Effects of dietary protein level and zinc oxide supplementation on performance responses and gastrointestinal tract characteristics in weaner pigs challenged with an enterotoxigenic strain of Escherichia coli
J. M. Heo A , J. C. Kim B , C. F. Hansen A C , B. P. Mullan B , D. J. Hampson A and J. R. Pluske A DA Animal Research Institute, School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, WA 6150, Australia.
B Animal Research and Development, Department of Agriculture and Food, Locked Bag Number 4, Bentley Delivery Centre, WA 6983, Australia.
C Department of Large Animal Sciences, Faculty of Life Sciences, University of Copenhagen, Groennegaardsvej 2, DK-1870 Frederiksberg C, Denmark.
D Corresponding author. Email: j.pluske@murdoch.edu.au
Animal Production Science 50(9) 827-836 https://doi.org/10.1071/AN10058
Submitted: 6 April 2010 Accepted: 30 June 2010 Published: 29 September 2010
Abstract
The interactive effects of dietary protein level, zinc oxide (ZnO) supplementation and infection with an enterotoxigenic strain of Escherichia coli (ETEC) on performance responses and gastrointestinal tract characteristics were examined. Ninety-six individually housed, 21-day-old pigs (1 : 1 gender ratio) with initial bodyweight (BW) of 7.2 ± 0.69 kg, were used in a split plot experiment, with the whole plot being challenge or no challenge with ETEC and the dietary treatments used as subplots and arranged in a completely randomised 2 × 2 factorial design, with the factors being (i) two dietary protein levels (251 versus 192 g/kg crude protein) and (ii) addition or no addition of 2.5 g/kg ZnO. No antibiotic was added to the diet. The ETEC infection decreased average daily gain (P < 0.001) and increased feed conversion ratio (P < 0.01). Protein level had no effect on performance of pigs while ZnO supplementation increased (P < 0.001) average daily gain and average daily feed intake and hence decreased feed conversion ratio (P < 0.001). There were no 2- or 3-way interactions for growth performance indices (P > 0.05). Feeding a lower protein diet did not influence (P > 0.05) faecal volatile fatty acid concentrations. In non-infected pigs, feeding a lower protein diet caused a lower pH in the jejunum and ileum compared with pigs fed a higher protein diet (P < 0.05 and P < 0.01, respectively). However, feeding ZnO-supplemented diets increased (P < 0.05) the pH in the stomach and caecum compared with feeding diets without ZnO supplementation. Protein level did not alter (P > 0.05) empty BW but dietary supplementation with ZnO increased empty BW (P < 0.05). Neither protein level nor ZnO supplementation modified small intestinal morphology, although a tendency for an interaction (P < 0.1) was detected for jejunal villous height between protein level and ZnO supplementation. The results indicate that feeding ZnO-supplemented diets improved pig performance, and feeding a lower protein diet without ZnO supplementation did not compromise performance nor modify measures of gastrointestinal tract structure and function compared with pigs fed a diet higher in protein after weaning.
Additional keywords: growth performance, post-weaning diarrhoea.
Acknowledgements
The authors thank Mr Bob Davis, Mr Richard Seaward, Ms Josie Mansfield, Ms Aracely Hernandez and Ms Danka Halas for technical assistance. This research was supported by an Australian Research Council-Linkage Grant, with Danish Pig Production, the Department of Agriculture and Food of Western Australia, and Wandalup Farms Ltd, as the industry partners. Evonik Degussa kindly donated the isoleucine and valine.
Bikker P,
Dirkzwager A,
Fledderus J,
Trevisi P,
le Huerou-Luron I,
Lalles JP, Awati A
(2006) The effect of dietary protein and fermentable carbohydrates levels on growth performance and intestinal characteristics in newly weaned piglets. Journal of Animal Science 84, 3337–3345.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Brannon PM
(1990) Adaptation of the exocrine pancreas to diet. Annual Review of Nutrition 10, 85–105.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Carlson D,
Poulsen HD, Vestergaard M
(2004) Additional dietary zinc for weaning piglets is associated with elevated concentrations of serum IGF-I. Journal of Animal Physiology and Animal Nutrition 88, 332–339.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Carlson MS,
Hill GM, Link JE
(1999) Early- and traditionally weaned nursery pigs benefit from phase-feeding pharmacological concentrations of zinc oxide: effect on metallothionein and mineral concentrations. Journal of Animal Science 77, 1199–1207.
|
CAS |
PubMed |
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.
|
CAS |
PubMed |
Chung TK, Baker DH
(1992) Ideal amino acid pattern for 10-kilogram pigs. Journal of Animal Science 70, 3102–3111.
|
CAS |
PubMed |
Halas D,
Heo JM,
Hansen CF,
Kim JC,
Hampson DJ,
Mullan BP, Pluske JR
(2007) Organic acids, prebiotics and protein level as dietary tools to control the weaning transition and reduce post-weaning diarrhoea in piglets. CAB Reviews: Perspectives in Agriculture, Veterinary Science. Nutrition and Natural Resources 2(079), 13.
Hara H,
Hashimoto N,
Akatsuka N, Kasai T
(2000) Induction of pancreatic trypsin by dietary amino acids in rats: four trypsinogen isozymes and cholecystokinin messenger RNA. The Journal of Nutritional Biochemistry 11, 52–59.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Heo JM,
Kim JC,
Hansen CF,
Mullan BP,
Hampson DJ, Pluske JR
(2008) Effects of feeding low protein diets to piglets on plasma urea nitrogen, faecal ammonia nitrogen, the incidence of diarrhoea and performance after weaning. Archives of Animal Nutrition 62, 343–358.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
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 postweaning diarrhea in weaned pigs challenged with an enterotoxigenic strain of Escherichia coli. Journal of Animal Science 87, 2833–2843.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Heo JM,
Kim JC,
Hansen CF,
Mullan BP,
Hampson DJ,
Maribo H,
Kjeldsen N, Pluske JR
(2010) Effects of dietary protein level and zinc oxide supplementation on the incidence of post-weaning diarrhoea in weaner pigs challenged with an enterotoxigenic strain of Escherichia coli. Livestock Science ,
| Crossref | GoogleScholarGoogle 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 or without the inclusion of an antibacterial agent on nursery pig performance. Journal of Animal Science 79, 934–941.
|
CAS |
PubMed |
Hoque KM,
Rajendran VM, Binder HJ
(2005) Zinc inhibits cAMP-stimulated Cl secretion via basolateral K-channel blockade in rat ileum. American Journal of Physiology. Gastrointestinal and Liver Physiology 288, G956–G963.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Htoo JK,
Araiza BA,
Sauer WC,
Rademacher M,
Zhang Y,
Cervantes M, Zijlstra RT
(2007) Effect of dietary protein content on ileal amino acid digestibility, growth performance, and formation of microbial metabolites in ileal and cecal digesta of early-weaned pigs. Journal of Animal Science 85, 3303–3312.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Huang SX,
McFall M,
Cegielski AC, Kirkwood RN
(1999) Effect of dietary zinc supplementation on Escherichia coli septicaemia in weaned pigs. Swine Health and Production 7, 109–111.
Huguet A,
Savary G,
Bobillier E,
Lebreton Y, Huerou-Luron Il
(2006) Effects of level of feed intake on pancreatic exocrine secretions during the early postweaning period in piglets. Journal of Animal Science 84, 2965–2972.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Le Bellego L, Noblet J
(2002) Performance and utilization of dietary energy and amino acids in piglets fed low protein diets. Livestock Production Science 76, 45–58.
| Crossref | GoogleScholarGoogle Scholar |
Le Bellego L,
Van Milgen J, Noblet J
(2002) Effect of high temperature and low-protein diets on the performance of growing-finishing pigs. Journal of Animal Science 80, 691–701.
|
CAS |
PubMed |
Li XL,
Yin JD,
Li DF,
Chen XJ,
Zang JJ, Zhou X
(2006) Dietary supplementation with zinc oxide increases IGF-I and IGF-I receptor gene expression in the small intestine of weanling piglets. The Journal of Nutrition 136, 1786–1791.
|
CAS |
PubMed |
Lordelo MM,
Gaspar AM,
Le Bellego L, Freire JPB
(2008) Isoleucine and valine supplementation of a low-protein corn-wheat-soybean meal-based diet for piglets: growth performance and nitrogen balance. Journal of Animal Science 86, 2936–2941.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Macfarlane GT,
Gibson GR,
Beatty E, Cummings JH
(1992) Estimation of short-chain fatty acid production from protein by human intestinal bacteria based on branched-chain fatty acid measurements. FEMS Microbiology Ecology 101, 81–88.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Mavromichalis I,
Peter CM,
Parr TM,
Ganessunker D, Baker DH
(2000) Growth-promoting efficacy 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.
|
CAS |
PubMed |
McDonald DE,
Pethick DW,
Mullan BP, Hampson DJ
(2001) Increasing viscosity of the intestinal contents alters small intestinal structure and intestinal growth, and stimulates proliferation of enterotoxigenic Escherichia coli in newly-weaned pigs. The British Journal of Nutrition 86, 487–498.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Montagne L,
Cavaney FS,
Hampson DJ,
Lalles JP, Pluske JR
(2004) Effect of diet composition on postweaning colibacillosis in piglets. Journal of Animal Science 82, 2364–2374.
|
CAS |
PubMed |
Nørgaard J, Fernández J
(2009) Isoleucine and valine supplementation of crude protein-reduced diets for pigs aged 5–8 weeks. Animal Feed Science and Technology 154, 248–253.
| Crossref | GoogleScholarGoogle Scholar |
Nunez MC,
Bueno JD,
Ayudarte MV,
Almendros A,
Rios A,
Suarez MD, Gil A
(1996) Dietary restriction induces biochemical and morphometric changes in the small intestine of nursing piglets. The Journal of Nutrition 126, 933–944.
|
CAS |
PubMed |
Nyachoti CM,
Omogbenigun FO,
Rademacher M, Blank G
(2006) Performance responses and indicators of gastrointestinal health in early-weaned pigs fed low-protein amino acid-supplemented diets. Journal of Animal Science 84, 125–134.
|
CAS |
Crossref |
PubMed |
Opapeju FO,
Rademacher M,
Blank G, Nyachoti CM
(2008) Effect of low-protein amino acid-supplemented diets on the growth performance, gut morphology, organ weights and digesta characteristics of weaned pigs. Animal 2, 1457–1464.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Opapeju FO,
Krause DO,
Payne RL,
Rademacher M, Nyachoti CM
(2009) Effect of dietary protein level on growth performance, indicators of enteric health, and gastrointestinal microbial ecology of weaned pigs induced with postweaning colibacillosis. Journal of Animal Science 87, 2635–2643.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Owusu-Asiedu A,
Nyachoti CM,
Baidoo SK,
Marquardt RR, Yang X
(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. Journal of Animal Science 81, 1781–1789.
|
CAS |
PubMed |
Partanen KH, Mroz Z
(1999) Organic acids for performance enhancement in pig diets. Nutrition Research Reviews 12, 117–145.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Pluske JR,
Williams IH, Aherne FX
(1996) Villous height and crypt depth in piglets in response to increases in the intake of cows’ milk after weaning. Animal Science 62, 145–158.
| Crossref |
Pluske JR,
Hampson DJ, Williams IH
(1997) Factors influencing the structure and function of the small intestine in the weaned pig: a review. Livestock Production Science 51, 215–236.
| Crossref | GoogleScholarGoogle Scholar |
Poulsen HD
(1995) Zinc oxide for weanling piglets. Acta Agriculturae Scandinavica, Section A
Animal Science 45, 159–167.
|
CAS |
Rodriguez P,
Darmon N,
Chappuis P,
Candalh C,
Blaton MA,
Bouchaud C, Heyman M
(1996) Intestinal paracellular permeability during malnutrition in guinea pigs: effect of high dietary zinc. Gut 39, 416–422.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Roselli M,
Finamore A,
Garaguso I,
Britti MS, Mengheri E
(2003) Zinc oxide protects cultured enterocytes from the damage induced by Escherichia coli. The Journal of Nutrition 133, 4077–4082.
|
CAS |
PubMed |
Sturniolo GC,
Fries W,
Mazzon E,
Di Leo V,
Barollo M, D’Inca R
(2002) Effect of zinc supplementation on intestinal permeability in experimental colitis. The Journal of Laboratory and Clinical Medicine 139, 311–315.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Van Beers-Schreurs HM,
Nabuurs MJ,
Vellenga L,
Kalsbeek-van der Valk HJ,
Wensing T, Breukink HJ
(1998) Weaning and the weanling diet influence the villous height and crypt depth in the small intestine of pigs and alter the concentrations of short-chain fatty acids in the large intestine and blood. The Journal of Nutrition 128, 947–953.
|
CAS |
PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Wellock IJ,
Fortomaris PD,
Houdijk JGM, Kyriazakis I
(2008) Effects of dietary protein supply, weaning age and experimental enterotoxigenic Escherichia coli infection on newly weaned pigs: health. Animal 2, 834–842.
|
CAS |
Williams BA,
Verstegen MWA, Tamminga S
(2001) Fermentation in the large intestine of single-stomached animals and its relationship to animal health. Nutrition Research Reviews 14, 207–227.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Yue LY, Qiao SY
(2008) Effects of low-protein diets supplemented with crystalline amino acids on performance and intestinal development in piglets over the first 2 weeks after weaning. Livestock Science 115, 144–152.
| Crossref | GoogleScholarGoogle Scholar |
Zhang BK, Guo YM
(2007) Beneficial effects of tetrabasic zinc chloride for weanling piglets and the bioavailability of zinc in tetrabasic form relative to ZnO. Animal Feed Science and Technology 135, 75–85.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Zhang BK, Guo YM
(2008) The growth-promoting effect of tetrabasic zinc chloride is associated with elevated concentration of growth hormone and ghrelin. Asian-Australasian Journal of Animal Sciences 21, 1473–1478.
|
CAS |
Zhang B, Guo Y
(2009) Supplemental zinc reduced intestinal permeability by enhancing occludin and zonula occludens protein-1 (ZO-1) expression in weaning piglets. The British Journal of Nutrition 102, 687–693.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Zheng CT,
Li DF,
Qiao SY,
Gong LM,
Zhang DF,
Thacker P, Han IK
(2001) Effects of isoleucine supplementation of a low protein, corn-soybean meal diet on the performance and immune function of weanling pigs. Asian-Australasian Journal of Animal Sciences 14, 70–76.
|
CAS |