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      Multiplex Antibody Analysis of IgM, IgA and IgG to SARS-CoV-2 in Saliva and Serum From Infected Children and Their Close Contacts

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      1 , 2 , , 1 , 1 , 1 , 3 , 1 , 1 , 1 , 4 , 4 , 4 , 5 , 6 , 1 , 1 , 1 , 1 , 1 , 1 , 7 , 7 , 8 , 8 , 9 , 10 , 5 , 11 , 5 , 11 , 5 , 12 , 5 , 12 , 13 , 1 , 3 , 4 , 14 , 15 , 3 , 5 , 16 , 17 , 3 , 4 , 5 , 8 , 9 , 18 , 1 , 2 , 3 , 4 , 5 , 1 , 3 , 5 , 6 , 1 , 2 ,
      Frontiers in Immunology
      Frontiers Media S.A.
      SARS-CoV-2, COVID-19, saliva, antibody - antigen complex, children, plasma, serum, surveillance

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          Abstract

          COVID-19 affects children to a lesser extent than adults but they can still get infected and transmit SARS-CoV-2 to their contacts. Field deployable non-invasive sensitive diagnostic techniques are needed to evaluate the infectivity dynamics of SARS-CoV-2 in pediatric populations and guide public health interventions, particularly if this population is not fully vaccinated. We evaluated the utility of high-throughput Luminex assays to quantify saliva IgM, IgA and IgG antibodies against five SARS-CoV-2 spike (S) and nucleocapsid (N) antigens in a contacts and infectivity longitudinal study in 122 individuals (52 children and 70 adults). We compared saliva versus serum/plasma samples in infected children and adults diagnosed by weekly RT-PCR over 35 days (n=62), and those who consistently tested negative over the same follow up period (n=60), in the Summer of 2020 in Barcelona, Spain. Saliva antibody levels in SARS-CoV-2 RT-PCR positive individuals were significantly higher than in negative individuals and correlated with those measured in sera/plasmas. Asymptomatic infected individuals had higher levels of anti-S IgG than symptomatic individuals, suggesting a protective anti-disease role for antibodies. Higher anti-S IgG and IgM levels in serum/plasma and saliva, respectively, in infected children compared to infected adults could also be related to stronger clinical immunity in them. Among infected children, males had higher levels of saliva IgG to N and RBD than females. Despite overall correlation, individual clustering analysis suggested that responses that may not be detected in blood could be patent in saliva, and vice versa.

          In conclusion, measurement of SARS-CoV-2-specific saliva antibodies should be considered as a complementary non-invasive assay to serum/plasma to determine COVID-19 prevalence and transmission in pediatric populations before and after vaccination campaigns.

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          Most cited references43

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          Temporal profiles of viral load in posterior oropharyngeal saliva samples and serum antibody responses during infection by SARS-CoV-2: an observational cohort study

          Summary Background Coronavirus disease 2019 (COVID-19) causes severe community and nosocomial outbreaks. Comprehensive data for serial respiratory viral load and serum antibody responses from patients infected with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) are not yet available. Nasopharyngeal and throat swabs are usually obtained for serial viral load monitoring of respiratory infections but gathering these specimens can cause discomfort for patients and put health-care workers at risk. We aimed to ascertain the serial respiratory viral load of SARS-CoV-2 in posterior oropharyngeal (deep throat) saliva samples from patients with COVID-19, and serum antibody responses. Methods We did a cohort study at two hospitals in Hong Kong. We included patients with laboratory-confirmed COVID-19. We obtained samples of blood, urine, posterior oropharyngeal saliva, and rectal swabs. Serial viral load was ascertained by reverse transcriptase quantitative PCR (RT-qPCR). Antibody levels against the SARS-CoV-2 internal nucleoprotein (NP) and surface spike protein receptor binding domain (RBD) were measured using EIA. Whole-genome sequencing was done to identify possible mutations arising during infection. Findings Between Jan 22, 2020, and Feb 12, 2020, 30 patients were screened for inclusion, of whom 23 were included (median age 62 years [range 37–75]). The median viral load in posterior oropharyngeal saliva or other respiratory specimens at presentation was 5·2 log10 copies per mL (IQR 4·1–7·0). Salivary viral load was highest during the first week after symptom onset and subsequently declined with time (slope −0·15, 95% CI −0·19 to −0·11; R 2=0·71). In one patient, viral RNA was detected 25 days after symptom onset. Older age was correlated with higher viral load (Spearman's ρ=0·48, 95% CI 0·074–0·75; p=0·020). For 16 patients with serum samples available 14 days or longer after symptom onset, rates of seropositivity were 94% for anti-NP IgG (n=15), 88% for anti-NP IgM (n=14), 100% for anti-RBD IgG (n=16), and 94% for anti-RBD IgM (n=15). Anti-SARS-CoV-2-NP or anti-SARS-CoV-2-RBD IgG levels correlated with virus neutralisation titre (R 2>0·9). No genome mutations were detected on serial samples. Interpretation Posterior oropharyngeal saliva samples are a non-invasive specimen more acceptable to patients and health-care workers. Unlike severe acute respiratory syndrome, patients with COVID-19 had the highest viral load near presentation, which could account for the fast-spreading nature of this epidemic. This finding emphasises the importance of stringent infection control and early use of potent antiviral agents, alone or in combination, for high-risk individuals. Serological assay can complement RT-qPCR for diagnosis. Funding Richard and Carol Yu, May Tam Mak Mei Yin, The Shaw Foundation Hong Kong, Michael Tong, Marina Lee, Government Consultancy Service, and Sanming Project of Medicine.
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            Clinical and immunological assessment of asymptomatic SARS-CoV-2 infections

            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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              IgA dominates the early neutralizing antibody response to SARS-CoV-2

              Early specific antibody responses against SARS-CoV-2 include IgG, IgM, and IgA, but IgA may neutralize virus and control infection to a larger extent.
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                Author and article information

                Contributors
                Journal
                Front Immunol
                Front Immunol
                Front. Immunol.
                Frontiers in Immunology
                Frontiers Media S.A.
                1664-3224
                27 January 2022
                2022
                27 January 2022
                : 13
                : 751705
                Affiliations
                [1] 1 ISGlobal, Hospital Clínic - Universitat de Barcelona , Barcelona, Spain
                [2] 2 Consorcio de Investigación Biomédica en Red (CIBER) de Enfermedades Infecciosas , Madrid, Spain
                [3] 3 Consorcio de Investigación Biomédica en Red de Epidemiología y Salud Pública (CIBERESP) , Madrid, Spain
                [4] 4 Pediatrics Department, Hospital Sant Joan de Déu, Universitat de Barcelona , Esplugues, Spain
                [5] 5 Institut de Recerca Sant Joan de Déu , Esplugues, Spain
                [6] 6 Paediatric Intensive Care Unit, Hospital Sant Joan de Déu, Universitat de Barcelona , Barcelona, Spain
                [7] 7 Biomolecular Screening and Protein Technologies Unit, Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology , Barcelona, Spain
                [8] 8 Fetal Medicine Research Center (Hospital Clínic and Hospital Sant Joan de Déu), Universitat de Barcelona , Barcelona, Spain
                [9] 9 Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS) , Barcelona, Spain
                [10] 10 Universitat Politècnica de Catalunya, BarcelonaTech , Barcelona, Spain
                [11] 11 Fundació Sant Joan de Déu , Barcelona, Spain
                [12] 12 Infectious Diseases Department, Hospital Sant Joan de Déu , Barcelona, Spain
                [13] 13 Biobank Hospital Sant Joan de Déu , Barcelona, Spain
                [14] 14 Centro de Investigação em Saúde de Manhiça (CISM) , Maputo, Mozambique
                [15] 15 Catalan Institution for Research and Advanced Studies (ICREA) , Barcelona, Spain
                [16] 16 Department of Medicine, Universitat Internacional de Catalunya , Barcelona, Spain
                [17] 17 Molecular Microbiology Department, Hospital Sant Joan de Déu , Esplugues, Spain
                [18] 18 Center for Biomedical Research on Rare Diseases (CIBER-ER) , Madrid, Spain
                Author notes

                Edited by: Tomer Hertz, Ben-Gurion University of the Negev, Israel

                Reviewed by: Luminița-Smaranda Iancu, Grigore T. Popa University of Medicine and Pharmacy, Romania; Massimo Pieri, University of Rome Tor Vergata, Italy

                *Correspondence: Carlota Dobaño, Carlota.dobano@ 123456isglobal.org ; Gemma Moncunill, Gemma.moncunill@ 123456isglobal.org

                †These authors share first authorship

                ‡These authors share senior authorship

                This article was submitted to Viral Immunology, a section of the journal Frontiers in Immunology

                Article
                10.3389/fimmu.2022.751705
                8828491
                36238312
                9d38cfb4-f571-4a2a-a334-6027d2c7a5fb
                Copyright © 2022 Dobaño, Alonso, Vidal, Jiménez, Rubio, Santano, Barrios, Pons Tomas, Melé Casas, Hernández García, Girona-Alarcón, Puyol, Baro, Millat-Martínez, Ajanovic, Balanza, Arias, Rodrigo Melero, Carolis, García-Miquel, Bonet-Carné, Claverol, Cubells, Fortuny, Fumadó, Codina, Bassat, Muñoz-Almagro, Fernández de Sevilla, Gratacós, Izquierdo, García-García, Aguilar, Jordan and Moncunill

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 01 August 2021
                : 06 January 2022
                Page count
                Figures: 5, Tables: 1, Equations: 0, References: 43, Pages: 13, Words: 4736
                Categories
                Immunology
                Original Research

                Immunology
                sars-cov-2,covid-19,saliva,antibody - antigen complex,children,plasma,serum,surveillance
                Immunology
                sars-cov-2, covid-19, saliva, antibody - antigen complex, children, plasma, serum, surveillance

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