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

Volumn 87, Issue 9, 2009, Pages 2833-2843

  Heo, J M ^a   Kim, J C ^b   Hansen, C F ^a   Mullan, B P ^b   Hampson, D J ^a   Pluske, J R ^a  

^a MURDOCH UNIVERSITY   (Australia)

^b Bentley Delivery Centre   (Australia)

Author keywords

Escherichia coli; Infection; Low protein; Pig; Postweaning diarrhea; Production

Indexed keywords

AMMONIA; VOLATILE FATTY ACID;

ANIMAL; ANIMAL DISEASE; ARTICLE; BODY WEIGHT; CHEMISTRY; DIARRHEA; EATING; ENTEROTOXIGENIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; FECES; FEMALE; FERMENTATION; GROWTH, DEVELOPMENT AND AGING; INCIDENCE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PROTEIN INTAKE; PROTEIN RESTRICTION; SWINE; SWINE DISEASE; UREA NITROGEN BLOOD LEVEL; WEANING;

AMMONIA; ANIMALS; BLOOD UREA NITROGEN; BODY WEIGHT; DIARRHEA; DIET, PROTEIN-RESTRICTED; DIETARY PROTEINS; EATING; ENTEROTOXIGENIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; FATTY ACIDS, VOLATILE; FECES; FEMALE; FERMENTATION; INCIDENCE; SWINE; SWINE DISEASES; WEANING;

ESCHERICHIA COLI; SUIDAE;

EID: 70249133718     PISSN: 00218812     EISSN: 15253163     Source Type: Journal    
DOI: 10.2527/jas.2008-1274     Document Type: Article

References (59)

1. AOAC. 1997. Official Methods of Analysis. 16th ed. Assoc. Off. Anal. Chem., Washington, DC.
2. Awati, A., S. D'Urso, B. A. Williams, M. Bosch, and M. W. A. Verstegen. 2007. Changes in the fermentation end-product profile in the gut of piglets during post-colostrum suckling period. Livest. Sci. 108:156-158.
3. Bach Knudsen, K. E. 1997. Carbohydrate and lignin contents of plant materials used in animal feeding. Anim. Feed Sci. Technol. 67:319-338.
4. Ball, R. O., and F. X. Aherne. 1987. Influence of dietary nutrient density, level of feed intake and weaning age on young pigs. II. Apparent nutrient digestibility and incidence and severity of diarrhea. Can. J. Anim. Sci. 67:1105-1115.
5. Bikker, P., A. Dirkzwager, J. Fledderus, P. Trevisi, I. le Huerou-Luron, J. P. Lalles, and A. Awati. 2006. The effect of dietary protein and fermentable carbohydrates levels on growth performance and intestinal characteristics in newly weaned piglets. J. Anim. Sci. 84:3337-3345.
6. Callesen, J., D. Halas, F. Thorup, K. E. Bach Knudsen, J. C. Kim, B. P. Mullan, D. J. Hampson, R. H. Wilson, and J. R. Pluske. 2007. The effects of weaning age, diet composition, and categorisation of creep feed intake by piglets on diarrhoea and performance after weaning. Livest. Sci. 108:120-123.
7. Chen, H.-Y., P. S. Miller, A. J. Lewis, C. K. Wolverton, and W. W. Stroup. 1995. Changes in plasma urea concentration can be used to determine protein requirements of two populations of pigs with different protein accretion rates. J. Anim. Sci. 73:2631-2639.
8. Chung, T. K., and D. H. Baker. 1992. Ideal amino acid pattern for 10-kilogram pigs. J. Anim. Sci. 70:3102-3111.
9. Cohen, S. A. 2001. Amino acid analysis using precolumn derivatisation with 6-aminoquinolyl-n-hydroxysuccinimidyl carbamate. Pages 39-47 in Methods in Molecular Biology No. 159. C. Cooper, N. Packer, and K. Williams, ed. Humana Press, Totowa, NJ.
10. Coma, J., D. R. Zimmerman, and D. Carrion. 1995. Relationship of rate of lean tissue growth and other factors to concentration of urea in plasma of pigs. J. Anim. Sci. 73:3649-3656.
11. CSIRO. 2008. Model Code of Practice for the Welfare of Animals: Pigs. 3rd ed. CSIRO Publishing, Collingwood, Victoria, Australia.
12. Ding, M. X., Y. L. Wang, H. L. Zhu, and Z. H. Yuan. 2006. Effects of cyadox and olaquindox on intestinal mucosal immunity and on fecal shedding of Escherichia coli in piglets. J. Anim. Sci. 84:2367-2373.
13. Gaskins, H. R. 2001. Intestinal bacteria and their influence on swine growth. Pages 585-608 in Swine Nutrition. 2nd ed. A. J. Lewis and L. L. Southern, ed. CRC Press, Boca Raton, FL.
14. Hampson, D. J. 1994. Postweaning Escherichia coli diarrhoea in pigs. Pages 171-191 in Escherichia coli in domestic animals and humans. C. L. Gyles, ed. CAB Int., Wallingford, UK.
15. Hansen, J. A., D. A. Knabe, and K. G. Burgoon. 1993. Amino acid supplementation of low-protein sorghum-soybean meal diets for 5- to 20-kilogram swine. J. Anim. Sci. 71:452-458.
16. Heo, J. M., J. C. Kim, C. F. Hansen, B. P. Mullan, D. J. Hampson, and J. R. Pluske. 2008. Effects of feeding low protein diets on plasma urea nitrogen, faecal ammonia nitrogen, the incidence of diarrhoea and performance after weaning. Arch. Anim. Nutr. 62:343-358.
17. Högberg, A., and J. E. Lindberg. 2004. Influence of cereal non-starch polysaccharides and enzyme supplementation on digestion site and gut environment in weaned piglets. Anim. Feed Sci. Technol. 116:113-128.
18. Htoo, J. K., B. A. Araiza, W. C. Sauer, M. Rademacher, Y. Zhang, M. Cervantes, and R. T. Zijlstra. 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. J. Anim. Sci. 85:3303-3312.
19. Jeaurond, E. A., M. Rademacher, J. R. Pluske, C. H. Zhu, and C. F. M. de Lange. 2008. Impact of feeding fermentable proteins and carbohydrates on growth performance, gut health and gastrointestinal function of newly weaned pigs. Can. J. Anim. Sci. 88:271-281.
20. Jensen, B. B. 2001. Possible ways of modifying type and amount of products from microbial fermentation in the gut. Pages 181-200 in Gut Environment of Pigs. A. Piva, K. E. Bach Knudsen, and J.-E. Lindberg, ed. Nottingham Univ. Press, Nottingham, UK.
21. Kim, J. C., B. P. Mullan, H. D. J. Hampson, and J. R. Pluske. 2008. Addition of oat hulls to an extruded rice-based diet for weaner pigs ameliorates the incidence of diarrhoea and reduces indices of protein fermentation in the gastrointestinal tract. Br. J. Nutr. 99:1217-1225.
22. Le Bellego, L., and J. Noblet. 2002. Performance and utilization of dietary energy and amino acids in piglets fed low protein diets. Livest. Prod. Sci. 76:45-58.
23. Lin, H. C., and W. J. Visek. 1991. Colon mucosal cell damage by ammonia in rats. J. Nutr. 121:887-893.
24. Linder, M. C. 1991. Nutrition and metabolism of proteins. Pages 87-109 in Nutritional Biochemistry and Metabolism with Clinical Applications. 2nd ed. M. C. Linder, ed. Appleton & Lange, Stamford, CT.
25. Lordelo, M. M., A. M. Gaspar, L. Le Bellego, and J. P. B. Freire. 2008. Isoleucine and valine supplementation of a low-protein corn-wheat-soybean meal-based diet for piglets: Growth performance and nitrogen balance. J. Anim. Sci. 86:2936-2941.
26. Macfarlane, G. T., G. R. Gibson, E. Beatty, and J. H. Cummings. 1992. Estimation of short-chain fatty acid production from protein by human intestinal bacteria based on branched-chain fatty acid measurements. FEMS Microbiol. Ecol. 101:81-88.
27. Madec, F., N. Bridoux, S. Bounaix, R. Cariolet, Y. Duval-Iflah, D. J. Hampson, and A. Jestin. 2000. Experimental models of porcine post-weaning colibacillosis and their relationship to post-weaning diarrhoea and digestive disorders as encountered in the field. Vet. Microbiol. 72:295-310.
28. Marquardt, R. R., L. Z. Jin, J. W. Kim, L. Fang, A. A. Frohlich, and S. K. Baidoo. 1999. Passive protective effect of egg-yolk antibodies against enterotoxigenic Escherichia coli K88+ infection in neonatal and early-weaned piglets. FEMS Immunol. Med. Microbiol. 23:283-288.
29. Mateos, G. G., F. Martin, M. A. Latorre, B. Vicente, and R. Lazaro. 2006. Inclusion of oat hulls in diets for young pigs based on cooked maize or cooked rice. Anim. Sci. 82:57-63.
30. Mavromichalis, I., D. M. Webel, J. L. Emmert, R. L. Moser, and D. H. Baker. 1998. Limiting order of amino acids in a low protein corn-soybean meal-whey-based diet for nursery pigs. J. Anim. Sci. 76:2833-2837.
31. McDonald, D. E., D. W. Pethick, B. P. Mullan, and D. J. Hampson. 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. Br. J. Nutr. 86:487-498.
32. Montagne, L., F. S. Cavaney, D. J. Hampson, J. P. Lallès, and J. R. Pluske. 2004. Effect of diet composition on postweaning colibacillosis in piglets. J. Anim. Sci. 82:2364-2374.
33. Moughan, P. J. 1999. Protein metabolism in the growing pigs. Pages 299-331 in A Quantitative Biology of the Pig. I. Kyriazakis, ed. CAB Publ., Wallingford, Oxon, UK.
34. Nabuurs, M. J. 1995. Microbiological, structural and functional changes of the small intestine of the pigs at weaning. Pig News Inf. 16:393N-397N.
35. Nabuurs, M. J. 1998. Weaning piglets as a model for studying pathophysiology of diarrhoea. Vet. Q. 20:42-45.
36. Nabuurs, M. J. A., A. Hoogendoorn, E. J. van der Molen, and A. L. van Osta. 1993. Villus height and crypt depth in weaned pigs reared under various circumstances in The Netherlands. Res. Vet. Sci. 55:78-84.
37. Nousiainen, J. T. 1991. Comparative observations on selected probiotics and olaquindox as feed additives for piglets around weaning. 2. Effect on villous length and crypt depth in the jejunum, ileum, caecum and colon. J. Anim. Physiol. Anim. Nutr. (Berl.) 66:224-230.
38. NRC. 1998. Nutrient Requirements of Swine. 10th rev. ed. Natl. Acad. Press, Washington, DC.
39. Nyachoti, C. M., F. O. Omogbenigun, M. Rademacher, and G. Blank. 2006. Performance responses and indicators of gastrointestinal health in early-weaned pigs fed low-protein amino acid-supplemented diets. J. Anim. Sci. 84:125-134.
40. Osek, J. 1999. Prevalence of virulence factors of Escherichia coli strains isolated from diarrheic and healthy piglets after weaning. Vet. Microbiol. 68:209-217.
41. Owusu-Asiedu, A., C. M. Nyachoti, and R. R. Marquardt. 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. J. Anim. Sci. 81:1790-1798.
42. Payne, H. G., M. C. Brumm, M. D'Antuono, J. R. Pluske, I. H. Williams, K. L. Moore, and B. P. Mullan. 2006. Review of group size effects on the performance of growing pigs. CAB Rev. Perspec. Agric. Vet. Sci. Nutr. Natur. Resour. 1, No. 012, 22pp.
43. Piva, A., A., E. Panciroli, Meola, and A. Formigoni. 1996. Lactitol enhances short-chain fatty acid and gas production by swine cecal microflora to a great extent when fermenting low rather than high fibre diets. J. Nutr. 126:280-289.
44. Pluske, J. R., J.-C. Kim, D. E. McDonald, D. W. Pethick, and D. J. Hampson. 2001. Non-starch polysaccharides in the diets of young weaned piglets. Pages 81-112 in The Weaner Pig. M. A. Varley and J. Wiseman, ed. CAB Int., Wallingford, UK.
45. Pluske, J. R., D. W. Pethick, D. E. Hopwood, and D. J. Hampson. 2002. Nutritional influences on some major enteric bacterial diseases of pigs. Nutr. Res. Rev. 15:333-371.
46. Reid, C.-A., and K. Hillman. 1999. The effects of retrogradation and amylose/amylopectin ratio of starches on carbohydrate fermentation and microbial populations in the porcine colon. Anim. Sci. 68:503-510.
47. Sauvant, D., J.-M. Perez, and G. Tran. 2004. Tables of composition and nutritional value of feed materials. Wageningen Acad. Publ., Wageningen, UK.
48. Schierack, P., H. Steinruck, S. Kleta, and W. Vahjen. 2006. Virulence factor gene profiles of Escherichia coli isolates from clinically healthy pigs. Appl. Environ. Microbiol. 72:6680-6686.
49. Stahly, T. 1996. Impact of immune system activation on growth and optimal dietary regimens of pigs. Pages 197-206 in Recent Advances in Animal Nutrition. P. C. Garnsworthy, J. Wiseman, and W. Haresign, ed. Nottingham Univ. Press, Nottingham, UK.
50. Stilwell, G. G., C. R. de Carvalho, M. S. Lima, and D. M. Broom. 2008. The effect of duration of manual restraint during blood sampling on plasma cortisol levels in calves. Anim. Welf. 17:383-385.
51. van der Klis, J. D., and A. J. M. Jansman. 2002. Optimising nutrient digestion, absorption and gut barrier function in monogastrics: Reality or illusion? Pages 15-36 in Nutrition and health of the gastrointestinal tract. M. C. Blok, H. A. Vahl, L. de Lange, A. E. van de Braak, G. Hemke, and M. Hessing, ed. Wageningen Academic Publishers, Wageningen, UK.
52. Visek, W. J. 1984. Ammonia: Its effects on biological systems, metabolic hormones, and reproduction. J. Dairy Sci. 67:481-498.
53. Weatherburn, M. W. 1967. Phenol-hypochlorite reaction for determination of ammonia. Anal. Chem. (Wash.) 39:971-974.
54. Wellock, I. J., P. D. Fortomaris, J. G. M. Houdijk, and I. Kyriazakis. 2006. The effect of dietary protein supply on the performance and risk of post-weaning enteric disorders in newly weaned pigs. Anim. Sci. 82:327-335.
55. Wellock, I. J., P. D. Fortomaris, J. G. M. Houdijk, and I. Kyriazakis. 2008a. Effect of dietary protein supply, weaning age and experimental enterotoxigenic Escherichi coli infection on newly weaned pigs: Health. Animal 2:834-842.
56. Wellock, I. J., P. D. Fortomaris, J. G. M. Houdijk, and I. Kyriazakis. 2008b. Effect of dietary protein supply, weaning age and experimental enterotoxigenic Escherichi coli infection on newly weaned pigs: Performance. Animal 2:825-833.
57. Wolter, B. F., M. Ellis, S. E. Curtis, E. N. Parr, and A. M. Webel. 2002. Effects of feeder-trough space and variation in body weight within a pen of pigs on performance in a wean-to-finish production system. J. Anim. Sci. 80:2241-2246.
58. Younes, H., K. A. Garleb, S. R. Behr, C. Demigne, and C. Remesy. 1998. Dietary fiber stimulates the extra-renal route of nitrogen excretion in partially nephrectomised rats. J. Nutr. Biochem. 9:613-620.
59. Yue, L. Y., and S. Y. Qiao. 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. Livest. Sci. 115:144-152.