Spatial Transmission of 2009 Pandemic Influenza in the US

Abstract

The 2009 H1N1 influenza pandemic provides a unique opportunity for detailed examination of the spatial dynamics of an emerging pathogen. In the US, the pandemic was characterized by substantial geographical heterogeneity: the 2009 spring wave was limited mainly to northeastern cities while the larger fall wave affected the whole country. Here we use finely resolved spatial and temporal influenza disease data based on electronic medical claims to explore the spread of the fall pandemic wave across 271 US cities and associated suburban areas. We document a clear spatial pattern in the timing of onset of the fall wave, starting in southeastern cities and spreading outwards over a period of three months. We use mechanistic models to tease apart the external factors associated with the timing of the fall wave arrival: differential seeding events linked to demographic factors, school opening dates, absolute humidity, prior immunity from the spring wave, spatial diffusion, and their interactions. Although the onset of the fall wave was correlated with school openings as previously reported, models including spatial spread alone resulted in better fit. The best model had a combination of the two. Absolute humidity or prior exposure during the spring wave did not improve the fit and population size only played a weak role. In conclusion, the protracted spread of pandemic influenza in fall 2009 in the US was dominated by short-distance spatial spread partially catalysed by school openings rather than long-distance transmission events. This is in contrast to the rapid hierarchical transmission patterns previously described for seasonal influenza. The findings underline the critical role that school-age children play in facilitating the geographic spread of pandemic influenza and highlight the need for further information on the movement and mixing patterns of this age group.

Author Summary

The determinants of influenza spatial spread are not fully understood, in part due to the insufficient geographic resolution of incidence data. We address this using a fine-grained private sector electronic health database of insurance claims data from health encounters in the US during 2009. We used physician diagnoses codes to generate a dataset of the weekly number of office visits with diagnosed influenza-like illness for 271 US locations. Applying statistical and mathematical models to these disease data, we find that the main autumn wave of the 2009 pandemic in the US was remarkably spatially structured. Its onset in the South Eastern US precipitated a slow radial spread that took 3 months to diffuse across the country. These patterns were replicated by models that included short-distance spatial transmission between nearby locations and increased transmission rates when school was in session. Our results contrast with previous modelling studies that indicated that environmental factors, population sizes, and long-distance transmission events (air traffic) are major determinants in disease spread. We conclude that the 2009 pandemic autumn wave spread slowly because transmissibility of the influenza virus was relatively low and children (who travel long distance far less than adults) were the predominant sources of infection.