Journal of the International Society of Sports Nutrition

ISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/rssn20

International society of sports nutrition position
stand: nutritional concerns of the female athlete
Stacy T. Sims, Chad M. Kerksick, Abbie E. Smith-Ryan, Xanne A.K. Jansede Jonge, Katie R. Hirsch, Shawn M. Arent, Susan Joyce Hewlings, Susan
M. Kleiner, Erik Bustillo, Jaime L. Tartar, Valerie G. Starratt, Richard B.
Kreider, Casey Greenwalt, Liliana I. Rentería, Michael J. Ormsbee, Trisha A.
VanDusseldorp, Bill I. Campbell, Douglas S. Kalman & Jose Antonio
To cite this article: Stacy T. Sims, Chad M. Kerksick, Abbie E. Smith-Ryan, Xanne A.K. Janse deJonge, Katie R. Hirsch, Shawn M. Arent, Susan Joyce Hewlings, Susan M. Kleiner, Erik Bustillo,
Jaime L. Tartar, Valerie G. Starratt, Richard B. Kreider, Casey Greenwalt, Liliana I. Rentería,
Michael J. Ormsbee, Trisha A. VanDusseldorp, Bill I. Campbell, Douglas S. Kalman & Jose
Antonio (2023) International society of sports nutrition position stand: nutritional concerns of
the female athlete, Journal of the International Society of Sports Nutrition, 20:1, 2204066, DOI:
10.1080/15502783.2023.2204066
To link to this article: https://doi.org/10.1080/15502783.2023.2204066© 2023 The Author(s). Published by Informa
UK Limited, trading as Taylor & Francis
Group.

Published online: 24 May 2023.

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JOURNAL OF THE INTERNATIONAL SOCIETY OF SPORTS NUTRITION
2023, VOL. 20, NO. 1, 2204066
https://doi.org/10.1080/15502783.2023.2204066

International society of sports nutrition position stand:nutritional concerns of the female athlete
Stacy T. Sims a, Chad M. Kerksick b, Abbie E. Smith-Ryan c, Xanne A.
K. Janse de Jonge d, Katie R. Hirsch e, Shawn M. Arent e, Susan Joyce Hewlings
Susan M. Kleiner g, Erik Bustilloh, Jaime L. Tartari, Valerie G. Starratti,
Richard B. Kreider j, Casey Greenwaltk, Liliana I. Renteríak, Michael J. Ormsbee k,
Trisha A. VanDusseldorp l,m, Bill I. Campbell n, Douglas S. Kalman o
and Jose Antonio p

f

,

a

SPRINZ Auckland University of Technology, Auckland, New Zealand; bExercise & Sport Nutrition Lab,
Department of Kinesiology and Sport Management, Saint Charles, TX, USA; cInstitute of Sports Sciences andMedicine, Florida State University, Nutrition and Integrative Physiology, Tallahassee, FL, USA; dLLC p/b JDS
Therapeutics, Bonafide Health, Harrison, NY; eJacksonville University, Department of Health and Exercise
Sciences, Jacksonville, FL, USA; fUniversity of South Florida, Performance and Physique Enhancement
Laboratory,Tampa, FL, USA; gDr. Kiran C Patel College of Osteopathic Medicine, Nova Southeastern
University, Nutrition Department, Davie, FL, USA; hNova Southeastern University, Exercise and Sport Science,Fight Science Lab, Davie, FL, USA; iCollege of Science, Technology,and Health, Lindenwood University,
Exercise and Performance Nutrition Laboratory, St Charles, MO, USA; jUniversity of North Carolina Chapel
Hill, Department of Exercise and Sport Science, Chapel Hill, NC, USA; kMacquarie University, Department of
Health Sciences, Macquarie Park, NSW, Australia; lUniversity of South, Department of Exercise Science,
Arnold School of Public Health, Carolina, Columbia, USA; mNutrasource, Guelph, Ontario, Canada; nHigh
Performance Nutrition LLC Mercer, Island, WA, USA; oErik Bustillo Consulting, Miami, FL, USA; pNova
Southeastern University, Department of Psychology and Neuroscience, Fort Lauderdale, FL, USA
ABSTRACTARTICLE HISTORY

Based on a comprehensive review and critical analysis of theliterature regarding the nutritional concerns of female athletes,
conducted by experts in the field and selected members of theInternational Society of Sports Nutrition (ISSN), the following
conclusions represent the official Position of the Society: 1.
Female athletes have unique and unpredictable hormone pro­files, which influence their physiology and nutritional needs
across their lifespan. To understand how perturbations in these
hormones affect the individual, we recommend that female ath­
letes of reproductive age should track their hormonal status(natural, hormone driven) against training and recovery to deter­mine their individual patterns and needs and peri and postmenopausal athletes should track against training and recovery
metrics to determine the individuals’ unique patterns. 2. The
primary nutritional consideration for all athletes, and in

Received 9 February 2023
Accepted 29 March 2023
KEYWORDS

Female athlete; Menstrual
cycle; Hormonal
contraceptive; Menopause;
Nutrition; Exercise

CONTACT Stacy T. Sims
stacy@drstacysims.com
SPRINZ Auckland University of Technology, Auckland, New
Zealand; Abbie Smith-Ryan
abbsmith@email.unc.edu
Institute of Sports Sciences and Medicine, Nutrition andIntegrative Physiology, Florida State University, Tallahassee, FL, USA; Chad M. Kerksick
ckerksick@lindenwood.edu
Department of Kinesiology and Sport Management, Exercise & Sport Nutrition Lab, Saint Charles, TX, USA© 2023 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (http://
creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium,provided the original work is properly cited. The terms on which this article has been published allow the posting of the AcceptedManuscript in a repository by the author(s) or with their consent.

JOURNAL OF THE INTERNATIONAL SOCIETY OF SPORTS NUTRITION

particular, female athletes, should be achieving adequate energy
intake to meet their energy requirements and to achieve an
optimal energy availability (EA); with a focus on the timing ofmeals in relation to exercise to improve training adaptations,performance, and athlete health. 3. Significant sex differences
and sex hormone influences on carbohydrate and lipid metabo­lism are apparent, therefore we recommend first ensuring ath­
letes meet their carbohydrate needs across all phases of themenstrual cycle. Secondly, tailoring carbohydrate intake to hor­monal status with an emphasis on greater carbohydrate intake
and availability during the active pill weeks of oral contraceptive
users and during the luteal phase of the menstrual cycle where
there is a greater effect of sex hormone suppression on gluco­
nogenesis output during exercise. 4. Based upon the limited
research available, we recommend that pre-menopausal, eume­
norrheic, and oral contraceptives using female athletes should
aim to consume a source of high-quality protein as close to
beginning and/or after completion of exercise as possible toreduce exercise-induced amino acid oxidative losses and initiate
muscle protein remodeling and repair at a dose of 0.32–0.38
g·kg−1. For eumenorrheic women, ingestion during the luteal
phase should aim for the upper end of the range due to thecatabolic actions of progesterone and greater need for aminoacids. 5. Close to the beginning and/or after completion of
exercise, peri- and post-menopausal athletes should aim fora bolus of high EAA-containing (~10 g) intact protein sources or
supplements to overcome anabolic resistance. 6. Daily protein
intake should fall within the mid- to upper ranges of current
sport nutrition guidelines (1.4–2.2 g·kg−1·day−1) for women at allstages of menstrual function (pre-, peri-, post-menopausal, andcontraceptive users) with protein doses evenly distributed, every
3-4 h, across the day. Eumenorrheic athletes in the luteal phaseand peri/post-menopausal athletes, regardless of sport, should
aim for the upper end of the range. 7. Female sex hormones
affect fluid dynamics and electrolyte handling. A greater predis­
position to hyponatremia occurs in times of elevated progester­one, and in menopausal women, who are slower to excretewater. Additionally, females have less absolute and relative fluid
available to lose via sweating than males, making the physiolo­
gical consequences of fluid loss more severe, particularly in theluteal phase. 8. Evidence for sex-specific supplementation is lack­ing due to the paucity of female-specific research and any differ­ential effects in females. Caffeine, iron, and creatine have themost evidence for use in females. Both iron and creatine arehighly efficacious for female athletes. Creatine supplementationof 3 to 5 g per day is recommended for the mechanistic supportof creatine supplementation with regard to muscle protein
kinetics, growth factors, satellite cells, myogenic transcription
factors, glycogen and calcium regulation, oxidative stress, andinflammation. Post-menopausal females benefit from bonehealth, mental health, and skeletal muscle size and function
when consuming higher doses of creatine (0.3 g·kg−1·d−1). 9. To
foster and promote high-quality research investigations involving
female athletes, researchers are first encouraged to stop exclud­ing females unless the primary endpoints are directly influenced

391

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S. T. SIMS ET AL.

by sex-specific mechanisms. In all investigative scenarios,
researchers across the globe are encouraged to inquire andreport upon more detailed information surrounding the athlete’s
hormonal status, including menstrual status (days since menses,
length of period, duration of cycle, etc.) and/or hormonal contra­
ceptive details and/or menopausal status.

1. Methods
The International Society of Sports Nutrition (ISSN) position stands are invited papers on
topics the Journal of the ISSN (JISSN) Editors and Research Committee identifies as beingof interest to JISSN readers. The process consists of editors and/or the ISSN ResearchCommittee identifying a lead author or team of authors to perform a comprehensive
literature review. Specifically, for this Female Athlete Position Stand, the scientific designof the studies was scrutinized for scientific validity [1, 2] as part of the inclusion criteria.
After the authors develop the content of the position stand, the draft is sent to leading
scholars in the field for a detailed review. Following a critical review by the scholars, thepaper was revised by a team of authors, approved by the ISSN Research Committee and
JISSN Editors, and published as a consensus statement and the official position of the ISSN
on the topic.

2. Introduction
As even a cursory review of the history of scientific advancement would reveal, thebiomedical community has long failed to give due deference to the importance of sex
differences in human physiology. Males have routinely been considered the exemplar bywhich all measures and standards were set. The issue of male bias goes far and theliterature is rife with examples of science that ignored women [3], even when womenshould have been a target demographic. For example, in the mid-1960’s observation thatwomen tend to have lower rates of cardiovascular disease until their estrogen levels
dropped after menopause spurred researchers to investigate whether hormone supple­
mentation was an effective preventive treatment. The study enrolled 8,341 men and no
women [4]. Similarly, the Multiple Risk Factor Intervention Trial (MRFIT) investigateddietary modifications and exercise to prevent cardiovascular disease, enrolling 13,000
male subjects and no women [5]. Given the significant sex differences from biology to
behavior, excluding females means one cannot assume that any findings would apply tofemales. Moreover, it is possible that by doing a sex-based analysis, scientific break­throughs could occur that could be important for all people by understanding how
certain interventions vary by sex. Fortunately for all active females, the opportunities forathletic endeavors and the body of female-centric human performance research arequickly expanding. However, female-centric research studies and female subject numbers
still lag significantly behind males [3,6].
While health and human performance research does target women, the focus of that
research is often the influence of the menstrual cycle. One of the earliest publications
regarding menstruation and physical activity was written in 1877 by Mary Putnam Jacobi,

JOURNAL OF THE INTERNATIONAL SOCIETY OF SPORTS NUTRITION

393

M.D., entitled “The question of rest for women during menstruation” [7]. The assumptions
made from these early writings are still prevalent today that physical activity might impair
reproductive function and harm the health of females. Thus, females were restricted frommost organized, high intensity physical activity and sport. The study of the female
menstrual cycle as it relates to sport performance began in earnest in 1953 and, as oftoday, ~400 studies on this topic have since been published [8]. Compared to males, thescientific design around the menstrual cycle has been deemed “complex” thus has been
an obstacle to developing and funding high numbers of research studies. Yet, despite theobvious endocrinological differences between the sexes and the growing interest in
menstrual cycle-specific research [9], exercise science and nutrition research continue togeneralize results from male data to women [10]. Recent guidelines have been publishedon the scientific design and methodology relevant to the study of women’s exercise
performance and nutrition [1,2,11]. Critically, these guidelines provide recommendations
on the conditions under which female sex hormones need to be considered [1,8,11]. This,
along with women’s increased individual interest in approaching peak mental andphysical performance has resulted in a growing body of research that addresses theseissues across the lifespan [12,13]. The aim of this position stand is to review this researchand provide practical evidence-based female-specific recommendations for sport
nutrition.

3. Overview of sex differences
The terms “sex” and “gender” have come to be used synonymously in the sport andexercise literature. However, there are two distinct concepts that should not be usedinterchangeably. “Sex” generally refers to the distinction between females and males
based on reproductively relevant differences in chromosomes, primary and secondary sex
characteristics, and endogenous hormonal profiles. “Gender” can refer to several things,
including one’s self-perceived identity as a woman, man, or otherwise – a trait, which is atleast partly biologically based and inherent to a person; one’s outward expression of one’s
gender identity – in terms of one’s appearance and other behaviors; and the role one is
expected to play in society based on one’s sex or gender identity – the specifics of which
can vary across sociocultural circumstances. While discussions of gender are certainly
relevant to the athletic community at large, the specific issue of nutrition among female
athletes will be better informed by a restriction of the current discussion to sex andhuman sexual differentiation.
Sex chromosome genes and sex hormones, including estrogen, progesterone, and andandrogens, contribute to the differential responses between the sexes. Following birth,
significant prepubertal differences exist between the structure and function of otherorgan systems in boys and girls, which are eventually further emphasized by hormone
activity and driven by a sex-specific reactivity to environmental stimuli, including nutri­ents and the diet in general. Although difficult to separate from the hormonal influences,
important sex differences exist in mitochondrial function [14–16], substrate utilization,and insulin sensitivity [17–24], immune responses [25–28], muscle morphology and bodycomposition [29–32], iron metabolism [33–40], thermoregulation [41–44], hydration[45,46]{Sims, 2008 #55, [47–53], appetite control [54–59], and energy availability andendocrine function [60–65].

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S. T. SIMS ET AL.

3.1. Female sex hormones and differential hormone profiles
The primary female sex hormones are 17β estradiol (E2), the predominant endogenous
estrogen in humans, and progesterone. Both hormones exert agonistic and antagonistic
effects on metabolism and nutrient needs whereby the ratios and levels of estradiol andprogesterone affect the proportions of macronutrients used as fuel, not only at rest but
also during exercise. Estrogen actions in hypothalamic nuclei differentially control foodintake, energy expenditure, and white adipose tissue distribution [22,66,67]. Estrogenactions in skeletal muscle, liver, adipose tissue, and immune cells are involved in insulin
sensitivity as well as prevention of lipid accumulation and inflammation [20,21,67,68].
Estrogen actions in pancreatic islet β-cells also regulate insulin secretion, nutrient home­ostasis, and survival [66,69,70]. Less is known of the specific mechanisms of metabolic
influences of progesterone. However, progesterone has direct effects on energy expen­
diture through a progesterone-mediated increase in metabolic rate [71–73]; alters serum
electrolyte balance through progesterone-mediated increases in aldosterone [74–77];
functions catabolically to increase amino acid oxidation and decreases muscle protein
synthesis [78–81], and affects glucose metabolism through the upregulation of GLUT1
expression to increase endometrial glycolytic metabolism, attenuating skeletal and hepa­
tic glycolytic pathways [82–85].
To better understand the potential effects of female sex hormones on metabolism andnutrient needs of female athletes, it is important to be aware of the many different
hormonal environments a female athlete of reproductive age could be experiencing.
For those athletes not using hormonal contraceptives (see the next section), this canrange from amenorrhea (absence of menstrual cycle) to oligomenorrhea (menstrual cycle
longer than 40 days, so less than 9 cycles per year) to naturally menstruating (menstrual
cycle length between 21 and 40 days). And within the naturally menstruating women
hormone fluctuations vary as a result of ovulatory cycles (eumenorrheic), as well as
menstrual cycles with anovulation or luteal phase deficiency [2].
The menstrual cycle (MC) and its systemic effect on the body is a crucial area forresearch, as it has been found that women [1] frequently experience different adaptations
and stress responses to their male counterparts [86,87]. For eumenorrheic women, the MC
is characterized by fluctuations in several hormones, most notably the gonadal steroids,
estrogen and progesterone, and is partitioned into the following phases: early follicular(EF), mid-follicular (MF), late follicular (LF), ovulation, early luteal, mid-luteal (ML), and lateluteal phases (Figure 1). Throughout each phase, fluctuations in hormones trigger not
only changes in the reproductive system but also in all the tissues of the body, which canhave a direct effect on stress resilience, metabolism, and adaptations [1,88]. As a brief
review, the length of a normal menstrual cycle is 21 to 40 days [89]. The first half of the MC
is comprised of the menstrual and follicular phases during which time estrogen levels arelow (early follicular/menstrual), then rise (mid follicular) and peak (late follicular) and ends
with the periovulatory phase in which follicular-stimulating hormones and luteinizing
hormones reach peak concentrations. After ovulation, the second half of the cycle iscomprised by the early luteal (during which time estrogen level drops and then rises while
progesterone rises), the mid-luteal (during which time estrogen and progesterone levelspeak), and finally, the late luteal phase (during which time estrogen and progesterone

JOURNAL OF THE INTERNATIONAL SOCIETY OF SPORTS NUTRITION

Estradiol (pmol/L)

1000

MidLate
Early
Follicular Follicular Luteal

EF

MF

LF

MidLuteal

Late
Luteal

ML

LL

EL

50

800

40

600

30

400

20

200

10

0

-14 -12

-10

-8

-6

-4

-2 OVU

Progesterone (nmol/L)

Early
Follicular

395

0
2

4

6

8

10

12

14

Day of menstrual cycle
Figure 1. Diagram illustrating the menstrual cycle phases in a typical 28-day cycle. (from Oosthuyse
et al [9]).

levels fall). These cyclic hormone changes can affect a number of physical and psycholo­
gical attributes and, ultimately, may influence sports performance, although the effects
are highly individual [88,90,91].

3.2. Hormonal contraceptives
Many female athletes decide to use hormonal contraceptives for various reasons [92].
Hormonal contraceptives (HC) contain derivatives of estrogens and progestogens, which
downregulate the regular cyclic hormone activity of the hypothalamic-pituitary-gonadalaxis, resulting in physiological responses that differ to those of endogenous ovarian
hormones [88,93]. Ethinyl estradiol (EE) and mestranol are the two estrogens used (withethynyl estradiol being much more frequently used), and several progestogens are
currently used [94]. A full overview of the different formulations and mechanism ofactions of HCs is out of scope of this position stand, thus the reader is referred to
Regidor [94,95] and Benagiano [96] for in-depth detail.
Effects of synthetic/exogenous hormones on different systems of the body may require
close consideration for the practitioner and athlete. For example, endogenous estrogenand progesterone have antagonistic effects on fluid balance: estrogens activate the renin–
angiotensin system, stimulating the production of angiotensinogen and leading to higher
levels of angiotensin, aldosterone, and sodium in plasma (sodium retention) [52], thus
resulting in increased water retention. On the other hand, progesterone is a potent
aldosterone antagonist [47], which stimulates the mineralocorticoid receptor preventing
sodium retention. However, in OCs, the progestogens are insufficient to counteract thesodium-retaining effect of the estradiol component; consequently, the estradiol compo­
nent causes fluid retention [97]. Further, Suh, Casazza et al. [98] examined the effects oforal contraceptives (OC), using a longitudinal design, on glucose flux and whole-bodysubstrate oxidation rates during rest (90 min) and two exercise intensities [60-min leg
ergometer cycling at 45% and 65% peak O2 uptake (V˙O2 peak)]. OCs significantly

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S. T. SIMS ET AL.

downregulated glucose flux during exercise, with exogenous hormones having a greater
effect on exercise glucose metabolism than endogenous hormones. Thus, exogenous
hormones might moderate physiological adaptations and nutritional needs in a different
manner to endogenous ovarian hormones [98].
The vaginal bleeding patterns associated with continuous estrogen – progestogen(combined oral contraceptive/COC) or progestogen-only contraceptive (progestin-onlypill; intrauterine device [IUD]; implants, injections) regimens are quite different fromspontaneous cyclical menstrual patterns. Women using COC are subject to a different 28day cycle wherein a 21-day intake period, characterized by constant daily doses ofa synthetic estrogen (estradiol or mestranol) and one of four generations of a synthetic
progesterone (termed progestin) is followed by a 7-day break inducing a withdrawal
bleed (often mistaken for a real menstrual bleed) [99]. This leads to a regular patternwhereby synthetic hormone levels are high during the 21-day intake period and low
during the 7-day pill break. Two major COC formulations are available: the monophasic,
whereby the dosage of estrogen and progestin do not change across the active pill cycles;or multiphasic, whereby the dose of hormones varies across the active pills, particularly
the progestin. The progestin provides most of the contraceptive effect and the genera­tion, type, and dosage of the exogenous progestin determines the potency and andro­
genicity (e.g. Norethindrone is a first-generation drug with weak progestin changes,
whereas Norgestrel and Levonorgestrel are second-generation drugs that are designed
to be more potent than the 1st generation approaches and subsequently have greater
androgenicity) [1,100,101]. The mechanism of action of the exogenous hormones is tocause ovarian suppression, preventing the surge of luteinizing hormone (LH) and ovula­tion. It is important to understand that the many different types and generations of COC
formulations mean that the sparse research available in women using COC is applicable tothat type of COC and not to all COC in general.
Alternatively, progestin and copper intrauterine devices (IUDs) do not inhibit ovulation
but reduce endometrial hyperplasia, resulting in an inhospitable environment for implan­tation [102]. Importantly, only orally administered steroids undergo hepatic first-passmetabolism; thus, the localized progestin of the IUD exerts different metabolic effects
as compared to the progestin of the COC with no changes in body composition or bodymass [103]. A full review of the types and mechanisms of action for IUDs is beyond thescope of this paper and has been written elsewhere [104–106]. Although research islacking regarding the impact of COC and IUD on metabolism and nutritional require­ments, understanding the hormonal implications can help to draw inferences fromresearch in eumenorrheic women.

3.3. Peri and post menopause
The menopausal transition, or perimenopause, is associated with profound reproductive
and hormonal changes. A time-related change in the character of menstrual cycles asmenopause approaches is well established, with an increasing proportion of cycles
observed with prolonged follicular phases that may exhibit delayed ovulatory cycles orno ovulatory cycle altogether. Hormonal patterns during the luteal phase of the menstrual
cycle also show changes with age, with greater absences of ovulatory cycles, while
reductions in luteal phase progesterone become more common [107–109]. The reduction

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397

in progesterone impacts the ratio of estradiol: progesterone (E:P), invoking an imbalance,
illustrated by anabolic resistance of muscle protein synthesis, insulin resistance, increased
abdominal adiposity, decreased lean mass, a reduction in bone mineral density, anda decrease in energy expenditure [110,111]. The majority of body composition changes
occur in the four to five years leading up to menopause (commonly defined as a period oftime of 12 months of no menses), after which body composition changes are more agerelated, rather than hormone-related [112]. By understanding the influence of hormone
shifts on physiological parameters of female athletes during menopause transition, nutri­tional recommendations to improve insulin sensitivity as well as to support lean mass andbone density may positively enhance body composition, health, and performance.

4. Energy requirements: intake and availability
Energy is required by the human body for a variety of metabolic processes and physio­
logical functions including muscular activity, heat production, nutrient and cellular trans­
port, biological growth, and synthesis of cell components and new tissues. Thus, a primarynutritional consideration for female athletes should be achieving adequate energy avail­ability (EA). EA is defined as the energy available for metabolic processes, after accounting
for dietary energy intake and physical activity energy expenditure [61,113]. Specifically,
the EA is defined as dietary energy intake (EI) minus exercise energy expenditure (EEE)
corrected for fat-free mass (FFM) relative to total body mass [65,114]. It is widely acceptedthat sufficient energy is crucial for training consistency, particularly during intensified
periods, as prolonged energy restriction can lead to impaired physiological function,
maladaptation to prescribed training, and an increased risk of fatigue, illness, and injury[61,64,114–116]. In both sexes, energy homeostasis is under the control of a variety ofhormones secreted from the gut, pancreas, adipose tissue, and gonads.
In this respect, the sex hormones are the primary sources of sex differences as it
pertains to regulation of energy intake [117]. Estrogen, a primarily female hormone,
reduces food intake and body weight and exerts an effect on meal size [118] andfunctions in conjunction with other circulating factors such as leptin and ghrelin toexert tonic inhibition of food intake [119]. During the late follicular phase of the menstrual
cycle, estrogen is high, while progesterone concentration is low. It is during this phasethat resting metabolic rate (RMR) and energy intake are lowest. Conversely, during the
mid-luteal phase of the menstrual cycle, both estrogen and progesterone concentrations
increase and reach a peak [58]. Accordingly, resting metabolic rates increase, while energy
intakes are commonly at their highest levels [59,120]. For example, Barr et al. [121]estimated that free living energy intake increases ~ 300 kcal/day during the luteal
phase of the menstrual cycle in recreationally active females.

4.1. Low energy availability
Low energy availability (LEA) is the underlying etiology of relative energy deficiency insport (RED-S) [114] and occurs when energy intake is less than energy expenditurethrough exercise. As a result, the body does not have enough energy left to appropriately
sustain physiological functions outside of exercise [63,64]. Research that investigates theeffects of LEA typically falls into two categories: socio-psychological and physiological.

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Athletes are at a greater risk for LEA from sociocultural pressures, such as social media
pressures, pressures from coaches/teammates/self to look a certain way, or from theprevailing belief that a lower body weight will result in greater performance outcomes[122–125]. Intentional dietary behavior modifications to achieve a certain sport esthetic
may be a driver for LEA, however many athletes may unintentionally fall into LEA duringphases of increased training volume or in sports with high energy expenditure[113,114,126]. Briefly, the known consequences of LEA cause a myriad of complications,which include reproductive dysfunction and impairments to skeletal, cardiovascular,
gastrointestinal, endocrine, and neurological function [113,115,127,128]. Whether inten­
tional or not, LEA may have significant detrimental effects on health and performance,
both in endurance and strength-power athletes. Reviews of the current knowledge ofhealth and performance impairments related to LEA and RED-S are discussed in detailelsewhere [114,126,129,130].
Nutrient sensing pathways are also sensitive to circulating estrogen; specifically, theregulation of hypothalamic kisspeptin neurons and the metabolic regulation of KISS1 gene
expression and release. Kisspeptin is a neuropeptide involved in the regulation of repro­
ductive function and also has a significant role in the regulation of glucose homeostasis,
feeding behavior, and body composition [131]. The threshold for downregulation of
kisspeptin signaling of gonadotropin-releasing hormone (GnRH) neurons has a greater
sensitivity in females than in males [132], Thought to be primarily due to sex differencesin the density of kisspeptinARC and kisspeptinAVPV/PeN neurons, kisspeptinAVPV/PeN neurons
are also almost exclusive to the female brain [133]. Estrogen increases expression of KISS1 inkisspeptinAVPV/PeN and downregulates the expression in kisspeptinARC promoting a decreasein energy intake. Importantly, when energy deficits occur, through undernutrition orexcessive energy expenditure, the KISS1 gene is downregulated resulting in subsequent
repression of the GnRH neurons and downregulation of the reproductive axis [134,135].
Exercise induced energy deficits as a means to promote fat loss are more effective inmen than in women [136,137]. This may be attributed in some respect to a sex disparity
between the way exercise alters energy-regulating hormones and appetite. Hagobian andcolleagues [57] demonstrated that in response to moderate-intensity continuous exercise
with an uncompensated energy deficit, naturally menstruating women have higher
concentrations of acylated ghrelin and lower concentrations of insulin, both of which
stimulate energy intake. When the energy deficit was addressed, the patterns of acylated
ghrelin and insulin were attenuated, but still persisted. In contrast, ghrelin concentrations
did not change in men, regardless of energy status, along with a slight reduction of insulin
in the energy deficit condition but not in energy balance [138]. In a follow-up study, anacute bout of moderate intensity aerobic exercise did not exert the same effects onghrelin and insulin for women using a monophasic COC and the participants maintained
an energy deficit after exercise (i.e. did not increase energy intake to match or exceed
exercise expenditure) [139]. Therefore, in women, higher acylated ghrelin and lower
insulin/leptin concentrations in response to physical activity may be a mechanism to
oppose energy deficit, defend body fat stores, and preserve reproduction function.
However, considering that the primary mechanism of action for many of COCs is tosuppress ovulation via the inhibition of the hypothalamic–pituitary–adrenal (HPA) axis,
hypothalamic responses to exercise and energy deficiency may be attenuated with theuse of COCs [114]. Therefore, the identification of LEA in athletes using COCs can be

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399

masked, reducing practitioner and athlete ability to treat and/or prevent longer term
implications of LEA.

4.2. Recommendations for prevention and treatment of LEA
Specific guidelines for an optimal EA for competitive female athletes have not been
established, but conceptual models of energy availability thresholds have been pro­
posed from well-controlled laboratory studies [63–65]. An EA of at least 45 kcal kg−1
FFM·day−1 appears to be a threshold to ensure optimal EA for physiological functions
and body mass maintenance in female athletes [124]. An EA > 45 kcal kg−1 FFM·day−1
provides enough energy for weight gain and muscle hypertrophy. In clinical studies, it
has been established that EA of 30 kcal kg−1 FFM·day−1 is the threshold at and below
which suppressed metabolic hormones and reductions in luteinizing hormone pulsa­
tility is observed after as little as 5 days in healthy females [64,65,129,140,141].
Planned periodization of changing EA status may be advantageous to attenuate thenegative consequences of LEA and achieve optimal body composition and power-toweight ratios for competition [142]. Continuous workload monitoring throughout theseason also plays an important role in assessing stress and recovery needs, as highenergy expenditure, high stress, and caloric needs often occur in the pre-season(lower fitness) and again during high travel and competition blocks [143–145]. In
addition, blood biomarkers, such as cortisol, creatine kinase (CK), sex hormones,
cytokines, hematological panels, and nutrient markers can be used to detect physio­
logical responses to overall stress and identify balances between training, recovery,
and performance outcomes [146–149]. Established EA thresholds may not be appro­
priate for reducing the risk of LEA in aging women due to the changing ratios of
estrogen and progesterone in perimenopause, the subsequent absence of estrogenand progesterone in menopause and the known biological impact on resting meta­
bolic rate and body composition [150]. As such, reducing the discrepancy between
training energy expenditure and energy intake, with careful attention to nutrient
timing, should be considered [151].
EA is likely to vary between training days (as a function of EEE), and it is the within-day
periods of low energy intake over 24-hours that are associated with negative healthindices and body composition changes despite optimal daily EA values [62,152].
Research has demonstrated that females with menstrual dysfunction exhibit greater
elevations in cortisol and decreases in RMR and estradiol the longer they delay nutrition
intake, post-exercise [62]. Of importance, nutrient timing has been proposed to havea significant impact on attenuating increasing health, exercise training, and recovery
implications [153]. It is important to point out that quantification of EA in free-living
athletes can be difficult and may have a wide margin of error. To determine the EA, thecalculation requires accurately measured FFM, EI and exercise EE of the athlete, in which
errors of validity and reliability will undoubtedly occur [150]. Moreover, non-purposefulphysical activity expenditure needs to be included to accurately reflect perturbations inenergy availability. Therefore, EA thresholds should be used to guide nutritional strategies
in which the individual’s training load, nutrient timing, and manipulation of macronu­
trients to ensure recovery and adaptation are the forefront of the athlete’s nutritional
plan.

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4.3. Key recommendations● The primary consideration for female athletes, regardless of hormonal status, is tomaintain an overall EA level that meets the specific goals and requirements of theirindividual training and performance demands.
● Due to the increased energy needs in the luteal phase of the menstrual cycle,
eumenorrheic athletes may consider increasing overall 24-h energy intake in thisphase.
● COC use can mask early signs of LEA, reducing the opportunity to identify LEA andprevent further implications.
● Specific attention to nutrient timing in relation to exercise may help to reduce timespent in a catabolic state and as a result improve health, performance, and asso­
ciated exercise training adaptations even in times of planned caloric deficit.
● It is acknowledged that at various points in the training cycle, a caloric deficit isdesired for optimizing body mass and composition, however, athletes and coachesof female athletes must understand the repercussion on the greater neuroendocrine
responses to low nutrition density.
● Monitoring biomarkers across training blocks and athletic seasons can provide
further insight into the balance between training, recovery, and performanceoutcomes.

5. Sex hormone effects and substrate metabolism
Robust evidence exists that demonstrates the important roles estrogen and progesterone
have in regulating substrate metabolism [20,24,66,70,80,82,84,154–159]. Estrogen, speci­
fically 17β-estradiol, promotes lipolysis and increases fatty acid availability while decreas­
ing the rate of gluconeogenesis with muscle and liver glycogen sparing. Although 17βestradiol lowers mitochondrial membrane viscosity (which creates a more fluid lipid
bilayer and facilitates movement and function of membrane proteins), Miotto and col­leagues [14] demonstrated that female skeletal muscle has a greater abundance of thefatty acid transporter CD36, a sex difference that results in a greater membrane transloca­
tion of the CD36 protein during muscle contraction that helps to explain the heightened
rates of lipid metabolism, which occur in females when compared to males during
exercise [160,161]. Further, these actions are independent of hormone influences andfurther promote carbohydrate sparing and higher lipid oxidation during exercise[155,162,163].
Progesterone decreases the sensitivity of IGF-1 mediated uptake of glucose into
skeletal muscle, but upregulates GLUT-4 and GLUT-1 translocation to enhance glycogenstorage in the endometrial tissue for embryonic support [84]. Progesterone also appears
to accentuate the carbohydrate-sparing actions of estrogen by decreasing hepatic glyco­
genolysis [157]. Progesterone also exerts influence over protein metabolism, specificallyduring the luteal phase, which corresponds with the previously observed increases inprotein oxidation at rest and during exercise at this time in the menstrual cycle [81,164].
This increase is attributed to a greater concentration of progesterone (lowered ratio of E:
P). The primary action of progesterone is to increase the net rate of protein catabolism
through enhancement of plasma-free amino acid utilization by the liver, reducing plasma

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amino acid concentrations and increasing total urinary nitrogen excretion (without
aminoaciduria) [157,165] due to increased protein biosynthesis of the endometrial lining.
Due to the aforementioned hormonal effects, research has demonstrated that sex
differences and sex hormone profiles (e.g. menstrual cycle phase, hormonal contraceptiveuse) influence glucose kinetics and net protein balance, which may affect exercise
capacity and/or performance in eumenorrheic female athletes [166,167]. For eumenor­
rheic women, research has demonstrated a lower rate of glucose appearance, disappear­
ance, and total glycogen utilization in the luteal phase as compared to the follicular phasewhen the energy demands of exercise are high enough to exert pressure on endogenous
glucose production (>50% VO2max) [168–171].

5.1. Sex mediated differences in carbohydrate metabolism
With respect to whole body carbohydrate (CHO) metabolism, eumenorrheic women havegenerally been observed to oxidize proportionally less CHO, more lipids, and less leucine
as compared to their male counterparts both at rest and during exercise of low tomoderately high intensities and durations [154,163,172–174]. The greater lipid oxidation
in women during submaximal exercise appears to be from adipose tissue, whereas themain source of increased fatty acid utilization at rest is from skeletal muscle [155]. Thissexual dimorphism is apparent after general adaptive changes in endurance training(decrease in muscle carbohydrate utilization and increase in lipid oxidation). In thisrespect, women utilize more lipid when compared to men and this is largely attributable
to sex-specific hormonal influences and epigenetic adaptations to endurance exercise[86,175–177]. Moreover, in response to exercise, women maintain the same level ofglycemia as men, despite having lower glucose flux [173]; indicating that women increase
glucose clearance less so than men.
Exogenous ovarian hormones appear to exert greater effects on glucose flux during
exercise than endogenous hormones, as decreases in rates of glucose appearance anddisappearance can be observed in recently fed women using combined oral contracep­
tives (COC) compared to before COC use [178]. Findings from studies investigating COC
use and substrate utilization will likely vary due to the use of different types of COC
agents, monophasic vs. triphasic and different COC formulations as described in earlier
sections of this Position Stand. Evidence shows that COCs with higher concentrations ofhormones can decrease glucose tolerance, in turn augmenting insulin resistance in adultpremenopausal women [179]. Additionally, increases in C-reactive protein levels, throughglucose tolerance testing of Olympic female athletes on COC, have been observed,
indicative of an upregulated inflammatory response [180]; with significantly higher oxi­
dative stress in female athletes using COCs than their non-COC user counterparts irre­
spective of lifestyle habits [181].
Resting muscle glycogen in eumenorrheic female athletes may be reduced during thefollicular phase [182,183] and carbohydrate loading (8.4–9.0 g.kg body weight−1.d−1) has
been shown to increase resting muscle glycogen concentration in the mid-follicular (MF)phase of the menstrual cycle [184,185]. In contrast, CHO loading using a similar pattern
and amount of carbohydrate intake during the mid-luteal (ML) phase failed to change
resting muscle glycogen concentrations [182] or only documented a modest increase(13%) [186] compared to what is generally reported for male athletes (18–47%) [185,187–

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191] or female athletes during the follicular phase (17–31%) [184,185]. It is considered thatthe increased presence of progesterone in the mid-luteal phase promotes the shuttling of
glucose into the liver, as well as upregulating GLUT-4 and GLUT-1 translocation toenhance glycogen storage in the endometrial tissue for embryonic support [84,157]. As
a result, supercompensation of glycogen in skeletal muscle and hepatic tissue may be
more difficult to attain in the mid-luteal phase without higher routine daily carbohydrate
levels due to changes in insulin sensitivity and decreased sensitivity of IGF-1 mediatedglucose uptake. Although the lower level of muscle glycogen storage in the mid-follicularphase of the menstrual cycle appears to be overcome by CHO loading, the greater
intramuscular glycogen concentrations failed to translate into improved time trial perfor­
mance [182,184].
The impact of CHO loading on the muscle glycogen content of COC users is even lessclear. At this time, it is unknown what effect CHO loading may have on muscle glycogenconcentration in female athletes taking COC with different concentrations of ethynyl
estradiol and generations of progestins. More research is needed to address these
considerations.
Achieving the high intakes of CHO (≥8 g.kg body weight−1 day−1) commonly recom­
mended for CHO loading can be difficult for women whose habitual energy intakes are<2000 kcal.d−1 [192–194], as this dose amounts to ingesting more than 70–90% of thetotal energy intake as CHO for a 60-kg woman. Thus, in view of ovarian hormone effects
on glucose kinetics and to ensure adequate carbohydrate availability is met, it is recom­
mended that all women follow the recommendation to consume a pre-exercise meal or
snack containing CHO three to four hours before beginning endurance exercise. This
recommendation is particularly prudent during the active pill weeks of COC users andduring the luteal phase of the menstrual cycle of eumenorrheic women, where there isa greater effect of sex hormone suppression of gluconeogenesis output during exercise[90,166].

5.2. Key recommendations● During all times, but especially during the follicular phase (reduced glycogen sto­rage) and times of competitive or training scenarios where absolute glycogenavailability may limit performance, eumenorrheic women should pay particularattention to consuming sufficient energy with a primary focus on consuming
enough carbohydrate to support overall health as well as the duration, intensity,and environmental factors (heat, cold, altitude) of performance.
● Women using COC should also ensure adequate carbohydrate availability across allphases of the active pill cycle to attenuate exogenous hormone-linked higher
oxidative stress.

5.2.1. Sex mediated differences in carbohydrate metabolism - during exercise
It is well documented that carbohydrate availability during exercise is ergogenic as CHO
feeding can help maintain plasma glucose and prevent hypoglycemia, spare hepatic
glycogen, and delay muscle glycogen depletion [195–198]. However, in women, estrogenand muscle metabolic effects directly reduce carbohydrate utilization due to a marked
hepatic glycogen sparing effect and insulin-mediated storage, thus indirectly shifting

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403

substrate utilization toward lipids across low to moderate intensity exercise. Moreover,there is a greater sensitivity in women to the lipolytic effects of catecholamines, thought
to be due to an exercise-mediated upregulation of β1-(lipolysis stimulating) receptors (ascompared to men) [173,199]. Recommendations for carbohydrate intake during exercise
are dependent on exercise duration, absolute intensity, environmental conditions (heat,humidity, altitude), and gastrointestinal tolerance. However, these guidelines have largely
been established from male data and generalized to women, with the acknowledgmentthat more female-centric research is needed. Based on the limited research conducted infemales, several considerations exist for female athletes to improve overall carbohydrate
availability for training, performance, and recovery. First, a diet high in carbohydrate(≥60% of daily energy intake) plus intake of exogenous carbohydrate during exercise
has shown to increase the percentage of total energy from CHO oxidation in women, withan even greater effect than seen in men [200]. This increase was not attributable toa higher percentage of exogenous carbohydrate oxidation, but, alternatively, was attrib­
uted to a smaller decrease in endogenous CHO oxidation in eumenorrheic women during
exercise [201]. Women using COC demonstrate a slightly lower reliance on exogenous
CHO oxidation as compared to non-COC users [98,179,201]. Second, females exhibit
slower gastric emptying and gut motility [202,203], a greater incidence of exerciseinduced gastroparesis as compared to males [204]. Eumenorrheic women reportedly
experience greater gastrointestinal distress across the early-follicular and late-luteal
stages of the menstrual cycle as compared to other phases of the cycle [205]. Third,
carbohydrate intake during exercise should be scaled according to the characteristics ofthe event. During sustained high-intensity sports lasting approximately one-hour, small
amounts of pre-exercise carbohydrate (~30 g) [206], enhance performance. Althoughcarbohydrate mouth rinsing has been shown to have ergogenic effects in men [207],
the same does not appear to hold true for trained female athletes, in either high intensityshort duration or resistance exercises [208,209]. As observed in studies involving males,
evidence in females also supports CHO ingestion rates of 30–60 g · h−1 of as an appro­
priate target for sports of longer duration (≥60 min) [210]. However, it has not been
established if multiple transportable carbohydrate blends at high doses (up to 90 g ·h−1) improve peak exogenous oxidation rates in females [201,211]. During the follicularphase in endurance-trained women, the greatest exogenous CHO oxidation and endo­
genous CHO sparing were observed when CHO was ingested at a rate of 60 g·h−1 with nofurther increases when the rate was increased to 90 g·h−1 [212]. Lastly, provision of a CHOelectrolyte beverage during endurance exercise in the heat attenuates immune distur­bances compared to a placebo beverage, more so in the luteal phase of the menstrual
cycle [213]. Moreover, amino acid catabolism rates appear to be reduced when CHO
supplementation was provided during exercise [214].

5.3. Key recommendations● In light of the limited data available, female athletes should track their menstrual

cycle/hormone status to identify any times of increased GI issues across the cycle andif carbohydrate dosing thresholds toward the upper limits of CHO ingestion (>60g·h−1) affect GI tolerance.

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● A realistic starting recommendation is to ingest CHO at a rate of 30-60 g·h−1 during

exercise to offset menstrual cycle effects on glucose kinetics/exercise metabolism.
This will also limit potential gastrointestinal distress, immune disturbances, andprotein catabolism.
● The major factor limiting maximal exogenous CHO oxidation is intestinal absorption.
In addition, hepatic limitations which can influence the release of CHO to systemic
circulation, energy demands of exercise, gut health, and carbohydrate tolerance tointake should all be considered when developing a carbohydrate ingestion regimen.

5.3.1. Sex mediated differences in carbohydrate metabolism - post-exercise
In the acute post-exercise recovery phase, eumenorrheic women have a greater ability tomaintain glycemia following prolonged exercise as compared with males irrespective ofmenstrual cycle phase. This is mainly due to a more immediate decrease in glucose flux atthe end of exercise in women, whereas more time is required in men to re-establish basal
glucose homeostasis [154]. Evidence indicates that during exercise tasks of similar relative
intensity and the same duration, women display a greater capacity for lipid oxidation andregain control over glycemia and glucose flux more rapidly in recovery than do men[154,155]. Additionally, metabolic perturbations of exercise are still evident 21 hours after
60–90 min of low to moderate intensity exercise in men but are no longer apparent after
3 hours in women [155,172,215].
To the authors’ knowledge, limited investigations have examined the effect of men­strual cycle phase or hormonal contraceptives on muscle glycogen resynthesis with nonein peri- and post-menopausal populations. From this limited evidence, muscle glycogenrepletion is reduced in the follicular phase when compared to the luteal phase inmoderately trained eumenorrheic women, suggesting an ovarian hormone influence on
muscle glycogen resynthesis [216]. When compared to males, muscle glycogen resynth­esis during the follicular phase of the menstrual cycle occurs at similar rates following CHO
consumption of 1.2 g·kg−1 of CHO in the acute recovery period following glycogendepleting exercise [195,217]. In addition, post-exercise supplementation (1.2 g·kg−1 of
CHO, 0.1 g·kg−1 of protein, and 0.02 g·kg−1 of fat), following four training sessions acrossa week during the follicular phase, improved time to exhaustion during endurance cyclingat 75% of VO2peak. [218]. Peri- and post-menopausal athletes should adhere to the same
recommendation as the effects of ovarian hormones are slight compared to sex differ­ences in post-exercise glycemia. Moreover, due to an increase in insulin resistanceassociated with peri and post menopause [219]; athletes in this life phase should takeadvantage of the non-insulin dependent first phase of glycogen synthesis, which lasts 30–
40 minutes if glycogen depletion is substantial [220]. In this respect, close consideration to
nutrient timing recommendations [153] should be employed as well as other strategies tomaximize glycogen recovery [221].
5.4. Key recommendations● The replenishment of endogenous glycogen stores after high volume and/or multi­

ple sessions in a 24-hour period is of the utmost importance to optimize perfor­
mance. As a result, strategies to improve carbohydrate availability can promote
positive training adaptations and health.

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405● With the limited data available, we recommend female athletes should focus on

rapid consumption of at least 1.2 g·kg−1 of CHO following prolonged exercise inorder to restore spent muscle glycogen.
● Peri and post-menopausal women should focus on rapid consumption of CHO per
above, with close consideration to nutrient timing to maximize glycogen recovery.

5.5. Sex mediated differences in protein metabolism
Skeletal muscle is viewed to be the primary reservoir for amino acids (AA), and failure todeliver adequate amino acids from the diet can challenge the body’s ability to respond todaily protein turnover, particularly muscle protein. When essential AAs are low, skeletal
muscle breakdown rates are increased resulting in a release of AAs necessary to maintainproteostasis throughout the body. In contrast, when AA levels are high, muscle protein
synthesis increases so that more AAs can be incorporated into muscle and other key
organs and tissues. As AAs are the building blocks of proteins and play an essential role in
the regulation of protein turnover, maintaining adequate protein intake is essential toensure that a balance is maintained between the rate of muscle protein breakdown (MPB)
and muscle protein synthesis (MPS) to maintain muscle mass.
To briefly review, 21 AAs are required for MPS; nine of these are essential amino acids(EAAs) as they cannot be synthesized in humans and must be supplied in the diet, while
the remaining are nonessential and can be readily made by other tissues. The anabolic
effects of AA ingestion on MPS are the result of the EAAs, specifically leucine, whichindirectly activates the mammalian target of rapamycin (mTOR); note that althoughleucine triggers the essential signaling for MPS, all AAs are necessary to increase MPS in
humans [222]. Feeding and exercise are potent stimuli for MPS, with the feeding-induced
stimulation being transient and not solely responsible for muscle protein accretion.
Exercise, primary resistance-based, enhances MPS. However, the consumption of protein
post-exercise is necessary to maximize the rates of MPS and overall stimulation of skeletal
muscle hypertrophy [223].
Although sex-based differences in protein metabolism are likely small comparedto those observed in carbohydrate and lipid metabolism, the depth of research on
female athletes is lacking. No studies are currently available that specifically address
the protein requirements of female athletes across the menstrual cycle or with theuse of hormonal contraceptives. In eumenorrheic women, evidence suggests protein
catabolism is higher at rest and following aerobic endurance exercise in the luteal
phase, when estrogen and progesterone are elevated, compared to the early folli­
cular phase when estrogen and progesterone concentrations are low[81,164,223,224]. Moreover, it has been shown that protein oxidation during exercise
appears to be greater during the mid-luteal phase [164,223] and that females require
more lysine during the luteal phase than the follicular phase [81] with a lower ability
to uptake and utilize amino acids for protein synthesis. Although the blood aminoacid profiles of COC users are shown to differ from non-users [225], the impact of
COC on protein metabolism needs at rest or in response to exercise is yet to beelucidated. The major variable in determining needs is the formulation of thecontraceptive, specifically the generation of the progestin due to differences inandrogenicity, and how this may influence skeletal muscle adaptations to training

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(e.g. first-generation progestins are derived from testosterone and have high andro­
genic activity, whereas third-generation progestins have been modified to have low
androgenic activity). OCs also reduce endogenous levels of estrogen, progesterone,
free testosterone, and insulin-growth factor-1 (IGF-1), but enhances cortisol, all ofwhich affect the degree of anabolic responses to training [92]. For example, recent
data have shown that low androgenic activity progestins impairs myofibrillar protein
FSR at rest and 24 h post-endurance exercise as compared to rates observed during
the follicular phase of eumenorrheic women, but they have no effect on myofibrillar
protein breakdown [226]. An additional study compared the effects of two different
dosages of a third-generation OC with a non-user control group on resistancetraining adaptations. During a 10-week supervised progressive resistance training
program, a 30 μg ethynyl estradiol dose from a third-generation OC was associatedwith a trend toward a greater increase in muscle mass and a significantly greater
increase in type I muscle fiber area compared to a 20 μg dose of ethynyl estradiol
and non-users, though no changes in muscle strength related to training were
found. This study highlights that the dosage provided by ethinyl estradiol may
also be a key variable to consider relative to the skeletal muscle adaptations thatare observed [227].
Considering that adequate dietary protein is important for supporting physiological
adaptations to exercise, understanding the effects of sex differences, hormonal status,
types of exercise, and training status is essential for supporting female athletes. Mercer
and colleagues [228] published an in-depth review that indicates the estimated average
requirement for protein intake of eumenorrheic recreationally active and/or competitive
female athletes is similar for aerobic endurance exercise (1.28–1.63 g·kg−1·day−1), resis­
tance exercise (1.49 g·kg−1·day−1) and intermittent exercise (1.41 g·kg−1·day−1), noting
these requirements are within the mid-range of current sports nutrition guidelines (1.4–
2.0 g·kg−1·day−1) [229,230]. Moreover, pre- and post-exercise protein intakes of 0.32–0.38
g·kg−1are recommended for beneficial adaptations in recreational and competitive
female athletes. As also commonly observed and recommended in males, higher protein
diets (>2.0 g·kg−1·day−1), coupled with heavy resistance training, have been shown to beimportant for maintaining lean mass and resting energy expenditure under periods ofintentional and unintentional caloric restriction [231,232], which has been shown to beprevalent among recreationally active to elite female athletes [113,124,233–236]. If female
athletes desire skeletal muscle hypertrophy, a review by Bosse and Dixon suggests that insome populations as much as a 60% increase from habitual protein intake may be needed
to support this goal [237]. High protein diets (>2.2 g·kg−1·day−1) have not resulted in any
adverse effects to bone mineral density or kidney function in healthy women [238,239].
As mentioned earlier, the timing of nutrient consumption around exercise directly
influences performance, recovery, fat oxidation, and energy expenditure [129,153].
Female athletes often follow special diets for various reasons [113,124,125,129,233]
and/or exercise in a fasted state. However, evidence indicates that for women specifically,
exercising in a fasted state can blunt fat oxidation [240], whereas exercising in a fed state
will result in a greater total daily energy expenditure and increased fat oxidation, poten­
tially improving body composition [134,135]. A recent analysis suggests that consuming
a bolus of protein (18 g protein, 2 g carbohydrate, 1.5 g fat) 1 hour prior to a single bout of
resistance exercise (4 sets at 70–75% 1RM for nine different exercises), as opposed toJOURNAL OF THE INTERNATIONAL SOCIETY OF SPORTS NUTRITION

407

consuming a bolus of carbohydrate (1 g protein, 19 g carbohydrate, 1 g fat), significantly
augments energy expenditure when protein was consumed [241].
Peri-menopausal and post-menopausal athletes will need to consider daily protein
intake at the mid to higher range (1.8–2.0 g·kg−1·day−1) of recommendations due to thedecline of estradiol and the ensuing insulin and anabolic resistance coupled with thedemands of physical activity [242–244]. Although muscle protein synthesis rates are
greater in older women at rest [245], they still experience an accelerated loss of muscle
mass around menopause [246]. This can be partly explained by a higher muscle protein
synthesis rate in postmenopausal women, which is counteracted by an upregulation ofprotein breakdown [246]. Both an upregulation of stimulatory and inhibitory muscle
growth regulatory genes in postmenopausal women compared with premenopausal
women have also been reported [245]. An effective strategy to overcome age andhormone-mediated reductions in anabolic sensitivity in older women is the combinationof resistance exercise and essential amino acid ingestion. Notably, MPS rates increased at
0–2 hours and remained elevated through 4 hours when resistance exercise was com­bined with ingestion of 6 to 10 grams of essential amino acids in older women [247,248].

5.5.1. Pre-sleep protein intake
Research suggests that at least 30% of the adults in the US obtain less than seven hours of
sleep per night [249]. Additionally, many elite athletes fall short of their sleep require­ments whereby only 3% of elite athletes reported getting enough sleep per night to feelsatisfied [250]. Further, menstruating women may be at even greater risk of sleep
deprivation throughout different phases of their menstrual cycle [251]. Multiple studies
have reported that during the luteal phase of the menstrual cycle, an increased occur­
rence of sleep disturbances and decreased sleep quality result [252–254]. However, not all
studies agree and some report no changes in sleep quality between the phases of themenstrual cycle [255,256]. Nevertheless, sleep deprivation after a hard bout of exercise,particularly in the evening, may lead to poor recovery, resulting in impaired muscle
glycogen repletion, reduced muscle damage repair, and decreased cognitive function
coupled with an increase in mental fatigue [257].
To combat these negative outcomes, data has accumulated to support the strategic
manipulation of pre-sleep nutrition to meet daily caloric and protein intake needs tosupport the recovery demands of sport. Specifically, studies that have examined pre-sleep
protein ingestion have shown efficacy in improving overnight MPS, various indices ofrecovery, and longitudinal improvements in strength and performance when consumed
after an evening bout of exercise [258]. Recently, Apweiler et al. [259] determined that ~40 g pre-sleep casein protein ingestion, did not enhance functional recovery aftera morning bout of exercise in healthy, active individuals. While no proper study has
demonstrated that the time of day for exercise is a key influence on the potential efficacy
of pre-sleep feeding strategies, it appears to be most efficacious for recovery when
consumed after an evening workout when compared to a morning workout [258–260].
Recent research indicates that consuming protein before sleep may have beneficial
responses in women, such as reduced muscle soreness and improvements in recovery,
with no changes to lipolysis or fat oxidation [261]. Some data support an increased nextmorning resting metabolic rate following pre-sleep protein ingestion; however, it isunclear if this result is positive or negative and likely depends upon the goal of the408

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athlete [261]. Additionally, there is no difference in the morning resting metabolic rate orincreases in oxygen consumption between consuming isoenergetic/isonitrogenous highprotein food (cottage cheese) versus a high-protein (casein) liquid shake [262]. It has also
been shown that consuming chocolate milk before sleep increases resting and exercise
carbohydrate oxidation, but this did not translate to improved next-morning running
performance in female athletes [261]. However, the caloric content of the chocolate milk
drink (355 ml; 180 kcal; 30 g CHO; 12 g PRO; 0 g Fat) was likely too low to have an impact
on performance some eight hours post-ingestion.
Nevertheless, very little research is available that has examined the impact of pre-sleep
nutrition on sleep quantity or quality, particularly amongst female athletes. Recent
correlations between higher carbohydrate intake in teenage females and decreased
total sleep, suggest prioritizing fats or proteins pre-sleep may be more beneficial tosleep duration [263]. Consuming foods within 4 hours of sleep, especially larger meals
higher in fat, however, may also induce heart burn [264] which may be detrimental tosleep onset. Although there is the risk of disrupted sleep with pre-sleep nutrition,
potential optimization of macronutrient distribution as well as size and timing of meals
may decrease these negative effects while allowing for improvements in recovery andperformance in women.
Pre-sleep protein ingestion has favorable outcomes in some athletes and recreationallyactive individuals but has yet to be elucidated in female athletes. Further, no data isavailable that tracks pre-sleep nutrition and internal markers of recovery such as restingheart rate or heart rate variability in athletes. These data would be intriguing due to theirclose association with next-day readiness to play while also offering insight for athletes tooptimize pre-sleep nutrition. Moreover, these markers combined with knowledge of themenstrual cycle phases may be the next major leap forward for female athlete nutrition
recommendations.

5.6. Key recommendations● Minimal research has explored the endogenous and exogenous hormonal effects on

the protein needs of female athletes.
● Pre-menopausal eumenorrheic and OC-using female athletes should aim to con­sume a source of high-quality protein at a dose of 0.32-0.38 g·kg−1 as soon after
exercise as possible to replenish any exercise-induced amino acid oxidative losses
and initiate muscle protein remodeling and repair.
● As close to the end of exercise as possible, peri and post-menopausal athletes should
aim for a bolus of high EAA (~6-10 g) containing protein food or supplement toovercome anabolic resistance.
● For women at all stages of menstrual function (pre-, peri-, and post-menopausal),daily protein intake should fall within the mid-to upper ranges of current sport
nutrition guidelines (1.8 – 2.2 g·kg−1·day−1). Eumenorrheic athletes in the luteal
phase should consider increasing intake by ~ 12% to offset the increased protein
catabolism effects of progesterone. Peri and post-menopausal women, regardless ofsport, should aim for the upper end of the range. Meal dosing should be moderate inprotein (∼0.3 g protein·kg−1) every 3 hours to maximize muscle protein repair andremodeling during prolonged (>24 h) recovery periods.

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409● Pre-sleep protein ingestion has not been elucidated as specifically beneficial for

female athletes in eucaloric states, however those in a low energy availability state
may benefit from protein, pre-sleep, to help attenuate muscle soreness and improve
recovery.

6. Special considerations
6.1. Electrolyte handling and hydration
Menstrual cycle hormones affect fluid dynamics by altering capillary permeability, vaso­
motor function, fluid regulatory hormone release, and plasma osmolality [265]. The
elevation in plasma progesterone concentration during the luteal phase inhibits aldoster­
one-dependent sodium reabsorption in the kidneys due to progesterone competing withaldosterone for the mineralocorticoid receptor.
Both estrogens and progestogens can influence neural and hormonal control ofthirst, fluid intake, sodium appetite, and sodium regulation. Additionally, sex differ­ences are present in the activity and stimulus of the cell bodies of the periventricular
nuclei and the supraoptic nuclei (located in the anterior hypothalamus), where argi­nine vasopression is synthesized [266,267]. Four studies by Stachenfeld and colleagues[48,49,53,268] and another by
Verney et al. [269] demonstrated an estrogen-associated shift to an earlier threshold in
the osmotic sensitivity of thirst and release of vasopressin, indicating a smaller increase inplasma osmolality is required to trigger vasopressin release and thirst in the brain.
Notably, this shift persists during OC use.
Additionally, thermoregulatory and cardiovascular capacity may be impaired at lower
relative magnitudes of exercise-induced dehydration in females compared with males.
Females have, on average, lower absolute total water volume as compared with males(~31 vs.~44 L) [270] even when expressed as a proportion of body mass (~49% vs. 58%)[271]. It has been suggested that the lower body water in females vs. males results ina larger proportion of a female’s total body water lost during exercise-induced dehydration.
However, there appears to be equivalent losses of plasma volume between the sexes undersimilar exercise conditions [272,273] potentially representing sex differences in the com­
partmentalization of fluids. Thus, with less total body water and blood volume in conjunc­tion with a lower proportion of total body water [274] distributed to the extracellularcompartment, as compared to males, females have less absolute and relative fluid available
to lose via sweating making the physiological consequences of fluid loss more severe [45].
Exercise-associated hyponatremia refers to a clinically relevant reduction in blood
sodium concentrations during or up to 24 hours after physical activity. This can bea result of solute (primarily sodium) loss and/or excess fluid load [275]. Women are at
greater risk for exercise-associated hyponatremia, and this risk has been primarily attrib­
uted to their lower body weight and size, excess water ingestion, and longer racing times
relative to men [276]. Variations in thirst across the menstrual cycle [277] may increase therisk of hyponatremia, during prolonged races, in one phase over another if athletes are
not accounting for alterations in fluid losses associated with perturbations across themenstrual cycle. While these factors may contribute to the greater incidence of

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hyponatremia in women, it is likely that the differential effects of female sex hormones on
sodium handling also play a role.

6.2. Menopause, aging, and hydration
Independent of menopause, aging has important effects on fluid balance. Aging is
associated with a higher baseline plasma osmolality, coupled with an age-related blunt­ing of thirst sensation during exercise (and water deprivation), the usual thirst mechanismthat occurs with a drop in fluid volume (dehydration) is impaired [278]. Older women are
slower to excrete water (as compared to younger, premenopausal women) increasing therisk of hyponatremia [279,280]. Moreover, rehydration is a slower process with aging,primarily due to slower kidney function and hormonal responses to sodium and water
flux. Estrogen-based hormone replacement therapy results in an increased basal plasma
osmolality, plasma volume expansion, and an earlier osmotic threshold for arginine
vasopressin release (e.g. 280 vs. 285 mOsmol/kg H2O), but a reduction in urine output,
resulting in greater overall fluid retention. However, the higher overall fluid retention is
not due to increased free-water retention, but rather increased sodium retention- thesynthetic estrogens inducing a reduction in sodium excretion [278,281], eliciting a slight
reduction in the hyponatremic risk.

7. Supplements
Dietary supplement use is the highest among females [282]. Research on collegiate
female athletes suggests that more than half (65.4%) are using either traditional (single
and multivitamin/mineral supplements) or non-traditional (herbals, botanicals, and otherbiologic and nutrient) sports supplements at least one time per month [283]. Recently,
a standardized audit of the literature was conducted to determine representation for thefemale athlete of recognized sports supplements [284] (beta-alanine, caffeine, creatine,glycerol, nitrates/beet juice, and sodium bicarbonate) and it was determined that there isa lack of depth and elucidation of supplement use and dosages for the female athlete.
Though the majority of dietary supplements have been evaluated primarily in men, thefollowing overview introduces potential dietary supplements that may be efficacious for
women based on physiological theory and sex-physiology [284].
Beta Alanine. The evidence for beta alanine (BA) determined potential erogenicity bydelaying the onset of both anaerobic and aerobic fatigue allowing for longer and/or more
intense training sessions, which increases the potential for greater physiological adapta­
tions and subsequent performance [285,286]. However, lower initial muscle carnosine
levels have been reported by women, suggesting women could potentially see greater
benefits as compared to men. For example, Varanoske and colleagues [287] recruited 26
recreationally active participants (13 females) for 28 days of BA (6 g·d−1) supplementation.
BA resulted in greater muscle carnosine concentration in females, yet no difference infatigue attenuation was demonstrated between the females and males. Moreover,females who have greater muscle carnosine levels from higher dietary protein intake
are able to delay fatigue compared to women who have lower carnosine levels [288].
Currently recommendations suggest that BA supplementation should not differ between
females and males, with a total dose of 4–6 g·d−1 divided into at least 1–2 doses toJOURNAL OF THE INTERNATIONAL SOCIETY OF SPORTS NUTRITION

411

increase muscle carnosine concentrations over a 4-wk timeframe [289]. For additional
details, we refer interested readers to the ISSN Position Stand on Beta Alanine [290].
However, a specific dosing regimen (amount, timing, etc.) for female athletes may berequired beyond what has been published in the current literature for BA and should be
elucidated across pre-, peri-, and post-menopausal females to optimize supplementation
effects.
Caffeine. Caffeine is one of the most widely used psychoactive compounds and reduces
fatigue or improves alertness by blocking adenosine receptors in the brain. A full review ofcaffeine effects is beyond the scope of this position stand, thus, we refer interested
readers to the ISSN Position Stand on Caffeine [291]. With regard to females,a menstrual cycle phase effect on elimination of caffeine has been demonstrated withgreater accumulation and slower elimination in the luteal phase (although no phasedifference in half-life) [292]. Beyond this, the evidence for caffeine erogenicity in females
is mixed at best. For example, caffeine has been shown to improve strength performancein resistance-trained women [293], but erogenicity was reduced in habituated caffeine
users unless ingestion of an acute dose of caffeine equivalent to the athlete’s daily
caffeine ingestion is used [294,295]. Moreover, a recent systematic review [296] demon­
strated that the effects of caffeine during resistance exercise may be reduced in womenwhen compared to men ingesting the same caffeine dosage. In addition, some of thecaffeine-induced stimulant effects are of smaller magnitude in women than in men [297].
It may be that the physiological responder status of caffeine has a greater implication on
caffeine efficacy [298]; with a dose–response relationship relative to body weight needed
to invoke effectiveness [291]. Additional research is needed to determine any sex differ­ence or sex hormone effect on caffeine uptake, dosage, and/or efficacy.
Nitrates. Dietary nitrate is growing in popularity as a sports nutrition supplement.
Inorganic nitrate is present in numerous foodstuffs and is abundant in green leafy
vegetables and beetroot. Following ingestion, nitrate is converted in the body to nitrite
and stored and circulated in the blood. In conditions of low oxygen availability, nitrite canbe converted into nitric oxide, which is known to play a number of important roles invascular and metabolic control [299]. Dietary nitrate supplementation has been shown toincrease plasma nitrite concentration and reduce resting blood pressure [300]. Nitrate
supplementation may reduce the oxygen cost of submaximal exercise and can, in maleathletes, enhance exercise tolerance and performance [301]. A significant literature gap ispresent in nitrate/beet juice exercise research, with few studies including female partici­
pants or examining relevant outcomes exclusively in female populations. In this respect,
limited evidence has demonstrated how untrained and recreationally trained females
respond to nitrate supplementation. As routinely observed in males, untrained andrecreationally trained females also experience a decrease in O2 costs of submaximal
exercise [302,303]. Alternatively, Wickham et al. [304] investigated the effects of acuteand chronic supplementation in recreationally trained COC-users and found no effect on
submaximal cycling vO2 or time trial performance, despite increases in plasma [NO3–] and[NO2–] in both acute and chronic supplementation conditions. Post-menopausal womenare a unique population with reduced endogenous nitric oxide bioavailability as com­pared to men and younger women. Recently, Proctor and colleagues investigated grip
strength and force development in 13 post-menopausal women using a double-blind
randomized design and found that NO3− supplementation enhanced force development

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and increased time to fatigue [305]. This study highlights the potential efficacy of NO3−
supplementation in postmenopausal women, however future research should be con­ducted, in trained females controlling for hormonal status (phases of the natural and OC
cycles, perimenopause, and post menopause) to determine the effects of dietary NO3–
supplementation on exercise and performance metrics.
Creatine. Evidence to support the benefits of creatine supplementation for women is
growing, with positive benefits related to strength, hypertrophy, performance, as wellas energetic and cognitive outcomes [306]. Compared to men, females exhibit 70–80%
lower endogenous intramuscular phosphocreatine stores and consume considerably
lower amounts of dietary creatine [307] yet have higher reported (~10%) resting levels
of intramuscular creatine concentrations [308], indicating supplementation at higher
doses may be more efficacious [309]. Moreover, creatine kinase perturbations have also
been shown to align with the cyclical pattern of estrogen across the menstrual cycle[310,311]. It has been suggested that supplementation in the luteal phase may be
more effective for the mechanistic support of creatine supplementation with regard tomuscle protein kinetics, growth factors, satellite cells, myogenic transcription factors,
glycogen and calcium regulation, oxidative stress, and inflammation [312,313], but
original investigations are needed to further explore this notion. Additionally, no
research has investigated the relationship between hormonal contraceptive patterns
and creatine kinase. Short- and long-term creatine supplementation has shown sig­
nificant beneficial ergogenic outcomes in strength, hypertrophy, and exercise perfor­
mance in trained and untrained female populations when compared to placebo
controls [313,314]. Currently, evidence shows consistent recommended dosage
amounts for males and females. In this respect, creatine supplementation typicallyfollows a pattern of a loading dose of ~ 20 g per day for 5 days (4 × 5 g doses taken
every 4 hours), followed by 3-5 g per day [306]. We refer interested readers to the ISSN
Position Stand on Creatine for a full review of the mechanistic/physiological effects ofcreatine [315].
Iron. Iron deficiency anemia and iron deficiency are five to seven times more common
in female athletes as compared to males [316]. These prevalence rates are linked to sex
differences [317], poor dietary intake, exercise-induced iron losses, and menstrual cycle
perturbations of iron regulation [38,318,319]. During the early follicular phase (days 0–5),
lower estrogen and progesterone hormone concentrations and iron regulatory hormonal
activity may facilitate increased iron absorption and recycling [38]. In the late follicularphase (days 6–14), the gradual rise in estrogen maintains low hepcidin activity, enablingiron absorption and recycling in the days following menses [320]. At ovulation, estrogenand testosterone peak, associated with increased iron uptake and erythropoiesis [321].
Following ovulation, increases in progesterone increase hepcidin expression, which limits
iron utilization [322]. The increase in inflammatory markers prior to menses [1,38] canexacerbate hepcidin activity, causing further limiting of iron utilization. Previous research
results demonstrate a rebound in hepcidin, serum iron, and transferrin saturation postovulation that stabilizes during the luteal phase [320]. Thus, iron supplementation ineumenorrheic female athletes may be more effective in the follicular vs. the luteal phase,
although additional research is needed to elucidate phase-based supplementation [323].
As hormonal contraceptive use is protective against iron deficiency [324], it is notrecommended for oral contraceptive users to supplement iron without medical advice.

JOURNAL OF THE INTERNATIONAL SOCIETY OF SPORTS NUTRITION

413

Moreover, a slower recovery of post-exercise basal hepcidin levels has been observed in
post-menopausal women for up to 24 h [325], thus planning the timing of iron supple­
mentation in postmenopausal women who exhibit iron deficiency may increase ironhomeostasis in this population.

8. Conclusion
Although women have been underrepresented in nutrition, sport, and exercise science
research, evidence continues to accumulate that highlights how sex differences and sex
hormones influence the nutritional requirements to maximize health, performance, andrecovery of female athletes. Due to the known wide intra-individual differences createdsecondary to specific hormonal profiles of female athletes, diligent tracking of menstrual
cycle and hormonal contraceptive use in premenopausal women is recommended.
Furthermore, attention should be paid in female athletes who may be transitioning fromperi to post-menopausal status to best understand their unique patterns, which can provide
insight and objective data on personalized approaches to nutritional strategies. Specificattention to overall energy status is the biggest driver in facilitating positive exercise training
adaptations, promotion of optimal performance, and health outcomes. From there, key
considerations should be made relative to the sex hormone's effects on metabolism.
A widespread lack of studies in females assessing nutritional strategies for performance,
body composition manipulation, and supplementation exists across the literature. It is ourhope that this position stand will bring to light many of these key areas and motivate futurescientific investigations to incorporate more females into all studies involving these outcomes.

Disclosure statement
No potential conflict of interest was reported by the author(s).

Funding
The author(s) reported there is no funding associated with the work featured in this article.

ORCID
Stacy T. Sims
http://orcid.org/0000-0002-3255-5428
Chad M. Kerksick
http://orcid.org/0000-0003-0458-7294
http://orcid.org/0000-0002-5405-304X
Abbie E. Smith-Ryan
Xanne A.K. Janse de Jonge
http://orcid.org/0000-0003-3657-5298
Katie R. Hirsch
http://orcid.org/0000-0002-0899-0139
Shawn M. Arent
http://orcid.org/0000-0003-0647-0591
Susan Joyce Hewlings
http://orcid.org/0000-0001-8540-2591
Susan M. Kleiner
http://orcid.org/0000-0002-2947-2517
Richard B. Kreider
http://orcid.org/0000-0002-3906-1658
http://orcid.org/0000-0002-1939-7656
Michael J. Ormsbee
Trisha A. VanDusseldorp
http://orcid.org/0000-0001-9057-2720
Bill I. Campbell
http://orcid.org/0000-0002-4106-3871
Douglas S. Kalman
http://orcid.org/0000-0003-0882-9748
Jose Antonio
http://orcid.org/0000-0002-8930-1058

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S. T. SIMS ET AL.

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