Sports Medicine

, Volume 41, Issue 7, pp 587–607 | Cite as

Obstacles in the Optimization of Bone Health Outcomes in the Female Athlete Triad

  • Gaele Ducher
  • Anne I. Turner
  • Sonja Kukuljan
  • Kathleen J. Pantano
  • Jennifer L. Carlson
  • Nancy I. Williams
  • Mary Jane De Souza
Review Article

Abstract

Maintaining low body weight for the sake of performance and aesthetic purposes is a common feature among young girls and women who exercise on a regular basis, including elite, college and high-school athletes, members of fitness centres, and recreational exercisers. High energy expenditure without adequate compensation in energy intake leads to an energy deficiency, which may ultimately affect reproductive function and bone health. The combination of low energy availability, menstrual disturbances and low bone mineral density is referred to as the ‘female athlete triad’. Not all athletes seek medical assistance in response to the absence of menstruation for 3 or more months as some believe that long-term amenorrhoea is not harmful. Indeed, many women may not seek medical attention until they sustain a stress fracture.

This review investigates current issues, controversies and strategies in the clinical management of bone health concerns related to the female athlete triad. Current recommendations focus on either increasing energy intake or decreasing energy expenditure, as this approach remains the most efficient strategy to prevent further bone health complications. However, convincing the athlete to increase energy availability can be extremely challenging.

Oral contraceptive therapy seems to be a common strategy chosen by many physicians to address bone health issues in young women with amenorrhoea, although there is little evidence that this strategy improves bone mineral density in this population. Assessment of bone health itself is difficult due to the limitations of dual-energy X-ray absorptiometry (DXA) to estimate bone strength. Understanding how bone strength is affected by low energy availability, weight gain and resumption of menses requires further investigations using 3-dimensional bone imaging techniques in order to improve the clinical management of the female athlete triad.

Notes

Acknowledgements

No funding was used to assist in the preparation of the manuscript. The authors have no conflict of interest.

References

  1. 1.
    Nattiv A, Loucks AB, Manore MM, et al. American College of Sports Medicine position stand: the female athletetriad. Med Sci Sports Exerc 2007 Oct; 39 (10): 1867–82PubMedCrossRefGoogle Scholar
  2. 2.
    Beals KA, Meyer NL. Female athlete triad update. Clin Sports Med 2007 Jan; 26 (1): 69–89PubMedCrossRefGoogle Scholar
  3. 3.
    Wade GN, Schneider JE, Li HY. Control of fertility by metabolic cues. Am J Physiol 1996 Jan; 270 (1Pt1): E1–19PubMedGoogle Scholar
  4. 4.
    Edwards JE, Lindeman AK, Mikesky AE, et al. Energy balance in highly trained female endurance runners. Med Sci Sports Exerc 1993 Dec; 25 (12): 1398–404PubMedGoogle Scholar
  5. 5.
    Mulligan K, Butterfield GE. Discrepancies between energy intake and expenditure in physically active women. Br JNutr 1990 Jul; 64 (1): 23–36CrossRefGoogle Scholar
  6. 6.
    Myerson M, Gutin B, Warren MP, et al. Resting metabolic rate and energy balance in amenorrheic and eumenorrheicrunners. Med Sci Sports Exerc 1991 Jan; 23 (1): 15–22PubMedGoogle Scholar
  7. 7.
    Nelson ME, Fisher EC, Catsos PD, et al. Diet and bone status in amenorrheic runners. Am J Clin Nutr 1986 Jun; 43 (6): 910–6PubMedGoogle Scholar
  8. 8.
    Bonci CM, Bonci LJ, Granger LR, et al. National Athletic Trainers’ Association position statement: preventing,detecting, and managing disordered eating in athletes. J Athletic Train 2008; 43 (1): 80–108CrossRefGoogle Scholar
  9. 9.
    De Souza MJ, Williams NI. Physiological aspects and clinical sequelae of energy deficiency and hypoestrogenismin exercising women. Hum Reprod Update 2004; 10 (5): 433–48PubMedCrossRefGoogle Scholar
  10. 10.
    Goodman LR, Warren MP. The female athlete and menstrual function. Curr Opin Obstet Gynecol 2005; 17: 466–70PubMedCrossRefGoogle Scholar
  11. 11.
    Loucks AB. Energy balance and body composition in sports and exercise. J Sports Sci 2004; 22 (1): 1–14PubMedCrossRefGoogle Scholar
  12. 12.
    Manore MM, Kam LC, Loucks AB. The female athlete triad: components, nutrition issues, and health consequences. J Sports Sci 2007; 25 (1): S61–71PubMedCrossRefGoogle Scholar
  13. 13.
    Warren MP, Chua AT. Exercise-induced amenorrhea and bone health in the adolescent athlete. Ann NY Acad Sci 2008; 1135: 244–52PubMedCrossRefGoogle Scholar
  14. 14.
    Zanker C, Hind K. The effect of energy balance on endocrine function and bone health in youth. In: Daly RM, Petit MA, editors. Optimizing bone mass and strength:the role of physical activity and nutrition during growth. Basel: Karger, 2007: 80–101Google Scholar
  15. 15.
    The Practice Committee of the American Society for Reproductive Medicine. Current evaluation of amenorrhea. Fertil Steril 2004 Sep; 82 Suppl. 1: S33–9Google Scholar
  16. 16.
    Golden NH, Carlson JL. The pathophysiology of amenorrhea in the adolescent. Ann NY Acad Sci 2008; 1135: 163–78PubMedCrossRefGoogle Scholar
  17. 17.
    Loucks AB, Horvath SM. Athletic amenorrhea: a review. Med Sci Sports Exerc 1985 Feb; 17 (1): 56–72PubMedGoogle Scholar
  18. 18.
    Bennell K, Matheson G, Meeuwisse W, et al. Risk factors for stress fractures. Sports Med 1999 Aug; 28 (2): 91–122PubMedCrossRefGoogle Scholar
  19. 19.
    Pearce G, Bass S, Young N, et al. Does weight-bearing exercise protect against the effects of exercise-inducedoligomenorrhea on bone density? Osteoporos Int 1996; 6 (6): 448–52PubMedCrossRefGoogle Scholar
  20. 20.
    Christo K, Prabhakaran R, Lamparello B, et al. Bone metabolism in adolescent athletes with amenorrhea, athleteswith eumenorrhea, and control subjects. Pediatrics 2008; 121: 1127–36PubMedCrossRefGoogle Scholar
  21. 21.
    Fredericson M, Kent K. Normalization of bone density in a previously amenorrheic runner with osteoporosis. Med Sci Sports Exerc 2005; 37 (9): 1481–6PubMedCrossRefGoogle Scholar
  22. 22.
    Gibson JH, Harries M, Mitchell A, et al. Determinants of bone density and prevalence of osteopenia among femalerunners in their second to seventh decades of age. Bone 2000 Jun; 26 (6): 591–8PubMedCrossRefGoogle Scholar
  23. 23.
    Gremion G, Rizzoli R, Slosman D, et al. Oligo-amenorrheic long-distance runners may lose more bone in spine thanin femur. Med Sci Sports Exerc 2001 Jan; 33 (1): 15–21PubMedGoogle Scholar
  24. 24.
    Hind K. Recovery of bone mineral density and fertility in a former amenorrheic athlete. J Sports Sci Med 2008; 7: 415–8Google Scholar
  25. 25.
    Keen AD, Drinkwater BL. Irreversible bone loss in former amenorrheic athletes. Osteoporos Int 1997; 7: 311–5PubMedCrossRefGoogle Scholar
  26. 26.
    Stacey E, Korkia P, Hukkanen MV, et al. Decreased nitric oxide levels and bone turnover in amenorrheic athleteswith spinal osteopenia. J Clin Endocrinol Metab 1998 Sep; 83 (9): 3056–61PubMedCrossRefGoogle Scholar
  27. 27.
    Abraham SF, Beumont PJ, Fraser IS, et al. Body weight, exercise and menstrual status among ballet dancers intraining. Br J Obstet Gynaecol 1982; 89: 507–10PubMedCrossRefGoogle Scholar
  28. 28.
    Bennell KL, Malcolm SA, Thomas SA, et al. Risk factors for stress fractures in female track-and-field athletes: aretrospective analysis. Clin J Sport Med 1995; 5: 229–35PubMedCrossRefGoogle Scholar
  29. 29.
    Carlberg KA, Buckman MT, Peake GT, et al. A survey of menstrual function in athletes. Eur J Appl Physiol 1983; 51 (2): 211–22CrossRefGoogle Scholar
  30. 30.
    Castelo-Branco C, Reina F, Montivero AD, et al. Influence of high-intensity training and of dietetic and anthropometricfactors on menstrual cycle disorders in ballet dancers. Gynecol Endocrinol 2006 Jan; 22 (1): 31–5PubMedCrossRefGoogle Scholar
  31. 31.
    Dusek T. Influence of high intensity training on menstrual cycle disorders in athletes. Croat Med J 2001; 42: 79–82PubMedGoogle Scholar
  32. 32.
    Nichols JF, Rauh MJ, Lawson MJ, et al. Prevalence of the female athlete triad syndrome among high school athletes. Arch Pediatr Adolesc Med 2006; 160 (2): 137–42PubMedCrossRefGoogle Scholar
  33. 33.
    Beals K, Manore M. Disorders of the female athlete triad among collegiate athletes. Int J Sport Nutr Exerc Metab 2002; 12: 281–93PubMedGoogle Scholar
  34. 34.
    Beals KA, Hill AK. The prevalence of disordered eating, menstrual dysfunction, and low bone mineral densityamong US collegiate athletes. Int J Sport Nutr Exerc Metab 2006 Feb; 16 (1): 1–23PubMedGoogle Scholar
  35. 35.
    Mudd LM, Fornetti W, Pivarnik JM. Bone mineral density in collegiate female athletes: comparisons among sports. J Athlet Training 2007; 42 (3): 403–8Google Scholar
  36. 36.
    Legro RS, Lin HM, Demers LM, et al. Rapid maturation of the reproductive axis during perimenarche independentof body composition. J Clin Endocrinol Metab 2000 Mar; 85 (3): 1021–5PubMedCrossRefGoogle Scholar
  37. 37.
    Metcalf MG, Skidmore DS, Lowry GF, et al. Incidence of ovulation in the years after the menarche. J Endocrinol 1983 May; 97 (2): 213–9PubMedCrossRefGoogle Scholar
  38. 38.
    Metcalf MG. Incidence of ovulation from the menarche to the menopause: observations of 622 New Zealand women. N Z Med J 1983 Aug 24; 96 (738): 645–8PubMedGoogle Scholar
  39. 39.
    Treloar AE, Boynton RE, Behn BG, et al. Variation of the human menstrual cycle through reproductive life. Int JFertil 1967 Jan-Mar; 12 (1Pt2): 77–126Google Scholar
  40. 40.
    Zanker CL, Cooke CB, Truscott JG, et al. Annual changes of bone density over 12 years in an amenorrheic athlete. Med Sci Sports Exerc 2004; 36 (1): 137–42PubMedCrossRefGoogle Scholar
  41. 41.
    Carlson JL, Curtis M, Halpern-Felsher B. Clinician practices for the management of amenorrhea in the adolescentand young adult athlete. J Adolesc Health 2007 Apr; 40 (4): 362–5PubMedCrossRefGoogle Scholar
  42. 42.
    Haberland CA, Seddick D, Marcus R, et al. A physician survey of therapy for exercise-associated amenorrhea: abrief report. Clin J Sport Med 1995; 5 (4): 246–50PubMedCrossRefGoogle Scholar
  43. 43.
    Troy K, Hoch AZ, Stavrakos JE. Awareness and comfort in treating the female athlete triad: are we failing ourathletes? Wisconsin Med J 2006; 105 (7): 21–4Google Scholar
  44. 44.
    The IOC Medical Commission Working Group Women in Sport. Position stand on the female athlete triad [online]. Available from URL: http://multimedia.olympic.org/pdf/en_report_917.pdf [Accessed 2009 Sep 27]
  45. 45.
    Cobb KL, Bachrach LK, Sowers M, et al. The effect of oral contraceptives on bone mass and stress fractures in femalerunners. Med Sci Sports Exerc 2007 Sep; 39 (9): 1464–73PubMedCrossRefGoogle Scholar
  46. 46.
    Gibson JH, Mitchell A, Reeve J, et al. Treatment of reduced bone mineral density in athletic amenorrhea: a pilotstudy. Osteoporos Int 1999; 10 (4): 284–9PubMedCrossRefGoogle Scholar
  47. 47.
    Warren MP, Brooks-Gunn J, Fox RP, et al. Persistent osteopenia in ballet dancers with amenorrhea and delayedmenarche despite hormone therapy: a longitudinal study. Fertil Steril 2003; 80 (2): 398–404PubMedCrossRefGoogle Scholar
  48. 48.
    Otis CL, Drinkwater B, Johnson M, et al. American College of Sports Medicine position stand: the female athletetriad. Med Sci Sports Exerc 1997 May; 29 (5): i–ixPubMedCrossRefGoogle Scholar
  49. 49.
    Liu SL, Lebrun CM. Effect of oral contraceptives and hormone replacement therapy on bone mineral density inpremenopausal and perimenopausal women: a systematicreview. Br J Sports Med 2006; 40 (1): 11–24PubMedCrossRefGoogle Scholar
  50. 50.
    Mann BJ, Grana WA, Indelicato PA, et al. A survey of sports medicine physicians regarding psychological issuesin patient-athletes. Am J Sports Med 2007; 35: 2140–7PubMedCrossRefGoogle Scholar
  51. 51.
    Papanek PE. The female athlete triad: an emerging role for physical therapy. J Orthop Sports Phys Ther 2003; 33 (10): 594–614PubMedGoogle Scholar
  52. 52.
    Pantano KJ. Strategies used by physical therapists in the U.S. for treatment and prevention of the female athlete triad. Phys Ther Sport 2009; 10: 3–11PubMedCrossRefGoogle Scholar
  53. 53.
    Adams J, Bishop N. DXA in adults and children. In: Rosen CJ, Compston JE, Lian JB, editors. Primer on the metabolicbone diseases and disorders of mineral metabolism. 7th ed. Washington, DC: American Society for Bone andMineral Research, 2008: 152–8Google Scholar
  54. 54.
    Hans D, Downs Jr RW, Duboeuf F, et al. Skeletal sites for osteoporosis diagnosis: the 2005 ISCD Official Positions. J Clin Densitom 2006 Jan-Mar; 9 (1): 15–21PubMedCrossRefGoogle Scholar
  55. 55.
    Baim S, Binkley N, Bilezikian JP, et al. Official positions of the International Society for Clinical Densitometry andexecutive summary of the 2007 ISCD Position Development Conference. J Clin Densitom 2008; 11 (1): 75–91PubMedCrossRefGoogle Scholar
  56. 56.
    Robinson TL, Snow-Harter C, Taaffe DR, et al. Gymnasts exhibit higher bone mass than runners despite similarprevalence of amenorrhea and oligomenorrhea. J Bone Miner Res 1995; 10 (1): 26–35PubMedCrossRefGoogle Scholar
  57. 57.
    Fehling PC, Alekel L, Clasey J, et al. A comparison of bone mineral densities among female athletes in impact loadingand active loading sports. Bone 1995; 17 (3): 205–10PubMedCrossRefGoogle Scholar
  58. 58.
    Wolman RL, Faulmann L, Clark P, et al. Different training patterns and bone mineral density of the femoral shaft inelite, female athletes. Ann Rheum Dis 1991 Jul; 50 (7): 487–9PubMedCrossRefGoogle Scholar
  59. 59.
    Valentino R, Savastano S, Tommaselli AP, et al. The influence of intense ballet training on trabecular bone mass,hormone status, and gonadotropin structure in youngwomen. J Clin Endocrinol Metab 2001 Oct; 86 (10): 4674–8PubMedCrossRefGoogle Scholar
  60. 60.
    Gibson JH, Mitchell A, Harries MG, et al. Nutritional and exercise-related determinants of bone density in elite femalerunners. Osteoporos Int 2004 Aug; 15 (8): 611–8PubMedCrossRefGoogle Scholar
  61. 61.
    Kaufman BA, Warren MP, Dominguez JE, et al. Bone density and amenorrhea in ballet dancers are related to adecreased resting metabolic rate and lower leptin levels. J Clin Endocrinol Metab 2002; 87: 2777–83PubMedCrossRefGoogle Scholar
  62. 62.
    Warren MP, Brooks-Gunn J, Fox RP, et al. Osteopenia in exercise-associated amenorrhea using ballet dancers as amodel: a longitudinal study. J Clin Endocrinol Metab 2002; 87 (7): 3162–8PubMedCrossRefGoogle Scholar
  63. 63.
    Young N, Formica C, Szmukler G, et al. Bone density at weight-bearing and non weight-bearing sites in balletdancers: the effects of exercise, hypogonadism, and bodyweight. J Clin Endocrinol Metab 1994; 78 (2): 449–54PubMedCrossRefGoogle Scholar
  64. 64.
    Prior JC, Vigna YM, Barr SI, et al. Cyclic medroxyprogesterone treatment increases bone density: a controlledtrial in active women with menstrual cycle disturbances. AmJ Med 1994 Jun; 96 (6): 521–30CrossRefGoogle Scholar
  65. 65.
    Khan KM, Liu-Ambrose T, Sran MM, et al. New criteria for female athlete triad syndrome? Br J Sports Med 2002; 36: 10–3PubMedCrossRefGoogle Scholar
  66. 66.
    Marshall D, Johnell O, Wedel H. Meta-analysis of how well measures of bone mineral density predict occurrenceof osteoporotic fractures. BMJ 1996; 312: 1254–9PubMedCrossRefGoogle Scholar
  67. 67.
    Land C, Schoenau E. Fetal and postnatal bone development: reviewing the role of mechanical stimuli and nutrition. Best Pract Res Clin Endocrinol Metab 2008 Feb; 22 (1): 107–18PubMedCrossRefGoogle Scholar
  68. 68.
    Carter DR, Bouxsein ML, Marcus R. New approaches for interpreting projected bone densitometry data. J Bone Miner Res 1992; 7: 137–45PubMedCrossRefGoogle Scholar
  69. 69.
    Leonard MB, Zemel BS. Current concepts in pediatric bone disease. Pediatr Clin North Am 2002 Feb; 49 (1): 143–73PubMedCrossRefGoogle Scholar
  70. 70.
    Hansen MA, Hassager C, Overgaard K, et al. Dual-energy x-ray absorptiometry: a precise method of measuringbone mineral density in the lumbar spine. J Nucl Med 1990 Jul; 31 (7): 1156–62PubMedGoogle Scholar
  71. 71.
    Bolotin HH. DXA in vivo BMD methodology: an erroneous and misleading research and clinical gauge of bonemineral status, bone fragility, and bone remodelling. Bone 2007 Jul; 41 (1): 138–54PubMedCrossRefGoogle Scholar
  72. 72.
    Svendsen OL, Hendel HW, Gotfredsen A, et al. Are soft tissue composition of bone and non-bone pixels in spinalbone mineral measurements by DXA similar? Impact ofweight loss. Clin Physiol Funct Imaging 2002 Jan; 22 (1): 72–7PubMedCrossRefGoogle Scholar
  73. 73.
    Robling AG, Hinant FM, Burr DB, et al. Improved bone structure and strength after long-term mechanical loadingis greatest if loading is separated into short bouts. J Bone Miner Res 2002 Aug; 17 (8): 1545–54PubMedCrossRefGoogle Scholar
  74. 74.
    Bass SL, Saxon L, Daly RM, et al. The effect of mechanical loading on the size and shape of bone in pre-, peri-, andpostpubertal girls: a study in tennis players. J Bone Miner Res 2002; 17 (12): 2274–80PubMedCrossRefGoogle Scholar
  75. 75.
    Ducher G, Courteix D, Mëme S, et al. Bone geometry in response to long-term tennis playing and its relationshipwith muscle Vol.: a quantitative magnetic resonanceimaging study in tennis players. Bone 2005; 37 (4): 457–66PubMedCrossRefGoogle Scholar
  76. 76.
    Duncan CS, Blimkie CJ, Kemp A, et al. Mid-femur geometry and biomechanical properties in 15- to 18-yr-oldfemale athletes. Med Sci Sports Exerc 2002; 34 (4): 673–81PubMedCrossRefGoogle Scholar
  77. 77.
    Greene DA, Naughton GA, Briody JN, et al. Bone strength index in adolescent girls: does physical activity make adifference? Br J Sports Med 2005; 39: 622–7PubMedCrossRefGoogle Scholar
  78. 78.
    Greene DA, Naughton GA, Briody JN, et al. Bone and muscle geometry in female adolescent middle-distancerunners. Pediatr Ex Sci 2005; 17: 377–89Google Scholar
  79. 79.
    Ducher G, Daly RM, Bass SL. The effects of repetitive loading on bone mass and geometry in young male tennisplayers: a quantitative study using MRI. J Bone Miner Res 2009; 24 (10): 1686–92PubMedCrossRefGoogle Scholar
  80. 80.
    Cann CE, Cavanaugh DJ, Schnurpfiel K, et al. Menstrual history is the primary determinant of trabecular bone density in women [abstract]. Med Sci Sports Exerc 1988; 20 Suppl.2: S59Google Scholar
  81. 81.
    Cann CE, Martin MC, Genant HK, et al. Decreased spinal mineral content in amenorrheic women. JAMA 1984 Feb 3; 251 (5): 626–9PubMedCrossRefGoogle Scholar
  82. 82.
    Ward K, Mughal Z, Adams JE. Tools for measuring bone in children and adolescents. In: Sawyer AJ, Bachrach LK, Fung EB, editors. Bone densitometry in growing patients:guidelines for clinical practice. Totowa (NJ): Humana Press, 2007: 15–40CrossRefGoogle Scholar
  83. 83.
    Liu D, Manske SL, Kontulainen SA, et al. Tibial geometry is associated with failure load ex vivo: a MRI, pQCT andDXA study. Osteoporos Int 2007 Jul; 18 (7): 991–7PubMedCrossRefGoogle Scholar
  84. 84.
    Hudelmaier M, Kuhn V, Lochmüller EM, et al. Can geometry- based parameters from pQCT and material parametersfrom quantitative ultrasound (QUS) improve theprediction of radial bone strength over that by bone mass(DXA)? Osteoporos Int 2004; 15: 375–81PubMedCrossRefGoogle Scholar
  85. 85.
    Muller ME, Webber CE, Bouxsein ML. Predicting the failure load of the distal radius. Osteoporos Int 2003; 14: 345–52PubMedCrossRefGoogle Scholar
  86. 86.
    Ashe MC, Khan KM, Kontulainen SA, et al. Accuracy of pQCT for evaluating the aged human radius: an ashing,histomorphometry and failure load investigation. Osteoporos Int 2006; 17: 1241–51PubMedCrossRefGoogle Scholar
  87. 87.
    Lochmuller EM, Lill CA, Kuhn V, et al. Radius bone strength in bending, compression, and falling and itscorrelation with clinical densitometry at multiple sites. J Bone Miner Res 2002 Sep; 17 (9): 1629–38PubMedCrossRefGoogle Scholar
  88. 88.
    Louis O, Boulpaep F, Willnecker J, et al. Cortical mineral content of the radius assessed by peripheral QCT predictscompressive strength on biomechanical testing. Bone 1995 Mar; 16 (3): 375–9PubMedCrossRefGoogle Scholar
  89. 89.
    Kontulainen SA, Johnston JD, Liu D, et al. Strength indices from pQCT imaging predict up to 85% of variancein bone failure properties at tibial epiphysis and diaphysis. J Musculoskelet Neuronal Interact 2008 Oct-Dec; 8 (4): 401–9PubMedGoogle Scholar
  90. 90.
    Milos G, Spindler A, Rüegsegger P, et al. Cortical and trabecular bone density and structure in anorexia nervosa. Osteoporos Int 2005; 16 (7): 783–90PubMedCrossRefGoogle Scholar
  91. 91.
    Resch H, Newrkla S, Grampp S, et al. Ultrasound and X-ray-based bone densitometry in patients with anorexianervosa. Calcif Tissue Int 2000; 66: 338–41PubMedCrossRefGoogle Scholar
  92. 92.
    Schneider P, Biko J, Schlamp D, et al. Comparison of total and regional body composition in adolescent patientswith anorexia nervosa and pair-matched controls. Eating Weight Disord 1998; 3: 179–87Google Scholar
  93. 93.
    Fricke O, Tutlewski O, Stabrey A, et al. A Cybernetic approach to osteoporosis in anorexia nervosa. J Musculoskelet Neuronal Interact 2005; 5 (2): 155–61PubMedGoogle Scholar
  94. 94.
    Eser P, Hill B, Ducher G, et al. Skeletal benefits after longterm retirement in former elite female gymnasts. J Bone Miner Res 2009; 24 (12): 1981–8PubMedCrossRefGoogle Scholar
  95. 95.
    Ducher G, Eser P, Hill B, et al. History of amenorrhoea compromises some of the exercise-induced benefits incortical and trabecular bone in the peripheral and axialskeleton: a study in retired elite gymnasts. Bone 2009 Jun 29; 45: 760–7PubMedCrossRefGoogle Scholar
  96. 96.
    Ducher G, Bass SL, Karlsson MK. Growing a healthy skeleton: the importance of mechanical loading. In: Rosen CJ, Compston JE, Lian JB, editors. Primer on the metabolicbone diseases and disorders of mineral metabolism. 7th ed. Washington, DC: American Society for Bone and Mineral Research, 2008: 86–90CrossRefGoogle Scholar
  97. 97.
    Seeman E. Periosteal bone formation-a neglected determinant of bone strength. N Engl J Med 2003; 349 (4): 320–3PubMedCrossRefGoogle Scholar
  98. 98.
    Chavassieux P, Seeman E, Delmas PD. Insights into material and structural basis of bone fragility from diseasesassociated with fractures: how determinants of the biomechanicalproperties of bone are compromised by disease. Endocr Rev 2007 Apr; 28 (2): 151–64PubMedCrossRefGoogle Scholar
  99. 99.
    Baim S, Leonard MB, Bianchi ML, et al. Official positions of the International Society for Clinical Densitometry andexecutive summary of the 2007 ISCD Pediatric Position Development Conference. J Clin Densitom 2008; 11 (1): 6–21PubMedCrossRefGoogle Scholar
  100. 100.
    Ihle R, Loucks AB. Dose-response relationships between energy availability and bone turnover in young exercisingwomen. J Bone Miner Res 2004; 19 (8): 1231–40PubMedCrossRefGoogle Scholar
  101. 101.
    Henriksen DB, Alexandersen P, Bjarnason NH, et al. Role of gastrointestinal hormones in postprandial reductionof bone resorption. J Bone Miner Res 2003 Dec; 18 (12): 2180–9PubMedCrossRefGoogle Scholar
  102. 102.
    Zanker CL, Swaine IL. Bone turnover in amenorrhoeic and eumenorrhoeic women distance runners. Scand J Med Sci Sports 1998 Feb; 8 (1): 20–6PubMedCrossRefGoogle Scholar
  103. 103.
    Zanker CL, Swaine IL. Relation between bone turnover, oestradiol, and energy balance in women distance runners. Br J Sports Med 1998 Jun; 32 (2): 167–71PubMedCrossRefGoogle Scholar
  104. 104.
    Okano H, Mizunuma H, Soda M, et al. Effects of exercise and amenorrhea on bone mineral density in teenage runners. Endocr J 1995 Apr; 42 (2): 271–6PubMedCrossRefGoogle Scholar
  105. 105.
    De Souza MJ, West SL, Jamal SA, et al. The presence of both an energy deficiency and estrogen deficiency exacerbatealterations of bone metabolism in exercisingwomen. Bone 2008; 43: 140–8PubMedCrossRefGoogle Scholar
  106. 106.
    Heer M, Mika C, Grzella I, et al. Bone turnover during inpatient nutritional therapy and outpatient follow-up inpatients with anorexia nervosa compared with that inhealthy control subjects. Am J Clin Nutr 2004 Sep; 80 (3): 774–81PubMedGoogle Scholar
  107. 107.
    Heer M, Mika C, Grzella I, et al. Changes in bone turnover in patients with anorexia nervosa during eleven weeks ofinpatient dietary treatment. Clin Chem 2002 May; 48 (5): 754–60PubMedGoogle Scholar
  108. 108.
    Loucks AB, Thuma JR. Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularlymenstruating women. J Clin Endocrinol Metab 2003; 88 (1): 297–311PubMedCrossRefGoogle Scholar
  109. 109.
    Loucks AB. Low energy availability in the marathon and other endurance sports. Sports Med 2007; 37 (4-5): 348–52PubMedCrossRefGoogle Scholar
  110. 110.
    Bass S, Daly R, Blimkie CJ. Growing a healthy skeleton: exercise — the primary driving force. In: Hebestreit H, Bar-Or O, editors. The encyclopaedia of sports medicine:the young athlete. Oxford: Blackwell Publishing, 2008: 112–26Google Scholar
  111. 111.
    Clark EM, Ness AR, Bishop NJ, et al. Association between bone mass and fractures in children: a prospective cohortstudy. J Bone Miner Res 2006 Sep; 21 (9): 1489–95PubMedCrossRefGoogle Scholar
  112. 112.
    Kalkwarf HJ, Zemel BS, Gilsanz V, et al. The Bone Mineral Density in Childhood Study: bone mineral contentand density according to age, sex, and race. J Clin Endocrinol Metab 2007; 92: 2087–99PubMedCrossRefGoogle Scholar
  113. 113.
    Arabi A, Nabulsi M, Maalouf J, et al. Bone mineral density by age, gender, pubertal stages, and socioeconomic statusin healthy Lebanese children and adolescents. Bone 2004; 35: 1169–79PubMedCrossRefGoogle Scholar
  114. 114.
    Van Coeverden SCCM, De Ridder CM, Roos JC, et al. Pubertal maturation characteristics and the rate of bonemass development longitudinally toward menarche. J Bone Miner Res 2001; 16: 774–81PubMedCrossRefGoogle Scholar
  115. 115.
    Jones IE, Williams SM, Dow N, et al. How many children remain fracture-free during growth? A longitudinal study of children and adolescents participating in the Dunedin Multidisciplinary Health and Development Study. Osteoporos Int 2002; 13 (12): 990–5PubMedCrossRefGoogle Scholar
  116. 116.
    Cooper C, Dennison EM, Leufkens HGM, et al. Epidemiology of childhood fractures in Britain: a study usingthe general practice research database. J Bone Miner Res 2004; 19 (12): 1976–81PubMedCrossRefGoogle Scholar
  117. 117.
    Goulding A. Risk factors for fractures in normally active children and adolescents. Med Sport Sci 2007; 51: 102–20PubMedCrossRefGoogle Scholar
  118. 118.
    Warren MP, Ramos RH, Bronson EM. Exercise-associated amenorrhea. Phys Sportsmed 2002; 30 (10): 41–6PubMedCrossRefGoogle Scholar
  119. 119.
    Bass S, Delmas PD, Pearce G, et al. The differing tempo of growth in bone size, mass, and density in girls is regionspecific. J Clin Invest 1999; 104 (6): 795–804PubMedCrossRefGoogle Scholar
  120. 120.
    Leonard MB, Shults J, Elliott DM, et al. Interpretation of whole body dual energy x-ray absorptiometry measures inchildren: comparison with peripheral quantitative computedtomography. Bone 2004; 34: 1044–52PubMedCrossRefGoogle Scholar
  121. 121.
    Bailey DA, McKay HA, Mirwald RL, et al. A six-year longitudinal study of the relationship of physical activityto bone mineral accrual in growing children: the universityof Saskatchewan bone mineral accrual study. J Bone Miner Res 1999; 14 (10): 1672–9PubMedCrossRefGoogle Scholar
  122. 122.
    Bailey DA, Wedge JH, McCulloch RG, et al. Epidemiology of fractures of the distal end of the radius in children asassociated with growth. J Bone Joint Surg 1989; 71 (8): 1225–31PubMedGoogle Scholar
  123. 123.
    Tuchman S, Thayu M, Shults J, et al. Interpretation of biomarkers of bone metabolism in children: impact ofgrowth velocity and body size in healthy children andchronic disease. J Pediatr 2008; 153: 484–90PubMedCrossRefGoogle Scholar
  124. 124.
    Seeman E, Hopper JL, Young NR, et al. Do genetic factors explain associations between muscle strength, lean mass,and bone density? A twin study. Am J Physiol 1996; 270 (33): E320–E7PubMedGoogle Scholar
  125. 125.
    Bonjour JP, Theintz G, Buchs B, et al. Critical years and stages of puberty for spinal and femoral bone mass accumulationduring adolescence. J Clin Endocrinol Metab 1991; 73 (3): 555–63PubMedCrossRefGoogle Scholar
  126. 126.
    Wiksten-Almstromer M, Hirschberg AL, Hagenfeldt K. Reduced bone mineral density in adult women diagnosedwith menstrual disorders during adolescence. Acta Obstet Gynecol Scand 2009; 88 (5): 543–9PubMedCrossRefGoogle Scholar
  127. 127.
    Csermely T, Halvax L, Vizer M, et al. Relationship between adolescent amenorrhea and climacteric osteoporosis. Maturitas 2007 Apr 20; 56 (4): 368–74PubMedCrossRefGoogle Scholar
  128. 128.
    Nicodemus KK, Folsom AR, Anderson KE. Menstrual history and risk of hip fractures in postmenopausalwomen. Am J Epidemiol 2001; 153: 251–5PubMedCrossRefGoogle Scholar
  129. 129.
    Cooper GS, Sandler DP. Long-term effects of reproductive- age menstrual cycle patterns on peri- and postmenopausalfracture risk. Am J Epidemiol 1997; 145 (9): 804–9PubMedCrossRefGoogle Scholar
  130. 130.
    Wyshak G, Frisch RE, Albright TE, et al. Bone fractures among former college athletes compared with nonathletesin the menopausal and postmenopausal years. Obstet Gynecol 1987 Jan; 69 (1): 121–6PubMedGoogle Scholar
  131. 131.
    Vescovi JD, Jamal SA, De Souza MJ. Strategies to reverse bone loss in women with functional hypothalamic amenorrhea:a systematic review of the literature. Osteoporos Int 2008; 19: 465–78PubMedCrossRefGoogle Scholar
  132. 132.
    American Academy of Pediatrics. Committee on Sports Medicine. Amenorrhea in adolescent athletes. Pediatrics 1989 Sep; 84 (2): 394–5Google Scholar
  133. 133.
    Rogol AD. Delayed puberty in girls and primary and secondary amenorrhea. In: Hebestreit H, Bar-Or O, editors. The encyclopaedia of sports medicine: the young athlete. Oxford: Blackwell Publishing, 2008: 227–42Google Scholar
  134. 134.
    Lebrun CM. The female athlete triad: what’s a doctor to do? Curr Sports Med Rep 2007; 6: 397–404PubMedCrossRefGoogle Scholar
  135. 135.
    Jamieson MA. Hormone replacement in the adolescent with anorexia and hypothalamic amenorrhea: yes or no [letter]? J Pediatr Adolesc Gynecol 2001; 14 (1): 39PubMedCrossRefGoogle Scholar
  136. 136.
    Legroux-Gerot I, Vignau J, Collier F, et al. Factors influencing changes in bone mineral density in patients withanorexia nervosa-related osteoporosis: the effect of hormonereplacement therapy. Calcif Tissue Int 2008; 83: 315–23PubMedCrossRefGoogle Scholar
  137. 137.
    Bennell K, White S, Crossley K. The oral contraceptive pill: a revolution for sportswomen? Br J Sports Med 1999 Aug; 33 (4): 231–8PubMedCrossRefGoogle Scholar
  138. 138.
    Rickenlund A, Carlstrom K, Ekblom B, et al. Effects of oral contraceptives on body composition and physicalperformance in female athletes. J Clin Endocrinol Metab 2004; 89 (9): 4364–70PubMedCrossRefGoogle Scholar
  139. 139.
    Castelo-Branco C, Vicente JJ, Pons F, et al. Bone mineral density in young, hypothalamic oligoamenorrheic womentreated with oral contraceptives. J Reprod Med 2001 Oct; 46 (10): 875–9PubMedGoogle Scholar
  140. 140.
    Hergenroeder AC, O’Brian Smith E, Shypailo R, et al. Bone mineral changes in young women with hypothalamicamenorrhea treated with oral contraceptives,medroxyprogesterone, or placebo over 12 months. Am JObstet Gynecol 1997; 176: 1017–25CrossRefGoogle Scholar
  141. 141.
    Braam LA, Knapen MH, Geusens P, et al. Factors affecting bone loss in female endurance athletes: a two-yearfollow-up study. Am J Sports Med 2003 Nov-Dec; 31 (6): 889–95PubMedGoogle Scholar
  142. 142.
    Hind K, Truscott J, Carroll S. Female athlete triad in monozygotic twins. Phys Sportsmed 2009; 36 (1): 119–24CrossRefGoogle Scholar
  143. 143.
    De Cree C, Lewin R, Ostyn M. Suitability of cyproterone acetate in the treatment of osteoporosis associated withathletic amenorrhea. Int J Sports Med 1988 Jun; 9 (3): 187–92PubMedCrossRefGoogle Scholar
  144. 144.
    Martin AD, McCulloch RG. Bone dynamics: stress, strain and fracture. J Sports Sci 1987 Summer; 5 (2): 155–63PubMedCrossRefGoogle Scholar
  145. 145.
    Bennell KL, Malcolm SA, Thomas SA. Risk factors for stress fractures in track and field athletes: a 12 monthprospective study. Am J Sports Med 1996; 24: 810–8PubMedCrossRefGoogle Scholar
  146. 146.
    Winfield AC, Moore J, Bracker M, et al. Risk factors associated with stress reactions in female marines. Mil Med 1997 Oct; 162 (10): 698–702PubMedGoogle Scholar
  147. 147.
    Lappe JM, Cullen D, Haynatzki G, et al. Calcium and vitamin D supplementation decreases incidence of stressfractures in female navy recruits. J Bone Miner Res 2008; 23 (5): 741–9PubMedCrossRefGoogle Scholar
  148. 148.
    Barrow GW, Saha S. Menstrual irregularity and stress fractures in collegiate female distance runners. Am JSports Med 1988 May-Jun; 16 (3): 209–16CrossRefGoogle Scholar
  149. 149.
    Myburgh KH, Hutchins J, Fataar AB, et al. Low bone density is an etiologic factor for stress fractures in athletes. Ann Intern Med 1990 Nov 15; 113 (10): 754–9PubMedGoogle Scholar
  150. 150.
    Heaney RP, Recker RR, Saville PD. Menopausal changes in bone remodeling. J Lab Clin Med 1978; 92 (6): 964–70PubMedGoogle Scholar
  151. 151.
    Hassager C, Colwell A, Assiri AMA, et al. Effect of menopause and hormone replacement therapy on urinaryexcretion of pyridinuim cross-links: a longitudinal andcross-sectional study. Clin Endocrinol 1992; 37: 45–50CrossRefGoogle Scholar
  152. 152.
    Turner RT, Riggs BL, Spelsberg TC. Skeletal effects of estrogen. Endocr Rev 1994; 15: 275–99PubMedGoogle Scholar
  153. 153.
    Popat VB, Calis KA, Vanderhoof VH, et al. Bone mineral density in estrogen-deficient young women. J Clin Endocrinol Metab 2009 Jul; 94 (7): 2277–83PubMedCrossRefGoogle Scholar
  154. 154.
    De Souza MJ, Leidy HJ, O’Donnell E, et al. Fasting ghrelin levels in physically active women: relationship with menstrualdisturbances and metabolic hormones. J Clin Endocrinol Metab 2004 Jul; 89 (7): 3536–42PubMedCrossRefGoogle Scholar
  155. 155.
    Laughlin GA, Yen SS. Nutritional and endocrine-metabolic aberrations in amenorrheic athletes. J Clin Endocrinol Metab 1996 Dec; 81 (12): 4301–9PubMedCrossRefGoogle Scholar
  156. 156.
    Miller KK, Lawson EA, Mathur V, et al. Androgens in women with anorexia nervosa and normal-weight womenwith hypothalamic amenorrhea. J Clin Endocrinol Metab 2007 Apr; 92 (4): 1334–9PubMedCrossRefGoogle Scholar
  157. 157.
    Warren MP, Perlroth NE. The effect of intense exercise on the female reproductive system. J Endocrinol 2001; 170Google Scholar
  158. 158.
    Russell RG. Bisphosphonates: from bench to bedside. Ann N Y Acad Sci 2006 Apr; 1068: 367–401PubMedCrossRefGoogle Scholar
  159. 159.
    Russell RG, Watts NB, Ebetino FH, et al. Mechanisms of action of bisphosphonates: similarities and differencesand their potential influence on clinical efficacy. Osteoporos Int 2008 Jun; 19 (6): 733–59PubMedCrossRefGoogle Scholar
  160. 160.
    Milgrom C, Finestone A, Novack V, et al. The effect of prophylactic treatment with risedronate on stress fractureincidence among infantry recruits. Bone 2004; 35: 418–24PubMedCrossRefGoogle Scholar
  161. 161.
    Stewart GW, Brunet ME, Manning MR, et al. Treatment of stress fractures in athletes with intravenous pamidronate. Clin J Sport Med 2005; 15 (2): 92–4PubMedCrossRefGoogle Scholar
  162. 162.
    Grinspoon S, Baum H, Lee K, et al. Effects of short-term recombinant human insulin-like growth factor I administrationon bone turnover in osteopenic women with anorexianervosa. J Clin Endocrinol Metab 1996 Nov; 81 (11): 3864–70PubMedCrossRefGoogle Scholar
  163. 163.
    Grinspoon S, Thomas L, Miller K, et al. Effects of recombinant human IGF-I and oral contraceptive administrationon bone density in anorexia nervosa. J Clin Endocrinol Metab 2002; 87 (6): 2883–91PubMedCrossRefGoogle Scholar
  164. 164.
    Grinspoon SK, Baum HBA, Peterson S, et al. Effects of rhIGF-I administration on bone turnover during shorttermfasting. J Clin Invest 1995; 96: 900–6PubMedCrossRefGoogle Scholar
  165. 165.
    Miller KK, Grieco KA, Klibanski A. Testosterone administration in women with anorexia nervosa. J Clin Endocrinol Metab 2005; 90: 1428–33PubMedCrossRefGoogle Scholar
  166. 166.
    Gordon CM, Grace E, Emans SJ, et al. Changes in bone turnover markers and menstrual function after shorttermoral DHEA in young women with anorexia nervosa. J Bone Miner Res 1999; 14: 136–45PubMedCrossRefGoogle Scholar
  167. 167.
    Misra M. What is the best strategy to combat low bone mineral density in functional hypothalamic amenorrhea? Nat Clin Pract Endocrinol Metab 2008; 4 (10): 542–3PubMedCrossRefGoogle Scholar
  168. 168.
    Welt CK, Chan JL, Bullen J, et al. Recombinant human leptin in women with hypothalamic amenorrhea. N Engl JMed 2004 Sep 2; 351 (10): 987–97CrossRefGoogle Scholar
  169. 169.
    Holick MF, Chen TC. Vitamin D deficiency: a worldwide problem with health consequences. Am J Clin Nutr 2008; 87 Suppl.: 1080S–6SGoogle Scholar
  170. 170.
    Mithal A, Wahl DA, Bonjour JP, et al. Global vitamin D status and determinants of hypovitaminosis D. Osteoporos Int 2009 Nov; 20 (11): 1807–20PubMedCrossRefGoogle Scholar
  171. 171.
    Holick MF. Vitamin D status: measurement, interpretation, and clinical application. Ann Epidemiol 2009 Feb; 19 (2): 73–8PubMedCrossRefGoogle Scholar
  172. 172.
    Willis KS, Peterson NJ, Larson-Meyer DE. Should we be concerned about the vitamin D status of athletes? Int J Sport Nutr Exerc Metab 2008; 18 (2): 204–24PubMedGoogle Scholar
  173. 173.
    Cannell JJ, Hollis BW, Sorenson MB, et al. Athletic performance and vitamin D. Med Sci Sports Exerc 2009; 41 (5): 1102–10PubMedCrossRefGoogle Scholar
  174. 174.
    Lovell G. Vitamin D status of females in an elite gymnastics program. Clin J Sport Med 2008; 18 (2): 159–61PubMedCrossRefGoogle Scholar
  175. 175.
    Ward KA, Das G, Berry JL, et al. Vitamin D status and muscle function in post-menarchal adolescent girls. J Clin Endocrinol Metab 2009; 94: 559–63PubMedCrossRefGoogle Scholar
  176. 176.
    Misra M. Bone density in the adolescent athlete. Rev Endocr Metab Disord 2008; 9 (2): 139–44PubMedCrossRefGoogle Scholar
  177. 177.
    American Academy of, Committee on Sports. Medical concerns in the female athlete. Pediatrics 2000 Sep; 106 (3): 610–3CrossRefGoogle Scholar
  178. 178.
    Dei M, Seravalli V, Bruni V, et al. Predictors of recovery of ovarian function after weight gain in subjects with amenorrhearelated to restrictive eating disorders. Gynecol Endocrinol 2008 Aug; 24 (8): 459–64PubMedCrossRefGoogle Scholar
  179. 179.
    Bass S, Saxon L, Corral A-M, et al. Near normalisation of lumbar spine bone density in young women recoveredfrom adolescent onset anorexia nervosa: a longitudinalstudy. J Pediatr Endocrinol Metab 2005; 18 (9): 897–907PubMedCrossRefGoogle Scholar
  180. 180.
    Dominguez J, Goodman L, Sen Gupta S, et al. Treatment of anorexia nervosa is associated with increases in bonemineral density, and recovery is a biphasic process involvingboth nutrition and return of menses. Am J Clin Nutr 2007; 86: 92–9PubMedGoogle Scholar
  181. 181.
    Miller KK, Lee EE, Lawson EA, et al. Determinants of skeletal loss and recovery in anorexia nervosa. J Clin Endocrinol Metab 2006 Aug; 91 (8): 2931–7PubMedCrossRefGoogle Scholar
  182. 182.
    Misra M, Prabhakaran R, Miller KK, et al. Weight gain and restoration of menses as predictors of bone mineraldensity change in adolescent girls with anorexia nervosa-1. J Clin Endocrinol Metab 2008; 93 (4): 1231–7PubMedCrossRefGoogle Scholar
  183. 183.
    Viapiana O, Gatti D, Dalle Grave R, et al. Marked increases in bone mineral density and biochemical markersof bone turnover in patients with anorexia nervosa gainingweight. Bone 2007; 40 (4): 1073–7PubMedCrossRefGoogle Scholar
  184. 184.
    Bolton JG, Patel S, Lacey JH, et al. A prospective study of changes in bone turnover and bone density associatedwith regaining weight in women with anorexia nervosa. Osteoporos Int 2005 Dec; 16 (12): 1955–62PubMedCrossRefGoogle Scholar
  185. 185.
    Jonnavithula S, Warren MP, Fox RP, et al. Bone density is compromised in amenorrheic women despite return ofmenses: a 2-year study. Obstet Gynecol 1993 May; 81 (5Pt1): 669–74PubMedGoogle Scholar
  186. 186.
    Drinkwater BL, Nilson K, Ott S, et al. Bone mineral density after resumption of menses in amenorrheic athletes. JAMA 1986 Jul 18; 256 (3): 380–2PubMedCrossRefGoogle Scholar
  187. 187.
    Kopp-Woodroffe SA, Manore MM, Dueck CA, et al. Energy and nutrient status of amenorrheic athletes participatingin a diet and exercise training intervention program. Int J Sport Nutr 1999 Mar; 9 (1): 70–88PubMedGoogle Scholar
  188. 188.
    Lindberg JS, Powell MR, Hunt MM, et al. Increased vertebral bone mineral in response to reduced exercise inamenorrheic runners. West JMed 1987 Jan; 146 (1): 39–42Google Scholar
  189. 189.
    Williams NI, Caston-Balderrama AL, Helmreich DL, et al. Longitudinal changes in reproductive hormones andmenstrual cyclicity in cynomolgus monkeys during strenuousexercise training: abrupt transition to exerciseinducedamenorrhea. Endocrinology 2001; 142 (6): 2381–9PubMedCrossRefGoogle Scholar
  190. 190.
    Martyn-St James M, Carroll S. Progressive high-intensity resistance training and bone mineral density changesamong premenopausal women evidence of discordant sitespecificskeletal effects. Sports Med 2006; 36 (8): 683–704PubMedCrossRefGoogle Scholar
  191. 191.
    Lohman T, Going S, Going S, et al. Effects of resistance training on regional and total bone mineral density inpremenopausal women: a randomized prospective study. J Bone Miner Res 1995; 10 (7): 1015–24PubMedCrossRefGoogle Scholar
  192. 192.
    Nickols-Richardson SM, Miller LE, Wootten DF, et al. Concentric and eccentric isokinetic resistance training similarlyincreases muscular strength, fat-free soft tissuemass, and specific bone mineral measurements in youngwomen. Osteoporos Int 2007; 18: 789–96PubMedCrossRefGoogle Scholar
  193. 193.
    del Valle MF, Perez M, Santana-Sosa E, et al. Does resistance training improve the functional capacity and wellbeing of very young anorexic patients? A randomizedcontrolled trial. J Adolesc Health 2010 Apr; 46 (4): 352–8PubMedCrossRefGoogle Scholar
  194. 194.
    Beumont PJ, Arthur B, Russell JD, et al. Excessive physical activity in dieting disorder patients: proposals for a supervisedexercise program. Int J Eat Disord 1994 Jan; 15 (1): 21–36PubMedCrossRefGoogle Scholar
  195. 195.
    Chantler I, Szabo CP, Green K. Muscular strength changes in hospitalized anorexic patients after an eight week resistancetraining program. Int J Sports Med 2006 Aug; 27 (8): 660–5PubMedCrossRefGoogle Scholar
  196. 196.
    Szabo CP, Green K. Hospitalized anorexics and resistance training: impact on body composition and psychologicalwell-being — a preliminary study. Eat Weight Disord 2002 Dec; 7 (4): 293–7PubMedGoogle Scholar
  197. 197.
    Thien V, Thomas A, Markin D, et al. Pilot study of a graded exercise program for the treatment of anorexia nervosa. Int J Eat Disord 2000 Jul; 28 (1): 101–6PubMedCrossRefGoogle Scholar
  198. 198.
    Chilibeck PD, Calder A, Sale DG, et al. Twenty weeks of weight training increases lean tissue mass but not bonemineral mass or density in healthy, active young women. Can J Physiol Pharmacol 1996; 74 (10): 1180–5PubMedCrossRefGoogle Scholar
  199. 199.
    Sinaki M, Wahner H, Bergstrahl E, et al. Three-year randomized trial of the effect of dose-specified loading andstrengthening exercises on bone mineral density of spineand femur in nonathletic, physically active women. Bone 1996; 19: 233–44PubMedCrossRefGoogle Scholar
  200. 200.
    Heinonen A, Sievänen H, Kannus P, et al. High-impact exercise and bones of growing girls: a 9-month controlledtrial. Osteoporos Int 2000; 11 (12): 1010–7PubMedCrossRefGoogle Scholar
  201. 201.
    MacKelvie KJ, McKay HA, Khan KM, et al. A schoolbased exercise intervention augments bone mineral accrualin early pubertal girls. J Pediatr 2001; 139 (4): 501–8PubMedCrossRefGoogle Scholar
  202. 202.
    Bassey EJ, Ramsdale SJ. Increase in femoral bone density in young women following high-impact exercise. Osteoporos Int 1994 Mar; 4 (2): 72–5PubMedCrossRefGoogle Scholar
  203. 203.
    Heinonen A, Kannus P, Sievänen H, et al. Randomised controlled trial of effect of high-impact exercise on selectedrisk factors for osteoporotic fractures. Lancet 1996; 348 (9038): 1343–7PubMedCrossRefGoogle Scholar
  204. 204.
    Warden SJ, Bogenschutz ED, Smith HD, et al. Throwing induces substantial torsional adaptation within the midshafthumerus of male baseball players. Bone 2009 Nov; 45 (5): 931–41PubMedCrossRefGoogle Scholar
  205. 205.
    Friedlander AL, Genant HK, Sadowsky S, et al. A twoyear program of aerobics and weight training enhancesbone mineral density of young women. J Bone Miner Res 1995; 10 (4): 574–85PubMedCrossRefGoogle Scholar
  206. 206.
    Lee K, Jessop H, Suswillo R, et al. Bone adaptation requires oestrogen receptor-alpha. Nature 2003 Jul 24; 424 (6947): 389PubMedCrossRefGoogle Scholar
  207. 207.
    Warden SJ, Burr DB, Brukner PD. Stress fractures: pathophysiology, epidemiology, and risk factors. Curr Osteoporos Rep 2006 Sep; 4 (3): 103–9PubMedCrossRefGoogle Scholar
  208. 208.
    Feingold D, Hame SL. Female athlete triad and stress fractures. Orthop Clin North Am 2006; 37 (4): 575–83PubMedCrossRefGoogle Scholar
  209. 209.
    Loud KJ, Micheli LJ, Bristol S, et al. Family history predicts stress fracture in active female adolescents. Pediatrics 2007 Aug; 120 (2): e364–72CrossRefGoogle Scholar
  210. 210.
    Valimaki VV, Afthan H, Lehmuskallio E, et al. Risk factors for clinical stress fractures in male military recruits: aprospective cohort study. Bone 2005; 37 (2): 267–73PubMedCrossRefGoogle Scholar
  211. 211.
    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: 754–9PubMedGoogle Scholar
  212. 212.
    Carbon R, Sambrook PN, Deakin V, et al. Bone density of elite female athletes with stress fractures. Med J Aust 1990; 153 (7): 373–6PubMedGoogle Scholar
  213. 213.
    Giladi M, Milgrom C, Simkin A, et al. Stress fractures: identifiable risk factors. Am J Sports Med 1991; 19: 647–52PubMedCrossRefGoogle Scholar
  214. 214.
    Grimston SK, Engsberg JR, Kloiber R. Bone mass, external loads, and stress fracture in female runners. J Appl Biomech 1991; 7 (3): 293–302Google Scholar
  215. 215.
    Korpelainen R, Orava S, Karpakka J, et al. Risk factors for recurrent stress fractures in athletes. Am J Sports Med 2001; 29 (3): 304–10PubMedGoogle Scholar
  216. 216.
    Evans RK, Negus C, Antczak AJ, et al. Sex differences in parameters of bone strength in new recruits: beyondbone density. Med Sci Sports Exerc 2008; 40 (11 Suppl.): S645–S53PubMedGoogle Scholar
  217. 217.
    Beck TJ, Ruff CB, Mourtada FA, et al. Dual-energy X-ray absorptiometry derived structural geometry for stressfracture prediction in male US Marine Corps recruits. J Bone Miner Res 1996; 11 (5): 645–53PubMedCrossRefGoogle Scholar
  218. 218.
    Milgrom C, Giladi M, Simkin A, et al. The area moment of inertia of the tibia: a risk factor for stress fractures. J Biomech 1989; 22: 1243–8PubMedCrossRefGoogle Scholar
  219. 219.
    Crossley K, Bennell K, Wrigley T, et al. Ground reaction forces, bone characteristics, and tibial stress fracture inmale runners. Med Sci Sports Exerc 1999; 31 (8): 1088–93PubMedCrossRefGoogle Scholar
  220. 220.
    Franklyn M, Oakes BW, Field B, et al. Section modulus is the optimum geometric predictor for stress fractures andmedial tibial stress syndrome in both male and femaleathletes. Am J Sports Med 2008; 36 (6): 1179–89PubMedCrossRefGoogle Scholar
  221. 221.
    Tommasini SM, Nasser P, Schaffler MB, et al. Relationship between bone morphology and bone quality in maletibias: implications for stress fracture risk. J Bone Miner Res 2005; 20: 1372–80PubMedCrossRefGoogle Scholar
  222. 222.
    Milgrom C, Radeva-Petrova DR, Finestone A, et al. The effect of muscle fatigue on in vivo tibial strains. J Biomech 2007; 40: 845–50PubMedCrossRefGoogle Scholar
  223. 223.
    Prouteau S, Ducher G, Nanyan P, et al. Fractal analysis of bone texture: a screening tool for stress fracture risk? Eur J Clin Invest 2004; 34 (2): 137–42PubMedCrossRefGoogle Scholar
  224. 224.
    Knobloch K, Schreibmueller L, Jagodzinski M, et al. Rapid rehabilitation programme following sacral stressfracture in a long-distance running female athlete. Arch Orthop Trauma Surg 2007; 127: 809–13PubMedCrossRefGoogle Scholar
  225. 225.
    Fredericson M, Ngo J, Cobb K. Effects of ball sports on future risk of stress fracture in runners. Clin J Sport Med 2005; 15 (3): 136–41PubMedCrossRefGoogle Scholar

Copyright information

© Adis Data Information BV 2011

Authors and Affiliations

  • Gaele Ducher
    • 1
    • 2
  • Anne I. Turner
    • 1
  • Sonja Kukuljan
    • 1
  • Kathleen J. Pantano
    • 3
  • Jennifer L. Carlson
    • 4
  • Nancy I. Williams
    • 2
  • Mary Jane De Souza
    • 2
  1. 1.Centre for Physical Activity and Nutrition Research, School of Exercise and Nutrition SciencesDeakin UniversityBurwoodAustralia
  2. 2.123 Noll Laboratory, Department of KinesiologyPennsylvania State University, State CollegeUniversity ParkUSA
  3. 3.Physical Therapy Program, Department of Health SciencesCleveland State UniversityClevelandUSA
  4. 4.Division of Adolescent Medicine, Department of PediatricsLucile Packard Children’s Hospital at StanfordPalo AltoUSA

Personalised recommendations