FLUORIDE IN DRINKING WATER

A SCIENTIFIC REVIEW OF EPA’S STANDARDS

Committee on Fluoride in Drinking Water

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.
www.nap.edu



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Fluoride in Drinking Water: A Scientific Review of EPA’S Standards FLUORIDE IN DRINKING WATER A SCIENTIFIC REVIEW OF EPA’S STANDARDS Committee on Fluoride in Drinking Water 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. www.nap.edu

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Fluoride in Drinking Water: A Scientific Review of EPA’S Standards 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 Institute 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 No. 68-C-03-013 between the National Academy of Sciences and the U.S. Environmental Protection Agency. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the organizations or agencies that provided support for this project. International Standard Book Number 10 0-309-10128-X (Book) International Standard Book Number 13 978-0-309-10128-8 (Book) International Standard Book Number 10 0-309-65796-2 (PDF) International Standard Book Number 13 978-0-309-65796-9 (PDF) Library of Congress Control Number 2006933237 Additional copies of this report are available from The National Academies Press 500 Fifth Street, NW Box 285 Washington, DC 20055 800-624-6242 202-334-3313 (in the Washington metropolitan area) http://www.nap.edu Copyright 2006 by the National Academy of Sciences. All rights reserved. Printed in the United States of America

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Fluoride in Drinking Water: A Scientific Review of EPA’S Standards THE NATIONAL ACADEMIES Advisers to the Nation on Science, Engineering, and Medicine 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. Wm. A. Wulf 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 responsibility 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 National 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. Wm. A. Wulf are chair and vice chair, respectively, of the National Research Council. www.national-academies.org

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Fluoride in Drinking Water: A Scientific Review of EPA’S Standards COMMITTEE ON FLUORIDE IN DRINKING WATER Members JOHN DOULL (Chair), University of Kansas Medical Center, Kansas City KIM BOEKELHEIDE, Brown University, Providence, RI BARBARA G. FARISHIAN, Washington, DC ROBERT L. ISAACSON, Binghamton University, Binghamton, NY JUDITH B. KLOTZ, University of Medicine and Dentistry of New Jersey, Piscataway JAYANTH V. KUMAR, New York State Department of Health, Albany HARDY LIMEBACK, University of Toronto, Ontario, Canada CHARLES POOLE, University of North Carolina at Chapel Hill, Chapel Hill J. EDWARD PUZAS, University of Rochester, Rochester, NY NU-MAY RUBY REED, California Environmental Protection Agency, Sacramento KATHLEEN M. THIESSEN, SENES Oak Ridge, Inc., Oak Ridge, TN THOMAS F. WEBSTER, Boston University School of Public Health, Boston, MA Staff SUSAN N. J. MARTEL, Project Director CAY BUTLER, Editor TAMARA DAWSON, Senior Program Assistant Sponsor U.S. ENVIRONMENTAL PROTECTION AGENCY

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Fluoride in Drinking Water: A Scientific Review of EPA’S Standards COMMITTEE ON TOXICOLOGY Members WILLIAM E. HALPERIN (Chair), New Jersey Medical School, Newark LAWRENCE S. BETTS, Eastern Virginia Medical School, Norfolk EDWARD C. BISHOP, Parsons Corporation, Pasadena, CA JAMES V. BRUCKNER, University of Georgia, Athens GARY P. CARLSON, Purdue University, West Lafayette, IN MARION EHRICH, Virginia Tech, Blacksburg SIDNEY GREEN, Howard University, Washington, DC MERYL KAROL, University of Pittsburgh, Pittsburgh, PA JAMES MCDOUGAL, Wright State University School of Medicine, Dayton, OH ROGER MCINTOSH, Science Applications International Corporation, Baltimore, MD GERALD WOGAN, Massachusetts Institute of Technology, Cambridge Staff KULBIR S. BAKSHI, Program Director EILEEN N. ABT, Senior Program Officer for Risk Analysis ELLEN K. MANTUS, Senior Program Officer SUSAN N. J. MARTEL, Senior Program Officer AIDA NEEL, Program Associate TAMARA DAWSON, Senior Program Assistant RADIAH ROSE, Senior Editorial Assistant ALEXANDRA STUPPLE, Senior Editorial Assistant SAMMY BARDLEY, Librarian

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Fluoride in Drinking Water: A Scientific Review of EPA’S Standards BOARD ON ENVIRONMENTAL STUDIES AND TOXICOLOGY1 Members JONATHAN M. SAMET (Chair), Johns Hopkins University, Baltimore, MD RAMÓN ALVAREZ, Environmental Defense, Austin, TX JOHN M. BALBUS, Environmental Defense, Washington, DC THOMAS BURKE, Johns Hopkins University, Baltimore, MD DALLAS BURTRAW, Resources for the Future, Washington, DC JAMES S. BUS, Dow Chemical Company, Midland, MI COSTEL D. DENSON, University of Delaware, Newark E. DONALD ELLIOTT, Willkie Farr & Gallagher LLP, Washington, DC J. PAUL GILMAN, Oak Ridge National Laboratory, Oak Ridge, TN SHERRI W. GOODMAN, Center for Naval Analyses, Alexandria, VA JUDITH A. GRAHAM, American Chemistry Council, Arlington, VA DANIEL S. GREENBAUM, Health Effects Institute, Cambridge, MA WILLIAM P. HORN, Birch, Horton, Bittner and Cherot, Washington, DC ROBERT HUGGETT, Michigan State University (emeritus), East Lansing JAMES H. JOHNSON, JR., Howard University, Washington, DC JUDITH L. MEYER, University of Georgia, Athens PATRICK Y. O’BRIEN, ChevronTexaco Energy Technology Company, Richmond, CA DOROTHY E. PATTON, International Life Sciences Institute, Washington, DC STEWARD T.A. PICKETT, Institute of Ecosystem Studies, Millbrook, NY DANNY D. REIBLE, University of Texas, Austin JOSEPH V. RODRICKS, ENVIRON International Corporation, Arlington, VA ARMISTEAD G. RUSSELL, Georgia Institute of Technology, Atlanta LISA SPEER, Natural Resources Defense Council, New York, NY KIMBERLY M. THOMPSON, Massachusetts Institute of Technology, Cambridge MONICA G. TURNER, University of Wisconsin, Madison MARK J. UTELL, University of Rochester Medical Center, Rochester, NY CHRIS G. WHIPPLE, ENVIRON International Corporation, Emeryville, CA LAUREN ZEISE, California Environmental Protection Agency, Oakland Senior Staff JAMES J. REISA, Director DAVID J. POLICANSKY, Scholar RAYMOND A. WASSEL, Senior Program Officer for Environmental Sciences and Engineering 1 This study was planned, overseen, and supported by the Board on Environmental Studies and Toxicology.

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Fluoride in Drinking Water: A Scientific Review of EPA’S Standards KULBIR BAKSHI, Senior Program Officer for Toxicology EILEEN N. ABT, Senior Program Officer for Risk Analysis K. JOHN HOLMES, Senior Program Officer ELLEN K. MANTUS, Senior Program Officer SUSAN N.J. MARTEL, Senior Program Officer SUZANNE VAN DRUNICK, Senior Program Officer RUTH E. CROSSGROVE, Senior Editor

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Fluoride in Drinking Water: A Scientific Review of EPA’S Standards OTHER REPORTS OF THE BOARD ON ENVIRONMENTAL STUDIES AND TOXICOLOGY 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) Health Risks from Dioxin and Related Compounds: Evaluation of the EPA Reassessment (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 (4 volumes, 2000-2004) 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 (1999) Hormonally Active Agents in the Environment (1999) Research Priorities for Airborne Particulate Matter (4 volumes, 1998-2004) The National Research Council’s Committee on Toxicology: The First 50 Years (1997) Carcinogens and Anticarcinogens in the Human Diet (1996)

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Fluoride in Drinking Water: A Scientific Review of EPA’S Standards Upstream: Salmon and Society in the Pacific Northwest (1996) Science and the Endangered Species Act (1995) Wetlands: Characteristics and Boundaries (1995) Biologic Markers (5 volumes, 1989-1995) Review of EPA’s Environmental Monitoring and Assessment Program (3 volumes, 1994-1995) 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

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Fluoride in Drinking Water: A Scientific Review of EPA’S Standards OTHER REPORTS OF THE COMMITTEE ON TOXICOLOGY Review of the Department of Defense Research Program on Low-Level Exposures to Chemical Warfare Agents (2005) Emergency and Continuous Exposure Guidance Levels for Selected Submarine Contaminants, Volume 1 (2004) Spacecraft Water Exposure Guidelines for Selected Contaminants, Volume 1 (2004) Toxicologic Assessment of Jet-Propulsion Fuel 8 (2003) Review of Submarine Escape Action Levels for Selected Chemicals (2002) Standing Operating Procedures for Developing Acute Exposure Guideline Levels for Hazardous Chemicals (2001) Evaluating Chemical and Other Agent Exposures for Reproductive and Developmental Toxicity (2001) Acute Exposure Guideline Levels for Selected Airborne Contaminants, Volume 1 (2000), Volume 2 (2002), Volume 3 (2003), Volume 4 (2004) Review of the US Navy’s Human Health Risk Assessment of the Naval Air Facility at Atsugi, Japan (2000) Methods for Developing Spacecraft Water Exposure Guidelines (2000) Review of the U.S. Navy Environmental Health Center’s Health-Hazard Assessment Process (2000) Review of the U.S. Navy’s Exposure Standard for Manufactured Vitreous Fibers (2000) Re-Evaluation of Drinking-Water Guidelines for Diisopropyl Methylphosphonate (2000) Submarine Exposure Guidance Levels for Selected Hydrofluorocarbons: HFC-236fa, HFC-23, and HFC-404a (2000) Review of the U.S. Army’s Health Risk Assessments for Oral Exposure to Six Chemical-Warfare Agents (1999) Toxicity of Military Smokes and Obscurants, Volume 1(1997), Volume 2 (1999), Volume 3 (1999) Assessment of Exposure-Response Functions for Rocket-Emission Toxicants (1998) Toxicity of Alternatives to Chlorofluorocarbons: HFC-134a and HCFC-123 (1996) Permissible Exposure Levels for Selected Military Fuel Vapors (1996) Spacecraft Maximum Allowable Concentrations for Selected Airborne Contaminants, Volume 1 (1994), Volume 2 (1996), Volume 3 (1996), Volume 4 (2000)

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Fluoride in Drinking Water: A Scientific Review of EPA’S Standards Preface In 1986, the U.S. Environmental Protection Agency (EPA) established a maximum-contaminant-level goal (MCLG) of 4 milligrams per liter (mg/L) and a secondary maximum contaminant level (SMCL) of 2 mg/L for fluoride in drinking water. These exposure values are not recommendations for the artificial fluoridation of drinking water, but are guidelines for areas in the United States that are contaminated or have high concentrations of naturally occurring fluoride. The goal of the MCLG is to establish an exposure guideline to prevent adverse health effects in the general population, and the goal of the SMCL is to reduce the occurrence of adverse cosmetic consequences from exposure to fluoride. Both the MCLG and the SMCL are nonenforceable guidelines. The regulatory standard for drinking water is the maximum contaminant level (MCL), which is set as close to the MCLG as possible, with the use of the best technology available. For fluoride, the MCL is the same as the MCLG of 4 mg/L. In 1993, a previous committee of the National Research Council (NRC) reviewed the health effects of ingested fluoride and EPA’s MCL. It concluded that the MCL was an appropriate interim standard, but that further research was needed to fill data gaps on total exposures to fluoride and its toxicity. Because new research on fluoride is now available and because the Safe Drinking Water Act requires periodic reassessment of regulations for drinking water contaminants, EPA requested that the NRC evaluate the adequacy of its MCLG and SMCL for fluoride to protect public health. In response to EPA’s request, the NRC convened the Committee on Fluoride in Drinking Water, which prepared this report. The committee was charged to review toxicologic, epidemiologic, and clinical data on fluoride,

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Fluoride in Drinking Water: A Scientific Review of EPA’S Standards particularly data published since 1993, and exposure data on orally ingested fluoride from drinking water and other sources. Biographical information on the committee members is provided in Appendix A. This report presents the committee’s review of the scientific basis of EPA’s MCLG and SMCL for fluoride, and their adequacy for protecting children and others from adverse health effects. The committee considers the relative contribution of various sources of fluoride (e.g., drinking water, food, dental hygiene products) to total exposure, and identifies data gaps and makes recommendations for future research relevant to setting the MCLG and SMCL for fluoride. Addressing questions of economics, risk-benefit assessment, or water-treatment technology was not part of the committee’s charge. This report has been reviewed in draft form by individuals chosen for their diverse perspectives and technical expertise, in accordance with procedures approved by the NRC’s Report Review Committee. The purpose of this 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 for objectivity, evidence, and responsiveness to the study charge. The review comments and draft manuscript remain confidential to protect the integrity of the deliberative process. We wish to thank the following individuals for their review of this report: Kenneth Cantor, National Cancer Institute; Caswell Evans, Jr., University of Illinois at Chicago; Michael Gallo, University of Medicine and Dentistry of New Jersey; Mari Golub, California Environmental Protection Agency; Philippe Grandjean, University of Southern Denmark; David Hoel, Medical University of South Carolina; James Lamb, The Weinberg Group Inc.; Betty Olson, University of California at Irvine; Elizabeth Platz, Johns Hopkins Bloomberg School of Public Health; George Stookey, Indiana University School of Dentistry; Charles Turner, University of Indiana; Robert Utiger, Harvard Institute of Medicine; Gary Whitford, Medical College of Georgia; and Gerald Wogan, Massachusetts Institute of Technology. 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 this report was overseen by John C. Bailar, University of Chicago, and Gilbert S. Omenn, University of Michigan Medical School. Appointed by the NRC, they were responsible for making certain that an independent examination of this report was carried out in accordance with institutional procedures and that all review comments were carefully considered. Responsibility for the final content of this report rests entirely with the authoring committee and the institution. The committee gratefully acknowledges the individuals who made presentations to the committee at its public meetings. They include Paul Con-

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Fluoride in Drinking Water: A Scientific Review of EPA’S Standards nett, St. Lawrence University; Joyce Donohue, EPA; Steve Levy, University of Iowa; William Maas, Centers for Disease Control and Prevention; Edward Ohanian, EPA; Charles Turner, Indiana University; and Gary Whitford, University of Georgia. The committee also wishes to thank Thomas Burke, Johns Hopkins University; Michael Morris, University of Michigan; Bernard Wagner, Wagner and Associates; and Lauren Zeise, California Environmental Protection Agency, who served as consultants to the committee. The committee is grateful for the assistance of the NRC staff in preparing the report. It particularly wishes to acknowledge the outstanding staff support from project director Susan Martel. We are grateful for her persistence and patience in keeping us focused and moving ahead on the task and her expertise and skill in reconciling the differing viewpoints of committee members. Other staff members who contributed to this effort are James Reisa, director of the Board on Environmental Studies and Toxicology; Kulbir Bakshi, program director for the Committee on Toxicology; Cay Butler, editor; Mirsada Karalic-Loncarevic, research associate; Jennifer Saunders, research associate; and Tamara Dawson, senior project assistant. Finally, I would like to thank all the members of the committee for their efforts throughout the development of this report. John Doull, M.D., Ph.D., Chair Committee on Fluoride in Drinking Water

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Fluoride in Drinking Water: A Scientific Review of EPA’S Standards Contents     SUMMARY   1 1   Introduction   13      Fluoride in Drinking Water,   14      History of EPA’s Regulation of Fluoride,   16      Committee’s Task,   18      Committee’s Approach,   21      Structure of the Report,   22 2   MEASURES OF EXPOSURE TO FLUORIDE IN THE UNITED STATES   23      Sources of Fluoride Exposure,   24      Recent Estimates of Total Fluoride Exposure,   54      Total Exposure to Fluoride,   55      Summary of Exposure Assessment,   64      Biomarkers of Exposure, Effect, and Susceptibility,   69      Findings,   81      Recommendations,   87 3   PHARMACOKINETICS OF FLUORIDE   89      Overview of Fluoride Chemistry, Units, and Measurement,   89      Short Review of Fluoride Pharmacokinetics: Absorption, Distribution, and Elimination,   90      Pharmacokinetic Models,   92     Fluoride Concentrations in Human Bone Versus Water Concentration,   93

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Fluoride in Drinking Water: A Scientific Review of EPA’S Standards                Fluoride Concentrations in Bones after Clinical Studies,   96      Comparative Pharmacokinetics of Rats and Humans,   98      Organofluorine Compounds,   99      Factors Modifying Pharmacokinetics and Their Implications for Potentially Susceptible Populations,   99      Findings,   101      Research Recommendations,   101 4   EFFECTS OF FLUORIDE ON TEETH   103      Enamel Fluorosis,   103      Other Dental Effects,   126      Findings,   127      Recommendations,   130 5   MUSCULOSKELETAL EFFECTS   131      Chemistry of Fluoride As It Relates to Mineralizing Tissues,   131      Effect of Fluoride on Cell Function,   133      Effects of Fluoride on Human Skeletal Metabolism,   138      Effect of Fluoride on Chondrocyte Metabolism and Arthritis,   177      Findings,   178      Recommendations,   180 6   REPRODUCTIVE AND DEVELOPMENTAL EFFECTS OF FLUORIDE   181      Reproductive Effects,   181      Developmental Effects,   193      Findings,   204      Recommendations,   204 7   NEUROTOXICITY AND NEUROBEHAVIORAL EFFECTS   205      Human Studies,   205      Animal Studies,   214      Neurochemical Effects and Mechanisms,   218      Findings,   220      Recommendations,   222 8   EFFECTS ON THE ENDOCRINE SYSTEM   224      Thyroid Follicular Cells,   224      Thyroid Parafollicular Cells,   236      Parathyroid Glands,   238      Pineal Gland,   252      Other Endocrine Organs,   256      Summary,   260      Recommendations,   266

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Fluoride in Drinking Water: A Scientific Review of EPA’S Standards 9   EFFECTS ON THE GASTROINTESTINAL, RENAL, HEPATIC, AND IMMUNE SYSTEMS   268      GI System,   268      The Renal System,   280      Hepatic System,   292      Immune System,   293      Findings,   295      Recommendations,   302 10   GENOTOXICITY AND CARCINOGENICITY   304      Genotoxicity,   304      Carcinogenicity,   316      EPA Guidelines and Practice in Setting MCLGs Regarding Carcinogenicity,   334      Findings,   335      Recommendations,   338 11   DRINKING WATER STANDARDS FOR FLUORIDE   340      Current Methods for Setting Standards for Drinking Water,   340      New Risk Assessment Considerations,   342      Fluoride Standards,   345      Findings and Recommendations,   352     REFERENCES   354     APPENDIXES     A   Biographical Information on the Committee on Fluoride in Drinking Water,   411 B   Measures of Exposure to Fluoride in the United States: Supplementary Information,   416 C   Ecologic and Partially Ecologic Studies in Epidemiology,   439 D   Comparative Pharmacokinetics of Rats and Humans,   442 E   Detailed Information on Endocrine Studies of Fluoride,   447

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Fluoride in Drinking Water: A Scientific Review of EPA’S Standards FLUORIDE IN DRINKING WATER

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