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Evaluation of the preventative effects exerted by Lactobacillus fermentum in an experimental model of septic shock induced in mice

  • Belén Arribas (a1), Maria Elena Rodríguez-Cabezas (a1), Mònica Comalada (a1), Elvira Bailón (a1), Desireé Camuesco (a1), Mónica Olivares (a2), Jordi Xaus (a2) (a3), Antonio Zarzuelo (a1) and Julio Gálvez (a1)...
Abstract

The preventative effects of the probiotic Lactobacillus fermentum CECT5716 were evaluated in the lipopolysaccharide (LPS) model of septic shock in mice. The probiotic was administered suspended in drinking water at the final concentration of 108 colony-forming units/ml for 2 weeks before the induction of an endotoxic shock by an intraperitoneal injection of LPS (400 μg/200 μl per mouse). Blood and different organs were collected after 24 h to evaluate the severity of the endotoxic shock and the preventative effects of the probiotic. L. fermentum reduced TNF-α levels in blood, which promotes the major alterations observed during septic shock, as well as the infiltration of activated neutrophils into the lungs. Furthermore, free radical overproduction and oxidative stress were associated with a significant decrease in hepatic glutathione levels in septic mice, and with an excessive NO production attributed to the induction of the inducible isoform of NO synthase (iNOS). In fact, hepatic glutathione levels were significantly increased in the group of mice receiving the probiotic, and the increased iNOS expression both in the colon and lungs was down-regulated in those mice treated with L. fermentum. Finally, pre-treatment with L. fermentum may also exert its protective action modulating the expression of different cytokines in splenocyte-derived T cells such us IL-2, IL-5, IL-6 or IL-10. In conclusion, pre-treatment with L. fermentum may exert its protective action against LPS-induced organ damage in mice by a combination of several actions including its antioxidant properties and by reduction of the synthesis of the pro-inflammatory TNF-α and IL-6.

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Corresponding author
*Corresponding author: Dr Julio Galvez, fax +34 958248964, email jgalvez@ugr.es
References
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1Forchielli, ML & Walker, WA (2005) The role of gut-associated lymphoid tissues and mucosal defence. Br J Nutr 93, Suppl. 1, S41S48.
2Asher, MI, Montefort, S, Björkstén, B, Lai, CK, Strachan, DP, Weiland, SK & Williams, H (2006) Worldwide time trends in the prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and eczema in childhood: ISAAC Phases One and Three repeat multicountry cross-sectional surveys. Lancet 368, 733743.
3Guarner, F & Schaafsma, GJ (1998) Probiotics. Int J Food Microbiol 39, 237238.
4Ouwehand, AC, Salminen, S & Isolauri, E (2002) Probiotics: an overview of beneficial effects. Antonie Van Leeuwenhoek 82, 279289.
5Parvez, S, Malik, KA, Ah Kang, S & Kim, HY (2006) Probiotics and their fermented food products are beneficial for health. J Appl Microbiol 100, 11711185.
6Olivares, M, MPaz Díaz-Ropero, M, Gómez, N, Sierra, S, Lara-Villoslada, F, Martín, R, Miquel Rodríguez, J & Xaus, J (2006) Dietary deprivation of fermented foods causes a fall in innate immune response. Lactic acid bacteria can counteract the immunological effect of this deprivation. J Dairy Res 73, 492498.
7Malin, M, Verronen, P, Korhonen, H, Syväoja, EL, Salminen, S, Mykkänen, H, Arvilommi, H, Eerola, E & Isolauri, E (1997) Dietary therapy with Lactobacillus GG, bovine colostrum or bovine immune colostrum in patients with juvenile chronic arthritis: evaluation of effect on gut defence mechanisms. Inflammopharmacology 5, 219236.
8Kato, I, Endo-Tanaka, K & Yokokura, T (1998) Suppressive effects of the oral administration of Lactobacillus casei on type II collagen-induced arthritis in DBA/1 mice. Life Sci 63, 635644.
9Baharav, E, Mor, F, Halpern, M & Weinberger, A (2004) Lactobacillus GG bacteria ameliorate arthritis in Lewis rats. J Nutr 134, 19641969.
10Sheil, B, McCarthy, J, O'Mahony, L, Bennett, MW, Ryan, P, Fitzgibbon, JJ, Kiely, B, Collins, JK & Shanahan, F (2004) Is the mucosal route of administration essential for probiotic function? Subcutaneous administration is associated with attenuation of murine colitis and arthritis. Gut 53, 694700.
11Isolauri, E, Arvola, T, Sütas, Y, Moilanen, E & Salminen, S (2000) Probiotics in the management of atopic eczema. Clin Exp Allergy 30, 16041610.
12Rosenfeldt, V, Benfeldt, E, Nielsen, SD, Michaelsen, KF, Jeppesen, DL, Valerius, NH & Paerregaard, A (2003) Effect of probiotic Lactobacillus strains in children with atopic dermatitis. J Allergy Clin Immunol 111, 389395.
13Macfarlane, GT & Cummings, JH (2002) Probiotics, infection and immunity. Curr Opin Infect Dis 15, 501506.
14Vaarala, O (2003) Immunological effects of probiotics with special reference to lactobacilli. Clin Exp Allergy 33, 16341640.
15Shibolet, O, Karmeli, F, Eliakim, R, Swennen, E, Brigidi, P, Gionchetti, P, Campieri, M, Morgenstern, S & Rachmilewitz, D (2002) Variable response to probiotics in two models of experimental colitis in rats. Inflamm Bowel Dis 8, 399406.
16Peran, L, Camuesco, D, Comalada, M, Bailon, E, Henriksson, A, Xaus, J, Zarzuelo, A & Galvez, J (2007) A comparative study of the preventative effects exerted by three probiotics. Bifidobacterium lactis, Lactobacillus casei and Lactobacillus acidophilus, in the TNBS model of rat colitis. J Appl Microbiol 103, 836844.
17Ayala, A, Lehman, DL, Herdon, CD & Chaudry, IH (1994) Mechanism of enhanced susceptibility to sepsis following hemorrhage. Interleukin-10 suppression of T-cell response is mediated by eicosanoid-induced interleukin-4 release. Arch Surg 129, 11721178.
18Liu, SF & Malik, AB (2006) NF-κB activation as a pathological mechanism of septic shock and inflammation. Am J Physiol Lung Cell Mol Physiol 290, L622L645.
19Jørgensen, VL, Nielsen, SL, Espersen, K & Perner, A (2006) Increased colorectal permeability in patients with severe sepsis and septic shock. Intensive Care Med 32, 17901796.
20Yende, S & Angus, DC (2007) Long-term outcomes from sepsis. Curr Infect Dis Rep 9, 382386.
21Díaz-Ropero, MP, Martín, R, Sierra, S, Lara-Villoslada, F, Rodríguez, JM, Xaus, J & Olivares, M (2007) Two Lactobacillus strains, isolated from breast milk, differently modulate the immune response. J Appl Microbiol 102, 337343.
22Olivares, M, Díaz-Ropero, MP, Sierra, S, Lara-Villoslada, F, Fonollá, J, Navas, M, Rodríguez, JM & Xaus, J (2007) Oral intake of Lactobacillus fermentum CECT5716 enhances the effects of influenza vaccination. Nutrition 23, 254260.
23Olivares, M, Díaz-Ropero, MP, Martín, R, Rodríguez, JM & Xaus, J (2006) Antimicrobial potential of four Lactobacillus strains isolated from breast milk. J Appl Microbiol 101, 7279.
24Geier, MS, Butler, RN, Giffard, PM & Howarth, GS (2007) Lactobacillus fermentum BR11, a potential new probiotic, alleviates symptoms of colitis induced by dextran sulfate sodium (DSS) in rats. Int J Food Microbiol 114, 267274.
25Hung, J, Cooper, D, Turner, MS, Walsh, T & Giffard, PM (2003) Cystine uptake prevents production of hydrogen peroxide by Lactobacillus fermentum BR11. FEMS Microbiol Lett 227, 9399.
26Kullisaar, T, Zilmer, M, Mikelsaar, M, Vihalemm, T, Annuk, H, Kairane, C & Kilk, A (2002) Two antioxidative lactobacilli strains as promising probiotics. Int J Food Microbiol 72, 215224.
27Peran, L, Camuesco, D, Comalada, M, Nieto, A, Concha, A, Adrio, JL, Olivares, M, Xaus, J, Zarzuelo, A & Galvez, J (2006) Lactobacillus fermentum, a probiotic capable to release glutathione, prevents colonic inflammation in the TNBS model of rat colitis. Int J Colorectal Dis 21, 737746.
28Songisepp, E, Kals, J, Kullisaar, T, Mändar, R, Hütt, P, Zilmer, M & Mikelsaar, M (2005) Evaluation of the functional efficacy of an antioxidative probiotic in healthy volunteers. Nutr J 4, 22.
29Sánchez de Medina, F, Gálvez, J, Romero, JA & Zarzuelo, A (1996) Effect of quercitrin on acute and chronic experimental colitis in the rat. J Pharmacol Exp Ther 278, 771779.
30Anderson, ME (1985) Determination of glutathione and glutathione disulfide in biological samples. Methods Enzymol 113, 548555.
31Comalada, M, Camuesco, D, Sierra, S, Ballester, I, Xaus, J, Gálvez, J & Zarzuelo, A (2005) In vivo quercitrin anti-inflammatory effect involves release of quercetin, which inhibits through down-regulation of the NF-κB pathway. Eur J Immunol 35, 584592.
32Comalada, M, Ballester, I, Bailón, E, Sierra, S, Xaus, J, Gálvez, J, de Medina, FS & Zarzuelo, A (2006) Inhibition of pro-inflammatory markers in primary bone marrow-derived mouse macrophages by naturally occurring flavonoids: analysis of the structure–activity relationship. Biochem Pharmacol 72, 10101021.
33Peran, L, Sierra, S, Comalada, M, et al. (2007) 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 97, 96103.
34Leite, MS, Pacheco, P, Gomes, RN, Guedes, AT, Castro-Faria-Neto, HC, Bozza, PT & Koatz, VL (2005) Mechanisms of increased survival after lipopolysaccharide-induced endotoxic shock in mice consuming olive oil-enriched diet. Shock 23, 173178.
35Annane, D, Bellissant, E & Cavaillon, JM (2005) Septic shock. Lancet 365, 6378.
36Welbourn, CR & Young, Y (1992) Endotoxin, septic shock and acute lung injury: neutrophils, macrophages and inflammatory mediators. Br J Surg 79, 9981003.
37Salvemini, D & Cuzzocrea, S (2002) Oxidative stress in septic shock and disseminated intravascular coagulation. Free Radic Biol Med 33, 11731185.
38Patel, GP, Gurka, DP & Balk, RA (2003) New treatment strategies for severe sepsis and septic shock. Curr Opin Crit Care 9, 390396.
39Hotchkiss, RS & Karl, IE (2003) The pathophysiology and treatment of sepsis. N Engl J Med 348, 138150.
40Kim, GY, Roh, SI, Park, SK, Ahn, SC, Oh, YH, Lee, JD & Park, YM (2003) Alleviation of experimental septic shock in mice by acidic polysaccharide isolated from the medicinal mushroom Phellinus linteus. Biol Pharm Bull 26, 14181423.
41Hsu, CS, Chiu, WC, Yeh, CL, Hou, YC, Chou, SY & Yeh, SL (2006) Dietary fish oil enhances adhesion molecule and interleukin-6 expression in mice with polymicrobial sepsis. Br J Nutr 96, 854860.
42Barton, BE (1996) The biological effects of interleukin 6. Med Res Rev 1, 87109.
43Hack, CE, De Groot, ER, Felt-Bersma, RJ, Nuijens, JH, Strack Van Schijndel, RJ, Eerenberg-Belmer, AJ, Thijs, LG & Aarden, LA (1989) Increased plasma levels of interleukin-6 in sepsis. Blood 74, 17041710.
44Watanabe, E, Hirasawa, H, Oda, S, Matsuda, K, Hatano, M & Tokuhisa, T (2005) Extremely high interleukin-6 blood levels and outcome in the critically ill are associated with tumor necrosis factor- and interleukin-1-related gene polymorphisms. Crit Care Med 33, 8997.
45Cuzzocrea, S, Mazzon, E, EDi Paola, R, Esposito, E, Macarthur, H, Matuschak, GM & Salvemini, D (2006) A role for nitric oxide-mediated peroxynitrite formation in a model of endotoxin-induced shock. J Pharmacol Exp Ther 319, 7381.
46Sener, G, Toklu, H, Kapucu, C, Ercan, F, Erkanli, G, Kaçmaz, A, Tilki, M & Yegen, BC (2005) Melatonin protects against oxidative organ injury in a rat model of sepsis. Surg Today 35, 5259.
47Cuzzocrea, S, McDonald, MC, Mazzon, E, Dugo, L, Lepore, V, Fonti, MT, Ciccolo, A, Terranova, ML, Caputi, AP & Thiemermann, C (2000) Tempol, a membrane-permeable radical scavenger, reduces dinitrobenzene sulfonic acid-induced colitis. Eur J Pharmacol 406, 127137.
48Besselink, MG, van Santvoort, HC, Buskens, E, et al. (2008) Probiotic prophylaxis in predicted severe acute pancreatitis: a randomised, double-blind, placebo-controlled trial. Lancet 371, 651659.
49Anukam, KC, Osazuwa, EO, Osadolor, HB, Bruce, AW & Reid, G (2008) Yogurt containing probiotic Lactobacillus rhamnosus GR-1 and L. reuteri RC-14 helps resolve moderate diarrhea and increases CD4 count in HIV/AIDS patients. J Clin Gastroenterol 42, 239243.
50Trois, L, Cardoso, EM & Miura, E (2008) Use of probiotics in HIV-infected children: a randomized double-blind controlled study. J Trop Pediatr 54, 1924.
51Bibiloni, R, Fedorak, RN, Tannock, GW, Madsen, KL, Gionchetti, P, Campieri, M, De Simone, C & Sartor, RB (2005) VSL#3 probiotic-mixture induces remission in patients with active ulcerative colitis. Am J Gastroenterol 100, 15391546.
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