[Source: Proceedings of the National Academy of Sciences of the United States of America, full page: (LINK). Abstract, edited.]
Prevalent Eurasian avian-like H1N1 swine influenza virus with 2009 pandemic viral genes facilitating human infection
Honglei Sun, Yihong Xiao, Jiyu Liu, Dayan Wang, Fangtao Li, Chenxi Wang, Chong Li, Junda Zhu, Jingwei Song, Haoran Sun, Zhimin Jiang, Litao Liu, Xin Zhang, Kai Wei, Dongjun Hou, Juan Pu, Yipeng Sun, Qi Tong, Yuhai Bi, Kin-Chow Chang, Sidang Liu, George F. Gao, and Jinhua Liu
PNAS first published June 29, 2020 https://doi.org/10.1073/pnas.1921186117
Contributed by George F. Gao, April 28, 2020 (sent for review December 9, 2019; reviewed by Ian H. Brown and Xiu-Feng Henry Wan)
Pigs are intermediate hosts for the generation of pandemic influenza virus. Thus, systematic surveillance of influenza viruses in pigs is a key measure for prewarning the emergence of the next pandemic influenza. Here, we identified a reassortant EA H1N1 virus possessing pdm/09 and TR-derived internal genes, termed as G4 genotype, which has become predominant in swine populations since 2016. Similar to pdm/09 virus, G4 viruses have all the essential hallmarks of a candidate pandemic virus. Of concern is that swine workers show elevated seroprevalence for G4 virus. Controlling the prevailing G4 EA H1N1 viruses in pigs and close monitoring in human populations, especially the workers in swine industry, should be urgently implemented.
Pigs are considered as important hosts or “mixing vessels” for the generation of pandemic influenza viruses. Systematic surveillance of influenza viruses in pigs is essential for early warning and preparedness for the next potential pandemic. Here, we report on an influenza virus surveillance of pigs from 2011 to 2018 in China, and identify a recently emerged genotype 4 (G4) reassortant Eurasian avian-like (EA) H1N1 virus, which bears 2009 pandemic (pdm/09) and triple-reassortant (TR)-derived internal genes and has been predominant in swine populations since 2016. Similar to pdm/09 virus, G4 viruses bind to human-type receptors, produce much higher progeny virus in human airway epithelial cells, and show efficient infectivity and aerosol transmission in ferrets. Moreover, low antigenic cross-reactivity of human influenza vaccine strains with G4 reassortant EA H1N1 virus indicates that preexisting population immunity does not provide protection against G4 viruses. Further serological surveillance among occupational exposure population showed that 10.4% (35/338) of swine workers were positive for G4 EA H1N1 virus, especially for participants 18 y to 35 y old, who had 20.5% (9/44) seropositive rates, indicating that the predominant G4 EA H1N1 virus has acquired increased human infectivity. Such infectivity greatly enhances the opportunity for virus adaptation in humans and raises concerns for the possible generation of pandemic viruses.
swine influenza – Eurasian avian-like H1N1 virus – 2009 pandemic H1N1 virus – reassortant – pandemic potential
1 H.S., Y.X., and J.L. contributed equally to this work.
2 To whom correspondence may be addressed. Email: firstname.lastname@example.org or email@example.com.
Author contributions: Honglei Sun, Y.X., S.L., G.F.G., and Jinhua Liu designed research; Honglei Sun, Y.X., Jiyu Liu, F.L., C.L., J.Z., J.S., Haoran Sun, Z.J., L.L., X.Z., K.W., D.H., and Q.T. performed research; Honglei Sun, Jiyu Liu, D.W., C.W., J.P., Y.B., and Jinhua Liu analyzed data; and Honglei Sun, J.P., Y.S., K.-C.C., G.F.G., and Jinhua Liu wrote the paper.
Reviewers: I.H.B., Animal and Plant Health Agency; and X.-F.H.W., University of Missouri.
The authors declare no competing interest.
Data deposition: The sequences generated in this study have been deposited in the GenBank database (accession nos. are listed in SI Appendix, Table S3).
This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1921186117/-/DCSupplemental.
Published under the PNAS license.
Keywords: Influenza A; Reassortant strain; Avian Influenza; Swine Influenza; Pigs; Human; China; H1N1; H1N1pdm09.