Bibliometric review of journal articles on pancreatic cancer: insights into productivity and impact

Introduction

Pancreatic cancer is characterized by its high aggressiveness and ranks as the fourth foremost cause of cancer-associated mortality in the United States (1). Although pancreatic malignancies have been a highly stressed field of research, the advances in improving its outcomes are yet limited, and extensive research efforts have been made to enhance the current treatment strategies available.

In the last three decades, a rapid increase in medical journals and publications has occurred. Still, a significant knowledge gap exists concerning the most preeminent publishers of articles about pancreatic cancer, as well as the journals that showcase the most impactful contributions in this domain. While ongoing debates persist regarding the significance of citation rates, they persist as the principal determinant employed to assess the influence of published literature (1,2). The frequency with which an article is cited assumes paramount importance, serving as a crucial metric to evaluate the caliber and productivity of scholarly endeavors. Institutions can harness this parameter to effectively allocate research funding, recalibrate research support mechanisms, and regulate or invigorate research activities within specific fields (3,4). Furthermore, researchers investigating pancreatic cancer face a scarcity of objective data to guide their selection of the most suitable journal for manuscript submission. Many factors may influence author selection, such as article processing charges, impact factors, and time to accept or deny. This research endeavor aims to address these inquiries, offering valuable insights to authors and consumers of published literature within the realm of pancreatic cancer.

Bibliometric review is highly regarded as indispensable instruments in facilitating decision-making processes concerning the determination of research priorities, tracking the advancements of scientific endeavors, and acknowledging scientific excellence, among other uses. Originally stemming from the domain of information and library science, these techniques have rapidly broadened their scope, surpassing disciplinary confines. This expansion can be attributed to the abundance of extensive data resources and the convenient accessibility to such information. Furthermore, the proliferation of processing and analytical tools, ranging from simple to intricate, has made modern bibliometric analyses attainable for scientists and practitioners of all proficiency levels (5). Several other articles have successfully utilized bibliometric review as a research method to advance their field (1,6). By examining pivotal articles in a field, authors, and journals that publish these articles, a broad overview of the leaders and research deficits that need to be investigated are generated.

Bibliometric indices collected were h-index, impact factor, and eigenfactor. The h-index estimates the impact of research papers published by an author and assesses his productivity in the field. Thus, the h-index of authors publishing in a scientific journal can be measured indirectly by the level of journal visibility by the scientific community and be an indicator of the profile or performance of researchers submitting their work. Additionally, citation analysis is an important tool for predicting the impact of a scientific journal and is considered the standard measure for calculating the impact of each publication. Citations indirectly demonstrate the value of the content to other experts in the field as they add content or references from the citation to build their research articles and gather reliable information.

Pancreatic cancer is characterized by its high aggressiveness and ranks as the fourth foremost cause of cancer-associated mortality in the United States (7). This poses a considerable oncological challenge, primarily attributable to delayed diagnoses, limited therapeutic modalities, and a low overall survival rate of 6% (8,9). Given the intricacy and severity of this disease, conducting a bibliometric review focused on pancreatic cancer research is paramount. Such an investigation can shed light on the current state of scientific exploration in this field, revealing trends identifying knowledge gaps, and areas of active research. By quantitatively assessing research productivity, influential journals, and prominent authors, this study aims to provide a roadmap for researchers and clinicians to strategically direct their efforts to prioritize research directions to enhance understanding and management of pancreatic cancer (6,10). We present this article in accordance with the BIBLIO reporting checklist (available at https://apc.amegroups.com/article/view/10.21037/apc-24-22/rc).

Materials and methods

This study employed a bibliometric analysis to conduct a citation analysis, evaluating journals, articles, and authors. A comprehensive search of the Scopus database was conducted to identify articles related to pancreatic cancer. The search criteria included the keyword “Pancreatic Cancer” within the subject area of “Medicine” (Table 1). The search was limited to articles published in academic journals between January 1989 and December 2022. Systematic reviews and literature reviews were considered as “Review” (Table 2).

Additionally, several document types, including “Letter”, “Note”, “Conference Paper”, “Editorial”, “Short Survey”, “Erratum”, “Articles in Press”, “Book”, “Conference Review”, and “Retracted” were considered as “Article” (Table 3). All of the articles retrieved from the search strategy above were included. This study aimed to analyze the most important trends in the 52,154 articles. Exclusion criteria for this study consisted of articles not available in the English language, and this filter was added during the search strategy in the Scopus database. Three authors participated in the search strategy, article inclusion and table creation (C.W., Z.S., J.A.K).

While there are many metrics used to perform this analysis, the impact factor is one of the more widely used metrics to evaluate specific journals, while the h-index is used to evaluate authors (11,12). The impact factor uses all indexed citations received by a given journal divided by a number of citable articles published by the journal during the census period (13,14). To analyze publication and citation counts, Pivot Tables were employed. Median citation counts per journal were calculated using the MEDIAN function as a derived field within the Pivot Table data model. This approach was utilized to mitigate the impact of highly cited articles, which could skew the average citation count for a specific journal. Consequently, median citation counts provided a more accurate representation of the number of citations for a typical article from each journal. Additionally, the Bibliometrix^© tool was used to identify the most frequent authors, and VOSviewer^© was used to identify keyword co-occurrence clusters. WordCounter^© was used to identify the most common treatment strategies mentioned in the articles’ titles (15,16).

For each journal, first author, and last author, total citation and article counts were obtained using Microsoft^© Excel and the Bibliometrix^© tool. For each journal and each first author, total citation counts and total article counts were obtained. Additionally, the top 10 articles with the highest citation counts were cross-referenced with citation counts from PubMed to ensure the reliability of their performance. Cross-reference was performed by C.W. and was done by searching article names on Google Scholar, subsequently checking citation counts displayed on the author profile related to the searched article and comparing citation counts with the Scopus platform. To assess the reliability of the Scopus search results the overall top 50 articles by citation counts were obtained from Google Scholar (Table 4). Statistical analysis was performed using a Student t-test. Standard deviations, interquartile ranges (IQRs), and normality distributions were performed using the R software for statistical computing (R version 4.0.1).

Results

The search was conducted in July 1, 2023. The search yielded 52,154 articles from 3,155 journals, accounting for 1,903,916 citations. There were 34,367 unique first authors and a total of 388,989 authors. Additionally, there were 1,788 single-authored manuscripts, which represents 3.42% of the total number of manuscripts. Table 5 displays the article’s and review’s most common countries of origin. The three most common sources of publications were the United States, China, and Japan.

Figure 1 shows the number of unique journals that published articles on pancreatic cancer rose from 193 in 1989 to 836 in 2022, representing a 333% increase in the number of journals published on pancreatic cancer. The number of articles published on pancreatic cancer increased from 448 in 1989 to 3,766 in 2022, representing a 741% increase in published articles over 30 years. The number of articles published per journal increased from 2.32 in 1989 to 4.5 in 2022, representing a 94% increase. A total of 17,998 research papers were retrieved from 1998 to 2009. Subsequently, 17,515 research papers were retrieved from 2010 to 2018 and 16,643 from 2018 to 2022.

Figure 1 Distribution of articles and journals over time.

Articles

Our study gathered data from the most cited papers from January 1989 to December 2022 (Table 4). We analyzed the 50 most cited papers in the study timeframe and compiled data from the publishing journals. The median number of citations for the top 50 articles was 1453, with an IQR of 1,000.

The period with the most cited papers being published was 2010 to 2019, with 26 highly cited research papers within the top 50, followed by 2000 to 2009, with 17 highly cited research papers within the top 50. Only six highly cited papers were in the top 50 in the 1989–1999 timeframe, and no papers from 2020 to 2022 were classified in the top 50 most cited articles about pancreatic ductal adenocarcinoma (PDAC). The most frequent journals appearing in our top 50 most cited articles were: New England Journal of Medicine (n=14, 28%), Cancer Cell (n=5, 10%), JAMA (n=4, 8%), Cancer Research (n=4, 8%), Annals of Surgery (n=3, 6%), Journal of Clinical Oncology (n=3, 6%), The Lancet (n=3, 6%). Of the 50 papers, 41 were research articles, and 9 were reviews.

The most cited paper in our cohort is “Safety and activity of anti-PD-L1 antibody in patients with advanced cancer”, with 6,027 citations since 2012. While this article contains information about pancreatic cancer, it is not its main topic. The most cited paper focusing predominantly on pancreatic cancer is “FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer”, published in 2011 and accumulating 5,399 citations.

Our study analyzed trending topics within the articles retrieved in the three-decade period. In this sense, three chemotherapies were the main subject of multiple articles retrieved in our search, “gemcitabine” was the subject of 2,113 articles, while “nab-paclitaxel” was the focus of 324 articles, and “5-fluorouracil” of 290 articles. Nonetheless, surgical treatments were the subject of a large portion of well-cited literature; the keyword “resection” was the topic of 1,857 articles, “pancreaticoduodenectomy” was the subject of 1,267 articles, and “pancreatectomy” was the focus of 1,165 articles. Additionally, we have performed a keyword co-occurrence cluster to identify the most popular keywords associated with the articles encountered in our search strategy (Figure 2). Three main clusters are identified in green, red, and blue. For the green cluster, the major themes surrounded cellular characteristics like “invasion”, “microRNA”, and “cytotoxicity”. The red cluster had diagnostic and therapeutic themes, and the blue cluster had more to do with trials of protocol of drugs like “gemcitabine”, “folfirinox”. Other smaller clusters in purple and blue could also be identified, which surrounded the themes of “incidence”, “risk”, and “antitumor activity”, respectively.

Figure 2 Keyword co-occurrence clusters among included articles.

Journals

The journal with the most articles on pancreatic cancer during the census period was Pancreas, with 1,773 from 1989 to 2022 (Table 6). Of the top 30 journals by article count, Annals of Surgery had the highest median citation count, with 76 (Figure 3). In the realm of medical journals, JAMA attained the top rank in terms of median citation count among journals that published five or more articles during the census period. Notably, this distinguished journal exhibited a remarkable median citation count of 340 for a total of 33 articles published (Table 7).

Figure 3 Relationship between number of articles and median citation counts for top 30 journals in number of publications.

In our investigation, we conducted a comparative analysis of annual article output among specific journals, taking into consideration their respective impact factors from 2022. Our findings revealed that journals with high-impact factors exhibited minimal to negligible growth in the number of published articles over time. However, journals with a more specialized focus, such as Pancreas, demonstrated a consistent rise in annual article publication, while journals like Cancers demonstrated a prominent and rapid escalation in article productivity (Figure 4).

Figure 4 Publication trends in select journals over the years.

In the initial period from 1989 to 2002, Pancreas emerged as the foremost publication, displaying the highest volume of articles. It was closely followed by Hepato-Gastroenterology and Cancer Research in terms of article output (Figure 5). Moving forward to the subsequent period from 2003 to 2012, the journal Pancreas maintained the lead, surpassing others by publishing the greatest number of articles (Figure 6). In the most recent decade, covering the years from 2013 to 2022, Cancers published 765 articles and was the leading journal in terms of article output. It was succeeded by Oncotarget, which displayed a considerable publication volume 764, then Pancreas 705 (Figure 7). These data suggest that there has been increased research and interest related to pancreatic cancer over the past 30+ years, with a corresponding overall increase in the articles focusing on pancreatic cancer in individual journals. This increase is likely attributed to the increase in specialized journals.

Figure 5 Top 10 journals with the highest article count across three time periods: 1989–2002.

Figure 6 Top 10 journals with the highest article count across three time periods: 2003–2012.

Figure 7 Top 10 journals with the highest article count across three time periods: 2013–2022.

Authors

The top 10 ranked authors in total number of publications as first and senior authors combined were ranked relatively low in terms of median citations (Table 8). This indicates that despite their high productivity in terms of article quantity, the impact of their research is comparatively modest. Conversely, the top 10 authors, in terms of their median citations have lower ranks in terms of the number of their publications (Table 9). There was a significant difference between the two groups in average number of publications (119.4±39.8 vs. 13.9±5.5, P<0.001), as well as the average median number of citations (41.0±21.1 vs. 136.5±14.1, P<0.001). These findings highlight a disparity between prolificacy and citation impact among the top-ranked authors.

Discussion

The findings of this study highlight the valuable insights obtained through a targeted bibliometric review. By focusing on pancreatic cancer, we have identified noteworthy patterns that can be leveraged by research institutions, hospitals, and individuals seeking relevant publications. Furthermore, our analysis has successfully pinpointed influential articles and significant contributions in the field of pancreatic cancer. The objective data generated from this study effectively addresses inquiries concerning prolific journals, influential authors, and impactful articles, thereby aiding in informed decision-making for journal subscriptions, article submissions, and research consumption.

This study constitutes the first comprehensive investigation to date, delving into the extensive body of published literature pertaining to pancreatic cancer. It serves as a pioneering effort in meticulously examining essential metrics of research in the field of pancreatic cancer while simultaneously providing an impartial assessment of the leading journals renowned for their substantial productivity and notable influence in this specialized domain. It is the first to determine trending topics in pancreatic cancer. It demonstrates the most relevant chemotherapies cited in literature, while reminding authors of the noteworthiness surgery plays in this field of study.

The authors of the previously published bibliometric review on pancreatic cancer concentrated on specific subtopics within the field, including the incidence of the disease in Middle Eastern and North African (MENA) countries, research trends in exosomes studies, the impact of gut microbiota, as well as therapy strategies and immunology related to pancreatic cancer. However, our study distinguishes itself from the existing literature by offering a broader perspective and a more comprehensive overview of the topic (17-21).

When analyzing the top 10 authors ranked by their cumulative publications as both first and senior authors, we discovered that they attained comparatively lower positions concerning the median citation count. This observation suggests that the quantity of publications is not always a substitute or proxy for the impact of work. In contrast, among the top 10 authors with the highest median citation counts, there were relatively fewer total number of their publications.

When analyzing the top-performing articles, both papers mentioned in the results section as most cited within the field, the first encompassing pancreatic cancer within its topics and the second with pancreatic cancer as its primary focus, were published by the New England Journal of Medicine. This finding showcases the importance of this journal in publishing and disseminating content about pancreatic cancer to the scientific community. These newfound insights offer valuable considerations for the field of pancreatic cancer research and the impact of scholarly contributions.

The findings of this study provide guidance on journal subscriptions, allowing consumers of this data to make informed decisions. Subscribing to top journals in terms of publication count may provide a comprehensive range of research materials on pancreatic cancer. Journals with a high number of articles on pancreatic cancer and a relatively high median citation score per article offer a blend of volume and impactful research.

These results signify the growing interest and research activity in pancreatic cancer over the past three decades, as evident from the increasing number of articles published and the rise of specialized journals in the field. Researchers and institutions can employ objective data to guide their journal selections. They may benefit from analyzing the keyword co-occurrence cluster to identify the most popular topics within the field and read the most influential articles in the field of pancreatic cancer to better understand the most influential advances in the past three decades. Additionally, the analysis emphasizes the importance and limitations of using bibliometric approaches to assess research productivity and impact, providing valuable insights for authors seeking to strategically target journals with similar articles. Authors may use the list of most cited journals to guide their submission process and, thus, maximize their scientific impact. By understanding these trends, the scientific community can continue advancing pancreatic cancer research effectively and make informed decisions to contribute to the fight against this challenging disease.

Limitations

There are two major limitations to this study. Firstly, while Scopus is currently the most reliable database for citation data, there are other databases, such as Google Scholar, which provide similar information. However, the current interface for Google Scholar is prohibitive in performing a comparable study and easily cross-referencing data. The frequency of data updates is different between the citation databases as is the number of journals surveyed and the underlying algorithms that generate the citation data. The second limitation of this study concerns the difficulty in gathering first-author information from such a large dataset. A single author may have multiple versions of their names cited from article to article. Conversely, multiple authors may share similar names, further conflating results. Care was taken to look at the individual authors and institutions for the top articles cited in this study. A unique author ID with uniform adoption would solve this problem. The third limitation of this study is that one of the measures used for article recognition and visibility was citations. Although citations are a highly used method of determining the broader impact of a research article or research journal, the development, writing, and publishing process of research papers may take months, and thus, citations grow over time. The lower number of citations in manuscripts written from 2018 to 2022 is likely justified by their recent publication date rather than the inherent limited merit of these scientific manuscripts. Newly created journals likely have accrued lower citation counts than journals created several years ago.

Conclusions

This analysis highlights the evolving landscape of pancreatic cancer research, with increased interest, specialized journals, and a growing focus on treatment-related investigations. Topic-related bibliometric analyses also allow institutions and individuals to target journal submissions, journal subscriptions, and literature research.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the BIBLIO reporting checklist. Available at https://apc.amegroups.com/article/view/10.21037/apc-24-22/rc

Peer Review File: Available at https://apc.amegroups.com/article/view/10.21037/apc-24-22/prf

Funding: This work was supported in part by the NCI grant to A.G. (No. 3U54CA118948-17S).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://apc.amegroups.com/article/view/10.21037/apc-24-22/coif). 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.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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