Safety and protective effectiveness of two strains of Lactobacillus with probiotic features in an experimental model of salmonellosis

International Journal of Environmental Research and Public Health

Volumn 11, Issue 9, 2014, Pages 8755-8776

  Steinberg, Raphael S ^a   Silva, Lilian C S ^a   Souza, Tássia C ^a   Lima, Maurcio T ^a   de Oliveira, Nayara L G ^a   Vieira, Leda Q ^a   Arantes, Rosa M E ^a   Miyoshi, Anderson ^a   Nicoli, Jacques R ^a   Neumann, Elisabeth ^a   Nunes, Álvaro C ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

Cattle; Immunomodulation; Lactobacillus; Mouse experimental model; Salmonellosis

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN A; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 12P40; INTERLEUKIN 17; INTERLEUKIN 18; INTERLEUKIN 5; INTERLEUKIN 6; PROBIOTIC AGENT; SECRETORY IMMUNOGLOBULIN; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE;

BACTERIUM; CATTLE; DIGESTIVE SYSTEM DISORDER; EXPERIMENTAL STUDY; GENE EXPRESSION; IMMUNE RESPONSE; IMMUNOASSAY; TESTING METHOD;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BACTERIAL STRAIN; BODY WEIGHT; CELL INFILTRATION; CONTROLLED STUDY; DRUG EFFECT; DRUG EFFICACY; DRUG SAFETY; FEMALE; GENE EXPRESSION; IMMUNOGLOBULIN PRODUCTION; IMMUNOMODULATION; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS SALIVARIUS; LIVER SIZE; MALE; MOUSE; NONHUMAN; SALMONELLOSIS; SMALL INTESTINE; SPLEEN SIZE; ANIMAL; ANIMAL HUSBANDRY; BIOLOGICAL MODEL; BOVINE; CHEMISTRY; DISEASE MODEL; DRUG EFFECTS; FECES; INTESTINE; LACTOBACILLUS; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALMONELLA; SALMONELLA INFECTIONS;

ANIMAL HUSBANDRY; ANIMALS; CATTLE; CYTOKINES; DISEASE MODELS, ANIMAL; FECES; FEMALE; IMMUNOMODULATION; INTESTINES; LACTOBACILLUS; LACTOBACILLUS ACIDOPHILUS; MALE; MICE; MODELS, BIOLOGICAL; PROBIOTICS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SALMONELLA; SALMONELLA INFECTIONS;

EID: 84906831411     PISSN: 16617827     EISSN: 16604601     Source Type: Journal    
DOI: 10.3390/ijerph110908755     Document Type: Article

References (66)

1. Food and Agricultural Organization/World Health Organization. Report of a Joint FAO/WHO Expert Consultation on Guidelines for the Evaluation of Probiotics in Food. FAO/WHO of the United Nations: London, ON, Canada, 2002.
2. European Union. Regulation (EC) No. 1831/2003 of the European Parliament and of the Council of 22 September 2003 on Additives for Use in Animal Nutrition. Available online: http://europa.eu/legislation_summaries/food_safety/animal_nutrition/l12037d_en.htm (accessed on 20 August 2012).
3. U.S. Food and Drug Administration. The Judicious Use of Medically Important Antimicrobial Drugs in Food-Producing Animals; New Animal Drugs and New Animal Drug Combination Products Administered in or on Medicated Feed or Drinking Water of Food Producing Animals: Recommendations for Drug Sponsors for Voluntarily Aligning Product Use Conditions with GFI #209; U.S. Food and Drug Administration: Rockville, MD, USA, 2012.
4. U.S. Food and Drug Administration. Draft Guidance for Industry #213, New Animal Drugs and New Animal Drug Combination Products Administered in or on Medicated Feed or Drinking Water of Food-Producing Animals: Recommendations for Drug Sponsors for Voluntarily Aligning Product Use Conditions with GFI #209; U.S. Food and Drug Administration: Rockville, MD, USA, 2012.
5. Fagundes, C.T.; Souza, D.G.; Nicoli, J.R.; Teixeira, M.M. Control of host inflammatory responsiveness by indigenous microbiota reveals an adaptive component of the innate immune system. Microbes Infect. 2011, 13, 1121-1132, doi:10.1016/j.micinf.2011.07.012.
6. Franz, C.M.A.P.; Cho, G.-S.; Holzapfel, W.H.; Galvez, A. Safety of Lactic Acid Bacteria. In Biotechnology of Lactic Acid Bacteria: Novel Applications; Mozzi, F., Raya, R.R., Vignolo, G.M., Eds.; Wiley-Blackwell: Ames, IA, USA, 2010; pp. 341-360.
7. Jouany, J.P.; Morgavi, D.P. Use of -natural{norm of matrix} products as alternatives to antibiotic feed additives in ruminant production. Animal 2007, 1, 1443-1466, doi:10.1017/S1751731107000742.
8. Higgins, J.P.; Higgins, S.E.; Wolfenden, A.D.; Henderson, S.N.; Torres-Rodriguez, A.; Vicente, J.L.; Hargis, B.M.; Tellez, G. Effect of lactic acid bacteria probiotic culture treatment timing on Salmonella Enteritidis in neonatal broilers. Poult. Sci. 2010, 89, 43-247,doi:10.3382/ps.2009-00436.
9. Brashears, M.M.; Galyean, M.L.; Loneragan, G.H.; Mann, J.E.; Killinger-Mann, K. Prevalence of Escherichia coli O157:H7 and performance by beef feedlot cattle given Lactobacillus direct-fed microbials. J. Food Prot. 2003, 66, 748-754.
10. Tabe, E.S.; Oloya, J.; Doetkott, D.K.; Bauer, M.L.; Gibbs, P.S.; Khaitsa, M.L. Comparative effect of direct-fed microbials on fecal shedding of Escherichia coli O157:H7 and Salmonella in naturally infected feedlot cattle. J. Food Prot. 2008, 71, 539-544.
11. Parvez, S.; Malik, K.A.; Ah Kang, S.; Kim, H.Y. Probiotics and their fermented food products are beneficial for health. J. Appl. Microbiol. 2006, 100, 1171-1185.
12. Ng, S.C.; Hart, A.L.; Kamm, M.A.; Stagg, A.J.; Knight, S.C. Mechanisms of action of probiotics: Recent advances. Inflamm. Bowel. Dis. 2009, 15, 300-310, doi:10.1002/ibd.20602.
13. Maassen, C.B.; Van Holten-Neelen, C.; Balk, F.; Den Bak-Glashouwer, M.J.; Leer, R.J.; Laman, J.D.; Boersma, W.J.; Claassen, E. Strain-dependent induction of cytokine profiles in the gut by orally administered Lactobacillus strains. Vaccine 2000, 18, 2613-2623.
14. Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. J. Immunol. 2002, 168, 171-178.
15. Perdigón, G.; Galdeano, M.C.; Valdez, J.C.; Medici, M. Interaction of lactic acid bacteria with the gut immune system. Eur. J. Clin. Nutr. 2002, 564, 21-26.
16. Isolauri, E.; Sütas, Y.; Kankaanpää, P.; Arvilommi, H.; Salminen, S. Probiotics: Effects on immunity. Am. J. Clin. Nutr. 2001, 73 (Suppl. 2), 444S-450S.
17. Gackowska, L.; Michalkiewicz, J.; Krotkiewski, M.; Helmin-Basa, A.; Kubiszewska, I.; Dzierzanowska D. Combined effect of different lactic acid bacteria strains on the mode of cytokines pattern expression in human peripheral blood mononuclear cells. J. Physiol. Pharmacol. 2006, 57, 13-21.
18. Winkler, P.; Ghadimi, D.; Schrezenmeir, J.; Kraehenbuhl, J. Molecular and cellular basis of microflora-Host interactions. J. Nutr. 2007, 137 (Suppl. 2), 756S-772S.
19. Cross, M.L. Microbes versus microbes: immune signals generated by probiotic lactobacilli and their role in protection against microbial pathogens. FEMS Immunol. Med. Microbiol. 2002, 34, 245-253.
20. Filho-Lima, J.V.M.; Vieira, E.C.; Nicoli, J.R. Antagonistic effect of Lactobacillus acidophilus, Saccharomyces boulardii and Escherichia coli combinations against experimental infections with Shigella flexneri and Salmonella enteritidis subsp. Typhimurium in gnotobiotic mice. J. Appl. Microbiol. 2000, 88, 365-370.
21. Silva, A.M.; Barbosa, F.H.F.; Duarte, R.; Vieira, L.Q.; Arantes, R.M.E.; Nicoli, J.R. Effect of Bifidobacterium longum ingestion on experimental salmonellosis in mice. J. Appl. Microbiol. 2004, 97, 29-37.
22. Vieira, L.Q.; Santos, L.M.; Neumann, E.; Silva, A.P.; Moura, L.N.; Nicoli, J.R. Probiotics protect mice against experimental infections. J. Clin. Gastroenterol. 2008, 42 (Suppl. 3), S168-S169, doi:10.1097/MCG.0b013e31818063d4.
23. Martins, F.S.; Silva, A.A.; Vieira, A.T.; Barbosa, F.H.F.; Arantes, R.M.E.; Teixeira, M.M.; Nicoli, J.R. Comparative study of Bifidobacterium animalis, Escherichia coli, Lactobacillus casei and Saccharomyces boulardii probiotic properties. Arch. Microbiol. 2009, 191, 623-630, doi:10.1007/s00203-009-0491-x.
24. Perdigón, G.; Alvarez, S.; Macias, M.E.N.; Roux, M.E.; Ruiz Holgado, A.P. The oral administration of lactic acid bacteria increases the mucosal intestinal immunity in response to enteropathogens. J. Food. Prot. 1990, 53, 404-410.
25. Martins, F.S.; Elian, S.D.A.; Vieira, A.T.; Tiago, F.C.P.; Martins, A.K.S.; Silva, F.C.P.; Souza, E.L.S.; Sousa, L.P.; Araújo, H.R.C.; Pimenta, P.F. et al. Oral treatment with Saccharomyces cerevisiae strain UFMG 905 modulates immune response and interferes with signal pathways involved in the activation of inflammation in a murine model of typhoid fever. Int. J. Med. Microbiol. 2011, 301, 359-364, doi:10.1016/j.ijmm.2010.11.002.
26. Khuntia, A.; Chaudhary, L.C. Performance of male crossbred calves as influenced by substitution of grain by wheat bran and the addition of lactic acid bacteria to diet. Asian-Aust. J. Anim. Sci. 2002, 15, 188-194.
27. Peterson, R.E.; Klopfenstein, T.J.; Erickson, G.E.; Folmer, J.; Hinkley, S; Moxley, R.A.; Smith, D.R. Effect of Lactobacillus acidophilus strain NP51 on Escherichia coli O157:H7 fecal shedding and finishing performance in beef feedlot cattle. J. Food. Prot. 2007, 70, 287-291.
28. Steinberg, R.S.; Lima, M.T.; Gomes de Oliveira, N.L.; Miyoshi, A.; Nicoli, J.R.; Neumann, E.; Nunes A.C. Effect of intestinal colonization by two Lactobacillus strains on the immune responses of gnotobiotic mice. Benef. Microbes 2014, doi:10.3920/BM2013.0075.
29. Colégio Brasileiro de Experimentação Animal (COBEA). Legislação e Ética. Available online: urlwww.cobea.org.br (accessed on 1 March 2009).
30. Arantes, R.M.; Nogueira, A.M. Distribution of enteroglucagon and peptide YY-immunoreactive cells in the intestinal mucosa of germ-free and conventional mice. Cell Tissue Res. 1997, 290, 61-69.
31. Castor, M.G.M.; Rezende, B.; Bernardes, P.T.T.; Vieira, T.A.; Arantes, R.M.E.; Souza, D.G.; Silva, T.A.; Teixeira, M.M.; Pinho, V. PI3K controls leukocyte recruitment, tissue injury and lethality in a model of graft-versus-host disease in mice. J. Leukoc. Biol. 2011, 89, 955-964, doi:10.1189/jlb.0810464.
32. Chomczynski, P.; Sacchi, N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 1987, 162, 156-159.
33. Arunachalam, K.; Gill, H.S.; Chandra, R.K. Enhancement of natural immune function by dietary consumption of Bifidobacterium lactis (HN019). Eur. J. Clin. Nutr. 2000, 54, 263-267.
34. Giulietti, A.; Overbergh, L.; Valckx, D.; Decallonne, B.; Bouillon, R.; Mathieu, C. An overview of real-time quantitative PCR: applications to quantify cytokine gene expression. Methods 2001, 25, 386-401.
35. European Food Safety Authority. Opinion of the scientific committee on a request from EFSA related to a generic approach to the safety assessment by EFSA of microorganisms used in food/feed and the production of food/feed additives. EFSA J. 2005, 226, 1-12.
36. Zhou, J.S.; Shu, Q.; Rutherfurd, K.J.; Prasad, J.; Birtles, M.J.; Gopal, P.K.; Gill, H.S. Safety assessment of potential probiotic lactic acid bacterial strains Lactobacillus rhamnosus HN001, Lb. acidophilus HN017, and Bifidobacterium lactis HN019 in BALB/c mice. Int. J. Food Microbiol. 2000, 56, 87-96.
37. Arunachalam, K.; Gill, H.S.; Chandra, R.K. Enhancement of natural immune function by dietary consumption of Bifidobacterium lactis (HN019). Eur. J. Clin. Nutr. 2000, 54, 263-267.
38. Haller, D.; Bode, C.; Hammes, W.P.; Pfeifer, A.M.A.; Schiffrin, E.J.; Blum, S. Non-pathogenic bacteria elicit a differential cytokine response by intestinal epithelial cell/leucocyte co-cultures. Gut 2000, 47, 79-87.
39. Levings, M.K.; Bacchetta, R.; Schulz, U.; Roncarolo, M.G. The Role of IL10 and TGF-γ in the differentiation and effector function of T regulatory cells. Int. Arch. Allergy Immunol. 2002, 129, 263-276.
40. Zaph, C.; Du, Y.; Saenz, S.A.; Nair, M.G.; Perrigoue, J.G.; Taylor, B.C.; Troy, A.E.; Kobuley, D.E.; Kastelein, R.A.; Cua, D.J.; et al. type=contributor>Commensal-dependent expression of IL-25 regulates the IL-23-IL-17 axis in the intestine. J. Exp. Med. 2008, 205, 2191-2198.
41. Lee, Y.K.; Mazmanian, S.K. Has the microbiota played a critical role in the evolution of the adaptive immune system? Science 2010, 330, 1768-1773, doi:10.1126/science.1195568.
42. Kalliomaki, M.; Salminen, S.; Poussa, T.; Arvilommi, H.; Isolauri, E. Probiotics and prevention of atopic disease: 4-year follow-up of a randomised placebo-controlled trial. Lancet 2003, 361, 1869-1871.
43. Kalliomaki, M.; Isolauri, E. Role of intestinal flora in the development of allergy. Curr. Opin. Allergy Clin. Immunol. 2003, 3, 15-20.
44. Cross, M.L.; Mortensen, R.R.; Kudsk, J.; Gill, H.S. Dietary intake of Lactobacillus rhamnosus HNOO1 enhances production of both Th1 and Th2 cytokines in antigen-primed mice. Med. Microbiol. Immunol. 2002, 191, 49-53.
45. Reid, G.; Younes, J.A.; Van Der Mei, H.C.; Gloor, G.B.; Knight, R.; Busscher, H.J. Microbiota restoration: Natural and supplemented recovery of human microbial communities. Nat. Rev. Microbiol. 2011, 9, 27-38, doi:10.1038/nrmicro2473.
46. Eckmann, L.; Kagnoff, M.F. Cytokines in host defense against Salmonella. Microbes Infect. 2001, 3, 1191-1200.
47. Mittrücker, H.; Kaufmann, S.H.E. Immune response to infection with Salmonella Typhimurium in mice. J. Leukoc. Biol. 2000, 67, 457-463.
48. Hess, J.; Ladel, C.; Miko, D.; Kaufmann, S.H.E. Salmonella typhimurium aroA2 infection in gene-targeted mice. J. Immunol. 1996, 156, 3321-3326.
49. - lymphocytes during infection with Salmonella enterica serovar Enteritidis and has a mild effect in bacterial clearance. Int. Immunol. 2008, 20, 1129-1138, doi:10.1093/intimm/dxn069.
50. Van de Veerdonk, F.L.; Gresnigt, M.S.; Kullberg, B.J.; Van der Meer, J.W.M.; Joosten, L.A.B.; Netea, M.G. Th17 responses and host defense against microorganisms: an overview. BMB Rep. 2009, 42, 776-787.
51. Mead, G.C. Prospects for 'competitive exclusion'treatment to control salmonellas and other foodborne pathogens in poultry. Vet. J. 2000, 159, 111-123.
52. Hart, A.L.; Lammers, K.; Brigidi, P.; Vitali, B.; Rizzello, F.; Gionchetti, P.; Campieri, M.; Kamm, M.A.; Knight, S.C.; Stagg A.J. Modulation of human dendritic cell phenotype and function by probiotic bacteria. Gut 2004, 53, 1602-1609.
53. Foligne, B.; Zoumpopoulou, G.; Dewulf, J.; Younes, A.B.; Chareyre, F.; Sirard, J.; Pot, B.; Grangette, C. A key role of dendritic cells in probiotic functionality. PLoS One 2007, 2, e313, doi:10.1371/journal.pone.0000313.
54. Mohamadzadeh, M.; Pfeiler, E.A.; Brown, J.B.; Zadeh, M.; Gramarossa, M.; Managlia, E.; Bere, P.; Sarraj, B.; Khan, M.W.; Pakanati, K.C., et al. Regulation of induced colonic inflammation by Lactobacillus acidophilus deficient in lipoteichoic acid. Proc. Natl. Acad. Sci. USA 2011, 108, 4623-4630, doi:10.1073/pnas.1005066107.
55. Roselli, M.; Finamore, A.; Nuccitelli, S.; Carnevali, P.; Brigidi, P.; Vitali, B.; Nobili, F.; Rami, R.; Garaguso, I.; Mengheri, E. Prevention of TNBS-induced colitis by different Lactobacillus and Bifidobacterium strains is associated with an expansion of γΔT and regulatory T cells of intestinal intraepithelial lymphocytes. Inflamm. Bowel Dis. 2009, 15, 1526-1536, doi: 10.1002/ibd.20961.
56. Di Giacinto, C.; Marinaro, M.; Sanchez, M.; Strober, W.; Boirivant, M. Probiotics ameliorate recurrent Th1-mediated murine colitis by inducing IL10 and IL10-dependent TGF-beta-bearing regulatory cells. J. Immunol. 2005, 174, 3237-3246.
57. Park, S.R.; Kim, H.A.; Chun, S.K.; Park, J.B.; Kim, P.H. Mechanisms underlying the effects of LPS and activation-induced cytidine deaminase on IgA isotype expression. Mol. Cells 2005, 19, 445-451.
58. Corthésy B. Roundtrip ticket for secretory IgA: role in mucosal homeostasis? J. Immunol. 2007, 178, 27-32.
59. Michetti, P.; Porta, N.; Mahan, M.J.; Slauch, J.M.; Mekalanos, J.J.; Blum, A.L.; Kraehenbuhl, J.P.; Neutra, M.R. Monoclonal immunoglobulin A prevents adherence and invasion of polarized epithelial cell monolayers by Salmonella Typhimurium. Gastroenterology 1994, 107, 915-923.
60. Galdeano, C.M.; De Leblanc, A.; Vinderola, G.; Bonet, M.E.B.; Perdigón, G. Proposed model: Mechanisms of immunomodulation induced by probiotic bacteria. Clin. Vaccine Immunol. 2007, 14, 485-492.
61. Jain, S.; Yadav, H.; Sinha, P.R.; Naito, Y.; Marotta, F. Dahi containing probiotic Lactobacillus acidophilus and Lactobacillus casei has a protective effect against Salmonella enteritidis infection in mice. Int. J. Immunopathol. Pharmacol. 2008, 21, 1025-1033.
62. Jain, S.; Yadav, H.; Sinha, P.R. Probiotic Dahi containing Lactobacillus casei protects against Salmonella enteritidis infection and modulates immune response in mice. J. Med. Food 2009, 12, 576-583, doi:10.1089/jmf.2008.0246.
63. Mantis, N.J.; Forbes, S.J. Secretory IgA: Arresting microbial pathogens at epithelial borders. Immunol. Invest. 2010, 39, 383-406, doi:10.3109/08820131003622635.
64. Marteau, P.; Vaerman, J.P.; Dehennin, J.P.; Bord, S.; Brassart, D; Pochart, P.; Desjeux, J.F.; Rambaud, J.C. Effect of intrajejunal perfusion and chronic ingestion of Lactobacillus johnsonii strain La1 on serum concentrations and jejunal secretions of immunoglobulins and serum proteins in healthy humans. Gastroenterol. Clin. Biol. 1997, 21, 293-298.
65. Spanhaak, S.; Havenaar, R.; Schaafsma, G. The effect of consumption of milk fermented by Lactobacillus casei strain Shirota on the intestinal microflora and immune parameters in humans. Eur. J. Clin. Nutr. 1998, 52, 899-907.
66. Dogi, C.A.; Galdeano, C.M.; Perdigón, G. Gut immune stimulation by nonpathogenic Gram(+) and Gram(-) bacteria. Comparison with a probiotic strain. Cytokine 2008, 41, 223-231, doi:10.1016/j.cyto.2007.11.014.