DRI DIETARY REFERENCE INTAKES FOR Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride

Standing Committee on the Scientific Evaluation of Dietary Reference Intakes

Food and Nutrition Board

Institute of Medicine

NATIONAL ACADEMY PRESS
Washington, D.C.



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DRI DIETARY REFERENCE INTAKES FOR Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride DRI DIETARY REFERENCE INTAKES FOR Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride Standing Committee on the Scientific Evaluation of Dietary Reference Intakes Food and Nutrition Board Institute of Medicine NATIONAL ACADEMY PRESS Washington, D.C.

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DRI DIETARY REFERENCE INTAKES FOR Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride NATIONAL ACADEMY PRESS 2101 Constitution Avenue, N.W. Washington, DC 20418 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 report has been reviewed by a group other than the authors according to procedures approved by a Report Review Committee consisting of members of the National Academy of Sciences, the National Academy of Engineering, and the Institute of Medicine. The Institute of Medicine was established in 1970 by the National Academy of Sciences to enlist distinguished members of the appropriate professions in the examination of policy matters pertaining to the health of the public. In this, the Institute acts under both the Academy's 1863 congressional charter responsibility to be an adviser to the federal government and its own initiative in identifying issues of medical care, research, and education. Dr. Kenneth I. Shine is president of the Institute of Medicine. This project was funded by the U.S. Department of Agriculture (Grant No. 59-0700-6-061), the National Institutes of Health (Grant No. N01-OD-4-2139, TO 19), the Food and Drug Administration (Grant No. 223-90-2223), and with assistance from Health Canada. The opinions or conclusions expressed herein do not necessarily reflect those of the funders. Library of Congress Cataloging-in-Publication Data Dietary reference intakes for calcium, phosphorus, magnesium, vitamin D, and fluoride / Standing Committee on the Scientific Evaluation of Dietary Reference Intakes, Food and Nutrition Board, Institute of Medicine. p. cm. Includes bibliographical references and index. ISBN 0-309-06350-7 (cloth). — ISBN 0-309-06403-1 (pbk.) 1. Diet. 2. Nutrition. I. Institute of Medicine (U.S.). Standing Committee on the Scientific Evaluation of Dietary Reference Intakes. TX551.D466 1997 613.2′85—dc21 97-33777 Additional copies of this report are available from the National Academy Press , 2101 Constitution Avenue, NW, Lock Box 285, Washington, DC 20055. Call (800) 624-6242 or (202) 334-3313 (in the Washington Metropolitan Area). Order electronically via Internet at http://www.nap.edu. For more information about the Institute of Medicine, visit the IOM home page at http://www.nap.edu/iom. Copyright 1997 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 image adopted as a logotype by the Institute of Medicine is based on a relief carving from ancient Greece, now held by the Staatliche Museen in Berlin.

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DRI DIETARY REFERENCE INTAKES FOR Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride STANDING COMMITTEE ON THE SCIENTIFIC EVALUATION OF DIETARY REFERENCE INTAKES VERNON R. YOUNG (Chair), * † Laboratory of Human Nutrition, School of Science, Massachusetts Institute of Technology, Cambridge JOHN W. ERDMAN, JR. (Vice Chair), Division of Nutritional Sciences, College of Agricultural, Consumer and Environmental Sciences, University of Illinois, Urbana-Champaign JANET C. KING (Vice-Chair), * U.S. Department of Agriculture Western Human Nutrition Research Center, Presidio of San Francisco LINDSAY H. ALLEN, Department of Nutrition, University of California, Davis STEPHANIE A. ATKINSON, Department of Pediatrics, Faculty of Health Sciences, McMaster University, Hamilton, Canada JOHANNA T. DWYER, Frances Stern Nutrition Center, New England Medical Center and Tufts University, Boston, Massachusetts JOHN D. FERNSTROM, University of Pittsburgh School of Medicine, Western Psychiatric Institute and Clinic, Pittsburgh, Pennsylvania SCOTT M. GRUNDY, * Center for Human Nutrition, University of Texas Southwestern Medical Center, Dallas CHARLES H. HENNEKENS, Division of Preventive Medicine, Brigham and Women's Hospital, Boston, Massachusetts SANFORD A. MILLER, Graduate School of Biomedical Sciences, University of Texas Health Science Center, San Antonio U.S. Government Liaison LINDA MEYERS, Office of Disease Prevention and Health Promotion, U.S. Department of Health and Human Services, Washington, D.C. Canadian Government Liaison PETER W.F. FISCHER, Nutrition Research Division, Health Protection Branch, Health Canada, Ottawa, Canada Staff ALLISON A. YATES, Study Director CAROL W. SUITOR, Senior Program Officer, Study Director (April 1997–July 1997) SANDRA A. SCHLICKER, Senior Program Officer SHEILA A. MOATS, Research Associate (April 1996–November 1996) *   Member, Institute of Medicine. †   Member, National Academy of Sciences.

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DRI DIETARY REFERENCE INTAKES FOR Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride ELISABETH A. REESE, Research Associate KIMBERLY A. BREWER, Research Assistant ALICE L. KULIK, Research Assistant DONNA M. LIVINGSTON, Project Assistant (April 1996–January 1997) GERALDINE KENNEDO, Project Assistant GAIL E. SPEARS, Administrative Assistant

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DRI DIETARY REFERENCE INTAKES FOR Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride PANEL ON CALCIUM AND RELATED NUTRIENTS STEPHANIE A. ATKINSON (Chair), Department of Pediatrics, Faculty of Health Sciences, McMaster University, Hamilton, Canada STEVEN A. ABRAMS, Department of Pediatrics, Baylor College of Medicine, USDA Children 's Nutrition Research Center, Houston, Texas BESS DAWSON-HUGHES, Calcium and Bone Metabolism Laboratory, Jean Mayer USDA Human Nutrition Research Center on Aging, Tufts University, Boston, Massachusetts ROBERT P. HEANEY, John A. Creighton University Professor, Creighton University, Omaha, Nebraska MICHAEL F. HOLICK, Endocrinology, Nutrition and Diabetes Section and Vitamin D, Skin, and Bone Research Laboratory, Boston University School of Medicine and Boston Medical Center, Boston, Massachusetts SUZANNE P. MURPHY, Department of Nutritional Sciences, University of California, Berkeley ROBERT K. RUDE, Department of Medicine, University of Southern California, Los Angeles BONNY L. SPECKER, Department of Pediatrics, University of Cincinnati and Children's Hospital Medical Center, Ohio CONNIE M. WEAVER, Department of Food and Nutrition, Purdue University, West Lafayette, Indiana GARY M. WHITFORD, Department of Oral Biology and Physiology, School of Dentistry, Medical College of Georgia, Augusta Staff SANDRA A. SCHLICKER, Study Director SHEILA A. MOATS, Research Associate (April 1996–November 1996) ELISABETH A. REESE, Research Associate KIMBERLY A. BREWER, Research Assistant ALICE L. KULIK, Research Assistant DONNA M. LIVINGSTON, Project Assistant (April 1996–January 1997) GERALDINE KENNEDO, Project Assistant GAIL E. SPEARS, Administrative Assistant

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DRI DIETARY REFERENCE INTAKES FOR Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride SUBCOMMITTEE ON UPPER REFERENCE LEVELS OF NUTRIENTS IAN C. MUNRO (Chair), CanTox, Incorporated, Mississauga, Canada STEVEN A. ABRAMS, Baylor College of Medicine, USDA Children's Nutrition Research Center, Houston, Texas ROBERT P. HEANEY, John A. Creighton University Professor, Creighton University, Omaha, Nebraska WALTER MERTZ, Retired, Human Nutrition Research Center, Rockville, Maryland RITA B. MESSING, Minnesota Department of Health, Division of Environmental Health, St. Paul SANFORD A. MILLER, Graduate School of Biomedical Sciences, University of Texas Health Sciences Center, San Antonio SUZANNE P. MURPHY, Department of Nutritional Sciences, University of California, Berkeley JOSEPH V. RODRICKS, ENVIRON Corporation, Arlington, Virginia IRWIN H. ROSENBERG, * Clinical Nutrition Division, USDA Human Nutrition Research Center on Aging, Tufts University and New England Medical Center, Boston, Massachusetts STEVE L. TAYLOR, Department of Food Science and Technology, University of Nebraska, Lincoln ROBERT H. WASSERMAN, † Department of Physiology, College of Veterinary Medicine, Cornell University, Ithaca, New York Consultants SHEILA DUBOIS, Food Directorate, Health Canada, Ottawa, Canada HERBERT BLUMENTHAL, Retired, Food and Drug Administration, Washington, D.C. Staff SANDRA A. SCHLICKER, Study Director SHEILA A. MOATS, Research Associate (April 1996–November 1996) ELISABETH A. REESE, Research Associate KIMBERLY A. BREWER, Research Assistant ALICE L. KULIK, Research Assistant DONNA M. LIVINGSTON, Project Assistant (April 1996–January 1997) GERALDINE KENNEDO, Project Assistant GAIL E. SPEARS, Administrative Assistant *   Member, Institute of Medicine. †   Member, National Academy of Sciences.

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DRI DIETARY REFERENCE INTAKES FOR Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride FOOD AND NUTRITION BOARD CUTBERTO GARZA (Chair), Division of Nutrition, Cornell University, Ithaca, New York JOHN W. ERDMAN, JR. (Vice Chair), Division of Nutritional Sciences, College of Agricultural, Consumer and Environmental Sciences, University of Illinois, Urbana-Champaign LINDSAY H. ALLEN, Department of Nutrition, University of California, Davis BENJAMIN CABALLERO, Center for Human Nutrition, Johns Hopkins School of Hygiene and Public Health, Baltimore, Maryland FERGUS M. CLYDESDALE, Department of Food Science, University of Massachusetts, Amherst ROBERT J. COUSINS, Center for Nutritional Sciences, University of Florida, Gainesville MICHAEL P. DOYLE, Center for Food Safety and Quality Enhancement, Department of Food Science and Technology, University of Georgia, Griffin JOHANNA T. DWYER, Frances Stern Nutrition Center, New England Medical Center and Tufts University, Boston, Massachusetts SCOTT M. GRUNDY, * Center for Human Nutrition, University of Texas Southwestern Medical Center, Dallas CHARLES H. HENNEKENS, Department of Medicine, Ambulatory Care and Prevention, Harvard Medical School, and Division of Preventive Medicine, Brigham and Women's Hospital, Boston, Massachusetts JANET C. KING, * University of California, Berkeley, and U.S. Department of Agriculture Western Human Nutrition Research Center, Presidio of San Francisco SANFORD A. MILLER, Graduate School of Biomedical Sciences, University of Texas Health Science Center, San Antonio ROSS L. PRENTICE, * Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, Washington A. CATHARINE ROSS, Department of Nutrition, The Pennsylvania State University, University Park ROBERT E. SMITH, R.E. Smith Consulting, Incorporated, Newport, Vermont VIRGINIA A. STALLINGS, Division of Gastroenterology and Nutrition, The Children's Hospital of Philadelphia, Pennsylvania VERNON R. YOUNG, * † Laboratory of Human Nutrition, School of Science, Massachusetts Institute of Technology, Cambridge *   Member, Institute of Medicine. †   Member, National Academy of Sciences.

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DRI DIETARY REFERENCE INTAKES FOR Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride Ex-Officio Member STEVE L. TAYLOR, Department of Food Science and Technology and Food Processing Center, University of Nebraska, Lincoln Institute of Medicine Council Liaison HARVEY R. COLTEN, * Northwestern University School of Medicine, Chicago, Illinois Staff ALLISON A. YATES, Director GAIL E. SPEARS, Administrative Assistant CARLOS GABRIEL, Financial Associate

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DRI DIETARY REFERENCE INTAKES FOR Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride Preface This report represents the initial report of a major new activity of the Food and Nutrition Board (FNB): the development of a comprehensive set of reference values for dietary nutrient intakes for the healthy population in the United States and Canada. Hallmarks of the new activity include (1) the establishment of a set of reference values to replace the Recommended Dietary Allowances (RDAs) for the United States published previously by the FNB; (2) for the first time, a single set of reference values for the United States and Canada; (3) the clear documentation of the derivation of the reference values; (4) the promotion of nutrient function and biologic-physical well-being; (5) the consideration of evidence concerning the prevention of disease and developmental disorders in addition to more traditional evidence of sufficient nutrient intake (for example, prevention of deficiency); (6) the examination of data about selected food components that have not been considered essential nutrients; and (7) recommendations for future research directions based on the knowledge gaps identified. Since the publication of the last version of the U.S. Recommended Dietary Allowances (NRC, 1989a) and of the Canadian Recommended Nutrient Intakes (Health Canada, 1990), there has been a significant expansion of the research base, an increased understanding of nutrient requirements and food constituents, and a better appreciation for the different types of nutrient data needed to address the applications of dietary reference values for individuals and population groups. There are now convincing reasons to conclude that

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DRI DIETARY REFERENCE INTAKES FOR Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride past approaches to establishing and applying the RDAs can be improved. Thus, the FNB considered it essential to reassess the nutrient requirement estimates that are needed for various purposes, how estimates of nutrient requirements should be developed, and how these values could be used in various settings of clinical and public health importance. To this end, the FNB's Standing Committee on the Scientific Evaluation of Dietary Reference Intakes (DRI Committee) is taking steps that should help eliminate some of the limitations, misinterpretations, and misuses of the 1989 RDAs and their predecessors. Indeed, the DRI Committee has already concluded that the 1989 edition of the Recommended Dietary Allowances should now be replaced in its entirety, rather than merely updated, by a new series of publications. The DRI Committee aims to achieve a consistent and coherent definition of requirements and of reference intakes for all essential nutrients and food components evaluated. (A brief description of the process is given in Appendix A.) In this context, the reference intake values presented in this and subsequent reports should have a broad, enduring, and useful application. This report defines requirements and other reference intake values for calcium, phosphorus, magnesium, vitamin D, and fluoride and represents the first in a series of reports providing both dietary reference intakes and guidance related to how to use them. Changes in the prepublication version (which was released in August, 1997) have been made to increase the readability and clarity of the information provided. Improvements in format and descriptions have been made consistent with the second report released in the series (which covers B vitamins and choline, the prepublication version of which was released in April, 1998). The DRI Committee deeply appreciates the comments received from many reviewers and individuals following the release of the prepublication version. Because of the limitations of present scientific knowledge, there are differences of opinion among scientists about some of the matters covered in this report. Reaching agreement on the interpretation of the evidence relating to calcium requirements has been a challenge, both because of the compelling conceptual argument to use maximal calcium retention as an indicator of adequacy as was presented in the prepublication version of this report, and subsequent statistical questions raised in the methodology used to estimate it after that version was released. In order to address these statistical issues, the DRI Committee chose in this final printed version of the report to refer to the indicator of adequacy used to

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DRI DIETARY REFERENCE INTAKES FOR Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride establish recommended intakes for calcium as desirable calcium retention. The balance data originally used in assessing maximal calcium retention were then recalculated (see Appendix E) to establish the estimates for adequacy of dietary calcium based on achieving the estimated desirable amount of calcium retention. In either case, consistent achievement of either maximal or desirable calcium intakes as the indicator of adequacy is presumed to reduce the risk of fracture secondary to osteopenia or osteoporosis. After much careful weighing of the evidence, the DRI Committee determined that, because reducing risk of chronic disease was the intended endpoint and there were many uncertainties about the epidemiologic and experimental data, the setting of Estimated Average Requirements and Recommended Dietary Allowances for calcium could not be justified. Thus, as described in the report, Adequate Intake values were set instead. It is not the function of this report, given the scope of work (see Appendix A, “Charge to the Panel on Calcium and Related Nutrients and Subcommittee on Upper Reference Levels”), to address applications of the DRIs. However, some uses for the different types of DRIs are described briefly in Chapter 9. The DRI Committee intends to issue a subsequent report that will focus on the uses of DRIs in various settings. It is hoped that the critical, comprehensive analyses of available information and of knowledge gaps will greatly assist the private sector, foundations, universities, government laboratories, and other institutions with their research interests and with the development of an exciting and realistic research agenda for the next decade. The support of Canada and Canadian scientists in this initiative for DRIs represents a pioneering first step toward the standardization of nutrient reference intakes at least within one continent. This report reflects the work of the FNB's DRI Committee, an expert Panel on Calcium and Related Nutrients, and the Subcommittee on Upper Reference Levels of Nutrients. The committee, the panel, and the subcommittee owe a considerable debt of gratitude to the many experts who have assisted with this report. Many, but far from all, of these people are named in Appendix B. Thanks also go to the many experts who devoted so much time to discussing these issues and to Burton Altura, Chor San Khoo, and Charles Pak, initial members of the Panel on Calcium and Related Nutrients and/or the Subcommittee on Upper Reference Levels of Nutrients. The respective chairs and members of the panel and subcommittee have performed their work under great time pressure. It

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DRI DIETARY REFERENCE INTAKES FOR Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride is because of their dedication that this report has come into being. All gave of their time willingly and without financial reward; both the science and practice of nutrition are major beneficiaries. The DRI Committee wishes to acknowledge the tireless efforts of the former and present FNB chairs, Janet King and Cutberto Garza, who began the initiative and played a key role in securing the funding that has been received to date. Similarly, thanks go to Allison Yates who has been instrumental in guiding this complex activity, and to Stephanie Atkinson and Ian Munro, who gave generously of their time and effort in chairing the Panel on Calcium and Related Nutrients and the Subcommittee on Upper Reference Levels of Nutrients, respectively. Finally, it is the staff of FNB who get the work completed. Special gratitude is expressed to Sandra Schlicker, study director for both the calcium panel and subcommittee, and Carol Suitor, who assumed the added responsibility of acting director of the FNB during the last few months of this project. The committee also recognizes the contributions of Elisabeth Reese, Kimberly Brewer, Alice Kulik, Sheila Moats, Gail Spears, Donna Livingston, and Geraldine Kennedo. We also thank Judith Grumstrup-Scott for editing the manuscript and Mike Edington and Claudia Carl for assistance with publication. Vernon Young Chair, Standing Committee on the Scientific Evaluation of Dietary Reference Intakes Cutberto Garza Chair, Food and Nutrition Board

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DRI DIETARY REFERENCE INTAKES FOR Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride Contents     SUMMARY   1  1   DIETARY REFERENCE INTAKES   21      Introduction,   21      What Are Dietary Reference Intakes?,   21      Categories of DRIs,   23      Uses of Dietary Reference Intakes,   27      Comparison with Other Countries,   28      Parameters for Dietary Reference Intakes,   31      Summary,   37  2   CALCIUM AND RELATED NUTRIENTS: OVERVIEW AND METHODS   38      Overview,   38      Methodological Considerations,   39      Nutrient Intake Estimates,   42      Dietary Intakes in the United States and Canada,   43      Use of Adequate Intake Rather Than Estimated Average Requirement,   48  3   A MODEL FOR THE DEVELOPMENT OF TOLERABLE UPPER INTAKE LEVELS   51      Background Information,   51      A Model for Derivation of Tolerable Upper Intake Levels,   52      Risk Assessment and Food Safety,   53

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DRI DIETARY REFERENCE INTAKES FOR Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride      Application of the Risk Assessment Model to Nutrients,   58      Steps in the Development of the UL,   62      Glossary,   69  4   CALCIUM   71      Background Information,   71      Estimating Requirements for Calcium,   84      Findings by Life Stage and Gender Group,   91      Tolerable Upper Intake Levels,   134      Research Recommendations   144  5   PHOSPHORUS   146      Background Information,   146      Estimating Requirements for Phosphorus,   158      Findings by Life Stage and Gender Group,   160      Tolerable Upper Intake Levels,   180      Research Recommendations,   189  6   MAGNESIUM   190      Background Information,   190      Estimating Requirements for Magnesium,   202      Findings by Life Stage and Gender Group,   208      Tolerable Upper Intake Levels,   242      Research Recommendations,   248  7   VITAMIN D   250      Background Information,   250      Estimating Requirements for Vitamin D,   259      Findings by Life Stage and Gender Group,   263      Tolerable Upper Intake Levels,   278      Research Recommendations,   286  8   FLUORIDE   288      Background Information,   288      Estimating Requirements for Fluoride,   298      Findings by Life Stage and Gender Group,   301      Tolerable Upper Intake Levels,   306      Research Recommendations,   313  9   USES OF DIETARY REFERENCE INTAKES   314      Overview,   314      Using Recommended Dietary Allowances,   315      Using Adequate Intakes,   317

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DRI DIETARY REFERENCE INTAKES FOR Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride      Using Tolerable Upper Intake Levels,   317      Using Estimated Average Requirements,   319      Other Uses of Dietary Reference Intakes,   323      Addressing Discrepancies Between Usual Intake and the AI,   324      Summary,   324     REFERENCES   325     APPENDIXES    A   Origin and Framework of the Development of Dietary Reference Intakes   375  B   Acknowledgments   381  C   Options for Dealing with Uncertainties   383  D   1994 CSFII Adjusted Data for Calcium, Phosphorus, and Magnesium   387  E   Model for Estimating Calcium Intake for Desirable Calcium Retention   394  F   Biographical Sketches of Committee, Subcommittee, Panel Members and Staff   399     INDEX   413

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