Prevalence of Peri-implant Diseases – Part 1

Aim: Determine the prevalence of peri-implant diseases; mucositis and periodontitis, of patients from the Center of Studies of Continuing Education in Implant Dentistry of the Federal University of Santa Catarina. In addition to the extension of the disease, the proportion of affected implants was studied. Materials and Methods: A cross-sectional study was carried out in 200 patients presenting 760 external-hexed cylindrical dental implant supported prosthesis with at least 1 year of loading time (range: 1–9 years). Probing depth, bleeding on probing and suppuration data was collected. Radiographs were required to evaluate supporting bone levels around implants. Results: One hundred and thirty-nine (69%) patients presented all healthy implants, 46 (23%) patients presented peri-implant mucositis and 15 (8%) presented peri-implantitis. The overall outcome was 547 (72%) healthy implants, 161(21%) with peri-implant mucostitis and 62 (7%) with peri-implantitis. Conclusion: According to the results, it is concluded that the prevalence of peri-implant mucositis was 23% and peri-implantitis to 8%.


Introduction
Peri-implant mucositis is clinically described as the inflammation of the peri-implant mucosa without bone loss; being the most important clinical diagnosis the presence of bleeding on probing (BOP) [2]. Periimplantitis is associated with clinical characteristics of mucositis in combination with radiographic presence of bone loss [3,4].
The prevalence of peri-implant diseases has not yet been presented with absolute values due to insufficient number of studies [1]. The absence of this information may be attributed to the lack of standardization of the scientific methodology; as well as, to the different definitions for peri-implant diseases [5][6][7]. It has been reported that peri-implant diseases are present in 28% to 56% [1] of individuals that present dental implants. Retrospective studies [8][9][10][11][12][13][14][15], with dental implant loaded for 5 or more years, revealed that periimplant diseases were a frequent finding; however, they showed very variable results. In 2008, the Council of the 6th European Workshop on Periodontology expressed the need for more studies to provide sufficient information in regards to the prevalence of peri-implant diseases [4].
This study aims to determine the prevalence of peri-implant diseases; mucositis and periodontitis, of patients from the Center of Continuing Education in Implant Dentistry (CEPID) of the Federal University of Santa Catarina (UFSC). In addition, the extension (the proportion of affected implants) of the disease was studied.

Materials and Methods
The present study was approved by the Human Ethics Committee of the Federal University of Santa Catarina and an informed consent was obtained from each participant.

Sample selection
Two hundred patients from the CEPID-UFSC database were randomly selected summing an amount of 760 external-hexed cylindrical implants presenting implant supported prosthesis placed for more than 1 year, from the period of 2001 to 2010. Of the 760 implants placed, 43% were mandibular teeth and 67% were maxillary. After initial adjustments of the suprastructures, the participants had not been recalled or maintained by the institute as part of a clinical routine, which was provided by the referring dentist.

Surgical protocol
A consensus report from the 3rd European Workshop on Periodontology used the bone level at implant loading as the baseline [16]. All the implants were place with the platform placed at the level of the alveolar crest. When the implant was planned to be placed at a lower level then the existing bony ridge, the crest or the edentulous ridge was reduced. The platform-crest level surgical protocol used by the institution allowed an expected saucerization of < 2 mm for reaching the biological width [17]. Therefore, a bone loss of ≥ 2 mm was considered peri-implantitis [14,18] when associated with presence of probing depth (PD) > 4 mm and/or bleeding/suppuration upon probing [19,20].

Data collection
After each prosthesis was removed, the following data was collected: BOP index: Presence or absence was registered after the introduction of 1 mm of the periodontal probe (PCV12PT Hu-Friedy Inc., Chicago, IL, USA) into the gingival sulcus with a gingival "sweep" movement [2]. Data was analyzed after removal of the periodontal probe and time elapsed for 30 seconds; PD: PD measurements were collected on the mesial, mid-buccal, distal and the deepest site on the palatal/lingual, after calibration of the examiner for a probing pressure of 0.25 N [4]; and, Suppuration: Visible presence or absence of suppuration was registered after probing the peri-implant sulcus.

Radiographic analysis
Bone level was measured around the dental implants using the parallel cone technique in order to obtain radiographic images (Kodak Insight film, Carestream, INC., New York, EUA) for analyses. The radiographs were digitalized by and image analysis program (Digimizer® version 3.7.0, Medical Software Brolkstraat, Belgium). The values were obtained by measuring the distance from the implant platform to the first radiographic bone contact on the mesial (MBL); and, on the distal (DBL). The measurements were made at baseline (T0) by only one calibrated examiner, different from the clinical examiner; and, repeated after 7 days (T7). The mean bone loss value obtained from both measurements (T0 and T7) was used as the final measurement of each site. For the final measurement for each implant, a mean bone loss value was established by adding the mesial mean with the distal mean values and dividing the sum by 2.

Group analysis and division
The following criteria were used as the definition for the clinical and radiographic analyses. Peri-implant mucositis was considered when the probing depth was of ≤ 4 mm with presence of BOP around an implant presenting < 2 mm of bone loss. Data was compiled according to each implant and 4 sites (mesial, distal, mid-buccal and palatal/lingual). Peri-implantitis was defined when showing PD of > 4 mm, associated with BOP and/or suppuration, and bone loss ≥ 2 mm [6]. Bone loss was evaluated from the data compiled in 2 sites (mesial and distal) only, due to the inability to evaluate the mid-buccal and lingual/palatal implant sites in an x-ray.
In the prevalence analyses, patients were divided into 3 groups: 1) Healthy; 2) presenting mucositis (at least 1 implant with mucositis); and, 3) presenting peri-implantitis (at least 1 implant with peri-implantitis). While analyzing the results when all the implants were taken into consideration, they were divided into 4 groups; implants without bleeding and with less than 2 mm of bone loss; implants without bleeding and with ≥ 2 mm of bone loss; implants with mucositis; and, implants with peri-implantitis. The division of the healthy implants (without bleeding) into 2 groups aimed to optimize the evaluation of the subjects presenting peri-implant bone loss of ≥ 2 mm, even in the absence of bleeding, which may suggest a history of peri-implantitis [7].

Statistical analyses
All data were compiled and compared between groups. The extraexaminer reproducibility of the MBL and DBL measurements was tested with the intra-class correction coefficient (ICC).
Binary logistic regression analysis was applied for the comparison amongst the groups of the presence of mucositis and peri-implantitis. The assumed confidence interval was of 95%. The Microsoft Excel (Microsoft Office XP) and Statistical Package for Social Science (SPSS) programs for Windows (version 13.0) were used for value data tab and data analyses. Statistical significance was considered significant when P was less than 0.05.

Results
The sample size was composed of 200 patients that summed a total amount of 760 dental implants. Regarding the time the implant supported prostheses were in function, 162 patients (611 implants) had the prostheses for up to 5 years, and 38 patients (149 implants) for more than 5 years. The mean time interval with the prostheses in function was of 4.02 years (standard deviation of 1.67 years). The patient age ranged from 21 to 86 years, with an average of 50.6 years (standard deviation of 11.22). Gender was distributed as 64% females. Sample details are presented in Table 1.  From a total of 139 (69%) patients presenting all implants healthy, 46 (23%) patients presented at least 1 implant with peri-implant mucositis and 15 (8%) patients with at least 1 implant with periimplantitis. Table 2 shows the distribution of patients according to sex and the prevalence category of the peri-implant diseases. 2) Patients with peri-implant mucositis;

Discussion
Studies show a considerable variation in the prevalence of periimplant diseases. However, Pjetursson et al. [21] has presented similar results to the present study. They conducted a systematic review which indicated an incidence of 8.6% for peri-implantitis for dental implants in function for more than 5 years. Another similar analysis was shown by Berglundh et al. [22], Ferreira et al. [23] and Rinke et al. [24], when the prevalence of peri-implantitis was of 6.4%, 8,9% and 11,2%, respectively.
The prevalence of peri-implantitis in the present study differ from the ones presented by the systematic review conducted by Zitzmann and Berglundh [1], where 80% of the subjects showed peri-implant mucositis and 28% -56% presented peri-implantitis. Our results also differ from those presented by Koldsland et al. [6] and Mir-Mari et al. [7]. It can be assumed that this higher percentage could be attributed to the time that the implants were in function, which in this review was a minimum of 5 years. Therefore, even after separating the data of the 38 patients with dental implants in function for more than 5 years, the results still show great discrepancy. Karoussis et al. [25] and Rinke et al. [24] showed that studies evaluating dental implants in function for less than 5 to 10 years may not reproduce the differences in the susceptibility to bone loss due to the fact that peri-implant diseases can take years to develop [26].
Variations in the factors and methods of analyses may contribute to the discrepant results shown in the literature. As already described [1], the diverse methods of analysis (participants/dental implants) was a determinant factor for the exclusion of the majority of the 683 studies reviewed. Other exclusion factors of this review are the clinical and radiographic criteria used for the identification of peri-implant diseases, which make it impractical to compare results from different studies. In regards to this criteria, 2 problems are evident; the absence of fundamental criterions, and the lack of standardization. An example of this lack of criterion was that in one study there was absence of clinical data, as: BOP, which is fundamental for diagnosis of the presence of a peri-implant disease.
Dental implant loss may be due to multiple episodes of peri-implant infections [27] and; therefore, in some instances absence of clinical signs may mask the previous disease. Based in this premise, it may be suggested to add the data from the group presenting implants with bone loss of ≥ 2 mm and without BOP of the present study, to the date from the group presenting peri-implantitis. This would indicate a result similar to the one presented by Ellegaard et al. [28] and Karoussis et al. [25].
The greatest discrepancies of the results were found in the prevalence of peri-implant mucositis. The prevalence of the disease in the present study was significantly lower than the literature reviewed. A possible factor for this discrepancy could be the force used to perform the BOP exam. The standardization of the probing pressure was a determinant factor for the correct diagnosis of the peri-implant diseases and this factor should be considered while validating the comparison amongst results. Some studies show that the peri-implant mucosa could be more sensitive to probing, which would account for a higher percentage of BOP in these tissues when compared to teeth [29][30]. In the present study, the selection and calibration of the examiners demonstrates the importance of applying only the necessary force for measuring the clinical inflammation accurately. From a total of 14 possible trained examiners, only 2 presented a tolerant limit of applied force variation. Twelve examiners demonstrated force limitations of 50 N, even after calibration; therefore, they were not used in this study. Radiological studies show that the tip of the periodontal probe was in close proximity to the peri-implant marginal bone when the probing forces were of 0.5N or more [31]. Ericsson and Lindhe [32] also showed, in an experimental study, that in the healthy peri-implant mucosa, a probing force of 0.5 N resulted in the tip of the probe passing through the connective tissue and being in close proximity to the marginal bone. It is possible that the discrepancy of the results, regarding specifically peri-implant mucositis, could be due to this factor. Some reviewed studies did not mention the probing force applied or the calibration phase as part of the methodology. The authors of the present study suggest the use of electronic periodontal probes to standardize clinical measurements.
The total number of existing cases in a determined population indicates the prevalence of a disease. Therefore, the prevalence of a disease should be determined by the number of individuals and not the number of individual dental implants [1]. Finally, there is a need for describing the extension of the diseases; that is, in regards to the amount and the severity (quantity of bone loss) of dental implants affected in each individual. The ability of obtaining data in a more