A cross-sectional and prospective cohort study of the role of schools in the SARS-CoV-2 second wave in Italy

Abstract

Background: During COVID-19 pandemic, school closure has been mandated in analogy to its effect against influenza, but it is unclear whether schools are early COVID-19 amplifiers.

Methods: We performed a cross-sectional and prospective cohort study in Italy during the second COVID-19 wave (from September 30, 2020 until at least February 28, 2021). We used databases from the Italian Ministry of Education, the Veneto region systems of SARS-CoV-2 cases notification and of schools' secondary cases tracing to compare SARS-CoV-2 incidence in students/school staff and general population and incidence across age groups. Number of tests, secondary infections by type of index case and ratio cases/ tests per school were estimated using an adjusted multivariable generalized linear regression model. Regional reproduction numbers R_t were estimated from Italian Civil Protection daily incidence data with a method of posterior distribution using a Markov Chain Monte Carlo algorithm.

Findings: SARS-CoV-2 incidence among students was lower than in the general population. Secondary infections at school were <1%, and clusters of ≥2 secondary cases occurred in 5-7% of the analysed schools. Incidence among teachers was comparable to the population of similar age (P = 0.23). Secondary infections among teachers were rare, occurring more frequently when the index case was a teacher than a student (37% vs. 10%, P = 0.007). Before and around the date of school opening in Veneto, SARS-CoV-2 incidence grew maximally in 20-29- and 45-49-years old individuals, not among students. The lag between school opening dates in Italian regions and the increase in the regional COVID-19 R_t was not uniform. Finally, school closures in two regions where they were implemented before other measures did not affect R_t decrease.

Interpretation: This analysis does not support a role for school opening as a driver of the second COVID-19 wave in Italy, a large European country with high SARS-CoV-2 incidence.

Funding: Fondazione MITE.

Fig. 1

Incidence of SARS-CoV-2 is lower among students than in the general population. Bubble graphs of SARS-CoV-2 incidence between September 12 and November 7 among 6–13 years old (A) and 14–18 years old (B) students and among teaching and non-teaching staff members (C) in Italian regions and autonomous provinces compared to the incidence in the general population. Size of bubbles is proportional to the measured incidence in the analysed school populations. The 45° line indicates equivalence between general population and school population incidence. Bubbles are color-coded in a green-yellow-red gradient proportional to the value of the ratio between the analysed population and the general population. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 2

Increases in R_t are not univocally correlated with school opening times in different Italian territories. Pairwise comparison of median R_t in the indicated 7 days periods (±5–95% Credible Intervals) in the provinces of Bolzano and Trento (A) and in the indicated regions (B-D). The periods of school opening are highlighted by a box shaded in the same color of the respective province or region.

Fig. 3

Increases in R_t are not univocally correlated with school opening times across Italian regions. Box plots of the indicated quantiles for the days of delay between school openings (A) and September 20–21 national election day (B) and R_t increase in Italian regions clustered by their school opening dates. Date of R_t increase was calculated as the first day of the period when median R_t started an increase sustained in time (>3 consecutives periods).

Fig. 4

During the second COVID-19 wave incidence of SARS-CoV-2 rises initially among young adults and 45–49 years old individuals in Veneto region. (A, B) Daily incidence and 7 days adjacent average (7DMA) of SARS-CoV-2 positivity among individuals of the indicated age range. Consistency of the population in each age bracket was from ISTAT and is detailed in Table 6. (C) Heatmap of weekly incidence of SarsCoV2 in individuals of the indicated age ranges in the Veneto region during the indicated timeframe. The color scale goes from green (low incidence) to beige (medium incidence) and to red (high incidence). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 5

School closures do not affect R_t decrease in Lombardy and Campania. (A, C) Median R_t in the indicated 7 days periods (±5–95% Credible Intervals) in Lombardy (A) and Campania (C). Days of school opening and closure are indicated. (B, D) First order derivative of R_t in Lombardy (B) and Campania (D). Days of school opening and closure are indicated.