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.
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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
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Miller, K. K., Klibanski, A.
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84: 1775-1783
[Full Text]
De Souza, M. J., Miller, B. E., Luciano, A. A., Stier, S., Ulreich, S., Weigert, J.
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83: 3758-3758
[Full Text]
Stacey, E., Korkia, P., Hukkanen, M. V. J., Polak, J. M., Rutherford, O. M.
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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]
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(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.
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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.
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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]
Rencken, M. L., Chesnut, C. H. III, Drinkwater, B. L.
(1996). Bone Density at Multiple Skeletal Sites in Amenorrheic Athletes. JAMA
276: 238-240
[Abstract]
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]
White, C. M., Hergenroeder, A. C., Klish, W. J.
(1992). Bone Mineral Density in 15- to 21-Year-Old Eumenorrheic and Amenorrheic Subjects. Arch Pediatr Adolesc Med
146: 31-35
[Abstract]
Rigotti, N. A., Neer, R. M., Skates, S. J., Herzog, D. B., Nussbaum, S. R.
(1991). The Clinical Course of Osteoporosis in Anorexia Nervosa: A Longitudinal Study of Cortical Bone Mass. JAMA
265: 1133-1138
[Abstract]
Myburgh, K. H., Hutchins, J., Fataar, A. B., Hough, S. F., Noakes, T. D.
(1990). Low Bone Density Is an Etiologic Factor for Stress Fractures in Athletes. ANN INTERN MED
113: 754-759
[Abstract]
Naessen, T., Persson, I., Adami, H.-O., Bergstrom, R., Bergkvist, L.
(1990). Hormone Replacement Therapy and the Risk for First Hip Fracture: A Prospective, Population-based Cohort Study. ANN INTERN MED
113: 95-103
[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]
Shangold, M., Rebar, R. W., Wentz, A. C., Schiff, I.
(1990). Evaluation and Management of Menstrual Dysfunction in Athletes. JAMA
263: 1665-1669
[Abstract]
Drinkwater, B. L., Bruemner, B., Chesnut, C. H. III
(1990). Menstrual History as a Determinant of Current Bone Density in Young Athletes. JAMA
263: 545-548
[Abstract]
Michel, B. A., Bloch, D. A., Fries, J. F.
(1989). Weight-Bearing Exercise, Overexercise, and Lumbar Bone Density Over Age 50 Years. Arch Intern Med
149: 2325-2329
[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]
DING, J.-H., SHECKTER, C. B., DRINKWATER, B. L., SOULES, M. R., BREMNER, W. J.
(1988). High Serum Cortisol Levels in Exercise-Associated Amenorrhea. ANN INTERN MED
108: 530-534
[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]
Heymsfield, S. B., Rolandelli, R., Casper, K., Settle, R. G., Koruda, M.
(1987). Application of Electromagnetic and Sound Waves in Nutritional Assessment. JPEN J Parenter Enteral Nutr
11: 64S-69S
[Abstract]
FINKELSTEIN, J. S., KLIBANSKI, A., NEER, R. M., GREENSPAN, S. L., ROSENTHAL, D. I., CROWLEY, W. F. Jr
(1987). Osteoporosis in Men with Idiopathic Hypogonadotropic Hypogonadism. ANN INTERN MED
106: 354-361
[Abstract]
Drinkwater, B. L., Nilson, K., Ott, S., Chesnut, C. H. III
(1986). Bone Mineral Density After Resumption of Menses in Amenorrheic Athletes. JAMA
256: 380-382
[Abstract]
Riggs, B. L., Eastell, R.
(1986). Exercise, Hypogonadism, and Osteopenia. JAMA
256: 392-393
[Abstract]
GREENSPAN, S. L., NEER, R. M., RIDGWAY, E. C., KLIBANSKI, A.
(1986). Osteoporosis in Men with Hyperprolactinemic Hypogonadism. ANN INTERN MED
104: 777-782
[Abstract]
Lane, N. E., Bloch, D. A., Jones, H. H., Marshall, W. H. Jr, Wood, P. D., Fries, J. F.
(1986). Long-Distance Running, Bone Density, and Osteoarthritis. JAMA
255: 1147-1151
[Abstract]
MARCUS, R., CANN, C., MADVIG, P., MINKOFF, J., GODDARD, M., BAYER, M., MARTIN, M., GAUDIANI, L., HASKELL, W., GENANT, H.
(1985). Menstrual Function and Bone Mass in Elite Women Distance Runners: Endocrine and Metabolic Features. ANN INTERN MED
102: 158-163
[Abstract]
HEATH, H. III
(1985). Athletic Women, Amenorrhea, and Skeletal Integrity. ANN INTERN MED
102: 258-260
[Abstract]