1887
  1. Home
  2. Eurosurveillance
  3. Volume 24, Issue 14, 04/Apr/2019
  4. Article
Research Open Access
Like 0
Download

Abstract

Introduction

Estimating the contribution of influenza to excess mortality in the population presents substantial methodological challenges.

Aim

In a modelling study we combined environmental, epidemiological and laboratory surveillance data to estimate influenza-attributable mortality in Greece, over four seasons (2013/14 to 2016/17), specifically addressing the lag dimension and the confounding effect of temperature.

Methods

Associations of influenza type/subtype-specific incidence proxies and of daily mean temperature with mortality were estimated with a distributed-lag nonlinear model with 30 days of maximum lag, separately by age group (all ages, 15–64 and ≥ 65 years old). Total and weekly deaths attributable to influenza and cold temperatures were calculated.

Results

Overall influenza-attributable mortality was 23.6 deaths per 100,000 population per year (95% confidence interval (CI): 17.8 to 29.2), and varied greatly between seasons, by influenza type/subtype and by age group, with the vast majority occurring in persons aged ≥ 65 years. Most deaths were attributable to A(H3N2), followed by influenza B. During periods of A(H1N1)pdm09 circulation, weekly attributable mortality to this subtype among people ≥ 65 years old increased rapidly at first, but then fell to zero and even negative, suggesting a mortality displacement (harvesting) effect. Mortality attributable to cold temperatures was much higher than that attributable to influenza.

Conclusions

Studies of influenza-attributable mortality need to consider distributed-lag effects, stratify by age group and adjust both for circulating influenza virus types/subtypes and daily mean temperatures, in order to produce reliable estimates. Our approach addresses these issues, is readily applicable in the context of influenza surveillance, and can be useful for other countries.

© Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2019.24.14.1800118
2019-04-04
2024-04-18
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2019.24.14.1800118
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/24/14/eurosurv-24-14-2.html?itemId=/content/10.2807/1560-7917.ES.2019.24.14.1800118&mimeType=html&fmt=ahah

References

  1. Iuliano AD, Roguski KM, Chang HH, Muscatello DJ, Palekar R, Tempia S, et al. , Global Seasonal Influenza-associated Mortality Collaborator Network. Estimates of global seasonal influenza-associated respiratory mortality: a modelling study. Lancet. 2018;391(10127):1285-300.  https://doi.org/10.1016/S0140-6736(17)33293-2  PMID: 29248255 
  2. Osterholm MT, Kelley NS, Sommer A, Belongia EA. Efficacy and effectiveness of influenza vaccines: a systematic review and meta-analysis. Lancet Infect Dis. 2012;12(1):36-44.  https://doi.org/10.1016/S1473-3099(11)70295-X  PMID: 22032844 
  3. Belongia EA, Simpson MD, King JP, Sundaram ME, Kelley NS, Osterholm MT, et al. Variable influenza vaccine effectiveness by subtype: a systematic review and meta-analysis of test-negative design studies. Lancet Infect Dis. 2016;16(8):942-51.  https://doi.org/10.1016/S1473-3099(16)00129-8  PMID: 27061888 
  4. Li L, Wong JY, Wu P, Bond HS, Lau EHY, Sullivan SG, et al. Heterogeneity in Estimates of the Impact of Influenza on Population Mortality: A Systematic Review. Am J Epidemiol. 2018;187(2):378-88.  https://doi.org/10.1093/aje/kwx270  PMID: 28679157 
  5. Nunes B, Viboud C, Machado A, Ringholz C, Rebelo-de-Andrade H, Nogueira P, et al. Excess mortality associated with influenza epidemics in Portugal, 1980 to 2004. PLoS One. 2011;6(6):e20661.  https://doi.org/10.1371/journal.pone.0020661  PMID: 21713040 
  6. Gasparrini A, Guo Y, Hashizume M, Lavigne E, Zanobetti A, Schwartz J, et al. Mortality risk attributable to high and low ambient temperature: a multicountry observational study. Lancet. 2015;386(9991):369-75.  https://doi.org/10.1016/S0140-6736(14)62114-0  PMID: 26003380 
  7. Schwartz J. The distributed lag between air pollution and daily deaths. Epidemiology. 2000;11(3):320-6.  https://doi.org/10.1097/00001648-200005000-00016  PMID: 10784251 
  8. Cooper BS, Kotirum S, Kulpeng W, Praditsitthikorn N, Chittaganpitch M, Limmathurotsakul D, et al. Mortality attributable to seasonal influenza A and B infections in Thailand, 2005-2009: a longitudinal study. Am J Epidemiol. 2015;181(11):898-907.  https://doi.org/10.1093/aje/kwu360  PMID: 25899091 
  9. Green HK, Andrews N, Fleming D, Zambon M, Pebody R. Mortality attributable to influenza in England and Wales prior to, during and after the 2009 pandemic. PLoS One. 2013;8(12):e79360.  https://doi.org/10.1371/journal.pone.0079360  PMID: 24348993 
  10. Hardelid P, Pebody R, Andrews N. Mortality caused by influenza and respiratory syncytial virus by age group in England and Wales 1999-2010. Influenza Other Respir Viruses. 2013;7(1):35-45.  https://doi.org/10.1111/j.1750-2659.2012.00345.x  PMID: 22405488 
  11. van Asten L, van den Wijngaard C, van Pelt W, van de Kassteele J, Meijer A, van der Hoek W, et al. Mortality attributable to 9 common infections: significant effect of influenza A, respiratory syncytial virus, influenza B, norovirus, and parainfluenza in elderly persons. J Infect Dis. 2012;206(5):628-39.  https://doi.org/10.1093/infdis/jis415  PMID: 22723641 
  12. Gasparrini A, Armstrong B, Kenward MG. Distributed lag non-linear models. Stat Med. 2010;29(21):2224-34.  https://doi.org/10.1002/sim.3940  PMID: 20812303 
  13. Reichert TA, Simonsen L, Sharma A, Pardo SA, Fedson DS, Miller MA. Influenza and the winter increase in mortality in the United States, 1959-1999. Am J Epidemiol. 2004;160(5):492-502.  https://doi.org/10.1093/aje/kwh227  PMID: 15321847 
  14. Donaldson GC, Keatinge WR. Excess winter mortality: influenza or cold stress? Observational study. BMJ. 2002;324(7329):89-90.  https://doi.org/10.1136/bmj.324.7329.89  PMID: 11786453 
  15. National Oceanic and Atmospheric Administration (NOAA). National Centers for Environmental Information (NCEI) Climate Data Online Search. [Accessed 26 Dec 2017]. Available from: https://www.ncdc.noaa.gov/cdo-web/search
  16. Schlaud M, Brenner MH, Hoopmann M, Schwartz FW. Approaches to the denominator in practice-based epidemiology: a critical overview. J Epidemiol Community Health. 1998;52(Suppl 1):13S-9S. PMID: 9764265 
  17. Goldstein E, Viboud C, Charu V, Lipsitch M. Improving the estimation of influenza-related mortality over a seasonal baseline. Epidemiology. 2012;23(6):829-38.  https://doi.org/10.1097/EDE.0b013e31826c2dda  PMID: 22992574 
  18. Goldstein E, Cobey S, Takahashi S, Miller JC, Lipsitch M. Predicting the epidemic sizes of influenza A/H1N1, A/H3N2, and B: a statistical method. PLoS Med. 2011;8(7):e1001051.  https://doi.org/10.1371/journal.pmed.1001051  PMID: 21750666 
  19. Zanobetti A, Wand MP, Schwartz J, Ryan LM. Generalized additive distributed lag models: quantifying mortality displacement. Biostatistics. 2000;1(3):279-92.  https://doi.org/10.1093/biostatistics/1.3.279  PMID: 12933509 
  20. Gasparrini A, Leone M. Attributable risk from distributed lag models. BMC Med Res Methodol. 2014;14(1):55.  https://doi.org/10.1186/1471-2288-14-55  PMID: 24758509 
  21. R Core Team. R: A Language and Environment for Statistical Computing [Internet]. Vienna, Austria: R Foundation for Statistical Computing; 2015. Available from: http://www.R-project.org/
  22. Gasparrini A. Distributed Lag Linear and Non-Linear Models in R: The Package dlnm. J Stat Softw. 2011;43(8):1-20.  https://doi.org/10.18637/jss.v043.i08  PMID: 22003319 
  23. Rocklöv J, Forsberg B, Meister K. Winter mortality modifies the heat-mortality association the following summer. Eur Respir J. 2009;33(2):245-51.  https://doi.org/10.1183/09031936.00037808  PMID: 18799511 
  24. Kinney PL, Schwartz J, Pascal M, Petkova E, Tertre AL, Medina S, et al. Winter Season Mortality: Will Climate Warming Bring Benefits? Environ Res Lett. 2015;10(6):064016.  https://doi.org/10.1088/1748-9326/10/6/064016  PMID: 26495037 
  25. Hajat S, Gasparrini A. The Excess Winter Deaths Measure: Why Its Use Is Misleading for Public Health Understanding of Cold-related Health Impacts. Epidemiology. 2016;27(4):486-91.  https://doi.org/10.1097/EDE.0000000000000479  PMID: 26986872 
  26. Nicoll A, Ciancio BC, Lopez Chavarrias V, Mølbak K, Pebody R, Pedzinski B, et al. Influenza-related deaths--available methods for estimating numbers and detecting patterns for seasonal and pandemic influenza in Europe. Euro Surveill. 2012;17(18):20162.  https://doi.org/10.2807/ese.17.18.20162-en  PMID: 22587958 
  27. Vestergaard LS, Nielsen J, Krause TG, Espenhain L, Tersago K, Bustos Sierra N, et al. Excess all-cause and influenza-attributable mortality in Europe, December 2016 to February 2017. Euro Surveill. 2017;22(14):30506.  https://doi.org/10.2807/1560-7917.ES.2017.22.14.30506  PMID: 28424146 
  28. Nielsen J, Krause TG, Mølbak K. Influenza-associated mortality determined from all-cause mortality, Denmark 2010/11-2016/17: The FluMOMO model. Influenza Other Respir Viruses. 2018;12(5):591-604.  https://doi.org/10.1111/irv.12564  PMID: 29660769 
  29. Antalis E, Oikonomopoulou Z, Kottaridi C, Kossyvakis A, Spathis A, Magkana M, et al. Mixed viral infections of the respiratory tract; an epidemiological study during consecutive winter seasons. J Med Virol. 2018;90(4):663-70.  https://doi.org/10.1002/jmv.25006  PMID: 29244214 
  30. Loerbroks A, Stock C, Bosch JA, Litaker DG, Apfelbacher CJ. Influenza vaccination coverage among high-risk groups in 11 European countries. Eur J Public Health. 2012;22(4):562-8.  https://doi.org/10.1093/eurpub/ckr094  PMID: 21750011 
  31. Goodwin K, Viboud C, Simonsen L. Antibody response to influenza vaccination in the elderly: a quantitative review. Vaccine. 2006;24(8):1159-69.  https://doi.org/10.1016/j.vaccine.2005.08.105  PMID: 16213065 
  32. Paules CI, Sullivan SG, Subbarao K, Fauci AS. Chasing Seasonal Influenza - The Need for a Universal Influenza Vaccine. N Engl J Med. 2018;378(1):7-9.  https://doi.org/10.1056/NEJMp1714916  PMID: 29185857 
Mortality attributable to seasonal influenza in Greece, 2013 to 2017: variation by type/subtype and age, and a possible harvesting effect
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Theodore+Lytras&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Lytras Theodore</a>, <a href="/search?value1=Katerina+Pantavou&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Pantavou Katerina</a>, <a href="/search?value1=Elisavet+Mouratidou&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Mouratidou Elisavet</a>, <a href="/search?value1=Sotirios+Tsiodras&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Tsiodras Sotirios</a></span>. Mortality attributable to seasonal influenza in Greece, 2013 to 2017: variation by type/subtype and age, and a possible harvesting effect. <a href="/content/ecdc">Euro Surveill.</a> 2019;24(14):pii=1800118. <a href="https://doi.org/10.2807/1560-7917.ES.2019.24.14.1800118" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2019.24.14.1800118</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 14 Mar 2018;&nbsp;&nbsp; <span class="generated">Accepted</span>: 21 Mar 2019 </span> </p>
/content/10.2807/1560-7917.ES.2019.24.14.1800118
/content/10.2807/1560-7917.ES.2019.24.14.1800118
Loading

Data & Media loading...

Supplementary data

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error