Skip Navigation
Skip to contents

KMJ : Kosin Medical Journal



Page Path
HOME > Kosin Med J > Volume 29(1); 2014 > Article
Review Article
Management of Low Bone Mass in Female Athletes
Hoon Choi
Kosin Medical Journal 2014;29(1):1-10.
Published online: December 17, 2014

Department of Obstetrics and Gynecology, College of Medicine, Inje University, Sanggyepaik Hospital, Seoul, Korea

Corresponding Author: Hoon Choi, Department of Obstetrics and Gynecology, Inje University, School of Medicine Inje University Sanggyepaik Hospital, 1342, Dongil-ro, Nowon-gu, Seoul, 139-707, Korea TEL: +82-2-950-1058 FAX: +82-00-00-00 E-mail:
• Received: March 14, 2014   • Revised: March 14, 2014   • Accepted: March 17, 2014

Copyright © 2014 Kosin University School of Medicine Proceedings

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

  • 8 Download
  • As female athletic participation has increased, the positive effects of exercise on health have become evident. However, with this growth in sports activity, a set of health problems unique to the female athlete has emerged. The female athlete triad and its components can occur in females of all ages in every sport. The Female Athlete Triad poses serious health risks, both short and long term, to the overall well-being of affected individuals. Sustained low energy availability can impair health, causing many medical complications within the skeletal, endocrine, cardiovascular, reproductive, and central nervous systems. With the surge of females participating in athletics within the past 10 to 15 years, it is both conceivable and likely that the prevalence of this syndrome will continue to grow. Therefore, it is imperative that appropriate screening and diagnostic measures are enacted by a multidisciplinary team of health care providers, counselors, teachers, and dieticians in order to provide the proper care to affected athletes. Initial awareness should take place within the educational confines of elementary and high schools. Screening for female athletes exhibiting risk factors for the triad should also take place at the time of sports physicals. If one component of the triad is identified, the clinician should take the time to effectively workup the other. Treatment for each component of the triad includes both pharmacological and nonpharmacological measures, with emphasis placed upon increased energy availability and overall improved nutritional health. Using this all-encompassing type of approach, sports medicine practitioners should feel empowered to continue to promote the lifelong well-being of female athletes in the years to come.
Fig. 1.
The female athlete triad.
Fig. 2.
Average bone mineral density among collegiate female athletes by sport.
Table 1.
Risk Factors and Warning Signs of the Female
Athlete Triad Athletes at risk for eating disorders
Restriction of dietary energy intake or vegetarianism
Psychosocial pressures to achieve thinness
Low self-esteem or poor family dynamics
Initiation of training at young age or increase in training
Participation in lean/aesthetic sports
Athletes at risk for menstrual dysfunction
Low body mass index
Participation in lean/aesthetic sports
Athletes at risk for stress fractures
Low bone mineral density or history of stress fractures
Menstrual disturbances
Delayed menarche
Dietary insufficiency
Errors in training
Warning signs
Decline in performance
Weight loss
Mood changes
Frequent illness or injury
Dissatisfaction with appearance
  • 1. Gibbs JC, Williams NI, De Souza MJ. Prevalence of individual and combined components of the female athlete triad. Med Sci Sports Exerc 2013;45:985–96.ArticlePubMed
  • 2. Otis CL, Drinkwater B, Johnson M, Loucks A, Wilmone J. American College of Sports Medicine position stand: the Female Athlete Triad. Med Sci Sports Exerc 1997;29:i–ix.
  • 3. Nichols DL, Sanborn CF, Essery EV. Bone density and young athletic women: an update. Sports Med 2007;37:1001–14.PubMed
  • 4. Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP. American College of Sports Medicine. American College of Sports Medicine position stand: the female athlete triad. Med Sci Sports Exerc 2007;39:1867–82.PubMed
  • 5. Lebrun CM. The Female Athlete Triad: what's a doctor to do? Curr Sports Med Rep 2007;6:397–404.ArticlePubMed
  • 6. Beals KA, Hill AK. The prevalence of disordered eating, menstrual dysfunction, and low bone mineral density among US collegiate athletes. Int J Sports Nutr Exerc Metab 2006;16:1–23.Article
  • 7. Hoch AZ, Pajewski NM, Moraski L, Carrera GF, Wilson CR, Hoffmann RG, et al. Prevalence of the Female Athlete Triad in high school athletes and sedentary students. Clin J Sports Med 2009;19:421–8.Article
  • 8. Nattiv A, Loucks AB, Manore MM, et al. Position Stand: the female athlete triad. Med Sci Sports Exerc 2007;39:1867–82.PubMed
  • 9. Manore MM. Nutritional needs of the female athlete. Clin J Sports Med 1999;18:549–63.Article
  • 10. Witkop CT, Warren MP. Understanding the spectrum of the Female Athlete Triad. Am Coll Obstet Gynecol 2010;116:1444–8.Article
  • 11. Sundgot-Borgen J. Risk and trigger factors for the development of eating disorders in female elite athletes. Med Sci Sports Exerc 1994;26:414–9.ArticlePubMed
  • 12. Boden BP, Osbahr DC. High-risk stress fractures: evaluation and treatment. J Am Acad Orthop Surg 2000;8:344–53.ArticlePubMed
  • 13. Kadel NJ, Teitz CC, Kronmal RA. Stress fractures in ballet dancers. Am J Sports Med 1992;20:445–9.ArticlePubMed
  • 14. Gibbs JC, Williams NI, Scheid JL, Toombs RJ, De Souza MJ. The association of a high drive for thinness with energy deficiency and severe menstrual disturbances: confirmation in a large population of exercising women. Int J Sport Nutr Exerc Metab 2011;21:280–90.ArticlePubMed
  • 15. Pritts SD, Susman J. Diagnosis of eating disorders in primary care. Am Fam Physician 2003;67:297–304.PubMed
  • 16. Sundgot-Borgen J. Risk and trigger factors for the development of eating disorders in female elite athletes. Med Sci Sports Exerc 1994;26:414–9.ArticlePubMed
  • 17. Byrne S, McLean N. Elite athletes: effects of the pressure to be thin. J Sci Med Sport 2002;5:80–94.ArticlePubMed
  • 18. Redman LM, Loucks AB. Menstrual disorders in athletes. Sports Med 2005;35:747–55.ArticlePubMed
  • 19. Kelsey JL, Bachrach LK, Procter-Gray E, Nieves J, Greendale GA, Sowers M, et al. Risk factors for stress fracture among young female cross-country runners. Med Sci Sports Exerc 2007;39:1457–63.ArticlePubMed
  • 20. Bolin D, Kemper A, Brolinson PG. Current concepts in the evaluation and management of stress fractures. Curr Sports Med Rep 2005;4:295–300.ArticlePubMed
  • 21. Bonci CM, Bonci LJ, Granger LR, Johnson CL, Malina RM, Milne LW, et al. National Athletic Trainers' Association position statement: preventing, detecting, and managing disordered eating in athletes. J Athl Train 2008;43:80–108.ArticlePubMedPMC
  • 22. Loucks AB, Nattiv A. Essay: the female athlete triad. Lancet 2005;366:S49–50.ArticlePubMed
  • 23. Martinsen M, Sundgot-Borgen J. Higher prevalence of eating disorders among adolescent elite athletes than controls. Med Sci Sports Exerc 2013;45:1188–97.ArticlePubMed
  • 24. Smolak L, Murnen SK, Ruble AE. Female athletes and eating problems: a metaanalysis. Int J Eat Disord 2000;27:371–80.ArticlePubMed
  • 25. 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.ArticlePubMed
  • 26. Beals KA, Meyer NL. Female Athlete Triad update. Clin Sports Med 2007;26:69–89.ArticlePubMed
  • 27. Baxter-Jones AD, Helms P, Baines-Preece J, Preece M. Menarche in intensively trained gymnasts, swimmers and tennis players. Ann Hum Biol 1994;21:407–15.ArticlePubMed
  • 28. De Souza MJ, Toombs RJ, Scheid JL O'Donnell E, Weat SL, Willams NI. High prevalence of subtle and severe menstrual disturbances in exercising women: confirmation using daily hormone measures. Hum Reprod 2010;25:491–503.ArticlePubMed
  • 29. Practice Committee of the American Society for Reproductive Medicine. Current evaluation of amenorrhea. Fertil Steril 2004;82:S33–9.ArticlePubMed
  • 30. Carlberg KA, Buckman MT, Peake GT, Riedesel ML. A survey of menstrual function in athletes. Eur J Appl Physiol 1983;51:211–22.Article
  • 31. Legro RS, Lin HM, Demers LM, Lloyd T. Rapid maturation of the reproductive axis during perimenarche independent of body composition. J Clin Endocrinol Metab 2000;85:1021–5.ArticlePubMed
  • 32. Di Cagno A, Marchetti M, Battaglia C, Giombini A, Calcagno G, Fiorilli G, et al. Is menstrual delay a serious problem for elite rhythmic gymnasts? J Sports Med Phys Fitness 2012;52:647–53.PubMed
  • 33. Beals KA, Manore MM. Disorders of the female athlete triad among collegiate athletes. Int J Sport Nutr Exerc Metab 2002;12:281–93.ArticlePubMed
  • 34. Chumlea WC, Schubert CM, Roche AF, Kulin HE, Lee PA, Himes JH, et al. Age at menarche and racial comparisons in US girls. Pediatrics 2003;111:110–3.ArticlePubMed
  • 35. 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 2006;160:137–42.ArticlePubMed
  • 36. Sanborn CF, Martin BJ, Wagner WW Jr. Is athletic amenorrhea specific to runners? Am J Obstet Gynecol 1982;143:859–61.ArticlePubMed
  • 37. Williams NI, Helmreich DL, Parfitt DB, Caston-Balderrama A, Cameron JL. Evidence for a causal role of low energy availability in the induction of menstrual cycle disturbances during strenuous exercise training. J Clin Endocrinol Metab 2001;86:5184–93.ArticlePubMed
  • 38. Loucks AB, Thuma JR. Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. J Clin Endocrinol Metab 2003;88:297–311.ArticlePubMed
  • 39. Misra M. Effects of hypogonadism on bone metabolism in female adolescents and young adults. Nat Rev Endocrinol 2012;8:395–404.ArticlePubMed
  • 40. De Souza MJ, Williams NI. Beyond hypoestrogenism in amenorrheic athletes: energy deficiency as a contributing factor for bone loss. Curr Sports Med Rep 2005;4:38–44.PubMed
  • 41. Shapses SA, Heymsfield SB, Ricci TA, et al. Voluntary weight reduction increases bone turnover and loss In Burckhardt P., Dawson-Hughes B, Heaney RB(eds) Nutritional Aspects of Osteoporosis. New York, NY: Springer-Verlag, 1998, pp..180–4.
  • 42. Grinspoon SK, Baum HB, Kim V, Coggins C, Klibanski A. Decreased bone formation and increased mineral dissolution during acute fasting in young women. J Clin Endocrinol Metab 1995;80:3628–33.ArticlePubMed
  • 43. Ihle R, Loucks AB. Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res 2004;19:1231–40.ArticlePubMed
  • 44. Andersen RE, Wadden TA, Herzog RJ. Changes in bone mineral content in obese dieting women. Metabolism 1997;46:857–61.ArticlePubMed
  • 45. Compston JE, Laskey MA, Croucher PI, Coxon A, Kreitzman S. Effect of diet-induced weight loss on total body bone mass. Clin Sci (Lond) 1992;82:429–32.ArticlePubMed
  • 46. Lloyd T., Myers C., Buchanan J.R., Demers LM. Collegiate women athletes with irregular menses during adolescence have decreased bone density. Obstet Gynecol 1988;72:639–42.PubMed
  • 47. Drinkwater BL, Bruemner B, Chesnut CH III. Menstrual history as a determinant of current bone density in young athletes. JAMA 1990;263:545–8.ArticlePubMed
  • 48. Nattiv A, Puffer JC, Casper J, Dorey F, Kabo JM, Hame S, et al. Stress fracture risk factors, incidence and distribution: a 3-year prospective study in collegiate runners. Med Sci Sports Exerc 2000;32:S347.
  • 49. Ackerman KE, Nazem T, Chapko D, Russell M, Mendes N, Taylor AP, et al. Bone microarchitecture is impaired in adolescent amenorrheic athletes compared with eumenorrheic athletes and nonathletic controls. J Clin Endocrinol Metab 2011;96:3123–33.ArticlePubMedPMC
  • 50. Bennell KL, Malcolm SA, Thomas SA, Reid SJ, Brukner PD, Ebeling PR, et al. Risk factors for stress fractures in track and field athletes: a twelve-month prospective study. Am J Sports Med 1996;24:810–8.ArticlePubMed
  • 51. Bailey DA, Martin AD, McKay HA, Whiting S. Mirwald R. Calcium accretion in girls and boys during puberty: a longitudinal analysis. J Bone Miner Res 2000;15:2245–50.ArticlePubMed
  • 52. Yurth EF. Female athlete triad. West J Med 1995;162:149–50.PubMedPMC
  • 53. Compston JE, McConachie C, Stott C, Hannon RA, Kaptoge S, Debiram I, et al. Changes in bone mineral density, body composition and biochemical markers of bone turnover during weight gain in adolescents with severe anorexia nervosa: a 1-year prospective study. Osteoporos Int 2006;17:77–84.ArticlePubMed
  • 54. Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP. American College of Sports Medicine. American College of Sports Medicine position stand. The female athlete triad. Med Sci Sports Exerc 2007;39:1867–82.PubMed
  • 55. Cobb KL, Bachrach LK, Greendale G, Marcus R, Neer RM, Nieves J, et al. Disordered eating, menstrual irregularity, and bone mineral density in female runners. Med Sci Sports Exerc 2002;35:711–9.Article
  • 56. Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP. American College of Sports Medicine.Bone mineral density in collegiate female athletes: comparisons among sports. J Athletic Train 2007;42:403–8.
  • 57. Torstveit MK, Sundgot-Borgen J. The female athlete triad: are elite athletes at increased risk? Med Sci Sports Exerc 2005;37:184–93.ArticlePubMed
  • 58. Mendelsohn FA, Warren MP. Anorexia, bulimia, and the female athlete triad: evaluation and management. J Clin Endocrinol Metab 2010;39:155–67.Article
  • 59. Deimel JF, Dunlap BJ. The female athlete triad. Clin Sports Med 2012;31:247–54.ArticlePubMed
  • 60. IOC Medical Commission Working Group Women in Sports. Position Stand on Female Athlete Triad 2005. INTER REF. Accessed July 29.2013.
  • 61. American Dietetic Association; Dietitians of Canada; American College of Sports Medicine. Rodriguez NR, Di Marco NM, Langley S. American College of Sports Medicine position stand. Nutrition and athletic performance. Med Sci Sports Exerc 2009;41:709–31.PubMed
  • 62. National Research Council, Subcommittee on the Tenth Edition of the RDAs. Recommended Dietary Allowances. 10th ed.Washington, DC: National Academy Press; 1989.
  • 63. Economos CD, Bortz SS, Nelson ME. Nutritional practices of elite athletes: practical recommendations. Sports Med 1993;16:381–99.PubMed

Figure & Data



    Citations to this article as recorded by  

      • PubReader PubReader
      • Cite
        export Copy
      • Download Citation
        Download Citation
        Download a citation file in RIS format that can be imported by all major citation management software, including EndNote, ProCite, RefWorks, and Reference Manager.

        • RIS — For EndNote, ProCite, RefWorks, and most other reference management software
        • BibTeX — For JabRef, BibDesk, and other BibTeX-specific software
        • Citation for the content below
        Management of Low Bone Mass in Female Athletes
        Kosin Med J. 2014;29(1):1-10.   Published online December 17, 2014
      • XML DownloadXML Download

      KMJ : Kosin Medical Journal