In February 2022, a small five-single nucleotide polymorphism (SNP) single linkage cluster of eight cases of infection with monophasic Salmonella enterica subsp. enterica serotype Typhimurium (1,4,5,12:i:-) eBG 1, sequence type (ST) 34 was identified in the United Kingdom (UK). The cluster was unusual, with all but one reported case younger than 10 years, and the strain demonstrated genotypic markers of an unusual antimicrobial resistance pattern not commonly seen in livestock, food or human disease cases in the UK. The cluster was not closely related to any other UK strains of monophasic S. Typhimurium.
Exploratory interviews using an open-ended, anthropological approach (not binary yes/no questions) were undertaken with the parents/guardians of five cases in England for hypothesis generation. Subsequently, a targeted questionnaire to refine hypotheses identified through the exploratory interviews was used, confirming a strong signal for a specific brand of chocolate products.
Following the UK’s notification on the European Centre for Disease Prevention and Control (ECDC) EpiPulse Food and Waterborne Diseases (FWD) platform on 17 February 2022, and an Early Warning and Response System (EWRS) alert on 25 March, Germany, Sweden, France, the Netherlands and subsequently Luxembourg, Norway, Ireland, Belgium and Spain reported confirmed or probable cases in their respective countries.
Multi-country collaboration through teleconferences and sharing of information between public health agencies and reference laboratories indicated that cases in affected countries commonly reported consumption of a specific brand of chocolate products. Overall, of 101 case interviews carried out across the 10 affected countries, 88 cases (87%) confirmed consumption of these products. The most commonly consumed product was Product A, marketed primarily for children in the age group 3–10 years, but multiple other product types were also reported.
Food chain investigations in the affected countries indicated that the majority of the products implicated in the epidemiological investigations were produced predominantly at a single production site in Belgium. This was the same facility from which the outbreak strain had been identified in December 2021 in the processing equipment.
Based on the strong descriptive epidemiological evidence implicating these products in this outbreak, on the identified food chain links and on evidence of contamination previously identified at production, risk management actions were taken in all affected countries, including withdrawal of all product lines produced in the implicated production facility and extensive product recalls, supported by news alerts and advice for consumers, starting with the first recall on 2 April in the UK and Ireland and extended to other countries shortly after. Extended recalls were carried out from 7 April as the investigations in a number of countries progressed, resulting in further evidence to support these recalls. On 8 April 2022, Belgian authorities stopped production at the facility in Belgium and, following the European Rapid Alert System Food and Feed (RASFF) alert notifications (RASFF 2022.1799), the World Health Organization/Food and Agriculture Organization International Food Safety Authorities Network (INFOSAN) also issued a global alert on 10 April notifying 77 countries and territories to which distribution of the implicated products had been established to initiate a global recall (see the Supplement for a non-exhaustive list of country-specific recall notices).
As at 10 April 2022, investigations are still ongoing to define specific national supply chains for the implicated products and common sourcing of raw ingredients. Root cause analysis for the outbreak is also ongoing to determine whether the outbreak was caused by a contaminated ingredient or another (potentially multi-strain) source of contamination.
Historically, chocolate-associated outbreaks have been protracted and usually of large scale, probably reflecting both the long shelf life of chocolate and the long survival of Salmonella in these products, as well as difficulties in detecting and resolving such outbreaks [7–9]. Previous investigations have resulted in recovery of only small amounts of Salmonella bacteria from sampling of chocolate products, suggesting that contamination in chocolate may be difficult to detect in product sampling, as well as difficult to mitigate through routine food hygiene procedures [7]. It has been suggested that the high fat content of chocolate may have a protective effect for the bacteria [10,11], including against gastric acid, and possibly altering the functional infective dose of Salmonella, resulting in clinically severe disease from exposure to only very low levels of contamination [12,13].
By 10 April, this outbreak involved at least 150 reported cases in nine EU/EEA countries and the UK. Owing to known under-reporting of Salmonella surveillance systems and the varying sensitivities of microbiological techniques used across countries, the scale of the outbreak is certainly underestimated, especially considering that very high volumes of the implicated chocolate products are consumed in the EU/EEA and the UK. However, while the period between initial detection of the outbreak in the UK and subsequent control measures taken at the international level spanned a duration of more than 2 months, once definitive epidemiological links with the implicated product were made, control actions followed rapidly. Indeed, compared with previous outbreaks of salmonellosis associated with chocolate products, the duration of this investigation was relatively short [7,14–16].
The field of infectious disease epidemiology for Salmonella has been considerably impacted by the adoption of next generation sequencing technologies combined with novel epidemiological approaches such as iterative open-ended interviewing [17]. The increasing use of WGS enables us to detect and resolve outbreaks more quickly, especially where common serovars such as S. Typhimurium are involved, allowing consolidation of evidence implicating specific food vehicles of infection at the international level [18–20].
Another notable aspect of this outbreak was the multidrug resistance profile of the outbreak strain and specifically resistance to kanamycin and gentamicin, and the presence of lnu(F), a determinant of resistance to lincosamides, which are relatively rare for monophasic S. Typhimurium in Europe. While not of especial clinical significance as the outbreak strain is susceptible to fluoroquinolones, azithromycin and third-generation cephalosporins which provide effective treatment options for cases of bloodstream infection, the unusual AMR profile constituted an additional characteristic of the outbreak strain to be assessed by all countries in the early stages of investigation for case ascertainment and possible hypothesis generation. This emphasises the usefulness of including more uncommon AMR profiles in early international communications and subsequent incorporation as part of the international outbreak case definitions, where this facilitates identification of possible or probable cases before the application of WGS and/or epidemiological investigations to confirm outbreak cases.
Early notification of the detection of the outbreak and preliminary findings of the UK investigation followed by rapid multi-country collaboration in information sharing, coordinated and supported by ECDC, was essential to the rapid progress of the outbreak investigations. The descriptive epidemiological information provided strong evidence implicating the vehicle of infection in this outbreak, especially when amalgamated at an international level, sufficient to enable public health and food safety authorities to undertake the rapid, necessary controls. The subsequent information about the detection of the outbreak strain in the implicated processing facility, provided further microbiological confirmation of the link between the company’s products and the Europe-wide outbreak. This demonstrated the utility of and highlighted the need for rapid sharing of microbiological sequence information, derived not just from human disease cases as occurred during this outbreak investigation, but also from, food, animal and environmental sampling.
The control measures taken across all affected countries probably constitute one of the largest chocolate product withdrawals and recalls in European commercial history.
The authors would like to thank the study group for their work on the multi-country outbreak investigations and their contributions to this manuscript. The study group were involved in collation and analysis of the data presented at the national level. The members of the study group were: Anais Painset, John Cowden, Robert Smith, Paul Cabrey, Sarah Gee, Martin Cormican, Inne Nauwelaers, Thijs Bosch, Eelco Franz, Ondřej Daniel, Andrea Mancikova.
We would also like to thank ECDC for their ongoing support in coordinating and supporting the international investigations, with especial thanks to Johanna Takkinen.
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