Transmissibility of influenza during the 21st-century epidemics, Spain, influenza seasons 2001/02 to 2017/18

Lidia Redondo-Bravo, Concepción Delgado-Sanz, Jesús Oliva, Tomás Vega, Jose Lozano, Amparo Larrauri, Spanish Influenza Sentinel Surveillance System, Lidia Redondo-Bravo, Concepción Delgado-Sanz, Jesús Oliva, Tomás Vega, Jose Lozano, Amparo Larrauri, Spanish Influenza Sentinel Surveillance System

Abstract

BackgroundUnderstanding influenza seasonality is necessary for determining policies for influenza control.AimWe 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.MethodsWe 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.ResultsIndividuals 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).ConclusionsThese 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.

Keywords: epidemiology; influenza; influenza-like illnesses; surveillance.

Conflict of interest statement

Conflict of interest: None declared.

Figures

Figure 1
Figure 1
Weekly analysed swabs and influenza positivity rate, Spain, influenza seasons 2001/02–2017/18
Figure 2
Figure 2
Influenza epidemic thresholds and intensity levels according to the moving epidemic method (MEM), overall (A) and by age group (B,C,D), using Proxya, Spain, influenza seasons 2001/02–2017/18

References

    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. 10.1016/S0140-6736(17)33293-2
    1. 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. 10.1371/journal.pone.0134701
    1. 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. 10.3390/ijerph14121469
    1. 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: .
    1. 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. 10.1111/j.1750-2659.2012.00422.x
    1. 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. 10.1017/S0950268816002727
    1. 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. 10.1093/aje/kwx334
    1. 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:
    1. 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). 10.2807/1560-7917.ES.2018.23.11.18-00079
    1. 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. 10.1017/S0950268814001757
    1. 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. 10.1111/irv.12330
    1. Oliva J, Delgado-Sanz C, Larrauri A, Spanish 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. 10.1111/irv.12499
    1. 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:
    1. 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. 10.1371/journal.pmed.1001051
    1. Lozano JE. lozalojo/mem: Second release of the MEM R library. Zenodo; 10 Nov 2016. Available from: 10.5281/zenodo.165983
    1. 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. 10.1186/1472-6947-12-112
    1. 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. 10.1177/0962280211414853
    1. 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. 10.1186/1472-6947-10-37
    1. 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. 10.1017/S0022172400069928
    1. 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. 10.1371/journal.pone.0077244
    1. 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. 10.1017/S0950268814003422
    1. Khiabanian H, Farrell GM, St George K, Rabadan R. Differences in patient age distribution between influenza A subtypes. PLoS One. 2009;4(8):e6832. 10.1371/journal.pone.0006832
    1. Reed C, Katz JM, Hancock K, Balish A, Fry AM, H1N1 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. 10.1371/journal.pone.0048187
    1. 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. 10.2807/ese.16.26.19903-en
    1. 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. 10.1016/j.vaccine.2016.03.035
    1. European Centre for Disease Prevention and Control (ECDC). Seasonal influenza in the EU/EEA countries, 2014-2015. Stockholm: ECDC; Jan 2015. Available from:
    1. Chong Y, Ikematsu H. Effect of seasonal vaccination on the selection of influenza A/H3N2 epidemic variants. Vaccine. 2017;35(2):255-63. 10.1016/j.vaccine.2016.11.084
    1. 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. 10.1016/j.jcv.2017.06.007
    1. 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. 10.1093/aje/kwr037
    1. 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. 10.1093/aje/kwj317
    1. 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.
    1. 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. 10.1097/EDE.0000000000000571
    1. 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. 10.1016/S2213-2600(14)70034-7
    1. 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. 10.1017/S0950268812002506
    1. 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. 10.1016/S0140-6736(10)60206-1
    1. 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.
    1. Larrauri Cámara A, Jiménez-Jorge S, Mateo Ontañón S, Pozo Sánchez F, Ledesma Moreno J, Casas Flecha I, Spanish Influenza Surveillance System (SISS) Epidemiology of the 2009 influenza pandemic in Spain. Enferm Infecc Microbiol Clin. 2012;30(Suppl 4):2-9. 10.1016/S0213-005X(12)70098-8
    1. Larrauri A, de Mateo S, Spanish 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. 10.2807/esm.12.05.00706-en
    1. 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:
    1. 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:
    1. 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:
    1. 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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