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Effect of rearing environment and dietary zinc oxide on the response of group-housed weaned pigs to enterotoxigenic Escherichia coli O149 challenge

Published online by Cambridge University Press:  11 March 2011

R. D. Slade ,
I. Kyriazakis ,
S. M. Carroll ,
F. H. Reynolds ,
I. J. Wellock ,
L. J. Broom  and
H. M. Miller
R. D. Slade
Affiliation:
Faculty of Biological Sciences, Institute of Integrative and Comparative Biology, University of Leeds, Leeds LS2 9JT, UK
I. Kyriazakis
Affiliation:
School of Agriculture, Food and Rural Development, Newcastle University, Newcastle upon Tyne NE1 7RU, UK
S. M. Carroll
Affiliation:
Faculty of Biological Sciences, Institute of Integrative and Comparative Biology, University of Leeds, Leeds LS2 9JT, UK
F. H. Reynolds
Affiliation:
Faculty of Biological Sciences, Institute of Integrative and Comparative Biology, University of Leeds, Leeds LS2 9JT, UK
I. J. Wellock
Affiliation:
ABN Ltd, ABN House, Oundle Road, Peterborough PE2 9PW, UK
L. J. Broom*
Affiliation:
Faculty of Biological Sciences, Institute of Integrative and Comparative Biology, University of Leeds, Leeds LS2 9JT, UK
H. M. Miller
Affiliation:
Faculty of Biological Sciences, Institute of Integrative and Comparative Biology, University of Leeds, Leeds LS2 9JT, UK
*
†E-mail: l.j.broom@leeds.ac.uk
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Abstract

A 2 × 2 factorial experiment was conducted to determine the effects of rearing environment (indoor (In) v. outdoor (Out)) and dietary zinc oxide (ZnO) supplementation (0 (−Zn) v. 3100 (+Zn) mg/kg feed) on the response of weaned pigs to a challenge infection with enterotoxigenic Escherichia coli (ETEC). Pigs from the two rearing environments were weaned onto trial diets at 4 weeks of age, moved into conventional accommodation and infected 3 days later with 109 CFU ETEC per os. Faecal ETEC shedding was determined before and after challenge. After 7 days of ETEC infection, all pigs were euthanized for gut lactic acid bacteria (LAB)-to-coliform ratio, pH and small intestine morphological measurements. Both ZnO and outdoor rearing reduced ETEC excretion, and these effects were additive. Outdoor rearing increased small intestine and colon tissue weight. ZnO increased villus height and goblet cell number in the upper small intestine, LAB-to-coliform ratio (through reduced coliforms) in the lower small intestine and proximal colon, and improved growth performance. There were interactive effects of rearing environment and ZnO supplementation on upper small intestine villus height and daily gain, as outdoor rearing conferred advantages on these variables only with ZnO dietary supplementation. Daily gains were 233, 174, 277 and 347 (s.e.m. 27.2) g/day for the In − Zn, Out − Zn, In + Zn and Out + Zn, respectively. These results suggest different, but complementary mechanisms of intestinal health and performance in outdoor-reared pigs and those offered ZnO supplemented diets. The results indicate that the benefits of ZnO to the weaned pig extend beyond suppression of ETEC and appear mediated through altered development of the small intestine mucosa.

Keywords

Escherichia colipigintestinal morphologyzinc oxiderearing environment
Type
Full Paper
Information
animal , Volume 5 , Issue 8 , August 2011 , pp. 1170 - 1178
Copyright
Copyright © The Animal Consortium 2011

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References

Blomberg, L, Krivan, HC, Cohen, PS, Conway, PL 1993. Piglet ileal mucus contains protein and glycolipid (galactosylceramide) receptors specific for Escherichia coli K88 fimbriae. Infection and Immunity 61, 2526–2531.CrossRefGoogle ScholarPubMed
Blomberg, L, Gustafsson, L, Cohen, PS, Conway, PL, Blomberg, A 1995. Growth of Escherichia coli K88 in piglet ileal mucosa: protein expression as an indicator of type of metabolism. Journal of Bacteriology 177, 6695–6703.CrossRefGoogle Scholar
Carlson, D, Poulsen, HD, Vestergaard, M 2004. Additional dietary zinc for weaning piglets is associated with elevated concentrations of serum IGF-1. Journal of Animal Physiology and Animal Nutrition 88, 332–339.CrossRefGoogle Scholar
Case, CL, Carlson, MS 2002. Effect of feeding organic and inorganic sources of additional zinc on growth performance and zinc balance in nursery pigs. Journal of Animal Science 80, 1917–1924.CrossRefGoogle ScholarPubMed
Crane, JK, Naeher, TM, Shulgina, I, Zhu, C, Boedeker, EC 2007. Effect of zinc in enteropathogenic Escherichia coli infection. Infection and Immunity 75, 5974–5984.CrossRefGoogle ScholarPubMed
Dean-Nystrom, EA, Samuel, JE 1994. Age related resistance to 987P fimbria mediated colonization correlates with specific glycolipid receptors in intestinal mucus in swine. Infection and Immunity 62, 4789–4794.CrossRefGoogle ScholarPubMed
Gentry, JG, McGlone, JJ, Miller, MF, Blanton, JR 2002. Diverse birth and rearing environment effects on pig growth and meat quality. Journal of Animal Science 80, 1707–1715.CrossRefGoogle ScholarPubMed
Hahn, JD, Baker, DH 1993. Growth and plasma zinc responses of young pigs fed pharmacological levels of zinc. Journal of Animal Science 71, 3020–3024.CrossRefGoogle ScholarPubMed
Hampson, DJ 1986. Attempts to modify changes in the piglet small intestine after weaning. Research in Veterinary Science 40, 313–317.CrossRefGoogle ScholarPubMed
Hedemann, MS, Jensen, BB, Poulsen, HD 2006. Influence of dietary zinc and copper on digestive enzyme activity and intestinal morphology in weaned pigs. Journal of Animal Science 84, 3310–3320.CrossRefGoogle ScholarPubMed
Heo, JM, Kim, JC, Hansen, CF, Mullan, BP, Hampson, DJ, Pluske, JR 2009. Feeding a diet with decreased protein content reduces indices of protein fermentation and the incidence of post weaning diarrhea in weaned pigs challenged with an enterotoxigenic strain of Escherichia coli. Journal of Animal Science 87, 2833–2843.CrossRefGoogle Scholar
Hill, GM, Mahan, DC, Carter, SD, Cromwell, GL, Ewan, RC, Harrold, RL, Lewis, AJ, Miller, PS, Shurson, GC, Veum, TL 2001. Effect of pharmacological concentrations of zinc oxide with and without the inclusion of an antibacterial agent on nursery pig performance. Journal of Animal Science 79, 934–941.CrossRefGoogle ScholarPubMed
Hojberg, O, Canibe, N, Poulsen, HD, Hedemann, MS, Jensen, BB 2005. Influence of dietary zinc oxide and copper sulfate on the gastrointestinal ecosystem in newly weaned piglets. Applied and Environmental Microbiology 71, 2267–2277.CrossRefGoogle ScholarPubMed
Ilsley, SE, Miller, HM, Kamel, C 2005. Effects of dietary quillaja saponin and curcumin on the performance and immune status of weaned piglets. Journal of Animal Science 83, 82–88.CrossRefGoogle ScholarPubMed
Jin, LZ, Marquardt, RR, Baidoo, SK 2000. Inhibition of enterotoxigenic Escherichia coli K88, K99 and 987P by the Lactobacillus isolates from porcine intestine. Journal of the Science of Food and Agriculture 80, 619–624.3.0.CO;2-7>CrossRefGoogle Scholar
Katouli, M, Melin, L, Jensen-Waern, M, Wallgren, P, Mollby, R 1999. The effect of zinc oxide on the stability of the intestinal flora with special reference to composition of coliforms in weaned pigs. Journal of Applied Microbiology 87, 564–573.CrossRefGoogle ScholarPubMed
Kelly, D, King, TP 2001. Digestive physiology and development in pigs. In The weaner pig: nutrition and management (ed. MA Varley and J Wiseman), pp. 179–206. CABI Publishing, UK.Google Scholar
Kelly, D, Begbie, R, King, TP 1992. Postnatal intestinal development. In Neonatal survival and growth (ed. MA Varley, PEV Williams and TLJ Lawrence), pp. 63–79. British Society of Animal Production – Occasional Publication no. 15, UK.Google Scholar
Kyriazakis, I, Houdijk, JGM 2007. Food intake and performance of pigs during health, disease and recovery. In Paradigms in pig science (ed. J Wiseman, MA Varley, S McOrist and B Kemp), pp. 493–513. Nottingham University Press, Nottingham, UK.Google Scholar
Li, BT, Van Kessel, AG, Caine, WR, Huang, SX, Kirkwood, RN 2001. Small intestinal morphology and bacterial populations in the ileal digesta and feces of newly weaned pigs receiving a high dietary level of zinc oxide. Canadian Journal of Animal Science 81, 511–516.CrossRefGoogle Scholar
Li, XL, Yin, JD, Li, DF, Chen, XJ, Zang, JJ, Zhou, X 2006. Dietary supplementation with zinc oxide increases IGF-1 and IGF-1 receptor gene expression in the small intestine of the weanling piglets. Journal of Nutrition 136, 1786–1791.CrossRefGoogle ScholarPubMed
Madec, F, Bridoux, N, Bounaix, S, Cariolet, R, Duval-Iflah, Y, Hampson, DJ, Jestin, A 2000. Experimental models of porcine post-weaning colibacillosis and their relationship to post-weaning diarrhoea and digestive disorders as encountered in the field. Veterinary Microbiology 72, 295–310.CrossRefGoogle ScholarPubMed
Mavromichalis, I, Peter, CM, Parr, TM, Ganessunker, D, Baker, DH 2000. Growth-promoting efficiency in young pigs of two sources of zinc oxide having either a high or low bioavailability of zinc. Journal of Animal Science 78, 2896–2902.CrossRefGoogle ScholarPubMed
Miller, HM, Toplis, P, Slade, RD 2009. Can outdoor rearing and increased weaning age compensate for the removal of in-feed antibiotic growth promoters and zinc oxide? Livestock Science 125, 121–131.CrossRefGoogle Scholar
Miller, BG, Newby, TJ, Stokes, CR, Bourne, FJ 1984. Influence of diet on post-weaning malabsorption and diarrhoea in the pig. Research in Veterinary Science 36, 187–193.CrossRefGoogle ScholarPubMed
Miller, HM, Carroll, SM, Reynolds, FH, Slade, RD 2007. Effect of rearing environment and age on gut development of piglets at weaning. Livestock Science 108, 124–127.CrossRefGoogle Scholar
Mulder, IE, Schmidt, B, Stokes, CR, Lewis, M, Bailey, M, Aminov, RI, Prosser, JI, Gill, BP, Pluske, JR, Mayer, CD, Musk, CC, Kelly, D 2009. Environmentally-acquired bacteria influence microbial diversity and natural innate immune responses at gut surfaces. BMC Biology 7, 79.CrossRefGoogle ScholarPubMed
Owusu-Asiedu, A, Nyachoti, CM, Marquardt, RR 2003. Response of early weaned pigs to an enterotoxigenic Escherichia coli (K88) challenge when fed diets containing spray-dried porcine plasma or pea protein isolate plus egg yolk antibody, zinc oxide, fumaric acid, or antibiotic. Journal of Animal Science 81, 1790–1798.CrossRefGoogle ScholarPubMed
Ragland, D, Schneider, JR, Amas, SF, Hill, M 2006. Alternatives to the use of antimicrobial feed additives in nursery diets: a pilot study. Journal of Swine Health and Production 14, 82–88.Google Scholar
Roselli, M, Finamore, A, Garaguso, I, Britti, MS, Mengheri, E 2003. Zinc oxide protects cultured enterocytes from the damage induced by Escherichia coli. Journal of Nutrition 133, 4077–4082.CrossRefGoogle ScholarPubMed
Tarnow, P, Argen, M, Steenfos, H, Jansson, JO 1994. Topical zinc oxide treatment increases endogenous gene expression of insulin-like growth factor-1 in granulation tissue from porcine wounds. Scandinavian Journal of Plastic and Reconstructive Surgery 28, 255–259.CrossRefGoogle ScholarPubMed
Van Dijk, AJ, Enthoven, PMM, Van den Hoven, SGC, Van Laarhoven, MMMH, Niewold, TA, Nabuurs, MJA, Benyen, AC 2002. The effect of dietary spray-dried porcine plasma on clinical response in weaned piglets challenged with a pathogenic Escherichia coli. Veterinary Microbiology 84, 207–218.CrossRefGoogle ScholarPubMed
Vente-Spreeuwenberg, MAM, Beynen, AC 2003. Diet modulation of small intestine integrity in weaned piglets. In Weaning the pig: concepts and consequences (ed. JR Pluske, J Le Dividich and MWA Verstegen), pp. 145–198. Wageningen Academic Publishers, The Netherlands.Google Scholar
Wellock, IJ, Fortomaris, PD, Houdijk, JGM, Kyriazakis, I 2006. The effect of dietary protein supply on the performance and risk of post-weaning enteric disorders in newly weaned pigs. Animal Science 82, 327–335.CrossRefGoogle Scholar
Wellock, IJ, Fortomaris, PD, Houdijk, JGM, Kyriazakis, I 2008a. The interaction between dietary protein supply, weaning age and enterotoxigenic Escherichia coli infection on the performance and health of newly weaned pigs: performance. Animal 2, 834–842.CrossRefGoogle Scholar
Wellock, IJ, Fortomaris, PD, Houdijk, JGM, Kyriazakis, I 2008b. The interaction between dietary protein supply, weaning age and enterotoxigenic Escherichia coli infection on the performance and health of newly weaned pigs: health. Animal 2, 825–833.CrossRefGoogle Scholar
Wulbers-Mindermann, M, Algers, B, Berg, C, Lundeheim, N, Sigvardsson, J 2002. Primiparous and multiparous maternal ability in sows in relation to indoor and outdoor farrowing systems. Livestock Production Science 73, 285–297.CrossRefGoogle Scholar