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Probiotics – do they have a role in the pig industry?

Published online by Cambridge University Press:  14 October 2010

M. Kenny ,
H. Smidt ,
E. Mengheri  and
B. Miller
M. Kenny
Affiliation:
Division of Food Animal Sciences, Department of Clinical Veterinary Sciences, University of Bristol, Lower Langford, North Somerset, BS40 5DU, UK
H. Smidt
Affiliation:
Laboratory of Microbiology, Wageningen University, Dreijenplein 10, 6703 HB Wageningen, The Netherlands
E. Mengheri
Affiliation:
INRAN, Via Ardeatina 546, Roma 00178, Italy
B. Miller*
Affiliation:
Division of Food Animal Sciences, Department of Clinical Veterinary Sciences, University of Bristol, Lower Langford, North Somerset, BS40 5DU, UK
*
†E-mail: Bev.Miller@bris.ac.uk
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Abstract

The delivery of certain living microorganisms in food has long been suggested as having positive health effects in humans. This practice has extended into food animal production, with a variety of microorganisms being used; lactic acid bacteria, various Bacillus species and the yeast Saccharomyces cerevisiae have been particularly used in the pig industry. The increased interest in probiotics is essentially due to the problem of microbial resistance to antibiotics and following the ban of the use of antibiotics in animal production, probiotics being considered an alternative means to reduce pathogen infection and improve animal health especially around the time of weaning. However, there is still a need to clarify the probiotic effectiveness in pigs, and the underlying mechanisms. When assessing the efficacy of probiotics one must consider the particular strain of organism being used and the production stage of the pigs being treated. The reproducible delivery of probiotics in industrial pig production is problematic as maintenance of viability is key to their beneficial activity, but difficult to achieve with commonly used feed processing technologies. One specific context where probiotics organisms may be reliably delivered is in systems utilising fermented liquid feeds. Liquid feed may be fermented by the activity of wild lactic acid bacteria or may be stimulated using specific isolates as ‘starters’; the latter system has advantages in terms of reproducibility and speed of fermentation. The farm context in which the organism is used is likely to be critical; the use of probiotics is more likely to result in measurable economic gains in animals living in sub-optimal conditions rather than in those reared in the highest welfare and husbandry conditions. The establishment of a beneficial lactic acid bacteria population at birth may lead to healthier animals, this may be most effectively achieved by treating sows, which provide an amplification step and flood the neonatal pigs’ environment with desirable bacterial strains. In contrast, it may be sufficient to provide a supportive, protective microbiota around the time of weaning as this is a time of major crisis with instability and loss of certain bacterial populations.

Keywords

pigprobioticperfomancehealth
Type
Full Paper
Information
animal , Volume 5 , Issue 3 , March 2011 , pp. 462 - 470
Copyright
Copyright © The Animal Consortium 2011

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References

Alakomi, HL, Skytta, E, Saarela, M, Mattila-Sandholm, T, Latva-Kala, K, Helander, IM 2000. Lactic acid permeabilizes gram-negative bacteria by disrupting the outer membrane. Applied and Environmental Microbiology 66, 2001–2005.CrossRefGoogle ScholarPubMed
Bäckhed, F, Ding, H, Wang, T, Hooper, LV, Koh, GY, Nagy, A, Semenkovich, CF, Gordon, JI 2004. The gut microbiota as an environmental factor that regulates fat storage. Proceedings of the National Academy of Sciences of the United States of America 101, 15718–15723.CrossRefGoogle ScholarPubMed
Bailey, M 2009. The mucosal immune system: recent developments and future directions in the pig. Developmental and Comparative Immunology 33, 375–383.CrossRefGoogle ScholarPubMed
Biasucci, G, Benenati, B, Morelli, L, Bessi, E, Boehm, G 2008. Cesarean delivery may affect the early biodiversity of intestinal bacteria. Journal of Nutrition 138, 1796s–1800s.CrossRefGoogle ScholarPubMed
Bibiloni, R, Fedorak, RN, Tannock, GW, Madsen, KL, Gionchetti, P, Campieri, M, De Simone, C, Sartor, RB 2005. VSL3 probiotic-mixture induces remission in patients with active ulcerative colitis. American Journal of Gastroenterology 100, 1539–1546.CrossRefGoogle Scholar
Bird, AR, Vuaran, M, Crittenden, R, Hayakawa, T, Playne, MJ, Brown, IL, Topping, DL 2009. Comparative effects of a high-amylose starch and a fructooligosaccharide on fecal bifidobacteria numbers and short-chain fatty acids in pigs fed Bifidobacterium animalis. Digestive Diseases and Sciences 54, 947–954.CrossRefGoogle Scholar
Boesen, HT, Jensen, TK, Schmidt, AS, Jensen, BB, Jensen, SM, Moller, K 2004. The influence of diet on Lawsonia intracellularis colonization in pigs upon experimental challenge. Veterinary Microbiology 103, 35–45.CrossRefGoogle ScholarPubMed
Boirivant, M, Amendola, A, Butera, A 2008. Intestinal microflora and immunoregulation. Mucosal Immunology 1, S47–S49.CrossRefGoogle ScholarPubMed
Bomba, A, Nemcova, R, Gancarcikova, S, Herich, R, Guba, P, Mudronova, D 2002. Improvement of the probiotic effect of micro-organisms by their combination with maltodextrins, fructo-oligosaccharides and polyunsaturated fatty acids. British Journal of Nutrition 88, S95–S99.CrossRefGoogle ScholarPubMed
Bry, L, Falk, PG, Midtvedt, T, Gordon, JI 1996. A model of host-microbial interactions in an open mammalian ecosystem. Science 273, 1380–1383.CrossRefGoogle Scholar
Caballero-Franco, C, Keller, K, De Simone, C, Chadee, K 2007. The VSL3 probiotic formula induces mucin gene expression and secretion in colonic epithelial cells. American Journal of Physiology-Gastrointestinal and Liver Physiology 292, G315–G322.CrossRefGoogle Scholar
Calder, PC, Krauss-Etschmann, S, de Jong, EC, Dupont, C, Frick, JS, Frokiaer, H, Heinrich, J, Garn, H, Koletzko, S, Lack, G, Mattelio, G, Renz, H, Sangild, PT, Schrezenmeir, J, Stulnig, TM, Thymann, T, Wold, AE, Koletzko, B 2006. Early nutrition and immunity – progress and perspectives. British Journal of Nutrition 96, 774–790.Google Scholar
Canibe, N, Jensen, BB 2003. Fermented and nonfermented liquid feed to growing pigs: effect on aspects of gastrointestinal ecology and growth performance. Journal of Animal Science 81, 2019–2031.CrossRefGoogle ScholarPubMed
Canibe, N, Hojberg, O, Badsberg, JH, Jensen, BB 2007. Effect of feeding fermented liquid feed and fermented grain on gastrointestinal ecology and growth performance in piglets. Journal of Animal Science 85, 2959–2971.CrossRefGoogle ScholarPubMed
Cheeson, A 1994. Probiotics and other intestinal mediators. In Principles of pig science (ed. DJA Cole, J Wiseman and MA Varley), pp. 197–214. Nottingham University Press, Nottingham.Google Scholar
Coconnier-Polter, MH, Moal, VLL, Servin, AL 2005. A Lactobacillus acidophilus strain of human gastrointestinal microbiota origin elicits killing of enterovirulent Salmonella enterica serovar typhimurium by triggering lethal bacterial membrane damage. Applied and Environmental Microbiology 71, 6115–6120.CrossRefGoogle ScholarPubMed
Collado, MC, Isolauri, E, Salminen, S, Sanz, Y 2009. The impact of probiotic on gut health. Current Drug Metabolism 10, 68–78.CrossRefGoogle ScholarPubMed
Cotter, PD, Hill, C, Ross, RP 2005. Bacteriocins: developing innate immunity for food. Nature Reviews Microbiology 3, 777–788.CrossRefGoogle ScholarPubMed
Doron, SI, Hibberd, PL, Gorbach, SL 2008. Probiotics for prevention of antibiotic-associated diarrhea. Journal of Clinical Gastroenterology 42, S58–S63.CrossRefGoogle ScholarPubMed
Dritz, SS, Tokach, MD, Goodband, RD, Nelssen, JL 2002. Effects of administration of antimicrobials in feed on growth rate and feed efficiency of pigs in multisite production systems. Journal of the American Veterinary Medical Association 220, 1690–1695.CrossRefGoogle ScholarPubMed
Duncker, SC, Lorentz, A, Schroeder, B, Breves, G, Bischoff, SC 2006. Effect of orally administered probiotic E.coli strain Nissle 1917 on intestinal mucosal immune cells of healthy young pigs. Veterinary Immunology and Immunopathology 111, 239–250.CrossRefGoogle ScholarPubMed
FAO/WHO (Food and Agriculture Organization/World Health Organisation) 2001. Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Report of a Joint FAO/WHO Expert Consultation on Evaluation of Health and Nutritional Properties of Probiotics in Food Including Powder Milk with Live Lactic Acid Bacteria, 1–4 October 2001, Córdoba, Argentina, pp. 1–33.Google Scholar
Favier, CF, Vaughan, EE, De Vos, WM, Akkermans, ADL 2002. Molecular monitoring of succession of bacterial communities in human neonates. Applied and Environmental Microbiology 68, 219–226.CrossRefGoogle ScholarPubMed
Fayol-Messaoudi, D, Berger, UN, Coconnier-Polter, MH, Lievin-Le Moal, V, Servin, AL 2005. pH-, lactic acid-, and non-lactic acid-dependent activities of probiotic lactobacilli against Salmonella enterica serovar typhimurium. Applied and Environmental Microbiology 71, 6008–6013.CrossRefGoogle ScholarPubMed
Fukushima, Y, Kawata, Y, Hara, H, Terada, A, Mitsuoka, T 1998. Effect of a probiotic formula on intestinal immunoglobulin A production in healthy children. International Journal of Food Microbiology 42, 39–44.CrossRefGoogle ScholarPubMed
Gronlund, MM, Lehtonen, OP, Eerola, E, Kero, P 1999. Fecal microflora in healthy infants born by different methods of delivery: permanent changes in intestinal flora after cesarean delivery. Journal of Pediatric Gastroenterology and Nutrition 28, 19–25.Google ScholarPubMed
Henker, J, Laass, MW, Blokhin, BM, Maydannik, VG, Bolbot, YK, Elze, M, Wolff, C, Schreiner, A, Schulze, J 2008. Probiotic Escherichia coli Nissle 1917 versus placebo for treating diarrhea of greater than 4 days duration in infants and toddlers. Pediatric Infectious Disease Journal 27, 494–499.CrossRefGoogle ScholarPubMed
Hooper, LV, Midtvedt, T, Gordon, JI 2002. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annual Review of Nutrition 22, 283–307.CrossRefGoogle ScholarPubMed
Huys, G, Vancanneyt, M, D’Haene, K, Vankerckhoven, V, Goossens, H, Swings, J 2006. Accuracy of species identity of commercial bacterial cultures intended for probiotic or nutritional use. Research in Microbiology 157, 803–810.CrossRefGoogle ScholarPubMed
Inman, CF, Haverson, K, Konstantinov, RS, Jones, PH, Harris, C, Smidt, H, Miller, B, Bailey, M, Stokes, C 2010. Rearing environment affects development of the immune system in neonates. Clinical and Experimental Immunology 160, 431–439. Epub ahead of print, doi:10.1111/j.1365-2249.2010.04090.x.CrossRefGoogle ScholarPubMed
Isolauri, E, Kalliomaki, M, Rautava, S, Salminen, S, Laitinen, K 2009. Obesity – extending the hygiene hypothesis. In Microbial–host interaction: tolerance versus allergy (ed. P Brandtzaeg, E Isolauri and SL Prescott), 64th Nestlé Nutrition Institute Workshop. Pediatric Program, pp. 75–89, (Summary pp. 251–257). Nestec Ltd, Vevey/S. Karger AG, Basel.CrossRefGoogle Scholar
Jin, LZ, Zhao, X 2000. Intestinal receptors for adhesive fimbriae of enterotoxigenic Escherichia coli (ETEC) K88 in swine – a review. Applied Microbiology and Biotechnology 54, 311–318.CrossRefGoogle ScholarPubMed
Kim, EY, Kim, YH, Rhee, MH, Song, JC, Lee, KW, Kim, KS, Lee, SP, Lee, IS, Park, SC 2007. Selection of Lactobacillus sp PSC101 that produces active dietary enzymes such as amylase, lipase, phytase and protease in pigs. Journal of General and Applied Microbiology 53, 111–117.CrossRefGoogle ScholarPubMed
Klaenhammer, TR, Altermann, E, Pfeiler, E, Brock, BL, Goh, YJ, O’Flaherty, S, Barrangou, R, Duong, T 2008. Functional genomics of probiotic Lactobacilli. Journal of Clinical Gastroenterology 42, S160–S162.CrossRefGoogle ScholarPubMed
Konstantinov, SR, Awati, AA, Williams, BA, Miller, BG, Jones, P, Stokes, CR, Akkermans, ADL, Smidt, H, de Vos, WM 2006. Post-natal development of the porcine microbiota composition and activities. Environmental Microbiology 8, 1191–1199.CrossRefGoogle ScholarPubMed
Konstantinov, SR, Smidt, H, Akkermans, ADL, Casini, L, Trevisi, P, Mazzoni, M, De Filippi, S, Bosi, P, de Vos, WM 2008. Feeding of Lactobacillus sobrius reduces Escherichia coli F4 levels in the gut and promotes growth of infected piglets. FEMS Microbiology Ecology 66, 599–607.CrossRefGoogle ScholarPubMed
Kritas, SK, Morrison, RB 2005. Evaluation of probiotics as a substitute for antibiotics in a large pig nursery. Veterinary Record 156, 447–448.CrossRefGoogle Scholar
Kumar, H, Kawai, T, Akira, S 2009. Toll-like receptors and innate immunity. Biochemical and Biophysical Research Communications 388, 621–625.CrossRefGoogle ScholarPubMed
Kyriakis, SC, Tsiloyiannis, VK, Vlemmas, J, Sarris, K, Tsinas, AC, Alexopoulos, C, Jansegers, L 1999. The effect of probiotic LSP 122 on the control of post-weaning diarrhoea syndrome of piglets. Research in Veterinary Science 67, 223–228.CrossRefGoogle ScholarPubMed
Lallès, J-P, Bosi, P, Smidt, H, Stokes, CR 2007. Nutritional management of gut health in pigs around weaning. Proceedings of the Nutrition Society 66, 260–268.CrossRefGoogle ScholarPubMed
Lawlor, PG, Lynch, PB, Gardiner, GE, Caffrey, PJ, O’Doherty, JV 2002. Effect of liquid feeding weaned pigs on growth performance to harvest. Journal of Animal Science 80, 1725–1735.CrossRefGoogle ScholarPubMed
Lee, B, Lee, JH, Lee, HS, Bae, EA, Huh, CS, Ahn, YT, Kim, DH 2009. Glycosaminoglycan degradation-inhibitory lactic acid bacteria ameliorate 2,4,6-trinitrobenzenesulfonic acid-induced colitis in mice. Journal of Microbiology and Biotechnology 19, 616–621.Google Scholar
Lessard, M, Dupuis, M, Gagnon, N, Nadeau, E, Matte, JJ, Goulet, J, Fairbrother, JM 2009. Administration of Pediococcus acidilactici or Saccharomyces cerevisiae boulardii modulates development of porcine mucosal immunity and reduces intestinal bacterial translocation after Escherichia coli challenge. Journal of Animal Science 87, 922–934.CrossRefGoogle ScholarPubMed
Linde, A, Ross, CR, Davis, EG, Dib, L, Blecha, F, Melgarejo, T 2008. Innate immunity and host defense peptides in veterinary medicine. Journal of Veterinary Internal Medicine 22, 247–265.CrossRefGoogle ScholarPubMed
Lodemann, U, Hubener, K, Jansen, N, Martens, H 2006. Effects of Enterococcus faecium NCIMB 10415 as probiotic supplement on intestinal transport and barrier function of piglets. Archives of Animal Nutrition 60, 35–48.CrossRefGoogle ScholarPubMed
Lodemann, U, Lorenz, BM, Weyrauch, KD, Martens, H 2008. Effects of Bacillus cereus var. toyoi as probiotic feed supplement on intestinal transport and barrier function in piglets. Archives of Animal Nutrition 62, 87–106.CrossRefGoogle ScholarPubMed
Lomax, AR, Calder, PC 2009. Probiotics, immune function, infection and inflammation: a review of the evidence from studies conducted in humans. Current Pharmaceutical Design 15, 1428–1518.CrossRefGoogle ScholarPubMed
Mack, DR, Michail, S, Wei, S, McDougall, L, Hollingsworth, MA 1999. Probiotics inhibit enteropathogenic E.coli adherence in vitro by inducing intestinal mucin gene expression. American Journal of Physiology – Gastrointestinal and Liver Physiology 276, G941–G950.CrossRefGoogle ScholarPubMed
Madsen, K, Cornish, A, Soper, P, McKaigney, C, Jijon, H, Yachimec, C, Doyle, J, Jewell, L, De Simone, C 2001. Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology 121, 580–591.CrossRefGoogle ScholarPubMed
Marchesi, J, Shanahan, F 2007. The normal intestinal microbiota. Current Opinion in Infectious Diseases 20, 508–513.CrossRefGoogle ScholarPubMed
Marcobal, A, Underwood, MA, Mills, DA 2008. Rapid determination of the bacterial composition of commercial probiotic products by terminal restriction fragment length polymorphism analysis. Journal of Pediatric Gastroenterology and Nutrition 46, 608–611.CrossRefGoogle ScholarPubMed
Martin, R, Delgado, S, Maldonado, A, Jimenez, E, Olivares, M, Fernandez, L, Sobrino, OJ, Rodriguez, JM 2009. Isolation of lactobacilli from sow milk and evaluation of their probiotic potential. Journal of Dairy Research 76, 418–425.CrossRefGoogle ScholarPubMed
McFall-Ngai, MJ 2002. Unseen forces: the influence of bacteria on animal development. Developmental Biology 242, 1–14.CrossRefGoogle ScholarPubMed
Metges, CC 2000. Contribution of microbial amino acids to amino acid homeostasis of the host. Journal of Nutrition 130, 1857S–1864S.CrossRefGoogle ScholarPubMed
Mimura, T, Rizzello, F, Helwig, U, Poggioli, G, Schreiber, S, Talbot, IC, Nicholls, RJ, Gionchetti, P, Campieri, M, Kamm, MA 2004. Once daily high dose probiotic therapy (VSL3) for maintaining remission in recurrent or refractory pouchitis. Gut 53, 108–114.CrossRefGoogle ScholarPubMed
Mondel, M, Schroeder, BO, Zimmermann, K, Huber, H, Nuding, S, Beisner, J, Fellermann, K, Stange, EF, Wehkamp, J 2009. Probiotic E. coli treatment mediates antimicrobial human beta-defensin synthesis and fecal excretion in humans. Mucosal Immunology 2, 166–172.CrossRefGoogle ScholarPubMed
Mueller, S, Saunier, K, Hanisch, C, Norin, E, Alm, L, Midtvedt, T, Cresci, A, Silvi, S, Orpianesi, C, Verdenelli, MC, Clavel, T, Koebnick, C, Zunft, HJF, Dore, J, Blaut, M 2006. Differences in fecal microbiota in different European study populations in relation to age, gender, and country: a cross-sectional study. Applied and Environmental Microbiology 72, 1027–1033.CrossRefGoogle ScholarPubMed
Mulder, IE, Schmidt, B, Stokes, CR, Lewis, M, Bailey, M, Aminov, RI, Prosser, JI, Gill, BP, Pluske, JR, Mayer, CD, Musk, CC, Kelly, D 2009. Environmentally-acquired bacteria influence microbial diversity and natural innate immune responses at gut surfaces. BMC Biology 7, Article number 79.CrossRefGoogle ScholarPubMed
Nanthakumar, NN, Dai, DW, Newburg, DS, Walker, WA 2003. The role of indigenous microflora in the development of murine intestinal fucosyl- and sialyltransferases. FASEB Journal 17, 44–46.CrossRefGoogle ScholarPubMed
Niven, SJ, Beal, JD, Brooks, PH 2006. The effect of controlled fermentation on the fate of synthetic lysine in liquid diets for pigs. Animal Feed Science and Technology 129, 304–315.CrossRefGoogle Scholar
O’Hara, AM, O’Regan, P, Fanning, A, O’Mahony, C, MacSharry, J, Lyons, A, Bienenstock, J, O’Mahony, L, Shanahan, F 2006. Functional modulation of human intestinal epithelial cell responses by Bifidobacterium infantis and Lactobacillus salivarius. Immunology 118, 202–215.CrossRefGoogle ScholarPubMed
Ouwehand, AC, Salminen, S, Isolauri, E 2002. Probiotics: an overview of beneficial effects. Antonie van Leeuwenhoek – International Journal of General and Molecular Microbiology 82, 279–289.CrossRefGoogle ScholarPubMed
Parkes, GC, Sanderson, JD, Whelan, K 2009. The mechanisms and efficacy of probiotics in the prevention of Clostridium difficile-associated diarrhoea. Lancet Infectious Diseases 9, 237–244.CrossRefGoogle ScholarPubMed
Penders, J, Stobberingh, EE, Van den Brandt, PA, Thijs, C 2007. The role of the intestinal microbiota in the development of atopic disorders. Allergy 62, 1223–1236.CrossRefGoogle ScholarPubMed
Pieper, R, Janczyk, P, Urubschurov, V, Korn, U, Pieper, B, Souffrant, WB 2009. Effect of a single oral administration of Lactobacillus plantarum DSMZ 8862/8866 before and at the time point of weaning on intestinal microbial communities in piglets. International Journal of Food Microbiology 130, 227–232.CrossRefGoogle ScholarPubMed
Plumed-Ferrer, C, von Wright, A 2009. Fermented pig liquid feed: nutritional, safety and regulatory aspects. Journal of Applied Microbiology 106, 351–368.CrossRefGoogle ScholarPubMed
Plumed-Ferrer, C, Kivela, I, Hyvonen, P, Wright, A 2005. Survival, growth and persistence under farm conditions of a Lactobacillus plantarum strain inoculated into liquid pig feed. Journal of Applied Microbiology 99, 851–858.CrossRefGoogle ScholarPubMed
Putaala, H, Salusjarvi, T, Nordstrom, M, Saarinen, M, Ouwehand, AC, Hansen, EB, Rautonen, N 2008. Effect of four probiotic strains and Escherichia coli O157:H7 on tight junction integrity and cyclo-oxygenase expression. Research in Microbiology 159, 692–698.CrossRefGoogle ScholarPubMed
Rachmilewitz, D, Katakura, K, Karmeli, F, Hayashi, T, Reinus, C, Rudensky, B, Akira, S, Takeda, K, Lee, J, Takabayashi, K, Raz, E 2004. Toll-like receptor 9 signaling mediates the anti-inflammatory effects of probiotics in murine experimental colitis. Gastroenterology 126, 520–528.CrossRefGoogle ScholarPubMed
Resta, SC 2009. Effects of probiotics and commensals on intestinal epithelial physiology: implications for nutrient handling. Journal of Physiology (London) 587, 4169–4174.CrossRefGoogle ScholarPubMed
Rinne, M, Kalliomaki, M, Arvilommi, H, Salminen, S, Isolauri, E 2005. Effect of probiotics and breastfeeding on the Bifidobacterium and Lactobacillus/Enterococcus microbiota and humoral immune responses. Journal of Pediatrics 147, 186–191.CrossRefGoogle ScholarPubMed
Roselli, M, Finamore, A, Britti, MS, Konstantinov, SR, Smidt, H, de Vos, WM, Mengheri, E 2007. The novel porcine Lactobacillus sobrius strain protects intestinal cells from enterotoxigenic Escherichia coli K88 infection and prevents membrane barrier damage. Journal of Nutrition 137, 2709–2716.CrossRefGoogle ScholarPubMed
Savilahti, E, Kuitunen, M, Vaarala, O 2008. Pre and probiotics in the prevention and treatment of food allergy. Current Opinion in Allergy and Clinical Immunology 8, 243–248.CrossRefGoogle ScholarPubMed
Sazawal, S, Hiremath, G, Dhingra, U, Malik, P, Deb, S, Black, RE 2006. Efficacy of probiotics in prevention of acute diarrhoea: a meta-analysis of masked, randomised, placebo-controlled trials. Lancet Infectious Diseases 6, 374–382.CrossRefGoogle ScholarPubMed
Scharek, L, Guth, J, Filter, M, Schmidt, MFG 2007. Impact of the probiotic bacteria Enterococcus faecium NCIMB 10415 (SF68) and Bacillus cereus var. toyoi NCIMB 40112 on the development of serum IgG and faecal IgA of sows and their piglets. Archives of Animal Nutrition 61, 223–234.CrossRefGoogle ScholarPubMed
Schlee, M, Harder, J, Koten, B, Stange, EF, Wehkamp, J, Fellermann, K 2008. Probiotic lactobacilli and VSL3 induce enterocyte beta-defensin 2. Clinical and Experimental Immunology 151, 528–535.CrossRefGoogle Scholar
Sears, CL 2005. A dynamic partnership: celebrating our gut flora. Anaerobe 11, 247–251.CrossRefGoogle ScholarPubMed
Servin, AL 2004. Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiology Reviews 28, 405–440.CrossRefGoogle ScholarPubMed
Setia, A, Bhandari, SK, House, JD, Nyachoti, CM, Krause, DO 2009. Development and in vitro evaluation of an Escherichia coli probiotic able to inhibit the growth of pathogenic Escherichia coli K88. Journal of Animal Science 87, 2005–2012.CrossRefGoogle ScholarPubMed
Shanahan, F 2009. Therapeutic implications of manipulating and mining the microbiota. Journal of Physiology (London) 587, 4175–4179.CrossRefGoogle ScholarPubMed
Shimosato, T, Tohno, M, Kitazawa, H, Katoh, S, Watanabe, K, Kawai, Y, Aso, H, Yamaguchi, T, Saito, T 2005. Toll-like receptor 9 is expressed on follicle-associated epithelia containing M cells in swine Peyer’s patches. Immunology Letters 98, 83–89.CrossRefGoogle ScholarPubMed
Strachan, DP 1989. Hay-fever, hygiene, and household size. British Medical Journal 299, 1259–1260.CrossRefGoogle ScholarPubMed
Su, Y, Yao, W, Perez-Gutierrez, ON, Smidt, H, Zhu, WY 2008. Changes in abundance of Lactobacillus spp. and Streptococcus suis in the stomach, jejunum and ileum of piglets after weaning. FEMS Microbiology Ecology 66, 546–555.CrossRefGoogle ScholarPubMed
Sutmuller, RPM, Morgan, ME, Netea, MG, Grauer, O, Adema, GJ 2006. Toll-like receptors on regulatory T cells: expanding immune regulation. Trends in Immunology 27, 387–393.CrossRefGoogle ScholarPubMed
Szabo, I, Wieler, LH, Tedin, K, Scharek-Tedin, L, Taras, D, Hensel, A, Appel, B, Nockler, K 2009. Influence of a probiotic strain of Enterococcus faecium on Salmonella enterica Serovar Typhimurium DT104 infection in a porcine anima linfection model. Applied and Environmental Microbiology 75, 2621–2628.CrossRefGoogle Scholar
Taras, D, Vahjen, W, Macha, M, Simon, O 2005. Response of performance characteristics and fecal consistency to long-lasting dietary supplementation with the probiotic strain Bacillus cereus var. toyoi to sows and piglets. Archives of Animal Nutrition 59, 405–417.CrossRefGoogle ScholarPubMed
Thanantong, N, Edwards, S, Sparagano, OAE 2006. Characterization of lactic acid bacteria and other gut bacteria in pigs by a macroarraying method. Impact of emerging zoonotic diseases on animal health. Annals of the New York Academy of Sciences 1081, 276–279.CrossRefGoogle Scholar
Thomas, AV, Broers, AD, Vandegaart, HF, Desmecht, DJM 2006. Genomic structure, promoter analysis and expression of the porcine (Sus scrofa) TLR4 gene. Molecular Immunology 43, 653–659.CrossRefGoogle ScholarPubMed
Tohno, M, Kitazawa, H, Shimosato, T, Matsumoto, M, Katoh, S, Kawai, Y, Saito, T 2005. A swine toll-like receptor 2-expressing transfectant as a potential primary screening system for immunobiotic microorganisms. FEMS Immunology and Medical Microbiology 44, 283–288.CrossRefGoogle ScholarPubMed
Trevisi, P, De Filippi, S, Minieri, L, Mazzoni, M, Modesto, M, Biavati, B, Bosi, P 2008. Effect of fructo-oligosaccharides and different doses of Bifidobacterium animalis in a weaning diet on bacterial translocation and Toll-like receptor gene expression in pigs. Nutrition 24, 1023–1029.CrossRefGoogle Scholar
Turnbaugh, PJ, Ley, RE, Mahowald, MA, Magrini, V, Mardis, ER, Gordon, JI 2006. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027–1031.CrossRefGoogle ScholarPubMed
van Baarlen, P, Troost, FJ, van Hemert, S, van der Meer, C, de Vos, WM, de Groot, PJ, Hooiveld, GJ, Brummer, RJ, Kleerebezem, M 2009. Differential NF-{kappa}B pathways induction by Lactobacillus plantarum in the duodenum of healthy humans correlating with immune tolerance. Proceedings of the National Academy of Sciences of the United States of America 106, 2371–2376.CrossRefGoogle ScholarPubMed
van der Wolf, PJ, Wong, DMAL, Wolbers, WB, Elbers, ARW, van der Heijden, HMJF, van Schie, FW, Hunneman, WA, Willeberg, P, Tielen, MJM 2001. A longitudinal study of Salmonella enterica infections in high- and low-seroprevalence finishing swine herds in the Netherlands. Veterinary Quarterly 23, 116–121.CrossRefGoogle ScholarPubMed
van Winsen, RL, Keuzenkamp, D, Urlings, BAP, Lipman, LJA, Snijders, JAM, Verheijden, JHM, van Knapen, F 2002. Effect of fermented feed on shedding of Enterobacteriaceae by fattening pigs. Veterinary Microbiology 87, 267–276.CrossRefGoogle ScholarPubMed
Vrieze, A, Holleman, F, Zoetendal, EG, de Vos, WM, Hoekstra, JB, Nieuwdorp, M 2010. The environment within: how gut microbiota may influence metabolism and body composition. Diabetologia 53, 606–613.CrossRefGoogle ScholarPubMed
Wagner, RD 2008. Effects of microbiota on GI health: gnotobiotic research. GI microbiota and regulation of the immune system. Advances in Experimental Medicine and Biology 635, 41–56.CrossRefGoogle Scholar
Walsh, MC, Gardiner, GE, Hart, OM, Lawlor, PG, Daly, M, Lynch, B, Richert, BT, Radcliffe, S, Giblin, L, Hill, C, Fitzgerald, GF, Stanton, C, Ross, P 2008. Predominance of a bacteriocin-producing Lactobacillus salivarius component of a five-strain probiotic in the porcine ileum and effects on host immune phenotype. FEMS Microbiology Ecology 64, 317–327.CrossRefGoogle ScholarPubMed
Wang, AN, Yu, HF, Gao, X, Li, XJ, Qiao, SY 2009. Influence of Lactobacillus fermentum I5007 on the intestinal and systemic immune responses of healthy and E. coli challenged piglets. Antonie van Leeuwenhoek – International Journal of General and Molecular Microbiology 96, 89–98.CrossRefGoogle ScholarPubMed
Wen, K, Azevedo, MSP, Gonzalez, A, Zhang, W, Saif, LJ, Li, GH, Yousef, A, Yuan, LJ 2009. Toll-like receptor and innate cytokine responses induced by lactobacilli colonization and human rotavirus infection in gnotobiotic pigs. Veterinary Immunology and Immunopathology 127, 304–315.CrossRefGoogle ScholarPubMed
Wierup, M 2001. The Swedish experience of the 1986 year ban of antimicrobial growth promoters, with special reference to animal health, disease prevention, productivity, and usage of antimicrobials. Microbial Drug Resistance – Mechanisms Epidemiology and Disease 7, 183–190.CrossRefGoogle ScholarPubMed
Williams, AM, Probert, CSJ, Stepankova, R, Tlaskalova-Hogenova, H, Phillips, A, Bland, PW 2006. Effects of microflora on the neonatal development of gut mucosal T cells and myeloid cells in the mouse. Immunology 119, 470–478.CrossRefGoogle ScholarPubMed
Zeyner, A, Boldt, E 2006. Effects of a probiotic Enterococcus faecium strain supplemented from birth to weaning on diarrhoea patterns and performance of piglets. Journal of Animal Physiology and Animal Nutrition 90, 25–31.CrossRefGoogle ScholarPubMed
Zhang, W, Wen, K, Azevedo, MSP, Gonzalez, A, Saif, LJ, Li, G, Yousef, AE, Yuan, L 2008. Lactic acid bacterial colonization and human rotavirus infection influence distribution and frequencies of monocytes/macrophages and dendritic cells in neonatal gnotobiotic pigs. Veterinary Immunology and Immunopathology 121, 222–231.CrossRefGoogle ScholarPubMed
Zoetendal, EG, Akkermans, ADL, Akkermans-Van Vliet, WM, de Visser, JAGM, de Vos, WM 2001. The host genotype affects the bacterial community in the human gastrointestinal tract. Microbial Ecology in Health and Disease 13, 129–134.CrossRefGoogle Scholar