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Probiotic alternatives to reduce gastrointestinal infections: the poultry experience

Published online by Cambridge University Press:  28 February 2007

G. M. Nava ,
L. R. Bielke ,
T. R. Callaway  and
M. P Castañeda
G. M. Nava*
Affiliation:
Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autonoma de Mexico, Mexico City 04510, Mexico
L. R. Bielke
Affiliation:
Department of Poultry Science, University of Arkansas, Fayetteville AR 72701, USA
T. R. Callaway
Affiliation:
USDA/ARS/SPARC/FFSRU, 2881 F&B Road, College Station, TX 77845, USA
M. P Castañeda
Affiliation:
Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autonoma de Mexico, Mexico City 04510, Mexico
*
*Animal Science, Laboratory, Room 410, University of Illinois, Urbana-Champaign, 1207 W. Gregory Avenue, Urbana, IL 61801, USA., navag@runbox.com and gnavamo2@uiuc.edu
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Abstract

The intestinal mucosa represents the most active defense barrier against the continuous challenge of food antigens and pathogenic microorganisms present in the intestinal lumen. Protection against harmful agents is conferred by factors such as gastric acid, peristalsis, mucus, intestinal proteolysis, and the intestinal biota. The establishment of beneficial bacterial communities and metabolites from these complex ecosystems has varying consequences for host health. This hypothesis has led to the introduction of novel therapeutic interventions based on the consumption of beneficial bacterial cultures. Mechanisms by which probiotic bacteria affect the microecology of the gastrointestinal tract are not well understood, but at least three mechanisms of action have been proposed: production/presence of antibacterial substances (e.g., bacteriocins or colicins), modulation of immune responses and specific competition for adhesion receptors to intestinal epithelium. The rapid establishment of bacterial communities has been thought to be essential for the prevention of colonization by pathogenic bacteria. Some animal models suggest that the reduction in bacterial translocation in neonatal animals could be associated with an increase in intestinal bacterial communities and bacteriocin-like inhibitory substances produced by these species. This review emphasizes the role of the intestinal microbiota in the reduction of the gastrointestinal infections and draws heavily on studies in poultry.

Keywords

probioticmicrobiotaintestineSalmonellachicken
Type
Research Article
Information
Animal Health Research Reviews , Volume 6 , Issue 1 , June 2005 , pp. 105 - 118
Copyright
Copyright © CAB International 2005

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References

Abreu, MT, Vora, P, Faure, E, Thomas, LS, Arnold, ET and Arditi, M (2001). Decreased expression of Toll-like receptor-4 and MD-2 correlates with intestinal epithelial cell protection against dysregulated proinflammatory gene expression in response to bacterial lipopolysaccharide. Journal of Immunology 167: 1609–1616.CrossRefGoogle ScholarPubMed
Anderson, WR, Mitchell, WR, Barnum, DA and Julian, RJ (1984). Practical aspects of competitive exclusion for the control of Salmonella in turkeys. Avian Diseases 28: 1071–1078.CrossRefGoogle ScholarPubMed
Ardawi, MS and Newshole, EA (1985). Fuel utilization in colonocytes of the rat. Biochemical Journal 231: 713–719.CrossRefGoogle ScholarPubMed
Argenzio, RA, Southworth, M, Lowe, JE and Stevens, CE (1977). Inter/relationship of Na, HCO 3 and volatile fatty acid transport by equine large intestine. American Journal of Physiology 233: 469–478.Google Scholar
Ash, R and Dobson, A (1963). The effect of absorption on the acidity of the rumen contents. Journal of Physiology 169: 36–61.CrossRefGoogle ScholarPubMed
Audisio, MC, Oliver, G and Apella, MC (1999). Antagonistic effect of Enterococcus faecium J96 against human and poultry pathogenic Salmonella spp. Journal of Food Protection 62: 751–755.CrossRefGoogle ScholarPubMed
Audisio, M, Oliver, G and Apella, MC (2001). Effect of different complex carbon source on growth and bacteriocin synthesis of Enterococcus faecium. International Journal of Food Microbiology 63: 235–241.CrossRefGoogle ScholarPubMed
Baba, E, Nagaishi, S, Fukata, T and Arakawa, A (1991). The role of intestinal microflora on the prevention of Salmonella colonization on gnotobiotic chickens. Poultry Science 70: 1902–1907.CrossRefGoogle ScholarPubMed
Bailey, JS, Blankenship, JL, Stern, NJ, Cox, NA and McHan, F (1988). Effect of anticoccidial and antimicrobial feed additives on prevention of Salmonella colonization of chicks treated with anaerobic cultures of chicken feces. Avian Diseases 32: 324–329.CrossRefGoogle ScholarPubMed
Balla, E, Dicks, LMT, Du Toit, M, Van Der Merwe, MJ and Holzapfel, WH (2000). Characterization and cloning of the genes encoding enterocin 1071a and enterocin 1071B, two anitimicrobial peptides produced by Enterococcus faecalis BFE 1071. Applied and Environmental Microbiology 66: 1298–1304.CrossRefGoogle Scholar
Banasaz, M, Norin, E, Holma, R and Midtvedt, T (2002). Increased enterocyte production in gnotobiotic rats mono-associated with Lactobacillus rhamnosus GG. Applied Environmental Microbiology 68: 3031–3034.CrossRefGoogle ScholarPubMed
Barcelo, A, Claustre, J, Moro, F, Chayvialle, JA, Cuber, JC and Plaisancie, P (2000). Mucin secretion is modulated by luminal factors in the isolated vascularly perfused rat colon. Gut 46: 218–224.CrossRefGoogle ScholarPubMed
Barefoot, SF and Klaenhammer, TR (1983). Detection and activity of lactacin B, a bacteriocin produced by Lactobacillus acidophilus. Applied and Environmental Microbiology 45: 1808–1815.CrossRefGoogle ScholarPubMed
Barnes, EM, Impey, CS and Stevens, BJH (1979). Factors affecting the incidence and anti-salmonella activity of the anaerobic caecal flora of young chick. Journal of Hygiene 82: 263–283.CrossRefGoogle ScholarPubMed
Barrow, PA and Tucker, JF (1986). Inhibition of colonization of the chicken caecum with Salmonella typhimurium by pre-treatment with strains of Escherichia coli. Journal of Hygiene (London) 96: 161–169.CrossRefGoogle ScholarPubMed
Blankenship, LC, Bailey, JS, Cox, NA, Stern, NJ, Brewer, R and Williams, O (1993). Two-step mucosal competitive exclusion flora treatment to diminish salmonellae in commercial broiler chickens. Poultry Science 72: 1667–1672.CrossRefGoogle ScholarPubMed
Bennet, R, Eriksson, M, Nord, CE and Zetterstrom, R (1986). Fecal bacterial microflora of newborn infants during intensive care management and treatment with five antibiotic regimens. Pediatric Infectious Disease Journal 5: 533–539.CrossRefGoogle ScholarPubMed
Bielke, LR, Elwood, AL, Donoghue, DJ, Donoghue, AM, Newberry, LA, Neighbor, NK and Hargis, BM (2003). Approach for selection of individual enteric bacteria for competitive exclusion in turkey poults. Poultry Science 82: 1378–1382.CrossRefGoogle ScholarPubMed
Booth, SJ, Johnson, JL and Wilkins, TD (1977). Bacteriocin production by strains of bacteroides isolated from human feces and the role of these strains in the bacterial ecology of the colon. Antimicrobial Agents and Chemotherapy 11: 718–724.CrossRefGoogle ScholarPubMed
Borruel, N, Casellas, F, Antolin, M, Llopis, M, Carol, M, Espiin, E, Naval, J, Guarner, F and Malagelada, JR (2003). Effects of nonpathogenic bacteria on cytokine secretion by human intestinal mucosa. American Journal of Gastroenterology 98: 865–870.CrossRefGoogle ScholarPubMed
Braat, H, van den Brande, J, van Tol, E, Hommes, D, Peppelenbosch, M and van Deventer, S (2004). Lactobacillus rhamnosus induces peripheral hyporesponsiveness in stimulated CD4+ T cells via modulation of dendritic cell function. American Journal of Clinical Nutrition 80: 1618–1625.CrossRefGoogle ScholarPubMed
Brook, I, Barrett, CT, Brinkman, CR III, Martin, WJ and Finegold, SM (1979). Aerobic and anaerobic bacterial flora of the maternal cervix and newborn gastric fluid and conjunctiva: a prospective study. Pediatrics 63: 451–455.CrossRefGoogle ScholarPubMed
Butler, RN, Stafford, I, Triantafillos, E, O'Dee, CD, Jarrett, IG, Fettman, MJ and Roberts-Thomson, IC (1990). Pyruvate sparing by butyrate and propionate in proliferating colonic epithelium. Comparative Biochemistry and Physiology B: Comparative Biochemistry 97: 333–337.CrossRefGoogle ScholarPubMed
Cano, PG and Perdigon, G (2003). Probiotics induce resistance to enteropathogens in a re-nourished mouse model. Journal of Dairy Research 70: 433–440.CrossRefGoogle Scholar
Carina Audisio, M, Oliver, G and Apella, MC (2000). Protective effect of Enterococcus faecium J96, a potential probiotic strain, on chicks infected with Salmonella pullorum. Journal of Food Protection 63: 1333–1337.CrossRefGoogle ScholarPubMed
Carroll, SM, Mayrhofer, G, Dawkins, HJ and Grove, DI (1984). Kinetics of intestinal lamina propria mast cells, globule leucocytes, intraepithelial lymphocytes, goblet cells and eosinophils in murine strongyloidiasis. International Archives of Allergy and Applied Immunology 74: 311–317.CrossRefGoogle ScholarPubMed
Cason, JA, Cox, NA and Bailey, JS (1994). Transmission of Salmonella typhimurium during hatching of broiler chicks. Avian Diseases 38: 583–588.CrossRefGoogle ScholarPubMed
Center for Disease Control and Prevention (2000). CDC Surveillance Summaries, March 17, 2000. Morbidity and Mortality Weekly Report 49(SS-1).Google Scholar
Chang, YY and Cronan, JE Jr (1999). Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli. Molecular Microbiology 33: 249–259.CrossRefGoogle Scholar
Cherbut, C, Aube, AC, Blottiere, HM, Pacaud, P, Scarpignato, C and Galmiche, JP (1996). In vitro contractile effects of short chain fatty acids in the rat terminal ileum. Gut 38: 53–58.CrossRefGoogle ScholarPubMed
Cherbut, C, Ferrier, L, Roze, C, Anini, Y, Blottiere, H, Lecannu, G and Galmiche, JP (1998). Short-chain fatty acids modify colonic motility through nerves and polypeptide YY release in the rat. American Journal of Physiology 275: 1415–1422.Google ScholarPubMed
Cherbuy, C, Andrieux, C, Honvo-Houeto, E, Thomas, M, Ide, C, Druesne, N, Chaumontet, C, Darcy-Vrillon, B and Duee, PH (2004). Expression of mitochondrial HMGCoA synthase and glutaminase in the colonic mucosa is modulated by bacterial species. European Journal of Biochemistry 271: 87–95.CrossRefGoogle ScholarPubMed
Corrier, DE, Nisbet, DJ, Scanlan, MC, Tellez, G, Hargis, BM and DeLoach, JR (1994a). Inhibition of Salmonella enteritidis cecal and organ colonization in Leghorn chicks by a defined culture of cecal bacteria and dietary lactose. Journal of Food Protection 56: 337–381.Google Scholar
Corrier, DE, Hollister, AG, Nisbet, DJ, Scanlan, CM, Beier, RC and DeLoach, JR (1994b). Competitive exclusion of Salmonella enteritidis in leghorn chicks: comparison of treatment by crop gavage, drinking water, spray, or lyophilized alginate beads. Avian Diseases 38: 297–303.CrossRefGoogle ScholarPubMed
Corrier, DE, Nisbet, DJ, Scanlan, CM, Hollister, AG and Deloach, JR (1995a). Control of Salmonella typhimurium colonization in broiler chicks with a continuous-flow characterized mixed culture of cecal bacteria. Poultry Science 74: 916–924.CrossRefGoogle ScholarPubMed
Corrier, DE, Nisbet, DJ, Scanlan, CM, Hollister, AG, Caldwell, DJ, Thomas, LA, Hargis, BM, Tomkins, T and Deloach, JR (1995b). Treatment of commercial broiler chickens with a characterized culture of cecal bacteria to reduce salmonellae colonization. Poultry Science 74: 1093–1101.CrossRefGoogle ScholarPubMed
Corrier, DE, Nisbet, DJ, Hargis, BM, Holt, PS and DeLoach, JR (1997). Provision of lactose to molting hens enhances resistance to Salmonella enteritidis colonization. Journal of Food Protection 60: 10–15.CrossRefGoogle ScholarPubMed
Dabard, J, Bridonneau, A, Phillipe, C, Anglade, P, Molle, D, Nardi, M, Ladire, M, Girardin, H, Marcille, F, Gomez, A and Fons, M (2001). Ruminococci A, a new lantibiotic produced by a Ruminococcus gnavus strain isolated from human feces. Applied and Environmental Microbiology 67: 4111–4118.CrossRefGoogle Scholar
de Jong,, EC, Vieira, PL, Kalinski, P, Schuitemaker, JH, Tanaka, Y, Wierenga, EA, Yazdanbakhsh, M and Kapsenberg, ML (2002). Microbial compounds selectively induce Th1 cell-promoting or Th2 cell-promoting dendritic cells in vitro with diverse Th cell-polarizing signals. Journal of Immunology 168: 1704–1709.CrossRefGoogle ScholarPubMed
Duchmann, R, Kaiser, I, Hermann, E, Mayet, W, Ewe, K and Meyer zum Buschenfelde, KH (1995). Tolerance exists towards resident intestinal flora but is broken in active inflammatory bowel disease (IBD). Clinical and Experimental Immunology 102: 448–455.CrossRefGoogle ScholarPubMed
Eckmann, L, Kagnoff, MF and Fierer, J (1993). Epithelial cells secrete the chemokine interleukin-8 in response to bacterial entry. Infection and Immunity 61: 4569–4574.CrossRefGoogle ScholarPubMed
Eckmann, L, Stenson, WF, Savidge, TC, Lowe, DC, Barrett, KE, Fierer, J, Smith, JR and Kagnoff, MF (1997). Role of intestinal epithelial cells in the host secretory response to infection by invasive bacteria. Bacterial entry induces epithelial prostaglandin h synthase-2 expression and prostaglandin E2 and F2alpha production. Journal of Clinical Investigation 100: 296–309.CrossRefGoogle ScholarPubMed
Elewaut, D, DiDonato, JA, Kim, JM, Truong, F, Eckmann, L and Kagnoff, MF (1999). NF-kappa B is a central regulator of the intestinal epithelial cell innate immune response induced by infection with enteroinvasive bacteria. Journal of Immunology 163: 1457–1466.CrossRefGoogle ScholarPubMed
Ewing, WN and Cole, DJA (1994). The Living Gut. Dungannon, UK: Context Publications, p. 9.Google Scholar
Frankel, WL, Zhang, W, Singh, A, Klurfeld, DM, Don, S, Sakata, T, Modlin, I and Rombeau, JL (1994). Mediation of the trophic effects of short-chain fatty acids on the rat jejunum and colon. Gastroenterology 106: 375–380.CrossRefGoogle ScholarPubMed
Fukumoto, S, Tatewaki, M, Yamada, T, Fujimiya, M, Mantyh, C, Voss, M, Eubanks, S, Harris, M, Pappas, TN and Takahashi, T (2003). Short-chain fatty acids stimulate colonic transit via intraluminal 5-HT release in rats. The American Journal of Physiology–Regulatory, Integrative and Comparative Physiology 284: 1269–1276.CrossRefGoogle ScholarPubMed
Fuller, R (1989). Probiotics in man and animals. Applied Bacteriology 66: 365–378.Google Scholar
Fusunyan, RD, Quinn, JJ, Fujimoto, M, MacDermott, RP and Sanderson, IR (1999). Butyrate switches the pattern of chemokine secretion by intestinal epithelial cells through histone acetylation. Molecular Medicine 5: 631–640.CrossRefGoogle ScholarPubMed
Ganzle, MG, Hertel, C, van der Vossen, JM and Hammes, WP (1999). Effect of bacteriocin-producing lactobacilli on the survival of Escherichia coli and Listeria in a dynamic model of the stomach and the small intestine. International Journal of Food Microbiology 48: 21–35.CrossRefGoogle Scholar
Gaudier, E, Forestier, L, Gouyer, V, Huet, G, Julien, R and Hoebler, C (2004). Butyrate regulation of glycosylation-related gene expression: evidence for galectin-1 upregulation in human intestinal epithelial goblet cells. Biochemical and Biophysical Research Communications 325: 1044–1051.CrossRefGoogle ScholarPubMed
Gibson, GR and Wang, X (1994). Enrichment of bifidobacteria from human gut contents by oligofructose using continuous culture. FEMS Microbiology Letters 118: 121–127.CrossRefGoogle ScholarPubMed
Gomez, S, Cosson, C and Deschamps, AM (1997). Evidence for a bacteriocins-like substance produced by a new strain of Streptococcus sp., inhibitory to gram food-borne pathogens. Research in Immunology 148: 757–766.Google Scholar
Gordon, DM and Riley, MA (1999). A theoretical and empirical investigation of the invasion dynamics of colicinogeny. Microbiology 145: 655–661.CrossRefGoogle ScholarPubMed
Gronlund, MM, Lehtonen, OP, Eerola, E and 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
Guerin-Danan, C, Meslin, JC, Chambard, A, Charpilienne, A, Relano, P, Bouley, C, Cohen, J and Andrieux, C (2001). Food supplementation with milk fermented by Lactobacillus casei DN-114 001 protects suckling rats from rotavirus-associated diarrhea. Journal of Nutrition 131: 111–117.CrossRefGoogle ScholarPubMed
Gusils, C, Perez Chaia, A, Gonzalez, S and Oliver, G (1999a). Lactobacilli isolated from chicken intestines: potential use as probiotics. Journal of Food Protection 62: 252–256.CrossRefGoogle ScholarPubMed
Gusils, C, Gonzalez, SN and Oliver, G (1999b). Some probiotic properties of chicken lactobacilli. Canadian Journal of Microbiology 45: 981–987.CrossRefGoogle ScholarPubMed
Gusils, C, Morata, V and Gonzales, S (2004). Determination of bacterial adhesion to intestinal mucus. Methods in Molecular Biology 268: 411–415.Google ScholarPubMed
Ha, SD, Ricke, SC, Nisbet, DJ, Corrier, DE and DeLoach, JR (1994). Serine utilization as a potential competition mechanism between Salmonella and a chicken cecal bacterium. Journal of Food Protection 57: 1074–1079.CrossRefGoogle Scholar
Hakkinen, M and Schneitz, C (1999). Efficacy of a commercial competitive exclusion product against Campylobacter jejuni. British Poultry Science 40: 619–621.CrossRefGoogle ScholarPubMed
Hallstrom, M, Eerola, E, Vuento, R, Janas, M and Tammela, O (2004). Effects of mode of delivery and necrotising enterocolitis on the intestinal microflora in preterm infants. European Journal of Clinical Microbiology and Infectious Diseases 23: 463–470.CrossRefGoogle ScholarPubMed
Henning, SJ and Hird, FJ (1972). Transport of acetate and butyrate in the hind/gut of rabbits. Biochemical Journal 130: 791–796.CrossRefGoogle ScholarPubMed
Hinton, A, Jr Corrier, DE, Spates, GE, Norman, JO, Ziprin, RL, Beier, RC and DeLoach, JR (1990). Biological control of Salmonella typhimurium in young chickens. Avian Diseases 34: 626–633.CrossRefGoogle ScholarPubMed
Hinton, A, Jr Corrier, DE, Ziprin, RL, Spates, GE and DeLoach, JR (1991). Comparison of the efficacy of cultures of cecal anaerobes as inocula to reduce Salmonella typhimurium colonization in chicks with or without dietary lactose. Poultry Science 70: 67–73.CrossRefGoogle ScholarPubMed
Hollister, AG, Corrier, DE, Nisbet, DJ, Beier, RC and DeLoach, JR (1994). Comparison of effects of chicken cecal microorganisms maintained in continuous culture and provision of dietary lactose on cecal colonization by Salmonella typhimurium in turkey poults and broiler chicks. Poultry Science 73: 640–647.CrossRefGoogle ScholarPubMed
Hollister, AG, Corrier, DE, Nisbet, DJ and DeLoach, JR (1999). Effects of chicken derived cecal microorganisms maintained in continuous culture on cecal colonization by Salmonella typhimurium in turkey poults. Poutlry Science 78: 546–549.Google ScholarPubMed
Hosoi, T, Ametani, A, Kiuchi, K and Kaminogawa, S (1999). Changes in fecal microflora induced by intubation of mice with Bacillus subtilis (natto) spores are dependent upon dietary components. Canadian Journal of Microbiology 45: 59–66.CrossRefGoogle ScholarPubMed
Hosoi, T, Ametani, A, Kiuchi, K and Kaminogawa, S (2000). Improved growth and viability of lactobacilli in the presence of Bacillus subtilis (natto), catalase, or subtilisin. Canadian Journal of Microbiology 46: 892–897.CrossRefGoogle ScholarPubMed
Hoszowski, A and Truszczynski, M (1997). Prevention of Salmonella typhimurium caecal colonisation by different preparations for competitive exclusion. Compositions in Immunology and Infectious Diseases 20: 111–117.Google ScholarPubMed
Hume, ME, Hollister, AG, Nisbet, DJ, Corrier, DE and DeLoach, JR (1996a). Effect of a characterized continuous-flow culture of cecal bacteria on Salmonella typhimurium crop colonization in broiler chicks. Avian Diseases 40: 391–397.CrossRefGoogle ScholarPubMed
Hume, ME, Corrier, DE, Nisbet, DJ and DeLoach, JR (1996b). Reduction of Salmonella crop and cecal colonization by a characterized competitive exclusion culture in broilers during grow-out. Journal of Food Protection 59: 688–693.CrossRefGoogle ScholarPubMed
Hume, ME, Corrier, DE, Nisbet, DJ and DeLoach, JR (1998). Early Salmonella challenge time and reduction in chick cecal colonization following treatment with a characterized competitive exclusion culture. Journal of Food Protection 61: 673–676.CrossRefGoogle ScholarPubMed
Impey, CS, Mead, GC and Hinton, M (1987). Influence of continuous challenge via the feed on competitive exclusion of Salmonellas from broiler chicks. Journal of Applied Bacteriology 63: 139–146.CrossRefGoogle ScholarPubMed
Impey, CS and Mead, GC (1989). Fate of Salmonellas in the alimentary tract of chicks pre-treated with a mature caecal microflora to increase colonization resistance. Journal of Applied Bacteriology 66: 469–475.CrossRefGoogle ScholarPubMed
Isolauri, E, Kaila, M, Mykkanen, H, Ling, WH and Salminen, S (1994). Oral bacteriotherapy for viral gastroenteritis. Digestive Diseases and Sciences 39: 2595–2600.CrossRefGoogle ScholarPubMed
Jennes, W, Dicks, LM and Verwoerd, DJ (2000). Enterocin 012, a bacteriocin produced by Enterococcus gallinarum isolated from the intestinal tract of ostrich. Journal of Applied Microbiology 88: 349–357.CrossRefGoogle ScholarPubMed
Jin, LZ, Ho, YW, Abdullah, N and Jalaludin, S (2000). Digestive and bacterial enzyme activities in broilers fed diets supplemented with Lactobacillus cultures. Poultry Science 79: 886–891.CrossRefGoogle ScholarPubMed
Kibe, R, Sakamoto, M, Hayashi, H, Yokota, H and Benno, Y (2004). Maturation of the murine cecal microbiota as revealed by terminal restriction fragment length polymorphism and 16S rRNA gene clone libraries. FEMS Microbiology Letters 235: 139–146.CrossRefGoogle ScholarPubMed
Kim, BH, Kim, S, Kim, HG, Lee, J, Lee, IS and Park, YK (2005). The formation of cyclopropane fatty acids in Salmonella enterica serovar Typhimurium. Microbiology 151: 209–218.CrossRefGoogle ScholarPubMed
Koruda, MJ, Rolandelli, RH, Bliss, DZ, Hastings, J, Rombeau, JL and Settle, RG (1990). Parenteral nutrition supplemented with short-chain fatty acids: effect on the small-bowel mucosa in normal rats. American Journal Clinical Nutrition 51: 685–689.CrossRefGoogle ScholarPubMed
Kripke, SA, Fox, AD, Berman, JM, Settle, RG and Rombeau, JL (1989). Stimulation of intestinal mucosal growth with intracolonic infusion of short-chain fatty acids. Journal of Parenteral Enteral Nutrition 13: 109–116.CrossRefGoogle ScholarPubMed
Kubena, LF, Bailey, RH, Byrd, JA, Young, CR, Corrier, DE, Stanker, LH and Rottinghaust, GE (2001a). Cecal volatile fatty acids and broiler chick susceptibility to Salmonella typhimurium colonization as affected by aflatoxins and T-2 toxin. Poultry Science 80: 411–417.CrossRefGoogle ScholarPubMed
Kubena, LF, Byrd, JA, Young, CR and Corrier, DE (2001b). Effects of tannic acid on cecal volatile fatty acids and susceptibility to Salmonella typhimurium colonization in broiler chicks. Poultry Science 80: 1293–1298.CrossRefGoogle ScholarPubMed
Kwon, YM and Ricke, SC (1998). Induction of acid resistance of Salmonella typhimurium by exposure to short-chain fatty acids. Applied and Environmental Microbiology 64: 3458–3463.CrossRefGoogle ScholarPubMed
Lai, A, Fat, RF, McClelland, DB and van Furth, R (1976). In vitro synthesis of immunoglobulins, secretory component, complement and lysozyme by human gastrointestinal tissues. I. Normal tissues. Clinical Experimental Immunology 23: 9–19.Google Scholar
Leser, TD, Amenuvor, JZ, Jensen, TK, Lindecrona, RH, Boye, M and Moller, K (2002). Culture-independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited. Applied Environmental Microbiology 68: 673–690.CrossRefGoogle ScholarPubMed
Mackie, RI (1997). Gut environment and evolution of mutualistic fermentative digestion. In: Mackie, RI and White, BA (editors). Gastrointestinal Microbiology. New York: Chapman and Hall Press, pp. 13–35.CrossRefGoogle Scholar
Majarmaa, H and Isolauri, E (1997). Probiotics: a novel approach in the management of food allergy. Journal of Allergy and Clinical Immunology 99: 179–185.CrossRefGoogle Scholar
Marteau, P, Lepage, P, Mangin, I, Suau, A, Doré, J, Pochart, P and Seksik, P (2004). Gut flora and inflammatory bowel disease. Alimentary Pharmacology and Therapeutics 20: 18–23.CrossRefGoogle ScholarPubMed
Mathew, AG, Jones, T and Franklin, MA (1994). Effect of creep feeding on selected microflora and short-chain fatty acids in the ileum of weanling pigs. Journal of Animal Sciences 72: 3163–3168.CrossRefGoogle ScholarPubMed
McReynolds, JL, Caldwell, DY, McElroy, AP, Hargis, BM and Caldwell, DJ (2000). Antimicrobial residue detection in chicken yolk samples following administration to egg-producing chickens and effects of residue detection on competitive exclusion culture (PREEMPT) establishment. Journal of Agricultural Food Chemistry 48: 6435–6438.CrossRefGoogle ScholarPubMed
Mead,, GC (1989). Microbes of the avian caecum: types present and substrates utilised. Journal of Experimental Zoology 3: 48–54.CrossRefGoogle Scholar
Meijer-Severs, GJ, Van Santen, E and Meijer, BC (1990). Short-chain fatty acid and organic acid concentrations in feces of healthy human volunteers and their correlations with anaerobe cultural counts during systemic ceftriaxone administration. Scandinavian Journal of Gastroenterology 25: 698–704.CrossRefGoogle ScholarPubMed
Moreau, MC, Corthier, G, Muller, MC, Dubos, F and Raibaud, P (1986). Relationships between rotavirus diarrhea and intestinal microflora establishment in conventional and gnotobiotic mice. Journal of Clinical Microbiology 23: 863–868.CrossRefGoogle ScholarPubMed
Murray, CS and Woodcock, A (2002). Gut microflora and atopic disease. In: Tannock, GW (editor). Probiotics and Prebiotics: Where are We Going? Wymondham, UK: Caister Academic Press, pp. 239–261.Google Scholar
Neish, AS, Gewirtz, AT, Zeng, H, Young, AN, Hobert, ME, Karmali, V, Rao, AS and Madara, JL (2000). Prokaryotic regulation of epithelial responses by inhibition of IkappaB-alpha ubiquitination. Science 289: 1560–1563.CrossRefGoogle ScholarPubMed
Nisbet, DJ, Corrier, DE and DeLoach, JR (1993a). Effect of mixed cecal microflora maintained in continuous culture and of dietary lactose on Salmonella typhimurium colonization in broiler chicks. Avian Diseases 37: 528–535.CrossRefGoogle ScholarPubMed
Nisbet, DJ, Corrier, DE, Scalan, CM, Hollister, AG, Beier, RC and DeLoach, JR (1993b). Effect of a defined continuous-flow derived bacterial culture and dietary lactose on Salmonella typhimurium colonization in broiler chickens. Avian Diseases 37: 1017–1025.CrossRefGoogle ScholarPubMed
Nisbet, DJ, Corrier, DE, Ricke, SC, Hume, ME, Byrd, JA II and DeLoach, JR (1996). Maintenance of the biological efficacy in chicks of a cecal competitive-exclusion culture against Salmonella by continuous-flow fermentation. Journal of Food Protection 59: 1279–1283.CrossRefGoogle ScholarPubMed
Nishimura, A, Fujimoto, M, Oguchi, S, Fusunyan, RD, MacDermott, RP and Sanderson, IR (1998). Short-chain fatty acids regulate IGF-binding protein secretion by intestinal epithelial cells. American Journal of Physiology 275: 55–63.Google ScholarPubMed
Noack, J, Kleessen, B, Proll, J, Dongowski, G and Blaut, M (1998). Dietary guar gum and pectin stimulate intestinal microbial polyamine synthesis in rats. Nutrition 128: 1385–1391.Google ScholarPubMed
Nuotio, L, Schneitz, C, Halonen, U and Nurmi, E (1992). Use of competitive exclusion to protect newly-hatched chicks against intestinal colonisation and invasion by Salmonella enteritidis PT4. British Poultry Science 33: 775–779.CrossRefGoogle ScholarPubMed
Nurmi, E and Rantala, M (1973). New aspects of Salmonella infection in broiler production. Nature 241: 210–211.CrossRefGoogle ScholarPubMed
Nurmi, E (1974). The influence of zinc bacitracin on the colonization of Salmonella infantis in the intestine of broiler chickens. Research in Veterinary Science 17: 24–27.CrossRefGoogle ScholarPubMed
Nurmi, EV, Schneitz, CE and Makela, PH (1987). Process for the production of a bacterial preparation for the prophylaxis of intestinal disturbances in poultry. United States Patent 4,689,226.Google Scholar
Ono, S, Karaki, S and Kuwahara, A (2004). Short-chain fatty acids decrease the frequency of spontaneous contractions of longitudinal muscle via enteric nerves in rat distal colon. Japanese Journal of Physiology 54: 483–493.Google ScholarPubMed
Oumer, A, Garde, S, Gaya, P, Medina, M and Nunez, M (2001). The effects of cultivating lactic starter cultures with bacteriocin-producing lactic acid bacteria. Journal of Food Protection 64: 81–86.CrossRefGoogle ScholarPubMed
Palmu, L and Camelin, I (1997). The use of competitive exclusion in broilers to reduce the level of Salmonella contamination on the farm and at the processing plant. Poultry Science 76: 1501–1505.CrossRefGoogle ScholarPubMed
Pena, JA, Rogers, AB, Ge, Z, Ng, V, Li, SY, Fox, JG and Versalovic, J (2005). Probiotic Lactobacillus spp. diminish Helicobacter hepaticus -induced inflammatory bowel disease in interleukin-10-deficient mice. Infection and Immunology 73: 912–920.CrossRefGoogle ScholarPubMed
Perdigón, GC, Maldonado-Galdeano, J, Valdez, C and Medici, M (2002). Interaction of lactic acid bacteria with the gut immune system. European Journal of Clinical Nutrition 56: 21–27.CrossRefGoogle ScholarPubMed
Perdigon, G, Locascio, M, Medici, M, Pesce de Ruiz Holgado, A and Oliver, G (2003). Interaction of bifidobacteria with the gut and their influence in the immune function. Biocell 27: 1–9.CrossRefGoogle ScholarPubMed
Piva, A, Knudsen, KE and Lindberg, JE (2001). Gut Environment of Pigs. Nottingham, UK: Nottingham University Press, p. 105.Google Scholar
Portrait, V, Gendron-Gaillard, S, Cottenceau, G and Pons, AM (1999). Inhibition of pathogenic Salmonella enteritidis growth mediated by Escherichia coli microcin J25 producing strains. Canadian Journal of Microbiology 45: 988–994.CrossRefGoogle ScholarPubMed
Portrait, V, Cottenceau, G and Pons, AM (2000). A Fusobacterium mortiferum strain produces a bacteriocin-like substance(s) inhibiting Salmonella enteritidis. Letters in Applied Microbiology 31: 115–117.CrossRefGoogle ScholarPubMed
Prioult, G, Pecquet, S and Fliss, I (2004). Stimulation of interleukin-10 production by acidic beta-lactoglobulin-derived peptides hydrolyzed with Lactobacillus paracasei NCC2461 peptidases. Clinical and Diagnostic Laboratory Immunology 11: 266–271.Google ScholarPubMed
Qureshi, ST and Medzhitov, R (2003). Toll-like receptors and their role in experimental models of microbial infection. Genes and Immunity 4: 87–94.CrossRefGoogle ScholarPubMed
Rakoff-Nahoum, S, Paglino, J, Eslami-Varzaneh, F, Edberg, S and Medzhitov, R (2004). Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118: 229–241.CrossRefGoogle ScholarPubMed
Rantala, M (1974). Nitrovin and tetracycline: a comparison of their effect on salmonellosis in chicks. British Poultry Science 15: 299–303.CrossRefGoogle ScholarPubMed
Rantala, M and Nurmi, E (1974). Hazards involved in the use of furazolidone for the prevention of salmonellosis in broiler chickens. Journal of Hygiene, Cambridge 72: 349–354.CrossRefGoogle ScholarPubMed
Reilly, KJ, Frankel, WL, Bain, AM and Rombeau, JL (1995). Colonic short chain fatty acids mediate jejunal growth by increasing gastrin. Gut 37: 81–86.CrossRefGoogle ScholarPubMed
Roediger, W (1980a). Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man. Gut 21: 793–798.CrossRefGoogle ScholarPubMed
Roediger, WE (1980b). The colonic epithelium in ulcerative colitis: an energy-deficiency disease? Lancet 2: 712–715.CrossRefGoogle ScholarPubMed
Roediger, W (1995). The place of short-chain fatty acids in colonocyte metabolism in health and ulcerative colitis: the impaired colonocyte barrier. In: Cummings, JH, Rombeau, JL and Sakata, T (editors). Physiological and Clinical Aspects of Short-chain Fatty Acids. Cambridge, UK: Cambridge University Press, pp. 337–387.Google Scholar
Ruebsamen, K and Engelhardt, WV (1978). Bicarbonate secretion and solute absorption in fore stomach of the llama. American Journal of Physiology 235: 1–6.Google Scholar
Ruppin, H, Bar-Meir, S, Soergel, KH, Wood, CM and Schimitt, MG (1980). Absorption of short-chain fatty acids by the colon. Gastroenterology 78: 1500–1507.CrossRefGoogle ScholarPubMed
Sakata, T and Setoyama, H (1995). Local stimulatory effect of short-chain fatty acids on the mucus release from the hindgut mucosa of rats (Rattus norvegicus). Comparative Biochemistry and Physiology A: Comparative Physiology 111: 429–432.CrossRefGoogle ScholarPubMed
Samanya, M and Yamauchi, KE (2002). Histological alterations of intestinal villi in chickens fed dried Bacillus subtilis var. natto. Comparative Biochemistry and Physiology A: Molecular and Integrative Physiology 133: 95–104.CrossRefGoogle ScholarPubMed
Sanderson, IR (2004). Short chain fatty acid regulation of signaling genes expressed by the intestinal epithelium. Journal of Nutrition 134: 2450–2454.CrossRefGoogle ScholarPubMed
Savage, DC, Siegel, JE, Snellen, JE and Whitt, DD (1981). Transit time of epithelial cells in the small intestines of germfree mice and ex-germfree mice associated with indigenous microorganisms. Applied Environmental Microbiology 42: 996–1001.CrossRefGoogle ScholarPubMed
Scanlan, CM (1997). Current concepts of competitive exclusion cultures for the control of salmonellae in domestic poultry. Advances in Experimental Medicine and Biology 412: 421–426.CrossRefGoogle ScholarPubMed
Schmit, MG, Soergel, KH and Wood, CM (1976). Absorption of short chain fatty acids from the human jejunum. Gastroenterology 70: 211–215.CrossRefGoogle Scholar
Schmit, MG, Soergel, KH and Wood, CM (1977). Absorption of short chain fatty acids from the human ileum. American Journal of Digestive Diseases 22: 340–347.CrossRefGoogle Scholar
Schneitz, C, Nuotio, L, Kiiskinen, T and Nurmi, E (1991). Pilot-scale testing of the competitive exclusion method in chickens. British Poultry Science 32: 881–884.CrossRefGoogle ScholarPubMed
Schneitz, C and Nuotio, L (1992). Efficacy of different microbial preparations for controlling Salmonella colonisation in chicks and turkey poults by competitive exclusion. British Poultry Science 33: 207–211.CrossRefGoogle ScholarPubMed
Schultz, M, Munro, K, Tannock, GW, Melchner, I, Gottl, C, Schwietz, H, Scholmerich, J and Rath, HC (2004). Effects of feeding a probiotic preparation (SIM) containing insulin on the severity of colitis and on the composition of the intestinal microflora in HLA-B27 transgenic rats. Clinical and Diagnostic Laboratory Immunology 11: 581–587.Google Scholar
Seo, KH, Holt, PS, Gast, RK and Hofacre, CL (2000). Combined effect of antibiotic and competitive exclusion treatment on Salmonella enteritidis fecal shedding in molted laying hens. Journal of Food Protection 63: 648–656.CrossRefGoogle ScholarPubMed
Seuna, E, Schneitz, C, Nurmi, E and Makela, PH (1980). Combined therapy of Salmonella infection in chickens by antimicrobial agents followed by cultured cecal bacteria. Poultry Science 59: 1187–1192.CrossRefGoogle ScholarPubMed
Shimotoyodome, A, Meguro, S, Hase, T, Tokimitsu, I and Sakata, T (2000). Short chain fatty acids but not lactate or succinate stimulate mucus release in the rat colon. Comparative Biochemistry and Physiology A: Molecular and Integrative Physiology 125: 525–531.CrossRefGoogle ScholarPubMed
Shin, S, Castanie-Cornet, MP, Foster, JW, Crawford, JA, Brinkley, C and Kaper, JB (2001). An activator of glutamate decarboxylase genes regulates the expression of enteropathogenic Escherichia coli virulence genes through control of the plasmid-encoded regulator. Perspectives in Molecular Microbiology 41: 1133–1150.CrossRefGoogle ScholarPubMed
Smith, SI, Aweh, AJ, Coker, AO, Savage, KO, Abosede, DA and Oyedeji, KS (2001). Lactobacilli in human dental caries and saliva. Microbios 105: 77–85.Google ScholarPubMed
Snoeyenbos, GH, Weinack, OM and Smyser, CF (1979). Further studies on competitive exclusion for controlling Salmonellae in chickens. Avian Diseases 24: 904–914.CrossRefGoogle Scholar
Soerjadi, AS, Stehman, SM, Snoeyenbos, GH, Weinack, OM and Smyser, CF (1981). Some measurements of protection against pareatyphoid Salmonella and Escherichia coli by competitive exclusion in chickens. Avian Diseases 25: 706–712.CrossRefGoogle ScholarPubMed
Soerjadi, AS, Rufner, R, Snoeyenbos, GH and Weinack, OM (1982). Adherence of salmonellae and native gut microflora to the gastrointestinal mucosa of chicks. Avian Diseases 26: 520–524.CrossRefGoogle Scholar
Sonnenburg, JL, Angenent, LT and Gordon, JI (2004). Getting a grip on things: how do communities of bacterial symbionts become established in our intestine? Nature Immunology 5: 569–573.CrossRefGoogle ScholarPubMed
Souza, DG, Vieira, AT, Soares, AC, Pinho, V, Nicoli, JR, Vieira, LQ and Teixeira, MM (2004). The essential role of the intestinal microbiota in facilitating acute inflammatory responses. Journal of Immunology 173: 4137–4146.CrossRefGoogle ScholarPubMed
Stavric, S, Gleeson, TM, Blanchfield, B and Pivnick, H (1987). Role of adhering microflora in competitive exclusion of Salmonella from young chickens. Journal of Food Protection 50: 928–932.CrossRefGoogle Scholar
Stern, NJ (1994). Mucosal competitive exclusion to diminish colonization of chickens by Campylobacter jejuni. Poultry Science 73: 402–407.CrossRefGoogle ScholarPubMed
Stiver, HG, Forward, KR, Tyrrell, DL, Krip, G, Livingstone, RA, Fugere, P, Lemay, M, Verschelden, G, Hunter, JD and Carson, GD (1984). Comparative cervical microflora shifts after cefoxitin or cefazolin prophylaxis against infection following cesarean section. American Journal of Obstetrics and Gynecology 149: 718–721.CrossRefGoogle ScholarPubMed
Suau, A, Bonnet, R, Sutren, M, Godon, JJ, Gibson, GR, Collins, MD and Dore, J (1999). Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Applied Environmental Microbiology 65: 4799–4807.CrossRefGoogle ScholarPubMed
Sudo, N, Sawamura, S, Tanaka, K, Aiba, Y, Kubo, C and Koga, Y (1997). The requirement of intestinal bacterial flora for the development of an IgE production system fully susceptible to oral tolerance induction. Journal of Immunology 159: 1739–1745.CrossRefGoogle ScholarPubMed
Sutas, Y, Hurme, M and Isolauri, E (1996). Down-regulation of anti-CD3 antibody-induced IL-4 production by bovine caseins hydrolysed with Lactobacillus GG-derived enzymes. Scandinavian Journal of Immunology 43: 687–689.CrossRefGoogle ScholarPubMed
Tagg, JR, Dajani, AS and Wannamaker, LW (1975). Bacteriocin of a group B Streptococcus: partial purification and characterization. Antimicrobials Agents and Chemotherapy 7: 764–772.CrossRefGoogle ScholarPubMed
Tamas, LC, Hoekstra, RF and Pagie, L (2002). Chemical warfare between microbes promotes biodiversity. Proceedings of the National Academy of Sciences of USA 99: 786–790.Google Scholar
Tannock, GW, Fuller, R, Smith, SL and Hall, MA (1990). Plasmid profiling of members of the family Enterobacteriaceae, lactobacilli and bifidobacteria to study the transmission of bacteria from mother to infant. Journal of Clinical Microbiology 28: 1225–1228.CrossRefGoogle Scholar
Tasman-Jones, C, Maher, C, Thomsen, L, Lee, SP and Vanderwee, M (1987). Mucosal defences and gastroduodenal disease. Digestion 37: 1–7.CrossRefGoogle ScholarPubMed
Thompson, JS, Quigley, EM and Adrian, TE (1998). Qualitative changes in enteric flora and short-chain fatty acids after intestinal resection. Digestive Diseases and Sciences 43: 624–631.CrossRefGoogle ScholarPubMed
Tucker, DL, Tucker, N, Ma, Z, Foster, JW, Miranda, RL, Cohen, PS and Conway, T (2003). Genes of the GadX-GadW regulon in Escherichia coli. Journal of Bacteriology 185: 3190–3201.CrossRefGoogle ScholarPubMed
van Leeuwen, P, Mouwen, JM, van der Klis, JD and Verstegen, MW (2004). Morphology of the small intestinal mucosal surface of broilers in relation to age, diet formulation, small intestinal microflora and performance. British Poultry Science 45: 41–48.CrossRefGoogle ScholarPubMed
Vinderola, CG, Medici, M and Perdigon, G (2004). Relationship between interaction sites in the gut, hydrophobicity, mucosal immunomodulating capacities and cell wall protein profiles in indigenous and exogenous bacteria. Journal of Applied Microbiology 96: 230–243.CrossRefGoogle ScholarPubMed
Walker, WA (1975). Antigen absorption from the small intestine and gastrointestinal disease. Pediatric Clinics of North America 22: 731–746.CrossRefGoogle ScholarPubMed
Walker, WA (1979). Gastrointestinal host defence: importance of gut closure in control of macromolecular transport. Ciba Foundation Symposium 16: 201–219.Google Scholar
Wierup, M, Wold-Troell, M, Nurmi, E and Hakkinen, M (1988). Epidemiological evaluation of the Salmonella -controlling effect of a nationwide use of a competitive exclusion culture in poultry. Poultry Science 67: 1026–1033.CrossRefGoogle ScholarPubMed
Wilson, KH and Freter, R (1986). Interaction of Clostridium difficile and Escherichia coli with microfloras in continuous-flow cultures and gnotobiotic mice. Infection and Immunity 54: 354–358.CrossRefGoogle ScholarPubMed
Windmueller, HG and Spaeth, AE (1978). Identification of ketone bodies and glutamine as the major respiratory fuels in vivo for postaborptive rat small intestine. Journal of Biological Chemistry 253: 69–79.CrossRefGoogle Scholar
World Health Organization (1994). Report of the WHO-FEDESA-FEP Workshop on Competitive Exclusion, Vaccination and Antimicrobials in Salmonella Control in Poultry, WHO/CDS/VPS/94.134. Geneva: World Health Organization.Google Scholar
Yajima, T (1985). Contractile effect of short-chain fatty acids on the isolated colon of the rat. Journal of Physiology 368: 667–678.CrossRefGoogle ScholarPubMed
Yang, MG, Manoharan, K and Mickelsen, O (1970). Nutritional contribution of volatile fatty acids from the cecum of rats. Journal of Nutrition 100: 545–550.CrossRefGoogle ScholarPubMed
Young, SL, Simon, MA, Baird, MA, Tannock, GW, Bibiloni, R, Spencely, K, Lane, JM, Fitzharris, P, Crane, J, Town, I, Addo-Yobo, E, Murray, CS and Woodcock, A (2004). Bifidobacterial species differentially affect expression of cell surface markers and cytokines of dendritic cells harvested from cord blood. Clinical and Diagnostic Laboratory Immunology 11: 686–690.Google ScholarPubMed
Zhu, XY, Zhong, T, Pandya, Y and Joerger, RD (2002). 16S rRNA-based analysis of microbiota from the cecum of broiler chickens. Applied Environmental Microbiology 68: 124–137.CrossRefGoogle ScholarPubMed
Ziprin, RL, Corrier, DE, Hinton, A Jr, Beier, RC, Spates, GE, DeLoach, JR and Elissalde, MH (1990). Intracloacal Salmonella typhimurium infection of broiler chickens: reduction of colonization with anaerobic organisms and dietary lactose. Avian Diseases 34: 749–753.CrossRefGoogle ScholarPubMed
Ziprin, RL, Corrier, DE and DeLoach, JR (1993). Control of established Salmonella typhimurium intestinal colonization with in vivo-passaged anaerobes. Avian Diseases 37: 183–188.CrossRefGoogle ScholarPubMed