SummaryBACKGROUND: Few studies have explored the spread of SARS-CoV-2 in schools in 2021, with the advent of variants of concern. We aimed to examine the evolution of the proportion of seropositive children at schools from June-July 2020 to March-April 2021. We also examined symptoms, under-detection of infections, potential preventive effect of face masks, and reasons for non-participation in the study.
METHODS: Children in lower (7–10 years), middle (8–13 years) and upper (12–17 years) school levels in randomly selected schools and classes in the canton of Zurich, Switzerland, were invited to participate in the prospective cohort study Ciao Corona. Three testing rounds were completed in June-July 2020, October-November 2020 and March-April 2021. From 5230 invited, 2974 children from 275 classes in in 55 schools participated in at least one testing round. We measured SARS-CoV-2 serology in venous blood, and parents filled in questionnaires on sociodemographic information and symptoms.
RESULTS: The proportion of children seropositive for SARS-CoV-2 increased from 1.5% (95% credible interval [CrI] 0.6–2.6%) by June-July 2020, to 6.6% (4.0–8.9%) by October-November, and to 16.4% (12.1–19.5%) by March-April 2021. By March-April 2021, children in upper school level (12.4%; 7.3–16.7%) were less likely to be seropositive than those in middle (19.5%; 14.2–24.4%) or lower school levels (16.0%; 11.0–20.4%). The ratio of PCR-diagnosed to all seropositive children changed from one to 21.7 (by June-July 2020) to one to 3.5 (by March-April 2021). Potential clusters of three or more newly seropositive children were detected in 24 of 119 (20%) classes, 17 from which could be expected by chance. Clustering was not higher than expected by chance in middle and upper school levels. Children in the upper school level, who were wearing face masks at school from November 2020, had a 5.1% (95% confidence interval 9.4% to 0.7%) lower than expected seroprevalence by March-April 2021 than those in middle school level, based on difference-in-differences analysis. Symptoms were reported by 37% of newly seropositive and 16% seronegative children. Fear of blood sampling (64%) was the most frequently reported reason for non-participation.
CONCLUSIONS: Although the proportion of seropositive children increased from 1.5% in June-July 2020 to 16.4% in March-April 2021, few infections were likely associated with potential spread within schools. In March-April 2021, significant clustering of seropositive children within classes was observed only in the lower school level.
Trial Registration: ClinicalTrials.gov NCT04448717
IntroductionIn response to the high incidence of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infections and emerging variants of concern in the autumn and winter of 2020/2021  attendance of schools has been disrupted in many countries. Half of the countries worldwide and in Europe interrupted physical attendance of schools for at least 30 weeks from March 2020 to June 2021 , but this was only for 7 weeks in Switzerland. Nevertheless, by November 2020, only minimal clustering of seropositive children was observed in the canton of Zurich, Switzerland, after 2–3 months of school attendance including 2–6 weeks of high community incidence . Other studies showed that the spread of SARS-CoV-2 infection within schools was not larger than in the surrounding community in 2020, when variants of concern such as Alpha (B.1.1.7) and Delta (B.1.617.2) were not prevalent in most of the countries, and the rates of secondary attack and outbreaks low [4–7]. In contrast, the expected damage caused by school closures could result in worse mental health in children, reduced learning and subsequent income losses, and amplify gender and socioeconomic inequalities within and between countries .
However, only scarce information is available yet on SARS-CoV-2 infection in schools since December 2020, when alpha and subsequently delta variants of SARS-CoV-2 started dominating in Europe and other countries. In Switzerland, approximately 80% of SARS-CoV-2 infections were due to the alpha variant in March 2021 (see appendix 1) . Children below the age of 12 will be the last group to be offered vaccination. Preventive measures in schools will likely need to be adjusted as new variants spread while more people, especially vulnerable populations, become vaccinated. Thus, monitoring the evolution of seroprevalence and clustering of infections within schools remains relevant.
The Ciao Corona study uniquely examines SARS-CoV-2 seroprevalence on the class, school, and district level. The objectives of this study were to assess longitudinally, with measurements in June-July and October-November 2020, and March-April 2021, the proportion of seropositive children and adolescents within school levels, cantonal districts and the region (canton of Zurich), the association of seropositivity with reported symptoms, and the frequency and evolution of clustering of seropositive children within classes in schools. In addition, we examined the potential effect of face masks on the evolution of seroprevalence in upper school level children and reasons for participation and non-participation in this cohort study, in order to address potential participation bias.
Materials and methodsThe protocol  and previous results of this longitudinal study [3, 11] are reported elsewhere. This study is part of the nationally coordinated research network Corona Immunitas . The study follows a cohort of randomly selected schools and classes in the canton of Zurich, Switzerland. The canton has a population of 1.5 million linguistically and ethnically diverse inhabitants in both rural and urban settings, and comprises 18% of the Swiss population .
During the COVID-19 pandemic in Switzerland, physical attendance of schools was interrupted only in March-May 2020. Preventive measures, such as distancing and reduced mixing of classes, were implemented with some variation between schools. All schools required ill children to stay home unless with very mild symptoms. Adults at school were required to wear masks from October 2020, secondary school children from November 2020, and primary school children in the middle school level grades from late January 2021.
School-specific contact tracing was implemented in school year 2020/2021. Testing and quarantine recommendations depended on the specific situation. As a general rule, the whole class was quarantined when two or more infected children were detected in the class simultaneously. If children were wearing masks, only close contacts were quarantined. Daily incidence of diagnosed SARS-CoV-2 cases between October 2020 and April 2021 in the canton of Zurich and Switzerland and the proportion of variants of concern is shown in appendix 1.
Ethics approvalThe study was approved by the Ethics Committee of the Canton of Zurich, Switzerland (2020-01336). All participants provided written informed consent before being enrolled in the study.
PopulationAs described previously [3, 10, 11], in May-June 2020 we randomly selected primary schools in the canton of Zurich and matched the geographically closest secondary school. The number of schools invited in the 12 districts of the canton was proportional to population size.
We randomly selected classes within participating schools, stratified by school level: grades 1 to 2 in lower level (attended by 6-to 9-year-old-children), grades 4 to 5 in middle level (9- to 13-year-old children) and grades 7 to 8 in upper school level (12- to 16-year-old-children); grades were selected from the eligible grades in the school randomly. We aimed to invite at least three classes or at least 40 children in each invited school level of a school (i.e., ensuring that at least 40 children were invited if fewer than three classes were eligible within smaller schools, and a sufficient number of classes so that a total of at least 40 children are invited in schools with small classes). The random invitation of schools and classes ensured that the invited population is approximately representative for the school-aged children within the districts of the canton of Zurich.
Eligible children and adolescents (hereafter referred to as children) of the selected classes could participate in any of the testing rounds. Major exclusion criterion was suspected or confirmed SARS-CoV-2 infection during the testing (precluding child’s attendance of the testing at school).
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