Levels and genotypes of Salmonella and levels of Escherichia coli in frozen ready-to-cook chicken and turkey products in England tested in 2020 in relation to an outbreak of S. Enteritidis

Frieda Jørgensen; Jim McLauchlin; Neville Q Verlander; Heather Aird; Sooria Balasegaram; Marie Anne Chattaway; Tim Dallman; M Trent Herdman; Ann Hoban; Sandra Lai; Lesley Larkin; Jacquelyn McCormick; Lorraine Sadler Reeves; Caroline Willis

doi:10.1016/j.ijfoodmicro.2022.109609

Levels and genotypes of Salmonella and levels of Escherichia coli in frozen ready-to-cook chicken and turkey products in England tested in 2020 in relation to an outbreak of S. Enteritidis

Int J Food Microbiol. 2022 May 16:369:109609. doi: 10.1016/j.ijfoodmicro.2022.109609. Epub 2022 Mar 3.

Authors

Affiliations

¹ Food Water and Environmental Microbiology Laboratory Porton, UK Health Security Agency, Salisbury, UK. Electronic address: frieda.jorgensen@phe.gov.uk.
² Food Water and Environmental Microbiology Services, UK Health Security Agency, London, UK. Electronic address: jim.mclauchlin@phe.gov.uk.
³ Statistics, Modelling and Economics Department, UK Health Security Agency, London, UK. Electronic address: neville.verlander@phe.gov.uk.
⁴ Food Water and Environmental Microbiology Laboratory York, UK Health Security Agency, York, UK. Electronic address: heather.aird@phe.gov.uk.
⁵ Field Service, UK Health Security Agency, London, UK. Electronic address: sooria.balasegaram@phe.gov.uk.
⁶ Gastrointestinal Bacteria Reference Unit, UK Health Security Agency, London, UK. Electronic address: marie.chattaway@phe.gov.uk.
⁷ Gastrointestinal Bacteria Reference Unit, UK Health Security Agency, London, UK. Electronic address: t.j.dallman@uu.nl.
⁸ Field Service, UK Health Security Agency, London, UK. Electronic address: trent.herdman@nhs.net.uk.
⁹ Gastrointestinal Pathogens and Food Safety (One Health) Division, UK Health Security Agency, London, UK. Electronic address: ann.hoban@phe.gov.uk.
¹⁰ Food Water and Environmental Microbiology Laboratory London, UK Health Security Agency, London, UK. Electronic address: sandra.lai@phe.gov.uk.
¹¹ Gastrointestinal Pathogens and Food Safety (One Health) Division, UK Health Security Agency, London, UK. Electronic address: lesley.larkin@phe.gov.uk.
¹² Gastrointestinal Pathogens and Food Safety (One Health) Division, UK Health Security Agency, London, UK. Electronic address: jacquelyn.mccormick@phe.gov.uk.
¹³ Food Water and Environmental Microbiology Laboratory Porton, UK Health Security Agency, Salisbury, UK; Field Service, UK Health Security Agency, London, UK. Electronic address: lorraine.sadler-reeves@phe.gov.uk.
¹⁴ Food Water and Environmental Microbiology Laboratory Porton, UK Health Security Agency, Salisbury, UK. Electronic address: caroline.willis@phe.gov.uk.

PMID: 35299050
DOI: 10.1016/j.ijfoodmicro.2022.109609

Abstract

Frozen reformulated (FR) breaded chicken products have previously been implicated in causing human salmonellosis. A multi-country Salmonella enterica serovar Enteritidis outbreak involving several strains with >400 reported human cases in the UK occurred in 2020. Initially S. Infantis was detected in one sample from a case home but S. Enteritidis was then also isolated using a S. Enteritidis specific PCR in combination with isolation via a Craigie-tube. This prompted a survey to examine the presence and levels of Salmonella and E. coli in ready-to-cook FR poultry products in England in 2020. From a total of 483 samples, including two from cases' homes, Salmonella was detected in 42 chicken samples, these originated from six out of 53 production plants recorded. Salmonella detection was associated with elevated levels of generic E. coli (OR = 6.63). S. Enteritidis was detected in 17 samples, S. Infantis in 25, S. Newport in four and S. Java, S. Livingstone and S. Senftenberg in one each. The highest levels of Salmonella were 54 MPN/g for S. Infantis and 28 MPN/g for S. Enteritidis; 60% of the Salmonella-positive samples had <1.0 MPN/g. S. Enteritidis was detected together with S. Infantis in five samples and with S. Livingstone in one. Where S. Enteritidis was detected with other Salmonella, the former was present at between 2 and 100-fold lower concentrations. The Salmonella contamination was homogeneously distributed amongst chicken pieces from a single pack and present in both the outer coating and inner content. The S. Enteritidis were all outbreak strains and detected in six products that were linked to four production plants which implicated a Polish origin of contamination. Despite S. Infantis being most prevalent in these products, S. Infantis from only two contemporaneous human cases in the UK fell into the same cluster as isolates detected in one product. Except for one human case falling into the same cluster as one of the S. Newport strains from the chicken, no further isolates from human cases fell into clusters with any of the other serovars detected in the chicken samples. This study found that higher E. coli levels indicated a higher probability of Salmonella contamination in FR chicken products. The results also highlight the importance of recognising co-contamination of foods with multiple Salmonella types and has provided essential information for detecting and understanding outbreaks where multiple strains are involved.

Keywords: Food safety; Frozen reformulated chicken; MPN; WGS.

MeSH terms

Animals
Chickens*
Disease Outbreaks
Escherichia coli* / genetics
Genotype
Salmonella enteritidis / genetics