The Microbiologic Profile Associated with

Peri-Implantitis in Humans: A Systematic Review

Mia Rakic, DDS, PhD1/Maria Gabriella Grusovin, DDS2/Luigi Canullo, DDS, PhD3

Purpose: To qualitatively investigate the microbiologic profile in peri-implantitis by systematically reviewing

the published literature on peri-implant infection. Materials and Methods: Searches of the US National
Institutes of Health free digital archives of the biomedical and life sciences journal literature (PubMed)
and The Cochrane Library of the Cochrane Collaboration (CENTRAL), as well as a hand search of other
literature, were conducted to identify articles potentially relevant for the review. Randomized clinical
trials, prospective cohort studies, longitudinal studies, case-control studies, and cross-sectional studies in
humans reporting microbiologic findings in patients with diagnosed peri-implantitis were considered eligible
for this review. Screening, data extraction, and quality assessment were conducted independently and in
duplicate. Results: Twenty-one articles were eligible for inclusion in this review. Early studies focused on the
identification of target periopathogens, whereas more recent studies used advanced molecular techniques
for comprehensive overview of the peri-implantitis–associated microbiome. In summary, the microbiologic
profile in peri-implantitis (1) is complex and variable, (2) consists of gram-negative anaerobic periopathogens
and opportunistic microorganisms in almost the same ratio, (3) is frequently associated with the Epstein-Barr
virus and nonsaccharolytic anaerobic gram-positive rods, (4) is not so strictly associated with Staphylococcus
aureus, and (5) is different from that of periodontitis. A meta-analysis could not be performed because of
the heterogeneity of the reviewed studies. Conclusion: Although a comparison of the published results was
limited because of the inhomogeneity of the studies, it is clear that the microbiologic profile of peri-implantitis
consists of aggressive and resistant microorganisms and is distinct from that of periodontitis. It seems that
the quantitative characteristics of the microflora cohabitants represent the key determinant of disease,
rather than the qualitative composition, which is very similar in healthy and peri-implantitis states. Int J Oral
Maxillofac Implants 2016;31:359–368. doi: 10.11607/jomi.4150

Keywords: bacteria, microbiota, peri-implantitis, periodontitis

P eri-implantitis is a late complication of oral im-

plants characterized by inflammatory bone loss.1
The central pathologic process in peri-implantitis is
inflammatory osteoclastogenesis, which could be
triggered by infection, lesions of the peri-implant
attachment, excessive biomechanical stress, and/or
biocorrosion.2 However, infection remains the major
1 Assistant Professor, Institute for Biological Research
“Sinisa Stankovic,” University of Belgrade, Belgrade, Serbia;
Centre for Osteoarticular and Dental Tissue Engineering
INSERM U791, Faculty of Dental Surgery, University of
Nantes, Nantes, France.
2 Adjunct Professor, Dental School, Vita-Salute San Raffaele
University, Milan, Italy.
3 Private Practice, Rome, Italy.
Correspondence to: Dr Mia Rakic, Institute for Biological
Research “Sinisa Stankovic,” University of Belgrade,
Belgrade, Serbia, Bulevar Despota Stefana 142,
11000 Belgrade, Serbia. Email: mia.rakic@ibiss.bg.ac.rs
©2016 by Quintessence Publishing Co Inc.
cause of peri-implantitis, and it is considered that all
other factors sooner or later act in conjunction with
infection.2–4 Although peri-implantitis was once con-
sidered a counterpart of periodontitis at implant sites,
recent studies have indicated that peri-implant pathol-
ogy seems to be more complex and differs from peri-
odontal disease pathology.5 This complexity relates
primarily to the structural specificities of peri-implant
tissues and to the implants themselves. Some studies
have suggested that the lack of periodontal ligament
and cementum makes the peri-implant tissues more
susceptible to infection and trauma and leads to fast
progression of disease.6–11 Furthermore, the implant
surface oxide layer (so-called “ceramic-like” layer),
which is the major factor of titanium implant biocom-
patibility, requires certain physicochemical conditions
to maintain its stability and, hence, implant biocom-
patibility. Related to this, the anaerobic peri-implant
infection, which creates an acid microenvironment full
of reactive host-derived factors (such as free radicals),
is considered a physicochemical threat to the stability

The International Journal of Oral & Maxillofacial Implants 359

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Rakic et al
of the oxide layer that could increase inflammatory
bone loss.4 For these reasons, knowledge of the mi-
crobiologic profile associated with peri-implantitis
(which would guide infection control and supportive
periodontal therapy measures) seems to be one of
the factors that is essential for the success of implant
treatment, particularly in subjects with a history of
periodontitis. Despite this great necessity, the micro-
biologic profile of peri-implantitis has not yet been
clearly defined.13–15
The objective of this review was to qualitatively
estimate the microbiologic profile associated with
peri-implantitis in humans through a review of the
literature.
MATERIALS AND METHODS
This systematic review complies with the PRISMA guide-
lines (Preferred Reporting Items for Systematic Reviews
and Meta-Analyses; www.prisma-statement.org).
Study Protocol and Criteria
The protocol was designed to answer the following
question: “What are the characteristics of the microbi-
ologic profile in patients with peri-implantitis?” Includ-
ed were randomized clinical trials, prospective cohort
studies, case-control studies, and cross-sectional stud-
ies in humans reporting microbiologic findings in pa-
tients diagnosed with peri-implantitis. Peri-implantitis
was defined as the radiographic presence of bone loss
≥ 2 mm since the time of prosthetic replacement, posi-
tive bleeding on probing, and probing depth ≥ 5 mm.
Only studies published in English were included. Ex-
cluded were in vitro and animal studies and studies of
blade implants.
Furthermore, the following PECO (population,
exposure, comparison, outcome) definitions were
considered.
• Population. Studies had to include systemically
healthy patients with at least one implant affected
by peri-implantitis; microbiologic findings from
affected sites had to be provided.
• Exposure. Peri-implantitis was the exposure consid-
ered for evaluation.
• Comparison. The specific comparisons investigated
were either differences throughout the course
of peri-implantitis or differences between peri-
implantitis and peri-mucositis, healthy peri-implant
tissues, or periodontitis.
• Outcome measures. The primary outcome variable
was microbiologic status (total flora, presence of
certain bacterial pathogens, and percentages and
proportions of flora of certain bacterial pathogens).
360 Volume 31, Number 2, 2016
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NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Search Strategy
Searches of the U.S. National Institutes of Health free
digital archives of biomedical and life sciences journal
literature (PubMed) and The Cochrane Library of the
Cochrane Collaboration (CENTRAL), as well as a hand
search of other literature, were conducted to identify
articles of potential relevance. The search included
articles accepted for publication up to August 2014.
Previously published review articles on similar topics
were also analyzed to assess potentially relevant pub-
lications. The following key words were used for this
purpose: periimplantitis OR peri-implantitis OR peri
implantitis OR peri-implant AND infection OR bacteria
OR microorganism OR biofilm OR plaque.
Quality Assessment
Quality assurance was developed according to Khan
et al16 via independent screening by two reviewers,
resolution of disagreement by consensus, discarding
of studies when consensus was not achieved, and data
extraction in duplicate.
Data Extraction and Synthesis
Two independent reviewers (MR, LC) analyzed titles
and abstracts in the first stage of screening. Irrelevant
articles were discarded. Then, the full texts of the ar-
ticles considered to be potentially relevant for the
review were read to determine whether the studies
fulfilled the predetermined inclusion criteria. Any dis-
agreement regarding eligibility of the articles was in-
dividually resolved between the reviewers. Data were
collated into evidence tables and grouped according
to the microbiologic analyses that were performed:
(1) evaluation of target pathogens or (2) evaluation
of the entire microbiome. Furthermore, the extracted
data were stratified and expressed in chronologic or-
der according to the publication date. Synthesis of
the data was performed based on the evidence tables
alone, and the data were further interpreted in relation
to the performed study design (cross-sectional, case-
control, or longitudinal). Meta-analysis was not carried
out because of the marked heterogeneity of many as-
pects of the included studies.
RESULTS
The initial search of the literature up to June 2014 yield-
ed 631 potentially suitable papers. Following exclusion
of reviews, animal and in vitro studies, and studies that
inappropriately identified peri-implantitis, 21 publica-
tions remained fully eligible for this review. The κ value
for interreviewer agreement for study inclusion was
0.93 for titles and abstracts and 1.00 for full-text arti-
cles, indicating strong agreement. The major findings

of the reviewed articles were sorted into two tables
according to the type of microbiologic analysis per-
formed. Table 1 covers the studies that evaluated the
target pathogens,17–31 and Table 2 includes studies
that evaluated the entire microbiome.32–37
Target Pathogens of Peri-implantitis
Fifteen studies evaluated target pathogens using cul-
tures, checkerboard hybridization, polymerase chain
reaction (PCR), or DNA probes. Most studies were
cross-sectional and case-control studies; only three
were longitudinal studies.
In the case-control study evaluating the micro-
biologic profiles of peri-implantitis and healthy peri-
implant tissues, distinct differences were observed
between peri-implantitis and clinically healthy im-
plants.17 Porphyromonas gingivalis, Actinobacillus
actinomycetemcomitans, Prevotella intermedia, and
Prevotella nigrescens were identified in 60%, while
Staphylococcus epidermidis, enterics, and Candida
albicans were seen in 55% of cases. P intermedia and
P nigrescens were the most common organisms found
in peri-implantitis, while Enterobacter and Klebsiella
were the most common of the enterics. However,
A actinomycetemcomitans was the microorganism most
significantly associated with peri-implantitis, whereas
A actinomycetemcomitans and P gingivalis were seen in
only one patient with healthy tissues. Another cross-
sectional study21 of the microbiologic profiles of 213
participants with healthy implants, peri-implant mu-
cositis, and peri-implantitis demonstrated no signifi-
cant differences between these conditions. However,
peri-implant pockets with the deepest probing depth
were correlated with levels of Eikenella corrodens,
Fusobacterium nucleatum sp vincentii, P gingivalis, and
Micromonas micros. Moreover, the case-control study
that evaluated the microbiologic profiles of patients
with peri-implantitis and healthy subjects did not report
higher mean counts of P gingivalis, Treponema denticola,
or Tannerella forsythia in both supramucosal and sub-
mucosal samples in peri-implantitis patients, whereas
there was no significant difference between supra- and
submucosal specimens originating from the same site.22
Another cross-sectional study evaluated periopatho-
gens in patients with peri-implantitis, peri-implant mu-
cositis, and healthy peri-implant tissues and reported
high levels of A actinomycetemcomitans, P gingivalis,
P intermedia, T forsythia, and T denticola in peri-im-
plantitis.19 Another cross-sectional study evaluated 40
different bacterial species among patients with peri-im-
plantitis, peri-implant mucositis, and healthy implants
and indicated that Actinomyces gerencseriae was pres-
ent in lower mean counts and T forsythia was present in
higher mean counts in peri-implantitis than in implants
that were diagnosed with peri-implant mucositis and in
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Rakic et al
healthy implants, whereas Capnocytophaga ochracea
was higher in mucositis than in the other groups.23 It was
also observed that P gingivalis showed the highest levels
in peri-implantitis as opposed to the healthy implants, at
which red-complex periopathogens were found in very
low levels. Furthermore, a cross-sectional study investi-
gated microflora in 15 cases of peri-implantitis using cul-
tures and established an association among T forsythia,
Campylobacter sp, and Parvimonas micra with peri-im-
plantitis.24 Additionally, a positive correlation between
pain and the presence of P micra, Fusobacterium, and
Eubacterium sp was reported. A more recent cross-sec-
tional study estimated the frequency of Campylobacter
rectus, P gingivalis, T forsythia, P intermedia, T denticola,
and A actinomycetemcomitans between equivalent
peri-implant and periodontal conditions; it showed that
the occurrence of investigated bacteria was generally
higher in teeth than in implants.29 The frequency of all
bacteria except P intermedia was significantly higher in
peri-implantitis compared to healthy implants, while
P gingivalis and red-complex species occurred more
frequently in peri-implantitis than in peri-implant mu-
cositis. P gingivalis and A actinomycetemcomitans were
similarly distributed between periodontitis and peri-
implantitis, but the occurrence of all other species was
higher in periodontitis than in peri-implantitis. More-
over, a case-control study evaluated 78 different bacte-
rial species among peri-implantitis and healthy implant
samples and showed a bacterial load of T forsythia,
P gingivalis, Treponema socranskii, Staphylococcus
aureus, Streptococcus intermedius, Streptococcus mitis,
and Haemophilus influenzae that was increased by
about four times in peri-implantitis when compared to
healthy implants.30 Following comprehensive statisti-
cal analysis, it was suggested that this cluster of bacte-
ria, including T forsythia and S aureus, is associated with
peri-implantitis.
Three studies evaluated the association of
periopathogenic viruses with peri-implantitis.27,28,31
One study27 analyzed the presence of human cyto-
megalovirus (HCMV) and Epstein-Barr virus (EBV)
within different peri-implant conditions and showed a
high prevalence of HCMV and EBV in the subgingival
plaque of peri-implantitis sites. The same group of au-
thors estimated the prevalence of different genotypes
of HCMV and EBV in subgingival plaque samples from
peri-implantitis, peri-implant mucositis, and healthy
implants and reported a high prevalence of HCMV-2
and EBV-1 in peri-implantitis.28 Furthermore, an esti-
mation of both periopathogenic bacteria and viruses
in saliva and subgingival samples from healthy implant
and peri-implantitis sites in 23 patients demonstrated
higher counts of EBV, CMV, T denticola, and T forsythia in
peri-implantitis.31 Evaluation of these microorganisms
as susceptibility factors for peri-implantitis showed
The International Journal of Oral & Maxillofacial Implants 361
Rakic et al

Table 1 Major Microbiologic Findings Regarding Target Periopathogens in Peri-implantitis

Sampling
Study No. of cases Study method Identification
Leonhardt et al17 (1999) 37 peri-implantitis Case-control PP Culture
51 healthy implants

Mombelli et al18 (2001) 25 peri-implantitis Longitudinal PP Culture, DFM

Hultin et al19 (2002) 17 patients; Cross-sectional PP DNA probe analysis

45 peri-implantitis
53 healthy implants
Leonhardt et al20 (2003) 9 peri-implantitis Longitudinal PP Culture

Renvert et al21 (2007) 31 peri-implantitis Cross-sectional PP DCH

127 peri-implant mucositis
55 healthy implants
Shibli et al22 (2008) 22 peri-implantitis Case-control CT DCH
22 healthy implants
Maximo et al23 (2009) 13 peri-implantitis Cross-sectional CT DCH
12 peri-implant mucositis
10 healthy implants
Tabanella et al24 (2009) 15 peri-implantitis Case-control PP Culture
15 healthy implants (split-mouth)
Persson et al25 (2010) 31 peri-implantitis Randomized PP Expanded DCH assay
longitudinal

Casado et al26 (2011) 10 peri-implantitis, Cross-sectional PP PCR

10 peri-implant mucositis
10 healthy implants
Jankovic et al27 (2011) 20 peri-implantitis Cross-sectional PP Qualitative PCR
18 mucositis
18 healthy implants
Jankovic et al28 (2011) 35 peri-implantitis Cross-sectional PP Qualitative PCR
30 peri-implant mucositis
30 healthy implants
Cortelli et al29 (2013) 53 healthy implants, Cross-sectional CT PCR
53 periodontally healthy
50 peri-implant mucositis
50 peri-implantitis
Persson and Renvert30 (2013) 166 peri-implantitis Case-control PP DCH
47 healthy implants
Verdugo et al31 (2014) 23 peri-implantitis Case-control PP Qualitative PCR for
23 healthy implants (split-mouth) periopathogens,
Quantitative PCR for EBV
and CMV
Sampling: CT = curette; PP = paper points.
Microbiologic methods: DCH = DNA–DNA checkerboard hybridization; DFM = dark-field microscopy.
Bacteria: AA = Aggregatibacter actinomycetemcomitans; AG = Actinomyces gerensceriae; BF = Bacteroides forsythus; CA = Capnocytophaga sp;
CMV = Cytomegalovirus; CR = Campylobacter rectus; EBV = Epstein-Barr virus; EC = Eikenella corrodens; FN = Fusobacterium nucleatum; FU =
Fusobacterium sp; HI = Haemophilus influenzae; HP = Helicobacter pylori; MM = Micromonas micros; PG = Porphyromonas gingivalis; PI = Prevotella
intermedia; PM = Parvimonas micra; PN = Prevotella nigrescens; SA = Staphylococcus aureus; SI = Streptococcus intermedius; SM = Streptococcus
mitis; TF = Tannerella forsythia; TD = Treponema denticola; TS = Treponema socranskii.

that peri-implantitis was 14.2 and 3 times more likely to
harbor EBV than healthy implants and saliva, whereas
the odds ratios for T denticola and T forsythia were 6.79
and 3 times higher as well, respectively; thus, EBV was
suggested as a potential risk factor for peri-implantitis.
In the three longitudinal studies considered in this
review,18,20,25 researchers evaluated periopathogens
as well as some opportunistic microorganisms and
the responses to different treatment approaches. One
study18 included 30 implants affected by peri-implan-
titis and evaluated the treatment effect of tetracycline.
At baseline, high frequencies of C rectus, T forsythia,
Fusobacterium sp, and P intermedia/nigrescens and low
frequencies of A actinomycetemcomitans, P gingivalis,

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Microbiologic findings in peri-implantitis Implant type

Distinct bacterial profile between peri-implantitis and healthy implants. PG, AA, PI, PN in 60%, Brånemark,
Staphylococcus epidermidis, enterics, and Candida albicans in 55%. PI and PN the most common Nobel Biocare
microorganisms, while AA was significantly associated with peri-implantitis. Staphylococci, enterics, and
yeasts more frequent in peri-implantitis than in periodontitis. Similar profile between healthy implants
and periodontium.
45%: CR, FU, PI/PN; TF 36% PI/PN, Fusobacterium sp, BF, and CR reduced levels M1, M3, and M6 ITI
following treatment.
75%–100% implants: AA, FN, PN, PI; 50%–75% implants: PG, PM, CR, EC 14 Brånemark,
3 ITI

7 patients: PI/PN; 6 patients: AA; 3 patients: enterics; 1 patient: PG, SA. PI/PN and enterics persisted 6 Nobel Biocare
mo, 1 y, 5 y posttreatment.
EC, FB sp vincentii, PG, and MM were correlated with the deepest pocket depths. Brånemark,
Nobel Biocare

Higher counts of PG, TD, TF in peri-implantitis. Supra- and subgingival profiles were not substantially Brånemark-like
different.
AG lower counts, TF higher counts in peri-implantitis compared to mucositis and healthy implants. PG Brånemark
was at the highest levels in peri-implantitis. PM, TF, PG, and TD from TS significantly reduced 3 mo
posttreatment in peri-implantitis.
9 implants: FU, TF; 7 implants: CR, PM; 5 implants: PG, PI 11 Brånemark,
4 3i
Baseline: AA (serotype b), FN sp, HP, Staphylococcus sp, and TF. 30 minutes following curettage: reduced No data
counts of AA, Lactobacillus acidophilus, Streptococcus anginosus, and Veillonella parvula. Baseline and 6
mo: no differences in bacterial counts.
AA, PG, PI, TD, and TF identified in all conditions No data

HCMV 13 (65%), EBV in 9 (45%) in peri-implantitis Predominantly

Nobel Biocare

HCMV-2 in 53.3% and EBV-1 in 46.6% peri-implantitis Predominantly

Nobel Biocare

CR, PG, TF, TD, and AA higher in peri-implantitis than in healthy implants. PG and red-complex species Nobel Biocare
higher in peri-implantitis compared to mucositis. PG and AA similar between periodontitis and peri-
implantitis; CR, TF, PI, TD higher in periodontitis.

TF, PG, TS, SA, SI, SM, and HI 4× increased total load in peri-implantitis and suggested a cluster of No data
bacteria, including TF and SA, as related to peri-implantitis.
Higher counts of EBV, CMV, TD, and TF in peri-implantitis. Peri-implantitis 14.2 and 3 times more likely No data
to harbor EBV than healthy implants and saliva, while odds ratios for TD and TF were 6.79 and 3 times
higher than in healthy sites.

and E corrodens were seen.18 Another study20 evaluat-
ed the effect of open-flap debridement in conjunction
with systemic antibiotics against target microorgan-
isms. At baseline, six sites were positive for A actinomy-
cetemcomitans, seven for P intermedia and P nigrescens,
one for P gingivalis, one for S aureus, and three for both
Escherichia coli and Enterobacter cloacae.20 At 6 months
and 1 year posttreatment, P intermedia/P nigrescens
and enterics persisted; after 5 years, P intermedia/
P nigrescens had reached a peak, as they were now
present in eight patients (versus seven patients at base-
line). Furthermore, in a study that evaluated treatment
outcomes in patients with peri-implantitis after two
different kinds of mechanical debridement (curettes/

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Rakic et al

Table 2 Major Microbiologic Findings Obtained by Metagenomic and Metatranscriptomic

Analysis of the Entire Microbiome in Peri-implantitis
Sampling
Authors N cases Study method Identification
Koyanagi et al32 (2010) 3 peri-implantitis Cross-sectional PP 16S rRNA gene sequencing
3 healthy implants
3 periodontitis

Kumar et al33 (2012) 10 peri-implantitis Cross-sectional PP 16S pyrosequencing

10 healthy implants
10 periodontally healthy
10 periodontitis

Koyanagi et al34 (2013) 6 peri-implantitis, Cross-sectional PP 16S rRNA gene sequencing

6 periodontitis
Tamura et al35 (2013) 15 peri-implantitis Case-control PP Culture +
15 healthy implants 16S DNA gene sequencing

Dabdoub et al36 (2013) 20 peri-implantitis Cross-sectional PP 16S rRNA gene sequencing

20 peri-implant mucositis
13 gingivitis
12 periodontitis
da Silva et al37 (2010) 10 peri-implantitis Case-control CT 16S rRNA gene sequencing
10 healthy implants

Sampling: CT = curette; PP = paper points.

Microbiologic methods: DCH = DNA–DNA checkerboard hybridization; DFM = dark-field microscopy.
Bacteria: AA = Aggregatibacter actinomycetemcomitans; AG = Actinomyces gerensceriae; BF = Bacteroides forsythus; CA = Capnocytophaga sp;
CMV = Cytomegalovirus; CR = Campylobacter rectus; EBV = Epstein-Barr virus; EC = Eikenella corrodens; FN = Fusobacterium nucleatum;
FU = Fusobacterium sp; MM = Micromonas micros; PG = Porphyromonas gingivalis; PI = Prevotella intermedia; PM = Parvimonas micra;
PN = Prevotella nigrescens; SA = Staphylococcus aureus; SM = Streptococcus mutans; TF = Tannerella forsythia; TD = Treponema denticola;
TS = Treponema socranskii.

ultrasound),25 A actinomycetemcomitans (serotype b), F implants and periodontitis. Another cross-sectional

nucleatum sp, Helicobacter pylori, staphylococci, and T
forsythia were identified at baseline. At 30 minutes af-
ter curettage, the counts of A actinomycetemcomitans,
Lactobacillus acidophilus, Streptococcus anginosus, and
Veillonella parvula were reduced, while at 6 months the
microflora had been re-established, as evidenced by an
absence of differences versus the baseline findings.
Microbiome of Peri-implantitis
In a cross-sectional study that analyzed the microbio-
logic profile using a sequencing technique, 77 bac-
terial species were identified in peri-implantitis, 57
in periodontitis, and 12 around healthy implants.32
The microorganisms detected only in peri-implanti-
tis were Chloroflexi, Tenericutes, and Synergistetes sp,
P micra, Peptostreptococcus stomatis, Pseudoramibacter
alactolyticus, and Solobacterium moorei, while A ac-
tinomycetemcomitans and P gingivalis were present
in low levels. Hence, it was concluded that most of
the microbiota in peri-implantitis consisted of gram-
negative species and was more diverse than in healthy
study33 analyzed subgingival/submucosal plaque
samples from 40 participants with periodontitis, peri-
implantitis, and periodontal and peri-implant health
using 16S pyrosequencing and reported lower lev-
els of Prevotella and Leptotrichia sp and higher levels
of Actinomyces, Peptococcus, and Campylobacter sp,
non-mutans streptococci, Butyrivibrio sp, and Strepto-
coccus mutans in peri-implantitis when compared to
healthy implants.33 A comparison of peri-implantitis
and periodontitis demonstrated lower levels of Pre-
votella sp, non-mutans streptococci, and Lactobacillus,
Selenomonas, Leptotrichia, and Actinomyces sp and higher
levels of Peptococcus, Mycoplasma, Eubacterium, Campy-
lobacter, and Butyrivibrio sp, S mutans, and Treponema sp
in peri-implantitis. Hence, the authors concluded that the
microbiomes of periodontitis and peri-implantitis differ
significantly. A similar study demonstrated that the micro-
biologic profile was more diverse in peri-implantitis than
in periodontitis.34 Fusobacterium sp and Streptococcus sp
were predominant in both disorders, while P micra was
detected only in peri-implantitis. This study outlined the

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 Rakic et al

Microbiologic findings in peri-implantitis Implant type

Peri-implantitis harbored mainly gram-negative species, more diverse microflora than healthy No data
implants and periodontitis. Chloroflexi, Tenericutes, and Synergistetes, PM, Peptostreptococcus
stomatis, Pseudoramibacter alactolyticus, and Solobacterium moorei detected only at peri-implantitis
sites; PG and AA detected at low levels.
Peri-implantitis was associated with lower levels of Prevotella and Leptotrichia and higher levels of Astra Tech, Zimmer,
Actinomyces, Peptococcus, Campylobacter, non-mutans Streptococcus, Butyrivibrio, and SM. Lower Nobel Biocare
levels of Prevotella, non-mutans Streptococcus, Lactobacillus, Selenomonas, Leptotrichia, Actinomyces
and higher levels of Peptococcus, Mycoplasma, Eubacterium, Campylobacter, Butyrivibrio, SM, and
Treponema compared to periodontitis.
The microbial composition of peri-implantitis more diverse than that of periodontitis. Fusobacterium No data
sp and Streptococcus sp were predominant in both diseases. PM detected only in peri-implantitis.
Peri-implantitis about 10-fold higher mean colony-forming units (69 different bacterial species No data
identified) than healthy implants (53 different bacterial species identified). Predominant species
in peri-implantitis: Eubacterium nodatum (7%), PI (5%), FN (3%), Filifactor alocis (3%), E brachy (3%),
Parascardovia denticolens (3%), and PM (3%).
Periodontal microbiome demonstrated significantly higher diversity than the implant; distinct bacterial No data
lineages were associated with health and disease in each ecosystem. Members of the genera
Staphylococcus and Treponema were significantly associated with peri-implantitis.

Great differences were observed between healthy implants compared to peri-implantitis. FN, No data
Campylobacter gracilis, Dialister invisus, Streptococcus sp, Eubacterium infirmum, Filifactor alocis,
and Mitsuokella sp presented a higher mean proportion, while Veillonella dispar, Streptococcus mitis,
Actinomyces meyeri, Granulicatella adiacens showed lower mean proportions in the peri-implantitis
sites than in healthy implants.

higher prevalence of periopathogens and more complex
microflora in peri-implantitis compared to periodontitis.
Furthermore, in another case-control study, microbio-
logic specimens obtained from healthy implant sites and
peri-implantitis were investigated; the results showed
10-fold higher mean colony-forming units in peri-
implantitis.35 The predominant species in peri-implan-
titis sites were Streptococcus and Eubacterium, while
the predominant species around healthy implants
were Streptococcus, Veillonella, and Actinomyces. Al-
though Streptococcus was common in both groups,
the prevalence of bacterial species was completely
different between the investigated groups. Sixty-nine
different bacterial species were identified in peri-
implantitis sites, and predominant bacterial species
were Eubacterium nodatum, E brachy, E saphenum, Fi-
lifactor alocis, Slackia exigua, Parascardovia denticolens,
P intermedia, F nucleatum, P gingivalis, Centipeda peri-
odontii, and P micra; the number of species at healthy
implants was 53. Based on the significantly higher
prevalence of nonsaccharolytic anaerobic gram-pos-
itive rods in peri-implantitis and compared to healthy
implant sites, where these bacteria were almost un-
detectable, it was suggested that this group of bac-
teria could play an important role in peri-implantitis.
Furthermore, a cross-sectional study was performed36
to profile peri-implant and periodontal microflora
in healthy and diseased conditions using a sequencing
method; it revealed that peri-implant and periodontal
microbiomes are distinct ecosystems and indicated
a more diverse profile in periodontitis. Members of
the genera Staphylococcus and Treponema were sig-
nificantly associated with peri-implantitis.36 A case-
control study that estimated microbiomes of healthy
implants and peri-implantitis showed different profiles
for peri-implantitis and healthy implants; peri-implantitis
was associated with more periopathogenic bacte-
rial species than healthy implants.37 Higher mean
proportions of F nucleatum, Campylobacter gracilis,
Dialister invisus, Streptococcus sp, human oral taxon (HOT)
064, Eubacterium infirmum, F alocis, and Mitsuokella sp
HOT 131, along with lower mean proportions of Veillon-
ella dispar, S mitis, Actinomyces meyeri, and Granulicatella
adiacens, were the findings in peri-implantitis.

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Rakic et al
DISCUSSION
As pointed out in a previous review of this issue,38 early
studies focused on comparisons of the microbiologic
profiles in peri-implantitis and chronic periodontitis
using routine culture techniques, hybridization, and
PCR to evaluate target periopathogenic bacteria, ie,
the so-called periopathogens. In brief, these studies
showed that the qualitative profile of periopathogens
was similar between healthy and peri-implantitis–
affected implants, whereas the quantitative composi-
tion of periopathogens was the distinguishing factor
between health and disease. Furthermore, an analysis
of the periopathogen profiles of healthy versus dis-
eased implants and corresponding conditions in teeth
revealed an increased frequency of periopathogens
in teeth. Generally, investigations of periopathogens
were unable to establish a clear microbiologic pro-
file associated with peri-implantitis, and it was ac-
cepted that the microbiologic and immunopathologic
profiles of peri-implantitis and periodontitis differ.5
Therefore, more recent studies have been directed
toward comprehensive analyses of the microbiome
in peri-implantitis.33–37 Advanced molecular tech-
niques, such as sequencing methods, render a com-
prehensive overview of phylogenetic and taxonomic
bacterial diversity and indirectly compensate for the
limitations of cultures and lack of reactivity of con-
ventional biochemical tests that are typical for a num-
ber of fastidious anaerobic microorganisms.39 For the
aforementioned reasons, during the last 4 years the
newer sequencing approaches have been widely used
to profile the peri-implantitis microflora and offer new
insights. Microbiologic screens employing sequencing
techniques have shown the following: (1) peri-implan-
titis harbored mainly gram-negative species, and an
association of certain periopathogens with peri-im-
plantitis was confirmed; (2) nonsaccharolytic bacteria
are associated with peri-implantitis; (3) S aureus is not
strictly present in peri-implantitis; (4) a different and
more diverse microflora is present in peri-implantitis
than in healthy implants; (5) the microbiomes in peri-
implantitis and periodontitis are different ecosystems.
In fact, these metagenomic and metatranscriptomic
techniques revealed more diverse microbiologic pro-
files in both periodontitis and peri-implantitis than
previously thought, and in general it has been sug-
gested that the role of periopathogens must be re-
interpreted.40 When considering the reported results
as a whole, the peri-implantitis microflora consists of
periopathogens and opportunistic bacteria in almost
the same measure.41 The lack of conclusive evidence
about the impact of periopathogens on the peri-im-
plantitis microflora could be possibly explained by the
recently reported “keystone pathogen” hypothesis of
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periodontal infection.42 This hypothesis indicates that
similar bacteria are present in both healthy and dis-
eased conditions, while the changes in bacterial pro-
portions represent the key pathologic determinant.
In addition, it is suggested that the most important
role of periopathogens is the conversion of a symbi-
otic ecosystem into a dysbiotic one.43 Translated to
peri-implantitis, it seems that periopathogens provide
permissive conditions for the overgrowth of opportu-
nistic bacteria, thus orchestrating their conversion from
physiologically harmless to pathological members of
microflora. In this regard, an evaluation of opportunis-
tic bacteria is the subject of recent studies that focused
primarily on the identification of these bacteria. One
study30 quantitatively evaluated opportunistic bacteria
together with periopathogens and estimated their risk
rate. It showed that, of 78 analyzed bacteria, a cluster
of four opportunistic bacteria (S aureus, S intermedius,
S mitis, and H influenzae) and three periopathogens
(T forsythia, P gingivalis, and T socranskii) are associated
with peri-implantitis.30 This additionally supports the
theory that opportunistic bacteria and their quantita-
tive content represent the important determinants of
the microbiologic profile in peri-implantitis.
Considering the reviewed studies as a whole, there
is a high rate of inhomogeneity in their protocols that
significantly reduces the applicability of the reported
results. The use of several different diagnostic protocols
contributed to inhomogeneity in the expression of mi-
crobiologic outcome variables (total bacterial counts,
frequencies, proportions, loads, etc); thus, compari-
sons of the findings between groups remain limited.
In general, the reviewed studies were performed on
relatively small samples (never more than 50 peri-
implantitis cases, and, on average, 20 peri-implantitis
cases) and provided very heterogenous observational
findings that render between-study comparisons dif-
ficult. Hence, despite the great efforts of the implant
research community, most of the reported results are
observational and descriptive, such that it is almost im-
possible to determine meaningful patterns concerning
the microbiologic profile of peri-implantitis. Further-
more, earlier studies mostly evaluated the qualitative
and quantitative profiles of periopathogens, whereas
more recent studies revealed the implications of oth-
er pathogens, which remain merely identified, while
their quantitative profiles and pathologic mechanisms
have not yet been clearly established. Moreover, the
reported results originated predominantly from case-
control and cross-sectional studies (only 3 of 21 were
longitudinal studies), although it seems that changes
in bacterial counts represent the key determinant of
peri-implantitis microflora. Therefore, future research
in this area should be oriented toward the quantita-
tive assessment of peri-implant microflora cohabitants

in well-designed prospective studies. Since it is obvi-
ous that the peri-implantitis microbiologic profile is
complex and determined by numerous members with
complex interrelationships, advanced statistical tools for
risk estimation should be considered in future research
as well.
When considering the microbiologic profile from
a clinical standpoint, peri-implantitis is associated
with aggressive and resistant bacterial strains and vi-
ruses; therefore, mechanical anti-infective treatment
usually fails to reduce or eliminate periopathogens
without auxiliary antimicrobial therapy.18,25,44 Further-
more, the opportunistic bacteria characteristic of peri-
implantitis are highly resistant and do not respond to
some antibiotics that are routinely administered in peri-
odontology, such as metronidazole. Additionally, it was
previously reported that the implant-abutment connec-
tion could harbor a reservoir of bacteria in both healthy
and diseased implants, based on the “circular model” of
bacterial contamination.45,46 Therefore, it seems that the
contaminated implant surface represents a reservoir of
periopathogens with the ability to firmly adhere to both
biotic and abiotic systems.47 This could possibly explain
the better treatment outcome in patients in whom sur-
face decontamination was performed25 compared to
the outcome following routine mechanical treatment
with curettes and ultrasound devices.23 Related to this,
microbiologic contamination of the implant surface
represents an intrinsic characteristic of peri-implant pa-
thology that can interrupt the stability of the implant
surface oxide layer and stimulate further detrimental
processes. Finally, effective infection control through
targeted anti-infective approaches, implant surface
decontamination, and supportive periodontal therapy
remains crucial treatment for peri-implantitis.
CONCLUSIONS
Considering the reviewed studies as a whole, the mi-
crobiologic profile in peri-implantitis: (1) is complex
and variable, (2) consists of gram-negative anaerobic
periopathogens and opportunistic microorganisms
in almost the same ratio, (3) is frequently associated
with Epstein-Barr virus and nonsaccharolytic anaerobic
gram-positive rods, (4) is not so strictly associated with
Staphylococcus aureus, and (5) is different from that of
periodontitis. It seems that the presence of titanium cre-
ates a distinct microenvironment, and as a consequence,
the microbiologic profile in peri-implantitis remains
different from that of periodontitis. Furthermore, micro-
organisms that constitute the microbiologic profile in
peri-implantitis have the potential to disrupt the stability
of the implant surface layer and, hence, might contrib-
ute to a pathologic interface with the implant surface.
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NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Rakic et al
ACKNOWLEDGMENTS
The authors report no conflicts of interest related to this study.
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