eMedicine Specialties > Sports Medicine > Introductory Topics in Sports Medicine
Female Athlete Triad
Updated: May 30, 2008
Introduction
Background
History
Athletic activity by women and girls has dramatically increased in the last few decades. Much of this increase can be attributed to Title IX legislation, which mandated that equal money and opportunities be made available to females at publicly funded institutions, particularly public schools, ranging from elementary schools to the universities.1, 2 For the most part, this legislation has led to many health benefits, as generations of young women were given to chance to compete in a variety of sports.
Women's athletics has grown to the point that women's basketball has become a professional sport in the United States. The number of girls participating in youth baseball or tee-ball has risen from almost a rarity to rates that nearly match those of their male counterparts. Participation in high school sports rose from 3.7% in 1972 to 40% in 2002, and participation in college spots rose from 2% in 1972 to 43% in 2002.
With the increase in female participation in sports, the incidence of a triad of disorders particular to women has also increased. This triad, the female athlete triad, although more common in the athletic population, can also occur in the nonathletic population. However, despite first being described by the American College of Sports Medicine (ACSM) Meeting in 1993,3, 4 observations about bone mineral densities (BMDs), stress fractures, eating disorders, and female athletics had been described for decades before the syndrome was named.
Often difficult to recognize, the female athlete triad can have a significant impact on morbidity and even mortality in a relatively young segment of the population. Indeed, the full impact of this syndrome may not be realized until these women reach menopause, when bone loss is accelerated.
For excellent patient education resources, visit eMedicine's Osteoporosis and Bone Health Center, Exercise, Nutrition, and Weight Management Center, and Women's Health Center. Also, see eMedicine's patient education articles Anorexia Nervosa, Bulimia, and Amenorrhea.
Related eMedicine topics:
Amenorrhea
Eating Disorder: Anorexia
Eating Disorder: Bulimia
Stress Fractures
Related Medscape topics:
Resource Center Adolescent Medicine
Resource Center Exercise and Sports Medicine
Resource Center Nutrition
CME Bone Density Evaluation in Teens Prevents Future Osteoporosis
The Female Athlete Triad: Do Female Athletes Need to Take Special Care to Avoid Low Energy Availability
Components of the Female Athlete Triad
Research on the female athlete triad for the past decade or so has culminated in an updated definition published by ACSM. The 2007 ACSM positional stand looks at each disorder as it exists on a continuous spectrum instead of a severe pathologic endpoint.7 Disordered eating has been replaced by a spectrum from “optimal energy availability” to “low energy availability with or without an eating disorder.” Amenorrhea has been replaced by a spectrum from “eumenorrhea” to “functional hypothalamic amenorrhea.” Finally, osteoporosis has been replaced by a spectrum from “optimal bone health” to “osteoporosis.”
The 2007 ACSM positional stand also emphasizes that energy availability is the cornerstone that the rest of the triad stems from.7 Without correction of this key component, full recovery from the female athlete triad is not possible.
Energy Availability7, 8
This component of the female athlete triad is defined as “dietary energy intake minus exercise energy expenditure” and is aimed toward capturing the athletes who may have eating and weight concerns, but who do not have “significant psychopathology” and who do not meet the criteria for disordered eating.
The term disordered eating was coined to include pathologic eating behaviors that do not meet the strict Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition (DSM-IV) requirements for anorexia or bulimia and therefore includes anorexia nervosa and bulimia nervosa but is not limited to these diagnoses. Indeed, disordered eating includes a spectrum of behaviors from as simple as the athlete not taking in enough food to offset the energy that is expended to preoccupation with eating and a fear of becoming fat by instituting measures such as food restrictions and/or the use of diet pills, laxatives, and/or diuretics.
Menstrual Dysfunction7
This component is now used to describe the spectrum from eumenorrhea to amenorrhea and enables clinicians to capture a large portion of athletes who may have low estrogen levels but who may still experience menstruation. This condition includes luteal suppression, anovulation, oligomenorrhea, and primary and secondary amenorrhea. Luteal suppression is marked by a shortened luteal phase and a prolonged follicular phase in which there is a decrease in estradiol levels. The cycle length usually does not change, the athlete will continue to ovulate—although it may be later in the cycle—and the athlete usually has regular menstruation.
Anovulation is marked by low levels of estradiol and progesterone that deter follicular development, as well as an absence of ovulation. Although the circulating hormones are decreased, female athletes will often menstruate, some experiencing shortened or prolonged cycles due to their uterine lining being stimulated by the low levels of estradiol. Oligomenorrhea is defined as “greater than 35 days between cycles.”
Amenorrhea usually refers to secondary amenorrhea, although delayed menarche (primary amenorrhea) can occur in young athletes. By consensus, secondary amenorrhea is the “absence of menstrual cycles lasting more than 3 months after menarche has occurred.” Physicians are cautioned that a full workup be completed to rule out any other causes of menstrual dysfunction before attribution to low estradiol levels stemming from low energy availability.9
Bone Health7, 10
The final component of the female athlete triad exists on a continuum from optimal bone health to osteoporosis and focuses on bone strength, which consists of BMD and/or content and bone quality. Bone quality refers to bone turnover rates—resorption versus formation, microarchitecture or trabeculae, time for maturation of the new bone matrix, bone geometry and size, etc. The inability to measure bone quality at this time leaves one half of the equation for bone health empty and offers an explanation for why some athletes with the same poor bone density as their colleagues, may suffer more fractures. Therefore, dual energy x-ray absorptiometry (DXA) scans are used as a quantitative measure of bone health.
When reporting BMD, T-scores are used for the diagnosis of osteopenia and osteoporosis. However, the T-score measures the standard deviations (SDs) below the mean to predict fracture risks for postmenopausal woman. Concern over mislabeling of our premenopausal athletes, adolescents and children, led to a positional stand to be issued by the International Society for Clinical Densitometry (ISCD).10 The recommendation is to determine BMD by comparing chronologic age and sex using a Z-score distribution. The ISCD further recommends that the term osteopenia not be used in describing bone density and that the term osteoporosis be reserved for “low BMDs” with secondary clinical risk factors such as “chronic malnutrition, eating disorders, hypogonadism, glucocorticoid exposure, and previous fractures.”10
Athletes that have a Z-score that is 2 SDs below the mean are to be termed “low bone density below the expected range for age” for premenopausal women and “low bone density for chronologic age” for children. The ACSM, in their 2007 positional stand, further defined “low BMD” as “a history of nutritional deficiencies, hypoestrogenism, stress fractures, and/or other secondary clinical risk factors for fracture together with a BMD Z-score between –1.0 and –2.0,” and osteoporosis as “secondary clinical risk factors for fracture with a Z-score ≤ –2.0.”7
Because most athletes already have a higher BMD than nonathletes, the ACSM also cautions physicians to perform further workup for any athlete with a BMD Z-score < –1.0, even in the absence of fracture.7
Related eMedicine topics:
Low Energy Availability in the Female Athlete
Menstruation Disorders
Utility of Bone Markers in Osteoporosis
Related Medscape topics:
Resource Center Eating Disorders
Specialty Site Women's Health
Frequency
United States
Although all female athletes are at risk for the female athlete triad or any of its components, sports that have an aesthetic component (eg, ballet, figure skating, gymnastics) or sports tied to a weight class (eg, tae kwon do, judo, wrestling) have a higher prevalence of affected female athletes.7, 11, 12, 13, 14 Obtaining exact epidemiologic data is difficult because of the lack of reporting and/or gathering of data from athletes. Similar to individuals with anorexia or bulimia, many athletes with the triad try to hide their symptoms or behavior from friends, family, trainers, or coaches. This is the primary reason why diagnosis is so difficult. In fact, the vast majority of cases are diagnosed only after advanced symptoms become apparent. Milder cases may be extremely difficult to diagnose if the physician does not already have a high degree of suspicion.7, 15, 16, 17, 18
The prevalence of how many athletes suffer from low energy availability is difficult to assess. Multiple factors (eg, gathering accurate caloric intake data from athletes, measuring energy expenditure, which sports to include, which eating attitude survey to use, definitions of “eating disorder”) compound the issue. However, it is known that an athlete is at increased risk to suffer from the spectrum of reduced to low energy availability with or without an eating disorder if the athlete has a comorbid psychologic disorder, such as anxiety, depression, and/or obsessive compulsive disorder (OCD). In some studies, disordered eating in the female athletic population has been estimated to be as high as 62%, with the incidence of anorexia nervosa and bulimia (as defined in the DSM-IV) estimated at 4-39%.
The prevalence of menstrual dysfunction is also difficult to assess. Many studies have reported a range from as low as 6% to as high as 79%, depending on the sport studied, the patient's age, the definition and assessment of menstrual dysfunction, the use of oral contraceptives, the training volume, and the presence of subclinical menstrual disorders, such as luteal suppression and anovulation. Studies continue to be performed, and hopefully, more data will be available soon.
The prevalence of bone health, reported in the form of BMD, is likewise difficult to assess due to the cost prohibitiveness of DXA scans. Osteopenia has been reported as high as 50% and as low as 22% for athletes relative to 12% in the nonathlete population. Osteoporosis has been also reported from 0-13% for athletes and 2.3% for nonathletes. With the ISCD recommendations of using Z-scores instead of T-scores, more research will need to be done to obtain accurate data for athletes.
In the near future, epidemiologic data regarding the female athlete triad may become available. Many preparticipation physical questionnaires now include questions about whether the athlete is satisfied with her current weight and about how much weight she would like to gain or lose. These simple inquiries may reveal the first warning signs of the female athlete triad.
Functional Anatomy
Bones of the lower extremities, pelvis, and vertebrae are the most common to be affected by poor bone health when an athlete is suffering from the female athlete triad, manifesting as stress and frank fractures of these areas. Peak bone mass is obtained between the ages of 20 and 30 years, with peak bone mineral content being accrued between ages 9 and 20 years.
Menstruating athletes gain approximately 2-4% of bone mass per year, whereas amenorrheic athletes tend to loose 2% of BMD per year. Therefore, it is easy to see why athletes who are involved in high-impact sports can still be more susceptible to fractures than their nonathletic and menstruating athletic counterparts. Often these fractures are due to the increased stress sustained by these bones in the course of physical activity. In this respect, athletes with the female athlete triad are not unlike their healthy counterparts. However, those who have the triad or portions of it are more susceptible to multiple fractures, and they are also more likely to sustain fractures in larger, less commonly affected bones (eg, femoral neck, pelvis, vertebra).
Related eMedicine topics:
Femoral Neck Stress Fracture
Lumbosacral Spine Acute Bony Injuries
Pelvic Fractures
Related Medscape topics:
Resource Center Exercise and Sports Medicine
Resource Center Osteoporosis
Resource Center Trauma
Clinical
History
When an athlete is identified as being at risk for the female athlete triad, a detailed screening history should be obtained. The purpose of the screening process is to gather information about the patient's medical history and dietary and exercise behaviors and to evaluate the athlete for existing psychopathology and medical complications.
The team physician should not undertake every aspect of the evaluation and care of a woman with female athlete triad; rather, a multidisciplinary approach should be used. If available and deemed necessary, consultation with a psychiatrist or clinical psychologist with experience in disordered eating, an orthopedic surgeon, a gynecologist, a cardiologist, a sports nutritionist, and the athlete's athletic trainer should be added to the treatment team to augment the physicians personal knowledge of the athlete and team.
Past medical history
Particular attention should be given to any other endocrine disorders, such as thyroid abnormalities, panhypopituitarism, and diabetes. A careful and thorough history of past stress fractures and complete fractures should be elicited, and the history should be verified with trainers, coaches, or parents, if possible.
Menstrual history
Menstrual history should include the age of menarche, length of menses, and menstrual cycle, as well as any missed menses and the menstrual pattern during the season or that time period when the athlete is exercising the most. Athletes in some sports in which strength is important may be using anabolic steroids, which are a potential cause of secondary amenorrhea. However, because the most common cause of secondary amenorrhea in young females is pregnancy, this possibility should be discussed and ruled out.
Psychosocial history
At the first visit, routine questions should be asked, such as those pertaining to tobacco or alcohol use. As trust is built up over the next few visits, further details about the patient's background should be elicited, such as illegal drug use, sexual or physical abuse, depression, anxiety, previous eating disorders, suicidal behavior, recent trauma or illness, change in coaches, failure at school or work, or other significant personal events.
The lack of a family or social support system is a risk factor for the female athlete triad. Women just entering college are often in a new environment that is physically distant from their friends and family. This move can be made more traumatic if the pressure to perform as a collegiate athlete is added to the athlete's psyche. Sometimes, these women fall back on athletics—one of the few things that may have remained constant since high school—to gain acceptance from coaches and fellow athletes.
Exercise history
The number of hours per day that the athlete spends in practice and exercise should be determined. The examiner should make a point of asking how much time is spent in formal practice with the team or coach and how much additional time apart from scheduled workouts is spent, for example, conditioning, running, and lifting. The athlete should also be asked if this workout pattern changes during the off-season or if it continues year round.
Nutritional assessment
Just because the athlete is consuming what would otherwise be considered a normal number of calories per day does not mean that she is consuming enough calories for her lifestyle. Women who exercise for hours per day are likely to need more than the 1600-2000 kcal that their body weight would indicate.The Eating Disorder Inventory (EDI), for example, is a questionnaire designed to help identify those with disordered eating. Although the EDI is not a precise instrument to aid in identifying eating disorders, it can be used to identify people at risk for anorexia or bulimia.
Some athletes with the triad adopt restrictive diets, and they may sometimes use personal convictions or religious beliefs to justify their behavior. Many times, the athlete may develop a recognizable pattern of disordered eating in which they progressively establish and exceed dietary boundaries. For example, a diet of no red meat may progress to vegetarianism, then to veganism over the course of months.
The athlete's convictions may be subconscious excuses reflecting what is socially acceptable to her peers and authority figures. Of course, not every athlete with a diet that restricts certain foods has the female athlete triad, and not every athlete is consciously participating in disordered eating. For many athletes, the low energy availability is due to lack of education about caloric needs for their exercise and/or training. This is yet another reason why the diagnosis is difficult to establish.
Current medications
The patient's history should include the use of any prescription medications, including contraceptive medications, over-the-counter (OTC) medications, as well as herbal medicines and dietary supplements. Many people do not consider OTC medicines to be "real" medicines, and athletes with the triad commonly use or abuse dietary supplements or ergogenic aids. Athletes may take the common stimulant ephedrine, to lose weight or to burn fat; however, this stimulant is known to cause mild tachycardia and has been at least temporally associated with several deaths in the athletic population. This tachycardia could potentially mask the bradycardia found in athletes with advanced eating disorders. Attention should also be directed toward any present or past use of hormones because they can also cause menstrual irregularities.
Physical
In general, a complete screening physical examination should be preformed. As with the history taking, postponing some parts of the physical examination until a relationship has developed between the athlete and physician may be appropriate. For example, a gynecologic and breast examination may be better suited for a second or third visit. The exception to this rule is if the amenorrhea is primary, that is, if the athlete has never had normal menses. In this case, pelvic examination to verify the presence of a uterus should be performed at the first visit. Pelvic ultrasonography can aid in this determination. The diagnosis is largely clinical, and no test enables definitive diagnosis of the female athlete triad.
Many times, the physician diagnoses a stress fracture first; then the menstrual dysfunction; and, lastly, the low energy availability, with or without an eating disorder. However, this sequence is the reverse of the order in which the female athlete triad develops.
Of note, female athletes who come to a summertime preparticipation physical examination wearing many baggy clothes or sweatpants and sweatshirts should raise concern. Athletes with the triad may try to hide their body weight loss. In addition, some athletes may present for the examination and then refuse to let the physician or anyone else examine them. This is often the case in 14- to 16-year-old athletes who participate in high school sports.
- Anthropometric data and vital signs should be obtained without comment about weight or weight-to-height ratios.
- Body mass index (BMI) charts are calibrated for the general population and may not be suitable for the athletic subpopulation.
- If possible, the patient's percentage of body fat composition can be determined.
- Pediatric growth charts are often helpful in teenagers or college students.
- The remainder of the physical examination is directed toward other causes of amenorrhea or osteoporosis and secondary signs of the triad.
- The thyroid should be palpated for possible goiter.
- The parotid glands should be palpated for evidence of hypertrophy. This is sometimes found after chronic purging.
- Bulimia can cause bloodshot eyes and petechiae of the sclera or cheeks. Dental examination can show dental caries or pitting from the regurgitation of stomach acid through the oropharynx. If a finger is used to induce vomiting, the knuckles may be scarred from the patient biting down on them during regurgitation. The Russell sign is typical callous formation on the distal extensor surface of the long finger that is used to induce vomiting.
- Anorexia may cause cachexia, bradycardia, and hypotension later in the course of the disease. Although many well-conditioned athletes may have a resting heart rate below that of the general population, an electrocardiogram (ECG) should be obtained if the athlete's resting heart rate less than 50 beats per minute (bpm). Sinus bradycardia is an early cardiac sign in eating disorders, but conduction abnormalities (eg, atrioventricular conduction blocks, ventricular tachycardia) may become evident in more advanced cases. A baseline ECG may also be obtained for future comparison.
- Dermatologic examination sometimes reveals lanugo or the dry or yellow skin that is sometimes found in those with anorexia.
- Athletes with the female athlete triad usually report signs or symptoms related to osteoporosis (eg, fracture, stress fracture) before they report menstrual abnormalities.
Causes
The theory behind the female athlete triad is that this syndrome is caused by an energy drain/caloric deficit (ie, the athlete's energy expenditure exceeds her dietary energy intake).7, 8 This low energy availability, whether subconscious or conscious, causes disruption of the hypothalamic-pituitary-ovarian axis, which results in decreased gonadotropin-releasing hormone (GnRH) pulsatility and low luteinizing hormone (LH) and follicle-stimulating hormone (FSH) levels.19 This, in turn, leads to decreased estrogen production, causing menstrual dysfunction, and the decreased estrogen levels in turn affect calcium resorption and bone accretion, causing decreased bone health.
Some studies have shown that 30 kcal/kg of lean body mass is a crucial threshold for maintaining menstrual function7; they have also demonstrated that increasing exercise drastically, but covering the energy expenditure with increased caloric intake did not result in disruption of LH pulsatility. Conversely, decreasing an athlete’s caloric intake to less than 30 kcal/kg within 5 days resulted in decreased LH pulsatility. All of which support the energy drain theory.
The hormone leptin has also garnered increased interest. Secreted by adipocytes, leptin appears to influence the metabolic rate, and levels are proportional to a person's BMI. This hormone may be a significant mediator of reproductive function, and many studies have demonstrated that low levels of leptin correlate positively with amenorrhea and infertility. Furthermore, leptin receptors have been found on hypothalamic neurons involved in the control of GnRH pulsatility and in bone, which may also affect osteoblastic function.
As discussed previously, athletes in some sports that are linked to an aesthetic component or a weight class are more likely to develop the triad. These athletes often attempt to reach unrealistic weight and body fat goals dictated by their sport, to the detriment of their health.11, 12, 20, 21 Emotional stressors can also often be identified as inciting factors in athletes with the triad. Death of a coach or family member, growth spurts, illness that prevents training, and other events that an athlete cannot control often lead to disordered eating and excessive training—a portion of their life that they can control.
For many, moving to a university setting initiates the triad cascade. Some young women may move long distances away from their family and friends, and they have the added increase in responsibility of a sports scholarship and academic workload. Collegiate athletes have the additional pressure of performing up to the more difficult standards of collegiate competition, with a new coach and trainer, as well as alongside athletes who may have had the benefit of 2-3 years of additional experience. Not surprisingly, the prevalence of the triad suddenly increases in college freshman.
| ||||||||||
References
Beals KA, Meyer NL. Female athlete triad update. Clin Sports Med. Jan 2007;26(1):69-89. [Medline].
Templeton KJ, Hame SL, Hannafin JA, et al. Sports injuries in women: sex- and gender-based differences in etiology and prevention. Instr Course Lect. 2008;57:539-52. [Medline].
American College of Sports Medicine. The female athlete triad: disordered eating, amenorrhea, osteoporosis -- a call to action. Sports Med Bull. 1992;27:4.
Brunet M 2nd. Female athlete triad. Clin Sports Med. Jul 2005;24(3):623-36, ix. [Medline].
Otis CL, Drinkwater B, Johnson M, Loucks A, Wilmore J. American College of Sports Medicine position stand. The female athlete triad. Med Sci Sports Exerc. May 1997;29(5):i-ix. [Medline].
Burrows M, Shepherd H, Bird S, MacLeod K, Ward B. The components of the female athlete triad do not identify all physically active females at risk. J Sports Sci. Oct 2007;25(12):1289-97. [Medline].
Nattiv A, Loucks AB, Manore MM, et al. American College of Sports Medicine position stand. The female athlete triad. Med Sci Sports Exerc. Oct 2007;39(10):1867-82. [Medline].
De Souza MJ, Williams NI. Beyond hypoestrogenism in amenorrheic athletes: energy deficiency as a contributing factor for bone loss. Curr Sports Med Rep. Feb 2005;4(1):38-44. [Medline].
Shangold M, Rebar RW, Wentz AC, Schiff I. Evaluation and management of menstrual dysfunction in athletes. JAMA. Mar 23-30 1990;263(12):1665-9. [Medline].
The Writing Group for the International Society for Clinical Densitometry (ISCD) Position Development Conference. Diagnosis of osteoporosis in men, premenopausal women, and children. J Clin Densitom. Spring 2004;7(1):17-26. [Medline].
Rosen LW, Hough DO. Pathogenic weight-control behavior of female college gymnasts. Phys Sportsmed. 1988;16(9):141-6.
Kiernan M, Rodin J, Brownell KD, Wilmore JH, Crandall C. Relation of level of exercise, age, and weight-cycling history to weight and eating concerns in male and female runners. Health Psychol. 1992;11(6):418-21. [Medline].
Sabatini S. The female athlete triad. Am J Med Sci. Oct 2001;322(4):193-5. [Medline].
Sanborn CF, Horea M, Siemers BJ, Dieringer KI. Disordered eating and the female athlete triad. Clin Sports Med. Apr 2000;19(2):199-213. [Medline].
Bonci CM, Bonci LJ, Granger LR, et al. National athletic trainers' association position statement: preventing, detecting, and managing disordered eating in athletes. J Athl Train. Jan-Mar 2008;43(1):80-108. [Medline]. [Full Text].
Lebrun CM. The female athlete triad: what's a doctor to do?. Curr Sports Med Rep. Dec 2007;6(6):397-404. [Medline].
Nichols JF, Rauh MJ, Lawson MJ, Ji M, Barkai HS. Prevalence of the female athlete triad syndrome among high school athletes. Arch Pediatr Adolesc Med. Feb 2006;160(2):137-42. [Medline].
Waldrop J. Early identification and interventions for female athlete triad. J Pediatr Health Care. Jul-Aug 2005;19(4):213-20. [Medline].
Loucks AB. Effects of exercise training on the menstrual cycle: existence and mechanisms. Med Sci Sports Exerc. Jun 1990;22(3):275-80. [Medline].
Wilmore JH. Eating and weight disorders in the female athlete. Int J Sport Nutr. Jun 1991;1(2):104-17. [Medline].
Brownell KD, Steen SN, Wilmore JH. Weight regulation practices in athletes: analysis of metabolic and health effects. Med Sci Sports Exerc. Dec 1987;19(6):546-56. [Medline].
Skolnick AA. 'Female athlete triad' risk for women. JAMA. Aug 25 1993;270(8):921-3. [Medline].
Nattiv A, Agostini R, Drinkwater B, Yeager KK. The female athlete triad. The inter-relatedness of disordered eating, amenorrhea, and osteoporosis. Clin Sports Med. Apr 1994;13(2):405-18. [Medline].
Burckes-Miller ME, Black DR. Male and female college athletes: prevalence of anorexia nervosa and bulimia nervosa. J Athl Train. 1988;23(2):137-40.
Di Pietro L, Stachenfeld N, Pierce JB. The female athlete triad revisited. Med Sci Sports Exerc. Sep 2005;37(9):1643; author reply 1644. [Medline].
Drinkwater BL, Bruemner B, Chesnut CH 3rd. Menstrual history as a determinant of current bone density in young athletes. JAMA. Jan 26 1990;263(4):545-8. [Medline].
Drinkwater BL, Nilson K, Chesnut CH 3rd, et al. Bone mineral content of amenorrheic and eumenorrheic athletes. N Engl J Med. Aug 2 1984;311(5):277-81. [Medline].
Fagan KM. Pharmacologic management of athletic amenorrhea. Clin Sports Med. Apr 1998;17(2):327-41. [Medline].
Frisch RE, Gotz-Welbergen AV, McArthur JW, et al. Delayed menarche and amenorrhea of college athletes in relation to age of onset of training. JAMA. Oct 2 1981;246(14):1559-63. [Medline].
Frisch RE, McArthur JW. Menstrual cycles: fatness as a determinant of minimum weight for height necessary for their maintenance or onset. Science. Sep 13 1974;185(4155):949-51. [Medline].
Loucks AB, Horvath SM. Athletic amenorrhea: a review. Med Sci Sports Exerc. Feb 1985;17(1):56-72. [Medline].
Loucks AB, Nattiv A. Essay: the female athlete triad. Lancet. Dec 2005;366(suppl 1):S49-50. [Medline].
NIH Consensus Development Panel on Optimal Calcium Intake. NIH Consensus conference. Optimal calcium intake. JAMA. Dec 28 1994;272(24):1942-8. [Medline].
Otis CL. Exercise-associated amenorrhea. Clin Sports Med. Apr 1992;11(2):351-62. [Medline].
Palla B, Litt IF. Medical complications of eating disorders in adolescents. Pediatrics. May 1988;81(5):613-23. [Medline].
Rigotti NA, Neer RM, Skates SJ, Herzog DB, Nussbaum SR. The clinical course of osteoporosis in anorexia nervosa. A longitudinal study of cortical bone mass. JAMA. Mar 6 1991;265(9):1133-8. [Medline].
Torstveit MK, Sundgot-Borgen J. The female athlete triad exists in both elite athletes and controls. Med Sci Sports Exerc. Sep 2005;37(9):1449-59. [Medline].
Warren MP. The effects of exercise on pubertal progression and reproductive function in girls. J Clin Endocrinol Metab. Nov 1980;51(5):1150-7. [Medline].
Warren MP, Brooks-Gunn J, Hamilton LH, Warren LF, Hamilton WG. Scoliosis and fractures in young ballet dancers. Relation to delayed menarche and secondary amenorrhea. N Engl J Med. May 22 1986;314(21):1348-53. [Medline].
Warren MP, Perlroth NE. The effects of intense exercise on the female reproductive system. J Endocrinol. Jul 2001;170(1):3-11. [Medline].
Further Reading
Keywords
FAT, sports amenorrhea, sports-related amenorrhea, amenorrhea, female athletes, disordered eating, anorexia, bulimia, osteoporosis, energy availability, low energy availability in the female athlete, menstrual dysfunction, menstruation disorders, bone health, functional hypothalamic amenorrhea
