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vi Contents

Chapter 10 Menstrual Function and Dysfunction in the Female Athlete............205

Anne B. Loucks

Chapter 11 Recommendations for Optimizing Bone Strength and

Reducing Fracture Risk in Female Athletes..................................... 229
Michelle Barrack
Index....................................................................................................................... 247
Preface
Research examining the effects of nutrition on sports performance (i.e., sport nutri-
tion) has exploded over the last 25 years. The interest in and proliferation of sport nutri-
tion research has led to the creation of two scientific journals, numerous textbooks, and
countless Web sites devoted specifically to this topic. Sports dietitians, coaches, and
trainers are basing nutrition recommendations to their female athletes on the exist-
ing sport nutrition research. Similarly, the existing sport nutrition research is guiding
and marketing the manufacturing of sport nutrition products to female athletes. All
the while, a key limitation of much of the existing sport nutrition research is being
overlooked; with a few exceptions, the majority of studies have employed only male
subjects. The results of these studies are then generalized to females with no scientific
support for the validity or accuracy of such a generalization. This oversight is not
exclusive to sports nutrition research. One need only review the history of sports in
general to appreciate the relative dominance by men and limited inclusion of women
in all facets of athletics.
In the United States, relatively few women competed in sports until the late 19th
and early 20th centuries, when social changes in North America favored increased
female participation in society as equals with men (Oglesby 1978). Although women
were technically permitted to participate in sports, relatively few did due to the social
stigma as well as concerns regarding the effects of strenuous exercise on a wom-
an’s physical “constitution” (in particular, her reproductive health) (Oglesby 1978).
Two World Wars and a couple of key social “movements” (i.e., the civil rights and
women’s movements) brought more women onto the athletic playing fields. However,
it was not until 1972 when the U.S. Congress passed Title IX of the Educational
Movements that the door to women’s participation in sports was truly opened (Bell
2007). Subsequent to Title IX, women and girls have become much more involved
in sports. College women’s athletic participation has increased from 15% in 1972 to
43% in 2001. High school girl’s athletic participation increased from 295,000 in 1971
to 2.8 million in 2002–2003, an increase of over 840% (Carpenter and Acosta 2005).
With an increase in women’s sports participation has come a greater recognition
of and appreciation for the biomechanical and physiological differences between
men and women. Over the last 30 years, sports equipment and clothing manufactur-
ers have become more interested in developing and marketing products specifically
for women. I have witnessed this “evolution” personally. In the late 1970s, when
I first took up distance running, there were no “women’s running shoes”; I had to
make do with the smallest-sized men’s shoe I could find. Similarly, if I wanted nylon
running shorts I had to search the boy’s or young men’s department. Today, every
major running shoe manufacturer has not one but several shoes designed specifically
for women, and there are numerous clothing lines that cater specifically to women’s
exercise wear.
Thanks in large part to the innovative studies conducted in the early 1990s by
Mark Tarnopolsky and others at McMaster University (Ontario, Canada), researchers

vii
viii Preface

are also starting to appreciate that the physiological differences between men and
women may translate into different responses and adaptations to nutritional manipu-
lations and, thus, different recommendations in terms of sport nutrition practices.
Therein lies the premise of this book.
It is now well established that females are metabolically unique from their male
counterparts; thus, their nutritional requirements for optimal training and athletic
performance are likely also unique.
Chapter 1 sets the stage for the discussion of gender-specific nutrition recommenda-
tions by highlighting recent research indicating that substrate utilization during exercise
differs significantly between men and women. Written by the pioneer in this particular
topic area, Mark Tarnopolsky, and one of his recent PhD students, Amy Maher, pro-
vide a number of possible explanations for the gender differences in substrate utiliza-
tion as well as implications for gender-specific nutritional recommendations.
Louise Burke and Christine Dziedzic tackle the topic of carbohydrate needs of
female athletes in Chapter 2. More specifically, the validity of generalizing the cur-
rent guidelines for carbohydrate replacement before, during, and after exercise to
female athletes is examined. Examples of ways in which female athletes can address
their carbohydrate intake goals in the context of other nutritional needs and dietary
concerns are also provided.
In Chapter 3, Nancy Rodriguez addresses the importance of adequate dietary
protein in the diets of female athletes by reviewing the myriad of structural and
functional roles that protein plays within the athlete’s body. The effects of inadequate
protein intake, particularly in combination with inadequate energy intake, on the
health and performance of the female athlete are discussed and are used to guide
recommendations for dietary protein intake.
Proper hydration is as important as carbohydrate and protein intake in terms of
optimizing performance and the overall health of the female athlete. Dehydration
negatively impacts performance as water increases body core temperature, heart
rate, glycogen utilization, and perceived exertion. Nina Stachenfeld has spent a sig-
nificant portion of her research career investigating the effects of reproductive hor-
mones on the fluid and temperature regulatory systems in women. In Chapter 4, she
and her former postdoctoral associate, Megan Wenner, examine sex differences in
thermoregulation and fluid balance in order to determine whether female-specific
fluid recommendations are necessary.
Although they do not provide energy or support hydration, there is no question
that micronutrients (i.e., vitamins and minerals) play a critical role in supporting
training, competition, and the overall health of the female athlete. Nonetheless,
research indicates that female athletes often have suboptimal micronutrient intakes
that place them at risk for deficiency. Nutrients that seem to be of particular concern
for female athletes are discussed in Chapters 5 through 7. In Chapter 5, Pamela
Hinton highlights the importance of iron and zinc for athletic performance and pro-
vides suggestions for helping female athletes meet their iron and zinc requirements.
Bone nutrients are covered in Chapter 6 by Kristine Spence. In Chapter 7, Kathleen
Woolf, Dara LoBuono, and Melinda Manore provide a comprehensive review of the
exercise-related functions, food sources, and recommended intakes for each of the
B vitamins.
Preface ix

The final four chapters of the book (i.e., Chapters 8 through 11) are devoted to
a discussion of a set of three distinct yet often interrelated disorders including low
energy availability, menstrual dysfunction, and poor bone health that have come to
be known as the female athlete triad (Triad). Katherine Beals examines the concept
of energy availability and summarizes the existing research regarding the etiology,
prevalence, and consequences of low energy availability among female athletes. The
foremost expert in endocrinology and the female athlete, Anne Loucks, provides
a comprehensive review of the research examining menstrual dysfunction among
female athletes with an emphasis on its prevalence, causes, consequences, and treat-
ment options. Finally, Michelle Barrack addresses the third and final component of
the Triad, bone health. Her chapter highlights genetic and lifestyle characteristics,
including sport-specific factors that affect bone health, and provides behavioral rec-
ommendations female athletes can employ to optimize bone health and reduce their
risk of musculoskeletal injuries.

REFERENCES
Bell, R. C. A history of women in sport prior to Title IX. The Sport Journal. 2007. Volume
10. http//www.thesportjournal.org/article/history-women-sport-prior-title-ix. Accessed
May 1, 2012.
Carpenter, L. J., and R. V. Acosta. 2005. Title IX. Champaign, IL: Human Kinetics.
Oglesby, C. A. 1978. Women and Sport: From Myth to Reality. Philadelphia, PA: Lea & Febiger.

Katherine A. Beals
Division of Nutrition
University of Utah
Salt Lake City, Utah
The Editor
Katherine A. Beals, PhD, RD, FACSM, CSSD, is an associate professor (clinical)
in the Division of Nutrition and an adjunct lecturer in the Department of Exercise
and Sports Sciences at the University of Utah (Salt Lake City). She teaches graduate
courses in macro- and micronutrient metabolism, sports nutrition, and exercise and
aging. Prior to her work at the University of Utah, she held an academic appointment
as an associate professor in the Department of Family and Consumer Sciences at
Ball State University in Muncie, Indiana.
Dr. Beals holds a PhD in exercise science and physical education from Arizona
State University, is a registered dietitian, a fellow of the American College of
Sports Medicine, and a Certified Specialist in Sports Dietetics. She has published
more than a dozen articles and several book chapters on disordered eating and the
female athlete triad. In addition, she has published two books on disordered eating
including Disordered Eating among Athletes: A Comprehensive Guide for Health
Professionals (Human Kinetics, 2004) and The Hidden Faces of Eating Disorders
and Body Image (Human Kinetics, 2009).

xi
Contributors
Michelle Barrack, PhD, RD Nancy R. Rodriguez, PhD, RD,
California State University–Northridge FACSM, CSSD
University of Connecticut
Louise M. Burke, PhD, RD, FACSM Storrs, Connecticut
Sports Nutrition
Australian Institute of Sport Kristine Spence, MS, RD, CSSD
Canberra, Australia Utah Dairy Council
Salt Lake City, Utah
Christine E. Dziedzic
Sports Nutrition Nina S. Stachenfeld, PhD
Australian Institute of Sport The John B. Pierce Laboratory
Canberra, Australia New Haven, Connecticut
and
Pamela Hinton, PhD Department of Obstetrics,
University of Missouri–Columbia Gynecology and Reproductive
Columbia, Missouri Sciences
Yale School of Public Health
Dara L. LoBuono Yale School of Medicine
New York University New Haven, Connecticut
New York, New York

Anne B. Loucks, PhD Mark A. Tarnopolsky, MD, PhD

Department of Biological Sciences McMaster University
Ohio University Hamilton, Ontario, Canada
Athens, Ohio
Megan M. Wenner, PhD
Amy C. Maher, MSc, PhD Department of Kinesiology and
University of Guelph Applied Physiology
Guelph, Ontario, Canada University of Delaware
Newark, Delaware
Melinda M. Manore, PhD, RD,
FACSM Kathleen Woolf, PhD, RD, FACSM
Oregon State University New York University
Corvallis, Oregon New York, New York

xiii
 1 Substrate Utilization
in Female Athletes
Implications for Fuel
Selection and Macronutrient
Requirements
Amy C. Maher and Mark A. Tarnopolsky

CONTENTS
Introduction................................................................................................................. 1
Sex Differences in Substrate Utilization during Endurance Exercise......................... 2
Methodological Considerations for Measuring Substrate Utilization in
Female Athletes........................................................................................................... 3
Sex Differences in Carbohydrate Metabolism during Exercise.................................. 4
Overview of Carbohydrate Oxidation.................................................................... 4
Sex Differences in Carbohydrate (CHO) Oxidation.............................................. 5
Carbohydrate Utilization and Exercise Performance in Women Athletes.................. 6
Sex Differences in Fat Metabolism............................................................................. 8
Overview of Fat Metabolism.................................................................................. 8
Sex Differences in Fat Oxidation........................................................................... 9
Effects of Estrogen on CHO and Fat Utilization during Endurance Exercise..... 11
Sex Differences in Protein Metabolism during Exercise.......................................... 14
Summary................................................................................................................... 15
References................................................................................................................. 16

INTRODUCTION
Until recently, it was assumed that men and women responded similarly to the
metabolic stress of exercise; however, accumulating evidence supports that sex
(gender) influences fuel metabolism during exercise. Specifically, controlled
studies accounting for menstrual cycle phase, diet, habitual training, and aerobic
capacity have consistently shown that women have higher relative fat oxidation
and lower protein and carbohydrate (CHO) oxidation during submaximal inten-
sity exercise as compared to men (Tarnopolsky et al. 1990; Phillips et al. 1993;
Tarnopolsky et al. 1995; Friedlander et al. 1998; Horton et al. 1998; Davis et al.

1
2 Nutrition and the Female Athlete: From Research to Practice

2000; Carter et al. 2001a; Lamont et al. 2001b; Ruby et al. 2002; Devries et al.
2005). Sex differences in metabolism are likely genetically regulated either by
predetermined expression of genes or by the regulation of gene expression through
cell signaling mechanisms, likely mediated through sex hormones (estrogen, pro-
gesterone, and testosterone) (Wolfe et al. 2000; Ferrando et al. 2002; Fu et al.
2009; Maher et al. 2009). Despite the differences in substrate utilization during
exercise, the adaptations in aerobic capacity to endurance exercise training appear
to be similar between men and women (Friedlander et al. 1998; McKenzie et al.
2000; Skinner et al. 2001).
Research examining the impact that metabolic differences due to sex, menstrual
cycle, and age have on nutritional recommendations in recreational and top sport
female athletes is still in its infancy. Thus, at this time, we can only speculate on how
sex differences in substrate utilization may affect nutritional recommendations for
the physically active woman. However, recent advances in modern techniques such as
proteomics and gene expression array analysis are proving useful in helping us under-
stand the molecular basis for differences in these areas. This chapter will focus on
describing sex differences in macronutrient fuel selection, the possible mechanisms
for these differences, and implications that these differences may have with respect to
nutritional recommendations to optimize performance for the female athlete.

SEX DIFFERENCES IN SUBSTRATE UTILIZATION

DURING ENDURANCE EXERCISE
For years it was assumed that substrate utilization during exercise was similar
between men and women. This assumption was based largely on a study con-
ducted by David Costill and colleagues (1976) in which they compared trained
women with men (track athletes) and also untrained women with untrained men.
Their results suggested that when compared based on training history, men and
women had similar VO2max (ml/kg × min –1), enzyme activity, and muscle fiber
types (Costill et al. 1976). Consequently, much of the research regarding energy
metabolism and fuel utilization during exercise has been conducted predomi-
nately on men as there was no reason to believe that the generalization of results
did not apply to women. Indeed, it was not until the last decade that researchers
began to seriously consider the probability of sex differences in exercise sub-
strate metabolism.
In 1990 Tarnopolsky and colleagues compared substrate utilization in women and
men during an acute treadmill run at 65% of VO2max (Tarnopolsky et al. 1990). The
women and men were matched for training history and consumed a controlled iso-
caloric diet for 3 days prior to testing (55% CHO, 30% fat, 15% protein). The women
had a significantly lower respiratory exchange ratio (RER)*, 25% lower muscle gly-
cogen utilization, and 30% lower urea nitrogen excretion (Tarnopolsky et al. 1990).

* RER is the ratio of the volume of carbon dioxide eliminated from the lungs to the volume of oxygen
taken into the lungs per minute and gives an estimation of the ratio of fuel being metabolized (e.g., pure
fat has an RER of 0.7 while pure CHO has an RER of 1.0).
Substrate Utilization in Female Athletes 3

These results were pivotal in demonstrating that during submaximal, long-duration

exercise, women utilize more fat and less CHO and protein compared with men.
Most cross-sectional studies have found that whole-body oxidation rates are dif-
ferent for women as compared with men during endurance exercise at submaximal
exercise intensities (Froberg and Pedersen 1984; Blatchford et al. 1985; Phillips et
al. 1993; Tarnopolsky et al. 1995, 1997; Friedlander et al. 1998; Horton et al. 1998;
Goedecke et al. 2000; McKenzie et al. 2000; Carter et al. 2001a; Lamont et al. 2001a;
Melanson et al. 2002; Roepstorff et al. 2002; Steffensen et al. 2002; Lamont et al.
2003; Zehnder et al. 2005; Devries et al. 2006; Horton et al. 2006; Roepstorff et al.
2006; Wallis et al. 2006; Pillard et al. 2007; Kang et al. 2009; Maher et al. 2010b).
Specifically, women demonstrate a relatively greater fat oxidation and concomitantly
lower CHO and protein oxidation compared to men at the same relative exercise
intensity ranging from 50 to 70% VO2max. This has been demonstrated in studies
employing cycling as well as treadmill running as the mode of exercise for duration
of 60 to 120 minutes. These sex differences in substrate oxidation can be observed
in both trained (exercise three or more times a week) and untrained (do not exercise)
men versus women (reviewed in Tarnopolsky 2008).
It should be noted that not all studies have found gender differences in whole-
body substrate utilization (Costill et al. 1979; Davis et al. 2000; Romijn et al. 2000;
Mittendorfer et al. 2002; Riddell et al. 2003; M’Kaouar et al. 2004), partly due to
methodological differences (which will be described in detail in the next section).
Nonetheless, when whole-body RER values from all gender comparative studies
were combined into a “meta-analysis” (even those not showing an effect), the spe-
cific sex differences in substrate utilization were maintained (Tarnopolsky 2008).
Specifically, the results of the meta-analysis supported the relatively greater fat oxi-
dation of women compared to men (~62% versus 43%, respectively) and relatively
higher CHO and protein oxidation rates for men compared to women (52% ver-
sus 36% and 5% versus 2%, respectively) (Phillips et al. 1993; Tarnopolsky 2000;
Lamont et al. 2001a, 2005).

METHODOLOGICAL CONSIDERATIONS FOR MEASURING

SUBSTRATE UTILIZATION IN FEMALE ATHLETES
Whole-body substrate metabolism has generally been evaluated during endurance
exercise using indirect calorimetry, whereas RER is used for the estimation of
whole-body fat and CHO utilization. There are several factors that may alter sub-
strate oxidation rates during exercise that must be controlled for when conducting
studies designed to evaluate the effects of gender differences in fuel selection and
substrate utilization. Specifically, the subject’s size (weight), training status and his-
tory, and habitual and pre-exercise dietary intake status. On average, women have
a higher percentage of body fat (~5 to 10%) and lower muscle mass compared with
similar age- and activity-matched men (Tarnopolsky et al. 1990, 2000; Carter et al.
2001a; Tarnopolsky, Zawada et al. 2001). Therefore, it is important to express the
main indicator of fitness (VO2max) relative to lean body mass (ml O2/kg LBM/min),
as comparisons based on absolute VO2max would lead to the selection of females who
are heavier than the males. Similarly, exercise training has multiple consequences on
4 Nutrition and the Female Athlete: From Research to Practice

physiological and metabolic function, which ultimately alters VO2max, which is why
subjects should also be matched based on training history (Cureton and Sparling
1980). To overcome the issue of training history, a longitudinal approach can be
taken in research such that untrained people are placed on a set exercise program to
ensure equality of training (Devries et al. 2008). This matching approach takes into
account both environmental (training state) factors and genetic (VO2max potential)
factors that contribute to VO2max and expresses them relative to the mass of metaboli-
cally active tissues (Tarnopolsky and Saris 2001).
Habitual dietary intake should be compared between men and women in the same
study, as high-CHO-low-fat diets lead to a greater reliance on CHO metabolism and
low-CHO-high-fat diets lead to a greater reliance on fat metabolism (Spriet and Peters
1998), which could ultimately skew results if one sex prefers a diet slightly differ-
ent than the other. It is noteworthy that most sex-based studies comparing habitual
diet records from men and women show no significant difference in the ratio of
CHO:fats:protein (Roepstorff et al. 2002; Timmons et al. 2005; Devries et al. 2006;
Tarnopolsky et al. 2007; Fu et al. 2009; Maher et al. 2010b). Dietary intake prior to
testing should also be controlled by administering an isocaloric (kcal/kg) meal at the
same time as pre-exercise in both men and women for the same reasons listed above.
Because the relative ratio of female sex hormones (i.e., estrogen:progesterone)
can influence substrate utilization, women should all be in the same phase of their
menstrual cycle, and menstrual irregularities such as oligoamenorrhea and amen-
orrhea must be controlled or accounted for (Nicklas et al. 1989; Campbell, Angus
et al. 2001; Devries et al. 2006). Studies should also consider oral contraceptive use,
as oral contraceptives have a slight effect on substrate selection during endurance
exercise, with a higher glycerol rate of appearance (lipolysis) (Devries et al. 2006).
Sex comparison studies should also test men and women during the same experi-
mental time period (and not with historical data) to control for variations in meta-
bolic assessment equipment (i.e., metabolic carts) and equipment calibrations (i.e.,
calibration of gas supply), as well as the research staff responsible for subject testing.
Subjects must be in a steady state of exercise intensity and exercising below the
anaerobic threshold (<75% of VO2max in trained athletes and <65% for untrained
individuals) as sex comparisons of substrate oxidation rates exceeding the lactate
threshold do not yield accurate or valid results due to hyperventilation (inaccurate
RER), rapid fatigue, and inability to sustain the work intensity (Tate and Holtz 1998).
Taken together, it is important to consider the aforementioned factors to reduce vari-
ance and the potential to produce false conclusions regarding sex differences. The
following sections describe sex differences in CHO and fat oxidation during endur-
ance exercise and the role that estrogen plays in modulating substrate use.

SEX DIFFERENCES IN CARBOHYDRATE

METABOLISM DURING EXERCISE
Overview of Carbohydrate Oxidation
The primary substrate sources for sustaining muscle contraction during submaximal
endurance exercise are CHO and fat, with protein contributing only a small amount
Substrate Utilization in Female Athletes 5

of energy (2 to 5%) under normal circumstances (Lamont 2005). CHOs are stored in
the muscle (1 to 2% of total muscle mass) and liver (<8% total mass, 100 to 120 g)
in the form of glycogen. Glycogen provides a rapid source of energy to the cells
during exercise, particularly at intensities greater than 50% of VO2max (Powers and
Howley 1996). Glycogen stores are limited and can be depleted within a couple of
hours of prolonged exercise, depending on intensity and fiber type. The greater the
exercise intensity and the more fast twitch fiber recruitment, the more rapidly glyco-
gen will be depleted (Gollnick et al. 1974). Endurance performance can be altered
by changing habitual dietary CHO intake, increasing CHO intake prior to an event
(CHO loading), consuming CHOs during an event, and consuming CHOs immedi-
ately post-exercise, ultimately changing substrate utilization. (For more on this topic
see Chapter 2.)

Sex Differences in Carbohydrate (CHO) Oxidation

As previously mentioned, the majority of cross-sectional studies have found that
whole-body CHO oxidation rates are lower for women compared to men during
endurance exercise (running, walking, and cycling) at submaximal exercise intensi-
ties (45 to 70% VO2max), for durations ranging from 60 to 120 minutes (Tarnopolsky
2008). Moreover, these differences persist after 2 to 3 months of monitored exercise
training (Friedlander et al. 1998; Horton et al. 1998; McKenzie et al. 2000; Carter
et al. 2001a), further supporting the notion that the sex-based differences in substrate
selection are attributable to sex, and not matching issues related to unequal training
status.
The mechanism for the reduction in CHO oxidation in women is unclear. There
does not seem to be a sex difference in basal muscle glycogen content in trained or
untrained women compared with men (McKenzie et al. 2000; Tarnopolsky, Zawada
et al. 2001). This suggests that the difference in CHO utilization between men and
women likely involves an attenuation of hepatic and muscle glycogen utilization in
women. In support of this notion, several studies have shown that the rate of glucose
appearance (Ra) and disappearance (Rd) was lower in women compared with men
(Roepstorff et al. 2002; Devries et al. 2006; Horton et al. 2006). In one particular
study, the A-V (arteriovenous) balance method was used to examine substrate use
across the leg during 90 min of bicycle exercise at 58% of VO2max in seven endur-
ance-trained men and women (Roepstorff et al. 2002). The results indicated that
the glucose rate of appearance into the blood from the liver was lower for women
(Roepstorff et al. 2002), suggesting that at least some of the sparing of CHO oxida-
tion in women must involve the liver.
Sex differences in CHO utilization may be due to upstream biological factors such
as glucagon, epinephrine, and sex hormones. Glucagon is a hormone secreted by the
pancreas that stimulates liver and muscle glycogenolysis and release of glucose from
the liver to maintain blood glucose levels. Horton et al. (2006) and Tarnopolsky et
al. (1990) reported that men had a greater reduction in blood glucagon levels during
exercise compared with women (Tarnopolsky et al. 1990; Horton et al. 2006). If the
liver takes up glucagon (binds receptors or is internalized into the cells) in order to
promote glycogenolysis, then these results could suggest that glucagon may partially