An overview of animal models for investigating the pathogenesis and therapeutic strategies in acute hepatic failure

World Journal of Gastroenterology

Volumn 15, Issue 25, 2009, Pages 3086-3098

  Tuñón, María Jesús ^a   Alvarez, Marcelino ^c   Culebras, Jesús M ^a,b   González Gallego, Javier ^a  

^a UNIVERSITY OF LEÓN   (Spain)

^b Hospital of Leon   (Spain)

^c Department of Animal Health   (Spain)

Author keywords

Acute hepatic failure; Chemical models; Surgical models; Viral models

Indexed keywords

AMANITIN; AZOXYMETHANE; CARBON TETRACHLORIDE; CONCANAVALIN A; GALACTOSAMINE; LIPOPOLYSACCHARIDE; PARACETAMOL; POISON; THIOACETAMIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; BLEEDING DISORDER; CHEMICAL MODEL; CLINICAL FEATURE; DEVASCULARIZATION; DISEASE MODEL; DOG; EXPERIMENTAL ANIMAL; HEPATIC ENCEPHALOPATHY; LIVER FAILURE; MOUSE; NONHUMAN; PARTIAL HEPATECTOMY; PATHOGENESIS; RABBIT; RAT; REVIEW; SWINE;

EID: 67651250551     PISSN: 10079327     EISSN: None     Source Type: Journal    
DOI: 10.3748/wjg.15.3086     Document Type: Review

References (163)

1. Auzinger G, Wendon J. Intensive care management of acute liver failure. Curr Opin Crit Care 2008; 14: 179-188
2. Nussler A, Konig S, Ott M, Sokal E, Christ B, Thasler W, Brulport M, Gabelein G, Schormann W, Schulze M, Ellis E, Kraemer M, Nocken F, Fleig W, Manns M, Strom SC, Hengstler JG. Present status and perspectives of cell-based therapies for liver diseases. J Hepatol 2006; 45: 144-159
3. Stravitz RT. Critical management decisions in patients with acute liver failure. Chest 2008; 134: 1092-1102
4. Riordan SM, Williams R. Perspectives on liver failure: past and future. Semin Liver Dis 2008; 28: 137-141
5. Trey C, Davidson LS. The management of fulminant hepatic failure. In: Popper H, Schaffner F, eds. Progress in liver disease. New York: Grune & Stratton, 1970; 3: 282-298
6. O'Grady JG, Williams R. Classification of acute liver failure. Lancet 1993; 342: 743
7. Bernuau J, Rueff B, Benhamou JP. Fulminant and subfulminant liver failure: definitions and causes. Semin Liver Dis 1986; 6: 97-106
8. Bernuau J, Benhamou JP. Classifying acute liver failure. Lancet 1993; 342: 252-253
9. Peláez-Luna M, Martinez-Salgado J, Olivera-Martinez MA. Utility of the MAYO End-Stage Liver Disease score, King's College Criteria, and a new in-hospital mortality score in the prognosis of in-hospital mortality in acute liver failure. Transplant Proc 2006; 38: 927-929
10. Tost JR. The Spanish Group for the Study of ALF. Characteristics of acute liver failure (ALF) in Spain. J Hepatol 2000; 32: 57
11. O'Grady JG, Alexander GJ, Hayllar KM, Williams R. Early indicators of prognosis in fulminant hepatic failure. Gastroenterology 1989; 97: 439-445
12. Fernández JA, Robles R, Marín C, Hernández Q, Sánchez Bueno F, Ramírez P, Rodríguez JM, Luján JA, Acosta F, Parrilla P. Fulminant hepatic failure and liver transplantation: experience of Virgen de la Arrixaca Hospital. Transplant Proc 2003; 35: 1852-1854
13. Lee WM. Etiologies of acute liver failure. Semin Liver Dis 2008; 28: 142-152
14. O'Grady JG. Acute liver failure. Postgrad Med J 2005; 81: 148-154
15. Ibáñez L, Pérez E, Vidal X, Laporte JR. Prospective surveillance of acute serious liver disease unrelated to infectious, obstructive, or metabolic diseases: epidemiological and clinical features, and exposure to drugs. J Hepatol 2002; 37: 592-600
16. Holubek WJ, Kalman S, Hoffman RS. Acetaminophen induced acute liver failure: results of a United States multicenter, prospective study. Hepatology 2006; 43: 880; author reply 882
17. Fontana RJ. Acute liver failure due to drugs. Semin Liver Dis 2008; 28: 175-187
18. Grabhorn E, Richter A, Burdelski M, Rogiers X, Ganschow R. Neonatal hemochromatosis: long-term experience with favorable outcome. Pediatrics 2006; 118: 2060-2065
19. Nakazawa H, Ito T, Makishima H, Misawa N, Okiyama W, Uehara T, Hidaka E, Kiyosawa K, Ishida F. Adenovirus fulminant hepatic failure: disseminated adenovirus disease after unrelated allogeneic stem cell transplantation for acute lymphoblastic leukemia. Intern Med 2006; 45: 975-980
20. Fontana RJ. Acute liver failure including acetaminophen overdose. Med Clin North Am 2008; 92: 761-794, viii
21. Lee WM, Seremba E. Etiologies of acute liver failure. Curr Opin Crit Care 2008; 14: 198-201
22. Córdoba J, Crespin J, Gottstein J, Blei AT. Mild hypothermia modifies ammonia-induced brain edema in rats after portacaval anastomosis. Gastroenterology 1999; 116: 686-693
23. Rose C, Michalak A, Rao KV, Quack G, Kircheis G, Butterworth RF. L-ornithine-L-aspartate lowers plasma and cerebrospinal fluid ammonia and prevents brain edema in rats with acute liver failure. Hepatology 1999; 30: 636-640
24. Izumi S, Langley PG, Wendon J, Ellis AJ, Pernambuco RB, Hughes RD, Williams R. Coagulation factor V levels as a prognostic indicator in fulminant hepatic failure. Hepatology 1996; 23: 1507-1511
25. Leifeld L, Dumoulin FL, Purr I, Janberg K, Trautwein C, Wolff M, Manns MP, Sauerbruch T, Spengler U. Early upregulation of chemokine expression in fulminant hepatic failure. J Pathol 2003; 199: 335-344
26. Zwingmann C, Chatauret N, Leibfritz D, Butterworth RF. Selective increase of brain lactate synthesis in experimental acute liver failure: results of a [H-C] nuclear magnetic resonance study. Hepatology 2003; 37: 420-428
27. Schiødt FV, Balko J, Schilsky M, Harrison ME, Thornton A, Lee WM. Thrombopoietin in acute liver failure. Hepatology 2003; 37: 558-561
28. Fischer JE, Funovics JM, Aguirre A, James JH, Keane JM, Wesdorp RI, Yoshimura N, Westman T. The role of plasma amino acids in hepatic encephalopathy. Surgery 1975; 78: 276-290
29. Swain M, Butterworth RF, Blei AT. Ammonia and related amino acids in the pathogenesis of brain edema in acute ischemic liver failure in rats. Hepatology 1992; 15: 449-453
30. Sielaff TD, Hu MY, Rollins MD, Bloomer JR, Amiot B, Hu WS, Cerra FB. An anesthetized model of lethal canine galactosamine fulminant hepatic failure. Hepatology 1995; 21: 796-804
31. Detry O, De Roover A, Honore P, Meurisse M. Brain edema and intracranial hypertension in fulminant hepatic failure: pathophysiology and management. World J Gastroenterol 2006; 12: 7405-7412
32. Bernal W, Hall C, Karvellas CJ, Auzinger G, Sizer E, Wendon J. Arterial ammonia and clinical risk factors for encephalopathy and intracranial hypertension in acute liver failure. Hepatology 2007; 46: 1844-1852
33. Bhatia V, Singh R, Acharya SK. Predictive value of arterial ammonia for complications and outcome in acute liver failure. Gut 2006; 55: 98-104
34. Clemmesen JO, Larsen FS, Kondrup J, Hansen BA, Ott P. Cerebral herniation in patients with acute liver failure is correlated with arterial ammonia concentration. Hepatology 1999; 29: 648-653
35. Jalan R, Olde Damink SW, Hayes PC, Deutz NE, Lee A. Pathogenesis of intracranial hypertension in acute liver failure: inflammation, ammonia and cerebral blood flow. J Hepatol 2004; 41: 613-620
36. Wendon J, Lee W. Encephalopathy and cerebral edema in the setting of acute liver failure: pathogenesis and management. Neurocrit Care 2008; 9: 97-102
37. Fausto N, Campbell JS, Riehle KJ. Liver regeneration. Hepatology 2006; 43: S45-S53
38. Khan SA, Shah N, Williams R, Jalan R. Acute liver failure: a review. Clin Liver Dis 2006; 10: 239-258, vii-viii
39. Riordan SM, Williams R. Acute liver failure: targeted artificial and hepatocyte-based support of liver regeneration and reversal of multiorgan failure. J Hepatol 2000; 32: 63-76
40. Miwa Y, Harrison PM, Farzaneh F, Langley PG, Williams R, Hughes RD. Plasma levels and hepatic mRNA expression of transforming growth factor-beta1 in patients with fulminant hepatic failure. J Hepatol 1997; 27: 780-788
41. Lyons RM, Keski-Oja J, Moses HL. Proteolytic activation of latent transforming growth factor-beta from fibroblast-conditioned medium. J Cell Biol 1988; 106: 1659-1665
42. Newsome PN, Nelson LJ, Ansell I, Ross JPC. Hayes R, Plevris JN. The inhibition of growth due to fulminant hepatic failure serum is not due to increased apoptosis/necrosis. J Hepatol 2000; 32 Suppl 2: 59
43. Limaye PB, Bhave VS, Palkar PS, Apte UM, Sawant SP, Yu S, Latendresse JR, Reddy JK, Mehendale HM. Upregulation of calpastatin in regenerating and developing rat liver: role in resistance against hepatotoxicity. Hepatology 2006; 44: 379-388
44. Jalan R. Acute liver failure: current management and future prospects. J Hepatol 2005; 42 Suppl: S115-S123
45. Chiu A, Fan ST. MARS in the treatment of liver failure: controversies and evidence. Int J Artif Organs 2006; 29: 660-667
46. Allen JW, Hassanein T, Bhatia SN. Advances in bioartificial liver devices. Hepatology 2001; 34: 447-455
47. Li LJ, Du WB, Zhang YM, Li J, Pan XP, Chen JJ, Cao HC, Chen Y, Chen YM. Evaluation of a bioartificial liver based on a nonwoven fabric bioreactor with porcine hepatocytes in pigs. J Hepatol 2006; 44: 317-324
48. Stadlbauer V, Jalan R. Acute liver failure: liver support therapies. Curr Opin Crit Care 2007; 13: 215-221
49. Newsome PN, Plevris JN, Nelson LJ, Hayes PC. Animal models of fulminant hepatic failure: a critical evaluation. Liver Transpl 2000; 6: 21-31
50. Rahman TM, Hodgson HJ. Animal models of acute hepatic failure. Int J Exp Pathol 2000; 81: 145-157
51. van de Kerkhove MP, Hoekstra R, van Gulik TM, Chamuleau RA. Large animal models of fulminant hepatic failure in artificial and bioartificial liver support research. Biomaterials 2004; 25: 1613-1625
52. Terblanche J, Hickman R. Animal models of fulminant hepatic failure. Dig Dis Sci 1991; 36: 770-774
53. Gorini P, Fogli L, Morsiani E. [Acute and fulminant liver failure: experimental models] Ann Ital Chir 2000; 71: 293-300
54. Filipponi F, Mosca F. Animal models of fulminant hepatic failure: need to test liver support devices. Dig Liver Dis 2001; 33: 607-613
55. Fournea I. Potentially reversible model of acute liver failure in the pig. A model to test the efficiency of bioartificial liver. Thesis: Leuven University Press, 2001; 41-56
56. Mann FC. Studies in the physiology of the liver: I. Technique and general effects of removal. Am J Med Sci 1921; 161: 37-42
57. He Y, Zhou J, Dou KF, Chen Y. A rat model for acute hepatic failure. Hepatobiliary Pancreat Dis Int 2003; 2: 423-425
58. Makino H, Togo S, Kubota T, Morioka D, Morita T, Kobayashi T, Tanaka K, Shimizu T, Matsuo K, Nagashima Y, Shimada H. A good model of hepatic failure after excessive hepatectomy in mice. J Surg Res 2005; 127: 171-176
59. Filipponi F, Fabbri LP, Marsili M, Falcini F, Benassai C, Nucera M, Romagnoli P. A new surgical model of acute liver failure in the pig: experimental procedure and analysis of liver injury. Eur Surg Res 1991; 23: 58-64
60. Morita T, Togo S, Kubota T, Kamimukai N, Nishizuka I, Kobayashi T, Ichikawa Y, Ishikawa T, Takahashi S, Matsuo K, Tomaru Y, Okazaki Y, Hayashizaki Y, Shimada H. Mechanism of postoperative liver failure after excessive hepatectomy investigated using a cDNA microarray. J Hepatobiliary Pancreat Surg 2002; 9: 352-359
61. Liu ZC, Chang TM. Transdifferentiation of bioencapsulated bone marrow cells into hepatocyte-like cells in the 90% hepatectomized rat model. Liver Transpl 2006; 12: 566-572
62. Gäbelein G, Nüssler AK, Morgott F, Ping Y, Nüssler N, Neuhaus P, Glanemann M. Intrasplenic or subperitoneal hepatocyte transplantation to increase survival after surgically induced hepatic failure? Eur Surg Res 2008; 41: 253-259
63. Aoki K, Mizumoto H, Nakazawa K, Funatsu K, Kajiwara T. Evaluation of a hybrid artificial liver module with liver lobule-like structure in rats with liver failure. Int J Artif Organs 2008; 31: 55-61
64. Eguchi S, Lilja H, Hewitt WR, Middleton Y, Demetriou AA, Rozga J. Loss and recovery of liver regeneration in rats with fulminant hepatic failure. J Surg Res 1997; 72: 112-122
65. Filipponi F, Boggi U, Meacci L, Burchielli S, Vistoli F, Bellini R, Prota C, Colizzi L, Kusmic C, Campani D, Gneri C, Trivella MG, Mosca F. A new technique for total hepatectomy in the pig for testing liver support devices. Surgery 1999; 125: 448-455
66. Sosef MN, van Gulik TM. Total hepatectomy model in pigs: revised method for vascular reconstruction using a rigid vascular prosthesis. Eur Surg Res 2004; 36: 8-12
67. Knubben K, Thiel C, Schenk M, Etspüler A, Schenk T, Morgalla MH, Königsrainer A. A new surgical model for hepatectomy in pigs. Eur Surg Res 2008; 40: 41-46
68. Ytrebø LM, Nedredal GI, Langbakk B, Revhaug A. An experimental large animal model for the assessment of bioartificial liver support systems in fulminant hepatic failure. Scand J Gastroenterol 2002; 37: 1077-1088
69. Nakazawa K, Ijima H, Fukuda J, Sakiyama R, Yamashita Y, Shimada M, Shirabe K, Tsujita E, Sugimachi K, Funatsu K. Development of a hybrid artificial liver using polyurethane foam/hepatocyte spheroid culture in a preclinical pig experiment. Int J Artif Organs 2002; 25: 51-60
70. Gao Y, Mu N, Xu XP, Wang Y. Porcine acute liver failure model established by two-phase surgery and treated with hollow fiber bioartificial liver support system. World J Gastroenterol 2005; 11: 5468-5474
71. Sen S, Rose C, Ytrebø LM, Davies NA, Nedredal GI, Drevland SS, Kjønnø M, Prinzen FW, Hodges SJ, Deutz NE, Williams R, Butterworth RF, Revhaug A, Jalan R. Effect of albumin dialysis on intracranial pressure increase in pigs with acute liver failure: a randomized study. Crit Care Med 2006; 34: 158-164
72. Ytrebø LM, Korvald C, Nedredal GI, Elvenes OP, Nielsen Grymyr OJ, Revhaug A. N-acetylcysteine increases cerebral perfusion pressure in pigs with fulminant hepatic failure. Crit Care Med 2001; 29: 1989-1995
73. Ryska M, Kieslichová E, Pantoflícek T, Ryska O, Zazula R, Skibová J, Hájek M. Devascularization surgical model of acute liver failure in minipigs. Eur Surg Res 2004; 36: 179-184
74. Rose C, Ytrebø LM, Davies NA, Sen S, Nedredal GI, Belanger M, Revhaug A, Jalan R. Association of reduced extracellular brain ammonia, lactate, and intracranial pressure in pigs with acute liver failure. Hepatology 2007; 46: 1883-1892
75. Ekse S, Clapp LH, Revhaug A, Ytrebø LM. Endothelium-derived hyperpolarization factor (EDHF) is up-regulated in a pig model of acute liver failure. Scand J Gastroenterol 2007; 42: 356-365
76. Totsuka O, Takeyoshi I, Tsutsumi H, Hashimoto N, Sunose Y, Tokumine M, Ohwada S, Matsumoto K, Morishita Y. The effects of a bradykinin B2 receptor antagonist in extended liver resection with ischemia in dogs. Hepatogastroenterology 2004; 51: 1771-1775
77. Chen Z, Ding YT. Functional evaluation of a new bioartificial liver system in vitro and in vitro. World J Gastroenterol 2006; 12: 1312-1316
78. Ladurner R, Hochleitner B, Schneeberger S, Barnas U, Krismer A, Kleinsasser A, Offner F, Königsrainer I, Margreiter R, Königsrainer A. Extended liver resection and hepatic ischemia in pigs: a new, potentially reversible model to induce acute liver failure and study artificial liver support systems. Eur Surg Res 2005; 37: 365-369
79. Frühauf NR, Oldhafer KJ, Westermann S, Sotiropoulos GC, Kaiser GM. Acute hepatic failure in swine: hepatectomy versus vascular occlusion. J Invest Surg 2004; 17: 163-171
80. Gunawan BK, Liu ZX, Han D, Hanawa N, Gaarde WA, Kaplowitz N. c-Jun N-terminal kinase plays a major role in murine acetaminophen hepatotoxicity. Gastroenterology 2006; 131: 165-178
81. Nakagawa H, Maeda S, Hikiba Y, Ohmae T, Shibata W, Yanai A, Sakamoto K, Ogura K, Noguchi T, Karin M, Ichijo H, Omata M. Deletion of apoptosis signal-regulating kinase 1 attenuates acetaminophen-induced liver injury by inhibiting c-Jun N-terminal kinase activation. Gastroenterology 2008; 135: 1311-1321
82. Henderson NC, Pollock KJ, Frew J, Mackinnon AC, Flavell RA, Davis RJ, Sethi T, Simpson KJ. Critical role of c-jun (NH2) terminal kinase in paracetamol- induced acute liver failure. Gut 2007; 56: 982-990
83. Gregus Z, Madhu C, Klaassen CD. Species variation in toxication and detoxication of acetaminophen in vivo: a comparative study of biliary and urinary excretion of acetaminophen metabolites. J Pharmacol Exp Ther 1988; 244: 91-99
84. Rahman TM, Selden AC, Hodgson HJ. A novel model of acetaminophen-induced acute hepatic failure in rabbits. J Surg Res 2002; 106: 264-272
85. Sakai H, Park SS, Kikkawa Y. Differential oxidase activity of hepatic and pulmonary microsomal cytochrome P-450 isozymes after treatment with cytochrome P-450 inducers. Biochem Biophys Res Commun 1992; 187: 1262-1269
86. Miller DJ, Hickman R, Fratter R, Terblanche J, Saunders SJ. An animal model of fulminant hepatic failure: a feasibility study. Gastroenterology 1976; 71: 109-113
87. Francavilla A, Makowka L, Polimeno L, Barone M, Demetris J, Prelich J, Van Thiel DH, Starzl TE. A dog model for acetaminophen-induced fulminant hepatic failure. Gastroenterology 1989; 96: 470-478
88. Doering CB, Parker ET, Nichols CE, Lollar P. Decreased factor VIII levels during acetaminophen-induced murine fulminant hepatic failure. Blood 2003; 102: 1743-1744
89. Nguyen TH, Mai G, Villiger P, Oberholzer J, Salmon P, Morel P, Bühler L, Trono D. Treatment of acetaminophen-induced acute liver failure in the mouse with conditionally immortalized human hepatocytes. J Hepatol 2005; 43: 1031-1037
90. Belardinelli MC, Pereira F, Baldo G, Vicente Tavares AM, Kieling CO, da Silveira TR, Meurer L, Soares Duarte ME, Giugliani R, Matte U. Adult derived mononuclear bone marrow cells improve survival in a model of acetaminophen-induced acute liver failure in rats. Toxicology 2008; 247: 1-5
91. Randle LE, Sathish JG, Kitteringham NR, Macdonald I, Williams DP, Park BK. alpha(1)-Adrenoceptor antagonists prevent paracetamol-induced hepatotoxicity in mice. Br J Pharmacol 2008; 153: 820-830
92. Blitzer BL, Waggoner JG, Jones EA, Gralnick HR, Towne D, Butler J, Weise V, Kopin IJ, Walters I, Teychenne PF, Goodman DG, Berk PD. A model of fulminant hepatic failure in the rabbit. Gastroenterology 1978; 74: 664-671
93. Horowitz ME, Schafer DF, Molnar P, Jones EA, Blasberg RG, Patlak CS, Waggoner J, Fenstermacher JD. Increased blood-brain transfer in a rabbit model of acute liver failure. Gastroenterology 1983; 84: 1003-1011
94. Keppler D, Lesch R, Reutter W, Decker K. Experimental hepatitis induced by D-galactosamine. Exp Mol Pathol 1968; 9: 279-290
95. Kalpana K, Ong HS, Soo KC, Tan SY, Prema Raj J. An improved model of galactosamine-induced fulminant hepatic failure in the pig. J Surg Res 1999; 82: 121-130
96. Anand R, Harry D, Holt S, Milner P, Dashwood M, Goodier D, Jarmulowicz M, Moore K. Endothelin is an important determinant of renal function in a rat model of acute liver and renal failure. Gut 2002; 50: 111-117
97. Arai K, Lee K, Berthiaume F, Tompkins RG, Yarmush ML. Intrahepatic amino acid and glucose metabolism in a D-galactosamine-induced rat liver failure model. Hepatology 2001; 34: 360-371
98. Galun E, Zeira E, Pappo O, Peters M, Rose-John S. Liver regeneration induced by a designer human IL-6/sIL-6R fusion protein reverses severe hepatocellular injury. FASEB J 2000; 14: 1979-1987
99. Cuesta E, Boada J, Calafell R, Perales JC, Roig T, Bermudez J. Fructose 1,6-bisphosphate prevented endotoxemia, macrophage activation, and liver injury induced by D-galactosamine in rats. Crit Care Med 2006; 34: 807-814
100. Ho DW, Yang ZF, Lau CK, Tam KH, To JY, Poon RT, Fan ST. Therapeutic potential of cardiotrophin 1 in fulminant hepatic failure: dual roles in antiapoptosis and cell repair. Arch Surg 2006; 141: 1077-1084; discussion 1084
101. Cauli O, Rodrigo R, Boix J, Piedrafita B, Agusti A, Felipo V. Acute liver failure-induced death of rats is delayed or prevented by blocking NMDA receptors in brain. Am J Physiol Gastrointest Liver Physiol 2008; 295: G503-G511
102. Hermenegildo C, Marcaida G, Montoliu C, Grisolía S, Miñana MD, Felipo V. NMDA receptor antagonists prevent acute ammonia toxicity in mice. Neurochem Res 1996; 21: 1237-1244
103. Kuwahata M, Tomoe Y, Harada N, Amano S, Segawa H, Tatsumi S, Ito M, Oka T, Miyamoto K. Characterization of the molecular mechanisms involved in the increased insulin secretion in rats with acute liver failure. Biochim Biophys Acta 2007; 1772: 60-65
104. Jauregui HO, Mullon CJ, Trenkler D, Naik S, Santangini H, Press P, Muller TE, Solomon BA. In vivo evaluation of a hollow fiber liver assist device. Hepatology 1995; 21: 460-469
105. Shinoda M, Tilles AW, Kobayashi N, Wakabayashi G, Takayanagi A, Totsugawa T, Harada H, Obara H, Suganuma K, Berthiaume F, Shimazu M, Shimizu N, Tanaka N, Kitajima M, Tompkins RG, Toner M, Yarmush ML. A bioartificial liver device secreting interleukin-1 receptor antagonist for the treatment of hepatic failure in rats. J Surg Res 2007; 137: 130-140
106. Yamamoto S, Steers JL, Wharen RE Jr, Eckman CB, Nguyen JH. Cerebrospinal fluid drainage and cranial decompression prolong survival in rats with fulminant hepatic failure. Transpl Int 2006; 19: 675-682
107. Namisaki T, Yoshiji H, Kojima H, Yoshii J, Ikenaka Y, Noguchi R, Sakurai S, Yanase K, Kitade M, Yamazaki M, Asada K, Uemura M, Nakamura M, Fukui H. Salvage effect of the vascular endothelial growth factor on chemically induced acute severe liver injury in rats. J Hepatol 2006; 44: 568-575
108. Kuhla A, Eipel C, Siebert N, Abshagen K, Menger MD, Vollmar B. Hepatocellular apoptosis is mediated by TNFalpha-dependent Fas/FasLigand cytotoxicity in a murine model of acute liver failure. Apoptosis 2008; 13: 1427-1438
109. Wen Y, Cui W, Liu P. Type I inositol 1, 4, 5-triphosphate receptors increase in kidney of mice with fulminant hepatic failure. World J Gastroenterol 2007; 13: 2344-2348
110. Pritchard MT, Roychowdhury S, McMullen MR, Guo L, Arteel GE, Nagy LE. Early growth response-1 contributes to galactosamine/ lipopolysaccharide-induced acute liver injury in mice. Am J Physiol Gastrointest Liver Physiol 2007; 293: G1124-G1133
111. Ma KF, Yang HY, Chen Z, Qi LY, Zhu DY, Lou YJ. Enhanced expressions and activations of leukotriene C4 synthesis enzymes in D-galactosamine/lipopolysaccharide-induced rat fulminant hepatic failure model. World J Gastroenterol 2008; 14: 2748-2756
112. Feng B, Wu S, Lv S, Liu F, Chen H, Yan X, Li Y, Dong F, Wei L. Metabolic profiling analysis of a D-galactosamine/ lipopolysaccharide-induced mouse model of fulminant hepatic failure. J Proteome Res 2007; 6: 2161-2167
113. Takamura M, Matsuda Y, Yamagiwa S, Tamura Y, Honda Y, Suzuki K, Ichida T, Aoyagi Y. An inhibitor of c-Jun NH2-terminal kinase, SP600125, protects mice from D-galactosamine/lipopolysaccharide-induced hepatic failure by modulating BH3-only proteins. Life Sci 2007; 80: 1335-1344
114. Le Minh K, Kuhla A, Abshagen K, Minor T, Stegemann J, Ibrahim S, Eipel C, Vollmar B. Uncoupling protein-2 deficiency provides protection in a murine model of endotoxemic acute liver failure. Crit Care Med 2009; 37: 215-222
115. Shi Z, Wakil AE, Rockey DC. Strain-specific differences in mouse hepatic wound healing are mediated by divergent T helper cytokine responses. Proc Natl Acad Sci USA 1997; 94: 10663-10668
116. Brattin WJ, Glende EA Jr, Recknagel RO. Pathological mechanisms in carbon tetrachloride hepatotoxicity. J Free Radic Biol Med 1985; 1: 27-38
117. Clawson GA. Mechanisms of carbon tetrachloride hepatotoxicity. Pathol Immunopathol Res 1989; 8: 104-112
118. Hickman R, Alp MH. A predictable pathophysiological model of porcine hepatic failure. Eur Surg Res 1986; 18: 283-292
119. Taniguchi M, Takeuchi T, Nakatsuka R, Watanabe T, Sato K. Molecular process in acute liver injury and regeneration induced by carbon tetrachloride. Life Sci 2004; 75: 1539-1549
120. Weber LW, Boll M, Stampfl A. Hepatotoxicity and mechanism of action of haloalkanes: carbon tetrachloride as a toxicological model. Crit Rev Toxicol 2003; 33: 105-136
121. López-Diazguerrero NE, Luna-López A, Gutiérrez-Ruiz MC, Zentella A, Königsberg M. Susceptibility of DNA to oxidative stressors in young and aging mice. Life Sci 2005; 77: 2840-2854
122. Kobayashi N, Ito M, Nakamura J, Cai J, Hammel JM, Fox IJ. Treatment of carbon tetrachloride and phenobarbital-induced chronic liver failure with intrasplenic hepatocyte transplantation. Cell Transplant 2000; 9: 671-673
123. Mikami K, Goto T, Miura K, Ohshima S, Yoneyama K, Lin JG, Watanabe D, Segawa D, Kataoka E, Shibuya T, Watanabe S. Gabexate mesilate, a synthetic protease inhibitor, attenuates carbon tetrachloride-induced liver injury in rats. J Gastroenterol 2005; 40: 260-265
124. Hayashi S, Itoh A, Isoda K, Kondoh M, Kawase M, Yagi K. Fucoidan partly prevents CCl4-induced liver fibrosis. Eur J Pharmacol 2008; 580: 380-384
125. Yen FL, Wu TH, Lin LT, Cham TM, Lin CC. Naringenin-loaded nanoparticles improve the physicochemical properties and the hepatoprotective effects of naringenin in orally-administered rats with CCl(4)-induced acute liver failure. Pharm Res 2009; 26: 893-902
126. Caraceni P, Giannone F, Catani L, Talarico S, Pertosa AM, Domenicali M, Fogli M, Principe A, Trevisani F, Baccarani M, Bernardi M, Lemoli RM. Effects of granulocyte colony stimulating-factor in a rat model of acute liver injury. Dig Liver Dis 2007; 39: 943-951
127. Chieli E, Malvaldi G. Role of the microsomal FAD-containing monooxygenase in the liver toxicity of thioacetamide S-oxide. Toxicology 1984; 31: 41-52
128. Pallottini V, Martini C, Bassi AM, Romano P, Nanni G, Trentalance A. Rat HMGCoA reductase activation in thioacetamide-induced liver injury is related to an increased reactive oxygen species content. J Hepatol 2006; 44: 368-374
129. Shapiro H, Ashkenazi M, Weizman N, Shahmurov M, Aeed H, Bruck R. Curcumin ameliorates acute thioacetamide-induced hepatotoxicity. J Gastroenterol Hepatol 2006; 21: 358-366
130. Margeli AP, Papadimitriou L, Ninos S, Manolis E, Mykoniatis MG, Theocharis SE. Hepatic stimulator substance administration ameliorates liver regeneration in an animal model of fulminant hepatic failure and encephalopathy. Liver Int 2003; 23: 171-178
131. Chu CJ, Hsiao CC, Wang TF, Chan CY, Lee FY, Chang FY, Chen YC, Huang HC, Wang SS, Lee SD. Prostacyclin inhibition by indomethacin aggravates hepatic damage and encephalopathy in rats with thioacetamide-induced fulminant hepatic failure. World J Gastroenterol 2005; 11: 232-236
132. Avraham Y, Zolotarev O, Grigoriadis NC, Poutahidis T, Magen I, Vorobiav L, Zimmer A, Ilan Y, Mechoulam R, Berry EM. Cannabinoids and capsaicin improve liver function following thioacetamide-induced acute injury in mice. Am J Gastroenterol 2008; 103: 3047-3056
133. Harputuoglu MM, Demirel U, Ciralik H, Temel I, Firat S, Ara C, Aladag M, Karincaoglu M, Hilmioglu F. Protective effects of Gingko biloba on thioacetamide-induced fulminant hepatic failure in rats. Hum Exp Toxicol 2006; 25: 705-713
134. Huang HC, Wang SS, Lee FY, Chan CY, Chang FY, Lin HC, Chu CJ, Chen YC, Lee SD. Simvastatin for rats with thioacetamide-induced liver failure and encephalopathy. J Gastroenterol Hepatol 2008; 23: e236-e242
135. Chu CJ, Chang CC, Wang TF, Lee FY, Chang FY, Chen YC, Chan CC, Huang HC, Wang SS, Lee SD. Detrimental effects of nitric oxide inhibition on hepatic encephalopathy in rats with thioacetamide-induced fulminant hepatic failure: role of nitric oxide synthase isoforms. J Gastroenterol Hepatol 2006; 21: 1194-1199
136. Matkowskyj KA, Marrero JA, Carroll RE, Danilkovich AV, Green RM, Benya RV. Azoxymethane-induced fulminant hepatic failure in C57BL/6J mice: characterization of a new animal model. Am J Physiol 1999; 277: G455-G462
137. Bélanger M, Côté J, Butterworth RF. Neurobiological characterization of an azoxymethane mouse model of acute liver failure. Neurochem Int 2006; 48: 434-440
138. Shimojima N, Eckman CB, McKinney M, Sevlever D, Yamamoto S, Lin W, Dickson DW, Nguyen JH. Altered expression of zonula occludens-2 precedes increased blood-brain barrier permeability in a murine model of fulminant hepatic failure. J Invest Surg 2008; 21: 101-108
139. Mizuhara H, O'Neill E, Seki N, Ogawa T, Kusunoki C, Otsuka K, Satoh S, Niwa M, Senoh H, Fujiwara H. T cell activation-associated hepatic injury: mediation by tumor necrosis factors and protection by interleukin 6. J Exp Med 1994; 179: 1529-1537
140. Lazarus DD, Kambayashi T, Yato-Kioka M, Baumann H, Jacob CO, Strassmann G. Vesnarinone inhibits immune-mediated but not Fas (CD95) agonist-mediated hepatic injury. Int J Immunopharmacol 1997; 19: 49-58
141. Torisu T, Nakaya M, Watanabe S, Hashimoto M, Yoshida H, Chinen T, Yoshida R, Okamoto F, Hanada T, Torisu K, Takaesu G, Kobayashi T, Yasukawa H, Yoshimura A. Suppressor of cytokine signaling 1 protects mice against concanavalin A-induced hepatitis by inhibiting apoptosis. Hepatology 2008; 47: 1644-1654
142. Wolf AM, Wolf D, Avila MA, Moschen AR, Berasain C, Enrich B, Rumpold H, Tilg H. Up-regulation of the anti-inflammatory adipokine adiponectin in acute liver failure in mice. J Hepatol 2006; 44: 537-543
143. Saito Y, Kon S, Fujiwara Y, Nakayama Y, Kurotaki D, Fukuda N, Kimura C, Kanayama M, Ito K, Diao H, Matsui Y, Komatsu Y, Ohtsuka E, Uede T. Osteopontin small interfering RNA protects mice from fulminant hepatitis. Hum Gene Ther 2007; 18: 1205-1214
144. Takada Y, Ishiguro S, Fukunaga K. Large-animal models of fulminant hepatic failure. J Artif Organs 2003; 6: 9-13
145. Ishiguro S, Takada Y, Gu M, Fukunaga K, Taniguchi H, Seino K, Kawamoto T, Yuzawa K, Otsuka M, Todoroki T, Fukao K. Auxiliary partial orthotopic liver transplantation for fulminant hepatitis: regeneration of the diseased native liver in a pig model. Transplantation 2003; 75: 1901-1904
146. Nakayama Y, Shimizu Y, Hirano K, Ebata K, Minemura M, Watanabe A, Sugiyama T. CTLA-4Ig suppresses liver injury by inhibiting acquired immune responses in a mouse model of fulminant hepatitis. Hepatology 2005; 42: 915-924
147. Ishizawa Y, Totsuka E, Umehara M, Nishimura A, Ono H, Sasaki M. Efficacy of double-filtration plasmapheretic cross-circulation with a high-permeability membrane using canine harvested liver in porcine fulminant hepatic failure model. Transplant Proc 2004; 36: 2344-2348
148. Schmitz V, Dombrowski F, Prieto J, Qian C, Diehl L, Knolle P, Sauerbruch T, Caselmann WH, Spengler U, Leifeld L. Induction of murine liver damage by overexpression of CD40 ligand provides an experimental model to study fulminant hepatic failure. Hepatology 2006; 44: 430-439
149. Skawran S, Palmes D, Budny T, Bahde R, Stratmann U, Spiegel HU. Development and evaluation of an experimental model for investigating the pathogenesis and therapeutic strategies of acute liver failure. Transplant Proc 2003; 35: 3142-3146
150. Yuasa T, Yamamoto T, Rivas-Carrillo JD, Chen Y, Navarro-Alvarez N, Soto-Guiterrez A, Noguchi H, Matsumoto S, Tanaka N, Kobayashi N. Laparoscopy-assisted creation of a liver failure model in pigs. Cell Transplant 2008; 17: 187-193
151. Ando K, Moriyama T, Guidotti LG, Wirth S, Schreiber RD, Schlicht HJ, Huang SN, Chisari FV. Mechanisms of class I restricted immunopathology. A transgenic mouse model of fulminant hepatitis. J Exp Med 1993; 178: 1541-1554
152. Ding JW, Ning Q, Liu MF, Lai A, Leibowitz J, Peltekian KM, Cole EH, Fung LS, Holloway C, Marsden PA, Yeger H, Phillips MJ, Levy GA. Fulminant hepatic failure in murine hepatitis virus strain 3 infection: tissue-specific expression of a novel fgl2 prothrombinase. J Virol 1997; 71: 9223-9230
153. Tunon MJ, Sanchez-Campos S, Garcia-Ferreras J, Alvarez M, Jorquera F, Gonzalez-Gallego J. Rabbit hemorrhagic viral disease: characterization of a new animal model of fulminant liver failure. J Lab Clin Med 2003; 141: 272-278
154. Liu SJ, Xue HP, Pu BQ, Quian NH. A new viral disease in rabbits. An Hus Vet Med (Xumu yu Shouyi) 16: 253-255
155. Mikami O, Park JH, Kimura T, Ochiai K, Itakura C. Hepatic lesions in young rabbits experimentally infected with rabbit haemorrhagic disease virus. Res Vet Sci 1999; 66: 237-242
156. Gould AR, Kattenbelt JA, Lenghaus C, Morrissy C, Chamberlain T, Collins BJ, Westbury HA. The complete nucleotide sequence of rabbit haemorrhagic disease virus (Czech strain V351): use of the polymerase chain reaction to detect replication in Australian vertebrates and analysis of viral population sequence variation. Virus Res 1997; 47: 7-17
157. Prieto JM, Fernandez F, Alvarez V, Espi A, García Marín JF, Alvarez M, Martín JM, Parra F. Immunohistochemical localisation of rabbit haemorrhagic disease virus VP-60 antigen in early infection of young and adult rabbits. Res Vet Sci 2000; 68: 181-187
158. Alonso C, Oviedo JM, Martín-Alonso JM, Díaz E, Boga JA, Parra F. Programmed cell death in the pathogenesis of rabbit hemorrhagic disease. Arch Virol 1998; 143: 321-332
159. San-Miguel B, Alvarez M, Culebras JM, González-Gallego J, Tuñón MJ. N-acetyl-cysteine protects liver from apoptotic death in an animal model of fulminant hepatic failure. Apoptosis 2006; 11: 1945-1957
160. Muto Y, Nouri-Aria KT, Meager A, Alexander GJ, Eddleston AL, Williams R. Enhanced tumour necrosis factor and interleukin-1 in fulminant hepatic failure. Lancet 1988; 2: 72-74
161. Sánchez-Campos S, Alvarez M, Culebras JM, Gonzalez-Gallego J, Tuñón MJ. Pathogenic molecular mechanisms in an animal model of fulminant hepatic failure: rabbit hemorrhagic viral disease. J Lab Clin Med 2004; 144: 215-222
162. Webber EM, Bruix J, Pierce RH, Fausto N. Tumor necrosis factor primes hepatocytes for DNA replication in the rat. Hepatology 1998; 28: 1226-1234
163. Fausto N. Liver regeneration. J Hepatol 2000; 32: 19-31