Accuracy of serological testing for SARS-CoV-2 antibodies: First results of a large mixed-method evaluation study.
Identifieur interne : 000826 ( Main/Exploration ); précédent : 000825; suivant : 000827Accuracy of serological testing for SARS-CoV-2 antibodies: First results of a large mixed-method evaluation study.
Auteurs : Daniel Brigger [Suisse] ; Michael P. Horn [Suisse] ; Luke F. Pennington [États-Unis] ; Abigail E. Powell [États-Unis] ; Denise Siegrist [Suisse] ; Benjamin Weber [Suisse] ; Olivier Engler [Suisse] ; Vanja Piezzi [Suisse] ; Lauro Damonti [Suisse] ; Patricia Iseli [Suisse] ; Christoph Hauser [Suisse] ; Tanja K. Froehlich [Suisse] ; Peter M. Villiger [Suisse] ; Martin F. Bachmann [Suisse] ; Stephen L. Leib [Suisse] ; Pascal Bittel [Suisse] ; Martin Fiedler [Suisse] ; Carlo R. Largiadèr [Suisse] ; Jonas Marschall [Suisse] ; Hanspeter Stalder [Suisse] ; Peter S. Kim [États-Unis] ; Theodore S. Jardetzky [États-Unis] ; Alexander Eggel [Suisse] ; Michael Nagler [Suisse]Source :
- Allergy [ 1398-9995 ] ; 2020.
Abstract
BACKGROUND
Serological immunoassays that can identify protective immunity against SARS-CoV-2 are needed to adapt quarantine measures, assess vaccination responses, and evaluate donor plasma. To date, however, the utility of such immunoassays remains unclear. In a mixed-design evaluation study, we compared the diagnostic accuracy of serological immunoassays that are based on various SARS-CoV-2 proteins and assessed the neutralizing activity of antibodies in patient sera.
METHODS
Consecutive patients admitted with confirmed SARS-CoV-2 infection were prospectively followed alongside medical staff and biobank samples from winter 2018/2019. An in-house enzyme-linked immunosorbent assay utilizing recombinant receptor-binding domain (RBD) of the SARS-CoV-2 spike protein was developed and compared to three commercially available enzyme-linked immunosorbent assays (ELISAs) targeting the nucleoprotein (N), the S1 domain of the spike protein (S1), and a lateral flow immunoassay (LFI) based on full-length spike protein. Neutralization assays with live SARS-CoV-2 were performed.
RESULTS
One thousand four hundred and seventy-seven individuals were included comprising 112 SARS-CoV-2 positives (defined as a positive real-time PCR result; prevalence 7.6%). IgG seroconversion occurred between day 0 and day 21. While the ELISAs showed sensitivities of 88.4% for RBD, 89.3% for S1, and 72.9% for N protein, the specificity was above 94% for all tests. Out of 54 SARS-CoV-2 positive individuals, 96.3% showed full neutralization of live SARS-CoV-2 at serum dilutions ≥ 1:16, while none of the 6 SARS-CoV-2-negative sera revealed neutralizing activity.
CONCLUSIONS
ELISAs targeting RBD and S1 protein of SARS-CoV-2 are promising immunoassays which shall be further evaluated in studies verifying diagnostic accuracy and protective immunity against SARS-CoV-2.
DOI: 10.1111/all.14608
PubMed: 32997812
PubMed Central: PMC7537154
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Froehlich</name><affiliation wicri:level="3"><nlm:affiliation>University Institute of Clinical Chemistry, Inselspital University Hospital, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>University Institute of Clinical Chemistry, Inselspital University Hospital, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName></affiliation></author><author><name sortKey="Villiger, Peter M" sort="Villiger, Peter M" uniqKey="Villiger P" first="Peter M" last="Villiger">Peter M. Villiger</name><affiliation wicri:level="3"><nlm:affiliation>Department of Rheumatology, Immunology, and Allergology, Inselspital University Hospital, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of Rheumatology, Immunology, and Allergology, Inselspital University Hospital, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName></affiliation></author><author><name sortKey="Bachmann, Martin F" sort="Bachmann, Martin F" uniqKey="Bachmann M" first="Martin F" last="Bachmann">Martin F. Bachmann</name><affiliation wicri:level="3"><nlm:affiliation>Department of Rheumatology, Immunology, and Allergology, Inselspital University Hospital, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of Rheumatology, Immunology, and Allergology, Inselspital University Hospital, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName></affiliation><affiliation wicri:level="4"><nlm:affiliation>Department of BioMedical Research, University of Bern, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of BioMedical Research, University of Bern, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName><orgName type="university">Université de Berne</orgName></affiliation></author><author><name sortKey="Leib, Stephen L" sort="Leib, Stephen L" uniqKey="Leib S" first="Stephen L" last="Leib">Stephen L. Leib</name><affiliation wicri:level="4"><nlm:affiliation>Institute for Infectious Diseases, University of Bern, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Institute for Infectious Diseases, University of Bern, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName><orgName type="university">Université de Berne</orgName></affiliation></author><author><name sortKey="Bittel, Pascal" sort="Bittel, Pascal" uniqKey="Bittel P" first="Pascal" last="Bittel">Pascal Bittel</name><affiliation wicri:level="4"><nlm:affiliation>Institute for Infectious Diseases, University of Bern, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Institute for Infectious Diseases, University of Bern, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName><orgName type="university">Université de Berne</orgName></affiliation></author><author><name sortKey="Fiedler, Martin" sort="Fiedler, Martin" uniqKey="Fiedler M" first="Martin" last="Fiedler">Martin Fiedler</name><affiliation wicri:level="3"><nlm:affiliation>University Institute of Clinical Chemistry, Inselspital University Hospital, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>University Institute of Clinical Chemistry, Inselspital University Hospital, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName></affiliation></author><author><name sortKey="Largiader, Carlo R" sort="Largiader, Carlo R" uniqKey="Largiader C" first="Carlo R" last="Largiadèr">Carlo R. Largiadèr</name><affiliation wicri:level="3"><nlm:affiliation>University Institute of Clinical Chemistry, Inselspital University Hospital, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>University Institute of Clinical Chemistry, Inselspital University Hospital, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName></affiliation></author><author><name sortKey="Marschall, Jonas" sort="Marschall, Jonas" uniqKey="Marschall J" first="Jonas" last="Marschall">Jonas Marschall</name><affiliation wicri:level="3"><nlm:affiliation>Department of Infectious Diseases, Bern University Hospital, University of Bern, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of Infectious Diseases, Bern University Hospital, University of Bern, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName></affiliation></author><author><name sortKey="Stalder, Hanspeter" sort="Stalder, Hanspeter" uniqKey="Stalder H" first="Hanspeter" last="Stalder">Hanspeter Stalder</name><affiliation wicri:level="4"><nlm:affiliation>Vetsuisse Faculty, Institute of Virology and Immunology, University of Bern, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Vetsuisse Faculty, Institute of Virology and Immunology, University of Bern, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName><orgName type="university">Université de Berne</orgName></affiliation></author><author><name sortKey="Kim, Peter S" sort="Kim, Peter S" uniqKey="Kim P" first="Peter S" last="Kim">Peter S. Kim</name><affiliation wicri:level="2"><nlm:affiliation>Standford Chem-H and Department of Biochemistry, Stanford University School of Medicine, Stanford, CA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Standford Chem-H and Department of Biochemistry, Stanford University School of Medicine, Stanford, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation><affiliation wicri:level="2"><nlm:affiliation>Chan Zuckerberg Biohub, San Francisco, CA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Chan Zuckerberg Biohub, San Francisco, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Jardetzky, Theodore S" sort="Jardetzky, Theodore S" uniqKey="Jardetzky T" first="Theodore S" last="Jardetzky">Theodore S. Jardetzky</name><affiliation wicri:level="2"><nlm:affiliation>Department of Structural Biology, Stanford University School of Medicine, Stanford, CA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Structural Biology, Stanford University School of Medicine, Stanford, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Eggel, Alexander" sort="Eggel, Alexander" uniqKey="Eggel A" first="Alexander" last="Eggel">Alexander Eggel</name><affiliation wicri:level="3"><nlm:affiliation>Department of Rheumatology, Immunology, and Allergology, Inselspital University Hospital, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of Rheumatology, Immunology, and Allergology, Inselspital University Hospital, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName></affiliation><affiliation wicri:level="4"><nlm:affiliation>Department of BioMedical Research, University of Bern, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of BioMedical Research, University of Bern, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName><orgName type="university">Université de Berne</orgName></affiliation></author><author><name sortKey="Nagler, Michael" sort="Nagler, Michael" uniqKey="Nagler M" first="Michael" last="Nagler">Michael Nagler</name><affiliation wicri:level="3"><nlm:affiliation>University Institute of Clinical Chemistry, Inselspital University Hospital, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>University Institute of Clinical Chemistry, Inselspital University Hospital, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno type="RBID">pubmed:32997812</idno><idno type="pmid">32997812</idno><idno type="doi">10.1111/all.14608</idno><idno type="pmc">PMC7537154</idno><idno type="wicri:Area/Main/Corpus">000280</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000280</idno><idno type="wicri:Area/Main/Curation">000280</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Curation">000280</idno><idno type="wicri:Area/Main/Exploration">000280</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Accuracy of serological testing for SARS-CoV-2 antibodies: First results of a large mixed-method evaluation study.</title><author><name sortKey="Brigger, Daniel" sort="Brigger, Daniel" uniqKey="Brigger D" first="Daniel" last="Brigger">Daniel Brigger</name><affiliation wicri:level="3"><nlm:affiliation>Department of Rheumatology, Immunology, and Allergology, Inselspital University Hospital, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of Rheumatology, Immunology, and Allergology, Inselspital University Hospital, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName></affiliation><affiliation wicri:level="4"><nlm:affiliation>Department of BioMedical Research, University of Bern, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of BioMedical Research, University of Bern, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName><orgName type="university">Université de Berne</orgName></affiliation></author><author><name sortKey="Horn, Michael P" sort="Horn, Michael P" uniqKey="Horn M" first="Michael P" last="Horn">Michael P. Horn</name><affiliation wicri:level="3"><nlm:affiliation>University Institute of Clinical Chemistry, Inselspital University Hospital, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>University Institute of Clinical Chemistry, Inselspital University Hospital, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName></affiliation></author><author><name sortKey="Pennington, Luke F" sort="Pennington, Luke F" uniqKey="Pennington L" first="Luke F" last="Pennington">Luke F. Pennington</name><affiliation wicri:level="2"><nlm:affiliation>Department of Structural Biology, Stanford University School of Medicine, Stanford, CA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Structural Biology, Stanford University School of Medicine, Stanford, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Powell, Abigail E" sort="Powell, Abigail E" uniqKey="Powell A" first="Abigail E" last="Powell">Abigail E. Powell</name><affiliation wicri:level="2"><nlm:affiliation>Standford Chem-H and Department of Biochemistry, Stanford University School of Medicine, Stanford, CA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Standford Chem-H and Department of Biochemistry, Stanford University School of Medicine, Stanford, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation><affiliation wicri:level="2"><nlm:affiliation>Chan Zuckerberg Biohub, San Francisco, CA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Chan Zuckerberg Biohub, San Francisco, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Siegrist, Denise" sort="Siegrist, Denise" uniqKey="Siegrist D" first="Denise" last="Siegrist">Denise Siegrist</name><affiliation wicri:level="1"><nlm:affiliation>Spiez Laboratory, Federal Office for Civil Protection, Spiez, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Spiez Laboratory, Federal Office for Civil Protection, Spiez</wicri:regionArea><wicri:noRegion>Spiez</wicri:noRegion></affiliation></author><author><name sortKey="Weber, Benjamin" sort="Weber, Benjamin" uniqKey="Weber B" first="Benjamin" last="Weber">Benjamin Weber</name><affiliation wicri:level="1"><nlm:affiliation>Spiez Laboratory, Federal Office for Civil Protection, Spiez, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Spiez Laboratory, Federal Office for Civil Protection, Spiez</wicri:regionArea><wicri:noRegion>Spiez</wicri:noRegion></affiliation></author><author><name sortKey="Engler, Olivier" sort="Engler, Olivier" uniqKey="Engler O" first="Olivier" last="Engler">Olivier Engler</name><affiliation wicri:level="1"><nlm:affiliation>Spiez Laboratory, Federal Office for Civil Protection, Spiez, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Spiez Laboratory, Federal Office for Civil Protection, Spiez</wicri:regionArea><wicri:noRegion>Spiez</wicri:noRegion></affiliation></author><author><name sortKey="Piezzi, Vanja" sort="Piezzi, Vanja" uniqKey="Piezzi V" first="Vanja" last="Piezzi">Vanja Piezzi</name><affiliation wicri:level="3"><nlm:affiliation>Department of Infectious Diseases, Bern University Hospital, University of Bern, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of Infectious Diseases, Bern University Hospital, University of Bern, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName></affiliation></author><author><name sortKey="Damonti, Lauro" sort="Damonti, Lauro" uniqKey="Damonti L" first="Lauro" last="Damonti">Lauro Damonti</name><affiliation wicri:level="3"><nlm:affiliation>Department of Infectious Diseases, Bern University Hospital, University of Bern, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of Infectious Diseases, Bern University Hospital, University of Bern, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName></affiliation></author><author><name sortKey="Iseli, Patricia" sort="Iseli, Patricia" uniqKey="Iseli P" first="Patricia" last="Iseli">Patricia Iseli</name><affiliation wicri:level="3"><nlm:affiliation>Occupational Medicine, Inselspital University Hospital, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Occupational Medicine, Inselspital University Hospital, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName></affiliation></author><author><name sortKey="Hauser, Christoph" sort="Hauser, Christoph" uniqKey="Hauser C" first="Christoph" last="Hauser">Christoph Hauser</name><affiliation wicri:level="3"><nlm:affiliation>Department of Infectious Diseases, Bern University Hospital, University of Bern, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of Infectious Diseases, Bern University Hospital, University of Bern, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName></affiliation></author><author><name sortKey="Froehlich, Tanja K" sort="Froehlich, Tanja K" uniqKey="Froehlich T" first="Tanja K" last="Froehlich">Tanja K. Froehlich</name><affiliation wicri:level="3"><nlm:affiliation>University Institute of Clinical Chemistry, Inselspital University Hospital, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>University Institute of Clinical Chemistry, Inselspital University Hospital, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName></affiliation></author><author><name sortKey="Villiger, Peter M" sort="Villiger, Peter M" uniqKey="Villiger P" first="Peter M" last="Villiger">Peter M. Villiger</name><affiliation wicri:level="3"><nlm:affiliation>Department of Rheumatology, Immunology, and Allergology, Inselspital University Hospital, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of Rheumatology, Immunology, and Allergology, Inselspital University Hospital, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName></affiliation></author><author><name sortKey="Bachmann, Martin F" sort="Bachmann, Martin F" uniqKey="Bachmann M" first="Martin F" last="Bachmann">Martin F. Bachmann</name><affiliation wicri:level="3"><nlm:affiliation>Department of Rheumatology, Immunology, and Allergology, Inselspital University Hospital, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of Rheumatology, Immunology, and Allergology, Inselspital University Hospital, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName></affiliation><affiliation wicri:level="4"><nlm:affiliation>Department of BioMedical Research, University of Bern, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of BioMedical Research, University of Bern, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName><orgName type="university">Université de Berne</orgName></affiliation></author><author><name sortKey="Leib, Stephen L" sort="Leib, Stephen L" uniqKey="Leib S" first="Stephen L" last="Leib">Stephen L. Leib</name><affiliation wicri:level="4"><nlm:affiliation>Institute for Infectious Diseases, University of Bern, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Institute for Infectious Diseases, University of Bern, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName><orgName type="university">Université de Berne</orgName></affiliation></author><author><name sortKey="Bittel, Pascal" sort="Bittel, Pascal" uniqKey="Bittel P" first="Pascal" last="Bittel">Pascal Bittel</name><affiliation wicri:level="4"><nlm:affiliation>Institute for Infectious Diseases, University of Bern, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Institute for Infectious Diseases, University of Bern, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName><orgName type="university">Université de Berne</orgName></affiliation></author><author><name sortKey="Fiedler, Martin" sort="Fiedler, Martin" uniqKey="Fiedler M" first="Martin" last="Fiedler">Martin Fiedler</name><affiliation wicri:level="3"><nlm:affiliation>University Institute of Clinical Chemistry, Inselspital University Hospital, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>University Institute of Clinical Chemistry, Inselspital University Hospital, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName></affiliation></author><author><name sortKey="Largiader, Carlo R" sort="Largiader, Carlo R" uniqKey="Largiader C" first="Carlo R" last="Largiadèr">Carlo R. Largiadèr</name><affiliation wicri:level="3"><nlm:affiliation>University Institute of Clinical Chemistry, Inselspital University Hospital, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>University Institute of Clinical Chemistry, Inselspital University Hospital, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName></affiliation></author><author><name sortKey="Marschall, Jonas" sort="Marschall, Jonas" uniqKey="Marschall J" first="Jonas" last="Marschall">Jonas Marschall</name><affiliation wicri:level="3"><nlm:affiliation>Department of Infectious Diseases, Bern University Hospital, University of Bern, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of Infectious Diseases, Bern University Hospital, University of Bern, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName></affiliation></author><author><name sortKey="Stalder, Hanspeter" sort="Stalder, Hanspeter" uniqKey="Stalder H" first="Hanspeter" last="Stalder">Hanspeter Stalder</name><affiliation wicri:level="4"><nlm:affiliation>Vetsuisse Faculty, Institute of Virology and Immunology, University of Bern, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Vetsuisse Faculty, Institute of Virology and Immunology, University of Bern, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName><orgName type="university">Université de Berne</orgName></affiliation></author><author><name sortKey="Kim, Peter S" sort="Kim, Peter S" uniqKey="Kim P" first="Peter S" last="Kim">Peter S. Kim</name><affiliation wicri:level="2"><nlm:affiliation>Standford Chem-H and Department of Biochemistry, Stanford University School of Medicine, Stanford, CA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Standford Chem-H and Department of Biochemistry, Stanford University School of Medicine, Stanford, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation><affiliation wicri:level="2"><nlm:affiliation>Chan Zuckerberg Biohub, San Francisco, CA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Chan Zuckerberg Biohub, San Francisco, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Jardetzky, Theodore S" sort="Jardetzky, Theodore S" uniqKey="Jardetzky T" first="Theodore S" last="Jardetzky">Theodore S. Jardetzky</name><affiliation wicri:level="2"><nlm:affiliation>Department of Structural Biology, Stanford University School of Medicine, Stanford, CA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Structural Biology, Stanford University School of Medicine, Stanford, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Eggel, Alexander" sort="Eggel, Alexander" uniqKey="Eggel A" first="Alexander" last="Eggel">Alexander Eggel</name><affiliation wicri:level="3"><nlm:affiliation>Department of Rheumatology, Immunology, and Allergology, Inselspital University Hospital, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of Rheumatology, Immunology, and Allergology, Inselspital University Hospital, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName></affiliation><affiliation wicri:level="4"><nlm:affiliation>Department of BioMedical Research, University of Bern, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of BioMedical Research, University of Bern, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName><orgName type="university">Université de Berne</orgName></affiliation></author><author><name sortKey="Nagler, Michael" sort="Nagler, Michael" uniqKey="Nagler M" first="Michael" last="Nagler">Michael Nagler</name><affiliation wicri:level="3"><nlm:affiliation>University Institute of Clinical Chemistry, Inselspital University Hospital, Bern, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>University Institute of Clinical Chemistry, Inselspital University Hospital, Bern</wicri:regionArea><placeName><settlement type="city">Berne</settlement><region type="région" nuts="3">Canton de Berne</region></placeName></affiliation></author></analytic><series><title level="j">Allergy</title><idno type="eISSN">1398-9995</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p><b>BACKGROUND</b></p><p>Serological immunoassays that can identify protective immunity against SARS-CoV-2 are needed to adapt quarantine measures, assess vaccination responses, and evaluate donor plasma. To date, however, the utility of such immunoassays remains unclear. In a mixed-design evaluation study, we compared the diagnostic accuracy of serological immunoassays that are based on various SARS-CoV-2 proteins and assessed the neutralizing activity of antibodies in patient sera.</p></div><div type="abstract" xml:lang="en"><p><b>METHODS</b></p><p>Consecutive patients admitted with confirmed SARS-CoV-2 infection were prospectively followed alongside medical staff and biobank samples from winter 2018/2019. An in-house enzyme-linked immunosorbent assay utilizing recombinant receptor-binding domain (RBD) of the SARS-CoV-2 spike protein was developed and compared to three commercially available enzyme-linked immunosorbent assays (ELISAs) targeting the nucleoprotein (N), the S1 domain of the spike protein (S1), and a lateral flow immunoassay (LFI) based on full-length spike protein. Neutralization assays with live SARS-CoV-2 were performed.</p></div><div type="abstract" xml:lang="en"><p><b>RESULTS</b></p><p>One thousand four hundred and seventy-seven individuals were included comprising 112 SARS-CoV-2 positives (defined as a positive real-time PCR result; prevalence 7.6%). IgG seroconversion occurred between day 0 and day 21. While the ELISAs showed sensitivities of 88.4% for RBD, 89.3% for S1, and 72.9% for N protein, the specificity was above 94% for all tests. Out of 54 SARS-CoV-2 positive individuals, 96.3% showed full neutralization of live SARS-CoV-2 at serum dilutions ≥ 1:16, while none of the 6 SARS-CoV-2-negative sera revealed neutralizing activity.</p></div><div type="abstract" xml:lang="en"><p><b>CONCLUSIONS</b></p><p>ELISAs targeting RBD and S1 protein of SARS-CoV-2 are promising immunoassays which shall be further evaluated in studies verifying diagnostic accuracy and protective immunity against SARS-CoV-2.</p></div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">32997812</PMID><DateRevised><Year>2020</Year><Month>11</Month><Day>13</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1398-9995</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2020</Year><Month>Sep</Month><Day>30</Day></PubDate></JournalIssue><Title>Allergy</Title><ISOAbbreviation>Allergy</ISOAbbreviation></Journal><ArticleTitle>Accuracy of serological testing for SARS-CoV-2 antibodies: First results of a large mixed-method evaluation study.</ArticleTitle><ELocationID EIdType="doi" ValidYN="Y">10.1111/all.14608</ELocationID><Abstract><AbstractText Label="BACKGROUND" NlmCategory="BACKGROUND">Serological immunoassays that can identify protective immunity against SARS-CoV-2 are needed to adapt quarantine measures, assess vaccination responses, and evaluate donor plasma. To date, however, the utility of such immunoassays remains unclear. In a mixed-design evaluation study, we compared the diagnostic accuracy of serological immunoassays that are based on various SARS-CoV-2 proteins and assessed the neutralizing activity of antibodies in patient sera.</AbstractText><AbstractText Label="METHODS" NlmCategory="METHODS">Consecutive patients admitted with confirmed SARS-CoV-2 infection were prospectively followed alongside medical staff and biobank samples from winter 2018/2019. An in-house enzyme-linked immunosorbent assay utilizing recombinant receptor-binding domain (RBD) of the SARS-CoV-2 spike protein was developed and compared to three commercially available enzyme-linked immunosorbent assays (ELISAs) targeting the nucleoprotein (N), the S1 domain of the spike protein (S1), and a lateral flow immunoassay (LFI) based on full-length spike protein. Neutralization assays with live SARS-CoV-2 were performed.</AbstractText><AbstractText Label="RESULTS" NlmCategory="RESULTS">One thousand four hundred and seventy-seven individuals were included comprising 112 SARS-CoV-2 positives (defined as a positive real-time PCR result; prevalence 7.6%). IgG seroconversion occurred between day 0 and day 21. While the ELISAs showed sensitivities of 88.4% for RBD, 89.3% for S1, and 72.9% for N protein, the specificity was above 94% for all tests. Out of 54 SARS-CoV-2 positive individuals, 96.3% showed full neutralization of live SARS-CoV-2 at serum dilutions ≥ 1:16, while none of the 6 SARS-CoV-2-negative sera revealed neutralizing activity.</AbstractText><AbstractText Label="CONCLUSIONS" NlmCategory="CONCLUSIONS">ELISAs targeting RBD and S1 protein of SARS-CoV-2 are promising immunoassays which shall be further evaluated in studies verifying diagnostic accuracy and protective immunity against SARS-CoV-2.</AbstractText><CopyrightInformation>© 2020 The Authors. Allergy published by European Academy of Allergy and Clinical Immunology and John Wiley & Sons Ltd.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Brigger</LastName><ForeName>Daniel</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Department of Rheumatology, Immunology, and Allergology, Inselspital University Hospital, Bern, Switzerland.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of BioMedical Research, University of Bern, Bern, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Horn</LastName><ForeName>Michael P</ForeName><Initials>MP</Initials><AffiliationInfo><Affiliation>University Institute of Clinical Chemistry, Inselspital University Hospital, Bern, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pennington</LastName><ForeName>Luke F</ForeName><Initials>LF</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-7947-8714</Identifier><AffiliationInfo><Affiliation>Department of Structural Biology, Stanford University School of Medicine, Stanford, CA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Powell</LastName><ForeName>Abigail E</ForeName><Initials>AE</Initials><AffiliationInfo><Affiliation>Standford Chem-H and Department of Biochemistry, Stanford University School of Medicine, Stanford, CA, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Chan Zuckerberg Biohub, San Francisco, CA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Siegrist</LastName><ForeName>Denise</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Spiez Laboratory, Federal Office for Civil Protection, Spiez, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Weber</LastName><ForeName>Benjamin</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>Spiez Laboratory, Federal Office for Civil Protection, Spiez, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Engler</LastName><ForeName>Olivier</ForeName><Initials>O</Initials><AffiliationInfo><Affiliation>Spiez Laboratory, Federal Office for Civil Protection, Spiez, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Piezzi</LastName><ForeName>Vanja</ForeName><Initials>V</Initials><AffiliationInfo><Affiliation>Department of Infectious Diseases, Bern University Hospital, University of Bern, Bern, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Damonti</LastName><ForeName>Lauro</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Department of Infectious Diseases, Bern University Hospital, University of Bern, Bern, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Iseli</LastName><ForeName>Patricia</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Occupational Medicine, Inselspital University Hospital, Bern, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hauser</LastName><ForeName>Christoph</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Department of Infectious Diseases, Bern University Hospital, University of Bern, Bern, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Froehlich</LastName><ForeName>Tanja K</ForeName><Initials>TK</Initials><AffiliationInfo><Affiliation>University Institute of Clinical Chemistry, Inselspital University Hospital, Bern, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Villiger</LastName><ForeName>Peter M</ForeName><Initials>PM</Initials><AffiliationInfo><Affiliation>Department of Rheumatology, Immunology, and Allergology, Inselspital University Hospital, Bern, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bachmann</LastName><ForeName>Martin F</ForeName><Initials>MF</Initials><Identifier Source="ORCID">https://orcid.org/0000-0003-4370-2099</Identifier><AffiliationInfo><Affiliation>Department of Rheumatology, Immunology, and Allergology, Inselspital University Hospital, Bern, Switzerland.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of BioMedical Research, University of Bern, Bern, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Leib</LastName><ForeName>Stephen L</ForeName><Initials>SL</Initials><AffiliationInfo><Affiliation>Institute for Infectious Diseases, University of Bern, Bern, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bittel</LastName><ForeName>Pascal</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Institute for Infectious Diseases, University of Bern, Bern, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Fiedler</LastName><ForeName>Martin</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>University Institute of Clinical Chemistry, Inselspital University Hospital, Bern, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Largiadèr</LastName><ForeName>Carlo R</ForeName><Initials>CR</Initials><AffiliationInfo><Affiliation>University Institute of Clinical Chemistry, Inselspital University Hospital, Bern, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Marschall</LastName><ForeName>Jonas</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Infectious Diseases, Bern University Hospital, University of Bern, Bern, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Stalder</LastName><ForeName>Hanspeter</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Vetsuisse Faculty, Institute of Virology and Immunology, University of Bern, Bern, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kim</LastName><ForeName>Peter S</ForeName><Initials>PS</Initials><AffiliationInfo><Affiliation>Standford Chem-H and Department of Biochemistry, Stanford University School of Medicine, Stanford, CA, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Chan Zuckerberg Biohub, San Francisco, CA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jardetzky</LastName><ForeName>Theodore S</ForeName><Initials>TS</Initials><AffiliationInfo><Affiliation>Department of Structural Biology, Stanford University School of Medicine, Stanford, CA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Eggel</LastName><ForeName>Alexander</ForeName><Initials>A</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-8746-3339</Identifier><AffiliationInfo><Affiliation>Department of Rheumatology, Immunology, and Allergology, Inselspital University Hospital, Bern, Switzerland.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of BioMedical Research, University of Bern, Bern, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nagler</LastName><ForeName>Michael</ForeName><Initials>M</Initials><Identifier Source="ORCID">https://orcid.org/0000-0003-4319-2367</Identifier><AffiliationInfo><Affiliation>University Institute of Clinical Chemistry, Inselspital University Hospital, Bern, Switzerland.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><Agency>Research Fund of the Swiss Lung Association, Bern and the Uniscientia foundation</Agency><Country></Country></Grant><Grant><GrantID>179334</GrantID><Agency>Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>09</Month><Day>30</Day></ArticleDate></Article><MedlineJournalInfo><Country>Denmark</Country><MedlineTA>Allergy</MedlineTA><NlmUniqueID>7804028</NlmUniqueID><ISSNLinking>0105-4538</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Antibodies</Keyword><Keyword MajorTopicYN="N">COVID-19 [Supplementary Concept]</Keyword><Keyword MajorTopicYN="N">COVID-19 diagnostic testing [Supplementary Concept]</Keyword><Keyword MajorTopicYN="N">Enzyme-Linked Immunosorbent Assay [Mesh]</Keyword><Keyword MajorTopicYN="N">Neutralizing [Mesh]</Keyword><Keyword MajorTopicYN="N">Severe Acute Respiratory Syndrome Coronavirus 2 [Supplementary Concept]</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>08</Month><Day>03</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>09</Month><Day>11</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>09</Month><Day>13</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>10</Month><Day>1</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>10</Month><Day>1</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>9</Month><Day>30</Day><Hour>17</Hour><Minute>12</Minute></PubMedPubDate></History><PublicationStatus>aheadofprint</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32997812</ArticleId><ArticleId IdType="doi">10.1111/all.14608</ArticleId><ArticleId IdType="pmc">PMC7537154</ArticleId></ArticleIdList><ReferenceList><Title>REFERENCES</Title><Reference><Citation>Krammer F, Simon V. 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Emerg Infect Dis. 2020;26:10.</Citation></Reference></ReferenceList></PubmedData></pubmed><affiliations><list><country><li>Suisse</li><li>États-Unis</li></country><region><li>Californie</li><li>Canton de Berne</li></region><settlement><li>Berne</li></settlement><orgName><li>Université de Berne</li></orgName></list><tree><country name="Suisse"><region name="Canton de Berne"><name sortKey="Brigger, Daniel" sort="Brigger, Daniel" uniqKey="Brigger D" first="Daniel" last="Brigger">Daniel Brigger</name></region><name sortKey="Bachmann, Martin F" sort="Bachmann, Martin F" uniqKey="Bachmann M" first="Martin F" last="Bachmann">Martin F. Bachmann</name><name sortKey="Bachmann, Martin F" sort="Bachmann, Martin F" uniqKey="Bachmann M" first="Martin F" last="Bachmann">Martin F. 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Froehlich</name><name sortKey="Hauser, Christoph" sort="Hauser, Christoph" uniqKey="Hauser C" first="Christoph" last="Hauser">Christoph Hauser</name><name sortKey="Horn, Michael P" sort="Horn, Michael P" uniqKey="Horn M" first="Michael P" last="Horn">Michael P. Horn</name><name sortKey="Iseli, Patricia" sort="Iseli, Patricia" uniqKey="Iseli P" first="Patricia" last="Iseli">Patricia Iseli</name><name sortKey="Largiader, Carlo R" sort="Largiader, Carlo R" uniqKey="Largiader C" first="Carlo R" last="Largiadèr">Carlo R. Largiadèr</name><name sortKey="Leib, Stephen L" sort="Leib, Stephen L" uniqKey="Leib S" first="Stephen L" last="Leib">Stephen L. Leib</name><name sortKey="Marschall, Jonas" sort="Marschall, Jonas" uniqKey="Marschall J" first="Jonas" last="Marschall">Jonas Marschall</name><name sortKey="Nagler, Michael" sort="Nagler, Michael" uniqKey="Nagler M" first="Michael" last="Nagler">Michael Nagler</name><name sortKey="Piezzi, Vanja" sort="Piezzi, Vanja" uniqKey="Piezzi V" first="Vanja" last="Piezzi">Vanja Piezzi</name><name sortKey="Siegrist, Denise" sort="Siegrist, Denise" uniqKey="Siegrist D" first="Denise" last="Siegrist">Denise Siegrist</name><name sortKey="Stalder, Hanspeter" sort="Stalder, Hanspeter" uniqKey="Stalder H" first="Hanspeter" last="Stalder">Hanspeter Stalder</name><name sortKey="Villiger, Peter M" sort="Villiger, Peter M" uniqKey="Villiger P" first="Peter M" last="Villiger">Peter M. Villiger</name><name sortKey="Weber, Benjamin" sort="Weber, Benjamin" uniqKey="Weber B" first="Benjamin" last="Weber">Benjamin Weber</name></country><country name="États-Unis"><region name="Californie"><name sortKey="Pennington, Luke F" sort="Pennington, Luke F" uniqKey="Pennington L" first="Luke F" last="Pennington">Luke F. Pennington</name></region><name sortKey="Jardetzky, Theodore S" sort="Jardetzky, Theodore S" uniqKey="Jardetzky T" first="Theodore S" last="Jardetzky">Theodore S. Jardetzky</name><name sortKey="Kim, Peter S" sort="Kim, Peter S" uniqKey="Kim P" first="Peter S" last="Kim">Peter S. Kim</name><name sortKey="Kim, Peter S" sort="Kim, Peter S" uniqKey="Kim P" first="Peter S" last="Kim">Peter S. Kim</name><name sortKey="Powell, Abigail E" sort="Powell, Abigail E" uniqKey="Powell A" first="Abigail E" last="Powell">Abigail E. Powell</name><name sortKey="Powell, Abigail E" sort="Powell, Abigail E" uniqKey="Powell A" first="Abigail E" last="Powell">Abigail E. 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