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      Multi-center nationwide comparison of seven serology assays reveals a SARS-CoV-2 non-responding seronegative subpopulation

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          Abstract

          Background

          An Israeli national taskforce performed a multi-center clinical and analytical validation of seven serology assays to determine their utility and limitations for SARS-CoV-2 diagnosis.

          Methods

          Serology assays from Roche, Abbott, Diasorin, BioMerieux, Beckman-Coulter, Siemens, and Mt.-Sinai ELISA were included. Negative samples from 2391 individuals representative of the Israeli population, and 698 SARS-CoV-2 PCR positive patients, collected between March and May 2020, were analyzed

          Findings

          Immunoassays sensitivities between 81.5%-89.4% and specificities between 97.7%-100% resulted in a profound impact on the expected Positive Predictive Value (PPV) in low (<15%) prevalence scenarios. No meaningful increase was detected in the false positive rate in children compared to adults. A positive correlation between disease severity and antibody titers, and no decrease in antibody titers in the first 8 weeks after PCR positivity was observed. We identified a subgroup of symptomatic SARS-CoV-2 positive patients (~5% of patients), who remained seronegative across a wide range of antigens, isotypes, and technologies.

          Interpretation

          wThe commercially available automated immunoassays exhibit significant differences in performance and expected PPV in low prevalence scenarios. The low false-positivity rate in under 20′s suggests that cross-reactive immunity from previous CoV strains is unlikely to explain the milder disease course in children. Finding no decrease in antibody titers in the first 8 weeks is in contrast to some reports of short half-life for SARS-CoV-2 antibodies. The ~5% who were seronegative non-responders, using multiple assays in a population-wide manner, represents the proportion of patients that may be at risk for re-infection.

          Funding

          Israel Ministry of Health.

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          Most cited references33

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          Clinical and immunological assessment of asymptomatic SARS-CoV-2 infections

          Quan-Xin Long, Xiao-Jun Tang, Qiu-Lin Shi … (2020)
          The clinical features and immune responses of asymptomatic individuals infected with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) have not been well described. We studied 37 asymptomatic individuals in the Wanzhou District who were diagnosed with RT-PCR-confirmed SARS-CoV-2 infections but without any relevant clinical symptoms in the preceding 14 d and during hospitalization. Asymptomatic individuals were admitted to the government-designated Wanzhou People's Hospital for centralized isolation in accordance with policy1. The median duration of viral shedding in the asymptomatic group was 19 d (interquartile range (IQR), 15-26 d). The asymptomatic group had a significantly longer duration of viral shedding than the symptomatic group (log-rank P = 0.028). The virus-specific IgG levels in the asymptomatic group (median S/CO, 3.4; IQR, 1.6-10.7) were significantly lower (P = 0.005) relative to the symptomatic group (median S/CO, 20.5; IQR, 5.8-38.2) in the acute phase. Of asymptomatic individuals, 93.3% (28/30) and 81.1% (30/37) had reduction in IgG and neutralizing antibody levels, respectively, during the early convalescent phase, as compared to 96.8% (30/31) and 62.2% (23/37) of symptomatic patients. Forty percent of asymptomatic individuals became seronegative and 12.9% of the symptomatic group became negative for IgG in the early convalescent phase. In addition, asymptomatic individuals exhibited lower levels of 18 pro- and anti-inflammatory cytokines. These data suggest that asymptomatic individuals had a weaker immune response to SARS-CoV-2 infection. The reduction in IgG and neutralizing antibody levels in the early convalescent phase might have implications for immunity strategy and serological surveys.
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            Antibody responses to SARS-CoV-2 in patients with COVID-19

            Quan-Xin Long, Bai-Zhong Liu, Hai-Jun Deng … (2020)
            We report acute antibody responses to SARS-CoV-2 in 285 patients with COVID-19. Within 19 days after symptom onset, 100% of patients tested positive for antiviral immunoglobulin-G (IgG). Seroconversion for IgG and IgM occurred simultaneously or sequentially. Both IgG and IgM titers plateaued within 6 days after seroconversion. Serological testing may be helpful for the diagnosis of suspected patients with negative RT-PCR results and for the identification of asymptomatic infections.
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              SARS-CoV-2 Infection in Children

              Xiaoxia Lu, Liqiong Zhang, Hui Du … (2020)
              To the Editor: As of March 10, 2020, the 2019 novel coronavirus (SARS-CoV-2) has been responsible for more than 110,000 infections and 4000 deaths worldwide, but data regarding the epidemiologic characteristics and clinical features of infected children are limited. 1-3 A recent review of 72,314 cases by the Chinese Center for Disease Control and Prevention showed that less than 1% of the cases were in children younger than 10 years of age. 2 In order to determine the spectrum of disease in children, we evaluated children infected with SARS-CoV-2 and treated at the Wuhan Children’s Hospital, the only center assigned by the central government for treating infected children under 16 years of age in Wuhan. Both symptomatic and asymptomatic children with known contact with persons having confirmed or suspected SARS-CoV-2 infection were evaluated. Nasopharyngeal or throat swabs were obtained for detection of SARS-CoV-2 RNA by established methods. 4 The clinical outcomes were monitored up to March 8, 2020. Of the 1391 children assessed and tested from January 28 through February 26, 2020, a total of 171 (12.3%) were confirmed to have SARS-CoV-2 infection. Demographic data and clinical features are summarized in Table 1. (Details of the laboratory and radiologic findings are provided in the Supplementary Appendix, available with the full text of this letter at NEJM.org.) The median age of the infected children was 6.7 years. Fever was present in 41.5% of the children at any time during the illness. Other common signs and symptoms included cough and pharyngeal erythema. A total of 27 patients (15.8%) did not have any symptoms of infection or radiologic features of pneumonia. A total of 12 patients had radiologic features of pneumonia but did not have any symptoms of infection. During the course of hospitalization, 3 patients required intensive care support and invasive mechanical ventilation; all had coexisting conditions (hydronephrosis, leukemia [for which the patient was receiving maintenance chemotherapy], and intussusception). Lymphopenia (lymphocyte count, <1.2×109 per liter) was present in 6 patients (3.5%). The most common radiologic finding was bilateral ground-glass opacity (32.7%). As of March 8, 2020, there was one death. A 10-month-old child with intussusception had multiorgan failure and died 4 weeks after admission. A total of 21 patients were in stable condition in the general wards, and 149 have been discharged from the hospital. This report describes a spectrum of illness from SARS-CoV-2 infection in children. In contrast with infected adults, most infected children appear to have a milder clinical course. Asymptomatic infections were not uncommon. 2 Determination of the transmission potential of these asymptomatic patients is important for guiding the development of measures to control the ongoing pandemic.
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                Author and article information

                Journal
                Journal ID (nlm-ta): EClinicalMedicine
                Journal ID (iso-abbrev): EClinicalMedicine
                Title: EClinicalMedicine
                Publisher: The Authors. Published by Elsevier Ltd.
                ISSN (Electronic): 2589-5370
                Publication date PMC-release: 19 November 2020
                Publication date (Electronic): 19 November 2020
                Electronic Location Identifier: 100651
                Affiliations
                [a ]Canopy Immuno-Therapeutics and MeMed Diagnostics, Tirat Carmel, Israel
                [b ]The Gertner Institute of Epidemiology and Health Policy Research, Sheba Medical Center, Tel Hashomer, Israel
                [c ]Laboratory of Clinical Virology Clalit HMO and Soroka Medical Center, Beer-Sheva, Israel
                [d ]Laboratory Division, Maccabi HMO, Rehovot, Israel
                [e ]Laboratory Division, Meuhedet HMO, Rehovot, Israel
                [f ]Laboratory Division, Leumit HMO, Or-Yehuda, Israel
                [g ]Directorate of Defence Research and Development, Ministry of Defense, Tel Aviv, Israel
                [h ]Central Virology Laboratory, Ministry of Health and Sheba Medical Center, Tel-Hashomer, Israel
                [i ]Magen David National Blood Services, Tel Hashomer, Israel
                [j ]Israel Center for Disease Control, Ministry of Health, Chaim Sheba Medical center, Tel-Hashomer, Israel
                [k ]Sackler Faculty of Medicine, Tel-Aviv University, Israel
                [l ]Ministry of Health, Jerusalem, Israel
                [m ]Asaaf Harofeh Medical Center, Be'er Ya'akov, Israel
                [n ]Sheba Medical Center. Tel Hashomer, Israel
                [o ]The Technion Institute of Technology, Haifa, Israel
                [p ]Dept. of Biomolecular Sciences, Weizmann Institute of Science, Rehovot, Israel
                Author notes
                [* ]Corresponding author.
                [1]

                These authors contributed equally to this work.

                [2]

                These authors contributed equally to this work.

                Article
                Publisher Item ID: S2589-5370(20)30395-3 Publisher ID: 100651
                DOI: 10.1016/j.eclinm.2020.100651
                PMC ID: 7676374
                PubMed ID: 33235985
                SO-VID: 4e4dcf2a-4f90-4255-9653-1196722a8850
                Copyright © © 2020 The Authors
                License:

                Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.

                History
                Date received : 30 September 2020
                Date revision received : 3 November 2020
                Date accepted : 5 November 2020
                Categories
                Subject: Article

                Keywords: covid-19,serology,sars-cov-2,antibodies,validation study,seronegative subpopulation,igg
                Data availability:
                Keywords: covid-19, serology, sars-cov-2, antibodies, validation study, seronegative subpopulation, igg

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