Inverse relationship between heat stable enterotoxin-b induced fluid accumulation and adherence of F4ac-positive enterotoxigenic Escherichia coli in ligated jejunal loops of F4ab/ac fimbria receptor-positive swine

Joseph Erume, Prageeth Wijemanne, Emil M. Berberov, Stephen D. Kachman, Daniel J. Oestmann, David H. Francis, Rodney A. Moxley

Research output: Contribution to journalArticle

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Abstract

Heat-labile enterotoxin (LT) produced by enterotoxigenic Escherichia coli (ETEC) increases bacterial adherence to porcine enterocytes in vitro and enhances small intestinal colonization in swine. Heat-stable enterotoxin-b (STb) is not known to affect colonization; however, through an induction of net fluid accumulation it might reduce bacterial adherence. The relationship between fluid accumulation and bacterial adherence in jejunal loops inoculated with ETEC strains that produce LT, STb, both, or neither toxin was studied. Ligated jejunal loops were constructed in weaned Yorkshire pigs in two independent experiments (Exp. 1, n=5, 8-week-old; Exp. 2, n=6, 6-8-week-old). Each pig was inoculated with six F4ac+ E. coli strains: (1) LT+, STb+ parent (WAM2317); (2) STb- (ΔestB) mutant (MUN297); (3) MUN297 complemented with STb (MUN298); (4) LT- STb- (ΔeltAB ΔestB) mutant (MUN300); (5) MUN300 complemented with LT (MUN301); and (6) 1836-2 (non-enterotoxigenic, wild-type). Pigs were confirmed to be K88 (F4)ab/ac receptor-positive in Exp. 2 by testing for intestinal mucin-type glycoproteins and inferred to be receptor-positive in both Exp. 1 and 2 based on histopathologic evidence of bacterial adherence. Strains that produced STb induced marked fluid accumulation with the response (ml/cm) to WAM2317 and MUN298 significantly greater than that to the other strains (P<0.0001). Conversely, bacterial adherence scores based on immunohistochemistry and CFU/g of washed mucosa were both lowest in the strains that expressed STb and highest in those that did not. For the two experiments combined, the Pearson correlation coefficient (R) between fluid volume (ml/cm) and log CFU per gram was -0.57021 (P<0.0001); R2=0.3521 (n=197). These results support the hypothesis that enterotoxin-induced fluid accumulation flushes progeny organisms into the lumen of the bowel, thereby increasing the likelihood of fecal shedding and transmission of the pathogen to new hosts.

Original languageEnglish (US)
Pages (from-to)315-324
Number of pages10
JournalVeterinary Microbiology
Volume161
Issue number3-4
DOIs
StatePublished - Jan 25 2013

Fingerprint

Enterotoxigenic Escherichia coli
enterotoxigenic Escherichia coli
fimbriae
Enterotoxins
enterotoxins
Swine
Hot Temperature
heat
bacterial adhesion
receptors
swine
Mucin-2
fluids
mutants
Infectious Disease Transmission
Enterocytes
mucins
Yorkshire (swine breed)
enterocytes
mucosa

Keywords

  • Escherichia coli
  • Heat-labile enterotoxin
  • Heat-stable enterotoxin-b
  • Mucin-4 gene

ASJC Scopus subject areas

  • Microbiology
  • veterinary(all)

Cite this

Inverse relationship between heat stable enterotoxin-b induced fluid accumulation and adherence of F4ac-positive enterotoxigenic Escherichia coli in ligated jejunal loops of F4ab/ac fimbria receptor-positive swine. / Erume, Joseph; Wijemanne, Prageeth; Berberov, Emil M.; Kachman, Stephen D.; Oestmann, Daniel J.; Francis, David H.; Moxley, Rodney A.

In: Veterinary Microbiology, Vol. 161, No. 3-4, 25.01.2013, p. 315-324.

Research output: Contribution to journalArticle

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abstract = "Heat-labile enterotoxin (LT) produced by enterotoxigenic Escherichia coli (ETEC) increases bacterial adherence to porcine enterocytes in vitro and enhances small intestinal colonization in swine. Heat-stable enterotoxin-b (STb) is not known to affect colonization; however, through an induction of net fluid accumulation it might reduce bacterial adherence. The relationship between fluid accumulation and bacterial adherence in jejunal loops inoculated with ETEC strains that produce LT, STb, both, or neither toxin was studied. Ligated jejunal loops were constructed in weaned Yorkshire pigs in two independent experiments (Exp. 1, n=5, 8-week-old; Exp. 2, n=6, 6-8-week-old). Each pig was inoculated with six F4ac+ E. coli strains: (1) LT+, STb+ parent (WAM2317); (2) STb- (ΔestB) mutant (MUN297); (3) MUN297 complemented with STb (MUN298); (4) LT- STb- (ΔeltAB ΔestB) mutant (MUN300); (5) MUN300 complemented with LT (MUN301); and (6) 1836-2 (non-enterotoxigenic, wild-type). Pigs were confirmed to be K88 (F4)ab/ac receptor-positive in Exp. 2 by testing for intestinal mucin-type glycoproteins and inferred to be receptor-positive in both Exp. 1 and 2 based on histopathologic evidence of bacterial adherence. Strains that produced STb induced marked fluid accumulation with the response (ml/cm) to WAM2317 and MUN298 significantly greater than that to the other strains (P<0.0001). Conversely, bacterial adherence scores based on immunohistochemistry and CFU/g of washed mucosa were both lowest in the strains that expressed STb and highest in those that did not. For the two experiments combined, the Pearson correlation coefficient (R) between fluid volume (ml/cm) and log CFU per gram was -0.57021 (P<0.0001); R2=0.3521 (n=197). These results support the hypothesis that enterotoxin-induced fluid accumulation flushes progeny organisms into the lumen of the bowel, thereby increasing the likelihood of fecal shedding and transmission of the pathogen to new hosts.",
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AU - Berberov, Emil M.

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AU - Oestmann, Daniel J.

AU - Francis, David H.

AU - Moxley, Rodney A.

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