Screening of healthcare workers for SARS-CoV-2 highlights the role of asymptomatic carriage in COVID-19 transmission.

Decision letter: Screening of healthcare workers for SARS-CoV-2 highlights the role of asymptomatic carriage in COVID-19 transmission

Significant differences exist in the availability of healthcare worker (HCW) SARS-CoV-2 testing between countries, and existing programmes focus on screening symptomatic rather than asymptomatic staff. Over a 3 week period (April 2020), 1032 asymptomatic HCWs were screened for SARS-CoV-2 in a large UK teaching hospital. Symptomatic staff and symptomatic household contacts were additionally tested. Real-time RT-PCR was used to detect viral RNA from a throat+nose self-swab. 3% of HCWs in the asymptomatic screening group tested positive for SARS-CoV-2. 17/30 (57%) were truly asymptomatic/pauci-symptomatic. 12/30 (40%) had experienced symptoms compatible with coronavirus disease 2019 (COVID-19)>7 days prior to testing, most self-isolating, returning well. Clusters of HCW infection were discovered on two independent wards. Viral genome sequencing showed that the majority of HCWs had the dominant lineage B∙1. Our data demonstrates the utility of comprehensive screening of HCWs with minimal or no symptoms. This approach will be critical for protecting patients and hospital staff.

Diminished incidence of COVID-19 amongst healthcare workers in a comprehensive screening programme demonstrates how effective infection control measures and staff testing can prevent hospitals becoming independent 'hubs' of SARS-CoV-2 transmission.

Article Figures and data Abstract Introduction Results Discussion Materials and methods Data availability References Decision letter Author response Article and author information Metrics Abstract We conducted voluntary Covid-19 testing programmes for symptomatic and asymptomatic staff at a UK teaching hospital using naso-/oro-pharyngeal PCR testing and immunoassays for IgG antibodies. 1128/10,034 (11.2%) staff had evidence of Covid-19 at some time. Using questionnaire data provided on potential risk-factors, staff with a confirmed household contact were at greatest risk (adjusted odds ratio [aOR] 4.82 [95%CI 3.45–6.72]). Higher rates of Covid-19 were seen in staff working in Covid-19-facing areas (22.6% vs. 8.6% elsewhere) (aOR 2.47 [1.99–3.08]). Controlling for Covid-19-facing status, risks were heterogenous across the hospital, with higher rates in acute medicine (1.52 [1.07–2.16]) and sporadic outbreaks in areas with few or no Covid-19 patients. Covid-19 intensive care unit staff were relatively protected (0.44 [0.28–0.69]), likely by a bundle of PPE-related measures. Positive results were more likely in Black (1.66 [1.25–2.21]) and Asian (1.51 [1.28–1.77]) staff, independent of role or working location, and in porters and cleaners (2.06 [1.34–3.15]). Introduction On 23rd March 2020 the UK followed other European countries in locking down its population to mitigate the impact of the rapidly evolving Covid-19 pandemic. By 5th May the UK had recorded Europe's highest attributed death toll (Johns Hopkins Coronavirus Resource Centre, 2020). Lock-down isolated many UK households but staff maintaining healthcare services continued to be exposed to patients and to other healthcare workers (HCW). National Health Service (NHS) hospitals endeavoured to provide personal protective equipment (PPE) in line with Public Health England (PHE) guidelines in clinical areas and encouraged social distancing elsewhere. Despite these measures the incidence of Covid-19 among HCWs is higher than in the general population (Nguyen et al., 2020; Disparities in the risk and outcomes from COVID-19, 2020). Multiple studies have investigated Covid-19 in HCWs (Nguyen et al., 2020; Rivett et al., 2020; Shields et al., 2020; Houlihan et al., 2020). However, crucial to designing a safe working environment and maintaining effective healthcare services is an understanding of the risks associated with specific roles and to individuals, and whether risk is associated with social-mixing, direct exposure to Covid-19 patients or PPE type. Some studies have suggested exposure to Covid-19 patients poses increased risk (Nguyen et al., 2020; Ran et al., 2020; Lombardi et al., 2020), whilst others have not (Hunter et al., 2020; Galan et al., 2020; Folgueira et al., 2020). However, none have addressed these questions by comprehensively investigating all staff groups across an institution, simultaneously assessing symptomatic and asymptomatic incidence. Alongside routine SARS-CoV-2 PCR testing of symptomatic staff, Oxford University Hospitals NHS Foundation Trust (OUH) has offered SARS-CoV-2 PCR and antibody testing to all asymptomatic staff to improve infection prevention and control for staff and patients. We present the results of this large, high-uptake programme. Results Oxford University Hospitals Covid-19 context From mid-March 2020 OUH saw daily admissions of patients with Covid-19. By 8th June, 636 patients had been admitted within a week of a confirmed Covid-19 diagnosis. Weekly incidence of new Covid-19 diagnoses in these patients peaked during the week beginning 30th March (n = 136/week, Figure 1A). Routine SARS-CoV-2 PCR testing of symptomatic staff (with fever or new persistent cough) began on 27th March; weekly incidence of new staff diagnoses peaked the week beginning 6th April (n = 98/week, Figure 1B). Up to and including the 8th June, 348/1498 (23%) symptomatic staff tested were PCR-positive (2.5% of all 13,800 staff employed at OUH). Ten staff were admitted to hospital with Covid-19 (0.07%); four died (0.03%). Figure 1 Download asset Open asset Epidemiological curve for hospital inpatients (panel A) and staff (panel B) diagnosed with Covid-19, by week and timing of asymptomatic staff testing (panel C). Each patient admitted to hospital with a diagnosis of Covid-19 within ±7 days of any day during their admission is plotted based on the date of their positive PCR test. Testing for symptomatic staff was made available from 27th March 2020; staff were asked to attend on days 2–4 of symptoms and are plotted in the week of their positive test. Of 1128 staff positive by PCR or serology at the asymptomatic staff clinic, 192 had been previously diagnosed at the symptomatic staff clinic. Of the remaining 936 positive staff, 449 (48%) reported a date when they believed a Covid-19 illness had begun, these are plotted in yellow above, many with symptoms before the availability of staff testing. As 487 (52%) of staff did not provide a date of symptom onset the true values for the yellow bars on the y-axis are likely to be around two times higher. Panel C shows the week asymptomatic staff were tested, those testing SARS-CoV-2 PCR-positive and/or IgG-positive are shown in black and those with negative tests in grey. The overall percentage of staff tested each week with positive PCR and/or antibody results is shown above each bar. The bar for 01 June also includes 31 staff tested on 08 June. Asymptomatic staff testing A voluntary asymptomatic screening programme offering SARS-CoV-2 PCR and antibody testing to all staff working anywhere on site commenced on 23rd April 2020. Between 23rd April and 8th June, 10,610 of the 13,800 (77%) staff employed by OUH registered for asymptomatic testing and 10,034 (73%) were tested at least once, 9926 by PCR and 9958 by serology. The majority of testing was undertaken in the first three weeks of May 2020 (Figure 1C). 288/9926 (2.9%) staff were PCR-positive on their first asymptomatic screen; 145 were permitted to remain at work: 61 (21%) had tested PCR-positive >7 days previously while symptomatic and had since recovered and 84 (29%) had a history suggestive of previous Covid-19 (in most, prior to the availability of symptomatic staff testing). The remainder, 130/288 (45%), were assessed to have a new infection and self-isolated. Documentation was incomplete for six staff and seven could not be contacted. Duration of PCR positivity Having observed asymptomatic staff who were PCR-positive following symptomatic recovery, we investigated the duration of PCR positivity using data from staff and patients with consecutive tests. Repeat testing of patients was guided by individual clinician request, in conjunction with the infection consult service. Repeat testing of staff was available in those attending asymptomatic screening who had previously been tested by the symptomatic testing service and was also undertaken up to weekly in the cohort of staff who attended the asymptomatic testing service during the first week of testing. Fewer staff than patients were persistently positive at 7–13 days (exact p=0.003), but results were similar by 14–20 days, 68/159 (43% [95% CI 35–51%]) overall. 34/141 (24% [17–32%]) samples taken after ≥42 days were positive (Figure 2). Figure 2 Download asset Open asset Proportion of staff and patients remaining PCR-positive on repeat nasopharyngeal swabs. Panel A shows pooled data and Panel B data separately for staff and patients. The number of individuals with a repeat test in each time interval is shown below each bar and 95% exact binomial confidence intervals are plotted. All tests following a first positive sample are included up until the first negative sample per patient. The number of tests positive after a repeat swab on the same day is indicative of the sensitivity of a single swab, 15/16 of these swabs were obtained from patients on wards by any available staff member, whereas staff sampling was undertaken by specially trained teams. Combined serology and PCR results in asymptomatic staff Considering the first asymptomatic clinic PCR and serology samples from each staff member, 1128/10,034 (11.2%) staff attending for asymptomatic screening were positive by PCR or serology, indicating a composite primary outcome of 'Covid-19 at some time', including 192 previously diagnosed via symptomatic staff testing. 1069/9958 (10.7%) staff with an immunoassay result were IgG-positive (see Supplementary file 1A for a comparison of results by the two assays). In staff providing questionnaire data prior to asymptomatic testing, 552/1126 (49.0%) staff subsequently testing positive thought they had already had Covid-19, compared to 1106/8906 (12.4%) testing negative. Symptoms predictive of Covid-19 We asked all staff attending asymptomatic screening about possible Covid-19-related symptoms since 1st February 2020 (Table 1). In a multivariable model containing all symptoms, anosmia or loss of taste was most strongly predictive of Covid-19 (aOR 17.7 [95%CI 14.1–22.2], p<0.001). Other independent predictors included myalgia, fever and cough. Adjusting for other symptoms, sore throat was a negative predictor for Covid-19. Table 1 Association of self-reported symptoms and Covid-19 in hospital staff. SymptomSymptom reportedSymptom not reportedUnivariableMultivariable nCovid-19 positiveCovid-19 negative% positiveNCovid-19 positiveCovid-19 negative% positiveOr (95% CI)P valueOr (95% CI)P valueAnosmia or loss of taste85848936957.0917463785376.917.7 (15.1–20.8)<0.00117.7 (14.1–22.2)<0.001Myalgia1796501129527.9823662576117.64.7 (4.1–5.4)<0.0012.1 (1.7–2.6)<0.001Fever1465406105927.7856772078478.44.2 (3.6–4.8)<0.0011.5 (1.2–1.8)<0.001Nausea or vomiting41713028731.29615996861910.43.9 (3.1–4.9)<0.0011.2 (0.9–1.6)0.18Fatigue2718591212721.7731453567797.33.5 (3.1–4)<0.0011.0 (0.8–1.2)0.81Cough1813403141022.2821972374968.83 (2.6–3.4)<0.0011.2 (1.0–1.5)0.04Shortness of breath102224577724.0901088181299.82.9 (2.5–3.4)<0.0011.2 (0.9–1.5)0.30Diarrhoea60714746024.29425979844610.42.8 (2.2–3.4)<0.0011.1 (0.9–1.5)0.30Hoarseness64513650921.19387990839710.52.3 (1.8–2.8)<0.0011.2 (0.9–1.7)0.23Nasal congestion1871355151619.0816177173909.42.2 (2–2.6)<0.0011.0 (0.8–1.2)0.63Sore throat2248356189215.8778477070149.91.7 (1.5–2)<0.0010.6 (0.5–0.8)<0.001*Hoarseness + Anosmia or loss of taste0.5 (0.3–0.8)0.002*Shortness of breath + Anosmia or loss of taste0.5 (0.3–0.7)<0.001 *All interactions with an interaction Wald p values < 0.01 are shown. Risk factors for Covid-19 in healthcare workers We used pre-test questionnaire data provided by 10,032 asymptomatic staff to estimate risk factors for Covid-19 (two staff tested did not provide questionnaire data). Staff diagnosed via the symptomatic testing clinic alone were not included as no detailed questionnaire data were collected from these staff. However, the 192/348 (55%) staff diagnosed by the symptomatic testing service who subsequently attended the asymptomatic clinic were included. 67/174 (38.5%) staff reporting household contact with a PCR-confirmed case tested positive, compared to 1059/9858 (10.7%) without (p<0.001). SARS-CoV-2 infected staff were also more likely to report suspected, but unconfirmed contacts, and non-household contacts (Figure 3, Supplementary file 1B). 368/2165 (17.0%) staff reporting workplace contact without PPE with a known or suspected Covid-19 patient tested positive, compared with 758/7867 (9.6%) not reporting similar exposure (p<0.001). To mitigate recall bias, we repeated this analysis restricted to staff who did not think they had had Covid-19: 167/1653 (10.1%) reporting an exposure were positive compared to 407/6721 (6.1%) who did not (p<0.001). Figure 3 Download asset Open asset Univariable (panel A) and multivariable (panel B) relationships between risk factors and staff infection with SARS-CoV-2 in 10,032 healthcare workers. See Supplementary file 1B for count data, univariable and multivariable odds ratios. Pairwise interactions were sought between all variables the multivariable model, a single interaction exceeded the p<0.01 screening threshold, representing decreased risk of Covid-19 in emergency department staff reporting exposure to a Covid-19 without PPE (p=0.002). However, given the large number of interactions sought and biological implausibility, the interaction is omitted from the model presented. For the purpose of plotting p values <0.001 were rounded up to 0.001. Risk factor data were not available for two staff members. In panel A, the category for 01 June also includes 31 staff tested on 08 June. We further investigated risk of workplace Covid-19 acquisition. 358/1586 (22.6%) staff on wards caring for patients with Covid-19 were infected, compared to 631/7369 (8.6%) on non-Covid-19 facing wards/other areas, and 139/1079 (12.9%) staff working across multiple areas (p<0.001). Covid-19 facing areas included the emergency department, acute medical and surgical wards, the respiratory high dependency unit (HDU) and three intensive care units (ICUs). However, the proportion of staff with a positive test working in acute medicine (222/793, 28.0%) was greater than in the emergency department (41/344, 11.9%) and in the ICUs (44/448, 9.8%) (Figure 3A, Figure 4, Supplementary file 1B). Figure 4 Download asset Open asset Proportion of staff testing positive by specialty area. The number of staff tested within each speciality is shown within each bar. The error bar indicates the 95% confidence interval. The 'Other' group includes staff members without a self-reported specialty. Staff working in a specialty area are predominantly nurses, healthcare assistances, doctors and therapists. Rates of Covid-19 infection varied by staff occupational role: porters and cleaners had the highest rates (60/323, 18.6%), followed by physio-, occupational and speech and language therapists (47/316, 14.9%) and nurses/healthcare-assistants (562/3971, 14.2%). Junior medical staff had higher rates (113/853, 13.2%) than senior medical staff (57/704, 8.1%). Administrative staff had the lowest proportion (88/1218, 7.2%) of any major staff group (Figure 3A, Figure 5, Supplementary file 1B). Figure 5 Download asset Open asset Proportion of staff testing positive by role. The number of staff tested within each role is shown within each bar. The error bar indicates the 95% confidence interval. There was limited evidence that male staff were more at risk of infection than female staff (313/2562 [12.2%] positive vs. 812/7452 [10.9%], p=0.07) and that risk decreased with increasing age (univariable odds ratio [OR], per 10 years, 0.95 [95%CI 0.90–1.00, p=0.04], Figure 6). Covid-19 rates varied by self-described ethnicity. 686/7237 (9.5%) staff describing themselves as White (British/Irish/other) were infected, compared to 281/1673 (16.8%) and 71/394 (18.0%) staff describing themselves as Asian (British/Pakistani/Indian/Bangladeshi/other) or Black (British/African/Caribbean/other) respectively. Rates in staff describing themselves of mixed ethnicity or Chinese were 28/242 (11.6%) and 7/93 (7.5%) (Figure 3A, Figure 7, Supplementary file 1B). There was no evidence that the proportion of asymptomatic staff with a positive PCR and/or antibody varied by week of testing, in keeping with most asymptomatic staff testing occurring after the peak in Covid-19 in the hospital (Figure 1A–C). Figure 6 Download asset Open asset Relationship between age and Covid-19 infection in hospital staff. Panel A shows a histogram of staff ages for those attending asymptomatic screening, staff with a positive SARS-CoV-2 IgG antibody and/or PCR test at their first asymptomatic clinic attendance as shown in blue and those who were both PCR and antibody negative are shown in red. Panel B shows the univariable modelled percentage of staff positive by age, the solid line shows the expected value and the ribbon the 95% confidence interval. Figure 7 Download asset Open asset Proportion of staff testing positive by self-described ethnicity. The number of staff tested within each group is shown within each bar. The error bar indicates the 95% confidence interval. Risk factors: multivariable analysis In multivariable analysis (Figure 3B, Supplementary file 1B), controlling for factors including hospital-based Covid-19 exposure, role, specialty and ethnicity, household contact with known (adjusted OR [aOR] 4.82, 95% CI 3.45–6.72, p<0.001) or suspected (1.75, 1.37–2.24, p<0.001) cases remained important risk factors. Working in Covid-19 facing areas (2.47, 1.99–3.08, p<0.001) or throughout the hospital (1.39, 1.04–1.85, p=0.02) was associated with increased risk compared to non-Covid-19 areas, as was workplace-based exposure to a suspected or known Covid-19-positive patient without PPE (1.44, 1.24–1.67, p<0.001). The latter could not be entirely accounted for by recall-bias as the association persisted restricting to staff who did not think they had had Covid-19 (1.30, 1.06–1.59, p=0.01). Risk of Covid-19 infection varied by speciality, even after accounting for working in a Covid-19 facing area. Those working in acute medicine were at increased risk (aOR 1.52, 95% CI 1.07–2.16, p=0.02), while those working in ICUs were at lower risk (0.44, 0.28–0.69, p<0.001). Increased risk was also seen in in orthopaedics and haematology, reflecting staff-based outbreaks as these wards saw very few Covid-19 patients. The greatest risk of infection by role remained for porters and cleaners (2.06, 1.34–3.15, p=0.001). By ethnic group, Black (1.66, 1.25–2.21, p<0.001) and Asian (1.51, 1.28–1.77, p<0.001) staff were at greatest risk of Covid-19. Risk factors for presence of SARS-CoV-2 IgG antibodies were very similar to the main model with a composite point including PCR results. The same factors were selected in the multivariable model (Supplementary file 1C), with the addition of gender: male healthcare workers had increased risk of SARS-CoV-2 seropositivity (aOR 1.19, 95% CI 1.01–1.40, p=0.03). Heterogeneity in risk of Covid-19 in healthcare workers between hospitals and wards We investigated the relationship between infectious pressure from patients and the proportion of staff infected by considering each admitted patient infectious from −2 to +7 days around their first positive SARS-CoV-2 PCR. At a hospital building level (Figure 8A), the two buildings admitting most patients with Covid-19 had higher levels of staff infection (14.1%, 15.3%) than the majority of other buildings (5.4–8.6%). However, one site with low rates of patient infection and another, non-clinical site without patients had rates of 13.5% and 19.7% respectively. At a ward level (Figure 8B), there was only a weak positive correlation between Covid-19 pressure from patients and staff infection rates (R2 = 0.09, p=0.02). ICUs and the HDU had lower rates of staff infection for a given Covid-19 pressure than general Covid-19 facing wards (adjusted linear regression coefficient −29% [95% CI −46%, −12%; p=0.002]). While dedicated Covid-19 cohort wards had similar rates of staff Covid-19 to general wards overall (Supplementary file 1D), several general wards had much higher rates (Figure 8B). Figure 8 Download asset Open asset Proportion of staff infected by extent of Covid-19 infectious pressure from patients, by eight hospital buildings across four hospitals (panel A) and by ward (panel B). Covid-19 infectious pressure was calculated by considering each patient infectious from −2 to +7 days around the date of their first positive SARS-CoV-2 PCR test. Only staff working in a single hospital or ward are included in the plot. Wards with fewer than 10 staff tested are not plotted. Covid-19 cohort wards admitted only patients with suspected or known Covid-19, whereas Covid-19 general wards were acute medical wards receiving new admissions and acute medical patients initially believed not to have Covid-19. Non Covid-19 areas did not admit suspected Covid-19 patients and any suspected or confirmed Covid-19 patients were transferred off these wards as soon as possible. Contact tracing PCR-positive asymptomatic staff who had not previously had Covid-19 were asked to name all colleagues with whom they had had >5 min of face-to-face conversation or been within 2 m for >15 min, within the past 48 hr, without a face mask. During the first 2 weeks of asymptomatic screening, 130 contacts were tested 7 days after contact with their index case, and 62 re-attended at day 14. Only one contact tested positive. As this rate of detection was below the background rate, contact tracing was discontinued for asymptomatic staff. Discussion We present the results of a large and comprehensive Covid-19 staff testing programme across four teaching hospital sites in one UK county, attended by 73% of 13,800 staff employed by OUH. Using a composite outcome of either a positive PCR or serology result, by 8th June we detected evidence of Covid-19 at some time in 11.2% of staff. Put in context, UK-wide seroprevalence was 6.8% on 28th May 2020, with a higher incidence among healthcare workers than in the general population (Office of National Statistics Coronavirus, 2020). We observed varying risk to our hospital staff associated with working location, occupational role and demographic factors. The greatest risk was associated with Covid-19 infected household contacts (although only 38.5% of staff with a contact became infected) and with working in Covid-19-facing areas (22.6% vs. 8.6% elsewhere) where there was one additional SARS-CoV-2 infection per ~7 staff compared to elsewhere. On univariable analysis staff with most direct patient contact were at increased risk including porters, cleaners, nurses, healthcare-assistants, therapists and junior doctors. Adjusting for working in a Covid-19 area much of this for porters and cleaners who had the highest risk of any staff group, and who across the A heterogenous also across Covid-19-facing Risk seen on acute medical wards was greater than in the emergency department was by Covid-19 patients, whilst working on a Covid-19 facing was relatively across these areas was the of PPE and the time was PPE and face was on and HDU whereas time on other wards (Table 2). staff on and HDU in and and had dedicated and for this whereas ward staff did to 1st April 2020, in line with in acute medical areas of Covid-19 cohort wards PPE surgical and was only for contact with patients with known or suspected Covid-19, to exposure to patients in whom Covid-19 was not suspected, as patients with or likely the greater number of staff infected in several acute medical wards in the of Figure 8B), compared to Covid-19 cohort wards in Table 2 for PPE and testing, based on Public Health England February and face with above for suspected cases with history For without and for no to with history surgical and for symptomatic but unconfirmed inpatients to be risk of PPE for confirmed cases and with history surgical and risk for for suspected and confirmed Covid-19 inpatients on to Covid-19 cohort wards and on intensive care and for respiratory illness admission to hospital and either evidence of or or illness with fever above All suspected Covid-19 patients admitted via acute medicine the emergency PPE across all wards PPE for as Working in higher risk area with confirmed and PPE based on either positive swab or 'Covid-19 illness and and no admission testing for all patients of clinical The reported rates of exposure without PPE were similar among medical and staff and Supplementary file likely reflecting to staff wards to patients. admission testing was only on April 2020, and the limited availability and of testing in the of the likely of some Covid-19 is to whether PPE was protective than Increased Covid-19 in staff reporting exposure to a Covid-19 patient without PPE surgical some and from has been reported to be similar using surgical et al., However, is likely that a bundle of measures and for and increased the lower risk in and HDU staff (Figure 3, Figure As with many infection control is to was most is also likely that based on high Covid-19 rates in several wards without large of Covid-19 patients. studies analysis of the of patients and staff to Increased risk of outcomes has been reported in Black and Asian ethnic groups et al., 2020), with evidence they are also at increased risk of infection in the risk and outcomes from COVID-19, 2020; et al., 2020). we Black and Asian staff were at greater risk of infection after controlling for age, working location, role, and exposure at role be thought of as a for background but we were not to control for or other potential staff working as porters or cleaners had the greatest risk of infection is with a in reflecting of the hospital, for of to lower Multiple relationships are included within the multivariable For ethnicity via occupational role, speciality and the hospital, all subsequently infection the multivariable model the for ethnicity only the of the infection risk associated with ethnicity that is not by the other factors in the As the overall impact of ethnicity in the context of be by the univariable the reported for speciality the speciality specific risk that is not via the of the healthcare workers is included As most risk in our model was by working in a Covid-19 area than by the risks of the speciality per to patient working in Covid-19 areas at risk the for each speciality are in to a Covid-19 risk all factors in the multivariable model to be that is simultaneously for all the For an Asian Covid-19-facing medical is more likely to be infected than a this the risk of with with known Covid-19 (aOR 4.82, 95% CI We observed of remained PCR-positive at weeks Fewer staff than patients were persistently positive at 7–13 days, reflecting greater time from infection to diagnosis in asymptomatic staff compared to symptomatic patients, and/or infection in staff. However, the of patients and staff persistently positive were similar from days

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