Advertisement

Digestive Diseases and Sciences

, Volume 56, Issue 12, pp 3534–3545 | Cite as

Lemon Verbena Infusion Consumption Attenuates Oxidative Stress in Dextran Sulfate Sodium-Induced Colitis in the Rat

  • Loïc Lenoir
  • Adrien Rossary
  • Juliette Joubert-Zakeyh
  • Juliette Vergnaud-Gauduchon
  • Marie-Chantal Farges
  • Didier Fraisse
  • Odile Texier
  • Jean-Louis Lamaison
  • Marie-Paule Vasson
  • Catherine FelginesEmail author
Original Article

Abstract

Background

Inflammatory bowel diseases (IBD) consist of an uncontrolled intestinal inflammation leading to mucosal disruption. This inflammation is accompanied by an excessive production of reactive oxygen species (ROS). Polyphenols are micronutrients with antioxidative and anti-inflammatory properties, and may play an interesting role in the prevention of intestinal inflammation. Lemon verbena (Aloysia triphylla) infusion is a popular herbal infusion rich in polyphenols (flavones and verbascoside).

Aims

This study evaluated the preventive effects of lemon verbena infusion consumption against mild-to-moderate dextran sulfate sodium (DSS)-induced colitis in rats.

Methods

Wistar rats drank water or lemon verbena infusion for 14 days. On day 15, half of the rats received DSS (4%) in their drink for 7 days. At the end of the experimental period, the colon was taken for histopathological examination and determination of myeloperoxidase (MPO) activity, antioxidant enzyme activities (superoxide dismutase [SOD], glutathione peroxidase [GPx], glutathione reductase [GR], catalase [CAT]), glutathione and lipid peroxidation. Lymphocyte populations were determined in blood, mesenteric nodes and Peyer’s patches.

Results

Rats ingested daily 5.6 μmol of polyphenols. DSS reduced food intake and induced colitis, as reflected by histological lesions and increased MPO activity. Although these alterations were not significantly counteracted by lemon verbena consumption, the herbal infusion increased colonic SOD activity and decreased lipid peroxidation (malondialdehyde). Other oxidative stress markers (GPx, GR, CAT, glutathione) were not significantly modified.

Conclusion

Our study shows that the preventive consumption of lemon verbena infusion offered some antioxidative protection during experimental colitis by stimulating SOD activity and decreasing lipid peroxidation.

Keywords

Lemon verbena Polyphenols Dextran sodium sulfate Colitis Oxidative stress Rat 

Notes

Acknowledgements

This work was funded by 3inature BIOSPHERE.

References

  1. 1.
    Sands BE. Inflammatory bowel disease: past, present, and future. J Gastroenterol. 2007;42:16–25.PubMedCrossRefGoogle Scholar
  2. 2.
    Kruidenier L, Verspaget HW. Review article: oxidative stress as a pathogenic factor in inflammatory bowel disease—radicals or ridiculous? Aliment Pharmacol Ther. 2002;16:1997–2015.PubMedCrossRefGoogle Scholar
  3. 3.
    Damiani CR, Benetton CA, Stoffel C, Bardini KC, Cardoso VH, Di Giunta G, Pinho RA, Dal-Pizzol F, Streck EL. Oxidative stress and metabolism in animal model of colitis induced by dextran sulfate sodium. J Gastroenterol Hepatol. 2007;22:1846–1851.PubMedCrossRefGoogle Scholar
  4. 4.
    Buffinton GD, Doe WF. Depleted mucosal antioxidant defences in inflammatory bowel disease. Free Radic Biol Med. 1995;19:911–918.PubMedCrossRefGoogle Scholar
  5. 5.
    Koutroubakis IE, Malliaraki N, Dimoulios PD, Karmiris K, Castanas E, Kouroumalis EA. Decreased total and corrected antioxidant capacity in patients with inflammatory bowel disease. Dig Dis Sci. 2004;49:1433–1437.PubMedCrossRefGoogle Scholar
  6. 6.
    Trebble TM, Arden NK, Wootton SA, Calder PC, Mullee MA, Fine DR, Stroud MA. Fish oil and antioxidants alter the composition and function of circulating mononuclear cells in Crohn disease. Am J Clin Nutr. 2004;80:1137–1144.PubMedGoogle Scholar
  7. 7.
    Aghdassi E, Wendland BE, Steinhart AH, Wolman SL, Jeejeebhoy K, Allard JP. Antioxidant vitamin supplementation in Crohn’s disease decreases oxidative stress. A randomized controlled trial. Am J Gastroenterol. 2003;98:348–353.PubMedGoogle Scholar
  8. 8.
    Seidner DL, Lashner BA, Brzezinski A, Banks PL, Goldblum J, Fiocchi C, Katz J, Lichtenstein GR, Anton PA, Kam LY, Garleb KA, Demichele SJ. An oral supplement enriched with fish oil, soluble fiber, and antioxidants for corticosteroid sparing in ulcerative colitis: a randomized, controlled trial. Clin Gastroenterol Hepatol. 2005;3:358–369.PubMedCrossRefGoogle Scholar
  9. 9.
    González-Gallego J, García-Mediavilla MV, Sánchez-Campos S, Tuñón MJ. Fruit polyphenols, immunity and inflammation. Br J Nutr. 2010;104:S15–S27.PubMedCrossRefGoogle Scholar
  10. 10.
    Del Rio D, Costa LG, Lean ME, Crozier A. Polyphenols and health: what compounds are involved? Nutr Metab Cardiovasc Dis. 2010;20:1–6.PubMedCrossRefGoogle Scholar
  11. 11.
    Romier B, Schneider YJ, Larondelle Y, During A. Dietary polyphenols can modulate the intestinal inflammatory response. Nutr Rev. 2009;67:363–378.PubMedCrossRefGoogle Scholar
  12. 12.
    Shapiro H, Singer P, Halpern Z, Bruck R. Polyphenols in the treatment of inflammatory bowel disease and acute pancreatitis. Gut. 2007;56:426–435.PubMedCrossRefGoogle Scholar
  13. 13.
    Atoui AK, Mansouri A, Boskou G, Kefalas P. Tea and herbal infusions: their antioxidant activity and phenolic profile. Food Chem. 2005;89:27–36.CrossRefGoogle Scholar
  14. 14.
    Teuscher E, Anton R, Lobstein A. Plantes aromatiques. Paris: Lavoisier; 2005.Google Scholar
  15. 15.
    Valentão P, Fernandes E, Carvalho F, Andrade PB, Seabra RM, de Lourdes Basto M. Studies on the antioxidant activity of Lippia citriodora infusion: scavenging effect on superoxide radical, hydroxyl radical and hypochlorous acid. Biol Pharm Bull. 2002;25:1324–1327.PubMedCrossRefGoogle Scholar
  16. 16.
    Bilia AR, Giomi M, Innocenti M, Gallori S, Vincieri FF. HPLC-DAD-ESI-MS analysis of the constituents of aqueous preparations of verbena and lemon verbena and evaluation of the antioxidant activity. J Pharm Biomed Anal. 2008;46:463–470.PubMedCrossRefGoogle Scholar
  17. 17.
    Zamorano-Ponce E, Morales C, Ramos D, Sepúlveda C, Cares S, Rivera P, Fernández J, Carballo MA. Anti-genotoxic effect of Aloysia triphylla infusion against acrylamide-induced DNA damage as shown by the comet assay technique. Mutat Res. 2006;603:145–150.PubMedGoogle Scholar
  18. 18.
    Carnat A, Carnat AP, Fraisse D, Lamaison JL. The aromatic and polyphenolic composition of lemon verbena tea. Fitoterapia. 1999;70:44–49.CrossRefGoogle Scholar
  19. 19.
    Mazzon E, Esposito E, Di Paola R, Riccardi L, Caminiti R, Dal Toso R, Pressi G, Cuzzocrea S. Effects of verbascoside biotechnologically produced by Syringa vulgaris plant cell cultures in a rodent model of colitis. Naunyn Schmiedebergs Arch Pharmacol. 2009;380:79–94.PubMedCrossRefGoogle Scholar
  20. 20.
    Hausmann M, Obermeier F, Paper DH, Balan K, Dunger N, Menzel K, Falk W, Schoelmerich J, Herfarth H, Rogler G. In vivo treatment with the herbal phenylethanoid acteoside ameliorates intestinal inflammation in dextran sulphate sodium-induced colitis. Clin Exp Immunol. 2007;148:373–381.PubMedCrossRefGoogle Scholar
  21. 21.
    Ashokkumar P, Sudhandiran G. Protective role of luteolin on the status of lipid peroxidation and antioxidant defense against azoxymethane-induced experimental colon carcinogenesis. Biomed Pharmacother. 2008;62:590–597.PubMedCrossRefGoogle Scholar
  22. 22.
    Steghens JP, Flourié F, Arab K, Collombel C. Fast liquid chromatography-mass spectrometry glutathione measurement in whole blood: micromolar GSSG is a sample preparation artifact. J Chromatogr B Analyt Technol Biomed Life Sci. 2003;798:343–349.PubMedCrossRefGoogle Scholar
  23. 23.
    Steghens JP, van Kappel AL, Denis I, Collombel C. Diaminonaphtalene, a new highly specific reagent for HPLC-UV measurement of total and free malondialdehyde in human plasma or serum. Free Radic Biol Med. 2001;31:242–249.PubMedCrossRefGoogle Scholar
  24. 24.
    Pérez-Jiménez J, Fezeu L, Touvier M, Arnault N, Manach C, Hercberg S, Galan P, Scalbert A. Dietary intake of 337 polyphenols in French adults. Am J Clin Nutr. 2011;93:1220–1228.PubMedCrossRefGoogle Scholar
  25. 25.
    Gaudio E, Taddei G, Vetuschi A, Sferra R, Frieri G, Ricciardi G, Caprilli R. Dextran sulfate sodium (DSS) colitis in rats: clinical, structural, and ultrastructural aspects. Dig Dis Sci. 1999;44:1458–1475.PubMedCrossRefGoogle Scholar
  26. 26.
    Cooper HS, Murthy SN, Shah RS, Sedergran DJ. Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab Invest. 1993;69:238–249.PubMedGoogle Scholar
  27. 27.
    Kitajima S, Takuma S, Morimoto M. Tissue distribution of dextran sulfate sodium (DSS) in the acute phase of murine DSS-induced colitis. J Vet Med Sci. 1999;61:67–70.PubMedCrossRefGoogle Scholar
  28. 28.
    Holma R, Salmenperä P, Virtanen I, Vapaatalo H, Korpela R. Prophylactic potential of montelukast against mild colitis induced by dextran sulphate sodium in rats. J Physiol Pharmacol. 2007;58:455–467.PubMedGoogle Scholar
  29. 29.
    Koetzner L, Grover G, Boulet J, Jacoby HI. Plant-derived polysaccharide supplements inhibit dextran sulfate sodium-induced colitis in the rat. Dig Dis Sci. 2010;55:1278–1285.PubMedCrossRefGoogle Scholar
  30. 30.
    Kwon KH, Murakami A, Tanaka T, Ohigashi H. Dietary rutin, but not its aglycone quercetin, ameliorates dextran sulfate sodium-induced experimental colitis in mice: attenuation of pro-inflammatory gene expression. Biochem Pharmacol. 2005;69:395–406.PubMedCrossRefGoogle Scholar
  31. 31.
    Arafa HM, Hemeida RA, El-Bahrawy AI, Hamada FM. Prophylactic role of curcumin in dextran sulfate sodium (DSS)-induced ulcerative colitis murine model. Food Chem Toxicol. 2009;47:1311–1317.PubMedCrossRefGoogle Scholar
  32. 32.
    Vowinkel T, Kalogeris TJ, Mori M, Krieglstein CF, Granger DN. Impact of dextran sulfate sodium load on the severity of inflammation in experimental colitis. Dig Dis Sci. 2004;49:556–564.PubMedCrossRefGoogle Scholar
  33. 33.
    Martín AR, Villegas I, La Casa C, de la Lastra CA. Resveratrol, a polyphenol found in grapes, suppresses oxidative damage and stimulates apoptosis during early colonic inflammation in rats. Biochem Pharmacol. 2004;67:1399–1410.PubMedCrossRefGoogle Scholar
  34. 34.
    Cui X, Jin Y, Hofseth AB, Pena E, Habiger J, Chumanevich A, Poudyal D, Nagarkatti M, Nagarkatti PS, Singh UP, Hofseth LJ. Resveratrol suppresses colitis and colon cancer associated with colitis. Cancer Prev Res. 2010;3:549–559.CrossRefGoogle Scholar
  35. 35.
    Karrasch T, Kim JS, Jang BI, Jobin C. The flavonoid luteolin worsens chemical-induced colitis in NF-kappaB (EGFP) transgenic mice through blockade of NF-kappaB-dependent protective molecules. PLoS One. 2007;2:e596.PubMedCrossRefGoogle Scholar
  36. 36.
    Serteyn D, Grulke S, Franck T, Mouithys-Mickalad A, Deby-Dupont G. La myéloperoxydase des neutrophiles, une enzyme de défense aux capacités oxydantes. Ann Méd Vét. 2003;147:79–93.Google Scholar
  37. 37.
    Roessner A, Kuester D, Malfertheiner P, Schneider-Stock R. Oxidative stress in ulcerative colitis-associated carcinogenesis. Pathol Res Pract. 2008;204:511–524.PubMedCrossRefGoogle Scholar
  38. 38.
    Fraga CG, Galleano M, Verstraeten SV, Oteiza PI. Basic biochemical mechanisms behind the health benefits of polyphenols. Mol Aspects Med. 2010;31:435–445.PubMedCrossRefGoogle Scholar
  39. 39.
    Kruidenier L, Kuiper I, Van Duijn W, Mieremet-Ooms MA, van Hogezand RA, Lamers CB, Verspaget HW. Imbalanced secondary mucosal antioxidant response in inflammatory bowel disease. J Pathol. 2003;201:17–27.PubMedCrossRefGoogle Scholar
  40. 40.
    Zhou YH, Yu JP, Liu YF, Teng XJ, Ming M, Lv P, An P, Liu SQ, Yu HG. Effects of Ginkgo biloba extract on inflammatory mediators (SOD, MDA, TNF-alpha, NF-kappaBp65, IL-6) in TNBS-induced colitis in rats. Mediators Inflamm. 2006;2006:92642.PubMedCrossRefGoogle Scholar
  41. 41.
    Seguí J, Gil F, Gironella M, Alvarez M, Gimeno M, Coronel P, Closa D, Piqué JM, Panés J. Down-regulation of endothelial adhesion molecules and leukocyte adhesion by treatment with superoxide dismutase is beneficial in chronic immune experimental colitis. Inflamm Bowel Dis. 2005;11:872–882.PubMedCrossRefGoogle Scholar
  42. 42.
    Singh K, Jaggi AS, Singh N. Exploring the ameliorative potential of Punica granatum in dextran sulfate sodium induced ulcerative colitis in mice. Phytother Res. 2009;23:1565–1574.PubMedCrossRefGoogle Scholar
  43. 43.
    Camuesco D, Gálvez J, Nieto A, Comalada M, Rodríguez-Cabezas ME, Concha A, Xaus J, Zarzuelo A. Dietary olive oil supplemented with fish oil, rich in EPA and DHA (n-3) polyunsaturated fatty acids, attenuates colonic inflammation in rats with DSS-induced colitis. J Nutr. 2005;135:687–694.PubMedGoogle Scholar
  44. 44.
    Oz HS, Chen TS, McClain CJ, de Villiers WJS. Antioxidants as novel therapy in a murine model of colitis. J Nutr Biochem. 2005;16:297–304.PubMedCrossRefGoogle Scholar
  45. 45.
    Egger B, Bajaj-Elliott M, MacDonald TT, Inglin R, Eysselein VE, Büchler MW. Characterisation of acute murine dextran sodium sulphate colitis: cytokine profile and dose dependency. Digestion. 2000;62:240–248.PubMedCrossRefGoogle Scholar
  46. 46.
    Shi XZ, Winston JH, Sarna SK. Differential immune and genetic responses in rat models of Crohn’s colitis and ulcerative colitis. Am J Physiol Gastrointest Liver Physiol. 2011;300:G41–G51.PubMedCrossRefGoogle Scholar
  47. 47.
    Vicario M, Amat C, Rivero M, Moretó M, Pelegrí C. Dietary glutamine affects mucosal functions in rats with mild DSS-induced colitis. J Nutr. 2007;137:1931–1937.PubMedGoogle Scholar
  48. 48.
    Pérez-Bosque A, Pelegrí C, Vicario M, Castell M, Russell L, Campbell JM, Quigley JD 3rd, Polo J, Amat C, Moretó M. Dietary plasma protein affects the immune response of weaned rats challenged with S. aureus superantigen B. J. Nutr. 2004;134:2667–2672.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Loïc Lenoir
    • 1
    • 4
  • Adrien Rossary
    • 2
  • Juliette Joubert-Zakeyh
    • 3
  • Juliette Vergnaud-Gauduchon
    • 2
  • Marie-Chantal Farges
    • 2
  • Didier Fraisse
    • 1
  • Odile Texier
    • 1
  • Jean-Louis Lamaison
    • 1
  • Marie-Paule Vasson
    • 2
  • Catherine Felgines
    • 1
    Email author
  1. 1.Laboratoire de Pharmacognosie et Phytothérapie, Faculté de PharmacieClermont Université, Université d’Auvergne, EA 4233Clermont-FerrandFrance
  2. 2.Laboratoire de Biochimie, Biologie Moléculaire et NutritionClermont Université, Université d’Auvergne Clermont-FerrandFrance
  3. 3.Service d’Anatomie et de Cytologie PathologiquesCHU Clermont-FerrandClermont-FerrandFrance
  4. 4.3inature BIOSPHERE (M. Dubourdeaux), Le NaturopôleSaint-Bonnet-de-RochefortFrance

Personalised recommendations