Bone Health in Highly Trained Female Athletes:

A review of the current state of knowledge.


Highly trained female athletes are often at peak cardiovascular fitness but face important threats to their skeletal health. Women who train intensively may produce abnormally low levels of estrogen, which may lead to weakened bones. Low bone strength, or "osteopenia", is a risk factor for stress fractures (1,2,3). Young adults with osteopenia are also more likely to develop osteoporosis later in life (4).

Exercise, estrogen-deficiency, and menstrual irregularity.

Regular vigorous exercise is associated with decreased estrogen levels in the blood (5,6,7). In one study (6), healthy women who began training for a marathon reduced their estrogen levels by over 50%. Low estrogen levels result in menstrual irregularity in a large proportion of intensively training athletes. Irregularities can include a late onset of menstrual periods, infrequent or absent periods, or more subtle abnormalities, such as shortened luteal phase and anovulatory cycles. We recently surveyed competitive collegiate cross country runners and found that 56% missed several menstrual periods a year or had no periods at all. The cause of estrogen-deficiency and menstrual irregularity in athletes is not known with certainty, but risk factors include earlier onset of training, more intense training, psychological stress, nutritional inadequacy, low body weight, low body fat mass, and changes in body composition (8).

Estrogen and bone

Estrogen is essential for maintaining bone health in women. Events that result in rapid declines in a woman's estrogen level, such as menopause and ovariectomy (the removal of the ovaries), also result in rapid losses in her bone mass and bone strength. These losses can be prevented by estrogen treatment (9,10,11). Young women who develop hormonal conditions that cause estrogen deficiency, such as hyperprolactinemia, gonadal failure, and premature ovarian failure, also stop menstruating and lose bone (12-15). The extent of the bone loss in these women is directly proportional to the length of time that they have been without a period (15). Various estrogen replacement therapies have been shown to increase bone in these women (16-18).

Diet and bone

It is likely that poor nutrition and disordered eating adds to the risk of bone health problems in female athletes. Low body weight and a lean physique are desirable attributes in many sports, such as gymnastics, dancing, figure skating, and running. Athletes striving to excel in these sports may develop disordered eating patterns that contribute to both their menstrual irregularities and to the weakened state of their bones. Proper nutrition is essential for normal menstruation and for healthy bone; non-athletic women who are malnourished, such as women with anorexia nervosa, will develop amenorrhea (the absence of a menstrual period), osteopenia, and even osteoporosis (19,20,21). The combination of disordered eating, amenorrhea, and osteoporosis has been termed the "female athlete triad" (22).

Exercise-associated menstrual irregularity and bone

Because exercise is normally beneficial to bone, it has been hypothesized that women athletes may escape bone loss even if they develop menstrual irregularities. However, studies show that this is not the case for most sports. Nineteen studies have been conducted in which the bone strength (measured as bone density) of normally menstruating women was compared to the bone strength of athletes with irregular or absent periods ("amenorrheic" or "oligomenorrheic" athletes). Fifteen of these studies showed that bone density was significantly lower in amenorrheic and/or oligomenorrheic athletes (23-37). Three of the four remaining studies (38-41) showed a trend towards lower bone density in amenorrheic/oligomenorrheic athletes that was not statistically significant (38-40).

Women in late adolescence and early adulthood should still be building bone. Studies that measure athletes at a single time point cannot tell us if osteopenic athletes simply halt this building process or if they also break down existing bone. However, three studies have been conducted in which amenorrheic/oligomenorrheic athletes were measured yearly (42-44). These studies found that amenorrheic athletes in their late teens and early twenties not only fail to gain, but actually begin to lose bone.

The magnitude of bone loss is serious. Amenorrheic/oligomenorrheic athletes have 8-31% lower bone density than normally-menstruating athletes, and 3-24% lower bone density than non-exercising, normally-menstruating controls (23-37). Alarmingly, many of these women have extremely low bone mass; some have bone densities comparable to women in their 70's and 80's (32,36).

Most studies have considered athletes with infrequent or absent periods (oligomenorrhea or amenorrhea) and have not evaluated athletes with more subtle menstrual disturbances. However, one study found that runners who menstruate monthly but who have anovulatory cycles and/or shortened luteal phase also lose bone (45). This study is of particular interest because it demonstrates that highly training females who appear to be menstruating normally may still be at risk for osteopenia; asymptomatic hormonal changes and menstrual disturbances may be sufficient to cause bone loss.

Several studies show that the lower an athlete's estrogen level falls and the longer that her menstrual irregularity persists, the greater the deficits in her bone (26,27,34,36). These observations suggest a direct relationship between a low estrogen state and bone loss. In theory, then, the establishment of normal estrogen levels should prevent and even reverse bone loss. Oral contraceptives (birth control pills) provide estrogen and regulate the menstrual cycle; thus, it has been hypothesized that oral contraceptives can be used to strengthen the bones of women athletes. However, this hypothesis has never been formally tested.

Stress fractures and menstrual irregularity

Stress fractures plague young female athletes. In our recent survey of competitive collegiate cross country runners, 44% had experienced at least one stress fracture and 21% had suffered multiple stress fractures. Stress fractures may be related to estrogen deficiency and menstrual irregularity. Several studies report an association between current menstrual irregularity and stress fracture incidence among female athletes (5,23,25,46,47). Two studies (2,48) also found that a history of menstrual irregularity is a risk factor for stress fractures. These studies found that stress fracture risk was 2-4 times greater for amenorrheic/oligomenorrheic athletes than for normally-menstruating athletes.

Oral contraceptive use and stress fractures

Oral contraceptives may be protective against stress fractures. Four retrospective studies found that female athletes who took oral contraceptives had suffered 2-4 times fewer stress fractures than non-users (1,5,47,48). These studies suggest that oral contraceptive use reduces stress fracture incidence. However, these studies cannot establish a cause and effect relationship. For example, the women who chose to take oral contraceptives may have had greater bone mass before they started taking oral contraceptives. A randomized trial is urgently needed to establish if oral contraceptives can prevent bone problems in female athletes.

Reversibility of bone loss

Few studies have evaluated long-term outcomes for athletes with menstrual irregularities and low bone density. Three studies that followed amenorrheic athletes over time found that some recovery of bone mass can occur (42-44); athletes who gained weight, decreased training, and resumed menses (concomitant with increased estrogen levels) had bone density gains of 3-9% over the first year. However, formerly amenorrheic athletes still had significantly lower bone density compared to controls, suggesting that bone health may be permanently compromised if intervention is initiated too late. The longest study to follow previously amenorrheic/oligomenorrheic athletes lasted eight years (42). Despite the return of regular menstrual periods for several years, the bone density of formerly amenorrheic/oligomenorrheic athletes remained 15% less than the bone density of athletes who had never been amenorrheic. This suggests that some bone loss may be irreversible and that
early intervention is crucial.


amenorrhea - The absence of a menstrual period, or less than 4 periods per year.

anovulatory cycle - A disturbance of the menstrual cycle in which ovulation (the release of an egg from the ovary to the fallopian tube) does not occur.

bone density - A measure of bone strength.

eumenorrhea - Having a normal number of menstrual periods per year (10 -13).

oligomenorrhea - Infrequent menstruation, 4 -9 periods per year.

osteopenia - Having abnormally low bone mineral density for one's age.

ovariectomy - Surgical removal of the ovaries.

randomized trial - A type of study in which subjects are randomly assigned to either a treatment or control group and then are monitored over time as to their progress. This type of study can be used to establish causality between a treatment and an effect.

shortened luteal phase - A type of menstrual irregularity in which the luteal phase of a woman's menstrual cycle lasts for an abnormally short amount of time.


1. Myburgh KH, Hutchins J, Fataar AB, Hough SF, Noakes TD. Low bone density is an etiologic factor for stress fractures in athletes. Annals Int Med 1990; 113:754-759.

2. Bennell K, Malcolm SA, Thomas SA, Reid SJ, Brunker PD, Ebeling PR, Wark JD. Risk factors for stress fractures in track and field athletes: a twelve-month prospective study. Am J Sports Med 1996; 24:810-818.

3. Pouilles JM, Bernard J, Tremollieres F, Louvet JP, Ribot C. Femoral bone density in young male adults with stress fractures. Bone 1989; 10:105-108.

4. Johnston CC and Longcope C. Premenopausal bone loss-- a risk factor for osteoporosis. N Engl J Med 1990; 323:1271-1272.

5. Lloyd T, Triantafyllou SJ, Baker ER, Houts PS, Whiteside JA, Kalenak A, Stumpf PG. Women athletes with menstrual irregularity have increased muscoloskeletal injuries. Med Sci Sports Exerc 1986; 18: 374-379.

6. Boyden TW, Pamenter RW, Stanforth P, Rotkis T, Wilmore JH. Sex steroids and endurance running in women. Fertil Steril 1983; 39:629-632.

7. Russell JB, Mitchell D, Musey PL, Collins DC. The relationship of exercise to anovulatory cycles in female athletes: hormonal and physical characteristics. Obstet Gynecol 1984; 63:452.

8. Souza MJ and Metzger DA. Reproductive dysfunction in amenorrheic athletes and anorexic patients: a review. Med Sci Sports Exerc 1991; 23:995-1007.

9. Ettinger B, Genant HK, Cann CE. Long-term estrogen replacement therapy prevents bone loss and fractures. Ann Intern Med 1985; 102: 319-324.

10.Aitken JM, Hart DM, Lindsay R. Estrogen replacement therapy for prevention of osteoporosis after oophorectomy. Br Med J 1973; 3:515-518.

11. Felson DT, Zhang Y, Hannan MT, Kiel DP, Wison PWF, Anderson JJ. The effect of postmenopausal estrogen therapy on bone density in elderly women. N Engl J Med 1993; 329:1141-1146.

12. Klibanski A, Neer RM, Beitins IZ. Decreased bone density in hyperprolactinemic women. N Engl J Med 1980; 303:1511-1514.

13. Cann CE, Genant HK, Ettinger B. Spinal mineral loss in oophorectomized women: determination by quantitative computed tomography. JAMA 1980; 24:2056.

14. Klibanski A, Biller BMK, Rosenthal D, Schoenfeld DA, Saxe V. Effects of prolactin and estrogen deficiency in amenorrheic bone loss. J Clin Endrocrinol Metab 1988; 67:124-130.

15. Davies MC, Hall ML, Jacobs HS. Bone mineral loss in young women with amenorrhea. BMJ 1990; 301:790-793.

16. Klibanski A and Greenspan SL. Increase in bone mass after treatment of hyperprolactinemia amenorrhea. N Engl J Med 1986; 315:542-546.

17. Haennggi W, Casez JP, Birkhauser MH, Lippuner K, Jaegar P. Bone mineral density in young women with long-standing amenorrhea: limited effect of hormone replacement therapy with ethinylestradiol and desogestrel. Osteoporosis Int 1994: 4:99-103.

18. Gulekli B, Davies MC, Jacobs HS. Effect of treatment on established osteoporosis in young women with amenorrhea. Clin Endrocrinol 1994; 41:275-281.

19. Bachrach, LK. Osteopenia in childhood and adolescence. Osteoporosis. Eds R Marcus, J Kelsey, D Feldmen. San Diego: Academic Press, 1996, 785-800.

20. Rigotti NA, Nussbaum SR, Herzog DB, Neer RM. Osteoporosis in women with anorexia nervosa. N Engl J Med 1984; 11:1601-6.

21. Biller BMK, Saxe V, Herzog DB, Rosenthal D, Holzman S, Kilbanski A. Mechanisms of osteoporosis in adult and adolescent women with anorexia nervosa. J Clin Endrocrinol Metab 1989; 68:548-554.

22. Nativ A, Agostini R, Drinkwater B, Yeager KK. The female athlete triad. Clinics in Sports Med 1994; 13:405-418.

23. Lindberg JS, Fears WB, Hunt MM, Powell MR, Boll D, Wade CE. Exercise-induced amenorrhea and bone density. Annals of Int Med 1984; 101:647-648.

24. Drinkwater BL, Nilson K, Chesnut CH, Bremner WJ, Shainholtz S, Southworth MB. Bone mineral content of amenorrheic and eumenorrheic athletes. N Engl J Med 1984; 311:277-281.

25. Marcus R, Cann C, Madvig P, Minkoff J, Goddard M, Bayer M, Martin M, Gaudia L, Haskell W, Genant H. Menstrual function and bone mass in elite women distance runners. Annals Int Med 1985; 102:158-163.

26. Nelson ME, Fischer EC, Castos PD, Meredith CN, Turskoy RN, Evans WJ. Diet and bone status in amenorrheic runners. Am J Clin Nutr; 43:910-916.

27.Fischer EC, Nelson ME, Frontera WR, Turskoy RN, Evans WJ. Bone mineral content and levels of gonadotropins and estrogens in amenorrheic running women. J Clin Endrocrinol Metab 1986; 62:1232-1236.

28. Lloyd T, Myers C, Buchanan JR, Demers LM. Collegiate women athletes with irregular menses during adolescence have decreased bone density. Obstet Gynecol 1988; 72:639-642.

29. Wolman RL, Clark P, McNally E, Harris M, Reeve J. Menstrual state and exercise as determinants of spinal trabecular bone density in female athletes. BMJ 1990; 301:516-518.

30. Drinkwater BL, Bruemner B, Chesnut CH. Menstrual history as a determinant of current bone density in young athletes. JAMA 1990; 263:545-548.

31. Warren MP, Brooks-Gunn J, Fox RP, Lancelot C, Newman D, Hamilton WG. Lack of bone accretion and amenorrhea: evidence for relative osteopenia in weight-bearing bones. J Clin Endrocrinol Metab 1991; 72:847-853.

32. Myerson M, Gutin B, Warren MP, Wang J, Lichman S, Pierson RN. Total body bone density in amenorrheic runners. Obstet Gynecol 1992; 79:973-978.

33. Snead DB, Stubbs CC, Weltman JY, Evans WS, Veldhuis JD, Rogol AD, Teates DC, Welman A. Dietary patterns, eating behaviors, and bone mineral density in women runners. Am J Clin Nutr 1992; 56:705-711.

34. Myburgh KH, Bachrach LK, Lewis B, Kent K, Marcus R. Low bone mineral density at axial and appendicular sites in amenorrheic athletes. Med Sci Sports Exerc 1993; 25:1197-1202.

35. 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 Endrocrinol Metab 1994; 78:449-454.

36. Rencken ML, Chesnut CH, Drinkwater BL. Bone density at multiple skeletal sites in amenorrheic athletes. JAMA 1996; 276:238-240.

37. Micklesfield LK, Lambert EV, Fataar AB, Noakes TD, Myburgh KH. Bone mineral density in mature, premenopausal ultramarathon runners. Med Sci Sports Exerc 1995; 27: 688-696.

38. Linnell SL, Stager JM, Blue PW, Oyster N, Robertshaw D. Bone mineral content and menstrual regularity in female runners. Med Sci Sports Exerc 1984; 16:343-348.

39. Lloyd T, Buchanan JR, Blitzer S, Waldman CJ, Myers K, Ford BG. Interrelationships of diet, athletic activity, menstrual status, and bone density in collegiate women. Am J Clin Nutr 1987; 46:681-684.

40. Robinson TL, Snow-harter C, Taaffe DR, Shaw DG, Marcus R. Gymnasts exhibit higher bone mass than runners despite similar prevalence of amenorrhea and oligomenorrhea. J Bone Miner Res 1995; 10:26-35.

41. Okano H, Mizunuma H, Soda M, Matsui H, Aoki I, Honjo S, Ibuki H. Effects of exercise and amenorrhea on bone mineral density in teenage runners. Endocrine J 1995; 42:271-276.

42. Keen Adand Drinkwater BL. Irreversible loss in former amenorrheic athletes. Osteoporosis Int 1997; 7:311-315.

43. Lindberg JS, Powell MR, Hunt MM, Ducey DE, Wade CE. Increased vertebral bone mineral in response to reduced exercise in amenorrheic runners. West J Med 1987; 146:39-42.

44. Jonnavithula S, Warren MP, Fox RP, Lazaro MI. Bone density is compromised in amenorrheic women despite return of menses: a 2-year study. Obstet Gynecol 1993; 81:669-74.

45. Prior JC, Vigna YM, Schechter MT, Burgess AE. Spinal bone loss and ovulatory disturbances. N Engl J Med 1990; 323:1221-1227. Int J Sports Med 1987; 8:221-226.

46. Friedel KE, Nuovo JA, Patience TH, Dettori JR. Factors associated with stress fracture in young army women: indications for further research. Mil Med 1992; 157:334-338.

47. Barrow GW and Subrata S. Menstrual irregularity and stress fractures in collegiate female distance runners. Am J Sports Med 1988; 16:209-215.

48. Carbon R, Sambrook PN, Deakin V, Fricker P, Eisman JA, Kelly P, Maguire K, Yeates MG. Bone density of elite female athletes with stress fractures. Med J Aust 1990; 153:373-376.