Abstract
The purpose of this study was to investigate the role of infliximab on acute lung injury induced by intestinal ischemia/reperfusion (I/R). A total of 30 male Wistar albino rats were divided into three groups: sham, I/R and I/R+ infliximab; each group contain 10 animals. Sham group animals underwent laparotomy without I/R injury. After I/R groups animals underwent laparotomy, 1 h of superior mesenteric artery ligation were followed by 1 h of reperfusion. In the infliximab group, 3 days before I/R, infliximab (3 mg/kg) was administered by intravenously. All animals were sacrificed at the end of reperfusion and lung tissues samples were obtained for biochemical and histopathological investigation in all groups. To date, no more biochemical and histopathological changes on intestinal I/R injury in rats by infliximab treatment have been reported. Infliximab treatment significantly decreased the elevated tissue malondialdehyde levels and increased of reduced superoxide dismutase, and glutathione peroxidase enzyme activities in lung tissues samples. Intestinal I/R caused severe histopathological injury including edema, hemorrhage, increased thickness of the alveolar wall and a great number of inflammatory cells that infiltrated the interstitium and alveoli. Infliximab treatment significantly attenuated the severity of intestinal I/R injury. Furthermore, there is a significant reduction in the activity of inducible nitric oxide synthase and arise in the expression of surfactant protein D in lung tissue of acute lung injury induced by intestinal I/R with infliximab therapy. It was concluded that infliximab treatment might be beneficial in acute lung injury, therefore, shows potential for clinical use. Because of its anti-inflammatory and antioxidant effects, infliximab pretreatment may have protective effects in acute lung injury induced by intestinal I/R.
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References
Barocelli E, Ballabeni V, Ghizzardi P, Cattaruzza F, Bertoni S, Lagrasta CA, Impicciatore M (2006) The selective inhibition of inducible nitric oxide synthase prevents intestinal ischemia-reperfusion injury in mice. Nitric Oxide 14:212–218
Breithaupt-Faloppa AC, Vitoretti LB, Coelho FR, dos Santos Franco AL, Domingos HV, Sudo-Hayashi LS, Oliveira-Filho RM, Tavares de Lima W (2009) Nitric oxide mediates lung vascular permeability and lymph-borne IL-6 after an intestinal ischemic insult. Shock 32:55–61
Casini A, Ceni E, Salzano R, Biondi P, Parola M, Galli A, Foschi M, Caligiuri A, Pinzani M, Surrenti C (1997) Neutrophil-derived superoxide anion induces lipid peroxidation and stimulates collagen synthesis in human hepatic stellate cells: role of nitric oxide. Hepatology 25:361–367
Cheng IW, Ware LB, Greene KE, Nuckton TJ, Eisner MD, Matthay MA (2003) Prognostic value of surfactant proteins A and D in patients with acute lung injury. Crit Care Med 31:20–27
Cury DH, Costa JE, Irika K, Mijji L, Garcez A, Buchiguel C, Silva I, Sipahi A (2008) Protective effect of octreotide and infliximab in an experimental model of indomethacin-induced inflammatory bowel disease. Dig Dis Sci 53:2516–2520
Deitch EA (2001) Role of the gut in multiple system organ failure. Curr Opin Crit Care 7:92–98
Di Sabatino A, Ciccocioppo R, Benazzato L, Sturniolo GC, Corazza GR (2004) Infliximab downregulates basic fibroblast growth factor and vascular endothelial growth factor in Crohn’s disease patients. Aliment Pharmacol Ther 19:1019–1024
Fink MP (2002) Reactive oxygen species as mediators of organ dysfunction caused by sepsis, acute respiratory distress syndrome, or hemorrhagic shock: potential benefits of resuscitation with Ringer’s ethyl pyruvate solution. Curr Opin Clin Nutr Metab Care 5:167–174
Frutos-Vivar F, Ferguson ND, Esteban A (2006) Epidemiology of acute lung injury and acute respiratory distress syndrome. Semin Respir Crit Care Med 27:327
Galili Y, Ben-Abraham R, Weinbroum A, Klausner J, Rabau M, Kluger Y (1998) Methylene blue prevents pulmonary injury following intestinal ischemia reperfusion. J Trauma 45:222–226
Giakoustidis AE, Giakoustidis DE, Iliadis S, Papageorgiou G, Koliakou K, Kontos N, Taitzoglou I, Botsoglou E, Papanikolaou V, Atmatzidis K, Takoudas D, Antoniadis A (2006) Attenuation of intestinal ischemia/reperfusion induced liver and lung injury by intraperitoneal administration of (-)-epigallocatechin-3-gallate. Free Radic Res 40:103–110
Guzel A, Basaran U, Aksu B, Kanter M, Yalcin O, Aktas C, Guzel A, Karasalihoglu S (2008) Protective effects of S-methylisothiourea sulfate on different aspiration materials-induced lung injury in rats. Int J Pediatr Otorhinolaryngol 72(8):1241–1250
Guzel A, Kanter M, Guzel A, Yucel AF, Erboga M (2011) Protective effect of curcumin on acute lung injury induced by intestinal ıschemia/reperfusion. Toxicol Ind Health. doi:10.1177/0748233711430984 [Epub ahead of print]
Hassoun HT, Kone BC, Mercer DW, Moody FG, Weisbrodt NW, Moore FA (2001) Postinjury multiple organ failure: the role of the gut. Shock 15:1–10
Herbein JF, Wright JR (2001) Enhanced clearance of surfactant protein D during LPS-induced acute inflammation in rat lung. Am J Physiol Lung Cell Mol Physiol 281:268–277
Hsu SM, Raine L, Fanger H (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29:577–580
Ito K, Ozasa H, Kojima N, Miura M, Iwai T, Senoo H, Horikawa S (2003) Pharmacological preconditioning protects lung injury induced by intestinal ischemia/reperfusion in rat. Shock 19:462–468
Koksoy C, Kuzu MA, Ergun H, Demirpençe E, Zülfikaroglu B (2000) Intestinal ischaemia and reperfusion impairs vasomotor functions of pulmonary vascular bed. Ann Surg 231:105–111
Kumamoto Y, Suematsu M, Shimazu M, Kato Y, Sano T, Makino N, Hirano KI, Naito M, Wakabayashi G, Ishimura Y, Kitajima M (1999) Kupffer cell-independent acute hepatocellular oxidative stress and decreased bile formation in post-cold-ischemic rat liver. Hepatology 30:1454–1463
Leth-Larsen R, Nordenback C, Tornoe I, Moeller V, Schlosser A, Koch C, Teisner B, Junker P, Holmskov U (2003) Surfactant protein D (SP-D) serum levels in patients with community-acquired pneumonia. Clin Immunol 108:29–37
Lowry OH, Rosenbrough NJ, Farr AC, Randall RJ (1951) Protein measurement with the folin phenol regent. J Biol Chem 193:265–275
Mayer AM, Spitzer JA (1993) Modulation of superoxide anion generation by manoalide, arachidonic acid and staurosporine in liver infiltrated neutrophils in a rat model of endotoxemia. J Pharmacol Exp Ther 267:400–409
McCord JM (1985) Oxygen-derived free radicals in postischemic tissue injury. N Engl J Med 312:159–163
Mitsuoka H, Kistler EB, Schmid-Schonbein GW (2002) Protease inhibition in the intestinal lumen: attenuation of systemic inflammation and early indicators of multiple organ failure in shock. Shock 17:205–209
Ohkawa H, Oshishi N, Yagi K (1979) Assay of lipid peroxidation in animal tissue by thiobarbituric acid reaction. Anal Biochem 95:351–358
Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterisation of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–169
Pararajasingam R, Weight SC, Bell PR, Nicholson ML, Sayers RD (2000) Pulmonary nitric oxide metabolism following infrarenal aortic cross-clamp-induced ischaemia-reperfusion injury. Eur J Vasc Endovasc Surg 19:41–47
Parks DA, Bulkley GB, Granger DN (1983) Role of oxygen-derived free radicals in digestive tract diseases. Surgery 94:415–422
Pascher A, Klupp J, Langrehr JM, Neuhaus P (2005) Anti-TNF-alpha therapy for acute rejection in intestinal transplantation. Transplant Proc 37:1635–1636
Pergel A, Kanter M, Yucel AF, Aydin I, Erboga M, Guzel A (2011) Anti-inflammatory and anti-oxidant effects of infliximab in a rat model of intestinal ischemia/reperfusion injury. Toxicol Ind Health. doi:10.1177/0748233711427056 [Epub ahead of print]
Ravanat JL, Di Mascio P, Martinez GR, Medeiros MH, Cadet J (2000) Singlet oxygen induces oxidation of cellular DNA. J Biol Chem 275:40601–40604
Rossman JE, Caty MG, Zheng S, Karamanoukian HL, Thusu K, Azizkhan RG, Dandona P (1997) Mucosal protection from intestinal ischemia-reperfusion reduces oxidant injury to the lung. J Surg Res 73:41–46
Sartani G, Silver PB, Rizzo LV, Chan CC, Wiggert B, Mastorakos G, Caspi RR (1996) Anti-tumor necrosis factor alpha therapy suppresses the induction of experimental autoimmune uveoretinitis in mice by inhibiting antigen priming. Invest Ophthalmol Vis Sci 37:2211–2218
Schoenberg MH, Beger HG (1993) Reperfusion injury after intestinal ischemia. Crit Care Med 21:1376–1386
Shen L, Zhang J (2003) Ginsenoside Rg1 increases ischemia-induced cell proliferation and survival in the dentate gyrus of adult gerbils. Neurosci Lett 344:1–4
Spitzer JA, Mayer AM (1993) Hepatic neutrophil influx: eicosanoid and superoxide formation in endotoxemia. J Surg Res 55:60–67
Sun Y, Oberley LW, Li Y (1988) A simple method for clinical assay of superoxide dismutase. Clin Chem 34:497–500
Takil A, Umuroglu T, Gogus YF, Eti Z, Yildizeli B, Ahiskali R (2003) Histopathologic effects of lipid content of enteral solutions after pulmonary aspiration in rats. Nutrition 19:666–669
Terada LS, Mahr NN, Jacobson ED (1996) Nitric oxide decreases lung injury after intestinal ischemia. J Appl Physiol 81:2456–2460
Turnage RH, Guice KS, Oldham KT (1994) Pulmonary microvascular injury following intestinal reperfusion. New Horiz 2:463–475
Turnage RH, Kadesky KM, Bartula L, Myers SI (1995) Intestinal reperfusion up-regulates inducible nitric oxide synthase activity within the lung. Surgery 118:288–293
Uchida K, Mishima S, Ohta S, Yukioka T (2007) Inhibition of inducible nitric oxide synthase ameliorates lung injury in rats after gut ischemia-reperfusion. J Trauma 63:603–607
Yucel AF, Kanter M, Pergel A, Erboga M, Guzel A (2011) The role of curcumin on intestinal oxidative stress, cell proliferation and apoptosis after ischemia/reperfusion injury in rats. J Mol Histol 42(6):579–587
Zhou JL, Jin GH, Yi YL, Zhang JL, Huang XL (2003) Role of nitric oxide and peroxynitrite anion in lung injury induced by intestinal ischemia-reperfusion in rats. World J Gastroenterol 9:1318–1322
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Guzel, A., Kanter, M., Guzel, A. et al. Anti-inflammatory and antioxidant effects of infliximab on acute lung injury in a rat model of intestinal ischemia/reperfusion. J Mol Hist 43, 361–369 (2012). https://doi.org/10.1007/s10735-012-9396-0
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DOI: https://doi.org/10.1007/s10735-012-9396-0