About this Journal Submit a Manuscript Table of Contents
BioMed Research International
Volume 2013 (2013), Article ID 192029, 12 pages
http://dx.doi.org/10.1155/2013/192029
Review Article

The Impact of Hepatic Steatosis on Hepatic Ischemia-Reperfusion Injury in Experimental Studies: A Systematic Review

1Department of Surgery, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand
2Maurice Wilkins Centre for Biodiscovery, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand
3School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand
4New Zealand Liver Transplant Unit, Auckland City Hospital, Private Bag 92024, Auckland 1023, New Zealand

Received 8 April 2013; Accepted 23 July 2013

Academic Editor: Mohamed Tarek Shata

Copyright © 2013 Michael J. J. Chu et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. Angulo, “Nonalcoholic fatty liver disease and liver transplantation,” Liver Transplantation, vol. 12, no. 4, pp. 525–534, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. K. E. Underwood Ground, “Prevalence of fatty liver in healthy male adults accidently killed,” Aviation Space and Environmental Medicine, vol. 55, no. 1, pp. 59–61, 1984. View at Scopus
  3. M. Hilden, P. Christoffersen, E. Juhl, and J. B. Dalgaard, “Liver histology in a ‘normal’ population—examinations of 503 consecutive fatal traffic casualties,” Scandinavian Journal of Gastroenterology, vol. 12, no. 5, pp. 593–597, 1977. View at Scopus
  4. A. Nocito, A. M. El-Badry, and P.-A. Clavien, “When is steatosis too much for transplantation?” Journal of Hepatology, vol. 45, no. 4, pp. 494–499, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. G. Hu, J. Lindström, P. Jousilahti et al., “The increasing prevalence of metabolic syndrome among Finnish men and women over a decade,” Journal of Clinical Endocrinology & Metabolism, vol. 93, no. 3, pp. 832–836, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. E. S. Ford, W. H. Giles, and A. H. Mokdad, “Increasing prevalence of the metabolic syndrome among U. S. adults,” Diabetes Care, vol. 27, no. 10, pp. 2444–2449, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. R. J. Ploeg, A. M. D'Alessandro, S. J. Knechtle et al., “Risk factors for primary dysfunction after liver transplantation—a multivariate analysis,” Transplantation, vol. 55, no. 4, pp. 807–813, 1993. View at Scopus
  8. K. E. Behrns, G. G. Tsiotos, N. F. DeSouza, M. K. Krishna, J. Ludwig, and D. M. Nagorney, “Hepatic steatosis as a potential risk factor for major hepatic resection,” Journal of Gastrointestinal Surgery, vol. 2, no. 3, pp. 292–298, 1998. View at Scopus
  9. R. Adam, M. Reynes, M. Johann et al., “The outcome of steatotic grafts in liver transplantation,” Transplantation Proceedings, vol. 23, no. 1, part 2, pp. 1538–1540, 1991. View at Scopus
  10. S. Todo, A. J. Demetris, L. Makowka et al., “Primary nonfunction of hepatic allografts with preexisting fatty infiltration,” Transplantation, vol. 47, no. 5, pp. 903–905, 1989. View at Scopus
  11. J. Belghiti, K. Hiramatsu, S. Benoist, P. P. Massault, A. Sauvanet, and O. Farges, “Seven hundred forty-seven hepatectomies in the 1990s: an update to evaluate the actual risk of liver resection,” Journal of the American College of Surgeons, vol. 191, no. 1, pp. 38–46, 2000. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Selzner and P. A. Clavien, “Fatty liver in liver transplantation and surgery,” Seminars in Liver Disease, vol. 21, no. 1, pp. 105–113, 2001. View at Publisher · View at Google Scholar · View at Scopus
  13. A. M. D'Alessandro, M. Kalayoglu, H. W. Sollinger et al., “The predictive value of donor liver biopsies for the development of primary nonfunction after orthotopic liver transplantation,” Transplantation, vol. 51, no. 1, pp. 157–163, 1991. View at Scopus
  14. P. A. Clavien, P. R. C. Harvey, and S. M. Strasberg, “Preservation and reperfusion injuries in liver allografts. An overview and synthesis of current studies,” Transplantation, vol. 53, no. 5, pp. 957–978, 1992. View at Scopus
  15. C. Fondevila, R. W. Busuttil, and J. W. Kupiec-Weglinski, “Hepatic ischemia/reperfusion injury—a fresh look,” Experimental and Molecular Pathology, vol. 74, no. 2, pp. 86–93, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. H. Jaeschke, “Mechanisms of reperfusion injury after warm ischemia of the liver,” Journal of Hepato-Biliary-Pancreatic Surgery, vol. 5, no. 4, pp. 402–408, 1998. View at Scopus
  17. A. M. Seifalian, V. Chidambaram, K. Rolles, and B. R. Davidson, “In vivo demonstration of impaired microcirculation in steatotic human liver grafts,” Liver Transplantation and Surgery, vol. 4, no. 1, pp. 71–77, 1998. View at Scopus
  18. K. Teramoto, J. L. Bowers, J. B. Kruskal, and M. E. Clouse, “Hepatic microcirculatory changes after reperfusion in fatty and normal liver transplantation in the rat,” Transplantation, vol. 56, no. 5, pp. 1076–1082, 1993. View at Scopus
  19. T. Fukumori, N. Ohkohchi, S. Tsukamoto, and S. Satomi, “Why is fatty liver unsuitable for transplantation? Deterioration of mitochondrial ATP synthesis and sinusoidal structure during cold preservation of a liver with steatosis,” Transplantation Proceedings, vol. 29, no. 1-2, pp. 412–415, 1997. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Ijaz, W. Yang, M. C. Winslet, and A. M. Seifalian, “Impairment of hepatic microcirculation in fatty liver,” Microcirculation, vol. 10, no. 6, pp. 447–456, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. G. C. Farrell, N. C. Teoh, and R. S. McCuskey, “Hepatic microcirculation in fatty liver disease,” Anatomical Record, vol. 291, no. 6, pp. 684–692, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. D. Acosta and D. G. Wenzel, “Injury produced by free fatty acids to lysosomes and mitochondria in cultured heart muscle and endothelial cells,” Atherosclerosis, vol. 20, no. 3, pp. 417–426, 1974. View at Scopus
  23. M. Trauner, M. Arrese, and M. Wagner, “Fatty liver and lipotoxicity,” Biochimica et Biophysica Acta, vol. 1801, no. 3, pp. 299–310, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. S. C. Hand and M. A. Menze, “Mitochondria in energy-limited states: mechanisms that blunt the signaling of cell death,” The Journal of Experimental Biology, vol. 211, part 12, pp. 1829–1840, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. Z. Zhong, H. Connor, R. F. Stachlewitz et al., “Role of free radicals in primary nonfunction of marginal fatty grafts from rats treated acutely with ethanol,” Molecular Pharmacology, vol. 52, no. 5, pp. 912–919, 1997. View at Scopus
  26. E. M. Brunt and D. G. Tiniakos, “Histopathology of nonalcoholic fatty liver disease,” World Journal of Gastroenterology, vol. 16, no. 42, pp. 5286–5296, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Varela-Rey, N. Embade, U. Ariz, S. C. Lu, J. M. Mato, and M. L. Martínez-Chantar, “Non-alcoholic steatohepatitis and animal models: understanding the human disease,” The International Journal of Biochemistry & Cell Biology, vol. 41, no. 5, pp. 969–976, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. C. Z. Larter and M. M. Yeh, “Animal models of NASH: getting both pathology and metabolic context right,” Journal of Gastroenterology and Hepatology, vol. 23, no. 11, pp. 1635–1648, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. J. D. Ellett, Z. P. Evans, C. Atkinson, M. G. Schmidt, R. G. Schnellmann, and K. D. Chavin, “Toll-like receptor 4 is a key mediator of murine steatotic liver warm ischemia/reperfusion injury,” Liver Transplantation, vol. 15, no. 9, pp. 1101–1109, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. K. Yamagami, Y. Yamamoto, M. Kume et al., “Heat shock preconditioning ameliorates liver injury following normothermic ischemia-reperfusion in steatotic rat livers,” Journal of Surgical Research, vol. 79, no. 1, pp. 47–53, 1998. View at Publisher · View at Google Scholar · View at Scopus
  31. S. He, C. Atkinson, Z. Evans et al., “A role for complement in the enhanced susceptibility of steatotic livers to ischemia and reperfusion injury,” The Journal of Immunology, vol. 183, no. 7, pp. 4764–4772, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. P. Caraceni, M. Domenicali, G. Vendemiale et al., “The reduced tolerance of rat fatty liver to ischemia reperfusion is associated with mitochondrial oxidative injury,” Journal of Surgical Research, vol. 124, no. 2, pp. 160–168, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. N. Selzner, M. Selzner, W. Jochum, B. Amann-Vesti, R. Graf, and P.-A. Clavien, “Mouse livers with macrosteatosis are more susceptible to normothermic ischemic injury than those with microsteatosis,” Journal of Hepatology, vol. 44, no. 4, pp. 694–701, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. P. Caraceni, B. Nardo, M. Domenicali et al., “Ischemia-reperfusion injury in rat fatty liver: role of nutritional status,” Hepatology, vol. 29, no. 4, pp. 1139–1146, 1999. View at Scopus
  35. K. Hakamada, M. Sasaki, K. Takahashi, Y. Umehara, and M. Konn, “Sinusoidal flow block after warm ischemia in rats with diet-induced fatty liver,” Journal of Surgical Research, vol. 70, no. 1, pp. 12–20, 1997. View at Publisher · View at Google Scholar · View at Scopus
  36. A. M. Hui, S. Kawasaki, M. Makuuchi, J. Nakayama, T. Ikegami, and S. Miyagawa, “Liver injury following normothermic ischemia in steatotic rat liver,” Hepatology, vol. 20, no. 5, pp. 1287–1293, 1994. View at Publisher · View at Google Scholar · View at Scopus
  37. K. Takahashi, K. Hakamada, E. Totsuka, Y. Umehara, and M. Sasaki, “Warm ischemia and reperfusion injury in diet-induced canine fatty livers,” Transplantation, vol. 69, no. 10, pp. 2028–2034, 2000. View at Scopus
  38. S. Yamada, T. Tomiya, Y. Yamaguchi, M. Hiura, and M. Otsuki, “Activation of hepatic macrophage contributes to hepatic necrosis after post-ischemic reperfusion in alcoholic fatty liver,” Hepatology Research, vol. 26, no. 3, pp. 209–216, 2003. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Yamada, T. Iida, T. Tabata et al., “Alcoholic fatty liver differentially induces a neutrophil-chemokine and hepatic necrosis after ischemia-reperfusion in rat,” Hepatology, vol. 32, no. 2, pp. 278–288, 2000. View at Scopus
  40. H. A. Marsman, M. Heger, J. J. Kloek, S. L. Nienhuis, F. J. W. ten Kate, and T. M. van Gulik, “Omega-3 fatty acids reduce hepatic steatosis and consequently attenuate ischemia-reperfusion injury following partial hepatectomy in rats,” Digestive and Liver Disease, vol. 43, no. 12, pp. 984–990, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. W. Andraus, G. F. P. de Souza, M. G. de Oliveira et al., “S-nitroso-N-acetylcysteine ameliorates ischemia-reperfusion injury in the steatotic liver,” Clinics, vol. 65, no. 7, pp. 715–721, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. X.-Y. Luo, T. Takahara, J. Hou et al., “Theaflavin attenuates ischemia-reperfusion injury in a mouse fatty liver model,” Biochemical and Biophysical Research Communications, vol. 417, no. 1, pp. 287–293, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. M. Domenicali, G. Vendemiale, G. Serviddio et al., “Oxidative injury in rat fatty liver exposed to ischemia-reperfusion is modulated by nutritional status,” Digestive and Liver Disease, vol. 37, no. 9, pp. 689–697, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. R. S. Koti, W. Yang, G. Glantzounis, A. Quaglia, B. R. Davidson, and A. M. Seifalian, “Effect of ischaemic preconditioning on hepatic oxygenation, microcirculation and function in a rat model of moderate hepatic steatosis,” Clinical Science, vol. 108, no. 1, pp. 55–63, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. G. Fusai, G. K. Glantzounis, T. Hafez et al., “N-acetylcysteine ameliorates the late phase of liver ischaemia/reperfusion injury in the rabbit with hepatic steatosis,” Clinical Science, vol. 109, no. 5, pp. 465–473, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. T. S. Hafez, G. K. Glantzounis, G. Fusai et al., “Intracellular oxygenation and cytochrome oxidase C activity in ischemic preconditioning of steatotic rabbit liver,” American Journal of Surgery, vol. 200, no. 4, pp. 507–518, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. A. P. Rolo, J. S. Teodoro, C. Peralta, J. Rosello-Catafau, and C. M. Palmeira, “Prevention of I/R injury in fatty livers by ischemic preconditioning is associated with increased mitochondrial tolerance: the key role of ATPsynthase and mitochondrial permeability transition,” Transplant International, vol. 22, no. 11, pp. 1081–1090, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. H. Astarcioglu, S. Karademir, K. Atila et al., “The effects of vascular bed expansion in steatotic rat liver graft viability,” Transplant International, vol. 17, no. 4, pp. 188–194, 2004. View at Scopus
  49. M. Hayashi, Y. Tokunaga, T. Fujita, K. Tanaka, Y. Yamaoka, and K. Ozawa, “The effects of cold preservation on steatotic graft viability in rat liver transplantation,” Transplantation, vol. 56, no. 2, pp. 282–287, 1993. View at Scopus
  50. Y. F. Cheng, C. L. Chen, C.-Y. Lai et al., “Assessment of donor fatty livers for liver transplantation,” Transplantation, vol. 71, no. 9, pp. 1221–1225, 2001. View at Scopus
  51. M. Schmeding, S. Rademacher, S. Boas-Knoop et al., “RHuEPo reduces ischemia-reperfusion injury and improves survival after transplantation of fatty livers in rats,” Transplantation, vol. 89, no. 2, pp. 161–168, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. F. Berthiaume, L. Barbe, Y. Mokuno, A. D. MacDonald, R. Jindal, and M. L. Yarmush, “Steatosis reversibly increases hepatocyte sensitivity to hypoxia-reoxygenation injury,” Journal of Surgical Research, vol. 152, no. 1, pp. 54–60, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. D. Morioka, T. Kubota, H. Sekido et al., “Prostaglandin E1 improved the function of transplanter fatty liver in a rat reduced-size-liver transplantation model under conditions of permissible cold preservation,” Liver Transplantation, vol. 9, no. 1, pp. 79–86, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. M. von Heesen, K. Seibert, M. Hlser et al., “Multidrug donor preconditioning protects steatotic liver grafts against ischemia-reperfusion injury,” American Journal of Surgery, vol. 203, no. 2, pp. 168–176, 2012. View at Publisher · View at Google Scholar · View at Scopus
  55. E. S. Baskin-Bey, A. Canbay, S. F. Bronk et al., “Cathepsin B inactivation attenuates hepatocyte apoptosis and liver damage in steatotic livers after cold ischemia-warm reperfusion injury,” American Journal of Physiology, vol. 288, no. 2, pp. G396–G402, 2005. View at Publisher · View at Google Scholar · View at Scopus
  56. I. Arnault, Y.-M. Bao, M. Sebagh et al., “Beneficial effect of pentoxifylline on microvesicular steatotic livers submitted to a prolonged cold ischemia,” Transplantation, vol. 76, no. 1, pp. 77–83, 2003. View at Scopus
  57. R. W. Jamieson, M. Zilvetti, D. Roy et al., “Hepatic steatosis and normothermic perfusion-preliminary experiments in a porcine model,” Transplantation, vol. 92, no. 3, pp. 289–295, 2011. View at Publisher · View at Google Scholar · View at Scopus
  58. P. Caraceni, M. Domenicali, A. M. Pertosa et al., “The nutritional status modulates preservation-reperfusion injury in rat fatty liver,” Journal of Surgical Research, vol. 127, no. 2, pp. 190–196, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. P. Caraceni, C. Bianchi, M. Domenicali et al., “Impairment of mitochondrial oxidative phosphorylation in rat fatty liver exposed to preservation-reperfusion injury,” Journal of Hepatology, vol. 41, no. 1, pp. 82–88, 2004. View at Publisher · View at Google Scholar · View at Scopus
  60. U. Puetz, R. H. Tolba, S. Akbar, F. Dombrowski, and T. Minor, “Effects of L-carnitine-hydrochloride in the cold ischemic preservation of fatty liver grafts,” Transplantation Proceedings, vol. 33, no. 4, pp. 2523–2524, 2001. View at Publisher · View at Google Scholar · View at Scopus
  61. T. Minor, S. Akbar, R. Tolba, and F. Dombrowski, “Cold preservation of fatty liver grafts: prevention of functional and ultrastructural impairments by venous oxygen persufflation,” Journal of Hepatology, vol. 32, no. 1, pp. 105–111, 2000. View at Scopus
  62. N. Selzner, M. Selzner, W. Jochum, B. Amann-Vesti, R. Graf, and P.-A. Clavien, “Mouse livers with macrosteatosis are more susceptible to normothermic ischemic injury than those with microsteatosis,” Journal of Hepatology, vol. 44, no. 4, pp. 694–701, 2006. View at Publisher · View at Google Scholar · View at Scopus
  63. J. H. Pringle, “Notes on the arrest of hepatic hemorrhage due to trauma,” Annals of Surgery, vol. 48, no. 4, pp. 541–549, 1908. View at Publisher · View at Google Scholar
  64. M. Selzner, C. A. Camargo, and P.-A. Clavien, “Ischemia impairs liver regeneration after major tissue loss in rodents: protective effects of interleukin-6,” Hepatology, vol. 30, no. 2, pp. 469–475, 1999. View at Publisher · View at Google Scholar · View at Scopus
  65. R. W. Busuttil and K. Tanaka, “The utility of marginal donors in liver transplantation,” Liver Transplantation, vol. 9, no. 7, pp. 651–663, 2003. View at Publisher · View at Google Scholar · View at Scopus
  66. G. C. Farrell and C. Z. Larter, “Nonalcoholic fatty liver disease: from steatosis to cirrhosis,” Hepatology, vol. 43, no. 2, supplement 1, pp. S99–S112, 2006. View at Publisher · View at Google Scholar · View at Scopus
  67. L. Hebbard and J. George, “Animal models of nonalcoholic fatty liver disease,” Nature Reviews Gastroenterology and Hepatology, vol. 8, no. 1, pp. 35–44, 2011. View at Publisher · View at Google Scholar · View at Scopus
  68. A. M. El-Badry, S. Breitenstein, W. Jochum et al., “Assessment of hepatic steatosis by expert pathologists: the end of a gold standard,” Annals of Surgery, vol. 250, no. 5, pp. 691–697, 2009. View at Publisher · View at Google Scholar · View at Scopus
  69. R. Veteläinen, A. K. van Vliet, and T. M. van Gulik, “Severe steatosis increases hepatocellular injury and impairs liver regeneration in a rat model of partial hepatectomy,” Annals of Surgery, vol. 245, no. 1, pp. 44–50, 2007. View at Publisher · View at Google Scholar · View at Scopus
  70. T. M. Fishbein, M. I. Fiel, S. Emre et al., “Use of livers with microvesicular fat safely expands the donor pool,” Transplantation, vol. 64, no. 2, pp. 248–251, 1997. View at Publisher · View at Google Scholar · View at Scopus
  71. M. A. G. Ureña, F. C. Ruiz-Delgado, E. M. González et al., “Assessing risk of the use of livers with macro and microsteatosis in a liver transplant program,” Transplantation Proceedings, vol. 30, no. 7, pp. 3288–3291, 1998. View at Publisher · View at Google Scholar · View at Scopus
  72. L. Llacuna, A. Fernández, C. V. Montfort et al., “Targeting cholesterol at different levels in the mevalonate pathway protects fatty liver against ischemia-reperfusion injury,” Journal of Hepatology, vol. 54, no. 5, pp. 1002–1010, 2011. View at Publisher · View at Google Scholar · View at Scopus
  73. M. Bessems, R. Tolba, B. M. Doorschodt, et al., “The isolated perfused rat liver: standardization of a time-honoured model,” Laboratory Animals, vol. 40, no. 3, pp. 236–246, 2006. View at Publisher · View at Google Scholar · View at Scopus
  74. S. Feng, N. P. Goodrich, J. L. Bragg-Gresham et al., “Characteristics associated with liver graft failure: the concept of a donor risk index,” American Journal of Transplantation, vol. 6, no. 4, pp. 783–790, 2006. View at Publisher · View at Google Scholar · View at Scopus
  75. T. Kubota, K. Takabe, M. Yang, et al., “Minimum sizes for remnant and transplanted livers in rats,” Journal of Hepato-Biliary-Pancreatic Surgery, vol. 4, no. 4, pp. 398–404, 1997. View at Scopus
  76. A. L. Spitzer, O. B. Lao, A. A. S. Dick et al., “The biopsied donor liver: incorporating macrosteatosis into high-risk donor assessment,” Liver Transplantation, vol. 16, no. 7, pp. 874–884, 2010. View at Publisher · View at Google Scholar · View at Scopus
  77. F. Dahm, P. Georgiev, and P.-A. Clavien, “Small-for-size syndrome after partial liver transplantation: definition, mechanisms of disease and clinical implications,” American Journal of Transplantation, vol. 5, no. 11, pp. 2605–2610, 2005. View at Publisher · View at Google Scholar · View at Scopus