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 Schanzer; Rodrigo 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; Nicholas Andrews; Helen Green; Richard Pebody; Ayoub Saei; David Shay; Cecile Viboud

doi:10.1371/journal.pmed.1001558

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, Nicholas Andrews, Helen Green, Richard Pebody, Ayoub Saei, David Shay, Cecile Viboud

^*Corresponding author for this work

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

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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.

Original language	English
Article number	e1001558
Journal	PLoS Medicine
Volume	10
Issue number	11
DOIs	https://doi.org/10.1371/journal.pmed.1001558
Publication status	Published - Nov 2013

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Simonsen, L., Spreeuwenberg, P., Lustig, R., Taylor, R. J., Fleming, D. M., Kroneman, M., Van Kerkhove, M. D., Mounts, A. W., Paget, W. J., Echenique, H., Savy, V., Muscatello, D., MacIntyre, C. R., Dwyer, D. E., Azziz-Baumgartner, E., Homaira, N., Moura, F. E. A., Schuck, C., Akwar, H., ... Viboud, C. (2013). Global Mortality Estimates for the 2009 Influenza Pandemic from the GLaMOR Project: A Modeling Study. PLoS Medicine, 10(11), Article e1001558. https://doi.org/10.1371/journal.pmed.1001558

@article{b546939959714c33802355c6aa941b5c,

title = "Global Mortality Estimates for the 2009 Influenza Pandemic from the GLaMOR Project: A Modeling Study",

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.",

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

year = "2013",

month = nov,

doi = "10.1371/journal.pmed.1001558",

language = "English",

volume = "10",

journal = "PLoS Medicine",

issn = "1549-1277",

publisher = "Public Library of Science",

number = "11",

}

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, H, 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

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, Nicholas

AU - Green, Helen

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.

UR - http://www.scopus.com/inward/record.url?scp=84889074313&partnerID=8YFLogxK

U2 - 10.1371/journal.pmed.1001558

DO - 10.1371/journal.pmed.1001558

M3 - Article

C2 - 24302890

AN - SCOPUS:84889074313

SN - 1549-1277

VL - 10

JO - PLoS Medicine

JF - PLoS Medicine

IS - 11

M1 - e1001558

ER -

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

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