From 1982 to 1991, 19 patients at Nara Medical University, Kashihara, Japan, underwent resection of aggressive benign and malignant bone tumors, with limb salvage and reconstruction by free vascularized fibula grafts. The patients were followed up for an average of 54 months. The reconstructed site was the jaw in 6 cases, upper extremity in 3, spine in 1, pelvis in 2, and lower extremity in 7. Six patients had aggressive benign lesions, and 13 had malignant lesions. The sizes of the resultant bone defect ranged from 6 to 20 cm, and the lengths of fibula used ranged from 8 to 24 cm. The average time to union was 4.1 months (2-9 months) in the extremities and pelvis. Local recurrence was observed in 3 cases, for whom vascularized fibula grafts were performed for recurrent tumors. In cases of primary untreated tumors, no recurrences occurred. Therefore, this procedure should be performed at the time of primary operation after extensive resection of an aggressive benign or malignant bone tumor. o 1992 wiley-Liss, Inc. MICROSURGERY 13:227-233
1992
VASCULARIZED FIBULA GRAFT FOR RECONSTRUCTION AFTER RESECTION OF AGGRESSIVE BENIGN AND MALIGNANT BONE TUMORS HlROSHl YAJIMA, M.D., SUSUMU TAMAI, M.D., SHIGERU MIZUMOTO, M.D., MASAHITO SUGIMURA, M.D., and KATSUHIRO HORIUCHI, M.D.
In recent years, the introduction of chemotherapies, represented by intraarterial administration of Adriamycine and high-dose of methotrexate therapy, has made it possible to reduce primary lesions of malignant bone tumors and to suppress their metastasis. In addition, advances in diagnostic imaging (e.g., CT and MRJ) have facilitated accurate assessment of the extent of malignant bone tumors. In 1980, Enneking et al.' proposed a surgical staging system, which presented clear criteria for determining the indications for limb-sparing surgery, and stimulated attempts at limb salvage at many institutions. Thereafter, limb-sparing surgery for malignant bone tumors in the extremities has been widely attempted. The segmental bony defect has been reconstructed using prosthetic replacements, allografts, and autogenous bone grafting. Of these, prosthetic replacement has been most commonly used, although numerous associated problems have been noted (e.g., durability and postoperative infection). On the other hand, recent advances in microsurgical techniques have made it possible to transfer various kinds of
From the Departments of Orthopaedic Surgery (H.Y., S.T., S.M.), and Oral Surgery (M.S., K.H.), Nara Medical University, Kashihara, Japan. Address reprint requests to Dr. Hiroshi Yajima. Department of Otihopaedic Surgery. Nara Medical University, Kashihara, Nara. 634 Japan. Presented at the Eleventh Congress of the International Microsurgical Society, Rhodes, Greece, June 21-26, 1992. Received for publication June 15, 1992. 0 1992 Wiley-Liss, Inc.
autogenous composite tissues and to apply vascularized bone grafts to patients with long bone defects. In 1975, Taylor et aL2 first reported free vascularized fibula grafting for the patient with a large tibia1 defect. This technique has been primarily used for reconstruction after resection of malignant and aggressive benign bone tumors of the extremities, because of its own linear form. In addition, vascularized fibula grafting has been applied to the reconstruction of the mandible, using an osteotomizing technique. In the present study, we analyzed 19 cases of free vascularized fibula grafting for reconstruction after surgical resection of bone tumors to examine the indications and clinical significance of this procedure. MATERIALS AND METHODS
From July 1982 to June 1992 in our clinic, vascularized fibula grafting was performed in 20 patients with malignant or aggressive benign bone tumors. Nineteen of these patients who were followed up for over 6 months were analyzed (Table l). Ten patients were men and 9 were women, with ages at operation ranging from 13 to 80 years (mean: 39.4 years). They were followed up for an average of 4 years and 6 months (ranging from 6 months to 9 years 10 months). The reconstructed sites were the jaw in 6 cases, the upper extremity in 3, the spine in 1, the pelvis in 2, and the lower extremity in 7. Six patients had aggressive benign lesions, 13 had malignant lesions: there were giant cell tumors in 6
228
Yajima et al.
cases, squamous cell carcinoma in 5 , adamantinoma in 3, chondrosarcoma in 2, Ewing’s sarcoma in 1, parosteal osteosarcoma in 1, and malignant fibrous histiocytoma in 1. When the 19 cases were classified according to Enneking’s surgical staging system,’ 2 cases were stage IA, 9 were stage IB, and 8 were stage IIB. Marginal excision was performed for Ewing’s sarcoma affecting the iliac bone. Intralesional excision was undertaken for a giant cell tumor of the thoracic vertebrae. Wide excision was performed for the other 17 tumors. Reconstruction with vascularized fibula grafting was carried out in 13 cases with primary untreated tumors, and 5 cases with recurrent tumors. In one case, it was applied to replace an existing implant with a vascularized fibula graft. The lengths of the bone defects after tumor resection ranged from 6 to 20 cm (mean: 12 cm). The lengths of fibular grafts ranged from 8 to 24 cm. In one case (case l ) , dual vascularized fibulae were grafted. In 3 cases (cases 15, 16 and 19), a twin-barrel fibula graft on a single vascular pedicle was grafted. In 4 cases (cases 7, 8, 17 and 18) that underwent reconstruction of the mandibula, the fibula was cut into pieces and then reformed to fit the shape of the defect. Simultaneous reconstructions of bone and soft tissue defects were accomplished by grafting of a fibular osteocutaneous flap (6 X 4 cm-24 x 12 cm) in 8 patients. A buoy flap for vascular monitoring of the fibular graft was attached to the fibula in 5 patients. RESULTS
In one case, the flap showed color change after operation, necessitating reexploration. This case had venous thrombosis, and received thrombectomy followed by vein grafting. Including this case, the flap survived in all cases. Primary bony union occurred in 16 of 19 cases (84%). Four cases underwent an additional iliac bone grafting after the vascularized fibula grafting, 3 cases due to delayed union and 1 case due to stress fracture. The mean periods required to obtain radiographical bony union in 12 cases after reconstruction of the extremities or the pelvis ranged from 2 to 9 months (mean: 4.1 months). In cases that underwent reconstruction of the spine or mandibule, accurate assessment of the timing of complete bone union was difficult on plain roentgenograms. In all of these cases, however, bone union of the grafts was confirmed by CT or tomography. Fracture of the grafted fibula occurred in 4 cases, of whom 1 received an additional bone grafting, 1 underwent an additional external skeletal fixation, and 2 required cast immobilization. Bone union was achieved in all 4 cases. Local tumor recurrence was seen in 3 cases, of whom 2 required amputation (Cases 1 and 2) and one (Case 6: recurrence in the thoracic vertebrae) underwent curettage and bone grafting. In all of these 3 cases, vascularized fibula grafting had been performed for reconstruction after surgical treatment of the recurrent tumor. Local tumor recurrence has occurred in none of the cases undergoing vascularized fibula grafting
for the primary untreated tumor. One patient (Case 15) died of lung metastasis 11 months after operation without local recurrence. CASE REPORT Case 14 A 55-year-old man developed squamous cell carcinoma
after chronic osteomyelitis of 25 years. In May 1989, the anterior aspect of the left leg developed redness, swelling and pain surrounding the fistula. At that time, the patient received conservative treatment at a nearby clinic. However, the symptoms worsened and the granulation increased in size. The patient was consequently referred to our hospital in July. On the first examination, the patient showed a cauliflower-like growth of granulation in the anterior aspect of the left leg with bloody secretion (Fig. 1A). Roentgenography revealed an irregular bone absorption in the center of the tibia (Fig. 1B). CT revealed extensive destruction of the tibia. The patient was admitted to our hospital and the biopsy finding revealed the typical signs of well-differentiated squamous cell carcinoma. Based on these findings, the patient was diagnosed as having squamous cell carcinoma that had developed from the fistula associated with chronic osteomyelitis. The cancer stage was T,No according to the international classification. In August 1989, the 18 cm tibia including the cancer tissue with the anterior compartment was resected, followed by transplantation of a 23 cm fibula with a 24 x 12 cm flap, which was harvested from the contralateral leg (Fig. 1C). The peroneal artery of the graft was anastomosed to the peroneal artery of the recipient site at the proximal leg, and the venae comitantes of the graft were anastomosed to the venae comitantes of the recipient peroneal artery. The distal end of the peroneal artery was anastomosed to the distal stump of the anterior tibia1 artery at a point near the ankle joint in order to maintain the circulation of the foot. Since bone union in the proximal region was delayed at 5 months, an additional iliac bone graft was performed, followed by external skeletal fixation. Although fracture of the grafted fibula occurred 14 months postoperatively, bone union was achieved after two months of cast immobilization. A functional brace was used in the subsequent six months. At present, two years and nine months postoperatively, the grafted fibula shows hypertrophy, and no tumor recurrence has occurred (Fig. 1D). DISCUSSION
Vascularized fibula grafting has been used to treat intractable diseases such as traumatic bone defect, osteomyelitis, uncurable nonunion, and congenital pseudoarthrosis. In such cases, this technique has yielded excellent results. Since increasing attempts have been made to salvage limbs affected with malignant bone tumors following advances in
Vascularized Fibula Graft
229
Figure 1. Case 14: A 55-year-old man with squamous cell cardnoma of left lower leg. A: Preoperative photograph of the anterior aspect of the left leg showing a cauliflower-likegrowth of granulation. B: Preoperative lateral radiograph of the left tibia showing irregular
bone absorption. C: Vascularizedfibula with a 24 x 12 cm flap was transferred to reconstruct the defect after tumor resection. 0: Anterior-posterior radiograph at 2 years and 9 months postoperatively demonstrating perfect union without tumor recurrence.
chemotherapy and radiotherapy, vascularized fibula grafting has been receiving more attention as a means of reconstructi~n.~-~ Formerly, these defects had been commonly reconstructed by autogenous and homogeneous bone grafting, or prosthetic replacement. When nonvascularized
bone, autogenous or homogenous, is grafted, however, the time required for bone union is significantly long especially if the graft is more than 7 cm long. According to Enneking et al. ,9 the incidence of nonunion was 32% after grafting a nonvascularized bone of 7.5-25 cm in length. With vascu-
230
Yajirna et al.
Figure 2. Case 15: A 13-year-oldgirl with Ewing’s sarcoma of the right iliac bone. A: Preoperative angiography showing pooling of the contrast media consistent with the tumor. 6:Anterior-posterior radiograph at 4 months after twin barrel vascularized fibula (star) and
nonvascularized fibula (asterisk) grafting. Bone union of the vascularized fibula grafts was completed, while that of the nonvascularized fibula graft was delayed.
larized fibula grafting, which involves grafting a viable bone while preserving its blood flow, more rapid bone union can be obtained irrespective of the length of the graft. When we used this technique for reconstruction of the ex-
tremities and pelvis after resection of bone tumors, the mean time until completion of bone union was as short as 4.1 months even though the size of the bone defects was large (6-20 cm; mean, 12 cm). Figure 2B shows a radio-
231
Vascularized Fibula Graft Table 1. Summary of Cases Treated.
Case 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19
Age (yrs) 27 63 68 27 68 29 80 18 55 25 26 44 44 55 13 19 14
53 21
Recipient site Femur Tibia Tibia Radius Mandibula Spine Mandibula Mandibula Mandibula Femur Radius Femur Radius Tibia Pelvis Femur Mandibula Mandibula Pelvis
Tumor Giant cell tumor (R)b
M.F.H.C (R) Adamantinoma Giant cell tumor Squamous cell carcinoma Giant cell tumor (R) Squamous cell carcinoma Adamantinoma Squarnous cell carcinoma Parosteal osteosarcoma (R) Giant cell tumor Chondrosarcorna Giant cell tumor (R) Squamous cell carcinoma Ewing's sarcoma Giant cell tumor Adamantinoma Squamous cell carcinoma Chondrosarcoma
Surgical stagea
Bone defect
Follow
IB IIB IB IA I1B IB IIB IA I1 B IB IB IB IB IIB II B IB IB IIB II B
17(cm) 18 20 6 8 9 10 14 8 10 18 14 9 18
9y. 10m. 9y. 6m. 8;. IIm. 7y. 11m. 6y. 5m. 6y. 3rn. 5y. 5m. 4y. 11m. 4y. 7rn. 4y. 7m. 2y. 2m. 3y. 3m. 2y. I l m . 2y. 9m. llrn. 2y. 2m. ly. 6m. 8m. 6rn.
11
10 12 14 12
UP
Fibula fracture
+
Additional bone graft -
Local recurrence
-
+
+ +
-
-
-
'Surgical Staging System of Enneking. b(R), recurrent tumor. 'M.F.H.,malignant fibrous histiocytoma.
graph of the pelvis in a 13-year-old girl in whom a twin barrel vascularized fibula and a nonvascularized fibula were grafted for the reconstruction of a pelvic defect after resection of an Ewing's sarcoma. Complete bone unions are visible at the vascularized fibula grafts, while bone union is not achieved at the nonvascularized fibula graft. These results clearly demonstrate the usefulness of vascularized fibula grafting. Furthermore, since it is richly vascularized, it is highly resistant to infection and hence enhances the safety of chemotherapy after grafting. Although some investigators have reported that postoperative chemotherapy affects bone only one of our cases showed delayed bone union attributable to chemotherapy after grafting. Although infection is likely to occur after reconstruction of the mandible with conventional methods, none of our cases showed infection after jaw reconstruction. The greatest advantage of vascularized fibula grafting seems to lie in the feasibility of one-stage reconstruction for various tissues. The use of the peroneal artery as a vascular pedicle makes it possible to obtain a flap, nerves, and muscles, together with the fibula. For this reason, this technique is particularly superior to the conventional techniques in cases of malignant bone tumor where a wide soft tissue defect is created by tumor resection (Fig. 1C). Another advantage of this technique is hypertrophy of the fibula after grafting. This is a very interesting feature of this surgery. We think that this phenomenon occurs because the grafted fibula is alive." The hypertrophy of the grafted fibula develops more rapidly the younger the patient. However, even at the relatively advanced age of 63 years (Case 3), the
grafted fibula showed an increase in width to a level comparable to the width of the original fibula (Fig. 3B). This phenomenon was prompted by stress fractures. In the present study, 4 cases showed fracture of the grafted fibula. In 3 of these 4 cases, bone union was completed rapidly, and the grafted bone showed marked hypertrophy after completion of union. The greatest problem associated with this technique is that it is much more complex than the conventional techniques, thus requiring more time and causing more blood loss and surgical stress. Since most patients for whom this technique is indicated have malignant tumors, it is important to avoid putting too much emphasis on limb salvage, so as not to increase the incidence of fatal metastasis. This technique also has problems pertaining to the donor site and postoperative monitoring. However, these problems are negligible in view of the great advantages provided. Vascularized fibula grafting for reconstruction of bone defects after tumor resection is indicated in the following cases: (1) cases in which the bone defect is larger than 7 cm, (2) cases accompanied by extensive soft tissue defects, (3) cases requiring reconstruction of the distal end of the radius, and (4) cases having undergone multiple operations previously even if the recurrent defect is small. Enneking's stage IA, IB, and IIA cases are good indications for this technique. Tomita' reported that stage IIB cases are not indicated for this technique. According to Saito et al.,* who applied this technique to 4 cases of stage IIB, one case died while the remaining 3 cases had an excellent, recurrencefree postoperative course. Our stage IIB cases responded
232
Yajima et al.
Figure 3. Case 3: A 68-year-old man with right tibial adamantinoma. A: A 24 cm vascularized fibula with peroneal flap was transferred for the reconstruction of the bone and soft tissue defect. 6:Anteriorposterior radiograph at 8 years and 1 1 months postoperatively showing marked hypertrophy of the grafted fibula.
poorly to this technique. Therefore, the use of this technique in Stage IIB cases requires a careful approach. In this study, 3 cases developed local recurrence. In all these cases, vascularized fibula grafting was used after resection of recurrent tumor. Therefore, the indications for this technique in reconstruction after resection of recurrent tumors need to be reviewed. In cases where this technique was used for reconstruction after the first resection of tumor, the results were excellent. These results suggest that wide excision should be performed during the first operation and that, additionally, this technique of reconstruction be used during the same operation. Of course, this technique of reconstruction is not indicated in cases complicated by remote metastasis. Such cases require amputation or prosthetic replacement. In cases where the tumor is located in the vicinity of the knee joint, the selection of this technique (for arthrodesis) or prosthetic replacement should be determined based on age, gender, occupation of the patient and other factors. In view of the short life, the susceptibility to infection, and other problems of the currently available artificial joints, arthrodesis with this technique seems to be preferable if the patient is young. Since the maximum length of fibula that can be donated is 24-26 cm, the extent of reconstruction possible with this technique is limited. However, even when the length of fibula that can be obtained is not long enough to cover the defect, this technique can be used if the patient is young and limb lengthening can
be done later. In middle-aged or elderly patients, prosthetic replacement (bone and joint) should be adopted if the size of the fibula that can be donated is not large enough for reconstruction. Vascularized bone or joint allografting may be realized in the future.'*
REFERENCES 1. Enneking WF, Spanier SS, Goodman MA: A system for the surgical
staging of the muscloskeletal sarcoma. Clin Orrhop 153: 106-120, 1980. 2. Taylor GI, Miller GD, Ham FG: The free vascularized bone graft: A clinical extension of microvascular techniques. Plusr Reconsrr Surg 551533-544, 1975. 3. Moore JR, Weiland AJ, Daniel R K Use of free vascularized bone grafts in the treatment of bone tumors. Clin Orthop 175:37-44, 1983. 4. Usui M, lshii S, Yamamura M, Minami A, Sakuma T: Microsurgical reconstructive surgery following wide resection of bone and soft tissue sarcomas in the upper extremities. J Reconstr Surg 2:77-84, 1986. 5 . Gidumal R, Wood MB, Sim FH, Shives TC: Vascularized bone transfer for limb salvage and reconstruction after resection of aggressive bone tumor. J Reconstr Surg 3:183-188, 1987. 6 . Aberg M , Rydholm A, Holmberg J, Wieslander JB: Reconstruction with a free vascularized fibular graft for malignant bone tumor. A ( m Orthop Scund 59:430-437, 1988. 7. Tomita K: Vascularized bone grafts for limb salvage and reconstruction after resection of malignant bone tumors. Bessatsu Seikei Ceku 8:174-180, 1985 (in Japanese). 8. Saito H: Vascularized fibula grafts in limb sparing tumor surgery. Shujuru 42:289-298, 1988 (in Japanese). 9. Enneking WF, Eady JL, Burchardt H: Autogenous cortical bone grafts
-
Vascularized Fibula Graft in the reconstruction of segmental skeletal defects. J B o n e Joinr Surg 62A:1039-1058, 1980. 10. Friedelaender GE, Tross RB, Doganis AC, Kirkwood JM, Baron R: Effects of chemotherapeutic agent on bone: 1. Short-term methotrexate and doxorubicin (adriamycin) treatment in a rat model. J Bone Joint Surg 66A:602-607, 1984.
233
11. Mizumoto S, Tamai S, Yajima H, Yoshii T: Experimental study of vascularized tibio-fibula graft in inbred rats: A preliminary report. J Reconstr Microsurg 3: 1-9, 1986. 12. Randolph MA, Yaremchuk MJ, Moore JR, Robinson RA, Weiland AJ: Experimental vascularized bone allografting. Microsurgery 8: 210-217, 1980.
1992
VASCULARIZED FIBULA GRAFT FOR RECONSTRUCTION AFTER RESECTION OF AGGRESSIVE BENIGN AND MALIGNANT BONE TUMORS HlROSHl YAJIMA, M.D., SUSUMU TAMAI, M.D., SHIGERU MIZUMOTO, M.D., MASAHITO SUGIMURA, M.D., and KATSUHIRO HORIUCHI, M.D.
In recent years, the introduction of chemotherapies, represented by intraarterial administration of Adriamycine and high-dose of methotrexate therapy, has made it possible to reduce primary lesions of malignant bone tumors and to suppress their metastasis. In addition, advances in diagnostic imaging (e.g., CT and MRJ) have facilitated accurate assessment of the extent of malignant bone tumors. In 1980, Enneking et al.' proposed a surgical staging system, which presented clear criteria for determining the indications for limb-sparing surgery, and stimulated attempts at limb salvage at many institutions. Thereafter, limb-sparing surgery for malignant bone tumors in the extremities has been widely attempted. The segmental bony defect has been reconstructed using prosthetic replacements, allografts, and autogenous bone grafting. Of these, prosthetic replacement has been most commonly used, although numerous associated problems have been noted (e.g., durability and postoperative infection). On the other hand, recent advances in microsurgical techniques have made it possible to transfer various kinds of
From the Departments of Orthopaedic Surgery (H.Y., S.T., S.M.), and Oral Surgery (M.S., K.H.), Nara Medical University, Kashihara, Japan. Address reprint requests to Dr. Hiroshi Yajima. Department of Otihopaedic Surgery. Nara Medical University, Kashihara, Nara. 634 Japan. Presented at the Eleventh Congress of the International Microsurgical Society, Rhodes, Greece, June 21-26, 1992. Received for publication June 15, 1992. 0 1992 Wiley-Liss, Inc.
autogenous composite tissues and to apply vascularized bone grafts to patients with long bone defects. In 1975, Taylor et aL2 first reported free vascularized fibula grafting for the patient with a large tibia1 defect. This technique has been primarily used for reconstruction after resection of malignant and aggressive benign bone tumors of the extremities, because of its own linear form. In addition, vascularized fibula grafting has been applied to the reconstruction of the mandible, using an osteotomizing technique. In the present study, we analyzed 19 cases of free vascularized fibula grafting for reconstruction after surgical resection of bone tumors to examine the indications and clinical significance of this procedure. MATERIALS AND METHODS
From July 1982 to June 1992 in our clinic, vascularized fibula grafting was performed in 20 patients with malignant or aggressive benign bone tumors. Nineteen of these patients who were followed up for over 6 months were analyzed (Table l). Ten patients were men and 9 were women, with ages at operation ranging from 13 to 80 years (mean: 39.4 years). They were followed up for an average of 4 years and 6 months (ranging from 6 months to 9 years 10 months). The reconstructed sites were the jaw in 6 cases, the upper extremity in 3, the spine in 1, the pelvis in 2, and the lower extremity in 7. Six patients had aggressive benign lesions, 13 had malignant lesions: there were giant cell tumors in 6
228
Yajima et al.
cases, squamous cell carcinoma in 5 , adamantinoma in 3, chondrosarcoma in 2, Ewing’s sarcoma in 1, parosteal osteosarcoma in 1, and malignant fibrous histiocytoma in 1. When the 19 cases were classified according to Enneking’s surgical staging system,’ 2 cases were stage IA, 9 were stage IB, and 8 were stage IIB. Marginal excision was performed for Ewing’s sarcoma affecting the iliac bone. Intralesional excision was undertaken for a giant cell tumor of the thoracic vertebrae. Wide excision was performed for the other 17 tumors. Reconstruction with vascularized fibula grafting was carried out in 13 cases with primary untreated tumors, and 5 cases with recurrent tumors. In one case, it was applied to replace an existing implant with a vascularized fibula graft. The lengths of the bone defects after tumor resection ranged from 6 to 20 cm (mean: 12 cm). The lengths of fibular grafts ranged from 8 to 24 cm. In one case (case l ) , dual vascularized fibulae were grafted. In 3 cases (cases 15, 16 and 19), a twin-barrel fibula graft on a single vascular pedicle was grafted. In 4 cases (cases 7, 8, 17 and 18) that underwent reconstruction of the mandibula, the fibula was cut into pieces and then reformed to fit the shape of the defect. Simultaneous reconstructions of bone and soft tissue defects were accomplished by grafting of a fibular osteocutaneous flap (6 X 4 cm-24 x 12 cm) in 8 patients. A buoy flap for vascular monitoring of the fibular graft was attached to the fibula in 5 patients. RESULTS
In one case, the flap showed color change after operation, necessitating reexploration. This case had venous thrombosis, and received thrombectomy followed by vein grafting. Including this case, the flap survived in all cases. Primary bony union occurred in 16 of 19 cases (84%). Four cases underwent an additional iliac bone grafting after the vascularized fibula grafting, 3 cases due to delayed union and 1 case due to stress fracture. The mean periods required to obtain radiographical bony union in 12 cases after reconstruction of the extremities or the pelvis ranged from 2 to 9 months (mean: 4.1 months). In cases that underwent reconstruction of the spine or mandibule, accurate assessment of the timing of complete bone union was difficult on plain roentgenograms. In all of these cases, however, bone union of the grafts was confirmed by CT or tomography. Fracture of the grafted fibula occurred in 4 cases, of whom 1 received an additional bone grafting, 1 underwent an additional external skeletal fixation, and 2 required cast immobilization. Bone union was achieved in all 4 cases. Local tumor recurrence was seen in 3 cases, of whom 2 required amputation (Cases 1 and 2) and one (Case 6: recurrence in the thoracic vertebrae) underwent curettage and bone grafting. In all of these 3 cases, vascularized fibula grafting had been performed for reconstruction after surgical treatment of the recurrent tumor. Local tumor recurrence has occurred in none of the cases undergoing vascularized fibula grafting
for the primary untreated tumor. One patient (Case 15) died of lung metastasis 11 months after operation without local recurrence. CASE REPORT Case 14 A 55-year-old man developed squamous cell carcinoma
after chronic osteomyelitis of 25 years. In May 1989, the anterior aspect of the left leg developed redness, swelling and pain surrounding the fistula. At that time, the patient received conservative treatment at a nearby clinic. However, the symptoms worsened and the granulation increased in size. The patient was consequently referred to our hospital in July. On the first examination, the patient showed a cauliflower-like growth of granulation in the anterior aspect of the left leg with bloody secretion (Fig. 1A). Roentgenography revealed an irregular bone absorption in the center of the tibia (Fig. 1B). CT revealed extensive destruction of the tibia. The patient was admitted to our hospital and the biopsy finding revealed the typical signs of well-differentiated squamous cell carcinoma. Based on these findings, the patient was diagnosed as having squamous cell carcinoma that had developed from the fistula associated with chronic osteomyelitis. The cancer stage was T,No according to the international classification. In August 1989, the 18 cm tibia including the cancer tissue with the anterior compartment was resected, followed by transplantation of a 23 cm fibula with a 24 x 12 cm flap, which was harvested from the contralateral leg (Fig. 1C). The peroneal artery of the graft was anastomosed to the peroneal artery of the recipient site at the proximal leg, and the venae comitantes of the graft were anastomosed to the venae comitantes of the recipient peroneal artery. The distal end of the peroneal artery was anastomosed to the distal stump of the anterior tibia1 artery at a point near the ankle joint in order to maintain the circulation of the foot. Since bone union in the proximal region was delayed at 5 months, an additional iliac bone graft was performed, followed by external skeletal fixation. Although fracture of the grafted fibula occurred 14 months postoperatively, bone union was achieved after two months of cast immobilization. A functional brace was used in the subsequent six months. At present, two years and nine months postoperatively, the grafted fibula shows hypertrophy, and no tumor recurrence has occurred (Fig. 1D). DISCUSSION
Vascularized fibula grafting has been used to treat intractable diseases such as traumatic bone defect, osteomyelitis, uncurable nonunion, and congenital pseudoarthrosis. In such cases, this technique has yielded excellent results. Since increasing attempts have been made to salvage limbs affected with malignant bone tumors following advances in
Vascularized Fibula Graft
229
Figure 1. Case 14: A 55-year-old man with squamous cell cardnoma of left lower leg. A: Preoperative photograph of the anterior aspect of the left leg showing a cauliflower-likegrowth of granulation. B: Preoperative lateral radiograph of the left tibia showing irregular
bone absorption. C: Vascularizedfibula with a 24 x 12 cm flap was transferred to reconstruct the defect after tumor resection. 0: Anterior-posterior radiograph at 2 years and 9 months postoperatively demonstrating perfect union without tumor recurrence.
chemotherapy and radiotherapy, vascularized fibula grafting has been receiving more attention as a means of reconstructi~n.~-~ Formerly, these defects had been commonly reconstructed by autogenous and homogeneous bone grafting, or prosthetic replacement. When nonvascularized
bone, autogenous or homogenous, is grafted, however, the time required for bone union is significantly long especially if the graft is more than 7 cm long. According to Enneking et al. ,9 the incidence of nonunion was 32% after grafting a nonvascularized bone of 7.5-25 cm in length. With vascu-
230
Yajirna et al.
Figure 2. Case 15: A 13-year-oldgirl with Ewing’s sarcoma of the right iliac bone. A: Preoperative angiography showing pooling of the contrast media consistent with the tumor. 6:Anterior-posterior radiograph at 4 months after twin barrel vascularized fibula (star) and
nonvascularized fibula (asterisk) grafting. Bone union of the vascularized fibula grafts was completed, while that of the nonvascularized fibula graft was delayed.
larized fibula grafting, which involves grafting a viable bone while preserving its blood flow, more rapid bone union can be obtained irrespective of the length of the graft. When we used this technique for reconstruction of the ex-
tremities and pelvis after resection of bone tumors, the mean time until completion of bone union was as short as 4.1 months even though the size of the bone defects was large (6-20 cm; mean, 12 cm). Figure 2B shows a radio-
231
Vascularized Fibula Graft Table 1. Summary of Cases Treated.
Case 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19
Age (yrs) 27 63 68 27 68 29 80 18 55 25 26 44 44 55 13 19 14
53 21
Recipient site Femur Tibia Tibia Radius Mandibula Spine Mandibula Mandibula Mandibula Femur Radius Femur Radius Tibia Pelvis Femur Mandibula Mandibula Pelvis
Tumor Giant cell tumor (R)b
M.F.H.C (R) Adamantinoma Giant cell tumor Squamous cell carcinoma Giant cell tumor (R) Squamous cell carcinoma Adamantinoma Squarnous cell carcinoma Parosteal osteosarcoma (R) Giant cell tumor Chondrosarcorna Giant cell tumor (R) Squamous cell carcinoma Ewing's sarcoma Giant cell tumor Adamantinoma Squamous cell carcinoma Chondrosarcoma
Surgical stagea
Bone defect
Follow
IB IIB IB IA I1B IB IIB IA I1 B IB IB IB IB IIB II B IB IB IIB II B
17(cm) 18 20 6 8 9 10 14 8 10 18 14 9 18
9y. 10m. 9y. 6m. 8;. IIm. 7y. 11m. 6y. 5m. 6y. 3rn. 5y. 5m. 4y. 11m. 4y. 7rn. 4y. 7m. 2y. 2m. 3y. 3m. 2y. I l m . 2y. 9m. llrn. 2y. 2m. ly. 6m. 8m. 6rn.
11
10 12 14 12
UP
Fibula fracture
+
Additional bone graft -
Local recurrence
-
+
+ +
-
-
-
'Surgical Staging System of Enneking. b(R), recurrent tumor. 'M.F.H.,malignant fibrous histiocytoma.
graph of the pelvis in a 13-year-old girl in whom a twin barrel vascularized fibula and a nonvascularized fibula were grafted for the reconstruction of a pelvic defect after resection of an Ewing's sarcoma. Complete bone unions are visible at the vascularized fibula grafts, while bone union is not achieved at the nonvascularized fibula graft. These results clearly demonstrate the usefulness of vascularized fibula grafting. Furthermore, since it is richly vascularized, it is highly resistant to infection and hence enhances the safety of chemotherapy after grafting. Although some investigators have reported that postoperative chemotherapy affects bone only one of our cases showed delayed bone union attributable to chemotherapy after grafting. Although infection is likely to occur after reconstruction of the mandible with conventional methods, none of our cases showed infection after jaw reconstruction. The greatest advantage of vascularized fibula grafting seems to lie in the feasibility of one-stage reconstruction for various tissues. The use of the peroneal artery as a vascular pedicle makes it possible to obtain a flap, nerves, and muscles, together with the fibula. For this reason, this technique is particularly superior to the conventional techniques in cases of malignant bone tumor where a wide soft tissue defect is created by tumor resection (Fig. 1C). Another advantage of this technique is hypertrophy of the fibula after grafting. This is a very interesting feature of this surgery. We think that this phenomenon occurs because the grafted fibula is alive." The hypertrophy of the grafted fibula develops more rapidly the younger the patient. However, even at the relatively advanced age of 63 years (Case 3), the
grafted fibula showed an increase in width to a level comparable to the width of the original fibula (Fig. 3B). This phenomenon was prompted by stress fractures. In the present study, 4 cases showed fracture of the grafted fibula. In 3 of these 4 cases, bone union was completed rapidly, and the grafted bone showed marked hypertrophy after completion of union. The greatest problem associated with this technique is that it is much more complex than the conventional techniques, thus requiring more time and causing more blood loss and surgical stress. Since most patients for whom this technique is indicated have malignant tumors, it is important to avoid putting too much emphasis on limb salvage, so as not to increase the incidence of fatal metastasis. This technique also has problems pertaining to the donor site and postoperative monitoring. However, these problems are negligible in view of the great advantages provided. Vascularized fibula grafting for reconstruction of bone defects after tumor resection is indicated in the following cases: (1) cases in which the bone defect is larger than 7 cm, (2) cases accompanied by extensive soft tissue defects, (3) cases requiring reconstruction of the distal end of the radius, and (4) cases having undergone multiple operations previously even if the recurrent defect is small. Enneking's stage IA, IB, and IIA cases are good indications for this technique. Tomita' reported that stage IIB cases are not indicated for this technique. According to Saito et al.,* who applied this technique to 4 cases of stage IIB, one case died while the remaining 3 cases had an excellent, recurrencefree postoperative course. Our stage IIB cases responded
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Figure 3. Case 3: A 68-year-old man with right tibial adamantinoma. A: A 24 cm vascularized fibula with peroneal flap was transferred for the reconstruction of the bone and soft tissue defect. 6:Anteriorposterior radiograph at 8 years and 1 1 months postoperatively showing marked hypertrophy of the grafted fibula.
poorly to this technique. Therefore, the use of this technique in Stage IIB cases requires a careful approach. In this study, 3 cases developed local recurrence. In all these cases, vascularized fibula grafting was used after resection of recurrent tumor. Therefore, the indications for this technique in reconstruction after resection of recurrent tumors need to be reviewed. In cases where this technique was used for reconstruction after the first resection of tumor, the results were excellent. These results suggest that wide excision should be performed during the first operation and that, additionally, this technique of reconstruction be used during the same operation. Of course, this technique of reconstruction is not indicated in cases complicated by remote metastasis. Such cases require amputation or prosthetic replacement. In cases where the tumor is located in the vicinity of the knee joint, the selection of this technique (for arthrodesis) or prosthetic replacement should be determined based on age, gender, occupation of the patient and other factors. In view of the short life, the susceptibility to infection, and other problems of the currently available artificial joints, arthrodesis with this technique seems to be preferable if the patient is young. Since the maximum length of fibula that can be donated is 24-26 cm, the extent of reconstruction possible with this technique is limited. However, even when the length of fibula that can be obtained is not long enough to cover the defect, this technique can be used if the patient is young and limb lengthening can
be done later. In middle-aged or elderly patients, prosthetic replacement (bone and joint) should be adopted if the size of the fibula that can be donated is not large enough for reconstruction. Vascularized bone or joint allografting may be realized in the future.'*
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staging of the muscloskeletal sarcoma. Clin Orrhop 153: 106-120, 1980. 2. Taylor GI, Miller GD, Ham FG: The free vascularized bone graft: A clinical extension of microvascular techniques. Plusr Reconsrr Surg 551533-544, 1975. 3. Moore JR, Weiland AJ, Daniel R K Use of free vascularized bone grafts in the treatment of bone tumors. Clin Orthop 175:37-44, 1983. 4. Usui M, lshii S, Yamamura M, Minami A, Sakuma T: Microsurgical reconstructive surgery following wide resection of bone and soft tissue sarcomas in the upper extremities. J Reconstr Surg 2:77-84, 1986. 5 . Gidumal R, Wood MB, Sim FH, Shives TC: Vascularized bone transfer for limb salvage and reconstruction after resection of aggressive bone tumor. J Reconstr Surg 3:183-188, 1987. 6 . Aberg M , Rydholm A, Holmberg J, Wieslander JB: Reconstruction with a free vascularized fibular graft for malignant bone tumor. A ( m Orthop Scund 59:430-437, 1988. 7. Tomita K: Vascularized bone grafts for limb salvage and reconstruction after resection of malignant bone tumors. Bessatsu Seikei Ceku 8:174-180, 1985 (in Japanese). 8. Saito H: Vascularized fibula grafts in limb sparing tumor surgery. Shujuru 42:289-298, 1988 (in Japanese). 9. Enneking WF, Eady JL, Burchardt H: Autogenous cortical bone grafts
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Vascularized Fibula Graft in the reconstruction of segmental skeletal defects. J B o n e Joinr Surg 62A:1039-1058, 1980. 10. Friedelaender GE, Tross RB, Doganis AC, Kirkwood JM, Baron R: Effects of chemotherapeutic agent on bone: 1. Short-term methotrexate and doxorubicin (adriamycin) treatment in a rat model. J Bone Joint Surg 66A:602-607, 1984.
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11. Mizumoto S, Tamai S, Yajima H, Yoshii T: Experimental study of vascularized tibio-fibula graft in inbred rats: A preliminary report. J Reconstr Microsurg 3: 1-9, 1986. 12. Randolph MA, Yaremchuk MJ, Moore JR, Robinson RA, Weiland AJ: Experimental vascularized bone allografting. Microsurgery 8: 210-217, 1980.
