Contribution of cropland to the spread of Shiga toxin phages and the emergence of new Shiga toxin-producing strains

Pablo Quirós,Maite Muniesa

doi:10.1038/s41598-017-08169-6

Abstract

A growing interest in healthy eating has lead to an increase in the consumption of vegetables, associated with a rising number of bacterial outbreaks related to fresh produce. This is the case of the outbreak in Germany, caused by a O104:H4 enteroaggregative E. coli strain lysogenic for a Stx phage. Temperate Stx phages released from their hosts occur as free particles in various environments. This study reports the occurrence of Stx phages in vegetables (lettuce, cucumber, and spinach) and cropland soil samples. Infectious Stx2 phages were found in all samples and many carried also Stx1 phages. Their persistence in vegetables, including germinated sprouts, of Stx phage 933 W and an E. coli C600 (933 W∆stx::gfp-cat) lysogen used as surrogate, showed reductions below 2 log10 units of both microorganisms at 23 °C and 4 °C over 10 days. Higher reductions (up to 3.9 log10) units were observed in cropland soils at both temperatures. Transduction of a recombinant 933 W∆stx::kan phage was observed in all matrices. Protecting against microbial contamination of vegetables is imperative to ensure a safe food chain. Since the emergence of new Stx strains by Stx phage transduction is possible in vegetable matrices, methods aimed at reducing microbial risks in vegetables should not neglect phages.

Highlights

Shiga toxin-producing Escherichia coli (STEC) are foodborne pathogens associated world wide[1] with human diseases such as diarrhea, hemorrhagic colitis, hemolytic uremic syndrome (HUS), and thrombotic thrombocytopenic purpura (TTP)[2]
An increase in bacterial and viral foodborne disease outbreaks in recent years has been associated with this emerging trend for “healthy eating”
Some bacterial pathogens are found in internal plant tissues, and cannot be washed off or killed by disinfectants

Summary

Introduction

Shiga toxin-producing Escherichia coli (STEC) are foodborne pathogens associated world wide[1] with human diseases such as diarrhea, hemorrhagic colitis, hemolytic uremic syndrome (HUS), and thrombotic thrombocytopenic purpura (TTP)[2]. Recent years have witnessed a global trend toward eating a healthy diet rich in fruits, vegetables, and fresh, raw vegetable products These vegetables may have been grown in soil in open fields, entailing a risk of contamination by toxins or pathogens[14]. Soil, manure, and irrigation water are important sources of plant contamination[15, 16] At all these stages, the interactions between vegetables and enteric pathogens may be more complex than previously thought. A growing number of foodborne illnesses have been increasingly traced back to fruits and vegetables in the last ten years[18,19,20,21], arousing concern that plants might be an important vehicle for human enteric pathogens. In 2011, there was a major outbreak in the European Union (Germany and France) of STEC O104:H4 traced to sprouted fenugreek seeds produced in Egypt, in which 3,816 people were infected, 845 developed HUS and 54 died[22, 23]

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