Unseasonal transmission of H3N2 influenza A virus during the swine-origin H1N1 pandemic

Abstract

The initial wave of swine-origin influenza A virus (pandemic H1N1/09) in the United States during the spring and summer of 2009 also resulted in an increased vigilance and sampling of seasonal influenza viruses (H1N1 and H3N2), even though they are normally characterized by very low incidence outside of the winter months. To explore the nature of virus evolution during this influenza "off-season," we conducted a phylogenetic analysis of H1N1 and H3N2 sequences sampled during April to June 2009 in New York State. Our analysis revealed that multiple lineages of both viruses were introduced and cocirculated during this time, as is typical of influenza virus during the winter. Strikingly, however, we also found strong evidence for the presence of a large transmission chain of H3N2 viruses centered on the south-east of New York State and which continued until at least 1 June 2009. These results suggest that the unseasonal transmission of influenza A viruses may be more widespread than is usually supposed.

FIG. 1.

ML tree (unrooted) of 652 HA1 sequences of seasonal H1N1 virus sampled globally during the period from 2008 to 2009. The seven viruses sampled from New York State during the period 27 April to 26 May are shaded red, with each likely introduction event marked by a square. A possible transmission cluster is denoted with an asterisk; the bootstrap value for this node is also shown.

FIG. 2.

(a) ML tree (unrooted) of 1,258 HA1 sequences of seasonal H3N2 sampled globally during the period from 2008 to 2009. The 41 viruses sampled from New York State during the period 27 April to 1 June are shaded red, with each likely introduction event marked by a square. Possible transmission clusters are noted by asterisks, and their associated bootstrap values are also shown. Although a bootstrap value <70% is observed for the main transmission cluster, this group of sequences is strongly supported (0.84) under the approximate likelihood ratio test available in PHYML. (b) Counties of New York State from where the putative H3N2 transmission cluster was sampled (shaded circles). (c) Magnification of the 21-sequence cluster that provides strong evidence for the unseasonal transmission of H3N2.