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Published in: BMC Infectious Diseases 1/2012

Open Access 01-12-2012 | Research article

The community impact of the 2009 influenza pandemic in the WHO European Region: a comparison with historical seasonal data from 28 countries

Authors: Liana Martirosyan, W John Paget, Pernille Jorgensen, Caroline S Brown, Tamara J Meerhoff, Dmitriy Pereyaslov, Joshua A Mott, the EuroFlu group

Published in: BMC Infectious Diseases | Issue 1/2012

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Abstract

Background

The world has recently experienced the first influenza pandemic of the 21st century that lasted 14 months from June 2009 to August 2010. This study aimed to compare the timing, geographic spread and community impact during the winter wave of influenza pandemic A (H1N1) 2009 to historical influenza seasons in countries of the WHO European region.

Methods

We assessed the timing of pandemic by comparing the median peak of influenza activity in countries of the region during the last seven influenza seasons. The peaks of influenza activity were selected by two independent researchers using predefined rules. The geographic spread was assessed by correlating the peak week of influenza activity in included countries against the longitude and latitude of the central point in each country. To assess the community impact of pandemic influenza, we constructed linear regression models to compare the total and age-specific influenza-like-illness (ILI) or acute respiratory infection (ARI) rates reported by the countries in the pandemic season to those observed in the previous six influenza seasons.

Results

We found that the influenza activity reached its peak during the pandemic, on average, 10.5 weeks (95% CI 6.4-14.2) earlier than during the previous 6 seasons in the Region, and there was a west to east spread of pandemic A(H1N1) influenza virus in the western part of the Region. A regression analysis showed that the total ILI or ARI rates were not higher than historical rates in 19 of the 28 countries. However, in countries with age-specific data, there were significantly higher consultation rates in the 0-4 and/or 5-14 age groups in 11 of the 20 countries.

Conclusions

Using routine influenza surveillance data, we found that pandemic influenza had several differential features compared to historical seasons in the region. It arrived earlier, caused significantly higher number of outpatient consultations in children in most countries and followed west to east spread that was previously observed during some influenza seasons with dominant A (H3N2) ifluenza viruses. The results of this study help to understand the epidemiology of 2009 influenza pandemic and can be used for pandemic preparedness planning.
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Literature
2.
go back to reference Shrestha SS, Swerdlow DL, Borse RH, Prabhu VS, Finelli L, Atkins CY, et al: Estimating the Burden of 2009 Pandemic Influenza A (H1N1) in the United States (April 2009-April 2010). Clinical Infectious Diseases. 2011, 52: S75-S82. 10.1093/cid/ciq012.CrossRefPubMed Shrestha SS, Swerdlow DL, Borse RH, Prabhu VS, Finelli L, Atkins CY, et al: Estimating the Burden of 2009 Pandemic Influenza A (H1N1) in the United States (April 2009-April 2010). Clinical Infectious Diseases. 2011, 52: S75-S82. 10.1093/cid/ciq012.CrossRefPubMed
3.
go back to reference Nguyen-Van-Tam JS, Openshaw PJ, Hashim A, Gadd EM, Lim WS, Semple MG, et al: Risk factors for hospitalisation and poor outcome with pandemic A/H1N1 influenza: United Kingdom first wave (May-September 2009). Thorax. 2010, 65: 645-651. 10.1136/thx.2010.135210.CrossRefPubMedPubMedCentral Nguyen-Van-Tam JS, Openshaw PJ, Hashim A, Gadd EM, Lim WS, Semple MG, et al: Risk factors for hospitalisation and poor outcome with pandemic A/H1N1 influenza: United Kingdom first wave (May-September 2009). Thorax. 2010, 65: 645-651. 10.1136/thx.2010.135210.CrossRefPubMedPubMedCentral
5.
go back to reference Centers for Disease Control and Prevention (CDC): Swine influenza A (H1N1) infection in two children--Southern California, March-April 2009. MMWR Morb Mortal Wkly Rep. 2009, 58: 400-402. Centers for Disease Control and Prevention (CDC): Swine influenza A (H1N1) infection in two children--Southern California, March-April 2009. MMWR Morb Mortal Wkly Rep. 2009, 58: 400-402.
7.
go back to reference Reed C, Angulo FJ, Swerdlow DL, Lipsitch M, Meltzer MI, Jernigan D, et al: Estimates of the prevalence of pandemic (H1N1) 2009, United States, April-July 2009. Emerg Infect Dis. 2009, 15: 2004-2007.CrossRefPubMedPubMedCentral Reed C, Angulo FJ, Swerdlow DL, Lipsitch M, Meltzer MI, Jernigan D, et al: Estimates of the prevalence of pandemic (H1N1) 2009, United States, April-July 2009. Emerg Infect Dis. 2009, 15: 2004-2007.CrossRefPubMedPubMedCentral
8.
go back to reference Novel Swine-Origin Influenza A (H1N1) Investigation Team: Emergence of a Novel Swine-Origin Influenza A (H1N1) Virus in Humans. New England Journal of Medicine. 2009, 360: 2605-2615.CrossRef Novel Swine-Origin Influenza A (H1N1) Investigation Team: Emergence of a Novel Swine-Origin Influenza A (H1N1) Virus in Humans. New England Journal of Medicine. 2009, 360: 2605-2615.CrossRef
10.
go back to reference Neuzil KM, Hohlbein C, Zhu Y: Illness among schoolchildren during influenza season: effect on school absenteeism, parental absenteeism from work, and secondary illness in families. Arch Pediatr Adolesc Med. 2002, 156: 986-991.CrossRefPubMed Neuzil KM, Hohlbein C, Zhu Y: Illness among schoolchildren during influenza season: effect on school absenteeism, parental absenteeism from work, and secondary illness in families. Arch Pediatr Adolesc Med. 2002, 156: 986-991.CrossRefPubMed
11.
go back to reference van Hoek AJ, Underwood A, Jit M, Miller E, Edmunds WJ: The Impact of Pandemic Influenza H1N1 on Health-Related Quality of Life: A Prospective Population-Based Study. PLoS ONE. 2011, 6: e17030-10.1371/journal.pone.0017030.CrossRefPubMedPubMedCentral van Hoek AJ, Underwood A, Jit M, Miller E, Edmunds WJ: The Impact of Pandemic Influenza H1N1 on Health-Related Quality of Life: A Prospective Population-Based Study. PLoS ONE. 2011, 6: e17030-10.1371/journal.pone.0017030.CrossRefPubMedPubMedCentral
12.
go back to reference Kelly HA, Grant KA, Williams S, Fielding J, Smith D: Epidemiological characteristics of pandemic influenza H1N1 2009 and seasonal influenza infection. Med J Aust. 2009, 191: 146-149.PubMed Kelly HA, Grant KA, Williams S, Fielding J, Smith D: Epidemiological characteristics of pandemic influenza H1N1 2009 and seasonal influenza infection. Med J Aust. 2009, 191: 146-149.PubMed
14.
go back to reference Nicoll A, Ammon A, Amato A, Ciancio B, Zucs P, Devaux I, et al: Experience and lessons from surveillance and studies of the 2009 pandemic in Europe. Public Health. 2010, 124: 14-23. 10.1016/j.puhe.2009.12.001.CrossRefPubMed Nicoll A, Ammon A, Amato A, Ciancio B, Zucs P, Devaux I, et al: Experience and lessons from surveillance and studies of the 2009 pandemic in Europe. Public Health. 2010, 124: 14-23. 10.1016/j.puhe.2009.12.001.CrossRefPubMed
15.
go back to reference Paget J, Marquet R, Meijer A: van dV: Influenza activity in Europe during eight seasons (1999-2007): an evaluation of the indicators used to measure activity and an assessment of the timing, length and course of peak activity (spread) across Europe. BMC Infect Dis. 2007, 7: 141-10.1186/1471-2334-7-141.CrossRefPubMedPubMedCentral Paget J, Marquet R, Meijer A: van dV: Influenza activity in Europe during eight seasons (1999-2007): an evaluation of the indicators used to measure activity and an assessment of the timing, length and course of peak activity (spread) across Europe. BMC Infect Dis. 2007, 7: 141-10.1186/1471-2334-7-141.CrossRefPubMedPubMedCentral
16.
go back to reference Deckers JG, Paget WJ, Schellevis FG, Fleming DM: European primary care surveillance networks: their structure and operation. Fam Pract. 2006, 23: 151-158.CrossRefPubMed Deckers JG, Paget WJ, Schellevis FG, Fleming DM: European primary care surveillance networks: their structure and operation. Fam Pract. 2006, 23: 151-158.CrossRefPubMed
17.
go back to reference Aguilera JF, Paget WJ, Mosnier A, Heijnen ML, Uphoff H, van Dv, et al: Heterogeneous case definitions used for the surveillance of influenza in Europe. Eur J Epidemiol. 2003, 18: 751-754.CrossRefPubMed Aguilera JF, Paget WJ, Mosnier A, Heijnen ML, Uphoff H, van Dv, et al: Heterogeneous case definitions used for the surveillance of influenza in Europe. Eur J Epidemiol. 2003, 18: 751-754.CrossRefPubMed
22.
go back to reference Shaman J, Kohn M: Absolute humidity modulates influenza survival, transmission, and seasonality. Proc Natl Acad Sci USA. 2009, 106: 3243-3248. 10.1073/pnas.0806852106.CrossRefPubMedPubMedCentral Shaman J, Kohn M: Absolute humidity modulates influenza survival, transmission, and seasonality. Proc Natl Acad Sci USA. 2009, 106: 3243-3248. 10.1073/pnas.0806852106.CrossRefPubMedPubMedCentral
23.
go back to reference Shaman J, Pitzer VE, Viboud C, Grenfell BT, Lipsitch M: Absolute humidity and the seasonal onset of influenza in the continental United States. PLoS Biol. 2010, 8: e1000316-10.1371/journal.pbio.1000316.CrossRefPubMedPubMedCentral Shaman J, Pitzer VE, Viboud C, Grenfell BT, Lipsitch M: Absolute humidity and the seasonal onset of influenza in the continental United States. PLoS Biol. 2010, 8: e1000316-10.1371/journal.pbio.1000316.CrossRefPubMedPubMedCentral
25.
go back to reference Chao DL, Halloran ME, Longini IM: School opening dates predict pandemic influenza A(H1N1) outbreaks in the United States. J Infect Dis. 2010, 202: 877-880. 10.1086/655810.CrossRefPubMedPubMedCentral Chao DL, Halloran ME, Longini IM: School opening dates predict pandemic influenza A(H1N1) outbreaks in the United States. J Infect Dis. 2010, 202: 877-880. 10.1086/655810.CrossRefPubMedPubMedCentral
26.
go back to reference Shaman J, Goldstein E, Lipsitch M: Absolute Humidity and Pandemic Versus Epidemic Influenza. American Journal of Epidemiology. 2011, 173: 127-135. 10.1093/aje/kwq347.CrossRefPubMed Shaman J, Goldstein E, Lipsitch M: Absolute Humidity and Pandemic Versus Epidemic Influenza. American Journal of Epidemiology. 2011, 173: 127-135. 10.1093/aje/kwq347.CrossRefPubMed
28.
go back to reference Paget WJ, Meerhoff TJ, Meijer A: Epidemiological and virological assessment of influenza activity in Europe during the 2003-2004 season. Euro Surveill. 2005, 10: 107-111.PubMed Paget WJ, Meerhoff TJ, Meijer A: Epidemiological and virological assessment of influenza activity in Europe during the 2003-2004 season. Euro Surveill. 2005, 10: 107-111.PubMed
29.
go back to reference Holmes EC, Ghedin E, Miller N, Taylor J, Bao Y, St George K, et al: Whole-Genome Analysis of Human Influenza A Virus Reveals Multiple Persistent Lineages and Reassortment among Recent H3N2 Viruses. PLoS Biol. 2005, 3: e300-10.1371/journal.pbio.0030300.CrossRefPubMedPubMedCentral Holmes EC, Ghedin E, Miller N, Taylor J, Bao Y, St George K, et al: Whole-Genome Analysis of Human Influenza A Virus Reveals Multiple Persistent Lineages and Reassortment among Recent H3N2 Viruses. PLoS Biol. 2005, 3: e300-10.1371/journal.pbio.0030300.CrossRefPubMedPubMedCentral
30.
go back to reference Belongia EA, Irving SA, Waring SC, Coleman LA, Meece JK, Vandermause M, et al: Clinical characteristics and 30-day outcomes for influenza A 2009 (H1N1), 2008-2009 (H1N1), and 2007-2008 (H3N2) infections. JAMA. 2010, 304: 1091-1098. 10.1001/jama.2010.1277.CrossRefPubMed Belongia EA, Irving SA, Waring SC, Coleman LA, Meece JK, Vandermause M, et al: Clinical characteristics and 30-day outcomes for influenza A 2009 (H1N1), 2008-2009 (H1N1), and 2007-2008 (H3N2) infections. JAMA. 2010, 304: 1091-1098. 10.1001/jama.2010.1277.CrossRefPubMed
31.
go back to reference Carcione D, Giele C, Dowse GK, Mak DB, Goggin L, Kwan K, et al: Comparison of pandemic (H1N1) 2009 and seasonal influenza, Western Australia, 2009. Emerg Infect Dis. 2010, 16: 1388-1395.CrossRefPubMedPubMedCentral Carcione D, Giele C, Dowse GK, Mak DB, Goggin L, Kwan K, et al: Comparison of pandemic (H1N1) 2009 and seasonal influenza, Western Australia, 2009. Emerg Infect Dis. 2010, 16: 1388-1395.CrossRefPubMedPubMedCentral
32.
go back to reference Cowling BJ, Chan KH, Fang VJ, Lau LL, So HC, Fung RO, et al: Comparative epidemiology of pandemic and seasonal influenza A in households. N Engl J Med. 2010, 362: 2175-2184. 10.1056/NEJMoa0911530.CrossRefPubMedPubMedCentral Cowling BJ, Chan KH, Fang VJ, Lau LL, So HC, Fung RO, et al: Comparative epidemiology of pandemic and seasonal influenza A in households. N Engl J Med. 2010, 362: 2175-2184. 10.1056/NEJMoa0911530.CrossRefPubMedPubMedCentral
33.
go back to reference Paget WJ, Meerhoff TJ, Goddard NL: Mild to moderate influenza activity in Europe and the detection of novel A(H1N2) and B viruses during the winter of 2001-02. Euro Surveill. 2002, 7: 147-157.PubMed Paget WJ, Meerhoff TJ, Goddard NL: Mild to moderate influenza activity in Europe and the detection of novel A(H1N2) and B viruses during the winter of 2001-02. Euro Surveill. 2002, 7: 147-157.PubMed
34.
go back to reference Brownstein JS, Wolfe CJ, Mandl KD: Empirical evidence for the effect of airline travel on inter-regional influenza spread in the United States. PLoS Med. 2006, 3: e401-10.1371/journal.pmed.0030401.CrossRefPubMedPubMedCentral Brownstein JS, Wolfe CJ, Mandl KD: Empirical evidence for the effect of airline travel on inter-regional influenza spread in the United States. PLoS Med. 2006, 3: e401-10.1371/journal.pmed.0030401.CrossRefPubMedPubMedCentral
35.
go back to reference Miller E, Hoschler K, Hardelid P, Stanford E, Andrews N, Zambon M: Incidence of 2009 pandemic influenza A H1N1 infection in England: a cross-sectional serological study. Lancet. 2010, 375: 1100-1108. 10.1016/S0140-6736(09)62126-7.CrossRefPubMed Miller E, Hoschler K, Hardelid P, Stanford E, Andrews N, Zambon M: Incidence of 2009 pandemic influenza A H1N1 infection in England: a cross-sectional serological study. Lancet. 2010, 375: 1100-1108. 10.1016/S0140-6736(09)62126-7.CrossRefPubMed
36.
go back to reference Hancock K, Veguilla V, Lu X, Zhong W, Butler EN, Sun H, et al: Cross-reactive antibody responses to the 2009 pandemic H1N1 influenza virus. N Engl J Med. 2009, 361: 1945-1952. 10.1056/NEJMoa0906453.CrossRefPubMed Hancock K, Veguilla V, Lu X, Zhong W, Butler EN, Sun H, et al: Cross-reactive antibody responses to the 2009 pandemic H1N1 influenza virus. N Engl J Med. 2009, 361: 1945-1952. 10.1056/NEJMoa0906453.CrossRefPubMed
37.
go back to reference Ikonen N, Strengell M, Kinnunen L, Osterlund P, Pirhonen J, Broman M, et al: High frequency of cross-reacting antibodies against 2009 pandemic influenza A(H1N1) virus among the elderly in Finland. Euro Surveill. 2010, 15: Ikonen N, Strengell M, Kinnunen L, Osterlund P, Pirhonen J, Broman M, et al: High frequency of cross-reacting antibodies against 2009 pandemic influenza A(H1N1) virus among the elderly in Finland. Euro Surveill. 2010, 15:
38.
go back to reference Rizzo C, Rota MC, Bella A, Alfonsi V, Declich S, Caporali MG, et al: Cross-reactive antibody responses to the 2009 A/H1N1v influenza virus in the Italian population in the pre-pandemic period. Vaccine. 2010, 28: 3558-3562. 10.1016/j.vaccine.2010.03.006.CrossRefPubMed Rizzo C, Rota MC, Bella A, Alfonsi V, Declich S, Caporali MG, et al: Cross-reactive antibody responses to the 2009 A/H1N1v influenza virus in the Italian population in the pre-pandemic period. Vaccine. 2010, 28: 3558-3562. 10.1016/j.vaccine.2010.03.006.CrossRefPubMed
39.
go back to reference Tang JW, Tambyah PA, Wilder-Smith A, Puong KY, Shaw R, Barr IG, et al: Cross-reactive antibodies to pandemic (H1N1) 2009 virus, Singapore. Emerg Infect Dis. 2010, 16: 874-876.CrossRefPubMedPubMedCentral Tang JW, Tambyah PA, Wilder-Smith A, Puong KY, Shaw R, Barr IG, et al: Cross-reactive antibodies to pandemic (H1N1) 2009 virus, Singapore. Emerg Infect Dis. 2010, 16: 874-876.CrossRefPubMedPubMedCentral
40.
go back to reference Miller MA, Viboud C, Balinska M, Simonsen L: The Signature Features of Influenza Pandemics - Implications for Policy. New England Journal of Medicine. 2009, 360: 2595-2598. 10.1056/NEJMp0903906.CrossRefPubMed Miller MA, Viboud C, Balinska M, Simonsen L: The Signature Features of Influenza Pandemics - Implications for Policy. New England Journal of Medicine. 2009, 360: 2595-2598. 10.1056/NEJMp0903906.CrossRefPubMed
41.
go back to reference Stephenson I, Zambon M: The epidemiology of influenza. Occup Med (Lond). 2002, 52: 241-247. 10.1093/occmed/52.5.241.CrossRef Stephenson I, Zambon M: The epidemiology of influenza. Occup Med (Lond). 2002, 52: 241-247. 10.1093/occmed/52.5.241.CrossRef
42.
go back to reference Tilston N, Eames K, Paolotti D, Ealden T, Edmunds WJ: Internet-based surveillance of Influenza-like-illness in the UK during the 2009 H1N1 influenza pandemic. BMC Public Health. 2010, 10: 650-10.1186/1471-2458-10-650.CrossRefPubMedPubMedCentral Tilston N, Eames K, Paolotti D, Ealden T, Edmunds WJ: Internet-based surveillance of Influenza-like-illness in the UK during the 2009 H1N1 influenza pandemic. BMC Public Health. 2010, 10: 650-10.1186/1471-2458-10-650.CrossRefPubMedPubMedCentral
43.
go back to reference Cauchemez S, Valleron AJ, Boelle PY, Flahault A, Ferguson NM: Estimating the impact of school closure on influenza transmission from Sentinel data. Nature. 2008, 452: 750-754. 10.1038/nature06732.CrossRefPubMed Cauchemez S, Valleron AJ, Boelle PY, Flahault A, Ferguson NM: Estimating the impact of school closure on influenza transmission from Sentinel data. Nature. 2008, 452: 750-754. 10.1038/nature06732.CrossRefPubMed
44.
go back to reference Welliver R, Monto AS, Carewicz O, Schatteman E, Hassman M, Hedrick J, et al: Effectiveness of Oseltamivir in Preventing Influenza in Household Contacts. JAMA: The Journal of the American Medical Association. 2001, 285: 748-754. 10.1001/jama.285.6.748.CrossRefPubMed Welliver R, Monto AS, Carewicz O, Schatteman E, Hassman M, Hedrick J, et al: Effectiveness of Oseltamivir in Preventing Influenza in Household Contacts. JAMA: The Journal of the American Medical Association. 2001, 285: 748-754. 10.1001/jama.285.6.748.CrossRefPubMed
45.
go back to reference Aledort J, Lurie N, Wasserman J, Bozzette S: Non-pharmaceutical public health interventions for pandemic influenza: an evaluation of the evidence base. BMC Public Health. 2007, 7: 208-10.1186/1471-2458-7-208.CrossRefPubMedPubMedCentral Aledort J, Lurie N, Wasserman J, Bozzette S: Non-pharmaceutical public health interventions for pandemic influenza: an evaluation of the evidence base. BMC Public Health. 2007, 7: 208-10.1186/1471-2458-7-208.CrossRefPubMedPubMedCentral
Metadata
Title
The community impact of the 2009 influenza pandemic in the WHO European Region: a comparison with historical seasonal data from 28 countries
Authors
Liana Martirosyan
W John Paget
Pernille Jorgensen
Caroline S Brown
Tamara J Meerhoff
Dmitriy Pereyaslov
Joshua A Mott
the EuroFlu group
Publication date
01-12-2012
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2012
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/1471-2334-12-36

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