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Severe Acute Respiratory Syndrome Coronavirus 2 Infections in Primary School Age Children After Partial Reopening of Schools in England

Powell, Annabel A. Bsc*; Amin-Chowdhury, Zahin BSc*; Mensah, Anna MSc*; Ramsay, Mary E. FFPH*,†; Saliba, Vanessa MD*; Ladhani, Shamez N. MRCPCH*,‡

Author Information
The Pediatric Infectious Disease Journal: June 2021 - Volume 40 - Issue 6 - p e243-e245
doi: 10.1097/INF.0000000000003120
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Abstract

Children account for only 1–3% of coronavirus disease 2019 (COVID-19) cases, but their role in infection and transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) remains under considerable debate. Early in the pandemic, most countries closed their schools as part of national lockdown to control the spread of the virus.1 In England, COVID-19 emerged in late January 2020 and, as cases started increasing rapidly from early March 2020, all educational settings were closed from 20 March, followed by national lockdown 23 March.2 Cases plateaued in mid-April and declined gradually during May 2020.2 From June 1, 2020, some primary school years returned to school but with strict infection control practices and social distancing measures, including smaller class sizes organized into distinct bubbles of ≤ 15 children to limit the risk of transmission within educational settings.3 Children of key workers were allowed to attend school throughout the pandemic. We recently reported on cases and outbreaks during the summer half-term in England (June 1, to July 18, 2020).3 Here, we describe the national epidemiology, risk factors including school attendance, clinical features and outcomes of SARS-CoV-2 infection in primary school-aged children after the partial reopening of schools in England.

METHODS

Public Health England (PHE) conducts SARS-CoV-2 surveillance in England. Nationally, SARS-CoV-2 tests are performed through different routes called “Pillars”.2 Pillar 1 swabs are taken in National Health Service (NHS) hospitals for those with a clinical need and for health and care workers and their household members. Pillar 2 testing is for the wider community, for example, tests carried out at mobile testing sites or regional test centers. PHE receives daily reports of national tests which are reported weekly online.2 For this analysis, confirmed cases in primary school-age children in pillar 1 and 2 during June 2020 were linked to the personal demographic service (PDS), an online national database which holds demographic data and death status for all NHS registered patients (https://digital.nhs.uk/services/demographics), to obtain contact information. Those with registered phone numbers were interviewed by telephone and a standard questionnaire completed on information on symptoms, reason for testing for SARS-CoV-2, illness in family members including index cases, school attendance, potential source of infection and outcomes of infection. Indices of multiple deprivation data were estimated from patient postcode using the English indices of deprivation (2019), which is based on income, employment, education, health and other measures (https://www.gov.uk/government/statistics/english-indices-of-deprivation-2019).

RESULTS

The number of open primary school settings in England rose from 6900 on June 01, to 18,100 on June 30, and the number of children attending these setting increased from 475,000 to 1,646,000. The weekly number of cases in academic years that returned to school (Reception, Year 1 and Year 6) did not differ from academic years that did not return to school (Years 2–5) (Fig. 1). During June 2020, 25,432 SARS-CoV-2 infections were confirmed in England. There were 446 primary school-age children with a recorded NHS number, including 54 tested through pillar 1 and 392 through pillar 2 (Table 1). Of these, 24% (63/259) were attending school, and 12% (32/259) had a sibling who was attending school. Overall, 41% (182/446) were in the lowest quintile (most deprived) for multiple deprivation compared with 11% (49/446) in the highest quintile (least deprived). Parents considered themselves to be the source of infection in 43% (112/259) of cases, while 3% (9/259) of all parents or 14% (9/63) of parents of children attending school considered the school to be the source of their child’s infection.

TABLE 1. - Characteristics and Outcome of Observed Cases
All Cases Pillar 1 Pillar 2 P*
Characteristics of all cases
 Total cases, n 446 54 392
 Male, n/N (%) 224/446 (50.22) 32/54 (59.26) 192/392 (48.98) 0.16
 Median age, yr (IQR) 8 (6–10) 7.5 (5–10) 8 (6–10) 0.86
 IMD quintile 1, n/N (%) 182/446(40.81) 15/54(27.78) 167/392(42.60) 0.15
 IMD quintile 2, n/N (%) 103/446(23.09) 14/54(25.93) 89/392(22.70)
 IMD quintile 3, n/N (%) 58/446(13.00) 12/54(22.22) 46/392(11.73)
 IMD quintile 4, n/N (%) 54/446(12.11) 7/54(12.96) 47/392(11.99)
 IMD quintile 5, n/N (%) 49/446(10.99) 6/54(11.11) 43/392(10.97)
 Contactable by telephone, n 411 54 357 0.02
 Agreed to be interviewed, n (%) 259 (58.07) 41 (75.9) 218 (55.6) 0.005
Characteristics and outcomes of interviewed
 Male, n/N (%) 137/259 (52.90) 26/41 (63.41) 111/218 (50.92) 0.14
 Median age, yr (IQR) 7 (5–10) 7 (5–10) 7 (5–10) 0.9
 Symptomatic children, n/N (%) 131/259 (50.58) 14/41 (34.15) 117/218 (53.67) 0.022
 Hospitalized, n/N (%) 22/259 (8.49) 22/41 (53.66)* 0/218 (0) < 0.001
 Child was the only positive case, n/N (%) 58/259(22.39) 30/41(73.17) 28/218 (12.84) < 0.001
 Infection source (not known), n/N (%) 97/259 (37.45) 26/41 (63.41) 71/218 (32.57) < 0.001
 Infection source (community), n/N (%) 41/259 (15.83) 1/41 (2.44) 40/218 (18.35)
 Infection source (parents work), n/N (%) 112/259 (43.24) 11/41 (26.83) 101/218 (46.33)*
 Infection source (school), n/N (%) 9/259 (3.47) 3/41 (7.32) 6/218 (2.75)
 Attended school in June 2020, n/N (%) 63/259 (24.32) 10/41 (24.39) 53/218 (24.31) 0.99
 Sibling attending school, n/N (%) 32/259 (12.36) 4/41 (9.76) 28/218 (12.84) 0.58
 Still unwell after > 1 mo. n/N (%) 7/259 (2.70) 4/41 (9.76) 3/218 (1.38) 0.002
IMD indicates index of multiple deprivation; IQR, interquartile range.
*Proportions were compared using the using the χ2 or Fisher exact test as appropriate, while medians with IQRs were compared using the Mann-Whitney U test.

FIGURE 1.
FIGURE 1.:
Number of cases in children according to their social academic year group from commencing May 4 to week commencing July 27, 2020. Note that only reception, year 1 and year 6 (circled) returned to school from June 1, 2020. The red bars indicate the group children with confirmed SARS-CoV-2 infection during June 2020 who were followed up as part of the enhanced national surveillance. *Reception = included children under 5 years were not routinely tested in the community until June 1, 2020.

Of the 41 children tested through pillar 1, 14 (34%) SARS-CoV-2–positive children attended the emergency department with suspected COVID-19, including 9 of 14 (64%) with typical COVID-19 symptoms (fever, new continuous cough or anosmia), and 3/14 (21%) were hospitalized. The other 27 children were routinely tested for SARS-CoV-2 infection when they attended the emergency department with a non–COVID-19 illness (n = 16), because they were a household contact of a confirmed case (n = 7) or other (n = 4). At follow-up, 7/259 children (2.7%) reported excessive fatigue (n = 4), dyspnea (n = 1), body aches (n = 1) or brain fog (n = 1) more than a month later.

Compared with pillar 1 testing, children tested through pillar 2 were more likely to be symptomatic (117/218; 54%), with 95 of 117 (81%) fulfilling the COVID-19 case definition, and none were hospitalized. Most children tested through pillar 2 (190/218; 87%) had another SARS-CoV-2 positive household contact.

Discussion

The partial reopening of some school years in England was not associated with any increase in confirmed SARS-CoV-2 infections among primary school-age children, despite more than a million children returning to school in June 2020. This is consistent with the experience of countries such as Iceland and Norway that kept their preschools and primary schools open during their lockdown and those that reopened their schools after easing of their lockdown such as Germany.1 Most SARS-CoV-2–positive children in England were tested in the community (pillar 2) because their parent developed COVID-19 or, less frequently, because the child developed COVID-19 symptoms.

In contrast, most children testing positive through pillar 1 had been screened for SARS-CoV-2 because they attended the emergency department with a non–COVID-19 illness or their parent, a healthcare worker, developed COVID-19, which explains the high proportion of asymptomatic infections. Reassuringly, hospitalizations for COVID-19 were rare, consistent with the reported literature.4 Seven children had persistent symptoms (> 1 month), raising an important question about the risk of long COVID in children, as has been reported in adults.5

Although a quarter of the children with SARS-CoV-2 were attending school during June 2020, only 3% of parents considered their child to have been infected in school. At that time, community infection rates across England were at their lowest because of the preceding national lockdown and stringent infection control practices had been implemented in schools, especially the restriction of staff with small numbers of students into discrete bubbles.3 Since September 2020, however, when community SARS-CoV-2 infection rates were higher than in June, children across all primary and secondary years returned to school, raising significant challenges for maintaining physical distancing and infection control measures. In England, childhood cases in every academic year group started increasing since mid-August 2020, before schools reopening, and have increased week-on-week until the midterm holidays in mid-October, although the relative contributions of SARS-CoV-2 infection and transmission within and outside educational settings remains unclear. Cases by academic school year are reported weekly in England (https://www.gov.uk/government/statistics/national-flu-and-covid-19-surveillance-reports).

Our analysis had some limitations. This was not a community survey; the cases comprise of children who presented to a healthcare or community testing center because they were unwell or because they were contacts of a confirmed case. Additionally, families taking part in the telephone interview may be different to families that could not be contacted or declined the interview. The data were collected through telephone interviews, too, and may be prone to subjective and recall biases.

In conclusion, our findings indicate that, during periods of low community SARS-CoV-2 incidence, primary school-age children may safely attend school if appropriate social distancing and infection control measures, including restriction of class sizes, can be implemented. Primary school-age children typically had mild infection, and hospitalizations were rare. Ongoing surveillance will provide important information on SARS-CoV-2 infection and transmission across all educational settings.

ACKNOWLEDGMENTS

The authors would like to thank all the parents of children with SARS-CoV-2 infection who agreed to take part in the interview. The authors are also grateful to Mr. Paul Charter and Ms. Michele Olphonce for all their help with contacting the families.

REFERENCES

1. Levinson M, Cevik M, Lipsitch M. Reopening primary schools during the pandemic. N Engl J Med. 2020;383:981–985.
2. Public Health England (PHE). Weekly Coronavirus Disease 2019 (COVID-19) Surveillance Report: Summary of COVID-19 Surveillance Systems. Available at: https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/880925/COVID19_Epidemiological_Summary_w17.pdf. Accessed November 15, 2020.
3. Ismail S, Saliba V, Lopez-Bernal J, et al. SARS-CoV-2 infection and transmission in educational settings: cross-sectional analysis of clusters and outbreaks in England [published online ahead of print December 8, 2020]. Lancet Infect Dis 2020:S1473-3099(20)30882-3. doi: 10.1016/S1473-3099(20)30882-3.
4. Ludvigsson JF. Systematic review of COVID-19 in children shows milder cases and a better prognosis than adults. Acta Paediatr. 2020;109:1088–1095.
5. Sudre C, Murray B, Varsavsky T, et al. Attributes and predictors of Long-COVID: analysis of COVID cases and their symptoms collected by the Covid Symptoms Study App. MedRxiv. October 21, 2020. doi: https://doi.org/10.1101/2020.10.19.20214494.
Keywords:

coronavirus disease 2019; epidemiology; pediatrics

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