Outbreaks of Shiga Toxin–Producing Escherichia coli Linked to Sprouted Seeds, Salad, and Leafy Greens: A Systematic Review

Abstract

ABSTRACT Shiga toxin–producing Escherichia coli (STEC) outbreaks involving ready-to-eat salad products have been described in the scientific literature since 1995. These products typically do not undergo a definitive control step such as cooking to eliminate pathogens. To reduce the number of STEC infections from salad products, efforts will need to focus on preventing and reducing contamination throughout the food chain. We performed a systematic review of STEC outbreaks involving sprouted seeds, salad, or leafy green products to determine whether there were recurrent features, such as availability of microbiological evidence or identification of the contamination event, which may inform future investigations and prevention and control strategies. Thirty-five STEC outbreaks linked to contaminated leafy greens were identified for inclusion. The outbreaks occurred from 1995 to 2018 and ranged from 8 to more than 8,500 cases. Detection of STEC in the food product was rare (4 of 35 outbreaks). For the remaining outbreaks, the determination of leafy greens as the source of the outbreak mainly relied on analytical epidemiology (20 of 35) or descriptive evidence (11 of 35). The traceback investigation in 21 of 32 outbreaks was not able to identify possible routes leading to where the STEC bacteria came from or how the leaves were contaminated. Investigations in eight outbreaks found poor practice during processing that may have contributed to the outbreak, such as insufficient postharvest disinfection of the product. Six outbreak investigations were able to identify the outbreak strain in animal feces near the growing fields; two of these were also able to find it in irrigation water on the farms, providing a likely route of contamination. These results highlight the limitations of relying on microbiological confirmation as a basis to initiate investigations of upstream production to understand the source of contamination. This review also demonstrates the importance of, and difficulties associated with, food-chain traceback studies to inform control measures and future prevention.