From the EFSA report, "The outbreak strain was detected in France from a mixed salad dish, containing cherry tomatoes and green leafy vegetables, prepared on 17 August 2022 but not served. Tomatoes from the salad in France and tomatoes in Austria were suspected as the vehicle of infections by national authorities and were traced back to wholesalers in Germany, the Netherlands and Spain, and to growers in the Netherlands, Spain and Morocco. In the absence of microbiological evidence from the tomatoes, the source of the infections could not be established."
https://www.efsa.europa.eu/en/supporting/pub/en-8211
Multi-country outbreak of Salmonella Senftenberg ST14 infections possibly linked to cherry like tomatoes
Published: 27 July 2023
Adopted: 27 July 2023
https://www.efsa.europa.eu/en/supporting/pub/en-8211
Multi-country outbreak of Salmonella Senftenberg ST14 infections possibly linked to cherry like tomatoes
Published: 27 July 2023
Adopted: 27 July 2023
Abstract
Since August 2022 and as of 12 July 2023, 92 cases of Salmonella Senftenberg have been reported in Austria (5), Belgium (4), Czechia (4), Estonia (1), Finland (12), France (16), Germany (26), Ireland (1), the Netherlands (5), Norway (1), Sweden (11), the United Kingdom (4), and the United States (2). In total, 69.6% of the reported cases were female. One patient has died of the infection. The first case was reported in France with an isolation date of 22 August 2022 and the most recent case was reported on 24 June 2023 in Sweden. Most cases were reported between October 2022 and March 2023, with a decline in the number of countries with exposures after December. In Austria, Germany, and France, cherry-like tomatoes were identified as the food exposure most reported by interviewed cases. The outbreak strain was detected in France from a mixed salad dish, containing cherry tomatoes and green leafy vegetables, prepared on 17 August 2022 but not served. Tomatoes from the salad in France and tomatoes in Austria were suspected as the vehicle of infections by national authorities and were traced back to wholesalers in Germany, the Netherlands and Spain, and to growers in the Netherlands, Spain and Morocco. In the absence of microbiological evidence from the tomatoes, the source of the infections could not be established. The genetic similarity of the human outbreak strains suggests a likely common source(s) causing a prolonged, cross-border food-borne outbreak with cases intermittently reported in 11 EU/EEA countries, the UK, and the US for about 10 months. The contamination may have originated from farms growing tomatoes. Since December 2022, as the number of cases has declined, the risk of new infections has decreased to a low level.
Event background
On 12 February 2023, Germany reported 10 cases of Salmonella Senftenberg infection in the European Surveillance portal for Infectious Diseases (EpiPulse, 2023-FWD-00009) between calendar weeks 44/2022 and 2/2023. Several countries subsequently reported cases between August 2022 and early March 2023 belonging to the same genetically defined cluster. This pointed to a common source(s) of infection for human cases and triggered the initiation of a Notification Summary by the European Centre for Disease Prevention and Control (ECDC) on 16 March 2023. The Notification Summary, with a risk assessment, was distributed to the European Commission’s Directorate General for Health and Food Safety (DG SANTE) for posting in the Early Warning and Response System (EWRS) and to the food safety (Rapid Alert System for Food and Feed) and public health (European Food- and Waterborne Diseases and zoonoses network) networks on 30 March 2023.
New cases continued to be reported in March−April 2023 and on 26 April 2023, public health authorities in France (Santé publique France) were informed by the national food reference laboratory (Laboratoire National de Référence) that S. Senftenberg ST14 had been isolated from a mixed salad, which was prepared on 17 August 2022. This new microbiological evidence in food resulted in traceback investigations and, as new cases continued to be reported, ECDC and the European Food Safety Authority (EFSA) decided to upgrade the Notification Summary to a Joint Notification Summary, which was distributed to the Member States and EU-level risk managers on 26 May 2023. As further new cases have been reported, ECDC and EFSA decided to publish this multi-country food-borne outbreak as a Rapid Outbreak Assessment.
S. Senftenberg is a relatively uncommon serotype in human cases of salmonellosis; between 2007 and 2021, a total of 2 174 human cases of S. Senftenberg were reported, ranking the serotype 48th out of 1 210 serotypes reported to ECDC (Annex). During the period 2007−2021, the average annual number of cases was 145. In 2020 and 2021, 36 and 75 cases respectively were reported to ECDC.
Outbreak strain characterisation
The representative German outbreak strain is characterised as follows:
• Salmonella serotype Senftenberg, sequence type (ST) 14, SeqSphere complex type (CT) 17028.
• The EnteroBase core genome multilocus sequence typing (cgMLST) hierarchical cluster designation for the outbreak isolates is HC5_325504 [1,2].
• The genome of the representative German isolate is available in EnteroBase: 23-00207 (SAL_QB9631AA).
• Predicted antimicrobial resistance determinants (qnrB19) against ciprofloxacin were detected in the Austrian, French, German, Irish, Norwegian, and Swedish isolates. Phenotypic resistance to ciprofloxacin was also confirmed in the Austrian (MIC 0.38 µg/ml) and German (MIC 0.25 µg/ml) strains.
European outbreak case definition
The European outbreak case definition is as follows:
A confirmed outbreak case
• A laboratory-confirmed Salmonella Senftenberg ST14 case with disease onset on or after 1 June 2022 (date of sampling or date of receipt by the laboratory if date of onset is not available).
AND
• Fulfilling at least one of the following laboratory criteria:
− within five cg-allelic differences (AD) from at least one of the representative German outbreak strains in the national cgMLST pipeline, OR
− clustering within six cg-allelic differences in a single linkage analysis in a centralised whole genome
sequencing (WGS) analysis, OR
− belonging to the cgMLST HC5_325504 hierarchical cluster by EnteroBase scheme, OR
− clustering according to a national single-nucleotide polymorphism (SNP) pipeline within five SNPs of the German outbreak strain, OR
− belonging to a 5-SNP single linkage cluster with SNP designation 1.1.4.204.227.230.% according to the pipeline in the United Kingdom Health Security Agency (UKHSA) [3].
A possible outbreak case
• A laboratory-confirmed S. Senftenberg case with symptom onset on or after 1 June 2022 (date of sampling or date of receipt by the reference laboratory if date of onset was not available) without molecular typing data.
AND
• No or unknown history of travel outside of the EU/EEA seven days prior to onset of symptoms.
JOINT OUTBREAK ASSESSMENT Multi-country outbreak of S. Senftenberg ST14, possibly linked to cherry-like tomatoes – 27 July 2023
Epidemiological and microbiological investigations of human cases
As of 12 July 2023, 92 cases (81 confirmed and 11 possible) of S. Senftenberg have been reported in 11 EU/EEA countries, the United Kingdom (UK), and the United States (US) since August 2022 (Table 1, Figure 1). At least 12 cases were hospitalised in Germany (10), Ireland (1), and the UK (1). One patient in Germany has died of S. Senftenberg infection. Of 44 cases with information on sample material available, 15 cases (34.1%) had S. Senftenberg isolated from urine. Isolation from one case was via abdominal fluid.
The first cases were reported in France in August 2022 and the most recent case was reported in Sweden in June 2023 (Figure 1). When looking at the number of countries by month within an estimated exposure time range, based on the first and last case reported in the country, the time period during which there appears to have been wide exposure to a suspected vehicle across countries was October 2022 to March 2023. The geographical area of exposure in terms of number of countries peaked in December 2022 in the EU/EEA (Figure 1). There is a clear predominance of women with a female-to-male ratio of 2.3:1 (p < 0.001, chi-square). Table 1. Demographic and background information for 92 human S. Senftenberg cases in 11 EU/EEA countries, the UK and the US, as of 12 July 2023
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