Ischemia/reperfusion accelerates the outgrowth of hepatic micrometastases in a highly standardized murine model

Hepatology

Volumn 42, Issue 1, 2005, Pages 165-175

  Van Der Bilt, Jarmila D W ^a   Kranenburg, Onno ^a   Nijkamp, Maarten W ^a   Smakman, Niels ^a   Veenendaal, Liesbeth M ^a   Te Velde, Elisabeth A ^a   Voest, Emile E ^a   Van Diest, Paul J ^a   Borel Rinkes, Inne H M ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; ANTIOXIDANT; ASCORBIC ACID; GLUTATHIONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CARCINOMA CELL; COLORECTAL CANCER; CONTROLLED STUDY; HEART INFARCTION PREVENTION; INFLAMMATORY CELL; LIVER BLOOD FLOW; LIVER FUNCTION; LIVER ISCHEMIA; LIVER METASTASIS; LIVER PERFUSION; LIVER SURGERY; LIVER TUMOR; MOUSE; NONHUMAN; PRIORITY JOURNAL; STANDARDIZATION; TARGET ORGAN; TUMOR GROWTH;

ANIMALS; COLORECTAL NEOPLASMS; LIVER NEOPLASMS; MICE; MODELS, ANIMAL; NEOPLASM RECURRENCE, LOCAL; REPERFUSION INJURY;

EID: 21344466512     PISSN: 02709139     EISSN: None     Source Type: Journal    
DOI: 10.1002/hep.20739     Document Type: Article

References (50)

1. Bengmark S, Hafstrom L. The natural history of primary and secondary malignant tumors of the liver. I. The prognosis for patients with hepatic metastases from colonic and rectal carcinoma by laparotomy. Cancer 1969; 23:198-202.
2. Selzner M, Clavien PA. Resection of hepatic tumors: special emphasis on neoadjuvant and adjuvant therapy. In: Clavien PA, ed. Malignant Liver Tumors: Current and Emerging Therapies. Sudbury, MA: Jones and Bartlett Publishers, 2004:153-169.
3. Kooby DA, Stockman J, Ben Porat L, Gonen M, Jarnagin WR, Dematteo RP, 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.
4. Jarrar D, Chaudry IH, Wang P. Organ dysfunction following hemorrhage and sepsis: mechanisms and therapeutic approaches [Review]. Int J Mol Med 1999;4:575-583.
5. Abdalla EK, Noun R, Belghiti J. Hepatic vascular occlusion: which technique? Surg Clin North Am 2004;84:563-585.
6. Man K, Fan ST, Ng IO, Lo CM, Liu CL, Wong J. Prospective evaluation of Pringle maneuver in hepatectomy for liver tumors by a randomized study. Ann Surg 1997;226:704-711.
7. Grace PA. Ischaemia-reperfusion injury. Br J Surg 1994;81:637-647.
8. Jaeschke H. Molecular mechanisms of hepatic ischemia-reperfusion injury and preconditioning. Am J Physiol Gastrointest Liver Physiol 2003;284: G15-G26.
9. Ku Y, Kusunoki N, Shiotani M, Maeda I, Iwasaki T, Tominaga M, et al. Stimulation of haematogenous liver metastases by ischaemia-reperfusion in rats. Eur J Surg 1999;165:801-807.
10. Doi K, Horiuchi T, Uchinami M, Tabo T, Kimura N, Yokomachi J, et al. Hepatic ischemia-reperfusion promotes liver metastasis of colon cancer. J Surg Res 2002;105:243-247.
11. Weitz J, Koch M, Kienle P, Schrodel A, Willeke F, Benner A, et al. Detection of hematogenic tumor cell dissemination in patients undergoing resection of liver metastases of colorectal cancer. Ann Surg 2000;232:66-72.
12. Finlay IG, McArdle CS. Occult hepatic metastases in colorectal carcinoma. Br J Surg 1986;73:732-735.
13. Linnemann U, Schimanski CC, Gebhardt C, Berger MR. Prognostic value of disseminated colorectal tumor cells in the liver: results of follow-up examinations. Int J Colorectal Dis 2004;19:380-386.
14. Metzger H, Heuber-Metzger S. The hypoxic response to hypovolemia. Adv Exp Med Biol 1984;180:599-607.
15. Heijnen BH, Elkhaloufi Y, Straatsburg IH, Van Gulik TM. Influence of acidosis and hypoxia on liver ischemia and reperfusion injury in an in vivo rat model. J Appl Physiol 2002;93:319-323.
16. Heijnen BH, van Veen SQ, Straatsburg IH, Van Gulik TM. Pronounced effect of minor changes in body temperature on ischemia and reperfusion injury in rat liver. J Appl Physiol 2001;91:265-268.
17. 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.
18. Selzner N, Rudiger H, Graf R, Clavien PA. Protective strategies against ischemic injury of the liver. Gastroenterology 2003;125:917-936.
19. Fan C, Zwacka RM, Engelhardt JF. Therapeutic approaches for ischemia/reperfusion injury in the liver. J Mol Med 1999;77:577-592.
20. Teoh N, Dela PA, Farrell G. Hepatic ischemic preconditioning in mice is associated with activation of NF-kappaB, p38 kinase, and cell cycle entry. HEPATOLOGY 2002;36:94-102.
21. Yadav SS, Sindram D, Perry DK, Clavien PA. Ischemic preconditioning protects the mouse liver by inhibition of apoptosis through a caspase-dependent pathway. HEPATOLOGY 1999;30:1223-1231.
22. Clavien PA, Selzner M, Rudiger HA, Graf R, Kadry Z, Rousson V, et al. A prospective randomized study in 100 consecutive patients undergoing major liver resection with versus without ischemic preconditioning. Ann Surg 2003;238:843-850.
23. Schauer RJ, Gerbes AL, Vonier D, op den Winkel M, Fraunberger P, Bilzer M. Induction of cellular resistance against Kupffer cell-derived oxidant stress: a novel concept of hepatoprotection by ischemic preconditioning. HEPATOLOGY 2003;37:286-295.
24. Isozaki H, Adam R, Gigou M, Szekely AM, Shen M, Bismuth H. Experimental study of the protective effect of intermittent hepatic pedicle clamping in the rat. Br J Surg 1992;79:310-313.
25. Belghiti J, Noun R, Malafosse R, Jagot P, Sauvanet A, Pierangeli F, et al. Continuous versus intermittent portal triad clamping for liver resection: a controlled study. Ann Surg 1999;229:369-375.
26. Chiappa A, Makuuchi M, Zbar AP, Biella F, Vezzoni A, Pozzi S, et al. Comparison of continuous versus intermittent hepatic pedicle clamping in an experimental model. Hepatogastroenterology 2001;48:1416-1420.
27. Marubayashi S, Dohi K, Sugino K, Kawasaki T. The protective effect of administered alpha-tocopherol against hepatic damage caused by ischemia-reperfusion or endotoxemia. Ann N Y Acad Sci 1989;570:208-218.
28. Ozaki M, Fuchinoue S, Teraoka S, Ota K. The in vivo cytoprotection of ascorbic acid against ischemia/reoxygenation injury of rat liver. Arch Biochem Biophys 1995;318:439-445.
29. Seo MY, Lee SM. Protective effect of low dose of ascorbic acid on hepatobiliary function in hepatic ischemia/reperfusion in rats. J Hepatol 2002; 36:72-77.
30. Taha MO, Souza HS, Carvalho CA, Fagundes DJ, Simoes MJ, Novo NF, et al. Cytoprotective effects of ascorbic acid on the ischemia-reperfusion injury of rat liver. Transplant Proc 2004;36:296-300.
31. Cerwenka H, Bacher H, Werkgartner G, El Shabrawi A, Quehenberger F, Hauser H, et al. Antioxidant treatment during liver resection for alleviation of ischemia-reperfusion injury. Hepatogastroenterology 1998;45:777-782.
32. Giakoustidis D, Papageorgiou G, Iliadis S, Kontos N, Kostopoulou E, Papachrestou A, et al. Intramuscular administration of very high dose of alpha-tocopherol protects liver from severe ischemia/reperfusion injury. World J Surg 2002;26:872-877.
33. Drixler TA, Borel Rinkes IH, Ritchie ED, van Vroonhoven TJ, Gebbink MF, Voest EE. Continuous administration of angiostatin inhibits accelerated growth of colorectal liver metastases after partial hepatectomy. Cancer Res 2000;60:1761-1765.
34. te Velde EA, Vogten JM, Gebbink MF, Van Gorp JM, Voest EE, Borel Rinkes IH. Enhanced antitumour efficacy by combining conventional chemotherapy with angiostatin or endostatin in a liver metastasis model. Br J Surg 2002;89:1302-1309.
35. Horiuchi T, Muraoka R, Tabo T, Uchinami M, Kimura N, Tanigawa N. Optimal cycles of hepatic ischemia and reperfusion for intermittent pedicle clamping during liver surgery. Arch Surg 1995;130:754-758.
36. Baker MA, Cerniglia GJ, Zaman A. Microtiter plate assay for the measurement of glutathione and glutathione disulfide in large numbers of biological samples. Anal Biochem 1990;190:360-365.
37. Yoong KF, Afford SC, Randhawa S, Hubscher SG, Adams DH. Fas/Fas ligand interaction in human colorectal hepatic metastases: a mechanism of hepatocyte destruction to facilitate local tumor invasion. Am J Pathol 1999;154:693-703.
38. McCord JM. Oxygen-derived free radicals in postischemic tissue injury. N Engl J Med 1985;312:159-163.
39. O'Reilly MS, Holmgren L, Chen C, Folkman J. Angiostatin induces and sustains dormancy of human primary tumors in mice. Nat Med 1996;2: 689-692.
40. Fisher B, Fisher ER. Experimental evidence in support of the dormant tumor cell. Science 1959;130:918-919.
41. McNamara DA, Harmey JH, Walsh TN, Redmond HP, Bouchier-Hayes DJ. Significance of angiogenesis in cancer therapy. Br J Surg 1998;85: 1044-1055.
42. van der Bilt JD, Borel Rinkes IH. Surgery and angiogenesis. Biochim Biophys Acta 2004;1654:95-104.
43. Panis Y, Ribeiro J, Chretien Y, Nordlinger B. Dormant liver metastases: an experimental study. Br J Surg 1992;79:221-223.
44. Jaeschke H, Farhood A. Kupffer cell activation after no-flow ischemia versus hemorrhagic shock. Free Radic Biol Med 2002;33:210-219.
45. Jaeschke H, Smith CW. Mechanisms of neutrophil-induced parenchymal cell injury. J Leukoc Biol 1997;61:647-653.
46. Menger MD, Richter S, Yamauchi J, Vollmar B. Role of microcirculation in hepatic ischemia/reperfusion injury. Hepatogastroenterology 1999; 46(Suppl 2):1452-1457.
47. Harris AL. Hypoxia-a key regulatory factor in tumour growth. Nat Rev Cancer 2002;2:38-47.
48. Brahimi-Horn C, Berra E, Pouyssegur J. Hypoxia: the tumor's gateway to progression along the angiogenic pathway. Trends Cell Biol 2001;11:S32-S36.
49. Vajdova K, Heinrich S, Tian Y, Graf R, Clavien PA. Ischemic preconditioning and intermittent clamping improve murine hepatic microcirculation and Kupffer cell function after ischemic injury. Liver Transpl 2004; 10:520-528.
50. Rudiger HA, Kang KJ, Sindram D, Riehle HM, Clavien PA. Comparison of ischemic preconditioning and intermittent and continuous inflow occlusion in the murine liver. Ann Surg 2002;235:400-407.