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• W4364375976 abstract "Affecting primarily the large extrahepatic bile ducts, primary sclerosing cholangitis (PSC) is a chronic, inflammatory, and fibro-obliterative cholangiopathy with an unknown trigger.[1]European Association for the Study of the Liver. Electronic address eee, European Association for the Study of the LEASL clinical practice guidelines on sclerosing cholangitis.J Hepatol. 2022; 77: 761-806Abstract Full Text Full Text PDF PubMed Scopus (26) Google Scholar In PSC, concomitant inflammatory bowel disease (IBD) is prevalent, with ulcerative colitis (UC) diagnosed in the majority of such cases. However, UC in patients with PSC differs from classical UC[2]Beheshti-Maal A. Tamimi A. Iravani S. Memarnejadian A. Sorouri M. Aghdaei H.A. et al.PSC associated inflammatory bowel disease: a distinct entity.Expert Rev Gastroenterol Hepatol. 2022; 16: 129-139Crossref PubMed Scopus (2) Google Scholar with (i) a predominantly right-sided and often mild-to-moderate colitis, (ii) a significantly higher risk for colon cancer in the ascending colon, and (iii) different responses to pharmacological therapies. As such, in the pathophysiology of PSC-IBD, the idea of a gut-liver-axis has been hypothesized, whereby a gut-derived trigger reaches the large bile ducts in disease onset.[3]Hov J.R. Karlsen T.H. The microbiota and the gut-liver axis in primary sclerosing cholangitis.Nat Rev Gastro Hepat. 2022; 20: 135-154Crossref PubMed Scopus (0) Google Scholar However, a unifying concept on the pathogenesis of PSC remains elusive, e.g. with neither direct evidence of a “toxic bile”[4]Gauss A. Ehehalt R. Lehmann W.D. Erben G. Weiss K.H. Schaefer Y. et al.Biliary phosphatidylcholine and lysophosphatidylcholine profiles in sclerosing cholangitis.World J Gastroentero. 2013; 19: 5454-5463Crossref PubMed Scopus (26) Google Scholar nor a specific role of long-lived, gut-derived lymphocytes.[5]Graham J.J. Mukherjee S. Yuksel M. Mateos R.S. Si T.F. Huang Z.L. et al.Aberrant hepatic trafficking of gut-derived T cells is not specific to primary sclerosing cholangitis.Hepatology. 2022; 75: 518-530Crossref PubMed Scopus (11) Google Scholar Also, even if such a trigger exists, how it could reach the large bile ducts remains in question. One idea involves the portal vein (PV), whereby translocated gut-derived components travel in the PV to the liver sinusoids (possibly activating inflammatory pathways), are taken up by hepatocytes, and then enter into the biliary system via canalicular transport/secretion (akin to bile acids and other cholephiles). However, such a scenario suggests an initial, awaited injury to the small bile ducts, which is not the case in PSC. Perhaps there exists a more direct path to the large bile ducts via PV branches. The blood supply to the extrahepatic bile ducts is derived from branches of the hepatic artery (HA).[6]Morell C.M. Fabris L. Strazzabosco M. Vascular biology of the biliary epithelium.J Gastroenterol Hepatol. 2013; 28: 26-32Crossref PubMed Scopus (23) Google Scholar For the common bile duct (CBD), these branches supply the epicholedocal and pericholedocal arterial plexuses.[7]Ramesh Babu C.S. Sharma M. Biliary tract anatomy and its relationship with venous drainage.J Clin Exp Hepatol. 2014; 4: S18-S26Abstract Full Text Full Text PDF PubMed Scopus (54) Google Scholar The venous drainage follows the same, with the epicholedochal venous plexus (of Saint) draining into marginal veins of the paracholedochal venous plexus (of Petren), which eventually connect into veins that drain into the PV. However, the PV is known to supply ∼75% of the total blood flow and ∼50% of the total amount of oxygenated blood to the liver. Also, in patients undergoing pancreatoduonectomy, the PV was shown on intraoperative Doppler ultrasound to contribute ∼40% of the microvascular blood flow surrounding the CBD.[8]Slieker J.C. Farid W.R.R. van Eijck C.H.J. Lange J.F. van Bommel J. Metselaar H.J. et al.Significant contribution of the portal vein to blood flow through the common bile duct.Ann Surg. 2012; 255: 523-527Crossref PubMed Scopus (32) Google Scholar In a different study involving similar operative patients, the space surrounding the CBD helped characterize a new anatomical structure called the interstitium: a pre-lymphatic space of fluid-filled collagen bundles lined with cells positive for vascular and lymphatic endothelial markers.[9]Benias P.C. Wells R.G. Sackey-Aboagye B. Klavan H. Reidy J. Buonocore D. et al.Structure and distribution of an unrecognized interstitium in human tissues.Sci Rep. 2018; 8: 4947Crossref PubMed Scopus (208) Google Scholar As first reported by Couinaud, the parabiliary venous plexus alongside the anterior PV is thought to be an accessory portal system of different embryonic origins to the PV system.[7]Ramesh Babu C.S. Sharma M. Biliary tract anatomy and its relationship with venous drainage.J Clin Exp Hepatol. 2014; 4: S18-S26Abstract Full Text Full Text PDF PubMed Scopus (54) Google Scholar Perhaps there also exist PV branches or a parabiliary PV plexus passing through the interstitium of the CBD before draining back into the PV. We therefore explored whether such a pathway could exist in vivo in mice (n = 5, BL/6, 6-months old, 25 g BW). Indian Ink was introduced into the PV via median laparatomy under general anesthesia (isoflurane) at an infusion rate of 1 ml/min (well below the PV flow-rate observed in mice).[10]Xie C. Wei W. Zhang T. Dirsch O. Dahmen U. Monitoring of systemic and hepatic hemodynamic parameters in mice.J Vis Exp. 2014; e51955Crossref Google Scholar The liver and ligamentum hepatoduodenale were retrieved en bloc after euthanasia by cervical dislocation. On histology, Indian ink filled the liver sinusoids (Fig. 1A), and, notably, the vessels surrounding the large bile ducts (e.g. within the CBD wall) and interstitium (Fig. 1B and Fig. S1). Thus, in mice, there could be PV branches that travel through the vascular space and interstitium surrounding the CBD and large bile ducts before draining back into the PV. We then asked whether the same phenotype was present in human samples. In brief, the liver and ligamentum hepataduodenale were retrieved en bloc from whole-body anatomical donations within 48 hours post-mortem (n = 5). After irrigation with crystalloid, the HA and PV were slowly infused with blue and red acrylic respectively at physiologic parameters similar to those previously described (see Supplementary Methods). Similar to our observations in mice, histology of human samples showed the CBD primarily surrounded by branches from the PV (Fig. 1C, D). Thus, in both mice and humans, a pathway could exist from the PV to the CBD, with PV branches traveling through a parabiliary vascular space and interstitium surrounding the large bile ducts. To help visualize these branches, we next performed microCT on human samples (n = 2), which were prepared and retrieved as described above, except the PV was infiltrated with acrylic mixed with gadolinium and the HA with acrylic only (see Supplementary Methods). On microCT, a network or plexus of PV branches appear present in the interstitium surrounding the large bile ducts (Fig. 1G, H and Supplementary Video 1). The following is/are the supplementary data related to this article:eyJraWQiOiI4ZjUxYWNhY2IzYjhiNjNlNzFlYmIzYWFmYTU5NmZmYyIsImFsZyI6IlJTMjU2In0.eyJzdWIiOiI2MWZiOGM5NTlkNzRmMDNkOTAxOTM2NDJkZGRlODM0NiIsImtpZCI6IjhmNTFhY2FjYjNiOGI2M2U3MWViYjNhYWZhNTk2ZmZjIiwiZXhwIjoxNjg2MTA3NTg2fQ.lY_YZhcFFQGBeYSZuz8NsCYiNvX-vOy9G_536Rpt_98F-NrME_F84DTlQuTwIHo0EcrudCGUN6rrOupUgGW78Ayn_dyH2LFajJJ3EZBSjAiDalZgxsg3XEJ0Y_gWPE-HGMt9WGN-CKsnE18uGXW7qfTYG2skuhjSQ2ube6oxRU88lHmFDxxZZdqfMIZJoFUYtxoM4y9AemL7OIYDR3nLKQ9UjscRmNyPGpM6b5ZYjqTFLYZLhiqfyEyWc215SV_hGcdNCCYfV9waIDmk-PIiJXFopBlLPAeUs3b0sfSAHcbJh25f5z60LkWsBmu3X323HSNdm3G04N6-T_fK9qZ8dw(mp4, (7.94 MB) Download video eyJraWQiOiI4ZjUxYWNhY2IzYjhiNjNlNzFlYmIzYWFmYTU5NmZmYyIsImFsZyI6IlJTMjU2In0.eyJzdWIiOiI2MWZiOGM5NTlkNzRmMDNkOTAxOTM2NDJkZGRlODM0NiIsImtpZCI6IjhmNTFhY2FjYjNiOGI2M2U3MWViYjNhYWZhNTk2ZmZjIiwiZXhwIjoxNjg2MTA3NTg2fQ.lY_YZhcFFQGBeYSZuz8NsCYiNvX-vOy9G_536Rpt_98F-NrME_F84DTlQuTwIHo0EcrudCGUN6rrOupUgGW78Ayn_dyH2LFajJJ3EZBSjAiDalZgxsg3XEJ0Y_gWPE-HGMt9WGN-CKsnE18uGXW7qfTYG2skuhjSQ2ube6oxRU88lHmFDxxZZdqfMIZJoFUYtxoM4y9AemL7OIYDR3nLKQ9UjscRmNyPGpM6b5ZYjqTFLYZLhiqfyEyWc215SV_hGcdNCCYfV9waIDmk-PIiJXFopBlLPAeUs3b0sfSAHcbJh25f5z60LkWsBmu3X323HSNdm3G04N6-T_fK9qZ8dw(mp4, (7.94 MB) Download video Taken together, our data in mice and human samples suggest a possible anatomical correlate for a gut-large-bile-duct-axis, with PV branches or a parabiliary PV plexus traveling through the pre-lymphatic interstitium of the CBD. Such an enterobiliary pathway shown herein would help to lay an important foundation for future work on the pathophysiology of PSC and other anatomically related pathologies of the large bile ducts. The authors received no financial support to produce this manuscript. Authors declare that they have no conflicts of interest. Please refer to the accompanying ICMJE disclosure forms for further details. A.L.: designed the experiments, contributed data and analysis tools, collection of data, and wrote the manuscript. H.R.: contributed data and analysis tools. N.H.: contributed data and analysis tools, supervised the project. H.D.: contributed data and analysis tools, supervised the project. P.F.: conceived the hypothesis, designed the experiments, contributed data and analysis tools, collection of data, wrote the manuscript, and supervised the project. The authors wish to thank Dr. Eduardo Machado-Charry, Ph.D. (Institute for Solid State Physics, Graz University of Technology) for his technical assistance with the TESCAN microCT and 3D rendering, and Dr. Emina Talakic, M.D. (Department of Radiology, Medical University of Graz) for her careful review of the microCT images. The following are the supplementary data to this article: Download .pdf (.32 MB) Help with pdf files Multimedia component 1 Download .pdf (.54 MB) Help with pdf files Mutimedia component 3" @default.
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• W4364375976 title "Portal venous branches as an anatomic railroad for a gut-bile duct-axis" @default.
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