Delayed production of neutralizing antibodies correlates with fatal COVID-19
Recent studies have provided insights into innate and adaptive immune dynamics in coronavirus disease 2019 (COVID-19). However, the exact features of antibody responses that govern COVID-19 disease outcomes remain unclear. In this study, we analyzed humoral immune responses in 229 patients with asym...
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| Published in | Nature medicine Vol. 27; no. 7; pp. 1178 - 1186 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York
Nature Publishing Group US
01.07.2021
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Recent studies have provided insights into innate and adaptive immune dynamics in coronavirus disease 2019 (COVID-19). However, the exact features of antibody responses that govern COVID-19 disease outcomes remain unclear. In this study, we analyzed humoral immune responses in 229 patients with asymptomatic, mild, moderate and severe COVID-19 over time to probe the nature of antibody responses in disease severity and mortality. We observed a correlation between anti-spike (S) immunoglobulin G (IgG) levels, length of hospitalization and clinical parameters associated with worse clinical progression. Although high anti-S IgG levels correlated with worse disease severity, such correlation was time dependent. Deceased patients did not have higher overall humoral response than discharged patients. However, they mounted a robust, yet delayed, response, measured by anti-S, anti-receptor-binding domain IgG and neutralizing antibody (NAb) levels compared to survivors. Delayed seroconversion kinetics correlated with impaired viral control in deceased patients. Finally, although sera from 85% of patients displayed some neutralization capacity during their disease course, NAb generation before 14 d of disease onset emerged as a key factor for recovery. These data indicate that COVID-19 mortality does not correlate with the cross-sectional antiviral antibody levels per se but, rather, with the delayed kinetics of NAb production.
A longitudinal analysis of humoral immune responses in patients with COVID-19 with varying disease severities reveals that mortality does not correlate with antiviral antibody levels but, instead, with slower seroconversion. |
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| AbstractList | Recent studies have provided insights into innate and adaptive immune dynamics in coronavirus disease 2019 (COVID-19). However, the exact features of antibody responses that govern COVID-19 disease outcomes remain unclear. In this study, we analyzed humoral immune responses in 229 patients with asymptomatic, mild, moderate and severe COVID-19 over time to probe the nature of antibody responses in disease severity and mortality. We observed a correlation between anti-spike (S) immunoglobulin G (IgG) levels, length of hospitalization and clinical parameters associated with worse clinical progression. Although high anti-S IgG levels correlated with worse disease severity, such correlation was time dependent. Deceased patients did not have higher overall humoral response than discharged patients. However, they mounted a robust, yet delayed, response, measured by anti-S, anti-receptor-binding domain IgG and neutralizing antibody (NAb) levels compared to survivors. Delayed seroconversion kinetics correlated with impaired viral control in deceased patients. Finally, although sera from 85% of patients displayed some neutralization capacity during their disease course, NAb generation before 14 d of disease onset emerged as a key factor for recovery. These data indicate that COVID-19 mortality does not correlate with the cross-sectional antiviral antibody levels per se but, rather, with the delayed kinetics of NAb production. Recent studies have provided insights into innate and adaptive immune dynamics in coronavirus disease 2019 (COVID-19). However, the exact features of antibody responses that govern COVID-19 disease outcomes remain unclear. In this study, we analyzed humoral immune responses in 229 patients with asymptomatic, mild, moderate and severe COVID-19 over time to probe the nature of antibody responses in disease severity and mortality. We observed a correlation between anti-spike (S) immunoglobulin G (IgG) levels, length of hospitalization and clinical parameters associated with worse clinical progression. Although high anti-S IgG levels correlated with worse disease severity, such correlation was time dependent. Deceased patients did not have higher overall humoral response than discharged patients. However, they mounted a robust, yet delayed, response, measured by anti-S, anti-receptor-binding domain IgG and neutralizing antibody (NAb) levels compared to survivors. Delayed seroconversion kinetics correlated with impaired viral control in deceased patients. Finally, although sera from 85% of patients displayed some neutralization capacity during their disease course, NAb generation before 14 d of disease onset emerged as a key factor for recovery. These data indicate that COVID-19 mortality does not correlate with the cross-sectional antiviral antibody levels per se but, rather, with the delayed kinetics of NAb production. A longitudinal analysis of humoral immune responses in patients with COVID-19 with varying disease severities reveals that mortality does not correlate with antiviral antibody levels but, instead, with slower seroconversion. Recent studies have provided insights into innate and adaptive immune dynamics in coronavirus disease 2019 (COVID-19). However, the exact features of antibody responses that govern COVID-19 disease outcomes remain unclear. In this study, we analyzed humoral immune responses in 229 patients with asymptomatic, mild, moderate and severe COVID-19 over time to probe the nature of antibody responses in disease severity and mortality. We observed a correlation between anti-spike (S) immunoglobulin G (IgG) levels, length of hospitalization and clinical parameters associated with worse clinical progression. Although high anti-S IgG levels correlated with worse disease severity, such correlation was time dependent. Deceased patients did not have higher overall humoral response than discharged patients. However, they mounted a robust, yet delayed, response, measured by anti-S, anti-receptor-binding domain IgG and neutralizing antibody (NAb) levels compared to survivors. Delayed seroconversion kinetics correlated with impaired viral control in deceased patients. Finally, although sera from 85% of patients displayed some neutralization capacity during their disease course, NAb generation before 14 d of disease onset emerged as a key factor for recovery. These data indicate that COVID-19 mortality does not correlate with the cross-sectional antiviral antibody levels per se but, rather, with the delayed kinetics of NAb production.Recent studies have provided insights into innate and adaptive immune dynamics in coronavirus disease 2019 (COVID-19). However, the exact features of antibody responses that govern COVID-19 disease outcomes remain unclear. In this study, we analyzed humoral immune responses in 229 patients with asymptomatic, mild, moderate and severe COVID-19 over time to probe the nature of antibody responses in disease severity and mortality. We observed a correlation between anti-spike (S) immunoglobulin G (IgG) levels, length of hospitalization and clinical parameters associated with worse clinical progression. Although high anti-S IgG levels correlated with worse disease severity, such correlation was time dependent. Deceased patients did not have higher overall humoral response than discharged patients. However, they mounted a robust, yet delayed, response, measured by anti-S, anti-receptor-binding domain IgG and neutralizing antibody (NAb) levels compared to survivors. Delayed seroconversion kinetics correlated with impaired viral control in deceased patients. Finally, although sera from 85% of patients displayed some neutralization capacity during their disease course, NAb generation before 14 d of disease onset emerged as a key factor for recovery. These data indicate that COVID-19 mortality does not correlate with the cross-sectional antiviral antibody levels per se but, rather, with the delayed kinetics of NAb production. Recent studies have provided insights into innate and adaptive immune dynamics in coronavirus disease 2019 (COVID-19). However, the exact features of antibody responses that govern COVID-19 disease outcomes remain unclear. In this study, we analyzed humoral immune responses in 229 patients with asymptomatic, mild, moderate and severe COVID-19 over time to probe the nature of antibody responses in disease severity and mortality. We observed a correlation between anti-spike (S) immunoglobulin G (IgG) levels, length of hospitalization and clinical parameters associated with worse clinical progression. Although high anti-S IgG levels correlated with worse disease severity, such correlation was time dependent. Deceased patients did not have higher overall humoral response than discharged patients. However, they mounted a robust, yet delayed, response, measured by anti-S, anti-receptor-binding domain IgG and neutralizing antibody (NAb) levels compared to survivors. Delayed seroconversion kinetics correlated with impaired viral control in deceased patients. Finally, although sera from 85% of patients displayed some neutralization capacity during their disease course, NAb generation before 14 d of disease onset emerged as a key factor for recovery. These data indicate that COVID-19 mortality does not correlate with the cross-sectional antiviral antibody levels per se but, rather, with the delayed kinetics of NAb production. A longitudinal analysis of humoral immune responses in patients with COVID-19 with varying disease severities reveals that mortality does not correlate with antiviral antibody levels but, instead, with slower seroconversion. |
| Audience | Academic |
| Author | Mohanty, Subhasis Yildirim, Inci Lucas, Carolina Grubaugh, Nathan D. Wong, Patrick Oh, Ji Eun Wisnewski, Adam V. Omer, Saad B. Moore, Adam J. Israelow, Benjamin Vogels, Chantal B. F. Casanovas-Massana, Arnau Park, Annsea Farhadian, Shelli Shaw, Albert C. Sundaram, Maria E. Wyllie, Anne L. Lu, Peiwen Muenker, M. Catherine Campbell, Melissa Mao, Tianyang Venkataraman, Arvind Iwasaki, Akiko Ko, Albert I. Silva, Julio Liu, Feimei Chun, Hyung J. Chang, C-Hong Zell, Joseph Lee, Alfred I. Schulz, Wade L. Klein, Jon Tokuyama, Maria Dela Cruz, Charles Ring, Aaron M. Huang, Jiefang Fournier, John B. |
| AuthorAffiliation | 1 Department of Immunobiology, Yale University School of Medicine, New Haven, CT, USA 5 Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT, USA 11 Department of Medicine, Section of Pulmonary and Critical Care Medicine, Yale University School of Medicine, New Haven, CT, USA 4 Department of Medicine, Section of Infectious Diseases, Yale University School of Medicine, New Haven, CT, USA 3 Centre for Vaccine Preventable Diseases, University of Toronto Dalla Lana School of Public Health, Toronto, ON, Canada 8 Department of Hematology, Yale University School of Medicine, New Haven, CT, USA 13 Yale Institute for Global Health, Yale University, New Haven, CT, USA 2 ICES, Toronto, ON, Canada 12 Department of Pediatric, Section of Infectious Diseases and Global Health, Yale University School of Medicine, New Haven, CT, USA 9 Department of Laboratory Medicine, Yale University School of Medicine, New Haven, CT, USA 14 Howard Hughes Medical Institute, Chevy Chase, |
| AuthorAffiliation_xml | – name: 11 Department of Medicine, Section of Pulmonary and Critical Care Medicine, Yale University School of Medicine, New Haven, CT, USA – name: 1 Department of Immunobiology, Yale University School of Medicine, New Haven, CT, USA – name: 6 Department of Medicine, Section of Cardiovascular Medicine, Yale University School of Medicine, New Haven, CT, USA – name: 8 Department of Hematology, Yale University School of Medicine, New Haven, CT, USA – name: 10 Center for Outcomes Research and Evaluation, Yale-New Haven Hospital, New Haven, CT, USA – name: 13 Yale Institute for Global Health, Yale University, New Haven, CT, USA – name: 14 Howard Hughes Medical Institute, Chevy Chase, MD, USA – name: 5 Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT, USA – name: 9 Department of Laboratory Medicine, Yale University School of Medicine, New Haven, CT, USA – name: 2 ICES, Toronto, ON, Canada – name: 3 Centre for Vaccine Preventable Diseases, University of Toronto Dalla Lana School of Public Health, Toronto, ON, Canada – name: 12 Department of Pediatric, Section of Infectious Diseases and Global Health, Yale University School of Medicine, New Haven, CT, USA – name: 4 Department of Medicine, Section of Infectious Diseases, Yale University School of Medicine, New Haven, CT, USA – name: 7 Department of Internal Medicine/Section General Medicine, Yale University School of Medicine, New Haven, CT, USA |
| Author_xml | – sequence: 1 givenname: Carolina orcidid: 0000-0003-4590-2756 surname: Lucas fullname: Lucas, Carolina organization: Department of Immunobiology, Yale University School of Medicine – sequence: 2 givenname: Jon orcidid: 0000-0002-3552-7684 surname: Klein fullname: Klein, Jon organization: Department of Immunobiology, Yale University School of Medicine – sequence: 3 givenname: Maria E. surname: Sundaram fullname: Sundaram, Maria E. organization: ICES, Centre for Vaccine Preventable Diseases, University of Toronto Dalla Lana School of Public Health – sequence: 4 givenname: Feimei orcidid: 0000-0003-2663-6544 surname: Liu fullname: Liu, Feimei organization: Department of Immunobiology, Yale University School of Medicine – sequence: 5 givenname: Patrick surname: Wong fullname: Wong, Patrick organization: Department of Immunobiology, Yale University School of Medicine – sequence: 6 givenname: Julio orcidid: 0000-0001-8212-7440 surname: Silva fullname: Silva, Julio organization: Department of Immunobiology, Yale University School of Medicine – sequence: 7 givenname: Tianyang orcidid: 0000-0001-9251-8592 surname: Mao fullname: Mao, Tianyang organization: Department of Immunobiology, Yale University School of Medicine – sequence: 8 givenname: Ji Eun orcidid: 0000-0003-2511-7064 surname: Oh fullname: Oh, Ji Eun organization: Department of Immunobiology, Yale University School of Medicine – sequence: 9 givenname: Subhasis surname: Mohanty fullname: Mohanty, Subhasis organization: Department of Immunobiology, Yale University School of Medicine, Department of Medicine, Section of Infectious Diseases, Yale University School of Medicine – sequence: 10 givenname: Jiefang surname: Huang fullname: Huang, Jiefang organization: Department of Immunobiology, Yale University School of Medicine, Department of Medicine, Section of Infectious Diseases, Yale University School of Medicine – sequence: 11 givenname: Maria surname: Tokuyama fullname: Tokuyama, Maria organization: Department of Immunobiology, Yale University School of Medicine – sequence: 12 givenname: Peiwen orcidid: 0000-0001-6118-872X surname: Lu fullname: Lu, Peiwen organization: Department of Immunobiology, Yale University School of Medicine – sequence: 13 givenname: Arvind surname: Venkataraman fullname: Venkataraman, Arvind organization: Department of Immunobiology, Yale University School of Medicine – sequence: 14 givenname: Annsea surname: Park fullname: Park, Annsea organization: Department of Immunobiology, Yale University School of Medicine – sequence: 15 givenname: Benjamin orcidid: 0000-0002-1308-8246 surname: Israelow fullname: Israelow, Benjamin organization: Department of Immunobiology, Yale University School of Medicine, Department of Medicine, Section of Infectious Diseases, Yale University School of Medicine – sequence: 16 givenname: Chantal B. F. orcidid: 0000-0003-0027-6480 surname: Vogels fullname: Vogels, Chantal B. F. organization: Department of Epidemiology of Microbial Diseases, Yale School of Public Health – sequence: 17 givenname: M. Catherine orcidid: 0000-0002-0450-0868 surname: Muenker fullname: Muenker, M. Catherine organization: Department of Epidemiology of Microbial Diseases, Yale School of Public Health – sequence: 18 givenname: C-Hong surname: Chang fullname: Chang, C-Hong organization: Department of Medicine, Section of Cardiovascular Medicine, Yale University School of Medicine – sequence: 19 givenname: Arnau surname: Casanovas-Massana fullname: Casanovas-Massana, Arnau organization: Department of Epidemiology of Microbial Diseases, Yale School of Public Health – sequence: 20 givenname: Adam J. surname: Moore fullname: Moore, Adam J. organization: Department of Epidemiology of Microbial Diseases, Yale School of Public Health – sequence: 21 givenname: Joseph surname: Zell fullname: Zell, Joseph organization: Department of Internal Medicine/Section General Medicine, Yale University School of Medicine – sequence: 22 givenname: John B. surname: Fournier fullname: Fournier, John B. organization: Department of Medicine, Section of Infectious Diseases, Yale University School of Medicine – sequence: 24 givenname: Anne L. orcidid: 0000-0001-6015-0279 surname: Wyllie fullname: Wyllie, Anne L. organization: Department of Epidemiology of Microbial Diseases, Yale School of Public Health – sequence: 25 givenname: Melissa surname: Campbell fullname: Campbell, Melissa organization: Department of Medicine, Section of Infectious Diseases, Yale University School of Medicine – sequence: 26 givenname: Alfred I. surname: Lee fullname: Lee, Alfred I. organization: Department of Hematology, Yale University School of Medicine – sequence: 27 givenname: Hyung J. orcidid: 0000-0003-3508-2678 surname: Chun fullname: Chun, Hyung J. organization: Department of Medicine, Section of Cardiovascular Medicine, Yale University School of Medicine – sequence: 28 givenname: Nathan D. orcidid: 0000-0003-2031-1933 surname: Grubaugh fullname: Grubaugh, Nathan D. organization: Department of Epidemiology of Microbial Diseases, Yale School of Public Health – sequence: 29 givenname: Wade L. orcidid: 0000-0002-2048-4028 surname: Schulz fullname: Schulz, Wade L. organization: Department of Laboratory Medicine, Yale University School of Medicine, Center for Outcomes Research and Evaluation, Yale-New Haven Hospital – sequence: 30 givenname: Shelli orcidid: 0000-0001-7230-1409 surname: Farhadian fullname: Farhadian, Shelli organization: Department of Medicine, Section of Infectious Diseases, Yale University School of Medicine – sequence: 31 givenname: Charles orcidid: 0000-0002-5258-1797 surname: Dela Cruz fullname: Dela Cruz, Charles organization: Department of Medicine, Section of Pulmonary and Critical Care Medicine, Yale University School of Medicine – sequence: 32 givenname: Aaron M. orcidid: 0000-0003-3699-2446 surname: Ring fullname: Ring, Aaron M. organization: Department of Immunobiology, Yale University School of Medicine – sequence: 33 givenname: Albert C. surname: Shaw fullname: Shaw, Albert C. organization: Department of Immunobiology, Yale University School of Medicine, Department of Medicine, Section of Infectious Diseases, Yale University School of Medicine – sequence: 34 givenname: Adam V. surname: Wisnewski fullname: Wisnewski, Adam V. organization: Department of Internal Medicine/Section General Medicine, Yale University School of Medicine – sequence: 35 givenname: Inci surname: Yildirim fullname: Yildirim, Inci organization: Department of Pediatric, Section of Infectious Diseases and Global Health, Yale University School of Medicine, Yale Institute for Global Health, Yale University – sequence: 36 givenname: Albert I. orcidid: 0000-0001-9023-2339 surname: Ko fullname: Ko, Albert I. organization: Department of Medicine, Section of Infectious Diseases, Yale University School of Medicine, Department of Epidemiology of Microbial Diseases, Yale School of Public Health – sequence: 37 givenname: Saad B. orcidid: 0000-0002-5383-3474 surname: Omer fullname: Omer, Saad B. organization: Department of Medicine, Section of Infectious Diseases, Yale University School of Medicine, Department of Epidemiology of Microbial Diseases, Yale School of Public Health, Yale Institute for Global Health, Yale University – sequence: 38 givenname: Akiko orcidid: 0000-0002-7824-9856 surname: Iwasaki fullname: Iwasaki, Akiko email: akiko.iwasaki@yale.edu organization: Department of Immunobiology, Yale University School of Medicine, Howard Hughes Medical Institute |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33953384$$D View this record in MEDLINE/PubMed |
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| Cites_doi | 10.1136/bmj.m3939 10.3201/eid2612.203334 10.1016/S0140-6736(20)31604-4 10.1016/j.chom.2020.04.017 10.1038/s41591-020-1051-9 10.1016/j.cell.2020.08.025 10.1126/sciimmunol.abe0240 10.1038/s41586-020-2588-y 10.1016/j.cell.2020.12.015 10.1016/S2213-2600(20)30076-X 10.1126/scitranslmed.abf1555 10.1038/s41392-020-00301-9 10.1016/S0140-6736(20)30183-5 10.1016/j.immuni.2020.10.004 10.1371/journal.pone.0237901 10.1016/j.immuni.2020.07.020 10.1016/j.xcrm.2020.100078 10.1172/jci.insight.146242 10.1016/j.cell.2020.02.052 10.1111/j.1464-410X.1987.tb05006.x 10.1128/mBio.02940-20 10.1016/j.cell.2020.10.052 10.1038/s41564-020-0761-6 10.1016/j.cell.2020.06.025 10.1016/j.chom.2020.04.009 10.1136/bmj.m4072 10.1126/science.abc8511 10.1371/journal.ppat.1008796 10.1101/2020.06.08.140871 10.1126/science.abc6284 10.1038/s41591-020-0897-1 10.1016/j.apsb.2020.10.025 10.1056/NEJMoa2029849 10.1038/s41591-020-0913-5 10.1126/science.abb2762 10.1172/JCI137244 10.1038/s41586-020-2456-9 10.1056/NEJMc2016359 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 These authors contributed equally: Carolina Lucas, Jon Klein. A list of authors and their affiliations appears at the end of the paper. A.I.K. and A.I. conceived the study. C.L., J.K., J.S., J.E.O. and T.M collected and processed patient PBMC and plasma samples. C.L. and J.K. performed the neutralization assays. C.L, did the data analyses. P.W, performed the flow cytometry, and C.L. did the flow data analyses. J.S. and B.I. collected epidemiological and clinical data. F.L. and C.L. performed the SARS-CoV-2 specific antibody ELISAs. A.R. supervised the ELISAs. A.L.W., C.B.F., P.L., A.V., A.P. and M.T. performed sample processing, extractions and RT-qPCR assays, under the supervision of N.D.G. A.C.-M. and M.C.M. processed and stored patient specimens. J.Z. and A.V.W. assisted in mild disease volunteer recruitment. M.C., J.B.F., C.D.C. and S.F. assisted with the identification and enrolment of hospitalized patients. W.L.S. supervised clinical data management. C.L. and A.I. drafted the manuscript. All authors helped to edit the manuscript. A.I. secured funds and supervised the project. Author contributions |
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| References | Röltgen, K. et al. Defining the features and duration of antibody responses to SARS-CoV-2 infection associated with disease severity and outcome. Sci. Immunol.5, eabe0240 (2020). ChenYA comprehensive, longitudinal analysis of humoral responses specific to four recombinant antigens of SARS-CoV-2 in severe and non-severe COVID-19 patientsPLoS Pathog.202016e10087961:CAS:528:DC%2BB3cXhvVeitr3E10.1371/journal.ppat.1008796 MathewDDeep immune profiling of COVID-19 patients reveals distinct immunotypes with therapeutic implicationsScience2020369eabc85111:CAS:528:DC%2BB3cXhslCltrnF10.1126/science.abc8511 ChenXDisease severity dictates SARS-CoV-2-specific neutralizing antibody responses in COVID-19Signal Transduct. Target Ther.202051801:CAS:528:DC%2BB3cXhslGqtbvI10.1038/s41392-020-00301-9 Del ValleDMAn inflammatory cytokine signature predicts COVID-19 severity and survivalNat. Med.2020261636164310.1038/s41591-020-1051-9 Yu, K. K. Q. et al. Comorbid illnesses are associated with altered adaptive immune responses to SARS-CoV-2. JCI Insighthttps://doi.org/10.1172/jci.insight.146242 (2021). LongQXAntibody responses to SARS-CoV-2 in patients with COVID-19Nat. Med.2020268458481:CAS:528:DC%2BB3cXot1aktLk%3D10.1038/s41591-020-0897-1 LucasCLongitudinal analyses reveal immunological misfiring in severe COVID-19Nature20205844634691:CAS:528:DC%2BB3cXhsF2ntL3K10.1038/s41586-020-2588-y YanRStructural basis for the recognition of SARS-CoV-2 by full-length human ACE2Science2020367144414481:CAS:528:DC%2BB3cXlslymsLo%3D10.1126/science.abb2762 KanekoNLoss of Bcl-6-expressing T follicular helper cells and germinal centers in COVID-19Cell20201831431571:CAS:528:DC%2BB3cXhslygsLvO10.1016/j.cell.2020.08.025 Hu, W. T. et al. Antibody profiles according to mild or severe SARS-CoV-2 infection, Atlanta, Georgia, USA, 2020. Emerg. Infect. Dis.26, 2974–2978 (2020). AtyeoCDistinct early serological signatures track with SARS-CoV-2 survivalImmunity20205352453210.1016/j.immuni.2020.07.020 Eli Lilly and Company. Lilly statement regarding NIH’s ACTIV-3 clinical trial. https://www.lilly.com/news/stories/statement-activ3-clinical-trial-nih-covid19 (October 26, 2020). May, B. Regeneron halts enrollment of critically ill patients in a COVID-19 antibody trial. https://www.biospace.com/article/regeneron-halts-enrollment-in-covid-19-trial-following-safety-signal-in-critically-ill-patients (BioSpace, 2020). Guthmiller, J. J. et al. SARS-CoV-2 infection severity is linked to superior humoral immunity against the spike. mBiohttps://doi.org/10.1128/mBio.02940-20 (2021). FolegattiPMSafety and immunogenicity of the ChAdOx1 nCoV-19 vaccine against SARS-CoV-2: a preliminary report of a phase 1/2, single-blind, randomised controlled trialLancet20203964674781:CAS:528:DC%2BB3cXhsVaku7fE10.1016/S0140-6736(20)31604-4 RodriguezLSystems-level immunomonitoring from acute to recovery phase of severe COVID-19Cell Rep. Med.2020110007810.1016/j.xcrm.2020.100078 AmanatFA serological assay to detect SARS-CoV-2 seroconversion in humansNat. Med.202026103310361:CAS:528:DC%2BB3cXptFyqsbY%3D10.1038/s41591-020-0913-5 Zhou, Z. et al. Heightened innate immune responses in the respiratory tract of COVID-19 patients. Cell Host Microbe27, 883–890 (2020). AgarwalAConvalescent plasma in the management of moderate covid-19 in adults in India: open label phase II multicentre randomised controlled trial (PLACID Trial)Brit. Med. J.2020371m393910.1136/bmj.m3939 HollimanRSealDVArcherHDomanSControlled trial of chemical disinfection of urinary drainage bags. Reduction in hospital-acquired catheter-associated infectionBr. J. Urol.1987604194221:STN:280:DyaL1c7gvVClsw%3D%3D10.1111/j.1464-410X.1987.tb05006.x XuZPathological findings of COVID-19 associated with acute respiratory distress syndromeLancet Respir. Med.202084204221:CAS:528:DC%2BB3cXjsValtbk%3D10.1016/S2213-2600(20)30076-X Zohar, T. et al. Compromised humoral functional evolution tracks with SARS-CoV-2 mortality. Cell183, 1508–1519 (2020). Wyllie, A. L. et al. Saliva is more sensitive for SARS-CoV-2 detection in COVID-19 patients than nasopharyngeal swabs. N. Engl. J. Med.https://doi.org/10.1056/NEJMc2016359 (2020). Garcia-BeltranWFCOVID-19-neutralizing antibodies predict disease severity and survivalCell20211844764881:CAS:528:DC%2BB3MXnsFCgsw%3D%3D10.1016/j.cell.2020.12.015 WangZEnhanced SARS-CoV-2 neutralization by dimeric IgASci. Transl. Med.202113eabf15551:CAS:528:DC%2BB3MXit1yks70%3D10.1126/scitranslmed.abf1555 AbryPSpatial and temporal regularization to estimate COVID-19 reproduction number R(t): promoting piecewise smoothness via convex optimizationPLoS ONE202015e02379011:CAS:528:DC%2BB3cXhs1OntrnF10.1371/journal.pone.0237901 Giamarellos-BourboulisEJComplex immune dysregulation in COVID-19 patients with severe respiratory failureCell Host Microbe20202799210001:CAS:528:DC%2BB3cXnvFehsb4%3D10.1016/j.chom.2020.04.009 Zhou, Z., Wang, X., Fu, Y., Zhang, X. & Liu, C. Neutralizing antibodies for the treatment of COVID-19. Acta Pharm. Sin. B11, 304–307 (2020). Hoffmann, M. et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell181, 271–280 (2020). YuJDNA vaccine protection against SARS-CoV-2 in rhesus macaquesScience20203698068111:CAS:528:DC%2BB3cXhsF2qsrrN10.1126/science.abc6284 Chen, G. et al. Clinical and immunologic features in severe and moderate Coronavirus Disease 2019. J. Clin. Invest.130, 2620–2629 (2020). Chen, P. et al. SARS-CoV-2 neutralizing antibody LY-CoV555 in outpatients with Covid-19. N. Engl. J. Med.384, 229–237 (2020). RobbianiDFConvergent antibody responses to SARS-CoV-2 in convalescent individualsNature20205844374421:CAS:528:DC%2BB3cXhsFegtb3P10.1038/s41586-020-2456-9 FDA authorizes monoclonal antibodies for treatment of COVID-19. https://www.fda.gov/news-events/press-announcements/coronavirus-covid-19-update-fda-authorizes-monoclonal-antibodies-treatment-covid-19 (U.S. Food and Drug Administration, 2020). PathakEBConvalescent plasma is ineffective for covid-19Brit. Med. J.2020371m407210.1136/bmj.m4072 ValkSJConvalescent plasma or hyperimmune immunoglobulin for people with COVID-19: a rapid reviewCochrane Database Syst. Rev.20205CD01360032406927 HuangCClinical features of patients infected with 2019 novel coronavirus in Wuhan, ChinaLancet20203954975061:CAS:528:DC%2BB3cXhs1Kqu7c%3D10.1016/S0140-6736(20)30183-5 VogelsCBFAnalytical sensitivity and efficiency comparisons of SARS-CoV-2 RT-qPCR primer-probe setsNat. Microbiol.20205129913051:CAS:528:DC%2BB3cXhtlOjtbzF10.1038/s41564-020-0761-6 RippergerTJOrthogonal SARS-CoV-2 serological assays enable surveillance of low-prevalence communities and reveal durable humoral immunityImmunity2020539259331:CAS:528:DC%2BB3cXit1aktb3K10.1016/j.immuni.2020.10.004 BarnesCOStructures of human antibodies bound to SARS-CoV-2 spike reveal common epitopes and recurrent features of antibodiesCell20201828288421:CAS:528:DC%2BB3cXhtlGmsb3P10.1016/j.cell.2020.06.025 Schmidt, F. et al. Measuring SARS-CoV-2 neutralizing antibody activity using pseudotyped and chimeric viruses. J. Exp. Med.217, e20201181 (2020). F Amanat (1355_CR40) 2020; 26 DM Del Valle (1355_CR10) 2020; 26 PM Folegatti (1355_CR21) 2020; 396 1355_CR35 1355_CR14 1355_CR36 C Atyeo (1355_CR26) 2020; 53 Z Wang (1355_CR15) 2021; 13 A Agarwal (1355_CR31) 2020; 371 R Holliman (1355_CR33) 1987; 60 Z Xu (1355_CR3) 2020; 8 L Rodriguez (1355_CR9) 2020; 1 X Chen (1355_CR17) 2020; 5 EB Pathak (1355_CR32) 2020; 371 EJ Giamarellos-Bourboulis (1355_CR6) 2020; 27 SJ Valk (1355_CR34) 2020; 5 1355_CR7 N Kaneko (1355_CR30) 2020; 183 1355_CR5 WF Garcia-Beltran (1355_CR22) 2021; 184 1355_CR39 DF Robbiani (1355_CR13) 2020; 584 1355_CR18 1355_CR1 1355_CR37 1355_CR38 C Huang (1355_CR4) 2020; 395 CO Barnes (1355_CR12) 2020; 182 1355_CR19 P Abry (1355_CR29) 2020; 15 Y Chen (1355_CR16) 2020; 16 J Yu (1355_CR20) 2020; 369 1355_CR41 CBF Vogels (1355_CR42) 2020; 5 1355_CR25 C Lucas (1355_CR8) 2020; 584 R Yan (1355_CR2) 2020; 367 D Mathew (1355_CR11) 2020; 369 TJ Ripperger (1355_CR24) 2020; 53 QX Long (1355_CR23) 2020; 26 1355_CR28 1355_CR27 34145437 - Nat Med. 2021 Jun 18 |
| References_xml | – reference: Hoffmann, M. et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell181, 271–280 (2020). – reference: Röltgen, K. et al. Defining the features and duration of antibody responses to SARS-CoV-2 infection associated with disease severity and outcome. Sci. Immunol.5, eabe0240 (2020). – reference: Chen, G. et al. Clinical and immunologic features in severe and moderate Coronavirus Disease 2019. J. Clin. Invest.130, 2620–2629 (2020). – reference: Guthmiller, J. J. et al. SARS-CoV-2 infection severity is linked to superior humoral immunity against the spike. mBiohttps://doi.org/10.1128/mBio.02940-20 (2021). – reference: HollimanRSealDVArcherHDomanSControlled trial of chemical disinfection of urinary drainage bags. Reduction in hospital-acquired catheter-associated infectionBr. J. Urol.1987604194221:STN:280:DyaL1c7gvVClsw%3D%3D10.1111/j.1464-410X.1987.tb05006.x – reference: Schmidt, F. et al. Measuring SARS-CoV-2 neutralizing antibody activity using pseudotyped and chimeric viruses. J. Exp. Med.217, e20201181 (2020). – reference: Garcia-BeltranWFCOVID-19-neutralizing antibodies predict disease severity and survivalCell20211844764881:CAS:528:DC%2BB3MXnsFCgsw%3D%3D10.1016/j.cell.2020.12.015 – reference: May, B. Regeneron halts enrollment of critically ill patients in a COVID-19 antibody trial. https://www.biospace.com/article/regeneron-halts-enrollment-in-covid-19-trial-following-safety-signal-in-critically-ill-patients (BioSpace, 2020). – reference: Zhou, Z. et al. Heightened innate immune responses in the respiratory tract of COVID-19 patients. Cell Host Microbe27, 883–890 (2020). – reference: Zhou, Z., Wang, X., Fu, Y., Zhang, X. & Liu, C. Neutralizing antibodies for the treatment of COVID-19. Acta Pharm. Sin. B11, 304–307 (2020). – reference: MathewDDeep immune profiling of COVID-19 patients reveals distinct immunotypes with therapeutic implicationsScience2020369eabc85111:CAS:528:DC%2BB3cXhslCltrnF10.1126/science.abc8511 – reference: RippergerTJOrthogonal SARS-CoV-2 serological assays enable surveillance of low-prevalence communities and reveal durable humoral immunityImmunity2020539259331:CAS:528:DC%2BB3cXit1aktb3K10.1016/j.immuni.2020.10.004 – reference: AmanatFA serological assay to detect SARS-CoV-2 seroconversion in humansNat. Med.202026103310361:CAS:528:DC%2BB3cXptFyqsbY%3D10.1038/s41591-020-0913-5 – reference: AgarwalAConvalescent plasma in the management of moderate covid-19 in adults in India: open label phase II multicentre randomised controlled trial (PLACID Trial)Brit. Med. J.2020371m393910.1136/bmj.m3939 – reference: KanekoNLoss of Bcl-6-expressing T follicular helper cells and germinal centers in COVID-19Cell20201831431571:CAS:528:DC%2BB3cXhslygsLvO10.1016/j.cell.2020.08.025 – reference: FDA authorizes monoclonal antibodies for treatment of COVID-19. https://www.fda.gov/news-events/press-announcements/coronavirus-covid-19-update-fda-authorizes-monoclonal-antibodies-treatment-covid-19 (U.S. Food and Drug Administration, 2020). – reference: RodriguezLSystems-level immunomonitoring from acute to recovery phase of severe COVID-19Cell Rep. Med.2020110007810.1016/j.xcrm.2020.100078 – reference: FolegattiPMSafety and immunogenicity of the ChAdOx1 nCoV-19 vaccine against SARS-CoV-2: a preliminary report of a phase 1/2, single-blind, randomised controlled trialLancet20203964674781:CAS:528:DC%2BB3cXhsVaku7fE10.1016/S0140-6736(20)31604-4 – reference: AbryPSpatial and temporal regularization to estimate COVID-19 reproduction number R(t): promoting piecewise smoothness via convex optimizationPLoS ONE202015e02379011:CAS:528:DC%2BB3cXhs1OntrnF10.1371/journal.pone.0237901 – reference: PathakEBConvalescent plasma is ineffective for covid-19Brit. Med. J.2020371m407210.1136/bmj.m4072 – reference: Del ValleDMAn inflammatory cytokine signature predicts COVID-19 severity and survivalNat. Med.2020261636164310.1038/s41591-020-1051-9 – reference: XuZPathological findings of COVID-19 associated with acute respiratory distress syndromeLancet Respir. Med.202084204221:CAS:528:DC%2BB3cXjsValtbk%3D10.1016/S2213-2600(20)30076-X – reference: YuJDNA vaccine protection against SARS-CoV-2 in rhesus macaquesScience20203698068111:CAS:528:DC%2BB3cXhsF2qsrrN10.1126/science.abc6284 – reference: Zohar, T. et al. Compromised humoral functional evolution tracks with SARS-CoV-2 mortality. Cell183, 1508–1519 (2020). – reference: LongQXAntibody responses to SARS-CoV-2 in patients with COVID-19Nat. Med.2020268458481:CAS:528:DC%2BB3cXot1aktLk%3D10.1038/s41591-020-0897-1 – reference: Chen, P. et al. SARS-CoV-2 neutralizing antibody LY-CoV555 in outpatients with Covid-19. N. Engl. J. Med.384, 229–237 (2020). – reference: ValkSJConvalescent plasma or hyperimmune immunoglobulin for people with COVID-19: a rapid reviewCochrane Database Syst. Rev.20205CD01360032406927 – reference: Giamarellos-BourboulisEJComplex immune dysregulation in COVID-19 patients with severe respiratory failureCell Host Microbe20202799210001:CAS:528:DC%2BB3cXnvFehsb4%3D10.1016/j.chom.2020.04.009 – reference: WangZEnhanced SARS-CoV-2 neutralization by dimeric IgASci. Transl. Med.202113eabf15551:CAS:528:DC%2BB3MXit1yks70%3D10.1126/scitranslmed.abf1555 – reference: Hu, W. T. et al. Antibody profiles according to mild or severe SARS-CoV-2 infection, Atlanta, Georgia, USA, 2020. Emerg. Infect. Dis.26, 2974–2978 (2020). – reference: Wyllie, A. L. et al. Saliva is more sensitive for SARS-CoV-2 detection in COVID-19 patients than nasopharyngeal swabs. N. Engl. J. Med.https://doi.org/10.1056/NEJMc2016359 (2020). – reference: BarnesCOStructures of human antibodies bound to SARS-CoV-2 spike reveal common epitopes and recurrent features of antibodiesCell20201828288421:CAS:528:DC%2BB3cXhtlGmsb3P10.1016/j.cell.2020.06.025 – reference: Eli Lilly and Company. Lilly statement regarding NIH’s ACTIV-3 clinical trial. https://www.lilly.com/news/stories/statement-activ3-clinical-trial-nih-covid19 (October 26, 2020). – reference: AtyeoCDistinct early serological signatures track with SARS-CoV-2 survivalImmunity20205352453210.1016/j.immuni.2020.07.020 – reference: LucasCLongitudinal analyses reveal immunological misfiring in severe COVID-19Nature20205844634691:CAS:528:DC%2BB3cXhsF2ntL3K10.1038/s41586-020-2588-y – reference: ChenXDisease severity dictates SARS-CoV-2-specific neutralizing antibody responses in COVID-19Signal Transduct. Target Ther.202051801:CAS:528:DC%2BB3cXhslGqtbvI10.1038/s41392-020-00301-9 – reference: VogelsCBFAnalytical sensitivity and efficiency comparisons of SARS-CoV-2 RT-qPCR primer-probe setsNat. Microbiol.20205129913051:CAS:528:DC%2BB3cXhtlOjtbzF10.1038/s41564-020-0761-6 – reference: RobbianiDFConvergent antibody responses to SARS-CoV-2 in convalescent individualsNature20205844374421:CAS:528:DC%2BB3cXhsFegtb3P10.1038/s41586-020-2456-9 – reference: Yu, K. K. Q. et al. Comorbid illnesses are associated with altered adaptive immune responses to SARS-CoV-2. JCI Insighthttps://doi.org/10.1172/jci.insight.146242 (2021). – reference: HuangCClinical features of patients infected with 2019 novel coronavirus in Wuhan, ChinaLancet20203954975061:CAS:528:DC%2BB3cXhs1Kqu7c%3D10.1016/S0140-6736(20)30183-5 – reference: ChenYA comprehensive, longitudinal analysis of humoral responses specific to four recombinant antigens of SARS-CoV-2 in severe and non-severe COVID-19 patientsPLoS Pathog.202016e10087961:CAS:528:DC%2BB3cXhvVeitr3E10.1371/journal.ppat.1008796 – reference: YanRStructural basis for the recognition of SARS-CoV-2 by full-length human ACE2Science2020367144414481:CAS:528:DC%2BB3cXlslymsLo%3D10.1126/science.abb2762 – volume: 371 start-page: m3939 year: 2020 ident: 1355_CR31 publication-title: Brit. Med. J. doi: 10.1136/bmj.m3939 – ident: 1355_CR18 doi: 10.3201/eid2612.203334 – volume: 396 start-page: 467 year: 2020 ident: 1355_CR21 publication-title: Lancet doi: 10.1016/S0140-6736(20)31604-4 – ident: 1355_CR7 doi: 10.1016/j.chom.2020.04.017 – volume: 26 start-page: 1636 year: 2020 ident: 1355_CR10 publication-title: Nat. Med. doi: 10.1038/s41591-020-1051-9 – volume: 183 start-page: 143 year: 2020 ident: 1355_CR30 publication-title: Cell doi: 10.1016/j.cell.2020.08.025 – volume: 5 start-page: CD013600 year: 2020 ident: 1355_CR34 publication-title: Cochrane Database Syst. Rev. – ident: 1355_CR27 doi: 10.1126/sciimmunol.abe0240 – volume: 584 start-page: 463 year: 2020 ident: 1355_CR8 publication-title: Nature doi: 10.1038/s41586-020-2588-y – volume: 184 start-page: 476 year: 2021 ident: 1355_CR22 publication-title: Cell doi: 10.1016/j.cell.2020.12.015 – volume: 8 start-page: 420 year: 2020 ident: 1355_CR3 publication-title: Lancet Respir. Med. doi: 10.1016/S2213-2600(20)30076-X – volume: 13 start-page: eabf1555 year: 2021 ident: 1355_CR15 publication-title: Sci. Transl. Med. doi: 10.1126/scitranslmed.abf1555 – volume: 5 start-page: 180 year: 2020 ident: 1355_CR17 publication-title: Signal Transduct. Target Ther. doi: 10.1038/s41392-020-00301-9 – volume: 395 start-page: 497 year: 2020 ident: 1355_CR4 publication-title: Lancet doi: 10.1016/S0140-6736(20)30183-5 – volume: 53 start-page: 925 year: 2020 ident: 1355_CR24 publication-title: Immunity doi: 10.1016/j.immuni.2020.10.004 – volume: 15 start-page: e0237901 year: 2020 ident: 1355_CR29 publication-title: PLoS ONE doi: 10.1371/journal.pone.0237901 – volume: 53 start-page: 524 year: 2020 ident: 1355_CR26 publication-title: Immunity doi: 10.1016/j.immuni.2020.07.020 – ident: 1355_CR37 – volume: 1 start-page: 100078 year: 2020 ident: 1355_CR9 publication-title: Cell Rep. Med. doi: 10.1016/j.xcrm.2020.100078 – ident: 1355_CR19 doi: 10.1172/jci.insight.146242 – ident: 1355_CR1 doi: 10.1016/j.cell.2020.02.052 – volume: 60 start-page: 419 year: 1987 ident: 1355_CR33 publication-title: Br. J. Urol. doi: 10.1111/j.1464-410X.1987.tb05006.x – ident: 1355_CR25 doi: 10.1128/mBio.02940-20 – ident: 1355_CR28 doi: 10.1016/j.cell.2020.10.052 – volume: 5 start-page: 1299 year: 2020 ident: 1355_CR42 publication-title: Nat. Microbiol. doi: 10.1038/s41564-020-0761-6 – volume: 182 start-page: 828 year: 2020 ident: 1355_CR12 publication-title: Cell doi: 10.1016/j.cell.2020.06.025 – volume: 27 start-page: 992 year: 2020 ident: 1355_CR6 publication-title: Cell Host Microbe doi: 10.1016/j.chom.2020.04.009 – volume: 371 start-page: m4072 year: 2020 ident: 1355_CR32 publication-title: Brit. Med. J. doi: 10.1136/bmj.m4072 – volume: 369 start-page: eabc8511 year: 2020 ident: 1355_CR11 publication-title: Science doi: 10.1126/science.abc8511 – volume: 16 start-page: e1008796 year: 2020 ident: 1355_CR16 publication-title: PLoS Pathog. doi: 10.1371/journal.ppat.1008796 – ident: 1355_CR14 doi: 10.1101/2020.06.08.140871 – volume: 369 start-page: 806 year: 2020 ident: 1355_CR20 publication-title: Science doi: 10.1126/science.abc6284 – volume: 26 start-page: 845 year: 2020 ident: 1355_CR23 publication-title: Nat. Med. doi: 10.1038/s41591-020-0897-1 – ident: 1355_CR35 doi: 10.1016/j.apsb.2020.10.025 – ident: 1355_CR39 doi: 10.1056/NEJMoa2029849 – volume: 26 start-page: 1033 year: 2020 ident: 1355_CR40 publication-title: Nat. Med. doi: 10.1038/s41591-020-0913-5 – volume: 367 start-page: 1444 year: 2020 ident: 1355_CR2 publication-title: Science doi: 10.1126/science.abb2762 – ident: 1355_CR5 doi: 10.1172/JCI137244 – ident: 1355_CR36 – volume: 584 start-page: 437 year: 2020 ident: 1355_CR13 publication-title: Nature doi: 10.1038/s41586-020-2456-9 – ident: 1355_CR41 doi: 10.1056/NEJMc2016359 – ident: 1355_CR38 – reference: 34145437 - Nat Med. 2021 Jun 18;: |
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| Snippet | Recent studies have provided insights into innate and adaptive immune dynamics in coronavirus disease 2019 (COVID-19). However, the exact features of antibody... |
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| SubjectTerms | 631/250/2152/2153/1291 631/250/255/2514 Aged Aged, 80 and over Antibodies Antibodies, Neutralizing - immunology Antibodies, Viral - immunology Antiviral drugs Biomedical and Life Sciences Biomedicine Cancer Research Carrier State - immunology Coronaviruses COVID-19 COVID-19 - immunology COVID-19 - mortality COVID-19 - prevention & control COVID-19 Vaccines - therapeutic use Data recovery Female Humans IgG antibody Immune response Immune response (humoral) Immunity, Humoral Immunoglobulin G Immunoglobulin G - immunology Infectious Diseases Kinetics Length of Stay - statistics & numerical data Male Medical research Medicine, Experimental Metabolic Diseases Middle Aged Molecular Medicine Mortality Neurosciences Neutralization Neutralizing Patients Physiological aspects SARS-CoV-2 - immunology Seroconversion Severity of Illness Index Spike Glycoprotein, Coronavirus - immunology Time dependence Time Factors Viral antibodies Viral diseases |
| Title | Delayed production of neutralizing antibodies correlates with fatal COVID-19 |
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