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Exploring the Biological
Contributions to
Human Health
Does Sex Matter?
Committee on Understanding the Biology of
Sex and Gender Differences
Theresa M. Wizemann and Mary-Lou Pardue, Editors
Board on Health Sciences Policy
INSTITUTE OF MEDICINE
NATIONAL ACADEMY PRESS
Washington, D.C.
OCR for page R2
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.
Support for this project was provided by the U.S. Department of Health and Human
Services (Office on Women's Health, National Institutes of Health Office of Research on
Women's Health, National Institute of Environmental Health Sciences, National Institute on
Drug Abuse, National Institute of Mental Health, U.S. Food and Drug Administration,
Centers for Disease Control and Prevention), the National Science Foundation, the Environ-
mental Protection Agency, the National Aeronautics and Space Administration, the Society
for Women's Health Research, the Research Foundation for Health and Environmental
Effects, Ortho-McNeil/Johnson & Johnson, and the Unilever United States Foundation. The
views presented in this report are those of the Committee on Understanding the Biology of
Sex and Gender Differences and are not necessarily those of the funding organizations.
Library of Congress Cataloging-in-Publication Data
Institute of Medicine (U.S.~. Committee on Understanding the Biology of
Sex and Gender Differences.
Exploring the biological contributions to human health: does sex
matter? / Committee on Understanding the Biology of Sex and Gender
Differences; Theresa M. Wizemann and Mary-Lou Pardue, editors.
p. ; cm.
Includes bibliographical references and index.
ISBN 0-309-07281-6 (hardcover)
1. Sex differences. 2. Sex factors in disease.
[DNLM: 1. Sex Factors. 2. Genetics, Biochemical. 3. Health. 4.
Research Design standards. 5. Sex Characteristics. QZ 53 I59e 2001]
I. Wizemann, Theresa M. II. Pardue, Mary Lou. III. Title.
QP81.5 .156 2001
616'.001'57846 dc21
2001002537
Additional copies of this report are available for sale from the National Academy Press,
2101 Constitution Avenue, N.W., Box 285, Washington, DC 20055. Call (800) 624-6242 or
(202) 334-3313 (in the Washington metropolitan area), or visit the NAP's home page at
www.nap.edu. The full text of this report is available at www.nap.edu.
For more information about the Institute of Medicine, visit the IOM home page at
www.iom.edu.
Copyright 2001 by the National Academy of Sciences. All rights reserved.
Printed in the United States of America
Cover photograph: Human X and Y Chromosomes (magnified 35,000 times). Source:
Biophoto Associates, Photo Researchers, Inc.
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"I(nowing is not enough; we invest apply.
Willing is not enough; we invest do."
Goethe
............. .......... -.-- .-.-
....... .... . .. . . .......
I NSTITUTE OF MEDICI N E
Shaping the Future for Health
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National Acaclemy of Sciences
National Acaclemy of Engineering
Institute of Meclicine
National Research Council
The National Academy of Sciences is a private, nonprofit, self-perpetuating soci-
ety of distinguished scholars engaged in scientific and engineering research, dedi-
cated 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. Bruce M. Alberts is president of the National
Academy of Sciences.
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of the National Academy of Sciences, as a parallel organization of outstanding
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A. Wulf is president of the National Academy of Engineering.
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its own initiative, to identify issues of medical care, research, and education. Dr.
Kenneth I. Shine 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
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ernment. Functioning in accordance with general policies determined by the Acad-
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Academy of Sciences and the National Academy of Engineering in providing
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nities. The Council is administered jointly by both Academies and the Institute of
Medicine. Dr. Bruce M. Alberts and Dr. William A. Wulf are chairman and vice
chairman, respectively, of the National Research Council.
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COMMITTEE ON UNDERSTANDING THE BIOLOGY OF SEX
AND GENDER DIFFERENCES
MARY-LOU PARDUE (Chair), Boris Magasanik Professor, Department
of Biology, Massachusetts Institute of Technology, Cambridge
DANIEL L. AZARNOFF, President, D. L. Azarnoff Associates, and
Senior Vice President, Clinical/Regulatory Affairs, Cellegy
Pharmaceuticals, South San Francisco
SHERI BERENBAUM, Professor, Department of Physiology, Southern
Illinois University School of Medicine, Carbondale
KAREN I. BERKLEY, McKenzie Professor, Program in Neuroscience,
Florida State University, Tallahassee
ANNE FAUSTO-STERLING, Professor of Biology and Women's
Studies, Senior Fellow, Francis Wayland Collegium, Brown
University, Providence
DANIEL D. FEDERMAN, Senior Dean for Alumni Relations and
Clinical Teaching, Carl W. Walter Professor of Medicine and
Medical Education, Harvard Medical School, Boston
BARBARA ANN GILCHREST, Professor and Chairman, Department
of Dermatology, Boston University, Boston
MELVIN M. GRUMBACH, Edward B. Shaw Professor of Pediatrics,
University of California San Francisco School of Medicine, San
Francisco
SHIRIKI KUMANYIKA, Associate Dean, Health Promotion and
Disease Prevention, Center for Clinical Epidemiology and
Biostatistics, University of Pennsylvania School of Medicine,
Philadelphia
JUDITH H. LaROSA, Professor, Department of Preventive Medicine
and Community Health, State University of New York Downstate
Medical Center at Brooklyn, Brooklyn
MICHAEL D. LOCKSHIN, Director, Barbara Volcker Center for
Women and Rheumatic Disease, Hospital for Special Surgery, and
Professor of Medicine, Weill College of Medicine of Cornell
University, New York
JILL PANETTA, Senior Research Scientist, Research Manager, Lilly
Center for Women's Health, Eli Lilly & Company, Indianapolis
CARMEN SAPIENZA, Professor of Pathology, Temple University
School of Medicine, Philadelphia
SALLY E. SHAYWITZ, Professor of Pediatrics, Yale University School
of Medicine, New Haven
JOHN G. VANDENBERGH, Professor, Department of Zoology, North
Carolina State University, Raleigh
v
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HUNTINGTON F. WILLARD, President and Director, Research
Institute of University Hospitals of Cleveland; Director, Center for
Human Genetics, University Hospitals of Cleveland; and Professor,
Department of Genetics, Case Western Reserve University,
Cleveland
Board on Health Sciences Policy Liaison
MARY WOOLLEY, President, Research!America, Washington, D.C.
IOM Project Staff
THERESA M. WIZEMANN, Study Director
THELMA COX, Project Assistant
SARAH PITLUCK, Research Associate (through rune 2000)
IOM Staff
ANDREW POPE, Director, Board on Health Sciences Policy
ALDEN CHANG, Administrative Assistant
DALIA GILBERT, Senior Project Assistant
CARLOS GABRIEL, Financial Associate
MICHAEL EDINGTON, Managing Editor (through February 2001)
Copy Editor
MICHAEL K. HAYES
Consultant
KATHI MANNA
Al
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Reviewers
This report has been reviewed in draft form by individuals chosen for
their diverse perspectives and technical expertise, in accordance with pro-
cedures approved by the National Research Council's (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:
LESLIE Z. BENET, Professor, Department of Biopharmaceutical
Sciences, University of California, San Francisco
DAVID P. CREWS, Ashbel Smith Professor of Zoology and
Psychology, University of Texas at Austin
ALICE EAGLY, Professor, Department of Psychology, Northwestern
University, Evanston, IL
SHERINE E. GABRIEL, Director, Center for Patient Oriented Research,
Mayo Clinic, Rochester, MN
JANET S. HYDE, Chair, Department of Psychology, University of
Wisconsin at Madison
ELEANOR E. MACCOBY, Professor Emeritus, Department of
Psychology, Stanford University, Stanford
v''
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V111
REVIEWERS
BRUCE S. MCEWEN, Alfred E. Mirsky Professor, Harold and Margaret
Milliken Hatch Laboratory of Neuroendocrinology, The Rockefeller
University, New York
RUTH B. MERKATZ, Director/Team Leader Pfizer Women's Health,
Pfizer Inc., New York, Associate Clinical Professor, Albert Einstein
College of Medicine, New York
HARRY OSTRER, Associate Professor and Director of Human Genetics
Program, Department of Pediatrics, New York University School of
Medicine, New York
ORA H. PESCOVITZ, Section Director of Pediatrics, Edwin Letzter
Professor of Pediatrics, Indiana University, Indianapolis
DAVID S. PISETSKY, Professor of Medicine and Professor of
Immunology, Duke University Medical Center, Durham, NC
CHRISTINE E. SEIDMAN, Professor, Department of Genetics,
Harvard Medical School, Boston
CAROLINE C. WHITACRE, Professor and Chair, Department of
Molecular Virology, Immunology and Medical Genetics, Ohio State
University, Columbus
Although the reviewers listed above have provided many construc-
tive comments and suggestions, they were not asked to endorse the con-
clusions or recommendations, nor did they see the final draft of the report
before its release. The review of this report was overseen by ELIZABETH
BARRETT-CONNOR, Professor and Chief, Division of Epidemiology,
University of California, San Diego, appointed by the Institute of Medi-
cine, and BARBARA CALEEN HANSEN, Professor of Physiology and
Director, Obesity and Diabetes Research Center, University of Maryland
School of Medicine at Baltimore, appointed by the NRC's Report Review
Committee, who were responsible for making certain that an indepen-
dent examination of this report was carried out in accordance with insti-
tutional procedures and that all review comments were carefully consid-
ered. Responsibility for the final content of this report rests entirely with
the authoring committee and the institution.
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Preface
Does sex matter? Almost anyone would answer "yes" to this simple
question. However, subsumed within this question are two much more
difficult questions: When does sex matter? and How does sex matter?
These two questions define the task undertaken by the Committee on
Understanding the Biology of Sex and Gender Differences. This commit-
tee was charged with evaluating the current scientific understanding of
the answers to these questions with respect to their influence on human
health.
Specifically, the committee was charged with considering biology at
the cellular, developmental, organ, organismal, and behavioral levels. The
goal, as in all studies of biology, is to understand the organism in terms of
all of the interactions that occur between levels within the organism as
well as the mutual interactions between the organism and its environ-
ment. This was a broad charge, which required a committee made up of
individuals drawn from a wide range of subfields of biology and medi-
cine. We have learned much from each other and from a number of in-
vited speakers specializing in fields in which the committee did not have
expertise. We also made an extensive survey of the relevant literature.
The most obvious and best-studied differences between the sexes are
in the reproductive systems. Much less work has been done on sex differ-
ences in nonreproductive areas of biology, and this is where the commit-
tee has focused its efforts. Differences are much less expected in nonre-
productive areas of biology, but differences do occur, and some of these
differences have important consequences. Understanding these differ-
IX
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x
PREFACE
ences makes it possible to design health care more effectively for indi-
viduals, both males and females.
An additional and more general reason for studying differences be-
tween the sexes is that these differences, like other forms of biological
variation, can offer important insights into underlying biological mecha-
nisms. An often-quoted piece of advice to those studying biology is to
"cherish your exceptions." These exceptions traditionally include organ-
isms with mutations and organisms from different species that accom-
plish the same goal in slightly modified ways. Only relatively recently has
it been recognized that sexual variations are as important as these excep-
tions in providing similarities and contrasts that can reveal important
details about the processes involved.
This is an especially opportune time to take stock of what is known
about differences and similarities in the basic biology of the sexes, be-
cause in the last few years biological research has acquired an arsenal of
powerful tools that can be used to answer new questions. Reviews like
the one presented in this report juxtapose knowledge from different sub-
fields, create new connections between subfields, and inevitably, raise
new questions. The arsenal of new tools enables us to answer questions
that only a short time ago seemed impossible to answer.
The picture that emerges from the study described in this report
shows that there are numerous sex differences in nonreproductive tis-
sues. Some of these differences can be explained by what we now know.
Some are unexplained and point to important questions for future study.
Some are large and have known effects on the health of individuals; these
differences have immediate consequences in terms of health care. Some of
the differences are small, with no known effects on health, but they may
provide clues that can be used to solve new biological questions. This
report provides a broad view of the research and issues that the commit-
tee considered. It is, of necessity, a summary with a small number of
examples chosen to illustrate the points that we make and to convey the
interesting science that is being done in these areas.
Sex does matter. It matters in ways that we did not expect. Undoubt-
edly, it also matters in ways that we have not begun to imagine.
Mary-Lou Pardue, Ph.D.
Chair
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Acknowledgments
The committee is indebted to the experts in many scientific disci-
plines who presented informative talks to the committee and participated
in lively discussions (see Appendix A). In addition, the committee is grate-
ful to the members of the scientific community who made themselves
available by phone and e-mail for consultation and technical advice.
The committee also wishes to thank the Institute of Medicine staff
who contributed to the report. Theresa Wizemann has done a superb job
as study director. Thelma Cox has taken very good care of the committee,
in spite of severe weather conditions at two of the meetings that pre-
sented challenges to her management skills. Sarah Pitluck provided able
assistance in the early part of the study and Dalia Gilbert assisted in the
later stages. Kathi Hanna, Michael Hayes, and Michael Edington pro-
vided helpful style guidance and technical editing. Valerie Setlow helped
guide the early development stages of the project. The committee thanks
Andrew Pope, Director of the Board on Health Sciences Policy for his
continuing interest in this work and guidance throughout the process.
Many thanks go to Bruce Alberts, President of the National Academy
of Sciences and Chair of the National Research Council, and Ken Shine,
President of the Institute of Medicine, for advice and guidance in focusing
the task. Thanks also go to the staff of the National Research Council
Board on Biology for helpful suggestions and nominations of committee
members and reviewers.
This report was made possible by the generous support of 14 spon-
sors: U.S. Department of Health and Human Services (Office on Women's
Health, National Institutes of Health Office of Research on Women's
Xl
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X11
ACKNOWLEDGMENTS
Health, National Institute of Environmental Health Sciences, National
Institute on Drug Abuse, National Institute of Mental Health, U.S. Food
and Drug Administration, Centers for Disease Control and Prevention),
the National Science Foundation, the Environmental Protection Agency,
the National Aeronautics and Space Administration, the Society for
Women's Health Research, the Research Foundation for Health and Envi-
ronmental Effects, Ortho-McNeil/Iohnson & Johnson, and the Unilever
United States Foundation. Special thanks go to Phyllis Greenberger of the
Society for Women's Health Research, Vivian Pinn of the National Insti-
tutes of Health Office of Research on Women's Health, and Susan Wood,
formerly of the Office on Women's Health of the U.S. Department of
Health and Human Services for their persistence and vision in develop-
ing the proposal for this study.
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Contents
ABSTRACT
EXECUTIVE SUMMARY
1 INTRODUCTION
Scope of the Report, 14
Sex Differences Beyond the Reproductive System, 19
Evolving Research Policy, 21
Organization of Report, 26
2 EVERY CELL HAS A SEX
Sex and the Human Genome, 29
Basic Molecular Genetics: What Is the Potential for Differences
Between the Sexes?, 32
Effects of Parental Imprinting on the Expression of Genetic
Information, 40
Unexpected or Nonobvious Sex Differences, 41
Genetics as a Tool, 42
Findings and Recommendations, 44
3 SEX BEGINS IN THE WOMB
Biology of Sex, 46
Early Development, 50
Puberty, 62
Adulthood, 72
Findings and Recommendations, 77
. . .
x'''
ax
1
13
28
45
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xIv
4 SEX AFFECTS BEHAVIOR AND PERCEPTION
Sex Differences in Behavior and Cognitive Abilities, 79
Effects of Hormones on Behavior and Cognition, 89
Sex Differences in Perception of Pain, 105
Animal Models of Cerebrovascular and Cardiovascular
Diseases, 112
Findings and Recommendations, 115
5 SEX AFFECTS HEALTH
Sex Differences in Response to Therapeutic Agents:
Diagnostic and Therapeutic Interventions, 118
Metabolism, Lifestyle, and Physical Performance, 130
Sex Differences in Autoimmune Conditions, 142
A Spectrum of Sex Differences Across a Disease:
Coronary Heart Disease, 158
Findings and Recommendations, 170
CONTENTS
79
117
6 THE FUTURE OF RESEARCH ON BIOLOGICAL SEX
DIFFERENCES: CHALLENGES AND OPPORTUNITIES 173
Terminology, 174
Research Tools and Resources, 176
Interdisciplinary and Collaborative Research, 181
Non-Health-Related Implications of Research on Sex
Differences in Health, 183
REFERENCES
APPENDIXES
A Data Sources and Acknowledgments
B Physiological and Pharmacological Differences
Between the Sexes
C Glossary
D Committee and Staff Biographies
INDEX
TABLES, FIGURES, AND BOXES
Tables
3-1 Some Genes Involved in Human Sex Determination, 53
3-2 Selected Examples of Variations in Sexual Differentiation, 63
185
229
233
239
243
255
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CONTENTS
3-3 Life Expectancy at Birth, Age 65, and Age 75 Years, United States,
All Races, 1998, 75
xv
Sex Prevalence of Some Common Painful Syndromes and Potential
Contributing Causes, 106
A Growing List of Therapies for Pain, 110
Sex-Specific Responses to an Experimental Traumatic or Ischemic
Cerebral Insult, 113
5-1 Factors Affecting Absorption of Chemicals, 120
5-2 Differences in Drug Concentrations Between the Mother and Fetus
and Between Males and Females, 124
5-3 Receptor, Enzyme, and Structural Differences Between Males and
Females, 128
5-4 Obesity Prevalence Data for Selected U.S. Adults, by Sex, 135
5-5 Sex Differences in Immunocytes as Determined in Representative
Recent Studies, 145
5-6 Sex Differences in Immunization, 146
5-7 Sex Differences in Viral Infections in Humans, 148
5-8 Sex Differences in Mycobacterial, Fungal, and Parasitic
Diseases, 149
5-9 Female/Male Ratios Associated with Common Autoimmune
Diseases, 150
5-10 Autoimmune Diseases in Which Environmental Triggers Are
Prominent, 151
5-11 Peak Ages of Various Autoimmune Diseases, 154
5-12 Animal Models of Human Autoimmune Diseases, 156
5-13 Estimated Risk of Symptoms of Coronary Heart Disease and
Death from Myocardial Infarction in Heterozygotes at
Different Ages, 160
5-14 Smoking Prevalence by Race and Sex, 1998, 163
5-15 Complications of Acute Myocardial Infarctions, by Sex, 167
5-16 Male: Female Odds Ratios for Use of Diagnostic Procedures for
Coronary Heart Disease, 169
Figures
2-1 Schematic representations of two general models used to explain
sex differences in gene expressions, 30
Comparison of gene content and gene organization on the X and Y
chromosomes, 33
Schematic representation of X-chromosome inactivation in female
somatic cells, 36
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X'7t1
Van
i
CONTENTS
3-1 From genotype to phenotype: a diagrammatic representation of hu-
man sex determination and differentiation, 52
Hypothetical diagrammatic representation of the cascade of sex
chromosomal and autosomal genes involved in testis determination
and the hormones involved in male sex differentiation (representa-
tion 1), 56
Hypothetical diagrammatic representation of the cascade of sex
chromosomal and autosomal genes involved in testis determination
(A) and the hormones involved in male sex differentiation (B) (rep-
resentation 2), 57
3-4 Comparison of the pattern of change of serum testosterone (T) levels
and hCG and serum pituitary LH (LER-960) and FSH (LER-869)
levels in the human male fetus during gestation with morphological
changes in the fetal testis, 59
3-5 Adolescent growth spurts in girls and boys (growth velocity
curves), 69
3-6 Life expectancy at birth for males and females in several U.S. ethnic
groups (data are from 1989 to 1994), 76
Life expectancy at birth for males and females, selected years be-
tween 1900 and 1998, United States, all races, 76
Frequency distribution of scores on a hypothetical cognitive test
plotted separately by sex, 85
Behavioral development in rodents, 96
Composite images of the distribution of activations upon perfor-
mance of rhyme-case tasks (phonological processing) for 19 males
and 19 females, 103
5-1 Schematic representation of absorption, distribution, metabolism,
and excretion of drugs, 119
5-2 The major affecters of body fat, 132
5-3 Death rates for diseases of the heart by age and sex, 1995-1997, 161
5-4 Age-adjusted high serum cholesterol levels (>240 mg/dl)
among individuals ages 20 to 74 years by sex and race, 1988-1994,
163
5-5 Non-age-adjusted high serum cholesterol levels (>240 mg/dl)
by sex and age, 164
5-6
5-7
Mortality from coronary heart disease and diabetes in men and
women ages 25 to 64, 166
External agents, 171
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CONTENTS
. .
XVII
Boxes
1 Summary of Barriers to Progress in Research on Sex Differences, 10
2 Summary of Recommendations, 11
Definitions, 17
Examples of Sex Differences Beyond the Reproductive System, 22
2-1 Genetic Factors That May Differentially Affect the Basic Biochemis-
try of Male and Female Cells, 31
Sex Differences in the Relationship of Onset of Pubertal Growth
Spurt to Sexual Maturation in Girls and Boys, 67
Sex Differences in the Timing of the Onset of Estrogen Synthesis in
Girls and Boys, 68
5-1 Definitions, 118
5-2 Levels and Types of Models for Study of Infection and
Inflammation, 143
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Abstract
One of the most compelling reasons for looking at what is known about
the biology of sex differences is that there are striking differences in human
disease that are not explained at this time.
Being male or female is an important basic human variable that affects
health and illness throughout the life span. Differences in health and illness
are influenced by individual genetic and physiological constitutions, as
well as by an individual's interaction with environmental and experiential
factors. The incidence and severity of diseases vary between the sexes and
may be related to differences in exposures, routes of entry and the process-
ing of aforeign agent, and cellular responses. Although in many cases these
sex differences can be traced to the direct or indirect effects of hormones
associated with reproduction, differences cannot be solely attributed to hor-
mones. Therefore, sex should be considered when designing and analyzing
studies in all areas and at all levels of biomedical and health-related re-
search.
The study of sex differences is evolving into a mature science. There is
now sufficient knowledge of the biological basis of sex differences to validate
the scientific study of sex differences and to allow the generation of hypoth-
eses with regard to health. The next step is to move from the descriptive to
the experimental phase and establish the conditions that must be in place to
facilitate and encourage the scientific study of the mechanisms and origins
of sex differences. Naturally occurring variations in sex differentiation can
provide unique opportunities to obtain a better understanding of basic
differences and similarities between and within the sexes.
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xx
ABSTRACT
Barriers to the advancement of knowledge about sex differences in health
and illness exist and must be eliminated. Scientists conducting research on
sex differences are confronted with an array of barriers to progress, includ-
ing ethical,financial, sociological, and scientific factors.
The committee provides scientific evidence in support of the conclusions
presented above and makes recommendations to advance the understand-
ing of sex differences and their effects on health and illness.