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Phylogeography of swine influenza H3N2 in the United States: translational public health for zoonotic disease surveillance.

ABSTRACT: The field of phylogeography has received a lot of attention for its application to molecular evolution and geographic migration of species. More recent work has included infectious diseases especially zoonotic RNA viruses like influenza and rabies. Phylogeography of viruses has the potential to advance surveillance at agencies such as public health departments, agriculture departments, and wildlife agencies. However, little is known about how these agencies could use phylogeography for applied surveillance and the integration of animal and human sequence data. Here, we highlight its potential to support 'translational public health' that could bring sequence data to the forefront of surveillance. We focus on swine influenza H3N2 because of the recent link to a variant form that has also infected humans. We discuss the implications to applied surveillance and the need for an integrated biomedical informatics approach for adoption at agencies of animal and public health.

SUBMITTER: Scotch M

PROVIDER: S-EPMC3537880 | biostudies-literature | 2013 Jan

REPOSITORIES: biostudies-literature

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Publications

Phylogeography of swine influenza H3N2 in the United States: translational public health for zoonotic disease surveillance.

Scotch Matthew M Mei Changjiang C

Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases 20121106

The field of phylogeography has received a lot of attention for its application to molecular evolution and geographic migration of species. More recent work has included infectious diseases especially zoonotic RNA viruses like influenza and rabies. Phylogeography of viruses has the potential to advance surveillance at agencies such as public health departments, agriculture departments, and wildlife agencies. However, little is known about how these agencies could use phylogeography for applied s ...[more]

PMID: 23137647

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Project description:During 1998, severe outbreaks of influenza were observed in four swine herds in the United States. This event was unique because the causative agents, H3N2 influenza viruses, are infrequently isolated from swine in North America. Two antigenically distinct reassortant viruses (H3N2) were isolated from infected animals: a double-reassortant virus containing genes similar to those of human and swine viruses, and a triple-reassortant virus containing genes similar to those of human, swine, and avian influenza viruses (N. N. Zhou, D. A. Senne, J. S. Landgraf, S. L. Swenson, G. Erickson, K. Rossow, L. Liu, K.-J. Yoon, S. Krauss, and R. G. Webster, J. Virol. 73:8851-8856, 1999). Because the U.S. pig population was essentially naive in regard to H3N2 viruses, it was important to determine the extent of viral spread. Hemagglutination inhibition (HI) assays of 4, 382 serum samples from swine in 23 states indicated that 28.3% of these animals had been exposed to classical swine-like H1N1 viruses and 20.5% had been exposed to the triple-reassortant-like H3N2 viruses. The HI data suggested that viruses antigenically related to the double-reassortant H3N2 virus have not become widespread in the U.S. swine population. The seroreactivity levels in swine serum samples and the nucleotide sequences of six additional 1999 isolates, all of which were of the triple-reassortant genotype, suggested that H3N2 viruses containing avian PA and PB2 genes had spread throughout much of the country. These avian-like genes cluster with genes from North American avian viruses. The worldwide predominance of swine viruses containing an avian-like internal gene component suggests that these genes may confer a selective advantage in pigs. Analysis of the 1999 swine H3N2 isolates showed that the internal gene complex of the triple-reassortant viruses was associated with three recent phylogenetically distinct human-like hemagglutinin (HA) molecules. Acquisition of HA genes from the human virus reservoir will significantly affect the efficacy of the current swine H3N2 vaccines. This finding supports continued surveillance of U.S. swine populations for influenza virus activity.

Project description:Influenza pandemics are associated with severe morbidity, mortality, and social and economic disruption. Every summer in the United States, youths attending agricultural fairs are exposed to genetically diverse influenza A viruses (IAVs) circulating in exhibition swine, resulting in over 450 lab-confirmed zoonotic infections since 2010. Exhibition swine represent a small, defined population (∼1.5% of the U.S. herd), presenting a realistic opportunity to mitigate a pandemic threat by reducing IAV transmission in the animals themselves. Through intensive surveillance and genetic sequencing of IAVs in exhibition swine in six U.S. states in 2018 (n = 212), we characterized how a heterogeneous circuit of swine shows, comprising fairs with different sizes and geographic coverage, facilitates IAV transmission among exhibition swine and into humans. Specifically, we identified the role of an early-season national show in the propagation and spatial dissemination of a specific virus (H1δ-2) that becomes dominant among exhibition swine and is associated with the majority of zoonotic infections in 2018. These findings suggest that a highly targeted mitigation strategy, such as postponing swine shows for 1 to 2 weeks following the early-season national show, could potentially reduce IAV transmission in exhibition swine and spillover into humans, and this merits further study.IMPORTANCE The varying influenza A virus (IAV) exposure and infection status of individual swine facilitates introduction, transmission, and dissemination of diverse IAVs. Since agricultural fairs bring people into intimate contact with swine, they provide a unique interface for zoonotic transmission of IAV. Understanding the dynamics of IAV transmission through exhibition swine is critical to mitigating the high incidence of variant IAV cases reported in association with agricultural fairs. We used genomic sequences from our exhibition swine surveillance to characterize the hemagglutinin and full genotypic diversity of IAV at early-season shows and the subsequent dissemination through later-season agricultural fairs. We were able to identify a critical time point with important implications for downstream IAV and zoonotic transmission. With improved understanding of evolutionary origins of zoonotic IAV, we can inform public health mitigation strategies to ultimately reduce zoonotic IAV transmission and risk of pandemic IAV emergence.

Dataset Information

Phylogeography of swine influenza H3N2 in the United States: translational public health for zoonotic disease surveillance.

Publications

Phylogeography of swine influenza H3N2 in the United States: translational public health for zoonotic disease surveillance.

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