Prevalence and Epidemiology of Non-O157 Escherichia coli Serogroups O26, O103, O111, and O145 and Shiga Toxin Gene Carriage in Scottish Cattle, 2014-2015.

Deborah V Hoyle,Marianne Keith,Margo E Chase-Topping,Helen Williamson,Anne Holmes,Madeleine K Henry,Sue C Tongue,Rebecca Mclean,Judith Evans,Rebecca Callaby,Lesley Allison,Heather Mathie,Carol Currie,Nuno Silva,Thibaud Porphyre,Kareen Macleod,David L Gally,Ian Handel,George J Gunn

doi:10.1128/aem.03142-20

Abstract

Cattle are a reservoir for Shiga toxin-producing Escherichia coli (STEC), zoonotic pathogens that cause serious clinical disease. Scotland has a higher incidence of STEC infection in the human population than the European average. The aim of this study was to investigate the prevalence and epidemiology of non-O157 serogroups O26, O103, O111, and O145 and Shiga toxin gene carriage in Scottish cattle. Fecal samples (n = 2783) were collected from 110 herds in 2014 and 2015 and screened by real-time PCR. Herd-level prevalence (95% confidence interval [CI]) for O103, O26, and O145 was estimated as 0.71 (0.62, 0.79), 0.43 (0.34, 0.52), and 0.23 (0.16, 0.32), respectively. Only two herds were positive for O111. Shiga toxin prevalence was high in both herds and pats, particularly for stx2 (herd level: 0.99; 95% CI: 0.94, 1.0). O26 bacterial strains were isolated from 36 herds on culture. Fifteen herds yielded O26 stx-positive isolates that additionally harbored the intimin gene; six of these herds shed highly pathogenic stx2-positive strains. Multiple serogroups were detected in herds and pats, with only 25 herds negative for all serogroups. Despite overlap in detection, regional and seasonal effects were observed. Higher herd prevalence for O26, O103, and stx1 occurred in the South West, and this region was significant for stx2 at the pat level (P = 0.015). Significant seasonal variation was observed for O145 prevalence, with the highest prevalence in autumn (P = 0.032). Negative herds were associated with Central Scotland and winter. Herds positive for all serogroups were associated with autumn and larger herd size and were not housed at sampling.IMPORTANCE Cattle are reservoirs for Shiga toxin-producing Escherichia coli (STEC), bacteria shed in animal feces. Humans are infected through consumption of contaminated food or water and by direct contact, resulting in serious disease and kidney failure in the most vulnerable. The contribution of non-O157 serogroups to STEC illness was underestimated for many years due to the lack of specific tests. Recently, non-O157 human cases have increased, with O26 STEC of particular note. It is therefore vital to investigate the level and composition of non-O157 in the cattle reservoir and to compare them historically and by the clinical situation. In this study, we found cattle prevalence high for toxin, as well as for O103 and O26 serogroups. Pathogenic O26 STEC were isolated from 14% of study herds, with toxin subtypes similar to those seen in Scottish clinical cases. This study highlights the current risk to public health from non-O157 STEC in Scottish cattle.

Highlights

Shiga toxin-producing Escherichia coli (STEC) strains are zoonotic bacteria that cause a spectrum of disease in humans, from asymptomatic carriage or mild diarrhea through to hemorrhagic colitis and hemolytic uremic syndrome (HUS) [1]
O103 was the most common serogroup, followed by O26, and only 25 farms were negative for all four non-O157 serogroups
The prevalence for all non-O157 serogroups examined was higher, mirroring the current pattern observed in Scottish human clinical cases

Summary

Introduction

Shiga toxin-producing Escherichia coli (STEC) strains are zoonotic bacteria that cause a spectrum of disease in humans, from asymptomatic carriage or mild diarrhea through to hemorrhagic colitis and hemolytic uremic syndrome (HUS) [1]. A new classification system has recently been proposed, the JEMRA scheme [13], based upon virulence gene composition Under this scheme, STEC strains carrying the stx2a gene (with or without stx1a) together with eae are classified as JEMRA level 1, the most pathogenic tier, capable of inducing bloody diarrhea and HUS. The predominance of nonO157 STEC has become evident over the past decade, in Ireland [14], the wider European Union/European Economic Area region [15], and the United States [16,17,18] This is due in part to the change in methodology of molecular-based assays, as well as to mandatory requirements to report non-O157 STEC cases in many countries. Non-O157 STEC strains represent an increasing public health concern

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