What Is the Role of Endodontic Predisposing Factors in Early Implant Failure?

Dental implant therapy has been introduced as a successful treatment modality for the replacement of missing teeth. Although it has a high overall success rate, implant failures due to infection may occur during the initial healing stage, the first year of loading, maintenance, or after loading.¹ 

Dental implant failures can be classified as early or late according to the stage in which they occur. The failures that occur before the abutment connection stage are considered to be early, whereas failures that occur after occlusal loading are regarded as late. This classification is essential because the failures in these 2 stages may be related to different etiologic factors. Late implant failures are often associated with marginal peri-implantitis, whereas retrograde peri-implantitis is mostly responsible for early implant failure (EIF).^2,3 

Retrograde peri-implantitis is described as an infectious inflammation in the tissues surrounding the implant apex, while the coronal part of the implant is usually osseointegrated.⁴  Etiologic factors such as surgical trauma, excessive heating of the bone while preparing the implant space, bacterial contamination during implantation, early loading, and presence of preexisting inflammation are associated with retrograde peri-implantitis.^5–7  Among these factors, preexisting inflammation may be of particular interest to endodontists because this type of inflammation usually arises from an endodontic pathology of an adjacent tooth or an implant recipient site.

To date, most of the available information on endodontic predisposing factors in the etiology of EIF have been based on case reports⁸  and very few clinical studies.^9–12  A review of retrograde peri-implantitis cases¹³  reported a positive correlation between the neighborhood of an endodontic pathology and implant removal. Even an asymptomatic root canal–treated adjacent tooth with a normal periapical radiographic appearance could be responsible for an implant failure.¹⁴  In addition, implant placement into the extraction sites of teeth with a periapical lesion (PL) was suggested to be one of the major risk factors of EIF.^9,12  Despite all of this literature, the influence of the duration between implant placement and root canal treatment (RCT) on EIF has not been adequately clarified.

Therefore, this study aimed to investigate the relationship between EIF and the following factors: (1) presence of an adjacent tooth with RCT and/or PL; (2) extraction of the tooth with RCT and/or a PL before immediate, early, or late implantation; and (3) the time elapsed between RCT and implant placement.

The protocol for this retrospective study adhered to the principles of the Declaration of Helsinki and was approved by the Medical Ethics Committee of Baskent University (project No. D-KA17/05). Electronic patient records and radiologic data from the dental polyclinic of Baskent University's Adana Dr. Turgut Noyan Healthcare Center were used in this study.

Records of the patients who had received dental implants (BEGO Implant Systems GmbH & Co. KG, Bremen, Germany) between 2013 and 2016 and who had been followed up for at least 1 year were curated. Implantation procedures were performed by 5 resident oral surgeons or periodontists with at least 10 years of experience. The exclusion criteria included disorders known to impair bone metabolism, histories of diabetes mellitus, osteoporosis, chemotherapy, ongoing immunosuppressive pharmacotherapy, and smoking status. Furthermore, patients were excluded if their implantation sites required major bone augmentation, if they were totally edentulous, or if follow-up data were unavailable. Based on these criteria, 810 implants from 342 patients (146 male patients and 196 female patients; mean age: 48.8 ± 12.2 years; age range: 21–83 years) were selected. Digital radiologic data for these patients were also collected.

Periapical radiographs were shot with the parallelism technique using an intraoral X-ray unit (BEST-X-AC; New Life Radiology, Torino, Italy) set at 70 kV and 8 mA and a digital sensor with its accompanying software (Handy Medical Equipment Co, Shanghai, China). Panoramic radiographs were taken with a Veraviewepocs 2D device (Morita, Kyoto, Japan) with a tube voltage of 60–80 kV and a current of 8 mA. All cone beam computerized tomography scans were performed with a Pax-i3D apparatus (Vatech, Hwaseong, Republic of Korea) with the manufacturer's recommended exposure conditions (24 seconds, 90 kVp, and 5.7 mA) and a voxel size of 0.200 mm. EasyDent V4 Viewer software (version 4.1.4.5; Vatech, Hwaseong, Republic of Korea) was used for image reconstruction.

The collected data were examined by 2 evaluators (S.N.S. and Z.O.P.), who scored each case for the presence or absence of the following features: EIF, implants with an adjacent root canal–treated tooth, implants with an adjacent tooth without RCT, implants with no adjacent teeth, implants with an adjacent tooth with PL, extraction of a tooth with PL before implantation, and extraction of a tooth with RCT before implantation. Additional variables of interest included age, gender, and the implant location.

EIF was defined as an implant needing to be removed before or during abutment connection surgery. A root canal–treated tooth was described as the appearance of any radiopaque material in the pulp chamber and/or the root canals. The evaluators detected PL with periapical index (PAI) values,¹⁵  which ranged from 1 (ie, healthy) to 5 (ie, severe apical periodontitis). A PAI value of ≥3 was regarded as indicating the presence of PL. The evaluator-assigned PAI values were compared, and differences were resolved through group discussions.

The intervals between tooth extraction and implantation were categorized as follows¹⁶ : immediate implant placement, early implant placement (ie, implantation after at least 6 weeks of healing time), and late implant placement (ie, implantation at the old extraction site and after at least 6 months of healing time).

The time elapsed from the RCT of the adjacent teeth to implant placement was categorized as follows: less than 4 weeks before implantation, 4–12 weeks before implantation, at least 12 weeks before implantation, up to 4 weeks after implantation, and at least 4 weeks after implantation.

In terms of the RCTs, 55.5% of the procedures were performed by staff clinicians or endodontists in our polyclinic. The rest were performed in other private clinics, at which the time elapsed from RCT was always categorizable as at least 12 weeks before implantation.

The raw data were reviewed by an independent statistician and analyzed with the Statistical Package for the Social Sciences software (version 22; IBM, Armonk, NY). Normally distributed continuous variables were presented as mean values ± standard deviations, and categorical variables were presented as counts and percentages. Student t test was used for between-group comparisons of normally distributed quantitative data. Between-group comparisons of categorical variables were performed with the chi-square test, Fisher exact test, or the Yates continuity correction method. Odds ratios were calculated to assess risks. A P value <.05 was considered a statistically significant result.

The effect of age and gender on EIF was not significant (Table 1). Of a total of 810 implants, 16 (2%) failed at the abutment connection stage. Eleven of the 394 maxillary implants (2.8%) failed, while 5 of 416 mandibular implants (1.2%) failed. The significance was recorded at P > .05.

With respect to the implants, 139 (17.2%) were placed immediately, 176 (21.7%) were placed after extraction and at least 6 weeks of healing time, and 495 (61.1%) were placed in old extraction sites (Figure 1).

A total of 116 (14.3%) implants were adjacent to root canal–treated teeth, while 437 (54%) of them had no prior RCT; 30 (3.7%) implants were adjacent to teeth with PL, while 257 (31.7%) of them had no adjacent teeth (Figure 2). Since preoperative radiographic data of the implantation site (extraction of teeth with RCT or a prior PL) were missing for 7 study subjects, 803 implants were enrolled for the analysis. Of 803 implants, 132 (16.4%) were placed in the extraction sites with prior RCT, while 188 (23.4%) were placed in the extraction site of teeth with PL. Table 2 summarizes the evaluation of EIF according to defined endodontic predisposing factors. A significant relationship was found between EIF and implant placement into the extraction sites of teeth with prior PL (P < .05), with the probability of failure being 4.3 (95% confidence interval [CI]: 1.6–11.9) times higher (Figure 3).

In addition, the time elapsed between implant placement and RCT had a significant effect on EIF (P < .05). The prevalence of EIF was found to be significantly higher (40%) when RCT was performed within the first 4 weeks after implantation (Figure 4).

A few previous studies have commented on the relationship between endodontic parameters and EIF.^9–12  The most important finding of this study is the significant relationship between implantation into extraction sites with prior PL and the occurrence of EIF. This result is consistent with those of some previous retrospective studies^9,12  and case reports.^17–20 

Quirynen et al⁹  found that implant insertion into the sites with prior PL increased the frequency of EIF by 3 times. Lopez-Martinez et al¹²  reported a very high peri-implantitis rate (31.5%) in implants with prior RCT; however, a limitation of their study was that both prior RCT and adjacent endodontic failure were considered together. In addition, only implant peri-implantitis values were demonstrated in the results instead of EIF or retrograde peri-implantitis. It is well-known that many nonendodontic etiologic factors such as occlusal loading, periodontitis, and poor oral hygiene can result in peri-implantitis after prosthetic rehabilitation of an implant. Endodontic predisposing factors are mostly associated with early-stage implant complications; therefore, evaluation after the abutment connection stage might reveal misleading results.

In most of the retrograde peri-implantitis cases, a history of endodontic infection at the recipient site was present.⁸  It has been claimed that bacteria can stay encapsulated as biofilms in both the maxilla and mandible even 1 year after extraction.²¹  More recently, the Epstein-Barr virus, which is involved in symptomatic PL in root canal–treated teeth, has been implicated as a possible etiologic factor for retrograde peri-implantitis.²² 

In this study, an adjacent tooth with RCT or PL was not associated with EIF. These results are consistent with those reported by Laird et al¹⁰  and Doyle et al²³  but contrast with those reported by Quirynen et al,⁹  who observed that the EIF incidence rate was 5 times higher in such cases. Furthermore, many case reports have noted that retrograde peri-implantitis was related to the infection originating from adjacent teeth,^24–27  even in cases with radiographically successful and clinically asymptomatic root canal fillings.¹⁴  However, Steiner²⁶  reported a case in which a PL associated with an implant was treated by RCT of the adjacent tooth, and he criticized earlier case reports that cited adjacent root canal–treated teeth as the reason for EIF with “unwarranted conclusions.”

Besides the influence of previous PL, the question as to whether an immediate or delayed implantation protocol should be followed is also critical. Some investigators have suggested avoiding immediate placement of an implant if an infection was present at the extraction site.^28,29  On the other hand, many recent studies have reported satisfying results with immediate implantation.^30,31  In the present study, the surgeons followed the protocols of the ITI Consensus Conferences and accordingly decided the most appropriate timing for implant placement for each case.¹⁶  According to the findings, the duration between extraction and implantation did not have a significant effect on EIF.

In the present study, the EIF rate was calculated as 2%, which is comparable with the studies done by Borba et al³²  (2.84%), Chrcanovic et al³  (1.74%), Laird et al¹⁰  (3.4%), and Zhou et al¹¹  (3.9%). Grisar et al³³  (4.6%) and Quirynen et al⁹  (6.1%) observed slightly higher EIF rates. These discrepancies might have arisen from the usage of different implant types and different inclusion criteria, such as including smokers, patients with diabetes, and patients undergoing chemotherapy. Borba et al³²  reported that implant placement in the maxilla, which has a lower bone density than the mandible does, is a risk factor for EIF, but Chrcanovic et al³  and Grisar et al³³  found no difference in EIF rates when comparing maxillary and mandibular implants. In the present study, the EIF frequencies for maxillary and mandibular implants were calculated as 2.8% and 1.2%, respectively, with no significant difference.

During the present study's planning stage, it was observed that the effect of the timing of RCT adjacent to an implant was not well established. Zhou et al¹¹  investigated how the durations between implantation and RCT influenced retrograde peri-implantitis outcomes, and they found that longer durations were associated with a lower incidence of retrograde peri-implantitis. Similarly, in the present study, it was found that RCT of an adjacent tooth within 4 weeks after implantation was associated with an increased risk of EIF. However, this result must be treated as preliminary because of the small and unbalanced sample size of implants with adjacent root canal–treated teeth. This limitation arose because of this study's single-center retrospective design. However, conducting a prospective study with more cases is not feasible. Further investigations with larger and more balanced samples may clarify whether the interval between RCT and implantation is associated with EIF outcomes. Such investigations may also clarify the relevance of other RCT-related variables, such as initial PAI values of the teeth on which RCT is performed and the number of clinical visits.

The present findings indicate that prior PL is associated with a quadrupling of the risk of EIF. Additional studies concerning the relevance of the timing of RCT adjacent to an implant are necessary to determine the accuracy of our findings and to facilitate the development of new guidelines.

Abbreviations

EIF:

early implant failure

PAI:

periapical index

PL:

periapical lesion

RCT:

root canal treatment

This study was approved by Baskent University Institutional Review Board (project No. D-KA17/05) and supported by Baskent University Research Fund. We would like to thank Çağla Sarıtürk, the biostatistics specialist of Baskent University's Adana Dr. Turgut Noyan Healthcare Center, for statistical analysis.

The authors deny any conflicts of interest.