Background Limb-salvage surgery has been well recognized as a standard treatment and alternative to amputation for patients with malignant bone tumors. Various limb-sparing techniques have been developed including tumor prosthesis, allograft, autograft and graft-prosthesis composite. However, each of these methods has short- and long-term disadvantages such as nonunion, mechanical failures and poor limb function. The technique of intracorporeal devitalization of tumor-bearing bone segment in situ by microwave-induced hyperthermia after separating it from surrounding normal tissues with a safe margin is a promising limb-salvage method, which may avoid some shortcomings encountered by the above-mentioned conventional techniques. The purpose of this study is to assess the healing process and revitalization potential of the devitalized bone segment by this method in a dog model. In addition, the immediate effect of microwave on the biomechanical properties of bone tissue was also explored in an in vitro experiment. Methods We applied the microwave-induced hyperthermia to devitalize the distal femurs of dogs in situ. Using a monopole microwave antenna, we could produce a necrotic bone of nearly 20 mm in length in distal femur. Radiography, bone scintigraphy, microangiography, histology and functional evaluation were performed at 2 weeks and 1, 2, 3, 6, 9 and 12 months postoperatively to assess the healing process. In a biomechanical study, two kinds of bone specimens, 3 and 6 cm in length, were used for compression and three-point bending test respectively immediately after extracorporeally devitalized by microwave. Findings An in vivo study showed that intracorporeally and in situ devitalized bone segment by microwave had great revitalization potential. An in vitro study revealed that the initial mechanical strength of the extracorporeally devitalized bone specimen may not be affected by microwave. Conclusion Our results suggest that the intracorporeal microwave devitalization of tumor-bearing bone segment in situ may be a promising limb-salvage method.
References
[1]
Baumgart R, Lenze U (2009) Expandable endoprostheses in malignant bone tumors in children: indications and limitations. Recent Results Cancer Res 179: 59–73.
[2]
Kumta SM, Cheng JC, Li CK, Griffith JF, Chow LT, et al. (2002) Scope and limitations of limb-sparing surgery in childhood sarcomas. J Pediatr Orthop 22: 244–248.
[3]
Muscolo DL, Ayerza MA, Aponte-Tinao L, Farfalli G (2008) Allograft reconstruction after sarcoma resection in children younger than 10 years old. Clin Orthop Relat Res 466: 1856–1862.
[4]
Saghieh S, Abboud MR, Muwakkit SA, Saab R, Rao B, et al. (2010) Seven-year experience of using Repiphysis expandable prosthesis in children with bone tumors. Pediatr Blood Cancer 55: 457–463.
[5]
Ottaviani G, Robert RS, Huh WW, Jaffe N (2009) Functional, psychosocial and professional outcomes in long-term survivors of lower-extremity osteosarcomas: amputation versus limb salvage. Cancer Treat Res 152: 421–436.
[6]
Marulanda GA, Henderson ER, Johnson DA, Letson GD, Cheong D (2008) Orthopedic surgery options for the treatment of primary osteosarcoma. Cancer Control 15: 13–20.
[7]
Kinkel S, Lehner B, Kleinhans JA, Jakubowitz E, Ewerbeck V, et al. (2009) Medium to long-term results after reconstruction of bone defects at the knee with tumor endoprostheses. J Surg Oncol 101: 166–169.
[8]
Mankin HJ, Gebhardt MC, Jennings LC, Springfield DS, Tomford WW (1996) Long-term results of allograft replacement in the management of bone tumors. Clin Orthop Relat Res 324: 86–97.
[9]
Ogilvie CM, Crawford EA, Hosalkar HS, King JJ, Lackman RD (2009) Long-term results for limb salvage with osteoarticular allograft reconstruction. Clin Orthop Relat Res 467: 2685–2690.
[10]
Manabe J, Ahmed AR, Kawaguchi N, Matsumoto S, Kuroda H (2004) Pasteurized autologous bone graft in surgery for bone and soft tissue sarcoma. Clin Orthop Relat Res 419: 258–266.
[11]
Moran M, Stalley PD (2009) Reconstruction of the proximal humerus with a composite of extracorporeally irradiated bone and endoprosthesis following excision of high grade primary bone sarcomas. Arch Orthop Trauma Surg 129: 1339–1345.
[12]
Chen CF, Chen WM, Cheng YC, Chiang CC, Huang CK, et al. (2009) Extracorporeally irradiated autograft-prosthetic composite arthroplasty using AML extensively porous-coated stem for proximal femur reconstruction: a clinical analysis of 14 patients. J Surg Oncol 100: 418–422.
[13]
Shimizu K, Masumi S, Yano H, Fukunaga T, Ikebe S, et al. (1999) Revascularization and new bone formation in heat-treated bone grafts. Arch Orthop Trauma Surg 119: 57–61.
[14]
Bohm P, Fritz J, Thiede S, Budach W (2003) Reimplantation of extracorporeal irradiated bone segments in musculoskeletal tumor surgery: clinical experience in eight patients and review of the literature. Langenbecks Arch Surg 387: 355–365.
[15]
Bohm P, Springfeld R, Springer H (1998) Re-implantation of autoclaved bone segments in musculoskeletal tumor surgery. Clinical experience in 9 patients followed for 1.1–8.4 years and review of the literature. Arch Orthop Trauma Surg 118: 57–65.
[16]
Canadell J, Forriol F, Cara JA (1994) Removal of metaphyseal bone tumours with preservation of the epiphysis. Physeal distraction before excision. J Bone Joint Surg Br 76: 127–132.
[17]
Quan GM, Slavin JL, Schlicht SM, Smith PJ, Powell GJ, et al. (2005) Osteosarcoma near joints: assessment and implications. J Surg Oncol 91: 159–166.
[18]
Kawaguchi N, Ahmed AR, Matsumoto S, Manabe J, Matsushita Y (2004) The concept of curative margin in surgery for bone and soft tissue sarcoma. Clin Orthop Relat Res 419: 165–172.
[19]
Cho HS, Oh JH, Han I, Kim HS (2009) Joint-preserving limb salvage surgery under navigation guidance. J Surg Oncol 100: 227–232.
[20]
Kumta SM, Chow TC, Griffith J, Li CK, Kew J, et al. (1999) Classifying the location of osteosarcoma with reference to the epiphyseal plate helps determine the optimal skeletal resection in limb salvage procedures. Arch Orthop Trauma Surg 119: 327–331.
[21]
Abed YY, Beltrami G, Campanacci DA, Innocenti M, Scoccianti G, et al. (2009) Biological reconstruction after resection of bone tumours around the knee: long-term follow-up. J Bone Joint Surg Br 91: 1366–1372.
[22]
Watanabe H, Ahmed AR, Shinozaki T, Yanagawa T, Terauchi M, et al. (2003) Reconstruction with autologous pasteurized whole knee joint II: application for osteosarcoma of the proximal tibia. J Orthop Sci 8: 180–186.
[23]
Jeon DG, Kim MS, Cho WH, Song WS, Lee SY (2007) Pasteurized autograft-prosthesis composite for distal femoral osteosarcoma. J Orthop Sci 12: 542–549.
[24]
Jeon DG, Kim MS, Cho WH, Song WS, Lee SY (2007) Pasteurized autograft-prosthesis composite for reconstruction of proximal tibia in 13 sarcoma patients. J Surg Oncol 96: 590–597.
[25]
Jeys L, Grimer R (2009) The long-term risks of infection and amputation with limb salvage surgery using endoprostheses. Recent Results Cancer Res 179: 75–84.
[26]
Bullens PH, Minderhoud NM, de Waal Malefijt MC, Veth RP, Buma P, et al. (2009) Survival of massive allografts in segmental oncological bone defect reconstructions. Int Orthop 33: 757–760.
[27]
Tyler WK, Healey JH, Morris CD, Boland PJ, O'Donnell RJ (2009) Compress periprosthetic fractures: interface stability and ease of revision. Clin Orthop Relat Res 467: 2800–2806.
[28]
Zouari L, Bousson V, Hamze B, Roulot E, Roqueplan F, et al. (2008) CT-guided percutaneous laser photocoagulation of osteoid osteomas of the hands and feet. Eur Radiol 18: 2635–2641.
[29]
Nielsen OS, Horsman M, Overgaard J (2001) A future for hyperthermia in cancer treatment? Eur J Cancer 37: 1587–1589.
[30]
Wust P, Hildebrandt B, Sreenivasa G, Rau B, Gellermann J, et al. (2002) Hyperthermia in combined treatment of cancer. Lancet Oncol 3: 487–497.
[31]
Gillams A (2008) Tumour ablation: current role in the liver, kidney, lung and bone. Cancer Imaging 8 Spec No A: S1–5.
[32]
Liapi E, Geschwind JF (2007) Transcatheter and ablative therapeutic approaches for solid malignancies. J Clin Oncol 25: 978–986.
[33]
Simon CJ, Dupuy DE (2005) Image-guided ablative techniques in pelvic malignancies: radiofrequency ablation, cryoablation, microwave ablation. Surg Oncol Clin N Am 14: 419–431.
[34]
Carrafiello G, Lagana D, Mangini M, Fontana F, Dionigi G, et al. (2008) Microwave tumors ablation: principles, clinical applications and review of preliminary experiences. Int J Surg 6: Suppl 1S65–69.
[35]
Simon CJ, Dupuy DE (2006) Percutaneous minimally invasive therapies in the treatment of bone tumors: thermal ablation. Semin Musculoskelet Radiol 10: 137–144.
[36]
Fan QY, Ma BA, Zhou Y, Zhang MH, Hao XB (2003) Bone tumors of the extremities or pelvis treated by microwave-induced hyperthermia. Clin Orthop Relat Res 406: 165–175.
[37]
Fan QY, Ma BA, Qlu XC, Li YL, Ye J, et al. (1996) Preliminary report on treatment of bone tumors with microwave-induced hyperthermia. Bioelectromagnetics 17: 218–222.
[38]
Van Laere K, Casier K, Uyttendaele D, Mondelaers W, De Sadeleer C, et al. (1998) Technetium-99m-MDP scintigraphy and long-term follow-up of treated primary malignant bone tumors. J Nucl Med 39: 1563–1569.
[39]
Mankin HJ, Springfield DS, Gebhardt MC, Tomford WW (1992) Current status of allografting for bone tumors. Orthopedics 15: 1147–1154.
[40]
Morello E, Buracco P, Martano M, Peirone B, Capurro C, et al. (2001) Bone allografts and adjuvant cisplatin for the treatment of canine appendicular osteosarcoma in 18 dogs. J Small Anim Pract 42: 61–66.
[41]
Ehara S, Nishida J, Shiraishi H, Tamakawa Y (2000) Pasteurized intercalary autogenous bone graft: radiographic and scintigraphic features. Skeletal Radiol 29: 335–339.
[42]
Ahmed AR (2009) Technetium-99 m-MDP scintigraphy and long-term follow-up of musculo-skeletal sarcoma reconstructed with pasteurized autologous bone graft. Arch Orthop Trauma Surg 129: 475–482.
[43]
Enneking WF, Campanacci DA (2001) Retrieved human allografts : a clinicopathological study. J Bone Joint Surg Am 83-A: 971–986.
[44]
Asada N, Tsuchiya H, Kitaoka K, Mori Y, Tomita K (1997) Massive autoclaved allografts and autografts for limb salvage surgery. A 1–8 year follow-up of 23 patients. Acta Orthop Scand 68: 392–395.
[45]
Eisenschenk A, Witzel C, Lautenbach M, Ekkernkamp A, Weber U, et al. (2006) Impact of radiation therapy on healing and stability of vascularized bone grafts in a dog model. Microsurgery 26: 412–416.
[46]
Liebergall M, Abu-Sneineh CH, Eylon S, Mendelson S, Segal D, et al. (2000) Effect of microwave oven induced mild hyperthermia on bone viability and strength. Clin Orthop Relat Res 372: 272–279.
[47]
Rong Y, Sato K, Sugiura H, Ito T, Sakano S, et al. (1995) Effect of elevated temperature on experimental swarm rat chondrosarcoma. Clin Orthop Relat Res 311: 227–231.
[48]
Lu DS, Raman SS, Vodopich DJ, Wang M, Sayre J, et al. (2002) Effect of vessel size on creation of hepatic radiofrequency lesions in pigs: assessment of the “heat sink” effect. AJR Am J Roentgenol 178: 47–51.
[49]
Kolios MC, Sherar MD, Hunt JW (1995) Large blood vessel cooling in heated tissues: a numerical study. Phys Med Biol 40: 477–494.
[50]
Kubo T, Sugita T, Shimose S, Arihiro K, Tanaka H, et al. (2004) Histological findings in a human autogenous pasteurized bone graft. Anticancer Res 24: 1893–1896.
[51]
Shin S, Yano H, Fukunaga T, Ikebe S, Shimizu K, et al. (2005) Biomechanical properties of heat-treated bone grafts. Arch Orthop Trauma Surg 125: 1–5.
[52]
Liebergall M, Simkin A, Mendelson S, Rosenthal A, Amir G, et al. (1998) Effect of moderate bone hyperthermia on cell viability and mechanical function. Clin Orthop Relat Res 349: 242–248.
[53]
Poffyn B, Sys G, Van Maele G, Van Hoorebeke L, Forsyth R, et al. (2010) Radiographic analysis of extracorporeally irradiated autografts. Skeletal Radiol 39: 999–1008.
