Abstract
Peri-implant mucositis is a common inflammatory lesion of the soft tissues surrounding endosseous implants, with no loss of the supporting bone. Its prevention or early diagnosis are vital for dental implant success.
The aim of this review was to investigate knowledge strengths and gaps in clinicians’ perceptions of peri-implant mucositis prevalence and evidence for successful treatment.
A literature search for articles published until 2020, reporting on the prevalence of peri-implant mucositis and its treatment was performed in standard online databases. The inclusion criteria were as follows: studies in English; studies with an available abstract; studies on humans with at least 1 dental implant; and studies reporting on the prevalence and/or treatment of peri-implant mucositis. Sixty-five studies fulfilled the inclusion criteria. The included papers were analyzed to identify data on the prevalence and treatment of peri-implant mucositis. The prevalence statistics for peri-implant mucositis had wide ranges in both the patient-based (PB) analysis and the implant-based (IB) analysis; the possible reasons for these wide ranges are discussed. Treatment methods for peri-implant mucositis were analyzed individually and compared to the management of gingivitis.
It was determined that the currently available information on the prevalence rates and the standardized therapeutic protocols for peri-implant mucositis are insufficient. Since the mean gingivitis and peri-implant mucositis prevalence rates in the PB analysis were similar, it is possible that peri-implant mucositis is underestimated due to variables related to implant rehabilitation itself.
Keywords: inflammation, dental implant, literature review, oral mucositis, peri-implant healing
Introduction
Dental implants are widely used for oral rehabilitation. They are biocompatible prosthetic devices implanted in living bone and, for this reason, the peri-implant tissue conditions can change over time.1, 2 Healthy peri-implant tissues are characterized by the absence of erythema, bleeding on probing (BoP), swelling, and suppuration.3
Once osteointegration has been achieved, allowing for the healing time after implant insertion, implant complications can occur due to mechanical problems, inflammation and/or the loss of the surrounding tissues (the oral mucosa and the supporting bone). These could lead to relevant discomfort for the patient as well as implant failure over time.4 After osteointegration has occurred, implants may become contaminated and peri-implant tissues could become inflamed, causing peri-implant mucositis and/or peri-implantitis.3
In an animal study on beagle dogs, Berglundh et al. compared the anatomy and histology of peri-implant and periodontal tissues in block biopsies.5 A histological examination showed that both presented well-keratinized areas (the oral epithelium and the outward portion of the peri-implant mucosa), but periodontal tissues presented only a few cells of thick epithelium in contact with the implant abutment. Also, peri-implant tissue fibers displayed a parallel course originating from the crestal bone, while periodontal tissue fibers were perpendicular to the dental root, going from the root cementum to the alveolar bone.5
Likewise, blood supply differed from an anatomical point of view – the peri-implant bone vasculature consisted only in the periosteum source, while gingival supply was guaranteed by a double source composed of supraperiosteal and periodontal ligament vessels.6
Being aware of histological differences between peri-implant tissues and the periodontium is fundamental to better understand the peri-implant tissue biology. Clinicians, implant-rehabilitated patients and the dental industry have mainly based their maintenance approaches on the techniques and tools derived from the pre-implant era.
Peri-implant mucositis is an inflammatory lesion of the soft tissues surrounding an endosseous implant, with no loss of the supporting bone or the continuing marginal bone.7 Conversely, peri-implantitis is described as a pathological condition occurring in tissues around dental implants that is characterized by inflammation in the peri-implant connective tissue and a progressive loss of the supporting bone.8
The etiology of peri-implant mucositis has been described as the accumulation of bacterial biofilm around the implant, which may cause signs and symptoms of inflammation, such as local swelling, redness, pain, and BoP.7 The diagnosis of peri-implant mucositis vs. peri-implantitis is made by the evidence of pathological bone loss.9 While peri-implant mucositis exhibits signs of inflammation with no bone loss besides the remodeling process of the alveolar bone during the first year after implantation, peri-implantitis shows signs of inflammation associated with a further loss of the crestal bone.3, 7 In recent years, there has been a general consensus that following the first year of implant functioning, bone loss around dental implants ≥2 mm represents peri-implantitis.10
Data indicates that patients diagnosed with peri-implant mucositis may develop peri-implantitis, especially in the absence of regular maintenance care, but the processes and reasons for this pathological progress remain unknown.11 Factors associated with peri-implant mucositis include biofilm accumulation, smoking and radiation therapy.7 Regular supportive peri-implant care with biofilm removal is an important preventive strategy against the conversion of a healthy tissue to peri-implant mucositis, and also against the progression of peri-implant mucositis into peri-implantitis.7, 11
There is evidence that peri-implant mucositis can be successfully treated. The resolution of the clinical signs of inflammation may take more than 3 weeks following the restoration of plaque/biofilm control.11 The management of peri-implant inflammation should be addressed in terms of infection control, decontamination of the implant surface and regeneration of the alveolar bone when needed.12
The early diagnosis and prevention of peri-implant infections are essential for the long-term dental implant success. In order to perform a thorough evaluation of the peri-implant conditions, peri-implant probing and relative radiographs are always required.12, 13
The purpose of this review was to highlight possible clinicians’ perception problems related to peri-implant mucositis, to investigate the prevalence of peri-implant mucositis reported in the literature and to analyze the evidence-based data regarding its treatment.
Material and methods
Focus question
The focus question for the literature search was: “What is the clinician’s perception regarding the prevalence levels and treatment strategy efficacy/evidence for peri-implant mucositis?”
It was structured according to the PICO format14:
– Population: patients rehabilitated with dental implants;
– Intervention: implant prosthesis, peri-implant tissue, and peri-implant mucositis prevalence and treatment;
– Comparison: diagnostic criteria and peri-implant mucositis treatment;
– Outcome: finding consistency between prevalence and perception, and differences between various kinds of treatment.
Search strategy
The PubMed/MEDLINE, Embase, Scopus, Web of Science, and Cochrane databases were searched to identify published articles reflecting the inclusion criteria: studies in English; studies with an available abstract; studies involving humans with at least 1 dental implant; and studies reporting data on the prevalence and/or treatment of peri-implant mucositis. The search strategy was divided into 2 parts: a pre-search to avoid discrepancies between findings due to the device used (a personal computer or a mobile device); and a focus question search.
The pre-search was used to determine the device and keywords that provided the greatest number of results in order to establish the focus question search. The pre-search concerned peri-implant mucositis studies published up to 2020. The terms used for the identification of keywords were: ‘peri implant’ OR ‘peri-implant’ OR ‘peri-implant mucositis’ AND ‘mucositis’.
The focus question search was carried out on a personal computer to analyze the abovementioned databases, using the 2 keywords that yielded the greatest number of results in the pre-search. The focus question search concerned peri-implant mucositis studies published up to 2020. The terms used for the identification of keywords were: ‘peri implant mucositis’ OR ‘peri-implant mucositis’ AND ‘prevalence’ OR ‘treatment’.
The focus question search yielded 99 articles for “peri implant mucositis prevalence”, 99 for “peri-implant mucositis prevalence”, 300 for “peri implant mucositis treatment”, and 271 for “peri-implant mucositis treatment”.
Screening and selection
The inclusion criteria were as follows: studies in English; studies with an available abstract; studies involving humans with at least 1 dental implant; and studies reporting on the prevalence and/or treatment of peri-implant mucositis.
The exclusion criteria were as follows: studies in a language other than English; studies without an available abstract; non-clinical studies; studies without dental implants; and studies reporting on neither the prevalence nor the treatment of peri-implant mucositis.
Once the studies were selected according to the abovementioned initial screening, only those fitting the following categories were included: randomized clinical trials (RCTs); controlled clinical trials (CCTs); cohort studies; cross-sectional studies; and case–control studies.
The studies were first screened by titles and abstracts, and examined by 2 reviewers. The full text of the selected articles was retrieved and the study results were analyzed. Review articles and systematic reviews were also studied in order to find other articles that did not emerge during database inquiries.
Full-text studies admitted for final analysis were divided into 2 groups: the prevalence group; and the treatment group.
Results
Sixty-five studies fulfilled all the inclusion criteria: 25 RCTs; 3 CCTs; 15 cohort studies; 20 cross-sectional studies; and 2 case–control studies. All these studies were divided into 2 main groups according to the ‘prevalence’ (n = 34) or ‘treatment’ (n = 31) Medical Subject Headings (MeSH). The results according to the type of study are shown in Table 1 for the prevalence group and in Table 2 for the treatment group.
In the prevalence group, cohort and cross-sectional studies constituted the majority of the research devoted to peri-implant mucositis (Table 1). In cohort studies, the peri-implant mucositis prevalence rates ranged between 7.14% and 68.00% in the patient-based (PB) analysis (referring to the number of patients included in the analysis), and between 5.06% and 38.00% in the implant-based (IB) analysis (referring to the number of implants included in the analysis). In cross-sectional studies, the peri-implant mucositis prevalence ranges varied from 20.80% to 80.90% in the PB analysis, and from 21.00% to 90.00% in the IB analysis (Table 3).
In the treatment group, there were RCTs, CCTs, cohort studies, and 1 case–control study (Table 2). The search found 1 RCT on the use of sodium hypochlorite gel, 1 RCT about the modification of the prosthesis, 1 RCT on the use of a drying agent associated with manual debridement, 2 RCTs in which chlorhexidine gel was used, 1 RCT in which a mouth rinse with 0.03% chlorhexidine and 0.05% cetylpyridinium was assessed, 1 RCT that investigated 0.12% chlorhexidine gluconate, 3 RCTs in which toothpastes containing triclosan were assessed, 1 RCT in which chitosan brushes were used, 5 RCTs about probiotics (in one of the studies, photodynamic therapy was added to probiotic administration), 2 RCTs about photodynamic therapy, 3 RCTs about air polishing, 1 RCT in which an enamel matrix derivative was used, 1 RCT on the use of ozone and/or hydrogen peroxide, and 2 RCTs in which systemic antibiotics supported mechanical debridement. The 2 cohort studies were about mechanical debridement and biofilm control (Table 4).
The selected studies proposed various kinds of treatment, including sodium hypochlorite gel, a desiccant agent, chlorhexidine, triclosan, chitosan brushes, probiotics, diode laser therapy, photodynamic therapy, air polishing, and antibiotics. Most of these consisted of mechanical debridement combined with an additional therapy, such as sodium hypochlorite gel, a desiccant agent, chlorhexidine, probiotics, photodynamic therapy, an enamel matrix derivative, and systemic azithromycin (Table 5).
Discussion
The prevalence data found in this literature review revealed a wide gap in percentage ranges. This could be due to the relevant heterogeneity of the prevalence reported among the 13 cohort studies and 20 cross-sectional studies. Other aspects to consider in order to explain this gap are the sample size and the population observed. Some articles addressed a population composed of smokers or subjects affected by diabetes mellitus; both smoking and diabetes mellitus are well-known periodontal risk factors.
Comparing the results of this review regarding the prevalence of peri-implant mucositis to the prevalence of gingivitis provided by the U.S. National Center for Health Statistics (38.70% PB), a tight overlap can be observed.9, 15
According to the available data, the average prevalence values for gingivitis and peri-implant mucositis look very similar. This observation is in contrast with the results of a recent study investigating clinical and biological responses in experimental gingivitis and peri-implant mucositis in humans.16 Although less biofilm accumulation was observed at the implant sites, the peri-implant mucosa yielded a higher proportion of BoP sites as compared to the gingiva.16 This result probably indicates that less visible plaque accumulation is needed for peri-implant mucositis to develop and that the lack of keratinized gingiva, which is a frequent condition around implants, leading to a weaker seal, can contribute to biofilm migration. This would make the onset and progression of peri-implant mucositis easier and faster than in the case of gingivitis. A possible explanation of this discrepancy is that signs of peri-implant mucositis are generally rarely identified because of the great morphological variability of the overhanging prosthesis.
With regard to prosthodontics, it must be emphasized that it definitely plays a crucial role in mucosal homeostasis. Design, structural connections and constituent materials are all factors concretely correlated to plaque accumulation and the soft tissue response. This heterogeneity may help explain the wide gap in peri-implant mucositis percentage ranges found in this review.
During the present investigation, a general deficiency of the available data on this topic emerged, suggesting more focused research is needed in the future, with a general recommendation for more detailed information in the upcoming studies about peri-implant mucositis.
Another relevant aspect concerns the varying clinical indicators used by different studies. Plaque index (PI), BoP, probing pocket depth (PPD), and marginal recession are not always accompanied by radiological examinations to exclude the presence of peri-implantitis. Therefore, it is advisable to collect all the biometric parameters of signs of inflammation, such as redness, swelling, bleeding, and suppuration, and support them with periodontal indices (BoP and PPD) and radiographic examinations.17
These limitations are stressed and partially addressed by the 2017 classification of periodontal and peri-implant diseases and conditions.18 It is literally cited that “a local dot of bleeding resulting from probing may be the result of a traumatic probing that should not be considered, in the absence of other inflammatory changes, a definitive criterion to characterize a peri-implant soft tissue lesion”.8 For a correct examination, it is consequently crucial to perform circumferential peri-implant probing, using the walking probe method, and to collect all clinical and radiographic parameters to evaluate them as a whole before formulating a diagnosis.
Therefore, considering that attaining a peri-implant mucositis diagnosis seems more complex than a gingivitis diagnosis, the above reported similar prevalence data leads one to presume that the peri-implant mucositis prevalence rates might be underestimated, resulting in a lower clinical perception of this pathology.
Peri-implant mucositis treatment protocols should focus on infection control and the decontamination of the implant surface. Bacterial plaque and calculus must be professionally removed, and the patient must be instructed and motivated to perform proper oral hygiene procedures at home. While gingivitis treatment could achieve restitutio ad integrum through professional hygiene care, mechanical debridement and comprehensive home care, peri-implant mucositis treatment appears more complex, requiring several treatment modalities and devices. Many treatment procedures are performed in association with mechanical debridement, using ultrasonic devices with dedicated polyetheretherketone-coated tips and implant-friendly instruments, such as titanium-coated, carbon-fiber, teflon, and plastic curettes. Also, air-abrasive devices or lasers can be used in conjunction with local antibiotics or antiseptics.11, 19
In the treatment of gingivitis, scaling and periodontal debridement are able to remove bacterial plaque and calculus from the tooth surfaces, allowing proper healing. None of the proposed therapies for peri-implant mucositis presented in this review led to a complete or strongly predictable resolution, but mechanical debridement accompanied by an adjunctive therapy, such as probiotics, chlorhexidine or photodynamic therapy, proved to provide additional improvement over mechanical debridement alone.20, 21 Galofré et al. compared the effect of the oral probiotic Lactobacillus reuteri as an adjuvant to non-surgical mechanical therapy.20 In their triple-blind RCT, oral probiotics and mechanical therapy together produced additional improvement over treatment with mechanical therapy alone.20 Also, Javed et al. investigated the outcome of mechanical curettage with or without the adjunct of antimicrobial photodynamic therapy.21 Forty-four patients were involved in this RCT study, and after 12 weeks of follow-up, mechanical debridement with photodynamic therapy was determined to be more effective in the treatment of peri-implant mucositis as compared with mechanical debridement alone.21
Another promising proposed treatment modality is the use of glycine powder air-polishing devices, which were demonstrated to be as effective as mechanical debridement in a study by Schwarz et al.22 The same study group, after an electronic and manual search, selected 7 studies which showed that other therapies added to professionally administered plaque removal were quite promising.23
A proper prosthetic design that allows good oral hygiene and low plaque accumulation is certainly a key factor in the prevention of peri-implant mucositis. De Tapia et al. reported that when peri-implant tissue inflammation occurs, the prosthetic design should be assessed and modified if necessary to correct the design defects which may be impeding proper hygiene as well as to diminish biomechanical stress factors if involved.24 A recent RCT compared peri-implant mucositis treatment through chitosan brushes on oscillating handpieces and titanium curettes; a chitosan brush seems to be a safe and efficient device for the debridement of dental implants.25 Likewise, the regular use of a toothpaste containing triclosan appears to be able to reduce the clinical signs of inflammation in the mucosa adjacent to dental implants.26 Finally, it has been shown that there is a minimal difference between the non-surgical treatment of peri-implant mucositis with and without systemic antibiotics.27
Conclusions
Currently, the available information on the prevalence rates and the standardized therapeutic protocols for peri-implant mucositis are insufficient. Also, it can be presumed that the prevalence rates may be underestimated due to difficulty with making a clinical diagnosis, leading to a lower level of perception among practitioners.
Peri-implant mucositis is a frequently encountered condition. The absence of effective standardized therapeutic procedures that would result in an empirical choice of therapeutic modalities may lead to diminished effectiveness and unsatisfactory treatment outcomes.
It has to be emphasized that implant placement and prosthetic restorations must allow for proper cleaning and plaque control to prevent peri-implant mucositis.
Further research is needed to improve clinicians’ skills in the detection of peri-implant mucositis and to determine effective standardized therapies.