The aim of this review was to determine the most common peri-implant mucositis and peri-implantitis case definitions used worldwide in the implant dentistry literature. A systematic assessment of peri-implant disease classification was conducted using all publications in MEDLINE, EMBASE, SCOPUS, and Google Scholar between 1994 and November 2017. Screening of eligible studies and data extraction were conducted in duplicate and independently by 2 reviewers. The search protocol identified 3049 unique articles, of which 2784 were excluded based on title and abstract. In total, 265 full texts were screened, 106 of which met the eligibility criteria. Of these, 41 defined peri-implant mucositis. Eight (19.6%) used bleeding on probing (BOP) only; 8 (19.6.7%) used a combination of probing depth (PD), BOP, and radiograph; and 5 (12.3%) used PD and BOP. Cases with crestal bone loss of ≤2 mm in the first year and ≤0.2 mm in each subsequent year were considered as peri-implant mucositis. Ninety-three articles defined peri-implantitis; 28 (30.1%) used a combination of PD with suppuration, BOP, and radiograph, followed by 25 (26.9%) using a combination of PD, BOP, and radiograph. The main criteria in most of the studies were considered to be BOP, PD, and radiograph. Cases of crestal bone loss of ≥2 mm and PD ≥3 mm are considered peri-implantitis. Different peri-implant disease case definitions may affect disease prevalence and treatment strategies. We need to standardize case definitions to avoid discrepancies in case diagnosis and prognosis.
Introduction
Peri-implant disease is classified into 2 types: peri-implant mucositis (equivalent to gingivitis) and peri-implantitis (similar to periodontitis1,2). The definitions of both diseases were first proposed at the 1st European Workshop on Periodontology.3 Peri-implantitis is considered an inflammatory process associated with loss of supporting bone around a functioning implant. Peri-implant mucositis is a reversible inflammatory process limited to soft tissues only. It can lead to loss of the implant if not diagnosed correctly or not managed properly.4 Based on published studies, the prevalence of peri-implant disease varies significantly among populations.3,5 It could be due to differences in data collection methods or case definitions of these diseases.
Mucositis is characterized by typical signs of soft-tissue inflammation such as reddening, swelling, and bleeding on periodontal probing.6,7 However, these signs are not clearly visible in many cases.8 Moreover, sufficient evidence of predictive and diagnostic value in implant dentistry is still lacking, limited to bleeding on probing (BOP) and probing around the implants. However, it is a common indicator of peri-implant disease.9 In peri-implantitis, the most common hard- and soft-tissue signs are bone resorption, purulence, decreased implant osseointegration, and increased pocket formation.1,2,8 However, some of these signs (eg, BOP, bone loss, pocket depth) could be due to other reasons, such as deep or buccal insertion of the implant,10 type and implant diameter, abutment connection, materials, and type of prosthetic suprastructure.4
The diagnostic criteria and treatments for peri-implant diseases are not currently standardized.3,8,11 This situation is similar, to some extent, to the case definition of periodontitis.7,12–15 This can affect the accuracy of any comparison made between any 2 studies. The absence of standardized diagnostic methods and universal classifications for peri-implantitis might lead to controversial diagnoses as well as difficulty in determining actual prevalence, pathology, and prognosis of the disease,11 which in turn makes it hard for clinicians to agree on whether an implant failed or can be treated.11 Thus, little is known about the common case definition of peri-implant disease in the epidemiological literature. Thus, the purpose of this systematic review was to assess the various definitions associated with peri-implant disease.
Methods
Search strategies
We conducted a systematic assessment using all publications in MEDLINE, EMBASE, SCOPUS, and Google Scholar between 1994 and November 2017. The terms we used to identify epidemiological articles reporting on periodontology were the following: “peri-implantitis” (MeSH term and keyword) and “peri-implant (periimplant) mucositis” (keyword). These terms were combined with one of the following terms: “prevalence” (MeSH term), “epidemiologic studies” (MeSH term), “epidemiology” (MeSH term), and “epidemiologic research design” (MeSH term). Hand-searched journals and bibliographies of the selected articles and reviews were checked for additional articles.
Eligibility criteria
The following articles were included: (1) original article (ie, letters to the editor, authors' responses, and review studies were excluded); (2) only humans (ie, animal and in vitro studies were excluded); and (3) observational, population screening, or prevalence studies (ie, case report, case series, and randomized clinical trials were excluded). Articles included definitions of “peri-implantitis” and “peri-implant mucositis,” and measurements were written in English only. We excluded articles that did not define what they meant by “peri-implantitis” and “peri-implant mucositis.” Furthermore, we excluded any methodological and interventional studies as well as any studies for which the full text was not available/accessible through a license at our institutes.
Screening process
Five reviewers (2 in each article; Z.S.N. with N.A., E.A., Z.B., or R.J.) independently screened and selected articles for eligibility based on title and abstract. Disagreements were resolved via discussion. After consensus, full-text articles were retrieved, and 5 reviewers (2 in each article; Z.S.N. with N.A., E.A., Z.B., or R.J.) screened the full-text articles and extracted data. In case of doubt of any article, a new third reviewer in the same group was involved.
Data extraction
Items extracted from articles included study design (eg, cohort, case-control), type of disease, case definition, and method of diagnosis. To ensure consistent data extraction, a standardized task sheet was formed. It was tested and modified several times, and all reviewers were trained on how to use the sheet.
Descriptive analysis
Results were summarized using descriptive statistics of frequencies and percentages. We did not perform a quantitative analysis, as this was beyond the scope of our review. In addition, meta-analysis for these definitions was inapplicable because of the heterogeneity and limited number of studies in several groups.
Patient involvement
No patients were involved in any part of this study.
Results
The search strategy found 3049 unique articles, of which 2784 were excluded after reviewing each article title and abstract. In total, 265 full texts were screened, 106 of which met the eligibility criteria and were included in this review (Figure).
Peri-implant mucositis case definitions
Overall, 41 articles defined peri-implant mucositis. Eight (19.6%) used BOP only; 8 (19.6%) used a combination of probing depth (PD), BOP, and radiograph; and 5 (12.3%) used PD and BOP (Table 1). Several methods that are rarely used were included in the studies, such as the combination of PD with BOP and gingival index or PD with BOP, radiograph, and swelling (1 study each). However, BOP was considered the main criterion in most of them. The combination of several criteria was used more commonly than a single criterion. Therefore, it is important to consider cases of peri-implant mucositis that present with a crestal bone loss of ≤2 mm in the first year and ≤0.2 mm in each subsequent year and PD ≤5 mm.
Peri-implantitis case definitions
Overall, 93 articles defined peri-implantitis. Twenty-eight (30.1%) used a combination of PD with suppuration, BOP, and radiograph, followed by 25 (26.9%) that used a combination of PD, BOP, and radiograph (Table 2). Several methods were also included that have been used rarely. However, BOP, PD, and radiograph were considered the main criteria in most of them. The combination of several criteria was used more commonly than a single criterion. It is important to consider cases of peri-implantitis that present with a crestal bone loss of ≥2 mm and PD ≥3 mm.
Discussion
Case definition is a key factor in the medical field. It helps in diagnosis, treatment, and prognosis of a disease. It is a concern in dental practice. However, only a few articles have been published on that topic on implant dentistry.2,3,8 In this article, we have demonstrated that there are different definitions for peri-implant diseases in the dental implant literature, which can affect estimates of prevalence, incidence, and treatment strategies. It is also clear that variation in the diagnosis criteria for a combination of PD, suppuration, and radiograph at a given site leads to different evidence of peri-implant disease at that site. Selection of these criteria is very critical and has been investigated in several articles.2,3,8 Any changes in these criteria can lead to major changes in the disease status, which may overestimate or underestimate the actual disease prevalence/incidence.
The number of criteria used is another factor. Each criterion has its advantages, including the following: PD assessments might be indicative of current disease status,16 radiographs measure lifetime bone loss accumulated from past disease,7,15,17 and BOP indicates the presence of active signs of inflammation.14,16 Mobility was one of the least common signs used, which indicates the final stage of peri-implant disease and complete loss of the direct bone-to-implant contact.9,18–20 However, after review of the current literature, some studies used only 1 criterion, and other studies combined multiple.
It is always a challenge to detect inflammation around implants. It depends on several factors, such as the amount of force behind the periodontal probe, soft-tissue vertical thickness, implant position, oral hygiene, and implant-abutment connection.21–25 Marginal bone loss in radiographs is another challenging factor because of the difficulty in distinguishing between (1) pathologic bone loss due to infection and (2) physiologic bone remodeling that occurs early after implant is functioning. (The latter might be related to the implant biological width and biomechanical response of the bone to occlusal loading.11,26)
The ability to take a standardized radiograph for comparisons between before and after implantation is another concern in peri-implantitis diagnosis.20 Radiographs should be exposed parallel to the implant fixture with a clear proximal bone crest.20 Periapical radiographs are recommended.1,15,17 Panoramic radiographs could be useful for peri-implantitis diagnosis in molar sites.17 However, 3-dimensional radiographs are considered superior, in which proximal and buccolingual/palatal bone walls can be evaluated.1,15,17
Many studies have been conducted using different diagnostic classifications regarding peri-implant diseases. The most common classifications used are Lindhe and Meyle. They used probing at 4 surfaces, BOP, suppuration, and mobility. The researchers also advised clinicians to take a radiograph.20 Lang and Berghlundh recorded PD, BOP, and suppuration. In addition, they encouraged clinicians to take a radiograph if the PD was ≥5mm.27 Sanz et al used radiographs and considered 2 mm of bone loss from the expected marginal bone level as peri-implantitis in the absence of previous radiographic records with evidence of peri-implant inflammation.28
The American Academy of Periodontology (AAP) used probing, BOP, suppuration, mobility, and radiographs to diagnose peri-implant disease.19 They even contemplated using bacterial culturing, inflammatory markers, and genetics in the diagnosis.19 Some investigators even took a step forward and classified peri-implantitis based on the severity as early, moderate, and advanced using different PD levels and percentage of bone loss around implant length29 (or based on etiology30). The recent 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions, co-presented by the AAP and the European Federation of Periodontology,31,32 established new parameters based on certain articles. However, it is too early to evaluate the actual effect of this consensus and its global acceptance.
Although bone loss is key in defining peri-implantitis, it is difficult to consider it as the only diagnostic feature.11 Bone resorption can be caused by several physiologic or induced factors (eg, deep implant insertion or insufficient implant-implant/tooth distance).10,33 Moreover, not every PD >5 mm around implants can be considered clear signs of peri-implantitis. Soft-tissue conditioning and contact point height can be created in any esthetic zone. This can help in the creation of the visual illusion of a long interdental papilla as well as increase the distance from the implant shoulder to the mucosal margin by up to 5 mm.34
Conclusion
Several clinical examination parameters of peri-implant diseases were used in this research, including measurement of BOP for peri-implant mucositis as well as PD, BOP, suppuration, and alveolar bone loss for peri-implantitis. There is clearly a lack of standardization, which leads to difficulty in drawing valid conclusions. Clear definitions of the disease and associated parameters should be established worldwide to ensure accurate results in future studies.
Abbreviations
Acknowledgments
The authors acknowledge Dr Randa Abuahmad, Lina Alsharif, Dr Hanan Alrowithi, Dr Duaa Alsini, and Dr Hetaf A. Salih for their assistance with the article search.
Note
The authors have stated explicitly that there are no conflicts of interest in connection with this article.
