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Oxidative Medicine and Cellular Longevity
Volume 2014 (2014), Article ID 906965, 13 pages
http://dx.doi.org/10.1155/2014/906965
Review Article

Global Consequences of Liver Ischemia/Reperfusion Injury

1Second Department of Surgery, School of Medicine, Aretaieion University Hospital, University of Athens, 76 Vassilisis Sofia’s Avenue, 11528 Athens, Greece
2Second Department of Anesthesiology, School of Medicine, Attikon University Hospital, University of Athens, 1 Rimini Street, 12462 Athens, Greece
3Division of Surgery & Interventional Sciences, Royal Free Hospital Campus, University College London, 8 South Pond Street, Hampstead, London NW3 2QG, UK
4First Department of Anesthesiology, Aretaieion Hospital, University of Athens School of Medicine, Vassilissis Sofias 76, 11528 Athens, Greece
5Fourth Department of Surgery, School of Medicine, Attikon University Hospital, University of Athens, 1 Rimini Street, 12462 Athens, Greece

Received 21 August 2013; Revised 2 January 2014; Accepted 13 January 2014; Published 1 April 2014

Academic Editor: Mengzhou Xue

Copyright © 2014 Constantinos Nastos 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. E. E. Douzinas, O. Livaditi, M.-K. Tasoulis et al., “Nitrosative and oxidative stresses contribute to post-ischemic liver injury following severe hemorrhagic shock: the role of hypoxemic resuscitation,” PLoS ONE, vol. 7, no. 3, Article ID e32968, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. N. Arkadopoulos, G. Defterevos, C. Nastos et al., “Development of a porcine model of post-hepatectomy liver failure,” Journal of Surgical Research, vol. 170, no. 2, pp. e233–e242, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. H. Jaeschke, “Molecular mechanisms of hepatic ischemia-reperfusion injury and preconditioning,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 284, no. 1, pp. G15–G26, 2003. View at Google Scholar · View at Scopus
  4. F. Serracino-Inglott, N. A. Habib, and R. T. Mathie, “Hepatic ischemia-reperfusion injury,” American Journal of Surgery, vol. 181, no. 2, pp. 160–166, 2001. View at Publisher · View at Google Scholar · View at Scopus
  5. Y. Chen and X. Xie, “Tacrolimus attenuates myocardium damage to the total hepatic ischemia-reperfusion via regulation of the mitochondrial function,” Journal of Surgical Research, vol. 172, no. 1, pp. e47–e54, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. C. Nastos, K. Kalimeris, N. Papoutsidakis et al., “Antioxidant treatment attenuates intestinal mucosal damage and gut barrier dysfunction after major hepatectomy. Study in a porcine model,” Journal of Gastrointestinal Surgery, vol. 15, no. 5, pp. 809–817, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. K. Kalimeris, C. Nastos, N. Papoutsidakis et al., “Iron chelation prevents lung injury after major hepatectomy,” Hepatology Research, vol. 40, no. 8, pp. 841–850, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. B. Vollmar, J. Glasz, R. Leiderer, S. Post, and M. D. Menger, “Hepatic microcirculatory perfusion failure is a determinant of liver dysfunction in warm ischemia-reperfusion,” American Journal of Pathology, vol. 145, no. 6, pp. 1421–1431, 1994. View at Google Scholar · View at Scopus
  9. V. Smyrniotis, C. Farantos, G. Kostopanagiotou, and N. Arkadopoulos, “Vascular control during hepatectomy: review of methods and results,” World Journal of Surgery, vol. 29, no. 11, pp. 1384–1396, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. G. Garcea, A. Gescher, W. Steward, A. Dennison, and D. Berry, “Oxidative stress in humans following the Pringle manoeuvre,” Hepatobiliary and Pancreatic Diseases International, vol. 5, no. 2, pp. 210–214, 2006. View at Google Scholar · View at Scopus
  11. I. Marzi, Y. Takei, M. Rücker et al., “Endothelin-1 is involved in hepatic sinusoidal vasoconstriction after ischemia and reperfusion,” Transplant International, vol. 7, supplement 1, pp. S503–S506, 1994. View at Google Scholar · View at Scopus
  12. B. Vollmar and M. D. Menger, “The hepatic microcirculation: mechanistic contributions and therapeutic targets in liver injury and repair,” Physiological Reviews, vol. 89, no. 4, pp. 1269–1339, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. D. Uhlmann, S. Glasser, G. Gaebel et al., “Improvement of postischemic hepatic microcirculation after endothelin A receptor blockade—endothelin antagonism influences platelet-endothelium interactions,” Journal of Gastrointestinal Surgery, vol. 9, no. 2, pp. 187–197, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. C. D. Collard and S. Gelman, “Pathophysiology, clinical manifestations, and prevention of ischemia-reperfusion injury,” Anesthesiology, vol. 94, no. 6, pp. 1133–1138, 2001. View at Google Scholar · View at Scopus
  15. M. Mendes-Braz, M. Elias-Miro, M. B. Jimenez-Castro, A. Casillas-Ramirez, F. S. Ramalho, and C. Peralta, “The current state of knowledge of hepatic ischemia-reperfusion injury based on its study in experimental models,” Journal of Biomedicine and Biotechnology, vol. 2012, Article ID 298657, 20 pages, 2012. View at Publisher · View at Google Scholar
  16. N. C. Teoh and G. C. Farrell, “Hepatic ischemia reperfusion injury: pathogenic mechanisms and basis for hepatoprotection,” Journal of Gastroenterology and Hepatology, vol. 18, no. 8, pp. 891–902, 2003. View at Publisher · View at Google Scholar · View at Scopus
  17. 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
  18. A. P. Betrosian, B. Agarwal, and E. E. Douzinas, “Acute renal dysfunction in liver diseases,” World Journal of Gastroenterology, vol. 13, no. 42, pp. 5552–5559, 2007. View at Google Scholar · View at Scopus
  19. V. Arroyo, J. Fernandez, and P. Ginès, “Pathogenesis and treatment of hepatorenal syndrome,” Seminars in Liver Disease, vol. 28, no. 1, pp. 81–95, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. C. L. Davis, T. A. Gonwa, and A. H. Wilkinson, “Pathophysiology of renal disease associated with liver disorders: implications for liver transplantation. Part I,” Liver Transplantation, vol. 8, no. 2, pp. 91–109, 2002. View at Publisher · View at Google Scholar · View at Scopus
  21. Y. M. Barri, E. Q. Sanchez, L. W. Jennings et al., “Acute kidney injury following liver transplantation: definition and outcome,” Liver Transplantation, vol. 15, no. 5, pp. 475–483, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. H. M. Wadei, M. L. Mai, N. Ahsan, and T. A. Gonwa, “Hepatorenal syndrome: pathophysiology and management,” Clinical Journal of the American Society of Nephrology, vol. 1, no. 5, pp. 1066–1079, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Schepke, “Hepatorenal syndrome: current diagnostic and therapeutic concepts,” Nephrology, Dialysis, Transplantation, vol. 22, supplement 8, pp. viii2–viii4, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Rivera-Huizar, A. R. Rincón-Sánchez, A. Covarrubias-Pinedo et al., “Renal dysfunction as a consequence of acute liver damage by bile duct ligation in cirrhotic rats,” Experimental and Toxicologic Pathology, vol. 58, no. 2-3, pp. 185–195, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. Y. Tanaka, J. M. Maher, C. Chen, and C. D. Klaassen, “Hepatic ischemia-reperfusion induces renal heme oxygenase-1 via NF-E2-related factor 2 in rats and mice,” Molecular Pharmacology, vol. 71, no. 3, pp. 817–825, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. A. Tsung, R. A. Hoffman, K. Izuishi et al., “Hepatic ischemia/reperfusion injury involves functional TLR4 signaling in nonparenchymal cells,” Journal of Immunology, vol. 175, no. 11, pp. 7661–7668, 2005. View at Google Scholar · View at Scopus
  27. R. M. Levy, K. P. Mollen, J. M. Prince et al., “Systemic inflammation and remote organ injury following trauma require HMGB1,” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 293, no. 4, pp. R1538–R1544, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Kadkhodaee, S. Mikaeili, M. Zahmatkesh et al., “Alteration of renal functional, oxidative stress and inflammatory indices following hepatic ischemia-reperfusion,” General Physiology and Biophysics, vol. 31, no. 2, pp. 195–202, 2012. View at Google Scholar
  29. S. W. Park, M. Kim, K. M. Brown, V. D. D'Agati, and H. T. Lee, “Paneth cell-derived interleukin-17A causes multiorgan dysfunction after hepatic ischemia and reperfusion injury,” Hepatology, vol. 53, no. 5, pp. 1662–1675, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. T. A. Sutton, H. E. Mang, S. B. Campos, R. M. Sandoval, M. C. Yoder, and B. A. Molitoris, “Injury of the renal microvascular endothelium alters barrier function after ischemia,” American Journal of Physiology—Renal Physiology, vol. 285, no. 2, pp. F191–F198, 2003. View at Google Scholar · View at Scopus
  31. B. A. Molitoris, R. Sandoval, and T. A. Sutton, “Endothelial injury and dysfunction in ischemic acute renal failure,” Critical Care Medicine, vol. 30, no. 5, supplement, pp. S235–S240, 2002. View at Google Scholar · View at Scopus
  32. K. Meyer, M. F. Brown, G. Zibari et al., “ICAM-1 upregulation in distant tissues after hepatic ischemia/reperfusion: a clue to the mechanism of multiple organ failure,” Journal of Pediatric Surgery, vol. 33, no. 2, pp. 350–353, 1998. View at Publisher · View at Google Scholar · View at Scopus
  33. H. T. Lee, S. W. Park, M. Kim, and V. D. D'Agati, “Acute kidney injury after hepatic ischemia and reperfusion injury in mice,” Laboratory Investigation, vol. 89, no. 2, pp. 196–208, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. H. T. Lee, M. Kim, M. Jan, R. B. Penn, and C. W. Emala, “Renal tubule necrosis and apoptosis modulation by A1 adenosine receptor expression,” Kidney International, vol. 71, no. 12, pp. 1249–1261, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. B. Li, B. Chen, G. Zhang, K. Wang, L. Zhou, and S. Hu, “Cell apoptosis and Fas gene expression in liver and renal tissues after ischemia-reperfusion injury in liver transplantation,” Transplantation Proceedings, vol. 42, no. 5, pp. 1550–1556, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. L. E. C. Miranda, V. K. Capellini, G. S. Reis, A. C. Celotto, C. G. Carlotti Jr., and P. R. B. Evora, “Effects of partial liver ischemia followed by global liver reperfusion on the remote tissue expression of nitric oxide synthase: lungs and kidneys,” Transplantation Proceedings, vol. 42, no. 5, pp. 1557–1562, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. C. Polat, Ç. Tokyol, A. Kahraman, B. Sabuncuoǧlu, and S. Yìlmaz, “The effects of desferrioxamine and quercetin on hepatic ischemia-reperfusion induced renal disturbance,” Prostaglandins Leukotrienes and Essential Fatty Acids, vol. 74, no. 6, pp. 379–383, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. B. Seifi, M. Kadkhodaee, F. Delavari, S. Mikaeili, S. Shams, and S. N. Ostad, “Pretreatment with pentoxifylline and N-acetylcysteine in liver ischemia reperfusion-induced renal injury,” Renal Failure, vol. 34, no. 5, pp. 610–615, 2012. View at Google Scholar
  39. J. A. Lee, J. W. Choi, J. H. In et al., “Hepatic ischemic preconditioning provides protection against distant renal ischemia and reperfusion injury in mice,” Journal of Korean Medical Science, vol. 27, no. 5, pp. 547–552, 2012. View at Google Scholar
  40. J. D. Joo, M. Kim, V. D. D'Agati, and H. T. Lee, “Ischemic preconditioning provides both acute and delayed protection against renal ischemia and reperfusion injury in mice,” Journal of the American Society of Nephrology, vol. 17, no. 11, pp. 3115–3123, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Torres and H. J. Forman, “Redox signaling and the MAP kinase pathways,” BioFactors, vol. 17, no. 1–4, pp. 287–296, 2003. View at Google Scholar · View at Scopus
  42. P. S. Kellerman, S. L. Norenberg, and G. M. Jones, “Early recovery of the actin cytoskeleton during renal ischemic injury in vivo,” American Journal of Kidney Diseases, vol. 27, no. 5, pp. 709–714, 1996. View at Google Scholar · View at Scopus
  43. B. A. Molitoris, “Actin cytoskeleton in ischemic acute renal failure,” Kidney International, vol. 66, no. 2, pp. 871–883, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. S. R. White, P. Williams, K. R. Wojcik et al., “Initiation of apoptosis by actin cytoskeletal derangement in human airway epithelial cells,” American Journal of Respiratory Cell and Molecular Biology, vol. 24, no. 3, pp. 282–294, 2001. View at Google Scholar · View at Scopus
  45. D. Dinour and M. Brezis, “Effects of adenosine on intrarenal oxygenation,” American Journal of Physiology—Renal Fluid and Electrolyte Physiology, vol. 261, no. 5, part 2, pp. F787–F791, 1991. View at Google Scholar · View at Scopus
  46. H. T. Lee, G. Gallos, S. H. Nasr, and C. W. Emala, “A1 adenosine receptor activation inhibits inflammation, necrosis, and apoptosis after renal ischemia-reperfusion injury in mice,” Journal of the American Society of Nephrology, vol. 15, no. 1, pp. 102–111, 2004. View at Publisher · View at Google Scholar · View at Scopus
  47. S. W. Park, S. W. C. Chen, M. Kim, K. M. Brown, V. D. D'Agati, and H. T. Lee, “Protection against acute kidney injury via A1 adenosine receptor-mediated Akt activation reduces liver injury after liver ischemia and reperfusion in mice,” Journal of Pharmacology and Experimental Therapeutics, vol. 333, no. 3, pp. 736–747, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. T. G. Cross, D. Scheel-Toellner, N. V. Henriquez, E. Deacon, M. Salmon, and J. M. Lord, “Serine/threonine protein kinases and apoptosis,” Experimental Cell Research, vol. 256, no. 1, pp. 34–41, 2000. View at Publisher · View at Google Scholar · View at Scopus
  49. M. J. Rane, P. Y. Coxon, D. W. Powell et al., “p38 Kinase-dependent MAPKAPK-2 activation functions as 3-phosphoinositide-dependent kinase-2 for Akt in human neutrophils,” The Journal of Biological Chemistry, vol. 276, no. 5, pp. 3517–3523, 2001. View at Publisher · View at Google Scholar · View at Scopus
  50. M. J. Rane, Y. Pan, S. Singh et al., “Heat shock protein 27 controls apoptosis by regulating Akt activation,” The Journal of Biological Chemistry, vol. 278, no. 30, pp. 27828–27835, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. S. W. Park, S. W. C. Chen, M. Kim, V. D. D'Agati, and H. T. Lee, “Human activated protein C attenuates both hepatic and renal injury caused by hepatic ischemia and reperfusion injury in mice,” Kidney International, vol. 76, no. 7, pp. 739–750, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. S. W. Park, M. Kim, S. W. C. Chen, K. M. Brown, V. D. D'Agati, and H. T. Lee, “Sphinganine-1-phosphate protects kidney and liver after hepatic ischemia and reperfusion in mice through S1P 1 receptor activation,” Laboratory Investigation, vol. 90, no. 8, pp. 1209–1224, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. S. W. Park, M. Kim, S. W. C. Chen, V. D. D'Agati, and H. T. Lee, “Sphinganine-1-phosphate attenuates both hepatic and renal injury induced by hepatic ischemia and reperfusion in mice,” Shock, vol. 33, no. 1, pp. 31–42, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. Y. Chen, Z. Liu, and X. Xie, “Hydrogen sulphide attenuates renal and cardiac injury after total hepatic ischemia and reperfusion,” Journal of Surgical Research, vol. 164, no. 2, pp. e305–e313, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. S. Suzuki, A. Serizawa, T. Sakaguchi et al., “The roles of platelet-activating factor and endothelin-1 in renal damage after total hepatic ischemia and reperfusion,” Transplantation, vol. 69, no. 11, pp. 2267–2273, 2000. View at Google Scholar · View at Scopus
  56. D. J. Plevak, P. A. Southorn, B. J. Narr, and S. G. Peters, “Intensive-care unit experience in the Mayo liver transplantation program: the first 100 cases,” Mayo Clinic Proceedings, vol. 64, no. 4, pp. 433–445, 1989. View at Google Scholar · View at Scopus
  57. T. Miyata, I. Yokoyama, S. Todo, A. Tzakis, R. Selby, and T. E. Starzl, “Endotoxaemia, pulmonary complications, and thrombocytopenia in liver transplantation,” The Lancet, vol. 2, no. 8656, pp. 189–191, 1989. View at Google Scholar · View at Scopus
  58. L. M. Colletti, S. L. Kunkel, A. Walz et al., “Chemokine expression during hepatic ischemia/reperfusion-induced lung injury in the rat. The role of epithelial neutrophil activating protein,” The Journal of Clinical Investigation, vol. 95, no. 1, pp. 134–141, 1995. View at Google Scholar · View at Scopus
  59. L. M. Colletti, A. Cortis, N. Lukacs, S. L. Kunkel, M. Green, and R. M. Strieter, “Tumor necrosis factor up-regulates intercellular adhesion molecule 1, which is important in the neutrophil-dependent lung and liver injury associated with hepatic ischemia and reperfusion in the rat,” Shock, vol. 10, no. 3, pp. 182–191, 1998. View at Google Scholar · View at Scopus
  60. N. Arkadopoulos, K. Kalimeris, A. Papalois et al., “Treatment with bioartificial liver improves lung injury in a swine model of partial hepatectomy and ischemia/reperfusion,” International Journal of Artificial Organs, vol. 33, no. 2, pp. 105–113, 2010. View at Google Scholar · View at Scopus
  61. A. Serizawa, S. Nakamura, S. Suzuki, S. Baba, and M. Nakano, “Involvement of platelet-activating factor in cytokine production and neutrophil activation after hepatic ischemia-reperfusion,” Hepatology, vol. 23, no. 6, pp. 1656–1663, 1996. View at Publisher · View at Google Scholar · View at Scopus
  62. G. A. Wanner, W. Ertel, P. Müller et al., “Liver ischemia and reperfusion induces a systemic inflammatory response through Kupffer cell activation,” Shock, vol. 5, no. 1, pp. 34–40, 1996. View at Google Scholar · View at Scopus
  63. D. Takeuchi, H. Yoshidome, H. Kurosawa et al., “Interleukin-18 exacerbates pulmonary injury after hepatic ischemia/reperfusion in mice,” Journal of Surgical Research, vol. 158, no. 1, pp. 87–93, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. T. Okaya, R. Holthaus, A. Kato, and A. B. Lentsch, “Involvement of the neuropeptide substance P in lung inflammation induced by hepatic ischemia/reperfusion,” Inflammation Research, vol. 53, no. 6, pp. 257–261, 2004. View at Publisher · View at Google Scholar · View at Scopus
  65. H. Yoshidome, A. Kato, M. J. Edwards, and A. B. Lentsch, “Interleukin-10 inhibits pulmonary NF-κB activation and lung injury induced by hepatic ischemia-reperfusion,” American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 277, no. 5, part 1, pp. L919–L923, 1999. View at Google Scholar · View at Scopus
  66. M. P. Callery, T. Kamei, M. J. Mangino, and M. W. Flye, “Organ interactions in sepsis: Host defense and the hepatic-pulmonary macrophage axis,” Archives of Surgery, vol. 126, no. 1, pp. 28–32, 1991. View at Google Scholar · View at Scopus
  67. L. C. J. M. Lemaire, B. A. van Wagensveld, T. M. van Gulik, J. Dankert, J. J. B. van Lanschot, and D. J. Gouma, “Bacterial translocation to the thoracic duct in a setting of ischemia, partial resection and reperfusion of the porcine liver,” Digestive Surgery, vol. 16, no. 3, pp. 222–228, 1999. View at Publisher · View at Google Scholar · View at Scopus
  68. G. M. Matuschak, K. A. Henry, C. A. Johanns, and A. J. Lechner, “Liver-lung interactions following Escherichia coil bacteremic sepsis and secondary hepatic ischemia/reperfusion injury,” American Journal of Respiratory and Critical Care Medicine, vol. 163, no. 4, pp. 1002–1009, 2001. View at Google Scholar · View at Scopus
  69. L. M. Colletti and M. Green, “Lung and liver injury following hepatic ischemia/ reperfusion in the rat is increased by exogenous lipopolysaccharide which also increases hepatic tnf production in vivo and in vitro,” Shock, vol. 16, no. 4, pp. 312–319, 2001. View at Google Scholar · View at Scopus
  70. S. Q. van Veen, S. Dinant, A. K. van Vliet, and T. M. van Gulik, “Alkaline phosphatase reduces hepatic and pulmonary injury in liver ischaemia-reperfusion combined with partial resection,” British Journal of Surgery, vol. 93, no. 4, pp. 448–456, 2006. View at Publisher · View at Google Scholar · View at Scopus
  71. A. Weinbroum, V. G. Nielsen, S. Tan et al., “Liver ischemia-reperfusion increases pulmonary permeability in rat: role of circulating xanthine oxidase,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 268, no. 6, pp. G988–G996, 1995. View at Google Scholar · View at Scopus
  72. V. G. Nielsen, S. Tan, A. Weinbroum et al., “Lung injury after hepatoenteric ischemia-reperfusion: role of xanthine oxidase,” American Journal of Respiratory and Critical Care Medicine, vol. 154, no. 5, pp. 1364–1369, 1996. View at Google Scholar · View at Scopus
  73. C. Peralta, N. Prats, C. Xaus, E. Gelpí', and J. Roselló-Catafau, “Protective effect of liver ischemic preconditioning on liver and lung injury induced by hepatic ischemia-reperfusion in the rat,” Hepatology, vol. 30, no. 6, pp. 1481–1489, 1999. View at Google Scholar · View at Scopus
  74. P. Liu, B. Xu, and C. E. Hock, “Inhibition of nitric oxide synthesis by L-name exacerbates acute lung injury induced by hepatic ischemia-reperfusion,” Shock, vol. 16, no. 3, pp. 211–217, 2001. View at Google Scholar · View at Scopus
  75. Y. Takamatsu, K. Shimada, K. Yamaguchi, S. Kuroki, K. Chijiiwa, and M. Tanaka, “Inhibition of inducible nitric oxide synthase prevents hepatic, but not pulmonary, injury following ischemia-reperfusion of rat liver,” Digestive Diseases and Sciences, vol. 51, no. 3, pp. 571–579, 2006. View at Publisher · View at Google Scholar · View at Scopus
  76. A. A. Weinbroum, G. Paret, O. Szold, V. Rudick, and L. Krupitzky, “Selective attenuation of acute lung ventilatory injury by methylene blue after liver ischemia-reperfusion: a drug response study in an isolated perfused double organ model,” Transplantation, vol. 72, no. 3, pp. 385–392, 2001. View at Google Scholar · View at Scopus
  77. A. A. Weinbroum, I. Shapira, R. B. Abraham, and A. Szold, “Mannitol dose-dependently attenuates lung reperfusion injury following liver ischemia reperfusion: a dose-response study in an isolated perfused double-organ model,” Lung, vol. 180, no. 6, pp. 327–338, 2002. View at Publisher · View at Google Scholar · View at Scopus
  78. K.-C. Chan, C.-J. Lin, P.-H. Lee et al., “Propofol attenuates the decrease of dynamic compliance and water content in the lung by decreasing oxidative radicals released from the reperfused liver,” Anesthesia and Analgesia, vol. 107, no. 4, pp. 1284–1289, 2008. View at Publisher · View at Google Scholar · View at Scopus
  79. X. Lv, Z.-M. Wang, S.-D. Huang, S.-H. Song, F.-X. Wu, and W.-F. Yu, “Emulsified isoflurane preconditioning reduces lung injury induced by hepatic ischemia/reperfusion in rats,” International Journal of Medical Sciences, vol. 8, no. 5, pp. 353–361, 2011. View at Google Scholar · View at Scopus
  80. S. K. Hong, S. Hwang, S. G. Lee et al., “Pulmonary complications following adult liver transplantation,” Transplantation Proceedings, vol. 38, no. 9, pp. 2979–2981, 2006. View at Publisher · View at Google Scholar · View at Scopus
  81. X.-H. Wen, H.-Y. Kong, S.-M. Zhu, J.-H. Xu, S.-Q. Huang, and Q.-L. Chen, “Plasma levels of tumor necrotic factor-alpha and interleukin-6, -8 during orthotopic liver transplantation and their relations to postoperative pulmonary complications,” Hepatobiliary and Pancreatic Diseases International, vol. 3, no. 1, pp. 38–41, 2004. View at Google Scholar · View at Scopus
  82. X.-J. Chi, J. Cai, C.-F. Luo et al., “Relationship between the expression of Toll-like receptor 2 and 4 in mononuclear cells and postoperative acute lung injury in orthotopic liver transplantation,” Chinese Medical Journal, vol. 122, no. 8, pp. 895–899, 2009. View at Publisher · View at Google Scholar · View at Scopus
  83. M. Goto, Y. Takei, S. Kawano et al., “Tumor necrosis factor and endotoxin in the pathogenesis of liver and pulmonary injuries after orthotopic liver transplantation in the rat,” Hepatology, vol. 16, no. 2, pp. 487–493, 1992. View at Publisher · View at Google Scholar · View at Scopus
  84. C. Spencer Yost, M. A. Matthay, and M. A. Gropper, “Etiology of acute pulmonary edema during liver transplantation: a series of cases with analysis of the edema fluid,” Chest, vol. 119, no. 1, pp. 219–223, 2001. View at Publisher · View at Google Scholar · View at Scopus
  85. C. C. Silliman, L. K. Boshkov, Z. Mehdizadehkashi et al., “Transfusion-related acute lung injury: epidemiology and a prospective analysis of etiologic factors,” Blood, vol. 101, no. 2, pp. 454–462, 2003. View at Publisher · View at Google Scholar · View at Scopus
  86. I. T. A. Pereboom, M. T. de Boer, E. B. Haagsma, H. G. D. Hendriks, T. Lisman, and R. J. Porte, “Platelet transfusion during liver transplantation is associated with increased postoperative mortality due to acute lung injury,” Anesthesia and Analgesia, vol. 108, no. 4, pp. 1083–1091, 2009. View at Publisher · View at Google Scholar · View at Scopus
  87. E. Abdala, C. E. Sandoll Baía, S. Mies et al., “Bacterial translocation during liver transplantation: a randomized trial comparing conventional with venovenous bypass vs. piggyback methods,” Liver Transplantation, vol. 13, no. 4, pp. 488–496, 2007. View at Publisher · View at Google Scholar · View at Scopus
  88. K. S. Filos, I. Kirkilesis, I. Spiliopoulou et al., “Bacterial translocation, endotoxaemia and apoptosis following Pringle manoeuvre in rats,” Injury, vol. 35, no. 1, pp. 35–43, 2004. View at Publisher · View at Google Scholar · View at Scopus
  89. C. Zheyu and Y. Lunan, “Early changes of small intestine function in rats after liver transplantation,” Transplantation Proceedings, vol. 38, no. 5, pp. 1564–1568, 2006. View at Publisher · View at Google Scholar · View at Scopus
  90. E. Okay, A. Karadenizli, B. Müezzinoglu, U. Zeybek, H. A. Ergen, and T. Isbir, “N-acetylcysteine attenuates bacterial translocation after partial hepatectomy in rats,” Journal of Surgical Research, vol. 127, no. 2, pp. 164–170, 2005. View at Publisher · View at Google Scholar · View at Scopus
  91. I. H. Alexandris, S. F. Assimakopoulos, C. E. Vagianos et al., “Oxidative state in intestine and liver after partial hepatectomy in rats. Effect of bombesin and neurotensin,” Clinical Biochemistry, vol. 37, no. 5, pp. 350–356, 2004. View at Publisher · View at Google Scholar · View at Scopus
  92. F. Bongard, N. Pianim, S. Dubecz et al., “Adverse consequences of increased intra-abdominal pressure on bowel tissue oxygen,” Journal of Trauma—Injury, Infection and Critical Care, vol. 39, no. 3, pp. 519–525, 1995. View at Google Scholar · View at Scopus
  93. S. Wattanasirichaigoon, M. J. Menconi, R. L. Delude, and M. P. Fink, “Effect of mesenteric ischemia and reperfusion or hemorrhagic shock on intestinal mucosal permeability and ATP content in rats,” Shock, vol. 12, no. 2, pp. 127–133, 1999. View at Google Scholar · View at Scopus
  94. D. G. Farmer, F. Amersi, J. Kupiec-Weglinski, and R. W. Busuttil, “Current status of ischemia and reperfusion injury in the liver,” Transplantation Reviews, vol. 14, no. 2, pp. 106–126, 2000. View at Google Scholar · View at Scopus
  95. X. D. Wang, H. Parsson, R. Andersson, V. Soltesz, K. Johansson, and S. Bengmark, “Bacterial translocation, intestinal ultrastructure and cell membrane permeability early after major liver resection in the rat,” British Journal of Surgery, vol. 81, no. 4, pp. 579–584, 1994. View at Publisher · View at Google Scholar · View at Scopus
  96. B. A. van Wagensveld, T. M. van Gulik, E. E. E. Gabeler, A. J. van der Kleij, H. Obertop, and D. J. Gouma, “Intrahepatic tissue pO2 during continuous or intermittent vascular inflow occlusion in a pig liver resection model,” European Surgical Research, vol. 30, no. 1, pp. 13–25, 1998. View at Publisher · View at Google Scholar · View at Scopus
  97. X.-D. Wang, W.-D. Guo, Q. Wang et al., “The association between enteric bacterial overgrowth and gastrointestinal motility after subtotal liver resection or portal vein obstruction in rats,” European Journal of Surgery, Acta Chirurgica, vol. 160, no. 3, pp. 153–160, 1994. View at Google Scholar · View at Scopus
  98. S. Raha and B. H. Robinson, “Mitochondria, oxygen free radicals, and apoptosis,” American Journal of Medical Genetics—Seminars in Medical Genetics, vol. 106, no. 1, pp. 62–70, 2001. View at Publisher · View at Google Scholar · View at Scopus
  99. I. Yokoyama, M. Negita, A. Hayakawa et al., “Free radicals and apoptosis of the endothelial cells,” Transplantation Proceedings, vol. 32, no. 1, p. 26, 2000. View at Publisher · View at Google Scholar · View at Scopus
  100. I. Stoian, A. Oros, and E. Moldoveanu, “Apoptosis and free radicals,” Biochemical and Molecular Medicine, vol. 59, no. 2, pp. 93–97, 1996. View at Publisher · View at Google Scholar · View at Scopus
  101. C. Zhang, Z.-Y. Sheng, S. Hu, J.-C. Gao, S. Yu, and Y. Liu, “The influence of apoptosis of mucosal epithelial cells on intestinal barrier integrity after scald in rats,” Burns, vol. 28, no. 8, pp. 731–737, 2002. View at Publisher · View at Google Scholar · View at Scopus
  102. T. Noda, R. Iwakiri, K. Fujimoto, S. Matsuo, and T. Y. Aw, “Programmed cell death induced by ischemia-reperfusion in rat intestinal mucosa,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 274, no. 2, part 1, pp. G270–G276, 1998. View at Google Scholar · View at Scopus
  103. H. Ikeda, Y. Suzuki, M. Suzuki et al., “Apoptosis is a major mode of cell death caused by ischaemia and ischaemia/reperfusion injury to the rat intestinal epithelium,” Gut, vol. 42, no. 4, pp. 530–537, 1998. View at Google Scholar · View at Scopus
  104. K. A. Shah, S. Shurey, and C. J. Green, “Apoptosis after intestinal ischemia-reperfusion injury: a morphological study,” Transplantation, vol. 64, no. 10, pp. 1393–1397, 1997. View at Google Scholar · View at Scopus
  105. J.-F. Beaulieu, “Differential expression of the VLA family of integrins along the crypt-villus axis in the human small intestine,” Journal of Cell Science, vol. 102, part 3, pp. 427–436, 1992. View at Google Scholar · View at Scopus
  106. R. Probstmeier, R. Martini, and M. Schachner, “Expression of J1/tenascin in the crypt-villus unit of adult mouse small intestine: implications for its role in epithelial cell shedding,” Development, vol. 109, no. 2, pp. 313–321, 1990. View at Google Scholar · View at Scopus
  107. S. M. Frisch and H. Francis, “Disruption of epithelial cell-matrix interactions induces apoptosis,” Journal of Cell Biology, vol. 124, no. 4, pp. 619–626, 1994. View at Google Scholar · View at Scopus
  108. S. Mochida, M. Arai, A. Ohno, and K. Fujiwara, “Bacterial translocation from gut to portal blood in the recipient as a factor of hypercoagulopathy in hepatic sinusoids after orthotopic liver transplantation in rats,” Transplantation Proceedings, vol. 29, no. 1-2, pp. 874–875, 1997. View at Publisher · View at Google Scholar · View at Scopus
  109. A. Bedurlu, S. Gokahmetoglu, K. C. Kucuk, I. Soyuer, L. Guler, and O. Sakrak, “Bacterial translocation after partial hepatic resection under ischemia and reperfusion in rats: incidence and time course,” Turkish Journal of Medical Sciences, vol. 33, pp. 135–140, 2003. View at Google Scholar
  110. H. Jiang, F. Meng, W. Li, L. Tong, H. Qiao, and X. Sun, “Splenectomy ameliorates acute multiple organ damage induced by liver warm ischemia reperfusion in rats,” Surgery, vol. 141, no. 1, pp. 32–40, 2007. View at Publisher · View at Google Scholar · View at Scopus
  111. I. Leister, J. Sydow, T. Stojanovic et al., “Impact of vasoactive intestinal polypeptide and gastrin-releasing peptide on small bowel microcirculation and mucosal injury after hepatic ischemia/reperfusion in rats,” International Journal of Colorectal Disease, vol. 20, no. 1, pp. 42–48, 2005. View at Publisher · View at Google Scholar · View at Scopus
  112. H. Ochiai, S. Nakamura, S. Suzuki, S. Baba, and S. Baba, “Pancreatic damage resulting from temporary portal triad interruption during partial hepatectomy: protective effect of a prostaglandin I2 analogue,” Journal of Surgical Research, vol. 73, no. 2, pp. 129–136, 1997. View at Publisher · View at Google Scholar · View at Scopus
  113. E. Ronholm, H. Tomasdottir, J. Runeborg et al., “Complement system activation during orthotopic liver transplantation in man: indications of peroperative complement system activation in the gut,” Transplantation, vol. 57, no. 11, pp. 1594–1597, 1994. View at Google Scholar · View at Scopus
  114. Z.-W. Wu, K.-J. Xu, L.-J. Li et al., “Investigation of intestinal bacterial translocation in 78 patients with cirrhosis after liver transplantation,” Zhonghua Wai Ke Za Zhi, vol. 44, no. 21, pp. 1456–1459, 2006. View at Google Scholar · View at Scopus
  115. T. Tsuzuki, S. Shimizu, S. Takahashi, and H. Iio, “Hyperamylasemia after hepatic resection,” American Journal of Gastroenterology, vol. 88, no. 5, pp. 734–736, 1993. View at Google Scholar · View at Scopus
  116. S. Sjovall, T. Holmin, A. Evander, and U. Stenram, “Splenic and gastro-duodenal vein occlusion-influence on the pancreatic gland and on the outcome of experimental pancreatitis,” International Journal of Pancreatology, vol. 3, no. 2-3, pp. 143–149, 1988. View at Google Scholar · View at Scopus
  117. S. Miyagawa, M. Makuuchi, S. Kawasaki, and T. Kakazu, “Changes in serum amylase level following hepatic resection in chronic liver disease,” Archives of Surgery, vol. 129, no. 6, pp. 634–638, 1994. View at Google Scholar · View at Scopus
  118. S. Miyagawa, M. Makuuchi, S. Kawasaki, T. Kakazu, K. Hayashi, and H. Kasai, “Serum amylase elevation following hepatic resection in patients with chronic liver disease,” American Journal of Surgery, vol. 171, no. 2, pp. 235–238, 1996. View at Publisher · View at Google Scholar · View at Scopus
  119. N. Hashimoto, S. Haji, H. Nomura, and H. Ohyanagi, “Hyperamylasemia after hepatic resection,” Hepato-Gastroenterology, vol. 50, no. 53, pp. 1472–1473, 2003. View at Google Scholar · View at Scopus
  120. K. Kubota, M. Makuuchi, T. Noie et al., “Risk factors for hyperamylasemia after hepatectomy using the pringle maneuver: randomized analysis of surgical parameters,” Archives of Surgery, vol. 133, no. 3, pp. 303–308, 1998. View at Publisher · View at Google Scholar · View at Scopus
  121. K. Meyer, M. F. Brown, G. Zibari et al., “ICAM-1 upregulation in distant tissues after hepatic ischemia/reperfusion: a clue to the mechanism of multiple organ failure,” Journal of Pediatric Surgery, vol. 33, no. 2, pp. 350–353, 1998. View at Publisher · View at Google Scholar · View at Scopus
  122. H. Ochiai, S. Nakamura, S. Suzuki, S. Baba, and S. Baba, “Pancreatic damage resulting from temporary portal triad interruption during partial hepatectomy: protective effect of a prostaglandin I2 analogue,” Journal of Surgical Research, vol. 73, no. 2, pp. 129–136, 1997. View at Publisher · View at Google Scholar · View at Scopus
  123. J.-C. Yang, Z.-W. Wang, C.-L. Li, J.-H. Lin, X.-G. Liu, and Q.-X. Ji, “Multiple organ injury at early stage of intestinal and hepatic ischemia-reperfusion in rats,” Di Yi Jun Yi da Xue Xue Bao, vol. 24, no. 2, pp. 198–203, 2004. View at Google Scholar · View at Scopus
  124. N. Arkadopoulos, C. Nastos, G. Defterevos et al., “Pancreatic injury after major hepatectomy: a study in a porcine model,” Surgery Today, vol. 42, no. 4, pp. 368–375, 2012. View at Publisher · View at Google Scholar · View at Scopus
  125. C. A. Camargo Jr., P. D. Greig, G. A. Levy, and P.-A. Clavien, “Acute pancreatitis following liver transplantation,” Journal of the American College of Surgeons, vol. 181, no. 3, pp. 249–256, 1995. View at Google Scholar · View at Scopus
  126. Y. Li, P.-J. Zhang, C. Jin et al., “Protective effects of deferoxamine mesylate preconditioning on pancreatic tissue in orthotopic liver autotransplantation in rats,” Transplantation Proceedings, vol. 43, no. 5, pp. 1450–1455, 2011. View at Publisher · View at Google Scholar · View at Scopus
  127. A. D. Gouliamos, A. Metafa, S. G. Ispanopoulou, F. Stamatelopoulou, L. J. Vlahos, and J. D. Papadimitriou, “Right adrenal hematoma following hepatectomy,” European Radiology, vol. 10, no. 4, pp. 583–585, 2000. View at Google Scholar · View at Scopus
  128. R. W. Prokesch, W. Schima, G. Berlakovich, and J. Zacherl, “Adrenal hemorrhage after orthotopic liver transplantation: MR appearance,” European Radiology, vol. 11, no. 12, pp. 2484–2487, 2001. View at Publisher · View at Google Scholar · View at Scopus
  129. T. Iwasaki, M. Tominaga, T. Fukumoto et al., “Relative adrenal insufficiency manifested with multiple organ dysfunction in a liver transplant patient,” Liver Transplantation, vol. 12, no. 12, pp. 1896–1899, 2006. View at Publisher · View at Google Scholar · View at Scopus
  130. P. E. Marik, T. Gayowski, and T. E. Starzl, “The hepatoadrenal syndrome: a common yet unrecognized clinical condition,” Critical Care Medicine, vol. 33, no. 6, pp. 1254–1259, 2005. View at Publisher · View at Google Scholar · View at Scopus
  131. T. G. Vishnyakova, A. V. Bocharov, I. N. Baranova et al., “Binding and internalization of lipopolysaccharide by Cla-1, a human orthologue of rodent scavenger receptor B1,” The Journal of Biological Chemistry, vol. 278, no. 25, pp. 22771–22780, 2003. View at Publisher · View at Google Scholar · View at Scopus
  132. W. H. Ettinger, V. K. Varma, M. Sorci-Thomas et al., “Cytokines decrease apolipoprotein accumulation in medium from Hep G2 cells,” Arteriosclerosis and Thrombosis, vol. 14, no. 1, pp. 8–13, 1994. View at Google Scholar · View at Scopus
  133. J. M. Mann, M. Pierre-Louis, P. J. Kragel, A. H. Kragel, and W. C. Roberts, “Cardiac consequences of massive acetaminophen overdose,” American Journal of Cardiology, vol. 63, no. 13, pp. 1018–1021, 1989. View at Google Scholar · View at Scopus
  134. R. A. Wakeel, H. T. Davies, and J. D. Williams, “Toxic myocarditis in paracetamol poisoning,” British Medical Journal, vol. 295, no. 6606, p. 1097, 1987. View at Google Scholar · View at Scopus
  135. N. K. Parekh, L. S. Hynan, J. De Lemos et al., “Elevated troponin I levels in acute liver failure: is myocardial injury an integral part of acute liver failure?” Hepatology, vol. 45, no. 6, pp. 1489–1495, 2007. View at Publisher · View at Google Scholar · View at Scopus
  136. N. Papoutsidakis, N. Arkadopoulos, V. Smyrniotis et al., “Early myocardial injury is an integral component of experimental acute liver failure—a study in two porcine models,” Archives of Medical Science, vol. 7, no. 2, pp. 217–223, 2011. View at Publisher · View at Google Scholar · View at Scopus