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. 1996 May 15;97(10):2308–2315. doi: 10.1172/JCI118673

Use of maltose hydrolysis measurements to characterize the interaction between the aqueous diffusion barrier and the epithelium in the rat jejunum.

M D Levitt 1, C Fine 1, J K Furne 1, D G Levitt 1
PMCID: PMC507311  PMID: 8636411

Abstract

Rates of intestinal absorption and surface hydrolysis are determined by the interaction of two barriers: poorly stirred fluid adjacent to the mucosa, and the epithelial cell. These two barriers commonly are modeled as a fixed, flat layer of epithelium covered by a fixed thickness of unstirred fluid. To more accurately simulate these barriers in a villous mucosa, maltase activity (measured in vitro) was distributed over an anatomically correct model of rat jejunal villi. We then determined what interaction of the aqueous and epithelial barriers best predicted in vivo maltose hydrolysis rates measured over a broad range of infusate concentrations. Hydrolysis was accurately predicted by a model in which unstirred fluid extended from 20 microm over the villous tips throughout the intervillous space. In this model, the depth of diffusion into the intervillous space is inversely proportional to the efficiency of epithelial handling of the solute. As a result, both the aqueous barrier and the functional surface area are variables rather than constants. Some implications of our findings (relative to the conventional model) include: higher predicted Vmax, efficient handling of low concentrations of a solute at the villous tips while high concentrations must penetrate thick aqueous barriers, and sensitive regulation of transport rates via ease of access to the intervillous space.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. DOW P. Estimations of cardiac output and central blood volume by dye dilution. Physiol Rev. 1956 Jan;36(1):77–102. doi: 10.1152/physrev.1956.36.1.77. [DOI] [PubMed] [Google Scholar]
  2. Dietschy J. M., Sallee V. L., Wilson F. A. Unstirred water layers and absorption across the intestinal mucosa. Gastroenterology. 1971 Dec;61(6):932–934. [PubMed] [Google Scholar]
  3. Fine K. D., Santa Ana C. A., Porter J. L., Fordtran J. S. Effect of D-glucose on intestinal permeability and its passive absorption in human small intestine in vivo. Gastroenterology. 1993 Oct;105(4):1117–1125. doi: 10.1016/0016-5085(93)90957-e. [DOI] [PubMed] [Google Scholar]
  4. Frase L. L., Strickland A. D., Kachel G. W., Krejs G. J. Enhanced glucose absorption in the jejunum of patients with cystic fibrosis. Gastroenterology. 1985 Feb;88(2):478–484. doi: 10.1016/0016-5085(85)90510-4. [DOI] [PubMed] [Google Scholar]
  5. Gray G. M., Ingelfinger F. J. Intestinal absorption of sucrose in man: interrelation of hydrolysis and monosaccharide product absorption. J Clin Invest. 1966 Mar;45(3):388–398. doi: 10.1172/JCI105354. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Harris M. S., Kennedy J. G. Relationship between distention and absorption in rat intestine. II. Effects of volume and flow rate on transport. Gastroenterology. 1988 May;94(5 Pt 1):1172–1179. doi: 10.1016/0016-5085(88)90009-1. [DOI] [PubMed] [Google Scholar]
  7. Harris M. S., Kennedy J. G., Siegesmund K. A., Yorde D. E. Relationship between distention and absorption in rat intestine. I. Effect of luminal volume on the morphology of the absorbing surface. Gastroenterology. 1988 May;94(5 Pt 1):1164–1171. doi: 10.1016/0016-5085(88)90008-x. [DOI] [PubMed] [Google Scholar]
  8. Levitt M. D., Furne J. K., Strocchi A., Anderson B. W., Levitt D. G. Physiological measurements of luminal stirring in the dog and human small bowel. J Clin Invest. 1990 Nov;86(5):1540–1547. doi: 10.1172/JCI114873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Levitt M. D., Strocchi A., Levitt D. G. Human jejunal unstirred layer: evidence for extremely efficient luminal stirring. Am J Physiol. 1992 Mar;262(3 Pt 1):G593–G596. doi: 10.1152/ajpgi.1992.262.3.G593. [DOI] [PubMed] [Google Scholar]
  10. McMichael H. B., Webb J., Dawson A. M. The absorption of maltose and lactose in man. Clin Sci. 1967 Aug;33(1):135–145. [PubMed] [Google Scholar]
  11. Read N. W., Barber D. C., Levin R. J., Holdsworth C. D. Unstirred layer and kinetics of electrogenic glucose absorption in the human jejunum in situ. Gut. 1977 Nov;18(11):865–876. doi: 10.1136/gut.18.11.865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Schwartz R. M., Furne J. K., Levitt M. D. Paracellular intestinal transport of six-carbon sugars is negligible in the rat. Gastroenterology. 1995 Oct;109(4):1206–1213. doi: 10.1016/0016-5085(95)90580-4. [DOI] [PubMed] [Google Scholar]
  13. Smithson K. W., Millar D. B., Jacobs L. R., Gray G. M. Intestinal diffusion barrier: unstirred water layer or membrane surface mucous coat? Science. 1981 Dec 11;214(4526):1241–1244. doi: 10.1126/science.7302593. [DOI] [PubMed] [Google Scholar]
  14. Thomson A. B., Dietschy J. M. Derivation of the equations that describe the effects of unstirred water layers on the kinetic parameters of active transport processes in the intestine. J Theor Biol. 1977 Jan 21;64(2):277–294. doi: 10.1016/0022-5193(77)90357-5. [DOI] [PubMed] [Google Scholar]
  15. Westergaard H., Dietschy J. M. Delineation of the dimensions and permeability characteristics of the two major diffusion barriers to passive mucosal uptake in the rabbit intestine. J Clin Invest. 1974 Sep;54(3):718–732. doi: 10.1172/JCI107810. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Westergaard H., Holtermüller K. H., Dietschy J. M. Measurement of resistance of barriers to solute transport in vivo in rat jejunum. Am J Physiol. 1986 Jun;250(6 Pt 1):G727–G735. doi: 10.1152/ajpgi.1986.250.6.G727. [DOI] [PubMed] [Google Scholar]
  17. Winne D. Unstirred layer, source of biased Michaelis constant in membrane transport. Biochim Biophys Acta. 1973 Feb 27;298(1):27–31. doi: 10.1016/0005-2736(73)90005-9. [DOI] [PubMed] [Google Scholar]
  18. Womack W. A., Barrowman J. A., Graham W. H., Benoit J. N., Kvietys P. R., Granger D. N. Quantitative assessment of villous motility. Am J Physiol. 1987 Feb;252(2 Pt 1):G250–G256. doi: 10.1152/ajpgi.1987.252.2.G250. [DOI] [PubMed] [Google Scholar]

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