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Resistant starch reduces large intestinal pH and promotes fecal lactobacilli and bifidobacteria in pigs

Published online by Cambridge University Press:  10 May 2018

B. U. Metzler-Zebeli ,
N. Canibe ,
L. Montagne ,
J. Freire ,
P. Bosi ,
J. A. M. Prates ,
S. Tanghe  and
P. Trevisi
B. U. Metzler-Zebeli*
Affiliation:
Institute of Animal Nutrition and Functional Plant Compounds, Department for Farm Animals and Veterinary Public Health, Vetmeduni Vienna, 1210 Vienna, Austria
N. Canibe
Affiliation:
Department of Animal Science, Aarhus University, 8830 Tjele, Denmark
L. Montagne
Affiliation:
PEGASE, Agrocampus Ouest, INRA, 35590, Saint-Gilles, France
J. Freire
Affiliation:
LEAF, Instituto Superior de Agronomia, University of Lisbon, Tapada da Ajuda, 1349-017 Lisbon, Portugal
P. Bosi
Affiliation:
Department of Agricultural and Food Science (DISTAL), University of Bologna, 40127 Bologna, Italy
J. A. M. Prates
Affiliation:
CIISA, Faculty of Veterinary Medicine, University of Lisbon, Avenida da Universidade Técnica, Alto da Ajuda, 1300-477 Lisbon, Portugal
S. Tanghe
Affiliation:
Nutritional Solutions Divisions, Nutrition Sciences N.V., 9031 Ghent, Belgium
P. Trevisi
Affiliation:
Department of Agricultural and Food Science (DISTAL), University of Bologna, 40127 Bologna, Italy
*
†E-mail: barbara.metzler@vetmeduni.ac.at
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Abstract

Dietary resistant starch (RS) may have prebiotic properties but its effects on fermentation and the microbial population are inconsistent. This meta-analysis aimed to quantify the relationship between RS type 2 (RS2) and intestinal short-chain fatty acids (SCFA) and pH as well as certain key bacterial taxa for intestinal health in pigs. From the 24 included articles with sufficient information about the animal, and dietary and physiological measurements published between 2000 and 2017, individual sub-data sets for fermentation metabolites, pH, bacterial abundances and apparent total tract digestibility were built and used to parameterize prediction models on the effect of RS2, accounting for inter- and intra-study variability. In addition, the effect of pig’s BW at the start of the experiment and duration of the experimental period on response variables were also evaluated using backward elimination analysis. Dietary RS levels ranged from 0% to 78.0% RS, with median and mean RS levels of 28.8% and 23.0%, respectively. Negative relationships could be established between dietary RS and pH in the large intestine (P<0.05), with a stronger effect in the mid and distal colon, and feces (R2=0.64 to 0.81; P<0.001). A dietary level of 15% RS would lower the pH in the proximal, mid-, distal colon and feces by 0.2, 0.6, 0.4 and 0.6 units, respectively. Increasing RS levels, however, did not affect SCFA concentrations in the hindgut, but enhanced the molar proportion of propionate in mid-colon and reduced those of acetate in mid-colon and of butyrate in mid- and distal colon (R2=0.46 to 0.52; P<0.05). Backward elimination indicated an age-related decrease in mid-colonic propionate proportion and increase in mid- and distal colonic butyrate proportion (P<0.05), thereby modulating RS2 effects. In feces, increasing RS levels promoted fecal lactobacilli (R2=0.46; P<0.01) and bifidobacteria (R2=0.57; P<0.01), whereby the slope showed the need for a minimal RS level of 10% for a 0.5 log unit-increase in their abundance. Best-fit equations further supported that a longer experimental period increased fecal lactobacilli but decreased fecal bifidobacteria (P<0.05). In conclusion, dietary RS2 seems to effectively decrease digesta pH throughout the large intestine and increase lactic acid-producing bacteria in feces of pigs which may limit the growth of opportunistic pathogens in the hindgut. To achieve these physiologically relevant changes, dietary RS should surpass 10% to 15%.

Keywords

resistant starch type 2gastrointestinal tractmeta-analysislactic acid-producing bacteriashort-chain fatty acids

Information

Type
Research Article
Information
animal , Volume 13 , Issue 1 , January 2019 , pp. 64 - 73
Copyright
© The Animal Consortium 2018 

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References

Bach Knudsen, KE, Hedemann, MS and Lærke, HN 2012. The role of carbohydrates in intestinal health of pigs. Animal Feed Science and Technology 173, 41–53.Google Scholar
Bach Knudsen, KE, Jensen, BB and Hansen, I 1993. Digestion of polysaccharides and other major components in the small and large intestine of pigs fed diets consisting of oat fractions rich in β-d-glucan. British Journal of Nutrition 70, 537–556.Google Scholar
Bergman, EN 1990. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiological Reviews 70, 567–583.Google Scholar
Bian, G, Ma, S, Zhu, Z, Su, Y, Zoetendal, EG, Mackie, R, Liu, J, Mu, C, Huang, R, Smidt, H and Zhu, W 2016. Age, introduction of solid feed and weaning are more important determinants of gut bacterial succession in piglets than breed and nursing mother as revealed by a reciprocal cross-fostering model. Environmental Microbiology 18, 1566–1577.Google Scholar
Bird, AR, Vuaran, M, Crittenden, R, Hayakawa, T, Playne, MJ, Brown, IL and 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.Google Scholar
Birt, DF, Boylston, T, Hendrich, S, Jane, JL, Hollis, J, Li, L, McClelland, J, Moore, S, Phillips, GJ, Rowling, M, Schalinske, K, Scott, MP and Whitley, EM. 2013. Resistant starch: promise for improving human health. Advances in Nutrition 4, 587–601.Google Scholar
Champ, M 1992. Determination of resistant starch in foods and food products: interlaboratory study. European Journal of clinical Nutrition 46, S51–S62.Google Scholar
Charbonneau, E, Pellerin, D and Oetzel, GR 2006. Impact of lowering dietary cation-anion difference in nonlactating dairy cows: a meta-analysis. Journal of Dairy Science 89, 537–548.Google Scholar
Collins, JF, Honda, T, Knobel, S, Bulus, NM, Conary, J, DuBois, R and Ghishan, FK 1993. Molecular cloning, sequencing, tissue distribution, and functional expression of a Na1/H1 exchanger (NHE-2). Proceedings of the National Academy of Sciences of the United States of America 90, 3938–3942.Google Scholar
Cummings, JH and Macfarlane, GT 1991. The control and consequences of bacterial fermentation in the human colon. Journal of Applied Bacteriology 70, 443–459.Google Scholar
Englyst, HN and Cummings, JH 1984. Simplified method for the measurement of total non-starch polysaccharides by gas-liquid chromatography of constituent sugars as alditol acetates. Analyst 109, 937–942.Google Scholar
Fairbrother, JM, Nadeau, E and Gyles, CL 2005. Escherichia coli in postweaning diarrhea in pigs: an update on bacterial types, pathogenesis, and prevention strategies. Animal Health Research Reviews 6, 17–39.Google Scholar
Giuberti, G, Gallo, A, Moschini, M and Masoero, F 2015. New insight into the role of resistant starch in pig nutrition. Animal Feed Science and Technology 201, 1–13.Google Scholar
Haenen, D, Zhang, J, da Silva, CS, Bosch, G, van der Meer, IM, van Arkel, J, van den Borne, JJGC, Pérez Gutiérrez, O, Smidt, H, Kemp, B, Müller, M and Hooiveld, GJEJ 2013. A diet high in resistant starch modulates microbiota composition, SCFA concentrations, and gene expression in pig intestine. Journal of Nutrition 143, 274–283.Google Scholar
Hein, I, Lehner, A, Rieck, P, Klein, K, Brandl, E and Wagner, M. 2001. Comparison of different approaches to quantify Staphylococcus aureus cells by real-time quantitative PCR and application of this technique for examination of cheese. Applied and Environmental Microbiology 67, 3122–3126.Google Scholar
Heo, JM, Agyekum, AK, Yin, YL, Rideout, TC and Nyachoti, CM 2014. Feeding a diet containing resistant potato starch influences gastrointestinal tract traits and growth performance of weaned pigs. Journal of Animal Science 92, 3906–3913.Google Scholar
Kamiya, T, Watanabe, Y, Makino, S, Kano, H and Tsuji, NM 2016. Improvement of intestinal immune cell function by lactic acid bacteria for dairy products. Microorganisms 5, E1.Google Scholar
Kandasamy, S, Chattha, KS, Vlasova, AN, Rajashekara, G and Saif, LJ 2014. Lactobacilli and Bifidobacteria enhance mucosal B cell responses and differentially modulate systemic antibody responses to an oral human rotavirus vaccine in a neonatal gnotobiotic pig disease model. Gut Microbes 5, 639–651.Google Scholar
Lipsey, M and Wilson, D 2001. Practical meta-analysis. Sage, Thousand Oaks, CA, USA.Google Scholar
Louis, P and Flint, HJ 2017. Formation of propionate and butyrate by the human colonic microbiota. Environmental Microbiology 19, 29–41.Google Scholar
Louis, P, Scott, KP, Duncan, SH and Flint, HJ 2007. Understanding the effects of diet on bacterial metabolism in the large intestine. Journal of Applied Microbiology 102, 1197–1208.Google Scholar
Martínez-Puig, D, Pérez, JF, Castillo, M, Andaluz, A, Anguita, M, Morales, J and Gasa, J 2003. Consumption of raw potato starch increases colon length and fecal excretion of purine bases in growing pigs. Journal of Nutrition 133, 134–139.Google Scholar
Mentschel, J and Claus, R 2003. Increased butyrate formation in the pig colon by feeding raw potato starch leads to a reduction of colonocyte apoptosis and a shift to the stem cell compartment. Metabolism 52, 1400–1405.Google Scholar
Metzler-Zebeli, BU, Mann, E, Schmitz-Esser, S, Wagner, M, Ritzmann, M and Zebeli, Q 2013. Changing dietary calcium-phosphorus level and cereal source selectively alters abundance of bacteria and metabolites in the upper gastrointestinal tracts of weaned pigs. Applied and Environmental Microbiology 79, 7264–7272.Google Scholar
Metzler-Zebeli, BU, Eberspächer, E, Grüll, D, Kowalczyk, L, Molnar, T and Zebeli, Q 2015a. Enzymatically modified starch ameliorates postprandial serum triglycerides and lipid metabolome in growing pigs. PLoS One 10, e0130553.Google Scholar
Metzler-Zebeli, BU, Schmitz-Esser, S, Mann, E, Grüll, D, Molnar, T and Zebeli, Q 2015b. Adaptation of the cecal bacterial microbiome of growing pigs in response to resistant starch type 4. Applied and Environmental Microbiology 81, 8489–8499.Google Scholar
Metzler-Zebeli, BU, Trevisi, P, Prates, JAM, Tanghe, S, Bosi, P, Canibe, N, Montagne, L, Freire, J and Zebeli, Q 2017. Assessing the effect of dietary inulin supplementation on gastrointestinal fermentation, digestibility and growth in pigs: a meta-analysis. Animal Feed Science and Technology 233, 120–132.Google Scholar
Morales, MD, Escarpa, A and González, MC 1997. Simultanous determination of resistant and digestible starch in foods and food products. Starch 49, 448–453.Google Scholar
Morrison, DJ and Preston, T 2016. Formation of short-chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes 7, 189–200.Google Scholar
Motta, V, Trevisi, P, Bertolini, F, Ribani, A, Schiavo, G, Fontanesi, L and Bosi, P 2017. Exploring gastric bacterial community in young pigs. PLoS One 12, e0173029.Google Scholar
Nielsen, TS, Lærke, HN, Theil, PK, Sørensen, JF, Saarinen, M, Forssten, S and Knudsen, KE 2014. Diets high in resistant starch and arabinoxylan modulate digestion processes and SCFA pool size in the large intestine and faecal microbial composition in pigs. British Journal of Nutrition 112, 1837–1849.Google Scholar
O’Shea, CJ, Sweeney, T, Bahar, B, Ryan, MT, Thornton, K and O'Doherty, JV 2012. Indices of gastrointestinal fermentation and manure emissions of growing-finishing pigs as influenced through singular or combined consumption of Lactobacillus plantarum and inulin. Journal of Animal Science 90, 3848–3857.Google Scholar
Pluske, JR, Montagne, L, Cavaney, FS, Mullan, BP, Pethick, DW and Hampson, DJ 2007. Feeding different types of cooked white rice to piglets after weaning influences starch digestion, digesta and fermentation characteristics and the faecal shedding of b-haemolytic Escherichia coli . British Journal of Nutrition 97, 298–306.Google Scholar
Regmi, PR, Metzler-Zebeli, BU, Gänzle, MG, van Kempen, TA and Zijlstra, RT 2011. Starch with high amylose content and low in vitro digestibility increases intestinal nutrient flow and microbial fermentation and selectively promotes bifidobacteria in pigs. Journal of Nutrition 141, 1273–1280.Google Scholar
Reichardt, N, Duncan, SH, Young, P, Belenguer, A, McWilliam Leitch, C, Scott, KP, Flint, HJ and Louis, P 2014. Phylogenetic distribution of three pathways for propionate production within the human gut microbiota. ISME Journal 8, 1323–1335.Google Scholar
Sales, J 2014. Effects of access to pasture on performance, carcass composition, and meat quality in broilers: a meta-analysis. Poultry Science 93, 1523–1533.Google Scholar
Schmidt, EG, Claesson, MH, Jensen, SS, Ravn, P and Kristensen, NN 2010. Antigen-presenting cells exposed to Lactobacillus acidophilus NCFM, Bifidobacterium bifidum BI-98, and BI-504 reduce regulatory T cell activity. Inflammatory Bowel Disease 16, 390–400.Google Scholar
Sepponen, K, Ruusunen, M, Pakkanen, JA and Pösö, AR 2007. Expression of CD147 and monocarboxylate transporters MCT1, MCT2, MCT4 in porcine small intestine and colon. The Veterinary Journal 174, 122–128.Google Scholar
St-Pierre, NR 2001. Integrating quantitative finding from multiple studies using mixed model methodology. Journal of Dairy Science 84, 741–755.Google Scholar
Sun, Y, Su, Y and Zhu, W 2016. Microbiome-metabolome responses in the cecum and colon of pig to a high resistant starch diet. Frontiers in Microbiology 7, 779.Google Scholar
Sun, Y, Zhou, L, Fang, L, Su, Y and Zhu, W 2015. Responses in colonic microbial community and gene expression of pigs to a long-term high resistant starch diet. Frontiers in Microbiology 6, 877.Google Scholar
Thwaites, DT and Anderson, CMH 2007. H-coupled nutrient, micronutrient and drug transporters in the mammalian small intestine. Experimental Physiology 92, 603–619.Google Scholar
Wang, JF, Zhu, YH, Li, DF, Wang, Z and Jensen, BB 2004. In vitro fermentation of various fiber and starch sources by pig fecal inocula. Journal of Animal Science 82, 2615–2622.Google Scholar
Wang, Z, Wang, L, Chen, Z, Ma, X, Yang, X, Zhang, J and Jiang, Z 2016. In vitro evaluation of swine-derived Lactobacillus reuteri: Probiotic properties and effects on intestinal porcine epithelial cells challenged with enterotoxigenic Escherichia coli K88. Journal of Microbiology Biotechnology 26, 1018–1025.Google Scholar
Yang, Y, Galle, S, Le, MH, Zijlstra, RT and Gänzle, MG 2015. Feed fermentation with reuteran- and levan-producing Lactobacillus reuteri reduces colonization of weanling pigs by enterotoxigenic Escherichia coli . Applied and Environmental Microbiology 81, 5743–5752.Google Scholar
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