Estimating age-specific cumulative incidence for the 2009 influenza pandemic: A meta-analysis of A(H1N1)pdm09 serological studies from 19 countries

Maria D. Van Kerkhove, Siddhivinayak Hirve, Artemis Koukounari, Anthony W. Mounts, Regina Allwinn, D. Don Bandaranayake, A. Antonino Bella, Angie Bone, Fabrice Carrat, Mandeep S. Chadha, Mark Chen, Chia Yu Chi, C. M.Chad M. Cox, Michelle Cretikos, Natasha Crowcroft, Jeffery Cutter, Christl A. Donnelly, Xavier de Lamballerie, K. Koussay Dellagi, George DoukasSandra Dudareva-Vizule, Neil M. Ferguson, Alicia M. Fry, Gwendolyn L. Gilbert, Walter Haas, Pia Hardelid, Peter Horby, Q. Sue Huang, Olav Hungnes, Niina Ikonen, Kyoko Iwatsuki-Horimoto, Iikka Julkunen, Jacqueline Katz, Yoshi Kawaoka, Ajit Lalvani, Daniel Levy-Bruhl, Helena C. Maltezou, Jodie McVernon, Elizabeth Miller, A. C. Mishra, Mohsen Moghadami, Shailesh D. Pawar, Carrie Reed, Steven Riley, Caterina Rizzo, Laura Rosella, Ted M. Ross, Yuelong Shu, Danuta M. Skowronski, Saranya Sridhar, Anneke Steens, Babasaheb V. Tandale, Maria Theodoridou, Michiel van Boven, Kristian Waalen, Jen Ren Wang, Joseph T. Wu, Cuiling Xu, Shanta Zimmer

Research output: Contribution to journalReview article

109 Citations (Scopus)

Abstract

Background: The global impact of the 2009 influenza A(H1N1) pandemic (H1N1pdm) is not well understood. Objectives: We estimate overall and age-specific prevalence of cross-reactive antibodies to H1N1pdm virus and rates of H1N1pdm infection during the first year of the pandemic using data from published and unpublished H1N1pdm seroepidemiological studies. Methods: Primary aggregate H1N1pdm serologic data from each study were stratified in standardized age groups and evaluated based on when sera were collected in relation to national or subnational peak H1N1pdm activity. Seropositivity was assessed using well-described and standardized hemagglutination inhibition (HI titers ≥32 or ≥40) and microneutralization (MN ≥ 40) laboratory assays. The prevalence of cross-reactive antibodies to the H1N1pdm virus was estimated for studies using sera collected prior to the start of the pandemic (between 2004 and April 2009); H1N1pdm cumulative incidence was estimated for studies in which collected both pre- and post-pandemic sera; and H1N1pdm seropositivity was calculated from studies with post-pandemic sera only (collected between December 2009-June 2010). Results: Data from 27 published/unpublished studies from 19 countries/administrative regions - Australia, Canada, China, Finland, France, Germany, Hong Kong SAR, India, Iran, Italy, Japan, Netherlands, New Zealand, Norway, Reunion Island, Singapore, United Kingdom, United States, and Vietnam - were eligible for inclusion. The overall age-standardized pre-pandemic prevalence of cross-reactive antibodies was 5% (95%CI 3-7%) and varied significantly by age with the highest rates among persons ≥65 years old (14% 95%CI 8-24%). Overall age-standardized H1N1pdm cumulative incidence was 24% (95%CI 20-27%) and varied significantly by age with the highest in children 5-19 (47% 95%CI 39-55%) and 0-4 years old (36% 95%CI 30-43%). Conclusions: Our results offer unique insight into the global impact of the H1N1 pandemic and highlight the need for standardization of seroepidemiological studies and for their inclusion in pre-pandemic preparedness plans. Our results taken together with recent global pandemic respiratory-associated mortality estimates suggest that the case fatality ratio of the pandemic virus was approximately 0·02%.

Original languageEnglish
Pages (from-to)872-886
Number of pages15
JournalInfluenza and other Respiratory Viruses
Volume7
Issue number5
DOIs
Publication statusPublished - 2013 Sep

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Pandemics
Human Influenza
Meta-Analysis
Incidence
H1N1 Subtype Influenza A Virus
Seroepidemiologic Studies
Serum
Antibodies
Reunion
Vietnam
Singapore
Hemagglutination
Hong Kong

All Science Journal Classification (ASJC) codes

  • Epidemiology
  • Pulmonary and Respiratory Medicine
  • Public Health, Environmental and Occupational Health
  • Infectious Diseases

Cite this

Van Kerkhove, Maria D. ; Hirve, Siddhivinayak ; Koukounari, Artemis ; Mounts, Anthony W. ; Allwinn, Regina ; Bandaranayake, D. Don ; Bella, A. Antonino ; Bone, Angie ; Carrat, Fabrice ; Chadha, Mandeep S. ; Chen, Mark ; Chi, Chia Yu ; Cox, C. M.Chad M. ; Cretikos, Michelle ; Crowcroft, Natasha ; Cutter, Jeffery ; Donnelly, Christl A. ; de Lamballerie, Xavier ; Dellagi, K. Koussay ; Doukas, George ; Dudareva-Vizule, Sandra ; Ferguson, Neil M. ; Fry, Alicia M. ; Gilbert, Gwendolyn L. ; Haas, Walter ; Hardelid, Pia ; Horby, Peter ; Huang, Q. Sue ; Hungnes, Olav ; Ikonen, Niina ; Iwatsuki-Horimoto, Kyoko ; Julkunen, Iikka ; Katz, Jacqueline ; Kawaoka, Yoshi ; Lalvani, Ajit ; Levy-Bruhl, Daniel ; Maltezou, Helena C. ; McVernon, Jodie ; Miller, Elizabeth ; Mishra, A. C. ; Moghadami, Mohsen ; Pawar, Shailesh D. ; Reed, Carrie ; Riley, Steven ; Rizzo, Caterina ; Rosella, Laura ; Ross, Ted M. ; Shu, Yuelong ; Skowronski, Danuta M. ; Sridhar, Saranya ; Steens, Anneke ; Tandale, Babasaheb V. ; Theodoridou, Maria ; van Boven, Michiel ; Waalen, Kristian ; Wang, Jen Ren ; Wu, Joseph T. ; Xu, Cuiling ; Zimmer, Shanta. / Estimating age-specific cumulative incidence for the 2009 influenza pandemic : A meta-analysis of A(H1N1)pdm09 serological studies from 19 countries. In: Influenza and other Respiratory Viruses. 2013 ; Vol. 7, No. 5. pp. 872-886.
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title = "Estimating age-specific cumulative incidence for the 2009 influenza pandemic: A meta-analysis of A(H1N1)pdm09 serological studies from 19 countries",
abstract = "Background: The global impact of the 2009 influenza A(H1N1) pandemic (H1N1pdm) is not well understood. Objectives: We estimate overall and age-specific prevalence of cross-reactive antibodies to H1N1pdm virus and rates of H1N1pdm infection during the first year of the pandemic using data from published and unpublished H1N1pdm seroepidemiological studies. Methods: Primary aggregate H1N1pdm serologic data from each study were stratified in standardized age groups and evaluated based on when sera were collected in relation to national or subnational peak H1N1pdm activity. Seropositivity was assessed using well-described and standardized hemagglutination inhibition (HI titers ≥32 or ≥40) and microneutralization (MN ≥ 40) laboratory assays. The prevalence of cross-reactive antibodies to the H1N1pdm virus was estimated for studies using sera collected prior to the start of the pandemic (between 2004 and April 2009); H1N1pdm cumulative incidence was estimated for studies in which collected both pre- and post-pandemic sera; and H1N1pdm seropositivity was calculated from studies with post-pandemic sera only (collected between December 2009-June 2010). Results: Data from 27 published/unpublished studies from 19 countries/administrative regions - Australia, Canada, China, Finland, France, Germany, Hong Kong SAR, India, Iran, Italy, Japan, Netherlands, New Zealand, Norway, Reunion Island, Singapore, United Kingdom, United States, and Vietnam - were eligible for inclusion. The overall age-standardized pre-pandemic prevalence of cross-reactive antibodies was 5{\%} (95{\%}CI 3-7{\%}) and varied significantly by age with the highest rates among persons ≥65 years old (14{\%} 95{\%}CI 8-24{\%}). Overall age-standardized H1N1pdm cumulative incidence was 24{\%} (95{\%}CI 20-27{\%}) and varied significantly by age with the highest in children 5-19 (47{\%} 95{\%}CI 39-55{\%}) and 0-4 years old (36{\%} 95{\%}CI 30-43{\%}). Conclusions: Our results offer unique insight into the global impact of the H1N1 pandemic and highlight the need for standardization of seroepidemiological studies and for their inclusion in pre-pandemic preparedness plans. Our results taken together with recent global pandemic respiratory-associated mortality estimates suggest that the case fatality ratio of the pandemic virus was approximately 0·02{\%}.",
author = "{Van Kerkhove}, {Maria D.} and Siddhivinayak Hirve and Artemis Koukounari and Mounts, {Anthony W.} and Regina Allwinn and Bandaranayake, {D. Don} and Bella, {A. Antonino} and Angie Bone and Fabrice Carrat and Chadha, {Mandeep S.} and Mark Chen and Chi, {Chia Yu} and Cox, {C. M.Chad M.} and Michelle Cretikos and Natasha Crowcroft and Jeffery Cutter and Donnelly, {Christl A.} and {de Lamballerie}, Xavier and Dellagi, {K. Koussay} and George Doukas and Sandra Dudareva-Vizule and Ferguson, {Neil M.} and Fry, {Alicia M.} and Gilbert, {Gwendolyn L.} and Walter Haas and Pia Hardelid and Peter Horby and Huang, {Q. Sue} and Olav Hungnes and Niina Ikonen and Kyoko Iwatsuki-Horimoto and Iikka Julkunen and Jacqueline Katz and Yoshi Kawaoka and Ajit Lalvani and Daniel Levy-Bruhl and Maltezou, {Helena C.} and Jodie McVernon and Elizabeth Miller and Mishra, {A. C.} and Mohsen Moghadami and Pawar, {Shailesh D.} and Carrie Reed and Steven Riley and Caterina Rizzo and Laura Rosella and Ross, {Ted M.} and Yuelong Shu and Skowronski, {Danuta M.} and Saranya Sridhar and Anneke Steens and Tandale, {Babasaheb V.} and Maria Theodoridou and {van Boven}, Michiel and Kristian Waalen and Wang, {Jen Ren} and Wu, {Joseph T.} and Cuiling Xu and Shanta Zimmer",
year = "2013",
month = "9",
doi = "10.1111/irv.12074",
language = "English",
volume = "7",
pages = "872--886",
journal = "Influenza and other Respiratory Viruses",
issn = "1750-2640",
publisher = "Wiley-Blackwell",
number = "5",

}

Van Kerkhove, MD, Hirve, S, Koukounari, A, Mounts, AW, Allwinn, R, Bandaranayake, DD, Bella, AA, Bone, A, Carrat, F, Chadha, MS, Chen, M, Chi, CY, Cox, CMCM, Cretikos, M, Crowcroft, N, Cutter, J, Donnelly, CA, de Lamballerie, X, Dellagi, KK, Doukas, G, Dudareva-Vizule, S, Ferguson, NM, Fry, AM, Gilbert, GL, Haas, W, Hardelid, P, Horby, P, Huang, QS, Hungnes, O, Ikonen, N, Iwatsuki-Horimoto, K, Julkunen, I, Katz, J, Kawaoka, Y, Lalvani, A, Levy-Bruhl, D, Maltezou, HC, McVernon, J, Miller, E, Mishra, AC, Moghadami, M, Pawar, SD, Reed, C, Riley, S, Rizzo, C, Rosella, L, Ross, TM, Shu, Y, Skowronski, DM, Sridhar, S, Steens, A, Tandale, BV, Theodoridou, M, van Boven, M, Waalen, K, Wang, JR, Wu, JT, Xu, C & Zimmer, S 2013, 'Estimating age-specific cumulative incidence for the 2009 influenza pandemic: A meta-analysis of A(H1N1)pdm09 serological studies from 19 countries', Influenza and other Respiratory Viruses, vol. 7, no. 5, pp. 872-886. https://doi.org/10.1111/irv.12074

Estimating age-specific cumulative incidence for the 2009 influenza pandemic : A meta-analysis of A(H1N1)pdm09 serological studies from 19 countries. / Van Kerkhove, Maria D.; Hirve, Siddhivinayak; Koukounari, Artemis; Mounts, Anthony W.; Allwinn, Regina; Bandaranayake, D. Don; Bella, A. Antonino; Bone, Angie; Carrat, Fabrice; Chadha, Mandeep S.; Chen, Mark; Chi, Chia Yu; Cox, C. M.Chad M.; Cretikos, Michelle; Crowcroft, Natasha; Cutter, Jeffery; Donnelly, Christl A.; de Lamballerie, Xavier; Dellagi, K. Koussay; Doukas, George; Dudareva-Vizule, Sandra; Ferguson, Neil M.; Fry, Alicia M.; Gilbert, Gwendolyn L.; Haas, Walter; Hardelid, Pia; Horby, Peter; Huang, Q. Sue; Hungnes, Olav; Ikonen, Niina; Iwatsuki-Horimoto, Kyoko; Julkunen, Iikka; Katz, Jacqueline; Kawaoka, Yoshi; Lalvani, Ajit; Levy-Bruhl, Daniel; Maltezou, Helena C.; McVernon, Jodie; Miller, Elizabeth; Mishra, A. C.; Moghadami, Mohsen; Pawar, Shailesh D.; Reed, Carrie; Riley, Steven; Rizzo, Caterina; Rosella, Laura; Ross, Ted M.; Shu, Yuelong; Skowronski, Danuta M.; Sridhar, Saranya; Steens, Anneke; Tandale, Babasaheb V.; Theodoridou, Maria; van Boven, Michiel; Waalen, Kristian; Wang, Jen Ren; Wu, Joseph T.; Xu, Cuiling; Zimmer, Shanta.

In: Influenza and other Respiratory Viruses, Vol. 7, No. 5, 09.2013, p. 872-886.

Research output: Contribution to journalReview article

TY - JOUR

T1 - Estimating age-specific cumulative incidence for the 2009 influenza pandemic

T2 - A meta-analysis of A(H1N1)pdm09 serological studies from 19 countries

AU - Van Kerkhove, Maria D.

AU - Hirve, Siddhivinayak

AU - Koukounari, Artemis

AU - Mounts, Anthony W.

AU - Allwinn, Regina

AU - Bandaranayake, D. Don

AU - Bella, A. Antonino

AU - Bone, Angie

AU - Carrat, Fabrice

AU - Chadha, Mandeep S.

AU - Chen, Mark

AU - Chi, Chia Yu

AU - Cox, C. M.Chad M.

AU - Cretikos, Michelle

AU - Crowcroft, Natasha

AU - Cutter, Jeffery

AU - Donnelly, Christl A.

AU - de Lamballerie, Xavier

AU - Dellagi, K. Koussay

AU - Doukas, George

AU - Dudareva-Vizule, Sandra

AU - Ferguson, Neil M.

AU - Fry, Alicia M.

AU - Gilbert, Gwendolyn L.

AU - Haas, Walter

AU - Hardelid, Pia

AU - Horby, Peter

AU - Huang, Q. Sue

AU - Hungnes, Olav

AU - Ikonen, Niina

AU - Iwatsuki-Horimoto, Kyoko

AU - Julkunen, Iikka

AU - Katz, Jacqueline

AU - Kawaoka, Yoshi

AU - Lalvani, Ajit

AU - Levy-Bruhl, Daniel

AU - Maltezou, Helena C.

AU - McVernon, Jodie

AU - Miller, Elizabeth

AU - Mishra, A. C.

AU - Moghadami, Mohsen

AU - Pawar, Shailesh D.

AU - Reed, Carrie

AU - Riley, Steven

AU - Rizzo, Caterina

AU - Rosella, Laura

AU - Ross, Ted M.

AU - Shu, Yuelong

AU - Skowronski, Danuta M.

AU - Sridhar, Saranya

AU - Steens, Anneke

AU - Tandale, Babasaheb V.

AU - Theodoridou, Maria

AU - van Boven, Michiel

AU - Waalen, Kristian

AU - Wang, Jen Ren

AU - Wu, Joseph T.

AU - Xu, Cuiling

AU - Zimmer, Shanta

PY - 2013/9

Y1 - 2013/9

N2 - Background: The global impact of the 2009 influenza A(H1N1) pandemic (H1N1pdm) is not well understood. Objectives: We estimate overall and age-specific prevalence of cross-reactive antibodies to H1N1pdm virus and rates of H1N1pdm infection during the first year of the pandemic using data from published and unpublished H1N1pdm seroepidemiological studies. Methods: Primary aggregate H1N1pdm serologic data from each study were stratified in standardized age groups and evaluated based on when sera were collected in relation to national or subnational peak H1N1pdm activity. Seropositivity was assessed using well-described and standardized hemagglutination inhibition (HI titers ≥32 or ≥40) and microneutralization (MN ≥ 40) laboratory assays. The prevalence of cross-reactive antibodies to the H1N1pdm virus was estimated for studies using sera collected prior to the start of the pandemic (between 2004 and April 2009); H1N1pdm cumulative incidence was estimated for studies in which collected both pre- and post-pandemic sera; and H1N1pdm seropositivity was calculated from studies with post-pandemic sera only (collected between December 2009-June 2010). Results: Data from 27 published/unpublished studies from 19 countries/administrative regions - Australia, Canada, China, Finland, France, Germany, Hong Kong SAR, India, Iran, Italy, Japan, Netherlands, New Zealand, Norway, Reunion Island, Singapore, United Kingdom, United States, and Vietnam - were eligible for inclusion. The overall age-standardized pre-pandemic prevalence of cross-reactive antibodies was 5% (95%CI 3-7%) and varied significantly by age with the highest rates among persons ≥65 years old (14% 95%CI 8-24%). Overall age-standardized H1N1pdm cumulative incidence was 24% (95%CI 20-27%) and varied significantly by age with the highest in children 5-19 (47% 95%CI 39-55%) and 0-4 years old (36% 95%CI 30-43%). Conclusions: Our results offer unique insight into the global impact of the H1N1 pandemic and highlight the need for standardization of seroepidemiological studies and for their inclusion in pre-pandemic preparedness plans. Our results taken together with recent global pandemic respiratory-associated mortality estimates suggest that the case fatality ratio of the pandemic virus was approximately 0·02%.

AB - Background: The global impact of the 2009 influenza A(H1N1) pandemic (H1N1pdm) is not well understood. Objectives: We estimate overall and age-specific prevalence of cross-reactive antibodies to H1N1pdm virus and rates of H1N1pdm infection during the first year of the pandemic using data from published and unpublished H1N1pdm seroepidemiological studies. Methods: Primary aggregate H1N1pdm serologic data from each study were stratified in standardized age groups and evaluated based on when sera were collected in relation to national or subnational peak H1N1pdm activity. Seropositivity was assessed using well-described and standardized hemagglutination inhibition (HI titers ≥32 or ≥40) and microneutralization (MN ≥ 40) laboratory assays. The prevalence of cross-reactive antibodies to the H1N1pdm virus was estimated for studies using sera collected prior to the start of the pandemic (between 2004 and April 2009); H1N1pdm cumulative incidence was estimated for studies in which collected both pre- and post-pandemic sera; and H1N1pdm seropositivity was calculated from studies with post-pandemic sera only (collected between December 2009-June 2010). Results: Data from 27 published/unpublished studies from 19 countries/administrative regions - Australia, Canada, China, Finland, France, Germany, Hong Kong SAR, India, Iran, Italy, Japan, Netherlands, New Zealand, Norway, Reunion Island, Singapore, United Kingdom, United States, and Vietnam - were eligible for inclusion. The overall age-standardized pre-pandemic prevalence of cross-reactive antibodies was 5% (95%CI 3-7%) and varied significantly by age with the highest rates among persons ≥65 years old (14% 95%CI 8-24%). Overall age-standardized H1N1pdm cumulative incidence was 24% (95%CI 20-27%) and varied significantly by age with the highest in children 5-19 (47% 95%CI 39-55%) and 0-4 years old (36% 95%CI 30-43%). Conclusions: Our results offer unique insight into the global impact of the H1N1 pandemic and highlight the need for standardization of seroepidemiological studies and for their inclusion in pre-pandemic preparedness plans. Our results taken together with recent global pandemic respiratory-associated mortality estimates suggest that the case fatality ratio of the pandemic virus was approximately 0·02%.

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U2 - 10.1111/irv.12074

DO - 10.1111/irv.12074

M3 - Review article

C2 - 23331969

AN - SCOPUS:84876180604

VL - 7

SP - 872

EP - 886

JO - Influenza and other Respiratory Viruses

JF - Influenza and other Respiratory Viruses

SN - 1750-2640

IS - 5

ER -