Durability of SARS-CoV-2-Specific T-Cell Responses at 12 Months Postinfection

Zhongyan Lu; Eric D. Laing; Jarina Pena Damata; Katherine Pohida; Marana S. Tso; Emily C. Samuels; Nusrat J. Epsi; Batsukh Dorjbal; Camille Lake; Stephanie A. Richard; Ryan C. Maves; David A. Lindholm; Julia S. Rozman; Caroline English; Nikhil Huprikar; Katrin Mende; Rhonda E. Colombo; Christopher J. Colombo; Christopher C. Broder; Anuradha Ganesan; Charlotte A. Lanteri; Brian K. Agan; David Tribble; Mark P. Simons; Clifton L. Dalgard; Paul W. Blair; Josh Chenoweth; Simon D. Pollett; Andrew L. Snow; Timothy H. Burgess; Allison M.W. Malloy; J. Cowden; S. Deleon; A. Markelz; K. Mende; T. Merritt; S. Merritt; R. Walter; T. Wellington; S. Bazan; P. Kay; L. Brandon; N. Dimascio-Johnson; E. Ewers; K. Gallagher; D. Larson; M. Odom; A. Rutt; D. Clark; S. Chambers; C. Conlon; K. Everson; P. Faestel; T. Ferguson; L. Gordon; S. Grogan; S. Lis; C. Mount; D. Musfeldt; W. Robb-Mcgrath; R. Sainato; C. Schofield; C. Skinner; M. Stein; M. Switzer; M. Timlin; S. Wood; G. Atwood; S. Banks; R. Carpenter; C. Eickhoff; K. Kronmann; T. Lalani; T. Lee; A. Smith; R. Tant; T. Warkentien; J. Arnold; C. Berjohn; S. Cammarata; S. Husain; N. Kirkland; A. Lane; J. Parrish; G. Utz; S. Chi; E. Filan; K. Fong; T. Horseman; M. Jones; A. Kanis; A. Kayatani; W. Londeree; C. Madar; J. Masel; M. McMahon; K. Miyasato; G. Murphy; V. Ngauy; E. Schoenman; C. Uyehara; R. Villacorta Lyew; C. Byrne; K. Chung; Christian Coles; C. Fox; M. Grother; D. Gunasekera; P. Hickey; J. Livezey; C. Morales; T. Oliver; E. Parmelee; J. Rusiecki; M. Sanchez-Edwards; A. Scher; A. Fries; I. Barahona; D. Gunasekera; M. Oyeneyin; M. Banda; B. Davis; T. Hunter; O. Ikpekpe-Magege; S. Kemp; R. Mody; R. Resendez; P. Sandoval; M. Wiggins

doi:10.1093/infdis/jiab543

Durability of SARS-CoV-2-Specific T-Cell Responses at 12 Months Postinfection

Zhongyan Lu, Eric D. Laing, Jarina Pena Damata, Katherine Pohida, Marana S. Tso, Emily C. Samuels, Nusrat J. Epsi, Batsukh Dorjbal, Camille Lake, Stephanie A. Richard, Ryan C. Maves, David A. Lindholm, Julia S. Rozman, Caroline English, Nikhil Huprikar, Katrin Mende, Rhonda E. Colombo, Christopher J. Colombo, Christopher C. Broder, Anuradha GanesanCharlotte A. Lanteri, Brian K. Agan, David Tribble, Mark P. Simons, Clifton L. Dalgard, Paul W. Blair, Josh Chenoweth, Simon D. Pollett, Andrew L. Snow, Timothy H. Burgess, Allison M.W. Malloy, J. Cowden, S. Deleon, A. Markelz, K. Mende, T. Merritt, S. Merritt, R. Walter, T. Wellington, S. Bazan, P. Kay, L. Brandon, N. Dimascio-Johnson, E. Ewers, K. Gallagher, D. Larson, M. Odom, A. Rutt, D. Clark, S. Chambers, C. Conlon, K. Everson, P. Faestel, T. Ferguson, L. Gordon, S. Grogan, S. Lis, C. Mount, D. Musfeldt, W. Robb-Mcgrath, R. Sainato, C. Schofield, C. Skinner, M. Stein, M. Switzer, M. Timlin, S. Wood, G. Atwood, S. Banks, R. Carpenter, C. Eickhoff, K. Kronmann, T. Lalani, T. Lee, A. Smith, R. Tant, T. Warkentien, J. Arnold, C. Berjohn, S. Cammarata, S. Husain, N. Kirkland, A. Lane, J. Parrish, G. Utz, S. Chi, E. Filan, K. Fong, T. Horseman, M. Jones, A. Kanis, A. Kayatani, W. Londeree, C. Madar, J. Masel, M. McMahon, K. Miyasato, G. Murphy, V. Ngauy, E. Schoenman, C. Uyehara, R. Villacorta Lyew, C. Byrne, K. Chung, Christian Coles, C. Fox, M. Grother, D. Gunasekera, P. Hickey, J. Livezey, C. Morales, T. Oliver, E. Parmelee, J. Rusiecki, M. Sanchez-Edwards, A. Scher, A. Fries, I. Barahona, D. Gunasekera, M. Oyeneyin, M. Banda, B. Davis, T. Hunter, O. Ikpekpe-Magege, S. Kemp, R. Mody, R. Resendez, P. Sandoval, M. Wiggins

School of Medicine

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

Abstract

Background: Characterizing the longevity and quality of cellular immune responses to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) enhances understanding of coronavirus disease 2019 (COVID-19) immunity that influences clinical outcomes. Prior studies suggest SARS-CoV-2-specific T cells are present in peripheral blood 10 months after infection. Analysis of the function, durability, and diversity of cellular response long after natural infection, over a range of ages and disease phenotypes, is needed to identify preventative and therapeutic interventions. Methods: We identified participants in our multisite longitudinal, prospective cohort study 12 months after SARS-CoV-2 infection representing a range of disease severity. We investigated function, phenotypes, and frequency of T cells specific for SARS-CoV-2 using intracellular cytokine staining and spectral flow cytometry, and compared magnitude of SARS-CoV-2-specific antibodies. Results: SARS-CoV-2-specific antibodies and T cells were detected 12 months postinfection. Severe acute illness was associated with higher frequencies of SARS-CoV-2-specific CD4 T cells and antibodies at 12 months. In contrast, polyfunctional and cytotoxic T cells responsive to SARS-CoV-2 were identified in participants over a wide spectrum of disease severity. Conclusions: SARS-CoV-2 infection induces polyfunctional memory T cells detectable at 12 months postinfection, with higher frequency noted in those who experienced severe disease.

Original language	English (US)
Pages (from-to)	2010-2019
Number of pages	10
Journal	Journal of Infectious Diseases
Volume	224
Issue number	12
DOIs	https://doi.org/10.1093/infdis/jiab543
State	Published - Dec 15 2021

Keywords

12 months
COVID-19
SARS-CoV-2
T cell
antibody
cytotoxicity
durability
memory
polyfunctionality

ASJC Scopus subject areas

General Medicine

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10.1093/infdis/jiab543

Cite this

Lu, Z., Laing, E. D., Pena Damata, J., Pohida, K., Tso, M. S., Samuels, E. C., Epsi, N. J., Dorjbal, B., Lake, C., Richard, S. A., Maves, R. C., Lindholm, D. A., Rozman, J. S., English, C., Huprikar, N., Mende, K., Colombo, R. E., Colombo, C. J., Broder, C. C., ... Wiggins, M. (2021). Durability of SARS-CoV-2-Specific T-Cell Responses at 12 Months Postinfection. Journal of Infectious Diseases, 224(12), 2010-2019. https://doi.org/10.1093/infdis/jiab543

Lu, Z, Laing, ED, Pena Damata, J, Pohida, K, Tso, MS, Samuels, EC, Epsi, NJ, Dorjbal, B, Lake, C, Richard, SA, Maves, RC, Lindholm, DA, Rozman, JS, English, C, Huprikar, N, Mende, K, Colombo, RE, Colombo, CJ, Broder, CC, Ganesan, A, Lanteri, CA, Agan, BK, Tribble, D, Simons, MP, Dalgard, CL, Blair, PW, Chenoweth, J, Pollett, SD, Snow, AL, Burgess, TH, Malloy, AMW, Cowden, J, Deleon, S, Markelz, A, Mende, K, Merritt, T, Merritt, S, Walter, R, Wellington, T, Bazan, S, Kay, P, Brandon, L, Dimascio-Johnson, N, Ewers, E, Gallagher, K, Larson, D, Odom, M, Rutt, A, Clark, D, Chambers, S, Conlon, C, Everson, K, Faestel, P, Ferguson, T, Gordon, L, Grogan, S, Lis, S, Mount, C, Musfeldt, D, Robb-Mcgrath, W, Sainato, R, Schofield, C, Skinner, C, Stein, M, Switzer, M, Timlin, M, Wood, S, Atwood, G, Banks, S, Carpenter, R, Eickhoff, C, Kronmann, K, Lalani, T, Lee, T, Smith, A, Tant, R, Warkentien, T, Arnold, J, Berjohn, C, Cammarata, S, Husain, S, Kirkland, N, Lane, A, Parrish, J, Utz, G, Chi, S, Filan, E, Fong, K, Horseman, T, Jones, M, Kanis, A, Kayatani, A, Londeree, W, Madar, C, Masel, J, McMahon, M, Miyasato, K, Murphy, G, Ngauy, V, Schoenman, E, Uyehara, C, Villacorta Lyew, R, Byrne, C, Chung, K, Coles, C, Fox, C, Grother, M, Gunasekera, D, Hickey, P, Livezey, J, Morales, C, Oliver, T, Parmelee, E, Rusiecki, J, Sanchez-Edwards, M, Scher, A, Fries, A, Barahona, I, Gunasekera, D, Oyeneyin, M, Banda, M, Davis, B, Hunter, T, Ikpekpe-Magege, O, Kemp, S, Mody, R, Resendez, R, Sandoval, P & Wiggins, M 2021, 'Durability of SARS-CoV-2-Specific T-Cell Responses at 12 Months Postinfection', Journal of Infectious Diseases, vol. 224, no. 12, pp. 2010-2019. https://doi.org/10.1093/infdis/jiab543

@article{21d8d380caea4ea3920e9eb433dbee33,

title = "Durability of SARS-CoV-2-Specific T-Cell Responses at 12 Months Postinfection",

abstract = "Background: Characterizing the longevity and quality of cellular immune responses to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) enhances understanding of coronavirus disease 2019 (COVID-19) immunity that influences clinical outcomes. Prior studies suggest SARS-CoV-2-specific T cells are present in peripheral blood 10 months after infection. Analysis of the function, durability, and diversity of cellular response long after natural infection, over a range of ages and disease phenotypes, is needed to identify preventative and therapeutic interventions. Methods: We identified participants in our multisite longitudinal, prospective cohort study 12 months after SARS-CoV-2 infection representing a range of disease severity. We investigated function, phenotypes, and frequency of T cells specific for SARS-CoV-2 using intracellular cytokine staining and spectral flow cytometry, and compared magnitude of SARS-CoV-2-specific antibodies. Results: SARS-CoV-2-specific antibodies and T cells were detected 12 months postinfection. Severe acute illness was associated with higher frequencies of SARS-CoV-2-specific CD4 T cells and antibodies at 12 months. In contrast, polyfunctional and cytotoxic T cells responsive to SARS-CoV-2 were identified in participants over a wide spectrum of disease severity. Conclusions: SARS-CoV-2 infection induces polyfunctional memory T cells detectable at 12 months postinfection, with higher frequency noted in those who experienced severe disease.",

keywords = "12 months, COVID-19, SARS-CoV-2, T cell, antibody, cytotoxicity, durability, memory, polyfunctionality",

author = "Zhongyan Lu and Laing, {Eric D.} and {Pena Damata}, Jarina and Katherine Pohida and Tso, {Marana S.} and Samuels, {Emily C.} and Epsi, {Nusrat J.} and Batsukh Dorjbal and Camille Lake and Richard, {Stephanie A.} and Maves, {Ryan C.} and Lindholm, {David A.} and Rozman, {Julia S.} and Caroline English and Nikhil Huprikar and Katrin Mende and Colombo, {Rhonda E.} and Colombo, {Christopher J.} and Broder, {Christopher C.} and Anuradha Ganesan and Lanteri, {Charlotte A.} and Agan, {Brian K.} and David Tribble and Simons, {Mark P.} and Dalgard, {Clifton L.} and Blair, {Paul W.} and Josh Chenoweth and Pollett, {Simon D.} and Snow, {Andrew L.} and Burgess, {Timothy H.} and Malloy, {Allison M.W.} and J. Cowden and S. Deleon and A. Markelz and K. Mende and T. Merritt and S. Merritt and R. Walter and T. Wellington and S. Bazan and P. Kay and L. Brandon and N. Dimascio-Johnson and E. Ewers and K. Gallagher and D. Larson and M. Odom and A. Rutt and D. Clark and S. Chambers and C. Conlon and K. Everson and P. Faestel and T. Ferguson and L. Gordon and S. Grogan and S. Lis and C. Mount and D. Musfeldt and W. Robb-Mcgrath and R. Sainato and C. Schofield and C. Skinner and M. Stein and M. Switzer and M. Timlin and S. Wood and G. Atwood and S. Banks and R. Carpenter and C. Eickhoff and K. Kronmann and T. Lalani and T. Lee and A. Smith and R. Tant and T. Warkentien and J. Arnold and C. Berjohn and S. Cammarata and S. Husain and N. Kirkland and A. Lane and J. Parrish and G. Utz and S. Chi and E. Filan and K. Fong and T. Horseman and M. Jones and A. Kanis and A. Kayatani and W. Londeree and C. Madar and J. Masel and M. McMahon and K. Miyasato and G. Murphy and V. Ngauy and E. Schoenman and C. Uyehara and {Villacorta Lyew}, R. and C. Byrne and K. Chung and Christian Coles and C. Fox and M. Grother and D. Gunasekera and P. Hickey and J. Livezey and C. Morales and T. Oliver and E. Parmelee and J. Rusiecki and M. Sanchez-Edwards and A. Scher and A. Fries and I. Barahona and D. Gunasekera and M. Oyeneyin and M. Banda and B. Davis and T. Hunter and O. Ikpekpe-Magege and S. Kemp and R. Mody and R. Resendez and P. Sandoval and M. Wiggins",

note = "Publisher Copyright: {\textcopyright} 2021 Published by Oxford University Press for the Infectious Diseases Society of America 2021.",

year = "2021",

month = dec,

day = "15",

doi = "10.1093/infdis/jiab543",

language = "English (US)",

volume = "224",

pages = "2010--2019",

journal = "Journal of Infectious Diseases",

issn = "0022-1899",

publisher = "Oxford University Press",

number = "12",

}

TY - JOUR

T1 - Durability of SARS-CoV-2-Specific T-Cell Responses at 12 Months Postinfection

AU - Lu, Zhongyan

AU - Laing, Eric D.

AU - Pena Damata, Jarina

AU - Pohida, Katherine

AU - Tso, Marana S.

AU - Samuels, Emily C.

AU - Epsi, Nusrat J.

AU - Dorjbal, Batsukh

AU - Lake, Camille

AU - Richard, Stephanie A.

AU - Maves, Ryan C.

AU - Lindholm, David A.

AU - Rozman, Julia S.

AU - English, Caroline

AU - Huprikar, Nikhil

AU - Mende, Katrin

AU - Colombo, Rhonda E.

AU - Colombo, Christopher J.

AU - Broder, Christopher C.

AU - Ganesan, Anuradha

AU - Lanteri, Charlotte A.

AU - Agan, Brian K.

AU - Tribble, David

AU - Simons, Mark P.

AU - Dalgard, Clifton L.

AU - Blair, Paul W.

AU - Chenoweth, Josh

AU - Pollett, Simon D.

AU - Snow, Andrew L.

AU - Burgess, Timothy H.

AU - Malloy, Allison M.W.

AU - Cowden, J.

AU - Deleon, S.

AU - Markelz, A.

AU - Mende, K.

AU - Merritt, T.

AU - Merritt, S.

AU - Walter, R.

AU - Wellington, T.

AU - Bazan, S.

AU - Kay, P.

AU - Brandon, L.

AU - Dimascio-Johnson, N.

AU - Ewers, E.

AU - Gallagher, K.

AU - Larson, D.

AU - Odom, M.

AU - Rutt, A.

AU - Clark, D.

AU - Chambers, S.

AU - Conlon, C.

AU - Everson, K.

AU - Faestel, P.

AU - Ferguson, T.

AU - Gordon, L.

AU - Grogan, S.

AU - Lis, S.

AU - Mount, C.

AU - Musfeldt, D.

AU - Robb-Mcgrath, W.

AU - Sainato, R.

AU - Schofield, C.

AU - Skinner, C.

AU - Stein, M.

AU - Switzer, M.

AU - Timlin, M.

AU - Wood, S.

AU - Atwood, G.

AU - Banks, S.

AU - Carpenter, R.

AU - Eickhoff, C.

AU - Kronmann, K.

AU - Lalani, T.

AU - Lee, T.

AU - Smith, A.

AU - Tant, R.

AU - Warkentien, T.

AU - Arnold, J.

AU - Berjohn, C.

AU - Cammarata, S.

AU - Husain, S.

AU - Kirkland, N.

AU - Lane, A.

AU - Parrish, J.

AU - Utz, G.

AU - Chi, S.

AU - Filan, E.

AU - Fong, K.

AU - Horseman, T.

AU - Jones, M.

AU - Kanis, A.

AU - Kayatani, A.

AU - Londeree, W.

AU - Madar, C.

AU - Masel, J.

AU - McMahon, M.

AU - Miyasato, K.

AU - Murphy, G.

AU - Ngauy, V.

AU - Schoenman, E.

AU - Uyehara, C.

AU - Villacorta Lyew, R.

AU - Byrne, C.

AU - Chung, K.

AU - Coles, Christian

AU - Fox, C.

AU - Grother, M.

AU - Gunasekera, D.

AU - Hickey, P.

AU - Livezey, J.

AU - Morales, C.

AU - Oliver, T.

AU - Parmelee, E.

AU - Rusiecki, J.

AU - Sanchez-Edwards, M.

AU - Scher, A.

AU - Fries, A.

AU - Barahona, I.

AU - Gunasekera, D.

AU - Oyeneyin, M.

AU - Banda, M.

AU - Davis, B.

AU - Hunter, T.

AU - Ikpekpe-Magege, O.

AU - Kemp, S.

AU - Mody, R.

AU - Resendez, R.

AU - Sandoval, P.

AU - Wiggins, M.

PY - 2021/12/15

Y1 - 2021/12/15

N2 - Background: Characterizing the longevity and quality of cellular immune responses to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) enhances understanding of coronavirus disease 2019 (COVID-19) immunity that influences clinical outcomes. Prior studies suggest SARS-CoV-2-specific T cells are present in peripheral blood 10 months after infection. Analysis of the function, durability, and diversity of cellular response long after natural infection, over a range of ages and disease phenotypes, is needed to identify preventative and therapeutic interventions. Methods: We identified participants in our multisite longitudinal, prospective cohort study 12 months after SARS-CoV-2 infection representing a range of disease severity. We investigated function, phenotypes, and frequency of T cells specific for SARS-CoV-2 using intracellular cytokine staining and spectral flow cytometry, and compared magnitude of SARS-CoV-2-specific antibodies. Results: SARS-CoV-2-specific antibodies and T cells were detected 12 months postinfection. Severe acute illness was associated with higher frequencies of SARS-CoV-2-specific CD4 T cells and antibodies at 12 months. In contrast, polyfunctional and cytotoxic T cells responsive to SARS-CoV-2 were identified in participants over a wide spectrum of disease severity. Conclusions: SARS-CoV-2 infection induces polyfunctional memory T cells detectable at 12 months postinfection, with higher frequency noted in those who experienced severe disease.

AB - Background: Characterizing the longevity and quality of cellular immune responses to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) enhances understanding of coronavirus disease 2019 (COVID-19) immunity that influences clinical outcomes. Prior studies suggest SARS-CoV-2-specific T cells are present in peripheral blood 10 months after infection. Analysis of the function, durability, and diversity of cellular response long after natural infection, over a range of ages and disease phenotypes, is needed to identify preventative and therapeutic interventions. Methods: We identified participants in our multisite longitudinal, prospective cohort study 12 months after SARS-CoV-2 infection representing a range of disease severity. We investigated function, phenotypes, and frequency of T cells specific for SARS-CoV-2 using intracellular cytokine staining and spectral flow cytometry, and compared magnitude of SARS-CoV-2-specific antibodies. Results: SARS-CoV-2-specific antibodies and T cells were detected 12 months postinfection. Severe acute illness was associated with higher frequencies of SARS-CoV-2-specific CD4 T cells and antibodies at 12 months. In contrast, polyfunctional and cytotoxic T cells responsive to SARS-CoV-2 were identified in participants over a wide spectrum of disease severity. Conclusions: SARS-CoV-2 infection induces polyfunctional memory T cells detectable at 12 months postinfection, with higher frequency noted in those who experienced severe disease.

KW - 12 months

KW - COVID-19

KW - SARS-CoV-2

KW - T cell

KW - antibody

KW - cytotoxicity

KW - durability

KW - memory

KW - polyfunctionality

UR - http://www.scopus.com/inward/record.url?scp=85122770832&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85122770832&partnerID=8YFLogxK

U2 - 10.1093/infdis/jiab543

DO - 10.1093/infdis/jiab543

M3 - Article

C2 - 34673956

AN - SCOPUS:85122770832

SN - 0022-1899

VL - 224

SP - 2010

EP - 2019

JO - Journal of Infectious Diseases

JF - Journal of Infectious Diseases

IS - 12

ER -

Durability of SARS-CoV-2-Specific T-Cell Responses at 12 Months Postinfection

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Keywords

ASJC Scopus subject areas

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