Robust SARS-CoV-2-specific and heterologous immune responses in vaccine-naïve residents of long-term care facilities who survive natural infection

Gokhan Tut; Tara Lancaster; Megan S. Butler; Panagiota Sylla; Eliska Spalkova; David Bone; Nayandeep Kaur; Christopher Bentley; Umayr Amin; Azar T. Jadir; Samuel Hulme; Morenike Ayodel; Alexander C. Dowell; Hayden Pearce; Jianmin Zuo; Sandra Margielewska-Davies; Kriti Verma; Samantha Nicol; Jusnara Begum; Elizabeth Jinks; Elif Tut; Rachel Bruton; Maria Krutikov; Madhumita Shrotri; Rebecca Giddings; Borscha Azmi; Chris Fuller; Aidan Irwin-Singer; Andrew Hayward; Andrew Copas; Laura Shallcross; Paul Moss

doi:10.1038/s43587-022-00224-w

Robust SARS-CoV-2-specific and heterologous immune responses in vaccine-naïve residents of long-term care facilities who survive natural infection

Gokhan Tut^*, Tara Lancaster, Megan S. Butler, Panagiota Sylla, Eliska Spalkova, David Bone, Nayandeep Kaur, Christopher Bentley, Umayr Amin, Azar T. Jadir, Samuel Hulme, Morenike Ayodel, Alexander C. Dowell, Hayden Pearce, Jianmin Zuo, Sandra Margielewska-Davies, Kriti Verma, Samantha Nicol, Jusnara Begum, Elizabeth JinksElif Tut, Rachel Bruton, Maria Krutikov, Madhumita Shrotri, Rebecca Giddings, Borscha Azmi, Chris Fuller, Aidan Irwin-Singer, Andrew Hayward, Andrew Copas, Laura Shallcross, Paul Moss

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

Abstract

We studied humoral and cellular immunity against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in 152 long-term care facility staff and 124 residents over a prospective 4-month period shortly after the first wave of infection in England. We show that residents of long-term care facilities developed high and stable levels of antibodies against spike protein and receptor-binding domain. Nucleocapsid-specific responses were also elevated but waned over time. Antibodies showed stable and equivalent levels of functional inhibition against spike-angiotensin-converting enzyme 2 binding in all age groups with comparable activity against viral variants of concern. SARS-CoV-2 seropositive donors showed high levels of antibodies to other beta-coronaviruses but serostatus did not impact humoral immunity to influenza or other respiratory syncytial viruses. SARS-CoV-2-specific cellular responses were similar across all ages but virus-specific populations showed elevated levels of activation in older donors. Thus, survivors of SARS-CoV-2 infection show a robust and stable immunity against the virus that does not negatively impact responses to other seasonal viruses.

Original language	English
Pages (from-to)	536-547
Number of pages	12
Journal	Nature Aging
Volume	2
Issue number	6
DOIs	https://doi.org/10.1038/s43587-022-00224-w
Publication status	Published - Jun 2022
Externally published	Yes

Bibliographical note

Funding Information:
We thank the staff and residents in the LTCFs who participated in this study and M. Marshall at NHS England who pseudonymized the electronic health records. This report is independent research funded by the Department of Health and Social Care (COVID-19 surveillance studies). A.H. is supported by Health Data Research UK (grant no. LOND1), which is funded by the UK Medical Research Council, Engineering and Physical Sciences Research Council, Economic and Social Research Council, Department of Health and Social Care (England), Chief Scientist Office of the Scottish Government Health and Social Care Directorates, Health and Social Care Research and Development Division (Welsh Government), Public Health Agency (Northern Ireland), British Heart Foundation and Wellcome Trust. L.S. is funded by an NIHR Clinician Scientist Award (no. CS-2016-007). M.K. is funded by a Wellcome Trust Clinical PhD Fellowship (no. 222907/Z/21/Z). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. The views expressed in this publication are those of the authors and not necessarily those of the NHS, Public Health England or the UK Government Department of Health and Social Care.

Funding Information:
We thank the staff and residents in the LTCFs who participated in this study and M. Marshall at NHS England who pseudonymized the electronic health records. This report is independent research funded by the Department of Health and Social Care (COVID-19 surveillance studies). A.H. is supported by Health Data Research UK (grant no. LOND1), which is funded by the UK Medical Research Council, Engineering and Physical Sciences Research Council, Economic and Social Research Council, Department of Health and Social Care (England), Chief Scientist Office of the Scottish Government Health and Social Care Directorates, Health and Social Care Research and Development Division (Welsh Government), Public Health Agency (Northern Ireland), British Heart Foundation and Wellcome Trust. L.S. is funded by an NIHR Clinician Scientist Award (no. CS-2016-007). M.K. is funded by a Wellcome Trust Clinical PhD Fellowship (no. 222907/Z/21/Z). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. The views expressed in this publication are those of the authors and not necessarily those of the NHS, Public Health England or the UK Government Department of Health and Social Care.

Publisher Copyright:
© 2022, The Author(s).

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10.1038/s43587-022-00224-w

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Tut, G., Lancaster, T., Butler, M. S., Sylla, P., Spalkova, E., Bone, D., Kaur, N., Bentley, C., Amin, U., Jadir, A. T., Hulme, S., Ayodel, M., Dowell, A. C., Pearce, H., Zuo, J., Margielewska-Davies, S., Verma, K., Nicol, S., Begum, J., ... Moss, P. (2022). Robust SARS-CoV-2-specific and heterologous immune responses in vaccine-naïve residents of long-term care facilities who survive natural infection. Nature Aging, 2(6), 536-547. https://doi.org/10.1038/s43587-022-00224-w

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title = "Robust SARS-CoV-2-specific and heterologous immune responses in vaccine-na{\"i}ve residents of long-term care facilities who survive natural infection",

abstract = "We studied humoral and cellular immunity against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in 152 long-term care facility staff and 124 residents over a prospective 4-month period shortly after the first wave of infection in England. We show that residents of long-term care facilities developed high and stable levels of antibodies against spike protein and receptor-binding domain. Nucleocapsid-specific responses were also elevated but waned over time. Antibodies showed stable and equivalent levels of functional inhibition against spike-angiotensin-converting enzyme 2 binding in all age groups with comparable activity against viral variants of concern. SARS-CoV-2 seropositive donors showed high levels of antibodies to other beta-coronaviruses but serostatus did not impact humoral immunity to influenza or other respiratory syncytial viruses. SARS-CoV-2-specific cellular responses were similar across all ages but virus-specific populations showed elevated levels of activation in older donors. Thus, survivors of SARS-CoV-2 infection show a robust and stable immunity against the virus that does not negatively impact responses to other seasonal viruses.",

author = "Gokhan Tut and Tara Lancaster and Butler, {Megan S.} and Panagiota Sylla and Eliska Spalkova and David Bone and Nayandeep Kaur and Christopher Bentley and Umayr Amin and Jadir, {Azar T.} and Samuel Hulme and Morenike Ayodel and Dowell, {Alexander C.} and Hayden Pearce and Jianmin Zuo and Sandra Margielewska-Davies and Kriti Verma and Samantha Nicol and Jusnara Begum and Elizabeth Jinks and Elif Tut and Rachel Bruton and Maria Krutikov and Madhumita Shrotri and Rebecca Giddings and Borscha Azmi and Chris Fuller and Aidan Irwin-Singer and Andrew Hayward and Andrew Copas and Laura Shallcross and Paul Moss",

note = "Funding Information: We thank the staff and residents in the LTCFs who participated in this study and M. Marshall at NHS England who pseudonymized the electronic health records. This report is independent research funded by the Department of Health and Social Care (COVID-19 surveillance studies). A.H. is supported by Health Data Research UK (grant no. LOND1), which is funded by the UK Medical Research Council, Engineering and Physical Sciences Research Council, Economic and Social Research Council, Department of Health and Social Care (England), Chief Scientist Office of the Scottish Government Health and Social Care Directorates, Health and Social Care Research and Development Division (Welsh Government), Public Health Agency (Northern Ireland), British Heart Foundation and Wellcome Trust. L.S. is funded by an NIHR Clinician Scientist Award (no. CS-2016-007). M.K. is funded by a Wellcome Trust Clinical PhD Fellowship (no. 222907/Z/21/Z). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. The views expressed in this publication are those of the authors and not necessarily those of the NHS, Public Health England or the UK Government Department of Health and Social Care. Funding Information: We thank the staff and residents in the LTCFs who participated in this study and M. Marshall at NHS England who pseudonymized the electronic health records. This report is independent research funded by the Department of Health and Social Care (COVID-19 surveillance studies). A.H. is supported by Health Data Research UK (grant no. LOND1), which is funded by the UK Medical Research Council, Engineering and Physical Sciences Research Council, Economic and Social Research Council, Department of Health and Social Care (England), Chief Scientist Office of the Scottish Government Health and Social Care Directorates, Health and Social Care Research and Development Division (Welsh Government), Public Health Agency (Northern Ireland), British Heart Foundation and Wellcome Trust. L.S. is funded by an NIHR Clinician Scientist Award (no. CS-2016-007). M.K. is funded by a Wellcome Trust Clinical PhD Fellowship (no. 222907/Z/21/Z). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. The views expressed in this publication are those of the authors and not necessarily those of the NHS, Public Health England or the UK Government Department of Health and Social Care. Publisher Copyright: {\textcopyright} 2022, The Author(s).",

year = "2022",

month = jun,

doi = "10.1038/s43587-022-00224-w",

language = "English",

volume = "2",

pages = "536--547",

journal = "Nature Aging",

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Tut, G, Lancaster, T, Butler, MS, Sylla, P, Spalkova, E, Bone, D, Kaur, N, Bentley, C, Amin, U, Jadir, AT, Hulme, S, Ayodel, M, Dowell, AC, Pearce, H, Zuo, J, Margielewska-Davies, S, Verma, K, Nicol, S, Begum, J, Jinks, E, Tut, E, Bruton, R, Krutikov, M, Shrotri, M, Giddings, R, Azmi, B, Fuller, C, Irwin-Singer, A, Hayward, A, Copas, A, Shallcross, L & Moss, P 2022, 'Robust SARS-CoV-2-specific and heterologous immune responses in vaccine-naïve residents of long-term care facilities who survive natural infection', Nature Aging, vol. 2, no. 6, pp. 536-547. https://doi.org/10.1038/s43587-022-00224-w

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T1 - Robust SARS-CoV-2-specific and heterologous immune responses in vaccine-naïve residents of long-term care facilities who survive natural infection

AU - Tut, Gokhan

AU - Lancaster, Tara

AU - Butler, Megan S.

AU - Sylla, Panagiota

AU - Spalkova, Eliska

AU - Bone, David

AU - Kaur, Nayandeep

AU - Bentley, Christopher

AU - Amin, Umayr

AU - Jadir, Azar T.

AU - Hulme, Samuel

AU - Ayodel, Morenike

AU - Dowell, Alexander C.

AU - Pearce, Hayden

AU - Zuo, Jianmin

AU - Margielewska-Davies, Sandra

AU - Verma, Kriti

AU - Nicol, Samantha

AU - Begum, Jusnara

AU - Jinks, Elizabeth

AU - Tut, Elif

AU - Bruton, Rachel

AU - Krutikov, Maria

AU - Shrotri, Madhumita

AU - Giddings, Rebecca

AU - Azmi, Borscha

AU - Fuller, Chris

AU - Irwin-Singer, Aidan

AU - Hayward, Andrew

AU - Copas, Andrew

AU - Shallcross, Laura

AU - Moss, Paul

N1 - Funding Information: We thank the staff and residents in the LTCFs who participated in this study and M. Marshall at NHS England who pseudonymized the electronic health records. This report is independent research funded by the Department of Health and Social Care (COVID-19 surveillance studies). A.H. is supported by Health Data Research UK (grant no. LOND1), which is funded by the UK Medical Research Council, Engineering and Physical Sciences Research Council, Economic and Social Research Council, Department of Health and Social Care (England), Chief Scientist Office of the Scottish Government Health and Social Care Directorates, Health and Social Care Research and Development Division (Welsh Government), Public Health Agency (Northern Ireland), British Heart Foundation and Wellcome Trust. L.S. is funded by an NIHR Clinician Scientist Award (no. CS-2016-007). M.K. is funded by a Wellcome Trust Clinical PhD Fellowship (no. 222907/Z/21/Z). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. The views expressed in this publication are those of the authors and not necessarily those of the NHS, Public Health England or the UK Government Department of Health and Social Care. Funding Information: We thank the staff and residents in the LTCFs who participated in this study and M. Marshall at NHS England who pseudonymized the electronic health records. This report is independent research funded by the Department of Health and Social Care (COVID-19 surveillance studies). A.H. is supported by Health Data Research UK (grant no. LOND1), which is funded by the UK Medical Research Council, Engineering and Physical Sciences Research Council, Economic and Social Research Council, Department of Health and Social Care (England), Chief Scientist Office of the Scottish Government Health and Social Care Directorates, Health and Social Care Research and Development Division (Welsh Government), Public Health Agency (Northern Ireland), British Heart Foundation and Wellcome Trust. L.S. is funded by an NIHR Clinician Scientist Award (no. CS-2016-007). M.K. is funded by a Wellcome Trust Clinical PhD Fellowship (no. 222907/Z/21/Z). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. The views expressed in this publication are those of the authors and not necessarily those of the NHS, Public Health England or the UK Government Department of Health and Social Care. Publisher Copyright: © 2022, The Author(s).

PY - 2022/6

Y1 - 2022/6

N2 - We studied humoral and cellular immunity against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in 152 long-term care facility staff and 124 residents over a prospective 4-month period shortly after the first wave of infection in England. We show that residents of long-term care facilities developed high and stable levels of antibodies against spike protein and receptor-binding domain. Nucleocapsid-specific responses were also elevated but waned over time. Antibodies showed stable and equivalent levels of functional inhibition against spike-angiotensin-converting enzyme 2 binding in all age groups with comparable activity against viral variants of concern. SARS-CoV-2 seropositive donors showed high levels of antibodies to other beta-coronaviruses but serostatus did not impact humoral immunity to influenza or other respiratory syncytial viruses. SARS-CoV-2-specific cellular responses were similar across all ages but virus-specific populations showed elevated levels of activation in older donors. Thus, survivors of SARS-CoV-2 infection show a robust and stable immunity against the virus that does not negatively impact responses to other seasonal viruses.

AB - We studied humoral and cellular immunity against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in 152 long-term care facility staff and 124 residents over a prospective 4-month period shortly after the first wave of infection in England. We show that residents of long-term care facilities developed high and stable levels of antibodies against spike protein and receptor-binding domain. Nucleocapsid-specific responses were also elevated but waned over time. Antibodies showed stable and equivalent levels of functional inhibition against spike-angiotensin-converting enzyme 2 binding in all age groups with comparable activity against viral variants of concern. SARS-CoV-2 seropositive donors showed high levels of antibodies to other beta-coronaviruses but serostatus did not impact humoral immunity to influenza or other respiratory syncytial viruses. SARS-CoV-2-specific cellular responses were similar across all ages but virus-specific populations showed elevated levels of activation in older donors. Thus, survivors of SARS-CoV-2 infection show a robust and stable immunity against the virus that does not negatively impact responses to other seasonal viruses.

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Robust SARS-CoV-2-specific and heterologous immune responses in vaccine-naïve residents of long-term care facilities who survive natural infection

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