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Villous height and crypt depth in piglets in response to increases in the intake of cows' milk after weaning

Published online by Cambridge University Press:  02 September 2010

J. R. Pluske
Affiliation:
Animal Science, Faculty of Agriculture, University of Western Australia, Nedlands, WA 6907, Australia
I. H. Williams
Affiliation:
Animal Science, Faculty of Agriculture, University of Western Australia, Nedlands, WA 6907, Australia
F. X. Aherne
Affiliation:
Department of Agricultural, Food and Nutritional Sciences, University of Alberta, Edmonton AB T6G 2P5, Canada
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Abstract

The hypothesis tested in this experiment was that the structure and function of the small intestine of piglets given a milk liquid diet after weaning depends on their level of energy intake. At weaning (28 days), 42 piglets were allocated to one of five treatments: (1) control group killed at weaning; (2) piglets offered a dry starter diet ad libitum; (3) piglets given cow's fresh milk at maintenance energy intake (Ma); (4) piglets given cow's fresh milk at 2-5 Ma; and (5) piglets given cow's fresh milk ad libitum. On the 5th day all piglets were killed and samples of gut were taken for histological and biochemical examination. Piglets given milk ad libitum grew faster (P < 0·001) than piglets on all other treatments. Piglets offered the dry starter diet ingested similar quantities of dry matter and energy, and grew at the same rate as piglets given cows' milk at 2·5 Ma. As predicted, piglets given milk at maintenance energy intake grew slower (P < 0·001) and consumed less food (P < 0·001) than piglets in all other treatments. For piglets given both cows' fresh milk and the dry starter diet, there were significant linear relationships (r = 0·72 to 0·82, P < 0·05) between villous height and crypt depth with dry matter (energy) intake after weaning. In turn, mean villous height in both milk-fed and starter-fed piglets was significantly correlated (r = 0·68 to 0·79, P < 0·05) to empty body-weight gain in the first 5 days after weaning. Estimates of digestive enzyme activity and absorptive capacity of the gut did not corroborate the large differences seen between treatments in villous height and crypt depth, and possible reasons are discussed. These data illustrate the interdependence between voluntary food intake and mucosal architecture in determining piglet performance after weaning.

Type
Research Article
Copyright
Copyright © British Society of Animal Science 1996

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References

Aherne, F. X., Williams, I. H. and Head, R. H. 1991. Nutrition-reproduction interactions in swine. In Recent developments in animal nutrition in Australia 1991 (ed. Farrell, D. J.), pp. 185202. Department of Biochemistry, Microbiology and Nutrition, University of New England, Armidale, NSW.Google Scholar
Al-Dewachi, H. S., Wright, N. A., Appleton, D. R. and Watson, A. J. 1975. The effect of starvation and refeeding on cell population kinetics in the rat small bowel mucosa. Journal of Anatomy 119: 105121.Google Scholar
Altmann, G. G. 1971. Influence of bile and pancreatic secretions on the size of the intestinal villi in the rat. American journal of Anatomy 132: 167178.CrossRefGoogle ScholarPubMed
Altmann, G. G. 1972. Influence of starvation and refeeding on mucosal size and epithelial renewal in the rat small intestine. American Journal of Anatomy 133: 391400.CrossRefGoogle ScholarPubMed
Altmann, G. G. and Leblond, C. P. 1970. Factors influencing villus size in the small intestine of adult rats as revealed by transposition of intestinal segments. American Journal of Anatomy 127: 1536.CrossRefGoogle ScholarPubMed
Bardócz, S., Grant, G., Brown, D. S., Ewen, S. W. B., Stewart, J. C. and Pusztai, A. 1991. Effect of fasting and refeeding on basolateral polyamine uptake and metabolism by the rat small bowel. Digestion 50: 2835.CrossRefGoogle ScholarPubMed
Berg, N. O., Dahlqvist, A., Lindberg, T. and Nordén, Å. 1973. Correlation between morphological alterations and enzyme activities in the mucosa of the small intestine. Scandinavian Journal of'Gastroenterology 8: 703712.CrossRefGoogle ScholarPubMed
Björk, A. K. K. 1989. Is social stress in pigs a detrimental factor to health and growth that can be avoided by amperozide treatment? Applied Animal Behavioural Science 23: 3947.CrossRefGoogle Scholar
Buddie, J. R. and Bolton, J. R. 1992. The pathophysiology of diarrhoea in pigs. Pig News and Information 13: 41N45N.Google Scholar
Castillo, R. O., Feng, J. J., Stevenson, D. K., Kerner, J. A. and Kwong, L. K. 1990. Regulation of intestinal ontogeny by intraluminal nutrients. Journal of Pediatric Gastroenterology and Nutrition 10: 199205.Google ScholarPubMed
Close, W. H. and Fowler, V. R. 1985. Energy requirements of pigs. In Recent developments in pig nutrition (ed. Cole, D. J. A. and Haresign, W.), pp. 116. Butterworths, London.Google Scholar
Dowling, R. H. 1967. Compensatory changes in intestinal absorption. British Medical Bulletin 23: 275278.CrossRefGoogle ScholarPubMed
Esposito, G. 1967. Intestinal absorption of sugars in semi-starved rats. Proceedings of the Society for Experimental Biology and Medicine 125: 452455.CrossRefGoogle ScholarPubMed
Feldman, E. J., Dowling, R. H., McNaughton, J. and Peters, T. I. 1976. Effects of oral versus intravenous nutrition on intestinal adaptation after small bowel resection in the dog. Gastroenterology 70: 712719.CrossRefGoogle ScholarPubMed
Fenton, M. and Aherne, F. X. 1987. Determination of glycerol in pig plasma by capillary gas chromatography. journal of Chromatography 410: 480483.CrossRefGoogle ScholarPubMed
Gay, C. C., Barker, I. K. and Moore, P. 1976. Changes in piglet intestinal villous structure and intestinal enzyme activity associated with weaning. Proceedings of the fourth International Pig Veterinary Society congress, vol. 5 (ed. Brandt, W. E., Glock, R. D., Harris, D. L., Hutton, N. E. and Lennon, A. D.), p. 11. American Association of Swine Practitioners, College of Veterinary Medicine, Iowa State University, Ames, Ia.Google Scholar
Goldstein, R. M., Hebiguchi, T., Luk, G. D., Taqi, F., Guilarte, T. R., Franklin, F. A., Niemiec, P. W. and Dudgeon, D. L. 1985. The effects of total parenteral nutrition on gastrointestinal growth and development. journal of Pediatric Surgery 20: 785791.CrossRefGoogle ScholarPubMed
Goodlad, R. A., Plumb, J. A. and Wright, N. A. 1988. Epithelial cell proliferation and intestinal absorptive function during starvation and refeeding in the rat. Clinical Science 74: 301306.CrossRefGoogle ScholarPubMed
Goodlad, R. A. and Wright, N. A. 1984. The effects of starvation and refeeding on intestinal cell proliferation in the mouse. Virchows Archiv [Cell Pathology] 45: 6373.CrossRefGoogle ScholarPubMed
Gupta, P. D. and Waheed, A. A. 1992. Effect of starvation on glucose transport and membrane fluidity in rat intestinal epithelial cells. FEBS Letters 300: 263267.CrossRefGoogle ScholarPubMed
Hall, G. A. and Byrne, T. F. 1989. Effects of age and diet on small intestinal structure and function in gnotobiotic piglets. Research in Veterinary Science 47: 387392.CrossRefGoogle ScholarPubMed
Hamilton, D. L. and Roe, W. E. 1977. Electrolyte levels and net fluid and electrolyte movements in the gastrointestinal tract of weanling swine. Canadian journal of Comparative Medicine 41: 241250.Google ScholarPubMed
Hampson, D. J. 1983. Post-weaning changes in the piglet small intestine in relation to growth-checks and diarrhoea. Ph.D. thesis, University of Bristol.Google Scholar
Hampson, D. J. 1986a. Alterations in piglet small intestinal structure at weaning. Research in Veterinary Science 40: 3240.CrossRefGoogle ScholarPubMed
Hampson, D. J. 1986b. Attempts to modify changes in the piglet small intestine after weaning. Research in Veterinary Science 40: 313317.CrossRefGoogle ScholarPubMed
Hampson, D. J. 1987. The osmolality of caecal contents in piglets following weaning. New Zealand Veterinary Journal 35: 3536.CrossRefGoogle ScholarPubMed
Hampson, D. J. and Kidder, D. E. 1986. Influence of creep feeding and weaning on brush border enzyme activities in the piglet small intestine. Research in Veterinary Science 40: 2431.CrossRefGoogle ScholarPubMed
Hampson, D. J. and Smith, W. C. 1986. Influence of creep feeding and dietary intake after weaning on malabsorption and occurrence of diarrhoea in the newly weaned pig. Research in Veterinary Science 41: 6369.CrossRefGoogle ScholarPubMed
Hopper, A. F., Rose, P. M. and Wannemacher, R. W. 1972. Cell population changes in the intestinal mucosa of protein-depleted or starved rats. II. Changes in cellular migration rates. Journal of Cell Biology 53: 225230.CrossRefGoogle ScholarPubMed
Kanayama, S. and Liddle, R. A. 1991. Influence of food deprivation on intestinal cholecystokinin and somatostatin. Gastroenterology 100: 909915.CrossRefGoogle ScholarPubMed
Kelly, D., King, T. P., McFadyen, M. and Travis, A. J. 1991a. Effect of lactation on the decline of brush border lactase activity in neonatal pigs. Gut 32: 386392.CrossRefGoogle ScholarPubMed
Kelly, D., O'Brien, J. J. and McCracken, K. J. 1990b. Effect of creep feeding on the incidence, duration and severity of post-weaning diarrhoea in pigs. Research in Veterinary Science 49: 223228.CrossRefGoogle ScholarPubMed
Kelly, D., Smyth, J. A. and McCracken, K. J. 1990a. Effect of creep feeding on structural and functional changes of the gut of early weaned pigs. Research in Veterinary Science 48: 350356.CrossRefGoogle ScholarPubMed
Kelly, D., Smyth, J. A. and McCracken, K. J. 1991b. Digestive development in 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. British Journal of Nutrition 65:169180.CrossRefGoogle ScholarPubMed
Kelly, D., Smyth, J. A. and McCracken, K. J. 1991c. Digestive development in the early-weaned pig. II. Effect of level of food intake on digestive enzyme activity during the immediate post-weaning period. British Journal of Nutrition 65: 181188.CrossRefGoogle Scholar
Kershaw, T. G., Neame, K. D. and Wiseman, G. 1960. The effect of semistarvation on absorption by the rat small intestine in vitro and in vivo. Journal of Physiology 152: 182190.CrossRefGoogle ScholarPubMed
Koga, A. and Kimura, S. 1978. Influence of restricted diet on epithelial renewal and maturation in the mice jejunum. Journal of Nutritional Science and Vitaminology 24: 323329.CrossRefGoogle ScholarPubMed
Koga, A. and Kimura, S. 1979. Influence of restricted diet on the cell renewal of the mouse small intestine. Journal of Nutritional Science and Vitaminology 25: 265267.CrossRefGoogle ScholarPubMed
Koga, A. and Kimura, S. 1980. Influence of restricted diet on the cell cycle in the crypt of mouse small intestine. Journal of Nutritional Science and Vitaminology 26: 3338.CrossRefGoogle ScholarPubMed
Lebenthal, E., Sunshine, P. and Kretchmer, N. 1973. Effect of prolonged nursing on the activity of intestinal lactase in rats. Gastroenterology 64:11361141.CrossRefGoogle ScholarPubMed
Lifshitz, F., Hawkins, R. L., Diaz-Bensussen, S. and Wapnir, R. A. 1972. Absorption of carbohydrates in malnourished rats. Journal of Nutrition 102:13031310.CrossRefGoogle ScholarPubMed
Lucas, I. A. M. and Lodge, G. A. 1961. Nutrition of the young pig. Technical bulletin, Commonwealth Agricultural Bureaux, no. 22.Google Scholar
McCracken, K. J. 1984. Effect of diet composition on digestive development of early-weaned pigs. Proceedings of the Nutrition Society 43:109a.Google Scholar
McManus, J. P. A. and Isselbacher, K. J. 1970. Effect of fasting versus feeding on the rat small intestine. Morphological, biochemical, and functional differences. Gastroenterology 59: 214221.CrossRefGoogle ScholarPubMed
Maindonald, J. H. 1992. Statistical design, analysis and presentation issues. New Zealand journal of Agricultural Research 35: 121141.CrossRefGoogle Scholar
Merritt, A. M. and Duelly, P. 1983. Phoroglucind microassay for plasma xylose in dogs and horses. American Journal of Veterinary Research 44: 21842185.Google ScholarPubMed
Miller, B. G., James, P. S., Smith, M. W. and Bourne, F. J. 1986. Effect of weaning on the capacity of pig intestinal villi to digest and absorb nutrients. Journal of Agricultural Science, Cambridge, 107: 579589.CrossRefGoogle Scholar
Miller, B. G., Newby, T. J., Stokes, C. R. and Bourne, F. J. 1984. Influence of diet on postweaning malabsorption and diarrhoea in the pig. Research in Veterinary Science 36: 187193.CrossRefGoogle ScholarPubMed
Moon, H. W. 1971. Epithelial cell migration in the alimentary mucosa of the suckling pig. Proceedings of the Society for Experimental Biology and Medicine 137:151154.CrossRefGoogle ScholarPubMed
Nichols, B. L. and Nichols, V. N. 1988. Carbohydrate maldigestion and malabsorption. In Clinical nutrition of the young child (ed. Brunser, O., Carrazza, F. R., Gracey, M., Nichols, B. L. and Senterre, J.), pp. 217240. Nestlé Nutrition, Vervey/Raven Press Ltd, New York.Google Scholar
Noblet, J. and Etienne, M. 1987. Body composition, metabolic rate and utilization of milk nutrients in suckling piglets. Reproduction, Nutrition, Developpement 27: 829839.CrossRefGoogle ScholarPubMed
Nordström, C. and Dahlqvist, A. 1973. Quantitative distribution of some enzymes along the villi and crypts of human small intestine. Scandinavian Journal of Gastroenterology 8: 407416.CrossRefGoogle ScholarPubMed
Perrin, D. R. 1958. The calorific value of milk of different species. Journal of Dairy Research 25: 215220.CrossRefGoogle Scholar
Pluske, J. R., Williams, I. H. and Aherne, F. X. 1996. Maintenance of villous height and crypt depth in piglets by providing continuous nutrition after weaning. Animal Science 62:131144.CrossRefGoogle Scholar
Rey, J., Schmitz, J., Rey, F. and Jos, J. 1971. Cellular differentiation and enzymatic deficits. Lancet ii: 218.CrossRefGoogle Scholar
Rudo, N. D., Rosenberg, I. H. and Wissler, R. W. 1976. The effect of partial starvation and glucagon treatment on intestinal villus morphology and cell migration. Proceedings of the Society for Experimental Biology and Medicine 152: 277280.CrossRefGoogle ScholarPubMed
Smith, M. W. 1984. Effect of postnatal development and weaning upon the capacity of pig intestinal villi to transport alanine. Journal of Agricultural Science, Cambridge 102: 625633.CrossRefGoogle Scholar
Steiner, M., Bourges, H. R., Freedman, R. W. and Gray, S. J. 1968. Effect of starvation on the tissue composition of the small intestine in the rat. American Journal of Physiology 215:7577.CrossRefGoogle ScholarPubMed
Stevens Hooper, C. and Blair, M. 1958. The effect of starvation on epithelial renewal in the rat duodenum. Experimental Cell Research 14:175181.CrossRefGoogle Scholar
Tivey, D. R. and Shulman, R. J. 1991. Effect of pancreatic secretions upon ileal disaccharidase activities of neonatal miniature pigs. Expcrientia 47: 452454.CrossRefGoogle ScholarPubMed
Wapnir, R. A. and Lifshitz, F. 1974. Absorption of amino acids in malnourished rats. Journal of Nutrition 104: 843849.CrossRefGoogle ScholarPubMed
Wilkinson, L. 1990. SYSTAT: the system for statistics. Systat, Inc., Evanston, Il.Google Scholar
Williamson, R. C. N. 1978. Intestinal adaptation. II. Mechanisms of control. New England Journal of Medicine 298: 14441450.CrossRefGoogle Scholar