Population dynamics of cocirculating swine influenza A viruses in the United States from 2009 to 2012

Abstract

Background: Understanding the ecology and evolution of influenza A viruses (IAV) in mammalian hosts is critical to reduce disease burden in production animals and lower zoonotic infection risk in humans. Recent advances in influenza surveillance in US swine populations allow for timely epidemiological, phylogenetic, and virological analyses that monitor emergence of novel viruses and assess changes in viral population dynamics.

Methods: To better understand IAV in the North American swine population, we undertook a phylogenetic analysis of 1075 HA, 1049 NA, and 1040 M sequences of IAV isolated from US swine during 2009-2012 through voluntary and anonymous submissions to the US Department of Agriculture IAV swine surveillance system.

Results: Analyses revealed changes in population dynamics among multiple clades of A/H1N1, A/H3N2, and A/H1N2 cocirculating in US swine populations during 2009-2012. Viral isolates were categorized into one of seven genetically and antigenically distinct hemagglutinin lineages: H1α, H1β, H1γ, H1δ1, H1δ2, H1pdm09, and H3 cluster IV. There was an increase in occurrence of H1δ1 in samples submitted, with a concurrent decrease in H1pdm09. H3 cluster IV exhibited increasing diversification, warranting a re-evaluation of phylogenetic nomenclature criteria. Although H3N2 represented 25% of identified viruses, this subtype was reported in increasing proportion of sequenced isolates since late 2011.

Conclusions: Surveillance and reporting of IAV in US swine have increased since 2009, and we demonstrate a period of expanded viral diversity. These data may be used to inform intervention strategies of vaccine and diagnostic updates and changes in swine health management.

Keywords: Epidemiology; influenza A virus; surveillance; swine; vaccines; zoonotic diseases.

Figure 1

Sequenced swine influenza A viruses in United States. submitted to the anonymous and voluntary USDA surveillance system through the NAHLN laboratories from 2009 to 2012. (A) Swine influenza A subtypes (H1N1, H1N2, H3N2, and mixed) identified by year; and (B) participating US states and number of isolates submitted, and hog population (in 1000s). The surveillance system was initiated in the fourth quarter of 2009; consequently, the 2009 data represent the final 3 months of 2009.

Figure 2

Phylogenetic relationships of hemagglutinin (HA) sequences collected in the United States from 2009 to 2012 of: (A) 804 H1N1 and H1N2 influenza A virus isolates; and (B) 279 H3N2 influenza A virus isolates. H1 and H3 HA sublineages are indicated by colored legends (H1: H1α, H1β, H1γ, H1δ1, H1δ2, H1pdm09; H3: cluster I, II, II, and IV). The tree is midpoint rooted for clarity; scale bar indicates nucleotide substitutions per site. The phylogenies with tip labels included are in Figure S5.

Figure 3

Frequency of the triple‐reassortment matrix (North American) versus pandemic matrix (Pandemic) genome segments by yearly quarter from 2009 to 2012 (A), and by subtype and/or antigenic phylogenetic cluster (B).

Figure 4

Monthly sequenced swine influenza A isolates submitted into the USDA surveillance system through the NAHLN laboratories from 2010 to 2012 for (A) A/H1N1; (B) A/H1N2; and (C) H3N2.

Figure 5

Seasonal time series decomposition by Loess (STL) of H1N1 isolates by month in the USDA swine IAV surveillance system from 2010 to 2012. Data: monthly abundance of H1N1 isolates submitted to the USDA surveillance system through the NAHLN laboratories; seasonal: seasonal component of the time series; trend: fitted long‐term trend; remainder: residual component. The three components (seasonal, trend, remainder) sum to the time series raw data. The panel scales are not identical: the vertical bar at right of each panel indicates relative variation in scaling.