Hostname: page-component-8448b6f56d-c47g7 Total loading time: 0 Render date: 2024-04-23T16:38:15.567Z Has data issue: false hasContentIssue false
  • English
  • Français

Dietary supplementation with a nucleotide-rich yeast extract modulates gut immune response and microflora in weaned pigs in response to a sanitary challenge

Published online by Cambridge University Press:  20 June 2017

S. M. Waititu ,
F. Yin ,
R. Patterson ,
A. Yitbarek ,
J. C. Rodriguez-Lecompte  and
C. M. Nyachoti
S. M. Waititu
Affiliation:
Department of Animal Science, University of Manitoba, Winnipeg, MB, Canada, R3T 2N2
F. Yin
Affiliation:
Department of Animal Science, University of Manitoba, Winnipeg, MB, Canada, R3T 2N2
R. Patterson
Affiliation:
Canadian Bio-Systems Inc., Calgary, AB, Canada, T2C 0J7
A. Yitbarek
Affiliation:
Department of Animal Science, University of Manitoba, Winnipeg, MB, Canada, R3T 2N2
J. C. Rodriguez-Lecompte
Affiliation:
Department of Pathology and Microbiology, Atlantic Veterinary College, University of Prince Edward Island, Charlottetown, Prince Edward Island, Canada, C1A 4P3
C. M. Nyachoti*
Affiliation:
Department of Animal Science, University of Manitoba, Winnipeg, MB, Canada, R3T 2N2
*
†E-mail: Martin_Nyachoti@umanitoba.ca
Get access

Abstract

An experiment was carried out to evaluate the short-term effect of supplementing a nucleotide-rich yeast extract (NRYE) on growth performance, gut structure, immunity and microflora of piglets raised under sanitary and unsanitary conditions. A total of 84, 21-day old piglets were used in this study; 42 piglets were raised in a room designated as the clean room that was washed once per week, whereas the other 42 piglets were raised in a room designated as the unclean room in which 7 kg of manure from the sow herd was spread on each pen floor on day 1 and 7 and the room was not washed throughout the experiment. The pigs were fed a corn–soybean meal-based diet without or with 0.1% NRYE. Each treatment had 7 replicate pens in each room, and each pen housed 3 pigs. Feed disappearance and BW were recorded on day 1 and 14. On day 14, one pig per pen was euthanized to collect ileum, mesenteric lymph nodes and spleen tissues, and cecum and colon digesta. Overall, NRYE supplementation did not affect growth performance in both clean and unclean conditions, improved kidney weight in both clean (P=0.0002) and unclean room (P<0.0001) and tended to improve the villus height/crypt depth ratio in the clean room (P=0.073). Supplementing NRYE was associated with upregulation of Ileal programmed cell death gene-1 (P=0.0003), interleukin (IL)-1β (P<0.0001), IL-6 (P=0.0003), IL-10 (P<0.0001) and tumor necrosis factor-α (TNF-α) (P<0.0001) in pigs raised in the unclean room. Supplementing the NRYE in pigs raised in the clean room suppressed growth of cecal Enterobacteriacea (P<0.0001) members and colonic Enterococcus spp. (P<0.019), improved proliferation of cecal Lactobacillus spp. (P<0.002) and colonic Clostridium cluster IV (P<0.011) and XVIa members (P<0.0002). Supplementing the NRYE in the unclean room improved proliferation of cecal Clostridium cluster IV (P<0.026) and suppressed proliferation of colonic Enterococcus spp. (P<0.037). In conclusion, supplementing the NRYE to piglets under unsanitary conditions improved ileal immune response by upregulating inflammatory cytokines, and positively modulated proliferation of beneficial gut bacteria and suppression of harmful ones in both clean and unclean rooms.

Keywords

growth performancegut bacteriaimmune responsenucleotidespiglets
Type
Research Article
Information
animal , Volume 11 , Issue 12 , December 2017 , pp. 2156 - 2164
Copyright
© The Animal Consortium 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

a

Present address: Department of Pathobiology, University of Guelph, Guelph, ON, Canada, N1G 2W1

References

Andres-Elias, N, Pujols, J, Badiola, I and Torrallardona, D 2007. Effect of nucleotides and carob pulp on gut health and performance of weanling piglets. Livestock Science 108, 280–283.Google Scholar
Association of Official Analytical Chemists 1990. Official methods of analysis of the AOAC. AOAC, Washington, DC.Google Scholar
Baer, AA, Miller, MJ and Dilger, AC 2013. Pathogens of interest to the pork industry: a review of research on interventions to assure food safety. Comprehensive Reviews in Food Science and Food Safety 12, 183–217.Google Scholar
Bartosch, S, Fite, A, Macfarlane, GT and McMurdo, ME 2004. Characterization of bacterial communities in feces from healthy elderly volunteers and hospitalized elderly patients by using real-time PCR and effects of antibiotic treatment on the fecal microbiota. Applied and Environmental Microbiology 70, 3575–3581.Google Scholar
Brulé, D, Sarwar, G, Savoie, L, Campbell, J and Van Zeggelaar, M 1988. Differences in uricogenic effects of dietary purine bases, nucleosides and nucleotides in rats. Journal of Nutrition 118, 780–786.Google Scholar
Canadian Council on Animal Care 2009. CCAC guidelines on: the care and use of farm animals in research, teaching and testing. Canadian Council on Animal Care, Ottawa, ON, Canada.Google Scholar
D’Elia, RV, Harrison, K, Oyston, PC, Lukaszewski, RA and Clark, GC 2013. Targeting the “cytokine storm” for therapeutic benefit. Clinical and Vaccine Immunology 20, 319–327.Google Scholar
Gil, A, Corral, E, Martinez, A and Molina, J 1986. Effects of the addition of nucleotides to an adapted milk formula on the microbial pattern of faeces in at term newborn infants. Journal of Clinical Nutrition Gastroenterology 1, 127–132.Google Scholar
Grimble, GK and Westwood, OM 2001. Nucleotides as immunomodulators in clinical nutrition. Current Opinion in Clinical Nutrition and Metabolic Care 4, 57–64.Google Scholar
Hamer, HM, Jonkers, D, Venema, K, Vanhoutvin, S, Troost, F and Brummer, R 2008. Review article: the role of butyrate on colonic function. Alimentary Pharmacology & Therapeutics 27, 104–119.Google Scholar
Ivarsson, E, Roos, S, Liu, H and Lindberg, J 2014. Fermentable non-starch polysaccharides increases the abundance of Bacteroides-Prevotella-Porphyromonas in ileal microbial community of growing pigs. Animal 8, 1777–1787.Google Scholar
Kogan, G and Kocher, A 2007. Role of yeast cell wall polysaccharides in pig nutrition and health protection. Livestock Science 109, 161–165.Google Scholar
Kulkarni, AD, Rudolph, FB and Van Buren, CT 1994. The role of dietary sources of nucleotides in immune function: a review. Journal of Nutrition 124, 1442S–1446S.Google Scholar
Lee, D-H, Zo, Y-G and Kim, S-J 1996. Nonradioactive method to study genetic profiles of natural bacterial communities by PCR-single-strand-conformation polymorphism. Applied and Environmental Microbiology 62, 3112–3120.Google Scholar
Levine, UY, Looft, T, Allen, HK and Stanton, TB 2013. Butyrate-producing bacteria, including mucin degraders, from the swine intestinal tract. Applied and Environmental Microbiology 79, 3879–3881.Google Scholar
Li, H, Zhao, P, Lei, Y, Li, T and Kim, I 2015. Response to an Escherichia coli K88 oral challenge and productivity of weanling pigs receiving a dietary nucleotides supplement. Journal of Animal Science and Biotechnology 6, 1–9.Google Scholar
Li, M, Gong, J, Cottrill, M, Yu, H, de Lange, C, Burton, J and Topp, E 2003. Evaluation of QIAamp® DNA Stool Mini Kit for ecological studies of gut microbiota. Journal of Microbiological Methods 54, 13–20.Google Scholar
Liang, SC, Latchman, YE, Buhlmann, JE, Tomczak, MF, Horwitz, BH, Freeman, GJ and Sharpe, AH 2003. Regulation of PD‐1, PD‐L1, and PD‐L2 expression during normal and autoimmune responses. European Journal of Immunology 33, 2706–2716.Google Scholar
Mateo, CD 2005. Aspects of nucleotide nutrition in pigs. Doctoral dissertation, South Dakota State University, Brookings, USA.Google Scholar
Matsuki, T, Watanabe, K, Fujimoto, J, Miyamoto, Y, Takada, T, Matsumoto, K, Oyaizu, H and Tanaka, R 2002. Development of 16S rRNA-gene-targeted group-specific primers for the detection and identification of predominant bacteria in human feces. Applied and Environmental Microbiology 68, 5445–5451.Google Scholar
McCracken, BA, Spurlock, ME, Roos, MA, Zuckermann, FA and Gaskins, HR 1999. Weaning anorexia may contribute to local inflammation in the piglet small intestine. Journal of Nutrition 129, 613–619.Google Scholar
Medzhitov, R 2007. Recognition of microorganisms and activation of the immune response. Nature 449, 819–826.Google Scholar
NRC 2012. Nutrient requirements of swine, 11th edition. National Academic Press, Washington, DC.Google Scholar
Pescovitz, M, Pabst, R, Rothkötter, H, Murtaugh, M, Foss, D, Butler, J, Lunney, J, Vogeli, P, Llanes, D and Trebichavsky, I 1998. Immunology of the pig. In Handbook of vertebrate immunology (ed. PP Pastoret, P Griebel, H Bazin and A Govaerts), pp. 373–419. Academic Press, London.Google Scholar
Pié, S, Lallès, JP, Blazy, F, Laffitte, J, Sève, B and Oswald, IP 2004. Weaning is associated with an upregulation of expression of inflammatory cytokines in the intestine of piglets. Journal of Nutrition 134, 641–647.Google Scholar
Pluske, JR, Thompson, MJ, Atwood, CS, Bird, PH, Williams, IH and Hartmann, PE 1996. Maintenance of villus height and crypt depth, and enhancement of disaccharide digestion and monosaccharide absorption, in piglets fed on cows’ whole milk after weaning. British Journal of Nutrition 76, 409–422.Google Scholar
Rasmussen, R 2001. Quantification on the LightCycler. In Rapid cycle real-time PCR (ed. S Meuer, C Wittwer and KI Nakagawara), pp. 21–34. Springer, Berlin.Google Scholar
Rinttilä, T, Kassinen, A, Malinen, E, Krogius, L and Palva, A 2004. Development of an extensive set of 16S rDNA‐targeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real‐time PCR. Journal of Applied Microbiology 97, 1166–1177.Google Scholar
Sauer, N, Eklund, M, Roth, S, Rink, F, Jezierny, D, Bauer, E and Mosenthin, R 2012. Short-term effect of dietary yeast nucleotide supplementation on small intestinal enzyme activities, bacterial populations and metabolites and ileal nutrient digestibilities in newly weaned pigs. Journal of Animal Physiology and Animal Nutrition 96, 700–708.Google Scholar
Sauer, N, Mosenthin, R and Bauer, E 2011. The role of dietary nucleotides in single-stomached animals. Nutrition Research Reviews 24, 46–59.Google Scholar
Sharpe, AH, Wherry, EJ, Ahmed, R and Freeman, GJ 2007. The function of programmed cell death 1 and its ligands in regulating autoimmunity and infection. Nature Immunology 8, 239–245.Google Scholar
Story, D, Shrader, R, Theriault, L, Lumijarvi, D, Shenoy, T, Savaiano, D, Shaffer, R, Ho, C and Clifford, A 1977. Effects of dietary protein, adenine, and allopurinol on growth and metabolism of rats. Journal of Nutrition 107, 1044–1052.Google Scholar
Tanaka, R and Mutai, M 1980. Improved medium for selective isolation and enumeration of Bifidobacterium. Applied and Environmental Microbiology 40, 866–869.Google Scholar
Toback, FG, Walsh-Reitz, MM, Mendley, SR and Kartha, S 1990. Kidney epithelial cells release growth factors in response to extracellular signals. Pediatric Nephrology 4, 363–371.Google Scholar
Uauy, R, Quan, R and Gil, A 1994. Role of nucleotides in intestinal development and repair: implications for infant nutrition. Journal of Nutrition 124, 1436S–1441S.Google Scholar
Uauy, R, Stringel, G, Thomas, R and Quan, R 1990. Effect of dietary nucleosides on growth and maturation of the developing gut in the rat. Journal of Pediatric Gastroenterology and Nutrition 10, 497–503.Google Scholar
Van Barneveld, R and Dunshea, F 2011. Colostrum protein isolate increases gut and whole body growth and plasma IGF-I in neonatal pigs. Asian-Australasian Journal of Animal Sciences 24, 670–677.Google Scholar
Van Buren, CT and Rudolph, F 1997. Dietary nucleotides: a conditional requirement. Nutrition 13, 470–472.Google Scholar
Walter, J, Hertel, C, Tannock, GW, Lis, CM, Munro, K and Hammes, WP 2001. Detection of Lactobacillus, Pediococcus, Leuconostoc, and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Applied and Environmental Microbiology 67, 2578–2585.CrossRefGoogle ScholarPubMed
Zhao, J, Harper, A, Estienne, M, Webb, K, McElroy, A and Denbow, D 2007. Growth performance and intestinal morphology responses in early weaned pigs to supplementation of antibiotic-free diets with an organic copper complex and spray-dried plasma protein in sanitary and nonsanitary environments. Journal of Animal Science 85, 1302–1310.Google Scholar