SARS-CoV-2 infection rates and associated risk factors in healthcare settings: systematic review and meta-analysis

doi:10.21203/rs.3.rs-4602421/v1

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Systematic Review

SARS-CoV-2 infection rates and associated risk factors in healthcare settings: systematic review and meta-analysis

https://doi.org/10.21203/rs.3.rs-4602421/v1

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Background: Reducing infection rates has been crucial to protect healthcare workers (HCWs) during the COVID-19 pandemic. Therefore, we determined the rates and potential risk factors for SARS-CoV-2 infection in HCWs.

Methods: We searched MEDLINE, Embase, and Google Scholar from 1 December 2019 to 5 February 2024. The potential risk factors for SARS-CoV-2 infection in HCWs included occupational and household exposure to SARS-CoV-2; personal protective equipment (PPE) use, infection prevention and control (IPC) training; hand hygiene, aerosol generating procedures; quarantine; decontamination of high-touch areas; and working in environmental services. Odd ratios (ORs) for each risk factor were pooled from the selected studies in R.

Results: From 498 initial records, 190 articles were reviewed, and 63 studies were eligible. Globally, 10% (95% confidence interval (CI): 8-12) of 279,590 HCWs were infected with SARS-CoV-2. Household exposure (OR: 7.07; 95% CI: 3.93-12.73), working as cleaner (OR: 2.72; 95% CI: 1.39-5.32), occupational exposure (OR:1.79; 95% CI: 1.49-2.14), inadequate IPC training (OR: 1.46; 95% CI: 1.14-1.87), inefficient use of PPE (OR: 1.45; 95% CI: 1.14-1.84), performing aerosol generating procedures (OR: 1.36; 95% CI: 1.21-1.52) and inadequate hand hygiene (OR: 1.17; 95% CI: 0.79-1.73) were associated with an increased SARS-CoV-2 infection. Conversely, history of quarantine and frequent decontamination of high touch areas were protective factors against SARS-CoV-2 infection (OR: 0.23; 95% CI: 0.08-0.60; and OR: 0.52; 95% CI: 0.42-0.64 respectively). These findings indicate a tiered risk of infection in HCWs.

Conclusions and Relevance: We found high global SARS-CoV-2 infection rates of 10% among HCWs. Household exposures and working as cleaner were the strongest risk factors for SARS-CoV-2 infection, whereas history of quarantine and frequent decontamination of high touch areas were protective. We suggest a three-step strategy (minimising exposure and decontamination practices, IPC and aerosol-limiting procedure training, and PPE use) to mitigate the spread of SARS-CoV-2.

healthcare workers (HCWs)

COVID-19

SARS-CoV-2

infection

risk factor

occupational

household

quarantine

To mitigate the spread of respiratory viruses in a future outbreak/pandemic, identifying factors associated with infection and incorporating them into the current infection control and prevention (IPC) measures are essential. Therefore, we conducted a systematic review and meta-analysis of risk assessment to quantify the potential risk factors for SARS-CoV-2 infection in healthcare workers (HCWs) during the recent COVID-19 pandemic. The main risk factors for SARS-CoV-2 infection in HCWs are household exposure, working as cleaners, inefficient use of personal protective equipment (PPE), and performing aerosol generating procedures. In contrast, quarantine and frequent decontamination of high touch areas were protective factors. Here, we suggest a three-step hierarchy of controls strategy: 1) hazard elimination both in the household and at work (e.g., quarantine and frequent decontamination of high touch areas); 2) Behaviour-based safety: infection control and prevention (IPC) training and procedure training including cleaners; and 3) selection and accessibility of PPE.

There has been an increase in emerging infectious diseases with a pandemic potential in the last decades^1-3. The most recent COVID-19 pandemic caused significant and widespread morbidity and mortality, prompting changed behaviours⁴. Globally, over 775 million COVID-19 cases have been confirmed as of 14 April 2024, and there have been more than 7 million excess mortalities⁵. Healthcare workers (HCWs) have experienced considerable morbidity and mortality during the pandemic⁶ with an estimated overall global case fatality rate (CFR) of approximately 9 deaths per 1000 infections, alongside an infection rate of 14.5%. However, studies have reported infection rates as high as 59% among HCWs during the COVID-19 pandemic^7-9. Despite effective national SARS-CoV-2 control measures^7,10,11, HCWs remain disproportionately susceptible to infection, leading to nosocomial outbreaks that significantly impacted healthcare capacity due to large-scale quarantine.

Viral outbreaks and pandemics pose a continued challenge to healthcare capacity on a global scale. Healthcare institutions need to take preventive measures to limit the spread of infections at an individual and hospital level. Due to the inherent moderate transmission potential of SARS-CoV-2¹², it was among the most common nosocomial adverse events that affect patient safety. Early in the pandemic, public health warnings were put in place globally to stop the SARS-CoV-2 virus from spreading. These included handwashing, wearing masks, and physical isolation. A number of studies^7,11,13,14 have examined how well these interventions work in lowering SARS-CoV-2 incidence, transmission, and mortality. The infection prevention and control (IPC) policies that aim to curtail the spread of infectious respiratory viruses work best when multi-faceted^7,11,15.

Personal protective equipment (PPE) use is designed to protect the wearer from hazards, but it is not always effective. PPE can be unsuitable, incorrectly fitted or, not properly maintained, and used. Moreover, PPE can restrict mobility or vision, or require the wearer to carry additional weight, which may lead to musculoskeletal problems. As a result, HCWs may not wear PPEs because of discomfort, and they may then be blamed for their own infection. A critical shortage of PPEs emerged globally during the initial months of the COVID-19 pandemic. This necessitated the reuse of single-use PPE, often without established protocols for optimisation or adaptation of procedures. There is a need for coherent and simple IPC policies with continued viral surveillance to identify infection rates and potential transmission risk factors, particularly during high community spread¹⁶. Standardising respirator use across wards is crucial for staff protection¹⁶. Hand hygiene is another important measure for reducing SARS-CoV-2 transmission in healthcare settings. A systematic review published in 2021 found that community hand hygiene interventions were effective in reducing the incidence of SARS-CoV-2 infection¹³. More recently, the presence of SARS-CoV-2 RNA on the hands of primary cases and contacts, as well as on commonly touched household surfaces, is linked to SARS-CoV-2 transmission to household contacts¹⁷, but not the presence of viral RNA levels in the upper respiratory tracts of primary cases. Notably, this British study did not establish causative relationship¹⁷. Some COVID-19 pandemic mitigation measures such as quarantine and sick leave^18,19 negatively impacted healthcare capacity, including individual behavioural changes, such as fear-induced avoidance of workplaces and other public gathering places. Nonetheless, the exact risk profiling of different factors among HCWs is still largely unknown.

In this systematic review and meta-analysis, we took advantage of the considerable SARS-CoV-2 infection data among HCWs and determined the SARS-CoV-2 infection rates, thus quantifying the potential risk factors for infection. We evaluated which non-pharmacological variables reduced the spread of SARS-CoV-2 in healthcare settings, focusing on exposure elimination, usage of PPE, and hospital environmental services. The findings of this study provide insights into SARS-CoV-2 transmission in healthcare settings and will aid in hospital preparedness for emerging respiratory viral outbreaks/epidemics and pandemics.

We included previously published data; therefore, the study was exempt from ethical review and informed consents. The study followed the reporting guidelines²⁰ set forth by Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA).

Design: We conducted a systematic search and systematic review to determine global SARS-CoV-2 infection rates and identify key risk or protective factors associated with SARS-CoV-2 infection among HCWs. Eligible studies were published between 1 December 2019 to 5 February 2024, in which the association between risk factors and SARS-CoV-2 infection is quantitatively described (Table 1). SARS-CoV-2 transmission risk characterises the likelihood of an infected person transmitting the virus to a susceptible person through various routes (through-the-air at work/home and direct contact), and activities such as aerosol generating procedures, PPE use, decontamination of high touch areas, working in environmental services and hand hygiene.

This review examines transmission risk factors, including occupational and household exposure to SARS-CoV-2, and behaviour or activities listed above. Transmission risk and infection or susceptibility risk are related. While susceptibility risk is broader and includes factors like age and prior immunity, this review focuses on the aspects influencing transmission among HCWs.

Search strategy: We selected three electronic databases for study identification: PubMed, EMBASE and Google Scholar. Inclusion and exclusion criteria limited the search to human participants, English language, and selected article type (clinical trials, observational study, letters, case reports) (Table 1). Our main outcome measure was SARS-CoV-2 infection (determined by reverse transcription polymerase chain reaction (RT-PCR) test, nucleoprotein seropositivity, or spike-protein seropositivity in unvaccinated individuals). Search terms included SARS-CoV-2 infection rates, risk assessment, occupational exposure to SARS-CoV-2, household exposure to SARS-CoV-2, masking, infection prevention control training, hand hygiene, environmental/hospital infection control, COVID-19, COVID, coronavirus, Wuhan, 2019, SARS, SARS-CoV-2, coronavirus 2, 2019-ncov, SARS-2, health worker, health workforce, health professional, nurse, sero-epidemiologic studies, seroprevalence, antibodies, serological tests, risk factors, immunoglobulin, public health intervention, masking, and hand washing.

Data collection process: Studies were screened by titles and abstracts first. Table 1 describes defined inclusion and exclusion criteria. The relevant data from included studies were extracted and reviewed by the first author. The number of cases of SARS-CoV-2 infection and controls in connection with exposure variables were extracted from the existing global HCW literature. The Risk Of Bias In Non-randomized Studies - of Exposure (ROBINS-E) and Risk-of-bias VISualization (robvis) tools²¹ was used to assess the risk of bias of included studies (Supplementary Figures 1-2). The mandatory risk of bias assessment was conducted by two independent reviewers.

Statistics of meta-analysis: Quantitative synthesis of included studies was performed using both fixed and random-effects models and the metaprop and metabin function (meta²² package) in R version 4.3.2. Pooled effect estimates with corresponding 95% confidence intervals (CI) were reported. Heterogeneity among studies was assessed using I² test statistic, with two-tailed p values. For each potential risk factor, the random-effects model was used to compare the risk of infection since each study was conducted in a different population with differing effect sizes. Funnel test was used to qualitatively assess publication bias.

Registration: This systematic review was registered on OSF Registries on 21-12-2023 (DOI 10.17605/OSF.IO/VW9FN)

Results: risk factors and role of public health interventions in HCWs

We investigated the risk factors for SARS-CoV-2 infection, which included occupational exposure to SARS-CoV-2, inadequate IPC training, inefficient use of PPE at work, performing aerosol-generating procedures, hygiene measures, quarantine and household exposure.

Study selection: We used Covidence to streamline the production of the systematic review (Covidence systematic review software, Veritas Health Innovation, Melbourne, Australia. Available at www.covidence.org). The search yielded 498 studies, of which 370 studies were screened through titles and abstracts (Figure 1). A total of 190 studies were thoroughly reviewed in full text. Of these, 63 studies met the inclusion criteria and were included in this meta-analysis. Out of 63 studies, quantifiable data on infection rates was available from 60 studies.

Infection rate: Studies included data collected from December 2019 to the end of December 2021 (Table 2). All the included studies predominantly focused on HCWs without prior infection or those with a primary infection, as opposed to those with breakthrough infection. In addition, all studies were peer-reviewed and approximately half of the studies investigated the risk association with SARS-CoV-2, during a period when the ancestral strain was presumably prevalent. The SARS-CoV-2 infection rates in HCWs varied widely (ranging between 1-59%) in different parts of the world with different transmission settings^7,9,23. SARS-CoV-2 infection rates with 95% CI among HCWs were reported from 27 countries (Figure 2). Globally, 29,443 out of 279,590 HCWs were infected with SARS-CoV-2, which amounted to an infection rate of 10% (95% CI: 8-12%). We found a wider range of infection rates in the USA^24,25 (1-35%) and India^26,27 (5-20%) in 2020-21. The highest infection rates among HCWs reported in Mexico⁹ was 59% (95% CI: 49-68%) during August 2020 - January 2021, 43% (95% CI: 40-46%) in Poland²⁸ in January 2021, and 41% (95% CI: 36-47%) in DRC⁸ during July-August 2020. In contrast, Australia²⁹, Germany³⁰, Japan³¹ and Switzerland³² had the lowest HCW SARS-CoV-2 infection rates (< 2%) in 2020. As this list of studies demonstrates, there is a significant over-representation of research from high-income nations. There is limited data from South America, Africa, and the Middle East, which is likely related to inadequate surveillance in less developed countries and linguistic barriers.

Occupational exposure to SARS-CoV-2: We deducted data for occupational exposure from 56 studies including 185,712 HCWs (Figure 3 and Supplementary Figure 3). High-risk occupational exposure for HCWs was defined as direct patient care that likely exposed them to COVID-19 cases, such as HCWs working in infectious disease wards. Conversely, HCWs with minimal or no contact with COVID-19 cases, like those in the administration or other designated low-risk areas, were considered low-risk for occupational exposure. The global pooled OR for SARS-CoV-2 infection against high-risk occupational exposure was 1.79 (95% CI: 1.49-2.14; I² = 98.5%) compared to low-risk exposure; meaning that HCWs with high risk of occupational exposure were nearly twice as likely to be infected with SARS-CoV-2 than HCWs with limited or no occupational exposure. Although patient contacts play a key role in occupational exposure, the chance of being infected is influenced by other important work-related factors such as IPC training and practices, PPE use, and working tasks. Hence, this estimate of infection risk for occupational exposure requires further assessment.

Work-related factors: In healthcare settings, various factors can pose risk or protect against SARS-CoV-2 infection. Hospitals often provide IPC training for HCWs. However, the extent, the duration and the frequency of training vary largely by hospital department and between hospitals, regions, and nations, depending on the availability of resources. During the COVID-19 pandemic, inadequate IPC training encompassed insufficient training in various ways such as depth, duration and resources available. Our meta-analyses showed that the pooled OR for inadequate IPC training was 1.46 (95% CI: 1.14-1.87; I² =59%) for SARS-CoV-2 infection, including data from 6,257 HCWs derived from 7 studies^27,28,33-37 (Figure 4 and Supplementary Figure 4). Furthermore, the use of PPE as appropriate when in contact with patients or performing certain procedures is often included in IPC training for HCWs. In practice, PPE may not be efficiently used. We retrieved data for occupational exposure with inefficient PPE use from 28 studies^{8,25-27,30,32-35,37-53} including a total of 41,529 HCWs. In most studies, "inefficient PPE" encompasses two key areas: neglecting to wear PPE as recommended and/or utilizing the incorrect or malfunctioning type of PPE for the given hazard. The pooled OR for occupational exposure with inefficient PPE use was 1.45 (95% CI: 1.14-1.84; I² =79%). Additionally, performing aerosol generating procedures was associated with higher odds (OR 1.36; 95% CI: 1.21-1.52; I² =24%) of SARS-CoV-2 infectivity, including data from 36,804 HCWs extracted from 12 studies^{32-34,38,39,43,49,52,54-56}. Intriguingly, the pooled OR for history of working as a cleaner was 2.72 (95% CI: 1.39-5.32; I² =84%), using data from 10,759 HCWs retrieved from 11 studies^{8,29,38,52,55-62}.

Hygiene: We investigated whether frequent decontamination of high touch surfaces was a protective factor against SARS-CoV-2 infection. However, there is potential of bias as only 2 studies^37,47 collected this type of data from 2,163 HCWs and were included in this subgroup analysis. The pooled OR effect estimates for frequent decontamination of high touch surfaces was 0.52 (95% CI: 0.42-0.64; I² =0%) (Figure 5 and Supplementary Figure 5). In addition, hand hygiene is an important protective factor against infections. However, hand hygiene practices are often in reality not optimal. We included data on inadequate hand hygiene as a risk factor for SARS-CoV-2 infection from 10 studies^{27,28,33,34,37,42,45,47,51,63} involving a total of 9,488 HCWs. The evaluation of hand hygiene practices differed across studies, with some adhering to the national or global⁶⁴ guidelines and others relying on single-question surveys such as consistency of hand washing. Nevertheless, we found that HCWs with inadequate hand hygiene practices had higher odds of being infected with SARS-CoV-2 (pooled OR 1.17; 95% CI: 0.79-1.73; I² =63%) than those with good hand hygiene practices.

Quarantine: We extracted data from 5 studies^{48,49,63,65,66} investigating the history of quarantine as a risk factor for SARS-CoV-2 infection. HCWs with a history of quarantine were removed from work because of a close contact with a COVID-19 case. However, one study⁶⁵ quarantined HCWs who suffered from COVID-19 like illness, which might influence the results. This situation is more accurately described as isolation than quarantine. It reflects a different risk profile and prior probability of SARS-CoV-2 infection compared to asymptomatic individuals who are removed from work based on contact tracing. Data from a total of 13,941 HCWs was included in this analysis. We found the pooled OR for history of quarantine was 0.23 (95% CI: 0.08-0.60; I² =97%) against SARS-CoV-2 infection, suggesting that HCWs with a history of quarantine were protected against SARS-CoV-2 infection when returning to work (Figure 5 and Supplementary Figure 5). However, data was not available for how long the HCWs were in quarantine or how long they had been back at work before the data was collected.

Household exposure to SARS-CoV-2: Available data was retrieved from 15 studies^{32,38,45-49,54,61,62,67-69} including 54,796 HCWs and the pooled OR calculated (Figure 5 and Supplementary Figure 5). We found that the odds of being infected with SARS-CoV-2 were much higher (OR 7.07; 95% CI: 3.93-12.73; I² = 97%) for HCWs with household exposure than those with no household exposure to SARS-CoV-2. Therefore, HCWs who were exposed to SARS-CoV-2 within their household were 7 times more likely to be infected with SARS-CoV-2 than HCWs without household exposure. This highlights the importance of strengthening IPC practices, both at home and at work.

Biases and sensitivity analyses: The findings of this study revealed an asymmetrical funnel plot, suggesting potential issues like publication bias, small sample sizes, between-study heterogeneity, or random chance.Due to this limitation, we recommend cautious interpretation of the results. Estimates from random-effects models may be more appropriate, as they account for potential heterogeneity between studies.Furthermore, we evaluated the potential for bias in each estimate arising from several sources using ROBINS-E and robvis²¹. These include confounding variables, measurement errors in exposure or risk factor classification, selection bias, interventions after exposure (e.g., vaccination), missing data, outcome measurement errors (e.g., PCR and serology tests), and reporting bias. Risk of bias assessment was conducted by two independent reviewers. We then assigned each study an overall risk-of-bias rating (low, some concerns, high, and very high) based on the domain and the estimate judged to have the highest risk of bias. We found that24 studies had low concerns and 39 had some concerns (Supplementary Figures 1-2). As no individual study was rated as having high concerns for bias using the ROBINS-E tool, sensitivity analysis was not deemed necessary.

In this meta-analysis, we analysed potential risk factors for infection in HCWs during COVID-19 pandemic as a case study for future pandemic preparedness. We identified the potential risk factors for SARS-CoV-2 infection in HCWs to reduce infection rates, including household exposure, occupational exposure, PPE usage, and quarantine. We found a generally high risk of being infected by household exposure to SARS-CoV-2 globally. This suggests that IPC measures and practices are often difficult to follow at home. Our meta-analysis revealed that working in the cleaning profession, and inadequate IPC practices substantially increased SARS-CoV-2 infection risk among HCWs. Conversely, quarantine and frequent cleaning and disinfection of high-touch surfaces were protective. Therefore, we recommended a three-step strategy based upon the global risk assessment. Using a unified approach against respiratory viruses, we suggest the three-step in the hierarchy of controls, along with examples: 1) hazard elimination both at household and work including quarantine, frequent decontamination of high touch areas, and sick leaves; 2) Behaviour-based safety: IPC training of HCWs including those who perform non-clinical roles, especially cleaners; and 3) PPE: selection and accessibility of PPE for all hospital employees based upon potential levels of viral exposure. The recommendations were further subdivided as ongoing safety measures and three-step strategy in the event of outbreak(s) (Tables 3, Figure 6).

Our findings provide valuable insights and improve the implementation of evidence-based preventive strategies during potential respiratory viruses outbreaks (Figure 6). Similarly, Klompas and Rhee⁷⁰ proposed a simplified approach to respiratory viral precautions, suggesting a single set of measures that would apply to all viruses, including gowns, gloves, eye protection, and fitted respirators in well-ventilated areas. This would replace the current system, which uses different precautions for different viruses and lacks a strong evidence base⁷⁰. We propose incorporating enhanced predicting methodologies for extreme scenarios and a robust evidence-based PPE inventory management strategy as critical elements of our pandemic preparedness plan. These lessons can help to protect HCWs and patients preventing the spread of respiratory viruses. It is important to note that we did not directly compare the epidemiology of SARS-CoV-2 infection among HCWs to that of other respiratory viral infections such as influenza, SARS, and Middle East respiratory syndrome (MERS). Furthermore, new variants may be more infectious and require adjustments in different approaches.

During 2020 and 2021, our pooled data showed that 10% of HCWs globally were infected with SARS-CoV-2. We found a generally moderate occupational risk of SARS-CoV-2 infection among HCWs globally (OR: 1.8; 95% CI: 1.5-2.1). Three studies^53,71,72 found high infection rates (14-27%) among HCWs in the New York area (USA) in 2020. However, only one study⁷¹ reported substantially higher occupational risk (OR: 26; 95% CI: 24-26), which is potentially related to inadequate availability of PPE at work and higher community spread in the early period of COVID-19 pandemic. On the contrary, we found a generally high risk of being infected by household exposure to SARS-CoV-2 globally (OR: 7; 95% CI: 4-13). Particularly several studies found higher household risk among HCWs in Switzerland^32,46,54 with ORs ranging 20-317; and Chicago, USA⁶⁷ (OR: 28; 95% CI: 18-43) which is likely related to inadequate IPC precautions at home. Household exposure is a risk factor for everyone. HCWs have a likely higher baseline exposure risk to SARS-CoV-2 due to their work profile. When two risk factors come together, HCWs face a substantially higher risk of contracting the virus compared to the general public with household exposure alone. This is detrimental as frontline HCWs are regularly in contact with vulnerable patients who are at-risk of severe COVID-19. Therefore, exposure limitation strategies should be followed both at work and at home. However, we may need further refined strategies that can be applied effectively at home.

Common IPC practices including training, PPE use, hand hygiene measures, and quarantine were all likely beneficial in reducing the risk of SARS-CoV-2 infection in HCWs. Our findings align with this and highlight the importance of taking preventive measures to reduce the risk of SARS-CoV-2 infection, such as wearing appropriate PPE, washing hands frequently, and frequent decontamination of high touch areas in the event of respiratory viral outbreaks. The results of this meta-analysis provide strong evidence that IPC training, PPE use and frequent decontamination of high touch areas are effective in preventing SARS-CoV-2. The ORs for inadequate IPC training and inefficient PPE use were similar, and it suggests that both factors are similarly associated with the infection. Although not implying that one factor is irrelevant if the other is present. Both inadequate IPC training and inefficient PPE use could independently increase the odds of the infection among HCWs due to the gap between theoretical knowledge and practical application. Furthermore, we found a paradox that working as a cleaner was risk factor while frequent decontamination of high-touch surfaces was a protective measure against SARS-CoV-2 infection. Considering the vulnerability of cleaners, we highlight the need for rigorous training programs, along with feasibility studies investigating innovative approaches such cost-effectiveness of adjunct automated decontamination systems. These measures should be implemented as part of a comprehensive strategy to control the viral spread. While IPC training is noticeably important, other measures such as HCW scheduling, access limitations, and work process design, may also be helpful and require further studies to determine their role in mitigating viral exposure.

Efficient PPE use, based upon occupational exposure and risk-assessment, within healthcare settings is essential in preventing viral spread. The type of PPE required depends on the level of risk and the strength of microbial exposure. A systematic review published in 2020 found that HCWs who wore particulate-filtering facepiece respirator (N95 or equivalent) had a significantly lower risk of SARS-CoV-2 infection as compared to those who wore surgical masks or no mask⁷³. In a Norwegian cohort study, HCWs using partial PPE when managing patients with SARS-CoV-2 had 2.5-fold higher odds of being seropositive than HCW with no COVID-19 patient contact in 2020²³. As universal masking was associated with lowered SARS-CoV-2 incidence among HCWs, while the infection rate in the nearby population continued to rise⁷⁴, it protected HCWs against respiratory illness. During a respiratory viral outbreak, we recommend employing wider use of respirators and eye protection by HCWs particularly throughout patient contacts and in at-risk departments (e.g., emergency department, intensive care unit, and while managing patients at extremes of age and those with immunosuppression). There is some evidence to recommend mask wearing in healthcare settings based upon risk assessment (ORs with inefficient PPE use in HCWs were 1.45; 95% CI: 1.14-1.84; I² =79%). It is reasonable to advocate mask wearing for household contacts of HCWs who are exposed to SARS-CoV-2. Additionally, adequate caution should be taken to reduce risk of potential exposure (e.g., suspected/confirmed SARS-CoV-2 infection or other respiratory infection, close contact with patient/visitors and high-risk procedural exposure).

Physical distancing, ‘stay at home’ mandates and tele-medicine (work-from-home and home delivery of medicines) interventions played a critical role in the pandemic to limit the spread of the virus^13,73,75. Australian researchers estimated that community physical distancing behaviour lowered the risk of SARS-CoV-2 transmission/infection by 7 to 56% in Victoria in 2020¹⁵. Although, these are likely dependent on community resilience and socio-cultural factors. We found the history of quarantine to be a protective factor against SARS-CoV-2 infection in HCWs (OR 0.23; 95% CI: 0.08-0.60). While this study investigated quarantine, quantitative data on isolation, differing screening strategies, telemedicine's role and environmental measures remains a knowledge gap requiring further investigation. In addition, the role of differing testing strategies, environmental cleaning, and ventilation are potentially important for healthcare capacity in an unexplained respiratory outbreak; however, we could not find data quantifying this risk in HCWs. More research is needed to optimise their cost-effective use in different healthcare settings.

SARS-CoV-2 is likely transmitted through a spectrum rather than a single predominant mode^76,77. Transmission may primarily occur through-the-air with infectious respiratory particles (akin to droplets transmission)⁷⁸ and fomites⁷⁹ in close contact situations; however, it is less likely through faecal–oral⁸⁰ routes. Atsushi⁸¹ et al. developed a model to assess the risk of SARS-CoV-2 infection from multiple exposure pathways in healthcare settings such as hand contact, droplet spray, and inhalation of inspirable and respirable particles. They found that droplet spray was the major infection pathway (contributing to 60%–86% cases), followed by hand contact (9%–32%). Our findings support these results as we found frequent decontamination of high touch areas as a protective factor and inadequate hand hygiene as risk factor for SARS-CoV-2 infection. Additionally, like other RNA viruses, SARS-CoV-2 mutates over time. These mutations in the virus, however, might alter its properties such as how quickly it spreads, the severity of the disease, and how well vaccination, medication, diagnosis, and other public health and social initiatives work. Potential transmission mechanisms⁸² of SARS-CoV-2 variants of concern are enhanced contagious window and viral shedding^83-87, enhanced environmental stability^88,89, and improved binding to host ACE2 receptors, and reduced cross-reactivity or decay of neutralising antibodies⁹⁰. The alpha, delta and omicron variants had a greater community spread in 2020- 2021^7,91, which may influence infection rates. Published data from early 2020 to late 2021 were included in our meta-analysis and our analysis did not reveal substantial changes with differing circulating variants. This is likely due to improved access to PPE and increased knowledge gained from IPC training during the later stages of the pandemic.

Limitations of the review

This review has a few limitations. The quality of included studies was inconsistent with high heterogeneity in results and asymmetric funnel plots were found. Larger studies, often characterised by more rigorous methodologies, exhibited greater effect sizes. However, it is plausible that some smaller studies employed different methods, contributing to their stronger results. The heterogeneity observed between countries could be attributed to diverse factors like socioeconomic status, lifestyle choices, cultural practices, and hospital infection control policies. It is worth considering that high degrees of heterogeneity may reflect substantial variations in pre-existing immunity among HCWs across various geographical regions, age groups, genders, and community transmission patterns. Unfortunately, detailed covariate information (e.g., geographical regions, age groups, gender and differing SARS-CoV-2 spread and variants) was not available for most of the studies to perform sensitivity analyses. Drawing clear conclusions is hampered by some concerns of the risk of bias in included studies and differing recommendations and spread of the virus. As an alternative approach, we utilised a random-effects model, assuming that the effects being evaluated across studies do not follow identical patterns but rather conform to a distribution with an average effect at the centre and a dispersion representing the heterogeneity's extent.

In the case of an epidemic or pandemic, infection control procedures must be strictly enforced as top priority to protect HCWs. Evidence-based measures for reducing respiratory transmission in healthcare settings are ensuring quarantine or sick leave to HCWs with household exposure, appropriate IPC training for all HCWs including cleaners, reduce risk of exposure when in contact with patients by adequate PPE use, and decontamination of high touch areas. A quick and organised response will be needed to prevent the spread of respiratory viruses; therefore, we suggest a three-step hierarchy of controls including hazard elimination, IPC training, and ensuring fair PPE availability.

Acknowledgements: We pay tribute to healthcare workers for their work during the pandemic. We thank Vesna Birkic, librarian at the University of Melbourne, Australia, for helping in refining the search strategy by key risk factors and concepts (See Table 1 and Supplementary Tables 1-13 for details). We thank the Bergen COVID-19 research group members for their continued support and contribution in our two studies included in this systematic review and meta-analysis.

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SARS-CoV-2 infection rates and associated risk factors in healthcare settings: systematic review and meta-analysis

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