Science Brief: Transmission of SARS-CoV-2 in K-12 schools

Science Brief: Transmission of SARS-CoV-2 in K-12 schools

Background

Schools are an important part of the infrastructure of communities. They provide safe, supportive learning environments for students and employ teachers and other staff.1 Schools also provide critical services including school meal programs and social, physical, behavioral, and mental health services.1,2 Schools have indirect benefits to the community, including enabling parents, guardians, and caregivers to work.1,3 In the spring of 2020, all public kindergarten to grade 12 (K-12) schools in the United States closed for in-person instruction as a strategy to slow the spread of SARS-CoV-2. With the beginning of the fall term 2020, K-12 schools have variably used several models of instruction, including in-person, virtual, and hybrid models of instruction. Other countries have opened schools at varying points in the pandemic. Their experiences have contributed to our knowledge of the nature of SARS-CoV-2 transmission in schools and their surrounding communities.

COVID-19 among children and adolescents

Although children can be infected with SARS-CoV-2, can get sick from COVID-19, and can spread the virus to others, less than 10% of COVID-19 cases in the United States have been among children and adolescents aged 5–17 years (COVID Data Tracker). Compared with adults, children and adolescents who have COVID-19 are more commonly asymptomatic (never develop symptoms) or have mild, non-specific symptoms.4-11 Similar to adults with SARS-CoV-2 infections, children can spread SARS-CoV-2 to others when they don’t have symptoms or have mild, non-specific symptoms and thus might not know that they are infected and infectious. Children are less likely to develop severe illness or die from COVID-19.6,12-15 Nonetheless, 203 COVID-19 deaths among persons ages 0–18 have been reported to the National Center for Health Statistics through January 27, 2021. Although rates of severe outcomes from COVID-19 including mortality and hospitalization in school-aged children are low,16,17 health disparities in the occurrence of severe disease are evident in childhood. Hispanic ethnicity and Black race are associated with increased risks for hospitalization and ICU admission among children.16 Underlying medical conditions are also more commonly reported among children who are hospitalized or admitted to an ICU.16

Evidence from several studies suggests that children and adolescents may be less commonly infected with SARS-CoV-2 than adults.18-25 The proportion of persons infected among those exposed to SARS-CoV-2 is one measure of susceptibility to infection. The biological mechanisms underlying children’s decreased susceptibility to COVID-19 are unclear; proposed mechanisms include decreased expression of ACE2 receptors26 in the respiratory tract and age-related differences in immune response to SARS-CoV-2.14,27,28 However, children generally have a lower risk of cumulative exposures and a lower likelihood of being tested compared with adults. For these reasons, it is difficult to determine how much of an observed difference in detected infection rates between children and adults may be attributed to biological differences. Household transmission investigations and population screening studies during periods when schools are open for in-person instruction likely provide the strongest methods to evaluate risk of infection in children relative to adults. Some studies using such methods have demonstrated infection rates in children similar to those observed in adults.7 Other evidence suggests that differences in susceptibility between children and adults is not entirely due to lack of testing because children are more likely to be asymptomatic or show mild symptoms.5,18-20,22,29,30 For example, several population screening studies found lower incidences of SARS-CoV-2 infection among children under age 10 compared with adolescents or adults.18,21,24 Studies that traced household contacts and tested all contacts of index cases, regardless of symptom status, have also found lower rates of infection among children compared with adults.19,20,23,25 The questions of susceptibility and infectivity among children and adolescents require further study to explore potential explanations and mechanisms.

Younger children (<10 years of age) may be less likely to be infected than adolescents.21,22,29 This possibility is supported by contact tracing studies;29,31 test positivity data from children, adolescents, and adults;16,17 and population screening studies using seroprevalence data.18,21 Susceptibility to SARS-CoV-2 infection and the proportion among those infected experiencing symptoms both generally increase with age.5

Schools and SARS-CoV-2 transmission

Based on the data available, in-person learning in schools has not been associated with substantial community transmission. Although national COVID-19 case incidence rates among children and adolescents have risen over time, this trend parallels trends observed among adults.17 Increases in case incidence among school-aged children and school reopenings do not appear to pre-date increases in community transmission.17,32-34

For schools to provide in-person learning, associations between levels of community transmission and risk of transmission in school should be considered.32 If community transmission is high, students and staff are more likely to come to school while infectious, and COVID-19 can spread more easily in schools.

Some studies have found that it is possible for communities to reduce incidence of COVID-19 while keeping schools open for in-person instruction.10,20 A study comparing county-level COVID-19 hospitalizations between counties with in-person learning and those without in-person learning found no effect of in-person school reopening on COVID-19 hospitalization rates when baseline hospitalization rates were low or moderate.35 The association between COVID-19 incidence and transmission in school settings and levels of community transmission underscores the importance of controlling disease spread in the community to protect teachers, staff, and students in schools.32

Some outbreaks have occurred in schools, leading to closures.36,37 Significant secondary transmission of SARS-CoV-2 infection can and does occur in school settings when mitigation strategies are not implemented or are not followed.36 When outbreaks occur in school settings, they tend to result in increased transmission among teachers and school staff rather than among students. In Israel, high schools were closed less than two weeks after reopening when two symptomatic students attended in-person learning, leading to 153 cases among students and 25 among staff members, from among 1,161 students and 151 staff members tested.36 Importantly, mitigation strategies were not adhered to – including lifting of a mask requirement because of a heat wave and classroom crowding.

Though outbreaks do occur in school settings, multiple studies have shown that transmission within school settings is typically lower than – or at least similar to – levels of community transmission, when mitigation strategies are in place in schools. Enhanced national surveillance data from the United Kingdom (UK) showed an association between regional COVID-19 incidence and incidence in schools. For every 5 additional cases per 100,000 population in regional incidence, the risk of a school outbreak increased by 72%.32 Few cases in Australian schools were reported when community transmission levels were low, and cases in schools increased when community transmission increased.3 In Michigan and Washington, delivery of in-person instruction was not associated with increased spread of COVID-19 in schools when community transmission was low, but cases in schools did increase at moderate-to-high levels of community transmission.38 When community transmission was low, there was no association between in-person learning and community spread.38

International and domestic experiences have demonstrated that even when a school carefully coordinates, plans, and prepares for reopening, cases of COVID-19 may still occur.39 Expecting and planning for the occurrence of one or more cases of COVID-19 in schools can help schools respond immediately to minimize spread within schools and allow the school to remain open for in-person learning.

SARS-CoV-2 transmission among students, families, and teachers and school staff

Based on the greater risk of severe illness and death among adults with COVID-19, reasonable concerns have been raised about the occupational risk of SARS-CoV-2 infection for teachers and school staff. Evidence suggests that staff-to-staff transmission is more common than transmission from students to staff, staff to student, or student to student.32,34,36,40,41 In the large UK study mentioned, for example, most outbreak cases were associated with an index case in a staff member.32 Therefore, school interventions should include measures to reduce transmission among staff members. Detection of cases in schools does not necessarily mean that transmission occurred in schools. The majority of cases that are acquired in the community and are brought into a school setting result in limited spread inside schools, if comprehensive mitigation strategies are in place.39,42,53,54

Findings from several studies suggest that SARS-CoV-2 transmission among students is relatively rare. An Australian study of 39 COVID-19 cases among students (32 students) and staff (7 staff) traced contacts across 28 schools and 6 early childhood centers and found only 44 secondary positive cases (28 students, 5 staff members) out of 3,439 close child contacts and 385 close staff contacts.44,47 Several contact tracing studies have found limited student-to-student transmission in schools.34,40,45 A study of factors associated with SARS-CoV-2 infection among children and adolescents in Mississippi found that school attendance was not associated with a positive SARS-CoV-2 test result. However, close contacts with persons with COVID-19, attending gatherings, and having visitors in the home were associated with SARS-CoV-2 infections among children and adolescents.43 The evidence to date suggests that staff-to-student and student-to-student transmission are not the primary means of exposure to SARS-CoV-2 among infected children. Several studies have also concluded that students are not the primary sources of exposure to SARS-CoV-2 among adults in school settings.34,46,47

There is some evidence to indicate that COVID-19 might spread more easily within high school settings than in elementary school settings.22 For example, researchers in Italy identified and tested nearly all (99.8%) contacts of 1,198 cases in school settings and reported a lower attack rate in elementary schools (1 secondary case; 0.38% attack rate) than the attack rate in middle and high schools (37 secondary cases; 6.46% attack rate).48 This pattern was consistent with findings from a study in New South Wales, Australia, that reported higher attack rates in high schools than in elementary/primary schools.44 It is possible that the apparent increased risk of SARS-CoV-2 transmission among adolescents may be in part attributable to more social interactions with non-household members outside schools.49 Nonetheless, evidence for greater transmission in middle schools and high schools compared with elementary schools suggests that the former may need to move more quickly to virtual instruction when community transmission is high.32

School in-person learning and mitigation

When mitigation strategies – especially mask use and physical distancing – are consistently and correctly used, the risk of transmission in the school environment is decreased.50 CDC’s school guidance for COVID-19 emphasizes 5 key mitigation strategies: consistent and correct use of masks, physical distancing, handwashing and respiratory etiquette, cleaning and ventilation, and contact tracing in combination with isolation and quarantine. Use of multiple strategies – sometimes called layered mitigation – provides greater protection in breaking transmission chains than implementing a single strategy.51 The guidance recommends layering two or more mitigation strategies, with particular emphasis on universal use of masks and physical distancing.

Studies of COVID-19 transmission in schools that used consistent implementation of multiple mitigation strategies have shown success in limiting transmission in schools.32,35,39,52 A study of 11 school districts in North Carolina with in-person learning for at least 9 weeks during the fall 2020 semester reported minimal school-related transmission even while community transmission was high. These schools implemented and strictly adhered to multiple mitigation strategies, including universal mask use and physical distancing. Breaches in mask use likely explained the few instances of in-school spread of SARS-CoV-2.39 A study of Italian schools, which implemented a comprehensive mitigation approach that included layered mitigation and cancellation of extracurricular activities, found that school reopening was not associated with the second wave of COVID-19 in Italy.34 Similarly, a surveillance study of symptomatic and asymptomatic children in Swiss schools found limited secondary transmission when multiple protective measures were used in schools,53 including mask use, physical distancing, and other interventions. Data from surveillance of German school outbreaks detected outbreaks before any mitigation strategies were implemented. After schools reopened with mitigation strategies in place, the average number of outbreaks and cases was smaller, suggesting that mitigation strategies had some protective effect.37 A study of private schools that reopened for in-person instruction in Chicago revealed that implementation of layered mitigation found minimal in-school transmission.54 When a combination of effective mitigation strategies is implemented and strictly adhered to in the K-12 in-person learning environment, the risk of transmission in the school setting appears to be lower than or equivalent to the transmission risk in other community settings.34

Sports and other extracurricular activities

Many sports or other types of group extracurricular activities can increase the risk of SARS-CoV-2 transmission for participants, coaches, and spectators.55-58 Participation in extracurricular activities and sports may also increase the risk of SARS-CoV-2 transmission among other students, teachers, and staff.58-60 Close contact team sports and indoor sports such as wrestling appear to represent particularly high-risk activities, because participants cannot maintain at least 6 feet of distance from others and ventilation may be limited.57,58 Intense exercise causes participants to breathe heavily, which can cause potentially infected respiratory droplets to travel further than they would from persons at rest upon exhaling.57 Other extracurricular activities, especially ones that occur indoors and involve shouting or singing, also increase risk of transmission if a participant is infectious, because respiratory droplets may travel a greater distance and at a higher velocity.61 For these reasons, strategies to control COVID-19 transmission in schools should take the role of sports and other extracurricular activities into account, as well as differences in transmission dynamics for these activities compared with in-person instruction.

Conclusions

COVID-19 transmission in schools is associated with community transmission. Transmission spread within schools can be limited with strict implementation of layered mitigation strategies.14,32,34 When community rates of COVID-19 are high, there is an increased likelihood that SARS-CoV-2 will be introduced to, and potentially transmitted within, a school setting. Evidence to date suggests that when schools implement mitigation strategies with fidelity, transmission within schools can be limited.

Reducing transmission in schools is a shared responsibility. A combination of effective mitigation strategies (including consistent and correct use of masks; physical distancing; handwashing and respiratory etiquette; cleaning and maintaining healthy facilities; and contact tracing in combination with isolation and quarantine) implemented with strict adherence can limit transmission in the school setting. CDC has developed guidance for mitigation strategies that K-12 school administrators can use to help protect students, teachers, and staff and slow the spread of COVID-19, as well as other tools and resources to assist with implementation of mitigation strategies and returning to in-person learning.

 

References
    1. National Academies of Sciences, Engineering, and Medicine (NASEM). Reopening K-12 Schools During the COVID-19 Pandemic: Prioritizing Health, Equity, and Communities. Consensus study report from The National Academies Press. 2020; doi:10.17226/25858
    2. Donohue JM, Miller E. COVID-19 and School Closures. JAMA. 2020;324(9):845-847. doi:10.1001/jama.2020.13092
    3. Russell FM, Ryan K, Snow K, Danchin M, Mulholland K, Goldfeld S. COVID-19 in Victorian Schools: An analysis of child-care and school outbreak data and evidence-based recommendations for opening schools and keeping them open. Report from Murdoch Children’s Research Institute and the University of Melbourne. 2020; Published 2020 September 25.
    4. CDC COVID-19 Response Team. Coronavirus Disease 2019 in Children — United States, February 12–April 2, 2020. MMWR Morb Mortal Wkly Rep. 2020;69(14):422-426. Published 2020 April 10. doi:10.15585/mmwr.mm6914e4
    5. Davies NG, Klepac P, Liu Y, et al. Age-dependent effects in the transmission and control of COVID-19 epidemics. Nat Med. 2020;26(8):1205-1211. doi:10.1038/s41591-020-0962-9
    6. Dong Y, Mo X, Hu Y, et al. Epidemiology of COVID-19 Among Children in China. Pediatrics. 2020;145(6):e20200702. doi:10.1542/peds.2020-0702
    7. Laws RL, Chancey RJ, Rabold EM, et al. Symptoms and Transmission of SARS-CoV-2 Among Children — Utah and Wisconsin, March–May 2020. Pediatrics. 2021;147(1):e2020027268. doi:10.1542/peds.2020-027268
    8. Lee B, Raszka WV. COVID-19 in Children: Looking Forward, Not Back. Pediatrics. 2021;147(1):e2020029736. doi:10.1542/peds.2020-029736
    9. Lu X, Zhang L, Du H, et al. SARS-CoV-2 Infection in Children. N Engl J Med. 2020;382(17):1663-1665. doi:10.1056/NEJMc2005073
    10. Ludvigsson JF. Children are unlikely to be the main drivers of the COVID‐19 pandemic – A systematic review. Acta Paediatr. 2020;109(8):1525-1530. doi:10.1111/apa.15371
    11. Munro APS, Faust SN. COVID-19 in children: current evidence and key questions. Curr Opin Infect Dis. 2020;33(6):540-547. doi:10.1097/QCO.0000000000000690
    12. Castagnoli R, Votto M, Licari A, et al. Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Infection in Children and Adolescents: A Systematic Review. JAMA Pediatr. 2020;174(9):882-889. doi:10.1001/jamapediatrics.2020.1467
    13. Choi SH, Kim HW, Kang JM, Kim DH, Cho EY. Epidemiology and clinical features of coronavirus disease 2019 in children. Clin Exp Pediatr. 2020;63(4):125-132. doi:10.3345/cep.2020.00535
    14. Zimmermann P, Curtis N. Why is COVID-19 less severe in children? A review of the proposed mechanisms underlying the age-related difference in severity of SARS-CoV-2 infections. Arch Dis Child. 2020;archdischild-2020-320338. Published online ahead of print 2020 December 1. doi:10.1136/archdischild-2020-320338
    15. Götzinger F, Santiago-García B, Noguera-Julián A, et al. COVID-19 in children and adolescents in Europe: a multinational, multicentre cohort study. Lancet Child Adolesc Health. 2020;4(9):653-661. doi:10.1016/S2352-4642(20)30177-2
    16. Leeb RT, Price S, Sliwa S, et al. COVID-19 Trends Among School-Aged Children — United States, March 1–September 19, 2020. MMWR Morb Mortal Wkly Rep. 2020;69(39):1410-1415. Published 2020 Oct 2. doi:10.15585/mmwr.mm6939e2
    17. Leidman E, Duca LM, Omura JD, Proia K, Stephens JW, Sauber-Schatz EK. COVID-19 Trends Among Persons Aged 0–24 Years — United States, March 1–December 12, 2020. MMWR Morb Mortal Wkly Rep. 2021;70(3):88-94. Published 2021 January 22. doi:10.15585/mmwr.mm7003e1
    18. Gudbjartsson DF, Helgason A, Jonsson H, et al. Spread of SARS-CoV-2 in the Icelandic Population. N Engl J Med. 2020;382(24):2302-2315. doi:10.1056/NEJMoa2006100
    19. Madewell ZJ, Yang Y, Longini IM, Halloran ME, Dean NE. Household Transmission of SARS-CoV-2: A Systematic Review and Meta-analysis. JAMA Netw Open. 2020;3(12):e2031756. doi:10.1001/jamanetworkopen.2020.31756
    20. Zhang J, Litvinova M, Liang Y, et al. Changes in contact patterns shape the dynamics of the COVID-19 outbreak in China. Science. 2020;368(6498):1481-1486. doi:10.1126/science.abb8001
    21. Viner RM, Mytton OT, Bonell C, et al. Susceptibility to SARS-CoV-2 Infection Among Children and Adolescents Compared With Adults: A Systematic Review and Meta-analysis. JAMA Pediatr. 2020;e204573. Published online ahead of print 2020 Sep 25. doi:10.1001/jamapediatrics.2020.4573
    22. Goldstein E, Lipsitch M, Cevik M. On the Effect of Age on the Transmission of SARS-CoV-2 in Households, Schools, and the Community. J Infect Dis. 2020; Published online 2020 October 29. doi:10.1093/infdis/jiaa691
    23. Somekh E, Gleyzer A, Heller E, et al. The Role of Children in the Dynamics of Intra Family Coronavirus 2019 Spread in Densely Populated Area. Pediatr Infect Dis J. 2020;39(8):e202-e204. doi:10.1097/INF.0000000000002783
    24. Lavezzo E, Franchin E, Ciavarella C, et al. Suppression of a SARS-CoV-2 outbreak in the Italian municipality of Vo’. Nature. 2020;584(7821):425-429. doi:10.1038/s41586-020-2488-1
    25. Zhu Y, Bloxham CJ, Hulme KD, et al. A meta-analysis on the role of children in SARS-CoV-2 in household transmission clusters. Clin Infect Dis. 2020;ciaa1825. Published online ahead of print 2020 December 6. doi:10.1093/cid/ciaa1825
    26. Bunyavanich S, Do A, Vicencio A. Nasal Gene Expression of Angiotensin-Converting Enzyme 2 in Children and Adults. JAMA. 2020;323(23):2427-2429. doi:10.1001/jama.2020.8707
    27. Carsetti R, Quintarelli C, Quinti I, et al. The immune system of children: the key to understanding SARS-CoV-2 susceptibility?. Lancet Child Adolesc Health. 2020;4(6):414-416. doi:10.1016/S2352-4642(20)30135-8
    28. Weisberg SP, Connors TJ, Zhu Y, et al. Distinct antibody responses to SARS-CoV-2 in children and adults across the COVID-19 clinical spectrum. Nat Immunol. 2021;22(1):25-31. doi:10.1038/s41590-020-00826-9
    29. Dattner I, Goldberg Y, Katriel G, et al. The role of children in the spread of COVID-19: Using household data from Bnei Brak, Israel, to estimate the relative susceptibility and infectivity of children. Preprint. MedRxiv. 2020; Posted online 2020 October 11. doi:10.1101/2020.06.03.20121145
    30. Park YJ, Choe YJ, Park O, et al. Contact Tracing during Coronavirus Disease Outbreak, South Korea, 2020. Emerg Infect Dis. 2020;26(10):2465-2468. doi:10.3201/eid2610.201315
    31. Hu S, Wang W, Wang Y, et al. Infectivity, susceptibility, and risk factors associated with SARS-CoV-2 transmission under intensive contact tracing in Hunan, China. Preprint. MedRxiv. 2020; Posted online 2020 November 3. doi:10.1101/2020.07.23.20160317
    32. Ismail SA, Saliba V, Lopez Bernal J, Ramsay ME, Ladhani SN. SARS-CoV-2 infection and transmission in educational settings: a prospective, cross-sectional analysis of infection clusters and outbreaks in England. Lancet Infect Dis. 2020;S1473-3099(20)30882-3. Published online ahead of print 2020 December 8. doi:10.1016/S1473-3099(20)30882-3
    33. Aleta A, Moreno Y. Age differential analysis of COVID-19 second wave in Europe reveals highest incidence among young adults. Preprint. MedRxiv. 2020; Posted 2020 November 13. doi:10.1101/2020.11.11.20230177
    34. Gandini S, Rainisio M, Iannuzzo ML, Bellerba F, Cecconi F, Scorrano L. No evidence of association between schools and SARS-CoV-2 second wave in Italy. Preprint. MedRxiv. 2021; Posted online 2021 January 8. doi:10.1101/2020.12.16.20248134
    35. Harris DN, Ziedan E, Hassig S. The Effects of School Reopenings on COVID-19 Hospitalizations. Technical Report from the National Center for Research on Education Access and Choice (REACH). 2021; Published 2021 January 4.
    36. Stein-Zamir C, Abramson N, Shoob H, et al. A large COVID-19 outbreak in a high school 10 days after schools’ reopening, Israel, May 2020. Euro Surveill. 2020;25(29):2001352. doi:10.2807/1560-7917.ES.2020.25.29.2001352
    37. Otte Im Kampe E, Lehfeld AS, Buda S, Buchholz U, Haas W. Surveillance of COVID-19 school outbreaks, Germany, March to August 2020. Euro Surveill. 2020;25(38):2001645. doi:10.2807/1560-7917.ES.2020.25.38.2001645
    38. Goldhaber D, Imberman SA, Strunk KO, et al. To What Extent Does In-Person Schooling Contribute to the Spread of COVID-19? Evidence from Michigan and Washington. Report from the Center for Education Data & Research (CEDR), National Center for Analysis of Longitudinal Data in Education Research (CALDER), and Education Policy Innovation Collaborative (EPIC). 2020; Published 2020 December.
    39. Zimmerman KO, Akinboyo IC, Brookhart A, et al. Incidence and Secondary Transmission of SARS-CoV-2 Infections in Schools. Pediatrics. 2021;e2020048090. Published online ahead of print 2021 January 8. doi:10.1542/peds.2020-048090
    40. Yung CF, Kam KQ, Nadua KD, et al. Novel coronavirus 2019 transmission risk in educational settings. Clin Infect Dis. 2020;ciaa794. Published online ahead of print 2020 June 25. doi:10.1093/cid/ciaa794
    41. Ehrhardt J, Ekinci A, Krehl H, et al. Transmission of SARS-CoV-2 in children aged 0 to 19 years in childcare facilities and schools after their reopening in May 2020, Baden-Württemberg, Germany. Euro Surveill. 2020;25(36):2001587. doi:10.2807/1560-7917.ES.2020.25.36.2001587
    42. Falk A, Benda A, Falk P, Steffen S, Wallace Z, Høeg TB. COVID-19 Cases and Transmission in 17 K–12 Schools — Wood County, Wisconsin, August 31–November 29, 2020. MMWR Morb Mortal Wkly Rep. 2021;70(4):136-140. Published 2021 January 29. doi:10.15585/mmwr.mm7004e3
    43. Hobbs CV, Martin LM, Kim SS, et al. Factors Associated with Positive SARS-CoV-2 Test Results in Outpatient Health Facilities and Emergency Departments Among Children and Adolescents Aged <18 Years — Mississippi, September–November 2020. MMWR Morb Mortal Wkly Rep. 2020;69(50):1925-1929. Published 2020 December 18. doi:10.15585/mmwr.mm6950e3
    44. National Centre for Immunisation Research and Surveillance (NCIRS). COVID-19 in schools and early childhood education and care services – the Term 3 experience in NSW. Report from National Centre for Immunisation Research and Surveillance (NCIRS). 2020; Published 2020 October 21.
    45. Dub T, Erra E, Hagberg L, et al. Transmission of SARS-CoV-2 following exposure in school settings: experience from two Helsinki area exposure incidents. Preprint. MedRxiv. 2020; Posted 2020 July 30. doi:10.1101/2020.07.20.20156018
    46. 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):2000903. doi:10.2807/1560-7917.ES.2020.25.21.2000903
    47. Macartney K, Quinn HE, Pillsbury AJ, et al. Transmission of SARS-CoV-2 in Australian educational settings: a prospective cohort study. Lancet Child Adolesc Health. 2020;4(11):807-816. doi:10.1016/S2352-4642(20)30251-0
    48. Larosa E, Djuric O, Cassinadri M, et al. Secondary transmission of COVID-19 in preschool and school settings in northern Italy after their reopening in September 2020: a population-based study. Euro Surveill. 2020;25(49):2001911. doi:10.2807/1560-7917.ES.2020.25.49.2001911
    49. Murillo-Llorente MT, Perez-Bermejo M. COVID-19: Social Irresponsibility of Teenagers Towards the Second Wave in Spain. J Epidemiol. 2020;30(10):483. doi:10.2188/jea.JE20200360
    50. Honein MA, Barrios LC, Brooks JT. Data and Policy to Guide Opening Schools Safely to Limit the Spread of SARS-CoV-2 Infection. JAMA. 2021;10.1001/jama.2021.0374. Published online ahead of print 2021 January 26. doi:10.1001/jama.2021.0374
    51. Honein MA, Christie A, Rose DA, et al. Summary of Guidance for Public Health Strategies to Address High Levels of Community Transmission of SARS-CoV-2 and Related Deaths, December 2020. MMWR Morb Mortal Wkly Rep. 2020;69(49):1860-1867. Published 2020 Dec 11. doi:10.15585/mmwr.mm6949e2
    52. Brandal LT, Ofitserova TS, Meijerink H, et al. Minimal transmission of SARS-CoV-2 from paediatric COVID-19 cases in primary schools, Norway, August to November 2020. Euro Surveill. 2021;26(1):2002011. doi:10.2807/1560-7917.ES.2020.26.1.2002011
    53. Kriemler S, Ulyte A, Ammann P, et al. Surveillance of acute SARS-CoV-2 infections in school children and point-prevalence during a time of high community transmission in Switzerland. Preprint. MedRxiv. 2020; Posted 2020 December 26. doi:10.1101/2020.12.24.20248558
    54. Fricchione MJ, Seo JY, Arwady MA. Data-Driven Reopening of Urban Public Education Through Chicago’s Tracking of COVID-19 School Transmission. J Public Health Manag Pract. 2020; Published online ahead of print 2020 December 30. doi:10.1097/PHH.0000000000001334
    55. Jang S, Han SH, Rhee JY. Cluster of Coronavirus Disease Associated with Fitness Dance Classes, South Korea. Emerg Infect Dis. 2020;26(8):1917-1920. doi:10.3201/eid2608.200633
    56. Bae S, Kim H, Jung TY, et al. Epidemiological Characteristics of COVID-19 Outbreak at Fitness Centers in Cheonan, Korea. J Korean Med Sci. 2020;35(31):e288. Published 2020 August 10. doi:10.3346/jkms.2020.35.e288
    57. Atrubin D, Wiese M, Bohinc B. An Outbreak of COVID-19 Associated with a Recreational Hockey Game — Florida, June 2020. MMWR Morb Mortal Wkly Rep. 2020;69(41):1492-1493. Published 2020 October 16. doi:10.15585/mmwr.mm6941a4
    58. Atherstone C, Siegel M, Schmitt-Matzen E, et al. SARS-CoV-2 Transmission Associated with High School Wrestling Tournaments — Florida, December 2020–January 2021. MMWR Morb Mortal Wkly Rep. 2021;70(4):141-143. Published 2021 Jan 29. doi:10.15585/mmwr.mm7004e4
    59. Hamner L, Dubbel P, Capron I, et al. High SARS-CoV-2 Attack Rate Following Exposure at a Choir Practice — Skagit County, Washington, March 2020. MMWR Morb Mortal Wkly Rep. 2020;69(19):606-610. Published 2020 May 15. doi:10.15585/mmwr.mm6919e6
    60. Charlotte N. High Rate of SARS-CoV-2 Transmission Due to Choir Practice in France at the Beginning of the COVID-19 Pandemic. J Voice. 2020;S0892-1997(20)30452-5. Published online ahead of print 2020 December 23. doi:10.1016/j.jvoice.2020.11.029
    61. Bahl P, de Silva C, Bhattacharjee S, et al. Droplets and Aerosols Generated by Singing and the Risk of Coronavirus Disease 2019 for Choirs. Clin Infect Dis. 2020;ciaa1241. Published online ahead of print 2020 Sep 18. doi:10.1093/cid/ciaa1241