Orthograde primary endodontic therapy

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1 LITERATURE REVIEW Postextraction Implant in Sites With Endodontic Infection as an Alternative to Endodontic Retreatment: A Review of Literature Stefano Corbella, DDS, PhD* Silvio Taschieri, MD, DDS Igor Tsesis, DMD Massimo Del Fabbro, PhD The aim of this literature review is to evaluate the outcomes of implants placed after extraction of teeth with infections of endodontic origin. An electronic search was performed through electronic databases (Medline and Embase) using the terms immediate implant, post-extractive implants, endodontic infection, infected site, and extraction socket combined with the use of Boolean operators ( AND and OR ). Only articles on human subjects were considered. At least 12 month of mean follow-up was required for inclusion. No restriction was placed regarding study design. Ten studies were included in this review. Survival rates ranged from 92% to 100%. A total of 497 implants were placed in sites with endodontic infection. In nine studies the use of bone substitutes was associated with immediate implant placement. Because of the low number of included studies and the heterogeneity of study design, more well-designed studies are required to assess the relevance of this treatment alternative. Key Words: dental implants, postextraction sockets, apical periodontitis, immediate implants, treatment planning INTRODUCTION Orthograde primary endodontic therapy is an effective treatment, as indicated by systematic reviews reporting success rates ranging between 31% and 100% 1,2 ; the variability was mainly due to the inclusion criteria of the studies and to the adopted criteria of success. In cases of failures with persistent periradicular lesions, secondary endodontic treatment was recommended, and those outcomes were investigated in systematic reviews. 3,4 Reported success rates for nonsurgical or surgical secondary treatment are greater than 70% Department of Biomedical, Surgical and Dental Sciences, Università degli Studi di Milano, IRCCS Istituto Ortopedico Galeazzi, Milan, Italy. * Corresponding author, stefano.corbella@unimi.it DOI: /AAID-JOI-D for both, 3,5 and no significant difference in outcomes between procedures was found. 4,5 Endodontic surgery performed with a modern technique, that is, with the aid of microinstruments, magnification devices, and retrograde canal preparation through the use of ultrasonic retrotips, has been reported to achieve a success rate greater than 90% after 1 year. 6 When the tooth pathologic condition cannot be solved with endodontic retreatment (either orthograde or retrograde) or in the presence of root fractures that become evident during diagnostic or treatment phases, the extraction of the involved tooth becomes the most indicated solution. Tooth extraction and immediate placement of dental implant in the extraction socket is a viable and effective technique in anterior zones 7,8 and posterior regions, though many requisites need to be considered. The presence of active infection in the extraction site is considered one of the main contraindications Journal of Oral Implantology 399

2 Implant in Infected Sites to immediate implant insertion in the socket because of the increased possibility of infection spreading to peri-implant tissues during the healing period Animal studies showed that the presence of periodontal or endodontic infections, even in the active phase, did not compromise the osseointegration of immediately placed implants and did not reduce the bone-to-implant contact after the healing phase The aim of this study was to review the existing literature about the immediate placement of implants in endodontically infected sites in humans and to discuss the clinical and scientific implications of this treatment modality. MATERIAL AND METHODS An electronic search was conducted in Medline and Embase for the period from January 1966 to August 2011 using a combination of different searches using the terms dental implants, immediate implant, extraction socket, infected teeth, infected site, and infected socket. The initial search yielded 264 titles and abstracts, which were independently screened by two reviewers (S.C. and S.T.). No restriction was placed regarding the language and the study design. For clinical studies, a minimum mean follow-up of 12 months was considered for inclusion. Only studies with a clear description of causes of teeth infections were included to allow the analysis. Animal studies were excluded from this review. By screening titles and abstracts, a total of 10 articles were found that met the inclusion criteria The 2011 study by Truninger 24 presented updated data from the same cohort of patients treated in the 2007 study by Siegenthaler 21 ; therefore, only the most recent study was considered. Data extracted were (1) implant survival, defined as the implant in function without pathologic processes ongoing at the time of the investigation; and (2) reasons for tooth extraction, which were classified as endodontic cause, periodontal cause, root fractures, or combined endodontic-periodontal cause. RESULTS Clinical trials Data from clinical trials are summarized in Table 1. Considering all the included studies, a total of 523 implants were inserted in infected sites in 410 patients. The follow-up varied from 3 to 117 months from loading. Guided bone regeneration was performed in all studies with the exception of one 23 to compensate for gaps between the fixtures and socket walls. The survival rate of the treatment was high in all evaluated studies, ranging from 92% to 100%. Table 2 reports the nature of lesions affecting treated teeth, which were purely endodontic in 82.3% of cases. Periodontal lesions were diagnosed in 12.8% of sites, while root fractures and endoperio lesions were less represented (1.4% and 1.0%, respectively). Because of the different nature of periodontal and endodontic lesions, a separate analysis of implants placed only in sites with endodontic or endo-perio infection was performed (Table 3). A total of 497 implants were placed in sites with endodontic infection. The surgical protocol always included an accurate debridement of the sockets after teeth extractions. The case series presented by Novaes Jr and Novaes 17 was the first scientific article describing the immediate insertion of implant in infected sites. Three cases were presented with endo perio lesions and root fractures associated with endodontic infections. In one of the described cases suppuration was observed. The teeth were extracted following a strict atraumatic protocol. An accurate debridement of sockets was then performed. Guided bone regeneration was also used to compensate for bone resorption due to chronic infection of the site. Follow-up time for the 3 cases varied from 7 to 24 months and was uneventful. Years later other researchers 18 compared the insertion of immediate implants in sites with chronic infections with a delayed implant insertion. After randomization, 50 implants were placed in maxilla: 25 were immediately placed after tooth extraction in sites affected with chronic periapical pathosis, and 25 were placed after a healing period of 3 months (control group). Guided bone regeneration was always performed in the first group. One year after the surgery the survival rate in the experimental group was 92%, which was not significantly different from that of the control group. Casap and coworkers 19 described and analyzed the immediate placement of dental implants into 400 Vol. XXXIX / No. Three / 2013

3 Corbella et al TABLE 1 Summary of data from clinical trials* Study Type of Study No. of Patients No. of Implants Guided Tissue Regeneration Loading Follow-up Survival (%) Novaes Jr et Case series 3 Yes Delayed 7 24 mo 100% al 17 (6 7 Lindeboom et Prospective 25 treated with 25 Yes Delayed 1 y 92% al 18 randomized immediate implants Casap et al 19 Prospective Yes Delayed ( mo 96.67% Villa et al 20 Prospective Yes Immediate 1 y 97.40% (,36 h) Del Fabbro et Prospective Yes (PRGF) Delayed 1 y 98.4% al 22 (3 4 Crespi et al 23 2 y 100% Prospective randomized 30 (15 with teeth with root fractures and/or caries; 15 with teeth with periapical chronic lesions) 30 No Delayed (3 Truninger et Prospective 13 with sites with 13 Yes Delayed (3 3 y 100% al 24 randomized periapical pathology Bell et al 25 Retrospective Yes (PRP þ aut) Delayed ( mo 97.5% Fugazzotto 26 Retrospective NR 64 Yes Delayed ( mo 98.1% *NR indicates not reported; PRGF, platelet rich in growth factors; PRP þ aut, platelet rich plasma þ autogenous bone. infected sockets (with chronic or subacute infections and initially affected by subacute periodontal infection, chronic periodontal infection, and endodontic periapical lesions) after accurate debridement. Of the initial 30 implants placed in 20 patients, only one was lost in the follow-up period, which varied from 12 to 72 months after surgery. Another implant was removed because it showed mobility after prosthetic restoration. Surgical complications, such as membrane exposure, were also reported, but they were always correlated to guided tissue regeneration procedures. Of the 10 implants placed in endodontically infected sites, only one implant was lost during the observation period. In 2007, Villa and Rangert 20 published their clinical investigation about the immediate and early function of implants placed in extraction sockets of infected maxillary teeth. A total of 76 implants were inserted in 33 patients with teeth considered hopeless because of endodontic lesions, periodon- Study Total No. of Implants TABLE 2 Clinical trials: Implant distribution by nature of the infection Endodontic % (No.) Periodontal % (No.) Type of Lesion Endo-perio % (No.) Root Fracture % (No.) Not Specified Novaes Jr et al % (1) 66.0% (2) Lindeboom et al % (25) Casap et al % (5) 66.7% (20) 16.7% (5) Villa et al % (15) 72.3% (55) 7.7% (6) Del Fabbro et al % (61) Crespi et al % (15) 50.0% (15) Truninger et al % (13) Bell et al % (285) Fugazzotto % (64) Total % (483) 12.8% (75) 1.0% (6) 1.4% (8) 2.6% (15) Journal of Oral Implantology 401

4 Implant in Infected Sites TABLE 3 Clinical trials: Survival rates considering only implants placed in endodontically infected sites Study Implants % Follow-up % Survival Weight Novaes Jr et al % 7 24 mo 100% Lindeboom et al % 12 mo 92.0% Casap et al % mo 90.0% Villa et al % 12 mo 100% Del Fabbro et al % 12 mo 98.4% Crespi et al % 24 mo 100% Truninger et al % 36 mo 100% Bell et al % 3 93 mo 97.5% Fugazzotto % mo 98.1% Total mo 97.5% 1 tal lesions, or root fractures. Immediate loading of inserted implants was performed within 36 hours of surgery. After 1 year of function, 2 implants were lost, resulting in a 97.4% survival rate. No sign of infection was observed in peri-implant tissues. No failure occurred among the 21 implants placed in sites with periapical lesions. The authors concluded that the presence of infection in the site of the insertion is not associated to an increase of the risk of implant failure. Del Fabbro and coworkers 22 published the results of their prospective study investigating success and survival rates of implants placed in fresh extraction sockets with chronic endodontic infection. Sixty-one implants were placed immediately after teeth extractions and accurate debridement. Only one implant failed because of infection 2 months after insertion. All patients reported full satisfaction with the treatment. Bone resorption, measured through radiographic examination, was mm. Crespi et al 23 inserted 15 immediate implants in sites with chronic endodontic infection and 15 in patients with teeth extracted because of caries or root fractures. After 3 months, implants were loaded and follow-up visits were scheduled up to 24 months. Cumulative survival rate was 100% in both groups. Soft and hard tissue healing around implants was equal between the 2 groups. In 2011, Truninger et al 24 published the 3-year results of the comparative study in which the 1-year results were previously published in Thirteen implants placed in infected sites (8 of which presented suppuration before tooth extraction) were successful after 3 years from placement. In 2011, Bell and coworkers 25 reported data from a retrospective investigation of 285 implants placed in sites with chronic endodontic infections. The follow-up varied from 3 to 93 months. The cumulative survival rate for implants in infected sites was 97.5%, which was not significantly different from the survival rate of implants placed in sites without infection. Another retrospective comparative investigation 26 reported long-term data for implants placed in sites with periapical infection. A 100% survival rate was observed for 64 implants with a follow-up varying from 24 to 117 months, which was not significantly different with respect to the outcome of implants placed in healed sites. Eight of the included studies described the application of guided bone regeneration techniques with the use of resorbable and nonresorbable membranes in conjunction with autologous or etherologous bone filler as described in Table ,22,24 26 In 2 studies, platelet concentrates were used in the surgical procedure. 22,25 No differences were reported in terms of implant survival rates. Antibiotic prophylaxis was administered in 7 studies with different modalities (Table 4) ,22 24 In one study, antibiotic therapy was generally cited without any specification, 25 and in another study it was not reported. 26 Antibiotic therapy was prescribed in 7 studies after surgical treatment ,22 24 DISCUSSION The success of primary endodontic treatment was influenced and determined by many factors that may influence the outcome of this procedure. 2 Presence or absence of periapical lesion (identified 402 Vol. XXXIX / No. Three / 2013

5 Corbella et al TABLE 4 Clinical trials: Description of surgical regenerative technique and preoperative antibiotic prescription* Study GTR Antibiotics Novaes Jr et al 17 Porous hydroxyapatite þ Gengiflex membrane 312 mg ( IU) penicillin V every 8 h for 10 d, starting at 24 h, then 100 mg doxycycline once a day for another 21 days Lindeboom et al 18 Autogenous corticocancellous bone þ BioGide Prophylactic regimen with 600 mg clindamycin Casap et al 19 DBBM þ Reinforced e-ptfe 1.5 g amoxicillin or 0.9 clindamycin 4 d before surgery and for 10 d after Villa et al 20 Autogenous bone alone (n ¼ 8); DBBM þ Collagen membrane (n ¼ 19) 1 g amoxicillin twice a day for 1 d before and for 5 d after surgery Del Fabbro et al 22 PRGFÀ clot as a covering membrane Prophylactic regimen with 2 g amoxicillin þ clavulanic acid Crespi et al 23 Not reported 1 g amoxicillin 1 h before surgery, then 1 g twice a day for a week after surgery Truninger et al 24 DBBM þ Collagen membrane 750 mg amoxicillin 1 h before surgery and for 5 d Bell et al 25 Platelet-rich plasma þ Autogenous bone þ Intravenous antibiotics (in general) Xenograft Fugazzotto 26 Mineralized or demineralized freeze-dried bone allograft or DBBM Not reported *GTR indicates guided tissue regeneration; DBBM, deproteinized bovine bone mineral; e-ptfe, expanded-polytetrafluoroethylene; PGRF, platelet rich in growth factors. ÀPRGF System IV, BTI Biotechnology Institute, Vitoria, Alava, Spain. through radiographs) in the apical portion of teeth, an adequate coronal restoration, and a correct and complete filling of the root canal extending within 2 mm from the radiologic apex could significantly influence the outcome of primary endodontic treatment. 2 Similar criteria were also considered as positive prognostic factors for nonsurgical retreatment, although the scientific literature is scarce. 3,5 Tsesis and colleagues 6 reported high success rates for endodontic surgery performed using a modern microsurgical protocol. However, most of the prospective controlled studies included in evidence-based systematic reviews estimate the treatment effect in an ideal situation as they are normally carried out using a standardized protocol with selective inclusion criteria, experienced surgical teams, and controlled variables. Therefore, such studies do not closely reflect the everyday clinical practice in which there is a much larger variability in study parameters. Some epidemiologic studies reported the success rate of endodontic orthograde treatment by presenting retrospective data from large sample populations. In 2007, Chen and colleagues 27 reported that 5 years after endodontic treatment, 89.7% of teeth were healthy and there were no complications, demonstrating a high success rate of the treatment even when the techniques are performed by different dentists. In this study, the tooth retention rate was 92.9%, which was comparable with rates reported in previous studies. 28,29 These results were confirmed by another more recent study. 30 Hence, endodontic primary and secondary treatment could also be considered viable treatment options in cases with persistent apical periodontitis. In treatment planning, however, the heterogeneity of the reported results should be taken into consideration together with patients expectations. Recent reviews evaluated nonsurgical endodontic treatment versus single-tooth implants. 31,32 They concluded that implants and nonsurgical endodontic treatment followed by prosthetic restoration are both excellent treatment modalities, and the choice of the treatment plan should not be based on outcomes evaluation only. 31 Other factors, such as the impossibility of achieving an optimal coronal seal with the postendodontical restoration, root fractures that may be evident during periapical surgery, or failures of endodontic surgery, may lead to tooth extraction and replacement with implants. Also patients preference has to be considered to fully satisfy their expectations and obtain better compliance. Journal of Oral Implantology 403

6 Implant in Infected Sites Immediate implant placement in fresh extraction sites is a viable technique with success rates comparable to those of implants inserted in healed sites. 10 Presence of active infection was considered one of the major contraindications of immediate postextraction insertion of implants The scientific literature on immediate implants in infected sites is poor. Only 10 studies were found and included. Clinical studies reviewed in the present study reported high survival rates, comparable with those reported in studies describing immediate implant insertion in noninfected postextraction sites. 33 In all studies, tooth extraction was always described as atraumatic, and an accurate debridement of the residual socket was reported to be necessary to thoroughly remove the lesion, reducing the risk of early infection of the tissues surrounding the implant. Furthermore, none of the authors of the included studies reported that presence of suppuration was correlated with an increased failure rate. So, an accurate and complete lesion debridement, associated with antibiotic prophylaxis and therapy, appears to be sufficient to avoid perisurgical infective complications and massive bone loss. Eight studies reported the use of guided bone regeneration to fill gaps between implant and socket and to treat bone dehiscences due to the previous inflammatory process, if present. No differences were highlighted in implant survival rates using different materials and techniques for guided bone regeneration, even if it was observed that exposure of nonresorbable membrane could have a negative effect on implant osseointegration. This may be considered a relative contraindication in this treatment protocol. Notwithstanding the limitations of this review related to the small number of studies, the heterogeneity of protocols, the size of samples, and the follow-up period, the present analysis could be useful for quantifying the evidence on major therapeutic alternatives for endodontists. In general, the decision-making process should not only rely on the success rates of the treatment and on the available evidence but must also take into account the patients expectations and preference as well as the surgeon s skills and attitudes. A clear difference in success rates among surgical retreatment, nonsurgical retreatment, and immediate implant insertion in endodontically infected sites is still not demonstrated. Hence, tooth preservation should be considered the primary treatment option in cases of infected hopeless teeth; thus, immediate implant placement represents an increasingly accepted treatment option. CONCLUSIONS Immediate implant insertion in infected sites could be considered a viable alternative to secondary endodontic treatment. More well-designed, randomized, controlled trials with a longer follow-up are required to confirm implant insertion in infected extraction sockets as a safe procedure with longterm, high success rates. ABBREVIATIONS GBR: guided bone regeneration NR: not reported PRGF: platelet rich in growth factors PRP þ aut: platelet rich plasma þ autogenous bone REFERENCES 1. Ng Y-L, Mann V, Rahbaran S, Lewsey J, Gulabivala K. Outcome of primary root canal treatment: systematic review of the literature part 1. Effects of study characteristics on probability of success. Int Endod J. 2007;40: Ng Y-L, Mann V, Rahbaran S, Lewsey J, Gulabivala K. Outcome of primary root canal treatment:systematic review of the literature part 2. Influence of clinical factors. Int Endod J. 2008;41: Ng Y-L, Mann V, Gulabivala K. Outcome of secondary root canal treatment: a systematic review of literature. Int Endod J. 2008; 41: Del Fabbro M, Taschieri S, Testori T, Francetti L, Weinstein RL. Surgical versus non-surgical endodontic re-treatment for periradicular lesions. Cochrane Database Syst Rev. 2007;18: CD Torabinejad M, Corr R, Handysides R, Shabahang S. Outcomes of nonsurgical retreatment and endodontic surgery: a systematic review. J Endod. 2009;35: Tsesis I, Faivishevsky V, Kfir A, Rosen E. Outcome of surgical endodontic treatment performed by a modern technique: a metaanalysis of literature. J Endod. 2009;35: De Rouck T, Collys K, Cosyn J. Single-tooth replacement in the anterior maxilla by means of immediate implantation and provisionalization: a review. Int J Oral Maxillofac Implants. 2008;23: Chen ST, Buser D. Clinical and esthetic outcomes of implants placed in postextraction sites. Int J Oral Maxillofac Implants. 2009;24: Schwartz-Arad D, Chaushu G. The ways and wherefores of immediate placement of implants into fresh extraction sites: a literature review. J Periodontol. 1997;68: Vol. XXXIX / No. Three / 2013

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