Summary
Ischaemia of the dog intestine lasting 1 h causes desquamation of the epithelium at the villus tips and congestion in the villus capillaries. The crypt cells are relatively undamaged. These changes are associated with a loss of active transport of organic solutes, determined in vitro, a reduction in mucosal sucrase activity and an abolition of glucose absorption in vivo. A profuse net loss of water and electrolytes into the lumen in vivo develops. The net sodium loss is due primarily to an inhibition of the lumen-blood flux of this ion, the blood-lumen flux being relatively unchanged. In uraemic dogs, the loss of urea into the lumen is the same in control and ischaemic loops, testifying to the lack of change in the unidirectional water flow from blood to lumen.
Perfusion of the dog intestine with 1% Triton X-100 leads to morphological changes that have certain similarities with those provoked by ischaemia. Damage was restricted to the villus tips, protection from further alterations apparently being provided by a mucus layer that forms on the mucosal surface; the crypt region remained unchanged. After 10 min exposure, organic solute transport in vitro and glucose absorption in vivo were both reduced but not abolished; sodium and water absorption in vivo were suppressed, but no net secretion occurred.
To account for these observations, we have suggested that the normal crypt cell is a secretory element with respect to sodium and water. During maturation, its absorptive properties develop such that the mature enterocyte, possessing both absorptive and secretory mechanisms, is capable of net absorption of sodium. After destruction of the villus tips, net secretion continues in the crypts; if there are insufficient villus cells remaining to ensure reabsorption, a net secretory capacity is observed.
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References
Browning JG, Hardcastle J, Hardcastle PT, Redfern JS (1978) Localization of the effect of acetylcholine in regulating intestinal ion transport. J Physiol (Lond) 281:15–27
Charney AN, Donowitz M (1976) Prevention and reversal of cholera enterotoxin-induced intestinal secretion by methylprednisolone induction of Na+-K+-ATPase. J Clin Invest 57:1590–1599
Charney AN, Gots RE, Giannella RA (1974) (Na+-K+)-stimulated adenosine-triphosphatase in isolated villus tip and crypt cells. Biochim Biophys Acta 367:265–270
Clarke RM, Kobayashi S (1975) The cytological effects of infusion of luminal polyethylene glycol in the rat small intestinal mucosa. Arch Histol Japon 38:133–150
Cook BH, Wilson ER, Taylor AE (1971) Intestinal fluid loss in hemorrhagic shock. Am J Physiol 221:1494–1498
Dahlqvist A (1964) Method for assay of intestinai disaccharidases. Anal Biochem 7:18–25
Dawson RMC, Elliott DC, Elliott WH, Jones KM (1959) Data for Biochemical Research. Clarendon Press, Oxford, pp 208–209
de Jonge HR (1975) The response of small intestinal villous and crypt epithelium to cholera toxin in rat and guinea pig. Evidence against a specific role of the crypt cells in cholerageninduced secretion. Biochim Biophys Acta 381:128–143
Drüeke T, Ganeval D, Pleau JM (1972) Perfusion d'une anse jéjunale isolée chez la rat urémique. Étude de flux nets et de clearances. Possibilités actuelles d'application à l'homme. Rev Eur Ét Clin Biol 17:159–168
Duffy PA, Granger DN, Taylor AE (1978) Intestinal secretion induced by volume expansion in the dog. Gastroenterology 75:413–418
Eder M (1965) Experimentelle Untersuchungen über Schädigung der Dünndarmschleimhaut. Verh Dtsch Ges Pathol 49:330–333
Field M (1974) Intestinal secretion. Gastroenterology 66:1063–1084
Field M (1976) Regulation of active ion transport in the small intestine. CIBA Fdn Symp 42:109–127
Gall DG, Chapman D, Kelly M, Hamilton JR (1977) Na+ transport in jejunal crypt cells. Gastroenterology 72:452–456
Goulson KJ, Skyring A (1966) The effect of colchicine on the absorption of water and electrolytes by rat jejunum. Austr J Exp Biol Med Sci 44:93–100
Gutschmidt S, Kaul W, Riecken EO (1979) A quantitative histochemical technique for the characterisation ofα-glucosidases in the brush-border membrane of rat jejunum. Histochemistry 63:81–101
Hamilton JR (1967) Prolonged infusion of the small intestine of the rat. Effect of dilute solutions of lactic acid on fat absorption and mucosal morphology. Pediat Res 1:341–353
Hornych A, Loreau N, Richet G (1971) Unidirectional Na flow in rat jejunum before and during intravenous infusion of 0.9% NaCl. Rev Eur Ét Clin Biol 16:673–678
Imondi AR, Balis ME, Lipkin M (1969) Changes in enzyme levels accompanying differentiation of intestinal epithelial cells. Exp Cell Res 58:341–353
Kingham JGC, Whorwell PJ, Loehry CA (1976) Small intestinal permeability. I. Effects of ischaemia and exposure to acetyl salicylate. Gut 17:354–361
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
Menge H, Robinson JWL (1979) Early phase of jejunal regeneration after short term ischemia in the rat. Lab Invest 40:25–30
Menge H, Robinson JWL, Mirkovitch V (1977) Influence of the colonic contents on the structure and function of the rat jejunal mucosa. Exp Molec Pathol 26:204–213
Mirkoyitch V, Menge H, Robinson JWL (1974) The effect of intraluminal hydrostatic pressure on intestinal absorption in vivo. Experientia 30:912–913
Mirkovitch V, Menge H, Robinson JWL (1975) Protection of the intestinal mucosa during ischaemia by intraluminal perfusion. Res Exp Med 166:183–191
Modigliani R, Bernier JJ (1972) Effets du glucose sur les mouvements nets et unidirectionnels de l'eau et des électrolytes dans l'intestin grêle de l'homme. Biol Gastroent 5:165–174
Nasset ES, Ju JS (1973) Micropipet collection of succus entericus at crypt ostia of guinea pig jejunum. Digestion 9:205–211
Riecken EO, Bloch R, Menge H, Idelberger K, Kramer F, Miller B, Lorenz-Meyer H (1972) Morphologische und funktionelle Befunde nach Milchsäuredauerinfusion in das Jejunum der Ratte. Z Zellforsch Mikr Anat 132:107–129
Robinson JWL, Menge H, Sepúlveda FV, Cobo F, Mirkovitch V (1976) The functional response of the dog ileum to one hour's ischaemia. Clin Sci molec Med 50:115–122
Robinson JWL, Mirkovitch V (1972) The recovery of function and microcirculation in small intestinal loops following ischaemia. Gut 13:784–789
Robinson JWL, Mirkovitch V (1977) The roles of intraluminal oxygen and glucose in the protection of the rat intestinal mucosa from the effects of ischaemia. Biomedicine 27:60–62
Robinson JWL, Mirkovitch V, Menge H (1977) Consequences of the destruction of the villus epithelium by ischaemia or Triton X-100. Gut 18:425
Roggin GM, Banwell JG, Yardley JH, Hendrix TR (1972) Unimpaired response of rabbit jejunum to cholera toxin after selective damage to villus epithelium. Gastroenterology 63:981–989
Serebro HA, Iber FL, Yardley JH, Hendrix TR (1969) Inhibition of cholera toxin action in the rabbit by cycloheximide. Gastroenterology 56:506–511
Stamm B, Mirkovitch V, Winistörfer B, Robinson JWL, Ozzello L (1974) Regeneration and functional recovery of canine intestinal mucosa following injury caused by formalin. Virchows Arch Zellpathol 17:137–148
van Dongen JM, Kooyman J, Visser WJ, Holt SJ, Galjaard H (1977) The effect ofincreased crypt cell proliferation on the activity and subcellular localization of esterases and alkaline phosphatase in the rat small intestine. Histochem J 9:61–75
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Part of this work was presented to the British Society of Gastroenterology in March 1977, and an abstract was published at that time (32)
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Robinson, J.W.L., Winistörfer, B. & Mirkovitch, V. Source of net water and electrolyte loss following intestinal ischaemia. Res. Exp. Med. 176, 263–275 (1980). https://doi.org/10.1007/BF01855846
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DOI: https://doi.org/10.1007/BF01855846