Lactobacillus and Its Probiotic Role in the Digestive and Nutritional Processes of Pigs: A Review

Abstract

The activity of a probiotic is dependent on the strain’s ability to confer health benefits to the host through oral consumption of viable cells. The main objective of this study was to carry out a review about the importance of Lactobacillus and its probiotic role in the digestive and nutritional processes of pigs. The study focused on seven strains of Lactobacillus and their varied uses in feeding different categories of pigs. We obtained a clear conceptualization of Lactobacillus’ effect on the immune system, its genome and how it is used in probiotic drinks. Based on the results, we can conclude that the use of Lactobacillus improves swine health and nutrition, making it a viable alternative to replace the indiscriminate use of antibiotics as growth promoters.


Keywords: probiotics, antibiotics, digestive process, endogenous species, pig categories.


RESUMEN


La habilidad de un probiótico está en dependencia de la capacidad de la cepa de conferir beneficios de salud al hospedador mediante el consuno oral de células viables. El presente trabajo tuvo como objetivo principal realizar una aproximación conceptual de varios autores acerca de la importancia de los Lactobacillus y su papel probiótico en el proceso digestivo y nutricional en cerdos. Para ello, se hizo necesario realizar una profusa búsqueda, selección y procesamiento de las más prominentes fuentes bibliográficas, que tratan sobre este tema. El estudio se llevó a cabo sobre 7 cepas de Lactobacillus y sus diferentes formas de uso en la alimentación de las diferentes categorías porcinas; obteniéndose entre los principales resultados una clara conceptualización de la acción de los Lactobacillus en el sistema inmunológico, genoma y el modo de utilización en bebidas probióticas. A modo de conclusión, se puede mencionar que la totalidad de los autores citados concuerdan que la utilización de Lactobacillus mejora fundamentalmente la sanidad y nutrición porcina, convirtiéndose en la alternativa más viable para remplazar el uso indiscriminado de los antibióticos como promotores de crecimiento.


Palabras claves: probióticos, antibióticos, proceso digestivo, especies endógenas, categorías porcinas.

References
[1] Kelly D, Mulder IE. Microbiome and immunological interactions. Nutrition Reviews. 2012;70(Suppl 1):18–30.

[2] Gu S, Chen D, Zhang J-N et al. Bacterial community mapping of the mouse gastrointestinal tract. PloS One. 2013;8(10):749-57.

[3] Sekirov I, Russell S, Antunes CM, Finlay BB. Gut microbiota in health and disease. Physiological Reviews. 2010;90:859–904.

[4] Martín R, Sánchez B, Suárez JE, Urdaci MC. Characterization of the adherence properties of human Lactobacilli strains to be used as vaginal probiotics. FEMS Microbiology Letters. 2012;328(2):166–73.

[5] Garrote G, Abraham A, de Antoni G. Chemical and microbiological characterisation of kefir grains. Journal of Dairy Research. 2001;68(4):639–52.

[6] Bernardeau M, Vernoux JP, Henri-Dubernet S, Guéguen M. Safety assessment of dairy microorganisms: The Lactobacillus genus. International Journal of Food Microbiology. 2008;126(3):278–85.

[7] Dušková M, Šedo O, Kšicová K, Zdráhal Z, Karpíšková R. Identification of lactobacilli isolated from food by genotypic methods and MALDI-TOF MS. International Journal of Food Microbiology. 2012;159(2):107–14.

[8] Servin AL. Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiology Reviews. 2004;28(4):405–40.

[9] Humen M, de Antoni G, Benyacoub J et al. Lactobacillus johnsonii La1 antagonizes Giardia intestinalis in vivo. Infection and Immunity. 2005;73(2):1265–1269.

[10] Corthésy B, Gaskins H, Mercenier A. 2007. Cross-talk between probiotic bacteria and the host immune system. The Journal of Nutrition. 2007;781–790.

[11] Yamamoto M, Sato S, Hemmi H et al. Essential role for TIRAP in activation of the signalling cascade shared by TLR2 and TLR4. Natur. 2002;420:324-329.

[12] Land MH, Rouster-Stevens K, Woods CR, Cannon ML, Cnota J, Shetty AK. Lactobacillus sepsis associated with probiotic therapy. Pediatrics. 2005;115(1):178–81.

[13] Fradiani PA, Petrucca A, Ascenzioni F et al. Endocarditis caused by Lactobacillus jensenii in an immunocompetent patient. Journal of Medical Microbiology. 2010;59(5):607–9.

[14] Pathmakanthan S, Li CK, Cowie J, Hawkey CJ. Lactobacillus plantarum 299: beneficial in vitro immunomodulation in cells extracted from inflamed human colon. J Gastroenterol Hepatol. 2004;19:166-173.

[15] Stingele F, Corthesy B, Kusy N, Porcelli SA, Kasper DL, Tzianabos AO. Zwitterionic polysaccharides stimulate T cells with no preferential V beta usage and promote anergy, resulting in protection against experimental abscess formation. J Immunol . 2004;172:1483-1490.

[16] Gámez HJ, Ramírez C, Martínez J. 2013. Evaluación in vivo de Lactobacillus plantarum como alternativa al uso de antibióticos en lechones. Revista MVZ Córdoba. 2013;18(3):3648-3657.

[17] Fredricks DN, Fiedler TL, Marrazzo JM. Molecular identifcation of bacteria associated with bacterial vaginosis. N Engl J Med. 2005; 353:1899-1911.

[18] Ljungh A, Wadstrom T. Editores. Lactobacillus molecular biology. From genomics to probiotics. Norfolk: Caister Academic Press; 2009.

[19] Marín Z, Cortés M, Montoya O. Evaluación de la viabilidad de crecimiento de la cepa nativa Lactobacillus plantarum LPBM10 y la cepa comercial Lactobacillus casei ATCC 393 en pulpa de uchuva y en solución isotónica de glucosa. Rev VITAE. 2009; 16(2):210-217.

[20] Zhan YZ, Bon J, Joan MK. Production of lactic acid from renewable materials by Rhizopus fungi. Chem Eng Process. 2006; 46:361-374.

[21] González BA, Domínguez R, Alcocer BR. Aloe vera como sustrato para el crecimiento de Lactobacillus plantarum y L. casei. Ciencia y Tecnología Alimentaria. 2008;6(2):152-157.

[22] Estela W, Rychtera M, Melzoch K, Quillama E, Egoavil E. Producción de ácido láctico por Lactobacillus plantarum L10 en cultivos batch ycontinuo. Rev Perú Biol. 2007; 14(2):271-276.

[23] Nemcova R, Laukova A, Gancarcikova S, Kastel R. In vitro studies of porcine |lactobacilli for posible use. Berl. Munch. Tieraztl. Wschr. 1997;110:413.

[24] Guerin C, Meslin J, Chambard A et al. 2001. Food supplementation with milk fermented by Lactobacillus casei DN - 114 001 protects suckling rats from rotavirus associated diarrhea. J. Nutr. 2001;131:111.

[25] Iñiguez C, Jiménez R, Vázquez L, Ramos G, Acedo E. Proteincarbohydrate interactions between Lactobacillus salivarius and pig mucins. J. Nutr. 2011;132:110

[26] Pieper R, Janczyk P, Schumann R, Souffrant WB. The intestinal microflora of piglets around weaning – With emphasis on lactobacilli. Arch. Zootech. 2006;9:29.

[27] Fuller R. Probiotics in man and animal. J. Appl. Bacteriol. 1989;66:365.

[28] Casey P, Gardiner G, Casey G et al. A fvestrain probiotic combination reduces pathogen shedding and alleviates disease signs in pigs chalenged with Salmonella enterica serovar Typhimurium. Appl. Environ. Microbiol. 2007;73:1858.

[29] Yeo J, Kim K. Effect of feeding diets containingan antibiotic, a probiotic, or yucca extract on growth and intestinal urease activity in broiler chicks. Poult. Sci. 1997;76:381

[30] Mejía W, Rubio J, Calatayud D, Rodríguez A, Quintero, A. Evaluación de dos probióticos sobre parámetros productivos en lechones lactantes. Zootécnia Trop. 2007;25:301.

[31] Holzapfel WH, Haberer P, Geisen R, Björkroth J, Schillinger U. Taxonomy and important features of probiotic microorganisms in food and nutrition. American Journal of Clinical Nutrition. 2001; 73(supplement):365-373.

[32] 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. European Journal of Clinical Nutrition. 1998;52:899-907.

[33] Matsuzaki T. Immunomodulation by treatment with Lactobacillus casei strain Shirota. International Journal of Food Microbiology. 1998;41:133-140.

[34] Reid G. Minireview: The scientific basis for probiotic strains of Lactobacillus. Applied Environmental Microbiology. 1999;65:3763-3766.

[35] Bomba A, Nemcová R, Gancarčíková S, Herich R, Kaštel R. Mechanisms in the pathogenesis of enteric diseases 2. (P.S. Paul, y D.H. Francis, editores). New York: Kluwer Academic/Plenum Publishers; 1999. New York Potentation of the effectiveness of Lactobacillus casei in the prevention of E. coli induced diarrea in conventional and gnotobiotic pigs. p. 185-190

[36] Alander M, Korpela R, Saxelin M, Salmela VT, Mattila-Sandholm T, von WA. Recovery of Lactobacillus rhamnosus GG from human colonic biopsies. Lett. Appl. Microbiol. 1997;24:361.

[37] Alltech. BIO-MOS in the poultry industry. Biotech. in the feed industry. Supplement to the Proc. Alltech’s Biotech. Feed Industry. Lyons TP, editor. Nicholasville; 1995.

[38] Avila F, Parlillo A, Schocken R, Lucas F, Orgaz A, Quintana J. A comparative study of the efficiency of a probiotic and anti-K99 and antiA14 vaccines in the control of diarrhea in calves in Brazil. Rev. Elev. Med. Vet. Pays. Trop. 1995;48:239.

[39] Alltech. BIO-MOS in the poultry industry. Biotech. In the feed industry. Supplement to the Proc. Alltech’s Biotech. Feed Iindustry. Lyons TP, editor. Nicholasville; 1996.

[40] Boucourt R, Savón L, Díaz J et al. Efecto de la actividad probiótica de Lactobacillus rhamnosus en indicadores fisiológicos de lechones. Revista Cubana de Ciencia Agrícola. 2004;38(4):411-416.

[41] Biricik H, Türkmen II. The effect of Saccharomyces cerevisiae on in vitro rumen digestibilities of dry matter, organic matter and neutral detergent fibre of different forage: Concenrate ratios in diets. J. Fac. Vet. Med. 2001:20:29.

[42] Shimazu T, Villena J, Tohno M et al. Immunobiotic Lactobacillus jensenii elicit anti-inflammatory activity in porcine intestinal epithelial cells by modulating negative regulators of the toll-like receptor signaling pathway. Infect Immun. 2012;80:276–288.

[43] Villena J, Suzuki R, Fujie H et al. Immunobiotic Lactobacillus jensenii modulates toll-like receptor 4-induced inflammatory response via negative regulation in porcine antigen presenting cells. Clin Vaccine Immunol. 2012;19:1038–1053.

[44] Oh PL, Benson AK, Peterson DA et al. Diversification of the gut symbiont Lactobacillus reuteri as a result of host-driven evolution. ISME J. 2010; 4:377–87.

[45] Chang YH, Kim JK, Kim HJ, Kim WY, Kim YB, Park YH. Selection of a potential probiotic Lactobacillus strain and subsequent in vivo studies. Antonie Van Leeuwenhoek. 2001;80:193–9.

[46] Hou C, Wang Q, Zeng X et al. Complete genome sequence of Lactobacillus reuteri I5007, a probiotic strain isolated from healthy piglet. J Biotechnol. 2014;179:63–4.

[47] Hou C, Zeng X, Yang F, Liu H, Qiao S. (2015). Study and use of the probiotic Lactobacillus reuteri in pigs: A review. Journal of animal science and biotechnology. 2015;6(1):14.

[48] Huang CH, Qiao SY, Li DF, Piao XS, Ren JP. Effects of Lactobacillus on the performance, diarrhea incidence, VFA concentration and gastrointestinal microbial flora of weaning pigs. Asian-Aust J Anim Sci. 2004;17:401–9.

[49] Chang YH, Kim JK, Kim HJ, Kim WY, Kim YB, Park YH. Selection of a potential probiotic Lactobacillus strain and subsequent in vivo studies. Antonie Van Leeuwenhoek. 2001;80:193–9.

[50] Yu B, Liu JR, Chiou MY, Hsu YR, Chiou PWS. The effects of probiotic Lactobacillus reuteri Pg4 strain on intestinal characteristics and performance in broilers. Asian-Aust J Anim Sci. 2007;20:1243–51.

[51] Seo BJ, Mun MR, Kumar JR et al. Bile tolerant Lactobacillus reuteri isolated from pig feces inhibits enteric bacterial pathogens and porcine rotavirus. Vet Res Commun. 2010; 34:323–33.

[52] Urbanska M, Szajewska H. The efficacy of Lactobacillus reuteri DSM 17938 in infants and children: A review of the current evidence. Eur J Pediatr. 2014;173:1327–37.

[53] Lee DY, Seo YS, Rayamajhi N, Kang ML, Lee SI, Yoo HS. Isolation, characterization, and evaluation of wild isolates of Lactobacillus reuteri from pig feces. J Microbiol. 2009;47:663–72.

[54] Hou C, Wang Q, Zeng X et al. Complete genome sequence of Lactobacillus reuteri I5007, a probiotic strain isolated from healthy piglet. J Biotechnol. 2014;179:63–4.

[55] Heavens D, Tailford LE, Crossman L et al. Genome sequence of the vertebrate gut symbiont Lactobacillus reuteri ATCC 53608. J Bacteriol. 2011;193:4015–6.

[56] Rosander A, Connolly E, Roos S. Removal of antibiotic resistance genecarrying plasmids from Lactobacillus reuteri ATCC 55730 and characterization of the resulting daughter strain, L. reuteri DSM 17938. Appl Environ Microbiol. 2008; 74:6032–40.

[57] van de Guchte M, Serror P, Chervaux C, Smokvina T, Ehrlich SD, Maguin E. Stress responses in lactic acid bacteria. Antonie Van Leeuwenhoek. 2002;82:187–216.

[58] Liu XT, Hou CL, Zhang J, Zeng XF, Qiao SY. Fermentation conditions influence the fatty acid composition of the membranes of Lactobacillus reuteri I5007 and its survival following freeze-drying. Lett Appl Microbiol. 2014;59:398–403.

[59] Lebeer S, Vanderleyden J, De Keersmaecker SC. Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev. 2008;72:728–64.

[60] Bian L. An in vitro antimicrobial and safety study of Lactobacillus reuteri DPC16 for validation of probiotic concept [Master’s tesis]. Massey University; 2008.

[61] Morita H, Toh H, Fukuda S, Horikawa H et al. Comparative genome analysis of Lactobacillus reuteri and Lactobacillus fermentum reveal a genomic island for reuterin and cobalamin production. DNA Res. 2008; 15:151–61.

[62] Gänzle MG, Höltzel A, Walter J, Jung G, Hammes WP. Characterization of reutericyclin produced by Lactobacillus reuteri LTH2584. Appl Environ Microbiol. 2000; 66:4325–33.

[63] Mukai T, Asasaka T, Sato E, Mori K, Matsumoto M, Ohori H. Inhibition of binding of Helicobacter pylori to the glycolipid receptors by probiotic Lactobacillus reuteri. FEMS Immunol Med Microbiol. 2002;32:105–10.

[64] Taranto MP, Vera JL, Hugenholtz J, De Valdez GF, Sesma F. Lactobacillus reuteri CRL1098 produces cobalamin. J Bacteriol. 2003;185:5643–7.

[65] Wang AN, Yi XW, Yu HF, Dong B, Qiao SY. Free radical scavenging activity of Lactobacillus fermentum in vitro and its antioxidative effect on growingfinishing pigs. J Appl Microbiol. 2009;107:1140–8.

[66] Hoffmann M, Rath E, Holzlwimmer G et al. Lactobacillus reuteri 100–23 transiently activates intestinal epithelial cells of mice that have a complex microbiota during early stages of colonization. J Nutr. 2008;138:1684–91.

[67] Dicksved J, Schreiber O, Willing B et al. Lactobacillus reuteri maintains a functional mucosal barrier during DSS treatment despite mucus layer dysfunction. PLoS One. 2012;7:46399.

[68] Martinez RC, Seney SL, Summers KL, Nomizo A, De Martinis EC, Reid G. Effect of Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14 on the ability of Candida albicans to infect cells and induce inflammation. Microbiol Immunol. 2009;53:487–95.