In vitro fermentation of carbohydrates by porcine faecal inocula and their influence on Salmonella Typhimurium growth in batch culture systems

FEMS Microbiology Ecology

Volumn 66, Issue 3, 2008, Pages 608-619

  Martín Peláez, Sandra ^b   Gibson, Glenn R ^a   Martín Orúe, Susana M ^b   Klinder, Annett ^a   Rastall, Robert A ^a   La Ragione, Roberto M ^c   Woodward, Martin J ^c   Costabile, Adele ^a  

^a UNIVERSITY OF READING   (United Kingdom)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^c VETERINARY LABORATORIES AGENCY   (United Kingdom)

Author keywords

Batch cultures; FISH; Nondigestible carbohydrates; Pigs; Salmonella Typhimurium; Short chain fatty acids

Indexed keywords

FRUCTOSE OLIGOSACCHARIDE; GENTIOOLIGOSACCHARIDE; INULIN; LACTIC ACID; LACTULOSE; OLIGOSACCHARIDE; SHORT CHAIN FATTY ACID; UNCLASSIFIED DRUG; XYLOOLIGOSACCHARIDE;

BACTERIUM; CARBOHYDRATE; FECES; FERMENTATION; GROWTH RESPONSE; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; QUANTITATIVE ANALYSIS; SURVIVAL;

ARTICLE; BACTERIAL COUNT; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIUM; BACTERIUM CULTURE; BATCH FERMENTATION; BIFIDOBACTERIUM; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; FECES CULTURE; FLUORESCENCE IN SITU HYBRIDIZATION; IN VITRO STUDY; LACTOBACILLUS; LEUCONOSTOC; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SALMONELLA; SALMONELLA TYPHIMURIUM; SWINE; WEISSELLA;

ANIMALS; BACTERIA; BIFIDOBACTERIUM; CARBOHYDRATE METABOLISM; FECES; FERMENTATION; LACTOBACILLUS; OLIGOSACCHARIDES; SALMONELLA TYPHIMURIUM; SWINE;

BACTERIA (MICROORGANISMS); BIFIDOBACTERIUM; LACTOBACILLUS; LEUCONOSTOC; SALMONELLA; SALMONELLA TYPHIMURIUM; SUIDAE; SUS; WEISSELLA;

EID: 55949129345     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/j.1574-6941.2008.00610.x     Document Type: Article

References (61)

1. Alm EW, Oerther DB, Larsen N, Stahl DA Raskin L (1996) The oligonucleotide probe database. Appl Environ Microb 62 : 3557 3559.
2. Apanavicius CJ, Powell KL, Vester BM, Karr-Lilienthal LK, Pope LL, Fastinger ND, Wallig MA, Tappenden KA Swanson KS (2007) Fructan supplementation and infection affect food intake, fever, and epithelial sloughing from Salmonella challenge in weanling puppies. J Nutr 137 : 1923 1930.
3. Bailey JS, Blankenship LC Cox NA (1991) Effect of fructooligosaccharide on Salmonella colonization of the chicken intestine. Poultry Sci 70 : 2433 2438.
4. Bauer E, Williams BA, Bosch MW, Voigt C, Mosenthin R Verstegen MWA (2004) Differences in microbial activity of digesta from three sections of the porcine large intestine according to in vitro fermentation of carbohydrate-rich substrates. J Sci Food Agr 84 : 2097 2104.
5. Böhmer BM, Branner GR Roth-Maier DA (2005) Precaecal and faecal digestibility of inulin (DP 10-12) or an inulin/Enterococcus faecium mix and effects on nutrient digestibility and microbial gut flora. J Anim Physiol An N (Berlin) 89 : 388 396.
6. Bohnhoff M, Miller CP Martin WR (1964) Resistance of the mouse's intestinal tract to experimental Salmonella infection: II. Factors responsible for its loss following streptomycin treatment. J Exp Med 120 : 817 828.
7. Burkey TE, Dritz SS, Nietfeld JC, Johnson BJ Minton JE (2004) Effect of dietary mannanoligosaccharide and sodium chlorate on the growth performance, acute-phase response, and bacterial shedding of weaned pigs challenged with Salmonella enterica serotype Typhimurium. J Anim Sci 82 : 397 404.
8. Casey PG, Gardiner GE, Casey G et al 2007) A five-strain probiotic combination reduces pathogen shedding and alleviates disease signs in pigs challenged with Salmonella enterica serovar Typhimurium. Appl Environ Microb 73 : 1858 1863.
9. Chiu HH, Tsai CC, Hsih HY Tsen HY (2008) Screening from pickled vegetables the potential probiotic strains of lactic acid bacteria able to inhibit the Salmonella invasion in mice. J Appl Microb 104 : 605 612.
10. Clemens ET Stevens CE (1974) Digesta flow and organic-acid production in gastrointestinal-tract of pig. Gastroenterology 66 : 677 677.
11. Coates ME, Drasar BS, Mallett AK Rowland IR (1988) Methodological considerations for the study of bacterial metabolism. Role of Gut Flora in Toxicity and Cancer (Rowland IR, ed), pp. 1 21. Academic Press, London.
12. Coles LT, Moughan PJ Darraugh AJ (2005) In vitro digestion and fermentation methods, including gas production techniques, as applied to nutritive evaluation of foods in the hindgut of humans and other simple-stomached animals. Anim Feed Sci Technol 123-124 : 421 444.
13. Collins MD Gibson GR (1999) Probiotics, prebiotics, and synbiotics: approaches for modulating the microbial ecology of the gut. Am J Clin Nutr 69 : 1052S 1057S.
14. Correa-Matos NJ, Donovan SM, Isaacson RE, Gaskins HR, White BA Tappenden KA (2003) Fermentable fiber reduces recovery time and improves intestinal function in piglets following Salmonella Typhimurium infection. J Nutr 133 : 1845 1852.
15. Daims H, Stoecker K Wagner M (2005) Fluorescence in situ hybridization for the detection of prokaryotes. Advanced Methods in Molecular Microbial Ecology (Osborn AM Smith CJ, eds), pp. 213 239. Bios-Garland, Abingdon, UK.
16. de Jong B Ekdahl K (2006) The comparative burden of salmonellosis in the European Union member states, associated and candidate countries. BMC Public Health 10 : 6 4.
17. De Vuyst L Leroy F (2007) Bacteriocins from lactic acid bacteria: production, purification, and food applications. J Mol Microb Biotech 13 : 194 199.
18. Durant JA, Corrier DE Ricke SC (2000) Short-chain volatile fatty acids modulate the expression of the hilA and invF genes of Salmonella Typhimurium. J Food Protect 63 : 573 578.
19. Ewing WN Cole DJA (1994) The Living Gut. An Introduction to Microorganisms in Nutrition. Context Publications, Ireland.
20. Fayol-Messaoudi D, Berger CN, Coconnier-Polter MH, Liévin-Le Moal V Servin AL (2005) pH-, lactic acid-, and non-lactic acid-dependent activities of probiotic Lactobacilli against Salmonella enterica serovar Typhimurium. Appl Environ Microb 71 : 6008 6013.
21. Franks AH, Harmsen HJ, Raangs GC, Jansen GJ, Schut F Welling GW (1998) Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Appl Environ Microb 64 : 3336 3345.
22. Fuller R (1977) The importance of lactobacilli in maintaining normal microbial balance in the crop. Poultry Sci 18 : 85 94.
23. Gantois I, Ducatelle R, Pasmans F, Haesebrouck F, Hautefort I, Thompson A, Hinton JC Van Immerseel F (2006) Butyrate specifically down-regulates Salmonella pathogenicity island 1 gene expression. Appl Environ Microb 72 : 946 949.
24. Gibson GR Roberfroid MB (1995) Dietary modulation of the colonic microbiota: introducing the concept of prebiotics. J Nutr 125 : 1401 1412.
25. Gibson GR, Ottaway PB Rastall RA (2000) Prebiotics: New Developments in Functional Foods. Chandos Publishing Oxford, Oxford, UK.
26. Hansen CF (2004) Choice of dry feed influences gastric conditions, incidence of Salmonella and performance in growing - finishing pigs. PhD Thesis. The Royal Veterinary and Agricultural University, Denmark.
27. Haraga A, Ohlson MB Miller SI (2008) Salmonellae interplay with host cells. Nat Rev Microbiol 6 : 53 66.
28. Harmsen HJ, Raangs GC, He T, Degener JE Welling GW (2002) Extensive set of 16S rRNA-based probes for detection of bacteria in human feces. Appl Environ Microb 68 : 2982 2990.
29. Harmsen HJM, Elfferich P, Schut F Welling GW (1999) A 16S rRNA-targeted probe for detection of lactobacilli and enterococci in fecal samples by fluorescent in situ hybridization. Microbiol Ecol Health Dis 11 : 3 12.
30. Harmsen HJM, Wildeboer-Veloo ACM, Grijpstra J, Knol J, Degener JE Welling GW (2000) Development of 16S rRNA-based probes for the Coriobacterium group and the Atopobium cluster and their application for enumeration of Coriobacteriaceae in human feces from volunteers of different age groups. Appl Environ Microbiol 66 : 4523 4527.
31. Horswill AR Escalante-Semerena JC (1999) Salmonella Typhimurium LT2 catabolizes propionate via the 2-methylcitric acid cycle. J Bacteriol 181 : 5615 5623.
32. Hudault S, Liévin V, Bernet-Camard MF Servin AL (1997) Antagonistic activity exerted in vitro and in vivo by Lactobacillus casei (strain GG) against Salmonella Typhimurium C5 infection. Appl Environ Microb 63 : 513 518.
33. Kamphues J, Papenbrock S, Brüning I, Amtsberg G Verspohl J (2005) Effects of grinding intensity combined with potassium diformate (KDF) as feed additive in reared piglets experimentally infected with Salmonella Derby. Proc Nutr Soc Nutr Phys 14 : 68.
34. Kaplan H Hutkins RW (2000) Fermentation of fructoligosaccharides by lactic acid bacteria and bifidobacteria. Appl Environ Microb 66 : 2682 2684.
35. Krueger M, Schroedl W, Isik W, Lange W Hagemann L (2002) Effects of lactulose on the intestinal microflora of periparturient sows and their piglets. Eur J Nutr 41 (suppl 1) : I26 I31.
36. Langendijk PS, Schut F, Jansen GJ, Raangs GC, Kamphuis GR, Wilkinson MH Welling GW (1995) Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in fecal samples. Appl Environ Microb 61 : 3069 3075.
37. Lawhon SD, Maurer R, Suyemoto M Altier C (2002) Intestinal short-chain fatty acids alter Salmonella Typhimurium invasion gene expression and virulence through BarA/SirA. Mol Microbiol 46 : 1451 1464.
38. Letellier A, Messier S, Pare J, Menard J Quessy S (1999) Distribution of Salmonella in swine herds in Québec. Vet Microbiol 67 : 299 306.
39. Liao W, Cui XS, Jin XY Floren CH (1994) Lactulose - a potential drug for the treatment of inflammatory bowel disease. Med Hypotheses 43 : 234 238.
40. Loh G, Eberhard M, Brunner RM, Hennig U, Kuhla S, Kleessen B Metges CC (2006) Inulin alters the intestinal microbiota and short-chain fatty acid concentrations in growing pigs regardless of their basal diet. J Nutr 136 : 1198 1202.
41. Manz W, Amann R, Ludwig W, Vancanneyt M Schleifer KH (1996) Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum Cytophaga-Flavobacter-Bacteroides in the natural environment. Microbiology 142 : 1097 1106.
42. McHan F Shotts EB (1993) Effect of short-chain fatty acids on the growth of Salmonella Typhimurium in an in vitro system. Avian Dis 37 : 396 398.
43. Meynell GG (1963) Antibacterial mechanisms o the mouse gut: II. The role of EH and volatile fatty acids in the normal gut. Brit J Exp Pathol 44 : 209 219.
44. Mountzouris KC, Balaskas C, Fava F, Tuohy KM, Gibson GR Fegeros K (2006) Profiling of composition and metabolic activities of the colonic microflora of growing pigs fed diets supplemented with prebiotic oligosaccharides. Anaerobe 12 : 178 185.
45. Nordentoft S, Christensen H Wegener HC (1997) Evaluation of a fluorescence-labelled oligonucleotide probe targeting 23S rRNA for in situ detection of Salmonella serovars in paraffin-embedded tissue sections and their rapid identification in bacterial smears. J Clin Microbiol 35 : 2642 2648.
46. Oli MW, Petschow BW Buddington RK (1998) Evaluation of fructooligosaccharide supplementation of oral electrolyte solutions for treatment of diarrhea: recovery of the intestinal bacteria. Digest Dis Sci 43 : 138 147.
47. Oyarzabal OA Conner DE (1995) In vitro fructooligosaccharide utilization and inhibition of Salmonella spp. by selected bacteria. Poultry Sci 74 : 1418 1425.
48. Postma PW, Keizer HG Koolwijk P (1986) Transport of trehalose in Salmonella Typhimurium. J Bacteriol 168 : 1107 1111.
49. Prohászka L, Jayarao BM, Fábián A Kovács S (1990) The role of intestinal volatile fatty acids in the Salmonella shedding of pigs. Zentralb Vet Riehe B 37 : 570 574.
50. Roberts JA, Cumberland P, Sockett PN, Wheeler J, Rodrigues LC, Sethi D Roderick PJ (2003) Infectious Intestinal Disease Study Executive. The study of infectious intestinal disease in England: socio-economic impact. Epidemiol Infect 130 : 1 11.
51. Sakai K, Aramaki K, Takasaki M, Inaba H, Tokunaga T Ohta A (2001) Effect of dietary short-chain fructooligosaccharides on the cecal microflora in gastrectomized rats. Biosci Biotechnol Bioch 65 : 264 269.
52. Shim SB, Verstegen MW, Kim IH, Kwon OS Verdonk JM (2005) Effects of feeding antibiotic-free creep feed supplemented with oligofructose, probiotics or synbiotics to suckling piglets increases the preweaning weight gain and composition of intestinal microbiota. Arch Anim Nutr 59 : 419 427.
53. Silva AM, Bambirra EA, Oliveira AL, Souza PP, Gomes DA, Vieira EC Nicoli JR (1999) Protective effect of bifidus milk on the experimental infection with Salmonella enteritidis subsp. Typhimurium in conventional and gnotobiotic mice. J Appl Microbiol 86 : 331 336.
54. Smith HW Jones JE (1963) Observations on the alimentary tract and its bacterial flora in healthy and diseased pigs. J Pathol Bacteriol 86 : 387 412.
55. Sockett PN Roberts JA (1991) The social and economic impact of salmonellosis. A report of a national survey in England and Wales of laboratory-confirmed Salmonella infections. Epidemiol Infect 107 : 335 347.
56. Tako E, Glahn RP, Welch RM, Lei X, Yasuda K Miller DD (2008) Dietary inulin affects the expression of intestinal enterocyte iron transporters, receptors and storage protein and alters the microbiota in the pig intestine. Brit J Nutr 99 : 472 480.
57. Tzortzis G, Goulas AK, Gee JM Gibson GR (2005) A novel galactooligosaccharide mixture increases the bifidobacterial population numbers in a continuous in vitro fermentation system and in the proximal colonic contents of pigs in vivo. J Nutr 135 : 1726 1731.
58. Van Immerseel F, De Buck J, Pasmans F, Velge P, Bottreau E, Fievez V, Haesebrouck F Ducatelle R (2003) Invasion of Salmonella enteritidis in avian intestinal epithelial cells in vitro is influenced by short-chain fatty acids. Int J Food Microbiol 85 : 237 248.
59. Van Loo J (2007) How chicory Fructans contribute to zootechnical performance and well-being in livestock and companion animals. J Nutr 137 : 2594S.
60. Walker AW, Duncan SH, Leitch ECM, Child MW Flint HJ (2005) pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon. Appl Environ Microb 71 : 3692 3700.
61. Williams BA, Voigt C Verstegen M (1998) The faecal microbial population can be representative of large intestinal microfloral activity. Proceedings of the British Society of Animal Science, p. 165.