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Digestive Diseases and Sciences

, Volume 54, Issue 5, pp 947–954 | Cite as

Comparative Effects of a High-Amylose Starch and a Fructooligosaccharide on Fecal Bifidobacteria Numbers and Short-Chain Fatty Acids in Pigs Fed Bifidobacterium animalis

  • Anthony R. Bird
  • Michelle Vuaran
  • Ross Crittenden
  • Takashi Hayakawa
  • Martin J. Playne
  • Ian L. Brown
  • David L. ToppingEmail author
Original Article

Abstract

Pigs were fed a freeze-dried probiotic (Bifidobacterium animalis CSCC 1941) plus a high-amylose maize starch (HAMS) and a fructooligosaccharide (FOS) separately or together. Fecal output and total and individual major short-chain fatty acid (SCFA) concentrations and excretion were higher and pH was lower with HAMS than with FOS relative to when they were fed a low-amylose maize starch (LAMS; control). Fecal bifidobacteria numbers and total excretion were equally higher during feeding of FOS or HAMS and highest with HAMS + FOS. When probiotic supplementation was stopped, bifidobacteria numbers declined rapidly when they were fed LAMS, more slowly with FOS or HAMS, and were maintained with HAMS + FOS. The data confirm that both HAMS and FOS are prebiotics and suggest that they act through different mechanisms and that they are most effective in combination. However only HAMS raises fecal SCFA.

Keywords

Fructooligosaccharides Pigs Prebiotics Probiotics Starch 

Abbreviations

FOS

Fructooligosaccharides

LAB

Lactic acid bacteria

NSP

Nonstarch polysaccharides (“fibre”)

OS

Oligosaccharides

RS

Resistant starch

SCFA

Short-chain fatty acids

Notes

Acknowledgment

We wish to thank Ms D. Davies and M. McManus for excellent technical assistance and care of the animals and Ms A. Reid for statistical analyses. Financial support was received from the Co-operative Research Centre for Food Industry Innovation.

References

  1. 1.
    Cummings JH, Macfarlane GT. The control and consequences of bacterial fermentation in the human large intestine. J Appl Bacteriol. 1991;70:443–459.PubMedGoogle Scholar
  2. 2.
    Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr. 1995;125:1401–1412.PubMedGoogle Scholar
  3. 3.
    Topping DL, Clifton PM. Short chain fatty acids and human colonic function—relative roles of resistant starch and non-starch polysaccharides. Physiol Rev. 2001;81:1031–1064.PubMedGoogle Scholar
  4. 4.
    Brouns F, Kettlitz B, Arrigoni E. Resistant starch and “the butyrate revolution”. Trends Food Sci Technol. 2002;13:251–261. doi: 10.1016/S0924-2244(02)00131-0.CrossRefGoogle Scholar
  5. 5.
    Weaver GA, Krause JA, Miller TL, Wolin MJ. Cornstarch fermentation by the colonic microbial community yields more butyrate than does cabbage fermentation; cornstarch fermentation rates correlate negatively with methanogenesis. Am J Clin Nutr. 1992;47:61–66.Google Scholar
  6. 6.
    van Munster IP, Tangerman A, Nagengast FM. Effect of resistant starch on colonic fermentation, bile acid metabolism, and mucosal proliferation. Dig Dis Sci. 1994;39:834–842. doi: 10.1007/BF02087431.PubMedCrossRefGoogle Scholar
  7. 7.
    Noakes M, Clifton P, Nestel PJ, Le Leu R, McIntosh GH. Effect of high amylose starch and oat bran on metabolic variables and bowel function in subjects with hypertriglyceridemia. Am J Clin Nutr. 1996;64:944–951.PubMedGoogle Scholar
  8. 8.
    Brown IL, Warhurst M, Arcot J, Playne MJ, Illman RJ, Topping DL. Fecal numbers of bifidobacteria are higher in pigs fed bifidobacterium longum with a high amylose (amylomaize) starch than with a low amylose starch. J Nutr. 1997;127:1822–1827.PubMedGoogle Scholar
  9. 9.
    Martinez-Puig D, Pérez JF, Castillo M, et al. Consumption of raw potato starch increases colon length and fecal excretion of purine bases in growing pigs. J Nutr. 2003;133:134–139.PubMedGoogle Scholar
  10. 10.
    Cummings JH, Beatty ER, Kingman SM, Bingham SA, Englyst HN. Digestion and physical properties of resistant starch in the human large bowel. Br J Nutr. 1996;75:733–747. doi: 10.1079/BJN19960177.PubMedCrossRefGoogle Scholar
  11. 11.
    Bird AR, Brown IL, Topping DL. Starches, resistant starches, the gut microflora and human health. Curr Issues Intest Microbiol. 2000;1:25–37.PubMedGoogle Scholar
  12. 12.
    Bartram HP, Scheppach W, Gerlach S, Ruckdeschel G, Kelber E, Kaspar H. Does yoghurt enriched with Bifidobacterium longum affect colonic microbiology and fecal metabolites in healthy humans? Am J Clin Nutr. 1994;59:428–432.PubMedGoogle Scholar
  13. 13.
    Macfarlane S, Macfarlane GT, Cummings JH. Prebiotics in the gastrointestinal tract. Aliment Pharmacol Ther. 2006;24:701–714. doi: 10.1111/j.1365-2036.2006.03042.x.PubMedCrossRefGoogle Scholar
  14. 14.
    Flickinger EA, van Loo J, Fahey GC Jr. Nutritional responses to the presence of inulin and oligofructose in the diets of domesticated animals. Crit Rev Food Sci Nutr. 2003;43:19–60. doi: 10.1080/10408690390826446.PubMedCrossRefGoogle Scholar
  15. 15.
    Kleessen B, Schwarz S, Boehm A, et al. Jerusalem artichoke and chicory inulin in bakery products affects faecal microbioita in human volunteers. Br J Nutr. 2007;98:540–549.PubMedCrossRefGoogle Scholar
  16. 16.
    Ten Bruggencate SJ, Bovee-Oudenhoven IM, Lettink-Wissink ML, van der Meer R. Dietary fructooligosaccharides increase intestinal permeability in rats. J Nutr. 2005;135:837–842.PubMedGoogle Scholar
  17. 17.
    Ten Bruggencate SJ, Bovee-Oudenhoven IM, Lettink-Wissink ML, Katan MB, van der Meer R. Dietary fructooligosaccharides affect intestinal barrier function in healthy men. J Nutr. 2006;136:70–74.PubMedGoogle Scholar
  18. 18.
    Wang X, Brown IL, Evans AJ, Conway PL. The protective effects of high amylose maize (amylomaize) starch granules on the survival of Bifidobacterium spp. in the mouse intestinal tract. J Appl Microbiol. 1999;87:631–639. doi: 10.1046/j.1365-2672.1999.00836.x.PubMedCrossRefGoogle Scholar
  19. 19.
    Morita T, Kasaoka S, Kiriyama S, Brown IL, Topping DL. Comparative effects of acetylated and unmodified high amylose maize starch in rats. Starch/Stärke. 2005;57:246–253.CrossRefGoogle Scholar
  20. 20.
    Knutson CS. A simplified colorimetric procedure for determination of amylose in maize starches. Cereal Chem. 1986;63:89–93.Google Scholar
  21. 21.
    Pachenari A, Conway PL, Playne MJ. Bifidus-blood agar-a differentiating medium for the isolation and enumeration of bifidobacteria from faecal samples. Biosci Microflora. 2001;20:85–88.Google Scholar
  22. 22.
    Campbell JM, Fahey GC Jr, Wolf BW. Selected indigestible oligosaccharides affect large bowel mass, cecal and fecal short-chain fatty acids, pH and microflora in rats. J Nutr. 1997;127:130–136.PubMedGoogle Scholar
  23. 23.
    Djouzi Z, Andrieux C. Compared effects of three oligosaccharides on metabolism of intestinal microflora in rats inoculated with a human faecal flora. Br J Nutr. 1997;8:313–324. doi: 10.1079/BJN19970149.CrossRefGoogle Scholar
  24. 24.
    Bouhnik Y, Vahedi K, Achour L, et al. Short-chain fructo-oligosaccharide administration dose-dependently increases fecal bifidobacteria in healthy humans. J Nutr. 1999;(129):113–116.Google Scholar
  25. 25.
    Silvi S, Rumney CJ, Cresci A, Rowland IR. Resistant starch modifies gut microflora and microbial metabolism in human flora-associated rats inoculated with faeces from Italian and UK donors. J Appl Microbiol. 1999;86:521–530. doi: 10.1046/j.1365-2672.1999.00696.x.PubMedCrossRefGoogle Scholar
  26. 26.
    Sghir A, Chow JM, Mackie RI. Continuous culture selection of bifidobacteria and lactobacilli from human faecal samples using fructooligosaccharide as selective substrate. J Appl Microbiol. 1998;85:769–7. doi: 10.1111/j.1365-2672.1998.00590.x.PubMedCrossRefGoogle Scholar
  27. 27.
    Wang X, Conway PL, Brown IL, Evans AJ. In vitro utilization of amylopectin and high-amylose maize (Amylomaize) starch granules by human colonic bacteria. Appl Environ Microbiol. 1999;65:4848–4854.PubMedGoogle Scholar
  28. 28.
    Bird AR, Hayakawa T, Marsono Y, et al. Coarse brown rice increases fecal and large bowel short-chain fatty acids and starch but lowers calcium in the large bowel of pigs. J Nutr. 2000;130:1780–1787.PubMedGoogle Scholar
  29. 29.
    Brown IL, Wang X, Topping DL, Playne MJ, Conway PL. High amylose maize starch as a versatile prebiotic for use with probiotic bacteria. Food Aust. 1998;50:603–610.Google Scholar
  30. 30.
    Brown IL, Mcnaught KJ, Moloney E. Hi-maize TM: new directions in starch technology and nutrition. Food Aust. 1995;47:272–275.Google Scholar
  31. 31.
    Gancz H, Niderman-Meyer O, Broz M, Kashi Y, Shimoni E. Adhesion of Vibrio cholerae to granular starches. Appl Environ Microbiol. 2005;71:4850–4855. doi: 10.1128/AEM.71.8.4850-4855.2005.PubMedCrossRefGoogle Scholar
  32. 32.
    Topping DL, Illman RJ, Clarke JM, Trimble RP, Jackson KA, Marsono Y. Dietary fat and fiber alter large bowel and portal venous volatile fatty acids and plasma cholesterol but not biliary steroids in pigs. J Nutr. 1993;123:33–43.Google Scholar
  33. 33.
    Marsono Y, Illman RJ, Clarke JM, Trimble RP, Topping DL. Plasma lipids and large bowel volatile fatty acids in pigs fed white rice, brown rice and rice bran. Br J Nutr. 1993;70:503–513. doi: 10.1079/BJN19930144.PubMedCrossRefGoogle Scholar
  34. 34.
    Smiricky-Tjardes MR, Grieshop CM, Flickinger EA, Bauer LL, Fahey GC Jr. Dietary galactooligosaccharides affect ileal and total-tract nutrient digestibility and fecal bacterial concentrations, and ilea fermentative characteristics of growing pigs. J Anim Sci. 2003;81:2535–2545.PubMedGoogle Scholar
  35. 35.
    Björck I, Ostman E, Nilsson A. Modulating glycemia with cereal products. In: Marquart L, Jacobs DR, McIntosh GH Jr, Poutanen K, Reicks M, eds. Whole Grains and Health. Ames: Blackwell; 2007:177–184.CrossRefGoogle Scholar
  36. 36.
    Le Blay G, Michel C, Blottiere HM, Cherbut C. Prolonged intake of fructo-oligosaccharides induces a short-term elevation of lactic acid-producing bacteria and a persistent increase in cecal butyrate in rats. J Nutr. 1999;129:2231–2235.PubMedGoogle Scholar
  37. 37.
    Nilsson U, Nyman M. Short-chain fatty acid formation in the hindgut of rats fed oligosaccharides varying in monomeric composition, degree of polymerisation and solubility. Br J Nutr. 2005;94:705–713. doi: 10.1079/BJN20051531.PubMedCrossRefGoogle Scholar
  38. 38.
    Gibson GR, Beatty ER, Wang X, Cummings JH. Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology. 1995;108:975–982. doi: 10.1016/0016-5085(95)90192-2.PubMedCrossRefGoogle Scholar
  39. 39.
    Andersson HB, Ellegard LH. Bosaeus, Nondigestibility characteristics of inulin and oligofructose in humans. J Nutr. 1999;129:428S–1430S.Google Scholar
  40. 40.
    Houdijk JG, Bosch MW, Tamminga S, Verstegen MW, Berenpas EB, Knoop H. Apparent ileal and total-tract nutrient digestion by pigs as affected by dietary nondigestible oligosaccharides. J Anim Sci. 1999;77:148–158.PubMedGoogle Scholar
  41. 41.
    Cats A, De Vries EG, Mulder NH, Kleibeuker JH. Regional differences of physiological functions and cancer susceptibility in the human large intestine. Int J Oncol. 1996;9:1055–1069.Google Scholar
  42. 42.
    Toden S, Bird AR, Topping DL, Conlon MA. Resistant starch attenuates colonic DNA damage induced by high dietary protein in rats. Nutr Cancer. 2005;51:45–51. doi: 10.1207/s15327914nc5101_7 Google Scholar
  43. 43.
    Rafter J, Bennett M, Caderni G, et al. Dietary synbiotics reduce cancer risk factors in polypectomized and colon cancer patients. Am J Clin Nutr. 2007;85:488–496.PubMedGoogle Scholar
  44. 44.
    Visek WJ. Diet and cell growth modulation by ammonia. Am J Clin Nutr. 1978;31:S216–S220.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Anthony R. Bird
    • 1
    • 2
  • Michelle Vuaran
    • 1
  • Ross Crittenden
    • 1
    • 3
  • Takashi Hayakawa
    • 1
    • 4
  • Martin J. Playne
    • 1
    • 5
  • Ian L. Brown
    • 1
    • 6
  • David L. Topping
    • 1
    • 2
    Email author
  1. 1.Co-operative Research Centre for Food Industry InnovationCSIRO Human NutritionAdelaideAustralia
  2. 2.Food Futures National Research FlagshipCSIRO Human NutritionAdelaideAustralia
  3. 3.Food Science AustraliaWerribeeAustralia
  4. 4.Department of Food Science, Faculty of AgricultureGifu UniversityGifuJapan
  5. 5.Melbourne BiotechnologyHamptonAustralia
  6. 6.Faculty of Health and Behavioural ScienceUniversity of WollongongNorth WollongongAustralia

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