The Female Athlete Triad - American Academy of Pediatrics

 
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
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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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