Summary

Identifying, controlling, and preventing population exposures to potentially harmful environmental chemicals have been cornerstones of U.S. environmental health efforts. Biomonitoring has become a tool that is central to these efforts. Repeatedly, biomonitoring data have confirmed environmental exposures and validated public-health policies. For example, population data on blood lead concentrations associated with adverse health effects provided impetus for the U.S. Environmental Protection Agency’s (EPA’s) regulatory reduction of lead in gasoline. Blood lead concentrations declined in parallel with the resulting reduction. Methylmercury concentrations in blood and hair that correlated with adverse neurodevelopmental effects provided a rationale for EPA’s revision of the oral reference dose.1 Serum cotinine, a marker of exposure to secondhand smoke, in U.S. children and adults declined by more than 50% among nonsmokers from 1998 to 2002, indicating the effectiveness of smoking cessation efforts in the United States.

Biomonitoring is defined in this report as one method for assessing human exposure to chemicals by measuring the chemicals or their metabolites in human tissues or specimens, such as blood and urine. In studies conducted by the Centers for Disease Control and Prevention (CDC), biomonitoring data have helped to identify chemicals found in the environ-

1

A reference dose is an estimate (with uncertainty spanning perhaps an order of magnitude) of a daily oral exposure to the human population (including sensitive subgroups) that is likely to be without an appreciable risk of deleterious effects during a lifetime.



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Human Biomonitoring for Environmental Chemicals Summary Identifying, controlling, and preventing population exposures to potentially harmful environmental chemicals have been cornerstones of U.S. environmental health efforts. Biomonitoring has become a tool that is central to these efforts. Repeatedly, biomonitoring data have confirmed environmental exposures and validated public-health policies. For example, population data on blood lead concentrations associated with adverse health effects provided impetus for the U.S. Environmental Protection Agency’s (EPA’s) regulatory reduction of lead in gasoline. Blood lead concentrations declined in parallel with the resulting reduction. Methylmercury concentrations in blood and hair that correlated with adverse neurodevelopmental effects provided a rationale for EPA’s revision of the oral reference dose.1 Serum cotinine, a marker of exposure to secondhand smoke, in U.S. children and adults declined by more than 50% among nonsmokers from 1998 to 2002, indicating the effectiveness of smoking cessation efforts in the United States. Biomonitoring is defined in this report as one method for assessing human exposure to chemicals by measuring the chemicals or their metabolites in human tissues or specimens, such as blood and urine. In studies conducted by the Centers for Disease Control and Prevention (CDC), biomonitoring data have helped to identify chemicals found in the environ- 1 A reference dose is an estimate (with uncertainty spanning perhaps an order of magnitude) of a daily oral exposure to the human population (including sensitive subgroups) that is likely to be without an appreciable risk of deleterious effects during a lifetime.

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Human Biomonitoring for Environmental Chemicals ment and in human tissues, to monitor changes in exposure, and to investigate the distribution of exposure among the general population. Biomonitoring provides a measurement of exposure that—when used with available epidemiologic, toxicologic, and pharmacokinetic modeling data—can be used to estimate how much of a chemical has been absorbed into the body and to provide an indicator of potential health risk. State and local officials can use biomonitoring data to help assess environmental risks to specific sites or populations. In occupational and clinical medicine, biomonitoring can be used as a surveillance tool to help interpret a clinical problem or to monitor an exposure trend. Biomonitoring, in short, is a versatile means of assessing exposure. Many population-based biomonitoring efforts are taking place in the United States and in Europe. In the United States, CDC publishes periodic national reports on human exposure to environmental chemicals that detail the concentrations of chemicals and their breakdown products in blood and urine of a representative sample of the U.S. population. Other government organizations, including EPA and the National Institutes of Health (NIH), are conducting and sponsoring biomonitoring studies. In spite of the potential value of biomonitoring, tremendous challenges surround its use. They include improving our ability to design biomonitoring studies, interpreting what biomonitoring data mean for public health, addressing ethical uses of the data, and communicating results to study participants, policy-makers, and the public. The ability to generate new biomonitoring data often exceeds the ability to evaluate whether and how a chemical measured in an individual or population may cause a health risk or to evaluate its sources and pathways for exposure. As CDC states in its National Reports on Human Exposure to Environmental Chemicals, the presence of a chemical in a blood or urine specimen does not mean that the chemical causes a health risk or disease. The challenge for public-health officials is to understand the health implications of the biomonitoring data, to provide the public with appropriate information, and to craft appropriate public-health policy responses. To address some of those challenges raised by biomonitoring data, Congress2 directed EPA to ask the National Research Council (NRC) of the National Academies to perform an independent study. CHARGE TO THE COMMITTEE In response to the request, the NRC established the Committee on Human Biomonitoring for Environmental Toxicants, which prepared this 2 In the conference report to accompany H.R. 2861, the Department of Veterans Affairs and Housing and Urban Development, and Independent Agencies Appropriations Act, 2004.

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Human Biomonitoring for Environmental Chemicals report. The committee was charged to review current practices and recommend ways to improve the interpretation and uses of human biomonitoring data on environmental chemicals. It was asked to develop an overall research agenda for addressing the uncertainties in biomonitoring data, to improve evaluations and characterizations of health risks from biomonitoring data, and to improve tracking of changes in biomonitoring data potentially relevant to public health. In undertaking its evaluation, the committee focused primarily on biomonitoring in population-based studies, such as CDC’s National Report on Human Exposures to Environmental Chemicals and EPA’s National Human Exposure Assessment Survey, because these studies raise the most far-reaching and challenging issues regarding the interpretation of biomonitoring data. The population-based studies have demonstrated that representative samples of the population have relatively low concentrations of chemicals in their bodies; 3 however, for most of these chemicals, the data and methods needed to interpret what the concentrations mean are often not available. The committee also considered applications of biomonitoring beyond the population-based studies—such as source investigations, occupational investigations, and individual risk characterization— since biomonitoring is used for myriad purposes. THE COMMITTEE’S EVALUATION Biomonitoring is a tool with great potential. It has been of value in identifying human exposures to chemicals that pose potential harm to human health, in understanding exposure status and trends, in fostering public-health interventions, and in validating environmental-health policies. Rapidly developing technological capabilities to measure chemicals in the human body have increased the availability of biomonitoring information. However, the complete potential of this tool has yet to be realized, inasmuch as the science (epidemiology, toxicology, pharmacokinetic modeling, and exposure assessment) needed to understand the implications of biomonitoring data for human health is still in its nascent stages. For some chemicals (such as mercury and lead), the health risks and effects are well known; but for most of the chemicals currently measured, the risks cannot be interpreted. Scientists, policy-makers, and the public are just beginning to grasp the tremendous ethical and communication challenges that the biomonitoring data are creating. In this report, the committee presents a roadmap for addressing many of the unanswered questions. The roadmap begins with a framework for 3 In the 1-part-per-billion (ppb) range or below for many commonly used chemicals or their breakdown products.

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Human Biomonitoring for Environmental Chemicals characterizing the properties of biomarkers of exposure4 and understanding the potential uses of the data. The committee then describes scientific principles and practices to ensure the proper conduct of biomonitoring studies; the guidelines are essential to ensure valid collection of the biomonitoring data. The committee uses this framework to illustrate various options for interpreting biomonitoring data, which depend on the properties of specific biomarkers. Chemical-specific data are used to demonstrate the various interpretative options. Challenges in communicating results in light of the difficulty of interpreting the data are discussed. In the sections that follow, the committee presents its roadmap and the findings and recommendations in the research agenda that have evolved from the roadmap. Framework for Characterizing Biomarkers and Uses of Biomonitoring Data As the number of biomonitoring studies and the number of subjects and chemicals measured increases, there is a need for clarification of the appropriate uses and interpretation of biomonitoring data. The general public needs to know the meaning and limitations of the data, and public-health officials, who are often called on for interpretation of results, also need to be adequately informed. In Chapter 3 of this report, the committee presents a systematic framework or matrix to characterize the properties of biomarkers as a means to inform scientists and the general public about biomarkers and their significance in biomonitoring studies. The framework generally summarizes what is known about a biomarker and indicates potential research gaps that need to be addressed to meet the requirements for some specific uses. The framework is intended to crystallize scientific discussion of specific biomarker issues. The committee recommends that investigators undertaking biomonitoring studies use the framework for considering all biomarkers that they intend to use. The framework will serve as a guide for interpreting the studies, in setting priorities among research needs, and in communicating study objectives to various audiences. Considerations in the Design of Biomonitoring Studies The National Report on Human Exposure to Environmental Chemicals, produced by CDC, is based on a representative sample of the population and a large number of chemicals, and uses well-documented analytic techniques. However, not all biomonitoring studies are conducted with the 4 A biomarker of exposure is a chemical, its metabolite, or the product of an interaction between a chemical or some target molecule or cell that is measured in humans.

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Human Biomonitoring for Environmental Chemicals same rigor as the CDC studies. In Chapter 4 of this report, the committee discusses scientific practices in biomonitoring (study design, conduct, and analysis). Issues of design include selecting biomarkers for the study, identifying the population to be sampled, developing the sampling strategy to address the study questions or objectives, and assessing communication and ethical considerations. Study conduct includes consideration of the appropriate tissue or specimen to use, collection of samples, transportation of samples to the laboratory for analysis, and banking of the samples for additional analysis. Epidemiologic and statistical analyses stem from the objectives of the study design. The committee concludes that it is critical for biomarker researchers to adhere to appropriate statistical principles when sampling populations to ensure that the biomonitoring results are valid and representative of the sampled population. In addition, biomarker studies should collect detailed information on cofactors (for example, socioeconomic status and lifestyle factors) to facilitate interpreting the data—an inconsistent practice at present. Laboratory analysis of human samples for trace concentrations of chemicals inevitably introduces some deviation from the true concentration into the sample results; federal agencies, such as CDC and the National Institute for Standards and Technology, and statutes, such as the Clinical Laboratory Improvement Act, could play important roles in improving the overall quality of biomonitoring data and their utility for health-related applications. Incorporating communication in the design of a biomonitoring study is essential to ensure easier communication at the end of the study and may make the technical aspects of the study proceed more smoothly. To that end, the committee recommends that biomonitoring program sponsors require planning for communication and evaluation in any application for funding. Interpreting Biomonitoring Data Considerable controversy often surrounds the interpretation of biomonitoring data. Researchers are generating biomonitoring data whose relevance to human health is unclear in many cases. For example, news-media reports present stories of people who have had their blood tested and are alarmed to learn that it contains hundreds of chemicals. For a number of those chemicals, scientific data could enable interpretation of individual measurements in comparison with validated reference values, but usually the interpretation stops with the mere observation that the chemical is present. Biomonitoring data may be interpreted through either descriptive or risk-based approaches. The descriptive approaches present a statistical review of the data (for example, 10th, 25th, 50th, 75th, and 90th percentiles) to relate a given population to a comparable or reference population. Risk-based approaches are much more data-intensive and may use toxico-

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Human Biomonitoring for Environmental Chemicals logic, epidemiologic, or pharmacokinetic modeling data to relate biomonitoring data to other measures of toxicity in an effort to evaluate the risk associated with the amount of chemical in the body. Risk-based approaches potentially can provide better information on the health effects related to the biomonitoring data. However, for most chemicals that are capable of being measured in the human body, the available data are insufficient to assess risks based on measured concentrations. Because some of the interpretative approaches involve modeling and extrapolation, there are additional uncertainties and limitations in assessing the biomonitoring results. Understanding the uncertainties and limitations is important both for providing full disclosure regarding the reliability and credibility of the biomonitoring results and for defining data gaps and research needs. Several risk-based approaches may be used, depending on the data available. The strongest approach, biomonitoring-based risk assessment, relies on biomarker-response relationships established in epidemiologic studies. Few chemicals are in that data-rich category (lead and mercury are two). Risk assessments that combine data from animal toxicology and human-exposure assessment studies can also be used to interpret biomonitoring data; the biomonitoring results may be interpreted within the context of the results of the risk assessment. Interpretations of chemical exposures that have used that approach include the herbicide glyphosate and the insecticide permethrin. For most other chemicals, however, there are no epidemiologic data on the relationship between the biomarker and the effect, and the exposure sources and routes are not known. Therefore, interpretation of the biomonitoring data is not possible via traditional risk assessment approaches, and an alternative risk-based approach, biomonitoring-led risk assessment, is used. In this case, pharmacokinetic modeling techniques are applied to convert the biomonitoring data into a format that can be used as exposure information in risk assessments. The specific approaches that may be used depend on the properties of each chemical and on the data available. Chemicals that have been subjected to biomonitoring-led risk assessment include dioxin, chlorpyrifos, perfluorooctanoic acid (PFOA), and phthalates. The committee concludes that descriptive approaches are often important in laying a foundation on which risk-based approaches can build. The interpretative power of risk-based approaches varies widely, depending on the information available. To improve the interpretation of biomonitoring results, an expansion of the scientific database on many chemicals is needed. Communicating Results from Biomonitoring Studies Communicating biomonitoring results may be the most vexing challenge to the field of biomonitoring. Communication is essential to proper

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Human Biomonitoring for Environmental Chemicals interpretation and use of biomonitoring data, and it is intimately intertwined with and as important as technical aspects of biomonitoring. There is no one recipe for good biomonitoring communications, which will vary by study goals, the population sampled, biomarkers selected, exposures and health effects assessed, and audiences. If done properly, communication can assist experts to reach consensus on the meaning of biomonitoring results and help institutional and individual decision-makers determine appropriate courses of action. To achieve proper communication requires explicit funding, early planning, and empirical evaluation of communication methods and messages. Perhaps most critically, early planning must assess the needs of the various audiences for biomonitoring information, and the study must be designed to meet those needs if feasible. Achieving these goals might entail pursuing partnerships with one or more audiences on project design, implementation, or interpretation and communication. Only rarely will communication with constituencies be one-way only (for example, scientists to public or policy-makers). In Chapter 6, the committee presents several practical and research recommendations to address communication challenges. Practical measures include use of consistent terminology and concepts, expanded biomonitoring education for constituencies, communication training, and public documentation of methods to reduce exposures contributing to biomarkers of concern. Research measures include identifying how experts and nonexperts think about exposure and health effects, assessing current biomonitoring communication methods and impacts, identifying communication issues with respect to uncertainties in biomonitoring studies, and identifying beliefs and attitudes about exposure reduction and risk managers. Given the central role of communication in the interpretation and use of biomonitoring data and the great uncertainty about what makes communication effective, building infrastructure and research in this field must have high priority for biomonitoring investigators and sponsors. RESEARCH AGENDA To realize the potential of biomonitoring, investment in research is needed to address the critical knowledge gaps that hinder the ability to use biomonitoring data and interpret what they mean with respect to risks to public health. The committee’s research recommendations focus not on specific chemicals but rather on methods that can be applied to a broad array of chemicals. Implementation of the research recommendations by federal and state agencies and universities will benefit from an improvement in some parts of our nation’s research infrastructure.

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Human Biomonitoring for Environmental Chemicals Research Recommendations To address the challenge of improving the interpretation and use of biomonitoring data, the committee has developed four major findings and corresponding research recommendations. They will require a broader vision of biomonitoring—one that integrates a scientific approach for setting priorities among biomarkers for development; supports the epidemiology, toxicology, and exposure-assessment science required to interpret biomonitoring data; develops strategies for advancing the reporting of biomonitoring results; and strengthens understanding of the ethical issues that constrain the advancement of this field. Finding: There has not been a coordinated and consistent public-health-based strategy for selecting how chemicals are included in or excluded from biomonitoring studies. There is a need for a consistent rationale for selecting chemicals for study based on exposure and public-health concerns. Recommendation: Develop a coordinated strategy for biomarker development and population biomonitoring based on the potential for population exposure and public-health concerns. Biomonitoring offers great promise as an effective technique for identifying chemicals and exposures of potential public-health significance. The committee finds that broad population screening for a large number of chemical biomarkers has provided valuable and, at times, surprising evidence of human exposure. That type of screening should continue. However, it can be improved. Most current biomonitoring relies on biomarkers that are generated through a variety of research avenues (such as epidemiology, analytic chemistry, and workplace monitoring), but the uncoordinated fashion in which such biomonitoring has occurred has allowed widespread exposures to go undetected—for example, polybrominated diphenyl ethers and PFOA. In addition, susceptible subpopulations, including infants and children, are generally omitted from large-scale biomonitoring studies because of difficulty in sample collection. The committee recommends that a coordinated scientific strategy be developed to ensure that the selection of chemicals and the development of biomarkers focus first and foremost on the potential of chemicals to cause harm and consider the likelihood of substantial or widespread population exposure, including exposure of susceptible subpopulations. The biomonitoring strategy needs to set priorities among chemicals on the basis of one or more of the following: evidence of substantial or widespread exposure of the general population, biomonitoring data or exposure-analysis information that indicates exposure of susceptible subpopulations, toxicologic data

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Human Biomonitoring for Environmental Chemicals indicating that a chemical is capable of causing effects of public-health significance, and environmental persistence or use-pattern information that indicates that exposure will probably persist or increase in the future. Developing the coordinated scientific strategy will require input from various agencies involved in biomonitoring and supporting disciplines, including CDC, EPA, and NIH (especially the National Institute of Environmental Health Sciences, and the National Toxicology Program), as well as the Food and Drug Administration and the U.S. Department of Agriculture. The coordinated input from those agencies would ensure that population-based biomonitoring studies would target chemicals of public-health concern as well as chemicals that are prudent to monitor because of exposure considerations. The scientific strategy would need to be transparent and well explained. Such a coordinated approach might reduce redundancies in research efforts among agencies and help to leverage funds for the most pressing public-health questions. Finding: The ability to detect chemicals has outpaced the ability to interpret health risks. Epidemiologic, toxicologic, and exposure-assessment studies have not adequately incorporated biomonitoring data for interpretation of health risks at the individual, community, and population levels. Recommendation: Develop biomonitoring-based epidemiologic, toxicologic, and exposure-assessment investigations and public-health surveillance to interpret the risks posed by low-level exposure to environmental chemicals. Where possible, enhance existing exposure-assessment, epidemiologic, and toxicologic studies with biomonitoring to improve the interpretation of results of such studies. To better interpret biomonitoring data in the context of the committee’s framework and to understand the public-health implications of the data, the committee offers a number of research recommendations in epidemiology, toxicology, pharmacokinetics, and exposure assessment. Development of biomarkers in epidemiology is needed to improve understanding of the relationships between biomonitoring data and health effects. Such development includes increasing the number of biosamples collected and stored in epidemiologic studies to provide future research opportunities for assessing associations between biomarkers and outcomes in existing study designs. Likewise, animal toxicologic-study designs need to include the collection of relevant biomarker data to facilitate development of biomarker-response relationships for the purpose of extrapolating biomonitoring results to humans. NTP toxicologic protocols serve as a relevant example. The committee also recommends the development of pharmacokinetic models to help

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Human Biomonitoring for Environmental Chemicals assess the influence of such factors as metabolism and sampling time that are critical to interpretation of the biomonitoring data. To understand the sources of exposure better, when interpreting the biomonitoring data, exposure assessment should be a component of population-based biomonitoring studies. Specifically, in large-scale biomonitoring studies, the committee recommends inclusion of a detailed and accurate exposure analysis for a subset of the population. It should include information on environmental media that are relevant to the specific chemical exposure pathways. Finding: Effective communication of results is among the biggest challenges to the future of biomonitoring. Without appropriate strategies for understanding communication issues in the design, implementation, and evaluation of biomonitoring studies, the power to interpret and use the resulting data effectively is hampered. Recommendation: Advance individual, community, and population-based strategies for reporting results of biomonitoring studies. Given the central role of communication in interpreting and using biomonitoring data, research on public communication must have high priority for investigators and sponsors. To that end, the committee recommends research on how scientists and nonscientists understand causal links between external dose, internal dose, and biologic effects. In addition, assessing the content of current biomonitoring education and communication materials will help to evaluate their efficacy and determine the extent to which beliefs about causal linkages are accurately addressed in them. Finding: Biomonitoring research presents a number of ethical issues about informed consent and the interpretation of results. For example, biomonitoring research is conducted with anonymized samples that limit the communication of results and potential follow-up with study subjects. Recommendation: There is a need for review of the bioethical issues confronting the future of biomonitoring, including confidentiality, informed consent, reporting of results, and public-health or clinical followup. Participants in public-health studies that measure hundreds of biomarkers might give “informed consent” only with respect to the general objectives of the study on the grounds that detailed discussion of each biomarker is not feasible. However, failing to provide more detailed information raises ethical questions. The committee recommends research

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Human Biomonitoring for Environmental Chemicals to identify methods to ethically and practically inform subjects who are participating in biomonitoring studies that measure hundreds of chemicals in a single person. In addition, the committee recommends the development of new approaches for obtaining blanket consent for future uses of biomonitoring data, inasmuch as controversy surrounding this issue has led to increased difficulty in obtaining approval for some biomonitoring studies. Infrastructure Needs to Implement Research Agenda The current scientific infrastructure to support the committee’s research recommendations is severely limited. Improvements in research-related infrastructure are needed to support these recommendations and to enhance the value of biomonitoring activities. The infrastructure needs encompass enhancing laboratory capabilities, expanding the scope and utility of CDC’s National Health and Nutrition Examination Survey (NHANES) data, maximizing the use of collected human samples, and fostering international biomonitoring collaboration. Many of these recommendations for infrastructure improvement are cost-effective because they rely on expansion of structures and activities that are already in place. Targeted investments in federal, state, and university laboratories are needed to create the national capacity to use biomonitoring fully as a public-health tool. Analysis of human specimens for trace concentrations of environmental chemicals poses serious challenges to analytic chemistry. The growth in biomonitoring has provided for a new generation of more sensitive and selective instruments for chemical analysis; however, the costs associated with that equipment and the specialized skills required to perform the analyses have limited the number of laboratories capable of conducting the measurements. In recognition of the national deficiencies in laboratory capacity, CDC funded 33 states to identify local public-health problems and to develop plans to create the biomonitoring-laboratory capacity needed to address them; however, financial constraints limited the number of grants and the total amount of funding that was ultimately awarded. The committee recommends that CDC emphasize support of state public-health laboratories. In addition, improvements in laboratory methods are needed, including improved quality of laboratory data, better analytic sensitivity, ability to measure a greater number of chemicals reliably, and development of analytic methods that use more readily obtainable specimens (such as saliva, exhaled breath, and breast milk). The need for high-throughput, low-cost testing procedures will be increasingly apparent as biomonitoring techniques are more widely applied to large-scale epidemiologic studies and mass-casualty events, such as chemical terrorism or chemical accidents.

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Human Biomonitoring for Environmental Chemicals CDC’s National Reports on Human Exposure to Environmental Chemicals provide the most comprehensive summary of biomonitoring data on a representative sample of the U.S. population. The committee supports CDC’s efforts but argues for an expansion of the biomonitoring program and for procedural changes that would enhance the data’s utility. The committee recognizes that in some cases CDC may not be able to undertake such efforts but that other organizations may be more appropriate. The committee concludes that additional data are needed on some ethnic groups, specific locations, and the young (infants, toddlers, and preschoolers). CDC should report additional data in the printed version of the national exposure reports, such as results below the 50th percentile, and ensure that the publicly available database is sortable by sample type, chemical, location, and socioeconomic characteristics. Because of the scientific and cost-effective value of specimen banks for maintaining samples for future analyses, the committee concludes that there should be provisions for increased availability of previously collected and characterized samples. In addition, long-term funding for both existing and new biorepositories should be supported. Biomonitoring is conducted on an international level by numerous organizations, and there is much knowledge to be gained from understanding patterns of exposure worldwide. The committee encourages the global exchange of biomonitoring information and expertise, including sharing of data, study approaches, and tracking of trends. To that end, the committee encourages the development of such information exchanges between EPA and the Organisation for Economic Co-operation and Development (OECD). CONCLUSION Advances in biomonitoring have provided a potentially powerful new lens for examining public exposures to toxic chemicals. However, the full promise of this tool for improving the nation’s public health is still far from being realized. Unprecedented analytic sensitivity has brought new insights and new challenges. Population-based biomonitoring studies provide potentially valuable data for researchers, public-health officials, and the public for identifying human exposures, understanding trends, fostering public-health interventions, and validating environmental-health policies. However, the tool has underscored the critical need to address methodologic, ethical, and communication challenges. This report presents a roadmap for approaching those challenges. It provides an overview of the state of the science, a profile of international applications, and guidance for the design of biomonitoring studies. It also presents a systematic approach to interpreting the public-health implica-

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Human Biomonitoring for Environmental Chemicals tions of biomonitoring results and communicating findings to the public. In its final chapter, the committee presents a research agenda that incorporates an integrated approach for setting priorities among biomarkers for development; supports the epidemiologic, toxicologic, and exposure-assessment science required to interpret biomonitoring data; and fosters the ethical and communication research required to convey study results effectively.

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