Survival of dental implants placed in autogenous bone grafts and bone flaps in head and neck oncology patients: a systematic review

The use of implants to retain prostheses as part of oral and dental rehabilitation of head and neck (H&N) cancer patients is becoming an increasingly common treatment approach [1‐3]. A number of benefits advocating implant anchorage over conventionally secured prostheses have been proposed [4] but importantly include a significant improvement in the reported quality of life (QoL) of patients [5].

Patients with H&N cancer often undergo ablative surgery with or without surgical reconstruction, radiotherapy and chemotherapy [4, 6]. Both surgical and non-surgical interventions can lead to significant disability, including facial deformity, loss of hard and soft tissue, impaired speech, swallowing and mastication [7]. Oral and dental rehabilitation has conventionally required the use of removable prostheses to obturate defects, to replace missing tissue structures and to restore function and aesthetics. In this patient group, removable prostheses are often poorly tolerated, are difficult for the patient to maintain and frequently fail to fully achieve the intended functional improvement. The use of dental implants has been proposed to enable secure anchorage for prostheses, reduced loading on vulnerable tissues and provide a better functional and cosmetic solution [8].

However, dental implants can only be placed if there is sufficient bone to encase the implant so that a direct interface between the implant surface and bone can be achieved. Frequently following resective surgery, insufficient bone volume remains and bony reconstruction of the surgical defect is required to enable successful dental implant placement [9]. Patients are commonly reconstructed with either a non-vascularised bone graft or a composite free flap. A non-vascularised bone graft is a free piece of non-vascularised bone (or bone substitute) that is placed in the tissues. A free flap is a vascularised piece of bone (pedicled), which is being increasingly used to reconstruct tumour patients.

High ‘survival’ and ‘success’ rates have been reported in the literature for dental implants placed into autogenous bone grafts in healthy patients but notably the success rates remain lower for implants placed into healthy native bone [10, 11]. With the increasing use of complex reconstructive techniques in rehabilitation following H&N cancer and the placement of dental implants into transported bone, there is a need to appraise the highly varied evidence that is currently available in order to help inform clinical decision making.

It is the aim of this systematic review to evaluate the survival of dental implants placed into autogenous bone grafts, in H&N oncology patients.

Studies that met the following criteria where included:

Studies were excluded if they met the following criteria:

The overall implant survival of implants placed into autogenous bone grafts varied highly (both at implant and patient levels) between the included studies ranging from 100% with a mean follow-up of 3.5 years ± 0.3 years in a study by Wang et al. [30] to 54% with a mean follow-up 5.4 years ± 3.2 years by Yerit et al. [16].,(at an implant level) (Table 2).

Eleven studies compared implant survival in autogenous bone grafts to that in native bone within their studies. Nine of these studies (Barrowman et al. [7], Yerit et al. [16], Linsen et al. [17], Fenlon et al. [19], Ch’ng et al. [20], Hessling et al. [28], Watzinger et al. [29], Shaw et al. [31], Klein et al. [32]) reported higher implant failure rates within autogenous bone grafts than those within implants placed into the native bone; however, two studies (Buddula et al. [24], Teoh et al. [26]) reported no significant difference.

Seventeen studies reported on the specific bone graft type (non-vascularised or vascularised) into which the implants were placed. In the remaining three studies (Buddula et al. [24], Fierz et al. [25], Yerit et al. [16]), this distinction was not possible.

Of these 17 studies, 8 studies reported on implant survival in non-vascularised bone grafts and 14 studies reported on implant survival in vascularised bone grafts with 5 studies (Barrowman et al. [7], Hessling et al. [28], Watzinger et al. [29], Shaw et al. [31], Chiapasco et al. [33]), therefore reporting on implant survival in both non-vascularised and vascularised bone grafts within their study (Table 3). Implant survival appears to be higher for those implants placed into vascularised bone grafts in comparison to non-vascularised bone grafts. Of the five studies reporting on both vascularised and non-vascularised bone grafts, three of these studies (Barrowman et al. [7], Watzinger et al. [29], Chiapasco et al. [33]) reported higher implant survival in vascularised bone grafts whereas the other two studies (Hessling et al. [28], Shaw et al. [31]) reported higher implant survival in non-vascularised bone grafts. Shaw et al. [31] reported that implants placed into ‘vascularized bone graft were superior to non-vascularized bone. In particular, those implants in composite radial forearm flaps performed badly. With the proportion of patients with implant loss in these bone flaps within their study being 27% in iliac crest, 33% in fibula, and 100% in radius and that implants placed in composite fibula and iliac crest flaps performed approximately as well as in native maxilla within their study’ [31].

Twelve studies reported on the use of more than one autogenous bone graft donor site within their study (Barrowman et al. [7], Schultes et al. [15], Yerit et al. [16], Fenlon et al. [19], Chiapasco et al. [23], Buddula et al. [24], Fierz et al. [25], Burgess et al. [27], Hessling et al. [28], Watzinger et al. [29], Shaw et al. [31] and Chiapasco et al. [33]); of these, five studies reported on the effect of the autogenous bone graft donor site on implant survival. Two studies (Fenlon et al. [19], Burgess et al. [27]) reported no significant effect on implant survival in varying graft donor sites; however, three studies (Hessling et al. [28], Shaw et al. [31], Chiapasco et al. [33]) reported varying implant survival rates within different autogenous bone grafts but only one study (Hessling et al. [28]) reported that implant loss was significant with this being for implants placed into fibula bone grafts. Shaw et al,. [31] reporting that implants placed into ‘vascularized bone graft were superior to non-vascularized bone. In particular, those implants in composite radial forearm flaps performed badly. With the proportion of patients with implant loss in these bone flaps within their study being 27% in iliac crest, 33% in fibula, and 100% in radius and that implants placed in composite fibula and iliac crest flaps performed approximately as well as in native maxilla within their study’ [31].

Seven studies reported on outcomes related to implant survival in irradiated autogenous bone grafts (Barrowman et al. [7], Fenlon et al. [19], Ch’ng et al. [20], Buddula et al. [24], Fierz et al. [25], Teoh et al. [26], Burgess et al. [27]) (Table 4). One study reported solely on irradiated patients (Buddula et al. [24]) the other six studies (Barrowman et al. [7], Fenlon et al. [19], Ch’ng et al. [20], Fierz et al. [25], Teoh et al. [26], Burgess et al. [27]) reported on both irradiated and non-irradiated patients. These six studies (Barrowman et al. [7], Fenlon et al. [19], Ch’ng et al. [20], Fierz et al. [25], Teoh et al. [26], Burgess et al. [27]) all reported higher implant failure (at an implant and a patient level (where applicable)) of implants placed into autogenous bone grafts in irradiated patients in comparison to those patients who did not received radiotherapy (Table 4).

All of these studies (Barrowman et al. [7], Fenlon et al. [19], Ch’ng et al. [20], Fierz et al. [25], Teoh et al. [26], Burgess et al. [27]) reported on the deleterious effect of radiotherapy on implant survival in autogenous bone grafts within their studies and was found to be statistically significant in two studies (Fenlon et al. [19], Ch’ng et al. [20]) with Fenlon [19] reporting a close correspondence of implant survival (in vascularised free composite grafts) and an absence of radiotherapy using a multiple correspondence analysis and Ch’ng et al. [20] who reported a statistical significance associated with higher implant failure in irradiated fibula free flaps in comparison to non-irradiated fibula free flaps (P = 0.041). However, in two studies (Teoh et al. [26], Burgess et al. [27]), no statistical significance was found despite higher implant failure.

Six studies clearly reported the use of both primary and secondary implant placement within their study (Fenlon et al. [19], Ch’ng et al. [20], Zou et al. [22], Burgess et al. [27], Watzinger et al. [29], Wu et al. [30]); however, only one study (Fenlon et al. [19]) reported on implant survival in primary and secondary implant placement within autogenous bone grafts. Felon et al. [19] reported on implant survival in immediate vs delayed placement of the implant fixtures into free vascularised grafts and found that implant survival of immediately placed implants was significantly worse than that of implants placed after a delay of 3 months in free vascularized grafts.

With regards to cancer type (malignant vs benign), three studies (Schultes et al. [15], Watzinger et al. [29], Klein et al. [32]) reported exclusively on implant survival in patients with malignant H&N cancers with varying implant survival rates being reported, whilst one study reported exclusively on benign H&N cancer patients (Wang et al. [21]) with a 100% implant survival rate being reported (Table 2). Two studies (Fenlon et al. [19], Burgess et al. [27]) provided non-descriptive terms (cancer, head and neck neoplasia) for the type of H&N cancer of the patients within their studies and therefore differentiation between benign and malignant disease could not be made. The other 14 studies reported on both malignant and benign H&N cancers; however, the implant survival data was not reported or presented in a way in which comparison of implant survival in patients with malignant or benign H&N cancers could be made.

Only one study (Linsen et al. [17]) reported on the effect of the peri-implant soft tissue and implant survival of implants placed into autogenous bone grafts. Linsen et al. [17] reported a higher implant failure of implants placed into bone and soft tissue grafts in comparison to implants placed into a bone grafts with residual soft tissues. This difference, however, was not found to be statistically significant (p = 0.436).

In the other 19 studies, the effect of the peri-implant soft tissue was not directly reported as being a factor for implant survival. However, implant success appeared to be significantly affected by the peri-implant soft tissues (see the “Implant survival and Implant Success” and “Complications” sections – for further details).

In nine studies (Schultes et al. [15], Fenlon et al. [19], Wang et al. [21], Zou et al. [22], Chiapasco et al. [18], Chiapasco et al. [23], Watzinger et al. [29] Wu et al. [30], Chiapasco et al. [33]), both implant survival and success data was reported or provided (Table 2). When comparing implant survival and implant success in eight studies (Schultes et al. [15], Fenlon et al. [19], Wang et al. [21], Zou et al. [22], Chiapasco et al. [18], Chiapasco et al. [23], Watzinger et al. [29], Wu et al. [30], Chiapasco et al. [33]) implant success was found to be lower than implant survival but in one study (Chiapasco et al. [33]) implant survival and success were reported as being the same. The reasons for a lack of implant success within these eight studies (other than implant failure/loss) were related to excessive peri-implant bone loss in five studies (Wang et al. [21], Zou et al. [22], Chiapasco et al. [18], Chiapasco et al. [23], Wu et al. [30]), an inability to prosthetically restore the implants in four studies (Schultes et al. [15], Fenlon et al. [19], Watzinger et al. [29], Wu et al. [30]) and gingival hyperplasia in one study (Zou [22]). Six of these studies (Schultes et al. [15], Wang et al. [21], Zou et al. [22], Chiapasco et al. [18], Chiapasco et al. [23], Wu et al. [30]) reported some of this lack of success to the peri-implant soft tissue which was most frequently the soft tissue component of a combined bone and soft tissue free flap (most commonly the external skin).

A variety of implant-based complications were documented. Complications were often described within the study rather than being formal assessed, defined or used as outcome measures. Due to there being a lack of formal definition and variability in the documentation within the studies, the data cannot be considered robust to be collectively appraised but is described for information purposes. Common “complications” reported in the studies include soft tissue overgrowth/hyperplasia of the peri-implant tissues (Wang et al. [21], Chiapasco et al. [18], Teoh et al. [26], Wu et al. [30], Shaw et al. [31]), peri-implantitis and periodontal pocketing (Barrowman et al. [7], Schultes et al. [15], Linsen et al. [17], Burgess et al. [27], Hessling et al. [28]), the need for soft tissue debulking/modification around free flaps (Ch’ng et al. [20], Shaw et al. [31]) and the need for mucosal/soft tissue graft around implants to improve the soft tissue profile (Chiapasco et al. [23], Teoh et al. [26], Chiapasco et al. [33]). These peri-implant complications were most commonly seen when the soft tissue profile around the implant was related to a soft tissue graft and therefore did not have attached keratinised mucosa which is needed to provide a soft tissue profile that is conducive to peri-implant health. Other complications include poor oral hygiene (Wang et al. [21], Zou [22]), challenging prosthodontic rehabilitation/inability to tolerate the prosthesis provided (Barrowman et al. [7], Zou et al. [22], Fierz et al. [25]), poor implant position (Schultes et al. [15], Fenlon et al. [19], Watzinger et al. [29], Wu et al. [30]) and osteoradionecrosis (Ch’ng et al. [20]) (Table 2).