Potential Health Risks to DOD
FIRING-RANGE PERSONNEL
from Recurrent Lead Exposure

Committee on Potential Health Risks from Recurrent
Lead Exposure of DOD Firing Range Personnel

Committee on Toxicology

Board on Environmental Studies and Toxicology

Division on Earth and Life Studies

NATIONAL RESEARCH COUNCIL
OF THE NATIONAL ACADEMIES

THE NATIONAL ACADEMIES PRESS

Washington, D.C.

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Committee on Potential Health Risks from Recurrent Lead Exposure of DOD Firing Range Personnel Committee on Toxicology Board on Environmental Studies and Toxicology Division on Earth and Life Studies

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THE NATIONAL ACADEMIES PRESS 500 Fifth Street, NW Washington, DC 20001 NOTICE: The project that is the subject of this report was approved by the Governing Board of the National Research Council, whose members are drawn from the councils of the National Academy of Sciences, the National Academy of Engineering, and the Insti- tute of Medicine. The members of the committee responsible for the report were chosen for their special competences and with regard for appropriate balance. This project was supported by Contract W81K04-11-D-0017 between the National Acad- emy of Sciences and the Department of Defense. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author) and do not neces- sarily reflect the view of the organizations or agencies that provided support for this pro- ject. International Standard Book Number-13: 978-0-309-26736-6 International Standard Book Number-10: 0-309-26736-6 Additional copies of this report are available for sale from the National Academies Press, 500 Fifth Street, NW, Keck 360, Washington, DC 20001; (800) 624-6242 or (202) 334- 3313; http://www.nap.edu/. Copyright 2013 by the National Academy of Sciences. All rights reserved. Printed in the United States of America.

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The National Academy of Sciences is a private, nonprofit, self-perpetuating society of distinguished scholars engaged in scientific and engineering research, dedicated to the furtherance of science and technology and to their use for the general welfare. Upon the authority of the charter granted to it by the Congress in 1863, the Academy has a mandate that requires it to advise the federal government on scientific and technical matters. Dr. Ralph J. Cicerone is president of the National Academy of Sciences. The National Academy of Engineering was established in 1964, under the charter of the National Academy of Sciences, as a parallel organization of outstanding engineers. It is autonomous in its administration and in the selection of its members, sharing with the National Academy of Sciences the responsibility for advising the federal government. The National Academy of Engineering also sponsors engineering programs aimed at meeting national needs, encourages education and research, and recognizes the superior achievements of engineers. Dr. Charles M. Vest is president of the National Academy of Engineering. The Institute of Medicine was established in 1970 by the National Academy of Sciences to secure the services of eminent members of appropriate professions in the examination of policy matters pertaining to the health of the public. The Institute acts under the re- sponsibility given to the National Academy of Sciences by its congressional charter to be an adviser to the federal government and, upon its own initiative, to identify issues of medical care, research, and education. Dr. Harvey V. Fineberg is president of the Institute of Medicine. The National Research Council was organized by the National Academy of Sciences in 1916 to associate the broad community of science and technology with the Academy’s purposes of furthering knowledge and advising the federal government. Functioning in accordance with general policies determined by the Academy, the Council has become the principal operating agency of both the National Academy of Sciences and the Na- tional Academy of Engineering in providing services to the government, the public, and the scientific and engineering communities. The Council is administered jointly by both Academies and the Institute of Medicine. Dr. Ralph J. Cicerone and Dr. Charles M. Vest are chair and vice chair, respectively, of the National Research Council. www.national-academies.org

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COMMITTEE ON POTENTIAL HEALTH RISKS FROM RECURRENT LEAD EXPOSURE OF DOD FIRING RANGE PERSONNEL Members DAVID C. DORMAN (Chair), North Carolina State University, Raleigh, NC SUSAN H. BENOFF, Feinstein Institute for Medical Research (retired), Riverdale, NY EDWARD C. BISHOP, Parsons Government Services (retired), Council Bluffs, IA MARGIT L. BLEECKER, Center for Occupational and Environmental Neurology, Baltimore, MD LISA M. BROSSEAU, University of Minnesota School of Public Health, Minneapolis, MN ROSE H. GOLDMAN, Harvard Medical School and Harvard School of Public Health, Boston, MA JOSEPH H. GRAZIANO, Columbia University Mailman School of Public Health, New York, NY SHERYL A. MILZ, University of Toledo, Toledo, OH SUNG KYUN PARK, University of Michigan School of Public Health, Ann Arbor, MI MARK A. ROBERTS, Exponent, Chicago, IL BRISA N. SANCHEZ, University of Michigan, Ann Arbor, MI BRIAN S. SCHWARTZ, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD LAUREN ZEISE, California Environmental Protection Agency, Oakland, CA JUDITH T. ZELIKOFF, New York University School of Medical, Tuxedo, NY Staff SUSAN N.J. MARTEL, Project Director KERI STOEVER, Research Associate NORMAN GROSSBLATT, Senior Editor MIRSADA KARALIC-LONCAREVIC, Manager, Technical Information Center RADIAH ROSE, Manager, Editorial Projects TAMARA DAWSON, Program Associate Sponsor US Department of Defense v

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COMMITTEE ON TOXICOLOGY Members GARY P. CARLSON (Chair), Purdue University (retired), West Lafayette, IN LAWRENCE S. BETTS, Eastern Virginia Medical School, Norfolk DEEPAK K. BHALLA, Wayne State University, Detroit, MI DEBORAH A. CORY-SLECHTA, University of Rochester School of Medicine and Dentistry, Rochester, NY MARY E. DAVIS, West Virginia University, Morgantown DAVID C. DORMAN, North Carolina State University, Raleigh MARGARET M. MACDONELL, Argonne National Laboratory, Argonne, IL IVAN RUSYN, University of North Carolina, Chapel Hill, NC KENNETH R. STILL, Portland State University, Portland, OR JOYCE S. TSUJI, Exponent, Inc., Bellevue, WA Staff SUSAN N.J. MARTEL, Senior Program Officer for Toxicology MIRSADA KARALIC-LONCAREVIC, Manager, Technical Information Center RADIAH ROSE, Manager, Editorial Projects TAMARA DAWSON, Program Associate vi

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BOARD ON ENVIRONMENTAL STUDIES AND TOXICOLOGY Members ROGENE F. HENDERSON (Chair), Lovelace Respiratory Research Institute, Albuquerque, NM PRAVEEN AMAR, Clean Air Task Force, Boston, MA MICHAEL J. BRADLEY, M.J. Bradley & Associates, Concord, MA JONATHAN Z. CANNON, University of Virginia, Charlottesville GAIL CHARNLEY, HealthRisk Strategies, Washington, DC FRANK W. DAVIS, University of California, Santa Barbara CHARLES T. DRISCOLL, JR., Syracuse University, New York LYNN R. GOLDMAN, George Washington University, Washington, DC LINDA E. GREER, Natural Resources Defense Council, Washington, DC WILLIAM E. HALPERIN, University of Medicine and Dentistry of New Jersey, Newark STEVEN P. HAMBURG, Environmental Defense Fund, New York, NY ROBERT A. HIATT, University of California, San Francisco PHILIP K. HOPKE, Clarkson University, Potsdam, NY SAMUEL KACEW, University of Ottawa, Ontario H. SCOTT MATTHEWS, Carnegie Mellon University, Pittsburgh, PA THOMAS E. MCKONE, University of California, Berkeley TERRY L. MEDLEY, E.I. du Pont de Nemours & Company, Wilmington, DE JANA MILFORD, University of Colorado at Boulder, Boulder RICHARD L. POIROT, Vermont Department of Environmental Conservation, Waterbury MARK A. RATNER, Northwestern University, Evanston, IL KATHRYN G. SESSIONS, Health and Environmental Funders Network, Bethesda, MD JOYCE S. TSUJI, Exponent Environmental Group, Bellevue, WA Senior Staff JAMES J. REISA, Director DAVID J. POLICANSKY, Scholar RAYMOND A. WASSEL, Senior Program Officer for Environmental Studies ELLEN K. MANTUS, Senior Program Officer for Risk Analysis SUSAN N.J. MARTEL, Senior Program Officer for Toxicology EILEEN N. ABT, Senior Program Officer MIRSADA KARALIC-LONCAREVIC, Manager, Technical Information Center RADIAH ROSE, Manager, Editorial Projects vii

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OTHER REPORTS OF THE BOARD ON ENVIRONMENTAL STUDIES AND TOXICOLOGY Science for Environmental Protection: The Road Ahead (2012) Exposure Science in the 21st Century: A Vision and A Strategy (2012) A Research Strategy for Environmental, Health, and Safety Aspects of Engineered Nanomaterials (2012) Macondo Well–Deepwater Horizon Blowout: Lessons for Improving Offshore Drilling Safety (2012) Feasibility of Using Mycoherbicides for Controlling Illicit Drug Crops (2011) Improving Health in the United States: The Role of Health Impact Assessment (2011) A Risk-Characterization Framework for Decision-Making at the Food and Drug Administration (2011) Review of the Environmental Protection Agency’s Draft IRIS Assessment of Formaldehyde (2011) Toxicity-Pathway-Based Risk Assessment: Preparing for Paradigm Change (2010) The Use of Title 42 Authority at the U.S. Environmental Protection Agency (2010) Review of the Environmental Protection Agency’s Draft IRIS Assessment of Tetrachloroethylene (2010) Hidden Costs of Energy: Unpriced Consequences of Energy Production and Use (2009) Contaminated Water Supplies at Camp Lejeune—Assessing Potential Health Effects (2009) Review of the Federal Strategy for Nanotechnology-Related Environmental, Health, and Safety Research (2009) Science and Decisions: Advancing Risk Assessment (2009) Phthalates and Cumulative Risk Assessment: The Tasks Ahead (2008) Estimating Mortality Risk Reduction and Economic Benefits from Controlling Ozone Air Pollution (2008) Respiratory Diseases Research at NIOSH (2008) Evaluating Research Efficiency in the U.S. Environmental Protection Agency (2008) Hydrology, Ecology, and Fishes of the Klamath River Basin (2008) Applications of Toxicogenomic Technologies to Predictive Toxicology and Risk Assessment (2007) Models in Environmental Regulatory Decision Making (2007) Toxicity Testing in the Twenty-first Century: A Vision and a Strategy (2007) Sediment Dredging at Superfund Megasites: Assessing the Effectiveness (2007) Environmental Impacts of Wind-Energy Projects (2007) Scientific Review of the Proposed Risk Assessment Bulletin from the Office of Management and Budget (2007) Assessing the Human Health Risks of Trichloroethylene: Key Scientific Issues (2006) New Source Review for Stationary Sources of Air Pollution (2006) Human Biomonitoring for Environmental Chemicals (2006) viii

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Health Risks from Dioxin and Related Compounds: Evaluation of the EPA Reassessment (2006) Fluoride in Drinking Water: A Scientific Review of EPA’s Standards (2006) State and Federal Standards for Mobile-Source Emissions (2006) Superfund and Mining Megasites—Lessons from the Coeur d’Alene River Basin (2005) Health Implications of Perchlorate Ingestion (2005) Air Quality Management in the United States (2004) Endangered and Threatened Species of the Platte River (2004) Atlantic Salmon in Maine (2004) Endangered and Threatened Fishes in the Klamath River Basin (2004) Cumulative Environmental Effects of Alaska North Slope Oil and Gas Development (2003) Estimating the Public Health Benefits of Proposed Air Pollution Regulations (2002) Biosolids Applied to Land: Advancing Standards and Practices (2002) The Airliner Cabin Environment and Health of Passengers and Crew (2002) Arsenic in Drinking Water: 2001 Update (2001) Evaluating Vehicle Emissions Inspection and Maintenance Programs (2001) Compensating for Wetland Losses Under the Clean Water Act (2001) A Risk-Management Strategy for PCB-Contaminated Sediments (2001) Acute Exposure Guideline Levels for Selected Airborne Chemicals (thirteen volumes, 2000-2012) Toxicological Effects of Methylmercury (2000) Strengthening Science at the U.S. Environmental Protection Agency (2000) Scientific Frontiers in Developmental Toxicology and Risk Assessment (2000) Ecological Indicators for the Nation (2000) Waste Incineration and Public Health (2000) Hormonally Active Agents in the Environment (1999) Research Priorities for Airborne Particulate Matter (four volumes, 1998-2004) The National Research Council’s Committee on Toxicology: The First 50 Years (1997) Carcinogens and Anticarcinogens in the Human Diet (1996) Upstream: Salmon and Society in the Pacific Northwest (1996) Science and the Endangered Species Act (1995) Wetlands: Characteristics and Boundaries (1995) Biologic Markers (five volumes, 1989-1995) Science and Judgment in Risk Assessment (1994) Pesticides in the Diets of Infants and Children (1993) Dolphins and the Tuna Industry (1992) Science and the National Parks (1992) Human Exposure Assessment for Airborne Pollutants (1991) Rethinking the Ozone Problem in Urban and Regional Air Pollution (1991) Decline of the Sea Turtles (1990) Copies of these reports may be ordered from the National Academies Press (800) 624-6242 or (202) 334-3313 www.nap.edu ix

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Preface Lead poses an occupational health hazard, and the Occupational Safety and Health Administration (OSHA) developed a lead standard in 1978 for gen- eral industry that regulates many workplace exposures to this metal, including exposures on firing ranges. A large body of literature on health effects of lead exposure and factors that influence lead toxicity has been published since the lead standard was established. Most recently, the National Toxicology Program released a monograph on the health effects of low-level lead exposure, and the US Environmental Protection Agency is in the process of updating its Integrated Science Assessment for Lead in support of its review of the National Ambient Air Quality Criteria for lead. In light of improved knowledge about the hazards posed by occupational lead exposure, the Department of Defense (DOD) asked the National Research Council to evaluate potential health risks related to recurrent lead exposure of firing-range personnel. Specifically, DOD asked the National Research Council to determine whether current exposure standards for lead on DOD firing ranges protect their workers adequately and to evaluate potential risk-assessment op- tions. In response to DOD’s request, the National Research Council convened the Committee on Potential Health Risks from Recurrent Lead Exposure of DOD Firing Range Personnel, which prepared this report. The members of the committee were selected for their expertise in general toxicology, inhalation toxicology, neurotoxicology, reproductive and developmental toxicology, im- munotoxicology, toxicokinetics, epidemiology, industrial hygiene, occupational medicine, exposure assessment, risk assessment, and biostatistics (see Appendix A for biographic information on the members). This report has been reviewed in draft form by persons chosen for their diverse perspectives and technical expertise in accordance with procedures ap- proved by the National Research Council’s Report Review Committee. The pur- pose of the independent review is to provide candid and critical comments that will assist the institution in making its published report as sound as possible and to ensure that the report meets institutional standards of objectivity, evidence, and responsiveness to the study charge. The review comments and draft manu- xi

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xii Preface script remain confidential to protect the integrity of the deliberative process. We thank the following for their review of this report: Floyd Bloom, The Scripps Research Institute; Deborah Cory-Slechta, University of Rochester; William Halperin, University of Medicine and Dentistry of New Jersey; David Lawrence, The Wadsworth Center; William J. Moorman, National Institute for Occupa- tional Safety and Health (retired); Rosemary Sokas, Georgetown University; Kenneth Still, Portland State University; and Rochelle Tyl, RTI International. Although the reviewers listed above have provided many constructive comments and suggestions, they were not asked to endorse the conclusions or recommendations, nor did they see the final draft of the report before its release. The review of the report was overseen by Robert Goyer, University of Western Ontario (retired), and Linda McCauley, Emory University. Appointed by the National Research Council, they were responsible for making certain that an independent examination of the report was carried out in accordance with insti- tutional procedures and that all review comments were carefully considered. Responsibility for the final content of the report rests entirely with the author committee and the institution. The committee is grateful for the assistance of National Research Council staff in preparing the report. It particularly wishes to acknowledge the support of project director Susan Martel, who coordinated the project and contributed to the committee’s report. Other staff members who contributed to this effort are James Reisa, director of the Board on Environmental Studies and Toxicology; Keri Stoever, research assistant; Tamara Dawson, program associate; Norman Grossblatt, senior editor; and Mirsada Karalic-Loncarevic, manager of the Technical Information Center. Finally, I thank all the members of the committee for their efforts throughout the development of this report. David C. Dorman, DVM, PhD, Chair Committee on Potential Health Risks from Recurrent Lead Exposure of DoD Firing Range Personnel

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Abbreviations ACGIH® American Conference of Governmental Industrial Hygienists ACOEM American College of Occupational and Environmental Medicine AIHA® American Industrial Hygiene Association ALA aminolevulinic acid ALAD delta-aminolevulinic acid dehydratase ALAU aminolevulinic acid level in urine AOEC Association of Occupational and Environmental Clinics AQCD air quality criteria document BAT biological tolerance values (German) BAEP brainstem auditory evoked potential BEI® biological exposure index BLL blood lead level CaNa2EDTA calcium disodium ethylenediamine tetraacetic acid CBLI cumulative blood lead index CD cluster of differentiation CDC Centers for Disease Control and Prevention CES-D Center for Epidemiological Studies – Depression Scale CI confidence interval CKD chronic kidney disease CPA Center for Policy Alternatives (at the Massachusetts Institute of Technology) CPT current perception threshold CSTE Council of State and Territorial Epidemiologists CTL cytotoxic T lymphocyte CVD cardiovascular disease DBP diastolic blood pressure DMSA 2,3-dimercaptosuccinic acid ECG electrocardiogram EEG electroencephalogram EPO erythropoietin FEP free erythrocyte protoporphyrin xiii

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xiv Abbreviations GFR glomerular filtration rate HFE human hemochromatosis protein HR hazard ratio HSE Health and Safety Executive Ig immunoglobulin (also called an antibody) IgA immunoglobulin A IgD immunoglobulin D IgE immunoglobulin E IgG immunoglobulin G IgM immunoglobulin M IFNγ interferon gamma IL-10 interleukin-10 cytokine (released from TH-2 cells) MCV mean corpuscular volume MCH mean corpuscular hemoglobin MMSE Mini-mental State Examination MRI magnetic resonance imaging MRS magnetic resonance spectroscopy NAG N-acetyl-beta-D-glucosaminidase NF-κB nuclear factor κB NHANES National Health and Nutrition Examination Survey NIOSH National Institute for Occupational Safety and Health NK-CD56+ natural killer cells NTP National Toxicology Program NIEHS National Institute of Environmental Health Sciences OR odds ratio OSHA Occupational Safety and Health Administration PBPK physiologically based pharmacokinetic PEL permissible exposure limit PKC protein kinase C PNS peripheral nervous system POMS Profile of Mood State ROS reactive oxygen species SBP systolic blood pressure SCOEL Scientific Committee on Occupational Exposure Limits (European Union) SD standard deviation SE standard error SMR standardized mortality ratio SRT simple reaction time SWHS Swedish Women’s Health Study TH T-helper lymphocyte TH1 T-helper 1 lymphocyte TH2 T-helper 2 lymphocyte TLV® threshold limit value TNF-α tumor necrosis factor α (TH-1 pro-inflammatory cytokine)

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Abbreviations xv TWA time-weighted average VEP visual evoked potential WMC white matter change XRF x-ray fluorescence ZPP zinc protoporphyrin

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Contents SUMMARY ........................................................................................................ 3 1 INTRODUCTION ............................................................................... 8 The Committee’s Task, 9 Approach to the Study, 10 Firing-Range Environments, 11 Department of Defense Firing-Range Personnel, 13 Lead Exposure on Department of Defense Firing Ranges, 15 Organization of the Report, 17 References, 26 2 OCCUPATIONAL STANDARDS AND GUIDELINES FOR LEAD............................................................... 29 US Standards and Guidelines, 29 Guidelines of Other Countries, 38 Exposure-Assessment Methods, 41 Additional Considerations, 43 References, 44 3 TOXICOKINETICS OF LEAD ....................................................... 47 How Exposure Becomes Dose, 47 Toxicokinetic Considerations, 48 Measuring Internal Lead Dose, 50 Dose-Response Considerations, 51 Pharmacokinetic Models for Lead, 53 Lead Dose and Health, 56 References, 57 4 NONCANCER HEALTH EFFECTS .............................................. 62 Environmental Protection Agency and National Toxicology Program Assessments, 62 Neurologic Effects, 63 xvii

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xviii Contents Hematopoietic Effects, 86 Renal Effects, 91 Reproductive and Developmental Effects, 99 Immunologic Effects, 109 Cardiovascular Effects, 119 References, 130 5 CANCER EFFECTS ....................................................................... 147 Conclusions from the 2006 International Agency for Research on Cancer, 2011 National Toxicology Program, and 2012 Environmental Protection Agency Reports, 148 Other Studies Considered, 149 Summary Findings, 159 References, 159 6 CONCLUSIONS .............................................................................. 164 Are Occupational Safety and Health Guidelines for Blood Lead Levels Adequate to Protect Department of Defense Firing-Range Personnel?, 165 Is the Current Occupational Safety and Health Administration Permissible Exposure Limit Adequately Protective of Department of Defense Firing-Range Personnel?, 168 Is the Current Occupational Safety and Health Administration Action Level for Medical Surveillance Appropriate?, 168 Were Data Gaps Identified in Answering the Questions Above? Is Research Needed to Fill Those Gaps?, 169 Potential Risk-Assessment Options, 169 Additional Considerations, 170 References, 171 APPENDIX BIOGRAPHIC INFORMATION ON THE COMMITTEE ON POTENTIAL HEALTH RISKS FROM RECURRENT LEAD EXPOSURE OF DOD FIRING RANGE PERSONNEL............................ 174 FIGURES AND TABLES FIGURES 3-1 Compartmental model for lead (modified from O’Flaherty 1993), 49 3-2 Schematic of a hypothetical worker’s dose over time, 52

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Contents xix 3-3 Time-dependent relationship between BLL and air lead concentration as estimated with the CPA model used by OSHA to develop the permissible exposure level, 55 4-1 The biosynthetic pathway of heme, 89 TABLES 1-1 Airborne Lead Concentration During Performance of Different Job Duties on US Army Weapons and Small-Arms Firing Ranges, 18 1-2 Airborne Lead Concentration (μg/m3) During Performance of Different Job Duties on US Navy Weapons and Small-arms Firing Ranges, 21 1-3 Lead Exposure on US Air Force Firing Ranges (2007-2012)—Air Lead Concentrations on Weapons and Small-Arms Firing Ranges and Blood Lead Levels of Combat-Arms Training and Maintenance Instructors, 22 1-4 Air and Blood Lead Concentrations Measured on Indoor and Outdoor Firing Ranges, 23 2-1 Occupational-Exposure Guidelines for Lead, 30 3-1 Assumptions Used by Occupational Safety and Health Administration for Center for Policy Alternatives Model and Committee’s Evaluation, 54 4-1 Key Studies of the Effects of Lead on Neurologic Outcomes, 77 4-2 Key Studies of the Hematopoietic Effects of Lead, 92 4-3 Key Studies of the Renal Effects of Lead, 100 4-4 Key Studies of the Male Reproductive Effects of Lead, 110 4-5 Key Studies of the Female Reproductive Effects of Lead, 111 4-6 Key Studies of the Immunologic Effects of Lead, 120 4-7 Key Studies of the Effects of Lead on Cardiovascular Disease, 128 5-1 Key Human Studies of the Carcinogenic Effects of Lead, 150 5-2 Dose-Response Data on Renal Tumors from Some Oral Studies in Rodents, 157

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