Endodontic Microbiology: A Bibliometric Analysis of the Top 50 Classics

Background Citation analysis has emerged to play a significant role in recognition of the most useful areas of research. Endodontic microbiology has been a topic of interest for endodontists as well as periodontists and oral surgeons. This bibliometric analysis is aimed at identifying and reporting the characteristics of the top 50 cited articles on endodontic microbiology. Methods The articles were identified through a search on Web of Science (WoS), property of Clarivate Analytics database published on endodontic microbiology. The citation information of the selected articles was recorded. The Journal of Endodontics, International Endodontic Journal, Oral Surgery Oral Medicine Oral Pathology Oral Radiology and Endodontology, Dental Traumatology, and Australian Endodontic Journal were searched in the search title. Descriptive and bivariate analyses were performed using a statistical software package SPSS. Statistical analysis was performed using Shapiro-Wilk, Kruskal-Wallis, Post hoc, Mann-Kendall trend, and Spearman-rank tests. Results The 50 most cited articles were published from 1965 to 2012 with citation count varying from 1065 to 103 times. The total citation counts of articles recorded were 11,525 (WoS), 12,602 (Elseviers' Scopus), and 28,871 (Google Scholar). The most prolific years in terms of publications were 2001, 2002, and 2003, with five publications each, followed by 2005 with four. The year with most citations was 1998, with 1,330 citations, followed by 1965 and 2001, with 1,065 and 1,015 citations, respectively. A total of 136 authors contributed to the top 50 most cited articles with 27 corresponding institutions from 12 different countries. The most common methodological design was in vitro study, followed by clinic-laboratory study, literature review, systematic review and meta-analysis, and animal study. Conclusions The present study provided a detailed list of the top 50 most cited and classic articles on microbiology in endodontics. This will help researchers, students, and clinicians in the field of endodontics as an impressive source of information.


Introduction
Endodontic microbiology is a vast, interesting, and widely explored area of dentistry [1][2][3][4]. The pulpal and periradicular infections are mediated by the formation of biofilm [5]. This biofilm is located in areas that are inaccessible to mechanical cleansing of the root canal system. If these pathogenic microbes persist and are not appropriately removed [2,4,5], there is a high chance of postendodontic treatment failure [6,7]. It has been suggested that every endodontic infection is polymicrobial, i.e., it is a collective outcome of multiple microbes which leads to pathogenesis [8]. Hence, understanding the nature of this polymicrobial infection is very important to ensure its removal and success of endodontic treatment.
In this advancing era of digital libraries and the availability of diverse research materials in the fields of dentistry from different parts of the world, citation analysis has emerged to play a significant role in recognition of the most useful areas of research. Endodontic microbiology has been a topic of interest not only for endodontists but also for periodontists and oral surgeons. It is a field that requires a multidisciplinary approach, involving contributions from different parts of the world and by authors of different origins and institutions. Hence, a bibliometric analysis makes it easier for students, budding researchers, or academicians to identify the articles that are most commendable in their field of interest [9]. This analysis not only provides information on the most cited articles but also helps in retrieving highly impactful research in the related field [10]. The first article on endodontic microbiology first appeared in the month of September 1965 in PubMed, followed by in the year 1987, 1989, 1990 to 1997, and so on.
Classics have been defined differently by multiple authors. The founder of the institution of Scientific Information (ISI), Dr. Eugene Garfield, poised the term "citation classics." The purpose of this was to help acknowledge the frequently cited and peer-reviewed research [11]. A study conducted by researchers evaluated the bibliometrics' predictive ability to calculate the citation rate [12]. A work was referred to as a classic in some fields if it was cited more than 100 times [13][14][15], while in others it was mandatory to receive 400 citations and above to achieve the title of being called a classic [3]. In the last decade, citation analysis has become a very common tool of interest in both the fields of medicine [16][17][18] and dentistry [3,13,[19][20][21][22][23][24]. However, to the best of our knowledge, citation analysis of the top 50 most cited classic articles in endodontic microbiology has not been carried out. This article is aimed at identifying and analysing the top 50 most cited classic articles in the field of endodontic microbiology.

Search Methodology and Data
Source. The Web of Science (WoS), property of Clarivate Analytics database, was utilized to retrieve the data on articles published on microbiology in endodontics and their citation information. The data search was performed using (https://www.webofknowledge .com) all database on 1st of July 2020; the top journals in endodontics, Journal of Endodontics; International Endodontic Journal; Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontology; Dental Traumatology; and Australian Endodontic Journal, were searched in the search title. There was no restriction in the search regarding the publication year and the design of the study.
The top 50 most cited articles were selected and were arranged according to the decreasing number of their citation count. Manual reviewing of the selected articles was performed by the two authors independently by accessing the abstract and full-length if required; any disarrangement between them was solved with the consultation from the third author. The citation count of the top 50 articles was searched and recorded using Elsevier's Scopus (ES) and Google Scholar (GS). The current density of the articles was also calculated by dividing the total number of citations achieved with the number of the years since publication.

Data
Extraction. The article title, article citation count, publication year, study design, financial support, name of first author and coauthors, country of origin, corresponding institution, and the keywords of the top 50 most cited articles were recorded. The country of origin and the institute of articles were determined by the address published as correspondence and reprints.
(1) Five-Year Journal Impact Factor. This indicator represents the citation counts received by a journal, in one year, of the citable papers published in the last 5 years. Its calculation follows the following formula: citations from journal citation report (JCR) year of documents published in the last 5 years divided by the total number of citable documents [25] (2) CiteScore (CS). This is a newly introduced indicator adopted to assess the impact of journals so that more rigorous results can be obtained. Its calculation follows the following formula: the ratio of citation counts from all items in 1 year to all items published over the past 3 years for a journal [25,26] (3) Eigenfactor Score (ES). This is regarded as an indicator of the global repercussions or impact of documents published online in JCR. Its calculation is based on the citation counts of items published in the past 5 years in the JCR per annum. It also takes into account which journals have contributed to these citations, so that highly cited journals will impact the network greater than lesser cited journals; references from one paper to another paper from the same journal are eliminated, so that ES is not biased by journal self-citation [25,26] [27] was used to create collaboration network maps regarding the cooccurrences of all keywords. Statistical analysis was performed using software package, i.e., IBM SPSS Statistics version 24.0 (IBM, Chicago, IL). Shapiro-Wilk test was used to assess the normality of the data; based on normality and distribution of data, the mean standard deviation was calculated. The Kruskal-Wallis test was performed to assess the median differences between the independent groups. Post hoc testing was conducted to evaluate the median differences within each group. The Mann-Kendall trend test was performed to investigate any increase or decrease in the time-dependent trends. The correlation between the age of the journal and the publication count of the journal were evaluated using the Spearman-rank test. The p < 0:05 value was considered statistically significant.  [28] and was published in the Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontology. Its citation density (CD) was 19.72, with the current citation index (CCI) of 41. The second most cited article, with a total of 791 (WoS), 839 (ES), and 1883 (GS) citations, was titled "Microbiologic Analysis of Teeth with Failed Endodontic Treatment and the Outcome of Conservative Re-treatment" [29] and also was published in the Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontology. Its CD was 37.67, with the CCI of 26. The third most cited article, with a total of 539 (WoS), 576 (ES), and 1269 (GS) citations, was titled "Microbiological Status of Root-Filled Teeth with Apical Periodontitis" [30] and was published in the International Endodontic Journal. Its CD was 25.67, with the CCI of 14. According to the CCI 2019, the top-ranked article was the literature review published in 2008, securing 321 citations [31]. As per CD, the clinic-laboratory study by Sundqvist et al. [29] has the highest score, i.e., 37.67.

Results
The age of the article has shown a nonsignificant relation towards the higher citation count (r = 0:011, p = 0:840) (Figure 1(a)). Further, a significant negative trend towards an increased citation density was observed (r = −0:482, p < 0:05) (Figure 1(b)). According to the Shapiro-Wilk test, the distribution of data regarding citation count, citation density, and article age was not normal (p < 0:05).
The number of "classic" articles published in that journal has shown a statistically significant trend (p < 0:01) in relation with the age of the journal. Though, a statistically nonsignificant trend (p = 0:348) was observed in relation with the impact factor of the journal. According to the simple linear regression analysis, a statistically significant association was observed between self-citation (p = 0:041), CiteScore    (Table 3).

Evidence Level.
Out of the total five evidence levels (ELs) [33], the top 50 most cited publications could primarily be classified into three ELs. Most of the articles were within evidence level V (n = 35), followed by EL III (n = 14) and EL I (n = 1). Among these ELs, the total citation counts (r = −0:2310, p = 0:076) and the citation density (r = 0:122, p = 0:436) did not vary significantly.

Discussion
The researchers and nonresearchers, like science journalists from various disciplines, are interested in knowing the milestone publications in their specialized field. This study was conducted to identify and characterise the top 50 most cited articles on the topic of endodontic microbiology published in endodontic journals. The oldest and the most recent articles were from the years 1965 and 2012, respectively. With international recognition and scientific outcomes in the specialized field, it is evident that both the article and the journal have contributed to the specialization [34]. A research article that has obtained the most frequent citation in its area of research is considered to have achieved a milestone in the field of scientific research [20]. Garfield states that an article which has secured 100 or more citations in the field of research could be considered as a classic article, depending on the speciality of research [35]. The articles included in the present study were cited more than 100 times. Hence, the top 50 articles are the classic articles in the field of endodontic microbiology. The top 50 articles were cited between 103 and 1065 times and evaluated using the WoS all database as a benchmark. The WoS record suggests that less than 10% of its scientific articles remain uncited, probably even much less than that, because uncited articles in the database might have been cited by someone somewhere [36]. The WoS all database measures the scientific articles using an extensive period from 1945 to date. Contrastingly, Scopus and Google Scholar revealed fluctuations in the citation count. Scopus measures the citations starting from 1996, which is a severe flaw when evaluating the most cited articles, and Google Scholar covers all thesis, dissertation, reports, preprints, conference, and books which affects the scientific article counts in journals [37].
Publication year acts as an important factor with the citation count of an article; the citation of a scientific publication mostly follows a time-lapse. It is usually not cited until 1-2 years after the publication, reaching a peak in 3-10 years and then drops [38]. The older articles get ample time to be recognized, will be at a higher chance of getting cited when compared with the recently published ones [9,13]. Hence, the recently published articles despite having a significant finding could not be identified. Furthermore, such studies achieve fewer citations, and the contribution has not been recognized universally. This could be the reason why the recently published articles have not been identified in the top 50 articles, and it is known as "obliteration by incorporation" effect [39]; hence, citation density of each article was calculated to overcome this bias. This study revealed that the first three most cited articles were published in the years 1965 to 1998, and most articles were from 2001, 2002, and 2003 contributing to 5 articles from each year. The differences in the publication rate in the years 2001 to 2003 may be due to the advancement in materials and techniques promoting research and scientific growth. One of the important feature of this study was the presence of two studies among the top 50 articles which were published in the last 10 years, i.e., 2012 and 2010 [32,40]; this highlights the quality of the research and its relevance to the microbiology in endodontics with clinical implementation.
The findings of this study are in accordance with other bibliometric analyses performed within dentistry, suggesting that the institutes from the United States of America (USA) were involved in the top 50 most cited articles [3,14,37,[41][42][43]. The huge financial resources and the presence of a big scientific population and its active researcher community clarify the chief contribution of the USA [44]. It is important to mention that 24 articles are from European countries which are identified in the top 50 as international collaboration. In respect to research articles by the institution, Sweden, Switzerland, and Brazil with 5 articles, each was top on the list. Whereas research papers compared by individual authors, Siqueira Jr JF from Brazil was top on the list. A single article from Asian countries was identified and no contribution from African and Middle Eastern countries. Worldwide publication activity shows that the countries having low to middle income have a lower level of scientific articles published in high impact factor medical journals [45]. This could be due to difficulties in research and education, healthcare systems, limitations in achieving publications, lack of access to the information, and language barrier. Hence, further concern and research related to the microbiology in endodontics in the developing countries of the world is needed.
The journals' ranking based on their impact factor has become an important factor to consider when authors decide where to submit their research. The impact factor is corrupted as a proxy for the quality of individual publications [12]. Usually, authors target journals with the highest impact factor instead of journals having the best readers for their      BioMed Research International article [12]. Using bibliometric analysis to evaluate scientific evidence is a complex task; therefore, ranking journals using a single index would yield inaccurate results. Scientific publications must be evaluated keeping the impact factor aside. Impact factors can be misleading at times as general dentistry journals can have a much higher impact compared to their specialized counterparts. ES is becoming increasingly valuable as it focusses on the importance of specific papers, but there is dependence to a great extent on citation count which is a major limitation. Other bibliometric indexes are less predictable as they do not consider the quality of the evidence published [12].
The study design is linked to the contribution of the research, which marks the level of evidence. Depending on evidence-based practice, and the research design hierarchy suggests that the importance is given to the high graded stud-ies like a systematic review, cohort studies, and randomized clinical trials [46]. In this analysis, the majority of the articles were on original research (both in vivo and in vitro studies) followed by narrated reviews and only one systematic review and meta-analysis [47]. The review articles in the list indicate that the researchers inclined towards gathering the existing research information and data in the field of microbiology in endodontics to provide benefits to the readers. The present study did not identify any randomized clinical trial (RCT). A study conducted by Crumley et al. (2005) revealed the most common reasons RCT or controlled clinical trial articles were missed in the electronic search were due to inadequate or inappropriate indexing. Additionally, why articles were not recognized in a database, includes they were published as reports, letters, books, book reviews, supplements, etc., or authors did not report keywords or methodology in the manuscript, and articles were missing from resources [48].
Keywords are an important component of a research article; on conducting a literature search, the use of keyword retrieves the more relevant results when compared with the use of sentences or phrases. The keywords act as code to source the required scientific articles [49]. The most used keywords were smear layer, root canal therapy, Enterococcus faecalis, endodontic re-treatment, endodontic failure, microbiology, and root canal infection. Several articles in this study did not contain the keywords. The literature suggests that the authors submitted the manuscript to the database with the keywords, but the published articles did not display [9]. The purpose of identifying the keywords is that it will guide and assist the researchers in searching for scientific papers

Limitations
The limitation of this study was that the search was confined to the endodontic category of the WoS database. Studies on microbiology in endodontics can be published in nonendodontic journals focusing on microbiology and smear layer. Citation analysis is a fair technique for scientific article recognition. However, it does not consider the self-citation and negative citations [50]. This study includes only the top 50 articles due to the time limitation, which resulted in the exclusion of many articles from the list of classic articles. Hence, the top 50 articles which achieved the maximum citation were included in this study. The most recently published articles are at a disadvantage, regardless of the quality and the content of the paper as they were out of time criteria consideration. Future studies can be planned to use a broader category to include both endodontic and nonendodontic journals for inclusion of more articles.

Conclusion
The present study provided a detailed list of the top 50 most cited and classic articles on microbiology in endodontics. This will help researchers, students, and clinicians in the field of endodontics as an impressive source of information. The citation analysis provides the quantitative analysis of the scientific articles but not the quality or the important content of the article.

Data Availability
The data used to support the findings of this study are available from the corresponding author upon request.