Environmental Chemicals,
the Human Microbiome,
and Health Risk
— A RESEARCH STRATEGY —
Committee on Advancing Understanding of the Implications
of Environmental-Chemical Interactions with the Human Microbiome
Board on Environmental Studies and Toxicology
Board on Life Sciences
Division on Earth and Life Studies
A Consensus Study Report of
THE NATIONAL ACADEMIES PRESS
Washington, DC
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This project was supported by Contract EP-C-14-005, TO#0012 between the National Academies of Sciences, Engineering, and Medicine and the US Environmental Protection Agency, and Contract HHSN263201200074I, TO#HHSN26300097, US Department of Health and Human Services. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the authors and do not necessarily reflect the view of the organizations or agencies that provided support for this project.
International Standard Book Number-13: 978-0-309-46869-5
International Standard Book Number-10: 0-309-46869-8
Digital Object Identifier: https://doi.org/10.17226/24960
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Suggested citation: National Academies of Sciences, Engineering, and Medicine. 2018. Environmental Chemicals, the Human Microbiome, and Health Risk: A Research Strategy. Washington, DC: The National Academies Press. doi: https://doi.org/10.17226/24960.
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COMMITTEE ON ADVANCING UNDERSTANDING OF THE IMPLICATIONS OF ENVIRONMENTAL-CHEMICAL INTERACTIONS WITH THE HUMAN MICROBIOME
Members
RONALD M. ATLAS (Chair), University of Louisville, Louisville, KY
KJERSTI M. AAGAARD, Baylor College of Medicine, Houston, TX
ELAINE HSIAO, University of California, Los Angeles, CA
YVONNE HUANG, University of Michigan, Ann Arbor, MI
CURTIS HUTTENHOWER, Harvard University, Boston, MA
ROSA KRAJMALNIK-BROWN, Arizona State University, Tempe, AZ
SUSAN LYNCH, University of California, San Francisco, CA
WILLIAM W. NAZAROFF, University of California, Berkeley, CA
ANDREW D. PATTERSON, Pennsylvania State University, University Park, PA
JOHN F. RAWLS, Duke University School of Medicine, Durham, NC
JOSEPH V. RODRICKS, Ramboll Environ, Arlington, VA
PAMELA SHUBAT (Retired), Minnesota Department of Health, MN
BRIAN THRALL, Pacific Northwest National Laboratory, Richland, WA
Staff
ELLEN K. MANTUS, Project Director
ANDREA HODGSON, Associate Program Officer
MIRSADA KARALIC-LONCAREVIC, Manager, Technical Information Center
RADIAH ROSE-CRAWFORD, Manager, Editorial Projects
IVORY CLARKE, Research Assistant
Sponsors
US ENVIRONMENTAL PROTECTION AGENCY
NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES
BOARD ON ENVIRONMENTAL STUDIES AND TOXICOLOGY
Members
WILLIAM H. FARLAND (Chair), Colorado State University, Fort Collins, CO
RICHARD A. BECKER, American Chemistry Council, Washington, DC
E. WILLIAM COLGLAZIER, AAAS, Washington, DC
DOMINIC M. DITORO, University of Delaware, Newark, DE
DAVID C. DORMAN, North Carolina State University, Raleigh, NC
CHARLES T. DRISCOLL, JR., Syracuse University, Syracuse, NY
ANNE FAIRBROTHER, Exponent, Inc., Philomath, OR
GEORGE GRAY, The George Washington University, Washington, DC
STEVEN P. HAMBURG, Environmental Defense Fund, New York, NY
ROBERT A. HIATT, University of California, San Francisco, CA
SAMUEL KACEW, University of Ottawa, Ontario
H. SCOTT MATTHEWS, Carnegie Mellon University, Pittsburgh, PA
ROBERT PERCIASEPE, Center for Climate and Energy Solutions, Arlington, VA
R. CRAIG POSTLEWAITE, Department of Defense, Burke, VA
MARK A. RATNER, Northwestern University, Evanston, IL
JOAN B. ROSE, Michigan State University, East Lansing, MI
GINA M. SOLOMON, California Environmental Protection Agency, Sacramento, CA
ROBERT M. SUSSMAN, Sussman and Associates, Washington, DC
DEBORAH L. SWACKHAMER, University of Minnesota, St. Paul, MN
PETER S. THORNE, University of Iowa, Iowa City, IA
Senior Staff
TERESA A. FRYBERGER, Director
ELLEN K. MANTUS, Scholar and Director of Risk Assessment
RAYMOND A. WASSEL, Scholar and Director of Environmental Studies
SUSAN N.J. MARTEL, Senior Program Officer for Toxicology
ELIZABETH BOYLE, Program Officer
TAMARA DAWSON, Program Associate
BERNIDEAN WILLIAMS-SMITH, Financial Associate
SUZANNE THILENIUS, Administrative Coordinator
BOARD ON LIFE SCIENCES
Members
JAMES P. COLLINS (Chair), Arizona State University
A. ALONSO AGUIRRE, George Mason University
ENRIQUETA C. BOND, Burroughs Wellcome Fund
ROGER D. CONE, University of Michigan
NANCY D. CONNELL, Rutgers New Jersey Medical School
JOSEPH R. ECKER, Salk Institute for Biological Studies
SCOTT V. EDWARDS, Harvard University
SARAH C.R. ELGIN, Washington University, St. Louis
ROBERT J. FULL, University of California, Berkeley
ELIZABETH HEITMAN, Vanderbilt University Medical Center
JUDITH KIMBLE, University of Wisconsin–Madison
MARY E. MAXON, Lawrence Berkeley National Laboratory
JILL P. MESIROV, University of California, San Diego
KAREN E. NELSON, J. Craig Venter Institute
CLAIRE POMEROY, Albert and Mary Lasker Foundation
MARY E. POWER, University of California, Berkeley
LANA SKIRBOLL, Sanofi
JANIS WEEKS, University of Oregon
Senior Staff
FRANCES SHARPLES, Director
JO HUSBANDS, Senior Scholar
JAY LABOV, Senior Scholar
LIDA ANESTIDOU, Senior Program Officer
KATIE BOWMAN, Senior Program Officer
KEEGAN SAWYER, Senior Program Officer
AUDREY THEVENON, Program Officer
ANDREA HODGSON, Associate Program Officer
BETHELHEM MEKASHA, Financial Associate
JENNA OGILVIE, Research Associate
ANGELA KOLESNIKOVA, Senior Program Assistant
AANIKA SENN, Senior Program Assistant
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Acknowledgments
This Consensus Study Report was reviewed in draft form by individuals chosen for their diverse perspectives and technical expertise. The purpose of this independent review is to provide candid and critical comments that will assist the National Academies of Sciences, Engineering, and Medicine in making each published report as sound as possible and to ensure that it meets the institutional standards for quality, 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 thank the following individuals for their review of this report:
Gary Ginsberg, Connecticut Department of Public Health
Elizabeth Grice, University of Pennsylvania
Karen Guillemin, University of Oregon
Rob Knight, University of California, San Diego
Kun Lu, University of North Carolina, Chapel Hill
Linda McCauley, Emory University
M. Allen Northrup, MIODx
Howard Rosen, AcelRx Pharmaceuticals, Inc.
Joyce Tsuji, Exponent
Lauren Zeise, California Environmental Protection Agency
Although the reviewers listed above provided many constructive comments and suggestions, they were not asked to endorse the conclusions or recommendations of this report nor did they see the final draft before its release. The review of the report was overseen by Michael Ladisch, Purdue University, and Charles Haas, Drexel University, who were responsible for making certain that an independent examination of the report was carried out in accordance with institutional procedures and that all review comments were carefully considered. Responsibility for the final content rests entirely with the authoring committee and the National Academies.
The committee gratefully acknowledges the following for their presentations to the committee during open sessions: Tina Bahadori, US Environmental Protection Agency; Lisa Chadwick, National Institute of Environmental Health Sciences; Jay Garland, US Environmental Protection Agency; Elizabeth Grice, University of Pennsylvania; Kerry Kinney, University of Texas, Austin; Laura Kolb, US Environmental Protection Agency; Tamara Tal, US Environmental Protection Agency; Peter Turnbaugh, University of California, San Francisco; and Vincent Young, University of Michigan. The committee is also grateful for the assistance of Norman Grossblatt who served as the report editor.
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Contents
The Committee’s Approach to Its Task
Factors That Contribute to Variation in the Human Microbiome
Variation Between Human and Animal Microbiomes
3 CHARACTERIZING INTERACTIONS BETWEEN THE HUMAN MICROBIOME AND ENVIRONMENTAL CHEMICALS
Direct Effects of a Chemical on Microbiome Composition
Alterations in the Functions of Epithelial Barriers
Direct Chemical Transformations
Transformation of Host-Generated Metabolites
Alterations in Expression of Host-Tissue Metabolic Enzymes
Interindividual Variability and Microbiome Metabolism of Environmental Chemicals
4 CURRENT METHODS FOR STUDYING THE HUMAN MICROBIOME
Systems for Studying the Human Microbiome
Technologies for Assaying the Microbiome
Analyzing Microbiome Population and Exposure Data
5 RISK ASSESSMENT: INCORPORATING CHEMICAL–MICROBIOME INTERACTIONS
Data Sources and Requirements for Risk Assessment
Major Risk-Assessment Issues Related to Chemical–Microbiome Interactions
Research to Address Risk-Assessment Needs and Implications
Identifying Health Risk Assessments That Might Need Re-Evaluation
Selection of Chemicals for Experimental Approaches
Effects of Environmental Chemicals on the Human Microbiome
The Role of the Human Microbiome in Modulating Exposures to Environmental Chemicals
The Importance of Microbiome Variation and Variability
Opportunities for Collaboration and Coordination
BOXES AND FIGURES
BOXES
1-2 Definitions of Selected Terms
6-1 Physiologically Based Pharmacokinetic or Pharmacodynamic Models
6-2 Resources for Research Collaborations
FIGURES
S-1 Standard four-step framework for risk assessment
4-1 Culture-independent molecular approaches to study host–microbiome interactions