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Seroprevalence of SARS-CoV-2 antibodies and associated factors in healthcare workers: a systematic review and meta-analysis

Published:November 16, 2020DOI:https://doi.org/10.1016/j.jhin.2020.11.008

      Summary

      Background

      Healthcare workers (HCWs) represent a high-risk population for infection with severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2).

      Aim

      To determine the seroprevalence of SARS-CoV-2 antibodies among HCWs, and identify the factors associated with this seroprevalence.

      Methods

      The Preferred Reporting Items for Systematic Reviews and Meta-Analysis guidelines were applied for this systematic review and meta-analysis. Databases including PubMed/MEDLINE and preprint services (medRχiv and bioRχiv) were searched from inception to 24th August 2020.

      Findings

      Forty-nine studies including 127,480 HCWs met the inclusion criteria. The estimated overall seroprevalence of SARS-CoV-2 antibodies among HCWs was 8.7% (95% confidence interval 6.7–10.9%). Seroprevalence was higher in studies conducted in North America (12.7%) compared with those conducted in Europe (8.5%), Africa (8.2) and Asia (4%). Meta-regression showed that increased sensitivity of antibody tests was associated with increased seroprevalence. The following factors were associated with seropositivity: male gender; Black, Asian and Hispanic HCWs; work in a coronavirus disease 2019 (COVID-19) unit; patient-related work; front-line HCWs; healthcare assistants; shortage of personal protective equipment; self-reported belief of previous SARS-CoV-2 infection; previous positive polymerase chain reaction test; and household contact with suspected or confirmed cases of COVID-19.

      Conclusion

      The seroprevalence of SARS-CoV-2 antibodies among HCWs is high. Excellent adherence to infection prevention and control measures; sufficient and adequate personal protective equipment; and early recognition, identification and isolation of HCWs infected with SARS-CoV-2 are imperative to decrease the risk of SARS-CoV-2 infection.

      Keywords

      Introduction

      Severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) and coronavirus disease 2019 (COVID-19) emerged from Wuhan, Hubei Province, China in December 2019, and the World Health Organization (WHO) declared a pandemic situation on 11th March 2020 [
      • Li Q.
      • Guan X.
      • Wu P.
      • Wang X.
      • Zhou L.
      • Tong Y.
      • et al.
      Early transmission dynamics in Wuhan, China, of novel coronavirus-infected pneumonia.
      ]. As of 2nd October 2020, WHO reported 34,079,542 cases and 1,015,963 deaths globally due to COVID-19 [
      World Health Organization
      WHO coronavirus disease (COVID-19) dashboard.
      ].
      Healthcare workers (HCWs) are a high-risk group for infection. A recent meta-analysis with 11 studies found that the proportion of HCWs who were SARS-CoV-2 positive among all patients with COVID-19 was 10.1%, but severity and mortality among HCWs were lower than among all patients with COVID-19 [
      • Sahu A.K.
      • Amrithanand V.T.
      • Mathew R.
      • Aggarwal P.
      • Nayer J.
      • Bhoi S.
      COVID-19 in health care workers – a systematic review and meta-analysis.
      ]. This proportion varied substantially between countries: China, 4.2%; Italy, 9%; and USA, 17.8% [
      • Sahu A.K.
      • Amrithanand V.T.
      • Mathew R.
      • Aggarwal P.
      • Nayer J.
      • Bhoi S.
      COVID-19 in health care workers – a systematic review and meta-analysis.
      ]. The lower proportion in China is probably due to immediate implementation of strong public health interventions, such as lockdown measures, home isolation, quarantine measures, wearing masks and social (physical) distancing [
      • Xiang B.
      • Li P.
      • Yang X.
      • Zhong S.
      • Manyande A.
      • Feng M.
      The impact of novel coronavirus SARS-CoV-2 among healthcare workers in hospitals: an aerial overview.
      ].
      SARS-CoV-2 and COVID-19 have significant diagnostic issues, and serological tests aim to identify previous SARS-CoV-2 infection by detecting the presence of SARS-CoV-2 antibodies. It is known that SARS-CoV-2 antibody tests are accurate to detect previous SARS-CoV-2 infection if performed >14 days after the onset of symptoms, but they have very low sensitivity in the first week after symptom onset [
      • Deeks J.J.
      • Dinnes J.
      • Takwoingi Y.
      • Davenport C.
      • Spijker R.
      • Taylor-Phillips S
      Cochrane COVID-19 Diagnostic Test Accuracy Group. Antibody tests for identification of current and past infection with SARS-CoV-2.
      ]. Also, rapid diagnostic tests for SARS-CoV-2 antibodies have low pooled sensitivity (64.8) and high pooled specificity (98%), but these data suffer from low power and other significant limitations [
      • Riccò M.
      • Ferraro P.
      • Gualerzi G.
      • Ranzieri S.
      • Henry B.M.
      • Said Y.B.
      • et al.
      Point-of-care diagnostic tests for detecting SARS-CoV-2 antibodies: a systematic review and meta-analysis of real-world data.
      ].
      Knowledge of the seroprevalence of SARS-CoV-2 antibodies among HCWs is important to understand the spread of COVID-19 among healthcare facilities, and to assess the success of public health interventions. To the authors' knowledge, the overall seroprevalence of SARS-CoV-2 antibodies among HCWs and the associated factors are unknown. Thus, the primary objective of this systematic review and meta-analysis was to determine the seroprevalence of SARS-CoV-2 antibodies among HCWs, and the secondary objective was to identify the factors associated with this seroprevalence.

      Methods

      Data sources and strategy

      The Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) guidelines were applied in this systematic review and meta-analysis [
      • Moher D.
      • Liberati A.
      • Tetzla J.
      • Altman D.G.
      • Altman D.
      • Antes G.
      • et al.
      Preferred Reporting Items for Systematic Reviews and Meta-Analyses: the PRISMA Statement.
      ]. The PRISMA checklist is presented in Table S1 (see online supplementary material). PubMed/MEDLINE and preprint services (medRχiv and bioRχiv) were searched from inception to 24th August 2020. In addition, reference lists of all relevant articles were searched, and duplicates were removed. The following search strategy was used: (‘sars-cov-2 antibodies’ OR ‘COVID-19 antibodies’ OR ‘sars-cov-2’ OR ‘COVID-19’ OR antibodies) AND (‘health care personnel’ OR ‘healthcare personnel’ OR ‘health-care personnel’ OR ‘health care workers’ OR ‘health-care workers’ OR ‘healthcare workers’ OR ‘healthcare staff’ OR ‘health care staff’ OR ‘health-care staff’ OR ‘medical staff’).

      Selection and eligibility criteria

      Two authors undertook study selection independently, and a third (senior) author resolved any disagreements. All studies written in English (except case reports) that reported the seroprevalence of SARS-CoV-2 antibodies among HCWs and associated factors were included. In addition, studies reporting any serological test (e.g. enzyme-linked immunosorbent assay, chemiluminescence immunoassay) used to detect SARS-CoV-2 antibodies (IgA, IgG and IgM) in all HCWs were included. Finally, studies performed under screening conditions where HCWs were not selected for participation based on previous exposure to SARS-CoV-2 or symptoms were also included.

      Data extraction and quality assessment

      Data collected included authors, location, dates of data collection, sample size, setting, study design, antibody tests, sensitivity and specificity of antibody tests, number of HCWs with SARS-CoV-2 antibodies, factors associated with seroprevalence of SARS-CoV-2 antibodies, and level of analysis (univariate or multi-variate).
      The quality of studies was assessed using the Joanna Briggs Institute critical appraisal tools, where a nine-point scale is used for prevalence studies, an eight-point scale is used for cross-sectional studies and an 11-point scale is used for cohort studies [
      • Santos W.
      • Secoli S.R.
      • Püschel V.
      The Joanna Briggs Institute approach for systematic reviews.
      ]. In prevalence studies, a score of 8–9 indicates good quality, a score of 5–7 indicates moderate quality and a score ≤4 indicates poor quality. In cross-sectional studies, a score of 7–8 indicates good quality, a score of 4–6 indicates moderate quality and a score ≤3 indicates poor quality. In cohort studies, a score of 9–11 indicates good quality, a score of 5–8 indicates moderate quality and a score ≤4 indicates poor quality.

      Statistical analysis

      For each study, the total number of HCWs and the number of HCWs who were positive for SARS-CoV-2 antibodies were extracted. Seroprevalence and 95% confidence intervals (CI) were calculated for each included study. Seroprevalence was transformed with the Freeman–Tukey double arcsine method before pooling [
      • Barendregt J.J.
      • Doi S.A.
      • Lee Y.Y.
      • Norman R.E.
      • Vos T.
      Meta-analysis of prevalence.
      ]. Between-studies heterogeneity was assessed using Hedges Q statistic and I2 statistic. Statistical significance for Hedges Q statistic is set at P<0.1, while I2 values >75% indicate high heterogeneity [
      • Higgins J.P.T.
      • Thompson S.G.
      • Deeks J.J.
      • Altman D.G.
      Measuring inconsistency in meta-analyses.
      ]. A random effects model was applied to estimate pooled seroprevalence as heterogeneity between results was very high [
      • Higgins J.P.T.
      • Thompson S.G.
      • Deeks J.J.
      • Altman D.G.
      Measuring inconsistency in meta-analyses.
      ,
      • Ioannidis J.P.
      • Patsopoulos N.A.
      • Evangelou E.
      Heterogeneity in meta-analyses of genome-wide association investigations.
      ]. Study quality, sample size, sensitivity and specificity of antibody tests, publication type (journal or preprint service) and the continent where studies were conducted were considered as prespecified sources of heterogeneity, and explored using subgroup analysis and meta-regression analysis. In addition, leave-one-out sensitivity analysis was performed by removing one study at a time to determine the influence of each study on overall prevalence. A funnel plot and Egger's test were used to assess publication bias. P<0.05 for Egger's test indicates publication bias [
      • Egger M.
      • Davey Smith G.
      • Schneider M.
      • Minder C.
      Bias in meta-analysis detected by a simple, graphical test.
      ]. Meta-analysis was not performed for factors associated with the seroprevalence of SARS-CoV-2 antibodies as the data were very scarce. Statistical analysis was performed using OpenMeta[Analyst] [
      • Wallace B.C.
      • Schmid C.H.
      • Lau J.
      • Trikalinos T.A.
      Meta-Analyst: software for meta-analysis of binary, continuous and diagnostic data.
      ].

      Results

      Identification and selection of studies

      A flowchart of the literature search is summarized in PRISMA format (Figure 1). Initially, 3632 potential records were identified through PubMed and 103 records were identified through preprint services for health sciences (i.e. medRχiv and bioRχiv) after removal of duplicates. After screening the titles and abstracts, 3684 records were removed. Twelve additional records were identified and included after searching the reference lists. Finally, 49 studies that met the inclusion criteria were included in this meta-analysis.
      Figure 1
      Figure 1Flowchart of the literature search according to the Preferred Reporting Items for Systematic Reviews and Meta-Analysis guidelines.

      Characteristics of the studies

      The main characteristics of the 49 studies included in this systematic review and meta-analysis are shown in Table I. In total, 127,480 HCWs were included. Forty-nine studies [
      • Moscola J.
      • Sembajwe G.
      • Jarrett M.
      • Farber B.
      • Chang T.
      • McGinn T.
      • et al.
      Northwell Health COVID-19 Research Consortium
      Prevalence of SARS-CoV-2 antibodies in health care personnel in the New York City area.
      ,
      • Jeremias A.
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      • Pollack S.
      • Engellenner W.
      • Thakore A.
      • et al.
      Prevalence of SARS-CoV-2 infection among health care workers in a tertiary community hospital.
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      • Kelly G.
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      Pandemic peak SARS-CoV-2 infection and seroconversion rates in London frontline health-care workers.
      ,
      • Poulikakos D.
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      SARS-CoV-2 antibody screening in healthcare workers in a tertiary centre in North West England.
      ,
      • Steensels D.
      • Oris E.
      • Coninx L.
      • Nuyens D.
      • Delforge M.L.
      • Vermeersch P.
      • et al.
      Hospital-wide SARS-CoV-2 antibody screening in 3056 staff in a tertiary center in Belgium.
      ,
      • Blairon L.
      • Mokrane S.
      • Wilmet A.
      • Dessilly G.
      • Kabamba-Mukadi B.
      • Beukinga I.
      • et al.
      Large-scale, molecular and serological SARS-CoV-2 screening of healthcare workers in a 4-site public hospital in Belgium after COVID-19 outbreak.
      ,
      • Pallett S.
      • Rayment M.
      • Patel A.
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      • Denny S.J.
      • Charani E.
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      Point-of-care serological assays for delayed SARS-CoV-2 case identification among health-care workers in the UK: a prospective multicentre cohort study.
      ,
      • Korth J.
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      • Anastasiou O.E.
      • Krawczyk A.
      • Jahn M.
      • et al.
      SARS-CoV-2-specific antibody detection in healthcare workers in Germany with direct contact to COVID-19 patients.
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      • Martin C.
      • Montesinos I.
      • Dauby N.
      • Gilles C.
      • Dahma H.
      • Van Den Wijngaert S.
      • et al.
      Dynamics of SARS-CoV-2 RT-PCR positivity and seroprevalence among high-risk healthcare workers and hospital staff.
      ,
      • Amendola A.
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      • Folgori L.
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      • Bianchi S.
      • Gori M.
      • et al.
      Low seroprevalence of SARS-CoV-2 infection among healthcare workers of the largest children hospital in Milan during the pandemic wave.
      ,
      • Self W.H.
      • Tenforde M.W.
      • Stubblefield W.B.
      • Feldstein L.R.
      • Steingrub J.S.
      • Shapiro N.I.
      • et al.
      Seroprevalence of SARS-CoV-2 among frontline health care personnel in a multistate hospital network-13 academic medical centers, April–June 2020.
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      • Grant J.J.
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      Seroprevalence of SARS-CoV-2 antibodies in healthcare workers at a London NHS trust.
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      The prevalence of severe acute respiratory coronavirus virus 2 (SARS-CoV-2) IgG antibodies in intensive care unit (ICU) healthcare personnel (HCP) and its implications – a single-center, prospective, pilot study.
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      • Moscola J.
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      • Jarrett M.
      • Farber B.
      • Chang T.
      • McGinn T.
      • et al.
      Northwell Health COVID-19 Research Consortium
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      ,
      • Jeremias A.
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      • Thakore A.
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      Prevalence of SARS-CoV-2 infection among health care workers in a tertiary community hospital.
      ,
      • Steensels D.
      • Oris E.
      • Coninx L.
      • Nuyens D.
      • Delforge M.L.
      • Vermeersch P.
      • et al.
      Hospital-wide SARS-CoV-2 antibody screening in 3056 staff in a tertiary center in Belgium.
      ,
      • Blairon L.
      • Mokrane S.
      • Wilmet A.
      • Dessilly G.
      • Kabamba-Mukadi B.
      • Beukinga I.
      • et al.
      Large-scale, molecular and serological SARS-CoV-2 screening of healthcare workers in a 4-site public hospital in Belgium after COVID-19 outbreak.
      ,
      • Korth J.
      • Wilde B.
      • Dolff S.
      • Anastasiou O.E.
      • Krawczyk A.
      • Jahn M.
      • et al.
      SARS-CoV-2-specific antibody detection in healthcare workers in Germany with direct contact to COVID-19 patients.
      ,
      • Martin C.
      • Montesinos I.
      • Dauby N.
      • Gilles C.
      • Dahma H.
      • Van Den Wijngaert S.
      • et al.
      Dynamics of SARS-CoV-2 RT-PCR positivity and seroprevalence among high-risk healthcare workers and hospital staff.
      ,
      • Amendola A.
      • Tanzi E.
      • Folgori L.
      • Barcellini L.
      • Bianchi S.
      • Gori M.
      • et al.
      Low seroprevalence of SARS-CoV-2 infection among healthcare workers of the largest children hospital in Milan during the pandemic wave.
      ,
      • Self W.H.
      • Tenforde M.W.
      • Stubblefield W.B.
      • Feldstein L.R.
      • Steingrub J.S.
      • Shapiro N.I.
      • et al.
      Seroprevalence of SARS-CoV-2 among frontline health care personnel in a multistate hospital network-13 academic medical centers, April–June 2020.
      ,
      • Grant J.J.
      • Wilmore S.
      • McCann N.S.
      • Donnelly O.
      • Lai R.
      • Kinsella M.J.
      • et al.
      Seroprevalence of SARS-CoV-2 antibodies in healthcare workers at a London NHS trust.
      ,
      • Hunter E.
      • Price D.A.
      • Murphy E.
      • van der Loeff I.S.
      • Baker K.F.
      • Lendrem D.
      • et al.
      First experience of COVID-19 screening of health-care workers in England.
      ,
      • Plebani M.
      • Padoan A.
      • Fedeli U.
      • Schievano E.
      • Vecchiato E.
      • Lippi G.
      • et al.
      SARS-CoV-2 serosurvey in health care workers of the Veneto region.
      ,
      • Mansour M.
      • Leven E.
      • Muellers K.
      • Stone K.
      • Mendu D.R.
      • Wajnberg A.
      Prevalence of SARS-CoV-2 antibodies among healthcare workers at a tertiary academic hospital in New York City.
      ,
      • Sotgiu G.
      • Barassi A.
      • Miozzo M.
      • Saderi L.
      • Piana A.
      • Orfeo N.
      • et al.
      SARS-CoV-2 specific serological pattern in healthcare workers of an Italian COVID-19 forefront hospital.
      ,
      • Garcia-Basteiro A.L.
      • Moncunill G.
      • Tortajada M.
      • Vidal M.
      • Guinovart C.
      • Jiménez A.
      • et al.
      Seroprevalence of antibodies against SARS-CoV-2 among health care workers in a large Spanish reference hospital.
      ,
      • Sydney E.
      • Kishore P.
      • Laniado I.
      • Rucker L.
      • Bajaj K.
      • Zinaman M.
      Antibody evidence of SARS-CoV-2 infection in healthcare workers in the Bronx.
      ,
      • Stubblefield W.B.
      • Talbot H.K.
      • Feldstein L.
      • Tenforde M.W.
      • Rasheed M.
      • Mills L.
      • et al.
      Seroprevalence of SARS-CoV-2 among frontline healthcare personnel during the first month of caring for COVID-19 patients – Nashville, Tennessee.
      ,
      • Lackermair K.
      • William F.
      • Grzanna N.
      • Lehmann E.
      • Fichtner S.
      • Kucher H.B.
      • et al.
      Infection with SARS-CoV-2 in primary care health care workers assessed by antibody testing.
      ,
      • Paderno A.
      • Fior M.
      • Berretti G.
      • Schreiber A.
      • Grammatica A.
      • Mattavelli D.
      • et al.
      SARS-CoV-2 infection in health care workers: cross-sectional analysis of an otolaryngology unit.
      ,
      • Kassem A.M.
      • Talaat H.
      • Shawky S.
      • Fouad R.
      • Amer K.
      • Elnagdy T.
      • et al.
      SARS-CoV-2 infection among healthcare workers of a gastroenterological service in a tertiary care facility.
      ,
      • Iversen K.
      • Bundgaard H.
      • Hasselbalch R.B.
      • Kristensen J.H.
      • Nielsen P.B.
      • Pries-Heje M.
      • et al.
      Risk of COVID-19 in health-care workers in Denmark: an observational cohort study.
      ,
      • Fusco F.M.
      • Pisaturo M.
      • Iodice V.
      • Bellopede R.
      • Tambaro O.
      • Parrella G.
      • et al.
      COVID-19 among healthcare workers in a specialist infectious diseases setting in Naples, Southern Italy: results of a cross-sectional surveillance study.
      ,
      • Xu X.
      • Sun J.
      • Nie S.
      • Li H.
      • Kong Y.
      • Liang M.
      • et al.
      Seroprevalence of immunoglobulin M and G antibodies against SARS-CoV-2 in China.
      ,
      • Galán I.
      • Velasco M.
      • Casas M.L.
      • Goyanes M.J.
      • Rodriguez-Caravaca G.
      • Losa J.E.
      • et al.
      SARS CoV-2 seroprevalence among all workers in a teaching hospital in Spain: unmasking the risk.
      ,

      Psichogiou M, Karabinis A, Pavlopoulou I, Basoulis D, Petsios K, Roussos S, et al. Antibodies against SARS-CoV-2 among health care workers in a country with low burden of COVID-19. PLoS One 2020;15:e0243025

      ,
      • Fujita K.
      • Kada S.
      • Kanai O.
      • Hata H.
      • Odagaki T.
      • Satoh-Asahara N.
      • et al.
      Quantitative SARS-CoV-2 antibody screening of healthcare workers in the southern part of Kyoto city during the COVID-19 peri-pandemic period.
      ,
      • Rudberg A.S.
      • Havervall S.
      • Manberg A.
      • Falk A.J.
      • Aguilera K.
      • Ng H.
      • et al.
      SARS-CoV-2 exposure, symptoms and seroprevalence in health care workers.
      ,
      • Shields A.M.
      • Faustini S.E.
      • Perez-Toledo M.
      • Jossi S.
      • Aldera E.L.
      • Allen J.D.
      • et al.
      SARS-CoV-2 seroconversion in health care workers.
      ] investigated factors for SARS-CoV-2 antibody positivity.
      Table IMain characteristics of studies included in the systematic review and meta-analysis
      ReferenceCity or state/countryFemales (%)Age (years), mean (SD)Sample size (N)Study designSampling methodResponse rate (%)Dates of data collectionSettingPublication
      Moscola et al., 2020 [
      • Moscola J.
      • Sembajwe G.
      • Jarrett M.
      • Farber B.
      • Chang T.
      • McGinn T.
      • et al.
      Northwell Health COVID-19 Research Consortium
      Prevalence of SARS-CoV-2 antibodies in health care personnel in the New York City area.
      ]
      New York/USA73.742.7 (17.1)40,329Cross-sectionalConvenience sampling65.120 April–23 JunePrimary care facilities and hospitalsJournal
      Jeremias et al., 2020 [
      • Jeremias A.
      • Nguyen J.
      • Levine J.
      • Pollack S.
      • Engellenner W.
      • Thakore A.
      • et al.
      Prevalence of SARS-CoV-2 infection among health care workers in a tertiary community hospital.
      ]
      New York/USA70.242.8 (13.8)1699Cross-sectionalConvenience samplingNR1 March–30 AprilHospitalsJournal
      Houlihan et al., 2020 [
      • Houlihan C.F.
      • Vora N.
      • Byrne T.
      • Lewer D.
      • Kelly G.
      • Heaney J.
      • et al.
      Pandemic peak SARS-CoV-2 infection and seroconversion rates in London frontline health-care workers.
      ]
      London/UKNR35.8 (11.2)181CohortConvenience samplingNR26 March–8 AprilHospitalsJournal
      Poulikakos et al., 2020 [
      • Poulikakos D.
      • Sinha S.
      • Kalra P.A.
      SARS-CoV-2 antibody screening in healthcare workers in a tertiary centre in North West England.
      ]
      North West England/UK73NR281PrevalenceConvenience samplingNRNRHospitalsJournal
      Steensels et al., 2020 [
      • Steensels D.
      • Oris E.
      • Coninx L.
      • Nuyens D.
      • Delforge M.L.
      • Vermeersch P.
      • et al.
      Hospital-wide SARS-CoV-2 antibody screening in 3056 staff in a tertiary center in Belgium.
      ]
      Genk/BelgiumNRNR3056Cross-sectionalConvenience sampling7422–30 AprilHospitalsJournal
      Blairon et al., 2020 [
      • Blairon L.
      • Mokrane S.
      • Wilmet A.
      • Dessilly G.
      • Kabamba-Mukadi B.
      • Beukinga I.
      • et al.
      Large-scale, molecular and serological SARS-CoV-2 screening of healthcare workers in a 4-site public hospital in Belgium after COVID-19 outbreak.
      ]
      Brussels/Belgium72.443.9 (1.7)
      For females.


      47.4 (2.1)
      For males.
      1485Cross-sectionalConvenience sampling47.725 May–19 JuneHospitalsJournal
      Pallett et al., 2020 [
      • Pallett S.
      • Rayment M.
      • Patel A.
      • Fitzgerald-Smith S.
      • Denny S.J.
      • Charani E.
      • et al.
      Point-of-care serological assays for delayed SARS-CoV-2 case identification among health-care workers in the UK: a prospective multicentre cohort study.
      ]
      London/UK72.739.1 (12.1)6440CohortConvenience samplingNR8 April–12 JuneHospitalsJournal
      Korth et al., 2020 [
      • Korth J.
      • Wilde B.
      • Dolff S.
      • Anastasiou O.E.
      • Krawczyk A.
      • Jahn M.
      • et al.
      SARS-CoV-2-specific antibody detection in healthcare workers in Germany with direct contact to COVID-19 patients.
      ]
      Essen/GermanyNRNR316Cross-sectionalConvenience sampling6525 March–21 AprilHospitalsJournal
      Martin et al., 2020 [
      • Martin C.
      • Montesinos I.
      • Dauby N.
      • Gilles C.
      • Dahma H.
      • Van Den Wijngaert S.
      • et al.
      Dynamics of SARS-CoV-2 RT-PCR positivity and seroprevalence among high-risk healthcare workers and hospital staff.
      ]
      Brussels/Belgium7337 (11.3)326CohortConvenience sampling87.315 April–18 MayHospitalsJournal
      Amendola et al., 2020 [
      • Amendola A.
      • Tanzi E.
      • Folgori L.
      • Barcellini L.
      • Bianchi S.
      • Gori M.
      • et al.
      Low seroprevalence of SARS-CoV-2 infection among healthcare workers of the largest children hospital in Milan during the pandemic wave.
      ]
      Milan/Italy83.7NR547Cross-sectionalConvenience sampling89.415 AprilHospitalsJournal
      Self et al., 2020 [
      • Self W.H.
      • Tenforde M.W.
      • Stubblefield W.B.
      • Feldstein L.R.
      • Steingrub J.S.
      • Shapiro N.I.
      • et al.
      Seroprevalence of SARS-CoV-2 among frontline health care personnel in a multistate hospital network-13 academic medical centers, April–June 2020.
      ]
      Washington, Oregon, California, Minnesota, Tennessee, Ohio, North Carolina, New York, Massachusetts, Utah, Colorado, Maryland/USA65.638.5 (12.6)3248Cross-sectionalConvenience samplingNR3 April–19 MayHospitalsJournal
      Grant et al., 2020 [
      • Grant J.J.
      • Wilmore S.
      • McCann N.S.
      • Donnelly O.
      • Lai R.
      • Kinsella M.J.
      • et al.
      Seroprevalence of SARS-CoV-2 antibodies in healthcare workers at a London NHS trust.
      ]
      London/UKNR40.3 (11.1)2004Cross-sectionalConvenience sampling54.215 May–5 JunePrimary care facilities and hospitalsJournal
      Mughal et al., 2020 [
      • Mughal M.S.
      • Kaur I.P.
      • Patton C.D.
      • Mikhail N.H.
      • Vareechon C.
      • Granet K.M.
      The prevalence of severe acute respiratory coronavirus virus 2 (SARS-CoV-2) IgG antibodies in intensive care unit (ICU) healthcare personnel (HCP) and its implications – a single-center, prospective, pilot study.
      ]
      New Jersey/USA7538.5 (15.4)121PrevalenceConvenience samplingNR1 March–30 AprilHospitalsJournal
      Hunter et al., 2020 [
      • Hunter E.
      • Price D.A.
      • Murphy E.
      • van der Loeff I.S.
      • Baker K.F.
      • Lendrem D.
      • et al.
      First experience of COVID-19 screening of health-care workers in England.
      ]
      Indiana/USA70.143 (NR)690Cross-sectionalConvenience samplingNR29 April–8 MayHospitalsJournal
      Plebani et al., 2020 [
      • Plebani M.
      • Padoan A.
      • Fedeli U.
      • Schievano E.
      • Vecchiato E.
      • Lippi G.
      • et al.
      SARS-CoV-2 serosurvey in health care workers of the Veneto region.
      ]
      Veneto Region/Italy71.643.2 (11.6)8285Cross-sectionalConvenience samplingNR22 February–29 MayPrimary care facilities and hospitalsJournal
      Mansour et al., 2020 [
      • Mansour M.
      • Leven E.
      • Muellers K.
      • Stone K.
      • Mendu D.R.
      • Wajnberg A.
      Prevalence of SARS-CoV-2 antibodies among healthcare workers at a tertiary academic hospital in New York City.
      ]
      New York/USA4638.4 (10.8)285Cross-sectionalConvenience samplingNR24 March–4 AprilHospitalsJournal
      Sotgiu et al., 2020 [
      • Sotgiu G.
      • Barassi A.
      • Miozzo M.
      • Saderi L.
      • Piana A.
      • Orfeo N.
      • et al.
      SARS-CoV-2 specific serological pattern in healthcare workers of an Italian COVID-19 forefront hospital.
      ]
      Milan/Italy65.344.6 (14.2)202Cross-sectionalConvenience samplingNR2–16 AprilHospitalsJournal
      Garcia-Basteiro et al., 2020 [
      • Garcia-Basteiro A.L.
      • Moncunill G.
      • Tortajada M.
      • Vidal M.
      • Guinovart C.
      • Jiménez A.
      • et al.
      Seroprevalence of antibodies against SARS-CoV-2 among health care workers in a large Spanish reference hospital.
      ]
      Barcelona/Spain72.142.1 (11.6)578Cross-sectionalRandom sampling74.39 MarchHospitalsJournal
      Sydney et al., 2020 [
      • Sydney E.
      • Kishore P.
      • Laniado I.
      • Rucker L.
      • Bajaj K.
      • Zinaman M.
      Antibody evidence of SARS-CoV-2 infection in healthcare workers in the Bronx.
      ]
      New York/USANRNR1700Cross-sectionalConvenience samplingNR28 April–4 MayHospitalsJournal
      Khalil et al., 2020 [
      • Khalil A.
      • Hill R.
      • Wright A.
      • Ladhani S.
      • O’Brien P.
      SARS-CoV-2-specific antibody detection in healthcare workers in a UK maternity hospital: correlation with SARS-CoV-2 RT-PCR results.
      ]
      London/UKNRNR190PrevalenceConvenience samplingNR15–28 MayHospitalsJournal
      Stubblefield et al., 2020 [
      • Stubblefield W.B.
      • Talbot H.K.
      • Feldstein L.
      • Tenforde M.W.
      • Rasheed M.
      • Mills L.
      • et al.
      Seroprevalence of SARS-CoV-2 among frontline healthcare personnel during the first month of caring for COVID-19 patients – Nashville, Tennessee.
      ]
      Tennessee/USA65.533.7 (8.7)249Cross-sectionalConvenience samplingNR3–13 AprilHospitalsJournal
      Lackermair et al., 2020 [
      • Lackermair K.
      • William F.
      • Grzanna N.
      • Lehmann E.
      • Fichtner S.
      • Kucher H.B.
      • et al.
      Infection with SARS-CoV-2 in primary care health care workers assessed by antibody testing.
      ]
      Bavaria/Germany8337.9 (4)151Cross-sectionalConvenience sampling63.72–6 AprilPrimary care facilitiesJournal
      Paderno et al., 2020 [
      • Paderno A.
      • Fior M.
      • Berretti G.
      • Schreiber A.
      • Grammatica A.
      • Mattavelli D.
      • et al.
      SARS-CoV-2 infection in health care workers: cross-sectional analysis of an otolaryngology unit.
      ]
      Brescia/Italy65.541 (NR)58Cross-sectionalConvenience sampling100NRHospitalsJournal
      Kassem et al., 2020 [
      • Kassem A.M.
      • Talaat H.
      • Shawky S.
      • Fouad R.
      • Amer K.
      • Elnagdy T.
      • et al.
      SARS-CoV-2 infection among healthcare workers of a gastroenterological service in a tertiary care facility.
      ]
      Cairo/Egypt59.532.5 (5.2)74Cross-sectionalConvenience sampling58.71–14 JuneHospitalsJournal
      Olalla et al., 2020 [
      • Olalla J.
      • Correa A.M.
      • Martín-Escalante M.D.
      • Hortas M.L.
      • Martin-Sendarrubias M.J.
      • Fuentes V.
      • et al.
      Search for asymptomatic carriers of SARS-CoV-2 in healthcare workers during the pandemic: a Spanish experience.
      ]
      Marbella/Spain8041.5 (8.9)498PrevalenceConvenience samplingNR15–25 AprilHospitalsJournal
      Iversen et al., 2020 [
      • Iversen K.
      • Bundgaard H.
      • Hasselbalch R.B.
      • Kristensen J.H.
      • Nielsen P.B.
      • Pries-Heje M.
      • et al.
      Risk of COVID-19 in health-care workers in Denmark: an observational cohort study.
      ]
      Capital Region of Denmark/Denmark78.944.4 (12.6)28,792Cross-sectionalConvenience sampling96.317–22 AprilHospitalsJournal
      Hains et al., 2020 [
      • Hains D.S.
      • Schwaderer A.L.
      • Carroll A.E.
      • Starr M.C.
      • Wilson A.C.
      • Amanat F.
      • et al.
      Asymptomatic seroconversion of immunoglobulins to SARS-CoV-2 in a pediatric dialysis unit.
      ]
      Indiana/USA8841.2 (9.2)25PrevalenceConvenience samplingNR25 March–11 AprilHospitalsJournal
      Solodky et al., 2020 [
      • Solodky M.L.
      • Galvez C.
      • Russias B.
      • Detourbet P.
      • N'Guyen-Bonin V.
      • Herr A.L.
      • et al.
      Lower detection rates of SARS-COV2 antibodies in cancer patients versus health care workers after symptomatic COVID-19.
      ]
      Lyon/FranceNRNR244PrevalenceConvenience samplingNR1 March–16 AprilHospitalsJournal
      Behrens et al., 2020 [
      • Behrens G.
      • Cossmann A.
      • Stankov M.V.
      • Witte T.
      • Ernst D.
      • Happle C.
      • et al.
      Perceived versus proven SARS-CoV-2-specific immune responses in health-care professionals.
      ]
      Hannover, Germany6536.5 (11.3)217PrevalenceConvenience samplingNR23 March–17 AprilHospitalsJournal
      Brandstetter et al., 2020 [
      • Brandstetter S.
      • Roth S.
      • Harner S.
      • Buntrock-Döpke H.
      • Toncheva A.A.
      • Borchers N.
      • et al.
      Symptoms and immunoglobulin development in hospital staff exposed to a SARS-CoV-2 outbreak.
      ]
      Regensburg/Germany85.118–35 years, 35.8%; 36–50 years, 35.8%; 51–65 years, 28.4%201PrevalenceConvenience samplingNRNRHospitalsJournal
      Fusco et al., 2020 [
      • Fusco F.M.
      • Pisaturo M.
      • Iodice V.
      • Bellopede R.
      • Tambaro O.
      • Parrella G.
      • et al.
      COVID-19 among healthcare workers in a specialist infectious diseases setting in Naples, Southern Italy: results of a cross-sectional surveillance study.
      ]
      Naples/Italy4942.1 (14.6)115Cross-sectionalConvenience sampling95.823 March–2 AprilHospitalsJournal
      Lahner et al., 2020 [
      • Lahner E.
      • Dilaghi E.
      • Prestigiacomo C.
      • Alessio G.
      • Marcellini L.
      • Simmaco M.
      • et al.
      Prevalence of SARS-CoV-2 infection in health workers (HWs) and diagnostic test performance: the experience of a teaching hospital in central Italy.
      ]
      Rome/Italy63.845.2 (11.1)2115PrevalenceConvenience samplingNR18 March–27 AprilHospitalsJournal
      Schmidt et al., 2020 [
      • Schmidt S.B.
      • Grüter L.
      • Boltzmann M.
      • Rollnik J.D.
      Prevalence of serum IgG antibodies against SARS-CoV-2 among clinic staff.
      ]
      Hessisch Oldendorf/Germany8018–29 years, 14.3%; 30–49 years, 40%; 50–64 years, 44.2%; >64 years, 1.5%406PrevalenceConvenience sampling77.320–30 AprilHospitalsJournal
      Xu et al., 2020 [
      • Xu X.
      • Sun J.
      • Nie S.
      • Li H.
      • Kong Y.
      • Liang M.
      • et al.
      Seroprevalence of immunoglobulin M and G antibodies against SARS-CoV-2 in China.
      ]
      Hubei Province, Chongqing, Guangzhou, Guangdong/China75.237.1 (13.3)4384Cross-sectionalConvenience samplingNR9 March–10 AprilHospitalsJournal
      Zhao et al., 2020 [
      • Zhao R.
      • Li M.
      • Song H.
      • Chen J.
      • Ren W.
      • Feng Y.
      • et al.
      Early detection of SARS-CoV-2 antibodies in COVID-19 patients as a serologic marker of infection.
      ]
      Beijing, Zhejiang province/ChinaNRNR276PrevalenceConvenience samplingNRNRHospitalsJournal
      Fernández-Rivas et al., 2020 [
      • Fernández-Rivas G.
      • Quirant-Sánchez B.
      • González V.
      • Doladé M.
      • Martinez-Caceres E.
      • Piña M.
      • et al.
      Seroprevalence of SARS-CoV-2 IgG specific antibodies among healthcare workers in the northern metropolitan area of Barcelona, Spain, after the first pandemic wave.
      ]
      Barcelona/Spain7643.8 (12.4)7563PrevalenceConvenience sampling81.24–22 MayPrimary care facilities and hospitalsPreprint service
      Kammon et al., 2020 [
      • Kammon A.M.
      • El-Arabi A.A.
      • Erhouma E.A.
      • Mehemed T.M.
      • Mohamed O.A.
      Seroprevalence of antibodies against SARS-CoV-2 among public community and health-care workers in Alzintan City of Libya.
      ]
      Alzintan/Libya53>40 years, 37.4%77PrevalenceConvenience samplingNR2 April–18 MayHospitalsPreprint service
      Xiong et al., 2020 [
      • Xiong S.
      • Guo C.
      • Dittmer U.
      • Zheng X.
      • Wang B.
      The prevalence of antibodies to SARS-CoV-2 in asymptomatic healthcare workers with intensive exposure to COVID-19.
      ]
      Wuhan/China88.531.2 (4.7)797PrevalenceConvenience samplingNR12 February–17 MarchHospitalsPreprint service
      Galán et al., 2020 [
      • Galán I.
      • Velasco M.
      • Casas M.L.
      • Goyanes M.J.
      • Rodriguez-Caravaca G.
      • Losa J.E.
      • et al.
      SARS CoV-2 seroprevalence among all workers in a teaching hospital in Spain: unmasking the risk.
      ]
      Madrid/Spain73.943.8 (11.1)2590Cross-sectionalConvenience sampling90.514–27 AprilHospitalsPreprint service
      Nakamura et al., 2020 [
      • Nakamura A.
      • Sato R.
      • Ando S.
      • Oana N.
      • Nozaki E.
      • Endo H.
      • et al.
      Seroprevalence of antibodies to SARS-CoV-2 in healthcare workers in non-epidemic region: a hospital report in Iwate Prefecture, Japan.
      ]
      Iwate/Japan73.640 (11)1000PrevalenceConvenience sampling76.818–29 MayHospitalsPreprint service
      Psichogiou et al., 2020 [

      Psichogiou M, Karabinis A, Pavlopoulou I, Basoulis D, Petsios K, Roussos S, et al. Antibodies against SARS-CoV-2 among health care workers in a country with low burden of COVID-19. PLoS One 2020;15:e0243025

      ]
      Athens/Greece69.746.4 (10.3)1495Cross-sectionalConvenience sampling7713 April–15 MayHospitalsPreprint service
      Chibwana et al., 2020 [
      • Chibwana M.G.
      • Jere K.C.
      • Kamngona R.
      • Mandolo J.
      • Katunga-Phiri V.
      • Tembo D.
      • et al.
      High SARS-CoV-2 seroprevalence in health care workers but relatively low numbers of deaths in urban Malawi.
      ]
      Blantyre/Malawi5331.4 (7.3)500PrevalenceConvenience samplingNR22 May–19 JuneHospitalsPreprint service
      Tosato et al., 2020 [
      • Tosato F.
      • Pelloso M.
      • Gallo N.
      • Giraudo C.
      • Llanaj G.
      • Cosma C.
      • et al.
      Severe acute respiratory syndrome coronavirus 2 serology in asymptomatic healthcare professionals: preliminary experience of a tertiary Italian academic center.
      ]
      Padova/Italy8847 (10)133PrevalenceConvenience samplingNRNRHospitalsPreprint service
      Paradiso et al., 2020 [
      • Paradiso A.V.
      • De Summa S.
      • Silvestris N.
      • Tommasi S.
      • Tufaro A.
      • De Palma G.
      • et al.
      COVID-19 screening and monitoring of asymptomatic health workers with a rapid serological test.
      ]
      Bari/Italy60.647.9 (8.6)606PrevalenceConvenience samplingNR26 March–17 AprilHospitalsPreprint service
      Fujita et al., 2020 [
      • Fujita K.
      • Kada S.
      • Kanai O.
      • Hata H.
      • Odagaki T.
      • Satoh-Asahara N.
      • et al.
      Quantitative SARS-CoV-2 antibody screening of healthcare workers in the southern part of Kyoto city during the COVID-19 peri-pandemic period.
      ]
      Kyoto/Japan64.120–29 years, 32.6%; 30–39 years, 31.5%; 40–49 years, 22.8%; >49 years, 13%92Cross-sectionalConvenience samplingNR10–20 AprilHospitalsPreprint service
      Sikora et al., 2020 [
      • Sikora K.
      • Barwick I.
      • Hamilton C.
      Serological prevalence of antibodies to SARS CoV-2 amongst cancer centre staff.
      ]
      Reading, Newport, Liverpool, Bedlington/UK50.343 (NR)161PrevalenceConvenience samplingNR14–24 AprilCancer centersPreprint service
      Rudberg et al., 2020 [
      • Rudberg A.S.
      • Havervall S.
      • Manberg A.
      • Falk A.J.
      • Aguilera K.
      • Ng H.
      • et al.
      SARS-CoV-2 exposure, symptoms and seroprevalence in health care workers.
      ]
      Stockholm/Sweden8544 (12)410Cross-sectionalConvenience sampling10014 April–8 MayHospitalsPreprint service
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      Birmingham/UK75.240.9 (15.6)516Cross-sectionalConvenience sampling93.125 AprilHospitalsPreprint service
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      Tokyo/Japan3520–29 years, 0%; 30–39 years, 9%; 40–49 years, 36%; 50–59 years, 16%; 60–69, 31%; 70–80 years, 7%55PrevalenceConvenience samplingNR21–28 AprilPrimary care facilitiesPreprint service
      NR, not reported; SD, standard deviation.
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      • Wright A.
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      • Olalla J.
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      • Wilson A.C.
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      ] used a convenience sample, and the response rate ranged from 47.7% [
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      • Beukinga I.
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      • Schreiber A.
      • Grammatica A.
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      • Rudberg A.S.
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      • Poulikakos D.
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      ,
      • Steensels D.
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      • Nuyens D.
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      • Anastasiou O.E.
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      • et al.
      SARS-CoV-2-specific antibody detection in healthcare workers in Germany with direct contact to COVID-19 patients.
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      Low seroprevalence of SARS-CoV-2 infection among healthcare workers of the largest children hospital in Milan during the pandemic wave.
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      SARS-CoV-2-specific antibody detection in healthcare workers in a UK maternity hospital: correlation with SARS-CoV-2 RT-PCR results.
      ,
      • Stubblefield W.B.
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      Seroprevalence of SARS-CoV-2 among frontline healthcare personnel during the first month of caring for COVID-19 patients – Nashville, Tennessee.
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      ,
      • Kassem A.M.
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      • Fouad R.
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      SARS-CoV-2 infection among healthcare workers of a gastroenterological service in a tertiary care facility.
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      ,
      • Hains D.S.
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      Asymptomatic seroconversion of immunoglobulins to SARS-CoV-2 in a pediatric dialysis unit.
      ,
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      Lower detection rates of SARS-COV2 antibodies in cancer patients versus health care workers after symptomatic COVID-19.
      ,
      • Behrens G.
      • Cossmann A.
      • Stankov M.V.
      • Witte T.
      • Ernst D.
      • Happle C.
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      Perceived versus proven SARS-CoV-2-specific immune responses in health-care professionals.
      ,
      • Brandstetter S.
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      ].
      Validity assessment (sensitivity and specificity) for antibody tests used in the included studies according to the manufacturers' data are presented in Table S2 (see online supplementary material). Sensitivity ranged from 50% to 100%, and specificity ranged from 80.5% to 100%.

      Quality assessment

      Quality assessments of prevalence studies, cross-sectional studies and cohort studies are shown in Tables S3, S4 and S5, respectively (see online supplementary material). Quality was moderate in 37 studies, good in 10 studies and poor in two studies. Regarding prevalence studies, 16 were at moderate risk of bias, three were at low risk and one was at high risk. Moreover, 20 cross-sectional studies were at moderate risk of bias, five were at low risk and one was at high risk. Two cohort studies were at low risk of bias and one was at moderate risk.

      Meta-analysis of the seroprevalence

      A random effects model was applied to estimate pooled prevalence as heterogeneity between results was very high (I2=99.34, P-value for Hedges Q statistic <0.001). The estimated overall seroprevalence of SARS-CoV-2 antibodies among HCWs was 8.7% (95% CI 6.7–10.9%) (Figure 2). Seroprevalence among studies ranged from 0% to 45.3%.
      Figure 2
      Figure 2Forest plot of the seroprevalence of severe acute respiratory syndrome coronavirus-2 antibodies with corresponding 95% confidence intervals. The size of the black boxes is positively proportional to the weight assigned to studies, and horizontal lines represent the 95% confidence intervals according to random effects analysis.

      Subgroup and meta-regression analysis

      According to subgroup analysis, seroprevalence of SARS-CoV-2 antibodies was higher for studies of poor quality (11.6%, 95% CI 0.7–32.7%) compared with studies of moderate quality (8.8%, 95% CI 6.0–12%) and good quality (7.9%, 95% CI 4.1–12.8%). Moreover, seroprevalence was higher for studies that had been published in journals (9%, 95% CI 6.7–11.6%) compared with preprint services (7.7%, 95% CI 3.4–13.4%). Seroprevalence was higher in studies conducted in North America (12.7%, 95% CI 8.6–17.5%) compared with those conducted in Europe (8.5%, 95% CI 5.8–11.6%), Africa (8.2%, 95% CI 0.8–22.3%) and Asia (4%, 95% CI 1.8–7.1%). Meta-regression showed that increased sensitivity of antibody tests was associated with increased seroprevalence (coefficient = 0.004, 95% CI 0.0001–0.009; P=0.038). Moreover, seroprevalence was independent of sample size (P=0.65) and specificity (P=0.20).

      Sensitivity analysis

      Leave-one-out sensitivity analysis showed that no single study had a disproportionate effect on overall seroprevalence, which varied between 8.2% (95% CI 6.2–10.3%) with Hoolihan et al. [
      • Houlihan C.F.
      • Vora N.
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      • Lewer D.
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      ] excluded and 9.0% (95% CI 6.9–11.2%) with Nakamura et al. [
      • Nakamura A.
      • Sato R.
      • Ando S.
      • Oana N.
      • Nozaki E.
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      Seroprevalence of antibodies to SARS-CoV-2 in healthcare workers in non-epidemic region: a hospital report in Iwate Prefecture, Japan.
      ] excluded (Figure S1, see online supplementary material).

      Publication bias

      Egger's test (P=0.0001) and the asymmetric shape of the funnel plot (Figure S2, see online supplementary material) implied potential publication bias.

      Factors associated with SARS-CoV-2 antibody positivity

      Twenty-seven studies [
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