Screening and vaccination against COVID-19 to minimise school closure: a modelling study

Abstract

Background: Schools were closed extensively in 2020-21 to counter SARS-CoV-2 spread, impacting students' education and wellbeing. With highly contagious variants expanding in Europe, safe options to maintain schools open are urgently needed. By estimating school-specific transmissibility, our study evaluates costs and benefits of different protocols for SARS-CoV-2 control at school.

Methods: We developed an agent-based model of SARS-CoV-2 transmission in schools. We used empirical contact data in a primary and a secondary school and data from pilot screenings in 683 schools during the alpha variant (B.1.1.7) wave in March-June, 2021, in France. We fitted the model to observed school prevalence to estimate the school-specific effective reproductive number for the alpha (R^alpha) and delta (B.1.617.2; R^delta) variants and performed a cost-benefit analysis examining different intervention protocols.

Findings: We estimated R^alpha to be 1·40 (95% CI 1·35-1·45) in the primary school and 1·46 (1·41-1·51) in the secondary school during the spring wave, higher than the time-varying reproductive number estimated from community surveillance. Considering the delta variant and vaccination coverage in Europe as of mid-September, 2021, we estimated R^delta to be 1·66 (1·60-1·71) in primary schools and 1·10 (1·06-1·14) in secondary schools. Under these conditions, weekly testing of 75% of unvaccinated students (PCR tests on saliva samples in primary schools and lateral flow tests in secondary schools), in addition to symptom-based testing, would reduce cases by 34% (95% CI 32-36) in primary schools and 36% (35-39) in secondary schools compared with symptom-based testing alone. Insufficient adherence was recorded in pilot screening (median ≤53%). Regular testing would also reduce student-days lost up to 80% compared with reactive class closures. Moderate vaccination coverage in students would still benefit from regular testing for additional control-ie, weekly testing 75% of unvaccinated students would reduce cases compared with symptom-based testing only, by 23% in primary schools when 50% of children are vaccinated.

Interpretation: The COVID-19 pandemic will probably continue to pose a risk to the safe and normal functioning of schools. Extending vaccination coverage in students, complemented by regular testing with good adherence, are essential steps to keep schools open when highly transmissible variants are circulating.

Funding: EU Framework Programme for Research and Innovation Horizon 2020, Horizon Europe Framework Programme, Agence Nationale de la Recherche, ANRS-Maladies Infectieuses Émergentes.

Figure 1

School closure in Europe, empirical contact network features, and field screening data in schools in France (A) Number of in-presence weeks lost by students in European countries because of school closures due to the pandemic. (B) Daily mean number of distinct contacts per individual within the class or between classes; horizontal dashed lines represent the mean class size, which was 23·2 students (SD 1·4) in the primary school and 35·8 (4·1) in the secondary school. (C) Daily mean time that an individual spends in interaction with contacts within the class or in other classes. (D) Daily mean time that a teacher or student spends in interaction with contacts. In panels B–D, histogram bars refer to the empirical networks, and points and error bars (with 95% bootstrap CIs) refer to the synthetic networks. In panels B and C, the increase in average number of contacts and duration in the synthetic secondary school networks compared with their empirical counterparts is due to the ad-hoc addition of contacts between school years. In panel D, no empirical data is shown for teachers in secondary schools as they did not participate in the data collection and their contact behaviour was inferred from another dataset (appendix p 15). (E) Number of schools participating in the pilot screenings during the spring 2021 wave in the Ain, Loire, and Rhône departments. (F) Observed adherence to screening; boxplots represent the median (middle line), IQR (box limits), and 2·5th and 97·5th percentiles (whiskers). (G) Number of schools participating in the pilot screenings and weekly incidence (dotted line) over time from community surveillance in the Ain, Loire, and Rhône departments during the 2021 spring wave; the vertical shaded areas indicate the school closures.

Figure 2

Estimates of R in the school setting during the 2021 spring wave in France due to the alpha variant (A) Estimates of R in primary and secondary schools obtained with the reference and the sensitivity inclusion criteria by fitting the model to pilot screening data; estimates refer to the alpha variant during the 2021 spring wave in France, when reactive closure of classes and facemask mandates were in place, and error bars indicate 95% CIs. (B) Predicted offspring distribution in primary and secondary schools; bold vertical lines indicate R (ie, the average of the distribution) obtained with the reference inclusion criteria. (C) Comparison between the estimate of R for the alpha variant (bold horizontal line; the shaded area corresponds to its 95% CI) and R_t estimated from community surveillance in the Ain, Loire, and Rhône departments during the rise of the 2021 spring wave for primary schools and secondary schools. MLE=maximum likelihood estimate. R=effective reproductive number. R_t=time-varying reproductive number.

Figure 3

Efficiency of regular testing in educational environments (A) Predicted case reduction relative to symptom-based testing alone in primary schools and secondary schools; the reduction is computed on the final epidemic size over 90 days. Error bars correspond to 95% bootstrap CIs (in some cases smaller than the symbol size). The empty marker corresponds to the adherence estimated from empirical data. (B) Probability distribution of the simulated epidemic size over 90 days in the primary school and secondary school for selected protocols (regular testing is performed weekly). C) Probability distribution of the additional number of classes in the primary school and secondary school with at least one active infection when a case is confirmed, for selected protocols (regular testing is performed weekly). In all panels, simulations are parameterised with sustained introductions and the estimated effective reproductive number for the delta variant when reactive class closures and facemask mandates are in place, and accounting for differences in vaccination coverage. *All protocols involve symptom-based testing. †Reactive screening of the class is done on the day after detection of the case, followed by a control screening on day 4 after case identification, with 100% adherence among the non-vaccinated. ‡Regular testing is performed with one test every 1 week (medium-sized circle) or 2 weeks (smallest circle) or two tests per week (largest circle).

Figure 4

Cost–benefit analysis of regular testing in educational environments and the impact of introductions and R (A) Predicted increase in student-days lost relative to symptom-based testing alone. Regular testing is performed weekly. Simulations are parameterised with sustained introductions and the estimated R^delta when reactive class closures and facemask mandates are in place, accounting for differences in vaccination coverage. (B) Predicted case reduction versus predicted increase in student-days lost in the primary school (R 1·46–2·00) and secondary school (R 0·97–1·34) for each protocol relative to symptom-based testing only. Regular testing is performed weekly. Simulations are parameterised with sustained introductions. (C) Predicted case reduction relative to symptom-based testing only for selected protocols (regular testing is performed weekly) as a function of the level of introductions; simulations are parameterised with the estimated R^delta. (D) Predicted case reduction relative to symptom-based testing alone for selected protocols in the primary school and secondary school as a function of R. Regular testing involves weekly screening unless otherwise indicated. Simulations are parameterised with sustained introductions. All protocols involve symptom-based testing. R=effective reproductive number. R^delta=effective reproductive number for the delta variant. *Reactive screening of the class is done on the day after detection of the case, followed by a control screening on day 4 after case identification, with 100% adherence among the non-vaccinated.

Figure 5

Impact of vaccination coverage on case reduction, epidemic size, and student-days lost (A) Predicted case reduction relative to symptom-based testing alone for selected protocols as a function of the vaccination coverage in teachers in the primary school. (B) Predicted case reduction relative to symptom-based testing alone for selected protocols as a function of vaccination coverage in children in the primary school. (C) Predicted case reduction relative to symptom-based testing alone for selected protocols as a function of vaccination coverage inç adolescents in the secondary school. (D) Predicted final epidemic size over 90 days versus vaccination coverage in children in the primary school for selected protocols. (E) Predicted increase in student-days lost relative to symptom-based testing alone for selected protocols as a function of the vaccination coverage in children in the primary school. (F) Minimal vaccination coverage in children above which regular testing with 75% adherence among the non-vaccinated in the primary school has at most a benefit of 20% case reduction, as a function of R. In all panels, simulations are parameterised with sustained introductions, all protocols include symptom-based testing, and regular testing is performed weekly. R=effective reproductive number.