A Novel Method to Reduce ELISA Serial Dilution Assay Workload Applied to SARS-CoV-2 and Seasonal HCoVs

Assays using ELISA measurements on serially diluted serum samples have been heavily used to measure serum reactivity to SARS-CoV-2 antigens and are widely used in virology and elsewhere in biology. We test a method using Bayesian hierarchical modelling to reduce the workload of these assays and meas...

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Published inViruses Vol. 14; no. 3; p. 562
Main Authors Pattinson, David, Jester, Peter, Guan, Lizheng, Yamayoshi, Seiya, Chiba, Shiho, Presler, Robert, Rao, Hongyu, Iwatsuki-Horimoto, Kiyoko, Ikeda, Nobuhiro, Hagihara, Masao, Uchida, Tomoyuki, Mitamura, Keiko, Halfmann, Peter, Neumann, Gabriele, Kawaoka, Yoshihiro
Format Journal Article
LanguageEnglish
Published Switzerland MDPI AG 09.03.2022
MDPI
Subjects
Antibodies
Antibodies, Viral
Antigens
Bayes Theorem
Bayesian analysis
Bayesian theory
blood serum
computer software
Coronaviruses
COVID-19
COVID-19 - diagnosis
COVID-19 infection
Disease transmission
ELISA
Enzyme-Linked Immunosorbent Assay
HCoV-229E
HCoV-HKU1
HCoV-NL63
HCoV-OC43
Humans
Infections
Influenza
Laboratories
Microbiology
Middle East respiratory syndrome
nucleoproteins
Pandemics
QR1-502
Respiratory diseases
SARS-CoV-2
SARS-CoV-2; HCoV-OC43; HCoV-HKU1; HCoV-229E; HCoV-NL63; ELISA; Bayesian analysis; hierarchical modelling; endpoint assay; inflection titer
Seasons
Serology
Severe acute respiratory syndrome coronavirus 2
Spike protein
Standard deviation
virology
Workload
United States > US
SARS-CoV-2
HCoV-229E
HCoV-HKU1
HCoV-NL63
hierarchical modelling
inflection titer
endpoint assay
Bayesian analysis
ELISA
HCoV-OC43
Online AccessGet full text
ISSN1999-4915
1999-4915
DOI10.3390/v14030562

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Abstract Assays using ELISA measurements on serially diluted serum samples have been heavily used to measure serum reactivity to SARS-CoV-2 antigens and are widely used in virology and elsewhere in biology. We test a method using Bayesian hierarchical modelling to reduce the workload of these assays and measure reactivity of SARS-CoV-2 and HCoV antigens to human serum samples collected before and during the COVID-19 pandemic. Inflection titers for SARS-CoV-2 full-length spike protein (S1S2), spike protein receptor-binding domain (RBD), and nucleoprotein (N) inferred from 3 spread-out dilutions correlated with those inferred from 8 consecutive dilutions with an R2 value of 0.97 or higher. We confirm existing findings showing a small proportion of pre-pandemic human serum samples contain cross-reactive antibodies to SARS-CoV-2 S1S2 and N, and that SARS-CoV-2 infection increases serum reactivity to the beta-HCoVs OC43 and HKU1 S1S2. In serial dilution assays, large savings in resources and/or increases in throughput can be achieved by reducing the number of dilutions measured and using Bayesian hierarchical modelling to infer inflection or endpoint titers. We have released software for conducting these types of analysis.
AbstractList Assays using ELISA measurements on serially diluted serum samples have been heavily used to measure serum reactivity to SARS-CoV-2 antigens and are widely used in virology and elsewhere in biology. We test a method using Bayesian hierarchical modelling to reduce the workload of these assays and measure reactivity of SARS-CoV-2 and HCoV antigens to human serum samples collected before and during the COVID-19 pandemic. Inflection titers for SARS-CoV-2 full-length spike protein (S1S2), spike protein receptor-binding domain (RBD), and nucleoprotein (N) inferred from 3 spread-out dilutions correlated with those inferred from 8 consecutive dilutions with an R value of 0.97 or higher. We confirm existing findings showing a small proportion of pre-pandemic human serum samples contain cross-reactive antibodies to SARS-CoV-2 S1S2 and N, and that SARS-CoV-2 infection increases serum reactivity to the beta-HCoVs OC43 and HKU1 S1S2. In serial dilution assays, large savings in resources and/or increases in throughput can be achieved by reducing the number of dilutions measured and using Bayesian hierarchical modelling to infer inflection or endpoint titers. We have released software for conducting these types of analysis.
Assays using ELISA measurements on serially diluted serum samples have been heavily used to measure serum reactivity to SARS-CoV-2 antigens and are widely used in virology and elsewhere in biology. We test a method using Bayesian hierarchical modelling to reduce the workload of these assays and measure reactivity of SARS-CoV-2 and HCoV antigens to human serum samples collected before and during the COVID-19 pandemic. Inflection titers for SARS-CoV-2 full-length spike protein (S1S2), spike protein receptor-binding domain (RBD), and nucleoprotein (N) inferred from 3 spread-out dilutions correlated with those inferred from 8 consecutive dilutions with an R² value of 0.97 or higher. We confirm existing findings showing a small proportion of pre-pandemic human serum samples contain cross-reactive antibodies to SARS-CoV-2 S1S2 and N, and that SARS-CoV-2 infection increases serum reactivity to the beta-HCoVs OC43 and HKU1 S1S2. In serial dilution assays, large savings in resources and/or increases in throughput can be achieved by reducing the number of dilutions measured and using Bayesian hierarchical modelling to infer inflection or endpoint titers. We have released software for conducting these types of analysis.
Assays using ELISA measurements on serially diluted serum samples have been heavily used to measure serum reactivity to SARS-CoV-2 antigens and are widely used in virology and elsewhere in biology. We test a method using Bayesian hierarchical modelling to reduce the workload of these assays and measure reactivity of SARS-CoV-2 and HCoV antigens to human serum samples collected before and during the COVID-19 pandemic. Inflection titers for SARS-CoV-2 full-length spike protein (S1S2), spike protein receptor-binding domain (RBD), and nucleoprotein (N) inferred from 3 spread-out dilutions correlated with those inferred from 8 consecutive dilutions with an R2 value of 0.97 or higher. We confirm existing findings showing a small proportion of pre-pandemic human serum samples contain cross-reactive antibodies to SARS-CoV-2 S1S2 and N, and that SARS-CoV-2 infection increases serum reactivity to the beta-HCoVs OC43 and HKU1 S1S2. In serial dilution assays, large savings in resources and/or increases in throughput can be achieved by reducing the number of dilutions measured and using Bayesian hierarchical modelling to infer inflection or endpoint titers. We have released software for conducting these types of analysis.
Assays using ELISA measurements on serially diluted serum samples have been heavily used to measure serum reactivity to SARS-CoV-2 antigens and are widely used in virology and elsewhere in biology. We test a method using Bayesian hierarchical modelling to reduce the workload of these assays and measure reactivity of SARS-CoV-2 and HCoV antigens to human serum samples collected before and during the COVID-19 pandemic. Inflection titers for SARS-CoV-2 full-length spike protein (S1S2), spike protein receptor-binding domain (RBD), and nucleoprotein (N) inferred from 3 spread-out dilutions correlated with those inferred from 8 consecutive dilutions with an R2 value of 0.97 or higher. We confirm existing findings showing a small proportion of pre-pandemic human serum samples contain cross-reactive antibodies to SARS-CoV-2 S1S2 and N, and that SARS-CoV-2 infection increases serum reactivity to the beta-HCoVs OC43 and HKU1 S1S2. In serial dilution assays, large savings in resources and/or increases in throughput can be achieved by reducing the number of dilutions measured and using Bayesian hierarchical modelling to infer inflection or endpoint titers. We have released software for conducting these types of analysis.Assays using ELISA measurements on serially diluted serum samples have been heavily used to measure serum reactivity to SARS-CoV-2 antigens and are widely used in virology and elsewhere in biology. We test a method using Bayesian hierarchical modelling to reduce the workload of these assays and measure reactivity of SARS-CoV-2 and HCoV antigens to human serum samples collected before and during the COVID-19 pandemic. Inflection titers for SARS-CoV-2 full-length spike protein (S1S2), spike protein receptor-binding domain (RBD), and nucleoprotein (N) inferred from 3 spread-out dilutions correlated with those inferred from 8 consecutive dilutions with an R2 value of 0.97 or higher. We confirm existing findings showing a small proportion of pre-pandemic human serum samples contain cross-reactive antibodies to SARS-CoV-2 S1S2 and N, and that SARS-CoV-2 infection increases serum reactivity to the beta-HCoVs OC43 and HKU1 S1S2. In serial dilution assays, large savings in resources and/or increases in throughput can be achieved by reducing the number of dilutions measured and using Bayesian hierarchical modelling to infer inflection or endpoint titers. We have released software for conducting these types of analysis.
Assays using ELISA measurements on serially diluted serum samples have been heavily used to measure serum reactivity to SARS-CoV-2 antigens and are widely used in virology and elsewhere in biology. We test a method using Bayesian hierarchical modelling to reduce the workload of these assays and measure reactivity of SARS-CoV-2 and HCoV antigens to human serum samples collected before and during the COVID-19 pandemic. Inflection titers for SARS-CoV-2 full-length spike protein (S1S2), spike protein receptor-binding domain (RBD), and nucleoprotein (N) inferred from 3 spread-out dilutions correlated with those inferred from 8 consecutive dilutions with an R 2 value of 0.97 or higher. We confirm existing findings showing a small proportion of pre-pandemic human serum samples contain cross-reactive antibodies to SARS-CoV-2 S1S2 and N, and that SARS-CoV-2 infection increases serum reactivity to the beta-HCoVs OC43 and HKU1 S1S2. In serial dilution assays, large savings in resources and/or increases in throughput can be achieved by reducing the number of dilutions measured and using Bayesian hierarchical modelling to infer inflection or endpoint titers. We have released software for conducting these types of analysis.
Author Gabriele Neumann
Peter Jester
Tomoyuki Uchida
Keiko Mitamura
Shiho Chiba
Yoshihiro Kawaoka
Lizheng Guan
Hongyu Rao
Nobuhiro Ikeda
Peter Halfmann
Kiyoko Iwatsuki-Horimoto
Seiya Yamayoshi
Masao Hagihara
Robert Presler
David Pattinson
AuthorAffiliation 1 Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, Madison, WI 53706, USA; david.pattinson@wisc.edu (D.P.); peter.jester@wisc.edu (P.J.); lizheng.guan@wisc.edu (L.G.); shiho.chiba@wisc.edu (S.C.); robert.presler@wisc.edu (R.P.); hongyu.rao@wisc.edu (H.R.); peter.halfmann@wisc.edu (P.H.); gabriele.neumann@wisc.edu (G.N.)
6 Division of Infection Control, Eiju General Hospital, Tokyo 104-0045, Japan; mitamurakeiko77@gmail.com
4 Department of General Internal Medicine, Eiju General Hospital, Tokyo 104-0045, Japan; n-ikeda@eijuhp.com
7 Department of Special Pathogens, International Research Center for Infectious Diseases, Institute of Medical Science, University of Tokyo, Tokyo 108-0071, Japan
3 The Research Center for Global Viral Diseases, Research Institute, National Center for Global Health and Medicine, Tokyo 162-8665, Japan
5 Department of Hematology, Eiju General Hospital, Tokyo 104-0045, Japan; hagihara@eijuhp.com (M.H.); i8i_i8i@hot
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Cites_doi 10.1016/j.tim.2016.03.003
10.1016/bs.aivir.2018.01.001
10.1038/s41591-020-0913-5
10.1093/infdis/jiab333
10.1016/j.eclinm.2021.100734
10.1128/JCM.00533-08
10.1016/j.mayocp.2020.05.032
10.1016/0022-1759(87)90289-4
10.1038/s41467-021-23074-3
10.1016/j.jcv.2007.08.007
10.1371/journal.pone.0146021
10.1097/INF.0000000000002660
10.7717/peerj-cs.55
10.1093/infdis/jiaa680
10.1016/S0929-6646(09)60066-8
10.3390/microorganisms8121993
10.1056/NEJMoa2001017
10.1101/2020.06.22.20137695
10.1016/S0022-1759(98)00170-7
10.1128/JCM.00636-10
10.1172/JCI146927
10.1016/j.jviromet.2015.02.014
10.1101/2020.10.10.20210070
10.1080/22221751.2021.1905488
10.1126/science.abd0826
10.1016/j.cell.2021.02.010
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Issue 3
Keywords SARS-CoV-2
HCoV-229E
HCoV-HKU1
HCoV-NL63
hierarchical modelling
inflection titer
endpoint assay
Bayesian analysis
ELISA
HCoV-OC43
Language English
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These authors contributed equally to this work.
Postal address: Influenza Research Institute, 575 Science Dr, Madison, WI 53711, USA.
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References Gaunt (ref_5) 2010; 48
Amanat (ref_21) 2020; 26
Hsieh (ref_22) 2020; 369
Karpinski (ref_25) 1987; 103
Corman (ref_7) 2018; 100
Zimmermann (ref_29) 2020; 39
ref_11
Rucinski (ref_18) 2020; 95
ref_30
ref_19
Frey (ref_20) 1998; 221
Henss (ref_13) 2021; 223
Shao (ref_26) 2007; 40
Yue (ref_8) 2020; 102
ref_15
Yamayoshi (ref_23) 2021; 32
Shrwani (ref_17) 2021; 224
Gao (ref_32) 2016; 115
Zhu (ref_1) 2020; 382
Su (ref_6) 2016; 24
Song (ref_16) 2021; 12
Dijkman (ref_27) 2008; 46
ref_3
ref_2
Westgeest (ref_31) 2015; 217
Anderson (ref_10) 2021; 184
Morgenlander (ref_14) 2021; 131
ref_9
Dijkman (ref_28) 2009; 108
ref_4
Guo (ref_12) 2021; 10
Salvatier (ref_24) 2016; 2
References_xml – volume: 24
  start-page: 490
  year: 2016
  ident: ref_6
  article-title: Epidemiology, Genetic Recombination, and Pathogenesis of Coronaviruses
  publication-title: Trends Microbiol.
  doi: 10.1016/j.tim.2016.03.003
– volume: 100
  start-page: 163
  year: 2018
  ident: ref_7
  article-title: Hosts and Sources of Endemic Human Coronaviruses
  publication-title: Adv. Virus Res.
  doi: 10.1016/bs.aivir.2018.01.001
– volume: 26
  start-page: 1033
  year: 2020
  ident: ref_21
  article-title: A serological assay to detect SARS-CoV-2 seroconversion in humans
  publication-title: Nat. Med.
  doi: 10.1038/s41591-020-0913-5
– ident: ref_30
– ident: ref_3
– volume: 224
  start-page: 1305
  year: 2021
  ident: ref_17
  article-title: Detection of serum cross-reactive antibodies and memory response to SARS-CoV-2 in pre-pandemic and post-COVID-19 convalescent samples
  publication-title: J. Infect. Dis.
  doi: 10.1093/infdis/jiab333
– volume: 32
  start-page: 100734
  year: 2021
  ident: ref_23
  article-title: Antibody titers against SARS-CoV-2 decline, but do not disappear for several months
  publication-title: EClinicalMedicine
  doi: 10.1016/j.eclinm.2021.100734
– volume: 46
  start-page: 2368
  year: 2008
  ident: ref_27
  article-title: Human coronavirus NL63 and 229E seroconversion in children
  publication-title: J. Clin. Microbiol.
  doi: 10.1128/JCM.00533-08
– volume: 102
  start-page: 557
  year: 2020
  ident: ref_8
  article-title: High prevalence of pre-existing serological cross-reactivity against severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) in sub-Saharan Africa
  publication-title: Int. J. Infect. Dis.
– volume: 95
  start-page: 1701
  year: 2020
  ident: ref_18
  article-title: Seasonality of Coronavirus 229E, HKU1, NL63, and OC43 from 2014 to 2020
  publication-title: Mayo Clin. Proc.
  doi: 10.1016/j.mayocp.2020.05.032
– volume: 115
  start-page: e54573
  year: 2016
  ident: ref_32
  article-title: Measuring Influenza Neuraminidase Inhibition Antibody Titers by Enzyme-linked Lectin Assay
  publication-title: J. Vis. Exp.
– volume: 103
  start-page: 189
  year: 1987
  ident: ref_25
  article-title: Statistical considerations in the quantitation of serum immunoglobulin levels using the enzyme-linked immunosorbent assay (ELISA)
  publication-title: J. Immunol. Methods
  doi: 10.1016/0022-1759(87)90289-4
– volume: 12
  start-page: 2938
  year: 2021
  ident: ref_16
  article-title: Cross-reactive serum and memory B-cell responses to spike protein in SARS-CoV-2 and endemic coronavirus infection
  publication-title: Nat. Commun.
  doi: 10.1038/s41467-021-23074-3
– volume: 40
  start-page: 207
  year: 2007
  ident: ref_26
  article-title: Seroepidemiology of group I human coronaviruses in children
  publication-title: J. Clin. Virol.
  doi: 10.1016/j.jcv.2007.08.007
– ident: ref_19
  doi: 10.1371/journal.pone.0146021
– volume: 39
  start-page: 355
  year: 2020
  ident: ref_29
  article-title: Coronavirus Infections in Children Including COVID-19: An Overview of the Epidemiology, Clinical Features, Diagnosis, Treatment and Prevention Options in Children
  publication-title: Pediatr. Infect. Dis. J.
  doi: 10.1097/INF.0000000000002660
– volume: 2
  start-page: e55
  year: 2016
  ident: ref_24
  article-title: Probabilistic programming in Python using PyMC3
  publication-title: PeerJ Comput. Sci.
  doi: 10.7717/peerj-cs.55
– volume: 223
  start-page: 56
  year: 2021
  ident: ref_13
  article-title: Analysis of Humoral Immune Responses in Patients with Severe Acute Respiratory Syndrome Coronavirus 2 Infection
  publication-title: J. Infect. Dis.
  doi: 10.1093/infdis/jiaa680
– volume: 108
  start-page: 270
  year: 2009
  ident: ref_28
  article-title: Human coronaviruses 229E and NL63: Close yet still so far
  publication-title: J. Formos. Med. Assoc.
  doi: 10.1016/S0929-6646(09)60066-8
– ident: ref_15
  doi: 10.3390/microorganisms8121993
– ident: ref_4
– volume: 382
  start-page: 727
  year: 2020
  ident: ref_1
  article-title: A Novel Coronavirus from Patients with Pneumonia in China, 2019
  publication-title: N. Engl. J. Med.
  doi: 10.1056/NEJMoa2001017
– ident: ref_9
  doi: 10.1101/2020.06.22.20137695
– ident: ref_2
– volume: 221
  start-page: 35
  year: 1998
  ident: ref_20
  article-title: A statistically defined endpoint titer determination method for immunoassays
  publication-title: J. Immunol. Methods
  doi: 10.1016/S0022-1759(98)00170-7
– volume: 48
  start-page: 2940
  year: 2010
  ident: ref_5
  article-title: Epidemiology and clinical presentations of the four human coronaviruses 229E, HKU1, NL63, and OC43 detected over 3 years using a novel multiplex real-time PCR method
  publication-title: J. Clin. Microbiol. Am. Soc. Microbiol.
  doi: 10.1128/JCM.00636-10
– volume: 131
  start-page: 1
  year: 2021
  ident: ref_14
  article-title: Antibody responses to endemic coronaviruses modulate COVID-19 convalescent plasma functionality
  publication-title: J. Clin. Investig.
  doi: 10.1172/JCI146927
– volume: 217
  start-page: 55
  year: 2015
  ident: ref_31
  article-title: Optimization of an enzyme-linked lectin assay suitable for rapid antigenic characterization of the neuraminidase of human influenza A(H3N2) viruses
  publication-title: J. Virol. Methods
  doi: 10.1016/j.jviromet.2015.02.014
– ident: ref_11
  doi: 10.1101/2020.10.10.20210070
– volume: 10
  start-page: 664
  year: 2021
  ident: ref_12
  article-title: Cross-reactive antibody against human coronavirus OC43 spike protein correlates with disease severity in COVID-19 patients: A retrospective study
  publication-title: Emerg. Microbes Infect.
  doi: 10.1080/22221751.2021.1905488
– volume: 369
  start-page: 1501
  year: 2020
  ident: ref_22
  article-title: Structure-based design of prefusion-stabilized SARS-CoV-2 spikes
  publication-title: Science
  doi: 10.1126/science.abd0826
– volume: 184
  start-page: 1858
  year: 2021
  ident: ref_10
  article-title: Seasonal human coronavirus antibodies are boosted upon SARS-CoV-2 infection but not associated with protection
  publication-title: Cell
  doi: 10.1016/j.cell.2021.02.010
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Snippet Assays using ELISA measurements on serially diluted serum samples have been heavily used to measure serum reactivity to SARS-CoV-2 antigens and are widely used...
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SubjectTerms Antibodies
Antibodies, Viral
Antigens
Bayes Theorem
Bayesian analysis
Bayesian theory
blood serum
computer software
Coronaviruses
COVID-19
COVID-19 - diagnosis
COVID-19 infection
Disease transmission
ELISA
Enzyme-Linked Immunosorbent Assay
HCoV-229E
HCoV-HKU1
HCoV-NL63
HCoV-OC43
Humans
Infections
Influenza
Laboratories
Microbiology
Middle East respiratory syndrome
nucleoproteins
Pandemics
QR1-502
Respiratory diseases
SARS-CoV-2
SARS-CoV-2; HCoV-OC43; HCoV-HKU1; HCoV-229E; HCoV-NL63; ELISA; Bayesian analysis; hierarchical modelling; endpoint assay; inflection titer
Seasons
Serology
Severe acute respiratory syndrome coronavirus 2
Spike protein
Standard deviation
virology
Workload
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Title A Novel Method to Reduce ELISA Serial Dilution Assay Workload Applied to SARS-CoV-2 and Seasonal HCoVs
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Volume 14
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