Natural T cell–mediated protection against seasonal and pandemic Influenza: results of the Flu Watch cohort study

Rationale: A high proportion of influenza infections are asymptomatic. Animal and human challenge studies and observational studies suggest T cells protect against disease among those infected, but the impact of T-cell immunity at the population level is unknown. Objectives: To investigate wheth...

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Main Authors: Hayward, Andrew C., Wang, Lili, Goonetilleke, Nilu, Fragaszy, Ellen B., Bermingham, Alison, Copas, Andrew, Dukes, Oliver, Millett, Elizabeth R.C., Nazareth, Irwin, Nguyen-Van-Tam, Jonathan S., Watson, John M., Zambon, Maria, Johnson, Anne M., McMichael, Andrew J.
Format: Article
Published: American Thoracic Society 2015
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Online Access:https://eprints.nottingham.ac.uk/41751/
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author Hayward, Andrew C.
Wang, Lili
Goonetilleke, Nilu
Fragaszy, Ellen B.
Bermingham, Alison
Copas, Andrew
Dukes, Oliver
Millett, Elizabeth R.C.
Nazareth, Irwin
Nguyen-Van-Tam, Jonathan S.
Watson, John M.
Zambon, Maria
Johnson, Anne M.
McMichael, Andrew J.
author_facet Hayward, Andrew C.
Wang, Lili
Goonetilleke, Nilu
Fragaszy, Ellen B.
Bermingham, Alison
Copas, Andrew
Dukes, Oliver
Millett, Elizabeth R.C.
Nazareth, Irwin
Nguyen-Van-Tam, Jonathan S.
Watson, John M.
Zambon, Maria
Johnson, Anne M.
McMichael, Andrew J.
author_sort Hayward, Andrew C.
building Nottingham Research Data Repository
collection Online Access
description Rationale: A high proportion of influenza infections are asymptomatic. Animal and human challenge studies and observational studies suggest T cells protect against disease among those infected, but the impact of T-cell immunity at the population level is unknown. Objectives: To investigate whether naturally preexisting T-cell responses targeting highly conserved internal influenza proteins could provide cross-protective immunity against pandemic and seasonal influenza. Methods: We quantified influenza A(H3N2) virus–specific T cells in a population cohort during seasonal and pandemic periods between 2006 and 2010. Follow-up included paired serology, symptom reporting, and polymerase chain reaction (PCR) investigation of symptomatic cases. Measurements and Main Results: A total of 1,414 unvaccinated individuals had baseline T-cell measurements (1,703 participant observation sets). T-cell responses to A(H3N2) virus nucleoprotein (NP) dominated and strongly cross-reacted with A(H1N1)pdm09 NP (P < 0.001) in participants lacking antibody to A(H1N1)pdm09. Comparison of paired preseason and post-season sera (1,431 sets) showed 205 (14%) had evidence of infection based on fourfold influenza antibody titer rises. The presence of NP-specific T cells before exposure to virus correlated with less symptomatic, PCR-positive influenza A (overall adjusted odds ratio, 0.27; 95% confidence interval, 0.11–0.68; P = 0.005, during pandemic [P = 0.047] and seasonal [P = 0.049] periods). Protection was independent of baseline antibodies. Influenza-specific T-cell responses were detected in 43%, indicating a substantial population impact. Conclusions: Naturally occurring cross-protective T-cell immunity protects against symptomatic PCR-confirmed disease in those with evidence of infection and helps to explain why many infections do not cause symptoms. Vaccines stimulating T cells may provide important cross-protective immunity.
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spelling nottingham-417512024-08-15T15:17:09Z https://eprints.nottingham.ac.uk/41751/ Natural T cell–mediated protection against seasonal and pandemic Influenza: results of the Flu Watch cohort study Hayward, Andrew C. Wang, Lili Goonetilleke, Nilu Fragaszy, Ellen B. Bermingham, Alison Copas, Andrew Dukes, Oliver Millett, Elizabeth R.C. Nazareth, Irwin Nguyen-Van-Tam, Jonathan S. Watson, John M. Zambon, Maria Johnson, Anne M. McMichael, Andrew J. Rationale: A high proportion of influenza infections are asymptomatic. Animal and human challenge studies and observational studies suggest T cells protect against disease among those infected, but the impact of T-cell immunity at the population level is unknown. Objectives: To investigate whether naturally preexisting T-cell responses targeting highly conserved internal influenza proteins could provide cross-protective immunity against pandemic and seasonal influenza. Methods: We quantified influenza A(H3N2) virus–specific T cells in a population cohort during seasonal and pandemic periods between 2006 and 2010. Follow-up included paired serology, symptom reporting, and polymerase chain reaction (PCR) investigation of symptomatic cases. Measurements and Main Results: A total of 1,414 unvaccinated individuals had baseline T-cell measurements (1,703 participant observation sets). T-cell responses to A(H3N2) virus nucleoprotein (NP) dominated and strongly cross-reacted with A(H1N1)pdm09 NP (P < 0.001) in participants lacking antibody to A(H1N1)pdm09. Comparison of paired preseason and post-season sera (1,431 sets) showed 205 (14%) had evidence of infection based on fourfold influenza antibody titer rises. The presence of NP-specific T cells before exposure to virus correlated with less symptomatic, PCR-positive influenza A (overall adjusted odds ratio, 0.27; 95% confidence interval, 0.11–0.68; P = 0.005, during pandemic [P = 0.047] and seasonal [P = 0.049] periods). Protection was independent of baseline antibodies. Influenza-specific T-cell responses were detected in 43%, indicating a substantial population impact. Conclusions: Naturally occurring cross-protective T-cell immunity protects against symptomatic PCR-confirmed disease in those with evidence of infection and helps to explain why many infections do not cause symptoms. Vaccines stimulating T cells may provide important cross-protective immunity. American Thoracic Society 2015-06-15 Article PeerReviewed Hayward, Andrew C., Wang, Lili, Goonetilleke, Nilu, Fragaszy, Ellen B., Bermingham, Alison, Copas, Andrew, Dukes, Oliver, Millett, Elizabeth R.C., Nazareth, Irwin, Nguyen-Van-Tam, Jonathan S., Watson, John M., Zambon, Maria, Johnson, Anne M. and McMichael, Andrew J. (2015) Natural T cell–mediated protection against seasonal and pandemic Influenza: results of the Flu Watch cohort study. American Journal of Respiratory and Critical Care Medicine, 191 (12). pp. 1422-1431. ISSN 1535-4970 cellular immunity; T lymphocytes; cohort studies http://www.atsjournals.org/doi/10.1164/rccm.201411-1988OC doi:10.1164/rccm.201411-1988OC doi:10.1164/rccm.201411-1988OC
spellingShingle cellular immunity; T lymphocytes; cohort studies
Hayward, Andrew C.
Wang, Lili
Goonetilleke, Nilu
Fragaszy, Ellen B.
Bermingham, Alison
Copas, Andrew
Dukes, Oliver
Millett, Elizabeth R.C.
Nazareth, Irwin
Nguyen-Van-Tam, Jonathan S.
Watson, John M.
Zambon, Maria
Johnson, Anne M.
McMichael, Andrew J.
Natural T cell–mediated protection against seasonal and pandemic Influenza: results of the Flu Watch cohort study
title Natural T cell–mediated protection against seasonal and pandemic Influenza: results of the Flu Watch cohort study
title_full Natural T cell–mediated protection against seasonal and pandemic Influenza: results of the Flu Watch cohort study
title_fullStr Natural T cell–mediated protection against seasonal and pandemic Influenza: results of the Flu Watch cohort study
title_full_unstemmed Natural T cell–mediated protection against seasonal and pandemic Influenza: results of the Flu Watch cohort study
title_short Natural T cell–mediated protection against seasonal and pandemic Influenza: results of the Flu Watch cohort study
title_sort natural t cell–mediated protection against seasonal and pandemic influenza: results of the flu watch cohort study
topic cellular immunity; T lymphocytes; cohort studies
url https://eprints.nottingham.ac.uk/41751/
https://eprints.nottingham.ac.uk/41751/
https://eprints.nottingham.ac.uk/41751/