Abstract
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Background
- Unexpectedly, during the coronavirus disease 2019 (COVID-19) pandemic (2020–2022), it was reported that the number of acute gastroenteritis outbreaks (AGEOs) increased abruptly in childcare centers and kindergartens due to the increase in norovirus GII.4 transmission. However, changes in AGEOs in schools have not been reported during the same period. Therefore, this study aimed to compare the characteristics of AGEOs in schools before and after 2020.
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Methods
- We analyzed the results of AGEO epidemiological investigation reports in Seoul.
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Results
- The number of AGEO cases in schools decreased after 2020. Norovirus was identified as the causative pathogen in 10 of 11 cases in 2019, while only five cases were caused by norovirus among the 12 cases between 2020 and 2022. The average attack rate decreased from 10.2% in 2019 to 5.2% between 2020 and 2022. The average duration of patient occurrence also decreased from 7.5 days in 2019 to 4 days between 2020 and 2022. Secondary transmission occurred in all 2019 cases. However, secondary transmission was not observed in half of the cases between 2020 and 2022.
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Conclusion
- Norovirus outbreaks and secondary transmission in schools declined after the onset of the COVID-19 pandemic, probably because of infection control measures implemented to prevent COVID-19 transmission.
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Keywords: COVID-19; Gastroenteritis; Health policy; Norovirus; Schools
Introduction
- In Korea, acute gastroenteritis outbreaks (AGEOs) are commonly referred to as food poisoning outbreaks [1]. This is because gastrointestinal symptoms such as vomiting, abdominal pain, or diarrhea are induced in individuals who consume contaminated food [2]. The occurrence of AGEOs due to contaminated food has been effectively prevented by the separation of the water supply and sewerage systems [3] and strict hygiene practices in restaurants and group cafeterias.
- However, AGEOs can also occur through person-to-person transmission within groups, originating from an infected individual [4]. This is one of the reasons why occasional AGEOs still occur in settings such as childcare centers, schools, and workplaces where group meals are common despite stringent preventive food safety measures. Generally, the fatality rates of waterborne and foodborne diseases remain low [5]. However, persistent infection can lead to prolonged pathogen shedding, thereby increasing the risk of secondary transmission [4]. Therefore, prompt epidemiological investigations are crucial to identifying the source of AGEOs and preventing further spread of pathogens.
- Norovirus is the leading cause of waterborne and foodborne diseases worldwide [6-8] and is particularly prevalent among individuals under 20 years of age [8,9]. In general, norovirus accounts for the highest proportion of AGEO cases in childcare centers, kindergartens [10], and schools [11]. One of the key characteristics of norovirus is its high transmissibility among individuals, attributed to its stability and genetic diversity. Additionally, transmission can persist even after the resolution of patient symptoms [12,13].
- It was estimated that measures to prevent coronavirus disease 2019 (COVID-19) transmission would effectively prevent person-to-person transmission of pathogens that induce AGEOs. However, we recently reported a sudden increase in AGEOs in childcare centers and kindergartens, particularly those caused by norovirus GII.4 from 2020 to 2022 [10]. Moreover, most AGEOs in childcare centers and kindergartens occurred unexpectedly via person-to-person transmission. Thus, studies are needed to compare AGEOs before and after the COVID-19 pandemic in schools; however, to the best of our knowledge, there have been no such reports. This study aimed to analyze and characterize AGEOs in schools and propose school health policies to prevent AGEOs.
Methods
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Ethics statement: The data were obtained through epidemiological investigations conducted under the Infectious Disease Control and Prevention Act for Public Health. Therefore, Institutional Review Board approval was not required for this study. The epidemiological investigation of AGEOs generally proceeds with voluntary consent from school staff and parental consent for lower-grade elementary school students. We mainly used data from epidemiological investigation result reports, which contain no personal information. Therefore, patient consent was not relevant for this study.
- 1. Data collection
- The status of AGEOs was investigated using a database stored in the Seoul Metropolitan Government and the Korea Disease Control and Prevention Agency (KDCA) integrated disease management system.
- The number of patients with total gastrointestinal infections and norovirus infections in Korea between 2015 and 2022 was obtained from the Infectious Diseases Homepage, which is managed by the KDCA and offers open access to data on infectious diseases (https://dportal.kdca.go.kr/pot/is/st/gstrnftn.do). The data were generated by a sentinel surveillance system and not by a mandatory surveillance system. It contains data on Salmonella, Vibrio parahaemolyticus, enteropathogenic Escherichia coli (EPEC), enterotoxigenic Escherichia coli (ETEC), enteroinvasive Escherichia coli, Campylobacter, Clostridium perfringens, Staphylococcus aureus, Bacillus cereus, Yersinia enterocolitica, Listeria monocytogenes, group A rotaviruses, astrovirus, adenovirus, norovirus, and sapovirus.
- For epidemiological data, we reviewed the epidemiological investigation result reports of AGEOs that occurred after 2019, as maintained by the Seoul Metropolitan Government. However, one case from 2022 was excluded due to the absence of epidemiological investigation result reports from the public health office. Instead, we included two cases that occurred in the fourth quarter of 2022. Cases that occurred outside school settings, such as retreats, clubs, sports clubs, and after-school activities, which were not related to school meals, were excluded. These cases differed significantly in scale from those of typical AGEO in schools. Due to the small scale, the attack rate was exceptionally high compared to general outbreaks. Moreover, due to the small sample size and the difficulty in performing a precise epidemiologic investigation, it was often difficult to identify the cause of AGEO. Therefore, these cases were excluded to increase comparability. As a result, three cases from 2018, two from 2019, one from 2020, and one from 2022 were excluded. Among the 29 outbreaks from 2019 to the third quarter of 2022, we excluded eight cases based on the aforementioned criteria. With the addition of two cases in the fourth quarter of 2022, a total of 23 epidemiological investigation result reports were analyzed.
- 2. Data analysis
- Data analysis was performed as previously described [10]. Briefly, to examine humans and the environment, rectal smears and swabs were the main methods used to collect samples; stool samples were also used occasionally. These samples were sent to the Seoul Research Institute of Public Health and Environment (SRIPHE) for testing, and the results were subsequently reported to public health centers. The standard procedure for testing at SRIPHE is based on the KDCA guidelines, which are available online (https://www.kdca.go.kr/board/board.es?mid=a20507020000&bid=0019, uploaded on July 14, 2017).
- Based on the SRIPHE data, causative pathogens were defined as those detected in more than two symptomatic patients, and both the epidemic curve and clinical symptoms were consistent with the infection. The attack rate was calculated as previously described [14]. In brief, it was calculated by dividing the sum of symptomatic patients and asymptomatic individuals with detected causative pathogens by the total number of people affected by school-provided group meals.
- The incubation period of the causative pathogen was determined based on data provided by the KDCA (https://www.kdca.go.kr/board/board.es?mid=a20507020000&bid=0019&tag=&act=view&list_no=725067). Based on these guidelines, the incubation period of norovirus was calculated as 40 hours (10–50 hours), that of EPEC as 120 hours (1–6 days), that of ETEC as 62 hours (10 hours–3 days), that of Campylobacter jejuni as 72 hours (2–5 days), and that of Salmonella typhimurium as 66 hours (6–72 hours).
- To objectively identify secondary transmission occurrence, we defined it as occurring when the interval between symptom onset in the first and last cases exceeded the range of the incubation period for the causative pathogen, as mentioned above. In other words, secondary transmission was confirmed when the ratio of the interval between the first and last cases and the incubation period of the causative pathogen was greater than one. If the causative pathogen was unknown, it was defined as confirmed if the interval was longer than 2 days.
- 3. Statistics
- For statistical analysis, the Fisher exact, Shapiro-Wilk, and Mann-Whitney U-tests were performed using R (version 4.5.2, https://cran.r-project.org; R Foundation for Statistical Computing, Vienna, Austria). The Wilcoxon t-test was performed using Microsoft Excel in Office 16 (Microsoft, Redmond, WA, USA). In the case of two causative pathogens, each was counted as one when the Fisher exact test was performed, and when the number of occurrences was expressed numerically, each was counted as 0.5.
Results
- 1. Frequency of acute gastroenteritis outbreaks from 2016 to the third quarter of 2022 in Seoul schools
- Between 2016 and 2019, approximately 4.3 cases of AGEOs in schools were reported per quarter. Eleven such cases were reported in 2019. However, in 2020, only one case was reported per quarter, and in 2021, only 10 cases were reported in seven quarters (Fig. 1).
- 2. Proportion of norovirus in acute gastroenteritis outbreaks in Seoul schools and infectious enterocolitis in Korea
- Among the 11 cases of AGEOs in schools in 2019, norovirus was the causative pathogen in 10 of them. In one case, norovirus was the causative pathogen combined with EPEC. However, among the 12 cases reported since 2020, norovirus was the causative pathogen in only five of them, with EPEC detected in one case. The proportion of norovirus among the AGEO causative pathogens in schools has significantly decreased since 2020 (Fig. 2A). In other cases, EPEC, ETEC, or C. jejuni was the causative pathogen.
- After the outbreak of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infections, the number of patients with total gastrointestinal infectious diseases decreased in 2020 and then gradually increased again. Although the proportion of norovirus infections in total gastrointestinal infectious diseases in Korea decreased significantly in 2022 compared to 2019, the absolute difference was below 4% points (27.45% in 2019 vs. 23.51% in 2022) (Fig. 2B).
- 3. Comparison of acute gastroenteritis outbreak characteristics in Seoul schools between 2019 and 2020 to 2022
- Although not statistically significant, the average attack rate decreased from 10.2% in 2019 to 5.2% in 2020 to 2022. The median value also decreased from 8.7% to 5.5% (Fig. 3A). During the outbreak, the duration of patient occurrence decreased significantly from approximately 7.5 to 4 days and 7 days to 3 days in median value (Fig. 3B). To adjust for the varying incubation periods of different causative pathogens, we divided the duration of patient occurrence by the incubation period range of the causative pathogen. This value significantly decreased from approximately 3.77 in 2019 to 1.58 in 2020 to 2022 (Fig. 3C). Subsequent or continuous transmission occurs when the duration of patient occurrence is sufficiently long. Therefore, secondary transmission was defined as cases where the duration of patient occurrence exceeded the expected range (refer to the data analysis section). Although secondary transmission occurred in all 11 cases in 2019, it occurred in only half of the cases between 2020 and 2022. The possibility of secondary transmission during outbreaks significantly decreased (Fig. 3D). Even when the threshold for defining secondary transmission was doubled, as continuous transmission from the index case would have been possible, still all 11 cases in 2019 remained positive. However, only four of the 12 cases were classified as positive in 2020 to 2022 (data not shown).
Discussion
- In Korea, the COVID-19 pandemic began in January 2020. To prevent the transmission of SARS-CoV-2, wearing masks was mandatory in all settings, except homes. The importance of hand hygiene was also emphasized. Additionally, individuals with infectious symptoms such as fever, cough, etc., were isolated immediately.
- During the COVID-19 pandemic, schools in Korea suspended in-person attendance completely or implemented alternating attendance schedules to reduce the density of students to limit SARS-CoV-2 transmission. The incidence of AGEOs decreased in 2020 and 2021, likely owing to school attendance-related policies. However, this decline persisted even after all restrictions, including school attendance measures, were lifted in the first quarter of 2022 (Fig. 1). In addition, the total number of AGEO reports was 74, which was higher than the 64 reports in the same period in 2019 (data not shown), suggesting that other factors contributed to the decline in AGEO cases in schools. Furthermore, changes in the AGEO characteristics in schools cannot be explained only by the suspension of school attendance or alternative school attendance (Figs. 2, 3).
- The most significant change in AGEO cases in schools was the significant decrease in the proportion of cases in which norovirus was the causative pathogen (Fig. 2A). Although the proportion of norovirus-positive patients among those with gastrointestinal infectious diseases in Korea has remained relatively stable (Fig. 2B), the norovirus detection rate has significantly decreased. In 2019, norovirus was detected in 10 of the 11 AGEO cases. However, after 2020, only five of the 12 cases were attributed to norovirus infection (Fig. 2A). Noroviruses are highly contagious [15] and considerable norovirus outbreaks are caused by person-to-person transmission [10]. Therefore, these data suggest that the transmission of causative pathogens from person to person has been well controlled, which has probably led to a decrease in norovirus outbreaks in schools.
- The second change was a decrease in the average attack rate. Although the difference in attack rate was not statistically significant, likely owing to a large standard deviation and small number of cases, the average attack rate was reduced by half (Fig. 3A). We speculated that the decrease in attack rate was due to a reduction in the duration of patient occurrence and the frequency of secondary transmission occurrence (Fig. 3B–3D).
- The duration of patient occurrence could be prolonged by secondary or continuous transmission [14]. However, continuous transmission through food was considered negligible, as school meals had generally stopped after epidemiological investigation. Therefore, we speculated that the prolonged intervals between the index and last cases were due to secondary transmission. Additionally, secondary transmission was likely caused by person-to-person transmission. Therefore, these data also strongly suggest that person-to-person transmission of AGEOs has been effectively controlled in schools since the onset of the COVID-19 pandemic.
- We speculated four possible reasons for the decrease in person-to-person transmission of AGEOs in schools.
- First, the importance of hand hygiene was strongly emphasized in preventing the spread of SARS-CoV-2. In Korea, the government promoted hand hygiene through advertisements, while public health centers provided education at each facility to publicize the proper ways to keep hands clean [16,17]. Therefore, students made extra efforts to wash their hands, which may have contributed to the decrease in disease transmission.
- Second, the use of hand sanitizers increased [18]. Following the onset of the COVID-19 pandemic, hand sanitizers were placed in classrooms and restrooms. Moreover, some students carried and frequently used their own hand sanitizers. Students in schools generally take a 10-minute break after 40 to 50 minutes of class, during which many may rush to the restroom. As the waiting time to use the sinks increases, the possibility that certain students may skip washing their hands after using the restroom may increase. However, the availability of hand sanitizers provides an alternative, increasing the possibility of students maintaining hand hygiene. In fact, it was reported that the proportion of hand sanitizer use has increased since the COVID-19 pandemic. Therefore, the number of students cleaning their hands with soap or hand sanitizers has increased accordingly [18].
- Third, the rapid isolation of students with symptoms played a crucial role in disease prevention. One of the most significant behavioral changes due to the COVID-19 pandemic was the absence from school or returning home quickly when symptoms such as fever occurred. In certain cases, norovirus was detected before symptoms occurred; however, patients with norovirus infections generally became contagious only after symptom onset [13,15]. Thus, rapid isolation may be highly effective in preventing the transmission of norovirus and other AGEO pathogens.
- The final factor was a change in the school food distribution method. On March 23, 2020, the Seoul Metropolitan Office of Education introduced a new school meal management plan. When serving food in cafeterias, the seating arrangements were modified to ensure an adequate distance between students; temporary table screens were installed on tables, and the serving time was staggered by grade or class. In addition, hand sanitizers were placed at the entrance to and inside the cafeteria. After each meal session, ventilation and disinfection were carried out for the next serving. Considering the cafeteria’s role not only as a place for eating but also as a gathering point for all students, the measures implemented to prevent SARS-CoV-2 transmission also possibly prevented person-to-person transmission in the cafeteria and the transmission of norovirus.
- Wearing masks may also have prevented the transmission of norovirus, as several studies have indicated that norovirus can be transmitted through aerosols [19,20]. Unlike childcare centers, the decline in norovirus outbreaks in schools may be attributed to a shift in the dominant norovirus genotypes from GII.2 to GII.4 [10]. In other words, the exact reason for the reduction in the occurrence of AGEOs in schools, especially due to norovirus infections, after the onset of the COVID-19 pandemic, remains unclear.
- Therefore, further studies are needed to examine the effects of hand sanitizers, rapid isolation of students with symptoms, and the use of temporary screens, ventilation, and disinfection for the next serving in cafeterias. These studies will help to determine how AGEO and norovirus outbreaks in schools can be prevented in the post-COVID-19 era.
- Finally, we recommend sharing data on the current characteristics of AGEO, such as causative pathogens or foods at metropolitan or provincial levels, with public health centers. Understanding the epidemiology of AGEO would help guide the direction of investigations. For example, based on the distribution of patients and epi-curve at the time of the investigation, it was easy to determine that it was the cause of a common origin in schools such as food (Supplementary Fig. 1A, 1B) [21]. However, at the time, it was known that norovirus was not the predominant causative pathogen of AGEOs in schools, but both E. coli and norovirus were responsible for a similar proportion of cases. The case detailed in the Supplementary Meterial 1 was due to EPEC and norovirus infections occurring simultaneously in a different manner (Supplementary Table 1, Supplementary Fig. 1C–1F). It would have presented a significant analytical challenge to an epidemiological investigation if it had been performed under the assumption of a single cause. However, a rapid and accurate investigation was possible because the epidemiology of currently prevalent AGEOs in schools was well understood. Similar to this case, sharing epidemiological data improves the quality of epidemiological investigation [22].
- Our study has several limitations that should be considered when interpreting the results. First, as this was a retrospective observational study, a definitive causal relationship could not be established. Further multicenter collaborative studies are warranted.
- Second, our analysis was restricted to only 23 cases. Regarding analyses of data from before the COVID-19 pandemic, we could only use 2019 data because AGEO epidemiological investigation result reports up to 2018 were archived by other institutions. Furthermore, our data are restricted to Seoul, the largest city in Korea. Therefore, our findings should be applied to other regions with caution. To address these limitations, a larger dataset from a wider geographical and temporal scope is necessary, possibly collected by the KDCA or other metropolitan and provincial governments together.
- As noted above, our analysis was conducted within the context of the COVID-19 pandemic. This period experienced significant changes in the awareness and behavior of students, parents, and teachers. Additionally, as mentioned above, the dominant circulating norovirus strain also changed. The presence of these changes makes it more challenging to analyze causal relationships.
- Finally, we analyzed the occurrence of secondary transmission based on the duration of case onset and the incubation period of the causative pathogens. Although this method is simple and objective, it carries the risk of misclassification. Specifically, a case could be incorrectly determined as secondary transmission in rare instances if the patient’s symptoms appeared outside the typical incubation period, even if no actual secondary transmission occurred. Conversely, cases of secondary transmission could have been misclassified if the patient’s symptoms appeared unusually early. Therefore, it is important to remember that the most accurate method for identifying the occurrence of secondary transmission is to investigate patient contact history and analyze the epidemic curve.
- In conclusion, since the onset of the COVID-19 pandemic, the proportion of AGEO cases caused by noroviruses has declined, along with a reduction in secondary transmission. This was probably due to a decrease in person-to-person transmission of AGEO-causing pathogens. Further multicenter studies are necessary to establish this causal relationship more clearly and to translate these findings into school policies.
Supplementary materials
Supplementary Table 1, Supplementary Fig. 1, and Supplementary Material 1 can be found at https://doi.org/10.12701/jyms.2025.42.65.
Supplementary Fig. 1.
Results of epidemiological investigation of the outbreak. (A) Distribution of patients at the initial time of epidemiological investigation. (B–F) Results after the end of the outbreak. (B) Epidemic curve for school. Light blue bars represent the occurrence of cases in classroom X, 2nd grade, and gray bars represent the occurrence of cases in other classrooms of the school. (C) Epidemic curve for classroom X, 2nd grade. (D) Epidemic curve for the other classrooms. (E) Frequencies of symptoms in the 70 cases. Light blue bars represent the frequencies of symptoms among cases in classroom X, 2nd grade. The grey bars represent those in the other classrooms. Multiple symptom selection is allowed. (F) The proportion of symptoms among 15 cases in classroom X, 2nd grade, and 55 cases in the other classrooms.
jyms-2025-42-65-Supplementary-Fig-1.pdf
Article information
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Conflicts of interest
No potential conflict of interest relevant to this article was reported.
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Acknowledgments
Dr. Son would like to express sincere gratitude to the public health centers in Seoul, Seoul Research Institute of Public Health and Environment, the Ministry of Food and Drug Safety, and Seoul Metropolitan Office of Education for their effort to prevent AGEO in schools together. He also extends his appreciation to the Infectious Disease Control Division of the Seoul Metropolitan Government. It was a huge luck and a pleasure to work together during his military service.
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Funding
None.
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Author contributions
Conceptualization, Formal analysis, Supervision, Validation: ES, YHK; Data curation, Methodology, Project administration, Visualization, Investigation, Resources, Software: ES; Writing-original draft: ES; Writing-review & editing: ES, YHK.
Fig. 1.The number of acute gastroenteritis outbreaks (AGEOs) reports in schools per quarter. Using a database from Seoul, the number of AGEO cases in schools in Seoul from 2016 to the third quarter of 2022 is shown. The cases in which school meals are not involved are excluded. Q, quarter.
Fig. 2.Causative pathogens of acute gastroenteritis outbreaks (AGEOs) in schools and the proportion of norovirus infections among the total gastrointestinal (GI) infections in Korea. (A) The causative pathogen was analyzed using epidemiological investigation results of AGEOs in schools. Salmonella and Campylobacter refer specifically to Salmonella typhimurium and Campylobacter jejuni, respectively. Statistical analysis was performed using the Fisher exact test. *p≤0.05. (B) The number of total GI infection and norovirus infection reports from 2015 to 2022 is shown. COVID-19, coronavirus disease 2019; EPEC, enteropathogenic Escherichia coli; ETEC, enterotoxigenic Escherichia coli.
Fig. 3.The occurrence of secondary infections and attack rates in acute gastroenteritis outbreaks (AGEOs). (A–C) Data are presented by box-and-whisker plots. The horizontal lines represent the maximum and minimum values, except for outlier data. The boxes represent the range of the interquartile range. The ‘X’ marks represent the mean value, and the line in the box represents the median value. (A) Attack rate was calculated as the number of patient cases divided by the total number of individuals exposed to school meals. For statistics, the Mann-Whitney U-test is performed. (B) The interval days between symptom onset in the first and last cases were calculated using the epidemic curve from the epidemiological investigation result reports. (C) The range of incubation period of the causative pathogen is defined as mentioned in the Methods section. Each interval between the first and last patients is divided by each causative pathogen’s range of incubation period. If the causative pathogen is more than one, the longer range is used. (B, C) For statistics, the Welch t-test was performed after the Shapiro-Wilk test result was confirmed. *p≤0.05, **p≤0.01. (D) For statistics, the Fisher exact test is performed. *p≤0.05.
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