The Female Athlete Triad - American Academy of Pediatrics
←
→
Page content transcription
If your browser does not render page correctly, please read the page content below
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.
Downloaded from www.aappublications.org/news by guest on December 26, 2020
PEDIATRICS Volume 138, number 2, August 2016:e20160922 FROM THE AMERICAN ACADEMY OF PEDIATRICSAdolescent 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 EAtriad 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
Downloaded from www.aappublications.org/news by guest on December 26, 2020
PEDIATRICS Volume 138, number 2, August 2016 e3TABLE 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
Downloaded from www.aappublications.org/news by guest on December 26, 2020
e4 FROM THE AMERICAN ACADEMY OF PEDIATRICSdilation (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
Downloaded from www.aappublications.org/news by guest on December 26, 2020
e6 FROM THE AMERICAN ACADEMY OF PEDIATRICSintake 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,
Downloaded from www.aappublications.org/news by guest on December 26, 2020
PEDIATRICS Volume 138, number 2, August 2016 e7psychological, 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 December 26, 2020
e8 FROM THE AMERICAN ACADEMY OF PEDIATRICS17. 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 December 26, 2020
PEDIATRICS Volume 138, number 2, August 2016 e9Conference 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
Downloaded from www.aappublications.org/news by guest on December 26, 2020
e10 FROM THE AMERICAN ACADEMY OF PEDIATRICSThe 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;
Updated Information & including high resolution figures, can be found at:
Services http://pediatrics.aappublications.org/content/138/2/e20160922
References This article cites 73 articles, 9 of which you can access for free at:
http://pediatrics.aappublications.org/content/138/2/e20160922#BIBL
Subspecialty Collections This article, along with others on similar topics, appears in the
following collection(s):
Current Policy
http://www.aappublications.org/cgi/collection/current_policy
Council on Sports Medicine and Fitness
http://www.aappublications.org/cgi/collection/council_on_sports_me
dicine_and_fitness
Sports Medicine/Physical Fitness
http://www.aappublications.org/cgi/collection/sports_medicine:physi
cal_fitness_sub
Permissions & Licensing Information about reproducing this article in parts (figures, tables) or
in its entirety can be found online at:
http://www.aappublications.org/site/misc/Permissions.xhtml
Reprints Information about ordering reprints can be found online:
http://www.aappublications.org/site/misc/reprints.xhtml
Downloaded from www.aappublications.org/news by guest on December 26, 2020The 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
Pediatrics is the official journal of the American Academy of Pediatrics. A monthly publication, it
has been published continuously since 1948. Pediatrics is owned, published, and trademarked by
the American Academy of Pediatrics, 345 Park Avenue, Itasca, Illinois, 60143. Copyright © 2016
by the American Academy of Pediatrics. All rights reserved. Print ISSN: 1073-0397.
Downloaded from www.aappublications.org/news by guest on December 26, 2020You can also read
