The Use of Endoscopic Ultrasound Guided Fine Needle Biopsy for the Diagnosis of Microcystic Serous Cystic Neoplasms of the Pancreas

The Use of Endoscopic Ultrasound Guided Fine Needle Biopsy for the Diagnosis of Microcystic Serous Cystic Neoplasms of the Pancreas | 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 The Use of Endoscopic Ultrasound Guided Fine Needle Biopsy for the Diagnosis of Microcystic Serous Cystic Neoplasms of the Pancreas Kanika Garg, Kesany Boupapanh, Netanel Zilberstein, Thomas Wang, and 6 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-5435718/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 Background: Pancreatic cysts, frequently identified incidentally on imaging, present diagnostic challenges due to their variable malignant potential. Serous cystic neoplasms (SCNs) are benign and account for 1-2% of pancreatic lesions. However, imaging techniques alone often lack the accuracy to definitively diagnose these lesions, leading to unnecessary surveillance and interventions. Aims: This study evaluates the safety and diagnostic efficacy of endoscopic ultrasound-guided fine-needle biopsy (EUS-FNB) for identifying microcystic SCNs. Methods: We conducted a retrospective analysis of 39 patients who underwent EUS-FNB for solitary pancreatic lesions with microcystic features, identified through cross-sectional imaging at our medical center between 2018 and 2024. Patients with a stellate scar or definitive imaging features of microcystic SCNs were excluded. Outcomes assessed included histologic results and complications. Results: Histological confirmation of microcystic SCN was achieved in 79.5% of cases, eliminating the need for further imaging and surveillance. A single complication—mild intra-lesional bleeding—occurred in one patient, which resolved without further intervention. Conclusions: EUS-FNB is a safe and effective method for diagnosing microcystic SCNs, offering a definitive diagnosis and reducing unnecessary surveillance and interventions. This approach provides a favorable risk-benefit profile for managing SCNs. However, future multicenter studies with larger cohorts are needed to further validate these findings and refine diagnostic protocols for pancreatic cystic neoplasms. Figures Figure 1 Figure 2 Introduction Pancreatic cysts are increasingly found incidentally in patients undergoing cross-sectional imaging for unrelated reasons with an incidence as high as 25–49% in some studies. 1 , 2 While some pancreatic cysts have the potential for malignant transformation, the overall risk of malignancy across all pancreatic cysts remains low, at just 0.24%. 2 Pancreatic cysts can be broadly categorized as neoplastic and non-neoplastic based on their mucin-producing abilities. Given their varying malignant potential, surveillance of cysts is recommended based on certain criteria. Mucin producing cysts, including intraductal papillary mucinous neoplasms (IPMNs) and mucinous cystic neoplasms (MCNs), have a higher malignant potential, and thus generally warrant surveillance. 3 Serous cystic neoplasms, however, have minimal malignant potential at less than 1% and routine surveillance is not usually recommended. 3 – 5 Some studies have shown that the cost of surveillance over 10 years can be up to $ 1,924,607, highlighting the need for accurate and effective surveillance guidelines. 6 Pancreatic serous cystic neoplasms (SCNs) are rare, benign lesions accounting for approximately 1–2% of all pancreatic tumors. 7 These neoplasms exhibit distinct histological characteristics, including glycogen-rich cuboidal or columnar epithelial cells lining numerous small cysts, often accompanied by fibrous tissue in the stroma. 8 , 9 SCNs can present in various morphological patterns, among which, the microcystic variant is the most prevalent. Microcystic SCNs frequently present with features that resemble solid lesions on cross-sectional imaging, often complicating the diagnostic process. 10 , 11 Despite significant advancements in diagnostic imaging techniques, cross-sectional imaging alone yields a definitive diagnosis in only about 50% of SCN cases, underscoring the inherent challenges in accurately identifying these lesions. 12 , 13 EUS imaging can also be helpful, but studies have shown only a 60–70% accuracy in diagnosing these lesions. 3 In the absence of characteristic imaging features, clinicians often turn to endoscopic ultrasound-guided fine-needle aspiration (EUS-FNA) as the next diagnostic modality, particularly for larger microcystic lesions. 14 However, the effectiveness of FNA can be limited by inconclusive cytology results and insufficient fluid samples for comprehensive analyses. 15 , 16 Another inherent challenge when dealing with these lesions is the inability to aspirate fluid for studies due to their microcystic nature. Other diagnostic tools, such as needle-based confocal laser endomicroscopy, are costly and lack definite diagnostic criteria. Given all of these compounding limiting factors, a large number of SCNs are not conclusively diagnosed, which leads to continued surveillance, adding to costs, risks, and patient anxiety as well. While previous studies have suggested the potential efficacy of fine needle biopsies (FNB) in diagnosing SCNs, these investigations have been constrained by small patient cohorts, limiting their generalizability. 17 , 18 To address this gap in knowledge, we present our single-center experience using FNB for the histological diagnosis of suspected microcystic SCNs. Methods This was a single-center retrospective review of electronic health records of all patients who underwent EUS and subsequent FNB for the investigation of solitary pancreatic lesions initially detected via cross-sectional imaging from 2018 to 2024. The study protocol was approved by the Institutional Review Board of the Rush University Medical Center. The inclusion criteria encompassed patients 18 years and older who had cross-sectional imaging which showed a pancreatic mass or cystic lesion for which they were referred for further evaluation with EUS. Patients with a stellate scar or imaging features diagnostic of microcystic SCNs were excluded. The patients for which EUS showed multi-septate cystic lesions but with cystic components small enough for the endosonographer to believe that fluid aspiration would be non-diagnostic, or with mixed cystic and microcystic areas, were further included in the study. All patients underwent FNB using a 22-gauge fork-tip biopsy needle (SharkCore, Medtronic, Minneapolis, MN, USA), employing either a transgastric or transduodenal approach, depending on the location of the lesion in the pancreas. The acquired tissue was placed in formalin, subjected to standard histologic handling, and was reviewed by an expert gastrointestinal pathologist to ensure accurate diagnosis and characterization of the lesions. All patients received intravenous antibiotics during the procedure followed by oral antibiotics for a total of 3 days. Any intraprocedural complications (bleeding, perforation) or post-procedural complications (pancreatitis, delayed bleeding, or infection) were reported. Results A total of 39 patients were included in the study. The mean age of the cohort was 67.5 ± 12.5 years with 74% female participants (29 out of 39). The average cyst size, measured in its largest diameter, was 32.6 ± 14.2 mm (range: 8–74 mm). The lesions were distributed across various regions of the pancreas, with 13 in the body, 13 in the head/uncinate, 9 in the tail, and 4 in the genu. (Table 1 ). Table 1 Baseline Characteristics Mean (± SD) or N (%) Age (years) 67.5 ± 12.5 Gender (M/F) 10 (26%) / 29 (74%) Cyst Size (mm) 32.6 (± 14.2) Cyst Location Body 13 (33.3%) Head/Uncinate 13 (33.3%) Tail 9 (23.1%) Genu 4 (10.3%) Histology: A histological diagnosis of microcystic SCN was established in 79.5% (31/39) of the lesions, and no further surveillance or imaging was recommended for these patients. (Fig. 1, Fig. 2 ). Among the remaining lesions, 5 were identified as benign pancreatic parenchyma, 1 as renal clear cell carcinoma and 2 samples were non-diagnostic. One of the patients with benign pancreatic parenchyma on FNB histology underwent surgical resection due to symptoms of sinistral portal hypertension secondary to mass effect from her cyst and having high-risk features on imaging, and was confirmed to have a microcystic SCN on pathology. The median number of passes obtained during the FNB procedure was 2 ± 1.0 (range: 1–5). (Table 2 ). Table 2 Histology Median (± IQR) or N (%) Number of passes 2 (± 1) Histologic Diagnosis Serous Cyst Adenoma 31 (79.5%) Benign Pancreatic parenchyma 5 (12.8%) Renal Clear Cell Carcinoma 1 (2.6%) Non-Diagnostic 2 (5.1%) Complications: One patient experienced intra-lesional bleeding after the initial needle puncture, resulting in only one pass being obtained. Although there was no evidence of bleeding at the end of the procedure, the patient reported abdominal pain and was admitted for observation. A computed tomography (CT) scan of the abdomen and pelvis was unremarkable, and the pain resolved spontaneously without requiring further intervention. No other adverse events, such as infection, perforation, or pancreatitis, were noted in the study cohort. Discussion The increasing use of abdominal imaging has led to a higher incidental detection of cystic neoplasms of the pancreas on cross-sectional imaging and abdominal ultrasound. 19 Among these cystic neoplasms, microcystic SCNs represent a common variant, accounting for approximately one-third of all pancreatic cystic neoplasms (PCNs). 20 Unlike mucinous cysts, these lesions are typically benign, with less than 1% transforming into serous cystadenocarcinomas. 21 This case series corroborates the predominance of microcystic SCNs in women and the later age of diagnosis, typically occurring in the 5th to 7th decade of life. 22 Most patients with SCNs are asymptomatic, but when symptoms do occur, they often include abdominal pain, the presence of an abdominal mass, or early satiety. 23 , 24 CT is the most widely used radiographic test for evaluating microcystic SCNs, on which, these lesions exhibit a characteristic "honeycomb" appearance with a central fibronodular scar. 25 The central fibrous scar, also referred to as a "stellate central scar," is enhanced with iodinated contrast on CT, serving as an important distinguishing feature of SCNs, as they are considered the only hypervascular PCNs. 26 , 27 When further imaging is necessary, endoscopic ultrasound is often employed to obtain high-resolution images of the lesions, as it is considered the ideal imaging modality. Additionally, EUS can be combined with FNA and/or FNB for further evaluation of the lesion. 28 While FNA and FNB can assist in acquiring a definitive diagnosis for the type of PCN, it is crucial to acknowledge the potential pitfalls of these interventions, including sampling error, inadequate cystic contents, and inherent risks of complications such as acute pancreatitis, abdominal pain, bleeding, and infection. 29 – 31 FNA, which is more commonly performed than FNB, allows clinicians to perform cyst fluid analysis. Fluid analysis is highly accurate in differentiating mucinous from non-mucinous lesions but is usually not diagnostic for SCNs. Additionally, in patients with microcystic SCNs, the cytology sample obtained is often inadequate for diagnosis. 32 In contrast, FNB enables a more accurate diagnosis by providing a core biopsy of the cyst wall and the internal septations, allowing pathologists to evaluate the cyst wall histology for subtyping and grading of dysplasia. This approach can lead to a reduction in surveillance imaging and prevent unnecessary invasive interventions for further workup. 33 , 34 The safety and feasibility of EUS-guided FNB for diagnosing microcystic SCNs have been a topic of debate, with some studies suggesting an elevated risk of intraprocedural bleeding. 35 However, our case series challenges this notion, demonstrating a low incidence of adverse events and no significant bleeding complications. The ability to obtain a definitive diagnosis through FNB can have substantial implications for patient management, as it eliminates the need for follow-up imaging and surveillance once the diagnosis is confirmed. Moreover, this approach can help prevent unnecessary surgical interventions in cases of larger lesions where EUS-guided FNA fails to yield a diagnosis. 36 , 37 Despite avoiding unnecessary surgery in majority of the patients, one of the patients in the study with a non-diagnostic FNB underwent surgical resection due to high-risk imaging features (duct dilatation, interval increase in size, and abdominal discomfort). The final pathology for this patient who underwent surgical resection was SCN. Despite the promising findings of our study, it is important to acknowledge its limitations. The retrospective nature of the study and the relatively small sample size may limit the generalizability of the results. Additionally, the single-center design may introduce potential biases related to institutional practices and expertise. Future prospective, multicenter studies with larger patient cohorts are needed to further validate the safety and efficacy of EUS-guided FNB for the diagnosis of microcystic SCNs. Conclusion Our case series highlights the safety and feasibility of EUS-guided FNB for diagnosing microcystic SCNs, challenging previous literature suggesting elevated intraprocedural bleeding risks. This diagnostic approach offers the potential for cost-effectiveness by eliminating the need for follow-up imaging and surveillance once a definitive diagnosis is established. Furthermore, it can help prevent unnecessary surgical interventions in cases where EUS-guided FNA fails to provide a diagnosis. As the incidental detection of pancreatic cystic neoplasms continues to rise with the increasing use of abdominal imaging, the role of EUS-guided FNB in the diagnostic algorithm for microcystic SCNs warrants further consideration to optimize patient management and outcomes. Declarations Author Contribution K.G., K.B., and A.S. wrote the main manuscript text. K.G., T.W., G.K, N.Z, and A.S. collected and analyzed the data. K.G, R.A., and A.S. prepared the figures. N.M, C.C, I.W., and A.S, performed the procedures. All authors reviewed the manuscript. Data Availability Raw data for our dataset is not publicly available to preserve individuals’ privacy. References Kromrey ML, Bülow R, Hübner J, et al. Prospective study on the incidence, prevalence and 5-year pancreatic-related mortality of pancreatic cysts in a population-based study. Gut. Jan 2018;67(1):138–145. doi: 10.1136/gutjnl-2016-313127 Vege SS, Ziring B, Jain R, Moayyedi P, Committee CG, Association AG. American gastroenterological association institute guideline on the diagnosis and management of asymptomatic neoplastic pancreatic cysts. Gastroenterology . Apr 2015;148(4):819 – 22; quize12-3. doi: 10.1053/j.gastro.2015.01.015 Elta GH, Enestvedt BK, Sauer BG, Lennon AM. 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Pancreatology. 2010;10(2–3):144–50. doi: 10.1159/000243733 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. 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-5435718","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":379141275,"identity":"1a8d9f5c-d352-4095-84c4-109740476649","order_by":0,"name":"Kanika Garg","email":"","orcid":"","institution":"Rush University Medical Center","correspondingAuthor":false,"prefix":"","firstName":"Kanika","middleName":"","lastName":"Garg","suffix":""},{"id":379141276,"identity":"c19c0d11-b0d2-435a-a261-94d1272ebfec","order_by":1,"name":"Kesany Boupapanh","email":"","orcid":"","institution":"Rush University Medical 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Singh","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAABD0lEQVRIiWNgGAWjYFCCAyDCgoGBGYQqgGwJIOYhrEUCquUMUVoYoFqAgJmxjQgt/I2Hn0kX1EgwyLfzHn5dOO9e4vzZDYwP3rbhMf7AMTPpGcckGAwO86VZz9xWnLjhzgFmw7l4tDAcOGAmzcMG1MLMY2bMuy0hcYNEAps0Lx4t8geOf5Pm+Qd0WDNIy5yExPkzEth/49NicOCMGdBMoJcP8xg/5m1ISGy4kcDGjE+L4YEzxdYz+0B+4TFj5jmWYLzhRmKz5JxzuLXI3Ti+8XbBNxsG+f4zxp95ahJk589IPvjhTRke70scYJEGUvUNDAxskNhhYGzAox4I+BuYP0OZzB/wKx0Fo2AUjIKRCgC6T09ZJmzlkwAAAABJRU5ErkJggg==","orcid":"","institution":"Rush University Medical Center","correspondingAuthor":true,"prefix":"","firstName":"Ajaypal","middleName":"","lastName":"Singh","suffix":""}],"badges":[],"createdAt":"2024-11-12 03:23:09","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-5435718/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-5435718/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":71564875,"identity":"ff064401-b506-4469-819d-fceb25bfd9d0","added_by":"auto","created_at":"2024-12-16 17:29:24","extension":"jpeg","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":73498,"visible":true,"origin":"","legend":"\u003cp\u003eSee image above for figure legend\u003c/p\u003e","description":"","filename":"Figure1.jpeg","url":"https://assets-eu.researchsquare.com/files/rs-5435718/v1/35ddce60085f91b1568fffd5.jpeg"},{"id":71564874,"identity":"710187c4-36ff-4469-85ba-88ad619c0b59","added_by":"auto","created_at":"2024-12-16 17:29:24","extension":"jpeg","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":61372,"visible":true,"origin":"","legend":"\u003cp\u003eSee image above for figure legend\u003c/p\u003e","description":"","filename":"Figure2.jpeg","url":"https://assets-eu.researchsquare.com/files/rs-5435718/v1/b579be68987bc33ffeed35de.jpeg"},{"id":72229313,"identity":"b5f8a823-bdac-4428-8f46-df82b3d9c65f","added_by":"auto","created_at":"2024-12-24 03:01:38","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":466032,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-5435718/v1/3327bccc-0d85-4732-9c39-384ef9e12ce9.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"The Use of Endoscopic Ultrasound Guided Fine Needle Biopsy for the Diagnosis of Microcystic Serous Cystic Neoplasms of the Pancreas","fulltext":[{"header":"Introduction","content":" \u003cp\u003ePancreatic cysts are increasingly found incidentally in patients undergoing cross-sectional imaging for unrelated reasons with an incidence as high as 25\u0026ndash;49% in some studies.\u003csup\u003e \u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e,\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e \u003c/sup\u003e While some pancreatic cysts have the potential for malignant transformation, the overall risk of malignancy across all pancreatic cysts remains low, at just 0.24%.\u003csup\u003e2\u003c/sup\u003e Pancreatic cysts can be broadly categorized as neoplastic and non-neoplastic based on their mucin-producing abilities. Given their varying malignant potential, surveillance of cysts is recommended based on certain criteria. Mucin producing cysts, including intraductal papillary mucinous neoplasms (IPMNs) and mucinous cystic neoplasms (MCNs), have a higher malignant potential, and thus generally warrant surveillance.\u003csup\u003e \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e \u003c/sup\u003e Serous cystic neoplasms, however, have minimal malignant potential at less than 1% and routine surveillance is not usually recommended. \u003csup\u003e \u003cspan additionalcitationids=\"CR4\" citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e \u003c/sup\u003e Some studies have shown that the cost of surveillance over 10 years can be up to \u003cspan\u003e$\u003c/span\u003e1,924,607, highlighting the need for accurate and effective surveillance guidelines.\u003csup\u003e \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e \u003c/sup\u003e \u003c/p\u003e \u003cp\u003ePancreatic serous cystic neoplasms (SCNs) are rare, benign lesions accounting for approximately 1\u0026ndash;2% of all pancreatic tumors.\u003csup\u003e\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e\u003c/sup\u003e These neoplasms exhibit distinct histological characteristics, including glycogen-rich cuboidal or columnar epithelial cells lining numerous small cysts, often accompanied by fibrous tissue in the stroma.\u003csup\u003e\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e,\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e\u003c/sup\u003e SCNs can present in various morphological patterns, among which, the microcystic variant is the most prevalent. Microcystic SCNs frequently present with features that resemble solid lesions on cross-sectional imaging, often complicating the diagnostic process.\u003csup\u003e\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e,\u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e\u003c/sup\u003e Despite significant advancements in diagnostic imaging techniques, cross-sectional imaging alone yields a definitive diagnosis in only about 50% of SCN cases, underscoring the inherent challenges in accurately identifying these lesions.\u003csup\u003e\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e,\u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e\u003c/sup\u003e EUS imaging can also be helpful, but studies have shown only a 60\u0026ndash;70% accuracy in diagnosing these lesions.\u003csup\u003e\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e\u003c/sup\u003e\u003c/p\u003e \u003cp\u003eIn the absence of characteristic imaging features, clinicians often turn to endoscopic ultrasound-guided fine-needle aspiration (EUS-FNA) as the next diagnostic modality, particularly for larger microcystic lesions.\u003csup\u003e\u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e\u003c/sup\u003e However, the effectiveness of FNA can be limited by inconclusive cytology results and insufficient fluid samples for comprehensive analyses.\u003csup\u003e\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e,\u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e16\u003c/span\u003e\u003c/sup\u003e Another inherent challenge when dealing with these lesions is the inability to aspirate fluid for studies due to their microcystic nature. Other diagnostic tools, such as needle-based confocal laser endomicroscopy, are costly and lack definite diagnostic criteria. Given all of these compounding limiting factors, a large number of SCNs are not conclusively diagnosed, which leads to continued surveillance, adding to costs, risks, and patient anxiety as well.\u003c/p\u003e \u003cp\u003eWhile previous studies have suggested the potential efficacy of fine needle biopsies (FNB) in diagnosing SCNs, these investigations have been constrained by small patient cohorts, limiting their generalizability. \u003csup\u003e\u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e,\u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e18\u003c/span\u003e\u003c/sup\u003e To address this gap in knowledge, we present our single-center experience using FNB for the histological diagnosis of suspected microcystic SCNs.\u003c/p\u003e"},{"header":"Methods","content":"\u003cp\u003eThis was a single-center retrospective review of electronic health records of all patients who underwent EUS and subsequent FNB for the investigation of solitary pancreatic lesions initially detected via cross-sectional imaging from 2018 to 2024. The study protocol was approved by the Institutional Review Board of the Rush University Medical Center.\u003c/p\u003e \u003cp\u003eThe inclusion criteria encompassed patients 18 years and older who had cross-sectional imaging which showed a pancreatic mass or cystic lesion for which they were referred for further evaluation with EUS. Patients with a stellate scar or imaging features diagnostic of microcystic SCNs were excluded. The patients for which EUS showed multi-septate cystic lesions but with cystic components small enough for the endosonographer to believe that fluid aspiration would be non-diagnostic, or with mixed cystic and microcystic areas, were further included in the study.\u003c/p\u003e \u003cp\u003eAll patients underwent FNB using a 22-gauge fork-tip biopsy needle (SharkCore, Medtronic, Minneapolis, MN, USA), employing either a transgastric or transduodenal approach, depending on the location of the lesion in the pancreas. The acquired tissue was placed in formalin, subjected to standard histologic handling, and was reviewed by an expert gastrointestinal pathologist to ensure accurate diagnosis and characterization of the lesions. All patients received intravenous antibiotics during the procedure followed by oral antibiotics for a total of 3 days. Any intraprocedural complications (bleeding, perforation) or post-procedural complications (pancreatitis, delayed bleeding, or infection) were reported.\u003c/p\u003e"},{"header":"Results","content":"\u003cp\u003eA total of 39 patients were included in the study. The mean age of the cohort was 67.5\u0026thinsp;\u0026plusmn;\u0026thinsp;12.5 years with 74% female participants (29 out of 39). The average cyst size, measured in its largest diameter, was 32.6\u0026thinsp;\u0026plusmn;\u0026thinsp;14.2 mm (range: 8\u0026ndash;74 mm). The lesions were distributed across various regions of the pancreas, with 13 in the body, 13 in the head/uncinate, 9 in the tail, and 4 in the genu. (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e\u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"2\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eBaseline Characteristics\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eMean (\u0026plusmn;\u0026thinsp;SD) or N (%)\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAge (years)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e67.5\u0026thinsp;\u0026plusmn;\u0026thinsp;12.5\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eGender (M/F)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e10 (26%) / 29 (74%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eCyst Size (mm)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e32.6 (\u0026plusmn;\u0026thinsp;14.2)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c2\" namest=\"c1\"\u003e \u003cp\u003eCyst Location\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eBody\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e13 (33.3%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eHead/Uncinate\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e13 (33.3%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eTail\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e9 (23.1%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eGenu\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e4 (10.3%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eHistology: A histological diagnosis of microcystic SCN was established in 79.5% (31/39) of the lesions, and no further surveillance or imaging was recommended for these patients. (Fig.\u0026nbsp;1, \u003cb\u003eFig.\u0026nbsp;2\u003c/b\u003e). Among the remaining lesions, 5 were identified as benign pancreatic parenchyma, 1 as renal clear cell carcinoma and 2 samples were non-diagnostic. One of the patients with benign pancreatic parenchyma on FNB histology underwent surgical resection due to symptoms of sinistral portal hypertension secondary to mass effect from her cyst and having high-risk features on imaging, and was confirmed to have a microcystic SCN on pathology. The median number of passes obtained during the FNB procedure was 2\u0026thinsp;\u0026plusmn;\u0026thinsp;1.0 (range: 1\u0026ndash;5). (Table\u0026nbsp;\u003cspan refid=\"Tab2\" class=\"InternalRef\"\u003e2\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab2\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 2\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e\u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"2\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eHistology\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eMedian (\u0026plusmn;\u0026thinsp;IQR) or N (%)\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eNumber of passes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e2 (\u0026plusmn;\u0026thinsp;1)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c2\" namest=\"c1\"\u003e \u003cp\u003eHistologic Diagnosis\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSerous Cyst Adenoma\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e31 (79.5%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eBenign Pancreatic parenchyma\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e5 (12.8%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eRenal Clear Cell Carcinoma\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e1 (2.6%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eNon-Diagnostic\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e2 (5.1%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eComplications: One patient experienced intra-lesional bleeding after the initial needle puncture, resulting in only one pass being obtained. Although there was no evidence of bleeding at the end of the procedure, the patient reported abdominal pain and was admitted for observation. A computed tomography (CT) scan of the abdomen and pelvis was unremarkable, and the pain resolved spontaneously without requiring further intervention. No other adverse events, such as infection, perforation, or pancreatitis, were noted in the study cohort.\u003c/p\u003e"},{"header":"Discussion","content":"\u003cp\u003eThe increasing use of abdominal imaging has led to a higher incidental detection of cystic neoplasms of the pancreas on cross-sectional imaging and abdominal ultrasound.\u003csup\u003e\u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e19\u003c/span\u003e\u003c/sup\u003e Among these cystic neoplasms, microcystic SCNs represent a common variant, accounting for approximately one-third of all pancreatic cystic neoplasms (PCNs).\u003csup\u003e\u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e20\u003c/span\u003e\u003c/sup\u003e Unlike mucinous cysts, these lesions are typically benign, with less than 1% transforming into serous cystadenocarcinomas.\u003csup\u003e\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e\u003c/sup\u003e This case series corroborates the predominance of microcystic SCNs in women and the later age of diagnosis, typically occurring in the 5th to 7th decade of life.\u003csup\u003e\u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e22\u003c/span\u003e\u003c/sup\u003e Most patients with SCNs are asymptomatic, but when symptoms do occur, they often include abdominal pain, the presence of an abdominal mass, or early satiety.\u003csup\u003e\u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e23\u003c/span\u003e,\u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e24\u003c/span\u003e\u003c/sup\u003e\u003c/p\u003e \u003cp\u003eCT is the most widely used radiographic test for evaluating microcystic SCNs, on which, these lesions exhibit a characteristic \"honeycomb\" appearance with a central fibronodular scar.\u003csup\u003e\u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e25\u003c/span\u003e\u003c/sup\u003e The central fibrous scar, also referred to as a \"stellate central scar,\" is enhanced with iodinated contrast on CT, serving as an important distinguishing feature of SCNs, as they are considered the only hypervascular PCNs.\u003csup\u003e\u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e26\u003c/span\u003e,\u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e27\u003c/span\u003e\u003c/sup\u003e When further imaging is necessary, endoscopic ultrasound is often employed to obtain high-resolution images of the lesions, as it is considered the ideal imaging modality. Additionally, EUS can be combined with FNA and/or FNB for further evaluation of the lesion.\u003csup\u003e\u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e28\u003c/span\u003e\u003c/sup\u003e\u003c/p\u003e \u003cp\u003eWhile FNA and FNB can assist in acquiring a definitive diagnosis for the type of PCN, it is crucial to acknowledge the potential pitfalls of these interventions, including sampling error, inadequate cystic contents, and inherent risks of complications such as acute pancreatitis, abdominal pain, bleeding, and infection.\u003csup\u003e\u003cspan additionalcitationids=\"CR30\" citationid=\"CR29\" class=\"CitationRef\"\u003e29\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e31\u003c/span\u003e\u003c/sup\u003e FNA, which is more commonly performed than FNB, allows clinicians to perform cyst fluid analysis. Fluid analysis is highly accurate in differentiating mucinous from non-mucinous lesions but is usually not diagnostic for SCNs. Additionally, in patients with microcystic SCNs, the cytology sample obtained is often inadequate for diagnosis.\u003csup\u003e\u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e32\u003c/span\u003e\u003c/sup\u003e In contrast, FNB enables a more accurate diagnosis by providing a core biopsy of the cyst wall and the internal septations, allowing pathologists to evaluate the cyst wall histology for subtyping and grading of dysplasia. This approach can lead to a reduction in surveillance imaging and prevent unnecessary invasive interventions for further workup.\u003csup\u003e\u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e33\u003c/span\u003e,\u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e34\u003c/span\u003e\u003c/sup\u003e\u003c/p\u003e \u003cp\u003eThe safety and feasibility of EUS-guided FNB for diagnosing microcystic SCNs have been a topic of debate, with some studies suggesting an elevated risk of intraprocedural bleeding.\u003csup\u003e\u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e35\u003c/span\u003e\u003c/sup\u003e However, our case series challenges this notion, demonstrating a low incidence of adverse events and no significant bleeding complications. The ability to obtain a definitive diagnosis through FNB can have substantial implications for patient management, as it eliminates the need for follow-up imaging and surveillance once the diagnosis is confirmed. Moreover, this approach can help prevent unnecessary surgical interventions in cases of larger lesions where EUS-guided FNA fails to yield a diagnosis.\u003csup\u003e\u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e36\u003c/span\u003e,\u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e37\u003c/span\u003e\u003c/sup\u003e Despite avoiding unnecessary surgery in majority of the patients, one of the patients in the study with a non-diagnostic FNB underwent surgical resection due to high-risk imaging features (duct dilatation, interval increase in size, and abdominal discomfort). The final pathology for this patient who underwent surgical resection was SCN.\u003c/p\u003e \u003cp\u003eDespite the promising findings of our study, it is important to acknowledge its limitations. The retrospective nature of the study and the relatively small sample size may limit the generalizability of the results. Additionally, the single-center design may introduce potential biases related to institutional practices and expertise. Future prospective, multicenter studies with larger patient cohorts are needed to further validate the safety and efficacy of EUS-guided FNB for the diagnosis of microcystic SCNs.\u003c/p\u003e"},{"header":"Conclusion","content":"\u003cp\u003eOur case series highlights the safety and feasibility of EUS-guided FNB for diagnosing microcystic SCNs, challenging previous literature suggesting elevated intraprocedural bleeding risks. This diagnostic approach offers the potential for cost-effectiveness by eliminating the need for follow-up imaging and surveillance once a definitive diagnosis is established. Furthermore, it can help prevent unnecessary surgical interventions in cases where EUS-guided FNA fails to provide a diagnosis. As the incidental detection of pancreatic cystic neoplasms continues to rise with the increasing use of abdominal imaging, the role of EUS-guided FNB in the diagnostic algorithm for microcystic SCNs warrants further consideration to optimize patient management and outcomes.\u003c/p\u003e"},{"header":"Declarations","content":"\u003ch2\u003eAuthor Contribution\u003c/h2\u003e\u003cp\u003eK.G., K.B., and A.S. wrote the main manuscript text. K.G., T.W., G.K, N.Z, and A.S. collected and analyzed the data. K.G, R.A., and A.S. prepared the figures. N.M, C.C, I.W., and A.S, performed the procedures. All authors reviewed the manuscript.\u003c/p\u003e\u003ch2\u003eData Availability\u003c/h2\u003e\u003cp\u003eRaw data for our dataset is not publicly available to preserve individuals\u0026rsquo; privacy.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eKromrey ML, B\u0026uuml;low R, H\u0026uuml;bner J, et al. 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Nov 2014;122(11):804\u0026ndash;9. doi:\u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003e10.1002/cncy.21460\u003c/span\u003e\u003cspan address=\"10.1002/cncy.21460\" targettype=\"DOI\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eCorrea-Gallego C, Ferrone CR, Thayer SP, Wargo JA, Warshaw AL, Fern\u0026aacute;ndez-Del Castillo C. Incidental pancreatic cysts: do we really know what we are watching? Pancreatology. 2010;10(2\u0026ndash;3):144\u0026ndash;50. doi:\u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003e10.1159/000243733\u003c/span\u003e\u003cspan address=\"10.1159/000243733\" targettype=\"DOI\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"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":"","lastPublishedDoi":"10.21203/rs.3.rs-5435718/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-5435718/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003e\u003cstrong\u003eBackground:\u003c/strong\u003e Pancreatic cysts, frequently identified incidentally on imaging, present diagnostic challenges due to their variable malignant potential. Serous cystic neoplasms (SCNs) are benign and account for 1-2% of pancreatic lesions. However, imaging techniques alone often lack the accuracy to definitively diagnose these lesions, leading to unnecessary surveillance and interventions.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAims:\u003c/strong\u003e This study evaluates the safety and diagnostic efficacy of endoscopic ultrasound-guided fine-needle biopsy (EUS-FNB) for identifying microcystic SCNs.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eMethods: \u003c/strong\u003eWe conducted a retrospective analysis of 39 patients who underwent EUS-FNB for solitary pancreatic lesions with microcystic features, identified through cross-sectional imaging at our medical center between 2018 and 2024. Patients with a stellate scar or definitive imaging features of microcystic SCNs were excluded. Outcomes assessed included histologic results and complications.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eResults:\u003c/strong\u003e Histological confirmation of microcystic SCN was achieved in 79.5% of cases, eliminating the need for further imaging and surveillance. A single complication—mild intra-lesional bleeding—occurred in one patient, which resolved without further intervention.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConclusions: \u003c/strong\u003eEUS-FNB is a safe and effective method for diagnosing microcystic SCNs, offering a definitive diagnosis and reducing unnecessary surveillance and interventions. This approach provides a favorable risk-benefit profile for managing SCNs. However, future multicenter studies with larger cohorts are needed to further validate these findings and refine diagnostic protocols for pancreatic cystic neoplasms.\u003c/p\u003e","manuscriptTitle":"The Use of Endoscopic Ultrasound Guided Fine Needle Biopsy for the Diagnosis of Microcystic Serous Cystic Neoplasms of the Pancreas","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-12-16 17:29:19","doi":"10.21203/rs.3.rs-5435718/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":"e654d956-66a6-476a-a542-cf2a8725164f","owner":[],"postedDate":"December 16th, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[],"tags":[],"updatedAt":"2024-12-24T02:53:32+00:00","versionOfRecord":[],"versionCreatedAt":"2024-12-16 17:29:19","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-5435718","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-5435718","identity":"rs-5435718","version":["v1"]},"buildId":"qtupq5eGEP_6zYnWcrvyt","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}