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Understanding influenza seasonality is necessary for determining policies for influenza control.


We characterised transmissibility during seasonal influenza epidemics, including one influenza pandemic, in Spain during the 21th century by using the moving epidemic method (MEM) to calculate intensity levels and estimate differences across seasons and age groups.


We applied the MEM to Spanish Influenza Sentinel Surveillance System data from influenza seasons 2001/02 to 2017/18. A modified version of Goldstein’s proxy was used as an epidemiological-virological parameter. We calculated the average starting week and peak, the length of the epidemic period and the length from the starting week to the peak of the epidemic, by age group and according to seasonal virus circulation.


Individuals under 15 years of age presented higher transmissibility, especially in the 2009 influenza A(H1N1) pandemic. Seasons with dominance/co-dominance of influenza A(H3N2) virus presented high intensities in older adults. The 2004/05 influenza season showed the highest influenza-intensity level for all age groups. In 12 seasons, the epidemic started between week 50 and week 3. Epidemics started earlier in individuals under 15 years of age (−1.8 weeks; 95% confidence interval (CI):−2.8 to −0.7) than in those over 64 years when influenza B virus circulated as dominant/co-dominant. The average time from start to peak was 4.3 weeks (95% CI: 3.6–5.0) and the average epidemic length was 8.7 weeks (95% CI: 7.9–9.6).


These findings provide evidence for intensity differences across seasons and age groups, and can be used guide public health actions to diminish influenza-related morbidity and mortality.


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  1. Iuliano AD, Roguski KM, Chang HH, Muscatello DJ, Palekar R, Tempia S, et al. 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. Soebiyanto RP, Gross D, Jorgensen P, Buda S, Bromberg M, Kaufman Z, et al. Associations between Meteorological Parameters and Influenza Activity in Berlin (Germany), Ljubljana (Slovenia), Castile and León (Spain) and Israeli Districts. PLoS One. 2015;10(8):e0134701.  https://doi.org/10.1371/journal.pone.0134701  PMID: 26309214 
  3. Gomez-Barroso D, León-Gómez I, Delgado-Sanz C, Larrauri A. Climatic Factors and Influenza Transmission, Spain, 2010-2015. Int J Environ Res Public Health. 2017;14(12):E1469.  https://doi.org/10.3390/ijerph14121469  PMID: 29182525 
  4. World Health Organization (WHO). Pandemic Influenza Severity Assessment (PISA): A WHO guide to assess the severity of influenza epidemics and pandemics. Geneva: WHO; 2017. Available from: http://apps.who.int/iris/bitstream/handle/10665/259392/WHO-WHE-IHM-GIP-2017.2-eng.pdf;jsessionid=8B606E83D4B7B796BABDF82CDBCEC640?sequence=1.
  5. Vega T, Lozano JE, Meerhoff T, Snacken R, Mott J, Ortiz de Lejarazu R, et al. Influenza surveillance in Europe: establishing epidemic thresholds by the moving epidemic method. Influenza Other Respir Viruses. 2013;7(4):546-58.  https://doi.org/10.1111/j.1750-2659.2012.00422.x  PMID: 22897919 
  6. Bangert M, Gil H, Oliva J, Delgado C, Vega T, DE Mateo S, et al. Pilot study to harmonize the reported influenza intensity levels within the Spanish Influenza Sentinel Surveillance System (SISSS) using the Moving Epidemic Method (MEM). Epidemiol Infect. 2017;145(4):715-22.  https://doi.org/10.1017/S0950268816002727  PMID: 27916023 
  7. Biggerstaff M, Kniss K, Jernigan DB, Brammer L, Bresee J, Garg S, et al. Systematic Assessment of Multiple Routine and Near Real-Time Indicators to Classify the Severity of Influenza Seasons and Pandemics in the United States, 2003-2004 Through 2015-2016. Am J Epidemiol. 2018;187(5):1040-50.  https://doi.org/10.1093/aje/kwx334  PMID: 29053783 
  8. Fielding JE, Regan AK, Dalton CB, Chilver MB, Blakeley D, Levy A, et al. Appropriate assessment of seasonal severity - media interpretation of notifications data versus surveillance. In: Incidence, Severity, and Impact of Influenza; 2016 Jan 21-22; Paris, France. England: The International Society for Influenza and other Respiratory Virus Diseases; 2016. Available from: https://isirv2016.influenza.hk/
  9. Murray JLK, Marques DFP, Cameron RL, Potts A, Bishop J, von Wissmann B, et al. Moving epidemic method (MEM) applied to virology data as a novel real time tool to predict peak in seasonal influenza healthcare utilisation. The Scottish experience of the 2017/18 season to date. Euro Surveill. 2018;23(11).  https://doi.org/10.2807/1560-7917.ES.2018.23.11.18-00079  PMID: 29560854 
  10. Green HK, Charlett A, Moran-Gilad J, Fleming D, Durnall H, Thomas DR, et al. Harmonizing influenza primary-care surveillance in the United Kingdom: piloting two methods to assess the timing and intensity of the seasonal epidemic across several general practice-based surveillance schemes. Epidemiol Infect. 2015;143(1):1-12.  https://doi.org/10.1017/S0950268814001757  PMID: 25023603 
  11. Vega T, Lozano JE, Meerhoff T, Snacken R, Beauté J, Jorgensen P, et al. Influenza surveillance in Europe: comparing intensity levels calculated using the moving epidemic method. Influenza Other Respir Viruses. 2015;9(5):234-46.  https://doi.org/10.1111/irv.12330  PMID: 26031655 
  12. Oliva J, Delgado-Sanz C, Larrauri ASpanish Influenza Surveillance System. Estimating the burden of seasonal influenza in Spain from surveillance of mild and severe influenza disease, 2010-2016. Influenza Other Respir Viruses. 2018;12(1):161-70.  https://doi.org/10.1111/irv.12499  PMID: 28960828 
  13. European Commission (EC). Commission Decision of 30 April 2009 amending Decision 2002/253/EC laying down case definitions for reporting communicable diseases to the Community network under Decision No 2119/98/EC of the European Parliament and of the Council (notified under document number C(2009) 3517) (Text with EEA relevance). Brussels: Official Journal of the European Union. 1.5.2009 (L 110):58. Available from: https://eur-lex.europa.eu/eli/dec/2009/363/oj
  14. 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 
  15. Lozano JE. lozalojo/mem: Second release of the MEM R library. Zenodo; 10 Nov 2016. Available from: http://doi.org/10.5281/zenodo.165983
  16. Closas P, Coma E, Méndez L. Sequential detection of influenza epidemics by the Kolmogorov-Smirnov test. BMC Med Inform Decis Mak. 2012;12(1):112.  https://doi.org/10.1186/1472-6947-12-112  PMID: 23031321 
  17. Conesa D, Martínez-Beneito MA, Amorós R, López-Quílez A. Bayesian hierarchical Poisson models with a hidden Markov structure for the detection of influenza epidemic outbreaks. Stat Methods Med Res. 2015;24(2):206-23.  https://doi.org/10.1177/0962280211414853  PMID: 21873301 
  18. Steiner SH, Grant K, Coory M, Kelly HA. Detecting the start of an influenza outbreak using exponentially weighted moving average charts. BMC Med Inform Decis Mak. 2010;10(1):37.  https://doi.org/10.1186/1472-6947-10-37  PMID: 20587013 
  19. Tillett HE, Spencer IL. Influenza surveillance in England and Wales using routine statistics. Development of ‘cusum’ graphs to compare 12 previous winters and to monitor the 1980/81 winter. J Hyg (Lond). 1982;88(1):83-94.  https://doi.org/10.1017/S0022172400069928  PMID: 7057029 
  20. Tay EL, Grant K, Kirk M, Mounts A, Kelly H. Exploring a proposed WHO method to determine thresholds for seasonal influenza surveillance. PLoS One. 2013;8(10):e77244.  https://doi.org/10.1371/journal.pone.0077244  PMID: 24146973 
  21. Beauté J, Zucs P, Korsun N, Bragstad K, Enouf V, Kossyvakis A, et al. Age-specific differences in influenza virus type and subtype distribution in the 2012/2013 season in 12 European countries. Epidemiol Infect. 2015;143(14):2950-8.  https://doi.org/10.1017/S0950268814003422  PMID: 25648399 
  22. Khiabanian H, Farrell GM, St George K, Rabadan R. Differences in patient age distribution between influenza A subtypes. PLoS One. 2009;4(8):e6832.  https://doi.org/10.1371/journal.pone.0006832  PMID: 19718262 
  23. Reed C, Katz JM, Hancock K, Balish A, Fry AMH1N1 Serosurvey Working Group. Prevalence of seropositivity to pandemic influenza A/H1N1 virus in the United States following the 2009 pandemic. PLoS One. 2012;7(10):e48187.  https://doi.org/10.1371/journal.pone.0048187  PMID: 23118949 
  24. Amato-Gauci A, Zucs P, Snacken R, Ciancio B, Lopez V, Broberg E, et al. Surveillance trends of the 2009 influenza A(H1N1) pandemic in Europe. Euro Surveill. 2011;16(26):19903.  https://doi.org/10.2807/ese.16.26.19903-en  PMID: 21745444 
  25. Gherasim A, Pozo F, de Mateo S, Gamarra IA, García-Cenoz M, Vega T, et al. . Waning protection of influenza vaccine against mild laboratory confirmed influenza A(H3N2) and B in Spain, season 2014-15. Vaccine. 2016;34(20):2371-7.  https://doi.org/10.1016/j.vaccine.2016.03.035  PMID: 27020713 
  26. European Centre for Disease Prevention and Control (ECDC). Seasonal influenza in the EU/EEA countries, 2014-2015. Stockholm: ECDC; Jan 2015. Available from: https://ecdc.europa.eu/sites/portal/files/media/en/publications/Publications/seasonal-influenza-risk-assessment.pdf
  27. Chong Y, Ikematsu H. Effect of seasonal vaccination on the selection of influenza A/H3N2 epidemic variants. Vaccine. 2017;35(2):255-63.  https://doi.org/10.1016/j.vaccine.2016.11.084  PMID: 27919631 
  28. Trebbien R, Fischer TK, Krause TG, Nielsen L, Nielsen XC, Weinreich LS, et al. Changes in genetically drifted H3N2 influenza A viruses and vaccine effectiveness in adults 65 years and older during the 2016/17 season in Denmark. J Clin Virol. 2017;94:1-7.  https://doi.org/10.1016/j.jcv.2017.06.007  PMID: 28697450 
  29. Schanzer D, Vachon J, Pelletier L. Age-specific differences in influenza A epidemic curves: do children drive the spread of influenza epidemics? Am J Epidemiol. 2011;174(1):109-17.  https://doi.org/10.1093/aje/kwr037  PMID: 21602300 
  30. Wallinga J, Teunis P, Kretzschmar M. Using data on social contacts to estimate age-specific transmission parameters for respiratory-spread infectious agents. Am J Epidemiol. 2006;164(10):936-44.  https://doi.org/10.1093/aje/kwj317  PMID: 16968863 
  31. Viboud C, Boëlle P-Y, Cauchemez S, Lavenu A, Valleron A-J, Flahault A, et al. Risk factors of influenza transmission in households. Br J Gen Pract. 2004;54(506):684-9. PMID: 15353055 
  32. Goldstein E, Pitzer VE, O’Hagan JJ, Lipsitch M. Temporally varying relative risks for infectious diseases: implications for infectious disease control. Epidemiology. 2017;28(1):136-44.  https://doi.org/10.1097/EDE.0000000000000571  PMID: 27748685 
  33. Hayward AC, Fragaszy EB, Bermingham A, Wang L, Copas A, Edmunds WJ, et al. Comparative community burden and severity of seasonal and pandemic influenza: results of the Flu Watch cohort study. Lancet Respir Med. 2014;2(6):445-54.  https://doi.org/10.1016/S2213-2600(14)70034-7  PMID: 24717637 
  34. Bollaerts K, Antoine J, Van Casteren V, Ducoffre G, Hens N, Quoilin S. Contribution of respiratory pathogens to influenza-like illness consultations. Epidemiol Infect. 2013;141(10):2196-204.  https://doi.org/10.1017/S0950268812002506  PMID: 23217849 
  35. Nair H, Nokes DJ, Gessner BD, Dherani M, Madhi SA, Singleton RJ, et al. Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: a systematic review and meta-analysis. Lancet. 2010;375(9725):1545-55.  https://doi.org/10.1016/S0140-6736(10)60206-1  PMID: 20399493 
  36. Instituto de Salud Carlos III. [Carlos III Health Institute]. Informe de vigilancia de la gripe en España. Temporada 2017-18 (semanas 40/2017-20/2018). [Influenza surveillance report in Spain. Season 2017-18 (weeks 40/2017-20/2018)]. Madrid: Carlos III Health Institute; 2018. Spanish.
  37. Larrauri Cámara A, Jiménez-Jorge S, Mateo Ontañón S, Pozo Sánchez F, Ledesma Moreno J, Casas Flecha ISpanish Influenza Surveillance System (SISS). Epidemiology of the 2009 influenza pandemic in Spain. Enferm Infecc Microbiol Clin. 2012;30(Suppl 4):2-9.  https://doi.org/10.1016/S0213-005X(12)70098-8  PMID: 23116786 
  38. Larrauri A, de Mateo SSpanish Influenza Sentinel Surveillance System. Characterisation of swabbing for virological analysis in the Spanish Influenza Sentinel Surveillance System during four influenza seasons in the period 2002-2006. Euro Surveill. 2007;12(5):E5-6.  https://doi.org/10.2807/esm.12.05.00706-en  PMID: 17991396 
  39. López-Perea N, Delgado Sanz C, Jiménez Jorge S, Simón Méndez L, de Mateo Ontañón S, Larrauri A. Swabbing characterization for virological confirmation in the Spanish Influenza Surveillance System (SISS): Prepandemic and pandemic/post-pandemic seasons. In: European Scientific Conference on Applied Infectious Disease Epidemiology (ESCAIDE); 2012 Oct 24-26; Edinburgh, United Kingdom. Stockholm: European Centre for Disease Prevention and Control; 2012. Available from: https://escaide.eu/sites/escaide/files/documents/ESCAIDE-2012-abstract-book.pdf
  40. World Organization of National Colleges Academies and Academic Associations of General Practitioners Classification Committee and the World Health Organization (WHO). ICHPPC-2: international classification of health problems in primary care (1979 revision, an adaptation of the International Classification of Diseases (9th revision, intended for use in general medicine (ICD-9-GM)). Oxford: Oxford University Press; 1979. Available from: https://apps.who.int/iris/handle/10665/40636
  41. Budd A, Blanton L, Grohskopf L, Campbell A, Dugan V, Wentworth DE, et al. Chapter 6: Influenza. In: Roush SW, Baldy LM, Kirkconnell Hall MA. Manual for the Surveillance of Vaccine-Preventable Diseases. Atlanta: Centers for Disease Control and Prevention (CDC). [Accessed 17 Dec 2019]. Available from: https://www.cdc.gov/vaccines/pubs/surv-manual/chpt06-influenza.html
  42. Negro E, Larrauri A, de Mateo S. Evaluación de las Redes Centinelas Sanitarias Integradas en el Sistema de Vigilancia de Gripe en España. Temporada 2007-2008. [Evaluation of the sentinel networks integrated into the Spanish Influenza Sentinel Surveillance System. Season 2007-2008]. [Accessed 31 Jul 2018]. Spanish.

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