Determinants of epidemic size and the impacts of lulls in seasonal influenza virus circulation

Simon P.J. de Jong; Zandra C. Felix Garza; Joseph C. Gibson; Sarah van Leeuwen; Robert P. de Vries; Geert Jan Boons; Marliek van Hoesel; Karen de Haan; Laura E. van Groeningen; Katina D. Hulme; Hugo D.G. van Willigen; Elke Wynberg; Godelieve J. de Bree; Amy Matser; Margreet Bakker; Lia van der Hoek; Maria Prins; Neeltje A. Kootstra; Dirk Eggink; Brooke E. Nichols; Alvin X. Han; Menno D. de Jong; Colin A. Russell

doi:10.1038/s41467-023-44668-z

Determinants of epidemic size and the impacts of lulls in seasonal influenza virus circulation

Simon P.J. de Jong
, Zandra C. Felix Garza
, Joseph C. Gibson
, Sarah van Leeuwen
, Robert P. de Vries
, Geert Jan Boons
, Marliek van Hoesel
, Karen de Haan
, Laura E. van Groeningen
, Katina D. Hulme
, Hugo D.G. van Willigen
, Elke Wynberg
, Godelieve J. de Bree
, Amy Matser
, Margreet Bakker
, Lia van der Hoek
, Maria Prins
, Neeltje A. Kootstra
, Dirk Eggink
, Brooke E. Nichols

Alvin X. Han, Menno D. de Jong, Colin A. Russell^*

^*Corresponding author for this work

University of Amsterdam
Municipal Health Service of Amsterdam
National Institute of Public Health and the Environment
Boston University

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

Abstract

During the COVID-19 pandemic, levels of seasonal influenza virus circulation were unprecedentedly low, leading to concerns that a lack of exposure to influenza viruses, combined with waning antibody titres, could result in larger and/or more severe post-pandemic seasonal influenza epidemics. However, in most countries the first post-pandemic influenza season was not unusually large and/or severe. Here, based on an analysis of historical influenza virus epidemic patterns from 2002 to 2019, we show that historic lulls in influenza virus circulation had relatively minor impacts on subsequent epidemic size and that epidemic size was more substantially impacted by season-specific effects unrelated to the magnitude of circulation in prior seasons. From measurements of antibody levels from serum samples collected each year from 2017 to 2021, we show that the rate of waning of antibody titres against influenza virus during the pandemic was smaller than assumed in predictive models. Taken together, these results partially explain why the re-emergence of seasonal influenza virus epidemics was less dramatic than anticipated and suggest that influenza virus epidemic dynamics are not currently amenable to multi-season prediction.

Original language	English
Article number	591
Pages (from-to)	1-11
Number of pages	11
Journal	Nature Communications
Volume	15
Issue number	1
DOIs	https://doi.org/10.1038/s41467-023-44668-z
Publication status	Published - 18 Jan 2024

Bibliographical note

Publisher Copyright:
© 2024, The Author(s).

Funding

A.X.H., Z.C.F.G. and C.A.R. were supported by ERC NaviFlu (No. 818353). J.G. and C.A.R. were supported by NIH R01 (5R01AI132362-04). C.A.R. was also supported by an NWO Vici Award (09150182010027). R.P.d.V. was supported by ERC starting grant 802780 and a Beijerinck Premium of the Royal Dutch Academy of Sciences. G.J.B. was supported by the Netherlands Organization for Scientific Research (NWO TOPPUNT 718.015.003) and by an ERC advanced grant (101020769). The RECoVERED cohort is supported by NWO ZonMw (No. 10150062010002) and the Public Health Service of Amsterdam (Research & Development grant number 21–14). The Amsterdam Cohort Studies on HIV infection and AIDS, a collaboration between the Public Health Service Amsterdam, the Amsterdam UMC of the University of Amsterdam, Medical Center Jan van Goyen and the HIV Focus Center of the DC-Clinics, are part of the Netherlands HIV Monitoring Foundation and financially supported by the Center for Infectious Disease Control of the Netherlands National Institute for Public Health and the Environment. We gratefully acknowledge the authors and originating and submitting laboratories (supplementary information) for the reference sequences retrieved from GISAID’s EpiFlu Database used in this study. The authors thank all ACS and RECoVERED study participants. We are also grateful to Mr. Reinier van der Palen of the department of Chemical Biology and Drug Discovery, Utrecht University for his practical assistance with turkey erythrocyte glycan remodelling.

Funders	Funder number
ERC NaviFlu	818353
NWO ZonMw	10150062010002
Netherlands HIV Monitoring Foundation
Public Health Service Amsterdam
Public Health Service of Amsterdam	21–14
Royal Dutch Academy of Sciences
National Institutes of Health	5R01AI132362-04
National Institutes of Health
European Research Council	802780
European Research Council
Nederlandse Organisatie voor Wetenschappelijk Onderzoek	TOPPUNT 718.015.003, 09150182010027, 101020769
Nederlandse Organisatie voor Wetenschappelijk Onderzoek
Rijksinstituut voor Volksgezondheid en Milieu

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s41467-023-44668-zFinal published version, 3.92 MBLicence: CC BY

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de Jong, S. P. J., Felix Garza, Z. C., Gibson, J. C., van Leeuwen, S., de Vries, R. P., Boons, G. J., van Hoesel, M., de Haan, K., van Groeningen, L. E., Hulme, K. D., van Willigen, H. D. G., Wynberg, E., de Bree, G. J., Matser, A., Bakker, M., van der Hoek, L., Prins, M., Kootstra, N. A., Eggink, D., ... Russell, C. A. (2024). Determinants of epidemic size and the impacts of lulls in seasonal influenza virus circulation. Nature Communications, 15(1), 1-11. Article 591. https://doi.org/10.1038/s41467-023-44668-z

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title = "Determinants of epidemic size and the impacts of lulls in seasonal influenza virus circulation",

abstract = "During the COVID-19 pandemic, levels of seasonal influenza virus circulation were unprecedentedly low, leading to concerns that a lack of exposure to influenza viruses, combined with waning antibody titres, could result in larger and/or more severe post-pandemic seasonal influenza epidemics. However, in most countries the first post-pandemic influenza season was not unusually large and/or severe. Here, based on an analysis of historical influenza virus epidemic patterns from 2002 to 2019, we show that historic lulls in influenza virus circulation had relatively minor impacts on subsequent epidemic size and that epidemic size was more substantially impacted by season-specific effects unrelated to the magnitude of circulation in prior seasons. From measurements of antibody levels from serum samples collected each year from 2017 to 2021, we show that the rate of waning of antibody titres against influenza virus during the pandemic was smaller than assumed in predictive models. Taken together, these results partially explain why the re-emergence of seasonal influenza virus epidemics was less dramatic than anticipated and suggest that influenza virus epidemic dynamics are not currently amenable to multi-season prediction.",

author = "\{de Jong\}, \{Simon P.J.\} and \{Felix Garza\}, \{Zandra C.\} and Gibson, \{Joseph C.\} and \{van Leeuwen\}, Sarah and \{de Vries\}, \{Robert P.\} and Boons, \{Geert Jan\} and \{van Hoesel\}, Marliek and \{de Haan\}, Karen and \{van Groeningen\}, \{Laura E.\} and Hulme, \{Katina D.\} and \{van Willigen\}, \{Hugo D.G.\} and Elke Wynberg and \{de Bree\}, \{Godelieve J.\} and Amy Matser and Margreet Bakker and \{van der Hoek\}, Lia and Maria Prins and Kootstra, \{Neeltje A.\} and Dirk Eggink and Nichols, \{Brooke E.\} and Han, \{Alvin X.\} and \{de Jong\}, \{Menno D.\} and Russell, \{Colin A.\}",

note = "Publisher Copyright: {\textcopyright} 2024, The Author(s).",

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month = jan,

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doi = "10.1038/s41467-023-44668-z",

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de Jong, SPJ, Felix Garza, ZC, Gibson, JC, van Leeuwen, S, de Vries, RP , Boons, GJ, van Hoesel, M, de Haan, K, van Groeningen, LE, Hulme, KD, van Willigen, HDG, Wynberg, E, de Bree, GJ, Matser, A, Bakker, M, van der Hoek, L, Prins, M, Kootstra, NA, Eggink, D, Nichols, BE, Han, AX, de Jong, MD & Russell, CA 2024, 'Determinants of epidemic size and the impacts of lulls in seasonal influenza virus circulation', Nature Communications, vol. 15, no. 1, 591, pp. 1-11. https://doi.org/10.1038/s41467-023-44668-z

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T1 - Determinants of epidemic size and the impacts of lulls in seasonal influenza virus circulation

AU - de Jong, Simon P.J.

AU - Felix Garza, Zandra C.

AU - Gibson, Joseph C.

AU - van Leeuwen, Sarah

AU - de Vries, Robert P.

AU - Boons, Geert Jan

AU - van Hoesel, Marliek

AU - de Haan, Karen

AU - van Groeningen, Laura E.

AU - Hulme, Katina D.

AU - van Willigen, Hugo D.G.

AU - Wynberg, Elke

AU - de Bree, Godelieve J.

AU - Matser, Amy

AU - Bakker, Margreet

AU - van der Hoek, Lia

AU - Prins, Maria

AU - Kootstra, Neeltje A.

AU - Eggink, Dirk

AU - Nichols, Brooke E.

AU - Han, Alvin X.

AU - de Jong, Menno D.

AU - Russell, Colin A.

PY - 2024/1/18

Y1 - 2024/1/18

N2 - During the COVID-19 pandemic, levels of seasonal influenza virus circulation were unprecedentedly low, leading to concerns that a lack of exposure to influenza viruses, combined with waning antibody titres, could result in larger and/or more severe post-pandemic seasonal influenza epidemics. However, in most countries the first post-pandemic influenza season was not unusually large and/or severe. Here, based on an analysis of historical influenza virus epidemic patterns from 2002 to 2019, we show that historic lulls in influenza virus circulation had relatively minor impacts on subsequent epidemic size and that epidemic size was more substantially impacted by season-specific effects unrelated to the magnitude of circulation in prior seasons. From measurements of antibody levels from serum samples collected each year from 2017 to 2021, we show that the rate of waning of antibody titres against influenza virus during the pandemic was smaller than assumed in predictive models. Taken together, these results partially explain why the re-emergence of seasonal influenza virus epidemics was less dramatic than anticipated and suggest that influenza virus epidemic dynamics are not currently amenable to multi-season prediction.

AB - During the COVID-19 pandemic, levels of seasonal influenza virus circulation were unprecedentedly low, leading to concerns that a lack of exposure to influenza viruses, combined with waning antibody titres, could result in larger and/or more severe post-pandemic seasonal influenza epidemics. However, in most countries the first post-pandemic influenza season was not unusually large and/or severe. Here, based on an analysis of historical influenza virus epidemic patterns from 2002 to 2019, we show that historic lulls in influenza virus circulation had relatively minor impacts on subsequent epidemic size and that epidemic size was more substantially impacted by season-specific effects unrelated to the magnitude of circulation in prior seasons. From measurements of antibody levels from serum samples collected each year from 2017 to 2021, we show that the rate of waning of antibody titres against influenza virus during the pandemic was smaller than assumed in predictive models. Taken together, these results partially explain why the re-emergence of seasonal influenza virus epidemics was less dramatic than anticipated and suggest that influenza virus epidemic dynamics are not currently amenable to multi-season prediction.

UR - https://www.scopus.com/pages/publications/85182624069

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DO - 10.1038/s41467-023-44668-z

M3 - Article

C2 - 38238318

AN - SCOPUS:85182624069

SN - 2041-1723

VL - 15

SP - 1

EP - 11

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 591

ER -

Determinants of epidemic size and the impacts of lulls in seasonal influenza virus circulation

Abstract

Bibliographical note

Funding

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