Traumatology and Orthopedics of RussiaTraumatology and Orthopedics of RussiaТравматология и ортопедия России2311-29052542-0933Vreden National Medical Research Center of Traumatology and Orthopedics1756910.17816/2311-2905-17569ReviewsОбзорыReviewsReview ArticleOutcomes of oncologic arthroplasty in children and adolescents with malignant limb tumors: a systematic reviewИсходы онкоэндопротезирования у детей и подростков при злокачественных новообразованиях конечностей: систематический обзор литературыhttps://orcid.org/0000-0002-9712-55094651-8232ZorinVyacheslav I.ЗоринВячеслав Иванович
Russian Federation

Cand. Sci. (Med.)

канд. мед. наук

zoringlu@yandex.ruhttps://orcid.org/0000-0003-4235-5048VissarionovSergei V.ВиссарионовСергей Валентинович
Russian Federation

Dr. Sci. (Med.), Professor

д-р мед. наук, профессор, член-корр. РАН

vissarionovs@gmail.comhttps://orcid.org/0000-0002-1546-8517MakarovAlexandr Y.МакаровАлександр Юрьевич
Russian Federation
makarov.alexandr97@mail.ruhttps://orcid.org/0000-0002-4180-5353RybinskikhTimofey S.РыбинскихТимофей Сергеевич
Russian Federation
timofey1999r@gmail.comhttps://orcid.org/0000-0001-6187-2097RodionovaKristina N.РодионоваКристина Николаевна
Russian Federation
rkn0306@mail.ruH. Turner National Medical Research Center for Сhildren’s Orthopedics and Trauma SurgeryФГБУ «Национальный медицинский исследовательский центр детской травматологии и ортопедии им. Г.И. Турнера» Минздрава РоссииMechnikov North-Western State Medical UniversityФГБОУ ВО «Северо-Западный государственный медицинский университет им. И.И. Мечникова» Минздрава РоссииH. Turner National Medical Research Center for Сhildren’s Orthopedics and Trauma SurgeryФГБУ «Национальный медицинский исследовательский центр детской травматологии и ортопедии им. Г.И. Турнера» Минздрава России15112024181220243041571672106202408082024Copyright ©; 2024, Eco-VectorCopyright ©; 2024, Эко-ВекторCopyright ©; 2024,2024Eco-VectorЭко-Векторhttps://creativecommons.org/licenses/by-nc-nd/4.0https://journal.rniito.org/jour/article/view/17569

Background. Amputation was historically the primary surgical intervention for children with limb bone sarcomas. However, the development and refinement of chemotherapy and radiotherapy protocols, along with advances in surgical techniques and implants, have significantly altered the treatment landscape for these patients. Currently, limb-sparing oncologic arthroplasty is the preferred surgical approach for treating limb sarcomas in children.

The aim of the systematic review is to analyse the outcomes of oncologic arthroplasty in children and adolescents.

Methods. A comprehensive literature search was performed in Google Scholar, PubMed, ScienceDirect, and eLIBRARY databases focusing on the keywords “endoprostheses, tumors, children”, from 2000 to 2024. Data collection included patient demographics (number of patients, gender, age), follow-up period, disease diagnosis, tumor location, type of endoprosthesis, complications, functional outcomes based on the Musculoskeletal Tumor Society score (MSTS) in percentage, overall survival rates, and prosthesis survival rates.

Results. The review included the data from 30 articles on a total of 792 patients aged 2 to 18 years, with 422 males and 370 females. The average age was 11.4 years, and the average follow-up period was 6.5 years. Osteosarcoma was the most common diagnosis, accounting for 716 (88.8%) cases, followed by Ewing sarcoma with 67 (8.3%) cases. Distal femoral arthroplasties were performed most frequently (573 cases, 71.1%), followed by proximal tibial arthroplasty (148 cases, 18.3%). The most commonly used type of endoprosthesis was the non-invasively extendable type (540 cases, 67%). A total of 756 complications were recorded, resulting in a complication rate of 96%. The complications were predominantly oncologic (188 cases, 25%) and pediatric orthopedic (166 cases, 22%). The 5-year and 10-year overall survival rates were 81.68% and 77.63%, respectively, with an average prosthesis survival rate of 53.93%.

Conclusion. The data obtained indicate an extremely high frequency of complications during oncologic arthroplasty in children, mainly of an orthopedic profile, which requires analysis and development of measures to prevent them, as well as organizational solutions for the correction of these disorders.

Актуальность. При саркомах костей конечностей у детей операцией выбора до 1980-х гг. являлась ампутация. Создание и совершенствование протоколов химиотерапии, лучевой терапии, развитие хирургической техники и имплантатов кардинально изменили возможности и результаты оказания помощи данной группе пациентов. В настоящее время органосохраняющая технология онкологического эндопротезирования является методом выбора в хирургическом лечении детей с саркомами конечностей.

Целью систематического обзора является анализ исходов онкологического эндопротезирования у детей и подростков.

Материал и методы. Поиск источников выполнялся в базах данных Google Scholar, PubMed, ScienceDirect, eLIBRARY по ключевым словам «endoprostheses, tumors, children, эндопротезы, злокачественные опухоли, дети» с глубиной поиска с 2000 по 2024 г. Выполнялся анализ следующих данных: количество пациентов, пол, возраст, период наблюдения, диагноз, локализация опухоли, тип устанавливаемого эндопротеза, наличие осложнений, результаты оценки функции конечности по шкале Musculoskeletal Tumor Society (MSTS) в процентах, общая выживаемость и выживаемость эндопротеза.

Результаты. в анализируемый материал вошли данные из 30 статей, включающих всего 792 пациента в возрасте от 2 до 18 лет, из них 422 мальчика и 370 девочек. Средний возраст — 11,4 года, средний период наблюдения — 6,5 лет. На первом месте по встречаемости расположилась остеосаркома — 716 (88,8%) наблюдений, на втором — саркома Юинга — 67 (8,3%). Чаще всего выполнялось эндопротезирование дистального отдела бедренной кости — 573 (71,1%), а также проксимального отдела большеберцовой кости — 148 (18,3%). Наиболее часто используемый тип эндопротеза — неинвазивно удлиняемый — 540 (67%). Было зафиксировано 756 осложнений, частота встречаемости — 96%. В структуре осложнений преобладали онкологические и ортопедические осложнения на фоне роста ребенка — 188 (25%) и 166 (22%) соответственно. Общая выживаемость пациентов за 5 и 10 лет составила в среднем 81,68% и 77,63% соответственно при среднем значении выживаемости эндопротеза 53,93% за десятилетний период.

Заключение. Полученные данные свидетельствуют о крайне высокой частоте осложнений при онкопротезировании у детей, преимущественно ортопедических, что требует анализа и разработки мер по их предупреждению, а также организационных решений для коррекции данных нарушений.

arthroplastyoncologic arthroplastymalignant tumorschildrenperiprosthetic fracturesperiprosthetic infectionэндопротезированиеонкопротезированиезлокачественные опухолидетиперипротезные переломыперипротезная инфекцияБольшаков Н.А., Артемов А.Ю., Ворочай А.М., Хамин И.Г., Тихонова М.В., Слинин А.С. и др. Эндопротезирование коленного сустава как хирургический этап лечения пациентов детского и подросткового возраста с опухолями костей. Вопросы гематологии/онкологии и иммунопатологии в педиатрии. 2019;18(1):55-61. doi: 10.24287/1726-1708-2019-18-1-55-61. Bolshakov N.A., Artemov A.Yu., Vorochai A.M., Khamin I.G., Tikhonova M.V., Slinin А.S. et al. Endoprosthesis reconstruction, as a surgical treatment of children and adolescence with bone tumors around the knee. Pediatric Hematology/Oncology and Immunopathology. 2019;18(1):55-61. (In Russian). doi: 10.24287/1726-1708-2019-18-1-55-61.Hagleitner M.M., de Bont E.S., Te Loo D.M. Survival trends and long-term toxicity in pediatric patients with osteosarcoma. Sarcoma. 2012;2012:636405. doi: 10.1155/2012/636405.Dotan A., Dadia S., Bickels J., Nirkin A., Flusser G., Issakov J. et al. Expandable endoprosthesis for limb-sparing surgery in children: long-term results. J Child Orthop. 2010;4(5):391-400. doi: 10.1007/s11832-010-0270-x.Groundland J.S., Ambler S.B., Houskamp L.D.J., Orriola J.J., Binitie O.T., Letson G.D. Surgical and Functional Outcomes After Limb-Preservation Surgery for Tumor in Pediatric Patients: A Systematic Review. JBJS Rev. 2016;4(2):e2. doi: 10.2106/JBJS.RVW.O.00013.Henderson E.R., O’Connor M.I., Ruggieri P., Windhager R., Funovics P.T., Gibbons C.L. et al. Classification of failure of limb salvage after reconstructive surgery for bone tumours : a modified system Including biological and expandable reconstructions. Bone Joint J. 2014;96-B(11):1436-1440. doi: 10.1302/0301-620X.96B11.34747.Penna V., Toller E.A., Pinheiro C., Becker R.G. A new approach to partialknee endoprosthesis in primary bone sarcomas. Rev Bras Ortop. 2015;44(1):46-51. doi: 10.1016/S2255-4971(15)30048-3.Badr I., Eid T.A., Salem D., Shaheen Ahmed el Dadawy, Habeeb Mohammed el Sawy, Donati Davide Marie et al. Functional outcome and Limb length discrepancy after endoprosthetic reconstruction in skeletally immature patients with bone tumor. Egyptian Orthop J. 2019;54(Suppl 1):25-30.Савлаев К.Ф., Петриченко А.В., Иванова Н.М., Шароев Т.А. Осложнения эндопротезирования при опухолях костей у детей. Quantum Satis. 2021;4(1-4):19-22. Savlaev K.F., Petrichenko A.V., Ivanova N.M., Sharoev T.A. Complications of endoproshetics for bone tumors in children. Quantum Satis. 2021;4(1-4):19-22. (In Russian).Henderson E.R., Pepper A.M., Letson G.D. What are estimated reimbursements for lower extremity prostheses capable of surgical and nonsurgical lengthening? Clin Orthop Relat Res. 2012;470(4):1194-1203. doi: 10.1007/s11999-011-2186-2.Zan P., Shen J., Liu K., Wang H., Cai Z., Ma X. et al. Custom-made semi-joint prosthesis replacement combined ligament advanced reinforcement system (LARS) ligament reconstruction for the limb salvage surgery of malignant tumors in the distal femur in skeletal immature children. Front Pediatr. 2023;11:1168637. doi: 10.3389/fped.2023.1168637.Benevenia J., Patterson F., Beebe K., Tucker K., Moore J., Ippolito J. et al. Results of 20 consecutive patients treated with the Repiphysis expandable prosthesis for primary malignant bone. Springerplus. 2015;4:793. doi: 10.1186/s40064-015-1582-6.Haidar R., Sagghieh S., Muwakitt S., Mumtaz G., Akel S., Kamzoul R. et al. Limb salvage surgery for children and adolescents with malignant bone tumors in a developing country. Pediatr Blood Cancer. 2008; 51(6):787-791. doi: 10.1002/pbc.21696.Futani H., Minamizaki T., Nishimoto Y., Abe S., Yabe H., Ueda T. Long-term follow-up after limb salvage in skeletally immature children with a primary malignant tumor of the distal end of the femur. J Bone Joint Surg Am. 2006;88(3):595-603. doi: 10.2106/JBJS.C.01686.Gundavda M.K., Agarwal M.G. Growing Without Pain: The Noninvasive Expandable Prosthesis is Boon for Children with Bone Cancer, as well as Their Surgeons! Indian J Orthop. 2019;53(1):174-182. doi: 10.4103/ortho.IJOrtho_53_17.Raciborska A., Malesza I., Bilska K., Koziński T., Pachuta B. Double Endoprosthesis in the Management of Refractory Metastatic Primary Bone Tumors in Children and Young Adults. Adv Orthop. 2021;2021:9944702. doi: 10.1155/2021/9944702.Shehadeh A., Al-Qawasmi M., Al Btoush O., Obeid Z. Tibia Multiplanar Deformities and Growth Disturbance Following Expandable Endoprosthetic Distal Femur Replacement. J Clin Med. 2022;11(22):6734. doi: 10.3390/jcm11226734.Staals E.L., Colangeli M., Ali N., Casanova J.M., Donati D.M., Manfrini M. Are Complications Associated With the Repiphysis(®) Expandable Distal Femoral Prosthesis Acceptable for Its Continued Use? Clin Orthop Relat Res. 2015;473(9):3003-3013. doi: 10.1007/s11999-015-4355-1.Masrouha K., Abboud M., Saab R., Muwakkit S.A., Khoury N., Haidar R. et al. Long-term follow-up of children treated with the Repiphysis expandable prosthesis for lower extremity bone sarcoma. J Pediatr Orthop B. 2022;31(2):e258-e263. doi: 10.1097/BPB.0000000000000891.Torner F., Segur J.M., Ullot R., Soldado F., Domenech P., DeSena L. et al. Non-invasive expandable prosthesis in musculoskeletal oncology paediatric patients for the distal and proximal femur. First results. Int Orthop. 2016;40(8):1683-1688. doi: 10.1007/s00264-016-3163-x.Raciborska A., Bilska K., Malesza I., Rodriguez-Galindo C., Pachuta B. Distal Tibial Reconstruction in the Management of Primary Bone Tumors in Children and Adolescents. Foot Ankle Int. 2021;42(11): 1447-1453. doi: 10.1177/10711007211012690.Sewell M.D., Spiegelberg B.G., Hanna S.A., Aston W.J., Bartlett W., Blunn G.W. et al. Total femoral endoprosthetic replacement following excision of bone tumours. J Bone Joint Surg Br. 2009;91(11):1513-1520. doi: 10.1302/0301-620X.91B11.21996.Ahlmann E.R., Menendez L.R., Kermani C., Gotha H. Survivorship and clinical outcome of modular endoprosthetic reconstruction for neoplastic disease of the lower limb. J Bone Joint Surg Br. 2006;88(6): 790-795. doi: 10.1302/0301-620X.88B6.17519.Cipriano C.A., Gruzinova I.S., Frank R.M., Gitelis S., Virkus W.W. Frequent complications and severe bone loss associated with the repiphysis expandable distal femoral prosthesis. Clin Orthop Relat Res. 2015;473(3): 831-838. doi: 10.1007/s11999-014-3564-3.Sambri A., Staals E., Medellin M.R., Abudu A., Gikas P., Pollock R. et al. Stanmore noninvasive extendible endoprosthesis in the treatment of bone sarcoma in the preadolescent. J Surg Oncol. 2019;120(2):176-182. doi: 10.1002/jso.25501.Gong T., Lu M., Min L., Luo Y., Tu C. Reconstruction of a 3D-printed endoprosthesis after joint-preserving surgery with intraoperative physeal distraction for childhood malignancies of the distal femur. J Orthop Surg Res. 2023;18(1):534. doi: 10.1186/s13018-023-04037-4.Gilg M.M., Gaston C.L., Jeys L., Abudu A., Tillman R.M., Stevenson J.D. et al. The use of a non-invasive extendable prosthesis at the time of revision arthroplasty. Bone Joint J. 2018;100-B(3):370-377. doi: 10.1302/0301-620X.100B3.BJJ-2017-0651.R1.Tsuda Y., Fujiwara T., Sree D., Stevenson J.D., Evans S., Abudu A. Physeal-preserving endoprosthetic replacement with short segment fixation in children with bone sarcomas. Bone Joint J. 2019;101-B(9):1144-1150. doi: 10.1302/0301-620X.101B9.BJJ-2018-1333.R1.Saghieh S., Abboud M.R., Muwakkit S.A., Saab R., Rao B., Haidar R. Seven-year experience of using Repiphysis expandable prosthesis in children with bone tumors. Pediatr Blood Cancer. 2010;55(3):457-463. doi: 10.1002/pbc.22598.Zou C., Zhao Z., Lin T., Huang Y., Xie X., Yin J. et al. Long-term outcomes of limb salvage treatment with custom-made extendible endoprosthesis for bone sarcoma around the knee in children. J Orthop Surg Res. 2020;15(1):14. doi: 10.1186/s13018-019-1534-x.Gilg M.M., Gaston C.L., Parry M.C., Jeys L., Abudu A., Tillman R.M. et al. What is the morbidity of a non-invasive growing prosthesis? Bone Joint J. 2016;98-B(12): 1697-1703. doi: 10.1302/0301-620X.98B12.BJJ-2016-0467.Ajit Singh V., Earnest Kunasingh D., Haseeb A., Yasin N.F. Outcome of expandable endoprosthesis: A single centre retrospective review. J Orthop Surg (Hong Kong). 2019;27(2):2309499019850313. doi: 10.1177/2309499019850313.Huang J., Cheng J., Bi W., Xu M., Jia J., Han G. et al. Neoadjuvant Chemotherapy and Expandable Prosthesis Reconstruction to Treat Osteosarcoma around the Knee in Children. Orthop Surg. 2023;15(1):162-168. doi: 10.1111/os.13563.Ji T., Yang Y., Li D.S., Tang X.D., Guo W. Limb Salvage Using Non-hinged Endoprosthesis and Staged Correction of Leg-length Discrepancy for Children with Distal Femoral Malignant Tumors. Orthop Surg. 2019;11(5):819-825. doi: 10.1111/os.12525.El Ghoneimy A.M., Shehab A.M., Farid N. What is the Cumulative Incidence of Revision Surgery and What Are the Complications Associated With Stemmed Cementless Nonextendable Endoprostheses in Patients 18 Years or Younger With Primary Bone Sarcomas About the Knee. Clin Orthop Relat Res. 2022;480(7):1329-1338. doi: 10.1097/CORR.0000000000002150.Eaton B.R., Schwarz R., Vatner R., Yeh B., Claude L., Indelicato D.J. et al. Osteosarcoma. Pediatr Blood Cancer. 2021;68 Suppl 2:e28352. doi: 10.1002/pbc.28352.Jafari F., Javdansirat S., Sanaie S., Naseri A., Shamekh A., Rostamzadeh D. et al. Osteosarcoma: A comprehensive review of management and treatment strategies. Ann Diagn Pathol. 2020;49:151654. doi: 10.1016/j.anndiagpath.2020.151654.Panez-Toro I., Muñoz-García J., Vargas-Franco J.W., Renodon-Cornière A., Heymann M.F., Lézot F. et al. Advances in Osteosarcoma. Curr Osteoporos Rep. 2023;21(4):330-343. doi: 10.1007/s11914-023-00803-9.Петриченко А.В., Букреева Е.А., Романов П.А., Тиганова О.А., Иванова Н.М., Очкуренко А.А. и др. Анализ ортопедических последствий многокомпонентного лечения костных сарком у детей. Ортопедия, травматология и восстановительная хирургия детского возраста. 2019;7(1):57-70. doi: 10.17816/PTORS7157-70. Petrichenko A.V., Bukreeva E.A., Romanov P.A., Tiganova O.A., Ivanova N.M., Ochkurenko A.A. et al. Musculoskeletal sequelae of childhood bone sarcoma survivors. Pediatric Traumatology, Orthopaedics and Reconstructive Surgery. 2019;7(1):57-70. (In Russian). doi: 10.17816/PTORS7157-70.Vitale M.G., Levy D.E., Johnson M.G., Gelijns A.C., Moskowitz A.J., Roye B.P. et al. Assessment of quality of life in adolescent patients with orthopaedic problems: are adult measures appropriate? J Pediatr Orthop. 2001;21(5):622-628.Bergin P.F., Noveau J.B., Jelinek J.S., Henshaw R.M. Aseptic loosening rates in distal femoral endoprostheses: does stem size matter? Clin Orthop Relat Res. 2012;470(3):743-750. doi: 10.1007/s11999-011-2081-x.Zhang H.R., Zhang J.Y., Yang X.G., Qiao R.Q., Li J.K., Ren Z.P. et al. The effects of length of femoral stem on aseptic loosening following cemented distal femoral endoprosthetic replacement in tumour surgery. Int Orthop. 2020;44(7):1427-1433. doi: 10.1007/s00264-020-04629-3.Aponte-Tinao L., Ayerza M.A., Muscolo D.L., Farfalli G.L. Survival, recurrence, and function after epiphyseal preservation and allograft reconstruction in osteosarcoma of the knee. Clin Orthop Relat Res. 2015;473(5):1789-1796. doi: 10.1007/s11999-014-4028-5.Scanferla R., Scolari F., Muratori F., Tamburini A., Delcroix L., Scoccianti G. et al. Joint-Sparing Resection around the Knee for Osteosarcoma: Long-Term Outcomes of Biologic Reconstruction with Vascularized Fibula Graft Combined with Massive Allograft. Cancers (Basel). 2024;16(9):1672. doi: 10.3390/cancers16091672.Takeuchi A., Yamamoto N., Hayashi K., Matsubara H., Miwa S., Igarashi K. et al. Joint-preservation surgery for pediatric osteosarcoma of the knee joint. Cancer Metastasis Rev. 2019;38(4):709-722. doi: 10.1007/s10555-019-09835-z.Liu W., He H.B., Zhang C., Liu Y.P., Wan J. Distraction-suppression effect on osteosarcoma. Med Hypotheses. 2018;121:4-5. doi: 10.1016/j.mehy.2018.09.004.