Impact of vaccination against SARS-CoV-2 on the incidence of infection in school settings

Abstract

Background

The SARS-CoV-2 pandemic affected the school-aged population because of the disease itself and due to the measures applied for prevention and control of the infection. The aim of the study was to evaluate the effect of population-based vaccination against COVID-19 on the incidence of infection in school settings.

Material and methods

A retrospective descriptive study of COVID-19 cases and school outbreaks was carried out at the province level. Students, teachers and staff from different educational stages of the schools were included. The outcome measure was the incidence according to educational stage, case profile and clinic during the first of the academic year 2020/2021 versus the same period 2021/2022.

Results

The total incidence of SARS-CoV-2 in classrooms was 2470 cases per 100,000 population in the first trimester of the academic year 2020/2021 and 2720 cases per 100,000 population in the same period 2021/2022. The number of reported school outbreaks was 7 times higher in this second period; and the risk of infection in classrooms over 12 years of age (students and teachers) was reduced by 43.1% (vaccinated in high percentage).

Conclusions

This study shows a reduction in transmission of SARS-CoV-2 infection in students of higher educational stages (secondary and high school) during the first of the academic year 2021/2022 (group with high vaccination coverage at the beginning of the period) compared to the previous school year (without vaccination).

Resumen

Antecedentes

La pandemia por SARS-CoV-2 afectó a la población en edad escolar debido a la propia enfermedad y, al mismo tiempo, por las medidas aplicadas de prevención y control de la infección. El objetivo del estudio fue evaluar el efecto de la vacunación poblacional contra COVID-19 en la incidencia de infección en ámbito escolar

Materiales y métodos

Se realizó un estudio descriptivo retrospectivo de casos y brotes escolares por COVID-19 a nivel provincial. Se incluyó alumnado, docentes y personal de diferentes etapas educativas de los centros. La medida principal de resultados fue la incidencia acumulada en función de etapa educativa, perfil del caso y clínica durante el primer trimestre del curso 2020/2021 frente al mismo periodo 2021/2022.

Resultados

La incidencia total de infección por SARS-CoV-2 en las aulas fue de 2.470 casos por cada 100.000 habitantes en el primer trimestre del curso 2020/2021 y de 2.720 casos por cada 100.000 habitantes en el mismo periodo 2021/2022. El número de brotes escolares notificados fue 7 veces mayor en este segundo periodo; y, al mismo tiempo, el riesgo de infección en las aulas de mayores de 12 años (alumnos y docentes) se redujo un 43,1% (vacunados en elevado porcentaje).

Conclusiones

Este estudio muestra menor transmisión de infección por SARS-CoV-2 en los alumnos de las etapas educativas superiores (Secundaria y Bachillerato) durante el primer trimestre escolar 2021/2022 (grupo con elevada cobertura vacunal al inicio del período) respecto al curso previo (sin vacunación).

Introduction

The school population has been affected by the severe acute respiratory syndrome type 2 (SARS-CoV-2) coronavirus pandemic, not only directly by the disease itself, but also through the implementation of infection prevention and control measures, with physical, mental, and educational repercussions.¹ The negative effect on well-being and mental health due to school closures has been reflected in a systematic review with data from 20 countries.²

In Spain, the incidence of COVID-19 infection over these 2 years was very variable. The type of variant circulating and the age groups affected also varied. The initial SARS-CoV-2 lineage was circulating during the first trimester of the 2020/2021 school year, and children were considered less susceptible to infection.³ In contrast, in the first school trimester 2021/2022, the emergence of the delta lineage variant (B.1.617.2 and AY subvariants) with higher transmission capacity resulted in higher incidences in the group of children aged 5 to 12 years. The susceptibility of the paediatric population to SARS-CoV-2 infection was comparable to that of other age groups. However, the severity of the disease is low in children under 18 years of age, in terms of hospitalisation and case fatality.⁴

The reopening of schools after the closure during the first wave of the pandemic made it possible to evaluate the transmission of SARS-CoV-2 infection in school settings. Several published studies have shown a lower level of COVID-19 transmission in schools compared to the family or social setting, after applying the recommended infection response measures.^5-7

Vaccination is the best available preventive tool against severe symptomatic COVID-19 disease.^8-10 Vaccination in Spain started on 27 December 2020 in accordance with the recommendations of the Vaccination Strategy,¹¹ and teachers, school staff, and children aged 12–19 years had access to vaccination prior to the start of the 2021/2022 school year. This national immunisation programme provided vaccination coverage of 89.7% in the population aged 12 years and over as of 22 December 2021 (end of the school trimester).¹²

Despite the proven effectiveness of immunisation against COVID-19 against the severity and fatality of the infection, vaccine efficacy in reducing the number of cases has been highly questioned. Therefore, we believe it appropriate to assess the effect of population-based vaccination on the incidence of SARS-CoV-2 infection in the school setting, the representative population with and without access to vaccination, by age and time period.

Objectives

Primary objective: to assess the impact of population-based vaccination against SARS-CoV-2 on infection in the school setting at provincial level.

Secondary objectives: to analyse COVID-19 infection (cases and outbreaks) in the school setting according to educational stage, profile (pupil/teacher/staff), and case symptomatology. To describe the differences in incidence in schools in the first trimester of the 2020/2021 school year compared to the same period 2021/2022, and to analyse the vaccination status of confirmed cases of SARS-CoV-2 infection among pupils, teachers, and school staff.

Material and methods

We conducted a retrospective descriptive observational epidemiological study of school cases and outbreaks of COVID-19 infection in the province of Valladolid. The study included pupils, teachers, and staff in the second cycle of infant, primary, secondary, and baccalaureate stages in public, state-subsidised, and private schools. The first trimester of the 2021/2022 school year (10 September 2021 to 22 December 2021) was evaluated compared to the first trimester of the 2020/2021 school year (9 September 2020 to 22 December 2020).

Case, outbreak, and close contact were defined according to the Action Guide for the onset of cases of COVID-19 in schools¹³ at regional level (asymptomatic or symptomatic case with positive diagnostic test for active infection [PDIA] and attendance at the school within the last 48 h from the onset of symptoms or the date of PDIA [invalid self-test]; outbreak as a grouping of 3 or more cases with active infection with an epidemiological link established in the last 10–14 days). And, in the educational stages, the 2nd cycle of infant education and the 1st year of primary education were considered a joint school group because they were exempt from wearing masks (GSM), following the definitions of the protocol in force in Castilla y León,¹³ which grouped these educational levels into a single subgroup with specific prevention and control measures because they were allowed not to wear masks and due to their greater social interaction. During this study, the prevention measures of social distancing, hand hygiene, masks, and ventilation in enclosed spaces were applied in the schools; together with the mitigation measures of close school contact tracing for confirmed cases with PDIA, following the protocol and applying quarantine for 10 days (14 days in the 2020/2021 school year) from the last contact with a confirmed GSM case and in the case of a non-GSM (not exempt from mask wearing) outbreak (in the 2020/2021 school year, quarantine was applied to all close contacts in non-GSM classrooms; however, in the 2021/2022 school year, it was applied only to unvaccinated or vulnerable close contacts).¹³

During the study period, vaccination in Spain included groups 6B and 6C (teachers and school staff) and group 13 (persons aged 12–19 years, born between 2002 and 2009 inclusively) following Spain's COVID-19 vaccination strategies.¹¹ The immunisation schedule (full, partial, and unvaccinated) was defined according to the current state strategy for primary vaccination, following the recommendations and the technical data sheet of the vaccines according to age, vaccine preparation, number of doses, and intervals between doses.

Data sources: a separate register was created in the Epidemiological Surveillance System of the Epidemiology Section of the Territorial Health Service of Valladolid with the notification of confirmed cases, contacts, and outbreaks identified by the COVID-19 team of the Provincial Directorate of Education. It was extended with the collection of clinical information on the cases through the primary care and hospital care systems of the public and private network of the province and the Epidemiological Surveillance Information System of Castilla y León. Vaccination against COVID-19 was collected from the VACU vaccine module registry. Data on cumulative incidence and population vaccination coverage in the province were extracted through the “Datos Abiertos” (Open Data) portal of Castilla y León¹⁴ and taking the data collected by the National Institute of Statistics as the estimated reference population for the province of Valladolid.¹⁵

Outcome measures: the main outcome measure was the calculation of the cumulative incidence of SARS-CoV-2 infection in schools in the first trimester of the academic year 2020/2021 and the same period in 2021/2022. It was then disaggregated according to the profile of the case in classrooms (pupil or teacher) and educational stage (2nd cycle infant with 1st year of primary school, 2nd to 6th year of primary school, secondary school, and baccalaureate), comparing both periods. In addition, cases and outbreaks of coronavirus infection were characterised and the vaccination status (unvaccinated, partial, or full schedule) was analysed with respect to the primary vaccination of COVID-19 cases in the 2021/2022 school year in students over 12 years of age, teachers, and school staff.

Analysis of outcomes: the association of qualitative variables was analysed by comparing proportions of independent samples using Pearson's χ² test. Fisher's exact test or the likelihood ratio test was used for variables with more than 2 categories if the number of cells with expected values less than 5 was greater than 20%. P-values < .05 were considered statistically significant. We used the statistical programmes SPSS version 15.0.1 (SPSS Inc., Chicago, USA) and EPIDAT version 4.2 (EPIDAT, Spain).

This study was approved by the Valladolid West Area Drug Research Ethics Committee.

Results

A total of 1911 cases of active SARS-CoV-2 infection were reported in the school setting during the first quarter of the academic year 2020/2021 and 2010 cases during the same period in 2021/2022. The distribution by sex and case profile (pupil, teacher, and staff) was homogeneous in both periods, as was the proportion of cases with clinical symptoms (n = 943; 61.7% vs. n = 1254; 59.4%). Table 1 presents the general characteristics of cases and outbreaks in both periods.

Table 1.

General characteristics of school cases and outbreaks of COVID-19 infection during the first quarter of the school year 2020/2021 and 2021/2022.

	School year 2020/2021	School year 2021/2022
Total number of cases	1911	2010
Total number of outbreaks	15	108
Average number of cases in outbreaksRange of number of cases in outbreaks	6.27(21 to 3)	4.66(17 to 3)
Gender (% of females of the total)	1024 (54%)	1109 (53%)
Case profile (count, %)
Pupil	1680 (87.9%)	1786 (84.6%)
Teacher	207 (10.8%)	275 (13.1%)
Staff	24 (1.3%)	49 (2.3%)
Educational stage of the case (count and %)
2nd cycle infants and 1st year primary school	438 (23.1%)	564 (26.9%)
2nd to 6th year primary	646 (34%)	1056 (50.9%)
Secondary	587 (30.9%)	318 (15.2%)
Baccalaureate	228 (12%)	155 (7.4%)
Symptomatology in case (symptom count and %)	943 (61.7%)	1254 (59.4%)

The cumulative incidence in classrooms (pupils and teachers) was 2470 cases per 100,000 inhabitants in the first quarter of the academic year 2020/2021 and 2720 cases per 100,000 inhabitants in the same period 2021/2022. The case counts per case profile in classrooms (pupils and teachers) according to educational stage in both trimesters of the study are presented in Fig. 1.

Fig. 1.

Cases of COVID-19 infection in pupils and teachers by educational stage during the first trimester of the 2020/2021 and 2021/2022 school years. Abbreviations: VAC (vaccinated), UNVAC (unvaccinated).

The risk of SARS-CoV-2 infection increased by 51.6% in under-12 classes (unvaccinated) in the 2021/2022 study period compared to the same period in 2020/2021. However, in classes over 12 years of age (highly vaccinated) the risk of infection between these periods decreased by 43.1%. In both cases the differences were statistically significant. In the analysis by subgroups, we observe that secondary school and baccalaureate pupils had a 53.3% and 36% decrease in risk respectively in the period 2021/2202 compared to 2020/2021; in contrast, the risk was 72.5% higher in students in years 2–6 of primary school. Table 2 presents the results of the cumulative incidences by case profile and educational stage of the classes analysed in the periods of the study.

Table 2.

Cumulative 3-month incidences of COVID-19 infection in classrooms during the first trimester of school years 2020/2021 and 2021/2022.

	School year 2020/2021	School year 2021/2022	p-value
Total CI	2470/100000 inhab.	2720/100000 inhab.	0.002
Total CI per classroom
Under 12 years old	2391/100000 inhab.	3625/100000 inhab.	<0.001
Over 12 years old	2578/100000 inhab.	1466/100000 inhab.	<0.001
CI in pupils
2nd cycle infants and 1st year primary	2310/100000 inhab.	2848/100000 inhab.	0.002
2nd to 6th year primary	2221/100000 inhab.	3831/100000 inhab.	<0.001
Secondary	2514/100000 inhab.	1175/100000 inhab.	<0.001
Baccalaureate	3259/100000 inhab.	2085/100000 inhab.	<0.001
CI in teachers
Under 12 years old	3990/100000 inhab.	5741/100000 inhab.	0.001
Over 12 years old	1712/100000 inhab.	1888/100000 inhab.	0.555

CI: Cumulative Incidence; inhab.: inhabitants.

We recorded 15 outbreaks in our study in the first period 2020/2021 versus 108 outbreaks in the first trimester of the academic year 2021/2022, and the average number of cases involved in each outbreak was higher in the first period (6.27 cases per outbreak versus 4.66 cases per outbreak). Characterisation of outbreaks according to person, time, and space (urban, semi-urban in populations with more than 20,000 inhabitants, and rural) between the two periods showed some differences. In the study period of the 2020/2021 school year, more outbreaks were reported in classrooms in 2nd cycle infants and 1st year primary (n = 7; 47%). However, in the 2021/2022 school year, the highest number of outbreaks was reported in the 2nd-6th years of primary school (n = 75; 69%). Urban schools had the highest number of cases involved in outbreaks in the second period (n = 338; 67.2%), in contrast to rural schools in the first period (n = 39; 41.5%). In both periods, pupils were the cases most involved in outbreaks.

The vaccination status of cases reported in school settings (pupils, teachers, and school staff) was analysed for the 2021/2022 quarter, a period when staff, teachers, and children aged 12 years and older had access to vaccination. The vaccination schedule was complete in more than 90% of COVID-19 cases in teachers and school staff. For pupils over 12 years of age, partial or full schedule immunisation was approximately 88% of confirmed cases (p = .002). Table 3 shows the vaccination status of COVID-19 cases according to the outbreak they fell under, case profile, educational stage, and symptoms.

Table 3.

Vaccination status of COVID-19 cases in the school setting who had access to immunisation during the first school trimester 2021/2022 (12 years and older, teachers, and school staff). The vaccination schedule was defined according to primary vaccination as per the technical data sheet of the vaccine preparation administered.

	Vaccination status
		Unvaccinated		Partial vaccination schedule		Full vaccination schedule		p-value
		n	%	n	%	n	%
Outbreak case	No	54	8.9	28	4.6	524	86.5	0.279
	Yes	7	7.9	1	1.1	81	91
Case profile	Pupil	44	11.7	22	5.9	309	82.4	0.002
	Teacher	13	4.8	7	2.6	252	92.6
	Staff	4	8.3	0	0.0	44	91.7
Educational stageof the case	Infants and 1st primary(teachers and staff)	6	5.6	3	2.8	98	91.6	0.239
	2nd to 6th primary(teachers and staff)	7	5.8	4	3.3	110	90.9
	Secondary(teachers, staff, and pupils)	35	11.6	16	5.3	251	83.1
	Baccalaureate(teachers, staff and pupils)	12	7.8	6	3.9	136	88.3
Symptoms inthe case	No	20	11.9	5	3	143	85.1	0.190
	Yes	41	7.8	24	4.5	462	87.7

The supplementary material contains a graphical summary of the study (Graphical summary).

Discussion

This study analysed the epidemiological situation of SARS-CoV-2 infection in schools during the first trimesters of the school year in the province of Valladolid, evaluating both periods. The sample (pupils, teachers, and educational staff) can be considered homogeneous, as can the periods of interest (first trimester of the academic year 2020/2021 and 2021/2022), and the protocols, protection, and control measures applied in COVID-19 infection in the school setting during the time of the study. Therefore, the differences observed between the study periods may be due to the effect of population-based vaccination in the 2021/2022 school year; without forgetting the impact of the different circulating variants of SARS-CoV-2.

During the 2020/2021 and 2021/2022 school trimesters considered, the total incidence of COVID-19 in the schools was similar. If we evaluate the total population incidence of infection in our province in the same periods of this study, we observe that in the first school trimester 2021/2022 it was 2568 cases per 100,000 inhabitants, in contrast to the previous school year when it was 4434 cases per 100,000 inhabitants. The population and school incidence results obtained for the 2021/2022 school year are consistent and compatible with those extracted in the study by Viner et al.¹⁶ which associated the prevalence of infections in the school environment with the incidence of infection in the community population.

In the first trimester of the 2021/2022 school year, the highest number of cases of COVID-19 in pupils were in the 2nd to 6th year of primary school, followed by cases in the 2nd cycle of infants and 1st year of primary school; in contrast to the 2020/2021 period where they were in high school and secondary school pupils. The data described in this first period of the school year in our study are analogous to those recorded in the study by Gamboa Moreno et al.⁶ conducted in the Basque Country during the first wave (which saw a greater secondary attack rate in the higher educational stages such as baccalaureate compared to infants) and in the study by Alonso et al.⁵

The increased transmissibility of the delta variant circulating in the second period of the study was reflected in the 7-fold increase in the number of school outbreaks in the period 2021/2022 compared to the same period 2020/2021, which mostly occurred in the 2nd-6th years of primary school. In addition, potential superspreader events in the school setting were reported as outbreaks involving a high number of cases in trimesters of the school year (21 cases in one outbreak in the first trimester and 17 cases in another outbreak in the second trimester), where the social link coexisted with the school setting.

Availability and access to vaccination against COVID-19 in our province for the group of teachers and school staff born between 1966 and 2003 occurred as of March 2021 (those born before 1966 had access by age group a few weeks later) and for those born between 2002 and 2009 as of August 2021, following Spain's COVID-19 Vaccination Strategy.¹¹ In our province, the population vaccination coverage against COVID-19 (persons over 12 years of age) was 82.62% and 78.27% with 1 and 2 doses, respectively, at the beginning of the 2021/2022 school year (10 September 2020); as of 22 December 2021 it was 86.64 and 84.12% (1 and 2 doses),¹⁷ and in the subgroup of children aged 12 to 19 years in our province, the vaccination rates for the same dates were 81% for 1 dose and 37% for 2 doses; and 94% and 88% for 1 and 2 doses, chronologically.

The vaccination status of students aged 12 years and older, teachers, and school staff with COVID-19 infection during the first quarter of the 2021/2022 school year was in line with the high population-based vaccination coverage at the provincial level (full or partial vaccination schedule in at least 85% of study cases, statistically significant values). Among COVID-19 cases, there was a significantly higher proportion of unvaccinated students over 12 years of age (11.7%) than teachers (4.8%) and other non-teaching school staff (8.3%). These differences did not reach statistical significance.

In our study, cases of infection among teachers did not decrease in this second period with access to vaccination (vaccine approval from March 2021). We do not have sufficient data on vaccination coverage and the specific vaccination schedule received by this population subgroup.

Limitations

This study has some limitations that should be considered when interpreting the results. The descriptive design of the study itself restricts the scope of the results extracted. At the same time, comparing the data between the two periods defined in a trimester conditions the representation of the total school year. It should also be borne in mind that the data were obtained from a register compiled by the Surveillance System of the Epidemiology Section of the Territorial Health Service of Valladolid, which involved pooling different sources of information, but it cannot be ruled out that confirmed cases in the school setting may have been lost.

Conclusions

This study shows a decrease in the incidence of SARS-CoV-2 infection in pupils in higher educational stages (secondary and baccalaureate) during the first trimester of the 2021/2022 school year (in which most were vaccinated) compared to the same period of the previous school year (in which they were unvaccinated). This is despite the increased transmissibility of the circulating delta variant, reflected in the increase in the number of outbreaks reported in schools in the first trimester of the school year compared to the previous year. However, in pupils from 2nd cycle infants to 6th year primary (not vaccinated in any of the trimesters studied), this incidence increased in both trimesters.

Further studies are needed to analyse the epidemiological situation of COVID-19 infection in schools after vaccination was introduced in children aged 5–12 years and the booster doses recommended in the population together with the new infection control measures.

Agreements

We would like to thank the COVID-19 team of the Provincial Directorate of Education of Valladolid for their work since the beginning of the pandemic and their collaboration with the Territorial Health Service.

Ethical responsibilities

The study was evaluated and approved by the Ethics Committee of the Valladolid West Health Area. Study Ref.: 22-PI061.

Funding

No funding was received for this study.

Authorship contribution

All the authors contributed intellectually to its elaboration, and have read and approved the final version of the submitted manuscript.