Assessment of bone grafts placed within an oral and maxillofacial training programme for implant rehabilitation
Dr Arun Chandu
Department of Oral and Maxillofacial Surgery
Royal Dental Hospital of Melbourne
720 Swanston Street
Carlton VIC 3053
Background: This study aimed to review the survival of bone grafting procedures, performed by surgical trainees and assess factors affecting survival of these bone grafts as an adjunct to implant rehabilitation.
Methods: Data were collected from patients between 2003 and 2009 receiving bone grafting. Graft failure was defined as any complete or partial graft loss, graft which had to be removed or regrafted, or was unable to have an implant placed. Implant survival rates were not assessed in this study.
Results: Seventy-five patients received 86 bone grafts over a period of 7 years. Overall graft survival was 87.3% with 7 complete graft failures (8.1%) and 3 partial graft failures (4.6%). All failed grafts were of the block graft type, predominately in the anterior maxilla. The main reason for failure was secondary infection. Other complications occurred in about 27% of patients. Factors significantly increasing the risk of graft failure included use of bone block augmentation (p = 0.001), mixed autogenous/bone substitute grafts (p = 0.007) and diabetes mellitus (p = 0.006). Smoking was not found to affect graft survival.
Conclusions: Good results were found in a series of patients treated in an oral and maxillofacial training programme. Care should be taken in regards to planning block grafts in diabetic patients.
Abbreviations and acronyms:
Cone beam computed tomography
Creutzfeldt Jacob Disease
Royal Dental Hospital of Melbourne
Dental implants are increasingly being inserted to replace missing teeth.1 However, a common problem encountered is insufficient bone volume due to resorption of the alveolus. This problem can be overcome by bone grafting, which can either be performed prior to implant placement or if primary stability can be achieved, then at the time of implant placement.
The use of autogenous bone is often considered as a ‘gold standard’2,3 in regards to grafting in the jaws and is preferred in maxillofacial reconstruction. However, increasingly, due to the unique resorptive properties of the alveolus post extraction, bone substitutes may also be used.4,5 Depending on the size of the area to be grafted, bone can be harvested from a number different areas.6–8 Local bone defects requiring small grafts will often receive grafts harvested from within the oral cavity including the implant site, external oblique ridge, mandibular ramus, mental region, maxillary tuberosity or the anterior nasal spine region.6
Originally, autogenous grafts were preferred because of a decreased risk of rejection and their osteoinductive, osteoconductive and osteogenic properties.9 Most graft materials are osteoconductive and vary in osteoinductive potential. However, osteogenesis appears to be unique to autogenous bone grafts.7 This osteogenic potential is thought to be derived from precursor cells as few osteoblasts survive the transplantation process.10 For sinus lift procedures, Merkx et al.11 found that autogenous bone grafts resulted in the greatest amount of bone found after a 4–6 month healing period as compared to hydroxyapatite or bovine bone mineral. Using histomorphometric analysis, the autogenous bone grafts group has been found to have higher amounts of vital bone at the recipient site,12 and higher total bone volume than bone substitute material.3 The disadvantage of autogenous grafts is in having an additional surgical site and hence the risk of donor site morbidity.13–15
However, over recent years bone substitutes including bovine bone are increasingly being used to augment osseous defects, with good results,5,8,16 and with no difference in the survival of implants placed into sites grafted with various bone substitute material.17 Bone substitute materials have slower rates of resorption which may help maintain graft volume18 but they are not osteogenic19 and can result in less vital bone.12 There is a theoretical risk with bovine bone of Creutzfeldt Jacob Disease (CJD) transmission. However, this is considered to be very low,20 although iatrogenic transmission has been reported with the use of some medical products.21 Acknowledgement of this risk has been made but no case of transmission of infectious diseases was described in the studies reviewed by Nkenke et al.17
An important part of oral and maxillofacial surgical training is dental implant surgery and oral rehabilitation. In Melbourne, Australia, trainees obtain a significant proportion of this training at the Department of Oral and Maxillofacial Surgery, the Royal Dental Hospital of Melbourne (RDHM). There has been a steady increase in the number of bone graft procedures at the RDHM as the area of implantology develops, from 3 procedures in 2003 to over 17 in 2009 and 13 within the first 6 months of 2010. A recent study by Smith et al.1 confirmed the success of implants placed by trainees in the surgical training programme. However, there are no studies assessing the outcomes of bone grafts placed in an oral and maxillofacial training programme. The aim of this study was to evaluate the outcomes of the bone grafts placed to facilitate implant placement and to assess factors affecting the survival of these grafts.
Materials and methods
This was a retrospective audit of treatment outcomes of patients who have had bone grafts consecutively placed between 2003 to 2009 in the Department of Oral and Maxillofacial Surgery at the RDHM. The RDHM provides general and specialist dental treatment for those patients who are health care card holders in the state of Victoria. The Department of Oral and Maxillofacial Surgery is an integral part of the multidisciplinary implant programme at the hospital, which is run in conjunction with the Melbourne Dental School at the University of Melbourne. Patients are initially referred for assessment to the implant clinic and a treatment plan derived.1 Once patients are accepted into the implant treatment programme, those patients requiring bone grafting either prior or during implant placement are then referred to Oral and Maxillofacial Surgery.
All patients who have undergone bone grafting procedures in the department during the review time were included for analysis. Procedures included alveolar augmentation prior to or during implant placement. Data were excluded from the analysis if the patient had bone augmentation under the care of another specialist department or the procedure was performed in another hospital. The RDHM has day surgery facilities only and those patients with serious medical comorbidities such as significant cardiovascular or pulmonary disease, insulin dependent diabetes or patients who require overnight admission were referred to other maxillofacial units with inpatient facilities.1 Patients were also excluded if the surgery was not primarily carried out by a surgical trainee. Accredited trainees at levels of basic and advanced surgical training performed all these procedures. This study was approved by the Human and Research Ethics Committee of the RDHM.
Those patients requiring both vertical and horizontal bone augmentation were treated with block grafting. Block grafts were secured with titanium screws (Osteomed, Texas, USA) for fixation. Particulate grafts were used preoperatively for sinus lift procedures, ridge split procedures or in situations where simultaneous primary grafting and implant placement such as closed or open sinus lifts, or where reconstruction of minor bone deficiencies were required.
Surgery for all patients was performed under general anaesthesia in the day surgery unit. All procedures were carried out by surgical trainees under the supervision of a consultant oral and maxillofacial surgeon. Standard surgical protocol for procedures included sterile preparation and draping of patients for surgery, intravenous antibiotics (penicillin or cephazolin) and dexamethasone on induction, postoperative course of antibiotics and analgesia. Bone grafts were harvested from various intraoral sites which were assessed through preoperative cone beam computed tomography (CBCT) with site selection on an individual patient basis. Donor sites included the mandibular ramus, chin, maxillary tuberosity, anterior nasal spine, bone from the implant osteotomy site or from another surgical extraction site being performed at the same time. During all procedures, a bone catcher (Innova Technologies Corporation, Toronto, Canada) was used. Particulate grafts were either taken with the use of a drill, rongeur or bone scraper (Ebner-Salvin Dental, North Carolina, USA; Biomet 3i, NSW, Australia). Some particulate grafts were mixed with bone substitute material (Bio-Oss, Geistlich Biomaterials, Wolhusen, Switzerland; or MIS 4Bone, MIS, Melbourne, Australia). Collagen membranes were used for all particulate grafts (Bio-Gide, Geistlich Biomaterials, Wolhusen, Switzerland).
Patients were reviewed postoperatively at 2 weeks and 3 months, with further reviews at 6 months if required. Assessment of graft success was made at 3 months, prior to the decision to proceed with implant placement. For those with bone grafting prior to implant placement, patients were examined clinically and underwent CBCT examination for assessment of bone volume and treatment planning prior to implant placement. For those patients having simultaneous graft with implant placement, graft success evaluation was performed through orthopantomogram examination and clinical assessment. Orthopantomogram examination was used for assessment of bone in-growth into the implant threads. Further CBCT examination was reserved for those patients with clinical evidence of infection or inflammation, discolouration or thinning of the mucosa overlying the implant or obvious fenestration of the implant threads through the mucosa and presence of draining sinuses. CBCT examination was only used in these circumstances and not routinely for all patients having simultaneous implant and bone graft placement due to issues of cost and unnecessary radiation dosage.
Patients were identified using hospital databases. The patients’ records were obtained and screened to identify patients who fulfilled the inclusion criteria. The records of patients who were suitable for the study were reviewed and data were recorded in a secure spreadsheet.
The primary outcome variable was bone graft failure, defined as either complete or partial graft loss or any graft that had to be removed or regrafted for any reason or if an implant was unable to be placed in the grafted site without additional graft procedures. Other variables recorded included: graft variables (type of graft, site of graft, complications); patient demographic data; and health variables (smoking status, diabetes, osteoporosis, bisphosphonate use, immunosuppression or other significant medical history).
All data were assessed statistically using SPSS version 18 (IBM Corporation, Somers, NY, USA). Data were presented in a descriptive fashion. Assessment of factors affecting graft survival was performed using chi-square tests in a 2 × 2 cross-tabulation. A p value of less than 0.05 was taken as being significant.
Seventy-five patients who received 86 bone grafts (average of 1.16 bone graft per patient) were included for analysis. The mean age for these patients was 37 years (range 18–77). Forty-nine female patients received 54 bone grafts while 36 males received 42 bone grafts. Twenty-one per cent of patients were smokers, 5.3% were ex-smokers, 1.3% suffered from diabetes mellitus while 2.7% were on oral corticosteroids.
Of the 86 bone grafts, 41 (47.6%) were particulate grafts while 45 (52.3%) were block grafts. Autogenous bone was used in 64 (74.4%) grafts with 4 (4.7%) bone substitute grafts and 18 (20.9%) a combination of autogenous and bone substitute material. The various donor sites for autogenous grafts are shown in Table 1. The bone substitute material used was Bio-Oss (91.3%) and MIS ‘4bone’ (8.7%). The different types of surgical grafting procedures used are shown in the Table 2.
Table 1. Donor sites used for autologous bone grafts
|No. of patients |
(% of patients)
|35 (41.7%)||18 (21.4%)||20 (23.8%)||1 (1.2%)||8 (9.5%)||2 (2.4%)|
Table 2. Types of graft procedures
|No. of patients |
(% of patients)
|47 (54.6%)||25 (29%)||13 (15.1%)||1 (1.2%)|
In regards to graft failure, there were 10 failures for the group (12.7%) with 7 complete graft failures (8.1%) and 3 partial graft failures (4.6%) were recorded. Of this group, 8 were female and 2 were males with an average age of 31.3 years (range 20–47). All failures occurred with block grafts, predominately in the anterior maxilla (Table 3). Of the 64 patients with autogenous grafts only, 6 failed (9%), while failure occurred in 4 of 18 patients (20%) with a combination of autogenous and non-autogenous grafts. One patient was a smoker and 1 suffered from diabetes mellitus. The remainder of the patients’ medical histories in patients where graft failure occurred were unremarkable. The reason for failure is recorded in Table 4, with the majority of grafts failing due to secondary infection.
Table 3. Graft type and site data for graft failures
|Donor site||Mandibular ramus||8 (80%)|
|Mandibular symphysis||2 (20%)|
|Recipient site||Anterior maxilla||8 (80%)|
|Posterior maxilla||2 (20%)|
Table 4. Reason for graft failure
|Number of failure (out of total of 10) (% of total failure)||6 (60%)||1 (10%)||1 (10%)||2 (20%)|
Patients with failed bone grafts were further reviewed and managed. Management included regrafting for 6 out of the 10 patients in whom the bone graft failed, 1 patient declined regrafting, and 3 patients received simultaneous particulate bone grafting with implant placement).
There were a number of complications recorded in the population group (27.9%). Recipient site complications (18.6%) included 8 patients who had local infection, which were managed with broad spectrum oral antibiotics. Five patients had wound dehiscence, 1 developed haematoma and 2 had persistent swelling or inflammation. Donor site morbidity (9.3%) included 8 patients with transient sensory impairment of the inferior alveolar nerve.
Assessment of factors affecting bone graft survival found that bone block augmentation (chi-square =10.31, p = 0.001), use of mixed autogenous and bone substitute grafts (chi-square = 7.22, p = 0.007) and diabetes mellitus (chi-square = 7.69, p = 0.006) significantly increased bone graft failure. Anterior recipient site for bone graft placement approached significance with a trend of increased failure rates in the anterior region of the mouth (chi-square = 3.18, p = 0.07).
Bone grafting procedures for maxillofacial augmentation have been described extensively in the literature and require specific training in order to be performed. This is an important area which forms part of the maxillofacial surgery training curriculum,22 where trainees learn to perform these procedures under supervision. There are no studies at present which look at the success of bone augmentation related to the level of surgeon experience or outcomes of bone grafts placed by surgical trainees. However, there are a few studies that have assessed the outcomes of implants placed by trainees. Smith et al.1 demonstrated a good success rate of implants placed by trainees in a surgical training programme that were comparable to the literature. Melo et al.23 found similarly that there was no statistically significant difference in survival rates of implants related to different levels of training, but no such study exists in relation to bone grafting procedures.
The purpose of alveolar augmentation is to increase the alveolar bone volume sufficiently to allow primary stability and to ensure that the implant is surrounded by bone. Autogenous grafts are either taken intra or extraorally.8 Intraoral donor sites have relatively low morbidity and costs relative to other sites such as rib, hip and calvaria grafts. Other benefits include proximity of donor and recipient site, no cutaneous scar, and reduced discomfort.8,24 All grafts placed in the present study have been harvested from intraoral donor sites. Increasingly, bone substitutes are also being used due to slower resorption rates,25,26 allowing a sufficient scaffold to maintain graft dimensions.18
The present study demonstrated a 12.7% bone graft failure rate. Of these 10 failures, 3 were able to have fixtures subsequently placed with simultaneous bone grafting to replace any graft loss. Our results are consistent with the study by Schwartz-Arad et al.27 looking at the success of intraoral autogenous block graft for alveolar ridge augmentation. These authors reported a graft failure rate of 12.5%.27 However, this is a higher failure rate than that reported by Chiapasco et al.4 assessing grafted atrophic maxilla from various donor sites. In that study only 4 out of 692 patients did not receive dental implants due to loss of the graft prior to implant placement. Chiapasco et al.8 also reviewed bone augmentation and found a partial loss of graft in 3.3% of cases while a total loss of the graft occurred in 1.4% of cases for onlay bone grafts with the majority related to the extensively reconstructed atrophic maxilla.
In the present study, those patients who had block grafts had a significantly higher failure rate than those that had particulate grafts, with all grafts failing being of the block variety. Block grafts are typically cortical9 or corticocancellous in nature and preserve bone volume better than particulate grafts.3 However, revascularization in mandibular block grafts is slow.28,29 A systematic review by Wallace et al.30 also found block grafting resulted in a lower implant survival rate (83.3%) than particulate grafts (92.3%).
The addition of bone substitute to autogenous grafts has been found to accelerate bone formation31,32 but, interestingly, the present study found a higher rate of graft failure in patients who received mixed autogenous and bone substitute grafts. This is in contrast to De Vicente et al.33 who assessed the success of composite autogenous grafts with bovine bone for implant survival (98.9%) and concluded a predictable outcome regarding the amount of bone formation. Also, a study by Cordaro et al.34 assessed block grafts alone compared to block grafts with bovine bone and collagen membrane and found no difference in the success rates of these grafts, but there was a higher complication rate in the later group.
Smoking and diabetes mellitus are risk factors that significantly affect the outcomes of bone grafts.27,35 Smoking has previously been found to compromise healing after mucogingival surgery.9,13 Studies have demonstrated significantly higher failure rates of bone augmentation and increased incidence of postoperative complications in smokers.27,36 Lindfors et al.36 reported success rates of 62.5% in smokers compared to 94.7% in non-smokers. Levin et al.35 reported 4 out of 12 onlay bone grafts in smokers had major complications with graft mobility, and one graft exposure. However, Wallace et al.30 concluded that there was insufficient data to statistically evaluate the effects of smoking which is consistent with the findings of the present study. While smoking may be one risk factor, diabetes is another factor which may affect grafting outcomes. Schwartz-Arad et al.27 also reported that 4 diabetic patients in their study had complications after onlay bone grafts and 3 had failures, which is consistent with the current study where diabetes was found to be a significant factor in the outcomes of bone grafts.
A major concern in using autogenous bone is donor site morbidity.14,15,37,38 In this present study a small number of donor site complications, including 8 patients (9.3%) with transient sensory nerve impairment was found, which is comparable to that reported in the literature.13,39 Studies have reported increased morbidity related to chin donor sites.8,13,14,37 Acocella et al.28 reported paraesthesia in 8.3% of patients having mandibular ramus bone harvesting as compared with 16% for the chin as the donor site. Nkenke et al.13 in a prospective study of 20 patients reported 8 patients with temporary sensory impairment from grafts taken from the chin, while Becktor et al.39 reported only 1 of their 61 patients with paraesthesia from particulate grafts from the mandibular ramus. Minor complications such as swelling, haematoma, transient tooth sensitivity, have also been reported but often resolve without sequelae.38 The present study found a number of complications at the recipient site. Some of these contributed to the failure of grafts, in particular infection at the recipient site. These were slightly higher than that reported by Becktor et al.39 who found that 3 of 61 (5%) patients developed local infection of the recipient site. Like any other procedure, bone augmentation procedure carries some risk of complications. However subjectively, Andersson40 found that patients were generally satisfied with treatment and the outcome of autogenous bone grafting from intraoral site prior to implant treatment.
In conclusion, this study has found good survival rates for bone grafts placed in an oral and maxillofacial surgical training programme as an adjunct to implant placement. A number of different factors were identified which contributed to graft failure, particularly block grafts, mixed grafts and diabetes.