Abstract
Ischemia—Reperfusion injury of the intestine is a significant problem in abdominal aortic aneurysm surgery, small bowel transplantation, cardiopulmonary bypass, strangulated hernias, and neonatal necrotizing enterocolitis. It can also occur as a consequence of collapse of systemic circulation, as in hypovolemic and septic shock. It is associated with a high morbidity and mortality. This article is a comprehensive review of the current status of the molecular biology and the strategies to prevent Ischemia—Reperfusion injury of the intestine. Various treatment modalities have successfully been applied to attenuate reperfusion injury in animal models of reperfusion injury of the intestine. Ischemic preconditioning has been found to be the most promising strategy against reperfusion injury during the last few years, appearing to increase the tolerance of the intestine to reperfusion injury. Although ischemic preconditioning has been shown to be beneficial in the human heart and the liver, prospective controlled studies in humans involving ischemic preconditioning of the intestine are lacking. Research focused on the application of novel drugs that can mimic the effects of ischemic preconditioning to manipulate the cellular events during reperfusion injury of the intestine is required.
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REFERENCES
Koike K, Moore FA, Moore EE, Read RA, Carl VS, Banerjee A: Gut ischemia mediates lung injury by a xanthine oxidase-dependent neutrophil mechanism. J Surg Res 54(5):469–473, 1993
Collard CD, Gelman S: Pathophysiology, clinical manifestations, and prevention of ischemia-reperfusion injury. Anesthesiology 94(6):1133–1138, 2001
Moore EE, Moore FA, Franciose RJ, Kim FJ, Biffl WL, Banerjee A: The postischemic gut serves as a priming bed for circulating neutrophils that provoke multiple organ failure. J Trauma 37(6):881–887, 1994
Swank GM, Deitch EA: Role of the gut in multiple organ failure: Bacterial translocation and permeability changes. World J Surg 20(4):411–417, 1996
Stallion A, Kou TD, Miller KA, Dahms BB, Dudgeon DL, Levine AD: IL-10 is not protective in intestinal ischemia reperfusion injury. J Surg Res 105(2):145–152, 2002
Granger DN, Hollwarth ME, Parks DA: Ischemia-reperfusion injury: Role of oxygen-derived free radicals. Acta Physiol Scand Suppl 548:47–63, 1986
Yamamoto S, Tanabe M, Wakabayashi G, Shimazu M, Matsumoto K, Kitajima M: The role of tumor necrosis factor-alpha and interleukin-1 beta in ischemia-reperfusion injury of the rat small intestine. J Surg Res 99(1):134–141, 2001
Kong SE, Blennerhassett LR, Heel KA, McCauley RD, Hall JC: Ischaemia-reperfusion injury to the intestine. Aust NZ J Surg 68(8):554–561, 1998
Takeyoshi I, Zhang S, Nakamura K, Ikoma A, Zhu Y, Starzl TE, Todo S: Effect of ischemia on the canine large bowel: Acomparison with the small intestine. J Surg Res 62(1):41–48, 1996
Hinnebusch BF, Ma Q, Henderson JW, Siddique A, Archer SY, Hodin RA: Enterocyte response to ischemia is dependent on differentiation state. J Gastrointest Surg 6(3):403–409, 2002
Molmenti EP, Ziambaras T, Perlmutter DH: Evidence for an acute phase response in human intestinal epithelial cells. J Biol Chem 268(19):14116–14124, 1993
Wang Q, Meyer TA, Boyce ST, Wang JJ, Sun X, Tiao G, Fischer JE, Hasselgren PO: Endotoxemia in mice stimulates production of complement C3 and serum amyloid A in mucosa of small intestine. Am J Physiol 275(5, Pt 2):R1584–R1592, 1998
Zamir O, Hasselgren PO, Higashiguchi T, Frederick JA, Fischer JE: Effect of sepsis or cytokine administration on release of gut peptides. Am J Surg 163(1):181–185, 1992
Mester MD, Tompkins MD, Gelfand MD, Dinarello MD: Intestinal production of interleukin-1[alpha] during endotoxemia in the mouse. J Surg Res 54(6):584–591, 1993
Meyer TA, Wang J, Tiao GM, Ogle CK, Fischer JE, Hasselgren PO: Sepsis and endotoxemia stimulate intestinal interleukin-6 production. Surgery 118(2):336–342, 1995
Jassem W, Fuggle SV, Rela M, Koo DD, Heaton ND: The role of mitochondria in ischemia/reperfusion injury. Transplantation 73(4):493–499, 2002
Carden DL and Granger DN: Pathophysiology of ischaemia-reperfusion injury. J Pathol 190(3):255–266, 2000
Ogle CK, Mao JX, Wu JZ, Ogle JD, Alexander JW: The 1994 Lindberg Award. The production of tumor necrosis factor, interleukin-1, interleukin-6, and prostaglandin E2 by isolated enterocytes and gut macrophages: Effect of lipopolysaccharide and thermal injury. J Burn Care Rehabil 15(6):470–477, 1994
Kuenzler KA, Pearson PY, Schwartz MZ: Interleukin-11 enhances intestinal absorptive function after ischemia-reperfusion injury. J Pediatr Surg 37(3):457–459, 2002
Prasad R, Alavi K, Schwartz MZ: GLP-2alpha accelerates recovery of mucosal absorptive function after intestinal ischemia/reperfusion. J Pediatr Surg 36(4):570–572, 2001
Rajeevprasad R, Alavi K, Schwartz MZ: Glucagonlike peptide-2 analogue enhances intestinal mucosal mass and absorptive function after ischemia-reperfusion injury. J Pediatr Surg 35(11):1537–1539, 2000
Scolapio JS, Fleming CR: Short bowel syndrome. Gastroenterol Clin North Am 27(2):467–479, viii, 1998
Sileri P, Morini S, Schena S, Rastellini C, Abcarian H, Benedetti E, Cicalese L: Intestinal ischemia/reperfusion injury produces chronic abnormalities of absorptive function. Transplant Proc 34(3):984, 2002
Van Leeuwen PA, Boermeester MA, Houdijk AP, Ferwerda CC, Cuesta MA, Meyer S, Wesdorp RI: Clinical significance of translocation. Gut 35(Suppl 1):S28–S34, 1994
Cicalese L, Sileri P, Green M, Abu-Elmagd K, Kocoshis S, Reyes J: Bacterial translocation in clinical intestinal transplantation. Transplantation 71(10):1414–1417, 2001
Aksoyek S, Cinel I, Avlan D, Cinel L, Ozturk C, Gurbuz P, Nayci A, Oral U: Intestinal ischemic preconditioning protects the intestine and reduces bacterial translocation. Shock 18(5):476–480, 2002
Iijima S, Shou J, Naama H, Calvano SE, Daly JM: Beneficial effect of enteral glycine in intestinal ischemia/reperfusion injury. J Gastrointest Surg 1(1):53–60, 1997
Xia G, Martin AE, Michalsky MP, Besner GE: Heparin-binding EGF-like growth factor preserves crypt cell proliferation and decreases bacterial translocation after intestinal ischemia/reperfusion injury. J Pediatr Surg 37(7):1081 [Discussion], 2002
Berg RD: Bacterial translocation from the gastrointestinal tract. Adv Exp Med Biol 473:11–30, 1999
Ceppa EP, Fuh KC, Bulkley GB: Mesenteric hemodynamic response to circulatory shock. Curr Opin Crit Care 9(2):127–132, 2003
Koksoy C, Kuzu MA, Kuzu I, Ergun H, Gurhan I: Role of tumour necrosis factor in lung injury caused by intestinal ischaemia-reperfusion. Br J Surg 88(3):464–468, 2001
Xiao F, Eppihimer MJ, Young JA, Nguyen K, Carden DL: Lung neutrophil retention and injury after intestinal ischemia/reperfusion. Microcirculation 4(3):359–367, 1997
Marshall JC: The gut as a potential trigger of exercise-induced inflammatory responses. Can J Physiol Pharmacol 76(5):479–484, 1998
Parks DA, Williams TK, Beckman JS: Conversion of xanthine dehydrogenase to oxidase in ischemic rat intestine: A reevaluation. Am J Physiol 254(5, Pt 1):G768–G774, 1988
Meneshian A and Bulkley GB: The physiology of endothelial xanthine oxidase: From urate catabolism to reperfusion injury to inflammatory signal transduction. Microcirculation 9(3):161–175, 2002
Younes M, Schoenberg MH, Jung H, Fredholm BB, Haglund U, Schildberg FW: Oxidative tissue damage following regional intestinal ischemia and reperfusion in the cat. Res Exp Med (Berl) 184(4):259–264, 1984
Harrison R: Structure and function of xanthine oxidoreductase: Where are we now? Free Radic Biol Med 33(6):774–797, 2002
Halliwell B, Gutteridge J: Free Radicals in Biology and Medicine, 3rd ed. New York: Oxford University Press, 1999
Ozel SK, Yuksel M, Haklar G, Durakbasa CU, Dagli TE, Aktan AO: Nitric oxide and endothelin relationship in intestinal ischemia/reperfusion injury (II). Prostaglandins Leukot Essent Fatty Acids 64(4–5):253–257, 2001
Inoue A, Yanagisawa M, Kimura S, Kasuya Y, Miyauchi T, Goto K, Masaki T: The human endothelin family: three structurally and pharmacologically distinct isopeptides predicted by three separate genes. Proc Natl Acad Sci USA 86(8):2863–2867, 1989
Yanagisawa M, Kurihara H, Kimura S, Tomobe Y, Kobayashi M, Mitsui Y, Yazaki Y, Goto K, Masaki T: A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 332(6163):411–415, 1988
Clozel M, Gray GA, Breu V, Loffler BM, Osterwalder R: The endothelin ETB receptor mediates both vasodilation and vasoconstriction in vivo. Biochem Biophys Res Commun 186(2):867–873, 1992
Anadol AZ, Bayram O, Dursun A, Ercan S: Role of endogenous endothelin peptides in intestinal ischemia-reperfusion injury in rats. Prostaglandins Leukot Essent Fatty Acids 59(4):279–283, 1998
Andrasi TB, Kekesi V, Blazovics A, Dobi I, Szabo G, Juhasz-Nagy A: ET(A) receptor blockade protects the small intestine against is-chaemia/reperfusion injury in dogs via an enhancement of antioxidant defences. Clin Sci (Lond) 103 (Suppl 48):59S–63S, 2002
Buyukgebiz O, Aktan AO, Yegen C, Yalcin AS, Haklar G, Yalin R, Ercan ZS: Captopril increases endothelin serum concentrations and preserves intestinal mucosa after mesenteric ischemia-reperfusion injury. Res Exp Med (Berl) 194(6):339–348, 1994
Oktar BK, Gulpinar MA, Bozkurt A, Ghandour S, Cetinel S, Moini H, Yegen BC, Bilsel S, Granger DN, Kurtel H: Endothelin receptor blockers reduce I/R-induced intestinal mucosal injury: Role of blood flow. Am J Physiol Gastrointest Liver Physiol 282(4):G647–G655, 2002
Wolfard A, Szalay L, Kaszaki 1J, Sahin-Toth G, Vangel R, Balogh A, Boros M: Dynamic in vivo observation of villus microcirculation during small bowel autotransplantation: Effects of endothelin—A receptor inhibition. Transplantation 73(9):1511–1513, 2002
Oktar BK, Coskun T, Bozkurt A, Yegen BC, Yuksel M, Haklar G, Bilsel S, Aksungar FB, Cetinel U, Granger DN, Kurtel H: Endothelin-1-induced PMN infiltration and mucosal dysfunction in the rat small intestine. Am J Physiol Gastrointest Liver Physiol 279(3):G483–G491, 2000
Tsuruma T, Yagihashi A, Matsuno T, Zou XM, Asanuma K, Sasaki K, Hirata K: The heat-shock protein 70 family reduces ischemia/reperfusion injury in small intestine. Transplant Proc 28(5):2629–2630, 1996
Hotchkiss R, Nunnally I, Lindquist S, Taulien J, Perdrizet G, Karl I: Hyperthermia protects mice against the lethal effects of endotoxin. Am J Physiol 265(6, Pt 2):R1447–R1457, 1993
Ryan AJ, Flanagan SW, Moseley PL, Gisolfi CV: Acute heat stress protects rats against endotoxin shock. J Appl Physiol 73(4):1517–1522, 1992
Fleming SD, Starnes BW, Kiang JG, Stojadinovic A, Tsokos GC, Shea-Donohue T: Heat stress protection against mesenteric I/R-induced alterations in intestinal mucosa in rats. J Appl Physiol 92(6):2600–2607, 2002
Stojadinovic A, Kiang J, Smallridge R, Galloway R, Shea-Donohue T: Induction of heat-shock protein 72 protects against ischemia/reperfusion in rat small intestine. Gastroenterology 109(2):505–515, 1995
Tsuruma T, Yagihashi A, Watanabe N, Yajima T, Kameshima H, Araya J, Hirata K: Heat-shock protein-73 protects against small intestinal warm ischemia-reperfusion injury in the rat. Surgery 125(4):385–395, 1999
Hayward R and Lefer AM: Time course of endothelial-neutrophil interaction in splanchnic artery ischemia-reperfusion. AmJ Physiol 275(6, Pt 2):H2080–H2086, 1998
Hierholzer C, Kalff JC, Audolfsson G, Billiar TR, Tweardy DJ, Bauer AJ: Molecular and functional contractile sequelae of rat intestinal ischemia/reperfusion injury. Transplantation 68(9):1244–1254, 1999
Cooper D, Russell J, Chitman KD, Williams MC, Wolf RE, Granger DN: Leukocyte dependence of platelet adhesion in postcapillary venules. Am J Physiol Heart Circ Physiol 286(5):H1895–H1900, 2004
Mbachu EM, Klein LV, Rubin BB, Lindsay TF: A monoclonal antibody against cytokine-induced neutrophil chemoattractant attenuates injury in the small intestine in a model of ruptured abdominal aortic aneurysm. J Vasc Surg 39(5):1104–1111, 2004
Massberg S, Gonzalez AP, Leiderer R, Menger MD, Messmer K: In vivo assessment of the influence of cold preservation time on microvascular reperfusion injury after experimental small bowel transplantation. Br J Surg 85(1):127–133, 1998
Sisley AC, Desai T, Harig JM, Gewertz BL: Neutrophil depletion attenuates human intestinal reperfusion injury. J Surg Res 57(1):192–196, 1994
Granger DN, Korthuis RJ: Physiologic mechanisms of postischemic tissue injury. Annu Rev Physiol 57:311–332, 1995
Naito Y, Takagi T, Uchiyama K, Handa O, Tomatsuri N, Imamoto E, Kokura S, Ichikawa H, Yoshida N, Yoshikawa T: Suppression of intestinal ischemia-reperfusion injury by a specific peroxisome proliferator-activated receptor-gamma ligand, pioglitazone, in rats. Redox Rep 7(5):294–299, 2002
Grisham MB, Granger DN, Lefer DJ: Modulation of leukocyte-endothelial interactions by reactive metabolites of oxygen and nitrogen: Relevance to ischemic heart disease. Free Radic Biol Med 25(4–5):404–433, 1998
Granger DN: Role of xanthine oxidase and granulocytes in ischemia-reperfusion injury. Am J Physiol 255(6, Pt 2):H1269–H1275, 1988
Panes J, Perry M, Granger DN: Leukocyte-endothelial cell adhesion: Avenues for therapeutic intervention. Br J Pharmacol 126(3):537–550, 1999
Riaz AA, Wan MX, Schaefer T, Schramm R, Ekberg H, Menger MD, Jeppsson B, Thorlacius H: Fundamental and distinct roles of P-selectin and LFA-1 in ischemia/reperfusion-induced leukocyte-endothelium interactions in the mouse colon. Ann Surg 236(6):777–784, 2002
Carden DL, Smith JK, Korthuis RJ: Neutrophil-mediated microvascular dysfunction in postischemic canine skeletal muscle. Role of granulocyte adherence. Circ Res 66(5):1436–1444, 1990
Weiss SJ: Tissue destruction by neutrophils. N Engl J Med 320(6):365–376, 1989
Bagge U, Amundson B, Lauritzen C: White blood cell deformability and plugging of skeletal muscle capillaries in hemorrhagic shock. Acta Physiol Scand 108(2):159–163, 1980
Nalini S, Mathan MM, Balasubramanian KA: Oxygen free radical induced damage during intestinal ischemia/reperfusion in normal and xanthine oxidase deficient rats. Mol Cell Biochem 124(1):59–66, 1993
Albrecht EW, Stegeman CA, Heeringa P, Henning RH, van Goor H: Protective role of endothelial nitric oxide synthase. J Pathol 199(1):8–17, 2003
Qu XW, Wang H, De Plaen IG, Rozenfeld RA, Hsueh W: Neuronal nitric oxide synthase (NOS) regulates the expression of inducible NOS in rat small intestine via modulation of nuclear factor kappa B. FASEB J 15(2):439–446, 2001
Hasan K, Heesen BJ, Corbett JA, McDaniel ML, Chang K, Allison W, Wolffenbuttel BH, Williamson JR, Tilton RG: Inhibition of nitric oxide formation by guanidines. Eur J Pharmacol 249(1):101–106, 1993
Naka M, Nanbu T, Kobayashi K, Kamanaka Y, Komeno M, Yanase R, Fukutomi T, Fujimura S, Seo HG, Fujiwara N, Ohuchida S, Suzuki K, Kondo K, Taniguchi N: A potent inhibitor of inducible nitric oxide synthase, ONO-1714, a cyclic amidine derivative. Biochem Biophys Res Commun 270(2):663–667, 2000
Salzman AL: Nitric oxide in the gut. New Horiz 3(2):352–364, 1995
Kubes P and McCafferty DM: Nitric oxide and intestinal inflammation. Am J Med 109(2):150–158, 2000
Suzuki Y, Deitch EA, Mishima S, Lu Q, Xu D: Inducible nitric oxide synthase gene knockout mice have increased resistance to gut injury and bacterial translocation after an intestinal ischemia-reperfusion injury. Crit Care Med 28(11):3692–3696, 2000
Cuzzocrea S, Zingarelli B, Caputi AP: Role of constitutive nitric oxide synthase and peroxynitrite production in a rat model of splanchnic artery occlusion shock. Life Sci 63(9):789–799, 1998
Wu B, Iwakiri R, Tsunada S, Utsumi H, Kojima M, Fujise T, Ootani A, Fujimoto K: iNOS enhances rat intestinal apoptosis after ischemia-reperfusion. Free Radic Biol Med 33(5):649–658, 2002
Virlos IT, Inglott FS, Williamson RC, Mathie RT: Differential expression of pulmonary nitric oxide synthase isoforms after intestinal ischemia-reperfusion. Hepatogastroenterology 50(49):31–36, 2003
Wink DA, Hanbauer I, Krishna MC, DeGraff W, Gamson J, Mitchell JB: Nitric oxide protects against cellular damage and cytotoxicity from reactive oxygen species. Proc Natl Acad Sci USA 90(21):9813–9817, 1993
Kosonen O, Kankaanranta H, Malo-Ranta U, Moilanen E: Nitric oxide-releasing compounds inhibit neutrophil adhesion to endothelial cells. Eur J Pharmacol 382(2):111–117, 1999
Gidday JM, Park TS, Shah AR, Gonzales ER: Modulation of basal and postischemic leukocyte-endothelial adherence by nitric oxide. Stroke 29(7):1423–1429, 1998
Guo JP, Murohara T, Buerke M, Scalia R, Lefer AM: Direct measurement of nitric oxide release from vascular endothelial cells. J Appl Physiol 81(2):774–779, 1996
Lefer AM, Lefer DJ: The role of nitric oxide and cell adhesion molecules on the microcirculation in ischaemia-reperfusion. Cardiovasc Res 32(4):743–751, 1996
Wink DA, Mitchell JB: Chemical biology of nitric oxide: Insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radic Biol Med 25(4–5):434–456, 1998
Gauthier TW, Davenpeck KL, Lefer AM: Nitric oxide attenuates leukocyte-endothelial interaction via P-selectin in splanchnic ischemia-reperfusion. Am J Physiol 267(4, Pt 1):G562–G568, 1994
Ito K, Ozasa H, Kojima N, Miura M, Iwa T, Senoo H, Horikawa S: Pharmacological preconditioning protects lung injury induced by intestinal ischemia/reperfusion in rat. Shock 19(5):462–468, 2003
Attuwaybi BO, Kozar RA, Moore-Olufemi SD, Sato N, Hassoun HT, Weisbrodt NW, Moore FA: Heme oxygenase-1 induction by hemin protects against gut ischemia/reperfusion injury. J Surg Res 118(1):53–57, 2004
Nakao A, Kimizuka K, Stolz DB, Neto JS, Kaizu T, Choi AM, Uchiyama T, Zuckerbraun BS, Nalesnik MA, Otterbein LE, Murase N: Carbon monoxide inhalation protects rat intestinal grafts from ischemia/reperfusion injury. AmJ Pathol 163(4):1587–1598, 2003
Squiers EC, Bruch D, Buelow R, Tice DG: Pretreatment of small bowel isograft donors with cobalt-protoporphyrin decreases preservation injury. Transplant Proc 31(1–2):585–586, 1999
Choi AM, Alam J: Heme oxygenase-1: Function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am J Respir Cell Mol Biol 15(1):9–19, 1996
Katori M, Busuttil RW, Kupiec-Weglinski JW: Heme oxygenase-1 system in organ transplantation. Transplantation 74(7):905–912, 2002
Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, Ames BN: Bilirubin is an antioxidant of possible physiological importance. Science 235(4792):1043–1046, 1987
Balla G, Jacob HS, Balla J, Rosenberg M, Nath K, Apple F, Eaton JW, Vercellotti GM: Ferritin: a cytoprotective antioxidant strategem of endothelium. J Biol Chem 267(25):18148–18153, 1992
Willis D, Moore AR, Frederick R, Willoughby DA: Heme oxygenase: A novel target for the modulation of the inflammatory response. Nat Med 2(1):87–90, 1996
Vachharajani TJ, Work J, Issekutz AC, Granger DN: Heme oxygenase modulates selectin expression in different regional vascular beds. Am J Physiol Heart Circ Physiol 278(5):H1613–H1617, 2000
Coito AJ, Buelow R, Shen XD, Amersi F, Moore C, Volk HD, Busuttil RW, Kupiec-Weglinski JW: Heme oxygenase-1 gene transfer inhibits inducible nitric oxide synthase expression and protects genetically fat Zucker rat livers from ischemia-reperfusion injury. Transplantation 74(1):96–102, 2002
Ceran C, Sonmez K, Turkyllmaz Z, Demirogullarl B, Dursun A, Duzgun E, Basaklar AC, Kale N: Effect of bilirubin in ischemia/reperfusion injury on rat small intestine. J Pediatr Surg 36(12):1764–1767, 2001
Hammerman C, Goldschmidt D, Caplan MS, Kaplan M, Bromiker R, Eidelman AI, Gartner LM, Hochman A: Protective effect of bilirubin in ischemia-reperfusion injury in the rat intestine. J Pediatr Gastroenterol Nutr 35(3):344–349, 2002
Anaya-Prado R, Toledo-Pereyra LH, Lentsch AB, Ward PA: Ischemia/reperfusion injury. J Surg Res 105(2):248–258, 2002
Zingarelli B, Sheehan M, Wong HR: Nuclear factor-kappaB as a therapeutic target in critical care medicine. Crit Care Med 31(Suppl 1):S105–S111, 2003
Siebenlist U, Franzoso G, Brown K: Structure, regulation and func-tion of NF-kappa B. Annu Rev Cell Biol 10:405–455, 1994
Collins T, Read MA, Neish AS, Whitley MZ, Thanos D, Maniatis T: Transcriptional regulation of endothelial cell adhesion molecules: NF-kappa B and cytokine-inducible enhancers. FASEB J 9(10):899–909, 1995
Barnes PJ: Nuclear factor-kappa B. Int J Biochem Cell Biol 29(6):867–870, 1997
Blackwell TS, Christman JW: The role of nuclear factor-kappa B in cytokine gene regulation. Am J Respir Cell Mol Biol 17(1):3–9, 1997
Spiecker M, Darius H, Kaboth K, Hubner F, Liao JK: Differential regulation of endothelial cell adhesion molecule expression by nitric oxide donors and antioxidants. J Leukoc Biol 63(6):732–739, 1998
Peng HB, Libby P, Liao JK: Induction and stabilization of I kappa B alpha by nitric oxide mediates inhibition of NF-kappa B. J Biol Chem 270(23):14214–14219, 1995
Austen Jr WG, Kobzik L, Carroll MC, Hechtman HB, Moore Jr FD: The role of complement and natural antibody in intestinal ischemia-reperfusion injury. Int J Immunopathol Pharmacol 16(1):1–8, 2003
Heller T, Hennecke M, Baumann U, Gessner JE, zu Vilsendorf AM, Baensch M, Boulay F, Kola A, Klos A, Bautsch W, Kohl J: Selection of a C5a receptor antagonist from phage libraries attenuating the inflammatory response in immune complex disease and ischemia/reperfusion injury. J Immunol 163(2):985–994, 1999
Kimura T, Andoh A, Fujiyama Y, Saotome T, Bamba T: A blockade of complement activation prevents rapid intestinal ischaemia-reperfusion injury by modulating mucosal mast cell degranulation in rats. Clin Exp Immunol 111(3):484–490, 1998
Wada K, Montalto MC, Stahl GL: Inhibition of complement C5 reduces local and remote organ injury after intestinal ischemia/reperfusion in the rat. Gastroenterology 120(1):126–133, 2001
Gibbs SA, Weiser MR, Kobzik L, Valeri CR, Shepro D, Hechtman HB: P-selectin mediates intestinal ischemic injury by enhancing complement deposition. Surgery 119(6):652–656, 1996
Montalto MC, Hart ML, Jordan JE, Wada K, Stahl GL: Role for complement in mediating intestinal nitric-oxide synthase-2 and superoxide dismutase expression. Am J Physiol Gastrointest Liver Physiol, 285(1):G 197–206, 2003
Hernandez LA, Grisham MB, Granger DN: A role for iron in oxidant-mediated ischemic injury to intestinal microvasculature. Am J Physiol 253(1, Pt 1):G49–G53, 1987
Lelli JL Jr, Pradhan S, Cobb LM: Prevention of postischemic injury in immature intestine by deferoxamine. J Surg Res 54(1):34–38, 1993
Richard V, Kaeffer N, Tron C, Thuillez C: Ischemic preconditioning protects against coronary endothelial dysfunction induced by ischemia and reperfusion. Circulation 89(3):1254–1261, 1994
Murry CE, Jennings RB, Reimer KA: Preconditioning with is-chemia: A delay of lethal cell injury in ischemic myocardium. Circulation 74(5):1124–1136, 1986
Koti RS, Seifalian AM, McBride AG, Yang W, Davidson BR: The relationship of hepatic tissue oxygenation with nitric oxide metabolism in ischemic preconditioning of the liver. FASEB J 16(12):1654–1656, 2002
Pang CY, Neligan P, Zhong A, He W, Xu H, Forrest CR: Effector mechanism of adenosine in acute ischemic preconditioning of skeletal muscle against infarction. AmJ Physiol 273(3, Pt 2):R887–R895, 1997
Glazier SS, O'Rourke DM, Graham DI, Welsh FA: Induction of ischemic tolerance following brief focal ischemia in rat brain. J Cereb Blood Flow Metab 14(4):545–553, 1994
Sakurai M, Hayashi T, Abe K, Aoki M, Sadahiro M, Tabayashi K: Enhancement of heat shock protein expression after transient ischemia in the preconditioned spinal cord of rabbits. J Vasc Surg 27(4):720–725, 1998
Turman MA, Bates CM: Susceptibility of human proximal tubular cells to hypoxia: effect of hypoxic preconditioning and comparison to glomerular cells. Ren Fail 19(1):47–60, 1997
Du ZY, Hicks M, Winlaw D, Spratt P, Macdonald P: Ischemic preconditioning enhances donor lung preservation in the rat. J Heart Lung Transplant 15(12):1258–1267, 1996
Li Y, Roth S, Laser M, Ma JX, Crosson CE: Retinal preconditioning and the induction of heat-shock protein 27. Invest Ophthalmol Vis Sci 44(3):1299–1304, 2003
Sola A, De Oca J, Gonzalez R, Prats N, Rosello-Catafau J, Gelpi E, Jaurrieta E, Hotter G: Protective effect of ischemic preconditioning on cold preservation and reperfusion injury associated with rat intestinal transplantation. Ann Surg 234(1):98–106, 2001
Davis JM, Gute DC, Jones S, Krsmanovic A, Korthuis RJ: Ischemic preconditioning prevents postischemic P-selectin expression in the rat small intestine. Am J Physiol 277(6, Pt 2):H2476–H2481, 1999
Vlasov TD, Smirnov DA, Nutfullina GM: Preconditioning of the small intestine to ischemia in rats. Neurosci Behav Physiol 32(4):449–453, 2002
Jenkins DP, Pugsley WB, Alkhulaifi AM, Kemp M, Hooper J, Yellon DM: Ischaemic preconditioning reduces troponin T release in patients undergoing coronary artery bypass surgery. Heart 77(4):314–318, 1997
Clavien PA, Selzner M, Rudiger HA, Graf R, Kadry Z, Rousson V, Jochum W: A prospective randomized study in 100 consecutive patients undergoing major liver resection with versus without ischemic preconditioning. Ann Surg 238(6):843–850, 2003
Hotter G, Closa D, Prados M, Fernandez-Cruz L, Prats N, Gelpi E, Rosello-Catafau J: Intestinal preconditioning is mediated by a transient increase in nitric oxide. Biochem Biophys Res Commun 222(1):27–32, 1996
Unal S, Demirkan F, Arslan E, Cin I, Cinel L, Eskandari G, Cinel I: Comparison of ischemic and chemical preconditioning in jejunal flaps in the rat. Plast Reconstr Surg 112(4):1024–1031, 2003
McCallion K, Wattanasirichaigoon S, Gardiner KR, Fink MP: Ischemic preconditioning ameliorates ischemia-and reperfusion-induced intestinal epithelial hyperpermeability in rats. Shock 14(4):429–434, 2000
Cohen MV, Baines CP, Downey JM: Ischemic preconditioning: From adenosine receptor of KATP channel. Annu Rev Physiol 62:79–109, 2000
Bolli R: The late phase of preconditioning. Circ Res 87(11):972–983, 2000
Yellon DM, Dana A: The preconditioning phenomenon: A tool for the scientist or a clinical reality? Circ Res 87(7):543–550, 2000
Ferencz A, Szanto Z, Kalmar-Nagy K, Horvath OP, Roth E: Mitigation of oxidative injury by classic and delayed ischemic preconditioning prior to small bowel autotransplantation. Transplant Proc 36(2):286–288, 2004
Ferencz A, Szanto Z, Borsiczky B, Kiss K, Kalmar-Nagy K, Szeberenyi J, Horvath PO, Roth E: The effects of preconditioning on the oxidative stress in small-bowel autotransplantation. Surgery 132(5):877–884, 2002
Tamion F, Richard V, Lacoume Y, Thuillez C: Intestinal preconditioning prevents systemic inflammatory response in hemorrhagic shock. Role of HO-1. Am J Physiol Gastrointest Liver Physiol 283(2):G408–G414, 2002
Wu B, Ootani A, Iwakiri R, Fujise T, Tsunada S, Toda S, Fujimoto K: Ischemic preconditioning attenuates ischemia-reperfusion-induced mucosal apoptosis by inhibiting the mitochondria-dependent pathway in rat small intestine. AmJ Physiol Gastrointest Liver Physiol 286(4):G580–G587, 2004
Sola A, Hotter G, Prats N, Xaus C, Gelpi E, Rosello-Catafau J: Modification of oxidative stress in response to intestinal preconditioning. Transplantation 69(5):767–772, 2000
Cinel I, Avlan D, Cinel L, Polat G, Atici S, Mavioglu I, Serinol H, Aksoyek S, Oral U: Ischemic preconditioning reduces intestinal epithelial apoptosis in rats. Shock 19(6):588–592, 2003
Ahmadinejad M, Rex M, Sutton RH, Pollitt CC, Cribb B: The effects of allopurinol on the ultrastructure of ischaemic and reperfused large intestine of sheep. Aust Vet J 74(2):135–139, 1996
Cuzzocrea S, Mazzon E, Dugo L, Caputi AP, Aston K, Riley DP, Salvemini D: Protective effects of a new stable, highly active SOD mimetic, M40401 in splanchnic artery occlusion and reperfusion. Br J Pharmacol 132(1):19–29, 2001
Balogh N, Krausz F, Levai P, Ribiczeyne PS, Vajdovich P, Gaal T: Effect of deferoxamine and L-arginine treatment on lipid peroxidation in an intestinal ischaemia-reperfusion model in rats. Acta Vet Hung 50(3):343–356, 2002
Cuzzocrea S, Mazzon E, Costantino G, Serraino I, De Sarro A, Caputi AP: Effects of n-acetylcysteine in a rat model of ischemia and reperfusion injury. Cardiovasc Res 47(3):537–548, 2000
Yamaguchi T, Dayton C, Shigematsu T, Carter P, Yoshikawa T, Gute DC, Korthuis RJ: Preconditioning with ethanol prevents postischemic leukocyte-endothelial cell adhesive interactions. Am J Physiol Heart Circ Physiol 283(3):H1019–H1030, 2002
Nakamura M, Ozaki M, Fuchinoue S, Teraoka S, Ota K: Ascorbic acid prevents ischemia-reperfusion injury in the rat small intestine. Transpl Int 10(2):89–95, 1997
Gunel E, Caglayan F, Caglayan O, Dilsiz A, Duman S, Aktan M: Treatment of intestinal reperfusion injury using antioxidative agents. J Pediatr Surg 33(10):1536–1539, 1998
Sener G, Akgun U, Satiroglu H, Topaloglu U, Keyer-Uysal M: The effect of pentoxifylline on intestinal ischemia/reperfusion injury. Fundam Clin Pharmacol 15(1):19–22, 2001
Hammerman C, Goldschmidt D, Caplan MS, Kaplan M, Schimmel MS, Eidelman AI, Branski D, Hochman A: Amelioration of ischemia-reperfusion injury in rat intestine by pentoxifylline-mediated inhibition of xanthine oxidase. J Pediatr Gastroenterol Nutr 29(1):69–74, 1999
Mocan H, Gedik Y, Erduran E, Mocan ZM, Okten A, Gacar N, Pul N: The role of calcium channel entry blocker in experimental ischemia-reperfusion-induced intestinal injury. Pol J Pharmacol 47(2):179–183, 1995
Simpson R, Alon R, Kobzik L, Valeri CR, Shepro D, Hechtman HB: Neutrophil and nonneutrophil-mediated injury in intestinal ischemia-reperfusion. Ann Surg 218(4):444–453, 1993
Kojima M, Iwakiri R, Wu B, Fujise T, Watanabe K, Lin T, Amemori S, Sakata H, Shimoda R, Oguzu T, Ootani A, Tsunada S, Fujimoto K: Effects of antioxidative agents on apoptosis in-duced by ischaemia-reperfusion in rat intestinal mucosa. Aliment Pharmacol Ther 18 (Suppl 1):139–145, 2003
Tomatsuri N, Yoshida N, Takagi T, Katada K, Isozaki Y, Imamoto E, Uchiyama K, Kokura S, Ichikawa H, Naito Y, Okanoue T, Yoshikawa T: Edaravone, a newly developed radical scavenger, protects against ischemia-reperfusion injury of the small intestine in rats. Int J Mol Med 13(1):105–109, 2004
Kawata K, Takeyoshi I, Iwanami K, Sunose Y, Aiba M, Ohwada S, Matsumoto K, Morishita Y: A spontaneous nitric oxide donor ameliorates small bowel ischemia-reperfusion injury in dogs. Dig Dis Sci 46(8):1748–1756, 2001
Aoki N, Johnson G, III, Lefer AM: Beneficial effects of two forms of NO administration in feline splanchnic artery occlusion shock. Am J Physiol 258(2, Pt 1):G275–G281, 1990
Kalia N, Brown NJ, Hopkinson K, Stephenson TJ, Wood RF, Pockley AG: FK409 inhibits both local and remote organ damage after intestinal ischaemia. J Pathol 197(5):595–602, 2002
Fox-Robichaud A, Payne D, Hasan SU, Ostrovsky L, Fairhead T, Reinhardt P, Kubes P: Inhaled NO as a viable antiadhesive therapy for ischemia/reperfusion injury of distal microvascular beds. J Clin Invest 101(11):2497–2505, 1998
Luo CC, Chen HM, Chiu CH, Lin JN, Chen JC: Effect of N(G)-nitro-L-arginine methyl ester on intestinal permeability following intestinal ischemia-reperfusion injury in a rat model. Biol Neonate 80(1):60–63, 2001
Naito Y, Takagi T, Ichikawa H, Tomatsuri N, Kuroda M, Isozaki Y, Katada K, Uchiyama K, Kokura S, Yoshida N, Okanoue T, Yoshikawa T: A novel potent inhibitor of inducible nitric oxide inhibitor, ONO-1714, reduces intestinal ischemia-reperfusion injury in rats. Nitric Oxide 10(3):170–177, 2004
Khanna A, Rossman J, Caty MG, Fung HL: Beneficial effects of intraluminal nitroglycerin in intestinal ischemia-reperfusion injury in rats. J Surg Res 114(1):15–24, 2003
Arumugam TV, Shiels IA, Woodruff TM, Reid RC, Fairlie DP, Taylor SM: Protective effect of a new C5a receptor antagonist against ischemia-reperfusion injury in the rat small intestine. J Surg Res 103(2):260–267, 2002
Zhao H, Montalto MC, Pfeiffer KJ, Hao L, Stahl GL: Murine model of gastrointestinal ischemia associated with complement-dependent injury. J Appl Physiol 93(1):338–345, 2002
Williams JP, Pechet TT, Weiser MR, Reid R, Kobzik L, Moore FD Jr, Carroll MC, Hechtman HB: Intestinal reperfusion injury is mediated by IgM and complement. J Appl Physiol 86(3):938–942, 1999
Karpel-Massler G, Fleming SD, Kirschfink M, Tsokos GC: Human C1 esterase inhibitor attenuates murine mesenteric ischemia/reperfusion induced local organ injury. J Surg Res 115(2):247–256, 2003
Souza DG, Coutinho SF, Silveira MR, Cara DC, Teixeira MM: Effects of a BLT receptor antagonist on local and remote reperfusion injuries after transient ischemia of the superior mesenteric artery in rats. Eur J Pharmacol 403(1–2):121–128, 2000
Souza DG, Cara DC, Cassali GD, Coutinho SF, Silveira MR, Andrade SP, Poole SP, Teixeira MM: Effects of the PAF receptor antagonist UK74505 on local and remote reperfusion injuries following ischaemia of the superior mesenteric artery in the rat. Br J Pharmacol 131(8):1800–1808, 2000
Sun Z, Olanders K, Lasson A, Dib M, Annborn M, Andersson K, Wang X, Andersson R: Effective treatment of gut barrier dysfunction using an antioxidant, a PAF inhibitor, and monoclonal antibodies against the adhesion molecule PECAM-1. J Surg Res 105(2):220–233, 2002
Souza DG, Cassali GD, Poole S, Teixeira MM: Effects of inhibition of PDE4 and TNF-alpha on local and remote injuries following ischaemia and reperfusion injury. Br J Pharmacol 134(5):985–994, 2001
Zou L, Attuwaybi B, Kone BC: Effects of NF-kappa Binhibition on mesenteric ischemia-reperfusion injury. Am J Physiol Gastrointest Liver Physiol 284(4):G713–G721, 2003
Hassoun HT, Zou L, Moore FA, Kozar RA, Weisbrodt NW, Kone BC: Alpha-melanocyte-stimulating hormone protects against mesenteric ischemia-reperfusion injury. Am J Physiol Gastrointest Liver Physiol 282(6):G1059–G1068, 2002
Riaz AA, Wan MX, Schafer T, Dawson P, Menger MD, Jeppsson B, Thorlacius H: Allopurinol and superoxide dismutase protect against leucocyte-endothelium interactions in a novel model of colonic ischaemia-reperfusion. Br J Surg 89(12):1572–1580, 2002
Harris NR, Granger DN: Organ procurements and preservation for transplantation. In: Ischemia/Reperfusion injury. New York: Springer Verlag, 1997, pp. 67–81
Carmody IC, Meng L, Shen XD, Anselmo D, Gao F, Ke B, Ma JP, Kupiec-Weglinski JW, McDiarmid SV, Busuttil RW, Shaw G, Farmer DG: P-Selectin knockout mice have improved outcomes with both warm ischemia and small bowel transplantation. Transplant Proc 36(2):263–264, 2004
Bowles MJ, Pockley AG, Wood RF: Effect of anti-LFA-1 mono-clonal antibody on rat small bowel allograft survival and circulating leukocyte populations. Transpl Immunol 8(1):75–80, 2000
Floyd TF, Boroughs A, Garvey C, Dasher J, Ikeda CB, Sloviter HA, Ziegler MM: Intestinal ischemia: treatment by peritoneal lavage with oxygenated perfluorochemical. J Pediatr Surg 22(12):1191–1197, 1987
Oldham KT, Guice KS, Gore D, Gourley WK, Lobe TE: Treatment of intestinal ischemia with oxygenated intraluminal perfluorocarbons. Am J Surg 153(3):291–294, 1987
Ricci JL, Sloviter HA, Ziegler MM: Intestinal ischemia: Reduction of mortality utilizing intraluminal perfluorochemical. Am J Surg 149(1):84–90, 1985
O'Donnell KA, Caty MG, Zheng S, Rossman JE, Azizkhan RG: Oxygenated intraluminal perfluorocarbon protects intestinal muscosa from ischemia/reperfusion injury. J Pediatr Surg 32(2):361–365, 1997
Ohara M, Unno N, Mitsuoka H, Kaneko H, Nakamura S: Peritoneal lavage with oxygenated perfluorochemical preserves intestinal mucosal barrier function after ischemia-reperfusion and ameliorates lung injury. Crit Care Med 29(4):782–788, 2001
Vejchapipat P, Proctor E, Ramsay A, Petros A, Gadian DG, Spitz L, Pierro A: Intestinal energy metabolism after ischemia-reperfusion: Effects of moderate hypothermia and perfluorocarbons. J Pediatr Surg 37(5):786–790, 2002
Fujino Y, Suzuki Y, Kakinoki K, Tanioka Y, Ku Y, Kuroda Y: Protection against experimental small intestinal ischaemia-reperfusion injury with oxygenated perfluorochemical. Br J Surg 90(8):1015–1020, 2003
Shashikant MP, Badellino MM, Cooper B, Shaffer TH, Myers SI, Wolfson MR: Physicochemical properties of perfluorochemical liquids influence ventilatory requirements, pulmonary mechanics, and microvascular permeability during partial liquid ventilation following intestinal ischemia/reperfusion injury. Crit Care Med 30(10):2300–2305, 2002
Fukatsu K, Zarzaur BL, Johnson CD, Lundberg AH, Wilcox HG, Kudsk KA: Enteral nutrition prevents remote organ injury and death after a gut ischemic insult. Ann Surg 233(5):660–668, 2001
Fukatsu K, Lundberg AH, Hanna MK, Wu Y, Wilcox HG, Granger DN, Gaber AO, Kudsk KA: Increased expression of intestinal P-selectin and pulmonary E-selectin during intravenous total parenteral nutrition. Arch Surg 135(10):1177–1182, 2000
Wu Y, Kudsk KA, DeWitt RC, Tolley EA, Li J: Route and type of nutrition influence IgA-mediating intestinal cytokines. Ann Surg 229(5):662–667, 1999
Lacey JM and Wilmore DW: Is glutamine a conditionally essential amino acid? Nutr Rev 48(8):297–309, 1990
Askanazi J, Carpentier YA, Michelsen CB, Elwyn DH, Furst P, Kantrowitz LR, Gump FE, Kinney JM: Muscle and plasma amino acids following injury. Influence of intercurrent infection. AnnSurg 192(1):78–85, 1980
Wilmore DW: Growth factors and nutrients in the short bowel syndrome. JPEN J Parenter Enteral Nutr 23(Suppl 5):S117–S120, 1999
Ziegler TR, Estivariz CF, Jonas CR, Gu LH, Jones DP, Leader LM: Interactions between nutrients and peptide growth factors in intestinal growth, repair, and function. JPEN J Parenter Enteral Nutr 23(Suppl 6):S174–S183, 1999
Li YS, Li JS, Jiang JW, Liu FN, Li N, Qin WS, Zhu H: Glycyl-glutamine-enriched long-term total parenteral nutrition attenuates bacterial translocation following small bowel transplantation in the pig. J Surg Res 82(1):106–111, 1999
Sakawaki T, Sasaki K, Hirata K: Saline with glutamine improves cold preserved small bowel graft mortality. Transplant Proc 30(7):3471–3474, 1998
Tamaki T, Konoeda Y, Yasuhara M, Tanaka M, Yokota N, Hayashi T, Katori M, Uchida Y, Kawamura A: Glutamine-induced heme oxygenase-1 protects intestines and hearts from warm ischemic injury. Transplant Proc 31(1–2):1018–1019, 1999
Zhang W, Bain A, Rombeau JL: Insulin-like growth factor-I (IGF-I) and glutamine improve structure and function in the small bowel allograft. J Surg Res 59(1):6–12, 1995
Ikeda S, Zarzaur BL, Johnson CD, Fukatsu K, Kudsk KA: Total parenteral nutrition supplementation with glutamine improves survival after gut ischemia/reperfusion. JPEN J Parenter Enteral Nutr 26(3):169–173, 2002
Wischmeyer PE: Glutamine and heat shock protein expression. Nutrition 18(3):225–228, 2002
Kelly D, Wischmeyer PE: Role of L-glutamine in critical illness: new insights. Curr Opin Clin Nutr Metab Care 6(2):217–222, 2003
Harward TR, Coe D, Souba WW, Klingman N, Seeger JM: Glutamine preserves gut glutathione levels during intestinal ischemia/reperfusion. J Surg Res 56(4):351–355, 1994
Lee MA, McCauley RD, Kong SE, Hall JC: Pretreatment with glycine reduces the severity of warm intestinal ischemic-reperfusion injury in the rat. Ann Plast Surg 46(3):320–326, 2001
Lee MA, McCauley RD, Kong SE, Hall JC: Influence of glycine on intestinal ischemia-reperfusion injury. JPEN J Parenter Enteral Nutr 26(2):130–135, 2002
Grotz MR, Pape HC, van Griensven M, Stalp M, Rohde F, Bock D, Krettek C: Glycine reduces the inflammatory response and organ damage in a two-hit sepsis model in rats. Shock 16(2):116–121, 2001
Kelly D, Zhong Z, Wheeler MD, Li X, Froh M, Schemmer P, Yin M, Bunzendaul H, Bradford B, Lemasters JJ: L-Glycine: A novel antiinflammatory, immunomodulatory, and cytoprotective agent. Curr Opin Clin Nutr Metab Care 6(2):229–240, 2003
Jacob T, Ascher E, Hingorani A, Kallakuri S: Glycine prevents the induction of apoptosis attributed to mesenteric ischemia/reperfusion injury in a rat model. Surgery 134(3):457–466, 2003
Ferrer JV, Ariceta J, Guerrero D, Gomis T, Larrea MM, Balen E, Lera JM: Allopurinol and N-acetylcysteine avoid 60% of intestinal necrosis in an ischemia-reperfusion experimental model. Transplant Proc 30(6):2672, 1998
Ozden A, Tetik C, Bilgihan A, Calli N, Bostanci B, Yis O, Duzcan E: Antithrombin III prevents 60 min warm intestinal ischemia reperfusion injury in rats. Res Exp Med (Berl) 198(5):237–246, 1999
Puglisi RN, Strande L, Santos M, Doolin EJ, Hewitt CW, Whalen TV: The effect of cyclosporine in gut ischemic injury: a com-puterized morphometric and enzymatic analysis. J Pediatr Surg 31(2):319–322, 1996
Berlanga J, Prats P, Remirez D, Gonzalez R, Lopez-Saura P, Aguiar J, Ojeda M, Boyle JJ, Fitzgerald AJ, Playford RJ: Prophylactic use of epidermal growth factor reduces ischemia/reperfusion intestinal damage. Am J Pathol 161(2):373–379, 2002
Ustundag B, Kazez A, Demirbag M, Canatan H, Halifeoglu I, Ozercan IH: Protective effect of melatonin on antioxidative system in experimental ischemia-reperfusion of rat small intestine. Cell Physiol Biochem 10(4):229–236, 2000
Kazez A, Demirbag M, Ustundag B, Ozercan IH, Saglam M: The role of melatonin in prevention of intestinal ischemia-reperfusion injury in rats. J Pediatr Surg 35(10):1444–1448, 2000
Dun Y, Hao YB, Wu YX, Zhang Y, Zhao RR: Protective effects of nitroglycerin-induced preconditioning mediated by calcitonin gene-related peptide in rat small intestine. Eur J Pharmacol 430(2–3):317–324, 2001
Cicalese L, Lee K, Schraut W, Watkins S, Borle A, Stanko R: Pyruvate prevents ischemia-reperfusion mucosal injury of rat small intestine. Am J Surg 171(1):97–100, 1996
Tetik C, Ozden A, Calli N, Bilgihan A, Bostanci B, Yis O, Bayramoglu H: Cytoprotective effect of trimetazidine on 60 minutes of intestinal ischemia-reperfusion injury in rats. Transpl Int 12(2):108–112, 1999
Tsuruma T, Yagihashi A, Hirata K, Matsuno T, Zou XM, Sasaki K, Asanuma K, Endo T: Evaluation of plasma IL-8 (CINC) concentration during ischemia and after reperfusion in the small intestine. Transplant Proc 28(3):1917–1918, 1996
Droy-Lefaix MT, Drouet Y, Geraud G, Hosford D, Braquet P: Superoxide dismutase (SOD) and the PAF-antagonist (BN 52021) reduce small intestinal damage induced by ischemia-reperfusion. Free Radic Res Commun 12–13 (Pt 2):725–735, 1991
Souza DG, Mendonca VA, de ACM, Poole S, Teixeira MM: Role of tachykinin NK receptors on the local and remote injuries following ischaemia and reperfusion of the superior mesenteric artery in the rat. Br J Pharmacol 135(2):303–312, 2002
Yagihashi A, Tsuruma T, Tarumi K, Kameshima T, Yajima T, Yanai Y, Watanabe N, Hirata K: Prevention of small intestinal ischemia-reperfusion injury in rat by anti-cytokine-induced neutrophil chemoattractant monoclonal antibody. J Surg Res 78(2):92–96, 1998
Chen Y, Hung WT, Chen SM, Tseng SH: Suppression of elevated plasma interleukin-8 levels due to total ischemia and reperfusion of the small intestine by luminal perfusion with fetal bovine serum. Pediatr Surg Int 18(2–3):107–109, 2002
Mazzon E, Dugo L, De SA, Li JH, Caputi AP, Zhang J, Cuzzocrea S: Beneficial effects of GPI 6150, an inhibitor of poly(ADP-ribose) polymerase in a rat model of splanchnic artery occlusion and reperfusion. Shock 17(3):222–227, 2002
Xia G, Martin AE, Besner GE: Heparin-binding EGF-like growth factor downregulates expression of adhesion molecules and infiltration of inflammatory cells after intestinal ischemia/reperfusion injury. J Pediatr Surg 38(3):434–439, 2003
Kuenzler KA, Pearson PY, Schwartz MZ: Hepatoctye growth factor pretreatment reduces apoptosis and mucosal damage after intestinal ischemia-reperfusion. J Pediatr Surg 37(7):1093 [discussion], 2002
Yang ZJ, Bosco G, Montante A, Ou XI, Camporesi EM: Hyperbaric O2 reduces intestinal ischemia-reperfusion-induced TNF-alpha production and lung neutrophil sequestration. Eur J Appl Physiol 85(1–2):96–103, 2001
Lane JS, Todd KE, Lewis MP, Gloor B, Ashley SW, Reber HA, McFadden DW, Chandler CF: Interleukin-10 reduces the systemic inflammatory response in a murine model of intestinal ischemia/reperfusion. Surgery 122(2):288–294, 1997
Dowdall JF, Winter DC, Bouchier-Hayes DJ: Inosine modulates gut barrier dysfunction and end organ damage in a model of ischemia-reperfusion injury. J Surg Res 108(1):61–68, 2002
Stroh R, Christopher TA, Lopez BL, Guo YP, Amico-Roxas M, Ma XL: L-Propionyl carnitine, an endogenous ester in fatty acid metabolism, exerts anti-shock and endothelial protective effects in rat splanchnic ischemia-reperfusion injury. Shock 9(3):216–222, 1998
Cuzzocrea S, Tailor A, Zingarelli B, Salzman AL, Flower RJ, Szabo C, Perretti M: Lipocortin 1 protects against splanchnic artery occlusion and reperfusion injury by affecting neutrophil migration. J Immunol 159(10):5089–5097, 1997
Warnecke HB, Schirmeier A, Nussler AK, Platz KP, Stange B, Nussler NC, Radke C, Neuhaus P, Mueller AR: The combined treatment with L-arginine and methylprednisolone improves graft morphology and mucosal barrier function. Transplant Proc 34(3):996–998, 2002
Loong CC, Chiu JH, Tiao RC, Chiu YY, Wu CW, Lui WY: Pre-treatment with magnolol attenuates ischemia-reperfusion injury in rat small intestine. Transplant Proc 33(7–8):3737–3738, 2001
Farmer DG, Amersi F, Shen XD, Gao F, Anselmo D, Ma J, Dry S, McDiarmid SV, Shaw G, Busuttil RW, Kupiec-Weglinski J: Improved survival through the reduction of ischemia-reperfusion injury after rat intestinal transplantation using selective P-selectin blockade with P-selectin glycoprotein ligand-Ig. Transplant Proc 34(3):985, 2002
Arumugam TV, Shiels IA, Margolin SB, Taylor SM, Brown L: Pirfenidone attenuates ischaemia-reperfusion injury in the rat small intestine. Clin Exp Pharmacol Physiol 29(11):996–1000, 2002
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Mallick, I.H., Yang, W., Winslet, M.C. et al. REVIEW: Ischemia—Reperfusion Injury of the Intestine and Protective Strategies Against Injury. Dig Dis Sci 49, 1359–1377 (2004). https://doi.org/10.1023/B:DDAS.0000042232.98927.91
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DOI: https://doi.org/10.1023/B:DDAS.0000042232.98927.91