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BREAST CANCER AND THE ENVIRONMENT A LIFE COURSE APPROACH Committee on Breast Cancer and the Environment: The Scientific Evidence, Research Methodology, and Future Directions Board on Health Care Services Board on Health Sciences Policy

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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 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 study was supported by a contract between the National Academy of Sciences and Susan G. Komen for the Cure®. 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. Library of Congress Cataloging-in-Publication Data Institute of Medicine (U.S.). Committee on Breast Cancer and the Environment: The Scientific Evidence, Research Methodology, and Future Directions. Breast cancer and the environment : a life course approach / Committee on Breast Cancer and the Environment: The Scientific Evidence, Research Methodology, and Future Directions, Board on Health Care Services, Board on Health Sciences Policy. p. ; cm. Includes bibliographical references. ISBN 978-0-309-22069-9 (pbk.) — ISBN 978-0-309-22070-5 (PDF) I. Title. [DNLM: 1. Breast Neoplasms—etiology. 2. Environmental Exposure—adverse effects. 3. Breast Neoplasms—prevention & control. 4. Risk Factors. WP 870] 362.19699’449—dc23 2012007110 Additional copies of this report are available 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. For more information about the Institute of Medicine, visit the IOM home page at: www. iom.edu. Copyright 2012 by the National Academy of Sciences. All rights reserved. Printed in the United States of America Cover credit: Illustration by Diana Ong/Getty Images. The serpent has been a symbol of long life, healing, and knowledge among almost all cultures and religions since the beginning of recorded history. The serpent adopted as a logotype by the Institute of Medicine is a relief carving from ancient Greece, now held by the Staatliche Museen in Berlin. Suggested citation: IOM (Institute of Medicine). 2012. Breast cancer and the environment: A life course approach. Washington, DC: The National Academies Press.

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“Knowing is not enough; we must apply. Willing is not enough; we must do.” — Goethe Advising the Nation. Improving Health.

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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 Acad- emy 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 engineer- ing programs aimed at meeting national needs, encourages education and research, and recognizes the superior achievements of engineers. Dr. Charles M. Vest is presi- dent 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 Insti- tute 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 Sci- ences 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. Charles M. Vest are chair and vice chair, respectively, of the National Research Council. www.national-academies.org

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COMMITTEE ON BREAST CANCER AND THE ENVIRONMENT: THE SCIENTIFIC EVIDENCE, RESEARCH METHODOLOGY, AND FUTURE DIRECTIONS IRVA HERTZ-PICCIOTTO (Chair), Professor and Chief, Division of Environmental and Occupational Health, University of California, Davis LUCILE ADAMS-CAMPBELL, Professor of Oncology, Associate Director, Minority Health and Health Disparities Research, Lombardi Comprehensive Cancer Center, Georgetown University Medical Center PEGGY DEVINE, Founder and President, Cancer Information and Support Network DAVID EATON, Associate Vice Provost for Research, and Professor and Director, Center for Ecogenetics and Environmental Health, University of Washington S. KATHARINE HAMMOND, Professor, Division of Environmental Health Sciences, School of Public Health, University of California, Berkeley KATHY J. HELZLSOUER, Director, The Prevention and Research Center, Mercy Medical Center ROBERT A. HIATT, Professor and Chair, Department of Epidemiology and Biostatistics, and Director, Population Sciences, Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco CHANITA HUGHES HALBERT, Associate Professor, Department of Psychiatry, University of Pennsylvania, and Director, Center for Community-Based Research and Health Disparities DAVID J. HUNTER, Dean for Academic Affairs and Vincent L. Gregory Professor in Cancer Prevention, Harvard School of Public Health BARNETT KRAMER, Editor-in-Chief, Journal of the National Cancer Institute, and Editor-in-Chief, National Cancer Institute Physician Data Query (PDQ) Screening and Prevention Editorial Board BRYAN M. LANGHOLZ, Professor, Division of Biostatistics, Department of Preventive Medicine, University of Southern California (resigned July 2011) PEGGY REYNOLDS, Senior Research Scientist, Cancer Prevention Institute of California JOYCE S. TSUJI, Principal Scientist, Center for Toxicology and Mechanistic Biology, Exponent CHERYL LYN WALKER, Welch Professor and Director, Institute of Biosciences and Technology, Texas A&M Health Science Center v

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LAUREN ZEISE, Chief, Reproductive and Cancer Hazard Assessment Branch, Office of Environmental Health Hazard Assessment, California Environmental Protection Agency Study Staff LOIS JOELLENBECK, Study Director JANE DURCH, Senior Program Officer SHARYL NASS, Senior Program Officer NIHARIKA SATHE, Research Assistant (from November 2010) CASSANDRA CACACE, Research Assistant (until December 2010) ASHLEY McWILLIAMS, Senior Program Assistant (until December 2010) PATRICK BURKE, Financial Associate ROGER HERDMAN, Director, Board on Health Care Services ANDREW POPE, Director, Board on Health Sciences Policy Commissioned Paper Authors REBECCA SMITH-BINDMAN, University of California, San Francisco School of Medicine LINDA DIX-COOPER, University of California, Berkeley vi

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Reviewers T his report has been reviewed in draft form by individuals chosen for their diverse perspectives and technical expertise, in accordance with procedures approved by the National Research Council’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 confiden- tial to protect the integrity of the deliberative process. We wish to thank the following individuals for their review of this report: Mary Helen Barcellos-Hoff, NYU Langone Medical Center Julia G. Brody, Silent Spring Institute Diana Chingos, USC Norris Comprehensive Cancer Center Kathryn Guyton, U.S. Environmental Protection Agency Leena Hilakivi-Clarke, Georgetown Lombardi Comprehensive Cancer Center William A. Knaus, The University of Virginia Health Sciences Center Ruth M. Parker, Emory University School of Medicine Lorenz Rhomberg, Gradient Stephen H. Safe, Texas A&M University Michael Thun, American Cancer Society vii

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viii REVIEWERS David M. Umbach, National Institute of Environmental Health Sciences, National Institutes of Health Sandy Walsh, California Breast Cancer Organizations Noel S. Weiss, University of Washington 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 David G. Hoel, Medi- cal University of South Carolina, and David A. Savitz, Brown University. Appointed by the National Research Council and the Institute of Medicine, 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.

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Acknowledgments T he committee is grateful for the contribution of participants at its three public meetings. The presentations and discussions at these meetings were valuable in informing the committee about relevant research findings, issues of interest in the research community, the per- spectives of advocacy organizations, and the concerns of individuals with breast cancer and their families. The agendas for these meetings appear in Appendix A. The committee was also ably assisted by Linda Dix-Cooper from the University of California, Berkeley, and Dr. Rebecca Smith-Bindman from the University of California, San Francisco, from whom the committee commissioned papers. The study was conducted with the generous support of Susan G. Komen for the Cure®. The Institute of Medicine staff worked closely with Dr. Amelie Ramirez, who is a member of the Susan G. Komen for the Cure Scientific Advisory Board and Director of the Institute for Health Promo- tion Research at the University of Texas Health Science Center at San Antonio. Dr. Ramirez was helpful and supportive as the committee’s point of contact with the Scientific Advisory Board, which originally requested this study. In addition, Kendall Bergman graciously assisted the staff in the administrative coordination with Komen for the Cure. The committee and project staff appreciate the work of copy edi- tor Laura Penny and gratefully acknowledge valuable assistance within the National Academies from Laura Harbold DeStefano, Greta Gorman, Diedtra Henderson, Jillian Laffrey, William McLeod, Janice Mehler, Abbey Meltzer, Michael Park, Christine Stencel, Vilija Teel, and Lauren Tobias. ix

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Contents ACRONYMS AND ABBREVIATIONS xix SUMMARY 1 1 INTRODUCTION 25 Study Charge and Committee Activities, 27 Approach to the Study, 28 Topics Beyond the Scope of the Study, 33 The Committee’s Report, 34 References, 34 2 BACKGROUND, DEFINITIONS, CONCEPTS 37 An Introduction to Breast Cancer, 37 Breast Cancer Incidence in the United States, 43 A Broad Perspective on the Environment, 52 Investigating Whether Environmental Factors Are Related to Breast Cancer, 54 Some Measures of Disease Risk, 62 Summary, 64 References, 64 3 WHAT WE HAVE LEARNED FROM CURRENT APPROACHES TO STUDYING ENVIRONMENTAL RISK FACTORS 73 Scope of the Review, 74 Discussion of Specific Environmental Factors, 80 xi

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Tables, Figures, and Boxes TABLES S-1 Summary of Committee Assessment of Opportunities for Actions by Women That May Reduce Risk of Breast Cancer, 12 4-1 Examples of Rat and Mouse Strains of Differing Sensitivity to Mammary Tumor Formation in Response to Carcinogenic Agents, 215 4-2 Lifetime Incidence of Breast Tumors in U.S. Men and Women and Overall Percentage of Control Animals That Developed Spontaneous Mammary Tumors in Recent Reports on National Toxicology Program Carcinogenesis Studies, 217 4-3 Theoretical Experimental Outcome from an Exposure That Induces an Increase in Absolute Risk of 6 Percentage Points, 221 4-4 Timing of Events in Mammary Development in Humans and Rodents, 222 6-1 Summary of Committee Assessment of Opportunities for Actions by Women That May Reduce Risk of Breast Cancer, 290 6-2 Absolute Risk, Expressed as a Percentage of Women at a Specified Age Expected to Be Diagnosed with Invasive Breast Cancer Within the Next 10 Years, 311 xv

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xvi TABLES, FIGURES, AND BOXES C-1 Compilation of Evidence Categories Used by Selected Organizations, 364 C-2 Supplemental Criteria Used by IARC and WCRF/AICR in Evaluation of Evidence, 382 D-1 Summary of Estimates of Population Attributable Risk for Risk Factors for Breast Cancer, 388 F-1 Selected Units of Ionizing Radiation, 413 F-2 Summary of U.S. Population’s Annual Exposure to Ionizing Radiation from Different Sources, 2006–2010, 419 F-3 Typical Effective Doses of Radiation for Common Conventional X-ray and CT Procedures, 423 F-4 Typical Annual Occupational Exposures to Radiation, 428 F-5 Estimated Number of Future Breast Cancers That Might Occur Related to a Single Year of Medical Radiation Exposure, 438 FIGURES 2-1 Age-specific incidence rates for invasive and in situ breast cancer among women in the United States, 2004–2008, 45 2-2 Age-adjusted incidence of invasive and in situ breast cancer in women, United States, 1975–2008, 46 2-3 Age-specific incidence rates for invasive and in situ breast cancer among white and black women in the United States, 2004–2008, 48 2-4 Multiple levels on which environmental exposures may act to influence breast cancer, 52 2-5 A schematic illustration of the potential for environmental exposures at various levels and times over the life course to influence the initiation and progression of breast cancer, 53 4-1 Overview of risk factors associated with breast cancer, 179 4-2 Illustration of an evidence-based complex-systems model of postmenopausal breast cancer causation, 180 4-3 Sources and amounts (g/yr) of dioxin-like compounds released in the United States in 1987, 1995, and 2000, 185 4-4 Estimated releases of perfluorooctane sulfonyl fluoride (POSF) from 1970 to 2012 and exponential temporal trends in biota, 186 4-5 Genetic variants associated with breast cancer arrayed on the basis of their frequency and their impact on breast cancer risk, 209 4-6 Development of the mammary gland in rats following in utero exposure to atrazine (ATR) and 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD), 226

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xvii TABLES, FIGURES, AND BOXES 5-1 Schematic representation of (a) the breast, showing lobules and ducts, (b) ductal carcinoma in situ (DCIS), and (c) invasive ductal cancer, 241 5-2 Breast cancer risk by pack-years of smoking before and after first childbirth among parous women, U.S. Radiologic Technologists Health Study, 1983–1998, 253 F-1 Energy spectrum of radiation, 410 F-2 Sample doses of and exposures to ionizing radiation, 411 F-3 Proportion of radiation from various sources, 1985 (left) and 2006 (right), 422 F-4 Median effective radiation dose (interquartile range, minimum, and maximum) for each type of CT study, 427 F-5 Estimated range in the lifetime attributable risk of cancer if a 20-year-old woman underwent one of several types of CT studies using observed radiation dose, 433 F-6 Projected number of future cancers (mean and 95% uncertainty limits) that could be related to CT scan use in the United States in 2007, according to cancer type, 437 BOXES S-1 Study Charge, 4 S-2 Environmental Factors Included in the Committee’s Evidence Review, 5 1-1 Study Charge, 28 2-1 Breast Cancer in Men, 38 2-2 Data on Breast Cancer, 44 3-1 Environmental Factors Included in the Committee’s Evidence Review, 81 5-1 Life Stages Representing Potential Windows of Susceptibility for Breast Carcinogenesis and Hypothesized Mechanisms of Carcinogenesis, 242 5-2 Nongenomic Estrogen Receptor Signaling by Environmental Estrogens, 259

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Acronyms and Abbreviations ACS American Cancer Society ADH alcohol dehydrogenase ADI acceptable daily intake AFFF aqueous fire fighting foams AFP alpha fetoprotein AhR aryl hydrocarbon receptor AHRQ Agency for Healthcare Research and Quality AICR American Institute for Cancer Research ALDH aldehyde dehydrogenase AMPK AMP-activated protein kinase AR attributable risk ASTDR Agency for Toxic Substances and Disease Registry ATH adipose tissue hypoxia BaP benzo[a]pyrene BBD benign breast disease BCAC Breast Cancer Association Consortium BMI body mass index BPA bisphenol A BPC3 Breast and Prostate Cancer Cohort Consortium CAR constitutive androstate receptor CDC Centers for Disease Control and Prevention CFR Code of Federal Regulations CGEMS Cancer Genetic Markers of Susceptibility project xix

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xx ACRONYMS AND ABBREVIATIONS CI confidence interval CISNET Cancer Intervention and Surveillance Modeling Network CT computed tomography CTS California Teachers Study CYP cytochrome P-450 DAG directed acyclic graphs DBP disinfection by-products DCIS ductal carcinoma in situ DDE dichlorodiphenyldichloroethylene DDT dichlorodiphenyltrichloroethane DEHP di(2-ethylhexyl) phthalate; also bis(2-ethylhexyl) phthalate DEP diethyl phthalate DES diethylstilbestrol DHEA dehydroepiandrosterone DINP diisononyl phthalate DMBA 7,12-dimethylbenz[a]anthracene DNA deoxyribonucleic acid DSHEA Dietary Supplement Health and Education Act ECA European Chemical Agency ECM extracellular matrix EDC endocrine disrupting compound EFSA European Food Safety Authority EGFR epidermal growth factor receptor ELF-EMF extremely low frequency electromagnetic field EPA Environmental Protection Agency ER estrogen receptor ER– estrogen receptor negative ER+ estrogen receptor positive ERE estrogen response element FAO Food and Agriculture Organization of the United Nations FDA Food and Drug Administration FSH follicle stimulating hormone GAO Government Accountability Office GST glutathione S-transferase GWAS genome-wide association studies HER human epidermal growth factor receptor HERS Heart and Estrogen/Progestin Replacement Study

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xxi ACRONYMS AND ABBREVIATIONS HHS Department of Health and Human Services HPA axis hypothalamic–pituitary–adrenal axis HPG axis hypothalamic–pituitary–gonadal axis HPV program High Production Volume Chemical program HR hazard ratio HT hormone therapy IARC International Agency for Research on Cancer IGF insulin-like growth factor IGFBP insulin-like growth factor binding protein IOM Institute of Medicine IPCS (WHO) International Program on Chemical Safety LH leutenizing hormone MAPK mitogen-activated protein kinase MBzP monobenzyl phthalate MCPP mono-(3-carboxylpropyl) phthalate MEP monoethyl phthalate MMTV mouse mammary tumor virus MNU N-methyl-N-nitrosourea; also N-nitroso-N-methylurea MPA medroxyprogesterone acetate MQSA Mammography Quality Standards Act MRFIT Multiple Risk Factor Intervention Trial mRNA messenger RNA NAS National Academy of Sciences NAT N-acetyltransferase NCI National Cancer Institute NHANES National Health and Nutrition Examination Survey NHS Nurses’ Health Study NIAAA National Institute on Alcohol Abuse and Alcoholism NIEHS National Institute of Environmental Health Sciences NIH National Institutes of Health NNH number needed to harm NNT number needed to treat NPCR National Program of Cancer Registries NRC National Research Council NTP National Toxicology Program OEHHA Office of Environmental Health Hazard Assessment OR odds ratio OSHA Occupational Safety and Health Administration

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xxii ACRONYMS AND ABBREVIATIONS OVX ovariectomized PAH polycyclic aromatic hydrocarbon PAR population attributable risk PBDE polybrominated diphenyl ether PCB polychlorinated biphenyl PDQ Physician Data Query PFOA perfluorooctanoic acid PFOS perfluorooctanesulfonic acid PI3K phosphoinositide 3-kinase PND postnatal day PPAR peroxisome proliferator-activated receptor ppm parts per million PR progesterone receptor PR– progesterone receptor negative PR+ progesterone receptor positive PSA prostate specific antigen REACH Registration, Evaluation, Authorisation and Restriction of Chemical Substances RNA ribonucleic acid ROC receiver operating characteristic ROS reactive oxygen species RR relative risk SEER Surveillance, Epidemiology, and End Results Program SERD selective estrogen receptor down-regulator SERM selective estrogen receptor modulator SHBG sex hormone binding globulin SNP single nucleotide polymorphism STAR Study of Tamoxifen and Raloxifene TCDD 2,3,7,8-tetrachlorodibenzo-p-dioxin TDLU terminal duct lobular unit TNBC triple negative breast cancer TNF tumor necrosis factor TSCA Toxic Substances Control Act USPSTF U.S. Preventive Services Task Force UV ultraviolet radiation VOC volatile organic compound

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xxiii ACRONYMS AND ABBREVIATIONS WCRF World Cancer Research Fund WECARE Women’s Environment, Cancer, and Radiation Epidemiology Study WHI Women’s Health Initiative WHO World Health Organization XOR xanthine oxidoreductase

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