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Table 1.  Demographic Information for 40 329 Health Care Personnel Voluntarily Tested for COVID-19 IgG Antibodies in the Greater NYC Areaa,b,c
Demographic Information for 40 329 Health Care Personnel Voluntarily Tested for COVID-19 IgG Antibodies in the Greater NYC Areaa,b,c
Table 2.  Occupational Measures for 40 329 Essential Health Care Personnel Voluntarily Tested for COVID-19 IgG Antibodies in the Greater NYC Areaa
Occupational Measures for 40 329 Essential Health Care Personnel Voluntarily Tested for COVID-19 IgG Antibodies in the Greater NYC Areaa
1.
Richardson  S, Hirsch  JS, Narasimhan  M,  et al; Northwell COVID-19 Research Consortium.  Presenting characteristics, comorbidities, and outcomes among 5700 patients hospitalized with COVID-19 in the New York City Area.   JAMA. 2020;323(20):2052-2059. doi:10.1001/jama.2020.6775PubMedGoogle ScholarCrossref
2.
Shanafelt  T, Ripp  J, Trockel  M.  Understanding and addressing sources of anxiety among health care professionals during the COVID-19 pandemic.   JAMA. 2020;323(21):2133-2134. doi:10.1001/jama.2020.5893PubMedGoogle ScholarCrossref
3.
Association of Public Health Laboratories, Council of State and Territorial Epidemiologists. Public Health Considerations: Serologic Testing for COVID-19. Version 1. Published May 7, 2020. Accessed June 1, 2020. https://www.aphl.org/programs/preparedness/crisis-management/documents/serologic-Testing-for-COVID-19.pdf
4.
Rosenberg  ES, Tesoriero  JM, Rosenthal  EM,  et al.  Cumulative incidence and diagnosis of SARS-CoV-2 infection in New York.   Ann Epidemiol. Published online June 17, 2020. doi:10.1001/jama.2020.4326PubMedGoogle Scholar
5.
Sood  N, Simon  P, Ebner  P,  et al.  Seroprevalence of SARS-CoV-2-specific antibodies among adults in Los Angeles County, California, on April 10-11, 2020.   JAMA. 2020;323(23):2425-2427. doi:10.1001/jama.2020.8279PubMedGoogle ScholarCrossref
6.
Steensels  D, Oris  E, Coninx  L,  et al.  Hospital-wide SARS-CoV-2 antibody screening in 3056 staff in a tertiary center in Belgium.   JAMA. 2020;324(2):195-197. doi:10.1001/jama.2020.11160PubMedGoogle ScholarCrossref
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    4 Comments for this article
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    Seropositivity After Infection
    Victor Soriano, MD | Private Practice
    93.5% of patients with PCR-confirmed infection were positive for antibodies I think that's the main conclusion of this study and the one that should be highlighted the most.
    CONFLICT OF INTEREST: None Reported
    Protection of Healthcare Personnel Against COVID-19
    Michael McAleer, PhD(Econometrics),Queen's | Asia University, Taiwan
    The results of this study would have been even more meaningful and robust with:

    (1) broader representation of males and of races/ethnicities;

    (2) proportional representation of physicians to nurses;

    (3) distinguishing between male-female nurses and male-female physicians;

    (4) duration between prior positive PCR tests and subsequent PCR positivity and seropositivity.

    Robust findings from voluntary participation is essential for healthcare personnel to be safe and healthy, as well as everyone with whom they come into close personal contact, who need their protection the most.
    CONFLICT OF INTEREST: None Reported
    Duration of Antibody positivity?--eagerly await follow up data
    Liz Jenny-Avital, MD | Jacobi Medical Center; Bronx NY
    Ongoing study of well characterized cohorts, such as the Northwell Health System employees, can provide great insights. It will be of interest to learn how long antibody persists--and if exposure, based on antibody, is protective during our ongoing low level epidemic in the greater NY area.
    CONFLICT OF INTEREST: None Reported
    Dominant Cross-Reactivity of SARS-CoV-2 Nucleocapsid Protein
    Yang Xu, MD, PhD | Shanghai University of Medicine and Health Sciences
    To The Editor:

    Serological testing is a key investigative tool in the COVID-19 epidemic and can locate an infected family or school cluster, especially patients with mild illness. Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) serological testing may assist diagnose suspected patients with negative polymerase chain reaction (PCR) results and those with mild or asymptomatic infections (1). This will allow a more accurate determination of the percentage of infected people.

    In the study by Moscola and colleagues (2), a seropositive rate of 13.7% (5523 of 40329 samples) was performed in 7 different assays with 3 assays using
    a nucleocapsid protein as an antigen [See Supplemental Content, eTable. Assays Used in the Study of Seroprevalence to SARS-CoV-2 Antibodies in Health Care Personnel in the New York City Area]. However, negative control samples from seasonal “common cold” patients were not surveyed using the immunoassay, which might affect the seroprevalence in the population. Four seasonal “common cold” human coronaviruses, 229E, HKU1, NL63, and OC43, are continuously circulating among the global population for about 5% of acute respiratory tract infections.

    SARS-CoV-2 and seasonal “common cold” human coronaviruses patients have cross-reactivity of SARS-CoV-2 T cell epitopes. Mateus and colleagues (3) revealed that memory CD4+ T cells recognizing four common cold coronaviruses can exhibit substantial cross-reactivity to the homologous epitope in SARS-CoV-2. Grifoni and colleagues (4) analyzed donors who were not exposed to COVID-19. About 50% SARS-CoV-2 non-spike-specific CD4+ T cell responses in COVID-19 cases were discovered among non-contact donors. It was recognized that non-contact donors have cross-reactivity to SARS-CoV-2 non-spike peptide.

    SARS-CoV-2 patients have cross-reactivity of nucleocapsid protein of SARS-CoV. Long and colleagues (1) showed samples from SARS-CoV-2 and SARS-CoV patients have cross-reactivity of spike receptor-binding domain (RBD) and nucleocapsid protein. Lv and colleagues (5) described samples of patients with COVID-19 that showed significant cross-reactivity with SARS-CoV nucleocapsid protein. The author also found samples from patients with severe acute respiratory syndrome (SARS) that could significantly cross-react with SARS-CoV-2 spike RBD and nucleocapsid protein (5).

    Therefore, the cross-reactivity of SARS-CoV-2 antibody testing may affect seroprevalence. The answers to these questions need to be addressed earnestly in public health, because it might have a problem for the false positive rate of serological testing. For example, the false positive rate will be seen in population with seasonal “common cold” human coronaviruses infections that might affect accurate statistics regarding the incidence of COVID-19, which might influence public health decisions. The authors should address the limitation of the three testing kits which are designed to detect IgG antibodies to the nucleocapsid protein of SARS-CoV-2 in their study.

    References

    1. Long Q, et al. Antibody responses to SARS-CoV-2 in patients with COVID-19. Nat. Med. 2020. 26: 845-848.
    2. Moscola J, et al. Prevalence of SARS-CoV-2 antibodies in health care personnel in the New York City area. JAMA 2020. doi:10.1001/jama.2020.14765.
    3. Mateus J, et al. Selective and cross-reactive SARS-CoV-2 T cell epitopes in unexposed humans. Science 2020. doi: 10.1126/science.abd3871.
    4. Grifoni A, et al. Cell 2020; 181:1489–1501.
    5. Lv H, et al. Cell Rep. 2020 31: 107725. doi: 10.1016/j.celrep.2020.107725.
    CONFLICT OF INTEREST: None Reported
    READ MORE
    Research Letter
    August 6, 2020

    Prevalence of SARS-CoV-2 Antibodies in Health Care Personnel in the New York City Area

    Author Affiliations
    • 1Northwell Health, New Hyde Park, New York
    • 2Feinstein Institutes for Medical Research, Northwell Health, Manhasset, New York
    • 3Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Northwell Health, Hempstead, New York
    • 4Northwell Health Laboratories, Northwell Health, Lake Success, New York
    JAMA. 2020;324(9):893-895. doi:10.1001/jama.2020.14765

    The greater New York City (NYC) area, including the 5 boroughs and surrounding counties, has a high incidence of coronavirus disease 2019 (COVID-19),1 and health care personnel (HCP) working there have a high exposure risk. HCP have expressed concerns about access to testing so that infection spread to patients, other HCP, and their families can be minimized.2 The Northwell Health System, the largest in New York State, sought to address this concern by offering voluntary antibody testing to all HCP. We investigated the prevalence of antibodies against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) among HCP and associations with demographics, primary work location and type, and suspicion of virus exposure.

    Methods

    All Northwell HCP (employees) were provided with personal protective equipment from March 7, 2020, onward. SARS-CoV-2 testing by reverse transcriptase–polymerase chain reaction (PCR) began March 7, 2020, and was available for any HCP who had COVID-19–like symptoms or suspected exposure. From April 20, 2020, to June 23, 2020, all Northwell HCP were offered free, voluntary antibody testing, regardless of symptoms, at 52 sites in the greater NYC area. HCP missing all identifying data were excluded. Testing was for qualitative IgG or total immunoreactivity to SARS-CoV-2.3 Seven different assays were used (eTable in the Supplement); Northwell Health Laboratories validated all testing.

    The main outcome was seroprevalence. Seroprevalence with 95% confidence interval was calculated by the exact binomial technique. HCP reported demographics, primary work location, job function, direct patient care, work on a COVID or non-COVID unit, and their level of suspicion of virus exposure: “Do you believe you were infected with COVID-19?” (range, 1-9; 1 = no; 9 = yes definitely; 7-9 = high suspicion). Associations among seroprevalence and these variables was assessed using Poisson logistic regression. All eligible persons were included in all analyses by creating a missingness subcategory for each variable. R version 4.0.1 (R Foundation for Statistical Computing) was used for analyses. P < .05 (2-sided) defined statistical significance. The Northwell Health institutional review board approved this research; all participants provided electronic informed consent.

    Results

    All Northwell HCP (n = 70 812) were invited: 46 117 (65.1%) were tested as of June 23, 2020. The final consented sample of 40 329 (56%) (median age, 42 [interquartile range, 31.5-54.5] years) included 73.7% women, 16.0% Black, 0.8% multiracial, and 14.0% Hispanic HCP (Table 1) and 28.4% nurses and 9.3% physicians (Table 2).

    Overall, 5523 of 40 329 (13.7% [95% CI, 13.4%-14.0%]) HCP were seropositive. Of 6078 with previous PCR testing, 2186 (34.8%) were PCR positive. Of these PCR-positive HCP, 2044 (93.5%) were also seropositive, leaving 142 (6.5%) with negative antibody test results. Of the 3892 PCR-negative HCP, 3490 (89.7%) were also seronegative. Of 34 251 with no PCR testing, 3077 (9.0%) were seropositive (Table 2).

    Missing data ranged from 0% to 15.4%. Working in COVID-19 units or in intensive care units were each associated with seroprevalence in bivariate analyses but not in multivariable analyses. In a fully adjusted model, a previous positive PCR test result (relative risk, 1.52 [95% CI, 1.44-1.60]; P < .001) and reported high suspicion of virus exposure (relative risk, 1.23 [95% CI, 1.18-1.28]; P < .001) were associated with seroprevalence (Table 2).

    Discussion

    A 13.7% prevalence of SARS-CoV-2 antibodies in this large cohort study of HCP in the greater NYC area was similar to that among adults randomly tested in New York State (14.0%)4 but higher than among adults in Los Angeles (4.1%).5 HCP in a single hospital in Belgium had lower seroprevalence (6.4%), which was significantly associated only with household contact.6 In this study, high levels of HCP-reported suspicion of virus exposure and prior positive PCR testing results were most strongly associated with seropositivity.

    Study limitations include voluntary testing, with only 56% of HCP participating; restriction to the greater NYC area; 7 different assays with variable sensitivity and specificity used; and time between PCR and antibody testing unknown and possibly too short to detect antibody response. Only HCP-reported suspicion of overall exposure was recorded, so distinguishing among community-, home-, and health care–acquired exposures was not possible.

    Providing HCP with data about their SARS-CoV-2 virus exposure is important so they can protect themselves, their patients, their colleagues, and their families. High levels of HCP-reported suspicion of virus exposure may be useful as an indication for SARS-CoV-2 testing.

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

    Corresponding Author: Karina W. Davidson, PhD, MASc, Northwell Health, 130 E 59th St, Ste 14C, New York, NY 10022 (kdavidson2@northwell.edu).

    Accepted for Publication: July 23, 2020.

    Published Online: August 6, 2020. doi:10.1001/jama.2020.14765

    Author Contributions: Drs Davidson and Chang 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: All authors.

    Acquisition, analysis, or interpretation of data: Sembajwe, Jarrett, Farber, Chang, Davidson.

    Drafting of the manuscript: Moscola, Sembajwe, Farber, Chang, Davidson.

    Critical revision of the manuscript for important intellectual content: Sembajwe, Jarrett, McGinn, Davidson.

    Statistical analysis: Sembajwe.

    Obtained funding: Davidson.

    Administrative, technical, or material support: Moscola, Jarrett, Farber, Chang, McGinn, Davidson.

    Supervision: McGinn, Davidson.

    Conflict of Interest Disclosures: None reported.

    Funding/Support: This work was supported by grants R24AG064191 from the National Institute on Aging and R01LM012836 from the National Library of Medicine.

    Role of the Funder/Sponsor: The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; or decision to submit the manuscript for publication.

    Disclaimer: The views expressed in this article are those of the authors and do not represent the views of the National Institutes of Health, the US Department of Health and Human Services, or any other government entity. Dr Davidson is a member of the US Preventive Services Task Force (USPSTF). This article does not represent the views and policies of the USPSTF.

    Additional Contributions: We thank the members of the Northwell Health COVID-19 Research Consortium who contributed to this study: Lance B. Becker, MD (North Shore University Hospital/Long Island Jewish Emergency Medical Department, Northwell Health); Dwayne A. Breining, MD, Jacqueline Moline, MD, MSc (Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Northwell Health); Mark J. Butler, PhD, Jennifer Cookingham, MHA, Andrew J. Dominello, BA, Louise Falzon, BA, PGDipInf, Cirrus Foroughi, PhD, Jennifer C. Johnson, MS, MA, Jazmin N. Mogavero, MA, Rachel Monane, BBA, Frank Vicari, BS (Feinstein Institutes for Medical Research, Northwell Health); James M. Crawford, MD, PhD, Sharon S. Fox, BS, Stefan Juretschko, PhD, D(ABMM), Cheryl B. Schleicher, MS-HCA, BA (Northwell Health Laboratories, Northwell Health); Christopher J. Hutchins, Kristen M. McPhillips, MBA, PMP, and Abraham Saraya, MD, MSc (Northwell Health). None of these individuals received any compensation for their contributions.

    References
    1.
    Richardson  S, Hirsch  JS, Narasimhan  M,  et al; Northwell COVID-19 Research Consortium.  Presenting characteristics, comorbidities, and outcomes among 5700 patients hospitalized with COVID-19 in the New York City Area.   JAMA. 2020;323(20):2052-2059. doi:10.1001/jama.2020.6775PubMedGoogle ScholarCrossref
    2.
    Shanafelt  T, Ripp  J, Trockel  M.  Understanding and addressing sources of anxiety among health care professionals during the COVID-19 pandemic.   JAMA. 2020;323(21):2133-2134. doi:10.1001/jama.2020.5893PubMedGoogle ScholarCrossref
    3.
    Association of Public Health Laboratories, Council of State and Territorial Epidemiologists. Public Health Considerations: Serologic Testing for COVID-19. Version 1. Published May 7, 2020. Accessed June 1, 2020. https://www.aphl.org/programs/preparedness/crisis-management/documents/serologic-Testing-for-COVID-19.pdf
    4.
    Rosenberg  ES, Tesoriero  JM, Rosenthal  EM,  et al.  Cumulative incidence and diagnosis of SARS-CoV-2 infection in New York.   Ann Epidemiol. Published online June 17, 2020. doi:10.1001/jama.2020.4326PubMedGoogle Scholar
    5.
    Sood  N, Simon  P, Ebner  P,  et al.  Seroprevalence of SARS-CoV-2-specific antibodies among adults in Los Angeles County, California, on April 10-11, 2020.   JAMA. 2020;323(23):2425-2427. doi:10.1001/jama.2020.8279PubMedGoogle ScholarCrossref
    6.
    Steensels  D, Oris  E, Coninx  L,  et al.  Hospital-wide SARS-CoV-2 antibody screening in 3056 staff in a tertiary center in Belgium.   JAMA. 2020;324(2):195-197. doi:10.1001/jama.2020.11160PubMedGoogle ScholarCrossref
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