Female athletes often complain of low energy availability, which is defined as energy from oral nutrition less energy used for exercise. As such, low energy may result (whether intentionally or unintentionally) from more energy expenditure, less oral nourishment, or both. A chronic energy deficit can occur in the female athlete with musculoskeletal and reproductive dysfunction. Low energy (with or without an eating disorder) in combination with a menstrual disorder and altered mineral bone density is known as the female athlete triad. Early identification of low energy in the female athlete and thorough understanding of the syndrome and its progression is important to prevent short- and long-term consequences.
The limiting factor for performance during training and competition in high-intensity sports of long duration is energy intake. A substantial percentage of energy intake is provided through carbohydrates, and to a lesser extent, proteins and fats. To maintain optimal energy availability, increased energy expenditure should ideally justify increased nutritional intake. However, this is not always the case. Many female athletes, either deliberately or inadvertently, fail to maintain adequate energy intake. There exists a direct correlation between carbohydrate availability and reproductive and skeletal health.
Female athletes in any sport, regardless of competition level, can potentially develop the triad. However, females participating in endurance sports such as track and field, swimming, and rowing or those requiring subjective judging like gymnastics and figure skating are most at risk.
When females intentionally create this energy deficit, it is described as an eating disorder. Females athletes are 5 to 10 times more likely than male athletes to have an eating disorder. The prevalence of clinical eating disorders, such as anorexia nervosa or bulimia nervosa, among female elite athletes ranges from 16% to 47%. A substantial percentage of females with eating disorders also have a concomitant personality disorder, substance abuse disorder, or obsessive-compulsive disorder, and the rates of suicide are greater for these women than for healthy females of the same age.
Low Energy Availability
Energy availability the energy acquired through oral nutrition less the energy expended during exercise and baseline daily metabolic requirements. Energy availability, whether through increased expenditure or decreased oral intake, is the main factor in the triad. Disordered eating may be intentional or unintentional. Eating disorders such as anorexia nervosa or bulimia nervosa are intentional causes. However, many female athletes without the diagnosis of an eating disorder may exhibit disordered eating habits. Most of the time, this will occur unknowingly, and the athlete will not take in enough energy. The extensive continuum of disordered eating ranges from healthy dieting to fasting, skipping meals, using diet pills or laxatives, and binging and purging A direct correlation exists between carbohydrate availability and reproductive and skeletal health. Low energy availability secondary to disordered eating results in menstrual dysfunction and low mineral density.
Altered Bone Mineral Density
Bone tissue is dynamic and constantly being remodeled by osteoclasts (which resorb old bone) and osteoblasts (which form new bone). This is done under the control of polypeptides, steroid hormones, thyroid hormones, cytokines, and growth factors. Secondary to hypothalamic dysfunction, female athletes function at a low estrogen state. Estrogen's principal role in bone is to directly act on osteoblasts, and it has an indirect effect on osteoclasts to prevent bone resorption Athletes should have a 5% to 15% higher bone mineral density than age-matched nonathlete. Altered bone mineral density will increase bone fragility and increase the risk of fractures. The incidence of stress fractures is greater in amenorrheic athletes, and bone density has been shown to negatively correlate with the number of missed menstrual cycles since menarche.
Menstrual Dysfunction (amenorrhea or oligomenorrhea)
Menstrual abnormalities result from altered hypothalamic function. Menstrual dysfunction in the female athlete directly correlates to decreased estrogen. It may be primary or secondary amenorrhea. Primary amenorrhea is defined as no menstruation by 14 years of age without the development of secondary sexual characteristics or by 16 years, even if the female has undergone other normal changes that occur during puberty. The persistent absence of menstrual cycles beginning sometime after menarche is called secondary amenorrhea.
All female athletes need a thorough history in addition to the routine history, with a focus on the components of the athlete's nutritional, musculoskeletal, menstrual, endocrine/metabolic, psychosocial, performance, and medication history.
The physical examination should screen for pathologies that could cause metabolic and hormonal abnormalities. Thyroid should be palpated for evidence of enlargement or irregularity. Pay particular attention to the teeth, noting tooth decay from repeated vomiting and subsequent hard brushing, and parotid glands for evidence of hypertrophy, as with bulimia nervosa. Perform visual field testing to assess for pituitary macroadenoma; if large enough, it may press on the optic chiasm and cause bitemporal non-homonomous hemianopsia. A thorough skin exam should also be performed.
A pelvic examination should be performed when appropriate, particularly when a patient presents with delayed or disordered menarche.
A trainer or team physician should conduct a baseline urinary acetoacetate measurement. Normally menstruating athletes can self-measure or have a trainer perform monthly measurements of urinary acetoacetate in times of increased training. The goal is to completely remove urinary ketones before and after a meal as well as before and after training.
Pelvic Ultrasound can be useful for determining the etiology of primary amenorrhea (eg, the presence of ovaries, uterus). If an abnormal pituitary function is suspected, thin-section magnetic resonance imaging (MRI) of the head through the sella turcica should be performed. Electrocardiography may show bradycardia, which is common in athletes, and a resting heart rate of fewer than 50 beats per minute should be explored with a baseline ECG.
If evidence from the patient's history or physical examination suggests the presence of a stress fracture, plain radiography should be the initial test of choice. A 3-phase bone scan should be performed if the radiographs are negative. Dual radiograph absorptiometry can be used in athletes with multiple stress fractures.
A dual-energy x-ray absorptiometry scan can also be used to assess for osteopenia or osteoporosis.
Initial treatment involves correction of the underlying cause. Most of the time this is a low energy state whether through an increased caloric intake, decreased physical activity, or both. Consulting a nutritionist or sports dietician is important.
For menstrual dysfunction, the female athlete should be referred to an OB/GYN who can evaluate and treat the patient. Treatments for menstrual dysfunction in the female athlete are initially limited to hormone replacement therapy with cyclic estrogen and progesterone.
Female athletes with osteopenia or osteoporosis may be treated with oral vitamin D and calcium or bisphosphonates depending on the severity of the bone mineral density loss and risk factors for fractures.
Those females diagnosed with a mental health disorder such as depression, anxiety, or an eating disorder should be referred to a psychiatrist and/or psychologist for evaluation and treatment.
A 2014 consensus statement published in the British Journal of Sports Medicine stated that successful treatment of athletes and exercising women is contingent on an interprofessional approach for recovery from the triad, including a primary care and/or sports medicine physician, a sports dietitian, and a mental health nurse/practitioner. These patients have multiple organ dysfunction and yet at the same time remain noncompliant with therapy. The treatment is often prolonged and these patients need long term monitoring including bone density. The outcomes of these patients is guarded; despite mental health counseling, relapses are common.  (Level V)
|||O'Leary TJ,Gifford RM,Double RL,Reynolds RM,Woods DR,Wardle SL,Greeves JP, Skeletal responses to an all-female unassisted Antarctic traverse. Bone. 2019 Apr; [PubMed PMID: 30735797]|
|||Brook EM,Tenforde AS,Broad EM,Matzkin EG,Yang HY,Collins JE,Blauwet CA, Low energy availability, menstrual dysfunction, and impaired bone health: A survey of elite para athletes. Scandinavian journal of medicine [PubMed PMID: 30644600]|
|||Merrigan B,Leggit JC, Broadening the Female Athlete Triad: Relative Energy Deficiency in Sport. American family physician. 2019 Jan 15; [PubMed PMID: 30633487]|
|||Joy EA, Address risk factors to prevent bone stress injuries in male and female athletes. British journal of sports medicine. 2019 Feb; [PubMed PMID: 30606724]|
|||Kraus E,Tenforde AS,Nattiv A,Sainani KL,Kussman A,Deakins-Roche M,Singh S,Kim BY,Barrack MT,Fredericson M, Bone stress injuries in male distance runners: higher modified Female Athlete Triad Cumulative Risk Assessment scores predict increased rates of injury. British journal of sports medicine. 2019 Feb; [PubMed PMID: 30580252]|
|||Sawai A,Mathis BJ,Natsui H,Zaboronok A,Mitsuhashi R,Warashina Y,Mesaki N,Shiraki H,Watanabe K, Risk of female athlete triad development in Japanese collegiate athletes is related to sport type and competitive level. International journal of women's health. 2018; [PubMed PMID: 30464644]|
|||Daily JP,Stumbo JR, Female Athlete Triad. Primary care. 2018 Dec; [PubMed PMID: 30401345]|
|||Tosi M,Maslyanskaya S,Dodson NA,Coupey SM, The Female Athlete Triad: A Comparison of Knowledge and Risk in Adolescent and Young Adult Figure Skaters, Dancers, and Runners. Journal of pediatric and adolescent gynecology. 2019 Apr; [PubMed PMID: 30395981]|
|||Cleary S,Chi V,Feinstein R, Female athletes: managing risk and maximizing benefit. Current opinion in pediatrics. 2018 Dec; [PubMed PMID: 30300327]|
|||Ackerman KE,Singhal V,Baskaran C,Slattery M,Campoverde Reyes KJ,Toth A,Eddy KT,Bouxsein ML,Lee H,Klibanski A,Misra M, Oestrogen replacement improves bone mineral density in oligo-amenorrhoeic athletes: a randomised clinical trial. British journal of sports medicine. 2019 Feb; [PubMed PMID: 30301734]|
|||Silva AM, Structural and functional body components in athletic health and performance phenotypes. European journal of clinical nutrition. 2019 Feb; [PubMed PMID: 30287933]|
|||Syed-Abdul MM,Soni DS,Wagganer JD, Impact of a Professional Nutrition Program on a Female Cross Country Collegiate Athlete: A Case Report. Sports (Basel, Switzerland). 2018 Aug 19; [PubMed PMID: 30126236]|
|||Shampain K,Gaetke-Udager K,Leschied JR,Meyer NB,Hammer MR,Denay KL,Yablon CM, Injuries of the adolescent girl athlete: a review of imaging findings. Skeletal radiology. 2019 Jan; [PubMed PMID: 30123946]|
|||Heikura IA,Uusitalo ALT,Stellingwerff T,Bergland D,Mero AA,Burke LM, Low Energy Availability Is Difficult to Assess but Outcomes Have Large Impact on Bone Injury Rates in Elite Distance Athletes. International journal of sport nutrition and exercise metabolism. 2018 Jul 1; [PubMed PMID: 29252050]|
|||Tenforde AS,Carlson JL,Chang A,Sainani KL,Shultz R,Kim JH,Cutti P,Golden NH,Fredericson M, Association of the Female Athlete Triad Risk Assessment Stratification to the Development of Bone Stress Injuries in Collegiate Athletes. The American journal of sports medicine. 2017 Feb; [PubMed PMID: 28038316]|