Top 100 most-cited papers on diabetes mellitus in Dentistry: a bibliometric study

Abstract This study assessed the features of the 100 most-cited papers on diabetes mellitus (DM) in dentistry using bibliometric measures. A search of the most cited papers on DM using journals included in the category “Dentistry, Oral Surgery and Medicine” in the Web of Science database up to January 2023 was performed. The complete bibliographic records of the selected papers were exported in plain text or Research Information Systems (RIS) file format. The following bibliometric indicators were collected: title, year, authors, number of citations, mean number of citations, institution, country, continent, study design, journal, impact factor, and keywords. Graphical bibliometric networks were created using the VOSviewer software. The number of citations for the 100 most-cited papers in DM research ranged from 111 to 566. Six papers each had more than 400 citations. Most were observational studies (n = 50) from the United States (USA) (n = 23) and were published in the Journal of Periodontology (30%; n=30). Robert Genco was the most cited author and contributed the most to the top 100 articles (3,653 citations; n = 13). The VOSviewer map of co-authorship showed the existence of clusters in research collaboration. The most prolific institutions were the Universities of Buffalo and Michigan (n = 6 each). “Diabetes mellitus” was the most frequent keyword, with 31 occurrences. In conclusion, the most cited studies that investigated the relationship between dentistry and DM were in periodontology. Observational studies, primarily from the USA, have been the most cited thus far.


Introduction
Diabetes mellitus (DM) is a metabolic disease characterized by hyperglycemia, which affected 537 million individuals aged 20-79 years in 2021. 1,2DM results in elevated levels of inflammatory markers and increased susceptibility to infections, 3,4 leading to progressive complications in various organs and tissues.This ultimately reduces quality of life and increases morbidity and mortality among patients. 5,6M exhibits a spectrum of oral manifestations and/or complications, including a high prevalence and severity of dental caries and periapical bone resorption, 7,8 impaired periodontal wound healing, 9,10 and an Declaration of Interests: The authors certify that they have no commercial or associative interest that represents a conflict of interest in connection with the manuscript.elevated risk of developing oral potentially malignant disorders. 11A recent systematic review also showed that DM is associated with increased degeneration and mineralization within pulp tissue. 2 Over the past 35 years, bibliometric analyses have measured the impact, trends, and development in various field of health research through qualiquantitative analyses of the number of citations of papers. 12][15][16] The evaluation of oral alterations and correlation between different materials/therapies and systemic disorders, such as DM, has become an emerging field of interest in oral health research over time.However, to the best of our knowledge, no bibliometric analysis has been undertaken to comprehensively understand the hot topics, leading research centers, and potential future directions of DM research within dentistry.
In this context, a bibliometric analysis of the mostcited articles pertaining to DM in oral health research can help clinicians and researchers identify prominent authors, countries, journals, and institutions with high publishing activity, while also delineating research trends over time.Therefore, this study assessed the features of the 100 most-cited papers on DM in Dentistry through bibliometric measures, aiming to elucidate the impact and dissemination of different study designs on DM across the dental scientific community.

Information sources and search strategy
In January 2023, a bibliometric analysis focused on the 100 most cited papers on DM research in Dentistry was conducted in the Web of Science "All Databases" (WoS-AD) and "Core Collection" (WoS-CC) in the category of 'Dentistry, Oral Surgery, and Medicine'.The following search terms were used: ("diabetes mellitus" OR diabetes OR diabetic OR diabetics OR "diabetic mellitus" OR "diabetics mellitus" OR "type 2 diabetes mellitus" OR "type 1 diabetes mellitus" OR "insulin resistance" OR "insulin sensitivity" OR" high glucose" OR hyperglycemic OR hyperglycaemia OR hyperglycemia OR "glycated hemoglobin" OR "diabetes complications").

Study selection and data collection
Three researchers (A.H.R.P., G.P.N. and K.S.P.) independently conducted the study selection based on eligibility criteria.These authors reviewed the title and abstracts of the identified articles, and if necessary, conducted full-text reading.The resulting list was arranged in descending order of WoS citations.The three researchers also undertook data extraction.During screening of the articles identified, restrictions on language or year of publication were not imposed in any way.Any disagreements on study selection and data extraction were resolved through discussion and consensus.Papers whose main focus was not related to DM or those that did not present at least a dedicated topic were excluded.Likewise, letters to the editor and reports on meeting abstracts were also excluded.In cases where more than one paper had the same number of citations, the more recently published paper received a higher rank.The assessment concluded upon finding the 100 th most-cited paper.Complete bibliographic records of the selected papers were exported in plain text or Research Information Systems (RIS) file format from WoS and imported into the VOSviewer software (version 1.6.7;Leiden University Center for Science and Technology Studies, Leiden, Netherlands) for statistical computation and graphics.
The following information was extracted from each paper: title of the article; year of publication; first and others authors; number of citations; the citation mean per year (ratio of the numbers of citations and the period since the year of publication until December 2022); research center or institution/university; country and continent based on corresponding author's affiliation; study design; journal and Journal Citation Reports Impact Factor (JCR ® IF 2021) in the WoS subject category "Dentistry, Oral Surgery & Medicine" for the year in which the papers had been published; and finally, the keywords.Study designs were classified as follows: literature review, laboratorial studies (in vitro, in vivo, in situ, ex vivo), observational study, randomized controlled trial (RCT), non-randomized clinical study, and systematic review with or without meta-analysis.

Data analysis and visualization
The VOSviewer software was used to generate bibliometric networks.Within these maps, authors' names were pooled into the VOSviewer as a unit of analysis and were linked to each other based on the number of co-authored papers.A collaboration network was constructed for co-authors who had contributed to three or more articles. 17In the networks, clusters consisted of groups of nodes that were closely related, with each cluster assigned a specific color.The node size indicated the total number of articles published by each co-author.Larger circles indicated more relevant terms, and strongly related terms were positioned closer to each other.Furthermore, lines between terms indicated existing relationships, with thicker lines representing stronger connections between two items. 18

Results
The screening process identified 12,436 papers from WoS-AD classified under the "Dentistry, Oral Surgery and Medicine" category.Following the ranking of this list in descending order of citation count, 132 papers were excluded due to their lack of focus on the evaluated field.The top 100 most-cited papers, along with their respective citation counts, are presented in Table 1.
The most-cited papers received a total of 18,694 citations (minimum: 111 citations; maximum: 566 citations) in WoS-AD, and 17,317 citations (minimum: 104 citations; maximum: 532 citations) in WoS-CC.The paper with the highest citation count 19 was cited 566 times and had an average of 35.37 citations per year according to WoS-AD.This paper was also the most cited in WoS-CC, with 532 citations.
The selected papers were published between the years 1978 and 2021 (Table 1 and Figure 1).The half-decade of 2005 to 2010 exhibited the highest number of most-cited articles (n = 39), with a peak in 2007 (n = 9).The oldest and newest papers within the top 100 were observational studies.The oldest study in the top 100 list, published in 1978 by Basker et al., 20 has been cited 154 times (average of 3.4 citations per year).The most recent study, published in 2021 by Moorthy et al., 21 has been cited 124 times (average of 17.33 citations per year).

Contributing authors
Well-differentiated clusters are shown in the co-authorship network map (Figure 2), highlighting prominent research groups led by American researchers such as Genco, Taylor, Lamster, and Shlossman.Publications with three or more authors were more prevalent.Among the 374 authors identified, those with the most publications as first authors were Brian Mealey (n = 4; 1,138 citations), George Taylor (n = 3; 907 citations), Giovanni Salvi (n = 3; 497 citations), and Toshiyuki Saito (n = 3; 460 citations).However, Robert Genco was the author with the most significant contribution to the top 100 list, having authored 13 papers with a total of 3,653 citations.Following Genco, George Taylor ranked second with seven papers and 1,936 citations.

Contributing institutions and countries
The articles originated from 54 institutions and were affiliated with 15 countries, identified through the corresponding author's institution.The University at Buffalo (1,844 citations) and the University of Michigan (1,674 citations) emerged as the most prominent contributors, each with six publications.They were followed by the University of Texas (n = 5; 1,185 citations) and Columbia University (n = 5; 809 citations).][24] In terms of the countries of origin, the United States of America (USA) led with the highest number of publications and citations (n = 51; 10,733 citations), followed by Japan (n = 6; 931 citations), Sweden (n = 6; 850 citations), England (n = 5; 1,107 citations), Brazil (n = 5; 879 citations), and Finland (n = 5; 619 citations).No papers from Africa and Oceania were included in the list (Figure 3).

Study design
Among the top 100 most-cited papers, 50 were observational studies (22,206 citations), 26 were literature reviews (5,209 citations), and 10 were systematic reviews (1,819 citations), with six including meta-analysis and four without (Table 2).Randomized and non-randomized clinical trials, laboratory studies, and case reports were less frequent in comparison.
Regarding the primary focus of the studies (Table 3), papers examining the relationship between DM and the periodontal disease were the most prevalent and achieved the highest citation count (n = 72; 14,077 citations).This was followed by research on the impact of DM on implant survival and/or osseointegration (n = 17; 2,399 citations).Only one included paper investigated the association between  coronavirus disease and the occurrence of oral infection in patients with diabetes (124 citations).

Discussion
The emerging scientific evidence indicates a bidirectional association between DM and oral conditions, with each impacting the other mutually. 25s a prevalent metabolic disease among patients, the relationship between DM and oral health has emerged as a promising area of study within both medical 26 and dental research. 27In this regard, this is the first bibliometric study to access the features of the 100 most-cited papers on DM research published in Dentistry.The most-cited papers in this bibliometric analysis received 18,694 in WoS-AD, with individual citations ranging from 111 to 566.
The existing literature suggests that classic papers typically have at least 400 citations, serving as key references in the advancement of research and clinical practice. 28Depending on the specific characteristics of the research area, articles with at least 100 citations can also be considered classics. 29,30n this bibliometric analysis, the paper ranked at position 100 had 111 citations in WoS-AD.Therefore, it is reasonable to infer that all selected papers have made a significant impact on the field of diabetes research in dental journals.This feature not only demonstrates the importance of the theme over the years but also implies that other "classic articles" might have been omitted.
When the papers were ranked in descending order of citation number, the literature review "Diabetes mellitus and periodontal diseases" written by Mealey & Oates 31 was ranked first.Besides citation count, other important aspects should be considered when evaluating the scientific impact of a paper, such as the methodological quality and study design. 30The most-cited paper received fewer citations per year compared to more recent papers that were ranked lower.For instance, an umbrella review published in 2020, 32 ranked 84 th , received more citations per year than the aforementioned article. 31Similarly, systematic reviews were the third most prevalent study design on the list, with six studies being systematic reviews complemented by meta-analysis, representing the top of scientific evidence.Thus, this higher citation density may be related to the topic and study design.Therefore, evaluating the average number of citations received per year, as also considered in other bibliometric analyses, 30,33 over citation count alone, may provide a more significant  To present the global burden of major oral diseases with an exegetical commentary on their current profiles, the critical issues in oral healthcare and future perspectives.To review all published evidence systematically and to quantify the impact of periodontal treatment on HbA1c.

26
Grossi SG, Skrepcinski FB, DeCaro T, Zambon JJ, Cummins D, Genco RJ.Response to periodontal therapy in diabetics and smokers.J Periodontol.1996 Oct;67 (10) To explore the effect of periodontal therapy on glycemic control in persons with type 2 diabetes mellitus.
To investigate the association between severe periodontitis and increase in inflammatory and metabolic risk factors for cardiovascular disease.
To evaluate measure fasting plasma lipids as well as blood glucose in non-diabetic periodontal disease patients and control subjects.
To identify possible risk factors for implant loss and periimplant diseases and to use those risk factors to form a predictive model for peri-implantitis and implant loss.It is also the aim to quantify the prevalence of peri-implant disease at ≈10 years after implant placement by using the best-available definitions of peri-implant diseases at the time of publication.To describe the prevalence of dry-mouth symptoms (xerostomia), the prevalence of hyposalivation in this population, and the possible interrelationships between salivary dysfunction and diabetic complications 37 Bullon P, Newman HN, Battino M. Obesity, diabetes mellitus, atherosclerosis and chronic periodontitis: a shared pathology via oxidative stress and mitochondrial dysfunction?Periodontol 2000.2014 Feb;64(1):139-153.https://doi.org/10.1111/j.1600-0757.2012.00455.x.
To review the literature to consider and discuss the mounting evidence that the basis for the inter-relationships between chronic periodontitis and atheromatous disease and diabetes lie at a fundamental intracellular level, namely oxidative stress, and mitochondrial dysfunction, as a meeting background among such chronic diseases and periodontitis.To review the literature concerning TNF-α produced by the adipose tissues of obese patients acts as a risk factor for periodontal inflammation, and TNF-α produced due to periodontal inflammation may be an additional important factor influencing insulin sensitivity in both obese and type 2 diabetic patients.To evaluate the available literature to assess whether smoking, diabetes, and periodontitis have an adverse effect on the outcomes of implants placed in patients with these conditions.

Continue
Based on the data collected from the selected papers, Periodontology emerges as the area that has most extensively investigated the relationship between DM and Dentistry.Conversely, areas such as Oral Pathology, Oral Implantology, and Endodontics were less frequently identified in the list.The most cited papers have predominantly explored the relationship bet ween DM and periodontal disease in humans, showcasing a significant interest in understanding the influence and correlation of DM and other prevalent diseases on the progression of periodontal infections.Most of the research has focused on diagnosing and treating periodontal conditions in diabetic patients, yielding positive outcomes for the improvement of the oral and systemic health of affected individuals.Furthermore, papers evaluating the impact of DM on osseointegration and stability of dental implants were also frequently observed.According to these features, "diabetes mellitus" and "periodontitis" were t he most u s ed key word s a mong t he most-cited papers.However, although the main topics of interest among the most-cited papers parameter for assessing the relevance of a study in a specific research area.
The 100 most-cited papers were published within a 45-year timeframe, which may not be considered a long period given the significant rise in the prevalence of DM in the population over the years 1 and the extensive efforts to control DM over decades.Although the oldest paper was an observational study not entirely focused on DM, 20 the authors conducted a causality analysis on burning mouth syndrome in diabetic patients, establishing an important relationship between the two conditions.However, the most influential papers were predominantly published in the 2000s, demonstrating the high interest in this research topic over the last 20 years.Additionally, more than half of all included studies (n = 68) were published in only three peer-reviewed journals: Journal of Periodontology, Journal of Clinical Periodontology, and Journal of Dental Research.These data confirm that leading journals in a research field tend to attract papers that are likely to have a high citation number, thereby maintaining the high impact factor of those journals. 34ere primarily concerned with the evaluation of different aspects of DM on periodontal research, many keywords were used in a single paper (72.5%).This point indicates a lack of standardization in the use of these important components of bibliographic search.Unfortunately, several papers did not include keywords, 20,[22][23][24][35][36][37][38][39][40][41][42][43][44][45][46] underscoring the importance of authors using strategic terms in their titles and abstracts that are closely related to the area and topic of interest, thus facilitating the retrieval of more relevant results.Overall, the greatest contribution was made by the American author Robert J. Genco, a pioneer in periodontal research, who also emerged as the most-cited author.George W. Taylor also played a crucial role in DM research, ranking second in terms of citations.Consequently, the State University of New York at Buffalo and the University of Michigan, the affiliations of these influential authors, emerged as the most prolific institutions in diabetes research in dentistry.In concordance with other bibliometric studies in diabetes, 14,15 the USA and its academic institutions continue to have the largest contributions in this research field.The USA is renowned for its well-established and extensive scientific community, bolstered by widespread public support and significant investment from the US government in scientific research.Furthermore, similar to previous bibliometric studies in Dentistry, 17,18,47 no papers from African countries were included in the list.This absence could be attributed to various factors, including language barriers, challenges in professional networking, and limited access to information.47 Considering the impact of different variables, such as demographic and economic factors, on the relationship between diabetes and oral health, few randomized clinical trials were identified among the most-cited papers in the current bibliometric analysis.Furthermore, this study has some limitations that need to be considered.Firstly, there is a possibility that some important articles without specific keywords or terms matching the current search strategy were not retrieved in the electronic search.Additionally, similar to other bibliometric studies published in Dentistry [48][49][50][51][52][53] and other biomedical fields, 13,14,16 only one database was used as the source of abstracts, citations, and other bibliometric data. The present anlysis only included papers from the WoS citation indexing database, which is considered a limitation of this article.This database was selected because it covers over 34,000 high-quality and peer-reviewed journals in more than 250 areas, 54 and has also measured citation numbers since 1950.55 However, other databases, such as Scopus and Google Scholar, should also be considered in future analysis.Finally, self-citations were not considered during the quantification of citations.Although self-citations may not significantly affect the order of the top 100 list, 33,56 they should be interpreted with caution.Self-citations could also be a common practice in lines of investigation involving a limited number of researchers and may serve to save space by referencing methodologies that have been previously described elsewhere.18,33 Based on the data derived from the assessed features of this bibliometric analysis, further studies are encouraged on this topic, particularly in lower-income areas, using large-scale, randomized designs in community settings.Additionally, a more comprehensive examination of demographic and economic variables is warranted to determine their effect on the relationship between DM and oral condition in humans, especially across other areas of Dentistry.

Conclusion
This bibliometric study provided useful data regarding the main features, direction, and most prolific research groups involved in DM research within Dentistry.The area of Periodontology stood out in the most cited studies that evaluated the relationship between Dentistry and DM, primarily originating from institutions such as the State University of New York at Buffalo and the University of Michigan in the USA.Observational studies exploring the relationship between DM and periodontal disease garnered the highest citation counts thus far.

Figure 1 .
Figure 1.The number of publications of the 100 most-cited papers per year.

Figure 2 .
Figure 2. Co-authorship network map in top 100 most-cited papers on diabetes research in Dentistry.

Figure 3 .
Figure 3. Global distribution of the top 100 most-cited papers on diabetes mellitus in Dentistry.

Figure 4 .
Figure 4. VOSviewer density map of co-occurrence of keywords.
Braz.Oral Res.2024;38:e075 Top 100 most-cited papers on diabetes mellitus in Dentistry: a bibliometric study Braz.Oral Res.2024;38:e075 Top 100 most-cited papers on diabetes mellitus in Dentistry: a bibliometric study Continue Braz.Oral Res.2024;38:e075 *mean based on the ratio of the numbers of citations and the period since the year of publication up to October 2022; n.a.: not applicable; n.i.: not informed; JCR® IF: Journal Citation Report Impact Factor.Braz.Oral Res.2024;38:e075 Reis-Prado AH, Paula KS, Nunes GP, Abreu LG, Cintra LTA, Peixoto IFC, et al.

Table 2 .
Characteristics of the 100 most-cited papers on diabetes research in Dentistry regarding study design.
*Number of citations/number of papers; WoS-AD: Web of Science -All Databases.