Summary
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 (Ralpha) and delta (B.1.617.2; Rdelta) variants and performed a cost–benefit analysis examining different intervention protocols.
Findings
We estimated Ralpha 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 Rdelta 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.
Introduction
Education: from disruption to recovery.
and their reopening has been continuously challenged by successive waves and the need for physical-distancing restrictions. In Europe, depending on the country, students lost from 10 weeks to almost 50 weeks of school from March, 2020, to October, 2021, due to partial or total school closures (figure 1A). Strategies were affected by the limited understanding of viral circulation in children and their contribution to transmission.
- Goldstein E
- Lipsitch M
- Cevik M
Figure 1School closure in Europe, empirical contact network features, and field screening data in schools in France
Education: from disruption to recovery.
(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.
- Han MS
- Choi EH
- Chang SH
- et al.
Despite the lower susceptibility to infections in children than in adults,
- Viner RM
- Mytton OT
- Bonell C
- et al.
viral circulation can occur in school settings, especially in secondary schools.
- Goldstein E
- Lipsitch M
- Cevik M
Accumulating evidence is consistent with increased transmission in the community if schools are open,
- Goldstein E
- Lipsitch M
- Cevik M
,
- Li Y
- Campbell H
- Kulkarni D
- et al.
and model-based findings suggest that school closure might be used as an additional brake against the COVID-19 pandemic if other physical-distancing options are exhausted or undesired.
- Rozhnova G
- van Dorp CH
- Bruijning-Verhagen P
- et al.
,
- Di Domenico L
- Pullano G
- Sabbatini CE
- Boëlle P-Y
- Colizza V
as well as reducing inequality. Several countries implemented safety protocols at schools, including the use of facemasks, hand hygiene, and staggered arrival and breaks. Regular testing
- Paltiel AD
- Zheng A
- Walensky RP
,
- Bergstrom T
- Bergstrom CT
- Li H
,
- Lasser J
- Sorger J
- Richter L
- Thurner S
- Schmid D
- Klimek P
,
- Leng T
- Hill EM
- Holmes A
- et al.
was introduced in a few countries as an additional control measure. Vaccination was extended to the population aged 5 years and older in Europe, yet it was reported to have progressed slowly in the majority of countries as of January, 2022.
Data on COVID-19 vaccination in the EU/EEA.
School protocols were challenged by the rapid surge of cases due to the delta (B.1.617.2) and omicron (B.1.1.529) variants in the 2021–22 winter season in Europe,
Assessment of the further spread and potential impact of the SARS-CoV-2 omicron variant of concern in the EU/EEA, 19th update.
threatening classroom safety. Assessing vaccination and protocols in schools is therefore key to maintaining schools open in light of a continuously evolving pandemic. Here, through an agent-based transmission model parameterised on empirical contacts at schools and fitted to field screening data in schools, we estimated the school-specific effective reproductive number (R) of SARS-CoV-2. We then evaluated intervention protocols combining school closures and screening, under varying immunity profiles of the school population, and accounting for age-specific differences in susceptibility to infection, contagiousness, contact patterns, and vaccine effectiveness.
Evidence before this study
We searched PubMed, medRxiv, bioRxiv, and arXiv for articles in English published up to Dec 3, 2021, which had, in the title or abstract, the terms “COVID-19”, “testing”, and “schools”. We found a total of 271 unique articles. 57 works were modelling papers on the spread of COVID-19, and of these 31 (54%) implemented agent-based models. However, very few integrated information from empirical contacts or considered the cost of school closures in terms of school-days lost by students. No study addressed the role of vaccination in children in the school setting or the interplay of adherence to screening with frequency of screening. Modelling studies reached a consensus on the fact that test turnaround time is more important than test sensitivity for efficient testing strategies.
Added value of this study
Governments around the world proposed school closures as a first measure to slow down viral spread; however, the need to safely keep schools open is arguably a primary objective for educational, mental health, and socioeconomic reasons. Using empirical contact data collected in a primary school and a secondary school and data on test results collected in pilot screenings during the 2021 spring wave of the alpha variant in France, we estimated the effective reproductive number specific to each school setting in that period and showed that transmission was higher in schools than in the community. Accounting for the transmission advantage of the delta variant and vaccination coverage in Europe as of mid-September, 2021, we showed the need for regularly testing a partly immunised school population to reduce the number of cases while limiting the number of student-days lost. In particular, we highlighted the importance of adherence to screening, showing that higher screening frequency is needed to compensate for lower adherence. Model estimates indicate that the low levels of adherence recorded in pilot screenings during the third wave would be insufficient to control viral circulation in the school population. Increasing vaccination coverage in teachers did not impact potential outbreaks, mainly due to the large mixing among students. Regular testing would still provide a key benefit in decreasing viral circulation in a moderately vaccinated student population, or under waned protection against infection, and it would be especially important under the high-incidence conditions observed in the omicron wave.
Implications of all the available evidence
By studying different epidemic contexts and vaccination conditions, we provided a range of alternatives to school closure, to be implemented according to the epidemic activity and the reported adherence. These strategies become particularly important as the safety and normal functioning of classrooms are threatened by high community transmission rates. These results can inform national education systems to safely keep schools open while avoiding unnecessary closures.
Findings from this work informed the recommendations of the French National Immunisation Technical Advisory Group (Haute Autorité de Santé) on vaccination of children in December, 2021.
Results
Figure 2Estimates 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 Rt 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. Rt=time-varying reproductive number.
Figure 3Efficiency 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 4Cost–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 Rdelta 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 Rdelta. (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. Rdelta=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 5Impact 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.
Discussion
Assessment of the further spread and potential impact of the SARS-CoV-2 omicron variant of concern in the EU/EEA, 19th update.
protocols at school remain a central issue as high community transmission leaves schools vulnerable and vaccination of children progresses slowly in most countries.
Data on COVID-19 vaccination in the EU/EEA.
Our analysis indicates that regularly screening the school population is efficient in preventing infections while reducing absence from school, especially in settings where the school population is not yet vaccinated, coverage is low to moderate, or vaccine protection has largely waned.
- Adam DC
- Wu P
- Wong JY
- et al.
,
These findings align with available evidence of increased transmission in the population if schools are open.
- Goldstein E
- Lipsitch M
- Cevik M
,
- Li Y
- Campbell H
- Kulkarni D
- et al.
In the absence of vaccination, secondary school students are predicted to infect on average a larger number of individuals than primary school students, consistent with previous observations,
- Goldstein E
- Lipsitch M
- Cevik M
due to age-specific epidemiological properties and contact patterns. However, more contagious variants and limited vaccination coverage in children currently put them at higher risk compared with the rest of the population, which is partially protected by vaccination. A disproportionately higher omicron circulation has been observed in children than in the general population (5500 cases per 100 000 children aged 6–10 years vs 3000 per 100 000 population in all age classes in France by mid-January, 2022) that is further sustained by transmission at school, resulting in large school disruption,
,
- Morin V
- Battaglia M
- Rof G
- et al.
a higher risk of infection for students’ household members,
- Grant R
- Charmet T
- Schaeffer L
- et al.
and rapid transmission in the community.
Even when conditions due to the circulating variant and vaccination coverage bring the school-specific R to below 1 (eg, as estimated under a delta wave in secondary schools in France with 77% vaccinated adolescents and high vaccine effectiveness; appendix pp 35–36), the predicted highly overdispersed offspring distribution suggests that, together with highly likely extinctions, chains of transmissions in schools are relatively rare but possible.
- Leng T
- Hill EM
- Holmes A
- et al.
Adherence is, however, critical, suggesting that at least three-quarters of non-vaccinated individuals should participate in weekly testing to achieve a considerable case reduction. This level of adherence was not achieved in the pilot screenings in early 2021 in France. Implementing regular testing should consider improving strategies for the communication and engagement of the school community to considerably boost participation and maintain it over time.
- Paltiel AD
- Zheng A
- Walensky RP
,
- Bergstrom T
- Bergstrom CT
- Li H
,
- Lasser J
- Sorger J
- Richter L
- Thurner S
- Schmid D
- Klimek P
Our study adds to previous work by estimating the school-specific R in primary and secondary schools and integrating empirical face-to-face proximity data, allowing us to quantify individual-level variation in SARS-CoV-2 transmission. It also provides a cost–benefit analysis considering successive variants, comparing multiple protocols, and evaluating the key role of adherence in the context of partly vaccinated school populations.
). It also has a limited value in epidemic control, as other classes might be already affected due to unobserved introductions from the community or silent spreading within the school. The effect of silent spreading becomes particularly important when between-classes mixing is higher, as observed in the primary school. Cohorting that reduces contacts between classes is therefore an important component of school protocols, in support to screening. While regular testing detects more cases than symptom-based detection, it keeps days lost low for two main reasons. First, isolation is only applied to cases during their infectious period, being therefore more targeted than class quarantine. Second, detecting cases that otherwise go unnoticed helps control the epidemic, breaking the chains of transmission and preventing further diffusion. As a consequence, the overall time spent in isolation is also reduced. Reactive screening, instead, would leave many cases undetected even when retesting a few days after. The iterative nature of regular testing is key to ensure control over time.
- Morin V
- Battaglia M
- Rof G
- et al.
Our findings support instead strengthening regular screening by increasing adherence and adjusting frequency to local incidence and policy expectations, next to cohorting, facemask use, and ventilation.
- Tartof SY
- Slezak JM
- Fischer H
- et al.
but yields limited protection for the school population, even under full coverage. This results from the small number of teachers and the observed lower rate of interaction they have with students, and it is confirmed even when community incidence in adults is much higher than in the student-age classes. Extending vaccination to students is needed to achieve a collective benefit, reducing the likelihood and size of school outbreaks with active vaccination protection. In these conditions, regular testing would bring a supplementary control whose application should be evaluated in light of resources, logistics, adherence, epidemic conditions, and waning of vaccine effectiveness. Regular testing remains, however, critical in moderate (or lower) coverage situations, or when protection against infection has waned, as it would prevent a substantial proportion of undetected infections, having a direct impact on the school environment, reducing the number of infections and long-COVID in children,
Prevalence of ongoing symptoms following coronavirus (COVID-19) infection in the UK: 1 April 2021.
and an indirect impact on the community, protecting students’ contacts.
- Grant R
- Charmet T
- Schaeffer L
- et al.
This study has limitations. First, it focuses on two school settings for which empirical contact data were available, but contacts in other schools might be different, depending on the structure of curricula and the organisation of activities. Findings on the efficiency of regular testing and vaccination are, however, robust across a range of epidemic conditions and synthetic contact patterns and can thus inform on the choice of strategies to safely keep schools open. Second, data availability for the inference was limited by the pilot screening. Further work could also focus on the downward phase of the alpha wave. Third, the study focuses on school outbreaks and it does not assess the impact that these strategies will have on the viral circulation in the community. Fourth, we did not model waning of vaccine effectiveness throughout the epidemic wave but tested lower effectiveness values that confirmed the efficiency of regular testing.
The COVID-19 pandemic will probably continue to pose a risk to the safe and normal functioning of schools. Regular testing remains a key strategy to epidemic control in school settings with moderate vaccination coverage or following waned vaccine protection, all the while minimising days lost.
VC and AB conceived and designed the study. EC, GB, and VC accessed and verified all the data and were responsible for the decision to submit for publication. EC, GB, DAC, and CP analysed the data. EC, GB, P-YB, and VC developed the inference framework. EC and DAC developed the code. EC and GB performed the numerical simulations and analysed the results. All authors interpreted the results. VC wrote the Article. All authors contributed to and approved the final version of the Article.
Acknowledgments
We thank Assistance Publique–Hôpitaux de Paris, Santé publique France, Niel Hens, Pieter Libin, Julia Bielicki, Pascal Crepey, and Raphaëlle Métras for useful discussions; Philippe Vanhems, Elisabeth Bothello-Nevers, Olivier Epaulard, Jean Beytout, Annabelle Ravni, Olivier Dugrip, and the Academie of the Auvergne-Rhône-Alpes region for the school screening initiatives; and the Ministry of National Education for supporting the surveillance activities. This study was partly funded by Agence Nationale de la Recherche projects COSCREEN (ANR-21-CO16-0005) and DATAREDUX (ANR-19-CE46-0008-03), ANRS–Maladies Infectieuses Émergentes project EMERGEN (ANRS0151), EU Horizon 2020 grants MOOD (H2020-874850; paper MOOD 037) and RECOVER (H2020-101003589), Horizon Europe grant VERDI (101045989), and REACTing COVID-19 grant.