- Open Access
Biological complications in implant-supported oral rehabilitation: as the pendulum swings back towards endodontics and tooth preservation
Evidence-Based Endodontics volume 2, Article number: 4 (2017)
The decision whether to retain a tooth by additional endodontic and restorative treatments or to extract it and replace it with an implant-supported restoration has been extensively debated, and the common approach to this clinical question has shifted back and forth many times. However, in recent years, it has become clear that implants are more prone to technical and biological complications, and require more postoperative treatments to maintain them than the natural dentition. A review of the currently available literature regarding the biological complications of implant-supported oral rehabilitation, and the ensuing effects on the clinical decision-making regarding the preservation of the teeth by endodontic treatments is presented.
The decision whether to retain a tooth by additional endodontic and restorative treatments or to extract it and replace it with an implant-supported restoration has been extensively debated. The common approach to this clinical question has shifted back and forth many times (Iqbal and Kim 2008; Tsesis et al. 2010; Setzer et al. 2017; Rosen et al. 2017). In the early days of implant dentistry, it was assumed that implants provide definite, perfect and risk-free solution to most patients. Thus, the pendulum tilted significantly towards extraction of the teeth that required relatively complex endodontic, periodontal, and/or restorative procedures, while replacing them with dental implants (Rosen et al. 2017).
As for up-to-date evidence, according to contemporary dentistry principles, reasonable efforts should be done to preserve the natural dentition while keeping in mind that the goal of dental implants is to replace missing, and not present, the teeth (Iqbal and Kim 2008; Tsesis et al. 2010). Thus, many factors such as the long-term prognosis, the alternatives in case of treatment failure, and, most importantly, the expected post-treatment complications and quality of life should all be evaluated and incorporated in the practitioners’ decision-making (Iqbal and Kim 2008; Tsesis et al. 2010; Rosen et al. 2017; Tsesis 2014).
Although endodontic treatments may sometimes be technically difficult to perform, the survival of endodontically treated teeth is comparable to dental implants (Setzer et al. 2017; Iqbal and Kim 2007; Doyle et al. 2006), and in the context of the expected post-treatment complications, based on up-to-date relevant literature, it has become clear that implants are more prone to technical and biological complications and require more postoperative treatments to be maintained compared to natural dentition (Tsesis 2014; Hannahan and Eleazer 2008).
As the information regarding the complications of implant-supported restorations gathered, especially concerning the significant incidence and extent of peri-implant diseases, the benefit of teeth extraction and their replacement with implants may be questioned. The benefit to maintain even the compromised teeth, by additional endodontic and restorative treatments, is nowadays well established (Tsesis et al. 2010; Setzer et al. 2017; Rosen et al. 2017).
Thus, in recent years, the pendulum swings back towards maintenance of the natural dentition by additional endodontic and restorative procedures while avoiding tooth extraction whenever possible (Setzer et al. 2017; Rosen et al. 2017). This study aims to review the currently available literature concerning the biological complications of implant-supported oral rehabilitation and the ensuing effects on the clinical decision-making regarding the preservation of the teeth by endodontic treatments.
Biological complications in implant-supported oral rehabilitation
Peri-implant diseases may affect both the surrounding hard and soft tissues. Peri-implant mucositis is a bacteria-induced, reversible inflammatory process of the peri-implant soft tissue with reddening, swelling, and bleeding on periodontal probing. Peri-implantitis is an inflammatory process of the peri-implant soft and hard tissues associated with clinically significant progressive crestal bone loss after the adaptive phase following prosthetic loading (Canullo et al. 2015). Peri-implant diseases are typically described as the result of an imbalance between host response and bacterial load, supported by gram-negative anaerobic microflora. Peri-implant mucositis may not result in peri-implantitis; however, apparently, all peri-implantitis cases had pre-existing mucositis (Ericsson et al. 1992; Leonhardt et al. 1993; Lindhe et al. 1992; Pontoriero et al. 1994; Renvert and Quirynen 2015; Salvi et al. 2012).
In recent years, it became apparent that these serious peri-implant biological complications are extremely frequent, and the incidence of mucositis has been reported to be around 80% and that of peri-implantitis between 28 and 56% (Lindhe et al. 2008). After 10 years in function, 10 to 50% of the dental implants showed signs of peri-implantitis (Roos-Jansaker et al. 2007). A recent meta-analysis reported that peri-implant mucositis is present in 43% (range 32–54%) of patients, while peri-implantitis in 22% (range 14–30%) of patients (Jepsen et al. 2015). Another recent long-term, cross sectional analysis has shown 91.6% implant survival rate, while peri-implant mucositis was found in 33% of the implants and 48% of the patients at the same time and peri-implantitis was detected in 16% of the implants and 26% of the patients. Which means that, after 11 years, in 1 out of 4 patients and 1 in 6 implants will suffer from peri-implantitis (Daubert et al. 2015).
However, although bacterial infection due to plaque accumulation is the main etiologic factor (Jepsen et al. 2015), this is not the only cause for the disease, as patient-, surgical-, and prosthetic-related factors also contribute to its development and severity (Albrektsson et al. 2012a; Albrektsson et al. 2012b; Carcuac and Berglundh 2014; Konstantinidis et al. 2015).
Risk factors are environmental, behavioral, or biological factors that if present directly increase the disease probability and if absent or removed that probability is reduced. Single factors may not be sufficient to produce a disease; therefore, several factors are usually present. Risk factors may be classified as local and general (Renvert and Quirynen 2015; Smeets et al. 2014). Local factors influence bacterial composition and load while the general are related to the individual and may influence the patient’s susceptibility to infection.
Among the general risk factors, present and past periodontal disease, faulty oral hygiene, parafunction, genetic predisposition, history of one or more implant failures, smoking habits, diabetes, immunosuppression, cardiovascular diseases, and an inadequate maintenance program have been reported. Among the local risk factors, inaccessibility for oral hygiene, deep peri-implant pockets, implant supra-structure connection, soft tissue characteristics (keratinized tissue), iatrogenic causes (cement remnants, implant malposition, surgical procedure), implant surface roughness, bone augmentation procedures, and full-arch rehabilitations have shown effect on disease development.
Successful periodontal treatment prior to implant placement lowers the risk for peri-implantitis. Residual pockets (PPD >5 mm) at the end of active periodontal therapy represent a significant risk for peri-implantitis and implant loss. Periodontal patients showed increased susceptibility to peri-implantitis (4.1 OR) (Derks et al. 2016). Patients experiencing recurrent periodontitis had a significantly greater risk for peri-implantitis and implant loss (Ong et al. 2008; Pjetursson et al. 2012; Salvi and Zitzmann 2014). Several studies have suggested that in partially edentulous patients, periodontal pathogens may be transmitted from the periodontally compromised teeth to the newly installed implants implying that periodontal niches may serve as reservoirs for bacterial colonization (Apse et al. 1989; Bragger et al. 1997; Kohavi 1993; Koka et al. 1993; Leonhardt et al. 1992; Mombelli et al. 1995; Quirynen and Listgarten 1990). The importance of treating existing periodontitis prior to the placement of dental implants has been widely reported (Mombelli et al. 1995; Quirynen and Listgarten 1990; Mombelli et al. 1987).
A positive relationship between peri-implantitis and the history of periodontal disease was found in several clinical evaluations. Although microorganisms initiate the infection, tissue breakdown is mainly caused by the host response. Individuals genetically predisposed to overproduce pro-inflammatory cytokines may have increased tissue destruction. Patients that previously suffered from periodontitis (especially aggressive periodontitis) (Theodoridis et al. 2017) are at higher risk to develop peri-implantitis and implant loss (Renvert and Quirynen 2015; Ong et al. 2008; Safii et al. 2010). Long-term survival and success rates are lower in patients with a history of periodontal disease, even adhering to maintenance (Salvi and Zitzmann 2014).
As plaque is the main etiological factor, there is, evidently, a close association between peri-implant bone loss and poor oral hygiene. Indeed, patients with poor oral hygiene or with no or even limited access for proper oral hygiene have been shown to be up to 14 times at greater odds of developing peri-implantitis (Lindhe et al. 2008). In a cohort of 23 patients with 109 implants, only 4% of the implants in patients with optimal oral hygiene presented with peri-implantitis, while 48% of implants presenting peri-implantitis had no accessibility and/or capability for proper oral hygiene (Jepsen et al. 2015; Serino and Strom 2009).
Smokers have been proven to present impaired humoral immune response. Nicotine may impair wound healing, especially considering that nicotine concentrations in the gingival crevice fluid are approximately times 300 than in the plasma. Although, the gingival blood and gingival crevice fluid flow increase already 3–5 days after smoking cessation, the enhanced susceptibility of smoking patients is reflected by a highly increased risk for peri-implantitis, bone loss, and implant failure, especially in the maxilla (Renvert and Quirynen 2015; Apatzidou et al. 2005; Cesar-Neto et al. 2006; Gamal and Bayomy 2002; Graswinckel et al. 2004; Keenan and Veitz-Keenan 2016; Morozumi et al. 2004; Ryder et al. 1998a; Ryder et al. 1998b; Tanur et al. 2000; Tipton and Dabbous 1995; Tran et al. 2016; Veitz-Keenan 2016).
Implants placed too close together, too deeply, or buccally may result in bone loss, and higher ORs were observed for implants in the mandible (OR, 2.0) and for a distance from the prosthetic margin to the crestal bone at baseline of 1.5 mm or less (OR, 2.3) (Derks et al. 2016). The proficiency of the clinician performing the oral rehabilitation has been shown to influence the odds ratio for peri-implantitis by 4.3 (Derks et al. 2016). Cement excess seems to be an important risk factor, 81% of implants with cement remnants had peri-implant disease, and in the same patients, no excess cement found in any of the healthy implants. In 74% of the implants, removal of excess cement leads to absence of peri-implant disease. All implants with cement remnants in patients with a history of periodontitis developed peri-implantitis (Renvert and Quirynen 2015; Linkevicius et al. 2013a; Linkevicius et al. 2013b; Wilson 2009; Korsch et al. 2015).
Patients with four or more implants had an increased risk for peri-implantitis (OR, 15.1) (Derks et al. 2016). Implants from certain brands and surface treatment seem to be more prone to disease than others (Derks et al. 2016).
Enrollment in regular maintenance program including anti-infective preventive measures usually leads to higher long-term survival and success rates of dental implants and their restorations. Therapy of peri-implant mucositis should be considered as a preventive measure for the onset of peri-implantitis. The simple fact of including patients in a regular maintenance program may reduce the risk of peri-implantitis from 43.9 to 18% at patient level (Aguirre-Zorzano et al. 2015; Costa et al. 2012). Patient compliance to these programs may represent a fundamental factor for peri-implantitis prevention (Frisch et al. 2014).
Due to the lack of long-term efficacy and evidence-based guidelines for the treatment of peri-implantitis, prevention strategies are extremely important. Prevention of peri-implant disease starts with a thorough evaluation of individual risk factors, establishment of optimal soft and hard tissue conditions, the choice of the correct implant design followed by a maximally atraumatic approach, and regular clinical examinations and maintenance (Smeets et al. 2014).
Patients must be made aware that implants are more susceptible to plaque-related diseases than the natural teeth (Pjetursson et al. 2012; Fardal and Grytten 2013). Implant therapy must not be limited to the placement and restoration of dental implants but to the implementation of peri-implant maintenance therapy to potentially prevent biologic complications and hence to heighten the long-term success rate. Mean peri-implant preventive maintenance therapy interval was demonstrated to influence the incidence of peri-implantitis. The maintenance program must be tailored to a patient’s risk profiling, with a minimum recall interval of 5 to 6 months (Tonetti et al. 2015). However, it must be stressed that even with regular preventive maintenance, biologic complications might occur (Monje et al. 2016). Professional mechanical plaque removal as the sole element of professional preventive care is inappropriate since education and behavior change are fundamental to sustained improvements in health status. The use of adjunctive chemical approaches to biofilm control in support of mechanical plaque removal protocols in high-risk patients should be considered.
Long-term results of peri-implantitis treatments have been proven unpredictable, with advanced lesions usually commanding implants retrieval. Furthermore, most treatment protocols involve a surgical intervention, which leads to considerable gingival recession accompanied by esthetic and functional impairment. There is no reliable evidence suggesting which could be the most effective interventions for treating peri-implantitis. Systematic reviews have found no evidence that the more complex and expensive therapies were more beneficial than the non-surgical therapies, which basically consisted of simple subgingival mechanical debridement combined or not with some type of anti-infective treatment. Follow-up longer than 1 year suggested recurrence of peri-implantitis in up to 100% of the treated cases for some of the tested interventions, making re-treatment necessary. Larger well-designed RCTs with follow-ups longer than 1 year are still needed (Esposito et al. 2012).
Different preventive/treatment protocols have been suggested. One of the first ones was the Cumulative Interceptive Supportive Therapy (CIST) described by (Lang et al. 2000).
CIST is cumulative in nature and includes four steps, which should not be used as single procedures but rather as a sequence of therapeutic procedures with increasing antibacterial potential depending on the severity and extent of the lesion. Diagnosis, therefore, represents a key characteristic of this maintenance care program.
Evidence posterior to the Lang et al. 2000 publication has revealed that chlorhexidine was not more effective than placebo for treatment of peri-implant mucositis and that locally applied chlorhexidine, as rinses and gels, have limited antimicrobial effects in peri-implant lesions (Porras et al. 2002; Renvert et al. 2006; Carcuac et al. 2015; Menezes et al. 2016), and no statistically significant differences were found between the test and control groups at any time. Recent clinical evaluations have shown limited evidence that systemic antibiotics are helpful (Lindhe et al. 2008). Accordingly, application of local slow release antibiotic devices, which remain at the site of action for at least 7–10 days in a concentration high enough to penetrate the submucosal biofilm, has been proven an effective treatment approach.
Only once infection is successfully controlled, with absence of suppuration and reduced edema, it is reasonable to discuss treatment approaches to either restore the bony support of the implant by means of regenerative techniques or to reshape the peri-implant soft tissues and/or bony architecture by means of resective surgical techniques, depending on the esthetic considerations and morphological characteristics of the lesion.
However, even if the bone fill of peri-implant defects may be achieved using the biological principle of guided tissue regeneration (Hammerle et al. 1995; Persson et al. 1996), re-osseointegration of a previously contaminated implant surface into a regenerated one does not seem to be a usual outcome (Wetzel et al. 1999).
Deep circumferential and intrabony defects may be treated thorough debridement, implant-surface decontamination, and defect reconstruction while defects without clear bony walls or predominantly supra-bony by thorough debridement and apical repositioning of the marginal mucosa (Figuero et al. 2014). Although the new bone, and/or the bone graft, may fill the osseous defects, as documented by an increase in radiographic bone density, in most cases, it is apparently a simple healing process, where this radio-opaque material is not really connected to the implant surface. A recent meta-analysis has shown that despite the clinically important improvements, a complete disease resolution may not be expected by any of the treatment protocols investigated (Schwarz et al. 2015). Furthermore, the major drawback of surgical therapy for peri-implant disease seems to be that healing usually leads to marked gingival recession compromising the esthetic and functional result of the restoration (Schwarz et al. 2015); therefore, this type of treatment should be considered only in cases where non-surgical therapy was not effective.
If clinical signs of infection may not be controlled by any means, or if a previously osseointegrated oral implant has lost most of its bone support and/or becomes clinically mobile, explantation is mandatory (Lang et al. 2000).
Since the primary objective of surgical treatment in peri-implantitis is debridement and decontamination of the implant surface which may lead to resolution of the inflammatory lesion, and due to the side effects of surgical interventions, non-surgical treatment alternatives are preferable (Lindhe et al. 2008). Most authors recommend surgical interventions only when non-surgical therapy has failed. However, the patient must be fully aware that due to gingival recession, surgical procedures will compromise the esthetic result of the restoration and lead to functional impairment (Figuero et al. 2014). Accordingly, the actual trend is to try to deal with early and moderate peri-implant lesions by non-surgical treatment alternatives.
For periodontal treatment, adjunctive subgingival administration of minocycline following non-surgical periodontal treatment was shown to present a significantly better and prolonged effect compared to scaling/root planing alone on the reduction of probing depth, clinical attachment loss, gingival index, and interleukin-1beta content (Lu and Chei 2005), together with a greater reduction in the proportions and numbers of red complex bacteria (Bland et al. 2010).
Subgingival debridement plus use of locally applied antibiotics as a slow release device has also been proven effective for peri-implantitis treatment (Faggion and Schmitter 2010). Clinical results after application of minocycline microspheres as an adjunct to mechanical treatment of incipient peri-implant infections compared to adjunctive treatment employing 1% chlorhexidine gel application have been evaluated. The combined mechanical/antimicrobial treatment for the chlorhexidine group did not result in any reduction in probing depth and but only limited reduction of bleeding scores. The adjunctive use of minocycline microspheres (ARESTIN®), on the other hand, resulted in improvements in both probing depths and bleeding scores (Renvert et al. 2006; Renvert et al. 2004; Bassetti et al. 2014; Salvi et al. 2007).
Among the non-surgical treatments evaluated, especially in initial/moderate peri-implantitis, debridement in conjunction with local minocycline microspheres in a slow-release device (SRD) application (Arestin®) achieved the greatest additional reduction in probing pocket depth, number of bleeding upon probing positive sites, and counts of Porphyromonas gingivalis and Tannerella forsythia (Renvert et al. 2006; Bassetti et al. 2014; Salvi et al. 2007; Schar et al. 2013).
A recent meta-analysis has shown that ARESTIN® was more effective than slow-release chips containing chlorhexidine for peri-implant inflammation treatment (Faggion et al. 2014).
Besides its antibacterial effect, minocycline microspheres (Arestin®) have also an important anti-inflammatory action. Its application locally reduces cytokine levels (i.e., interleukin 1b), combined with debridement results in serum reductions of cholesterol, C-reactive protein, and interleukin 1 level (Lu and Chei 2005; D’Aiuto et al. 2005; Persson et al. 2006). However, the effect of adjunctive therapy diminishes with time, being the most positive effect is within 1 to 2 months; therefore, the risk for reinfection favors repeated SRD application in peri-implant areas, meaning that this anti-infective/anti-inflammatory must be periodically repeated (Renvert et al. 2006; Bassetti et al. 2014; Salvi et al. 2007; Bonito et al. 2005).
It should be kept in mind that prevention is always the best treatment alternative. Based on the individual risk assessment for a certain patient, presence of clinical signs of inflammation, and loss of implant bone support, a maintenance and treatment protocol based on three combined actions is suggested: debridement, decontamination, and anti-infective/anti-inflammatory therapy (DDA). Debridement is usually performed with ultrasonic scalers and hand curettes, where the therapeutic action is mainly cleaning and rinsing of the submucosal area and allow access for the decontamination devices. Calculus does not strongly adhere to titanium surfaces; therefore, only light contact with the metal surfaces of the abutment and/or implant is recommended. Release of titanium particles into the soft tissue, due to scaling of the implant surface, may cause a foreign body inflammatory reaction and even bone resorption (Eger et al. 2017).
Decontamination may be performed with a combined application of a sodium hypochlorite gel, with an activating vehicle (PERISOLV®) (Jurczyk et al. 2016; Roos-Jansaker et al. 2017), irrigation and decontamination with hydrogen peroxide 3% which has also lead to good clinical outcomes (Jepsen et al. 2016; Suarez et al. 2013), and submucosal cleaning with a chitosan brush (LABRIDA™). Once bleeding stops, the third step is the submucosal application of the anti-infective/anti-inflammatory minocycline microspheres (Arestin®).
As the pendulum swings back towards endodontics
Dental implants have led to a new era in dentistry and provide excellent and effective functional and esthetic solutions that were not available in the past to patients. However, as presented in the current review, in recent years, it became clear that peri-implant diseases are extremely common and significant, and their prevention and treatment is complex. Thus, their substantial extent may pose significant effects on the post-treatment quality of life of many of the patients (Iqbal and Kim 2008; Doyle et al. 2006; Hannahan and Eleazer 2008).
With the increasing reports regarding the complications associated with implants, the readiness adopted by many clinicians in the past, to easily extract the teeth and replace them with implants, significantly decreased. It seems that in recent years, the pendulum swings back towards maintaining even the compromised teeth by additional endodontic and restorative procedures (Tsesis et al. 2010; Setzer et al. 2017; Rosen et al. 2017).
The increased scientific understanding of the endodontic disease together with recent technological advances in endodontics, such as the use of electronic apex locators, surgical operation microscopes, modern imaging systems, and ultrasonic instruments (Taschieri et al. 2010; Tsesis et al. 2015), have resulted in the ability to predictably treat and retain the teeth that were previously considered untreatable (Rosen et al. 2017).
Furthermore, modern endodontics provides a variety of treatment alternatives including non-surgical and surgical endodontic treatments and management of complications such as root perforations and separated instruments (Rosen et al. 2017). These treatment alternatives may provide predictable prognosis even for complicated cases and the compromised teeth. In fact, to-date the vast majority of the teeth that undergo endodontic treatment survive and function for the long term, and those which are eventually lost, are usually extracted because of non-endodontic-related causes, such as prosthetic and periodontal complications (Rosen et al. 2017; Ng et al. 2010; Salehrabi and Rotstein 2004).
The overall goal of dentistry is to provide long-term functional and esthetic solution to the patient (Tsesis et al. 2010; Setzer et al. 2017; Rosen et al. 2017). Therefore, the option to preserve the natural teeth by additional treatments, and the option to extract compromised teeth and replace them with implants, should be regarded as complementary options and not as competing ones (Iqbal and Kim 2008; Setzer et al. 2017; Rosen et al. 2017; Iqbal and Kim 2007). Modern endodontics provides excellent conservative alternatives that with proper restoration offer predictable results in maintaining even the compromised teeth (Tsesis et al. 2010; Rosen et al. 2017; Tsesis 2014). Furthermore, in light of the severity and extent of per-implant diseases, the option to extract the teeth and replace them with implant-supported restoration should be preserved mainly for cases where all conservative treatments failed and the teeth were determined as clinically hopeless (Tsesis et al. 2010; Setzer et al. 2017; Rosen et al. 2017).
This pendulum swing towards maintaining the teeth by additional endodontic and restorative treatments is expected to be beneficial both for the long-term dental functioning and quality of life of the patients and for the reduction of unnecessary implant-related medical and medico-legal complications that practitioners may face in their daily practice.
Aguirre-Zorzano LA, Estefania-Fresco R, Telletxea O, Bravo M. Prevalence of peri-implant inflammatory disease in patients with a history of periodontal disease who receive supportive periodontal therapy. Clin Oral Implants Res. 2015;26(11):1338–44.
Albrektsson T, Buser D, Chen ST, Cochran D, DeBruyn H, Jemt T, et al. Statements from the Estepona Consensus meeting on peri-implantitis, February 2–4, 2012. Clin Implant Dent Relat Res. 2012a;14(6):781–2.
Albrektsson T, Buser D, Sennerby L. Crestal bone loss and oral implants. Clin Implant Dent Relat Res. 2012b;14(6):783–91.
Apatzidou DA, Riggio MP, Kinane DF. Impact of smoking on the clinical, microbiological and immunological parameters of adult patients with periodontitis. J Clin Periodontol. 2005;32(9):973–83.
Apse P, Ellen RP, Overall CM, Zarb GA. Microbiota and crevicular fluid collagenase activity in the osseointegrated dental implant sulcus: a comparison of sites in edentulous and partially edentulous patients. J Periodontal Res. 1989;24(2):96–105.
Bassetti M, Schar D, Wicki B, Eick S, Ramseier CA, Arweiler NB, et al. Anti-infective therapy of peri-implantitis with adjunctive local drug delivery or photodynamic therapy: 12-month outcomes of a randomized controlled clinical trial. Clin Oral Implants Res. 2014;25(3):279–87.
Bland PS, Goodson JM, Gunsolley JC, Grossi SG, Otomo-Corgel J, Doherty F, et al. Association of antimicrobial and clinical efficacy: periodontitis therapy with minocycline microspheres. J Int Acad Periodontol. 2010;12(1):11–9.
Bonito AJ, Lux L, Lohr KN. Impact of local adjuncts to scaling and root planing in periodontal disease therapy: a systematic review. J Periodontol. 2005;76(8):1227–36.
Bragger U, Burgin WB, Hammerle CH, Lang NP. Associations between clinical parameters assessed around implants and teeth. Clin Oral Implants Res. 1997;8(5):412–21.
Canullo L, Schlee M, Wagner W, Covani U. Montegrotto Group for the study of peri-implant disease. International Brainstorming Meeting on Etiologic and Risk Factors of Peri-implantitis, Montegrotto (Padua, Italy), August 2014. Int J Oral Maxillofac Implants. 2015;30(5):1093–104.
Carcuac O, Berglundh T. Composition of human peri-implantitis and periodontitis lesions. J Dent Res. 2014;93(11):1083–8.
Carcuac O, Abrahamsson I, Charalampakis G, Berglundh T. The effect of the local use of chlorhexidine in surgical treatment of experimental peri-implantitis in dogs. J Clin Periodontol. 2015;42(2):196–203.
Cesar-Neto JB, Benatti BB, Sallum EA, Casati MZ, Nociti Jr FH. The influence of cigarette smoke inhalation and its cessation on the tooth-supporting alveolar bone: a histometric study in rats. J Periodontal Res. 2006;41(2):118–23.
Costa FO, Takenaka-Martinez S, Cota LO, Ferreira SD, Silva GL, Costa JE. Peri-implant disease in subjects with and without preventive maintenance: a 5-year follow-up. J Clin Periodontol. 2012;39(2):173–81.
D’Aiuto F, Nibali L, Parkar M, Suvan J, Tonetti MS. Short-term effects of intensive periodontal therapy on serum inflammatory markers and cholesterol. J Dent Res. 2005;84(3):269–73.
Daubert DM, Weinstein BF, Bordin S, Leroux BG, Flemming TF. Prevalence and predictive factors for peri-implant disease and implant failure: a cross-sectional analysis. J Periodontol. 2015;86(3):337–47.
Derks J, Schaller D, Hakansson J, Wennstrom JL, Tomasi C, Berglundh T. Effectiveness of implant therapy analyzed in a Swedish population: prevalence of peri-implantitis. J Dent Res. 2016;95(1):43–9.
Doyle SL, Hodges JS, Pesun IJ, Law AS, Bowles WR. Retrospective cross sectional comparison of initial nonsurgical endodontic treatment and single-tooth implants. J Endod. 2006;32(9):822–7.
Eger M, Sterer N, Liron T, Kohavi D, Gabet Y. Scaling of titanium implants entrains inflammation-induced osteolysis. Sci Rep. 2017;7:39612.
Ericsson I, Berglundh T, Marinello C, Liljenberg B, Lindhe J. Long-standing plaque and gingivitis at implants and teeth in the dog. Clin Oral Implants Res. 1992;3(3):99–103.
Esposito M, Grusovin MG, Worthington HV. Treatment of peri-implantitis: what interventions are effective? A Cochrane systematic review. Eur J Oral Implantol. 2012;5 Suppl:S21–41.
Faggion Jr CM, Schmitter M. Using the best available evidence to support clinical decisions in implant dentistry. Int J Oral Maxillofac Implants. 2010;25(5):960–9.
Faggion Jr CM, Listl S, Fruhauf N, Chang HJ, Tu YK. A systematic review and Bayesian network meta-analysis of randomized clinical trials on non-surgical treatments for peri-implantitis. J Clin Periodontol. 2014;41(10):1015–25.
Fardal O, Grytten J. A comparison of teeth and implants during maintenance therapy in terms of the number of disease-free years and costs—an in vivo internal control study. J Clin Periodontol. 2013;40(6):645–51.
Figuero E, Graziani F, Sanz I, Herrera D, Sanz M. Management of peri-implant mucositis and peri-implantitis. Periodontol 2000. 2014;66(1):255–73.
Frisch E, Ziebolz D, Vach K, Ratka-Kruger P. Supportive post-implant therapy: patient compliance rates and impacting factors: 3-year follow-up. J Clin Periodontol. 2014;41(10):1007–14.
Gamal AY, Bayomy MM. Effect of cigarette smoking on human PDL fibroblasts attachment to periodontally involved root surfaces in vitro. J Clin Periodontol. 2002;29(8):763–70.
Graswinckel JE, van der Velden U, van Winkelhoff AJ, Hoek FJ, Loos BG. Plasma antibody levels in periodontitis patients and controls. J Clin Periodontol. 2004;31(7):562–8.
Hammerle CH, Fourmousis I, Winkler JR, Weigel C, Bragger U, Lang NP. Successful bone fill in late peri-implant defects using guided tissue regeneration. A short communication. J Periodontol. 1995;66(4):303–8.
Hannahan JP, Eleazer PD. Comparison of success of implants versus endodontically treated teeth. J Endod. 2008;34(11):1302–5.
Iqbal MK, Kim S. For teeth requiring endodontic treatment, what are the differences in outcomes of restored endodontically treated teeth compared to implant-supported restorations? Int J Oral Maxillofac Implants. 2007;22(Suppl):96–116.
Iqbal MK, Kim S. A review of factors influencing treatment planning decisions of single-tooth implants versus preserving natural teeth with nonsurgical endodontic therapy. J Endod. 2008;34(5):519–29.
Jepsen S, Berglundh T, Genco R, Aass AM, Demirel K, Derks J, et al. Primary prevention of peri-implantitis: managing peri-implant mucositis. J Clin Periodontol. 2015;42 Suppl 16:S152–7.
Jepsen K, Jepsen S, Laine ML, Anssari Moin D, Pilloni A, Zeza B, et al. Reconstruction of peri-implant osseous defects: a multicenter randomized trial. J Dent Res. 2016;95(1):58–66.
Jurczyk K, Nietzsche S, Ender C, Sculean A, Eick S. In-vitro activity of sodium-hypochlorite gel on bacteria associated with periodontitis. Clin Oral Investig. 2016;20(8):2165–73.
Keenan JR, Veitz-Keenan A. The impact of smoking on failure rates, postoperative infection and marginal bone loss of dental implants. Evid Based Dent. 2016;17(1):4–5.
Kohavi D. Complications in the tissue integrated prostheses components: clinical and mechanical evaluation. J Oral Rehabil. 1993;20(4):413–22.
Koka S, Razzoog ME, Bloem TJ, Syed S. Microbial colonization of dental implants in partially edentulous subjects. J Prosthet Dent. 1993;70(2):141–4.
Konstantinidis IK, Kotsakis GA, Gerdes S, Walter MH. Cross-sectional study on the prevalence and risk indicators of peri-implant diseases. Eur J Oral Implantol. 2015;8(1):75–88.
Korsch M, Robra BP, Walther W. Cement-associated signs of inflammation: retrospective analysis of the effect of excess cement on peri-implant tissue. Int J Prosthodont. 2015;28(1):11–8.
Lang NP, Wilson TG, Corbet EF. Biological complications with dental implants: their prevention, diagnosis and treatment. Clin Oral Implants Res. 2000;11 Suppl 1:146–55.
Leonhardt A, Berglundh T, Ericsson I, Dahlen G. Putative periodontal pathogens on titanium implants and teeth in experimental gingivitis and periodontitis in beagle dogs. Clin Oral Implants Res. 1992;3(3):112–9.
Leonhardt A, Adolfsson B, Lekholm U, Wikstrom M, Dahlen G. A longitudinal microbiological study on osseointegrated titanium implants in partially edentulous patients. Clin Oral Implants Res. 1993;4(3):113–20.
Lindhe J, Berglundh T, Ericsson I, Liljenberg B, Marinello C. Experimental breakdown of peri-implant and periodontal tissues. A study in the beagle dog. Clin Oral Implants Res. 1992;3(1):9–16.
Lindhe J, Meyle J, Group DoEWoP. Peri-implant diseases: Consensus Report of the Sixth European Workshop on Periodontology. J Clin Periodontol. 2008;35(8 Suppl):282–5.
Linkevicius T, Puisys A, Vindasiute E, Linkeviciene L, Apse P. Does residual cement around implant-supported restorations cause peri-implant disease? A retrospective case analysis. Clin Oral Implants Res. 2013a;24(11):1179–84.
Linkevicius T, Vindasiute E, Puisys A, Linkeviciene L, Maslova N, Puriene A. The influence of the cementation margin position on the amount of undetected cement. A prospective clinical study. Clin Oral Implants Res. 2013b;24(1):71–6.
Lu HK, Chei CJ. Efficacy of subgingivally applied minocycline in the treatment of chronic periodontitis. J Periodontal Res. 2005;40(1):20–7.
Menezes KM, Fernandes-Costa AN, Silva-Neto RD, Calderon PS, Gurgel BC. Efficacy of 0.12% chlorhexidine gluconate for non-surgical treatment of peri-implant mucositis. J Periodontol. 2016;87(11):1305–13.
Mombelli A, van Oosten MA, Schurch Jr E, Land NP. The microbiota associated with successful or failing osseointegrated titanium implants. Oral Microbiol Immunol. 1987;2(4):145–51.
Mombelli A, Marxer M, Gaberthuel T, Grunder U, Lang NP. The microbiota of osseointegrated implants in patients with a history of periodontal disease. J Clin Periodontol. 1995;22(2):124–30.
Monje A, Aranda L, Diaz KT, Alarcon MA, Bagramian RA, Wang HL, et al. Impact of maintenance therapy for the prevention of peri-implant diseases: a systematic review and meta-analysis. J Dent Res. 2016;95(4):372–9.
Morozumi T, Kubota T, Sato T, Okuda K, Yoshie H. Smoking cessation increases gingival blood flow and gingival crevicular fluid. J Clin Periodontol. 2004;31(4):267–72.
Ng YL, Mann V, Gulabivala K. Tooth survival following non-surgical root canal treatment: a systematic review of the literature. Int Endod J. 2010;43(3):171–89.
Ong CT, Ivanovski S, Needleman IG, Retzepi M, Moles DR, Tonetti MS, et al. Systematic review of implant outcomes in treated periodontitis subjects. J Clin Periodontol. 2008;35(5):438–62.
Persson LG, Ericsson I, Berglundh T, Lindhe J. Guided bone regeneration in the treatment of periimplantitis. Clin Oral Implants Res. 1996;7(4):366–72.
Persson GR, Salvi GE, Heitz-Mayfield LJ, Lang NP. Antimicrobial therapy using a local drug delivery system (Arestin) in the treatment of peri-implantitis. I: microbiological outcomes. Clin Oral Implants Res. 2006;17(4):386–93.
Pjetursson BE, Helbling C, Weber HP, Matuliene G, Salvi GE, Bragger U, et al. Peri-implantitis susceptibility as it relates to periodontal therapy and supportive care. Clin Oral Implants Res. 2012;23(7):888–94.
Pontoriero R, Tonelli MP, Carnevale G, Mombelli A, Nyman SR, Lang NP. Experimentally induced peri-implant mucositis. A clinical study in humans. Clin Oral Implants Res. 1994;5(4):254–9.
Porras R, Anderson GB, Caffesse R, Narendran S, Trejo PM. Clinical response to 2 different therapeutic regimens to treat peri-implant mucositis. J Periodontol. 2002;73(10):1118–25.
Quirynen M, Listgarten MA. Distribution of bacterial morphotypes around natural teeth and titanium implants ad modum Branemark. Clin Oral Implants Res. 1990;1(1):8–12.
Renvert S, Quirynen M. Risk indicators for peri-implantitis. A narrative review. Clin Oral Implants Res. 2015;26 Suppl 11:15–44.
Renvert S, Lessem J, Lindahl C, Svensson M. Treatment of incipient peri-implant infections using topical minocycline microspheres versus topical chlorhexidine gel as an adjunct to mechanical debridement. J Int Acad Periodontol. 2004;6(4 Suppl):154–9.
Renvert S, Lessem J, Dahlen G, Lindahl C, Svensson M. Topical minocycline microspheres versus topical chlorhexidine gel as an adjunct to mechanical debridement of incipient peri-implant infections: a randomized clinical trial. J Clin Periodontol. 2006;33(5):362–9.
Roos-Jansaker AM, Renvert H, Lindahl C, Renvert S. Surgical treatment of peri-implantitis using a bone substitute with or without a resorbable membrane: a prospective cohort study. J Clin Periodontol. 2007;34(7):625–32.
Roos-Jansaker AM, Almhojd US, Jansson H. Treatment of peri-implantitis: clinical outcome of chloramine as an adjunctive to non-surgical therapy, a randomized clinical trial. Clin Oral Implants Res. 2017;28(1):43–8.
Rosen E, Nemcovsky CE, Tsesis I. Evidence-Based Decision Making in Dentistry. Switzerland: Springer International Publishing; 2017.
Ryder MI, Fujitaki R, Johnson G, Hyun W. Alterations of neutrophil oxidative burst by in vitro smoke exposure: implications for oral and systemic diseases. Ann Periodontol. 1998a;3(1):76–87.
Ryder MI, Fujitaki R, Lebus S, Mahboub M, Faia B, Muhaimin D, et al. Alterations of neutrophil L-selectin and CD18 expression by tobacco smoke: implications for periodontal diseases. J Periodontal Res. 1998b;33(6):359–68.
Safii SH, Palmer RM, Wilson RF. Risk of implant failure and marginal bone loss in subjects with a history of periodontitis: a systematic review and meta-analysis. Clin Implant Dent Relat Res. 2010;12(3):165–74.
Salehrabi R, Rotstein I. Endodontic treatment outcomes in a large patient population in the USA: an epidemiological study. J Endod. 2004;30(12):846–50.
Salvi GE, Zitzmann NU. The effects of anti-infective preventive measures on the occurrence of biologic implant complications and implant loss: a systematic review. Int J Oral Maxillofac Implants. 2014;29(Suppl):292–307.
Salvi GE, Persson GR, Heitz-Mayfield LJ, Frei M, Lang NP. Adjunctive local antibiotic therapy in the treatment of peri-implantitis II: clinical and radiographic outcomes. Clin Oral Implants Res. 2007;18(3):281–5.
Salvi GE, Aglietta M, Eick S, Sculean A, Lang NP, Ramseier CA. Reversibility of experimental peri-implant mucositis compared with experimental gingivitis in humans. Clin Oral Implants Res. 2012;23(2):182–90.
Schar D, Ramseier CA, Eick S, Arweiler NB, Sculean A, Salvi GE. Anti-infective therapy of peri-implantitis with adjunctive local drug delivery or photodynamic therapy: six-month outcomes of a prospective randomized clinical trial. Clin Oral Implants Res. 2013;24(1):104–10.
Schwarz F, Becker K, Sager M. Efficacy of professionally administered plaque removal with or without adjunctive measures for the treatment of peri-implant mucositis. A systematic review and meta-analysis. J Clin Periodontol. 2015;42 Suppl 16:S202–13.
Serino G, Strom C. Peri-implantitis in partially edentulous patients: association with inadequate plaque control. Clin Oral Implants Res. 2009;20(2):169–74.
Setzer F, Kim S. Preserving the Natural Tooth Versus Extraction and Implant Placement: An Evidence-Based Approach. In: Rosen E, Nemcovsky CE, Tsesis I, editors. Evidence-Based Decision Making in Dentistry Springer International Publishing; 2017. p. 73–95.
Smeets R, Henningsen A, Jung O, Heiland M, Hammacher C, Stein JM. Definition, etiology, prevention and treatment of peri-implantitis—a review. Head Face Med. 2014;10:34.
Suarez F, Monje A, Galindo-Moreno P, Wang HL. Implant surface detoxification: a comprehensive review. Implant Dent. 2013;22(5):465–73.
Tanur E, McQuade MJ, McPherson JC, Al-Hashimi IH, Rivera-Hidalgo F. Effects of nicotine on the strength of attachment of gingival fibroblasts to glass and non-diseased human root surfaces. J Periodontol. 2000;71(5):717–22.
Taschieri S, Del Fabbro M, Weinstein T, Rosen E, Tsesis I. Magnification in modern endodontic practice. Refuat Hapeh Vehashinayim (1993). 2010;27(3):18–22. 61.
Theodoridis C, Grigoriadis A, Menexes G, Vouros I. Outcomes of implant therapy in patients with a history of aggressive periodontitis. A systematic review and meta-analysis. Clin Oral Investig. 2017;21(2):485–503.
Tipton DA, Dabbous MK. Effects of nicotine on proliferation and extracellular matrix production of human gingival fibroblasts in vitro. J Periodontol. 1995;66(12):1056–64.
Tonetti MS, Chapple IL, Jepsen S, Sanz M. Primary and secondary prevention of periodontal and peri-implant diseases: introduction to, and objectives of the 11th European Workshop on Periodontology consensus conference. J Clin Periodontol. 2015;42 Suppl 16:S1–4.
Tran DT, Gay IC, Diaz-Rodriguez J, Parthasarathy K, Weltman R, Friedman L. Survival of dental implants placed in grafted and nongrafted bone: a retrospective study in a university setting. Int J Oral Maxillofac Implants. 2016;31(2):310–7.
Tsesis I. Complications in Endodontic Surgery: Prevention, Identification and Management. Berlin: Springer-Verlag; 2014.
Tsesis I, Nemkowsky CE, Tamse E, Rosen E. Preserving the natural tooth versus extraction and implant placement: making a rational clinical decision. Refuat Hapeh Vehashinayim. 2010;27(1):37–46. 75.
Tsesis I, Blazer T, Ben-Izhack G, Taschieri S, Del Fabbro M, Corbella S, et al. The precision of electronic apex locators in working length determination: a systematic review and meta-analysis of the literature. J Endod. 2015;41(11):1818–23.
Veitz-Keenan A. Marginal bone loss and dental implant failure may be increased in smokers. Evid Based Dent. 2016;17(1):6–7.
Wetzel AC, Vlassis J, Caffesse RG, Hammerle CH, Lang NP. Attempts to obtain re-osseointegration following experimental peri-implantitis in dogs. Clin Oral Implants Res. 1999;10(2):111–9.
Wilson Jr TG. The positive relationship between excess cement and peri-implant disease: a prospective clinical endoscopic study. J Periodontol. 2009;80(9):1388–92.
CEN and ER prepared the manuscript. Both authors read and approved the final manuscript.
Carlos E. Nemcovsky is an Advisory Board Member, and Eyal Rosen is the Editor-in-Chief of Evidence-based endodontics journal.
The authors declare that they have no competing interests.
Ethics approval and consent to participate
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.