Workshop Summary

The Human Microbiome,
Diet, and Health

Leslie Pray, Laura Pillsbury, and Emily Tomayko, Rapporteurs
Food Forum
Food and Nutrition Board

INSTITUTE OF MEDICINE
       OF THE NATIONAL ACADEMIES

THE NATIONAL ACADEMIES PRESS
Washington, D.C.
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Workshop Summary The Human Microbiome, Diet, and Health Leslie Pray, Laura Pillsbury, and Emily Tomayko, Rapporteurs Food Forum Food and Nutrition Board

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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 Govern- ing Board of the National Research Council, whose members are drawn from the councils of the National Academy of Sciences, the National Academy of Engineer- ing, and the Institute of Medicine. This study was supported by Contract Nos. AG-3A94-P-11-0081, FS-11-DC-01, and CNPP/IOM-11-01 (U.S. Department of Agriculture), N01-OD-4-2139 (­ ational N I ­ nstitutes of Health), and HHSF22301020T (Food and Drug Administration) with the National Academy of Sciences. Additional support came from Abbott Labo- ratories, Cargill, Coca-Cola Company, ConAgra Foods, General Mills, Kellogg Company, Kraft Foods, Mars, McDonald’s, Mead Johnson Nutrition, Monsanto, Nestlé Nutrition, and PepsiCo. The views expressed in this publication are those of the author(s) and do not necessarily reflect the views of the organizations or agencies that provided support for this project. International Standard Book Number-13:  978-0-309-26585-0 International Standard Book Number-10:  0-309-26585-1 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 2013 by the National Academy of Sciences. All rights reserved. Printed in the United States of America 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 a ­ dopted as a logotype by the Institute of Medicine is a relief carving from ancient Greece, now held by the Staatliche Museen in Berlin. Cover credit: Image designed by Casey Weeks. Suggested citation: IOM (Institute of Medicine). 2013. The human microbiome, diet, and health: Workshop summary. 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 en- gineers. 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 Coun- cil 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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PLANNING COMMITTEE ON THE HUMAN MICROBIOME, DIET, AND HEALTH1 GORDON L. JENSEN (Chair), Pennsylvania State University, University Park JENNIFER BRULC, General Mills, Inc., Minneapolis, Minnesota SUSAN CROCKETT, General Mills, Inc., Minneapolis, Minnesota CINDY DAVIS, National Institutes of Health, Bethesda, Maryland ERIC DECKER, University of Massachusetts Amherst MARGARET LEAHY, The Coca-Cola Company, Atlanta, Georgia SARAH ROLLER, Kelley Drye & Warren LLP, Washington, DC PAMELA STARKE-REED, National Institutes of Health, Bethesda, Maryland IOM Staff LAURA PILLSBURY, Study Director GERALDINE KENNEDO, Administrative Assistant LINDA D. MEYERS, Senior Director, Food and Nutrition Board 1  Institute of Medicine planning committees are solely responsible for organizing the work- shop, identifying topics, and choosing speakers. The responsibility for the published workshop summary rests with the workshop rapporteurs and the institution. v

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FOOD FORUM1 FRANK BUSTA (Chair), University of Minnesota, St. Paul MARK ANDON, ConAgra Foods, Inc., Omaha, Nebraska PAUL M. COATES, National Institutes of Health, Bethesda, Maryland DAVID B. COCKRAM, Abbott Laboratories, Columbus, Ohio SUSAN J. CROCKETT, General Mills, Minneapolis, Minnesota ERIC A. DECKER, University of Massachusetts Amherst CAROLINE SMITH DEWAAL, Center for Science in the Public Interest, Washington, DC SAMUEL GODEFROY, Health Canada, Ottawa, Ontario DAVID GOLDMAN, U.S. Department of Agriculture, Washington, DC CINDY GOODY, McDonald’s Corporation, Oak Brook, Illinois SONYA A. GRIER, American University, Washington, DC BRENDA HALBROOK, U.S. Department of Agriculture, Alexandria, Virginia JERRY HJELLE, Monsanto Company, St. Louis, Missouri KATE J. HOUSTON, Cargill Incorporated, Washington, DC VAN S. HUBBARD, National Institutes of Health, Bethesda, Maryland LEE-ANN JAYKUS, North Carolina State University, Raleigh GORDON L. JENSEN, Pennsylvania State University, University Park RENÉE S. JOHNSON, Congressional Research Service, Washington, DC WENDY L. JOHNSON-ASKEW, Nestlé Nutrition, Florham Park, New Jersey GENE KAHN, Bill & Melinda Gates Foundation, Seattle, Washington CAROL KELLAR, Kraft Foods, Glenview, Illinois MICHAEL M. LANDA, Food and Drug Administration, College Park, Maryland MARGARET LEAHY, The Coca-Cola Company, Atlanta, Georgia ERIK D. OLSON, Pew Health Group, Washington, DC ROBERT C. POST, U.S. Department of Agriculture, Alexandria, Virginia STEVEN W. RIZK, Mars Chocolate North America, Hackettstown, New Jersey SARAH ROLLER, Kelley Drye & Warren LLP, Washington, DC SYLVIA B. ROWE, SR Strategy, LLC, Washington, DC PETER VAN DAEL, Mead Johnson Nutrition, Evansville, Indiana PARKE E. WILDE, Tufts University, Boston, Massachusetts DEREK YACH, PepsiCo, Purchase, New York 1  Institute of Medicine forums and roundtables do not issue, review, or approve individual documents. The responsibility for the published workshop summary rests with the workshop rapporteurs and the institution. vi

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Food Forum Staff LAURA PILLSBURY, Director EMILY TOMAYKO, Mirzayan Science & Technology Policy Fellow (from August 2012) GERALDINE KENNEDO, Administrative Assistant ANTON L. BANDY, Financial Associate LINDA D. MEYERS, Senior Director, Food and Nutrition Board vii

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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 process. We wish to thank the following individuals for their review of this report: Cindy Davis, National Institutes of Health, Bethesda, Maryland Robert W. Hutkins, University of Nebraska, Lincoln Artem Khlebnikov, The Dannon Company, Inc., White Plains, New York David Mills, University of California, Davis Connie M. Weaver, Purdue University, West Lafayette, Indiana Although the reviewers listed above have provided many constructive comments and suggestions, they did not see the final draft of the report before its release. The review of this report was overseen by Melvin Worth. Appointed by the Institute of Medicine, he was 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 authors and the institution. ix

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Contents OVERVIEW 1 Studying the Microbiome, 3 The Microbiome, Health, and Disease, 5 How the Microbiome Influences Host Diet Metabolism, 6 How Diet Impacts the Microbiome, 7 Probiotics and Prebiotics, 8 Understanding Consumer Behavior and Regulatory Challenges, 11 Moving Forward, 13 References, 14 1 INTRODUCTION 23 Organization of This Report, 24 Keynote Address: The Future Impact of Beneficial Microbes and Gut Health, 25 Major Overarching Themes, 28 References, 31 2 STUDY OF THE HUMAN MICROBIOME 33 Defining the Human Microbiome, 33 Tools and Models for Assessment of the Microbiome, 40 Metabolome and Microbiome, 43 Open Discussion, 48 References, 50 xi

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xii CONTENTS 3 INTERACTION BETWEEN THE MICROBIOME AND HEALTH AND ENVIRONMENT 55 Overview of Pediatric Clinical Implications and Interventions, 55 Impact of Microbiome on Oral Health and Disease, 60 Impact of Microbiome on Gastrointestinal Health, 62 References, 67 4 INFLUENCE OF THE MICROBIOME ON THE METABOLISM OF DIET AND DIETARY COMPONENTS 69 Diet, Obesity, and the Gut Microbiome, 69 Microbial Metabolites of Dietary Components, 74 Biogeography of the GI Tract, 77 References, 78 5 INFLUENCE OF DIET AND DIETARY COMPONENTS ON THE MICROBIOME 81 Human Breast Milk, 81 Host-Microbe Interactions in the Perinatal Period, 83 The Resistome as a Driver of the Microbiome, 88 Probiotic Mechanisms of Action, 92 Prebiotic Mechanisms of Action, 96 Translation of Probiotic Science into Probiotic Foods, 100 Developing Delivery Systems, 105 How the Microbiome Revolution Fuels Functional Food Research, 109 Discussion, 112 References, 115 6 SOCIETAL AND POLICY IMPLICATIONS 121 How Americans Eat and Drink to Improve Health, 121 Consumer Insights from the Industry Perspective, 125 Probiotic and Prebiotic Health Claims in Europe: Scientific Assessment and Requirements, 129 Evaluation of Viable Microbes Using Regulatory Requirements Developed for Nonviable Ingredients, 132 Health Claims and False Advertising, 137 Regulatory Frameworks: The Industry Experience, 140 The Regulatory Environment: A Synthesis, 142 References, 145

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CONTENTS xiii 7 POSSIBILITIES FOR THE FUTURE 147 Moving the Science Forward: Studying Health Versus Disease, 148 Changing the Regulatory Framework for Food Claims, 149 The Microbiome, Environment, and Health: Future Research Needs, 151 Reference, 154 APPENDIXES A WORKSHOP AGENDA 155 B SPEAKER BIOGRAPHICAL SKETCHES 159 C WORKSHOP ATTENDEES 171 D ABBREVIATIONS AND ACRONYMS 179

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