Investigations,actions and learning from an outbreak of SARS-CoV-2 infection among healthcare workers in the United Kingdom

Abstract

Background:

We report an outbreak of SARS coronavirus-2 (SARS-CoV-2) infection among healthcare workers (HCW) in an NHS elective healthcare facility.

Methodology:

A narrative chronological account of events after declaring an outbreak of SARS-CoV-2 among HCWs. As part of the investigations, HCWs were offered testing during the outbreak. These were: (1) screening by real-time reverse transcriptase polymerase chain reaction (RT- PCR) to detect a current infection; and (2) serum samples to determine seroprevalence.

Results:

Over 180 HCWs were tested by real-time RT-PCR for SARS-CoV-2 infection. The rate of infection was 15.2% (23.7% for clinical or directly patient-facing HCWs vs. 4.8% in non-clinical non-patient-facing HCWs). Of the infected HCWs, 57% were asymptomatic. Seroprevalence (SARS-CoV-2 IgG) among HCWs was 13%. It was challenging to establish an exact source for the outbreak. The importance of education, training, social distancing and infection prevention practices were emphasised. Additionally, avoidance of unnecessary transfer of patients and minimising cross-site working for staff and early escalation were highlighted. Establishing mass and regular screening for HCWs are also crucial to enabling the best care for patients while maintaining the wellbeing of staff.

Conclusion:

To our knowledge, this is the first UK outbreak report among HCWs and we hope to have highlighted some key issues and learnings that can be considered by other NHS staff and HCWs globally when dealing with such a task in future.

Keywords

SARS-CoV-2 IgG COVID-19 novel coronavirus pandemic

Background

The coronavirus disease 2019 (COVID-19) pandemic, caused by the highly infectious severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), has significantly increased demand on healthcare systems globally. Healthcare workers (HCW) are at the front line of the pandemic response and as such they are at a higher risk of exposure. HCW infection was a considerable challenge during the SARS 2002–2003 outbreak in Toronto, especially as a means of onward transmission (Low, 2004). Onward transmission in a healthcare setting can occur from patients to HCWs and vice versa.

Most people with SARS-CoV-2 infection develop asymptomatic or mild and uncomplicated illness. Variable incidence rates of asymptomatic cases have been reported, in the range of 1.6%–56% depending on the population studied. Other reports suggest mild to moderate cases form up to 90% of cases (Bi et al., 2020; Gao et al, 2020). Asymptomatic HCWs can act as outbreak sources, hence the importance of screening at the earliest opportunity (ideally at regular intervals) to detect cases, isolate and trace their contacts, thus preventing and/or minimising outbreaks.

During the COVID-19 crisis, private healthcare providers such as the Nuffield Health Wessex Hospital (NHWH), the Spire Hospital and the Southampton Treatment Centre (Care UK) at the Royal South Hants Hospital (RSH), were working with University Hospital Southampton NHS Foundation Trust (UHS) to provide care for patients and to relieve pressure on main NHS site facilities.

In April 2020, as part of this preparedness, it was agreed that NHWH would admit, postoperative and trauma patients with medical needs for intensive rehabilitation, after these patients had negative screens by real-time reverse transcription polymerase chain reaction (RT-PCR) or post-COVID-19 recovery and fulfilled Public Health England’s criteria for de-isolation ( i.e. re-tested negative for SARS-CoV-2 RNA before transfer). NHWH cared for up to 10 NHS and no private patients at any one time. All were in side rooms with their own toilet facilities. A number of these patients required high-level nursing intervention. On some occasions, it took up to four nurses and a physiotherapist to turn and hoist these patients.

The aim of the present study was to report investigations, actions and learning from a cluster of SARS-CoV-2 infection in NHWH among HCWs. We aim to share our findings and learning points with other healthcare and NHS providers when dealing with this novel and challenging infection.

Methodology

This is a narrative chronological account of events, during an outbreak of SARS-CoV-2 infection among HCWs in an elective surgical NHS facility.

As part of the outbreak investigations, all HCWs were offered testing during the outbreak. These were:

(1) Screening by real-time RT-PCR to detect a current infection. For this, a combined nose and throat swab were transported in VIROCULT virus transport medium. Samples were extracted and purified using magnetic particle extraction on the Thermo Scientific KingFisher Flex. PCR amplification was performed on the Applied Biosystems (ABI) 7500 by using the Viasure SAR-CoV-2 RT-PCR kit, targeting ORF1ab and N gene was. Additionally, primers and probes for the World Health Organization (WHO) E gene assay (including an internal positive amplification control from extraction) were also used to enhance the sensitivity. Two consultant virologists validated the PCR results.

(2) Serum samples to determine seroprevalence. These were obtained from the staff members who consented to the investigation. They were tested on the LIAISON® platform, for the quantitative determination of S1/S2 specific IgG antibodies to SARS-CoV-2 by chemiluminescence immunoassay (CLIA) technology (DiaSorin S.p.A.. Via Crescentino snc, Saluggia, VC, Italy).

The NHWH ordinarily provides 50 beds (only 10 beds were occupied during the outbreak), all of which have side rooms with their own toilet facilities. HCWs were classified as: (1) clinical or directly patient-facing HCWs (e.g. doctors, nurses, allied health professionals, porters, etc.); or (2) non-clinical including non-patient-facing HCWs (e.g. laboratory, clerical, administrative, information technology, secretarial, etc.).

On Thursday 7 May 2020, a HCW on duty reported feeling unwell with a tight chest The HCW was referred for SARS-CoV-2 PCR and was advised to self-isolate for at least 14 days regardless of the test result, with a back-up plan given in case of deterioration. The SARS-CoV-2 PCR test result came back positive. Later that day, a senior nurse phoned reporting symptoms compatible with infection with COVID-19, who was also referred to the NHS testing hub and later was confirmed positive for SARS-CoV-2 after admission to hospital.

After these two cases, the hospital management at the NHWH sent out a communication to all staff reiterating to adhere to infection prevention practices, including social distancing and wearing masks at all times. HCWs and staff were also advised if they had any symptoms suggestive of COVID-19 to report to occupational health for further advice and guidance.

Results

The above events and cases described in the methodology, triggered outbreak declaration, staff screening and the sequence of events, results, findings and actions are provided in Tables 1 and 2.

Table 1.

How the incident was detected, sequence of events and what actions followed.

Date	Event – what actually happened?	Subsequent actions and/ or Comments
7 May	A known asthmatic HCW on duty reported feeling unwell with chest tightness and a temperature at 10am. The HCW was an assistant on the ward, providing day-to-day care, helping with turning patients on the ward (a routine temperature check that day at 7am showed no fever). Booked SARS-CoV-2 PCR testing via the NHS hub.	The HCW was advised to self-isolate for at least 14 days, with a back-up plan given in case of deterioration.* The SARS-CoV-2 PCR test result came back positive.
	Later that day, a senior nurse phoned reporting symptoms compatible with COVID-19. They were referred to the NHS testing hub and confirmed positive following admission to hospital.	A communication went out to all staff reiterating to adhere to infection prevention practices, including social distancing and wearing masks at all times.
8–11 May	Five HCWs (potential contacts of the first case) reported COVID-19 symptoms. These were tested for SARS-CoV-2 PCR and four out of five tested positive.	NHWH’s hospital director escalated their concern to the consultant microbiologist at UHS. An outbreak was declared.
12 May	Outbreak meeting: Meeting with senior clinical staff at UHS including Medical Director, Head of Infection Prevention and Control, Consultant Microbiologist, Matron and Hospital Director from NHWH.The following key decisions and actions were made.
	Screening of all inpatients (n = 10) identified two positive asymptomatic patients;^† all 10 patients were informed of their respective results and all were transferred back to UHS and were isolated/cohorted.	Patients who were found to be PCR-negative were offered surveillance screening at days 7 and 14, including when they were transferred back to UHS.
	Screening (nose and throat swab for PCR testing) were commenced for clinical or directly patient-facing asymptomatic HCWs that had been looking after patients on the ward.	Results were available within 8 h. HCWs who were screened negative were advised to be retested at 7 and 14 days after their first test. Given this was during the height of the pandemic, all positives were regarded as true positives. Interestingly majority of the positves were detected during the first round of testing, only four HCWs were positve on the second round of testing.
13 May	Given the high rate of positivity among and heightened anxiety, a clinical decision was made to mass screen the whole staff (i.e. clinical or directly patient-facing and non-clinical including non-patient-facing at NHWH). These were performed between 13 and 15 May. Additionally, staff were offered, if they were willing to donate a serum sample, to check for SARS-CoV-2 IgG as part of an antibody test verification assessment.
14 May	Outbreak meeting key actions: A decision was made to cancel further admission to NHWH, to empty and deep clean the hospital. A surgical list for the week commencing 18 May 2020 was cancelled and not due to start operating until the following week pending results from repeated screening and the completion of the deep clean.
18–19 May	All NHWH staff had been rescreened and a number of staff provided serum samples with information on whether they had experienced symptoms of COVID-19 or not in the preceding weeks or since the pandemic started (Table 2).The hospital is empty by now and the deep clean process of the site has been commenced and completed (involving the environment and equipment undergoing the deep clean process; using detergent, steam cleaning, and hydrogen peroxide into the environment).A surgical list for the week commencing 18 May 2020 was cancelled and not due to start operating until the following week pending results from repeated screening and the completion of the deep clean.Infection Control visit and audit to NHWH by UHS Infection Control Consultant and a Consultant Microbiologist resulted in:further plans were made to changing rooms to allow good social distancing; reiterate the importance of mask wearing; social distancing in communal areas, e.g. restaurants.In the restaurant, several tables and chairs were removed and social distancing and information regarding wearing PPE was promoted in all clinical areas.
22 May	Outbreak meeting key actions: Check all actions were achieved including hospital deep clean, no further staff were affected or positive cases identified. Plan to recommence activities and opening the hospital for surgery and receiving patients on 26 May.Additionally, given the findings of staff screening, weekly screening of direct patient-facing HCWs becomes mandatory at NHWH and was rolled out to other sites.
24 May to date	Screening of all clinical direct patient-facing staff weekly	Continuous monitoring of the situation: no new positive staff or patients have been identified since 14 May

This advice was given to all symptomatic staff members with or without a positive COVID-19 test.

†

All patients (the two positives and eight negatives) were moved to UHS and followed up clinically with regular screening with full duty of candour to patients and their families.

HCW, healthcare worker; NHWH, Nuffield Health Wessex Hospital; PCR, polymerase chain reaction; PPE, personal protective equipment; UHS, University Hospital Southampton Foundation Trust.

Table 2.

Number and PCR positivity rates among staff tested for SARS-CoV-2.

	Total tested (n)	Positive result (n)	Age (years)	M: F
Clinical or directly patient-facing staff	101	24 (23.76)*	55 (22–69)	3: 25
Non-clinical, non-patient-facing staff	83	4 (4.82)
Total staff number	184	28 (15.22)	51 (19–72)	35: 149

Values are given as n (%) or median (range) unless otherwise specified. Median CT values were 23 (range = 17–33).

Among clinical or directly patient-facing HCWs, all radiographers tested negative for SARS-CoV-2 PCR.

HCW, healthcare worker; PCR, polymerase chain reaction.

As this was the height of the pandemic, there was anxiety among HCWs and concerns around staff-to-staff and staff-to-patient transmission. In total, 184 HCWs were tested by PCR within days 0, 7 and 14 after identifying the first case; 28 (15.2%) were positive for SARS-CoV-2 PCR (Table 2). PCR positivity among clinical directly patient-facing HCWs was 24 (23.7%). Out of 28 infected HCWs, 16 (57%) were and remained asymptomatic throughout. Of these 28 cases, 24 were positive within the first round of screening (five days after the first positive case). The reminder (n = 4) became positive on the second round, within eight days of the first identified case. No further positive cases were identified on subsequent screenings. Only two of the infected HCWs were admitted to hospital; they both fully recovered.

In total, 135 HCWs donated a serum sample for serology testing; 17 (~13%) had detectable levels of SARS-CoV-2 IgG, six of whom (~35%) did not recall any symptoms (temperature, cough, runny nose, sore throat, shortness of breath, loss of taste or smell) of COVID-19 since the pandemic had been declared. None of these patients had a positive PCR test during this outbreak or since the pandemic was declared on 11 March 2020.

Out of the 10 inpatients, at that time of the investigation and who had contacts with affected staff, two tested positive (PCR CT values were 23 and 27) (Table 1); the rest remained negative when tested on days 7 and 14 after potential exposure.

Discussion

To date, an accurate seroprevalence of past SARS-CoV-2 infection, among the general population and HCWs specifically, remain unknown in the UK. To our knowledge, this is the first report on seroprevalence rates among HCWs in the UK, combining 13% seroprevalence, with a total 15% PCR detectability means by late May 2020. As over half of these were asymptomatic, this adds to the challenges for infection prevention. Outbreaks may be undetected until much later down the line, especially if there are no local or national guidelines or indeed capacity to regularly screen asymptomatic HCWs.

The variable prevalence rate has been reported depending on time point; for example, in London, the reported overall adjusted prevalence among the general population increased from 1.5% in the first week of April 2020 to 12.3% by 15 April 2020, and 17.5% by 21 April 2020 (Public Health England, 2020). Additionally, HCW-related infections have been difficult to ascertain in the UK, at least until now, but government data in mid-April 2020 show that 13.8%–16.2% of positive PCR tests are from critical key workers, including NHS staff (Heneghan et al., 2020). However, this does not indicate the proportion of the NHS staff and does not account for the differences in the rate of testing among HCWs versus the general population. In a retrospective analysis of 138 patients in another study, 40 were HCWs (29%); of these, 31 (77.5%) worked on general wards, 7 (17.5%) in the emergency department and 2 (5%) in the ICU (Chen et al., 2020). These data may not be applicable to the UK NHS staff both with regards to infection prevention practices as well as the timeline of the pandemic. A UK report demonstrated an average of 14% past infection rates among HCW staff, with a steady increase from early March to late March 2020 (Hunter et al., 2020).

Unlike findings from Hunter et al. (2020), in our cohort, non-clinical, non-patient-facing HCWs had much lower positivity rates (4.8%) compared to clinical, patient-facing HCWs (23.7%). This can help future follow-up and outbreak investigations, regarding who to prioritise for screening, in resource-limited circumstances. We proportionally tested more non-clinical staff compared to Hunter et al. (Table 2). Furthermore, as two PCR positive patients were found, we think compliance with infection control practices, e.g. wearing appropriate personal protective equipment (PPE) and maintaining hand hygiene is an effective way for protecting patients.

Additionally, our investigation and data provide several important insights into the SARS-CoV-2 pandemic among HCWs and learning on managing clusters or outbreaks. First, it was challenging to establish an exact source for the outbreak. The index case had contacts with other clinical directly patient-facing HCWs and the patients. However, it is possible that a staff member was infected, asymptomatically initially or it was introduced by a patient transferred from another site but incubating when negative on screening. We appreciate that the impact of asymptomatic infection on onward transmission remains controversial. On 8 June, WHO’s COVID-19 technical lead, Dr Van Kerkhove stated, ‘From the data we have, it still seems to be rare that an asymptomatic person actually transmits onward to a secondary individual’. Our data, however, support a potentially important role of asymptomatic onward transmission of SARS-CoV-2, due to a high number of HCWs with antibodies and reported symptoms many weeks before the index case.

Regarding the importance of social distancing and infection prevention practices, before the outbreak there was limited opportunity for HCWs to socially distance in changing rooms due to space. However, after this, HCWs were advised to continue wearing masks while changing in the changing rooms and only three staff were allowed at a time. Additionally, new changing rooms on the ward were made available away from patient rooms. Adherence to hand hygiene and social distancing, particularly in communal areas such as restaurants and cafes, were reinformed. All staff had completed the COVID-19 training online and had attended the updated Infection Control and Hand Hygiene training; despite this, the outbreak occurred.

UHS introduced regular systematic screening after this outbreak to all patient-facing HCWs at all of its sites. We think this is crucial to keep the hospitals free of SARS-CoV-2, as much as feasibly possible, by enabling early identification and isolation of infected HCWs, to protect patients and the wider community at large. We do realise that, given the high infectivity of SARS-CoV-2, this is a risk-reduction approach, rather than risk elimination. The additional benefit provided by regular screening is the psychological reassurance of members of staff, an important factor in staff wellbeing.

Since the introduction of regular screening, we have not identified any further positive staff members or patients at NHWH up to the time of writing this report in early June 2020. We still had cases coming to our hospitals with COVID-19, subsequently and until now (mid-September 2020, we have not had any more cases among staff, nor among the patients we look after at the NHWH, this may be due to lower community numbers and not staff screening. Suggestions for adhering to social distancing, hand hygiene and face covering are more crucial. Screening of asymptomatic staff may be of better value when the numbers are higher in the community and further studies are required to define thresholds for asymptotic screening among HCWs outside local outbreaks.

Additionally, avoidance of unnecessary patients’ transfer both inter- and intra-hospital or sites. Minimise cross-site staff working to only essential works. This is even more challenging than norovirus outbreaks, where the incubation period is shorter and potentially have less asymptomatic shedders.

The importance of early escalation of concerns, early detection and rapid actions can help to limit spread. Again, this can be extremely difficult as most cases can be asymptomatic as we have shown in this cohort, which can potentially lead to larger outbreaks undetected for a long period of time. However, as previously stated, this event happened in May 2020, and measures introduced at the time may not be applicable when the prevalence rates are lower in the community. Nevertheless, regular asymptomatic screening of staff and patients could allow for early identification of cases or even an outbreak and implementation of control measures as soon as possible; however the threshold for deciding when to commence or stop asymptomatic screening of staff requires further studies and cost-effectiveness analyses.

Being open and transparent is key to share learnings and request support from experts and colleagues. Organising mass testing was done through willingness and cooperation of staff, support from managers and senior nursing staff. There was also significant support from the UHS microbiologists, infection prevention team, ward nurses leaders and huge support from the Southampton Specialist Virology Centre staff in testing and providing rapid results, despite the pressure on the laboratory caused by the significant increase in workload. Having results available in a timely manner is crucial to determine the next steps in the outbreak management. It also provides reassurance to staff and their families and contacts.

A site visit is invaluable in assessing the environment for any ongoing risks; these may be missed by people who have worked in the same environment for many years. During any outbreak, staff morale can be affected. Feelings of guilt and insecurity can result in a negative environment. The high mortality associated with COVID-19 could make this feeling worse. It is important that staff engagement is ensured with timely communication and support for staff in every role. The value of positive feedback during an outbreak period helps to create a positive mindset for outbreak resolution. Managing staff concerns and anxieties was addressed through availability of senior staff and advice was accessible at all times. Last, but not least, the virus itself, with an incubation period thought to extend to 14 days (median = 4–5 days), can provide additional pressure on staff and infection prevention; however, working together and addressing issues in a transparent way can help these matters, enabling the best care for patients while maintaining the wellbeing of staff.

Conclusion

Since the start of the pandemic, SARS-CoV-2 has continued to challenge healthcare professionals and policy makers. To our knowledge, this is the first UK outbreak report among HCWs and we hope to have highlighted some key issues and learnings that can be considered by other NHS staff and indeed other HCWs globally when dealing with such a task in future.

Footnotes

Acknowledgements

We would like to thank patients and relatives at NHWH and staff who not only provided samples to investigate this outbreak, but also for their cooperation and professionalism during those challenging times.

We would also like to thank all staff at the Southampton Specialist Virology Centre at the University Hospital Southampton, not only for their support with investigating this outbreak, but also for their continuous enthusiasm throughout the pandemic. We thank the clinical and nursing staff at UHS for re-accepting and looking after patients from NHWH and thanks to the managers who also provided valuable support to control this outbreak.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Peer review statement

Not commissioned; blind peer-reviewed.

ORCID iDs

Kordo Saeed

Nusreen Ahmad-Saeed

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