ORIGINAL ARTICLE
Evaluation of Bone Height of the Free Fibula Flap in Mandible Reconstruction Takaya Makiguchi, MD, PhD, Satoshi Yokoo, DMD, DMSc, Kazunobu Hashikawa, MD, PhD,y Hidetaka Miyazaki, DDS, PhD, and Hiroto Terashi, MD, PhDy Background: Use of a vascularized free fibula flap has become a
preferred method of mandible reconstruction after oncologic surgical ablation. Despite its many advantages, the low vertical height of the graft is a potential drawback and severe long-term atrophy of fibular bones may cause stress fracture and is disadvantageous for osseointegrated dental implants and facial contours. Therefore, it is important to investigate the degree of resorption based on the fibular height and the factors related to resorption over time. The influence of aspects of the intraoperative surgical procedure, such as preservation of a nutrient artery from the peroneal artery to the fibula bone marrow and the number of segmental osteotomies, has not been examined previously. Therefore, the purpose of this study was to examine the change in fibular height and the factors influencing resorption, including those associated with the surgical procedure. Patients and Methods: A retrospective analysis was performed in 19 patients who underwent free vascularized fibular mandibular reconstruction for oncologic surgical defects without radiotherapy. Postoperative Panorex examinations were used to evaluate fibular height, and 7 factors with a potential influence on long-term fibular height were evaluated: age, gender, length of the mandible defect, number of segmental osteotomies, preservation of a direct nutrient artery from the peroneal artery to the fibula bone marrow, length of follow-up, and delayed placement of osseointegrated dental implants. Results: Fibular bone height decreased in 13 patients (68%), was unchanged in 2 (11%), and increased in 4 (21%). Segmental osteotomies and female gender were significant factors promoting fibular bone resorption (P < 0.001 and P < 0.001, respectively), and preservation of a nutrient artery to the bone marrow, male gender, and delayed placement of osseointegrated dental implants were significant factors inhibiting bone resorption (P < 0.01, P < 0.001, and P < 0.05, respectively). Age, length of follow-up period, and length of the mandibular defect showed no significant relationship with bone resorption (P ¼ 0.77, P ¼ 0.78, and P ¼ 0.105, respectively). Conclusion: The results of this study showed that fibular height in mandibular reconstruction can be maintained by preservation of a From the Department of Stomatology and Maxillofacial Surgery, Gunma University Graduate School of Medicine, Gunma; and yDepartment of Plastic Surgery, Kobe University Graduate School of Medicine, Kobe, Japan. Received July 6, 2014. Accepted for publication December 2, 2014. Address correspondence and reprint requests to Takaya Makiguchi, MD, PhD, Department of Stomatology and Maxillofacial Surgery, Gunma University Graduate School of Medicine, 3-39-22, Showa-machi, Maebashi, Gunma 371-8511, Japan; E-mail: [email protected] The authors report no conflicts of interest. Copyright # 2015 by Mutaz B. Habal, MD ISSN: 1049-2275 DOI: 10.1097/SCS.0000000000001509
The Journal of Craniofacial Surgery
direct nutrient artery to bone marrow, avoidance of osteotomies, and delayed placement of osseointegrated dental implants, all of which inhibit fibular bone resorption. Key Words: bone height, bone resorption, fibula flap, mandible reconstruction, risk factor (J Craniofac Surg 2015;26: 673–676)
U
se of a vascularized free fibula flap has become a preferred method of mandibular reconstruction after oncologic surgical ablation1–5 due to advantages of a satisfactory functional and aesthetic outcome, a sufficient bone length for the graft, low donor-site morbidity, and potential use of a 2-team approach in the operation. Use of the fibula for reconstruction of the mandible differs from lower extremity reconstruction. More osteotomies are generally performed to achieve mandibular shape and osseointegrated dental implants are sometimes inserted in the flap. Furthermore, transferred fibular bones in the lower extremity tend to undergo hypertrophy, whereas in the mandible these bones tend to be absorbed.6– 9 Despite its many advantages, the fibular bone vertical height is less than that of the scalp and iliac crest bone flap for the mandible. Severe atrophy of fibular bones may cause stress fracture and may limit placement of a dental implant,10 whereas severe resorption causes aesthetic problems with the contour of the face. These problems make it important to investigate the degree of resorption of the fibular bone mass and factors related to resorption over time. However, there have only been a few retrospective follow-up studies of bone mass and loss of vertical height, with the conclusion that age, follow-up duration, placement of osseointegrated dental implants, radiotherapy, and site of reconstruction are not significantly associated with decreased bone height.7–9 However, there has been no previous study of the effects of factors
FIGURE 1. Measurement of fibular bone resorption. Bone height was measured in the mid-portion of the transferred fibula bone. For an osteotomized fibula flap, bone height was measured at the middle of the distal segment of the fibula. Differences in Panorex magnification were adjusted for by comparison of miniplate measurements. A, Bone height immediately after surgery. B, Bone height at late follow-up.
Volume 26, Number 3, May 2015
673
Copyright © 2015 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
The Journal of Craniofacial Surgery
Makiguchi et al
Volume 26, Number 3, May 2015
TABLE 1. Details of 19 Cases and Fibular Bone Resorption Index (FBRI) Patient (n ¼ 19) 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19
Gender
Age (yr)
Length of Defects (mm)
No. Osteotomies
Nutrient Artery
Dental Implant
Length of Follow-Up (mo)
FBRI (%)
F M M M F F M F F M F F F M M F F M F
55 65 46 64 51 58 71 45 56 65 61 27 65 64 66 35 67 52 68
78 115 67 77 89 55 66 145 88 84 107 51 55 89 83 110 54 83 96
0 2 0 0 0 0 0 2 1 0 1 1 0 1 0 0 0 1 1
Preservation — Preservation Preservation — Preservation — — — Preservation — — Preservation — — — Preservation — —
Placement — Placement — — — — Placement — — — — — — — Placement — — —
115 18 28 12 22 12 16 77 24 12 17 39 62 15 16 13 17 21 25
0 33 11 5 0 8.3 7.7 38 24 5.9 24 20 5.3 13 6.3 6.3 7.7 13 31
M, male; F, female.
related to intraoperative surgical procedures, such as preservation of a direct nutrient artery from the peroneal artery to the fibula bone marrow and performance of segmental osteotomies. In other words, no previous issue reported absorption of reconstructed fibula, based on differences of blood supply for it. Therefore, the purpose of this study was to determine the influence of such factors on the change in fibular height and bone resorption.
PATIENTS AND METHODS A retrospective analysis was performed in 26 patients who underwent vascularized free fibula flap mandible reconstruction after oncologic resection requiring segmental mandibulectomy between 1995 and 2012 at Kobe University Graduate School of Medicine and Gunma University Graduate School of Medicine. Panorex examinations were used to evaluate fibular height after segmental mandibulectomy. Of these patients, 19 with at least 12 months of follow-up and without radiotherapy were included in this study. Seven factors with a potential influence on long-term fibular height were evaluated: age, gender, length of mandibular defect, number of segmental osteotomies (excluding the ends of the graft), preservation of a direct nutrient artery from the peroneal artery to the fibula bone marrow, length of follow-up, and delayed placement of osseointegrated dental implants. The fibular bone resorption index (FBRI) was defined to evaluate the extent of bone resorption or hypertrophy (Fig. 1). Negative, positive, and zero values of FBRI indicate resorption, hypertrophy, and no change in fibular bone, respectively. Fixation hardware or a dental implant was used as a reference to prevent measurement errors caused by projection on magnification. Multiple regression
model for multivariate analysis was carried out to identify factors associated with bone resorption using SPSS Statistics 22. A P value of less than 0.05 was considered statistically significant.
RESULTS The patients included 8 males and 11 females, and had a mean age of 56.9 years (range, 27-71 years). Panorex examinations were performed 12 to 115 months postoperatively (mean, 29.5 months). The mean FBRI was 10.4%. Fibular height decreased in 13 patients (FBRI, 38% to 5%), was unchanged in 2 (FBRI, 0%), and increased in 4 (FBRI, þ6.3% to þ11%) (Tables 1, 2; Figs. 2, 3).
TABLE 2. Fibular Bone Resorption Index (FBRI)
FBRI > 0 (hypertrophy) FBRI ¼ 0 FBRI < 0 (resorption) All
674
No. Cases
FBRI Range (Mean)
4 2 13 19
þ6.3% to þ11% (þ7.8%) 0% 38% to 5% (17.6%) 38% to þ11% (10.4%)
FIGURE 2. Results from the case with most absorption (FBRI, 33%). Panorex examination immediately after surgery (A) and at 77 months after surgery (B). The patient was a 45-year-old female in whom 2 segmental osteotomies were performed. Cutting of the nutrient artery was required in the reconstruction stage.
#
2015 Mutaz B. Habal, MD
Copyright © 2015 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
The Journal of Craniofacial Surgery
Volume 26, Number 3, May 2015
Bone Height of the Free Fibula Flap
strongly with fibular resorption, whereas preservation of a nutrient artery to the fibula marrow inhibited resorption (Figs. 4, 5). Osseointegrated dental implants were placed in 2 of 4 patients in whom hypertrophy of the fibula bone occurred, and this procedure may be linked to bone hypertrophy.
DISCUSSION
FIGURE 3. Results from the case with most thickening (FBRI, þ11%). Panorex examination immediately after surgery (A) and at 28 months after surgery (B). The patient was a 46-year-old male who received delayed placement of osteointegrated dental implants. The nutrient artery to the fibula was preserved.
Zero to two segmental osteotomies were performed per patient, including 1 in 6 patients and 2 in 2 patients. Four patients had delayed placement of osseointegrated dental implants. The length of mandibular defects ranged from 51 to 145 mm (mean, 83.8 mm). A nutrient artery direct to the fibula bone was preserved in 7 patients, whereas this artery had to be cut at the reconstruction stage in 12 patients because of a problem with the length of the pedicle. No stress fracture was observed and bony union was attained in all patients in the follow-up period. Segmental osteotomies of the fibula flap and female gender were significant factors associated with fibular bone resorption (P < 0.001 and P < 0.001, respectively), and preservation of the nutrient artery to the fibula marrow, male gender, and delayed placement of osseointegrated dental implants were significantly associated with inhibition of fibular bone resorption (P < 0.01, P < 0.001, and P < 0.05, respectively). Age and length of followup and length of the mandibular defect showed no significant association with a change in bone resorption (P ¼ 0.77, P ¼ 0.78, and P ¼ 0.105, respectively) (Table 3). Among factors related to intraoperative surgical procedures, the number of segmental osteotomies of the fibula flap correlated
Use of a vascularized free fibular flap is an approved technique for mandibular primary reconstruction after oncologic resection requiring segmental mandibulectomy.1– 5 However, low fibular height is sometimes a problem for insertion of implants. This problem can be resolved using the ‘‘double-barrel’’ technique or vertical distraction osteogenesis, but the first of these approaches is restricted in terms of the extent of reconstruction and the second requires a long time.11,12 We found a mean FBRI of 10.4% in mandibular reconstruction, consistent with previous results showing retention of fibular height.7–9 Disa et al8 concluded that the height of the transferred fibula is maintained in most patients regardless of age, site of reconstruction, length of mandible defect, radiation, follow-up duration, and placement of osseointegrated dental implants. In their study, the mean resorption rate of less than 10% was a good result, but in 2 cases, the fibular height decreased by 22% and 33%, respectively. In our study, in 6 cases, absorption rates were also greater than 20% and FBRI of the most absorbed case was 38%. It is important to evaluate the cause of these high resorption rates. Therefore, we examined the effects of intraoperative surgical procedures, including the number of segmental osteotomies and preservation of a nutrient artery to the fibula bone marrow. These factors have not been examined in previous reports. In other words, a novel point of the article is to evaluate the fibula absorption, based on differences of blood supply for reconstructed fibula. The fibular bone flap receives blood supply from nutrient arteries that connect directly to fibular bone marrow from the peroneal artery, which is bifurcated at about one-third proximal to the end of the fibula and has many periosteal branches at distal sites (Fig. 6).13 Blood flow through a cross-section of the fibula decreased after cutting the nutrient artery to the bone marrow by our experience (Fig. 7). It is generally believed that the nutrient arteries provide the dominant blood supply to the fibula, but the periosteal branches may also supply blood to the fibular bone because the distal osteotomized bone segment of the fibula free flap was not necrotic and bony union with an adjacent normal mandible was attained without a nutrient artery. That is, free fibula flap could take if only periosteal branches would be preserved. However, our results indicate that segmental osteotomies of the fibula bone flap correlate strongly with fibular bone resorption, whereas preservation of a direct nutrient artery to the fibula bone marrow inhibits resorption. That is, the blood supply to the fibula bone marrow from the nutrient artery plays an important role in postoperative bone remodeling after flap survival. Thus, to inhibit fibular resorption, it is important to preserve the direct nutrient artery to the fibula, in contrast to findings in previous reports.7,8
TABLE 3. Factors Influencing Fibular Bone Resorption (Result of Multiple Regression Model for Multivariate Analysis) Factors Promoting Resorption (P < 0.05) Osteotomies of fibula (P < 0.001) Female gender (P < 0.001)
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2015 Mutaz B. Habal, MD
Factors Inhibiting Resorption (P < 0.05)
No Relationship With Resorption (P > 0.05)
Preserving nutrient artery (P < 0.01) Male gender (P < 0.001) Osteointegrated dental implant (P < 0.05)
Aging (P ¼ 0.77) Length of follow-up (P ¼ 0.78) Length of defects (P ¼ 0.105)
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Copyright © 2015 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
Makiguchi et al
The Journal of Craniofacial Surgery
Volume 26, Number 3, May 2015
FIGURE 7. Blood flow in a cross-section of the fibula before (A) and after (B) cutting the nutrient artery to the fibula bone marrow. After cutting the nutrient artery, blood flow in the fibula decreased.
FIGURE 4. Relationship of the number of osteotomies with FBRI. The number of segmental osteotomies of the fibula bone flap correlated strongly with fibular bone resorption.
dental implants in the fibula bone contribute to mastication ability, as pointed out by Schmelzeisen et al.14 The length of the follow-up period was not a significant factor in bone resorption in the current study, which included patients with at least 12 months of follow-up. Disa et al also found that the duration of follow-up was not a significant factor determining bone height based on a follow-up period of at least 24 months.7,8 Collectively, these studies demonstrate that fibular bone height does not change significantly in 12 to 24 months after the operation. In conclusion, our evaluation of factors with a potential influence on fibular bone in mandibular reconstruction showed that preservation of a nutrient artery to bone marrow, avoidance of osteotomies, and delayed placement of osseointegrated dental implants will inhibit bone resorption and maintain the fibular height.
REFERENCES
FIGURE 5. Relationship between preservation of a direct nutrient artery to bone marrow and FBRI. Large negative FBRI values were found for cases in which a nutrient artery was not preserved.
We also found that delayed placement of osseointegrated dental implants correlated with inhibition of bone resorption. Pressure from the tongue, lip, maxillary teeth, and food are transmitted to fibular bone via dental implants, and this intermittent kinetic load might contribute to bony formation. However, fibular bone and surrounding tissue such as the skin paddle of the fibular flap do not have an occlusal sensation. This makes it unclear if osseointegrated
FIGURE 6. Vascular anatomy of fibular bone. The fibula bone flap receives blood supply from nutrient arteries to the fibula bone marrow from the peroneal artery, which is bifurcated about one-third proximal to the end of the fibula and has many periosteal branches in the distal portion. The figure was modified from Mathes and Nahai.13
676
1. Hidalgo DA. Fibula free flap: a new method of mandible reconstruction. Plast Reconstr Surg 1989;84:71–79 2. Hidalgo DA, Pusic AL. Free-flap mandibular reconstruction: a 10-year follow-up study. Plast Reconstr Surg 2002;110:438–449 discussion 450–1 3. Wei FC, Seah CS, Tsai YC, et al. Fibula osteoseptocutaneous flap for reconstruction of composite mandibular defects. Plast Reconstr Surg 1994;93:294–304 discussion 305–6 4. Ferri J, Piot B, Ruhin B, et al. Advantages and limitations of the fibula free flap in mandibular reconstruction. J Oral Maxillofac Surg 1997;55:440–448 discussion 448–9 5. Sieg P, Zieron JO, Bierwolf S, et al. Defect-related variations in mandibular reconstruction using fibula grafts. A review of 96 cases. Br J Oral Maxillofac Surg 2002;40:322–329 6. El-Gammal TA, El-Sayed A, Kotb MM. Hypertrophy after free vascularized fibular transfer to the lower limb. Microsurgery 2002;22:367–370 7. Disa JJ, Winters RM, Hidalgo DA. Long-term evaluation of bone mass in free fibula flap mandible reconstruction. Am J Surg 1997;174:503–506 8. Disa JJ, Hidalgo DA, Cordeiro PG, et al. Evaluation of bone height in osseous free flap mandible reconstruction: an indirect measure of bone mass. Plast Reconstr Surg 1999;103:1371–1377 9. Ho¨lzle F, Watola A, Kesting MR, et al. Atrophy of free fibular grafts after mandibular reconstruction. Plast Reconstr Surg 2007;119:151–156 10. Levin L, Carrasco L, Kazemi A, et al. Enhancement of the fibula free flap by alveolar distraction for dental implant restoration: report of a case. Facial Plast Surg 2003;19:87–94 11. Jones NF, Swartz WM, Mears DC, et al. The ‘‘double barrel’’ free vascularized fibular bone graft. Plast Reconstr Surg 1988;81:378–385 12. Siciliano S, Lengele´ B, Reychler H. Distraction osteogenesis of a fibula free flap used for mandibular reconstruction: preliminary report. J Craniomaxillofac Surg 1998;26:386–390 13. Mathes SJ, Nahai F. Reconstructive Surgery. Principles, Anatomy and Technique. Fibula Flap. London, UK: Churchill Livingstone; 1997:1353–1370 14. Schmelzeisen R, Neukam FW, Shirota T, et al. Postoperative function after implant insertion in vascularized bone grafts in maxilla and mandible. Plast Reconstr Surg 1996;97:719–725
#
2015 Mutaz B. Habal, MD
Copyright © 2015 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
Evaluation of Bone Height of the Free Fibula Flap in Mandible Reconstruction Takaya Makiguchi, MD, PhD, Satoshi Yokoo, DMD, DMSc, Kazunobu Hashikawa, MD, PhD,y Hidetaka Miyazaki, DDS, PhD, and Hiroto Terashi, MD, PhDy Background: Use of a vascularized free fibula flap has become a
preferred method of mandible reconstruction after oncologic surgical ablation. Despite its many advantages, the low vertical height of the graft is a potential drawback and severe long-term atrophy of fibular bones may cause stress fracture and is disadvantageous for osseointegrated dental implants and facial contours. Therefore, it is important to investigate the degree of resorption based on the fibular height and the factors related to resorption over time. The influence of aspects of the intraoperative surgical procedure, such as preservation of a nutrient artery from the peroneal artery to the fibula bone marrow and the number of segmental osteotomies, has not been examined previously. Therefore, the purpose of this study was to examine the change in fibular height and the factors influencing resorption, including those associated with the surgical procedure. Patients and Methods: A retrospective analysis was performed in 19 patients who underwent free vascularized fibular mandibular reconstruction for oncologic surgical defects without radiotherapy. Postoperative Panorex examinations were used to evaluate fibular height, and 7 factors with a potential influence on long-term fibular height were evaluated: age, gender, length of the mandible defect, number of segmental osteotomies, preservation of a direct nutrient artery from the peroneal artery to the fibula bone marrow, length of follow-up, and delayed placement of osseointegrated dental implants. Results: Fibular bone height decreased in 13 patients (68%), was unchanged in 2 (11%), and increased in 4 (21%). Segmental osteotomies and female gender were significant factors promoting fibular bone resorption (P < 0.001 and P < 0.001, respectively), and preservation of a nutrient artery to the bone marrow, male gender, and delayed placement of osseointegrated dental implants were significant factors inhibiting bone resorption (P < 0.01, P < 0.001, and P < 0.05, respectively). Age, length of follow-up period, and length of the mandibular defect showed no significant relationship with bone resorption (P ¼ 0.77, P ¼ 0.78, and P ¼ 0.105, respectively). Conclusion: The results of this study showed that fibular height in mandibular reconstruction can be maintained by preservation of a From the Department of Stomatology and Maxillofacial Surgery, Gunma University Graduate School of Medicine, Gunma; and yDepartment of Plastic Surgery, Kobe University Graduate School of Medicine, Kobe, Japan. Received July 6, 2014. Accepted for publication December 2, 2014. Address correspondence and reprint requests to Takaya Makiguchi, MD, PhD, Department of Stomatology and Maxillofacial Surgery, Gunma University Graduate School of Medicine, 3-39-22, Showa-machi, Maebashi, Gunma 371-8511, Japan; E-mail: [email protected] The authors report no conflicts of interest. Copyright # 2015 by Mutaz B. Habal, MD ISSN: 1049-2275 DOI: 10.1097/SCS.0000000000001509
The Journal of Craniofacial Surgery
direct nutrient artery to bone marrow, avoidance of osteotomies, and delayed placement of osseointegrated dental implants, all of which inhibit fibular bone resorption. Key Words: bone height, bone resorption, fibula flap, mandible reconstruction, risk factor (J Craniofac Surg 2015;26: 673–676)
U
se of a vascularized free fibula flap has become a preferred method of mandibular reconstruction after oncologic surgical ablation1–5 due to advantages of a satisfactory functional and aesthetic outcome, a sufficient bone length for the graft, low donor-site morbidity, and potential use of a 2-team approach in the operation. Use of the fibula for reconstruction of the mandible differs from lower extremity reconstruction. More osteotomies are generally performed to achieve mandibular shape and osseointegrated dental implants are sometimes inserted in the flap. Furthermore, transferred fibular bones in the lower extremity tend to undergo hypertrophy, whereas in the mandible these bones tend to be absorbed.6– 9 Despite its many advantages, the fibular bone vertical height is less than that of the scalp and iliac crest bone flap for the mandible. Severe atrophy of fibular bones may cause stress fracture and may limit placement of a dental implant,10 whereas severe resorption causes aesthetic problems with the contour of the face. These problems make it important to investigate the degree of resorption of the fibular bone mass and factors related to resorption over time. However, there have only been a few retrospective follow-up studies of bone mass and loss of vertical height, with the conclusion that age, follow-up duration, placement of osseointegrated dental implants, radiotherapy, and site of reconstruction are not significantly associated with decreased bone height.7–9 However, there has been no previous study of the effects of factors
FIGURE 1. Measurement of fibular bone resorption. Bone height was measured in the mid-portion of the transferred fibula bone. For an osteotomized fibula flap, bone height was measured at the middle of the distal segment of the fibula. Differences in Panorex magnification were adjusted for by comparison of miniplate measurements. A, Bone height immediately after surgery. B, Bone height at late follow-up.
Volume 26, Number 3, May 2015
673
Copyright © 2015 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
The Journal of Craniofacial Surgery
Makiguchi et al
Volume 26, Number 3, May 2015
TABLE 1. Details of 19 Cases and Fibular Bone Resorption Index (FBRI) Patient (n ¼ 19) 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19
Gender
Age (yr)
Length of Defects (mm)
No. Osteotomies
Nutrient Artery
Dental Implant
Length of Follow-Up (mo)
FBRI (%)
F M M M F F M F F M F F F M M F F M F
55 65 46 64 51 58 71 45 56 65 61 27 65 64 66 35 67 52 68
78 115 67 77 89 55 66 145 88 84 107 51 55 89 83 110 54 83 96
0 2 0 0 0 0 0 2 1 0 1 1 0 1 0 0 0 1 1
Preservation — Preservation Preservation — Preservation — — — Preservation — — Preservation — — — Preservation — —
Placement — Placement — — — — Placement — — — — — — — Placement — — —
115 18 28 12 22 12 16 77 24 12 17 39 62 15 16 13 17 21 25
0 33 11 5 0 8.3 7.7 38 24 5.9 24 20 5.3 13 6.3 6.3 7.7 13 31
M, male; F, female.
related to intraoperative surgical procedures, such as preservation of a direct nutrient artery from the peroneal artery to the fibula bone marrow and performance of segmental osteotomies. In other words, no previous issue reported absorption of reconstructed fibula, based on differences of blood supply for it. Therefore, the purpose of this study was to determine the influence of such factors on the change in fibular height and bone resorption.
PATIENTS AND METHODS A retrospective analysis was performed in 26 patients who underwent vascularized free fibula flap mandible reconstruction after oncologic resection requiring segmental mandibulectomy between 1995 and 2012 at Kobe University Graduate School of Medicine and Gunma University Graduate School of Medicine. Panorex examinations were used to evaluate fibular height after segmental mandibulectomy. Of these patients, 19 with at least 12 months of follow-up and without radiotherapy were included in this study. Seven factors with a potential influence on long-term fibular height were evaluated: age, gender, length of mandibular defect, number of segmental osteotomies (excluding the ends of the graft), preservation of a direct nutrient artery from the peroneal artery to the fibula bone marrow, length of follow-up, and delayed placement of osseointegrated dental implants. The fibular bone resorption index (FBRI) was defined to evaluate the extent of bone resorption or hypertrophy (Fig. 1). Negative, positive, and zero values of FBRI indicate resorption, hypertrophy, and no change in fibular bone, respectively. Fixation hardware or a dental implant was used as a reference to prevent measurement errors caused by projection on magnification. Multiple regression
model for multivariate analysis was carried out to identify factors associated with bone resorption using SPSS Statistics 22. A P value of less than 0.05 was considered statistically significant.
RESULTS The patients included 8 males and 11 females, and had a mean age of 56.9 years (range, 27-71 years). Panorex examinations were performed 12 to 115 months postoperatively (mean, 29.5 months). The mean FBRI was 10.4%. Fibular height decreased in 13 patients (FBRI, 38% to 5%), was unchanged in 2 (FBRI, 0%), and increased in 4 (FBRI, þ6.3% to þ11%) (Tables 1, 2; Figs. 2, 3).
TABLE 2. Fibular Bone Resorption Index (FBRI)
FBRI > 0 (hypertrophy) FBRI ¼ 0 FBRI < 0 (resorption) All
674
No. Cases
FBRI Range (Mean)
4 2 13 19
þ6.3% to þ11% (þ7.8%) 0% 38% to 5% (17.6%) 38% to þ11% (10.4%)
FIGURE 2. Results from the case with most absorption (FBRI, 33%). Panorex examination immediately after surgery (A) and at 77 months after surgery (B). The patient was a 45-year-old female in whom 2 segmental osteotomies were performed. Cutting of the nutrient artery was required in the reconstruction stage.
#
2015 Mutaz B. Habal, MD
Copyright © 2015 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
The Journal of Craniofacial Surgery
Volume 26, Number 3, May 2015
Bone Height of the Free Fibula Flap
strongly with fibular resorption, whereas preservation of a nutrient artery to the fibula marrow inhibited resorption (Figs. 4, 5). Osseointegrated dental implants were placed in 2 of 4 patients in whom hypertrophy of the fibula bone occurred, and this procedure may be linked to bone hypertrophy.
DISCUSSION
FIGURE 3. Results from the case with most thickening (FBRI, þ11%). Panorex examination immediately after surgery (A) and at 28 months after surgery (B). The patient was a 46-year-old male who received delayed placement of osteointegrated dental implants. The nutrient artery to the fibula was preserved.
Zero to two segmental osteotomies were performed per patient, including 1 in 6 patients and 2 in 2 patients. Four patients had delayed placement of osseointegrated dental implants. The length of mandibular defects ranged from 51 to 145 mm (mean, 83.8 mm). A nutrient artery direct to the fibula bone was preserved in 7 patients, whereas this artery had to be cut at the reconstruction stage in 12 patients because of a problem with the length of the pedicle. No stress fracture was observed and bony union was attained in all patients in the follow-up period. Segmental osteotomies of the fibula flap and female gender were significant factors associated with fibular bone resorption (P < 0.001 and P < 0.001, respectively), and preservation of the nutrient artery to the fibula marrow, male gender, and delayed placement of osseointegrated dental implants were significantly associated with inhibition of fibular bone resorption (P < 0.01, P < 0.001, and P < 0.05, respectively). Age and length of followup and length of the mandibular defect showed no significant association with a change in bone resorption (P ¼ 0.77, P ¼ 0.78, and P ¼ 0.105, respectively) (Table 3). Among factors related to intraoperative surgical procedures, the number of segmental osteotomies of the fibula flap correlated
Use of a vascularized free fibular flap is an approved technique for mandibular primary reconstruction after oncologic resection requiring segmental mandibulectomy.1– 5 However, low fibular height is sometimes a problem for insertion of implants. This problem can be resolved using the ‘‘double-barrel’’ technique or vertical distraction osteogenesis, but the first of these approaches is restricted in terms of the extent of reconstruction and the second requires a long time.11,12 We found a mean FBRI of 10.4% in mandibular reconstruction, consistent with previous results showing retention of fibular height.7–9 Disa et al8 concluded that the height of the transferred fibula is maintained in most patients regardless of age, site of reconstruction, length of mandible defect, radiation, follow-up duration, and placement of osseointegrated dental implants. In their study, the mean resorption rate of less than 10% was a good result, but in 2 cases, the fibular height decreased by 22% and 33%, respectively. In our study, in 6 cases, absorption rates were also greater than 20% and FBRI of the most absorbed case was 38%. It is important to evaluate the cause of these high resorption rates. Therefore, we examined the effects of intraoperative surgical procedures, including the number of segmental osteotomies and preservation of a nutrient artery to the fibula bone marrow. These factors have not been examined in previous reports. In other words, a novel point of the article is to evaluate the fibula absorption, based on differences of blood supply for reconstructed fibula. The fibular bone flap receives blood supply from nutrient arteries that connect directly to fibular bone marrow from the peroneal artery, which is bifurcated at about one-third proximal to the end of the fibula and has many periosteal branches at distal sites (Fig. 6).13 Blood flow through a cross-section of the fibula decreased after cutting the nutrient artery to the bone marrow by our experience (Fig. 7). It is generally believed that the nutrient arteries provide the dominant blood supply to the fibula, but the periosteal branches may also supply blood to the fibular bone because the distal osteotomized bone segment of the fibula free flap was not necrotic and bony union with an adjacent normal mandible was attained without a nutrient artery. That is, free fibula flap could take if only periosteal branches would be preserved. However, our results indicate that segmental osteotomies of the fibula bone flap correlate strongly with fibular bone resorption, whereas preservation of a direct nutrient artery to the fibula bone marrow inhibits resorption. That is, the blood supply to the fibula bone marrow from the nutrient artery plays an important role in postoperative bone remodeling after flap survival. Thus, to inhibit fibular resorption, it is important to preserve the direct nutrient artery to the fibula, in contrast to findings in previous reports.7,8
TABLE 3. Factors Influencing Fibular Bone Resorption (Result of Multiple Regression Model for Multivariate Analysis) Factors Promoting Resorption (P < 0.05) Osteotomies of fibula (P < 0.001) Female gender (P < 0.001)
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2015 Mutaz B. Habal, MD
Factors Inhibiting Resorption (P < 0.05)
No Relationship With Resorption (P > 0.05)
Preserving nutrient artery (P < 0.01) Male gender (P < 0.001) Osteointegrated dental implant (P < 0.05)
Aging (P ¼ 0.77) Length of follow-up (P ¼ 0.78) Length of defects (P ¼ 0.105)
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Copyright © 2015 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
Makiguchi et al
The Journal of Craniofacial Surgery
Volume 26, Number 3, May 2015
FIGURE 7. Blood flow in a cross-section of the fibula before (A) and after (B) cutting the nutrient artery to the fibula bone marrow. After cutting the nutrient artery, blood flow in the fibula decreased.
FIGURE 4. Relationship of the number of osteotomies with FBRI. The number of segmental osteotomies of the fibula bone flap correlated strongly with fibular bone resorption.
dental implants in the fibula bone contribute to mastication ability, as pointed out by Schmelzeisen et al.14 The length of the follow-up period was not a significant factor in bone resorption in the current study, which included patients with at least 12 months of follow-up. Disa et al also found that the duration of follow-up was not a significant factor determining bone height based on a follow-up period of at least 24 months.7,8 Collectively, these studies demonstrate that fibular bone height does not change significantly in 12 to 24 months after the operation. In conclusion, our evaluation of factors with a potential influence on fibular bone in mandibular reconstruction showed that preservation of a nutrient artery to bone marrow, avoidance of osteotomies, and delayed placement of osseointegrated dental implants will inhibit bone resorption and maintain the fibular height.
REFERENCES
FIGURE 5. Relationship between preservation of a direct nutrient artery to bone marrow and FBRI. Large negative FBRI values were found for cases in which a nutrient artery was not preserved.
We also found that delayed placement of osseointegrated dental implants correlated with inhibition of bone resorption. Pressure from the tongue, lip, maxillary teeth, and food are transmitted to fibular bone via dental implants, and this intermittent kinetic load might contribute to bony formation. However, fibular bone and surrounding tissue such as the skin paddle of the fibular flap do not have an occlusal sensation. This makes it unclear if osseointegrated
FIGURE 6. Vascular anatomy of fibular bone. The fibula bone flap receives blood supply from nutrient arteries to the fibula bone marrow from the peroneal artery, which is bifurcated about one-third proximal to the end of the fibula and has many periosteal branches in the distal portion. The figure was modified from Mathes and Nahai.13
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2015 Mutaz B. Habal, MD
Copyright © 2015 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
