The use of extracorporeally irradiated autografts in pelvic reconstruction following tumour resection
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1 ONCOLOGY The use of extracorporeally irradiated autografts in pelvic reconstruction following tumour resection H. Wafa, R. J. Grimer, L. Jeys, A. T. Abudu, S. R. Carter, R. M. Tillman From The Royal Orthopaedic Hospital NHS Trust, Bristol Road South, Birmingham, United Kingdom The aim of this study was to evaluate the functional and oncological outcome of extracorporeally irradiated autografts used to reconstruct the pelvis after a P1/2 internal hemipelvectomy. The study included 18 patients with a primary malignant bone tumour of the pelvis. There were 13 males and five females with a mean age of 24.8 years (8 to 62). Of these, seven had an osteogenic sarcoma, six a Ewing s sarcoma, and five a chondrosarcoma. At a mean follow-up of 51.6 months (4 to 185), nine patients had died with metastatic disease while nine were free from disease. Local recurrence occurred in three patients all of whom eventually died of their disease. Deep infection occurred in three patients and required removal of their graft in two while the third underwent a hindquarter amputation for extensive flap necrosis. The mean Musculoskeletal Tumor Society functional score of the 16 patients who could be followed-up for at least 12 months was 77% (50 to 90). Those 15 patients who completed the Toronto Extremity Salvage Score questionnaire had a mean score of 71% (53 to 85). Extracorporeal irradiation and re-implantation of bone is a valid method of reconstruction after an internal hemipelvectomy. It has an acceptable morbidity and a functional outcome that compares favourably with other available reconstructive techniques. Cite this article: Bone Joint J 2014;96-B: H. Wafa, MSc (Orth), MD, FRCSEd(Tr&Orth), Consultant Orthopaedic R. J. Grimer, FRCS(Tr&Orth), DSc, Consultant Orthopaedic L. Jeys, FRCS(Tr&Orth), Consultant Orthopaedic A. T. Abudu, FRCS(Tr& Orth), Consultant Orthopaedic S. R. Carter, FRCS, Consultant Orthopaedic R. M. Tillman, FRCS(Tr&Orth), Consultant Orthopaedic The Royal Orthopaedic Hospital NHS Trust, Bristol Road South, Northfield, Birmingham, West Midlands, B31 2AP, UK. Correspondence should be sent to Mr H. Wafa; hazem.wafa@nhs.net 2014 The British Editorial Society of Bone & Joint Surgery doi: / x.96b $2.00 Bone Joint J 2014;96-B: Received 24 November 2013; Accepted after revision 14 July 2014 Limb salvage surgery for pelvic sarcoma has now become a commonplace procedure. 1-5 The principles of resection are the same as for those in other anatomical regions of the body, namely resection of the tumour with clear margins, followed by reconstruction using a method that is safe and durable with a low complication rate and, if possible, restoration of near-normal function. The three main areas of the pelvis in which tumours arise have been classified by Enneking and Dunham 6 as P1 (ilium), P2 (acetabulum) and P3 (pubis and ischium). It is generally accepted that both P1 and P3 resections can be left empty or reconstructed by a variety of well-reported methods. 7,8 P2 and P2/3 resections are more challenging but are usually reconstructed using either a prosthesis or, sometimes, an allograft. 3,4,9-11 A far more difficult challenge is the P1/2 resection (Fig. 1) where the whole of the ilium and the hip joint have been resected. Some authors have favoured resection arthroplasty in this situation, believing that the functional result is acceptable, especially when taking into account the reported complication rate for reconstruction. 5,12 One of the main problems of any reconstruction is attaching the prosthesis/ allograft to the side of the sacrum (which will have been partially resected in most cases) while providing a stable seating for any reconstruction of the hip. In this situation, both endoprosthetic replacement and allograft reconstruction have a high rate of failure. 13,14 It is, however, desirable to reconstruct the pelvis as anatomically as possible to maintain limb length and muscle function and leave a leg which functions almost normally. The re-implantation of segments of tumourbearing bone which have been excised and sterilised by means of irradiation or autoclaving has been reported by many authors to be a viable method of reconstruction Since 1996, we have used this technique in a selected number of patients for whom there is no other simple or reliable form of reconstruction. We report our experience of using this technique for reconstruction after resection of a pelvic P1/2 tumour. Patients and Methods Between 1996 and 2012, 18 patients with a primary malignant tumour of the pelvis involving the ilium and acetabulum were treated in 1404 THE BONE & JOINT JOURNAL
2 THE USE OF EXTRACORPOREALLY IRRADIATED AUTOGRAFTS IN PELVIC RECONSTRUCTION FOLLOWING TUMOUR RESECTION 1405 Fig. 1 Diagrammatic representation of the bone involved in P1/2 pelvic resection. Table I. Data on patients Case Age (yrs) Gender Site Diagnosis Complications Survival (mths) MSTS score TESS score Mankin score M P1,2 Chondrosarcoma Excellent 2 46 M P1,2 Chondrosarcoma Superficial wound DOD infection 3 20 M P1 Ewing s sarcoma Stress fracture Good 4 16 M P1 Ewing s sarcoma Local recurrence, DOD Good chest metastasis 5 8 M P1,2 Ewing s sarcoma Hip subluxation, Excellent 2 cm LLD 6 14 F P1 Ewing s sarcoma Superficial wound DOD Good infection 7 14 M P1 Ewing s sarcoma Local recurrence, DOD Good multiple metastasis 8 27 M P2 Osteosarcoma Local recurrence, DOD Excellent chest metastasis 9 13 F P1,2 Osteosarcoma Chest metastasis DOD Good F P1,2 Osteosarcoma Partial graft resorption, Fair AVN of the femoral head, chest metastasis F P1,2 Osteosarcoma Deep infection DOD Failure F P1,2 Osteosarcoma Hip dislocation, chest Excellent metastasis, acetabular loosening M P1,2 Osteosarcoma Deep infection DOD Failure M P2,3 Ewing s Sarcoma Chest metastasis DOD M P1,2 Chondrosarcoma Stress fracture Excellent M P1,2 Chondrosarcoma Deep infection with Failure flap necrosis M P1,2 Chondrosarcoma Excellent M P1 Osteosarcoma Excellent P1, Ilium; P2, Acetabulum; P3, Pubis; AVN, Avascular necrosis; DOD, Died of disease; AWD, Alive with evidence of disease; MSTS, Musculoskeletal Tumor Society; TESS, Toronto Extremity Salvage Score; LLD, leg length discrepancy our unit by en bloc resection of the lesion, with reconstruction by re-implantation of the extracorporeally-irradiated segment of bone. There were 13 males and five females with a mean age of 24.8 years (8 to 62). The histological diagnosis was osteosarcoma in seven patients, Ewing s sarcoma in six and chondrosarcoma in five (Table I). 20 All patients underwent pre-operative staging studies consisting of plain radiographs of the lesion, computed tomography (CT) of the lungs, 99 m Tc bone scanning and MRI of the pelvis to evaluate the extent of the lesion and to search for possible skip lesions. All patients with osteosarcoma and Ewing s sarcoma received pre- and post-operative adjuvant chemotherapy according to the protocol that the unit was using at the time. The decision to use this technique was based on the absence of a simple alternative form of reconstruction and VOL. 96-B, No. 10, OCTOBER 2014
3 1406 H. WAFA, R. J. GRIMER, L. JEYS, A. T. ABUDU, S. R. CARTER, R. M. TILLMAN Fig. 2a Fig. 2b a) Pre-operative anteroposterior (AP) pelvic radiograph of a 19-year-old female patient (patient 12) with osteosarcoma involving area P1/2; b) AP radiograph of the pelvis at 90 months follow-up showing incorporation of the irradiated bone segment. the expectation that its likely functional benefits exceeded any known risks. Operative technique. Wide excision of the tumour was carried out using a standard technique, usually through a curved incision over the iliac crest which was extended to the front of the thigh. The planned level of transection was determined in all cases in this series by measurement and reference to anatomical landmarks (although currently computer navigation would be used). 21,22 The resected segment was then taken away from the operating table and, in a sterile environment, all unnecessary soft tissue was removed, leaving only the insertions of important ligaments and tendons including the sartorius muscle, straight head of rectus femoris muscle, and tensor fasciae latae. Biopsies were taken from any worrying margin and sent separately. All visible tumour was removed from the bone and sent for histological examination and the resected segment was then wrapped in a sterile drape soaked in a solution of vancomycin (1 gm in 500 ml of saline) and placed in two sterile plastic bags before being transported to the radiotherapy department in a sealed box. The excised bone segment was irradiated with a dose of 90 Gy using a linear accelerator. The irradiation took about 35 minutes. After irradiation, the bone segment was brought back to the operating theatre, removed from the sterile drapes and soaked in a solution of isotonic saline and vancomycin before being re-implanted. The irradiated autografts were fixed to the remaining ilium and/or sacrum with plates (Fig. 2) and/or 6.5 mm cancellous screws (Fig. 3). A cemented total hip replacement (THR) was used in ten cases of acetabular resection and a Birmingham Hip Resurfacing (BHR, Smith & Nephew, Warwick, United Kingdom) in one. Two children had their own femoral heads left in place even though part of the acetabulum had been irradiated and re-implanted. The remaining five patients had P1 resections i.e. resections of the iliac bone above the level of the acetabulum. Each patient had five days of antibiotics and mechanical anti-embolism prophylaxis. Chemical prophylaxis was not used because of the high risk of bleeding from the large resection. Patients were usually kept in bed for five to ten days until the wound had healed and were then allowed to embark on toe-touch weight-bearing for six weeks. At this stage increased weight-bearing was allowed, progressing to full weight-bearing, usually at three months. All patients were re-admitted for a course of physiotherapy and hydrotherapy six weeks after their operation. Patients were then followed-up at three-monthly intervals with regular radiographs of the pelvis and chest for two years and at six-monthly intervals up to five years. Cross-sectional imaging was only used if there was concern about possible tumour recurrence, or if there were mechanical problems. In the patients who were alive at 12 months after operation, their outcome was assessed using the Musculoskeletal Tumor Society score (MSTS), 23 and their allografts were assessed according to Mankin et al s 20 allograft functional grading system. A total of 15 of those patients completed the Toronto Extremity Salvage Score questionnaire at the time of their final review (TESS). 24 Results At a mean follow-up of 51.6 months (4 to 185), nine patients had died with metastatic disease and nine were free from disease. All patients had clear surgical margins. Two patients, both with a Ewing s sarcoma, had clear margins but a poor response to chemotherapy with viable cells approaching the margin of excision. Both of these patients THE BONE & JOINT JOURNAL
4 THE USE OF EXTRACORPOREALLY IRRADIATED AUTOGRAFTS IN PELVIC RECONSTRUCTION FOLLOWING TUMOUR RESECTION 1407 Fig. 3a Fig. 3b Fig. 3c a) Pre-operative anteropsterior (AP) pelvic radiograph of a 21-year old male patient (patient 17) with chondrosarcoma of the P1/2 area; b) Coronal T1-weighted MR image showing tumour extension and c) AP radiograph of the pelvis at 12 months follow-up. The patient has an excellent Musculoskeletal Tumor Society functional score of 83%. developed local recurrence in the soft tissues, as did one patient with an osteosarcoma and a poor response to chemotherapy. One of these had a hindquarter amputation two months after his primary surgery, while the other two already had disseminated metastatic disease at the time of local recurrence and received palliative treatment. All three eventually died of disease progression. There were no recurrences in the irradiated bone. Identifying graft union was difficult both clinically and radiologically as no callus could be seen after rigid internal fixation of the resected segment of bone. No further surgery was needed for nonunion in any case: a pragmatic decision was made to allow partial weight-bearing for three months followed by full weight-bearing as comfort permitted. There have been no radiological failures at the sacroiliac joint even after prolonged follow-up. Three patients with a resection margin through the superior pubic ramus have an apparent nonunion but these patients remained asymptomatic. Partial graft resorption was seen in one patient (patient 10) who was aged 14 years at the time of initial surgery. She required a P1/2 resection and excision of gluteus medius but did not have a primary hip replacement. She returned to school and sports activities but developed avascular necrosis of the femoral head after 2.5 years, at which stage THR was undertaken. After ten years she developed further bone resorption with a central fracture-dislocation of the hip replacement. This was revised to a custom-made stemmed acetabular replacement. The patient is still capable of taking some weight on the affected limb and walks with two crutches 17 years after the original procedure. Another patient (patient 5) had an acetabular resection through the triradiate cartilage at the age of eight years. After 12 months he started to complain of pain and stiffness in the involved hip. Plain radiographs taken at that time showed closure of the triradiate cartilage. The stiffness at his hip was attributed to overgrowth of the femoral head VOL. 96-B, No. 10, OCTOBER 2014
5 1408 H. WAFA, R. J. GRIMER, L. JEYS, A. T. ABUDU, S. R. CARTER, R. M. TILLMAN relative to the non-growing acetabulum. At latest follow-up (94 months, now aged 16 years), he has regained a full painless range of movement of the hip. Clinical examination revealed a 2 cm leg-length discrepancy: plain radiographs showed slight subluxation of the femoral head outside the fused acetabulum. However, he was asymptomatic but walked with a slight limp and was able to play tennis and badminton and could referee rugby matches. Superficial wound infection occurred in two patients who were treated with wound debridement and parenteral antibiotics. Three patients developed a deep infection which necessitated removal of the graft in two, both of whom eventually died of metastatic disease at 16 and 39 months after their primary surgery. The third patient developed ischaemia of the posterior gluteal flap three weeks after the initial surgery and subsequently developed an infection, leading to the need for a hindquarter amputation. The mean MSTS functional score 23 in the 16 patients who could be followed-up for at least 12 months was 77% (50 to 90). Of those sixteen patients, five (31.3%) reported the need for a walking aid. The mean TESS of 15 patients was 71% (53 to 85) at final follow-up. According to Mankin s allograft functional grading system, 20 there were seven excellent, five good and one fair result, and three failures. Discussion Limb salvage surgery has become the standard treatment for a primary malignant bone tumour. Massive allograft reconstruction is a reasonable option but requires the establishment of a bone bank. However, there are difficulties in obtaining, processing and storing the allografts. Its major disadvantage is the relatively high risk of complication, the main ones being infection (11.8% to 38.5%), fracture (9.1%) and nonunion (18.8%). 3,4,25,26 Arthrodesis is rarely used after pelvic resection but hip transposition has been advocated as an inexpensive simple solution, with a reasonable functional outcome and a low rate of complication. Its main drawback is a permanently weak hip and short leg, with the need for at least one crutch in most cases. 26,27 Fuchs et al 28 reported a mean MSTS functional score of 48% in 12 patients after attempted primary iliofemoral fusion, with a mean MSTS score of 71% in the six patients who had a radiologically solid fusion compared with 25% in the subgroup with a pseudarthrosis. 28 Gebert et al 27,29 have described the hip transposition procedure following the periacetabular tumour resection. A type I 27 hip transposition can be used in those patients in whom the inferior part of the acetabulum is not involved by the tumour and can therefore be rotated by 90 and fixed to the preserved bone, while a MUTARS re-attachment tube (Implantcast GmbH, Buxtehude, Germany) is used in type II hip transposition when the whole acetabulum is resected with the tumour. They reported a mean leg shortening of 5.0 cm after type I reconstruction, 6.7 cm in type IIA, and 3.3 cm in type IIB. The mean MSTS functional score was 62% (43.3 to 93.3) in their series of 62 patients after a mean follow-up of 3.6 years. 29 High complication rates have been reported with the use of various types of endoprosthetic reconstruction because of difficulty in achieving adequate initial fixation and reliable bone ingrowth. 13,14,30-32 This precludes the use of these implants in patients needing a P1/2 resection. Menendez et al 11 reported a 56% incidence of major complications and 60% five-year implant survivorship with the use of the periacetabular reconstruction (PAR) endoprosthesis. There have been several reports on the outcome of the use of the saddle prosthesis in periacetabular tumours: the major reported complications were infection (16.7% to 26.7%), periprosthetic fracture (13.3% to 22.2%), and dislocation (18.8% to 22.2%), 1,30,31,33,34 with the patients having a mean MSTS functional score of 50.8% to 57%. However, the implant survivorship was poor being 33.3% at five years. 33 Fisher et al 2 reported the early results of inverted cone reconstruction of the pelvis. However, this type of pelvic replacement cannot be used to reconstruct a P1/2 resection as the stem of the prosthesis needs to be cited in the remaining ilium. Krieg et al 15 have reported the outcome of extracorporeally irradiated autografts for pelvic reconstruction in 13 patients with Ewing s sarcoma. No patient had macroscopic metastatic disease at diagnosis. Extracorporeal irradiation of the specimens in their series was performed using a single dose of 50 Gy. A total of four patients (31%) died from metastatic disease but none developed local recurrence. Local osteolysis was seen in three patients (23.1%), stress fracture in one (7.7%) and deep infection in one. They attributed their lower rate of graft complications including infection, bone resorption and fracture to the relatively lower dose of radiation. Higher doses of irradiation (> 250 Gy) seem to inactivate the proteins in the bone matrix thereby adversely affecting the revascularisation and osteoconductive properties of the irradiated bone. 15,35,36 Sys et al 19 reported a total of 13 complications in 15 patients who underwent pelvic reconstruction with an autograft irradiated extracorporeally with 300 Gy. A total of seven patients (46.7%) died after local recurrence of the tumour. It is not stated in their report whether local recurrence was present in the soft-tissue or in the irradiated bone. Our local control compares favourably with theirs. It therefore appears that a higher dose of irradiation (300 Gy vs 90 Gy) does not improve local control of the disease. They also reported three patients (20%) with a deep infection who responded to treatment with antibiotics. We were unable to control deep infection in any of our three patients while retaining the autograft, despite multiple wound debridements and washouts. The largest series of pelvic reconstructions using extracorporeally irradiated bone was reported by Hong et al. 37 They had 35 patients with a pelvic tumour and a 11% local THE BONE & JOINT JOURNAL
6 THE USE OF EXTRACORPOREALLY IRRADIATED AUTOGRAFTS IN PELVIC RECONSTRUCTION FOLLOWING TUMOUR RESECTION 1409 recurrence rate. No details were given about the type of resection or the functional outcome in these patients. We have now stopped using this technique in cases where the patient is likely to need adjuvant post-operative radiotherapy. Thus, any patient with a Ewing s sarcoma which is expected to respond poorly to chemotherapy and would therefore require radiotherapy, would be excluded. Although initially concerned about the ability to sterilise bone in cases of chondrosarcoma, we have had no recurrences to date and note that Hong et al 37 also had no recurrence in bone but reported a 20% local recurrence rate in soft-tissues. Longer term follow-up of these patients, possibly with international collaboration, would seem prudent. In summary, extracorporeal irradiation and reimplantation of part of the pelvis can result in improved function, with a relatively low rate of complications in selected patients. We believe that this procedure will inevitably only be indicated in a small proportion of patients with a pelvic tumour, but may allow reconstruction where no other option exists. The key indication, in our opinion, is the patient with a P1/2 tumour which can be safely resected with clear margins, and in whom the bone is of sufficient quality and solid enough to reimplant after extracorporeal radiotherapy. Relative contra-indications include any patient in whom another reconstruction may give a better outcome or if bony union is unlikely e.g. any patient requiring additional radiotherapy to the pelvis. It should ideally be used in patients with a reasonable prognosis as they can take up to a year to regain function. The problem of infection seems to have been resolved by soaking the bone in vancomycin while it is being irradiated. There have been no reported cases of tumour recurrence in the irradiated bone, even in cases of chondrosarcomas where the ability of radiotherapy to sterilise the bone is questionable. Any patient who is to undergo this procedure needs to be counselled carefully about the risks and benefits and should be warned of the possible late effects of bone resorption. No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. This article was primary edited by A. C. Ross and first proof edited by G. Scott. References 1. Aljassir F, Beadel GP, Turcotte RE, et al. Outcome after pelvic sarcoma resection reconstructed with saddle prosthesis. Clin Orthop Relat Res 2005;438: Fisher NE, Patton JT, Grimer RJ, et al. Ice-cream cone reconstruction of the pelvis: a new type of pelvic replacement: early results. J Bone Joint Surg [Br] 2011;93-B: Delloye C, Banse X, Brichard B, Docquier PL, Cornu O. Pelvic reconstruction with a structural pelvic allograft after resection of a malignant bone tumour. J Bone Joint Surg [Am] 2007;89-A: Bell RS, Davis AM, Wunder JS, et al. Allograft reconstruction of the acetabulum after resection of stage-iib sarcoma: intermediate-term results. J Bone Joint Surg [Am] 1997;79-A: Hu YC, Huang HC, Lun DX, Wang H. Resection hip arthroplasty as a feasible surgical procedure for periacetabular tumors of the pelvis. Eur J Surg Oncol 2012;38: Enneking WF, Dunham WK. Resection and reconstruction for primary neoplasms involving the innominate bone. J Bone Joint Surg [Am] 1978;60-A: Akiyama T, Clark JC, Miki Y, Choong PF. The non-vascularised fibular graft: a simple and successful method of reconstruction of the pelvic ring after internal hemipelvectomy. 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EK ET, Choong PF. Research: Is resection of tumours involving the pelvic ring justified? : A review of 49 consecutive cases. Int Semin Surg Oncol 2005;2: Krieg AH, Mani M, Speth BM, Stalley PD. Extracorporeal irradiation for pelvic reconstruction in Ewing s sarcoma. J Bone Joint Surg [Br] 2009;91-B: Khattak MJ, Umer M, Haroon-ur-Rasheed, Umar M. Autoclaved tumor bone for reconstruction: an alternative in developing countries. Clin Orthop Relat Res 2006;447: Uyttendaele D, De Schryver A, Claessens H, et al. Limb conservation in primary bone tumours by resection, extracorporeal irradiation and re-implantation. J Bone Joint Surg [Br] 1988;70-B: Chen WM, Chen TH, Huang CK, Chiang CC, Lo WH. Treatment of malignant bone tumours by extracorporeally irradiated autograft-prosthetic composite arthroplasty. J Bone Joint Surg [Br] 2002;84-B: Sys G, Uyttendaele D, Poffyn B, Verdonk R, Verstraete L. Extracorporeally irradiated autografts in pelvic reconstruction after malignant tumour resection. Int Orthop 2002;26: Mankin HJ, Gebhardt MC, Jennings LC, Springfield DS, Tomford WW. Longterm results of allograft replacement in the management of bone tumors. Clin Orthop Relat Res 1996;324: Ritacco LE, Milano FE, Farfalli GL, et al. Accuracy of 3-D planning and navigation in bone tumor resection. Orthopedics 2013;36: Jeys L, Matharu GS, Nandra RS, Grimer RJ. Can computer navigation-assisted surgery reduce the risk of an intralesional margin and reduce the rate of local recurrence in patients with a tumour of the pelvis or sacrum? Bone Joint J 2013;95- B: Enneking WF, Dunham W, Gebhardt MC, Malawer M, Pritchard DJ. A system for the functional evaluation of reconstructive procedures after surgical treatment of tumors of the musculoskeletal system. Clin Orthop Relat Res 1993;286: Davis AM, Wright JG, Williams JI, et al. Development of a measure of physical function for patients with bone and soft tissue sarcoma. Qual Life Res 1996;5: Ozaki T, Hillmann A, Bettin D, Wuisman P, Winkelmann W. High complication rates with pelvic allografts: experience of 22 sarcoma resections. Acta Orthop Scand 1996;67: Hillmann A, Hoffmann C, Gosheger G, et al. Tumors of the pelvis: complications after reconstruction. Arch Orthop Trauma Surg 2003;123: Gebert C, Gosheger G, Winkelmann W. Hip transposition as a universal surgical procedure for periacetabular tumours of the pelvis. J Surg Oncol 2009;99: Fuchs B, O Connor MI, Kaufman KR, Padgett DJ, Sim FH. Iliofemoral arthrodesis and pseudarthrosis: a long-term functional outcome evaluation. Clin Orthop Relat Res 2002;397: Gebert C, Wessling M, Hoffmann C, et al. Hip transposition as a limb salvage procedure following the resection of periacetabular tumors. J Surg Oncol 2011;103: Kitagawa Y, EK ET, Choong PF. Pelvic reconstruction using saddle prosthesis following limb salvage operation for periacetabular tumour. J Orthop Surg (Hong Kong) 2006;14: Donati D, D Apote G, Boschi M, Cevolani L, Benedetti MG. Clinical and functional outcomes of the saddle prosthesis. J Orthop Traumatol 2012;13: Schwartz AJ, Eckardt JJ, Beauchamp CP. Internal hemipelvectomy for musculoskeletal tumors-indications and options for reconstruction. US Oncology & Hematology 2011;7: Fu M, Shen JN, Huang G, et al. Reconstruction of the hemipelvis with saddle prosthesis after excision of malignant tumors around the pelvis and acetabulum: a report of 12 cases. Ai Zheng 2007;26: [Article in Chinese]. VOL. 96-B, No. 10, OCTOBER 2014
7 1410 H. WAFA, R. J. GRIMER, L. JEYS, A. T. ABUDU, S. R. CARTER, R. M. TILLMAN 34. Natarajan MV, Bose JC, Mazhavan V, Rajagopal TS, Selvam K. The saddle prosthesis in periacetabular tumours. Int Orthop 2001;25: Sabo D, Brocai DR, Eble M, Wannenmacher M, Ewerbeck V. Influence of extracorporeal irradiation on the reintegration of autologous grafts of bone and joint: study in a canine model. J Bone Joint Surg [Br] 2000;82-B: Currey JD, Foreman J, Laketi? I, et al. Effects of ionizing radiation on the mechanical properties of human bone. J Orthop Res 1997;15: Hong AM, Millington S, Ahern V, et al. Limb preservation surgery with extracorporeal irradiation in the management of malignant bone tumor: the oncological outcomes of 101 patients. Ann Oncol 2013;24: THE BONE & JOINT JOURNAL
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