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Lactobacillus rhamnosus GG antagonizes Giardia intestinalis induced oxidative stress and intestinal disaccharidases: an experimental study

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Abstract

The present study describes the in vivo modulatory potential of Lactobacillus rhamnosus GG (LGG), an effective probiotic, in Giardia intestinalis-infected BALB/c mice. Experimentally, it was observed that oral administration of lactobacilli prior or simultaneous with Giardia trophozoites to mice, efficiently (p < 0.05) reduced both the severity and duration of giardiasis. More specifically, probiotics fed, Giardia-infected mice, showed a significant increase in the levels of antioxidants [reduced glutathione (GSH) and superoxide dismutase (SOD)] and intestinal disaccharidases [sucrase and lactase] and decreased levels of oxidants in the small intestine, in comparison with Giardia-infected mice. Histopathological findings also revealed almost normal cellular morphology of the small intestine in probiotic-fed Giardia-infected mice compared with fused enterocytes, villous atrophy and increased infiltration of lymphocytes in Giardia-infected mice. The results of the present study has shed new light on the anti-oxidative properties of LGG in Giardia mediated tissue injury, thereby suggesting that the effects of probiotic LGG are biologically plausible and could be used as an alternative microbial interference therapy.

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Abbreviations

LGG:

Lactobacillus rhamnosus GG

GSH:

Reduced glutathione

SOD:

Superoxide dismutase

ALP:

Alkaline phosphatase

PBS:

Phosphate buffered saline

References

  • Archibald FS, Fridovich I (1981) Manganese, superoxide dismutase, and oxygen tolerance in some lactic acid bacteria. J Bacteriol 146:928–936

    CAS  Google Scholar 

  • Bergmeyer HU (1963) Methods of enzymatic analysis. Academic Press, Inc., New York

    Google Scholar 

  • Bergonzelli GE, Blum S, Brussow H, Corthesy-Theulaz I (2005) Probiotics as a treatment strategy for gastrointestinal diseases. Digestion 72:57–68

    Article  Google Scholar 

  • Buret AG (2007) Mechanisms of epithelial dysfunction in giardiasis. Gut 56:316–317

    Article  CAS  Google Scholar 

  • Carmen S, Alejandra MB, Miyoshi A, Rocha CS, Azevedo V, LeBlanc JG (2011) Oxidative stress-induced cell cycle blockage and a protease independent programmed cell death in microaerophilic Giardia lamblia. Drug Des Devel Ther 3:103–110

    Google Scholar 

  • Céu Sousa MC, Goncalves CA, Bairos VA, Poiares-Da-Silva J (2001) Adherence of Giardia lamblia trophozoites to Int-407 human intestinal cells. Clin Diagn Lab Immunol 8:258–265

    Google Scholar 

  • Dahlquist A (1964) Method for assay of intestinal disaccharides. Anal Biochem 1:18–25

    Article  Google Scholar 

  • Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–75

    Article  CAS  Google Scholar 

  • Gardner TB, Hill DR (2001) Treatment of giardiasis. Clin Microbiol Rev 14:114–128

    Article  CAS  Google Scholar 

  • Gillin FD, Diamond LS (1981) Inhibition of clonal growth of Giardia lamblia and Entamoeba histolytica by metronidazole, quinacrine, and other antimicrobial agents. J Antimicrob Chemother 8:305–316

    Article  CAS  Google Scholar 

  • Goyal N, Tiwari RP, Shukla G (2011). Lactobacillus rhamnosus GG as an effective probiotic for murine giardiasis. Interdiscip Perspect Infect Dis doi:10.1155/2011/795219

  • Han W, Mercenier A, Ait-Belgnaoui A, Pavan S, Lamine F, van Swam II, Kleerebezem M, Salvador-Cartier C, Hisbergues M, Bueno L, Theodorou V, Fioramonti J (2006) Improvement of an experimental colitis in rats by lactic acid bacteria producing superoxide dismutase. Inflamm Bowel Dis 12:1044–1052

    Article  Google Scholar 

  • Heyman M, Menard S (2002) Probiotic microorganisms: how they affect intestinal pathophysiology. Cell Mol Life Sci 59:1151–1165

    Article  CAS  Google Scholar 

  • Humen MA, De Antoni GL, Benyacoub J et al (2005) Lactobacillus johnsonii La1 antagonizes Giardia intestinalis in vivo. Infect Immun 73:1265–1269

    Article  CAS  Google Scholar 

  • James PS, Smith MW, Tivey DR, Wilson TJG (1987) Epidermal growth factor selectively increases maltase and sucrase activities in neonatal piglet intestine. J Physiol 393:583–594

    CAS  Google Scholar 

  • Katelaris PH, Naeem A, Farthing MJ (1995) Attachment of Giardia lamblia trophozoites to a cultured human intestinal cell line. Gut 37:512–528

    Article  CAS  Google Scholar 

  • Kessler M, Acuto O, Storelli C, Murer H, Muller M, Semenza G (1978) Modified procedure for rapid preparation of efficiently transporting vesicles from small intestinal brush border membranes. Biochim Biophys Acta 506:136–154

    Article  CAS  Google Scholar 

  • Khanna R, Vinayak VK, Mehta S, Kumkum Nain CK (1988) Giardia lamblia infection in immuno suppressed animals causes severe alterations to brush border membrane enzymes. Dig Dis Sci 33:1147–1152

    Article  CAS  Google Scholar 

  • Kono Y (1978) Generation of superoxide radical during auto-oxidation of hydroxylamine and an assay for superoxide dismutase. Arch Biochem Biophys 186:189–195

    Article  CAS  Google Scholar 

  • Kruidenier L, Kuiper I, Lamers CB, Verspaget HW (2003) Intestinal oxidative damage in inflammatory bowel disease: semi-quantification, localization, and association with mucosal antioxidants. J Pathol 201:28–36

    Article  CAS  Google Scholar 

  • Lemee V, Zaharia I, Nevez G, Rabodonirina M, Brasseur P, Ballet JJ, Favennec L (2000) Metronidazole and albendazole susceptibility of 11 clinical isolates of Giardia duodenalis from France. J Antimicrob Chemother 46:819–821

    Article  CAS  Google Scholar 

  • Lih-Brody L, Powell SR, Collier KP et al (1996) Increased oxidative stress and decrease antioxidant defenses in mucosa of inflammatory bowel disease. Dig Dis Sci 41:2078–2086

    Article  CAS  Google Scholar 

  • Lin AM, Chyi BY, Wu LY, Hwang LS, Ho LT (1998) The antioxidative property of green tea against iron-induced oxidative stress in rat brain. Chin J Physiol 41:189–194

    CAS  Google Scholar 

  • Mastronicola D, Giuffre A, Testa F, Mura A et al (2011) Giardia intestinalis escapes oxidative stress by colonizing the small intestine: a molecular hypothesis. IUBMB Life 63:21–25

    Article  CAS  Google Scholar 

  • Peran L, Sierra S, Comalada M et al (2007) A comparative study of the preventative effect exerted by two probiotics, Lactobacillus reuteri and Lactobacillus fermentum, in the trinitrobenzenesulfonic acid model of rat colitis. Br J Nutr 97:96–103

    Article  CAS  Google Scholar 

  • Pérez PF, Minnaard J, Rouvet R, Knabenhans C et al (2001) Inhibition of Giardia intestinalis by extracellular factors from lactobacilli: an in vitro study. Appl Environ Microbiol 67:5037–5042

    Article  Google Scholar 

  • Ratanapo S, Mungthin M, Soontrapa S (2008) Multiple modes of transmission of giardiasis in primary school children of a rural community, Thailand. Am J Trop Med Hyg 78:611–615

    Google Scholar 

  • Shukla G, Sidhu RK (2011) Lactobacillus casei as a probiotic in malnourished Giardia lamblia-infected mice: a biochemical and histopathological study. Can J Microbiol 57:127–135

    Article  CAS  Google Scholar 

  • Shukla G, Devi P, Sehgal R (2008) Effect of Lactobacillus casei as a probiotic on modulation of giardiasis. Dig Dis and Sci 53:2671–2679

    Article  Google Scholar 

  • Shukla G, Kaur T, Sehgal R, Rishi P, Prabha V (2010a) Protective potential of Lactobacillus acidophilus, a biotherapeutic agent in murine giardiasis. Cent Eur J Med 5:456–463

    Article  Google Scholar 

  • Shukla G, Sharma G, Goyal N (2010b) Probiotic characterization of lactobacilli and yeast strains isolated from whey beverage and therapeutic potential of Lactobacillus yoghurt in murine giardiasis. Am J Biomed Sci 2:248–261

    Article  Google Scholar 

  • Southcott E, Tooley KL, Howarth GS, Davidson GP, Butler RN (2008) Yoghurts containing probiotics reduces disruption of the small intestinal barrier in methotrexate-treated rats. Dig Dis Sci 53:1837–1841

    Article  CAS  Google Scholar 

  • Wills ED (1966) Mechanisms of lipid peroxide formation in animal tissues. Biochem J 99:667–676

    CAS  Google Scholar 

  • Windrow VR, Winyard PG, Morris CJ, Blake DR (1993) Free radicals in inflammation: second messengers and mediators of tissue destruction. Br Med Bull 49:506–522

    Google Scholar 

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Acknowledgments

The authors are thankful to Mr. Bhandari, Senior technician, PGIMER, Chandigarh, India for maintaining and providing Giardia intestinalis culture. The work was supported by funding from Indian the Council of Medical Research, New Delhi, India.

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Authors and Affiliations

  1. Department of Microbiology, Panjab University, Chandigarh, 160014, India

    Nisha Goyal, Praveen Rishi & Geeta Shukla

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  1. Nisha Goyal
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  2. Praveen Rishi
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  3. Geeta Shukla
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Correspondence to Geeta Shukla.

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Goyal, N., Rishi, P. & Shukla, G. Lactobacillus rhamnosus GG antagonizes Giardia intestinalis induced oxidative stress and intestinal disaccharidases: an experimental study. World J Microbiol Biotechnol 29, 1049–1057 (2013). https://doi.org/10.1007/s11274-013-1268-6

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  • DOI: https://doi.org/10.1007/s11274-013-1268-6

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