From the article, "Given that kimchi is acidic in nature, typically with a pH less than 4.5 [Reference Kim, Jang, Kim, Lee, Kim, Ryu and Rhee14], it is often assumed to be an unlikely source for foodborne outbreaks. However, the present outbreak, and those noted above from East Asia, have called this assumption into question. Interestingly, pH testing in this outbreak revealed that pH decreased over time throughout the product’s shelf life. With decreased pH thought to reduce pathogenic load, it is notable that cases in this outbreak had consumption dates closer to the beginning of the product’s shelf life, when pH was likely higher, and the product was less acidic. It is also notable that a positive result for STEC O157 in this outbreak was found in a product with a pH result of 4.1, indicating that this strain of STEC O157 may have also been acid-tolerant, surviving exposure to this pH. Research is ongoing to determine if this may have been the case. This outbreak serves as a reminder that kimchi is a potential source of foodborne outbreaks, and that mitigating measures to prevent pathogen introduction and growth should be considered in the manufacturing process."
Epidemiology and Infection
https://www.cambridge.org/core/journals/epidemiology-and-infection/article/fermenting-a-place-in-history-the-first-outbreak-of-escherichia-coli-o157-associated-with-kimchi-in-canada/B8EC9B59037C9506D1EAE19DDD4E9AAC
Fermenting a place in history: The first outbreak of Escherichia coli O157 associated with kimchi in Canada
Published online by Cambridge University Press: 08 June 2023
Courtney R. Smith , Heather Bond , Ashley Kearney, Kelvin Chau, Linda Chui, Monica Gerrie, Lance Honish, Yves Oukouomi Lowé, Victor Mah and Anna J. W. Manore
Abstract
A Canadian outbreak investigation was initiated in January 2022 after a cluster of cases of Shiga-toxin-producing Escherichia coli (STEC) O157 was identified through whole genome sequencing (WGS). Exposure information was collected through case interviews. Traceback investigations were conducted, and samples from case homes, retail, and the manufacturer were tested for STEC O157. Fourteen cases were identified in two provinces in Western Canada, with isolates related by 0–5 whole genome multi-locus sequence typing allele differences. Symptom onset dates ranged from 11 December 2021 to 7 January 2022. The median age of cases was 29.5 (range 0–61); 64% were female. No hospitalisations or deaths were reported. Of 11 cases with information available on fermented vegetable exposures, 91% (10/11) reported consuming Kimchi Brand A during their exposure period. The traceback investigation identified Manufacturer A in Western Canada as the producer. One open and one closed sample of Kimchi Brand A tested positive for STEC O157, with isolates considered genetically related by WGS to the outbreak strain. Napa cabbage within the kimchi product was hypothesised as the most likely source of contamination. This paper summarises the investigation into this STEC O157 outbreak associated with kimchi, the first reported outside of East Asia.
A Canadian outbreak investigation was initiated in January 2022 after a cluster of cases of Shiga-toxin-producing Escherichia coli (STEC) O157 was identified through whole genome sequencing (WGS). Exposure information was collected through case interviews. Traceback investigations were conducted, and samples from case homes, retail, and the manufacturer were tested for STEC O157. Fourteen cases were identified in two provinces in Western Canada, with isolates related by 0–5 whole genome multi-locus sequence typing allele differences. Symptom onset dates ranged from 11 December 2021 to 7 January 2022. The median age of cases was 29.5 (range 0–61); 64% were female. No hospitalisations or deaths were reported. Of 11 cases with information available on fermented vegetable exposures, 91% (10/11) reported consuming Kimchi Brand A during their exposure period. The traceback investigation identified Manufacturer A in Western Canada as the producer. One open and one closed sample of Kimchi Brand A tested positive for STEC O157, with isolates considered genetically related by WGS to the outbreak strain. Napa cabbage within the kimchi product was hypothesised as the most likely source of contamination. This paper summarises the investigation into this STEC O157 outbreak associated with kimchi, the first reported outside of East Asia.
Food safety investigation
Kimchi Brand A from Grocery Chain A was produced by Manufacturer A in Western Canada without any heat treatment steps, which is a common practice for kimchi processing. The product contained Napa cabbage, radish, red pepper powder, garlic, sweet rice powder, green onions, onion, salt, anchovy extract, salted shrimp, ginger, and sugar water.
Thirty-three retail and retention samples of Kimchi Brand A, representing 61 units from 31 production dates, were collected for testing. Best-before dates of these samples ranged from 22 January 2022 to 25 March 2022. Of the tested samples, two isolates from a single retention sample were positive for STEC O157. The remaining samples were not detected for STEC O157. The positive sample was a retention sample from Manufacturer A with a best-before date of 23 January 2022. The sample had a pH of 4.1, and the two STEC O157 isolates recovered from the sample matched the clinical isolates associated with the outbreak by wgMLST (Figure 2). The pH testing of various kimchi samples resulted in a range of pH from 4.1 to 5.3, with older samples having lower pH.
Kimchi Brand A with a best-before date of 29 January 2022 was only sold at Grocery Chain A in four provinces in Canada, including Province A and Province B, with the majority of the product distributed in Province A. The production dates for this product were 26 and 29 November 2021. Kimchi Brand A with a best-before date of 23 January 2022 was only sold at Grocery Chain A in one province in Western Canada; this province did not report any associated illnesses. The production date for this product was 23 November 2021. Production dates for both products occurred prior to the earliest case onset of 11 December 2022.
Napa cabbage was hypothesised to be the likeliest source of contamination in the kimchi product. This hypothesis was supported by four pieces of evidence. First, the Napa cabbage was the only raw vegetable ingredient that received no sanitising wash, and as per common practice for kimchi processing, no lethality steps. Second, the same shipment of imported Napa cabbage grown at Farm A in Washington state was used in the two lots of Kimchi Brand A found to contain STEC O157. This convergence was not identified for any other fresh ingredient in Kimchi Brand A. Third, this same shipment of Napa cabbage from Farm A was a new source temporarily used by Manufacturer A during the production of the two implicated lots; the manufacturer did not receive any additional shipments from this source after this period. Lastly, Napa cabbage comprised approximately 70% of the kimchi formulation by weight. This root cause hypothesis was unable to be confirmed, due to lack of appropriate samples. No connection was identified between the California romaine lettuce sample that matched the outbreak case isolates by wgMLST, and the Napa cabbage from Washington that is the suspected, although unconfirmed, source of the current outbreak.
Control measures
A Public Health Alert was posted on the Canadian Network for Public Health Intelligence to provide information on the outbreak investigation, including case definitions and the initial recall notice, to public health professionals across Canada. A food recall warning was issued on 28 January 2022 for the kimchi product with the best-before date of 29 January 2022. A second food recall warning was issued on 6 February 2022 for the product with the best-before date of 23 January 2022. A Public Health Notice was posted on 29 January 2022 to inform people in Canada of the outbreak and to not eat, sell, or serve the recalled kimchi. This Public Health Notice was updated on 8 February 2022 to reflect the second food recall warning.
The outbreak was declared over on 29 March 2022, based on the last recall date of 6 February 2022, a 10-day maximum incubation period for STEC O157, and the 90th percentile reporting delay of 41 days.
Discussion
A total of 14 cases of STEC O157 were identified in this outbreak across two provinces in Western Canada. The source of the outbreak was determined to be Kimchi Brand A, with Napa cabbage hypothesised as the source of contamination. This was the first outbreak of its kind to be reported outside of East Asia, and highlights the potential food safety risks of fermented vegetable products like kimchi. The alignment of the epidemiological, food safety, and laboratory findings in this outbreak investigation helped in the rapid identification of the source, and its removal from the Canadian market.
Although the hypothesis could not be confirmed, the investigation for this outbreak resulted in the identification of the Napa cabbage as the most likely source of contamination. Microbial testing in South Korea has indicated that salted Napa cabbage, such as that used in kimchi production, can be a major source of coliform bacteria and E. coli [Reference Kim, Jang, Kim, Lee, Kim, Ryu and Rhee14]. Outbreaks associated with kimchi in East Asia have prompted several research studies on the microbiological quality of Napa cabbage [Reference Kim, Jang, Kim, Lee, Cho, Kim and Rhee29, Reference Song, Chung, Kang and Ha30], and one research study was able to isolate E. coli from irrigation water used in Napa cabbage cultivation, albeit not STEC O157 [Reference Yun, Kim, Ryu, Kim, Park, Kim, Lee and Kim31]. Notably, no connection could be made between the Napa cabbage from Washington – the suspected source of contamination in this outbreak – and the romaine lettuce from California that was sampled during a previous US investigation. As such, this investigation supports the possibility that the same E. coli strain can be found in different leafy greens, in geographically distinct areas. Interestingly, the head of Napa cabbage is similar in shape to that of a head of romaine lettuce; the shape of romaine lettuce has been theorised to play a key role in STEC O157 contamination [Reference Coulombe, Catford, Martinez-Perez and Buenaventura5, Reference Marshall, Hexemer, Seelman, Fatica, Blessington, Hajmeer, Kisselburgh, Atkinson, Hill, Sharma, Needham, Peralta, Higa, Blickenstaff, Williams, Jhung, Wise and Gieraltowski7]. As romaine lettuce heads are relatively open, both outer and inner leaves have the potential for STEC O157 exposure from various sources, such as contaminated irrigation water [Reference Coulombe, Catford, Martinez-Perez and Buenaventura5]. The unique shape of romaine is thought to be a factor as to why a greater number of outbreaks of STEC O157 are linked to romaine lettuce compared to other, more compact, leafy greens. The similar shape of Napa cabbage could also play a role in its vulnerability to STEC O157 contamination.
Given that kimchi is acidic in nature, typically with a pH less than 4.5 [Reference Kim, Jang, Kim, Lee, Kim, Ryu and Rhee14], it is often assumed to be an unlikely source for foodborne outbreaks. However, the present outbreak, and those noted above from East Asia, have called this assumption into question. Interestingly, pH testing in this outbreak revealed that pH decreased over time throughout the product’s shelf life. With decreased pH thought to reduce pathogenic load, it is notable that cases in this outbreak had consumption dates closer to the beginning of the product’s shelf life, when pH was likely higher, and the product was less acidic. It is also notable that a positive result for STEC O157 in this outbreak was found in a product with a pH result of 4.1, indicating that this strain of STEC O157 may have also been acid-tolerant, surviving exposure to this pH. Research is ongoing to determine if this may have been the case. This outbreak serves as a reminder that kimchi is a potential source of foodborne outbreaks, and that mitigating measures to prevent pathogen introduction and growth should be considered in the manufacturing process.
There were several investigative strengths of this outbreak to highlight. Initial interviews at the local public health level were key to the early identification of cases reporting exposure related to Grocery Chain A. In addition, the quick completion of re-interviews at the federal level allowed for the rapid identification of a source and its removal from the market. In this outbreak, re-interviewing was expedited as a result of a standard process in Province A, whereby consent for re-interview by provincial or national public health authorities is sought at the time of initial interview. This negated the need to seek case consent for re-interview once an outbreak has been identified, as is the usual process in many jurisdictions in Canada. Similarly, the inclusion of a question about fermented vegetables on the PHAC E. coli hypothesis-generating questionnaire was also crucial for the quick identification of this exposure among the outbreak cases. This variable was added to the PHAC E. coli hypothesis-generating questionnaire in the fall of 2018 during a periodic review process, based on a comparison to the variables included in questionnaires in other jurisdictions. Given the turnaround time for WGS results, it is often the case that leftovers are not available from case homes for sampling at the time of re-interview by federal public health officials, or that product may no longer be available at retail to test. However, in this outbreak, the investigative team was able to identify the outbreak strain both in an open sample of kimchi from a case home (best-before date 29 January 2022) and in a retention sample from the manufacturer (best-before date 23 January 2022). Good record-keeping practices at the manufacturer were also helpful to identify the ingredients used in specific lots, and their sources, which was helpful for hypothesising about the root cause. Ultimately, the investigation resulted in a strong alignment of epidemiological, food safety, and laboratory evidence to implicate Kimchi Brand A as the source of the outbreak.
There are several limitations to consider in the context of this outbreak investigation. First, while there is support for the hypothesis that Napa cabbage was the source of contamination of the kimchi, this was not able to be confirmed and thus potential preventive measures at the farm level could not be implemented. Second, the product’s increasing acidity over time may have impacted the survival and detection of STEC O157 throughout the shelf life of the product. Only one of the four open samples from case homes had STEC O157 detected. However, these products were tested towards the end of their shelf life, when they were likely to be more acidic and less conducive to the survival of bacteria. For this reason, it is unclear whether all ‘not detected’ results truly mean that each product lot was free from STEC O157 at the beginning of its shelf life. Third, only one retention sample was available at Manufacturer A for many production dates, and therefore these single samples were likely not representative of the whole lot. Furthermore, kimchi is comprised of large pieces of vegetables which could contribute to heterogenous subsamples. Fourth, the distribution of the kimchi products went beyond the two provinces with identified cases. Although fewer cases of product were distributed in the other provinces, underreporting, especially as exacerbated by the COVID-19 pandemic, could also explain this result. Lastly, not all re-interviewed cases confirmed exposure to kimchi, and therefore the source of illness could not be confirmed for all outbreak cases. One case reported ‘don’t know’ to kimchi exposure, and one case reported ‘no’ to kimchi exposure. Although kimchi exposure cannot be explained for these two cases, it is rare within a foodborne outbreak investigation to account for every case’s exposure to the outbreak source. Of note, the case reporting ‘no’ to kimchi exposure was interviewed via proxy, and the case reporting ‘don’t know’ was admittedly a frequent kimchi eater. Lastly, there was an additional two cases that were lost to follow-up for re-interview, and their exposure to kimchi could not be ascertained.
This paper outlines an outbreak of STEC O157 in Canada associated with kimchi, the first known outbreak to occur outside of East Asia. The investigation highlights the potential food safety risks of kimchi, a fermented food often thought to be an inhospitable environment to pathogens. Future research will aim to further understand the food matrix of kimchi and the impact of the microbiota over time. As a known outbreak vehicle, outbreak investigators are encouraged to consider fermented vegetables, such as kimchi, as potential sources when investigating future outbreaks of STEC O157.
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9705866/
Effect of Enterotoxigenic Escherichia coli on Microbial Communities during Kimchi Fermentation
Woojung Lee,1,2 Hyo Ju Choi,1 Hyunwoo Zin,1 Eiseul Kim,2 Seung-Min Yang,2 Jinhee Hwang,1 Hyo-Sun Kwak,1,2 Soon Han Kim,corresponding author1,* and Hae-Yeong Kimcorresponding author2,*
The diverse microbial communities in kimchi are dependent on fermentation period and temperature. Here, we investigated the effect of enterotoxigenic Escherichia coli (ETEC) during the fermentation of kimchi at two temperatures using high-throughput sequencing. There were no differences in pH between the control group, samples not inoculated with ETEC, and the ETEC group, samples inoculated with ETEC MFDS 1009477. The pH of the two groups, which were fermented at 10 and 25°C, decreased rapidly at the beginning of fermentation and then reached pH 3.96 and pH 3.62. In both groups, the genera Lactobacillus, Leuconostoc, and Weissella were predominant. Our result suggests that microbial communities during kimchi fermentation may be affected by the fermentation parameters, such as temperature and period, and not enterotoxigenic E. coli (ETEC).
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