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19 November 2024

An Umbrella Review of the Association Between Periodontal Disease and Diabetes Mellitus

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1
Faculty of Dentistry, Universidad San Martín de Porres, Chiclayo 14012, Peru
2
Faculty of Human Medicine, Universidad San Martín de Porres, Chiclayo 14012, Peru
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Faculty of Stomatology, Universidad Nacional de Trujillo, Trujillo 13001, Peru
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Faculty of Health Science, Stomatology School, Universidad César Vallejo, Piura 20001, Peru
Healthcare2024, 12(22), 2311;https://doi.org/10.3390/healthcare12222311
This article belongs to the Section Community Care
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Abstract

Aim: To determine the clinical association between periodontal disease and diabetes mellitus through an umbrella review. Materials and Methods: A search for publications up to August 2023 was conducted using the following electronic databases: PubMed, Cochrane Database, Scopus, SciELO, Google Scholar, and OpenGrey. We included systematic reviews (SRs) with or without meta-analysis evaluating primary studies that investigated the association between periodontal disease and diabetes mellitus, and there were no time or language restrictions. Literature or narrative reviews, rapid reviews, intervention studies, observational studies, preclinical and basic research, abstracts, comments, case reports, protocols, personal opinions, letters, and posters were excluded. The AMSTAR-2 tool was used to determine the methodological quality of the included studies. Results: The preliminary search yielded a total of 577 articles, of which only 17 remained after discarding those that did not meet the selection criteria. Following their analysis, an association between periodontal disease and diabetes mellitus (type 1 and type 2 diabetes mellitus and gestational diabetes mellitus) was found. Conclusions: The findings and conclusions of this umbrella review indicate with high confidence that periodontal disease is associated with the onset of type 1 and type 2 diabetes mellitus and gestational diabetes.

1. Introduction

Diabetes mellitus (DM) is a common metabolic disease resulting from a defect in either insulin secretion or insulin action, or a combination of both [1,2]. This chronic disease is one of the most common in the world, and its prevalence is expected to increase by almost 50% in the coming years. It is estimated that by 2045, there will be around 700 million people living with diabetes, which will be one of the five main causes of death [3]. Mortality in people with diabetes occurs due to complications, of which the most important include microvascular changes, neuropathy, retinopathy, nephropathy, delayed healing, and periodontitis [4,5].
Periodontitis is a disease characterized by chronic inflammation of the entire periodontium that can irreparably destroy the tissue surrounding the tooth, leading to gingival bleeding, increased tooth mobility, and tooth loss [6]. It is estimated that approximately between 20 and 60% of the world’s population suffers from periodontal disease [7,8].
DM and periodontal disease (PD) are associated, despite lacking a common pathophysiology [6]. However, glucose alteration in these patients shows a positive association, which is evident in patients with poorly controlled diabetes having an 86% higher risk of developing periodontitis than non-diabetics or those with well-controlled diabetes [4]. Furthermore, PD may be a risk factor for diabetes mellitus, suggesting a possible bidirectional association [3]. The proposed link between the two diseases is based on characteristics of the immune response, neutrophil function, and cytokine biology [9,10].
The need for dentists to understand the associations and short- and long-term con-sequences of these diseases necessitates a deeper comprehension of the scientific basis using the highest quality evidence available for clinical decision-making [11]. The synthesis of knowledge within a single document can support clinical decision-making, thus facilitating the reading and understanding of a particular topic. To date, no comprehensive synthesis or evaluation of all systematic reviews, including those from recent years, has been performed. Therefore, the aim of this overview is to consolidate the available evidence and address the following question: “What is our current understanding of the link between periodontal disease and diabetes mellitus?” In addition, we assess the general confidence in the systematic reviews analyzing this issue.

2. Materials and Methods

2.1. Protocol and Registration

The study was executed in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analysis Protocols (PRISMA-P) [12] and subsequently registered in the Prospective Registry of Systematic Reviews (PROSPERO) [13]. The registry can be accessed by the general public under the number CRD42023464043. Furthermore, PRIO-harms (Preferred Reporting Items for Overview of Systematic Reviews Checklist) provides the basis for reporting in this study [14]. Notably, our methodology is based on Pauletto et al. [15], given its similarity to our approach. Ethical approval was not required for this umbrella review.

2.2. Eligibility Requirements and Noteworthy Results

All included articles were systematic reviews (SRs) that assessed primary research assessing the relationship between PD and DM, regardless of whether meta-analysis was employed and without regard to time or language constraints.
Exclusions included abstracts, remarks, case reports, procedures, personal opinions, letters, posters, fast reviews, intervention studies, observational studies, preclinical and fundamental research, and literature or narrative reviews.

2.3. Information Sources, Search Tactics and Further Searches for Primary Studies

An electronic search across the four databases PubMed, Cochrane Database, Scielo, and Scopus was completed on 20 August 2023. We also searched the gray literature using OpenGrey and Google Scholar. The reference lists of the included studies were also examined. Duplicate articles were removed from the identified articles and exported to Zotero®, a reference management program developed by the Center for History and New Media in Fairfax County, Virginia, USA. Table 1 lists the search approach used for each database.
Table 1. Database search strategy.

2.4. Data Management and Selection Process

The identified articles were inserted into Rayyan® Online Software (Qatar Research Institute of Computing at Hamad Bin Khalifa University (HBKU), Doha, Qatar). The studies were selected in two phases: In phase 1, two reviewers (F.C.O. and E.I.) independently selected the studies by reading the titles and abstracts. Subsequently, phase 2 was carried out, which consisted of reading the full texts, carried out independently by the same two reviewers. A third reviewer (F.C.Z.) was consulted in cases of disagreement.

2.5. Data Collection Process

Data from the study were independently collected in duplicate using a table previously prepared by two reviewers (E.B. and W.T.). Data were cross-checked, and any disagreements were resolved by the third review author (P.H.). Information on the following was extracted from the selected articles: authors, year of publication, study design, design of primary studies included, number of studies included in the qualitative and quantitative analysis, country, type of diabetes, results, main conclusions, and used or execution of Meta-analysis, PRISMA, PROSPERO, and Grading of Recommendations Assessment, Development and Evaluation (GRADE).

2.6. Evaluation of Meta-Bias, Evidence Quality, and Methodological Quality

Two reviewers (O.S. and R.O.) independently assessed the methodological quality of the included SRs in duplicate using the AMSTAR-2 checklist (A MeaSurement Tool to Assess Systematic Reviews), which was calibrated to a Kappa value of 0.85 [16]. Based on 16 questions that have three alternative answers—”yes”, “no”, or “partially yes”—the AM-STAR-2 assesses the methodological quality of the SR. Classification of a study as having high, moderate, low, or critically low confidence was conducted according to Shea et al. [16].

2.7. Measurement Summary

In cases of an SR meta-analysis, we considered the findings of that study along with any results displayed as mean difference, normalized mean difference, relative risk, or odds ratio.

2.8. Results Summary

The primary findings of the included SRs were compiled and categorized into the following categories: number of teeth, clinical attachment level, prevalence, general association, plaque index, gingival index, probing depth, and bleeding on probing.

3. Results

3.1. Examining and Choosing Original Research

After removing duplicates, 519 references remained of the 572 originally yielded from the electronic database search. Phase 1 involved evaluating the titles and abstracts of the selected studies and taking into consideration 12 papers that could be read in full. After adding two more articles from other umbrella reviews and four articles for various reasons, only eighteen SRs remained for quality synthesis. Table 2 provides the rationale behind exclusion for each relevant article [17,18,19,20,21,22,23]. Figure 1 depicts the entire procedure for identification and selection for the research.
Table 2. Reasons for exclusion of studies.
Figure 1. PRISMA diagram showing the process for inclusion and exclusion of studies.

3.2. Review and Characteristics of Included Studies

The included SRs were published in English between 2009 and 2023. They were carried out in Portugal [10], Peru [24], Malaysia [25], China [26,27], Germany [3], Italy [28,29,30], Australia [31], Japan [32], Denmark [33], the Netherlands [34], Spain [35], Brazil [36,37], and the United States [38,39]. More information on the characteristics of these SRs can be found in Table 3.
Table 3. Characteristics of included studies.

3.3. Assessment of Methodological Quality and Quality of Evidence

Based on the analysis, 13 SRs [3,10,24,25,26,30,33,34,35,36,37,38,39] were classified as having high confidence, 1 SR [32] as having low confidence, and 4 SRs [27,28,29,31] as having critically low confidence (Table 4).
Table 4. Assessment of the methodological quality and quality of evidence of the included studies.

3.4. Overlapping

A total of 296 primary studies [40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92] were identified within the SRs. Of these, 17.26% of the primary studies were included in more than one SR. Thirty-five studies were included twice, eight were included three times, and seven were included four times. More information on the overlap and characteristics of the primary studies is available in Table 5.
Table 5. Overlapping of primary studies in systematic reviews.

3.5. Synthesis of Results

The syntheses of the results are presented in Table 3.

3.6. General Association

Eleven of the included SRs [3,10,24,27,28,30,31,33,34,38,39] reported an association between PD and DM, while two SRs [32,36] reported no association. Meta-analysis was conducted in six SRs [3,28,33,34,36,38], where the relative risk ratio was found to range from 1.26 (CI: 1.12 to 1.41) [3] to 1.86 (CI: 1.25 to 2.77) [33] and the odds ratio from 1.69 (CI: 0.68 to 4.21) [36] to 2.59 (CI: 2.12 to 3.15) [34]. Costa et al. [10], León-Ríos et al. [24], Nguyen et al. [31], Graziani et al. [30], Ismail et al. [27] and Borgnakke et al. [39] presented the results descriptively and reported an association between PD and DM, while Tanaka et al. [32] reported no association between PD and DM.

3.7. Plaque Index

Three included SRs [25,26,29] that conducted meta-analysis reported an association between PD and DM, with a mean difference of 0.20 (CI: 0.18 to 0.23) [26] and a standardized mean difference ranging from 054 (CI: 0.20 to 0.87) [25] 0.71 (CI: 0.19 to 1.22) [29].

3.8. Gingival Index

Two included SRs [25,29] that conducted meta-analysis reported an association be-tween PD and DM, with a standardized mean difference ranging from 0.46 (CI: 0.08 to 0.84) [29] to 0.63 (CI: 0.39 to 0.87) [25].

3.9. Clinical Attachment Level

Four included SRs [25,26,28,29] reported an association between PD and DM, while one SR [37] reported an association of PD with type 2 diabetes mellitus (T2DM) but not type 1 diabetes mellitus (T1DM). Meta-analysis was conducted in all cases, finding a mean difference ranging from 0.26 (CI: 0.00 to 0.53) to 1.00 (CI: 0.15 to 1.84) [37] and a standardized mean difference ranging from 0.47 (CI: 0.37 to 0.57) [28] to 0.82 (CI: 0.59 to 1.04) [29].

3.10. Number of Teeth

One included SR [26] that conducted meta-analysis reported an association between PD and DM, with a mean difference of −2.14 (CI: −2.87 to −1.40).

3.11. Prevalence

Three included SRs [26,28,35] reported an association between PD and DM. Me-ta-analysis was conducted in two of these [26,28], where they found the odds ratio ranged from 0.19 (CI: 0.08 to 0.37) [28] to 1.85 (CI: 1.61 to 2.11) [26]. Mauri-Obradors et al. [35] presented the results descriptively and reported an association between PD and DM.

3.12. Probing Depth

Three included SRs [25,26,29] reported an association between PD and DM, while one SR [37] reported that an association of PD with T2DM but not T1DM. All conducted meta-analysis and found a mean difference ranging from 0.11 (CI: −0.03 to 0.25) to 0.46 (CI: 0.01 to 0.91) [37] and a standardized mean difference ranging from 0.36 (CI: 0.16 to 0.55) [29] to 0.67 (CI: 0.23 to 1.11) [25].

3.13. Bleeding on Probing

Three included SRs [25,26,29] reported an association between PD and DM. Two studies conducted meta-analysis, finding a mean difference of 7.90 (CI: 4.24 to 11.56) [26] and a standardized mean difference ranging from 0.32 (CI: 0.07 to 0.58) [25] to 0.65 (CI: 0.08 to 1.23) [29].

4. Discussion

The evaluation and analysis of the association between PD and systemic diseases, such as DM, has been of interest in recent years. Numerous RCTs have investigated this topic and reported supporting evidence for an association between these two diseases.
Some studies have evaluated this association in a general way, while others have evaluated it according to periodontal clinical parameters. As there are now several published SRs analyzing the association between PD and DM, it has become necessary to compile data from these to assess the methodological quality of each study.
Currently, three relevant umbrella reviews have been conducted, and all [11,93,94] reviewed the most current evidence on the nature of the relationship/association between PD and DM; however, studies that analyzed whether periodontal therapy was effective in people with DM were included, so the results and conclusions must be considered with caution.
An exhaustive literature search was conducted in the present study to summarize the available SRs investigating the association between PD and DM (T1DM, T2DM, and GDM), identifying 18 SRs that matched the inclusion criteria and were included in the analysis. SRs represent the highest level of the scientific evidence pyramid, but their results should be evaluated cautiously due to the potential for bias.
The SRs included in this study exhibit certain limitations related to the selected primary studies, such as the inclusion of different of study types, the selection criteria for inclusion of studies, the inclusion of different population groups (children, adolescents, and adults), different diagnostic criteria for periodontal diseases, and the evaluation of different types of diabetes mellitus (T1DM, T2DM and GDM).
On the other hand, more than 50% of the included studies demonstrated a high level of confidence, potentially enhancing the level of evidence for the results and conclusions presented in this study. However, the continued publication of SRs lacking a high level of confidence highlights the need for greater rigor in the development of such studies on this topic.
The AMSTAR-2 instrument, in its most current version, was used to assess the methodological quality of the included SRs. A factor related to the methodological quality that deserves emphasis is the critical domains 2, 4, 7, 9, 13, and 15 of AMSTAR-2. Some SRs failed to explicitly assess their methods, did not use an exhaustive search strategy, did not provide justification for the exclusion of studies, did not use a satisfactory technique to assess the risk of bias, and did not consider the risk of bias of the included studies when interpreting or discussing their results. In addition, they did not report the risk of publication bias. This highlights a need for these elements to be included in the development of future SRs.
Additionally, caution should be taken as some studies were included in the SRs more than once, leading to data being reevaluated multiple times, which could skew perceptions and findings. Although conducting new SRs to overcome methodological limitations, as recommended by Moher [95], would be of interest, in consideration of the high overlap rate, it is more important to carry out well-conducted RCTs with long-term follow-up and from different research groups to expand knowledge on this topic.

4.1. Evidence Summary

The present umbrella review was carried out to advance research on the association between PD and DM, with the aim of minimizing biases and random errors in SRs and meta-analyses on this subject. The findings are summarized and discussed below while considering the limitations of the SRs used in this study.
The SRs included in this study support a general association between PD and DM. This is similar to the report by the Consensus Report of the European Federation of Periodontics [17], which highlights that periodontitis is associated with diabetes mellitus. However, two of the included studies [32,36] reported no association between these two diseases, where one [32] focused only on the Japanese population, concluding there was little evidence on this topic for this population, while the other [36] performed subgroup analysis according to type of primary study, concluding that the association is supported by the cross-sectional studies but not the case–control studies.
In terms of plaque index, gingival index, number of missing teeth, prevalence, and bleeding on probing, the studies indicate that patients with DM have a greater probability of increases in all these clinical parameters, indicating an association between PD and DM.
The studies also indicate that patients with DM have a greater probability of increases in all these clinical parameters when considering the depth of catheterization and the clinical attachment level. However, one study [37] indicated that PD is associated with T2DM but not T1DM.
Furthermore, the following should be noted regarding the included studies: four [10,27,28,29] analyzed T1DM, with only one [10] demonstrating high overall confidence; three [24,36,38] analyzed GDM, with all demonstrating high overall confidence; and ten [3,25,26,30,31,32,33,35,37,39] analyzed DM in general, with eight [3,25,26,30,33,35,37,39] classified as having high general confidence.

4.2. Implications for Clinical Practice

Given the association between PD and DM, accurate anamnesis and correct diagnosis are critical to ensure that patients are presented with the most viable, straightforward, and least invasive treatment options, such as scaling and root planning, or the use of lasers and local antimicrobials.

4.3. Implications for Research

There are a high number of SRs available, but it is evident from our assessment that there is an immediate need for improved reporting quality. For future SRs, we recommend examining the instruments used in guiding their development, including quality evaluation tools. To obtain more reliable results, additional SRs on the relationship between PD and MGD should be conducted with strong methodological rigor. For future primary studies, we also recommend using the latest definitions for the diagnosing periodontal diseases.

5. Conclusions

According to the findings of this umbrella review, there is strong evidence supporting the association between periodontal disease and various forms of diabetes mellitus, including type 1 and type 2, and gestational diabetes. The reviewed studies demonstrate a consistent relationship across different clinical parameters, such as plaque index, gingival index, clinical attachment level, probing depth, and bleeding on probing, with diabetes patients showing a higher likelihood of experiencing worsened periodontal conditions. However, two studies did not find an association, highlighting the need for further research to address potential differences in study populations and methodologies.

Author Contributions

Conceptualization, H.I.A.-V.; methodology, H.I.A.-V. and F.H.C.-O.; software, F.T.C.-Z.; validation, E.D.I.-R., E.G.B.-A. and W.T.-C.; formal analysis, P.M.H.-P.; investigation, F.H.C.-O.; resources, O.A.S.-T.; data curation, R.E.O.-G.; writing—original draft preparation, F.T.C.-Z.; writing—review and editing, W.T.-C. and P.M.H.-P.; visualization, E.G.B.-A.; supervision, H.I.A.-V.; project ad-ministration, E.D.I.-R.; funding acquisition, F.T.C.-Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Data sharing is not applicable. No new data were created or analyzed in this study.

Conflicts of Interest

The authors declare no conflict of interest.

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