Skip to main content
Log in

Geometric and “True” Densitometric Characteristics of Bones in Athletes with Stress Fracture and Menstrual Disturbances: A Systematic Review

  • Systematic Review
  • Published:
Sports Medicine Aims and scope Submit manuscript

Abstract

Background

Stress fractures can lead to short- and long-term consequences, impacting participation in sport and general health. Recognizing which skeletal characteristics render bones susceptible to stress fracture may aid stress-fracture prevention. Menstrual disturbances among exercising women are a known risk factor for stress fracture; therefore, assessing skeletal commonalities between women with stress fractures and women with menstrual disturbances may increase our understanding of why menstrual disturbances put athletes at greater risk for stress fracture. Three-dimensional (3D) bone imaging tools provide detailed information about volumetric bone mineral density (vBMD) and bone structure that cannot be obtained using traditional two-dimensional (2D) techniques.

Objectives

This systematic review serves to: (1) evaluate the current literature available on vBMD, bone geometry, and bone structure in exercising women with menstrual disturbances and exercising women with stress fractures, and (2) assess the common skeletal characteristics between both conditions. Our aim is to reveal bone properties beyond 2D areal BMD that may indicate increased susceptibility to stress fracture among exercising women with menstrual disturbances.

Search Methods

A search of the PubMed/Medline database was completed in May 2018.

Eligibility Criteria

Eligible articles included those that reported vBMD, bone geometry, or bone structure obtained from 3D imaging techniques or estimated from 2D imaging techniques. Only studies conducted in premenopausal exercising women and girls who had a stress fracture, a menstrual disturbance, or both were included.

Results

Twenty-four articles met the inclusion criteria. Bone area and cortical thickness at the tibia were identified as altered both in women with menstrual disturbances and in women with stress fractures; however, there was inconsistency in the results observed for all bone parameters. The majority of skeletal parameters of the lower extremities were not significantly different between exercising women with and without stress fractures and between those with and without menstrual disturbances.

Discussion

Most studies were moderate or low quality based on study design, and only one article combined both conditions to explore vBMD and bone geometry in athletes with menstrual disturbances and a history of stress fracture. These findings highlight the need for more skeletal research on the intersection of these health conditions in exercising women. The lack of observed differences in skeletal parameters suggests that risk factors other than bone geometry and structure may be the primary causes of stress fracture in these women.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Barrack MT, Gibbs JC, De Souza MJ, Williams NI, Nichols JF, Rauh MJ, et al. Higher incidence of bone stress injuries with increasing female athlete triad-related risk factors: a prospective multisite study of exercising girls and women. Am J Sports Med. 2014;42(4):949–58. https://doi.org/10.1177/0363546513520295.

    Article  PubMed  Google Scholar 

  2. Jones BH, Thacker SB, Gilchrist J, Kimsey CD Jr, Sosin DM. Prevention of lower extremity stress fractures in athletes and soldiers: a systematic review. Epidemiol Rev. 2002;24(2):228–47.

    Article  Google Scholar 

  3. Lindberg JS, Fears WB, Hunt MM, Powell MR, Boll D, Wade CE. Exercise-induced amenorrhea and bone density. Ann Intern Med. 1984;101(5):647–8.

    Article  CAS  Google Scholar 

  4. Marcus R, Cann C, Madvig P, Minkoff J, Goddard M, Bayer M, et al. Menstrual function and bone mass in elite women distance runners. Endocrine and metabolic features. Ann Intern Med. 1985;102(2):158–63.

    Article  CAS  Google Scholar 

  5. Lloyd T, Triantafyllou SJ, Baker ER, Houts PS, Whiteside JA, Kalenak A, et al. Women athletes with menstrual irregularity have increased musculoskeletal injuries. Med Sci Sports Exerc. 1986;18(4):374–9.

    Article  CAS  Google Scholar 

  6. Barrow GW, Saha S. Menstrual irregularity and stress fractures in collegiate female distance runners. Am J Sports Med. 1988;16(3):209–16.

    Article  CAS  Google Scholar 

  7. Ackerman KE, Cano Sokoloff N, Denm G, Clarke HM, Lee H, Misra M. Fractures in relation to menstrual status and bone parameters in young athletes. Med Sci Sports Exerc. 2015;47(8):1577–86. https://doi.org/10.1249/mss.0000000000000574.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Duckham RL, Brooke-Wavell K, Summers GD, Cameron N, Peirce N. Stress fracture injury in female endurance athletes in the United Kingdom: A 12-month prospective study. Scand J Med Sci Sports. 2015;25(6):854–9. https://doi.org/10.1111/sms.12453.

    Article  CAS  PubMed  Google Scholar 

  9. Bennell KL, Malcolm SA, Thomas SA, Wark JD, Brukner PD. The incidence and distribution of stress fractures in competitive track and field athletes A twelve-month prospective study. Am J Sports Med. 1996;24(2):211–7.

    Article  CAS  Google Scholar 

  10. Nattiv A. Stress fractures and bone health in track and field athletes. J Sci Med Sport. 2000;3(3):268–79.

    Article  CAS  Google Scholar 

  11. Nattiv A, Kennedy G, Barrack MT, Abdelkerim A, Goolsby MA, Arends JC, et al. Correlation of MRI grading of bone stress injuries with clinical risk factors and return to play: a 5-year prospective study in collegiate track and field athletes. Am J Sports Med. 2013;41(8):1930–41. https://doi.org/10.1177/0363546513490645.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Kelsey JL, Bachrach LK, Procter-Gray E, Nieves J, Greendale GA, Sowers M, et al. Risk factors for stress fracture among young female cross-country runners. Med Sci Sports Exerc. 2007;39(9):1457–63. https://doi.org/10.1249/mss.0b013e318074e54b.

    Article  PubMed  Google Scholar 

  13. Wentz L, Liu PY, Haymes E, Ilich JZ. Females have a greater incidence of stress fractures than males in both military and athletic populations: a systemic review. Mil Med. 2011;176(4):420–30.

    Article  Google Scholar 

  14. Rauh MJ, Macera CA, Trone DW, Shaffer RA, Brodine SK. Epidemiology of stress fracture and lower-extremity overuse injury in female recruits. Med Sci Sports Exerc. 2006;38(9):1571–7. https://doi.org/10.1249/01.mss.0000227543.51293.9d.

    Article  PubMed  Google Scholar 

  15. Friedl KE, Nuovo JA, Patience TH, Dettori JR. Factors associated with stress fracture in young army women: indications for further research. Mil Med. 1992;157(7):334–8.

    Article  CAS  Google Scholar 

  16. Beck TJ, Ruff CB, Shaffer RA, Betsinger K, Trone DW, Brodine SK. Stress fracture in military recruits: gender differences in muscle and bone susceptibility factors. Bone. 2000;27(3):437–44.

    Article  CAS  Google Scholar 

  17. Shaffer RA, Rauh MJ, Brodine SK, Trone DW, Macera CA. Predictors of stress fracture susceptibility in young female recruits. Am J Sports Med. 2006;34(1):108–15. https://doi.org/10.1177/0363546505278703.

    Article  PubMed  Google Scholar 

  18. Schnackenburg KE, Macdonald HM, Ferber R, Wiley JP, Boyd SK. Bone quality and muscle strength in female athletes with lower limb stress fractures. Med Sci Sports Exerc. 2011;43(11):2110–9. https://doi.org/10.1249/MSS.0b013e31821f8634.

    Article  PubMed  Google Scholar 

  19. Chen YT, Tenforde AS, Fredericson M. Update on stress fractures in female athletes: epidemiology, treatment, and prevention. Curr Rev Musculoskelet Med. 2013;6(2):173–81. https://doi.org/10.1007/s12178-013-9167-x.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Goolsby MA, Barrack MT, Nattiv A. A displaced femoral neck stress fracture in an amenorrheic adolescent female runner. Sports Health. 2012;4(4):352–6. https://doi.org/10.1177/1941738111429929.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Duckham RL, Peirce N, Meyer C, Summers GD, Cameron N, Brooke-Wavell K. Risk factors for stress fracture in female endurance athletes: a cross-sectional study. BMJ Open. 2012;2(6):15. https://doi.org/10.1136/bmjopen-2012-001920.

    Article  Google Scholar 

  22. Bennell KL, Malcolm SA, Thomas SA, Ebeling PR, McCrory PR, Wark JD, et al. Risk factors for stress fractures in female track-and-field athletes: a retrospective analysis. Clin J Sport Med. 1995;5(4):229–35.

    Article  CAS  Google Scholar 

  23. Ackerman KE, Nazem T, Chapko D, Russell M, Mendes N, Taylor AP, et al. Bone microarchitecture is impaired in adolescent amenorrheic athletes compared with eumenorrheic athletes and nonathletic controls. J Clin Endocrinol Metab. 2011;96(10):3123–33. https://doi.org/10.1210/jc.2011-1614.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Christo K, Prabhakaran R, Lamparello B, Cord J, Miller KK, Goldstein MA, et al. Bone metabolism in adolescent athletes with amenorrhea, athletes with eumenorrhea, and control subjects. Pediatrics. 2008;121(6):1127–36. https://doi.org/10.1542/peds.2007-2392.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Gibbs JC, Nattiv A, Barrack MT, Williams NI, Rauh MJ, Nichols JF, et al. Low bone density risk is higher in exercising women with multiple triad risk factors. Med Sci Sports Exerc. 2014;46(1):167–76. https://doi.org/10.1249/MSS.0b013e3182a03b8b.

    Article  PubMed  Google Scholar 

  26. Current evaluation of amenorrhea. Fertil Steril. 2008;90(5 Suppl):S219–25. https://doi.org/10.1016/j.fertnstert.2008.08.038.

    Article  Google Scholar 

  27. De Souza MJ, Williams NI. Beyond hypoestrogenism in amenorrheic athletes: energy deficiency as a contributing factor for bone loss. Curr Sports Med Rep. 2005;4(1):38–44.

    Article  Google Scholar 

  28. De Souza MJ, Nattiv A, Joy E, Misra M, Williams NI, Mallinson RJ, et al. 2014 Female Athlete Triad Coalition Consensus Statement on Treatment and Return to Play of the Female Athlete Triad: 1st International Conference held in San Francisco, California, May 2012 and 2nd International Conference held in Indianapolis, Indiana, May 2013. Br J Sports Med. 2014;48(4):289. https://doi.org/10.1136/bjsports-2013-093218.

    Article  PubMed  Google Scholar 

  29. Torstveit MK, Sundgot-Borgen J. The female athlete triad: are elite athletes at increased risk? Med Sci Sports Exerc. 2005;37(2):184–93.

    Article  Google Scholar 

  30. Gibbs JC, Williams NI, De Souza MJ. Prevalence of individual and combined components of the female athlete triad. Med Sci Sports Exerc. 2013;45(5):985–96. https://doi.org/10.1249/MSS.0b013e31827e1bdc.

    Article  PubMed  Google Scholar 

  31. Seeman E. The structural and biomechanical basis of the gain and loss of bone strength in women and men. Endocrinol Metab Clin North Am. 2003;32(1):25–38.

    Article  CAS  Google Scholar 

  32. Seeman E. Estrogen, androgen, and the pathogenesis of bone fragility in women and men. Curr Osteoporos Rep. 2004;2(3):90–6.

    Article  Google Scholar 

  33. De Souza MJ, West SL, Jamal SA, Hawker GA, Gundberg CM, Williams NI. The presence of both an energy deficiency and estrogen deficiency exacerbate alterations of bone metabolism in exercising women. Bone. 2008;43(1):140–8. https://doi.org/10.1016/j.bone.2008.03.013.

    Article  CAS  PubMed  Google Scholar 

  34. Southmayd EA, Mallinson RJ, Williams NI, Mallinson DJ, De Souza MJ. Unique effects of energy versus estrogen deficiency on multiple components of bone strength in exercising women. Osteoporos Int. 2017;28(4):1365–76. https://doi.org/10.1007/s00198-016-3887-x.

    Article  CAS  PubMed  Google Scholar 

  35. Hart NH, Nimphius S, Rantalainen T, Ireland A, Siafarikas A, Newton RU. Mechanical basis of bone strength: influence of bone material, bone structure and muscle action. J Musculoskelet Neuronal Interact. 2017;17(3):114–39.

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Joy EA, Campbell D. Stress fractures in the female athlete. Curr Sports Med Rep. 2005;4(6):323–8.

    Article  Google Scholar 

  37. Nattiv A, Kennedy G, Barrack MT, Abdelkerim A, Goolsby MA, Arends JC, et al. Correlation of MRI grading of bone stress injuries with clinical risk factors and return to play: a 5-year prospective study in collegiate track and field athletes. Am J Sports Med. 2013;41(8):1930–41. https://doi.org/10.1177/0363546513490645.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Matheson GO, Clement DB, McKenzie DC, Taunton JE, Lloyd-Smith DR, MacIntyre JG. Stress fractures in athletes. A study of 320 cases. Am J Sports Med. 1987;15(1):46–58. https://doi.org/10.1177/036354658701500107.

    Article  CAS  PubMed  Google Scholar 

  39. Boden BP, Osbahr DC. High-risk stress fractures: evaluation and treatment. J Am Acad Orthop Surg. 2000;8(6):344–53.

    Article  CAS  Google Scholar 

  40. Bouxsein ML, Seeman E. Quantifying the material and structural determinants of bone strength. Best Pract Res Clin Rheumatol. 2009;23(6):741–53. https://doi.org/10.1016/j.berh.2009.09.008.

    Article  PubMed  Google Scholar 

  41. Yoshikawa T, Turner CH, Peacock M, Slemenda CW, Weaver CM, Teegarden D, et al. Geometric structure of the femoral neck measured using dual-energy x-ray absorptiometry. J Bone Miner Res. 1994;9(7):1053–64. https://doi.org/10.1002/jbmr.5650090713.

    Article  CAS  PubMed  Google Scholar 

  42. Beck TJ, Ruff CB, Warden KE, Scott WW Jr, Rao GU. Predicting femoral neck strength from bone mineral data. A structural approach. Invest Radiol. 1990;25(1):6–18.

    Article  CAS  Google Scholar 

  43. Beck TJ. Extending DXA beyond bone mineral density: understanding hip structure analysis. Curr Osteoporos Rep. 2007;5(2):49–55.

    Article  Google Scholar 

  44. Beck TJ, Ruff CB, Mourtada FA, Shaffer RA, Maxwell-Williams K, Kao GL, et al. Dual-energy X-ray absorptiometry derived structural geometry for stress fracture prediction in male U.S. Marine Corps recruits. J Bone Miner Res. 1996;11(5):645–53. https://doi.org/10.1002/jbmr.5650110512.

    Article  CAS  PubMed  Google Scholar 

  45. Choi K, Goldstein SA. A comparison of the fatigue behavior of human trabecular and cortical bone tissue. J Biomech. 1992;25(12):1371–81.

    Article  CAS  Google Scholar 

  46. Mandell JC, Khurana B, Smith SE. Stress fractures of the foot and ankle, part 2: site-specific etiology, imaging, and treatment, and differential diagnosis. Skelet Radiol. 2017;46(9):1165–86. https://doi.org/10.1007/s00256-017-2632-7.

    Article  Google Scholar 

  47. Tenforde AS, Kraus E, Fredericson M. Bone Stress Injuries in Runners. Phys Med Rehabil Clin N Am. 2016;27(1):139–49. https://doi.org/10.1016/j.pmr.2015.08.008.

    Article  PubMed  Google Scholar 

  48. Zeni AI, Street CC, Dempsey RL, Staton M. Stress injury to the bone among women athletes. Phys Med Rehabil Clin N Am. 2000;11(4):929–47.

    Article  CAS  Google Scholar 

  49. Shamseer L, Moher D, Clarke M, Ghersi D, Liberati A, Petticrew M, et al. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. BMJ. 2015;349:g7647. https://doi.org/10.1136/bmj.g7647.

    Article  Google Scholar 

  50. Bennell K, Crossley K, Jayarajan J, Walton E, Warden S, Kiss ZS, et al. Ground reaction forces and bone parameters in females with tibial stress fracture. Med Sci Sports Exerc. 2004;36(3):397–404.

    Article  Google Scholar 

  51. Popp KL, Hughes JM, Smock AJ, Novotny SA, Stovitz SD, Koehler SM, et al. Bone geometry, strength, and muscle size in runners with a history of stress fracture. Med Sci Sports Exerc. 2009;41(12):2145–50. https://doi.org/10.1249/MSS.0b013e3181a9e772.

    Article  PubMed  Google Scholar 

  52. Popp KL, McDermott W, Hughes JM, Baxter SA, Stovitz SD, Petit MA. Bone strength estimates relative to vertical ground reaction force discriminates women runners with stress fracture history. Bone. 2017;94:22–8. https://doi.org/10.1016/j.bone.2016.10.006.

    Article  PubMed  Google Scholar 

  53. Weidauer LA, Binkley T, Vukovich M, Specker B. Greater polar moment of inertia at the tibia in athletes who develop stress fractures. Orthop J Sports Med. 2014;2(7):2325967114541411. https://doi.org/10.1177/2325967114541411.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Franklyn M, Oakes B, Field B, Wells P, Morgan D. Section modulus is the optimum geometric predictor for stress fractures and medial tibial stress syndrome in both male and female athletes. Am J Sports Med. 2008;36(6):1179–89. https://doi.org/10.1177/0363546508314408.

    Article  PubMed  Google Scholar 

  55. Duckham RL, Brooke-Wavell K, Summers GD, Cameron N, Peirce N. Stress fracture injury in female endurance athletes in the United Kingdom: a 12-month prospective study. Scand J Med Sci Sports. 2015;25(6):854–9. https://doi.org/10.1111/sms.12453.

    Article  CAS  PubMed  Google Scholar 

  56. Armstrong DW 3rd, Rue JP, Wilckens JH, Frassica FJ. Stress fracture injury in young military men and women. Bone. 2004;35(3):806–16. https://doi.org/10.1016/j.bone.2004.05.014.

    Article  PubMed  Google Scholar 

  57. Ackerman KE, Putman M, Guereca G, Taylor AP, Pierce L, Herzog DB, et al. Cortical microstructure and estimated bone strength in young amenorrheic athletes, eumenorrheic athletes and non-athletes. Bone. 2012;51(4):680–7. https://doi.org/10.1016/j.bone.2012.07.019.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Ackerman KE, Pierce L, Guereca G, Slattery M, Lee H, Goldstein M, et al. Hip structural analysis in adolescent and young adult oligoamenorrheic and eumenorrheic athletes and nonathletes. J Clin Endocrinol Metab. 2013;98(4):1742–9. https://doi.org/10.1210/jc.2013-1006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Cano Sokoloff N, Eguiguren ML, Wargo K, Ackerman KE, Baskaran C, Singhal V, et al. Bone parameters in relation to attitudes and feelings associated with disordered eating in oligo-amenorrheic athletes, eumenorrheic athletes, and nonathletes. Int J Eat Disord. 2015;48(5):522–6. https://doi.org/10.1002/eat.22405.

    Article  PubMed  Google Scholar 

  60. Fazeli PK, Ackerman KE, Pierce L, Guereca G, Bouxsein M, Misra M. Sclerostin and Pref-1 have differential effects on bone mineral density and strength parameters in adolescent athletes compared with non-athletes. Osteoporos Int. 2013;24(9):2433–40. https://doi.org/10.1007/s00198-013-2353-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Mitchell DM, Tuck P, Ackerman KE, Cano Sokoloff N, Woolley R, Slattery M, et al. Altered trabecular bone morphology in adolescent and young adult athletes with menstrual dysfunction. Bone. 2015;81:24–30. https://doi.org/10.1016/j.bone.2015.06.021.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Ducher G, Eser P, Hill B, Bass S. History of amenorrhoea compromises some of the exercise-induced benefits in cortical and trabecular bone in the peripheral and axial skeleton: a study in retired elite gymnasts. Bone. 2009;45(4):760–7. https://doi.org/10.1016/j.bone.2009.06.021.

    Article  CAS  PubMed  Google Scholar 

  63. Mallinson RJ, Williams NI, Gibbs JC, Koehler K, Allaway HC, Southmayd E, et al. Current and past menstrual status is an important determinant of femoral neck geometry in exercising women. Bone. 2016;88:101–12. https://doi.org/10.1016/j.bone.2016.01.030.

    Article  PubMed  Google Scholar 

  64. Mallinson RJ, Williams NI, Hill BR, De Souza MJ. Body composition and reproductive function exert unique influences on indices of bone health in exercising women. Bone. 2013;56(1):91–100. https://doi.org/10.1016/j.bone.2013.05.008.

    Article  PubMed  Google Scholar 

  65. To WW, Wong MW, Lam IY. Bone mineral density differences between adolescent dancers and non-exercising adolescent females. J Pediatr Adolesc Gynecol. 2005;18(5):337–42. https://doi.org/10.1016/j.jpag.2005.06.005.

    Article  PubMed  Google Scholar 

  66. Duckham RL, Peirce N, Bailey CA, Summers G, Cameron N, Brooke-Wavell K. Bone geometry according to menstrual function in female endurance athletes. Calcif Tissue Int. 2013;92(5):444–50. https://doi.org/10.1007/s00223-013-9700-3.

    Article  CAS  PubMed  Google Scholar 

  67. Piasecki J, Ireland A, Piasecki M, Cameron J, McPhee JS, Degens H. The strength of weight-bearing bones is similar in amenorrheic and eumenorrheic elite long-distance runners. Scand J Med Sci Sports. 2018;28(5):1559–68. https://doi.org/10.1111/sms.13062.

    Article  CAS  PubMed  Google Scholar 

  68. Ruffing JA, Nieves JW, Zion M, Tendy S, Garrett P, Lindsay R, et al. The influence of lifestyle, menstrual function and oral contraceptive use on bone mass and size in female military cadets. Nutr Metab (Lond). 2007;4:17. https://doi.org/10.1186/1743-7075-4-17.

    Article  PubMed  PubMed Central  Google Scholar 

  69. Finestone A, Milgrom C. How stress fracture incidence was lowered in the Israeli army: a 25-yr struggle. Med Sci Sports Exerc. 2008;40(11 Suppl):S623–9. https://doi.org/10.1249/MSS.0b013e3181892dc2.

    Article  PubMed  Google Scholar 

  70. Giladi M, Milgrom C, Simkin A, Stein M, Kashtan H, Margulies J, et al. Stress fractures and tibial bone width. A risk factor. J Bone Jt Surg Br. 1987;69(2):326–9.

    Article  CAS  Google Scholar 

  71. Silva MJ. Biomechanics of osteoporotic fractures. Injury. 2007;38(Suppl 3):S69–76. https://doi.org/10.1016/j.injury.2007.08.014.

    Article  PubMed  Google Scholar 

  72. Pasco JA, Seeman E, Henry MJ, Merriman EN, Nicholson GC, Kotowicz MA. The population burden of fractures originates in women with osteopenia, not osteoporosis. Osteoporos Int. 2006;17(9):1404–9. https://doi.org/10.1007/s00198-006-0135-9.

    Article  CAS  PubMed  Google Scholar 

  73. Vainionpaa A, Korpelainen R, Sievanen H, Vihriala E, Leppaluoto J, Jamsa T. Effect of impact exercise and its intensity on bone geometry at weight-bearing tibia and femur. Bone. 2007;40(3):604–11. https://doi.org/10.1016/j.bone.2006.10.005.

    Article  PubMed  Google Scholar 

  74. Michalopoulou M, Kambas A, Leontsini D, Chatzinikolaou A, Draganidis D, Avloniti A, et al. Physical activity is associated with bone geometry of premenarcheal girls in a dose-dependent manner. Metab Clin Exp. 2013;62(12):1811–8. https://doi.org/10.1016/j.metabol.2013.08.006.

    Article  CAS  PubMed  Google Scholar 

  75. Maimoun L, Coste O, Philibert P, Briot K, Mura T, Galtier F, et al. Peripubertal female athletes in high-impact sports show improved bone mass acquisition and bone geometry. Metab Clin Exp. 2013;62(8):1088–98. https://doi.org/10.1016/j.metabol.2012.11.010.

    Article  CAS  PubMed  Google Scholar 

  76. Ferry B, Lespessailles E, Rochcongar P, Duclos M, Courteix D. Bone health during late adolescence: effects of an 8-month training program on bone geometry in female athletes. Jt Bone Spine. 2013;80(1):57–63. https://doi.org/10.1016/j.jbspin.2012.01.006.

    Article  Google Scholar 

  77. 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):136–41.

    Article  Google Scholar 

  78. Tenforde AS, Sainani KL, Carter Sayres L, Milgrom C, Fredericson M. Participation in ball sports may represent a prehabilitation strategy to prevent future stress fractures and promote bone health in young athletes. PM R. 2015;7(2):222–5. https://doi.org/10.1016/j.pmrj.2014.09.017.

    Article  PubMed  Google Scholar 

  79. Wade GN, Schneider JE. Metabolic fuels and reproduction in female mammals. Neurosci Biobehav Rev. 1992;16(2):235–72.

    Article  CAS  Google Scholar 

  80. De Souza MJ, Nattiv A, Joy E, Misra M, Williams NI, Mallinson RJ, et al. 2014 Female Athlete Triad Coalition consensus statement on treatment and return to play of the female athlete triad: 1st International Conference held in San Francisco, CA, May 2012, and 2nd International Conference held in Indianapolis, IN, May 2013. Clin J Sport Med. 2014;24(2):96–119. https://doi.org/10.1097/JSM.0000000000000085.

    Article  PubMed  Google Scholar 

  81. Mallinson RJ, Williams NI, Olmsted MP, Scheid JL, Riddle ES, De Souza MJ. A case report of recovery of menstrual function following a nutritional intervention in two exercising women with amenorrhea of varying duration. J Int Soc Sports Nutr. 2013;10(1):34. https://doi.org/10.1186/1550-2783-10-34.

    Article  PubMed  PubMed Central  Google Scholar 

  82. Russell M, Misra M. Influence of ghrelin and adipocytokines on bone mineral density in adolescent female athletes with amenorrhea and eumenorrheic athletes. Med Sport Sci. 2010;55:103–13. https://doi.org/10.1159/000321975.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Papageorgiou M, Dolan E, Elliott-Sale KJ, Sale C. Reduced energy availability: implications for bone health in physically active populations. Eur J Nutr. 2017. https://doi.org/10.1007/s00394-017-1498-8.

    Article  PubMed  PubMed Central  Google Scholar 

  84. Loucks AB, Callister R. Induction and prevention of low-T3 syndrome in exercising women. Am J Physiol. 1993;264(5 Pt 2):R924–30.

    CAS  PubMed  Google Scholar 

  85. Ihle R, Loucks AB. Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res. 2004;19(8):1231–40. https://doi.org/10.1359/JBMR.040410.

    Article  PubMed  Google Scholar 

  86. Sienkiewicz E, Magkos F, Aronis KN, Brinkoetter M, Chamberland JP, Chou S, et al. Long-term metreleptin treatment increases bone mineral density and content at the lumbar spine of lean hypoleptinemic women. Metabolism. 2011;60(9):1211–21. https://doi.org/10.1016/j.metabol.2011.05.016.

    Article  CAS  PubMed  Google Scholar 

  87. Papageorgiou M, Elliott-Sale KJ, Parsons A, Tang JCY, Greeves JP, Fraser WD, et al. Effects of reduced energy availability on bone metabolism in women and men. Bone. 2017;105:191–9. https://doi.org/10.1016/j.bone.2017.08.019.

    Article  CAS  PubMed  Google Scholar 

  88. Scheid JL, Toombs RJ, Ducher G, Gibbs JC, Williams NI, De Souza MJ. Estrogen and peptide YY are associated with bone mineral density in premenopausal exercising women. Bone. 2011;49(2):194–201. https://doi.org/10.1016/j.bone.2011.04.011.

    Article  CAS  PubMed  Google Scholar 

  89. Hughes JM, Popp KL, Yanovich R, Bouxsein ML, Matheny RW Jr. The role of adaptive bone formation in the etiology of stress fracture. Exp Biol Med (Maywood). 2017;242(9):897–906. https://doi.org/10.1177/1535370216661646.

    Article  CAS  PubMed  Google Scholar 

  90. Miller KK, Lee EE, Lawson EA, Misra M, Minihan J, Grinspoon SK, et al. Determinants of skeletal loss and recovery in anorexia nervosa. J Clin Endocrinol Metab. 2006;91(8):2931–7. https://doi.org/10.1210/jc.2005-2818.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Bonnick SL. HSA: beyond BMD with DXA. Bone. 2007;41(1 Suppl 1):S9–12. https://doi.org/10.1016/j.bone.2007.03.007.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the concept or design of the article and the drafting or revision of this manuscript. All authors approved the final version.

Corresponding author

Correspondence to Rebecca J. Mallinson.

Ethics declarations

Funding

No sources of funding were used to assist in the preparation of this article.

Conflict of interest

Rebecca Mallinson, Emily Southmayd and Mary Jane De Souza declare they have no conflicts of interest that are relevant to the content of this review.

Additional information

Part of the following topical collection: Athlete Health & Wellness.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mallinson, R.J., Southmayd, E.A. & De Souza, M.J. Geometric and “True” Densitometric Characteristics of Bones in Athletes with Stress Fracture and Menstrual Disturbances: A Systematic Review. Sports Med 49, 1059–1078 (2019). https://doi.org/10.1007/s40279-019-01109-6

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40279-019-01109-6

Navigation