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Maintenance of villous height and crypt depth in piglets by providing continuous nutrition after weaning

Published online by Cambridge University Press:  02 September 2010

J. R. Pluske ,
I. H. Williams  and
F. X. Aherne
J. R. Pluske
Affiliation:
Animal Science, Faculty of Agriculture, University of Western Australia, Nedlands, WA 6009, Australia
I. H. Williams
Affiliation:
Animal Science, Faculty of Agriculture, University of Western Australia, Nedlands, WA 6009, 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

Thirty-two piglets weaned at 28 days of age were used to test the hypothesis that maintenance of nutrition after weaning would prevent the normal decline in villous height and increase in crypt depth and hence preserve the structure and function of the small intestine. Piglets were allocated to one of four treatments at weaning: (1) control group killed at weaning; (2) piglets offered a dry starter diet ad libitum; (3) piglets offered ewes' fresh milk; and (4) piglets offered ewes' fresh milk plus 20 g t-glutamine per I. Piglets in treatments (3) and (4) were offered ewes' fresh milk every 2 h in a feeding schedule that increased from 1·2 I per piglet on the 1st day after weaning to 2·4 I on days 4 and 5. On the 5th day all piglets were killed and samples of small intestine were taken for histological and biochemical examination. Feeding ewes' milk or ewes' milk plus 20 g L-glutamine per I maintained (P > 0·05) villous height and crypt depth compared with piglets killed at weaning. In contrast, piglets given a dry starter diet had shorter villi (P < 0·001), deeper crypts (P < 0·001), and proportionately 0·21 to 0·28 less protein (P > 0·05) in their intestinal mucosa. Piglets given the starter diet proportionately grew from 0·49 to 0·62 more slowly (P < 0·01), ate the same amount of dry matter (DM; P > 0·05), but consumed proportionately 0·30 less energy (P < 0·001) than their counterparts given the milk diets. No treatment differences in the specific activity of lactase and sucrase were observed (P > 0·05). Significant correlations existed between voluntary food intake and villous height at the proximal jejunum for piglets given the starter diet and ewes' milk (P < 0·05 and P = 0·073, respectively). In turn, villous height was significantly correlated (r = 0·78 to 0·87, P < 0·05) with the rate of body-weight gain after weaning in these two groups. For piglets offered ewes' milk plus glutamine, an increase in DM intake was associated only with increases in crypt depth (P < 0·01). These data show that the structure and function of the small intestine can be preserved when a milk diet is given after weaning, and suggest an association between food intake and villous height in determining post-weaning weight gain.

Keywords

continuous nutritioncrypt depthglutaminepigletsvillous height
Type
Research Article
Information
Animal Science , Volume 62 , Issue 1 , February 1996 , pp. 131 - 144
Copyright
Copyright © British Society of Animal Science 1996

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References

Al-Mukhtar, M. Y. T., Polak, J. M., Bloom, S. R. and Wright, N. A. 1982. The search for appropriate measurements of proliferative and morphological status in studies on intestinal adaptation. In Mechanisms of intestinal adaptation (ed. Robinson, J. W. L., Dowling, R. H. and Riecken, E.-O.), pp. 3–25. MTP Press Limited, Lancaster.Google Scholar
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: 391–400.Google Scholar
Bailey, C. B., Kitts, W. D. and Wood, A. J. 1956. The development of the digestive enzyme system of the pig during its pre-weaning phase of growth. B. Intestinal lactase, sucrase and maltase. Canadian Journal of Agricultural Science 36: 51–58.Google Scholar
Bark, L. J., Crenshaw, T. D. and Leibbrandt, V. D. 1986. The effect of meal intervals and weaning on feed intake of early weaned pigs. Journal of Animal Science 62:1233–1239.Google Scholar
Campbell, R. G. 1989. The nutritional management of weaner pigs. In Manipulating pig production II (ed. Barnett, J. L. and Hennessy, D. P.), pp. 170–175. Australasian Pig Science Association, Werribee, Victoria.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 10:199–205.Google ScholarPubMed
Cera, K. R., Mahan, D. C., Cross, R. F., Reinhart, G. A. and Whitmoyer, R. E. 1988. Effect of age, weaning and postweaning diet on small intestinal growth and jejunal morphology in young swine. Journal of Animal Science 66: 574–584.Google Scholar
Cera, K., Mahan, D. C. and Simmen, F. A. 1987. In vitro growth-promoting activity of porcine mammary secretions: initial characterization and relationship to known peptide growth factors. Journal of Animal Science 65:1149–1159.Google Scholar
Cheng, H. and Leblond, C. P. 1974. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. v. Unitarian theory of the origin of the four epithelial cell types. American Journal of Anatomy 141: 537–562.Google Scholar
Cranwell, P. D. and Moughan, P. J. 1989. Biological limitations imposed by the digestive system to the growth performance of weaned pigs. In Manipulating pig production II (ed. Barnett, J. L. and Hennessy, D. P.), pp. 140–159. Australasian Pig Science Association, Werribee, Victoria.Google Scholar
Dahlqvist, A. and Nordstrom, C. 1966. The distribution of disaccharidase activities in the villi and crypts of the small-intestinal mucosa. Biochimica et Biophysica Ada 113: 624–626.Google Scholar
Déchelotte, P., Darmaun, D., Rongier, M., Hecketsweiler, B., Rigal, O. and Desjeux, J.-F. 1991. Absorption and metabolic effects of enterally administered glutamine in humans. American Journal of Physiology 260: G677–G682.Google Scholar
Diamond, J. M. and Karasov, W. H. 1983. Trophic control of the intestinal mucosa. Nature, London 304:18.Google Scholar
Gay, C. C. 1976. Intestinal disaccharidase activity and intestinal morphology of piglet intestine between birth and five weeks. 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. 10. American Association of Swine Practitioners, College of Veterinary Medicine, Iowa State University, Ames, Ia.Google Scholar
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
Gleeson, M. H., Cullen, J. and Dowling, R. H. 1972. Intestinal structure and function after small bowel by-pass in the rat. Clinical Science 43: 731–742.CrossRefGoogle ScholarPubMed
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 ofPediatric Surgery 20: 785–791.Google Scholar
Gornall, A. G., Bardawill, C. J. and David, M. M. 1949. Determination of serum proteins by means of the biuret reaction. Journal of Biological Chemistry 177: 751–766.CrossRefGoogle ScholarPubMed
Hampson, D. J. 1983. Post-weaning changes in the piglet small intestine in relation to growth-checks and diarrhoea. PhD. thesis, University of Bristol.Google Scholar
Hampson, D. J. 1986a. Alterations in piglet small intestinal structure at weaning. Research in Veterinary Science 40: 32–40.Google Scholar
Hampson, D. J. 1986b. Attempts to modify changes in the piglet small intestine after weaning. Research in Veterinary Science 40: 313–317.CrossRefGoogle ScholarPubMed
Hampson, D. J. 1987. Dietary influences on porcine postweaning diarrhoea. In Manipulating pig production (ed. Barnett, J. L., Batterham, E. S., Cronin, G. M., Hansen, C., Hemsworth, P. H., Hennessy, D. P., Hughes, P. E., Johnston, N. E. and King, R. H.), pp. 202–214. Australasian Pig Science Association, Werribee, Victoria.Google Scholar
Hampson, D. J., Fu, Z. F. and Smith, W. C. 1988 Pre-weaning supplementary feed and porcine post-weaning diarrhoea. Research in Veterinary Science 44: 309–314.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: 24–31.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: 63–69.Google Scholar
Harrell, R. J., Thomas, M. J. and Boyd, R. D. 1993. Limitations to sow milk yield on baby pig growth. Proceedings of the 1993 Cornell nutrition conference for feed manufacturers, pp. 156–164. Department of Animal Science and Division of Nutritional Sciences of the New York State College of Agriculture and Life Sciences, Cornell University, Ithaca, New York.Google Scholar
Hodge, R. W. 1974. Efficiency of food conversion and body composition of the preruminant lamb and young pig. British Journal of Nutrition 32:113–126.Google Scholar
Jaeger, L. A., Lamar, C. H., Bottoms, G. D. and Cline, T. R. 1987. Growth-stimulating substances in porcine milk. American Journal of Veterinary Research 48:1531–1533.Google Scholar
James, P. S., Smith, M. W., Tivey, D. R. and Wilson, T. J. G. 1987. Epidermal growth factor selectively increases maltase and sucrase activities in neonatal piglet intestine. Journal of Physiology 393: 583–594.Google Scholar
Jones, B. N. and Gilligan, J. P. 1983. o-Phthaldialdehyde pre-column derivatisation and reverse-phase high performance liquid chromatography of polypeptide hydrolysates and physiological fluids. Journal of Chromatography 266: 471–482.CrossRefGoogle Scholar
Kelly, D. 1985. The role of nutrition and E. coli in digestive tract development and performance of early-weaned pigs. Ph.D. thesis, The Queen's University of Belfast.Google Scholar
Kelly, D., King, T. P., Brown, D. S. and McFadyen, M. 1991d. Polyamide profiles of porcine milk and of intestinal tissue of pigs during suckling. Reproduction, Nutrition, Developpement 31: 73–80.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. Cut 32: 386–392.Google Scholar
Kelly, D., McFadyen, M., King, T. P. and Morgan, P. J. 1992. Characterisation and autoradiographic localisation of the epidermal growth factor receptor in the jejunum of neonatal and weaned pigs. Reproduction, Fertility and Development 4:183–191.Google Scholar
Kelly, D., Smyth, J. A. and McCracken, K. J. 1991b. Digestive development in the early-weaned pig. 1. 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 65:169–180.Google Scholar
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 65:181–188.CrossRefGoogle Scholar
Kidder, D. E. and Manners, M. J. 1980. The level and distribution of carbohydrases in the small intestine of pigs from 3 weeks to maturity. British Journal of Nutrition 43: 141–153.Google Scholar
King, T. P. and Kelly, D. 1990. Effect of lactation on the postnatal expression of intestinal membrane glycoconjugates in pigs. Proceedings of the Nutrition Society 49:142A.Google Scholar
Klimberg, V. S., Salloum, R. M., Kasper, M., Plumley, D. A., Dolson, D. J., Hautamaki, R. D., Mendenhall, W. R., Bova, F. C., Bland, K. I., Copeland, E. M. and Souba, W. W. 1990. Oral glutamine accelerates healing of the small intestine and improves outcome after whole-body abdominal radiation. Archives of Surgery 125: 1040–1045.Google Scholar
Koldovsky, O. 1989. Search for the role of milk-borne biologically active peptides for the suckling. Journal of Nutrition 119: 1543–1551.Google Scholar
Koong, L.-J., Nienaber, J. A., Pekas, J. C. and Yen, J.-T. 1982. Effects of plane of nutrition on organ size and fasting heat production in pigs. Journal of Nutrition 112: 1638–1642.Google Scholar
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
McCracken, K. J. and Kelly, D. 1984. Effect of diet and post-weaning food intake on digestive development of early-weaned pigs. Proceedings of the Nutrition Society 43: 110A.Google Scholar
McCracken, K. J. and Kelly, D. 1993. Development of digestive function and nutrition/disease interactions in the weaned pig. In Recent advances in animal nutrition in Australia 1993 (ed. Farrell, D. J.), pp. 182–192. Department of Biochemistry, Microbiology and Nutrition, University of New England, Armidale, NSW.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: 214–221.Google Scholar
McNeill, L. K. and Hamilton, J. R. 1971. The effect of fasting on disaccharidase activity in the rat small intestine. Pediatrics 47: 65–72.Google Scholar
Maindonald, J. H. 1992. Statistical design, analysis, and presentation issues. New Zealand journal of Agricultural Research 35: 121–141.Google Scholar
Meier, S. A., Knabe, D. A., Wu, G. and Borbolla, A. 1993. Glutamine supplementation to diets of 21 day-old pigs. Journal of Animal Science 71: suppl. 1, p. 170.Google Scholar
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: 579–589.Google 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: 187–193.Google Scholar
Newsholme, E. A., Crabtree, B. and Ardawi, M. S. M. 1985. The role of high rates of glycolysis and glutamine utilization in rapidly dividing cells. Bioscience Reports 5: 393–400.Google Scholar
Noblet, J. and Etienne, M. 1987. Body composition, metabolic rate and utilization of milk nutrients in suckling piglets. Reproduction, Nutrition, Developpement 27: 829–839.Google Scholar
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: 407–416.CrossRefGoogle ScholarPubMed
Pekas, J. C. 1986a. Morphometry of the intestine of the pig. I. A method for complete circumsection analysis. Digestive Diseases and Sciences 31: 79–89.Google Scholar
Pekas, J. C. 1986b. Morphometry of the intestine of the pig. II. Circumsection response to feeding schedules. Digestive Diseases mid Sciences 31: 90–96.Google Scholar
Pekas, J. C. and Wray, J. E. 1991. Principal gastrointestinal variables associated with metabolic heat production in pigs: statistical cluster analyses. Journal of Nutrition 121: 231–239.CrossRefGoogle ScholarPubMed
Perrin, D. R. 1958. The calorific value of milk of different species. Journal of Dairy Research 25: 215–220.Google Scholar
Pluske, J. R. and Williams, I. H. 1988. Split weaning increases the growth of small pigs. Proceedings of the Australian Society of Animal Production 17: 453.Google Scholar
Pluske, J. R., Williams, I. H. and Aherne, F. X. 1991. Maintenance of villous height and crypt depth in the small intestine of weaned piglets. In Manipulating pig production III (ed. Batterham, E. S.), p. 143. Australasian Pig Science Association, Werribee, Victoria.Google Scholar
Pluske, J. R., Williams, I. H. and Aherne, F. X. 1996. Villous height and crypt depth in piglets in response to increases in the intake of cows' milk after weaning. Animal Science 62: 145–158.Google Scholar
Puchal, A. A. and Buddington, R. K. 1992. Postnatal development of monosaccharide transport in pig intestine. American journal of Physiology 262: G895–G902.Google Scholar
Rey, J., Schmitz, J., Rey, F. and Jos, J. 1971. Cellular differentiation and enzymatic deficits. Lancet ii: 218.Google Scholar
Robertson, A. M., Clark, J. J. and Bruce, J. M. 1985. Observed energy intake of weaned piglets and its effect on temperature requirements. Animal Production 40: 475–479.Google Scholar
Salloum, R. M., Souba, W. W., Fernandez, A. and Stevens, B. R. 1990. Dietary modulation of small intestinal glutamine transport in intestinal brush border membrane vesicles of rats. Journal of Surgical Research 48: 635–638.Google Scholar
Salloum, R. M., Souba, W. W., Klimberg, V. S., Plumley, D. A., Dolson, D. J., Bland, K. I. and Copeland, E. M. 1989. Glutamine is superior to glutamate in supporting gut metabolism, stimulating intestinal glutaminase activity, and preventing bacterial translocation. Surgical Forum 40: 6–8.Google Scholar
Sangild, P. T., Cranwell, P. D., Serensen, H., Mortensen, K., Norén, O., Wetteberg, L. and Sjbstrom, H. 1991. Development of intestinal disaccharidases, intestinal peptidases and pancreatic proteases in sucking pigs. The effects of age and ACTH treatment. In Digestive physiology in pigs (ed. Verstegen, M. W. A., Huisman, J. and Hartog, L. A. den), proceedings of the fifth international symposium on digestive physiology in pigs, Wageningen, Netherlands, pp. 73–78.Google Scholar
Shulman, R. J., Fiorotto, M. L., Sheng, H.-P. and Garza, C. 1984. Effect of different total parenteral nutrition fuel mixes on the body composition of infant miniature pigs. Pediatric Research 18: 261–265.Google Scholar
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: 625–633.Google Scholar
Souba, W. W. 1991. Glutamine: a key substrate for the splanchnic bed. Annual Review of Nutrition 11: 285–308.CrossRefGoogle ScholarPubMed
Souba, W. W. 1992. Glutamine: physiology, biochemistry and nutrition in critical illness. Medical Intelligence Unit, R. G. Landes Company, Austin, Tx.Google Scholar
Souba, W. W. 1993. Intestinal glutamine metabolism and nutrition. journal of Nutritional Biochemistry 4: 2–9.Google 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: 75–77.Google Scholar
Tybirk, P. 1989. A model of food intake regulation in the growing pig. In Voluntary food intake of pigs (ed. Forbes, J. M., Varley, M. A. and Lawrence, T. L. J.), Occasional publication no. 13, British Society of Animal Production, pp. 105–109.Google Scholar
Webster, A. J. F. 1980. The energetic efficiency of growth. Livestock Production Science 7: 243–252.Google Scholar
Webster, A. J. F. 1981. The energetic efficiency of metabolism. Proceedings of the Nutrition Society 40:121–128.Google Scholar
Wilkinson, L. 1990. SYSTAT: the system for statistics. Systat Inc., Evanston, Il.Google Scholar
Williams, I. H. 1976. Nutrition of the young pig in relation to body composition. Ph.D. thesis, University of Melbourne.Google Scholar
Williamson, R. C. N. 1978. Intestinal adaptation. II. Mechanisms of control. New England journal of Medicine 298: 1444–1450.CrossRefGoogle Scholar
Windmueller, H. G. 1982. Glutamine utilization by the small intestine. Advances in Enzynwlogy 53: 201–237.Google Scholar
Windmueller, H. G. and Spaeth, A. E. 1980. Respiratory fuels and nitrogen metabolism in vivo in small intestine of fed rats. Journal of Biological Chemistry 255:107–112.Google Scholar
Wu, G. and Knabe, D. A. 1993. Glutamine metabolism in pig enterocytes. Journal of Animal Science 71: suppl. 1, p. 130.Google Scholar