Long-Term Evaluation After Mandibular Reconstruction With Fibular Grafts Versus Microsurgical Fibular Flaps

J Oral Maxillofac Surg 65:281-286, 2007

Long-Term Evaluation After Mandibular Reconstruction With Fibular Grafts Versus Microsurgical Fibular Flaps Lei Li, DMD, MD, PhD,* Felix Blake, MD, DMD,† Max Heiland, MD, DMD, PhD,‡ Rainer Schmelzle, MD, DMD, PhD,§ and Philipp Pohlenz, MD, DMD㛳 Purpose: This retrospective study was performed to compare the bone resorption rates of revascular-

ized free fibular flaps with those of avascular fibular bone grafts. Special attention was drawn to horizontal bone resorption. Patients and Methods: One hundred twelve patients who had received fibular grafts for reconstruction of the mandible were included in this study. Surgery was performed between 1991 and 2004, leading to a follow-up of 12 to 140 months. In 7 cases, microvascular onlay grafts (group A), and in 61 cases, microvascular reconstruction of segmental defects (group B) were performed. Avascular onlay grafts were applied (group C) in 41 patients and avascular reconstruction of segmental defects (group D) was performed in 7 patients. Bone heights were measured on panoramic views at 1, 3, and 7 years postoperatively. Results: Most of the resorption in group B occurred during the first postoperative year, at an average rate of 16% (range, 3% to 30%). After the first year, transplants became almost stable, and an average of 80% of bone height was maintained after 7 years. Conversely, bone resorption continued regularly in group C, and up to an average of 51% (range, 5% to 80%) of bone height was lost after 7 years postoperatively. Conclusion: After mandibular reconstruction with fibular transplants, resorption occurs among both microsurgical and free grafts; however, the bone resorption rate was higher among avascular grafts. In group A and B patients, fibular grafts became stable after 1 year, but bone resorption continued at a regular rate in groups C and D. © 2007 American Association of Oral and Maxillofacial Surgeons J Oral Maxillofac Surg 65:281-286, 2007

history of nearly 20 years.2 This has become the preferred donor site for many head and neck surgical centers.3-5 However, long-term follow-up studies on mandibular reconstruction with fibular transplant are few and are often based on a limited number of patients.6,7 Regarding the long-term success of bone reconstruction, the level of resorption that leads to loss in bone height is of major interest; however, these studies often deal with the iliac crest as the donor site.8 Bone grafts in cases of nonsegmental mandibular defects or of severely atrophied jaws are exposed to different biomechanical loadings and are difficult to compare.9,10 In this study, we focused on long-term results regarding bone resorption after mandibular reconstruction or augmentation performed with the fibular as the donor site. Resorption rates between revascularized free fibular flap and avascular fibular bone graft were compared. Both groups were subdivided according to the indication for bone transfer (ie, recon-

Thirty years have passed since the first vascularized fibular transplant was implemented in Japan to bridge a tibial defect.1 Mandibular reconstruction performed with use of the microsurgical free fibular flap has a Received from the Department of Oral and Maxillofacial Surgery, University Medical Center Hamburg-Eppendorf, Hamburg, Germany. *Senior Resident. †Senior Resident. ‡Associate Professor. §Professor and Head. 㛳Senior Resident. Address correspondence and reprint requests to Dr Pohlenz: Department of Oral and Maxillofacial Surgery, University Medical Center Hamburg-Eppendorf, Martinistr. 52, D-20246 Hamburg, Germany; e-mail: [email protected] © 2007 American Association of Oral and Maxillofacial Surgeons

0278-2391/07/6502-0020$32.00/0 doi:10.1016/j.joms.2006.08.009

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Indications for mandible reconstruction

number of patients

60 50

squamous- cell carcinoma atrophy of jaw

40

osteomyelitis ameloblastoma

30

injury

20

osteoradionecrosis adenoidzystics-carcinoma

10 0

osteogenetic sarcoma

Diagnosis

1

FIGURE 1. Indications for reconstruction of the mandible. Li et al. Long-Term Evaluation After Mandibular Reconstruction. J Oral Maxillofac Surg 2007.

struction of mandibular segmental defects vs onlay grafts). Resorption rates were determined after 1, 3, and 7 years, and the influences of radiotherapy and of inserted implants were evaluated.

Patients and Methods In the Department of Oral and Maxillofacial Surgery of the University Medical Center Hamburg-Eppendorf, mandibular reconstruction or augmentation with the use of fibular transplants was performed on 112 patients from 1992 to 2004. Among them were 68 cases in which microsurgical free fibular flaps were used for mandibular reconstruction after segmental resection; these occurred primarily because of squamous cell carcinoma. In 44 cases, avascular fibular grafts were used predominantly for mandibular augmentation (Fig 1). Bone-only fibular free flaps were harvested through a medial approach; avascular fibular grafts were harvested according to the technique described by Bschorer and Schmelzle.11 Patients were divided into 4 groups as follows: Group A: Microvascular onlay grafts Group B: Microvascular reconstruction of segmental defects Group C: Avascular onlay grafts Group D: Avascular reconstruction of segmental defects. Initial panoramic views were taken at between 1 and 2 weeks postoperatively. Follow-up examinations were performed after 12 to 140 months postoperatively. Bone heights were measured on radiographs at 1, 3, and 7 years postoperatively. Measurements were taken in the midportion of the fibular transplants and were compared with those from identical sites on sequential radiographs. Attention was paid to eliminating magnification as a possible source of error in measurement.

Results Five male and 2 female patients constituted group A, with a mean age of 56 years (range, 44 to 68 yr). Thirty-four male and 27 female patients made up group B, with a mean age of 55 years (range, 16 to 74 yr). Group C consisted of 27 male and 13 female patients with a mean age of 50 years (range, 29 to 67 yr), and group D comprised 2 male and 2 female patients with a mean age of 54 years (range, 48 to 66 yr). A total of 19 patients in groups A and B received radiation treatment after undergoing tumor resection; average dose was 65 Gy (range, 60 to 75 Gy). No fibular graft was transplanted before radiotherapy was received. Mean duration of operative time was 491 minutes, and mean duration of hospitalization was 34.5 days (range, 16 to 63 d) in groups A and B. Mean duration of operative time was 140 minutes, and mean duration of hospitalization was 16 days (range, 4 to 30 d) in groups C and D. For a mandibular segmental defect larger than 10 cm, free fibular flap is the only therapy of choice. Three fibular bone grafts measuring between 10 and 15 cm were used for augmentation. In group B, 1 perioperative death was caused by thrombocytopenia, 3 flap losses occurred in irradiated cases (3/19), and 1 flap loss was reported in a nonirradiated patient (1/42). Two fibular grafts (2/41) were lost completely and 2 nonunions were observed in group C. Both healed after surgical intervention. In terms of donor site complications, all patients experienced some early temporary gait disturbance. Reduced sensation in the functional area of the sural nerve was found in varying degrees in 5 patients from group B. Ongoing edema accompanied by pain was reported in 1 patient from group C. No

Horizontal Bone Resorption

60 50 40 30 20 10 0

51 21

19

38

bone resorption 7.postop

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18 15

47 42

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28

24

bone resorption 3.postop

bone resorption 1.postop

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microvascular onlay grafting

microvascular reconstruction of segmental defects

avascular onlay grafting

avascular reconstruction of segmental defects

FIGURE 2. Horizontal bone resorption rates 1, 3, and 7 years postoperatively. In groups A and B, most resorption occurred during the first postoperative year. Afterward, fibular transplants became stable and an average of 80% of bone height was maintained after 7 years. Transplants treated with radiotherapy caused no obvious differences. Bone resorption in groups C and D continued regularly, and up to 51% of bone height was lost. Li et al. Long-Term Evaluation After Mandibular Reconstruction. J Oral Maxillofac Surg 2007.

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motor weakness of the great toe and no ankle stiffness occurred in any patient. No immediate postoperative infection was encountered, but partial dehiscence occurred in 12 patients in group B. Bone resorption was measured indirectly by determination of fibular height at 1, 3, and 7 years postoperatively. A total of 80 patients— 42 in groups A and B and 38 in groups B and C—were followed for at least 7 years. Resorption rates are shown in Figure 2. Most resorption occurred during the first postoperative year in group A (15% on average [range, 5% to 28%]) and in group B (16% [range, 3% to 30%]). Transplants became almost stable, and an average of 80% of bone height was maintained after 7 years. Dividing groups A and B into subgroups with and without irradiation, respectively, caused no obvious differences. Conversely, bone resorption continued progressively in groups C and D; after 7 years, an average of 51% in group C (range, 5% to 80%) and in group D 47% of bone height was lost. Fourteen implants were placed in 7 patients from group A, as were 134 implants in 61 patients in group B, 84 implants in 43 patients in group C, and 7 implants in 4 patients in group D; dental implants were inserted an average of 8 months after bone grafting (range, 1 to 16 months; Fig 3). Figure 4 shows bone resorption rates of 35% and 49% after 7 years among patients with and without dental implants in groups C and D. A clinical example of segmental reconstruction after squamous cell carcinoma with the use of a microvascular fibular flap is shown in Figure 5, and various types of onlay grafting are presented in Figures 6 and 7.

graft volume proved uniformly stable, with only small losses occurring over a decade; more than 90% of fibular height was maintained.6 In patients with microvascular reconstruction of segmental defects, a mean of 16% (range, 3% to 30%) of graft height resorption was noted after 1 year; this has to be considered a form of bone remodeling. After this phase, microvascular fibular transplants became stable, with more than 80% of bone height preserved. This has been confirmed by follow-up of 80 patients after at least 7 years (range, 7 to 13 years). No obvious differences in bone resorption were noted with respect to preoperative irradiation, but secondary microsurgical reconstruction in the radiated field may be challenging for the surgeon. In this study, the avascular fibular graft was used primarily as an onlay graft for augmentation of the mandibular alveolar ridge. This approach found no application in irradiated cases. For recontruction of segmental defects, this technique was selected for 4 patients in whom general condition was too poor to permit a free flap procedure. The

A Implants Group A+B 30 25 20 15 10 5

Discussion Mandibular reconstruction with the use of a revascularized bone graft is a reliable procedure and the state-of-the-art technique at many head and neck reconstruction centers. The ileum, scapula, and fibula are preferred donor sites for mandibular reconstruction.3,4,12-16 The fibula has become more popular— even more popular than ileum— especially over the past 10 years.5,6 For many authors, the fibula is the flap of first choice for most mandible reconstructions. The main advantages of free fibular flap, which are well documented in the literature, include 1) its long, large caliber and anatomically constant pedicle, 2) its almost unlimited length, which allows multiple osteotomies for mandible reconstruction, and 3) the relatively insignificant morbidity of the donor site. It has proved to be a durable reconstruction over time from both functional and esthetic points of view. Hidalgo, one of the pioneers in this field, reported 20 cases of mandibular reconstruction in which revascularized free fibular flap was used that have been followed for at least 10 years. It was found that bone

0 0

1

2

3

group A (61) group B (7)

4

5

>6

B Implants Group C+D 25 20 15 10 5 0 0

1

2

3

4

group C (41) group D (4)

5

6

FIGURE 3. Distribution of dental implants. A, Patients with microvascular fibular transplants (groups A and B). B, Patients with avascular fibular transplants (groups C and D). Li et al. Long-Term Evaluation After Mandibular Reconstruction. J Oral Maxillofac Surg 2007.

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Effect of dental implants on bone resorption

50

45

40

resorption %

35

30

25 fbg+ implants fbg

20

15

10

5

0 1

3

7

years

FIGURE 4. Effects of dental implants on bone resorption. Dental implants inserted an average of 8 months after bone grafting may slow down the process of horizontal bone resorption in patients with avascular fibula grafts (groups B and C). fbg, avascular fibula bone graft. Li et al. Long-Term Evaluation After Mandibular Reconstruction. J Oral Maxillofac Surg 2007.

FIGURE 5. Panoramic views after microsurgical fibular flap. In a 63-year-old man, the mandibular defect after segmental resection because of squamous cell carcinoma was reconstructed with a microsurgical free fibular flap on the left side. A, Postoperative radiograph. B, 3 years postoperatively. Measurements were taken at the midportion of the fibular transplant with a horizontal bone resorption of 15%. Three dental implants were inserted 6 months after reconstruction. C, Follow-up panoramic view 7 years after transplantation. Bone resorption was measured at 18%. Li et al. Long-Term Evaluation After Mandibular Reconstruction. J Oral Maxillofac Surg 2007.

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quantity and the quality of soft tissue coverage are the key points to success in avascular bone grafts. In contrast to microsurgical fibular transplantation, water-tight closure over the avascular fibula is always required. Once wound dehiscence has occurred, it has proved difficult to manage by means of surgical revision. Two fibular bone grafts were lost this way. Bone grafting without microsurgical anastomoses did not result in durable reconstruction in that the resorption rate was high and infection was likely to occur.17 Numerous studies have investigated avascular iliac bone transplantation,18,19 but up to now, little has been known about the long-term fate of the fibular bone graft. It has been hypothesized that because of its high cortical bone content, the fibular bone graft as compared with the iliac transplant was less liable to be resorbed.11 This study provides insight into such issues on the basis of its review of 80 patients who were followed for at least 7 years. Resorption after avascular fibula bone graft transplantation did occur, and it continued at a regular rate. One half of fibular height was lost by the seventh postoperative year. Insertion of dental implants at an average of 8 months after bone grafting seemed to be an effective way of slowing down this process. No bone hypertrophy was observed in any case in spite of implant loading.

FIGURE 7. Panoramic views after avascular onlay grafting. A 59-year-old man underwent mandibular augmentation with avascular fibular transfer. A, Postoperative radiograph. B, One year postoperatively. C, Three years postoperatively. Li et al. Long-Term Evaluation After Mandibular Reconstruction. J Oral Maxillofac Surg 2007.

The retrospective study presented here focused on the horizontal resorption rate after fibular transplantation. For determination of the level of bone resorption, the study population was divided into 4 groups according to indication for bone transfer and the technique used. This resulted in heterogenous study groups of different sizes. However, despite this heterogeneity, results clearly show that the microvascular fibular transfer is superior in terms of long-term level of resorption. FIGURE 6. Panoramic views after microsurgical fibular onlay graft. A 47-year-old woman with atrophy of the mandible underwent onlay grafting with use of a microsurgical fibular flap. A, Postoperative radiograph. B, One year after bone flap. Li et al. Long-Term Evaluation After Mandibular Reconstruction. J Oral Maxillofac Surg 2007.

References 1. Ueba Y, Fujikawa S: Nine years follow-up of a vascularized fibular graft in neurofibromatosis: A case report and literature review. Orthop Trauma Surg 26:595

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2. Hidalgo DA: Fibula free flap: A new method of mandible reconstruction. Plast Reconstr Surg 84:71, 1989 3. Hidalgo DA, Rekow A: A review of 60 consecutive fibula free flap mandible reconstructions. Plast Reconstr Surg 96:585, 1995 4. Wei FC, Seah CS, Tsai YC, et al: Fibula osteoseptocutaneous flap for reconstruction of composite mandibular defects. Plast Reconstr Surg 93:294, 1994 5. Genden E, Haughey BH: Mandibular reconstruction by vascularized free tissue transfer. Am J Otolaryngol 17:219, 1996 6. Hidalgo DA, Pusic AL: Free-flap mandible reconstruction: A 10-year follow-up study. Plast Reconstr Surg 110:438, 2002 7. Munoz Guerra MF, Gias LN, Campo FJR, et al: Vascularized free fibular flap for mandibular reconstruction: A report of 26 cases. J Maxillofac Surg 59:140, 2001 8. Binger T, Hell B: Resorption of microsurgically vascularised bone grafts after augmentation. J Cranio Maxillofac Surg 27:82, 1999 9. Bell RB, Blakey GH, White RP, et al: Staged reconstruction of severely atrophic mandible with autogenous bone graft and endosteal implants. J Maxillofac Surg 60:1135, 2002 10. Verhoeven JW, Cune MS, Terlou M, et al: The combined use of endosteal implants and iliac crest onlay grafts in the severely atrophic mandible: A longitundinal study. J Oral Maxillofac Surg 26:351, 1997

11. Bschorer R, Schmelzle R: Verwendung des Fibulaspans bei der Kieferkammaugmentation. Ergebnisse nach 2 Jahren Mund Kiefer Gesichtschir 1:276, 1997 12. Daniel RK: Mandible reconstruction with free tissue transfers. Ann Plast Surg 1:346, 1978 13. Taylor GI: Reconstruction of the mandible with free composite iliac bone grafts. Ann Plast Surg 9:361, 1982 14. Schmelzle R: Vascular pedicled iliac crest transplant and its use in the jaw. Handchir Mikrochir Plast Chir 18:376, 1986 15. Shpitzer T, Neligan PC, Gullane PJ, et al: The free iliac crest and fibula flaps in vascularized oromandibular reconstruction: Comparison and long-term evaluation. Head Neck 21:639, 1999 16. Baker SR: Scapular flap, in Baker SR (ed): Microsurgical Reconstruction of the Head and Neck. New York, Churchill Livingstone, 1989, pp 159-190 17. Foster RD, Anthony JP, Sharma A, et al: Vascularized bone flap versus nonvascularized bone grafts for mandibular reconstruction: An outcome analysis of primary bony union and endosseous implant success. Head Neck 21:66, 1999 18. Farrell CD, Kent JN, Guerra LR: One stage interpositional bone grafting and vestibuloplasty of atrophic maxilla. J Oral Surg 34:901, 1976 19. Härle F: Follow-up investigation of surgical correction of the atrophic alveolar ridge by Visor-osteotomy. J Maxillofac Surg 7:283, 1979