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Seroprevalence and factors associated with SARS-CoV-2 infection among education workers after the first wave: the first cross-sectional study in Brazil

ABSTRACT

Background:

The school community was heavily impacted by the Covid-19 pandemic, especially with the long time of school closures. This study aimed to analyze the seroprevalence of SARS-CoV-2 antibodies and possible factors associated with seropositivity for COVID-19 in teachers and other school staff, and to estimate the fraction of asymptomatic individuals by sex and age group.

Methods:

We conducted a serological survey of SARS-CoV-2 infections. An analytical cross-sectional study was conducted in Fortaleza, Brazil. Teachers and other staff members from pre-schools to universities of higher education to were investigated.

Results:

A total of 1,901 professionals participated in the study, of which 1,021 were staff and 880 were teachers. The seroprevalence of SARS-CoV-2 was 8.0% (152/1901). In the seropositive group, 48.3% were asymptomatic. There was a predominance of women (68.4%); and, 47.1% of the participants were between 31 and 45 years old. There was an increase in prevalence with increasing age. An inverse relationship was found for education level: more professionals with less education tested positive for COVID-19. The presence of an infected person living in the same household was significantly associated with positive results for COVID-19 among the professionals.

Conclusions:

This is the first study to report the seroprevalence of IgG against SARS-CoV-2 in Brazilian educational staff after the first wave of the disease. In this study, the seroprevalence was much lower than that in the general population. During school reopening, a small fraction of school workers showed serologically detectable signs of SARS-CoV-2 exposure.

Keyword:
Covid-19; Survey; School; SARS-CoV-2

INTRODUCTION

The detection and spread of an emerging respiratory disease is associated with a huge amount of uncertainty regarding its epidemiological and serological characteristics11. World Health Organization (WHO). Population-based age-stratified seroepidemiological investigation protocol for coronavirus 2019 (COVID-19) infection. WHO. Published 2020. Accessed November 11, 2020. Available from: Available from: https://www.who.int/emergencies/diseases/novelcoronavirus-2019/technical-guidance/early-investigations
https://www.who.int/emergencies/diseases...
. The novel coronavirus, SARS-CoV-2, emerged in Wuhan, China, in December 2019 and rapidly spread to other countries22. Zhu N, Zhang D, Wang W, Li X, Yang B, Song, et al. A novel coronavirus from patients with pneumonia in China, 2019. N Engl J Med. 2020;382(8):727-33. Available from: https://doi.org/10.1056/NEJMoa2001017
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,33. Holshue ML, DeBolt C, Lindquist S, Lofy KH, Wiesman J, Bruce H, et al. First case of 2019 novel coronavirus in the United States. N Engl J Med . 2020;382(10):929-36. Available from: https://doi.org/10.1056/NEJMoa2001191
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. On March 11, 2020, the World Health Organization (WHO) declared the coronavirus disease (COVID-19) a pandemic44. World Health Organization (WHO). Coronavirus disease (Covid-19). Situation Report - 51. Published April 2020. Accessed April 04, 2021. Available from:Available from:https://apps.who.int/iris/bitstream/handle/10665/331780/nCoVsitrep11Apr2020-eng.pdf
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To reduce transmission speed, control measures were launched worldwide; thus, pubs, shopping malls, parks, and schools were closed to avoid social contact55. Domenico L, Pullano G, Sabbatini CE, Boelle PY, Colizza V, et al. Impact of lockdown on COVID-19 epidemic in Île-de-France and possible exit strategies. BMC Medicine. 2020;18(240):1-13. Available from: https://doi.org/10.1186/s12916-020-01698-4
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,66. Askitas N, Tatsiramos K, Verheyden B. Estimating worldwide efects of non-pharmaceutical interventions on COVID-19 incidence and population mobility patterns using a multiple-event study. Scientifc Reports. 2021;11(1972):1-13. Available from: https://doi.org/10.1038/s41598-021-81442-x
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Despite the reopening of several sectors of the economy, more than 100 countries did not schedule dates for the reopening of schools until May 202077. Reopening schools: when, where and how? Paris: United Nations Educational, Scientific and Cultural Organization. Published 2020. Accessed November 11, 2020. Available from:Available from:https://en.unesco.org/news/reopening-schools-when-where-and-how
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The state of Ceará in northeast Brazil was one of the first to confirm sustained SARS-CoV-2 transmission, and schools were closed on March 20, 2020. The state government of Ceará issued early guidance for safe operation through prevention, early detection, and control of COVID-19 in schools and other educational facilities88. State Government of Ceará. Reopening Protocols. Published 2020. Accessed November 11, 2020. Available from:Available from:https://www.ceara.gov.br/wp-content/uploads/2020/09/Protocolo-Setorial-18-Atividades-Educacionais-1.pdf
https://www.ceara.gov.br/wp-content/uplo...
. Sectoral protocol N.18 mentions, among other requirements, that alcohol gel must be available in all rooms; a minimum of 1.5 meters of space should be kept between school desks; classes should be filled up to 35% capacity; and, students, teachers, and staff should mandatorily use masks. In addition, all teachers and staff were tested for COVID-19 by RT-PCR until one week before classroom return.

Available evidence suggests that children and adolescents may be less susceptible and present less severe disease than adults99. Viner RM, Mytton OT, Bonell C, Torres GJM, Ward J, Hudson L, et al. Susceptibility to SARS-CoV-2 Infection Among Children and Adolescents Compared With Adults: A Systematic Review and Meta-analysis. JAMA Pediatr. 2021;175(2):143-56. Available from: https://doi.org/10.1001/jamapediatrics.2020.4573
https://doi.org/10.1001/jamapediatrics.2...
. However, there are reports in the northeast of the systemic inflammatory syndrome in children during the COVID-19 pandemic1010. Farias LABG, Almeida MM, Linhares PMC, Brito Alves BCF, Duarte Filho RJC, Leite RD, Safadi MAP, Cavalcanti LPG. Systemic inflammatory syndrome in children during COVID-19 pandemic in Ceará state, northeastern Brazil: an observational study. Rev Soc Bras Med Trop. 2021;54(e0383):1-6. Available from: https://doi: 10.1590/0037-8682-0383-2021.
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,1111. Silva APSC, Holanda ER, Abreu PD, Freitas MVA. COVID-19 in children in the state of Pernambuco: Spatial analysis of confirmed severe cases and the Human Development Index. Rev Soc Bras Med Trop . 2021;54(e0782-2020):1-9. Available from: https://doi: 10.1590/0037-8682-0782-2020.
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As SARS-CoV-2 is a new virus, its initial seroprevalence in the population is assumed to be negligible. Therefore, the surveillance of antibody seropositivity in specific populations can allow inferences regarding the extent of infection in this population and subsequent control measures. By the end of November 2020, the state of Ceará had reported 293.237 cases and 9.563 deaths1212. BRASIL. Secretaria de Saúde do Estado (Ceará), Secretaria de Vigilância em Saúde, Boletim Epidemiológico - Monitoramento dos casos do Novo Coronavirus (COVID-19). Nº 53. Published 2021. Accessed January 2021. https://coronavirus.ceara.gov.br/boletins/.
https://coronavirus.ceara.gov.br/boletin...
,1313. BRASIL. Secretaria de Saúde do Estado (Ceará), Secretaria de Vigilância em Saúde, Boletim Epidemiológico - Monitoramento dos casos do Novo Coronavirus (COVID-19). Published 2021. Accessed January 2021. https://saude.fortaleza.ce.gov.br/images/coronavirus/PDFS/Informe-semanal-COVID-19-SE-48-2020---SMS-FORTALEZA_compressed.pdf
https://saude.fortaleza.ce.gov.br/images...
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The main objective of this study was to measure the seroprevalence of antibodies against anti-SARS-CoV-2 IgG antibodies, to identify factors associated with infection in teachers and other school staff to ascertain the cumulative population immunity, and to estimate the prevalence of asymptomatic infection by sex and age group after the first wave of the disease in Brazil. This is particularly important in the context of novel respiratory pathogens, such as SARS-CoV-2, and in the context of education.

METHODS

We conducted a serological survey using chemiluminescence immunoassay for anti-SARS-CoV-2 immunoglobulin G (IgG) antibodies in 2,341 private school teachers and staff in Fortaleza, Brazil. In 2020, only private schools returned to classroom lessons five months after the first pandemic peak and two months after the schools reopened.

In this section, we describe the study location, sampling and recruitment approaches, specimen collection methods, antibody testing procedures, statistical methods, and ethical aspects.

Design and study site

This was an analytical cross-sectional survey study with data collected between October and November 2020 in Fortaleza, Northeastern Brazil.

Study Participants and Sample Recruitment

We contacted schools through the union of private schools in Fortaleza (SINEPE-CE) to explain the research. The union, founded in 1943, represented the private schools in Fortaleza. The study was authorized, and the schools and their respective employees were invited to participate in the research.

A Google Forms link was subsequently sent to all the schoolteachers, university professors, and staff. Individuals who clicked on the link were directed to a survey that provided information regarding the study. At the end of the questionnaire, blood sample collection was scheduled to be conducted at the school. Only individuals with participant IDs were allowed to enter the testing area. The education professionals who participated in the survey and provided blood samples received the results of their tests through a smartphone application.

Professionals from pre-schools to universities of higher education were invited.

Laboratory diagnoses

The collected blood samples for serum separation were transported to a local laboratory where they were centrifuged at 2500 rpm for 10 min in an EVLAB apparatus (Macro EV model 04). Subsequently, they were frozen at -20 °C and transported to the Laboratory of Clinical Analysis of the Unichristus University Center (Laboratório Escola de Análises Clínicas da Unichristus (LEAC), in Portuguese) or to the laboratory of the Fundação Oswaldo Cruz (FIOCRUZ-CE) for testing. All samples were tested for IgG using the Abbott ARCHITECT SARS-CoV-2 test, a fully automated indirect immunoassay that detected antibodies directed to a recombinant SARS-CoV-2 nucleocapsid antigen. The assay showed a very high specificity (94.4%) and 100% sensitivity for samples collected after 14 days of symptom onset1414. Meschi S, Colavita F, Bordi L, Matusali G, Lapa D, Amendola A, et al. Performance evaluation of Abbott ARCHITECT SARS-CoV-2 IgG immunoassay in comparison with indirect immunofluorescence and virus microneutralization test. J Clin Virol. 2020;129(104539):1-4. Available from: https://doi.org/10.1016/j.jcv.2020.104539
https://doi.org/10.1016/j.jcv.2020.10453...
,1515. Chew KL, Tan SS, Saw S, Pajarillaga A, Zaine S, Khoo C, et al. Clinical evaluation of serological IgG antibody response on the Abbott Architect for established SARS-CoV-2 infection. Clin Microbiol Infect. 26(9):1256.e9-1256.e11, 2020. Available from: https://doi.org/10.1016/j.cmi.2020.05.036
https://doi.org/10.1016/j.cmi.2020.05.03...
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Study variables and data analysis

The variables used in this study were demographic data: sex, age, educational level, family income, self-reported COVID-19 symptoms, and the presence of chronic diseases such as diabetes, hypertension, asthma, chronic kidney disease, and cancer. Other aspects were related to housing type (house or apartment), number of people living in the house, presence of basic sanitation, garbage collection, and water supply. Variables regarding working conditions included: work shift (morning, afternoon, or night), mode of transportation used, habits during the pandemic, and individual protection measures. We also investigated the class levels of the teachers, and, for the other employees, the sector in which they worked (secretary, administrative, canteen, concierge, and cleaning). In terms of ethnicity, we used a self-reported standard Brazilian skin color/ethnicity classification using five categories: white, black, brown, Asian, and indigenous. The “brown” or “pardo” category included individuals who self-reported having mixed ancestry.

Statistical analysis

The data were exported to IBM SPSS Statistics for Windows version 20.0. The association of the frequency of serum conversion to COVID-19 with other variables was checked using Pearson chi-square test or Fisher exact test. Variables with p<0.200 were subjected to a multivariable logistic regression model. Adjusted odds ratios and 95% CIs were calculated to determine the factors independently associated with COVID-19-IgG seroconversion.

Ethical aspects

The study was approved by CAAE 39691420.7.0000.5049.

RESULTS

Characteristics of the population

In total, 2,341 questionnaires were completed. After removing duplicates, 340 (14.5%) were excluded. After blood collection, another 100 (5%) were excluded due to insufficient material for testing. We then collected data from 1,901 professionals, including 1,021 employees and 880 teachers. Most of the teachers (34.2%) taught in elementary I; 24.0%, elementary II; 23.8%, higher education; and, 23.2%, preschools.

There was a predominance of women (68.4%), and 47.1% of the participants were between 31 and 45 years old (Table 1). Most participants lived in houses (63.1%) with up to three people (56.9%) (Table 1). Most of the interviewees reported the absence of persons diagnosed with COVID-19 at home (57.6%), and 68.4% reported knowing someone who had died from COVID-19.

TABLE 1:
Influence of socioeconomic factors on seroconversion in teachers and school employees during the first wave of the COVID-19 pandemic in the city of Fortaleza, Brazil.

The most used mode of transportation to work was personal cars (45.9%), followed by public transportation (31.9%). The majority (74.1%) reported to have avoided face-to-face activities during the pandemic. They stayed at their home offices, and 60.0% of them reported to leave home only to go to the marketplace and to the pharmacy (40.0%) (Tables 2 and 3).

TABLE 2:
Influence of professional profile on seroconversion in school teachers and employees during the first wave of the COVID-19 pandemic in the city of Fortaleza, Brazil.
TABLE 3:
Influence of daily routine on seroconversion in school teachers and employees during the first wave of the COVID-19 pandemic in the city of Fortaleza, Brazil.

Characteristics of positive cases of COVID-19

IgG antibodies were detected in 152 of the 1,901 samples, with a positive seroprevalence of 8.0% (95% CI: 6.8-9.3). Among the seropositive participants, 48.3% did not report prior COVID-19-like illnesses.

An increase in the seroprevalence was observed with increasing age. Individuals older than 45 years showed 12.0% positivity (PR=1.63; 95%CI: 1.11-2.41). The seroprevalence in the brown and black races was 9.6% (PR=1.97; 95%CI:1.35-2.88) and 11.7% (PR=2.18; 95%CI: 1.25-3.80), respectively, and it was significantly higher in them than those who declared themselves white (5.4%).

The seropositivity among the staff was slightly higher (8.5%; 95%CI: 7.0-10.2) as compared to that in teachers (7.4%; 95%CI: 5.9-9.4), but without a significant difference (p=0.363).

Contrastingly, for teachers, positivity for COVID-19 IgG antibodies was higher among those with more than 20 years of classroom teaching experience (11.5%; 95%CI: 7.6-17.6). Teachers working in preschool classes and elementary I showed 8.8% (95%CI: 5.6-13.6) and 9.0% (95%CI: 6.2-12.8) positivity, respectively, which was higher than the average positivity of the other classes (5.9%; 95%CI: 4.3-7.9).

It was also observed that teachers excluded from the present classroom activities showed no significant difference in positivity for COVID-19 (p=0.214) (Table 2). The presence of infected persons at home was significantly associated with positivity for COVID-19 among professionals (PR=3.76; 95%CI: 2.65-5.35).

Social isolation was declared as intense by 312 professionals, and this group had a mean prevalence of positivity of 6.1% (95%CI: 3.9-9.4), lower than that in professionals who did not maintain isolation at the same intensity (8.4%; 95%CI: 7.1-9.9). This was also observed in the social isolation routine, in which those who went out (8.5%; 95%CI: 7.2-9.9) and those who received more visitors (9.0%) (95%CI: 7.4-11.7) had higher positivity rates than those who stayed at home all the time (5.4%; 95%CI: 3.3-8.7).

The most prevalent symptoms among participants with positive tests who reported prior COVID-19-like illnesses were loss of smell, loss of taste, fever, body pain, and cough, with percentages higher than 25%, with a statistically significant difference from those professionals with the same symptoms but showing negative tests. The only symptom that was not statistically significant was headache, with only seven reports (p=0.078). Among the symptomatic patients, six different groups of medications were prescribed, and azithromycin (40.3%), dipyrone (35.1%), ivermectin (27.7%), and paracetamol (25.5%) were notable. However, none of the medications used was associated with COVID-19 symptoms (Table 4).

TABLE 4:
Perceptions of people who had symptoms regarding seroconversion in teachers and school employees during the first wave of the COVID-19 pandemic in the city of Fortaleza, Brazil.

In an adjusted analysis, the chance of positivity among those aged >45 years was 2.39 times higher (95%CI: 1.12-5.13; p=0.025), and seroconversion was 2.00 times lower in those who did not perform physical activity (95%CI: 1.09-3.57; p=0.025). For those who had patients with COVID-19 at home, the chance of positivity was 5.58 times higher (95%CI: 3.03-10.3; p<0.001). Regarding symptoms, difficulty in breathing and loss of smell were notable, which were 4.04 and 4.12 times higher among those who showed positive results (p<0.001), respectively.

Employees who used public transportation to attend school showed higher positivity rates. On the other hand, lower positivity rates were observed in teachers who worked only one shift, commuted alone in their cars, and had health insurance (Table 5).

TABLE 5:
Influence of professional profile on seroconversion in school teachers and employees during the first wave of the COVID-19 pandemic in the city of Fortaleza, Brazil.

DISCUSSION

This study was the first large-scale prevalence study conducted among educational workers in Brazil immediately after the first wave of the disease. This study was the first to measure the IgG antibody response to SARS-CoV-2 in a school community exposed to the virus. In our study, the immune response related to previous SARS-CoV-2 infections was < 10.0%. The seropositivity was lower than that of the general population (15.53%) when tested during the same period in the city of Fortaleza1313. BRASIL. Secretaria de Saúde do Estado (Ceará), Secretaria de Vigilância em Saúde, Boletim Epidemiológico - Monitoramento dos casos do Novo Coronavirus (COVID-19). Published 2021. Accessed January 2021. https://saude.fortaleza.ce.gov.br/images/coronavirus/PDFS/Informe-semanal-COVID-19-SE-48-2020---SMS-FORTALEZA_compressed.pdf
https://saude.fortaleza.ce.gov.br/images...
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Seroprevalence studies help understand the likelihood of asymptomatic infections. Among our participants who tested seropositive, 48.3% reported no prior COVID-19-like illnesses. This finding suggests that a significant proportion of patients with COVID-19 were asymptomatic. It is likely that these individuals did not self-isolate when infected, and they continued to spread the disease to other people.

A population-based survey conducted in another state in the northeast region of Brazil showed that the seroprevalence of total antibodies against SARS-CoV-2 was 40.4%1616. Silva AAM, Lima-Neto LG, Azevedo CMOS Costa LMM, Braganca MLBM, Barros-Filho AKD, et al. Population-based seroprevalence of SARS-CoV-2 and the herd immunity threshold in Maranhão. Rev Saúde Pública. 2020;131(54):1-14. Available from: https://doi.org/10.11606/s1518-8787.2020054003278.
https://doi.org/10.11606/s1518-8787.2020...
, much higher than that found in this study. A possible explanation for this low prevalence is that some teachers were working remotely at the time of the research. Another explanation for this difference is that we did not perform IgM antibody detection.

Prevalence studies conducted during the first wave of the disease reported varying results owing to the population studied, sampling, and type of laboratory test used1717. Menachemi N, Yiannoutsos CT, Dixon BE, Duszynski TJ, Fadel WF, Wools-Kaloustian KK, et al. Population Point Prevalence of SARS-CoV-2 Infection Based on a Statewide Random Sample - Indiana, April 25-29, 2020. MMWR Morb Mortal Wkly Rep. 2020;69(29):960-64. Available from: https://doi.org/10.15585/mmwr.mm6929e1
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,1818. Tess BH, Granato CFH, Alves MCGP, Pintao MC, Rizzatti E, Nunes MC, et al. SARS-CoV-2 seroprevalence in the municipality of São Paulo, Brazil, ten weeks after the first reported case. medRxiv preprint. Published 2020. Accessed April 2021. Available from: https://doi.org/10.1101/2020.06.29.20142331
https://doi.org/10.1101/2020.06.29.20142...
. In this study, most factors associated with SARS-CoV-2 infection were identified outside the workplace, suggesting that current infection prevention strategies within schools can be effective in preventing transmission in the workplace.

These assays detected the presence of antibodies, but neutralization assays would be fundamental and complementary in determining the functional role of antibodies in immune protection1818. Tess BH, Granato CFH, Alves MCGP, Pintao MC, Rizzatti E, Nunes MC, et al. SARS-CoV-2 seroprevalence in the municipality of São Paulo, Brazil, ten weeks after the first reported case. medRxiv preprint. Published 2020. Accessed April 2021. Available from: https://doi.org/10.1101/2020.06.29.20142331
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This study showed that almost half of the IgG-positive cases were asymptomatic. Anosmia and ageusia predominated among the symptomatic cases. A study conducted by a private laboratory in the city of Fortaleza showed that 18.8% of the reported cases were asymptomatic1919. Garcia YDO, Braga AA, Araujo FMC. Evaluation of the diagnostic profile of coronavirus disease 2019 in Fortaleza - Ceará, Brazil. Acad. J. Microbiol. Res. 2021;9(1):1-6. Available from: https://doi.org/10.15413/ajmr.2020.1252
https://doi.org/10.15413/ajmr.2020.1252...
. Among those who reported symptoms, the most frequently reported symptoms were headache (36.40%), cough (29.62%), weakness (29.68%), and fever (27.42%).

The percentage of asymptomatic patients was consistent with that reported in the literature2020. Oran DP, Topol EJ. The proportion of SARS-CoV-2 infections that are asymptomatic: a systematic review. Ann Intern Med. 2021;174(5):655-62. Available from: https://doi.org/10.7326/M20-6976.
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. Therefore, it is important to continue to reinforce the need for the correct use of proper face masks by professionals2121. Johansson MA, Quandelacy TM, Kada S, Prasad PV, Steele M, Brooks JT, et al. SARS-CoV-2 Transmission From People Without COVID-19 Symptoms. JAMA Netw Open. 2021;4(1):e2035057. Available from: https://doi.org/10.1001/jamanetworkopen.2020.35057
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, as asymptomatic cases may suggest a lower antibody response and titers decrease more quickly2222. Long QX, Tang XJ, Shi QL, Li Q, Deng HJ, Yuan J, et al. Clinical and immunological assessment of asymptomatic SARS-CoV-2 infections. Nat Med. 2020; 26(1200)1-4. Available from: https://doi.org/10.1038/s41591-020-0965-6.
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. However, due to the large number of asymptomatic cases or mild infections and the difficulty of access to laboratory diagnosis in developing countries such as Brazil, the available data of laboratory-confirmed cases do not capture the true extent of virus spread. Therefore, the serological detection of specific antibodies against SARS-CoV-2 can be used to better estimate the true number of infections.

The current evidence shows that schools have not evolved into silent hotspots of SARS-CoV-2 transmission. This is especially important as there are severe adverse effects of prolonged school closure, especially on populations that are more socially vulnerable2323. Nafisah SB, Alamery AH, Nafesa AA, Aleid B, Brazanju NA. School closure during novel influenza: A systematic review. J Infect Public Health. 2018;11(5):657-66. Available from: https://doi.org/10.1016/j.jiph.2018.01.003
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,2424. Jackson C, Mangtani P, Hawker J. The effects of school closures on influenza outbreaks and pandemics: systematic review of simulation studies. PLoS ONE. 2014; 9(5):e97297. Available from: https://doi.org/10.1371/journal.pone.0097297.
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. Furthermore, we cannot fail to mention that in socially disadvantaged contexts, even with school closure, social contacts and non-school encounters continue2525. Rashid H, Ridda I, King C. Evidence compendium and advice on social distancing and Other related measures for response to an influenza pandemic. Paediatr Respir Rev. 2015;16(2):119-26. Available from: https://doi.org/10.1016/j.prrv.2014.01.003.
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, thus reducing the potential benefit of school closure.

Our findings showed that those with higher education had a lower chance of a previous infection. This probably occurred because those with higher education had more access to information and, consequently, to disease prevention measures, such as social distancing, use of masks and chamging them within the period established by the competent bodies, use of face shields as physical barriers, and respiratory etiquette, among others recommended by the Brazilian Ministry of Health1212. BRASIL. Secretaria de Saúde do Estado (Ceará), Secretaria de Vigilância em Saúde, Boletim Epidemiológico - Monitoramento dos casos do Novo Coronavirus (COVID-19). Nº 53. Published 2021. Accessed January 2021. https://coronavirus.ceara.gov.br/boletins/.
https://coronavirus.ceara.gov.br/boletin...
. Furthermore, the greater adherence and compliance to safety rules by education professionals is notable.

Even in the scenario of high SARS-CoV-2 transmission, the spread within schools was very low. Modelling studies on the effect of school closure often rely on strong theoretical assumptions that do not easily adequately control for important confounders because of their ecological nature and, despite being interesting from a scientific point of view, they should not replace studies based on prospectively collected data. Schools should not be closed for a prolonged period, as they lead to overall harmful consequences on health, society, and the economy, in addition to increasing the existing inequalities between public and private education networks2626. Christakis DA. School Reopening-The Pandemic Issue That Is Not Getting Its Due. JAMA Pediatr . 2020;174(10):928. Available from: https://doi.org/10.1001/jamapediatrics.2020.2068
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27. Viner RM, Bonell C, Drake L, Jourdan D, Davier N, Baltag V, et al. A: Reopening schools during the COVID-19 pandemic: governments must balance the uncertainty and risks of reopening schools against the clear harms associated with prolonged closure. Arch Dis Child. 2021;(106):111-3. Available from: https://doi.org/10.1136/archdischild-2020-319963
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-2828. Loades ME, Chatburn E, Higson-Sweeney N. Rapid systematic review: the impact of social isolation and loneliness on the mental health of children and adolescents in the context of COVID-19. J Am Acad Child Adolesc Psychiatry. 2020;S0890-8567(20)30337-3. Available from: https://doi.org/10.1016/j.jaac.2020.05.009
https://doi.org/10.1016/j.jaac.2020.05.0...
. As evidence for COVID-19 evolves, there is heightened awareness of the disproportionate impact on the school community resulting from the closure of schools and an intensified call to reopen schools safely2929. Dooley DG, Bandealy A, Tschudy MM. Low-income children and coronavirus disease 2019 (COVID-19) in the US. JAMA Pediatr . 2020;174(10):922-3. Available from: https://doi.org/10.1001/jamapediatrics.2020.2065
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The need to respond to the pandemic has led to the closure of school buildings across the country, with little time to ensure continuity of instruction or to create a framework for deciding when and how to reopen schools3030. Dibner KA, Schweingruber HA, Christakis DA. Reopening K-12 Schools During the COVID-19 Pandemic: A Report From the National Academies of Sciences, Engineering, and Medicine. JAMA. 2020;324(9):833-4. Available from: https://doi.org/10.1001/jama.2020.1474.
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. This was the first time in our country that all schools were closed for so long, which provided a unique opportunity to assess the influence of school closure not only on schoolchildren but also on the economy. A recent study conducted in the Gaza Strip highlighted the profound economic and social consequences3131. Radwan A, Radwan E. Social and Economic Impact of School Closure during the Outbreak of the COVID-19 Pandemic: A Quick Online Survey in the Gaza Strip. Pedagogical Research. 2020;5(4):em0068. Available from: https://doi.org/10.29333/pr/8254
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. As a result, parents, schools, and social organizations need to pay more attention to the psychological state of students, especially those in elementary school who have remained out of school for long3232. Yanghao Z, Jianhua L, Maiyan Z. A survey of the psychological status of primary school students who were quarantined at home during the coronavirus disease 2019 epidemic in Hangzhou China. medRxiv preprint. Published June 2020.Available from: https://doi.org/10.1101/2020.05.28.20115311
https://doi.org/10.1101/2020.05.28.20115...
,3333. Esposito S, Principi N. School closure during the Coronavirus Disease 2019 (COVID-19) Pandemia: An Effective Intervention at Global Level? JAMA Pediatr . 2020;174(10):921-2. Available from: https://doi.org/10.1001/jamapediatrics.2020.189
https://doi.org/10.1001/jamapediatrics.2...
. Furthermore, our study involved professionals from private schools. Even though most of them, especially teachers, were public school teachers, they may present a different socioeconomic context than those who worked exclusively in public schools.

The presence of a person with a confirmed diagnosis of COVID-19 in the home increased the chance of testing positive by more than fivefold (5.58). The attack rates among family members were higher, and this finding reinforces previous literature that indicated the importance of isolation of close contacts and the need for mask use and intradomiciliary care3434. Grijalva CG, Rolfes MA, Zhu Y, McLean H, Hanson KE, Belongia EA, et al. Transmission of SARS-COV-2 Infections in Households - Tennessee and Wisconsin, April-September 2020. MMWR Morb Mortal Wkly Rep . 2020;69(44):1631-4. Published 2020 Nov 6 Available from: https://doi.org/10.15585/mmwr.mm6944e1
https://doi.org/10.15585/mmwr.mm6944e1...
.

Our study showed that the population of teachers and employees of private institutions aged over 45 years showed more than twice as high positivity (2.39) compared to the younger population. These findings corroborate the literature regarding age, indicating a higher positivity among older people3535. Hongdou L, Wang S, Zhong F Bao W, Li Y, Liu L, et al. Age-Dependent Risks of Incidence and Mortality of COVID-19 in Hubei Province and Other Parts of China. Front Med. 2020;7(190):1-6. Available from: https://doi.org/10.3389/fmed.2020.00190
https://doi.org/10.3389/fmed.2020.00190...
.

No significant sex-related difference was observed, although women represented 68% of the sample. Moreover, there were no differences in housing conditions, job function, shift, time or duration of teaching, type of transportation, area of activity in the school, and whether they were away from classroom activities. There was a higher incidence of positive COVID-19 cases in the brown and black populations. The reality of socioeconomic vulnerability is also associated with a housing issue, wherein households limited to a smaller geographic space having a high number of household contacts (above three people) worsen the spread of SARS-COV-23535. Hongdou L, Wang S, Zhong F Bao W, Li Y, Liu L, et al. Age-Dependent Risks of Incidence and Mortality of COVID-19 in Hubei Province and Other Parts of China. Front Med. 2020;7(190):1-6. Available from: https://doi.org/10.3389/fmed.2020.00190
https://doi.org/10.3389/fmed.2020.00190...
,3737. Louis-Jean J, Cenat K, Njoku CV, Sanon D. Coronavírus (COVID-19) e Disparidades Raciais: uma Análise em Perspectiva. J Racial and Ethnic Health Disparities. 2020;7:1039-45. Available from: https://doi.org/10.1007/s40615-020-00879-4
https://doi.org/10.1007/s40615-020-00879...
. The pandemic presented deep racial and social disparities, with more severe consequences in brown and black people2929. Dooley DG, Bandealy A, Tschudy MM. Low-income children and coronavirus disease 2019 (COVID-19) in the US. JAMA Pediatr . 2020;174(10):922-3. Available from: https://doi.org/10.1001/jamapediatrics.2020.2065
https://doi.org/10.1001/jamapediatrics.2...
,3838. Hooper MW, Nápoles AM, Pérez-Stable EJ. COVID-19 and Racial/Ethnic Disparities. JAMA. 2020;323(24):2466-7. Available from: https://doi.org/10.1001/jama.2020.8598
https://doi.org/10.1001/jama.2020.8598...
.

In the face of the unprecedented global health crisis in recent decades, public health authorities need seroprevalence data to estimate the exposure of the most vulnerable groups, especially in developing countries where access to molecular diagnostics is limited. These prevalence estimates should be used to calibrate the projections of the epidemic and its actual mortality rate. Several lessons have been learned over these months, and we hope that educators and decision-makers will be better prepared to act promptly in future education crises involving interrupted classroom instruction. Currently, there is broad agreement that school closures involve heavy burdens on students, parents, and the economy with profound equity implications3939. Goldhaber-Fiebert JD, Studdert DM, Mello MM. School Reopenings and the Community During the COVID-19 Pandemic. JAMA Health Forum. Published online October 28, 2020;1(10):e201294 Available from: https://doi.org/10.1001/jamahealthforum.2020.1294
https://doi.org/10.1001/jamahealthforum....
.

Future studies should investigate the structural conditions of the school, such as the size of the physical space of the institution and the capacity of the sanitary facilities, which may favor or prevent the spread of the virus. Governments should reinforce, as soon as possible, policies that decrease transmission in the community and implement control measures within schools so that they can simultaneously address both the health crisis represented by COVID-19 and the adverse consequences of prolonged school closures3636. COVID-net. Laboratory-Confirmed COVID-19-Associated Hospitalizations. Published 2020. Acessed April 2021. https://gis.cdc.gov/grasp/covidnet/covid19_3.html
https://gis.cdc.gov/grasp/covidnet/covid...
,4040. Head JR, Andrejko KL, Cheng Q. The effect of school closures and reopening strategies on COVID-19 infection dynamics in the San Francisco Bay Area: a cross-sectional survey and modeling analysis. medRxiv [Preprint]. 2020. doi: Available from: https://doi.org/10.1101/2020.08.06.20169797
https://doi.org/10.1101/2020.08.06.20169...
. Variation across schools in this condition is an additional complication in ensuring the health of students and staff at schools. To reopen safely, schools are encouraged to ensure ventilation and air filtration, clean surfaces frequently, provide facilities for regular handwashing, and provide space for physical distancing.

During the first epidemic wave, many countries included school closures among the measures implemented to limit viral transmission4141. Donohue JM, Miller E. COVID-19 e o fechamento de escolas. JAMA. 2020;324(9):845-7. Available from: https://doi.org/10.1001/jama.2020.13092
https://doi.org/10.1001/jama.2020.13092...
. Part of this decision was based on the experience of influenza transmission in schoolchildren4242. Cauchemez S, Valleron, AJ, Boëlle PY. Estimating the impact of school closure on influenza transmission from Sentinel data. Nature. 2008;(452):750-4 Available from: https://doi.org/10.1038/nature0673
https://doi.org/10.1038/nature0673...
,4343. Litvinova M, Liu QH, Kulikov ES. Reactive school closure weakens the network of social interactions and reduces the spread of influenza. PNAS. 2019;116:13174-181. Available from: https://doi.org/10.1073/pnas.1821298116
https://doi.org/10.1073/pnas.1821298116...
. With the circulation of new variants, it is critical to assess the risk of viral circulation among students and their teachers in schools3333. Esposito S, Principi N. School closure during the Coronavirus Disease 2019 (COVID-19) Pandemia: An Effective Intervention at Global Level? JAMA Pediatr . 2020;174(10):921-2. Available from: https://doi.org/10.1001/jamapediatrics.2020.189
https://doi.org/10.1001/jamapediatrics.2...
because, to the best of our knowledge, secondary transmission of SARS-CoV-2 in school settings has been limited, as reported in Australia, Ireland, and France4444. NCIRS. COVID-19 in schools - the experience in NSW Prepared by the National Centre for Immunisation Research and Surveillance. Published April 2020. Acessed April 2021. https://www.ncirs.org.au/sites/default/files/2020-04/NCIRS%20NSW%20Schools%20COVID_Summary_FINAL%20public_26%20April%202020.pdf
https://www.ncirs.org.au/sites/default/f...

45. Heavey L, Casey G, Kelly C, Kelly D, McDarby G. No evidence of secondary transmission of COVID-19 from children attending school in Ireland, 2020. Euro Surveill. 2020;25(21):pii=2000903. Available from: https://doi.org/10.2807/1560-7917.ES.2020.25.21.2000903
https://doi.org/10.2807/1560-7917.ES.202...
-4646. Danis K, Epaulard O, Bénet T, Gaymard A, Campoy S, Botelho-Nevers E, et al. Cluster of coronavirus disease 2019 (COVID-19) in the French Alps, February 2020. Clin Infect Dis. 2020;71(15):825-32. Available from: https://doi:10.1093/cid/ciaa424.
https://doi.org/10.1093/cid/ciaa424...
. It is also important to better understand the extent of infection among teachers and its role in transmission within the school, given the likely negative effects of school closures on educational performance and economic outcomes2626. Christakis DA. School Reopening-The Pandemic Issue That Is Not Getting Its Due. JAMA Pediatr . 2020;174(10):928. Available from: https://doi.org/10.1001/jamapediatrics.2020.2068
https://doi.org/https://doi.org/10.1001/...
,3333. Esposito S, Principi N. School closure during the Coronavirus Disease 2019 (COVID-19) Pandemia: An Effective Intervention at Global Level? JAMA Pediatr . 2020;174(10):921-2. Available from: https://doi.org/10.1001/jamapediatrics.2020.189
https://doi.org/10.1001/jamapediatrics.2...
. Future decisions regarding school closures during the pandemic should give greater weight to the potential effects of school closure on children’s health2626. Christakis DA. School Reopening-The Pandemic Issue That Is Not Getting Its Due. JAMA Pediatr . 2020;174(10):928. Available from: https://doi.org/10.1001/jamapediatrics.2020.2068
https://doi.org/https://doi.org/10.1001/...
.

A limitation that must be reported is that the tests may result in false negatives for very recent infections, especially in the first two weeks after infection; therefore, this prevalence would reflect the infection levels one or two weeks prior to the date of the survey. In addition, it is important to note that, at the time of the study, the expression of the new strains was quite limited, and we had not yet isolated P.1., which became predominant in February 20214747. GISAID. Vigilância genômica do sars-cov-2 no Brasil. [internet]. FIOCRUZ. [updated 2022 Mar 14; cited 2021 Nov 30]. Available from:Available from:http://www.genomahcov.fiocruz.br/presenca-das-linhagens-por-estado/
http://www.genomahcov.fiocruz.br/presenc...
. The use of online questionnaires and the convenience of sample size may have led to a bias in the results due to the interest of the persons participating in the study; however, we believe that given the high interest in the interviewees in taking the test for COVID-19, and given that the test was necessary for the return to work by the government of Ceará, this bias was minimized. In addition, the data collection of this study was carried out in a short period of time due to the need to obtain results that would enable an assessment of the association of the health situation of the employees with COVID-19. Furthermore, this study was conducted with professionals from private schools, and that its results must be extrapolated with restrictions to professionals from public schools, given the different working conditions of these professionals.

Therefore, in this new scenario, and considering the positive results of the measles vaccination4848. Eberhardt CS, Siegrist CA. Is there a role for childhood vaccination against COVID-19? Pediatr Allergy Immunol. 2021;32(1):9-16. Available from: https://doi: 10.1111/pai.13401. Epub 2020 Nov 20. PMID: 33113210.
https://doi.org/10.1111/pai.13401...
,4949. Klass P, Ratner AJ. Vaccinating Children against Covid-19 - The Lessons of Measles. N Engl J Med . 2021;384(7):589-91. Available from: https://doi: 10.1056/NEJMp2034765. Epub 2021 Jan 20. PMID: 33471977.
https://doi.org/10.1056/NEJMp2034765...
, it is essential to encourage vaccination not only for teachers and adolescents but also for the pediatric population. Without a doubt, schools need to reopen safely so that they can better serve students, families, and communities that depend on them.

ACKNOWLEDGMENTS

LPGC is recipient of a fellowship for research productivity granted by the Brazilian National Council for Scientific and Technological Development (CNPq/Brazil).

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  • Financial Support: This study was partially supported by the FIOCRUZ/Ce; Secretaria de Saúde do Ceará (SESA); Centro Universitario Christus (UNICHRISTUS) and Sindicato das Escolas Particulares de Fortaleza (SINEPE/Ce).

Publication Dates

  • Publication in this collection
    29 Apr 2022
  • Date of issue
    2022

History

  • Received
    30 Nov 2021
  • Accepted
    08 Mar 2022
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