Pretreatment with Lactobacillus reuteri F-9-35 attenuates ethanol-induced gastric injury in rats

  • Mao-Cheng Sun
  • Ping-Ping Hou
  • Xin-Yu Wang
  • Chang-Hui Zhao
  • Bi-Jun Cheng
  • Yan-Ling Wang
  • Hong-Wei Hao
  • Tie-Hua Zhang
  • Hai-Qing Ye
Keywords: Lactobacillus reuteri; ethanol; gastric injury; inflammatory; antioxidant

Abstract

Background: Previous studies suggested that probiotics intervention may be one of the methods for preventing and/or treating gastric ulcer.

Objective: The aim of the study was to compare the preventive effects of a spaceflight mutant Lactobacillus reuteri F-9-35 and its wild type on ethanol-induced gastric injury in rats.

Design: Forty rats were randomly allocated into five groups: a normal group (NOR), ethanol group (EtOH), skim milk group (MILK), L. reuteri F-9-35 group (F935) and wild-type group (WT). The NOR and EtOH groups received 1 ml of distilled water by daily gavage for 14 days. The MILK group received 1 ml of skim milk alone, while the F935 and WT groups were administered 1 ml of skim milk containing the mutant and wild type (1 × 1010 colony-forming unit/ml) by daily gavage for 14 days, respectively. Acute gastric injury was induced by absolute alcohol 1 h after the final administration of different treatments, except for the NOR group.

Results: Pretreatment with L. reuteri F-9-35, but not milk alone or milk with the L. reuteri wild type, showed significant reduction of ethanol-induced gastric injury, as evidenced by lowering of ulcer index, ulcer area (%), and histological lesion. F-9-35 decreased the levels of lipid peroxidation and myeloperoxidase and increased mucus, glutathione, and nitric oxide levels in gastric tissue. Moreover, F-9-35 inhibited the expression of proinflammatory genes including gastric tumor necrosis factor-α, interleukin-1β, and cyclooxygenase-2 and decreased the activity of nuclear factor kappa B (NF-κB).

Conclusion: These findings indicated that L. reuteri F-9-35 pretreatment can attenuate ethanol-induced gastric injury in rats by inhibiting oxidative stress and inflammatory response. Together, L. reuteri F-9-35 has potential preventive efficacy on gastric ulcer.

Downloads

Download data is not yet available.

References


  1. Heath DB, ed. International handbook on alcohol and culture. Westport: Greenwood Press; 1995.

  2. Huh K, Kwon TH, Shin US, Kim WB, Ahn BO, Oh TY, et al. Inhibitory effects of DA-9601 on ethanol-induced gastrohemorrhagic lesions and gastric xanthine oxidase activity in rats. J Ethnopharmacol 2003; 88(2–3): 269–73.

  3. Chou SP. An examination of the alcohol consumption and peptic ulcer association – results of a national survey. Alcohol Clin Exp Res 1994; 18(1): 149–53.

  4. Rami AB, Fouad AB, Jamil AMM, Mohammed AA, Hadi HA, Mohd AH, et al. In vivo antioxidant and antiulcer activity of Parkia speciosa ethanolic leaf extract against ethanol-induced gastric ulcer in rats. PLoS One 2013; 8(5): e64751.

  5. Asmari AA, Shahrani HA, Masri NA, Faraidi AA, Elfaki I, Arshaduddin M. Vanillin abrogates ethanol induced gastric injury in rats via modulation of gastric secretion, oxidative stress and inflammation. Toxicol Rep 2016; 3: 105–13.

  6. Vitetta L, Briskey D, Alford H, Hall S, Coulson S. Probiotics, prebiotics and the gastrointestinal tract in health and disease. Inflammopharmacology 2014; 22(3): 135–54.

  7. Lam EK, Yu L, Wong HP, Wu WK, Shin VY, Tai EK, et al. Probiotic Lactobacillus rhamnosus GG enhances gastric ulcer healing in rats. Eur J Pharmacol 2007; 565(1–3): 171–9.

  8. Lam EK, Tai EK, Koo MW, Wong HP, Wu WK, Yu L, et al. Enhancement of gastric mucosal integrity by Lactobacillus rhamnosus GG. Life Sci 2007; 80(23): 2128–36.

  9. Dharmani P, De Simone C, Chadee K. The probiotic mixture VSL#3 accelerates gastric ulcer healing by stimulating vascular endothelial growth factor. PLoS One 2013; 8(3): e58671.

  10. Kwon EK, Kang GD, Kim WK, Han MJ, Kim DH. Lactobacillus plantarum LC27 and Bifidobacterium longum LC67 simultaneously alleviate ethanol-induced gastritis and hepatic injury in mice. J Funct Foods 2017; 38: 389–98.

  11. Mu Q, Tavella VJ, Luo XM. Role of Lactobacillus reuteri in human health and diseases. Front Microbiol 2018; 9: 757.

  12. Hao HW, Zhang TH, Sun MC. A space flight-induced mutant L. reuteri F-9-35 and its application. China Patent; No. CN107828703A; 2018.

  13. Jin SE, Lee MY, Shin IS, Jeon WY, Ha H. Syzygium aromaticum water extract attenuates ethanolinduced gastric injury through antioxidant effects in rats. Mol Med Rep 2016; 14(1): 361–6.

  14. Park SW, Oh TY, Kim YS, Sim H, Park SJ, Jang EJ, et al. Artemisia asiatica extracts protect against ethanol-induced injury in gastric mucosa of rats. J Gastroenterol Hepatol 2008; 23(6): 976–84.

  15. Yang J, Zhou W, Gu Y, Dai J, Li X, Tai P, et al. Protective effect of Pu-erh tea extracts against ethanol-induced gastric mucosal damage in rats. Biomedical Rep 2018; 8(4): 335–42.

  16. Jahovic N, Erkanlı G, İşeri S, Arbak S, Alican İ. Gastric protection by α-melanocyte-stimulating hormone against ethanol in rats: involvement of somatostatin. Life Sci 2007; 80(11): 1040–5.

  17. Corne SJ, Morrissey SM, Woods RJ. Proceedings: a method for the quantitative estimation of gastric barrier mucus. J Physiol 1974; 242(2): 116P–17P.

  18. Ali MS, Neisi N, Darbor M, Hassanpour M, Makvandi M, Solgi G. β-carotene protects the gastric mucosa against ischemia-reperfusion injury in rats. Eur Cytokine Netw 2012; 23(4): 173–8.

  19. Konturek PC, Brzozowski T, Pajdo R, Nikiforuk A, Kwiecien S, Harsch I, et al. Ghrelin-a new gastroprotective factor in gastric mucosa. J Physiol Pharmacol 2004; 55(2): 325–36.

  20. Tamura M, Matsui H, Kaneko T, Hyodo I. Alcohol is an oxidative stressor for gastric epithelial cells: detection of superoxide in living cells. J Clin Biochem Nutr 2013; 53(2): 75–80.

  21. Santos FA, Rao VS. 1,8-cineol, a food flavoring agent, prevents ethanol-induced gastric injury in rats. Dig Dis Sci 2001; 46(2): 331–7.

  22. Almeida LR, Costa PS, Ama N, Reis M, Barros KO, Alvim LB, et al. Porcine stomachs with and without gastric ulcer differ in Lactobacillus load and strain characteristics. Can J Microbiol 2018; 64(7): 493–9.

  23. Shorrock CJ, Rees WD. Overview of gastroduodenal mucosal protection. Am J Med 1988; 84(2a): 25–34.

  24. Slomiany A, Morita M, Sano S, Piotrowski J, Skrodzka D, Slomiany BL. Effect of ethanol on gastric mucus glycoprotein synthesis, translocation, transport, glycosylation, and secretion. Alcohol Clin Exp Res 1997; 21(3): 417–23.

  25. Lindi C, Marciani P, Montorfano G, Omodeosale F. Age-related effects of chronic ethanol intake on physical properties, lipid composition and galactosyltransferase activity of rat small intestine microsomes. Alcohol Alcohol 1996; 31(2): 183–9.

  26. Petersson J. Nitrate, nitrite and nitric oxide in gastric mucosal defense. Doctor; Uppsala University, 2008.

  27. Yang HJ, Kim MJ, Kwon DY, Kang ES, Kang S, Park S. Gastroprotective actions of Taraxacum coreanum Nakai water extracts in ethanol-induced rat models of acute and chronic gastritis. J Ethnopharmacol 2017; 208: 84–93.

  28. Sibilia V, Pagani F, Lattuada N, De LV, Guidobono F, Soglian A, et al. Ticlopidine prevents the formation but delays the healing of ethanol-induced gastric lesions in the rat. Pharmacol Res 2007; 55(5): 418–25.

  29. Arab HH, Salama SA, Omar HA, El-Sa A, Maghrabi IA. Diosmin protects against ethanol-induced gastric injury in rats: novel anti-ulcer actions. PLoS One 2015; 10(3): e0122417.

  30. Liu Y, Liang J, Wu J, Chen H, Zhang Z, Yang H, et al. Transformation of patchouli alcohol to beta-patchoulene by gastric juice: β-patchoulene is more effective in preventing ethanol-induced gastric injury. Sci Rep 2017; 7(1): 5591.

  31. Ibrahim IAA, Abdulla MA, Hajrezaie M, Bader A, Shahzad N, Al-Ghamdi SS, et al. The gastroprotective effects of hydroalcoholic extract of Monolluma quadrangula against ethanol-induced gastric mucosal injuries in Sprague Dawley rats. Drug Design Dev Ther 2016; 10: 93–105.

  32. Konturek SJ, Brzozowski T, Majka J, Pytko-Polonczyk J, Stachura J. Inhibition of nitric oxide synthase delays healing of chronic gastric ulcers. Eur J Pharmacol 1993; 239(1–3): 215–17.

  33. Shen Y, Jia S, Chao N, Yu D, Chen Z, Cong W, et al. Mechanistic evaluation of gastroprotective effects of Kangfuxin on ethanol-induced gastric ulcer in mice. Chem Biol Interact 2017; 273: 115–24.

  34. Chang X, Luo F, Jiang W, Zhu L, Gao J, He H, et al. Protective activity of salidroside against ethanol-induced gastric ulcer via the MAPK/NF-κB pathway in vivo and in vitro. Int Immunopharmacol 2015; 28(1): 604–15.

  35. Wang QS, Zhu XN, Jiang HL, Wang GF, Cui YL. Protective effects of alginate-chitosan microspheres loaded with alkaloids from Coptis chinensis Franch. and Evodia rutaecarpa (Juss.) Benth. (Zuojin Pill) against ethanol-induced acute gastric mucosal injury in rats. Drug Des Devel Ther 2015; 9: 6151–65.

  36. Zhao W, Zhu FW, Fu A, Zheng L, Yan Z, Zhao L, et al. Protective effects of DIDS against ethanol-induced gastric mucosal injury in rats. Acta Biochim Biophys Sin 2009; 41(4): 301–8.

  37. Keshk WA, Zahran SM, Katary MA, Da EAA. Modulatory effect of silymarin on nuclear factor-erythroid-2-related factor 2 regulated redox status, nuclear factor-κB mediated inflammation and apoptosis in experimental gastric ulcer. Chem Biol Interact 2017; 273: 266–72.

  38. Piao X, Li S, Sui L, Guo L, Liu X, Li H, et al. 1-Deoxynojirimycin (DNJ) Ameliorates indomethacin-induced gastric ulcer in mice by affecting NF-kappaB signaling pathway. Front Pharmacol 2018; 9: 372.

  39. Li JH, Ju GX, Jiang JL, Li NS, Peng J, Luo XJ. Lipoic acid protects gastric mucosa from ethanol-induced injury in rat through a mechanism involving aldehyde dehydrogenase 2 activation. Alcohol 2016; 56: 21–8.

  40. Luo XJ, Liu B, Dai Z, Li TB, Li NS, Zhang XJ, et al. Expression of apoptosis-associated microRNAs in ethanol-induced acute gastric mucosal injury via JNK pathway. Alcohol 2013; 47(6): 481–93.

  41. Wang Y, Liu Y, Sidhu A, Ma Z, Mcclain C, Feng W. Lactobacillus rhamnosus GG culture supernatant ameliorates acute alcohol-induced intestinal permeability and liver injury. Am J Physiol Gastrointest Liver Physiol 2012; 303(1): G32–41.

  42. Videla LA, Fernandez V, Ugarte G, Valenzuela A. Effect of acute ethanol intoxication on the content of reduced glutathione of the liver in relation to its lipoperoxidative capacity in the rat. FEBS Lett 1980; 111(1): 6–10.

  43. Hashimoto S, Recknagel RO. No chemical evidence of hepatic lipid peroxidation in acute ethanol toxicity. Exp Mol Pathol 1968; 8(2): 225–42.

  44. Nordmann R, Ribiere C, Rouach H. Implication of free radical mechanisms in ethanol-induced cellular injury. Free Radic Biol Med 1992; 12(3): 219–40.

Published
2018-10-29
How to Cite
1.
Sun M-C, Hou P-P, Wang X-Y, Zhao C-H, Cheng B-J, Wang Y-L, Hao H-W, Zhang T-H, Ye H-Q. Pretreatment with <em>Lactobacillus reuteri</em&gt; F-9-35 attenuates ethanol-induced gastric injury in rats. fnr [Internet]. 2018Oct.29 [cited 2018Nov.19];620. Available from: https://foodandnutritionresearch.net/index.php/fnr/article/view/1469
Section
Original Articles