Pathophysiology and risk factors for osteonecrosis

Aaron RK, Gray R. Osteonecrosis: etiology, natural history, pathophysiology, and diagnosis. In: Callaghan JJ, Rosenberg AG, Rubash HE, editors. The adult hip. Philadelphia: Lippincott Williams & Wilkins; 2007. p. 465–76.

James J, Steijn-Myagkaya GL. Death of osteocytes. Electron microscopy after in vitro ischaemia. J Bone Joint Surg (Br). 1986;68(4):620–4.

Bauer TW, Stulberg BN. The histology of osteonecrosis and its distinction from histologic artifacts. In: Schoutens A et al., editors. Bone circulation and vascularization in normal and pathological conditions. New York: Plenum Press; 1993. p. 283–92.

Kenzora JE GM. Osteonecrosis. In: Kelly WN HE, Ruddy S, et al., editors. Textbook of rheumatology. Philadelphia: WB Saunders; 1981. p. 1755–82.

Glimcher MJ, Kenzora JE. The biology of osteonecrosis of the human femoral head and its clinical implications: I. Tissue biology. Clin Orthop Relat Res. 1979;138:284–309.

Glimcher MJ, Kenzora JE. The biology of osteonecrosis of the human femoral head and its clinical implications: II. The pathological changes in the femoral head as an organ and in the hip joint. Clin Orthop Relat Res. 1979;139:283–312.

Glimcher MJ, Kenzora JE. The biology of osteonecrosis of the human femoral head and its clinical implications: III Discussion of the etiology and genesis of the pathological sequelae; comments on treatment. Clin Orthop Relat Res. 1979;140:273–312.

Brown TD, Baker KJ, Brand RA. Structural consequences of subchondral bone involvement in segmental osteonecrosis of the femoral head. J Orthop Res. 1992;10(1):79–87.

Lorich D, Lazaro L. Fractures and bone repair. In: Aaron RK, editor. Skeletal circulation in clinical practice. Singapore: World Scientific; 2015. This chapter is a compendium of original work done to demonstrate the vascularity of the femoral head and the consequences of both interruption of vascularity and preservation of vascularity. As such, it is highly relevant to disorders of circulation most notably avascular necrosis.

Atsumi T. Bone arteriography of the femoral head of humans in normal and pathological conditions. In: Schoutens A et al., editors. Bone circulation and vascularization in normal and pathological conditions. US: Springer; 1993. p. 293–9.

Atsumi T, Kuroki Y. Role of impairment of blood supply of the femoral head in the pathogenesis of idiopathic osteonecrosis. Clin Orthop Relat Res. 1992;277:22–30.

Atsumi T, Kuroki Y, Yamano K. A microangiographic study of idiopathic osteonecrosis of the femoral head. Clin Orthop Relat Res. 1989;246:186–94.

Ohzono K et al. Intraosseous arterial architecture in nontraumatic avascular necrosis of the femoral head. Microangiographic and histologic study. Clin Orthop Relat Res. 1992;277:79–88.

Kiaer T et al. Intra-osseous pressure and oxygen tension in avascular necrosis and osteoarthritis of the hip. J Bone Joint Surg (Br). 1990;72(6):1023–30.

Tsukamoto H et al. Evaluation of marrow perfusion in the femoral head by dynamic magnetic resonance imaging. Effect of venous occlusion in a dog model. Invest Radiol. 1992;27(4):275–81.

Ficat RP. Idiopathic bone necrosis of the femoral head: early diagnosis and treatment. J Bone Joint Surg. 1985;67B:3–9.

Hungerford DS. Early diagnosis and treatment of ischemic necrosis of the femoral head. In: Weil UH, editor. Progress in orthopaedic surgery. Berlin: Springer-Verlag; 1981. p. 29.

Hungerford DS, Lennox DW. The importance of increased intraosseous pressure in the development of osteonecrosis of the femoral head: implications for treatment. In Orthopaedic clinics of North America1985. p. 635.

Camp JF, Colwell CW. Core decompression of the femoral head for osteonecrosis. J Bone Joint Surg. 1986;68A:1313.

Hauzeur JPH, Pasteels JL, Orloff S. Bilateral non-traumatic aseptic osteonecrosis in the femoral head. J Bone Joint Surg. 1987;69A:1221–5.

Learmonth ID, Maloon S, Dall G. Core decompression for early atraumatic osteonecrosis of the femoral head. J Bone Joint Surg. 1990;72B:387.

Welch RD et al. Bone changes associated with intraosseous hypertension in the caprine tibia. J Bone Joint Surg Am. 1993;75(1):53–60.

Arnoldi CC. The relationship between intraosseous and intra-articular pressure. In: Arlet J, Ficat RP, Hungerford DS, editors. Bone circulation. Baltimore: Williams & Wilkins; 1984. p. 213–21.

Downey DJ, Simkin PA, Taggart R. The effect of compressive loading on intraosseous pressure in the femoral head in vitro. J Bone Joint Surg. 1988;70A:871.

Kiaer T, Gronlund J, Sorensen KH. Subchondral pO2, pCO2, pressure, pH, and lactate in human osteoarthritis of the hip. Clin Orthop Relat Res. 1988;229:149–55.

Jones Jr JP. Concepts of etiology and early pathogenesis of osteonecrosis. Instr Course Lect. 1994;43:499–512.

Jones Jr JP. Etiology and pathogenesis of osteonecrosis. Semin Arthroplast. 1991;2:160–8.

Spitzer WO, Horwitz SM. Selected nonexperimental methods: an orientation. In: Troidl H et al., editors. Principles and practice of research. US: Springer; 1991. p. 104–13.

Johnson EO, Soultanis K, Soucacos PN. Vascular anatomy and microcirculation of skeletal zones vulnerable to osteonecrosis: vascularization of the femoral head. Orthop Clin N Am. 2004;35(3):285–91. viii.

Zlotorowicz M et al. The blood supply to the femoral head after posterior fracture/dislocation of the hip, assessed by CT angiography. Bone Joint J. 2013;95-B(11):1453–7.

Zlotorowicz M et al. Anatomy of the medial femoral circumflex artery with respect to the vascularity of the femoral head. J Bone Joint Surg Br. 2011;93(11):1471–4.

Assouline-Dayan Y et al. Pathogenesis and natural history of osteonecrosis. Semin Arthritis Rheum. 2002;32(2):94–124.

Slobogean GP, et al. Complications following young femoral neck fractures. Injury. 2014.

Liu Y et al. Femoral neck fractures: prognosis based on a new classification after superselective angiography. J Orthop Sci Off J Japan Orthop Assoc. 2013;18(3):443–50. This is a study demonstrating the anatomy of the femoral head vasculature using a technique of the super selective angiography. Implications in terms of femoral head vascularity after fractures are discussed.

Garden RS. Malreduction and avascular necrosis in subcapital fractures of the femur. J Bone Joint Surg. 1971;53B:183–90.

Barnes R et al. Subcapital fractures of the femur. A prospective review. J Bone Joint Surg (Br). 1976;58(1):2–24.

Nikolopoulos KE et al. Long-term outcome of patients with avascular necrosis, after internal fixation of femoral neck fractures. Injury. 2003;34(7):525–8.

Wang T et al. Analysis of risk factors for femoral head necrosis after internal fixation in femoral neck fractures. Orthopedics. 2014;37(12):e1117–23.

Papakostidis C, et al. Timing of internal fixation of femoral neck fractures. A systematic review and meta-analysis of the final outcome. Injury. 2015.

Doak J, Schiller J, Eberson C. Circulation of the pediatric and adolescent hip. In: Aaron RK, editor. Skeletal circulation in clinical practice. Singapore: World Scientific; 2015.

Shrader MW et al. Femoral neck fractures in pediatric patients: 30 years experience at a level 1 trauma center. Clin Orthop Relat Res. 2007;454:169–73.

Ng GP, Cole WG. Effect of early hip decompression on the frequency of avascular necrosis in children with fractures of the neck of the femur. Injury. 1996;27(6):419–21.

Barquet A et al. Avascular necrosis of the femoral head following trochanteric fractures in adults: a systematic review. Injury. 2014;45(12):1848–58.

Dwyer AJ et al. Complications after posterior dislocation of the hip. Int Orthop. 2006;30(4):224–7.

McKee MD et al. Irreducible fracture-dislocation of the hip: a severe injury with a poor prognosis. J Orthop Trauma. 1998;12(4):223–9.

Hougaard K, Thomsen PB. Traumatic posterior dislocation of the hip—prognostic factors influencing the incidence of avascular necrosis of the femoral head. Arch Orthop Trauma Surg Archiv fur orthopadische und Unfall-Chirurgie. 1986;106(1):32–5.

Gautier E et al. Anatomy of the medial femoral circumflex artery and its surgical implications. J Bone Joint Surg Br. 2000;82(5):679–83.

Bastian JD et al. Long-term outcome after traumatic anterior dislocation of the hip. Arch Orthop Trauma Surg. 2011;131(9):1273–8.

Dreinhofer KE et al. Isolated traumatic dislocation of the hip. Long-term results in 50 patients. J Bone Joint Surg Br. 1994;76(1):6–12.

Mukisi-Mukaza M et al. Prevalence, clinical features, and risk factors of osteonecrosis of the femoral head among adults with sickle cell disease. Orthopedics. 2000;23(4):357–63.

Matos MA et al. Avascular necrosis of the femoral head in sickle cell disease patients. Ortop Traumatol Rehabil. 2012;14(2):155–60. This work discusses the implications of sickle cell disease and intravascular occlusion on bone necrosis including subarticular disease.

Axelrod AR, Clifford GO, Tanaka KR. Sickle cell anemia (homozygous S) with aseptic necrosis of femoral head. Blood. 1956;11(11):998–1008.

Colin Y, Le Van Kim C, El Nemer W. Red cell adhesion in human diseases. Curr Opin Hematol. 2014;21(3):186–92.

Hernigou P et al. The natural history of asymptomatic osteonecrosis of the femoral head in adults with sickle cell disease. J Bone Joint Surg Am. 2006;88(12):2565–72.

Glueck CJ et al. Thrombophilia, hypofibrinolysis, the eNOS T-786C polymorphism, and multifocal osteonecrosis. J Bone Joint Surg Am. 2008;90(10):2220–9.

Zalavras CG et al. Genetic background of osteonecrosis: associated with thrombophilic mutations? Clin Orthop Relat Res. 2004;422:251–5.

Hadjigeorgiou G et al. Genetic association studies in osteonecrosis of the femoral head: mini review of the literature. Skelet Radiol. 2008;37(1):1–7.

Jones LC et al. Procoagulants and osteonecrosis. J Rheumatol. 2003;30(4):783–91.

Zalavras C et al. Potential aetiological factors concerning the development of osteonecrosis of the femoral head. Eur J Clin Investig. 2000;30(3):215–21.

Berger CE et al. Elevated levels of lipoprotein(a) in familial bone marrow edema syndrome of the hip. Clin Orthop Relat Res. 2000;377:126–31.

Cheras PA et al. Hypercoagulability and hypofibrinolysis in primary osteoarthritis. Clin Orthop Relat Res. 1997;334:57–67.

Gallistl S et al. The role of inherited thrombotic disorders in the etiology of Legg-Calve-Perthes disease. J Pediatr Orthop. 1999;19(1):82–3.

Kealey WD et al. The role of coagulation abnormalities in the development of Perthes' disease. J Bone Joint Surg (Br). 2000;82(5):744–6.

Kawai K, Tamaki A, Hirohata K. Steroid-induced accumulation of lipid in the osteocytes of the rabbit femoral head. A histochemical and electron microscopic study. J Bone Joint Surg Am. 1985;67(5):755–63.

Wang GJ et al. Fat-cell changes as a mechanism of avascular necrosis of the femoral head in cortisone-treated rabbits. J Bone Joint Surg Am. 1977;59(6):729–35.

Wang Y et al. Alcohol-induced adipogenesis in bone and marrow: a possible mechanism for osteonecrosis. Clin Orthop Relat Res. 2003;410:213–24.

Ikemura S et al. Lipid metabolism abnormalities in alcohol-treated rabbits: a morphometric and haematologic study comparing high and low alcohol doses. Int J Exp Pathol. 2011;92(4):290–5.

Felson DT, Anderson JJ. Across-study evaluation of association between steroid dose and bolus steroids and avascular necrosis of bone. Lancet. 1987;1(8538):902–6.

Aaron RK et al. Corticosteroid-associated avascular necrosis: dose relationships and early diagnosis. Ann N Y Acad Sci. 2011;1240:38–46. These studies put into appropriate perspective the true associations of corticosteroids and avascular necrosis using a longitudinal prospective model. Early diagnosis with screening MRI allows detection of avascular necrosis in an early stage where joint preservation is possible.

Cruess RL. Steroid-induced osteonecrosis. J R Coll Surg Edinb. 1981;26(2):69–77.

Fisher DE, Bickel WH. Corticosteroid-induced avascular necrosis. A clinical study of seventy-seven patients. J Bone Joint Surg Am. 1971;53(5):859–73.

Vakil N, Sparberg M. Steroid related osteonecrosis in inflammatory bowel disease. Gastroenterology. 1989;96:62–7.

Zizic TM et al. Corticosteroid therapy associated with ischemic necrosis of bone in systemic lupus erythematosus. Am J Med. 1985;79(5):596–604.

Schroer WC. Current concepts on the pathogenesis of osteonecrosis of the femoral head. Orthop Rev. 1994;23(6):487–97.

Joo YB, et al. Prevalence, incidence, and associated factors of avascular necrosis in Korean patients with systemic lupus erythematosus: a nationwide epidemiologic study. Rheumatol Int. 2014.

Arlet J. Nontraumatic avascular necrosis of the femoral head: past, present, and future. Clin Orthop Relat Res. 1992;277:12–21.

Patterson RJ, Bickel WH, Dahlin DC. Idiopathic avascular necrosis of the head of the femur. A study of fifty-two cases. J Bone Joint Surg Am. 1964;46:267–82.

Matsuo K et al. Influence of alcohol intake, cigarette smoking, and occupational status on idiopathic osteonecrosis of the femoral head. Clin Orthop Relat Res. 1988;234:115–23.

Deegan PB et al. Osseous manifestations of adult Gaucher disease in the era of enzyme replacement therapy. Medicine. 2011;90(1):52–60.

Poll LW et al. MRI bone marrow findings in 63 patients with type I Gaucher disease. Röfo. 2010;182(11):979–85.

Karimova EJ et al. Femoral head osteonecrosis in pediatric and young adult patients with leukemia or lymphoma. J Clin Oncol Off J Am Soc Clin Oncol. 2007;25(12):1525–31.

Niinimaki R et al. Incidence of severe osteonecrosis requiring total joint arthroplasty in children and young adults treated for leukemia or lymphoma: a nationwide, register-based study in Finland and Denmark. J Adolesc Young Adult Oncol. 2013;2(4):138–44.

Griffiths-Jones W et al. the equivalence of remote electronic and paper patient reported outcome (PRO) collection. J Arthroplasty. 2014;29(11):2136–9.

Jones Jr JP. Intravascular coagulation and osteonecrosis. Clin Orthop Relat Res. 1992;277:41–53.

Jacobs B. Epidemiology of traumatic and nontraumatic osteonecrosis. Clin Orthop Relat Res. 1978;130:51–67.

Steib-Furno S et al. Pregnancy-related hip diseases: incidence and diagnoses. Joint Bone Spine. 2007;74(4):373–8.

Sharareh B, Schwarzkopf R. Dysbaric osteonecrosis: a literature review of pathophysiology, clinical presentation, and management. Clin J Sport Med. 2014.

Schulte CM, Beelen DW. Avascular osteonecrosis after allogeneic hematopoietic stem-cell transplantation: diagnosis and gender matter. Transplantation. 2004;78(7):1055–63.

Jones L, Aaron RK. Circulatory pathology in osteonecrosis. In: Aaron RK, editor. Skeletal circulation in clinical practice. Singapore: World Scientific; 2015.