Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
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Dietary L-arginine Supplementation Improves Intestinal Function in Weaned Pigs after an Escherichia coli Lipopolysaccharide Challenge

  • Liu, Yulan (State Key Laboratory of Animal Nutrition, China Agricultural University) ;
  • Han, Jie (Hubei Key Laboratory of Animal Nutrition and Feed Science, Wuhan Polytechnic University) ;
  • Huang, Jingjing (Hubei Key Laboratory of Animal Nutrition and Feed Science, Wuhan Polytechnic University) ;
  • Wang, Xiaoqiu (State Key Laboratory of Animal Nutrition, China Agricultural University) ;
  • Wang, Fenglai (State Key Laboratory of Animal Nutrition, China Agricultural University) ;
  • Wang, Junjun (State Key Laboratory of Animal Nutrition, China Agricultural University)
  • Received : 2009.02.06
  • Accepted : 2009.07.02
  • Published : 2009.12.01
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Abstract

This study was conducted to determine whether L-arginine (Arg) supplementation could improve intestinal function in weaned pigs after an Escherichia coli lipopolysaccharide (LPS) challenge. Treatments included: i) non-challenged control (CONTR, pigs fed a control diet and injected with sterile saline); ii) LPS-challenged control (LPS, pigs fed the same control diet and challenged by injection with Escherichia coli LPS); iii) LPS+0.5% Arg (pigs fed a 0.5% Arg diet and challenged with LPS); and iv) LPS+1.0% Arg (pigs fed a 1.0% Arg diet and challenged with LPS). On d 16, pigs were administrated with LPS or sterile saline. D-xylose was orally administrated at 2 h following LPS challenge, and blood samples were collected at 3 h following LPS challenge. At 6 h post-challenge, pigs were sacrificed and intestinal mucosa samples were collected. Supplementation of Arg attenuated LPS-induced damage in gut digestive and barrier functions, as indicated by an increase in ileal lactase activity, and duodenal and ileal diamine oxidase activities (p<0.05). Arg administration also prevented the increase of jejunal malondialdehyde content and the decrease of ileal superoxide dismutase activity by LPS challenge (p<0.05). Furthermore, the jejunal nitric oxide level and inducible nitric oxide synthase activity were also improved after Arg supplementation (p<0.05). These results indicate that Arg supplementation has beneficial effects in alleviating the impairment of gut function induced by LPS challenge.

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References

  1. AOAC. 1990. Official methods of analysis (15th Ed.). Association of Official Analytical Chemists, Washington, DC
  2. Chander, V. and K. Chopra. 2005. Renal protective effect of molsidomine and L-arginine in ischemia-reperfusion induced injury in rats. J. Surg. Res. 128:132-139 https://doi.org/10.1016/j.jss.2005.04.023
  3. Corl, B. A., J. Odle, X. M. Niu, A. J. Moeser, L. A. Gatlin, O. T. Phillips, A. T. Blikslager and J. M. Rhoads. 2008. Arginine activates intestinal $p70^{s6k}$ and protein synthesis in piglet rotavirus enteritis. J. Nutr. 138:24-29
  4. Fang, Y. Z., S. Yang and G. Y. Wu. 2002. Free radicals, antioxidants, and nutrition. Nutrition 18:872-879 https://doi.org/10.1016/S0899-9007(02)00916-4
  5. Fink, M. P., J. B. Antonsson, H. L. Wang and H. R. Rothschild. 1991. Increased intestinal permeability in endotoxic pigs. Mesenteric hypoperfusion as an etiologic factor. Arch. Surg. 126:211-218 https://doi.org/10.1001/archsurg.1991.01410260101014
  6. Fotiadis, C., S. Adamis, E. P. Misiakos, M. Genetzakis, P. T. Antonakis, D. K. Tsekouras, V. G. Gorgoulis, G. C. Zografos, A. Papalois, M. Fotinou and D. Perrea. 2007. The prophylactic effect of L-arginine in acute ischaemic colitis in a rat model of ischaemia/reperfusion injury. Acta Chir. Belg. 107:192-200
  7. Gao, C. J., W. Chai, L. X. Xu, G. H. Zhang, H. Zhang, L. C. Han and X. D. Sun. 2006. Protective effects of hyperoxygenated solution preconditioning on intestinal ischemia-reperfusion injury in rabbits. J. Surg. Res. 135:268-274 https://doi.org/10.1016/j.jss.2006.03.019
  8. Gurbuz, A. T., J. Kunzelman and E. E. Ratzer. 1998. Supplemental dietary arginine accelerates intestinal mucosal regeneration and enhances bacterial clearance following radiation enteritis in rats. J. Surg. Res. 74:149-154 https://doi.org/10.1006/jsre.1997.5231
  9. Hampson, D. J. and D. E. Kidder. 1986. Influence of creep feeding and weaning on brush border enzyme activities in the piglet small intestine. Res. Vet. Sci. 40:24-31
  10. Han, J., Y. L. Liu, W. Fan, J. Chao, Y. Q. Hou, Y. L. Yin, H. L. Zhu, G. Q. Meng and Z. Q. Che. 2008. Dietary L-arginine supplementation alleviates immunosuppression induced by cyclophosphamide in weaned pigs. Amino Acids 10.1007/s00726-008-0184-9
  11. Hou, Y. Q., Y. L. Liu, J. Hu and W. H. Shen. 2006. Effects of lactitol and tributyrin on growth performance, small intestinal morphology and enzyme activity in weaned pigs. Asian-Aust. J. Anim. Sci. 19:1470-1477
  12. Kobayashi, H., T. Nonami, T. Kurokawa, Y. Takeuchi, A. Harada, A. Nakao and H. Takagi. 1995. Role of endogenous nitric oxide in ischemia-reperfusion injury in rat liver. J. Surg. Res. 59:772-779 https://doi.org/10.1006/jsre.1995.1238
  13. Kohli, R., C. J. Meininger, T. E. Haynes, W. Yan, J. T. Self and G. Wu. 2004. Dietary L-arginine supplementation enhances endothelial nitric oxide synthesis in streptozotocin-induced diabetic rats. J. Nutr. 134:600-608
  14. Kruzel, M. L., Y. Harari, C. Y. Chen and G. A. Castro. 2000. Lactoferrin protects gut mucosal integrity during endotoxemia induced by lipopolysaccharide in mice. Inflammation 24:33-44 https://doi.org/10.1023/A:1006935908960
  15. Liu, G. P., W. P. Zhou, W. X. Zhu, G. M. Cheng, S. J. Jiang and S. G. He. 2003. The protective effect of L-arginine on the intestine barrier of rats with obstructive jaundice. J. Hepatobiliary Surg. 11:153-154 (Chinese)
  16. Liu, K. X., T. Rinne, W. He, F. Wang and Z. Y. Xia. 2007. Propofol attenuates intestinal mucosa injury induced by intestinal ischemia-reperfusion in the rat. Can. J. Anesth. 54:366-374 https://doi.org/10.1007/BF03022659
  17. Liu, Y., H. Liu and Q. Y. Kong. 2005. The roles of superoxide dismutase, nitric oxide synthase and nitric oxide in the antitumor mechanism of arsenic trioxide. Acta Acad. Med. Xuzhou. 25:8-12
  18. Liu, Y. L., J. J. Huang, Y. Q. Hou, H. L. Zhu, S. J. Zhao, B. Y. Ding, Y. L. Yin, G. F. Yi, J. X. Shi and W. Fan. 2008a. Dietary arginine supplementation alleviates intestinal mucosal disruption induced by Escherichia coli lipopolysaccharide in weaned pigs. Br. J. Nutr. 100:552-560 https://doi.org/10.1017/S0007114508911612
  19. Liu, Y. L., J. Lu, J. X. Shi, Y. Q. Hou, H. L. Zhu, S. J. Zhao, H. M. Liu, B. Y. Ding, Y. L. Yin and G. F. Yi. 2008b. Increased expression of the peroxisome proliferator-activated receptor $\gamma$ in the immune system of weaned pigs after Escherichia coli lipopolysaccharide challenge. Vet. Immunol. Immunopathol. 124:82-92 https://doi.org/10.1016/j.vetimm.2008.02.014
  20. Lowry, O. H., N. J. Rosebrough, A. L. Farr and R. J. Randall. 1951. Protein measurement with folin phenol reagent. J. Biol. Chem. 193:265-275
  21. Mansoori, B., H. Nodeh, M. Modirsanei, S. Rahbari and P. Aparnak. 2009. d-Xylose absorption test: A tool for the assessment of the effect of anticoccidials on the intestinal absorptive capacity of broilers during experimental coccidiosis. Anim. Feed Sci. Technol. 148:301-308 https://doi.org/10.1016/j.anifeedsci.2008.04.009
  22. Mercer, D. W., G. S. Smith, J. M. Cross, D. H. Russell, L. Chang and J. Cacioppo. 1996. Effects of lipopolysaccharide on intestinal injury: potential role of nitric oxide and lipid peroxidation. J. Surg. Res. 63:185-192 https://doi.org/10.1006/jsre.1996.0245
  23. Miguez, I., G. Marino, B. Rodríguez and C. Taboada. 2004. Effects of dietary L-arginine supplementation on serum lipids and intestinal enzyme activities in diabetic rats. J. Physiol. Biochem. 60:31-37 https://doi.org/10.1007/BF03168218
  24. NRC. 1998. Nutrient requirements of swine (10th Ed.). National Academic Press, Washington, DC
  25. Orlando, G. F., G. Wolf and M. Engelmann. 2008. Role of neuronal nitric oxide synthase in the regulation of the neuroendocrine stress response in rodents: insights from mutant mice. Amino Acids 35:17-27 https://doi.org/10.1007/s00726-007-0630-0
  26. Peng, X., H. Yan, Z. Y. You, P. Wang and S. L. Wang. 2004. Effects of enteral supplementation with glutamine granules on intestinal mucosal barrier function in severe burned patients. Burns 30:135-139 https://doi.org/10.1016/j.burns.2003.09.032
  27. Rhoden, E. L., L. Pereira-Lima, C. R. Rhoden, M. L. Lucas, C. Teloken and A. Bello-Klein. 2001. Role of the L-arginine/nitric oxide pathway in renal ischaemia-reperfusion in rats. Eur. J. Surg. 167:224-228 https://doi.org/10.1080/110241501750099537
  28. Schleiffer, R. and F. Raul. 1996. Prophylactic administration of Larginine improves the intestinal barrier function after mesenteric ischaemia. Gut 39:194-198 https://doi.org/10.1136/gut.39.2.194
  29. Semrad, S. D. 2005. Malassimilation syndromes in large animals. In: Merck veterinary manual, ninth ed. (Ed. C. M. Kahn). Merck Co. Inc., Whitehouse Station, NJ, USA. pp. 301-306
  30. Spanos, C. P., P. Papaconstantinou, P. Spanos, M. Karamouzis, G. Lekkas and C. Papaconstantinou. 2007. The effect of Larginine and aprotinin on intestinal ischemia-reperfusion injury. J. Gastrointest. Surg. 11:247-255 https://doi.org/10.1007/s11605-007-0102-6
  31. Sukhotnik, I., J. Mogilner, M. M. Krausz, M. Lurie, M. Hirsh, A. G. Coran and E. Shiloni. 2004. Oral arginine reduces gut mucosal injury caused by lipopolysaccharide endotoxemia in rat. J. Surg. Res. 122:256-262 https://doi.org/10.1016/j.jss.2004.07.004
  32. Sukhotnik, I., H. Helou, J. Mogilner, M. Lurie, A. Bernsteyn, A. G. Coran and E. Shiloni. 2005. Oral arginine improves intestinal recovery following ischemia-reperfusion injury in rat. Pediatr. Surg. Int. 21:191-196 https://doi.org/10.1007/s00383-004-1318-0
  33. Verdonk, J. M. A. J., M. A. M. Spreeuwenberg, G. C. M. Bakker and M. W. A. Verstegen. 2001. Nutrient intake level affects histology and permeability of the small intestine in newly weaned piglets. In Digestive physiology of pigs (Ed. J. E. Lindberg and B. Ogle). pp. 332-334. Wallingford, UK: CABI Publishing
  34. Wang, J. J., L. X. Chen, D. F. Li, Y. L. Yin, X. Q. Wang, P. Li, L. J. Dangott, W. X. Hu and G. Y. Wu. 2008a. Intrauterine growth restriction affects the proteomes of the small intestine, liver, and skeletal muscle in newborn pigs. J. Nutr. 138:60-66
  35. Wang, J. J., L. X. Chen, P. Li, X. L. Li, H. J. Zhou, F. L. Wang, D. F. Li, Y. L. Yin and G. Y. Wu. 2008b. Gene expression is altered in piglet small intestine by weaning and dietary glutamine supplementation. J. Nutr. 138:1025-1032
  36. Wang, W. W., S. Y. Qiao and D. F. Li. 2009. Amino acids and gut function. Amino Acids 37:105-110 https://doi.org/10.1007/s00726-008-0152-4
  37. Wu, G., F. W. Bazer, T. A. Cudd, W. S. Jobgen, S. W. Kim, A. Lassala, P. Li, J. H. Matis, C. J. Meininger and T. E. Spencer. 2007a. Pharmacokinetics and safety of arginine supplementation in animals. J. Nutr. 137:1673S-1680S https://doi.org/10.1017/S000711450769936X
  38. Wu, G., F. W. Bazer, T. A. Davis, L. A. Jaeger, G. A. Johnson, S. W. Kim, D. A. Knabe, C. J. Meininger, T. E. Spencer and Y. L. Yin. 2007b. Important roles for the arginine family of amino acids in swine nutrition and production. Livest. Sci. 112:8-22 https://doi.org/10.1016/j.livsci.2007.07.003
  39. Wu, G., D. A. Knabe and S. W. Kim. 2004. Arginine nutrition in neonatal pigs. J. Nutr. 134:2783S-2390S
  40. Wu, G., C. J. Meininger, D. A. Knabe, F. W. Bazer and J. M. Rhoads. 2000. Arginine nutrition in development, health and disease. Curr. Opin. Clin. Nutr. Metab. Care 3:59-66 https://doi.org/10.1097/00075197-200001000-00010
  41. Yao, K., Y. L. Yin, W. Y. Chu, Z. Q. Liu, D. Deng, T. J. Li, R. L. Huang, J.S. Zhang, B. Tan, W. C. Wang and G. Y. Wu. 2008. Dietary arginine supplementation increases mTOR signaling activity in skeletal muscle of neonatal pigs. J. Nutr. 138:867-872 https://doi.org/10.1007/s00726-008-0176-9
  42. Zhan, Z. F., D. Y. Ou, X. S. Piao, S. W. Kim, Y. H. Liu and J. J. Wang. 2008. Dietary arginine supplementation affects microvascular development in the small intestine of earlyweaned pigs. J. Nutr. 138:1304-1309
  43. Zhang, C., Z. Y. Sheng, S. Hu, J. C. Gao, S. Yu and Y. Liu. 2002. The influence of apoptosis of mucosal epithelial cells on intestinal barrier integrity after scald in rats. Burns 28:731-737 https://doi.org/10.1016/S0305-4179(02)00210-3
  44. Zhang, L. P., C. Y. Yang, Y. P. Wang, F. Cui and Y. Zhang. 2008. Protective effect of polydatin against ischemia/reperfusion injury in rat heart. Acta Physiologica Sinica 60:161-168
  45. Zheng, C. T., T. Wang, Z. N. Lu, S. G. Zou, R. J. Xu and J. S. Zhang. 1999. EFfects of oral insulin and trypsinized formula milk on small intestinal growth and development in newborn pigs. Acta Veterinaria et Zootechnica Sinica. 30:405-413 (Chinese)

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