Comparative Study

. 2024 May 15;16(747):eadl1722.

doi: 10.1126/scitranslmed.adl1722. Epub 2024 May 15.

Comparative analysis of SARS-CoV-2 neutralization titers reveals consistency between human and animal model serum and across assays

Barbara Mühlemann^{1

2}, Samuel H Wilks³, Lauren Baracco⁴, Meriem Bekliz^{5

6}, Juan Manuel Carreño⁷, Victor M Corman^{1

2}, Meredith E Davis-Gardner⁸, Wanwisa Dejnirattisai^{9

10}, Michael S Diamond^{11

12

13}, Daniel C Douek¹⁴, Christian Drosten^{1

2}, Isabella Eckerle^{5

6

15}, Venkata-Viswanadh Edara⁸, Madison Ellis⁸, Ron A M Fouchier¹⁶, Matthew Frieman⁴, Sucheta Godbole¹⁴, Bart Haagmans¹⁶, Peter J Halfmann¹⁷, Amy R Henry¹⁴, Terry C Jones^{1

2

3}, Leah C Katzelnick¹⁸, Yoshihiro Kawaoka^{17

19

20

21}, Janine Kimpel²², Florian Krammer^{7

23

24}, Lilin Lai⁸, Chang Liu^{9

25}, Sabrina Lusvarghi²⁶, Benjamin Meyer²⁷, Juthathip Mongkolsapaya^{9

25}, David C Montefiori^{28

29}, Anna Mykytyn¹⁶, Antonia Netzl³, Simon Pollett^{30

31}, Annika Rössler²², Gavin R Screaton^{9

32}, Xiaoying Shen^{28

29}, Alex Sigal^{33

34

35}, Viviana Simon^{7

23

36

37}, Rahul Subramanian³⁸, Piyada Supasa⁹, Mehul S Suthar⁸, Sina Türeli³, Wei Wang²⁶, Carol D Weiss²⁶, Derek J Smith³

Affiliations

¹ Institute of Virology, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, 10117 Berlin, Germany.
² German Centre for Infection Research (DZIF), partner site Charité, 10117 Berlin, Germany.
³ Center for Pathogen Evolution, Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK.
⁴ Center for Pathogen Research, Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD 21201, USA.
⁵ Department of Medicine, Faculty of Medicine, University of Geneva, CH-1211 Geneva, Switzerland.
⁶ Centre for Emerging Viral Diseases, University Hospitals of Geneva and University of Geneva, CH-1211, Geneva, Switzerland.
⁷ Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
⁸ Department of Pediatrics, Emory Vaccine Center, Emory National Primate Research Center, Emory University School of Medicine, Atlanta, GA 30329, USA.
⁹ Wellcome Centre for Human Genetics, Nuffield Department of Medicine, University of Oxford, Oxford OX3 7BN, UK.
¹⁰ Division of Emerging Infectious Disease, Research Department, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok Noi, Bangkok 10700, Thailand.
¹¹ Departments of Medicine, Molecular Microbiology, Pathology & Immunology, Washington University School of Medicine, St. Louis, MO 63110, USA.
¹² Andrew M. and Jane M. Bursky the Center for Human Immunology and Immunotherapy Programs, Washington University School of Medicine, St. Louis, MO 63110, USA.
¹³ Center for Vaccines and Immunity to Microbial Pathogens, Washington University School of Medicine, St. Louis, MO 63110, USA.
¹⁴ Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.
¹⁵ Division of Infectious Diseases, Geneva University Hospitals, CH-1211 Geneva, Switzerland.
¹⁶ Viroscience Department, Erasmus Medical Center, 3015 Rotterdam, Netherlands.
¹⁷ Influenza Research Institute, Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, Madison, WI 53706, USA.
¹⁸ Viral Epidemiology and Immunity Unit, Laboratory of Infectious Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.
¹⁹ Division of Virology, Institute of Medical Science, University of Tokyo, Tokyo 108-8639, Japan.
²⁰ Research Center for Global Viral Diseases, National Center for Global Health and Medicine Research Institute, Tokyo 162-8655, Japan.
²¹ Pandemic Preparedness, Infection and Advanced Research Center (UTOPIA), University of Tokyo, Tokyo 162-8655, Japan.
²² Institute of Virology, Department of Hygiene, Microbiology and Public Health, Medical University of Innsbruck, Peter-Mayr-Str. 4b, 6020 Innsbruck, Austria.
²³ Department of Pathology, Cellular and Molecular Medicine, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
²⁴ Center for Vaccine Research and Pandemic Preparedness (C-VaRPP), Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
²⁵ Chinese Academy of Medical Science (CAMS) Oxford Institute (COI), University of Oxford, Oxford OX3 7BN, UK.
²⁶ 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.
²⁷ Centre of Vaccinology, Department of Pathology and Immunology, University of Geneva, CH-1211 Geneva, Switzerland.
²⁸ Department of Surgery, Duke University School of Medicine, Durham, NC 27710, USA.
²⁹ Duke Human Vaccine Institute, Duke University School of Medicine, Durham, NC 27710, USA.
³⁰ Infectious Disease Clinical Research Program, Department of Preventive Medicine and Biostatistics, Uniformed Services University of the Health Sciences, Bethesda, MD 20814, USA.
³¹ Henry M. Jackson Foundation for the Advancement of Military Medicine Inc., Bethesda, MD 20817, USA.
³² Oxford University Hospitals NHS Foundation Trust, Oxford OX3 9DU, UK.
³³ Africa Health Research Institute, Durban 4001, South Africa.
³⁴ School of Laboratory Medicine and Medical Sciences, University of KwaZulu-Natal, Durban 4001, South Africa.
³⁵ Centre for the AIDS Programme of Research in South Africa, Durban 4001, South Africa.
³⁶ Division of Infectious Diseases, Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
³⁷ Global Health and Emerging Pathogen Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
³⁸ 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.

PMID: 38748773
PMCID: PMC12362660
DOI: 10.1126/scitranslmed.adl1722

Comparative Study

Comparative analysis of SARS-CoV-2 neutralization titers reveals consistency between human and animal model serum and across assays

Barbara Mühlemann et al. Sci Transl Med. 2024.

. 2024 May 15;16(747):eadl1722.

doi: 10.1126/scitranslmed.adl1722. Epub 2024 May 15.

Authors

Affiliations

¹ Institute of Virology, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, 10117 Berlin, Germany.
² German Centre for Infection Research (DZIF), partner site Charité, 10117 Berlin, Germany.
³ Center for Pathogen Evolution, Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK.
⁴ Center for Pathogen Research, Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD 21201, USA.
⁵ Department of Medicine, Faculty of Medicine, University of Geneva, CH-1211 Geneva, Switzerland.
⁶ Centre for Emerging Viral Diseases, University Hospitals of Geneva and University of Geneva, CH-1211, Geneva, Switzerland.
⁷ Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
⁸ Department of Pediatrics, Emory Vaccine Center, Emory National Primate Research Center, Emory University School of Medicine, Atlanta, GA 30329, USA.
⁹ Wellcome Centre for Human Genetics, Nuffield Department of Medicine, University of Oxford, Oxford OX3 7BN, UK.
¹⁰ Division of Emerging Infectious Disease, Research Department, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok Noi, Bangkok 10700, Thailand.
¹¹ Departments of Medicine, Molecular Microbiology, Pathology & Immunology, Washington University School of Medicine, St. Louis, MO 63110, USA.
¹² Andrew M. and Jane M. Bursky the Center for Human Immunology and Immunotherapy Programs, Washington University School of Medicine, St. Louis, MO 63110, USA.
¹³ Center for Vaccines and Immunity to Microbial Pathogens, Washington University School of Medicine, St. Louis, MO 63110, USA.
¹⁴ Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.
¹⁵ Division of Infectious Diseases, Geneva University Hospitals, CH-1211 Geneva, Switzerland.
¹⁶ Viroscience Department, Erasmus Medical Center, 3015 Rotterdam, Netherlands.
¹⁷ Influenza Research Institute, Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, Madison, WI 53706, USA.
¹⁸ Viral Epidemiology and Immunity Unit, Laboratory of Infectious Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.
¹⁹ Division of Virology, Institute of Medical Science, University of Tokyo, Tokyo 108-8639, Japan.
²⁰ Research Center for Global Viral Diseases, National Center for Global Health and Medicine Research Institute, Tokyo 162-8655, Japan.
²¹ Pandemic Preparedness, Infection and Advanced Research Center (UTOPIA), University of Tokyo, Tokyo 162-8655, Japan.
²² Institute of Virology, Department of Hygiene, Microbiology and Public Health, Medical University of Innsbruck, Peter-Mayr-Str. 4b, 6020 Innsbruck, Austria.
²³ Department of Pathology, Cellular and Molecular Medicine, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
²⁴ Center for Vaccine Research and Pandemic Preparedness (C-VaRPP), Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
²⁵ Chinese Academy of Medical Science (CAMS) Oxford Institute (COI), University of Oxford, Oxford OX3 7BN, UK.
²⁶ 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.
²⁷ Centre of Vaccinology, Department of Pathology and Immunology, University of Geneva, CH-1211 Geneva, Switzerland.
²⁸ Department of Surgery, Duke University School of Medicine, Durham, NC 27710, USA.
²⁹ Duke Human Vaccine Institute, Duke University School of Medicine, Durham, NC 27710, USA.
³⁰ Infectious Disease Clinical Research Program, Department of Preventive Medicine and Biostatistics, Uniformed Services University of the Health Sciences, Bethesda, MD 20814, USA.
³¹ Henry M. Jackson Foundation for the Advancement of Military Medicine Inc., Bethesda, MD 20817, USA.
³² Oxford University Hospitals NHS Foundation Trust, Oxford OX3 9DU, UK.
³³ Africa Health Research Institute, Durban 4001, South Africa.
³⁴ School of Laboratory Medicine and Medical Sciences, University of KwaZulu-Natal, Durban 4001, South Africa.
³⁵ Centre for the AIDS Programme of Research in South Africa, Durban 4001, South Africa.
³⁶ Division of Infectious Diseases, Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
³⁷ Global Health and Emerging Pathogen Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
³⁸ 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.

PMID: 38748773
PMCID: PMC12362660
DOI: 10.1126/scitranslmed.adl1722

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.

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Conflict of interest statement

Competing interests

VMC is a co-inventor on a patent application entitled “Methods and reagents for diagnosis of SARS-CoV-2 infection” (Patent application no EP3809137A1). MSD is a consultant for Inbios, Vir Biotechnology, Ocugen, Topspin Therapeutics, Moderna, and Immunome. The Diamond laboratory has received unrelated funding support in sponsored research agreements from Moderna, Vir Biotechnology, Generate Biomedicines, and Emergent BioSolutions. YK received unrelated funding support from Daiichi Sankyo Pharmaceutical, Toyama Chemical, Tauns Laboratories, Inc., Shionogi & Co. LTD, Otsuka Pharmaceutical, KM Biologics, Kyoritsu Seiyaku, Shinya Corporation, and Fuji Rebio. The Icahn School of Medicine at Mount Sinai has filed patent applications relating to SARS-CoV-2 serological assays and NDV-based SARS-CoV-2 vaccines which list FK as co-inventor: “Influenza virus vaccination regimens” (Patent no 20190125859), “Influenza virus vaccines and uses thereof” (Patent no 9371366), “Influenza virus vaccines and uses thereof” (Patent nos 20180333479, 9968670, 20190099484, 20150335729, 10131695, 10137189, 20140328875, 20160361408, 20150132330, 20190106461, WO2013043729A1 WIPO (PCT), WO2016205347A1 WIPO (PCT)), “Influenza virus hemagglutinin proteins and uses thereof” (Patent nos WO2017218624A1 WIPO (PCT)), “Influenza virus vaccination regimens” (WO2016118937A1 WIPO (PCT)). Mount Sinai has spun out a company, Kantaro, to market serological tests for SARS-CoV-2. FK has consulted for Merck, Seqirus, Curevac and Pfizer, and is currently consulting for GSK, Gritstone, 3rd Rock Ventures and Avimex. FK is a co-founder and scientific advisory board member of CastleVax. The Krammer laboratory is also collaborating with Pfizer on animal models of SARS-CoV-2 and Dynavax on influenza virus vaccines. IE has received a research grant and speakers fees from Moderna. B. Meyer has received a research grant from Moderna. GRS is on the GSK Vaccines Scientific Advisory Board. Oxford University holds intellectual property related to the Oxford-AstraZeneca vaccine. MSS serves in an advisory role for Ocugen, Inc. SP reports that the Uniformed Services University (USU) Infectious Diseases Clinical Research Program (IDCRP), a US Department of Defense institution, and the Henry M. Jackson Foundation (HJF) were funded under a Cooperative Research and Development Agreement to conduct an unrelated phase III COVID-19 monoclonal antibody immunoprophylaxis trial sponsored by AstraZeneca. The HJF, in support of the USU IDCRP, was funded by the Department of Defense Joint Program Executive Office for Chemical, Biological, Radiological, and Nuclear Defense to augment the conduct of an unrelated phase III vaccine trial sponsored by AstraZeneca. Both trials were part of the U.S. Government COVID-19 response. Neither is related to the work presented here. Authors not listed above declare that they have no competing interests. The views expressed are those of the authors and do not reflect the official policy of the USUHS, Department of the Army, Department of the Navy, the Department of the Air Force, the Department of Defense or the U.S. Government and the Henry M. Jackson Foundation for the Advancement of Military Medicine, Inc. (HJF). The investigators have adhered to the policies for protection of human subjects as prescribed in 45 CFR 46. SL, WW, and CDW are US Government employees. Title 17 U.S.C. §105 provides that ‘Copyright protection under this title is not available for any work of the United States Government.’ Title 17 U.S.C. §101 defines a U.S. Government work as a work prepared by an employee of the U.S. Government as part of that person’s official duties.

Figures

**Figure 1:. Titers were compared between serum from humans, hamsters, and mice infected with the B.1.351 variant.**
(A) Raw titers for the B.1.351 convalescent serum groups are shown. (B) Shown is the posterior distribution of the dataset magnitude effect. Datasets are grouped by species (human, hamster, mouse) on the y-axis and colored by assay type. Vertical bars show the 95% highest posterior density interval, each with a colored dot denoting the mean. (C) Shown are titers after adjusting for dataset magnitude effects. In (A) and (C), each dot corresponds to the GMT of a variant titrated against all B.1.351 convalescent serum samples in a particular dataset; GMTs in (C) were calculated from titers adjusted for dataset magnitude effect. Dots are colored by the species. The gray bar heights indicate the median of the GMTs of the individual datasets. Equivalent plots for all six serum groups can be found in fig. S27 (titer magnitude) and S31 (titer variability).

**Figure 2:. Fold changes in the mRNA-1273 or BNT162b2 vaccinated (mRNA vax.), and D614G, B.1.351, B.1.617.2, and BA.1 convalescent (conv.) serum groups were measured in the 18 datasets.**
Dots show the mean estimated fold change for each variant in each dataset and the bars show the estimated 95% highest posterior density intervals, with the colors corresponding to the variant. Variants are ordered on the x-axis within-dataset by decreasing estimated mean fold change calculated in a particular serum group across all datasets. Datasets are grouped by assay on the x-axis with bold vertical lines separating the FRNT, LV-PV-neut, VSV-PV-neut, PRNT, Microneut, and CPE datasets. The light gray line in each panel indicates the estimated fold change per variant in a particular serum group calculated across all datasets in descending order. The black line shows the estimated fold change per variant in descending order after accounting for differences in fold change between datasets. Equivalent figures that include the B.1.1.7 and P.1 convalescent serum groups, as well as ordered by species (human, hamster, and mouse) are shown in fig. S30 and S31, respectively. Figures split by variant are shown in fig. S36 (by dataset), fig. S37 (by species), and fig. S38 (by assay). Empty spaces indicate that a dataset did not contain that serum group.

**Figure 3:. Serum groups exhibit different sensitivity to the E484K and N501Y substitutions.**
**(A and B)** Each row shows the average fold difference in titer between the two variants on the left, which differ by only the E484K (A) or the N501Y (B) substitution in the RBD. A positive fold difference corresponds to higher titers against the variant with the substitution, whereas a negative fold difference corresponds to higher titers against the variant without the substitution. Symbols and ranges correspond to the average fold difference and 95% highest posterior density intervals. Data are colored by species and the background of dataset names is colored by the assay. Vertical lines indicate the average fold difference in each dataset, colored by species. The gray line indicates no difference in titers between variants. Fig. S42 shows the same figure, split by assay. The ‘+E484K’ suffix to the variant names indicates that the E484K substitution is present in addition to any other substitutions present in that variant.

**Figure 4:. Antigenic maps constructed from the 18 datasets.**
(A) Antigenic maps are shown for each of the 18 datasets. Arrows point to the position of each variant in the merged map shown in (B), with shorter arrows indicating better correspondence between the maps. The first row contains human datasets with BA.1, ordered by the presence of BA.2 and BA.5. The second row contains hamster datasets with BA.1. The third row contains remaining datasets without BA.1 that were not generated using CPE assays. Data for the maps in the bottom row were generated using CPE assays. (B) Shown is an antigenic map constructed by merging all titers of the 18 datasets. D614G, B.1.351, B.1.617.2, BA.1, BA.2, and BA.4/BA.5 are highlighted. A version of this map colored by variant is shown in fig. S53. In both panels, variants are colored by substitutions in the RBD. Blue indicates no substitutions in RBD relative to the ancestral variant, except S477N; this includes the ancestral (D614G and 614D), A.23.1, B.1.526, and B.1.526+S477N variants. Turquoise indicates variants with only the N501Y substitution in the RBD, including the B.1.1.7 and D614G+N501Y variants. Light green indicates variants with only the E484K substitution in the RBD, including the B.1.525, R.1, P.2, and B.1.526+E484K variants. Yellow indicates variants with the E484K and N501Y substitutions in the RBD, including the P.1 (+K417T), B.1.351 (+K417N), B.1.1.7+E484K, and B.1.621 (+R346K) variants. Orange indicates variants with the L452R (or Q, in the case of C.37) substitution in the RBD, including the C.36.3, C.37 (+F490S), B.1.429, B.1.617.2 (+T478K), B.1.617.2+K417N (+T478K), AY.4.2 (+T478K), AY.1+K417N (+T478K), and AY.2+K417N (+T478K) variants. Maroon indicates variants with L452R and E484Q, including the B.1.617.1 (+T478K), B.1.630 (+T478K), and AY.3+E484Q (+T478K) variants. Dark magenta indicates Omicron BA.1 and BA.1.1 variants. Magenta indicates Omicron BA.2, BA.2.12.1, and BA.3 variants. Light pink indicates Omicron BA.4 and BA.5 variants.

See this image and copyright information in PMC

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Comparative analysis of SARS-CoV-2 neutralization titers reveals consistency between human and animal model serum and across assays

Affiliations

Comparative analysis of SARS-CoV-2 neutralization titers reveals consistency between human and animal model serum and across assays

Authors

Affiliations

Abstract

Conflict of interest statement

Figures

References

Publication types

MeSH terms

Grants and funding

LinkOut - more resources

Full Text Sources

Medical

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