Smoked fish and risk of listeriosis in high risk groups, including pregnancy and the immunocompromised
Updated 27 July 2023
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Executive summary
The UK Health Security Agency (UKHSA) has reviewed available evidence that consumption of smoked fish is an ongoing high risk for specific groups of people who are clinically vulnerable to invasive listeriosis, for example, those who are of an advanced age, pregnant or immunocompromised.
Food types that are higher risk for listeriosis can be identified through trends in cluster and outbreak investigations, testing of food products and published scientific studies in the world literature.
A review of the evidence by UKHSA suggests there is an ongoing risk of smoked fish causing listeriosis in the UK, and that the risk of L. monocytogenes transmission in England due to consumption of smoked fish has been increasingly recognised since 2015, which coincides with the introduction of whole genome sequencing (WGS) for typing of Listeria spp.
Smoked fish consumption has consistently been linked to outbreaks since 2015 with an increasing trend of associated cases since 2020 to date, compared to between 2015 and 2019. In addition, findings from UKHSA’s Food Water and Environmental Microbiology (FWEM) laboratories have demonstrated a significant increase in the odds of identification of L. monocytogenes in sampled smoked salmon products. This is within the wider context of multiple international outbreaks associated with smoked fish in recent years and a widespread recognition of smoked fish as a high risk product for Listeria contamination.
Introduction
Listeriosis is a predominately foodborne disease caused by the bacterium Listeria monocytogenes. Infection usually occurs after consumption of contaminated ready-to-eat foods (1). Overall it is a rare infection. There are an average of 160 cases per year in England and Wales. The majority of cases are asymptomatic or have mild self-limiting gastroenteritis (2).
Invasive listeriosis, however, although rare, has a case fatality rate of 20% to 30% and primarily occurs in the elderly, immunocompromised and those with underlying systemic illness (3, 4). People who are pregnant are also particularly susceptible, and infection during pregnancy can cause miscarriages, still-births, or severe sepsis and meningitis in neonates (5). Listeriosis is a relatively rare foodborne pathogen; however, it is an important public health concern due to the severity of illness in vulnerable patients and it is the most common cause of death in the EU from foodborne illness (6, 7).
Listeriosis cases are often sporadic; however, larger outbreaks do occur. Food production environments can be colonised with specific L. monocytogenes strains for long periods of time (years to decades) and, because of complex and far reaching distribution chains, cases related by common food exposures can be temporally and geographically very widely distributed (8, 9).
Due to a long incubation period (up to 70 days), the difficulties with lengthened food history recall periods and the wide variety of foods that can be contaminated with L. monocytogenes, a causative food can currently only be robustly attributed to approximately 10% of cases reported in England (10).
Introduction of WGS in 2015 significantly facilitated the investigation of incidents of foodborne disease, allowing a more sensitive and accurate method of matching of isolates from cases with food isolates, and increased detection of clusters of cases and national and international outbreaks (11). We have now applied this method of investigation to understand more clearly the current risk patterns.
UK data from outbreaks and incidents
All cases of listeriosis reported in the UK are requested to complete a food history questionnaire, asking about food exposures in the 30 days prior to illness onset (13). This questionnaire includes questions around smoked fish consumption and location of purchase. Where WGS of L. monocytogenes from multiple cases shows them to be matched, food exposures can be compared to identify similarities between cases, which allows potential vehicles of interest to be further investigated and the source of the outbreak to be identified.
However, the most common way to initially identify likely food sources is by the unrelated examination of foods as part of local authority routine food inspections and the matching by WGS analysis of food or environmental L. monocytogenes to those from cases of human listeriosis, sometimes several years apart. Where there is a match to a non-human isolate, food exposure information and traceback can identify a likely source of contamination, even in instances where there is only one case.
As of 30 June 2023, data from UKHSA investigations into outbreaks (and into single cases matching food isolates identified by WGS) have identified a total of 8 incidents linked to smoked fish between 2015 and June 2023 through microbiological evidence. Seven of these incidents were also linked to smoked fish epidemiologically through enhanced surveillance questionnaires (Table 1).
From 2015 to June 2023, there were a total of 31 cases linked to the 8 smoked fish incidents; with 8 deaths and 3 pregnancy-associated cases identified. Twenty-one of the 31 (68%) cases reported consumption of smoked fish. Incidents and cases of L. monocytogenes have continually been linked to smoked fish since 2015, resulting in a number of deaths and pregnancy-associated cases.
Table 1. Summary of incidents and cases from 2015 to 2023 with microbiological evidence implicating smoked fish as the vehicle of infection
| Incident | Total cases with microbiological links to smoked fish | Time period | Deaths | Pregnancy-associated cases | Cases with microbiological and epidemiological links to smoked fish |
|---|---|---|---|---|---|
| 1 | 2 | 2016 to 2021 | 0 | 1 | 1 |
| 2 | 1 | 2017 | 1 | 0 | 1 |
| 3 | 2 | 2017 to 2019 | 1 | 0 | 0 |
| 4 | 1 | 2018 | 0 | 0 | 1 |
| 5 | 4 | 2020 | 2 | 1 | 1 |
| 6 | 19 | 2020 to 2023 | 4 | 1 | 16 |
| 7 | 1 | 2021 | 0 | 0 | 1 |
| 8 | 1 | 2021 | 0 | 0 | 1 |
Review of cases with genetically matching food isolates
All human samples of L. monocytogenes identified between 2014 and June 2023 with microbiological linkage to matching food isolates by WGS, at the 5 single nucleotide polymorphism (SNP) level, were analysed. Smoked fish was the second most common food category (after ready-to-eat sandwiches and salads) associated with human cases of L. monocytogenes. The proportion of cases linked with smoked fish increased with advancing age (Table 2).
Table 2. Age distribution of cases microbiologically linked to smoked fish compared to all human cases microbiologically linked to food isolates
| Age group (years) | All human cases linked to food isolates (n = 156) | Human cases linked to smoked fish (n = 31) |
|---|---|---|
| < 18 | 7 (4.5%) | 2 (6.5%) |
| 18 to 49 | 22 (14.1%) | 4 (12.9%) |
| 50 to 64 | 27 (17.3%) | 3 (9.7%) |
| 65 to 74 | 36 (23.1%) | 4 (12.9%) |
| 75+ | 64 (41.0%) | 18 (58.1%) |
UKHSA’s Food, Water and Environmental microbiological testing data
L. monocytogenes is widely distributed in the environment. It can grow at low temperatures including in refrigerators, survive freezing and is salt tolerant, and can persist in food manufacturing environments for years (12).
Regulation (EC) 2073/2005 states that ready-to-eat foods able to support the growth of L. monocytogenes placed on the market must not exceed the limit of 100 colony forming units (CFUs) of L. monocytogenes per gram (g) in 5 samples during their shelf life, or where the producing food business operator (FBO) cannot demonstrate this to the competent authority, that L. monocytogenes must not be detected in five 25 gram samples before they have left the immediate control of the producing FBO (14, 15). Several studies and outbreaks have shown that this permissible limit of 100 CFUs/g does not prevent invasive listeriosis in high risk groups (16, 17, 18, 19).
The FAO and WHO have been undertaking risk assessment on L. monocytogenes in ready-to-eat foods since 1999 and their technical reports have recognised cold smoked fish as a high risk vehicle for human listeriosis (18, 19). The Food Standards Agency has listed smoked fish as a food associated with listeriosis outbreaks and a risk to vulnerable groups (20).
Results from sampling of smoked fish by UKHSA’s FWEM laboratories, given below, show a small but increasing trend in terms of the proportion of samples taken where L. monocytogenes was detected (Table 3). There is a continual detection of L. monocytogenes among smoked salmon tested between 2013 and 2022. Smoked salmon products tested by FWEM may not be representative of all smoked salmon products on the market; however, samples microbiologically linked to incidents of human listeriosis have been removed from the analysis to improve representativeness.
Table 3. Detection rate of L. monocytogenes by UKHSA FWEM laboratories, 2013 to 2021 in smoked salmon products
| Year | Number of samples tested* | Number of samples* where where L. monocytogenes was detected in 25 gram of sample (% of samples) | Number of samples with more than 100 CFU of L. monocytogenes per gram |
|---|---|---|---|
| 2013 | 118 | 2 (1.7%) | 0 |
| 2014 | 105 | 8 (7.6%) | 0 |
| 2015 | 173 | 8 (4.6%) | 0 |
| 2016 | 130 | 18 (13.8%) | 0 |
| 2017 | 107 | 5 (4.6%) | 0 |
| 2018 | 77 | 5 (6.4%) | 0 |
| 2019 | 105 | 14 (13.3%) | 3 |
| 2020 | 14 | 0 | – |
| 2021 | 43 | 2 (4.7%) | 0 |
* Results from samples collected from premises investigated in relation to the 5-SNP clusters associated with human cases of listeriosis were excluded.
In addition, a survey led by UKHSA FWEM testing smoked fish products collected at retail shops was conducted from November 2022 to March 2023. Of the 786 smoked fish samples tested during this survey, L. monocytogenes was detected in 28 samples (3.6%). Three of the L. monocytogenes isolates were the strain in the CC217 outbreak (cases from 2020 to 2023).
Scientific literature
Contamination of smoked fish products with L. monocytogenes
Vacuum-packed smoked fish and gravad fish (fish cured in salt and sugar without thermal treatment) have been identified as the ready-to-eat foods that are most frequently contaminated with L. monocytogenes (21).
An EU-wide baseline survey was carried out in 2010 to 2011; this established a prevalence of L. monocytogenes of 10.3% in samples taken at end of shelf life from smoked or gravad fish products (22). In comparison, in the same survey, L. monocytogenes was detected in 2.1% of packaged heat-treated meat product samples and 0.5% of soft or semi-soft cheese samples tested, and the proportion of samples containing over 100 colony forming units per gram (CFUs/g) (the legal food safety limit [Commission Regulation (EC) 2073/2005]) of the bacteria at the end of shelf life was highest for smoked fish or gravad fish (1.7%), followed by packaged heat-treated meat product samples (0.43%) and soft or semi-soft cheese samples (0.06%) (22).
Smoked fish is considered a high risk product for L. monocytogenes. Contamination of smoked fish products with L. monocytogenes can result from the presence of the bacteria in the raw fish itself or from the production environment, such as contaminated equipment, utensils, and brine, with persistence of the bacteria throughout processing (23, 24 , 25). The bacterium has been demonstrated to survive and multiply in smoked salmon at refrigerator temperatures below 5°C (24, 26). The long shelf-life and extended storage period of up to 3 weeks in the refrigerator provides opportunity for the bacterium to multiply, and no further bactericidal treatment of the fish occurs prior to consumption (23). Additionally, L. monocytogenes can grow without oxygen and therefore can multiply in vacuum-packaging (21).
Outbreaks of listeriosis in Europe associated with smoked fish
Smoked fish products have frequently been linked to outbreaks of listeriosis in humans, including a number of multi-country outbreaks outside the UK.
From 2015 to 2017, a multi-country outbreak of listeriosis was identified, consisting of 7 cases from Denmark and France (27). Five of the cases reported consumption of smoked or cured salmon and multiple smoked salmon samples from one factory genetically matched the outbreak strain, leading to the recall of the product.
From 2013 to 2015, 2 separate outbreaks of listeriosis, each consisting of 10 cases, affected Denmark and France (28). The first cluster of cases matched environmental isolates from a smoked salmon factory that had previously recalled products due to L. monocytogenes contamination; the second cluster matched food isolates from smoked halibut, smoked trout, and graved salmon.
In Finland, in 2010, an increase in listeriosis incidence was observed, which was thought to be at least partly caused by persistent L. monocytogenes contamination of 2 fishery production plants; 57% of cases reported from this time period reported eating smoked fish or gravad fish (29). In Sweden, an outbreak of 27 cases of listeriosis from 2013 to 2015 was associated with smoked fish and gravad fish products from one manufacturer (21).
A case control study in England and Wales identified cases occurring between 2005 and 2008 were significantly more likely to have consumed smoked salmon than the general population (30). Between 2020 and 2021, a large multinational L. monocytogenes outbreak of 55 cases was identified in Germany, Austria, Denmark and Switzerland. The cluster was epidemiologically and microbiologically linked through WGS to food isolates from smoked rainbow trout (31). In Germany alone, 22 outbreaks of L. monocytogenes identified between 2010 and 2021 were most likely associated with smoked and graved salmon consumption through WGS and epidemiological investigations (32).
Food consumption advice in other countries
Other European countries, as well as other countries with strong listeriosis surveillance systems, provide advice on foods to avoid for vulnerable groups and people who are pregnant. Australia, Canada, Denmark, France, Germany, Sweden and USA are included as countries where public health authorities provide advice against the consumption of smoked fish (33, 34, 35).
Conclusion
Recent evidence collated by UKHSA indicates that the risk of L. monocytogenes transmission in England due to consumption of smoked fish has been increasingly recognised since 2015, which coincides with the introduction of WGS.
A review of the evidence suggests that smoked fish is a high risk product for invasive listeriosis in the UK in vulnerable groups, although the overall risk to the population remains low.
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