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Maintenance of villus height and crypt depth, and enhancement of disaccharide digestion and monosaccharide absorption, in piglets fed on cows' whole milk after weaning

Published online by Cambridge University Press:  09 March 2007

John R. Pluske ,
Melinda J. Thompson ,
Craig S. Atwood ,
Peter H. Bird ,
Ian H. Williams  and
Peter E. Hartmann
John R. Pluske
Affiliation:
Animal Science, Faculty of Agriculture, University of Western Australia, Nedlands, WA 6907, Australia
Melinda J. Thompson
Affiliation:
Department of Biochemistry, University of Western Australia, Nedlands, WA 6907, Australia
Craig S. Atwood
Affiliation:
Department of Biochemistry, University of Western Australia, Nedlands, WA 6907, Australia
Peter H. Bird
Affiliation:
Department of Biochemistry, University of Western Australia, Nedlands, WA 6907, Australia
Ian H. Williams
Affiliation:
Animal Science, Faculty of Agriculture, University of Western Australia, Nedlands, WA 6907, Australia
Peter E. Hartmann
Affiliation:
Department of Biochemistry, University of Western Australia, Nedlands, WA 6907, Australia
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Abstract

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The aims of the present study were (a) to maintain the structure and function of the small intestine of the piglet after weaning, and (b) to compare the capacity in vivo of sucking and weaned piglets to digest oral boluses of lactose and sucrose and absorb their monosaccharide products. Piglets were fed on cows' whole milk ad libitum every 2 h for 5 d after weaning. Physiological doses of lactose plus fructose (treatment LAC + FRU) and sucrose plus galactose (treatment SUC + GAL) were administered on day 27 of lactation and on the fifth day after weaning, after which time piglets were killed. Villus height and crypt depth were maintained (P > 0·05) by feeding cows' milk after weaning. The areas under the curves (AUC) for galactose and glucose, adjusted for live weight and plasma volume, increased (P < 0·05) after weaning. Despite the enhancement of gut function after weaning, the galactose index (Gall: AUC for galactose ingested as lactose divided by the AUC for the same dose of galactose ingested as the monosaccharide) and fructose index (FruI: AUC for fructose ingested as sucrose divide by the AUC for the same dose of fructose ingested as the monosaccharide), which are indices of digestive and absorptive efficiency, both decreased after weaning. This apparent anomaly may be reconciled by increased growth, and hence surface area, of the small intestine between weaning and slaughter such that ‘total’ digestion and absorption most probably increased despite apparent decreases in GalI and FrnI. Positive correlations (P < 0.05) between villus height and Gall are consistent with the maximum activity of lactase occurring more apically along the villus. Significant linear relationships (P < 0·05) were recorded between villus height at the proximal jejunum and adjusted AUC for galactose and glucose following treatment LAC + FRU, and between villus height at the proximal jejunum and adjusted glucose AUC following treatment SUC + GAL. These relationships suggest that maximum digestion and absorption occurs at increasing distances along the crypt:villus axis in the weaned pig.

Keywords

PigletSugarsVillus heightCrypt depth
Type
Animal Nutrition
Information
British Journal of Nutrition , Volume 76 , Issue 3 , September 1996 , pp. 409 - 422
Copyright
Copyright © The Nutrition Society 1996

References

REFERENCES

Al-Mukhtar, M. Y. T., Polak, J. M., Bloom, S. R. & Wright, N. A. (1982). The search for appropriate measurements of proliferative and morphological status in studies on intestinal adaptation. In Mechanisms of Intestinal Adaptation, pp. 3–25 [Robinson, J. W. L., Dowling, R. H. and Riecken, E.-O., editors]. Lancaster: MTP Press.Google Scholar
Altmann, G. G. (1972). Influence of starvation and refeeding on mucosal size and epithelial renewal in the rat small intestine. Americun Journal of Anatomy 133, 391–400.CrossRefGoogle ScholarPubMed
Arthur, P. G., Kent, J. C. & Hartmann, P. E. (1989). Microanalysis of the metabolic intermediate of lactose synthesis in human milk and plasma using bioluminescent methods. Analytical Biochemistry 176, 449–456.CrossRefGoogle ScholarPubMed
Bergmeyer, H. U. & Bern't, E. (1974). D-Glucose: determination with glucose oxidase and peroxidase. In Methods of Enzymatic Analysis, 2nd ed., vol. 3, pp. 1205–1215 [Bergmeyer, H. U. editor]. New York: Academic Press.Google Scholar
Bird, P. H., Atwood, C. S. & Hartmann, P. E (1995). The responses of blood galactose to oral doses of lactose, galactose plus glucose and milk to piglets. British Journal of Nutrition 73, 753–761.CrossRefGoogle ScholarPubMed
Bird, P. H. & Hartmann, P. E. (1994). The response in the blood of piglets to oral doses of galactose and glucose and intravenous administration of galactose. British Journal of Nutrition 71, 553–561.Google ScholarPubMed
Bird, P. H. & Hartmann, P. E. (1996). Changes in the concentration of fructose in the blood of piglets of different ages after doses of fructose, fructose plus glucose and sucrose. British Journal of Nutrition 76, 399–407.CrossRefGoogle ScholarPubMed
Brand Miller, J., Holt, S., Thomas, D., Byrnes, S., Denyer, G. & Truswell, A. S. (1994). Glycaemic index: is it a useful tool in human health and disease? Proceedings of the Nutrition Society of Australia 18, 15–22.Google Scholar
Cera, K. R., Mahan, D. C., Cross, R. F., Reinhart, G. A. & 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.CrossRefGoogle ScholarPubMed
Clarke, R. M. (1975). The time-course of changes in mucosal architecture and epithelial cell production and cell shedding in the small intestine of the rat fed after fasting. Journal of Anatomy 120, 321–327.Google ScholarPubMed
Dahlqvist, A. & Nordström, C. (1966). The distribution of disaccharidase activities in the villi and crypts of the small-intestinal mucosa. Biochimica et Biophysica Acta 113, 624–626.CrossRefGoogle ScholarPubMed
Ekstrom, K. E., Benevenga, N. J. & Grummer, H. (1975). Changes in the intestinal lactase activity in the small intestine of two breeds of swine from birth to 6 weeks of age. Journal of Nutrition 105, 1032–1038.CrossRefGoogle ScholarPubMed
Gay, C. C., Barker, I. K. & Moore, P. (1976). Changes in piglet intestinal villous structure and intestinal enzyme activity associated with weaning. In Proceedings of the IVth International Pig Veterinary Society Congress, vol. 5, p. 11 [Brandt, W. E., Glock, R. D., Harris, D. L., Hutton, N. E. and Lennon, A. D. editors]. College of Veterinary Medicine, Iowa State University, Ames, Iowa: American Association of Swine Practitioners.Google Scholar
Goodlad, R. A., Plumb, J. A. & Wright, N. A. (1988). Epithelial cell proliferation and intestinal absorptive function during starvation and refeeding in the rat. Clinical Science 74, 301–306.CrossRefGoogle ScholarPubMed
Guppy, M., Sabaratnam, R., Devadason, S. & Whisson, M. E. (1990). Fructose formation in store blood. Biochemistry International 21, 210–224.Google Scholar
Hampson, D. J. (1986 a). Alterations in piglet small intestinal structure at weaning. Research in Veterinary Science 40, 32–40.CrossRefGoogle ScholarPubMed
Hampson, D. J. (1986 b). Attempts to modify changes in the piglet small intestine after weaning. Research in Veterinary Science 40, 313–317.CrossRefGoogle ScholarPubMed
Hampson, D. J. & 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. & Smith, W. C. 1986 Influence of creep feeding and distary intake after weaning on malabsorption and occurrence of diarrhoea in the newly weaned pig. Research in Veterinary Science 41, 63–69.CrossRefGoogle ScholarPubMed
Holmes, M. A., Arthur, P. G. & Hartmann, P. E. (1990). Changes in the concentrations of glucose and galactose in the peripheral blood of suckling piglets. Journal of Dairy Research 57, 331–337.CrossRefGoogle Scholar
Hornich, M., Salajka, E., Ulmann, L., Sarmanová, Z. & Sedlácek, M. (1973). Enteric Escherichia coli infections. Morphological findings in the intestinal mucosa of healthy and diseased piglets. Veterinary Pathology 10, 484–500.CrossRefGoogle ScholarPubMed
James, P. S., Smith, M. W. & Tivey, D. R. (1988). Single-villus analysis of disaccharidase expression by different regions of the mouse intestine. Journal of Physiology 401, 533–545.CrossRefGoogle ScholarPubMed
James, P. S., Smith, M. W., Tivey, D. R. & Wilson, T. J. G. (1987). Epidermal growth factor selectively increases maltase and sucrase activities in neonatal piglet intestine. Journal of Physiofogy 393, 583–594.CrossRefGoogle ScholarPubMed
Jonas, M. M., Montgomery, R. K. & Grand, R. J. (1985). Intestinal lactase synthesis during postnatal development in the rat. Pediatric Research 19, 956–962.CrossRefGoogle ScholarPubMed
Kaempf, J. W., Battaglia, F. C. & Sparks, J. W. (1990). Galactose clearance and carbohydrate metabolism across the gastrointestinal tract in the newborn lamb. Metabolism 39, 698–703.CrossRefGoogle ScholarPubMed
Kaempf, J. W., Li, H.-Q., Groothuis, J. R., Battaglia, F. C., Zerbe, G. O. & Sparks, J. W. (1988). Galactose, glucose, and lactate concentrations in the portal venous and arterial circulations of newborn lambs after nursing. Pediatric Research 23, 598–602.CrossRefGoogle ScholarPubMed
Kelly, D., King, T. P., McFadyen, M. & Travis, A. J. (1991 a). Effect of lactation on the decline of brush border lactase activity in neonatal pigs. Gut 32, 386–392.CrossRefGoogle ScholarPubMed
Kelly, D., Smyth, J. A. & McCracken, K. J. (1990). Effect of creep feeding on structural and functional changes of the gut of early weaned pigs. Research in Veterinary Science 48, 350–356.CrossRefGoogle ScholarPubMed
Kelly, D., Smyth, J. A. & McCracken, K. J. (1991 b). 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, 169–180.CrossRefGoogle ScholarPubMed
Kelly, D., Smyth, J. A. & McCracken, K. J. (1991 c). 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
Kenworthy, R. (1976). Observations on the effects of weaning in the young pig. Clinical and histopathological studies of intestinal function and morphology. Research in Veterinary Science 21, 69–75.CrossRefGoogle Scholar
Kidder, D. E. & Manners, M. J. (1980). The level and distribution of carbohydrases in the small intestine mucosa of pigs from 3 weeks of age to maturity. British Journal of Nutrition 43, 141–153.CrossRefGoogle ScholarPubMed
Kliegman, R. M. & Sparks, J. W. (1985). Perinatal galactose metabolism. Journal of Pediatrics 107, 831–841.CrossRefGoogle ScholarPubMed
Koldovsky, O., Sunshine, P. & Kretchmer, N. (1966). Cellular migration of intestinal epithelia in suckling and weaned rats. Nature 212, 1389–1390.CrossRefGoogle ScholarPubMed
Manners, M. J. & Stevens, J. A. (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. British Journal of Nutrition 28, 113–127.CrossRefGoogle ScholarPubMed
Miller, B. G., James, P. S., Smith, M. W. & 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.CrossRefGoogle Scholar
Miller, B. G., Newby, T. J., Stokes, C. R. & Bourne, F. J. (1984). Influence of diet on postweaning malabsorption and diarrhoea in the pig. Research in Veterinary Science 36, 187–193.CrossRefGoogle ScholarPubMed
Nabuurs, M. J. A., Hoogendoorn, A., van der Molen, E. J. & van Osta, A. L. M. (1993). Villus height and crypt depth in weaned and unweaned pigs, reared under various circumstances in the Netherlands. Research in Veterinary Science 55, 78–84.CrossRefGoogle ScholarPubMed
Nabuurs, M. J. A., Hoogendoorn, A. & van Zijderveld, F. G. (1994). Effects of weaning and enterotoxigenic Escherichia coli on net absorption in the small intestine of pigs. Research in Veterinary Science 56, 379–385.CrossRefGoogle ScholarPubMed
Noblet, J. & Etienne, M. (1987). Body composition, metabolic rate and utilization of milk nutrients in suckling piglets. Reproduction, Nutrition, Développement 27, 829–839.CrossRefGoogle ScholarPubMed
Nordström, C. & 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
Pluske, J. R., Williams, I. H. & Aherne, F. X. (1996 a). Maintenance of villous height and crypt depth in piglets by providing continuous nutrition after weaning. Animal Science 62, 131–144.CrossRefGoogle Scholar
Pluske, J. R., Williams, I. H. & Aherne, F. X. (1996 b). Villous height and crypt depth in piglets in response to increases in the intake of cows' milk after weaning. Animal Science 62, 145–158.CrossRefGoogle Scholar
Puchal, A. A. & Buddington, R. K. (1992). Postnatal development of monosaccharide transport in pig intestine. American Journal of Physiology 262, G895–G902.Google ScholarPubMed
Rey, J., Schmitz, J., Rey, F. & Jos, J. (1971). Cellular differentiation and enzymatic deficits. Lancet ii, 218.CrossRefGoogle Scholar
Rice, L., Ott, E. A., Beede, D. K., Wilcox, C. J., Johnson, E. L., Lieb, S. & Borum, P. (1992). Use of oral tolerance tests to investigate disaccharide digestion in neonatal foals. Journal of Animal Science 70, 1175–1181.CrossRefGoogle ScholarPubMed
Shulman, R. J., Henning, S. J. & Nicholls, B. L. (1988). The miniature pig as an animal model for the study of intestinal enzyme development. Pediatric Research 23, 311–315.CrossRefGoogle Scholar
Siegel, C. D., Sparks, J. W. & Battaglia, F. C. (1988). Patterns of serum glucose and galactose concentrations in term newborn infants after milk feeding. Biology of the Neonate 54, 301–306.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, 625–633.CrossRefGoogle Scholar
Smith, M. W. & James, P. S. (1987). Cellular origin of lactase decline in postweaned rats. Biochimica et Biophysica Acta 905, 503–506.CrossRefGoogle ScholarPubMed
Spedale, S. B., Battaglia, F. C. & Sparks, J. W. (1992). Hepatic metabolism of glucose, galactose, and lactate after milk feeding in newborn lambs. American Journal of Physiology 262, E46–E51.Google ScholarPubMed
Tsuboi, K. K., Kwong, L. K., D'Harlingue, A. E., Stevenson, D. K., Kerner, J. A. Jr & Sunshine, P. (1985). The nature of maturational decline of intestinal lactase activity. Biochimica et Biophysica Acta 840, 69–78.CrossRefGoogle ScholarPubMed
Tsuboi, K. K., Kwong, L. K., Neu, J. & Sunshine, P. (1981). A proposed mechanism of normal intestinal lactase decline in the postweaned mammal. Biochemical and Biophysical Research Communications 101, 645–652.CrossRefGoogle ScholarPubMed
Walker, D. M. 1959. The development of the digestive system of the young animal. II. Carbohydrase enzyme development in the young pig. Journal of Agricultural Science 52, 357–363.CrossRefGoogle Scholar
Williams, C. A. (1986). Metabolism of lactose and galactose in man. Progress in Biochemistry and Pharmacology 21, 219–247.Google ScholarPubMed
Williams, C. A., Philips, T. & Macdonald, I. (1983). The influence of glucose on serum galactose levels in man. Metabolism 32, 250–256.CrossRefGoogle ScholarPubMed
Wright, N. A. (1982). The experimental analysis of changes in proliferative and morphological status in studies on the intestine. Scandinavian Journal of Gastroenterology 17, Suppl. 74, 3–10.Google Scholar
Yeh, K. C. & Kwan, K. C. (1978). A comparison of numerical integrating algorithms by trapezoidal, lagrange and spline approximation. Journal of Pharmacokinetics and Biopharmaceutics 6, 79–98.CrossRefGoogle ScholarPubMed