Abstract
Background: Chromolena odorata is a tropical species of flowering shrub in the family Asteraceae, leaves of it have been reported to be widely used as herbal remedy for the treatment of various ailments. It is particularly reported to be useful in the healing of wounds.
Methods: We investigated the possibility of amelioration of intestinal ischemia–reperfusion (IR) injury in rats treated with methanolic extract of C. odorata (MECO). Wistar albino rats were divided randomly into five groups of six animals each as control, IR-treated, IR+200 mg/kg MECO, IR+400 mg/kg MECO, and IR+200 mg/kg vitamin C. Pre-treatment with MECO or vitamin C was for 7 days.
Results: The contents of hydrogen peroxide (H2O2) and malondialdehyde (MDA) were significantly reduced by MECO and vitamin C, while there were significant enhancements of the activities of superoxide dismutase (SOD), glutathione peroxidase (GPX), catalase (CAT), as well as the content of reduced glutathione (GSH) in pre-treated rats compared to IR-treated rats. Glutathione S-transferase (GST) activity was not significantly affected in all the groups. Histopathological examination of small intestinal mucosa revealed significant attenuation of intestinal pathology in animals pre-treated with MECO, while IR injury produced severe villi erosion, necrosis, and inflammatory cell infiltrations.
Conclusions: The present study highlights the antioxidant activities of MECO and its ability to inhibit inflammatory cell infiltration as mechanisms involved in its protection against IR injury in the intestine of rats, an effect that was largely comparable to that of vitamin C.
References
1. HaciogluA, AlginC, PasaogluO, PasaogluE, KanbakG. Protective effect of leptin against ischemia-reperfusion injury in the rat small intestine. BMC Gastroenterol2005;5:37.10.1186/1471-230X-5-37Search in Google Scholar PubMed PubMed Central
2. CollardCD, PathophysiologyGS. Clinical manifestations, and prevention of ischemia-reperfusion injury. Anesthesiology2001;94:1133–8.10.1097/00000542-200106000-00030Search in Google Scholar PubMed
3. MooreEE, MooreFA, FrancioseRJ, KimFJ, BifflWL, BanerjeeA. The postischemic gut serves as a priming bed for circulating neutrophils that provoke multiple organ failure. J Trauma1994;37:881–7.10.1097/00005373-199412000-00002Search in Google Scholar PubMed
4. SwankGM, DeitchEA. Role of the gut in multiple organ failure: bacterial translocation and permeability changes. World J Surg1996;20:411–17.10.1007/s002689900065Search in Google Scholar PubMed
5. KoikeK, MooreFA, MooreEE, ReadRA, CarlVS, BanerjeeA. Gut ischemia mediates lung injury by a xanthine oxidase-dependent neutrophil mechanism. J Surg Res1993;54:469–73.10.1006/jsre.1993.1072Search in Google Scholar PubMed
6. CerqueiraNF, HussniCA, YoshidaWB. Pathophysiology of mesenteric ischemia/reperfusion: a review. Acta Cir Bras2005;20:336–43.10.1590/S0102-86502005000400013Search in Google Scholar
7. CicaleseL, SileriP, GreenM, Abu-ElmagdK, KocoshisS, ReyesJ. Bacterial translocation in clinical intestinal transplantation. Transplantation2001;71:1414–17.10.1097/00007890-200105270-00010Search in Google Scholar PubMed
8. LinfertD, ChowdhryT, RabbH. Lymphocytes and ischemia/reperfusion injury. Transplant Rev (Orlando)2009;23:1–10.10.1016/j.trre.2008.08.003Search in Google Scholar PubMed PubMed Central
9. KuenzlerKA, PearsonPY, SchwartzMZ. Interleukin-11 enhances intestinal absorptive function after ischemia-reperfusion injury. J Pediatr Surg2002;37:457–9.10.1053/jpsu.2002.30861Search in Google Scholar PubMed
10. PrasadR, AlaviK, SchwartzMZ. GLP-2 alpha accelerates recovery of mucosal absorptive function after intestinal ischemia/reperfusion. J Pediatr Surg2001;36:570–2.10.1053/jpsu.2001.22284Search in Google Scholar PubMed
11. RajeevprasadR, AlaviK, SchwartzMZ. Glucagonlike peptide-2 analogue enhances intestinal mucosal mass and absorptive function after ischemia-reperfusion injury. J Pediatr Surg2000;35:1537–9.10.1053/jpsu.2000.18301Search in Google Scholar
12. MallickIH, YangW, WinsletMC, SeifalianAM. Ischemia-reperfusion injury of the intestine and protective strategies against injury. Dig Dis Sci2004;49:1359–77.10.1023/B:DDAS.0000042232.98927.91Search in Google Scholar
13. HarrisonR. Structure and function of xanthine oxidoreductase: where are we now?Free Radic Biol Med2002;33:774–97.10.1016/S0891-5849(02)00956-5Search in Google Scholar
14. CicaleseL, CaraceniP, NalesnikMA, BorleAB, SchrautWH. Oxygen free radical content and neutrophil in-filtration are important determinants in mucosal injury after rat small bowel transplantation. Transplantation1996;62:161–6.10.1097/00007890-199607270-00003Search in Google Scholar
15. DeshmukhDR, Mirochnitchenko GholeVS, AgneseD, ShahPC, ReddellM, BrolinRE, et al. Intestinal ischemia and reperfusion injury in transgenic mice over-expressing copper- zinc superoxide dismutase. Am J Physiol1997;273:C1130–C113S.10.1152/ajpcell.1997.273.4.C1130Search in Google Scholar
16. YoshikawaT, YasudaM, UedaS, NaitoY, TanigawaT, OyamadaH, et al. Vitamin E in gastric mucosal injury induced by ischemia-reperfusion. Am J Clin Nutr1991;53:21OS–4S.10.1093/ajcn/53.1.210SSearch in Google Scholar
17. KulahB, BeslerHT, AkdagM, OrucT, AltinokG, KulacogluH, et al. The effects of verapamil vs. Allopurinol on intestinal ischemia/reperfusion injury in rats. “An experimental study.” Hepatogastroenterology2004;51:401–7.Search in Google Scholar
18. HakguderG, AkgurFM, AtesO, OlgunerM, AktugT, OzerE. Short-term intestinal ischemia-reperfusion alters intestinal motility that can be preserved by xanthine oxidase inhibition. Dig Dis Sci2002;47:1279–83.10.1023/A:1015314312730Search in Google Scholar
19. MojzisJ, HegedusovaR, MirossayL. Role of mucus in ischemia/reperfusion-induced gastric mucosal injury in rats. Physiol Res2000;49:441–6.Search in Google Scholar
20. SencanA, YilmazO, OzerE, GunsarC, GencK, UlukusC, et al. Does sucralfate prevent apoptosis occurring in the ischemia/reperfusion-induced intestinal injury?Eur J Pediatr Surg2003;13:231–5.10.1055/s-2003-42235Search in Google Scholar
21. DunY, HaoYB, WuYX, ZhangY, ZhaoRR. Protective effects of nitroglycerin-induced preconditioning mediated by calcitonin gene-related peptide in rat small intestine. Eur J Pharmacol2001;430:317–24.10.1016/S0014-2999(01)01256-0Search in Google Scholar
22. KhannaA, RossmanJ, CatyMG, FungHL. Beneficial effects of intraluminal nitroglycerin in intestinal ischemia-reperfusion injury in rats. J Surg Res2003;114:15–24.10.1016/S0022-4804(03)00329-9Search in Google Scholar
23. CuzzocreaS, MazzonE, CostantinoG, SerrainoI, De SarroA, CaputiAP. Effects of n-acetylcysteine in a rat model of ischemia and reperfusion injury. Cardiovasc Res2000;47:537–48.10.1016/S0008-6363(00)00018-3Search in Google Scholar
24. SunZ, OlandersK, LassonA, DibM, AnnbornM, AnderssonK, et al. Effective treatment of gut barrier dysfunction using an antioxidant, a PAF inhibitor, and monoclonal antibodies against the adhesion molecule PECAM-1. J Surg Res2002;105:220–33.10.1006/jsre.2001.6342Search in Google Scholar
25. MonteroEF, AbrahaoMS, KoikeMK, MannaMC, RamalhoCE. Intestinal ischemia and reperfusion injury in growing rats: hypothermia and N-acetylcysteine modulation. Microsurgery2003;23:517–21.10.1002/micr.10163Search in Google Scholar
26. Byrka-OwczarekK, Steplewska-MazurK, KrasonM, BohosiewiczJ, KoszutskiT, WojtynekG. The evaluation of the protective action of antioxidants on small intestine of rabbits experimentally injured by ischemia and reperfusion. J Pediatr Surg2004;39:1226–9.10.1016/j.jpedsurg.2004.04.009Search in Google Scholar
27. IinoT, TashimaK, UmedaM, OgawaY, TakadaM, TakataK, et al. Effect of ellagic acid on gastric damage induced in ischemic rat stomachs following ammonia or reperfusion. Life Sci2002;70:1139–50.10.1016/S0024-3205(01)01493-XSearch in Google Scholar
28. GunelE, CaglayanF, CaglayanO, DilsizA, DumanS, AktanM. Treatment of intestinal reperfusion injury using antioxidative agents. J Pediatr Surg1998;33:1536–9.10.1016/S0022-3468(98)90492-4Search in Google Scholar
29. KöhlerHF, DeLuccaIM, Snraglia NetoL. Enteral antioxidants in ischemia/reperfusion injury in rats. Rev Col Bras Cir [Periódico Na Internet]2011;38. Disponível em URL: http://www.scielo.br/rcbcSearch in Google Scholar
30. NakamuraM, OzakiM, FuchinoueS, TeraokaS, OtaK. Ascorbic acid prevents ischemia-reperfusion injury in the rat small intestine. Transplant Int1997;10:89–95.10.1111/j.1432-2277.1997.tb00547.xSearch in Google Scholar
31. CathcartRF 3rd. Vitamin C: the nontoxic, non-rate-limited, antioxidant free radical scavenger. Med Hypotheses1985;18:61–77.10.1016/0306-9877(85)90121-5Search in Google Scholar
32. NakamuraM, OzakiM, FuchinoueS, TeraokaS, OtaK. Ascorbic acid prevents ischemia-reperfusion injury in the rat small intestine. Transplant Int1997;10:89–95.10.1111/j.1432-2277.1997.tb00547.xSearch in Google Scholar
33. HeiZQ, HuangHQ, ZhangJJ, ChenBX, LiXY. Protective effect of astragalus membranaceus on intestinal mucosa reperfusion injury after hemorrhagic shock in rats. World J Gastroenterol2005;11:4986–91.10.3748/wjg.v11.i32.4986Search in Google Scholar PubMed PubMed Central
34. TerziA, CobanS, YildizF, AtesM, BitirenM, TaskinA, et al. Protective effects of Nigella sativa on intestinal ischemia-reperfusion injury in rats. J Invest Surg2010;23:21–7.10.3109/08941930903469375Search in Google Scholar PubMed
35. KheirandishR, AzariO, SamadiehH, RasaZ. Protective effect of Trigonella foenum graecum (fenugreek) seed extract on experimental intestinal ischaemia/reperfusion injury in rats. Iranian J Vet Surg2011;6:37–44.Search in Google Scholar
36. AkinrinmadeJF, AkinrindeAS. Effect of oral administration of methanolic extract of ocimum gratissimum on intestinal ischemia-reperfusion injury in rats. Eur J Med Plants2013;3:591–602.10.9734/EJMP/2013/5425Search in Google Scholar
37. LingSK, MazuraMD, SalbiahM. Platelet-activating factor (PAF) receptor binding antagonist activity of the methanol extracts and isolated flavonoids from Chromolaena odorata (L.) King and Robinson. Biol Pharm Bull2007;30:1150–2.10.1248/bpb.30.1150Search in Google Scholar
38. PhanTT, WangL, SeeP, GrayerRJ, ChanSY, LeeST. Phenolic compounds of chromolaena odorata protect cultured skin cells from oxidative damage: implication for cutaneous wound healing. Biol Pharm Bull2001;24:1373–9.10.1248/bpb.24.1373Search in Google Scholar
39. Nur JannahMH, MahmoodAA, SidikK, SalmahI. Cytoprotective effects of honey in combination with aqueous and ethanol extracts from Chromolaena odorata L (Eupatorium odoratum) in rats. JUMMEC2006;9:7–13.10.22452/jummec.vol9no1.3Search in Google Scholar
40. OnkaramurthyM, VeerapurVP, ThippeswamyBS, ReddyTN, RayappaH, Anti-diabeticBS. Anticataract effects of chromolena odorata in streptozotocin-induced diabetic rats. J Ethnopharmacology2013;145:363–72.10.1016/j.jep.2012.11.023Search in Google Scholar
41. OwuDU, ObembeAO, NwokochaCR, EdohoIE, OsimEE. Gastric ulceration in diabetes mellitus: protective role of vitamin C. ISRN Gastroenterol2012:362805. Epub 16 Jun 2012. DOI:10.5402/2012/362805.10.5402/2012/362805Search in Google Scholar
42. WolffSP. Ferrous ion oxidation in the presence of ferric ion indicator xylenol orange for measurement of hydroperoxides. Method Enzymol1994;233:182–9.10.1016/S0076-6879(94)33021-2Search in Google Scholar
43. VarshneyR, KaleRK. Effect of calmodulin antagonists on radiation induced lipid peroxidation in microsomes. Int J Biol1990;158:733–41.10.1080/09553009014552121Search in Google Scholar
44. Adam-ViziV, SeregiM. Receptor dependent stimulatory effect of noradrenalin on Na+−K+ ATPase in rat brain homogenate. Role of lipid peroxidation. Biochem Pharmacol1982;31:2231–6.10.1016/0006-2952(82)90106-XSearch in Google Scholar
45. JollowDJ, MitchellJR, ZampaglioneN, GilletteJR. Bro-mobenzene induced liver necrosis: protective role of glutathione and evidence for 3, 4 bromobenzene oxide as the hepatotoxic metabolite. Pharmacology1974;11:151–69.10.1159/000136485Search in Google Scholar PubMed
46. RotruckJT, PopeAL, GantherHE, SwansonAB, HafemanDG, HoekstraWG. Selenium: biochemical role as a component of glutathione peroxidase. Science1973;179:588–90.10.1126/science.179.4073.588Search in Google Scholar
47. HabigWH, PabstMJ, JacobyWB. Glutathione-S-transferase activity: the enzymic step in mercapturic acid formation. J Biol Chem1974;249:130–9.Search in Google Scholar
48. MisraHP, FridovichI. The role of superoxide anion in the autooxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem1972;247:3170–5.10.1016/S0021-9258(19)45228-9Search in Google Scholar
49. SinhaKA. Colorimetric assay of catalase. Anal Biochem1971;47:389–94.10.1016/0003-2697(72)90132-7Search in Google Scholar
50. ChiuCJ, McArdleAH, BrownR, ScottHJ, GurdFN. Intestinal mucosal lesion in low-flow states. I. A morphological, hemodynamic, and metabolic reappraisal. Arch Surg1970;101:478–83.10.1001/archsurg.1970.01340280030009Search in Google Scholar
51. CardenDL, GrangerDN. Pathophysiology of ischemia-reperfusion injury. J Pathol2000;2000:255–66.Search in Google Scholar
52. SemenzaGL. Series introduction: tissue ischemia: pathophysiology and therapeutics. J Clin Invest2000;106:613–14.10.1172/JCI10913Search in Google Scholar
53. BedirliN, OfluogluE, KeremM, UtebeyG, AlperM, YilmazerD, et al. Hepatic energy metabolism and the differential protective effects of sevoflurane and isoflurane anesthesia in a rat hepatic ischemia-reperfusion injury model. Anesth Analg2008;106:830–7.10.1213/ane.0b013e3181616fc9Search in Google Scholar
54. TogashiH, ShinzawaH, YongH, TakahashiT, NodaH, OikawaK, et al. Ascorbic acid radical, superoxide, and hydroxyl radical are detected in reperfusion injury of rat liver using electron spin resonance spectroscopy. Arch Biochem Biophys1994;308:1–7.10.1006/abbi.1994.1001Search in Google Scholar
55. YounesM, KayserE, StrubeltO. Effect of antioxidants on hypoxia/re-oxygenation induced injury in isolated perfused rat liver. Pharmacol Toxicol1992;71:278–83.10.1111/j.1600-0773.1992.tb00983.xSearch in Google Scholar
56. LesnefskyEJ, GalloDS, YeJ, WhittinghamTS, LustWD. Aging increases ischemia-reperfusion injury in the isolated, buffer-perfused heart. J Lab Clin Med1994;124:843–51.Search in Google Scholar
57. GrishamMB, HernandezLA, GrangerDN. Xanthine oxidase and neutrophil infiltration in intestinal ischemia. Am J Physiol1986;251:G567–G574.10.1152/ajpgi.1986.251.4.G567Search in Google Scholar
58. OtamiriT. Oxygen radicals, lipid peroxidation, and neutrophil infiltration after small-intestinal ischemia and reperfusion. Surgery1989;1989:593–7.Search in Google Scholar
59. GrishamMB, BenoitJN, GrangerDN. Assessment of leukocyte involvement during ischemia and reperfusion of intestine. Methods Enzymol1990;186:729–42.10.1016/0076-6879(90)86172-RSearch in Google Scholar
60. OgunbiyiBA, AruboulaEA, SoladoyeAO. Analgesic, anti-inflammatory and antipyretic activities from flavonoid fractions of chromolaena odorata. J Med Res2008;2:219–25.Search in Google Scholar
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