ArticlePDF Available
687
MountjoyM, etal. Br J Sports Med 2018;52:687–697. doi:10.1136/bjsports-2018-099193
IOC consensus statement on relative energy
deficiency in sport (RED-S): 2018update
Margo Mountjoy,1 Jorunn Kaiander Sundgot-Borgen,2 Louise M Burke,3,4
Kathryn E Ackerman,5,6 Cheri Blauwet,7 Naama Constantini,8 Constance Lebrun,9
Bronwen Lundy,3 Anna Katarina Melin,10 Nanna L Meyer,11 Roberta T Sherman,12
Adam S Tenforde,13 Monica Klungland Torstveit,14 Richard Budgett15
Consensus statement
To cite: MountjoyM,
Sundgot-BorgenJK,
BurkeLM, etal.
Br J Sports Med
2018;52:687–697.
For numbered affiliations see
end of article.
Correspondence to
Dr Margo Mountjoy,
Department of Family Medicine,
Michael G. DeGroote School of
Medicine, McMaster University,
Hamilton, ON N2G 1C5,
Canada;
mmsportdoc@ mcmaster. ca
This article has been
copublished in the International
Journal of Sport Nutrition
and Exercise Metabolism; doi:
10.1123/IJSNEM.2018-0136.
Accepted 17 April 2018
INTRODUCTION
In 2014, the IOC published a consensus statement
entitled ‘Beyond the Female Athlete Triad: Rela-
tive Energy Deficiency in Sport (RED-S)’. The
syndrome of RED-S refers to ‘impaired physiolog-
ical functioning caused by relative energy deficiency
and includes, but is not limited to, impairments of
metabolic rate, menstrual function, bone health,
immunity, protein synthesis and cardiovascular
health’. The aetiological factor of this syndrome is
low energy availability (LEA).1
The publication of the RED-S consensus state-
ment stimulated activity in the field of Female
Athlete Triad science, including some initial contro-
versy2 3 followed by numerous scientific publica-
tions addressing:
1. The health parameters identified in the RED-S
conceptual model (figure 1).1 4
2. Relative energy deficiency in male athletes.
3. The measurement of LEA.
4. The performance parameters identified in the
RED-S conceptual model (figure 2).1 4
The IOC RED-S consensus authors have recon-
vened to provide an update summary of the interim
scientific progress in the field of relative energy
deficiency with the ultimate goal of stimulating
advances in RED-S awareness, clinical application
and scientific research to address current gaps in
knowledge.
Low energy availability
LEA, which underpins the concept of RED-S, is a
mismatch between an athlete’s energy intake (diet)
and the energy expended in exercise, leaving inade-
quate energy to support the functions required by the
body to maintain optimal health and performance.
Operationally, energy availability (EA) is defined as:
Energy Availability (EA)
= Energy Intake (EI) (kcal)
Exercise Energy Expenditure (EEE) (kcal)/
Fat Free Mass (FFM) (kg)
where exercise energy expenditure (EEE) is
calculated as the additional energy expended above
that of daily living during the exercise bout, and
the overall result is expressed relative to fat-free
mass (FFM), reflecting the body’s most metaboli-
cally active tissues.5 6 Rigorously controlled labo-
ratory trials in women have shown that optimal
EA for healthy physiological function is typically
achieved at an EA of 45 kcal/kg FFM/day (188 kJ/
kg FFM/day).7 8 Meanwhile, although some caveats
are noted in relation to differential responses of
various body systems,9 many of these systems are
substantially perturbed at an EA <30 kcal/kg FFM/
day (125 kJ/kg FFM/day), making it historically
a targeted threshold for LEA. However, recent
evidence suggests that this cut-off does not predict
amenorrhoea in all women.10 11 In addition, and
not withstanding differences across body sizes and
pubertal age, it is noted that an EA of 30 kcal/kg/
FFM roughly equates to the average resting meta-
bolic rate (RMR).5 Because LEA has proven robust
in explaining markers of suboptimal health and
function in both laboratory7 8 and field settings,12 13
it seems logical that an EA assessment could serve as
a diagnostic tool in the prevention or management
of RED-S.
Measurement of EA
Despite the primary importance of determining
whether an athlete has adequate EA, several barriers
prohibit the direct measurement of EA from being a
practical and reliable option. First, there is no stan-
dardised or reference protocol for undertaking an
EA assessment (eg, the number of collection days,
methodologies for assessing energy intake, exer-
cise energy expenditure or FFM). Furthermore,
there are significant concerns over the reliability
and validity of each of these metrics. The greatest
challenge is to gain an accurate record of usual
energy intake from self-reported sources.9 14 Other
challenges include the measuring of exercise energy
expenditure during many of the training/competi-
tion activities performed by athletes and accounting
for their additional recreational/lifestyle activity.9 15
These problems may partially explain why many
field studies report considerable discrepancies
between EA calculations and symptoms associated
with LEA.9 14 16–18 However, other explanations for
these observations include: (1) the temporal dissoci-
ation between the period of mismatched eating and
exercise behaviour that created the LEA problems
and the occasion on which the EA assessment was
undertaken and (2) the interaction of other dietary
characteristics that often co-exist with LEA and may
exacerbate its effects (eg, high intake of fibre, stim-
ulants and artificial sweeteners; low energy density
foods; high dietary restraint and poor spread of
energy within a day).19–23 Even if these problems
on 4 June 2018 by guest. Protected by copyright.http://bjsm.bmj.com/Br J Sports Med: first published as 10.1136/bjsports-2018-099193 on 17 May 2018. Downloaded from
688 MountjoyM, etal. Br J Sports Med 2018;52:687–697. doi:10.1136/bjsports-2018-099193
Consensus statement
could be solved, EA calculations would likely involve specialised
equipment and expertise (eg, dual energy X-ray absorptiom-
etry measurement of body composition), good motivation and
compliance of the athlete (eg, keeping a food record or compre-
hensive activity diary) and considerable time and expertise to
process the information. Additionally, LEA states may develop at
different stages of training and competition due to varying phys-
iological demands. An EA assessment may achieve some valu-
able outcomes, such as strengthening the interaction between
the practitioner and athlete, which can create rapport, trust and
an appreciation of EA needs. However, the considerable effort
needed to assess EA and its frailties as a stand-alone diagnostic
tool prevent expert bodies from instituting it as a universally
recommended measurement.
Low energy availability in male athletes
Similar to female athletes, there is growing evidence that males
may experience LEA in situations when there is a mismatch
between energy intake and the exercise energy expenditure
of training or competition. Populations of male athletes at
increased risk for LEA and resulting health consequences of
RED-S include cyclists, rowers, runners, jockeys and athletes
in weight class combat sports.24–30 Factors that contribute to
LEA in male athletes are varied and often unique to the sport.
They include the cyclical changes in body mass and composition
(‘making weight’), prolonged inadequate energy intake to meet
high exercise energy expenditure of endurance sport, punctuated
changes in training volume/intensity and participation in stren-
uous endurance events without accompanied changes in nutri-
tion.26 Inadequate food availability, including food insecurity
from cultural practices or lack of financial resources may also
contribute risk for LEA in some male athletes, even among high
calibre athletes, as it undoubtedly also does in female athletes.26
While RED-S may occur in both sexes, there are likely differ-
ences in biological responses to LEA in male athletes compared
with their female counterparts. The prevalence of LEA has been
suggested to be higher in females than in males, although precise
differences are unknown.31 The threshold and duration of the
LEA state required to induce RED-S in men is unknown. Reduc-
tion in the sex hormone testosterone is likely to be of greater
health concern in male athletes.28 32 33
Low energy availability in para-athletes
The prevalence of LEA in para-athletes is incompletely char-
acterised.34 When extrapolating from trends noted in general
populations of individuals with disability, it can be assumed that
athletes who use a wheelchair for daily mobility are likely to
have reduced baseline energy needs.35 36 Despite this, male and
female athletes with spinal cord injury (SCI) may monitor or
restrict body weight for sport and are at risk for nutrient defi-
ciencies.37 38 Athletes with central neurological injury, such as
cerebral palsy, who demonstrate aberrant movement patterns
that include dyskinesis or athetosis, may have higher energy
expenditures than similar athletes without such non-purposeful
movements.39 Additionally, the presence of central neurolog-
ical injury may result in alterations of the hypothalamic–pitu-
itary axis and baseline menstrual function, regardless of energy
status.40–42 Amputee athletes may have higher energy needs in
the setting of prosthetic use and resultant gait asymmetry.43
Para-athletes are at high risk for impaired bone health and
bone-related injury secondary to many factors, including altered
skeletal loading. For example, in unilateral amputees, the affected
limb may exhibit reduced bone mineral density (BMD).44 Athletes
with SCI have disuse osteopenia/osteoporosis affecting the lower
extremities; however, positive adaptive changes in upper body
BMD values have been reported in wheelchair basketball players
compared with non-athletes (greater radial BMD and trend
towards increased lumbar BMD).45Characterising effects of
Figure 1 Health consequences of Relative Energy Deficiency in Sport
(RED-S) showing an expanded concept of the Female Athlete Triad to
acknowledge a wider range of outcomes and the application to male
athletes (*Psychological consequences can either precede RED-S or be
the result of RED-S).1 4
Figure 2 Potential Performance consequences of Relative Energy
Deficiency in Sport (*Aerobic and anerobic performance).1 4
on 4 June 2018 by guest. Protected by copyright.http://bjsm.bmj.com/Br J Sports Med: first published as 10.1136/bjsports-2018-099193 on 17 May 2018. Downloaded from
689
MountjoyM, etal. Br J Sports Med 2018;52:687–697. doi:10.1136/bjsports-2018-099193
Consensus statement
LEA on bone in para-athletes requires consideration of baseline
effects of each individual’s underlying disability. More work is
needed in this area.
Given rising participation in para sport from grass roots to
elite levels, further research is needed to investigate the impact
of LEA in athletes with a disability. The para-athlete population
requires screening for LEA to reduce complications of RED-S,
including low BMD.
Race and low energy availability
Whether race plays a role in the incidence and underlying aeti-
ology of RED-S remains speculative. Research shows a lower risk
of disordered eating (DE) in African-American, but not Latino
female high-school athletes compared with Caucasians.46 47
It is currently unknown whether the prevalence of menstrual
disorders differs among racially diverse athletic groups. Stress
fractures in African-American military recruits are lower than
in Caucasian recruits.48 Meanwhile, male Kenyan runners have
been observed to have greater BMD at weight-bearing sites (eg,
proximal femur) than healthy controls, but not at the lumbar
spine, where Z scores were reported to be below −2.0 in 40% of
study subjects.49 Such runners may have LEA resulting from low
energy intake and high exercise energy expenditure associated
with heavy training loads,49 as has been previously shown.50 51 In
another study of young Kenyan female athletes, middle-distance
and long-distance runners were found to exhibit one or more
subclinical and/or clinical components of the RED-S, including a
greater risk for LEA and menstrual dysfunction than controls.52
A study of sport nutrition knowledge, behaviours and beliefs
across sex, race/ethnicity and socioeconomic status in high school
soccer players identified that general sports nutrition knowledge
is lower in adolescent soccer players compared with prior reports
in adolescent athletes and that specifically females and Latinos
may benefit from sport nutrition education.53 Published research
is greatly lacking on RED-S in African-American, Hispanic and
Asian athletes, with a few exceptions.54 55 Thus, there is a need
to include more diverse athlete populations in RED-S research
and to integrate race/ethnicity in the prevention and treatment
of RED-S.
HEALTH EFFECTS OF LOW ENERGY AVAILABILITY
Endocrine
Effects of LEA on the endocrine system have been described
predominantly in female athletes and only recently in male
athletes. Findings in some female athletes in LEA states
(measured EA and/or athletes with amenorrhoea) include disrup-
tion of the hypothalamic–pituitary–gonadal axis, alterations in
thyroid function, changes in appetite-regulating hormones (eg,
decreased leptin and oxytocin, increased ghrelin, peptide YY and
adiponectin), decreases in insulin and insulin-like growth factor
1 (IGF-1), increased growth hormone (GH) resistance and eleva-
tions in cortisol.8 56–59 Many of these hormonal changes likely
occur to conserve energy for more important bodily functions or
to use the body’s energy reserves for vital processes.60 61
Specific changes in men are not completely understood;
however, reduced leutinizing hormone (LH) pulsatility and
amplitude have been described in a case series of male mara-
thon runners, a population at high risk for LEA.62 Other studies,
primarily in endurance male athlete populations, have shown
reductions in testosterone and inconsistent findings in differ-
ences in basal LH parameters.63 64 Koehler et al assessed the
effects of short-term EA manipulation through diet and exercise
on various hormonal parameters in six male habitual exercisers.65
Each male experienced four separate 4-day conditions: LEA (15
kcal/kg FFM/day with and without exercise) and adequate EA
(40 kcal/kg FFM/day with and without exercise). Following both
LEA conditions, regardless of exercise, leptin and insulin were
reduced compared with baseline (−53% to −56% and −34%
to −38%, respectively). LEA did not significantly affect ghrelin,
triiodothyronine (T3), testosterone or IGF-1 levels. Thus, the
LEA state, often in combination with disruptions to endocrine
function in women and possibly men, may contribute to multiple
physiological disease states described by RED-S. However, the
relationship is likely to be subject to a large degree of within-par-
ticipant and between-participant variability; more research is
needed, particularly in men.11 66 67
Menstrual function
The effects of LEA on reproductive hormones and menstrual
function in female athletes have been well described,8 68 69
although the complex hormonal signalling pathways underpin-
ning these effects are still being fully elucidated. Current evidence
supports a LEA-associated disruption of gonadotropin releasing
hormone (GnRH) pulsatility at the hypothalamus, followed by
alterations of LH and follicle stimulating hormone release from
the pituitary and decreased oestradiol and progesterone levels;
this is considered a form of functional hypothalamic amenor-
rhoea (FHA).68 70 The duration and severity of LEA needed to
create such disturbances are also unclear, reflecting both the
complex nature of the problem and discrepancies associated
with the different methodologies used to study it. For example,
Loucks and Thuma studied previously sedentary women in a
laboratory setting and identified that well-controlled interven-
tions reducing EA below 30 kcal/kg FFM/day via the short-
term (5 day) manipulation of exercise energy expenditure and
energy intake were associated with a dose–response decrease
in LH pulsatility.8 More recently, Williams et al reduced EA via
manipulation of energy intake and exercise energy expenditure
over several menstrual cycles in untrained, previously eumenor-
rhoeic subjects.11 The researchers found that the frequency of
menstrual disturbances (including luteal phase defects, anovu-
lation and oligomenorrhoea) was affected by the magnitude of
energy deficit compared with baseline needs,11 but a specific
threshold of EA below which menstrual disturbances occurred
was not identified.10
Meanwhile, Reed et al performed a cross-sectional analysis of
EA (measured using 3-day diet logs to determine energy intake
and a combination of exercise logs and heart rate monitoring to
measure estimated exercise energy expenditure) in female athletes
with eumenorrhoea and various menstrual disturbances.71 These
investigators reported mean EA was >30.0 kcal/kg FFM/day
in all the groups (amenorrhoeic, oligomenorrhoeic, ovulatory
eumenorrhoeic, inconsistent subclinical menstrual dysfunction
eumenorrhoeic and anovulatory eumenorrhoeic athletes) and EA
did not discriminate subclinical forms of menstrual disturbance;
however, EA was lower in amenorrhoeic athletes compared with
eumenorrhoeic athletes (mean 30.9 vs 36.9 kcal/kg FFM/day).71
Thus, severe energy deficiency is known to lead to amenor-
rhoea, but more work is needed to better understand the inter-
play of change in short-term and long-term EA and more subtle
menstrual disruption.
Bone health
It is established that LEA contributes to impaired bone health in
athletes, particularly women. Cross-sectional studies of physi-
cally active female athletes with oligomenorrhoea/amenorrhoea
on 4 June 2018 by guest. Protected by copyright.http://bjsm.bmj.com/Br J Sports Med: first published as 10.1136/bjsports-2018-099193 on 17 May 2018. Downloaded from
690 MountjoyM, etal. Br J Sports Med 2018;52:687–697. doi:10.1136/bjsports-2018-099193
Consensus statement
or measured LEA have demonstrated decreased BMD, altered
bone microarchitecture and bone turnover markers, decreased
estimates of bone strength and increased risk for bone stress inju-
ries compared with eumenorrhoeic athletes and those who are
energy replete.66 69 72–74 Short-term LEA (via diet and exercise)
has prospectively been shown to negatively affect bone turnover
markers in women and some men.57 67 Specific female and male
sport populations are at increased risk for lower BMD, including
jockeys, runners, swimmers and cyclists.24 29 30 75–83 Anatomical
sites with less bone loading and/or greater trabecular versus
cortical bone content (lumbar spine and radius vs total hip) are
at greater risk for low BMD and impaired microarchitecture in
populations susceptible to LEA.72 73 77 78 84
Low body mass index (BMI) is an imperfect surrogate
marker for LEA. However, BMI ≤17.5 kg/m2, <85% expected
body weight for adolescents or ≥10% weight loss in 1 month
are proposed indicators of LEA,85 and indeed both BMI and
expected body weight cut-offs are associated with increased risk
for low BMD in both sexes.24 82 86 LEA may be accompanied
by DE/eating disorders (EDs), menstrual dysfunction and low
BMD, and the combination of factors places athletes at higher
risk for bone stress injury.87–89
Metabolic
LEA has been correlated with decreased RMR in female endur-
ance athletes.90 Prospectively, increasing training load while
maintaining constant EI over 4 weeks in male and female elite
rowers led to a significant reduction in RMR.91 In normal weight
women with induced energy deficits via exercise and dietary
manipulation, measured weight loss over 3 months was less than
predicted.92 Subjects who were moderately energy deficient had
a significant decrease in RMR, and those who were severely
energy deficient demonstrated significant decreases in leptin, T3,
IGF-1 and an increase in ghrelin.92
Haematological
Iron is essential for haematopoiesis and subsequent oxygen
carrying capacity. Iron deficiency, often seen in female athletes,
can contribute directly and indirectly to energy deficiency. This
is due to a potential reduction in appetite, decreased metabolic
fuel availability and impaired metabolic efficiency, leading to an
increase in energy expenditure during exercise and rest.93 Iron
deficiency may also interact with bone health via dysregulation
of the GH/IGF-1 axis, hypoxia and hypothyroidism, in addition
to playing an important role in thyroid function, fertility and
even psychological well-being.93 Thus, LEA may be partially
induced by, and may contribute to, iron deficiency.93 Surrogates
for LEA have been correlated with haematological dysfunction,
including low ferritin and iron deficiency anaemia, in adolescent
and young adult female athletes.94
Growth and development
Linear growth retardation has been reported in various studies of
male and female adolescents with severe anorexia nervosa, with
studies demonstrating partial, but not always complete, catch-up
growth after recovery.95–97 Decreases in IGF-1, increases in GH
and increased GH resistance are consistently noted in those
with anorexia nervosa.98 Studies in amenorrhoeic athletes have
demonstrated disorderly GH secretory patterns, decreased
GH and IGF-1 secretory response to exercise accompanied by
increased interpulse GH levels and decreased IGF-1/IGFBP-1
ratios, with more research needed to understand training and
growth implications.99 100
Cardiovascular
Early atherosclerosis may be associated with hypoestrogenism
and FHA in young athletes.101 Endothelial dysfunction and
unfavourable lipid profiles have been reported in amenorrhoeic
athletes,102 with resumption of menses leading to improvements
in vascular endothelial function.103 In one study, amenorrhoeic
athletes demonstrated lower heart rates and systolic blood
pressure compared with eumenorrhoeic athletes, in addition
to disruptions of the normal renin–angiotensin–aldosterone
response to an orthostatic challenge.104 In the more severe LEA
state of anorexia nervosa, significant cardiovascular changes can
occur, including valve abnormalities, pericardial effusion, severe
bradycardia, hypotension and arrhythmias.105
Gastrointestinal
In the severe LEA state of AN, negative health influences on
the full gastrointestinal tract such as altered sphincter function,
delayed gastric emptying, constipation and increased intestinal
transit time, have been described.106 Melin et al measured EA
and developed the Low Energy Availability among Female
Athletes Questionnaire (LEAF-Q), both of which found a nega-
tive correlation with EA and gastrointestinal symptoms in elite
Swedish and Danish athletes.12 These findings were supported in
a survey of adolescent American female athletes with surrogate
markers of LEA, who also reported a higher incidence of stool
leakage and constipation than those considered to have adequate
EA.94
Immunological
The immune system may be altered by LEA. A study of 21 Japa-
nese elite, collegiate runners reported more upper respiratory
symptoms and lower immunoglobulin A secretion rates in the
amenorrhoeic versus eumenorrhoeic athletes.107 Meanwhile,
in observational studies of elite Australian athletes in prepara-
tion for the 2016 Rio Olympic Games, LEA, as measured by
the LEAF-Q in female athletes, was associated with increased
likelihood of illnesses (including those of the upper respiratory
tract and gastrointestinal tract), bodily aches and head-related
symptoms in the previous month.108 109
Psychological
Psychological problems can precede or be caused by LEA.1 LEA
in athletes has been shown to have negative correlates with
various aspects of psychological well-being. Higher drive for
thinness may be a proxy for LEA, as higher drive for thinness
scores on the Eating Disorder Inventory have been associated
with reduced resting energy expenditure, lower T3 levels, and
higher ghrelin levels in female athletes.110 Athletes who scored
higher on DT also scored higher in domains of ineffective-
ness, cognitive restraint, and bulimic tendencies.110 Adolescent
females with FHA have been found to have a higher incidence of
mild depressive traits, psychosomatic disorders, and a decreased
ability to manage stress.111 112 A separate study found overlap in
adolescents with anorexia nervosa and those with FHA: both
groups demonstrated increased depression, social insecurity and
introversion and fears of weight gain compared with healthy
controls.113 More profound psychological disturbances were seen
in the presumably more restricted EA (anorexia nervosa) group
versus the FHA group.113 Results from a study with male athletes
indicated that dietary restraint and muscle building behaviours
were associated with bulimic symptomatology.114 Additionally,
studies of male body builders indicate that a prolonged EA of
approximately 20–25 kcal/kg FFM/day, as seen in the final stage
on 4 June 2018 by guest. Protected by copyright.http://bjsm.bmj.com/Br J Sports Med: first published as 10.1136/bjsports-2018-099193 on 17 May 2018. Downloaded from
691
MountjoyM, etal. Br J Sports Med 2018;52:687–697. doi:10.1136/bjsports-2018-099193
Consensus statement
of contest diets, might be pathological and have negative psycho-
logical effects for males.27 The restrictive diet patterns observed
resulted in a reduction in muscle mass and a loss of strength,
with reports of endocrine dysfunction and mood disturbances in
those athletes with body composition measurements of approxi-
mately 4% total body fat.27
Disordered eating and eating disorders
Disordered eating and eating disorders are more prevalent
among female and male athletes in weight-sensitive sports in
comparison to athletes representing sports in which leanness
is a less important performance variable.115–119 In a Norwegian
study of adolescent elite male and female athletes, a higher prev-
alence of disordered eating in non-athletes as compared with
athletes was found when using questionnaires,120 but when
using a clinical interview, the prevalence of eating disorders
was higher in athletes versus controls.121 These findings suggest
the need for personal interviews to diagnose eating disorders in
athletes.117 121 122 It should be noted that the revised diagnostic
criteria for eating disorders (Diagnostic and Statistical Manual,
fifth edition) may influence the prevalence of the different diag-
noses among athletes.123 124
The pathogenesis of eating disorders is multifactorial with
cultural, familial, individual and genetic/biochemical factors
playing roles.125 Weight pressure and unique eating disorder
risk and trigger factors have been reported and include perfor-
mance pressure, sudden increase in training volume, injury,
teammate modelling of eating disorder behaviours and team
weigh-ins.126–128 A desire to be leaner to enhance performance
seems to predict later disordered eating127 and the risk of eating
pathology increases when the coach–athlete relationship is char-
acterised by high conflict and low support.129 Disordered eating
seems to be influenced by perfectionism, competitiveness, pain
tolerance and the perceived performance advantage of weight
loss.130 These suggested risk factors need to be validated to
demonstrate a causal relationship. However, these findings serve
as a call to action for enhanced screening for eating disorder
risk among athletes who experience weight pressure, are injured,
or who have teammates with known disordered eating/eating
disorders.126
Performance consequences of low energy availability
Associations between various surrogates of LEA (eg, hormonal
aberrations, oligomenorrhoea/amenorrhoea, leanness sport
participation and increased scores on ED/DE/LEA screening
tools) and factors negatively influencing performance (eg, illness,
injury, iron deficiency, impaired cognition and mood) have been
reported.87 93 94 131–137 Intervention studies on long-term energy
restriction and sport performance are lacking.138 However, it has
been postulated that persistent LEA could impair sport perfor-
mance through a variety of different indirect mechanisms (eg,
impaired recovery leading to premature reduction in physical,
psychological and mental capacity and impairment of optimal
muscle mass and function).139 Indeed, LEA could be expected
to impair performance or interfere with optimal performance
gains via acute impairment of key processes such as glycogen
storage140 or protein synthesis,141 or by preventing consistent
and high quality training due to the increased risk of injury and
illness.108 109
Despite the importance of these associations, it is only recently
that studies have tried to measure the direct impact of LEA on
sports performance. For example, Silva and Paiva reported
that athletic performance, measured as competition ranking,
negatively correlated with EA in elite rhythmic gymnasts.142
Furthermore, Tornberg et al found no difference in aerobic
capacity (VO2, O2 (mL/min/kg)) between elite eumenorrhoeic
endurance athletes and elite endurance athletes with secondary
FHA, despite lower body weight and fat mass in the athletes
with FHA.143 However, subjects with FHA had decreased neuro-
muscular performance (measured as knee muscular strength
and endurance) and reaction time compared with the eumen-
orrhoeic athletes.143 Overall, lower neuromuscular performance
was associated with higher cortisol levels, and lower blood
glucose, T3, oestrogen and FFM in the tested leg.143 Although
striving for a greater power to mass ratio is commonly regarded
as important for running performance, this study suggests that
achieving an idealised body weight or body composition through
severe and persistent energy restriction is likely to negatively
affect performance and health.143 This finding is supported in
a study of East African runners.144 Woods et al followed male
and female national team rowers through a 4-week intensified
training period, which was accompanied by a lack of increase in
energy intake despite a 21% increase in training load.91 It was
concluded that inadequate EA likely negatively affected training
recovery, at least partially explaining the alterations in 5 km time
trial pacing strategy and reduced performance.91
Considering the reported high prevalence of menstrual
dysfunction caused by energy deficiency,145 surprisingly, only
one study has investigated the direct impact of LEA on sport
performance. Vanheest et al reported a 10% decline in swim-
ming velocity over a 400 m time trial (after 12 weeks of
training) among young elite swimmers with ovarian suppression
secondary to energy deficiency compared with an 8% improve-
ment in their eumenorrhoeic teammates.13 Clearly, more investi-
gations, including robust protocols involving random allocation
of athletes to intervention groups, are needed to provide further
evidence and explanation of the effects of LEA on training adap-
tations and sport performance.
PREVENTION OF RELATIVE ENERGY DEFICIENCY IN SPORT
The prevention of RED-S requires increased awareness among
athletes and their entourage. Current evidence suggests that
there is much work to be done. Surveys have reported that
less than 50% of physicians, coaches, physiotherapists and
athletic trainers could identify the triad components (LEA with
or without an eating disorder, menstrual dysfunction and low
BMD),70 146–152 and only 19% of 370 US high school nurses
could identify all three triad components.153 In a survey of 931
multispecialty physicians, only 37% were aware of the triad, and
only one-half of these were comfortable treating or referring a
patient.70 In a group of exercising Australian women, one-third
believed irregular periods were ‘normal’ for active females, and
approximately half reported knowing that menstrual dysfunc-
tion was a risk factor for poor bone health.154 Educational
programmes typically identify their target audiences as health
professionals, coaches, athletic trainers, teachers, school admin-
istrators, athletes and parents.155 However, a survey of Inter-
national Sport Federations (IFs) identified that only 2 of 28
Olympic IFs had programmes on RED-S, indicating the need to
also involve a top-down approach.156 Peer-based eating disorder/
body image/triad education and cognitive-dissonance based
programmes have shown promise,157–160 and similar RED-S
peer-led programmes should be developed.
Effective eating disorder prevention programmes should be
multimodal, interactive and target athletes and coaching staff.161
One successful intervention is a peer-led educational programme
on 4 June 2018 by guest. Protected by copyright.http://bjsm.bmj.com/Br J Sports Med: first published as 10.1136/bjsports-2018-099193 on 17 May 2018. Downloaded from
692 MountjoyM, etal. Br J Sports Med 2018;52:687–697. doi:10.1136/bjsports-2018-099193
Consensus statement
for female athletes that resulted in improved bulimic pathology
1 year postintervention.162 A Norwegian school-based controlled
intervention programme, including elite male and female
athletes163 and coaches,164 resulted in no new cases of eating
disorders among females in the intervention schools as opposed
to eight (13%) in females at the control schools.163 There
was only one new eating disorder case in a male at a control
school and none in males from the intervention schools.163
These results suggest that effective disordered eating and eating
disorder prevention should target individuals beyond athletes
and coaches, be gender specific, involve significant others and
include changes to sport regulations, policy measures and the
healthcare system.165
SCREENING FOR RELATIVE ENERGY DEFICIENCY IN SPORT
Early detection of athletes at risk for energy deficiency is crit-
ical to prevent long-term health sequelae.1 69 85 There are several
disordered eating/eating disorder screening tools intended for
general population.166–169 Some tools have been developed to
target athletes, although none are validated for Diagnostic
and Statistical Manual of Mental Disorders, Fifth Edition
criteria.170–172 Additionally, due to stigma associated with eating
disorders, athletes may be motivated to hide their illness. An
elevated Eating Disorder Inventory—drive for thinness score168
has been reported to indicate energy deficiency in exercising
women,173 and amenorrhoeic athletes seem more likely to have an
elevated drive for thinness score compared with eumenorrhoeic
athletes.173 In order to diagnose an eating disorder, additional
in-depth personal interviews must be performed.117 121 122 166
However, the prevalence of energy deficiency is reported to be
high in some athletes even without the presence of disordered
eating/eating disorders.90 145
Although coaches are in an ideal situation to identify athletes
with disordered eating/eating disorders, they sometimes have
difficulty distinguishing between athletes whose appearance or
body composition metrics meets their sport-type expectations
(eg, thin) from those with an eating disorder, especially if the
athlete’s performance is good.174 Even if disordered eating is
identified, coaches may have difficulty convincing athletes to
seek treatment.175
The Periodic Health Examination176 and the Preparticipation
Physical Evaluation177 include relevant questions that may be
helpful for early detection. Recently, the LEAF-Q was devel-
oped12 as a brief questionnaire on physiological symptoms linked
to energy deficiency, and the Low Energy Availability in Males
Questionnaire is in development. Expanded testing of these
questionnaires in various athletic populations is needed. There is
limited evidence for the efficacy of self-reported questionnaires,
and additional individual evaluation is recommended.1 85 The
RED-S Clinical Assessment Tool (RED-S CAT) can assist clini-
cians in screening for RED-S and the management of return to
play decisions,178 although validation is needed.
TREATMENT OF RELATIVE ENERGY DEFICIENCY IN SPORT
Non-pharmacological management
If LEA is due to unintentional under eating, then simple nutri-
tional education may suffice. Regardless of the severity of the
eating pathology, early involvement of an accredited or appro-
priately trained expert (eg, sports dietitian) is recommended
to enhance the athlete’s nutritional practices. Optimising
EA can improve function of the hypothalamic–pituitary–
gonadal axis, as well as other systems negatively affected by
LEA in females.15 179–181 Energy deficits should be addressed
via modification of exercise and nutrition practices68 182 in
both female and male athletes and energy needs may be even
higher in growing adolescents. Treatment is typically based on
increased food intake but may also require changes in food
choices, energy spread and other dietary characteristics; these
changes must be individualised and periodised according to
the athlete’s energy expenditure and exercise goals. A reduc-
tion or cessation of exercise may be necessary, depending on
the severity of the energy deficit, symptoms and compliance
level.
Adequate bone-building nutrients are critical; for example,
serum 25-hydroxy vitamin D levels <30 ng/mL are associated
with increased incidence of bone stress injury.183 184 Vitamin D
intake of 600–800 IU daily is recommended by USDA dietary
guidelines,185 but greater intake may be needed temporarily
to reach goal serum 25-hydroxy vitamin D levels of >30 ng/
mL.186–188 Improving 25-hydroxy vitamin D levels may also
reduce healing time and facilitate earlier return to play for bone
stress injury.189 Additionally, adequate consumption of calcium
may help decrease the incidence of bone stress injury.190 191 The
current recommendation for daily calcium intake is 1000 mg/day
of calcium for men and women aged 19–50 years, and 1300 mg/
day for children and adolescents aged 9–18 years.192
Cognitive behavioural therapy is another non-pharmacolog-
ical treatment for RED-S that has been shown to contribute
to the resumption of menses in some women with FHA.193 194
Initial non-pharmacological management of RED-S may restore
menstrual function over months,181 195 while improvements in
bone health take longer and may never reach optimal levels.15
Non-compliance with therapy may require removal of the athlete
from training/competition. Examples of treatment contracts and
clearance categories for return to play can be found in other
publications.1 85 196 Current recommendations need further vali-
dation and may lead to the eventual inclusion of other progress
parameters, such as RMR and blood biomarkers.
Pharmacological interventions
The use of combined oral contraceptives for the intention of
regaining menses or improving BMD in those with RED-S is
not recommended. Data regarding the effects of combined oral
contraceptives on BMD and fracture risk are inconsistent.68 197–200
If using combined oral contraceptives for contraception, the
athlete should understand that combined oral contraceptives
may mask the return of spontaneous menses, and bone loss may
continue if the energy deficit is not corrected. If menstrual cycles
do not return after a reasonable trial of nutritional, psycholog-
ical and/or modified exercise interventions, transdermal oestra-
diol (E2) therapy with cyclic oral progestin can be considered for
short-term use.68 Notably, transdermal E2 is not a reliable form
of hormonal contraception and an athlete should be counselled
to avoid unintended pregnancy if she receives transdermal E2
for bone health. Transdermal oestrogen does not affect IGF-1
secretion, a bone-trophic hormone that combined oral contra-
ceptives downregulate, and has been shown to improve BMD
in anorexia nervosa201 and BMD and bone microarchitecture
in oligo-amenorrhoeic athletes.202 Recombinant parathyroid
hormone 1–34 (rPTH) has been shown to improve BMD in
AN203 and rare, short-term use may be considered in adults with
LEA, FHA or RED-S in the setting of delayed fracture healing or
very low BMD.68 Transdermal oestrogen or rPTH should only
be prescribed in conjunction with a metabolic bone expert and it
is important to note that rPTH is contraindicated in adolescents
and young adults with open growth plates.68
on 4 June 2018 by guest. Protected by copyright.http://bjsm.bmj.com/Br J Sports Med: first published as 10.1136/bjsports-2018-099193 on 17 May 2018. Downloaded from
693
MountjoyM, etal. Br J Sports Med 2018;52:687–697. doi:10.1136/bjsports-2018-099193
Consensus statement
Treatment strategies for disordered eating/eating disorders
Apparent disordered eating/eating disorders should be treated
with a multidisciplinary team including medical, dietary and
mental health support. Inpatient treatment should be consid-
ered for patients with severe bradycardia, hypotension, ortho-
stasis and/or electrolyte imbalance.85 196 204 Athletes’ resistance to
treatment usually increases with the severity of the problem.205
Because many patients with eating disorders see their disorders
as purposeful and necessary,206 motivation to recover is a crit-
ical factor in treatment. With sport participation as leverage for
athletes, the desire to be healthy enough to return to sport most
often facilitates recovery for athletes with eating disorders.207
As higher levels of depression and anxiety are observed in
athletes with eating pathology,208 there is a need to treat these
pathologies in athletes with disordered eating/eating disor-
ders. Additionally, comorbid disorders of depression, anxiety
and substance abuse complicate eating disorder treatment and
require treatment modifications.165 209 Ideally, treatment should
be provided by a mental health professional experienced in
treating eating problems in athletes.205 For athletes, meeting
the diagnostic criteria for severe eating disorders (eg, anorexia
nervosa and bulimia nervosa), participation in competition is not
recommended.1
CONCLUSIONS
Since the original publication of the IOC consensus statement
on RED-S in 2014, there have been many scientific advances
to improve our understanding of the health and performance
effects of LEA in both female and male athletes. To address
remaining gaps, the IOC RED-S consensus authors encourage
scientific activity in the following domains:
1. Identification of athletes at risk for RED-S: it is evident
that there is no practical tool for the measurement of EA;
therefore, there is a recognised need to develop a methodology
to screen and identify athletes at risk for RED-S that is both
scientifically validated and relevant and applicable in clinical
sport practice.
2. Prevention of RED-S: improved awareness of RED-S is
required through educational initiatives for athletes, coaches,
members of the entourage and sport organisations. The
development of scientifically validated prevention interven-
tions is encouraged.
3. Male athletes: despite the improvement in the knowledge
base of RED-S in male athletes, there remains a gap in our
understanding of RED-S in specific sports with differing
energy demands, performance criteria, ethnicities and
cultural perspectives.
4. Health and performance consequences of RED-S: there is
still much to be learned about the psychological and physi-
ological health risks and long-term consequences of RED-S
in all athletes, particularly male athletes, para-athletes and
athletes of various races. To best engage the attention of
athletes and coaches, it is imperative to further increase our
understanding of the performance effects of RED-S.
5. Treatment and ‘return to play’: practical guidelines for the
treatment and safe return to play for athletes with RED-S
need to be further developed to improve athletes’ health and
performance.
Author affiliations
1Department of Family Medicine, Michael G DeGroote School of Medicine, McMaster
University, Hamilton, Ontario, Canada
2Department of Sports Medicine, The Norwegian School of Sport Sciences, Oslo,
Norway
3Sports Nutrition, Australian Institute of Sport, Beclonnen, Australia
4Centre for Exercise and Nutrition, Mary MacKillop Institute for Health Research,
Melbourne, Victoria, Australia
5Divisions of Sports Medicine and Endocrinology, Boston Children’s Hospital, Boston,
Massachusetts, USA
6Neuroendocrine Unit, Massachuetts General Hospital, Harvard Medical School,
Boston, Massachusetts, USA
7Department of Physical Medicine and Rehabilitation, Harvard Medical School,
Spaulding Rehabilitation Hospital/Brigham and Women’s Hospital, Boston,
Massachusetts, USA
8Heidi Rothberg Sport Medicine Center, Shaare Zedek Medical Center, Hebrew
University, Jerusalem, Israel
9Department of Family Medicine, Faculty of Medicine and Dentistry, Glen Sather
Sports Medicine Clinic, University of Alberta, Edmonton, Alberta, Canada
10Department of Nutrition, Exercise and Sport, University of Copenhagen,
Frederiksberg, Denmark
11Health Sciences Department Colorado Springs, University of Colorado, Denver,
Colorado, USA
12Independent researcher, USA
13Department of Physical Medicine and Rehabilitation, Harvard Medical School,
Spaulding Rehabilitation Hospital, Charlestown, Massachusetts, USA
14Faculty of Health and Sport Sciences, University of Agder, Kristiansand, Norway
15IOC Medical and Scientific Department, Lausanne, Switzerland
Acknowledgements The authors would like to gratefully acknowledge the work
of Barbara Drinkwater in the field of the Female Athlete Triad and for her ongoing
support of the advancement of science in this domain. A special thanks to Allyson L
Parziale and Bryan Holtzman for their logistical and editorial assistance.
Contributors MM, JKS-B, LMB substantially contributed to the conception and
design and are the co-coordinators of IOC Expert Group. MM, JKS-B, LMB and
KEA substantially contributed to drafting and revising the manuscript. CB, NC, CL,
BL, AKM, NLM, RTS, AST, MKT and RB are the members of IOC Expert Group and
substantially contributed to drafting the manuscript. RB is the Director IOC Medical
and Scientific Department and contributed to revising the manuscript. All authors
confirmed the final version to be published.
Funding The authors have not declared a specific grant for this research from any
funding agency in the public, commercial or not-for-profit sectors.
Competing interests None declared.
Patient consent Not required.
Provenance and peer review Not commissioned; externally peer reviewed.
Data sharing statement There is no unpublished data.
© Article author(s) (or their employer(s) unless otherwise stated in the text of the
article) 2018. All rights reserved. No commercial use is permitted unless otherwise
expressly granted.
RefeRences
1 Mountjoy M, Sundgot-Borgen J, Burke L, et al. The IOC consensus statement: beyond
the Female Athlete Triad – relative energy deficiency in sport (RED-S). Br J Sports
Med 2014;48:491–7.
2 De Souza MJ, Williams NI, Nattiv A, et al. Misunderstanding the female athlete triad:
refuting the IOC consensus statement on Relative Energy Deficiency in Sport (RED-S).
Br J Sports Med 2014;48:1461–5.
3 Mountjoy M, Sundgot-Borgen J, Burke L, et al. Authors’ 2015 additions to the IOC
consensus statement: Relative Energy Deficiency in Sport (RED-S). Br J Sports Med
2015;49:417–20.
4 Constantini N. Medical concerns of the dancer. IMS World Congress of Sports
Medicine. Budapest, Hungary, 2011.
5 Loucks AB, Kiens B, Wright HH. Energy availability in athletes. J Sports Sci
2011;29:S7–15.
6 Melin A, Lundy B. Measuring energy availability. In: Burke L, Deakin V, eds. Clinical
Sports Nutrition. Sydney: McGraw-Hilll, 2015:146–57.
7 Loucks AB, Heath EM. Induction of low-T3 syndrome in exercising women occurs
at a threshold of energy availability. Am J Physiol Regul Integr Comp Physiol
1994;266:R817–R823.
8 Loucks AB, Thuma JR. Luteinizing hormone pulsatility is disrupted at a threshold
of energy availability in regularly menstruating women. J Clin Endocrinol Metab
2003;88:297–311.
9 Burke LM, Deakin V. Clinical sports nutrition. 5th edn: McGraw-Hilll Education
Australia, 2015.
10 Lieberman JL, DE Souza MJ, Wagstaff DA, et al. Menstrual disruption with exercise is
not linked to an energy availability threshold. Med Sci Sports Exerc 2018;50:551–61.
11 Williams NI, Leidy HJ, Hill BR, et al. Magnitude of daily energy deficit predicts
frequency but not severity of menstrual disturbances associated with exercise and
caloric restriction. Am J Physiol Endocrinol Metab 2015;308:E29–E39.
on 4 June 2018 by guest. Protected by copyright.http://bjsm.bmj.com/Br J Sports Med: first published as 10.1136/bjsports-2018-099193 on 17 May 2018. Downloaded from
694 MountjoyM, etal. Br J Sports Med 2018;52:687–697. doi:10.1136/bjsports-2018-099193
Consensus statement
12 Melin A, Tornberg AB, Skouby S, et al. The LEAF questionnaire: a screening tool for
the identification of female athletes at risk for the female athlete triad. Br J Sports
Med 2014;48:540–5.
13 Vanheest JL, Rodgers CD, Mahoney CE, et al. Ovarian suppression impairs sport
performance in junior elite female swimmers. Med Sci Sports Exerc 2014;46:156–66.
14 Burke LM, Melin A, Lundy B. Pitfalls and problems with measuring energy
availability. Int J Sport Nutr Exerc Metab 2018. In press.
15 Cialdella-Kam L, Guebels CP, Maddalozzo GF, et al. Dietary intervention restored
menses in female athletes with exercise-associated menstrual dysfunction with
limited impact on bone and muscle health. Nutrients 2014;6:3018–39.
16 Aparicio-Ugarriza R, Mielgo-Ayuso J, Benito PJ, et al. Physical activity assessment
in the general population; instrumental methods and new technologies. Nutr Hosp
2015;31(Suppl 3):219–26.
17 Levine JA. Measurement of energy expenditure. Public Health Nutr 2005;8:1123–32.
18 Pinheiro Volp AC, Esteves de Oliveira FC, Duarte Moreira Alves R, et al. Energy
expenditure: components and evaluation methods. Nutr Hosp 2011;26:430–40.
19 Barron E, Cano Sokoloff N, Maffazioli GDN, et al. Diets high in fiber and vegetable
protein are associated with low lumbar bone mineral density in young athletes with
oligoamenorrhea. J Acad Nutr Diet 2016;116:481–9.
20 Gaskins AJ, Mumford SL, Zhang C, et al. Effect of daily fiber intake on reproductive
function: the BioCycle Study. Am J Clin Nutr 2009;90:1061–9.
21 Heikura IA, Uusitalo ALT, Stellingwerff T, et al. Low energy availability is difficult
to assess but outcomes have large impact on bone injury rates in elite distance
athletes. Int J Sport Nutr Exerc Metab 2017:1–30.
22 Melin A, Tornberg ÅB, Skouby S, et al. Low-energy density and high fiber intake
are dietary concerns in female endurance athletes. Scand J Med Sci Sports
2016;26:1060–71.
23 Reed JL, De Souza MJ, Kindler JM, et al. Nutritional practices associated
with low energy availability in Division I female soccer players. J Sports Sci
2014;32:1499–509.
24 Barrack MT, Fredericson M, Tenforde AS, et al. Evidence of a cumulative effect for risk
factors predicting low bone mass among male adolescent athletes. Br J Sports Med
2017;51:200–5.
25 Berkovich BE, Eliakim A, Nemet D, et al. Rapid weight loss among adolescents
participating in competitive judo. Int J Sport Nutr Exerc Metab 2016;26:276–84.
26 Burke LM, Tenforde AS, Morton JP, et al. Relative energy deficiency in sport (RED-S)
in male athletes. Int J Sport Nutr Exerc Metab 2018. In press.
27 Fagerberg P. Negative consequences of low energy availability in natural male
bodybuilding: a review. Int J Sport Nutr Exerc Metab 2017:1–31.
28 Tenforde AS, Barrack MT, Nattiv A, et al. Parallels with the Female Athlete Triad in
male athletes. Sports Med 2016;46:171–82.
29 Viner RT, Harris M, Berning JR, et al. Energy availability and dietary patterns of adult
male and female competitive cyclists with lower than expected bone mineral density.
Int J Sport Nutr Exerc Metab 2015;25:594–602.
30 Wilson G, Hawken MB, Poole I, et al. Rapid weight-loss impairs simulated riding
performance and strength in jockeys: implications for making-weight. J Sports Sci
2014;32:383–91.
31 Loucks AB. Low energy availability in the marathon and other endurance sports.
Sports Med 2007;37:348–52.
32 Hackney AC, Moore AW, Brownlee KK. Testosterone and endurance exercise:
development of the "exercise-hypogonadal male condition". Acta Physiol Hung
2005;92:121–37.
33 Hooper DR, Kraemer WJ, Saenz C, et al. The presence of symptoms of testosterone
deficiency in the exercise-hypogonadal male condition and the role of nutrition. Eur J
Appl Physiol 2017;117:1349–57.
34 Blauwet CA, Brook EM, Tenforde AS, et al. Low energy availability, menstrual
dysfunction, and low bone mineral density in individuals with a disability:
implications for the para athlete population. Sports Med 2017;47:1697–708.
35 Buchholz AC, Pencharz PB. Energy expenditure in chronic spinal cord injury. Curr
Opin Clin Nutr Metab Care 2004;7:635–9.
36 Price M. Energy expenditure and metabolism during exercise in persons with a spinal
cord injury. Sports Med 2010;40:681–96.
37 Krempien JL, Barr SI. Risk of nutrient inadequacies in elite Canadian athletes with
spinal cord injury. Int J Sport Nutr Exerc Metab 2011;21:417–25.
38 Krempien JL, Barr SI. Eating attitudes and behaviours in elite Canadian athletes with
a spinal cord injury. Eat Behav 2012;13:36–41.
39 Crosland J, Boyd C. Cerebral palsy and acquired brain injuries. Broad E, ed. Sports
nutrition for paralympic athletes. Boca Raton, Florida, USA, 2014:91–105.
40 Colantonio A, Mar W, Escobar M, et al. Women’s health outcomes after traumatic
brain injury. J Womens Health 2010;19:1109–16.
41 Ranganathan P, Kumar RG, Davis K, et al. Longitudinal sex and stress hormone
profiles among reproductive age and post-menopausal women after severe TBI: a
case series analysis. Brain Inj 2016;30:452–61.
42 Ripley DL, Harrison-Felix C, Sendroy-Terrill M, et al. The impact of female
reproductive function on outcomes after traumatic brain injury. Arch Phys Med
Rehabil 2008;89:1090–6.
43 Gonzalez EG, Corcoran PJ, Reyes RL. Energy expenditure in below-knee amputees:
correlation with stump length. Arch Phys Med Rehabil 1974;55:111–9.
44 Sherk VD, Bemben MG, Bemben DA. BMD and bone geometry in transtibial and
transfemoral amputees. J Bone Miner Res 2008;23:1449–57.
45 Goktepe AS, Yilmaz B, Alaca R, et al. Bone density loss after spinal cord injury: elite
paraplegic basketball players vs. paraplegic sedentary persons. Am J Phys Med
Rehabil 2004;83:279–83.
46 Pernick Y, Nichols JF, Rauh MJ, et al. Disordered eating among a multi-racial/ethnic
sample of female high-school athletes. J Adolesc Health 2006;38:689–95.
47 Rhea DJ. Eating disorder behaviors of ethnically diverse urban female adolescent
athletes and non-athletes. J Adolesc 1999;22:379–88.
48 Lappe JM, Stegman MR, Recker RR. The impact of lifestyle factors on stress fractures
in female Army recruits. Osteoporos Int 2001;12:35–42.
49 Tam N, Santos-Concejero J, Tucker R, et al. Bone health in elite Kenyan runners. J
Sports Sci 2018;36:456–61.
50 Mukeshi M, Thairu K. Nutrition and body build: a Kenyan review. World Rev Nutr
Diet 1993;72:218–26.
51 Beis LY, Willkomm L, Ross R, et al. Food and macronutrient intake of elite Ethiopian
distance runners. J Int Soc Sports Nutr 2011;8:7–19.
52 Muia EN, Wright HH, Onywera VO, et al. Adolescent elite Kenyan runners are at risk
for energy deficiency, menstrual dysfunction and disordered eating. J Sports Sci
2016;34:598–606.
53 Manore MM, Patton-Lopez MM, Meng Y, et al. Sport nutrition knowledge, behaviors
and beliefs of high school soccer players. Nutrients 2017;9:350.
54 Iwamoto J, Sato Y, Takeda T, et al. Analysis of stress fractures in athletes based on our
clinical experience. World J Orthop 2011;2:7–12.
55 Quah YV, Poh BK, Ng LO, et al. The female athlete triad among elite Malaysian
athletes: prevalence and associated factors. Asia Pac J Clin Nutr 2009;18:200–8.
56 Allaway HCM, Southmayd EA, De Souza MJ. The physiology of functional
hypothalamic amenorrhea associated with energy deficiency in exercising
women and in women with anorexia nervosa. Horm Mol Biol Clin Investig
2016;25:91–119.
57 Ihle R, Loucks AB. Dose-response relationships between energy availability and bone
turnover in young exercising women. J Bone Miner Res 2004;19:1231–40.
58 Logue D, Madigan SM, Delahunt E, et al. Low energy availability in athletes: a review
of prevalence, dietary patterns, physiological health, and sports performance. Sports
Med 2018;48:73–96.
59 Misra M. Neuroendocrine mechanisms in athletes. Handb Clin Neurol
2014;124:373–86.
60 Jasienska G. Energy metabolism and the evolution of reproductive suppression in the
human female. Acta Biotheor 2003;51:1–18.
61 Wade GN, Jones JE. Neuroendocrinology of nutritional infertility. Am J Physiol Regul
Integr Comp Physiol 2004;287:R1277–96.
62 MacConnie SE, Barkan A, Lampman RM, et al. Decreased hypothalamic
gonadotropin-releasing hormone secretion in male marathon runners. N Engl J Med
1986;315:411–7.
63 Hackney AC, Sinning WE, Bruot BC. Reproductive hormonal profiles of endurance-
trained and untrained males. Med Sci Sports Exerc 1988;20:60–5.
64 McColl EM, Wheeler GD, Gomes P, et al. The effects of acute exercise on pulsatile LH
release in high-mileage male runners. Clin Endocrinol 1989;31:617–22.
65 Koehler K, Hoerner NR, Gibbs JC, et al. Low energy availability in exercising men is
associated with reduced leptin and insulin but not with changes in other metabolic
hormones. J Sports Sci 2016;34:1921–9.
66 Papageorgiou M, Dolan E, Elliott-Sale KJ, et al. Reduced energy availability:
implications for bone health in physically active populations. Eur J Nutr 2018;57:1.
67 Papageorgiou M, Elliott-Sale KJ, Parsons A, et al. Effects of reduced energy
availability on bone metabolism in women and men. Bone 2017;105:191–9.
68 Gordon CM, Ackerman KE, Berga SL, et al. Functional hypothalamic amenorrhea:
an endocrine society clinical practice guideline. J Clin Endocrinol Metab
2017;102:1413–39.
69 Nattiv A, Loucks AB, Manore MM, et al. American College of Sports Medicine
position stand. The female athlete triad. Med Sci Sports Exerc 2007;39:1867–82.
70 Curry EJ, Logan C, Ackerman K, et al. Female athlete triad awareness among
multispecialty physicians. Sports Med Open 2015;1:38.
71 Reed JL, De Souza MJ, Mallinson RJ, et al. Energy availability discriminates clinical
menstrual status in exercising women. J Int Soc Sports Nutr 2015;12:11.
72 Ackerman KE, Nazem T, Chapko D, et al. Bone microarchitecture is impaired in
adolescent amenorrheic athletes compared with eumenorrheic athletes and
nonathletic controls. J Clin Endocrinol Metab 2011;96:3123–33.
73 Ackerman KE, Putman M, Guereca G, et al. Cortical microstructure and estimated
bone strength in young amenorrheic athletes, eumenorrheic athletes and non-
athletes. Bone 2012;51:680–7.
74 De Souza MJ, West SL, Jamal SA, et al. The presence of both an energy deficiency
and estrogen deficiency exacerbate alterations of bone metabolism in exercising
women. Bone 2008;43:140–8.
75 Andreoli A, Monteleone M, Van Loan M, et al. Effects of different sports on
bone density and muscle mass in highly trained athletes. Med Sci Sports Exerc
2001;33:507–11.
76 Barrack MT, Rauh MJ, Nichols JF. Prevalence of and traits associated with low BMD
among female adolescent runners. Med Sci Sports Exerc 2008;40:2015–21.
on 4 June 2018 by guest. Protected by copyright.http://bjsm.bmj.com/Br J Sports Med: first published as 10.1136/bjsports-2018-099193 on 17 May 2018. Downloaded from
695
MountjoyM, etal. Br J Sports Med 2018;52:687–697. doi:10.1136/bjsports-2018-099193
Consensus statement
77 Fredericson M, Chew K, Ngo J, et al. Regional bone mineral density in male
athletes: a comparison of soccer players, runners and controls. Br J Sports Med
2007;41:664–8.
78 Hind K, Truscott JG, Evans JA. Low lumbar spine bone mineral density in both male
and female endurance runners. Bone 2006;39:880–5.
79 Morel J, Combe B, Francisco J, et al. Bone mineral density of 704 amateur sportsmen
involved in different physical activities. Osteoporos Int 2001;12:152–7.
80 Nichols JF, Rauh MJ. Longitudinal changes in bone mineral density in male master
cyclists and nonathletes. J Strength Cond Res 2011;25:727–34.
81 Stewart AD, Hannan J. Total and regional bone density in male runners, cyclists, and
controls. Med Sci Sports Exerc 2000;32:1373–7.
82 Tenforde AS, Fredericson M, Sayres LC, et al. Identifying sex-specific risk
factors for low bone mineral density in adolescent runners. Am J Sports Med
2015;43:1494–504.
83 Wilson G, Hill J, Sale C, et al. Elite male Flat jockeys display lower bone density and
lower resting metabolic rate than their female counterparts: implications for athlete
welfare. Appl Physiol Nutr Metab 2015;40:1318–20.
84 Bilanin JE, Blanchard MS, Russek-Cohen E. Lower vertebral bone density in male
long distance runners. Med Sci Sports Exerc 1989;21:66–70.
85 De Souza MJ, Nattiv A, Joy E, et al. Expert Panel. 2014 Female Athlete Triad Coalition
Consensus Statement on Treatment and Return to Play of the Female Athlete Triad:
1st International Conference held in San Francisco, California, May 2012 and 2nd
International Conference held in Indianapolis, Indiana, May 2013. Br J Sports Med
2014;48:289.
86 Thralls KJ, Nichols JF, Barrack MT, et al. Body mass-related predictors of the
female athlete triad among adolescent athletes. Int J Sport Nutr Exerc Metab
2016;26:17–25.
87 Ackerman KE, Cano Sokoloff N, DE Nardo Maffazioli G, et al. Fractures in relation
to menstrual status and bone parameters in young athletes. Med Sci Sports Exerc
2015;47:1577–86.
88 Barrack MT, Gibbs JC, De Souza MJ, et al. Higher incidence of bone stress injuries
with increasing female athlete triad-related risk factors: a prospective multisite study
of exercising girls and women. Am J Sports Med 2014;42:949–58.
89 Tenforde AS, Carlson JL, Chang A, et al. Association of the female athlete triad risk
assessment stratification to the development of bone stress injuries in collegiate
athletes. Am J Sports Med 2017;45:302–10.
90 Melin A, Tornberg ÅB, Skouby S, et al. Energy availability and the female athlete triad
in elite endurance athletes. Scand J Med Sci Sports 2015;25:610–22.
91 Woods AL, Garvican-Lewis LA, Lundy B, et al. New approaches to determine fatigue
in elite athletes during intensified training: Resting metabolic rate and pacing profile.
PLoS One 2017;12:e0173807–17.
92 Koehler K, De Souza MJ, Williams NI. Less-than-expected weight loss in normal-
weight women undergoing caloric restriction and exercise is accompanied
by preservation of fat-free mass and metabolic adaptations. Eur J Clin Nutr
2017;71:365–71.
93 Petkus DL, Murray-Kolb LE, De Souza MJ. The unexplored crossroads of the
female athlete triad and iron deficiency: a narrative review. Sports Med
2017;47:1721–37.
94 Ackerman KE, Holtzman B, Cooper KM, et al. Low energy availability surrogates
correlate with health and performance consequences of relative energy deficiency in
sport (RED-S). Br J Sports Med 2018. In press.
95 Lantzouni E, Frank GR, Golden NH, et al. Reversibility of growth stunting in early
onset anorexia nervosa: a prospective study. J Adolesc Health 2002;31:162–5.
96 Modan-Moses D, Yaroslavsky A, Kochavi B, et al. Linear growth and final
height characteristics in adolescent females with anorexia nervosa. PLoS One
2012;7:e45504–8.
97 Modan-Moses D, Yaroslavsky A, Novikov I, et al. Stunting of growth as a major
feature of anorexia nervosa in male adolescents. Pediatrics 2003;111:270–6.
98 Fazeli PK, Klibanski A. Determinants of GH resistance in malnutrition. J Endocrinol
2014;220:R57–R65.
99 Laughlin GA, Yen SS. Nutritional and endocrine-metabolic aberrations in amenorrheic
athletes. J Clin Endocrinol Metab 1996;81:4301–9.
100 Waters DL, Qualls CR, Dorin R, et al. Increased pulsatility, process irregularity, and
nocturnal trough concentrations of growth hormone in amenorrheic compared to
eumenorrheic athletes. J Clin Endocrinol Metab 2001;86:1013–9.
101 O’Donnell E, Goodman JM, Harvey PJ. Clinical review: cardiovascular consequences
of ovarian disruption: a focus on functional hypothalamic amenorrhea in physically
active women. J Clin Endocrinol Metab 2011;96:3638–48.
102 Rickenlund A, Eriksson MJ, Schenck-Gustafsson K, et al. Amenorrhea in female
athletes is associated with endothelial dysfunction and unfavorable lipid profile. J
Clin Endocrinol Metab 2005;90:1354–9.
103 Hoch AZ, Jurva JW, Staton MA, et al. Athletic amenorrhea and endothelial
dysfunction. WMJ 2007;106:301–6.
104 O’Donnell E, Goodman JM, Mak S, et al. Discordant orthostatic reflex renin-
angiotensin and sympathoneural responses in premenopausal exercising-
hypoestrogenic women. Hypertension 2015;65:1089–95.
105 Spaulding-Barclay MA, Stern J, Mehler PS. Cardiac changes in anorexia nervosa.
Cardiol Young 2016;26:623–8.
106 Norris ML, Harrison ME, Isserlin L, et al. Gastrointestinal complications associated
with anorexia nervosa: A systematic review. Int J Eat Disord 2016;49:216–37.
107 Shimizu K, Suzuki N, Nakamura M, et al. Mucosal immune function comparison
between amenorrheic and eumenorrheic distance runners. J Strength Cond Res
2012;26:1402–6.
108 Drew M, Vlahovich N, Hughes D, et al. Prevalence of illness, poor mental health and
sleep quality and low energy availability prior to the 2016 Summer Olympic Games.
Br J Sports Med 2018;52:47–53.
109 Drew MK, Vlahovich N, Hughes D, et al. A multifactorial evaluation of illness risk
factors in athletes preparing for the Summer Olympic Games. J Sci Med Sport
2017;20:745–50.
110 De Souza MJ, Hontscharuk R, Olmsted M, et al. Drive for thinness score is a proxy
indicator of energy deficiency in exercising women. Appetite 2007;48:359–67.
111 Bomba M, Gambera A, Bonini L, et al. Endocrine profiles and neuropsychologic
correlates of functional hypothalamic amenorrhea in adolescents. Fertil Steril
2007;87:876–85.
112 Marcus MD, Loucks TL, Berga SL. Psychological correlates of functional hypothalamic
amenorrhea. Fertil Steril 2001;76:310–6.
113 Bomba M, Corbetta F, Bonini L, et al. Psychopathological traits of adolescents with
functional hypothalamic amenorrhea: a comparison with anorexia nervosa. Eat
Weight Disord 2014;19:41–8.
114 Petrie T, Galli N, Greenleaf C, et al. Psychosocial correlates of bulimic
symptomatology among male athletes. Psychol Sport Exerc 2014;15:680–7.
115 Kong P, Harris LM. The sporting body: body image and eating disorder
symptomatology among female athletes from leanness focused and nonleanness
focused sports. J Psychol 2015;149:141–60.
116 Sundgot-Borgen J. Prevalence of eating disorders in elite female athletes. Int J Sport
Nutr 1993;3:29–40.
117 Sundgot-Borgen J, Torstveit MK. Prevalence of eating disorders in elite athletes is
higher than in the general population. Clin J Sport Med 2004;14:25–32.
118 Sykora C, Grilo CM, Wilfley DE, et al. Eating, weight, and dieting disturbances
in male and female lightweight and heavyweight rowers. Int J Eat Disord
1993;14:203–11.
119 Thiemann P, Legenbauer T, Vocks S, et al. Eating disorders and their putative
risk factors among female German professional athletes. Eur Eat Disord Rev
2015;23:269–76.
120 Martinsen M, Bratland-Sanda S, Eriksson AK, et al. Dieting to win or to be thin? A
study of dieting and disordered eating among adolescent elite athletes and non-
athlete controls. Br J Sports Med 2010;44:70–6.
121 Martinsen M, Sundgot-Borgen J. Higher prevalence of eating disorders among
adolescent elite athletes than controls. Med Sci Sports Exerc 2013;45:1188–97.
122 Fairburn CG, Cooper Z, O’Connor M. Eating disorder examination. Cogn Behav Ther
Eat Disord 2008:270–308.
123 American Psychiatric Association. Diagnostic and statistical manual of mental
disorders: DSM-5. Washington, D.C: American Psychiatric Association, 2013.
124 Vo M, Accurso EC, Goldschmidt AB, et al. The impact of DSM-5 on eating disorder
diagnoses. Int J Eat Disord 2017;50:578–81.
125 Stice E, South K, Shaw H. Future directions in etiologic, prevention, and treatment
research for eating disorders. J Clin Child Adolesc Psychol 2012;41:845–55.
126 Arthur-Cameselle J, Sossin K, Quatromoni P. A qualitative analysis of factors related
to eating disorder onset in female collegiate athletes and non-athletes. Eat Disord
2017;25:199–215.
127 Krentz EM, Warschburger P. A longitudinal investigation of sports-related
risk factors for disordered eating in aesthetic sports. Scand J Med Sci Sports
2013;23:303–10.
128 Sundgot-Borgen J. Risk and trigger factors for the development of eating disorders
in female elite athletes. Med Sci Sports Exerc 1994;26:414–9.
129 Shanmugam V, Jowett S, Meyer C. Interpersonal difficulties as a risk factor for
athletes’ eating psychopathology. Scand J Med Sci Sports 2014;24:469–76.
130 Stirling A, Kerr G. Perceived vulnerabilities of female athletes to the development of
disordered eating behaviours. Eur J Sport Sci 2012;12:262–73.
131 Baskaran C, Plessow F, Ackerman KE, et al. A cross-sectional analysis of verbal
memory and executive control across athletes with varying menstrual status and
non-athletes. Psychiatry Res 2017;258:605–6.
132 Burden RJ, Morton K, Richards T, et al. Is iron treatment beneficial in, iron-deficient
but non-anaemic (IDNA) endurance athletes? A systematic review and meta-
analysis. Br J Sports Med 2015;49:1389–97.
133 Geesmann B, Gibbs JC, Mester J, et al. Association between energy balance and
metabolic hormone suppression during ultraendurance exercise. Int J Sports Physiol
Perform 2017;12:984–9.
134 Hagmar M, Berglund B, Brismar K, et al. Body composition and endocrine profile of
male Olympic athletes striving for leanness. Clin J Sport Med 2013;23:197–201.
135 Harber VJ, Petersen SR, Chilibeck PD. Thyroid hormone concentrations and muscle
metabolism in amenorrheic and eumenorrheic athletes. Can J Appl Physiol
1998;23:293–306.
136 Rauh MJ, Nichols JF, Barrack MT. Relationships among injury and disordered eating,
menstrual dysfunction, and low bone mineral density in high school athletes: a
prospective study. J Athl Train 2010;45:243–52.
on 4 June 2018 by guest. Protected by copyright.http://bjsm.bmj.com/Br J Sports Med: first published as 10.1136/bjsports-2018-099193 on 17 May 2018. Downloaded from
696 MountjoyM, etal. Br J Sports Med 2018;52:687–697. doi:10.1136/bjsports-2018-099193
Consensus statement
137 Thein-Nissenbaum JM, Carr KE, Hetzel S, et al. Disordered eating, menstrual
irregularity, and musculoskeletal injury in high school athletes: a comparison of oral
contraceptive pill users and nonusers. Sports Health 2014;6:313–20.
138 El Ghoch M, Soave F, Calugi S, et al. Eating disorders, physical fitness and sport
performance: a systematic review. Nutrients 2013;5:5140–60.
139 Fogelholm M. Effects of bodyweight reduction on sports performance. Sports Med
1994;18:249–67.
140 Tarnopolsky MA, Zawada C, Richmond LB, et al. Gender differences
in carbohydrate loading are related to energy intake. J Appl Physiol
2001;91:225–30.
141 Areta JL, Burke LM, Camera DM, et al. Reduced resting skeletal muscle protein
synthesis is rescued by resistance exercise and protein ingestion following short-term
energy deficit. AJP Endocrinol Metab 2014;306:E989–97.
142 Silva MR, Paiva T. Poor precompetitive sleep habits, nutrients’ deficiencies,
inappropriate body composition and athletic performance in elite gymnasts. Eur J
Sport Sci 2016;16:726–35.
143 Tornberg ÅB, Melin A, Koivula FM, et al. Reduced neuromuscular performance in
amenorrheic elite endurance athletes. Med Sci Sports Exerc 2017;49:2478–85.
144 Mooses M, Hackney AC. Anthropometrics and body composition in East
African runners: potential impact on performance. Int J Sports Physiol Perform
2017;12:422–30.
145 Gibbs JC, Williams NI, De Souza MJ. Prevalence of individual and combined
components of the female athlete triad. Med Sci Sports Exerc 2013;45:985–96.
146 Brown KN, Wengreen HJ, Beals KA. Knowledge of the female athlete triad, and
prevalence of triad risk factors among female high school athletes and their coaches.
J Pediatr Adolesc Gynecol 2014;27:278–82.
147 Feldmann JM, Belsha JP, Eissa MA, et al. Female adolescent athletes’ awareness
of the connection between menstrual status and bone health. J Pediatr Adolesc
Gynecol 2011;24:311–4.
148 Kroshus E, Sherman RT, Thompson RA, et al. Gender differences in high school
coaches’ knowledge, attitudes, and communication about the female athlete triad.
Eat Disord 2014;22:193–208.
149 Mukherjee S, Chand V, Wong XX, et al. Perceptions, awareness and knowledge of the
female athlete triad amongst coaches - are we meeting the expectations for athlete
safety? Int J Sport Sci Coach 2016;11:545–51.
150 Pantano KJ. Current knowledge, perceptions, and interventions used by collegiate
coaches in the U.S. regarding the prevention and treatment of the female athlete
triad. N Am J Sports Phys Ther 2006;1:195–207.
151 Pantano KJ. Knowledge, attitude, and skill of high school coaches with regard to the
female athlete triad. J Pediatr Adolesc Gynecol 2017;30:540–5.
152 Troy K, Hoch AZ, Stavrakos JE. Awareness and comfort in treating the female athlete
triad: are we failing our athletes? WMJ 2006;105:21.
153 Kroshus E, Fischer AN, Nichols JF. Assessing the awareness and behaviors of
U.S. high school nurses with respect to the female athlete triad. J Sch Nurs
2015;31:272–9.
154 Miller SM, Kukuljan S, Turner AI, et al. Energy deficiency, menstrual disturbances,
and low bone mass: what do exercising Australian women know about the female
athlete triad? Int J Sport Nutr Exerc Metab 2012;22:131–8.
155 Torres-McGehee TM, Pritchett KL, Zippel D, et al. Sports nutrition knowledge
among collegiate athletes, coaches, athletic trainers, and strength and conditioning
specialists. J Athl Train 2012;47:205–11.
156 Mountjoy M, Costa A, Budgett R, et al. Health promotion through sport:
international sport federations’ priorities, actions and opportunities. Br J Sports Med
2018;52:54–60.
157 Brown KN, Wengreen HJ, Beals KA, et al. Effects of peer-education on knowledge
of the female athlete triad among high school track and field athletes: a pilot study.
Women Sport Phys Activity J 2016;24:1–6.
158 Kilpela LS, Blomquist K, Verzijl C, et al. The body project 4 all: a pilot randomized
controlled trial of a mixed-gender dissonance-based body image program. Int J Eat
Disord 2016;49:591–602.
159 Temme KE, Hoch AZ, Jonardi M, et al. Prevalence of the female athlete triad and
effect of a peer-based mentoring program on triad knowledge in high school girls.
Clin J Sport Med 2013;23:134–5.
160 Valliant MW, Emplaincourt HP, Wenzel RK, et al. Nutrition education by a registered
dietitian improves dietary intake and nutrition knowledge of a NCAA female
volleyball team. Nutrients 2012;4:506–16.
161 Bar RJ, Cassin SE, Dionne MM, et al. Eating disorder prevention initiatives for
athletes: a review. Eur J Sport Sci 2016;16:325–35.
162 Becker CB, McDaniel L, Bull S, et al. Can we reduce eating disorder risk factors in
female college athletes? A randomized exploratory investigation of two peer-led
interventions. Body Image 2012;9:31–42.
163 Martinsen M, Bahr R, Børresen R, et al. Preventing eating disorders among young
elite athletes: a randomized controlled trial. Med Sci Sports Exerc 2014;46:435–47.
164 Martinsen M, Sherman RT, Thompson RA, et al. Coaches’ knowledge and
management of eating disorders: a randomized controlled trial. Med Sci Sports Exerc
2015;47:1070–8.
165 de Bruin APK. Athletes with eating disorder symptomatology, a specific population
with specific needs. Curr Opin Psychol 2017;16:148–53.
166 Fairburn CG, Beglin SJ. Assessment of eating disorders: interview or self-report
questionnaire? Int J Eat Disord 1994;16:363–70.
167 Garner DM, Garfinkel PE. The eating attitudes test: an index of the symptoms of
anorexia nervosa. Psychol Med 1979;9:273–9.
168 Garner DM, Olmstead MP, Polivy J. Development and validation of a
multidimensional eating disorder inventory for anorexia nervosa and bulimia. Int J
Eat Disord 1983;2:15–34.
169 Hill LS, Reid F, Morgan JF, et al. SCOFF, the development of an eating disorder
screening questionnaire. Int J Eat Disord 2010;43:344–51.
170 Hinton PS, Kubas KL. Psychosocial correlates of disordered eating in female
collegiate athletes: validation of the ATHLETE questionnaire. J Am Coll Health
2005;54:149–56.
171 McNulty KY, Adams CH, Anderson JM, et al. Development and validation of a
screening tool to identify eating disorders in female athletes. J Am Diet Assoc
2001;101:886–92.
172 Steiner H, Pyle RP, Brassington GS, et al. The College Health Related Information
Survey (C.h.R.I.s.-73): a screen for college student athletes. Child Psychiatry Hum
Dev 2003;34:97–109.
173 Gibbs JC, Williams NI, Scheid JL, et al. The association of a high drive for thinness
with energy deficiency and severe menstrual disturbances: confirmation in a large
population of exercising women. Int J Sport Nutr Exerc Metab 2011;21:280–90.
174 Plateau CR, Mcdermott HJ, Arcelus J, et al. Identifying and preventing disordered
eating among athletes. What can we learn from coaches? Appetite 2013;71:483.
175 Plateau CR, Arcelus J, Leung N, et al. Female athlete experiences of seeking and
receiving treatment for an eating disorder. Eat Disord 2017;25:273–7.
176 Ljungqvist A, Jenoure P, Engebretsen L, et al. The International Olympic Committee
(IOC) consensus statement on periodic health evaluation of elite athletes March
2009. Br J Sports Med 2009;43:631–43.
177 American Academy of Family Physicians, American Academy of Pediatrics,
American College of Sports Medicine. Preparticipation physical evaluation. 4th edn.
Washington, DC: American Academy of Family Physicians, 2010.
178 Mountjoy M, Sundgot-Borgen J, Burke L, et al. RED-S CAT. Relative energy deficiency
in sport (RED-S) clinical assessment tool (CAT). Br J Sports Med 2015;49:421–3.
179 a DC, Matt KS, Manore MM, et al. Treatment of athletic amenorrhea with a diet and
training intervention program. Int J Sport Nutr 1996;6:24–40.
180 Kopp-Woodroffe SA, Manore MM, Dueck CA, et al. Energy and nutrient status
of amenorrheic athletes participating in a diet and exercise training intervention
program. Int J Sport Nutr 1999;9:70–88.
181 Mallinson RJ, Williams NI, Olmsted MP, et al. A case report of recovery of menstrual
function following a nutritional intervention in two exercising women with
amenorrhea of varying duration. J Int Soc Sports Nutr 2013;10:34.
182 Bhasin S, Cunningham GR, Hayes FJ, et al. Task Force, Endocrine Society.
Testosterone therapy in men with androgen deficiency syndromes: an endocrine
society clinical practice guideline. J Clin Endocrinol Metab 2010;95:2536–59.
183 Moreira CA, Bilezikian JP. Stress Fractures: concepts and therapeutics. J Clin
Endocrinol Metab 2017;102:525–34.
184 Ruohola JP, Laaksi I, Ylikomi T, et al. Association between serum 25(OH)D
concentrations and bone stress fractures in Finnish young men. J Bone Miner Res
2006;21:1483–8.
185 U.S. Department of Agriculture. USDA national nutrient database for standard
reference. 2011 http://www. ars. usda. gov/ ba/ bhnrc/ ndl.
186 Golden NH, Carey DE. Vitamin D in health and disease in adolescents: when
to screen, whom to treat, and how to treat. Adolesc Med State Art Rev
2016;27:125–39.
187 Holick MF, Binkley NC, Bischoff-Ferrari HA, et al. Endocrine Society. Evaluation,
treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical
practice guideline. J Clin Endocrinol Metab 2011;96:1911–30.
188 Sacheck JM, Van Rompay MI, Chomitz VR, et al. Impact of three doses of Vitamin
D3 on serum 25(OH)D deficiency and insufficiency in at-risk schoolchildren. J Clin
Endocrinol Metab 2017;102:4496–505.
189 Kim BY, Kraus E, Fredericson M, et al. Serum vitamin D levels are inversely associated
with time lost to bone stress injury in a cohort of NCAA Division I distance runners.
Clin J Sport Med 2016:26.
190 Myburgh KH, Hutchins J, Fataar AB, et al. Low bone density is an etiologic factor for
stress fractures in athletes. Ann Intern Med 1990;113:754–9.
191 Nieves JW, Melsop K, Curtis M, et al. Nutritional factors that influence change in
bone density and stress fracture risk among young female cross-country runners. Pm
R 2010;2:740–50.
192 US Department of Health and Human Services. 2015–2020 Dietary guidelines for
Americans. Washington DC: USDA, 2015.
193 Berga SL, Loucks TL. Use of cognitive behavior therapy for functional hypothalamic
amenorrhea. Ann N Y Acad Sci. , 2006:1092, 114–29.
194 Michopoulos V, Mancini F, Loucks TL, et al. Neuroendocrine recovery initiated by
cognitive behavioral therapy in women with functional hypothalamic amenorrhea: a
randomized, controlled trial. Fertil Steril 2013;99:2084–91.
195 Arends JC, Cheung MY, Barrack MT, et al. Restoration of menses with
nonpharmacologic therapy in college athletes with menstrual disturbances: a 5-year
retrospective study. Int J Sport Nutr Exerc Metab 2012;22:98–108.
on 4 June 2018 by guest. Protected by copyright.http://bjsm.bmj.com/Br J Sports Med: first published as 10.1136/bjsports-2018-099193 on 17 May 2018. Downloaded from
697
MountjoyM, etal. Br J Sports Med 2018;52:687–697. doi:10.1136/bjsports-2018-099193
Consensus statement
196 Joy E, Kussman A, Nattiv A. 2016 update on eating disorders in athletes:
a comprehensive narrative review with a focus on clinical assessment and
management. Br J Sports Med 2016;50:154–62.
197 Cobb KL, Bachrach LK, Sowers M, et al. The effect of oral contraceptives
on bone mass and stress fractures in female runners. Med Sci Sports Exerc
2007;39:1464–73.
198 Ducher G, Turner AI, Kukuljan S, et al. Obstacles in the optimization of bone health
outcomes in the female athlete triad. Sports Med 2011;41:587–607.
199 Lopez LM, Chen M, Mullins Long S, et al. Steroidal contraceptives and bone fractures
in women: evidence from observational studies. Cochrane Database Syst Rev
2015;7:CD009849.
200 Lopez LM, Grimes DA, Schulz KF, et al. Steroidal contraceptives: effect on bone
fractures in women. Cochrane Database Syst Rev 2014:CD006033.
201 Misra M, Katzman D, Miller KK, et al. Physiologic estrogen replacement increases
bone density in adolescent girls with anorexia nervosa. Journal of Bone and Mineral
Research 2011;26:2430–8.
202 Ackerman KE, Singhal V, Baskaran C, et al. Transdermal 17-β estradiol has a
beneficial effect on bone parameters assessed using HRpQCT compared to oral
ethinyl estradiol-progesterone combination pills in oligo-amenorrheic athletes: a
randomized controlled trial. Denver, Colorado: ASBMR, 2017.
203 Fazeli PK, Wang IS, Miller KK, et al. Teriparatide increases bone formation and bone
mineral density in adult women with anorexia nervosa. The Journal of Clinical
Endocrinology & Metabolism 2014;99:1322–9.
204 Temme KE, Hoch AZ. Recognition and rehabilitation of the female athlete triad/
tetrad: a multidisciplinary approach. Curr Sports Med Rep 2013;12:190–9.
205 Thompson RA, Sherman RT. Eating disorders in sport. Abingdon, UK: Routledge,
2011.
206 Clausen L, Lübeck M, Jones A. Motivation to change in the eating disorders: a
systematic review. Int J Eat Disord 2013;46:755–63.
207 Arthur-Cameselle JN, Quatromoni PA. Eating disorders in collegiate female athletes:
factors that assist recovery. Eat Disord 2014;22:50–61.
208 Giel KE, Hermann-Werner A, Mayer J, et al. GOAL study group. Eating disorder
pathology in elite adolescent athletes. Int J Eat Disord 2016;49:553–62.
209 Sansone RA, Sansone LA. Eating disorders and psychiatric co-morbidity: prevalence
and treatment modifications. In: Yager J, Power PS, eds. Clinical manual of eating
disorders. Washington DC: American Psychiatric Publishing Inc, 2007:79–112.
on 4 June 2018 by guest. Protected by copyright.http://bjsm.bmj.com/Br J Sports Med: first published as 10.1136/bjsports-2018-099193 on 17 May 2018. Downloaded from
... EA is derived by subtracting exercise energy expenditure from energy intake and dividing by fat-free mass (FFM). EA ≥ 40-45 kcal/kg of FFM is considered to be optimal during the improvement season, supporting performance, training adaptation and health [10]. In contrary, low EA (<30 kcal/kg of FFM) is necessary for weight loss, but may negatively affect the performance, the production of various hormones and bone health [10,11] and thus may lead to a multisyndrome condition called relative energy deficiency in sport (RED-S) [10]. ...
... EA ≥ 40-45 kcal/kg of FFM is considered to be optimal during the improvement season, supporting performance, training adaptation and health [10]. In contrary, low EA (<30 kcal/kg of FFM) is necessary for weight loss, but may negatively affect the performance, the production of various hormones and bone health [10,11] and thus may lead to a multisyndrome condition called relative energy deficiency in sport (RED-S) [10]. Studies investigating weight loss in these athletes have shown that low EA may suppress leptin, triiodothyronine (T3), testosterone, and estradiol concentrations, and increase the incidence of menstrual irregularities, including amenorrhea [12] markers of immunosuppression [13], and adaptive thermogenesis [14]. ...
... EA ≥ 40-45 kcal/kg of FFM is considered to be optimal during the improvement season, supporting performance, training adaptation and health [10]. In contrary, low EA (<30 kcal/kg of FFM) is necessary for weight loss, but may negatively affect the performance, the production of various hormones and bone health [10,11] and thus may lead to a multisyndrome condition called relative energy deficiency in sport (RED-S) [10]. Studies investigating weight loss in these athletes have shown that low EA may suppress leptin, triiodothyronine (T3), testosterone, and estradiol concentrations, and increase the incidence of menstrual irregularities, including amenorrhea [12] markers of immunosuppression [13], and adaptive thermogenesis [14]. ...
Article
Full-text available
As the diet, hormones, amenorrhea, and bone mineral density (BMD) of physique athletes (PA) and gym enthusiasts (GE) are little-explored, we studied those in 69 females (50 PA, 19 GE) and 20 males (11 PA, 9 GE). Energy availability (EA, kcal·kgFFM−1·d−1 in DXA) in female and male PA was ~41.3 and ~37.2, and in GE ~39.4 and ~35.3, respectively. Low EA (LEA) was found in 10% and 26% of female PA and GE, respectively, and in 11% of male GE. In PA, daily protein intake (g/kg body mass) was ~2.9–3.0, whereas carbohydrate and fat intakes were ~3.6–4.3 and ~0.8–1.0, respectively. PA had higher protein and carbohydrate and lower fat intakes than GE (p < 0.05). Estradiol, testosterone, IGF-1, insulin, leptin, TSH, T4, T3, cortisol, or BMD did not differ between PA and GE. Serum IGF-1 and leptin were explained 6% and 7%, respectively, by EA. In non-users of hormonal contraceptives, amenorrhea was found only in PA (27%) and was associated with lower fat percentage, but not EA, BMD, or hormones. In conclusion, off-season dietary intakes, hormone levels, and BMD meet the recommendations in most of the PA and GE. Maintaining too-low body fat during the off-season may predispose to menstrual disturbances.
... If LEA persists, the body is forced to adapt and conserve energy wherever possible by no longer performing nonessential functions such as regular menses, hair growth, mood regulation, or executive thinking, as well as reducing cellular metabolism, weakening the potency of the immune system, and decreasing cardiovascular capacity [57] This conservation process reduces both absolute and relative resting metabolic rates (RMR) to protect the unfavourable breakdown of FFM (metabolically active protein tissue including muscles, bones and organs; [58]. This reduction in RMR can negatively impact both health and performance outcomes [59]. If energy availability falls below optimal levels, metabolically active tissue can breakdown to provide the vital body systems with sufficient energy for survival, leading to even greater decreases in RMR [59]. ...
... This reduction in RMR can negatively impact both health and performance outcomes [59]. If energy availability falls below optimal levels, metabolically active tissue can breakdown to provide the vital body systems with sufficient energy for survival, leading to even greater decreases in RMR [59]. Even the cardiac muscle may be used to produce this energy, with muscle mass and visceral adipose tissue also beginning to atrophy. ...
... Despite the serious consequences of LEA, there is not yet a standardised, reliable and valid assessment protocol for measuring energy availability [59]. Current measurement approaches require specialised equipment and expertise and are burdensome, requiring individuals to keep an excessively accurate food and execise log [59]. ...
Article
Full-text available
Individuals with eating disorders (ED) experience prolonged malnutrition, binge episodes, and compensatory behaviours that affect every organ system. Psychological and physiological symptoms are worsened with comorbid dysfunctional exercise, seen in up to 80% of those with an ED. Although return to exercise is an important component of treatment and recovery, little is known about the contraindications and risks of exercise engagement specific to those with an ED. This paper provides a comprehensive narrative review of the medical and physiological complications of engaging in exercise during ED treatment and outlines when exercise may be contraindicated or used in modified or cautionary ways. We conducted a literature search on MEDLINE, PubMed, and PsychArticles to identify relevant articles, which yielded six categories of medical and physiological complications of ED that may be exacerbated by exercise: energy availability, cardiovascular health, electrolyte abnormalities, biomedical function markers, sex hormones, and body composition. We summarize the evidence for these complications for readers and offer an initial set of recommendations for incorporating exercise during ED treatment based on our findings. This review may serve as a resource for members of ED treatment teams to help evaluate more readily and confidently whether exercise is safe for individual patients and when modifications and caution may be warranted.
... Professional athletes often suffer from energy deficits due to the long hours and intensity of training combined with strict diets for maximum performance. Low energy availability is related to both physiological and psychological disturbances [1]. Psychological problems can include disordered eating patterns, such as obsession with food and restriction or strict control of intake at meals, eating disorders (ED), preoccupation with body shape, depression, irrational behaviour, mood swings, social isolation or a severe level of anxiety [1]. ...
... Low energy availability is related to both physiological and psychological disturbances [1]. Psychological problems can include disordered eating patterns, such as obsession with food and restriction or strict control of intake at meals, eating disorders (ED), preoccupation with body shape, depression, irrational behaviour, mood swings, social isolation or a severe level of anxiety [1]. These may precede or be caused by low energy availability [2]. ...
Article
Full-text available
Low energy availability may precede or be caused by cognitive disturbances in professional athletes. Related psychological problems include disordered eating patterns, body shape preoccupation, depression or anxiety. The objective of this research was to evaluate the effects of different personalised dietary plans on psychological factors in young professional female handball players with low energy availability. This 12-week randomised clinical trial involved 21 female players aged 22 ± 4 years, 172.0 ± 5.4 cm and 68.4 ± 6.7 kg divided into three groups (FD: free diet; MD: Mediterranean diet; HAD: high antioxidant diet). Eating behaviour (Eating Attitude Test, EAT-26: diet, bulimia and oral control subscales), body image (Body Shape Questionnaire, BSQ) and mood state (Profile of Mode State, POMS: tension, vigour, anger, depression, fatigue) were assessed. All participants showed low energy availability (<30 kcal/lean mass per day). The different plans showed no significant differences between them but significant differences over time within groups for the variables: body image, Tension, Vigour and Depression (p < 0.05). Eating behaviour improved slightly but did not show statistically significant changes. Following an adequate nutritional planning for athletes seems to improve the mood and body perception of young female handball players. A longer intervention period is required to assess the differences between diets and improvement of other parameters.
... Competitive distance runners also may be subject to syndromes that compromise bone health. Relative energy deficiency in sport, which includes the female athlete triad (menstrual dysfunction, low energy availability, decreased bone mineral density), is defined by the involvement of many body systems including but not limited to endocrine, gastrointestinal, and cardiovascular [10]. Male athletes can experience their own three-part syndrome making them vulnerable to BSIs [11,12]. ...
... Beyond symptom-related questions, screening for relative energy deficiency in sport, a common syndrome that includes the female athlete triad, is required practice. Although more research is required, the Relative Energy Deficiency in Sport Clinical Assessment Tool (RED-S CAT) is recommended [10,36]. A detailed understanding of the athlete's training schedule and recent changes in that schedule are important. ...
Article
Full-text available
Stress fractures likely have a 1–2% incidence in athletes in general. In runners, a more vulnerable population, incidence rates likely range between 3.2 and 21% with female runners having greater susceptibility. The incidence of femoral shaft stress fractures is less well known. New basic and translational science research may impact the way clinicians diagnose and treat femoral stress fractures. By using a fictitious case study, this paper applies bone science to suggest new approaches to evaluating and treating femoral shaft stress fractures in the running population.
... However, maintaining sufficient energy intake during periods of progressive training is fundamentally difficult, and intentional deficits in carbohydrate intake without corresponding changes in training intensity may result in low energy availability (LEA) and eventual physiological impairment. The health and performance impairments associated with LEA are often reflected in lower energy expenditure (EE) and resting metabolic rate (RMR) [12,13], where these metabolic responses routinely adapt to changes in exercise and dietary intake to conserve energy [14][15][16][17]. ...
Article
Full-text available
Extreme carbohydrate deficits during a ketogenic diet (KD) may result in metabolic adaptations reflective of low energy availability; however, the manifestation of these adaptations outside of exercise have yet to be elucidated in cyclists and triathletes. The purpose of this study is to investigate the chronic and postprandial metabolic responses to a KD compared to a high-carbohydrate diet (HCD) and habitual diet (HD) in trained competitive cyclists and triathletes. For this randomized crossover trial, six trained competitive cyclist and triathletes (F: 4, M: 2) followed an ad libitum KD and HCD for 14 d each after their HD. Fasting energy expenditure (EE), respiratory exchange ratio (RER), and fat and carbohydrate oxidation (FatOx and CarbOx, respectively) were collected during their HD and after 14 d on each randomly assigned KD and HCD. Postprandial measurements were collected on day 14 of each diet following the ingestion of a corresponding test meal. There were no significant differences in fasting EE, RER, FatOx, or CarbOx among diet conditions (all p > 0.050). Although postprandial RER and CarbOx were consistently lower following the KD meal, there were no differences in peak postprandial RER (p = 0.452), RER incremental area under the curve (iAUC; p = 0.416) postprandial FatOx (p = 0.122), peak FatOx (p = 0.381), or FatOx iAUC (p = 0.164) between the KD and HD meals. An ad libitum KD does not significantly alter chronic EE or substrate utilization compared to a HCD or HD; postprandial FatOx appears similar between a KD and HD; this is potentially due to the high metabolic flexibility of cyclists and triathletes and the metabolic adaptations made to habitual high-fat Western diets in practice. Cyclists and triathletes should consider these metabolic similarities prior to a KD given the potential health and performance impairments from severe carbohydrate restriction.
Article
Full-text available
Background: Nutrition in sport is a priority; it is the basis for maintaining optimal health and a prerequisite for the high performance necessary for competitions. The aim of this study was to assess low energy availability and its possible consequences among female triathletes by using the Low Energy Availability in Females Questionnaire (LEAF-Q). Methods: The study involved 30 female triathetes. The LEAF-Q was used in the study. An analysis of the body composition was carried out with the seca device mBCA 515 medical Body Composition Analyzer. Results: Of the 30 female triathletes studied, 23.3% had a monthly cycle disorder, defined as an amenorrhea state for more than 90 days. No differences were found in injury rates or training days lost to injury due to menstrual disturbances. Menstruation changes were significantly greater due to increases in exercise intensity, frequency, and duration in the group experiencing menstrual disturbances (85.7 [95% CIs: 42.1–99.6] vs. 8.7 [95% CIs: 1.1–28.0]). The menstrual disorder group had a greater incidence of their periods stopping for more than 3 months than the group without menstrual disturbances. Conclusions: The female triathletes did not show abnormalities in body weight or composition, and these were not related to the incidence of menstrual disturbances. However, 20% of the triathletes either had, at the time of the study, or had had in the past monthly cycle disorders that could indicate an immediate risk of low energy availability. The LEAF-Q identified 10% of the triathletes as at risk (score > 8) of low energy availability and the physiological and performance consequences related to relative energy deficiency in sports (RED-S).
Article
Objective: To estimate the ratio of menstrual abnormalities, infertility, and other problems related to pregnancy and childbirth in former long-distance runners. We hypothesized that the female athlete triad during an athletic career affects future fertility and childbearing in former athletes. Design: Cross-sectional study. Setting: Participants of the All Japan University Women's Ekiden. Participants: Female former athletes who competed at national level were asked to complete the questionnaire; 137 valid responses were obtained. Independent variables: Age at menarche and at the onset of pregnancy, history of amenorrhea and gynecological disorders, and lowest body mass index (BMI) during their athletic career. Main outcome measures: Menstrual status, history of pregnancy and childbirth, any related infertility treatment and problems, and history of stress fractures. Results: The mean age at menarche was 13.3 ± 2.2 (range, 10-25) years. Five athletes (3.6%) had primary amenorrhea. Eleven of the 137 participants (8.0%) required treatment for infertility. Sixty participants had 121 pregnancies, of which 5 were yet to deliver during the survey. Fifteen of 116 pregnancies (12.9%) ended in miscarriage, induced abortion, or stillbirth. Logistic regression analysis showed that the factors related to "infertility treatment" were age at the onset of pregnancy (P = 0.047) and higher BMI during their athletic career (P = 0.032; odds ratio, 2.19). Conclusions: The main factor influencing infertility was an older age at the time of pregnancy, similar to that observed in the general population. Amenorrhea or being underweight during their athletic career was not associated with problems related to conception and childbirth.
Article
Full-text available
Purpose The aim of this case report was to describe the sleep responses in a male combat sport athlete, who was engaging in both chronic (CWL) and acute (AWL) weight loss practices in order to reduce body mass for a national competition. Methods During the first seven weeks of training (Phases 1 and 2), the athlete adhered to a daily energy intake (EI) equating to their resting metabolic rate (1700 kcal·day ⁻¹ ) followed by a reduction in EI (1200–1300 kcal·day ⁻¹ ) in the 5 days before weighing in (Phase 3). Nocturnal sleep was monitored throughout the 8-week training period using wristwatch actigraphy and frequent measurements of body mass/composition, daily exercise energy expenditure and training load (TL) were taken. Results The athlete was in a state of low energy availability (LEA) during the entire training period. There was a very large decrease in LEA status during phase 3 compared with phases 1 and 2 (3 vs. 20 kcal·kgFFM·day ⁻¹ ) and there was a small decrease in TL during phase 3 compared with phase 2 (410 vs. 523 AU). The athlete's sleep efficiency increased throughout the training period, but total sleep time displayed a small to moderate decrease in phase 3 compared with phases 1 and 2 (386 vs. 429 and 430 min). However, correlational analysis demonstrated trivial to small, non-significant relationships between sleep characteristics and the athlete's LEA status and TL. Conclusion These findings suggest that CWL and AWL practices that cause fluctuations in LEA and TL may be implemented without compromising the sleep of combat sport athletes.
Article
Full-text available
Low energy availability (EA) is suspected to be the underlying cause of both the Female Athlete Triad and the more recently defined syndrome, Relative Energy Deficiency in Sport (RED-S). The International Olympic Committee (IOC) defined RED-S as a syndrome of health and performance impairments resulting from an energy deficit. While the importance of adequate EA is generally accepted, few studies have attempted to understand whether low EA is associated with the health and performance consequences posited by the IOC. Objective The purpose of this cross-sectional study was to examine the association of low EA with RED-S health and performance consequences in a large clinical population of female athletes. Methods One thousand female athletes (15–30 years) completed an online questionnaire and were classified as having low or adequate EA. The associations between low EA and the health and performance factors listed in the RED-S models were evaluated using chi-squared test and the odds ratios were evaluated using binomial logistic regression (p<0.05). Results Athletes with low EA were more likely to be classified as having increased risk of menstrual dysfunction, poor bone health, metabolic issues, haematological detriments, psychological disorders, cardiovascular impairment and gastrointestinal dysfunction than those with adequate EA. Performance variables associated with low EA included decreased training response, impaired judgement, decreased coordination, decreased concentration, irritability, depression and decreased endurance performance. Conclusion These findings demonstrate that low EA measured using self-report questionnaires is strongly associated with many health and performance consequences proposed by the RED-S models.
Article
Full-text available
We aimed to (1) report energy availability (EA), metabolic/reproductive function, bone mineral density (BMD) and injury/illness rates in national/world-class female and male distance-athletes; and (2) investigate the robustness of various diagnostic criteria from the Female Athlete Triad (Triad), Low Energy Availability in Females Questionnaire (LEAF-Q) and Relative Energy Deficiency in Sport (RED-S) tools to identify risks associated with low EA. Athletes were distinguished according to benchmarks of reproductive function (amenorrheic [n=13] vs eumenorrheic [n=22]; low [lowest quartile of reference range, n=10] vs normal testosterone [n=14]) and EA calculated from 7-day food and training diaries (< or >30 kcal.kg-1FFM). Sex hormones (p<0.001), triiodothyronine (p<0.05) and BMD (females, p<0.05) were significantly lower in amenorrheic (37%) and low testosterone (40%; 15.1±3.0 nmol/L-1) athletes and bone injuries were ~4.5-fold more prevalent in amenorrheic (ES=0.85; large) and low testosterone (ES=0.52; moderate) groups compared to others. Categorization of females and males using Triad or RED-S tools revealed that higher risk groups had significantly lower T3 (female and male Triad and RED-S:p<0.05) and higher number of all-time fractures (male Triad:p<0.001; male RED-S and female Triad:p<0.01) as well as non-significant but markedly (up to 10-fold) higher number of training days lost to bone injuries during the preceding year. Based on the cross-sectional analysis, current reproductive function (questionnaires/blood hormone concentrations) appears to provide a more objective and accurate marker of optimal energy for health than the more error-prone and time-consuming dietary and training estimation of EA. This study also offers novel findings that athlete health is associated with EA indices.
Article
Full-text available
Objective Establish the prevalence of illness symptoms, poor sleep quality, poor mental health symptoms, low energy availability and stress-recovery state in an Olympic cohort late in the 3 months prior to the Summer Olympic Games. Methods Olympic athletes (n=317) from 11 sports were invited to complete questionnaires administered 3 months before the Rio 2016 Olympic Games. These questionnaires included the Depression, Anxiety and Stress Questionnaire, Perceived Stress Scale, Dispositional Resilience Scale, Recovery-Stress Questionnaire (REST-Q-52 item), Low Energy Availability in Females Questionnaire (LEAF-Q), Epworth Sleepiness Scale, Pittsburgh Sleep Quality Index and custom-made questionnaires on probiotic usage and travel. Multiple illness (case) definitions were applied. ORs and attributable fractions in the population were used. Factor analyses were used to explore the relationships between variables. Results The response rate was of 42% (male, n=47, age 25.8±4.1 years; female, n=85, age 24.3±3.9 years). Low energy availability was associated with sustaining an illness in the previous month (upper respiratory, OR=3.8, 95% CI 1.2 to 12). The main factor relating to illness pertained to a combination of anxiety and stress-recovery states (as measured by the REST-Q-52 item). All participants reported at least one episode of illness in the last month (100% prevalence). Conclusions All participants reported at least one illness symptom in the previous month. Low energy availability was a leading variable associated with illness in Olympic-class athletes. The estimates duration of symptoms ranged from 2 to 7 days. Factor analyses show the interdependence of various health domains and support multidisciplinary care.
Article
Full-text available
In a high-performance sports environment, athletes can present with low energy availability (LEA) for a variety of reasons, ranging from not consuming enough food for their specific energy requirements to disordered eating behaviors. Both male and female high-performance athletes are at risk of LEA. Longstanding LEA can cause unfavorable physiological and psychological outcomes which have the potential to impair an athlete’s health and sports performance. This narrative review summarizes the prevalence of LEA and its associations with athlete health and sports performance. It is evident in the published scientific literature that the methods used to determine LEA and its associated health outcomes vary. This contributes to poor recognition of the condition and its sequelae. This review also identifies interventions designed to improve health outcomes in athletes with LEA and indicates areas which warrant further investigation. While return-to-play guidelines have been developed for healthcare professionals to manage LEA in athletes, behavioral interventions to prevent the condition and manage its associated negative health and performance outcomes are required.
Article
Full-text available
Objective We investigated the daily dose of vitamin D needed to achieve serum 25-hydroxyvitamin D [25(OH)D] sufficiency among schoolchildren at-risk for deficiency. Study Design The Daily D Health Study was a randomized double-blind vitamin D supplementation trial among racially/ethnically diverse schoolchildren (n=685) in the northeastern U.S. Children were supplemented with vitamin D3 at 600, 1000, or 2000 IU/day for six months. Measurements included serum 25(OH)D at baseline (Oct-Dec), 3 months (Jan-March), 6 months (April-June), and 12 months (6 months post-supplementation). Results At baseline, mean ± SD serum 25(OH)D was 22.0 ± 6.8 ng/mL; with 5.5% severely vitamin D deficient (<12 ng/mL), 34.1% deficient (12-19 ng/mL), 49.0% insufficient (20-29 ng/ml), and 11.4% sufficient (≥30 ng/mL). The lowest levels of serum 25(OH)D were found among black (17.9 ± 6.7 ng/mL) and Asian children (18.9 ± 4.8 ng/mL), with no baseline differences by weight status. Serum 25(OH)D increased over 6 months in all three dose groups. The 2000 IU group achieved higher mean serum 25(OH)D than the other two dose groups (33.1 versus 26.3 and 27.5 ng/mL; p<0.001), with 59.9% of this group attaining sufficiency at 3 months and only 5.3% remaining severely deficient/deficient at 6 months. All dose groups demonstrated a fall in 25(OH)D at 12 months. Conclusions Children who are at risk for vitamin D deficiency benefit from daily sustained supplementation of 2000 IU/day compared to lower doses closer to the current RDA for vitamin D intake. This benefit occurred over the winter months when serum 25(OH)D levels tend to fall.
Article
Full-text available
Introduction: Secondary functional hypothalamic amenorrhea (SFHA) is common among female athletes, especially in weight-sensitive sports. The aim of this study was to investigate the link between SFHA and neuromuscular performance in elite endurance athletes. Methods: Sixteen eumenorrheic (EUM) and 14 SFHA athletes from national teams and competitive clubs participated. Methods included gynecological examination; body composition (DXA);; resting metabolic rate and work efficiency; exercise capacity; knee muscular strength (KMS) and knee muscular endurance (KME); reaction time (RT); blood sampling performed on the 3rd-5th day of the menstrual cycle, and 7-day assessment of energy availability. Results: SFHA athletes had lower estrogen (0.12 ±0.03 vs. 0.17 ±0.09 nmol/L, p<0.05), triiodothyronine (T3) (1.4 ±0.2 vs. 1.7 ±0.3 nmol/L, p<0.01), and blood glucose (3.8 ±0.3 vs 4.4 ±0.3 mmol/L, p<0.001) but higher cortisol levels (564 ±111 vs. 400 ±140 nmol/L, p<0.05) compared to EUM athletes. SFHA had a lower body weight (55.0 ±5.8 vs. 60.6 ±7.1 kg, p<0.05), but no difference in exercise capacity between groups was found (56.4 ±5.8 vs. 54.0 ±6.3 ml O2/min/kg). RT was 7% longer, and KMS and KME were 11% and 20% lower compared to EUM athletes. RT was negatively associated with glucose (r=-0.40, p<0.05), T3 (r=-0.37, p<0.05) and estrogen (r=-0.43, p<0.05), but positively associated with cortisol (r=0.38, p<0.05). KMS and KME correlated with fat free mass in the tested leg (FFMleg)(r=0.52, p<0.001; r=0.58, p<0.001) but were negatively associated with cortisol (r=-0.42, p<0.05; r=-0.59, p<0.001). FFMleg explained differences in KMS, while reproductive function and FFMleg independently explained the variability in KME. Conclusion: We found lower neuromuscular performance among SFHA compared to EUM athletes linked to a lower FFMleg, glucose, estrogen, T3 and elevated cortisol levels.
Article
To investigate the relationship between energy availability (dietary energy intake minus energy expended during exercise) and thyroid metabolism, we studied 27 untrained, regularly menstruating women who performed approximately 30 kcal.kg lean body mass (LBM)-1.day-1 of supervised ergometer exercise at 70% of aerobic capacity for 4 days in the early follicular phase. A clinical dietary product was used to set energy availability in four groups (10.8, 19.0, 25.0, 40.4 kcal.kg LBM-1.day-1). For 9 days beginning 3 days before treatments, blood was sampled once daily at 8 A.M. Initially, thyroxine (T4) and free T4 (fT4), 3,5,3'-triiodothyronine (T3) and free T3 (fT3), and reverse T3 (rT3) were in the normal range for all subjects. Repeated-measures one-way analysis of variance followed by one-sided, two-sample post hoc Fischer's least significant difference tests of changes by treatment day 4 revealed that reductions in T3 (16%, P < 0.00001) and fT3 (9%, P < 0.01) occurred abruptly between 19.0 and 25.0 kcal.kg LBM-1.day-1 and that increases in fT4 (11%, P < 0.05) and rT3 (22%, P < 0.01) occurred abruptly between 10.8 and 19.0 kcal.kg LBM-1.day-1. Changes in T4 could not be distinguished. If energy deficiency suppresses reproductive as well as thyroid function, athletic amenorrhea might be prevented or reversed by increasing energy availability through dietary reform to 25 kcal.kg LBM-1.day-1, without moderating the exercise regimen.
Article
Introduction: Chronic reductions in energy availability (EA) suppress reproductive function. A particular calculation of EA quantifies the dietary energy remaining after exercise for all physiological functions. Reductions in LH pulse frequency have been demonstrated when EA using this calculation is < 30 kcal/ kg ffm·d. Purpose: We determined whether menstrual disturbances (MD) are induced when EA is < 30 kcal/ kg ffm·d. Methods: Thirty-five sedentary, ovulatory women 18-24 yr (weight= 59.0 ± 0.8 kg, BMI= 21.8 ± 0.4 kg·m) completed a diet and exercise intervention over three menstrual cycles. Participants were randomized to groups that varied in the magnitude of negative energy balance created by the combination of exercise and energy restriction. MD were determined using daily urinary estrone-1-glucuronide (E1G) and pregnanediol glucuronide (PdG), mid-cycle LH, and menstrual calendars. In a secondary analysis, we calculated EA from energy balance data and tested the association of EA with menstrual disturbances. Results: A generalized linear mixed-effects model showed that the likelihood of a MD decreased by 9% for each unit increase in EA (odds ratio 0.91, 0.84 - 0.98, 95% CI, P=0.010). No specific value of EA emerged as a threshold below which MD were induced. When participants were partitioned into EA tertile groups (Low EA =23.4-34.1; n=11, Moderate EA =34.9-40.7; n=12, and High EA =41.2-50.1; n=12 (kcal/ kg ffm·d)), E1G (p<0.001), PdG (p<0.001), and luteal phase length (p=0.031) decreased significantly, independent of tertile. Conclusion: These findings do not support that a threshold of EA exists below which MD are induced but do suggest that MD increase linearly as EA decreases. MD can likely be prevented by monitoring EA using a simplified assessment of metabolic status.
Article
Background: The short-term effects of low energy availability (EA) on bone metabolism in physically active women and men are currently unknown. Purpose: We evaluated the effects of low EA on bone turnover markers (BTMs) in a cohort of women and a cohort of men, and compared effects between sexes. Methods: These studies were performed using a randomised, counterbalanced, crossover design. Eleven eumenorrheic women and eleven men completed two 5-day protocols of controlled (CON; 45kcal·kgLBM-1·d-1) and restricted (RES; 15kcal·kgLBM-1·d-1) EAs. Participants ran daily on a treadmill at 70% of their peak aerobic capacity (VO2 peak) resulting in an exercise energy expenditure of 15kcal·kgLBM-1·d-1 and consumed diets providing 60 and 30kcal·kgLBM-1·d-1. Blood was analysed for BTMs [β-carboxyl-terminal cross-linked telopeptide of type I collagen (β-CTX) and amino-terminal propeptide of type 1 procollagen (P1NP)], markers of calcium metabolism [parathyroid hormone (PTH), albumin-adjusted calcium (ACa), magnesium (Mg) and phosphate (PO4)] and regulatory hormones [sclerostin, insulin-like growth factor 1 (IGF-1), triiodothyronine (T3), insulin, leptin, glucagon-like-peptide-2 (GLP-2)]. Results: In women, β-CTX AUC was significantly higher (P=0.03) and P1NP AUC was significantly lower (P=0.01) in RES compared to CON. In men, neither β-CTX (P=0.46) nor P1NP (P=0.12) AUCs were significantly different between CON and RES. There were no significant differences between sexes for any BTM AUCs (all P values>0.05). Insulin and leptin AUCs were significantly lower following RES in women only (for both P=0.01). There were no differences in any AUCs of regulatory hormones or markers of calcium metabolism between men and women following RES (all P values>0.05). Conclusions: When comparing within groups, five days of low EA (15kcal·kgLBM-1·d-1) decreased bone formation and increased bone resorption in women, but not in men, and no sex specific differences were detected.