The Female Athlete Triad - American Academy of Pediatrics

 
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CLINICAL REPORT            Guidance for the Clinician in Rendering Pediatric Care

                           The Female Athlete Triad
                           Amanda K. Weiss Kelly, MD, FAAP, Suzanne Hecht, MD, FACSM, COUNCIL ON SPORTS MEDICINE AND FITNESS

The number of girls participating in sports has increased significantly since           abstract
the introduction of Title XI in 1972. As a result, more girls have been able
to experience the social, educational, and health-related benefits of sports
participation. However, there are risks associated with sports participation,
including the female athlete triad. The triad was originally recognized as the
interrelationship of amenorrhea, osteoporosis, and disordered eating, but
our understanding has evolved to recognize that each of the components
of the triad exists on a spectrum from optimal health to disease. The triad
occurs when energy intake does not adequately compensate for exercise-                 This document is copyrighted and is property of the American
related energy expenditure, leading to adverse effects on reproductive,                Academy of Pediatrics and its Board of Directors. All authors have
                                                                                       filed conflict of interest statements with the American Academy
bone, and cardiovascular health. Athletes can present with a single                    of Pediatrics. Any conflicts have been resolved through a process
                                                                                       approved by the Board of Directors. The American Academy of
component or any combination of the components. The triad can have                     Pediatrics has neither solicited nor accepted any commercial
a more significant effect on the health of adolescent athletes than on                  involvement in the development of the content of this publication.

adults because adolescence is a critical time for bone mass accumulation.              Clinical reports from the American Academy of Pediatrics benefit from
                                                                                       expertise and resources of liaisons and internal (AAP) and external
This report outlines the current state of knowledge on the epidemiology,               reviewers. However, clinical reports from the American Academy of
diagnosis, and treatment of the triad conditions.                                      Pediatrics may not reflect the views of the liaisons or the organizations
                                                                                       or government agencies that they represent.

                                                                                       The guidance in this report does not indicate an exclusive course of
                                                                                       treatment or serve as a standard of medical care. Variations, taking
                                                                                       into account individual circumstances, may be appropriate.
INTRODUCTION                                                                           All clinical reports from the American Academy of Pediatrics
                                                                                       automatically expire 5 years after publication unless reaffirmed,
                                                                                       revised, or retired at or before that time.
The benefits of exercise in adolescents are well established, including
                                                                                       DOI: 10.1542/peds.2016-0922
improved self-esteem, fewer risk-taking behaviors, increased bone
mineral density (BMD), and decreased obesity.1–3 However, when                         PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).
exercise occurs without adequate energy intake to compensate for                       Copyright © 2016 by the American Academy of Pediatrics
exercise-related energy expenditure, there may be adverse effects on
                                                                                       FINANCIAL DISCLOSURE: The authors have indicated they
reproductive, bone, and cardiovascular health. The female athlete triad
                                                                                       have no financial relationships relevant to this article to
(referred to hereafter as the “triad”) was first widely acknowledged                   disclose.
as the 3 interrelated conditions of amenorrhea, osteoporosis, and
                                                                                       FUNDING: No external funding.
disordered eating in an American College of Sports Medicine position
statement published in 1997.4 Since that time, a more inclusive definition             POTENTIAL CONFLICT OF INTEREST: The authors have
                                                                                       indicated they have no potential conflicts of interest to
has evolved because it has become clear that each component of the
                                                                                       disclose.
triad exists on a spectrum; the 3 components were renamed menstrual
function, BMD, and energy availability (EA) to more accurately represent
the spectrum, which can range from optimal health to disease in each                     To cite: Weiss Kelly AK, Hecht S, AAP COUNCIL ON SPORTS
                                                                                         MEDICINE AND FITNESS. The Female Athlete Triad. Pediatrics.
component.5 In addition, athletes may present with 1, 2, or all 3 of the
                                                                                         2016;137(6):e20160922
components.

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PEDIATRICS Volume 138, number 2, August 2016:e20160922                                   FROM THE AMERICAN             ACADEMY OF PEDIATRICS
Adolescent athletes are in a critical          age at sport specialization, family             TABLE 1 Examples of Sports Emphasizing
period of bone mass accumulation,              dysfunction, abuse, and dieting.5,17                     Leanness and Endurance
so the triad disorders can be                                                                  Wrestling
particularly harmful in this group.6           Energy Availability                             Light-weight rowing
Appropriate intervention during the                                                            Gymnastics
                                               EA is defined as daily dietary energy           Dance
adolescent years may improve peak              intake minus daily exercise energy              Figure skating
bone mass accrual, an important                expenditure corrected for fat-free              Cheerleading
predictor of postmenopausal                    mass (FFM).5 Optimal EA has been                Long and middle distance running
osteoporosis, potentially preventing                                                           Pole vaulting
                                               identified to be 45 kcal/kg FFM per
low BMD, postmenopausal                        day in female adults but may be
osteoporosis, and fractures in                 even higher in adolescents who are              is also a strong predictor for low
adulthood. Two investigators have              still growing and developing. The               BMD.13 Athletes with a high drive
also identified lower BMD as a risk            spectrum of EA ranges from optimal              for thinness or increased dietary
factor for stress fracture in athletes.7,8     EA to inadequate EA, with or without            restraint (an intention to restrict
It is difficult to estimate the true           the presence of disordered eating/              food intake to control weight) are
prevalence of the triad because of             eating disorder. Recently, it has               significantly more likely to have low
the complexity of evaluation of each           become clear that many athletes                 BMD or to sustain a musculoskeletal
of the components. Reports have                affected by the triad do not exhibit            injury than are athletes with normal
indicated that the prevalence of               pathologic eating behaviors, and                eating behaviors.26,27
individuals with all 3 components              their low EA is unintentional. Low EA
simultaneously is only 1% to 1.2% in                                                           Many triggers for the onset of
                                               adversely affects bone remodeling,
high school girls9,10 and 0% to 16%                                                            disordered eating in athletes have
                                               and EA
triad can range from anovulation and             TABLE 2 Causes of Secondary Amenorrhea in        is likely attained between the ages
luteal dysfunction to oligomenorrhea                       Adolescents                            of 20 and 30 years.42,43 By the end
and amenorrhea (primary or                       Pregnancy                                        of adolescence, almost 90% of adult
secondary). Primary amenorrhea is                Polycystic ovarian syndrome                      bone mass has been obtained.43
defined as the absence of menarche               Pituitary tumor
                                                 Prolactinoma                                     Genetics, participation in weight-
by the age of 15 years.29 The                    Hyperthyroidism                                  bearing activities, and diet all
absence of other signs of pubertal               Liver/kidney disease                             influence bone mass in children.44
development by 14 years of age                   Medications: oral contraceptive pills,           Appropriate dietary intake and
or a failure to achieve menarche                    chemotherapy, antipsychotics,
                                                    antidepressants, corticosteroids
                                                                                                  weight-bearing exercise can
within 3 years of thelarche is                                                                    positively influence maximum bone
                                                 Eating disorders
also abnormal.29,30 Secondary                                                                     mass gains during childhood and
amenorrhea is defined as the absence                                                              adolescence. With improved EA
of menses for 3 consecutive months               oligomenorrhea ranges from 5.4%                  and resumption of menses, some
or longer in a female after menarche.            to 18%.10,15,21,22,24,31 The prevalence          “catch up” bone mass accrual may be
Oligomenorrhea is defined as                     of anovulation and luteal phase                  possible in athletes with the triad;
menstrual cycles longer than 35 days.            deficiency has not been evaluated in             however, some will have persistently
Luteal phase deficiency is defined as            adolescent athletes but ranges from              lower BMD than their genetic
a menstrual cycle with a luteal phase            5.9% to 30% in adult athletes.11                 potential, highlighting the need for
shorter than 11 days in length or with                                                            early, aggressive intervention in
                                                 Amenorrheic adolescent athletes
a low concentration of progesterone.                                                              adolescent athletes identified with
                                                 have a significantly lower BMD than
Menstrual disturbances, such                                                                      triad components.45
                                                 eumenorrheic adolescent athletes
as anovulation and luteal phase
                                                 or sedentary controls.13,31,33 Some              BMD in children and adolescents is
deficiency, are asymptomatic, making
                                                 studies have found that athletes                 typically evaluated by using dual-
them difficult to diagnose by history
                                                 with menstrual irregularities are                energy radiograph absorptiometry
alone. After excluding other causes of
                                                 as much as 3 times more likely to                (DXA), which is best performed
amenorrhea (Table 2), amenorrhea
                                                 sustain bone stress injury and other             and interpreted by centers with
in the setting of inadequate EA is
                                                 musculoskeletal injury than are                  certified clinical densitometrists with
diagnosed as functional hypothalamic
                                                 eumenorrheic athletes,26,34–36 but               knowledge of the official pediatric
amenorrhea.5 The word “functional”
                                                 this finding has not been consistent.37          positions of the International Society
indicates suppression, attributable to
                                                 Oligomenorrhea and amenorrhea                    for Clinical Densitometry.6,46,47
lack of energy, of an otherwise intact
                                                 have also been associated with                   Because athletes participating in
reproductive endocrine axis.
                                                 cardiovascular risk factors, including           weight-bearing sports are expected to
                                                 increased cholesterol and abnormal               have higher BMDs than nonathletes,
Menstrual irregularities are
                                                 endothelial function.38,39 In                    the American College of Sports
common during adolescence and
                                                 addition, menstrual disturbance has              Medicine recommends different
are significantly more common in
                                                 recently been related to decreased               criteria than the International Society
adolescent athletes. Of the published
                                                 performance in swimmers with                     for Clinical Densitometry, as shown
studies of menstrual disturbances
                                                 evidence of ovarian suppression                  in Table 3. In athletes, a Z-score
in adolescent athletes, only 1 study
                                                 compared with those without ovarian              below –1.0 is considered lower than
included a sedentary control group.
                                                 suppression.40                                   expected and indicates that, even
That study reported an incidence
of menstrual irregularity of 21% in                                                               in the absence of previous fracture,
                                                 Bone Health                                      secondary causes of low BMD may
sedentary adolescents compared
with 54% in adolescent athletes.9                The decreased rate of bone                       be present.5 A full discussion of the
Other studies reported menstrual                 acquisition that can be associated               secondary causes of low BMD is
disturbances in adolescent athletes              with the triad in adolescent athletes            beyond the scope of this report, but
ranging from 12% to 54% for any                  is particularly concerning, because              evaluations for secondary causes
menstrual irregularity (primary                  bone mass gains during childhood                 typically include the items in Table 4.48
or secondary amenorrhea or                       and adolescence are critical for                 Measures of bone microarchitecture,
oligomenorrhea).9–11,21,22,24,31,32              the attainment of maximal peak                   although primarily used for research
When evaluating specific types of                bone mass and the prevention of                  purposes at this juncture, can add
menstrual irregularity, primary                  osteoporosis in adulthood.6,41 The               additional information regarding
amenorrhea in athletes ranges from               maximum rate of bone formation                   bone quality beyond that of
1.2% to 6%, secondary amenorrhea                 usually occurs between the ages of               BMD. Favorable changes in bone
ranges from 5.3% to 30%, and                     10 and 14 years, and peak bone mass              microarchitecture are associated

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PEDIATRICS Volume 138, number 2, August 2016                                                                                             e3
TABLE 3 Definition of BMD Criteria in Adolescents
                                                       ISCD Official Position for Children and Adolescents46                           ACSM Guidelines for Athletes5
Osteoporosis                                          Vertebral compression fracture or Z-score ≤ –2 and                          Z-Score ≤2 and clinical risk factorsb
                                                              clinically significant fracture historya
Low BMD                                                                        —                                              Z-Score –1.0 to –1.9 and clinical risk factors
Lower BMD than expected                                                        —                                                             Z-Score ≤ –1.0
ACSM, American College of Sports Medicine; ISCD, International Society for Clinical Densitometry.
a Two or more long bone fractures by age 10 or ≥3 long bone fractures at any age up to 19 years.
b Nutritional deficiencies, hypoestrogenism, or stress fracture.

with sports participation in female                            TABLE 4 Evaluation for Low BMD (BMD < –1.0)
adolescents. Weight-bearing athletic                           • Serum 25-hydroxyvitamin D
activity is associated with greater                            • Serum calcium
total trabecular area and greater                              • Complete blood count with differential
cortical perimeter in the tibia.49                             • Thyroid-stimulating hormone
                                                               • Parathyroid hormone
Conversely, oligomenorrhea and
                                                               • Bone-specific alkaline phosphatase
amenorrhea are associated with                                 • 24-h urine for calcium
unfavorable bone microarchitecture,                            • Screening for cortisol excess: morning cortisol or 24-h urine for cortisol
including lower total density, lower                           • Celiac disease: serum tissue transglutaminase antibodies, total IgA, tissue transglutaminase IgG (in the
trabecular number, and greater                                    IgA-deficient adolescent)
                                                               • Markers of bone formation and resorption: serum osteocalcin and urine N-telopeptide
trabecular separation at the tibia.49
                                                               • Reproductive hormone evaluation: estradiol, FSH, LH in girls, testosterone in boys
Estimations of bone strength
                                                               FSH, follicle-stimulating hormone; IgA, immunoglobulin A; IgG, immunoglobulin G; LH, luteinizing hormone.
indicate that eumenorrheic, but
not amenorrheic, athletes have
greater stiffness and load-to-failure                          runners have lower BMDs than                                    restraint, greater length of time
thresholds, which are associated with                          sprinters, gymnasts, and ball sport                             participating in endurance sports,
decreased fracture risk, compared                              athletes.31,51–56 Barrack et al53                               lower body weight, and lower
with nonathlete controls.11,50                                 reported a higher prevalence of                                 BMI.1,13,31,32,52 The deficits in
                                                               low BMD in adolescent endurance                                 BMD seen with the triad are
Although it is well known that                                 runners (40%) than in ball or power                             associated with low estrogen levels
exercise is a stimulus for bone                                sport athletes (10%). This study                                and energy deficiency. Levels of
formation, data support that different                         also showed that runners 17 to 18                               bone formation and resorption
types of exercise can have differing                           years of age had similar bone mineral                           markers are significantly lower in
effects on bone formation. For                                 content (BMC) compared with 13- to                              amenorrheic adolescent athletes than
example, adolescent and collegiate                             14-year-old runners, whereas BMC                                in nonendurance athlete controls,
swimmers have been shown to                                    in nonrunner athletes showed a                                  indicating a state of overall decreased
have a similar BMD compared                                    significantly higher BMC in the older                           bone turnover.33 The restriction of
with nonathlete controls and to                                group compared with the younger                                 EA has been shown to cause estradiol
have a lower BMD compared with                                 group. These findings suggest                                   suppression and increased bone
athletes in other sports.48 In fact, a                         a possible suppression of bone                                  resorption as well as suppression of
longitudinal BMD study in swimmers,                            accumulation in adolescent runners,                             bone formation.19
gymnasts, and nonathlete controls                              although other factors may be                                   A recent multisite prospective
over an 8-month competitive                                    contributing to this finding, including                         study34 identified the contribution
season showed that swimmers and                                possible variable bone accrual                                  of single and multiple triad-related
controls had no improvement in                                 patterns attributable to genetics, rate                         risk factors for bone stress injury in
BMD, whereas gymnasts showed                                   of maturation, specific type of current                         259 female adolescents and young
significant BMD gains despite more                             and previous physical activity, and                             adults participating in competitive
body dissatisfaction and menstrual                             EA and menstrual differences often                              or recreational exercise. The authors
disturbance.51                                                 found between endurance runners                                 found an increased risk of bone
                                                               and nonendurance athletes.53                                    stress injuries as the number of triad-
Numerous studies have shown
running to have a positive effect                              Many factors are associated with                                related risk factors increased.34
on BMD compared with inactive                                  an increased risk of low BMD in
controls,48 but there is emerging                              female adolescent athletes, including                           Cardiovascular Health
concern, predominantly from cross-                             late menarche, oligomenorrhea,                                  Endothelial dysfunction, measured
sectional studies, that endurance                              amenorrhea, elevated dietary                                    by brachial artery flow-mediated

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e4                                                                                                              FROM THE AMERICAN ACADEMY OF PEDIATRICS
dilation (FMD), is an important                  TABLE 5 The Female Athlete Triad Coalition’s Recommended Screening Questions for the Female
predictor of coronary endothelial                           Athlete Triad68
dysfunction, atherosclerotic disease             Question                                                                     Included on the Fourth-
progression, and cardiovascular                                                                                                 Edition PPE Form69
event rates.38,57,58 Endothelial                 1. Do you worry about your weight or body composition?                                 √
dysfunction has been correlated                  2. Do you limit or carefully control the foods that you eat?                           √
with low whole-body and lumbar                   3. Do you try to lose weight to meet weight or image/appearance                        √
                                                    requirements in your sport?
BMD, menstrual dysfunction, and
                                                 4. Does your weight affect the way you feel about yourself?                            —
low estrogen levels in dancers and               5. Do you worry that you have lost control over how much you eat?                      —
endurance athletes.38,39 In endurance            6. Do you make yourself vomit or use diuretics or laxatives after you eat?             —
athletes, oligomenorrheic and                    7. Do you currently or have you ever suffered from an eating disorder?                 √
amenorrheic athletes had impaired                8. Do you ever eat in secret?
                                                 9. What age was your first menstrual period?                                            √
FMD compared with eumenorrheic
                                                 10. Do you have monthly menstrual cycles?                                              √
athletes, with amenorrheic athletes              11. How many menstrual cycles have you had in the last year?                           √
showing the greatest impairment.39               12. Have you ever had a stress fracture?                                               √
In this group, amenorrhea was
also associated with increased
                                                 menstrual cycles, but they may                          Female Athlete Triad Coalition and
total cholesterol and low-density
                                                 show suppression of reproductive                        has been endorsed by the American
lipoprotein levels.39 Among
                                                 function nonetheless. There is a                        Academy of Pediatrics (AAP) for use
professional dancers, endothelial
                                                 small body of data suggesting that                      when performing the PPE (Table 5).
dysfunction alone was present in
                                                 male athletes with inadequate EA                        If an athlete answers “yes” to any of
64%, whereas the prevalence of
                                                 may also suffer from hormonal                           the triad questions on the PPE form,
dancers with endothelial dysfunction
                                                 changes and low BMD. Lower                              the remaining questions from the
and all 3 components of the triad
                                                 testosterone levels have been found                     Female Athlete Triad Coalition68 can
was 14%.38 All of the dancers
                                                 in male runners compared with                           be used for further evaluation.
who reported current menstrual
                                                 inactive controls.61 Similar to female                  A sports level of participation
dysfunction (36%) had reduced
                                                 athletes, male endurance runners                        and return-to-play medical risk
FMD.38 Amenorrheic runners and
                                                 have been found to have lower                           stratification scoring rubric has
dancers treated with 4 weeks of
                                                 BMD than male athletes in power or                      been developed by the Female
folic acid supplementation showed
                                                 ball sports.62 Adolescent males with                    Athlete Triad Coalition Consensus
improvements in FMD.15,59 Although
                                                 anorexia nervosa display low BMD at                     Panel to help the clinician assess
these studies were not exclusive
                                                 multiple skeletal sites.60,63                           an athlete with triad-related risk
to adolescents, adolescents were
                                                 Although the body of scientific                         factors into low-, moderate-, or
included in the study populations.
                                                 evidence is still developing, it is                     high-risk categories. Decisions
These results raise concern that
                                                 important to consider that adolescent                   regarding sports participation, level
an athlete diagnosed with the
                                                 males participating in sports that                      of participation permitted, and
triad could be at risk of developing
                                                 emphasize and reward leanness                           return-to-play are made on the basis
cardiovascular disease.
                                                 may be at risk of a constellation of                    of the risk category that the athlete
                                                 findings similar to those seen in                       falls into and can be reassessed
                                                 females with components of the                          as the athlete progresses through
MALE ATHLETES                                    triad.64–66                                             treatment.68
Although female athletes have been
the exclusive focus of research on
                                                 SCREENING                                               DIAGNOSIS
the triad, low EA resulting in the
suppression of the neuroendocrine                It is convenient to screen for the                      Obtaining a complete nutritional,
reproductive axis is likely not                  triad at the time of a well-child visit                 menstrual, fracture, and exercise
gender selective. Low testosterone               and/or the preparticipation physical                    history is the first step in diagnosis.
and estradiol levels have been                   evaluation (PPE). The Female Athlete                    Vital signs may reveal bradycardia,
documented in adolescent males                   Triad Coalition has developed 12                        which can also be a normal finding
diagnosed with anorexia nervosa.60               questions for screening (Table 5).67–69                 in well-trained athletes; orthostatic
This finding begs the question: is               Another screening tool is found in                      hypotension; low body weight (
eating disorders, cold/discolored             TABLE 6 Factors Prompting BMD Evaluation in Athletes With Stress Fracture
hands and feet, hypercarotenemia,             Low BMI (30                           they may give the athlete a false
disorder, a chemistry profile and             kcal/kg FFM per day can restore                           sense of security that EA has been
electrocardiography can be used to            menses, although an EA >45 kcal/                          restored, so their use is typically
evaluate for possible arrhythmia or           kg FFM per day is optimal.5,71 FFM                        avoided unless they are being
metabolic disturbance. BMD testing            can be measured by using DXA,                             prescribed for other indications. It
by DXA is indicated in athletes with          air-displacement plethysmography                          is important to recognize that the
any of the following: eating disorder         (ie, BodPod analysis [National                            hormonal environment provided
(diagnosed by using criteria of the           Institute for Fitness and Sport,                          by oral contraceptive pills is not
Diagnostic and Statistical Manual of          Indianapolis, IN]), bioelectrical                         the same as a naturally occurring
Mental Disorders, Fifth Edition70),           impedance analysis, or skinfold                           menstrual cycle. Misra et al75
weight 85% expected weight, and a                            treatment.5,6 Significantly more
Improving EA is the cornerstone of            minimum daily energy intake of 2000                       athletes with stress fractures have
treatment of the triad disorders and          kcal.48,60 A gradual increase of 200                      low calcium intakes than do athletes
has been associated with the return           to 600 kcal/day and a reduction in                        without stress fractures.35 Assessing
of normal menses and improvements             training volume of 1 day per week                         25-hydroxyvitamin D concentration
in BMD.5,48,60 A multidisciplinary            are usually sufficient to attain the                      is useful in athletes presenting
team approach is suggested and may            needed improvements in weight and                         with components of the triad.1,46
include a physician, a dietitian, a           EA.48,71 It is important to recognize                     The AAP currently recommends a
certified athletic trainer, a behavioral      that the resumption of menses may                         daily intake of 1300 mg calcium for
health clinician, and, at times, an           take up to 1 year or longer after                         children and adolescents ages 9 to
exercise physiologist. It is preferable       restoration of appropriate EA.48 A                        18 years and 600 IU vitamin D for
that the medical team be familiar             written treatment plan (contract)                         children and adolescents ages 1 to
with treating athletes. For athletes          signed by the providers and athlete/                      18 years, although many experts
with an unintentionally low EA                parent(s) can be a useful tool to                         recommend higher intakes of
without features of disordered eating         outline and define the treatment                          vitamin D, particularly in climates
or an eating disorder, a behavioral           plan and expectations on the part of                      where sun exposure is limited.1
health clinician may not be needed.           the athlete, parent(s), and medical                       The International Osteoporosis
Improvements in EA can be                     providers (for a sample contract, see                     Foundation calcium calculator can
accomplished by both decreasing               the Supplementary Data in ref 48).                        be used as a tool to estimate calcium

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e6                                                                                                 FROM THE AMERICAN ACADEMY OF PEDIATRICS
intake from dietary sources (www.                unhealthy behaviors. Refusal skills                   normal in athletes and may be
iof.org). In addition to calcium                 were practiced, and healthy norms                     detrimental to their health and
and vitamin D, other vitamins and                were reinforced. The control schools                  performance.
minerals are known to play a role                received pamphlets regarding
                                                                                                    4. Functional hypothalamic
in bone health (B vitamins, vitamin              disordered eating, drug use, and
                                                                                                       amenorrhea is a diagnosis of
K, and iron), thus underscoring the              sports nutrition. Questionnaires
                                                                                                       exclusion made after other
importance of a well-balanced diet.              administered before and after the
                                                                                                       causes for primary and
                                                 program revealed decreased use of
Bisphosphonates are antiresorptive                                                                     secondary amenorrhea have
                                                 diet pills, decreased intent to vomit
agents frequently used in the                                                                          been evaluated. The restoration
                                                 to lose weight, and improved healthy
treatment of postmenopausal                                                                            of optimal EA is the cornerstone
                                                 eating behaviors in the teenagers
osteoporosis. Unlike postmenopausal                                                                    of treatment of functional
                                                 in intervention schools. This trial
osteoporosis, the mechanism of low                                                                     hypothalamic amenorrhea.
                                                 shows that primary intervention
BMD in athletes affected by the triad                                                               5. The resumption of menses may
                                                 techniques that use education with
is predominantly attributable to                                                                       take up to 1 year or longer after
                                                 peer leaders can reduce the risk of
decreased bone formation rather than                                                                   restoration of appropriate EA.
                                                 disordered eating and other risk-
increased bone resorption. Therefore,
                                                 taking behaviors.                                  6. Oral contraceptive pills are
bisphosphonates would likely be less
effective in athletes with the triad.20                                                                not the first-line intervention
Other concerns regarding treatment                                                                     for an athlete with functional
                                                 CONCLUSIONS AND GUIDANCE FOR THE
with bisphosphonates include their               CLINICIAN                                             hypothalamic amenorrhea.
long half-life and potential teratogenic                                                            7. Weight-bearing exercise in
effects, thus making it prudent to                 1. The well-child visit or PPE
                                                      provides an opportune time for                   the context of appropriate
avoid them in females of childbearing                                                                  nutritional intake is important
age.6 It is important to note that the                the pediatrician to screen for and
                                                      provide education and guidance                   for the enhancement of bone
US Food and Drug Administration                                                                        mass accrual.
has not approved any pharmacologic                    regarding the components of the
interventions for the treatment of                    female athlete triad and the risks            8. The criteria for performing DXA to
osteoporosis in premenopausal                         of inadequate EA for athletes. The               measure BMD in athletes include
females.                                              AAP has published a PPE form                     menstrual dysfunction or low EA
                                                      that includes a comprehensive                    (45 kcal/kg FFM per
weight-control behaviors, drug use,                   inadequate energy intake.                        day. FFM can be determined by
and risk-taking behaviors.77 This                     Patients presenting with                         using DXA, biometrical impedance
randomized controlled intervention                    menstrual dysfunction                            measurements, or skinfold
included eight 45-minute, small-                      provide an opportunity for the                   measurements.
group classroom sessions guided                       pediatrician to counsel parents             10. When treating athletes with
by peer leaders. The curriculum                       and adolescent athletes that                    the triad, a multidisciplinary
included education regarding                          menstrual dysfunction and                       team capable of addressing
substance use, nutrition, and                         restricted energy intake are not                the medical, nutritional,

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PEDIATRICS Volume 138, number 2, August 2016                                                                                             e7
psychological, and sports                        Lisa K. Kluchurosky, MEd, ATC – National Athletic       athlete triad. Med Sci Sports Exerc.
     participation–related issues of                  Trainers Association                                    2007;39(10):1867–1882
     the triad is helpful. Weight-gain                                                                     6. Golden NH, Abrams SA; Committee on
                                                      CONSULTANTS
     or -loss concerns in an athlete are                                                                      Nutrition. Optimizing bone health in
     better addressed by medical and                  Neeru A. Jayanthi, MD                                   children and adolescents. Pediatrics.
                                                      Rebecca Carl, MD, FAAP                                  2014;134(4). Available at: www.pediatrics.
     nutritional professionals rather
                                                      Sally Harris, MD, FAAP                                  org/cgi/content/full/134/4/e1229
     than athletic coaching staff.
11. Adequate intakes of calcium                       STAFF                                                7. Bennell, Malcolm SA, Thomas SA, et
                                                                                                              al. Risk factors for stress fractures
    (1300 mg/day) and vitamin D                       Anjie Emanuel, MPH                                      in track and field athletes: a twelve-
    (600 IU/day) play an important                                                                            month prospective study. Am J Sports
    role in bone mass accrual for                                                                             Med. 1996;24(2):810–818
    all adolescents. Athletes with
                                                        ABBREVIATIONS
                                                                                                           8. Nattiv A, Puffer JC, Casper J, Dorey
    greater dietary intake of calcium                   AAP: American Academy of
                                                                                                              F. Stress fracture risk factors,
    will require less supplemental                           Pediatrics                                       incidence and distribution: a 3-year
    calcium. When determining                           BMC: bone mineral content                             prospective study in collegiate runners
    the amount of calcium                               BMD: bone mineral density                             [abstract]. Med Sci Sports Exerc.
    supplementation needed, some                        DXA: dual-energy radiograph                           2000;5(Suppl):S347
    adolescents may require higher                           absorptiometry                                9. Hoch AZ, Pajewski NM, Moraski L, et
    vitamin D intakes than others to                    EA: energy availability                               al. Prevalence of the female athlete
    achieve normal vitamin D levels.                    FFM: fat-free mass                                    triad in high school athletes and
                                                        FMD: flow-mediated dilation                           sedentary students. Clin J Sport Med.
12. Bisphosphonate use in
                                                        PPE: preparticipation physical                        2009;19(5):421–428
    adolescent females with a low
                                                             evaluation                                   10. Nichols JF, Rauh MJ, Lawson MJ, Ji M,
    BMD related to the triad is not
                                                                                                              Barkai HS. Prevalence of the female
    supported by current literature.
                                                                                                              athlete triad syndrome among high
13. Educational opportunities                                                                                 school athletes. Arch Pediatr Adolesc
    regarding the recognition,                        REFERENCES                                              Med. 2006;160(2):137–142
    prevention, and treatment of                                                                          11. Barrack MT, Ackerman KE, Gibbs
    issues related to the triad should                  1. Ackerman KE, Misra M. Bone health                  JC. Update on the female athlete
    be available for practicing                            and the female athlete triad in                    triad. Curr Rev Musculoskelet Med.
                                                           adolescent athletes. Phys Sportsmed.               2013;6(2):195–204
    pediatricians, pediatric residents,
                                                           2011;39(1):131–141
    and medical students.                                                                                 12. Fredericson M, Kent K. Normalization
                                                        2. Bailey DA, McKay HA, Mirwald RL,                   of bone density in a previously
LEAD AUTHORS                                               Crocker PR, Faulkner RA. A six-year                amenorrheic runner with
Amanda K. Weiss Kelly, MD, FAAP                            longitudinal study of the relationship             osteoporosis. Med Sci Sports Exerc.
Suzanne Hecht, MD, FACSM                                   of physical activity to bone mineral               2005;37(9):1481–1486
                                                           accrual in growing children: the
COUNCIL ON SPORTS MEDICINE AND                                                                            13. Gibbs JC, Williams NI, De Souza
                                                           University of Saskatchewan Bone
FITNESS EXECUTIVE COMMITTEE,                                                                                  MJ. Prevalence of individual and
                                                           Mineral Accrual Study. J Bone Miner
2014–2015                                                                                                     combined components of the female
                                                           Res. 1999;14(10):1672–1679
                                                                                                              athlete triad. Med Sci Sports Exerc.
Joel S. Brenner, MD, MPH, FAAP, Chairperson             3. Sabo DF, Miller KE, Farrell MP,                    2013;45(5):985–996
Cynthia R. LaBella, MD, FAAP, Chairperson-Elect
                                                           Melnick MJ, Barnes GM. High                    14. Hind K. Recovery of bone mineral
Margaret A. Brooks, MD, FAAP
                                                           school athletic participation, sexual              density and fertility in a former
Alex Diamond, DO, FAAP
William Hennrikus, MD, FAAP
                                                           behavior and adolescent pregnancy:                 amenorrheic athlete. J Sports Sci Med.
Michele LaBotz, MD, FAAP                                   a regional study. J Adolesc Health.                2008;7(3):415–418
Kelsey Logan, MD, FAAP                                     1999;25(3):207–216
                                                                                                          15. Hoch AZ, Papanek PE, Havlik HS,
Keith J. Loud, MDCM, MSc, FAAP                          4. Otis CL, Drinkwater B, Johnson M,                  Raasch WG, Widlansky ME, Schimke JE.
Kody A. Moffatt, MD, FAAP
                                                           Loucks A, Wilmore J. American College              Prevalence of the female athlete triad/
Blaise Nemeth, MD, FAAP
                                                           of Sports Medicine position stand: the             tetrad in professional ballet dancers
Brooke Pengel, MD, FAAP
Amanda K. Weiss Kelly, MD, FAAP
                                                           Female Athlete Triad. Med Sci Sports               [abstract]. Med Sci Sports Exerc.
                                                           Exerc. 1997;29(5):i–ix                             2009;41(5):524
LIAISONS                                                5. Nattiv A, Loucks AB, Manore MM,                16. Porucanik CA, Sullivan MM, Nunu J, Joy
Andrew J.M. Gregory, MD, FAAP – American                   Sanborn CF, Sundgot-Borgen J, Warren               E. Physician recognition, evaluation
College of Sports Medicine                                 MP; American College of Sports                     and treatment of the female athlete
Mark Halstead, MD, FAAP – American Medical                 Medicine. American College of Sports               triad [abstract]. Med Sci Sports Exerc.
Society for Sports Medicine                                Medicine position stand: the female                2009;41(5):83

                                        Downloaded from www.aappublications.org/news by guest on March 17, 2020
e8                                                                                                         FROM THE AMERICAN ACADEMY OF PEDIATRICS
17. Sundgot-Borgen J. Risk and trigger           28. Rosen LW, Hough DO. Pathogenic                   a cross-sectional study. BMJ Open.
     factors for the development of eating            weight-control behavior of female                2012;2(6):e001920
     disorders in female elite athletes. Med          college gymnasts. Phys Sportsmed.            38. Hoch AZ, Papanek P, Szabo A, Widlansky
     Sci Sports Exerc. 1994;26(4):414–419             1988;16(9):141–144                               ME, Schimke JE, Gutterman DD.
 18. Loucks AB, Thuma JR. Luteinizing             29. American College of Obstetricians                Association between the female athlete
     hormone pulsatility is disrupted at              and Gynecologists Committee                      triad and endothelial dysfunction
     a threshold of energy availability in            on Adolescent Health Care. ACOG                  in dancers. Clin J Sport Med.
     regularly menstruating women. J Clin             Committee Opinion No. 349, November              2011;21(2):119–125
     Endocrinol Metab. 2003;88(1):297–311             2006: menstruation in girls and              39. Rickenlund A, Eriksson MJ, Schenck-
 19. Ihle R, Loucks AB. Dose-response                 adolescents: using the menstrual                 Gustafsson K, Hirschberg AL.
     relationships between energy                     cycle as a vital sign. Obstet Gynecol.           Amenorrhea in female athletes
     availability and bone turnover in young          2006;108(5):1323–1328                            is associated with endothelial
     exercising women. J Bone Miner Res.          30. Diaz A, Laufer MR, Breech LL; American           dysfunction and unfavorable lipid
     2004;19(8):1231–1240                             Academy of Pediatrics Committee                  profile. J Clin Endocrinol Metab.
 20. Misra M, Klibanski A. Bone metabolism            on Adolescence; American College                 2005;90(3):1354–1359
     in adolescents with anorexia nervosa.            of Obstetricians and Gynecologists           40. Vanheest JL, Rodgers CD, Mahoney
     J Endocrinol Invest. 2011;34(4):324–332          Committee on Adolescent Health Care.             CE, De Souza MJ. Ovarian suppression
                                                      Menstruation in girls and adolescents:           impairs sport performance in junior
 21. Beals KA. Eating behaviors, nutritional
                                                      using the menstrual cycle as a vital             elite female swimmers. Med Sci Sports
     status, and menstrual function in elite
                                                      sign. Pediatrics. 2006;118(5):2245–2250          Exerc. 2014;46(1):156–166
     female adolescent volleyball players. J
     Am Diet Assoc. 2002;102(9):1293–1296         31. Barrack MT, Rauh MJ, Nichols JF.             41. NIH Consensus Development Panel on
                                                      Prevalence of and traits associated              Osteoporosis Prevention, Diagnosis,
 22. Nichols JF, Rauh MJ, Barrack MT,
                                                      with low BMD among female                        and Therapy. Osteoporosis prevention,
     Barkai HS, Pernick Y. Disordered
                                                      adolescent runners. Med Sci Sports               diagnosis, and therapy. JAMA.
     eating and menstrual irregularity in
                                                      Exerc. 2008;40(12):2015–2021                     2001;285(6):785–795
     high school athletes in lean-build and
     nonlean-build sports. Int J Sport Nutr       32. Gibbs JC, Nattiv A, Barrack MT, et al.       42. Bonjour JP, Theintz G, Buchs B,
     Exerc Metab. 2007;17(4):364–377                  Low bone density risk is higher in               Slosman D, Rizzoli R. Critical years
                                                      exercising women with multiple triad             and stages of puberty for spinal and
 23. Rosendahl J, Bormann B,
                                                      risk factors. Med Sci Sports Exerc.              femoral bone mass accumulation
     Aschenbrenner K, Aschenbrenner F,
                                                      2014;46(1):167–176                               during adolescence. J Clin Endocrinol
     Strauss B. Dieting and disordered
     eating in German high school athletes        33. Christo K, Prabhakaran R, Lamparello             Metab. 1991;73(3):555–563
     and non-athletes. Scand J Med Sci                B, et al. Bone metabolism in                 43. Sabatier JP, Guaydier-Souquières
     Sports. 2009;19(5):731–739                       adolescent athletes with amenorrhea,             G, Laroche D, et al. Bone mineral
                                                      athletes with eumenorrhea, and                   acquisition during adolescence and
 24. Havemann L, DeLange Z, Pieterse
                                                      control subjects. Pediatrics.                    early adulthood: a study in 574 healthy
     K, Wright HH. Disordered eating
                                                      2008;121(6):1127–1136                            females 10-24 years of age. Osteoporos
     and menstrual patterns in female
                                                  34. Barrack MT, Gibbs JC, De Souza MJ,               Int. 1996;6(2):141–148
     university netball players. South
     African J Sports Med. 2011;23(3):68–72           et al. Higher incidence of bone stress       44. Slemenda CW, Miller JZ, Hui SL, Reister
                                                      injuries with increasing female                  TK, Johnston CC Jr. Role of physical
 25. Cobb KL, Bachrach LK, Greendale G,
                                                      athlete triad-related risk factors:              activity in the development of skeletal
     et al. Disordered eating, menstrual
                                                      a prospective multisite study of                 mass in children. J Bone Miner Res.
     irregularity, and bone mineral density
                                                      exercising girls and women. Am J                 1991;6(11):1227–1233
     in female runners. Med Sci Sports
                                                      Sports Med. 2014;42(4):949–958               45. Barrack MT, Van Loan MD, Rauh
     Exerc. 2003;35(5):711–719
                                                  35. Myburgh KH, Hutchins J, Fataar                   MJ, Nichols JF. Body mass, training,
 26. Rauh MJ, Nichols JF, Barrack MT.
                                                      AB, Hough SF, Noakes TD. Low bone                menses, and bone in adolescent
     Relationships among injury and
                                                      density is an etiologic factor for stress        runners: a 3-yr follow-up. Med Sci
     disordered eating, menstrual
                                                      fractures in athletes. Ann Intern Med.           Sports Exerc. 2011;43(6):959–966
     dysfunction, and low bone mineral
                                                      1990;113(10):754–759                         46. Gordon CM, Leonard MB, Zemel BS;
     density in high school athletes:
     a prospective study. J Athl Train.           36. Thein-Nissenbaum JM, Rauh MJ, Carr               International Society for Clinical
     2010;45(3):243–252                               KE, Loud KJ, McGuine TA. Menstrual               Densitometry. 2013 Pediatric Position
                                                      irregularity and musculoskeletal injury          Development Conference: executive
 27. Thein-Nissenbaum JM, Rauh MJ, Carr
                                                      in female high school athletes. J Athl           summary and reflections. J Clin
     KE, Loud KJ, McGuine TA. Associations
                                                      Train. 2012;47(1):74–82                          Densitom. 2014;17(2):219–224
     between disordered eating, menstrual
     dysfunction, and musculoskeletal             37. Duckham RL, Peirce N, Meyer C,               47. Schousboe JT, Shepherd JA, Bilezikian
     injury among high school athletes.               Summers GD, Cameron N, Brooke-                   JP, Baim S. Executive summary of the
     J Orthop Sports Phys Ther.                       Wavell K. Risk factors for stress                2013 International Society for Clinical
     2011;41(2):60–69                                 fracture in female endurance athletes:           Densitometry Position Development

                                     Downloaded from www.aappublications.org/news by guest on March 17, 2020
PEDIATRICS Volume 138, number 2, August 2016                                                                                                  e9
Conference on bone densitometry. J              coronary vasodilator dysfunction                Triad Coalition consensus statement
      Clin Densitom. 2013;16(4):455–466               on adverse long-term outcome of                 on treatment and return to play of the
 48. Scofield KL, Hecht S. Bone health in              coronary heart disease. Circulation.            female athlete triad. Br J Sports Med.
     endurance athletes: runners, cyclists,           2000;101(16):1899–1906                          2014;48(4):289–309
     and swimmers. Curr Sports Med Rep.           59. Hoch AZ, Lynch SL, Jurva JW,                69. American Academy of Family
     2012;11(6):328–334                               Schimke JE, Gutterman DD. Folic acid            Physicians; American Academy of
 49. Ackerman KE, Nazem T, Chapko                     supplementation improves vascular               Pediatrics; American College of Sports
     D, et al. Bone microarchitecture                 function in amenorrheic runners. Clin           Medicine. In: Roberts W, Bernhardt
     is impaired in adolescent                        J Sport Med. 2010;20(3):205–210                 D, eds. Preparticipation Physical
     amenorrheic athletes compared with           60. Misra M, Prabhakaran R, Miller KK,              Evaluation. 4th ed. Elk Grove Village, IL:
     eumenorrheic athletes and nonathletic            et al. Weight gain and restoration of           American Academy of Pediatrics; 2010
     controls. J Clin Endocrinol Metab.               menses as predictors of bone mineral        70. American Psychiatric Association.
     2011;96(10):3123–3133                            density change in adolescent girls with         Diagnostic and Statistical Manual
                                                      anorexia nervosa-1. J Clin Endocrinol           of Mental Disorders, Fifth Edition.
 50. Boutroy S, Bouxsein ML, Munoz F,
                                                      Metab. 2008;93(4):1231–1237                     Washington, DC: American Psychiatric
     Delmas PD. In vivo assessment of
                                                                                                      Publishing; 2013
     trabecular bone microarchitecture            61. De Souza MJ, Arce JC, Pescatello LS,
     by high-resolution peripheral                    Scherzer HS, Luciano AA. Gonadal            71. Kopp-Woodroffe SA, Manore MM,
     quantitative computed tomography.                hormones and semen quality in male              Dueck CA, Skinner JS, Matt KS.
     J Clin Endocrinol Metab.                         runners: a volume threshold effect of           Energy and nutrient status of
     2005;90(12):6508–6515                            endurance training. Int J Sports Med.           amenorrheic athletes participating
                                                      1994;15(7):383–391                              in a diet and exercise training
 51. Taaffe DR, Robinson TL, Snow CM,                                                                 intervention program. Int J Sport Nutr.
     Marcus R. High-impact exercise               62. Fredericson M, Chew K, Ngo J, Cleek             1999;9(1):70–88
     promotes bone gain in well-trained               T, Kiratli J, Cobb K. Regional bone
     female athletes. J Bone Miner Res.                                                           72. Cobb KL, Bachrach LK, Sowers M, et
                                                      mineral density in male athletes:
     1997;12(2):255–260                                                                               al. The effect of oral contraceptives
                                                      a comparison of soccer players,
                                                                                                      on bone mass and stress fractures in
 52. Barrack MT, Rauh MJ, Barkai HS,                  runners and controls. Br J Sports Med.
                                                                                                      female runners. Med Sci Sports Exerc.
     Nichols JF. Dietary restraint and low            2007;41(10):664–668
                                                                                                      2007;39(9):1464–1473
     bone mass in female adolescent               63. Castro J, Toro J, Lazaro L, Pons F,         73. Golden NH, Lanzkowsky L, Schebendach
     endurance runners. Am J Clin Nutr.               Halperin I. Bone mineral density                J, Palestro CJ, Jacobson MS, Shenker
     2008;87(1):36–43                                 in male adolescents with anorexia               IR. The effect of estrogen-progestin
 53. Barrack MT, Rauh MJ, Nichols JF. Cross-          nervosa. J Am Acad Child Adolesc                treatment on bone mineral density in
     sectional evidence of suppressed                 Psychiatry. 2002;41(5):613–618                  anorexia nervosa. J Pediatr Adolesc
     bone mineral accrual among female            64. Miller BE, Hackney AC, De Souza MJ.             Gynecol. 2002;15(3):135–143
     adolescent runners. J Bone Miner Res.            The endurance training on hormone           74. Warren MP, Brooks-Gunn J, Fox RP,
     2010;25(8):1850–1857                             and semen profiles in marathon                   et al. Persistent osteopenia in ballet
 54. Mudd LM, Fornetti W, Pivarnik JM. Bone           runners. Fertil Steril. 1997;67(3):585–         dancers with amenorrhea and delayed
     mineral density in collegiate female             586; author reply: 586–587                      menarche despite hormone therapy:
     athletes: comparisons among sports. J        65. Hackney AC. Endurance exercise                  a longitudinal study. Fertil Steril.
     Athl Train. 2007;42(3):403–408                   training and reproductive endocrine             2003;80(2):398–404
 55. Nichols JF, Rauh MJ, Barrack MT,                 dysfunction in men: alterations in the      75. Misra M, Katzman D, Miller KK, et al.
     Barkai HS. Bone mineral density                  hypothalamic-pituitary-testicular axis.         Physiologic estrogen replacement
     in female high school athletes:                  Curr Pharm Des. 2001;7(4):261–273               increases bone density in adolescent
     interactions of menstrual function           66. Hackney AC. Effects of endurance                girls with anorexia nervosa. J Bone
     and type of mechanical loading. Bone.            exercise on the reproductive system             Miner Res. 2011;26(10):2430–2438
     2007;41(3):371–377                               of men: the “exercise-hypogonadal           76. Feldmann JM, Belsha JP, Eissa MA,
 56. Tenforde AS, Fredericson M. Influence             male condition”. J Endocrinol Invest.           Middleman AB. Female adolescent
     of sports participation on bone health           2008;31(10):932–938                             athletes’ awareness of the connection
     in the young athlete: a review of the        67. Mountjoy M, Hutchinson M, Cruz                  between menstrual status and bone
     literature. PM R. 2011;3(9):861–867              L, Lebrun C. Female athlete triad               health. J Pediatr Adolesc Gynecol.
 57. Anderson TJ, Uehata A, Gerhard MD,               screening questionnaire. Female                 2011;24(5):311–314
     et al. Close relation of endothelial             Athlete Triad Coalition. Available at:      77. Elliot DL, Goldberg L, Moe EL, et al.
     function in the human coronary and               www.femaleathletetriad.org/~triad/              Long-term outcomes of the ATHENA
     peripheral circulations. J Am Coll               wp-content/uploads/2008/11/ppe_for_             (Athletes Targeting Healthy Exercise
     Cardiol. 1995;26(5):1235–1241                    website.pdf. Accessed July 15, 2015             & Nutrition Alternatives) program for
 58. Schächinger V, Britten MB,                   68. De Souza MJ, Nattiv A, Joy E, et al;            female high school athletes. J Alcohol
     Zeiher AM. Prognostic impact of                  Expert Panel. 2014 Female Athlete               Drug Educ. 2008;52(2):73–92

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e10                                                                                                   FROM THE AMERICAN ACADEMY OF PEDIATRICS
The Female Athlete Triad
Amanda K. Weiss Kelly, Suzanne Hecht and COUNCIL ON SPORTS MEDICINE
                              AND FITNESS
                            Pediatrics 2016;138;
   DOI: 10.1542/peds.2016-0922 originally published online July 18, 2016;

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The Female Athlete Triad
Amanda K. Weiss Kelly, Suzanne Hecht and COUNCIL ON SPORTS MEDICINE
                              AND FITNESS
                            Pediatrics 2016;138;
   DOI: 10.1542/peds.2016-0922 originally published online July 18, 2016;

 The online version of this article, along with updated information and services, is
                        located on the World Wide Web at:
          http://pediatrics.aappublications.org/content/138/2/e20160922

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