Sports Medicine

, Volume 37, Issue 11, pp 1001–1014 | Cite as

Bone Density and Young Athletic Women

An Update
  • David L. Nichols
  • Charlotte F. Sanborn
  • Eve V. Essery
Review Article Bone Density and Young Athletic Women

Abstract

High-school girls and collegiate women have tremendous opportunities to participate in athletic teams. Young girls are also playing in club and select teams at an early age and often, year-round. There are many benefits for participating in sport and physical activity on both the physical and mental health of girls and women. Decreased risk for heart disease and diabetes mellitus, along with improved self-esteem and body-image, were among the first reported benefits of regular physical activity. In addition, sport participation and physical activity is also associated with bone health. Athletes have a greater bone mineral density compared with non-active and physically active females. The increase in bone mass should reduce the risk of fragility fractures in later life. There appears to be a window of opportunity during the development of peak bone mass in which the bone is especially responsive to weight-bearing physical activity. Impact loading sports such as gymnastics, rugby or volleyball tend to produce a better overall osteogenic response than sports without impact loading such as cycling, rowing and swimming. Relatively little is known about the impact of retiring from athletics on bone density. It appears that former athletes continue to have a higher bone density than non-athletes; however, the rate of bone loss appears to be similar in the femoral neck. The positive impact of sports participation on bone mass can be tempered by nutritional and hormonal status. It is not known whether female athletes need additional calcium compared with the general female population. Due to the increased energy expenditure of exercise and/or the pressure to obtain an optimal training bodyweight, some female athletes may develop low energy availability or an eating disorder and subsequently amenorrhoea and a loss of bone mineral density. The three inter-related clinical disorders are referred to as the ‘female athlete triad’. This article presents a review of the relationship between sports training and bone health, specifically bone mineral density, in young athletic women.

References

  1. 1.
    DeHass D. 2003–2004 NCAA gender-equity report. Indianapolis (IN): The National Collegiate Athletic Association, 2006 [online]. Available from URL: (http://www.ncaa/org/library/research/gender_equity_study_report.pdf) [Accessed 2007 Aug 28]Google Scholar
  2. 2.
    Carpenter LJ, Acosta RV. Women in intercollegiate sport: a longitudinal, national study twenty seven year update 177-2004. Women’s Sports Foundation. Available from URL: (http://www.womensports/foundation/org/cgibin/iowa/issues/part/article.html) [Accessed 2007 Aug 28]
  3. 3.
    Women participation at the Games of the XXVIII Olympiad, Athens 2004, statistics [online]. Available from URL: (http://www.olympic/org/uk/organisation/missions/women/activities/women_uk.asp) [Accessed 2007 Aug 28]
  4. 4.
    Benefits of girls playing sports. Women’s Sports Foundation 1999 [online]. Available from URL: (http://www.womensportsfoundation.org) [Accessed 2007 Aug 28]
  5. 5.
    US Department of Health and Human Services. Physical activity fundamental to preventing disease. Office of the Assistant Secretary for Planning and Evaluation 1-19. 6-20-2002 [online]. Available from URL: (http://www.aspe/hhs/gov/health/reports/physicalactivity/physicalactivity.pdf) [Accessed 2007 Aug 28]
  6. 6.
    Blair SN, Brodney S. et al. Effects of physical inactivity and obesity on morbidity and mortality: current evidence and research issues. Med Sci Sports Exerc 1999; 31: S646–62PubMedCrossRefGoogle Scholar
  7. 7.
    Kohrt WM, Bloomfield SA, Little KD, et al. American College of Sports Medicine position stand: physical activity and bone health. Med Sci Sports Exerc 2004; 36: 1985–96PubMedCrossRefGoogle Scholar
  8. 8.
    Khan K, McKay HA, Kannus P, Physical activity and bone health. 1st ed. Champaign (IL): Human Kinetics, 2001Google Scholar
  9. 9.
    Campbell AJ, Robertson MC, Gardner MM, et al. Randomised controlled trial of a general practice programme of home based exercise to prevent falls in elderly women. BMJ 1997; 315: 1065–9PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Gregg EW, Cauley JA, Seeley DG, et al. Physical activity and osteoporotic fracture risk in older women: study of Osteoporotic Fractures Research Group. Ann Intern Med 1998; 129: 81–8PubMedCrossRefGoogle Scholar
  11. 11.
    Grisso JA, Capezuti E, Schwartz A. Falls as risk factors for fractures. In: Marcus R, Feldman D, Kelsey J, editors. Osteoporosis. San Diego (CA): Academic Press, 1996: 599–611Google Scholar
  12. 12.
    Riggs BL, Melton LJ. Involutional osteoporosis. N Engl J Med 1986; 311: 1676–86CrossRefGoogle Scholar
  13. 13.
    Nichols DL, Bonnick SL, Sanborn CF. Bone health and osteoporosis. Clin Sports Med 2000; 19: 233–49PubMedCrossRefGoogle Scholar
  14. 14.
    Johnston CCJ, Slemenda CW. Peak bone mass, bone loss and risk of fracture. Osteoporos Int 1994; 4 Suppl. 1: 43–5CrossRefGoogle Scholar
  15. 15.
    Kanis JA, Johnell O, Oden A, et al. Ten year probabilities of osteoporotic fractures according to BMD and diagnostic thresholds. Osteoporos Int 2001; 12: 989–95PubMedCrossRefGoogle Scholar
  16. 16.
    Nordstrom A, Karlsson C, Nyquist F, et al. Bone loss and fracture risk after reduced physical activity. J Bone Miner Res 2005; 20: 202–7PubMedCrossRefGoogle Scholar
  17. 17.
    Greene DA, Naughton GA. Adaptive skeletal responses to mechanical loading during adolescence. Sports Med 2006; 36: 723–32PubMedCrossRefGoogle Scholar
  18. 18.
    Nikander R, Sievanen H, Heinonen A, et al. Femoral neck structure in adult female athletes subjected to different loading modalities. J Bone Miner Res 2005; 20: 520–8PubMedCrossRefGoogle Scholar
  19. 19.
    Bass SL. The prepubertal years: a uniquely opportune stage of growth when the skeleton is most responsive to exercise? Sports Med 2000; 30: 73–8PubMedCrossRefGoogle Scholar
  20. 20.
    Kontulainen S, Kannus P, Haapasalo H, et al. Good maintenance of female tennis and squash players: a prospective 5-year follow-up study of young and old starters and controls. J Bone Miner Res 2001; 16: 195–201PubMedCrossRefGoogle Scholar
  21. 21.
    Borer KT. Physical activity in the prevention and amelioration of osteoporosis in women: interaction of mechanical, hormonal and dietary factors. Sports Med 2005; 35: 779–830PubMedCrossRefGoogle Scholar
  22. 22.
    Yeager KK, Agostini R, Nattiv A, et al. The female athlete triad: disordered eating, amenorrhea, osteoporosis. Med Sci Sports Exerc 1993; 25: 775–7PubMedCrossRefGoogle Scholar
  23. 23.
    Byrne S, McLean N. Eating disorders in athletes: a review of the literature. J Sci Med Sport 2001; 4: 145–59PubMedCrossRefGoogle Scholar
  24. 24.
    Byrne S, McLean N. Elite athletes: effects of the pressure to be thin. J Sci Med Sport 2002; 5: 80–94PubMedCrossRefGoogle Scholar
  25. 25.
    Sundgot-Borgen J, Torstveit MK. Prevalence of eating disorders in elite athletes is higher than in the general population. Clin J Sport Med 2004; 14: 25–32PubMedCrossRefGoogle Scholar
  26. 26.
    Sundgot-Borgen J. Eating disorders in female athletes. Sports Med 1994; 17: 176–88PubMedCrossRefGoogle Scholar
  27. 27.
    Otis CL, Drinkwater B, Johnson M, et al. American College of Sports Medicine position stand: the female athlete triad. Med Sci Sports Exerc 1997; 29: i–ixPubMedCrossRefGoogle Scholar
  28. 28.
    Nattiv N, Loucks A, Manore MM, et al. The female athlete triad position stand. Med Sci Sports Exerc 2007; 39 (10): 1867–82PubMedCrossRefGoogle Scholar
  29. 29.
    Pettersson U, Stalnacke B, Ahlenius G, et al. Low bone mass density at multiple skeletal sites, including the appendicular skeleton in amenorrheic runners. Calcif Tissue Int 1999; 64: 117–25PubMedCrossRefGoogle Scholar
  30. 30.
    Richelson LS, Wahner HW, Melton LJ, et al. Relative contributions of aging and estrogen deficiency to postmenopausal bone loss. N Engl J Med 1984; 311: 1273–5PubMedCrossRefGoogle Scholar
  31. 31.
    Snow-Harter CM. Bone health and prevention of osteoporosis in active and athletic women. Clin Sports Med 1994; 13: 389–404PubMedGoogle Scholar
  32. 32.
    McKay HA, Petit MA, Schutz RW, et al. Augmented trochanteric bone mineral density after modified physical education classes: a randomized school-based exercise intervention study in prepubescent and early pubescent children. J Pediatr 2000; 136: 156–62PubMedCrossRefGoogle Scholar
  33. 33.
    Fuchs RK, Bauer JJ, Snow CM. Jumping improves hip and lumbar spine bone mass in prepubescent children: a randomized controlled trial. J Bone Miner Res 2001; 16: 148–56PubMedCrossRefGoogle Scholar
  34. 34.
    Mackelvie KJ, Khan KM, Petit MA, et al. A school-based exercise intervention elicits substantial bone health benefits: a 2-year randomized controlled trial in girls. Pediatrics 2003; 112: e447PubMedCrossRefGoogle Scholar
  35. 35.
    Reid IR, Ames RW, Evans MC, et al. Effect of calcium supplementation on bone loss in postmenopausal women. N Engl J Med 1993; 328: 460–4PubMedCrossRefGoogle Scholar
  36. 36.
    Dawson-Hughes B, Dallai GE, Krall EA, et al. A controlled trial of the effect of calcium supplementation on bone density in postmenopausal women. N Engl J Med 1990; 323: 878–83PubMedCrossRefGoogle Scholar
  37. 37.
    Lloyd T, Andon MB, Rollings N, et al. Calcium supplementation and bone mineral density in adolescent girls. JAMA 1993; 270: 841–4PubMedCrossRefGoogle Scholar
  38. 38.
    Heaney RP. Calcium, dairy products and osteoporosis. J Am Coll Nutr 2000; 19: 83S–99SPubMedCrossRefGoogle Scholar
  39. 39.
    Iuliano-Burns S, Saxon L, Naughton G, et al. Regional specificity of exercise and calcium during skeletal growth in girls: a randomized controlled trial. J Bone Miner Res 2003; 18: 156–62PubMedCrossRefGoogle Scholar
  40. 40.
    Stear SJ, Prentice A, Jones SC, et al. Effect of a calcium and exercise intervention on the bone mineral status of 16–18-y-old adolescent girls. Am J Clin Nutr 2003; 77: 985–92PubMedGoogle Scholar
  41. 41.
    Zanker CL, Cooke CB. Energy balance, bone turnover, and skeletal health in physically active individuals. Med Sci Sports Exerc 2004; 36: 1372–81PubMedCrossRefGoogle Scholar
  42. 42.
    Ihle R, Loucks AB. Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res 2004; 19: 1231–40PubMedCrossRefGoogle Scholar
  43. 43.
    Recker RR, Davies M, Hinders SM, et al. Bone gain in young adult women. JAMA 1992; 268: 2403–8PubMedCrossRefGoogle Scholar
  44. 44.
    Haapasalo H, Kannus P, Sievanen H, et al. Development of mass, density, and estimated mechanical characteristics of bones in Caucasian females. J Bone Miner Res 1996; 11: 1751–60PubMedCrossRefGoogle Scholar
  45. 45.
    Rico H, Revilla M, Hernandez ER, et al. Sex differences in the acquisition of total bone mineral mass peak assessed through dual energy x-ray absorptiometry. Calcif Tissue Int 1992; 51: 251–4PubMedCrossRefGoogle Scholar
  46. 46.
    Rizzoli R, Bonjour JP. Determinants of peak bone mass and mechanisms of bone loss. Osteoporos Int 1999; 9 Suppl. 2: S17–23CrossRefGoogle Scholar
  47. 47.
    Khan K, McKay HA, Haapasalo H, et al. Does childhood and adolescence provide a unique opportunity for exercise to strengthen the skeleton? J Sci Med Sport 2000; 3: 150–64PubMedCrossRefGoogle Scholar
  48. 48.
    Wang MC, Crawford PB, Hudes M, et al. Diet in midpuberty and sedentary activity in prepuberty predict peak bone mass. Am J Clin Nutr 2003; 77: 495–503PubMedGoogle Scholar
  49. 49.
    McKay HA, Petit MA, Bailey DA, et al. Analysis of proximal femur DXA scans in growing children: comparisons of different protocols for cross-sectional 8-month and 7-year longitudinal data. J Bone Miner Res 2000; 15: 1181–8PubMedCrossRefGoogle Scholar
  50. 50.
    Hans D, Downs Jr RW, Duboeuf F, et al. Skeletal sites for osteoporosis diagnosis: the 2005 ISCD official positions. J Clin Densitom 2006; 9: 15–21PubMedCrossRefGoogle Scholar
  51. 51.
    Kanis JA. Diagnosis of osteoporosis and assessment of fracture risk. Lancet 2002; 359: 1929–36PubMedCrossRefGoogle Scholar
  52. 52.
    Leib ES, Lewiecki EM, Binkley N, et al. Official positions of the International Society for Clinical Densitometry. South Med J 2004; 97: 107–10PubMedCrossRefGoogle Scholar
  53. 53.
    International Society for Clinical Densitometry Writing Group for the ISCD Position Development Conference. Diagnosis of osteoporosis in men, premenopausal women, and children. J Clin Densitom 2004; 7: 17–26PubMedCrossRefGoogle Scholar
  54. 54.
    Lewiecki EM, Watts NB, McClung MR, et al. Official positions of the international society for clinical densitometry. J Clin Endocrinol Metab 2004; 89: 3651–5PubMedCrossRefGoogle Scholar
  55. 55.
    Leib ES. Treatment of low bone mass in premenopausal women: when may it be appropriate? Curr Osteoporos Rep 2005; 3: 13–8PubMedCrossRefGoogle Scholar
  56. 56.
    IOC Medical Commission Working Group Women in Sport. International Olympic Committee Position Stand on the female athlete triad 2006 [online]. Available from URL: (http://multimedia.olympic.org/pdf/en_report_917.pdf) [Accessed 2007 Aug 28]
  57. 57.
    Leslie WD, Adler RA, Hajj FG, et al. Application of the 1994 WHO classification to populations other than postmenopausal Caucasian women: the 2005 ISCD Official Positions. J Clin Densitom 2006; 9: 22–30PubMedCrossRefGoogle Scholar
  58. 58.
    Bouxsein ML. Bone quality: where do we go from here? Osteoporos Int 2003; 14 Suppl. 5: 118–27CrossRefGoogle Scholar
  59. 59.
    Bouxsein ML, Karasik D. Bone geometry and skeletal fragility. Curr Osteoporos Rep 2006; 4: 49–56PubMedCrossRefGoogle Scholar
  60. 60.
    Ammann P, Rizzoli R. Bone strength and its determinants. Osteoporos Int 2003; 14 Suppl. 3: S13–8CrossRefGoogle Scholar
  61. 61.
    Genant HK, Jiang Y. Advanced imaging assessment of bone quality. Ann N Y Acad Sci 2006; 1068: 410–28PubMedCrossRefGoogle Scholar
  62. 62.
    Bennell KL, Malcolm SA, Khan KM, et al. Bone mass and bone turnover in power athletes, endurance athletes, and controls: a 12-month longitudinal study. Bone 1997; 20: 477–84PubMedCrossRefGoogle Scholar
  63. 63.
    Fehling PC, Alekel L, Clasey J, et al. A comparison of bone mineral densities among female athletes in impact loading and active loading sports. Bone 1995; 17: 205–10PubMedCrossRefGoogle Scholar
  64. 64.
    Heinonen A, Oja P, Kannus P, et al. Bone mineral density of female athletes in different sports. Bone Miner 1993; 23: 1–14PubMedCrossRefGoogle Scholar
  65. 65.
    Meyer NL, Shaw JM, Manore MM, et al. Bone mineral density of olympic-level female winter sport athletes. Med Sci Sports Exerc 2004; 36: 1594–601PubMedCrossRefGoogle Scholar
  66. 66.
    Nichols DL, Sanborn CF, Bonnick SL, et al. The effects of gymnastics training on bone mineral density. Med Sci Sports Exerc 1994; 26: 1220–5PubMedCrossRefGoogle Scholar
  67. 67.
    Taaffe DR, Snow-Harter C, Connolly DA, et al. Differential effects of swimming versus weight-bearing activity on bone mineral status of eumenorrheic athletes. J Bone Miner Res 1995; 10: 586–93PubMedCrossRefGoogle Scholar
  68. 68.
    Beshgetoor D, Nichols JF, Rego I. Effect of training mode and calcium intake on bone mineral density in female master cyclist, runners, and non-athletes. Int J Sport Nutr Exerc Metab 2000; 10: 290–301PubMedCrossRefGoogle Scholar
  69. 69.
    Laing EM, Wilson AR, Modlesky CM, et al. Initial years of recreational artistic gymnastics training improves lumbar spine bone mineral accrual in 4 to 8-year-old females. J Bone Miner Res 2005; 20: 509–19PubMedCrossRefGoogle Scholar
  70. 70.
    Goto S, Shigeta H, Hyakutake S, et al. Comparison between menopause-related changes in bone mineral density of the lumbar spine and the proximal femur in Japanese female athletes: a long-term longitudinal study using dual-energy x-ray absorptiometry. Calcif Tissue Int 1996; 59: 461–5PubMedCrossRefGoogle Scholar
  71. 71.
    Morel J, Combe B, Francisco J, et al. Bone mineral density of 704 amateur sportsmen involved in different physical activities. Osteoporos Int 2001; 12: 152–7PubMedCrossRefGoogle Scholar
  72. 72.
    Nevill A, Holder R, Stewart A. Do sporting activities convey benefits to bone mass throughout the skeleton? J Sports Sci 2004; 22: 645–50PubMedCrossRefGoogle Scholar
  73. 73.
    Nichols DL, Sanborn CF, Bonnick SL, et al. Relationship of regional body composition to bone mineral density in college females. Med Sci Sports Exerc 1995; 27: 178–82PubMedCrossRefGoogle Scholar
  74. 74.
    Heinonen A, Sievanen H, Kannus P, et al. Site-specific skeletal response to long-term weight training seems to be attributable to principal loading modality: a pQCT study of female weight-lifters. Calcif Tissue Int 2002; 70: 469–74PubMedCrossRefGoogle Scholar
  75. 75.
    Bass S, Pearce G, Bradney M, et al. Exercise before puberty may confer residual benefits in bone density in adulthood: studies in active prepubertal and retired female gymnasts. J Bone Miner Res 1998; 13: 500–7PubMedCrossRefGoogle Scholar
  76. 76.
    Kirchner EM, Lewis RD, O’Connor PJ. Effect of past gymnastics participation on adult bone mass. J Appl Physiol 1996; 80: 226–32PubMedCrossRefGoogle Scholar
  77. 77.
    Kudlac J, Nichols DL, Sanborn CF, et al. Impact of detraining on bone loss in former collegiate female gymnasts. Calcif Tissue Int 2004; 75: 482–7PubMedCrossRefGoogle Scholar
  78. 78.
    Wallace BA, Cumming RG. Systematic review of randomized trials of the effect of exercise on bone mass in pre-and post-menopausal women. Calcif Tissue Int 2000; 67: 10–8PubMedCrossRefGoogle Scholar
  79. 79.
    Courteix D, Lespessailles E, Peres SL, et al. Effect of physical training on bone mineral density in prepubertal girls: a comparative study between impact-loading and non-impact-loading sports. Osteoporos Int 1998; 8: 152–8PubMedCrossRefGoogle Scholar
  80. 80.
    Creighton DL, Morgan AL, Boardley D, et al. Weight-bearing exercise and markers of bone turnover in female athletes. J Appl Physiol 2001; 90: 565–70PubMedGoogle Scholar
  81. 81.
    Duncan CS, Blimkie CJ, Cowell CT, et al. Bone mineral density in adolescent female athletes: relationship to exercise type and muscle strength. Med Sci Sports Exerc 2002; 34: 286–94PubMedCrossRefGoogle Scholar
  82. 82.
    Duppe H, Gardsell P, Johnell O, et al. Bone mineral density in female junior, senior and former football players. Osteoporos Int 1996; 6: 437–41PubMedCrossRefGoogle Scholar
  83. 83.
    Emslander HC, Sinaki M, Muhs JM, et al. Bone mass and muscle strength in female college athletes (runners and swimmers). Mayo Clin Proc 1998; 73: 1151–60PubMedCrossRefGoogle Scholar
  84. 84.
    Heinonen A, Sievanen H, Kyrolainen H, Mineral mass, size, and estimated mechanical strength of triple jumpers’ lower limb. Bone 2001; 29: 279-85PubMedCrossRefGoogle Scholar
  85. 85.
    Jones G, Dwyer T. Bone mass in prepubertal children: gender differences and the role of physical activity and sunlight exposure. J Clin Endocrinol Metab 1998; 83: 4274–9PubMedGoogle Scholar
  86. 86.
    Lehtonen-Veromaa M, Mottonen T, Irjala K, et al. A 1-year prospective study on the relationship between physical activity, markers of bone metabolism, and bone acquisition in peripubertal girls. J Clin Endocrinol Metab 2000; 85: 3726–32PubMedGoogle Scholar
  87. 87.
    Lucas A, Lucas R, Sally V, et al. Effect of sub-elite competitive running on bone density, body composition and sexual maturity of adolescent females. Osteoporos Int 2003; 14: 848–56PubMedCrossRefGoogle Scholar
  88. 88.
    Nichols DL, Sanborn CF, Love AM. Resistance training and bone mineral density in adolescent females. J Pediatr 2001; 139: 494–500PubMedCrossRefGoogle Scholar
  89. 89.
    Pettersson U, Alfredson H, Nordstrom P, et al. Bone mass in female cross-country skiers: relationship between muscle strength and different BMD sites. Calcif Tissue Int 2000; 67: 199–206PubMedCrossRefGoogle Scholar
  90. 90.
    Pettersson U, Nordstrom P, Alfredson H, et al. Effect of high impact activity on bone mass and size in adolescent females: a comparative study between two different types of sports. Calcif Tissue Int 2000; 67: 207–14PubMedCrossRefGoogle Scholar
  91. 91.
    Sandstrom P, Jonsson P, Lorentzon R, et al. Bone mineral density and muscle strength in female ice hockey players. Int J Sports Med 2000; 21: 524–8PubMedCrossRefGoogle Scholar
  92. 92.
    Uusi-Rasi K, Sievanen H, Vuori I, et al. Associations of physical activity and calcium intake with bone mass and size in healthy women at different ages. J Bone Miner Res 1998; 13: 133–42PubMedCrossRefGoogle Scholar
  93. 93.
    Wang Q. Baseball and softball injuries. Curr Sports Med Rep 2006; 5: 115–9PubMedCrossRefGoogle Scholar
  94. 94.
    Oppliger RA, Case HS, Horswill CA, et al. American College of Sports Medicine position stand: weight loss in wrestlers. Med Sci Sports Exerc 1996; 28: ix–xiiPubMedGoogle Scholar
  95. 95.
    Torstveit MK, Sundgot-Borgen J. The female athlete triad: are elite athletes at increased risk? Med Sci Sports Exerc 2005; 37: 184–93PubMedCrossRefGoogle Scholar
  96. 96.
    Nichols DL, Sanborn CF. Female athletes and bone. In: Berning JR, Steen SN, editors. Nutrition for sport and exercise. 2nd ed. Gaithersburg: Aspen Publications, 1998: 205–15Google Scholar
  97. 97.
    Cann CE, Martin MC, Genant HK, et al. Decreased spinal mineral content in amenorrheic women. JAMA 1984; 251: 626–9PubMedCrossRefGoogle Scholar
  98. 98.
    Drinkwater BL, Nilson K, Chesnut CHI, et al. Bone mineral content of amenorrheic and eumenorrheic athletes. N Engl J Med 1984; 311: 277–81PubMedCrossRefGoogle Scholar
  99. 99.
    Drinkwater BL, Bruemner B, Chesnut CH. Menstrual history as a determinant of current bone density in young athletes. JAMA 1990; 263: 545–8PubMedCrossRefGoogle Scholar
  100. 100.
    Jonnavithula S, Warren MP, Fox RP, et al. Bone density is compromised in amenorrheic women despite return of menses: a 2-year study. Obstet Gynecol 1993; 81: 669–74PubMedGoogle Scholar
  101. 101.
    Keen AD, Drinkwater BL. Irreversible bone loss in former amenorrheic athletes. Osteoporos Int 1997; 7: 311–5PubMedCrossRefGoogle Scholar
  102. 102.
    De Souza MJ, Williams NI. Physiological aspects and clinical sequelae of energy deficiency and hypoestrogenism in exercising women. Hum Reprod Update 2004; 10: 433–48PubMedCrossRefGoogle Scholar
  103. 103.
    Redman LM, Loucks AB. Menstrual disorders in athletes. Sports Med 2005; 35: 747–55PubMedCrossRefGoogle Scholar
  104. 104.
    Loucks AB, Callister R. Induction and prevention of low-T3 syndrome in exercising women. Am J Physiol 1993; 264: R924–30PubMedGoogle Scholar
  105. 105.
    Loucks AB. Energy availability, not body fatness, regulates reproductive function in women. Exerc Sport Sci Rev 2003; 31: 144–8PubMedCrossRefGoogle Scholar
  106. 106.
    Torstveit MK, Sundgot-Borgen J. The female athlete triad exists in both elite athletes and controls. Med Sci Sports Exerc 2005; 37: 1449–59PubMedCrossRefGoogle Scholar
  107. 107.
    Cobb KL, Bachrach LK, Greendale G, et al. Disordered eating, menstrual irregularity, and bone mineral density in female runners. Med Sci Sports Exerc 2003; 35: 711–9PubMedCrossRefGoogle Scholar
  108. 108.
    Lauder TD, Williams MV, Campbell CS, et al. The female athlete triad: prevalence in military women. Mil Med 1999; 164: 630–5Google Scholar
  109. 109.
    DiPietro L, Stachenfeld NS. The female athlete triad myth [letter]. Med Sci Sports Exerc 2006; 38: 795PubMedCrossRefGoogle Scholar
  110. 110.
    Gibson JH, Mitchell A, Harries MG, et al. Nutritional and exercise-related determinants of bone density in elite female runners. Osteoporos Int 2004; 15: 611–8PubMedCrossRefGoogle Scholar
  111. 111.
    Rencken ML, Chesnut CHI, Drinkwater BL. Bone density at multiple skeletal sites in amenorrheic athletes. JAMA 1996; 276: 238–40PubMedCrossRefGoogle Scholar
  112. 112.
    Howat PM, Carbo ML, Wozniak P. The influence of diet, body fat, menstrual cycling, and activity upon the bone density of females. J Am Diet Assoc 1989; 89: 1305–7PubMedGoogle Scholar
  113. 113.
    Lindberg J, Fears W, Hunt M, et al. Exercise induced amenorrhea and bone density. Ann Intern Med 1984; 101: 647–8PubMedCrossRefGoogle Scholar
  114. 114.
    Robinson TL, Snow-Harter C, Taaffe DR, et al. Gymnasts exhibit higher bone mass than runners despite similar prevalence of amenorrhea and oligomenorrhea. J Bone Miner Res 1995; 10: 26–35PubMedCrossRefGoogle Scholar
  115. 115.
    Young N, Formica C, Szmukler G, et al. 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; 78: 449–54PubMedGoogle Scholar
  116. 116.
    Drinkwater BL, Nilson K, Ott S, et al. Bone mineral density after resumption of menses in amenorrheic athletes. JAMA 1986; 256: 380–2PubMedCrossRefGoogle Scholar
  117. 117.
    Bennell K, Matheson G, Meeuwisse W, et al. Risk factors for stress fractures. Sports Med 1999; 28: 91–122PubMedCrossRefGoogle Scholar
  118. 118.
    Myburgh KH, Hutchins J, Fataar AB, et al. Low bone density is an etiologic factor for stress fractures in athletes. Ann Intern Med 1990; 113: 754–9PubMedCrossRefGoogle Scholar
  119. 119.
    Nattiv A. Stress fractures and bone health in track and field athletes. J Sci Med Sport 2000; 3: 268–79PubMedCrossRefGoogle Scholar
  120. 120.
    Warren MP, Brooks-Gunn J, Hamilton LH, et al. Scoliosis and fractures in young ballet dancers: relation to delayed menarche and secondary amenorrhea. N Engl J Med 1986; 314: 1348–53PubMedCrossRefGoogle Scholar
  121. 121.
    Dugowson CE, Drinkwater BL, Clark JM. Nontraumatic femur fracture in an oligomenorrheic athlete. Med Sci Sports Exerc 1991; 23: 1323–5PubMedCrossRefGoogle Scholar
  122. 122.
    Wilson JH, Wolman RL. Osteoporosis and fracture complications in an amenorrhoeic athlete. Br J Rheumatol 1994; 33: 480–1PubMedCrossRefGoogle Scholar
  123. 123.
    Hosmer WD, Genant HK, Browner WS. Fractures before menopause: a red flag for physicians. Osteoporos Int 2002; 13: 337–41PubMedCrossRefGoogle Scholar
  124. 124.
    Wu F, Mason B, Horne A, et al. Fractures between the ages of 20 and 50 years increase women’s risk of subsequent fractures. Arch Intern Med 2002; 162: 33–6PubMedCrossRefGoogle Scholar
  125. 125.
    Khan KM, Liu-Ambrose T, Sran MM, et al. New criteria for female athlete triad syndrome? As osteoporosis is rare, should osteopenia be among the criteria for defining the female athlete triad syndrome? Br J Sports Med 2002; 36: 10–3PubMedPubMedCentralCrossRefGoogle Scholar
  126. 126.
    Zanker CL, Swaine IL. Relation between bone turnover, oestradiol, and energy balance in women distance runners. Br J Sports Med 1998; 32: 167–71PubMedPubMedCentralCrossRefGoogle Scholar
  127. 127.
    Hergenroeder AC, Smith EO, Shypailo R, et al. Bone mineral changes in young women with hypothalamic amenorrhea treated with oral contraceptives, medroxyprogesterone, or placebo over 12 months. Am J Obstet Gynecol 1997; 176: 1017–25PubMedCrossRefGoogle Scholar
  128. 128.
    Liu SL, Lebrun CM. Effect of oral contraceptives and hormone replacement therapy on bone mineral density in premenopausal and perimenopausal women: a systematic review. Br J Sports Med 2006; 40: 11–24PubMedPubMedCentralCrossRefGoogle Scholar
  129. 129.
    Grinspoon S, Herzog D, Klibanski A. Mechanisms and treat ment options for bone loss in anorexia nervosa. Psychophar macol Bull 1997; 33: 399–404Google Scholar
  130. 130.
    Food and Nutrition Board IoM. Dietary reference intakes for calcium, phosphorus, magnesium, vitamin D, and fluoride. Washington, DC: National Academy Press, 1997Google Scholar
  131. 131.
    Croll JK, Neumark-Sztainer D, Story M, et al. Adolescents involved in weight-related and power team sports have better eating patterns and nutrient intakes than non-sport-involved adolescents. J Am Diet Assoc 2006; 106: 709–17PubMedCrossRefGoogle Scholar
  132. 132.
    Cupisti A, D’Alessandro C, Castrogiovanni S, et al. Nutrition knowledge and dietary composition in Italian adolescent female athletes and non-athletes. Int J Sport Nutr Exerc Metab 2002; 12: 207–19PubMedCrossRefGoogle Scholar
  133. 133.
    Leachman SD, McClanahan BS, Clemens LH, et al. Food sources of calcium in a sample of African-American an Euro-American collegiate athletes. Int J Sport Nutr Exerc Metab 2001; 11: 199–208CrossRefGoogle Scholar
  134. 134.
    Papadopoulou SK, Papadopoulou SD, Gallos GK. Macro-and micro-nutrient intake of adolescent Greek female volleyball players. Int J Sport Nutr Exerc Metab 2002; 12: 73–80PubMedCrossRefGoogle Scholar
  135. 135.
    Hinton PS, Sanford TC, Davidson MM, et al. Nutrient intakes and dietary behaviors of male and female collegiate athletes. Int J Sport Nutr Exerc Metab 2004; 14: 389–405PubMedCrossRefGoogle Scholar
  136. 136.
    Burke LM, Slater G, Broad EM, et al. Eating patterns and meal frequency of elite Australian athletes. Int J Sport Nutr Exerc Metab 2003; 13: 521–38PubMedCrossRefGoogle Scholar
  137. 137.
    Caine D, Lewis R, O’Connor P, et al. Does gymnastics training inhibit growth of females? Clin J Sport Med 2001; 11: 260–70PubMedCrossRefGoogle Scholar
  138. 138.
    Garcia-Roves PM, Fernandez S, Rodriguez M, et al. Eating pattern and nutritional status of international elite flatwater paddlers. Int J Sport Nutr Exerc Metab 2000; 10: 182–98PubMedCrossRefGoogle Scholar
  139. 139.
    Jonnalagadda SS, Bernadot D, Nelson M. Energy and nutrient intakes of the United States National Women’s Artistic Gymnastics Team. Int J Sport Nutr 1998; 8: 331–44PubMedCrossRefGoogle Scholar
  140. 140.
    Ziegler P, Sharp R, Hughes V, et al. Nutritional status of teenage female competitive figure skaters. J Am Diet Assoc 2002; 102: 374–9PubMedCrossRefGoogle Scholar
  141. 141.
    Clark M, Reed DB, Crouse SF, et al. Pre-and post-season dietary intake, body composition, and performance indices of NCAA division I female soccer players. Int J Sport Nutr Exerc Metab 2003; 13: 303–19PubMedCrossRefGoogle Scholar
  142. 142.
    Winters-Stone KM, Snow CM. One year of oral calcium supplementation maintains cortical bone density in young adult female distance runners. Int J Sport Nutr Exerc Metab 2004; 14: 7–17PubMedCrossRefGoogle Scholar
  143. 143.
    Weaver CM, Fleet JC. Vitamin D requirements: current and future. Am J Clin Nutr 2004; 80: 1735S–9SPubMedGoogle Scholar
  144. 144.
    Manore MM. Dietary recommendations and athletic menstrual dysfunction. Sports Med 2002; 32: 887–901PubMedCrossRefGoogle Scholar
  145. 145.
    Lemon PW. Do athletes need more dietary protein and amino acids? Int J Sport Nutr 1995; 5 Suppl.: S39–61CrossRefGoogle Scholar
  146. 146.
    Lemon PW. Effects of exercise on dietary protein requirements. Int J Sport Nutr 1998; 8: 426–47PubMedCrossRefGoogle Scholar
  147. 147.
    Food and Nutrition Board IoM. Dietary intakes for energy, carbohydrate, fiber, fat, fatty acids, cholesterol, protein, and amino acids (macronutrients). Washington, DC: National Academy Press, 2005Google Scholar
  148. 148.
    Bonjour JP. Dietary protein: an essential nutrient for bone health. J Am Coll Nutr 2005; 24: 526S–36SPubMedCrossRefGoogle Scholar
  149. 149.
    New SA. Do vegetarians have a normal bone mass? Osteoporos Int 2004; 15: 679–88PubMedCrossRefGoogle Scholar
  150. 150.
    Fogelholm M. Dairy products, meat and sports performance. Sports Med 2003; 33: 615–31PubMedCrossRefGoogle Scholar
  151. 151.
    Nieman DC. Physical fitness and vegetarian diets: is there a relation? Am J Clin Nutr 1999; 70: 570S–5SPubMedGoogle Scholar
  152. 152.
    Venderley AM, Campbell WW. Vegetarian diets: nutritional considerations for athletes. Sports Med 2006; 36: 293–305PubMedCrossRefGoogle Scholar
  153. 153.
    Janelle KC and Barr SI. Nutrient intakes and eating behavior scores of vegetarian and nonvegetarian women. J Am Diet Assoc 1995; 95: 180–6PubMedCrossRefGoogle Scholar
  154. 154.
    Barr SI, Broughton TM. Relative weight, weight loss efforts and nutrient intakes among health-conscious vegetarian, past vegetarian and nonvegetarian women ages 18 to 50. J Am Coll Nutr 2000; 19: 781–8PubMedCrossRefGoogle Scholar
  155. 155.
    Davey GK, Spencer EA, Appleby PN, et al. EPIC-Oxford: lifestyle characteristics and nutrient intakes in a cohort of 33 883 meat-eaters and 31 546 non meat-eaters in the UK. Public Health Nutr 2003; 6: 259–69PubMedCrossRefGoogle Scholar
  156. 156.
    Smith AM. Veganism and osteoporosis: a review of the current literature. Int J Nurs Pract 2006; 12: 302–6PubMedCrossRefGoogle Scholar
  157. 157.
    Barr SI, Rideout CA. Nutritional considerations for vegetarian athletes. Nutrition 2004; 20: 696–703PubMedCrossRefGoogle Scholar
  158. 158.
    Klopp SA, Heiss CJ, Smith HS. Self-reported vegetarianism may be a marker for college women at risk for disordered eating. J Am Diet Assoc 2003; 103: 745–7PubMedCrossRefGoogle Scholar
  159. 159.
    Weinberg LG, Berner LA, Groves JE. Nutrient contributions of dairy foods in the United States: continuing survey of food intakes by individuals, 1994-1996, 1998. J Am Diet Assoc 2004; 104: 895–902PubMedCrossRefGoogle Scholar
  160. 160.
    Heaney RP, Rafferty K, Bierman J. Not all calcium-fortified beverages are equal. Nutr Today 2005; 40: 39–44Google Scholar
  161. 161.
    Turner LW, Bass MA. Osteoporosis knowledge, attitudes, and behaviors of female collegiate athletes. Int J Sport Nutr Exerc Metab 2001; 11: 482–9PubMedCrossRefGoogle Scholar
  162. 162.
    American College of Sports Medicine, American Dietetic Association and Dietitians of Canada. Joint position statement: nutrition and athletic performance. Med Sci Sports Exerc 2000; 32: 2130–45PubMedCrossRefGoogle Scholar
  163. 163.
    Manore MM. Nutritional needs of the female athlete. Clin Sports Med 1999; 18: 549–63PubMedCrossRefGoogle Scholar
  164. 164.
    Burke L, Deakin V. Clinical sports nutrition. 3rd ed. Roseville (NSW): McGraw-Hill Australia, 2006Google Scholar

Copyright information

© Adis Data Information BV 2007

Authors and Affiliations

  • David L. Nichols
    • 1
  • Charlotte F. Sanborn
    • 1
  • Eve V. Essery
    • 2
  1. 1.Department of KinesiologyTexas Woman’s UniversityDentonUSA
  2. 2.Department of Nutrition and Food SciencesTexas Woman’s UniversityDentonUSA

Personalised recommendations