A comprehensive guide to lymph node staging of cholangiocarcinoma by endoscopic ultrasound

A comprehensive guide to lymph node staging of cholangiocarcinoma by endoscopic ultrasound | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article A comprehensive guide to lymph node staging of cholangiocarcinoma by endoscopic ultrasound Willem J. Lammers, David M. de Jong, Marco J. Bruno, Lydi M.J.W. van Driel This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-8700524/v1 This work is licensed under a CC BY 4.0 License Status: Under Review Version 1 posted 11 You are reading this latest preprint version Abstract Accurate lymph node (LN) staging is critical for treatment planning in patients with perihilar cholangiocarcinoma (pCCA) and intrahepatic cholangiocarcinoma (iCCA). Cross-sectional imaging however has limited sensitivity for detecting LN metastases. Recent studies have demonstrated that endoscopic ultrasound (EUS) offers additional value in LN assessment for both pCCA and iCCA. Despite its advantages, reliably identifying the individual LN stations relevant to these malignancies can be challenging and requires detailed knowledge of regional anatomy. This article provides a standardized, systematic guide for identifying all major LN stations associated with pCCA and iCCA using linear EUS, with the aim of improving preoperative staging and optimizing treatment planning. Endoscopic ultrasound perihilar cholangiocarcinoma intrahepatic cholangiocarcinoma lymph node Figures Figure 1 Figure 2 Figure 3 Figure 4 Figure 5 Introduction Surgical resection or liver transplantation remains the only curative treatment option for patients with perihilar cholangiocarcinoma (pCCA) or intrahepatic cholangiocarcinoma (iCCA). In patients with regional or extraregional lymph node (LN) metastases however the potential benefit of surgery diminishes considerably and postoperative survival is poor (1-3). This makes accurate preoperative LN staging crucial for selecting appropriate candidates for curative intent therapies. Recently, the American Joint Committee on Cancer (AJCC) revised the definitions of nodal (N1, N2) and metastatic (M) disease in its staging system (4). These updates underscore the importance of precise LN assessment. For pCCA, LNs located beyond the hepatoduodenal ligament are now categorized as distant metastases, and N-stage is determined by the number of positive regional nodes rather than their anatomical location. In contrast, for iCCA the N and M categories depend on whether the tumor arises in the left or right hepatic lobe. Despite these refinements, cross-sectional imaging (CSI) continues to perform suboptimal in LN staging, with sensitivities and specificities of 61% and 88% for CT, 64% and 68% for MRI, and 33% and 97% for PET/CT, respectively (5-7). Given the limitations of CSI, there has been growing interest in endoscopic ultrasound (EUS) including EUS-guided tissue acquisition of LN as a more sensitive staging tool. The European Association for the Study of the Liver (EASL) guidelines on extrahepatic CCA (8) and intrahepatic CCA (9) are the first to systematically recommend preoperative EUS for LN staging. Despite significant interobserver agreement in defining suspicious or benign-looking LN (10), EUS has the potential to affect clinical decision making in 4-30% of patients (11-16). Even when CSI did not show suspicious LN, EUS still meaningfully impacted clinical decision making in a significant number of patients; either by detecting malignant LN, or by detection of other findings such as tumor invasion in the pancreas requiring a different treatment approach (11-16). To standardize LN terminology and improve communication across specialties, the Japanese Society of Hepato-Biliary-Pancreatic Surgery (JSHBPS) introduced the third edition of its classification of biliary tract cancers in 2015 (17). This system defines LN stations according to their relationship to key vascular landmarks ( Figure 1 ), much like Sharma et al. described EUS of the hepatoduodenal ligament (18). However, a corresponding EUS-based method for reliably identifying all important LN stations has not been established, creating a gap between radiologic, endosonographic, and surgical approaches. To address this need, the present article proposes a systematic EUS approach for identifying all LN stations relevant to pCCA and iCCA. By aligning EUS imaging with the JSHBPS classification, this method aims to enhance diagnostic accuracy and support optimal treatment planning. This systematic EUS evaluation is used in the POELH-I and POELH-II trial (Clinicaltrials.gov NCT05678218, registration date: 05-09-2022). Procedure LN evaluation is performed from three key locations within the gastrointestinal tract: the stomach, the duodenal bulb, and the second and third portions of the duodenum. From each of these vantage points, specific LN stations can be systematically assessed. LNs are classified according to their relationship to adjacent vascular structures, as defined by the JSHBPS classification system. This can be challenging when a LN lies at an equal distance from two major vessels. In such cases, the LN may be assigned to both potential stations. A further challenge arises in the presence of vascular anatomical variants, for which no universal classification rules exists. These situations require careful interpretation and correlation with known vascular landmarks and discussion of relevant issues and deviations in the endoscopy report.. To ensure that all relevant LN stations are evaluated, the examination is conducted in a stepwise and systematic manner, progressing through each anatomical window to minimize the risk of overlooking important nodal regions. We have used the linear EUS scope model EG38-J10UT (Pentax Medical, Tokyo, Japan) and color Doppler Machine Hitachi Arietta 850 for all evaluations. Stomach Lymph nodes along the celiac artery and abdominal aorta (stations 9, 16A1, 16A2, 16B1, 16B2) From the gastro-esophageal junction, the abdominal aorta can be identified dorsally to the stomach. Just below the diaphragm, its first major branch can be identified: the celiac artery. Station 9 LNs are located above the celiac artery, below the diaphragm, and to the left of the abdominal aorta ( Figure 2A ). In some cases, it may be challenging to distinguish station 9 nodes from station 16A1. LNs surrounding the abdominal aorta are collectively classified as station 16 and are further subdivided according to their anatomical relationship to major aortic branches. Station 16A1 LNs lie adjacent to the abdominal aorta, above the celiac artery, and between the aorta and the diaphragmatic crura. When a LN is located at an equal distance from the celiac trunk and the abdominal aorta, it may be described as station 9/16A1, following the principle that LNs are classified according to the vessel in closest proximity ( Figure 2B) . Station 16A2 LNs are located between the celiac trunk and the superior mesenteric artery ( Figure 2C ). Station 16B1 LNs lie between the superior mesenteric artery and the inferior mesenteric artery, whereas station 16B2 nodes are situated below the inferior mesenteric artery. Substations that are located further down alongside the aorta are not consistently visible from the stomach, often due to patient-related factors such as decreased echogenicity or the presence of a hiatal hernia. Lymph nodes along the superior mesenteric artery (stations 14P and 14D) From the abdominal aorta, the superior mesenteric artery can be followed until its first major branch, the middle colic artery, which typically curves toward the pancreatic body (towards the EUS probe). This segment, from its origin to the middle colic artery, can be divided into two equal parts: station 14P, comprising LNs along the proximal half closest to the origin of the superior mesenteric artery, and station 14D, comprising LNs along the distal half closest to the middle colic artery. These LN stations can also be visualized from the duodenum (see the section on assessment from the duodenum). Lymph nodes along the splenic artery and splenic hilum (stations 10 and 11) After arising from the aorta, the celiac trunk divides into the common hepatic artery and the splenic artery. The splenic artery follows a characteristically tortuous course along the pancreatic body and tail toward the splenic hilum. LNs distributed along the splenic artery are classified as station 11 ( Figure 2D ), whereas LNs clustered within the splenic hilum are classified as station 10 ( Figure 3A ). Lymph nodes along the hepatic artery and hepatoduodenal ligament (stations 8 and 12) From the celiac trunk bifurcation, the common hepatic artery can be traced towards the liver hilum. Along this course, LNs are classified according to their relationship with the artery and the EUS-probe. Station 8A LNs are located between the vessel and the EUS probe ( Figure 3B ). Station 8P LNs are located between the common hepatic artery and the portal vein ( Figure 3C ). As the common hepatic artery is traced distally, the vessel divides into the gastroduodenal artery and the proper hepatic artery. The proper hepatic artery together with the portal vein and the extrahepatic bile duct, form the portal triad; LNs in this region are classified as station 12. Station 12 LNs are further subdivided according to their proximity to adjacent anatomical landmarks: 12A: along the proper hepatic artery ( Figure 3D and 4A ), 12P: along the portal vein, 12B: along the extrahepatic bile duct ( Figure 4B ), 12C: along the cystic duct ( Figure 4C ). Each subgroup is additionally divided based on whether the nodes are closer to the liver hilum (e.g., 12A1, 12P1, 12B1) or the pancreas (e.g., 12A2, 12P2, 12B2), with the insertion of the cystic duct as the border ( Figure 4D ). LNs located above the bifurcation of the extrahepatic bile duct into left and right hepatic ducts are designated 12H. It should be emphasized that LNs in stations 8 and 12 may not always be clearly distinguishable based on anatomic landmarks, particularly in the presence of vascular variants. Lymph nodes around the pancreas (station 18) All LNs located below the pancreatic body or tail are classified as station 18 (as seen from the stomach). Duodenal bulb Lymph nodes along the hepatic artery and hepatoduodenal ligament (stations 8 and 12) All LNs located along the hepatic artery and within the hepatoduodenal ligament that are visualized from the stomach can also be evaluated from the duodenal bulb. For the description of subclassifications of these stations, see the section from the stomach. Importantly, LNs that are not accessible for EUS-guided sampling from the stomach often become accessible from the duodenal bulb because in this position, the extrahepatic bile duct lies closer to the transducer, whereas from the stomach the portal vein and hepatic artery are typically in closer proximity to the probe. Duodenum Several LN stations can be visualized from different portions of the duodenum, including stations 13, 14, 15, 16, 17 and 18. Lymph nodes along the posterior (station 13A and 13B) and anterior (stations 17A and 17B) surface of the pancreatic head Stations 13 and 17 correspond to LNs located along the posterior and anterior surfaces of the pancreatic head, respectively. Station 13 LNs are situated posterior to the pancreatic head, in the space between the pancreas and the inferior vena cava and the aorta. In contrast, station 17 LNs are located along the anterior surface of the pancreatic head, interposed between the pancreas and the gastroduodenal artery as well as the anterior superior pancreaticoduodenal vessels. The subdivision into A and B reflects the cranio-caudal relationship to the duodenal papilla: stations 13A and 17A are positioned proximal to the papilla, whereas stations 13B and 17B are located distal to it ( Figure 5B + C ). Lymph nodes along the superior mesenteric artery (stations 14P and 14D) and within the transverse mesocolon (station 15) Station 14 and 15 comprise LNs along the superior mesenteric artery and within the transverse mesocolon, respectively. From the second part of the duodenum, the aorta is first identified. With gradual clockwise rotation, the uncinate process comes into view, followed by the mesenteric vessels. These mesenteric vessels are visualized as parallel longitudinal structures, with the superior mesenteric vein closer to the probe than the superior mesenteric artery. The middle colic artery represents the first main branch of the superior mesenteric artery, often coursing in the direction of the probe. Station 14P LNs can be identified to the left of the MCA on the EUS screen around the superior mesenteric artery, in the direction of the aortic origin, whereas station 14D LNs are located to the right of the middle colic artery ( Figure 5A ). Station 15 LNs are associated with the transverse mesocolon, particularly along the trajectory of the middle colic artery as it travels toward the transverse colon. Tracing the superior mesenteric artery until the middle colic artery branches to the right. The fat plane around the middle colic artery is where station 15 LNs can be identified. Station 14 and 15 LNs may be more challenging to visualize, because of their distance from the duodenal lumen, overlying bowel gas, patient anatomy, and variable mesenteric fat. Their identification often requires subtle probe rotation and optimized Doppler imaging. Lymph nodes along the abdominal aorta (station 16) and around the pancreas (station 18) From the third part of the duodenum, para-aortic LNs of station 16 can also be visualized. This position can facilitate tissue acquisition in situations where sampling from the stomach is not possible. Station 18 LNs are retroperitoneal LNs situated along the caudal border of the pancreatic body and partly tail. These LN can be observed from the third part of the duodenum, anterior to the superior mesenteric vessel, just below the point where it crosses the uncinate process of the pancreas. These LNs are more easily biopsied from the duodenum than from the stomach, as the pancreatic body or tail lies between the probe and the LNs when approached from the stomach. According to the AJCC, regional LN stations for pCCA are 8, 12 and 13, and for right sided iCCA are considered at stations 8, 12, 13 and 17. The AJCC does not explicitly list this, but depending on surgical series, station 14P LN may sometimes be considered regional because they drain the same lymphatic basin ( Table 1 ). Left-sided iCCA tumors have additional drainage via the lesser omentum toward the left gastric artery (station 7 according to the Japanese classification). Therefore, regional LN stations for left-sided iCCA tumors are considered at stations 8, 12, and 7. Discussion This paper provides a structured, EUS-based approach to identifying all LN stations relevant to pCCA and iCCA, using the JSHBPS classification as a detailed anatomical framework. By systematically describing EUS views from the stomach, duodenal bulb, and distal duodenum, we illustrate how both regional and extraregional LN stations can be systematically evaluated. Importantly, the approach allows endosonographers to distinguish between LNs that fall within the AJCC-defined regional and extraregional locations. Accurate classification of LNs is essential, as involvement of extraregional LNs represents distant (M1) disease and typically precludes patients from curative resection or liver transplantation protocols. By integrating EUS imaging with established surgical anatomy, this systematic approach offers a practical framework that may enhance diagnostic accuracy and improve multidisciplinary communication among radiology, endoscopy, and hepatobiliary surgery teams. Further prospective studies are warranted to evaluate the impact of standardized EUS-based LN mapping on clinical decision-making, patient selection for resection or transplantation, and long-term oncological outcomes. Abbreviations pCCA Perihilar Cholangiocarcinoma iCCA Intrahepatic Cholangiocarcinoma LN Lymph Node EUS Endoscopic Ultrasound AJCC American Joint Committee on Cancer CT Computed Tomography-scan MRI Magnetic Resonance Imaging PET Positron Emission Tomography CSI Cross-sectional Imaging JSHBPS Japanese Society of Hepato-Biliary-Pancreatic Surgery N-stage Lymph node stage M-stage Metastatic disease stage Declarations Ethics approval and consent to participate: The images and figures are selected from the POELH-II trial. This trial received approval from IRB approval code MEC-2022-0402 (Ethical committee from the Erasmus MC University Medical Center). This trial was conducted in compliance with the Helsinki declaration and patients provided written informed consent (Clinicaltrials.gov NCT05678218, registration date: 05-09-2022). Consent for publication: Not applicable Availability of data and materials: All data generated or analysed during this study are included in this published article. Data on the POELH-I and POELH-II trials will be published separately. Competing interests: MJB reports research grants from Boston Scientific, Cook Medical, Pentax Medical, InterScope, 3M, and Mylan, and performed as a consultant for Boston Scientific, Cook Medical, and Pentax Medical. WJL received consultancy fees from Mediglobe. LMJWD received consultancy fees from Boston Scientific. DMJ declares that he does not have any conflict of interest. Funding: The authors did not receive any financial support to produce this manuscript. Authors’ contributions: WJL, DMJ, LMJWD: Initial draft, revision, editing and final approval. MJB: revision and final approval. Acknowledgements: Not applicable References Blechacz B, Cholangiocarcinoma. Current Knowledge and New Developments. Gut Liver. 2017;11(1):13–26. Jolissaint JS, Soares KC, Seier KP, Kundra R, Gönen M, Shin PJ, et al. Intrahepatic Cholangiocarcinoma with Lymph Node Metastasis: Treatment-Related Outcomes and the Role of Tumor Genomics in Patient Selection. Clin Cancer Res. 2021;27(14):4101–8. Radtke A, Konigsrainer A. Surgical Therapy of Cholangiocarcinoma. Visc Med. 2016;32(6):422–6. Amin MB, Greene SEF, Byrd DR, Brookland RK, Washington MK. American joint committee on cancer: Cancer staging manual. 8 ed. New York: Springer International Publishing; 2017. pp. 295–301. Ruys AT, van Beem BE, Engelbrecht MR, Bipat S, Stoker J, Van Gulik TM. 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J Hepatol. 2023;79(1):181–208. de Jong DM, Roosterman D, Bruno MJ, van Driel LMJW, Lammers WJ. Interobserver variability in lymph node evaluation with endoscopic ultrasonography in cholangiocarcinoma. Endosc Int Open. 2025;13(continuous publication). Gleeson FC, Rajan E, Levy MJ, Clain JE, Topazian MD, Harewood GC, et al. EUS-guided FNA of regional lymph nodes in patients with unresectable hilar cholangiocarcinoma. Gastrointest Endosc. 2008;67(3):438–43. Malikowski T, Levy MJ, Gleeson FC, Storm AC, Vargas EJ, Topazian MD, et al. Endoscopic Ultrasound/Fine Needle Aspiration Is Effective for Lymph Node Staging in Patients With Cholangiocarcinoma. Hepatology. 2020;72(3):940–8. de Jong DM, den Hoed CM, Willemssen FEJA, Thomeer MGJ, Bruno MJ, Koerkamp BG, et al. Impact of EUS in liver transplantation workup for patients with unresectable perihilar cholangiocarcinoma. Gastrointest Endosc. 2024;99(4):548–56. de Jong DM, van de Vondervoort S, Dwarkasing RS, Doukas M, Voermans RP, Verdonk RC, et al. Endoscopic ultrasound in patients with resectable perihilar cholangiocarcinoma: impact on clinical decision-making. Endosc Int Open. 2023;11(2):E162–8. de Jong DM, van de Vondervoort S, Dwarkasing RS, Thomeer MGJ, Doukas M, Voermans RP, et al. Endoscopic ultrasound with tissue acquisition of lymph nodes in patients with potentially resectable intrahepatic cholangiocarcinoma. Endosc Int Open. 2024;12(08):E998–1005. de Jong DM, van Driel LMJW, Lakhtakia S, Ramchandani M, Fathima Memon S, Tyagi A, et al. Endoscopic Ultrasound for Nodal Staging in Patients with Resectable Cholangiocarcinoma. J Clin Med. 2025;14(21):7545. Miyazaki M, Ohtsuka M, Miyakawa S, Nagino M, Yamamoto M, Kokudo N, et al. Classification of biliary tract cancers established by the Japanese Society of Hepato-Biliary-Pancreatic Surgery: 3(rd) English edition. J Hepatobiliary Pancreat Sci. 2015;22(3):181–96. Sharma M, Rameshbabu CS, Dietrich CF, Rai P, Bansal R. Endoscopic ultrasound of the hepatoduodenal ligament and liver hilum. Endosc Ultrasound. 2018;7(3):168–74. Table Table 1. Overview of the regional and extraregional LN Japanese LN Station Anatomical Region iCCA (left) iCCA (right) pCCA dCCA 8A/8P Common hepatic artery R R R R 12A/P/B/C/H Hepatoduodenal ligament R R R R 13A/B Posterior pancreatic head ER R R R 17A/B Anterior pancreatic head ER R ER R 14P Proximal superior mesenteric artery ER ER ER R 14D Distal superior mesenteric artery ER ER ER R 9 Celiac axis ER ER ER ER 10 Splenic hilum ER ER ER ER 11 Splenic artery ER ER ER ER 15 Transverse mesocolon ER ER ER ER 16A1/A2/B1/B2 Para-aortic ER ER ER ER 18 Inferior pancreatic body border ER ER ER ER Additional Declarations Competing interest reported. MJB reports research grants from Boston Scientific, Cook Medical, Pentax Medical, InterScope, 3M, and Mylan, and performed as a consultant for Boston Scientific, Cook Medical, and Pentax Medical. WJL received consultancy fees from Mediglobe. LMJWD received consultancy fees from Boston Scientific. DMJ declares that he does not have any conflict of interest. Cite Share Download PDF Status: Under Review Version 1 posted Reviews received at journal 23 Apr, 2026 Reviews received at journal 22 Apr, 2026 Reviews received at journal 16 Apr, 2026 Reviewers agreed at journal 11 Apr, 2026 Reviewers agreed at journal 09 Apr, 2026 Reviewers agreed at journal 07 Apr, 2026 Editor invited by journal 09 Mar, 2026 Reviewers invited by journal 11 Feb, 2026 Editor assigned by journal 04 Feb, 2026 Submission checks completed at journal 03 Feb, 2026 First submitted to journal 03 Feb, 2026 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-8700524","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":590088559,"identity":"4a80a26c-0fde-47ed-b787-3075113bf00b","order_by":0,"name":"Willem J. 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Bruno","email":"","orcid":"","institution":"Erasmus MC University Medical Center","correspondingAuthor":false,"prefix":"","firstName":"Marco","middleName":"J.","lastName":"Bruno","suffix":""},{"id":590088563,"identity":"f5d7b19c-21c0-41b2-89be-064f8f87209c","order_by":3,"name":"Lydi M.J.W. van Driel","email":"","orcid":"","institution":"Erasmus MC University Medical Center","correspondingAuthor":false,"prefix":"","firstName":"Lydi","middleName":"M.J.W. van","lastName":"Driel","suffix":""}],"badges":[],"createdAt":"2026-01-26 13:08:18","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-8700524/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-8700524/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":102828696,"identity":"170f68d8-3c17-4b6f-ba57-6f421b275fe4","added_by":"auto","created_at":"2026-02-17 09:25:49","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":168590,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cu\u003eOverview of all LN checked\u003c/u\u003e\u003c/p\u003e","description":"","filename":"1.png","url":"https://assets-eu.researchsquare.com/files/rs-8700524/v1/2f13f27ecaee081185ed83df.png"},{"id":102828959,"identity":"68efc9ec-40d8-47d0-829f-030823fe857d","added_by":"auto","created_at":"2026-02-17 09:26:53","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":443168,"visible":true,"origin":"","legend":"\u003cp\u003eA = station 9\u003c/p\u003e\n\u003cp\u003eB = station 16A1\u003c/p\u003e\n\u003cp\u003eC = station 16A2\u003c/p\u003e\n\u003cp\u003eD = station 11\u003c/p\u003e","description":"","filename":"2.png","url":"https://assets-eu.researchsquare.com/files/rs-8700524/v1/e93fa7cf1d411827abba10d3.png"},{"id":102828752,"identity":"80918335-733a-4b7b-bbc6-5c17dbaae70b","added_by":"auto","created_at":"2026-02-17 09:26:01","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":429381,"visible":true,"origin":"","legend":"\u003cp\u003eA = station 10\u003c/p\u003e\n\u003cp\u003eB = station 8A\u003c/p\u003e\n\u003cp\u003eC = station 8P\u003c/p\u003e\n\u003cp\u003eD = station 12A1/2\u003c/p\u003e","description":"","filename":"3.png","url":"https://assets-eu.researchsquare.com/files/rs-8700524/v1/64fe715ec0a7bd1fe012b904.png"},{"id":102828687,"identity":"7dd4b972-e18e-4279-8ce2-0ac9d7f86402","added_by":"auto","created_at":"2026-02-17 09:25:47","extension":"png","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":462575,"visible":true,"origin":"","legend":"\u003cp\u003eA = station 12A2\u003c/p\u003e\n\u003cp\u003eB = station 12B1 + station 12P1\u003c/p\u003e\n\u003cp\u003eC = station 12C\u003c/p\u003e\n\u003cp\u003eD = station 12\u003c/p\u003e","description":"","filename":"4.png","url":"https://assets-eu.researchsquare.com/files/rs-8700524/v1/d843623f63da8f02a08b2cdb.png"},{"id":102828700,"identity":"f173ea19-c3d3-4e6a-80f5-bbe986bfdaec","added_by":"auto","created_at":"2026-02-17 09:25:50","extension":"png","order_by":5,"title":"Figure 5","display":"","copyAsset":false,"role":"figure","size":339395,"visible":true,"origin":"","legend":"\u003cp\u003eA = station 14D\u003c/p\u003e\n\u003cp\u003eB = station 13A\u003c/p\u003e\n\u003cp\u003eC = station 13B\u003c/p\u003e","description":"","filename":"5.png","url":"https://assets-eu.researchsquare.com/files/rs-8700524/v1/3a6fae3eaaeed979625bb7f4.png"},{"id":102829031,"identity":"ea1b4e20-52c2-447f-aa93-36749a8f6de5","added_by":"auto","created_at":"2026-02-17 09:27:08","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":2578155,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-8700524/v1/8310c32d-cc09-47ae-8561-d7ff4c9019af.pdf"}],"financialInterests":"Competing interest reported. MJB reports research grants from Boston Scientific, Cook Medical, Pentax Medical, InterScope, 3M, and Mylan, and performed as a consultant for Boston Scientific, Cook Medical, and Pentax Medical. WJL received consultancy fees from Mediglobe. LMJWD received consultancy fees from Boston Scientific. DMJ declares that he does not have any conflict of interest.","formattedTitle":"A comprehensive guide to lymph node staging of cholangiocarcinoma by endoscopic ultrasound","fulltext":[{"header":"Introduction","content":"\u003cp\u003eSurgical resection or liver transplantation remains the only curative treatment option for patients with perihilar cholangiocarcinoma (pCCA) or intrahepatic cholangiocarcinoma (iCCA). In patients with regional or extraregional lymph node (LN) metastases however the potential benefit of surgery diminishes considerably and postoperative survival is poor (1-3). This makes accurate preoperative LN staging crucial for selecting appropriate candidates for curative intent therapies.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eRecently, the American Joint Committee on Cancer (AJCC) revised the definitions of nodal (N1, N2) and metastatic (M) disease in its staging system (4). These updates underscore the importance of precise LN assessment. For pCCA, LNs located beyond the hepatoduodenal ligament are now categorized as distant metastases, and N-stage is determined by the number of positive regional nodes rather than their anatomical location. In contrast, for iCCA the N and M categories depend on whether the tumor arises in the left or right hepatic lobe. Despite these refinements, cross-sectional imaging (CSI) continues to perform suboptimal in LN staging, with sensitivities and specificities of 61% and 88% for CT, 64% and 68% for MRI, and 33% and 97% for PET/CT, respectively (5-7).\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eGiven the limitations of CSI, there has been growing interest in endoscopic ultrasound (EUS) including EUS-guided tissue acquisition of LN as a more sensitive staging tool. The European Association for the Study of the Liver (EASL) guidelines on extrahepatic CCA (8) and intrahepatic CCA (9) are the first to systematically recommend preoperative EUS for LN staging. Despite significant interobserver agreement in defining suspicious or benign-looking LN (10), EUS has the potential to affect clinical decision making in 4-30% of patients (11-16). Even when CSI did not show suspicious LN, EUS still meaningfully impacted clinical decision making in a significant number of patients; either by detecting malignant LN, or by detection of other findings such as tumor invasion in the pancreas requiring a different treatment approach (11-16).\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eTo standardize LN terminology and improve communication across specialties, the Japanese Society of Hepato-Biliary-Pancreatic Surgery (JSHBPS) introduced the third edition of its classification of biliary tract cancers in 2015 (17). This system defines LN stations according to their relationship to key vascular landmarks (\u003cu\u003eFigure 1\u003c/u\u003e), much like Sharma et al. described EUS of the hepatoduodenal ligament (18). However, a corresponding EUS-based method for reliably identifying all important LN stations has not been established, creating a gap between radiologic, endosonographic, and surgical approaches.\u003c/p\u003e\n\u003cp\u003eTo address this need, the present article proposes a systematic EUS approach for identifying all LN stations relevant to pCCA and iCCA. By aligning EUS imaging with the JSHBPS classification, this method aims to enhance diagnostic accuracy and support optimal treatment planning. This systematic EUS evaluation is used in the POELH-I and POELH-II trial (Clinicaltrials.gov NCT05678218, registration date: 05-09-2022).\u0026nbsp;\u003c/p\u003e\n\n\n\n\n\n\n\n\n\n\n\n\n\n\n\n"},{"header":"Procedure ","content":"\u003cp\u003eLN evaluation is performed from three key locations within the gastrointestinal tract: the stomach, the duodenal bulb, and the second and third portions of the duodenum. From each of these vantage points, specific LN stations can be systematically assessed.\u003c/p\u003e\u003cp\u003eLNs are classified according to their relationship to adjacent vascular structures, as defined by the JSHBPS classification system. This can be challenging when a LN lies at an equal distance from two major vessels. In such cases, the LN may be assigned to both potential stations. A further challenge arises in the presence of vascular anatomical variants, for which no universal classification rules exists. These situations require careful interpretation and correlation with known vascular landmarks and discussion of relevant issues and deviations in the endoscopy report..\u003c/p\u003e\u003cp\u003eTo ensure that all relevant LN stations are evaluated, the examination is conducted in a stepwise and systematic manner, progressing through each anatomical window to minimize the risk of overlooking important nodal regions.\u003c/p\u003e\u003cp\u003eWe have used the linear EUS scope model EG38-J10UT (Pentax Medical, Tokyo, Japan) and color Doppler Machine Hitachi Arietta 850 for all evaluations.\u0026nbsp;\u003c/p\u003e"},{"header":"Stomach ","content":"\u003cp\u003e\u003cstrong\u003eLymph nodes along the celiac artery and abdominal aorta (stations 9, 16A1, 16A2, 16B1, 16B2)\u003c/strong\u003e\u0026nbsp;\u003c/p\u003e\u003cp\u003eFrom the gastro-esophageal junction, the abdominal aorta can be identified dorsally to the stomach. Just below the diaphragm, its first major branch can be identified: the celiac artery.\u0026nbsp;\u003c/p\u003e\u003cp\u003eStation 9 LNs are located above the celiac artery, below the diaphragm, and to the left of the abdominal aorta (\u003cu\u003eFigure 2A\u003c/u\u003e). In some cases, it may be challenging to distinguish station 9 nodes from station 16A1.\u0026nbsp;\u003c/p\u003e\u003cp\u003eLNs surrounding the abdominal aorta are collectively classified as station 16 and are further subdivided according to their anatomical relationship to major aortic branches.\u0026nbsp;\u003c/p\u003e\u003cp\u003eStation 16A1 LNs lie adjacent to the abdominal aorta, above the celiac artery, and between the aorta and the diaphragmatic crura. When a LN is located at an equal distance from the celiac trunk and the abdominal aorta, it may be described as station 9/16A1, following the principle that LNs are classified according to the vessel in closest proximity (\u003cu\u003eFigure 2B)\u003c/u\u003e.\u0026nbsp;\u003c/p\u003e\u003cp\u003eStation 16A2 LNs are located between the celiac trunk and the superior mesenteric artery (\u003cu\u003eFigure 2C\u003c/u\u003e).\u0026nbsp;\u003cbr\u003e\u0026nbsp;Station 16B1 LNs lie between the superior mesenteric artery and the inferior mesenteric artery, whereas station 16B2 nodes are situated below the inferior mesenteric artery. Substations that are located further down alongside the aorta are not consistently visible from the stomach, often due to patient-related factors such as decreased echogenicity or the presence of a hiatal hernia.\u0026nbsp;\u003c/p\u003e\u003cp\u003e\u003cstrong\u003eLymph nodes along the superior mesenteric artery (stations 14P and 14D)\u003c/strong\u003e\u0026nbsp;\u003c/p\u003e\u003cp\u003eFrom the abdominal aorta, the superior mesenteric artery can be followed until its first major branch, the middle colic artery, which typically curves toward the pancreatic body (towards the EUS probe). This segment, from its origin to the middle colic artery, can be divided into two equal parts: station 14P, comprising LNs along the proximal half closest to the origin of the superior mesenteric artery, and station 14D, comprising LNs along the distal half closest to the middle colic artery. These LN stations can also be visualized from the duodenum (see the section on assessment from the duodenum).\u0026nbsp;\u003c/p\u003e\u003cp\u003e\u003cstrong\u003eLymph nodes along the splenic artery and splenic hilum (stations 10 and 11)\u003c/strong\u003e\u0026nbsp;\u003c/p\u003e\u003cp\u003eAfter arising from the aorta, the celiac trunk divides into the common hepatic artery and the splenic artery. The splenic artery follows a characteristically tortuous course along the pancreatic body and tail toward the splenic hilum.\u0026nbsp;LNs distributed along the splenic artery are classified as station 11 (\u003cu\u003eFigure 2D\u003c/u\u003e), whereas LNs clustered within the splenic hilum are classified as station 10 (\u003cu\u003eFigure 3A\u003c/u\u003e).\u0026nbsp;\u003c/p\u003e\u003cp\u003e\u003cstrong\u003eLymph nodes along the hepatic artery and hepatoduodenal ligament (stations 8 and 12)\u003c/strong\u003e\u0026nbsp;\u003c/p\u003e\u003cp\u003eFrom the celiac trunk bifurcation, the common hepatic artery can be traced towards the liver hilum.\u0026nbsp;\u003cbr\u003eAlong this course, LNs are classified according to their relationship with the artery and the EUS-probe. Station 8A LNs are located between\u003cem\u003e\u0026nbsp;\u003c/em\u003ethe vessel and the EUS probe (\u003cu\u003eFigure 3B\u003c/u\u003e).\u0026nbsp;Station 8P LNs are located between the common hepatic artery and the portal vein (\u003cu\u003eFigure 3C\u003c/u\u003e).\u0026nbsp;\u003c/p\u003e\u003cp\u003eAs the common hepatic artery is traced distally, the vessel divides into the gastroduodenal artery and the proper hepatic artery. The proper hepatic artery together with the portal vein and the extrahepatic bile duct, form the portal triad; LNs in this region are classified as station 12.\u0026nbsp;\u003c/p\u003e\u003cp\u003eStation 12 LNs are further subdivided according to their proximity to adjacent anatomical landmarks:\u0026nbsp;12A: along the proper hepatic artery (\u003cu\u003eFigure 3D and 4A\u003c/u\u003e), 12P: along the portal vein, 12B: along the extrahepatic bile duct (\u003cu\u003eFigure 4B\u003c/u\u003e), 12C: along the cystic duct (\u003cu\u003eFigure 4C\u003c/u\u003e). Each subgroup is additionally divided based on whether the nodes are closer to the liver hilum (e.g., 12A1, 12P1, 12B1) or the pancreas (e.g., 12A2, 12P2, 12B2), with the insertion of the cystic duct as the border (\u003cu\u003eFigure 4D\u003c/u\u003e). LNs located above the bifurcation of the extrahepatic bile duct into left and right hepatic ducts are designated 12H.\u0026nbsp;\u003c/p\u003e\u003cp\u003eIt should be emphasized that LNs in stations 8 and 12 may not always be clearly distinguishable based on anatomic landmarks, particularly in the presence of vascular variants.\u0026nbsp;\u003c/p\u003e\u003cp\u003e\u003cstrong\u003eLymph nodes around the pancreas (station 18)\u003c/strong\u003e\u0026nbsp;\u003c/p\u003e\u003cp\u003eAll LNs located below the pancreatic body or tail are classified as station 18 (as seen from the stomach).\u0026nbsp;\u003c/p\u003e"},{"header":"Duodenal bulb ","content":"\u003cp\u003e\u003cstrong\u003eLymph nodes along the hepatic artery and hepatoduodenal ligament (stations 8 and 12)\u003c/strong\u003e\u0026nbsp;\u003c/p\u003e\u003cp\u003eAll LNs located along the hepatic artery and within the hepatoduodenal ligament that are visualized from the stomach can also be evaluated from the duodenal bulb. For the description of subclassifications of these stations, see the section from the stomach. Importantly, LNs that are not accessible for EUS-guided sampling from the stomach often become accessible from the duodenal bulb because in this position, the extrahepatic bile duct lies closer to the transducer, whereas from the stomach the portal vein and hepatic artery are typically in closer proximity to the probe.\u0026nbsp;\u003c/p\u003e\u003cp\u003e\u003cstrong\u003eDuodenum\u003c/strong\u003e\u0026nbsp;\u003c/p\u003e\u003cp\u003eSeveral LN stations can be visualized from different portions of the duodenum, including stations 13, 14, 15, 16, 17 and 18.\u0026nbsp;\u003c/p\u003e\u003cp\u003e\u003cstrong\u003eLymph nodes along the posterior (station 13A and 13B) and anterior (stations 17A and 17B) surface of the pancreatic head\u003c/strong\u003e\u003c/p\u003e\u003cp\u003eStations 13 and 17 correspond to LNs located along the posterior and anterior surfaces of the pancreatic head, respectively. Station 13 LNs are situated posterior to the pancreatic head, in the space between the pancreas and the inferior vena cava and the aorta. In contrast, station 17 LNs are located along the anterior surface of the pancreatic head, interposed between the pancreas and the gastroduodenal artery as well as the anterior superior pancreaticoduodenal vessels.\u0026nbsp;\u003c/p\u003e\u003cp\u003eThe subdivision into A and B reflects the cranio-caudal relationship to the duodenal papilla: stations 13A and 17A are positioned proximal to the papilla, whereas stations 13B and 17B are located distal to it (\u003cu\u003eFigure 5B + C\u003c/u\u003e).\u003c/p\u003e\u003cp\u003e\u003cstrong\u003eLymph nodes along the superior mesenteric artery (stations 14P and 14D)\u003c/strong\u003e \u003cstrong\u003eand within the transverse mesocolon (station 15)\u003c/strong\u003e\u003c/p\u003e\u003cp\u003eStation 14 and 15 comprise LNs along the superior mesenteric artery and within the transverse mesocolon, respectively. From the second part of the duodenum, the aorta is first identified. With gradual clockwise rotation, the uncinate process comes into view, followed by the mesenteric vessels. These mesenteric vessels are visualized as parallel longitudinal structures, with the superior mesenteric vein closer to the probe than the superior mesenteric artery. The middle colic artery represents the first main branch of the superior mesenteric artery, often coursing in the direction of the probe. Station 14P LNs can be identified to the left of the MCA on the EUS screen around the superior mesenteric artery, in the direction of the aortic origin, whereas station 14D LNs are located to the right of the middle colic artery (\u003cu\u003eFigure 5A\u003c/u\u003e).\u0026nbsp;\u003c/p\u003e\u003cp\u003eStation 15 LNs are associated with the transverse mesocolon, particularly along the trajectory of the middle colic artery as it travels toward the transverse colon.\u0026nbsp;Tracing the superior mesenteric artery until the middle colic artery branches to the right. The fat plane around the middle colic artery is where station 15 LNs can be identified.\u003c/p\u003e\u003cp\u003eStation 14 and 15 LNs may be more challenging to visualize, because of their distance from the duodenal lumen, overlying bowel gas, patient anatomy, and variable mesenteric fat. Their identification often requires subtle probe rotation and optimized Doppler imaging.\u0026nbsp;\u003c/p\u003e\u003cp\u003e\u003cstrong\u003eLymph nodes along the abdominal aorta (station 16) and around the pancreas (station 18)\u003c/strong\u003e\u0026nbsp;\u003c/p\u003e\u003cp\u003eFrom the third part of the duodenum, para-aortic LNs of station 16 can also be visualized.\u0026nbsp;This position can facilitate tissue acquisition in situations where sampling from the stomach is not possible.\u003c/p\u003e\u003cp\u003eStation 18 LNs are retroperitoneal LNs situated along the caudal border of the pancreatic body and partly tail. These LN can be observed from the third part of the duodenum, anterior to the superior mesenteric vessel, just below the point where it crosses the uncinate process of the pancreas. These LNs are more easily biopsied from the duodenum than from the stomach, as the pancreatic body or tail lies between the probe and the LNs when approached from the stomach.\u0026nbsp;\u003c/p\u003e\u003cp\u003eAccording to the AJCC, regional LN stations for pCCA are 8, 12 and 13, and for right sided iCCA are considered at stations 8, 12, 13 and 17. The AJCC does not explicitly list this, but depending on surgical series, station 14P LN may sometimes be considered regional because they drain the same lymphatic basin (\u003cu\u003eTable 1\u003c/u\u003e). Left-sided iCCA tumors have additional drainage via the lesser omentum toward the left gastric artery (station 7 according to the Japanese classification). Therefore, regional LN stations for left-sided iCCA tumors are considered at stations 8, 12, and 7. \u0026nbsp;\u003c/p\u003e"},{"header":"Discussion","content":"\u003cp\u003eThis paper provides a structured, EUS-based approach to identifying all LN stations relevant to pCCA and iCCA, using the JSHBPS classification as a detailed anatomical framework. By systematically describing EUS views from the stomach, duodenal bulb, and distal duodenum, we illustrate how both regional and extraregional LN stations can be systematically evaluated. Importantly, the approach allows endosonographers to distinguish between LNs that fall within the AJCC-defined regional and extraregional locations. Accurate classification of LNs is essential, as involvement of extraregional LNs represents distant (M1) disease and typically precludes patients from curative resection or liver transplantation protocols.\u003c/p\u003e \u003cp\u003eBy integrating EUS imaging with established surgical anatomy, this systematic approach offers a practical framework that may enhance diagnostic accuracy and improve multidisciplinary communication among radiology, endoscopy, and hepatobiliary surgery teams. Further prospective studies are warranted to evaluate the impact of standardized EUS-based LN mapping on clinical decision-making, patient selection for resection or transplantation, and long-term oncological outcomes.\u003c/p\u003e"},{"header":"Abbreviations","content":"\u003ctable border=\"1\" cellspacing=\"0\" cellpadding=\"0\" width=\"603\"\u003e\n \u003ctbody\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 84px;\"\u003e\n \u003cp\u003e\u0026nbsp;pCCA\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 519px;\"\u003e\n \u003cp\u003ePerihilar Cholangiocarcinoma\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 84px;\"\u003e\n \u003cp\u003eiCCA\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 519px;\"\u003e\n \u003cp\u003eIntrahepatic Cholangiocarcinoma\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 84px;\"\u003e\n \u003cp\u003eLN\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 519px;\"\u003e\n \u003cp\u003eLymph Node\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 84px;\"\u003e\n \u003cp\u003eEUS\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 519px;\"\u003e\n \u003cp\u003eEndoscopic Ultrasound\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 84px;\"\u003e\n \u003cp\u003eAJCC\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 519px;\"\u003e\n \u003cp\u003eAmerican Joint Committee on Cancer\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 84px;\"\u003e\n \u003cp\u003eCT\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 519px;\"\u003e\n \u003cp\u003eComputed Tomography-scan\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 84px;\"\u003e\n \u003cp\u003eMRI\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 519px;\"\u003e\n \u003cp\u003eMagnetic Resonance Imaging\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 84px;\"\u003e\n \u003cp\u003ePET\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 519px;\"\u003e\n \u003cp\u003ePositron Emission Tomography\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 84px;\"\u003e\n \u003cp\u003eCSI\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 519px;\"\u003e\n \u003cp\u003eCross-sectional Imaging\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 84px;\"\u003e\n \u003cp\u003eJSHBPS\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 519px;\"\u003e\n \u003cp\u003eJapanese Society of Hepato-Biliary-Pancreatic Surgery\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 84px;\"\u003e\n \u003cp\u003eN-stage\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 519px;\"\u003e\n \u003cp\u003eLymph node stage\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 84px;\"\u003e\n \u003cp\u003eM-stage\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 519px;\"\u003e\n \u003cp\u003eMetastatic disease stage\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tbody\u003e\n\u003c/table\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eEthics approval and consent to participate:\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe images and figures are selected from the POELH-II trial. This trial received approval from IRB approval code MEC-2022-0402 (Ethical committee from the Erasmus MC University Medical Center). This trial was conducted in compliance with the Helsinki declaration and patients provided written informed consent (Clinicaltrials.gov NCT05678218, registration date: 05-09-2022).\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConsent for publication:\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAvailability of data and materials:\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAll data generated or analysed during this study are included in this published article. Data on the POELH-I and POELH-II trials will be published separately.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCompeting interests:\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eMJB reports research grants from Boston Scientific, Cook Medical, Pentax Medical, InterScope, 3M, and Mylan, and performed as a consultant for Boston Scientific, Cook Medical, and Pentax Medical. WJL received consultancy fees from Mediglobe. LMJWD received consultancy fees from Boston Scientific. DMJ declares that he does not have any conflict of interest.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding:\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors did not receive any financial support to produce this manuscript.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAuthors\u0026rsquo; contributions:\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eWJL, DMJ, LMJWD: Initial draft, revision, editing and final approval. MJB: revision and final approval.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAcknowledgements:\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eBlechacz B, Cholangiocarcinoma. Current Knowledge and New Developments. Gut Liver. 2017;11(1):13\u0026ndash;26.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eJolissaint JS, Soares KC, Seier KP, Kundra R, G\u0026ouml;nen M, Shin PJ, et al. Intrahepatic Cholangiocarcinoma with Lymph Node Metastasis: Treatment-Related Outcomes and the Role of Tumor Genomics in Patient Selection. Clin Cancer Res. 2021;27(14):4101\u0026ndash;8.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eRadtke A, Konigsrainer A. Surgical Therapy of Cholangiocarcinoma. Visc Med. 2016;32(6):422\u0026ndash;6.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eAmin MB, Greene SEF, Byrd DR, Brookland RK, Washington MK. American joint committee on cancer: Cancer staging manual. 8 ed. New York: Springer International Publishing; 2017. pp. 295\u0026ndash;301.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eRuys AT, van Beem BE, Engelbrecht MR, Bipat S, Stoker J, Van Gulik TM. Radiological staging in patients with hilar cholangiocarcinoma: a systematic review and meta-analysis. Br J Radiol. 2012;85(1017):1255\u0026ndash;62.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eHanninen EL, Pech M, Jonas S, Ricke J, Thelen A, Langrehr J, et al. Magnetic resonance imaging including magnetic resonance cholangiopancreatography for tumor localization and therapy planning in malignant hilar obstructions. Acta Radiol. 2005;46(5):462\u0026ndash;70.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eFurukawa H, Ikuma H, Asakura-Yokoe K, Uesaka K. Preoperative staging of biliary carcinoma using 18F-fluorodeoxyglucose PET: prospective comparison with PET\u0026thinsp;+\u0026thinsp;CT, MDCT and histopathology. Eur Radiol. 2008;18(12):2841\u0026ndash;7.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMarzioni M, Maroni L, Aabakken L, Carpino G, Groot Koerkamp B, Heimbach J, et al. EASL Clinical Practice Guidelines on the management of extrahepatic cholangiocarcinoma. J Hepatol. 2025;83(1):211\u0026ndash;38.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eAlvaro D, Gores GJ, Walicki J, Hassan C, Sapisochin G, Komuta M, et al. EASL-ILCA Clinical Practice Guidelines on the management of intrahepatic cholangiocarcinoma. J Hepatol. 2023;79(1):181\u0026ndash;208.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003ede Jong DM, Roosterman D, Bruno MJ, van Driel LMJW, Lammers WJ. Interobserver variability in lymph node evaluation with endoscopic ultrasonography in cholangiocarcinoma. Endosc Int Open. 2025;13(continuous publication).\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eGleeson FC, Rajan E, Levy MJ, Clain JE, Topazian MD, Harewood GC, et al. EUS-guided FNA of regional lymph nodes in patients with unresectable hilar cholangiocarcinoma. Gastrointest Endosc. 2008;67(3):438\u0026ndash;43.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMalikowski T, Levy MJ, Gleeson FC, Storm AC, Vargas EJ, Topazian MD, et al. Endoscopic Ultrasound/Fine Needle Aspiration Is Effective for Lymph Node Staging in Patients With Cholangiocarcinoma. Hepatology. 2020;72(3):940\u0026ndash;8.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003ede Jong DM, den Hoed CM, Willemssen FEJA, Thomeer MGJ, Bruno MJ, Koerkamp BG, et al. Impact of EUS in liver transplantation workup for patients with unresectable perihilar cholangiocarcinoma. Gastrointest Endosc. 2024;99(4):548\u0026ndash;56.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003ede Jong DM, van de Vondervoort S, Dwarkasing RS, Doukas M, Voermans RP, Verdonk RC, et al. Endoscopic ultrasound in patients with resectable perihilar cholangiocarcinoma: impact on clinical decision-making. Endosc Int Open. 2023;11(2):E162\u0026ndash;8.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003ede Jong DM, van de Vondervoort S, Dwarkasing RS, Thomeer MGJ, Doukas M, Voermans RP, et al. Endoscopic ultrasound with tissue acquisition of lymph nodes in patients with potentially resectable intrahepatic cholangiocarcinoma. Endosc Int Open. 2024;12(08):E998\u0026ndash;1005.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003ede Jong DM, van Driel LMJW, Lakhtakia S, Ramchandani M, Fathima Memon S, Tyagi A, et al. Endoscopic Ultrasound for Nodal Staging in Patients with Resectable Cholangiocarcinoma. J Clin Med. 2025;14(21):7545.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMiyazaki M, Ohtsuka M, Miyakawa S, Nagino M, Yamamoto M, Kokudo N, et al. Classification of biliary tract cancers established by the Japanese Society of Hepato-Biliary-Pancreatic Surgery: 3(rd) English edition. J Hepatobiliary Pancreat Sci. 2015;22(3):181\u0026ndash;96.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSharma M, Rameshbabu CS, Dietrich CF, Rai P, Bansal R. Endoscopic ultrasound of the hepatoduodenal ligament and liver hilum. Endosc Ultrasound. 2018;7(3):168\u0026ndash;74.\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"},{"header":"Table","content":"\u003cp\u003eTable 1. Overview of the regional and extraregional LN\u003c/p\u003e\n\u003ctable border=\"1\" cellspacing=\"3\" cellpadding=\"0\" width=\"631\"\u003e\n \u003cthead\u003e\n \u003ctr\u003e\n \u003ctd\u003e\n \u003cp\u003e\u003cstrong\u003eJapanese LN Station\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003e\u003cstrong\u003eAnatomical Region\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003e\u003cstrong\u003eiCCA (left)\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e\u003cstrong\u003eiCCA (right)\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e\u003cstrong\u003epCCA\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e\u003cstrong\u003edCCA\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003c/thead\u003e\n \u003ctbody\u003e\n \u003ctr\u003e\n \u003ctd\u003e\n \u003cp\u003e\u003cstrong\u003e8A/8P\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003eCommon hepatic artery\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003eR\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eR\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eR\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eR\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd\u003e\n \u003cp\u003e\u003cstrong\u003e12A/P/B/C/H\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003eHepatoduodenal ligament\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003eR\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eR\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eR\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eR\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd\u003e\n \u003cp\u003e\u003cstrong\u003e13A/B\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003ePosterior pancreatic head\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eR\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eR\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eR\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd\u003e\n \u003cp\u003e\u003cstrong\u003e17A/B\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003eAnterior pancreatic head\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eR\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eR\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd\u003e\n \u003cp\u003e\u003cstrong\u003e14P\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003eProximal superior mesenteric artery\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eR\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd\u003e\n \u003cp\u003e\u003cstrong\u003e14D\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003eDistal superior mesenteric artery\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eR\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd\u003e\n \u003cp\u003e\u003cstrong\u003e9\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003eCeliac axis\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd\u003e\n \u003cp\u003e\u003cstrong\u003e10\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003eSplenic hilum\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd\u003e\n \u003cp\u003e\u003cstrong\u003e11\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003eSplenic artery\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd\u003e\n \u003cp\u003e\u003cstrong\u003e15\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003eTransverse mesocolon\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd\u003e\n \u003cp\u003e\u003cstrong\u003e16A1/A2/B1/B2\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003ePara-aortic\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd\u003e\n \u003cp\u003e\u003cstrong\u003e18\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003eInferior pancreatic body border\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eER\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tbody\u003e\n\u003c/table\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"bmc-gastroenterology","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"bmge","sideBox":"Learn more about [BMC Gastroenterology](http://bmcgastroenterol.biomedcentral.com/)","snPcode":"","submissionUrl":"https://www.editorialmanager.com/bmge/default.aspx","title":"BMC Gastroenterology","twitterHandle":"BMC_series","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"em","reportingPortfolio":"BMC Series","inReviewEnabled":true,"inReviewRevisionsEnabled":true},"keywords":"Endoscopic ultrasound, perihilar cholangiocarcinoma, intrahepatic cholangiocarcinoma, lymph node","lastPublishedDoi":"10.21203/rs.3.rs-8700524/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-8700524/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eAccurate lymph node (LN) staging is critical for treatment planning in patients with perihilar cholangiocarcinoma (pCCA) and intrahepatic cholangiocarcinoma (iCCA). Cross-sectional imaging however has limited sensitivity for detecting LN metastases. Recent studies have demonstrated that endoscopic ultrasound (EUS) offers additional value in LN assessment for both pCCA and iCCA. Despite its advantages, reliably identifying the individual LN stations relevant to these malignancies can be challenging and requires detailed knowledge of regional anatomy. This article provides a standardized, systematic guide for identifying all major LN stations associated with pCCA and iCCA using linear EUS, with the aim of improving preoperative staging and optimizing treatment planning.\u003c/p\u003e","manuscriptTitle":"A comprehensive guide to lymph node staging of cholangiocarcinoma by endoscopic ultrasound","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2026-02-17 09:23:25","doi":"10.21203/rs.3.rs-8700524/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"editorInvitedReview","content":"","date":"2026-04-23T17:43:46+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2026-04-22T08:28:46+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2026-04-16T16:59:04+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"77325206775649058204874002547809200057","date":"2026-04-11T08:17:11+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"184102115463202256703675309581322417759","date":"2026-04-09T07:28:47+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"206080707375826872566305370053154380786","date":"2026-04-07T18:52:43+00:00","index":"hide","fulltext":""},{"type":"editorInvited","content":"","date":"2026-03-09T10:12:35+00:00","index":"","fulltext":""},{"type":"reviewersInvited","content":"","date":"2026-02-11T08:01:38+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2026-02-04T07:14:22+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2026-02-03T13:06:50+00:00","index":"","fulltext":""},{"type":"submitted","content":"BMC Gastroenterology","date":"2026-02-03T12:23:17+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"bmc-gastroenterology","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"bmge","sideBox":"Learn more about [BMC Gastroenterology](http://bmcgastroenterol.biomedcentral.com/)","snPcode":"","submissionUrl":"https://www.editorialmanager.com/bmge/default.aspx","title":"BMC Gastroenterology","twitterHandle":"BMC_series","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"em","reportingPortfolio":"BMC Series","inReviewEnabled":true,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"49355e8d-a215-41fa-9140-ac660e71d92a","owner":[],"postedDate":"February 17th, 2026","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"under-review","subjectAreas":[],"tags":[],"updatedAt":"2026-02-17T09:23:26+00:00","versionOfRecord":[],"versionCreatedAt":"2026-02-17 09:23:25","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-8700524","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-8700524","identity":"rs-8700524","version":["v1"]},"buildId":"XKTyCvWXoU3ODBz1xrDgd","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}