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Stress and Insufficiency Fractures

  • Joseph L. Shaker
Review Paper

Abstract

Stress fractures are most common in athletes and military recruits but also occur in patients with underlying metabolic bone disease (insufficiency fractures). Stress fractures are most frequent in the lower extremities and more common in women. The female athlete triad is an important risk factor. At the cellular level, the osteocyte may be important in the detection of stress fractures. Further, osteocytes are probably important in the healing of stress fractures. In patients with recurrent stress fractures, a biochemical evaluation for underlying metabolic bone disease should be undertaken. Prevention includes avoidance of sudden increases in the exercise, the use of proper footwear, avoidance of rough and hilly surfaces, and adequate nutrition. In premenopausal women with persistent amenorrhea and hypoestrogenism, estrogen replacement should be considered. Altering the mechanics of running might decrease the risk in some patients. In the patient with a stress fracture, the offending activity must be stopped for the fracture to heal. In some high-risk stress fractures, orthopedic surgery is advised. There is no specific drug therapy. Stress fractures are also associated with several metabolic bone diseases which are highlighted in this review with clinical vignettes. Diagnosis and management of these conditions is critical in the treatment of these patients.

Keywords

Insufficiency fractures Stress fractures 

Notes

Compliance with Ethical Standards

The article does not contain any studies with human or animal subjects performed by the any of the authors. Informed consent is not needed as no studies on human subjects were performed.

Conflict of Interest

The author is on the Advisory Board, Alexion (2014); Advisory Board, Shire; and Advisory Board, Ultragenyx.

References

  1. 1.
    Breithaupt M. To the pathology of the human foot (in German). Med Zeitung. 1855;24:169.Google Scholar
  2. 2.
    Moreira CA, Bilezikian JP. Stress fractures: concepts and therapeutics. J Clin Endocrinol Metab. 2017;102:525–34.  https://doi.org/10.1210/jc.2016-2720.PubMedGoogle Scholar
  3. 3.
    Cosman F, Ruffing J, Zion M, Uhorchak J, Ralston S, Tendy S, et al. Determinants of stress fracture risk in United States Military Academy cadets. Bone. 2013;55(2):359–66.  https://doi.org/10.1016/j.bone.2013.04.011.PubMedCrossRefGoogle Scholar
  4. 4.
    Bennell K, Matheson G, Meeuwisse W, Brukner P. Risk factors for stress fractures. Sports Med. 1999;28(2):91–122.  https://doi.org/10.2165/00007256-199928020-00004.PubMedCrossRefGoogle Scholar
  5. 5.
    McKenna MJ, Heffernan E, Hurson C, McKiernan FE. Clinical approach to diagnosis of stress fractures including bisphosphonate-associated fractures. QJM. 2013;107(2):99–105.  https://doi.org/10.1093/qjmed/hct192.PubMedCrossRefGoogle Scholar
  6. 6.
    Pepper M, Akuthota V, McCarty EC. The pathophysiology of stress fractures. Clin Sports Med. 2006;25(1):1–16.  https://doi.org/10.1016/j.csm.2005.08.010.PubMedCrossRefGoogle Scholar
  7. 7.
    Burr DB, Forwood MR, Fyhrie DP, Martin RB, Schaffler MB, Turner CH. Bone microdamage and skeletal fragility in osteoporotic and stress fractures. J Bone Miner Res. 1997;12(1):6–15.  https://doi.org/10.1359/jbmr.1997.12.1.6.PubMedCrossRefGoogle Scholar
  8. 8.
    Carter DR, Caler WE. A cumulative damage model for bone fracture. J Orthop Res. 1985;3(1):84–90.  https://doi.org/10.1002/jor.1100030110.PubMedCrossRefGoogle Scholar
  9. 9.
    Dallas SL, Prideaux M, Bonewald LF. The osteocyte: an endocrine cell and more. Endocrine Rev. 2013;34(5):658–90.  https://doi.org/10.1210/er.2012-1026.CrossRefGoogle Scholar
  10. 10.
    Hazenberg JG, Freeley M, Foran E, Lee TC, Taylor D. Microdamage: a cell transducing mechanism based on ruptured osteocyte processes. J Biomech. 2006;39(11):2096–103.  https://doi.org/10.1016/j.jbiomech.2005.06.006.PubMedCrossRefGoogle Scholar
  11. 11.
    Mulargia S, Dooley C, Cristofolini L, Taylor D. Fracture and fatigue in osteocytes. J Mech Behav Biomed Mater. 2014;39:231–7.  https://doi.org/10.1016/j.jmbbm.2014.07.023.PubMedCrossRefGoogle Scholar
  12. 12.
    Dooley C, Cafferky D, Lee TC, Taylor D. Fatigue failure of osteocyte processes: implications for the repair of bone. European Cells and Materials. 2014;27:39–49.  https://doi.org/10.22203/eCM.v027a04.PubMedCrossRefGoogle Scholar
  13. 13.
    Wu AC, Kidd LJ, Cowling NR, Kelly WL, Forwood MR. Osteocyte expression of caspase-3, COX-2, IL-6 and sclerostin are spatially and temporally associated following stress fracture initiation. BoneKEy Reports. 2014;3  https://doi.org/10.1038/bonekey.2014.66.
  14. 14.
    Kahanov L, Eberman L, Games K, Wasik M. Diagnosis, treatment, and rehabilitation of stress fractures in the lower extremity in runners. Open Access Journal of Sports Medicine. 2015;87  https://doi.org/10.2147/oajsm.s39512.
  15. 15.
    Robertson GAJ, Wood AM. Lower limb stress fractures in sport: optimising their management and outcome. World Journal of Orthopedics. 2017;8(3):242–55.  https://doi.org/10.5312/wjo.v8.i3.242.PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Wright AA, Taylor JB, Ford KR, Siska L, Smoliga JM. Risk factors associated with lower extremity stress fractures in runners: a systematic review with meta-analysis. Br J Sports Med. 2015;49(23):1517–23.  https://doi.org/10.1136/bjsports-2015-094828.PubMedCrossRefGoogle Scholar
  17. 17.
    Guler G, Kutuk MO, Yildirim V, Celik GG, Toros F, Milcan A. Tibia stress fracture secondary to obsessive compulsive disorder. The International Journal of Psychiatry in Medicine. 2016;51(3):258–61.  https://doi.org/10.1177/0091217416651398.PubMedCrossRefGoogle Scholar
  18. 18.
    Kohring JM, Curtiss HM, Tyser AR. A scaphoid stress fracture in a female collegiate-level shot-putter and review of the literature. Case Reports in Orthopedics. 2016;2016:1–5.  https://doi.org/10.1155/2016/8098657.CrossRefGoogle Scholar
  19. 19.
    Christiansen E, Kanstrup IL. Increased risk of stress fractures of the ribs in elite rowers. Scand J Med Sci Sports. 1997;7(1):49–52.PubMedCrossRefGoogle Scholar
  20. 20.
    Lee AD. Golf-related stress fractures: a structured review of the literature. J Can Chiropr Assoc. 2009;53(4):290–9.PubMedPubMedCentralGoogle Scholar
  21. 21.
    Pedret C, Balius, Alomar X, Vilaró J, Ruiz-Cotorro A, Minoves M. Stress fracture of the supracondylar process of the humerus in a professional tennis player. Clin J Sport Med. 2015;25(1):e20–2.  https://doi.org/10.1097/jsm.0000000000000101.PubMedCrossRefGoogle Scholar
  22. 22.
    Young CC, Raasch WG, Geiser C. Ulnar stress fracture of the nondominant arm in a tennis player using a two-handed backhand. Clin J Sport Med. 1995;5(4):262–4.  https://doi.org/10.1097/00042752-199510000-00011.PubMedCrossRefGoogle Scholar
  23. 23.
    Meena S, Rastogi D, Solanki B, Chowdhury B. Stress fracture of ulna due to excessive push-ups. Journal of Natural Science, Biology and Medicine. 2014;5(1):225–7.  https://doi.org/10.4103/0976-9668.127349.CrossRefGoogle Scholar
  24. 24.
    Fredericson M, Bergman AG, Hoffman KL, Dillingham MS. Tibial stress reaction in runners. Correlation with clinical symptoms and scintigraphy with a new magnetic resonance imaging grading system. Am J Sports Med. 1995;23(4):472–81.  https://doi.org/10.1177/036354659502300418.PubMedCrossRefGoogle Scholar
  25. 25.
    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. Am J Sports Med. 2013;41(8):1930–41.  https://doi.org/10.1177/0363546513490645.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Wright AA, Hegedus EJ, Lenchik L, Kuh KJ, Santiago L, Smoliga JM. Diagnostic accuracy of various imaging modalities for suspected lower extremity stress fractures. Am J Sports Med. 2015;44(1):255–63.  https://doi.org/10.1177/0363546515574066.PubMedCrossRefGoogle Scholar
  27. 27.
    Chen YT, Tenforde AS, Fredericson M. Update on stress fractures in female athletes: epidemiology, treatment, and prevention. Current Reviews in Musculoskeletal Medicine. 2013;6(2):173–81.  https://doi.org/10.1007/s12178-013-9167-x.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    McCormick, Nwachukwu BU, Provencher MT. Stress fractures in runners. Clin Sports Med. 2012;31(2):291–306.  https://doi.org/10.1016/j.csm.2011.09.012.PubMedCrossRefGoogle Scholar
  29. 29.
    Milgrom C, Finestone AS. The effect of stress fracture interventions in a single elite infantry training unit (1983–2015). Bone. 2017;103:125–30.  https://doi.org/10.1016/j.bone.2017.06.026.PubMedCrossRefGoogle Scholar
  30. 30.
    Milgrom C, Finestone A, Segev S, Olin C, Arndt T, Ekenman I. Are overground or treadmill runners more likely to sustain tibial stress fracture? Br J Sports Med. 2003;37(2):160–3.  https://doi.org/10.1136/bjsm.37.2.160.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    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):e001920.  https://doi.org/10.1136/bmjopen-2012-001920.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Davey T, Lanham-New SA, Shaw AM, Hale B, Cobley R, Berry JL, et al. Low serum 25-hydroxyvitamin D is associated with increased risk of stress fracture during Royal Marine recruit training. Osteoporos Int. 2015;27(1):171–9.  https://doi.org/10.1007/s00198-015-3228-5.PubMedCrossRefGoogle Scholar
  33. 33.
    Miller JR, Dunn KW, Ciliberti LJ, Patel RD, Swanson BA. Association of vitamin D with stress fractures: a retrospective cohort study. The Journal of Foot and Ankle Surgery. 2016;55(1):117–20.  https://doi.org/10.1053/j.jfas.2015.08.002.PubMedCrossRefGoogle Scholar
  34. 34.
    Nieves JW, Melsop K, Curtis M, Kelsey JL, Bachrach LK, Greendale G, et al. Nutritional factors that influence change in bone density and stress fracture risk among young female cross-country runners. PM&R. 2010;2(8):740–50.  https://doi.org/10.1016/j.pmrj.2010.04.020.CrossRefGoogle Scholar
  35. 35.
    Strohbach CA, Scofield DE, Nindl BC, Centi AJ, Yanovich R, Evans RK, et al. Female recruits sustaining stress fractures during military basic training demonstrate differential concentrations of circulating IGF-I system components: a preliminary study. Growth Hormon IGF Res. 2012;22(5):151–7.  https://doi.org/10.1016/j.ghir.2012.04.007.CrossRefGoogle Scholar
  36. 36.
    Bulathsinhala L, Hughes JM, McKinnon CJ, Kardouni JR, Guerriere KI, Popp KL, et al. Risk of stress fracture varies by race/ethnic origin in a cohort study of 1.3 million US Army soldiers. J Bone Miner Res. 2017;32(7):1546–53.  https://doi.org/10.1002/jbmr.3131.PubMedCrossRefGoogle Scholar
  37. 37.
    Korpelainen R, Orava S, Karpakka J, Siira P, Hulkko A. Risk factors for recurrent stress fractures in athletes. Am J Sports Med. 2001;29(3):304–10.  https://doi.org/10.1177/03635465010290030901.PubMedCrossRefGoogle Scholar
  38. 38.
    Macera CA, Pate RR, Powell KE, Jackson KL, Kendrick JS, Craven TE. Predicting lower-extremity injuries among habitual runners. Arch Intern Med. 1989;149(11):2565–8.  https://doi.org/10.1001/archinte.1989.00390110117026.PubMedCrossRefGoogle Scholar
  39. 39.
    Armstrong DW, Rue J-P H, 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.PubMedCrossRefGoogle Scholar
  40. 40.
    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.  https://doi.org/10.1016/S8756-3282(00)00342-2.PubMedCrossRefGoogle Scholar
  41. 41.
    Popp KL, Hughes JM, Smock AJ, 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.PubMedCrossRefGoogle Scholar
  42. 42.
    Edwards WB, Gillette JC, Thomas JM, Derrick TR. Internal femoral forces and moments during running: implications for stress fracture development. Clin Biomech. 2008;23(10):1269–78.  https://doi.org/10.1016/j.clinbiomech.2008.06.011.CrossRefGoogle Scholar
  43. 43.
    Milner CE, Ferber R, Pollard CD, Hamill J, Davis IS. Biomechanical factors associated with tibial stress fracture in female runners. Med Sci Sports Exerc. 2006;38(2):323–8.  https://doi.org/10.1249/01.mss.0000183477.75808.92.PubMedCrossRefGoogle Scholar
  44. 44.
    Pohl MB, Mullineaux DR, Milner CE, Hamill J, Davis IS. Biomechanical predictors of retrospective tibial stress fractures in runners. J Biomech. 2008;41(6):1160–5.  https://doi.org/10.1016/j.jbiomech.2008.02.001.PubMedCrossRefGoogle Scholar
  45. 45.
    Milner CE, Davis IS, Hamill J. Free moment as a predictor of tibial stress fracture in distance runners. J Biomech. 2006;39(15):2819–25.  https://doi.org/10.1016/j.jbiomech.2005.09.022.PubMedCrossRefGoogle Scholar
  46. 46.
    Milner CE, Hamill J, Davis I. Are knee mechanics during early stance related to tibial stress fracture in runners? Clin Biomech. 2007;22(6):697–703.  https://doi.org/10.1016/j.clinbiomech.2007.03.003.CrossRefGoogle Scholar
  47. 47.
    Meardon SA, Willson JD, Gries SR, Kernozek TW, Derrick TR. Bone stress in runners with tibial stress fracture. Clin Biomech. 2015;30(9):895–902.  https://doi.org/10.1016/j.clinbiomech.2015.07.012.CrossRefGoogle Scholar
  48. 48.
    Meardon SA, Derrick TR. Effect of step width manipulation on tibial stress during running. J Biomech. 2014;47(11):2738–44.  https://doi.org/10.1016/j.jbiomech.2014.04.047.PubMedCrossRefGoogle Scholar
  49. 49.
    Zifchock RA, Davis I, Hamill J. Kinetic asymmetry in female runners with and without retrospective tibial stress fractures. J Biomech. 2006;39(15):2792–7.  https://doi.org/10.1016/j.jbiomech.2005.10.003.PubMedCrossRefGoogle Scholar
  50. 50.
    Dixon SJ, Creaby MW, Allsopp AJ. Comparison of static and dynamic biomechanical measures in military recruits with and without a history of third metatarsal stress fracture. Clin Biomech. 2006;21(4):412–9.  https://doi.org/10.1016/j.clinbiomech.2005.11.009.CrossRefGoogle Scholar
  51. 51.
    Weist R, Eils E, Rosenbaum D. The influence of muscle fatigue on electromyogram and plantar pressure patterns as an explanation for the incidence of metatarsal stress fractures. Am J Sports Med. 2004;32(8):1–6.  https://doi.org/10.1177/0363546504265191.CrossRefGoogle Scholar
  52. 52.
    Mizrahi J, Verbitsky O, Isakov E. Fatigue-related loading imbalance on the shank in running: a possible factor in stress fractures. Ann Biomed Eng. 2000;28(4):463–9.  https://doi.org/10.1114/1.284.PubMedCrossRefGoogle Scholar
  53. 53.
    Fyhrie DP, Milgrom C, Hoshaw SJ, Simkin A, Dar S, Drumb D, et al. Effect of fatiguing exercise on longitudinal bone strain as related to stress fracture in humans. Ann Biomed Eng. 1998;26(4):660–5.  https://doi.org/10.1114/1.103.PubMedCrossRefGoogle Scholar
  54. 54.
    Javed A, Tebben PJ, Fischer P, Lteif AN. Female athlete triad and its components: toward improved screening and management. Mayo Clin Proc. 2013;88(9):996–1009.  https://doi.org/10.1016/j.mayocp.2013.07.001.PubMedCrossRefGoogle Scholar
  55. 55.
    Androulakis I, Kaltsas G, Chrousos G. Pseudo-Cushing’s states. In ENDOTEXT.org. 2015.
  56. 56.
    Barrow GW, Saha S. Menstrual irregularity and stress fractures in collegiate female distance runners. Am J Sports Med. 1988;16(3):209–16.  https://doi.org/10.1177/036354658801600302.PubMedCrossRefGoogle Scholar
  57. 57.
    Lips P, van Schoor NM, Braverboer N. Vitamin D-related disorders. In: Rosen CJ, editor. Primer on the metabolic bone diseases and disorders of mineral metabolism. 8th ed: American Society for Bone and Mineral Research. Ames: Wiley-Blackwell; 2013. p. 613–23.Google Scholar
  58. 58.
    Ruppe MD, Jan de Beur SM. Disorders of phosphate homeostasis. In: Rosen CJ, editor. Primer on the metabolic bone diseases and disorders of mineral metabolism. 8th ed: American Society for Bone and Mineral Research. Ames: Wiley-Blackwell; 2013. p. 601–12.Google Scholar
  59. 59.
    Rathbun JC. “Hypophosphatasia”: a new developmental anomaly. Am J Dis Child. 1948;75(6):822–31.  https://doi.org/10.1001/archpedi.1948.02030020840003.PubMedCrossRefGoogle Scholar
  60. 60.
    Whyte MP. Hypophosphatasia: enzyme replacement therapy brings new opportunities and new challenges. J Bone Miner Res. 2017;32(4):667–75.  https://doi.org/10.1002/jbmr.3075.PubMedCrossRefGoogle Scholar
  61. 61.
    Whyte MP. Hypophosphatasia: an overview for 2017. Bone. 2017;102:15–25.  https://doi.org/10.1016/j.bone.2017.02.011.PubMedCrossRefGoogle Scholar
  62. 62.
    Schmidt T, Mussawy H, Rolvien T, Hawellek T, Hubert J, Rüther W, et al. Clinical, radiographic and biochemical characteristics of adult hypophosphatasia. Osteoporos Int. 2017;28(9):2653–62.  https://doi.org/10.1007/s00198-017-4087-z.PubMedCrossRefGoogle Scholar
  63. 63.
    Sutton RA, Mumm S, Coburn SP, Ericson KL, Whyte MP. “Atypical femoral fractures” during bisphosphonate exposure in adult hypophosphatasia. J Bone Miner Res. 2012;27(5):987–94.  https://doi.org/10.1002/jbmr.1565.PubMedCrossRefGoogle Scholar
  64. 64.
    Mckiernan FE, Berg RL, Fuehrer J. Clinical and radiographic findings in adults with persistent hypophosphatasemia. J Bone Miner Res. 2014;29(7):1651–60.  https://doi.org/10.1002/jbmr.2178.PubMedCrossRefGoogle Scholar
  65. 65.
    McKiernan FE, Dong J, Berg RL, Scotty E, Mundt P, Larson L, et al. Mutational and biochemical findings in adults with persistent hypophosphatasemia. Osteoporos Int. 2017;28(8):2343–8.  https://doi.org/10.1007/s00198-017-4035-y.PubMedCrossRefGoogle Scholar
  66. 66.
    Yavuz U, Sökücü S, Demir B, Akpınar E, Lapçin O, Atıcı Y, et al. An unusual stress fracture in an archer with hypophosphatasia. Case Reports in Orthopedics. 2013;2013:1–3.  https://doi.org/10.1155/2013/350236.CrossRefGoogle Scholar
  67. 67.
    Whyte MP, Greenberg CR, Salman NJ, Bober MB, McAlister WH, Wenkert D, et al. Enzyme-replacement therapy in life-threatening hypophosphatasia. N Engl J Med. 2012;366(10):904–13.  https://doi.org/10.1056/nejmoa1106173.PubMedCrossRefGoogle Scholar
  68. 68.
    Whyte MP, Madson KL, Phillips D, Reeves AL, McAlister WH, Yakimoski A, et al. Asfotase alfa therapy for children with hypophosphatasia. JCI Insight. 2016;1(9):e85971.  https://doi.org/10.1172/jci.insight.85971.PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Miller P, Aggers D, Carrithers E, Klidaras P, and Foran J. Asfotase alpha therapy heals recalcitrant bilateral pathologic femoral fractures in a patient with hypophosphatasia after one year of treatment, that were previously non-healing up to 9 years. ASBMR Meeting 2017; SA0338.Google Scholar
  70. 70.
    Whyte MP, Mumm S, Deal C. Adult hypophosphatasia treated with teriparatide. J Clin Endocrinol Metab. 2007;92(4):1203–8.  https://doi.org/10.1210/jc.2006-1902.PubMedCrossRefGoogle Scholar
  71. 71.
    Poonuru S, Findling JW, Shaker JL. Lower extremity insufficiency fractures: an underappreciated manifestation of endogenous Cushing’s syndrome. Osteoporos Int. 2016;27(12):3645–9.  https://doi.org/10.1007/s00198-016-3712-6.PubMedCrossRefGoogle Scholar
  72. 72.
    Cushing H. The basophil adenomas of the pituitary body and their clinical manifestations. Bull Johns Hopkins Hosp. 1932;50:137–95.Google Scholar
  73. 73.
    Albon LM, Rippin JD, Franklyn JA. “My feet are killing me!” An unusual presentation of Cushing’s syndrome. Endocrine Society Abstracts. 2003;5:P26.Google Scholar
  74. 74.
    Licata AA. Stress fractures in young athletic women case reports of unsuspected cortisol induced osteoporosis. Med Sci Sports Exerc. 1992;24(9):955–7.PubMedCrossRefGoogle Scholar
  75. 75.
    Ontell FK, Shelton DK. Multiple stress fractures, an unusual presentation of Cushing’s disease. Western J Medicine. 1995;162:364–6.Google Scholar
  76. 76.
    LiYeung LL, Lui TH. Adrenal adenoma can present with stress fractures of the feet. J Orthoped Case Rep. 2015;5:77–8.Google Scholar
  77. 77.
    Papadakis G, Uebelhart B, Goumaz M, Zawadynski S, Rizzzoli R. An unusual case of hypercortisolism with multiple weight-bearing bone fractures. Clinical Cases in Mineral and Bone Metabolism. 2013;10(3):213–7.PubMedGoogle Scholar
  78. 78.
    Villiers J, Khamashta M, Hepburn A. Recurrent atraumatic metatarsal, rib, and sacral insufficiency fractures in a woman with the antiphospholipid syndrome. BMJ Case Rep 2013; 11.  https://doi.org/10.1136/bcr-2013-201311.
  79. 79.
    Haddad FS, Mohanna PN, Goddard NJ. Bilateral femoral neck stress fractures following steroid treatment. Injury. 1997;28:9–10.CrossRefGoogle Scholar
  80. 80.
    Miyanishi K, Hara T, Hamada T, Maekawa M, Tsurusaki S, Moro-oka T, et al. Co-occurence of subchondral fracture of the femoral head and contralateral femoral neck in a rheumatic patient receiving steroid treatment. Mod Rheumatol. 2008;18(6):619–22.  https://doi.org/10.3109/s10165-008-0093-5.PubMedCrossRefGoogle Scholar
  81. 81.
    Mochizuki T, Momohara S, Ikari K, Kawamura K, Tsukahara S, Iwamoto T, et al. Spontaneous multiple insufficiency fractures after pelvic abscess and sepsis in a rheumatoid arthritis patient treated with high-load corticosteroid therapy a case report. Clin Rheumatol. 2007;26(11):1925–8.  https://doi.org/10.1007/s10067-007-0535-z.PubMedCrossRefGoogle Scholar
  82. 82.
    Bali K, Meena D, Krishnan V, Chana R, Rawall S, Aggarwal S. Steroid-induced stress fracture of the medial tibial condyle a case report. J Knee Surgery. 2013;26(Suppl 1):S25–9.Google Scholar
  83. 83.
    Canalis E. Mechanisms of glucocorticoid action in bone. Curr Osteoporosis Rep. 2005;3(3):98–102.  https://doi.org/10.1007/s11914-005-0017-7.CrossRefGoogle Scholar
  84. 84.
    Shaker JL. Paget’s disease of bone: a review of epidemiology, pathophysiology and management. Ther Adv Musculoskelet Dis. 2009;1(2):107–25.  https://doi.org/10.1177/1759720x09351779.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Siris E, Roodman GD. Paget’s disease of bone. In: Rosen CJ, Compston JE, Lian JB, editors. Primer on the metabolic bone diseases and disorders of mineral metabolism. 7th ed: American Society for Bone and Mineral Research. Ames: Wiley-Blackwell; 2008. p. 335–43.Google Scholar
  86. 86.
    Redden JF, Dixon J, Vennart W, Hosking DJ. Management of fissure fractures in Paget’s disease. Int Orthop. 1981;5(2):103–6.  https://doi.org/10.1007/BF00267839.PubMedCrossRefGoogle Scholar
  87. 87.
    Odvina CV, Zerwekh JE, Rao DS, Maalouf N, Gottschalk FA, Pak CYC. Severely suppressed bone turnover: a potential complication of alendronate therapy. J Clin Endocrinol Metab. 2005;90(3):1294–301.  https://doi.org/10.1210/jc.2004-0952.PubMedCrossRefGoogle Scholar
  88. 88.
    Visekruna M, Wilson D, Mckiernan FE. Severely suppressed bone turnover and atypical skeletal fragility. J Clin Endocrinol Metab. 2008;93(8):2948–52.  https://doi.org/10.1210/jc.2007-2803.PubMedCrossRefGoogle Scholar
  89. 89.
    Odvina CV, Levy S, Rao S, Zerwekh JE, Rao DS. Unusual mid-shaft fractures during long-term bisphosphonate therapy. Clin Endocrinol. 2010;72(2):161–8.  https://doi.org/10.1111/j.1365-2265.2009.03581.x.CrossRefGoogle Scholar
  90. 90.
    Ang BFH, Koh JBS, Ng ACM, Howe TS. Bilateral ulna fractures associated with bisphosphonate therapy. Osteoporos Int. 2012;24(4):1523–5.  https://doi.org/10.1007/s00198-012-2118-3.PubMedCrossRefGoogle Scholar
  91. 91.
    Erdem Y, Atbasi Z, Emre TY, Kavadar G, Demiralp B. Effect of long-term use of bisphosphonates on forearm bone: atypical ulna fractures in elderly woman with osteoporosis. Case Reports in Orthopedics. 2016;2016:1–4.  https://doi.org/10.1155/2016/4185202.CrossRefGoogle Scholar
  92. 92.
    Shane E, Burr D, Abrahamsen B, Adler RA, Brown TD, Cheung AM, et al. Atypical subtrochanteric and diaphyseal femoral fractures: second report of a task force of the American Society for Bone and Mineral Research. J Bone Miner Res. 2013;29(1):1–23.  https://doi.org/10.1002/jbmr.1998.PubMedCrossRefGoogle Scholar
  93. 93.
    Saita Y, Ishijima M, Kaneko K. Atypical femoral fractures and bisphosphonate use: current evidence and clinical implications. Ther Adv Chronic Dis. 2015;6(4):185–93.  https://doi.org/10.1177/2040622315584114.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Saita Y, Ishijima M, Mogami A, Kubota M, Baba T, Kaketa T, et al. The incidence of and risk factors for developing atypical femoral fractures in Japan. J Bone Miner Metab. 2015;33(3):311–8.  https://doi.org/10.1007/s00774-014-0591-9.PubMedCrossRefGoogle Scholar
  95. 95.
    Aspenberg P. Denosumab and atypical femoral fractures. Acta Orthop. 2014;85(1):1.  https://doi.org/10.3109/17453674.2013.859423.PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    McKiernan FE. Atypical femoral diaphyseal fractures documented by serial DXA. J Clin Densitom. 2010;13(1):102–3.  https://doi.org/10.1016/j.jocd.2009.11.002.PubMedCrossRefGoogle Scholar
  97. 97.
    McKenna MJ, van der Kamp S, Heffernan E, Hurson C. Incomplete atypical femoral fractures: assessing the diagnostic utility of DXA by extending femur length. J Clin Densitom. 2013;16(4):579–83.  https://doi.org/10.1016/j.jocd.2013.06.004.PubMedCrossRefGoogle Scholar
  98. 98.
    Mckiernan FE, Hocking J, Cournoyer S, Berg RL, Linneman J. A long femur scan field does not alter proximal femur bone mineral density measurements by dual-energy X-ray absorptiometry. J Clin Densitom. 2011;14(3):354–8.  https://doi.org/10.1016/j.jocd.2011.04.004.PubMedCrossRefGoogle Scholar
  99. 99.
    Gomberg SJ, Wustrack RL, Napoli N, Arnaud CD, Black DM. Teriparatide, vitamin D, and calcium healed bilateral subtrochanteric stress fractures in a postmenopausal woman with a 13-year history of continuous alendronate therapy. J Clin Endocrinol Metab. 2011;96(6):1627–32.  https://doi.org/10.1210/jc.2010-2520.PubMedCrossRefGoogle Scholar
  100. 100.
    Chiang CY, Zebaze RM, Ghasem-zadeh A, Iuliano-burns S, Hardidge A, Seeman E. Teriparatide improves bone quality and healing of atypical femoral fractures associated with bisphosphonate therapy. Bone. 2013;52(1):360–5.  https://doi.org/10.1016/j.bone.2012.10.006.PubMedCrossRefGoogle Scholar
  101. 101.
    Huang HT, Kang L, Huang PJ, Fu YC, Lin SY, Hsieh CH, et al. Successful teriparatide treatment of atypical fracture after long-term use of alendronate without surgical procedure in a postmenopausal woman: a case report. Menopause. 2012;19(12):1360–3.  https://doi.org/10.1097/gme.0b013e318260143d.PubMedCrossRefGoogle Scholar
  102. 102.
    Yates CJ, Bartlett MJ, Ebeling PR. An atypical subtrochanteric femoral fracture from pycnodysostosis: a lesson from nature. J Bone Miner Res. 2011;26(6):1377–9.  https://doi.org/10.1002/jbmr.308.PubMedCrossRefGoogle Scholar
  103. 103.
    Chapurlat RD. Odanacatib: a review of its potential in the management of osteoporosis in postmenopausal women. Ther Adv Musculoskelet Dis. 2015;7(3):103–9.  https://doi.org/10.1177/1759720X15580903.PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Oh D, Huh SJ. Insufficiency fracture after radiation therapy. Radiat Oncol J. 2014;32(4):213–20.  https://doi.org/10.3857/roj.2014.32.4.213.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Baxter NN, Habermann EB, Tepper JE, Durham SB, Virnig BA. Risk of pelvic fractures in older women following pelvic irradiation. JAMA. 2005;294(20):2587–93.  https://doi.org/10.1001/jama.294.20.2587.PubMedCrossRefGoogle Scholar
  106. 106.
    İğdem Ş, Alço G, Ercan T, Barlan M, Ganiyusufoğlu K, Ünalan B, et al. Insufficiency fractures after pelvic radiotherapy in patients with prostate cancer. International Journal of Radiation; Oncology, Biology, Physics. 2010;7(3):818–23.  https://doi.org/10.1016/j.ijrobp.2009.05.059.CrossRefGoogle Scholar
  107. 107.
    Moussazadeh N, Laufer I, Werner T, Krol G, Boland P, Bilsky MH, et al. Sacroplasty for cancer-associated insufficiency fractures. Neurosurgery. 2015;76(4):446–50.  https://doi.org/10.1227/NEU.0000000000000658.PubMedCrossRefGoogle Scholar
  108. 108.
    Wu CC, Econs MJ, DiMeglio LA, Insogna KL, Levine MA, Orchard PJ, et al. Diagnosis and management of osteopetrosis: consensus guidelines from the osteopetrosis working group. J Clin Endocrinol Metab. 2017;102(9):3111–23.  https://doi.org/10.1210/jc.2017-01127.PubMedCrossRefGoogle Scholar
  109. 109.
    Daffner RH, Pavlov H. Stress fractures: current concepts. Am J Roentgenol. 1992;159(2):245–52.  https://doi.org/10.2214/ajr.159.2.1632335.CrossRefGoogle Scholar
  110. 110.
    Cundy TF, Edmonds ME, Watkins PJ. Osteopenia and metatarsal fractures in diabetic neuropathy. Diabet Med. 1985;2(6):461–4.  https://doi.org/10.1111/j.1464-5491.1985.tb00683.x.PubMedCrossRefGoogle Scholar
  111. 111.
    Schwellnus MP, Jordaan G. Does calcium supplementation prevent bone stress injuries? A clinical trial. Int J Sport Nutr. 1992;2(2):165–74.  https://doi.org/10.1123/ijsn.2.2.165.PubMedCrossRefGoogle Scholar
  112. 112.
    Lappe J, Cullen D, Haynatzki G, Recker, Ahlf R, Thompson K. Calcium and vitamin D supplementation decreases incidence of stress fractures in female navy recruits. J Bone Miner Res. 2008;23(5):741–9.  https://doi.org/10.1359/jbmr.080102.PubMedCrossRefGoogle Scholar
  113. 113.
    Rome K, Handoll HH, Ashford RL. Interventions for preventing and treating stress fractures and stress reactions of bone of the lower limbs in young adults. In: Rome K, editor. Cochrane Database of Systematic Reviews. Chichester, West Sussex: John Wiley & Sons, Ltd.; 2005. p. 1–42.  https://doi.org/10.1002/14651858.cd000450.pub2.
  114. 114.
    Gordon CM, Ackerman KE, Berga SL, Kaplan JR, Mastorakos G, Misra M, et al. Functional hypothalamic amenorrhea: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab. 2017;102(5):1413–39.  https://doi.org/10.1210/jc.2017-00131.PubMedCrossRefGoogle Scholar
  115. 115.
    Milgrom C, Finestone A, Novack V, et al. The effect of prophylactic treatment with risedronate on stress fracture incidence among infantry recruits. Bone. 2004;35(2):418–24.  https://doi.org/10.1016/j.bone.2004.04.016.PubMedCrossRefGoogle Scholar
  116. 116.
    Simon MJK, Barvencik F, Luttke M, Amling M, Mueller-Wohlfahrt HW, Ueblacker P. Intravenous bisphosphonates and vitamin D in the treatment of bone marrow oedema in professional athletes. Injury. 2014;45(6):981–7.  https://doi.org/10.1016/j.injury.2014.01.023.PubMedCrossRefGoogle Scholar
  117. 117.
    Babu S, Sandiford NA, Vrahas M. Use of teriparatide to improve fracture healing: what is the evidence? World J Orthop. 2015;6(6):457–61.  https://doi.org/10.5312/wjo.v6.i6.457.PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Raghavan P, Christofides E. Role of teriparatide in accelerating metatarsal stress fracture healing: a case series and review of literature. Clinical Medicine Insights: Endocrinology and Diabetes. 2012;2012:39.  https://doi.org/10.4137/cmed.s9663.Google Scholar
  119. 119.
    Yoo J-I, Ha YC, Ryu H-J, Chang GW, Lee YK, Yoo MJ, et al. Teriparatide treatment in elderly patients with sacral insufficiency fracture. J Clin Endocrinol Metab. 2017;102(2):560–5.  https://doi.org/10.1210/jc.2016-3582.PubMedGoogle Scholar
  120. 120.
    Baillieul S, Guinot M, Dubois C, Prunier A, Mahler F, Gaudin P. Set the pace of bone healing—treatment of a bilateral sacral stress fracture using teriparatide in a long-distance runner. Joint Bone Spine. 2017;84(4):499–500.  https://doi.org/10.1016/j.jbspin.2016.06.003.PubMedCrossRefGoogle Scholar
  121. 121.
    Drake M, Farr JN. Inhibitors of sclerostin. Current Opinion in Rheumatology. 2014;26(4):447–52.  https://doi.org/10.1097/bor.0000000000000073.PubMedPubMedCentralCrossRefGoogle Scholar
  122. 122.
    McClung MR, Grauer A, Boonen S, Bolognese MA, Brown JP, Diez-Perez A, et al. Romosozumab in postmenopausal women with low bone mineral density. N Engl J Med. 2014;370(5):412–20.  https://doi.org/10.1056/nejmoa1305224.PubMedCrossRefGoogle Scholar
  123. 123.
    Cosman F, Crittenden DB, Adachi JD, et al. Romosozumab treatment in postmenopausal women with osteoporosis. N Engl J Med. 2016;375(16):1532–43.  https://doi.org/10.1056/nejmoa1607948.PubMedCrossRefGoogle Scholar
  124. 124.
    Saag KG, Petersen J, Brandi ML, Karaplis AC, Lorentzon M, Thomas T, et al. Romosozumab or alendronate for fracture prevention in women with osteoporosis. N Engl J Med. 2017;377(15):1417–27.  https://doi.org/10.1056/nejmoa1708322.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2017

Authors and Affiliations

  • Joseph L. Shaker
    • 1
    • 2
  1. 1.Department of Medicine (Endocrinology)Medical College of WisconsinWauwatosaUSA
  2. 2.Menomonee FallsUSA

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