Pathophysiology of bone loss in the female athlete
Irene Lambrinoudaki,
Dimitra Papadimitriou,
Irene Lambrinoudaki
Second Department of Obstetrics and Gynecology, University of Athens, Aretaieio Hospital, Athens Greece
Search for more papers by this authorDimitra Papadimitriou
Second Department of Obstetrics and Gynecology, University of Athens, Aretaieio Hospital, Athens Greece
Search for more papers by this authorIrene Lambrinoudaki,
Dimitra Papadimitriou,
Irene Lambrinoudaki
Second Department of Obstetrics and Gynecology, University of Athens, Aretaieio Hospital, Athens Greece
Search for more papers by this authorDimitra Papadimitriou
Second Department of Obstetrics and Gynecology, University of Athens, Aretaieio Hospital, Athens Greece
Search for more papers by this authorAddress for correspondence: Irene Lambrinoudaki, 4, Dorylaiou Street, Athens, GR-11521, Greece. [email protected]
Abstract
Low bone mass is frequent among female athletes. The “female athlete triad” is a term that describes the interaction among energy availability, menstrual function, and bone metabolism that may lead to amenorrhea and osteopenia or osteoporosis. The main pathophysiologic mechanisms that lead to low bone mass in female athletes are low energy availability and functional hypothalamic amenorrhea. Increased energy expenditure and/or decreased energy intake, as well as the presence of eating disorders, are associated with low bone mass. In addition, menstrual dysfunction is quite common, especially among athletes competing in sports favoring leanness, and also associates with low bone mass. Screening for bone loss in female athletes should take place in the presence of amenorrhea or body mass index <18 kg/m2. Management of low bone mass aims to restore normal energy availability and nutritional habits. Hormone replacement therapy has no effect in abnormally underweight patients unless normal eating behaviors are restored.
References
- 1 Whiting, S.J. et al . 2004. Factors that affect bone mineral accrual in the adolescent growth spurt. J. Nutr. 134: 696S–700S.
- 2 Nichols, J.F., M.J. Rauh, M.L. Lawson, et al . 2006. Prevalence of the female athlete triad syndrome among high school athletes. Arch. Pediatr. Adolesc. Med. 160: 137–142.
- 3 Ferretti, J.L., G.R. Cointry, R.F. Capozza & H.M. Frost. 2003. Bone mass, bone strength, muscle-bone interactions, osteopenias and osteoporoses. Mech. Ageing Dev. 124: 269–279.
- 4 Rautava, E., M. Lehtonen-Veromaa, H. Kautiainen, et al . 2007. The reduction of physical activityreflects on the bone mass among young females: a follow-up study of 142 adolescent girls. Osteoporos. Int. 18: 915–922.
- 5 Taaffe, D.R., T.L. Robinson, C.M. Snow & R. Marcus. 1997. High-impact exercise promotes bone gain in well-trained female athletes. J. Bone Miner. Res. 12: 255–260.
- 6 Egan, E., T. Reilly, M. Giacomoni, et al . 2006. Bone mineral density among female sports participants. Bone 38: 227–233.
- 7 Nichols, J.F., M.J. Rauh, M.T. Barrack & H.S. Barkai. 2007. Bone mineral density in female high school athletes: interactions of menstrual function and type of mechanical loading. Bone 41: 371–377.
- 8 Christo, K., R. Prabhakaran, B. Lamparello, et al . 2008. Bone metabolism in adolescent athletes with amenorrhea, athletes with eumenorrhea, and control subjects. Pediatrics 121: 1127–1136.
- 9 Nattiv, A., A.B. Loucks, M.M. Manore, et al . 2007. American college of sports medicine position stand. The female athlete triad. Med. Sci. Sports Exerc. 39: 1867–1882.
- 10 Rauch, F. 2007. Bone accrual in children: adding substance to surfaces. Pediatrics 119: S137–S140.
- 11 Willis, K.S., N.J. Peterson & D.E. Larson-Meyer. 2008. Should we be concerned about the vitamin D status of athletes? Int. J. Sport Nutr. Exerc. Metab. 18: 204–224.
- 12 Kass-Wolff, J.H. 2004. Calcium in women: healthy bones and much more. J. Obstet. Gynecol. Neonatal. Nurs. 33: 21–33.
- 13 Lovell, G. 2008. Vitamin D status of females in an elite gymnastics program. Clin. J. Sport Med. 18: 159–161.
- 14 Sundgot-Borgen, J. & M.K. Torstveit. 2004. Prevalence of eating disorders in elite athletes is higher than in the general population. Clin. J. Sport Med. 14: 25–32.
- 15 American Psychiatric Association Work Group on eating disorders. 2000. Practice guideline for the treatment of Patients with eating disorders (revision). Am. J. Psychiatry 157: 1–39.
- 16 Nielsen, S., S. Moller-Madsen, T. Isager, et al . 1998. Standardized mortality in eatingdisorders—a quantitative summary of previously published andnew evidence. J. Psychosom. Res. 44: 413–434.
- 17 Rauch, F. 2007. Bone accrual inchildren:adding substance to surfaces. Pediatrics 119: 137–140.
- 18 Cobb, K., L. Bachrach, G. Greendale, et al . 2003. Disordered eating, menstrual irregularity, and bone mineraldensity in female runners. Med. Sci. Sports Exerc. 35: 711–719.
- 19 Ihle, R. & A.B. Loucks. 2004. Dose-response relationships betweenenergy availability and bone turnover in young exercisingwomen. J. Bone Miner. Res. 19: 1231–1240.
- 20 Torstveit, M.K. & J. Sundgot-Borgen. 2005. The female athlete triad exists in both elite athletes and controls. Med. Sci. Sports Exerc. 37: 1449–1459.
- 21 De Souza, M.J., S.L. West, S.A. Jamal, et al . 2008. The presence of both an energy deficiency and estrogen deficiency exacerbate alterations of bone metabolism in exercising women. Bone 43: 140–148.
- 22 Riggs, B.L., S. Khosla & L.J. Melton 3rd. 2002. Sex steroids and the construction and conservation of the adult skeleton. Endocr. Rev. 23: 279–302.
- 23 Torstveit, M.K. & J. Sundgot-Borgen. 2005. Participation in leanness sports but not training volume is associated with menstrual dysfunction: a national survey of 1276 elite athletes and controls. Br. J. Sports Med. 39: 141–147.
- 24 Nichols, J.F., M.J. Rauh, M.T. Barrack, et al . 2007. Disordered eating and menstrual irregularity in high school athletes in lean-build and nonlean-build sports. Int. J. Sport Nutr. Exerc. Metab. 17: 364–377.
- 25 Welt, C.K., J.L. Chan, J. Bullen et al . 2004. Recombinant human leptin in women with hypothalamicamenorrhea. N. Engl. J. Med. 351: 987–997.
- 26 Kluge, M., P. Schussler, M. Uhr, et al . 2007. Ghrelinsuppresses secretion of luteinizing hormone in humans. J. Clin. Endocrinol. Metab. 92: 3202–3205.
- 27 De Souza, M.J., H.J. Leidy, E. O’Donnell, et al . 2004. Fasting ghrelin levels in physically active women: relationshipwith menstrual disturbances and metabolic hormones. J. Clin. Endocrinol. Metab. 89: 3536–3542.
- 28 Raastad, T., T. Bjoro & J. Hallen. 2000. Hormonal responses to high-andmoderate- intensity strength exercise. Eur. J. Appl. Physiol. 82: 121–128.
- 29 Laughlin, G. & S. Yen. 1996. Nutritional and endocrine-metabolic aberrations in amenorrheic athletes. J. Clin. Endocrinol. Metab. 81: 4301–4309.
- 30 Misra, M. 2008. Bone density in the adolescent athlete. Endocr. Metab. Disord. 9: 139–144.
- 31 Warren, M.P., J. Brooks-Gunn, R.P. Fox, et al . 2002. Osteopenia in exercise associated amenorrhea using ballet dancers as a model: alongitudinal study. J. Clin. Endocrinol. Metab. 87: 3162–3168.
- 32 Nattiv, A., J.C. Puffer, J. Carper, et al . 2000. Stress fracture risk factors, incidence and distribution: a 3-year prospective study in collegiate runners. Med. Sci. Sports Exerc. 32: S347.
- 33 Torstveit, M.K. & J. Sundgot-Borgen. 2005. The female athlete triad: are elite athletes at increased risk? Med. Sci. Sports Exerc. 37: 184–193.
- 34 Nichols, D.L. & C.F. Sanborn. 1998. Female athlete and bone. Nutr. Sport Exerc. 205–215.
- 35 Khan, A.A., L. Bachrach, J.P. Brown, et al . 2004. Standards and guidelines for performing central dual-energy x-ray absorptiometryin premenopausal women, men, and children. J. Clin. Densitom. 7: 51–64.
- 36 Viapiana, O., D. Gatti, R. Dalle Grave, et al . 2007. Marked increases in bone mineral density and biochemical markers of bone turnover in patients with anorexia nervosa gaining weight. Bone 40: 1073–1077.
- 37 Bolton, J.G., S. Patel, J.H. Lacey & S. White. 2005. A prospectivestudy of changes in bone turnover and bone density associatedwith regaining weight in women with anorexia nervosa. Osteoporos Int. 16: 1955–1962.
- 38 Compston, J.E., C. Mcconachie, C. Stott, et al . 2006. Changes in bonemineral 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. 17: 77–84.
- 39 Gordon, C.M., E. Grace, S.J. Emans, et al . 2002. Effects of oral dehydroepiandrosterone on bone density in young women with anorexia nervosa: a randomized trial. J. Clin. Endocrinol. Metab. 87: 4935–4941.
- 40 Liu, S.L. & C.M. Lebrun. 2006. Effect of oral contraceptives and hormone replacement therapy on bone mineral density in premenopausal and perimenopausal women: a systematic review. Br. J. Sports Med. 40: 11–24.
