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Stress, Nutrition, and Intestinal Immune Responses in Pigs - A Review

  • Lee, In Kyu (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, Seoul National University) ;
  • Kye, Yoon Chul (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, Seoul National University) ;
  • Kim, Girak (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, Seoul National University) ;
  • Kim, Han Wool (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, Seoul National University) ;
  • Gu, Min Jeong (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, Seoul National University) ;
  • Umboh, Johnny (Faculty of Animal Science, Sam Ratulangi University) ;
  • Maaruf, Kartini (Faculty of Animal Science, Sam Ratulangi University) ;
  • Kim, Sung Woo (Department of Animal Science, North Carolina State University) ;
  • Yun, Cheol-Heui (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, Seoul National University)
  • Received : 2016.02.14
  • Accepted : 2016.04.22
  • Published : 2016.08.01

Abstract

Modern livestock production became highly intensive and large scaled to increase production efficiency. This production environment could add stressors affecting the health and growth of animals. Major stressors can include environment (air quality and temperature), nutrition, and infection. These stressors can reduce growth performance and alter immune systems at systemic and local levels including the gastrointestinal tract. Heat stress increases the permeability, oxidative stress, and inflammatory responses in the gut. Nutritional stress from fasting, antinutritional compounds, and toxins induces the leakage and destruction of the tight junction proteins in the gut. Fasting is shown to suppress pro-inflammatory cytokines, whereas deoxynivalenol increases the recruitment of intestinal pro-inflammatory cytokines and the level of lymphocytes in the gut. Pathogenic and viral infections such as Enterotoxigenic E. coli (ETEC) and porcine epidemic diarrhea virus can lead to loosening the intestinal epithelial barrier. On the other hand, supplementation of Lactobacillus or Saccharaomyces reduced infectious stress by ETEC. It was noted that major stressors altered the permeability of intestinal barriers and profiles of genes and proteins of pro-inflammatory cytokines and chemokines in mucosal system in pigs. However, it is not sufficient to fully explain the mechanism of the gut immune system in pigs under stress conditions. Correlation and interaction of gut and systemic immune system under major stressors should be better defined to overcome aforementioned obstacles.

Keywords

Nutrition;Stress;Gut Immunity;Pigs

Acknowledgement

Supported by : Rural Development Administration, Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry and Fisheries (IPET), North Carolina Agricultural Foundation

References

  1. Bouhet, S., E. Hourcade, N. Loiseau, A. Fikry, S. Martinez, M. Roselli, P. Galtier, E. Mengheri, and I. P. Oswald. 2004. The mycotoxin fumonisin B1 alters the proliferation and the barrier function of porcine intestinal epithelial cells. Toxicol. Sci. 77:165-171.
  2. Bouhet, S., E. Le Dorze, S. Peres, J. M. Fairbrother, and I. P. Oswald. 2006. Mycotoxin fumonisin B1 selectively down-regulates the basal IL-8 expression in pig intestine: in vivo and in vitro studies. Food. Chem. Toxicol. 44:1768-1773. https://doi.org/10.1016/j.fct.2006.05.018
  3. Bracarense, A. P., J. Lucioli, B. Grenier, G. Drociunas Pacheco, W. D. Moll, G. Schatzmayr, and I. P. Oswald. 2012. Chronic ingestion of deoxynivalenol and fumonisin, alone or in interaction, induces morphological and immunological changes in the intestine of piglets. Br. J. Nutr. 107:1776-1786. https://doi.org/10.1017/S0007114511004946
  4. Cao, L., X. Ge, Y. Gao, Y. Ren, X. Ren, and G. Li. 2015. Porcine epidemic diarrhea virus infection induces NF-kappaB activation through the TLR2, TLR3, and TLR9 pathways in porcine intestinal epithelial cells. J. Gen. Virol. 96:1757-1767. https://doi.org/10.1099/vir.0.000133
  5. Chattha, K. S., A. N. Vlasova, S. Kandasamy, G. Rajashekara, and L. J. Saif. 2013. Divergent immunomodulating effects of probiotics on T cell responses to oral attenuated human rotavirus vaccine and virulent human rotavirus infection in a neonatal gnotobiotic piglet disease model. J. Immunol. 191:2446-2456. https://doi.org/10.4049/jimmunol.1300678
  6. Chaytor, A. C., M. T. See, J. A. Hansen, A. L. de Souza, T. F. Middleton, and S. W. Kim. 2011. Effects of chronic exposure of diets with reduced concentrations of aflatoxin and deoxynivalenol on growth and immune status of pigs. J. Anim. Sci. 89:124-135. https://doi.org/10.2527/jas.2010-3005
  7. Chen, Q., P. Gauger, M. Stafne, J. Thomas, P. Arruda, E. Burrough, D. Madson, J. Brodie, D. Magstadt, R. Derscheid, M. Welch, and J. Zhang. 2015. Pathogenicity and pathogenesis of a United States porcine deltacoronavirus cell culture isolate in 5-day-old neonatal piglets. Virology 482:51-59. https://doi.org/10.1016/j.virol.2015.03.024
  8. Cheon, I. S., S. M. Park, H. J. Lee, J. E. Hong, S. Y. Ji, B. S. Shim, K. H. Kim, P. S. Heo, Y. Y. Kim, H. J. Jung, H. Ka, S. H. Han, M. Song, and C. H. Yun. 2014. Functional characteristics of porcine peripheral T cells stimulated with IL-2 or IL-2 and PMA. Res. Vet. Sci. 96:54-61. https://doi.org/10.1016/j.rvsc.2013.11.018
  9. Collier, C. T., J. A. Carroll, M. A. Ballou, J. D. Starkey, and J. C. Sparks. 2011. Oral administration of Saccharomyces cerevisiae boulardii reduces mortality associated with immune and cortisol responses to Escherichia coli endotoxin in pigs. J. Anim. Sci. 89:52-58. https://doi.org/10.2527/jas.2010-2944
  10. de Arriba, M. L., A. Carvajal, J. Pozo, and P. Rubio. 2002. Isotype-specific antibody-secreting cells in systemic and mucosal associated lymphoid tissues and antibody responses in serum of conventional pigs inoculated with PEDV. Vet. Immunol. Immunopathol. 84:1-16. https://doi.org/10.1016/S0165-2427(01)00386-5
  11. Fairbrother, J. M., E. Nadeau, and C. L. Gyles. 2005. Escherichia coli in postweaning diarrhea in pigs: An update on bacterial types, pathogenesis, and prevention strategies. Anim. Health Res. Rev. 6:17-39. https://doi.org/10.1079/AHR2005105
  12. Gao, Q., S. Zhao, T. Qin, Y. Yin, and Q. Yang. 2015. Effects of porcine epidemic diarrhea virus on porcine monocyte-derived dendritic cells and intestinal dendritic cells. Vet. Microbiol. 179:131-141. https://doi.org/10.1016/j.vetmic.2015.05.016
  13. Gebert, A., H. J. Rothkotter, and R. Pabst. 1996. M cells in Peyer's patches of the intestine. Int. Rev. Cytol. 167:91-159. https://doi.org/10.1016/S0074-7696(08)61346-7
  14. Gu, M. J., S. K. Song, I. K. Lee, S. Ko, S. E. Han, S. Bae, S. Y. Ji, B. C. Park, K. D. Song, H. K. Lee, S. H. Han, and C. H. Yun. 2016. Barrier protection via Toll-like receptor 2 signaling in porcine intestinal epithelial cells damaged by deoxynivalnol. Vet. Res. 47:25. https://doi.org/10.1186/s13567-016-0309-1
  15. Gu, M. J., S. K. Song, S. M. Park, I. K. Lee, and C. H. Yun. 2014. Bacillus subtilis protects porcine intestinal barrier from deoxynivalenol via improved zonula occludens-1 expression. Asian Australas. J. Anim. Sci. 27:580-586.
  16. Hayes, M. R., E. G. Mietlicki-Baase, S. E. Kanoski, and B. C. De Jonghe. 2014. Incretins and amylin: Neuroendocrine communication between the gut, pancreas, and brain in control of food intake and blood glucose. Annu. Rev. Nutr. 34:237-260. https://doi.org/10.1146/annurev-nutr-071812-161201
  17. Horn, N., F. Ruch, G. Miller, K. M. Ajuwon, and O. Adeola. 2014. Impact of acute water and feed deprivation events on growth performance, intestinal characteristics, and serum stress markers in weaned pigs. J. Anim. Sci. 92:4407-4416. https://doi.org/10.2527/jas.2014-7673
  18. Im, J., J. E. Baik, K. W. Kim, S. S. Kang, J. H. Jeon, O. J. Park, H. Y. Kim, K. Y. Kum, C. H. Yun, and S. H. Han. 2015. Enterococcus faecalis lipoteichoic acid suppresses Aggregatibacter actinomycetemcomitans lipopolysaccharide-induced IL-8 expression in human periodontal ligament cells. Int. Immunol. 27:381-391. https://doi.org/10.1093/intimm/dxv016
  19. Kayama, H. and K. Takeda. 2012. Regulation of intestinal homeostasis by innate and adaptive immunity. Int. Immunol. 24:673-680.
  20. Kiarie, E., S. Bhandari, M. Scott, D. O. Krause, and C. M. Nyachoti. 2011. Growth performance and gastrointestinal microbial ecology responses of piglets receiving Saccharomyces cerevisiae fermentation products after an oral challenge with Escherichia coli (K88). J. Anim. Sci. 89:1062-1078. https://doi.org/10.2527/jas.2010-3424
  21. Kim, L., J. Hayes, P. Lewis, A. V. Parwani, K. O. Chang, and L. J. Saif. 2000. Molecular characterization and pathogenesis of transmissible gastroenteritis coronavirus (TGEV) and porcine respiratory coronavirus (PRCV) field isolates co-circulating in a swine herd. Arch. Virol. 145:1133-1147. https://doi.org/10.1007/s007050070114
  22. Lam, J. S., V. L. Taylor, S. T. Islam, Y. Hao, and D. Kocincova. 2011. Genetic and Functional Diversity of Pseudomonas aeruginosa Lipopolysaccharide. Front. Microbiol. 2:118.
  23. Lee, I. K., Y. M. Son, Y. J. Ju, S. K. Song, M. Gu, K. D. Song, H. C. Lee, J. S. Woo, J. G. Seol, S. M. Park, S. H. Han, and C. H. Yun. 2014. Survival of porcine fibroblasts enhanced by human FasL and dexamethasone-treated human dendritic cells in vitro. Transpl. Immunol. 30:99-106. https://doi.org/10.1016/j.trim.2014.01.002
  24. Meng, D., Y. Hu, C. Xiao, T. Wei, Q. Zou, and M. Wang. 2013. Chronic heat stress inhibits immune responses to H5N1 vaccination through regulating CD4(+) CD25(+) Foxp3(+) Tregs. Biomed. Res. Int. 2013:160859.
  25. Obremski, K., S. Gonkowski, and P. Wojtacha. 2015a. Zearalenone-induced changes in the lymphoid tissue and mucosal nerve fibers in the porcine ileum. Pol. J. Vet. Sci. 18:357-365. https://doi.org/10.1515/pjvs-2015-0046
  26. Obremski, K., P. Podlasz, M. Zmigrodzka, A. Winnicka, M. Wozny, P. Brzuzan, E. Jakimiuk, P. Wojtacha, M. Gajecka, L. Zielonka, and M. Gajecki. 2013. The effect of T-2 toxin on percentages of CD4+, CD8+, CD4+ CD8+ and CD21+ lymphocytes, and mRNA expression levels of selected cytokines in porcine ileal Peyer's patches. Pol. J. Vet. Sci. 16:341-349. https://doi.org/10.2478/pjvs-2013-0046
  27. Obremski, K., P. Wojtacha, P. Podlasz, and M. Zmigrodzka. 2015b. The influence of experimental administration of low zearalenone doses on the expression of Th1 and Th2 cytokines and on selected subpopulations of lymphocytes in intestinal lymph nodes. Pol. J. Vet. Sci. 18:489-497.
  28. Pearce, S. C., V. Mani, R. L. Boddicker, J. S. Johnson, T. E. Weber, J. W. Ross, R. P. Rhoads, L. H. Baumgard, and N. K. Gabler. 2013. Heat stress reduces intestinal barrier integrity and favors intestinal glucose transport in growing pigs. PLoS One 8:e70215. https://doi.org/10.1371/journal.pone.0070215
  29. Pearce, S. C., M. V. Sanz-Fernandez, J. H. Hollis, L. H. Baumgard, and N. K. Gabler. 2014. Short-term exposure to heat stress attenuates appetite and intestinal integrity in growing pigs. J. Anim. Sci. 92:5444-5454. https://doi.org/10.2527/jas.2014-8407
  30. Shen, Y. B., A. C. Weaver, and S. W. Kim. 2014. Effect of feed grade L-methionine on growth performance and gut health in nursery pigs compared with conventional DL-methionine. J. Anim. Sci. 92:5530-5539. https://doi.org/10.2527/jas.2014-7830
  31. Song, D. and B. Park. 2012. Porcine epidemic diarrhoea virus: A comprehensive review of molecular epidemiology, diagnosis, and vaccines. Virus Genes 44:167-175. https://doi.org/10.1007/s11262-012-0713-1
  32. St-Pierre, N. R., B. Cobanov, and G. Schnitkey. 2003. Economic Losses from Heat Stress by US Livestock Industries. J. Dairy Sci. 86:E52-E77. https://doi.org/10.3168/jds.S0022-0302(03)74040-5
  33. Trent, M. S., C. M. Stead, A. X. Tran, and J. V. Hankins. 2006. Diversity of endotoxin and its impact on pathogenesis. J. Endotoxin Res. 12:205-223. https://doi.org/10.1179/096805106X118825
  34. Turner, J. R., B. K. Rill, S. L. Carlson, D. Carnes, R. Kerner, R. J. Mrsny, and J. L. Madara. 1997. Physiological regulation of epithelial tight junctions is associated with myosin light-chain phosphorylation. Am. J. Physiol-Cell Phys. 273:C1378-C1385. https://doi.org/10.1152/ajpcell.1997.273.4.C1378
  35. Upadhyay, R. C. 2011. Impact of climate change on livestock production and health. Proceeding of the ICICCA. Sri Lanka. pp. 19-39.
  36. Verbrugghe, E., V. Vandenbroucke, M. Dhaenens, N. Shearer, J. Goossens, S. De Saeger, M. Eeckhout, K. D'Herde, A. Thompson, D. Deforce, F. Boyen, B. Leyman, A. Van Parys, P. De Backer, F. Haesebrouck, S. Croubels, and F. Pasmans. 2012. T-2 toxin induced Salmonella Typhimurium intoxication results in decreased Salmonella numbers in the cecum contents of pigs, despite marked effects on Salmonella-host cell interactions. Vet. Res. 43:22. https://doi.org/10.1186/1297-9716-43-22
  37. Wang, W., Z. Wu, G. Lin, S. Hu, B. Wang, Z. Dai, and G. Wu. 2014. Glycine stimulates protein synthesis and inhibits oxidative stress in pig small intestinal epithelial cells. J. Nutr. 144:1540-1548. https://doi.org/10.3945/jn.114.194001
  38. Weaver, A. C., J. M. Campbell, J. D. Crenshaw, J. Polo, and S. W. Kim. 2014a. Efficacy of dietary spray dried plasma protein to mitigate the negative effects on performance of pigs fed diets with corn naturally contaminated with multiple mycotoxins. J. Anim. Sci. 92:3878-3886. https://doi.org/10.2527/jas.2013-6939
  39. Weaver, A. C., M. T. See, J. A. Hansen, Y. B. Kim, A. L. P. De Souza, T. F. Middleton, and S. W. Kim. 2013. The use of feed additives to reduce the effects of aflatoxin and deoxynivalenol on pig growth, organ health and immune status during chronic exposure. Toxins 5:1261-1281. https://doi.org/10.3390/toxins5071261
  40. Weaver, A. C., M. T. See, and S. W. Kim. 2014b. Protective effect of two yeast based feed additives on pigs chronically exposed to deoxynivalenol and zearalenone. Toxins 6:3336-3353. https://doi.org/10.3390/toxins6123336
  41. Wilson, A. D., K. Haverson, K. Southgate, P. W. Bland, C. R. Stokes, and M. Bailey. 1996. Expression of major histocompatibility complex class II antigens on normal porcine intestinal endothelium. Immunology 88:98-103. https://doi.org/10.1046/j.1365-2567.1996.d01-640.x
  42. Wu, L., P. Liao, L. He, W. Ren, J. Yin, J. Duan, and T. Li. 2015. Growth performance, serum biochemical profile, jejunal morphology, and the expression of nutrients transporter genes in deoxynivalenol (DON)- challenged growing pigs. BMC Vet. Res. 11:144. https://doi.org/10.1186/s12917-015-0449-y
  43. Xiao, D., Z. Tang, Y. Yin, B. Zhang, X. Hu, Z. Feng, and J. Wang. 2013. Effects of dietary administering chitosan on growth performance, jejunal morphology, jejunal mucosal sIgA, occludin, claudin-1 and TLR4 expression in weaned piglets challenged by enterotoxigenic Escherichia coli. Int. Immunopharmacol. 17:670-676. https://doi.org/10.1016/j.intimp.2013.07.023
  44. Xu, C., Y. Wang, R. Sun, X. Qiao, X. Shang, and W. Niu. 2014. Modulatory effects of vasoactive intestinal peptide on intestinal mucosal immunity and microbial community of weaned piglets challenged by an enterotoxigenic Escherichia coli (K88). PLoS One 9:e104183. https://doi.org/10.1371/journal.pone.0104183
  45. Xu, X., H. Zhang, Q. Zhang, J. Dong, Y. Liang, Y. Huang, H. J. Liu, and D. Tong. 2013a. Porcine epidemic diarrhea virus E protein causes endoplasmic reticulum stress and up-regulates interleukin-8 expression. Virol. J. 10:26. https://doi.org/10.1186/1743-422X-10-26
  46. Xu, X., H. Zhang, Q. Zhang, Y. Huang, J. Dong, Y. Liang, H. J. Liu, and D. Tong. 2013b. Porcine epidemic diarrhea virus N protein prolongs S-phase cell cycle, induces endoplasmic reticulum stress, and up-regulates interleukin-8 expression. Vet. Microbiol. 164:212-221. https://doi.org/10.1016/j.vetmic.2013.01.034
  47. Yang, K. M., Z. Y. Jiang, C. T. Zheng, L. Wang, and X. F. Yang. 2014. Effect of Lactobacillus plantarum on diarrhea and intestinal barrier function of young piglets challenged with enterotoxigenic Escherichia coli K88.J. Anim. Sci. 92:1496-1503. https://doi.org/10.2527/jas.2013-6619
  48. Zhao, Y., A. C. Weaver, V. Fellner, R. L. Payne, and S. W. Kim. 2014. Amino acid fortified diets for weanling pigs replacing fish meal and whey protein concentrate: Effects on growth, immune status, and gut health. J. Anim. Sci. Biotechnol. 5:57. https://doi.org/10.1186/2049-1891-5-57

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