Screening and vaccination towards COVID-19 to minimise faculty closure: a modelling examine

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.

School closure has been extensively used worldwide against the COVID-19 pandemic. The first wave resulted in many countries going into strict lockdowns, closing schools for long periods of time,

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.

COVID-19 outbreaks in schools are difficult to document, as infections in children are mostly asymptomatic or present mild non-specific symptoms.

Despite the lower susceptibility to infections in children than in adults,

viral circulation can occur in school settings, especially in secondary schools.

Accumulating evidence is consistent with increased transmission in the community if schools are open,

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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.

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Keeping schools safely open remains a primary objective that goes beyond educational needs, affecting the social and mental development of children,

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

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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.

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,

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.

Contact networks measured through wearable sensors displayed a strong community structure around the classes, common to both the primary and secondary schools (appendix p 14). The patterns of interaction, however, varied substantially between the two settings. On average, children had a larger number of distinct contacts during a day than adolescents, interacting with almost their entire class (83% vs 33% of the class, Student’s t-test pfigure 1B). Approximately 50% more links occurred between classes than within classes in the primary school (28 vs 19 links, pvs 12 links, pfigure 1C) and established longer contacts than teachers (64% longer, p=0·009; figure 1D).

Using the empirical contact patterns, we inferred the school-specific transmissibility from screening data in primary schools that satisfied the inclusion criteria: 71 primary schools with 12 146 tested students met the reference inclusion criteria, and 103 primary schools with 15 916 tested students met the sensitivity inclusion criteria. Secondary schools were excluded because of limited participation, but with βMLE we could estimate the within-school Ralpha both in the primary school and in the secondary school. We estimated that Ralpha during the 2021 spring wave of the alpha variant in France when reactive class closures and facemask mandates were in place was 1·40 (95% CI 1·35–1·45) in primary schools that met the reference inclusion criteria, 1·44 (1·40–1·48) in primary schools that met the sensitivity inclusion criteria, 1·46 (1·41–1·51) in secondary schools that met the reference inclusion criteria, and 1·50 (1·46–1·54) in secondary schools that met the sensitivity inclusion criteria (figure 2A). Estimates were higher than the Rt obtained from age-specific community surveillance in the same period (one-sample t-test pfigure 2C). We quantified a large individual-level variation in SARS-CoV-2 transmission in both schools, corresponding to an estimated overdispersion parameter k of 0·56 (95% CI 0·49–0·63) in the primary school and 0·52 (0·46–0·58) in the secondary school (figure 2B). Accounting for the transmissibility advantage of the delta variant and vaccination coverage in Europe, we estimated a school-specific Rdelta of 1·66 (95% CI 1·60–1·71) for primary schools that met the reference inclusion criteria, 1·70 (1·66–1·75) for primary schools that met the sensitivity inclusion criteria, 1·10 (1·06–1·14) for secondary schools that met the reference inclusion criteria, and 1·13 (1·10–1·16) in secondary schools that met the sensitivity inclusion criteria. In the analysis of closure and screening protocols, we used the Rdelta estimate obtained with the reference inclusion criteria, and explored ranges for Rdelta of 1·46–2·00 in primary schools and 0·97–1·34 in secondary schools to account for the uncertainty associated with delta transmissibility, seasonal effects, and sensitivity inclusion criteria.

Under the estimated delta transmissibility and with sustained introductions, regular testing constitutes an efficient protocol for preventing infections in a partially immunised school population (figure 3A). If adherence among the non-vaccinated is large enough, regular testing can substantially outperform protocols based on simply identifying cases given recognisable symptoms and additionally closing or screening the class of the detected case (even with a follow-up control screening). However, screenings at schools during the 2021 spring wave in France were met with low or moderate participation rates. Adherence was higher in lower school levels (39% [IQR 26–49] in pre-school and 53% [43–65] in primary school) than in secondary schools (10% [5–17] in middle school and 6% [3–10] in high school; Mood’s median test pfigure 1F). We found that with 50% adherence among the non-vaccinated—ie, approximately the value recorded in the French primary schools—weekly screening would reduce the number of cases by 21% (95% CI 19–23) in primary schools and 26% (24–28) in secondary schools compared with symptom-based testing alone. Case reduction would rise to 34% (32–36) and 36% (35–39) in primary and secondary schools, respectively, with 75% adherence. Alternatively, similar reductions would be achieved with 50% adherence and twice-weekly testing. These data show how infection prevention improves with both adherence and frequency of tests, and higher frequency is needed to compensate for lower adherence. However, if adherence to regular testing is too low (10%), as recorded in the French secondary schools, weekly testing would have little impact (figure 3B; appendix p 41).

As well as reducing the number of infections, regular testing is predicted to strongly limit the number of days of absence of students. Quarantine of the class leads to 17·7 (95% CI 17·4–17·9) and 32·6 (31·9–33·5) times more student-days lost in primary and secondary schools, respectively, than when symptom-based testing is used alone (figure 4A). Days lost inevitably increase when reactive closure is extended to classes of the same level or specialisation. Not being sufficiently targeted, reactive closure quarantines individuals while their risk of infection might be low, and the virus might have spread to other classes (figure 3C). Reducing mixing across classes through cohorting improves control (appendix p 44). Despite detecting more cases, regular testing leads to a small increase in student-days lost, less than 6·6 (6·4–6·8) times the number of days lost with the basic strategy and about 63–80% less than reactive class closure as isolation is applied only to detected cases. The cost–benefit analysis shows that for all regular testing strategies, the cost expressed as student-days lost remains low, even when the benefit becomes high, for a range of different epidemic conditions (figure 4B). Strategies based on class closures do not reach substantial benefit, even at large costs. Reactive screening limits days lost but with a negligible impact on viral circulation. Closing the class at each case detected by regular testing improves case reduction but at the cost of increased absence from school (appendix p 43). Findings were robust to changes in detection rates and test sensitivity (appendix pp 51–52).

Higher incidence in the community (increasing the expected introductions at school) and larger values for R (increasing within-school transmission) reduce the benefit of weekly testing in primary schools, thus requiring increased adherence or frequency (figure 4C,D). The impact of introductions is milder in the secondary school than in the primary school due to vaccination of adolescents (figure 4D). Moreover, increasing R in this setting would increase the benefit of regular testing, contrary to the primary school case. This is due to a bell-shaped dependence of the infection prevention capacity of regular testing versus R (appendix p 46): in low-transmission conditions, only a few cases are present even under the scenario of symptom-based testing and case isolation, so that additional protocols yield marginal benefit; as transmission increases from small values (the secondary school case, where R is small thanks to vaccination), efficiency increases. In high-transmission conditions, case prevention is hindered by too many infections generated between successive screenings, and efficiency decreases as transmission increases (the primary school case, with high R because of unvaccinated children). Changes in epidemiological parameters (transmissibility and susceptibility) yield changes in R and consequently in protocols’ efficiencies, but protocols’ ranking according to their benefit remains robust (appendix pp 48–50). High-incidence conditions due to immune evasion and higher transmissibility, compatible with an omicron scenario, confirm the value of screening with high frequency (appendix p 37).

Benefits and costs of regular testing remain stable when vaccination coverage of teachers increases from 60% to 100% (figure 5A; appendix pp 41). Increasing vaccination coverage in students, both in primary and secondary schools, is a strong protective factor against school outbreaks (figure 5B–D), and compared with no vaccination, is expected to reduce the epidemic size by 38% (95% CI 36–40) with 20% coverage and by 75% (74–76) with 50% coverage in children under the basic protocol, considering vaccine effectiveness before waning occurs with time (figure 5D, appendix p 40). Regular testing would provide an important supplementary control, especially while rolling out vaccination campaigns in primary schools: weekly screening 75% of non-vaccinated students would additionally reduce cases compared with the basic protocol by 36% (95% CI 32–39) with 20% vaccination coverage in children, and by 23% (20–26) with 50% coverage, without impacting student-days lost (figure 5E). Similar results are obtained with lower vaccine effectiveness (appendix p 54). The minimum vaccination coverage to reduce the benefit of regular testing to 20% case reduction or below increases with R; for R between 1·6 and 2·0, the required coverage stabilises at around 55–60% (figure 5F).

Strategies to safely keep schools open during the COVID-19 pandemic are a matter of controversial debate, and knowledge from the field is scarce. Using screening data from schools during the 2021 spring wave in France and empirical contact data, our study provides the first estimate of SARS-CoV-2 transmissibility in different school settings, suggesting that contacts at school increase SARS-CoV-2 transmission potential compared with transmission in the community. With countries in Europe experiencing record-high cases due to the omicron variant,

protocols at school remain a central issue as high community transmission leaves schools vulnerable and vaccination of children progresses slowly in most countries.

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.

We estimated a higher transmissibility in the school than in the community during the 2021 spring wave of the alpha variant in France. This finding suggests that repeated contacts in dense classrooms, even with facemask mandates in place, except for during sport and at lunch, favour transmission in the absence of screening protocols, with potentially high overdispersion.

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These findings align with available evidence of increased transmission in the population if schools are open.

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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,

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,

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a higher risk of infection for students’ household members,

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.

Using the estimated school-specific transmission rate for delta and a range of realistic epidemic conditions (with regard to introductions, seasonality, and vaccination coverage), we found that regular testing with large enough adherence provides an optimal balance in controlling school outbreaks while maintaining schools open. This finding is consistent with results showing that twice-weekly testing in England helped to control within-school transmission in secondary schools.

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.

Our findings corroborate previous numerical evidence on the value of regular testing in preventing infections.

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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.

Reactive class closure is highly costly in terms of student-days lost, even though detecting a case is rarer in children than in adults. Countries adopting this strategy during the omicron wave registered record-high absenteeism from school (20% of students were in remote learning in Italy in January, 2022

). 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.

Our analysis on the omicron wave (appendix p 37) confirms the large benefit of regularly screening students compared with reactive strategies, even when these strategies are strengthened, for example, by increasing the number of reactive screenings following the index case. The reinforced reactive protocol adopted in France at the reopening of schools in January, 2022, required three screenings to be performed at days 0, 2, and 4 from detection. But under the high omicron incidence experienced at the start of 2022, this protocol led to an unprecedented demand in tests, impacting logistics, available resources, and surveillance capacity.

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.

Increasing vaccination in teachers protects them from infection and symptomatic disease

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,

and an indirect impact on the community, protecting students’ contacts.