Osteonecrosis of the Femoral Head: Current state of Therapy and Outcomes Strategical Step-by-Step Approach
Main Article Content
Keywords
Osteonecrosis of the femoral head, Joint preserving surgery, Hip arthroplasty
Abstract
Osteonecrosis of the femoral head (ONFH) is a challenging multifactorial condition that affects mainly young patients. The disease can lead to collapse of the femoral head and secondary degenerative osteoarthritis of the hip joint. Various therapies for different stages of ONFH have been well established. However, results are largely heterogeneous and there is still no universal consensus regarding the optimal approach. In this article, the current therapies of ONFH and their outcomes will be reviewed and categorized based on the ARCO classification.
References
1. Zalavras CG, Lieberman JR. Osteonecrosis of the femoral head: Evaluation and treatment. J Am Acad Orthop Surg. 2014;22(7):455–64. https://doi.org/10.5435/JAAOS-22-07-455
2. Drescher W, Kyung-Hoi, Windsor, Russell E. Advances in specialist hip surgery (S.293). Springer Nature Switzerland AG 2021.
3. Salem KH, Brockert A-K, Mertens R, et al. Avascular necrosis after chemotherapy for haematological malignancy in childhood. J Bone Joint Surg. 2013;95-B (12):1708–13. https://doi.org/10.1302/0301-620X.95B12.30688
4. Mont MA, Jones LC, Hungerford DS. Nontraumatic osteonecrosis of the femoral head: Ten years later. J Bone Joint Surg Am. 2006;88(5):1117–32. https://doi.org/10.2106/JBJS.E.01041
5. Min BW, Song KS, Cho CH, et al. Untreated asymptomatic hips in patients with osteonecrosis of the femoral head. Clin Orthop Relat Res. 2008;466(5):1087–92. https://doi.org/10.1007/s11999-008-0191-x
6. Lavernia CJ, Sierra RJ, Grieco FR. Osteonecrosis of the femoral head. J Am Acad Orthop Surg. 1999;7(4):250–61. https://doi.org/10.5435/00124635-199907000-00005
7. Radl R, Hungerford M, Materna W, et al. Higher failure rate and stem migration of an uncemented femoral component in patients with femoral head osteonecrosis than in patients with osteoarthrosis. Acta Orthop. 2005;76(1):49–55. https://doi.org/10.1080/00016470510030319
8. Castro FP Jr, Barrack RL. Core decompression and conservative treatment for avascular necrosis of the femoral head: A meta-analysis. Am J Orthop (Belle Mead NJ). 2000;29(3):187–94.
9. Ficat Rp, Arlet J. Diagnostic de I’osteonecrose femorocapitale primitive au stade I (stade pre-radiologique). Rev Chir Orthop. 1968;54:637–48.
10. Chughtai M, Piuzzi NS, Khlopas A, et al. An evidence-based guide to the treatment of osteonecrosis of the femoral head. Bone Joint J. 2017 Oct;99-B (10):1267–79. https://doi.org/10.1302/0301-620X.99B10.BJJ-2017-0233.R2
11. Pierce TP, Jauregui JJ, Elmallah RK, et al. A current review of core decompression in the treatment of osteonecrosis of the femoral head. Curr Rev Musculoskelet Med. 2015;8(3):228–32. https://doi.org/10.1007/s12178-015-9280-0
12. Calori GM, Mazza E, Colombo A, et al. Core decompression and biotechnologies in the treatment of avascular necrosis of the femoral head. EFORT Open Rev. 2017;2(2):41–50. https://doi.org/10.1302/2058-5241.2.150006
13. Tripathy SK, Goyal T, Sen RK. Management of femoral head osteonecrosis: Current concepts. Indian J Orthop. 2015;49:28–45. https://doi.org/10.4103/0019-5413.143911
14. Wang A, Ren M, Wang J. The pathogenesis of steroid-induced osteonecrosis of the femoral head: A systematic review of the literature. Gene. 2018;671:103–9. https://doi.org/10.1016/j.gene.2018.05.091
15. Hernigou P, Beaujean F, Lambotte JC. Decrease in the mesenchymal stem-cell pool in the proximal femur in corticosteroid-induced osteonecrosis. J Bone Joint Surg Br. 1999;81(2):349–55. https://doi.org/10.1302/0301-620x.81b2.8818
16. Sun Y, Feng Y, Zhang C. The effect of bone marrow mononuclear cells on vascularization and bone regeneration in steroid-induced osteonecrosis of the femoral head. Joint Bone Spine 2009;76:685–90. https://doi.org/10.1016/j.jbspin.2009.04.002
17. Lee HS, Huang GT, Chiang H, et al. Multipotential mesenchymal stem cells from femoral bone marrow near the site of osteonecrosis. Stem Cells. 2003;21(2):190–9. https://doi.org/10.1634/stemcells.21-2-190
18. Li C, Li G, Liu M, et al. Paracrine effect of inflammatory cytokine-activated bone marrow mesenchymal stem cells and its role in osteoblast function. J Biosci Bioeng. 2016;121(2):213–9. https://doi.org/10.1016/j.jbiosc.2015.05.017
19. Gangji V, Toungouz M, Hauzeur JP. Stem cell therapy for osteonecrosis of the femoral head. Expert Opin Biol Ther. 2005;5(4):437–42. https://doi.org/10.1517/14712598.5.4.437
20. Hernigou P, Beaujean F. Treatment of osteonecrosis with autologous bone marrow grafting. Clin Orthop Relat Res. 2002;(405):14–23. https://doi.org/10.1097/00003086-200212000-00003
21. Ma Y, Wang T, Liao J, et al. Efficacy of autologous bone marrow buffy coat grafting combined with core decompression in patients with avascular necrosis of femoral head: A prospective, double-blinded, randomized, controlled study. Stem Cell Res Ther. 2014;5(5):115. https://doi.org/10.1186/scrt505
22. Hernigou P, Dubory A, Homma Y, et al. Cell therapy versus simultaneous contralateral decompression in symptomatic corticosteroid osteonecrosis: A thirty year follow-up prospective randomized study of one hundred and twenty five adult patients. Int Orthop. 2018;42(7):1639–49. https://doi.org/10.1007/s00264-018-3941-8
23. Hauzeur JP, De Maertelaer V, Baudoux E. Inefficacy of autologous bone marrow concentrate in stage three osteonecrosis: A randomized controlled double-blind trial. Int Orthop. 2018;42(7):1429–35. https://doi.org/10.1007/s00264-017-3650-8
24. Eppley BL, Woodell JE, Higgins J. Platelet quantification and growth factor analysis from platelet-rich plasma: Implications for wound healing. Plast Reconstr Surg. 2004;114(6):1502–8. https://doi.org/10.1097/01.prs.0000138251.07040.51
25. Yokota K, Ishida O, Sunagawa T, et al. Platelet-rich plasma accelerated surgical angio-genesis in vascular-implanted necrotic bone: An experimental study in rabbits. Acta Orthop. 2008;79(1):106–10. https://doi.org/10.1080/17453670710014842
26. Tao SC, Yuan T, Rui BY, et al. Exosomes derived from human platelet-rich plasma prevent apoptosis induced by glucocorticoid-associated endoplasmic reticulum stress in rat osteonecrosis of the femoral head via the Akt/Bad/Bcl-2 signal pathway. Theranostics. 2017;7(3):733–50. https://doi.org/10.7150/thno.17450
27. Tong S, Yin J, Liu J. Platelet-rich plasma has beneficial effects in mice with osteonecrosis of the femoral head by promoting angiogenesis. Exp Ther Med. 2018;15(2):1781–8. https://doi.org/10.3892/etm.2017.5655
28. Han J, Gao F, Li Y, et al. The use of platelet-rich plasma for the treatment of osteonecrosis of the femoral head: A systematic review. Biomed Res Int. 2020;2020:2642439. https://doi.org/10.1155/2020/2642439
29. Aggarwal AK, Poornalingam K, Jain A, et al. Combining platelet-rich plasma instillation with core decompression improves functional outcome and delays progression in early-stage avascular necrosis of femoral head: A 4.5-to 6-year prospective randomized comparative study. J Arthroplasty. 2021;36(1):54–61. https://doi.org/10.1016/j.arth.2020.07.010
30. Rocchi M, Del Piccolo N, Mazzotta A, et al. Core decompression with bone chips allograft in combination with fibrin platelet-rich plasma and concentrated autologous mesenchymal stromal cells, isolated from bone marrow: Results for the treatment of avascular necrosis of the femoral head after 2 years minimum follow-up. Hip Int. 2020;30(2_suppl):3–12. https://doi.org/10.1177/1120700020964996
31. Davis JB, Fagan TE, Beals RK. Follow-up notes on articles previously published in the journal. Muscle-pedicle bone graft in hip fusion. J Bone Joint Surg Am. 1971;53(8):1645–7.
32. Yang F, Wei Q, Chen X, et al. Vascularized pedicle iliac bone grafts as a hip-preserving surgery for femur head necrosis: A systematic review. J Orthop Surg Res. 2019;14(1):270. https://doi.org/10.1186/s13018-019-1262-2
33. Plakseychuk AY, Kim SY, Park BC, et al. Vascularized compared with nonvascularized fibular grafting for the treatment of osteonecrosis of the femoral head. J Bone Joint Surg Am. 2003;85(4):589–96. https://doi.org/10.2106/00004623-200304000-00001
34. Yen CY, Tu YK, Ma CH, et al. Osteonecrosis of the femoral head: Comparison of clinical results for vascularized iliac and fibula bone grafting. J Reconstr Microsurg. 2006;22(1):21–4. https://doi.org/10.1055/s-2006-931902
35. Wassenaar RP, Verburg H, Taconis WK, et al. Avascular osteonecrosis of the femoral head treated with a vascularized iliac bone graft: Preliminary results and follow-up with radiography and MR imaging. Radiographics. 1996;16(3):585–94. https://doi.org/10.1148/radiographics.16.3.8897626
36. Urbaniak JR, Coogan PG, Gunneson EB, et al. Treatment of osteonecrosis of the femoral head with free vascularized fibular grafting. A long-term follow-up study of one hundred and three hips. J Bone Joint Surg Am. 1995;77(5):681–94. https://doi.org/10.2106/00004623-199505000-00004
37. Tripathy SK, Goyal T, Sen RK. Management of femoral head osteonecrosis: Current concepts. Indian J Orthop. 2015;49(1):28–45. https://doi.org/10.4103/0019-5413.143911
38. Leibold CS, Schmaranzer F, Siebenrock KA, et al. Femoral osteotomies for the treatment of avascular necrosis of the femoral head. Oper Orthop Traumatol. 2020 Apr;32(2):116–26. https://doi.org/10.1007/s00064-019-00642-x
39. Sugioka Y. Proximal femoral osteotomies in the treatment of idiopathic and steroid-induced osteonecrosis of the femoral head. In: Schoutens A, Arlet J, Gardeniers JWM, Hughes SPF, editors. Bone circulation and vascularization in normal and pathological conditions. NATO ASI Series (Series A: Life Sciences). Boston, MA: Springer; 1993, Vol 247.
40. Sakano S, Hasegawa Y, Torii Y, et al. Curved intertrochanteric varus osteotomy for osteonecrosis of the femoral head. J Bone Joint Surg Br. 2004;86(3):359–65. https://doi.org/10.1302/0301-620x.86b3.14383
41. Zhao G, Yamamoto T, Ikemura S, et al. Radiological outcome analysis of transtrochanteric curved varus osteotomy for osteonecrosis of the femoral head at a mean follow-up of 12.4 years. J Bone Joint Surg Br. 2010;92(6):781–6. https://doi.org/10.1302/0301-620X.92B6.23621
42. Atilla B, Bakırcıoğlu S, Shope AJ, et al. Joint-preserving procedures for osteonecrosis of the femoral head. EFORT Open Rev. 2020;4(12):647–58. https://doi.org/10.1302/2058-5241.4.180073
43. Dean MT, Cabanela ME. Transtrochanteric anterior rotational osteotomy for avascular necrosis of the femoral head. Long-term results. J Bone Joint Surg Br. 1993;75(4):597–601. https://doi.org/10.1302/0301-620X.75B4.8331115
44. Lee YK, Park CH, Ha YC, et al. Comparison of surgical parameters and results between curved varus osteotomy and rotational osteotomy for osteonecrosis of the femoral head. Clin Orthop Surg. 2017;9(2):160–8. https://doi.org/10.4055/cios.2017.9.2.160
45. Capone A, Bienati F, Marongiuet G, et al. Short stem total hip arthroplasty for osteonecrosis of the femoral head in patients 60 years or younger: A 3- to 10-year follow-up study. BMC Musculoskelet Disord. 2017;18(1):301. https://doi.org/10.1186/s12891-017-1662-6
46. Stauffer RN. Ten-year follow-up study of total hip replacement. J Bone Jt Surg Am. 1982;64:983–90.
47. Chandler HP, Reineck FT, Wixson RL, et al. Total hip replacement in patients younger than thirty years old. A five-year follow-up study. J Bone Joint Surg Am. 1981;63(9):1426–34.
48. Cornell CN, Salvati EA, Pellicci PM. Long-term follow-up of total hip replacement in patients with osteonecrosis. Orthop Clin North Am. 1985;16:757–69.
49. Singh JA, Chen J, Inacio MC, et al. An underlying diagnosis of osteonecrosis of bone is associated with worse outcomes than osteoarthritis after total hip arthroplasty. BMC Musculoskelet Disord. 2017;18(1):8. https://doi.org/10.1186/s12891-016-1385-0
50. Yuan B, Taunton MJ, Trousdale RT. Total hip arthroplasty for alcoholic osteonecrosis of the femoral head. Orthopedics 2009;32(6):400. https://doi.org/10.3928/01477447-20090511-06
51. Acurio MT, Friedman RJ. Hip arthroplasty in patients with sickle-cell haemoglobinopathy. J Bone Joint Surg Br. 1992;74(3):367–71. https://doi.org/10.1302/0301-620X.74B3.1587879
52. Stromboni M, Menguy F, Hardy P, et al. Total hip arthroplasty and femoral head osteonecrosis in renal transplant recipients]. Rev Chir Orthop Reparatrice Appar Mot. 2002;88(5):467–74.
53. Johannson HR, Zywiel MG, Marker DR, et al. Osteonecrosis is not a predictor of poor outcomes in primary total hip arthroplasty: A systematic literature review. Int Orthop. 2011;35(4):465-73. https://doi.org/10.1007/s00264-010-0979-7
54. Ponzio DY, Pitta M, Carroll KM, et al. Hip arthroplasty for osteonecrosis of the femoral head secondary to alcohol abuse. Arthroplast Today. 2018;5(2):172-175. https://doi.org/10.1016/j.artd.2018.07.003
55. Ilyas I, Alrumaih HA, Rabbani S. Noncemented total hip arthroplasty in sickle-cell disease: Long-term results. J Arthroplasty. 2018;33(2):477–81. https://doi.org/10.1016/j.arth.2017.09.010
56. Arlot ME, Bonjean M, Chavassieux PM, et al. Bone histology in adults with aseptic necrosis. Histomorphometric evaluation of iliac biopsies in seventy-seven patients. J Bone Joint Surg [Am]. 1983;65:1319–27.
57. Tingart M, Beckmann J, Opolka A, et al. Analysis of bone matrix composition and trabecular microarchitecture of the femoral metaphysis in patients with osteonecrosis of the femoral head. J Orthop Res. 2009; 27:1175–81. https://doi.org/10.1002/jor.20873
58. Laroche M, Costa L, Bernard J, et al. Dual-energy X‑ray absorptiometry in osteonecrosis of the femoral head. Rev Rhum Engl Ed. 1998;65: 393–96.
59. Calder JD, Pearse MF, Revell PA. The extent of osteocyte death in the proximal femur of patients with osteonecrosis of the femoral head. J Bone Joint Surg. 2001;83:419–422. https://doi.org/10.1302/0301-620x.83b3.10793
60. Zeh A, Weise A, Vasarhelyi A, et al. Medium-term results of the Mayo™ short-stem hip prosthesis after avascular necrosis of the femoral head]. Z Orthop Unfall. 2011;149(2):200–5. https://doi.org/10.1055/s-0030-1270710
61. Suksathien Y, Sueajui J. Mid-term results of short stem total hip arthroplasty in patients with osteonecrosis of the femoral head. Hip Int. 2019;29(6):603-608. https://doi.org/10.1177/1120700018816011
62. Ajmal M, Matas AJ, Kuskowski M, et al. Does statin usage reduce the risk of corticosteroid-related osteonecrosis in renal transplant population? Orthop Clin North Am. 2009;40(2):235–9. https://doi.org/10.1016/j.ocl.2009.01.004
63. Disch AC, Matziolis G, Perka C. The management of necrosis-associated and idiopathic bone-marrow oedema of the proximal femur by intravenous iloprost. J Bone Joint Surg Br. 2005;87(4):560–4. https://doi.org/10.1302/0301-620X.87B4.15658
64. Claßen T, Becker A, Landgraeber S, et al. Long-term clinical results after iloprost treatment for bone marrow edema and avascular necrosis. Orthop Rev (Pavia). 2016;8(1):6150. https://doi.org/10.4081/or.2016.6150
65. Petek D, Hannouche D, Suva D. Osteonecrosis of the femoral head: Pathophysiology and current concepts of treatment. EFORT Open Rev. 2019;4(3):85–97. https://doi.org/10.1302/2058-5241.4.180036
66. Chen CH, Chang JK, Lai KA, et al. Alendronate in the prevention of collapse of the femoral head in nontraumatic osteonecrosis: A two-year multicenter, prospective, randomized, double-blind, placebo-controlled study. Arthritis Rheum. 2012;64(5):1572–8. https://doi.org/10.1002/art.33498
67. Zhao W, Gao Y, Zhang S, et al. Extracorporeal shock wave therapy for bone marrow edema syndrome in patients with osteonecrosis of the femoral head: A retrospective cohort study. J Orthop Surg Res. 2021;16(1):21. https://doi.org/10.1186/s13018-020-02159-7
68. Ando W, Sakai T, Fukushima W, et al. Working group for ONFH guidelines, Sugano N. Japanese Orthopaedic Association 2019 Guidelines for osteonecrosis of the femoral head. J Orthop Sci. 2021;26(1):46–68. https://doi.org/10.1016/j.jos.2020.06.013
69. Hisatome T, Yasunaga Y, Takahashi K, et al. Progressive collapse of transposed necrotic area after transtrochanteric rotational osteotomy for osteonecrosis of the femoral head induces osteoarthritic change: Mid-term results of transtrochanteric rotational osteotomy for osteonecrosis of the femoral head. Arch Orthop Trauma Surg. 2004;124(2):77–81. https://doi.org/10.1007/s00402-003-0610-0
70. Hiranuma Y, Atsumi T, Kajiwara T, et al. Evaluation of instability after transtrochanteric anterior rotational osteotomy for nontraumatic osteonecrosis of the femoral head. J Orthop Sci. 2009;14(5):535–42. https://doi.org/10.1007/s00776-009-1363-6
71. Hungerford DS. Treatment of osteonecrosis of the femoral head: Everything’s new. J Arthroplasty 2007;22:91–4. https://doi.org/10.1016/j.arth.2007.02.009
72. Ha YC, Kim HJ, Kim SY, et al. Effects of age and body mass index on the results of transtrochanteric rotational osteotomy for femoral head osteonecrosis: Surgical technique. J Bone Joint Surg Am. 2011;93 Suppl 1:75–84. https://doi.org/10.2106/JBJS.J.01215
2. Drescher W, Kyung-Hoi, Windsor, Russell E. Advances in specialist hip surgery (S.293). Springer Nature Switzerland AG 2021.
3. Salem KH, Brockert A-K, Mertens R, et al. Avascular necrosis after chemotherapy for haematological malignancy in childhood. J Bone Joint Surg. 2013;95-B (12):1708–13. https://doi.org/10.1302/0301-620X.95B12.30688
4. Mont MA, Jones LC, Hungerford DS. Nontraumatic osteonecrosis of the femoral head: Ten years later. J Bone Joint Surg Am. 2006;88(5):1117–32. https://doi.org/10.2106/JBJS.E.01041
5. Min BW, Song KS, Cho CH, et al. Untreated asymptomatic hips in patients with osteonecrosis of the femoral head. Clin Orthop Relat Res. 2008;466(5):1087–92. https://doi.org/10.1007/s11999-008-0191-x
6. Lavernia CJ, Sierra RJ, Grieco FR. Osteonecrosis of the femoral head. J Am Acad Orthop Surg. 1999;7(4):250–61. https://doi.org/10.5435/00124635-199907000-00005
7. Radl R, Hungerford M, Materna W, et al. Higher failure rate and stem migration of an uncemented femoral component in patients with femoral head osteonecrosis than in patients with osteoarthrosis. Acta Orthop. 2005;76(1):49–55. https://doi.org/10.1080/00016470510030319
8. Castro FP Jr, Barrack RL. Core decompression and conservative treatment for avascular necrosis of the femoral head: A meta-analysis. Am J Orthop (Belle Mead NJ). 2000;29(3):187–94.
9. Ficat Rp, Arlet J. Diagnostic de I’osteonecrose femorocapitale primitive au stade I (stade pre-radiologique). Rev Chir Orthop. 1968;54:637–48.
10. Chughtai M, Piuzzi NS, Khlopas A, et al. An evidence-based guide to the treatment of osteonecrosis of the femoral head. Bone Joint J. 2017 Oct;99-B (10):1267–79. https://doi.org/10.1302/0301-620X.99B10.BJJ-2017-0233.R2
11. Pierce TP, Jauregui JJ, Elmallah RK, et al. A current review of core decompression in the treatment of osteonecrosis of the femoral head. Curr Rev Musculoskelet Med. 2015;8(3):228–32. https://doi.org/10.1007/s12178-015-9280-0
12. Calori GM, Mazza E, Colombo A, et al. Core decompression and biotechnologies in the treatment of avascular necrosis of the femoral head. EFORT Open Rev. 2017;2(2):41–50. https://doi.org/10.1302/2058-5241.2.150006
13. Tripathy SK, Goyal T, Sen RK. Management of femoral head osteonecrosis: Current concepts. Indian J Orthop. 2015;49:28–45. https://doi.org/10.4103/0019-5413.143911
14. Wang A, Ren M, Wang J. The pathogenesis of steroid-induced osteonecrosis of the femoral head: A systematic review of the literature. Gene. 2018;671:103–9. https://doi.org/10.1016/j.gene.2018.05.091
15. Hernigou P, Beaujean F, Lambotte JC. Decrease in the mesenchymal stem-cell pool in the proximal femur in corticosteroid-induced osteonecrosis. J Bone Joint Surg Br. 1999;81(2):349–55. https://doi.org/10.1302/0301-620x.81b2.8818
16. Sun Y, Feng Y, Zhang C. The effect of bone marrow mononuclear cells on vascularization and bone regeneration in steroid-induced osteonecrosis of the femoral head. Joint Bone Spine 2009;76:685–90. https://doi.org/10.1016/j.jbspin.2009.04.002
17. Lee HS, Huang GT, Chiang H, et al. Multipotential mesenchymal stem cells from femoral bone marrow near the site of osteonecrosis. Stem Cells. 2003;21(2):190–9. https://doi.org/10.1634/stemcells.21-2-190
18. Li C, Li G, Liu M, et al. Paracrine effect of inflammatory cytokine-activated bone marrow mesenchymal stem cells and its role in osteoblast function. J Biosci Bioeng. 2016;121(2):213–9. https://doi.org/10.1016/j.jbiosc.2015.05.017
19. Gangji V, Toungouz M, Hauzeur JP. Stem cell therapy for osteonecrosis of the femoral head. Expert Opin Biol Ther. 2005;5(4):437–42. https://doi.org/10.1517/14712598.5.4.437
20. Hernigou P, Beaujean F. Treatment of osteonecrosis with autologous bone marrow grafting. Clin Orthop Relat Res. 2002;(405):14–23. https://doi.org/10.1097/00003086-200212000-00003
21. Ma Y, Wang T, Liao J, et al. Efficacy of autologous bone marrow buffy coat grafting combined with core decompression in patients with avascular necrosis of femoral head: A prospective, double-blinded, randomized, controlled study. Stem Cell Res Ther. 2014;5(5):115. https://doi.org/10.1186/scrt505
22. Hernigou P, Dubory A, Homma Y, et al. Cell therapy versus simultaneous contralateral decompression in symptomatic corticosteroid osteonecrosis: A thirty year follow-up prospective randomized study of one hundred and twenty five adult patients. Int Orthop. 2018;42(7):1639–49. https://doi.org/10.1007/s00264-018-3941-8
23. Hauzeur JP, De Maertelaer V, Baudoux E. Inefficacy of autologous bone marrow concentrate in stage three osteonecrosis: A randomized controlled double-blind trial. Int Orthop. 2018;42(7):1429–35. https://doi.org/10.1007/s00264-017-3650-8
24. Eppley BL, Woodell JE, Higgins J. Platelet quantification and growth factor analysis from platelet-rich plasma: Implications for wound healing. Plast Reconstr Surg. 2004;114(6):1502–8. https://doi.org/10.1097/01.prs.0000138251.07040.51
25. Yokota K, Ishida O, Sunagawa T, et al. Platelet-rich plasma accelerated surgical angio-genesis in vascular-implanted necrotic bone: An experimental study in rabbits. Acta Orthop. 2008;79(1):106–10. https://doi.org/10.1080/17453670710014842
26. Tao SC, Yuan T, Rui BY, et al. Exosomes derived from human platelet-rich plasma prevent apoptosis induced by glucocorticoid-associated endoplasmic reticulum stress in rat osteonecrosis of the femoral head via the Akt/Bad/Bcl-2 signal pathway. Theranostics. 2017;7(3):733–50. https://doi.org/10.7150/thno.17450
27. Tong S, Yin J, Liu J. Platelet-rich plasma has beneficial effects in mice with osteonecrosis of the femoral head by promoting angiogenesis. Exp Ther Med. 2018;15(2):1781–8. https://doi.org/10.3892/etm.2017.5655
28. Han J, Gao F, Li Y, et al. The use of platelet-rich plasma for the treatment of osteonecrosis of the femoral head: A systematic review. Biomed Res Int. 2020;2020:2642439. https://doi.org/10.1155/2020/2642439
29. Aggarwal AK, Poornalingam K, Jain A, et al. Combining platelet-rich plasma instillation with core decompression improves functional outcome and delays progression in early-stage avascular necrosis of femoral head: A 4.5-to 6-year prospective randomized comparative study. J Arthroplasty. 2021;36(1):54–61. https://doi.org/10.1016/j.arth.2020.07.010
30. Rocchi M, Del Piccolo N, Mazzotta A, et al. Core decompression with bone chips allograft in combination with fibrin platelet-rich plasma and concentrated autologous mesenchymal stromal cells, isolated from bone marrow: Results for the treatment of avascular necrosis of the femoral head after 2 years minimum follow-up. Hip Int. 2020;30(2_suppl):3–12. https://doi.org/10.1177/1120700020964996
31. Davis JB, Fagan TE, Beals RK. Follow-up notes on articles previously published in the journal. Muscle-pedicle bone graft in hip fusion. J Bone Joint Surg Am. 1971;53(8):1645–7.
32. Yang F, Wei Q, Chen X, et al. Vascularized pedicle iliac bone grafts as a hip-preserving surgery for femur head necrosis: A systematic review. J Orthop Surg Res. 2019;14(1):270. https://doi.org/10.1186/s13018-019-1262-2
33. Plakseychuk AY, Kim SY, Park BC, et al. Vascularized compared with nonvascularized fibular grafting for the treatment of osteonecrosis of the femoral head. J Bone Joint Surg Am. 2003;85(4):589–96. https://doi.org/10.2106/00004623-200304000-00001
34. Yen CY, Tu YK, Ma CH, et al. Osteonecrosis of the femoral head: Comparison of clinical results for vascularized iliac and fibula bone grafting. J Reconstr Microsurg. 2006;22(1):21–4. https://doi.org/10.1055/s-2006-931902
35. Wassenaar RP, Verburg H, Taconis WK, et al. Avascular osteonecrosis of the femoral head treated with a vascularized iliac bone graft: Preliminary results and follow-up with radiography and MR imaging. Radiographics. 1996;16(3):585–94. https://doi.org/10.1148/radiographics.16.3.8897626
36. Urbaniak JR, Coogan PG, Gunneson EB, et al. Treatment of osteonecrosis of the femoral head with free vascularized fibular grafting. A long-term follow-up study of one hundred and three hips. J Bone Joint Surg Am. 1995;77(5):681–94. https://doi.org/10.2106/00004623-199505000-00004
37. Tripathy SK, Goyal T, Sen RK. Management of femoral head osteonecrosis: Current concepts. Indian J Orthop. 2015;49(1):28–45. https://doi.org/10.4103/0019-5413.143911
38. Leibold CS, Schmaranzer F, Siebenrock KA, et al. Femoral osteotomies for the treatment of avascular necrosis of the femoral head. Oper Orthop Traumatol. 2020 Apr;32(2):116–26. https://doi.org/10.1007/s00064-019-00642-x
39. Sugioka Y. Proximal femoral osteotomies in the treatment of idiopathic and steroid-induced osteonecrosis of the femoral head. In: Schoutens A, Arlet J, Gardeniers JWM, Hughes SPF, editors. Bone circulation and vascularization in normal and pathological conditions. NATO ASI Series (Series A: Life Sciences). Boston, MA: Springer; 1993, Vol 247.
40. Sakano S, Hasegawa Y, Torii Y, et al. Curved intertrochanteric varus osteotomy for osteonecrosis of the femoral head. J Bone Joint Surg Br. 2004;86(3):359–65. https://doi.org/10.1302/0301-620x.86b3.14383
41. Zhao G, Yamamoto T, Ikemura S, et al. Radiological outcome analysis of transtrochanteric curved varus osteotomy for osteonecrosis of the femoral head at a mean follow-up of 12.4 years. J Bone Joint Surg Br. 2010;92(6):781–6. https://doi.org/10.1302/0301-620X.92B6.23621
42. Atilla B, Bakırcıoğlu S, Shope AJ, et al. Joint-preserving procedures for osteonecrosis of the femoral head. EFORT Open Rev. 2020;4(12):647–58. https://doi.org/10.1302/2058-5241.4.180073
43. Dean MT, Cabanela ME. Transtrochanteric anterior rotational osteotomy for avascular necrosis of the femoral head. Long-term results. J Bone Joint Surg Br. 1993;75(4):597–601. https://doi.org/10.1302/0301-620X.75B4.8331115
44. Lee YK, Park CH, Ha YC, et al. Comparison of surgical parameters and results between curved varus osteotomy and rotational osteotomy for osteonecrosis of the femoral head. Clin Orthop Surg. 2017;9(2):160–8. https://doi.org/10.4055/cios.2017.9.2.160
45. Capone A, Bienati F, Marongiuet G, et al. Short stem total hip arthroplasty for osteonecrosis of the femoral head in patients 60 years or younger: A 3- to 10-year follow-up study. BMC Musculoskelet Disord. 2017;18(1):301. https://doi.org/10.1186/s12891-017-1662-6
46. Stauffer RN. Ten-year follow-up study of total hip replacement. J Bone Jt Surg Am. 1982;64:983–90.
47. Chandler HP, Reineck FT, Wixson RL, et al. Total hip replacement in patients younger than thirty years old. A five-year follow-up study. J Bone Joint Surg Am. 1981;63(9):1426–34.
48. Cornell CN, Salvati EA, Pellicci PM. Long-term follow-up of total hip replacement in patients with osteonecrosis. Orthop Clin North Am. 1985;16:757–69.
49. Singh JA, Chen J, Inacio MC, et al. An underlying diagnosis of osteonecrosis of bone is associated with worse outcomes than osteoarthritis after total hip arthroplasty. BMC Musculoskelet Disord. 2017;18(1):8. https://doi.org/10.1186/s12891-016-1385-0
50. Yuan B, Taunton MJ, Trousdale RT. Total hip arthroplasty for alcoholic osteonecrosis of the femoral head. Orthopedics 2009;32(6):400. https://doi.org/10.3928/01477447-20090511-06
51. Acurio MT, Friedman RJ. Hip arthroplasty in patients with sickle-cell haemoglobinopathy. J Bone Joint Surg Br. 1992;74(3):367–71. https://doi.org/10.1302/0301-620X.74B3.1587879
52. Stromboni M, Menguy F, Hardy P, et al. Total hip arthroplasty and femoral head osteonecrosis in renal transplant recipients]. Rev Chir Orthop Reparatrice Appar Mot. 2002;88(5):467–74.
53. Johannson HR, Zywiel MG, Marker DR, et al. Osteonecrosis is not a predictor of poor outcomes in primary total hip arthroplasty: A systematic literature review. Int Orthop. 2011;35(4):465-73. https://doi.org/10.1007/s00264-010-0979-7
54. Ponzio DY, Pitta M, Carroll KM, et al. Hip arthroplasty for osteonecrosis of the femoral head secondary to alcohol abuse. Arthroplast Today. 2018;5(2):172-175. https://doi.org/10.1016/j.artd.2018.07.003
55. Ilyas I, Alrumaih HA, Rabbani S. Noncemented total hip arthroplasty in sickle-cell disease: Long-term results. J Arthroplasty. 2018;33(2):477–81. https://doi.org/10.1016/j.arth.2017.09.010
56. Arlot ME, Bonjean M, Chavassieux PM, et al. Bone histology in adults with aseptic necrosis. Histomorphometric evaluation of iliac biopsies in seventy-seven patients. J Bone Joint Surg [Am]. 1983;65:1319–27.
57. Tingart M, Beckmann J, Opolka A, et al. Analysis of bone matrix composition and trabecular microarchitecture of the femoral metaphysis in patients with osteonecrosis of the femoral head. J Orthop Res. 2009; 27:1175–81. https://doi.org/10.1002/jor.20873
58. Laroche M, Costa L, Bernard J, et al. Dual-energy X‑ray absorptiometry in osteonecrosis of the femoral head. Rev Rhum Engl Ed. 1998;65: 393–96.
59. Calder JD, Pearse MF, Revell PA. The extent of osteocyte death in the proximal femur of patients with osteonecrosis of the femoral head. J Bone Joint Surg. 2001;83:419–422. https://doi.org/10.1302/0301-620x.83b3.10793
60. Zeh A, Weise A, Vasarhelyi A, et al. Medium-term results of the Mayo™ short-stem hip prosthesis after avascular necrosis of the femoral head]. Z Orthop Unfall. 2011;149(2):200–5. https://doi.org/10.1055/s-0030-1270710
61. Suksathien Y, Sueajui J. Mid-term results of short stem total hip arthroplasty in patients with osteonecrosis of the femoral head. Hip Int. 2019;29(6):603-608. https://doi.org/10.1177/1120700018816011
62. Ajmal M, Matas AJ, Kuskowski M, et al. Does statin usage reduce the risk of corticosteroid-related osteonecrosis in renal transplant population? Orthop Clin North Am. 2009;40(2):235–9. https://doi.org/10.1016/j.ocl.2009.01.004
63. Disch AC, Matziolis G, Perka C. The management of necrosis-associated and idiopathic bone-marrow oedema of the proximal femur by intravenous iloprost. J Bone Joint Surg Br. 2005;87(4):560–4. https://doi.org/10.1302/0301-620X.87B4.15658
64. Claßen T, Becker A, Landgraeber S, et al. Long-term clinical results after iloprost treatment for bone marrow edema and avascular necrosis. Orthop Rev (Pavia). 2016;8(1):6150. https://doi.org/10.4081/or.2016.6150
65. Petek D, Hannouche D, Suva D. Osteonecrosis of the femoral head: Pathophysiology and current concepts of treatment. EFORT Open Rev. 2019;4(3):85–97. https://doi.org/10.1302/2058-5241.4.180036
66. Chen CH, Chang JK, Lai KA, et al. Alendronate in the prevention of collapse of the femoral head in nontraumatic osteonecrosis: A two-year multicenter, prospective, randomized, double-blind, placebo-controlled study. Arthritis Rheum. 2012;64(5):1572–8. https://doi.org/10.1002/art.33498
67. Zhao W, Gao Y, Zhang S, et al. Extracorporeal shock wave therapy for bone marrow edema syndrome in patients with osteonecrosis of the femoral head: A retrospective cohort study. J Orthop Surg Res. 2021;16(1):21. https://doi.org/10.1186/s13018-020-02159-7
68. Ando W, Sakai T, Fukushima W, et al. Working group for ONFH guidelines, Sugano N. Japanese Orthopaedic Association 2019 Guidelines for osteonecrosis of the femoral head. J Orthop Sci. 2021;26(1):46–68. https://doi.org/10.1016/j.jos.2020.06.013
69. Hisatome T, Yasunaga Y, Takahashi K, et al. Progressive collapse of transposed necrotic area after transtrochanteric rotational osteotomy for osteonecrosis of the femoral head induces osteoarthritic change: Mid-term results of transtrochanteric rotational osteotomy for osteonecrosis of the femoral head. Arch Orthop Trauma Surg. 2004;124(2):77–81. https://doi.org/10.1007/s00402-003-0610-0
70. Hiranuma Y, Atsumi T, Kajiwara T, et al. Evaluation of instability after transtrochanteric anterior rotational osteotomy for nontraumatic osteonecrosis of the femoral head. J Orthop Sci. 2009;14(5):535–42. https://doi.org/10.1007/s00776-009-1363-6
71. Hungerford DS. Treatment of osteonecrosis of the femoral head: Everything’s new. J Arthroplasty 2007;22:91–4. https://doi.org/10.1016/j.arth.2007.02.009
72. Ha YC, Kim HJ, Kim SY, et al. Effects of age and body mass index on the results of transtrochanteric rotational osteotomy for femoral head osteonecrosis: Surgical technique. J Bone Joint Surg Am. 2011;93 Suppl 1:75–84. https://doi.org/10.2106/JBJS.J.01215