Avian-pathogenic Escherichia coli strains are similar to neonatal meningitis E. coli strains and are able to cause meningitis in the rat model of human disease

Abstract

Escherichia coli strains causing avian colibacillosis and human neonatal meningitis, urinary tract infections, and septicemia are collectively known as extraintestinal pathogenic E. coli (ExPEC). Characterization of ExPEC strains using various typing techniques has shown that they harbor many similarities, despite their isolation from different host species, leading to the hypothesis that ExPEC may have zoonotic potential. The present study examined a subset of ExPEC strains: neonatal meningitis E. coli (NMEC) strains and avian-pathogenic E. coli (APEC) strains belonging to the O18 serogroup. The study found that they were not easily differentiated on the basis of multilocus sequence typing, phylogenetic typing, or carriage of large virulence plasmids. Among the APEC strains examined, one strain was found to be an outlier, based on the results of these typing methods, and demonstrated reduced virulence in murine and avian pathogenicity models. Some of the APEC strains tested in a rat model of human neonatal meningitis were able to cause meningitis, demonstrating APEC's ability to cause disease in mammals, lending support to the hypothesis that APEC strains have zoonotic potential. In addition, some NMEC strains were able to cause avian colisepticemia, providing further support for this hypothesis. However, not all of the NMEC and APEC strains tested were able to cause disease in avian and murine hosts, despite the apparent similarities in their known virulence attributes. Thus, it appears that a subset of NMEC and APEC strains harbors zoonotic potential, while other strains do not, suggesting that unknown mechanisms underlie host specificity in some ExPEC strains.

FIG. 1.

Plasmids purified from the test and control strains. Previously sequenced plasmids present in APEC O1, APEC O2, and APEC χ7122 were used as size standards. All strains except NMEC 4 contained at least one large plasmid which correlated 100% with the presence of the RepFIB amplicon. Note that a similarly sized plasmid (∼133 kb) is carried by all APEC O18 isolates.

FIG. 2.

PFGE of XbaI-digested DNA from the O18 strains. Strain designations, phylogenetic groups, MLST assignments, and virulence genes associated with the conserved virulence region of APEC plasmids are shown at right. This dendrogram prepared by the unweighted-pair group method using average linkages was generated in BioNumerics software by using the Dice coefficient with a 1.0% band position tolerance. The scale above the dendrogram indicates percent similarity.

FIG. 3.

(A) Histopathology of rat brain tissue 24 h postinoculation with APEC 353 showed rod-shaped bacteria (arrow) in the meninges. (B) Histopathology of rat brain tissue 24 h postinoculation with NMEC 58 with rod-shaped bacteria in the meninges (arrows).

FIG. 4.

Percent mortality observed for each strain when it was examined using the murine and avian pathogenicity models. For each strain, the same lowercase letter on top of the column indicates that the mortality was not significantly different (P ≥ 0.05 by Fisher's exact test) between pathogenicity models. Note that not every strain was examined in all of the three pathogenicity models (marked by •).