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Joint-preservation surgery for pediatric osteosarcoma of the knee joint

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Abstract

The multi-disciplinary approach involving imaging, multi-agent chemotherapy, meticulous surgical procedures, and careful postoperative care has facilitated an increase in the use of limb-sparing surgery for pediatric osteosarcoma. Osteosarcoma usually occurs around the metaphysis of the distal femur or proximal tibia and needs wide excision with the adjacent joint and replacement by a megaprosthesis. The recent advancement in imaging modalities and surgical techniques supports joint-preservation surgery (JPS), involving the preservation of the adjacent epiphysis, for select patients following careful assessment of the tumor margins and precise tumor excision. An advantage of this surgery is that it maintains the adjacent joint and preserves the growth of the residual epiphysis, which provides excellent limb function. Various reconstruction options are available, including allograft, tumor-devitalized autograft, vascularized fibula graft, distraction osteogenesis, and custom-made implants. However, several complications are inevitable with these options, such as loosening, non-union at the host-graft junction, infection, fracture, implant loosening, breakage, deformity, limb-length discrepancy related to the reconstruction methods, or patient growth in pediatric osteosarcoma. Surgeons should fully understand the advantages and disadvantages of this procedure. In this review, we discuss the concept of JPS, types of reconstruction methods, and current treatment outcomes. It is our opinion that the further analysis by multi-institutional setting is necessary to clarify long-term outcomes and establish global guidelines on the indications and surgical procedure for JPS.

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References

  1. Ayerza, M. A., Farfalli, G. L., Aponte-Tinao, L., & Muscolo, D. L. (2010). Does increased rate of limb-sparing surgery affect survival in osteosarcoma? Clinical Orthopaedics and Related Research, 468(11), 2854–2859. https://doi.org/10.1007/s11999-010-1423-4.

    Article  Google Scholar 

  2. Li, X., Zhang, Y., Wan, S., Li, H., Li, D., Xia, J., Yuan, Z., Ren, M., Yu, S., Li, S., Yang, Y., Han, L., & Yang, Z. (2016). A comparative study between limbsalvage and amputation for treating osteosarcoma.Journal of Bone Oncology, 5(1), 15–21. https://doi.org/10.1016/j.jbo.2016.01.001.

    Article  Google Scholar 

  3. Yao, W., Cai, Q., Wang, J., & Gao, S. (2017). Treatment of osteosarcoma around the knee in skeletally immature patients. Oncology Letters, 14(5), 5241–5248. https://doi.org/10.3892/ol.2017.6903.

  4. Henderson, E. R., O’connor, M. I., Ruggieri, P., Windhager, R., Funovics, P. T., Gibbons, C. L., Guo, W., Hornicek, F. J., Temple, H. T., & Letson, G. D. (2014). Classification of failure of limb salvage after reconstructive surgery for bone tumours: a modified system including biological and expandable reconstructions. Bone Joint J, 96 (11), 1436-1440.https://doi.org/10.1302/0301-620X.96B11.

  5. Capanna, R., Scoccianti, G., Frenos, F., Vilardi, A., Beltrami, G., & Campanacci, D. A. (2015). What was the survival of megaprostheses in lower limb reconstructions after tumor resections? Clinical Orthopaedics and Related Research, 473(3), 820–830. https://doi.org/10.1007/s11999-014-3736-1.

    Article  PubMed  Google Scholar 

  6. Ogilvie, C. M., Crawford, E. A., Hosalkar, H. S., King, J. J., & Lackman, R. D. (2009). Long-term results for limb salvage with osteoarticular allograft reconstruction. Clinical Orthopaedics and Related Research, 467(10), 2685–2690. https://doi.org/10.1007/s11999-009-0726-9.

    Article  Google Scholar 

  7. Ruggieri, P., Mavrogenis, A. F., Pala, E., Romantini, M., Manfrini, M., & Mercuri, M. (2013). Outcome of expandable prostheses in children. Journal of Pediatric Orthopaedics, 33(3), 244–253. https://doi.org/10.1097/BPO.0b013e318286c178.

    Article  PubMed  Google Scholar 

  8. Cipriano, C. A., Gruzinova, I. S., Frank, R. M., Gitelis, S., & Virkus, W. W. (2015). Frequent complications and severe bone loss associated with the repiphysis expandable distal femoral prosthesis. Clinical Orthopaedics and Related Research, 473(3), 831–838. https://doi.org/10.1007/s11999-014-3564-3.

    Article  Google Scholar 

  9. Dotan, A., Dadia, S., Bickels, J., Nirkin, A., Flusser, G., Issakov, J., Neumann, Y., Cohen, I., Ben-Arush, M., Kollender, Y., & Meller, I. (2010). Expandable endoprosthesis for limb-sparing surgery in children: long-term results. Journal of Children’s Orthopaedics, 4(5), 391–400. https://doi.org/10.1007/s11832-010-0270-x.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Staals, E. L., Colangeli, M., Ali, N., Casanova, J. M., Donati, D. M., & Manfrini, M. (2015). Are complications associated with the Repiphysis® expandable distal femoral prosthesis acceptable for its continued use? Clinical Orthopaedics and Related Research, 473(9), 3003–3013. https://doi.org/10.1007/s11999-015-4355-1.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Hoffer, F. A., Nikanorov, A. Y., Reddick, W. E., Bodner, S. M., Xiong, X., Jones-Wallace, D., Gronemeyer, S. A., Rao, B. N., Kauffman, W. M., & Laor, T. (2000). Accuracy of MR imaging for detecting epiphyseal extension of osteosarcoma. Pediatric Radiology, 30(5), 289–298. https://doi.org/10.1007/s002470050743.

    Article  CAS  Google Scholar 

  12. Wong, K. C., & Kumta, S. M. (2013). Joint-preserving tumor resection and reconstruction using image-guided computer navigation tumor. Clinical Orthopaedics and Related Research, 471(3), 762–773. https://doi.org/10.1007/s11999-012-2536-8.

    Article  Google Scholar 

  13. Mei, J., Ni, M., Jia, G. Y., Chen, Y.X., & Zhu, X. Z. (2015). Intermittent internal fixation with a locking plate to preserve epiphyseal growth function during limb-salvage surgery in a child with osteosarcoma of the distal femur: a case report. Medicine (Baltimore), 94(20), e830 https://doi.org/10.1097/MD.0000000000000830.

    Article  Google Scholar 

  14. Aponte-tinao, L., Ayerza, M. A., & Muscolo, D. L. (2015). Survival, recurrence, and function after epiphyseal preservation and allograft reconstruction in osteosarcoma of the knee. Clinical Orthopaedics and Related Research, 473(5), 1789–1796. https://doi.org/10.1007/s11999-014-4028-5.

    Article  Google Scholar 

  15. Tsuchiya, H., Wan, S. L., Sakayama, K., Yamamoto, N., Nishida, H., & Tomita, K. (2005). Reconstruction using an autograft containing tumour treated by liquid nitrogen. The Journal of Bone and Joint Surgery, 87-B(2), 218–225. https://doi.org/10.1302/0301-620x.87b2.15325.

    Article  Google Scholar 

  16. Kiss, S., Terebessy, T., Szöke, G., Kiss, J., Antal, I., & Szendröi, M. (2013). Epiphysis preserving resection of malignant proximal tibial tumours. International Orthopaedics, 37(1), 99–104. https://doi.org/10.1007/s00264-012-1731-2.

    Article  Google Scholar 

  17. Tsuchiya, H., Abdel-Wanis, M. E., Sakurakichi, K., Yamashiro, T., & Tomita, K. (2002). Osteosarcoma around the knee. Intraepiphyseal excision and biological reconstruction with distraction osteogenesis. The Journal of bone and joint surgery. 84-(B)8, 1162–1166. https://doi.org/10.1302/0301-620x.84b8.13330.

  18. Manabe, J., Ahmed, A. R., Kawaguchi, N., Matsumoto, S., & Kuroda, H. (2004). Pasteurized autologous bone graft in surgery for bone and soft tissue sarcoma. Clinical Orthopaedics and Related Research, 419(2), 258–266. https://doi.org/10.1097/00003086-200402000-00042.

    Article  Google Scholar 

  19. Uyttendaele, D., De Schryver, A., Claessens, H., Roels, H., Berkvens, P., & Mondelaers, W. (1988). Limb conservation in primary bone tumours by resection, extracorporeal irradiation and re-implantation. The Journal of Bone and Joint Surgery, 70-(B)3, 348–353.

  20. Wong, K. C., Kumta, S. M., Antonio, G. E., & Tse, L. F. (2008). Image fusion for computer-assisted bone tumor surgery. Clinical Orthopaedics and Related Research, 466(10), 2533–2541. https://doi.org/10.1007/s11999-008-0374-5.

    Article  Google Scholar 

  21. Miwa, S., Takeuchi, A., Shirai, T., Taki, J., Yamamoto, N., Nishida, H., Hayashi, K., Tanzawa, Y., Kimura, H., Igarashi, K., Ooi, A., & Tsuchiya, H. (2013). Prognostic value of radiological response to chemotherapy in patients with osteosarcoma. PLoS One, 8(7). https://doi.org/10.1371/journal.pone.0070015.

    Article  CAS  Google Scholar 

  22. Enneking, W. F., Spanier, S. S., & Goodman, M. A. (1980). A system for the surgical staging of musculoskeletal sarcoma. Clinical Orthopaedics and Related Research, 153(11), 106–20.

  23. Takeuchi, A., Yamamoto, N., Hayashi, K., Matsubara, H., Kimura, H., Miwa, S., Higuchi, T., Abe, K., Taniguchi, Y., & Tsuchiya, H. (2018). Growth of epiphysis after epiphyseal-preservation surgery for childhood osteosarcoma around the knee joint. BMC Musculoskeletal Disorders, 19(1), 185. https://doi.org/10.1186/s12891-018-2109-4.

  24. Enneking, W. F., Dunham, W., Gebhardt, M. C., Malawar, M., & Pritchard, D. J. (1993). A system for the functional evaluation of reconstructive procedures after surgical treatment of tumors of the musculoskeletal system. Clinical Orthopaedics and Related Research, 286(1), 241–246.

  25. Bellanova, L., Paul, L., & Docquier, P. L. (2013). Surgical guides (patient-specific instruments) for pediatric tibial bone sarcoma resection and allograft reconstruction. Sarcoma, 2013, 787653. https://doi.org/10.1155/2013/787653.

    Article  Google Scholar 

  26. Andreou, D., Bielack, S. S., Carrle, D., Kevric, M., Kotz, R., Winkelmann, W., Jundt, G., Werner, M., Fehlberg, S., Kager, L., Kühne, T., Lang, S., Dominkus, M., Exner, G. U., Hardes, J., Hillmann, A., Ewerbeck, V., Heise, U., Reichardt, P., & Tunn, P. U. (2011). The influence of tumor- and treatment-related factors on the development of local recurrence in osteosarcoma after adequate surgery. An analysis of 1355 patients treated on neoadjuvant Cooperative Osteosarcoma Study Group protocols. Ann Oncol, 22(5), 1228–1235. https://doi.org/10.1093/annonc/mdq589.

    Article  CAS  Google Scholar 

  27. Fox, E. J., Hau, M. A., Gebhardt, M. C., Hornicek, F. J., Tomford, W. W., & Mankin, H. J. (2002). Long-term followup of proximal femoral allografts. Clinical orthopaedics and related research, 397(4), 106–113.

  28. Choong, P. F. M. (1997). The role of allografts in tumour surgery.Acta Orthopaedica Scandinavica, Supplement. 273, 89-94.https://doi.org/10.1080/17453674.1997.11744709.

    Article  Google Scholar 

  29. Ortiz-Cruz, E., Gebhardt, M. C., Jennings, L. C., Springfield, D. S., & Mankin, H. J. (1997). The results of transplantation of intercalary allografts after resection of tumors. A long-term follow-up study. The Journal of Bone and Joint Surgery, 79-A(1), 97–106. https://doi.org/10.2106/00004623-199701000-00010.

    Article  CAS  Google Scholar 

  30. Bus, M. P. A., Dijkstra, P. D. S., Van De Sande, M. A. J., Taminiau, A. H. M., Schreuder, H. W. B., Jutte, P. C., van der Geest, I. C., Schaap, G. R., & Bramer, J. A. (2014). Intercalary allograft reconstructions following resection of primary bone tumors: a nationwide multicenter study. The Journal of Bone and Joint Surgery, 96-A(4), 1–11. https://doi.org/10.2106/JBJS.M.00655.

    Article  CAS  Google Scholar 

  31. Muscolo, D. L., Ayerza, M. A., Aponte-Tinao, L. A., & Ranalletta, M. (2005). Partial epiphyseal preservation and intercalary allograft reconstruction in high-grade metaphyseal osteosarcoma of the knee. The Journal of Bone and Joint Surgery, 87-A(Suppl 1), 226-236. https://doi.org/10.2106/JBJS.E.00253.

    Article  Google Scholar 

  32. Houdek, M. T., Wagner, E. R., Stans, A. A., Shin, A. Y., Bishop, A. T., Sim, F. H., & Moran, S. L. (2016). What is the outcome of allograft and intramedullary free fibula (Capanna technique) in pediatric and adolescent patients with bone tumors? Clinical Orthopaedics and Related Research, 474(3), 660–668. https://doi.org/10.1007/s11999-015-4204-2.

    Article  Google Scholar 

  33. Puri, A., Byregowda, S., Gulia, A., Patil, V., Crasto, S., & Laskar, S. (2018). Reconstructing diaphyseal tumors using radiated (50 Gy) autogenous tumor bone graft. Journal of Surgical Oncology, 118(1), 138–143. https://doi.org/10.1002/jso.25092.

    Article  PubMed  Google Scholar 

  34. Hong, A. M., Millington, S., Ahern, S., McCowage, G., Boyle, R., Tattersall, M., et al. (2013). Limb preservation surgery with extracorporeal irradiation in the management of malignant bone tumor: the oncological outcomes of 101 patients. Annals of Oncology, 24(10), 2676–2680. https://doi.org/10.1093/annonc/mdt252.

    Article  CAS  PubMed  Google Scholar 

  35. Sharma, D. N., Rastogi, S., Bakhshi, S., Rath, G. K., Julka, P. K., Laviraj, M. A., Khan, S. A., & Kumar, A. (2013). Role of extracorporeal irradiation in malignant bone tumors. Indian Journal of Cancer, 50(4), 306–309. https://doi.org/10.4103/0019-509X.123601.

    Article  CAS  PubMed  Google Scholar 

  36. Wu, P. K., Chen, C. F., Chen, C. M., Cheng, Y. C., Tsai, S. W., Chen, T. H., & Chen, W. M. (2018). Intraoperative extracorporeal irradiation and frozen treatment on tumor-bearing autografts show equivalent outcomes for biologic reconstruction. Clinical Orthopaedics and Related Research, 476(4), 877–889. https://doi.org/10.1007/s11999.0000000000000022.

    Article  Google Scholar 

  37. Jeon, D. G., Kim, M. S., Cho, W. H., Song, W. S., & Lee, S. Y. (2007). Pasteurized autograft for intercalary reconstruction: an alternative to allograft. Clinical Orthopaedics and Related Research, 456(5), 203–210. https://doi.org/10.1097/BLO.0b013e31802e7ec8.

    Article  Google Scholar 

  38. Qu, H., Guo, W., Yang, R., Li, D., Tang, S., Yang, Y., Dong, S., & Zang, J. (2015). Reconstruction of segmental bone defect of long bones after tumor resection by devitalized tumor-bearing bone. World Journal of Surgical Oncology, 13, 282. https://doi.org/10.1186/s12957-015-0694-3.

  39. Ikuta, K., Nishida, Y., Sugiura, H., Tsukushi, S., Yamada, K., Urakawa, H., Arai, E., Hamada, S., & Ishiguro, N. (2018). Predictors of complications in heat-treated autograft reconstruction after intercalary resection for malignant musculoskeletal tumors of the extremity. Journal of Surgical Oncology, 117(7), 1469–1478. https://doi.org/10.1002/jso.25028.

    Article  Google Scholar 

  40. Igarashi, K., Yamamoto, N., Shirai, T., Hayashi, K., Nishida, H., Kimura, H., Takeuchi, A. & Tsuchiya, H. (2014). The long-term outcome following the use of frozen autograft treated with liquid nitrogen in the management of bone and soft-tissue sarcomas. Bone and Joint Journal, 96 B(4), 555–561. https://doi.org/10.1302/0301-620X.96B4.32629.

    Article  CAS  Google Scholar 

  41. Shimozaki, S., Yamamoto, N., Shirai, T., Nishida, H., Hayashi, K., Tanzawa, Y., Kimura, H., Takeuchi, A., Igarashi, K., Inatani, H., Kato, T., & Tsuchiya, H. (2014). Pedicle versus free frozen autograft for reconstruction in malignant bone and soft tissue tumors of the lower extremities. Journal of Orthopaedic Science, 19(1), 156–163. https://doi.org/10.1007/s00776-013-0487-x.

    Article  PubMed  Google Scholar 

  42. Eward, W. C., Kontogeorgakos, V., Levin, L. S., & Brigman, B. E. (2010). Free vascularized fibular graft reconstruction of large skeletal defects after tumor resection. Clinical Orthopaedics and Related Research, 468(2), 590–598. https://doi.org/10.1007/s11999-009-1053-x.

    Article  PubMed  Google Scholar 

  43. Stevenson, J. D., Doxey, R., Abudu, A., Parry, M., Evans, S., Peart, F., & Jeys, L. (2018). Vascularized fibular epiphyseal transfer for proximal humeral reconstruction in children with a primary sarcoma of bone. Bone and Joint Journal, 100B(4), 535–541. https://doi.org/10.1302/0301-620X.100B4.BJJ-2017-0830.R1.

    Article  Google Scholar 

  44. Demiralp, B., Ege, T., Kose, O., Yurttas, Y., & Basbozkurt, M. (2014). Reconstruction of intercalary bone defects following bone tumor resection with segmental bone transport using an Ilizarov circular external fixator. Journal of Orthopaedic Science, 19(6), 1004–1011. https://doi.org/10.1007/s00776-014-0632-1.

    Article  PubMed  Google Scholar 

  45. Watanabe, K., Tsuchiya, H., Yamamoto, N., Shirai, T., Nishida, H., Hayashi, K., Takeuchi, A., Matsubara, H., & Nomura, I. (2013). Over 10-year follow-up of functional outcome in patients with bone tumors reconstructed using distraction osteogenesis. Journal of Orthopaedic Science, 18(1), 101–109. https://doi.org/10.1007/s00776-012-0327-4.

    Article  PubMed  Google Scholar 

  46. Gupta, A., Pollock, R., Cannon, S. R., Briggs, T. W. R., Skinner, J., & Blunn, G. (2006). A knee-sparing distal femoral endoprosthesis using hydroxyapatite-coated extracortical plates: preliminary results. Journal of Bone and Joint Surgery, 88-B(10), 1367–1372. https://doi.org/10.1302/0301-620X.88B10.17756.

    Article  Google Scholar 

  47. Spiegelberg, B. G. I., Sewell, M. D., Aston, W. J. S., Blunn, G. W., Pollock, R., Cannon, S. R., & Briggs, T. W. R. (2009). The early results of joint-sparing proximal tibial replacement for primary bone tumours, using extracortical plate fixation. Journal of Bone and Joint Surgery, 91-B(10), 1373–1377. https://doi.org/10.1302/0301-620X.91B10.22076.

    Article  Google Scholar 

  48. Agarwal, M., Puri, A., Gulia, A., & Reddy, K. (2010). Joint-sparing or physeal-sparing diaphyseal resections: the challenge of holding small fragments. Clinical Orthopaedics and Related Research, 468(11), 2924–2932. https://doi.org/10.1007/s11999-010-1458-6.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Capanna, R., Bufalini, C., & Campanacci, M. (1993). A new technique for reconstructions of large metadiaphyseal bone defects. Orthopaedics and Traumatology, 2(3), 159–177. https://doi.org/10.1007/bf02620523.

    Article  Google Scholar 

  50. Ogura, K., Miyamoto, S., Sakuraba, M., Fujiwara, T., Chuman, H., & Kawai, A. (2015). Intercalary reconstruction after wide resection of malignant bone tumors of the lower extremity using a composite graft with a devitalized autograft and a vascularized fibula. Sarcoma, 2015, 861575. https://doi.org/10.1155/2015/861575.

    Article  Google Scholar 

  51. Davidson, A. W., Hong, A., McCarthy, S. W., & Stalley, P. D. (2005). En-bloc resection, extracorporeal irradiation, and re-implantation in limb salvage for bony malignancies. The Journal of Bone and Joint Surgery, 87-B(6), 851–857. https://doi.org/10.1302/0301-620x.87b6.15950.

    Article  Google Scholar 

  52. Sys, G., Uyttendaele, D., Poffyn, B., Verdonk, R., & Verstraete, K. L. (2002). Extracorporeally irradiated autografts in pelvic reconstruction after malignant tumour resection. International Orthopaedics, 26(3), 174–178. https://doi.org/10.1007/s00264-002-0352-6.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Marcove, R. C., & Miller, T. R. (1969). Treatment of primary and metastatic bone tumors by cryosurgery. JAMA: The Journal of the American Medical Association, 207(10), 1890–1894. https://doi.org/10.1001/jama.1969.03150230104014.

    Article  CAS  PubMed  Google Scholar 

  54. Marcove, R. C. (1982). A 17-year review of cryosurgery in the treatment of bone tumors. Clinical Orthopaedics and Related Research, 163(5), 231–234. https://doi.org/10.1097/00003086-198203000-00035.

  55. Yamamoto, N., Tsuchiya, H., & Tomita, K. (2003). Effects of liquid nitrogen treatment on the proliferation of osteosarcoma and the biomechanical properties of normal bone. Journal of Orthopaedic Science, 8(3), 374–380. https://doi.org/10.1007/s10776-002-0626-3.

    Article  PubMed  Google Scholar 

  56. Tsuchiya, H., Nishida, H., Srisawat, P., Shirai, T., Hayashi, K., Takeuchi, A., Yamamoto, N., & Tomita, K. (2010). Pedicle frozen autograft reconstruction in malignant bone tumors. Journal of Orthopaedic Science, 15(3), 340–349. https://doi.org/10.1007/s00776-010-1458-0.

    Article  PubMed  Google Scholar 

  57. Takata, M., Sugimoto, N., Yamamoto, N., Shirai, T., Hayashi, K., Nishida, H., Tanzawa, Y., Kimura, H., Miwa, S., Takeuchi, A., & Tsuchiya, H.  (2011). Activity of bone morphogenetic protein-7 after treatment at various temperatures: freezing vs. pasteurization vs. allograft. Cryobiology, 63(3), 235–239. https://doi.org/10.1016/j.cryobiol.2011.09.001.

    Article  CAS  Google Scholar 

  58. Nishida, H., Tsuchiya, H., & Tomita, K. (2008). Re-implantation of tumour tissue treated by cryotreatment with liquid nitrogen induces anti-tumour activity against murine osteosarcoma. The Journal of Bone and Joint Surgery, 90-B(9), 1249–1255. https://doi.org/10.1302/0301-620X.90B9.20671.

    Article  Google Scholar 

  59. Nishida, H., Yamamoto, N., Tanzawa, Y., & Tsuchiya, H. (2011). Cryoimmunology for malignant bone and soft-tissue tumors. International Journal of Clinical Oncology, 16(2), 109–117. https://doi.org/10.1007/s10147-011-0218-2.

    Article  PubMed  Google Scholar 

  60. Nishida, H., Shirai, T., Hayashi, K., Takeuchi, A., Tanzawa, Y., Mizokami, A., Namiki, M., & Tsuchiya, H. (2011). Cryotreatment against metastatic renal cell bone tumour reduced multiple lung metastases. Anticancer Research, 31(9), 2927–2930.

  61. Nakajima, C., Uekusa, Y., Iwasaki, M., Yamaguchi, N., Mukai, T., Gao, P., Tomura, M., Ono, S., Tsujimura, T., Fujiwara, H., & Hamaoka, T. (2001). A role of interferon-γ (IFN-γ) in tumor immunity: T cells with the capacity to reject tumor cells are generated but fail to migrate to tumor sites in IFN-γ-deficient mice. Cancer Research, 61(8), 3399–3405.

    CAS  PubMed  Google Scholar 

  62. Tugues, S., Burkhard, S. H., Ohs, I., Vrohlings, M., Nussbaum, K., Vom Berg, J., Kulig, P., & Becher, B. (2015). New insights into IL-12-mediated tumor suppression. Cell Death and Differentiation, 22(2), 237–246. https://doi.org/10.1038/cdd.2014.134.

    Article  CAS  PubMed  Google Scholar 

  63. Kuroda, A., Tabuchi, T., Iwami, E., Sasahara, K., Matsuzaki, T., Nakajima, T., Tsutsumi, Y., Eguchi, K., & Terashima, T. (2019). Abscopal effect of radiation on multiple lung metastases of lung adenocarcinoma: a case report. BMC Cancer, 19(1), 336. https://doi.org/10.1186/s12885-019-5566-8.

  64. Heitmann, C., Erdmann, D., & Levin, L. S. (2002). Treatment of segmental defects of the humerus with an osteoseptocutaneous fibular transplant. The Journal of Bone and Joint Surgery, 84-A(12), 2216–2223. https://doi.org/10.2106/00004623-200212000-00014.

    Article  CAS  Google Scholar 

  65. Taylor, G. I., Miller, G. D. H., & Ham, F. J. (1975). The free vascularized bone graft. Plastic and Reconstructive Surgery, 55(5), 533–544. https://doi.org/10.1097/00006534-197505000-00002.

    Article  CAS  Google Scholar 

  66. Weiland, A. J., Kleinert, H. E., Kutz, J. E., & Daniel, R. K. (1979). Free vascularized bone grafts in surgery of the upper extremity. Journal of Hand Surgery, 4(2), 129–144. https://doi.org/10.1016/S0363-5023(79)80129-X.

    Article  CAS  PubMed  Google Scholar 

  67. Chen, C. M., Disa, J. J., Lee, H. Y., Mehrara, B. J., Hu, Q. Y., Nathan, S., Boland, P., Healey, J., & Cordeiro, P. G. (2007). Reconstruction of extremity long bone defects after sarcoma resection with vascularized fibula flaps: a 10-year review. Plastic and Reconstructive Surgery, 119(3), 915–924. https://doi.org/10.1097/01.prs.0000252306.72483.9b.

    Article  CAS  Google Scholar 

  68. Manfrini, M., Innocenti, M., Ceruso, M., & Mercuri, M. (2003). Original biological reconstruction of the hip in a 4-year-old girl. Lancet, 361(9352), 140–142. https://doi.org/10.1016/S0140-6736(03)12192-7.

    Article  PubMed  Google Scholar 

  69. Petersen, M. M., Hovgaard, D., Elberg, J. J., Rechnitzer, C., Daugaard, S., & Muhic, A. (2010). Vascularized fibula grafts forreconstruction of bone defects after resection of bone sarcomas. Sarcoma, 2010, 524721. https://doi.org/10.1155/2010/524721.

    Article  Google Scholar 

  70. Accadbled, F., Thévenin Lemoine, C., Poinsot, E., Baron Trocellier, T., Dauzere, F., & De Gauzy, J. S. (2019). Bone reconstruction after malignant tumour resection using a motorized lengthening intramedullary nail in adolescents: preliminary results. Journal of Children’s Orthopaedics, 13(3), 324–329. https://doi.org/10.1302/1863-2548.13.190016.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Cañadell, J., Forriol, F., & Cara, J. A. (1994). Removal of metaphyseal bone tumours with preservation of the epiphysis. Physeal distraction before excision. The Journal of bone and joint surgery. 76-B(1), 127–32.

  72. Betz, M., Dumont, C. E., Fuchs, B., & Exner, G. U. (2012). Physeal distraction for joint preservation in malignant metaphyseal bone tumors in children. Clinical Orthopaedics and Related Research, 470(6), 1749–1754. https://doi.org/10.1007/s11999-011-2224-0.

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank Mr. Toshiya Nomura for drawing the figures. We also would like to thank Editage (www.editage.com) for English language editing.

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Authors and Affiliations

  1. Department of Orthopaedic Surgery, Kanazawa University Graduate School of Medical Sciences, 13-1 Takara-machi, Kanazawa, 920-8641, Japan

    Akihiko Takeuchi, Norio Yamamoto, Katsuhiro Hayashi, Hidenori Matsubara, Shinji Miwa, Kentaro Igarashi & Hiroyuki Tsuchiya

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  1. Akihiko Takeuchi
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  2. Norio Yamamoto
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  7. Hiroyuki Tsuchiya
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Contributions

Conception and design: AT, HT, and SM

Writing, review, and/or revision of the manuscript: AT, HT, SM, and KH

Searched the literature and edited the manuscript: NY and KI

All authors read approved the final manuscript.

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Correspondence to Akihiko Takeuchi.

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Takeuchi, A., Yamamoto, N., Hayashi, K. et al. Joint-preservation surgery for pediatric osteosarcoma of the knee joint. Cancer Metastasis Rev 38, 709–722 (2019). https://doi.org/10.1007/s10555-019-09835-z

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