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Abstract

Background

Children’s role in SARS-CoV-2 epidemiology remains unclear. We investigated an initially unnoticed SARS-CoV-2 outbreak linked to schools in northern France, beginning as early as mid-January 2020.

Aims

This retrospective observational study documents the extent of SARS-CoV-2 transmission, linked to an affected high school (n = 664 participants) and primary schools (n = 1,340 study participants), in the context of unsuspected SARS-CoV-2 circulation and limited control measures.

Methods

Between 30 March and 30 April 2020, all school staff, as well as pupils and their parents and relatives were invited for SARS-CoV-2 antibody testing and to complete a questionnaire covering symptom history since 13 January 2020.

Results

In the high school, infection attack rates were 38.1% (91/239), 43.4% (23/53), and 59.3% (16/27), in pupils, teachers, and non-teaching staff respectively vs 10.1% (23/228) and 12.0% (14/117) in the pupils’ parents and relatives (p < 0.001). Among the six primary schools, three children attending separate schools at the outbreak start, while symptomatic, might have introduced SARS-CoV-2 there, but symptomatic secondary cases related to them could not be definitely identified. In the primary schools overall, antibody prevalence in pupils sharing classes with symptomatic cases was higher than in pupils from other classes: 15/65 (23.1%) vs 30/445 (6.7%) (p < 0.001). Among 46 SARS-CoV-2 seropositive pupils < 12 years old, 20 were asymptomatic. Whether past HKU1 and OC43 seasonal coronavirus infection protected against SARS-CoV-2 infection in 6–11 year olds could not be inferred.

Conclusions

Viral circulation can occur in high and primary schools so keeping them open requires consideration of appropriate control measures and enhanced surveillance.

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This work is licensed under a Creative Commons Attribution 4.0 International License.
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2021-04-15
2025-05-21
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References

  1. Cauchemez S, Valleron AJ, Boëlle PY, Flahault A, Ferguson NM. Estimating the impact of school closure on influenza transmission from Sentinel data. Nature. 2008;452(7188):750-4.  https://doi.org/10.1038/nature06732  PMID: 18401408 
  2. Epidemiology Working Group for NCIP Epidemic Response, Chinese Center for Disease Control and Prevention. [The epidemiological characteristics of an outbreak of 2019 novel coronavirus diseases (COVID-19) in China]. Zhonghua Liu Xing Bing Xue Za Zhi. 2020;41(2):145-51. PMID: 32064853 
  3. Bialek S, Gierke R, Hughes M, McNamara LA, Pilishvili T, Skoff T, 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):422-6.  https://doi.org/10.15585/mmwr.mm6914e4  PMID: 32271728 
  4. Riccardo F, Ajelli M, Andrianou X, et al. Epidemiological characteristics of COVID-19 cases in Italy and estimates of the reproductive numbers one month into the epidemic. Medrxiv 2020; doi:  https://doi.org/10.1101/2020.04.08.20056861 .
  5. Dong Y, Mo X, Hu Y, Qi X, Jiang F, Jiang Z, et al. Epidemiology of Covid-19 among children in China. Pediatrics. 2020;145(6):e20200702.  https://doi.org/10.1542/peds.2020-0702  PMID: 32179660 
  6. Shekerdemian LS, Mahmood NR, Wolfe KK, Riggs BJ, Ross CE, McKiernan CA, et al. , International COVID-19 PICU Collaborative. Characteristics and Outcomes of Children With Coronavirus Disease 2019 (COVID-19) Infection Admitted to US and Canadian Pediatric Intensive Care Units. JAMA Pediatr. 2020;174(9):868-73.  https://doi.org/10.1001/jamapediatrics.2020.1948  PMID: 32392288 
  7. Viner RM, Mytton OT, Bonell C, Melendez-Torres GJ, 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.  https://doi.org/10.1001/jamapediatrics.2020.4573  PMID: 32975552 
  8. Stringhini S, Wisniak A, Piumatti G, Azman AS, Lauer SA, Baysson H, et al. Seroprevalence of anti-SARS-CoV-2 IgG antibodies in Geneva, Switzerland (SEROCoV-POP): a population-based study. Lancet. 2020;396(10247):313-9.  https://doi.org/10.1016/S0140-6736(20)31304-0  PMID: 32534626 
  9. Qiu H, Wu J, Hong L, Luo Y, Song Q, Chen D. Clinical and epidemiological features of 36 children with coronavirus disease 2019 (COVID-19) in Zhejiang, China: an observational cohort study. Lancet Infect Dis. 2020;20(6):689-96.  https://doi.org/10.1016/S1473-3099(20)30198-5  PMID: 32220650 
  10. Bi Q, Wu Y, Mei S, Ye C, Zou X, Zhang Z, et al. Epidemiology and transmission of COVID-19 in 391 cases and 1286 of their close contacts in Shenzhen, China: a retrospective cohort study. Lancet Infect Dis. 2020;20(8):911-9.  https://doi.org/10.1016/S1473-3099(20)30287-5  PMID: 32353347 
  11. Jiehao C, Jin X, Daojiong L, Zhi Y, Lei X, Zhenghai Q, et al. A Case series of children with 2019 novel coronavirus infection: clinical and epidemiological features. Clin Infect Dis. 2020;71(6):1547-51.  https://doi.org/10.1093/cid/ciaa198  PMID: 32112072 
  12. Cevik M, Tate M, Lloyd O, Maraolo AE, Schafers J, Ho A. SARS-CoV-2, SARS-CoV, and MERS-CoV viral load dynamics, duration of viral shedding, and infectiousness: a systematic review and meta-analysis. Lancet Microbe. 2021;2(1):e13-22.  https://doi.org/10.1016/S2666-5247(20)30172-5  PMID: 33521734 
  13. Jones TC, Mühlemann B, Veith T, et al. An analysis of SARS-CoV-2 viral load by patient age. https://zoonosen.charite.de/fileadmin/user_upload/microsites/m_cc05/virologie-ccm/dateien_upload/Weitere_Dateien/analysis-of-SARS-CoV-2-viral-load-by-patient-age.pdf
  14. L’Huillier AG, Torriani G, Pigny F, Kaiser L, Eckerle I. Culture-Competent SARS-CoV-2 in Nasopharynx of Symptomatic Neonates, Children, and Adolescents. Emerg Infect Dis. 2020;26(10):2494-7.  https://doi.org/10.3201/eid2610.202403  PMID: 32603290 
  15. Patel AB, Verma A. Nasal ACE2 Levels and COVID-19 in Children. JAMA. 2020;323(23):2386-7.  https://doi.org/10.1001/jama.2020.8946  PMID: 32432681 
  16. Huang YT, Tu YK, Lai PC. Estimation of the secondary attack rate of COVID-19 using proportional meta-analysis of nationwide contact tracing data in Taiwan. J Microbiol Immunol Infect. 2021;54(1):89-92.  https://doi.org/10.1016/j.jmii.2020.06.003  PMID: 32553448 
  17. Macartney K, Quinn HE, Pillsbury AJ, Koirala A, Deng L, Winkler N, et al. , NSW COVID-19 Schools Study Team. Transmission of SARS-CoV-2 in Australian educational settings: a prospective cohort study. Lancet Child Adolesc Health. 2020;4(11):807-16.  https://doi.org/10.1016/S2352-4642(20)30251-0  PMID: 32758454 
  18. Danis K, Epaulard O, Bénet T, Gaymard A, Campoy S, Botelho-Nevers E, et al. , Investigation Team. Cluster of coronavirus disease 2019 (COVID-19) in the French Alps, February 2020. Clin Infect Dis. 2020;71(15):825-32.  https://doi.org/10.1093/cid/ciaa424  PMID: 32277759 
  19. 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.  https://doi.org/10.2807/1560-7917.ES.2020.25.21.2000903  PMID: 32489179 
  20. Yung CF, Kam KQ, Nadua KD, Chong CY, Tan NWH, Li J, et al. Novel coronavirus 2019 transmission risk in educational settings. Clin Infect Dis. 2021;72(6):1055-8.  https://doi.org/10.1093/cid/ciaa794  PMID: 32584975 
  21. Ismail SA, Saliba V, Bernal JL, Ramsay ME, Ladhani SN. SARS-CoV-2 infection and transmission in educational settings: cross-sectional analysis of clusters and outbreaks in England. London: Public Health England. 2020. Available from: https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/911267/School_Outbreaks_Analysis.pdf
  22. Link-Gelles R, DellaGrotta AL, Molina C, Clyne A, Campagna K, Lanzieri TM, et al. Limited Secondary Transmission of SARS-CoV-2 in Child Care Programs - Rhode Island, June 1-July 31, 2020. MMWR Morb Mortal Wkly Rep. 2020;69(34):1170-2.  https://doi.org/10.15585/mmwr.mm6934e2  PMID: 32853185 
  23. Stein-Zamir C, Abramson N, Shoob H, Libal E, Bitan M, Cardash T, 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.  https://doi.org/10.2807/1560-7917.ES.2020.25.29.2001352  PMID: 32720636 
  24. Torres JP, Piñera C, De La Maza V, Lagomarcino AJ, Simian D, Torres B, et al. SARS-CoV-2 Antibody Prevalence in Blood in a Large School Community Subject to a COVID-19 Outbreak: A Cross-sectional Study. Clin Infect Dis. 2020;ciaa955.  https://doi.org/10.1093/cid/ciaa955  PMID: 32649743 
  25. Bernard Stoecklin S, Rolland P, Silue Y, Mailles A, Campese C, Simondon A, et al. , Investigation Team. First cases of coronavirus disease 2019 (COVID-19) in France: surveillance, investigations and control measures, January 2020. Euro Surveill. 2020;25(6):2000094.  https://doi.org/10.2807/1560-7917.ES.2020.25.6.2000094  PMID: 32070465 
  26. Fafi-Kremer S, Bruel T, Madec Y, Grant R, Tondeur L, Grzelak L, et al. Serologic responses to SARS-CoV-2 infection among hospital staff with mild disease in eastern France. EBioMedicine. 2020;59:102915.  https://doi.org/10.1016/j.ebiom.2020.102915  PMID: 32747185 
  27. Grzelak L, Temmam S, Planchais C, Demeret C, Tondeur L, Huon C, et al. A comparison of four serological assays for detecting anti-SARS-CoV-2 antibodies in human serum samples from different populations. Sci Transl Med. 2020;12(559):eabc3103.  https://doi.org/10.1126/scitranslmed.abc3103  PMID: 32817357 
  28. Sermet-Gaudelus I, Temmam S, Huon C, Behillil S, Gajdos V, Bigot T, et al. Prior infection by seasonal coronaviruses, as assessed by serology, does not prevent SARS-CoV-2 infection and disease in children, France, April to June 2020. Euro Surveill. 2021;26(13):2001782.  https://doi.org/10.2807/1560-7917.ES.2021.26.13.2001782  PMID: 33797390 
  29. Wölfel R, Corman VM, Guggemos W, Seilmaier M, Zange S, Müller MA, et al. Virological assessment of hospitalized patients with COVID-2019. Nature. 2020;581(7809):465-9.  https://doi.org/10.1038/s41586-020-2196-x  PMID: 32235945 
  30. Santé publique France (SPF). COVID-19. Point épidémiologique - Situation au 5 mars 2020 - 15h. [COVID-19. Epidemiological update - Situation on March 5, 2020 - 3 p.m.]. Saint-Maurice: SPF; 2020. French. Available from: https://www.santepubliquefrance.fr/content/download/235532/2526871
  31. Menni C, Valdes AM, Freidin MB, Sudre CH, Nguyen LH, Drew DA, et al. Real-time tracking of self-reported symptoms to predict potential COVID-19. Nat Med. 2020;26(7):1037-40.  https://doi.org/10.1038/s41591-020-0916-2  PMID: 32393804 
  32. Bénézit F, Le Turnier P, Declerck C, Paillé C, Revest M, Dubée V, et al. , RAN COVID Study Group. Utility of hyposmia and hypogeusia for the diagnosis of COVID-19. Lancet Infect Dis. 2020;20(9):1014-5.  https://doi.org/10.1016/S1473-3099(20)30297-8  PMID: 32304632 
  33. Buitrago-Garcia D, Egli-Gany D, Counotte MJ, Hossmann S, Imeri H, Ipekci AM, et al. Occurrence and transmission potential of asymptomatic and presymptomatic SARS-CoV-2 infections: A living systematic review and meta-analysis. PLoS Med. 2020;17(9):e1003346.  https://doi.org/10.1371/journal.pmed.1003346  PMID: 32960881 
  34. Long QX, Liu BZ, Deng HJ, Wu GC, Deng K, Chen YK, et al. Antibody responses to SARS-CoV-2 in patients with COVID-19. Nat Med. 2020;26(6):845-8.  https://doi.org/10.1038/s41591-020-0897-1  PMID: 32350462 
  35. Sette A, Crotty S. Pre-existing immunity to SARS-CoV-2: the knowns and unknowns. Nat Rev Immunol. 2020;20(8):457-8.  https://doi.org/10.1038/s41577-020-0389-z  PMID: 32636479 
  36. Anderson EM, Goodwin EC, Verma A, Arevalo CP, Bolton MJ, Weirick ME, et al. , UPenn COVID Processing Unit. Seasonal human coronavirus antibodies are boosted upon SARS-CoV-2 infection but not associated with protection. Cell. 2021;184(7):1858-1864.e10.  https://doi.org/10.1016/j.cell.2021.02.010  PMID: 33631096 
  37. Salje H, Tran Kiem C, Lefrancq N, Courtejoie N, Bosetti P, Paireau J, et al. Estimating the burden of SARS-CoV-2 in France. Science. 2020;369(6500):208-11.  https://doi.org/10.1126/science.abc3517  PMID: 32404476 
SARS-CoV-2 infection in schools in a northern French city: a retrospective serological cohort study in an area of high transmission, France, January to April 2020
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Arnaud+Fontanet&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Fontanet Arnaud</a>, <a href="/search?value1=Laura+Tondeur&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Tondeur Laura</a>, <a href="/search?value1=Rebecca+Grant&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Grant Rebecca</a>, <a href="/search?value1=Sarah+Temmam&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Temmam Sarah</a>, <a href="/search?value1=Yoann+Madec&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Madec Yoann</a>, <a href="/search?value1=Thomas+Bigot&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Bigot Thomas</a>, <a href="/search?value1=Ludivine+Grzelak&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Grzelak Ludivine</a>, <a href="/search?value1=Isabelle+Cailleau&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Cailleau Isabelle</a>, <a href="/search?value1=Camille+Besombes&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Besombes Camille</a>, <a href="/search?value1=Marie-No%C3%ABlle+Ungeheuer&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Ungeheuer Marie-Noëlle</a>, <a href="/search?value1=Charlotte+Renaudat&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Renaudat Charlotte</a>, <a href="/search?value1=Blanca+Liliana+Perlaza&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Perlaza Blanca Liliana</a>, <a href="/search?value1=Laurence+Arowas&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Arowas Laurence</a>, <a href="/search?value1=Nathalie+Jolly&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Jolly Nathalie</a>, <a href="/search?value1=Sandrine+Fernandes+Pellerin&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Pellerin Sandrine Fernandes</a>, <a href="/search?value1=Lucie+Kuhmel&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Kuhmel Lucie</a>, <a href="/search?value1=Isabelle+Staropoli&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Staropoli Isabelle</a>, <a href="/search?value1=Christ%C3%A8le+Huon&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Huon Christèle</a>, <a href="/search?value1=Kuang-Yu+Chen&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Chen Kuang-Yu</a>, <a href="/search?value1=Bernadette+Crescenzo-Chaigne&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Crescenzo-Chaigne Bernadette</a>, <a href="/search?value1=Sandie+Munier&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Munier Sandie</a>, <a href="/search?value1=Pierre+Charneau&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Charneau Pierre</a>, <a href="/search?value1=Caroline+Demeret&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Demeret Caroline</a>, <a href="/search?value1=Timoth%C3%A9e+Bruel&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Bruel Timothée</a>, <a href="/search?value1=Marc+Eloit&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Eloit Marc</a>, <a href="/search?value1=Olivier+Schwartz&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Schwartz Olivier</a>, <a href="/search?value1=Bruno+Hoen&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Hoen Bruno</a></span>. SARS-CoV-2 infection in schools in a northern French city: a retrospective serological cohort study in an area of high transmission, France, January to April 2020. <a href="/content/ecdc">Euro Surveill.</a> 2021;26(15):pii=2001695. <a href="https://doi.org/10.2807/1560-7917.ES.2021.26.15.2001695" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2021.26.15.2001695</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 17 Sept 2020;&nbsp;&nbsp; <span class="generated">Accepted</span>: 16 Feb 2021 </span> </p>
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