Abstract
Purpose
Postoperative pancreatic fistula is a common and serious complication after pancreaticoduodenectomy that significantly impairs patient recovery and prognosis. Despite extensive research, the field lacks systematic bibliometric visualization analyses, which hinders comprehensive understanding of its research landscape, evolutionary trends and key advancements. This study aims to address this gap by systematically analyzing relevant literature to clarify global research patterns and emerging directions.
Methods
A bibliometric analysis was conducted on literature regarding postoperative pancreatic fistula after pancreaticoduodenectomy published from January 2006 to December 2024. Data were retrieved from Web of Science Core Collection and Scopus databases. After removing duplicates, filtering by document type, language and time, and assessing eligibility, 4295 records were included. VOSviewer and Microsoft Excel were used to analyze publication trends, collaboration networks, core author contributions, keyword clustering and co-citation networks.
Results
The number of publications increased steadily with original research articles dominating. Japan the United States China Italy and Germany were the top contributing countries while England had the highest average citation rate per article. University of Verona, Universiteit van Amsterdam, and Heidelberg University were key contributing institutions. Core research themes included postoperative pancreatic fistula classification and definition, risk factors, preventive measures, and surgical technique comparison.
Conclusion
This study comprehensively maps the global research landscape and trends of postoperative pancreatic fistula after pancreaticoduodenectomy. The findings provide valuable insights for identifying research hotspots and guiding future studies, thereby promoting standardized and systematic advancement in this field.
Supplementary Information
The online version contains supplementary material available at 10.1007/s00423-025-03939-7.
Keywords: Postoperative pancreatic fistula, Pancreaticoduodenectomy, Bibliometric analysis
Introduction
Pancreatic head cancer, ampullary cancer, and other tumors invading the pancreatic head or distal common bile duct are often diagnosed at advanced stages due to complex anatomical locations and nonspecific early symptoms resulting in poor prognosis [1–3]. Despite advancements in systemic therapies, surgical resection remains the cornerstone for improving long-term survival [4]. Among surgical procedures, pancreaticoduodenectomy(PD) is the standard treatment for such tumors and is widely used in clinical practice [4]. It demonstrates acceptable perioperative safety when performed by experienced surgical teams. First introduced by Whipple in 1935, PD techniques have been continuously refined [5]. Nevertheless, the complexity of the procedure contributes to a complication rate exceeding 50% with postoperative pancreatic fistula(POPF) occurring in 21.6 to 37.7% of patients [6, 7].
POPF is defined as drainage fluid amylase concentration exceeding three times the upper normal serum limit on or after postoperative day three [8]. Severity is assessed using the ABC grading system established by the International Study Group of Pancreatic Surgery (ISGPS) [8]. This system categorizes leaks based on their impact on patient health. Grade A fistulas are biochemical with minimal drainage output and no significant effect on patient condition [8]. In contrast Grade B and C fistulas are more severe potentially complicating the clinical course and requiring additional drainage interventions extended intensive care unit stays or further surgical procedures [8]. Studies demonstrate that POPF significantly impairs postoperative outcomes leading to increased mortality secondary complications and elevated risk of cancer recurrence [9–11].
Intensive research focuses on POPF prevention and management but the vast volume of literature poses significant challenges. Decades of investigation have produced diverse studies covering risk factor identification surgical technique optimization such as anastomotic methods and stent use perioperative pharmacologic interventions enhanced drainage strategies predictive model development and refinement of the ISGPS classification [12–17]. Despite the extensive available data the field suffers from considerable fragmentation. Research efforts are dispersed across institutions and countries often focusing on isolated aspects of POPF. This fragmentation hinders synthesis of overarching trends identification of key evolving themes mapping of global collaboration networks and recognition of persistent knowledge gaps and emerging frontiers. Traditional narrative reviews provide valuable insights but often fail to quantitatively capture the dynamic evolution and structural organization of this expansive multidisciplinary knowledge base. This fragmentation underscores the urgent need for a comprehensive data driven synthesis to elucidate the global knowledge architecture of POPF research.
To address this gap our study employs rigorous bibliometric methods to analyze literature on POPF after PD published between 2006 and 2024. Our aim is to construct an objective large scale map of the research landscape surrounding this critical surgical complication. By quantifying publication trends collaboration dynamics keyword co-occurrence patterns citation networks and thematic bursts this analysis seeks to provide invaluable insights for clinicians researchers and policymakers. It will clarify the current trajectory of the field highlight influential studies and collaborations identify promising future directions and ultimately promote more targeted and collaborative research efforts to alleviate the significant burden of POPF.
Materials and methods
To identify studies on POPF following PD published from January 1, 2006, to December 31, 2024, a comprehensive literature search was conducted across two databases: Web of Science Core Collection and Scopus. For Web of Science Core Collection, the search query was structured as: “(TS=(pancreatic fistula OR POPF)) AND (TS=(Pancreaticoduodenectomy OR Duodenopancreatectomy OR whipple)),” retrieving 3980 records. For Scopus, the search strategy was: TITLE-ABS-KEY (pancreatic fistula OR “POPF”) AND TITLE-ABS-KEY (Pancreaticoduodenectomy OR “Duodenopancreatectomy” OR “Pancreatoduodenectomy” OR “whipple”), yielding 5322 records. In the identification phase, duplicate records (n = 897) were removed from the combined 9302 records using EndNote (version 21.5). Subsequently, in the screening phase, records were filtered by predefined criteria: document type (only original articles included; reviews, letters, proceeding papers, editorials, meeting abstracts, and other non-research articles excluded, n = 1115), language (non-English records excluded, n = 626), and temporal range (records outside the 2006–2024 timeframe excluded, n = 782). Thereafter, in the eligibility assessment phase, irrelevant records were excluded by screening titles and abstracts to evaluate alignment with the research focus, resulting in the exclusion of 1587 articles. Finally, 4295 records were included in the final bibliometric analysis (Fig. 1).
Fig. 1.
PRISMA flow diagram outlining the literature screening and selection process for bibliometric analysis
We employed VOSviewer (version 1.6.20) to create visual representations, with detailed analytical parameters specified as follows: the full counting method was adopted, and association strength was selected as the normalization approach. Thresholds were flexibly set based on the actual circumstances during the analysis of countries, authors, journals, keywords, and other dimensions. Clustering was conducted using the default modularity-based clustering algorithm embedded in VOSviewer. Author and institution name disambiguation was addressed by relying on the curated data provided by the Web of Science and Scopus databases, and self-citations were excluded from the analysis to ensure robustness. VOSviewer identified the most productive countries, institutions, and authors, along with the most frequently cited journals and co-occurring keywords. Each point on the visual graphs represents a specific country, institution, author, or publication, clustered by collaboration degree, with point size indicating publication count. In the keyword analysis, irrelevant terms were removed, and similar terms were consolidated. The analysis utilized two conventional weighting parameters: “link strength” and “total link strength,” the latter reflecting the cumulative strength of connections between each term and all related terms. Furthermore, to strengthen our findings, we conducted additional statistical analyses using Microsoft Excel (version 2310) to gain deeper insights into publication patterns.
Results
Analysis of annual publication output trends
Over the past 19 years, the cumulative number of publications has steadily increased, although annual counts have varied (Fig. 2). The majority of these publications are original research articles (4295 out of 6818, 63.00%), representing significant advancements in understanding pancreatic fistula following PD. Analysis of publication types indicates that original research articles dominate the field of POPF associated with PD. Variations in annual publications can be attributed to several factors, including the development and revision of International Study Group on Pancreatic Fistula(ISGPF) standards, advancements in minimally invasive pancreaticoduodenectomy(MIPD), the implementation of comprehensive management strategies, the consolidation of clinical research resources, interdisciplinary collaborations, and the impact of the pandemic.
Fig. 2.
Publication trends in POPF research (2006–2024). Annual publications (blue) and cumulative count (orange) are presented, with a dashed trend line indicating a consistent growth in research output
Analysis of publications by countries and regions
Eighty countries have contributed to the scientific literature on POPF following PD. The ten most prolific contributors—Japan, USA, China, Italy, Germany, South Korea, France, Netherlands, England, India—account for 98.00% (4209 out of 4295) of all publications. England leads with the highest average citation count per article (50.66), followed by the Netherlands (49.21), France (46.03), USA (40.45), and Italy (37.69) (Table 1). This indicates that research on POPF in England is highly credible and well-regarded in academic circles. Although Japan ranks first in publication volume within this field, its average citation count per article is relatively low, suggesting a need for improvement in the quality and visibility of Japanese research outputs. Analysis of 51 countries that had published at least 5 relevant articles revealed that their collaboration network comprises 9 distinct clusters, among which the collaboration between Italy and the United States is the most intensive (Fig. 3A). Regarding research trends, from 2006 to 2018, studies on POPF were predominantly concentrated in Japan, the United States, France, England, Germany and South Korea. However, after 2018, the field witnessed a surge in attention from other countries, reflecting expanded global participation and diversified research directions (Fig. 3B).
Table 1.
Analysis of top 10 prolific countries
| Rank | Country | Documents | Citations | Average citations | Total link strength |
|---|---|---|---|---|---|
| 1 | Japan | 888 | 21,808 | 24.56 | 211 |
| 2 | United States | 840 | 33,982 | 40.45 | 624 |
| 3 | China | 726 | 14,210 | 19.57 | 171 |
| 4 | Italy | 417 | 15,716 | 37.69 | 655 |
| 5 | Germany | 363 | 12,479 | 34.38 | 422 |
| 6 | South Korea | 216 | 5659 | 26.20 | 201 |
| 7 | France | 215 | 9896 | 46.03 | 388 |
| 8 | Netherlands | 213 | 10,482 | 49.21 | 501 |
| 9 | England | 208 | 10,538 | 50.66 | 480 |
| 10 | India | 123 | 4122 | 33.51 | 138 |
Fig. 3.
VOSviewer network visualizations illustrating country/region collaboration patterns. (A) Collaboration network of the top 80 countries/regions, with node size indicating publication output and line thickness representing collaboration intensity. (B) Temporal dynamics and collaborative trends among these top 80 countries/regions, where node color denotes publication years
Analysis of publications by institutions
This study employed collaborative network analysis to evaluate 2431 institutions. Sixty-six institutions with at least 30 publications were collectively categorized into 6 clusters(Fig. 4A).The largest cluster (Cluster 1) comprised 19 nodes representing various affiliated universities, while the smallest cluster (Cluster 6) contained only 5 nodes. The remaining clusters included 13 nodes (Cluster 2), 11 nodes (Cluster 3), 9 nodes (Cluster 4), and 9 nodes (Cluster 5). The top 25 universities cover the leading representative institutions in terms of publication volume within each respective cluster: University of Verona (n = 121, 2.82%, Cluster 3), Universiteit van Amsterdam (n = 97, 2.26%, Cluster 2), Heidelberg University (n = 93, 2.17%, Cluster 5), Nagoya University (n = 78, 1.82%, Cluster 1), Hôpital Beaujon (n = 46, 1.07%, Cluster 6), and Sichuan University (n = 59, 1.37%, Cluster 4) (Table 2). Furthermore, the analysis indicated that the Nagoya University, and Purdue University made significant contributions to this research domain from 2006 to 2018. After 2018, research efforts gradually expanded to other institutions, including Heidelberg University, Universiteit van Amsterdam, and Amsterdam UMC (location AMC) (Fig. 4B).
Fig. 4.
VOSviewer network visualizations of institutional collaborations in the research field. (A) Collaboration network of the top 66 universities/institutions, with node size indicating publication output and line thickness representing collaboration intensity. (B) Temporal dynamics and collaborative trends among these top 66 universities/institutions, where node color denotes publication years
Table 2.
Analysis of top 25 prolific institutions
| Institutions | Cluster | Documents | Total link strength |
|---|---|---|---|
| University of Verona | 3 | 121 | 204 |
| Universiteit van Amsterdam | 2 | 97 | 564 |
| Amsterdam UMC (location AMC) | 2 | 94 | 553 |
| Heidelberg University | 5 | 93 | 114 |
| Nagoya University | 1 | 78 | 19 |
| University Medical Center Utrecht | 2 | 70 | 436 |
| Erasmus MC | 2 | 65 | 384 |
| Radboud University Nijmegen | 2 | 64 | 471 |
| Sichuan University | 4 | 59 | 42 |
| Purdue University | 3 | 58 | 121 |
| Harvard University | 3 | 55 | 154 |
| Zhejiang University | 2 | 55 | 18 |
| St. Antonius Ziekenhuis | 2 | 54 | 389 |
| University of Pittsburgh medical center | 5 | 54 | 140 |
| YONSEI University | 1 | 54 | 45 |
| Catharina Ziekenhuis | 2 | 53 | 405 |
| University Hospital Heidelberg | 2 | 53 | 81 |
| Leiden University Medical Center | 2 | 52 | 377 |
| Amsterdam UMC (location VUmc) | 4 | 51 | 156 |
| University of Pennsylvania | 3 | 51 | 171 |
| University of Pisa | 1 | 50 | 119 |
| Chinese Academy of Medical Sciences & Peking Union Medical College | 4 | 49 | 43 |
| Indiana University School of Medicine | 3 | 48 | 118 |
| Seoul National University | 1 | 47 | 89 |
| Hôpital Beaujon | 6 | 46 | 135 |
Analysis of publications by authors
Price observed that a considerable proportion of papers in a specific field is authored by a distinct group of highly productive scholars [18]. Interestingly, the size of this group approximates the square root of the total number of authors involved in the research. In this study, a total of 15,975 authors contributed to the publication output within this domain. Applying Price’s Law, we identified the top 53 most productive authors, each with a publication output of 25 or more articles, whose visualizations revealed eight distinct clusters (Fig. 5A). Notably, the largest cluster was Cluster 1, consisting of 11 authors, whereas the smallest was Cluster 8, encompassing 4 authors. Among all authors, Marc Besselink topped the list with 102 publications, followed by Claudio Bassi (86 papers, ranking second) and Olivier Busch (85 papers, ranking third). As highlighted in Table 3, all top-ten authors have published more than 49 papers, reflecting their high research activity and substantial contributions to the field. Moreover, the analysis revealed that Charles M. Vollmer, Claudio Bassi, Olivier Busch, and Giuseppe Malleo made remarkable contributions to the research domain during the period 2006–2018. Notably, after 2018, the research landscape witnessed the emergence of new key contributors, such as Roberto Salvia and Marc Besselink (Fig. 5B).
Fig. 5.
VOSviewer network visualizations of author collaborations in the research field. (A) Collaboration network of the top 53 authors, with node size indicating publication output and line thickness representing collaboration intensity. (B) Temporal dynamics and collaborative trends among these top 53 authors, where node color denotes publication years
Table 3.
Analysis of top 10 prolific authors
| Rank | Author | Documents | Citations | Average citations | Total link strength |
|---|---|---|---|---|---|
| 1 | Marc Besselink | 102 | 4084 | 40.04 | 417 |
| 2 | Claudio Bassi | 86 | 5063 | 58.87 | 231 |
| 3 | Olivier Busch | 85 | 3766 | 44.31 | 352 |
| 4 | Roberto Salvia | 75 | 3697 | 49.29 | 218 |
| 5 | Giovanni Marchegiani | 61 | 2194 | 35.97 | 178 |
| 6 | Charles M Vollmer | 55 | 5124 | 93.16 | 84 |
| 7 | Giuseppe Malleo | 54 | 3238 | 59.96 | 171 |
| 8 | Tobias Keck | 54 | 2177 | 40.31 | 138 |
| 9 | Markus Büchler | 53 | 3593 | 67.79 | 72 |
| 10 | Amer Zureikat | 49 | 2358 | 48.12 | 95 |
Analysis of publications by journals
Analyzing and synthesizing articles from leading journals provides a clear overview of primary sources of relevant research literature in this field, enabling efficient literature searches, data gathering, and paper submissions. Our study conducted a comprehensive analysis of 466 journals that published articles related to POPF following PD. The findings revealed key insights: HPB emerged as the most prolific journal, publishing 247 articles. However, its recent impact factor, and citations per paper were lower, indicating limited academic influence. Enhancing the overall impact of this journal in POPF research is essential. Furthermore, the Annals of Surgery demonstrated exceptional performance, averaging 97.11 citations per publication and achieving the highest citation count of 13,984. Detailed information on the top ten prolific and highly cited journals is available in Supplementary Table S1. Within the 4295 records analyzed, Table 4 lists the top 10 most cited articles. The article by Johanna A.M.G. Tol et al. in Surgery, titled “Definition of a standard lymphadenectomy in surgery for pancreatic ductal adenocarcinoma: A consensus statement by the International Study Group on Pancreatic Surgery (ISGPS)” received the highest citation count of 549, significantly surpassing the second-ranked paper with 465 citations. The third most cited paper, entitled “Early versus late drain removal after standard pancreatic resections: results of a prospective randomized trial”, addresses the optimal timing of intra-abdominal drain removal following standard pancreatic resections, conducting a prospective randomized trial of 114 patients at low risk of POPF, and reporting key outcomes while identifying independent risk factors for POPF, with a total of 435 citations accumulated.
Table 4.
Analysis of top 10 citations
| Rank | Author | Number of citations | Title | Journal |
|---|---|---|---|---|
| 1 |
Johanna A.M.G. Tol et al. (2014) |
549 | Definition of a standard lymphadenectomy in surgery for pancreatic ductal adenocarcinoma: A consensus statement by the International Study Group on Pancreatic Surgery (ISGPS) | Surgery |
| 2 |
Jony van Hilst et al. (2019) |
465 | Laparoscopic versus open pancreatoduodenectomy for pancreatic or periampullary tumours (LEOPARD-2): a multicentre, patient-blinded, randomised controlled phase 2/3 trial | Lancet Gastroenterology & Hepatology |
| 3 |
Claudio Bassi et al. (2010) |
435 | Early versus late drain removal after standard pancreatic resections: results of a prospective randomized trial | Annals of Surgery |
| 4 |
Kristoffer Lassen et al. (2012) |
423 | Guidelines for perioperative care for pancreaticoduodenectomy: Enhanced Recovery After Surgery (ERAS) Society recommendations | Clinical Nutrition |
| 5 | Thomas Schnelldorfer et al. (2008) | 400 | Long-term survival after pancreatoduodenectomy for pancreatic adenocarcinoma: is cure possible? | Annals of Surgery |
| 6 |
Peter J. Allen et al. (2014) |
358 | Pasireotide for Postoperative Pancreatic Fistula | New England Journal of Medicine |
| 7 | Richard A Smith et al. (2009) | 357 | Preoperative platelet-lymphocyte ratio is an independent significant prognostic marker in resected pancreatic ductal adenocarcinoma | American Journal of Surgery |
| 8 |
Wataru Kimura et al. (2014) |
337 | A pancreaticoduodenectomy risk model derived from 8575 cases from a national single-race population (Japanese) using a web-based data entry system: the 30-day and in-hospital mortality rates for pancreaticoduodenectomy | Annals of Surgery |
| 9 |
C Palanivelu et al. (2017) |
332 | Randomized clinical trial of laparoscopic versus open pancreatoduodenectomy for periampullary tumours | British journal of surgery |
| 10 |
George Van Buren 2nd et al. (2014) |
331 | A randomized prospective multicenter trial of pancreaticoduodenectomy with and without routine intraperitoneal drainage | Annals of Surgery |
Analysis of co-citation references
A total of 28,664 references were included in this study, among which 74 had accumulated 5 or more citations. The co-citation network of these 74 references was analyzed and visualized using VOSviewer, leading to the identification of six distinct clusters (Fig. 6). Larger nodes within the network indicate highly cited references, while thicker lines denote stronger co-citation relationships. Table 5 highlights the top 10 most co-cited references, mainly published in reputable journals such as Surgery, Annals of Surgery, Surgical Endoscopy and Other Interventional Techniques, and Journal of the American College of Surgeons.
Fig. 6.
VOSviewer network visualization of co-cited references in the research field. Node size indicates citation frequency, and line connections represent co-citation relationships, highlighting the central role of key works
Table 5.
Analysis of top 10 co-citations
| Rank | Author | Number of citations | Title | Journal |
|---|---|---|---|---|
| 1 |
Moritz N Wente et al. (2007) |
265 | Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS) | Surgery |
| 2 |
Claudio Bassi et al. (2017) |
176 | The 2016 update of the International Study Group (ISGPS) definition and grading of postoperative pancreatic fistula: 11 Years After | Surgery |
| 3 |
Daniel Dindo et al. (2004) |
146 | Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey | Annals of Surgery |
| 4 |
Claudio Bassi et al. (2005) |
107 | Postoperative pancreatic fistula: an international study group (ISGPF) definition | Surgery |
| 5 |
M Gagner et al. (1994) |
72 | Laparoscopic pylorus-preserving pancreatoduodenectomy | Surgical Endoscopy and Other Interventional Techniques |
| 6 | Horacio J Asbun et al. (2012) | 28 | Laparoscopic vs. open pancreaticoduodenectomy: overall outcomes and severity of complications using the Accordion Severity Grading System | Journal of the American College of Surgeons |
| 7 | Mark P Callery et al. (2013) | 25 | A prospectively validated clinical risk score accurately predicts pancreatic fistula after pancreatoduodenectomy | Journal of the American College of Surgeons |
| 8 | Niccolò Napoli et al. (2016) | 18 | Indications, technique, and results of robotic pancreatoduodenectomy | Updates in Surgery |
| 9 |
Mark P Callery et al. (2013) |
17 | A prospectively validated clinical risk score accurately predicts pancreatic fistula after pancreatoduodenectomy | Journal of the American College of Surgeons |
| 10 |
A O Whipple et al. (1935) |
16 | Treatment of carcinoma of the ampulla of vater | Annals of Surgery |
Analysis of keywords
Keywords serve as concise indicators of relevant features in scientific research, clarifying focal points and their interconnections within a discipline. VOSviewer was utilized to create a keyword co-occurrence map based on high-frequency occurrences. Node sizes correspond to the frequency of keyword co-occurrence, emphasizing prominent themes in the research domain. A total of 37,649 keywords were involved in this study, among which only 139 had an occurrence frequency of 80 or more. Network graph analysis grouped these 139 high-frequency keywords into 3 distinct clusters (Fig. 7A). Identified as the most frequently occurring keywords were “pancreatoduodenectomy (n = 1517),” “whipple (n = 1325),” “POPF (n = 1172),” “complication (n = 956),” “outcome (n = 922),” and “surgery (n = 865).” Lower co-occurrence frequencies of other keywords suggest the need for further research to explore these topics in greater depth. These findings indicate the field is in an emerging research stage with significant implications. Additionally, a combined analysis of Fig. 7B; Table 6 highlights that, in recent years, the primary research foci pertaining to POPF following PD have centered on surgical procedures, perioperative management, complications, classification, risk factors, and outcomes. These findings provide critical insights into the dominant research trends and core themes associated with POPF, thereby fostering a more comprehensive understanding of this prevalent postoperative complication.
Fig. 7.
VOSviewer network visualizations of keywords in the research field. (A) Network analysis of the top 139 keywords, with node size indicating term frequency and line thickness representing association strength. (B) Temporal dynamics of these top 139 keywords, where node color denotes publication years
Table 6.
Frequency of occurrences and total link strengths of the top 10 keywords
| Rank | Keywords | Frequency | Total link strength |
|---|---|---|---|
| 1 | patient | 2249 | 34,877 |
| 2 | pancreatoduodenectomy | 1517 | 17,353 |
| 3 | study | 1442 | 23,054 |
| 4 | whipple | 1325 | 16,379 |
| 5 | popf | 1172 | 17,750 |
| 6 | complication | 956 | 16,121 |
| 7 | rate | 946 | 17,136 |
| 8 | outcome | 922 | 14,525 |
| 9 | surgery | 865 | 14,478 |
| 10 | group | 851 | 15,669 |
Analysis of research frontiers
Our analysis of keywords from 2018 to 2024 has generated a list of potential research frontiers, detailed in Table 7. These research frontiers comprise pancreatic cancer, laparoscopic surgery, risk factors, predictors, complications, and postoperative outcomes. Our findings highlight promising avenues for future exploration and provide valuable guidance for researchers.
Table 7.
Analysis of research keywords between 2006 and 2024
| Rank | Year | Occurrences | Keywords |
|---|---|---|---|
| 1 | 2017.3 | 1325 | whipple |
| 2 | 2018.4 | 1172 | popf |
| 3 | 2018.3 | 956 | complication |
| 4 | 2018.7 | 922 | outcome |
| 5 | 2018.1 | 427 | risk-factors |
| 6 | 2018.1 | 414 | long term survival |
| 7 | 2018.1 | 308 | pancreatic cancer |
| 8 | 2019.2 | 242 | laparoscopy |
| 9 | 2018.5 | 198 | predictor |
| 10 | 2019.7 | 141 | postoperative outcome |
Discussion
Bibliometric analyses offer a robust framework for systematically dissecting published literature in specific fields, distinct from traditional reviews by quantifying research trends and collaborative networks [19]. This study employed bibliometric methods to explore collaborative patterns, research hotspots, emerging themes, and future directions in POPF following PD. A total of 4295 records were retrieved from 466 journals, involving 15,975 authors from 2431 institutions across 80 countries.
The annual publication rate of PD-related POPF studies has fluctuated under the influence of technological advancements, research focus shifts, guideline updates, and socio-environmental factors, yet the overall upward trend confirms its status as a research hotspot—highlighting substantial potential for novel contributions. Academic output correlates significantly with national socio-economic status, with Japan leading in publication volume, followed by the United States, China, Italy, and Germany [20, 21]. The United States (n = 33982) and Japan (n = 21808) dominate total citations, while England boasts the highest average citation rate, reflecting its influential role in the field. International collaboration remains pivotal for academic productivity, though disparities exist across regions: the United States maintains strong partnerships with Italy and China, emphasizing the need to strengthen knowledge exchange between developed and developing nations [22]. Among institutions, the University of Verona, Universiteit van Amsterdam, Amsterdam UMC (AMC), Heidelberg University, and Nagoya University emerged as core contributors with stable collaborative networks. Notably, Marc Besselink has established himself as a preeminent figure in this domain over 19 years, pioneering advancements in POPF diagnostic criteria refinement, minimally invasive versus open PD outcome comparisons, severe POPF management optimization, risk assessment model development, and nutritional support/inflammatory response research—translating to tangible improvements in clinical decision-making and patient prognosis [8, 23–28]. His extensive publication record underscores his profound contributions to the field.
A critical strength of this study lies in bridging bibliometric clusters/keyword bursts with pivotal clinical milestones, addressing the gap between research trends and real-world surgical advancements. Co-citation analysis identified four core clusters, each demonstrating direct translational relevance to clinical practice. The “classification and definition” cluster aligns with landmark consensus developments: the 2005 ISGPF consensus established the first objective POPF grading system based on drain fluid amylase levels (≥ 3×upper limit of normal on postoperative day 3) and clinical impact, resolving historical reporting inconsistencies, while the 2016 ISGPS update reclassified grade A POPF as a “biochemical leak” and refined grades B/C to prioritize clinically relevant outcomes [8, 29]. This paradigm shift, mirrored in the cluster’s evolutionary trajectory, has standardized clinical documentation and cross-study comparisons, equipping surgeons to distinguish trivial leaks from actionable complications. Equally impactful is the integration of the “risk factors” and “preventive measures” clusters into clinical practice: the former centers on pancreatic gland texture, a well-validated preoperative predictor of POPF, and the development of tools including the Fistula Risk Score (FRS) and Alternative Fistula Risk Score (a-FRS), which have transitioned from bibliometric hotspots to clinical decision aids facilitating individualized risk assessment through integration of preoperative imaging features such as parenchymal texture and duct diameter with intraoperative variables [25]. The latter cluster translates into actionable perioperative strategies, including stent placement to reduce anastomotic pressure and the evolution from routine drainage to risk-based selective drainage with early removal protocols such as drain removal when amylase levels drop below 5000 U/L on postoperative day 1, which directly optimizes care algorithms [30, 31]. The “surgical technique comparison” and “pharmacological use” clusters reflect transformative clinical advancements: somatostatin analogues, a focus of preventive research, exhibit inconsistent efficacy in clinically relevant POPF, resulting in targeted administration to high-risk patients [32]. The surgical cluster meanwhile traces the clinical transformation of MIPD, progressing from feasibility assessments to demonstrating superior outcomes such as reduced blood loss and shorter hospital stays in high-volume centers, while also addressing challenges related to learning curves and application in high-risk cases involving soft pancreatic glands and small pancreatic ducts [33–35].This aligns with refinements in pancreaticojejunostomy such as the modified Blumgart anastomosis and robotic-assisted suturing, which enhance anastomotic safety. Complementing these clusters, keyword co-occurrence analysis highlights “perioperative management” as an emerging theme, mirroring clinical shifts toward multidisciplinary care including endocrinological glycemic control and preoperative nutritional optimization integrated into enhanced recovery after surgery (ERAS) pathways, where bibliometric trends directly inform clinical protocol development.
High-frequency keywords corroborate these trends, identifying core themes including Whipple procedure complications, international study group guidelines, risk factors, outcomes, and surgical techniques. Recent keyword bursts such as laparoscopy and postoperative outcomes reflect ongoing clinical priorities, namely comparing surgical methods and investigating risk factors and preventive measures for POPF [36, 37]. The prominence of these research directions highlights promising avenues for further exploration. In-depth investigation can deepen understanding of the complex etiology of POPF, ultimately advancing prevention and treatment strategies.
Building on these linkages, actionable research priorities for Hepatopancreatobiliary Surgeons are proposed. First, develop dynamic prediction models integrating preoperative radiomics, intraoperative perfusion assessment, and postoperative biomarkers to guide individualized intraoperative and postoperative management. Second, establish standardized MIPD training systems encompassing skill assessment protocols, simulation curricula, and complex case guidelines to address learning curve challenges. Third, conduct well-designed randomized controlled trials to evaluate novel anastomotic technologies, including modified techniques, absorbable stents, and tissue engineering products, for clinically relevant POPF reduction. Fourth, optimize multimodal ERAS pathways by integrating preoperative to postoperative interventions, with rigorous assessment of long-term outcomes. Fifth, perform large-scale multicenter long-term studies comparing oncological outcomes of MIPD and open PD, while exploring organ-preserving minimally invasive approaches under oncological safety constraints.
In summary, this bibliometric analysis establishes direct linkages between research trends and real-world surgical advancements. The proposed priorities provide a clear roadmap for translating research into clinical practice, ultimately advancing POPF management and improving patient outcomes.
Limitations
This study has several limitations. First, it relied solely on data from Web of Science and Scopus. While these platforms cover high-impact journals, they may exclude other databases relevant to the field, introducing potential selection bias. Second, only English language articles and reviews were included, which may overlook valuable contributions from non-English speaking regions and introduce language bias. Third, no fixed citation window was set for co-citation analysis. This lack of standardization may affect the accuracy of core literature clustering and research frontier identification. Fourth, despite using curated data from the two databases and excluding self-citations to address author and institution name disambiguation, residual issues remain. For instance, authors with identical names at different institutions may distort retrieval of relevant records. Fifth, parameter sensitivity was not systematically evaluated. Although VOSviewer version 1.6.20 was used with specific settings including full counting method, association strength normalization, flexible thresholds for dimensions like countries, authors, journals and keywords, default modularity-based clustering algorithm and two weighting parameters, changes to these settings were not tested and may alter result interpretation. Despite these limitations, the study still offers valuable insights into POPF.
Conclusion
This 19-year bibliometric analysis clarifies the evolutionary landscape of research on POPF following PD. The steady growth in original research reflects advancing progress, with Japan, the United States, China, Italy and Germany as dominant contributors and England achieving the highest average citation rate. Post-2018 witnessed expanded global participation and collaboration, while key institutions including University of Verona and Universiteit van Amsterdam, alongside prolific author Marc Besselink, drove knowledge advancement. Core research themes centered on classification and definition, risk factors, preventive measures and surgical technique comparison, guiding future directions. Annals of Surgery emerged as the most influential journal, underscoring the study’s value in mapping the field and informing targeted research.
Supplementary Information
Below is the link to the electronic supplementary material.
Acknowledgements
We extend our gratitude to the authors of all studies included in this paper and to the participants who contributed to each study.
Author contributions
M.T., P.C., X.P., and Y.C.: designed the study; M.T., P.C., X.P., and Y.C.: data collection and verification; M.T., X.P., and Y.C.: software analysis; M.T.: original draft, Y.C.: validation. All authors contributed to and approved the submitted article.
Funding
This study was funded by the Research Project on Teaching Reform in Ordinary Undergraduate Universities in Hunan Province(No:202502000774).
Data availability
No datasets were generated or analysed during the current study.
Declarations
Ethics approval and consent to participate
Our study is based on publicly accessible bibliographic data, thus no ethical approval was deemed necessary.
Consent for publication
All authors have reviewed and approved the final version of this manuscript.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s note
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Data Availability Statement
No datasets were generated or analysed during the current study.