Legg–Calvé–Perthes disease presenting with osteoarthritis: Mechanisms of the development and prospects of conservative therapy using bisphosphonates
Aleksei N. Kozhevnikov , Dmitrii B. Barsukov , Aigul R. Gubaeva
Pediatric Traumatology, Orthopaedics and Reconstructive Surgery ›› 2023, Vol. 11 ›› Issue (3) : 405 -416.
Legg–Calvé–Perthes disease presenting with osteoarthritis: Mechanisms of the development and prospects of conservative therapy using bisphosphonates
BACKGROUND: Aseptic necrosis of the femoral head in children remains a subject of great interest among specialists, despite its long history of study. The Legg–Calvé–Perthes disease is the most common form of aseptic necrosis of the femoral head in children. The necrotic lesion in the femoral head results from the blockage of the arterial blood supply to the epiphysis, leading to its infarction. Some children experience a more aggressive disease course, with signs of osteoarthritis, which can result in the early development of coxarthrosis. Numerous publications have demonstrated the successful use of bisphosphonates in adult patients with aseptic necrosis of the femoral head.
AIM: To generalize data on the use of bisphosphonates in children with the Legg–Calvé–Perthes disease presenting with signs of osteoarthritis through the analysis of contemporary global literature.
MATERIALS AND METHODS: A literature search was conducted in the open databases of PubMed, Science Direct, and Google Scholar, and the analysis depth spanned 20 years. The search terms used included “Legg–Calvé–Perthes disease,” “aseptic (avascular) necrosis of the femoral head,” and “bisphosphonates.” The review encompassed the literature on bisphosphonates, their biological action, effectiveness of their use in patients with aseptic necrosis of the femoral head, and results of our research.
RESULTS: Studies on the efficacy of bisphosphonates in children with Legg–Calvé–Perthes disease are limited. Currently, the effect of bisphosphonates on disease course and outcome is unknown. Despite this, mechanisms of chronic inflammation are increasingly mentioned in the literature, which may directly or indirectly influence the clinical course and outcome of the disease. The key is the hyperactivity of osteoclasts in osteonecrosis. The experience of using bisphosphonates in adult patients with aseptic necrosis of the femoral head had positive results in preventing the progression of the deformity of femoral head deformity.
CONCLUSIONS: Bisphosphonates are specific inhibitors of osteoclast activity, which has been used in many diseases. The results and inferences of using bisphosphonates in children with Legg–Calvé–Perthes disease will lead to the formulation of a new treatment algorithm.
avascular necrosis of the femoral head / Legg-Calve-Perthes disease / synovitis / osteoarthritis / bisphosphonates
| [1] |
Rodríguez-Olivas AO, Hernández-Zamora E, Reyes-Maldonado E. Legg-Calvé-Perthes disease overview. Orphanet J Rare Dis. 2022;17(1):125. DOI: 10.1186/s13023-022-02275-z |
| [2] |
Rodríguez-Olivas A.O., Hernández-Zamora E., Reyes-Maldonado E. Legg-Calvé-Perthes disease overview // Orphanet. J. Rare. Dis. 2022. Vol. 17. No. 1. P. 125. DOI: 10.1186/s13023-022-02275-z |
| [3] |
Kozhevnikov OV, Lysikov VA, Ivanov AV. Legg-Calve-Perthes disease: etiology, pathogenesis diagnosis and treatment. N.N. Priorov Journal of Traumatology and Orthopedics. 2017;24(1):77–87. (In Russ.) DOI: 10.17816/vto201724177-87 |
| [4] |
Кожевников О.В., Лысиков В.А., Иванов А.В. Болезнь Легга – Кальве – Пертеса: этиология, патогенез, диагностика и лечение // Вестник травматологии и ортопедии им. Н.Н. Приорова. 2017. Т. 24. № 1. С. 77–87. DOI: 10.17816/vto201724177-87 |
| [5] |
Shah H. Perthes disease: evaluation and management. Orthop Clin North Am. 2014;45(1):87–97. DOI: 10.1016/j.ocl.2013.08.005 |
| [6] |
Shah H. Perthes disease: evaluation and management // Orthop. Clin. North Am. 2014. Vol. 45. No. 1. P. 87–97. DOI: 10.1016/j.ocl.2013.08.005 |
| [7] |
Leo DG, Jones H, Murphy R, et al. The outcomes of Perthes’ disease. Bone Joint J. 2020;102-B(5):611–617. DOI: 10.1302/0301-620X.102B5.BJJ-2020-0072 |
| [8] |
Leo D.G., Jones H., Murphy R., et al. The outcomes of Perthes’ disease // Bone Joint J. 2020. Vol. 102-B. No. 5. P. 611–617. DOI: 10.1302/0301-620X.102B5.BJJ-2020-0072 |
| [9] |
Kim HK. Pathophysiology and new strategies for the treatment of Legg-Calve-Perthes disease. J Bone Joint Surg Am. 2012;94(7):659–669. DOI: 10.2106/JBJS.J.01834 |
| [10] |
Kim H.K. Pathophysiology and new strategies for the treatment of Legg-Calve-Perthes disease // J. Bone Joint Surg. Am. 2012. Vol. 94. No. 7. P. 659–669. DOI: 10.2106/JBJS.J.01834 |
| [11] |
Martí-Carvajal AJ, Solà I, Agreda-Pérez LH. Treatment for avascular necrosis of bone in people with sickle cell disease. Cochrane Database Syst Rev. 2019;12(12). DOI: 10.1002/14651858.CD004344.pub7 |
| [12] |
Martí-Carvajal A.J., Solà I., Agreda-Pérez L.H. Treatment for avascular necrosis of bone in people with sickle cell disease // Cochrane Database Syst. Rev. 2019. Vol. 12. No. 12. DOI: 10.1002/14651858.CD004344.pub7 |
| [13] |
Liu N, Zheng C, Wang Q, et al. Treatment of non-traumatic avascular necrosis of the femoral head (Review). Exp Ther Med. 2022;23(5):321. DOI: 10.3892/etm.2022.11250 |
| [14] |
Liu N., Zheng C., Wang Q., et al. Treatment of non-traumatic avascular necrosis of the femoral head (Review) // Exp. Ther. Med. 2022. Vol. 23. No. 5. P. 321. DOI: 10.3892/etm.2022.11250 |
| [15] |
Kumar V, Ali S, Verma V, et al. Do bisphosphonates alter the clinico-radiological profile of children with Perthes disease? A systematic review and meta-analysis. Eur Rev Med Pharmacol Sci. 2021;25(15):4875–4894. DOI: 10.26355/eurrev_202108_26445 |
| [16] |
Kumar V., Ali S., Verma V., et al. Do bisphosphonates alter the clinico-radiological profile of children with Perthes disease? A systematic review and meta-analysis // Eur. Rev. Med. Pharmacol. Sci. 2021. Vol. 25. No. 15. P. 4875–4894. DOI: 10.26355/eurrev_202108_26445 |
| [17] |
Krutikova NYu, Vinogradova AG. Legg–Calve–Perthes Disease. Current Pediatrics. 2015;14(5):548–552. (In Russ.) DOI: 10.15690/vsp.v14i5.1437 |
| [18] |
Крутикова Н.Ю., Виноградова А.Г. Болезнь Легга – Кальве – Пертеса // Вопросы современной педиатрии. 2015. Т. 14. № 5. С. 548–552. DOI: 10.15690/VSP.V14I5.1437 |
| [19] |
Pavone V, Chisari E, Vescio A, et al. Aetiology of Legg-Calvé-Perthes disease: a systematic review. World J Orthop. 2019;10(3):145–165. DOI: 10.5312/wjo.v10.i3.145 |
| [20] |
Pavone V., Chisari E., Vescio A., et al. Aetiology of Legg-Calvé-Perthes disease: a systematic review // World J. Orthop. 2019. Vol. 10. No. 3. P. 145–165. DOI: 10.5312/wjo.v10.i3.145 |
| [21] |
Gurion R, Tangpricha V, Yow E; et al. Atherosclerosis prevention in pediatric lupus erythematosus investigators. avascular necrosis in pediatric systemic lupus erythematosus: a brief report and review of the literature. Pediatr Rheumatol Online J. 2015;13:13. DOI: 10.1186/s12969-015-0008-x |
| [22] |
Gurion R., Tangpricha V., Yow E., et al. Atherosclerosis prevention in pediatric lupus erythematosus investigators. avascular necrosis in pediatric systemic lupus erythematosus: a brief report and review of the literature // Pediatr. Rheumatol. Online J. 2015. Vol. 13. P. 13. DOI: 10.1186/s12969-015-0008-x |
| [23] |
Kim HK. Legg-Calve-Perthes disease: etiology, pathogenesis, and biology. J Pediatr Orthop. 2011;31(2):S141–S146. DOI: 10.1097/BPO.0b013e318223b4bd |
| [24] |
Kim H.K. Legg-Calve-Perthes disease: etiology, pathogenesis, and biology // J. Pediatr. Orthop. 2011. Vol. 31. No. 2. P. S141–S146. DOI: 10.1097/BPO.0b013e318223b4bd |
| [25] |
Alexeeva EI., Dvoryakovskaya TM., Nikishina IP, et al. Systemic lupus erythematosus: clinical recommendations. Part 1. Current Pediatrics. 2018;17(1):19–37. (In Russ.) DOI: 10.15690/vsp.v17i1.1853 |
| [26] |
Алексеева Е.И., Дворяковская Т.М., Никишина И.П., и др. Системная красная волчанка: клинические рекомендации. Часть 1 // Вопросы современной педиатрии. 2018. Т. 17. № 1. С. 19–37. DOI: 10.15690/vsp.v17i1.1853 |
| [27] |
Sayarlioglu M, Yuzbasioglu N, Inanc M, et al. Risk factors for avascular bone necrosis in patients with systemic lupus erythematosus. Rheumatol Int. 2012;32(1):177–182. DOI: 10.1007/s00296-010-1597-9 |
| [28] |
Sayarlioglu M., Yuzbasioglu N., Inanc M., et al. Risk factors for avascular bone necrosis in patients with systemic lupus erythematosus // Rheumatol. Int. 2012. Vol. 32. No. 1. P. 177–182. DOI: 10.1007/s00296-010-1597-9 |
| [29] |
Benaziez F, Remilaoui A, Bahaz N, et al. Juvenile idiopathic arthritis and corticosteroid-induced osteonecrosis of the femoral head. Br J Rheumatol. 2022;61(2):4. DOI: 10.1093/rheumatology/keac496.004 |
| [30] |
Benaziez F., Remilaoui A., Bahaz N., et al. Juvenile idiopathic arthritis and corticosteroid-induced osteonecrosis of the femoral head // Br. J. Rheumatol. 2022. Vol. 61. No. 2. P. 4. DOI: 10.1093/rheumatology/keac496.004 |
| [31] |
Perry DC, Bruce CE, Pope D et al. Legg-Calve-Perthes disease in the UK: geographic and temporal trends in incidence reflecting differences in degree of deprivation in childhood. Arthritis Rheum. 2012;64(5):1673–1679. DOI: 10.1002/art.34316 |
| [32] |
Perry D.C., Bruce C.E., Pope D., et al. Legg-Calve-Perthes disease in the UK: geographic and temporal trends in incidence reflecting differences in degree of deprivation in childhood // Arthritis Rheum. 2012. Vol. 64. No. 5. P. 1673–1679. DOI: 10.1002/art.34316 |
| [33] |
Al-Naser S, Judd J, Clarke NMP. The effects of vitamin D deficiency on the natural progression of Perthes’ disease. Bone and Joint (BJJ). 2014;96-B(1):7. DOI: 10.1302/1358-992X.96BSUPP_1.BSCOS2013-007 |
| [34] |
Al-Naser S., Judd J., Clarke N.M.P. The effects of vitamin D deficiency on the natural progression of Perthes’ disease // Bone Joint (BJJ). 2014. Vol. 96-B. No. 1. P. 7. DOI: 10.1302/1358-992X.96BSUPP_1.BSCOS2013-007 |
| [35] |
Mailhot G, White JH. Vitamin D and immunity in infants and children. Nutrients. 2020;12(5):1233. DOI: 10.3390/nu12051233 |
| [36] |
Mailhot G., White J.H. Vitamin D and immunity in infants and children // Nutrients. 2020. Vol. 12. No. 5. P. 1233. DOI: 10.3390/nu12051233 |
| [37] |
Leandro MP, Almeida ND, Hocevar LS, et al. Polymorphisms and avascular necrosis in patients with sickle cell disease – a systematic review. Rev Paul Pediatr. 2022;40. DOI: 10.1590/1984-0462/2022/40/2021013IN |
| [38] |
Leandro M.P., Almeida N.D., Hocevar L.S., et al. Polymorphisms and avascular necrosis in patients with sickle cell disease – a systematic review // Rev. Paul. Pediatr. 2022. Vol. 40. DOI: 10.1590/1984-0462/2022/40/2021013IN |
| [39] |
Zhang Z, Zhu K, Dai H, et al. A novel mutation of COL2A1 in a large Chinese family with avascular necrosis of the femoral head. BMC Med Genomics. 2021;14(1):147. DOI: 10.1186/s12920-021-00995-y |
| [40] |
Zhang Z., Zhu K., Dai H., et al. A novel mutation of COL2A1 in a large Chinese family with avascular necrosis of the femoral head // BMC Med. Genomics. 2021. Vol. 14. No. 1. P. 147. DOI: 10.1186/s12920-021-00995-y |
| [41] |
Basit S, Khoshhal KI. Clinical and genetic characteristics of Legg-Calve-Perthes disease. J Musculoskelet Surg Res. 2022;6:1–8. DOI: 10.25259/JMSR_123_2021 |
| [42] |
Basit S., Khoshhal K.I. Clinical and genetic characteristics of Legg-Calve-Perthes disease // J. Musculoskelet. Surg. Res 2022. Vol. 6. No. 1. P. 1–8. DOI: 10.25259/JMSR_123_2021 |
| [43] |
Ren Y, Deng Z, Gokani V, et al. Anti-interleukin-6 therapy decreases hip synovitis and bone resorption and increases bone formation following ischemic osteonecrosis of the femoral head. J Bone Miner Res. 2021;36(2):357–368. DOI: 10.1002/jbmr.4191 |
| [44] |
Ren Y., Deng Z., Gokani V., et al. Anti-interleukin-6 therapy decreases hip synovitis and bone resorption and increases bone formation following ischemic osteonecrosis of the femoral head // J. Bone Miner. Res. 2021. Vol. 36. No. 2. P. 357–368. DOI: 10.1002/jbmr.4191 |
| [45] |
Campos LM, Kiss MH, D’Amico EA, et al. Antiphospholipid antibodies and antiphospholipid syndrome in 57 children and adolescents with systemic lupus erythematosus. Lupus. 2003;12(11):820–826. DOI: 10.1191/0961203303lu471oa |
| [46] |
Campos L.M., Kiss M.H., D’Amico E.A., et al. Antiphospholipid antibodies and antiphospholipid syndrome in 57 children and adolescents with systemic lupus erythematosus // Lupus. 2003. Vol. 12. No. 11. P. 820–826. DOI: 10.1191/0961203303lu471oa |
| [47] |
Kamiya N, Yamaguchi R, Adapala NS, et al. Legg-Calvé-Perthes disease produces chronic hip synovitis and elevation of interleukin-6 in the synovial fluid. J Bone Miner Res. 2015;30(6):1009–1013. DOI: 10.1002/jbmr.2435 |
| [48] |
Kamiya N., Yamaguchi R., Adapala N.S., et al. Legg-Calvé-Perthes disease produces chronic hip synovitis and elevation of interleukin-6 in the synovial fluid // J. Bone Miner. Res. 2015. Vol. 30. No. 6. P. 1009–1013. DOI: 10.1002/jbmr.2435 |
| [49] |
Wang C, Meng H, Wang Y, et al. Analysis of early stage osteonecrosis of the human femoral head and the mechanism of femoral head collapse. Int J Biol Sci. 2018;14(2):156–164. DOI: 10.7150/ijbs.18334 |
| [50] |
Wang C., Meng H., Wang Y., et al. Analysis of early stage osteonecrosis of the human femoral head and the mechanism of femoral head collapse // Int. J. Biol. Sci. 2018. Vol. 14. No. 2. P. 156–164. DOI: 10.7150/ijbs.18334 |
| [51] |
Li Y, Wang Y, Guo Y, et al. OPG and RANKL polymorphisms are associated with alcohol-induced osteonecrosis of the femoral head in the north area of China population in men. Medicine (Baltimore). 2016;95(25). DOI: 10.1097/MD.0000000000003981 |
| [52] |
Li Y., Wang Y., Guo Y., et al. OPG and RANKL polymorphisms are associated with alcohol-induced osteonecrosis of the femoral head in the north area of China population in men // Medicine (Baltimore). 2016. Vol. 95. No. 25. DOI: 10.1097/MD.0000000000003981 |
| [53] |
Gori F, Hofbauer LC, Dunstan CR, et al. The expression of osteoprotegerin and RANK ligand and the support of osteoclast formation by stromal-osteoblast lineage cells is developmentally regulated. Endocrinology. 2000;141:4768–4776. DOI: 10.1210/endo.141.12.7840 |
| [54] |
Gori F., Hofbauer L.C., Dunstan C.R., et al. The expression of osteoprotegerin and RANK ligand and the support of osteoclast formation by stromal-osteoblast lineage cells is developmentally regulated // Endocrinology. 2000. Vol. 141. No. 12. P. 4768–4776. DOI: 10.1210/endo.141.12.7840 |
| [55] |
Kim HK, Morgan-Bagley S, Kostenuik P. RANKL inhibition: a novel strategy to decrease femoral head deformity after ischemic osteonecrosis. J Bone Miner Res. 2006;21(12):1946–1954. DOI: 10.1359/jbmr.060905 |
| [56] |
Kim H.K., Morgan-Bagley S., Kostenuik P. RANKL inhibition: a novel strategy to decrease femoral head deformity after ischemic osteonecrosis // J. Bone Miner. Res. 2006. Vol. 21. No. 12. P. 1946–1954. DOI: 10.1359/jbmr.060905 |
| [57] |
Shabaldin NA, Golovkin, SI, Shabaldin AV. Clinical and immunological features of transient synovitis of the hip joint and disease Legg-Calve-Perthes in children of early and school age. Mother and Baby in Kuzbass. 2016;64(1):21–26. (In Russ.) |
| [58] |
Шабалдин Н.А., Головкин С.И., Шабалдин А.В. Клинико-иммунологические особенности транзиторного синовита тазобедренного сустава и болезни Легга – Кальве – Пертеса у детей раннего и школьного возраста // Мать и дитя в Кузбассе. 2016. Т. 64. № 1. С. 21–26. |
| [59] |
Nelitz M, Lippacher S, Krauspe R, et al. Perthes disease: current principles of diagnosis and treatment. Dtsch Arztebl Int. 2009;106(31–32):517–523. DOI: 10.3238/arztebl.2009.0517 |
| [60] |
Nelitz M., Lippacher S., Krauspe R., et al. Perthes disease: current principles of diagnosis and treatment // Dtsch. Arztebl. Int. 2009. Vol. 106. No. 31–32. P. 517–523. DOI: 10.3238/arztebl.2009.0517 |
| [61] |
Divi SN, Bielski RJ. Legg-Calvé-Perthes disease. Pediatr Ann. 2016;45(4):144–149. DOI: 10.3928/00904481-20160310-03 |
| [62] |
Divi S.N., Bielski R.J. Legg-Calvé-Perthes disease // Pediatr. Ann. 2016. Vol. 45. No. 4. P. 144–149. DOI: 10.3928/00904481-20160310-03 |
| [63] |
Kim HK, Herring JA. Pathophysiology, classifications, and natural history of Perthes disease. Orthop Clin N Am. 2011;42(3):285–295. DOI: 10.1016/j.ocl.2011.04.007 |
| [64] |
Kim H.K., Herring J.A. Pathophysiology, classifications, and natural history of Perthes disease // Orthop. Clin. N. Am. 2011. Vol. 42. No. 3. P. 285–295. DOI: 10.1016/j.ocl.2011.04.007 |
| [65] |
Ibrahim T, Little DG. The Pathogenesis and treatment of Legg-Calvé-Perthes Disease. JBJS Rev. 2016;4(7). DOI: 10.2106/JBJS.RVW.15.00063 |
| [66] |
Ibrahim T., Little D.G. The pathogenesis and treatment of Legg-Calvé-Perthes disease // JBJS Rev. 2016. Vol. 4. No. 7. DOI: 10.2106/JBJS.RVW.15.00063 |
| [67] |
Lisitsyn A, Alexeeva E, Pinelis V, et al. Experience of treatment with ibandronic acid in patients with rheumatological diseases and systemic osteoporosis. Current Pediatrics. 2010;9(1):116–121. (In Russ.) |
| [68] |
Лисицин А., Алексеева Е., Пинелис В., и др. Опыт применения ибандроновой кислоты у больных с тяжелым течением ревматических болезней и системным остеопорозом // Вопросы современной педиатрии. 2010. Т. 9. № 1. С. 116–121. |
| [69] |
Fernández-Martín S, López-Peña M, Muñoz F, et al. Bisphosphonates as disease-modifying drugs in osteoarthritis preclinical studies: a systematic review from 2000 to 2020. Arthritis Res Ther. 2021;23(1):60. DOI: 10.1186/s13075-021-02446-6 |
| [70] |
Fernández-Martín S., López-Peña M., Muñoz F., et al. Bisphosphonates as disease-modifying drugs in osteoarthritis preclinical studies: a systematic review from 2000 to 2020 // Arthritis. Res. Ther. 2021. Vol. 23. No. 1. P. 60. DOI: 10.1186/s13075-021-02446-6 |
| [71] |
Khomenko AI, Lobko SS. Bisphosphonates in the treatment for osteoporosis Meditsinskie novosti. 2014;7:27–31. (In Russ.) |
| [72] |
Хоменко А.И., Лобко С.С. Бисфосфонаты в клинике лечения остеопороза // Медицинские новости. 2014. Т. 7. С. 27–31. |
| [73] |
Krylov MYu, Nikitinskaya OA, Samarkina EYu, et al. Farnesyl diphosphate synthase (FDRS) and geranylgeranyl diphosphate synthase (GGSP1) gene polymorphisms and efficiency of therapy with bisphosphonates in russian women with postmenopausal osteoporosis: a pilot study. Rheumatology Science and Practice. 2016;54(1):49–52. (In Russ.) DOI: 10.14412/1995-4484-2016-49-52 |
| [74] |
Крылов М.Ю., Никитинская О.А., Самаркина Е.Ю., и др. Генетические полиморфизмы фарнезил-дифосфат синтазы (FDPS) и геранилгеранил-дифосфат синтазы (GGSP1) и эффективность терапии бисфосфонатами у российских женщин с постменопаузальным остеопорозом: пилотное исследование // Научно-практическая ревматология. 2016. Т. 54. № 1. С. 49–52. DOI: 10.14412/1995-4484-2016-49-52 |
| [75] |
Yakushevskaya OV, Yureneva SV. Patogeneticheskie osnovy razvitiya ostroy fazy otveta na vnutrivennoe vvedenie azotsoderzhashchikh bisfosfonatov. Osteoporosis and Bone Diseases. 2014;17(1):30–32. (In Russ.) DOI: 10.14341/osteo2014130-32 |
| [76] |
Якушевская О.В., Юренева С.В. Патогенетические основы развития острой фазы ответа на внутривенное введение азотсодержащих бисфосфонатов // Остеопороз и остеопатии. 2014. Т. 17. № 1. С. 30–32. DOI: 10.14341/osteo2014130-32 |
| [77] |
D Orth SA, Vijayvargiya M. A paradigm shift in osteonecrosis treatment with bisphosphonates: a 20-year study. JB JS Open Access. 2021;6(4). DOI: 10.2106/JBJS.OA.21.00042 |
| [78] |
D Orth S.A., Vijayvargiya M. A paradigm shift in osteonecrosis treatment with bisphosphonates: a 20-year study // JB JS Open Access. 2021. Vol. 6. No. 4. DOI: 10.2106/JBJS.OA.21.00042 |
| [79] |
Hsu SL, Wang CJ, Lee MS et al. Cocktail therapy for femoral head necrosis of the hip. Arch Orthop Trauma Surg. 2010;130(1):23–29. DOI: 10.1007/s00402-009-0918-5 |
| [80] |
Hsu S.L., Wang C.J., Lee M.S., et al. Cocktail therapy for femoral head necrosis of the hip // Arch. Orthop. Trauma Surg. 2010. Vol. 130. No. 1. P. 23–29. DOI: 10.1007/s00402-009-0918-5 |
| [81] |
Nishii T, Sugano N, Miki H, et al. Does alendronate prevent collapse in osteonecrosis of the femoral head? Clin Orthop Relat Res. 2006;443:273–279. DOI: 10.1097/01.blo.0000194078.32776.31 |
| [82] |
Nishii T., Sugano N., Miki H., et al. Does alendronate prevent collapse in osteonecrosis of the femoral head? // Clin. Orthop. Relat. Res. 2006. Vol. 443. P. 273–279. DOI: 10.1097/01.blo.0000194078.32776.31 |
| [83] |
Li D, Yang Z, Wei Z, et al. Efficacy of bisphosphonates in the treatment of femoral head osteonecrosis: a PRISMA-compliant meta-analysis of animal studies and clinical trials. Sci Rep. 2018;8(1):1450. DOI: 10.1038/s41598-018-19884-z |
| [84] |
Li D., Yang Z., Wei Z., et al. Efficacy of bisphosphonates in the treatment of femoral head osteonecrosis: a PRISMA-compliant meta-analysis of animal studies and clinical trials // Sci. Rep. 2018. Vol. 8. No. 1. P. 1450. DOI: 10.1038/s41598-018-19884-z |
| [85] |
Fan M, Jiang WX, Wang AY, et al. Effect and mechanism of zoledronate on prevention of collapse in osteonecrosis of the femoral head. Zhongguo Yi Xue Ke Xue Yuan Xue Bao. 2012;34(4):330–336. DOI: 10.3881/j.issn.1000-503X.2012.04.004 |
| [86] |
Fan M., Jiang W.X., Wang A.Y., et al. Effect and mechanism of zoledronate on prevention of collapse in osteonecrosis of the femoral head // Zhongguo Yi Xue Ke Xue Yuan Xue Bao. 2012. Vol. 34. No. 4. P. 330–336. DOI: 10.3881/j.issn.1000-503X.2012.04.004 |
| [87] |
Aruwajoye OO, Aswath PB, Kim HKW. Material properties of bone in the femoral head treated with ibandronate and BMP-2 following ischemic osteonecrosis. J Orthop Res. 2017;35(7):1453–1460. DOI: 10.1002/jor.23402 |
| [88] |
Aruwajoye O.O., Aswath P.B., Kim H.K.W. Material properties of bone in the femoral head treated with ibandronate and BMP-2 following ischemic osteonecrosis. // J. Orthop. Res. 2017. Vol. 35. No. 7. P. 1453–1460. DOI: 10.1002/jor.23402 |
| [89] |
Little DG, Kim HK. Potential for bisphosphonate treatment in Legg-Calve-Perthes disease. J Pediatr Orthop. 2011;31(2):S182–S188. DOI: 10.1097/BPO.0b013e318223b541 |
| [90] |
Little D.G., Kim H.K. Potential for bisphosphonate treatment in Legg-Calve-Perthes disease // J. Pediatr. Orthop. 2011. Vol. 31. No. 2. P. S182–S188. DOI: 10.1097/BPO.0b013e318223b541 |
| [91] |
Bradley J. Rabquer, Giselle J. Tan, et al. Synovial inflammation in patients with osteonecrosis of the femoral head. Clin Transl Sci. 2009;2(4):273–278. DOI: 10.1111/j.1752-8062.2009.00133.x |
| [92] |
Rabquer B.J., Tan G.J., Shaheen P.J., et al. Synovial inflammation in patients with osteonecrosis of the femoral head // Clin. Transl. Sci. 2009. Vol. 2. No. 4. P. 273–278. DOI: 10.1111/j.1752-8062.2009.00133.x |
| [93] |
Barsukov DB, Kamosko MM. Pelvic osteotomy in the complex treatment of children with Legg-Calve-Perthes disease. Pediatric Traumatology, Orthopaedics and Reconstructive Surgery. 2014;2(2):29–37. (In Russ.) DOI: 10.17816/PTORS2229-37 |
| [94] |
Барсуков Д.Б., Камоско М.М. Остеотомии таза в комплексном лечении детей с болезнью Легга – Кальве – Пертеса // Ортопедия, травматология и восстановительная хирургия детского возраста. 2014. Т. 2. № 2. С. 29–37. DOI: 10.17816/PTORS2229-37 |
| [95] |
Tuktiyeva N, Dossanov B, Sakalouski A, et al. Methods of treatment of Legg-Calvé-Perthes disease (review). Georgian Med News. 2021;313:127–134. |
| [96] |
Tuktiyeva N., Dossanov B., Sakalouski A., et al. Methods of treatment of Legg-Calvé-Perthes disease (review) // Georgian Med. News. 2021. Vol. 313. P. 127–134. |
| [97] |
Jamil K, Zacharin M, Foster B, et al. Protocol for a randomised control trial of bisphosphonate (zoledronic acid) treatment in childhood femoral head avascular necrosis due to Perthes disease. BMJ Paediatr Open. 2017;1(1). DOI: 10.1136/bmjpo-2017-000084 |
| [98] |
Jamil K., Zacharin M., Foster B., et al. Protocol for a randomised control trial of bisphosphonate (zoledronic acid) treatment in childhood femoral head avascular necrosis due to Perthes disease // BMJ Paediatr. Open. 2017. Vol. 1. No. 1. DOI: 10.1136/bmjpo-2017-000084 |
| [99] |
Huang ZQ, Fu FY, Li WL, et al. Current treatment modalities for osteonecrosis of femoral head in mainland china: a cross-sectional study. Orthop Surg. 2020;12(6):1776–1783. DOI: 10.1111/os.12810 |
| [100] |
Huang Z.Q., Fu F.Y., Li W.L., et al. Current treatment modalities for osteonecrosis of femoral head in mainland china: a cross-sectional study // Orthop. Surg. 2020. Vol. 12. No. 6. P. 1776–1783. DOI: 10.1111/os.12810 |
| [101] |
Kraus R, Laxer RM. Characteristics, treatment options, and outcomes of chronic non-bacterial osteomyelitis in children. Curr Treat Options in Rheum. 2020;6:205–222. DOI: 10.1007/s40674-020-00149-8 |
| [102] |
Kraus R., Laxer R.M. Characteristics, treatment options, and outcomes of chronic non-bacterial osteomyelitis in children // Curr. Treat. Options in Rheum. 2020. Vol. 6. P. 205–222. DOI: 10.1007/s40674-020-00149-8 |
| [103] |
Hospach T, Langendoerfer M, von Kalle T, et al. Spinal involvement in chronic recurrent multifocal osteomyelitis (CRMO) in childhood and effect of pamidronate. Eur J Pediatr. 2010;169(9):1105–1111. DOI: 10.1007/s00431-010-1188-5 |
| [104] |
Hospach T., Langendoerfer M., von Kalle T., et al. Spinal involvement in chronic recurrent multifocal osteomyelitis (CRMO) in childhood and effect of pamidronate // Eur. J. Pediatr. 2010. Vol. 169. No. 9. P. 1105–1111. DOI: 10.1007/s00431-010-1188-5 |
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