Cocirculation of avian H9N2 and contemporary "human" H3N2 influenza A viruses in pigs in southeastern China: potential for genetic reassortment?

Abstract

Pigs are permissive to both human and avian influenza viruses and have been proposed to be an intermediate host for the genesis of pandemic influenza viruses through reassortment or adaptation of avian viruses. Prospective virological surveillance carried out between March 1998 and June 2000 in Hong Kong, Special Administrative Region, People's Republic of China, on pigs imported from southeastern China, provides the first evidence of interspecies transmission of avian H9N2 viruses to pigs and documents their cocirculation with contemporary human H3N2 (A/Sydney/5/97-like, Sydney97-like) viruses. All gene segments of the porcine H9N2 viruses were closely related to viruses similar to chicken/Beijing/1/94 (H9N2), duck/Hong Kong/Y280/97 (H9N2), and the descendants of the latter virus lineage. Phylogenetic analysis suggested that repeated interspecies transmission events had occurred from the avian host to pigs. The Sydney97-like (H3N2) viruses isolated from pigs were related closely to contemporary human H3N2 viruses in all gene segments and had not undergone genetic reassortment. Cocirculation of avian H9N2 and human H3N2 viruses in pigs provides an opportunity for genetic reassortment leading to the emergence of viruses with pandemic potential.

FIG. 1

Phylogenetic tree for the H9 HA1 gene of influenza A viruses. The nucleotide sequences of the HA1 gene (960 bp from position 55 to 1014) were analyzed with the Phylogenetic Analysis Using Parsimony program using a maximum-parsimony algorithm. The HA1 phylogenetic tree is rooted to A/Dk/Alberta/60/76 (H12N5). The lengths of the horizontal lines are proportional to the minimum number of nucleotide differences required to join nodes. Vertical lines are for spacing branches and labels. The bootstrap value (∗) for 1,000 replications was computed using MEGA software (version 1.0; Pennsylvania State University, University Park), and the results for key branches in the tree are depicted. Abbreviations used in virus designations not used in the text are as follows: Gs, goose; Pg, pigeon; Ph, pheasant; SCk, silkie chicken; Ty, turkey; Kor, Korea; CA, California; WI, Wisconsin; AR, Arkansas; MN, Minnesota. Viruses isolated in this study are underlined. Group I, Qa/HK/G1/97 (H9N2) lineage; group II, Dk/HK/Y280//97 (H9N2) lineage; group III, Ck/Kor/006/96 (H9N2) lineage.

FIG. 2

Phylogenetic tree of the partial H3 HA1 gene (778 bp from position 33 to 810) of influenza A viruses. The method used and abbreviations are as given in the legend to Fig. 1. Viruses isolated in this study are underlined. The tree is rooted at Dk/Czechoslovakia/56 (H4N6).

FIG. 3

Phylogenetic trees for the M gene (residues 41 to 671) of swine influenza viruses from southeastern China. The method used and abbreviations are as given in the legend to Fig. 1. Viruses isolated in this study are underlined. The tree is rooted at A/Equine/Prague/1/56 (H7N7). Abbreviations used in virus designations not used in the text are as follows: Ger, Germany; IA, Iowa; KY, Kentucky; Neth, The Netherlands.