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Effects of Lactitol and Tributyrin on Growth Performance, Small Intestinal Morphology and Enzyme Activity in Weaned Pigs

  • Hou, Y.Q. (Hubei Key Laboratory of Animal Nutrition and Feed Science, Wuhan Polytechnic University) ;
  • Liu, Y.L. (Hubei Key Laboratory of Animal Nutrition and Feed Science, Wuhan Polytechnic University) ;
  • Hu, J. (Hubei Key Laboratory of Animal Nutrition and Feed Science, Wuhan Polytechnic University) ;
  • Shen, W.H. (Department of Pediatrics, Indiana University School of Medicine)
  • Received : 2005.11.18
  • Accepted : 2006.04.03
  • Published : 2006.10.01

Abstract

One hundred and sixty crossbred pigs ($6.62{\pm}0.36kg$) weaned at day $18{\pm}1$ were used to investigate the effects of lactitol and tributyrin on performance, small intestinal morphology and enzyme activity. The pigs were assigned to one of five dietary groups (4 pens/diet with 8 pigs/pen) and were fed the negative control diet or the negative control diet supplemented with 10 g/kg glutamine (as a positive control), or 3 g/kg lactitol (${\beta}$-D-galactopyranosyl-($1{\rightarrow}4$)-D-sorbitol), or 5 g/kg tributyrin (butanoic acid 1,2,3-propanetriyl ester), or 3 g/kg lactitol+5 g/kg tributyrin. Body weight and feed intake were measured weekly during the 4-week study. On day 7, four pigs per dietary treatment were sacrificed to examine small intestinal morphology and enzyme activity. The results showed that: (1) Compared with the negative control diet, the positive control diet improved weight gain and feed efficiency during weeks 1-2 and over the entire study (p<0.05), and also decreased duodenal and ileal crypt depth (p<0.05), but did not alter intestinal enzyme activity (p>0.05). Lactitol improved feed efficiency during weeks 3-4 and over the entire study (p<0.05), but did not improve weight gain and feed intake, intestinal morphology or enzyme activity (p>0.05). Tributyrin improved weight gain and reduced feed/gain during weeks 3-4 and over the entire study. Tributyrin significantly decreased crypt depth in the duodenum and ileum, and increased duodenal lactase and ileal maltase activity (p<0.05). Lactitol+tributyrin increased weight gain during weeks 3-4 and over the entire study, and improved feed efficiency during weeks 1-2 and 3-4 and over the entire study (p<0.05). Lactitol+tributyrin increased the jejunal villus height, and decreased the duodenal and ileal crypt depth (p<0.05). Lactitol+tributyrin also increased jejunal lactase and sucrase activity (p<0.05). (2) Compared with the positive control, tributyrin improved weight gain and reduced feed/gain during weeks 3-4 (p<0.05), decreased the ileal crypt depth, and improved the duodenal lactase and sucrase activity (p<0.05). Lactitol+ tributyrin improved weight gain during weeks 3-4, improved feed efficiency during weeks 3-4 and over the entire study, increased the ileal villus height, and increased jejunal lactase, sucrase and maltase activity (p<0.05). These results showed that tributyrin improved performance, intestinal morphology and enzyme activity, while the effect of lactitol was very limited. These results also showed that, compared with glutamine, tributyrin was more effective in improving intestinal morphology and enzyme activity, and tributyrin exerted a superior effect in improving performance as weaning progressed. These observations suggest that, as a chemical for repairing intestinal atrophy, glutamine and tributyrin should be used in the first and second periods of the starter phase, respectively.

Keywords

References

  1. Argenzio, R. A., J. A. Liacos, M. L. Levy, D. J. Meuten, J. G. Lecce and D. W. Powell. 1990. Villous atrophy, crypt hyperplasia, cellular infiltration, and impaired glucose-Na absorption in enteric cryptosporidiosis of pigs. Gastroenterol. 98:1129-1140 https://doi.org/10.1016/0016-5085(90)90325-U
  2. Ayonrinde, A. I., I. H. Williams, R. Mccauley and B. P. Mullan. 1995. Glutamine stimulates intestinal hyperplasia in weaned piglet. In Manipulating Pig Production (Ed. V. D. P. Hennessy and P. D. Cranwell). Australasian Pig Science Association, Werribee, Australia, pp. 180
  3. Cera, K. R., D. C. Mahan, R. F. Cross, G. A. Reinhart and R. E. Whitmoyer. 1988. Effect of age, weaning and postweaning diet on small intestinal growth and jejunal morphology in young swine. J. Anim. Sci. 66:574-584 https://doi.org/10.2527/jas1988.662574x
  4. Dahlqvist, A. and C. Nordström. 1966. The distribution of disaccharidase activities in the villi and crypts of the smallintestinal mucosa. Biochim. Biophys. Acta 113:624-626 https://doi.org/10.1016/S0926-6593(66)80024-3
  5. Gay, C. C., I. K. Barker and P. Moore. 1976. Changes in piglet intestinal villous structure and intestinal enzyme activity associated with weaning. In: Proceedings of the IVth IPVS Congress (Ed. W. E. Brandt, R. D. Glock, D. L. Harris, N. E. Hutton and A. D. Lennon). College of Veterinary Medicine. Iowa State University. Ames. IA. USA
  6. Hampson, D. J. and D. C. Kidder. 1986. Influence of creep feeding and weaning on brush border enzyme activities in the piglet small intestine. Res. Vet. Sci. 40:24-31
  7. Hampson, D. J. 1986a. Alterations in piglet small intestinal structure at weaning. Res. Vet. Sci. 40:32-40
  8. Hampson, D. J. 1986b. Attempts to modify changes in the piglet small intestine after weaning. Res. Vet. Sci. 40:313-317
  9. Hornich, M., E. Salajka, L. Ulmann, Z. Sarmanova and M. Sedlacek. 1973. Enteric Escherichia coli infections. Morphological findings in the intestinal mucosa of healthy and diseased piglets. Vet. Pathol. 10:484-500 https://doi.org/10.1177/030098587301000602
  10. James, P. S., M. W. Smith, D. R. Tivey and T. J. G. Wilson. 1987. Epidermal growth factor selectively increases maltase and sucrase activities in neonatal piglet intestine. J. Physiol. 293:583-594
  11. Kelly, D., J. A. Smyth and K. J. McCracken. 1991a. Digestive development of the early-weaned pig: I. Effect of continuous nutrient supply on the development of the digestive tract and on changes in digestive enzyme activity during the first week post-weaning. Br. J. Nutr. 65:169-180 https://doi.org/10.1079/BJN19910078
  12. Kelly, D., J. A. Smyth and K. J. McCracken. 1991b. Digestive development of the early-weaned pig: II. Effect of level of food intake on digestive enzyme activity during the immediate post-weaning period. Br. J. Nutr. 65:181-188 https://doi.org/10.1079/BJN19910079
  13. Kelly, D., J. A. Smyth and K. J. McCracken. 1990. Effect of creep feeding on structural and functional changes of the gut of early weaned pigs. Res. Vet. Sci. 48:350-356
  14. Kelly, D. 1990. Effect of creep feeding on the incidence, duration and severity of post-weaning diarrhoea. Res. Vet. Sci. 49:223-228
  15. Kenworthy, R. 1976. Observations on the effects of weaning in the young pig. Clinical and histopathological studies of intestinal function and morphology. Res. Vet. Sci. 21:69-75
  16. Kidder, D. E. and M. J. Manners. 1980. The level and distribution of carbohydrases in the small intestine mucosa of pigs from 3 weeks of age to maturity. Br. J. Nutr. 43:141-153 https://doi.org/10.1079/BJN19800073
  17. Lee, D. N., C. F. Wang, Y. H. Cheng, T. Y. Kuo, J. F. Wu and H. T. Yen. 2003. Dietary glutamine supplementation enhances weaned pigs mitogen-induced lymphocyte proliferation. Asian-Aust. J. Anim. Sci. 16:1182-1187 https://doi.org/10.5713/ajas.2003.1182
  18. Lee, D. N., Y. H. Cheng, F. Y. Wu, H. Sato, I. Shinzato, S. P. Chen and H. T. Yen. 2003. Effect of dietary glutamine supplement on performance and intestinal morphology of weaned pigs. Asian-Aust. J. Anim. Sci. 16:1770-1776 https://doi.org/10.5713/ajas.2003.1770
  19. Li, D. F., R. C. Thaler, J. L. Nelssen, D. L. Harmon, G. L. Allee and T. L. Weeden. 1990. Effect of fat sources and combinations on starter pig performance, nutrient digestibility and intestinal morphology. J. Anim. Sci. 68:3694-3704 https://doi.org/10.2527/1990.68113694x
  20. Lindemann, M. D., S. G. Cornelius, S. M. E. Kandelgy, R. L. Moser and J. E. Pettigew. 1986. Effect of age, weaning and diet on digestive enzyme levels in the piglet. J. Anim. Sci. 62:1298-1307 https://doi.org/10.2527/jas1986.6251298x
  21. Liu, T. 2002. Effects of glutamine on the trophic status of the intestinal tract and immune function of early-weaned piglets. Ph.D. Dissertation, Huzhong Agricultural University, Wuhan, China. pp. 35-41
  22. Liu, T., J. Peng, Y. Z. Xiong, S. Q. Zhou and X. H. Cheng. 2002. Effects of dietary glutamine and glutamate supplementation on small intestinal structure, active absorption and DNA, RNA concentrations in skeletal muscle tissue of weaned piglets during d 28 to 42 of age. Asian-Aust. J. Anim. Sci. 15:238-242 https://doi.org/10.5713/ajas.2002.238
  23. Luchansky, J. B. 2000. Use of biotherapeutics to enhance animal well being and food safety. In Proceedings of the 6th International Feed Production Conference, Piacenza, Italy. pp. 188-194
  24. Luna, L. G. 1968. Manual of histologic staining methods of the armed forces institute of pathology. 3rd ed. McGraw-Hill Book Company, New York. p. 258
  25. Manners, M. J. and J. A. Stevens. 1972. Changes from birth to maturity in the pattern of distribution of lactase and sucrase activity in the mucosa of the small intestine of pigs. Br. J. Nutr. 28:113-127 https://doi.org/10.1079/BJN19720014
  26. Miller, B. G., P. S. James, M. W. Smith and F. J. Bourne. 1986. Effect of weaning on the capacity of pig intestinal villi to digest and absorb nutrient. J. Agric. Sci. Cambridge 107:579- 589 https://doi.org/10.1017/S0021859600069756
  27. Nabuurs, M. J. A., A. Hoogendoorn, E. J. van der Molen and A. L. M. van Osta. 1993. Villus 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
  28. Nordstrom, C. and A. Dahlqvist. 1973. Quantitative distribution of some enzymes along the villi and crypts of human small intestine. Scand. J. Gastroentero. 8:407-416 https://doi.org/10.1159/000197344
  29. NRC. 1998. Nutrient Requirements of Swine (10th Ed.). National Academic Press, Washington, DC
  30. Piva, A., A. Panciroli, E. Meola and A. Formigoni. 1996. Lactitol enhances short-chain fatty acid and gas production by swine cecal microflora to a greater extent when fermenting low rather than high fiber diets. J. Nutr. 126:280-289 https://doi.org/10.1093/jn/126.1.280
  31. Piva, A., A. Prandini, L. Fiorentini, M. Morlacchini, F. Galvano and J. B. Luchansky. 2002. Tributyrin and lactitol synergistically enhanced the trophic status of the intestinal mucosa and reduced histamine levels in the gut of nursery pigs. J. Anim. Sci. 80:670-680
  32. Pluske, J. R. 2001. Morphological and functional changes in the small intestine of the newly weaned pig. In: Gut Environment of Pigs (Ed. A. Piva, K. E. Bach Knudsen and J. E. Lindberg). Nottingham University Press, Nottingham, UK. pp. 1-27
  33. Pluske, J. R., I. H. Williams and F. X. Aherne. 1996a. Maintenance of villus height and crypt depth in piglets by providing continuous nutrition after weaning. J. Anim. Sci. 62:131-144 https://doi.org/10.1017/S1357729800014417
  34. Pluske, J. R., I. H. Williams and F. X. Aherne. 1996b. Villus height and crypt depth in piglets in response to increases in the intake of cows' milk after weaning. J. Anim. Sci. 62:145-158 https://doi.org/10.1017/S1357729800014429
  35. Roediger, W. E. 1980. Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man. Gut 21:793-798 https://doi.org/10.1136/gut.21.9.793
  36. Scheppach, W., J. G. Muller, F. Boxberger, G. Dusel, F. Richter, H. P. Bartram, S. U. Christl, C. E. Dempfle and H. Kasper. 1997. Histological changes in the colonic mucosa following irrigation with short-chain fatty acids. Eur. J. Gastroenterol. Hepatol. 9:163-168 https://doi.org/10.1097/00042737-199702000-00010
  37. Schroder, O., S. Hess, W. F. Caspary and J. Stein. 1999. Mediation of differentiating effects of butyrate on the intestinal cell line Caco-2 by transforming growth factor-beta 1. Eur. J. Nutr. 38:45-50 https://doi.org/10.1007/s003940050045
  38. Shinzato, I., S. Chen, H. Yen, D. Lee, Y. Cheng, F. Wu and H. Sato. 2003. Effect of dietary glutamine supplement on performance and intestinal morphology of weaned pigs. Asian-Aust. J. Anim. Sci. 16:1770-1776 https://doi.org/10.5713/ajas.2003.1770
  39. Souba, W. W., V. S. Klimberg and D. A. Plumley. 1990. The role of glutamine in maintaining a healthy gut and supporting the metabolic response to injury and infecction. J. Surg. Res. 48:383-391 https://doi.org/10.1016/0022-4804(90)90080-L
  40. SPSS Inc. 1993. SPSS for Windows Base System User's Guide Release 6.0. SPSS Inc., Chicago, IL
  41. van Beers-Schreurs, H. G. M. 1996. The changes in the function of the large intestine of weaned pigs. Ph.D. thesis. Univ. of Utrecht, The Netherlands
  42. von Engelhardt, W., J. Bartels, S. Kirschberger, H. D. Meyer zu Düttingdorf and R. Busche. 1998. Role of short-chain fatty acids in the hindgut. Vet. Q. 20:S52-S59 https://doi.org/10.1080/01652176.1998.9694970
  43. Wu, G. and D. A. Knabe. 1994. Free and protein-bound amino acids in sow's colostrum and milk. J. Nutr. 124:415-424
  44. Wu, G., S. A. Meier and D. A. Knabe. 1996. Dietary glutamine supplementation prevents jejunal atrophy in weaned pigs. J. Nutr. 126:2578-2584
  45. Zhang, J. M., Z. C. Gao, L. D. Wang, Y. X. Jiang and Q. Zhang. 2001. Effect of dietary glutamine supplementation on intestinal enzymes of early-weaned piglets. Acta Zoonutrimenta Sinica 13, 18-23
  46. Zhang, J. M. and Z. C. Gao. 2002. Effectof glutamine supplementation on intestinal mucosa protein, DNA and mucosa morphology of early-weaned piglets. Scientia Agricultura Sinica 35:1264-1268
  47. Zijlstra, R. T., K. -Y. Whang, R. A. Easter and J. Odle. 1996. Effect of feeding a milk replacer to early weaned pigs on growth, body composition, and small intestinal morphology, compared with suckled littermates. J. Anim. Sci. 74:2948-2959

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