684 APICAL/RETROGRADE PERI-IMPLANTITIS
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-
I established treatment method for
replacing missing teeth. Several
studies have provided a high level of
evidence supporting the favorable
long-term survival and success rate
of implant therapy in general popula-
tions.1,2 Although the success rate of
dental implants is high, there are risks
of developing infectious complica-
tions.3
Infectious dental implant failures
can be divided into marginal periim-
plantitis and retrograde (or apical) peri-
implantitis. Periimplantitis has been
characterized as an inflammatory pro-
cess around an implant, which includes
both soft tissue inflammation and pro-
gressive loss of supporting marginal
bone beyond biological bone remodel-
ing.3 It is often associated with bleeding
at the periimplant margin after the inser-
tion of a periodontal probe into the peri-
implant space, increased periimplant
pocket-probing depth, mucosal reces-
sion, and/or suppuration.4 Periimplantitis
*PhD student, Clinic of Dental and Oral Pathology, Lithuanian
University of Health Sciences, Kaunas, Lithuania.
†Professor, Department of Maxillofacial Surgery, Lithuanian
University of Health Sciences, Kaunas, Lithuania.
‡Associate Professor, Department of Periodontics, College of
Dentistry, University of Illinois at Chicago, Chicago, IL.
Reprint requests and correspondence to: Tolga F. Tözüm,
DDS, PhD, Department of Periodontics, College of
Dentistry, University of Illinois at Chicago, Room 469G,
801 S. Paulina Street, Chicago, IL 60612, Phone: 312-
996-0265, Fax: 312-996-0943, E-mail: ttozum@uic.edu
ISSN 1056-6163/16/02505-684
Implant Dentistry
Volume 25
Number 5
Copyright © 2016 Wolters Kluwer Health, Inc. All rights
reserved.
DOI: 10.1097/ID.0000000000000424
Copyright Ó 2016 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
Objectives: To review the litera-
ture on retrograde periimplantitis
symptoms, risk factors, and treat-
ment methods and to propose a deci-
sion-making tree of retrograde
periimplantitis management.
Materials and Methods: An
electronic literature search was
conducted on the MEDLINE and
EMBASE databases for articles pub-
lished between 1990 and 2015. Clin-
ical human studies in the English
language were included.
Results: The search resulted in
44 case reports published by 27
authors. The average time of the
diagnosis of the pathology was found
to be 26.07 weeks after implant
placement (SD 6 39.7). Fistula for-
mation was found to be the most com-
mon clinical symptom, statistically
significantly more often occurring in
the maxilla (P ¼ 0.04). A negative
correlation was found between pain
was reported to occur in 18.8% of sub-
jects and 9.6% of implants.5 If periim-
plantitis is left undetected and untreated,
it will progress further and eventually
result in the loss of the implant.6
Retrograde periimplantitis (periap-
ical implant lesion; implant periapical
pathology, apical periimplantitis) was
first described in 1992 by McAllister
et al7 as an infectious-inflammatory
process in the tissues surrounding the
RAMANAUSKAITE ET AL
and the adjacent tooth with incom-
plete endodontic treatment/endodon-
tic pathology (r ¼ −0.4; P ¼ 0.009)
and a positive correlation between
the later risk factor and implant
removal (r ¼ 0.3; P ¼ 0.028). Regen-
erative treatment (45.2% of the cases)
or implant removal (35.7% of the
cases) was the most common treat-
ment techniques used. A decision-
making tree of retrograde periim-
plantitis management is suggested.
Conclusions: The etiology of
retrograde periimplantitis is most
often infectious. A decision-making
tree aimed at managing patients with
retrograde periimplantitis according
to the possible etiology and symptoms
of the disease can be a useful tool in
the treatment of the pathology.
(Implant Dent 2016;25:684–697)
Key Words: dental implants, periap-
ical periodontitis, bone regenera-
tion, apicoectomy, reoperation
implant apex. The pathology develops
shortly after implant insertion, while the
coronal portion of the implant achieves
a normal osseointegration.7 Of the 539
implants evaluated in a retrospective
study, this pathology was found to
occur in 1.6% of the implants in the
upper jaw and 2.7% in the lower jaw.8
Retrograde periimplantitis is a rapid
infective process, and it can not
only potentially cause devitalization of
RAMANAUSKAITE ET AL IMPLANT DENTISTRY / VOLUME 25, NUMBER 5 2016
adjacent teeth but also greatly reduce A periapical radiograph is the stan-
bone for future implants if not treated dard diagnostic indicator of an implant
early.9 periapical lesion, but it does not distin-
Many possible etiological factors guish between inactive and infected
have been associated with the periapical lesions.32 Reiser et al32 classified implant
implant pathology (Table 1). However, periapical lesions as noninfecteddthey
based on the case reports analyzed, it are diagnosed radiographically but do
seems that retrograde periimplantitis is not present any clinical symptoms. Such
most commonly associated with the lesions do not require any treatment,
infection from adjacent teeth with peri- unless there is an increase in the size of
apical pathology and/or incomplete the periapical radiolucency. Infected
endodontic treatment, and with residual lesions are usually accompanied by pain,
infection at the site of tooth extraction, tenderness, swelling, and/or the pres-
when the tooth was removed because of ence of a fistulous tract. Such lesions
periapical pathology. start at the implant apex but exhibit the
It has been suggested that retro- capacity to spread coronally, proxi-
grade periimplantitis resembles mar- mally, and facially. However, if retro-
ginal periimplantitis in that both are grade periimplantitis is not treated
site-specific infective processes.27 The immediately, it usually results in com-
main differences, however, lie in the plete implant loss when the bone loss
microbial composition, rate of expan- progresses to the complete implant
sion, and pathway of the infection. surface.32
Micro-organisms found in periimplan- The aim of this article was to
titis are closely associated with peri- review possible literature on retrograde
odontal pathogens, whereas those periimplantitis symptoms, possible risk
found in retrograde periimplantitis factors, and treatment methods and to
resemble the composition of endodon- propose a decision-making tree of ret-
tic pathogens.7,14 Furthermore, periim- rograde periimplantitis management
plantitis occurs coronally, whereas that could help clinicians cope with
retrograde periimplantitis initiates api- the pathology.
cally. Marginal periimplantitis can be
detected clinically by routine probing, MATERIALS AND METHODS
whereas retrograde periimplantitis re-
lies on patient complaint and radio- Protocol and Registration
graphic assessment.27 The methods of the analysis and
inclusion criteria were specified in
advance and documented in a protocol.
Table 1. Possible Etiological Factors
The review was registered in
Indicated in the Articles
PROSPERO, an international prospec-
No. of tive register of systematic reviews. The
Possible Etiological Factors Cases protocol can be accessed at http://www.
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-
due to the periapical istration number: CRD42015026852.
pathology10–13 The reporting of this systematic analysis
Infection from adjacent teeth 24 adhered to the Preferred Reporting
with periapical pathology Items for Systematic Review and Meta-
and/or incomplete Analyses (PRISMA) statement.33
endodontic treatment7,13–25
Periodontal pathology13 1 Focus Question
Impaired bone healing24 1 What are the symptoms, possible
Bone overheating26 1 risk factors, and treatment methods for
Retained root tip27 1 retrograde periimplantitis?
Excessive tightening during 2 implant lesion” AND (“symptoms”
insertion21,26 Types of Publications
Incomplete implant depth28 1 The review included studies on
Contaminated implant tip21 2 humans published in the English lan-
Questionable etiology23,29–31 7
guage. Letters, editorials, literature
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685
reviews, PhD theses, and abstracts were
excluded.
Types of Studies
The review included all human
prospective and retrospective follow-
up studies, clinical trials, cohort studies,
case-control studies, case series studies,
case reports published between January
1, 1990, and September 1, 2015, that
reported on symptoms, possible risk
factors, treatment methods, and out-
comes for retrograde periimplantitis.
Information Sources
The search strategy incorporated
the examination of electronic data-
bases, supplemented by hand searches.
A search was conducted on the National
Library of Medicine database
(MEDLINE) through its online site
(PubMed) and EMBASE databases.
Additionally, a hand search was con-
ducted in the following journals: Implant
Dentistry; Clinical Oral Implants
Research; Clinical Implant Dentistry
and Related Research; European Journal
of Oral Implantology; International Jour-
nal of Oral & Maxillofacial Implants;
Journal of Oral Implantology; Interna-
tional Journal of Oral and Maxillofacial
Surgery; International Journal of Oral
and Maxillofacial Surgery; Journal of
Periodontology; Journal of Clinical Peri-
odontology; International Journal of
Periodontics and Restorative Dentistry;
Journal of Prosthetic Dentistry; Interna-
tional Journal of Endodontics; Journal
of Endodontics; Oral Surgery, Oral
Medicine, Oral Pathology and Oral
Radiology; and Endodontology; Turkish
Journal of Medical Sciences.
study were screened to discover addi-
tional relevant publications.
Search
The PubMed and EMBASE
resource databases were explored
through advanced searches. The key-
words and search inquiries used during
the primary stage were as follows: “ret-
rograde peri-implantitis” OR “periapi-
cal peri-implantitis” OR “peri-apical
OR “risk factors” OR “treatment”).
The choice of keywords was intended
to be broad to collect as much relevant
data as possible without relying on
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
time of diagnosis of retrograde
periimplantitis after implant
placement
“Symptoms”dDescribed the
observed clinical symptoms,
including abscess formation, fis-
tula/sinus tract, swelling, pain,
implant mobility, radiographic
periapical radiolucency
“Risk factors”dDescribed the pos-
sible risk factors, including adja-
cent teeth with endodontic
pathology, tooth removal due
to periapical pathology, immedi-
ate placement, tooth trauma
before removal, guided bone
regeneration before implant
placement
“Regenerative treatment”dIndicated
articles where surgical regenera-
tive treatment of retrograde peri-
implantitis was used
“Bone substitute”dDescribed the
bone substitute materials used
for regenerative treatment
“Other material”dDescribed mate-
rials other than bone substitutes
used for regenerative treatment
“Membrane”dIndicated articles
where membrane was used dur-
ing surgical treatment
“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.
Assessment of Methodological Quality
The quality of all included studies
was assessed during the data extraction
process. The quality appraisal involved
evaluating the methodological ele-
ments that might influence the out-
comes of each study.
The Cochrane Collaboration’s
two-part tool for assessing risk of bias
(Higgins and Green39 2011) was used to
assess bias across the studies and iden-
tify articles with intrinsic methodologi-
cal and design flaws (Table 4).
Statistical Analysis
Statistical analysis of the data was
performed using a software package for
storage and analysis of data, SPSS 22.0
(Statistical Package for Social Science
22 for Windows, Armonk, NY). All
parametric data are expressed as the
mean 6 SD. The Kolmogorov-
Smirnov test was used for determina-
tion of quantitative data distribution.
When the distribution of variables was
normal, Student t test was used to com-
pare quantitative sizes of two indepen-
dent samples. The Mann-Whitney U
test was used to compare nonnormally
distributed variables. Quantitative data
when distribution was normal were
used in the Student t two-sided test
and when the test of normality of the
investigated variables was denied, Wil-
coxon nonparametric test. Chi-square
(x2) tests were used to compare fre-
quencies of qualitative variables.
Linear relationship of the variables
was assessed using Spearman correla-
tion in accordance with probability
distribution of the variables. To
assess minimally false and minimally
false-positive results with greatest accu-
racy, the method of ROC (receiver
operating characteristics) curve was
used. Logistic regression analysis was
performed to determine the odds ratio
(OR) predictive value. Differences
between groups were considered signif-
icant when the level of significance
P was less than ,0.05.
RESULTS
Study Selection
The initial search displayed a total
of 70 articles. After the screening of
the article titles and abstracts, 33 poten-
tially relevant articles were identified
and selected for full-text reading (Fig.
1). In total, 44 cases published by 27
authors from 1992 to 2015 were re-
viewed (Tables 2 and 3). No cohort,

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
Table 5. Symptoms of retrograde periimplantitis
Symptoms/Possible No. of
Risk Factors Cases (%)
Abscess 4 (9.1)
Fistula/sinus tract 21 (47.7)
Swelling 10 (22.7)
Pain 15 (34.1)
Implant mobility 3 (6.8)
*P value by chi-square (x2) goodness of fit test.
†P value by Fisher exact test.
case-controlled, or case series studies
except case reports were available.
Study Exclusion
Three articles were excluded
because they described implant periap-
ical lesions in general, not particular
cases.9,32,40 Two studies were excluded
because they did not provide detailed
description on retrograde periimplanti-
tis symptoms and treatment proto-
col.8,40 In addition, one article was
excluded, because it was a review
article.34
Quality Assessment
Summarizing the risk of bias for
each study, all 27 studies were classified
as high risk (of bias for 1 or more key
domains; Table 4).7,10–31,35–38
Study Characteristics
The cases included 20 (45.5%) men
and 24 (54.5%) women, with an aver-
age age of 47.1 (SD 6 15.9; minimum,
18; maximum, 76; median, 47) at the
time of diagnosis of retrograde periim-
plantitis. Twenty-eight cases (63.6%)
reported on retrograde periimplantitis
in the maxilla and 16 (36.4%) in the
mandible. There was no difference of
the disease occurrence between the
jaws (P ¼ 0.07; Table 2).
Table 6. Possible Risk Factors of Retrograde periimplantitis
Possible Risk Factors
Adjacent teeth with endodontic pathology/incomplete
endodontic treatment
Tooth removal due to periapical pathology
Immediate placement
Trauma before tooth removal
Guided bone regeneration before implant placement
Implant removal
Copyright Ó 2016 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
IMPLANT DENTISTRY / VOLUME 25, NUMBER 5 2016 693
mobile implant cases. The results found
as well a tendency of earlier diagnosis
Maxilla Mandibula of retrograde periimplantitis in cases
No. of No. of with implant mobility: time of diagno-
P* Cases (%) Cases (%) P† sis in cases of nonmobile implants,
0.001 1 (3.6) 3 (18.8) 0.129 6.155 (SD 6 12.6) weeks; in cases with
0.763 18 (64.3) 3 (18.8) 0.004 mobile implants, 6.667 (SD 6 8.1)
0.001 7 (25) 3 (18.8) 0.634 weeks; P ¼ 0.15.
0.035 9 (32.1) 6 (37.5) 0.718 The implants that were removed
0.001 2 (7.1) 1 (6.3) 1.0 were diagnosed with retrograde periim-
plantitis significantly earlier (P ¼
0.028) as compared with the implants
that were treated for the pathology.
Time of Diagnosis Using the ROC curve method, the opti-
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
nosis of retrograde periimplantitis was all implants that were removed were
made (Table 2). The average time of the diagnosed with the pathology up to 28
diagnosis of the pathology was 26.07 weeks (P ¼ 0.016). On a contrary, a bit
(SD 6 39.7) weeks after implant place- more than half of the remaining cases
ment (minimum, 1 week; maximum, (66.7% of implants) that were not
240 weeks; median, 16). Time of diag- removed but treated were diagnosed
nosis for symptomatic cases (according with the pathology up to week 28.
to Reiser et al,32 cases exhibiting pain,
swelling, abscess, and/or fistula) and for Symptoms and Risk Factors
nonsymptomatic cases did not differ All cases demonstrated radiolu-
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
fistula, the time of diagnosis is later cases (according to Reiser et al32) could
(P ¼ 0.11); average time of diagnosis be referred to as infected cases. Seven
in cases demonstrating fistula, 33.1 cases were10,18,22,24,28,37,38 diagnosed
(SD 6 51.807) weeks; with no fistula, only radiographically and could be con-
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
demonstrating implant mobility were pain, swelling, and abscess) to develop
diagnosed with retrograde periimplan- in the maxilla or mandible.
titis earlier: 39 cases of nonmobile Considering all the symptoms eval-
implants were diagnosed with retro- uated, only fistula formation was pre-
grade periimplantitis at around 27.56 sented in the higher part of the cases
(SD 6 40.78) weeks; and the average (Table 5). Fistula formation was signif-
time of diagnosis in 3 cases13,18 present- icantly more often diagnosed in maxilla
ing mobile implants was 6.67 (SD 6 (P ¼ 0.04). A tendency was found for
8.1) weeks (P ¼ 0.082). To enhance the case to develop fistula if the tooth
significance, six random samples of was removed because of periapical
cases with nonmobile implants of 39 pathology (P ¼ 0.07).
cases were selected and compared with Five possible risk factors, includ-
ing adjacent teeth with endodontic
pathology, tooth removal due to peri-
apical pathology, immediate implant
No. of
placement, tooth trauma before
Cases (%) P
removal, and guided bone regenera-
14 (31.8) 0.016 tion before implant placement, were
evaluated (Table 6). Adjacent teeth
15 (34.1) 0.035 with endodontic pathology/incom-
2 (4.5) 0.001 plete endodontic treatment and tooth
7 (15.9) 0.001 removal due to periapical pathology
8 (18.2) 0.001
were the most common risk factors
15 (34.1) 0.035
found in the clinical cases included in
694 APICAL/RETROGRADE PERI-IMPLANTITIS
Table 7. Summarized Treatment Methods Used for Retrograde Periimplantitis in the
Case Reports Included
Treatment Methods
Implant removal13–20,26,27,35
Nonsurgical23,24
Open-flap debridement10,11,13,14,23
Regenerative
Bone + membrane
Allograft7,14,29
Xenograft12,25,30
Alloplast36
Allograft + alloplast13,21
Vicryl barrier7,14
Bioabsorbable collagen
membrane12,13,21,25,29,30,36
Bioabsorbable glycolic and lactic
copolymers’ membrane30
Bone substitute alone
Xenograft38
Alloplats13,30
Allograft24,30
Enamel matrix protein derivate22
Calcium hydroxide paste11
Tetracycline paste + bioabsorbable
pericardium membrane31
the review. However, none of the risk
factors were shown to be statistically
significantly related to retrograde
periimplantitis.
Fig. 2. A decision-making tree of retrograde periimplantitis management.
Copyright Ó 2016 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
RAMANAUSKAITE ET AL
probability that it was caused not by
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-
Cases (%) Cases (%) Cases (%) P apical pathology, whereas 1 case
15 (35.7) 5 (18.5) 10 (66.7) 0.001 (7.8%) exhibited pain and adjacent
2 (4.5) 1 (3.6) 1 (6.3) 1.0 tooth with the periapical pathology
8 (18) 4 (14.3) 4 (25.0) 0.434 (P ¼ 0.01).
19 (45.2) 18 (66.7) 1 (6.7) ,0.001
11 (57.9) Treatment
Two cases were solved with non-
surgical treatment (Tables 3 and
7).28,37 The case of retrograde periim-
plantitis by Steiner et al22 was diag-
nosed only radiographically, without
any clinical symptoms, and was
5 (26.3) caused by endodontic pathology
involving teeth adjacent to an
implant.37 Endodontic treatment
resolved the lesion and retained both
1 (5.3) the implant and the tooth at the 14-
1 (5.3) month follow-up. The case reported
by Waasardorp et al28 was asymptom-
1 (5.3) atic and was solved by placing the
patient on a 10-day course of amoxi-
cillin (500 mg three times daily).28 In
an 11-month follow-up, a previously
large radiolucency surrounding the
A negative correlation was found apex of the implant was undetectable
between adjacent tooth with endodon- by radiographic examination.28
tic pathology and pain (r ¼ −0.4; P ¼ Fifteen implants (35.7%) were
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
significantly more often used in maxilla
than mandible (maxilla 18 [66.7%],
RAMANAUSKAITE ET AL
mandible 1 [6.7%]; P , 0.001). Differ-
ent materials were used for bone defect
regeneration: bone (allogenic,7,14,24,28,29
xenogenic,12,25,30,38 alloplastic13,21,22)
and substitutes with7,12–14,21,25,29,30,36 or
without membranes,24,30,31,38 calcium
hydroxide paste,22 enamel matrix pro-
tein derivates,11 and tetracycline paste
in combination with collagen mem-
brane31 (Tables 3 and 7).
Implant surface decontamination
was performed in 14 surgical cases of
29 using different methods: tetracycline
paste (5 cases),7,10,31 40% citric acid (1
case),7 chlorhexidine (4 cases),12,24,25,29
EDTA 24% (1 case),22 and Straumann
Universal Implant Deplaquer (4
cases).13,36 Apicoectomies of the implant
were performed in 6 cases14,23,25,30
(Table 3).
All surgically treated cases re-
mained osseointegrated and continued
to function successfully for up to 20.3
(SD, 6 24.9; minimum, 3; maximum,
96; median, 12) months. For the cases
treated with regenerative approach, the
follow-up time was 17.6 (SD, 6
21.9; minimum, 3; maximum, 84;
median, 12) weeks, and for the open-
flap curettage cases, 26.7 (SD, 6
32; minimum, 8; maximum, 96; median,
12) weeks (P ¼ 0.275 by Mann-
Whitney) with no significant difference.
DISCUSSION
This investigation included studies
reporting the symptoms, possible risk
factors, treatment methods, and out-
comes for retrograde periimplantitis.
An electronic search of MEDLINE
(PubMed) and EMBASE databases
was performed, including studies pub-
lished in the English language between
January 1, 1990, and May 1, 2015.
Additionally, a hand search was per-
formed in the dental implants and
endodontics-related journals.
The results of this review suggest
that retrograde periimplantitis was
diagnosed at 26.07 (639.7) weeks after
implant placement and is most com-
monly associated with the infection
from adjacent teeth with periapical
pathology and/or incomplete endodon-
tic treatment, and with residual infec-
tion at the site of tooth extraction,
when the tooth was removed because
Copyright Ó 2016 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
IMPLANT DENTISTRY / VOLUME 25, NUMBER 5 2016
of periapical pathology. This corre-
sponds to the results of a retrospective
study by Quirynen et al8 that aimed to
find predisposing conditions for retro-
grade periimplantitis. They found that
the extraction sites of teeth with a his-
tory of endodontic pathology and sites
adjacent to teeth with an obvious
endodontic pathology provoked the
pathology. In a study by Zhou et al,41
retrograde periimplantitis was diagnosed
for 7.8% of the implants that were adja-
cent to an endodontically treated tooth. It
was stressed that the incidence of retro-
grade periimplantitis may be reduced by
increasing the distance between the
implant and the adjacent tooth and/or
the duration of endodontically treated
adjacent tooth-to-implant placement.
Brisman et al18 reported four cases
in which even an asymptomatic, end-
odontically treated tooth with a normal
periapical radiographic appearance was
the cause of an implant failure. It has
been shown that even if a periapical area
seems to have been resolved on a radio-
graph, micro-organisms may persist
indefinitely. Therefore, an asymptom-
atic, endodontically treated tooth may
harbor a chronic infection, which may
cause implant failure.18,41
When evaluating the symptoms, all
cases presented radiographic radiolu-
cency at the apex of an implant and
higher part of the cases presented fistula
(P ¼ 0.763). Fistula was more often
present in maxilla (P ¼ 0.04) and in
cases where tooth was removed because
of periapical pathology (P ¼ 0.07).
Negative correlation was found
between pain and adjacent tooth with
incomplete endodontic treatment/end-
odontic pathology (P ¼ 0.009) and, on
a contrary, a positive correlation
between the latter risk factor and
implant removal (P ¼ 0.028).
Once diagnosed, identification of the
cause and removal of the infection source
could limit the extent of the disease
progression and possibly result in saving
the implant. According to Reiser et al,32
infected presentations of retrograde peri-
implantitis require surgical interven-
tion.32 However, Sussman et al15–17 are
of the opinion that the implant should
be extracted immediately to prevent oste-
omyelitis, because retaining the implant
may lead to irreversible bone loss.15–17
695
Based on these case reports, it
seems that the treatment of retrograde
periimplantitis is empirical. In the pres-
ent review, 35.7% of the implants,
diagnosed with retrograde periimplan-
titis, were removed. Statistically signif-
icantly more implants were removed in
the mandible (P ¼ 0.001) and when
there was an adjacent tooth with end-
odontic pathology (P ¼ 0.028).
Open-flap surgery was performed
in 18% of the cases and regenerative
treatment in most cases (45.2%).
Regenerative treatment was statistically
significantly more often used in maxilla
(P , 0.001). All surgically treated
cases, despite the technique applied,
remained osseointegrated and contin-
ued to function successfully for up to
20.3 months (SD 6 24.9) with no sig-
nificant difference. Whether regenera-
tive treatment gives superior results is
impossible to conclude based only on
these case reports. Data from longitudi-
nal studies are required.
A decision-making tree of retro-
grade periimplantitis management was
developed, which can be used as a guide
to assist clinicians in making diagnosis
leading to the proper management of
the pathology and aimed to save the
implant (Fig. 2).
The first step is to verify the exis-
tence of bone loss. Conventional bitew-
ings and periapical radiographs are
adequate to evaluate the bone around
the implants.32,42 If marginal bone
loss, which extends more than 2 mm
beyond crown/abutment-implant junc-
tion, could be observed on the radio-
graph, and bleeding on probing and/or
suppuration and pocket depth $4 mm
are found, the diagnosis of marginal
periimplantitis should be made.43
If radiolucency at the apex on an
implant could be observed, the diagno-
sis of retrograde periimplantitis should
be made.32 The next step would be to
evaluate possible etiological and/or risk
factors. According to it, retrograde peri-
implantitis could be categorized as
infective, caused by the adjacent tooth
with endodontic pathology, root frac-
ture of adjacent tooth, persisting pathol-
ogy in the bone, or chronic periodontitis
of adjacent tooth; traumatic retrograde
periimplantitis due to the bone over-
heating during site preparation or
696 APICAL/RETROGRADE PERI-IMPLANTITIS
bone overcompression during fixture
placement, or impaired bone healing
(impaired osseointegration); and retro-
grade periimplantitis that occurred
because of other possible etiological
and/or risk factors, such as incorrect
implant positioning, etc.
If the case presents implant mobil-
ity with or without clinical symptoms,
the implant must be removed despite
the possible etiological and/or risk
factor.
If there are symptoms such as
swelling and/or fistula and/or pain or
no clinical symptoms, just radiographic
periapical bone lesion, and an adjacent
tooth with periapical lesion or incom-
plete endodontic treatment, or root frac-
ture, endodontic treatment/re-treatment
at the first treatment stage, the case is to
be an infective. If there is a neighboring
tooth with root fracture, the tooth has to
be removed. The patient should be fol-
lowed up every 2 weeks, and at 1-2-3-6
months for 2 years to ensure that the
healing takes place and the symptoms
resolve. If the symptoms do not resolve,
surgical treatment should be indicated.
If there are no adjacent teeth with
endodontic pathology and/or incom-
plete endodontic treatment and/or root
fracture, the case is most likely to be
caused by trauma, persisting infection
in the bone, or other factors (like incor-
rect implant positioning). In these
cases, patient should be followed up
every 3 to 6 months for 2 years. If the
lesion is increasing in size or presents
clinical symptoms, such as pain, swell-
ing, and/or fistula, surgical treatment is
indicated.
The first step of surgical treatment
should be the debridement of granulation
tissues. Based on our own experience, we
would suggest always performing api-
coectomy of the implant apex to ensure
complete removal of inflammatory tissues
and totally eliminating bacteria colonized
over the implant surface. As reported in
the case report by Kutlu et al,25 during the
first surgical treatment of retrograde peri-
implantitis, apicoectomy of the implant
was not performed, which might cause
the recurrence of the disease.38
Decontamination of the implant
surface is considered mandatory for suc-
cessful treatment. The goal of such
decontamination is to eliminate bacteria
Copyright Ó 2016 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
and render the surface conductive to bone
regeneration and reosseointegration.44
Chlorhexidine digluconate (0.2%) dem-
onstrated a great decontamination capac-
ity with respect to both the killing and
the removal of biofilm cells.44 Therefore,
we would suggest using chlorhexidine
digluconate for decontamination.
To obtain optimal treatment re-
sults, we would recommend using the
regenerative treatment approach. We
suggest using bone substitute to fill the
bone defect that would act as a scaffold
for new bone cells to growth into the
bony defect, maintain space, and there-
fore prevent deformities of the soft
tissues.45 Clinical and experimental
studies provided significant evidence
that bone regeneration is significantly
enhanced when the invasion of soft tis-
sue into osseous defects is mechanically
impeded, allowing only osteogenic cell
populations derived from the parent
bone to repopulate the osseous wound
space.45,46 Therefore, we would recom-
mend using resorbable collagen mem-
brane over the bone grafting material.
Systemic antibiotics as an adjunct to
surgical treatment are recommended.
Bacteria associated with failing implants
have been found to be sensitive to
amoxicillin, metronidazole, or a combi-
nation of both.47,48 Neighboring teeth
should be free of periapical pathology;
therefore, a vitality test and concomitant
endodontic treatment/re-treatment might
be indicated. After surgical treatment, the
patient should be followed for 2 years,
every 3 to 6 months to ensure that reso-
lution of the disease takes place.
Limitations
This systematic review included
only case reports that are considered to
be of the lowest scientific evidence
because no other type publications of
higher scientific value were available on
the literature of the topic searched. More-
over, the review used two databases and
only included studies written in English,
which could introduce a publication bias.
CONCLUSIONS
The present systematic review re-
vealed that retrograde periimplantitis is
usually of infectious etiology occurring
from the periapical infection of adjacent
RAMANAUSKAITE ET AL
tooth or persisting bone infection. It is
most often diagnosed at week 26 (SD 6
39.7 weeks) as radiolucency around the
apex of the implant. The most common
clinical symptom is fistula, which is sta-
tistically significantly more often found
in maxilla (P ¼ 0.04). Treatment of ret-
rograde periimplantitis is empirical.
The most often used treatment methods
were the surgical regenerative approach
or implant removal. We suggested
a decision-making tree, which suggests
choosing the management of the
pathology according to its possible eti-
ological/risk factors. Yet, randomized
controlled trials with follow-ups of sev-
eral years and large sample sizes are
needed to determine the best treatment
to control retrograde periimplantitis.
DISCLOSURE
The authors claim to have no
financial interest, either directly or
indirectly, in the products or informa-
tion listed in the article.
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