Inferring epidemiologic dynamics from viral evolution: 2014–2015 Eurasian/North American highly pathogenic avian influenza viruses exceed transmission threshold, R₀ = 1, in wild birds and poultry in North America

Abstract

Highly pathogenic avian influenza virus (HPAIV) is a multihost pathogen with lineages that pose health risks for domestic birds, wild birds, and humans. One mechanism of intercontinental HPAIV spread is through wild bird reservoirs, and wild birds were the likely sources of a Eurasian (EA) lineage HPAIV into North America in 2014. The introduction resulted in several reassortment events with North American (NA) lineage low‐pathogenic avian influenza viruses and the reassortant EA/NA H5N2 went on to cause one of the largest HPAIV poultry outbreaks in North America. We evaluated three hypotheses about novel HPAIV introduced into wild and domestic bird hosts: (i) transmission of novel HPAIVs in wild birds was restricted by mechanisms associated with highly pathogenic phenotypes; (ii) the HPAIV poultry outbreak was not self‐sustaining and required viral input from wild birds; and (iii) reassortment of the EA H5N8 generated reassortant EA/NA AIVs with a fitness advantage over fully Eurasian lineages in North American wild birds. We used a time‐rooted phylodynamic model that explicitly incorporated viral population dynamics with evolutionary dynamics to estimate the basic reproductive number (R 0) and viral migration among host types in domestic and wild birds, as well as between the EA H5N8 and EA/NA H5N2 in wild birds. We did not find evidence to support hypothesis (i) or (ii) as our estimates of the transmission parameters suggested that the HPAIV outbreak met or exceeded the threshold for persistence in wild birds (R 0 > 1) and poultry (R 0 ≈ 1) with minimal estimated transmission among host types. There was also no evidence to support hypothesis (iii) because R 0 values were similar among EA H5N8 and EA/NA H5N2 in wild birds. Our results suggest that this novel HPAIV and reassortments did not encounter any transmission barriers sufficient to prevent persistence when introduced to wild or domestic birds.

Agricultural and geographic factors shaped the North American 2015 highly pathogenic avian influenza H5N2 outbreak

“…Additionally, other variables that represent potential migratory stopover habitats, such as Important Bird Areas and agricultural land, were not supported within the model, suggesting that if wild birds contributed to HPAI dispersal within the Midwest, their role was limited. This further supports previous studies, which indicated that the Midwestern portion of the outbreak was driven by inter-farm transmission (11,12,14). Several mechanisms have been proposed to explain HPAI transmission between farms during the 2015 outbreak, including equipment sharing, personnel overlap, and aerosolization.…”

“…Despite frequent reports of wild birds on the grounds and within barns of HPAI-positive turkey premises (10), a case-control study found no significant difference in exposure to wild birds between positive turkey premises and matched controls (11). Similarly, one phylodynamic analysis found no evidence of continued HPAI introductions into the Midwestern poultry industries (12), but other models have suggested multiple introductions (13,14). Geographic and environmental variables, such as human population, agricultural, climatological, and ecological measures, may help explain farm-to-farm transmission observed within the poultry industries.…”

“…For example, proximity between midwestern poultry premises has been implicated as an important risk factor for HPAI infection (11,13). Although it has been suggested that poultry production type did not affect outbreak transmission (12), this has not been formally tested. Despite extensive molecular epidemiological studies, such environmental and ecological covariates of viral spread during this outbreak have not been investigated.…”

The Expectations and Challenges of Wildlife Disease Research in the Era of Genomics: Forecasting with a Horizon Scan-like Exercise

“…In North America, genetic studies of puma (Puma concolor) and bobcat (Lynx rufus) populations indicate altered patterns of viral disease transmission and animal health in response to anthropogenic changes (Lee et al 2012;Ernest et al 2014;Carver et al 2016;Fountain-Jones et al 2017). Moreover, projects that integrate NGS tools can provide detailed information on the transmission of transcontinental diseases such as the spread of rabies in North America and in East Africa (Brunker et al 2015;Trewby et al 2017), and diseases circulating between wild and domesticated livestock on local and global scales (Nomikou et al 2015;Kamath et al 2016;Trewby et al 2016;Dippenaar et al 2017;Grear et al 2018).…”

Evolutionary perspectives on human infectious diseases: Challenges, advances, and promises

“…Complementing the work by Joseph et al., ; Grear, Hall, Dusek, and Ip () investigated mechanisms of intercontinental highly pathogenic avian influenza virus (HPAIV) spread through wild bird reservoirs possibly related to the North America outbreak in 2014. This introduction resulted in several reassortment events with North American (NA) lineage low‐pathogenic avian influenza viruses and the reassortant EA/NA H5N2 that went on to cause one of the largest HPAIV poultry outbreaks in North America.…”