Skip to main content Accessibility help
×
Home

Ileal and hindgut fermentation in the growing pig fed a human-type diet

  • Anna M. E. Hoogeveen (a1) (a2), Paul J. Moughan (a2), Edward S. de Haas (a2), Paul Blatchford (a3), Warren C. McNabb (a2) and Carlos A. Montoya (a2) (a4)...

Abstract

Dietary fibre fermentation in humans and monogastric animals is considered to occur in the hindgut, but it may also occur in the lower small intestine. This study aimed to compare ileal and hindgut fermentation in the growing pig fed a human-type diet using a combined in vivo/in vitro methodology. Five pigs (23 (sd 1·6) kg body weight) were fed a human-type diet. On day 15, pigs were euthanised. Digesta from terminal jejunum and terminal ileum were collected as substrates for fermentation. Ileal and caecal digesta were collected for preparing microbial inocula. Terminal jejunal digesta were fermented in vitro with a pooled ileal digesta inoculum for 2 h, whereas terminal ileal digesta were fermented in vitro with a pooled caecal digesta inoculum for 24 h. The ileal organic matter fermentability (28 %) was not different from hindgut fermentation (35 %). However, the organic matter fermented was 66 % greater for ileal fermentation than hindgut fermentation (P = 0·04). Total numbers of bacteria in ileal and caecal digesta did not differ (P = 0·09). Differences (P < 0·05) were observed in the taxonomic composition. For instance, ileal digesta contained 32-fold greater number of the genus Enterococcus, whereas caecal digesta had a 227-fold greater number of the genus Ruminococcus. Acetate synthesis and iso-valerate synthesis were greater (P < 0·05) for ileal fermentation than hindgut fermentation, but propionate, butyrate and valerate synthesis was lower. SCFA were absorbed in the gastrointestinal tract location where they were synthesised. In conclusion, a quantitatively important degree of fermentation occurs in the ileum of the growing pig fed a human-type diet.

Copyright

Corresponding author

*Corresponding author: Carlos A. Montoya, email carlos.montoya@agresearch.co.nz

References

Hide All
1.Cummings, JH & Englyst, HN (1987) Fermentation in the human large intestine and the available substrates. Am J Clin Nutr 45, 12431255.
2.Roediger, WE (1980) Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man. Gut 21, 793798.
3.Morrison, DJ & Preston, T (2016) Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes 7, 189200.
4.Wang, M, Ahrne, S, Jeppsson, B, et al. (2005) Comparison of bacterial diversity along the human intestinal tract by direct cloning and sequencing of 16S rRNA genes. FEMS Microbiol Ecol 54, 219231.
5.Zoetendal, EG, Raes, J, van den Bogert, B, et al. (2012) The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. ISME J 6, 14151426.
6.Metzler-Zebeli, BU, Hooda, S, Pieper, R, et al. (2010) Nonstarch polysaccharides modulate bacterial microbiota, pathways for butyrate production, and abundance of pathogenic Escherichia coli in the pig gastrointestinal tract. Appl Environ Microbiol 76, 36923701.
7.Montoya, CA, Henare, SJ, Zhu, Pet al. (2019) Adaptation over time of intestinal fermentation in the growing pig is influenced by the amount of kiwifruit consumed. Br J Nutr 121, 601614.
8.Englyst, HN & Cummings, JH (1987) Digestion of polysaccharides of potato in the small intestine of man. Am J Clin Nutr 45, 423431.
9.Holloway, WD, Tasman-Jones, C & Maher, K (1983) Pectin digestion in humans. Am J Clin Nutr 37, 253255.
10.Jaworski, NW & Stein, HH (2017) Disappearance of nutrients and energy in the stomach and small intestine, cecum, and colon of pigs fed corn-soybean meal diets containing distillers dried grains with solubles, wheat middlings, or soybean hulls. J Anim Sci 95, 727739.
11.Bach Knudsen, KE & Canibe, N (2000) Breakdown of plant carbohydrates in the digestive tract of pigs fed on wheat- or oat-based rolls. J Sci Food Agric 80, 12531261.
12.Lien, KA, McBurney, MI, Beyde, BI, et al. (1996) Ileal recovery of nutrients and mucin in humans fed total enteral formulas supplemented with soy fiber. Am J Clin Nutr 63, 584595.
13.Englyst, HN & Cummings, JH (1986) Digestion of the carbohydrates of banana (Musa paradisiaca sapientum) in the human small intestine. Am J Clin Nutr 44, 4250.
14.Montoya, CA, Henare, SJ, Rutherfurd, SM, et al. (2016) Potential misinterpretation of the nutritional value of dietary fiber: correcting fiber digestibility values for nondietary gut-interfering material. Nutr Rev 74, 517533.
15.Montoya, CA, Rutherfurd, SM & Moughan, PJ (2015) Nondietary gut materials interfere with the determination of dietary fiber digestibility in growing pigs when using the Prosky method. J Nutr 145, 19661972.
16.Graff, J, Brinch, K & Madsen, JL (2001) Gastrointestinal mean transit times in young and middle-aged healthy subjects. Clin Physiol 21, 253259.
17.Jensen, BB & Jørgensen, H (1994) Effect of dietary fiber on microbial activity and microbial gas production in various regions of the gastrointestinal tract of pigs. Appl Environ Microbiol 60, 18971904.
18.Montoya, CA, de Haas, ES & Moughan, PJ (2018) Development of an in vivo and in vitro ileal fermentation method in a growing pig model. J Nutr 148, 298305.
19.Coles, LT, Moughan, PJ, Awati, A, et al. (2013) Optimisation of inoculum concentration and incubation duration for an in vitro hindgut dry matter digestibility assay. Food Chem 136, 624631.
20.Food and Agriculture Organization (2013) Dietary protein quality evaluation in human nutrition. FAO Food Nutr Pap 92, 166.
21.Deglaire, A & Moughan, PJ (2012) Animal models for determining amino acid digestibility in humans – a review. Br J Nutr 108, Suppl. 2, S273S281.
22.Baer, DJ, Rumpler, WV, Miles, CW, et al. (1997) Dietary fiber decreases the metabolizable energy content and nutrient digestibility of mixed diets fed to humans. J Nutr 127, 579586.
23.National Research Council (1998) Nutrient Requirements of Swine, 10th rev. ed. Washington, DC: The National Academies Press.
24.Short, FJ, Gorton, P, Wiseman, J, et al. (1996) Determination of titanium dioxide added as an inert marker in chicken digestibility studies. Anim Feed Sci Technol 59, 215221.
25.AOAC (2012) Official Method of Analysis, 19th ed. Rockville, MD: AOAC International.
26.Prosky, L, Asp, NG, Schweizer, TF, et al. (1988) Determination of insoluble, soluble, and total dietary fiber in foods and food products: interlaboratory study. J Assoc Off Anal Chem 71, 10171023.
27.Montoya, CA, Rutherfurd, SM & Moughan, PJ (2016) Kiwifruit fibre level influences the predicted production and absorption of SCFA in the hindgut of growing pigs using a combined in vivo-in vitro digestion methodology. Br J Nutr 115, 13171324.
28.Healey, G, Murphy, R, Butts, C, et al. (2017) Variability in gut microbiota response to an inulin-type fructan prebiotic within an in vitro three-stage continuous colonic model system. Bioact Carbohydr Diet Fibre 11, 2637.
29.Nadkarni, MA, Martin, FE, Jacques, NA, et al. (2002) Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 148, 257266.
30.Kozich, JJ, Westcott, SL, Baxter, NT, et al. (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79, 51125120.
31.Caporaso, JG, Kuczynski, J, Stombaugh, J, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7, 335336.
32.Edgar, RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 24602461.
33.Edgar, RC, Haas, BJ, Clemente, JC, et al. (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 21942200.
34.DeSantis, TZ, Hugenholtz, P, Larsen, N, et al. (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72, 50695072.
35.Faith, DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61, 110.
36.Awati, A, Williams, BA, Bosch, MW, et al. (2006) Dietary carbohydrates with different rates of fermentation affect fermentation end-product profiles in different sites of gastro-intestinal tract of weaning piglet. Anim Sci 82, 837843.
37.Rowan, AM, Moughan, PJ & Wilson, MN (1992) The flows of deoxyribonucleic acid and diaminopimelic acid and the digestibility of dietary fibre components at the terminal ileum, as indicators of microbial activity in the upper digestive tract of ileostomised pigs. Anim Feed Sci Technol 36, 129141.
38.Wedekind, KJ, Mansfield, HR & Montgomery, L (1988) Enumeration and isolation of cellulolytic and hemicellulolytic bacteria from human feces. Appl Environ Microbiol 54, 15301535.
39.Falony, G, Joossens, M, Vieira-Silva, S, et al. (2016) Population-level analysis of gut microbiome variation. Science 352, 560564.
40.Cummings, JH, Pomare, EW, Branch, WJ, et al. (1987) Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 28, 12211227.
41.Boets, E, Gomand, SV, Deroover, L, et al. (2017) Systemic availability and metabolism of colonic-derived short-chain fatty acids in healthy subjects: a stable isotope study. J Physiol 595, 541.
42.Barcenilla, A, Pryde, SE, Martin, JC, et al. (2000) Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl Environ Microbiol 66, 16541661.
43.Walker, AW, Duncan, SH, Carol McWilliam Leitch, Eet al. (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 Microbiol 71, 36923700.
44.Long, W, Zhang, C, Liu, S, et al. (2017) Fiber-utilizing capacity varies in Prevotella- versus Bacteroides-dominated gut microbiota. Sci Rep 7, 2594.
45.Louis, P & Flint, HJ (2017) Formation of propionate and butyrate by the human colonic microbiota. Environ Microbiol 19, 2941.
46.Macfarlane, GT, Gibson, GR & Cummings, JH (1992) Comparison of fermentation reactions in different regions of the human colon. J Appl Bacteriol 72, 5764.
47.Schmitt, MG, Soergel, KH, Wood, CM, et al. (1977) Absorption of short-chain fatty acids from the human ileum. Am J Dig Dis 22, 340347.
48.McNeil, NI, Cummings, JH & James, WP (1978) Short chain fatty acid absorption by the human large intestine. Gut 19, 819822.
49.Kaji, I, Karaki, S-i, Tanaka, R, et al. (2011) Density distribution of free fatty acid receptor 2 (FFA2)-expressing and GLP-1-producing enteroendocrine L cells in human and rat lower intestine, and increased cell numbers after ingestion of fructo-oligosaccharide. J Mol Histol 42, 2738.
50.Kamath, PS, Phillips, SF & Zinsmeister, AR (1988) Short-chain fatty acids stimulate ileal motility in humans. Gastroenterology 95, 14961502.
51.Miller, ER & Ullrey, DE (1987) The pig as a model for human nutrition. Annu Rev Nutr 7, 361382.

Keywords

Type Description Title
WORD
Supplementary materials

Hoogeveen et al. supplementary material
Hoogeveen et al. supplementary material

 Word (58 KB)
58 KB

Ileal and hindgut fermentation in the growing pig fed a human-type diet

  • Anna M. E. Hoogeveen (a1) (a2), Paul J. Moughan (a2), Edward S. de Haas (a2), Paul Blatchford (a3), Warren C. McNabb (a2) and Carlos A. Montoya (a2) (a4)...

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.