key: cord-1046620-rrnu28dt
authors: Wee, Liang En; Conceicao, Edwin Philip; Tan, Jing Yuan; Magesparan, Kamini Devi; Amin, Ismawati Binte Mohamad; Ismail, Bushra Binte Shaik; Xian, Toh Hui; Pinhong, Jin; Jing, Zhang; Elaine, Wee Geok Ling; Ong, Sheena Jin Min; Lee, Gillian Li Xin; Wang, Amanda En-min; Bien, Molly How Kue; Yuen, Tan Kwee; Chee, Lee Lai; Choo, Phoon Poh; Yong, Yang; Aung, May Kyawt; Sim, Xiang Ying Jean; Venkatachalam, Indumathi; Ling, Moi Lin
title: Unintended consequences of infection prevention and control measures during COVID-19 pandemic
date: 2020-11-04
journal: Am J Infect Control
DOI: 10.1016/j.ajic.2020.10.019
sha: 1821ee2c83551050a9b830c2bbf13f2f0f4a0ed2
doc_id: 1046620
cord_uid: rrnu28dt

BACKGROUND: In the current COVID-19 pandemic, aggressive Infection Prevention and Control (IPC) measures have been adopted to prevent healthcare-associated transmission of COVID-19. We evaluated the impact of a multi-modal IPC strategy originally designed for the containment of COVID-19 on the rates of other hospital-acquired-infections (HAIs). METHODOLOGY: From February-August 2020, a multi-modal IPC strategy was implemented across a large healthcare campus in Singapore, comprising improved segregation of patients with respiratory symptoms, universal masking and heightened adherence to Standard Precautions. The following rates of HAI were compared pre- and post-pandemic: healthcare-associated respiratory-viral-infection (HA-RVI), MRSA and CP-CRE acquisition rates, healthcare-facility-associated C.difficile infections (HCFA-CDI) and device-associated HAIs. RESULTS: Enhanced IPC measures introduced to contain COVID-19 had the unintended positive consequence of containing HA-RVI. The cumulative incidence of HA-RVI decreased from 9.69 cases per 10,000 patient-days to 0.83 cases per 10,000 patient-days (incidence-rate-ratio=0.08; 95%CI=0.05-0.13, p<0.05). Hospital-wide MRSA acquisition rates declined significantly during the pandemic (incidence-rate-ratio=0.54, 95%CI=0.46-0.64, p<0.05), together with central-line-associated-bloodstream infection (CLABSI) rates (incidence-rate-ratio=0.24, 95%CI=0.07-0.57, p<0.05); likely due to increased compliance with Standard Precautions. Despite the disruption caused by the pandemic, there was no increase in CP-CRE acquisition, and rates of other HAIs remained stable. CONCLUSION: Multimodal IPC strategies can be implemented at scale to successfully mitigate healthcare-associated transmission of RVIs. Good adherence to personal-protective-equipment and hand hygiene kept other HAI rates stable even during an ongoing pandemic where respiratory infections were prioritized for interventions.

In the current COVID-19 pandemic, aggressive Infection Prevention and Control (IPC) measures have been adopted to prevent healthcare-associated transmission of COVID-19. [1] The unprecedented threat of a novel pathogen provided the impetus for hospital-wide deployment of various IPC strategies, such as universal masking, visitor restrictions, and deployment of droplet and contact precautions for patients with respiratory symptoms. [2] [3] [4] Prior to the pandemic, such strategies were only deployed in high-risk units, given concerns with cost-effectiveness and sustainability. [5, 6] The current pandemic thus provides an opportunity to assess the effect of multi-modal IPC bundles when deployed at scale. However, the prioritisation of COVID-19 may have also forced compromises in other areas, potentially raising rates of other hospital-acquired infections(HAIs). [7, 8] Increases in other HAIs, such as methicillin-resistant Staphylococcus aureus (MRSA) acquisition rates, were reported during the Severe Acute Respiratory Syndrome (SARS) outbreak in 2003. [9] Similar circumstances during the COVID-19 pandemic are anticipated to result in higher rates of central-line-associated blood-stream infections (CLABSI) and other device-associated infections (DAI). [7] The challenges posed by the COVID-19 pandemic may also limit the ability of overstretched healthcare systems to sustain surveillance for HAIs.

In Singapore, a Southeast Asian city-state with close travel links to mainland China, by end-February 2020, the majority of COVID-19 cases were attributed to local transmission. [10] Previous experiences with containing SARS in 2003 meant that local hospitals implemented multi-modal IPE bundles for COVID-19 early on; including universal masking policies, improved segregation of patients with respiratory symptoms, visitor screening, and adequate personal-protective-equipment (PPE). [11] [12] [13] To-date, despite significant community transmission, rates of healthcare-associated transmission of COVID-19 are extremely low. [11] [12] [13] Hospitals were not overwhelmed by the surge in cases and adequate PPE was made available for both frontline and ancillary healthcare workers (HCWs). [14] On the largest healthcare campus in Singapore, surveillance and containment efforts for other HAIs were sustained continuously throughout the pandemic. As such, it was feasible to evaluate the impact of a multi-modal IPC strategy originally designed for the containment of COVID-19 on the rates of other HAIs throughout the pandemic period.

The Outram campus of the Singapore Health Services group hosts the Singapore General Hospital (SGH), the largest hospital in Singapore with 1785 beds, and other specialist centres. SGH has 81,495 inpatient admissions per-year. Other specialist centres on the Outram campus include the National Heart Centre, Singapore (NHCS), National Cancer Centre, Singapore (NCC), Singapore National Eye Centre (SNEC), and the National Neuroscience Institute (NNI). The NHCS, NNI, NCC and SNEC are the largest specialized centres in Singapore. We compared rates of HAI over a seven-month period during the COVID-19 pandemic (1 st February 2020-31 st August 2020), after the introduction of enhanced IPC measures, with rates of HAI over the preceding 2 years (January 2018-January 2020). Over the corresponding period, our institution cared for ≥1600 cases of COVID-19, with no evidence of patient-HCW transmission. [12] [13] [14] There was only one potential cluster (N=2) of COVID-19 cases in an RSW, though healthcare-associated transmission could not be conclusively proven. [14] Infection-prevention practices prior to COVID-19 pandemic

Prior to the pandemic, the majority of inpatients were housed in multi-bedded cohorted open wards. This posed challenges for IPC, given the increased number of patients and shared facilities in open-plan general wards, [15] and known difficulties with maintaining adequate ventilation and indoor air quality in hot and humid tropical environments. [16] While patients with respiratory symptoms and PCR-proven RVI were isolated in single rooms where possible, this was not practised consistently, given the limited number of single rooms campus-wide. A universal masking policy was practiced only in high-risk units, such as the intensive-care-units (ICUs) and wards for haematology patients. At our institution, various bundles for HAI prevention, including hand hygiene, decontamination of the environment/equipment, active surveillance cultures, contact precautions for infected and colonised patients, and device bundles 

The first case of COVID-19 in Singapore was diagnosed at our institution on the 23 rd January 2020 (epidemiological-week, E-week 4). [12] From E-week 5 onwards, hospital-wide measures were progressively introduced to mitigate the risk of healthcare-associated transmission of COVID-19.

Improved segregation was introduced for patients with respiratory symptoms. [18] Patients with respiratory symptoms but no epidemiological risk factors for COVID-19 were segregated in designated clinical areas (termed as respiratory surveillance wards, RSWs). In these RSWs, distance between beds was increased to at least 1.5 metres to encourage safe distancing and usage of surgical masks amongst hospitalized inpatients was made mandatory. [12, 13] From E-week 10-12, PPE used by staff in the RSWs was progressively upgraded to N95 respirators, faceshields, gowns and gloves; staff used surgical masks initially. Confirmed COVID-19 cases were housed in dedicated airborne-infection-isolation-rooms (AIIRs), either in the SGH's purpose-built 51-bedded isolation ward (IW) or in a 50-bedded IW extension containing AIIRs modified from containers that was constructed during the COVID-19 pandemic. [19] In the IW and RSW, cleaning was done using 1:1000 hypochlorite-based disinfectant three times a day; UV-C disinfection was also utilised post-discharge in areas housing COVID-19 cases. Cleaners in these areas were required to wear PPE (N95 respirators, eye protection, disposable gown and gloves). Beds set aside for the management of COVID-19 suspects/cases constituted almost 20% of our institution's capacity during the pandemic. [12] Simultaneously, enhanced campus-wide IPC measures were introduced in the general ward setting, to mitigate the potential risk of an unsuspected case presenting outside of areas designated for COVID-19 management. From E-week 5, a universal masking policy for all HCWs in clinical areas was introduced, with usage of a surgical mask the mandatory minimum. Regular hand hygiene with alcohol handrub was also re-emphasised. For environmental cleaning, pre-pandemic all patient areas were cleaned with 1:1000 hypochlorite-based disinfectant, at a frequency of at least three times a day; during the pandemic, cleaning practices were reinforced and regular environmental cleaning audit using fluorescent markers (Glogerm) was maintained. UV-C disinfection was also utilised at our institution since 2017; during the COVID-19 pandemic, usage of UV-C disinfection for post-discharge cleaning was continued for general ward and ICU rooms with MDRO cases, in transplant rooms, and in the operating theatres after-hours, despite increased demand for UV-C disinfection in the areas designated for COVID-19 management.

Throughout the pandemic, cohorting was maintained in the general ward setting for patients with MDROs. While the COVID-19 pandemic placed pressure on isolation beds, additional isolation capacity was provided through the container IW extension. [19] Finally, as part of visitor management, campuswide temperature screening for all visitors and visitor restrictions (one visitor per patient) were introduced from E-week 8, with entry denied to visitors with a documented fever at the point of entry. Visitors were required to wear a face mask at all times. From E-week 15 to E-week 22, a no-visitor policy was enforced throughout hospital; this was in tandem with the community-wide imposition of an elevated set of safedistancing measures to preempt the trend of increasing local transmission of COVID-19, by closing schools and all physical workplace premises. [20] . The no-visitor policy was lifted from 2 nd June onwards (E-week 23); the remaining IPC measures were continued through the end of the study period.

During the pandemic, routine surveillance cultures for MDROs were maintained. We compared the following rates of HAI pre-and during-COVID-19: healthcare-associated respiratory viral infections (HA-RVI), MRSA acquisition, CP-CRE acquisition, multi-drug-resistant (MDR) and extremely drug-resistant (XDR) Pseudomonas aeruginosa (PsA) infection, healthcare-facility-associated C.difficile infection (HCFA-CDI), and device-associated HAI.

Over the study period, all inpatients campus-wide with respiratory symptoms were tested for both COVID-19 as well as a panel of 16 common RVI via multiplex PCR. Respiratory specimens were tested 

As part of active surveillance, all patients had nasal and axillary swabs taken for MRSA testing to determine MRSA carriage status on admission; active surveillance samples were repeated at D14 and then fortnightly for long stayers. A case of MRSA carriage was defined as an instance in which MRSA was recovered from a patient regardless of the site and type of specimen (i.e., a screening or clinical diagnostic specimen). MRSA-acquisition was defined as detection of MRSA carriage in a patient whose admission swabs for MRSA were initially negative. Healthcare-associated MRSA bacteremia was defined as onset of MRSA bacteremia ≥72 hours after hospital admission. Rates of MRSA-acquisition and rates of healthcareassociated MRSA bacteremia were calculated as the total number of cases divided by the total number of patient-days over the study period.

As part of active surveillance, patients with identified risk factors (history of hospitalization in the past 1

year; transfer cases from other institutions), all admissions to Haematology, Oncology and Renal wards and all ICU admissions had rectal swabs taken for CP-CRE testing to determine carriage status at the point of admission; active surveillance samples were repeated at D14. A case of CP-CRE carriage was defined as an instance in which CP-CRE was recovered from a patient regardless of the site and type of specimen (i.e., a screening or clinical diagnostic specimen). CP-CRE-acquisition was defined as detection of CP-CRE carriage in a patient whose admission swabs for CP-CRE were initially negative. Rates of CP-CRE-acquisition were calculated as the total number of cases divided by the total number of patient-days over the study period.

At our institution, MDR/XDR P.aeruginosa (PsA) constituted one of the most common causes of MDRgram-negative infections, apart from CP-CRE. All clinical isolates with MDR/XDR PsA were identified; MDR PsA was defined as isolates that were not sensitive to at least one antibiotic from three or more different classes, while XDR PsA was defined as a subset of MDR PsA isolates that were not sensitive to at least one antibiotic from five different classes. At our institution, the five antibiotic classes included in routine testing were aminoglycosides (gentamicin and amikacin), fluoroquinolones (ciprofloxacin), antipseudomonal cephalosporins (ceftazidime and cefepime), antipseudomonal penicillins (piperacillin/tazobactam), and carbapenems (meropenem). Rates of MDR/XDR PsA infections were calculated as the total number of cases divided by the total number of patient-days over the study period.

Cases of HCFA-CDI were identified using the standard epidemiological classification of CDI. [21] Only hospital-onset healthcare facility-associated (HO-HCFA) and community-onset healthcare facilityassociated (CO-HCFA) infections were considered as nosocomial. The algorithm employed for the microbiological diagnosis of CDI at our institution remained the same throughout (sequential qualitative detection of glutamate dehydrogenase and A and B toxins from C. difficile). Discrepancies were resolved through RT-PCR testing for the C. difficile toxin gene. Rates of HCFA-CDI were calculated as the total number of cases divided by the total number of patient-days over the study period.

Data on hospital-wide central line-associated primary bloodstream infections (CLABSIs), hospital-wide catheter-associated urinary tract infections (CAUTIs), and ventilator-associated pneumonia (VAP) occurring in patients hospitalized in ICUs were prospectively collected. Definitions of CLABSI, CAUTI and VAP were based on CDC criteria, [21] and rates were calculated for CLABSI, CAUTI and VAP based on central-line days, catheter-days, and ventilator-days, respectively. Compliance with CLABSI, CAUTI and VAP bundles were monitored and audited regularly by IPE staff throughout the pandemic. The components of the various bundles are described in Supplementary Table 1 .

Rates of compliance to the World Health Organisation (WHO) "Your 5 Moments for Hand Hygiene" were continuously monitored throughout the pandemic, and hand hygiene audit results were stratified by staff and hand hygiene moment. Regular environmental cleaning audit using fluorescent markers (Glogerm) was maintained in inpatient areas, procedural areas (eg. operating theatres), and in the emergency department (ED) even during the pandemic period. The average number of UV-C disinfections carried out during the pandemic was also tracked, as well as consumption of alcohol handrub and other PPE (surgical masks, N95 respirators, disposable gloves and gowns). Hand hygiene compliance, environmental cleaning audit results and PPE consumption over a seven-month period during the COVID-19 pandemic (1st February 2020-31st August 2020) was compared to results over the preceding year, in the pre-pandemic period (January 2019-January 2020).

Comparisons of HAI rates were made using the incidence-rate-ratio (IRR) method. When comparing rates per patient-days, 95% CIs around proportions were estimated. A p-value (2-tailed) of ≤0.05 was considered significant.

Pre-pandemic, the campus-wide cumulative incidence of HA-RVI was 9.69 cases per 10,000 patient-days (989 cases; 1,020,463 patient-days) (Figure 1a) . After introduction of enhanced IPC measures, the incidence of PCR-proven HA-RVI was 0.83 cases per 10,000 patient-days (22 cases; 264,904 patient-days).

The IRR of PCR-proven HA-RVI per 10,000 patient-days between the two periods (pre-and postpandemic) was 0.08(95% confidence interval, 95%CI=0.05-0.13, p<0.05). This decrease was seen across both enveloped HA-RVI and non-enveloped-HA-RVI, and was sustained even after the lifting of community-based measures ("lockdown"). During the pandemic, admissions for community-acquired RVIs at our institution remained stable. [22] For enveloped HA-RVI, the rates fell from 6.05 cases per 10,000 patient-days (618 cases) to 0.45 cases per 10,000 patient-days (12 cases) after the introduction of enhanced IPC measures (IRR=0.07, 95%CI=0.04-0.13, p<0.05), while for non-enveloped HA-RVI, the rates fell from 3.63 cases per 10,000 patient-days to 0.38 cases per 10,000 patient-days (IRR=0.10, 95%CI=0.05-0.19, p<0.05) (Figure 1a) .

Pre-pandemic, the rate of MRSA acquisition was 11.7 cases per-10,000 patient-days (1194 cases, 1,020,463 patient-days) (Figure 1b) . During the pandemic, the rate of MRSA acquisition decreased to 6.4 cases per-10,000 patient-days (169 cases, 264,904 patient-days); the difference was statistically significant (IRR=0.54, 95%CI=0.46-0.64, p<0.05). The rate of healthcare-associated MRSA bacteremia also decreased during the pandemic (pre-pandemic: 0.36 cases per 10,000 patient-days, 37 cases, 1,020,463 patient-days; pandemic period: 0.11 cases per 10,000 patient-days, 3 cases, 264,904 patient days; IRR=0.31, 95%CI=0.06-0.97, p=0.04). There was no significant increase in CP-CRE acquisition or MDR/XDR PsA infection during the pandemic (Figure 1c, 1d) Similarly, the rate of XDR-PsA infection pre-pandemic was 0.26 cases per 10,000 patient-days (27 cases, 1,020,463 patient-days). During the pandemic, the rate of XDR-PsA infection was 0.30 cases per 10,000 patient-days (8 cases, 264,904 patient-days); this difference was not statistically significant (IRR=1.14, 95%CI=0.45-2.58, p=0.74). There was no significant increase in HCFA-CDI during the pandemic (Figure 1e) . During the pandemic, the rate of HCFA-CDI was 3.47 cases per 10,000 patient-days (92 cases, 264,904 patient-days); the difference was not statistically significant compared to the pre-pandemic period (3.65 cases per 10,000 patient-days; 373 cases, 1,020,463 patient-days; IRR=0.95, CI=0.75-1.20, p=0.66).

The reduction in HA-RVI, and stable rates of other HAIs, were likely attributed to increased compliance with segregation of symptomatic patients, and hospital-wide increases in adherence to Standard Precautions. Hand hygiene audit compliance with the WHO "Your 5 Moments for Hand Hygiene" prior to COVID-19 was 85%, compared with 100% during the COVID-19 pandemic, across all categories of HCWs and all hand hygiene moments surveyed (Figure 2a) . Standards of environmental cleaning prepandemic on regular audit using fluorescent markers (Glogerm) were high, and these standards were maintained throughout the pandemic, both in general ward areas and areas designated for the management of COVID-19 suspects (Figure 2b) . UV-C disinfection was employed more frequently, rising from an average of 16 rooms treated per day pre-pandemic to 25 rooms treated per-day during the pandemic (Figure 2c) . Similarly, the rate of handrub consumption rose from 57.5 litres/day, prior to the COVID-19 pandemic (22697 litres consumed over 395 days), to 78.7 litres/day during the COVID-19 pandemic (16691 litres over 212 days) (Figure 2d) . Consumption of PPE, including N95 respirators, surgical masks, and disposable gowns rose significantly during the COVID-19 pandemic; in particular, consumption of surgical masks tripled and consumption of N95 respirators increased by almost fivefold.

With regards to DAIs, despite the disruptions caused by the COVID-19 pandemic, hospital-wide CLABSI rates decreased substantially during the COVID-19 pandemic, likely because of increased adherence to the CLABSI bundle (Figure 3a) . Prior to the COVID-19 pandemic, the rate of CLABSI was 0.83 incidents per-1000 device-days (95 incidents, 113,466 device-days). During the COVID-19 pandemic, the CLABSI rate decreased to 0.20 incidents per-1000 device-days (5 incidents, 25154 devicedays); the difference was statistically significant (IRR=0.24, 95%CI=0.07-0.57, p<0.05). Hospital-wide CAUTI rates remained stable at 1.8 incidents per-1000 device-days; increased compliance to the CAUTI bundle was also noted during the pandemic period (Figure 3a) . Increased compliance to CLABSI and CAUTI bundles was likely due to increased hand hygiene compliance during the pandemic. Across ICUs, rates of CLABSI, CAUTI and VAP remained stable during the pandemic period (Figure 3b) . While there was an ICU-wide trend towards decreased CLABSI rates (0.42 incidents per-1000 device-days during the COVID-19 pandemic, versus 1.1 incidents per-1000 device-days pre-pandemic), this was not statistically significant (IRR=0.39, 95%CI=0.04-1.54, p=0.18).

The key finding of this study was that enhanced IPC measures during the COVID-19 pandemic had the unintended but positive consequences of reducing HA-RVI without compromising other HAIs. At our centre during COVID-19, MRSA acquisition rates actually decreased; contrasted against the experience at other centres during the SARS outbreak in 2003, when significant and substantial rises in MRSA acquisition were noted in conjunction with IPC measures introduced for SARS. [9] While the concomitant rise in MRSA acquisition during the SARS outbreak was attributed to the potential for Staphylococcal superinfection in patients with viral pneumonia, as well as inappropriate reuse of PPE, [9] emerging evidence suggests that MRSA is not commonly identified as a co-pathogen in COVID-19

pneumonia. [23] However, the usage of contact as well as droplet-based precautions for high-risk COVID-19 suspects has been associated with clusters of CLABSI, likely due to sessional usage of fullsleeved gowns which hindered hand hygiene compliance. [8] At our institution, given adequate supplies of PPE, sessional use of PPE was discouraged and gowns/gloves were changed in-between patients, to avoid the healthcare-associated transmission of organisms other than SARS-CoV-2. Adherence to PPE was also high during the pandemic at our institution; around 90% of HCWs were adherent with Droplet Precautions, and 70% adherent with Contact Precautions, during significant contact episodes with highrisk COVID-19 suspects. [24] This likely explains the absence of a corresponding rise in HAIs, even amidst the disruption of a pandemic caused by a novel respiratory pathogen, and the potential for antibiotic misuse during an ongoing pandemic. Indeed, during the pandemic, utilization of broadspectrum antibiotics such as 4 th generation cephalosporins, carbapenems and vancomycin rose by almost 25% at our institution, potentially increasing the selection pressure for MDROs. pandemic. While other studies have reported declines in HCFA-CDI during the COVID-19 pandemic from enhanced IPC measures, [28, 29] rates of HCFA-CDI at our institution remained static. Hand hygiene and environmental cleaning standards at our institution were already at high levels pre-pandemic; the marginal additional increases observed during the pandemic may not have translated into a significant impact on HCFA-CDI. Furthermore, while the rate of consumption of alcohol handrub rose significantly during the COVID-19 pandemic, alcohol-based hand sanitiser is ineffective against C.difficile spores. Prior to the COVID-19 pandemic, almost one in ten inpatients in Singaporean hospitals had some form of HAI. [30] Surveillance and prevention efforts for HAI should not be compromised during IPC efforts for COVID-19. [7, 8] Implementation of a bundle of IPC measures designed to reduce healthcare-associated transmission of COVID-19 also resulted in a significant decrease in HA-RVI. Common respiratory viruses remain a major cause of morbidity and mortality amongst hospitalized inpatients with respiratory diagnoses; [31] accounting for almost one-quarter of admissions for pneumonia. [32] [33] HA-RVI remain an underappreciated cause of morbidity and mortality in hospitalized adult inpatients, and a significant cause of severe hospital-acquired pneumonia (HAP) requiring intensive care. [33] The current COVID-19 pandemic highlights the importance of strengthening IPC measures against common respiratory viruses. Across our healthcare system, the introduction of visitor screening, improved segregation of patients with respiratory symptoms, and mandatory sick leave for symptomatic staff resulted in an unprecedented decrease in HA-RVI. While reductions in HA-RVI have been reported in other centres during the COVID-19 pandemic, [34] and a significant decrease in community-acquired RVI was noted in Singapore, attributed to the introduction of community-based COVID-19 control measures, [20] admissions for community-acquired RVI at our institution remained static during the initial phase of the pandemic. [22] The reductions seen in HA-RVI were already attained prior to the imposition of community-wide "lockdown" measures and sustained even after reversal of "lockdown"; substantial decreases in HA-RVI were thus likely attributable primarily to the hospital-based measures introduced for COVID-19 control.

Our study has the following limitations. This study was conducted in a single healthcare system; hence the findings may not be fully generalisable to other settings. Additionally, implementing enhanced IPC measures at our institution required substantial investment to support increased PPE consumption and redesign patient spaces to improve distancing. [18, 19] Redesign and addition of institutional capacity is thus necessary if these IPC gains are to be sustained in the post-pandemic era.

In conclusion, while preventing healthcare-associated spread of COVID-19 is a priority for IPC, the impetus provided by the ongoing pandemic provides a window of opportunity to demonstrate the potential benefit of heightened IPC strategies in controlling the major health problem of HAIs and

MDROs. Enhanced IPC strategies should be continued in some form even after the pandemic is over.

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igure 1: Rates of healthcare-associated infections prior to and during COVID-19 pandemic across a large healthcare system in Singapore