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Table 1.  
Characteristics of Patients Undergoing Primary and Secondary Dental Implantation
Characteristics of Patients Undergoing Primary and Secondary Dental Implantation
Table 2.  
Patient-Related and Implant-Related Complicationsa
Patient-Related and Implant-Related Complicationsa
Table 3.  
Characteristics of Patients With Implant Failures
Characteristics of Patients With Implant Failures
Table 4.  
Characteristics Associated With Implant Failure
Characteristics Associated With Implant Failure
1.
Disa  JJ, Cordeiro  PG.  Mandible reconstruction with microvascular surgery.  Semin Surg Oncol. 2000;19(3):226-234.PubMedArticle
2.
Williams  RL.  Product-limit survival functions with correlated survival times.  Lifetime Data Anal. 1995;1(2):171-186.PubMedArticle
3.
Lee  E, Wei  LJ, Amato  D, Leurgans  S. Cox-type regression analysis for large numbers of small groups of correlated failure time observations. In: Klein  J, Goel  P, eds.  Survival Analysis: State of the Art. Vol 211. Amsterdam, the Netherlands: Springer; 1992:237-247.
4.
Hidalgo  DA.  Fibula free flap: a new method of mandible reconstruction.  Plast Reconstr Surg. 1989;84(1):71-79.PubMedArticle
5.
Urken  ML, Buchbinder  D, Costantino  PD,  et al.  Oromandibular reconstruction using microvascular composite flaps: report of 210 cases.  Arch Otolaryngol Head Neck Surg. 1998;124(1):46-55.PubMedArticle
6.
Chiapasco  M, Biglioli  F, Autelitano  L, Romeo  E, Brusati  R.  Clinical outcome of dental implants placed in fibula-free flaps used for the reconstruction of maxillo-mandibular defects following ablation for tumors or osteoradionecrosis.  Clin Oral Implants Res. 2006;17(2):220-228.PubMedArticle
7.
Roumanas  ED, Chang  TL, Beumer  J.  Use of osseointegrated implants in the restoration of head and neck defects.  J Calif Dent Assoc. 2006;34(9):711-718.PubMed
8.
Rohner  D, Kunz  C, Bucher  P, Hammer  B, Prein  J.  New possibilities for reconstructing extensive jaw defects with prefabricated microvascular fibula transplants and ITI implants [in German].  Mund Kiefer Gesichtschir. 2000;4(6):365-372.PubMedArticle
9.
Jaquiéry  C, Rohner  D, Kunz  C,  et al.  Reconstruction of maxillary and mandibular defects using prefabricated microvascular fibular grafts and osseointegrated dental implants: a prospective study.  Clin Oral Implants Res. 2004;15(5):598-606.PubMedArticle
10.
Sclaroff  A, Haughey  B, Gay  WD, Paniello  R.  Immediate mandibular reconstruction and placement of dental implants. At the time of ablative surgery.  Oral Surg Oral Med Oral Pathol. 1994;78(6):711-717.PubMedArticle
11.
Salinas  TJ, Desa  VP, Katsnelson  A, Miloro  M.  Clinical evaluation of implants in radiated fibula flaps.  J Oral Maxillofac Surg. 2010;68(3):524-529.PubMedArticle
12.
Urken  ML, Buchbinder  D, Weinberg  H, Vickery  C, Sheiner  A, Biller  HF.  Primary placement of osseointegrated implants in microvascular mandibular reconstruction.  Otolaryngol Head Neck Surg. 1989;101(1):56-73.PubMed
13.
Wei  FC, Santamaria  E, Chang  YM, Chen  HC.  Mandibular reconstruction with fibular osteoseptocutaneous free flap and simultaneous placement of osseointegrated dental implants.  J Craniofac Surg. 1997;8(6):512-521.PubMedArticle
14.
Hidalgo  DA.  Aesthetic improvements in free-flap mandible reconstruction.  Plast Reconstr Surg. 1991;88(4):574-585.Article
15.
Shen  YF, Rodriguez  ED, Wei  FC, Tsai  CY, Chang  YM.  Aesthetic and functional mandibular reconstruction with immediate dental implants in a free fibular flap and a low-profile reconstruction plate: five-year follow-up.  Ann Plast Surg. 2015;74(4):442-446.PubMedArticle
16.
Chang  YM, Tsai  CY, Wei  FC.  One-stage, double-barrel fibula osteoseptocutaneous flap and immediate dental implants for functional and aesthetic reconstruction of segmental mandibular defects.  Plast Reconstr Surg. 2008;122(1):143-145.PubMedArticle
17.
Ruhin  B, Menard  P, Ceccaldi  J, Dichamp  J, Bertrand  JC.  Double-barrel fibular free flap for mandibular reconstruction: beneficial alternative for dental implanted rehabilitation (5 cases).  Rev Stomatol Chir Maxillofac. 2006;107(5):338-344.Article
Original Investigation
May/Jun 2016

Evaluation of Clinical Outcomes of Osseointegrated Dental Implantation of Fibula Free Flaps for Mandibular Reconstruction

Author Affiliations
  • 1Department of Otolaryngology–Head and Neck Surgery, Washington University School of Medicine, St Louis, Missouri
  • 2Department of Otolaryngology–Head and Neck Surgery, Mayo Clinic, Rochester, Minnesota
  • 3Division of Oral and Maxillofacial Surgery, Mayo Clinic, Rochester, Minnesota
JAMA Facial Plast Surg. 2016;18(3):201-206. doi:10.1001/jamafacial.2015.2271
Abstract

Importance  Dental implantation has been used for oral rehabilitation to improve cosmesis and function.

Objective  We aim to evaluate the clinical outcomes and success rates of primary and secondary dental implant placement in vascularized fibula bone grafts used for segmental mandibulectomy defects.

Design, Setting, and Participants  A retrospective review was performed between November 2005 and July 2014 on all patients undergoing both fibula free tissue reconstruction of mandibular defects and endosseous dental implantation at an academic tertiary care referral hospital.

Interventions  Either primary (n = 20) or secondary (n = 26) dental implantation of the fibula was performed.

Main Outcomes and Measures  Timing of implantation, location of implants, history of tobacco, alcohol, and radiation, reason for mandibulectomy, and outcomes related to these parameters.

Results  Forty-six patients (31 males, 15 females; mean age, 58.0 years) underwent dental implantation to the fibula graft. A total of 227 implants were placed, with a mean of 5 implants per patient (range, 2-7). Of these, 44 were placed into native mandible and 183 into fibula flap. Twenty patients underwent primary implantation and received 96 implants, while 26 patients underwent secondary implantation and received 131 implants. There were no flap failures and 22 implant-related complications in 16 patients (implant failure, n = 10; granulation or soft-tissue overgrowth, n = 6; exposed bone around implant, n = 6). An implant failure occurred in 10 patients (22%) resulting in removal of 15 implants. Nine of these patients underwent successful dental rehabilitation, 5 without further implantation, and 4 with replaced implants. One patient was not rehabilitated secondary to failed implantation. Therefore, there was a 93% overall implant survival rate (n = 212) and 98% overall implant-supported prosthesis success rate (n = 45) at a mean follow-up of 22 months. There was no difference in implant survival between primary (94%) (n = 90) and secondary (93%) (n = 122) implantation. Neither a history of preimplant or postimplant radiation exposure nor the diagnosis of osteoradionecrosis affected implant survival.

Conclusions and Relevance  Osseointegrated dental implantation is a relatively safe procedure with few complications. Vascularized fibula grafts are a suitable method of mandibular reconstruction and are amenable to successful primary and secondary endosseous implantation.

Level of Evidence  4.

Introduction

Disease or trauma of the mandible requiring segmental mandibulectomy often requires vascularized bone grafts such as fibula free flaps to restore the natural arch of the mandible. There are multiple bony reconstruction donor sites that have proven acceptable for segmental mandibular reconstruction.1 Of these, the fibula has become an important donor site to reconstruct large mandibular defects as well as to provide enough bone stock for dental implantation.

Although fibula free tissue reconstruction alone can restore the natural arch of the mandible as well as restore a natural facial contour, patients are still left with a potential cosmetic and functional deficit. Primary and secondary dental implantation has been used for oral rehabilitation. This results in improved function by allowing the patient to masticate using an implant-supported fixed prosthesis. Patient aesthetics are also improved by providing lip support and aiding in oral competence.

Despite the improved functional and cosmetic outcomes resulting from dental implantation, implants are not routinely placed in many centers owing to physician preference, access to a team equipped for oral rehabilitation, and financial cost. Because of this, reports of dental implantation of fibula free flaps in mandibular reconstruction are few and with low patient numbers. In addition, the implications of the timing of implant placement are not yet well known and have not specifically been addressed.

Therefore, we aim to evaluate the clinical outcomes of dental implants in vascularized fibula bone grafts used for segmental mandibulectomy defects in a larger cohort of patients. Secondarily, we aim to evaluate the timing of osseointegrated implants placed primarily and secondarily.

Methods

After approval by the Mayo Clinic institutional review board, a retrospective review was performed between November 2005 and July 2014 on all patients undergoing both fibula free tissue reconstruction of mandibular defects and endosseous dental implantation at an academic tertiary care referral hospital. Patient written informed consent was waived.

Primary implantation was defined as endosseous dental implants placed simultaneously with the fibula free tissue transfer reconstruction. Secondary implantation was defined as dental implantation at a date after the fibula free tissue transfer reconstruction.

Procedure

All patients underwent vascularized fibula free tissue reconstruction of a segmental mandibulectomy defect. The fibula was routinely plated in a position to recreate the lower border of the mandible. Typically, 2 fixation screws were applied per mandibular segment. This allowed for adequate spacing to properly align and place the appropriate number of implants. After the fibula was plated to the native mandible, dental implants were placed by the oral and maxillofacial surgeon. Once the dental implants were placed, the cutaneous paddle was draped over the implants and sewn into the oral cavity, and the microvascular anastomosis was completed. Patients who underwent secondary implantation had ideally a minimum 3-month period of healing after the initial reconstruction to allow for bony union across the osteotomy sites. Patients undergoing primary implantation were implanted at the time of the segmental mandibulectomy and fibula free tissue reconstruction. After implantation, patients typically had a 3-month waiting period for osseointegration. The implants would then be uncovered, with either healing abutments alone or multiunit abutments and an acrylic stent fabricated and placed intraoperatively. The stent was required in most patients to help conform the soft tissue and to prevent soft-tissue overgrowth secondary to the height limitations of standard healing abutments. The stent remained in place for a minimum of 1 month and was then replaced with a final implant-retained prosthesis.

Outcomes by risk factor of interest were evaluated using simple tabulation. Time from implantation to implant failure was calculated using Kaplan-Meier survival function estimates. Standard error was adjusted for clustering of implants within patients, as described by Williams.2 Hazard ratios were used to test for association using Sandwich estimator to account for clustering of implants within patients.3

Results
Patient Characteristics

A total of 162 patients underwent fibula free tissue reconstruction of segmental mandibulectomy defects between November 2005 and July 2014. Forty-six of these patients (28.4%) underwent dental implantation to the fibula graft and were included in this study. There were 31 male and 15 female patients with a mean age 58.0 years (median, 61.6 years; range, 16.6-80.3 years). A total of 227 implants were placed, with a mean of 5 implants per patient (range, 2-7). Patient characteristics are further detailed in Table 1.

Timing of Use

The overall median time from implant placement to implant-fixed prosthesis delivery was 32 weeks. The median time was 34.6 weeks for those undergoing primary implantation and 31.1 weeks for those undergoing secondary implantation (P = .73). The overall median time to implant-fixed prosthesis use from free flap was 64 weeks. The median time was 34.6 weeks for those undergoing primary implantation and 75.4 weeks for those undergoing secondary implantation (P < .001).

Complications

There were no flap failures. Five flaps (10.8%) required patient return to the operating room for evacuation of a hematoma. Patient-related and implant-related complications are detailed in Table 2.

Implant Survival

An implant failure occurred in 10 patients (22%) resulting in removal of 15 implants. Characteristics of implant failures are listed in Table 3. Four implants (3 patients) failed in the native mandible, while 11 implants (7 patients) failed in the fibula graft. Failed implants were replaced in 4 patients. One patient was not rehabilitated secondary to failed implantation. The remaining 5 patients were successfully rehabilitated with remaining implants and did not require replacement. Therefore, there was a 93% overall implant survival rate (n = 212) and 98% overall implant-supported prosthesis success rate (n = 45) at a mean follow-up of 29.7 months (range 4.9 to 82.7). The survival rate of implants placed in the native mandible and fibula was 93.2% and 93.4%, respectively. None of the confounding factors evaluated were associated with increased risk of implant failure (Table 4). Of the 13 patients with osteoradionecrosis, 5 implants failed in 3 patients. There were no differences in implant survival between the irradiated and nonirradiated patients or based on timing of irradiation (Table 4).

Patient Survival

At last follow-up, 41 patients were alive (39 alive with no evidence of disease, 2 alive with disease), and 5 patients had died (4 dead of disease, 1 dead of other causes). Of those who had died, an implant-fixed prosthesis was placed an average of 19.5 months prior to death (range, 11.8-30.1 months).

Discussion

Patients undergoing segmental mandibulectomy are left with a defect that results in a significant functional and cosmetic deformity. Bony reconstruction restores the natural arch of the mandible and recreates the aesthetic contour of the mandibular border. The fibula free flap has sufficient bone stock to span large segmental mandibulectomy defects and support osseointegrated implants.4,5

We evaluated 46 patients who underwent fibula free flap reconstruction for segmental mandibulectomy defects and either simultaneous or delayed osseointegrated dental implantation to the vascularized fibula bone flap. The overall implant survival was 93% (n = 212) with a 98% implant-supported prosthesis success rate (n = 45) at a mean follow-up of 29.7 months, which is consistent with previously published reports.57 Implants placed in the fibula graft had survival rates similar to those placed in the native mandible. There were few complications and no flap failures in our study. Granulation tissue and soft-tissue overgrowth near dental implants was the most common untoward event. This has also been described in prior reports.8,9 The survival outcomes and rates of implant-supported prosthesis use were similar in those implanted primarily and secondarily.

The effects of irradiation on the outcomes of dental implants remain controversial. Sclaroff et al10 evaluated the effects of radiation on 22 patients undergoing primary dental implantation of fibula and iliac crest grafts and found no significant differences between those who received radiation therapy and those who did not. On the other hand, when comparing 22 irradiated and 22 nonirradiated patients, Salinas et al11 did not find that irradiation exposure affected implantation success. In the present study, we found a trend toward increased implant failure in irradiated patients, but this was not statistically significant. In addition, radiation exposure did not significantly influence the ability to use an implant-supported prosthesis. When looking specifically at patients who underwent segmental mandibulectomy for osteoradionecrosis (ORN), we did not find significantly lower implant survival than in those without ORN. Therefore, we do not believe that radiation exposure or ORN alone should exclude a patient from undergoing dental implantation; this should remain a case-by-case decision. In our very early experience, we were seeing wound healing difficulties in patients implanted in a delayed fashion secondary to uncovering the bone and interrupting the periosteum within 6 months in patients that were receiving radiation treatment after the fibula free flap. Therefore, we typically wait 6 months after irradiation to place dental implants if the implants are performed in a secondary fashion.

The timing of implantation remains controversial. In properly selected patients, primary implantation allows for better access to the grafted bone to be implanted, eliminates a second operation to place the implants, and allows for oral rehabilitation in a shorter time. Urken et al12 first reported primary dental implantation in 9 patients. They concluded that dental restoration provides an additional step in the rehabilitation of patients undergoing oromandibular reconstruction. Wei et al13 described their experience with patients undergoing primary dental implantation but cautioned that patient selection is important when considering a primary implantation approach. The timing of implantation becomes clinically important when considering the potential decreased life expectancy of those undergoing such procedures for oncologic reasons. We believe it is important to rehabilitate these patients early to provide improved quality of life from a cosmetic and oral function standpoint. The overall time from segmental mandibulectomy to complete dental rehabilitation with an implant-fixed prosthesis was decreased by nearly half in those implanted simultaneously compared with those implanted in a delayed fashion. Although this is an expected finding, it demonstrates that patients can be orally rehabilitated earlier without an increased risk of implant or graft failure. In addition, there is a theoretical cost and safety benefit of primary implantation, requiring only 1 anesthetic administration compared with secondary implantation, which requires a second visit to the operating room.

Timing in the present study was chosen based on patient and surgeon preferences on an individual basis. As our experience has grown, we favor primary dental implantation when feasible. Coordination between multiple specialties is required for primary implantation. This can be difficult when trying to expedite the scheduling of a multidisciplinary procedure in the operating room. Also, it takes additional time to perform the implantation primarily in an already lengthy procedure. In our experience, primary dental implantation added approximately 1 hour to the case length. This brings ischemia time into consideration, although we do not feel this has been an issue in our experience. Finally, the fibula segment length may be an important factor, as placement of implants requires some stripping of periosteum of the fibula graft, which can potentially devascularize short segments that already have minimal periosteum supplying nutrients to the underlying bone. Despite some of these challenges, primary implantation allows a patient to undergo only 1 general anesthetic procedure and earlier dental rehabilitation. It also allows for face-to-face communication between services to optimally place the dental implants in a mutually agreed location within the fibula segments. Therefore, unless contraindications exist, we now favor primary implantation in the majority of our patients.

Chiapasco et al6 raised the concern of fibula graft position as it relates to the native mandible. Since the fibula has a shorter vertical height than the native mandible, it has to be placed either at the lower border of the mandible, which improves cosmesis, or at the upper border of the mandible, which decreases implant height. Placing the graft at the lower border of the mandible offers good aesthetic results for facial contour.4,14 Some authors have performed “double barrel” reconstruction, while others placed the fibula graft in between and filled the lower mandibular border with soft tissue to accomplish both goals.1517 We plated all fibula grafts to the lower border of the native mandible. Although this created a discrepancy between the height of the native mandible and the fibula graft, the patients in our study had good facial contour as well as acceptable implant survival and implant-supported prosthesis results. Our population did not have prosthetic failures or implant failures related to the length after loading of implants. Most of the implant failures were prior to the fabrication of the prosthesis and loading of the implants.

Our study has several limitations. First, it is limited by the number of patients. Despite being one of the largest studies on dental implant placement to free fibula grafts, it still included too few patients to draw definitive conclusions on the variables associated with implant failure. With only 15 implant failures, it is difficult to draw conclusions regarding associations of causes of failure such as implant timing and the effects of radiation. In addition, we did not address the cost of dental rehabilitation. In general, dental implantation is costly, and many patients cannot afford the implants and the prosthesis. Financial cost is the main limitation of dental rehabilitation with an implant-fixed prosthesis in many patients who would otherwise qualify. This further limits the volume of patients available for review and introduces a source of bias on who receives dental implants. Finally, patients were not randomized to the timing of implantation. Therefore, there is a risk of selection bias in regard to who received dental implants as well as the timing of such implants.

Conclusions

Osseointegrated dental implantation is a relatively safe procedure with few complications. In properly selected patients, dental implants may be placed primarily, thus reducing the time to oral rehabilitation. Vascularized fibula grafts are a suitable method of mandibular reconstruction and are amenable to successful primary and secondary endosseous implantation.

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Article Information

Accepted for Publication: December 3, 2015.

Corresponding Author: Eric J. Moore, MD, Department of Otolaryngology–Head and Neck Surgery, Mayo Clinic, 200 First St SW, Rochester, MN 55905 (moore.eric@mayo.edu).

Published Online: February 11, 2016. doi:10.1001/jamafacial.2015.2271.

Author Contributions: Drs Jackson and Moore had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

Study concept and design: Jackson, Arce, Moore.

Acquisition, analysis, or interpretation of data: Jackson, Price, Arce.

Drafting of the manuscript: Jackson, Moore.

Critical revision of the manuscript for important intellectual content: Jackson, Price, Arce, Moore.

Statistical analysis: Jackson, Arce.

Study supervision: Price, Moore.

Conflict of Interest Disclosures: None reported.

Previous Presentation: This article was presented at American Head and Neck Society Annual Meeting at the Combined Otolaryngology Spring Meetings; April 22-23, 2015; Boston, Massachusetts.

References
1.
Disa  JJ, Cordeiro  PG.  Mandible reconstruction with microvascular surgery.  Semin Surg Oncol. 2000;19(3):226-234.PubMedArticle
2.
Williams  RL.  Product-limit survival functions with correlated survival times.  Lifetime Data Anal. 1995;1(2):171-186.PubMedArticle
3.
Lee  E, Wei  LJ, Amato  D, Leurgans  S. Cox-type regression analysis for large numbers of small groups of correlated failure time observations. In: Klein  J, Goel  P, eds.  Survival Analysis: State of the Art. Vol 211. Amsterdam, the Netherlands: Springer; 1992:237-247.
4.
Hidalgo  DA.  Fibula free flap: a new method of mandible reconstruction.  Plast Reconstr Surg. 1989;84(1):71-79.PubMedArticle
5.
Urken  ML, Buchbinder  D, Costantino  PD,  et al.  Oromandibular reconstruction using microvascular composite flaps: report of 210 cases.  Arch Otolaryngol Head Neck Surg. 1998;124(1):46-55.PubMedArticle
6.
Chiapasco  M, Biglioli  F, Autelitano  L, Romeo  E, Brusati  R.  Clinical outcome of dental implants placed in fibula-free flaps used for the reconstruction of maxillo-mandibular defects following ablation for tumors or osteoradionecrosis.  Clin Oral Implants Res. 2006;17(2):220-228.PubMedArticle
7.
Roumanas  ED, Chang  TL, Beumer  J.  Use of osseointegrated implants in the restoration of head and neck defects.  J Calif Dent Assoc. 2006;34(9):711-718.PubMed
8.
Rohner  D, Kunz  C, Bucher  P, Hammer  B, Prein  J.  New possibilities for reconstructing extensive jaw defects with prefabricated microvascular fibula transplants and ITI implants [in German].  Mund Kiefer Gesichtschir. 2000;4(6):365-372.PubMedArticle
9.
Jaquiéry  C, Rohner  D, Kunz  C,  et al.  Reconstruction of maxillary and mandibular defects using prefabricated microvascular fibular grafts and osseointegrated dental implants: a prospective study.  Clin Oral Implants Res. 2004;15(5):598-606.PubMedArticle
10.
Sclaroff  A, Haughey  B, Gay  WD, Paniello  R.  Immediate mandibular reconstruction and placement of dental implants. At the time of ablative surgery.  Oral Surg Oral Med Oral Pathol. 1994;78(6):711-717.PubMedArticle
11.
Salinas  TJ, Desa  VP, Katsnelson  A, Miloro  M.  Clinical evaluation of implants in radiated fibula flaps.  J Oral Maxillofac Surg. 2010;68(3):524-529.PubMedArticle
12.
Urken  ML, Buchbinder  D, Weinberg  H, Vickery  C, Sheiner  A, Biller  HF.  Primary placement of osseointegrated implants in microvascular mandibular reconstruction.  Otolaryngol Head Neck Surg. 1989;101(1):56-73.PubMed
13.
Wei  FC, Santamaria  E, Chang  YM, Chen  HC.  Mandibular reconstruction with fibular osteoseptocutaneous free flap and simultaneous placement of osseointegrated dental implants.  J Craniofac Surg. 1997;8(6):512-521.PubMedArticle
14.
Hidalgo  DA.  Aesthetic improvements in free-flap mandible reconstruction.  Plast Reconstr Surg. 1991;88(4):574-585.Article
15.
Shen  YF, Rodriguez  ED, Wei  FC, Tsai  CY, Chang  YM.  Aesthetic and functional mandibular reconstruction with immediate dental implants in a free fibular flap and a low-profile reconstruction plate: five-year follow-up.  Ann Plast Surg. 2015;74(4):442-446.PubMedArticle
16.
Chang  YM, Tsai  CY, Wei  FC.  One-stage, double-barrel fibula osteoseptocutaneous flap and immediate dental implants for functional and aesthetic reconstruction of segmental mandibular defects.  Plast Reconstr Surg. 2008;122(1):143-145.PubMedArticle
17.
Ruhin  B, Menard  P, Ceccaldi  J, Dichamp  J, Bertrand  JC.  Double-barrel fibular free flap for mandibular reconstruction: beneficial alternative for dental implanted rehabilitation (5 cases).  Rev Stomatol Chir Maxillofac. 2006;107(5):338-344.Article
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