Maturitas 75 (2013) 107–112
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Maturitas
journal homepage: www.elsevier.com/locate/maturitas
Review
Long term consequences of the female athlete triad
Jill Thein-Nissenbaum ∗
Physical Therapy Program, School of Medicine and Public Health, University of Wisconsin-Madison, 5173 Medical Sciences Center,
1300 University Avenue, Madison, WI 53706-1532, USA
a r t i c l e
i n f o
Article history:
Received 19 February 2013
Accepted 21 February 2013
Keywords:
Disordered eating
Menstrual irregularity
Bone mineral density
Anorexia nervosa
Bulimia nervosa
a b s t r a c t
In the past 40 years, female sports participation, particularly at the high school level, has significantly
increased. Physical activity in females has numerous positive benefits, including improved body image
and overall health. Unfortunately, a select population of exercising females may experience symptoms
related to the female athlete triad, which refers to the interrelatedness of energy availability, menstrual function, and bone mineral density. Clinically, these conditions can manifest as disordered eating
behaviors, menstrual irregularity, and stress fractures. Triad symptoms are distributed along a spectrum
between optimal health and disease; all of the components of the triad may not be affected simultaneously.
The female athlete triad was first identified in 1992. Since that time, a vast amount of research related
to the identification, management and prevention of this condition has been published. More recently,
research related to the long term effects of triad components has come into light. Women who were
diagnosed with female athlete triad syndrome as adolescents and young adults in the 1990s are now in
their 30s and 40s; negative long term effects of the female athlete triad, such as low bone mineral density,
are now starting to manifest.
Women of all ages should be assessed for triad components during routine annual physical examinations; appropriate measures to treat any current triad components should be implemented. In addition,
women in their 30s, 40s and early 50s should be screened for a history of the female athlete triad.
Multidisciplinary management of these conditions is strongly recommended.
© 2013 Elsevier Ireland Ltd. All rights reserved.
Contents
1.
2.
3.
4.
5.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Components of the female athlete triad energy availability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Long term affects of the female athlete triad . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Management of the long term affects of the female athlete triad . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Contributors and their role . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Competing interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Role of funding source . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Provenance and peer review . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction
Since the passage of Title IX in 1972, the United States has
seen girls’ participation in sports dramatically increase. Prior to its
∗ Tel.: +1 608 263 6354; fax: +1 608 262 7809.
E-mail address: thein@pt.wisc.edu
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http://dx.doi.org/10.1016/j.maturitas.2013.02.010
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implementation, girls comprised 7% of high school athletes.
Currently, girls comprise 42% of high school athletes [1].
Numerous benefits to female sports participation have been
observed; overall, the benefits of exercise far outweigh the risks [2].
However, in 1992, an association between disordered eating, amenorrhea, and osteoporosis in athletes was identified; the condition
was coined the female athlete triad (triad). The American College of Sports Medicine (ACSM) published a Position Stand on the
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Opmal energy
availability
Opmal bone
health
Eumenorrhea
Reduced energy availability
with or without
Disordered Eang
Subclinical
Menstrual
Disorders
Low BMD
Low energy availability
with or without
an Eang Disorder
Funconal
Hypothalamic
Amenorrhea
Osteoporosis
Fig. 1. Female athlete triad. The spectrums of energy availability, menstrual function, and bone mineral density.
condition in 1997 [3] and updated the Position Stand in 2007 [2].
One of the 2007 revisions was a change in terminology. Clinicians
and researchers soon realized that the terms disordered eating,
amenorrhea, and osteoporosis were too restrictive; females with
less severe conditions were not recognized as having the triad.
Therefore, the 2007 Position Stand boasts broader definitions along
a spectrum of energy availability, menstrual function, and bone mineral density. With these new definitions, more athletes are now
recognized as suffering from triad components [2] (Fig. 1).
A significant amount of research on the triad at the high school
level [4–9] and in the collegiate and elite female athlete populations
[10–12] exists. Women first identified as having triad-related conditions in the mid-1990s are now presenting with negative long
term consequences. Although no literature to date has examined
females for the long term consequences of the triad in its entirety,
research related to the long term effects of the individual components of the triad exists. Therefore, the purpose of this paper is to
review the latest research on the long term consequences of low
energy availability, menstrual irregularity, and low bone mass in
female athletes.
2. Components of the female athlete triad energy
availability
a. Energy availability
Energy availability is energy intake minus energy expenditure. The post-exercise energy is utilized for the regulation of
bodily functions, including tissue healing, cardiovascular functioning and menstruation [2,11]. Energy availability ranges from
optimal energy availability to low energy availability; low energy
availability may occur intentionally or unintentionally [2] (Fig. 1).
For example, some athletes may intentionally restrict caloric
intake while others may fall into a negative energy balance
because they are unaware of their caloric needs [13,14]. Intentional energy reduction occurs through excessive exercise, by
dramatically decreasing caloric intake, or by combining both methods. Intentional caloric restriction often manifests as disordered
eating (DE), which may involve restrictive eating, fasting, skipping meals, or use of diet pills, laxatives, diuretics, or binge-eating
followed by purging [2,11,13,15]. Specific sub-categories of DE
include anorexia nervosa (AN), bulimia nervosa (BN), and eatingdisorders not otherwise specified (EDNOS). These eating disorders
are all characterized by a significant preoccupation with weight and
shape [16]. Research suggests that, regardless of when unhealthy
eating attitudes and behaviors manifest, the behaviors are formed
during adolescence [17–19].
Anorexia nervosa is a serious psychiatric illness; criteria for the
diagnosis of AN includes refusal to maintain a minimal body weight
(less than 85% of expected), intense fear of weight gain and distorted body image [16]. Unfortunately, the outcome is poor; only
46% of patients fully recover from AN; 20% remain chronically ill
[21]. The prevalence of AN is listed in Table 1.
Bulimia nervosa is characterized by periods of fasting and dieting interrupted by binge eating and a feeling of a loss of control [16].
Binging is compensated for by self-induced vomiting, laxative, or
diuretic abuse. Criteria for BN requires a minimum frequency of 2
binges per week. Unlike AN, BN criteria involving binge duration
and food consumption are questionable. The prevalence of BN is
listed in Table 1.
Eating disorder not otherwise specified (EDNOS) is a catchall
diagnosis for patients with significant features of eating disorders
that do not meet the criteria for AN or BN. Although this category
is considered a “residual” category, it is the most common eating
disorder diagnosed. The behaviors which lead to the diagnosis of
EDNOS are oftentimes difficult to determine as they are typically
assessed via self-report. The prevalence of DE among various populations, determined by the use of surveys or food diaries, is listed
in Table 1.
b. Menstrual function
According to the 2007 Position Stand, menstrual function occurs
along a spectrum, ranging from eumenorrhea, or normal menses, to
amenorrhea [2] (Fig. 1). Menstrual dysfunction, often called menstrual irregularity (MI), includes primary amenorrhea, secondary
amenorrhea, and oligomenorrhea [2]. Primary amenorrhea is a
delay in menarche; the defining age for primary amenorrhea is 15
J. Thein-Nissenbaum / Maturitas 75 (2013) 107–112
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Table 1
Prevalence of disordered eating behaviors in various populations.
Anorexia nervosa
Adolescent/teenage females
Adult females
Collegiate or adult elite female athletes
0.2–1.0%
1.2–2.2%
[2,4]. Secondary amenorrhea is a cessation of menstruation for 3
consecutive months in the post-menarche female. Oligomenorrhea
is menstrual cycles occurring greater than 35 days apart [2].
Determining the prevalence of MI in the adolescent population
comes with challenges; MI immediately post-menarche is common. However, normalization of menstruation occurs within 2
years of menarche in 90% of females [24]. The prevalence of MI
in girls > 2 years post-menarche has been reported to range from
18.8 to 54% [6,7,9,22,23]. Lean build athletes and aesthetic athletes
(cheerleading, pom-pon squad, dance team, diving and gymnastics) have a significantly higher prevalence of MI-26.7% and 28.2%
respectively-when compared to general high school athletes [9,22].
The prevalence of secondary amenorrhea has been reported to be
as high as 65% in elite long-distance runners compared to 2–5% in
the general population [25]. Although primary amenorrhea prevalence is less than 1% in the general population, the prevalence in
collegiate cheerleading, diving and gymnastics athletes has been
reported to be as high as 22% [14,26,27].
c. Bone mineral density
Bone mineral density (BMD) occurs across a spectrum, ranging
from optimal bone health to osteoporosis [2] (Fig. 1). Osteopenia and osteoporosis are well-defined terms in post-menopausal
women; osteopenia is a bone mineral density (BMD) T-score
between −1.0 and −2.5, and osteoporosis is a T-score of less than
−2.5 [28]. However, T-scores scores are not be used in adolescent
and pre-menopausal females. The International Society for Clinical
Densitometry (ISCD) recommends that BMD in this population be
expressed as Z-scores, as these scores compare individuals to age
and sex-matched controls. Any Z-score lower than −2.0 is defined
as “low bone density for chronological age” in adolescent and premenopausal females [28].
An athlete’s BMD reflects numerous variables, including energy
availability, menstrual status, genetic composition and environmental factors. Therefore, a one-time “snapshot” of BMD in the
adolescent or pre-menopausal female may not provide as much
information as does changes over time [2,29]. As such, studies
related to BMD in the young female population are limited [6,7].
The prevalence of low bone mass in 170 high school females was
determined to be 21.8% [7]. In 80 high school female athletes, 13%
had a Z-score between −1.0 and −1.9, and 3% had a Z-score of ≤2.0
[6]. In addition, 19% reported a history of a stress fracture. These
findings are concerning; athletes participating in weightbearing
sports should have BMD 12–15% higher than sedentary controls;
this was not the case in this study [6].
3. Long term affects of the female athlete triad
Adolescence is a period of growth, development and maturation of numerous systems, especially the reproductive and skeletal
systems. Approximately 50% of peak bone mass is acquired during adolescence; the greatest increase is between 11 and 14 years
[20]. Women attain > 95% of their total BMD by age 18 [30]. Peak
bone mass attainment is site specific; peak bone mass accrual at the
femoral neck occurs by age 16, but in the lumbar spine, bone mass
continues to increase into the third decade of life [30]. Bone mass
acquisition involves the interaction of numerous hormones and
environmental factors, including dietary habits and physical activity [30]. The amount of skeletal mass acquired during adolescence
Bulimia nervosa
0.3%
1.0–2.0%
Eating disorder not otherwise specified
18.2–36.0%
15.2–32.4%
is one of the most important factors in determining osteoporosis
and fracture risk later in life [30]. These important events, unfortunately, coincide with the peak time for the development of eating
disorders [20].
Adolescent eating disorders have a high rate of medical complications [16]. Adolescents with AN are reported to have lower
Z-scores when compared to their healthy peers; the prevalence of
Z-scores of <−1 at the spine and hip was 50% and 30%, respectively [31]. When adolescent females with AN are followed over
a year, their bone mass accrual plateaus as compared to their
healthy peers, who show a continued increase [32]. Females with
AN who increased their body mass index (BMI) by 10% and resumed
menses over a 12-month period showed improved BMD, although
it remained less than controls [31,33].
When adult women with AN were examined for bone loss, those
with an onset of amenorrhea before age 18 had lower BMD than
those who developed amenorrhea after age 18, even after controlling for duration of amenorrhea [34]. These findings confirm the
importance of adolescent bone mass accrual.
Unfortunately, bone density may not improve with weight gain
and resumption of menses. In a study of 19 women with adolescentonset AN who had completely recovered from AN for 21 years, bone
density at the femur was lower than in controls; lumbar spine
BMD was no different than controls [35]. These findings mirror
the site-specific acquisition of bone; peak bone mass for the femur
occurs during adolescence whereas lumbar spine peak bone mass
is acquired later [30].
Another potential reason for site-specific gains in BMD in
women who have recovered from AN is related to bone type.
Because of the association between hypogonadism and decreased
trabecular bone density, resumption of menses may improve bone
density at trabecular-rich sites, such as the spine [34,36]. Cortical
bone density is reliant upon BMI and lean body mass, both of which
may remain low, even if the female has recovered from AN [35,37].
This offers a second explanation as to why cortical bone density
changes are less remarkable in patients with AN, even after they
have recovered [34,35,38].
When females with BN are of normal weight and have no history
of AN or amenorrhea, their bone density is similar to that of controls [39]. Exercising bulimic women may have higher BMD than
those who do not [40]. Other studies have refuted these findings
and determined that women with BN and EDNOS have significantly
lower BMD than controls [41]. In patients with AN, BN and EDNOS,
all 3 groups had decreased BMD; the findings were worst in the
EDNOS subgroup [42].
Looking more specifically at the EDNOS subgroup, adolescent
female competitive runners completed questionnaires regarding
eating behaviors and menstrual history and were assessed for BMD
[43]. Runners with “elevated dietary restraint” – a sub-category
of the eating questionnaire – had a significantly greater incidence
of low BMD than runners without elevated restraint. These findings suggest that dietary restraint may be the DE behavior most
associated with negative bone health in adolescent female runners
[43].
In a study of 91 female distance runners between the ages of 18
and 26, Cobb et al. examined the relationship between DE, MI and
BMD [10]. The authors determined that DE was associated with low
BMD, even in the absence of menstrual irregularity [10].
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Table 2
Barriers to bone mass acquisition in adolescence.
Decrease in lean body mass and body mass index (BMI)a
Hypogonadism
Hypercortisolemia
Malnutrition (such as low protein intake)
Low levels of insulin-like growth factor
Alterations in appetite-regulating hormones (leptin, peptide YY)
a
[16,20].
These findings – suboptimal Z-scores and low BMD in adolescent
and young females with DE behaviors – are alarming. The majority of bone mass is accumulated in adolescence; eating disorders
result in low energy availability and interfere with normal bone
acquisition, which can lead to permanent deficits [16]. Adolescents
with DE are at greater risk for the development of osteopenia or
osteoporosis; this is associated with fracture risk in adulthood 2–7×
higher than the adolescent without an eating disorder, especially
in non-spine fractures [16,44]. This would correlate with previous
data suggesting cortical bone recovers less than trabecular bone
[34,35,38].
Numerous factors contribute to the reduction in bone mass seen
in adolescents with DE and are summarized in Table 2. The most
important factor counteracting bone loss in adolescents with DE is
normalization of body weight [16].
The rate of suicide and suicide attempts is increased in individuals with eating disorders. Approximately 10–20% of patients with
AN report a suicide attempt; approximately 25–35% of patients
with BN report attempted suicide [16]. Approximately 5–6% of
women with AN suffer a premature death [16]. The mortality ratios
for women with AN, BN and EDNOS are 5.86, 1.93, and 1.92, respectively [21].
Menstrual function, the second triad component, has been
examined for its long-term effects. Women with previous secondary amenorrhea had significantly lower BMD in the pelvis and
lumbar spine than those with previous oligomenorrhea. The most
important counteraction at follow up with high physical activity
and BMI ≥ 22 [45]. Of 577 adolescent females aged 14–19 years
who were examined, those with oligomenorrhea at initial presentation were almost 3 times more likely to have oligomenorrhea at
follow-up [46].
As previously reported, a big concern related to adolescent low
bone mass is the risk these individuals run in attaining peak BMD in
adulthood. Barrack et al. [47] examined 40 female adolescent runners with low bone mass without an eating disorder; subjects were
followed over a 3-year period. The authors discovered that approximately 90% of girls with low bone mass at baseline also had low
bone mass at the 3-yr follow-up. Factors including higher training
levels, older age and older age at menarche were negatively associated with the change in BMD. The authors concluded that “catching
up” bone mass may be difficult. This study highlights factors other
than DE and menstruation as contributing to low BMD [47].
In a similar study, bone mass accrual among a cross-sectional
sample of 93 female adolescent runners and 90 girls participating
in a non-endurance running sport was determined [5]. Although
bone mass rose at all sites in the non-runners between the ages
of 13–14 years and 17–18 years, no such increase was noted in
the runners. Runners exhibited significantly lower Z-scores among
the older (16–18 years) but not younger (13–15 years) age groups.
These findings suggest that the runners, in contrast to the nonrunners, exhibited a suppressed bone accrual pattern. This supports
the notion that female adolescent endurance runners may be at risk
for inadequate bone mass gains and thus a low peak BMD [5].
Because of negative long term consequences of sustaining a
musculoskeletal injury at a younger age, and the increased prevalence of injuries in females as compared to males, research has
examined the relationship between triad components and injury
[8]. Of the 3 components, menstrual dysfunction exhibited the
strongest relationship to injury [8]. In a study of 249 high school
female athletes, those who reported MI sustained a higher percentage of severe injuries than did athletes who reported normal
menses [48]. The relationship among DE, MI, low BMD and musculoskeletal injury among 163 female high school athletes was
assessed; all three triad components were associated with musculoskeletal injuries [8]. These studies highlight the association
of triad components and musculoskeletal injury. The long-term
effects of sustaining an injury can be devastating; it may require
the athlete to modify activity or cease exercising altogether. This
can lead to negative systemic effects such as obesity, hypertension
and diabetes.
4. Management of the long term affects of the female
athlete triad
All of the components of the female athlete triad-energy availability, menstrual function, and bone density-appear to have a
negative long-term effect on bone. Negative energy balance and
poor diet cause a decrease in calcium and vitamin D, both essential for bone acquisition. With a lack of energy, numerous bodily
systems, including the reproductive system, go into “shut-down”
mode. Adolescent secondary amenorrhea and oligomenorrheawith or without an eating disorder-causes hypogonadism, or
low estrogen levels, which leads to decreased bone acquisition.
Decreased bone acquisition during the critical years of adolescence precludes the female from filling her “bone bank”; once
“withdraws” from the bone bank start in the mid- to late-20s,
low bone mass for chronological age will begin to manifest in
the pre-menopausal female; the condition will only worsen postmenopause.
As such, it becomes critical that all healthcare professionals perform a thorough history when working with female athletes of all
ages. A thorough discussion of past eating behaviors, menstrual history and previous DXA scans are critical steps in determining the
appropriate course of care. It is imperative that the questioning go
back as far as adolescence, as research has clearly demonstrated
how critical this time is in the development of eating behaviors,
menstrual function and bone acquisition. Any female who is identified as having current signs and symptoms of one female athlete
triad component should be examined for the other components and
treated appropriately. Any female, regardless of age, who reports
altered eating behaviors from adolescence to present day, reports
menstrual irregularity anytime throughout her reproductive lifetime, or reports stress fracture(s) or prolonged musculoskeletal
injury, should undergo a more detailed examination. A 3-day food
inventory, looking for adequate calcium and vitamin D intake,
should be performed. A complete pelvic examination should also be
performed; any pathologic findings should be addressed. Lastly, any
women reporting a history of disordered eating behaviors, menstrual irregularity (currently or in the past) or >1 stress fracture
should have their BMD assessed via DXA scan. Treatment strategies, such as diet modification, addressing menstrual dysfunction,
promotion of impact and weightbearing exercise should be implemented. Most importantly, changes in bone occur slowly; as such,
repeat assessments of BMD should be repeated every 6–12 months.
Further changes in the treatment regimen should reflect findings
in the changes in bone.
5. Conclusions
The female athlete triad exists in all ages. Since the triad
was first identified in 1992, women are now seeing the negative
J. Thein-Nissenbaum / Maturitas 75 (2013) 107–112
long term consequences of suffering from triad components.
Research suggests that disordered eating behaviors cause low
energy availability, resulting in shut down of the reproductive
and skeletal systems. Menstrual irregularity is associated with
hypoestrogenism, which affects bone mass accrual. Lack of bone
mass accrual during the critical time of adolescence is typically
not reversed; pre-menopausal and post-menopausal women will
“withdraw” bone from an already-depleted bone bank. The impact
of these conditions is medically significant, as a lack of bone
mass accrual has devastating effects. Any female who reports a
history of altered eating behaviors, menstrual irregularity, stress
fracture(s) or prolonged musculoskeletal injury should undergo a
more detailed examination. Treatment strategies include nutrition
counseling, diet modification, addressing menstrual dysfunction
and promotion of weightbearing exercise. Changes in bone occur
slowly; therefore, repeat assessments of BMD are warranted.
Contributors and their role
As sole author, I completed 100% of the work.
Competing interest
The authors have no conflict of interest or financial disclosure
to report.
Role of funding source
The authors have no conflict of interest or financial disclosure
to report.
Provenance and peer review
Commissioned and externally peer reviewed.
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