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This report describes the detection of a triple reassortant swine influenza A virus of H1 av N2 subtype. It evolved from an avian-like swine H1 av N1 that first acquired the N2 segment from a seasonal H3N2, then the M segment from a 2009 pandemic H1N1, in two reassortments estimated to have occurred 10 years apart. This study illustrates how recurrent influenza infections increase the co-infection risk and facilitate evolutionary jumps by successive gene exchanges. It recalls the importance of appropriate biosecurity measures inside holdings to limit virus persistence and interspecies transmissions, which both contribute to the emergence of new potentially zoonotic viruses.

We have previously shown a clear differential genetic evolution of the hemagglutinin (HA) of human AH1N1 and AH1N2 viruses, isolated in southern France between 2001 and 2004. However, our analysis revealed that one single AH1N2 isolate, detected in 2003 (A/Lyon/0838/2003), had its HA clustering within the HAs of the AH1N1 subtypes. To determine if this virus was a new reassortant, the nucleotide sequences of its eight RNA gene segments were compared with those of five representative strains of the AH1N1, AH1N2 and AH3N2 viruses, isolated during the same time-period. According to the sequences obtained, the neuraminidase (NA) gene segment of the A/Lyon/0838/2003 (H1N2) virus was genetically closely related to those of the AH1N2 viruses, whereas the six internal genes appeared to be clustering with those of the AH1N1 viruses. This suggested that the A/Lyon/0838/2003 (H1N2) virus was the result of a second reassortment event that had occurred during the winter of 2002-2003; the N2 gene segment of an AH1N2 virus being introduced into an AH1N1 genetic background. Subsequently, we analysed the extremities of each gene segment of the viruses from the different subtypes, and experimentally reproduced, in vitro, AH1N2 reassortant viruses through co-infection of Madin-Darby canine kidney (MDCK) cells with both AH1N1 and AH1N2 viruses, isolated in the 2002-2003 influenza season. While the comparison of the AH1N1 and the AH1N2 gene segment extremities revealed no major differences, we successfully reproduced an AH1N2 reassortant virus similar to the A/Lyon/0838/2003 (H1N2) virus. This result provided an experimental evidence of the compatibility between their respective surface H1 and N2 glycoproteins, and suggests that similar events may occur silently amongst human subtypes.