Next Article in Journal
DFT Investigation of Hydrogen Atom Abstraction from NHC-Boranes by Methyl, Ethyl and Cyanomethyl Radicals—Composition and Correlation Analysis of Kinetic Barriers
Next Article in Special Issue
Cytomorphometric Analysis of Inflammation Dynamics in the Periodontium Following the Use of Fixed Dental Prostheses
Previous Article in Journal
Ultrasound-Assisted Extraction Optimization of α-Glucosidase Inhibitors from Ceratophyllum demersum L. and Identification of Phytochemical Profiling by HPLC-QTOF-MS/MS
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:

Systemic Manifestations of the Periodontal Disease: A Bibliometric Review

AO Research Institute Davos, 7270 Davos Platz, Switzerland
Oral Medicine Unit, School of Dental Sciences, Universiti Sains Malaysia, Kota Bharu 16150, Kelantan, Malaysia
Paediatric Dentistry Unit, School of Dental Sciences, Universiti Sains Malaysia, Kota Bharu 16150, Kelantan, Malaysia
Paedodontics Department, Rashid Latif Dental College, Lahore 54600, Pakistan
Department of Prosthodontics and Dental Implantology, College of Dentistry, King Faisal University, Al-Ahsa 31982, Saudi Arabia
Author to whom correspondence should be addressed.
Molecules 2020, 25(19), 4508;
Original submission received: 15 September 2020 / Revised: 27 September 2020 / Accepted: 28 September 2020 / Published: 1 October 2020
(This article belongs to the Special Issue Advances of Molecular Sciences in Regenerative Dentistry)


This bibliometric review aimed to identify and analyze the top 100 most-cited publications on the systemic manifestations of periodontal disease (PD). A literature search was performed using the Web of Science (WoS) ‘All Databases’, without any restriction of language, publication year, or study design. Of 4418 articles, the top 100 were included based on their citation count. After downloading the full texts, their bibliometric information was extracted and analyzed. The citation counts for the top 100 articles ranged from 156 to 4191 (median 217). The most productive years were 2003 and 2005, with 20 articles on the list. Majority of the articles were published in the Journal of Periodontology (n = 25). The top 100 articles were generated primarily from the USA (n = 61). Most of the publications were clinical trials (n = 27) and focused on the cardiovascular manifestations of PD (n = 31). Most of the articles were within the evidence level V (n = 41). A total of 58 studies received funding and the most frequently used keyword in the top articles was “periodontal disease” (n = 39). The current citation analysis presents insights into the current trends in the systemic manifestations of periodontal disease.

1. Introduction

Periodontal disease is a chronic inflammatory microbial disease that directly damages the tooth-supporting structure (gingiva, periodontal ligament, alveolar bone, and cementum of the tooth) [1]. The sequelae of the periodontal disease are to gum swelling, gum bleeding, proceed to recession of junctional epithelium to apical loss of clinical attachment, and finally, pocket formation [2]. All these manifestations take time to develop and can be reversible, depending on the preventive strategies and intervention of the treatment [3]. Periodontal diseases are brought about by the host inflammatory response towards the virulence of the local biofilm [4]. Several modifiable factors include smoking, poor oral hygiene, female hormonal changes, diabetes mellitus, stress, and medications, with non-modifiable factors such as age, and hereditary factors, all of which predispose the host to periodontal diseases. The association of periodontal disease with systemic conditions were explored by various observational studies and clinical trials [5,6,7,8]. An association of different systemic conditions was documented on several occasions, which include cardiovascular diseases [9], renal problems [10], pregnancy-related issues [11], joint-related diseases [12], respiratory diseases [13], oncological predisposition [14], stroke [15], and diabetes [16]. Kinane et al. [17] suggested that periodontal diseases contributed to an increase in the total inflammatory and infectious disease burden, which could, in turn, lead to cardiovascular diseases and stroke. An exploratory investigation of atherosclerotic plaque composition was performed to hypothesize a biological origin that revealed the presence of bacterial DNA in a few studies [18,19]. However, other studies also negated this theory, which led to an uncertainty of the exact phenomenon [20,21]. Poor maternal periodontal health is correlated with low birth weight and pre-term babies [22,23,24]. Chronic periodontitis might lead to systemic inflammation as a response to the increased C-reactive protein levels. Increased levels of C-reactive proteins are associated with pre-term babies [25]. A review of previous cross-sectional studies and systematic reviews suggested that dental plaque might provide harbor to bacteria associated with respiratory tract infections, which could then be aspirated into the lungs to cause pneumonia [26]. A bidirectional association between periodontal diseases and diabetes was reported. Poorly controlled blood sugar levels were associated with periodontal conditions [27,28]. Increased levels of pro-inflammatory cytokines were noted in patients suffering from chronic periodontitis, which might then lead to insulin resistance, resulting in poor glycemic control [29,30,31]. P. gingivalis is one of the various periodontal pathogens, which is suspected of playing a role in the pathogenesis of rheumatoid arthritis [12,32,33]. The risk of developing systemic conditions is therefore increased with poor oral health, and a comprehensive healthcare system ensures healthy longevity.
“If I have seen further, it is by standing on the shoulders of giants.”
-Isaac Newton, Letter to Robert Hooke, 1675
This inspirational saying by Sir Isaac Newton [34] reflects the importance of past studies in science. Earlier studies are acknowledged by citing them in the modern research literature. Prior research and citation play a vital role in the evolution of knowledge [35]. Citation analysis is a bibliometric method to identify articles with the greatest impact on research and the clinical community, in a given discipline [36], providing the foundation for developing new research lines, techniques, and theories. This method was adopted in several areas of medicine such as urology [37], neuroscience [38], orthopedic trauma and surgery [39], suicidology [40], pediatrics [41], epilepsy [42], critical care medicine [43], and Parkinson‘s disease [44]. It is also used in different subfields in like dentistry, oral surgery, and medicine, including endodontics, orthodontics, periodontology, implant dentistry, prosthodontics, oral and maxillofacial surgery, dental traumatology, caries, squamous cell carcinoma, oral submucous fibrosis, oral leukoplakia, cleft lip and palate, and medication-related osteonecrosis of jaw (MRONJ) [45,46,47,48,49,50,51,52,53,54,55,56,57,58]. The definition of a “classic article” is a controversial topic across disciplines. The most suggested criterion is the securing of a certain citation count, for instance, at least 400 citations [36,38,44]. However, a publication that accomplished 100 or more citations could also be termed as a “classic publication,” depending upon the field under consideration, such as dentistry [59].
In periodontics, several bibliometric analyses were conducted [48,60,61]; however, no citation analysis of the most-cited “classic” articles published on the systemic manifestations of periodontal disease was performed. This study aimed to identify the top 100 most-cited “classic” articles published on the systemic complications of periodontal disease and to conduct an updated analysis to identify their fluctuating trends.

2. Results

2.1. Citation Count, Citation Density, and Current Citation Index

The primary characteristics of the top 100 most-cited articles are shown in Supplementary Table S1. The citation count of the top 100 publications varied from 156 to 4191 (median, 217), with a total citation count of 34,086. The most cited article, with a total of 4191 citations, was titled “Periodontal Disease in Pregnancy II. Correlation between Oral Hygiene and Periodontal Condition” [62], and was published in the Acta Odontologica Scandinavica. Its citation density (average citation count received per annum) was 76.20, with the current citation index (CCI) (number of citations received in 2019) of 177. The second most cited article, with a total of 4053 citations, was similar to the first article but was published one year earlier, titled “Periodontal disease in pregnancy I. Prevalence and severity” [11], and was published in the Acta Odontologica Scandinavica. Its citation density was 72.38, with the CCI of 140. The third most cited article, with a total of 903 citations, was titled “Periodontal disease and cardiovascular disease” [63] and was published in the Journal of Periodontology. Its citation density was 39.26, with the CCI of 15. According to the CCI 2019, the top-ranked article was the clinical trial published in 1964, securing 177 citations [62]. The second-ranked article was a literature review written by Hajishengallis G in 2015, with 169 citations [64]. The third-ranked article was the 1963 review, which counted 140 new citations [11]. As per citation density, the review by Hajishengallis had the highest score [64], with the second- and third-ranked articles being the clinical trials by Silness and Löe, with a citation density of 76.20 and 72.38, for [62] and [11], respectively.
According to the Shapiro–Wilk test, the distribution of data regarding citation count, citation density, and article age were not normal (p < 0.001). A non-significant trend towards a higher citation count with article age was observed (r = 0.009, p = 0.868) (Figure 1). However, a significant negative trend towards an increased citation density with the age of publication was observed (r = −0.440, p < 0.001) (Figure 1).

2.2. Distribution by Year

The top 100 most-cited articles were published between 1963 [11] and 2015 [64] (Figure 2). The most prolific years in terms of publications were 2003 and 2005, with ten publications each, followed by 2001 (n = 9). The year with most citations was 1964, with 4191 citations, followed by 1963 and 2003, with 4053 and 2308 citations, respectively. The decade with most publications (n = 69) and citations (n = 16,723) was the 2000s (Figure 2).

2.3. Contribution of Authors

Many articles (n = 76) had between one and six authors, but publications with more than six authors were the most common (n = 24). The majority of the contributions were made by Genco (n = 13, 3750 citations), followed by Beck (n = 10, 3735), Offenbacher (n = 11, 3910), Taylor (n = 7, 1831), Tonetti (n = 5, 1793), and Suvan (n = 5, 1664) (Figure 3).

2.4. Contribution of Countries and Institutions

The top 100 most-cited publications originated from 19 countries, including Austria, Australia, Brazil, Canada, Chile, Denmark, Finland, Germany, Italy, Israel, Japan, Netherlands, New Zealand, Norway, Spain, Sweden, Turkey, the United Kingdom, and the United States of America (Table 1). According to the number of publications, most of the articles originated from the United States of America (n = 61, 17,037 citations), followed by the United Kingdom (n = 9, 2745), Netherlands (n = 3, 1003), Chile (n = 3, 723), Australia (n = 3, 615), Germany (n = 3, 574), Finland (n = 3, 515), Spain (n = 2, 392), Sweden (n = 2, 355), Brazil (n = 2, 332), Norway (n = 1, 4191), Denmark (n = 1, 4053), New Zealand (n = 1, 332), Italy (n = 1, 297), Turkey (n = 1, 229), Canada (n = 1, 198), Japan (n = 1, 173), and Israel (n = 1, 157).
There was a total of 55 institutions with which the corresponding authors were affiliated. The most prolific institution, with 13 publications, was Department of Oral Biology, School of Dental Medicine, University at Buffalo, USA, followed by Department of Periodontology, School of Dentistry, University of North Carolina at Chapel Hill, USA (n = 9) and Division of Periodontics, College of Dental Medicine, Columbia University, USA (n = 6) (Table 1).

2.5. Journal of Publication

The top 100 most-cited articles were published in both specialized and comprehensive periodicals (n = 36) (Table 2). The journal with the most number of publications was the Journal of Periodontology (n = 23), followed by the Annals of Periodontology (n = 10), the Journal of Clinical Periodontology (n = 9) and the Journal of Dental Research (n = 6). Acta Odontologica Scandinavica had the highest citation count (n = 8409), followed by the Journal of Periodontology (n = 8011), Annals of Periodontology (n = 2753), Journal of Clinical Periodontology (n = 1597), and Journal of Dental Research (n = 1592). The impact factors of journals ranged from 0.920 (Oral Health and Preventive Dentistry) to 74.699 (New England Journal of Medicine).
According to the Spearman-rank test, a statistically significant trend (p < 0.024) was observed between a journal age and the number of “classic” articles published in that journal. However, a statistically non-significant trend (p = 0.204) was observed between the impact factor of the journal and the number of “classics” published in that journal.

2.6. Topic of Publication

According to the topic of the article, the majority of the topic covered by the top 100 publications were the association of periodontal disease with cardiovascular diseases (n = 31) (8598 citations) and association of periodontitis with diabetes mellitus (n = 29) (7660 citations), followed by the systemic complications of periodontitis (mixed manifestations) (n = 14) (3918 citations), pregnancy-related manifestations (n = 11) (10,909 citations), rheumatic (n = 10) (1955 citations), pulmonary (n = 2) (399 citations), cerebrovascular diseases (n = 2) (478 citations), and cancer (n = 1) (169 citations) (Table 3). No statistical significance was detected (p = 0.724) while analyzing the median difference in the citation count per publication, between periodontitis and cardiovascular diseases—221.5 (156–903), periodontitis and diabetes mellitus—215 (156–686), periodontitis and systemic complications—234.5 (163–574), periodontitis and pregnancy-related manifestations—319 (157–4191), periodontitis and rheumatic diseases 187 (164–251), periodontitis and pulmonary diseases—199.5 (180–219), periodontitis and cerebrovascular diseases—239 (174–304), and periodontitis and cancer—169 (169).

2.7. Methodological Design of Publication

The most common methodological design in the top 100 publications was clinical trial (n = 27) (15,792 citations), followed by literature review (n = 26) (6609 citations), randomized controlled trial (n = 12) (3567 citations), survey (n = 10) (2076 citations), case-control study (n = 8) (1695 citations), systematic review (n = 6) (1505 citations), meta-analysis (n = 3) (829 citations), systematic review and meta-analysis (n = 3) (792 citations), animal study (n = 3) (630 citations), and consensus report (n = 2) (600 citations) (Table 3). No statistical significance was detected (p = 0.608) while analyzing the median difference in the citation count per publication among clinical trials—242.4 (156–4191), literature review—193.5 (157–574), randomized controlled trials—198 (163–731), survey—200 (156–258), case-control study—207 (165–327), systematic review—234.5 (204–319), meta-analysis—295 (176–358), systematic review and meta-analysis—272 (182–338), animal study—172 (171–287), and consensus report—300 (297–300).

2.8. Evidence Level of Publication

The top 100 most-cited publications could be classified into all evidence levels (ELs). Most of the articles were within evidence level V (n = 35), followed by EL III (n = 29), EL I (n = 15), EL II (n = 14), and EL IV (n = 7). Among these ELs, the total citation counts (r = −0.208, p = 0.082) and the citation density (r = 0.080, p = 0.336) did not vary significantly.

2.9. Keywords

Out of the top 100 most-cited publications, only 76 articles contained keywords. A total of 182 keywords were identified. The most commonly used keyword was periodontal disease (n = 39), followed by periodontitis (n = 38), risk factors (n = 18), inflammation (n = 15), epidemiology (n = 14), diabetes mellitus (n = 14), atherosclerosis (n = 12), etiology (n = 11), and infection (n = 10). The distribution of the keywords over the decades is shown in Figure 4.

3. Discussion

This study aimed to identify the top 100 most-cited publications associated with the systemic manifestations of periodontal diseases and to analyze their primary bibliometric characteristics. Bibliometric analysis allows readers to gain historical insight and development of a particular specialty, by identifying and analyzing the most-cited publications that could assist researchers in understanding the emerging themes and future trends for a particular discipline [65,66]. For instance, the number of citations a publication receives could indicate other researchers’ interest in using the information for their own research. Highly cited articles could display a tendency in clinical practice and might, therefore, be considered to produce greater research and clinical interest in the reported disciplines [60]. Being the “most-cited” article, reflects its more frequent contribution to the studies published afterward; however, this characteristic alone does not provide sufficient information regarding its current impact and scientific quality as the main motive of citers if the selection of reference establishes the utility within research rather than scientific quality [67,68,69]. According to the definitions of “classic article” [70], a total of 354 (8%) articles were published on the systemic manifestations of periodontal diseases that achieved over 100 citations. Hence, all articles included in this study could be regarded as “classic articles.”
As our results depicted a fluctuating trend that was recently observed with regards to the contribution of international authors. For instance, during the 1990s, 86% of authors belonged to the institutions hailing from the US. This trend decreased significantly from 86% to 53% during the 2000s and again escalated recently during the 2010s from 53% to 71%. After the US, European countries, including the Netherlands and the UK, were prominent in this list of contributing authors. In addition to this study, several other bibliometric analyses reported that authors from Asia, Africa, and the Middle East, whether they were the first or the corresponding author, made a negligible contribution that could be considered a “classic” article [53,71,72,73,74]. Potential reasons might include language barriers, gaps in conducting research, and professional networking, as well as limited information access [75]. International organizations such as the World Health Organization and the United Nations could play a vital role in bolstering these healthcare developments.
As with several “most-cited” publications in medical and dental fields, this study reported that most of the most-cited articles originated from the United States. This significant contribution could be attributed to a larger scientific population, active researchers, and ample financial resources [46,53,72,74,76,77,78,79]. In addition to an unparalleled research work, an increased tendency among authors to cite articles originating from the US was observed [53,80]. It is noteworthy that first and second-ranked articles in the present study originated from the institutions hailing from Scandinavia, i.e., Norway and Denmark, respectively. As per the total citation count received by the top 100 articles, Norway and Denmark secured the second and third rank, despite their small population size. Importantly, a lack of multicenter studies was noticeable, as only the 13 most-cited articles had international collaborations, reflecting a need to escalate international collaboration.
Not surprisingly, the top 100 most-cited papers were authored in an array of specialties and were published in 35 different journals, indicating the multidisciplinary nature of research on systemic complications of periodontal diseases. Interestingly, approximately one-third of the top 100 highly cited articles were published in journals that are not necessarily dedicated to periodontitis and its systemic manifestations, including Circulation, Nature Reviews Immunology, and Journal of Dental Research. This might reflect a trend among authors to publish their research in high-impact journals to direct them to a broader audience.
In many bibliometric studies, it was reported that relevant studies were distributed among journals in accordance with Bradford’s law [81,82,83]. According to this bibliometric law, a few prolific journals account for a considerable percentage of all publications in a given discipline [84]. The studies published in these core journals are more likely to be referred to most commonly by successive articles [85]. Hence, the Journal of Periodontology, Annals of Periodontology, and Journal of Clinical Periodontology could be considered to be the core journals in this discipline, as approximately half of the most-cited articles were published in these (n = 45). Interestingly, in this study, the journal distribution pattern of the most-cited publications did not completely fit this law, as the list features almost negligible number of top-cited articles published by Periodontology 2000 and Journal of Periodontal Research, which are said to be one of the most prolific journals in the field of periodontics. Hence, the application of this law for conducting bibliometric analysis in some disciplines might cause inaccurate inferences.
In this study, no statistically significant association was found between the number of the most-cited articles published in a journal and the impact factor of that journal. This finding was in accordance with the findings of some bibliometric studies [86,87], but was contrary to those of several others [68]. This lack of association reflects that high-quality research might be highly cited, even if it is published in a relatively low-impact-factor journal [88]. In the current study, most articles (n = 52) were published by four prestigious periodontics journals, highlighting the expected significance of specialty journals. However, a substantial amount of non-periodontics journals with a higher impact factor than the periodontics journals published a smaller number of the most-cited articles.
Most of the highly cited publications were concerned with cardiovascular manifestations of periodontal diseases and diabetes mellitus, with 60 of the most-cited articles covering these two topics. The reason articles about systemic complications of periodontitis such as pulmonary diseases, cerebrovascular disorders, and cancer were not common among the list of 100 highly cited publications might be related to several factors; (a) majority of included papers originated from the US and European countries where complications of periodontitis related to diabetes mellitus and cardiovascular disease (CVD) are more common and relevant [89]; (b) the characteristics of both CVD and periodontal disease are very similar; they are usually chronic, multifactorial, and common [90], (c) in the USA and worldwide, CVD accounts for around 50% and 29% of deaths per year and is considered to be the second leading cause of death preceded by parasitic and infectious diseases [91], (d) globally, more than 18 million population suffer from diabetes mellitus and its severe complications, including blindness, leg amputation, CVD, impaired wound healing, renal dialysis, and death [92]. These findings do not necessarily reflect that high-quality research about other systemic manifestations of periodontal diseases was not commonly performed; rather it might mean that such studies were not cited as many times as studies on other complications.
From 1990 to 1999, the hottest research topic was the association between periodontitis and diabetes mellitus. From 2000 to 2009, the trend shifted to cardiovascular-related manifestations of periodontal diseases. However, from 2010 to 2015, the relationship between periodontitis and diabetes mellitus re-emerged as the hottest research topic. This could be explained by the fact that the relationship between periodontal diseases and diabetes mellitus is a long-discussed research topic with conflicting conclusions. In the general population, both these diseases have a relatively high incidence (periodontitis 14% and diabetes 1% to 6%), as well as several common pathways in their pathogenesis [93].
Based on the hierarchy of research evidence level, systematic reviews, meta-analyses, and randomized controlled trials (RCTs) provide the highest quality of evidence [36]. A distinctive characteristic of this analysis was that it included 29 highest quality evidence level studies, including systematic reviews, meta-analyses, both systematic reviews, and meta-analysis, as well as RCTs. These findings did not coincide with the findings of several other bibliometric analyses performed on various specialties within dentistry and medicine [39,53,59]. Recently, these high evidence level studies were performed and secured high citations, despite only being published in recent years [94]. Such reports are useful for facilitating decision-making, directing practice, and advancing research, so a high amount of such studies as reflected in the current study is not surprising and provides further proof of maturation of the discipline [95].
This bibliometric analysis had several limitations. First, for a given research field, many factors might influence the citation count, including the age of the publication, journal of publication, reputation of author, institution, and country of origin as well as the original language. Second, the analysis of self-citations and citations in textbooks and lectures was not performed. Moreover, some authors might be inclined to cite articles from a particular journal in which they intend to publish an article [96]. Third, the analysis of the contributing countries and institutions was based on the address of the corresponding author. A statistical bias might occur once the address of the corresponding author is changed [97]. Furthermore, for corresponding authors working in multiple institutions, we only considered the first institution.

4. Conclusions and Future Recommendations

Citation analysis aids in providing useful and interesting information for several disciplines, including determination of current trends and assessment of future direction the research might take. This study revealed that the most common topic observed in the top-cited publications was the association of periodontal disease with cardiovascular diseases and diabetes mellitus. Interestingly, articles related to the systemic manifestations of periodontal diseases, including pulmonary and cerebrovascular diseases as well as cancer, were uncommon among the most-cited publications, which reflects that more research is required in these domains. Surprisingly, unlike several other bibliometric studies performed within dentistry and medicine, the number of clinical trials was higher than the review articles. However, systematic reviews and meta-analyses with evidence might be needed in the literature.
Overall, further understanding of the associations between periodontal disease and its association with systemic complications could raise society’s awareness of the links between inflammatory diseases and oral health. This could lead to large-scale and far reaching general medical benefits through periodontal intervention, including improving glycemic control in diabetics [98], potentially decreasing mortality and morbidity in individuals predisposed to respiratory diseases [99,100], improving endothelial function in CVD patients [101], and possibly alleviating the risk of alveolar bone loss in patients with osteoporosis [102,103,104].

5. Materials and Methods

5.1. Data Sources and Search Methodology

This study, being a bibliometric review, was exempt from the institutional ethics committee review. Preferred Reporting Items for Systematic Reviews and Meta-Analysis guidelines were used for data retrieval and reporting [94]. Articles on the systemic complications of periodontitis were gathered from the Clarivate Analytics’ Web of Science (WoS) (, considering the ‘All Databases’ section, which included Derwent Innovations Index, Russian Science Citation Index, Web of Science Core Collection, SciELO Citation Index, and KCI—Korean Journal Database. There was no restriction of publication year and language. Since the database is still functioning, to avoid daily updating bias, an extensive search was conducted on a single day, 2nd February 2020. The search was performed using the terms: “Periodontitis OR Periodontal disease AND Respiratory”, “Periodontitis OR Periodontal disease AND Pulmonary”, “Periodontitis OR Periodontal disease AND Pneumonia”, “Periodontitis OR Periodontal disease AND Cardiovascular”, “Periodontitis OR Periodontal disease AND Hypertension”, “Periodontitis OR Periodontal disease AND Coronary Heart”, “Periodontitis OR Periodontal disease AND Myocardial Infarction”, “Periodontitis OR Periodontal disease AND Angina Pectoris”, “Periodontitis OR Periodontal disease AND Stroke”, “Periodontitis OR Periodontal disease AND Atherosclerosis”, “Periodontitis OR Periodontal disease AND Endothelial”, “Periodontitis OR Periodontal disease AND Ischemic Heart”, “Periodontitis OR Periodontal disease AND Diabetes Mellitus”, “Periodontitis OR Periodontal disease AND Pregnancy”, “Periodontitis OR Periodontal disease AND Low Birth Weight”, “Periodontitis OR Periodontal disease AND Rheumatic Disease”, “Periodontitis OR Periodontal disease AND Osteoporosis”, “Periodontitis OR Periodontal disease AND Arthritis”, “Periodontitis OR Periodontal disease AND Kidney”, “Periodontitis OR Periodontal disease AND Renal”, “Periodontitis OR Periodontal disease AND Cerebrovascular”, “Periodontitis OR Periodontal disease AND Alzheimer’s”, “Periodontitis OR Periodontal disease AND Dementia”, “Periodontitis OR Periodontal disease AND Cancer”, “Periodontitis OR Periodontal disease AND Carcinoma”, “Periodontitis OR Periodontal disease AND Systemic”, and “Periodontitis OR Periodontal disease AND Focal Infection” in the title field.

5.2. Publication Selection

According to the selected database, 4418 articles were retrieved. After finalizing the list of the top 100 most-cited publications, the retrieved articles were arranged in descending order, based on their citation count. Then, the full text of included articles was downloaded and analyzed to extract the data of interest.

5.3. Data Extraction

The following bibliometric variables were retrieved from each publication identified—article’s title and age (i.e., 2019 minus the year of publication), citation count, citation density (average citation count received by an article per year) [105], current citation index (number of citation received in 2019) [59], authorship (name, contribution and amount), institution and country of origin, publication year, journal’s title, age (i.e., the year in which the first issue was published), impact factor (i.e., Journal Citation Report 2019), keywords, methodological design [106], the topic of the publication, and evidence level. In the case of publications with equal citation count, the ranking was done based on citation density and publications with higher citation density was ranked higher. Additionally, the institution and country of article’s origin was determined based on the address provided for the corresponding author.
The methodological design (literature review, systematic review, meta-analysis, systematic review and meta-analysis, clinical trial, randomized clinical trial, case-control study, animal study, consensus report, and survey) was based on the Cochrane Collaboration Glossary [106]. The thematic fields were categorized into respiratory diseases (chronic obstructive pulmonary disease and pneumonia), cardiovascular diseases (hypertension, coronary heart disease, myocardial infarction, angina pectoris, stroke, atherosclerosis, and ischemic heart disease), diabetes mellitus, pregnancy-related complications (low birth weight and pre-term low birth weight), rheumatic disorders (arthritis and osteoporosis), cerebrovascular diseases (Alzheimer‘s disease and dementia), cancer, and other systemic manifestations associated with periodontal diseases, including focal infection.
The Visualization of Similarities viewer software [107] was used to create collaboration network maps regarding the co-occurrences of all keywords.

5.4. Statistical Analysis

Descriptive and bivariate analyses were performed using a statistical software package, i.e., IBM SPSS Statistics version 24.0 (IBM, Chicago, IL, USA). To assess the normality of the data (citation count, citation density, and age of article), the Shapiro-Wilk test was conducted. Mean (standard deviation) or median (interquartile range) (topic and study design of article) were calculated based on normality and distribution of data. To evaluate the median differences between the independent groups, the Kruskal–Wallis test was performed (topic and study design of article). Any decrease or increase in the time-dependent trends was analyzed by performing the Mann–Kendall trend test. The Spearman-rank test was performed to assess the correlation between the publication count of the journal and the age of the journal. A value of p < 0.05 was considered statistically significant.

Supplementary Materials

The following are available online. Table S1: Ranking list of the top 100 most cited articles.

Author Contributions

Conceptualization, P.A.; methodology, P.A.; investigation, A.I.A., Z.K.; data curation, P.A. and A.I.A.; writing—original draft preparation, P.A.; editing, M.S., Z.K., and E.D.B.; supervision, M.S. All authors have read and agreed to the published version of the manuscript.


P.A., E.D.B., and M.S. received support from the AO Foundation and AO CMF.

Conflicts of Interest

The authors declare no conflict of interest.


  1. Nazir, M. Prevalence of periodontal disease, its association with systemic diseases and prevention. Int. J. Health Sci. 2017, 11, 72–80. [Google Scholar]
  2. Kinane, D.; Marshall, G. Peridonatal manifestations of systemic disease. Aust. Dent. J. 2001, 46, 2–12. [Google Scholar] [CrossRef] [PubMed]
  3. Winning, L.; Linden, G. Periodontitis and Systemic Disease: Association or Causality? Curr. Oral Health Rep. 2017, 4, 1–7. [Google Scholar] [CrossRef][Green Version]
  4. Oppermann, R.V.; Weidlich, P.; Musskopf, M.L. Periodontal disease and systemic complications. Braz. Oral Res. 2012, 26, 39–47. [Google Scholar] [CrossRef] [PubMed][Green Version]
  5. Pretorius, C.; Jagatt, A.; Lamont, R.F. The relationship between periodontal disease, bacterial vaginosis, and preterm birth. J. Périnat. Med. 2007, 35, 93–99. [Google Scholar] [CrossRef]
  6. López, N.J.; Smith, P.C.; Gutierrez, J. Higher risk of preterm birth and low birth weight in women with periodontal disease. J. Dent. Res. 2002, 81, 58–63. [Google Scholar] [CrossRef]
  7. Michalowicz, B.S.; Hodges, J.S.; DiAngelis, A.J.; Lupo, V.R.; Novak, M.J.; Ferguson, J.E.; Buchanan, W.; Bofill, J.; Papapanou, P.N.; Mitchell, D.A.; et al. Treatment of Periodontal Disease and the Risk of Preterm Birth. N. Engl. J. Med. 2006, 355, 1885–1894. [Google Scholar] [CrossRef][Green Version]
  8. Offenbacher, S.; Beck, J. Effects of Periodontal Therapy on Rate of Preterm Delivery: A Randomized Controlled Trial. Obstet. Gynecol. 2010, 115, 386. [Google Scholar] [CrossRef]
  9. Persson, G.R.; Persson, R.E. Cardiovascular disease and periodontitis: An update on the associations and risk. J. Clin. Periodontol. 2008, 35, 362–379. [Google Scholar] [CrossRef]
  10. Shultis, W.A.; Weil, E.J.; Looker, H.C.; Curtis, J.M.; Shlossman, M.; Genco, R.J.; Knowler, W.C.; Nelson, R.G. Effect of Periodontitis on Overt Nephropathy and End-Stage Renal Disease in Type 2 Diabetes. Diabetes Care 2007, 30, 306–311. [Google Scholar] [CrossRef][Green Version]
  11. Löe, H.; Silness, J. Periodontal Disease in Pregnancy I. Prevalence and Severity. Acta Odontol. Scand. 1963, 21, 533–551. [Google Scholar] [CrossRef] [PubMed]
  12. Mercado, F.; Marshall, R.; Klestov, A.; Bartold, P.M. Relationship Between Rheumatoid Arthritis and Periodontitis. J. Periodontol. 2001, 72, 779–787. [Google Scholar] [CrossRef] [PubMed]
  13. Scannapieco, F.A.; Bush, R.B.; Paju, S. Associations Between Periodontal Disease and Risk for Nosocomial Bacterial Pneumonia and Chronic Obstructive Pulmonary Disease. A Systematic Review. Ann. Periodontol. 2003, 8, 54–69. [Google Scholar] [CrossRef][Green Version]
  14. Migliorati, C.A. Periodontal diseases and cancer. Lancet Oncol. 2008, 9, 510–512. [Google Scholar] [CrossRef]
  15. Janket, S.-J.; Baird, A.E.; Chuang, S.-K.; Jones, J.A. Meta-analysis of periodontal disease and risk of coronary heart disease and stroke. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 2003, 95, 559–569. [Google Scholar] [CrossRef] [PubMed]
  16. Preshaw, P.M.; Alba, A.L.; Herrera, D.; Jepsen, S.; Konstantinidis, A.; Makrilakis, K.; Taylor, R. Periodontitis and diabetes: A two-way relationship. Diabetologia 2011, 55, 21–31. [Google Scholar] [CrossRef] [PubMed][Green Version]
  17. Kinane, D.; Bouchard, P.; Group E of the European Workshop on Periodontology. Periodontal diseases and health: Consensus Report of the Sixth European Workshop on Periodontology. J. Clin. Periodontol. 2008, 35, 333–337. [Google Scholar] [CrossRef] [PubMed]
  18. Mahendra, J.; Mahendra, L.; Kurian, V.; Jaishankar, K.; Mythilli, R. 16S rRNA-based detection of oral pathogens in coronary atherosclerotic plaque. Indian J. Dent. Res. 2010, 21, 248. [Google Scholar] [CrossRef] [PubMed]
  19. Gaetti-Jardim, E.; Marcelino, S.L.; Feitosa, A.C.R.; Romito, G.A.; Ávila-Campos, M. Quantitative detection of periodontopathic bacteria in atherosclerotic plaques from coronary arteries. J. Med. Microbiol. 2009, 58, 1568–1575. [Google Scholar] [CrossRef] [PubMed]
  20. Aimetti, M.; Romano, F.; Nessi, F. Microbiologic Analysis of Periodontal Pockets and Carotid Atheromatous Plaques in Advanced Chronic Periodontitis Patients. J. Periodontol. 2007, 78, 1718–1723. [Google Scholar] [CrossRef] [PubMed]
  21. Cairo, F.; Gaeta, C.; Dorigo, W.; Oggioni, M.R.; Pratesi, C.; Prato, G.P.P.; Pozzi, G. Periodontal pathogens in atheromatous plaques. A controlled clinical and laboratory trial. J. Periodont. Res. 2004, 39, 442–446. [Google Scholar] [CrossRef] [PubMed]
  22. Jeffcoat, M.K.; Geurs, N.C.; Reddy, M.S.; Cliver, S.P.; Goldenberg, R.L.; Hauth, J.C. Periodontal infection and preterm birth. J. Am. Dent. Assoc. 2001, 132, 875–880. [Google Scholar] [CrossRef] [PubMed]
  23. Offenbacher, S.; Boggess, K.A.; Murtha, A.P.; Jared, H.; Lieff, S.; McKaig, R.G.; Mauriello, S.M.; Moss, K.L.; Beck, J.D. Progressive Periodontal Disease and Risk of Very Preterm Delivery. Obstet. Gynecol. 2006, 107, 29–36. [Google Scholar] [CrossRef] [PubMed][Green Version]
  24. Pitiphat, W.; Joshipura, K.; Gillman, M.W.; Williams, P.L.; Douglass, C.W.; Rich-Edwards, J.W. Maternal periodontitis and adverse pregnancy outcomes. Community Dent. Oral Epidemiol. 2007, 36, 3–11. [Google Scholar] [CrossRef]
  25. Lohsoonthorn, V.; Qiu, C.; Williams, M.A. Maternal serum C-reactive protein concentrations in early pregnancy and subsequent risk of preterm delivery. Clin. Biochem. 2007, 40, 330–335. [Google Scholar] [CrossRef][Green Version]
  26. Manjunath, B.C.; Praveen, K.; Chandrashekar, B.R.; Rani, R.M.V.; Bhalla, A. Periodontal infections: A risk factor for various systemic diseases. Natl. Med. J. India 2012, 24, 214–219. [Google Scholar]
  27. Mealey, B.L.; Oates, T.W. Diabetes Mellitus and Periodontal Diseases. J. Periodontol. 2006, 77, 1289–1303. [Google Scholar] [CrossRef]
  28. Taylor, G.W. Bidirectional Interrelationships Between Diabetes and Periodontal Diseases: An Epidemiologic Perspective. Ann. Periodontol. 2001, 6, 99–112. [Google Scholar] [CrossRef]
  29. Lazenby, M.G.; Crook, M.A. The innate immune system and diabetes mellitus: The relevance of periodontitis? A hypothesis. Clin. Sci. 2010, 119, 423–429. [Google Scholar] [CrossRef][Green Version]
  30. Taylor, G.W.; Burt, B.A.; Becker, M.P.; Genco, R.J.; Shlossman, M.; Knowler, W.C.; Pettitt, D.J. Severe Periodontitis and Risk for Poor Glycemic Control in Patients with Non-Insulin-Dependent Diabetes Mellitus. J. Periodontol. 1996, 67, 1085–1093. [Google Scholar] [CrossRef][Green Version]
  31. Nishimura, F.; Iwamoto, Y.; Mineshiba, J.; Shimizu, A.; Soga, Y.; Murayama, Y. Periodontal Disease and Diabetes Mellitus: The Role of Tumor Necrosis Factor-α in a 2-Way Relationship. J. Periodontol. 2003, 74, 97–102. [Google Scholar] [CrossRef] [PubMed]
  32. Gleissner, C.; Willershausen, B.; Kaesser, U.; Bolten, W.W. The role of risk factors for periodontal disease in patients with rheumatoid arthritis. Eur. J. Med. Res. 1998, 3, 387–392. [Google Scholar] [PubMed]
  33. Scardina, G.A.; Messina, P. Microvascular periodontal alterations: A possible relationship between periodontitis and rheumatoid arthritis. Clin. Hemorheol. Microcirc. 2007, 37, 229–235. [Google Scholar] [PubMed]
  34. Mäntylä, M.; Garousi, V. Citations in Software Engineering—Paper-related, Journal-related, and Author-related Factors. arXiv 2019, arXiv:1908.04122. [Google Scholar]
  35. Hamrick, T.A.; Fricker, R.D.; Brown, G.G. Assessing What Distinguishes Highly Cited from Less-Cited Papers Published in Interfaces. Interfaces 2010, 40, 454–464. [Google Scholar] [CrossRef][Green Version]
  36. De La Flor-Martinez, M.; Galindo-Moreno, P.; Sánchez-Fernández, E.; Piattelli, A.; Cobo, M.J.; Herrera-Viedma, E. H-classic: A new method to identify classic articles in Implant Dentistry, Periodontics, and Oral Surgery. Clin. Oral Implant. Res. 2016, 27, 1317–1330. [Google Scholar] [CrossRef] [PubMed]
  37. Hennessey, K.; Afshar, K.; MacNeily, A.E. The top 100 cited articles in urology. Can. Urol. Assoc. J. 2009, 3, 293–302. [Google Scholar] [CrossRef][Green Version]
  38. Ponce, F.A.; Lozano, A.M. Highly cited works in neurosurgery. Part I: The 100 top-cited papers in neurosurgical journals. J. Neurosurg. 2010, 112, 223–232. [Google Scholar] [CrossRef][Green Version]
  39. Lefaivre, K.A.; Shadgan, B.; O’Brien, P.J. 100 Most Cited Articles in Orthopaedic Surgery. Clin. Orthop. Relat. Res. 2010, 469, 1487–1497. [Google Scholar] [CrossRef][Green Version]
  40. Stack, S. Citation Classics inSuicide and Life Threatening Behavior: A Research Note. Suicide Life Threat. Behav. 2012, 42, 628–639. [Google Scholar] [CrossRef]
  41. Ruttenstock, E.; Friedmacher, F.; Hollwarth, M.E.; Coran, A.G.; Puri, P. The 100 most-cited articles in Pediatric Surgery International. Pediatr. Surg. Int. 2012, 28, 563–570. [Google Scholar] [CrossRef] [PubMed]
  42. Ibrahim, G.M.; Snead, O.C.; Rutka, J.T.; Lozano, A.M. The most cited works in epilepsy: Trends in the “Citation Classics”. Epilepsia 2012, 53, 765–770. [Google Scholar] [CrossRef] [PubMed]
  43. Rosenberg, A.L.; Tripathi, R.S.; Blum, J. The most influential articles in critical care medicine. J. Crit. Care 2010, 25, 157–170. [Google Scholar] [CrossRef] [PubMed]
  44. Ponce, F.A.; Lozano, A.M. The most cited works in Parkinson’s disease. Mov. Disord. 2010, 26, 380–390. [Google Scholar] [CrossRef]
  45. Feijoo, J.F.; Limeres, J.; Fernández-Varela, M.; Ramos, I.; Diz, P. The 100 most cited articles in dentistry. Clin. Oral Investig. 2013, 18, 699–706. [Google Scholar] [CrossRef]
  46. Fardi, A.; Kodonas, K.; Gogos, C.; Economides, N. Top-cited Articles in Endodontic Journals. J. Endod. 2011, 37, 1183–1190. [Google Scholar] [CrossRef]
  47. Tarazona, B.; Lucas, R.; Paredes-Gallardo, V.; Alonso-Arroyo, A.; Vidal-Infer, A. The 100 most-cited articles in orthodontics: A bibliometric study. Angle Orthod. 2018, 88, 785–796. [Google Scholar] [CrossRef][Green Version]
  48. Corbella, S.; Francetti, L.; Taschieri, S.; Weinstein, R.; Del Fabbro, M. Analysis of the 100 most-cited articles in periodontology. J. Investig. Clin. Dent. 2016, 8, e12222. [Google Scholar] [CrossRef]
  49. Fardi, A.; Kodonas, K.; Lillis, T.; Veis, A. Top-Cited Articles in Implant Dentistry. Int. J. Oral Maxillofac. Implant. 2017, 32, 555–564. [Google Scholar] [CrossRef][Green Version]
  50. Praveen, G.; Chaithanya, R.; Alla, R.K.; Shammas, M.; Abdurahiman, V.; Anitha, A. The 100 most cited articles in prosthodontic journals: A bibliometric analysis of articles published between 1951 and2019. J. Prosthet. Dent. 2020, 123, 724–730. [Google Scholar] [CrossRef]
  51. Pervez, N.A.; Lubek, J.E. Most cited publications in oral and maxillofacial surgery: A bibliometric analysis. Oral Maxillofac. Surg. 2017, 22, 25–37. [Google Scholar] [CrossRef] [PubMed]
  52. Jafarzadeh, H.; Shirazi, A.S.; Andersson, L. The most-cited articles in dental, oral, and maxillofacial traumatology during 64 years. Dent. Traumatol. 2015, 31, 350–360. [Google Scholar] [CrossRef] [PubMed]
  53. Arshad, A.I.; Ahmad, P.; Dummer, P.M.; Alam, M.K.; Asif, J.A.; Mahmood, Z.; Rahman, N.A.; Mamat, N. Citation Classics on Dental Caries: A Systematic Review. Eur. J. Dent. 2020, 14, 128–143. [Google Scholar] [CrossRef][Green Version]
  54. Hassona, Y.; Qutachi, T. A bibliometric analysis of the most cited articles about squamous cell carcinoma of the mouth, lips, and oropharynx. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. 2019, 128, 25–32.e6. [Google Scholar] [CrossRef] [PubMed]
  55. Gondivkar, S.; Sarode, S.C.; Gadbail, A.R.; Gondivkar, R.S.; Chole, R.; Sarode, S.C. Bibliometric analysis of 100 most cited articles on oral submucous fibrosis. J. Oral Pathol. Med. 2018, 47, 781–787. [Google Scholar] [CrossRef] [PubMed]
  56. Liu, W.; Zhang, Y.; Wu, L.; Yang, X.; Shi, L. Characteristics and trends of oral leukoplakia research. Medicine 2019, 98, e16293. [Google Scholar] [CrossRef]
  57. Zhang, Q.; Yue, Y.; Shi, B.; Yuan, Z. A Bibliometric Analysis of Cleft Lip and Palate-Related Publication Trends From 2000 to 2017. Cleft Palate Craniofac. J. 2018, 56, 658–669. [Google Scholar] [CrossRef]
  58. Diniz-Freitas, M.; Pena-Cristobal, M.; Pérez-López, D.; Lago-Méndez, L.; Fernández-Feijoo, J.; Limeres-Posse, J.; Limeres, J. Bibliometric Analysis of Medication-Related Osteonecrosis of the Jaw: High Citation Rates but Low Evidence. J. Oral Maxillofac. Surg. 2019, 77, 1655.e1–1655.e17. [Google Scholar] [CrossRef]
  59. Ahmad, P.; Alam, M.K.; Jakubovics, N.; Schwendicke, F.; Asif, J. 100 Years of the Journal of Dental Research: A Bibliometric Analysis. J. Dent. Res. 2019, 98, 1425–1436. [Google Scholar] [CrossRef][Green Version]
  60. Faggion, C.M.; Málaga, L.; Monje, A.; Trescher, A.-L.; Listl, S.; Alarcón, M.A. The 300 most cited articles published in periodontology. Clin. Oral Investig. 2016, 21, 2021–2028. [Google Scholar] [CrossRef]
  61. Nieri, M.; Saletta, D.; Guidi, L.; Buti, J.; Franceschi, D.; Mauro, S.; Pini-Prato, G. Citation classics in periodontology: A controlled study. J. Clin. Periodontol. 2007, 34, 349–358. [Google Scholar] [CrossRef] [PubMed]
  62. Silness, J.; Löe, H. Periodontal Disease in Pregnancy II. Correlation Between Oral Hygiene and Periodontal Condition. Acta Odontol. Scand. 1964, 22, 121–135. [Google Scholar] [CrossRef] [PubMed]
  63. Genco, R.; Offenbacher, S.; Beck, J. Periodontal disease and cardiovascular disease: Epidemiology and possible mechanisms. J. Am. Dent. Assoc. 2002, 133, 14S–22S. [Google Scholar] [CrossRef] [PubMed][Green Version]
  64. Hajishengallis, G. Periodontitis: From microbial immune subversion to systemic inflammation. Nat. Rev. Immunol. 2015, 15, 30–44. [Google Scholar] [CrossRef]
  65. Huang, Z.; Chen, H.; Liu, Z. The 100 top-cited systematic reviews/meta-analyses in central venous catheter research: A PRISMA-compliant systematic literature review and bibliometric analysis. Intensiv. Crit. Care Nurs. 2020, 57, 102803. [Google Scholar] [CrossRef]
  66. Chen, X.; Yang, K.; Xu, Y.; Li, K. Top-100 highest-cited original articles in inflammatory bowel disease. Medicine 2019, 98, e15718. [Google Scholar] [CrossRef]
  67. Eyre-Walker, A.; Stoletzki, N. The Assessment of Science: The Relative Merits of Post-Publication Review, the Impact Factor, and the Number of Citations. PLoS Boil. 2013, 11, e1001675. [Google Scholar] [CrossRef]
  68. Khan, M.S.; Usman, M.S.; Fatima, K.; Hashmani, N.; Siddiqi, T.J.; Riaz, H.; Khan, A.R.; Khosa, F. Characteristics of Highly Cited Articles in Interventional Cardiology. Am. J. Cardiol. 2017, 120, 2100–2109. [Google Scholar] [CrossRef]
  69. Seglen, P.O. Citations and journal impact factors: Questionable indicators of research quality. Allergy 1997, 52, 1050–1056. [Google Scholar] [CrossRef]
  70. Andersen, J.; Belmont, J.; Cho, C.T. Journal impact factor in the era of expanding literature. J. Microbiol. Immunol. Infect. 2006, 39, 436–443. [Google Scholar]
  71. Baltussen, A.; Kindler, C.H. Citation classics in critical care medicine. Intensiv. Care Med. 2004, 30, 902–910. [Google Scholar] [CrossRef] [PubMed][Green Version]
  72. Baltussen, A.; Kindler, C.H. Citation Classics in Anesthetic Journals. Anesthesia Analg. 2004, 98, 443–451. [Google Scholar] [CrossRef] [PubMed]
  73. Fenton, J.E.; Roy, D.; Hughes, J.P.; Jones, A.S. A century of citation classics in otolaryngology—Head and neck surgery journals. J. Laryngol. Otol. 2002, 116, 494–498. [Google Scholar] [CrossRef] [PubMed]
  74. Paladugu, R.; Schein, M.; Gardezi, S.; Wise, L. One Hundred Citation Classics in General Surgical Journals. World J. Surg. 2002, 26, 1099–1105. [Google Scholar] [CrossRef] [PubMed]
  75. Uthman, O.A.; Okwundu, C.I.; Wiysonge, C.S.; Young, T.; Clarke, A. Citation Classics in Systematic Reviews and Meta-Analyses: Who Wrote the Top 100 Most Cited Articles? PLoS ONE 2013, 8, e78517. [Google Scholar] [CrossRef][Green Version]
  76. Brandt, J.S.; Downing, A.C.; Howard, D.L.; Kofinas, J.D.; Chasen, S.T. Citation classics in obstetrics and gynecology: The 100 most frequently cited journal articles in the last 50 years. Am. J. Obstet. Gynecol. 2010, 203, 355.e1–355.e7. [Google Scholar] [CrossRef]
  77. Lefaivre, K.A.; Guy, P.; O’brien, P.J.; Blachut, P.A.; Shadgan, B.; Broekhuyse, H.M. Leading 20 at 20: Top Cited Articles and Authors in the Journal of Orthopaedic Trauma, 1987–2007. J. Orthop. Trauma 2010, 24, 53–58. [Google Scholar] [CrossRef]
  78. Loonen, M.P.J.; Hage, J.J.; Kon, M. Plastic Surgery Classics: Characteristics of 50 Top-Cited Articles in Four Plastic Surgery Journals since 1946. Plast. Reconstr. Surg. 2008, 121, 320e–327e. [Google Scholar] [CrossRef]
  79. Shadgan, B.; Roig, M.; HajGhanbari, B.; Reid, W.D. Top-Cited Articles in Rehabilitation. Arch. Phys. Med. Rehabil. 2010, 91, 806–815. [Google Scholar] [CrossRef]
  80. Campbell, F.M. National bias: A comparison of citation practices by health professionals. Bull. Med. Libr. Assoc. 1990, 78, 376–382. [Google Scholar]
  81. Brinjikji, W.; Klunder, A.; Kallmes, D. The 100 Most-cited Articles in the Imaging Literature. Radiology 2013, 269, 272–276. [Google Scholar] [CrossRef] [PubMed]
  82. Shuaib, W.; Acevedo, J.N.; Khan, M.S.; Santiago, L.J.; Gaeta, T.J. The top 100 cited articles published in emergency medicine journals. Am. J. Emerg. Med. 2015, 33, 1066–1071. [Google Scholar] [CrossRef] [PubMed]
  83. Shuaib, W.; Costa, J.L. Anatomy of success: 100 most cited articles in diabetes research. Ther. Adv. Endocrinol. Metab. 2015, 6, 163–173. [Google Scholar] [CrossRef] [PubMed]
  84. Garfield, S. Essays of an information scientist. JAMA 1978, 240, 393–394. [Google Scholar]
  85. Brookes, B.C. Bradford’s Law and the Bibliography of Science. Nature 1969, 224, 953–956. [Google Scholar] [CrossRef]
  86. Usman, M.S.; Siddiqi, T.J.; Khan, M.S.; Fatima, K.; Butler, J.; Manning, W.J.; Khosa, F. A Scientific Analysis of the 100 Citation Classics of Valvular Heart Disease. Am. J. Cardiol. 2017, 120, 1440–1449. [Google Scholar] [CrossRef]
  87. Yılmaz, B.; Dinçol, M.E.; Yalcin, T.Y. A bibliometric analysis of the 103 top-cited articles in endodontics. Acta Odontol. Scand. 2019, 77, 574–583. [Google Scholar] [CrossRef]
  88. Huo, Y.-Q.; Pan, X.-H.; Li, Q.-B.; Wang, X.-Q.; Jiao, X.-J.; Jia, Z.-W.; Wang, S.-J. Fifty top-cited classic papers in orthopedic elbow surgery: A bibliometric analysis. Int. J. Surg. 2015, 18, 28–33. [Google Scholar] [CrossRef]
  89. Kuo, L.-C.; Polson, A.M.; Kang, T. Associations between periodontal diseases and systemic diseases: A review of the inter-relationships and interactions with diabetes, respiratory diseases, cardiovascular diseases and osteoporosis. Public Health 2008, 122, 417–433. [Google Scholar] [CrossRef]
  90. Mattila, K.J.; Nieminen, M.S.; Valtonen, V.V.; Rasi, V.P.; Kesäniemi, Y.A.; Syrjälä, S.L.; Jungell, P.S.; Isoluoma, M.; Hietaniemi, K.; Jokinen, M.J. Association between dental health and acute myocardial infarction. BMJ 1989, 298, 779–781. [Google Scholar] [CrossRef][Green Version]
  91. Association, A.H. Heart disease and stroke statistics—2006 update. Circulation 2005, 113, e85–e151. [Google Scholar]
  92. Mokdad, A.H.; Ford, E.S.; Bowman, B.A.; Nelson, D.E.; Engelgau, M.M.; Vinicor, F.; Marks, J.S. Diabetes trends in the US: 1990–1998. Diabetes Care 2000, 23, 1278–1283. [Google Scholar] [CrossRef] [PubMed][Green Version]
  93. Soskolne, W.A.; Klinger, A. The Relationship between Periodontal Diseases and Diabetes: An Overview. Ann. Periodontol. 2001, 6, 91–98. [Google Scholar] [CrossRef] [PubMed]
  94. Moher, D.; Liberati, A.; Tetzlaff, J.; Altman, D.G. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLOS Med. 2009, 151, 264–269. [Google Scholar]
  95. Swingler, G.H.; Volmink, J.; Ioannidis, J.P.A. Number of published systematic reviews and global burden of disease: Database analysis. BMJ 2003, 327, 1083–1084. [Google Scholar] [CrossRef] [PubMed][Green Version]
  96. Zhao, X.; Guo, L.; Lin, Y.; Wang, H.; Gu, C.; Zhao, L.; Tong, X. The top 100 most cited scientific reports focused on diabetes research. Acta Diabetol. 2015, 53, 13–26. [Google Scholar] [CrossRef] [PubMed]
  97. Zhang, Y.; Huang, J.; Du, L. The top-cited systematic reviews/meta-analyses in tuberculosis research. Medicine 2017, 96, e4822. [Google Scholar] [CrossRef]
  98. Collin, H.-L.; Uusitupa, M.; Niskanen, L.; Kontturi-Närhi, V.; Markkanen, H.; Koivisto, A.-M.; Meurman, J.H. Periodontal Findings in Elderly Patients with Non-Insulin Dependent Diabetes Mellitus. J. Periodontol. 1998, 69, 962–966. [Google Scholar] [CrossRef]
  99. Garcia, R.I.; Nunn, M.; Vokonas, P.S. Epidemiologic Associations Between Periodontal Disease and Chronic Obstructive Pulmonary Disease. Ann. Periodontol. 2001, 6, 71–77. [Google Scholar] [CrossRef]
  100. Page, R.C. Periodontitis and Respiratory Diseases: Discussion, Conclusions, and Recommendations. Ann. Periodontol. 2001, 6, 87–90. [Google Scholar] [CrossRef]
  101. Tonetti, M.S.; D’Aiuto, F.; Nibali, L.; Donald, A.; Storry, C.; Parkar, M.; Suvan, J.; Hingorani, A.D.; Vallance, P.; Deanfield, J.E. Treatment of Periodontitis and Endothelial Function. N. Engl. J. Med. 2007, 356, 911–920. [Google Scholar] [CrossRef] [PubMed][Green Version]
  102. Wactawski-Wende, J.; Grossi, S.G.; Trevisan, M.; Genco, R.J.; Tezal, M.; Dunford, R.G.; Ho, A.W.; Hausmann, E.; Hreshchyshyn, M.M. The Role of Osteopenia in Oral Bone Loss and Periodontal Disease. J. Periodontol. 1996, 67, 1076–1084. [Google Scholar] [CrossRef] [PubMed]
  103. Tezal, M.; Wactawski-Wende, J.; Grossi, S.G.; Ho, A.W.; Dunford, R.; Genco, R.J. The Relationship between Bone Mineral Density and Periodontitis in Postmenopausal Women. J. Periodontol. 2000, 71, 1492–1498. [Google Scholar] [CrossRef] [PubMed]
  104. Hirai, T.; Ishijima, T.; Hashikawa, Y.; Yajima, T. Osteoporosis and reduction of residual ridge in edentulous patients. J. Prosthet. Dent. 1993, 69, 49–56. [Google Scholar] [CrossRef]
  105. Li, H.; Zhao, X.; Zheng, P.; Hu, M.; Lu, Y.; Jia, F.; Tong, X. Classic Citations in Main Primary Health Care Journals. Medicine 2015, 94, e2219. [Google Scholar] [CrossRef]
  106. Rychetnik, L.; Hawe, P.; Waters, E.; Barratt, A.; Frommer, M. A glossary for evidence based public health. J. Epidemiol. Commun. Health 2004, 58, 538–545. [Google Scholar] [CrossRef][Green Version]
  107. Van Eck, N.J.; Waltman, L. Software survey: VOSviewer, a computer program for bibliometric mapping. Scientometrics 2009, 84, 523–538. [Google Scholar] [CrossRef][Green Version]
Figure 1. Association of (A) citation count and (B) citation density with age of publication.
Figure 1. Association of (A) citation count and (B) citation density with age of publication.
Molecules 25 04508 g001
Figure 2. Citation analysis of the top 100 most-cited articles over the (A) years and (B) decades.
Figure 2. Citation analysis of the top 100 most-cited articles over the (A) years and (B) decades.
Molecules 25 04508 g002
Figure 3. Citation analysis of the authors who contributed to the top 100 most-cited articles.
Figure 3. Citation analysis of the authors who contributed to the top 100 most-cited articles.
Molecules 25 04508 g003
Figure 4. The distribution of the keywords over (A) 1960s, (B) 1980s, (C) 1990s, (D) 2000s, and (E) 2010s. The size of the node represents the frequency of the keyword used.
Figure 4. The distribution of the keywords over (A) 1960s, (B) 1980s, (C) 1990s, (D) 2000s, and (E) 2010s. The size of the node represents the frequency of the keyword used.
Molecules 25 04508 g004aMolecules 25 04508 g004b
Table 1. List of contributing countries and institutions to the most-cited publications.
Table 1. List of contributing countries and institutions to the most-cited publications.
Name of CountryNo. of Publication
United States of America61
United Kingdom9
Netherlands 3
Chile 3
Australia 3
Germany 3
Finland 3
Sweden 2
Spain 2
Brazil 2
Denmark 1
New Zealand 1
Italy 1
Turkey 1
Canada 1
Japan 1
Austria 1
Israel 1
Name of Institution
School of Dental Medicine, University at Buffalo, USA13
School of Dentistry, University of North Carolina at Chapel Hill, USA9
College of Dental Medicine, Columbia University, USA6
School of Dentistry, University of Michigan, USA4
National Institute of Dental Research, National Institutes of Health, USA3
Academic Center for Dentistry Amsterdam (ACTA), The Netherlands3
Eastman Dental Institute and Hospital, University College London, UK3
Faculty of Dentistry, University of Chile, Chile 3
Table 2. List of journals that published the top 100 “classic” articles.
Table 2. List of journals that published the top 100 “classic” articles.
Journals (Abbreviation)Impact Factor *Journal Age (Years)Number of ArticlesTotal CitationMedian Citation
J. Periodontol.3.74288258011251
Ann. Periodontol.-23112753240
J. Clin. Periodontol.5.2414581597178.5
J. Dent. Res.4.91410071592205
Arterioscler. Thromb. Vasc. Biol.6.604384974258.5
Acta Odontol. Scand.1.57380384094053
Diabetes Care16.0194131082233
Am. Heart J.4.153943728195
Arch. Intern. Med.17.333 **1113664197
J. Am. Dent. Assoc.2.8031053635204
Oral Dis.2.613242462231
Arthritis Rheumatol.9.586612401200.5
Alzheimers. Dement.17.127141174174
Am. J. Epidemiol.4.526801206206
Clin. Microbiol. Infect.7.117231332332
Community Dent. Oral Epidemiol.2.135461258258
Eur. Heart J.22.673391168168
Int. Immunopharmacol.3.943181164164
J. Am. Coll. Cardiol.20.589361194194
J. Cardiovasc. Risk2.548 ***-1198198
J. Gen. Intern. Med.4.597331365365
J. Periodont. Res.2.926531172172
J. Rheumatol.3.350451200200
Lancet. Oncol.33.752191169169
Nat. Rev. Endocrinol.28.800141338338
Nat. Rev. Immunol.40.358181574574
Oral Health Prev. Dent.0.920161176176
Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod.1.457 #581295295
Periodontol. 20007.718261186186
N. Eng. J. Med.74.6991071731731
* Journal Citation Report, 2019; ** Journal Citation Report, 2014, *** Journal Citation Report, 2005; # Journal Citation Report, 2011.
Table 3. Distribution of topics and methodological designs of the 100 most-cited articles.
Table 3. Distribution of topics and methodological designs of the 100 most-cited articles.
TopicNo. of ArticleCitation CountAverage Citation CountMedian Citation
Cardiovascular diseases318598277.35217
Diabetes mellitus297660264.13229
Collective systemic manifestations143918279.85234.5
Pregnancy-related diseases1110909991.72319
Rheumatic diseases101955195.5187
Cerebrovascular diseases2478239239
Respiratory diseases2399199.5199.5
Study design
Clinical trial 2815788574.85249
Literature review266606254.08194
Randomized controlled trial 113566247.84179
Case-control study71695217.87204
Systematic review61504253.83237
Systematic review & meta-analysis3792297.75320
Animal study3630210.66173
Consensus report 2600303.50303.50

Share and Cite

MDPI and ACS Style

Ahmad, P.; Arshad, A.I.; Della Bella, E.; Khurshid, Z.; Stoddart, M. Systemic Manifestations of the Periodontal Disease: A Bibliometric Review. Molecules 2020, 25, 4508.

AMA Style

Ahmad P, Arshad AI, Della Bella E, Khurshid Z, Stoddart M. Systemic Manifestations of the Periodontal Disease: A Bibliometric Review. Molecules. 2020; 25(19):4508.

Chicago/Turabian Style

Ahmad, Paras, Anas Imran Arshad, Elena Della Bella, Zohaib Khurshid, and Martin Stoddart. 2020. "Systemic Manifestations of the Periodontal Disease: A Bibliometric Review" Molecules 25, no. 19: 4508.

Article Metrics

Back to TopTop