This study was designed to determine whether the hypoestrogenic status of 14 amenorrheic athletes was associated with a decrease in regional bone mass relative to that of 14 of their eumenorrheic peers. The two groups of athletes were matched for age, height, weight, sport, and training regimens. Bone mass was measured by dual-photon and single-photon absorptiometry at the lumbar vertebrae (L1 to L4) and at two sites on the radius. Vertebral mineral density was significantly lower in the amenorrheic group (mean, 1.12 g per square centimeter) than in the eumenorrheic group (mean, 1.30 g per square centimeter). There was no significant difference at either radial site. Radioimmunoassay confirmed a lower mean estradiol concentration (amenorrheic group, 38.58 pg per milliliter; eumenorrheic group, 106.99 pg per milliliter) and progesterone peak (amenorrheic group, 1.25 ng per milliliter; eumenorrheic group, 12.75 ng per milliliter) in the amenorrheic women, in four venous samples drawn at seven-day intervals. A three-day dietary history showed no significant differences in nutritional intake, including calcium with and without supplements. The two groups were similar in percentage of body fat, age at menarche, years of athletic participation, and frequency and duration of training but differed in number of miles run per week (amenorrheic group, 41.8 miles [67.3 km]; eumenorrheic group, 24.9 miles [40.1 km]). We conclude that the amenorrhea that is observed in female athletes may be accompanied by a decrease in mineral density of the lumbar vertebrae.
This article has been cited by other articles:
Sardinha, L. B., Baptista, F., Ekelund, U.
(2008). Objectively Measured Physical Activity and Bone Strength in 9-Year-Old Boys and Girls. Pediatrics
122: e728-e736
[Abstract][Full Text]
Micklesfield, L K, Hugo, J, Johnson, C, Noakes, T D, Lambert, E V
(2007). Factors associated with menstrual dysfunction and self-reported bone stress injuries in female runners in the ultra- and half-marathons of the Two Oceans. Br. J. Sports. Med.
41: 679-683
[Abstract][Full Text]
Loucks, A B
(2007). Refutation of "the myth of the female athlete triad". Br. J. Sports. Med.
41: 55-57
[Full Text]
Grewal, J., Sowers, M. R., Randolph, J. F. Jr., Harlow, S. D., Lin, X.
(2006). Low Bone Mineral Density in the Early Menopausal Transition: Role for Ovulatory Function. J. Clin. Endocrinol. Metab.
91: 3780-3785
[Abstract][Full Text]
Rickenlund, A., Carlstrom, K., Ekblom, B., Brismar, T. B., von Schoultz, B., Hirschberg, A. L.
(2004). Effects of Oral Contraceptives on Body Composition and Physical Performance in Female Athletes. J. Clin. Endocrinol. Metab.
89: 4364-4370
[Abstract][Full Text]
Markou, K. B., Mylonas, P., Theodoropoulou, A., Kontogiannis, A., Leglise, M., Vagenakis, A. G., Georgopoulos, N. A.
(2004). The Influence of Intensive Physical Exercise on Bone Acquisition in Adolescent Elite Female and Male Artistic Gymnasts. J. Clin. Endocrinol. Metab.
89: 4383-4387
[Abstract][Full Text]
De Souza, M. J., Williams, N. I.
(2004). Physiological aspects and clinical sequelae of energy deficiency and hypoestrogenism in exercising women. Hum Reprod Update
10: 433-448
[Abstract][Full Text]
Sherman, R. T., Thompson, R. A.
(2004). The Female Athlete Triad. The Journal of School Nursing
20: 197-202
[Abstract]
Yildirim, M, Gursoy, R, Varoglu, E, Oztasyonar, Y, Cogalgil, S
(2004). 99mTc-MDP bone SPECT in evaluation of the knee in asymptomatic soccer players. Br. J. Sports. Med.
38: 15-18
[Abstract][Full Text]
Klentrou, P, Plyley, M
(2003). Onset of puberty, menstrual frequency, and body fat in elite rhythmic gymnasts compared with normal controls. Br. J. Sports. Med.
37: 490-494
[Abstract][Full Text]
Braam, L. A. J. L. M., Knapen, M. H. J., Geusens, P., Brouns, F., Vermeer, C.
(2003). Factors Affecting Bone Loss in Female Endurance Athletes: A Two-Year Follow-Up Study. Am J Sports Med
31: 889-895
[Abstract][Full Text]
Burrows, M, Nevill, A M, Bird, S, Simpson, D
(2003). Physiological factors associated with low bone mineral density in female endurance runners. Br. J. Sports. Med.
37: 67-71
[Abstract][Full Text]
Casazza, G. A., Suh, S.-H., Miller, B. F., Navazio, F. M., Brooks, G. A.
(2002). Effects of oral contraceptives on peak exercise capacity. J. Appl. Physiol.
93: 1698-1702
[Abstract][Full Text]
Arfai, K., Pitukcheewanont, P. D., Goran, M. I., Tavare, C. J., Heller, L., Gilsanz, V.
(2002). Bone, Muscle, and Fat: Sex-related Differences in Prepubertal Children. Radiology
224: 338-344
[Abstract][Full Text]
Warren, M. P., Brooks-Gunn, J., Fox, R. P., Holderness, C. C., Hyle, E. P., Hamilton, W. G.
(2002). Osteopenia in Exercise-Associated Amenorrhea Using Ballet Dancers as a Model: A Longitudinal Study. J. Clin. Endocrinol. Metab.
87: 3162-3168
[Abstract][Full Text]
Riggs, B. L., Khosla, S., Melton, L. J. III
(2002). Sex Steroids and the Construction and Conservation of the Adult Skeleton. Endocr. Rev.
23: 279-302
[Abstract][Full Text]
Kaufman, B. A., Warren, M. P., Dominguez, J. E., Wang, J., Heymsfield, S. B., Pierson, R. N.
(2002). Bone Density and Amenorrhea in Ballet Dancers Are Related to a Decreased Resting Metabolic Rate and Lower Leptin Levels. J. Clin. Endocrinol. Metab.
87: 2777-2783
[Abstract][Full Text]
Khan, K M, Liu-Ambrose, T, Sran, M M, Ashe, M C, Donaldson, M G, Wark, J D, Nattiv, A
(2002). New criteria for female athlete triad syndrome?. Br. J. Sports. Med.
36: 10-13
[Full Text]
Harm, D. L., Jennings, R. T., Meck, J. V., Powell, M. R., Putcha, L., Sams, C. P., Schneider, S. M., Shackelford, L. C., Smith, S. M., Whitson, P. A.
(2001). Genome and Hormones: Gender Differences in Physiology: Invited Review: Gender issues related to spaceflight: a NASA perspective. J. Appl. Physiol.
91: 2374-2383
[Abstract][Full Text]
Williams, N. I., Helmreich, D. L., Parfitt, D. B., Caston-Balderrama, A., Cameron, J. L.
(2001). Evidence for a Causal Role of Low Energy Availability in the Induction of Menstrual Cycle Disturbances during Strenuous Exercise Training. J. Clin. Endocrinol. Metab.
86: 5184-5193
[Abstract][Full Text]
Ramsay, R, Wolman, R
(2001). Are synchronised swimmers at risk of amenorrhoea?. Br. J. Sports. Med.
35: 242-244
[Abstract][Full Text]
Williams, N. I., Caston-Balderrama, A. L., Helmreich, D. L., Parfitt, D. B., Nosbisch, C., Cameron, J. L.
(2001). Longitudinal Changes in Reproductive Hormones and Menstrual Cyclicity in Cynomolgus Monkeys during Strenuous Exercise Training: Abrupt Transition to Exercise-Induced Amenorrhea. Endocrinology
142: 2381-2389
[Abstract][Full Text]
Newcomb, P. A., Trentham-Dietz, A., Egan, K. M., Titus-Ernstoff, L., Baron, J. A., Storer, B. E., Willett, W. C., Stampfer, M. J.
(2001). Fracture History and Risk of Breast and Endometrial Cancer. Am J Epidemiol
153: 1071-1078
[Abstract][Full Text]
Abbot, A. E., Hannafin, J. A.
(2001). Stress Fracture of the Clavicle in a Female Lightweight Rower: A Case Report and Review of the Literature. Am J Sports Med
29: 370-372
[Full Text]
McLean, J. A, Barr, S. I, Prior, J. C
(2001). Cognitive dietary restraint is associated with higher urinary cortisol excretion in healthy premenopausal women. Am. J. Clin. Nutr.
73: 7-12
[Abstract][Full Text]
Compston, J. E.
(2001). Sex Steroids and Bone. Physiol. Rev.
81: 419-447
[Abstract][Full Text]
Cromer, B., Harel, Z.
(2000). Adolescents: At Increased Risk for Osteoporosis?. CLIN PEDIATR
39: 565-574
[Abstract]
Miller, K. K., Klibanski, A.
(1999). Amenorrheic Bone Loss. J. Clin. Endocrinol. Metab.
84: 1775-1783
[Full Text]
De Souza, M. J., Miller, B. E., Luciano, A. A., Stier, S., Ulreich, S., Weigert, J.
(1998). Ovulation and Spine Bone Mineral Density--Author's Responsef. J. Clin. Endocrinol. Metab.
83: 3758-3758
[Full Text]
Stacey, E., Korkia, P., Hukkanen, M. V. J., Polak, J. M., Rutherford, O. M.
(1998). Decreased Nitric Oxide Levels and Bone Turnover in Amenorrheic Athletes with Spinal Osteopenia. J. Clin. Endocrinol. Metab.
83: 3056-3061
[Abstract][Full Text]
Sundgot-Borgen, J., Bahr, R., Falch, J. A., Schneider, L. S.
(1998). Normal Bone Mass in Bulimic Women. J. Clin. Endocrinol. Metab.
83: 3144-3149
[Abstract][Full Text]
Hergenroeder, A. C.
(1998). Prevention of Sports Injuries. Pediatrics
101: 1057-1063
[Full Text]
De Cree, C., Ball, P., Seidlitz, B., Van Kranenburg, G., Geurten, P., Keizer, H. A.
(1997). Effects of a training program on resting plasma 2-hydroxycatecholestrogen levels in eumenorrheic women. J. Appl. Physiol.
83: 1551-1556
[Abstract][Full Text]
Devoe, D. J., Miller, W. L., Conte, F. A., Kaplan, S. L., Grumbach, M. M., Rosenthal, S. M., Wilson, C. B., Gitelman, S. E.
(1997). Long-Term Outcome in Children and Adolescents after Transsphenoidal Surgery for Cushing's Disease. J. Clin. Endocrinol. Metab.
82: 3196-3202
[Abstract][Full Text]
De Souza, M. J., Miller, B. E., Sequenzia, L. C., Luciano, A. A., Ulreich, S., Stier, S., Prestwood, K., Lasley, B. L.
(1997). Bone Health Is Not Affected by Luteal Phase Abnormalities and Decreased Ovarian Progesterone Production in Female Runners. J. Clin. Endocrinol. Metab.
82: 2867-2876
[Abstract][Full Text]
Tofler, I. R., Stryer, B. K., Micheli, L. J., Herman, L. R.
(1996). Physical and Emotional Problems of Elite Female Gymnasts. NEJM
335: 281-283
[Full Text]
Lonzer, M. D., Imrie, R., Rogers, D., Worley, D., Licata, A., Secic, M.
(1996). Effects of Heredity, Age, Weight, Puberty, Activity, and Calcium Intake on Bone Mineral Density in Children. CLIN PEDIATR
35: 185-189
[Abstract]
McGivney, S.
(1993). Estrogen and Postmenopausal Osteoporosis. ANN INTERN MED
118: 155-156
[Full Text]
Kadel, N. J., Teitz, C. C., Kronmal, R. A.
(1992). Stress fractures in ballet dancers. Am J Sports Med
20: 445-449
[Abstract]
Carruth, B. R., Goldberg, D. L.
(1990). Nutritional Issues of Adolescents: Athletics and the Body Image Mania. The Journal of Early Adolescence
10: 122-140
[Abstract]
Barrow, G. W., Saha, S.
(1988). Menstrual irregularity and stress fractures in collegiate female distance runners. Am J Sports Med
16: 209-216
[Abstract]
Cook, S. D., Harding, A. F., Thomas, K. A., Morgan, E. L., Schnurpfeil, K. M., Haddad, R. J. JR
(1987). Trabecular bone density and menstrual function in women runners. Am J Sports Med
15: 503-507
[Abstract]
