Outbreak Vehicle Research Articles

Multinational collaboration in solving a European Salmonella Braenderup outbreak linked to imported melons, 2021.

A genomic cluster of Salmonella Braenderup ST22, a serovar of Salmonella enterica subsp. enterica which causes symptoms of gastrointestinal illness, was notified by Danish authorities to the European Centre for Disease Prevention and Control (ECDC) on 3 May 2021. By 6 July 2021, S. Braenderup outbreak cases (n=348) had been reported from 12 countries in the European Union/European Economic Area (EU/EEA) and the United Kingdom (UK), including 68 hospitalised cases. With support from affected EU/EEA countries, and in partnership with the European Food Safety Authority (EFSA), ECDC established an international outbreak investigation team to rapidly identify the source and prevent outbreak spread. Consumption information was shared with affected countries through a standard line list, revealing that 124 of 197 cases (63%) reported having eaten (any) melons within 7 days prior to disease onset. The speed and completeness of the investigation, which identified the outbreak vehicle as galia melons imported from Honduras in June 2021, was a direct result of extensive collaboration and information sharing between countries' national food safety and public health authorities. This article describes the outbreak and the benefits, successes, and challenges of multi-country collaboration for consideration in future large foodborne outbreaks across Europe.

Simulation and identification of foodborne outbreaks in a large supermarket consumer purchase dataset

Foodborne outbreaks represent a significant public health burden. Outbreak investigations are often challenging and time-consuming, and most outbreak vehicles remain unidentified. The development of alternative investigative strategies is therefore needed. Automated analysis of Consumer Purchase Data (CPD) gathered by retailers represents one such alternative strategy. CPD-aided investigations do not require trawling questionnaires to create a hypothesis and can provide analytical measures of association by direct data analysis. Here, we used anonymized CPD from 920,384 customers enrolled in Norway’s largest supermarket loyalty program to simulate foodborne outbreaks across a range of different parameters and scenarios. We then applied a logistic regression model to calculate an odds ratio for each of the different possible food vehicles. By this method, we were able to identify outbreak vehicles with a 90% accuracy within a median of 6 recorded case-patients. The outbreak vehicle identification rate declined significantly when using data from only one of two retailers involved in a simulated outbreak. Performance was also reduced in simulations that restricted analysis from product ID to the product group levels accessible by trawling questionnaires. Our results show that—assuming agreements are in place with major retailers—CPD collection and analysis can solve foodborne outbreaks originating from supermarkets both more rapidly and accurately than than questionnaire-based methods and might provide a significant enhancement to current outbreak investigation methods.

Bi-national outbreak of Salmonella Newport infections linked to onions: the United States experience.

From 2016-2019, dry bulb onions were the suspected cause of three multistate outbreaks in the United States. We investigated a large multistate outbreak of Salmonella Newport infections that caused illnesses in both the United States and Canada in 2020. Epidemiologic, laboratory and traceback investigations were conducted to determine the source of the infections, and data were shared among U.S. and Canadian public health officials. We identified 1127 U.S. illnesses from 48 states with illness onset dates ranging from 19 June to 11 September 2020. Sixty-six per cent of ill people reported consuming red onions in the week before illness onset. Thirty-five illness sub-clusters were identified during the investigation and seventy-four per cent of sub-clusters served red onions to customers during the exposure period. Traceback for the source of onions in illness sub-clusters identified a common onion grower in Bakersfield, CA as the source of red onions, and onions were recalled at this time. Although other strains of Salmonella Newport were identified in environmental samples collected at the Bakersfield, CA grower, extensive environmental and product testing did not yield the outbreak strain. This was the third largest U.S. foodborne Salmonella outbreak in the last 30 years. It is the first U.S. multistate outbreak with a confirmed link to dry bulb onions, and it was nearly 10-fold larger than prior outbreaks with a suspected link to onions. This outbreak is notable for its size and scope, as well as the international data sharing that led to implication of red onions as the primary cause of the outbreak. Although an environmental assessment at the grower identified several factors that likely contributed to the outbreak, no main reason was identified. The expedient identification of the outbreak vehicle and response of multiple public health agencies allowed for recall and removal of product from the marketplace, and rapid messaging to both the public and industry on actions to protect consumers; these features contributed to a decrease in cases and expeditious conclusion of the outbreak.

An Overview of Traceback Investigations and Three Case Studies of Recent Outbreaks of Escherichia coli O157:H7 Infections Linked to Romaine Lettuce

Leafy greens contaminated with Shiga toxin-producing Escherichia coli have continued to cause foodborne illness outbreaks in recent years and present a threat to public health. An important component of foodborne illness outbreak investigations is determining the source of the outbreak vehicle through traceback investigations. The U.S. Food and Drug Administration is home to traceback investigation experts who use a standardized process to initiate, execute, and interpret the results of traceback investigations in collaboration with the Centers for Disease Control and Prevention and state and local partners. Traceback investigations of three outbreaks of Shiga toxin-producing E. coli infections linked to romaine lettuce in 2018 and 2019 were examined to demonstrate challenges, limitations, and opportunities for improvement. The three outbreaks resulted in a total of 474 illnesses, 215 hospitalizations, and 5 deaths. These illnesses were linked to the consumption of romaine lettuce from three distinct growing regions in Arizona and California. Some of the challenges encountered included the time it took to initiate a traceback, limited product-identifying information throughout the supply chain, lack of interoperability in record-keeping systems, and comingling of product from multiple suppliers. These challenges led to time delays in the identification of the farm source of the leafy greens and the inability to identify the root cause of contamination. Implementation of technology-enabled traceability systems, testing of these systems, and future regulations to incentivize adoption of traceability systems are some of the initiatives that will help address these challenges by improving traceback investigations and ultimately preventing foodborne illnesses and future outbreaks from occurring.

Modeling Mobility Pattern for the Corona-Virus Epidemic Spread Propagation and Death Rate in Nigeria using the Movement-Interaction-Return Model

Modeling the propagation rate of diseases in a society via social interaction has continued to pose its many challenges. The recent spread of the covid-19 epidemic cannot be left out. Thus, social interactions heralds its many benefits and has becomes a vehicle for epidemic outbreaks –which has continually left the world puzzled as the disease itself has come to stay. The nature of its rapid propagation on exposure alongside its migration spread pattern of this contagion (with retrospect of other epidemics) on daily basis, has also left experts rethinking the set protocols. Our study models the spread propagation of the corona-virus contagion using the movement-interaction-return on a social graph. Thus, weseek to measure if the corona-virus (covid-19)spread propagation can be minimized alongside its death rate using movement pattern as a threshold feature and set of protocols. We design a Markovian block model to help minimize targeted propagation with the advent of seed-node(s) using the susceptible-infect structure on a time-varying graph. Study results showed that movement pattern must be employed as an imperative factors when modeling the propagation of contagion(s).

Food recalls associated with foodborne disease outbreaks, United States, 2006-2016.

About 800 foodborne disease outbreaks are reported in the United States annually. Few are associated with food recalls. We compared 226 outbreaks associated with food recalls with those not associated with recalls during 2006-2016. Recall-associated outbreaks had, on average, more illnesses per outbreak and higher proportions of hospitalisations and deaths than non-recall-associated outbreaks. The top confirmed aetiology for recall-associated outbreaks was Salmonella. Pasteurised and unpasteurised dairy products, beef and molluscs were the most frequently implicated foods. The most common pathogen-food pairs for outbreaks with recalls were Escherichia coli-beef and norovirus-molluscs; the top pairs for non-recall-associated outbreaks were scombrotoxin-fish and ciguatoxin-fish. For outbreaks with recalls, 48% of the recalls occurred after the outbreak, 27% during the outbreak, 3% before the outbreak, and 22% were inconclusive or had unknown recall timing. Fifty per cent of recall-associated outbreaks were multistate, compared with 2% of non-recall-associated outbreaks. The differences between recall-associated outbreaks and non-recall-associated outbreaks help define the types of outbreaks and food vehicles that are likely to have a recall. Improved outbreak vehicle identification and traceability of rarely recalled foods could lead to more recalls of these products, resulting in fewer illnesses and deaths.

A Simple Assay to Assess Salmonella enterica Persistence in Lettuce Leaves After Low Inoculation Dose.

Salmonella enterica is an enterobacterium associated with numerous foodborne illnesses worldwide. Leafy greens have been a common vehicle for disease outbreaks caused by S. enterica. This human pathogen can be introduced into crop fields and potentially contaminate fresh produce. Several studies have shown that S. enterica can survive for long periods in the plant tissues. Often, S. enterica population does not reach high titers in leaves; however, it is still relevant for food safety due to the low infective dose of the pathogen. Thus, laboratory procedures to study the survival of S. enterica in fresh vegetables should be adjusted accordingly. Here, we describe a protocol to assess the population dynamics of S. enterica serovar Typhimurium 14028s in the leaf apoplast of three cultivars of lettuce (Lactuca sativa L.). By comparing a range of inoculum concentrations, we showed that vacuum infiltration of a bacterium inoculum level in the range of 3.4 Log CFU ml–1 (with a recovery of approximately 170 cells per gram of fresh leaves 2 h post inoculation) allows for a robust assessment of bacterial persistence in three lettuce cultivars using serial dilution plating and qPCR methods. We anticipate that this method can be applied to other leaf–human pathogen combinations in an attempt to standardize the procedure for future efforts to screen for plant phenotypic variability, which is useful for breeding programs.

Large Nationwide Outbreak of Invasive Listeriosis Associated with Blood Sausage, Germany, 2018-2019.

Invasive listeriosis is a severe foodborne infection in humans and is difficult to control. Listeriosis incidence is increasing worldwide, but some countries have implemented molecular surveillance programs to improve recognition and management of listeriosis outbreaks. In Germany, routine whole-genome sequencing, core genome multilocus sequence typing, and single nucleotide polymorphism calling are used for subtyping of Listeria monocytogenes isolates from listeriosis cases and suspected foods. During 2018–2019, an unusually large cluster of L. monocytogenes isolates was identified, including 134 highly clonal, benzalkonium-resistant sequence type 6 isolates collected from 112 notified listeriosis cases. The outbreak was one of the largest reported in Europe during the past 25 years. Epidemiologic investigations identified blood sausage contaminated with L. monocytogenes highly related to clinical isolates; withdrawal of the product from the market ended the outbreak. We describe how epidemiologic investigations and complementary molecular typing of food isolates helped identify the outbreak vehicle.

Use of 254 nm ultraviolet light for decontamination of fresh produce and wash water

Fresh produce has been identified as the transmission vehicle for many foodborne illness outbreaks every year. They could be contaminated by pathogens at any point within the farm-to-fork food chain. Washing is often used to remove dirt and pathogens on fresh produce. Moreover, an effective decontamination method is required for wash water to prevent cross-contamination. Our group developed a water-assisted ultraviolet (UV) decontamination system (WUV) which combined washing and UV treatments. We evaluated the influence of turbidity (0–100 NTU) and chemical oxygen demand (COD; 0–2500 ppm) on UV inactivation of Salmonella in simulated wash water with different produce extracts. In the worst condition tested (turbidity of 100 NTU and COD of 2500 ppm), Salmonella in simulated wash water could be eliminated by UV (23–28 mW/cm2; wavelength peak at 254 nm) in 90 s (>6 log CFU/mL reduction), indicating the potential of UV for fresh produce wash water disinfection. Within the ranges tested, the effectiveness of UV inactivation of Salmonella was significantly decreased with increasing COD, but not with turbidity. In addition, ultraviolet lamps were installed in different locations (above and/or in the washing tank).Three WUV configurations showed similar Salmonella reduction on blueberries (1.8–2.0 log) and tomatoes (2.4–2.9 log). However, the Overhead and Dual WUV configurations reduced significantly (P < 0.05) more Salmonella on lettuce than the Submersible WUV configuration.

Cross-border outbreak of Yersinia enterocolitica O3 associated with imported fresh spinach, Sweden and Denmark, March 2019.

In April 2019, a cross-border outbreak of Yersinia entercolitica O3 was identified in Sweden and Denmark and confirmed using whole genome sequencing. Close cross-border collaboration with representatives from human and food authorities helped direct resources and investigations. Combined epidemiological and trace-back investigations pointed to imported fresh spinach as the outbreak vehicle and highlight that other vehicles of Y. enterocolitica outbreaks than pork should be considered.

Outbreak of Shiga toxin-producing Escherichia coli O157:H7 linked to raw drinking milk resolved by rapid application of advanced pathogen characterisation methods, England, August to October 2017.

An outbreak of Shiga toxin-producing Escherichia coli (STEC) O157:H7 occurred on the Isle of Wight between August and October 2017. Of the seven cases linked to the outbreak, five were identified through the statutory notification process and two were identified through national surveillance of whole genome sequencing data. Enhanced surveillance questionnaires established a common link to a farm, and link to the likely food vehicle, raw drinking milk (RDM). Microbiological investigations, including PCR, identified the presence of STEC O157:H7 in samples of RDM. Analysis of core genome single nucleotide polymorphism (SNP) data of STEC O157:H7 from human stool specimens, animal faecal samples and RDM demonstrated a one SNP difference between isolates, and therefore close genetic relatedness. Control measures that were put in place included suspension of sales and recall of RDM, as well as restrictions on public access to parts of the farm. Successful integration of traditional epidemiological surveillance and advanced laboratory methods for the detection and characterisation of STEC O157:H7 from human, animal and environmental samples enabled prompt identification of the outbreak vehicle and provided evidence to support the outbreak control team’s decision-making, leading to implementation of effective control measures in a timely manner.

New product, old problem(s): multistate outbreak of Salmonella Paratyphi B variant L(+) tartrate(+) infections linked to raw sprouted nut butters, October 2015

A cluster of Salmonella Paratyphi B variant L(+) tartrate(+) infections with indistinguishable pulsed-field gel electrophoresis patterns was detected in October 2015. Interviews initially identified nut butters, kale, kombucha, chia seeds and nutrition bars as common exposures. Epidemiologic, environmental and traceback investigations were conducted. Thirteen ill people infected with the outbreak strain were identified in 10 states with illness onset during 18 July-22 November 2015. Eight of 10 (80%) ill people reported eating Brand A raw sprouted nut butters. Brand A conducted a voluntary recall. Raw sprouted nut butters are a novel outbreak vehicle, though contaminated raw nuts, nut butters and sprouted seeds have all caused outbreaks previously. Firms producing raw sprouted products, including nut butters, should consider a kill step to reduce the risk of contamination. People at greater risk for foodborne illness may wish to consider avoiding raw products containing raw sprouted ingredients.

From purchase to consumption of bivalve molluscs: A qualitative study on consumers’ practices and risk perceptions

Worldwide bivalve production has increased significantly in recent years. Bivalve meat is recommended in dietary regimens due to the benefits associated with their consumption but, at the same time, is internationally recognized as a potential vehicle for outbreaks of foodborne disease. To reduce food risk exposure, consumers must pay close attention when purchasing, handling and consuming bivalves. This study aimed to collect information on consumers' perceptions and practices related to bivalve purchasing, managing and consumption at home. A focus group methodology was adopted to better understand consumers' food practices and risk perceptions regarding molluscs. Four focus groups involving 42 consumers were conducted in Veneto and Marche region. The core analysis was then applied to each focus group discussion in order to identify, categorize and rank the information collected. The most important factors that came to light during the focus groups concerned the personal reasons for preparing bivalves at home; the place of purchase; the elements guiding consumers when purchasing bivalves; the bivalve preparation, cooking and storage conditions at home; the consumption of raw molluscs and the health risks; the consumers’ categories most at risk; and the production chain control by the authorities. The data reported in the article can provide useful information to public authorities working on food safety for developing effective risk communication strategies.

Analysis of consumer food purchase data used for outbreak investigations, a review.

BackgroundInvestigations of food-borne outbreaks are frequently unsuccessful and new investigation methods should be welcomed. Aim: Describe the use of consumer purchase datasets in outbreak investigations and consider methodological and practical difficulties. Methods: We reviewed published papers describing the use of consumer purchase datasets, where electronic data on the foods that case-patients had purchased before onset of symptoms were obtained and analysed as part of outbreak investigations. Results: For the period 2006–17, scientific articles were found describing 20 outbreak investigations. Most outbreaks involved salmonella or Shiga toxin-producing Escherichia coli and were performed in eight different countries. The consumer purchase datasets were most frequently used to generate hypotheses about the outbreak vehicle where case-interviews had not been fruitful. Secondly, they were used to aid trace-back investigation, where a vehicle was already suspected. A number of methodological as well as (in some countries) legal and practical impediments exist. Conclusions: Several of the outbreaks were unlikely to have been solved without the use of consumer purchase datasets. The method is potentially powerful and with future improved access to big data purchase information, may become a widely applicable tool for outbreak investigations, enabling investigators to quickly find hypotheses and at the same time estimate odds ratios or relative risks hereof. We suggest using the term ‘consumer purchase data’ to refer to the approach in the future.

National outbreak of Shiga toxin-producing Escherichia coli O157:H7 linked to mixed salad leaves, United Kingdom, 2016.

We investigated a large outbreak of Escherichia coli O157 in the United Kingdom (UK) with 165 cases between 31 May and 29 July 2016. No linked cases were reported in other countries. Cases were predominately female (n = 128) and adult (n = 150), 66 attended hospital and nine had features of haemorrhagic uraemic syndrome. A series of epidemiological studies (case–control, case–case, ingredients-based and venue-based studies) and supply chain investigations implicated mixed salad leaves from Supplier A as the likely outbreak vehicle. Whole genome sequencing (WGS) indicated a link with strains from the Mediterranean and informed the outbreak control team to request that Supplier A cease distributing salad leaves imported from Italy. Microbiological tests of samples of salad leaves from Supplier A were negative. We were unable to confirm the source of contamination or the contaminated constituent leaf although our evidence pointed to red batavia received from Italy as the most likely vehicle. Variations in Shiga toxin-producing E. coli surveillance and diagnosis may have prevented detection of cases outside the UK and highlights a need for greater standardisation. WGS was useful in targeting investigations, but greater coverage across Europe is needed to maximise its potential.

Multistate Outbreak of Salmonella Virchow Infections Linked to a Powdered Meal Replacement Product-United States, 2015-2016.

Nontyphoidal Salmonella is the leading cause of bacterial gastroenteritis in the United States. Meal replacement products containing raw and "superfood" ingredients have gained increasing popularity among consumers in recent years. In January 2016, we investigated a multistate outbreak of infections with a novel strain of Salmonella Virchow. Cases were defined using molecular subtyping procedures. Commonly reported exposures were compared with responses from healthy people interviewed in the 2006-2007 FoodNet Population Survey. Firm inspections and product traceback and testing were performed. Thirty-five cases from 24 states were identified; 6 hospitalizations and no deaths were reported. Thirty-one of 33 (94%) ill people interviewed reported consuming a powdered supplement in the week before illness; of these, 30 (97%) reported consuming product A, a raw organic powdered shake product consumed as a meal replacement. Laboratory testing isolated the outbreak strain of Salmonella Virchow from leftover product A collected from ill people's homes, organic moringa leaf powder (an ingredient in product A), and finished product retained by the firm. Firm inspections at 3 facilities linked to product A production did not reveal contamination at the facilities. Traceback investigation identified that the contaminated moringa leaf powder was imported from South Africa. This investigation identified a novel outbreak vehicle and highlighted the potential risk with similar products not intended to be cooked by consumers before consuming. The company issued a voluntary recall of all implicated products. As this product has a long shelf life, the recall likely prevented additional illnesses.

Incubation period for outbreak-associated, non-typhoidal salmonellosis cases, Minnesota, 2000-2015.

Incubation period for non-typhoidal Salmonella (NTS) infections is generally reported as 6-72 h despite numerous reports of foodborne NTS outbreaks with median incubation periods >3 days. We summarised 16 years of Minnesota foodborne NTS outbreaks to better estimate the expected range of incubation periods for NTS infections. Of the 1517 NTS outbreak cases, 725 had enough data to calculate a precise incubation period. The median incubation period was 45 h; 77 (11%) cases had incubations ⩽12 h and 211 (29%) cases had incubations >72 h. Incubation period length varied by outbreak vehicle type, Salmonella serotype and outbreak setting. Based on our data, a more accurate description would be that the incubation of NTS infection is usually from 12 to 96 h, that incubations in >96 to 144 h (>4 to 6-day) range are not unusual and that incubations from 7 to 9 days and occasionally longer also occur.

Geospatial Mapping of Early Cases in Multistate Foodborne Disease Outbreaks: A Strategy To Expedite Identification of Contaminated Imported Produce, United States, 2006 to 2013

From 1998 to 2008, produce-related illness outbreaks accounted for roughly one-half of reported foodborne outbreaks in the United States. In 2013, Mexico accounted for approximately 50 and 30% of the monetary value of all vegetables and fruits, respectively, imported into the United States. We used historical import data to examine the correlation between the port of entry for five implicated produce vehicles from five multistate outbreaks and the geospatial and temporal distribution of illnesses in the corresponding outbreaks in the United States. For comparison, we analyzed the geospatial and temporal distribution of cases from two U.S. multistate outbreaks associated with domestically grown produce. The geospatial distribution of illnesses in the two outbreaks linked to domestic produce differed from that of the import-related produce outbreaks. The results of our pilot study suggest that geospatial distribution of early-onset cases may be used to identify ports of entry for produce likely to be responsible for causing multistate outbreaks in the United States and that targeted sampling of produce items from these ports of entry may expedite identification of an outbreak vehicle.

International outbreak of multiple Salmonella serotype infections linked to sprouted chia seed powder - USA and Canada, 2013-2014.

Salmonella is a leading cause of bacterial foodborne illness. We report the collaborative investigative efforts of US and Canadian public health officials during the 2013-2014 international outbreak of multiple Salmonella serotype infections linked to sprouted chia seed powder. The investigation included open-ended interviews of ill persons, traceback, product testing, facility inspections, and trace forward. Ninety-four persons infected with outbreak strains from 16 states and four provinces were identified; 21% were hospitalized and none died. Fifty-four (96%) of 56 persons who consumed chia seed powder, reported 13 different brands that traced back to a single Canadian firm, distributed by four US and eight Canadian companies. Laboratory testing yielded outbreak strains from leftover and intact product. Contaminated product was recalled. Although chia seed powder is a novel outbreak vehicle, sprouted seeds are recognized as an important cause of foodborne illness; firms should follow available guidance to reduce the risk of bacterial contamination during sprouting.

Non-heat-treated frozen raspberries the most likely vehicle of a norovirus outbreak in Oslo, Norway, November 2013.

In November 2013, the Norwegian Institute of Public Health was notified of a gastroenteritis outbreak following two meetings held at a conference centre. Identical food and beverages were served during the meetings. We investigated in order to identify the vehicle of infection and implement control measures. Meeting participants completed an online questionnaire on consumption of foods and beverages. We asked symptomatic participants to provide a stool sample. We defined a case as diarrhoea and/or vomiting in a participant who became ill within 3 days after the meeting. We calculated attack rates (AR) and adjusted risk ratios (aRR) with 95% confidence intervals (CI) using binomial regression. We conducted environmental investigations. Overall, 147/168 (88%) participants responded, of which 74 (50%) met the case definition. All five stool samples provided were norovirus positive. No kitchen staff reported being sick. Risk of illness was higher in those who consumed raspberry mousse (aRR 3·4, 95% CI 1·4-8·2) and sliced fresh fruit (aRR 1·9, 95% CI 1·3-2·8). Seventy cases (95%) ate raspberry mousse. Frozen raspberries used for the mousse were imported and not heat-treated before consumption. Non-heat-treated frozen raspberries were the most likely outbreak vehicle. Contamination by a food handler could not be excluded. We recommend heat-treatment of imported frozen berries before consumption.