Global Mortality Estimates for the 2009 Influenza Pandemic from the GLaMOR Project: A Modeling Study

Lone Simonsen, Peter Spreeuwenberg, Roger Lustig, Robert J. Taylor, Douglas M. Fleming, Madelon Kroneman, Maria D. Van Kerkhove, Anthony W. Mounts, W. John Paget, Horacio Echenique, Vilma Savy, David Muscatello, C. Raina MacIntyre, Dominic E. Dwyer, Eduardo Azziz-Baumgartner, Nusrat Homaira, Fernanda Edna Araújo Moura, Cynthia Schuck, Holy Akwar, Dena SchanzerRodrigo Fuentes, Andrea Olea, Viviana Sotomayor, Luzhao Feng, Hongjie Yu, Anne Mazick, Kåre Mølbak, Jens Nielsen, Fabrice Carrat, Magali Lemaitre, Udo Buchholz, Brunhilde Schweiger, Michael Höhle, Silvan Vesenbeckh, Ben Cowling, Gabriel Leung, Thomas Tsang, Shuk Kwan Chuang, Michal Bromberg, Zalman Kaufman, Norio Sugaya, Kuniko Oka Ezoe, Shuichiro Hayashi, Megumi Matsuda, Hugo Lopez-Gatell, Celia Alpuche-Aranda, Daniel Noyola, Gerardo Chowell, Liselotte van Asten, Adam Meijer, Kees van den Wijngaard, Marianne van der Sande, Michael Baker, Jane Zhang, Jorge Gómez Benavides, César Munayco, Alberto Laguna-Torres, Daniel Rabczenko, Bogdan Wojtyniak, Sun Hee Park, Yeon Kyeng Lee, Laurentiu Zolotusca, Odette Popovici, Rodica Popescu, Li Wei Ang, Jeffery Cutter, Raymond Lin, Stefan Ma, Mark Chen, Vernon J. Lee, Katarina Prosenc, Maja Socan, Cheryl Cohen, Amparo Larrauri, Salvador de Mateo, Lorena Simón Méndez, Concha Delgado Sanz, Nick Andrews, Helen K. Green, Richard Pebody, Ayoub Saei, David Shay, Cecile Viboud

Research output: Contribution to journalArticle

176 Citations (Scopus)

Abstract

Background:Assessing the mortality impact of the 2009 influenza A H1N1 virus (H1N1pdm09) is essential for optimizing public health responses to future pandemics. The World Health Organization reported 18,631 laboratory-confirmed pandemic deaths, but the total pandemic mortality burden was substantially higher. We estimated the 2009 pandemic mortality burden through statistical modeling of mortality data from multiple countries.Methods and Findings:We obtained weekly virology and underlying cause-of-death mortality time series for 2005-2009 for 20 countries covering ∼35% of the world population. We applied a multivariate linear regression model to estimate pandemic respiratory mortality in each collaborating country. We then used these results plus ten country indicators in a multiple imputation model to project the mortality burden in all world countries. Between 123,000 and 203,000 pandemic respiratory deaths were estimated globally for the last 9 mo of 2009. The majority (62%-85%) were attributed to persons under 65 y of age. We observed a striking regional heterogeneity, with almost 20-fold higher mortality in some countries in the Americas than in Europe. The model attributed 148,000-249,000 respiratory deaths to influenza in an average pre-pandemic season, with only 19% in persons <65 y. Limitations include lack of representation of low-income countries among single-country estimates and an inability to study subsequent pandemic waves (2010-2012).Conclusions:We estimate that 2009 global pandemic respiratory mortality was ∼10-fold higher than the World Health Organization's laboratory-confirmed mortality count. Although the pandemic mortality estimate was similar in magnitude to that of seasonal influenza, a marked shift toward mortality among persons <65 y of age occurred, so that many more life-years were lost. The burden varied greatly among countries, corroborating early reports of far greater pandemic severity in the Americas than in Australia, New Zealand, and Europe. A collaborative network to collect and analyze mortality and hospitalization surveillance data is needed to rapidly establish the severity of future pandemics.Please see later in the article for the Editors' Summary.

Original languageEnglish (US)
Article numbere1001558
JournalPLoS Medicine
Volume10
Issue number11
DOIs
StatePublished - Nov 2013

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Pandemics
Human Influenza
Mortality
Linear Models
H1N1 Subtype Influenza A Virus
Virology
Influenza A virus
New Zealand
Cause of Death
Hospitalization
Public Health

ASJC Scopus subject areas

  • Medicine(all)

Cite this

Simonsen, L., Spreeuwenberg, P., Lustig, R., Taylor, R. J., Fleming, D. M., Kroneman, M., ... Viboud, C. (2013). Global Mortality Estimates for the 2009 Influenza Pandemic from the GLaMOR Project: A Modeling Study. PLoS Medicine, 10(11), [e1001558]. https://doi.org/10.1371/journal.pmed.1001558

Global Mortality Estimates for the 2009 Influenza Pandemic from the GLaMOR Project : A Modeling Study. / Simonsen, Lone; Spreeuwenberg, Peter; Lustig, Roger; Taylor, Robert J.; Fleming, Douglas M.; Kroneman, Madelon; Van Kerkhove, Maria D.; Mounts, Anthony W.; Paget, W. John; Echenique, Horacio; Savy, Vilma; Muscatello, David; MacIntyre, C. Raina; Dwyer, Dominic E.; Azziz-Baumgartner, Eduardo; Homaira, Nusrat; Moura, Fernanda Edna Araújo; Schuck, Cynthia; Akwar, Holy; Schanzer, Dena; Fuentes, Rodrigo; Olea, Andrea; Sotomayor, Viviana; Feng, Luzhao; Yu, Hongjie; Mazick, Anne; Mølbak, Kåre; Nielsen, Jens; Carrat, Fabrice; Lemaitre, Magali; Buchholz, Udo; Schweiger, Brunhilde; Höhle, Michael; Vesenbeckh, Silvan; Cowling, Ben; Leung, Gabriel; Tsang, Thomas; Chuang, Shuk Kwan; Bromberg, Michal; Kaufman, Zalman; Sugaya, Norio; Oka Ezoe, Kuniko; Hayashi, Shuichiro; Matsuda, Megumi; Lopez-Gatell, Hugo; Alpuche-Aranda, Celia; Noyola, Daniel; Chowell, Gerardo; van Asten, Liselotte; Meijer, Adam; van den Wijngaard, Kees; van der Sande, Marianne; Baker, Michael; Zhang, Jane; Benavides, Jorge Gómez; Munayco, César; Laguna-Torres, Alberto; Rabczenko, Daniel; Wojtyniak, Bogdan; Park, Sun Hee; Lee, Yeon Kyeng; Zolotusca, Laurentiu; Popovici, Odette; Popescu, Rodica; Ang, Li Wei; Cutter, Jeffery; Lin, Raymond; Ma, Stefan; Chen, Mark; Lee, Vernon J.; Prosenc, Katarina; Socan, Maja; Cohen, Cheryl; Larrauri, Amparo; de Mateo, Salvador; Méndez, Lorena Simón; Sanz, Concha Delgado; Andrews, Nick; Green, Helen K.; Pebody, Richard; Saei, Ayoub; Shay, David; Viboud, Cecile.

In: PLoS Medicine, Vol. 10, No. 11, e1001558, 11.2013.

Research output: Contribution to journalArticle

Simonsen, L, Spreeuwenberg, P, Lustig, R, Taylor, RJ, Fleming, DM, Kroneman, M, Van Kerkhove, MD, Mounts, AW, Paget, WJ, Echenique, H, Savy, V, Muscatello, D, MacIntyre, CR, Dwyer, DE, Azziz-Baumgartner, E, Homaira, N, Moura, FEA, Schuck, C, Akwar, H, Schanzer, D, Fuentes, R, Olea, A, Sotomayor, V, Feng, L, Yu, H, Mazick, A, Mølbak, K, Nielsen, J, Carrat, F, Lemaitre, M, Buchholz, U, Schweiger, B, Höhle, M, Vesenbeckh, S, Cowling, B, Leung, G, Tsang, T, Chuang, SK, Bromberg, M, Kaufman, Z, Sugaya, N, Oka Ezoe, K, Hayashi, S, Matsuda, M, Lopez-Gatell, H, Alpuche-Aranda, C, Noyola, D, Chowell, G, van Asten, L, Meijer, A, van den Wijngaard, K, van der Sande, M, Baker, M, Zhang, J, Benavides, JG, Munayco, C, Laguna-Torres, A, Rabczenko, D, Wojtyniak, B, Park, SH, Lee, YK, Zolotusca, L, Popovici, O, Popescu, R, Ang, LW, Cutter, J, Lin, R, Ma, S, Chen, M, Lee, VJ, Prosenc, K, Socan, M, Cohen, C, Larrauri, A, de Mateo, S, Méndez, LS, Sanz, CD, Andrews, N, Green, HK, Pebody, R, Saei, A, Shay, D & Viboud, C 2013, 'Global Mortality Estimates for the 2009 Influenza Pandemic from the GLaMOR Project: A Modeling Study', PLoS Medicine, vol. 10, no. 11, e1001558. https://doi.org/10.1371/journal.pmed.1001558
Simonsen L, Spreeuwenberg P, Lustig R, Taylor RJ, Fleming DM, Kroneman M et al. Global Mortality Estimates for the 2009 Influenza Pandemic from the GLaMOR Project: A Modeling Study. PLoS Medicine. 2013 Nov;10(11). e1001558. https://doi.org/10.1371/journal.pmed.1001558
Simonsen, Lone ; Spreeuwenberg, Peter ; Lustig, Roger ; Taylor, Robert J. ; Fleming, Douglas M. ; Kroneman, Madelon ; Van Kerkhove, Maria D. ; Mounts, Anthony W. ; Paget, W. John ; Echenique, Horacio ; Savy, Vilma ; Muscatello, David ; MacIntyre, C. Raina ; Dwyer, Dominic E. ; Azziz-Baumgartner, Eduardo ; Homaira, Nusrat ; Moura, Fernanda Edna Araújo ; Schuck, Cynthia ; Akwar, Holy ; Schanzer, Dena ; Fuentes, Rodrigo ; Olea, Andrea ; Sotomayor, Viviana ; Feng, Luzhao ; Yu, Hongjie ; Mazick, Anne ; Mølbak, Kåre ; Nielsen, Jens ; Carrat, Fabrice ; Lemaitre, Magali ; Buchholz, Udo ; Schweiger, Brunhilde ; Höhle, Michael ; Vesenbeckh, Silvan ; Cowling, Ben ; Leung, Gabriel ; Tsang, Thomas ; Chuang, Shuk Kwan ; Bromberg, Michal ; Kaufman, Zalman ; Sugaya, Norio ; Oka Ezoe, Kuniko ; Hayashi, Shuichiro ; Matsuda, Megumi ; Lopez-Gatell, Hugo ; Alpuche-Aranda, Celia ; Noyola, Daniel ; Chowell, Gerardo ; van Asten, Liselotte ; Meijer, Adam ; van den Wijngaard, Kees ; van der Sande, Marianne ; Baker, Michael ; Zhang, Jane ; Benavides, Jorge Gómez ; Munayco, César ; Laguna-Torres, Alberto ; Rabczenko, Daniel ; Wojtyniak, Bogdan ; Park, Sun Hee ; Lee, Yeon Kyeng ; Zolotusca, Laurentiu ; Popovici, Odette ; Popescu, Rodica ; Ang, Li Wei ; Cutter, Jeffery ; Lin, Raymond ; Ma, Stefan ; Chen, Mark ; Lee, Vernon J. ; Prosenc, Katarina ; Socan, Maja ; Cohen, Cheryl ; Larrauri, Amparo ; de Mateo, Salvador ; Méndez, Lorena Simón ; Sanz, Concha Delgado ; Andrews, Nick ; Green, Helen K. ; Pebody, Richard ; Saei, Ayoub ; Shay, David ; Viboud, Cecile. / Global Mortality Estimates for the 2009 Influenza Pandemic from the GLaMOR Project : A Modeling Study. In: PLoS Medicine. 2013 ; Vol. 10, No. 11.
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abstract = "Background:Assessing the mortality impact of the 2009 influenza A H1N1 virus (H1N1pdm09) is essential for optimizing public health responses to future pandemics. The World Health Organization reported 18,631 laboratory-confirmed pandemic deaths, but the total pandemic mortality burden was substantially higher. We estimated the 2009 pandemic mortality burden through statistical modeling of mortality data from multiple countries.Methods and Findings:We obtained weekly virology and underlying cause-of-death mortality time series for 2005-2009 for 20 countries covering ∼35{\%} of the world population. We applied a multivariate linear regression model to estimate pandemic respiratory mortality in each collaborating country. We then used these results plus ten country indicators in a multiple imputation model to project the mortality burden in all world countries. Between 123,000 and 203,000 pandemic respiratory deaths were estimated globally for the last 9 mo of 2009. The majority (62{\%}-85{\%}) were attributed to persons under 65 y of age. We observed a striking regional heterogeneity, with almost 20-fold higher mortality in some countries in the Americas than in Europe. The model attributed 148,000-249,000 respiratory deaths to influenza in an average pre-pandemic season, with only 19{\%} in persons <65 y. Limitations include lack of representation of low-income countries among single-country estimates and an inability to study subsequent pandemic waves (2010-2012).Conclusions:We estimate that 2009 global pandemic respiratory mortality was ∼10-fold higher than the World Health Organization's laboratory-confirmed mortality count. Although the pandemic mortality estimate was similar in magnitude to that of seasonal influenza, a marked shift toward mortality among persons <65 y of age occurred, so that many more life-years were lost. The burden varied greatly among countries, corroborating early reports of far greater pandemic severity in the Americas than in Australia, New Zealand, and Europe. A collaborative network to collect and analyze mortality and hospitalization surveillance data is needed to rapidly establish the severity of future pandemics.Please see later in the article for the Editors' Summary.",
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TY - JOUR

T1 - Global Mortality Estimates for the 2009 Influenza Pandemic from the GLaMOR Project

T2 - A Modeling Study

AU - Simonsen, Lone

AU - Spreeuwenberg, Peter

AU - Lustig, Roger

AU - Taylor, Robert J.

AU - Fleming, Douglas M.

AU - Kroneman, Madelon

AU - Van Kerkhove, Maria D.

AU - Mounts, Anthony W.

AU - Paget, W. John

AU - Echenique, Horacio

AU - Savy, Vilma

AU - Muscatello, David

AU - MacIntyre, C. Raina

AU - Dwyer, Dominic E.

AU - Azziz-Baumgartner, Eduardo

AU - Homaira, Nusrat

AU - Moura, Fernanda Edna Araújo

AU - Schuck, Cynthia

AU - Akwar, Holy

AU - Schanzer, Dena

AU - Fuentes, Rodrigo

AU - Olea, Andrea

AU - Sotomayor, Viviana

AU - Feng, Luzhao

AU - Yu, Hongjie

AU - Mazick, Anne

AU - Mølbak, Kåre

AU - Nielsen, Jens

AU - Carrat, Fabrice

AU - Lemaitre, Magali

AU - Buchholz, Udo

AU - Schweiger, Brunhilde

AU - Höhle, Michael

AU - Vesenbeckh, Silvan

AU - Cowling, Ben

AU - Leung, Gabriel

AU - Tsang, Thomas

AU - Chuang, Shuk Kwan

AU - Bromberg, Michal

AU - Kaufman, Zalman

AU - Sugaya, Norio

AU - Oka Ezoe, Kuniko

AU - Hayashi, Shuichiro

AU - Matsuda, Megumi

AU - Lopez-Gatell, Hugo

AU - Alpuche-Aranda, Celia

AU - Noyola, Daniel

AU - Chowell, Gerardo

AU - van Asten, Liselotte

AU - Meijer, Adam

AU - van den Wijngaard, Kees

AU - van der Sande, Marianne

AU - Baker, Michael

AU - Zhang, Jane

AU - Benavides, Jorge Gómez

AU - Munayco, César

AU - Laguna-Torres, Alberto

AU - Rabczenko, Daniel

AU - Wojtyniak, Bogdan

AU - Park, Sun Hee

AU - Lee, Yeon Kyeng

AU - Zolotusca, Laurentiu

AU - Popovici, Odette

AU - Popescu, Rodica

AU - Ang, Li Wei

AU - Cutter, Jeffery

AU - Lin, Raymond

AU - Ma, Stefan

AU - Chen, Mark

AU - Lee, Vernon J.

AU - Prosenc, Katarina

AU - Socan, Maja

AU - Cohen, Cheryl

AU - Larrauri, Amparo

AU - de Mateo, Salvador

AU - Méndez, Lorena Simón

AU - Sanz, Concha Delgado

AU - Andrews, Nick

AU - Green, Helen K.

AU - Pebody, Richard

AU - Saei, Ayoub

AU - Shay, David

AU - Viboud, Cecile

PY - 2013/11

Y1 - 2013/11

N2 - Background:Assessing the mortality impact of the 2009 influenza A H1N1 virus (H1N1pdm09) is essential for optimizing public health responses to future pandemics. The World Health Organization reported 18,631 laboratory-confirmed pandemic deaths, but the total pandemic mortality burden was substantially higher. We estimated the 2009 pandemic mortality burden through statistical modeling of mortality data from multiple countries.Methods and Findings:We obtained weekly virology and underlying cause-of-death mortality time series for 2005-2009 for 20 countries covering ∼35% of the world population. We applied a multivariate linear regression model to estimate pandemic respiratory mortality in each collaborating country. We then used these results plus ten country indicators in a multiple imputation model to project the mortality burden in all world countries. Between 123,000 and 203,000 pandemic respiratory deaths were estimated globally for the last 9 mo of 2009. The majority (62%-85%) were attributed to persons under 65 y of age. We observed a striking regional heterogeneity, with almost 20-fold higher mortality in some countries in the Americas than in Europe. The model attributed 148,000-249,000 respiratory deaths to influenza in an average pre-pandemic season, with only 19% in persons <65 y. Limitations include lack of representation of low-income countries among single-country estimates and an inability to study subsequent pandemic waves (2010-2012).Conclusions:We estimate that 2009 global pandemic respiratory mortality was ∼10-fold higher than the World Health Organization's laboratory-confirmed mortality count. Although the pandemic mortality estimate was similar in magnitude to that of seasonal influenza, a marked shift toward mortality among persons <65 y of age occurred, so that many more life-years were lost. The burden varied greatly among countries, corroborating early reports of far greater pandemic severity in the Americas than in Australia, New Zealand, and Europe. A collaborative network to collect and analyze mortality and hospitalization surveillance data is needed to rapidly establish the severity of future pandemics.Please see later in the article for the Editors' Summary.

AB - Background:Assessing the mortality impact of the 2009 influenza A H1N1 virus (H1N1pdm09) is essential for optimizing public health responses to future pandemics. The World Health Organization reported 18,631 laboratory-confirmed pandemic deaths, but the total pandemic mortality burden was substantially higher. We estimated the 2009 pandemic mortality burden through statistical modeling of mortality data from multiple countries.Methods and Findings:We obtained weekly virology and underlying cause-of-death mortality time series for 2005-2009 for 20 countries covering ∼35% of the world population. We applied a multivariate linear regression model to estimate pandemic respiratory mortality in each collaborating country. We then used these results plus ten country indicators in a multiple imputation model to project the mortality burden in all world countries. Between 123,000 and 203,000 pandemic respiratory deaths were estimated globally for the last 9 mo of 2009. The majority (62%-85%) were attributed to persons under 65 y of age. We observed a striking regional heterogeneity, with almost 20-fold higher mortality in some countries in the Americas than in Europe. The model attributed 148,000-249,000 respiratory deaths to influenza in an average pre-pandemic season, with only 19% in persons <65 y. Limitations include lack of representation of low-income countries among single-country estimates and an inability to study subsequent pandemic waves (2010-2012).Conclusions:We estimate that 2009 global pandemic respiratory mortality was ∼10-fold higher than the World Health Organization's laboratory-confirmed mortality count. Although the pandemic mortality estimate was similar in magnitude to that of seasonal influenza, a marked shift toward mortality among persons <65 y of age occurred, so that many more life-years were lost. The burden varied greatly among countries, corroborating early reports of far greater pandemic severity in the Americas than in Australia, New Zealand, and Europe. A collaborative network to collect and analyze mortality and hospitalization surveillance data is needed to rapidly establish the severity of future pandemics.Please see later in the article for the Editors' Summary.

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JF - Nature Methods

SN - 1548-7091

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