The Role of Environmental Transmission in Recurrent Avian Influenza Epidemics

Abstract

Avian influenza virus (AIV) persists in North American wild waterfowl, exhibiting major outbreaks every 2–4 years. Attempts to explain the patterns of periodicity and persistence using simple direct transmission models are unsuccessful. Motivated by empirical evidence, we examine the contribution of an overlooked AIV transmission mode: environmental transmission. It is known that infectious birds shed large concentrations of virions in the environment, where virions may persist for a long time. We thus propose that, in addition to direct fecal/oral transmission, birds may become infected by ingesting virions that have long persisted in the environment. We design a new host–pathogen model that combines within-season transmission dynamics, between-season migration and reproduction, and environmental variation. Analysis of the model yields three major results. First, environmental transmission provides a persistence mechanism within small communities where epidemics cannot be sustained by direct transmission only (i.e., communities smaller than the critical community size). Second, environmental transmission offers a parsimonious explanation of the 2–4 year periodicity of avian influenza epidemics. Third, very low levels of environmental transmission (i.e., few cases per year) are sufficient for avian influenza to persist in populations where it would otherwise vanish. Avian influenza viruses (AIVs) in wild waterfowl constitute the historic source of human influenza viruses, having a rich pool of genetic and antigenic diversity that often leads to cross-species transmission. Although the emergence of H5N1 avian influenza virus onto the international scene has captured the most attention, we do not as yet understand the mechanisms that underpin AIV persistence and dynamics in the wild. We developed a novel host–pathogen model intended to describe the epidemiology of low pathogenic AIV in temperate environments. Our model takes into account seasonality in migration and breeding together with multiple modes of transmission. AIVs have been detected in unconcentrated lake water, soil swabs, and mud samples. Laboratory experiments show that AIVs persist and remain infectious in water for extended periods. However, so far, the possibility of environmental transmission of AIV has been largely overlooked. Our work shows that environmental transmission provides a parsimonious explanation for the patterns of persistence and outbreaks of AIV documented in the literature. In addition to their scientific importance, our conclusions impact the design of control policies for avian influenza by emphasizing the dramatic and long-term role that environmental persistence of pathogens may play at the epidemic level.