Abstract

Environmental persistence of zoonotic pathogens is a key trait that influences the probability of zoonotic spillover. Pathogen survival outside of the host determines the window available for contact with the new recipient host species and the dose of pathogen available to that host. The longer a pathogen survives in the environment, the more disconnected the reservoir and recipient hosts can be in space and time, and the more likely that an infective dose will be available to recipient hosts. Therefore, environmental persistence is a key parameter for mechanistic models needed to predict pathogen spillover. Avian influenza can be transmitted from wildlife to poultry and people in part due to its ability to persist in the environment. Considerable work has been done to quantify trends in avian influenza persistence across environmental conditions, often published in separate studies with separate datasets. In this paper, we quantify the trends and variability of avian influenza viral persistence across environmental conditions by collating disjoint experimental data on viral particle persistence in water across many studies and a range of environmental conditions. The collated data represent 120 estimates from three different studies of the decay rates of highly pathogenic avian influenza H5N1 (90 estimates from Asia and 30 from Europe) in response to temperature, pH, and salinity. We analyzed these data with a Bayesian model to control for biases with random effects and used experimental replicates and R2 estimates of the publication’s regression procedures as statistical weights. We found temperature significantly decreases persistence of H5N1 virus in water, and this effect is stronger than that of salinity alone. Salinity interacts with temperature and probably drives the most contrasting persistence scenarios between cold-saline and warm-saline water bodies, where highest and lowest persistence times could occur respectively. Our work provides needed parameters for models that examine the risk of spillover of avian influenza viruses.

Highlights

  • The capacity of microorganisms to survive in the environment has fundamental consequences for their ecology, epidemiology, and ability to transmit between individuals and species (Ewald, 1987; Kuris et al, 2014; Plowright et al, 2017)

  • We provide estimates of the joint effect of salinity and temperature on the rates of decay of several strains of influenza H5N1, showing a stronger effect of temperature on environmental viability compared to salinity

  • The estimated rates of decay identified here are consistent with estimates for other influenza subtypes in response to salinity and temperature (Stallknecht et al, 1990a; Brown et al, 2007) and with those of low pathogenicity AIV (Dalziel et al, 2016)

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Summary

Introduction

The capacity of microorganisms to survive in the environment has fundamental consequences for their ecology, epidemiology, and ability to transmit between individuals and species (Ewald, 1987; Kuris et al, 2014; Plowright et al, 2017). Swine and other mammal models, influenza viruses replicate in the upper or lower respiratory tract, owing to the presence of the necessary sialic acid receptors, favoring airborne transmission (Kuiken et al, 2006; Taubenberger and Kash, 2010; Lipsitch et al, 2016). For this reason, studies of the environmental persistence of influenza viruses pathogenic to humans tend to focus on airborne transmission (Weber and Stilianakis, 2008; Shaman and Kohn, 2009). The environmental factors that are more relevant for AIV spillover and consequent adaptation to poultry, swine and humans are more likely to be those affecting waterborne survival

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