| TYPE Brief Research Report PUBLISHED 10 January 2023 DOI 10.3389/fped.2022.975454 Feasibility of severe acute respiratory syndrome EDITED BY Hulya Bukulmez, Case Western Reserve University, United States coronavirus 2 (SARS-CoV-2) REVIEWED BY Sema Ketenci, antigen self-testing in school İ stanbul Atlas Üniversitesi, Turkey Jilian Sacks, and summer camp attendees Foundation for Innovative New Diagnostics, Switzerland Andreu Colom-Cadena1,2†, Héctor Martínez-Riveros1,2,3†, *CORRESPONDENCE Cristina Agustí Anna Bordas1,2, Lucia Alonso-García1,2, cagusti@iconcologia.net Marcos Montoro-Fernández1, Pol Romano-deGea1,2, † These authors have contributed equally to this Josep Vidal-Alaball4,5,6, Elisabet Solà-Segura7, Josep M. Llibre8, work and share first authorship ‡ Boris Revollo8‡, Jordi Casabona1,2,9,10‡ and Cristina Agustí1,9‡* These authors have contributed equally to this 1 work and share senior authorship Centre of Epidemiological Studies on Sexually Transmitted Infections and AIDS of Catalonia (CEEISCAT), Ministry of Health, Government of Catalonia, Badalona, Spain, 2Institut d’Investigació SPECIALTY SECTION Germans Trias I Pujol (IGTP), Badalona, Spain, 3PhD in Methodology of Biomedical Research and This article was submitted to Pediatric Public Health, Department of Pediatrics, Obstetrics and Gynecology and Preventive Medicine, Univ Infectious Diseases, a section of the journal Autonòma de Barcelona, Badalona, Spain, 4Health Promotion in Rural Areas Research Group, Frontiers in Pediatrics Gerència Territorial de la Catalunya Central, Institut Català de la Salut, Sant Fruitós del Bages, Spain, 5 Unitat de Suport a la Recerca de la Catalunya Central, Fundació Institut Universitari per a la Recerca a RECEIVED 22 June 2022 l’Atenció Primària de Salut Jordi Gol I Gurina, Sant Fruitós del Bages, Spain, 6University of Vic-Central ACCEPTED 16 December 2022 University of Catalonia, Vic, Spain, 7Primary Heatlhcare Team Vic Nord, Institut Català de la Salut, Vic, PUBLISHED 10 January 2023 Spain, 8Division of Infectious Diseases and Foundation for Fighting AIDS, Infectious Diseases and CITATION Promoting Health and Science, University Hospital Germans Trias I Pujol, Badalona, Spain, 9 Departament de Pediatria, d’Obstetrícia I Ginecologia I de Medicina Preventiva I de Salut Publica, Colom-Cadena A, Martínez-Riveros H, Universitat Autònoma de Barcelona, Bellaterra, Spain, 10Spanish Consortium for Research on Bordas A, Alonso-García L Epidemiology and Public Health (CIBERESP), Instituto de Salud Carlos III, Madrid, Spain Montoro-Fernández M, Romano-deGea P, Vidal-Alaball J, Solà-Segura E, Llibre JM, Revollo B, Casabona J and Agustí C (2023) Background: SARS-CoV-2 screening is one of the pillars of Feasibility of severe acute respiratory syndrome non-pharmaceutical preventive strategies to early identify and isolate coronavirus 2 (SARS-CoV-2) antigen self- infected individuals and therefore decrease community incidence. testing in school and summer camp attendees. Front. Pediatr. 10:975454. Methods: We assessed the feasibility of severe acute respiratory syndrome doi: 10.3389/fped.2022.975454 coronavirus 2 self-testing with antigen-detecting rapid diagnostic tests in COPYRIGHT attendees of educational settings. © 2023 Colom-Cadena, Martínez-Riveros, Results: A total of 305 students (88.15%) and 41 staff (11.85%) from 9 to 56 Bordas, Alonso-García, Montoro-Fernández, years old participated in the self-testing procedure and answered the survey Romano-deGea, Vidal-Alaball, Solà-Segura, Llibre, Revollo, Casabona and Agustí. This is an at the end of the study. 91.3% (n = 313) did not need help, 96.1% of open-access article distributed under the terms participants reported the same outcome as the healthcare workers. 94.5% of the Creative Commons Attribution License strongly or slightly agree with the statement “I would repeat the experience”. (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original Conclusion: The study demonstrates that self-testing is acceptable and usable author(s) and the copyright owner(s) are in children, adolescents and adults when the epidemiological situation may credited and that the original publication in this require a systematic screening of these populations, although supervision by journal is cited, in accordance with accepted academic practice. No use, distribution or health care or previously trained personnel is recommended for younger age reproduction is permitted which does not groups. comply with these terms. KEYWORDS acceptability and usability, SARS-CoV-2 antigen testing, SARS-CoV-2, school public health, self-testing Frontiers in Pediatrics 01 frontiersin.org Colom-Cadena et al. 10.3389/fped.2022.975454 Introduction and summer camps. The field team consisted of between 2 and 4 healthcare workers (nurses and nursing assistants). Since the emergence of SARS-CoV-2 in December 2019 governments have implemented various measures to control the spread of the virus. Schools were severely affected and Material delivery and data collection initially closed in many countries, including Spain, despite uncertainty if school closures were an effective containment After signing the informed consent, participants received a measure, with a negative impact on the education of children sampling kit including: paper-based schematic and illustrated and adolescents (1). instructions for the self-testing procedure, a printed feasibility However, data from different countries showed that survey, ID labels and the SARS-CoV-2 Ag-RDT Kit [test reopening or never closing schools was not necessarily cassette, nasal swab, empty tube and plug, Pasteur pipette and associated with a significant increase in child-to-child or buffer solution; Panbio™ COVID-19 Ag Rapid Test Device community transmission in children under 14 years of age (2). (Abbot Laboratories, Chicago, US)]. Additionally, the self-test Measures must be adapted to each setting to prevent procedure was recorded on video and distributed to transmission of the virus (3). An important strategy to participating schools. minimize SARS-CoV-2 transmission is the rapid Tests were performed in accordance with biosecurity identification of infected people, symptomatic or not. Non- measures (well-ventilated area, separation between participants pharmaceutical preventive interventions such as screening of >1.5 m, table disinfection with alcohol before and after the asymptomatic people for SARS-CoV-2, have been shown to procedures). Subsequently, acceptability surveys were entered decrease incidence at the community level (3). Antigen into the EUSurvey platform by the research team. detection rapid diagnostic tests (Ag-RDTs) have been All test results were validated. In School B and summer proposed as suitable for point-of-care screening of potentially camps, participants read the test result themselves, and the exposed people. Advantages of Ag-RDTs include: low price, healthcare team validated the reliability, while in School A absence of referral to a high-tech laboratory, short previously trained older pupils (15–16 years old) supervised turnaround time for results and identification of people with the sampling procedure and read the results. potential to transmit their SARS-CoV-2 infection (3) Ag-RDT Positive cases were referred to the health center for However, taking into account that rapid tests are often a Reverse Transcription-PCR (RT-PCR) with nasal swab to developed and marketed when outbreaks are already confirm the results. advanced, should be considered as a medium to long term measure. Making Ag-RDTs available in educational centers could reduce care school closures, costs, response time and Feasibility evaluation eventually SARS-CoV-2 transmission. As nasal Ag-RDT self-testing is considered to be reliable We assessed the acceptability and usability of the and feasible in adults (4, 5), the main objective of this study intervention among participants based on a conceptual was to assess whether it is acceptable and usable in younger validated framework adapted from previous studies (7). Here, ages, by focusing on students and staff in schools and acceptance and use of SARS-CoV-2 Ag-RDT self-testing was summer camps during the fifth wave caused by the Delta adapted and divided into the following subdomains: B.1.617.2 variant of SARS-CoV-2 in Catalonia (Spain). Learnability, Willingness, Suitability, Satisfaction and Efficacy (see Table 1). A semi-structured interview was conducted with trained pupils who read the test results (School A) to assess the Materials and methods acceptability and usability of the experience, this was recorded Study population and period and later transcribed for analysis. The research took place between April and August 2021 in 2 schools [one from COVID-19 Sentinel Schools Network of Data analysis Catalonia (6) and other school from ESCORAT project] and 4 summer camps in Catalonia, Spain. Thus, here students over A descriptive analysis of the sample was carried out and the 9 years old were invited to participate and staff were included percentages of the categorical variables were calculated for each only in summer camps. In one school (School A) a category, stratifying by age group in accordance with the prospective cohort was established (testing weekly for educational stages of Catalonia based on Law 12/2009 of 10 8 weeks) while a cross-sectional study was done in School B July 2009 on education. The p-value was obtained by means Frontiers in Pediatrics 02 frontiersin.org TABLE 1 Acceptability and usability subdomains results by age groups. N = 346, April-August 2021, Catalonia (Spain). Participants by age range Total N 9–11 years 12–15 years 16–18 years 19–56 years p- (%) old N (%) old N (%) old N (%) old N (%) valuea ACCEPTABILITY & Learnability Has anyone helped you to take the self-test? <0.001 Colom-Cadena et al. USABILITYc Frontiers in Pediatrics Yes 30 (8.7%) 12 (27.9%) 18 (13.1%) 0 (0.00%) 0 (0.00%) b No 313 31 (72.1%) 119 (86.9%) 124 (100%) 39 (100%) (91.3%) Were you able to complete the self-test successfully? 1.000 Yes 340 43 (100%) 137 (99.3%) 121 (100%) 39 (100%) (99.7%) Nob 1 (0.3%) 0 (0.00%) 1 (0.72%) 0 (0.00%) 0 (0.00%) How easy or difficult did you find it to take the COVID-19 rapid 0.075 antigen self-test? Very easy + Slightly easy 301 35 (83.3%) 118 (84.3%) 109 (89.3%) 39 (100%) (87.8%) Neither easy nor difficult 38 (11.1%) 7 (16.7%) 19 (13.6%) 12 (9.84%) 0 (0.00%) Slightly difficult + Very difficult 4 (1.1%) 0 (0.00%) 3 (2.14%) 1 (0.82%) 0 (0.00%) 03 Reading success 0.215 Same outcome for participants vs. health workers 270 32 (94.1%) 85 (93.4%) 114 (97.4%) 39 (100%) (96.1%) Different outcome for participants vs. health workers 11 (3.9%) 2 (5.88%) 6 (6.59%) 3 (2.56%) 0 (0.00%) Willingness How much do you agree or disagree with the following statement: “I 0.136 would repeat the COVID-19 antigen rapid self-test in the future"? Strongly agree + Slightly agree 310 34 (89.5%) 119 (91.5%) 120 (98.4%) 37 (94.9%) (94.2%) Neither agree nor disagree 16 (4.86%) 3 (7.89%) 9 (6.92%) 2 (1.64%) 2 (5.13%) Slightly disagree + Strongly disagree 2 (0.61%) 1 (2.63%) 1 (0.77%) 0 (0.00%) 0 (0.00%) Other 1 (0.3%) 0 (0.00%) 1 (0.77%) 0 (0.00%) 0 (0.00%) Would you be willing to repeat this self-antigen test twice a week if 0.008 the epidemiological situation requires it? Yes 292 29 (87.9%) 113 (91.1%) 113 (98.3%) 37 (100%) (94.5%) No 17 (5.5%) 4 (12.1%) 11 (8.87%) 2 (1.74%) 0 (0.00%) If you had to repeat the COVID-19 antigen test, you would prefer to <0.001 frontiersin.org 10.3389/fped.2022.975454 do it in: (continued) TABLE 1 Continued Participants by age range Total N 9–11 years 12–15 years 16–18 years 19–56 years p- (%) old N (%) old N (%) old N (%) old N (%) valuea Health care centre 55 (17.7%) 14 (35.0%) 24 (18.6%) 13 (12.0%) 4 (11.8%) Colom-Cadena et al. Frontiers in Pediatrics At home 224 22 (55.0%) 84 (65.1%) 88 (81.5%) 30 (88.2%) (72.0%) Others 32 (10.3%) 4 (10.0%) 21 (16.3%) 7 (6.48%) 0 (0.00%) Suitability How much do you agree or disagree with the following statement: “I 0.030 am confident that the reading of the result I have made is correct"? Strongly agree + Slightly agree 254 29 (85.3%) 76 (89.4%) 114 (97.4%) 35 (89.7%) (92.4%) Neither agree nor disagree 20 (7.3%) 5 (14.7%) 8 (9.41%) 3 (2.56%) 4 (10.3%) Slightly disagree + Strongly disagree 1 (0.3%) 0 (0.00%) 1 (1.18%) 0 (0.00%) 0 (0.00%) How much do you agree or disagree with the following statement: “I 0.465 trust this type of self-test"? Strongly agree + Slightly agree 241 31 (93.9%) 76 (84.4%) 102 (87.9%) 32 (82.1%) (86.7%) 04 Neither agree nor disagree 30 (10.8%) 2 (6.06%) 12 (13.3%) 12 (10.3%) 4 (10.3%) Slightly disagree + Strongly disagree 7 (2.50%) 0 (0.00%) 2 (2.22%) 2 (1.72%) 3 (7.69%) Satisfaction What is your assessment of the experience of taking the COVID-19 0.099 antigen rapid self-test? Very satisfied + Slightly satisfied 307 36 (90.0%) 119 (86.9%) 113 (93.4%) 39 (100%) (91.1%) Neither satisfied nor dissatisfied 28 (8.31%) 4 (10.0%) 17 (12.4%) 7 (5.79%) 0 (0.00%) Slightly dissatisfied + Very dissatisfied 2 (0.59%) 0 (0.00%) 1 (0.73%) 1 (0.83%) 0 (0.00%) How much do you agree or disagree with the following statement: “I 0.774 would recommend the COVID-19 rapid antigen self-test to a friend"? Strongly agree + Slightly agree 266 33 (94.3%) 85 (93.4%) 112 (94.9%) 36 (92.3%) (94.0%) Neither agree nor disagree 15 (5.3%) 2 (5.71%) 5 (5.49%) 6 (5.08%) 2 (5.13%) Slightly disagree + Strongly disagree 2 (0.7%) 0 (0.00%) 1 (1.10%) 0 (0.00%) 1 (2.56%) a p-value calculated using chi-square test. b Reasons for those who need help or did not succeed on sampling are included as a text in the results section of the manuscript. c The Efficacy subdomain is not included in the table because is defined as the ability to create a network with the main actors of the local health and education system -primary care, epidemiological surveillance service, frontiersin.org 10.3389/fped.2022.975454 educational community, local political agents-, correct communication of results, management of positive cases according to governmental protocols, and appropriate waste management, and results are presented in the aforementioned section. Colom-Cadena et al. 10.3389/fped.2022.975454 of a Chi-square or Fisher test when the frequency was less than Acceptability and usability subdomain results of the survey 5 using R software (version R-4.0.5). are presented in Table 1. Regarding the Learnability subdomain, 91.3% (n = 313) did not need help (Table 1), and those needing help mainly chose: I was too nervous (n = 14; Ethics 48,3%), I needed help adding the buffer solution (n = 2; 6,9%), I needed help reading the result (n = 2; 6,9%) or Other reasons Fundació Institut Universitari per a la recerca a l’Atenció (n = 9; 31%) (data not shown). Primària de Salut Jordi Gol i Gurina (IDIAPJGol) (code 20/ Regarding advantages, most participants identified: Results 192-PCV) and the Ethics and Clinical Research Committee of within minutes (n = 245; 86.0%), Testing at school instead of at the Hospital Universitari Germans Trias (code PI-21-057), a health center (n = 244; 85.6%) and Tests improve safety and approved the study. Informed consent was obtained from all protection against Covid (n = 224; 78.6%); followed by others participants. such as I can take control of my health with respect to Covid (n = 191; 67.0%), It gives me a more relaxed feeling when meeting friends (n = 181; 63.5%), Contributes to the Results normalization of Covid tests (n = 164; 57.5%) and The test is free of charge (n = 160; 56.1%). Regarding disadvantages, the A total of 305 students (88.15%) and 41 staff (11.85%) from majority of participants identified that the test is Less reliable 9 to 56 years old participated in the self-testing procedure and than RT-PCR (n = 213; 76.9%), while a few considered You answered the survey at the end of the study. 207 were women have to interpret the result yourself (n = 48; 17.3%), or Not (60%), 132 were men (38,3%), 4 non-binary people (1,16%), having the emotional and/or logistical support to read the 2 transgender women (0,58%) and one participant with result (n = 17; 6.14%) as disadvantages. no information. Data was grouped in four age groups: 9–11 Regarding test reading, 96.1% of participants (n = 270) (n = 43; 12,4%), 12–15 (n = 140; 40,5%), 16–18 (n = 124; reported the same outcome as the healthcare workers (School 35,8%), 19–56 (n = 39; 11,3%) (Figure 1). B and summer camps). 11 participants (3.91%) scored a FIGURE 1 Summary of the total number of participants in the pilot study, Spain, N: 346. *Self-sampling: In school A, older pupils (15–16 years old) were trained beforehand to read the results of the other participants. ** Self-testing: In School B and summer camps, participants read the test result themselves, and the healthcare team validated the reliability. Frontiers in Pediatrics 05 frontiersin.org Colom-Cadena et al. 10.3389/fped.2022.975454 different outcome to the healthcare workers. Of these, 9 opportunistic sample, and it would be interesting to include students (81,1%) indicated a negative result when the students of younger ages. healthcare worker said positive, and 2 students (18,2%) Due to the current massive use of Ag-RDT in different answered that they don’t know the result, when healthcare countries at the domestic level, more studies on feasibility of worker recorded a negative result. home-based testing in children, both self-testing and family In terms of Efficacy, there was a rapid response and proper testing are needed. management of positive cases, both at the educational and public health levels. Through the semi-structured interview, the students of Conclusions School A reported a positive feeling about the research project; that the study helps to have a safer school and that a weekly The study demonstrates that SARS-CoV-2 antigen self- test is acceptable. However, trained students highlighted the testing with nasal swabs is acceptable and usable for heavy workload, with loss of class hours, and suggested implementation in schools and summer camps with students involvement of more students in the future. and staff, when the epidemiological situation may require a systematic screening of these populations as demonstrated during the 5th Covid wave in Spain. These data have public Discussion health implications and remain of interest in case of emergence of new SARS-CoV-2 variants or other potential Overall, the study demonstrates high acceptability and infectious agents. The strategy would relieve health centers usability of nasal swab Ag-RDT self-tests in students and staff work load, reducing the time it takes travel to health care in our settings. To our knowledge no previous results on centers for the educational community. However, in younger feasibility in-depth account of acceptability and usability in age groups supervision by healthcare or other previously younger groups in educational settings exist, although studies trained in-school personnel is recommended. on specificity and sensitivity of this method do (8). Our results for adults (students and staff) agree with previous studies with rapid antigen and antibody tests (5, 9). Data availability statement The results suggest that self-testing should be done under health workers or trained individuals’ supervision in The raw data supporting the conclusions of this article will participants under 15 years of age; they needed more help be made available by the authors, without undue reservation. and were less willing to repeat the test. Younger participants were also less confident about reading the result. In contrast to other studies, no statistical differences were found between Ethics statement age groups when reading the Ag-RDT result (10). In addition, there was a high (more than 90%) agreement The studies involving human participants were reviewed between self-reported and health care worker validated test and approved by The studies involving human participants readings. were reviewed and approved by Fundació Institut Universitari The results also show that participants of all ages perceive per a la recerca a l’Atenció Primària de Salut Jordi Gol i the turnaround time and not having to travel to a health Gurina (IDIAPJGol) (code 20/192-PCV) and the Ethics and center as positive elements of the experience. It has been Clinical Research Committee of the Hospital Universitari suggested that Ag-RDT self-testing can be a good tool for Germans Trias (code PI-21-057), approved the study. the monitoring outbreaks, avoiding health care bottlenecks and participants older than 16 years old or the participants’ legal improving access to diagnosis in places with less access to guardian of participants under 16 provided their written PCR laboratory tests. It also puts the patient at the center of informed consent to participate in this study. Written the management of an infectious disease (3, 11). However, informed consent to participate in this study was provided by risk must be considered in the actions taken by each the participants’ legal guardian/next of kin. individual in the event of a positive case in relation to existing public health measures. Also, in an epidemic context, rapid tests are often developed and made commercially available at Author contributions late stages, and therefore have to be considered as a medium to long term tool for outbreak management. CA, JC and BR: contributed to the conceptualisation of the The study has some limitations to be noted. The number of study and funding acquisition. ACC, HMR, AB, LAG, MMF, participants was small -especially with regard to the PRdG, JVA, ESS, JML, BR, JC and CA: contributed to the representation of certain age groups- it is based on an investigation. LAG and MMF: were responsible for data Frontiers in Pediatrics 06 frontiersin.org Colom-Cadena et al. 10.3389/fped.2022.975454 analysis. ACC and HMR: were responsible for writing the en Salut (DGRIS) and Institut Català de la Salut (ICS) that original draft. All authors contributed to the article and made this project possible, the town council of Vilassar de approved the submitted version.. Dalt and Lloret de Mar, and all the health care professionals acting as a COVID-19 pandemic health taskforce in Catalonia. Funding This work was supported by the Ministry of Health of the Conflict of interest Government of Catalonia with no grant number. This funding The authors declare that the research was conducted in the source had no role in the design of this study and any role during its execution, analyses, interpretation of the data or absence of any commercial or financial relationships that could be construed as a potential conflict of interest. decision to submit results. Acknowledgment Publisher’s note The authors would like to thank the schools and summer All claims expressed in this article are solely those of the camps and all the staff and students who participated. Thanks especially to Marina Herrero, Isabel Martínez, Juan Rus, Pilar authors and do not necessarily represent those of their Bonamusa and Gema Ballega from the research field team. affiliated organizations, or those of the publisher, the editors Also, we would like to thank the Department of Health and and the reviewers. Any product that may be evaluated in this Department of Education of the Government of the Catalonia article, or claim that may be made by its manufacturer, is not (Spain), the former Direcció General de Recerca i Innovació guaranteed or endorsed by the publisher. References 1. López-Bueno R, López-Sánchez GF, Casajús JA, Gil-Salmerón A, Grabovac I, sentinel network of schools. BMJ Open. (2022) 12:e055649. doi: 10.1136/ Tully MA, et al. Health-Related behaviors among school aged children bmjopen-2021-055649 and adolescents during the spanish COVID-19 confinement. Front Pediatr. 7. 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