The genetic diversity, replication, and transmission of 2009 pandemic H1N1 viruses in China

Hailiang Sun; Yongcui Wang; Hanlin Liu; Zifeng Pang; Xinxin Cui; Rui Zhao; Yanwei Liu; Xiaoyun Qu; Mian Huang; Changwen Ke; Ming Liao

doi:10.3389/fmicb.2023.1110100

The genetic diversity, replication, and transmission of 2009 pandemic H1N1 viruses in China

Front Microbiol. 2023 Feb 17:14:1110100. doi: 10.3389/fmicb.2023.1110100. eCollection 2023.

Authors

Hailiang Sun^{1

2

3}, Yongcui Wang⁴, Hanlin Liu^{1

2

3}, Zifeng Pang^{1

2

3}, Xinxin Cui^{1

2

3}, Rui Zhao^{1

2

3}, Yanwei Liu^{1

2

3}, Xiaoyun Qu^{1

2

3}, Mian Huang⁵, Changwen Ke⁶, Ming Liao^{1

2

3}

Affiliations

¹ College of Veterinary Medicine, South China Agricultural University, Guangzhou, China.
² National and Regional Joint Engineering Laboratory for Medicament of Zoonosis Prevention and Control, South China Agricultural University, Guangzhou, China.
³ Key Laboratory of Zoonosis Control and Prevention of Guangdong Province, South China Agricultural University, Guangzhou, China.
⁴ The Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining, China.
⁵ Guangzhou Zoo, The People's Government of Guangzhou Municipality, Guangzhou, China.
⁶ Guangdong Provincial Center for Disease Control and Prevention, The People's Government of Guangzhou Municipality, Guangzhou, China.

Abstract

Background: The 2009 pandemic H1N1 influenza A virus (pdm09) continue to evolve, and few studies have systemically analyzed the evolution, replication, and transmission of pmd09 viruses in China.

Methods: To better understand the evolution and pathogenicity of pdm09 viruses, we systematically analyzed viruses that were confirmed in 2009-2020 in China and characterized their replication and transmission ability. We extensively analyzed the evolution characteristics of pdm/09 in China over the past decades. The replication ability of 6B.1 and 6B.2 lineages on Madin-Darby canine kidney (MDCK) and human lung adenocarcinoma epithelial (A549) cells and their pathogenicity and transmission in guinea pigs were also compared.

Results: In total, 3,038 pdm09 viruses belonged to clade 6B.1 (62% of all pdm09 viruses) and clade 6B.2 (4%). Clade 6B.1 pdm09 viruses are the predominant clade, with proportions of 54.1%, 78.9%, 57.2%, 58.6%, 61.7%, 76.3%, and 66.6% in the North, Northeast, East, Central, South, Southwest, and Northeast regions in China, respectively. The isolation proportion of clade 6B.1 pdm/09 viruses was 57.1%, 74.3%, 96.1%, 98.2%, 86.7%, and 78.5% in 2015-2020, respectively. A clear differentiation time point appeared in 2015 before which the evolution trend of pdm09 viruses in China was similar to that in North America but then showed a different trend after that point. To characterize pdm09 viruses in China after 2015, we further analyzed 33 pdm09 viruses isolated in Guangdong in 2016-2017, among which A/ Guangdong/33/2016 and A/Guangdong/184/2016 (184/2016) belonged to clade 6B.2, and the other 31 strains belonged to clade 6B.1. A/Guangdong/887/2017 (887/2017) and A/Guangdong/752/2017 (752/2017) (clade 6B.1), 184/2016 (clade 6B.2) and A/California/04/2009 (CA04) replicated efficiently in MDCK cells and A549 cells, as well as the turbinates of guinea pigs. 184/2016 and CA04 could transmit among guinea pigs through physical contact.

Conclusion: Our findings provide novel insights into the evolution, pathogenicity, and transmission of pdm09 virus. The results show that enhancing surveillance of pdm09 viruses and timely evaluation of their virulence are essential.

Keywords: haplotypes analysis; influenza; phylogenetic analysis; replication; transmission.