Abstract
The pathophysiologic effects ofCampylobacterjejuni on weanling ferrets were investigated by assessing jejunal disaccharidase activities, glucose and theophylline stimulation of jejunal mucosal ion transport, fecal levels of reducing sugars, and histologic appearance of the gut. Compared with uninoculated controls, ferrets at the peak ofCampylobacter-induced watery diarrhea exhibited two- to threefold reductions in sucrase, maltase, and lactase activity, a sixfold lower short-circuit current response to glucose stimulation, and a twofold higher response to theophylline stimulation, plus a striking increase in fecal levels of reducing sugars. These physiologic alterations rapidly returned to normal as diarrhea subsided. Jejunal epithelial cells of all diarrheic animals appeared morphologically normal by light microscopy. Passively immunized kits, heavily colonized but not diarrheic, were indistinguishable from controls in every assessment. These observations suggest that (i)Campylobacterjejuni exerts its pathophysiologic effect primarily by inducing a transient depression of intestinal brush border function and (ii) such effects can be prevented by humoral antibodies.
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Literature Cited
Alpers DH, Seetharam B (1977) Pathophysiology of diseases involving intestinal brush-border proteins. Gastroenterology 296:1047–1050
An NQ, Evans HE (1988) Anatomy of the ferret. In: Fox JG (ed) Biology and diseases of the ferret. Philadelphia: Lea & Febiger, pp 14–65
Bell JA, Manning DD (1990) A domestic ferret model of immunity toCampylobacter jejuni-induced enteric disease. Infect Immun 58:1848–1852
Bell JA, Manning DD (1990) Pathogenicity ofCampylobacter jejuni in intraperitoneally or intravenously inoculated ferrets. Curr Microbiol 21:47–51
Black RE, Levine MM, Clements ML, Hughes TP, Blaser MJ (1988) ExperimentalCampylobacter jejuni infection in humans. J Infect Dis 157:472–479
Burgess EA, Levin B, Mahalanabis D, Tonge RE (1964) Hereditary sucrose intolerance: levels of sucrase activity in jejunal mucosa. Arch Dis Child 39:431–443
Fernandez H, Neto UF, Fernandez F, Pedra MA, Trabulsi LR (1983) Culture supernatants ofCampylobacter jejuni induce a secretory response in jejunal segments of adult rats. Infect Immun 40:429–431
Fox JG, Ackerman JI, Newcomer CE (1983) Ferret as a potential reservoir for human campylobacteriosis. Am J Vet Res 44:1049–1052
Fox JG, Krakowka S, Taylor N (1985) Acute-onsetCampylobacter-associated gastroenteritis in adult beagles. J Am Vet Med Assoc 187:1268–1271
Fox JG, Ackerman JI, Taylor N, Claps M, Murphy JC (1987)Campylobacter jejuni infection in the ferret: an animal model of human campylobacteriosis. Am J Vet Res 48:85–90
Gianella R (1979) Importance of the intestinal inflammatory reaction in salmonella-mediated intestinal secretion. Infect Immun 23:140–145
Guedon C, Schmitz J, Lerebours E, Metayer J, Audran E, Hemet J, Colin R (1986) Deceased brush border hydrolase activities without gross morphological changes in human intestinal mucosa after prolonged total parenteral nutritution of adults. Gastroenterology 90:373–378
Hore P, Messer M (1968) Studies on disaccharidase activities of the small intestine of the domestic cat and other carnivorous mammals. Comp Biochem Physiol 24:717–725
Jonas A, Krishman C, Forstner G (1978) Pathogenesis of mucosal injury in the blind loop syndrome. Gastroenterology 75:791–795
Kazmi SU, Roberson BS, Stean NJ (1984) Animal-passed virulence-enhancedCampylobacter jejuni enteritis in neonatal mice. Curr Microbiol 11:159–164
Kimberg DV, Field M, Johnson J, Henderson A, Gershon E (1971) Stimulation of intestinal mucosal adenyl cyclase by cholera enterotoxin and prostaglandins. J Clin Invest 50:1218–1230
Klipstein FA, Engert RF (1988) Properties of crudeCampylobacter jejuni heat-labile enterotoxin. Infect Immun 45:314–319
Klipstein FA, Engert RF, Short HB (1986) Enzyme-linked immunosorbent assays for virulence properties ofCampylobacter jejuni clinical isolates. J Clin Microbiol 23:1039–1043
Lifshitz F, Coella-Ramirez R, Gutierez-Topete G, Cornado-Cornet MC (1971) Carbohydrate intolerance in infants with diarrhea. J Pediat 79:760–767
Manninen KI, Prescott JF, Dohoo IR (1982) Pathogenicity ofCampylobacter jejuni isolates from animals and humans. Infect Immun 38:46–52
McClung HJ, Butler DG, Kerzner B, Gall DG, Hamilton JR (1976) Transmissible gastroenteritis: mucosal ion transport in acute viral enteritis. Gastroenterology 70:1091–1095
Munck BG (1972) Effects of sugar and amino acid transport on transepithelial fluxes of sodium and chloride of short circuited rat jejunum. J Physiol 223:699–717
Prescott JF, Karmali MA (1978) Attempts to transmitCampylobacter enteritis to dogs and cats. Can Med Assoc J 119:1001–1002
Rohde JE, Anderson B (1973) In vitro measurement of ion fluxes across biopsies of human jejunal mucosa during cholera. J App Physiol 35:557–561
van Spreeuwel JP, Duursma GC, Meijer CJLM, Bax R, Rosekrans PCM, Lindeman J (1985)Campylobacter colitis: histological, immunohistochemical and ultrastructural findings. Gut 26:945–951
Walker RI, Caldwell MB, Lee EC, Guerry P, Trust TJ, Ruiz-Palacios GM (1986) Pathophysiology ofCampylobacter enteritis. Microbiol Rev 50:81–94
Yeen WP, Puthucheary SD, Pang T (1983) Demonstration of a cytotoxin fromCampylobacter jejuni. J Clin Pathol 36:1237–1240
Youssef M, Cothier G, Goossens M, Tancrede C, Henry-Amar M, Andremont A (1987) Comparative translocation of enteropathogenicCampylobacter spp. andEscherichia coli from the intestinal tract of gnotobiotic mice. Infect Immun 55:1019–1021
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Bell, J.A., Manning, D.D. Role of temporary intestinal brush border dysfunction inCampylobacter jejuni diarrhea. Current Microbiology 21, 355–359 (1990). https://doi.org/10.1007/BF02199437
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DOI: https://doi.org/10.1007/BF02199437