Digestive Diseases and Sciences

, Volume 56, Issue 2, pp 285–294 | Cite as

Antioxidant Properties of Probiotics and Their Protective Effects in the Pathogenesis of Radiation-Induced Enteritis and Colitis

  • Basileios G. Spyropoulos
  • Evangelos P. Misiakos
  • Constantine Fotiadis
  • Christos N. Stoidis
Review

Abstract

Radiation therapy has become one of the most important treatment modalities for human malignancy, but certain immediate and delayed side-effects on the normal surrounding tissues limit the amount of effective radiation that can be administered. After exposure of the abdominal region to ionizing radiation, nearly all patients experience transient symptoms of irradiation of the bowel. Acute-phase symptoms may persist for a short time, yet long-term complications can represent significant clinical conditions with high morbidity. Data from both experimental studies and clinical trials suggest the potential benefit for probiotics in radiation-induced enteritis and colitis. On the other hand, it is well evidenced that both useful and harmful effects of therapeutic applications of ionizing radiation upon living systems are ascribed to free-radical production. Therefore, the hypothesis that probiotics reinforce antioxidant defense systems of normal mucosal cells exposed to ionizing radiation may explain to an extent their beneficial action. The aim of this review is threefold: First, to make a short brief into the natural history of radiation injury to the intestinal tract. Second, to describe the primary interaction of ionizing radiation at the cellular level and demonstrate the participation of free radicals in the mechanisms of injury and, third, to try a more profound investigation into the antioxidant abilities of probiotics and prebiotics based on the available experimental and clinical data.

Keywords

Radiation enteritis Radiation colitis Oxidative stress Probiotics Prebiotics 

Notes

Acknowledgments

The authors state that there was no extra-institutional funding. Supported by the National and Kapodιstrian University of Athens, Athens, Greece.

Competing interests

The authors declare that they have no competing interests.

Authors’ contributions

BGS, EPM, CNS, and CF have made contributions to conception and design. BGS and EPM contributed to the analysis and interpretation of data and wrote the manuscript. All authors read and approved the final manuscript. All authors contributed equally to the final draft of the manuscript. CF has given the final approval of the version to be published.

References

  1. 1.
    Ballas LK, Elkin EB, Schrag D, Minsky BD, Bach PB. Radiation therapy facilities in the United States. Int J Radiat Oncol Biol Phys. 2006;66:1204–1211.PubMedCrossRefGoogle Scholar
  2. 2.
    Wang J, Boerma M, Fu Q, Hauer-Jensen M. Significance of endothelial dysfunction in the pathogenesis of early and delayed radiation enteropathy. World J Gastroenterol. 2007;13:3047–3055.PubMedGoogle Scholar
  3. 3.
    Vozenin-Brotons MC. Tissue toxicity induced by ionizing radiation to the normal intestine: understanding the pathophysiological mechanisms to improve the medical management. World J Gastroenterol. 2007;13:3031–3032.PubMedGoogle Scholar
  4. 4.
    Berthrong M. Pathologic changes secondary to radiation. World J Surg. 1986;10:155–170.PubMedCrossRefGoogle Scholar
  5. 5.
    Bismar MM, Sinicrope FA. Radiation enteritis. Curr Gastroenterol Rep. 2002;4:361–365.PubMedCrossRefGoogle Scholar
  6. 6.
    Stone HB, Coleman CN, Anscher MS, McBride WH. Effects of radiation on normal tissue: consequences and mechanisms. Lancet Oncol. 2003;4:529–536.PubMedCrossRefGoogle Scholar
  7. 7.
    Akpolat M, Kanter M, Uzal MC. Protective effects of curcumin against gamma radiation-induced ileal mucosal damage. Arch Toxicol. 2009;83:609–617.PubMedCrossRefGoogle Scholar
  8. 8.
    Denham JW, Hauser-Jensen M. The radiotherapeutic injury-a complex ‘wound’. Radiother Oncol. 2002;63:129–145.PubMedCrossRefGoogle Scholar
  9. 9.
    Zhao W, Robbins ME. Inflammation and chronic oxidative stress in radiation-induced late normal tissue injury: therapeutic implications. Curr Med Chem. 2009;16:130–143.PubMedCrossRefGoogle Scholar
  10. 10.
    Weiss JF, Landauer MR. Radioprotection by antioxidants. Ann NY Acad Sci. 2000;899:44–60.PubMedCrossRefGoogle Scholar
  11. 11.
    Weiss JF. Pharmacologic approaches to protection against radiation-induced lethality and other damage. Environ Health Perspect. 1997;105:1473–1478.PubMedCrossRefGoogle Scholar
  12. 12.
    Nair CKK, Parida DK, Nomura T. Radioprotectors in radiotherapy. J Radiat Res. 2001;42:21–37.PubMedCrossRefGoogle Scholar
  13. 13.
    Wu W, Abraham L, Ogony J, Matthews R, Goldstein G, Ercal N. Effects of N-acetylcysteine amide (NACA), a thiol antioxidant on radiation-induced cytotoxicity in Chinese hamster ovary cells. Life Sci. 2008;82:1122–1130.PubMedCrossRefGoogle Scholar
  14. 14.
    Sazawal S, Hiremath G, Dhingra U, Malik P, Deb S, Black RE. Efficacy of probiotics in prevention of acute diarrhoea: a meta-analysis of masked, randomized, placebo-controlled trials. Lancet Infect Dis. 2006;6:374–382.PubMedCrossRefGoogle Scholar
  15. 15.
    Johnson-Henry KC, Mitchell DJ, Avitzur Y, Galindo-Mata E, Jones NL, Sherman PM. Probiotics reduce bacterial colonization, gastric inflammation in H. pylori-infected mice. Dig Dis Sci. 2004;49:1095–1102.PubMedCrossRefGoogle Scholar
  16. 16.
    Kukkonen K, Savilahti E, Haahtela T, et al. Probiotics and prebiotic galacto-oligosaccharides in the prevention of allergic diseases: a randomized, double-blind, placebo-controlled trial. J Allergy Clin Immunol. 2007;119:192–198.PubMedCrossRefGoogle Scholar
  17. 17.
    Madsen KL. The use of probiotics in gastrointestinal disease. Can J Gastroenterol. 2001;15:817–822.PubMedGoogle Scholar
  18. 18.
    Fotiadis CI, Stoidis CN, Spyropoulos BG, Zografos ED. Role of probiotics, prebiotics and synbiotics in chemoprevention for colorectal cancer. World J Gastroenterol. 2008;14:6453–6457.PubMedCrossRefGoogle Scholar
  19. 19.
    Wollowski I, Rechkemmer G, Pool-Zobel BL. Protective role of probiotics and prebiotics in colon cancer. Am J Clin Nutr. 2001;73:451S–455S.PubMedGoogle Scholar
  20. 20.
    Barbara G, Stanghellini V, Cremon C, et al. Probiotics and irritable bowel syndrome: rationale and clinical evidence for their use. J Clin Gastroenterol. 2008;42:S214–S217.PubMedCrossRefGoogle Scholar
  21. 21.
    Ewaschuk JB, Dieleman LA. Probiotics and prebiotics in chronic inflammatory bowel diseases. World J Gastroenterol. 2006;12:5941–5950.PubMedGoogle Scholar
  22. 22.
    Peran L, Sierra S, Comalada M, et al. A comparative study of the preventative effects exerted by two probiotics, Lactobacillus reuteri and Lactobacillus fermentum, in the trinitrobenzenesulfonic acid model of rat colitis. Br J Nutr. 2007;97:96–103.PubMedCrossRefGoogle Scholar
  23. 23.
    Peran L, Camuesco D, Comalada M, et al. Preventative effects of a probiotic, Lactobacillus salivarius ssp. salivarius, in the TNBS model of rat colitis. World J Gastroenterol. 2005;11:5185–5192.PubMedGoogle Scholar
  24. 24.
    Guarner F, Malagelada JR. Role of bacteria in experimental colitis. Best Pract Res Clin Gastroenterol. 2003;17:793–804.PubMedCrossRefGoogle Scholar
  25. 25.
    Seal M, Naito Y, Barreto R, Lorenzetti A, Safran P, Marotta F. Experimental radiotherapy-induced enteritis: a probiotic interventional study. J Dig Dis. 2007;8:143–147.PubMedCrossRefGoogle Scholar
  26. 26.
    Demirer S, Aydintug S, Aslim B, et al. Effects of probiotics on radiation-induced intestinal injury in rats. Nutrition. 2006;22:179–186.PubMedCrossRefGoogle Scholar
  27. 27.
    Delia P, Sansotta G, Donato V, et al. Use of probiotics for prevention of radiation-induced diarrhea. World J Gastroenterol. 2007;13:912–915.PubMedGoogle Scholar
  28. 28.
    Ciorba MA, Stenson WF. Probiotic therapy in radiation-induced intestinal injury and repair. Ann NY Acad Sci. 2009;1165:190–194.PubMedCrossRefGoogle Scholar
  29. 29.
    Smith DH, DeCosse JJ. Radiation damage to the small intestine. World J Surg. 1986;10:189–194.PubMedCrossRefGoogle Scholar
  30. 30.
    Andreyev J. Gastrointestinal symptoms after pelvic radiotherapy: a new understanding to improve management of symptomatic patients. Lancet Oncol. 2007;8:1007–1017.PubMedCrossRefGoogle Scholar
  31. 31.
    Cengiz M, Akbulut S, Atahan IL, Grigsby PW. Acute phase response during radiotherapy. Int J Radiat Oncol Biol Phys. 2001;46:1093–1096.Google Scholar
  32. 32.
    Westergaard H. Bile acid malabsorption. Curr Treat Options Gastroenterol. 2007;10:28–33.PubMedCrossRefGoogle Scholar
  33. 33.
    Erbil Y, Oztezcan S, Giriş M, et al. The effect of glutamine on radiation-induced organ damage. Life Sci. 2005;78:376–382.PubMedCrossRefGoogle Scholar
  34. 34.
    Cho LC, Antoine JE. Radiation injury to the gastrointestinal tract. In: Feldman M, Friedman LS, Sleisenger MH, eds. Sleisenger & Fordtran’s Gastrointestinal and Liver Disease. 8th ed. Philadelphia: WB Saunders; 2006:813–826.Google Scholar
  35. 35.
    Turina M, Mulhall AM, Mahid SS, Yashar C, Galandiuk S. Frequency and surgical management of chronic complications related to pelvic radiation. Arch Surg. 2008;143:46–52.PubMedCrossRefGoogle Scholar
  36. 36.
    Galland RB, Spencer J. Natural history and surgical management of radiation enteritis. Br J Surg. 1987;74:742–747.PubMedCrossRefGoogle Scholar
  37. 37.
    Abayomi J, Kirwan J, Hackett A. The prevalence of chronic radiation enteritis following radiotherapy for cervical or endometrial cancer and its impact on quality of life. Eur J Oncol Nurs. 2009;13:262–267.PubMedCrossRefGoogle Scholar
  38. 38.
    Regimbeau JM, Panis Y, Gouzi JL, Fagniez PL. Operative and long-term results after surgery for chronic radiation enteritis. Am J Surg. 2001;182:237–242.PubMedCrossRefGoogle Scholar
  39. 39.
    Hauser-Jensen M, Wang J, Denham JW. Bowel injury: current and evolving management strategies. Semin Radiat Oncol. 2003;13:357–371.Google Scholar
  40. 40.
    Cox JD, Byhardt RW, Wilson JF, Haas JS, Komaki R, Olson LE. Complications of radiation therapy and factors in their prevention. World J Surg. 1986;10:171–188.PubMedCrossRefGoogle Scholar
  41. 41.
    Rubio CA, Jalnas M. Dose-time-dependent histological changes following irradiation of the small intestine of rats. Dig Dis Sci. 1996;41:392–401.PubMedCrossRefGoogle Scholar
  42. 42.
    Gavazzi C, Bhoori S, Lovullo S, Cozzi G, Mariani L. Role of home parenteral nutrition in chronic radiation enteritis. Am J Gastroenterol. 2006;101:374–379.PubMedCrossRefGoogle Scholar
  43. 43.
    Muttillo IA, Elias D, Bolognese A, et al. Surgical treatment of severe late radiation injury to the bowel: a retrospective analysis of 83 cases. Hepatogastroenterology. 2002;49:1023–1026.PubMedGoogle Scholar
  44. 44.
    Dörr W, Hendry JH. Consequential late effects in normal tissues. Radiother Oncol. 2001;61:223–231.PubMedCrossRefGoogle Scholar
  45. 45.
    Matsuu-Matsuyama M, Shichijo K, Okaichi K, et al. Sucralfate protects intestinal epithelial cells from radiation-induced apoptosis in rats. J Radiat Res (Tokyo). 2006;47:1–8.CrossRefGoogle Scholar
  46. 46.
    Hwang JM, Chan DC, Chang TM, et al. Effects of oral arginine and glutamine on radiation-induced injury in the rat. J Surg Res. 2003;109:149–154.PubMedCrossRefGoogle Scholar
  47. 47.
    Ersin S, Tuncyurek P, Esassolak M, et al. The prophylactic and therapeutic effects of glutamine- and arginine-enriched diets on radiation-induced enteritis in rats. J Surg Res. 2000;89:121–125.PubMedCrossRefGoogle Scholar
  48. 48.
    Waddell BE, Rodriguez-Bigas MA, Lee RJ, Weber TK, Petrelli NJ. Prevention of chronic radiation enteritis. J Am Coll Surg. 1999;189:611–624.PubMedCrossRefGoogle Scholar
  49. 49.
    Ben-Josef E, Han S, Tobi M, et al. Intrarectal application of amifostine for the prevention of radiation-induced rectal injury. Semin Riadiat Oncol. 2002;12:81–85.CrossRefGoogle Scholar
  50. 50.
    Giriş M, Erbil Y, Oztezcan S, et al. The effect of heme oxygenase-1 induction by glutamine on radiation-induced intestinal damage: the effect of heme oxygenase-1 on radiation enteritis. Am J Surg. 2006;191:503–509.PubMedCrossRefGoogle Scholar
  51. 51.
    Diestel CF, Marques RG, Lopes-Paulo F, et al. Role of l-glutamine and glycine supplementation on irradiated colonic wall. Int J Colorectal Dis. 2007;22:1523–1529.PubMedCrossRefGoogle Scholar
  52. 52.
    Johnston MJ, Robertson GM, Frizelle FA. Management of late complications of pelvic radiation in the rectum and anus: a review. Dis Colon Rectum. 2003;46:247–259.PubMedCrossRefGoogle Scholar
  53. 53.
    Hovdenak N, Fajardo LF, Hauser-Jensen M. Acute radiation proctitis: a sequential clinicopathologic study during pelvic radiotherapy. Int J Radiat Oncol Biol Phys. 2000;48:1111–1117.PubMedCrossRefGoogle Scholar
  54. 54.
    Wang CJ, Leung SW, Chen HC, et al. The correlation of acute toxicity and late rectal injury in radiotherapy for cervical carcinoma: evidence suggestive of consequential late effect (CQLE). Int J Radiat Oncol Biol Phys. 1998;40:85–91.PubMedCrossRefGoogle Scholar
  55. 55.
    Babb RR. Radiation proctitis: a review. Am J Gastroenterol. 1996;91:1309–1311.PubMedGoogle Scholar
  56. 56.
    Kountouras J, Zavos C. Recent advances in the management of radiation colitis. World J Gastroenterol. 2008;14:7289–7301.PubMedCrossRefGoogle Scholar
  57. 57.
    Tagkalidis PP, Tjandra JJ. Chronic radiation proctitis. ANZ J Surg. 2001;71:230–237.PubMedCrossRefGoogle Scholar
  58. 58.
    Williams HR, Vlavianos P, Blake P, Dearnaley DP, Tait D, Andreyev HJ. The significance of rectal bleeding after pelvic radiotherapy. Aliment Pharmacol Ther. 2005;21:1085–1090.PubMedCrossRefGoogle Scholar
  59. 59.
    Tamai O, Nozato E, Miyazato H, et al. Radiation-associated rectal cancer: report of four cases. Dig Surg. 1999;16:238–243.PubMedCrossRefGoogle Scholar
  60. 60.
    Gillette EL, Gillette SM. Principles of radiation therapy. Semin Vet Med Surg (Small Anim). 1995;10:129–134.Google Scholar
  61. 61.
    Thomson A, Hemphill D, Jeejeebhoy KN. Oxidative stress and antioxidants in intestinal disease. Dig Dis. 1998;16:152–158.PubMedCrossRefGoogle Scholar
  62. 62.
    Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol. 2007;39:44–84.PubMedCrossRefGoogle Scholar
  63. 63.
    Abou-Seif MA, El-Naggar MM, El-Far M, Ramadan M, Salah N. Amelioration of radiation-induced oxidative stress and biochemical alteration by SOD model compounds in pre-treated gamma-irradiated rats. Clin Chim Acta. 2003;337:23–33.PubMedCrossRefGoogle Scholar
  64. 64.
    Empey LR, Papp JD, Jewell LD, Fedorak RN. Mucosal protective effects of vitamin E and misoprostol during acute radiation-induced enteritis in rats. Dig Dis Sci. 1992;37:205–214.PubMedCrossRefGoogle Scholar
  65. 65.
    De Grey AD. HO2*: the forgotten radical. DNA Cell Biol. 2002;21:251–257.PubMedCrossRefGoogle Scholar
  66. 66.
    Sobko T, Reinders C, Norin E, Midtvedt T, Gustafsson LE, Lundberg JO. Gastrointestinal nitric oxide generation in germ-free and conventional rats. Am J Physiol Gastrointest Liver Physiol. 2004;287:G993–G997.PubMedCrossRefGoogle Scholar
  67. 67.
    Freeman SL, MacNaughton WK. Ionizing radiation induces iNOS-mediated epithelial dysfunction in the absence of an inflammatory response. Am J Physiol Gastrointest Liver Physiol. 2000;278:G243–G250.PubMedGoogle Scholar
  68. 68.
    Erbil Y, Dibekoglu C, Turkoglu U, et al. Nitric oxide and radiation enteritis. Eur J Surg. 1998;164:863–868.PubMedCrossRefGoogle Scholar
  69. 69.
    Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev. 2007;87:315–324.PubMedCrossRefGoogle Scholar
  70. 70.
    Kilciksiz S, Demirel C, Erdal N, et al. The effect of N-acetylcysteine on biomarkers for radiation-induced oxidative damage in a rat model. Acta Med Okayama. 2008;62:403–409.PubMedGoogle Scholar
  71. 71.
    Barker S, Weinfeld M, Zheng J, Li L, Murray D. Identification of mammalian proteins cross-linked to DNA by ionizing radiation. J Biol Chem. 2005;280:33826–33838.PubMedCrossRefGoogle Scholar
  72. 72.
    Stadtman ER. Protein oxidation and aging. Science. 1992;257:1220–1224.PubMedCrossRefGoogle Scholar
  73. 73.
    Taysi S, Koc M, Büyükokuroğlu ME, Altinkaynak K, Sahin YN. Melatonin reduces lipid peroxidation and nitric oxide during irradiation-induced oxidative injury in the rat liver. J Pineal Res. 2003;34:173–177.PubMedCrossRefGoogle Scholar
  74. 74.
    Valko M, Morris H, Cronin MT. Metals, toxicity and oxidative stress. Curr Med Chem. 2005;12:1161–1208.PubMedCrossRefGoogle Scholar
  75. 75.
    Marnett LJ. Oxy radicals, lipid peroxidation and DNA damage. Toxicology. 2002;181–182:219–222.PubMedCrossRefGoogle Scholar
  76. 76.
    Matés JM, Sánchez-Jiménez FM. Role of reactive oxygen species in apoptosis: implications for cancer therapy. Int J Biochem Cell Biol. 2000;32:157–170.PubMedCrossRefGoogle Scholar
  77. 77.
    Molla M, Panes J. Radiation-induced intestinal inflammation. World J Gastroenterol. 2007;13:3043–3046.PubMedGoogle Scholar
  78. 78.
    Robbins ME, Zhao W. Chronic oxidative stress and radiation-induced late normal tissue injury: a review. Int J Radiat Biol. 2004;80:251–259.PubMedCrossRefGoogle Scholar
  79. 79.
    Hwang ES, Kim GH. Biomarkers for oxidative stress status of DNA, lipids, and proteins in vitro and in vivo cancer research. Toxicology. 2007;229:1–10.PubMedCrossRefGoogle Scholar
  80. 80.
    Kligler B, Cohrssen A. Probiotics. Am Fam Physician. 2008;78:1073–1078.PubMedGoogle Scholar
  81. 81.
    Lomax AR, Calder PC. Prebiotics, immune function, infection and inflammation: a review of the evidence. Br J Nutr. 2009;101:633–658.PubMedCrossRefGoogle Scholar
  82. 82.
    Kapkac M, Erikoglu M, Tuncyurek P, et al. Fiber enriched diets and radiation induced injury of the gut. Nutr Res. 2003;23:77–83.CrossRefGoogle Scholar
  83. 83.
    De Vrese M, Schrezenmeir J. Probiotics, prebiotics, and synbiotics. Adv Biochem Eng Biotechnol. 2008;111:1–66.PubMedGoogle Scholar
  84. 84.
    Otamiri T, Sjödahl R. Oxygen radicals: their role in selected gastrointestinal disorders. Dig Dis. 1991;9:133–141.PubMedCrossRefGoogle Scholar
  85. 85.
    Indaram AV, Visvalingam V, Locke M, Bank S. Mucosal cytokine production in radiation-induced proctosigmoiditis compared with inflammatory bowel disease. Am J Gastroenterol. 2000;95:1221–1225.PubMedCrossRefGoogle Scholar
  86. 86.
    Mutlu-Türkoğlu U, Erbil Y, Oztezcan S, Olgaç V, Toker G, Uysal M. The effect of selenium and/or vitamin E treatments on radiation-induced intestinal injury in rats. Life Sci. 2000;66:1905–1913.PubMedCrossRefGoogle Scholar
  87. 87.
    Grisham MB, MacDermott RP, Deitch EA. Oxidant defense mechanisms in the human colon. Inflammation. 1990;14:669–680.PubMedCrossRefGoogle Scholar
  88. 88.
    Haton C, François A, Vandamme M, Wysocki J, Griffiths NM, Benderitter M. Imbalance of the antioxidant network of mouse small intestinal mucosa after radiation exposure. Radiat Res. 2007;167:445–453.PubMedCrossRefGoogle Scholar
  89. 89.
    Adaramoye O, Ogungbenro B, Anyaegbu O, Fafunso M. Protective effects of extracts of Vernonia amygdalina, Hibiscus sabdariffa and vitamin C against radiation-induced liver damage in rats. J Radiat Res (Tokyo). 2008;49:123–131.CrossRefGoogle Scholar
  90. 90.
    Koc M, Taysi S, Buyukokuroglu ME, Bakan N. Melatonin protects rat liver against irradiation-induced oxidative injury. J Radiat Res (Tokyo). 2003;44:211–215.CrossRefGoogle Scholar
  91. 91.
    Seguí J, Gironella M, Sans M, et al. Superoxide dismutase ameliorates TNBS-induced colitis by reducing oxidative stress, adhesion molecule expression, and leukocyte recruitment into the inflamed intestine. J Leukoc Biol. 2004;76:537–544.PubMedCrossRefGoogle Scholar
  92. 92.
    Mollà M, Gironella M, Salas A, et al. Protective effect of superoxide dismutase in radiation-induced intestinal inflammation. Int J Radiat Oncol Biol Phys. 2005;61:1159–1166.PubMedCrossRefGoogle Scholar
  93. 93.
    Han W, Mercenier A, Ait-Belgnaoui A, et al. Improvement of an experimental colitis in rats by lactic acid bacteria producing superoxide dismutase. Inflamm Bowel Dis. 2006;12:1044–1052.PubMedCrossRefGoogle Scholar
  94. 94.
    Carroll IM, Andrus JM, Bruno-Bárcena JM, Klaenhammer TR, Hassan HM, Threadgill DS. Anti-inflammatory properties of Lactobacillus gasseri expressing manganese superoxide dismutase using the interleukin 10-deficient mouse model of colitis. Am J Physiol Gastrointest Liver Physiol. 2007;293:G729–G738.PubMedCrossRefGoogle Scholar
  95. 95.
    Kullisaar T, Zilmer M, Mikelsaar M, et al. Two antioxidative lactobacilli strains as promising probiotics. Int J Food Microbiol. 2002;72:215–224.PubMedCrossRefGoogle Scholar
  96. 96.
    Chang SK, Hassan HM. Characterization of superoxide dismutase in Streptococcus thermophilus. Appl Environ Microbiol. 1997;63:3732–3735.PubMedGoogle Scholar
  97. 97.
    de LeBlanc A, LeBlanc JG, Perdigón G, et al. Oral administration of a catalase-producing Lactococcus lactis can prevent a chemically induced colon cancer in mice. J Med Microbiol. 2008;57:100–105.PubMedCrossRefGoogle Scholar
  98. 98.
    Pompella A, Visvikis A, Paolicchi A, De Tata V, Casini AF. The changing faces of glutathione, a cellular protagonist. Biochem Pharmacol. 2003;66:1499–1503.PubMedCrossRefGoogle Scholar
  99. 99.
    Buffinton GD, Doe WF. Depleted mucosal antioxidant defenses in inflammatory bowel disease. Free Radic Biol Med. 1995;19:911–918.PubMedCrossRefGoogle Scholar
  100. 100.
    Loguercio C, D’Argenio G, Delle Cave M, et al. Glutathione supplementation improves oxidative damage in experimental colitis. Dig Liver Dis. 2003;35:635–641.PubMedCrossRefGoogle Scholar
  101. 101.
    Witschi A, Reddy S, Stofer B, Lauterburg BH. The systemic availability of oral glutathione. Eur J Clin Pharmacol. 1992;43:667–669.PubMedCrossRefGoogle Scholar
  102. 102.
    Mansour HH, Hafez HF, Fahmy NM, Hanafi N. Protective effect of N-acetylcysteine against radiation induced DNA damage and hepatic toxicity in rats. Biochem Pharmacol. 2008;75:773–780.PubMedCrossRefGoogle Scholar
  103. 103.
    Verrecchia F, Mauviel A. Transforming growth factor-beta and fibrosis. World J Gastroenterol. 2007;13:3056–3062.PubMedGoogle Scholar
  104. 104.
    Richter KK, Langberg CW, Sung CC, Hauer-Jensen M. Association of transforming growth factor beta (TGF-beta) immunoreactivity with specific histopathologic lesions in subacute and chronic experimental radiation enteropathy. Radiother Oncol. 1996;39:243–251.PubMedCrossRefGoogle Scholar
  105. 105.
    Lui RM, Pravia KA. Oxidative stress and glutathione in TGF-beta-mediated fibrogenesis. Free Radic Biol Med. 2010;48:1–15.CrossRefGoogle Scholar
  106. 106.
    Musenga A, Mandrioli R, Bonifazi P, Kenndler E, Pompei A, Raggi MA. Sensitive and selective determination of glutathione in probiotic bacteria by capillary electrophoresis-laser induced fluorescence. Anal Bioanal Chem. 2007;387:917–924.PubMedCrossRefGoogle Scholar
  107. 107.
    Peran L, Camuesco D, Comalada M, et al. Lactobacillus fermentum, a probiotic capable to release glutathione, prevents colonic inflammation in the TNBS model of rat colitis. Int J Colorectal Dis. 2006;21:737–746.PubMedCrossRefGoogle Scholar
  108. 108.
    Lutgendorff F, Trulsson LM, van Minnen LP, et al. Probiotics enhance pancreatic glutathione biosynthesis and reduce oxidative stress in experimental acute pancreatitis. Am J Physiol Gastrointest Liver Physiol. 2008;295:G1111–G1121.PubMedCrossRefGoogle Scholar
  109. 109.
    Lutgendorff F, Nijmeijer RM, Sandström PA, et al. Probiotics prevent intestinal barrier dysfunction in acute pancreatitis in rats via induction of ileal mucosal glutathione biosynthesis. PLoS One. 2009;4:e4512.PubMedCrossRefGoogle Scholar
  110. 110.
    Kodali VP, Sen R. Antioxidant and free radical scavenging activities of an exopolysaccharide from a probiotic bacterium. Biotechnol J. 2008;3:245–251.PubMedCrossRefGoogle Scholar
  111. 111.
    Sengül N, Aslím B, Uçar G, et al. Effects of exopolysaccharide-producing probiotic strains on experimental colitis in rats. Dis Colon Rectum. 2006;49:250–258.PubMedCrossRefGoogle Scholar
  112. 112.
    Lin MY, Yen CL. Antioxidative ability of lactic acid bacteria. J Agric Food Chem. 1999;47:1460–1466.PubMedCrossRefGoogle Scholar
  113. 113.
    Lee J, Hwang KT, Heo MS, Lee JH, Park KY. Resistance of Lactobacillus plantarum KCTC 3099 from Kimchi to oxidative stress. J Med Food. 2005;8:299–304.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Basileios G. Spyropoulos
    • 1
  • Evangelos P. Misiakos
    • 2
  • Constantine Fotiadis
    • 2
  • Christos N. Stoidis
    • 2
    • 3
  1. 1.1st Department of Propaedeutic SurgeryUniversity of Athens School of Medicine, Hippokration HospitalAthensGreece
  2. 2.3rd Department of SurgeryUniversity of Athens School of Medicine, Attikon University HospitalChaidari, AthensGreece
  3. 3.1st Department of SurgeryAthens Navy HospitalAthensGreece

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