Comparative analysis of SARS-CoV-2 neutralization titers reveals consistency between human and animal model serum and across assays
The evolution of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) requires ongoing monitoring to judge the ability of newly arising variants to escape the immune response. A surveillance system necessitates an understanding of differences in neutralization titers measured in different as...
Saved in:
Published in | Science translational medicine Vol. 16; no. 747; p. eadl1722 |
---|---|
Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
15.05.2024
|
Subjects | |
Online Access | Get more information |
Cover
Loading…
Abstract | The evolution of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) requires ongoing monitoring to judge the ability of newly arising variants to escape the immune response. A surveillance system necessitates an understanding of differences in neutralization titers measured in different assays and using human and animal serum samples. We compared 18 datasets generated using human, hamster, and mouse serum and six different neutralization assays. Datasets using animal model serum samples showed higher titer magnitudes than datasets using human serum samples in this comparison. Fold change in neutralization of variants compared to ancestral SARS-CoV-2, immunodominance patterns, and antigenic maps were similar among serum samples and assays. Most assays yielded consistent results, except for differences in fold change in cytopathic effect assays. Hamster serum samples were a consistent surrogate for human first-infection serum samples. These results inform the transition of surveillance of SARS-CoV-2 antigenic variation from dependence on human first-infection serum samples to the utilization of serum samples from animal models. |
---|---|
AbstractList | The evolution of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) requires ongoing monitoring to judge the ability of newly arising variants to escape the immune response. A surveillance system necessitates an understanding of differences in neutralization titers measured in different assays and using human and animal serum samples. We compared 18 datasets generated using human, hamster, and mouse serum and six different neutralization assays. Datasets using animal model serum samples showed higher titer magnitudes than datasets using human serum samples in this comparison. Fold change in neutralization of variants compared to ancestral SARS-CoV-2, immunodominance patterns, and antigenic maps were similar among serum samples and assays. Most assays yielded consistent results, except for differences in fold change in cytopathic effect assays. Hamster serum samples were a consistent surrogate for human first-infection serum samples. These results inform the transition of surveillance of SARS-CoV-2 antigenic variation from dependence on human first-infection serum samples to the utilization of serum samples from animal models. |
Author | Rössler, Annika Douek, Daniel C Mykytyn, Anna Shen, Xiaoying Frieman, Matthew Godbole, Sucheta Krammer, Florian Jones, Terry C Davis-Gardner, Meredith E Wang, Wei Corman, Victor M Supasa, Piyada Lai, Lilin Carreño, Juan Manuel Katzelnick, Leah C Kimpel, Janine Screaton, Gavin R Baracco, Lauren Lusvarghi, Sabrina Weiss, Carol D Eckerle, Isabella Ellis, Madison Simon, Viviana Netzl, Antonia Haagmans, Bart Liu, Chang Drosten, Christian Suthar, Mehul S Edara, Venkata-Viswanadh Henry, Amy R Wilks, Samuel H Dejnirattisai, Wanwisa Smith, Derek J Mühlemann, Barbara Fouchier, Ron A M Kawaoka, Yoshihiro Halfmann, Peter J Meyer, Benjamin Sigal, Alex Montefiori, David C Bekliz, Meriem Diamond, Michael S Pollett, Simon Subramanian, Rahul Türeli, Sina Mongkolsapaya, Juthathip |
Author_xml | – sequence: 1 givenname: Barbara orcidid: 0000-0002-5314-8530 surname: Mühlemann fullname: Mühlemann, Barbara organization: German Centre for Infection Research (DZIF), partner site Charité, 10117 Berlin, Germany – sequence: 2 givenname: Samuel H orcidid: 0000-0002-7760-8474 surname: Wilks fullname: Wilks, Samuel H organization: Center for Pathogen Evolution, Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK – sequence: 3 givenname: Lauren surname: Baracco fullname: Baracco, Lauren organization: Center for Pathogen Research, Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD 21201, USA – sequence: 4 givenname: Meriem surname: Bekliz fullname: Bekliz, Meriem organization: Centre for Emerging Viral Diseases, University Hospitals of Geneva and University of Geneva, CH-1211, Geneva, Switzerland – sequence: 5 givenname: Juan Manuel orcidid: 0000-0002-9039-9275 surname: Carreño fullname: Carreño, Juan Manuel organization: Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – sequence: 6 givenname: Victor M orcidid: 0000-0002-3605-0136 surname: Corman fullname: Corman, Victor M organization: German Centre for Infection Research (DZIF), partner site Charité, 10117 Berlin, Germany – sequence: 7 givenname: Meredith E orcidid: 0000-0002-6133-3613 surname: Davis-Gardner fullname: Davis-Gardner, Meredith E organization: Department of Pediatrics, Emory Vaccine Center, Emory National Primate Research Center, Emory University School of Medicine, Atlanta, GA 30329, USA – sequence: 8 givenname: Wanwisa orcidid: 0000-0001-7996-2699 surname: Dejnirattisai fullname: Dejnirattisai, Wanwisa organization: Division of Emerging Infectious Disease, Research Department, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok Noi, Bangkok 10700, Thailand – sequence: 9 givenname: Michael S orcidid: 0000-0002-8791-3165 surname: Diamond fullname: Diamond, Michael S organization: Center for Vaccines and Immunity to Microbial Pathogens, Washington University School of Medicine, St. Louis, MO 63110, USA – sequence: 10 givenname: Daniel C surname: Douek fullname: Douek, Daniel C organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA – sequence: 11 givenname: Christian orcidid: 0000-0001-7923-0519 surname: Drosten fullname: Drosten, Christian organization: German Centre for Infection Research (DZIF), partner site Charité, 10117 Berlin, Germany – sequence: 12 givenname: Isabella orcidid: 0000-0002-4850-7172 surname: Eckerle fullname: Eckerle, Isabella organization: Division of Infectious Diseases, Geneva University Hospitals, CH-1211 Geneva, Switzerland – sequence: 13 givenname: Venkata-Viswanadh orcidid: 0000-0001-9321-7839 surname: Edara fullname: Edara, Venkata-Viswanadh organization: Department of Pediatrics, Emory Vaccine Center, Emory National Primate Research Center, Emory University School of Medicine, Atlanta, GA 30329, USA – sequence: 14 givenname: Madison orcidid: 0000-0002-0325-5477 surname: Ellis fullname: Ellis, Madison organization: Department of Pediatrics, Emory Vaccine Center, Emory National Primate Research Center, Emory University School of Medicine, Atlanta, GA 30329, USA – sequence: 15 givenname: Ron A M orcidid: 0000-0001-8095-2869 surname: Fouchier fullname: Fouchier, Ron A M organization: Viroscience Department, Erasmus Medical Center, 3015 Rotterdam, Netherlands – sequence: 16 givenname: Matthew orcidid: 0000-0003-0107-0775 surname: Frieman fullname: Frieman, Matthew organization: Center for Pathogen Research, Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD 21201, USA – sequence: 17 givenname: Sucheta orcidid: 0000-0002-7564-1748 surname: Godbole fullname: Godbole, Sucheta organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA – sequence: 18 givenname: Bart orcidid: 0000-0001-6221-2015 surname: Haagmans fullname: Haagmans, Bart organization: Viroscience Department, Erasmus Medical Center, 3015 Rotterdam, Netherlands – sequence: 19 givenname: Peter J orcidid: 0000-0002-1648-1625 surname: Halfmann fullname: Halfmann, Peter J organization: Influenza Research Institute, Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, Madison, WI 53706, USA – sequence: 20 givenname: Amy R surname: Henry fullname: Henry, Amy R organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA – sequence: 21 givenname: Terry C orcidid: 0000-0003-1120-9531 surname: Jones fullname: Jones, Terry C organization: Center for Pathogen Evolution, Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK – sequence: 22 givenname: Leah C orcidid: 0000-0003-1033-6758 surname: Katzelnick fullname: Katzelnick, Leah C organization: Viral Epidemiology and Immunity Unit, Laboratory of Infectious Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA – sequence: 23 givenname: Yoshihiro orcidid: 0000-0001-5061-8296 surname: Kawaoka fullname: Kawaoka, Yoshihiro organization: Pandemic Preparedness, Infection and Advanced Research Center (UTOPIA), University of Tokyo, Tokyo 162-8655, Japan – sequence: 24 givenname: Janine orcidid: 0000-0002-5210-7905 surname: Kimpel fullname: Kimpel, Janine organization: Institute of Virology, Department of Hygiene, Microbiology and Public Health, Medical University of Innsbruck, Peter-Mayr-Str. 4b, 6020 Innsbruck, Austria – sequence: 25 givenname: Florian orcidid: 0000-0003-4121-776X surname: Krammer fullname: Krammer, Florian organization: Center for Vaccine Research and Pandemic Preparedness (C-VaRPP), Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – sequence: 26 givenname: Lilin surname: Lai fullname: Lai, Lilin organization: Department of Pediatrics, Emory Vaccine Center, Emory National Primate Research Center, Emory University School of Medicine, Atlanta, GA 30329, USA – sequence: 27 givenname: Chang surname: Liu fullname: Liu, Chang organization: Chinese Academy of Medical Science (CAMS) Oxford Institute (COI), University of Oxford, Oxford OX3 7BN, UK – sequence: 28 givenname: Sabrina orcidid: 0000-0003-1793-0450 surname: Lusvarghi fullname: Lusvarghi, Sabrina organization: Division of Viral Products, Office of Vaccines Research and Review, Center for Biologics Evaluation and Research, US Food and Drug Administration, Silver Spring, MD 20903, USA – sequence: 29 givenname: Benjamin orcidid: 0000-0003-0601-3550 surname: Meyer fullname: Meyer, Benjamin organization: Centre of Vaccinology, Department of Pathology and Immunology, University of Geneva, CH-1211 Geneva, Switzerland – sequence: 30 givenname: Juthathip surname: Mongkolsapaya fullname: Mongkolsapaya, Juthathip organization: Chinese Academy of Medical Science (CAMS) Oxford Institute (COI), University of Oxford, Oxford OX3 7BN, UK – sequence: 31 givenname: David C orcidid: 0000-0003-0856-6319 surname: Montefiori fullname: Montefiori, David C organization: Duke Human Vaccine Institute, Duke University School of Medicine, Durham, NC 27710, USA – sequence: 32 givenname: Anna orcidid: 0000-0001-7188-6871 surname: Mykytyn fullname: Mykytyn, Anna organization: Viroscience Department, Erasmus Medical Center, 3015 Rotterdam, Netherlands – sequence: 33 givenname: Antonia orcidid: 0000-0001-8034-2382 surname: Netzl fullname: Netzl, Antonia organization: Center for Pathogen Evolution, Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK – sequence: 34 givenname: Simon surname: Pollett fullname: Pollett, Simon organization: Henry M. Jackson Foundation for the Advancement of Military Medicine Inc., Bethesda, MD 20817, USA – sequence: 35 givenname: Annika orcidid: 0000-0002-5298-0288 surname: Rössler fullname: Rössler, Annika organization: Institute of Virology, Department of Hygiene, Microbiology and Public Health, Medical University of Innsbruck, Peter-Mayr-Str. 4b, 6020 Innsbruck, Austria – sequence: 36 givenname: Gavin R orcidid: 0000-0002-3549-4309 surname: Screaton fullname: Screaton, Gavin R organization: Oxford University Hospitals NHS Foundation Trust, Oxford OX3 9DU, UK – sequence: 37 givenname: Xiaoying orcidid: 0000-0002-8387-3952 surname: Shen fullname: Shen, Xiaoying organization: Duke Human Vaccine Institute, Duke University School of Medicine, Durham, NC 27710, USA – sequence: 38 givenname: Alex orcidid: 0000-0001-8571-2004 surname: Sigal fullname: Sigal, Alex organization: Centre for the AIDS Programme of Research in South Africa, Durban 4001, South Africa – sequence: 39 givenname: Viviana orcidid: 0000-0002-6416-5096 surname: Simon fullname: Simon, Viviana organization: Global Health and Emerging Pathogen Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – sequence: 40 givenname: Rahul orcidid: 0000-0002-1131-9952 surname: Subramanian fullname: Subramanian, Rahul organization: Office of Data Science and Emerging Technologies, Office of Science Management and Operations, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA – sequence: 41 givenname: Piyada orcidid: 0009-0006-3931-0569 surname: Supasa fullname: Supasa, Piyada organization: Wellcome Centre for Human Genetics, Nuffield Department of Medicine, University of Oxford, Oxford OX3 7BN, UK – sequence: 42 givenname: Mehul S orcidid: 0000-0002-2686-8380 surname: Suthar fullname: Suthar, Mehul S organization: Department of Pediatrics, Emory Vaccine Center, Emory National Primate Research Center, Emory University School of Medicine, Atlanta, GA 30329, USA – sequence: 43 givenname: Sina orcidid: 0000-0001-7342-9295 surname: Türeli fullname: Türeli, Sina organization: Center for Pathogen Evolution, Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK – sequence: 44 givenname: Wei orcidid: 0000-0003-2935-6388 surname: Wang fullname: Wang, Wei organization: Division of Viral Products, Office of Vaccines Research and Review, Center for Biologics Evaluation and Research, US Food and Drug Administration, Silver Spring, MD 20903, USA – sequence: 45 givenname: Carol D orcidid: 0000-0002-9965-1289 surname: Weiss fullname: Weiss, Carol D organization: Division of Viral Products, Office of Vaccines Research and Review, Center for Biologics Evaluation and Research, US Food and Drug Administration, Silver Spring, MD 20903, USA – sequence: 46 givenname: Derek J orcidid: 0000-0002-2393-1890 surname: Smith fullname: Smith, Derek J organization: Center for Pathogen Evolution, Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/38748773$$D View this record in MEDLINE/PubMed |
BookMark | eNo1kF9LwzAUxYMo7o9-A5F8gc42SdP0cRSdwkBww9eRJrdYSZORpJP66hc3MH04XDic--Pes0CX1llA6K7IV0VB-ENQffTSBjOAXkltioqQCzQvasYzThiZoUUIn3nOBS35NZpRUTFRVXSOfho3HKWXsT8BllaaKfQBuw7v1m-7rHHvGcEWxkQ3_XdKOYtjH8EH7OEE0gSsnE0rEayacAvxC8Dij3GQNuF0Uj9IgwenweAAfhzOtvIuBCxDkFO4QVddIsHt31yi_dPjvnnOtq-bl2a9zVRZ0JjVHABk25WUpUeqHIDnpRCUQF0JIYjSqmaU6lpJllNghLWkJZ0qWwWs1mSJ7s_Y49imng5Hn07z0-G_DPILU89n5Q |
CitedBy_id | crossref_primary_10_1038_s41541_024_00888_y crossref_primary_10_1128_jvi_00948_24 crossref_primary_10_3390_v16121936 crossref_primary_10_1016_j_celrep_2024_115140 crossref_primary_10_1073_pnas_2310917121 |
ContentType | Journal Article |
DBID | CGR CUY CVF ECM EIF NPM |
DOI | 10.1126/scitranslmed.adl1722 |
DatabaseName | Medline MEDLINE MEDLINE (Ovid) MEDLINE MEDLINE PubMed |
DatabaseTitle | MEDLINE Medline Complete MEDLINE with Full Text PubMed MEDLINE (Ovid) |
DatabaseTitleList | MEDLINE |
Database_xml | – sequence: 1 dbid: NPM name: PubMed url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database – sequence: 2 dbid: EIF name: MEDLINE url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search sourceTypes: Index Database |
DeliveryMethod | no_fulltext_linktorsrc |
Discipline | Medicine |
EISSN | 1946-6242 |
ExternalDocumentID | 38748773 |
Genre | Comparative Study Research Support, Non-U.S. Gov't Journal Article Research Support, N.I.H., Extramural |
GrantInformation_xml | – fundername: NIAID NIH HHS grantid: U19 AI057266 – fundername: Wellcome Trust – fundername: NIAID NIH HHS grantid: 75N93021C00017 – fundername: NIAID NIH HHS grantid: 75N93021C00014 – fundername: NIAID NIH HHS grantid: R01 AI157155 – fundername: NIAID NIH HHS grantid: 75N93019C00051 – fundername: NIH HHS grantid: P51 OD011132 – fundername: Gates Foundation grantid: INV-018944 |
GroupedDBID | --- 0R~ 4.4 53G 7~K ABJNI ACGFS AENEX AJGZS ALMA_UNASSIGNED_HOLDINGS BKF C45 CGR CUY CVF DU5 EBS ECM EIF EMOBN F5P HZ~ NPM O9- OFXIZ OVD OVIDX P2P RHI TEORI |
ID | FETCH-LOGICAL-c513t-96eeeabf53406870ee6058832e978882cdc9433d9ca403e424b2b2fc5bce49d2 |
IngestDate | Thu Aug 28 04:41:25 EDT 2025 |
IsPeerReviewed | true |
IsScholarly | true |
Issue | 747 |
Language | English |
LinkModel | OpenURL |
MergedId | FETCHMERGED-LOGICAL-c513t-96eeeabf53406870ee6058832e978882cdc9433d9ca403e424b2b2fc5bce49d2 |
ORCID | 0000-0001-8034-2382 0000-0002-3549-4309 0000-0002-6133-3613 0000-0002-5314-8530 0000-0002-8791-3165 0000-0002-6416-5096 0000-0002-2686-8380 0000-0001-8095-2869 0000-0002-5298-0288 0000-0001-7342-9295 0000-0001-7996-2699 0000-0002-5210-7905 0000-0001-8571-2004 0000-0003-0856-6319 0000-0002-1648-1625 0000-0003-4121-776X 0000-0001-7923-0519 0000-0003-0601-3550 0000-0002-8387-3952 0000-0003-1120-9531 0009-0006-3931-0569 0000-0002-7760-8474 0000-0003-2935-6388 0000-0001-6221-2015 0000-0001-5061-8296 0000-0002-9039-9275 0000-0002-9965-1289 0000-0002-7564-1748 0000-0003-1793-0450 0000-0002-3605-0136 0000-0003-0107-0775 0000-0001-7188-6871 0000-0003-1033-6758 0000-0002-2393-1890 0000-0002-4850-7172 0000-0002-0325-5477 0000-0001-9321-7839 0000-0002-1131-9952 |
PMID | 38748773 |
ParticipantIDs | pubmed_primary_38748773 |
PublicationCentury | 2000 |
PublicationDate | 2024-05-15 |
PublicationDateYYYYMMDD | 2024-05-15 |
PublicationDate_xml | – month: 05 year: 2024 text: 2024-05-15 day: 15 |
PublicationDecade | 2020 |
PublicationPlace | United States |
PublicationPlace_xml | – name: United States |
PublicationTitle | Science translational medicine |
PublicationTitleAlternate | Sci Transl Med |
PublicationYear | 2024 |
SSID | ssj0068356 |
Score | 2.46991 |
Snippet | The evolution of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) requires ongoing monitoring to judge the ability of newly arising variants to... |
SourceID | pubmed |
SourceType | Index Database |
StartPage | eadl1722 |
SubjectTerms | Animals Antibodies, Neutralizing - blood Antibodies, Neutralizing - immunology Antibodies, Viral - blood Antibodies, Viral - immunology COVID-19 - blood COVID-19 - immunology COVID-19 - virology Cricetinae Disease Models, Animal Humans Mice Neutralization Tests SARS-CoV-2 - immunology |
Title | Comparative analysis of SARS-CoV-2 neutralization titers reveals consistency between human and animal model serum and across assays |
URI | https://www.ncbi.nlm.nih.gov/pubmed/38748773 |
Volume | 16 |
hasFullText | |
inHoldings | 1 |
isFullTextHit | |
isPrint | |
link | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1LbxMxELZSkKpeEO_ylA_cIkeJ17tdH5sIVCGFAw2ot2r9EqjZpFI2SPTav8YPY8aPxg0BAZdVZEfO2vPFnoe_GULeKLBj1chIZgvNmXCqZI0pa1Y5aZRCFcIgOXn6oTr5JN6flWe93o_s1tK6UwN9tZNX8j9ShTaQK7Jk_0GyN4NCA3wG-cITJAzPv5LxJEvd3WTZRU6PP56yyfIz4_2FXXtfRmBb9n0WZYwUfLOYN1nj9dhV5-mX6cZWqNoXcrh-bZFcgsVy-jChdSin0fiTtQ9ad_N9lSu3aZ_o8PybJy_jdvR-irH58eTL3LaxQHOMeWQuoItV8Fa3a_jlm2DWGHNL62Wic29IbGN7ATP0vl3M29zmrgwuMAofyJwDG7ZfKSqGjJVb-3OV4fAo5OeM2y38DeaggfHdZ0GqXhlmDbMd7Pg6SPSy9fgo6iOw3kJhlT_3bmXoTl17ZA9sFSy-ih6joA1UoOFWkbIZyVq_vM4B2U9DbBk3XsmZ3Sf3onVCjwPUHpCeXTwk-9MowUfkOkMcTYijS0c3iKO3EUcD4mhEHM0QRyPiqEccDGdoQBz1iKMecaHZI44GxD0ms3dvZ5MTFst4MF2Oio7JylrbKFcWoDzC8WAthuLhJLES_S9cGy1FURipGzEsrOBCccWdLpW2Qhr-hNxZLBf2kFBRY-ojJ2tQqUStR6o2blhr0HCHSnBnnpGnYfXOL0OqlvO0rs9_2_OCHGyg-JLcdbAW9hUomp167SX5E6lvh6Q |
linkProvider | National Library of Medicine |
openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Comparative+analysis+of+SARS-CoV-2+neutralization+titers+reveals+consistency+between+human+and+animal+model+serum+and+across+assays&rft.jtitle=Science+translational+medicine&rft.au=M%C3%BChlemann%2C+Barbara&rft.au=Wilks%2C+Samuel+H&rft.au=Baracco%2C+Lauren&rft.au=Bekliz%2C+Meriem&rft.date=2024-05-15&rft.eissn=1946-6242&rft.volume=16&rft.issue=747&rft.spage=eadl1722&rft_id=info:doi/10.1126%2Fscitranslmed.adl1722&rft_id=info%3Apmid%2F38748773&rft_id=info%3Apmid%2F38748773&rft.externalDocID=38748773 |