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Figure 1.  Epidemic Timeline of Patients With COVID-19 Admitted to Hospital East-Limburg, Belgium, 2020
Epidemic Timeline of Patients With COVID-19 Admitted to Hospital East-Limburg, Belgium, 2020

The epidemic curve is shown as the number of patients with coronavirus disease 2019 (COVID-19) admitted at the institution each day. The first case was detected March 13. Serosurvey of staff was initiated from April 22, 2020, to April 30, 2020. Details of the infection prevention measures are depicted below the curve. FFP indicates filtering facepiece; RT-PCR, reverse transcriptase–polymerase chain reaction; TAT, turnaround time.

Figure 2.  Exposure and Symptomatology Predictors of SARS-CoV-2 Antibodies Among Staff, Hospital East-Limburg, Belgium, 2020
Exposure and Symptomatology Predictors of SARS-CoV-2 Antibodies Among Staff, Hospital East-Limburg, Belgium, 2020

A, 95% CIs of the odds ratios based on bivariable logistic regression analyses. B, 95% CIs of the odds ratios based on multivariable (with all symptoms included in the model) logistic regression analyses. SARS-CoV-2 indicates severe acute respiratory syndrome coronavirus 2.

aFever could be either subjective or confirmed.

1.
Epidemiological situation of the coronavirus in Belgium: daily report of national and international situation. Sciensano. Accessed May 6, 2020. https://covid-19.sciensano.be/nl/covid-19-epidemiologische-situatie
2.
Van Elslande  J, Houben  E, Depypere  M,  et al.  Diagnostic performance of 7 rapid IgG/IgM antibody tests and the Euroimmun IgA/IgG ELISA in COVID-19 patients.   Clin Microbiol Infect. Published online May 28, 2020. doi:10.1016/j.cmi.2020.05.023PubMedGoogle Scholar
3.
Bedford  J, Enria  D, Giesecke  J,  et al; WHO Strategic and Technical Advisory Group for Infectious Hazards.  COVID-19: towards controlling of a pandemic.   Lancet. 2020;395(10229):1015-1018. doi:10.1016/S0140-6736(20)30673-5PubMedGoogle ScholarCrossref
4.
Abbasi  J.  The promise and peril of antibody testing for COVID-19.   JAMA. Published online April 17, 2020. doi:10.1001/jama.2020.6170PubMedGoogle Scholar
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    4 Comments for this article
    EXPAND ALL
    PPE
    John Raines, MD | Retired
    I don't see comments in the article about PPE availability in Belgium. This would be of interest in trying to assess the import of this to other locales.
    CONFLICT OF INTEREST: None Reported
    Symptomatic staff not tested
    Bart Rutteman, M.D. | Hospital
    The seropositivity here presented in hospital staff is more or less simililar to that of the overall population in Belgium at the same time.

    The authors conclude that this relatively low seropositivity could be due to the protective measures that have been implemented.

    However, in the methods they state that staff with active symptoms were not tested. I believe this poses great implications to the conclusions that may be drawn from this study. There is a very high chance of a significantly higher seroprevalency in symptomatic staff. It is likely that the overall seroprevalence in the hospital is
    higher if symptomatic persons would have been tested. It is also likely that there would be a higher proportion of symptomatic staff involved in COVID-19+ patient care.

    Could the authors provide information on the number of staff with symptoms and on their exposure (with or without COVID-19+ patient contact)? Could the symptomatic staff be tested now?
    CONFLICT OF INTEREST: None Reported
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    Reply to Dr. Bart Rutteman
    Deborah Steensels, PharmD, PhD | Ziekenhuis Oost-Limburg, Belgium
    Staff members who were sick at the time of the sampling could not be tested for antibodies, since we could not allow symptomatic staff to enter the hospital for infection prevention. There were only 5 staff members on sick leave due to COVID-19 during the sampling period. Thus, testing was not performed due to quarantine for active COVID-19 infection in only 5 out of the total 1069 not-tested employees (0.5%). When compared with the 197 staff who were tested and had antibodies, this is also a low percentage (5/202, 2.3%). Moreover, even if fewer staff members were included due to active COVID-19, our conclusions would likely not have changed given the maximum incubation time for COVID-19 of 14 days. Testing was performed at the end of April and the first patient was cared for starting March 13 (i.e., >6 weeks have passed). In this time frame, we should have already seen differences in seroprevalence if in-hospital transmission would have occurred.
    CONFLICT OF INTEREST: None Reported
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    Cross-reactivity to seasonal “common cold” and SARS-CoV-2 seroprevalence
    Yang Xv, MD | Chinese Academy of Medical Sciences
    Steensels et al. (1) reported SARS-CoV-2 IgG positive rates were 6.4% in hospital staff and 13.7% in suspected household contacts, respectively. However, negative control samples from seasonal “common cold” were not investigated using the nucleocapsid protein test kit, which could affect the SARS-CoV-2 IgG positive rate in two populations.

    SARS-CoV-2 and SARS-CoV patients have cross-reactivity of spike receptor binding domain (RBD) and non-RBD. Lv et al. (2) reported 15 plasma samples of patients with COVID-19 that showed significant cross-reactivity with SARS-CoV spike non-RBD. However, only 5 of the 15 samples showed convincing cross-reaction with SARS-CoV RBD. The author
    also reported 7 plasma samples from patients with severe acute respiratory syndrome (SARS) that could significantly cross-react with SARS-CoV-2 spike non-RBD and RBD (2).

    SARS-CoV-2 and seasonal “common cold” human coronaviruses patients have cross-reactivity of SARS-CoV-2. Grifoni et al. (3) investigated donors who were not exposed to COVID-19. Approximately 40–60% SARS-CoV-2 non-spike-specific CD4+ T cell responses in COVID-19 cases were detected among non-contact donors. It was determined that non-contact donors have cross-reactivity to SARS-CoV-2 non-spike peptide.

    If the patient shows a non-spike cross-reaction and an anti-spike and nucleocapsid protein combination detection kit is used, it may affect the evaluation of SARS-CoV-2 seroprevalence.

    References
    1. Steensels D, et al. Hospital-wide SARS-CoV-2 antibody screening in 3056 staff in a tertiary center in Belgium. JAMA. 324, 195-197 (2020).
    2. Lv H, et al. Cross-reactive antibody response between SARSCoV-2 and SARS-CoV infections. Cell Rep. 31, 107725 (2020). doi: 10.1016/j.celrep.2020.107725.
    3. Grifoni A, et al. Targets of T cell responses to SARS-CoV-2 coronavirus in humans with COVID-19 disease and unexposed individuals. Cell 181, 1489–1501. (2020).
    CONFLICT OF INTEREST: None Reported
    READ MORE
    Research Letter
    June 15, 2020

    Hospital-Wide SARS-CoV-2 Antibody Screening in 3056 Staff in a Tertiary Center in Belgium

    Author Affiliations
    • 1Ziekenhuis Oost-Limburg, Genk, Belgium
    • 2Université Libre de Bruxelles, Brussels, Belgium
    • 3University Hospitals Leuven, Leuven, Belgium
    • 4Hasselt University, Hasselt, Belgium
    JAMA. 2020;324(2):195-197. doi:10.1001/jama.2020.11160

    Belgium has a high burden of coronavirus disease 2019 (COVID-19), especially the region surrounding the Hospital East-Limburg, a tertiary care center.1 Infection prevention measures were instituted in the hospital beginning March 4, 2020, including testing and contact tracing of all symptomatic patients and staff, changes in hospital operations, and provision of personal protective equipment (PPE). The first case was detected March 13 (Figure 1). We investigated the prevalence of antibodies against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) among hospital staff.

    Methods

    From April 22, 2020, to April 30, 2020, all persons who worked at Hospital East-Limburg (including clinical and nonclinical staff and volunteers) were invited for serologic testing. Staff with active symptoms were quarantined and not tested. A single-lane rapid IgG/IgM lateral flow assay directed to the nucleocapsid protein of SARS-CoV-2 (COVID-19 IgG/IgM Rapid Test Cassette; Multi-G) was used. The manufacturer reported high sensitivity and specificity; external validation found performance for IgG comparable to enzyme-linked immunosorbent assay,2 but the specificity and sensitivity for IgM were only 91.3% and 57.9%. Internal validation of the assay using 90 polymerase chain reaction–confirmed cases and 101 historic biobanked samples found a sensitivity of 92.2% and specificity of 97.0% for IgG. Because of inadequate performance, IgM results were excluded. Demographic characteristics and job title were obtained from human resources records. Staff were asked to complete a survey on exposure risks (patient, coworker, and household contact) and symptoms from March 1 (Figure 2). The seroprevalence 95% confidence interval was calculated by the asymptotic method. χ2 Tests were used to compare proportions, t tests to compare age. Odds ratios and 95% CIs were calculated with bivariable logistic regression to assess demographic and job characteristics associated with seroprevalence and with multivariable logistic regression to assess symptoms independently associated with seroprevalence, with all symptoms included as covariates (Figure 2). Missing data were excluded. A 2-sided P < .05 defined statistical significance. Analyses were performed using RStudio version 0.99.902. This study was approved by the local institutional review board, and written informed consent was obtained.

    Results

    All 4125 staff were invited and 3056 (74%) participated (306 physicians, 1266 nurses, 292 paramedical staff, 555 technical staff, 445 administrative staff, and 192 others, including students and volunteers). At least one-third of those not tested were individuals not at work during the period. Overall, 197 staff (6.4% [95% CI, 5.5%-7.3%]) had IgG antibodies for SARS-CoV-2. Age and sex were not statistically significantly different among staff with or without antibodies (mean age, 39.5 [SD, 13.1] vs 41.3 [SD, 12.4] years; 38/197 [19%] vs 614/2859 [21%] men). Being involved in clinical care, having worked during the lockdown phase, being involved in care for patients with COVID-19, and exposure to COVID-19–positive coworkers were not statistically significantly associated with seroprevalence (Figure 2A). In contrast, having a household contact with suspected or confirmed COVID-19 was associated with antibody positivity (81/593 [13.7%] with household contacts vs 116/2435 [4.8%] without household exposure; P < .001), with an odds ratio of 3.15 (95% CI, 2.33-4.25).

    A high proportion of staff mentioned at least 1 prior symptom (2294/3052 [75%]). Of those with antibodies, 30 of 197 (15%) reported no symptoms. Prior anosmia was associated with the presence of antibodies, with an odds ratio of 7.78 (95% CI, 5.22-11.53), as well as fever and cough (Figure 2B).

    Discussion

    In this hospital-wide screening study for SARS-CoV-2 antibodies among hospital staff, neither being directly involved in clinical care nor working in a COVID-19 unit increased the odds of being seropositive, while having a suspected COVID-19 household contact did. The high availability of PPE, high standards of infection prevention, and polymerase chain reaction screening in symptomatic staff, coupled with contact tracing and quarantine, might explain a relatively low seroprevalence.3

    Limitations of this study include the single-center design and testing of only 74% of staff. Seroconversion may have been missed if testing was too early, especially without IgM results that might reflect more recent infection than IgG.

    Quick screening of large cohorts is important to control the pandemic.4 Hospital-wide antibody screening for SARS-CoV-2 can help monitor transmission dynamics and evaluate infection control policies.

    Section Editor: Jody W. Zylke, MD, Deputy Editor.
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    Article Information

    Accepted for Publication: June 6, 2020.

    Corresponding Author: Deborah Steensels, PharmD, PhD, Department of Laboratory Medicine, Ziekenhuis Oost-Limburg, Schiepse Bos 6, 3600 Genk, Belgium (deborah.steensels@zol.be).

    Published Online: June 15, 2020. doi:10.1001/jama.2020.11160

    Author Contributions: Drs Steensels and Heylen had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

    Concept and design: Steensels, Oris, Nuyens, Heylen.

    Acquisition, analysis, or interpretation of data: Steensels, Oris, Coninx, Delforge, Vermeersch, Heylen.

    Drafting of the manuscript: Steensels, Oris, Nuyens, Heylen.

    Critical revision of the manuscript for important intellectual content: Oris, Coninx, Delforge, Vermeersch, Heylen.

    Statistical analysis: Steensels, Heylen.

    Administrative, technical, or material support: Steensels, Oris, Coninx, Nuyens, Delforge, Vermeersch.

    Supervision: Steensels, Heylen.

    Conflict of Interest Disclosures: None reported.

    Additional Information: We thank the hospital board of directors for their financial and organizational support, and nursing director Kurt Surmont, MSc, RN (Ziekenhuis Oost-Limburg), in particular. We thank Toon Schiemsky, MD, for data extraction and Joris Penders, MD, PhD (both at Ziekenhuis Oost-Limburg), for critical revision of the manuscript. None of these individuals received additional compensation beyond salary.

    References
    1.
    Epidemiological situation of the coronavirus in Belgium: daily report of national and international situation. Sciensano. Accessed May 6, 2020. https://covid-19.sciensano.be/nl/covid-19-epidemiologische-situatie
    2.
    Van Elslande  J, Houben  E, Depypere  M,  et al.  Diagnostic performance of 7 rapid IgG/IgM antibody tests and the Euroimmun IgA/IgG ELISA in COVID-19 patients.   Clin Microbiol Infect. Published online May 28, 2020. doi:10.1016/j.cmi.2020.05.023PubMedGoogle Scholar
    3.
    Bedford  J, Enria  D, Giesecke  J,  et al; WHO Strategic and Technical Advisory Group for Infectious Hazards.  COVID-19: towards controlling of a pandemic.   Lancet. 2020;395(10229):1015-1018. doi:10.1016/S0140-6736(20)30673-5PubMedGoogle ScholarCrossref
    4.
    Abbasi  J.  The promise and peril of antibody testing for COVID-19.   JAMA. Published online April 17, 2020. doi:10.1001/jama.2020.6170PubMedGoogle Scholar
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