Retrograde Peri-implantitis: A Scoping Review of Current Understanding of a Rare Complication in Dental Implants

Search strategy

A comprehensive literature search was performed in PubMed, Google Scholar, Web of Science, Midline, and Wiley online library databases in September 2024 to identify studies related to RPI. The search was performed using the following terms: retrograde peri-implantitis, implant apical lesions, and periapical implant lesions.

This scoping review included retrospective and prospective cohort studies, case-control studies, case series, and case reports published in English. Randomized controlled trials were not expected due to the condition’s rarity but were included if identified. Exclusion criteria included animal studies, in vitro experiments, surveys assessing knowledge and attitude, and reviews without original patient data. All case reports and clinical trials aimed at determining the prevalence, etiology, and treating or salvaging implants diagnosed with RPI were included in the analysis. All treatment modalities were considered, including nonsurgical approaches, surgical debridement, and/or apicoectomy performed on the implant.

Classification of the lesion

Numerous studies have attempted to classify RPI lesions based on various criteria. Sussman¹⁷ proposes a classification system that includes 2 types based on the etiology of the lesion in relation to the adjacent teeth. Type 1, termed an implant-to-tooth lesion, occurs when implant placement leads to the devitalization of the adjoining tooth. In contrast, type 2, known as tooth-to-implant lesions, arises when a periapical lesion from an adjacent endodontically involved tooth contaminates the implant surface.¹⁷ Additional causes of RPI are discussed in previous case reports. Smarst et al expands upon the previous classification by adding two additional classes: class 3, in which the implant is placed out of the alveolar bone housing by being angulated lingually or labially, and class 4, which includes implants placed in sites with residual infection.¹⁸ Other studies describe lesions as infected or inactive. An infected lesion results from the placement of the implant in proximity to the infected tissue, whereas an inactive lesion represents apical scar tissue formation due to the placement of the implant that is shorter than the drilled osteotomy or overheating of the bone when drilling the osteotomy, resulting in aseptic bone necrosis.^15,19 In a recent systematic review, periapical lesions were classified based on their histopathological presentation rather than their etiology. In this classification, 5 distinct classes were proposed: class 1, implant periapical inflammation, which includes both implant nonsuppurated lesions and chronic granuloma; class 2, acute suppurated, chronic suppurated-fistulized; class 3, implant periapical cyst; class 4, foreign body reaction; and class 5, poor bone healing. The histopathological presentation significantly influences the signs and symptoms of the lesion and may affect management decisions.²⁰

Prevalence and incidence

Several studies report this type of implant lesion, all showing a low prevalence. A retrospective study by Quirynen et al¹⁶ evaluates the incidence of RPI in single-tooth implants before and at the abutment connection. The study found that 1.6% of the implants placed in the maxilla and 2.7% placed in the mandible were affected.¹⁶ Another study by Di Murro et al examined 1749 implants placed more than 20 years ago, finding that only 6 implants were affected by RPI (0.35%).²¹ Alssum et al found that 2 implants affected 215 patients examined clinically and radiographically (0.9%), and both implants were placed next to root canal–treated teeth.²² In a retrospective case-control study by Solomonov et al, the incidence was reported to be 3.7%, which correlated with endodontic treatment in teeth adjacent to the implant.²³

Etiological factors

Different etiological factors have been associated with RPI. However, preexisting inflammation is considered the most common cause. The source of inflammation can be bacteria or inflammatory cells from the remaining cyst or granuloma, which can lead to an active periapical implant lesion.²⁴ Several studies document that the periapical area of an implant is colonized by different bacterial species when RPIs is diagnosed. One retrospective study found that RPI lesions harbored more anaerobic bacteria, including Porphyromonas gingivalis, Corynebacterium, Streptococcus, and Klebsiella pneumonia.²⁵ A case report of an implant that developed mesial radiolucency 1.5 years after placement detected the presence of sulfur granules when the granulation tissue was evaluated histologically. These granules were identified as actinomycotic colonies.²⁶ Conversely, Romanos et al²⁷ detected bacteria in 1 out of 4 cases of RPI. The remaining 3 patients presented aseptic bone necrosis.²⁷ Another study demonstrated many plasma cells and lymphocytes in the biopsy of a lesion adjacent to a tooth with insufficient root canal treatment, consistent with inflammatory granuloma.²⁸ One case report identified a potential link between RPI and HIV infection. In this instance, the lesion appeared 3 months after implant insertion. Histopathological examination revealed acute inflammatory changes in the presence of fibrous connective tissues. The authors suggested that the effect of HIV on bone resorption and formation could explain the observed histopathological features. Nevertheless, it is essential to acknowledge the current scarcity of literature on implant complications in patients with HIV.²⁹

In most case reports, active implant periapical lesions were found adjacent to teeth with unresolved periapical pathologies, contaminating the implant apex area. In a study by Zhou et al,³⁰ the incidence of RPI in implants placed next to endodontically treated teeth was 7.8%. The incidence increased when the implants were placed within a month of the completion of endodontic treatment of the adjacent teeth. Additionally, a positive correlation was found between the incidence of RPI and the distance between the implant and the adjacent teeth (Figure 2a).³⁰ Lefver et al report a high chance of developing an implant periapical lesion when the adjoining tooth had a clear periapical pathology (odds ratio = 8), whereas this chance dropped to 1% when the teeth did not show signs of endodontic pathology regardless of endodontic treatment.³¹ One systemic review that included 7 clinical studies evaluating the success of implants placed next to endodontically treated teeth or teeth with periapical pathology concluded that the present evidence suggests an association between the endodontic status of teeth adjacent to dental implants and the success/survival of the implant. However, the results of these studies are inconsistent and may be subject to bias.³² A case report presented 3 cases of RPI in implants placed next to asymptomatic endodontically treated teeth that had no clinical or radiographic symptoms. Due to an incomplete seal or inadequate obturation, the authors suggest that persistent bacteria can contaminate the implant surface and cause infection at the implant apex.³³ The correlation between the radiographic appearance of endodontically treated teeth and histological findings showed that teeth classified as successfully treated based on radiographs presented different reactions, ranging from normal and uninflamed to mild inflammation.³⁴ Moreover, radiographic studies reveal that the validity of periapical radiographs, commonly used to assess the success of endodontic treatment, is questionable. Some cases were documented as endodontically healthy because of the absence of periapical radiolucency on periapical radiographs that showed evidence of apical periodontitis on cone beam computerized tomography images.³⁵ This limitation should be considered when assessing teeth undergoing root canal treatment next to future implant sites.

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Despite the success of immediate implant placement in extraction sockets with or without apical pathology, several case reports document different forms of early implant failure with immediate placement. Apical pathology before tooth extraction is considered a form of preexisting inflammation that may increase the risk of RPI. A histopathological study of alveolar bone cores obtained from osteotomies during implant placement in sites that had been edentulous for a minimum of 1 year showed regions of nonviable bone and bacterial biofilms within the bone marrow spaces.³⁶ Drilling implant osteotomies may reactivate residual bacteria in the healed socket, contaminating the implant surface.²¹ Therefore, the dental history of the implant site may affect the prognosis and risk of developing RPI after implant insertion. The risk of developing periapical lesions increases when dental implants are inserted to replace teeth with a history of periapical lesions even if endodontic treatment is administered (odds ratio = 7.23).¹⁸ The chance of developing RPI reached 20% when implants were placed at sites with previous apical surgeries.²⁷

The root tip near the implant is a risk factor for implant success. Evidence regarding the placement of dental implants in contact with dental tissue remains controversial. A prospective study revealed the uneventful healing of implants placed in contact with fragments of ankylosed teeth over 12–24 months.³⁷ A case series of 6 patients who received dental implants encroached through a root fragment demonstrated clinically and radiographically stable implants.³⁸ However, other case reports document RPI in implants adjacent to root tips.^39,40 Park et al³⁹ report a case in which the lesion developed 22 days after implant placement, causing pain, swelling, and a fistula at the buccal site. One week after removing the root tip and replacing the existing implant with a wider one, the patient’s symptoms disappeared, and further complications did not appear at follow-up.³⁹

Management

To date, the treatment of RPI remains empirical as there is no clear consensus in the literature regarding its management. However, clinicians should address the causative factors and lesions when developing a treatment plan. Sarmast et al⁴¹ propose a decision tree for managing RPI lesions based on a literature review of 20 case reports of successfully treated cases. The decision tree addresses symptomatic and asymptomatic lesions and vital or nonvital adjacent teeth. The authors recommend antibiotic treatment for asymptomatic lesions that appear after implant placement. Surgical intervention was required if no signs of improvement were observed during follow-up. However, an endodontic assessment of the adjacent teeth is necessary when the lesions are symptomatic. Teeth with necrotic pulp should be treated first, and if root canal treatment resolves the lesion, no further treatment is needed. If no resolution is observed, apicectomy and surgical debridement of the implant lesions should be performed. Lesions that do not respond to the former treatment can be managed by implant apicectomy or guided bone regeneration (GBR). Conversely, surgical debridement of the lesion, with or without GBR, is performed when the pulp of the adjacent teeth is vital. Follow-up visits will help to determine the need for further treatment. Implant removal is indicated in cases of implant mobility or when surgical management fails to resolve lesions or symptoms (Table).⁴¹

In several case reports, a nonsurgical approach was used to treat RPI lesions, such as root canal treatment or extraction of the adjacent teeth, with or without systemic antibiotics.⁴² In a case series by Sarmast et al,⁴³ resolution of the implant periapical lesion was observed after nonsurgical root canal treatment of necrotic neighboring teeth. The treatment resulted in the clinical and radiographic resolution of the implant periapical lesion during a 2-year follow-up period.⁴³ Gong et al report a case in which radiographic evidence of healing of the RPI lesion was observed following extraction of the adjacent tooth, which was affected by a periapical infection.²⁸ Chang et al⁴⁴ document the successful management of an implant periapical lesion that developed 1 month after implant placement. Initial treatment with amoxicillin and acetaminophen did not yield improvement, but substituting prednisolone, augmentin, and mefenamic acid resulted in complete healing, as evidenced by radiographs, with no recurrence of symptoms during a 2-year follow-up.⁴⁴ Wassdorp et al⁴⁵ report a case of an extensive periapical lesion involving the apical third of an implant placed in the mandibular incisor. The lesion developed 4 months after implant placement and was managed with a course of systemic antibiotics, resulting in the resolution of the lesion after 9 months without further intervention.⁴⁵ Despite these few case reports, most authors agree that surgical exposure of the apical part of the implant should be considered to ensure proper debridement and removal of the infected tissue. Defects in the apical area can be managed either by GBR or resection of the apical part of the implant.

TableSummary of case reports demonstrating different management approaches for retrograde peri-implantitis lesion

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Several case reports propose surgical debridement of RPI lesions and resection of the apical portion of the implant as treatment methods. Using the resection approach, Dahlin et al⁴⁶ treated 2 cases of periapical lesions around implants that had been functional for 1 and 2 years. Following surgery, bone fill was noticed on radiographs, and the implants were stable.⁴⁶ Another retrospective study of 39 implants that were clinically and radiographically identified to exhibit periapical lesions and treated with apicectomies showed that all except these implants remained stable and functioned over a 4.5- to 15-year follow-up period.⁴⁷ Shaffer et al presented a case in which an implant with a periapical lesion was surgically saved by resection of the exposed apical part of the implant and grafting of the defect with demineralized freeze-dried bone allograft (DFDBA) and tetracycline powder.⁴⁸

The most used method for surgically managing RPI lesions is GBR. After exposing the apical part of the affected implant, the infected granulation tissue is removed, the exposed implant surface is debrided, and the lesion is grafted.⁴⁹ Graft materials are used to fill the cavity after debridement, which helps to stabilize blood clots and maintains space for optimal healing and complete bone regeneration. However, decontaminating the implant surface through mechanical debridement is a crucial step in ensuring the success of the bone graft. In a case study by Soldatos et al,⁵⁰ an Er, Cr:YSGG laser was used in conjunction with mechanical debridement for the surgical management of implants diagnosed as RPIs. After degranulation, the lesion was grafted with FDBA and covered with a collagen membrane. The patient healed uneventfully, resolving clinical symptoms and evidence of bone fill on radiographs taken at 6 and 13 months.⁵⁰ Sgarbanti and Mauro⁵¹ demonstrated the successful management of periapical lesions using DFDBA allografts and collagen membranes. In this case report, the patient presented with slight discomfort at the buccal surface of an implant placed 14 months previously, and a fistula developed at the implant apex and adjacent tooth. Radiography revealed a periapical lesion at the implant apex, proximal to the neighboring tooth. The patient was initially treated with antibiotics (amoxicillin, 500 mg thrice daily for 7 days); however, no improvement was observed. The vitality of adjacent teeth was assessed as nonvital. Endodontic treatment was performed, and GBR surgery was performed after 2 months. The implant surface was brushed with a titanium brush at a low oscillating speed, after which the area was decontaminated with tetracycline.⁵¹ Xenografts alone or in combination with platelet-rich fibrin were used in another case report to treat an implant periapical lesion 4 months after the immediate placement of an implant at the upper lateral incisor site. The implant was restored 4 months later and remained stable at the 1-year follow-up visit.^52,53 One case report documented the successful management of implant periapical lesions using a calcium hydroxide paste as a graft material without a barrier membrane.⁵⁴

Most studies investigating the management of RPI demonstrate implant stability after treatment over a specified follow-up period. However, implant removal is required in cases in which the osseointegration of the affected implant is compromised, and the implant is mobile (Figure 2b through d).^48,55