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Gut Health of Pigs: Challenge Models and Response Criteria with a Critical Analysis of the Effectiveness of Selected Feed Additives - A Review

  • Adewole, D.I. (Department of Animal Science) ;
  • Kim, I.H. (Department of Animal Resources and Science, Dankook University) ;
  • Nyachoti, C.M. (Department of Animal Science)
  • Received : 2015.09.23
  • Accepted : 2015.11.11
  • Published : 2016.07.01

Abstract

The gut is the largest organ that helps with the immune function. Gut health, especially in young pigs has a significant benefit to health and performance. In an attempt to maintain and enhance intestinal health in pigs and improve productivity in the absence of in-feed antibiotics, researchers have evaluated a wide range of feed additives. Some of these additives such as zinc oxide, copper sulphate, egg yolk antibodies, mannan-oligosaccharides and spray dried porcine plasma and their effectiveness are discussed in this review. One approach to evaluate the effectiveness of these additives in vivo is to use an appropriate disease challenge model. Over the years, researchers have used a number of challenge models which include the use of specific strains of enterotoxigenic Escherichia coli, bacteria lipopolysaccharide challenge, oral challenge with Salmonella enteric serotype Typhimurium, sanitation challenge, and Lawsonia intercellularis challenge. These challenge models together with the criteria used to evaluate the responses of the animals to them are also discussed in this review.

Keywords

References

  1. Amer, M. A. and J. E. Elliot. 1973. Influence of supplemental dietary copper and vitamin E on the oxidative stability of porcine depot fat. J. Anim. Sci. 37:87-90. https://doi.org/10.2527/jas1973.37187x
  2. Armstrong, T. A., C. M. Williams, J. W. Spears, and S. S. Shiffman. 2000. High dietary copper improves odor characteristics of swine waste. J. Anim. Sci. 78:859-864. https://doi.org/10.2527/2000.784859x
  3. Armstrong, T. A., D. R. Cook, M. M. Ward, C. M. Williams, and J. W. Spears. 2004. Effect of dietary copper source (cupric citrate and cupric sulfate) and concentration on growth performance and fecal copper excretion in weanling pigs. J. Anim. Sci. 82:1234-1240. https://doi.org/10.2527/2004.8241234x
  4. Balaji, R., K. J. Wright, C. M., Hill, S. S. Dritz, E. L. Knoppel, and J. E. Minton. 2000. Acute phase responses of pigs challenged orally with Salmonella typhimurium. J. Anim. Sci. 78:1885-1891. https://doi.org/10.2527/2000.7871885x
  5. Bhandari, S. K., B. Xu, C. M. Nyachoti, D. W. Giesting, and D. O. Krause. 2008. Evaluation of alternatives to antibiotics using an Escherichia coli K88+ model of piglet diarrhea: Effects on gut microbial ecology. J. Anim. Sci. 86:836-847. https://doi.org/10.2527/jas.2006-822
  6. Bischoff, S. C. 2011. 'Gut health': A new objective in medicine? BMC Med. 9:24-38. https://doi.org/10.1186/1741-7015-9-24
  7. Boddicker, N., E. H. Waide, R. R. Rowland, J. K. Lunney, D. J. Garrick, J. M. Reecy, and J. C. Dekkers. 2012. Evidence for a major QTL associated with host response to porcine reproductive and respiratory syndrome virus challenge. J. Anim. Sci. 90:1733-1746. https://doi.org/10.2527/jas.2011-4464
  8. Boguslawska-Tryk, M., A. Piotrowska, and K. Burlikowska. 2012. Dietary fructans and their potential beneficial influence on health and performance parameters in broiler chickens. J. Cent. Eur. Agric. 13:272-291.
  9. Bosi, P., L. Casini, A. Finamore, C. Cremokolini, G. Merialdi, P. Trevisi, F. Nobili, and E. Mengheri. 2004a. Spray-dried plasma improves growth performance and reduces inflammatory status of weaned pigs challenged with enterotoxigenic Escherichia coli K88. J. Anim. Sci. 82:1764-1772. https://doi.org/10.2527/2004.8261764x
  10. Bronsvoort, M., B. Norby, D. P. Bane, and I. A. Gardner. 2001. Management factors associated with seropositivity to Lawsonia intracellularis in U.S. swine herds. J. Swine Health Prod. 9:285-290.
  11. Burkey, T. E., S. S. Dritz, J. C. Nietfeld, B. J. Johnson, and J. E. Minton. 2004. Effect of dietary mannanoligosaccharides and sodium chlorate on the growth performance, acute-phase response, and bacterial shedding of weaned pigs challenged with Salmonella enteric serotype Typhimurium. J. Anim. Sci. 82:397-404. https://doi.org/10.2527/2004.822397x
  12. Carlson, M. S., G. M. Hill, J. E. Link, G. A. McCully, D. W. Rozeboom, and R. L. Weavers. 1995. Impact of zinc oxide and copper sulfate supplementation on the newly weaned pig. J. Anim. Sci. 73:72. https://doi.org/10.2527/1995.73suppl_272x
  13. Carlson, M. S., G. M. Hill, and J. E. Link. 1999. Early- and traditionally weaned nursery pigs benefit from phase-feeding pharmacological concentrations of zinc oxide: Effect on metallothionein and mineral concentrations. J. Anim. Sci. 77:1199-1207. https://doi.org/10.2527/1999.7751199x
  14. Casini, L., P. Bosi, C. Gremokolini, P. Trevisi, M. Mazzoni, and P. Bonilauri. 2004b Oral challenge with E. coli K88 as a tool to assess growth and health performance in feeding trials of weaned pigs. Ital. J. Anim. Sci. Suppl 1. 2:358-360.
  15. Castillo, M., S. M. Martin-Orue, J. A. Taylor-Pickard, J. F. Perez, and J. Gasa. 2008. Use of mannan-oligosaccharides and zinc chelate as growth promoters and diarrhea preventive in weaning pigs: Effects on microbiota and gut function. J. Anim. Sci. 86:94-101. https://doi.org/10.2527/jas.2005-686
  16. Chapman, M. E., W. Wang, G. F. Erf, and R. F. Widemand Jr. 2005. Pulmonary hypertensive responses of broilers to bacterial lipopolysaccharide (LPS); Evaluation of LPS source and dose and impact of pre-existing pulmonary hypertension and cellulose micro-particles selection. Poult. Sci. 84:432-441. https://doi.org/10.1093/ps/84.3.432
  17. Cho, J. H., Z. F. Zhang, and I. H. Kim. 2013. Effects of single or combined dietary supplementation of $\beta$-glucan and kefir on growth performance, blood characteristics and meat quality in broilers. Br. Poult. Sci. 54:216-221. https://doi.org/10.1080/00071668.2013.777691
  18. Coffey, R. D. and G. L. Cromwell 1995. The impact of environment and antimicrobial agents on the growth response of early-weaned pigs to spray dried porcine plasma. J. Anim. Sci. 73:2532-2539. https://doi.org/10.2527/1995.7392532x
  19. Coffey, R. D., G. L. Cromwell, and H. J. Monegue. 1994. Efficacy of a copper-lysine complex as a growth promotant for weanling pigs. J. Anim. Sci. 72:2880-2886. https://doi.org/10.2527/1994.72112880x
  20. Coma, J., D. R. Zimmerman, and D. Carrion. 1996. Lysine requirement of the lactating sow determined by using plasma urea nitrogen as a rapid response criterion. J. Anim. Sci. 74: 1056-1062. https://doi.org/10.2527/1996.7451056x
  21. Cromwell, G. L., T. S. Stahly, and H. J. Monegue. 1989. Effects of source and level of copper on performance and liver copper stores in weanling pigs. J. Anim. Sci. 67:2996-3002. https://doi.org/10.2527/jas1989.67112996x
  22. Davis, M. E., C. V. Maxwell, D. C. Brown, B. Z. de Rodas, Z. B. Johnson, E. B. Kegley, D. H. Hellwig, and R. A. Dvorak. 2002. Effect of dietary mannanoligosaccharide and(or) pharmacological additions of supplemental copper on growth performance and immunocompetence of weanling and growing/finishing pigs. J. Anim. Sci. 80:2887-2894. https://doi.org/10.2527/2002.80112887x
  23. de Lange, C. F. M., J. Pluske, J. Gong, and C. M. Nyachoti. 2010. Strategic use of feed ingredients and feed additives to stimulate gut health and development in young pigs. Livest. Sci. 134:124-134. https://doi.org/10.1016/j.livsci.2010.06.117
  24. Dinarello, C. A. 1984. Interleukin 1. Rev. Infect. Dis. 651.
  25. Domeneghini, C., A. Di Giancamillo, S. Arrighi, and G. Bosi. 2006. Gut-trophic feed additives and their effects upon the gut structure and intestinal metabolism. State of the art in the pig, and perspectives towards humans. Histol. Histopathol. 21:273-283.
  26. Dove, C. R. 1995. The effect of copper level on nutrient utilization of weanling pigs. J. Anim. Sci. 73:166-171. https://doi.org/10.2527/1995.731166x
  27. Dove, C. R. and K. D. Haydon. 1991. The effect of copper addition to diets with various iron levels on the performance and hematology of weanling swine. J. Anim. Sci. 69:2013-2019. https://doi.org/10.2527/1991.6952013x
  28. Fong, Y., L. L. Moldawer, M. Marano, H. Wei, A. Barber, K. Manogue, K. J. Tracey, G. Kuo, D. A. Fischman, A. Cerami, and S. F. Lowry. 1989. Cachectin/TNF or IL-1a induces cachexia with redistribution of body proteins. Am. J. Physiol. 256:R659-R665.
  29. Forshell, L. P. and M. Wierup. 2006. Salmonella contamination: A significant challenge to the global marketing of animal food products. Rev. Off. Int. Epizoot. 25:541-554. https://doi.org/10.20506/rst.25.2.1683
  30. Frank, J. W., J. A. Carroll, G. L. Allee, and M. E. Zannelli. 2003. The effects of thermal environment and spray-dried plasma on the acute-phase response of pigs challenged with lipopolysaccharide. J. Anim. Sci. 81:1166-1176. https://doi.org/10.2527/2003.8151166x
  31. Fusco, P., A. To, S. To, and C. Brinton, Jr. 1978. The purification and characterization of four types of E. coli pili and the specificity of E. coli pili for immunity, colonization and adhesion. In: XIIIth US-Japan Conference on Cholera (Ed. C. Miller). Atlanta, GA, USA. pp. 60-70.
  32. Gao, Y. Y., Z. Y. Jiang, Y. C. Lin, C. T. Zheng, G. L. Zhou, and F. Chen. 2011. Effects of spray-dried porcine plasma on serous and intestinal redox status and cytokines of neonatal piglets. J. Anim. Sci. 89:150-157. https://doi.org/10.2527/jas.2010-2967
  33. Gebru, E., J. S. Lee, J. C. Son, S. Y. Yang, S. A. Shin, B. Kim, M. K. Kim, and S. C. Park. 2010. Effect of probiotic-, bacteriophage-, or organic acid-supplemented feeds or fermented soybean meal on the growth performance, acute-phase response, and bacterial shedding of grower pigs challenged with Salmonella enteric serotype Typhimurium. J. Anim. Sci. 88:3880-3886. https://doi.org/10.2527/jas.2010-2939
  34. Gheisar, M. M. and I. H. Kim. 2014. Effect of Dietary Stevia on immune response of growing pigs challenged with Escherichia coli lipopolysaccharide. Int. J. Agric. Innov. Res. 2:1174-1177.
  35. Gibson, G. R. and M. B. Roberfroid. 1995. Dietary modulation of the human colonic microbiota: Introducing the concept of prebiotics. J. Nutr. 125:1401-1412.
  36. Goodman, M. N. 1991. Tumor necrosis factor induces skeletal muscle protein breakdown in rats. Synergism with interleukin-1. Am. J. Physiol. 260:E727-E730.
  37. Gyles, C. L. 1994. Escherichia coli verotoxin and other cytotoxins. In: Escherichia coli in Domestic Animals and Humans., (Ed. C. L. Gyles). CAB International, Wallingford, UK. pp. 151-170.
  38. Hahn, J. D. and D. H. Baker. 1993. Growth and plasma zinc responses of young pigs fed pharmacologic levels of zinc. J. Anim. Sci. 71:3020-3024. https://doi.org/10.2527/1993.71113020x
  39. Haley, C. A., D. A. Dargatz, E. J. Bush, M. M. Erdman, and P. J. Fedorka-Cray. 2012. Salmonella prevalence and antimicrobial susceptibility from the National Animal Health Monitoring System Swine 2000 and 2006 studies. J. Food Prot. 75:428-436. https://doi.org/10.4315/0362-028X.JFP-11-363
  40. Hashimoto, M., T. Bando, M. Iriki, and K. Hashimoto. 1988. Effect of indomethacin on febrile response to recombinant human interleukin 1-a in rabbits. Am. J. Physiol. 255:R527-R533.
  41. Heo J. M., F. O. Opapeju, J. R. Pluske, J. C. Kim, D. J. Hampson, and C. M. Nyachoti. 2013. Gastrointestinal health and function in weaned pigs: A review of feeding strategies to control post-weaning diarrhoea without using in-feed antimicrobials. J. Anim. Physiol. Anim. Nutr. 97:207-237. https://doi.org/10.1111/j.1439-0396.2012.01284.x
  42. Hill, G. M., D. C. Mahan, S. D. Carter, G. L. Cromwell, R. C. Ewan, R. L. Harrold, A. J. Lewis, P. S. Miller, G. C. Shurson, and T. L. Veum. 2001. Effect of pharmacological concentrations of zinc oxide with or without inclusion of an antibacterial agent on nursery pig performance. J. Anim. Sci. 79:934-941. https://doi.org/10.2527/2001.794934x
  43. Hill, G. M., G. L. Cromwell, T. D. Crenshaw, R. C. Ewan, D. A. Knabe, A. J. Lewis, D. C. Mahan, G. C. Shurson, L. L. Southern, and T. L. Veum. 1996. Impact of pharmacological intakes of zinc and (or) copper on performance of weanling pigs. J. Anim. Sci. 74:181.
  44. Ho, S. K. and J. I. Elliot. 1974. Fatty acid composition of porcine depot fat as related to the effect of supplemental dietary copper on the specific activities of fatty acyl desaturase systems. Can. J. Anim. Sci. 54:23-28. https://doi.org/10.4141/cjas74-004
  45. Hobbie, S., L. M. Chen, R. J. Davis, and J. E. Galan. 1997. Involvement of mitogen-activated protein kinase pathways in the nuclear responses and cytokine production induced by Salmonella typhimurium in cultured intestinal epithelia cells. J. Immunol. 159:5550-5559.
  46. Holm, A. 1988. Escherichia coli induced weaning diarrhea in pigs. Dietary supplementation of zinc oxide as an antibacterial method? Dan. Veterinaertidsskr.71:1118-1126.
  47. Jayaraman, B., J. Htoo, and C. M. Nyachoti. 2015. Effects of dietary threonine: lysine ratios and sanitary conditions on performance, plasma urea nitrogen, plasma-free threonine and lysine of weaned pigs. Anim. Nutr. 1:283-288. https://doi.org/10.1016/j.aninu.2015.09.003
  48. Jepson, M. M., J. M. Pell, P. C. Bates, and D. J. Millward. 1986. The effects of endotoxaemia on protein metabolism in skeletal muscle and liver of fed and fasted rats. Biochem. J. 235:329-336. https://doi.org/10.1042/bj2350329
  49. Jiang, R., X. Chang, B. Stoll, M. Z. Fan, J. Arthington, E. Weaver, J. Campbell, and D. G. Burrin. 2000. Dietary plasma protein reduces small intestinal growth and lamina propria cell density in early weaned pigs. J. Nutr. 130:21-26. https://doi.org/10.1093/jn/130.1.21
  50. Jiang, Z. Y., L. H. Sun, Y. C. Lin, X. Y. Ma, C. T. Zheng, G. L. Zhou, F. Chen, and S. T. Zou. 2009. Effects of dietary glycyl-glutamine on growth performance, small intestinal integrity, and immune responses of weaning piglets challenged with lipopolysaccharide. J. Anim. Sci. 87:4050-4056. https://doi.org/10.2527/jas.2008-1120
  51. Jin, L. Z., S. K. Baidoo, R. R. Marquardt, and A. A. Frohlich. 1998. In vitro inhibition of adhesion of enterotoxigenic Escherichia coli K88 to piglet intestinal mucus by egg-yolk antibodies. FEMS Immunol. Med. Microbiol. 21:313-321. https://doi.org/10.1111/j.1574-695X.1998.tb01179.x
  52. Johnson, R. W. 1997. Inhibition of growth by pro-inflammatory cytokines: an integrated view. J. Anim. Sci. 75:1244-1255. https://doi.org/10.2527/1997.7551244x
  53. Johnson, R. W. and E. von Borell. 1994. Lipopolysaccharide-induced sickness behaviour in pigs is inhibited by pretreatment with indomethacin. J. Anim. Sci. 72:309-314. https://doi.org/10.2527/1994.722309x
  54. Kahindi, R. 2014. Assessment of Standardized Ileal Digestible Lysine and Sulphur Amino Acids to Lysine Ratio for Weaned Piglets Fed Antibiotic-Free Diets. Ph.D. Thesis, University of Manitoba, Winnipeg, MB, Canada.
  55. Kahindi, R. K., J. K. Htoo, and C. M. Nyachoti. 2014. Short communication: Effect of dietary lysine content and sanitation conditions on performance of weaned pigs fed antibiotic-free diets. Can. J. Anim. Sci. 94:115-118. https://doi.org/10.4141/cjas2013-016
  56. Kegley, E. B., J. W. Spears, and S. K. Auman. 2001. Dietary phosphorus and an inflammatory challenge affect performance and immune function of weanling pigs. J. Anim. Sci. 79:413-419. https://doi.org/10.2527/2001.792413x
  57. Knetter, S. M., S. M. Bearson, T. H. Huang, D. Kurkiewicz, M. Schroyen, D. Nettleton, D. Berman, V. Cohen, J. K. Lunney, A. E. Ramer-Tait, M. J. Wannemuehler, and C. K. Tuggle. 2015. Salmonella enterica serovar Typhimurium-infected pigs with different shedding levels exhibit distinct clinical, peripheral cytokine and transcriptomic immune response phenotypes. Innate Immun. 21:227-241. https://doi.org/10.1177/1753425914525812
  58. Kiarie, E., B. A. Slominski, D. O Krause, and C. M. Nyachoti. 2009. Acute phase response of piglets fed diets containing non-starch polysaccharide hydrolysis products and egg yolk antibodies following an oral challenge with Escherichia coli (K88). Can. J. Anim. Sci. 89:353-360. https://doi.org/10.4141/CJAS09008
  59. Kim, K. H., J. H. Cho, and I. H. Kim. 2013. Effects of dietary carbohydrases on growth performance, nutrient digestibility and blood characteristics in finishing pigs. J. Anim. Sci. Tech. 55:289-293. https://doi.org/10.5187/JAST.2013.55.4.289
  60. Kornegay, E. T. and A. F. Harper. 1997. Environmental nutrition: Nutrient management strategies to reduce nutrient excretion of swine. Prof. Anim. Sci. 13:99-111.
  61. Lay, D. C., R. L. Matteri, J. A. Carrol, T. J. Fangman, and T. J. Safranski. 2002. Preweaning survival in swine. J. Anim. Sci. 80:E74-E86. https://doi.org/10.2527/animalsci2002.80E-Suppl_2E74x
  62. Lee, C., L. R. Giles, W. L. Bryden, J. L. Downing, P. C. Owens, A. C. Kirby, and P. C. Wynn. 2005. Performance and endocrine responses of group housed weaner pigs exposed to the air quality of a commercial environment. Livest. Prod. Sci. 93:255-262. https://doi.org/10.1016/j.livprodsci.2004.10.003
  63. Lee, J. S., E. G. Awji, S. J. Lee, D. D. Tassew, Y. B. Park, K. S. Park, M. K. Kim, B. Kim, and S. C. Park. 2012. Effect of Lactobacillus planetarium CJLP243 on the growth performance of cytokine response of weaning pigs challenged with enterotoxigenic Escherichia coli. J. Anim. Sci. 90:3709-3717. https://doi.org/10.2527/jas.2011-4434
  64. Le Floc'h, N., C. Jondreville, J. J. Matte, and B. Seve. 2006. Importance of sanitary environment for growth performance and plasma nutrient homeostasis during the post-weaning period in piglets. Arch. Anim. Nutr. 60:23-34. https://doi.org/10.1080/17450390500467810
  65. Le Floc'h, N., L. LeBellego, J. J. Matte, D. Melchior, and B. Seve. 2009. The effect of sanitary status degradation and dietary tryptophan content on growth rate and tryptophan metabolism in weaning pigs. J. Anim. Sci. 87:1686-1694. https://doi.org/10.2527/jas.2008-1348
  66. LeMieux, F. M., L. L. Southern, and T. D. Bidner. 2003. Effect of mannanoligosaccharides on growth performance of weanling pigs. J. Anim. Sci. 81:2482-2487. https://doi.org/10.2527/2003.81102482x
  67. Li, J. and I. H. Kim. 2013. Effects of levan-type fructan supplementation on growth performance, digestibility, blood profile, fecal microbiota, and immune responses after lipopolysaccharide challenge in growing pigs. J. Anim. Sci. 91:5336-5343. https://doi.org/10.2527/jas.2013-6665
  68. Li, X., J. Yin, D. Li, X. Chen, J. Zang, and X. Zhou. 2006 Dietary supplementation with zinc oxide increases IGF-1 and IGF-1 receptor gene expression in the small intestine of weanling piglets. J. Nutr. 136:1786-1791. https://doi.org/10.1093/jn/136.7.1786
  69. Liu, Y. L., D. F. Li, L. M. Gong, G. F. Yi, A. M. Gaines, and J. A. Carrol. 2003. Effects of fish oil supplementation on the performance and the immunological, adrenal, and somatotrophic responses of weaned pigs after an Escherichia coli lipopolysaccharide challenge. J. Anim. Sci. 81:2758-2765. https://doi.org/10.2527/2003.81112758x
  70. 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. https://doi.org/10.1111/j.1574-695X.1999.tb01249.x
  71. Mavcromichalis, I., C. M. peter, T. M. Parr, D. Ganessunker, and D. H. baker. 2000. Growth-promoting efficacy in young pigs of two sources of zinc oxide having either a high or a low bioavailability of zinc. J. Anim. Sci. 78:2896-2902. https://doi.org/10.2527/2000.78112896x
  72. Meng, Q. W., L. Yan, X. Ao, H. D. Jang, J. H. Cho, and I. H. Kim 2010. Effects of chito-oligosaccharide supplementation on egg production, nutrient digestibility, egg quality and blood profiles in laying hens. Asian Australas. J. Anim. Sci. 23:1476-1481. https://doi.org/10.5713/ajas.2010.10025
  73. Mitchell, A. D., A. M. Scholz, and H. J. Mersmann. 2001. Growth and body composition. In: Biology of the Domestic Pig (Eds. W. G. Pond and H. J. Mersmann). Cornell University Press, NY, USA. 225 p.
  74. Mohana Devi, S., S. I. Lee, and I. H. Kim. 2015. Effect of phytogenics on growth performance, fecal score, blood profiles, fecal noxious gas emission, digestibility, and intestinal morphology of weanling pigs challenged with Escherichia coli K88. Pol. J. Vet. Sci. 18:557-564. https://doi.org/10.1515/pjvs-2015-0072
  75. Moreto, M. and A. Perez-Bosque. 2009. Dietary plasma proteins, the intestinal immune system, and the barrier functions of the intestinal mucosa. J. Anim. Sci. 87:E92-E100. https://doi.org/10.2527/jas.2008-1381
  76. Morovat, A. and M. J. Dauncey. 1998. Effects of thyroid status on insulin-like growth factor-I, growth hormone and insulin are modified by food intake. Eur. J. Endocrinol. 138:95-103. https://doi.org/10.1530/eje.0.1380095
  77. Munyaka, P. M., H. Echeverry, A. Yitbarek, G. Camelo-Jaimes, S. Sharif, W. Guenter, J. D. House, and J. C. Rodriguez-Lecompte. 2012. Local and systemic innate immunity in broiler chickens supplemented with yeast-derived carbohydrates. Poult. Sci. 91: 2164-2172. https://doi.org/10.3382/ps.2012-02306
  78. Neumann, E. J., J. B. Kliebenstein, C. D. Johnson, J. W. Mabry, E. J. Bush, A. H. Seitzinger, A. L. Green, and J. J. Zimmerman. 2005. Assessment of the economic impact of porcine reproductive and respiratory syndrome on swine production in the United States. J. Am. Vet. Med. Assoc. 227:385-392. https://doi.org/10.2460/javma.2005.227.385
  79. Nyachoti, C. M., E. Kiarie, S. K Bhandari, G. Zhang, and D. O. Krause. 2012. Weaned pig responses to Escherichia coli K88 oral challenge when receiving a lysozyme supplement. J. Anim. Sci. 90:252-260. https://doi.org/10.2527/jas.2010-3596
  80. Ojha, S. and M. Kostrzynska. 2007. Approaches for reducing Salmonella in pork production. J. Food Prot. 70:2460-2694. https://doi.org/10.4315/0362-028X-70.11.2460
  81. Opapeju, F. O., D. O. Krause, R. L. Payne, M. Rademacher, and C. M. Nyachoti. 2009. Effect of dietary protein level on growth performance, indicators of enteric health, and gastrointestinal microbial ecology of weaned pigs induced with postweaning colibacillosis. J. Anim. Sci. 87:2635-2643. https://doi.org/10.2527/jas.2008-1310
  82. Owusu-Asiedu, A., S. K. Baidoo, C. M. Nyachoti, and R. R. Marquardt. 2002. Response of early-weaned pigs to spray-dried porcine or animal plasma based diets supplemented with egg-yolk antibodies against enterotoxigenic Escherichia coli. J. Anim. Sci. 80:2895-2903. https://doi.org/10.2527/2002.80112895x
  83. Owusu-Asiedu, A., C. M. Nyachoti, S. K. Baidoo, R. R. Marquardt, and X. Yang. 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. J. Anim. Sci. 81:1781-1789. https://doi.org/10.2527/2003.8171781x
  84. Pastorelli, H., J. van Milgen, P. Lovatto, and L. Montagne. 2012. Meta-analysis of feed intake and growth responses of growing pigs after a sanitary challenge. Animal 6:952-961. https://doi.org/10.1017/S175173111100228X
  85. Peace, R. M., J. Campbell, J. Polo, J. Creshaw, L. Russell, and A. Moeser. 2011. Spray-dried porcine plasma influences intestinal barrier function, inflammation, and diarrhea in weaned pigs. J. Nutr. 141:1312-1317. https://doi.org/10.3945/jn.110.136796
  86. Pluske, J. R., D. J. Hampson, and I. H. Williams. 1997. Factors influencing the structure and function of the small intestine in the weaned pig: a review. Livest. Prod. Sci. 51:215-236. https://doi.org/10.1016/S0301-6226(97)00057-2
  87. Poulsen, H. D. 1989. Zinc oxide for weaned pigs. In: Proc. 40th Annu. Mtg. Eur. Assoc. Anim. Prod., Dublin, Ireland, pp 8-10.
  88. Poulsen, H. D. 1995. Zinc oxide for weanling piglets. Acta Agric. Scand. A. Anim. Sci. 45:159-167.
  89. Rincker, M. J., G. M. Hill, J. E. Link, A. M. Meyer, and J. E. Rowntree. 2005. Effects of dietary zinc and iron supplementation on mineral excretion, body composition, and mineral status of nursery pigs. J. Anim. Sci. 83:2762-2774. https://doi.org/10.2527/2005.83122762x
  90. Roof, M. D. and D. C. Mahan. 1982. Effect of carbadox and various dietary copper levels for weanling swine. J. Anim. Sci. 55:1109-1117. https://doi.org/10.2527/jas1982.5551109x
  91. Rose-Dye, T. K., L. O. Burciaga-Robles, C. R. Krehbiel, D. L. Step, R. W. Fulton, A. W. Confer, and C. J. Richards. 2011. Rumen temperature change monitored with remote rumen temperature boluses after challenges with bovine viral diarrhea virus and Mannheimia haemolytica. J. Anim. Sci. 89:1193-1200. https://doi.org/10.2527/jas.2010-3051
  92. Rostagno, M. H. and T. R. Callaway. 2012. Pre-harvest risk factors for Salmonella enterica in pork production. Food Res. Int. 45:634-640. https://doi.org/10.1016/j.foodres.2011.04.041
  93. Sandberg, F. B., G. C. Emmans, and I. Kyriazakis. 2007. The effects of pathogen challenges on the performance of native and immune animals: The problem of prediction. Animal 1:67-86. https://doi.org/10.1017/S175173110765784X
  94. Schutz, J. S., J. A. Carrol, L. C. Gasbarre, T. A. Shelton, S. T. Nordstrom, J. P. Hutcheson, H. Van Campen, and T. E. Engle. 2012. Effects of gastrointestinal parasites on parasite burden, rectal temperature, and antibody titer responses to vaccination and infectious bovine rhinotrachritis virus challenge. J. Anim. Sci. 90:1948-1954. https://doi.org/10.2527/jas.2011-4059
  95. Shang, Y. 2014. Effects of Fructooligosaccharide Alone or in Combination with Phytase on Growth Performance, Nutrient Utilization, Immune Response and Gut Development of Broiler Chickens. M.Sc. thesis, University of Manitoba, Winnipeg, MB, Canada.
  96. Shields, R. G., D. C. Mahan, and P. L. Graham. 1983. Changes in swine body composition from birth to 145 kg. J. Anim. Sci. 57:43-54. https://doi.org/10.2527/jas1983.57143x
  97. Shini, S., P. Kaiser, A. Shini, and W. L. Bryden. 2008. Differential alterations in ultrastructural morphology of chicken heterophils and lymphocytes induced by corticosterone and lipopolysaccharide. Vet. Immunol. Immunopathol. 122:83-93. https://doi.org/10.1016/j.vetimm.2007.10.009
  98. Smith, J. W., M. D. Tokach, R. D. Goodband, J. L. Nelssen, and B. T. Richert. 1997. Effects of the interrelationship between zinc oxide and copper sulfate on growth performance of early-weaned pigs. J. Anim. Sci. 75:1861-1866. https://doi.org/10.2527/1997.7571861x
  99. Song, M., T. M. Che, Y. Liu, J. A. Soares, B. G. Harmon, and J. E. Pettigrew. 2012. Effects of dietary spray-dried egg on growth performance and health of weaned pigs. J. Anim. Sci. 90:3080-3087. https://doi.org/10.2527/jas.2011-4305
  100. Spring, P., C. Wenk, K. A. Dawson, and K. E. Newman. 2000. The effects of dietary mannanoligosaccharides on cecal parameters and the concentrations of enteric bacteria in the ceca of salmonella-challenged broiler chicks. Poult. Sci. 79:205-211. https://doi.org/10.1093/ps/79.2.205
  101. Thacker, P. A. 2013. Alternatives to antibiotics as growth promoters for use in swine production: A review. J. Anim. Sci. Biotechnol. 4:35. https://doi.org/10.1186/2049-1891-4-35
  102. Trevisi, P., D. Melchior, M. Mazzoni, L. Casini, S. De Filippi, L. Minieri, G. Lalata-Costerbosa, and P. Bosi. 2009. A tryptophan-enriched diet improves feed intake and growth performance of susceptible weanling pigs orally challenged with Escherichia coli K88. J. Anim. Sci. 87:148-156. https://doi.org/10.2527/jas.2007-0732
  103. Turner, J. L., S. S. Dritz, J. J. Higgins, K. L. Herkelman, and J. E. Minton. 2002. Effects of a Quillaja saponaria extract on growth performance and immune function of weanling pigs challenged with Salmonella typhimurium. J. Anim. Sci. 80:1939-1946. https://doi.org/10.2527/2002.8071939x
  104. Van der Peet-Schwering, C. M. C. and G. P. Binnendijk. 1995. The effect of spray-dried porcine plasma in diets with different protein sources on the performance of weanling piglets. In: Report P1. 137. Praktijkkonder-zoek Varkenshouderij, Rosmalen, The Netherland.
  105. van Dijk, A. J., H. Everts, M. J. A. Nabuurs, R. J. C. F. Margry, and A. C. Beynen. 2001. Growth performance of weanling pigs fed spray-dried animal plasma: A review. Livest. Prod. Sci. 68:263-274. https://doi.org/10.1016/S0301-6226(00)00229-3
  106. Walk, C. L., S. Srinongkote, and P. Wilcock. 2013. Influence of a microbial phytase and zinc oxide on young pig growth performance and serum minerals. J. Anim. Sci. 91:286-291. https://doi.org/10.2527/jas.2012-5430
  107. Wang, J. P., J. S. Yoo, H. D. Jang, J. H. Lee, J. H. Cho, and I. H. Kim. 2011. Effect of dietary fermented garlic by Weissella koreensis powder on growth performance, blood characteristic, and immune response of growing pigs challenged with Escherichia coli lipopolysaccharide. J. Anim. Sci. 89:2123-2131. https://doi.org/10.2527/jas.2010-3186
  108. Wannemacher, R. W. 1977. Key role of various individual amino acids in host response to infection. Am. J. Clin. Nutr. 30:1269-1280. https://doi.org/10.1093/ajcn/30.8.1269
  109. Webel, D. M., B. N. Finck, D. H. Baker, and R. W. Johnson. 1997. Time course of increased plasma cytokines, cortisol, and urea nitrogen in pigs following intraperitoneal injection of lipopolysaccharide. J. Anim. Sci. 75:1514-1520. https://doi.org/10.2527/1997.7561514x
  110. Wedekind, K. J., A. J. Lewis, M. A. Giesemann, and P. S. Miller. 1994. Bioavailability of zinc from inorganic and organic sources for pigs fed corn-soybean meal diets. J. Anim. Sci. 72:2681-2689. https://doi.org/10.2527/1994.72102681x
  111. Wedekind, K. J. and A. J. Lewis. 1993. Assessing zinc bioavailability with pigs fed corn-soybean meal diets. Nebraska Swine Report, Lincoln, NE, USA. 24 p.
  112. Wellock, I. J., J. G. M. Houdijk, A. C. Miller, B. P. Gill, and I. Kyriazakis. 2009. The effect of weaner diet protein content and diet quality on the long-term performance of pigs to slaughter. J. Anim. Sci. 87:1261-1269. https://doi.org/10.2527/jas.2008-1098
  113. White, M. E., T. G. Ramsay, J. M. Osborne, K. A. Kampman, and D. W. Leaman. 1991. Effect of weaning at different ages on serum insulin-like growth factor-I (IGF-I), IGF binding proteins, and serum in vitro mitogenic activity in swine. J. Anim. Sci. 69:134-145. https://doi.org/10.2527/1991.691134x
  114. White, L. A., M. C. Newman, G. L. Cromwell, and M. D. Lindemann. 2002. Brewers dried yeast as a source of mannanoligosaccharides for weanling pigs. J. Anim. Sci. 80:2619-2628. https://doi.org/10.2527/2002.80102619x
  115. Whitney, M. H., G. C. Shurson, and R. C. Guedes. 2006. Effect of dietary inclusion of distillers dried grains with solubles on the ability of growing pigs to resist a Lawsonia intracellularis challenge. J. Anim. Sci. 84:1880-1889. https://doi.org/10.2527/jas.2004-578
  116. Xu, Z. R., X. T. Zou, C. H. Hu, M. S. Xia, X. A. Zhan, and M. Q. Wang. 2003. Effects of dietary fructooligosaccharide on digestive enzyme activities, intestinal microflora and morphology of male broilers. Poult. Sci. 82:1030-1036. https://doi.org/10.1093/ps/82.6.1030
  117. Yang, X., Y. Guo, X. He, J. Yuan, Y. Yang, and Z. Wang. 2008. Growth performance and immune responses in chickens after challenge with lipopolysaccharide and modulation by dietary different oils. Animal 2:216-223.
  118. Yokoyama, H., R. C. Peralta, R. Diaz, S. Sendo, Y. Ikemori, and Y. Kodama. 1992. Passive protective effect of chicken egg yolk immunoglobulins against experimental enterotoxigenic Escherichia coli. Infect. Immun. 60:998-1007.
  119. Yolken, R. H., F. Leister, S. B. Wee, R. Miskuff, and S. Vonderfecht. 1988. Antibodies to rota viruses in chickens' eggs: a potential source of antiviral immunoglobulins suitable for human consumption. Pediatrics 81:291-295.
  120. Zannelli, M. E., K. J. Touchette, G. L. Allee, R. L. Matteri, L. A. Beausang, L. J. Luchene, and J. A. Carroll. 2000. A comparison of the immunological response to lipopolysaccharide (LPS) versus E. coli challenge in the weaned pig. J. Anim. Sci. 78:77.
  121. Zeng, Z., S. Zhang, H. Wang, and X. Piao. 2015. Essential oil and aromatic plants as feed additives in non-ruminant nutrition: A review. J. Anim. Sci. Biotechnol. 6:7. https://doi.org/10.1186/s40104-015-0004-5
  122. Zhang, B., Y. Guo, and Z. Wang. 2008. The modulating effect of $\beta$-1,3/1,6-glucan supplementation in the diet on performance and immunological responses of broiler chickens. Asian Australas. J. Anim. Sci. 21:237-244. https://doi.org/10.5713/ajas.2008.70207
  123. Zhao, P. Y., J. H. Jung, and I. H. Kim. 2012. Effect of mannan oligosaccharides and fructan on growth performance, nutrient digestibility, blood profile, and diarrhea score in weanling pigs. J. Anim. Sci. 90:833-839. https://doi.org/10.2527/jas.2011-3921
  124. Zhao, P. Y., J. P. Wang, and I. H. Kim. 2013. Evaluation of dietary fructan supplementation on growth performance, nutrient digestibility, meat quality, fecal microbial flora, and fecal noxious gas emission in finishing pigs. J. Anim. Sci. 91:5280-5286. https://doi.org/10.2527/jas.2012-5393

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