1

Journal of Oral Science, Vol. 59, No. 1, 1-11, 2017

Original

Prevalence and risk factors for peri-implant diseases
in Japanese adult dental patients
Yorimasa Ogata1), Yohei Nakayama1), Junichi Tatsumi2), Takehiko Kubota3), Shuichi Sato4),
Tetsuya Nishida4), Yasuo Takeuchi5), Tokuya Onitsuka6), Ryuji Sakagami6), Takenori Nozaki7),
Shinya Murakami7), Naritoshi Matsubara8), Maki Tanaka9), Toshiaki Yoshino9), Junya Ota10),
Taneaki Nakagawa10), Yuichi Ishihara11), Taichi Ito12), Atsushi Saito13), Keiko Yamaki14),
Etsuko Matsuzaki15), Toshirou Hidaka16), Daisuke Sasaki17), Takashi Yaegashi17),
Tadashi Yasuda18), Toshiaki Shibutani18), Kazuyuki Noguchi19), Hisao Araki20), Noriharu Ikumi21),
Yukihiko Aoyama22), Hideki Kogai23), Kenji Nemoto24), Shinji Deguchi24), Takashi Takiguchi25),
Matsuo Yamamoto25), Keita Inokuchi26), Takatoshi Ito26), Takashi Kado27), Yasushi Furuichi27),
Mikimoto Kanazashi28), Kazuhiro Gomi28), Yukie Takagi29), Keita Kubokawa30),
Nobuo Yoshinari30), Yoshiaki Hasegawa31), Tetsushi Hirose32), Toshinaga Sase33),
Hirokazu Arita34), Toshiro Kodama35), Kitetsu Shin2), Yuichi Izumi5), and Hiromasa Yoshie3)
1)Department of Periodontology and Research Institute of Oral Science,

Nihon University School of Dentistry at Matsudo, Matsudo, Japan

2)Division of Periodontology, Department of Oral Biology and Tissue Engineering,

Meikai University School of Dentistry, Sakado, Japan

3)Division of Periodontology, Department of Oral Biological Science,

Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan4)Department of Periodontology, Nihon University School of Dentistry, Tokyo, Japan5)Department of Periodontology, Graduate School of Medical and Dental Sciences,

Tokyo Medical and Dental University, Tokyo, Japan

6)Section of Periodontology, Department of Odontology, Fukuoka Dental College, Fukuoka, Japan
7)Department of Periodontology, Osaka University Graduate School of Dentistry, Suita, Japan
8)Matsubara Dental Clinic, Gifu, Japan

9)Seikeikai Hospital Internal and Dental Medicine, Yokohama, Japan

10)Department of Dentistry and Oral Surgery, Keio University School of Medicine, Tokyo, Japan

11)Department of Endodontology, School of Dentistry, Matsumoto Dental University, Shiojiri, Japan
12)Department of Oral and Maxillofacial Implantology, Tokyo Dental College, Tokyo, Japan
13)Department of Periodontology, Tokyo Dental College, Tokyo, Japan14)Division of Periodontology and Endodontology, Department of Oral Biology,

Tohoku University Graduate School of Dentistry, Sendai, Japan

15)Department of Operative Dentistry and Endodontology, Fukuoka Dental College, Fukuoka, Japan
16)Hidaka Dental Clinic, Tokyo, Japan17)Division of Periodontology, Department of Conservative Dentistry, Iwate Medical University, Morioka, Japan18)Department of Periodontology, Division of Oral Infection and Disease,

Asahi University School of Dentistry, Hozumi, Japan

19)Department of Periodontology, Kagoshima University Graduate School of Medical and Dental Sciences,

Kagoshima, Japan

220)Department of Restorative and Biomaterials Sciences, Division of Oral Rehabilitation,

Meikai University School of Dentistry, Sakado, Japan21)Ishikura Dental Clinic, Takasaki, Japan22)Hamamatsu Act Tower Aoyama Dental Office, Hamamatsu, Japan23)Sanno Hospital, Dentistry and Oral Surgery, Tokyo, Japan24)Department of Periodontal Regeneration, Kanagawa Dental University, Yokosuka, Japan
25)Department of Periodontology, Showa University School of Dentistry, Tokyo, Japan
26)Itoh Dento-Maxillofacial Hospital, Kumamoto, Japan27)Division of Periodontology and Endodontology, Department of Oral Rehabilitation, School of Dentistry, Health
Sciences University of Hokkaido, Hokkaido, Japan28)Department of Periodontology, Tsurumi University School of Dental Medicine, Yokohama, Japan29)Sachi Dental Clinic, Tsuchiura, Japan
30)Department of Periodontology, School of Dentistry, Matsumoto Dental University, Shiojiri, Japan
31)Hasegawa Dental Office, Tokyo, Japan32)Yuraku Dental Office, Yokohama, Japan33)Sase Dental Office, Chiba, Japan34)Arita Dental Clinic, Tokyo, Japan35)Division of Implantology and Periodontology, Department of Highly Advanced Stomatology,
Graduate School of Dentistry, Kanagawa Dental University, Yokosuka, Japan(Received January 15, 2016; Accepted April 23, 2016)

Abstract: We investigated the prevalences and risk

factors for peri-implant diseases in Japanese adultdental patients attending a follow-up visit at dental
hospitals or clinics as part of their maintenanceprogram. This cross-sectional multicenter study
enrolled patients with dental implants who attended
regular check-ups as part of a periodontal maintenance program during the period from October 2012
through September 2013. Patients with implants
with at least 3 years of loading time were included in
the study. The condition of peri-implant tissue was
examined and classified into the following categories:
healthy, peri-implant mucositis, and peri-implantitis.
Patients were also evaluated for implant risk factors.
A total of 267 patients (110 men, 157 women; mean
age: 62.5 ± 10.7 years) were analyzed. The prevalenceof patient-based peri-implant mucositis was 33.3% (n= 89), and the prevalence of peri-implantitis was 9.7%
(n = 26). Poor oral hygiene and a history of periodonCorrespondence to Dr. Yorimasa Ogata, Department of
Periodontology, Nihon University School of Dentistry at Matsudo,
2-870-1 Sakaecho-nishi, Matsudo, Chiba 271-8587, Japan
Fax: +81-47-360-9362 E-mail: ogata.yorimasa@nihon-u.ac.jp
J-STAGE Advance Publication: October 7, 2016
Color figures can be viewed in the online issue at J-STAGE.
doi.org/10.2334/josnusd.16-0027
DN/JST.JSTAGE/josnusd/16-0027

titis were strong risk factors for peri-implant disease.
The present prevalences were lower than those previously reported. The quality of periodontal therapy
before and after implant installation and patientcompliance and motivation, as indicated by plaquecontrol level, appear to be important in maintaining
peri-implant tissue health.
Keywords: multicenter study; peri-implant mucositis;
peri-implantitis; prevalence.

Introduction

Peri-implant diseases are classified into two categories:
peri-implant mucositis and peri-implantitis (1). Periimplant mucositis is a reversible inflammatory reactionin the mucosa surrounding a functional dental implant.
Peri-implantitis is an inflammatory reaction associatedwith functional deterioration of supporting bones arounda dental implant. These are the most frequent long-term
complications of dental implants (1-5). However, theabsence of widely accepted diagnostic criteria for thesepathologies complicates the interpretation of publishedvalues for prevalence (1,6,7). The Consensus of theSeventh European Workshop on Periodontology indicates that the key parameter for diagnosis of peri-implantmucositis is bleeding on gentle probing (<0.25 N).

3Moreover, peri-implantitis was defined as a change in thelevel of the crestal bone in conjunction with bleeding on
probing, with or without concomitant deepening of periimplant pockets (1). A number of studies have reported
fairly high prevalences for peri-implant mucositis andperi-implantitis (5,8-12). Some evidence suggests thatpoor oral hygiene (9), history of periodontitis (13,14),
smoking (15), lack of keratinized mucosa (16), andimplant surface topography (17) are associated withperi-implant mucositis and peri-implantitis. Furthermore, periodontally compromised patients who did notcompletely adhere to supportive periodontal therapy had
a higher implant failure rate (18,19).
Several studies have noted similarities in the pathogenesis of periodontitis and peri-implantitis (20-22).
Specifically, periodontal pathogens can translocate fromperiodontally involved teeth to peri-implant sulci inpartially dentate patients (23,24). These findings highlightthe importance of periodontal treatment of residual dentition before placement of osseointegrated dental implants(14,25). However, a recent hypothesis holds that the coremicrobiota in peri-implantitis and periodontitis exhibits
intraindividual variation (26,27).
To better understand the prevalence of peri-implantdiseases and the risk factors associated with these diseases
in Japanese adults, we investigated the prevalence andrisk factors for peri-implant diseases in Japanese adultdental patients who received periodontal treatment
by periodontal specialists before placement of dental
implants. All were enrolled in a periodontal maintenanceprogram that included routine follow-up visits at dental
hospitals or private dental clinics affiliated with the Japanese Society of Periodontology (JSP).

Materials and Methods

SampleThis cross-sectional study enrolled patients who were
included in a periodontal maintenance program by
periodontal specialists (with follow-up visits every 1-12
months) in dental hospitals or private dental clinics
affiliated with the JSP. The study was approved by the
Ethics Committee of the JSP (JSP2012001). All patientswith dental implants, more than 3 years of follow-up
after loading, and consecutive attendance at periodontal
maintenance appointments between October 2012 andSeptember 2013 were enrolled. They were assigned to thestudy cohort from an implant registry in a random order
based on the scheduling of their last routine consultation.
Written informed consent was obtained from each patient
after all procedures had been explained in detail. A totalof 267 patients (one implant and one natural tooth per

patient were included) were interviewed to update their
medical and dental histories, according to the protocolsof this study, and were categorized by age, sex, smoking
habit, implant manufacturer, surface topography, useof a one- or two-stage surgical approach, presence ofa screw- or cement-retained implant restoration, andhistory of periodontal disease (as determined by a review
of periodontal charts before and after implant treatment).
Periodontal treatment before placement of the dental
implant and the standardized periodontal maintenancecheck-ups were performed by periodontal specialists.
These check-ups included a complete periodontal examination comprising determination of probing pocket depth(PPD) (the deepest values for implant and natural teeth
in the same oral cavity were registered), modified plaqueindex (mPlI) and modified sulcus bleeding index (mSBI)
for implants (20), plaque index (PlI) (28) and gingivalindex (GI) (29) for natural teeth, bleeding on probing(BOP), suppuration, tooth/implant mobility, and width of
buccal keratinized mucosa, as well as an X-ray (intraoral
or panoramic radiographs) examination. A diagnosis ofperi-implant mucositis was defined as bleeding on gentle
probing (<0.25 N), and peri-implantitis was defined aschanges in the level of the crestal bone in conjunction
with BOP (1). Gingivitis was defined as the presence ofclinical signs of inflammation confined to the gingiva
and associated with teeth showing no attachment loss.
Chronic periodontitis (CP) is associated with accumulation of plaque and calculus, has a slow to moderate rateof disease progression, and is characterized as slight,
moderate, or severe (slight: 1-2 mm of clinical attachment loss; moderate: 3-4 mm of clinical attachment loss;
severe: ≥5 mm of clinical attachment loss). Aggressive
periodontitis differs from the chronic form primarily inthe rapid rate of disease progression seen in otherwise
healthy individuals, the absence of large accumulationsof plaque and calculus, and the presence of a family
history of aggressive disease suggestive of a genetic trait(30).
Quantification of periodontal bacteria from
subgingival plaque samples
Subgingival plaque samples were collected from twosites (the deepest PPD sites for implant and natural teeth
in the same oral cavity). Before sampling, supragingival
plaque was removed with sterile cotton pellets. Sterile
paper points were then inserted into the sample site,retained for 10 seconds (three times), and then immediately sent to a medical laboratory (BML Corporation,
Tokyo, Japan) for bacterial analysis. Aggregatibacter
actinomycetemcomitans (A. a.), Prevotella intermedia (P.

4i.), Porphyromonas gingivalis (P. g.), and total bacteria
were quantified using the modified Invader PLUS assay,
as described previously (31,32).
Measurement of IgG titers against periodontal
bacteria
Serum was extracted from a 50-µL sample of whole
capillary blood obtained from the middle fingertip, anddevice-treated serum was obtained according to procedures prescribed by Leisure, Inc. (Tokyo, Japan). IgG
titers against A. actinomycetemcomitans, P. intermedia,
Eikenella corrodens (E. c.), and P. gingivalis were determined using an enzyme-linked immunosorbent assay.
The details of the measurement method are described indetail elsewhere (33).
Statistical analysis
Differences among the three groups (healthy peri-implanttissue, peri-implant mucositis, and peri-implantitis) wereanalyzed by one-way ANOVA with the post-hoc TurkeyKramer test. The chi-square test for independence
confirmed by Fisher’s exact probability test was used
to determine whether a history of chronic periodontitis
was associated with healthy peri-implant tissue or periimplant mucositis. The associations of implant design andprosthesis type with peri-implant diseases were analyzed
by the Kruskal-Wallis test or the Mann-Whitney U test
(34).

Results

The age, sex, smoking habit, PPD, BOP, suppuration, andmobility distributions for the participants are shown in
Table 1. A total of 267 patients (mean ± SD age, 62.5 ±10.7 years) were included in the analysis. The group aged
60 to 69 years was the largest age group (114; 42.7%);
22 smokers were included in this study. Eight smokers
exhibited peri-implant mucositis, but there was no periimplantitis in these smokers. The average numbers ofresidual teeth and dental implants per participant were
20.9 ± 5.9 teeth and 3.8 ± 3.2 pieces. Average PPD(deepest value for implant and natural teeth in the sameoral cavity) was 3.4 ± 1.6 mm for implants and 4.0 ±2.0 mm for natural teeth. BOP was detected in 43.1%
of implants and in 50.2% of natural teeth. Suppuration
was detected in 6% of implants and in 4.5% of natural
teeth. Twenty-nine (11%) natural teeth exhibited toothmobility; there was no mobility (0%) in implants (Table1). The most common interval between follow-up visits
was 3 months (139; 52.1%), followed by intervals of 6months (36; 13.5%), 2 months (25; 9.4%), 1 month (20;
7.5%), and 4 months (19; 7.1%). Causal factors for tooth

Table 1 Characteristics and of subjects and clinical findings
for participantsAge, years
20~29
30~39
40~49
50~59
60~69
70~79
80~89
Males
Females
SmokerNonsmoker
Implant number
Residual teeth number
PPD (mm)62.5 ± 10.7
5 (2%)
5 (2%)
19 (7%)
58 (22%)114 (42%)56 (21%)19 (4%)
110 (41%)
157 (59%)
22 (8%)
245 (92%)
3.8 ± 3.2
20.9 ± 5.9(Imp) 3.4 ± 1.6(Teeth) 4.0 ± 2.0
BOP(Imp) 115 (43.1%)(Teeth) 134 (50.2%)
Suppuration(Imp) 16 (6.0%)(Teeth) 12 (4.5%)
Mobility(Imp) 0 (0%)(Teeth) 29 (11%)
n = 267, Mean ± SD, PPD: probing pocket depth, BOP: bleeding on
probing

extraction were periodontitis (122; 46%), tooth fracture(61; 22.8%), caries (43; 16.1%), apical periodontitis (5;1.9%), external injury (5; 1.9%), birth defect (3; 1.1%),
re-implantation (2; 0.7%), tooth perforation (1; 0.4%),
and unknown reasons (25; 9.4%) (Table 2A). Two (0.8%)
patients had one-piece implants, 82 (30.7%) had softtissue level (two-piece) implants, and 183 (68.5%) had
bone-level (two-piece) implants. Ninety-nine (37%) had
screw-retained implant prostheses, and 168 (63%) had
cement-retained implant prostheses. The prevalences ofhealthy peri-implant tissue, peri-implant mucositis, andperi-implantitis were 152 (57%), 89 (33.3%), and 26(9.7%), respectively (Table 2A). Associations of implantdesign (soft-tissue level or bone level) and prosthesis type(screw- or cement-retained) with peri-implant diseases
were analyzed with a nonparametric test (Table 2B).
Implant design and prosthesis type were not significantly
associated with peri-implant diseases.
Figure 1 shows the sites and numbers of dental implants
in the maxilla and mandible. The total numbers of dental
implants in the maxilla and mandible were 420 and 566
pieces, respectively. The upper and lower first molars
were the most frequent sites for dental implants. Figure
2 shows the implant systems used, in the order of theirfrequency of use. The three most frequently used dental

5
Table 2A Associations of causal factors of tooth extraction,
implant design, and prosthesis type with prevalence of periimplant diseases
Causal factors of tooth extraction
Periodontitis
Fracture tooth
CariesApical periodontitis
External injury
Birth defectRe-implantation
Perforated tooth
Unknown
Implant design
One-piece
Soft-tissue level (two-piece)
Bone level (two-piece)
Type of prosthesis
Screw-retained
Cement-retained
Peri-implant diseases
Healthy peri-implant tissue
Peri-implant mucositis
Peri-implantitisn = 267122 (46.0%)
61 (22.8%)
43 (16.1%)
5 (1.9%)5 (1.9%)3 (1.1%)2 (0.7%)1 (0.4%)25 (9.4%)
2 (0.8%)82 (30.7%)
183 (68.5%)
99 (37.0%)
168 (63.0%)
152 (57.0%)
89 (33.3%)
26 (9.7%)

Fig. 1   Sites and numbers of dental implants. Upper: maxilla.
Lower: mandible. There were 420 dental implants in the maxilla
and 566 in the mandible. The upper and lower first molars werethe most frequent sites of dental implants.

Table 2B Associations of peri-implant diseases with implant design and prosthesis type
One-piece (2)Healthy peri-implant tissue
Peri-implant mucositis
Peri-implantitis

2 (100%)0 (0%)
0 (0%)

Soft-tissue level (82)
two-piece
47 (57.3%)
26 (31.7%)
9 (11.0%)

Fig. 2   Implant systems used.

implants were the Nobel Replace (47; 17.6%), Straumann(44; 16.5%), and Brånemark systems (40; 15.0%). Figure
3 shows the surface textures of the implant bodies. The
three most frequently used implant surfaces were TiUnite(76; 28.5%), SLA surface (41; 15.4%), and hydroxyapa-

Bone-level (183)
two-piece
103 (56.3%)
63 (34.4%)
17 (9.3%)

Screw-retained(99)
54 (54.5%)
36 (36.4%)
9 (9.1%)

Cement-retained(168)
98 (58.3%)
53 (31.6%)
17 (10.1%)

Fig. 3   Surface textures of implant bodies.

tite (32; 12%). Bone graft substitutes were used for 77
patients (29%) during dental implant surgery, and thedetails are shown in Table 3. The two most frequently
used bone graft substitutes were autologous bone (33;43%) and β-tricalcium phosphate (30; 39%). Duration of

6
Table 3 Bone graft substitutes

Table 4 Functional duration of implants

Autologous bone
33 (43%)β-TCP
30 (39%)FDBA
5 (6.5%)DFDBA
2 (2.6%)
Bio-Oss
2 (2.6%)
Periosteum
1 (1.3%)
Boneject
1 (1.3%)β-TCP+Hydroxyapatite
1 (1.3%)
GEM 21S
1 (1.3%)
Hydroxyapatite
1 (1.3%)n = 77, FDBA: Freeze-dried bone allograft; DFDBA: Demineralized
freeze-dried bone allograft; Bio-Oss: Geistlich, Wolhusen,
Switzerland; Boneject: KOKEN Co., Ltd, Tokyo, Japan; GEM21:
Osteohealth, NY, USA.

Mean functional duration, months>260
240~259
220~239200~219180~199160~179140~159
120~139100~119
80~99
60~79
40~59
36~39
n = 267, Mean ± SD.

76.6 ± 46.1
1 (0.4%)2 (0.8%)2 (0.8%)3 (1.1%)3 (1.1%)8 (3.0%)7 (2.6%)14 (5.2%)
24 (9.0%)25 (9.4%)
54 (20.2%)
77 (28.8%)47 (17.6%)

Table 5 Patient comorbidities
Disease (149 per 267 participants)
Hypertension
Hyperlipidemia
Cardiovascular disorders
Diabetes mellitus
Stomach disease
Thyroid dysfunction
Gout
Liver ailment
AsthmaRheumatoid arthritis
Glaucoma
Kidney disease
Osteoporosis
Cataract
Stroke

No.
57
22
15
11
8
6
5
4
4
4
4
3
3
2
1

implant function is shown in Table 4. Mean duration offunction was 76.6 ± 46.1 months. In total, 149 patients(56%, Table 5) reported comorbidities, and 37 had morethan one comorbidity. The most frequent pre-existing
medical condition was hypertension (n = 57). Twentytwo patients had hyperlipidemia, 15 had cardiovasculardisorders, and 11 had diabetes mellitus.
The width of keratinized mucosa at the buccal centerof the implant is shown in Fig. 4. Men and women did
not differ in the width of keratinized mucosa. The width
was 2 mm in 62 (23.2%) patients, 3 mm in 58 (21.7%), 0
mm in 50 (18.7%), 4 mm in 38 (14.2%), and 1 mm in 31(11.6%). There was no association between peri-implantdiseases and the width of keratinized mucosa.

Fig. 4   Width of keratinized mucosa around implants. The widthof keratinized mucosa (mm) at the buccal center of implants isrepresented by the bars.

Table 6A shows the results of bacterial analyses ofplaque samples from the deepest PPD sites of implants
and natural teeth. The bacterial count of A. actinomycetemcomitans was undetectable in 261 (97.8%) and
262 (98.1%) samples from implants and natural teeth,
respectively. P. intermedia was undetectable in 220(82.4%) and 210 (78.7%) samples from implants andnatural teeth, respectively, and P. gingivalis could not
be detected in 188 (70.4%) and 183 (68.5%) samples of
implants and natural teeth, respectively. We divided the267 participants into three groups (healthy peri-implanttissue, peri-implant mucositis, and peri-implantitis),to investigate mean subgingival bacterial counts in the
deepest PPD sites of implants and natural teeth in the7
Table 6A Comparison of subgingival bacterial counts in the pockets
Bacterial counts (Log10)
Total bacteria
A. actinomycetemcomitans
P. intermedia
P. gingivalis

0
0
0
261
262
220
210
188
183

Implant
Natural teeth
Implant
Natural teeth
Implant
Natural teeth
Implant
Natural teeth

≥0.01
0
0
0
0
0
0
0
0

≥1
0
0
3
0
29
22
17
7

≥2
0
0
1
1
11
19
31
23

≥3
67
72
2
4
6
15
23
36

≥4
137
102
0
0
1
1
7
17

≥5
58
84
0
0
0
0
1
1

≥6
5
9
0
0
0
0
0
0

≥3.5
0
1
0
1

≥4
1
0
0
3

n = 267

Table 6B Mean subgingival bacterial counts in the pockets of implant and natural teeth
Implant sites (Log10)

Total bacteria

A. a.

P. i.

P. g.

Healthy peri-implant tissue

4.43 ± 0.67

0.03 ± 0.28

0.25 ± 0.67

0.56 ± 1.11

Peri-implant mucositis

4.41 ± 0.67

0.09 ± 0.50

0.33 ± 0.77

**

**

**

0.83 ± 1.39

*

**

**

Peri-implantitis

4.93 ± 0.82

0.05± 0.25

0.80 ± 1.32

2.17 ± 1.77

Natural teeth sites (Log10)

Total bacteria

A. a.

P. i.

P. g.

Healthy peri-implant tissue

4.51 ± 0.72

0.02 ± 0.25

0.41 ± 0.91

0.75 ± 1.41

Peri-implant mucositis

4.55 ± 0.77

0.13 ± 0.61

0.67 ± 1.21

1.22 ± 1.63

Peri-implantitis

4.84 ± 0.86

0.00 ± 0.00

0.36 ± 0.90

1.87 ± 1.93**

Mean ± SD, *P < 0.05, **P < 0.01

Table 7A IgG titers against periodontal bacteria
IgG titerA. actinomycetemcomitans
P. intermedia
E. corrodens
P. gingivalisn = 254

≤−1.0
0
0
3
13

≥−1.0
43
84
70
21

≥−0.5
151
128
144
33

≥0
39
29
22
44

≥0.5
10
7
9
40

≥1.0
5
2
1
36

≥1.5
2
1
3
36

≥2.0
0
1
2
19

≥2.5
2
0
0
5

≥3.0
1
1
0
3

Table 7B Mean IgG titers against periodontal bacteria, by group
IgG titer
Healthy peri-implant tissue
Peri-implant mucositis
Peri-implantitis
Mean ± SD

A. a.
−0.18 ± 0.53
−0.17 ± 0.75
−0.22 ± 0.49

P. i.
−0.33 ± 0.49
−0.29 ± 0.43
−0.21 ± 0.97

same oral cavity. Mean bacterial counts of total bacteria,
A. a., and P. i. in the deepest PPD sites of natural teeth,and mean bacterial counts of A. a. at the implant site, werevery similar among the three groups. The mean bacterial
counts of total bacteria, P. i., and P. g. at the implant sitesof the peri-implantitis group were significantly higher
than those for the healthy peri-implant tissue and periimplant mucositis groups. The mean bacterial count of
P. g. at natural teeth sites of the peri-implantitis groupwas significantly higher than in the healthy peri-implant

E. c.
−0.31 ± 0.44
−0.35 ± 0.38
−0.27 ± 0.72

P. g.
3.58 ± 6.92
5.53 ± 11.58
6.87 ± 11.12

tissue group (Table 6B). Table 7A shows the results of
IgG titers against periodontal bacteria (A. a., P. i., E. c.,and P. g.). The IgG titer against P. gingivalis was highest
among these periodontal bacteria. We then divided theparticipants into three groups (healthy peri-implant tissue,
peri-implant mucositis, and peri-implantitis), to examine
mean IgG titers. The mean IgG titers against A. a., P. i.,and E. c. were very low and quite similar. The mean IgG
titer of P. g. was highest in the peri-implantitis group;
however, the difference was not significant (Table 7B).

8
Table 8 Association between peri-implant diseases and clinical parameters of implants
Healthy peri-implant tissue
Peri-implant mucositis

mPlI

mSBI

PPD

0.3 ± 0.6

0.0 ± 0.0

2.7 ± 1.2

**

**

**

1.0 ± 0.7

Peri-implantitis

0.9 ± 0.9**

1.3 ± 0.5**

3.9 ± 1.1****

1.7 ± 0.9

5.6 ± 2.0**

Mean ± SD, **P < 0.01

Table 9A Association between history of peridontal diseases and peri-implant diseases
History of peridontal diseases before implant treatment
Healthy
Gingivitis
Slight CP
Moderate CP
Severe CP
Aggressive periodontitis

Healthy peri-implant tissue
2 (100%)2 (25%)
52 (71.2%)
66 (56.9%)30 (45.5%)0Peri-implant mucositis
0
6 (75%)
13 (17.8%)
40 (34.5%)
29 (43.9%)
1 (50%)

Peri-implantitis00
8 (11.0%)
10 (8.6%)
7 (10.6%)
1 (50%)

Table 9B Occurrence of peri-implant diseases in the slight, moderate and severe CP patients
History of chronic
periodontitis
Slight CP
Moderate CP
Severe CP

Healthy periimplant tissue
52
66
30

Peri-implant diseases
Peri-implant
Peri-implantitis
mucositis (PM)
(PI)
13
8
40
10
29
7

Table 8 shows data on the associations of peri-implantdiseases with clinical parameters (mPlI, mSBI, and PPD).
The scores for clinical parameters were significantly
higher in the peri-implant mucositis and peri-implantitis
groups than in the healthy peri-implant tissue group. The
mSBI scores and PPD were significantly higher in theperi-implantitis group than in the peri-implant mucositis
group.
Analysis of the association between history of periodontal diseases and peri-implant diseases is shown in
Table 9A. Periodontal condition before implant treatment
was classified into six groups (healthy, gingivitis, slight
CP, moderate CP, severe CP, and aggressive periodontitis). Among patients with slight CP, moderate CP, or
severe CP before implant treatment, 71.2%, 56.9%, and45.5%, respectively, had healthy peri-implant tissue;
17.8%, 34.5%, and 43.9% had peri-implant mucositis;
and 11%, 8.6%, and 10.6% had peri-implantitis. The
chi-square test for independence was used to test the null
hypothesis that history of periodontitis before implant
treatment and the extent of peri-implant disease wereindependent. The results indicated that slight CP was
significantly associated with healthy peri-implant tissue
and that moderate and severe CP were significantly asso-

Significance (P-value)
Healthy vs PM

Healthy vs PI

PM vs PI

8.33E-110.00061
0.861

1.35E-13
4.74E-14
8.31E-06

0.238
1.67E-06
1.71E-05

ciated with healthy peri-implant tissue and peri-implantmucositis (Table 9B).

Discussion

We investigated a sample of patients who had been treatedfor periodontitis in dental hospitals or private dental
clinics before implant placement. They had received
one or more implants, were followed for more than 3
years after loading, and were consecutively examined atperiodontal maintenance appointments. The prevalencesof peri-implant mucositis and peri-implantitis were33.3% and 9.7%, respectively. Estimating the frequency
of peri-implant disease is difficult and depends greatly
on assessment procedures. Variability in the prevalenceof peri-implant disease might be attributable to differences between studies in the clinical parameters used toassess and define the disease. In the present study, weused the diagnostic criteria suggested in the Consensus
of the Seventh European Workshop on Periodontology.
Peri-implant mucositis was defined as bleeding on gentle
probing, and peri-implantitis was defined as changes in
the level of the crestal bone in conjunction with BOP.
Previous studies reported varying prevalence and incidence rates for peri-implant disease, perhaps because of9variation in the duration of prosthesis use (1,35). Studiesof the incidence of peri-implant disease suggest that thefollow-up period for an implant system should be at least
5 years (8,35). In the present study, the average functional
duration was 76.6 months (6.38 years); thus, we believethat the present results are valid.
Different types of implant systems were used in thisstudy, and variability in surface characteristics could
have influenced the prevalence of peri-implant diseases(17,36). However, no clinical differences were seen
between the systems, as the vast majority of fixtures used
a TiUnite (28.5%), SLA surface (15.4%), or hydroxyapatite coating (12.0%).
Zupnik et al. reported that implant failure was strongly
associated with diabetes (37), whereas another reportfound no association (38). In this study, diabetes was not
associated with the development of peri-implant diseases,
perhaps because only a small number of patients withdiabetes were enrolled.
Smoking was identified as a strong risk factor for
peri-implant diseases (6,15,35,38-41). As compared with
nonsmokers, smokers have a 31-fold chance of having
peri-implantitis (39). However, a previous study (40)reported peri-implantitis rates of 23.53% for smokers
and 16.51% for nonsmokers, but the difference was not
significant. Twenty-two smokers, 52 former smokers,
and 193 nonsmokers were included in the present study.
Among the 22 smokers, eight (36.4%) had peri-implantmucositis, but none had peri-implantitis (0%). Amongthe 52 former smokers, 17 (32.7%) had peri-implantmucositis, and four had peri-implantitis (8%). Amongthe 193 nonsmokers, 64 (33.2%) had peri-implant mucositis, and 22 had peri-implantitis (11.4%). These results
suggest that smoking is not associated with developmentof peri-implant diseases.
It remains unclear whether a zone of keratinizedmucosa is required to maintain the health of peri-implanttissue. Several reviews noted insufficient evidence for theneed for keratinized mucosa around implants to maintainperi-implant tissue health (16,35,42,43). In the present
study, the width of keratinized mucosa was not associated with development of peri-implant diseases.
The effects of implant overload on bone and implantloss in clinically well-integrated implants have not been
comprehensively studied. In animal experiments, overload mimicked by supra-occlusal contacts in the presenceof inflammation significantly increased plaque-inducedbone resorption (44). With respect to implant prosthodontics, the risk for peri-implantitis was 3.6 times higher for
cemented restorations, 2.4 times higher when wear facets
were present on the prosthetic crown, and 16.1 times

higher for full-mouth rehabilitations (45). In the present
study, prosthesis type (screw- or cement-retained) was
not significantly associated with peri-implant diseases(Table 2B).
P. intermedia counts were significantly higher at
implant sites in the peri-implantitis group, and P. gingivalis counts were higher in the implant and natural-teeth
sites in the peri-implantitis groups (Table 6B). Therefore,
P. intermedia and P. gingivalis might be associatedwith development of peri-implantitis. However, several
recent studies reported that the microbial composition of
biofilm was more complex in peri-implant disease than inperiodontal disease. The prevalence of periodontopathic
bacteria is not high in peri-implantitis (26,27,46,47).
Future studies may help to clarify these findings.
IgG titers were significantly higher in periodontitis
patients than in healthy controls, especially among
those with sites of PPD greater than 4 mm (33). The
mean IgG titer against P. gingivalis was highest in theperi-implantitis group; however, the differences were notstatistically significant (Table 7B).
Previous studies suggest that oral hygiene conditions
are an important variable associated with peri-implant
health (9,48,49). In this study, high index scores for mPlI
were significantly associated with development of periimplant mucositis and peri-implantitis. In addition, highindex scores for mSBI and deeper PPD were significantly
associated with development of peri-implant mucositis
and peri-implantitis (Table 8). These results suggest thata high plaque score increases the risk of developing periimplant diseases. Thus, patient compliance, including
plaque control and supportive therapy, may be importantin peri-implant diseases.
Several studies reported that individuals with histories
of periodontal disease appear to have a higher risk ofperi-implant diseases (13,14,50). In the present study,
we divided patients with CP into three groups (slight,
moderate, and severe CP). The presence of slight CP
before implant treatment was significantly associatedwith healthy peri-implant tissue, and the presence ofmoderate or severe CP was significantly associated withhealthy peri-implant tissue and peri-implant mucositis(Table 9A, B).
In conclusion, the patient-based prevalences of periimplant mucositis and peri-implantitis were 33.3% and9.7%, respectively. These values are lower than thosereported previously. The present results suggest that poor
oral hygiene and a history of periodontitis are strong risk
factors for peri-implant diseases. Patient compliancewith elements such as periodontal therapy before andafter implant placement, plaque control, and supportive

10

therapy may be crucial in maintaining the health of periimplant tissue.

Acknowledgements

This work was supported by a Research Grant from the JapaneseSociety of Periodontology. All procedures performed in studies
involving human participants were in accordance with the
ethical standards of the Institutional Internal Review and Ethics
Committee of the JSP (JSP2012001) and with the 1964 Helsinki
Declaration and its later amendments or with comparable ethicalstandards.
Clinical Trials: UMIN000008954.

Conflict of interest

The authors have no conflict of interest to declare.

References

1. Lang NP, Berglundh T (2011) Periimplant diseases: where are
we now?--consensus of the seventh European workshop on
periodontology. J Clin Periodontol 38, Suppl 11, 178-181.
2. Lindhe J, Berglundh T, Ericsson I, Liljenberg B, Marinello
C (1992) Experimental breakdown of peri-implant and periodontal tissues. A study in the beagle dog. Clin Oral Implants
Res 3, 9-16.
3. Pontoriero R, Tonelli MP, Carnevale G, Mombelli A, Nyman
SR, Lang NP (1994) Experimentally induced peri-implantmucositis. A clinical study in humans. Clin Oral Implants Res
5, 254-259.
4. Esposito M, Hirsch JM, Lekholm U, Thomsen P (1998)
Biological factors contributing to failures of osseointegrated
oral implants. (II). Etiopathogenesis. Eur J Oral Sci 106,721-764.
5. Zitzmann NU, Berglundh T (2008) Definition and prevalenceof peri-implant diseases. J Clin Periodontol 35, 8 Suppl,
286-291.
6. Lindhe J, Meyle J (2008) Peri-implant diseases: consensus
report of the sixth European workshop on periodontology. J
Clin Periodontol 35, 8 Suppl, 282-285.
7. Lachmann S, Stehberger A, Axmann D, Weber H (2013) The
peri-implant health in patients attending an annual recall
program. A clinical and microbiological study in 74 patientsfrom the Tübingen Implant Registry. Clin Oral Implants Res
24, 1300-1309.
8. Berglundh T, Persson L, Klinge B (2002) A systematic reviewof the incidence of biological and technical complications in
implant dentistry reported in prospective longitudinal studies
of at least 5 years. J Clin Periodontol 29, Suppl 3, 197-212.
9. Ferreira SD, Silva GL, Cortelli JR, Costa JE, Costa FO(2006) Prevalence and risk variables for peri-implant disease
in Brazilian subjects. J Clin Periodontol 33, 929-935.
10. Roos-Jansåker AM, Renvert H, Lindahl C, Renvert S (2006)
Nine- to fourteen-year follow-up of implant treatment. Part
III: factors associated with peri-implant lesions. J Clin Periodontol 33, 296-301.
11. Koldsland OC, Scheie AA, Aass AM (2010) Prevalenceof peri-implantitis related to severity of the disease withdifferent degrees of bone loss. J Periodontol 81, 231-238.
12. Mir-Mari J, Mir-Orfila P, Figueiredo R, Valmaseda-Castellón
E, Gay-Escoda C (2012) Prevalence of peri-implant diseases.
A cross-sectional study based on a private practice environment. J Clin Periodontol 39, 490-494.
13. Roccuzzo M, Bonino F, Aglietta M, Dalmasso P (2012)
Ten-year results of a three arms prospective cohort study
on implants in periodontally compromised patients. Part 2:
clinical results. Clin Oral Implants Res 23, 389-395.
14. Pjetursson BE, Helbling C, Weber HP, Matuliene G, Salvi
GE, Brägger U et al. (2012) Peri-implantitis susceptibility as
it relates to periodontal therapy and supportive care. Clin Oral
Implants Res 23, 888-894.
15. Strietzel FP, Reichart PA, Kale A, Kulkarni M, Wegner B,
Küchler I (2007) Smoking interferes with the prognosis ofdental implant treatment: a systematic review and metaanalysis. J Clin Periodontol 34, 523-544.
16. Lin GH, Chan HL, Wang HL (2013) The significance of
keratinized mucosa on implant health: a systematic review. J
Periodontol 84, 1755-1767.
17. Teughels W, Van Assche N, Sliepen I, Quirynen M (2006)
Effect of material characteristics and/or surface topographyon biofilm development. Clin Oral Implants Res 17, Suppl 2,
68-81.
18. Roccuzzo M, De Angelis N, Bonino L, Aglietta M (2010)
Ten-year results of a three-arm prospective cohort study
on implants in periodontally compromised patients. Part 1:
implant loss and radiographic bone loss. Clin Oral Implants
Res 21, 490-496.
19. Costa FO, Takenaka-Martinez S, Cota LO, Ferreira SD, Silva
GL, Costa JE (2012) Peri-implant disease in subjects withand without preventive maintenance: a 5-year follow-up. J
Clin Periodontol 39, 173-181.
20. Mombelli A, Van Oosten MAC, Schürch E, Lang NP (1987)
The microbiota associated with successful or failing osseointegrated titanium implants. Oral Microbiol Immunol 2,
145-151.
21. Renvert S, Lindahl C, Renvert H, Persson GR (2008) Clinicaland microbiological analysis of subjects treated with Brånemark or AstraTech implants: a 7-year follow-up study. Clin
Oral Implants Res 19, 342-347.
22. Shibli JA, Melo L, Ferrari DS, Figueiredo LC, Faveri M,
Feres M (2008) Composition of supra- and subgingival
biofilm of subjects with healthy and diseased implants. Clin
Oral Implants Res 19, 975-982.
23. Botero JE, González AM, Mercado RA, Olave G, Contreras
A (2005) Subgingival microbiota in peri-implant mucosa
lesions and adjacent teeth in partially edentulous patients. J
Periodontol 76, 1490-1495.
24. Quirynen M, Vogels R, Peeters W, van Steenberghe D, Naert
I, Haffajee A (2006) Dynamics of initial subgingival colonization of 'pristine' peri-implantpockets. Clin Oral Implants
Res 17, 25-37.
25. Cho-Yan Lee J, Mattheos N, Nixon KC, Ivanovski S (2012)11
Residual periodontal pockets are a risk indicator for periimplantitis in patients treated for periodontitis. Clin Oral
Implants Res 23, 325-333.
26. Koyanagi T, Sakamoto M, Takeuchi Y, Maruyama N, Ohkuma
M, Izumi Y (2013) Comprehensive microbiological findingsin peri-implantitis and periodontitis. J Clin Periodontol 40,
218-226.
27. Maruyama N, Maruyama F, Takeuchi Y, Aikawa C, Izumi Y,
Nakagawa I (2014) Intraindividual variation in core microbiota in peri-implantitis and periodontitis. Sci Rep 4, 6602.
28. Silness J, Löe H (1964) Periodontal disease in pregnancy. II.
Correlation between oral hygiene and periodontal condition.
Acta Odontol Scand 22, 121-135.
29. Löe H, Silness J (1963) Periodontal disease in pregnancy. I.
Prevalence and severity. Acta Odontol Scand 21, 533-551.
30. Armitage GC (1999) Development of a classification systemfor periodontal diseases and conditions. Ann Periodontol 4,
1-6.
31. Tadokoro K, Yamaguchi T, Kawamura K, Shimizu H,
Egashira T, Minabe M et al. (2010) Rapid quantification of
periodontitis-related bacteria using a novel modification of
Invader PLUS technologies. Microbiol Res 165, 43-49.
32. Morozumi T, Kubota T, Abe D, Shimizu T, Komatsu Y,
Yoshie H (2010) Effects of irrigation with an antiseptic andoral administration of azithromycin on bacteremia caused byscaling and root planing. J Periodontol 81, 1555-1563.
33. Kudo C, Naruishi K, Maeda H, Abiko Y, Hino T, Iwata M etal. (2012) Assessment of the plasma/serum IgG test to screen
for periodontitis. J Dent Res 91, 1190-1195.
34. Kanda Y (2013) Investigation of the freely available easyto-use software 'EZR' for medical statistics. Bone Marrow
Transplant 48, 452-458.
35. Heitz-Mayfield LJ (2008) Peri-implant diseases: diagnosis
and risk indicators. J Clin Periodontol 35, 8 Suppl, 292-304.
36. Renvert S, Polyzois I, Claffey N (2011) How do implantsurface characteristics influence peri-implant disease? J Clin
Periodontol 38, Suppl 11, 214-222.
37. Zupnik J, Kim SW, Ravens D, Karimbux N, Guze K (2011)
Factors associated with dental implant survival: a 4-year
retrospective analysis. J Periodontol 82, 1390-1395.
38. Anner R, Grossmann Y, Anner Y, Levin L (2010) Smoking,diabetes mellitus, periodontitis, and supportive periodontal
treatment as factors associated with dental implant survival:a long-term retrospective evaluation of patients followed for
up to 10 years. Implant Dent 19, 57-60.

39. Rinke S, Ohl S, Ziebolz D, Lange K, Eickholz P (2011)
Prevalence of periimplant disease in partially edentulous
patients: a practice-based cross-sectional study. Clin Oral
Implants Res 22, 826-833.
40. Simonis P, Dufour T, Tenenbaum H (2010) Long-term
implant survival and success: a 10-16-year follow-up of
non-submerged dental implants. Clin Oral Implants Res 21,
772-777.
41. Atieh MA, Alsabeeha NHM, Faggion Jr CM, Duncan WJ(2013) The frequency of peri-implant diseases: a systematic
review and meta-analysis. J Periodontol 84, 1586-1598.
42. Wennström JL, Derks J (2012) Is there a need for keratinized mucosa around implants to maintain health and tissue
stability? Clin Oral Implants Res 23, Suppl 6, 136-146.
43. Brito C, Tenenbaum HC, Wong BK, Schmitt C, NogueiraFilho G (2014) Is keratinized mucosa indispensable tomaintain peri-implant health? A systematic review of theliterature. J Biomed Mater Res B Appl Biomater 102,643-650.
44. Naert I, Duyck J, Vandamme K (2012) Occlusal overload
and bone/implant loss. Clin Oral Implants Res 23, Suppl 6,
95-107.
45. Dalago HR, Schuldt Filho G, Rodrigues MA, Renvert S,
Bianchini MA (2016) Risk indicators for peri-implantitis. A
cross-sectional study with 916 implants. Clin Oral Implants
Res doi: 10.1111/clr.12772.
46. Kumar PS, Mason MR, Brooker MR, O'Brien K (2012) Pyrosequencing reveals unique microbial signatures associatedwith healthy and failing dental implants. J Clin Periodontol
39, 425-433.
47. Dabdoub SM, Tsigarida AA, Kumar PS (2013) Patient-specificanalysis of periodontal and peri-implant microbiomes. J Dent
Res 92, 12 Suppl, 168S-175S.
48. Zitzmann NU, Berglundh T, Marinello CP, Lindhe J (2001)
Experimental peri-implant mucositis in man. J Clin Periodontol 28, 517-523.
49. Mombelli A, Décaillet F (2011) The characteristics ofbiofilms in peri-implant disease. J Clin Periodontol 38, Suppl
11, 203-213.
50. De Boever AL, Quirynen M, Coucke W, Theuniers G, De
Boever JA (2009) Clinical and radiographic study of implant
treatment outcome in periodontally susceptible and nonsusceptible patients: a prospective long-term study. Clin Oral
Implants Res 20, 1341-1350.