PRO/AH/EDR> E. coli EHEC - Canada (02): (BC) O103, pazienti ospedalizzati, sedano tritato, 2021

E. COLI EHEC - CANADA (02): (BRITISH COLUMBIA) O103, HOSPITALIZED PATIENTS, MINCED CELERY, 2021

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Date: Mon 31 Jan 2022
Source: Canada Communicable Disease Report (CDDR) [edited]
https://www.canada.ca/en/public-health/services/reports-publications/canada-communicable-disease-report-ccdr/monthly-issue/2022-48/issue-1-january-2022/outbreak-escherichia-coli-0103-hospitalized-people-british-columbia.html

Citation
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Smith C, Griffiths A, Allison S, Hoyano D and Hoang L: _Escherichia coli_ O103 outbreak associated with minced celery among hospitalized individuals in Victoria, British Columbia, 2021 CCDR 2022; 48-1: 46-50, doi.org/10.14745/ccdr.v48i01a07

Introduction
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Foodborne illness caused by _Escherichia coli_ (_E. coli_) often occurs through the consumption of contaminated food items such as fresh produce, meat and cheese products, and may result in symptoms including watery diarrhea, hemorrhagic colitis and hemolytic uremic syndrome (1,2). Pathogenic Shiga toxin-producing _E. coli_ (STEC or enterohemorrhagic _E. coli_ EHEC)) are among the top 10 most common causes of foodborne illness in Canada (3). Although _E. coli_ O157 remains the more common EHEC, incidence rates of non-O157 EHEC infections, including _E. coli_ O103, have increased over time. The main factor contributing to this increase is an advancement in diagnostic testing (4).

_E. coli_ O103 outbreaks have previously been linked to clover sprouts, bison meat, ground beef, cured mutton sausages, raw cow milk and fermented sausages (5-8). Although celery has been reported as a vehicle for _Listeria monocytogenes_, norovirus and _E. coli_ O157:H7 (9-11), there have been no outbreaks of non-O157 _E. coli_ associated with celery reported in the literature to date.

In April 2021 a Shiga toxin-producing _E. coli_ O103 outbreak was identified among inpatients and outpatients at 2 hospitals in Victoria, British Columbia (BC), after an unusual increase in E. coli activity triggered an investigation by local public health officials. The objective of this article is to describe the first outbreak of non-O157 E. coli associated with celery in Canada and to identify issues of food safety for high-risk products prepared for vulnerable populations, in order to reduce the likelihood of these outbreaks in the future.

Outbreak
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An unusual increase in _E. coli_ O103 cases was detected in April 2021 in the Victoria area, which triggered an investigation to identify the source of the illness. The outbreak investigation took place between [16 Apr 2021], and [10 May 2021]. A confirmed case was defined as a resident of or visitor to the Island Health region with laboratory confirmation of _E. coli_ O103 and symptom onset or collection date on or after [15 Mar 2021]. Cases were interviewed by a single interviewer with BC's routine _E. coli_ questionnaire. The interviews collected information on travel, animal exposures and select high-risk foods associated with previous _E. coli_ outbreaks, including beef, leafy greens and unpasteurized dairy. Exposure information was collected for the 10-day period prior to the episode date (earliest of symptom onset or specimen collection date), reflecting the incubation period of _E. coli_. For those admitted to hospital during their incubation period, hospital menus were also reviewed for the 10-day period prior to their episode date.

Local investigators inspected the kitchen of Hospital A, where the majority of cases were inpatients or outpatients. The inspectors examined cooler temperatures and logs, dishwasher temperatures, sanitizing processes, dating of product and food handling practices for any deficiencies or potential for cross contamination. Inspectors also inquired about ill food handlers. Records were reviewed to determine the suppliers of various products. Local and federal investigators inspected the processing facility of the suspect source of the outbreak--Processor A. Inspectors collected supply records and investigated processes to determine potential sources of contamination and potential deficiencies in food safety. The outbreak was declared over when the maximum incubation period (10 days) plus 90th percentile reporting delay had passed since the most recent episode date of a confirmed case.

Results
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A total of 6 confirmed cases were identified throughout the course of the investigation. Episode dates ranged from [20 Mar 2021] to [9 Apr 2021] (Figure 1 - for figures, see original URL - Mod.LL). The majority of cases were female (n=4/6; 67%) and the median age was 61 years (age range 24-87 years). One death was reported (n=1/6; 17%), although _E. coli_ infection was not the cause of death. All cases had been admitted to, or visited, 2 Victoria-area hospitals during their exposure period. Of the 6 confirmed cases, 4 were admitted to Hospital A, 1 was admitted to Hospital B, and 1 case was not admitted to hospital, but visited the emergency room of Hospital A during the exposure period (Figure 2). For those cases with onset dates available, the median reporting delay was 19 days (range 18-23 days).

All confirmed cases from both Hospital A and Hospital B were considered highly related to each other by wgMLST within 0 to 4 allele differences (Figure 3), and distinct from historic cases of _E. coli_ O103. There were no related cases identified within the same timeframe of this outbreak nationally, or within the USA.

A total of 3 cases were interviewed, while the remaining 3 could not be interviewed as they were either deceased (n=1) or medically impaired (n=2). From the interview data, the only exposures reported by at least 2 of 3 confirmed cases were ground beef (n=2/3), cheese (n=3/3), cold cuts (n=2/3), lettuce (n=2/3) and tuna sandwiches (n=3/3). No commonalities in restaurants or grocery stores were identified. The case that visited the emergency room of Hospital A reported eating only a tuna sandwich during their visit, given to them by a healthcare worker. The tuna sandwich was prepared by Hospital A food services and came from the same source as the inpatient food.

Hospital menus were reviewed for the 5 cases that were admitted to hospital. All 5 cases had exposure to prepared sandwiches during their hospital stay including tuna (n=4/5), egg (n=2/5), chicken salad (n=4/5), turkey (n=1/5) and roast beef (n=4/5) sandwiches. The only common ingredient across all sandwiches was minced celery, and minced celery within sandwiches was the only exposure reported by n=6/6 cases. Inspection of the kitchen of Hospital A, where the majority of cases were exposed to minced celery as either inpatients or outpatients, revealed no food safety or cross-contamination concerns. There were no reported illnesses among food handling staff. The inspection did reveal concerns regarding temperature abuse, with sandwiches often left out of the fridge for extended periods on trays or in patient rooms before being consumed.

Trace back investigation revealed that the minced celery used in sandwiches at both Hospital A and Hospital B was purchased from the same batch from the same local supplier--Processor A, and sourced from the Guadalupe region of California. Trace forward investigation revealed that this minced celery product was exclusively supplied to Hospital A and Hospital B, and no other facilities, distributors or stores. Chopped celery from the same batch of product was supplied to a large distribution network exclusive of Hospital A and Hospital B. Inspection of Processor A revealed 2 concerns. First, pathogen testing was infrequent, with the previous _E. coli_ test occurring in [January 2020]; over a year prior to the present outbreak. Second, while the chlorination step met required standards, it occurred before mincing.

The hypothesized source of this outbreak was minced celery from Processor A. The root cause is hypothesized to be _E. coli_ that persisted after chlorination and was subsequently mixed throughout the product during the mincing process. Temperature abuse at Hospital A and Hospital B may have further contributed to propagation of _E. coli_ in this product. The outbreak was declared over on [10 May 2021].

As there was no product left when the investigation had reached its conclusion, no product action was taken. Local and federal food safety authorities performed a 2nd, joint inspection of Processor A to make recommendations for more frequent testing for _E. coli_ and to conduct a review of the chlorination process. Follow-up was also conducted at Hospital A and Hospital B to propose methods to reduce the likelihood of temperature abuse by using time stamps to record when sandwiches are removed from the fridge.

Discussion
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An outbreak investigation of 6 cases of _E. coli_ O103 was conducted in April 2021. The outbreak was associated with consumption of minced celery from a local processor and sourced from California. While this is not the first _E. coli_ outbreak reported in celery (11), this is the first to be caused by _E. coli_ O103 and the first to exclusively impact a vulnerable, hospitalized population. This investigation resulted in several recommendations to improve food safety of this food item within the Island Health region.

Evidence from the epidemiological and food safety investigations support minced celery as the source of this outbreak. All 6 confirmed cases were exposed to the suspect source, and no other product was reported across all 6 confirmed cases, despite detailed menus for all inpatients. The outlier case, an outpatient who ate a tuna and celery sandwich only during their emergency room visit to Hospital A, added further support to celery as the suspect source. This investigation also revealed strong trace back evidence--the minced celery served in Hospital A and Hospital B was provided by the same supplier; the investigation also revealed strong trace forward evidence--the supplier provided the minced celery product only to the 2 hospitals, and nowhere else. Because the contaminated product was no longer available by the time of the investigation, and due to the cleaning procedures at Processor A, neither product samples nor environmental samples were available for testing. Despite the lack of laboratory evidence, the authors believe the strong epidemiological, trace back and trace forward evidence is sufficient to implicate minced celery in this outbreak.

The outbreak highlights the risk of raw vegetables provided to vulnerable populations and draws particular attention to the risk of mincing during processing. While previous work has documented the potential food safety hazards of fresh-cut produce (13), this outbreak serves to document the potential risks posed by mincing, which provides the opportunity for small amounts of bacteria remaining on the surface of a product, even after chlorination, to be spread throughout an entire batch. Attribution of the mincing step as problematic in this outbreak scenario is further supported as trace forward investigation revealed that more coarsely chopped celery from the same batch was supplied to a wide distribution network, exclusive of Hospital A and Hospital B, with no cases of the outbreak strain of _E. coli_ O103 associated with this product.

Despite providing food to a population of approximately 800 inpatients each day, identification of only 6 cases across Hospital A and Hospital B could potentially be explained by a low level of contamination, which may have caused illness only amongst those whose sandwiches were subjected to temperature abuse. Temperature abuse is a known vehicle for pathogen propagation (14-16), and was reported by the hospitals during the investigation follow-up. It is hypothesized that any contamination present after the mincing step in Processor A was further propagated by these reports of temperature abuse, resulting in the illnesses reported. A recommendation was made at the 2 implicated hospitals to add a time stamp to all sandwiches to mark the time the product was taken out of the fridge, to reduce the risk of temperature abuse moving forward.

There are several limitations to consider in the interpretation of these outbreak data. First, exposure data for celery was not available for the healthy population controls to directly compare with outbreak cases. However, given that 100% of confirmed cases had exposure to the suspect source, and this was the only common exposure across all 6 cases, the authors feel confident in the epidemiological evidence for this product. Second, the reporting delay for this outbreak was long, which in turn delayed the outbreak identification and investigation. Reporting delays are influenced by a multitude of factors, but comorbidities among the inpatient and outpatient cases in this outbreak may have delayed consideration of an enteric illness diagnosis and thus the requisition of a stool sample for testing. Third, several cases were missing onset dates as they could not be interviewed. For these individuals, their onset date likely predated their specimen collection date, which would also impact their exposure period. This was taken into account when interpreting the exposure data and analyzing hospital menus. Fourth, there were no food samples available to test for presence of _E. coli_ O103; therefore, there was no laboratory data to definitively confirm the source of this outbreak. However, despite the lack of laboratory confirmation, the authors believe the epidemiological evidence, the trace back data and the trace forward data provided strong support of the suspect source. Lastly, it could not be determined where or how _E. coli_ was introduced, as a further follow-up at the grower in the USA was outside the investigative jurisdiction of this outbreak.

Conclusion
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Raw vegetables, such as celery, are a known source of _E. coli_ contamination and present a risk to vulnerable populations. Mincing during the processing of raw vegetables, and temperature abuse prior to consumption, may provide additional layers of risk. This outbreak resulted in several recommendations to reduce the risk of minced celery served in hospitals, including more frequent testing at the processor, a review of the chlorination and mincing process and a review of hospital food services practices to mitigate temperature abuse.

References
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1. Yang SC, Lin CH, Aljuffali IA, Fang JY. Current pathogenic _Escherichia coli_ foodborne outbreak cases and therapy development. Arch Microbiol 2017;199(6):811-25.
2. Croxen MA, Law RJ, Scholz R, Keeney KM, Wlodarska M, Finlay BB. Recent advances in understanding enteric pathogenic _Escherichia coli_. Clin Microbiol Rev 2013;26(4):822-80.
3. Thomas MK, Murray R, Flockhart L, et al. Estimates of the burden of foodborne illness in Canada for 30 specified pathogens and unspecified agents, circa 2006. Foodborne Pathog Dis 2013;10(7):639-48.
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5. CDC; List of Selected Multistate Foodborne Outbreak Investigations. Atlanta (GA); CDC; 2021 (accessed 2021-06-21). https://www.cdc.gov/foodsafety/outbreaks/multistate-outbreaks/outbreaks-list.html
6. Schimmer B, Nygard K, Eriksen HM, et al. Outbreak of haemolytic uraemic syndrome in Norway caused by stx2-positive _Escherichia coli_ O103:H25 traced to cured mutton sausages. BMC Infect Dis 2008;8:41.
7. Mylius M, Dreesman J, Pulz M, et al. Shiga toxin-producing _Escherichia coli_ O103:H2 outbreak in Germany after school trip to Austria due to raw cow milk, 2017 - The important role of international collaboration for outbreak investigations. Int J Med Microbiol 2018;308(5):539-44.
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12. BC Ministry of Health Services Guidelines and Protocols Advisory Committee. Infectious Diarrhea - Guideline for Ordering Stool Specimens. BC MOH; Mar 16, 2009.
https://www2.gov.bc.ca/gov/content/health/practitioner-professional-resources/bc-guidelines/infectious-diarrhea
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Communicated by:
ProMED

[This posting reports a well-done epidemiological study showing minced celery being the reservoir for a non-O157 EHEC cluster occurring in a more vulnerable (hospitalized) population. - Mod.LL

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