Keywords
marginal bone level - peri-implant disease - peri-implantitis
Introduction
Dental implants have been a part of our lives since 1965 when studies of Branemark
commenced. Today, ever increasing number of dental implants in total or partial edentulous
patients provides an outstanding treatment alternative to conventional prosthetic
rehabilitation all around the world. However, widespread use of dental implants has
brought alone a gradually increasing condition called “disease of peri-implant tissues”[1]. Therefore, the treatment of peri-implant diseases has been an upmost importance.
At first, interrelationship between dental implant and surrounding soft and hard tissues
was needed to be clarified at molecular cellular and clinical level.[2]
[3] To provide treatment for peri-implant disease, in the light of early studies, it
has been realized that peri-implant lesions are very similar to periodontal lesions
in terms of infectious and inflammatory characteristics.[4] Therefore, dental professionals have attempted to treat peri-implant lesions using
their experience and knowledge on periodontal diseases.[5]
[6] However, as the incident of peri-implant diseases rose, clinicians were in need
of classifying them.
In 1994, Albrektsson and Isidor[1] proposed for the first time the definitions of two peri-implant diseases, as PM
and peri-implantitis. PM was defined as a reversible inflammatory reaction in the
soft tissues surrounding a functioning implant while peri-implantitis as inflammatory
reactions associated with progressive loss of supporting bone. As the knowledge expanded
over the years, Zitzmann and Berglundh[7] revisited the descriptions where PM was defined as the presence of inflammation
in the mucosa at an implant with no signs of supporting bone loss and peri-implantitis
as the presence of supporting bone loss in addition to inflammation in the mucosa.
In the consensus report of the sixth European Workshop on Periodontology, in addition
to descriptions proposed by Zitzmann and Berglundh,[7] it was recommended that the extent as well as the severity (amount of bone loss)
of peri-implant lesions are needed to be clarified.[8] Taking this suggestion into account, Koldsland et al[9] evaluated the severity of peri-implantitis in terms of different levels of radiographic
bone loss and probing depth (PD) with the presence of bleeding on probing (BOP) and/or
suppuration. Absence of a well-established definition for peri-implant diseases leads
researchers to use several criteria in the clinical studies yielding to different
conclusions which may result in misdiagnosis and confusion. Ferreira et al[10] described PM as the presence of BOP and peri-implantitis as the presence of BOP
and/or suppuration, pocket depth ≥5 mm associated with the presence of bone loss.
Based on these definitions, they found a prevalence of 64.6 and 8.9% for PM and peri-implantitis,
respectively. On the contrary, Renvert et al[11] observed peri-implantitis prevalence as 63.7%, taking into account the criterion
of Sanz and Chapple[12] who described peri-implantitis as peri-implant bone loss >2 mm in association with
clinical signs of inflammation.
The lack of widely accepted diagnostic criteria for peri-implant diseases with particular
attention to PD and marginal bone level makes it difficult to interpret the results
of published studies. Therefore, the aim of this study was to explore the prevalence
of peri-implant diseases and subclassify peri-implantitis based on different levels
of radiographic and clinical findings.
Materials and Methods
This cross-sectional study was conducted in consecutive 200 patients who applied to
the Department of Periodontology, Dental Faculty, Marmara University, Istanbul, Turkey
between October 2014 and December 2015. The study was approved by the Ethics Committee
of the Marmara University (70737436-050.06.04-1400123324). Subjects ≥18 years of age and having dental implants in function for
at least 1 year were recruited. The implants had been placed either in private offices
or at university clinics.
Clinical Examination
Demographic information regarding age, sex, history of periodontitis, and smoking
habit were obtained from patients. Full mouth plaque index (PI),[13] gingival index (GI)[14], and PD at six sites per tooth/implant were measured. PI and GI were measured on
mesiobuccal, midbuccal, distobuccal, and midlingual surfaces around all teeth and
implants. PD was also measured in mesiolingual and distolingual sites. Periodontal
probe with a 0.5 mm diameter (University of North Carolina PCPUNC15, Hu Friedy Ins
Co. A.B.D.) was used for clinical examination. Additionally, BOP, presence of suppuration,
presence of midbuccal keratinized tissue, subgingival restoration margins, jaw of
placement, mean function time, and implant-abutment interface were evaluated at implant
sites. BOP was assessed as the presence/absence of bleeding observed 30 seconds after
probing and calculated as percentage and suppuration as the discharge of pus immediately
after probing.
Radiographs
The same clinician used standard long-cone parallel technique for the radiographic
examination of all implants. A single researcher (E.E.) evaluated the implant-abutment
interface and measured the distance between the reference point of implant platform
level and the most apical bone in contact with the implant, both on mesial and distal
sites.[11] The site with the most pronounced bone loss was chosen to represent the marginal
bone loss (MBL) around each implant.[9]
[15] The ImageJ (Wayne Rasband; National Institute of Health; MD, United States) program
was used for the analysis of peri-implant bone levels. Each periapical had a standard
1 mm marker ([Fig. 1]). The distance was converted into millimeter by dividing the length of the defect
into the length of the marker calculated by ImageJ program.
Fig. 1 Analysis of radiographic bone loss.
Definitions
Peri-implant health was defined as having no clinical signs of inflammation and MBL
< 2 mm, PM as the presence of BOP and/or suppuration and MBL < 2 mm, peri-implantitis
as the presence of BOP and/or suppuration and MBL ≥2 mm as proposed by the eighth
European Workshop on Periodontology.[12]
Furthermore, peri-implantitis was further subclassified using a severity leveling
in terms of MBL and PD as shown below:
-
MBL ≥2 mm at PD ≥4 and PD ≥5 mm
-
MBL ≥3 mm at PD ≥4 and PD ≥5 mm
-
MBL ≥4 mm at PD ≥4 and PD ≥5 mm
According to these criteria, characteristics of the subjects, clinical and radiographic
characteristics of peri-implant tissues in relation to peri-implant health and disease
were evaluated. Additionally, prevalence of peri-implant health and diseases at subject
and implant level were measured.
Intraexaminer Calibration
All the measurements were performed by an experienced clinician (E.E.). To assess
the intraexaminer variability for radiographic measurements, the mesial sites of the
first 25 implants and then 10 implants for each 50th implant were remeasured.[9] A total of 150 implants were used for calibration. The intraclass correlation coefficient
(ICC) was calculated as 0.87. Furthermore, to assess intraexaminer variability for
clinical measurements, PD (six sites/implant) of the first 25 implants were remeasured[9] and ICC was calculated as 0.97.
Data Analysis
The statistical analyses (SPSS v.15.0; SPSS, Chicago, IL, United States) included
descriptive statistics (mean ± standard deviation), Chi square, Kruskal–Wallis, and
Mann–Whitney U tests for clinical and radiographic parameters. The data were evaluated
both at subject and implant basis. The level of significance was set at p < 0.001.
Results
Subject Characteristics
The mean age of 200 subjects included in the present study was 52.8 ± 12.2 years and
63% were females. Subjects with smoking habit were 22% and those who had a history
of periodontitis constituted 64.5% of all. Registrations in relation to peri-implant
health and disease are presented in [Table 1]. According to the diagnostic criteria generated by Sanz and Chapple,[12] 2.5% of the subjects were diagnosed as healthy, 28% with PM, and 69.5% with peri-implantitis.
Table 1
Characteristics of the subjects with implants of which peri-implant tissues evaluated
according to the criteria of Sanz and Chapple[12]
|
Total
|
Healthy
|
Peri-implant mucositis
|
Peri-implantitis
|
p-Value
|
|
(n = 200)
|
(n = 5)
|
(n = 56)
|
(n = 139)
|
|
Abbreviation: SD, standard deviation.
aPearson’s Chi-square test.
bKruskal–Wallis test.
|
|
Female gender (%)
|
126 (63)
|
4 (80)
|
39 (69.6)
|
83 (59.7)
|
0.31a
|
|
Age (y) ± SD
|
52.8 ± 12.2
|
38.2 ± 12.2
|
49.5 ± 9.1
|
54.7 ± 12.8
|
0.01b
|
|
Smoking habit (%)
|
44 (22)
|
2 (40)
|
12 (21.4)
|
30 (21.6)
|
0.61a
|
|
History of periodontitis (%)
|
129 (64.5)
|
5 (100)
|
33 (59)
|
63 (45.3)
|
0.12a
|
Implant Characteristics and Peri-implant Clinical and Radiological Conditions
Out of 655 implants assessed in this study, 43.8% had been placed in the maxilla,
56.2% in the mandible ([Table 2]). Eighteen percent of the implants were in an anterior position (13–23 and 33–43),
whereas 92% had been placed in the premolar and molar region.
Table 2
Clinical and radiographic characteristics of peri-implant tissues in relation to peri-implant
health and disease
|
Total
|
Health
|
Peri-implant mucositis
|
Peri-implantitis
|
p-Value
|
|
Abbreviations: BOP, bleeding on probing; PD, probing depth; SD, standard deviation.
aPearson’s Chi-square test.
bKruskal–Wallis test.
c
p < 0.01 different from peri-implant mucositis, Mann–Whitney U test.
|
|
Jaw of placement (%)
|
|
Maxilla
|
43.8
|
41.7
|
37.8
|
47.6
|
0.11b
|
|
Mandible
|
56.2
|
58.3
|
62.2
|
52.4
|
0.20b
|
|
Mean function time (mo) ± SD
|
53.5 ± 36.7
|
40.8 ± 20.1
|
42.1 ± 30.8
|
61.2 ± 38.9
|
0.31b
|
|
BOP (%)
|
631 (93)
|
–
|
238 (100)
|
393 (100)
|
0.42a
|
|
Suppuration (%)
|
177
|
–
|
46 (19)
|
131 (33)
|
0.38a
|
|
Mean PD (mm) ± SD
|
3.7 ± 1.6
|
2.4 ± 0.5
|
3.2 ± 0.7
|
4.0c ± 1.8
|
0.000b
|
|
Mean marginal bone loss (mm) ± SD
|
3.0 ± 2.6
|
0.5 ± 0.6
|
0.8 ± 0.7
|
4.5c ± 2.2
|
0.000b
|
|
Prosthetic restoration type (%)
|
0.42b
|
|
Fixed
|
96.9
|
100
|
99.1
|
95.6
|
|
Overdenture
|
3.1
|
–
|
0.9
|
4.4
|
|
Keratinized tissue (midbuccal) (%)
|
0.58b
|
|
Present
|
64.9
|
79.2
|
75.2
|
57.8
|
|
Absent
|
35.1
|
21.8
|
24.8
|
42.2
|
|
Subgingival restoration margins (%)
|
0.17b
|
|
Present
|
54
|
54.2
|
70.6
|
44
|
|
Absent
|
46
|
45.8
|
29.4
|
56
|
|
Implant-abutment interface
|
0.45b
|
|
Platform switch
|
47.6
|
83.3
|
75.6
|
28.5
|
|
Platform match
|
52.4
|
16.7
|
24.4
|
71.5
|
Clinical examination demonstrated that BOP was present in 93% and suppuration in 27%
of the implants with a mean function time of 53.5 ± 36.7 months. The mean PD and MBL
of the implants were 3.6 ± 1.6 and 3.0 ± 2.6 mm, respectively. Registrations in relation
to peri-implant health and disease are presented in [Table 2]. Mean PD and MBL for implants with peri-implantitis were found significantly higher
compared with implants with PM (p < 0.001).
Majority of the implants observed were restorated with fixed prosthetics (96.9%).
Keratinized tissue was present at 64.9 and 57.8% of all implants and implants diagnosed
with peri-implantitis, respectively. Subgingival restoration margins were observed
in 54% of the implants, whereas it was 70.6% for implants with PM and 44% for implants
with peri-implantitis. Implants with platform switch were 47.6% of all. However, most
of the implants with peri-implantitis were with platform match (71.5%) ([Table 2]).
According to the previously mentioned diagnostic criteria (Sanz and Chapple[12]), 3.6% of the implants were healthy, 36% presented PM, and 60.4% peri-implantitis
([Table 3]).
Table 3
Prevalence of peri-implant health and diseases at subject and implant levels
|
Total
|
Health
|
Peri-implant mucositis
|
Peri-implantitis
|
|
Subject level (%)
|
200 (100)
|
5 (2.5)
|
56 (28)
|
139 (69.5)
|
|
Implant level (%)
|
655 (100)
|
24 (3.6)
|
238 (36)
|
393 (60.4)
|
Analysis of Prevalence at Subject and Implant Level using Different Diagnostic Criteria
When peri-implant tissues were evaluated at subject and implant level according to
Sanz and Chapple[12] diagnostic criteria, occurrence of PM was found 28 and 36%; peri-implantitis 69.5
and 60.4%, respectively ([Table 3]). Furthermore, when different levels of bone loss and PD parameters were added to
the criteria, the finding of peri-implantitis prevalence changed markedly and ranged
from 14.5 to 31% at subject level; from 10 to 22% at implant level as shown in ([Table 4]).
Table 4
Changes in the prevalence of peri-implantitis when different criteria were applied
|
BOP (±)
|
PD (mm)
|
Bone loss (mm)
|
n
|
%
|
p-Value
|
|
Abbreviations: BOP, bleeding on probing; n, number; PD, probing depth.
aPearson’s Chi-square test.
|
|
Subject level
|
|
+
|
≥4
|
≥2
|
62
|
31
|
0.000a
|
|
+
|
≥5
|
≥2
|
29
|
14.5
|
|
+
|
≥4
|
≥3
|
55
|
27.5
|
|
+
|
≥5
|
≥3
|
29
|
14.5
|
|
+
|
≥4
|
≥4
|
42
|
21
|
|
+
|
≥5
|
≥4
|
37
|
18.5
|
|
Implant level
|
|
+
|
≥4
|
≥2
|
143
|
22
|
0.000a
|
|
+
|
≥5
|
≥2
|
70
|
11
|
|
+
|
≥4
|
≥3
|
126
|
19
|
|
+
|
≥5
|
≥3
|
69
|
10.5
|
|
+
|
≥4
|
≥4
|
92
|
14
|
|
+
|
≥5
|
≥4
|
63
|
10
|
Discussion
As recommended in the consensus report of the sixth European Workshop on Periodontology,[8] a cross-sectional study design with implants placed both in university and private
clinics was used in this study to obtain information on the effectiveness rather than
efficacy of implant treatment. As most of the implant treatments are being performed
in private dental clinics worldwide, our study may give a clear point of view and
valid results about the prevalence of peri-implant diseases.
In this study, meeting the recommendation of using a cross-sectional study design
and a study sample greater than 100 implant-treated subjects,[8] clinical and radiological examinations were performed at 200 subjects having 655
implants similar to the other studies.[11]
[16]
[17]
Biofilm accumulating around natural teeth can also grow around dental implants and
on peri-implant tissues causing infection.[18] While defining peri-implant inflammation, it is also important to discriminate bone
loss due to infection and the one seen during remodeling.[19] Hence, in studies analyzing peri-implant disease prevalence, a criterion of an implant
in function at least for 1 year is accepted.[15]
[20]
[21] Therefore, only implants in function at least for 1 year were included for the analysis.
The mean age of patients with healthy implants was 38.2 years in our study. By the
increase in age, peri-implant situation worsened from PM to peri-implantitis which
was statistically significant (p < 0.01). In a study by Renvert et al,[11] 172 patients with a mean age of 68.2 years were analyzed and age was found as a
risk factor for peri-implantitis. In another study by Marrone et al,[22] peri-implantitis was found to be more in a group of people older than 65 years.
Parallel to our findings, age is considered as a risk factor for the development of
peri-implant diseases.
Cigarette smoking has been identified as a risk indicator in several studies,[23]
[24] causing the vasoconstruction of the vessels and decrease the nutrition of the tissues.
In our study, only 22% of patients were smokers, which makes it difficult to interpret
the results.
History of periodontitis was found to be a significant risk factor for the development
of peri-implant diseases[8]
[25]
[26]. Out of 200 patients included in this study, 64.5% were found to have a history
of periodontitis. Van der Weijden et al[27] calculated the implant success over 5 years in patients with and without a history
of periodontitis, and they observed more peri-implant bone loss and implant failures
in patients with a history of periodontitis. In a systematic review by Karoussis et
al,[28] increased PD and peri-implant bone loss were also found around implants placed in
patients with a history of periodontitis. Although a high number of patients were
with a history of periodontitis in our study, we did not find any correlation in peri-implant
health and disease. This may be explained by the discrepancy between numbers of the
healthy (n = 5) and peri-implant disease (n = 56 for PM and n = 139 for peri-implantitis) groups.
Roos-Jansåker et al[29] investigated the role of keratinized mucosa in peri-implant disease and found no
association between the absence of keratinized mucosa and disease progression. Wennström
and Derks[30] analyzed the literature if there was a need for keratinized mucosa to maintain health
and tissue stability but concluded that the current evidence was limited and weak.
Keratinized mucosa was present in 64.9% of all implants in this study. However, when
implants with peri-implantitis were further analyzed in relation to presence of keratinized
mucosa, there was no significant difference between health and disease which makes
it difficult to interpret the results as mentioned in previous studies.[29]
[30]
In the 11th Workshop of Periodontology,[31] for the primary prevention of peri-implant diseases, it was recommended that “if
cemented implant restorations have been selected, the restoration margins should be
located at the mucosal margin to allow meticulous removal of excess cement and clinicians
also have to be aware that implant placement at a submucosal level (to hide crown
margins) may carry a higher risk for peri-implant diseases”[31]. In our study, 70.6% of implants diagnosed with PM had subgingival restoration margins
confirming the risk of peri-implant disease. On the other hand, the presence of subgingival
restoration margins decreased to 44% for implants with peri-implantitis. This finding
may be explained by the MBL followed by gingival recession observed in most of the
peri-implantitis cases.
Farronato et al[32] found less MBL around platform switch implants as compared with platform match implants.
Finelle et al[33] assessed the effect of different design healing abutments on marginal bone level
and observed horizontal bone apposition on the implant shoulder of implants with narrow
healing abutments (platform switch) concluding that “the configuration of transmucosal
component directly influences marginal bone level.” In our study, 83.3% of healthy
implants and 75.6% of implants with PM had platform switch designs. On the other hand,
71.5% of implants diagnosed with peri-implantitis had platform match designs corroborating
the results of other studies.[32]
[33]
In this study, the definitions of peri-implant health and disease followed the recommendations
of the consensus report of the eighth European Workshop on Periodontology as the initial
radiographs of the patients were not present.[12] Our aim was to explore the prevalence of peri-implant diseases and subclassify peri-implantitis
based on different levels of radiographic and clinical parameters. The prevalence
of peri-implantitis was found to be 69.5 and 60.4% at subject and implant level, respectively.
However, with the inclusion of different PD and MBL levels, peri-implantitis prevalence
dramatically decreased to between 14.5 and 31% at subject level and between 10 and
22% at implant level. So far, studies analyzing the prevalence of peri-implant diseases
have yielded conflicting results[7]
[9]
[11]
[17] which can be explained by the use of different thresholds for diagnosis. Thus, the
prevalence rates of peri-implant diseases that have been claimed until today may be
controversial.
Mir-Mari et al[15] observed PM as 21.6% at implant level among subjects who were under strict maintenance
program. On the other hand, in our study, PM was found 36% at implant level. None
of the subjects included in our study sample followed a periodontal/peri-implant maintenance
program, which may explain the higher PM prevalence rates.
According to the recommendations in consensus report by Lindhe and Meyle,[8] when there is more than one implant in a single patient, the one with more inflammation
should be considered to describe the patient level peri-implant disease. As the other
studies in the literature, we calculated the patient level peri-implant disease according
to these criteria. This may explain the high percentage of subject level peri-implantitis
(69.5%) in our study.
Jemt and Johansson[34] observed MBL ≥3 mm only in 1.3% of the implants. Koldsland et al[9] using the same level of MBL to define peri-implantitis reported the prevalence 8.2%
at implant level. However, when they added PD value ≥4 mm into the criteria, peri-implantitis
prevalence decreased to 6%[9]. In our study, when PD ≥4 mm and MBL ≥3 mm were considered, the prevalence of peri-implantitis
was found to be 19% at implant level. Defining peri-implantitis as PD ≥4 mm and MBL
≥2 mm, Koldsland et al[9] observed the prevalence of peri-implantitis as 20.4 and 11.4% at subject and implant
levels, respectively, whereas in this study, the corresponding values were 31 and
22%, when the same definition was used and further subclassification was performed.
The size of our study sample both at subject and implant level was approximately twice
higher as compared with the study of Koldsland et al,[9] which gave rise to statistically significant difference. Additionally, all of the
implants observed by Koldsland et al[9] were placed in a university environment while our study sample consisted of implants
placed both in university and private clinics which reflects high clinical significance.
In the presence of initial radiographs taken right after implant placement, the analysis
of peri-implant health and disease can be studied much more precise. Because we analyzed
patients having implants placed in advance, it was one of the limitations of our study
that we could not compare them with the initial radiographs as they may have had the
bone resorption during the osseointegration period. Also, we were unable to know that
whether the implants were placed angulated or if they had machined collar surface
which some clinicians leave supracrestally. All these parameters may cause the miscalculation
of peri-implant bone level and PD resulting in different prevalences.
In conclusion, in the present study, the prevalence of PM was found to be 28 and 36%
and that of peri-implantitis to be 69.5 and 60.4% at subject and implant levels, respectively.
However, applying different thresholds to the peri-implantitis definition yielded
different prevalence rates ranging from 10 to 31%. Since no established diagnostic
criteria are being used today, results from clinical studies may not reflect the true
disease prevalence. There is a need for revision of peri-implant disease criteria
with the addition of subclassification system. Today, to treat periodontal diseases,
we diagnose and classify them. Therefore, with a precise definition of peri-implant
diseases, the treatment protocol for PM and peri-implantitis can be generalized and
more effective for all the population in the same way we have been doing for periodontal
diseases.
Clinical Relevance
In the absence of clinical signs of inflammation, clinicians can diagnose peri-implant
health. However, it is not the same to define a peri-implant disease as there are
so many patients and implant-based factors yielding different results.
