10.59987/ads/2018.3.106-110
Aims: Periapical implant lesions, also named apical peri-implantitis or retrograde peri-implantitis, were described since 1992, and are characterized by progressive bone loss at the periapex of the implant. Several case reports have suggested these lesions are possible causes for early implant failure. The aim of this article was to review the Literature to identify current knowledge on surgical management of acute retrograde peri-implantitis.
Methods: The Authors conducted an independent search of the literature, for reports published from 1st January 2008 up to 1st December 2018 in English in several databases: Pubmed, Web of Science, SciVerse, MEDLINE and through The Cochrane Database of Systematic Reviews. Only articles reporting data on the surgical treatment of dental implants affected by retrograde peri-implantitis were included. Articles with unclear or unavailable data or with less than 6 months of follow- up were excluded.
Results: A total of 47 records was identified through database searching. After removal of duplicates, twenty-three studies were selected for title and abstract analysis, with 14 articles considered for detailed screening. Eight studies were included in the present review: four case series and four case reports. A total of 36 dental implants was treated, with follow-up ranging from 6 months to 6 years. Successful resolution of the peri-apical lesion was observed in 34/36 implants (94.5%), with complete radiographic bone fill and absence of further symptomatology.
Conclusions: Several surgical techniques have been reported for lesions, with proper endodontic evaluation of adjacent teeth. Surgical and chemical debridement of the implant associated with GBR considered the preferred treatment option.
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Annali di stomatologia
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Surgical management of acute retrograde peri-implantitis: a review of current literature
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Surgical management of acute retrograde peri-implantitis: a review of current literature
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                                                                                                   Review article



    Surgical management of acute retrograde
    peri-implantitis: a review of current literature




                                                                                              li
                                                                                            na
    Bianca Di Murro DDS                                    peri-apical lesion was observed in 34/36 implants
    Piero Papi DDS                                         (94.5%), with complete radiographic bone fill and
    Giorgio Pompa MD, DDS                                  absence of further symptomatology.




                                                                                          io
                                                           Conclusions: Several surgical techniques have
                                                           been reported for lesions, with proper endodontic
    Oral Surgery Unit, Department of Oral and Maxillo-     evaluation of adjacent teeth. Surgical and chemi-




                                                                     az
    Facial Sciences, “Sapienza” University of Rome,        cal debridement of the implant associated with
    Rome, Italy                                            GBR considered the preferred treatment option.

                                                           Key Words: retrograde peri-implantitis, apical




                                                                   rn
    Corresponding Author:                                  peri-implantitis, surgical treatment, surgical man-
    Bianca Di Murro                                        agement, review.
    Oral Surgery Unit
    Department of Oral and Maxillo-Facial Sciences




                                                       te
    “Sapienza” University of Rome                          Introduction
    Via Caserta 6
    00161 Rome, Italy                                      In recent years, implant placement has become
    E-mail: biancadimurro@hotmail.it
                                                     In    widespread in clinical practice (1), with long-term suc-
                                                           cess and survival rates reported in literature (2). Its
                                                           massive use, however, has resulted in different types
    Summary                                                of complications, divided in mechanical (3,4) and bio-
                                                           logical (5-7). When, after implant placement, localized
                            ni

    Aims: Periapical implant lesions, also named api-      pain develops in the apical area, with or without radio-
    cal peri-implantitis or retrograde peri-implantitis,   graphic changes, a periapical implant lesion should be
    were described since 1992, and are characterized       suspected (8). Periapical implant lesions, also named
                          io


    by progressive bone loss at the periapex of the        apical peri-implantitis or retrograde peri-implantitis,
    implant. Several case reports have suggested           were described, for the first time, by McAllister et al.
    these lesions are possible causes for early im-        (9) in 1992. These lesions are characterized by pro-
                        iz



    plant failure. The aim of this article was to review   gressive bone loss at the periapex of the implant and
    the Literature to identify current knowledge on        several case reports have suggested they are the
    surgical management of acute retrograde peri-im-       possible cause of early implant failure (10-12).
          Ed




    plantitis.                                             The retrograde peri-implantitis (RPI) has a preva-
    Methods: The Authors conducted an independent          lence (13) of 0.26%, significantly lower than marginal
    search of the literature, for reports published        peri-implantitis; although its incidence may increase
    from 1st January 2008 up to 1st December 2018 in       up to 7.8% when teeth adjacent to the implant exhibit
    English in several databases: Pubmed, Web of           an endodontic infection (14).
    Science, SciVerse, MEDLINE and through The             It seems positively correlated with the presence of a
 IC




    Cochrane Database of Systematic Reviews. Only          small distance between an implant and its adjacent
    articles reporting data on the surgical treatment      tooth and a shorter time elapsing from the endodontic
    of dental implants affected by retrograde peri-im-     treatment of the adjacent tooth to the implant place-
    plantitis were included. Articles with unclear or      ment (13). The aetiology of this lesion is still unclear.
C




    unavailable data or with less than 6 months of fol-    According to several Authors, the most likely cause is
    low-up were excluded.                                  the endodontic pathology of the tooth replaced by the
    Results: A total of 47 records was identified          implant or of the adjacent tooth (15,16). Among other
    through database searching. After removal of du-       factors hypothesized, contamination of the implant
©




    plicates, twenty-three studies were selected for ti-   surface (17), bone overheating, pre-existing bone dis-
    tle and abstract analysis, with 14 articles consid-    ease, presence of root fragments or foreign bodies
    ered for detailed screening. Eight studies were in-    were reported in literature (10,18-20). The diagnosis
    cluded in the present review: four case series and     of RPI is both clinical and radiological, with lesions
    four case reports. A total of 36 dental implants       classified into two groups: inactive and active forms
    was treated, with follow-up ranging from 6             (17). The inactive lesions show no symptomatology
    months to 6 years. Successful resolution of the        and are radiologically represented as a radiolucency

    106                                                                      Annali di Stomatologia 2018;IX (3):106-110
    Treatment of retrograde peri-implantitis: a review


    around the apex of the implant. These lesions do not        Search strategy
    need further treatment, although these patients             The following search strategy was performed: “retro-
    should be inserted in a proper follow-up program:           grade peri-implantitis” OR “periapical peri-implantitis”
    standardized periapical X-rays every 6 months. If an        OR “periapical implant lesion” OR “apical peri-implan-
    expansion of radiolucency occurs, it may indicate ac-       titis” AND “treatment” OR “surgical treatment” OR




                                                                                                  li
    tivation and needs surgical intervention. On the con-       “surgical management”.
    trary, active lesions usually showed symptoms (17)




                                                                                                na
    such as: persisting pain at the mucosa correspondent        Study selection
    to the implant (19), inflammation, suppuration by fis-      Only articles in English and reporting data on the sur-
    tula discharge, mobility and dull percussion (21, 22).      gical treatment of at least one dental implant affected
    According to Pennarrocha- Diago et al. (23), the evo-       by retrograde peri-implantitis were included. Random-
    lution stage of the periapical lesion should be divided




                                                                                              io
                                                                ized clinical trial, prospective or retrospective cohort
    in three parts, promptly individuated and included in       studies, case-control studies, case series or case re-
    the diagnosis to determine the best suitable treatment      ports were included. Articles with unclear or unavail-
    strategy.                                                   able data or with less than 6 months of follow-up




                                                                          az
    Acute periapical lesion staging can be divided into         were excluded.
    three parts:
    1. Non-suppurated: there are no radiographically de-        Quality and risk of bias assessment
         tectable changes in bone density around the apex       To evaluate methodological quality of case reports




                                                                        rn
         of the implant, but a spontaneous and localized        and case series included, a recently modified version
         pain at the implant mucosa is present.                 of the Newcastle-Ottawa Scale was used (24). This
    2. Suppurated: an appreciable radiolucency is pre-          tool is divided into four sections: selection (1 item),
         sent as a result of purulent collection around the




                                                           te
                                                                ascertainment (2 items), causality (4 items) and re-
         apex of the implant, with an active process of         porting (1 item). As suggested by the Authors (24),
         bone reabsorption.
                                                                results of the items are not summarised to obtain an
    3. Suppurated-fistulized: there is a visible radiolu-
                                                                aggregate score to evaluate methodological quality:
                                                         In
         cency, a fistulous tract from the apex of the im-
                                                                on the contrary, an overall judgment is expressed for
         plant is detectable in the buccal plate or in coro-
                                                                each article (low-medium-high). The Cochrane Col-
         nal direction. Diagnosis of retrograde peri-implan-
                                                                laboration’s two-part tool for assessing risk of bias
         titis, and therefore its prevalence, may also be in-
                                                                was used. Bias is assessed as a judgment (high, low,
         fluenced by the limits of two-dimensional radi-
                               ni
                                                                or unclear) from five domains (selection, perfor-
         ographic imaging systems, with an underestima-
         tion that can be solved by the use of three-dimen-     mance, attrition, reporting, and other).
         sional cone beam.
                             io


    The aim of this article was to review the Literature to
    identify current knowledge on surgical management           Results
    of acute retrograde peri-implantitis.
                           iz



                                                                Study selection
                                                                Two reviewers (BDM, PP), independently from each
    Materials and methods                                       other, extracted pertinent data (year; study design;
           Ed




                                                                number of implants; surgical technique; outcome and
    To address the research purpose, the Authors (BDM,          follow-up time) from selected studies. A total of 47
    PP) conducted an independent electronic search of           records was identified through database searching.
    the literature for reports published from 1st January       After removal of duplicates, twenty-three studies were
    2008 up to 1st December 2018 in English in several          selected for title and abstract analysis, with 14 arti-
    databases: Pubmed library, Web of Science (Thom-            cles considered for detailed screening (Fig. 1). The
 IC




    son Reuters), SciVerse (Elsevier), MEDLINE (OVID)           kappa agreement between reviewers was 0.9.
    and through The Cochrane Database of Systematic
    Reviews (CDSR). In addition, a manual search was            Population
    performed in the databases of the following journals:       A total of 36 dental implants was treated, with follow-
C




    Implant Dentistry; Clinical Oral Implants Research;         up ranging from 6 months to 6 years. Successful res-
    Clinical Implant Dentistry and Related Research; Eu-        olution of the peri-apical lesion was observed in
    ropean Journal of Oral Implantology; International          34/36 implants (94.5%), with complete radiographic
    Journal of Oral & Maxillofacial Implants; Journal of        bone fill and absence of further symptomatology.
©




    Oral Implantology; International Journal of Oral and
    Maxillofacial Surgery; International Journal of Oral        Quality assessment
    and Maxillofacial Surgery; Journal of Periodontology;       Eight studies were included in the present review:
    Journal of Clinical Periodontology; International Jour-     four case series and four case reports. All articles
    nal of Periodontics and Restorative Dentistry; Journal      were classified as low-quality studies, in accordance
    of Prosthetic Dentistry; International Journal of En-       with the adapted version of the Newcastle-Ottawa
    dodontics; Journal of Endodontics.                          Scale.

    Annali di Stomatologia 2018;IX (3):106-110                                                                      107
    B. Di Murro et al.



                              
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    Figure 1. PRISMA Flow-chart of study selection.
                                      io


    Surgical treatment options:                                                            disappearance of the apical radiolucency. Follow-
    -Surgical and mechanical debridement of the apical                                     up time ranged from 12 to 36 months.
                                                                                      -    Quaranta et al. (27) (2014, case report): Surgical
                                    iz



    part of the implant.
    -Surgical and mechanical debridement of implant with                                   and mechanical debridement was performed on 1
    Guided Bone Regeneration (GBR) of the defect.                                          implant with application of tetracycline paste.
               Ed




    -Implant apex resection.                                                               Then, placement of a bioabsorbable pericardium
                                                                                           membrane over the defect. Resulted in complete
    Risk of bias                                                                           radiographic bone fill and absence of clinical
    All 8 studies included were classified as having a                                     symptoms. Five years follow-up.
    high-risk of bias (Tab. 1).                                                       -    Mohamed et al. (28) (2012, case report): Surgical
                                                                                           and mechanical debridement was performed on 1
    Study results                                                                          dental implant, then Guided Bone Regeneration
 IC




    Based on the analysis of studies included, the follow-                                 (GBR) with a xenograft and Platelet Rich Fibrin
    ing surgical options are presented in detail:                                          (PRF). Furthermore, endodontic retreatment of
    - Dahlin et al. (25) (2009, case series): Implant                                      adjacent teeth. Resulted in complete radiographic
        apex resection was performed on 2 implants. Re-                                    bone fill and absence of clinical symptoms. One
C




        sulted in complete healing without further sympto-                                 year follow-up.
        matology and complete radiographic bone fill into                             -    Penarrocha-Diago et al. (29) (2013, case series):
        the resected area. Follow-up period ranged from                                    Surgical and mechanical debridement was per-
        1 to 3 years.                                                                      formed on 22 dental implants, with an implant sur-
©




    - Zhou et al. (26) (2012, case series): Surgical and                                   vival rate of 91% with no radiologic or clinical al-
        mechanical debridement of periapical lesion was                                    terations. Follow-up period from 1 to 6 years.
        performed on 6 implants, trepanation and curet-                               -    Chan et al. (30) (2011, case series): Surgical and
        tage of the apical part of the implant within irriga-                              mechanical debridement was performed on 2 im-
        tion by natural saline and chlorhexidine, further                                  plants. Furthermore, irrigation with 0.12%
        application of tetracycline paste. Uneventful heal-                                chlorhexidine gluconate and GBR using an allo-
        ing resulted for all patients treated, with complete                               graft mixed with 250 mg tetracycline powder and

    108                                                                                                      Annali di Stomatologia 2018;IX (3):106-110
    Treatment of retrograde peri-implantitis: a review


    Table 1. Risk of bias of studies included (-: high risk of bias; +: low risk of bias).

    Author                        Random             Allocation          Blinding         Incomplete           Selective         Other
                                  sequence           concealment                          outcome data         reporting         bias
                                  generation




                                                                                                                       li
    Dahlin, et al.                -                  -                   -                -                    -                 +
    Zhou, et al.                  -                  -                   -                -                    -                 +




                                                                                                                     na
    Quaranta, et al.              -                  -                   -                -                    -                 +
    Mohamed, et al.               -                  -                   -                -                    -                 +
    Penarrocha-Diago, et al.      -                  -                   -                -                    -                 +




                                                                                                                   io
    Chan, et al.                  -                  -                   -                -                    -                 +
    Sarmast, et al.               -                  -                   -                -                    -                 +




                                                                                        az
    Soldatos, et al.              -                  -                   -                -                    -                 +




                                                                                      rn
        an absorbable membrane. Healing was unevent-                         just prescribing an antibiotic therapy to the patient
        ful and significant radiographic resolution of the                   with/without endodontic treatment of the adjacent
        lesions was observed. Six months follow-up.                          tooth, resection of the apical part of the dental im-
    -   Sarmast et al. (31) (2017, case report): Surgical                    plant, endodontic re-treatment and apicoectomy of




                                                                te
        and mechanical debridement was performed on 1                        the adjacent tooth to surgical/chemical debridement
        dental implant, irrigation with 0.9% sodium chlo-                    of the apical part of the implant with/without guided
        ride and chemical debridement using EDTA/                            bone regeneration (GBR) procedures (36).
        chlorhexidine 2%, tetracycline. GBR with freeze-
                                                              In             This systematic review included only case series and
        dried bone allograft (FDBA) 50/50 and an ab-                         case reports, which are considered to be of the
        sorbable membrane. Healing was characterized                         lowest scientific evidence, with absence of higher
        by absence of symptoms and radiographic bone                         quality studies. Another limitation is represented by
        filling. One year follow-up.                                         the limited follow-up available, with only one study
                                ni
    -   Soldatos et al. (32) (2018, case report): Surgical                   with long-term evaluation (>5 years), and by the very
        and mechanical debridement was performed on 1                        low amount of dental implants included (n=36).
        dental implant, with implant surface decontami-                      Peri-implant diseases are well documented condi-
                              io


        nated by means of an air-abrasive device with                        tions in literature, with a still unclear etiology (37, 38),
        amino acid glycine powder and Er,Cr:YSGG laser                       however the available scientific evidence on retro-
        (wavelength of 2,780 nm) at 1.5 W/25 Hz. GBR                         grade peri-implantitis is very limited, with only case
                            iz



        performed with FDBA and a collagen membrane.                         reports or case series present in literature (35).
        Resulted in complete remission of symptomatol-                       Based on the findings of this review, surgical and me-
        ogy and radiographic bone fill. Thirty-three                         chanical debridement of the apical part of the implant
             Ed




        months follow-up.                                                    associated with GBR with allograft and absorbable
                                                                             membrane was the surgical treatment option most
                                                                             used. Several chemical agents were used to decon-
    Discussion                                                               taminate the implant surface, with irrigation by means
                                                                             of physiologic saline solution and chlorhexidine as
    Retrograde peri-implantitis aetiology is still controver-                the most performed. Only one article reported data on
 IC




    sial and this leads to a large underestimation of the                    apex resection of the implant affected by RPI.
    pathology (17).
    In the past 20 years, various surgical techniques
    have been used and further studies with a longitudi-                     Acknowledgements
C




    nal design are needed to identify a proper clinical
    management (31). Treatment for RPI depends both                          The Authors declare they have no conflict of interest
    on clinical presentation and radiological findings: di-                  related to this study.
    agnosis range between 1 week and 4 years after im-
©




    plant placement (33, 34). If there is a radiolucent area
    around the apex of the implant, not present immedi-                      References
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