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



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).


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


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.


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.


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.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6


  1. 1.

    Sands BE. Inflammatory bowel disease: past, present, and future. J Gastroenterol. 2007;42:16–25.

    PubMed  Article  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google Scholar 

  4. 4.

    Buffinton GD, Doe WF. Depleted mucosal antioxidant defences in inflammatory bowel disease. Free Radic Biol Med. 1995;19:911–918.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  CAS  Google 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.

    PubMed  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  Article  CAS  Google 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.

    Article  CAS  Google 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.

    PubMed  Article  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  CAS  Google 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.

    Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  Google 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.

    Article  CAS  Google 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.

    PubMed  Article  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  CAS  Google 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.

    PubMed  Google Scholar 

Download references


This work was funded by 3inature BIOSPHERE.

Author information



Corresponding author

Correspondence to Catherine Felgines.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Lenoir, L., Rossary, A., Joubert-Zakeyh, J. et al. Lemon Verbena Infusion Consumption Attenuates Oxidative Stress in Dextran Sulfate Sodium-Induced Colitis in the Rat. Dig Dis Sci 56, 3534–3545 (2011). https://doi.org/10.1007/s10620-011-1784-x

Download citation


  • Lemon verbena
  • Polyphenols
  • Dextran sodium sulfate
  • Colitis
  • Oxidative stress
  • Rat