Skip to main content
PMC home page
British Journal of Sports Medicine logoLink to British Journal of Sports Medicine
. 2002 Feb;36(1):10–13. doi: 10.1136/bjsm.36.1.10

New criteria for female athlete triad syndrome?

K Khan 1, T Liu-Ambrose 1, M Sran 1, M Ashe 1, M Donaldson 1, J Wark 1, A Nattiv 1
PMCID: PMC1724456  PMID: 11867483

Full Text

The Full Text of this article is available as a PDF (112.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bachrach L. K., Guido D., Katzman D., Litt I. F., Marcus R. Decreased bone density in adolescent girls with anorexia nervosa. Pediatrics. 1990 Sep;86(3):440–447. [PubMed] [Google Scholar]
  2. Bennell K. L., Malcolm S. A., Wark J. D., Brukner P. D. Skeletal effects of menstrual disturbances in athletes. Scand J Med Sci Sports. 1997 Oct;7(5):261–273. doi: 10.1111/j.1600-0838.1997.tb00151.x. [DOI] [PubMed] [Google Scholar]
  3. Booth F. W., Gordon S. E., Carlson C. J., Hamilton M. T. Waging war on modern chronic diseases: primary prevention through exercise biology. J Appl Physiol (1985) 2000 Feb;88(2):774–787. doi: 10.1152/jappl.2000.88.2.774. [DOI] [PubMed] [Google Scholar]
  4. Brotman A. W., Stern T. A. Osteoporosis and pathologic fractures in anorexia nervosa. Am J Psychiatry. 1985 Apr;142(4):495–496. doi: 10.1176/ajp.142.4.495. [DOI] [PubMed] [Google Scholar]
  5. Cann C. E., Martin M. C., Genant H. K., Jaffe R. B. Decreased spinal mineral content in amenorrheic women. JAMA. 1984 Feb 3;251(5):626–629. [PubMed] [Google Scholar]
  6. Cantu Robert C. Posttraumatic Retrograde and Anterograde Amnesia: Pathophysiology and Implications in Grading and Safe Return to Play. J Athl Train. 2001 Sep;36(3):244–248. [PMC free article] [PubMed] [Google Scholar]
  7. Carmichael K. A., Carmichael D. H. Bone metabolism and osteopenia in eating disorders. Medicine (Baltimore) 1995 Sep;74(5):254–267. doi: 10.1097/00005792-199509000-00003. [DOI] [PubMed] [Google Scholar]
  8. Donaldson M. G., Khan K. M., McKay H. A., Wark J. D. Be careful with the term "bone loss". CMAJ. 2001 Aug 7;165(3):269–270. [PMC free article] [PubMed] [Google Scholar]
  9. Drinkwater B. L., Nilson K., Chesnut C. H., 3rd, Bremner W. J., Shainholtz S., Southworth M. B. Bone mineral content of amenorrheic and eumenorrheic athletes. N Engl J Med. 1984 Aug 2;311(5):277–281. doi: 10.1056/NEJM198408023110501. [DOI] [PubMed] [Google Scholar]
  10. Dugowson C. E., Drinkwater B. L., Clark J. M. Nontraumatic femur fracture in an oligomenorrheic athlete. Med Sci Sports Exerc. 1991 Dec;23(12):1323–1325. [PubMed] [Google Scholar]
  11. Dupuis F., Johnston K. M., Lavoie M., Lepore F., Lassonde M. Concussions in athletes produce brain dysfunction as revealed by event-related potentials. Neuroreport. 2000 Dec 18;11(18):4087–4092. doi: 10.1097/00001756-200012180-00035. [DOI] [PubMed] [Google Scholar]
  12. Finch C. F., McIntosh A. S., McCrory P. What do under 15 year old schoolboy rugby union players think about protective headgear? Br J Sports Med. 2001 Apr;35(2):89–94. doi: 10.1136/bjsm.35.2.89. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Grindel S. H., Lovell M. R., Collins M. W. The assessment of sport-related concussion: the evidence behind neuropsychological testing and management. Clin J Sport Med. 2001 Jul;11(3):134–143. doi: 10.1097/00042752-200107000-00003. [DOI] [PubMed] [Google Scholar]
  14. Grinspoon S., Herzog D., Klibanski A. Mechanisms and treatment options for bone loss in anorexia nervosa. Psychopharmacol Bull. 1997;33(3):399–404. [PubMed] [Google Scholar]
  15. Grinspoon S., Thomas E., Pitts S., Gross E., Mickley D., Miller K., Herzog D., Klibanski A. Prevalence and predictive factors for regional osteopenia in women with anorexia nervosa. Ann Intern Med. 2000 Nov 21;133(10):790–794. doi: 10.7326/0003-4819-133-10-200011210-00011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Guidelines for assessment and management of sport-related concussion. Canadian Academy of Sport Medicine Concussion Committee. Clin J Sport Med. 2000 Jul;10(3):209–211. doi: 10.1097/00042752-200007000-00012. [DOI] [PubMed] [Google Scholar]
  17. Hilton L. K., Loucks A. B. Low energy availability, not exercise stress, suppresses the diurnal rhythm of leptin in healthy young women. Am J Physiol Endocrinol Metab. 2000 Jan;278(1):E43–E49. doi: 10.1152/ajpendo.2000.278.1.E43. [DOI] [PubMed] [Google Scholar]
  18. Johnston K. M., Ptito A., Chankowsky J., Chen J. K. New frontiers in diagnostic imaging in concussive head injury. Clin J Sport Med. 2001 Jul;11(3):166–175. doi: 10.1097/00042752-200107000-00007. [DOI] [PubMed] [Google Scholar]
  19. Jordan B. D., Relkin N. R., Ravdin L. D., Jacobs A. R., Bennett A., Gandy S. Apolipoprotein E epsilon4 associated with chronic traumatic brain injury in boxing. JAMA. 1997 Jul 9;278(2):136–140. [PubMed] [Google Scholar]
  20. Kanis J. A., Melton L. J., 3rd, Christiansen C., Johnston C. C., Khaltaev N. The diagnosis of osteoporosis. J Bone Miner Res. 1994 Aug;9(8):1137–1141. doi: 10.1002/jbmr.5650090802. [DOI] [PubMed] [Google Scholar]
  21. Kelly James P. Loss of Consciousness: Pathophysiology and Implications in Grading and Safe Return to Play. J Athl Train. 2001 Sep;36(3):249–252. [PMC free article] [PubMed] [Google Scholar]
  22. Kors E. E., Terwindt G. M., Vermeulen F. L., Fitzsimons R. B., Jardine P. E., Heywood P., Love S., van den Maagdenberg A. M., Haan J., Frants R. R. Delayed cerebral edema and fatal coma after minor head trauma: role of the CACNA1A calcium channel subunit gene and relationship with familial hemiplegic migraine. Ann Neurol. 2001 Jun;49(6):753–760. doi: 10.1002/ana.1031. [DOI] [PubMed] [Google Scholar]
  23. Lauder T. D., Williams M. V., Campbell C. S., Davis G., Sherman R., Pulos E. The female athlete triad: prevalence in military women. Mil Med. 1999 Sep;164(9):630–635. [PubMed] [Google Scholar]
  24. Leininger B. E., Gramling S. E., Farrell A. D., Kreutzer J. S., Peck E. A., 3rd Neuropsychological deficits in symptomatic minor head injury patients after concussion and mild concussion. J Neurol Neurosurg Psychiatry. 1990 Apr;53(4):293–296. doi: 10.1136/jnnp.53.4.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Loucks A. B., Heath E. M. Dietary restriction reduces luteinizing hormone (LH) pulse frequency during waking hours and increases LH pulse amplitude during sleep in young menstruating women. J Clin Endocrinol Metab. 1994 Apr;78(4):910–915. doi: 10.1210/jcem.78.4.8157720. [DOI] [PubMed] [Google Scholar]
  26. Loucks A. B., Horvath S. M. Exercise-induced stress responses of amenorrheic and eumenorrheic runners. J Clin Endocrinol Metab. 1984 Dec;59(6):1109–1120. doi: 10.1210/jcem-59-6-1109. [DOI] [PubMed] [Google Scholar]
  27. Loucks A. B., Horvath S. M., Freedson P. S. Menstrual status and validation of body fat prediction in athletes. Hum Biol. 1984 May;56(2):383–392. [PubMed] [Google Scholar]
  28. Loucks A. B., Laughlin G. A., Mortola J. F., Girton L., Nelson J. C., Yen S. S. Hypothalamic-pituitary-thyroidal function in eumenorrheic and amenorrheic athletes. J Clin Endocrinol Metab. 1992 Aug;75(2):514–518. doi: 10.1210/jcem.75.2.1639953. [DOI] [PubMed] [Google Scholar]
  29. Loucks A. B., Mortola J. F., Girton L., Yen S. S. Alterations in the hypothalamic-pituitary-ovarian and the hypothalamic-pituitary-adrenal axes in athletic women. J Clin Endocrinol Metab. 1989 Feb;68(2):402–411. doi: 10.1210/jcem-68-2-402. [DOI] [PubMed] [Google Scholar]
  30. Loucks A. B., Vaitukaitis J., Cameron J. L., Rogol A. D., Skrinar G., Warren M. P., Kendrick J., Limacher M. C. The reproductive system and exercise in women. Med Sci Sports Exerc. 1992 Jun;24(6 Suppl):S288–S293. [PubMed] [Google Scholar]
  31. Loucks A. B., Verdun M., Heath E. M. Low energy availability, not stress of exercise, alters LH pulsatility in exercising women. J Appl Physiol (1985) 1998 Jan;84(1):37–46. doi: 10.1152/jappl.1998.84.1.37. [DOI] [PubMed] [Google Scholar]
  32. Loucks A. B., Verdun M. Slow restoration of LH pulsatility by refeeding in energetically disrupted women. Am J Physiol. 1998 Oct;275(4 Pt 2):R1218–R1226. doi: 10.1152/ajpregu.1998.275.4.R1218. [DOI] [PubMed] [Google Scholar]
  33. Lovell M. R., Collins M. W. Neuropsychological assessment of the college football player. J Head Trauma Rehabil. 1998 Apr;13(2):9–26. doi: 10.1097/00001199-199804000-00004. [DOI] [PubMed] [Google Scholar]
  34. Lovell M. R., Iverson G. L., Collins M. W., McKeag D., Maroon J. C. Does loss of consciousness predict neuropsychological decrements after concussion? Clin J Sport Med. 1999 Oct;9(4):193–198. doi: 10.1097/00042752-199910000-00002. [DOI] [PubMed] [Google Scholar]
  35. Lucas A. R., Beard C. M., O'Fallon W. M., Kurland L. T. 50-year trends in the incidence of anorexia nervosa in Rochester, Minn.: a population-based study. Am J Psychiatry. 1991 Jul;148(7):917–922. doi: 10.1176/ajp.148.7.917. [DOI] [PubMed] [Google Scholar]
  36. Maddocks D. L., Dicker G. D., Saling M. M. The assessment of orientation following concussion in athletes. Clin J Sport Med. 1995;5(1):32–35. doi: 10.1097/00042752-199501000-00006. [DOI] [PubMed] [Google Scholar]
  37. McCrea M., Kelly J. P., Kluge J., Ackley B., Randolph C. Standardized assessment of concussion in football players. Neurology. 1997 Mar;48(3):586–588. doi: 10.1212/wnl.48.3.586. [DOI] [PubMed] [Google Scholar]
  38. McCrea M., Kelly J. P., Randolph C., Kluge J., Bartolic E., Finn G., Baxter B. Standardized assessment of concussion (SAC): on-site mental status evaluation of the athlete. J Head Trauma Rehabil. 1998 Apr;13(2):27–35. doi: 10.1097/00001199-199804000-00005. [DOI] [PubMed] [Google Scholar]
  39. McCrory P. R., Ariens T., Berkovic S. F. The nature and duration of acute concussive symptoms in Australian football. Clin J Sport Med. 2000 Oct;10(4):235–238. doi: 10.1097/00042752-200010000-00002. [DOI] [PubMed] [Google Scholar]
  40. McCrory P. R., Berkovic S. F. Second impact syndrome. Neurology. 1998 Mar;50(3):677–683. doi: 10.1212/wnl.50.3.677. [DOI] [PubMed] [Google Scholar]
  41. McCrory P. Do mouthguards prevent concussion? Br J Sports Med. 2001 Apr;35(2):81–82. doi: 10.1136/bjsm.35.2.81. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. McCrory P., Johnston K. M., Mohtadi N. G., Meeuwisse W. Evidence-based review of sport-related concussion: basic science. Clin J Sport Med. 2001 Jul;11(3):160–165. doi: 10.1097/00042752-200107000-00006. [DOI] [PubMed] [Google Scholar]
  43. McIntosh A. S., McCrory P. Impact energy attenuation performance of football headgear. Br J Sports Med. 2000 Oct;34(5):337–341. doi: 10.1136/bjsm.34.5.337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Micklesfield L. K., Lambert E. V., Fataar A. B., Noakes T. D., Myburgh K. H. Bone mineral density in mature, premenopausal ultramarathon runners. Med Sci Sports Exerc. 1995 May;27(5):688–696. [PubMed] [Google Scholar]
  45. Myburgh K. H., Bachrach L. K., Lewis B., Kent K., Marcus R. Low bone mineral density at axial and appendicular sites in amenorrheic athletes. Med Sci Sports Exerc. 1993 Nov;25(11):1197–1202. [PubMed] [Google Scholar]
  46. Nattiv A., Agostini R., Drinkwater B., Yeager K. K. The female athlete triad. The inter-relatedness of disordered eating, amenorrhea, and osteoporosis. Clin Sports Med. 1994 Apr;13(2):405–418. [PubMed] [Google Scholar]
  47. Nelson M. E., Fisher E. C., Catsos P. D., Meredith C. N., Turksoy R. N., Evans W. J. Diet and bone status in amenorrheic runners. Am J Clin Nutr. 1986 Jun;43(6):910–916. doi: 10.1093/ajcn/43.6.910. [DOI] [PubMed] [Google Scholar]
  48. Otis C. L., Drinkwater B., Johnson M., Loucks A., Wilmore J. American College of Sports Medicine position stand. The Female Athlete Triad. Med Sci Sports Exerc. 1997 May;29(5):i–ix. doi: 10.1097/00005768-199705000-00037. [DOI] [PubMed] [Google Scholar]
  49. Pettersson U., Stålnacke B., Ahlénius G., Henriksson-Larsén K., Lorentzon R. Low bone mass density at multiple skeletal sites, including the appendicular skeleton in amenorrheic runners. Calcif Tissue Int. 1999 Feb;64(2):117–125. doi: 10.1007/s002239900589. [DOI] [PubMed] [Google Scholar]
  50. Rutherford O. M. Spine and total body bone mineral density in amenorrheic endurance athletes. J Appl Physiol (1985) 1993 Jun;74(6):2904–2908. doi: 10.1152/jappl.1993.74.6.2904. [DOI] [PubMed] [Google Scholar]
  51. Seeman E., Karlsson M. K., Duan Y. On exposure to anorexia nervosa, the temporal variation in axial and appendicular skeletal development predisposes to site-specific deficits in bone size and density: a cross-sectional study. J Bone Miner Res. 2000 Nov;15(11):2259–2265. doi: 10.1359/jbmr.2000.15.11.2259. [DOI] [PubMed] [Google Scholar]
  52. Seeman E., Szmukler G. I., Formica C., Tsalamandris C., Mestrovic R. Osteoporosis in anorexia nervosa: the influence of peak bone density, bone loss, oral contraceptive use, and exercise. J Bone Miner Res. 1992 Dec;7(12):1467–1474. doi: 10.1002/jbmr.5650071215. [DOI] [PubMed] [Google Scholar]
  53. Soyka L. A., Grinspoon S., Levitsky L. L., Herzog D. B., Klibanski A. The effects of anorexia nervosa on bone metabolism in female adolescents. J Clin Endocrinol Metab. 1999 Dec;84(12):4489–4496. doi: 10.1210/jcem.84.12.6207. [DOI] [PubMed] [Google Scholar]
  54. Teasdale G. M., Nicoll J. A., Murray G., Fiddes M. Association of apolipoprotein E polymorphism with outcome after head injury. Lancet. 1997 Oct 11;350(9084):1069–1071. doi: 10.1016/S0140-6736(97)04318-3. [DOI] [PubMed] [Google Scholar]
  55. Tomten S. E., Falch J. A., Birkeland K. I., Hemmersbach P., Høstmark A. T. Bone mineral density and menstrual irregularities. A comparative study on cortical and trabecular bone structures in runners with alleged normal eating behavior. Int J Sports Med. 1998 Feb;19(2):92–97. doi: 10.1055/s-2007-971888. [DOI] [PubMed] [Google Scholar]
  56. Warren M. P., Brooks-Gunn J., Fox R. P., Lancelot C., Newman D., Hamilton W. G. Lack of bone accretion and amenorrhea: evidence for a relative osteopenia in weight-bearing bones. J Clin Endocrinol Metab. 1991 Apr;72(4):847–853. doi: 10.1210/jcem-72-4-847. [DOI] [PubMed] [Google Scholar]
  57. Yeager K. K., Agostini R., Nattiv A., Drinkwater B. The female athlete triad: disordered eating, amenorrhea, osteoporosis. Med Sci Sports Exerc. 1993 Jul;25(7):775–777. doi: 10.1249/00005768-199307000-00003. [DOI] [PubMed] [Google Scholar]
  58. Young N., Formica C., Szmukler G., Seeman E. Bone density at weight-bearing and nonweight-bearing sites in ballet dancers: the effects of exercise, hypogonadism, and body weight. J Clin Endocrinol Metab. 1994 Feb;78(2):449–454. doi: 10.1210/jcem.78.2.8106634. [DOI] [PubMed] [Google Scholar]

Articles from British Journal of Sports Medicine are provided here courtesy of BMJ Publishing Group

RESOURCES