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

Author:

Mühlemann Barbara12ORCID,Wilks Samuel H.3ORCID,Baracco Lauren4,Bekliz Meriem56,Carreño Juan Manuel7ORCID,Corman Victor M.12ORCID,Davis-Gardner Meredith E.8ORCID,Dejnirattisai Wanwisa910ORCID,Diamond Michael S.111213ORCID,Douek Daniel C.14,Drosten Christian12ORCID,Eckerle Isabella5615ORCID,Edara Venkata-Viswanadh8ORCID,Ellis Madison8ORCID,Fouchier Ron A. M.16ORCID,Frieman Matthew4ORCID,Godbole Sucheta14ORCID,Haagmans Bart16ORCID,Halfmann Peter J.17ORCID,Henry Amy R.14,Jones Terry C.123ORCID,Katzelnick Leah C.18ORCID,Kawaoka Yoshihiro17192021ORCID,Kimpel Janine22ORCID,Krammer Florian72324ORCID,Lai Lilin8,Liu Chang925,Lusvarghi Sabrina26ORCID,Meyer Benjamin27ORCID,Mongkolsapaya Juthathip925,Montefiori David C.2829ORCID,Mykytyn Anna16ORCID,Netzl Antonia3ORCID,Pollett Simon3031,Rössler Annika22ORCID,Screaton Gavin R.932ORCID,Shen Xiaoying2829ORCID,Sigal Alex333435ORCID,Simon Viviana7233637ORCID,Subramanian Rahul38ORCID,Supasa Piyada9ORCID,Suthar Mehul S.8ORCID,Türeli Sina3ORCID,Wang Wei26ORCID,Weiss Carol D.26ORCID,Smith Derek J.3ORCID

Affiliation:

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.

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.

Publisher

American Association for the Advancement of Science (AAAS)

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