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Branched-chain Amino Acids are Beneficial to Maintain Growth Performance and Intestinal Immune-related Function in Weaned Piglets Fed Protein Restricted Diet

  • Ren, M. (State Key Laboratory of Animal Nutrition, China Agricultural University) ;
  • Zhang, S.H. (State Key Laboratory of Animal Nutrition, China Agricultural University) ;
  • Zeng, X.F. (State Key Laboratory of Animal Nutrition, China Agricultural University) ;
  • Liu, H. (State Key Laboratory of Animal Nutrition, China Agricultural University) ;
  • Qiao, S.Y. (State Key Laboratory of Animal Nutrition, China Agricultural University)
  • Received : 2014.02.21
  • Accepted : 2014.06.24
  • Published : 2015.12.01

Abstract

As a novel approach for disease control and prevention, nutritional modulation of the intestinal health has been proved. However, It is still unknown whether branched-chain amino acid (BCAA) is needed to maintain intestinal immune-related function. The objective of this study was to determine whether BCAA supplementation in protein restricted diet affects growth performance, intestinal barrier function and modulates post-weaning gut disorders. One hundred and eight weaned piglets ($7.96{\pm}0.26kg$) were randomly fed one of the three diets including a control diet (21% crude protein [CP], CON), a protein restricted diet (17% CP, PR) and a BCAA diet (BCAA supplementation in the PR diet) for 14 d. The growth performance, plasma amino acid concentrations, small intestinal morphology and intestinal immunoglobulins were tested. First, average daily gain (ADG) (p<0.05) and average daily feed intake (ADFI) (p<0.05) of weaned pigs in PR group were lower, while gain:feed ratio was lower than the CON group (p<0.05). Compared with PR group, BCAA group improved ADG (p<0.05), ADFI (p<0.05) and feed:gain ratio (p<0.05) of piglets. The growth performance data between CON and BCAA groups was not different (p>0.05). The PR and BCAA treatments had a higher (p<0.05) plasma concentration of methionine and threonine than the CON treatment. The level of some essential and functional amino acids (such as arginine, phenylalanine, histidine, glutamine etc.) in plasma of the PR group was lower (p<0.05) than that of the CON group. Compared with CON group, BCAA supplementation significantly increased BCAA concentrations (p<0.01) and decreased urea concentration (p<0.01) in pig plasma indicating that the efficiency of dietary nitrogen utilization was increased. Compared with CON group, the small intestine of piglets fed PR diet showed villous atrophy, increasing of intra-epithelial lymphocytes (IELs) number (p<0.05) and declining of the immunoglobulin concentration, including jejunal immunoglobulin A (IgA) (p = 0.04), secreted IgA (sIgA) (p = 0.03) and immunoglobulin M (p = 0.08), and ileal IgA (p = 0.01) and immunoglobulin G (p = 0.08). The BCAA supplementation increased villous height in the duodenum (p<0.01), reversed the trend of an increasing IELs number. Notably, BCAA supplementation increased levels of jejunal and ileal immunoglobulin mentioned above. In conclusion, BCAA supplementation to protein restricted diet improved intestinal immune defense function by protecting villous morphology and by increasing levels of intestinal immunoglobulins in weaned piglets. Our finding has the important implication that BCAA may be used to reduce the negative effects of a protein restricted diet on growth performance and intestinal immunity in weaned piglets.

Keywords

References

  1. AOAC. 2007. Official Methods of Analysis. 18th ed. AOAC international, Gaithersburg, MD, USA.
  2. Calder, P. C. and P. Yaqoob. 1999. Glutamine and the immune system. Amino Acids 17:227-241. https://doi.org/10.1007/BF01366922
  3. Carr, L. E., A. Kelman, S. G. Wu, R. Gopaul, E. Senkevitch, A. Aghvanyan, A. M. Turay, and K. A. Frauwirth. 2010. Glutamine uptake and metabolism are coordinately regulated by ERK/MAPK during T lymphocyte activation. J. Immunol. 185:1037-1044. https://doi.org/10.4049/jimmunol.0903586
  4. Con, J., B. Joseph, N. Kulvatunyou, A. Tang, T. O'Keeffe, J. L. Wynne, R. S. Friese, P. Rhee, and R. Latifi. 2011. Evidencebased immune-modulating nutritional therapy in critically ill and injured patients. Eur. Surg. 43:13-18. https://doi.org/10.1007/s10353-011-0588-8
  5. Cummins, A. G. and F. M. Thompson. 2002. Effect of breast milk and weaning on epithelial growth of the small intestine in human. Gut 51:748-754. https://doi.org/10.1136/gut.51.5.748
  6. Doppenberg, J. and P. J. van der Aar. 2010. Dynamics in Animal Nutrition. Wageingen Accademic Publishers, Wageingen, The Netherlands. Page 31-36.
  7. Dugan, M. E. R., D. A. Knabe, and G. Wu. 1994. Glutamine and glucose metabolism in intraepithelial lymphocytes from preand post-weaning pigs. Comp. Biochem. Phys. B. Comp. Biochem. 109:675-681. https://doi.org/10.1016/0305-0491(94)90130-9
  8. Evoy, D., M. D. Lieberman, T. J. Fahey, and J. M. Daly. 1998. Immuninutrition: The role of arginine. Nutrition 14:611-617. https://doi.org/10.1016/S0899-9007(98)00005-7
  9. Figueroa, J. L., A. J. Lewis, P. S. Miller, R. L. Fischer, R. S. Gomez, and R. M. Diedrichsen. 2002. Nitrogen metabolism and growth performance of gilts fed standard maize-soybean meal diets or low-crude protein, amino acid supplemented diets. J. Anim. Sci. 80:2911-2919. https://doi.org/10.2527/2002.80112911x
  10. Guay, F., S. M. Donovan, and N. L. Trottier. 2006. Biochemical and morphological developments are practically impaired in intestinal mucosa from growing pigs fed reduced-protein diets supplemented with crystalline amino acids. J. Anim. Sci. 84:1749-1760. https://doi.org/10.2527/jas.2005-558
  11. Guy-Grand, D, J. P. DiSanto, P. Henchoz, M. Malassis-Seris, and P. Vassalli. 1998. Small bowel enteropathy: role of interepithelial lymphocytes and of cytokines (IL-12, $INF-{\gamma}$, TNF) in the induction of epithelial cell death and renewal. Eur. J. Immunol. 28:730-744. https://doi.org/10.1002/(SICI)1521-4141(199802)28:02<730::AID-IMMU730>3.0.CO;2-U
  12. Heo, J. M., J. C. Kim, C. F. Hansen, B. P. Mullan, D. J. Hanpson, and J. R. Pluske. 2008. Effects of feeding low protein diets to piglets on plasma urea nitrogen, faecal ammonia nitrogen, the incidence of diarrhoea and performance after weaning. Arch. Anim. Nutr. 62:343-358. https://doi.org/10.1080/17450390802327811
  13. Htoo, J. K., B. A. Araiza, W. C. Sauer, M. Rademacher, Y. Zhang, M. Cervantes, and R. T. Aijlstra. 2007. Effect of dietary protein content on ileal amino acid digestibility, growth performance, and formation of microbial metabolites in ileal and cecal digest of early-weaned pigs. J. Anim. Sci. 85:3303-3312. https://doi.org/10.2527/jas.2007-0105
  14. Kerr, B. J. 2003. Dietary manipulation to reduce environmental impact. Page139-158 in 9th International Symposium on Digestive Physiology in Pigs, May 14-17, 2003; Banff, Alberta, Canada.
  15. Kinnebrew, M. A. and E. G. Pamer. 2012. Innate immune signaling in defense against intestinal microbes. Immunol. Rev. 245:113-131. https://doi.org/10.1111/j.1600-065X.2011.01081.x
  16. Lalles, J. P., P. Bosi, H. Smidt, and C. R. Stokes. 2007. Nutritional management of gut health in pigs around weaning. Proc. Nutr. Soc. 66:260-268. https://doi.org/10.1017/S0029665107005484
  17. Li, P., Y. Yin, D. Li, S. W. Kim, and G. Wu. 2007. Amino acids and immune function. Br. J. Nutr. 98:237-252. https://doi.org/10.1017/S000711450769936X
  18. 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. https://doi.org/10.2527/jas.2007-0222
  19. Lundqvist, C., V. Baranov, S. Hammarstrom, L. Athlin, and M. L. Hammarstrom. 1995. Intra-epithelial lymphocytes. Evidence for regional specialization and extrathymic T cell maturation in the human gut epithelium. Int. Immunol. 7:1473-1487. https://doi.org/10.1093/intimm/7.9.1473
  20. Mao, X., X. Zeng, S. Qiao, G. Wu, and D. Li. 2011. Specific roles of threonine in intestinal mucosal integrity and barrier function. Front Biosci. E3:1192-1200. https://doi.org/10.2741/e322
  21. McCracken, B. A., H. R. Gaskins, P. J. Ruwe-Kaiser, K. C. Klasing, and D. E. Jewell. 1995. Diet-dependent and dietindependent metabolic responses underlie growth stasis of pigs at weaning. J. Nutr. 125:2838-2845.
  22. McGuckin, A. M., R. Eri, L. A. Simms, T. H. J. Florin, and G. Radford-Smith. 2009. Intestinal barrier dysfunction in inflammatory bowel diseases. Inflamm. Bowel Dis. 15:100-113. https://doi.org/10.1002/ibd.20539
  23. Miller, B. G., P. S. Jamies, M. W. Smith, and F. J. Bourne. 1986. Effect of weaning on the capacity of pig intestinal villi to digest and absorb nutrients. J. Agric. Sci. Camb. 107:579-589. https://doi.org/10.1017/S0021859600069756
  24. Moore, S. 1963. On the determination of cystine as cysteic acid. J. Biol. Chem. 238:235-237.
  25. Nabuurs, M. J., A. Hoogendoorn, E. J. V. Molen, and A. L. Van Osta. 1993. Villous height and crypt depth in weaned and unweaned pigs, reared under various circumstances in the Netherlands. Res. Vet. Sci. 55:78-84. https://doi.org/10.1016/0034-5288(93)90038-H
  26. NRC. 1998. Nutrient Requirements of Swine, 10th Edition. National Academy Press, Washington DC, USA.
  27. NRC. 2012. Nutrient Requirements of Swine, 11th Edition. National Academy Press, Washington DC, USA.
  28. Nofrarías, M., E. G. Manzanilla, J. Pujols, X. Gibert, N. Majo, J. Segales and J. Gasa. 2006. Effects of spray- dried porcine plasma and plant exreacts on intestinal morphology and on leukocyte cell subsets of weaned pigs. J. Anim. Sci. 84:2735-2742. https://doi.org/10.2527/jas.2005-414
  29. Nyachoti, C. M., F. O. Omoghenigun, M. Rademacher, and G. Blank. 2006. Performance responses and indicators of gastrointestinal health in early-weaned pigs fed low-protein amino acids-supplemented diets. J. Anim. Sci. 84:125-134. https://doi.org/10.2527/2006.841125x
  30. Oswald, I. P. 2006. Role of intestinal epithelial cells in the innate immune defence of the pig intestine. Vet. Res. 37:359-368. https://doi.org/10.1051/vetres:2006006
  31. Wijtten, J. A. P., J. van der Meulen, and M. W. A. Verstegen. 2011. Intestinal barrier function and absorption in pigs after weaning: A review. Br. J. Nutr. 105:967-981. https://doi.org/10.1017/S0007114510005660
  32. Pie, S., J. P. Lalle, F. Blazy, J. Laffitte, B. Seve, and I. P. Oswald. 2004. Weaning is associated with an upregulation of expression of inflammatory cytokines in the intestine of piglets. J. Nutr. 124:641-647.
  33. Pluske, J. R., M. J. Thompson, C. S. Atwood, P. H. Bird, I. H. Williams, and P. E. Hartmann. 1996. Maintenance of villous height and crypt depth, and enhancement of disaccharide digestion and monosaccharide absorption, in piglets fed on cows' whole milk after weaning. Br. J. Nutr. 76:409-422. https://doi.org/10.1079/BJN19960046
  34. Pomorska-Mol, M. and I. Markowska-Daniel. 2011. Porcine cathelicidins and defensins. Med. Weter 67:20-24.
  35. Powell, D. J., K. N. Pollizzi, E. B. Heikamp, and M. R. Horton. 2012. Regulation of immune responses by mTOR. Annu. Rev. Immunol. 30:39-68. https://doi.org/10.1146/annurev-immunol-020711-075024
  36. Rose, N., G. Larour, G. Le Digyerher, E. Everno, J. P. Jolly, P. Blanchard, A. Oger, M. Le Dimna, A. Jestin, and F. Madec. 2003. Risk factors for porcine post-weaning multisystemic wasting syndrome (PMWS) in 149 French farrow-to-finish herds. Prev. Vet. Med. 61:209-225. https://doi.org/10.1016/j.prevetmed.2003.07.003
  37. Santaolalla, R., M. Fukata, and M. T. Abreu. 2011. Innate immunity in the small intestine. Curr. Opin. Gastroenterol. 27:125-131. https://doi.org/10.1097/MOG.0b013e3283438dea
  38. Simone, D. R., F. Vissicchio, C. Mingarelli, C. D. Nuccio, S. Visentin, M. A. Ajmone-Cat, and L. Minghetti. 2013. Branched-chain amino acids influence the immune properties of microglial cells and their responsiveness to proinflammatory signals. Biochim. Biophys. Acta Mol. Basis Dis. 1832:650-659. https://doi.org/10.1016/j.bbadis.2013.02.001
  39. Smith, F., J. E. Clark, B. L. Overman, C. C. Tozel, J. H. Huang, J. E. F Rivier, A. T. Blisklager, and A. J. Moeser. 2010. Early weaning stress impairs development of mucosal barrier function in the porcine intestine. Am. J. Physiol. Gastrointest. Liver Physiol. 298:352-363. https://doi.org/10.1152/ajpgi.00081.2009
  40. Stoll, B., J. Henry, P. J. Reeds, H. Yu, F. Jahoor, and D. G. Burrin. 1998. Catabolism dominates the first-pass intestinal metabolism of dietary essential amino acids in milk protein-fed piglets. J. Nutr. 128:606-614. https://doi.org/10.1093/jn/128.3.606
  41. Tan, B., X. G. Li, X. Kong, R. Huang, Z. Ruan, K. Yao, Z. Deng, M. Xie, I. Shinzato, Y. Yin, and G. Wu. 2009. Dietary Larginine supplementation enhances the immune status in earlyweaned pglets. Amino Acids. 37:323-331. https://doi.org/10.1007/s00726-008-0155-1
  42. Wang, J. J., L. Chen, P. Li, X. Li, H. Zhou, F. Wang, D. Li, Y. Yin, and G. Wu. 2008. Gene expression is altered in piglet small intestine by weaning and dietary glutamine supplementation. J. Nutr. 138:1025-1032. https://doi.org/10.1093/jn/138.6.1025
  43. Wells, J. M., L. M. P. Loonen, and J. M. Karczewski. 2010. The role of innate signalling in the homeostasis of tolerance and immunity in the intestine. Int. J. Med. Microbiol. 300:41-48. https://doi.org/10.1016/j.ijmm.2009.08.008
  44. Wu, G. 1998. Intestinal mucosal amino acid catabolism. J. Nutr. 128:1249-1252. https://doi.org/10.1093/jn/128.8.1249
  45. Wu, G. 2009. Amino acids: Metabolism, functions, and nutrition. Amino Acids 37:1-17.
  46. Yoneda, J., A. Andou, and K. Takehana. 2009. Regulatory roles of amino acids in immune response. Curr. Rheumatol. Rev. 5:252-258. https://doi.org/10.2174/157339709790192567
  47. Yue, L. Y. and S. Y. Qiao. 2007. 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.
  48. Zhang, F., X. Zeng, F. Yang, Z. Huang, H. Liu, X. Ma, and S. Qiao. 2013. Dietary N-carbamylglutamate supplementation boosts intestinal mucosal immunity in Escherichia coli challenged piglets. Plos One. 8(6):e66280. https://doi.org/10.1371/journal.pone.0066280
  49. Zhu, H. L., Y. L. Liu, X. L. Xie, J. J. Huang, and Y. Q. Hou. 2013. Effect of L-arginine on intestinal mucosal immune barrier function in weaned pigs after Escherichia coli LPS challenge. Innate Immun. 19:242-252. https://doi.org/10.1177/1753425912456223
  50. Zijlstra, R. T., J. Odle, W. F. Hall, B. W. Petschow, H. B. Gelbery, and R. E. Litov. 1994. Effect of orally administered epidermal growth factor on intestinal recovery of neonatal pigs infected with rotavirus. J. Pediatr. Gastroenterol. Nutr. 19:382-390. https://doi.org/10.1097/00005176-199411000-00003

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