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Journal of Toxicology and Environmental Health, Part A

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Bottom-Up and Top-Down Integration of Human And Ecological Risk Assessment

Glenn W. Suter II a a National Center for Environmental Assessment, U.S. Environmental Protection Agency, Cincinnati, Ohio, USA Online Publication Date: 01 April 2004 To cite this Article: Suter II, Glenn W. (2004) 'Bottom-Up and Top-Down Integration of Human And Ecological Risk Assessment', Journal of Toxicology and Environmental Health, Part A, 67:8, 779 - 790 To link to this article: DOI: 10.1080/15287390490428233 URL: http://dx.doi.org/10.1080/15287390490428233

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Journal of Toxicology and Environmental Health, Part A, 67:779790, 2004 Copyright Taylor & Francis Inc. ISSN: 15287394 print / 10872620 online DOI: 10.1080/15287390490428233

BOTTOM-UP AND TOP-DOWN INTEGRATION OF HUMAN AND ECOLOGICAL RISK ASSESSMENT

Glenn W. Suter II National Center for Environmental Assessment, U.S. Environmental Protection Agency, Cincinnati, Ohio, USA

The World Health Organization has published a framework for integrating human health and ecological risk assessments, and many others have argued for greater integration of health and environmental concerns in assessments. However, those who argue for integration do not agree on the expected benefits. This article provides a conceptual organization of the rationale for integration. The bottom-up line of argument begins with the premise that the mechanisms of transport, fate, exposure, and effects of chemicals on humans and nonhuman organisms are largely common. Therefore, integrated assessment should be more efficient and should employ the highest quality of science. The top-down line of argument begins with the premise that humans are organisms that reside in ecosystems. Therefore, changes in the environment imply changes in human health and welfare. These include changes in the many services of nature that contribute to human health, such as air and water purification, sentinel functions, and provision of recreation and food supplies. They also include the direct health benefits that have been associated with exposure of humans to plants, animals, and natural ecosystems. Integration should proceed from both the top and bottom.

In current practice, human health risk assessments and ecological risk assessments are typically conducted independently. Recently, some assessors have begun to realize that there are potentially large advantages to integrating those two assessment practices and potentially others such as economic and cultural impact assessments (Harvey et al., 1995; Suter, 1997; Cirone & Duncan, 2000; Di Giulio & Benson, 2002; Suter et al., 2003a). In particular, the World Health Organization (WHO) recently published a framework for integrated health and ecological risk assessment (WHO, 2001; Suter et al., 2003b). This article argues that the rationale for integration is clarified and expanded by considering two perspectives. The bottom-up perspective begins with the current practices of health risk assessors and ecological risk assessors, and asks how their work might be improved by integration. The top-down perspective begins by looking at the environment and asking how the assessment of anthropogenic risks might best be organized.
Accepted 6 August 2003. Address correspondence to Glenn W. Suter II, National Center for Environmental Assessment, U.S. Environmental Protection Agency, 26 W. Martin L. King Dr., MC-117, Cincinnati, OH 45268, USA. E-mail: suter.glenn@epa.gov 779

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BOTTOM-UP INTEGRATION Integration may begin at the level of practicing human and ecological risk assessors performing their tasks of data collection and analysis. To the extent that they are not inhibited by institutional barriers or methodological constraints, those two types of assessors may find that they can do their jobs better and more easily by collaborating (Figure 1). The benefits of this bottom-up integration include the following from the WHO report. Efficiency Integration of human health and ecological risk assessments offers significant increases in efficiency. For example, the processes of contaminant release, transport, and transformation are common to all receptors. Although only humans shower in water and only aquatic organisms respire water, many routes of uptake are common to both, and the processes that introduce the contaminants to water, degrade or transform them, and partition them among phases are common to all. Therefore, there are clear advantages in an integrated exposure model. Quality The scientific quality of assessments is improved through sharing of information and techniques between scientists from different fields. For example, in assessments of contaminated sites, human health assessors may use default uptake factors to estimate plant uptake, unaware that ecological assessors are measuring contaminant concentrations in plants from the site. Conversely, knowledge of mammalian toxicokinetics has been used in risk assessments for humans but is seldom used in assessments for wildlife. More fundamentally, environmental epidemiologists have come to realize that they must incorporate insights and techniques from population and ecosystem ecology (Pekkanen & Pearce, 2001). Sentinel Organisms Because nonhuman organisms often are more heavily exposed to environmental contaminants and may be more sensitive, they can serve as sentinels, suggesting potential sources of human hazards (NRC, 1991; Burkhart & Gardner,

Hazardous Agents

Human Health

Ecosystems

FIGURE 1. Bottom-up integration: Human health and ecological risk assessors have separate mandates to assess effects of hazardous agents but they exchange information to increase their efficiency and the quality and utility of their products.

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1997; Stahl, 1997; Sheffield et al., 1998; van der Schalie et al., 1999; Colborn & Thayer, 2000; Fox, 2001). Although the use of sentinels to prompt further study is not controversial, there are significant technical difficulties in going further and estimating risks to humans by extrapolating from observed effects on nonhuman species (Stahl, 1997). These difficulties result from differences in routes of exposure and in mechanisms of toxicity. However, human health assessors should carefully determine what information can be derived from sentinels rather than ignoring them, as is typically the case. In the authors experience, the public often has a better appreciation of sentinel organisms than health risk assessors. If the fish have tumors or the birds have deformities, the public that shares the environment with these organisms will be concerned, and assessors who have not integrated the health assessments with ecological assessments may have difficulty explaining why the public should or should not be concerned. The much higher exposure of nonhuman organisms to environmental contaminants makes them good sentinels, but observed ecological effects do not imply concurrent health effects. However, in some cases the high levels of effects on sentinel organisms may serve as estimators of much lower human health risks. For example, the New York State Department of Health has used dead crow density to estimate human risk from West Nile virus (Enserink, 2001). Coherent Expression of Assessment Results Coherent results of integrated health and ecological risk assessments provide a strong basis for action to support decision making. This point has been made by the U.S. Environmental Protection Agency (EPA) Science Advisory Board (SAB), which called for more integrated decision making, implying a need to integrate health and ecological risk assessment (SAB, 2000). However, when the results of independent health and ecological risk assessments are derived in an inconsistent manner and the bases for the inconsistency are unclear, decision making is complicated. Health and ecological risk assessments may be inconsistent because they are based on different spatial and temporal scales, different degrees of conservatism, or different assumptions, ranging from assumed parameter values to assumed land use scenarios. As a result, decision makers may find it difficult to decide if, for example, risks to humans justify a remedial action that will destroy an ecosystem. As another example, consider a decision whether to license a new pesticide that poses a decreased risk to humans and an increased risk to aquatic communities relative to a current pesticide. If the ecological risks are based on expected effects on a spatially distributed community, while the health risks are based on provision of a margin of safety on an effect level for a hypothetical, maximally exposed individual, the two estimates of risk cannot be compared. TOP-DOWN INTEGRATION An alternative approach to organizing an integrated practice of environmental assessment is to begin by asking what is the nature of the system in which

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environmental risks occur? It consists of one planet with both human and nonhuman organisms inhabiting the same air, water, and land and interacting in complex ways. Given that self-evident conclusion, we may reconsider the types of endpoints that must be assessed in order to provide the necessary scope of protection and ask whether the current health/ecology dichotomy makes sense. Human Health Risk The primary concern of the U.S. EPA has been the protection of human health from the direct effects of environmental contaminants. These include pesticides, industrial chemicals, radionuclides, pathogens, and atmospheric gases and particles. Conceptually, these assessments are simple; the dose to a hypothetical member of a susceptible human subpopulation is estimated, a dose-response relationship is estimated, and the two are combined to estimate the risk to such individuals. The results of these assessments are important because of the high value placed on human life and health. Even when toxic effects on human health are mediated by ecological processes, as in the promotion of toxic algal booms by nutrient pollution, the ecological processes that generate the bloom are seldom addressed in the health risk assessment (Van Dolah, 2000). Ecological Risk The contaminants that directly affect humans also directly affect a variety of nonhuman animals, plants, and microbes. In addition, they affect properties of higher levels of organization including populations, ecosystems, watersheds, and ecoregions. Further, the direct effects ramify through these systems, causing secondary and tertiary effects, such as loss of food and habitat for animals due to direct toxic effects on plants. Finally, various agents that have not concerned human health risk assessors are critically important for ecological risk assessment. These include alien competitors and predators, habitat loss, excess nutrients, and altered flow regimes. For these reasons, ecological risk assessments may be quite complex and difficult. Ecological risks are important because nonhuman organisms, populations, and ecosystems, like humans, are valued per se. That is, although animals are not valued to the same extent as humans, environmental laws and public sentiment require protection of the environment and its components. While the limited scope of human health risk assessment is in large part due to a focus on only one species and one level of biological organization, it is also due to a narrow vision of how humans are affected by the environment. While ecological risk assessors, like health risk assessors, are concerned with direct toxic effects, they are also concerned with indirect effects by mechanisms other than toxicity. Hence, to make environmental risk assessment for humans equivalent to ecological risk assessment, we must add at least one more category of environmental risks (human welfare) and possibly another (ecological promotion of human health).

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Human Welfare One missing component of environmental assessments is human welfare. Humans obtain a wide range of benefits from the environment, often termed services of nature, which make human life possible and enhance the quality of those lives (Daily & Ellison, 2002; Daily et al., 2002). At the most basic level, plants capture the energy of the sun and produce food for humans and their livestock and convert our CO2 into O2. Other life-support functions of ecosystems include purification of the water, air, and soil and cycling of water and nutrients. In addition, ecosystems produce a variety of goods, such as timber, fisheries, biomass fuels, and medicinal herbs, roots, and spices. These services are estimated to be worth more than the entire human economy (Costanza et al., 1997; Naeem et al., 1999). A more subtle aspect of this issue is improvements in the quality of human life provided by nature (Keach, 1998). An obvious example is the regenerative effect of a vacation spent fishing, hunting, bird watching, hiking, photographing nature, or simply visiting natural places. However, day-to-day contact with nature, such as walking in parks, feeding birds, and observing trees, flowers, and butterflies, may be more important to the quality of life. The importance of this relationship to peoples quality of life is reflected in various behavioral and economic measures, including the billions spent on feeding birds and the value of houses on large lots in the outer suburbs or on bodies of water. The inverse of this relationship is the consternation people feel when they observe trees dying along highways, dead fish along a river, or even images of oiled birds on the television. The idea that humans are naturally attentive to nature and benefit from the opportunity to observe and participate in nature has been termed biophilia (Kellert & Wilson, 1993). Finally, cultural values are often related to aspects of the environment. This is particularly true of indigenous peoples whose cultures require the use of certain natural resources and the presence of certain environmental features (Harris & Harper, 2000). The same is true of nonindigenous cultures, although in less obvious ways. Examples from the United States include the bald eagle as a national emblem and unspoiled wide-open spaces as a backdrop for the national mythos of cowboys and hearty pioneers. Ecological Promotion of Human Health This list of issues is brought full circle by the increasing body of evidence suggesting that the experience of nature affects human health. Various studies have shown an improvement in mental and physical health status of people exposed to animals, plants, or views of nature (Hartig et al., 1991; Frumkin, 2001; de Vries, 2001). One study showed that surgery patients recovered more quickly and required less medication for pain when the windows in their rooms faced a stand of trees than when they faced another building (Ulrich, 1984).

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IMPLICATIONS The top-down view suggests that the relationship between humans and the environment is too complicated to be resolved by simply bringing together health risk assessment and ecological risk assessment for the sake of efficiency and clarity. Rather, there is a complicated set of interrelations among risks to human health, human welfare, and ecosystems. Human welfare requires a functioning environment that satisfies material, aesthetic, and emotional needs. Human health depends on human welfare in obvious ways, which means it also depends indirectly on the environment. More subtly, health appears to benefit directly from an experience of ecological integrity. Conversely, environmental protection seems to be best achieved where people have sufficient welfare to not despoil the environment for short-term subsistence. Clearly, the assessment of human welfare is missing from current practice. Human health risk assessors address only the relatively simple problem of direct effects of contaminants on health. Ecological risk assessors address the more complex, but still concrete, problem of effects of contaminants on nonhuman organisms, populations and ecosystems. Normally, risks to human welfare from contaminants are not assessed. An obvious impediment is the fact that welfare is not as easily defined or recognized as human health, ecosystem production, or fish abundance. Human welfare is a state that results when people inhabit an environment with a particular mixture of natural, built, and cultural features. It results from the provision of nutrition, shelter, clothing, knowledge, sociality, recreation, and many other things requiring material products of nature, functions of nature, or the experience of nature in some combination with human culture. An implicit assumption of current environmental assessment practices is, if we protect human health and the natural environment, we will protect human welfare. Certainly that is true to a large extent, but more by happenstance than design. Although ecologists and environmental advocates point to services of nature as justification for environmentally protective regulations or enforcement, when designing and conducting research and assessments, ecologists focus on ecological attributes for their own sake or for the sake of the ecosystems of which they are a part. This is both ethically and legally appropriate. For example, the U.S. Clean Water Act requires protection of biological integrity, not protection of ecosystem services to humans. While this focus on ecology per se is likely to enhance human welfare, it does not guarantee it. Of the nearly infinite combination of ecological entities and attributes that may be chosen as ecological assessment endpoints, it is unlikely that the ones most important to human welfare would be chosen by ecologists. In particular, risks to ecological functions such as nutrient retention, removal of pathogens, or hydrological regulation are almost never assessed. Similarly, health risk assessors focus on cancer, developmental defects and so on; and do not expand their assessments to consider welfare. Neither group desires to take on the burden of expanded responsibilities. How might a more inclusive practice of environmental risk assessment be attained?

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Human health risk assessors might, like ecological risk assessors, broaden their vision to include both the direct and indirect effects of environmental disruption on humans (i.e., health and welfare) (Figure 2). This would seem to be precluded by the narrow mandates of health risk assessors and their exclusive focus on direct health effects. However, there are some signs of enlightenment, especially in the assessment of effects of global climate change on humans. A new assessment practice would arise with its own legal mandate to assess risks to human welfare. While this makes some sense, there is no apparent impetus for it (Figure 3). More realistically, assessment of risks to human welfare are likely to be performed as part of ecological risk assessment (Figure 4). The impetus comes from requirements for costbenefit analysis for environmental regulations. While the U.S. EPA has derived a standard value for human life ($6 million), there are no such standard values for ecological entities. In theory, almost any regulatory cost to protect ecosystems could be balanced by benefits to

Hazardous Agents

Human Welfare Human Health Ecosystems

FIGURE 2. Top-down integration in which human health risk assessors receive a mandate to consider all risks to human welfare as a result of hazardous agents in the environment.

Hazardous Agents

Human Health

Human Welfare

Ecosystems

FIGURE 3. Top-down integration in which a separate mandate to is created to perform assessments of environmental risks to human welfare. Welfare assessments are related to both ecological risk assessment and human health risk assessment, and, in addition, health risks may be directly related to environmental conditions.

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Hazardous Agents

Ecosystems Human Health Human Welfare

FIGURE 4. Top-down integration in which ecological risk assessors receive a mandate to consider risks to human welfare resulting from hazardous agents in the environment.

human welfare. In fact, the potential economic value of nature is so great that it has been suggested that environmental protection could be achieved by market forces alone (Daily & Ellison, 2002; Dailey, 2003). The classic example is New York City, which avoided spending $68 billion for a water treatment facility, plus operating costs, by spending $1.5 billion to protect the watersheds that supply the citys drinking water (Daily & Ellison, 2002). Ideally, environmental risk assessments would be truly integrated; human health would be a component of human welfare and human welfare would be a function of environmental modification (Figure 5). That is, a multidisciplinary team would develop an integrated assessment that would estimate the range of consequences of a proposed action. This is the type of assessment that was mandated by the National Environmental Policy Act (NEPA) of 1970. In particular, the act is concerned with restoring and maintaining environmental quality to the overall welfare and development
Hazardous Agents

Ecosystems Human Welfare Human Health

FIGURE 5. Top-down integration in which risk assessors receive a mandate to assess risks to human and nonhuman organisms as an integrated system. Human health is a subsystem of human welfare, which is a subsystem of the planetary environment.

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of man (Sec. 101, 42 USC 4331). However, the U.S. EPA does not perform NEPA assessments, and the environmental laws under which it assesses human and ecological risks have narrower or less integrative mandates. If the U.S. EPA adopted NEPA for the evaluation of its own actions, it could provide more complete assessments of consequences for the human environment system. INTEGRATED ASSESSMENT AND DECISION MAKING Integrated assessment approaches, whether based on NEPA or other considerations, could stimulate creative approaches to environmental regulation and management. For example, it has been suggested that cleanup of the major nuclear facilities is not only inordinately expensive but also environmentally destructive without significant benefits to human health. The major nuclear facilities in the United States include large areas that are relatively undisturbed and highly biodiverse, so the potential for ecological injury during remediation is great (Dale & Parr, 1998). Stabilization of wastes and maintenance of the sites as National Environmental Research Parks or equivalent uses could (1) reduce risks to human and ecological health, (2) protect cultural traditions, and (3) lower short-and long-term cleanup and remediation costs (Burger et al., 2003). However, that would require assessments of human welfare that look beyond health risks to hypothetical future homesteaders. It would require consideration of the net human and ecological benefits of alternative actions, which would require integrated risk assessments. PROSPECTS Bottom-up integration is practical and is already occurring to some extent. It must be encouraged and extended. Coordination and cooperation between human and ecological risk assessors could result in better and more useful human and ecological risk assessments. However, it is unlikely to result in assessment of the complex interactions among human and nonhuman inhabitants of the environment because it is focused on the existing disciplines. Top-down integration that involves explicit assessment of risks to human welfare would require institutional change and possibly new legislation. NEPA provides the mandate for such a broad view of environmental assessment and management, but only its procedural provisions have been implemented (Bear, 1989). A broader vision of environmental assessment and management may arise from the increasing dominance of the earths processes by human activities resulting in water shortages, flooding, climate change, soil loss, eutrophication of coastal waters, collapse of fisheries, and similar results of unsustainable resource management practices (Pimm, 2001). Just as Rachel Carsons popularization of the DDT story created the mandate for assessing risks from pesticides and other chemical pollutants, some vivid issue must eventually awake the public to the reductions in their welfare due to lost services of nature.

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In the interim, the only group that is likely to assess the issue of human welfare is ecological assessors. This seems grossly unfair, since they already reponsible for assessing risks to all but one of the thousands of species exposed to a chemical or other agent with only a small fraction of the research and assessment budget. Why should they pick up all assessment issues related to the human species except for direct toxic effects? They have three reasons. (1) As already mentioned, the monetary benefits from environmental protection are relatively easily calculated if they can be related to human welfare. (2) Unlike human health risk assessors, ecologists have the requisite skills in analysis of organism-environment interactions. (3) Ecologists want to influence decision makers to provide more environmental protection. Hence, they are likely to carry a large part of the burden of assessing risks to human welfare. However, most ecologists are reluctant to do so, and not only because it means extra work. Translating ecological effects into effects on human welfare within ecological risk assessments creates the false impression that protecting the environment for its own sake is not enough to justify regulatory or remedial actions. While integration is potentially beneficial for any environmental assessment, it is more likely in location-specific assessments than in assessments of new chemicals or technologies. That is because, when addressing the problems of a waste site and adjacent human or natural communities, a town with multiple pollution sources distributed among developed areas and natural areas, a lake that is used for recreation and aqueous waste disposal, or other place, the connections between the environment and human welfare become evident. A particularly good opportunity for integrated assessment is provided by the U.S. EPA program for watershed protection, which uses committees of stakeholders and local officials to develop concerted plans for management of resources and human activities in a designated watershed (U.S. EPA, 1996; Serveiss, 2002). Such committees are less constrained by traditional disciplinary compartments and are more likely to consider a broad range of benefits from the watershed than professional assessors or agency managers. CONCLUSIONS There is only one environment that receives pollutants and physical damage resulting in risks to humans and other organisms. Any remedial or regulatory decision must serve to benefit humans, nonhuman organisms, or ecosystems and should not do disproportionate harm to one class of receptors to benefit another. If integrated assessment results are not provided, the decision maker must either integrate the results him- or herself or choose between human health and ecology as the risk that informs the decision. Hence, assessment scientists should go outside their comfortable niches and consider how they might better inform those decision makers of the full range of consequences of alternative decisions. Such integration might lead to creative decisions that provide greater net benefits than conventional regulatory approaches.

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