TY - JOUR
T1 - Influenza virus infection history shapes antibody responses to influenza vaccination
AU - Auladell, Maria
AU - Phuong, Hoang Vu Mai
AU - Mai, Le Thi Quynh
AU - Tseng, Yeu Yang
AU - Carolan, Louise
AU - Wilks, Sam
AU - Thai, Pham Quang
AU - Price, David
AU - Duong, Nguyen Thanh
AU - Hang, Nguyen Le Khang
AU - Thanh, Le Thi
AU - Thuong, Nguyen Thi Hong
AU - Huong, Tran Thi Kieu
AU - Diep, Nguyen Thi Ngoc
AU - Bich, Vu Thi Ngoc
AU - Khvorov, Arseniy
AU - Hensen, Luca
AU - Duong, Tran Nhu
AU - Kedzierska, Katherine
AU - Anh, Dang Duc
AU - Wertheim, Heiman
AU - Boyd, Scott D.
AU - Good-Jacobson, Kim L.
AU - Smith, Derek
AU - Barr, Ian
AU - Sullivan, Sheena
AU - van Doorn, H. Rogier
AU - Fox, Annette
N1 - Funding Information:
Funding for this study was provided by the National Health and Medical Research Council, Australia (grant 1103367 to A.F.) and National Foundation for Science and Technology Development (NAFOSTED 108.04-2019.08, L.T.Q.M.). The WHO Collaborating Centre for Reference and Research on Influenza is funded by the Australian Government Department of Health. The Oxford University Clinical Research Unit ? Hanoi and H.R.v.D. are funded through Wellcome Africa Asia program grants (089276/Z/09/Z and 106680/Z/14/Z). We are grateful to the Ha Nam Preventive Medicine Centre and People?s Committees of Thanh Liem District for their support and the people of Thanh Ha Commune for participating in this study. We would like to thank the Thanh Ha Commune health workers for their dedication to conducting active surveillance and cross-sectional surveys. We also wish to thank the Ministry of Health of Vietnam for their continuing support of the research collaboration between the Oxford University Clinical Research Unit and the National Institute for Hygiene and Epidemiology. We are grateful to members of the Oxford University Clinical Research Unit, including P. Horby for his role in establishing the Ha Nam cohort, N. Nguyen Minh Trang for project coordination and B. Huyen Trang for administrative support. A. Malet, H. Peck and Y.-M. Deng and their staff at Melbourne WHO Collaborating Centre for Reference and Research performed initial isolation and characterization of many of the influenza viruses used. We thank S. Sanchez for assisting with microneutralization assays. Thanks also to K. Subbarao and N. Thi Hoang Oanh for helpful comments on the manuscript. K.K. was supported by the Australian National Health and Medical Research Council (Leadership Investigator Fellowship 1173871). M.A. and L.H. were supported by the Melbourne International Research Scholarship and the Melbourne International Fee Remission Scholarship from the University of Melbourne. The funders had no role in the conduct of the study.
Funding Information:
Funding for this study was provided by the National Health and Medical Research Council, Australia (grant 1103367 to A.F.) and National Foundation for Science and Technology Development (NAFOSTED 108.04-2019.08, L.T.Q.M.). The WHO Collaborating Centre for Reference and Research on Influenza is funded by the Australian Government Department of Health. The Oxford University Clinical Research Unit – Hanoi and H.R.v.D. are funded through Wellcome Africa Asia program grants (089276/Z/09/Z and 106680/Z/14/Z). We are grateful to the Ha Nam Preventive Medicine Centre and People’s Committees of Thanh Liem District for their support and the people of Thanh Ha Commune for participating in this study. We would like to thank the Thanh Ha Commune health workers for their dedication to conducting active surveillance and cross-sectional surveys. We also wish to thank the Ministry of Health of Vietnam for their continuing support of the research collaboration between the Oxford University Clinical Research Unit and the National Institute for Hygiene and Epidemiology. We are grateful to members of the Oxford University Clinical Research Unit, including P. Horby for his role in establishing the Ha Nam cohort, N. Nguyen Minh Trang for project coordination and B. Huyen Trang for administrative support. A. Malet, H. Peck and Y.-M. Deng and their staff at Melbourne WHO Collaborating Centre for Reference and Research performed initial isolation and characterization of many of the influenza viruses used. We thank S. Sanchez for assisting with microneutralization assays. Thanks also to K. Subbarao and N. Thi Hoang Oanh for helpful comments on the manuscript. K.K. was supported by the Australian National Health and Medical Research Council (Leadership Investigator Fellowship 1173871). M.A. and L.H. were supported by the Melbourne International Research Scholarship and the Melbourne International Fee Remission Scholarship from the University of Melbourne. The funders had no role in the conduct of the study.
Publisher Copyright:
© 2022, The Author(s), under exclusive licence to Springer Nature America, Inc.
PY - 2022/2
Y1 - 2022/2
N2 - Studies of successive vaccination suggest that immunological memory against past influenza viruses may limit responses to vaccines containing current strains. The impact of memory induced by prior infection is rarely considered and is difficult to ascertain, because infections are often subclinical. This study investigated influenza vaccination among adults from the Ha Nam cohort (Vietnam), who were purposefully selected to include 72 with and 28 without documented influenza A(H3N2) infection during the preceding 9 years (Australian New Zealand Clinical Trials Registry 12621000110886). The primary outcome was the effect of prior influenza A(H3N2) infection on hemagglutinin-inhibiting antibody responses induced by a locally available influenza vaccine administered in November 2016. Baseline and postvaccination sera were titrated against 40 influenza A(H3N2) strains spanning 1968–2018. At each time point (baseline, day 14 and day 280), geometric mean antibody titers against 2008–2018 strains were higher among participants with recent infection (34 (29–40), 187 (154–227) and 86 (72–103)) than among participants without recent infection (19 (17–22), 91 (64–130) and 38 (30–49)). On days 14 and 280, mean titer rises against 2014–2018 strains were 6.1-fold (5.0- to 7.4-fold) and 2.6-fold (2.2- to 3.1-fold) for participants with recent infection versus 4.8-fold (3.5- to 6.7-fold) and 1.9-fold (1.5- to 2.3-fold) for those without. One of 72 vaccinees with recent infection versus 4 of 28 without developed symptomatic A(H3N2) infection in the season after vaccination (P = 0.021). The range of A(H3N2) viruses recognized by vaccine-induced antibodies was associated with the prior infection strain. These results suggest that recall of immunological memory induced by prior infection enhances antibody responses to inactivated influenza vaccine and is important to attain protective antibody titers.
AB - Studies of successive vaccination suggest that immunological memory against past influenza viruses may limit responses to vaccines containing current strains. The impact of memory induced by prior infection is rarely considered and is difficult to ascertain, because infections are often subclinical. This study investigated influenza vaccination among adults from the Ha Nam cohort (Vietnam), who were purposefully selected to include 72 with and 28 without documented influenza A(H3N2) infection during the preceding 9 years (Australian New Zealand Clinical Trials Registry 12621000110886). The primary outcome was the effect of prior influenza A(H3N2) infection on hemagglutinin-inhibiting antibody responses induced by a locally available influenza vaccine administered in November 2016. Baseline and postvaccination sera were titrated against 40 influenza A(H3N2) strains spanning 1968–2018. At each time point (baseline, day 14 and day 280), geometric mean antibody titers against 2008–2018 strains were higher among participants with recent infection (34 (29–40), 187 (154–227) and 86 (72–103)) than among participants without recent infection (19 (17–22), 91 (64–130) and 38 (30–49)). On days 14 and 280, mean titer rises against 2014–2018 strains were 6.1-fold (5.0- to 7.4-fold) and 2.6-fold (2.2- to 3.1-fold) for participants with recent infection versus 4.8-fold (3.5- to 6.7-fold) and 1.9-fold (1.5- to 2.3-fold) for those without. One of 72 vaccinees with recent infection versus 4 of 28 without developed symptomatic A(H3N2) infection in the season after vaccination (P = 0.021). The range of A(H3N2) viruses recognized by vaccine-induced antibodies was associated with the prior infection strain. These results suggest that recall of immunological memory induced by prior infection enhances antibody responses to inactivated influenza vaccine and is important to attain protective antibody titers.
UR - http://www.scopus.com/inward/record.url?scp=85124721351&partnerID=8YFLogxK
U2 - 10.1038/s41591-022-01690-w
DO - 10.1038/s41591-022-01690-w
M3 - Article
C2 - 35177857
AN - SCOPUS:85124721351
SN - 1078-8956
VL - 28
SP - 363
EP - 372
JO - Nature Medicine
JF - Nature Medicine
IS - 2
ER -