684 APICAL/RETROGRADE PERI-IMPLANTITIS RAMANAUSKAITE ET AL

Apical/Retrograde Periimplantitis/
Implant Periapical Lesion: Etiology, Risk
Factors, and Treatment Options:
A Systematic Review
Ausra Ramanauskaite, DDS,* Gintaras Juodzbalys, DDS, MSD, PhD,† and Tolga F. Tözüm, DDS, PhD‡

mplant therapy is a well- Objectives: To review the litera- and the adjacent tooth with incom-

I established treatment method for

replacing missing teeth. Several
studies have provided a high level of
ture on retrograde periimplantitis
symptoms, risk factors, and treat-
ment methods and to propose a deci-
plete endodontic treatment/endodon-
tic pathology (r ¼ −0.4; P ¼ 0.009)
and a positive correlation between
evidence supporting the favorable sion-making tree of retrograde the later risk factor and implant
long-term survival and success rate
periimplantitis management. removal (r ¼ 0.3; P ¼ 0.028). Regen-
of implant therapy in general popula-
tions.1,2 Although the success rate of Materials and Methods: An erative treatment (45.2% of the cases)
dental implants is high, there are risks electronic literature search was or implant removal (35.7% of the
of developing infectious complica- conducted on the MEDLINE and cases) was the most common treat-
tions.3 EMBASE databases for articles pub- ment techniques used. A decision-
Infectious dental implant failures lished between 1990 and 2015. Clin- making tree of retrograde periim-
can be divided into marginal periim- ical human studies in the English plantitis management is suggested.
plantitis and retrograde (or apical) peri- language were included. Conclusions: The etiology of
implantitis. Periimplantitis has been Results: The search resulted in retrograde periimplantitis is most
characterized as an inflammatory pro- 44 case reports published by 27 often infectious. A decision-making
cess around an implant, which includes authors. The average time of the tree aimed at managing patients with
both soft tissue inflammation and pro- diagnosis of the pathology was found retrograde periimplantitis according
gressive loss of supporting marginal
to be 26.07 weeks after implant to the possible etiology and symptoms
bone beyond biological bone remodel-
ing.3 It is often associated with bleeding placement (SD 6 39.7). Fistula for- of the disease can be a useful tool in
at the periimplant margin after the inser- mation was found to be the most com- the treatment of the pathology.
tion of a periodontal probe into the peri- mon clinical symptom, statistically (Implant Dent 2016;25:684–697)
implant space, increased periimplant significantly more often occurring in Key Words: dental implants, periap-
pocket-probing depth, mucosal reces- the maxilla (P ¼ 0.04). A negative ical periodontitis, bone regenera-
sion, and/or suppuration.4 Periimplantitis correlation was found between pain tion, apicoectomy, reoperation

*PhD student, Clinic of Dental and Oral Pathology, Lithuanian

University of Health Sciences, Kaunas, Lithuania.
†Professor, Department of Maxillofacial Surgery, Lithuanian was reported to occur in 18.8% of sub- implant apex. The pathology develops
University of Health Sciences, Kaunas, Lithuania.
‡Associate Professor, Department of Periodontics, College of jects and 9.6% of implants.5 If periim- shortly after implant insertion, while the
Dentistry, University of Illinois at Chicago, Chicago, IL.
plantitis is left undetected and untreated, coronal portion of the implant achieves
Reprint requests and correspondence to: Tolga F. Tözüm, it will progress further and eventually a normal osseointegration.7 Of the 539
DDS, PhD, Department of Periodontics, College of
Dentistry, University of Illinois at Chicago, Room 469G,
result in the loss of the implant.6 implants evaluated in a retrospective
801 S. Paulina Street, Chicago, IL 60612, Phone: 312- Retrograde periimplantitis (periap- study, this pathology was found to
996-0265, Fax: 312-996-0943, E-mail: [email protected] ical implant lesion; implant periapical occur in 1.6% of the implants in the
ISSN 1056-6163/16/02505-684 pathology, apical periimplantitis) was upper jaw and 2.7% in the lower jaw.8
Implant Dentistry
Volume 25
Number 5 first described in 1992 by McAllister Retrograde periimplantitis is a rapid
Copyright © 2016 Wolters Kluwer Health, Inc. All rights
reserved. et al7 as an infectious-inflammatory infective process, and it can not
DOI: 10.1097/ID.0000000000000424 process in the tissues surrounding the only potentially cause devitalization of

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RAMANAUSKAITE ET AL IMPLANT DENTISTRY / VOLUME 25, NUMBER 5 2016 685

adjacent teeth but also greatly reduce A periapical radiograph is the stan- reviews, PhD theses, and abstracts were
bone for future implants if not treated dard diagnostic indicator of an implant excluded.
early.9 periapical lesion, but it does not distin-
Many possible etiological factors guish between inactive and infected Types of Studies
have been associated with the periapical lesions.32 Reiser et al32 classified implant The review included all human
implant pathology (Table 1). However, periapical lesions as noninfecteddthey prospective and retrospective follow-
based on the case reports analyzed, it are diagnosed radiographically but do up studies, clinical trials, cohort studies,
seems that retrograde periimplantitis is not present any clinical symptoms. Such case-control studies, case series studies,
most commonly associated with the lesions do not require any treatment, case reports published between January
infection from adjacent teeth with peri- unless there is an increase in the size of 1, 1990, and September 1, 2015, that
apical pathology and/or incomplete the periapical radiolucency. Infected reported on symptoms, possible risk
endodontic treatment, and with residual lesions are usually accompanied by pain, factors, treatment methods, and out-
infection at the site of tooth extraction, tenderness, swelling, and/or the pres- comes for retrograde periimplantitis.
when the tooth was removed because of ence of a fistulous tract. Such lesions Information Sources
periapical pathology. start at the implant apex but exhibit the The search strategy incorporated
It has been suggested that retro- capacity to spread coronally, proxi- the examination of electronic data-
grade periimplantitis resembles mar- mally, and facially. However, if retro- bases, supplemented by hand searches.
ginal periimplantitis in that both are grade periimplantitis is not treated A search was conducted on the National
site-specific infective processes.27 The immediately, it usually results in com- Library of Medicine database
main differences, however, lie in the plete implant loss when the bone loss (MEDLINE) through its online site
microbial composition, rate of expan- progresses to the complete implant (PubMed) and EMBASE databases.
sion, and pathway of the infection. surface.32 Additionally, a hand search was con-
Micro-organisms found in periimplan- The aim of this article was to ducted in the following journals: Implant
titis are closely associated with peri- review possible literature on retrograde Dentistry; Clinical Oral Implants
odontal pathogens, whereas those periimplantitis symptoms, possible risk Research; Clinical Implant Dentistry
found in retrograde periimplantitis factors, and treatment methods and to and Related Research; European Journal
resemble the composition of endodon- propose a decision-making tree of ret- of Oral Implantology; International Jour-
tic pathogens.7,14 Furthermore, periim- rograde periimplantitis management nal of Oral & Maxillofacial Implants;
plantitis occurs coronally, whereas that could help clinicians cope with Journal of Oral Implantology; Interna-
retrograde periimplantitis initiates api- the pathology. tional Journal of Oral and Maxillofacial
cally. Marginal periimplantitis can be Surgery; International Journal of Oral
detected clinically by routine probing, MATERIALS AND METHODS
and Maxillofacial Surgery; Journal of
whereas retrograde periimplantitis re- Periodontology; Journal of Clinical Peri-
lies on patient complaint and radio- Protocol and Registration
odontology; International Journal of
graphic assessment.27 The methods of the analysis and
Periodontics and Restorative Dentistry;
inclusion criteria were specified in
Journal of Prosthetic Dentistry; Interna-
advance and documented in a protocol.
Table 1. Possible Etiological Factors tional Journal of Endodontics; Journal
The review was registered in
Indicated in the Articles of Endodontics; Oral Surgery, Oral
PROSPERO, an international prospec-
Medicine, Oral Pathology and Oral
No. of tive register of systematic reviews. The
Radiology; and Endodontology; Turkish
Possible Etiological Factors Cases protocol can be accessed at http://www.
Journal of Medical Sciences.
crd.york.ac.uk/PROSPERO/display_
Residual infection at the site of 6 The references of each relevant
extraction/tooth removal record.asp?ID¼CRD42015026852; reg-
study were screened to discover addi-
due to the periapical istration number: CRD42015026852.
tional relevant publications.
pathology10–13 The reporting of this systematic analysis
Infection from adjacent teeth 24 adhered to the Preferred Reporting Search
with periapical pathology Items for Systematic Review and Meta- The PubMed and EMBASE
and/or incomplete Analyses (PRISMA) statement.33 resource databases were explored
endodontic treatment7,13–25 through advanced searches. The key-
Periodontal pathology13 1 Focus Question words and search inquiries used during
Impaired bone healing24 1 What are the symptoms, possible the primary stage were as follows: “ret-
Bone overheating26 1 risk factors, and treatment methods for rograde peri-implantitis” OR “periapi-
Retained root tip27 1 retrograde periimplantitis? cal peri-implantitis” OR “peri-apical
Excessive tightening during 2 implant lesion” AND (“symptoms”
insertion21,26 Types of Publications OR “risk factors” OR “treatment”).
Incomplete implant depth28 1 The review included studies on The choice of keywords was intended
Contaminated implant tip21 2 humans published in the English lan- to be broad to collect as much relevant
Questionable etiology23,29–31 7
guage. Letters, editorials, literature data as possible without relying on

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686 APICAL/RETROGRADE PERI-IMPLANTITIS RAMANAUSKAITE ET AL

electronic means alone to refine the mellitus, osteoporosis, or other con- based on the inclusion and exclusion
search results. traindicating systemic conditions criteria.
3. Studies of patients with machined
Selection of Studies Data Extraction
and hydroxyapatite surface im-
Two reviewers based on the inclu- The data were independently ex-
plants or ceramic implants
sion criteria independently screened tracted from studies in the form of
4. Studies not focused specifically
titles derived from this broad search. variables, according to the aims and
on the selected topic or that
The reviewers compared decisions and themes of the present review, as listed
included unclear data or had au-
resolved differences through discus- as follows.
thors who could not be contacted
sion, consulting a third party when for any reason. Data Items
consensus could not be reached. The Data were collected from the
third party was an experienced senior Sequential Search Strategy included articles and arranged in the
reviewer. Full reports were obtained for After the initial literature search, following fields:
all the studies deemed eligible for all article titles were screened to elim-
inclusion in this article. At the title and inate irrelevant publications, review “Year”dRevealed the year of pub-
abstract stage, one reviewer accepted articles, case reports, and in vitro and lication
the citations that seemed to meet the animal studies. Next, studies were “Gender”dIndicated the gender of
inclusion criteria and sent them for full- excluded based on data obtained from the patient
text review, with a second reviewer screening the abstracts. The final stage “Implant region”dDescribed the
assessing only those citations the first of screening involved reading the full location of the implant (the
reviewer deemed ineligible. texts to confirm each study’s eligibility jaw and/or tooth area)
Population
Subjects in the included studies Table 2. Assessment of the Risk of Bias
must have had at least one osseointe-
grated rough-surface, solid screw–type Random Incomplete
endosseous implant that presented with Sequence Allocation Outcome Selective Other
signs of retrograde periimplantitis. Ret- Author Generation Concealment Blinding Data Reporting Bias
rograde periimplantitis defined as infec- McAllister et al7 − − − − − +
tion limited to the apical portion of an Sussman et al34 − − − − − +
implant and diagnosed as radiolucency Sussman et al15 − − − − − +
around the apex of the fixture.7 Bretz et al16 − − − − − +
Sussman et al29 − − − − − +
Inclusion and Exclusion Criteria Shaffer et al14 − − − − − +
The applied inclusion criteria for Piattelli et al17 − − − − − +
the studies were as follows: Scarando − − − − − +
et al26
1. Investigated symptoms, possible Ayangco et al35 − − − − − +
risk factors, treatment methods, Brisman et al10 − − − − − +
and outcomes for retrograde Jalbout et al18 − − − − − +
periimplantitis in patients with at Flanagan et al30 − − − − − +
least one osseointegrated rough- Oh et al11 − − − − − +
surface, solid screw–type implant Park et al27 − − − − − +
that presented the signs of retro- Tseng et al19 − − − − − +
Ataullah et al20 − − − − − +
grade periimplantitis
Tözüm et al12 − − − − − +
2. Reporting on various retrograde
Tözüm et al21 − − − − − +
periimplantitis treatment meth- Lin et al36 − − − − − +
ods, treatment outcomes had to Steiner et al22 − − − − − +
include implant functioning after Dahlin et al37 − − − − − +
the surgery Waasdorp − − − − − +
3. Various times of follow-up. et al23
Chan et al28 − − − − − +
The following types of articles Mohamed − − − − − +
were excluded as follows: et al24
Kutlu et al38 − − − − − +
1. In vitro and animal studies; studies Quaranta et al25 − − − − − +
based on charts or questionnaires Mohamed − − − − − +
2. Studies of patients with immuno- et al31
logic diseases, uncontrolled diabetes +, low risk; −, high risk.

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 RAMANAUSKAITE
Table 3. Study Characteristics
Symptoms
Fistula/ Radiographic
Sinus Implant Periapical
Author Gender Cases/Implant Region Time of Diagnosis Abscess Tract Swelling Pain Mobility Radiolucency
McAllister et al7 Female Case 1, 4 implants in maxilla anterior region, 3 mo + +

ET AL
teeth 7, 8, 9, 10 region
Female Case 2, teeth 10–11 area 7 mo − + − − − +
Sussman et al15 Female Maxillar 1st left molar, tooth 14 1 mo − − + − − +
Sussman et al16 Female Mandibular incisors, teeth 23, 24, 25, 26 1 mo + +
Bretz et al29 Male Maxillary left lateral incisor, tooth 10 6 mo + +
Sussman et al17 Female Mandibular 1st premolar area 1 mo + +
Shaffer et al14 Male Case 1, mandibular right premolar, teeth 2 mo + +
28, 20 area
Male Case 2, maxilla right premolar, teeth 5, 6 3 mo + + +
area
Female Case 3, mandibular right canine, tooth 27 4 mo + +
Male Case 4, maxilla right 2nd premolar and 2 mo + +
lateral incisor, teeth 4 and 7
Piattelli et al26 Female Maxilla right 1st premolar, tooth 5 7 mo + +
Scarano et al35 Female Mandibular right premolar, tooth 28 6 mo − + +
Ayangco et al10 Female Case 1, maxillary left 1st premolar, tooth 12 18 mo + + +
Female Case 2, maxillary left 2nd premolar, tooth 9 mo − − +

IMPLANT DENTISTRY / VOLUME 25, NUMBER 5 2016

13
Female Case 3, mandibular right canine, tooth 27 1 mo − + +
Brisman et al18 Male Case 1, mandibular left/right lateral incisors, 6 wk + +
teeth 23 and 26
Male Case 2, mandibular 1st and 2nd molars 4 mo + +
Male Case 3, mandibular 1st and 2nd molars 4 mo +
Female Case 4, mandibular 2nd premolar 2 wk + + +
Jalbout et al30 Male Case 1, maxillary right 1st premolar, tooth 5 2 mo after prosthetic + + + +
rehabilitation; 14 mo after
placement
Male Case 2, maxillary left central incisor, tooth 9 5 mo + + +
Female Case 3, maxillary right central incisor, 13 mo + +
tooth 8
Female Case 4, maxillary right 1st premolar, tooth 5 3 mo after loading + +
Flanagan et al11 Female Maxillary left 1st premolar, tooth 12 10 wk + + +
Oh et al19 Female Mandibular right 1st molar, tooth 30 3 mo + +
Park et al27 Male Maxillary right 2nd premolar, tooth 4 20 d + +
Tsneg et al20 Female Mandibular right 2nd premolar, tooth 29 6 mo + +
Ataullah et al12 Male Maxillary left central incisor, tooth 9 2 mo − + + − +
Tözüm et al21 Male Maxillary right lateral incisor, tooth 7 5y + +
Tözüm et al36 Female Maxillar left lateral incisor, tooth 10 6 mo + + +
Lin et al22 Female Maxillary left 1st premolar, tooth 12 − − +
Steiner et al37 Female Maxillary left lateral incisor, tooth 10 14 mo +

(continued on next page)

687
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 688
Table 3. (Continued)

Symptoms

APICAL/RETROGRADE PERI-IMPLANTITIS
Fistula/ Radiographic
Sinus Implant Periapical
Author Gender Cases/Implant Region Time of Diagnosis Abscess Tract Swelling Pain Mobility Radiolucency
Dahlin et al23 Male Maxillary right lateral incisor, tooth 7 1y + − +
Male Mandibular right canine region (tooth 27 2y − + + − +
region)
Waasdorp et al28 Male Mandibular left lateral incisor, tooth 23 4 mo − − − +
Chan et al24 Male Case 1, mandibular right central incisor, 3 mo +
tooth 25
Female Case 2, maxillary left 1st premolar, tooth 12 1 wk + − +
Mohamed et al38 Male Maxillary left 2nd lateral incisor, tooth 10 4 mo − − − − +
Kutlu et al25 Female Maxillary left lateral incisor, tooth 10 9 mo (3 mo after prosthetic + + +
rehabilitation)
Quaranta et al31 Female Maxillary left 1st premolar, tooth 12 3 mo + + +
Mohamed et al13 Female Case 1, mandibular left central incisor, tooth 6 wk + +
2015 24
Male Case 2, maxillary left central incisor, tooth 9 2 wk + +
Male Case 3, mandibular left central incisor, tooth 24 1 mo + +
Male Case 4, maxillary left central incisor, tooth 8 2 wk + +

Risk factors
Adjacent Teeth With Tooth Removal Due to Immediate Tooth Trauma Guided Bone Regeneration Before
Author Endodontic Pathology Periapical Pathology Placement Before Removal Implant Placement
McAllister et al7 + + −
− + − − −
Sussman et al15 + − − − Autogenous bone and a calcium sulfate barrier for
alveolar ridge preservation
Sussman et al16 −
Bretz et al29 −
Sussman et al17 −
Shaffer et al14 −
−
+ + −
−
Piattelli et al26 + − −
Scarano et al35 − −
− − −

RAMANAUSKAITE
Ayangco et al10 +
+ − − −
+ − − −
Brisman et al18 + + −
+ −
+ −
+ − − Alloplastic bone graft

ET AL
(continued on next page)

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 RAMANAUSKAITE
Table 3. (Continued)

Risk factors
Adjacent Teeth With Tooth Removal Due to Immediate Tooth Trauma Guided Bone Regeneration Before
Author Endodontic Pathology Periapical Pathology Placement Before Removal Implant Placement
Jalbout et al30 −

ET AL
+ −
Particulated bovine bone and nonabsorbable
titanium-reinforced membrane
−
Flanagan et al11 − + − −
Oh et al19 + + −
Park et al27 −
Tsneg et al20 −
Ataullah et al12 − + − − Autogenous bone + anorganic hydroxyapatite
Tözüm et al21 + + −
Tözüm et al36 −
Lin et al22 + −
Steiner et al37 + −
Dahlin et al23 + − −
− − + −
Waasdorp et al28 − + − Autogenous bone + collagen membrane
Chan et al24 + − Allograft + collagen plug

IMPLANT DENTISTRY / VOLUME 25, NUMBER 5 2016

− − − −
Mohamed et al38 + − + + −
Kutlu et al25 + Xenograft + collagen membrane
Quaranta et al31 + −
Mohamed et al13 + + − − +
2015
+ − + −
− Autogenous block graft
+ −
+, present; −, absent.

689
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 690
Table 4. Treatment Methods
Author Cases Regenerative Treatment Bone Substitute Other Materials Used
McAllister et al7

APICAL/RETROGRADE PERI-IMPLANTITIS
Case 1; Case 2 + Demineralized freeze-dried bone allograft
Sussman et al15 1
Sussman et al16 1
Bretz et al29 1 + Demineralized freeze-dried bone
Sussman et al17 1
Shaffer et al14 Case 1
Case 2 + Demineralized freeze-dried bone + tetracycline
Case 3
Case 4
Piattelli et al26 1
Scarando et al35 1
Ayangco et al10 Case 1
Case 2
Case 3
Brisman et al18 Case 1
Case 2
Case 3
Case 4
Jalbout et al30 Case 1 + Particulate bovine bone
Case 2 + Particulate bovine bone
Case 3 + Demineralized bone matrix
Case 4 + Perioglass
Flanagan et al11 1 Calcium hydroxide paste
Oh et al19 1
Park et al27 1
Tseng et al20 1
Ataullah et al12 1 + Anorganic hydroxyapatite (Bio-Oss)
Tözüm et al21 1 + Calcium sulfate
Tözüm et al36 1 + Synthetic resorbable allograft and calcium sulfate
Lin et al22 1 + Enamel matrix protein derivate
Steiner et al37 1
Dahlin et al23 Case 1
Case 2
Waasdorp et al28 1
Chan et al24 Case 1 + Allograft + tetracycline powder
Case 2 + Allograft
Mohamed et al38 1 + Xenograft + platelet-rich fibrin
Kutlu et al25 1 + Xenograft cortical-cancellous bone Platelet-rich fibrin
Quaranta et al31

RAMANAUSKAITE
1 +
Mohamed et al13 2015 Case 1
Case 2 + Calcium phosphate and hydrase
Case 3 + Bioceramic bone graft
Case 4

(continued on next page)

ET AL
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 RAMANAUSKAITE
Table 4. (Continued)

Nonsurgical Implant
Author Membrane Decontamination Apicoectomy Treatment Follow-up Removal
McAllister et al7 + Tetracycline HCL on titanium fixtures, Primary antibiotic therapy (amoxicillin Case 1: 4 mo; Case 2:
40% citric acid on 2050 mg + metronidazole not reported
hydroxyapatite-coated fixtures 250 mg) failed

ET AL
Sussman et al15 +
Sussman et al16 +
Bretz et al29 + Chlorhexidine gluconate 17 mo
Sussman et al17 +
Shaffer et al14 +
+ + Not reported
+ Not reported
+
Piattelli et al26 +
Scarando et al35 +
Ayangco et al10 Tetracycline paste 8 mo
Tetracycline paste 1y
Tetracycline paste 8y
Brisman et al18 +
+
+
+
Jalbout et al30 + + 22 mo

IMPLANT DENTISTRY / VOLUME 25, NUMBER 5 2016

+ 24 mo
4 mo
7y
Flanagan et al11 No decontamination 11 mo
Oh et al19 +
Park et al27 +
Tseng et al20 +
Ataullah et al12 + Saline + chlorhexidine 3 mo
Tözüm et al21 + 6 mo
Tözüm et al36 + 6 mo
Lin et al22 2 min 24% EDTA 18 mo
Steiner et al37 Conservative treatment of adjacent tooth 14 mo
Dahlin et al23 + 1y
+ 3y
Waasdorp et al28 Amoxicillin 500 mg three times a day, 10 d 1y
Chan et al24 Chlorhexidine gluconate 6 mo
+ 6 mo
Mohamed et al38 Universal Implant Deplaquer (Straumann) 4 mo
Kutlu et al25 + Chlorhexidine gluconate + sterile saline + 12 mo
Quaranta et al31 + Tetracycline paste 5y
Mohamed et al13 2015 Universal Implant Deplaquer (Straumann) 1y
Universal Implant Deplaquer (Straumann) 1y
+ Universal Implant Deplaquer (Straumann) 1y
+

691
+, present.

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692 APICAL/RETROGRADE PERI-IMPLANTITIS RAMANAUSKAITE ET AL

“Time of diagnosis”dDescribed the Assessment of Methodological Quality and when the test of normality of the
time of diagnosis of retrograde The quality of all included studies investigated variables was denied, Wil-
periimplantitis after implant was assessed during the data extraction coxon nonparametric test. Chi-square
placement process. The quality appraisal involved (x2) tests were used to compare fre-
“Symptoms”dDescribed the evaluating the methodological ele- quencies of qualitative variables.
observed clinical symptoms, ments that might influence the out- Linear relationship of the variables
including abscess formation, fis- comes of each study. was assessed using Spearman correla-
tula/sinus tract, swelling, pain, The Cochrane Collaboration’s tion in accordance with probability
implant mobility, radiographic two-part tool for assessing risk of bias distribution of the variables. To
periapical radiolucency (Higgins and Green39 2011) was used to assess minimally false and minimally
“Risk factors”dDescribed the pos- assess bias across the studies and iden- false-positive results with greatest accu-
sible risk factors, including adja- tify articles with intrinsic methodologi- racy, the method of ROC (receiver
cent teeth with endodontic cal and design flaws (Table 4). operating characteristics) curve was
pathology, tooth removal due used. Logistic regression analysis was
to periapical pathology, immedi- Statistical Analysis performed to determine the odds ratio
ate placement, tooth trauma Statistical analysis of the data was (OR) predictive value. Differences
before removal, guided bone performed using a software package for between groups were considered signif-
regeneration before implant storage and analysis of data, SPSS 22.0 icant when the level of significance
placement (Statistical Package for Social Science P was less than ,0.05.
“Regenerative treatment”dIndicated 22 for Windows, Armonk, NY). All
articles where surgical regenera- parametric data are expressed as the
tive treatment of retrograde peri- mean 6 SD. The Kolmogorov- RESULTS
implantitis was used Smirnov test was used for determina-
“Bone substitute”dDescribed the tion of quantitative data distribution. Study Selection
bone substitute materials used When the distribution of variables was The initial search displayed a total
for regenerative treatment normal, Student t test was used to com- of 70 articles. After the screening of
“Other material”dDescribed mate- pare quantitative sizes of two indepen- the article titles and abstracts, 33 poten-
rials other than bone substitutes dent samples. The Mann-Whitney U tially relevant articles were identified
used for regenerative treatment test was used to compare nonnormally and selected for full-text reading (Fig.
“Membrane”dIndicated articles distributed variables. Quantitative data 1). In total, 44 cases published by 27
where membrane was used dur- when distribution was normal were authors from 1992 to 2015 were re-
ing surgical treatment used in the Student t two-sided test viewed (Tables 2 and 3). No cohort,
“Decontamination”dDescribed
decontamination method used
for implant surface during sur-
gical treatment
“Apicoectomy”dIndicated articles
where implant apicoectomy
was performed during surgical
treatment
“Nonsurgical treatment”dDescribed
nonsurgical treatments used in
retrograde periimplantitis cases
“Follow-up”dDescribed the dura-
tion of the observed treatment
outcomes
“Implant removal”dIndicated ar-
ticles where implants diagnosed
with retrograde periimplantitis
were removed.

Synthesis of Results
Relevant data of interest regarding
the previously stated variables were
collected and organized into 2 tables
based on the assessed treatment method Fig. 1. PRISMA flow diagram.
(Tables 2 and 3).

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RAMANAUSKAITE ET AL IMPLANT DENTISTRY / VOLUME 25, NUMBER 5 2016 693

Table 5. Symptoms of retrograde periimplantitis mobile implant cases. The results found
as well a tendency of earlier diagnosis
Maxilla Mandibula of retrograde periimplantitis in cases
Symptoms/Possible No. of No. of No. of with implant mobility: time of diagno-
Risk Factors Cases (%) P* Cases (%) Cases (%) P† sis in cases of nonmobile implants,
Abscess 4 (9.1) 0.001 1 (3.6) 3 (18.8) 0.129 6.155 (SD 6 12.6) weeks; in cases with
Fistula/sinus tract 21 (47.7) 0.763 18 (64.3) 3 (18.8) 0.004 mobile implants, 6.667 (SD 6 8.1)
Swelling 10 (22.7) 0.001 7 (25) 3 (18.8) 0.634 weeks; P ¼ 0.15.
Pain 15 (34.1) 0.035 9 (32.1) 6 (37.5) 0.718 The implants that were removed
Implant mobility 3 (6.8) 0.001 2 (7.1) 1 (6.3) 1.0 were diagnosed with retrograde periim-
*P value by chi-square (x2) goodness of fit test.
†P value by Fisher exact test.
plantitis significantly earlier (P ¼
0.028) as compared with the implants
that were treated for the pathology.
case-controlled, or case series studies Time of Diagnosis Using the ROC curve method, the opti-
except case reports were available. Forty-two cases were reported on mal diagnosis time was searched, which
time from implant placement until diag- was found to be 28 weeks, meaning that
Study Exclusion nosis of retrograde periimplantitis was all implants that were removed were
Three articles were excluded made (Table 2). The average time of the diagnosed with the pathology up to 28
because they described implant periap- diagnosis of the pathology was 26.07 weeks (P ¼ 0.016). On a contrary, a bit
ical lesions in general, not particular (SD 6 39.7) weeks after implant place- more than half of the remaining cases
cases.9,32,40 Two studies were excluded ment (minimum, 1 week; maximum, (66.7% of implants) that were not
because they did not provide detailed 240 weeks; median, 16). Time of diag- removed but treated were diagnosed
description on retrograde periimplanti- nosis for symptomatic cases (according with the pathology up to week 28.
tis symptoms and treatment proto- to Reiser et al,32 cases exhibiting pain,
col.8,40 In addition, one article was swelling, abscess, and/or fistula) and for Symptoms and Risk Factors
excluded, because it was a review nonsymptomatic cases did not differ All cases demonstrated radiolu-
article.34 significantly (P . 0.05). There is a ten- cency radiographically at the apex of
dency in that if the case demonstrates the implant (100%). Thirty-seven of 44
Quality Assessment fistula, the time of diagnosis is later cases (according to Reiser et al32) could
Summarizing the risk of bias for (P ¼ 0.11); average time of diagnosis be referred to as infected cases. Seven
each study, all 27 studies were classified in cases demonstrating fistula, 33.1 cases were10,18,22,24,28,37,38 diagnosed
as high risk (of bias for 1 or more key (SD 6 51.807) weeks; with no fistula, only radiographically and could be con-
domains; Table 4).7,10–31,35–38 18.91 (SD 6 23.067) weeks. sidered inactive.32 There was no differ-
There is a tendency that cases ence of the active lesions (exhibiting
Study Characteristics demonstrating implant mobility were pain, swelling, and abscess) to develop
The cases included 20 (45.5%) men diagnosed with retrograde periimplan- in the maxilla or mandible.
and 24 (54.5%) women, with an aver- titis earlier: 39 cases of nonmobile Considering all the symptoms eval-
age age of 47.1 (SD 6 15.9; minimum, implants were diagnosed with retro- uated, only fistula formation was pre-
18; maximum, 76; median, 47) at the grade periimplantitis at around 27.56 sented in the higher part of the cases
time of diagnosis of retrograde periim- (SD 6 40.78) weeks; and the average (Table 5). Fistula formation was signif-
plantitis. Twenty-eight cases (63.6%) time of diagnosis in 3 cases13,18 present- icantly more often diagnosed in maxilla
reported on retrograde periimplantitis ing mobile implants was 6.67 (SD 6 (P ¼ 0.04). A tendency was found for
in the maxilla and 16 (36.4%) in the 8.1) weeks (P ¼ 0.082). To enhance the case to develop fistula if the tooth
mandible. There was no difference of significance, six random samples of was removed because of periapical
the disease occurrence between the cases with nonmobile implants of 39 pathology (P ¼ 0.07).
jaws (P ¼ 0.07; Table 2). cases were selected and compared with Five possible risk factors, includ-
ing adjacent teeth with endodontic
Table 6. Possible Risk Factors of Retrograde periimplantitis pathology, tooth removal due to peri-
apical pathology, immediate implant
No. of
placement, tooth trauma before
Possible Risk Factors Cases (%) P
removal, and guided bone regenera-
Adjacent teeth with endodontic pathology/incomplete 14 (31.8) 0.016 tion before implant placement, were
endodontic treatment evaluated (Table 6). Adjacent teeth
Tooth removal due to periapical pathology 15 (34.1) 0.035 with endodontic pathology/incom-
Immediate placement 2 (4.5) 0.001 plete endodontic treatment and tooth
Trauma before tooth removal 7 (15.9) 0.001 removal due to periapical pathology
Guided bone regeneration before implant placement 8 (18.2) 0.001
were the most common risk factors
Implant removal 15 (34.1) 0.035
found in the clinical cases included in

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694 APICAL/RETROGRADE PERI-IMPLANTITIS RAMANAUSKAITE ET AL

Table 7. Summarized Treatment Methods Used for Retrograde Periimplantitis in the probability that it was caused not by
Case Reports Included the adjacent tooth (OR [95% CI],
11.375 [1.316–98.311]). There were
Maxilla Mandibula 14 cases (46.7%) presenting pain and
No. of No. of No. of exhibiting no adjacent teeth with peri-
Treatment Methods Cases (%) Cases (%) Cases (%) P apical pathology, whereas 1 case
Implant removal13–20,26,27,35 15 (35.7) 5 (18.5) 10 (66.7) 0.001 (7.8%) exhibited pain and adjacent
Nonsurgical23,24 2 (4.5) 1 (3.6) 1 (6.3) 1.0 tooth with the periapical pathology
Open-flap debridement10,11,13,14,23 8 (18) 4 (14.3) 4 (25.0) 0.434 (P ¼ 0.01).
Regenerative 19 (45.2) 18 (66.7) 1 (6.7) ,0.001
Bone + membrane 11 (57.9) Treatment
Allograft7,14,29 Two cases were solved with non-
Xenograft12,25,30 surgical treatment (Tables 3 and
Alloplast36
7).28,37 The case of retrograde periim-
Allograft + alloplast13,21
plantitis by Steiner et al22 was diag-
Vicryl barrier7,14
Bioabsorbable collagen
nosed only radiographically, without
membrane12,13,21,25,29,30,36
any clinical symptoms, and was
Bioabsorbable glycolic and lactic 5 (26.3) caused by endodontic pathology
copolymers’ membrane30 involving teeth adjacent to an
Bone substitute alone implant.37 Endodontic treatment
Xenograft38 resolved the lesion and retained both
Alloplats13,30 1 (5.3) the implant and the tooth at the 14-
Allograft24,30 1 (5.3) month follow-up. The case reported
Enamel matrix protein derivate22 by Waasardorp et al28 was asymptom-
Calcium hydroxide paste11 1 (5.3) atic and was solved by placing the
Tetracycline paste + bioabsorbable patient on a 10-day course of amoxi-
pericardium membrane31 cillin (500 mg three times daily).28 In
an 11-month follow-up, a previously
large radiolucency surrounding the
the review. However, none of the risk A negative correlation was found apex of the implant was undetectable
factors were shown to be statistically between adjacent tooth with endodon- by radiographic examination.28
significantly related to retrograde tic pathology and pain (r ¼ −0.4; P ¼ Fifteen implants (35.7%) were
periimplantitis. 0.009), showing that if the case removed.13–20,27,35 Five (18.5%) im-
presented pain, there was a higher plants were removed in maxilla and 10
(66.7%) in mandible, which is statisti-
cally significantly higher in mandible
(x2 ¼ 14.646; DF ¼ 2; P ¼ 0.001).
Correlation was found between the
cases presenting adjacent tooth with
endodontic pathology and implant
removal (r ¼ 0.3; P ¼ 0.028), meaning
that most implants with retrograde peri-
implantitis adjacent to the tooth pre-
senting endodontic pathology were
removed instead of treating the case
(OR [95% CI], 4.381 [1.13–16.985]).
Eight cases (53.3%) exhibited teeth
with endodontic periapical pathology,
and the implants were removed; in 6
cases (27%), the implants were treated
(P ¼ 0.028).
Twenty-seven cases were surgi-
cally treated: eight of them using
open-flap debridement (18%) and 19
using regenerative approach (45.2%).
Regenerative treatment was statistically
Fig. 2. A decision-making tree of retrograde periimplantitis management. significantly more often used in maxilla
than mandible (maxilla 18 [66.7%],

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RAMANAUSKAITE ET AL IMPLANT DENTISTRY / VOLUME 25, NUMBER 5 2016 695

mandible 1 [6.7%]; P , 0.001). Differ- of periapical pathology. This corre- Based on these case reports, it
ent materials were used for bone defect sponds to the results of a retrospective seems that the treatment of retrograde
regeneration: bone (allogenic,7,14,24,28,29 study by Quirynen et al8 that aimed to periimplantitis is empirical. In the pres-
xenogenic,12,25,30,38 alloplastic13,21,22) find predisposing conditions for retro- ent review, 35.7% of the implants,
and substitutes with7,12–14,21,25,29,30,36 or grade periimplantitis. They found that diagnosed with retrograde periimplan-
without membranes,24,30,31,38 calcium the extraction sites of teeth with a his- titis, were removed. Statistically signif-
hydroxide paste,22 enamel matrix pro- tory of endodontic pathology and sites icantly more implants were removed in
tein derivates,11 and tetracycline paste adjacent to teeth with an obvious the mandible (P ¼ 0.001) and when
in combination with collagen mem- endodontic pathology provoked the there was an adjacent tooth with end-
brane31 (Tables 3 and 7). pathology. In a study by Zhou et al,41 odontic pathology (P ¼ 0.028).
Implant surface decontamination retrograde periimplantitis was diagnosed Open-flap surgery was performed
was performed in 14 surgical cases of for 7.8% of the implants that were adja- in 18% of the cases and regenerative
29 using different methods: tetracycline cent to an endodontically treated tooth. It treatment in most cases (45.2%).
paste (5 cases),7,10,31 40% citric acid (1 was stressed that the incidence of retro- Regenerative treatment was statistically
case),7 chlorhexidine (4 cases),12,24,25,29 grade periimplantitis may be reduced by significantly more often used in maxilla
EDTA 24% (1 case),22 and Straumann increasing the distance between the (P , 0.001). All surgically treated
Universal Implant Deplaquer (4 implant and the adjacent tooth and/or cases, despite the technique applied,
cases).13,36 Apicoectomies of the implant the duration of endodontically treated remained osseointegrated and contin-
were performed in 6 cases14,23,25,30 adjacent tooth-to-implant placement. ued to function successfully for up to
(Table 3). Brisman et al18 reported four cases 20.3 months (SD 6 24.9) with no sig-
All surgically treated cases re- in which even an asymptomatic, end- nificant difference. Whether regenera-
mained osseointegrated and continued odontically treated tooth with a normal tive treatment gives superior results is
to function successfully for up to 20.3 periapical radiographic appearance was impossible to conclude based only on
(SD, 6 24.9; minimum, 3; maximum, the cause of an implant failure. It has these case reports. Data from longitudi-
96; median, 12) months. For the cases been shown that even if a periapical area nal studies are required.
treated with regenerative approach, the seems to have been resolved on a radio- A decision-making tree of retro-
follow-up time was 17.6 (SD, 6 graph, micro-organisms may persist grade periimplantitis management was
21.9; minimum, 3; maximum, 84; indefinitely. Therefore, an asymptom- developed, which can be used as a guide
median, 12) weeks, and for the open- atic, endodontically treated tooth may to assist clinicians in making diagnosis
flap curettage cases, 26.7 (SD, 6 harbor a chronic infection, which may leading to the proper management of
32; minimum, 8; maximum, 96; median, cause implant failure.18,41 the pathology and aimed to save the
12) weeks (P ¼ 0.275 by Mann- When evaluating the symptoms, all implant (Fig. 2).
Whitney) with no significant difference. cases presented radiographic radiolu- The first step is to verify the exis-
cency at the apex of an implant and tence of bone loss. Conventional bitew-
higher part of the cases presented fistula ings and periapical radiographs are
DISCUSSION (P ¼ 0.763). Fistula was more often adequate to evaluate the bone around
This investigation included studies present in maxilla (P ¼ 0.04) and in the implants.32,42 If marginal bone
reporting the symptoms, possible risk cases where tooth was removed because loss, which extends more than 2 mm
factors, treatment methods, and out- of periapical pathology (P ¼ 0.07). beyond crown/abutment-implant junc-
comes for retrograde periimplantitis. Negative correlation was found tion, could be observed on the radio-
An electronic search of MEDLINE between pain and adjacent tooth with graph, and bleeding on probing and/or
(PubMed) and EMBASE databases incomplete endodontic treatment/end- suppuration and pocket depth $4 mm
was performed, including studies pub- odontic pathology (P ¼ 0.009) and, on are found, the diagnosis of marginal
lished in the English language between a contrary, a positive correlation periimplantitis should be made.43
January 1, 1990, and May 1, 2015. between the latter risk factor and If radiolucency at the apex on an
Additionally, a hand search was per- implant removal (P ¼ 0.028). implant could be observed, the diagno-
formed in the dental implants and Once diagnosed, identification of the sis of retrograde periimplantitis should
endodontics-related journals. cause and removal of the infection source be made.32 The next step would be to
The results of this review suggest could limit the extent of the disease evaluate possible etiological and/or risk
that retrograde periimplantitis was progression and possibly result in saving factors. According to it, retrograde peri-
diagnosed at 26.07 (639.7) weeks after the implant. According to Reiser et al,32 implantitis could be categorized as
implant placement and is most com- infected presentations of retrograde peri- infective, caused by the adjacent tooth
monly associated with the infection implantitis require surgical interven- with endodontic pathology, root frac-
from adjacent teeth with periapical tion.32 However, Sussman et al15–17 are ture of adjacent tooth, persisting pathol-
pathology and/or incomplete endodon- of the opinion that the implant should ogy in the bone, or chronic periodontitis
tic treatment, and with residual infec- be extracted immediately to prevent oste- of adjacent tooth; traumatic retrograde
tion at the site of tooth extraction, omyelitis, because retaining the implant periimplantitis due to the bone over-
when the tooth was removed because may lead to irreversible bone loss.15–17 heating during site preparation or

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696 APICAL/RETROGRADE PERI-IMPLANTITIS RAMANAUSKAITE ET AL

bone overcompression during fixture and render the surface conductive to bone tooth or persisting bone infection. It is
placement, or impaired bone healing regeneration and reosseointegration.44 most often diagnosed at week 26 (SD 6
(impaired osseointegration); and retro- Chlorhexidine digluconate (0.2%) dem- 39.7 weeks) as radiolucency around the
grade periimplantitis that occurred onstrated a great decontamination capac- apex of the implant. The most common
because of other possible etiological ity with respect to both the killing and clinical symptom is fistula, which is sta-
and/or risk factors, such as incorrect the removal of biofilm cells.44 Therefore, tistically significantly more often found
implant positioning, etc. we would suggest using chlorhexidine in maxilla (P ¼ 0.04). Treatment of ret-
If the case presents implant mobil- digluconate for decontamination. rograde periimplantitis is empirical.
ity with or without clinical symptoms, To obtain optimal treatment re- The most often used treatment methods
the implant must be removed despite sults, we would recommend using the were the surgical regenerative approach
the possible etiological and/or risk regenerative treatment approach. We or implant removal. We suggested
factor. suggest using bone substitute to fill the a decision-making tree, which suggests
If there are symptoms such as bone defect that would act as a scaffold choosing the management of the
swelling and/or fistula and/or pain or for new bone cells to growth into the pathology according to its possible eti-
no clinical symptoms, just radiographic bony defect, maintain space, and there- ological/risk factors. Yet, randomized
periapical bone lesion, and an adjacent fore prevent deformities of the soft controlled trials with follow-ups of sev-
tooth with periapical lesion or incom- tissues.45 Clinical and experimental eral years and large sample sizes are
plete endodontic treatment, or root frac- studies provided significant evidence needed to determine the best treatment
ture, endodontic treatment/re-treatment that bone regeneration is significantly to control retrograde periimplantitis.
at the first treatment stage, the case is to enhanced when the invasion of soft tis-
be an infective. If there is a neighboring sue into osseous defects is mechanically
tooth with root fracture, the tooth has to impeded, allowing only osteogenic cell DISCLOSURE
be removed. The patient should be fol- populations derived from the parent The authors claim to have no
lowed up every 2 weeks, and at 1-2-3-6 bone to repopulate the osseous wound financial interest, either directly or
months for 2 years to ensure that the space.45,46 Therefore, we would recom- indirectly, in the products or informa-
healing takes place and the symptoms mend using resorbable collagen mem- tion listed in the article.
resolve. If the symptoms do not resolve, brane over the bone grafting material.
surgical treatment should be indicated. Systemic antibiotics as an adjunct to
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