The Role of Hepatic Ischemia–Reperfusion Injury and Liver Parenchymal Quality on Cancer Recurrence

Digestive Diseases and Sciences

Volumn 59, Issue 9, 2014, Pages 2058-2068

  Orci, Lorenzo A ^a   Lacotte, Stéphanie ^a   Oldani, Graziano ^a   Morel, Philippe ^a   Mentha, Gilles ^a   Toso, Christian ^a  

^a GENEVA UNIVERSITY HOSPITALS   (Switzerland)

Author keywords

Hepatectomy; Hepatocellular carcinoma; Ischemia reperfusion injury; Liver steatosis; Liver transplantation

Indexed keywords

ANGIOGENIC FACTOR;

CANCER GROWTH; CANCER RECURRENCE; CANCER SURGERY; CELL PROLIFERATION; CIRCULATING TUMOR CELL; HEPATIC ISCHEMIA REPERFUSION INJURY; HUMAN; LIVER CANCER; LIVER ISCHEMIA; LIVER PARENCHYMA; LIVER SURGERY; MEDICAL LITERATURE; MEDLINE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; RISK ASSESSMENT; SYSTEMATIC REVIEW; UPREGULATION;

ANIMALS; ANOXIA; CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LIVER; LIVER NEOPLASMS; NEOPLASM RECURRENCE, LOCAL; NEOPLASM SEEDING; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; REPERFUSION INJURY; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84907879113     PISSN: 01632116     EISSN: 15732568     Source Type: Journal    
DOI: 10.1007/s10620-014-3182-7     Document Type: Review

References (109)

1. Pan J, Konstas AA, Bateman B, Ortolano GA, Pile-Spellman J. Reperfusion injury following cerebral ischemia: pathophysiology, MR imaging, and potential therapies. Neuroradiology. 2007;49:93–102.
2. Collard CD, Gelman S. Pathophysiology, clinical manifestations, and prevention of ischemia-reperfusion injury. Anesthesiology. 2001;94:1133–1138.
3. Zhong H, Gao Z, Chen M, et al. Cardioprotective effect of remote ischemic postconditioning on children undergoing cardiac surgery: a randomized controlled trial. Paediatr Anaesth. 2013;23:726–733.
4. Orci LA, Toso C, Mentha G, Morel P, Majno PE. Systematic review and meta-analysis of the effect of perioperative steroids on ischaemia–reperfusion injury and surgical stress response in patients undergoing liver resection. Br J Surg. 2013;100:600–609.
5. Zhai Y, Petrowsky H, Hong JC, Busuttil RW, Kupiec-Weglinski JW. Ischaemia–reperfusion injury in liver transplantation—from bench to bedside. Nat Rev Gastroenterol Hepatol. 2013;10:79–89.
6. van der Vliet JA, Warle MC. The need to reduce cold ischemia time in kidney transplantation. Curr Opin Organ Transplant. 2013;18:174–178.
7. Bahde R, Spiegel HU. Hepatic ischaemia–reperfusion injury from bench to bedside. Br J Surg. 2010;97:1461–1475.
8. Powell JT, Tsapepas DS, Martin ST, Hardy MA, Ratner LE. Managing renal transplant ischemia reperfusion injury: novel therapies in the pipeline. Clin Transplant. 2013;27:484–491.
9. de Boer MT, Molenaar IQ, Porte RJ. Impact of blood loss on outcome after liver resection. Dig Surg. 2007;24:259–264.
10. Kooby DA, Stockman J, Ben-Porat L, et al. Influence of transfusions on perioperative and long-term outcome in patients following hepatic resection for colorectal metastases. Ann Surg. 2003;237:860–869. (discussion 869–870).
11. Katz SC, Shia J, Liau KH, et al. Operative blood loss independently predicts recurrence and survival after resection of hepatocellular carcinoma. Ann Surg. 2009;249:617–623.
12. Gurusamy KS, Naik P, Abu-Amara M, Fuller B, Davidson BR. Techniques of flushing and reperfusion for liver transplantation. Cochrane Database Syst Rev. 2012;3:CD007512.
13. Mullhaupt B, Dimitroulis D, Gerlach JT, Clavien PA. Hot topics in liver transplantation: organ allocation—extended criteria donor—living donor liver transplantation. J Hepatol. 2008;48:S58–S67.
14. Pascher A, Neuhaus P. Biliary complications after deceased-donor orthotopic liver transplantation. J Hepatobiliary Pancreat Surg. 2006;13:487–496.
15. Jay CL, Lyuksemburg V, Ladner DP, et al. Ischemic cholangiopathy after controlled donation after cardiac death liver transplantation: a meta-analysis. Ann Surg. 2011;253:259–264.
16. Clavien PA, Petrowsky H, DeOliveira ML, Graf R. Strategies for safer liver surgery and partial liver transplantation. N Engl J Med. 2007;356:1545–1559.
17. Marsman HA, Heger M, Kloek JJ, Nienhuis SL, ten Kate FJ, van Gulik TM. Omega-3 fatty acids reduce hepatic steatosis and consequently attenuate ischemia-reperfusion injury following partial hepatectomy in rats. Dig Liver Dis. 2011;43:984–990.
18. Selzner N, Selzner M, Jochum W, Clavien PA. Ischemic preconditioning protects the steatotic mouse liver against reperfusion injury: an ATP dependent mechanism. J Hepatol. 2003;39:55–61.
19. Serafin A, Rosello-Catafau J, Prats N, Xaus C, Gelpi E, Peralta C. Ischemic preconditioning increases the tolerance of fatty liver to hepatic ischemia-reperfusion injury in the rat. Am J Pathol. 2002;161:587–601.
20. Selzner N, Selzner M, Jochum W, Amann-Vesti B, Graf R, Clavien PA. Mouse livers with macrosteatosis are more susceptible to normothermic ischemic injury than those with microsteatosis. J Hepatol. 2006;44:694–701.
21. Selzner M, Selzner N, Jochum W, Graf R, Clavien PA. Increased ischemic injury in old mouse liver: an ATP-dependent mechanism. Liver Transpl. 2007;13:382–390.
22. Dutkowski P, Schlegel A, Slankamenac K, et al. The use of fatty liver grafts in modern allocation systems: risk assessment by the balance of risk (BAR) score. Ann Surg. 2012;256:861–868. (discussion 868–869).
23. Nocito A, El-Badry AM, Clavien PA. When is steatosis too much for transplantation? J Hepatol. 2006;45:494–499.
24. Guller U, Zajac P, Schnider A, et al. Disseminated single tumor cells as detected by real-time quantitative polymerase chain reaction represent a prognostic factor in patients undergoing surgery for colorectal cancer. Ann Surg. 2002;236:768–775. (discussion 775–766).
25. Yamaguchi K, Takagi Y, Aoki S, Futamura M, Saji S. Significant detection of circulating cancer cells in the blood by reverse transcriptase-polymerase chain reaction during colorectal cancer resection. Ann Surg. 2000;232:58–65.
26. Anasagasti MJ, Alvarez A, Martin JJ, Mendoza L, Vidal-Vanaclocha F. Sinusoidal endothelium release of hydrogen peroxide enhances very late antigen-4-mediated melanoma cell adherence and tumor cytotoxicity during interleukin-1 promotion of hepatic melanoma metastasis in mice. Hepatology. 1997;25:840–846.
27. Higashiyama A, Watanabe H, Okumura K, Yagita H. Involvement of tumor necrosis factor alpha and very late activation antigen 4/vascular cell adhesion molecule 1 interaction in surgical-stress-enhanced experimental metastasis. Cancer Immunol Immunother (CII). 1996;42:231–236.
28. Vidal-Vanaclocha F, Alvarez A, Asumendi A, Urcelay B, Tonino P, Dinarello CA. Interleukin 1 (IL-1)-dependent melanoma hepatic metastasis in vivo; increased endothelial adherence by IL-1-induced mannose receptors and growth factor production in vitro. J Natl Cancer Inst. 1996;88:198–205.
29. Chu MJ, Hickey AJ, Phillips AR, Bartlett AS. The impact of hepatic steatosis on hepatic ischemia-reperfusion injury in experimental studies: a systematic review. BioMed Res Int. 2013;2013:192029.
30. Murphy P, Alexander P, Senior PV, Fleming J, Kirkham N, Taylor I. Mechanisms of organ selective tumour growth by bloodborne cancer cells. Br J Cancer. 1988;57:19–31.
31. Robinson KP, Hoppe E. The development of blood-borne metastases. Effect of local trauma and ischemia. Arch Surg. 1962;85:720–724.
32. Kurata M, Okajima K, Kawamoto T, Uchiba M, Ohkohchi N. Antithrombin reduces reperfusion-induced hepatic metastasis of colon cancer cells. World J Gastroenterol. 2006;12:60–65.
33. Nicoud IB, Jones CM, Pierce JM, et al. Warm hepatic ischemia-reperfusion promotes growth of colorectal carcinoma micrometastases in mouse liver via matrix metalloproteinase-9 induction. Cancer Res. 2007;67:2720–2728.
34. Man K, Ng KT, Lo CM, et al. Ischemia-reperfusion of small liver remnant promotes liver tumor growth and metastases—activation of cell invasion and migration pathways. Liver Transpl. 2007;13:1669–1677.
35. Doi K, Horiuchi T, Uchinami M, et al. Neutrophil elastase inhibitor reduces hepatic metastases induced by ischaemia–reperfusion in rats. Eur J Surg. 2002;168:507–510.
36. Tamagawa K, Horiuchi T, Uchinami M, et al. Hepatic ischemia-reperfusion increases vascular endothelial growth factor and cancer growth in rats. J Surg Res. 2008;148:158–163.
37. Yoshida M, Horiuchi T, Uchinami M, et al. Intermittent hepatic ischemia-reperfusion minimizes liver metastasis in rats. J Surg Res. 2003;111:255–260.
38. Yoshimoto K, Tajima H, Ohta T, et al. Increased E-selectin in hepatic ischemia-reperfusion injury mediates liver metastasis of pancreatic cancer. Oncol Rep. 2012;28:791–796.
39. van der Bilt JD, Kranenburg O, Borren A, van Hillegersberg R, Borel Rinkes IH. Ageing and hepatic steatosis exacerbate ischemia/reperfusion-accelerated outgrowth of colorectal micrometastases. Ann Surg Oncol. 2008;15:1392–1398.
40. Doi K, Horiuchi T, Uchinami M, et al. Hepatic ischemia-reperfusion promotes liver metastasis of colon cancer. J Surg Res. 2002;105:243–247.
41. Fisher B, Fisher ER. Experimental studies of factors influencing hepatic metastases. III. Effect of surgical trauma with special reference to liver injury. Ann Surg. 1959;150:731–744.
42. Ichihashi H, Mabuchi H, Suenaga M, Kondo T. Liver regeneration and tumor growth in the rat after partial hepatectomy. Jpn J Surg. 1984;14:510–514.
43. Ikeda Y, Matsumata T, Takenaka K, Sasaki O, Soejima K, Sugimachi K. Preliminary report of tumor metastasis during liver regeneration after hepatic resection in rats. Eur J Surg Oncol. 1995;21:188–190.
44. Isbert C, Boerner A, Ritz JP, Schuppan D, Buhr HJ, Germer CT. In situ ablation of experimental liver metastases delays and reduces residual intrahepatic tumour growth and peritoneal tumour spread compared with hepatic resection. Br J Surg. 2002;89:1252–1259.
45. Mizutani J, Hiraoka T, Yamashita R, Miyauchi Y. Promotion of hepatic metastases by liver resection in the rat. Br J Cancer. 1992;65:794–797.
46. Picardo A, Karpoff HM, Ng B, Lee J, Brennan MF, Fong Y. Partial hepatectomy accelerates local tumor growth: potential roles of local cytokine activation. Surgery. 1998;124:57–64.
47. Schindel DT, Grosfeld JL. Hepatic resection enhances growth of residual intrahepatic and subcutaneous hepatoma, which is inhibited by octreotide. J Pediatr Surg. 1997;32:995–997. (discussion 997–998).
48. de Jong KP, Slooff MJ, de Vries EG, Brouwers MA, Terpstra OT. Effect of partial liver resection on tumour growth. J Hepatol. 1996;25:109–121.
49. Schnitzbauer AA, Lang SA, Goessmann H, et al. Right portal vein ligation combined with in situ splitting induces rapid left lateral liver lobe hypertrophy enabling 2-staged extended right hepatic resection in small-for-size settings. Ann Surg. 2012;255:405–414.
50. Dahm F, Georgiev P, Clavien PA. Small-for-size syndrome after partial liver transplantation: definition, mechanisms of disease and clinical implications. Am J Transplant. 2005;5:2605–2610.
51. Man K, Lo CM, Ng IO, et al. Liver transplantation in rats using small-for-size grafts: a study of hemodynamic and morphological changes. Arch Surg. 2001;136:280–285.
52. Oya H, Sato Y, Yamamoto S, et al. Surgical procedures for decompression of excessive shear stress in small-for-size living donor liver transplantation—new hepatic vein reconstruction. Transpl Proc. 2005;37:1108–1111.
53. Man K, Shih KC, Ng KT, et al. Molecular signature linked to acute phase injury and tumor invasiveness in small-for-size liver grafts. Ann Surg. 2010;251:1154–1161.
54. Busuttil RW, Tanaka K. The utility of marginal donors in liver transplantation. Liver Transpl. 2003;9:651–663.
55. Oldani G, Crowe LA, Orci LA, et al. Pre-retrieval reperfusion decreases cancer recurrence after rat ischemic liver graft transplantation. J Hepatol. 2014 (Epub ahead of print). doi:10.1016/j.jhep.2014.03.036.
56. Nijkamp MW, Hoogwater FJ, Steller EJ, et al. CD95 is a key mediator of invasion and accelerated outgrowth of mouse colorectal liver metastases following radiofrequency ablation. J Hepatol. 2010;53:1069–1077.
57. Giuliante F, Ardito F, Pulitano C, et al. Does hepatic pedicle clamping affect disease-free survival following liver resection for colorectal metastases? Ann Surg. 2010;252:1020–1026.
58. Xia F, Lau WY, Xu Y, Wu L, Qian C, Bie P. Does hepatic ischemia-reperfusion injury induced by hepatic pedicle clamping affect survival after partial hepatectomy for hepatocellular carcinoma? World J Surg. 2013;37:192–201.
59. Ferrero A, Russolillo N, Vigano L, Lo Tesoriere R, Muratore A, Capussotti L. Does Pringle maneuver affect survival in patients with colorectal liver metastases? World J Surg. 2010;34:2418–2425.
60. Matsuda A, Miyashita M, Matsumoto S, et al. Hepatic pedicle clamping does not worsen survival after hepatic resection for colorectal liver metastasis: results from a systematic review and meta-analysis. Ann Surg Oncol. 2013;20:3771–3778.
61. Xiaobin F, Shuguo Z, Jian Z, et al. Effect of the pringle maneuver on tumor recurrence of hepatocellular carcinoma after curative resection (EPTRH): a randomized, prospective, controlled multicenter trial. BMC Cancer. 2012;12:340.
62. van der Bilt JD, Kranenburg O, Nijkamp MW, et al. Ischemia/reperfusion accelerates the outgrowth of hepatic micrometastases in a highly standardized murine model. Hepatology. 2005;42:165–175.
63. Wong KH, Hamady ZZ, Malik HZ, Prasad R, Lodge JP, Toogood GJ. Intermittent Pringle manoeuvre is not associated with adverse long-term prognosis after resection for colorectal liver metastases. Br J Surg. 2008;95:985–989.
64. Makino I, Chijiiwa K, Kondo K, Ohuchida J, Kai M. Prognostic benefit of selective portal vein occlusion during hepatic resection for hepatocellular carcinoma. Surgery. 2005;137:626–631.
65. Yang Y, Fu SY, Lau WY, et al. Selective main portal vein clamping to minimize the risk of recurrence after curative liver resection for hepatocellular carcinoma. Hepatogastroenterology. 2012;59:1560–1565.
66. Grant RC, Sandhu L, Dixon PR, Greig PD, Grant DR, McGilvray ID. Living vs. deceased donor liver transplantation for hepatocellular carcinoma: a systematic review and meta-analysis. Clin Transplant. 2013;27:140–147.
67. Mathur A, Franco ES, Leone JP, et al. Obesity portends increased morbidity and earlier recurrence following liver transplantation for hepatocellular carcinoma. HPB (Oxford). 2013;15:504–510.
68. Jay C, Ladner D, Wang E, et al. A comprehensive risk assessment of mortality following donation after cardiac death liver transplant—an analysis of the national registry. J Hepatol. 2011;55:808–813.
69. Croome KP, Wall W, Chandok N, Beck G, Marotta P, Hernandez-Alejandro R. Inferior survival in liver transplant recipients with hepatocellular carcinoma receiving donation after cardiac death liver allografts. Liver Transpl. 2013;19:1214–1223.
70. Fong Y, Bentrem DJ. CASH (chemotherapy-associated steatohepatitis) costs. Ann Surg. 2006;243:8–9.
71. Vauthey JN, Pawlik TM, Ribero D, et al. Chemotherapy regimen predicts steatohepatitis and an increase in 90-day mortality after surgery for hepatic colorectal metastases. J Clin Oncol. 2006;24:2065–2072.
72. Hribal ML, Procopio T, Petta S, et al. Insulin-like growth factor-I, inflammatory proteins, and fibrosis in subjects with nonalcoholic fatty liver disease. J Clin Endocrinol Metab. 2013;98:E304–E308.
73. Ijaz S, Yang W, Winslet MC, Seifalian AM. Impairment of hepatic microcirculation in fatty liver. Microcirculation. 2003;10:447–456.
74. Fromenty B, Berson A, Pessayre D. Microvesicular steatosis and steatohepatitis: role of mitochondrial dysfunction and lipid peroxidation. J Hepatol. 1997;26:13–22.
75. VanSaun MN, Lee IK, Washington MK, Matrisian L, Gorden DL. High fat diet induced hepatic steatosis establishes a permissive microenvironment for colorectal metastases and promotes primary dysplasia in a murine model. Am J Pathol. 2009;175:355–364.
76. Hamady ZZ, Rees M, Welsh FK, et al. Fatty liver disease as a predictor of local recurrence following resection of colorectal liver metastases. Br J Surg. 2013;100:820–826.
77. Pannen BH, Al-Adili F, Bauer M, Clemens MG, Geiger KK. Role of endothelins and nitric oxide in hepatic reperfusion injury in the rat. Hepatology. 1998;27:755–764.
78. Vollmar B, Glasz J, Leiderer R, Post S, Menger MD. Hepatic microcirculatory perfusion failure is a determinant of liver dysfunction in warm ischemia-reperfusion. Am J Pathol. 1994;145:1421–1431.
79. Carmeliet P, Dor Y, Herbert JM, et al. Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature. 1998;394:485–490.
80. Ryan HE, Poloni M, McNulty W, et al. Hypoxia-inducible factor-1alpha is a positive factor in solid tumor growth. Cancer Res. 2000;60:4010–4015.
81. Stoeltzing O, McCarty MF, Wey JS, et al. Role of hypoxia-inducible factor 1alpha in gastric cancer cell growth, angiogenesis, and vessel maturation. J Natl Cancer Inst. 2004;96:946–956.
82. van der Bilt JD, Soeters ME, Duyverman AM, et al. Perinecrotic hypoxia contributes to ischemia/reperfusion-accelerated outgrowth of colorectal micrometastases. Am J Pathol. 2007;170:1379–1388.
83. Nijkamp MW, Hoogwater FJ, Govaert KM, et al. A role for CD95 signaling in ischemia/reperfusion-induced invasion and outgrowth of colorectal micrometastases in mouse liver. J Surg Oncol. 2011;104:198–204.
84. Fan F, Wey JS, McCarty MF, et al. Expression and function of vascular endothelial growth factor receptor-1 on human colorectal cancer cells. Oncogene. 2005;24:2647–2653.
85. Witte D, Thomas A, Ali N, Carlson N, Younes M. Expression of the vascular endothelial growth factor receptor-3 (VEGFR-3) and its ligand VEGF-C in human colorectal adenocarcinoma. Anticancer Res. 2002;22:1463–1466.
86. Li T, Zhu Y, Qin CY, et al. Expression and prognostic significance of vascular endothelial growth factor receptor 1 in hepatocellular carcinoma. J Clin Pathol. 2012;65:808–814.
87. Bates RC, Goldsmith JD, Bachelder RE, et al. Flt-1-dependent survival characterizes the epithelial-mesenchymal transition of colonic organoids. Current biology (CB). 2003;13:1721–1727.
88. Chung J, Bachelder RE, Lipscomb EA, Shaw LM, Mercurio AM. Integrin (alpha 6 beta 4) regulation of eIF-4E activity and VEGF translation: a survival mechanism for carcinoma cells. J Cell Biol. 2002;158:165–174.
89. Masood R, Cai J, Zheng T, Smith DL, Hinton DR, Gill PS. Vascular endothelial growth factor (VEGF) is an autocrine growth factor for VEGF receptor-positive human tumors. Blood. 2001;98:1904–1913.
90. Mercurio AM, Lipscomb EA, Bachelder RE. Non-angiogenic functions of VEGF in breast cancer. J Mammary Gland Biol Neoplasia. 2005;10:283–290.
91. Alexiou D, Karayiannakis AJ, Syrigos KN, et al. Serum levels of E-selectin, ICAM-1 and VCAM-1 in colorectal cancer patients: correlations with clinicopathological features, patient survival and tumour surgery. Eur J Cancer. 2001;37:2392–2397.
92. King JA, Ofori-Acquah SF, Stevens T, Al-Mehdi AB, Fodstad O, Jiang WG. Activated leukocyte cell adhesion molecule in breast cancer: prognostic indicator. Breast Cancer Res (BCR). 2004;6:R478–R487.
93. Yoong KF, McNab G, Hubscher SG, Adams DH. Vascular adhesion protein-1 and ICAM-1 support the adhesion of tumor-infiltrating lymphocytes to tumor endothelium in human hepatocellular carcinoma. J Immunol. 1998;160:3978–3988.
94. Afshari A, Wetterslev J, Brok J, Møller AM. Antithrombin III for critically ill patients. Cochrane Database Syst Rev. 2008;CD005370. doi:10.1002/14651858.CD005370.pub2.
95. Colletti LM, Kunkel SL, Walz A, et al. The role of cytokine networks in the local liver injury following hepatic ischemia/reperfusion in the rat. Hepatology. 1996;23:506–514.
96. Lentsch AB, Kato A, Yoshidome H, McMasters KM, Edwards MJ. Inflammatory mechanisms and therapeutic strategies for warm hepatic ischemia/reperfusion injury. Hepatology. 2000;32:169–173.
97. Zhai Y, Shen XD, Gao F, et al. CXCL10 regulates liver innate immune response against ischemia and reperfusion injury. Hepatology. 2008;47:207–214.
98. Huang F, Geng XP. Chemokines and hepatocellular carcinoma. World J Gastroenterol (WJG). 2010;16:1832–1836.
99. Schimanski CC, Bahre R, Gockel I, et al. Dissemination of hepatocellular carcinoma is mediated via chemokine receptor CXCR4. Br J Cancer. 2006;95:210–217.
100. Zipin-Roitman A, Meshel T, Sagi-Assif O, et al. CXCL10 promotes invasion-related properties in human colorectal carcinoma cells. Cancer Res. 2007;67:3396–3405.
101. Ling CC, Ng KT, Shao Y, et al. Post-transplant endothelial progenitor cell mobilization via CXCL10/CXCR3 signaling promotes liver tumor growth. J Hepatol. 2014;60:103–109.
102. Lu P, Weaver VM, Werb Z. The extracellular matrix: a dynamic niche in cancer progression. J Cell Biol. 2012;196:395–406.
103. Zucker S, Vacirca J. Role of matrix metalloproteinases (MMPs) in colorectal cancer. Cancer Metastasis Rev. 2004;23:101–117.
104. Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer. 2002;2:161–174.
105. Chen CF, Leu FJ, Chen HI, Wang D. Oxygen radicals and matrix metalloproteinases mediate reperfusion liver injury. Transpl Proc. 2005;37:4547–4549.
106. de Rougemont O, Lehmann K, Clavien PA. Preconditioning, organ preservation, and postconditioning to prevent ischemia-reperfusion injury to the liver. Liver Transpl. 2009;15:1172–1182.
107. Sugawara Y, Kubota K, Ogura T, et al. Protective effect of prostaglandin E1 against ischemia/reperfusion-induced liver injury: results of a prospective, randomized study in cirrhotic patients undergoing subsegmentectomy. J Hepatol. 1998;29:969–976.
108. Beck-Schimmer B, Breitenstein S, Urech S, et al. A randomized controlled trial on pharmacological preconditioning in liver surgery using a volatile anesthetic. Ann Surg. 2008;248:909–918.
109. van den Broek MA, Bloemen JG, Dello SA, van de Poll MC, Olde Damink SW, Dejong CH. Randomized controlled trial analyzing the effect of 15 or 30 min intermittent Pringle maneuver on hepatocellular damage during liver surgery. J Hepatol. 2011;55:337–345.