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Table of Contents
ORIGINAL ARTICLE
Year : 2019  |  Volume : 27  |  Issue : 4  |  Page : 204-210

Biological reconstruction of the bone defects with free fibula flap after resections of extremity located bone tumors: Clinical and radiological short-term results


1 Department of Orthopaedics and Traumatology, School of Medicine, Dokuz Eylul University, Izmir, Turkey
2 Department of Orthopaedics and Traumatology, School of Medicine, Marmara University, Istanbul, Turkey

Date of Submission29-Dec-2018
Date of Acceptance01-Sep-2019
Date of Web Publication26-Sep-2019

Correspondence Address:
Dr. Onur Basci
Department of Orthopaedics and Traumatology, Dokuz Eylul University Hospital, Ortopedi Ve Travmatoloji Ad, Inciralti, Mithatpasa Cd., Inciralti Yerleskesi No: 1606, 35340 Narlidere, Balcova, Izmir
Turkey
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/tjps.tjps_72_19

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  Abstract 


Background: Recently, limb salvage surgery is a preferred method in orthopedic oncology and extremity-located bone tumors treated by limb salvage surgery have a 90%–95% success rate. The aim of the study is functional and radiological evaluations of the undergone biological reconstruction with free fibula flap (FFF) after tumor surgery and the effects of the defect size on the functional results. Subjects and Methods: Between 2005 and 2010, 13 patients (7M/6F) who underwent limb salvage surgery for benign/malignant bone tumors were included in study. Diagnoses included five osteosarcomas, six Ewing's sarcomas, one high-grade chondrosarcoma, and one aneurysmal bone cyst. Diaphyseal and metaphyseal regions of femur (7), humerus (3), tibia (2), and radius (1) were reconstructed. FFF was combined with a strut femoral allograft in seven cases. Postoperatively, partial weight-bearing allowed at postoperative 3 month and increased gradually. The mean follow-up was 25 months (12–60) and evaluated by extremity function scoring of Musculoskeletal Tumor Society (MSTS) and radiologically. Results: On the 6th month, in 92.3% of patients (12/13), evident union, and on the 12th month, in all of the patients, evident union and bone flap hypertrophy were observed. The mean MSTS score was measured 77.58% (46.66–100). As the resection size increased, the MSTS scores were significantly decreased (P = 0.027); as the bone flap size increased, there were relatively low MSTS scores (P = 0.440). On the patients without bone flap hypertrophy on 6th month, the bone flap size was measured relatively higher (P = 0.069) and the operation duration was relatively higher (P = 0.100). As the operation duration increased, there were relatively lower MSTS scores (P = 0.062). In cases where allograft and VFG combined (7/9 patients) had higher MSTS scores than the ones, only FFF was used (P = 0.621). Conclusions: Limb salvage surgery improves the life quality without worsening the prognosis and is a method that should be preferred. The biologic reconstruction of the defects with FFF, following extremity located musculoskeletal tumor resections have positive effects on functional outcomes.

Keywords: Biological reconstruction, limb salvage surgery, vascularized fibula


How to cite this article:
Basci O, Erol B. Biological reconstruction of the bone defects with free fibula flap after resections of extremity located bone tumors: Clinical and radiological short-term results. Turk J Plast Surg 2019;27:204-10

How to cite this URL:
Basci O, Erol B. Biological reconstruction of the bone defects with free fibula flap after resections of extremity located bone tumors: Clinical and radiological short-term results. Turk J Plast Surg [serial online] 2019 [cited 2019 Nov 20];27:204-10. Available from: http://www.turkjplastsurg.org/text.asp?2019/27/4/204/267931




  Introduction Top


Recently, limb salvage surgery is a preferred method in orthopedic oncology, under appropriate conditions. In the past, similar conditions were candidates for amputations. The limb salvage phenomenon is emerged after the applications of the effective chemotherapy techniques, especially for sarcomas in the 1970s. It is proven that, the long-term survivals of the patients with bone sarcomas managed by limb salvage surgery were not negatively affected when compared to classical amputation.[1]

By better understanding of the tumor biology, effective systemic chemotherapy, and advances on biomaterials, together with the improvements in surgical techniques such as microsurgery, patients with extremity located bone tumors are treated by limb salvage surgery with a 90%–95% success rate.[2]

In children undergoing limb salvage surgery for the treatment of malignant bone tumors in the lower extremities, several problems arise with growth. Especially, limb length differences and tumor prosthesis loosening can cause severe limb dysfunction.[3] Biological reconstructions with different techniques in children and young adults, provide an active return to life that does not require permanent reconstruction and subsequent revision surgery.[4]

In cases requiring intercalary bone resection, autogenous free osseous flaps with massive allografts and appropriate fixation materials are used for reconstruction of the formed bone defect. However, despite all these technical advances, the rate of total complications, including infection, fracture, and nonunion increases up to 50%.[5]

Reconstruction with free osseous flaps following tumor resections was first described by Mckee (1978), Ueba and Fujikawa (1983), and Taylor (1975). Free fibula flap (FFF) has been popularized in orthopedic oncology due to limb-sparing surgery after long-bone resections. Large intercalated bone defects can easily be reconstructed with fibular bone. However, it is used in combination with massive allografts, especially when used after femoral resections due to the fine structure of the fibula. To be functionally successful, it may be necessary to monitor the extremity without weight-bearing for a long time. This period gives the time necessary for the bone flap to begin to union with the parent bone, marked thickening, and callus formation.[6] In the early period, Capanna et al. proposed a combination of a FFF with an allograft until the fibula took over the entire physical burden.[7]

The positive effects of biologic reconstruction of the defects with FFF, following extremity located musculoskeletal tumor resections, on tumor survival and functional outcomes have led to the preference of this technique in our clinic. The aim of this study was to evaluate the functional and radiological short-term results of patients who underwent biological reconstruction with FFF after wide surgical resection of bone tumors in our clinic and to reveal the effect of defect size on functional results.


  Subjects and Methods Top


Patients

With the approval of Marmara University Faculty of Medicine Ethics Committee (B.30.2.MAR.0.01.02/AEK/148 on 24.11.2011), 13 patients treated with bone tumor and reconstructed with FFF (±structural allograft) following wide surgical resection in Marmara University, Faculty of Medicine, Department of Orthopedics and Traumatology, between 2006 and 2010 were included in the study. The mean age at diagnosis was 12 years (range 3–35 years) in seven male and six female patients.

Preoperatif evaluation

In all patients, conventional radiography, contrast-enhanced magnetic resonance imaging and whole-body bone scintigraphy, and contrast-enhanced thorax and abdominal computed tomography were performed for local spread of the tumor. After radiological staging, pathological diagnosis was made by closed trocar or open incisional biopsy, and it was taken into oncological evaluation for neoadjuvant chemotherapy according to tumor type.

Tumor type and localization

About 92.3% of the patients (12/13 patients) had a diagnosis of malignant bone tumor. All malignant bone tumors were evaluated as Stage 2B according to Enneking's malignant tumor staging system. One patient was diagnosed as an aneurysmal bone cyst; a benign but locally aggressive tumor. Diagnoses were reported as Ewing's sarcoma (six patients), classic (high grade, intramedullary) osteosarcoma (five patients), chondrosarcoma (high grade) (one patient), and aneurysmal bone cyst (one patient).

Tumor localizations were mostly located in the lower extremity in 69.2% (9/13 patients). The diaphysis and metaphysodiaphysis of the femur (seven patients), humerus (three patients), tibia (two patients), and radius (one patient) constituted the reconstructed regions.

Neoadjuvant – adjuvant therapy

A total of 11 patients diagnosed with osteosarcoma and Ewing sarcoma were treated by neoadjuvant and adjuvant chemotherapies with epirubicin, cisplatin, and isophosphamide protocol for osteosarcoma and with isophosphamide, epirubicin, vincristin, adriamycin, and cisplatin protocol for Ewing's sarcoma. Preoperative radiotherapy was not routinely applied to any patient. Postoperatively, only one patient with Ewing's sarcoma was treated with radiotherapy.

Surgical procedure

All patients underwent biological reconstruction with FFF following resection of the tumor with wide surgical margins [Figure 1]a and [Figure 1]b. In femur resections, it was aimed to protect the extensor mechanism in all patients during tumor resection by isolating the rectus femoris muscle from vastus intermedius muscle on the quadriceps tendon level and partially preserving the vastus medialis or lateralis muscles according to tumor location. The mean amount of bone resection was 16.30 cm (range 9–25 cm). Fibula was prepared by Gilbert method leaving a thin layer of muscle on the posteromedial surface to protect the vascular pedicle. At the end of the procedure, the tourniquet was opened and bleeding of the periosteal and bone ends was observed, and the firmness of the pedicle was confirmed. The fibula was allowed to perfuse in its bed until the reconstruction site was prepared [Figure 2]a. Surgical instruments, gowns, gloves, and dressing were renewed to prevent tumor transplantation in these areas before the fibula was inserted. The flap pedicles were anastomosed with the recipient vessels of the femoral artery in femoral reconstructions, brachial artery in humeral reconstructions, radial artery in radius reconstruction, together with their adjacent veins. The anastomoses were performed by end-to-end fashion; however, in the absence of the recipient branches near to the resection site, end-to-side anastomosis was performed (2 femora, 1 humerus, and 1 radius). The fixation was performed with the appropriate method, while the anastomosis site was protected. Two different reconstruction techniques with FFF were used. In seven patients with lower extremity involvement, the FFF was used in combination with massive allografts as described by Capanna et al., whereas in the remaining six patients, it was used alone for reconstruction [Figure 2]b and [Figure 2]c. The mean length of the FFF used was 17.46 cm (range 13–23 cm), and the total duration of the operation was 8 h and 51 min (range 4.5–11.8 h).
Figure 1: (a) Wide surgical resection. (b) humoral material after resection

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Figure 2: (a) Fibular graft harvesting. (b) Strut femoral allograft. (c) Reconstruction with vascularized fibular graft in combination with strut femoral allograft

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Postoperative patient management

All patients were followed up with a rigid and fixed protocol postoperatively. Accordingly, all patients were followed up in the intensive care unit during the first 24–48 h postoperatively. Immediately after surgical anastomosis, 2 × 0.6 cc low-molecular-weight heparin (enoxaparin sodium) intramuscular and anticoagulant citrate dextrose solution (Rheomacrodex) were administered intravenously. Hemoglobin levels and systolic arterial blood pressures were maintained above 10 mg/dl and 100 mmHg, respectively.

In the early postoperative period, joint range of motion exercises was started under the guidance of a physiotherapist, and the patient was started to walk with double crutches or walker without weight bearing on the 2nd and 3rd weeks. After radiographic union was detected, partial load was allowed and full load was started following bone flap hypertrophy. In all lower and upper extremity reconstructions, physiotherapy was individually regulated according to structural stability.

Follow-up

Follow-up controls were performed at postoperative 1, 2, 3, 6, and 12 months and after this period at 6-month intervals for radiographic and clinical evaluations. The mean follow-up period was 25.15 months (range 12–60 months). The union of the bone flap with the main bone, thickening of the bone flap, and allograft-bone flap integration in allograft used cases was evaluated by conventional radiography.

Functional evaluation was performed by the Musculoskeletal Tumor Society (MSTS) score system, which included movement, pain, stability, deformity, strength, functional activities, and emotional acceptance parameters.

Statistical evaluation

The data obtained from the research results were evaluated in SPSS (13.0) package program (SPSS version 13.0 for Windows Student Version. Inc. SPSS. ©2005). Some research data are shown in tables containing absolute and percentage values, and arithmetic means (X + Sx) are taken where necessary. Pearson correlation test was used for statistical analysis.


  Results Top


Significant union was observed in 92.3% (12/13 patients) of the patients at the 6th-month radiological controls [Figure 3]a and [Figure 3]b. However, only 15.4% of the patients (2/13 patients) had thickening of the bone flap. At the 12th-month radiological controls, union and thickening of the bone flap were observed in all patients [Figure 4]a and [Figure 4]b. According to MSTS extremity function evaluation system, mean MSTS scores were measured as 77.58% (range 46.66–100.00) at 12 months [Table 1] and [Table 2].
Figure 3: (a) Postoperative X-ray of the reconstruction. (b) 6th-month union in X-ray

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Figure 4: (a)EarlypostoperativeX-ray of the reconstruction. (b) 12th-month-thickened fibular graft

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Table 1: Frequency distribution - qualitative data

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Table 2: Descriptive statistics - quantitative data

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When resection amounts and MSTS extremity function scores were compared; a statistically significant decrease was observed in MSTS scores as the amount of resection increased (r: −0.610, P= 0.027). When the free fibular flap size and MSTS limb function scores were compared, the relative decrease in MSTS scores was observed as the bone flap size increased (r: −0.235, P= 0.440). When the relationship between free fibular flap size and thickening of the bone flap at 6 months was examined, relatively higher bone flap size was measured in patients who did not develop thickening at 6 months (P = 0.069). There was a relatively longer operation time in patients who did not develop thickening at the 6th month (P = 0.100). When the operation time and MSTS extremity function scores were compared, the relative decrease in MSTS scores was observed with increasing operation time (r: −0.530, P= 0.062) [Table 2]. In the evaluation of the cases reconstructed with free fibular flap and allograft combination after the resection of the lower extremity tumor (7/9 patients), relatively higher MSTS limb function scores were observed than the cases using only the fibula bone flap for reconstruction (2/9 patients)(P = 0.621).

None of the patients had early or late complications except a nondisplaced fracture at postoperative 9th month (conservatively observed), an implant failure (plate revised), and a hematoma development (drained under general anesthesia) One patient with osteosarcoma developed local recurrence in the 2nd postoperative year; reresection, endoprosthetic reconstruction, and adjuvant chemotherapy were performed, but the patient died due to lung metastases at the end of the 3rd postoperative year. All of the remaining patients are still nonmetastatic.


  Discussion Top


The aim of bone tumor surgery is to maximize the cosmetic and functional outcomes of the patient and resection of the tumor using the most appropriate method without compromising the long-term survival of the patient. The main surgical methods are limb salvage surgery and amputation with wide surgical margins.

Limb salvage surgery can be presented as an alternative method if local tumor control of the primary tumor can be achieved by preserving the neurovascular function of the extremity. Numerous studies have shown no difference between long-term survival in patients treated with limb salvage surgery or amputation, if extensive surgical margins are achieved.[8]

In cases where limb salvage surgery is an option, it is difficult to choose between amputation and limb salvage surgery. In many cases, limb salvage surgery has a marked cosmetic advantage and offers gradual increased functional results, reducing the need for external prosthesis, and associated complications. However, this method is technically difficult to perform and has higher rates of complications such as infection, nonunion, fracture, prosthetic loosening, and local recurrence.[9]

In addition to the fact that there is no difference between survivals, on the basis of local recurrence of osteosarcoma is associated with poor prognosis.[10] There is a concern that there might be higher local recurrence rates in limb salvage surgery. However, in many studies, it has been agreed that extremity-conserving interventions have equal disease-free survival rates with amputation.[11],[12],[13],[14],[15] Again, in many studies, there was no significant difference between limb salvage surgery and amputation in terms of incidence of local relapse between 1% and 11%.[11],[12],[13] In these studies, precursors of local recurrence have been reported as surgical margins and tumor response to chemotherapy (necrosis).

Overall, the availability of advanced imaging techniques and improvement of surgical margins due to adjuvant chemotherapy have made limb salvage surgery as an accepted method of local control.

Endoprosthetic reconstruction gives good functional results with early stability, mobilization, emotional acceptance, and rapid restoration of function due to the advantage of early weight-bearing. However, problems such as infection, mechanical insufficiency, and aseptic loosening limit the long-term survival of the prosthesis, especially in patients with continuing skeletal development.[11],[12],[13]

Despite the improvements in long-term prosthesis results as a result of the development of designs and materials,[16] the risk of revision increases over time. In 2007, Myers reported the risk of revision surgery in the distal femurs regardless from the prosthesis as 50%, in the fixed hinged prosthesis as approximately 75%, and in the hinged prosthesis capable of rotation in the proximal tibia as 30%.[17],[18]

Extensible endoprosthesis in the treatment of bone tumors in patients with incomplete skeletal development may assist in achieving leg length equality. However, high rates of secondary operations and complications associated with this type of prosthesis limit its popularity.[19]

An ideal reconstruction should be similar to human biology, resistant to infection, strong, and mechanically resistant.[20],[21] Intercalary reconstruction in bone metaphysodiaphyseal regions is possible with massive allografts, free fibular flaps alone or free fibular flaps combined with massive bone allografts, or bone transport by Ilizarov method.[7],[22],[23]

A massive allograft can be used as an osteoarticular and intercalated support and can be combined with an endoprosthesis. Union of the allograft may take up to 24 months; nonunion up to 20%[24],[25],[26] and infection rates as high as 20%[26],[27] have been reported. The incidence of fracture is 15%–45% depending on fracture definition.[28] Another problem with osteoarticular allografts is joint degeneration. The use of osteoarticular allografts may be only a temporary solution in the surgery of malignant bone tumors, according to some authors, due to high complication rates and revision surgery rates.[24]

Bone transport with the Ilizarov technique is a more suitable option for small bone defects (<10 cm), whereas in large metaphysodiaphyseal defects, it is not an appropriate choice. In addition, the need for more time and patient cooperation for the outcome are factors that limit the use.[29]

Since it was first described for traumatic bone defects in the mid-1970s, free fibular flap has been of increasing popularity for reconstruction of defects following resection of bone tumors. The use of fibula is associated with the many advantages it provides. Fibula is a longitudinal cortical bone that can be used in limb reconstructions.[30] They can be up to 30 cm in length. At the same time, the dissection of the fibula is simple, and it can allow two separate surgical teams to work simultaneously. The growth plate of the fibula may also be included in the reconstruction site if necessary. Epiphyseal joint cartilage can be used, especially in reconstruction of the humerus and femur.[31] It has the capacity of remodeling and hypertrophy due to union and mechanical stress to the reconstructed bone.[32] In addition, it is stated in the literature that it has resistance to infection, radiotherapy, and chemotherapy.[33]

Free fibular flaps used in reconstruction provided union in the vast majority of cases, especially in the upper extremity.[34],[35],[36] However, it is thinner and weaker than femur and tibia. To perform a functional fibula replacement, a long load-free period is required. Even if bone union is achieved in the majority of cases, the fracture rate of this fibula is >30%–50%. It is possible to reduce the incidence of nonunion and bone flap fractures using a combination of free fibular flap and massive allograft.[37],[38]

The conventional reconstruction of the tumor resections with allografts and local tissue flaps has resulted in significant morbidity. The wide range of complications due to allograft failure included high rates of nonunion, infection, and fracture.[39] Autologous nonvascularized fibular grafting is another option for reconstruction of bone defects in long bones. However, there is also a debate on the autologous fibula graft to be vascularized or not. Although there is no significant difference between MSTS scores, free fibular flap usage for long-bone defect reconstructions is shown to be four times more likely to achieve union compared to nonvascularized fibula grafting.[40] Moore et al. recommended the use of nonvascularized fibula in <6 cm defects which led the surgeons to use FFF in reconstructions of larger bone defects.[41]

In our study results, when resection amounts and MSTS extremity function scores were compared, there was a statistically significant decrease in MSTS scores as the resection amount increased, which led to the conclusion that the operation technique could be guided according to the defect size. Accordingly, although a clear figure cannot be given, reconstruction with Capanna technique increases the chance of functional, oncologic, and radiological successes, especially in large metaphysodiaphyseal defects in the lower extremities.

Satisfactory oncological and functional results have been obtained, especially in reconstructions performed by Capanna method. When the defect following tumor resection in the lower extremity was reconstructed with free fibular flap and allograft combination (7/9 patients), it had a higher MSTS limb function score than the patients reconstructed with fibula bone flap alone (2/9 patients).

In the 6th month radiological controls, significant union was observed in 92.3%, and thickening of the bone flap was observed in 15.4%, which was consistent with the literature. Since bone flap thickening started after a significant increase in mechanical loading, only 12 months of radiological examination showed thickening of the bone flap. In addition, when the size of the free fibular flap placed at the defect site and the thickening of the bone flap at 6 months was compared, a relatively higher bone flap size was observed in cases where no thickening was observed at 6 months. In a study with a higher number of samples, it will be possible to reach significant results.


  Conclusions Top


In the present study, a number of subanalyzes of various factors affecting functional outcome were performed. The division of the groups by region, technique, tumor type, and the small number of patients included in the study led to a relatively low number of patients in some groups. The risk of Type 1 and Type 2 errors is increased accordingly. To reduce this risk, the results have been interpreted comparatively with the literature. On the other hand, the present study demonstrated the importance of measuring functional outcomes for further studies.

Although the study is a retrospective and noncontrol group, it may affect the level of evidence; the success of radiological, functional, and oncologic results is promising for future studies when compared with the current series. In conclusion, reconstruction of massive bone defects following tumor resection with free fibular flap is a method that improves the quality of life without adversely affecting tumor-related prognosis.

Acknowledgement

This article is based on the residency thesis of Onur Basci MD, in Marmara University School of Medicine, Depr. Orthopaedics and Traumatlogy, 2011.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Simon MA, Aschliman MA, Thomas N, Mankin HJ. Limb-salvage treatment versus amputation for osteosarcoma of the distal end of the femur 1986. J Bone Joint Surg Am 2005;87:2822.  Back to cited text no. 1
    
2.
Henshaw R, Malawer M. Review of endoprostehetic surgery in limb-sparing surgery. In Musculoskeletal Cancer Surgery: Treament of Sarcoma and Allied Diseases, Malawer, Martin M, Sugarbaker, Paul H. (eds.) Springer Netherlands, 2001. p. 383-403.  Back to cited text no. 2
    
3.
Yoshida Y, Osaka S, Tokuhashi Y. Analysis of limb function after various reconstruction methods according to tumor location following resection of pediatric malignant bone tumors. World J Surg Oncol 2010;8:39.  Back to cited text no. 3
    
4.
Brown KL. Limb reconstruction with vascularized fibular grafts after bone tumor resection. Clin Orthop Relat Res 1991;262:64-73.  Back to cited text no. 4
    
5.
Gebhardt MC, Flugstad DI, Springfield DS, Mankin HJ. The use of bone allografts for limb salvage in high-grade extremity osteosarcoma. Clin Orthop Relat Res 1991;270:181-96.  Back to cited text no. 5
    
6.
Ceruso M, Falcone C, Innocenti M, Delcroix L, Capanna R, Manfrini M. Skeletal reconstruction with a free vascularized fibula graft associated to bone allograft after resection of malignant bone tumor of limbs. Handchir Mikrochir Plast Chir 2001;33:277-82.  Back to cited text no. 6
    
7.
Capanna R, Buffalini C, Campanacci M. A new technique for reconstructions of large metadiaphyseal bone defects: A combined graft (Allograft shell plus vascularized fibula). Orthop Traumatol 1993;2:159-77.  Back to cited text no. 7
    
8.
Rodriguez RP. Amputation surgery and prostheses. Orthop Clin North Am 1996;27:525-39.  Back to cited text no. 8
    
9.
Refaat Y, Gunnoe J, Hornicek FJ, Mankin HJ. Comparison of quality of life after amputation or limb salvage. Clin Orthop Relat Res 2002;397:298-305.  Back to cited text no. 9
    
10.
Bacci G, Ferrari S, Mercuri M, Bertoni F, Picci P, Manfrini M, et al. Predictive factors for local recurrence in osteosarcoma: 540 patients with extremity tumors followed for minimum 2.5 years after neoadjuvant chemotherapy. Acta Orthop Scand 1998;69:230-6.  Back to cited text no. 10
    
11.
Bacci G, Picci P, Ferrari S, Ruggieri P, Casadei R, Tienghi A, et al. Primary chemotherapy and delayed surgery for nonmetastatic osteosarcoma of the extremities. Results in 164 patients preoperatively treated with high doses of methotrexate followed by cisplatin and doxorubicin. Cancer 1993;72:3227-38.  Back to cited text no. 11
    
12.
Petrilli AS, Gentil FC, Epelman S, Lopes LF, Bianchi A, Lopes A, et al. Increased survival, limb preservation, and prognostic factors for osteosarcoma. Cancer 1991;68:733-7.  Back to cited text no. 12
    
13.
Ruggieri P, De Cristofaro R, Picci P, Bacci G, Biagini R, Casadei R, et al. Complications and surgical indications in 144 cases of nonmetastatic osteosarcoma of the extremities treated with neoadjuvant chemotherapy. Clin Orthop Relat Res 1993;295:226-38.  Back to cited text no. 13
    
14.
Simon MA, Aschliman MA, Thomas N, Mankin HJ. Limb-salvage treatment versus amputation for osteosarcoma of the distal end of the femur. J Bone Joint Surg Am 1986;68:1331-7.  Back to cited text no. 14
    
15.
Bacci G, Ferrari S, Bertoni F, Rimondini S, Longhi A, Bacchini P, et al. Prognostic factors in nonmetastatic Ewing's sarcoma of bone treated with adjuvant chemotherapy: Analysis of 359 patients at the Istituto Ortopedico Rizzoli. J Clin Oncol 2000;18:4-11.  Back to cited text no. 15
    
16.
Ahlmann ER, Menendez LR, 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;88:790-5.  Back to cited text no. 16
    
17.
Myers GJ, Abudu AT, Carter SR, Tillman RM, Grimer RJ. The long-term results of endoprosthetic replacement of the proximal tibia for bone tumours. J Bone Joint Surg Br 2007;89:1632-7.  Back to cited text no. 17
    
18.
Myers GJ, Abudu AT, Carter SR, Tillman RM, Grimer RJ. Endoprosthetic replacement of the distal femur for bone tumours: Long-term results. J Bone Joint Surg Br 2007;89:521-6.  Back to cited text no. 18
    
19.
Eckardt JJ, Kabo JM, Kelley CM, Ward WG Sr., Asavamongkolkul A, Wirganowicz PZ, et al. Expandable endoprosthesis reconstruction in skeletally immature patients with tumors. Clin Orthop Relat Res 2000;373:51-61.  Back to cited text no. 19
    
20.
Plötz W, Rechl H, Burgkart R, Messmer C, Schelter R, Hipp E, et al. Limb salvage with tumor endoprostheses for malignant tumors of the knee. Clin Orthop Relat Res 2002;405:207-15.  Back to cited text no. 20
    
21.
Biau D, Faure F, Katsahian S, Jeanrot C, Tomeno B, Anract P. Survival of total knee replacement with a megaprosthesis after bone tumor resection. J Bone Joint Surg Am 2006;88:1285-93.  Back to cited text no. 21
    
22.
Muscolo DL, Ayerza MA, Aponte-Tinao LA, Ranalletta M. Partial epiphyseal preservation and intercalary allograft reconstruction in high-grade metaphyseal osteosarcoma of the knee. J Bone Joint Surg Am 2004;86:2686-93.  Back to cited text no. 22
    
23.
Tsuchiya H, Tomita K, Minematsu K, Mori Y, Asada N, Kitano S. Limb salvage using distraction osteogenesis. A classification of the technique. J Bone Joint Surg Br 1997;79:403-11.  Back to cited text no. 23
    
24.
Rödl RW, Ozaki T, Hoffmann C, Böttner F, Lindner N, Winkelmann W. Osteoarticular allograft in surgery for high-grade malignant tumours of bone. J Bone Joint Surg Br 2000;82:1006-10.  Back to cited text no. 24
    
25.
Aho AJ, Ekfors T, Dean PB, Aro HT, Ahonen A, Nikkanen V. Incorporation and clinical results of large allografts of the extremities and pelvis. Clin Orthop Relat Res 1994;307:200-13.  Back to cited text no. 25
    
26.
Ortiz-Cruz E, Gebhardt MC, Jennings LC, Springfield DS, Mankin HJ. The results of transplantation of intercalary allografts after resection of tumors. A long-term follow-up study. J Bone Joint Surg Am 1997;79:97-106.  Back to cited text no. 26
    
27.
Hornicek FJ Jr., Mnaymneh W, Lackman RD, Exner GU, Malinin TI. Limb salvage with osteoarticular allografts after resection of proximal tibia bone tumors. Clin Orthop Relat Res 1998;352:179-86.  Back to cited text no. 27
    
28.
Thompson RC Jr., Garg A, Clohisy DR, Cheng EY. Fractures in large-segment allografts. Clin Orthop Relat Res 2000;370:227-35.  Back to cited text no. 28
    
29.
Campanacci DA, Capanna R, Ceruso M. Indicationsfor combined grafts (allografts “vascularized fibula) after intercalary resections for bone tumor. In: Czitrom Andrei A, Winkler Heinz, (eds). Orthopaedic Allograft Surgery. Vienna: Springer-Verlag; 1996. p. 149.  Back to cited text no. 29
    
30.
Taylor GI, Miller GD, Ham FJ. The free vascularized bone graft. A clinical extension of microvascular techniques. Plast Reconstr Surg 1975;55:533-44.  Back to cited text no. 30
    
31.
Organek AJ, Klebuc MJ, Zuker RM. Indications and outcomes of free tissue transfer to the lower extremity in children: Review. J Reconstr Microsurg 2006;22:173-81.  Back to cited text no. 31
    
32.
de Boer HH, Wood MB. Bone changes in the vascularised fibular graft. J Bone Joint Surg Br 1989;71:374-8.  Back to cited text no. 32
    
33.
Canosa R, González del Pino J. Effect of methotrexate in the biology of free vascularized bone grafts. A comparative experimental study in the dog. Clin Orthop Relat Res 1994;301:291-301.  Back to cited text no. 33
    
34.
Weiland AJ, Kleinert HE, Kutz JE, Daniel RK. Free vascularized bone grafts in surgery of the upper extremity. J Hand Surg Am 1979;4:129-44.  Back to cited text no. 34
    
35.
Gerwin M, Weiland AJ. Vascularized bone grafts to the upper extremity. Indications and technique. Hand Clin 1992;8:509-23.  Back to cited text no. 35
    
36.
Yajima H, Tamai S, Ono H, Kizaki K. Vascularized bone grafts to the upper extremities. Plast Reconstr Surg 1998;101:727-35.  Back to cited text no. 36
    
37.
Zaretski A, Amir A, Meller I, Leshem D, Kollender Y, Barnea Y, et al. Free fibula long bone reconstruction in orthopedic oncology: A surgical algorithm for reconstructive options. Plast Reconstr Surg 2004;113:1989-2000.  Back to cited text no. 37
    
38.
Bernd L, Sabo D, Zahlten-Hinguranage A, Niemeyer P, Daecke W, Simank HG. Experiences with vascular pedicled fibula in reconstruction of osseous defects in primary malignant bone tumors. Orthopade 2003;32:983-93.  Back to cited text no. 38
    
39.
Chen CM, Disa JJ, Lee HY, Mehrara BJ, Hu QY, Nathan S, et al. Reconstruction of extremity long bone defects after sarcoma resection with vascularized fibula flaps: A 10-year review. Plast Reconstr Surg 2007;119:915-24.  Back to cited text no. 39
    
40.
Estrella EP, Wang EH. A comparison of vascularized free fibular flaps and nonvascularized fibular grafts for reconstruction of long bone defects after tumor resection. J Reconstr Microsurg 2017;33:194-205.  Back to cited text no. 40
    
41.
Moore JR, Weiland AJ, Daniel RK. Use of free vascularized bone grafts in the treatment of bone tumors. Clin Orthop Relat Res 1983;175:37-44.  Back to cited text no. 41
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
    Tables

  [Table 1], [Table 2]



 

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Abstract
Introduction
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