Esophageal motility disorders are a large group of pathologic conditions that involve both primary and secondary disorders of esophageal contraction (1). Motility disorders are considered to be primary if symptoms, such as dysphagia and chest pain, originate from the esophagus, and no other cause can be identified (1). The main primary conditions are achalasia, diffuse (distal) esophageal spasm, nutcracker esophagus, and hypertensive lower esophageal sphincter (1). The evaluation of esophageal motility disorders is mainly based on the use of manometry, and their classification is made according to the Chicago Classification system, which utilizes high-resolution manometry (HRM) (2). Although there is a fair amount of evidence for some of these disorders, such as achalasia, the data on others is not as granular.
Bibliometric citation analysis is a quantitative method that uses the number of citations received by scientific articles to develop citation ranking lists, in order to assess the quality and scientific impact of those articles (3). A publication receives a citation when another peer-reviewed publication references it. By establishing citation ranking lists, we can identify the most influential articles on a specific topic or scientific discipline and their impact on clinical practice. Bibliometric analysis can also provide insight into how our understanding of those topics or disciplines has evolved over the years (3).
In recent years, bibliometric citation analysis has been used to identify the most influential articles in various medical disciplines and specialties, such as plastic (4), orthopaedic (5), general (6), and emergency general surgery (7) as well as oncology (8). To date, the only bibliometric analysis in the field of esophageal diseases is on the topic of esophageal cancer (9). The purpose of this study is to determine which articles are the most cited and, therefore, influential on the subject of esophageal motility disorders and to examine how our understanding of these diseases has changed over time. It also aims to serve as a concise reference for the most cited papers on the subject.
The Web of Science citation indexing database and research platform of Clarivate Analytics was used to perform the study. The search strategy was to identify articles that contained specific search terms/keywords in their title, abstract or topic. After independent trial searches by two authors (P Kapsampelis, D Schizas), the following keywords were agreed upon and used in the final search: (esophag* OR oesophag*) AND (achalasia OR motility OR dysmotility OR spasm OR peristal* OR hypercontract* OR nutcracker OR hypertens* OR hypotens* OR sphincter* OR contraction* OR manometry OR dysphagia OR obstruction). The search was set to include results from all the databases within the Web of Science and all available years [1900–2018]. Also, it was set to include articles written only in the English language. The final search date was August 15th, 2018. This strategy is a modified version of the method initially developed by Paladugu and colleagues (6).
The returned results were sorted by the total number of citations, in descending order, and reviewed for inclusion, with the article with the most citations examined first. Papers focusing on esophageal motility disorders as their main topic and written in the English language were included. The exclusion criteria were: (I) articles written in any language other than English; (II) articles irrelevant to the subject; or (III) articles focusing on broader topics, such as esophageal and gastrointestinal diseases in general, without giving specific emphasis to esophageal motility disorders.
Initially, two reviewers (P Kapsampelis, D Schizas) independently assessed abstracts for inclusion. Consequently, the two lists were compared and full manuscripts of articles were reviewed, when deemed necessary. After conflicts were resolved by a third author (DI Tsilimigras) and the list of 100 most cited papers was finalized, the full manuscripts of included papers were analyzed to extract the data of interest.
The 100 most cited articles were analyzed for title, names of first author and co-authors, institution and country of the first author, year of publication, total number of citations and citation rate. The ranking within the 100 most cited papers list was also recorded. The purpose of calculating the citation rate was to control for historical publication bias since older articles can accumulate more citations over time. In a method described by Powell et al. (10), the citation rate is calculated by dividing a publication’s number of citations by the number of years since its publication. Also, in the case of articles with same citation numbers, the ranking was done according to the citation rate and articles that received the same number of citations in a shorter period of time were ranked higher.
The Web of Science search returned 29,521 full-length, English language papers. Table 1 lists the 100 most cited papers. The total cumulative number of citations received by the top 100 articles was 20,688. The article with the highest number of citations was “Peroral endoscopic myotomy (POEM) for esophageal achalasia” by Inoue et al., receiving 665 citations (11).
The oldest manuscript featured in the top 100 list was by Merendino et al. (“The concept of sphincter substitution by an interposed jejunal segment for anatomic and physiologic abnormalities at the esophagogastric junction”) and published in 1955 (48). “The Chicago classification of esophageal motility disorders, version 3.0” by Kahrilas et al. and “Per-oral endoscopic myotomy: a series of 500 patients” by Inoue et al. (17,108) were the most recent manuscripts, both published in 2015. Table 2 lists the number of articles from the top 100 list published in each decade.
To address the issue of historical bias, we calculated the citation rate of the manuscripts in the top 100 list. Table 3 shows the top 10 papers with the highest citation rate. “The Chicago classification of esophageal motility disorders, version 3.0” by Kahrilas et al., published in 2015, was the article with the highest citation rate (13,067 citations per year) (17).
The 100 most influential papers appeared in 26 journals (Table 4). The number of manuscripts per journal ranged from 1 to 32. The journal Gastroenterology featured the highest number of papers and accrued the highest total number of citations (32 articles and 6,675 citations respectively). Following that, Annals of Surgery had 12 manuscripts and 2,444 total citations and Gut had 10 manuscripts and 2,076 total citations. Endoscopy published the most cited paper in the top 100 list [“Peroral endoscopic myotomy (POEM) for esophageal achalasia” by Inoue et al.] (11).
The United States of America was the country that produced most publications, with 66 out of 100 articles, followed by Italy with 8 publications (Table 5). Belgium, Australia, and Germany had 4 publications each. Most manuscripts in the top 100 list originated from Northwestern University (13 manuscripts) (Table 6). Northwestern University was also the institution that accrued the highest total number of citations (3,238 citations). Showa University Northern Yokohama Hospital in Japan produced the most cited manuscript in the top 100 list [“Peroral endoscopic myotomy (POEM) for esophageal achalasia” by Inoue et al.] (11).
Table 7 lists all the authors that contributed to more than one manuscript, either as the 1st authors or as co-authors. Out of a total of 367 authors, 81 participated in the authorship of more than one publications featured in the top 100 list. Peter Kahrilas from Northwestern University was the most cited author (3,650 total citations), followed by Joel Richter from the University of South Florida (2,815 citations). Peter Kahrilas had 6 articles as the 1st author and 8 articles as co-author. Joel Richter had 4 articles as the 1st author and 10 articles as co-author.
This bibliometric analysis is the first of its kind to study the most cited papers on the topic of esophageal motility disorders. The article with the highest total number of citations and second highest citation rate is the one entitled “Peroral endoscopic myotomy (POEM) for esophageal achalasia” and was performed by Inoue et al. from Showa University Northern Yokohama Hospital in Japan (11). This article was the first description of POEM, a technique developed by Inoue and his colleagues to treat esophageal achalasia with the use of endoscopic surgery. Their short-term outcomes were excellent opening the way towards less invasive permanent treatment methods for esophageal achalasia (11). This technique was widely accepted as an alternative to surgical myotomy, and some years later, Inoue et al. published a large series of 500 patients who underwent POEM at their institution confirming the safety and efficacy of this approach (108). The second most cited article is “Esophageal peristaltic dysfunction in peptic esophagitis” by Kahrilas et al. from the Northwestern University (12). In this article, the authors examined the association of reflux esophagitis with esophageal motility, reporting an increasing prevalence of peristaltic dysfunction with worsening esophagitis (12). In fact, abnormal peristalsis was identified in 25% of patients with mild esophagitis and 48% of patients with severe esophagitis (12). This was one of the first studies to show the association between the reflux of gastric acid and the disturbances in esophageal peristalsis, thus attracting much attention mainly due to the significant clinical implications of these findings (12).
Most papers in the top 100 list were published in more recent decades. Seventy  out of the 100 papers were published after 1990 and 57 of them were published between 1991–2010 (Table 2). Possible explanations for this trend could be the increased use of manometry in evaluating esophageal motility, as well as the introduction of novel therapeutic approaches, mainly for the treatment of achalasia.
Also, manuscripts published in recent years had generally higher citation rates and this may imply that these will accrue more citations and become even more influential within the next years (Table 2). The citation rate index for the most influential articles on esophageal motility disorders ranged from 34.17 to 130.67 (Table 3). The comparison with the citation rate index of other subjects shows that esophageal motility disorders accrue citations at a slower rate. For example, in a bibliometric analysis of the most influential papers on esophageal cancer by Powell et al., the citation rate index ranged from 69 to 227 (9). “The Chicago classification of esophageal motility disorders, version 3.0” by Kahrilas et al. is the article with the highest citation rate and was published in 2015 (17). The Chicago Classification system uses HRM to categorize esophageal motility disorders and all versions of this system are featured in the top 100 list.
The majority of manuscripts were published in the journal Gastroenterology, followed by Annals of Surgery and Gut. Most manuscripts were published in journals in the field of gastroenterology (56 articles), as opposed to manuscripts published in surgery journals (21) and general and internal medicine journals (12). Accordingly, the majority of the manuscripts with the highest number of citations or the highest citation rate were published in gastroenterology journals (Tables 1,3).
Out of the 367 authors, 12 had more than 1,000 citations and only 4 had more than 2,000 citations. The most cited author was Peter Kahrilas from Northwestern University, followed by Joel Richter from the University of South Florida. The third and fourth most cited authors were Donald Castell from the Medical University of South Carolina and John Pandolfino from Northwestern University. These four authors were also the most published ones in terms of publication volume. Kahrilas and Richter authored 14 manuscripts each, whereas Castell and Pandolfino authored 10 manuscripts each.
The main limitation of this study is that some types of bias might have impacted the results. Self-citation, powerful person bias, institutional bias or geographical bias may have caused disproportionate number of citations. Language bias may also be present, mainly because the search was limited to manuscripts only in the English language. Another issue that has to be taken into consideration is the possibility of historical bias; older publications often have a higher number of citations because they accumulated citations over many years, regardless of their scientific impact. We tried to address this issue by calculating the citation rate of the articles, in addition to their citation number. Nevertheless, the scientific impact of an article may be underestimated or overestimated with this study format. On the one hand, articles need a certain lead-time to start receiving citations. On the other hand, the likelihood of receiving citations rises with the increasing numbers of articles being published in peer-reviewed journals.
This citation analysis is the first to examine the most cited papers on the disorders of esophageal motility and can serve as a reference on the manuscripts, authors, and institutions that defined our understanding of the subject. Researchers and clinicians can also use this analysis to examine what are the key characteristics of citable articles. Finally, by studying the most impactful papers, researchers can determine the future directions in the research on esophageal motility disorders.
Conflicts of Interest: The authors have no conflicts of interest to declare.
Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.
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