sKIDs surveillance

Public Health England (PHE) initiated SARS-CoV-2 surveillance in primary schools in May 2020 [11]. The sKIDs protocol is available online (https://www.gov.uk/guidance/covid-19-paediatric-surveillance). Primary schools across England were contacted to take part in the sKIDs surveillance. Pupils and staff members at participant schools were tested for SARS-CoV-2. The study comprised of two arms, with different sampling regimes;

• Weekly swabbing arm: nose swabs (weekly intervals from the 1^st June 2020 in schools with minimum 30 children and open for a minimum of 4 weeks) and one oral fluid sample at end of term.
• Blood sampling arm: blood samples, nose and throat swabs and oral fluid samples (OFS) (three study visits June, July and November 2020).

Staff and parent questionnaires

At the first sampling session in June 2020, after providing written informed consent, primary school staff completed a questionnaire at recruitment, which included optional questions about their acceptance, opinions, feasibility and frequency of testing for SARS-CoV-2 in school, with space for free text comments (S1 File). In primary schools involved with blood sampling, participating staff were also asked about their acceptability and frequency of blood tests to monitor SARS-CoV-2 antibodies (S1 File). Parents of primary school children also provide written informed consent and were asked the same questions for their child (S1 File). All parents, staff and children were invited to complete the questionnaire which was voluntary, however not all participants completed the questionnaire before and after their tests, and some only completed part of the questionnaire which was included in the analysis.

Student experiences

Participating primary school students were asked to complete an anonymised closed multi-choice paper questionnaire at one of the sKIDs sites (North London), which included six primary schools (S2 File) before and after their tests at the first visit. Both sKIDs investigators and teachers helped each student complete the questionnaire. The first part of the questionnaire was completed prior to any tests being done. Questions included a simple written and pictorial explanation of each type of sample (nose swab, throat swab, blood sample and oral fluid sample) and asked children to rate on a scale how they were feeling about the sample (e.g. “very nervous” to “looking forward to it”). The Wong-Baker pain emoji faces were used to rate any discomfort associated with each sampling method [12]. All children were invited to complete the questionnaire which was voluntary, however not all children completed the questionnaire before and after their tests, and some only completed part of the questionnaire which was included in the analysis. 135 children out of a of 244 from the six schools fully or partially completed the questionnaire. The questionnaire was anonymous and optional for children to complete.

Swabbing participation

We assessed rates of participation in the swabbing arm of the study by calculating the return percentages of participants from their first week of sampling. Because not all schools joined the study in the same week, the number of available sampling weeks (eligibility) differed between participants, with schools open for between two and six weeks of sampling. Moreover, because participants sometimes joined after the first sampling week at their school, we calculated eligible weeks at the level of the participant. For example, if a participant joined in the second week of sampling at a school that was open for the full six weeks of the study, the participant would have five eligible weeks of participation.

Data analysis

Data were entered into Microsoft Access and analysed using Stata v.15.0 (Statacorp, Tx). Data are mainly descriptive. Categorical variables are presented as proportions and compared using the chi-squared or Fisher’s Exact test as appropriate. MAXQDA Analytics Pro 2020 (Release 20.2.2) was used for coding of free texts. Only legible comments that were relevant to the question “what is the feasibility and acceptability of COVID-19 testing in schools?” were coded. Data were analysed using an iterative thematic framework approach. Drawing on current knowledge about parental attitudes regarding paediatric phlebotomy, and the research question, initial codes were considered prior to analysis (Parent/guardian comments, staff comments which were then sub-coded as appropriate to nose, throat, oral fluid, blood, or other), with scope to develop further codes as appropriate. The frequency of codes was counted in relation to feasibility and acceptability, as a measure of importance, with new codes added as appropriate.

Ethics approval

The sKIDs study was approved by the Public Health England Research Ethics Governance Group (R&D REGG Ref: NR0209, 16 May 2020).

Children’s questionnaire on acceptability of testing

Children’s experiences were assessed in six London schools participating in the blood sampling arm of sKIDs. A total of 134 children aged 4–7 years (n = 40) or 8–11 years (n = 95) completed partially or fully completed the questionnaire about their experience with nasal swabs, throat swabs, oral fluid and blood tests before and after sampling.

Before testing.

Prior to the tests, oral fluid sampling (107/132, 81%) was reported by the children to be the most acceptable test, compared to the throat swabs (80/134, 59%), nose swabs (77/132, 58%), and blood tests (48/130, 37%) (Table 1). The students were most concerned about the blood test, with nearly two-thirds reporting feeling “very nervous” (41/130, 32%) or “a little nervous” (41/130, 32%). Prior to testing, students aged 4–7 years were more likely to feel nervous about the nose swab (26/39 [67%] vs. 29/93 [31%]; P = 0.020) compared to 8–11 year-olds. Both age groups were similarly nervous about blood tests (24/38 [63%] vs. 58/92 [63%]; P = 0.995) (Table 1).

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Table 1. Children’s reported expectations before the test, and experiences after the test.

https://doi.org/10.1371/journal.pone.0255517.t001

Older children (8–11 yrs) were generally more relaxed about the tests compared to younger children (4–7 yrs) with the majority reporting they were “not worried” or “looking forward to” the nose swab (64/93 [69%] vs. 13/39 [33%]; P = 0.041) and throat swab (60/95 [63%] vs. 20/39 [51%]; P = 0.516). However, 8–11 year olds did report that they were nervous about the blood test, similar to 4–7 year olds (58/92 [63%] vs. 24/38 [63%]; P = 0.995).

Pre-testing apprehension (“very nervous”) was similar between both age categories for three of the four tests (nose: 7/39 [18%] vs. 10/93 [11%]; P = 0.329, blood: 15/38 [39%] vs. 26/92 [28%]; P = 0.375, oral fluid samples: 4/37 [11%] vs. 6/95 [6%]; P = 0.421), while younger children reported significantly greater apprehension about throat swabs than older children (throat (9/39 [23%) vs. 8/95 [8%]; P = 0.047) (Table 1).

After testing.

After completing their tests, a higher proportion of 4–7 year-olds reported the tests to have been “better than expected” compared to 8–11 year olds, including nose swabs (20/32 [62%] vs. 41/82 [50%]; P = 0.52), throat swabs (15/31 [48%] vs. 35/83 [42%]; P = 0.71), oral fluid sampling (20/31 [64%] vs. 35/88 [40%]: P = 0.17) and blood tests (17/26 [65%] vs. 43/85 [51%]; P = 0.48), although these differences were not statistically significant (Table 1).

Most children reported that all tests were “better” or “as expected” (86–95%), with a minority reporting that it was “worse” (5–14%). Even those who said they were “very nervous” about the tests reported that it was “better” than they expected. For the blood test, 5/9 (56%) of 4–7 year olds and 15/23 (65%) of 8–11 year olds who were “very nervous” beforehand, reported it was “better” than they had expected (P = 0.25). In older children aged 8–11 years, those who reported they were “not worried” about the tests, were more likely to indicate that the tests were “as they expected”, compared to 4–7 year olds who were more likely to say the test was “better” than they expected (Table 1). Children aged 8–11 years were more likely to report the tests to be “as expected” than 4–7 year olds. Only 2/26 (8%) of 4–7 year-olds reported the blood test to be as expected compared to 35/85 (41%) of 8–11 year olds (P = 0.015) (Table 1). When asked if they would have the tests again after their investigations, the students were more likely to agree to additional testing for nose swabs (61/113 [54%]) or to oral fluid (60/114 [53%]) [p = 0.838], followed by throat swabs (57/113 [50%]) and blood tests (40/108 [37%]) [p = 0.045] (Table 2). Younger children were significantly more likely to decline a repeat throat swab, blood test and oral fluid compared to older children (Table 2).

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Table 2. Children’s responses when asked if they would have each individual test again.

https://doi.org/10.1371/journal.pone.0255517.t002

Frequency of testing in

Swabbing schools.

In primary schools participating in weekly nasal swabbing, most parents and staff selected a preference for weekly nose swabbing (2445/3868 [63%], & 1209/2251 [54%]), throat swabbing (1374/3754 [37%] and 948/2186 [43%]) and oral fluid sample (1734/3779 [46%] and 1003/2188 [46%]) (Table 3). With respect to blood testing, 31% (673/2164) of staff and 11% (395/3676) of parents indicated they would tolerate blood tests once a week, while 10% (222/473) of staff refused to have a blood test and 43% (1584/3676) of parents refused blood tests for their child.

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Table 3. Responses of Staff and Parents of children in primary schools in relation to frequency of testing for each investigation in schools participating in (A) weekly swabbing and (B) blood sampling.

https://doi.org/10.1371/journal.pone.0255517.t003

Swabbing participation

Overall mean (±SD) return rates per week were 87.8% (8.98%), varying between 72.19% and 95.79% (recorded in the third and fourth sampling weeks for those eligible for six tests). These return rates were similar between students (86.6% ± 8.1%) and staff (89.0% ± 9.9%) and remained broadly consistent irrespective of eligible weeks (Fig 1 and S1 Table).

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Fig 1. Participant return rates of students and staff per eligible sampling week.

https://doi.org/10.1371/journal.pone.0255517.g001

Comparisons to published literature

Parental attitudes and factors relating to paediatric venepuncture has previously been explored, but predominantly in hospital/clinical settings. Parental presence, support of healthcare staff and quality information prior to procedure have been associated with reduced stress and pain for the child, in addition to improving participation and collaboration between parents and healthcare staff [16, 17]. Similar themes were also identified in the qualitative analysis of parent comments in our analysis.

In England, schools are accustomed to public health interventions, such as the National Child Measurement Programme where children have their height and weight measured anuually [18], and receive some of their vaccines (e.g. HPV, MenACWY, nasal influenza) vaccinations [19]. Vaccination though, unlike venepuncture, has a clear personal benefit, which may account for the high uptake in England [19]. The sKIDs surveillance, however, was potentially more intrusive because it involved multiple investigations, including blood sampling which, although performed by experienced staff, was mainly performed in the absence of parents, even though they were aware of the investigations and had provided written consent. Furthermore, it relied on the good will of participants to improve our knowledge of SARS-CoV-2, with little or no personal benefit. Indeed, participation had a risk of testing positive for SARS-CoV-2, which would result in the child/bubble being sent home for isolation, thus further disrupting access to education and creating childcare issues for working parents.

Overall, however, the large numbers of participants is a testimony to their willingness to support research on SARS-CoV-2 infection so that schools could remain open safely during the pandemic. We observed a higher return rates for weekly nasal swabbing (88%) compared to blood sampling (62–65%) [11], which is not surprising, but this was important because serum SARS-CoV-2 antibodies provide more robust evidence of prior exposure to the virus, including transient and asymptomatic infections [20]. Contemporaneous collection of oral fluid samples also allowed the development and validation of a non-invasive antibody test, which is now being used in a larger School Infection Survey (SIS) aiming to recruit up to 50,000 staff and students in 150 schools across England [21]. The willingness of the children to take part in this important investigation and the high retention rate for subsequent visits despite their nervousness about all the tests is commendable.

In the published literature, there are limited studies on the feasibility and acceptability of mass testing in schools. A study from 1994 in England investigated the feasibility and acceptability of venepuncture in schools, measuring haemoglobin, ferritin and cholesterol in school children [22]. They found no significant difference in refusal rates between families of children who received an explanation about the test before entering the testing room and those who received an explanation at the time of testing. The study also found lower response rates from parents in low- compared to high-socioeconomic groups [22]. Interestingly, the authors reported that some parents asked to be present during the procedure, but this often exacerbated the stress and anxiety of the child, which is similar to our experience. Indeed, allowing children to participate in the surveillance without their parents could potentially be beneficial through promotion of self-confidence and independence.

Limitations

The questionnaires were completed by staff and parents who had already agreed to take part in the sKIDs surveillance. This group may, therefore, not be representative of all staff and parents of children in primary schools. Similarly, the children completing the questionnaires had already agreed to take part and, since only six London schools were involved, may not be representative of all primary school children. We observed for example, that parental and staff preference for testing was influenced by the sKIDs investigations in those schools such that parents/staff in the blood sampling arm were more accepting of blood testing and frequent blood testing compared to those in the weekly swabbing schools. This is most likely explained by the fact that the parents in the blood sampling arm had already agreed for their children to have the blood test.

Implications and conclusions

The sKIDs surveillance has contributed significantly to our understanding of SARS-CoV-2 infection and transmission in educational settings and helped support the decision to reopen all school years in September 2020. The scale of the sKIDS surveillance was unprecedented, given that these were undertaken in the middle of a pandemic and involved multiple investigations including blood sampling in young children. We found that high-level surveillance is both positively received by this demographic and that there is a clear willingness to participate. Involving the children in the surveillance also provided an opportunity to help improve health literacy, particularly in relation to the pandemic, and provided the children with a greater understanding of public health surveillance, thus facilitating interest and discussion in science.