply to contaminants being available or acces-
sible 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 defini-
tions we offer account for the supply, or potential
supply, of contaminants to organisms (usually mi-
croorganisms or plants) for uptake, transformation,
or degradation.
Distinguishing between bioavailability and bioac-
cessibility 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 tech-
niques described in the literature, for example, actu-
ally estimate the bioaccessible rather than the
bioavailable fraction. In truth, remediation scientists
are probably more interested in what is bioaccessi-
ble over time at a given site than what is bioavailable.
Moreover, our proposed definitions raise a funda-
mental methodological question: Can the bioavail-
able 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 mi-
crobiology and ecotoxicology, Kieron J. Doick is a doc-
toral 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
Bioavailability
contamination includeprocesses
release of a solid-bound contaminant (A) and
subsequent transport (B), transport of bound contaminants (C), uptake
In both soil and sediment, processes that determine exposure to con-
across a physiological membrane (D), and incorporation into a living
tamination include release of a solid-bound contaminant (A) and subse-
system (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 process-
the lumen of the gut. The NRC report defines A, B, C, and D to be bio-
es 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 C
Absorbed Site of
contaminant in biological
Association A Dissociation D organism response
E
Released
contaminant B
Source: Ref. 1.
at the Pesticides Safety Directorate in the United
Kingdom. Hauke Harms is a professor of environmen-
tal microbiology at the UFZ Centre for Environmental
Research in Germany. Address correspondence to Semple
at k.semple@lancaster.ac.uk.
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