Etiology of Bile Duct Injuries During Laparoscopic Cholecystectomy

Etiology of Bile Duct Injuries During Laparoscopic Cholecystectomy | 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 Article Etiology of Bile Duct Injuries During Laparoscopic Cholecystectomy Prishita Banerji, Yajjat Garg This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-7797632/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract Introduction : Laparoscopic cholecystectomy (LC) is a surgical procedure indicated for the treatment of medical conditions involving the removal of a diseased gallbladder. One of the most common and severe complication of laparoscopic cholecystectomy (LC) is bile duct injury (BDI). In such a widely performed procedure it is imperative to understand the etiology as well as any underlying risk factors that may lead to BDI. The Aim : To assess and analyse the various causes and trends in the incidence and risk factors of bile duct injuries during a period of 25 years . Materials and Methods : We performed a retrospective cohort study involving 120 patients who underwent LC over a period of 25 years from 1994 till 2024, divided into 2 groups to analyse the changing trends over the course of time. Socio-demographic and clinical data was collected, the most statistically significant parameters included gender, anatomic anomalies, number of laparoscopic cholecystectomies performed by the surgeon, intraoperative cholangiography as a method of diagnosis as well as cause of the operation. Results : We found that 38 patients developed bile duct injury in the period of first five years from 1999–2004 (31.6%) while 23 patients developed bile duct injury in the period of last five years from 2019–2024 (19.1%). Acute cholecystitis was found to be leading risk factor in (47.40%) cases in first group and 56.20% cases in the second group. 88% patients developing BDI were female. Experience of surgeon reporting bile duct injury varied from less than 25 procedures performed (1999–2004) to more than 100 procedures performed (2019–2024). Conclusion : Our study indicates that proper training and experience of surgeons is a key determinant in development of BDI. Acute cholecystitis was recognised as a high risk factor that leads to complications during LC. The routine use of intra-operative cholangiography are the best methods currently available for timely identifying and hopefully preventing bile duct injuries during laparoscopic cholecystectomy. Health sciences/Diseases Health sciences/Gastroenterology Health sciences/Medical research Health sciences/Risk factors bile duct injury laparoscopic cholecystectomy prevention management Figures Figure 1 Figure 2 Figure 3 Figure 3 Introduction Laparoscopic cholecystectomy (LC) is the most commonly performed procedure in the field of digestive surgery as well as general surgery with 1.3 million of these procedures performed in the United States in 2021[1]. It is a surgical procedure involving the removal of a diseased gallbladder, indicated for the treatment of medical conditions such as cholecystitis (acute/chronic), symptomatic cholelithiasis, biliary dyskinesia, calculous and acalculous cholecystitis, gallstone pancreatitis, gallbladder masses/polyps and gallbladder cancer. First introduced in 1990 by Dubois et al.[2],Laparoscopic cholecystectomy has largely replaced open cholecystectomy as the standard of care for gallbladder excision. With advancements in medical techniques, it rapidly spread as a better and safer alternative to Open cholecystectomy (OC) for its minimally invasive nature as well as robust outcomes. The benefits of LC over open cholecystectomy derive from less operative trauma and ileus with minimum pain, short hospital stay and a reduced period of short-term disability with rapid return to full activity or work. Other benefits include decreased formation of intra-peritoneal adhesions and wound-related complications[3]. LC also replaced other modalities for therapy of symptomatic gallstone disease practised during the 1970s and 80s, such as extracorporeal shock-wave lithotripsy and chemical (bile salt) dissolution therapy. LC thus gained rapid and widespread acceptance among patients and surgeons before its effectiveness and safety were established[4]. Once the global expansion of the procedure was established, the question of possible complications during the procedure came to light over a period of time. One of the most common and severe complication of laparoscopic cholecystectomy (LC) being Bile duct injury (BDI)[5]. The scope of the injury can range from a simple cystic duct leak to the injury of the left and right hepatic duct confluence. The early and accurate diagnosis of BDI is very important for surgeons and gastroenterologists, because unrecognised BDI lead to serious complications such as biliary cirrhosis, hepatic failure and ultimately death[6][7].BDI is in direct correlation with surgical experience and knowledge of cholecystectomy albeit despite the evolution of surgical techniques and approaches, bile duct injury represents a significant complication, even in experienced hands. Past studies in the last three decades stated that the incidence of BDI after laparoscopic cholecystectomy (LC) was significantly greater than that after open cholecystectomy (OC) (0.4–0.6% and 0.1–0.2%, respectively). This was corresponding to the emergence of the laparoscopic technique in that era[8][9].However, Later studies found a considerable decline in the incidence of BDIs after LC, to around 0.2%, due to the improved surgical laparoscopic experience[10].Aside from patient morbidity and mortality, Bile duct injuries pose serious health and economic problems as they expose the surgeon to expensive medico-legal litigation. In addition, they increase substantially the economic burden to the patient, hospital and community, and some patients have needed hepatic transplantation for survival[11]. With the steady increase in cases of gall bladder pathology in recent years, it is inevitable that the number of laparoscopic cholecystectomies being performed are bound to rise in the upcoming years. And an increase in procedures ultimately ties in with an increased risk of complications as well. Thus, it is imperative to understand the etiology as well as any underlying risk factors that may lead to BDI in cases of LC to help prevent such a complication and appropriately adapt the preoperative and postoperative care of patients accordingly. Our current study aimed to assess and analyse the various causes and trends in the incidence and risk factors of bile duct injuries during the period of 25 years. Methods We performed a retrospective cohort study involving 120 patients over a period of 25 years from 1994 till 2024 to analyse the changing trends over the course of time. Subjects who were included in the database of the study were patients who were treated surgically for bile duct injuries during laparoscopic cholecystectomies. These included patients who were originally treated at the Digestive Surgery Clinic at the University Clinical Center of Nis as well as patients who were referred from 18 regional hospitals and tertiary Hepato-billiary centers. We divided the data sets into two groups (Group A and Group B) to analyse the trends over the course of two different decades. Group A included 38 patients who developed BDI in the first five year period from 1999 to 2004. Group B included 23 patients who developed BDI in the last five year period from 2019 to 2024. We collected socio-demographic and clinical data, the most statistically significant parameters included gender, anatomic anomalies, number of laparoscopic cholecystectomies performed by the surgeon, intraoperative cholangiography as a method of diagnosis as well as cause of the operation. The study was approved by the Ethical Board of the University Clinical Centre Nis. All procedures were performed following the Boards' guidelines and regulations. All participants provided written informed consent. The research results are presented in tabular and graphic form. P values of less than 0.05 were regarded as statistically significant. Numerical data were presented as percentage Results We found that 38 patients developed bile duct injury during laparoscopic cholecystectomy in the period of first five years from 1999–2004 (31.6%) and 23 patients developed bile duct injury during laparoscopic cholecystectomy in the period of last five years from 2019–2024 (19.1%). It was found that 88% of the cases of BDI were reported in women while 12% of the cases were reported in men presented in Fig. 1 . The number of LC performed i.e experience of the surgeon prior to performing the LC that lead to BDI in both groups is presented in Figure.2. In Group A (1999–2004) Surgeons reported the most BDI in their first 25 LC procedures and second most during their first 50 and after 200 LC procedures. While in Group B (2019–2024), Surgeons reported fewer BDI during their first 50 LC. The most BDI were reported after 100 LC procedures in Group B. Indications for the LC leading to most BDI are presented in the Figure.3 We found that BDI was more prevalent in LC done for Acute cholecystitis in both groups accounting for 47.40% (~ 18 cases out of 38) of BDI in Group A and 56.20% (~ 13 cases out of 23) of BDI in Group B. While the least number of BDI were seen in LC performed for Simple lithiasis accounting for 18.40% (~ 7 cases out of 38) of BDI in Group A and 17.40% (~ 4 cases out of 23) of BDI in Group B. Real anatomical anomalies were found to be an insignificant cause with only 2 cases or 3.27% of BDI reported in both groups combined. The BDI was recognised intraoperative in only 21% (13 out of 61) of cases. Out of which diagnosis based on Intraoperative cholangiography(IOCH) included 6 out of those 13 cases which makes the positive predictive value of IOCH as 46% presented in Table.1. Discussion Biliary duct injury is the most complication of laparoscopic cholecystectomies however, with the increasing knowledge of gallbladder surgeries, the incidence of such complications seems to be significantly decreasing. On account of the increased surgical skills in LC, Halbert et al. concluded that the overall rate of LC has declined to around 0.2% [12]. Our results also suggest that there is a significant declining trend in the the incidence of BDI during LC over the period of last 25 years from 31.6% to 19.1%. The etiology of BDI in the cases that occurred pointed to some key risk factors. The reported frequencies of BDI was unanimously greater in women than in men in both periods of the study making gender of the patient a statistically and clinically significant determinant of BDI development. Surgical experience played a significant role in determining whether a LC may lead to BDI in Group A but not so much in Group B which poses a question of whether causing a BDI is the product of a surgeons skill and experience or a chance happening which may occur even after a surgeon has been well adept to the procedure. It should be noted that medical techniques and equipment are being steadily updated and improvised so it is a possibility that in the earlier years, the technique of the procedure required rigorous practice and precision to prevent BDI however in current years with greater advancements and multiple approaches of beginner and advanced surgeons, number of LC performed may not be a good determinant. There is also an alternate possibility once a surgeon isn’t novice to the procedure, if not careful, a level of complacency could be expected as reported in Group B leading to more BDI among surgeons even after their first 100 or 200 LC procedures. Many studies in the literature agree that the most important factor that decreases the rate of BDI is surgical skill and knowledge in the prevention of BDI. All surgeons must be oriented with a critical view of safety (CVS), respect the Calot’s triangle during dissection of the Calot’s triangle, and be oriented and prepared with all possible biliary tree and hepatic artery anomalies. Disregarding the CVS, the use of thermal hemostats close to the main biliary system, or strenuous traction on the cystic duct is associated with high rates of BDI [13, 14] Acute cholecystitis was and still continues to be a major determinant of LC leading to BDI. In both the groups, majority of LC performed due to acute cholecystitis lead to BDI. Anomalies and anatomical variations of biliary ducts or vascular system were seen as rare and played an insignificant role in assessment of BDI etiology. BDIs are detected in different frames of time. The earlier the timing of detection, the better the outcomes for the patient [15,16].Iatrogenic injuries to the common hepatic duct or right hepatic duct with side branches are normally severe requiring immediate operative management. A well-timed planned operation and extensive surgical repair may help fair better outcomes and ensure long-term quality of life. The reason for performing IOC is to avoid and detect bile duct injuries as well as discovering stones in the common bile duct. Intraoperative detection of BDI is not an easy task; however, if it occurs, surgeons must be aware of what to do next. The use of intraoperative cholangiography (IOC), have been proven to facilitate the detection of challenging biliary anatomy and detect BDI intra-operatively but is not nearly performed as adequately as it should as for patients with suspected BDI, ultrasound remains the most used initial investigation as it diagnoses intra-peritoneal collections and biliary and intra-hepatic dilatation [17]. However, there is no consensus, on the routine usage of these techniques in cholecystectomies [18, 19]. A Meta-analysis undergone on 2,059 articles to evaluate the use of IOC, stated that BDI rates are lower with IOC than without IOC (depending only on the anatomical description) [20]. In our study as well, 46% of BDI diagnosed intra-operatively were recognised via IOC thus showing the benefit of IOC as a diagnostic tool to help prevent and diagnose BDI. It should be noted that the study has limitations due to its retrospective nature and the small sample size, which is a result of the limited number of cases referred to a single unit, and the decreased incidence of the condition. Furthermore, most of the cases reported were referred from another hospital with no surgical report, which limited the intraoperative data, especially the mechanism of injury. Conclusion Laparoscopic cholecystectomy is a widely performed procedure and though the complications related to the procedure has significantly reduced in recent times, there is still scope for improvement in understanding and preventing bile duct injuries during the surgery. This study serves to bring to light the most common causes and underlying risk factors that may lead to bile duct injuries during laparoscopic cholecystectomy. It is essential to carefully assess the patient profile and demographic prior to the surgery to estimate outcomes. Surgeons must be aware of primary diagnostic and preventative techniques and regularly improve their knowledge regarding laparoscopic surgeries, both to prevent BDI and avoid the accumulation of the risk of patient morbidity and mortality. In conclusion, in accordance with the parameters assessed in this study, proper training and experience of surgeons, identifying acute cholecystitis as a high-risk factor and routine use of intraoperative cholangiography are the best methods currently available for timely identifying and hopefully preventing Bile duct injuries during laparoscopic cholecystectomy. Declarations Author Contribution P.B and Y.G wrote the main manuscript text and P.B prepared figures and table. All authors reviewed the manuscript. References Tsui C., Klein R., Garabrant M. Minimally invasive surgery: national trends in adoption and future directions for hospital strategy. Surg Endosc. 2013;27:2253–2257. doi: 10.1007/s00464-013-2973-9. Deziel D. J., Millikan K. W., Economou S. G., Doolas A., Ko S. T., Airan M. C. Complications of laparoscopic cholecystectomy: a national survey of 4,292 hospitals and an analysis of 77,604 cases. Am J Surg. 1993 Jan;165(1):9–14. doi: 10.1016/s0002-9610(05)80397-6. F. Dubois, P. Icard, G. Berthelot, H. Levard.Coelioscopic cholecystectomy: preliminary report of 36 cases. Ann Surg, 211 (1990), pp. 60–62 B.V. MacFadyen, Vecchio, A.E. Ricardo, C.R. Mathis.Bile duct injury after laparoscopic cholecystectomy: the United States experience. Surg Endosc, 12 (1998), pp. 315–321 Archer SB, Brown DW, Smith CD, Branum GD, Hunter JG. Bile duct injury during laparoscopic cholecystectomy: results of a national survey. Ann Surg. 2001;234:549–558; discussion 558–559. doi: 10.1097/00000658-200110000-00014. Negi SS, Sakhuja P, Malhotra V, Chaudhary A. Factors predicting advanced hepatic fibrosis in patients with postcholecystectomy bile duct strictures. Arch Surg. 2004;139:299–303. doi: 10.1001/archsurg.139.3.299. Pellegrini CA, Thomas MJ, Way LW. Recurrent biliary stricture. Patterns of recurrence and outcome of surgical therapy. Am J Surg. 1984;147:175–180. doi: 10.1016/0002-9610(84)90054-0. Richardson MC, Bell G, Fullarton GM. Incidence and nature of bile duct injuries following laparoscopic cholecystectomy: an audit of 5913 cases. West of Scotland Laparoscopic Cholecystectomy Audit Group. Br J Surg. 1996;83(10):1356–60. doi: 10.1002/bjs.1800831009. Russell JC, Walsh SJ, Mattie AS, Lynch JT. Bile duct injuries, 1989–1993. A statewide experience. Connecticut Laparoscopic Cholecystectomy Registry. Arch Surg. 1996;131(4):382–8. doi: 10.1001/archsurg.1996.01430160040007. Halbert C, Pagkratis S, Yang J, Meng Z, Altieri MS, Parikh P, Pryor A, Talamini M, Telem DA. Beyond the learning curve: incidence of bile duct injuries following laparoscopic cholecystectomy normalize to open in the modern era. Surg Endosc. 2016;30(6):2239–43. doi: 10.1007/s00464-015-4485-2. A.J. Robertson, M. Rela, J. Karani, et al. Laparoscopic cholecystectomy injury: an unusual indication for liver transplantation. Transpl Int, 11 (1998), pp. 449–451 Halbert C, Pagkratis S, Yang J, Meng Z, Altieri MS, Parikh P, Pryor A, Talamini M, Telem DA. Beyond the learning curve: incidence of bile duct injuries following laparoscopic cholecystectomy normalize to open in the modern era. Surg Endosc. 2016;30(6):2239–43. doi: 10.1007/s00464-015-4485-2. Bhattacharjee P. Review Article-Bile duct injuries: Mechanism and prevention. Indian Journal of Surgery (ISSN: 0972–2068) 2005;67(2):67. Way LW, Stewart L, Gantert W, Liu K, Lee CM, Whang K, Hunter JG. Causes and prevention of laparoscopic bile duct injuries: analysis of 252 cases from a human factors and cognitive psychology perspective. Ann Surg. 2003;237(4):460–9. doi: 10.1097/01.SLA.0000060680.92690.E9. De’Angelis N, Catena F, Memeo R, Coccolini F, Martinez-Perez A, Romeo OM, De Simone B, Di Saverio S, Brustia R, Rhaiem R, et al. 2020 WSES guidelines for the detection and management of bile duct injury during cholecystectomy. World J Emerg Surg. 2021;16(1):30. doi: 10.1186/s13017-021-00369-w. Melton GB, Lillemoe KD, Cameron JL, et al: Major bile duct injuries associated with laparoscopic cholecystectomy: Effect of surgical repair on quality of life. Ann Surg 2002;235(6):888–895 ( 12035047; PMCID: 1422520). Thurley PD, Dhingsa R. Laparoscopic cholecystectomy: postoperative imaging. AJR Am J Roentgenol. 2008;191(3):794–801. doi: 10.2214/AJR.07.3485. Connor S, Garden OJ. Bile duct injury in the era of laparoscopic cholecystectomy. Br J Surg. 2006;93(2):158–68. doi: 10.1002/bjs.5266. Pesce A, Palmucci S, La Greca G, Puleo S. Iatrogenic bile duct injury: impact and management challenges. Clin Exp Gastroenterol. 2019;12:121–8. doi: 10.2147/CEG.S169492. Donnellan E, Coulter J, Mathew C, Choynowski M, Flanagan L, Bucholc M, Johnston A, Sugrue M. A meta-analysis of the use of intraoperative cholangiography; time to revisit our approach to cholecystectomy? Surg open Sci. 2021;3:8–15. doi: 10.1016/j.sopen.2020.07.004. Tables Table.1. Intra-operative diagnosis breakdown IOH Number % Recognized 13 21.31% Not recognized 48 78.6% Recognized on the IOCH - Positive predictive value 6/13 46% Additional Declarations No competing interests reported. Cite Share Download PDF Status: Posted Version 1 posted 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. 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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-7797632","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Article","associatedPublications":[],"authors":[{"id":525841433,"identity":"2cd7f750-44ce-48f7-9130-e71330c5dc36","order_by":0,"name":"Prishita 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09:55:31","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":9743,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eNumber of LC performed by surgeons prior to the one leading to BDI\u003c/strong\u003e\u003c/p\u003e","description":"","filename":"2.png","url":"https://assets-eu.researchsquare.com/files/rs-7797632/v1/b6bed05ec2b7f1aa8abbc2fd.png"},{"id":93029364,"identity":"0faad0a0-1b06-42b2-aaac-740ef7bf5ffb","added_by":"auto","created_at":"2025-10-08 09:55:31","extension":"eps","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":64255,"visible":true,"origin":"","legend":"Gender based occurrence of BDI in LC","description":"","filename":"drawingimage1.eps","url":"https://assets-eu.researchsquare.com/files/rs-7797632/v1/003eee1c5642dbac04acd42f.eps"},{"id":93029360,"identity":"9cf507f5-bcab-42e2-bdcc-4e9c1d5b95dd","added_by":"auto","created_at":"2025-10-08 09:55:31","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":19277,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eMost common indications for LC leading to BDI\u003c/strong\u003e\u003c/p\u003e","description":"","filename":"3.png","url":"https://assets-eu.researchsquare.com/files/rs-7797632/v1/0302484cf35ce375e8e4df36.png"},{"id":96372385,"identity":"57e21af8-a0ce-4815-86b0-3f45ce3adfed","added_by":"auto","created_at":"2025-11-20 10:27:22","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":437839,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-7797632/v1/33a2f42c-86ed-4f3f-9848-11c01673faff.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"\u003cp\u003eEtiology of Bile Duct Injuries During Laparoscopic Cholecystectomy\u003c/p\u003e","fulltext":[{"header":"Introduction","content":"\u003cp\u003eLaparoscopic cholecystectomy (LC) is the most commonly performed procedure in the field of digestive surgery as well as general surgery with 1.3\u0026nbsp;million of these procedures performed in the United States in 2021[1]. It is a surgical procedure involving the removal of a diseased gallbladder, indicated for the treatment of medical conditions such as cholecystitis (acute/chronic), symptomatic cholelithiasis, biliary dyskinesia, calculous and acalculous cholecystitis, gallstone pancreatitis, gallbladder masses/polyps and gallbladder cancer. First introduced in 1990 by Dubois et al.[2],Laparoscopic cholecystectomy has largely replaced open cholecystectomy as the standard of care for gallbladder excision.\u003c/p\u003e\u003cp\u003eWith advancements in medical techniques, it rapidly spread as a better and safer alternative to Open cholecystectomy (OC) for its minimally invasive nature as well as robust outcomes. The benefits of LC over open cholecystectomy derive from less operative trauma and ileus with minimum pain, short hospital stay and a reduced period of short-term disability with rapid return to full activity or work. Other benefits include decreased formation of intra-peritoneal adhesions and wound-related complications[3]. LC also replaced other modalities for therapy of symptomatic gallstone disease practised during the 1970s and 80s, such as extracorporeal shock-wave lithotripsy and chemical (bile salt) dissolution therapy. LC thus gained rapid and widespread acceptance among patients and surgeons before its effectiveness and safety were established[4]. Once the global expansion of the procedure was established, the question of possible complications during the procedure came to light over a period of time. One of the most common and severe complication of laparoscopic cholecystectomy (LC) being Bile duct injury (BDI)[5]. The scope of the injury can range from a simple cystic duct leak to the injury of the left and right hepatic duct confluence. The early and accurate diagnosis of BDI is very important for surgeons and gastroenterologists, because unrecognised BDI lead to serious complications such as biliary cirrhosis, hepatic failure and ultimately death[6][7].BDI is in direct correlation with surgical experience and knowledge of cholecystectomy albeit despite the evolution of surgical techniques and approaches, bile duct injury represents a significant complication, even in experienced hands. Past studies in the last three decades stated that the incidence of BDI after laparoscopic cholecystectomy (LC) was significantly greater than that after open cholecystectomy (OC) (0.4\u0026ndash;0.6% and 0.1\u0026ndash;0.2%, respectively). This was corresponding to the emergence of the laparoscopic technique in that era[8][9].However, Later studies found a considerable decline in the incidence of BDIs after LC, to around 0.2%, due to the improved surgical laparoscopic experience[10].Aside from patient morbidity and mortality, Bile duct injuries pose serious health and economic problems as they expose the surgeon to expensive medico-legal litigation. In addition, they increase substantially the economic burden to the patient, hospital and community, and some patients have needed hepatic transplantation for survival[11].\u003c/p\u003e\u003cp\u003eWith the steady increase in cases of gall bladder pathology in recent years, it is inevitable that the number of laparoscopic cholecystectomies being performed are bound to rise in the upcoming years. And an increase in procedures ultimately ties in with an increased risk of complications as well. Thus, it is imperative to understand the etiology as well as any underlying risk factors that may lead to BDI in cases of LC to help prevent such a complication and appropriately adapt the preoperative and postoperative care of patients accordingly. Our current study aimed to assess and analyse the various causes and trends in the incidence and risk factors of bile duct injuries during the period of 25 years.\u003c/p\u003e"},{"header":"Methods","content":"\u003cp\u003eWe performed a retrospective cohort study involving 120 patients over a period of 25 years from 1994 till 2024 to analyse the changing trends over the course of time. Subjects who were included in the database of the study were patients who were treated surgically for bile duct injuries during laparoscopic cholecystectomies. These included patients who were originally treated at the Digestive Surgery Clinic at the University Clinical Center of Nis as well as patients who were referred from 18 regional hospitals and tertiary Hepato-billiary centers.\u003c/p\u003e\u003cp\u003eWe divided the data sets into two groups (Group A and Group B) to analyse the trends over the course of two different decades.\u003c/p\u003e\u003cp\u003eGroup A included 38 patients who developed BDI in the first five year period from 1999 to 2004.\u003c/p\u003e\u003cp\u003eGroup B included 23 patients who developed BDI in the last five year period from 2019 to 2024.\u003c/p\u003e\u003cp\u003eWe collected socio-demographic and clinical data, the most statistically significant parameters included gender, anatomic anomalies, number of laparoscopic cholecystectomies performed by the surgeon, intraoperative cholangiography as a method of diagnosis as well as cause of the operation.\u003c/p\u003e\u003cp\u003e The study was approved by the Ethical Board of the University Clinical Centre Nis. All procedures were performed following the Boards' guidelines and regulations. All participants provided written informed consent. The research results are presented in tabular and graphic form. P values of less than 0.05 were regarded as statistically significant. Numerical data were presented as percentage\u003c/p\u003e"},{"header":"Results","content":"\u003cp\u003eWe found that 38 patients developed bile duct injury during laparoscopic cholecystectomy in the period of first five years from 1999\u0026ndash;2004 (31.6%) and 23 patients developed bile duct injury during laparoscopic cholecystectomy in the period of last five years from 2019\u0026ndash;2024 (19.1%).\u003c/p\u003e\u003cp\u003eIt was found that 88% of the cases of BDI were reported in women while 12% of the cases were reported in men presented in Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e. The number of LC performed i.e experience of the surgeon prior to performing the LC that lead to BDI in both groups is presented in Figure.2. In Group A (1999\u0026ndash;2004) Surgeons reported the most BDI in their first 25 LC procedures and second most during their first 50 and after 200 LC procedures. While in Group B (2019\u0026ndash;2024), Surgeons reported fewer BDI during their first 50 LC. The most BDI were reported after 100 LC procedures in Group B. Indications for the LC leading to most BDI are presented in the Figure.3 We found that BDI was more prevalent in LC done for Acute cholecystitis in both groups accounting for 47.40% (~\u0026thinsp;18 cases out of 38) of BDI in Group A and 56.20% (~\u0026thinsp;13 cases out of 23) of BDI in Group B. While the least number of BDI were seen in LC performed for Simple lithiasis accounting for 18.40% (~\u0026thinsp;7 cases out of 38) of BDI in Group A and 17.40% (~\u0026thinsp;4 cases out of 23) of BDI in Group B. Real anatomical anomalies were found to be an insignificant cause with only 2 cases or 3.27% of BDI reported in both groups combined.\u003c/p\u003e\u003cp\u003e\u003c/p\u003e\u003cp\u003eThe BDI was recognised intraoperative in only 21% (13 out of 61) of cases. Out of which diagnosis based on Intraoperative cholangiography(IOCH) included 6 out of those 13 cases which makes the positive predictive value of IOCH as 46% presented in Table.1.\u003c/p\u003e"},{"header":"Discussion","content":"\u003cp\u003eBiliary duct injury is the most complication of laparoscopic cholecystectomies however, with the increasing knowledge of gallbladder surgeries, the incidence of such complications seems to be significantly decreasing. On account of the increased surgical skills in LC, Halbert et al. concluded that the overall rate of LC has declined to around 0.2% [12].\u003c/p\u003e\u003cp\u003eOur results also suggest that there is a significant declining trend in the the incidence of BDI during LC over the period of last 25 years from 31.6% to 19.1%. The etiology of BDI in the cases that occurred pointed to some key risk factors. The reported frequencies of BDI was unanimously greater in women than in men in both periods of the study making gender of the patient a statistically and clinically significant determinant of BDI development.\u003c/p\u003e\u003cp\u003eSurgical experience played a significant role in determining whether a LC may lead to BDI in Group A but not so much in Group B which poses a question of whether causing a BDI is the product of a surgeons skill and experience or a chance happening which may occur even after a surgeon has been well adept to the procedure. It should be noted that medical techniques and equipment are being steadily updated and improvised so it is a possibility that in the earlier years, the technique of the procedure required rigorous practice and precision to prevent BDI however in current years with greater advancements and multiple approaches of beginner and advanced surgeons, number of LC performed may not be a good determinant. There is also an alternate possibility once a surgeon isn\u0026rsquo;t novice to the procedure, if not careful, a level of complacency could be expected as reported in Group B leading to more BDI among surgeons even after their first 100 or 200 LC procedures. Many studies in the literature agree that the most important factor that decreases the rate of BDI is surgical skill and knowledge in the prevention of BDI. All surgeons must be oriented with a critical view of safety (CVS), respect the Calot\u0026rsquo;s triangle during dissection of the Calot\u0026rsquo;s triangle, and be oriented and prepared with all possible biliary tree and hepatic artery anomalies. Disregarding the CVS, the use of thermal hemostats close to the main biliary system, or strenuous traction on the cystic duct is associated with high rates of BDI [13, 14]\u003c/p\u003e\u003cp\u003eAcute cholecystitis was and still continues to be a major determinant of LC leading to BDI. In both the groups, majority of LC performed due to acute cholecystitis lead to BDI. Anomalies and anatomical variations of biliary ducts or vascular system were seen as rare and played an insignificant role in assessment of BDI etiology.\u003c/p\u003e\u003cp\u003eBDIs are detected in different frames of time. The earlier the timing of detection, the better the outcomes for the patient [15,16].Iatrogenic injuries to the common hepatic duct or right hepatic duct with side branches are normally severe requiring immediate operative management. A well-timed planned operation and extensive surgical repair may help fair better outcomes and ensure long-term quality of life. The reason for performing IOC is to avoid and detect bile duct injuries as well as discovering stones in the common bile duct. Intraoperative detection of BDI is not an easy task; however, if it occurs, surgeons must be aware of what to do next. The use of intraoperative cholangiography (IOC), have been proven to facilitate the detection of challenging biliary anatomy and detect BDI intra-operatively but is not nearly performed as adequately as it should as for patients with suspected BDI, ultrasound remains the most used initial investigation as it diagnoses intra-peritoneal collections and biliary and intra-hepatic dilatation [17]. However, there is no consensus, on the routine usage of these techniques in cholecystectomies [18, 19]. A Meta-analysis undergone on 2,059 articles to evaluate the use of IOC, stated that BDI rates are lower with IOC than without IOC (depending only on the anatomical description) [20]. In our study as well, 46% of BDI diagnosed intra-operatively were recognised via IOC thus showing the benefit of IOC as a diagnostic tool to help prevent and diagnose BDI.\u003c/p\u003e\u003cp\u003eIt should be noted that the study has limitations due to its retrospective nature and the small sample size, which is a result of the limited number of cases referred to a single unit, and the decreased incidence of the condition. Furthermore, most of the cases reported were referred from another hospital with no surgical report, which limited the intraoperative data, especially the mechanism of injury.\u003c/p\u003e"},{"header":"Conclusion","content":"\u003cp\u003eLaparoscopic cholecystectomy is a widely performed procedure and though the complications related to the procedure has significantly reduced in recent times, there is still scope for improvement in understanding and preventing bile duct injuries during the surgery. This study serves to bring to light the most common causes and underlying risk factors that may lead to bile duct injuries during laparoscopic cholecystectomy. It is essential to carefully assess the patient profile and demographic prior to the surgery to estimate outcomes. Surgeons must be aware of primary diagnostic and preventative techniques and regularly improve their knowledge regarding laparoscopic surgeries, both to prevent BDI and avoid the accumulation of the risk of patient morbidity and mortality. In conclusion, in accordance with the parameters assessed in this study, proper training and experience of surgeons, identifying acute cholecystitis as a high-risk factor and routine use of intraoperative cholangiography are the best methods currently available for timely identifying and hopefully preventing Bile duct injuries during laparoscopic cholecystectomy.\u003c/p\u003e"},{"header":"Declarations","content":"\u003ch2\u003eAuthor Contribution\u003c/h2\u003e\u003cp\u003eP.B and Y.G wrote the main manuscript text and P.B prepared figures and table. All authors reviewed the manuscript.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eTsui C., Klein R., Garabrant M. Minimally invasive surgery: national trends in adoption and future directions for hospital strategy. Surg Endosc. 2013;27:2253\u0026ndash;2257. doi: 10.1007/s00464-013-2973-9.\u003c/span\u003e\u003c/li\u003e\u003cli\u003e\u003cspan\u003eDeziel D. J., Millikan K. W., Economou S. G., Doolas A., Ko S. T., Airan M. C. Complications of laparoscopic cholecystectomy: a national survey of 4,292 hospitals and an analysis of 77,604 cases. Am J Surg. 1993 Jan;165(1):9\u0026ndash;14. doi: 10.1016/s0002-9610(05)80397-6.\u003c/span\u003e\u003c/li\u003e\u003cli\u003e\u003cspan\u003eF. Dubois, P. Icard, G. Berthelot, H. Levard.Coelioscopic cholecystectomy: preliminary report of 36 cases. Ann Surg, 211 (1990), pp. 60\u0026ndash;62\u003c/span\u003e\u003c/li\u003e\u003cli\u003e\u003cspan\u003eB.V. MacFadyen, Vecchio, A.E. Ricardo, C.R. Mathis.Bile duct injury after laparoscopic cholecystectomy: the United States experience. Surg Endosc, 12 (1998), pp. 315\u0026ndash;321\u003c/span\u003e\u003c/li\u003e\u003cli\u003e\u003cspan\u003eArcher SB, Brown DW, Smith CD, Branum GD, Hunter JG. Bile duct injury during laparoscopic cholecystectomy: results of a national survey. Ann Surg. 2001;234:549\u0026ndash;558; discussion 558\u0026ndash;559. doi: 10.1097/00000658-200110000-00014.\u003c/span\u003e\u003c/li\u003e\u003cli\u003e\u003cspan\u003eNegi SS, Sakhuja P, Malhotra V, Chaudhary A. Factors predicting advanced hepatic fibrosis in patients with postcholecystectomy bile duct strictures. Arch Surg. 2004;139:299\u0026ndash;303. doi: 10.1001/archsurg.139.3.299.\u003c/span\u003e\u003c/li\u003e\u003cli\u003e\u003cspan\u003ePellegrini CA, Thomas MJ, Way LW. Recurrent biliary stricture. Patterns of recurrence and outcome of surgical therapy. Am J Surg. 1984;147:175\u0026ndash;180. doi: 10.1016/0002-9610(84)90054-0.\u003c/span\u003e\u003c/li\u003e\u003cli\u003e\u003cspan\u003eRichardson MC, Bell G, Fullarton GM. Incidence and nature of bile duct injuries following laparoscopic cholecystectomy: an audit of 5913 cases. West of Scotland Laparoscopic Cholecystectomy Audit Group. Br J Surg. 1996;83(10):1356\u0026ndash;60. doi: 10.1002/bjs.1800831009.\u003c/span\u003e\u003c/li\u003e\u003cli\u003e\u003cspan\u003eRussell JC, Walsh SJ, Mattie AS, Lynch JT. Bile duct injuries, 1989\u0026ndash;1993. A statewide experience. Connecticut Laparoscopic Cholecystectomy Registry. Arch Surg. 1996;131(4):382\u0026ndash;8. doi: 10.1001/archsurg.1996.01430160040007.\u003c/span\u003e\u003c/li\u003e\u003cli\u003e\u003cspan\u003eHalbert C, Pagkratis S, Yang J, Meng Z, Altieri MS, Parikh P, Pryor A, Talamini M, Telem DA. Beyond the learning curve: incidence of bile duct injuries following laparoscopic cholecystectomy normalize to open in the modern era. Surg Endosc. 2016;30(6):2239\u0026ndash;43. doi: 10.1007/s00464-015-4485-2.\u003c/span\u003e\u003c/li\u003e\u003cli\u003e\u003cspan\u003eA.J. Robertson, M. Rela, J. Karani, et al. Laparoscopic cholecystectomy injury: an unusual indication for liver transplantation. Transpl Int, 11 (1998), pp. 449\u0026ndash;451\u003c/span\u003e\u003c/li\u003e\u003cli\u003e\u003cspan\u003eHalbert C, Pagkratis S, Yang J, Meng Z, Altieri MS, Parikh P, Pryor A, Talamini M, Telem DA. Beyond the learning curve: incidence of bile duct injuries following laparoscopic cholecystectomy normalize to open in the modern era. Surg Endosc. 2016;30(6):2239\u0026ndash;43. doi: 10.1007/s00464-015-4485-2.\u003c/span\u003e\u003c/li\u003e\u003cli\u003e\u003cspan\u003eBhattacharjee P. Review Article-Bile duct injuries: Mechanism and prevention. Indian Journal of Surgery (ISSN: 0972\u0026ndash;2068) 2005;67(2):67.\u003c/span\u003e\u003c/li\u003e\u003cli\u003e\u003cspan\u003eWay LW, Stewart L, Gantert W, Liu K, Lee CM, Whang K, Hunter JG. Causes and prevention of laparoscopic bile duct injuries: analysis of 252 cases from a human factors and cognitive psychology perspective. Ann Surg. 2003;237(4):460\u0026ndash;9. doi: 10.1097/01.SLA.0000060680.92690.E9.\u003c/span\u003e\u003c/li\u003e\u003cli\u003e\u003cspan\u003eDe\u0026rsquo;Angelis N, Catena F, Memeo R, Coccolini F, Martinez-Perez A, Romeo OM, De Simone B, Di Saverio S, Brustia R, Rhaiem R, et al. 2020 WSES guidelines for the detection and management of bile duct injury during cholecystectomy. World J Emerg Surg. 2021;16(1):30. doi: 10.1186/s13017-021-00369-w.\u003c/span\u003e\u003c/li\u003e\u003cli\u003e\u003cspan\u003eMelton GB, Lillemoe KD, Cameron JL, et al: Major bile duct injuries associated with laparoscopic cholecystectomy: Effect of surgical repair on quality of life. Ann Surg 2002;235(6):888\u0026ndash;895 ( 12035047; PMCID: 1422520).\u003c/span\u003e\u003c/li\u003e\u003cli\u003e\u003cspan\u003eThurley PD, Dhingsa R. Laparoscopic cholecystectomy: postoperative imaging. AJR Am J Roentgenol. 2008;191(3):794\u0026ndash;801. doi: 10.2214/AJR.07.3485.\u003c/span\u003e\u003c/li\u003e\u003cli\u003e\u003cspan\u003eConnor S, Garden OJ. Bile duct injury in the era of laparoscopic cholecystectomy. Br J Surg. 2006;93(2):158\u0026ndash;68. doi: 10.1002/bjs.5266.\u003c/span\u003e\u003c/li\u003e\u003cli\u003e\u003cspan\u003ePesce A, Palmucci S, La Greca G, Puleo S. Iatrogenic bile duct injury: impact and management challenges. Clin Exp Gastroenterol. 2019;12:121\u0026ndash;8. doi: 10.2147/CEG.S169492.\u003c/span\u003e\u003c/li\u003e\u003cli\u003e\u003cspan\u003eDonnellan E, Coulter J, Mathew C, Choynowski M, Flanagan L, Bucholc M, Johnston A, Sugrue M. A meta-analysis of the use of intraoperative cholangiography; time to revisit our approach to cholecystectomy? Surg open Sci. 2021;3:8\u0026ndash;15. doi: 10.1016/j.sopen.2020.07.004.\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"},{"header":"Tables","content":"\u003cp\u003e\u003cstrong\u003eTable.1. Intra-operative diagnosis breakdown\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e\n\u003ctable border=\"1\" cellspacing=\"0\" cellpadding=\"0\" width=\"610\" class=\"fr-table-selection-hover\"\u003e\n \u003ctbody\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 47.541%;\"\u003e\n \u003cp\u003e\u003cstrong\u003eIOH\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 27.0492%;\"\u003e\n \u003cp\u003e\u003cstrong\u003eNumber \u0026nbsp;\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 25.4098%;\"\u003e\n \u003cp\u003e\u003cstrong\u003e%\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 47.541%;\"\u003e\n \u003cp\u003e\u003cstrong\u003eRecognized\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 27.0492%;\"\u003e\n \u003cp\u003e13\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 25.4098%;\"\u003e\n \u003cp\u003e21.31%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 47.541%;\"\u003e\n \u003cp\u003e\u003cstrong\u003eNot recognized\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 27.0492%;\"\u003e\n \u003cp\u003e48\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 25.4098%;\"\u003e\n \u003cp\u003e78.6%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" style=\"width: 47.541%;\"\u003e\n \u003cp\u003e\u003cstrong\u003eRecognized on the IOCH\u003c/strong\u003e\u003cstrong\u003e-\u003c/strong\u003e\u003c/p\u003e\n \u003cp\u003e\u003cstrong\u003ePositive predictive value\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 27.0492%;\"\u003e\n \u003cp\u003e6/13\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\" style=\"width: 25.4098%;\"\u003e\n \u003cp\u003e46%\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":false,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":true,"hideJournal":true,"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":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"bile duct injury, laparoscopic cholecystectomy, prevention, management","lastPublishedDoi":"10.21203/rs.3.rs-7797632/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-7797632/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003e\u003cstrong\u003eIntroduction\u003c/strong\u003e: Laparoscopic cholecystectomy (LC) is a surgical procedure indicated for the treatment of medical conditions involving the removal of a diseased gallbladder. One of the most common and severe complication of laparoscopic cholecystectomy (LC) is bile duct injury (BDI). In such a widely performed procedure it is imperative to understand the etiology as well as any underlying risk factors that may lead to BDI.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eThe Aim\u003c/strong\u003e: To assess and analyse the various causes and trends in the incidence and risk factors of bile duct injuries during a period of 25 years .\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eMaterials and Methods\u003c/strong\u003e: We performed a retrospective cohort study involving 120 patients who underwent LC over a period of 25 years from 1994 till 2024, divided into 2 groups to analyse the changing trends over the course of time. Socio-demographic and clinical data was collected, the most statistically significant parameters included gender, anatomic anomalies, number of laparoscopic cholecystectomies performed by the surgeon, intraoperative cholangiography as a method of diagnosis as well as cause of the operation.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eResults\u003c/strong\u003e: We found that 38 patients developed bile duct injury in the period of first five years from 1999–2004 (31.6%) while 23 patients developed bile duct injury in the period of last five years from 2019–2024 (19.1%). Acute cholecystitis was found to be leading risk factor in (47.40%) cases in first group and 56.20% cases in the second group. 88% patients developing BDI were female. Experience of surgeon reporting bile duct injury varied from less than 25 procedures performed (1999–2004) to more than 100 procedures performed (2019–2024).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConclusion\u003c/strong\u003e: Our study indicates that proper training and experience of surgeons is a key determinant in development of BDI. Acute cholecystitis was recognised as a high risk factor that leads to complications during LC. The routine use of intra-operative cholangiography are the best methods currently available for timely identifying and hopefully preventing bile duct injuries during laparoscopic cholecystectomy.\u003c/p\u003e","manuscriptTitle":"Etiology of Bile Duct Injuries During Laparoscopic Cholecystectomy","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2025-10-08 09:55:26","doi":"10.21203/rs.3.rs-7797632/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"c23a7968-305f-428f-bb1f-7186704a0e87","owner":[],"postedDate":"October 8th, 2025","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[{"id":55938502,"name":"Health sciences/Diseases"},{"id":55938503,"name":"Health sciences/Gastroenterology"},{"id":55938504,"name":"Health sciences/Medical research"},{"id":55938505,"name":"Health sciences/Risk factors"}],"tags":[],"updatedAt":"2025-11-20T10:24:37+00:00","versionOfRecord":[],"versionCreatedAt":"2025-10-08 09:55:26","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-7797632","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-7797632","identity":"rs-7797632","version":["v1"]},"buildId":"8U1c8b4HqxoKbykW_rLl7","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}