Should you suspect the female athlete triad?

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Applied Evidence

Should you suspect the female athlete triad?

J Fam Pract. 2014 April;63(4):187-192

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References

1. Nattiv A, Loucks AB, Manore MM, et al; American College of Sports Medicine. American College of Sports Medicine position stand on the female athlete triad. Med Sci Sports Exerc. 2007;39:1867-1882.

2. Nattiv A, Agostini R, Drinkwater B, et al. The female athlete triad. The inter-relatedness of disordered eating, amenorrhea, and osteoporosis. Clin Sports Med. 1994;13:405-418.

3. Nichols JF, Rauh MJ, Lawson MJ, et al. Prevalence of the female athlete triad syndrome among high school athletes. Arch Pediatr Adolesc Med. 2006;160:137-142.

4. Torstveit MK, Sungot-Borgen J. The female athlete triad exists in both athletes and controls. Med Sci Sports Exerc. 2005; 37:1449-1459.

5. Byrne S, McLean N. Elite athletes: effects of the pressure to be thin. J Sci Med Sport. 2002;5:80-94.

6. Sundgot-Borgen J, Torstveit MK. Prevalence of eating disorders in elite athletes is higher than in the general population. Clin J Sport Med. 2004;14:25-32.

7. Beals KA, Manore MM. Disorders of the female athlete triad among collegiate athletes. Int J Sport Nutr Exerc Metab. 2002;12:281-293.

8. De Souza MJ, Miller BE, Loucks AB, et al. High frequency of luteal phase deficiency and anovulation in recreational women runners: blunted elevation in follicle-stimulating hormone observed during luteal-follicular transition. J Clin Endocrinol Metab. 1998;83:4220-4232.

9. Khan KM, Liu-Ambrose T, Sran MM, et al. New criteria for the female athlete triad syndrome? As osteoporosis is rare, should osteopenia be among the criteria for defining the female athlete triad syndrome? Br J Sports Med. 2002;36:10-13.

10. Loucks AB. Effects of exercise training on the menstrual cycle: existence and mechanisms. Med Sci Sports Exerc. 1990;22:275-280.

11. Loucks AB, Verdun M, Heath EM. Low energy availability, not the stress of exercise, alters LH pulsatility in exercising women. J Appl Physiol (1985). 1998;84:37-46.

12. Mendelsohn FA, Warren MP. Anorexia, bulimia, and the female athlete triad: evaluation and management. Endocrinol Metab Clin N Am. 2010;39:155-167.

13. Misra M, Miller KK, Tsai P, et al. Elevated peptide YY levels in adolescent girls with anorexia nervosa. J Clin Endocrinol Metab. 2006;91:1027-1033.

14. Lawson EA, Klibanski A. Endocrine abnormalities in anorexia nervosa. Nat Clin Pract Endocrinol Metab. 2008;4:407-414.

15. Brancaccio P, Maffulli N, Buonauro R, et al. Serum enzyme monitoring in sports medicine. Clin Sports Med. 2008;27:1-18, vii.

16. NIH Consensus Development Panel on Osteoporosis Prevention, Diagnosis, and Therapy. Osteoporosis prevention, diagnosis, and therapy. JAMA. 2001;285:785-795.

17. 2007 ISCD Official Positions–Pediatric. The International Society for Clinical Densitometry Web site. Available at: http://www.iscd.org/official-positions/2007-iscd-official-positions-pediatric. Accessed February 26, 2014.

18. 2013 ISCD Official Positions–Adult. The International Society for Clinical Densitometry Web site. Available at: http://www.iscd.org/official-positions/2013-iscd-official-positions-adult. Accessed February 26, 2014.

19. Position stand on the female athlete triad. The Internal Olympic Committee Web site. Available at: http://www.olympic.org/Documents/Reports/EN/en_report_917.pdf. Accessed February 3, 2014.

20. The Female Athlete Triad Coalition Web site. Available at: http://www.femaleathletetriad.org. Accessed February 3, 2014.

21. Eating disorders. National Institute of Mental Health Web site. Available at: http://www.nimh.nih.gov/health/publications/eating-disorders/index.shtml. Accessed February 26, 2014.

22. Synthetic Calcitonin (Salmon) nasal spray (ns)—market withdrawal of all products, effective October 1st, 2013—for health professionals. Government of Canada Health Canadians Web site. Available at: http://healthycanadians.gc.ca/recall-alertrappel-avis/hc-sc/2013/34783a-eng.php. Accessed February 13, 2014.

23. Greer FR, Krebs NF; American Academy of Pediatrics Committee on Nutrition. Optimizing bone health and calcium intakes of infants, children, and adolescents. Pediatrics. 2006;117:578-585.

When an athlete has decreased body fat as a result of low energy availability, she may have decreased adipokines, particularly leptin, which is believed to play a role in the ovulatory (normal) menstrual cycle. Abnormal eating also can suppress ghrelin, a short-term hormonal regulator of eating cycles/food intake and a long-term regulator of energy balance. Thus, short-term ghrelin dysregulation can self-perpetuate and have long-term consequences.

In anorexia nervosa, the intestinally derived anorexigen peptide YY is elevated,¹³ which may contribute to bone loss. Patients with anorexia nervosa also have androgen deficiency and elevated cortisol, both of which are factors in energy metabolism and maintenance of bone density.¹⁴

Menstrual dysfunction. Female athletes may experience amenorrhea, oligomenorrhea (menstrual periods with intervals >35 days), or subclinical menstrual dysfunction. Amenorrhea that occurs after menarche is considered secondary amenorrhea. Brancaccio et al¹⁵ found the incidence of secondary amenorrhea was significantly higher in high school athletes (30%) than in controls (15%). The researchers noted that “strenuous training alone has not been shown to alter menstrual cycles; it is necessary for dietary restriction to occur.”¹⁵

Altered BMD. Osteoporosis is characterized by compromised bone strength that increases the risk of fracture,¹⁶ and BMD is an aspect of bone strength. Osteoporosis may be caused by inadequate accumulation of optimal BMD during childhood and adolescence. A diagnosis of osteoporosis in patients ages 5 to 19 requires the presence of low bone mass and a clinically significant fracture history.¹⁷

BMD is assessed by dual-energy x-ray absorptiometry (DXA). DXA results are reported as a T-score, in which a patient’s bone density is compared with that of a healthy 30-year-old woman, or Z-score, which compares patients’ BMD with age- and sex-matched controls. The International Society of Clinical Densitometry recommends using Z-scores instead of T-scores when screening for osteoporosis in premenopausal women and in children.¹⁸

Z-scores are expressed as the number of standard deviations above or below the average value of the reference group. For every reduction by one standard deviation in BMD, the patient’s fracture risk doubles. The American College of Sports Medicine defines “low BMD” as a Z-score between -1 and -2.0 and osteoporosis as a Z-score ≤-2.0.¹ For both definitions, the patient must have at least one secondary clinical risk factor for fracture, such as low estrogen, history of stress fracture, or nutritional deficiencies.

Screening for the triad: What to ask, what to look for

Screen all adolescent female athletes at preparticipation physicals or whenever they present with any of the triad’s signs and symptoms. Look for risk factors such as calorie restriction practices, vegetarianism, a history of injuries, extended exercise periods, or increased training, particularly sport-specific training.¹ Also consider social, genetic, and psychiatric issues, such as abuse and family dysfunction.

Strenuous training alone is not enough to alter menstrual cycles; dietary restriction must occur.If you believe a patient is at risk, ask her about her exercise and eating habits, menstrual cycles, and fracture history (TABLE 1).¹⁹ During the physical exam, look for signs that suggest the triad, including lanugo, enlarged parotid glands, and bradycardia (TABLE 2).¹ Be sure to calculate the patient’s body mass index or body fat percentage.

Based on the history and physical findings, consider laboratory testing for a complete blood count with differential, ferritin, serum iron, B12, folate, comprehensive metabolic panel, thyroid function tests, erythrocyte sedimentation rate, and a urinalysis.²⁰ For an athlete in whom you highly suspect the triad, order urine electrolytes, salivary amylase, and stool guaiac tests, as well as an electrocardiogram.¹⁹

If your patient is amenorrheic, be aware that functional amenorrhea is a diagnosis of exclusion. Other diagnoses to consider include pregnancy, polycystic ovary syndrome, prolactinoma, anatomic defect, and ovarian failure. A pregnancy test, FSH and LH levels, prolactin, and thyroid-stimulating hormone testing should all be considered during evaluation for amenorrhea.

All patients with a history of stress fracture should undergo a DXA scan, whether or not they have comorbid amenorrhea, oligomenorrhea, or disordered eating.²⁰ In patients with amenorrhea, the DXA may need to be repeated in one year if menses does not resume.

For patients who screen positive for disordered eating, amenorrhea, or decreased BMD, the International Olympic Committee (IOC) guidelines are an excellent starting point for further evaluation.¹⁹ The IOC has “decision trees” for female athletes with disordered eating, amenorrhea, and osteoporosis that are available at http://www.olympic.org/Documents/Reports/EN/en_report_917.pdf.¹⁹

In addition to screening female athletes for the triad, consider addressing eating attitudes, menses, and fracture history in routine office physicals for all female patients. Also, be aware that triad symptoms are not limited to female athletes; male athletes, particularly those in sports that focus on leanness, physique, or weight classes (eg, wrestling) also are at risk for low energy availability, disordered eating, and low BMD.