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Norovirus is the most common cause of acute gastroenteritis outbreaks worldwide (1). In China and some other Asian countries, most norovirus outbreaks occur in schools and kindergartens (2). Norovirus infection is difficult to control in these enclosed and crowded settings, which can easily lead to outbreaks of gastroenteritis (3). There are few studies on the risk factors of norovirus outbreaks in schools and kindergartens (4–6). This study analyzed the impact of facility conditions, disinfection procedures, and case activities on norovirus outbreaks in schools and kindergartens. Norovirus outbreaks were defined as the case group, and a 1∶2 matching approach was applied to select a control group with norovirus clusters. Univariate and multivariate conditional logistical regression analyses showed that students vomiting at school or kindergarten, case activity in public areas, and first case’s classroom less than 5 meters from toilets were risk factors for norovirus outbreaks. Taking targeted measures to reduce or eliminate the impact of these factors will help control norovirus outbreaks in schools and kindergartens.
Primary, secondary, and kindergarten schools in Beijing Municipality, China that reported norovirus clusters or outbreaks between July 2017 and June 2022 were selected for this study. Trained professionals conducted epidemiological investigations, collecting anal swabs or stool samples for nucleic acid detection, and a norovirus outbreak was confirmed if more than two cases tested positive for norovirus. Referring to the guidelines on outbreak investigation, prevention, and control of norovirus infection (7), an outbreak was defined as 20 or more epidemiologically linked cases occurring in a collective unit within 7 days. A cluster was defined as 3 or more epidemiologically linked cases occurring in a collective unit within 3 days, that did not meet the outbreak criteria. Outbreaks were used as the case group and were matched 1∶2 with clusters as the control group. In this study, a surveillance year started on July 1 and ended on June 30 of the following year. The urban area of Beijing includes Dongcheng, Xicheng, Chaoyang, Haidian, Fengtai, and Shijingshan districts. The suburbs include Changping, Daxing, Shunyi, Tongzhou, Jingkai, Fangshan, Mentougou, Huairou, Miyun, Pinggu, and Yanqing districts.
This study constructed a database using WPS Spreadsheets 2016 (Kingsoft Inc., Beijing, China) and performed statistical analyses using SPSS software (version 19.0, IBM, Chicago, IL, USA). The median, interquartile range (IQR), and composition ratio described the epidemiological characteristics of norovirus clusters and outbreaks. The timeliness of reporting refers to the interval between the onset time of the first case and the reporting time of norovirus clusters or outbreaks. Chi-square tests compared the epidemiological characteristics between norovirus clusters and outbreaks. After case-control matching, risk factors were assessed using univariate conditional logistic regression. Variables with P<0.1 were included in the multivariate conditional logistic regression analyses, and P<0.05 were considered statistically significant.
From July 2017 to June 2022, a total of 1,281 norovirus clusters and outbreaks were reported in Beijing, most of them (92.12%, 1,180/1,281) occurred in primary, secondary, and kindergarten schools, and most (98.56%, 1,163/1,180) were caused by person-to-person transmission. The 1,163 norovirus clusters and outbreaks of person-to-person transmission were included in the study, which involved all 17 districts of Beijing, and 73 (6.28%) of which were outbreaks. The median number of cases per cluster or outbreak was 8 (IQR 5-12), with a maximum of 156 cases. A total of 661 (56.84%) norovirus clusters and outbreaks occurred in kindergartens, and 43.16% (502/1,163) occurred in primary and secondary schools. The majority (82.54%, 960/1,163) were caused by GII genogroup noroviruses, 12.30% (143/1,163) by GI genogroup noroviruses, 2.84% (33/1,163) by co-infection of GI and GII genogroups, 2.15% (25/1,163) by co-infection of noroviruses and other viruses, and 0.17% (2/1,163) by noroviruses of unknown genogroup.
Epidemiological characteristics were compared between norovirus clusters and outbreaks, the timeliness of reporting for both norovirus clusters and outbreaks was 2 (IQR 1-3) days, and there was no significant difference between them (Z=−0.725, P=0.468). Statistically significant differences were found in the proportion by year (July 2017 to June 2022), school type (kindergarten and school), and region (urban and suburban) (Table 1). To exclude the impact of these external factors on norovirus outbreaks in schools and kindergartens, a 1∶2 match was used for occurrence times (every two months), school types, and regions. Seventy outbreaks and 134 clusters were successfully matched.
Characteristics Outbreaks (N=73) Clusters (N=1,090) χ 2 P n (%) n (%) Year 38.244 <0.001 July 2017−June 2018 18 (24.66) 133 (12.20) July 2018−June 2019 35 (47.94) 272 (24.95) July 2019−June 2020 7 (9.59) 125 (11.47) July 2020−June 2021 10 (13.70) 342 (31.38) July 2021−June 2022 3 (4.11) 218 (20.00) School type 30.135 <0.001 Primary and secondary schools 54 (73.97) 448 (41.10) Kindergartens 19 (26.03) 642 (58.90) Region 6.113 0.013 Urban 33 (45.21) 653 (59.91) Suburb 40 (54.79) 437 (40.09) Pathogen type Only norovirus 69 (94.52) 1,069 (98.07) 0.066* Norovirus mixed with other viruses 4 (5.48) 21 (1.93) * Fisher test. Table 1. Comparison of epidemiological characteristics between norovirus outbreaks and clusters in Beijing Municipality, China, July 2017–June 2022.
This study analyzed three types of internal factors in schools and kindergartens: facility conditions, disinfection measures, and the activities of cases (Table 2). Univariate factor conditional logistic regression analysis showed that 7 of the 12 factors were statistically significant (P<0.1): water supply, distance between the first case’s classroom and toilet, daily disinfection concentration, standard handling of vomit, case activity in public areas, vomiting site of the first case, and students vomiting at school or kindergarten. These seven factors were incorporated into a multivariate conditional logistic regression. The results showed that the risk of norovirus outbreaks was 18.63 times higher for students who vomited at school or kindergarten than for students who did not [95% confidence interval (CI): 1.89, 184.10], 3.46 times higher for cases that involved activity in public areas than for cases that involved staying in the classroom or going home on time (95% CI: 1.29, 9.26), and 3.19 times higher for the first case’s classrooms less than 5 meters from toilets than for classrooms more than 5 meters from toilets (95% CI: 1.15, 8.82) (Table 2).
Factors Outbreaks Clusters Univariate analysis Multivariate analysis (N=70) (N=134) OR (95% CI) P OR (95% CI) P Facility conditions Property of schools or kindergartens Public or registered 61 121 Reference Private or unregistered 9 13 1.46 (0.59−3.62) 0.420 Water supply Municipal 62 130 Reference Reference Self-harvesting or others 8 4 3.80 (1.14−12.68) 0.030* 2.68 (0.52−13.79) 0.238 Dining Food delivery or self-catering 15 31 Reference Canteen 55 102 1.12 (0.55−2.18) 0.763 Classroom lighting Non-south or indirect 13 28 Reference South or direct 57 106 1.19 (0.56−2.53) 0.658 Classroom ventilation ≥3 times/day 44 89 Reference <3 times/day 26 45 1.07 (0.52−2.20) 0.854 Distance between the first cases’ classroom and toilet >5 m 31 72 Reference Reference 0−5 m 34 51 2.13 (0.98−4.64) 0.057* 3.19 (1.15−8.82) 0.025† Disinfection measures Daily disinfection concentration ≥500 mg/L 24 66 Reference Reference <500 mg/L 45 64 2.51 (1.27−4.97) 0.008* 1.79 (0.67−4.81) 0.249 Partition usage of cleaning tools Yes 68 132 Reference No 2 2 2.00 (0.28−14.20) 0.488 Standard handling of vomit Yes 36 78 Reference Reference No 30 38 1.84 (0.90−3.75) 0.094* 1.01 (0.40−2.54) 0.983 Activities of cases Cases activity in public areas No 38 88 Reference Reference Yes 32 45 1.70 (0.94−3.08) 0.078* 3.46 (1.29−9.26) 0.014† Vomiting site of the first case Home 26 79 Reference Reference School 44 55 2.37 (1.30−4.32) 0.005* 1.87 (0.80−4.39) 0.151 Students vomiting at school or kindergarten No 5 41 Reference Reference Yes 65 93 7.85 (2.35−26.27) 0.001* 18.63 (1.89−184.10) 0.012† Note: Standard handling of vomit: evacuate students from the vomiting area as soon as possible, open windows for ventilation, wear personal protective equipment, disinfect the vomit with chlorine-containing preparations, and then remove the vomit and clean the floor, and at last, wipe them with clean water. Partition usage of cleaning tools: different tools for classrooms, corridors and toilets. Public area: public classrooms and playgrounds in schools and kindergartens.
Abbreviation: OR=odds ratio; CI=confidence interval.
* P<0.1;
† P<0.05.Table 2. The risk factors for norovirus outbreaks in schools and kindergartens in Beijing Municipality, China, July 2017–June 2022.
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From 2007 to 2021, norovirus outbreaks in China showed an overall increasing trend, with 89.22% occurring in schools and kindergartens (8). Therefore, there is a need to improve prevention and control measures in these settings. Studies on risk factors for norovirus outbreaks conducted outside of China have mostly focused on medical institutions (6). In China, two studies found that school types, region, and hand hygiene can affect the scale of norovirus outbreaks (4–5). However, few studies have focused on various internal factors in schools and kindergartens. This study used conditional logistic regression to analyze the risk factors for norovirus outbreaks and identified several key factors: students vomiting at school or kindergarten, case activity in public areas, and the first case’s classroom less than 5 meters from toilets. Norovirus outbreaks in schools or kindergartens in Beijing appear to be mainly influenced by the activities of cases. Effective measures to address these risk factors can help control norovirus outbreaks in schools and kindergartens.
Norovirus is typically excreted in feces. One study demonstrated that murine norovirus can be aerosolized when toilets are flushed (9). The feces of infected individuals can directly contaminate the environment and produce norovirus aerosols during defecation and flushing. This study found that when the first cases’ classroom was near a toilet, students from nearby classrooms were more likely to contact norovirus aerosols and contaminated environments, increasing their norovirus exposure and accelerating disease spread. Therefore, timely toilet disinfection and ventilation are critical. Vomiting in classrooms, toilets, and corridors can contaminate the surrounding environment and generate norovirus aerosols. Wanwan Sun et al. found that the odds ratio (OR) of norovirus infection among teachers who handled student vomit without respiratory protection was 15.75 times that of teachers without this exposure (10). Therefore, standard vomit disposal is critical for reducing norovirus outbreaks. Patient isolation is an effective means of preventing pathogen spread. If students remain active in common areas of schools and kindergartens after illness onset, more people will be at risk of exposure. Once someone falls ill, immediate isolation measures should be taken until three days after symptom resolution.
This study was subject to some limitations. First, this study only analyzed 12 factors in schools and kindergartens, without incorporating factors such as the timeliness of detection, the standardization of case management and transmission modes. Second, norovirus genotypes were not included in this study. Differences in the transmissibility of different norovirus genotypes may affect the occurrence of norovirus outbreaks.
If a norovirus cluster or outbreak occurs in a school or kindergarten, increasing the frequency of toilet disinfection, ensuring the timely and correct disposal of vomit, and immediately isolating cases will help control its scale, prevent further infection, and reduce the burden of disease.
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No conflicts of interest.
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We thank the staff of the district Center for Disease Prevention and Control in Beijing for performing epidemiological investigation and laboratory detection.
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