Contact, travel, and transmission: The impact of winter holidays on influenza dynamics in the United States

Background The seasonality of influenza is thought to vary according to environmental factors and human behavior. During winter holidays, potential disease-causing contact and travel deviate from typical patterns. We aim to understand these changes on age-specific and spatial influenza transmission. Methods We characterized the changes to transmission and epidemic trajectories among children and adults in a spatial context before, during, and after the winter holidays among aggregated physician medical claims in the United States from 2001 to 2009 and among synthetic data simulated from a deterministic, age-specific spatial metapopulation model. Results Winter holidays reduced influenza transmission and delayed the trajectory of influenza season epidemics. The holiday period was marked by a shift in the relative risk of disease from children toward adults. Model results indicated that holidays delayed epidemic peaks and synchronized incidence across locations, and that contact reductions from school closures, rather than age-specific mixing and travel, produced these observed holiday influenza dynamics. Conclusions Winter holidays delay seasonal influenza epidemic peaks and shift disease risk toward adults because of changes in contact patterns. These findings may inform targeted influenza information and vaccination campaigns during holiday periods.

[1]  C. Fraser,et al.  A New Framework and Software to Estimate Time-Varying Reproduction Numbers During Epidemics , 2013, American journal of epidemiology.

[2]  C. Bauch,et al.  Nine challenges in incorporating the dynamics of behaviour in infectious diseases models. , 2015, Epidemics.

[3]  Jeffrey Shaman,et al.  Absolute humidity modulates influenza survival, transmission, and seasonality , 2009, Proceedings of the National Academy of Sciences.

[4]  G. Glass,et al.  Assessing the impact of airline travel on the geographic spread of pandemic influenza , 2003 .

[5]  N. Ferguson,et al.  Closure of schools during an influenza pandemic , 2009, The Lancet Infectious Diseases.

[6]  John Steel,et al.  Influenza Virus Transmission Is Dependent on Relative Humidity and Temperature , 2007, PLoS pathogens.

[7]  M. Jehn,et al.  Effect of School Closure on the Incidence of Influenza among School-Age Children in Arizona , 2010, Public health reports.

[8]  A. Arab,et al.  Characterizing Influenza surveillance systems performance: application of a Bayesian hierarchical statistical model to Hong Kong surveillance data , 2014, BMC Public Health.

[9]  B. Cowling,et al.  Estimation of the Serial Interval of Influenza , 2009, Epidemiology.

[10]  Shweta Bansal,et al.  Detecting signals of seasonal influenza severity through age dynamics , 2015, bioRxiv.

[11]  R. Mikolajczyk,et al.  Social Contacts and Mixing Patterns Relevant to the Spread of Infectious Diseases , 2008, PLoS medicine.

[12]  Laura C Rosella,et al.  The social determinants of health and pandemic H1N1 2009 influenza severity. , 2012, American journal of public health.

[13]  Shweta Bansal,et al.  The Shifting Demographic Landscape of Pandemic Influenza , 2010, PloS one.

[14]  J. Pearl.  Causal inference in statistics: An overview , 2009 .

[15]  L. A. Rvachev,et al.  A mathematical model for the global spread of influenza , 1985 .

[16]  Andrea Stember.  Influenza-Like Illness, The Time to Seek Healthcare, and Influenza Antiviral Receipt during the 2010-2011 Influenza Season—United States , 2014 .

[17]  Mark A. Miller,et al.  Seasonal influenza in the United States, France, and Australia: transmission and prospects for control , 2007, Epidemiology and Infection.

[18]  N. Ferguson,et al.  Will travel restrictions control the international spread of pandemic influenza? , 2006, Nature Medicine.

[19]  V. Colizza,et al.  Metapopulation epidemic models with heterogeneous mixing and travel behaviour , 2014, Theoretical Biology and Medical Modelling.

[20]  L. Balluz,et al.  Self-reported influenza-like illness and receipt of influenza antiviral drugs during the 2009 pandemic, United States, 2009-2010. , 2012, American journal of public health.

[21]  Trevor Bedford,et al.  Global circulation patterns of seasonal influenza viruses vary with antigenic drift , 2015, Nature.

[22]  John S. Brownstein,et al.  Age-related trends in the timeliness and prediction of medical visits, hospitalizations and deaths due to pneumonia and influenza, British Columbia, Canada, 1998-2004. , 2008, Vaccine.

[23]  M. Suchard,et al.  Unifying Viral Genetics and Human Transportation Data to Predict the Global Transmission Dynamics of Human Influenza H3N2 , 2014, PLoS pathogens.

[24]  B. Sommers,et al.  Health reform and changes in health insurance coverage in 2014. , 2014, The New England journal of medicine.

[25]  Mark A. Miller,et al.  Synchrony, Waves, and Spatial Hierarchies in the Spread of Influenza , 2006, Science.

[26]  E. Lyons,et al.  Pandemic Potential of a Strain of Influenza A (H1N1): Early Findings , 2009, Science.

[27]  C. Jackson,et al.  School closures and influenza: systematic review of epidemiological studies , 2013, BMJ Open.

[28]  L. Danon,et al.  Individual identity and movement networks for disease metapopulations , 2010, Proceedings of the National Academy of Sciences.

[29]  Niel Hens,et al.  Different transmission patterns in the early stages of the influenza A(H1N1)v pandemic: a comparative analysis of 12 European countries. , 2011, Epidemics.

[30]  Robyn Tamblyn,et al.  Accuracy of physician billing claims for identifying acute respiratory infections in primary care. , 2008, Health services research.

[31]  Ellen Brooks-Pollock,et al.  Measured Dynamic Social Contact Patterns Explain the Spread of H1N1v Influenza , 2012, PLoS Comput. Biol..

[32]  E. Lofgren,et al.  Influenza Seasonality: Underlying Causes and Modeling Theories , 2006, Journal of Virology.

[33]  W. Edmunds,et al.  Delaying the International Spread of Pandemic Influenza , 2006, PLoS medicine.

[34]  G. Rubin,et al.  Health Protection Agency, , 2011 .

[35]  V. Colizza,et al.  Age-specific contacts and travel patterns in the spatial spread of 2009 H1N1 influenza pandemic , 2013, BMC Infectious Diseases.

[36]  S Michie,et al.  The impact of communications about swine flu (influenza A H1N1v) on public responses to the outbreak: results from 36 national telephone surveys in the UK. , 2010, Health technology assessment.

[37]  Alessandro Vespignani,et al.  The role of the airline transportation network in the prediction and predictability of global epidemics , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[38]  L. Simonsen,et al.  Pandemic versus epidemic influenza mortality: a pattern of changing age distribution. , 1998, The Journal of infectious diseases.

[39]  Keiji Fukuda,et al.  Mortality associated with influenza and respiratory syncytial virus in the United States. , 2003, JAMA.

[40]  J. Dushoff,et al.  Effects of School Closure on Incidence of Pandemic Influenza in Alberta, Canada , 2012 .

[41]  Punam Mangtani,et al.  The Effects of School Closures on Influenza Outbreaks and Pandemics: Systematic Review of Simulation Studies , 2014, PloS one.

[42]  J. Rainey,et al.  Comparing Observed with Predicted Weekly Influenza-Like Illness Rates during the Winter Holiday Break, United States, 2004-2013 , 2015, PloS one.

[43]  Bard Ermentrout,et al.  Local Variations in Spatial Synchrony of Influenza Epidemics , 2012, PloS one.

[44]  J. H. Ellis,et al.  Erratum: Assessing the Impact of Airline Travel on the Geographic Spread of Pandemic Influenza , 2004, European Journal of Epidemiology.

[45]  M. Meltzer,et al.  Effect of Winter School Breaks on Influenza-like Illness, Argentina, 2005–2008 , 2013, Emerging infectious diseases.

[46]  Benjamin J. Cowling,et al.  The Contribution of Social Behaviour to the Transmission of Influenza A in a Human Population , 2014, PLoS pathogens.

[47]  Alessandro Vespignani,et al.  Multiscale mobility networks and the spatial spreading of infectious diseases , 2009, Proceedings of the National Academy of Sciences.

[48]  L. Balluz,et al.  Impact of medical and behavioural factors on influenza-like illness, healthcare-seeking, and antiviral treatment during the 2009 H1N1 pandemic: USA, 2009–2010 , 2013, Epidemiology and Infection.

[49]  M. Kretzschmar,et al.  Using data on social contacts to estimate age-specific transmission parameters for respiratory-spread infectious agents. , 2006, American journal of epidemiology.

[50]  Alessandro Vespignani,et al.  Modeling the Worldwide Spread of Pandemic Influenza: Baseline Case and Containment Interventions , 2007, PLoS medicine.

[51]  W. H. Frost.  Statistics of Influenza Morbidity: With Special Reference to Certain Factors in Case Incidence and Case Fatality , 1920 .

[52]  E. Hook,et al.  Health Insurance Coverage, Health Care-Seeking Behaviors, and Genital Chlamydial Infection Prevalence in Sexually Active Young Adults , 2006, Sexually transmitted diseases.

[53]  Cécile Viboud,et al.  Demonstrating the Use of High-Volume Electronic Medical Claims Data to Monitor Local and Regional Influenza Activity in the US , 2014, PloS one.

[54]  Sutirth Dey,et al.  Stability via Asynchrony in Drosophila Metapopulations with Low Migration Rates , 2006, Science.

[55]  J. Swann,et al.  The impact of mass gatherings and holiday traveling on the course of an influenza pandemic: a computational model , 2010, BMC public health.

[56]  Cécile Viboud,et al.  Absolute Humidity and the Seasonal Onset of Influenza in the Continental United States , 2010, PLoS biology.

[57]  E. Lau,et al.  Effects of School Closures, 2008 Winter Influenza Season, Hong Kong , 2008, Emerging infectious diseases.

[58]  J. Brownstein,et al.  Empirical Evidence for the Effect of Airline Travel on Inter-Regional Influenza Spread in the United States , 2006, PLoS medicine.

[59]  Henrik Eriksson,et al.  Age as a Determinant for Dissemination of Seasonal and Pandemic Influenza: An Open Cohort Study of Influenza Outbreaks in Östergötland County, Sweden , 2012, PloS one.

[60]  J. Robins,et al.  Transmissibility of 1918 pandemic influenza , 2004, Nature.

[61]  Louise Pelletier,et al.  Age-specific Differences in Influenza A Epidemic Curves: Do Children Drive the Spread of Influenza Epidemics? , 2011, American journal of epidemiology.

[62]  A. Flahault,et al.  Estimating the impact of school closure on influenza transmission from Sentinel data , 2008, Nature.

[63]  I M Longini,et al.  Estimating household and community transmission parameters for influenza. , 1982, American journal of epidemiology.

[64]  N. Ferguson,et al.  Role of social networks in shaping disease transmission during a community outbreak of 2009 H1N1 pandemic influenza , 2011, Proceedings of the National Academy of Sciences.

[65]  K. Eames.  The influence of school holiday timing on epidemic impact , 2013, Epidemiology and Infection.

[66]  K. Viswanath,et al.  Associations between health communication behaviors, neighborhood social capital, vaccine knowledge, and parents' H1N1 vaccination of their children. , 2013, Vaccine.

[67]  A. Kucharski,et al.  School’s Out: Seasonal Variation in the Movement Patterns of School Children , 2015, PloS one.

[68]  Ken T D Eames,et al.  The impact of school holidays on the social mixing patterns of school children. , 2011, Epidemics.

[69]  Cécile Viboud,et al.  Risk factors of influenza transmission in households. , 2004, The British journal of general practice : the journal of the Royal College of General Practitioners.

[70]  T. Buchmueller,et al.  The Affordable Care Act has led to significant gains in health insurance and access to care for young adults. , 2013, Health affairs.