Eur J Pediatr Surg 2019; 29(04): 336-341
DOI: 10.1055/s-0039-1694009
Review Article
Georg Thieme Verlag KG Stuttgart · New York

Translational Research in Biliary Atresia: News from Mice and Men

Omid Madadi-Sanjani
1   Center of Pediatric Surgery, Hannover Medical School, Hannover, Germany
,
Claus Petersen
1   Center of Pediatric Surgery, Hannover Medical School, Hannover, Germany
› Author Affiliations
Further Information

Publication History

09 June 2019

25 June 2019

Publication Date:
14 August 2019 (online)

Abstract

Biliary atresia (BA) is a fibro-obliterative cholangiopathy of unknown etiology. While Kasai portoenterostomy achieves temporary biliary drainage in some cases, BA remains the most common indication for liver transplantation during childhood. During the last few decades, observations on BA, like cholestatic diseases in animals and the introduction of different animal models for BA, have not achieved the anticipated results, and we are still not able to translate the basic research to the patient's bedside. This article presents a review of the literature on available BA animal models and gives a glimpse of future developments.

 
  • References

  • 1 Lomer R. Ueber einen Fall von congenitaler partieller Obliteration der Gallengänge. Arch Pathol Anat Physiol Klin Med 1885; 99 (01) 130-139
  • 2 Thomson J. On congenital obliteration of the bile-ducts. Trans Edinb Obstet Soc 1892; 17 (08) 17-49
  • 3 Holmes JB. Congenital obliteration of the bile ducts: diagnosis and suggestions for treatment. Am J Dis Child 1916; 11: 405-431
  • 4 Ladd WE. Congenital atresia and stenosis of the bile ducts. JAMA 1928; 91 (15) 1082-1085
  • 5 Kasai M, Suzuki S. A new operation for, ‘non-correctable’ biliary atresia: hepatic porto-enterostomy. Shujitsu 1959; 13: 733-739
  • 6 Fricker J. Thomas Starzl. BMJ 2017; 357: j1806
  • 7 Calne RY, Rolles K, White DJ. , et al. Cyclosporin A initially as the only immunosuppressant in 34 recipients of cadaveric organs: 32 kidneys, 2 pancreases, and 2 livers. Lancet 1979; 2 (8151): 1033-1036
  • 8 Madadi-Sanjani O, Petersen C. Perioperative developments in biliary atresia treatment. Curr Pathobiol Rep 2018; 6 (04) 241-246
  • 9 Davenport M. Biliary atresia: from Australia to the zebrafish. J Pediatr Surg 2016; 51 (02) 200-205
  • 10 Leung DH, Narang A, Minard CG, Hiremath G, Goss JA, Shepherd R. A 10-Year united network for organ sharing review of mortality and risk factors in young children awaiting liver transplantation. Liver Transpl 2016; 22 (11) 1584-1592
  • 11 Arnon R, Annunziato RA, D'Amelio G, Chu J, Shneider BL. Liver transplantation for biliary atresia: is there a difference in outcome for infants?. J Pediatr Gastroenterol Nutr 2016; 62 (02) 220-225
  • 12 Arnon R, Annunziato R, Miloh T. , et al. Liver transplantation in children weighing 5 kg or less: analysis of the UNOS database. Pediatr Transplant 2011; 15 (06) 650-658
  • 13 Davenport M, Ong E, Sharif K. , et al. Biliary atresia in England and Wales: results of centralization and new benchmark. J Pediatr Surg 2011; 46 (09) 1689-1694
  • 14 Tyraskis A, Davenport M. Steroids after the Kasai procedure for biliary atresia: the effect of age at Kasai portoenterostomy. Pediatr Surg Int 2016; 32 (03) 193-200
  • 15 Qiu J-L, Shao M-Y, Xie W-F. , et al. Effect of combined ursodeoxycholic acid and glucocorticoid on the outcome of Kasai procedure: a systematic review and meta-analysis. Medicine (Baltimore) 2018; 97 (35) e12005
  • 16 Zhang M-Z, Xun P-C, He K, Cai W. Adjuvant steroid treatment following Kasai portoenterostomy and clinical outcomes of biliary atresia patients: an updated meta-analysis. World J Pediatr 2017; 13 (01) 20-26
  • 17 Petersen C, Biermanns D, Kuske M, Schäkel K, Meyer-Junghänel L, Mildenberger H. New aspects in a murine model for extrahepatic biliary atresia. J Pediatr Surg 1997; 32 (08) 1190-1195
  • 18 Petersen C, Grasshoff S, Luciano L. Diverse morphology of biliary atresia in an animal model. J Hepatol 1998; 28 (04) 603-607
  • 19 Klemann C, Schröder A, Dreier A. , et al. Interleukin 17, produced by γδ T cells, contributes to hepatic inflammation in a mouse model of biliary atresia and is increased in livers of patients. Gastroenterology 2016; 150 (01) 229.e5-241.e5
  • 20 Bastianello SS, Nesbit JW. The pathology of a case of biliary atresia in a foal. J S Afr Vet Assoc 1986; 57 (02) 117-120
  • 21 Thiel C, Steinbach S, Schmidt M. , et al. Extrahepatic biliary atresia in a 4-week-old Pug. Vet Surg 2015; 44 (01) 35-40
  • 22 Harper P, Plant JW, Unger DB. Congenital biliary atresia and jaundice in lambs and calves. Aust Vet J 1990; 67 (01) 18-22
  • 23 Cai S-Y, Lionarons DA, Hagey L, Soroka CJ, Mennone A, Boyer JL. Adult sea lamprey tolerates biliary atresia by altering bile salt composition and renal excretion. Hepatology 2013; 57 (06) 2418-2426
  • 24 Lorent K, Moore JC, Siekmann AF, Lawson N, Pack M. Reiterative use of the notch signal during zebrafish intrahepatic biliary development. Dev Dyn 2010; 239 (03) 855-864
  • 25 Lorent K, Gong W, Koo KA. , et al. Identification of a plant isoflavonoid that causes biliary atresia. Sci Transl Med 2015; 7 (286) 286ra67
  • 26 Chung-Davidson Y-W, Davidson PJ, Scott AM. , et al. A new clarification method to visualize biliary degeneration during liver metamorphosis in sea lamprey (Petromyzon marinus). J Vis Exp 2014; (88) e51648
  • 27 Yeh C-Y, Chung-Davidson Y-W, Wang H, Li K, Li W. Intestinal synthesis and secretion of bile salts as an adaptation to developmental biliary atresia in the sea lamprey. Proc Natl Acad Sci U S A 2012; 109 (28) 11419-11424
  • 28 Suchy FJ. Biliary atresia in sea lampreys. What can it tell us about the disorder in human infants?. Hepatology 2013; 57 (06) 2114-2116
  • 29 Petersen C. Biliary atresia: the animal models. Semin Pediatr Surg 2012; 21 (03) 185-191
  • 30 Rabin, Vardi, Jovici N. The intrahepatic portal vein-hepatic artery relationship. Surg Gynecol Obstet 1965; 120: 38-44
  • 31 Morgan Jr WW, Rosenkrantz JC, Hill Jr RB. Hepatic arterial interruption in the fetus--an attempt to simulate biliary atresia. J Pediatr Surg 1966; 1 (04) 342-346
  • 32 Holder TM, Ashcraft KW. Production of experimental biliary atresia by ligation of the common bile duct in the fetus. Surg Forum 1966; 17: 356-357
  • 33 Spitz L. Ligation of the common bile duct in the fetal lamb: an experimental model for the study of biliary atresia. Pediatr Res 1980; 14 (05) 740-748
  • 34 Schweizer P. Modell einer extrahepatischen Gallengangsatresie. Z Kinderchir 1974; 14: 90-101
  • 35 Wang J-B, Liu C, Yeh Y-C. , et al. A novel rat model simulating biliary atresia after a Kasai operation. J Invest Surg 2014; 27 (03) 183-190
  • 36 de Aro Braz MJ, Corbi LE, Tannuri ACA. , et al. Analysis of the reversibility of biliary cirrhosis in young rats submitted to biliary obstruction. J Pediatr Surg 2018; 53 (07) 1408-1413
  • 37 Ogawa T, Suruga K, Kojima Y, Kitahara T, Kuwabara N. Experimental study of the pathogenesis of infantile obstructive cholangiopathy and its clinical evaluation. J Pediatr Surg 1983; 18 (02) 131-135
  • 38 Schmeling DJ, Oldham KT, Guice KS, Kunkel RG, Johnson KJ. Experimental obliterative cholangitis. A model for the study of biliary atresia. Ann Surg 1991; 213 (04) 350-355
  • 39 Tatekawa Y, Nakada A, Nakamura T. Intrahepatic biliary ablation with pure ethanol: an experimental model of biliary atresia. Surg Today 2013; 43 (06) 661-669
  • 40 Andrade Wde C, Tannuri U, da Silva LFF, Alves VAF. Effects of the administration of pentoxifylline and prednisolone on the evolution of portal fibrogenesis secondary to biliary obstruction-an experimental study in growing animals. J Pediatr Surg 2009; 44 (11) 2071-2077
  • 41 Chen C-C, Ho C-Y, Chaung H-C. , et al. Fish omega-3 fatty acids induce liver fibrosis in the treatment of bile duct-ligated rats. Dig Dis Sci 2013; 58 (02) 440-447
  • 42 Riepenhoff-Talty M, Schaekel K, Clark HF. , et al. Group A rotaviruses produce extrahepatic biliary obstruction in orally inoculated newborn mice. Pediatr Res 1993; 33 (4, Pt 1): 394-399
  • 43 Petersen C, Davenport M. Aetiology of biliary atresia: what is actually known?. Orphanet J Rare Dis 2013; 8: 128
  • 44 Petersen C, Madadi-Sanjani O. Role of viruses in biliary atresia: news from mice and men. Innov Surg Sci 2018; 3 (02) 101-106
  • 45 Leonhardt J, Kuebler JF, Turowski C, Tschernig T, Geffers R, Petersen C. Susceptibility to experimental biliary atresia linked to different hepatic gene expression profiles in two mouse strains. Hepatol Res 2010; 40 (02) 196-203
  • 46 Barnes BH, Tucker RM, Wehrmann F, Mack DG, Ueno Y, Mack CL. Cholangiocytes as immune modulators in rotavirus-induced murine biliary atresia. Liver Int 2009; 29 (08) 1253-1261
  • 47 Jafri M, Donnelly B, Allen S. , et al. Cholangiocyte expression of alpha2beta1-integrin confers susceptibility to rotavirus-induced experimental biliary atresia. Am J Physiol Gastrointest Liver Physiol 2008; 295 (01) G16-G26
  • 48 Oetzmann von Sochaczewski C, Pintelon I, Brouns I. , et al. Rotavirus particles in the extrahepatic bile duct in experimental biliary atresia. J Pediatr Surg 2014; 49 (04) 520-524
  • 49 Czech-Schmidt G, Verhagen W, Szavay P, Leonhardt J, Petersen C. Immunological gap in the infectious animal model for biliary atresia. J Surg Res 2001; 101 (01) 62-67
  • 50 Kuebler JF, Czech-Schmidt G, Leonhardt J, Ure BM, Petersen C. Type-I but not type-II interferon receptor knockout mice are susceptible to biliary atresia. Pediatr Res 2006; 59 (06) 790-794
  • 51 Chan RYY, Tan CEL, Czech-Schmidt G, Petersen C. Computerized three-dimensional study of a rotavirus model of biliary atresia: comparison with human biliary atresia. Pediatr Surg Int 2005; 21 (08) 615-620
  • 52 Sundaram SS, Mack CL, Feldman AG, Sokol RJ. Biliary atresia: indications and timing of liver transplantation and optimization of pretransplant care. Liver Transpl 2017; 23 (01) 96-109
  • 53 Kasahara M, Umeshita K, Sakamoto S, Fukuda A, Furukawa H, Uemoto S. Liver transplantation for biliary atresia: a systematic review. Pediatr Surg Int 2017; 33 (12) 1289-1295
  • 54 Chardot C, Buet C, Serinet M-O. , et al. Improving outcomes of biliary atresia: French national series 1986-2009. J Hepatol 2013; 58 (06) 1209-1217
  • 55 Asai A, Miethke A, Bezerra JA. Pathogenesis of biliary atresia: defining biology to understand clinical phenotypes. Nat Rev Gastroenterol Hepatol 2015; 12 (06) 342-352
  • 56 Al-Masri AN, Flemming P, Rodeck B, Melter M, Leonhardt J, Petersen C. Expression of the interferon-induced Mx proteins in biliary atresia. J Pediatr Surg 2006; 41 (06) 1139-1143
  • 57 Rauschenfels S, Krassmann M, Al-Masri AN. , et al. Incidence of hepatotropic viruses in biliary atresia. Eur J Pediatr 2009; 168 (04) 469-476
  • 58 Girard M, Panasyuk G. Genetics in biliary atresia. Curr Opin Gastroenterol 2019; 35 (02) 73-81
  • 59 Cameron-Christie SR, Wilde J, Gray A. , et al. Genetic investigation into an increased susceptibility to biliary atresia in an extended New Zealand Māori family. BMC Med Genomics 2018; 11 (01) 121
  • 60 Lin Z, Xie X, Lin H. , et al. Epistatic association of CD14 and NOTCH2 genetic polymorphisms with biliary atresia in a southern Chinese population. Mol Ther Nucleic Acids 2018; 13: 590-595
  • 61 Liang J, Wen Z, Zhao J. , et al. Association of IL18 genetic polymorphisms with increased risk of biliary atresia susceptibility in southern Chinese children. Gene 2018; 677: 228-231
  • 62 Tian L, Ye Z, Kafka K. , et al. Biliary atresia relevant human induced pluripotent stem cells recapitulate key disease features in a dish. J Pediatr Gastroenterol Nutr 2019; 68 (01) 56-63
  • 63 Machhua S, Kumar Y, Prakash Kanojia R. , et al. An improved and easy protocol for primary epithelial cell culture from atretic tissue in biliary atresia. Tissue Cell 2019; 56: 83-89
  • 64 Yamazaki T, Wakai M, Enosawa S, Tokiwa T. Analysis of soluble factors in conditioned media derived from primary cultures of cirrhotic liver of biliary atresia. In Vitro Cell Dev Biol Anim 2017; 53 (06) 564-573
  • 65 Coots A, Donnelly B, Mohanty SK, McNeal M, Sestak K, Tiao G. Rotavirus infection of human cholangiocytes parallels the murine model of biliary atresia. J Surg Res 2012; 177 (02) 275-281