Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-19T10:38:53.737Z Has data issue: false hasContentIssue false
  • English
  • Français

Health-promoting effects of Lactobacillus-fermented barley in weaned pigs challenged with Escherichia coli K88 +

Published online by Cambridge University Press:  20 August 2019

B. Koo ,
D. Bustamante-García Open the ORCID record for D. Bustamante-García [Opens in a new window] ,
J. W. Kim  and
C. M. Nyachoti
B. Koo
Affiliation:
Department of Animal Science, University of Manitoba, Winnipeg, MB R3T 2N2, Canada
D. Bustamante-García
Affiliation:
Instituto de Ciencia Animal, San José de las Lajas, 32700, Cuba
J. W. Kim
Affiliation:
Department of Animal Science, University of Manitoba, Winnipeg, MB R3T 2N2, Canada
C. M. Nyachoti*
Affiliation:
Department of Animal Science, University of Manitoba, Winnipeg, MB R3T 2N2, Canada
*
†E-mail: martin.nyachoti@umanitoba.ca
Get access

Abstract

Fermented feeds are being considered as practical alternatives to antimicrobial growth promoters (AGP) supplemented in nursery pig diets. This study aimed to investigate health-promoting effects of fermented barley in weaned pigs challenged with Escherichia coli K88 +. A total of 37 piglets were weaned at 21 ± 1 day of age (6.41 ± 0.47 kg of BW) and assigned to either of the following five treatment groups: (1) unchallenged control (UCC; n = 7), (2) challenged control (CC; n = 7), (3) AGP (CC + 0.1% AGP; n = 7), (4) Ferm1 (challenged and fed homofermentative Lactobacillus plantarum (Homo)-fermented barley; n = 8) and (5) Ferm2 (challenged and fed heterofermentative L. buchneri (Hetero)-fermented barley; n = 8). The control diet included unfermented barley. Barley was fermented with either Homo or Hetero for 90 days under anaerobic conditions. On day 10, all pigs except those in UCC group were orally inoculated with E. coli K88 + (6 × 109 colony forming units/ml). The pre-planned orthogonal test was performed to compare (1) UCC and CC, (2) CC and AGP, (3) CC and Ferm1 + Ferm2, as well as (4) Ferm1 and Ferm2. Challenged control pigs showed shorter (P < 0.05) villus height (VH) in the duodenum and deeper (P < 0.05) crypt depth (CD) in the jejunum than UCC pigs. The AGP group had higher (P < 0.05) VH and lower (P < 0.05) IL-6 gene expression in the jejunum compared with CC group. Compared to CC, Ferm1 and Ferm2 had decreased (P < 0.05) CD in the duodenum, IL-6 gene expression in the jejunum and rectal temperature at 24 h post-challenge. Pigs fed fermented barley diets showed greater (P < 0.05) faecal abundance of Clostridium Cluster IV and Lactobacilli than those fed UCC diet. Ferm2-fed pigs showed lower (P < 0.05) concentrations of band cells, eosinophils and lymphocytes at 6, 24 and 48 h after challenge, respectively, and lower (P < 0.05) faecal abundance of Enterobacteriaceae 24 h after challenge than the Ferm1-fed pigs. In conclusion, the substitution of unfermented barley with fermented barley in a nursery diet showed similar results as those shown by AGP supplementation in terms of enhancing the intestinal morphology and modulating faecal microbiota composition, as well as down-regulating the pro-inflammatory cytokines; therefore, fermented barley can be a possible nutritional strategy for managing nursery pigs fed diets without in-feed AGP.

Keywords

cytokineintestinal morphologygut healthgrowth performancemicrobiota
Type
Research Article
Information
animal , Volume 14 , Issue 1 , January 2020 , pp. 39 - 49
Copyright
© The Animal Consortium 2019 

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.)

References

Association of Official Analytical Chemists (AOAC) 2006. Official methods of analysis, 18th edition. Washington, DC. AOAC, Arlington, VA, USA.Google Scholar
Blumenreich, MS 1990. The white blood cell and differential count. In Clinical methods: the history, physical, laboratory examinations (ed. Walker, HK, Hall, WD and Hurst, JW), 3rd edition, pp. 724–727. Butterworth Publishers, Oxford, UK.Google ScholarPubMed
Broadway, PR, Carroll, JA, Burdick Sanchez, NC, Bass, BE and Frank, JW 2016. Supplementation of a Lactobacillus acidophilus fermentation product can attenuate the acute phase response following a lipopolysaccharide challenge in pigs. Journal of Animal Science 94, 144.Google Scholar
Canadian Council on Animal Care 2009. Guidelines on: the care and use of farm animals in research, teaching and testing. CCAC, Ottawa, ON, Canada.Google Scholar
Croxen, MA and Finlay, BB 2009. Molecular mechanisms of Escherichia coli pathogenicity. Nature Reviews Microbiology 8, 26.Google Scholar
Dibner, J and Buttin, P 2002. Use of organic acids as a model to study the impact of gut microflora on nutrition and metabolism. The Journal of Applied Poultry Research 11, 453–463.CrossRefGoogle Scholar
Dibner, JJ and Richards, JD 2005. Antibiotic growth promoters in agriculture: history and mode of action. Poultry Science 84, 634–643.CrossRefGoogle ScholarPubMed
Gadde, U, Kim, WH, Oh, ST and Lillehoj, HS 2017. Alternatives to antibiotics for maximizing growth performance and feed efficiency in poultry: a review. Animal Health Research Review 18, 26–45.CrossRefGoogle ScholarPubMed
Gaskins, HR, Collier, CT and Anderson, DB 2002. Antibiotics as growth promotants: mode of action. Animal Biotechnology 13, 29–42.CrossRefGoogle ScholarPubMed
Goering, HK and van Soest, PJ 1970. Forage fiber analyses (apparatus, reagents, procedures, and some applications) Agriculture Handbook No. 379. Agricultural Research Service, United States Department of Agriculture, Washington, DC, USA.Google Scholar
Harvey, RB, Anderson, RC, Genovese, KJ, Callaway, TR and Nisbet, DJ 2005. Use of competitive exclusion to control enterotoxigenic strains of Escherichia coli in weaned pigs. Journal of Animal Science 83, E44–E47.Google Scholar
Hasday, JD, Fairchild, KD and Shanholtz, C 2000. The role of fever in the infected host. Microbes and Infection 2, 1891–1904.CrossRefGoogle ScholarPubMed
Holzer, M, Mayrhuber, E, Danner, H and Braun, R 2003. The role of Lactobacillus buchneri in forage preservation. Trends in Biotechnology 21, 282–287.CrossRefGoogle ScholarPubMed
Jayaraman, B, Regassa, A, Htoo, JK and Nyachoti, CM 2017. Effects of dietary standardized ileal digestible tryptophan:lysine ratio on performance, plasma urea nitrogen, ileal histomorphology and immune responses in weaned pigs challenged with Escherichia coli K88. Livestock Science 203, 114–119.CrossRefGoogle Scholar
Kiarie, E, Bhandari, S, Scott, M, Krause, DO and Nyachoti, CM 2011. Growth performance and gastrointestinal microbial ecology responses of piglets receiving Saccharomyces cerevisiae fermentation products after an oral challenge with Escherichia coli (K88). Journal of Animal Science 89, 1062–1078.CrossRefGoogle Scholar
Konstantinov, SR, Smidt, H, Akkermans, ADL, Casini, L, Trevisi, P, Mazzoni, M, De Filippi, S, Bosi, P and De Vos, WM 2008. Feeding of Lactobacillus sobrius reduces Escherichia coli F4 levels in the gut and promotes growth of infected piglets. FEMS Microbiology Ecology 66, 599–607.CrossRefGoogle ScholarPubMed
Koo, B, Bustamante-Garcia, D and Nyachoti, C 2018a. 353 Effects of Lactobacillus-fermented barley on intestinal morphology, cytokine gene expression, and fecal microbiota in weaned pigs challenged with Escherichia coli K88 +. Journal of Animal Science 96, 176–176.CrossRefGoogle Scholar
Koo, B, Bustamante-García, D and Nyachoti, CM 2018b. Energy content and nutrient digestibility of diets containing Lactobacillus-fermented barley or wheat fed to weaned pigs. Journal of Animal Science 96, 4802–4811.CrossRefGoogle ScholarPubMed
Koo, B, Kim, JW and Nyachoti, CM 2018c. Nutrient and energy digestibility, and microbial metabolites in weaned pigs fed diets containing Lactobacillus-fermented wheat. Animal Feed Science and Technology 241, 27–37.CrossRefGoogle Scholar
Lallès, J-P, Boudry, G, Favier, C, Floc’h, NL, Luron, I, Montagne, L, Oswald, IP, Pié, S, Piel, C and Sève, B 2004. Gut function and dysfunction in young pigs: physiology. Animal Research 53, 301–316.CrossRefGoogle Scholar
Le, MHA, Galle, S, Yang, Y, Landero, JL, Beltranena, E, Gänzle, MG and Zijlstra, RT 2016. Effects of feeding fermented wheat with Lactobacillus reuteri on gut morphology, intestinal fermentation, nutrient digestibility, and growth performance in weaned pigs. Journal of Animal Science 94, 4677–4687.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Liu, H, Zhang, J, Zhang, S, Yang, F, Thacker, PA, Zhang, G, Qiao, S and Ma, X 2014. Oral Administration of Lactobacillus fermentum I5007 favors intestinal development and alters the intestinal microbiota in formula-fed piglets. Journal of Agricultural and Food Chemistry 62, 860–866.Google ScholarPubMed
Livak, KJ and Schmittgen, TD 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.CrossRefGoogle Scholar
Loh, TC, Thanh, NT, Foo, HL, Hair-Bejo, M and Azhar, BK 2010. Feeding of different levels of metabolite combinations produced by Lactobacillus plantarum on growth performance, fecal microflora, volatile fatty acids and villi height in broilers. Animal Science Journal 81, 205–214.CrossRefGoogle ScholarPubMed
National Center for Biotechnology Information 2018. Enterobacteriaceae family. Retrieved on 3 December 2018 from https://www.ncbi.nlm.nih.gov/Taxonomy/Browser Google Scholar
National Research Council 2012. Nutrient requirements of swine, 11th revised edition. National Academy Press, Washington, DC, USA.Google Scholar
Nyachoti, CM, Kiarie, E, Bhandari, SK, Zhang, G and Krause, DO 2012. Weaned pig responses to Escherichia coli K88 oral challenge when receiving a lysozyme supplement. Journal of Animal Science 90, 252–260.CrossRefGoogle ScholarPubMed
Scholten, RHJ, van der Peet-Schwering, CMC, den Hartog, LA, Balk, M, Schrama, JW and Verstegen, MWA 2002. Fermented wheat in liquid diets: effects on gastrointestinal characteristics in weanling piglets. Journal of Animal Science 80, 1179–1186.CrossRefGoogle ScholarPubMed
Scholten, RHJ, van der Peet-Schwering, CMC, Verstegen, MWA, den Hartog, LA, Schrama, JW and Vesseur, PC 1999. Fermented co-products and fermented compound diets for pigs: a review. Animal Feed Science and Technology 82, 1–19.CrossRefGoogle Scholar
Urlings, HAP, Mug, AJ, van ‘t Klooster, AT, Bijker, PGH, van Logtestijn, JG and van Gils, LGM 1993. Microbial and nutritional aspects of feeding fermented feed (poultry by-products) to pigs. Veterinary Quarterly 15, 146–151.CrossRefGoogle Scholar
van Winsen, RL, Urlings, BAP, Lipman, LJA, Snijders, JMA, Keuzenkamp, D, Verheijden, JHM and van Knapen, F 2001. Effect of fermented feed on the microbial population of the gastrointestinal tracts of pigs. Applied and Environmental Microbiology 67, 3071–3076.CrossRefGoogle ScholarPubMed
Waititu, SM, Yin, F, Patterson, R, Rodriguez-Lecompte, JC and Nyachoti, CM 2016. Short-term effect of supplemental yeast extract without or with feed enzymes on growth performance, immune status and gut structure of weaned pigs challenged with Escherichia coli lipopolysaccharide. Journal of Animal Science and Biotechnology 7, 64.CrossRefGoogle ScholarPubMed
Waititu, SM, Yin, F, Patterson, R, Yitbarek, A, Rodriguez-Lecompte, JC and Nyachoti, CM 2017. Dietary supplementation with a nucleotide-rich yeast extract modulates gut immune response and microflora in weaned pigs in response to a sanitary challenge. Animal 11, 2156–2164.CrossRefGoogle ScholarPubMed
Wu, S, Zhang, F, Huang, Z, Liu, H, Xie, C, Zhang, J, Thacker, PA and Qiao, S 2012. Effects of the antimicrobial peptide cecropin AD on performance and intestinal health in weaned piglets challenged with Escherichia coli . Peptides 35, 225–230.CrossRefGoogle ScholarPubMed
Xie, Z, Hu, L, Li, Y, Geng, S, Cheng, S, Fu, X, Zhao, S and Han, X 2017. Changes of gut microbiota structure and morphology in weaned piglets treated with fresh fermented soybean meal. World Journal of Microbiology and Biotechnology 33, 213.CrossRefGoogle ScholarPubMed
Supplementary material: File

Koo et al. supplementary material

Koo et al. supplementary material 1

Download Koo et al. supplementary material(File)
File 63 KB