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Sports Medicine

, Volume 28, Issue 2, pp 91–122 | Cite as

Risk Factors for Stress Fractures

  • Kim Bennell
  • Gordon Matheson
  • Willem Meeuwisse
  • Peter Brukner
Review Article

Abstract

Preventing stress fractures requires knowledge of the risk factors that predispose to this injury. The aetiology of stress fractures is multifactorial, but methodological limitations and expediency often lead to research study designs that evaluate individual risk factors. Intrinsic risk factors include mechanical factors such as bone density, skeletal alignment and body size and composition, physiological factors such as bone turnover rate, flexibility, and muscular strength and endurance, as well as hormonal and nutritional factors. Extrinsic risk factors include mechanical factors such as surface, footwear and external loading as well as physical training parameters. Psychological traits may also play a role in increasing stress fracture risk. Equally important to these types of analyses of individual risk factors is the integration of information to produce a composite picture of risk.

The purpose of this paper is to critically appraise the existing literature by evaluating study design and quality, in order to provide a current synopsis of the known scientific information related to stress fracture risk factors. The literature is not fully complete with well conducted studies on this topic, but a great deal of information has accumulated over the past 20 years. Although stress fractures result from repeated loading, the exact contribution of training factors (volume, intensity, surface) has not been clearly established. From what we do know, menstrual disturbances, caloric restriction, lower bone density, muscle weakness and leg length differences are risk factors for stress fracture.Other time-honoured risk factors such as lower extremity alignment have not been shown to be causative even though anecdotal evidence indicates they are likely to play an important role in stress fracture pathogenesis.

Keywords

Adis International Limited Stress Fracture Female Athlete Overuse Injury Ballet Dancer 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    McBryde AM. Stress fractures in runners. Clin Sports Med 1985; 4: 737–52PubMedGoogle Scholar
  2. 2.
    Lysens RJ, de Weerdt W, Nieuwboer A. Factors associated with injury proneness. Sports Med 1991; 12: 281–9PubMedCrossRefGoogle Scholar
  3. 3.
    Meeuwisse WH. Athletic injury etiology: distinguishing between interaction and confounding. Clin J Sport Med 1994; 4: 171–5CrossRefGoogle Scholar
  4. 4.
    Lanyon LE, Hampson WGJ, Goodship AE, et al. Bone deformation recorded in vivo from strain gauges attached to the human tibial shaft. Acta Orthop Scand 1975; 46: 256–68PubMedCrossRefGoogle Scholar
  5. 5.
    Burr DB, Milgrom C, Fyhrie D, et al. In vivo measurement of human tibial strains during vigorous activity. Bone 1996; 18: 405–10PubMedCrossRefGoogle Scholar
  6. 6.
    Ekenman I, Halvorsen K, Westblad P, et al. Local bone deformation at two predominant sites for stress fractures of the tibia: an in vivo study. Foot Ankle Int 1998; 19: 479–84PubMedGoogle Scholar
  7. 7.
    Milgrom C, Burr D, Fyhrie D, et al. Acomparison of the effect of shoes in human tibial axial strains recorded during dynamic loading. Foot Ankle Int 1998; 19: 85–90PubMedGoogle Scholar
  8. 8.
    Carter DR. Anisotropic analysis of strain rosette information from cortical bone. J Biomech 1978; 11: 199–202PubMedCrossRefGoogle Scholar
  9. 9.
    Alho A, Husby T, Hoiseth A. Bone mineral content andmechanical strength: an ex vivo study on human femora at autopsy. Clin Orthop Relat Res 1986; 227: 292–7Google Scholar
  10. 10.
    Carter DR, Hayes WC. The compressive behavior of bone as a two-phase porous structure. J Bone Joint Surg Am 1977; 59: 954–62PubMedGoogle Scholar
  11. 11.
    Hayes WC, Gerhart TN. Biomechanics of bone: applications for assessment of bone strength. In: Peck WA, editor. Bone and Mineral Research/3. New York: Elsevier Science, 1985: 259–94Google Scholar
  12. 12.
    Nordin M, Frankel VH. Basic biomechanics of the musculoskeletal system. 2nd ed. Philadelphia: Lea and Febiger, 1989Google Scholar
  13. 13.
    Einhorn TA. Biomechanics of bone. In: Bilezikian JP, Raisz LG, Rodan GA, editors. Principles of bone biology. San Diego: Academic Press, 1996: 25–37Google Scholar
  14. 14.
    Nordsletten L, Ekeland A. Muscle contraction increases the structural capacity of the lower leg: an in vivo study in the rat. J Orthop Res 1993; 11: 299–304PubMedCrossRefGoogle Scholar
  15. 15.
    Nordsletten L, Kaastad TS, Obrant KJ, et al. Muscle contraction increases the in vivo structural strength to the same degree in osteopenic and normal rat tibiae. J Bone Miner Res 1994; 9: 679–85PubMedCrossRefGoogle Scholar
  16. 16.
    Yoshikawa T, Mori S, Santiesteban AJ, et al. The effects of muscle fatigue on bone strain. J Exp Biol 1994; 188: 217–33PubMedGoogle Scholar
  17. 17.
    Morris FL, Naughton GA, Gibbs JL, et al. Prospective tenmonth exercise intervention in premenarcheal girls: positive effects on bone and lean mass. J Bone Miner Res 1997; 12: 1453–62PubMedCrossRefGoogle Scholar
  18. 18.
    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
  19. 19.
    Carter DR, Hayes WC. Compact bone fatigue damage 1: residual strength and stiffness. J Biomech 1977; 10: 325–37PubMedCrossRefGoogle Scholar
  20. 20.
    Burr DB, Martin RB, Schaffler MB, et al. Bone remodeling in response to in vivo fatigue microdamage. J Biomech 1985; 18: 189–200PubMedCrossRefGoogle Scholar
  21. 21.
    Forwood MR, Parker AW. Microdamage in response to repetitive torsional loading in the rat tibia. Calcif Tiss Int 1989; 45: 47–53CrossRefGoogle Scholar
  22. 22.
    Schaffler MB, Radin EL, Burr DB. Mechanical and morphological effects of strain rate on fatigue of compact bone. Bone 1989; 10: 207–14PubMedCrossRefGoogle Scholar
  23. 23.
    Schaffler MB, Radin EL, Burr DB. Long-term fatigue behavior of compact bone at lowstrain magnitude and rate. Bone 1990; 11: 321–6PubMedCrossRefGoogle Scholar
  24. 24.
    Mori S, Burr DB. Increased intracortical remodeling following fatigue damage. Bone 1993; 14: 103–9PubMedCrossRefGoogle Scholar
  25. 25.
    Frost HM. Transient-steady state phenomena in microdamage physiology: a proposed algorithm for lamellar bone. Calcif Tiss Int 1989; 44: 367–81CrossRefGoogle Scholar
  26. 26.
    Roub LW, Gumerman LW, Hanley EN, et al. Bone stress: a radionuclide imaging perspective. Radiology 1979; 132: 431–8PubMedGoogle Scholar
  27. 27.
    Li G, Zhang S, Chen G, et al. Radiographic and histologic analyses of stress fracture in rabbit tibias. Am J SportsMed 1985; 13: 285–94CrossRefGoogle Scholar
  28. 28.
    Straus FH. Marching fractures of metatarsal bones with a report of the pathology. Surg Gynecol Obstet 1932; 54: 581–4Google Scholar
  29. 29.
    Burrows HJ. Fatigue infraction of the middle of the tibia in ballet dancers. J Bone Joint Surg 1956; 38: 83–94Google Scholar
  30. 30.
    Johnson LC, Stradford HT, Geis RW, et al. Histogenesis of stress fractures. J Bone Joint Surg 1963; 45: 1542Google Scholar
  31. 31.
    Michael RH, Holder LE. The soleus syndrome: a cause of medial tibial stress (shin splints). Am J Sports Med 1985; 13: 87–94PubMedCrossRefGoogle Scholar
  32. 32.
    Carter DR, Caler WE, Spengler DM, et al. Uniaxial fatigue of human cortical bone: the influence of tissue physical characteristics. J Biomech 1981; 14: 461–70PubMedCrossRefGoogle Scholar
  33. 33.
    Cummings SR, Black DM, Nevitt MC, et al. Bone density at various sites for prediction of hip fractures. Lancet 1993; 341: 72–5PubMedCrossRefGoogle Scholar
  34. 34.
    Melton LJ, Atkinson EJ, O’Fallon WM, et al. Long-term fracture prediction by bone mineral assessed at different skeletal sites. J Bone Miner Res 1993; 8: 1227–33PubMedCrossRefGoogle Scholar
  35. 35.
    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
  36. 36.
    Brukner PD, Bennell KL. Stress fractures. Crit Rev Phys Rehabil Med 1997; 9: 151–90Google Scholar
  37. 37.
    Bennell KL, Malcolm SA, Wark JD, et al. Skeletal effects of menstrual disturbances in athletes. Scand J Sci Med Sport 1997; 7: 261–73CrossRefGoogle Scholar
  38. 38.
    Giladi M, Milgrom C, Simkin A, et al. Stress fractures: identifiable risk factors. Am J Sports Med 1991; 19: 647–52PubMedCrossRefGoogle Scholar
  39. 39.
    Beck TJ, Ruff CB, Mourtada FA, et al. Dual-energy x-ray absorptiomety derived structural geometry for stress fracture prediction in male US marine corps recruits. J Bone Miner Res 1996; 11: 645–53PubMedCrossRefGoogle Scholar
  40. 40.
    Bennell KL, Malcolm SA, Thomas SA, et al. Risk factors for stress fractures in track and field athletes: a 12 month prospective study. Am J Sports Med 1996; 24: 810–8PubMedCrossRefGoogle Scholar
  41. 41.
    Pouilles JM, Bernard J, Tremollieres F, et al. Femoral bone density in young male adultswith stress fractures. Bone 1989; 10: 105–8PubMedCrossRefGoogle Scholar
  42. 42.
    Carbon R, Sambrook PN, Deakin V, et al. Bone density of elite female athletes with stress fractures. Med J Aust 1990; 153: 373–6PubMedGoogle Scholar
  43. 43.
    Frusztajer NT, Dhuper S, Warren MP, et al. Nutrition and the incidence of stress fractures in ballet dancers. Am J Clin Nutr 1990; 51: 779–83PubMedGoogle Scholar
  44. 44.
    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
  45. 45.
    Grimston SK, Engsberg JR, Kloiber R, et al. Bone mass, external loads, and stress fractures in female runners. Int J Sport Biomech 1991; 7: 293–302Google Scholar
  46. 46.
    Bennell KL, Malcolm SA, Thomas SA, et al. Risk factors for stress fractures in female track-and-field athletes: a retrospective analysis. Clin J Sport Med 1995; 5: 229–35PubMedCrossRefGoogle Scholar
  47. 47.
    Cline AD, Jansen GR, Melby CL. Stress fractures in female army recruits: implications of bone density, calcium intake, and exercise. J Am Coll Nutr 1998; 17: 128–35PubMedGoogle Scholar
  48. 48.
    Crossley K, Bennell KL, Wrigley T, et al. Ground reaction forces, bone characteristics and tibial stress fracture in male runners. Med Sci Sports Exerc 1999. In pressGoogle Scholar
  49. 49.
    Miller GJ, Purkey WW. The geometric properties of paired human tibiae. J Biomech 1980; 13: 1–8PubMedCrossRefGoogle Scholar
  50. 50.
    Martens M, Van Auderkerke R, de Meester P, et al. The geometrical properties of human femur and tibia and their importance for the mechanical behaviour of these bone structures. Acta Orthop Traumatic Surg 1981; 98: 113–20CrossRefGoogle Scholar
  51. 51.
    Giladi M, Milgrom C, Simkin A, et al. Stress fractures and tibial bone width: a risk factor. J Bone Joint Surg Br 1987; 69: 326–9PubMedGoogle Scholar
  52. 52.
    Milgrom C, Giladi M, Simkin A, et al. An analysis of the biomechanical mechanismof tibial stress fractures among Israeli infantry recruits. Clin Orthop Relat Res 1988; 231: 216–21PubMedGoogle Scholar
  53. 53.
    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
  54. 54.
    Friberg O. Leg length asymmetry in stress fractures: a clinical and radiological study. J Sports Med 1982; 22: 485–8Google Scholar
  55. 55.
    Giladi M, Milgrom C, Stein M, et al. The low arch, a protective factor in stress fractures: a prospective study of 295 military recruits. Orthop Rev 1985; 14: 709–12Google Scholar
  56. 56.
    Giladi M, Milgrom C, Stein M, et al. External rotation of the hip: a predictor of risk for stress fractures. Clin Orthop Relat Res 1987; 216: 131–4PubMedGoogle Scholar
  57. 57.
    Montgomery LC, Nelson FRT, Norton JP, et al. Orthopaedic history and examination in the etiology of overuse injuries. Med Sci Sports Exerc 1989; 21: 237–43PubMedGoogle Scholar
  58. 58.
    Simkin A, Leichter I, Giladi M, et al. Combined effect of foot arch structure and an orthotic device on stress fractures. Foot Ankle 1989; 10: 25–9PubMedGoogle Scholar
  59. 59.
    Milgrom C, Finestone A, Shlamkovitch N, et al. Youth is a risk factor for stress fracture: a study of 783 infantry recruits. J Bone Joint Surg Br 1994; 76: 20–2PubMedGoogle Scholar
  60. 60.
    Cowan DN, Jones BH, Frykman PN, et al. Lower limbmorphology and risk of overuse injury among male infantry trainees. Med Sci Sports Exerc 1996; 28: 945–52PubMedCrossRefGoogle Scholar
  61. 61.
    Winfield AC, Bracker M, Moore J, et al. Risk factors associated with stress reactions in female marines. Mil Med 1997; 162: 698–702PubMedGoogle Scholar
  62. 62.
    Hughes LY. Biomechanical analysis of the foot and ankle for predisposition to developing stress fractures. J Orthop Sport Phys Ther 1985; 7: 96–101Google Scholar
  63. 63.
    Brunet ME, Cook SD, Brinker MR, et al. A survey of running injuries in 1505 competitive and recreational runners. J Sports Med Phys Fitness 1990; 30: 307–15PubMedGoogle Scholar
  64. 64.
    Brosh T, Arcan M. Toward early detection of the tendency to stress fractures. Clin Biomech 1994; 9: 111–6CrossRefGoogle Scholar
  65. 65.
    Ekenman I, Tsai-Fellander L, Westblad P, et al. A study of intrinsic factors in patientswith stress fractures of the tibia. Foot Ankle Int 1996; 17: 477–82PubMedGoogle Scholar
  66. 66.
    Matheson GO, Clement DB, McKenzie DC, et al. Stress fractures in athletes: a study of 320 cases. Am J Sports Med 1987; 15: 46–58PubMedCrossRefGoogle Scholar
  67. 67.
    Taunton JE, Clement DB, Webber D. Lower extremity stress fractures in athletes. Physician Sports Med 1981; 9: 77–86Google Scholar
  68. 68.
    Sullivan D, Warren RF, Pavlov H, et al. Stress fractures in 51 runners. Clin Orthop Relat Res 1984; 187: 188–92PubMedGoogle Scholar
  69. 69.
    D’Amico JC, Dinowitz HD, Polchaninoff M. Limb length discrepancy: an electrodynographic analysis. J Am Podiatr Med Assoc 1985; 75: 639–43PubMedGoogle Scholar
  70. 70.
    Frederick EC, Hagy JL. Factors affecting peak vertical ground reaction forces in running. Int J Sport Biomech 1986; 2: 41–9Google Scholar
  71. 71.
    Lloyd T, Triantafyllou SJ, Baker ER, et al. Women athletes with menstrual irregularity have increased musculoskeletal injuries. Med Sci Sports Exerc 1986; 18: 374–9PubMedGoogle Scholar
  72. 72.
    Warren MP, Brooks-Gunn J, Hamilton LH, et al. Scoliosis and fractures in young ballet dancers. N Engl J Med 1986; 314: 1348–53PubMedCrossRefGoogle Scholar
  73. 73.
    Barrow GW, Saha S. Menstrual irregularity and stress fractures in collegiate female distance runners. Am J Sports Med 1988; 16: 209–16PubMedCrossRefGoogle Scholar
  74. 74.
    Kadel NJ, Teitz CC, Kronmal RA. Stress fractures in ballet dancers. Am J Sports Med 1992; 20: 445–9PubMedCrossRefGoogle Scholar
  75. 75.
    Taimela S, Kujala UM, Dahlstrom S, et al. Risk factors for stress fractures during physical training programs. Clin J SportMed 1992; 2: 105–8CrossRefGoogle Scholar
  76. 76.
    Murguia MJ, Vailas A, Mandelbaum B, et al. Elevated plasma hydroxyproline: a possible risk factor associatedwith connective tissue injuries during overuse. Am J Sports Med 1988; 16: 660–4PubMedCrossRefGoogle Scholar
  77. 77.
    Bennell KL, Malcolm SA, Brukner PD, et al. A 12-month prospective study of the relationship between stress fractures and bone turnover in athletes. Calcif Tiss Int 1998; 63: 80–5CrossRefGoogle Scholar
  78. 78.
    Stanitski CL, McMaster JH, Scranton PE. On the nature of stress fractures. Am J Sports Med 1978; 6: 391–6PubMedCrossRefGoogle Scholar
  79. 79.
    Meyer SA, Saltzman CL, Albright JP. Stress fractures of the foot and leg. Clin Sports Med 1993; 12: 395–413PubMedGoogle Scholar
  80. 80.
    Voloshin A, Wosk J. An in vivo study of lowback pain and shock absorption in the human locomotor system. J Biomech 1982; 15: 21–7PubMedCrossRefGoogle Scholar
  81. 81.
    Cavanagh PR, LaFortune MA. Ground reaction forces in distance running. J Biomech 1980; 13: 397–406PubMedCrossRefGoogle Scholar
  82. 82.
    Bates BT, Osternig LR, Sawhill JA. An assessment of subject variability, subject-shoe interaction, and the evaluation of running shoes using ground reaction force data. J Biomech 1983; 16: 181–91PubMedCrossRefGoogle Scholar
  83. 83.
    McNitt-Gray J. Kinematics and impulse characteristics of drop landings from three heights. Int J Sports Biomech 1991; 7: 201–23Google Scholar
  84. 84.
    Paul IL, Munro MB, Abernethy PJ, et al. Musculo-skeletal shock absorption: relative contribution of bone and soft tissues at various frequencies. J Biomech 1978; 11: 237–9PubMedCrossRefGoogle Scholar
  85. 85.
    Clement DB. Tibial stress syndrome in athletes. J Sports Med 1975; 2: 81–5Google Scholar
  86. 86.
    Benazzo F, Barnabei G, Ferrario A, et al. Stress fractures in track and field athletes. J Sports Traumatol Rel Res 1992; 14: 51–65Google Scholar
  87. 87.
    Milgrom C. The Israeli elite infantry recruit: a model for understanding the biomechanics of stress fractures. J R Coll Surg Edinb 1989; 34 (6 Suppl.): S18–22PubMedGoogle Scholar
  88. 88.
    Scott SH, Winter DA. Internal forces at chronic running injury sites. Med Sci Sports Exerc 1990; 22: 357–69PubMedGoogle Scholar
  89. 89.
    Hoffman JR, Chapnik L, Shamis A, et al. The effect of leg strength on the incidence of lower extremity overuse injuries during military training. Mil Med 1999; 164: 153–6PubMedGoogle Scholar
  90. 90.
    Grimston SK, Nigg BM, Fisher V, et al. External loads throughout a 45 minute run in stress fracture and non-stress fracture runners [abstract]. J Biomech 1994; 27: 668CrossRefGoogle Scholar
  91. 91.
    Malina RM, Spriduso WW, Tate C, et al. Age at menarche and selected menstrual characteristics in athletes at different competitive levels and in different sports. Med Sci Sports Exerc 1978; 10: 218–22Google Scholar
  92. 92.
    Kaiserauer S, Snyder AC, Sleeper M, et al. Nutritional, physiological, and menstrual status of distance runners. Med Sci Sports Exerc 1989; 21: 120–5PubMedGoogle Scholar
  93. 93.
    Nattiv A, Puffer JC, Green GA. Lifestyles and health risks of collegiate athletes: a multi-center study. Clin J Sport Med 1997; 7: 262–72PubMedCrossRefGoogle Scholar
  94. 94.
    Wolman RL, Harries MG. Menstrual abnormalities in elite athletes. Clin Sports Med 1989; 1: 95–100Google Scholar
  95. 95.
    Drinkwater BL, Nilson K, Chesnut III CH, et al. Bone mineral content of amenorrheic and eumenorrheic athletes. N Engl J Med 1984; 5: 277–81CrossRefGoogle Scholar
  96. 96.
    Rutherford OM. Spine and total body bone mineral density in amenorrheic endurance athletes. J Appl Physiol 1993; 74: 2904–8PubMedGoogle Scholar
  97. 97.
    Micklesfield LK, Lambert EV, Fataar AB, et al. Bone mineral density in mature, premenopausal ultramarathon runners. Med Sci Sports Exerc 1995; 27: 688–96PubMedGoogle Scholar
  98. 98.
    Tomten SE, Falch JA, Birkeland KI, et al. Bone mineral density and menstrual irregularities: a comparative study on cortical and trabecular bone structures in runners with alleged normal eating behaviour. Int J Sports Med 1998; 19: 92–7PubMedCrossRefGoogle Scholar
  99. 99.
    Beitins IZ, McArthur JW, Turnbull BA, et al. Exercise induces two types of human luteal dysfunction: confirmation by urinary free progesterone. J Clin Endocrinol Metab 1991; 72: 1350–8PubMedCrossRefGoogle Scholar
  100. 100.
    Prior JC, Vigna YM. Ovulation disturbances and exercise training. Clin Obstet Gynecol 1991; 34: 180–90PubMedCrossRefGoogle Scholar
  101. 101.
    Snow GR, Anderson C. The effects of continuous progestogen treatment on cortical bone remodelling activity in beagles. Calcif Tiss Int 1985; 37: 282–6CrossRefGoogle Scholar
  102. 102.
    Karambolova KK, Snow GR, Anderson C. Surface activity on the periosteal and corticoendosteal envelopes following continuous progestogen supplementation in spayed beagles. Calcif Tiss Int 1986; 38: 239–43CrossRefGoogle Scholar
  103. 103.
    Snow GR, Anderson C. The effects of 17β-estradiol and progestagen on trabecular bone remodeling in oophorectomized dogs. Calcif Tiss Int 1986; 39: 198–205CrossRefGoogle Scholar
  104. 104.
    Prior JC, Vigna YM, Schechter MT, et al. Spinal bone loss and ovulatory disturbances. N Engl J Med 1990; 323: 1221–7PubMedCrossRefGoogle Scholar
  105. 105.
    Snead DB, Weltman A, Weltman JY, et al. Reproductive hormones and bone mineral density in women runners. J Appl Physiol 1992; 72: 2149–56PubMedCrossRefGoogle Scholar
  106. 106.
    Barr SI, Prior JC, Vigna YM. Restrained eating and ovulatory disturbances: possible implications for bone health. AmJ Clin Nutr 1994; 59: 92–7Google Scholar
  107. 107.
    Nelson ME, Clark N, Otradovec C, et al. Elite women runners: association between menstrual status, weight history and stress fractures [abstract]. Med Sci Sports Exerc 1987; 19: S13Google Scholar
  108. 108.
    Clark N, Nelson M, Evans W. Nutrition education for elite female runners. Physician Sports Med 1988; 16: 124–36Google Scholar
  109. 109.
    Lindberg JS, Fears WB, Hunt MM, et al. Exercise-induced amenorrhea and bone density. Ann Intern Med 1984; 101: 647–8PubMedGoogle Scholar
  110. 110.
    Marcus R, Cann C, Madvig P, et al. Menstrual function and bone mass in elite women distance runners. Ann Intern Med 1985; 102: 158–63PubMedGoogle Scholar
  111. 111.
    Cook SD, Harding AF, Thomas KA, et al. Trabecular bone density and menstrual function in women runners. Am J Sports Med 1987; 15: 503–7PubMedCrossRefGoogle Scholar
  112. 112.
    Warren MP, Brooks-Gunn J, Fox RP, et al. Lack of bone accretion and amenorrhea: evidence for a relative osteopenia in weight bearing bones. J Clin Endocrinol Metab 1991; 72: 847–53PubMedCrossRefGoogle Scholar
  113. 113.
    Grimston SK, Engsberg JR, Kloiber R, et al. Menstrual, calcium, and training history: relationship to bone health in female runners. Clin Sports Med 1990; 2: 119–28Google Scholar
  114. 114.
    Guler F, Hascelik Z. Menstrual dysfunction rate and delayed menarche in top athletes of team games. Sports Med Train Rehabil 1993; 4: 99–106CrossRefGoogle Scholar
  115. 115.
    MacDougall JD, Webber CE, Martin J, et al. Relationship among running mileage, bone density, and serumtestosterone in male runners. J Appl Physiol 1992; 73: 1165–70PubMedGoogle Scholar
  116. 116.
    Hetland ML, Haarbo J, Christiansen C. Low bone mass and high bone turnover in male long distance runners. J Clin Endocrinol Metab 1993; 77: 770–5PubMedCrossRefGoogle Scholar
  117. 117.
    Smith R, Rutherford OM. Spine and total body bone mineral density and serum testosterone levels in male athletes. Eur J Appl Physiol 1993; 67: 330–4CrossRefGoogle Scholar
  118. 118.
    Burge MR, Lanzi RA, Skarda ST, et al. Idiopathic hypogonadotropic hypogonadism in a male runner is reversed by clomiphene citrate. Fertil Steril 1997; 67: 783–5PubMedCrossRefGoogle Scholar
  119. 119.
    Skarda ST, Burge MR. Prospective evaluation of risk factors for exercise-induced hypogonadism in male runners. West J Med 1998; 169: 9–12PubMedGoogle Scholar
  120. 120.
    Malina RM. Menarche in athletes: a synthesis and hypothesis. Ann Hum Biol 1983; 10: 1–24PubMedCrossRefGoogle Scholar
  121. 121.
    Stager JM, Hatler LK. Menarche in athletes: the influence of genetics and prepubertal training. Med Sci Sports Exerc 1988; 20: 369–73PubMedCrossRefGoogle Scholar
  122. 122.
    Lu PW, Briody JN, Ogle GD, et al. Bonemineral density of total body, spine, and femoral neck in children and young adults: a cross-sectional and longitudinal study. J Bone Miner Res 1994; 9: 1451–8PubMedCrossRefGoogle Scholar
  123. 123.
    Young D, Hopper JL, Nowson CA, et al. Determinants of bone mass in 10- to 26-year-old females: a twin study. J Bone Miner Res 1995; 10: 558–67PubMedCrossRefGoogle Scholar
  124. 124.
    Dhuper S, Warren MP, Brooks-Gunn J, et al. Effects of hormonal status on bone density in adolescent girls. J Clin Endocrinol Metab 1990; 71: 1083–8PubMedCrossRefGoogle Scholar
  125. 125.
    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
  126. 126.
    Fehily AM, Coles RJ, Evans WD, et al. Factors affecting bone density in young adults. Am J Clin Nutr 1992; 56: 579–86PubMedGoogle Scholar
  127. 127.
    Myburgh KH, Bachrach LK, Lewis B, et al. Low bone mineral density at axial and appendicular sites in amenorrheic athletes. Med Sci Sports Exerc 1993; 25: 1197–202PubMedGoogle Scholar
  128. 128.
    Katzman DK, Bachrach LK, Carter DR, et al. Clinical and anthropometric correlates of bone mineral acquisition in healthy adolescent girls. J Clin Endocrinol Metab 1991; 73: 1332–9PubMedCrossRefGoogle Scholar
  129. 129.
    Armamento-Villareal R, Villareal DT, Avioli LV, et al. Estrogen status and heredity are major determinants of premenopausal bone loss. J Clin Invest 1992; 90: 2464–71PubMedCrossRefGoogle Scholar
  130. 130.
    Elliot JR, Gilchrist NL, Wells JE, et al. Historical assessment of risk factors in screening for osteopenia in a normal Caucasian population. Aust N Z J Med 1993; 23: 458–62PubMedCrossRefGoogle Scholar
  131. 131.
    Fox KM, Magaziner J, Sherwin R, et al. Reproductive correlates of bone mass in elderly women. J Bone Miner Res 1993; 8: 901–8PubMedCrossRefGoogle Scholar
  132. 132.
    Frisch RE, Gotz-Welbergen AV, McArthur JW, et al. Delayed menarche and amenorrhea of college athletes in relation to age of onset of training. JAMA 1981; 246: 1559–63PubMedCrossRefGoogle Scholar
  133. 133.
    Moisan J, Meyer F, Gingras S. A nested case-control study of the correlates of early menarche. Am J Epidemiol 1990; 132: 953–61PubMedGoogle Scholar
  134. 134.
    Mustajoki P, Laapio H, Meurman K. Calcium metabolism, physical activity, and stress fractures. Lancet 1983; I: 797CrossRefGoogle Scholar
  135. 135.
    Lanyon LE, Rubin CT, Baust G. Modulation of bone loss during calcium insufficiency by controlled dynamic loading. Calcif Tiss Int 1986; 38: 209–16CrossRefGoogle Scholar
  136. 136.
    Ferretti JL, Tessaro RD, Audisio EO, et al. Long-term effects of high or low Ca intakes and of lack of parathyroid function on rat femur biomechanics. Calcif Tiss Int 1985; 37: 608–12CrossRefGoogle Scholar
  137. 137.
    Specker BL. Evidence for an interaction between calcium intake and physical activity on changes in bone mineral density. J Bone Miner Res 1996; 11: 1539–44PubMedCrossRefGoogle Scholar
  138. 138.
    Uusirasi K, Sievanen H, Vuori I, et al. Associations of physical activity and calciumintakewith bone mass and size in healthy women at different ages. J Bone Miner Res 1998; 13: 133–42CrossRefGoogle Scholar
  139. 139.
    Johnston CC, Miller JZ, Slemenda CW, et al. Calcium supplementation and increases in bone mineral density in children. N Engl J Med 1992; 327: 82–7PubMedCrossRefGoogle Scholar
  140. 140.
    Lee WTK, Leung SSF, Wang SH, et al. Double-blind, controlled calcium supplementation and bone mineral accretion in children accustomed to a low-calcium diet. Am J Clin Nutr 1994; 60: 744–50PubMedGoogle Scholar
  141. 141.
    Matkovic V, Heaney RP. Calcium balance during human growth: evidence for threshold behaviour. Am J Clin Nutr 1992; 55: 992–6PubMedGoogle Scholar
  142. 142.
    Schwellnus MP, Jordaan G. Does calcium supplementation prevent bone stress injuries? A clinical trial. Int J Sport Nutr 1992; 2: 165–74PubMedGoogle Scholar
  143. 143.
    Myburgh KH, Grobler N, Noakes TD. Factors associated with shin soreness in athletes. Physician Sports Med 1988; 16: 129–34Google Scholar
  144. 144.
    Gardner LI, Dziados JE, Jones BH, et al. Prevention of lower extremity stress fractures: a controlled trial of a shock absorbent insole. Am J Public Health 1988; 78: 1563–7PubMedCrossRefGoogle Scholar
  145. 145.
    Shaffer RA, Brodine SK, Almeida SA, et al. Use of simple measures of physical activity to predict stress fractures in young men undergoing a rigorous physical training program. Am J Epidemiol 1999; 149: 236–42PubMedCrossRefGoogle Scholar
  146. 146.
    Swissa A, Milgrom C, Giladi M, et al. The effect of pretraining sports activity on the incidence of stress fractures among military recruits. Clin Orthop Relat Res 1989; 245: 256–60PubMedGoogle Scholar
  147. 147.
    Worthen BM, Yanklowitz BAD. The pathophysiology and treatment of stress fractures in military personnel. J Am Podiatr Med Assoc 1978; 68: 317–25Google Scholar
  148. 148.
    Scully TJ, Besterman G. Stress fracture: a preventable training injury. Mil Med 1982; 147: 285–7PubMedGoogle Scholar
  149. 149.
    Reinker KA, Ozburne S. A comparison of male and female orthopaedic pathology in basic training. Mil Med 1979; 144: 532–6PubMedGoogle Scholar
  150. 150.
    Greaney RB, Gerber RH, Laughlin RL, et al. Distribution and natural history of stress fractures in US marine recruits. Radiology 1983; 146: 339–46PubMedGoogle Scholar
  151. 151.
    Proztman RR. Physiologic performance of women compared to men. Am J Sports Med 1979; 7: 191–4CrossRefGoogle Scholar
  152. 152.
    Pester S, Smith PC. Stress fractures in the lower extremities of soldiers in basic training. Orthop Rev 1992; 21: 297–303PubMedGoogle Scholar
  153. 153.
    Goldberg B, Pecora C. Stress fractures: a risk of increased training in freshman. Physician Sports Med 1994; 22: 68–78Google Scholar
  154. 154.
    Courtenay BG, Bowers DM. Stress fractures: clinical features and investigation. Med J Aust 1990; 153: 155–6PubMedGoogle Scholar
  155. 155.
    Pecina M, Bojanic I, Dubravcic S. Stress fractures in figure skaters. Am J Sports Med 1990; 18: 277–9PubMedCrossRefGoogle Scholar
  156. 156.
    Devas MB, Sweetnam R. Stress fractures of the fibula: a review of fifty cases in athletes. J Bone Joint Surg 1956; 38: 818–29Google Scholar
  157. 157.
    McMahon TA, Greene PR. The influence of track compliance on running. J Biomech 1979; 12: 893–904PubMedCrossRefGoogle Scholar
  158. 158.
    Steele JR, Milburn PD. Effect of different synthetic sport surfaces on ground reactions forces at landing in netball. Int J Sports Biomech 1988; 4: 130–45Google Scholar
  159. 159.
    Marti B, Vader JP, Minder CE, et al. On the epidemiology of running injuries: the 1984 BernGrand-Prix study. Am J Sports Med 1988; 16: 285–94PubMedCrossRefGoogle Scholar
  160. 160.
    Walter SD, Hart LE, McIntosh JM, et al. The Ontario cohort study of running-related injuries. Arch Intern Med 1989; 149: 2561–4PubMedCrossRefGoogle Scholar
  161. 161.
    Frey C. Footwear and stress fractures. In: Mandelbaum BR, Knapp TP, editors. Clinics in sports medicine. Vol. 16. Philadelphia (PA): W.B. Saunders Company, 1997: 249–57Google Scholar
  162. 162.
    Cook SD, Brinker MR, Poche M. Running shoes. Sports Med 1990; 10: 1–8PubMedCrossRefGoogle Scholar
  163. 163.
    Finestone A, Shlamkovitch N, Eldad A, et al. A prospective study of the effect of the appropriateness of foot-shoe fit and training shoe type on the incidence of overuse injuries among infantry recruits. Mil Med 1992; 157: 489–90PubMedGoogle Scholar
  164. 164.
    Milgrom C, Burr D, Fyhrie D, et al. The effect of shoe gear on human tibial strains recorded during dynamic loading: a pilot study. Foot Ankle Int 1996; 17: 667–71PubMedGoogle Scholar
  165. 165.
    Cinats J, Reid DC, Haddow JB. A biomechanical evaluation of sorbothane. Clin Orthop Relat Res 1987; 222: 281–8PubMedGoogle Scholar
  166. 166.
    Voloshin AS, Wosk J. Influence of artificial shock absorbers on human gait. Clin Orthop Relat Res 1981; 160: 52–6PubMedGoogle Scholar
  167. 167.
    Milgrom C, Burr DB, Boyd RD, et al. The effect of a viscoelastic orthotic on the incidence of tibial stress fractures in an animal model. Foot Ankle 1990; 10: 276–9PubMedGoogle Scholar
  168. 168.
    Milgrom C, Giladi M, Kashtan H, et al. A prospective study of the effect of a shock-absorbing orthotic device on the incidence of stress fractures inmilitary recruits. Foot Ankle 1985; 6: 101–4PubMedGoogle Scholar
  169. 169.
    Schwellnus MP, Jordaan G, Noakes TD. Prevention of common overuse injuries by the use of shock absorbing insoles. Am J Sports Med 1990; 18: 636–41PubMedCrossRefGoogle Scholar
  170. 170.
    Nigg BM, Herzog W, Read LJ. Effect of viscoelastic shoe insoles on vertical impact forces in heel-toe running. Am J Sports Med 1988; 16: 70–6PubMedCrossRefGoogle Scholar
  171. 171.
    Brodsky JW, Kourosh S, Stills M, et al. Objective evaluation of insert material for diabetic and athletic footwear. Foot Ankle 1988; 9: 111–6PubMedGoogle Scholar
  172. 172.
    Nigg BM. Biomechanics, load analysis and sports injuries in the lower extremities. Sports Med 1985; 2: 367–79PubMedCrossRefGoogle Scholar
  173. 173.
    Schaffler MB, Choi K, Milgrom C. Aging and matrix microdamage accumulation in human compact bone. Bone 1995; 17: 521–5PubMedCrossRefGoogle Scholar
  174. 174.
    Theintz G, Buchs B, Rizzoli R, et al. Longitudinal monitoring of bone mass accumulation in healthy adolescents: evidence for a marked reduction after 16 years of age at the levels of the lumbar spine and femoral neck in female subjects. J Clin Endocrinol Metab 1992; 75: 1060–5PubMedCrossRefGoogle Scholar
  175. 175.
    Brudvig TJS, Gudger TD, Obermeyer L. Stress fractures in 295 trainees: a one-year study of incidence as related to age, sex, and race. Mil Med 1983; 148: 666–7PubMedGoogle Scholar
  176. 176.
    Burr DB. Bone, exercise, and stress fractures. Exerc Sport Sci Rev 1997; 25: 171–94PubMedCrossRefGoogle Scholar
  177. 177.
    Matheson GO, Macintyre JG, Taunton JE, et al. Musculoskeletal injuries associated with physical activity in older adults. Med Sci Sports Exerc 1989; 21: 379–85PubMedGoogle Scholar
  178. 178.
    Taimela S, Kujala UM, Osterman K. Intrinsic risk factors and athletic injuries. Sports Med 1990; 9: 205–15PubMedCrossRefGoogle Scholar
  179. 179.
    Mosley JR, Lanyon LE. Strain rate as a controlling influence on adaptive modeling in response to dynamic loading of the ulna in growing male rats. Bone 1998; 23: 313–8PubMedCrossRefGoogle Scholar

Copyright information

© Adis International Limited 1999

Authors and Affiliations

  • Kim Bennell
    • 1
  • Gordon Matheson
    • 2
  • Willem Meeuwisse
    • 3
  • Peter Brukner
    • 4
  1. 1.School of PhysiotherapyUniversity of MelbourneCarltonAustralia
  2. 2.Division of Sports MedicineStanford University School of MedicineStanfordUSA
  3. 3.University of Calgary Sports Medicine CentreCalgaryCanada
  4. 4.Olympic Park Sports Medicine CentreMelbourneAustralia

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