Expansion of Genotypic Diversity and Establishment of 2009 H1N1 Pandemic-Origin Internal Genes in Pigs in China

Liang, Huyi; Lam, Tommy Tsan-Yuk; Fan, Xiao; Chen, Xinchun; Zeng, Yu; Zhou, Ji; Duan, Lian; Tse, Tsemay M.; Chan, Chung-Hei; Li, Lifeng; Leung, Tak-Ying; Yip, Chun-Hung; Cheung, Y. M.; Zhou, Boping; Smith, David K.; Poon, Leo L. M.; Peiris, Malik; Guan, Yi; Zhu, Hua

doi:10.1128/jvi.01327-14

Cited by 88 publications

(104 citation statements)

References 44 publications

(66 reference statements)

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“…A possible explanation is that the TRIG lineage is more permissive to reassortment with H1N1pdm09 and incorporation of internal genes. Reassortants with H1N1pdm09-TRIG internal genes were also more frequently detected in China, and the reassortants that circulated the longest had at least five H1N1pdm09-origin genes (16). These Chinese H1N1pdm09 reassortants became predominant with time, and the authors speculated that the H1N1pdm09 internal genes replace the Eurasian and TRIG internal genes in China (16).…”

Section: Discussionmentioning

confidence: 99%

“…Notably, the introduction of H1N1pdm09 into pigs was concurrent with an increase in genetic diversity at the whole-genome and surface gene levels of contemporary swine IAV. Reassortment events between endemic swine and H1N1pdm09 viruses have been reported in many countries (8,10,14,15), and viruses containing different constellations of H1N1pdm09 internal genes are now predominant among IAV circulating in Chinese pigs (16). In the United States, the M gene from H1N1pdm09 quickly replaced the TRIG M gene, but other H1N1pdm09 internal genes were also detected (5,17).…”

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confidence: 99%

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Reassortment between Swine H3N2 and 2009 Pandemic H1N1 in the United States Resulted in Influenza A Viruses with Diverse Genetic Constellations with Variable Virulence in Pigs

Rajão

Walia

Campbell

et al. 2017

J Virol

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Repeated spillovers of the H1N1 pandemic virus (H1N1pdm09) from humans to pigs resulted in substantial evolution of influenza A viruses infecting swine, contributing to the genetic and antigenic diversity of influenza A viruses (IAV) currently circulating in swine. The reassortment with endemic swine viruses and maintenance of some of the H1N1pdm09 internal genes resulted in the circulation of different genomic constellations in pigs. Here, we performed a whole-genome phylogenetic analysis of 368 IAV circulating in swine from 2009 to 2016 in the United States. We identified 44 different genotypes, with the most common genotype (32.33%) containing a clade IV-A HA gene, a 2002-lineage NA gene, an M-pdm09 gene, and remaining gene segments of triple reassortant internal gene (TRIG) origin. To understand how different genetic constellations may relate to viral fitness, we compared the pathogenesis and transmission in pigs of six representative genotypes. Although all six genotypes efficiently infected pigs, they resulted in different degrees of pathology and viral shedding. These results highlight the vast H3N2 genetic diversity circulating in U.S. swine after 2009. This diversity has important implications in the control of this disease by the swine industry, as well as a potential risk for public health if swine-adapted viruses with H1N1pdm09 genes have an increased risk to humans, as occurred in the 2011-2012 and 2016 human variant H3N2v cases associated with exhibition swine. IMPORTANCE People continue to spread the 2009 H1N1 pandemic (H1N1pdm09) IAV to pigs, allowing H1N1pdm09 to reassort with endemic swine IAV. In this study, we determined the 8 gene combinations of swine H3N2 IAV detected from 2009 to 2016. We identified 44 different genotypes of H3N2, the majority of which contained at least one H1N1pdm09 gene segment. We compared six representative genotypes of H3N2 in pigs. All six genotypes efficiently infected pigs, but they resulted in different degrees of lung damage and viral shedding. These results highlight the vast genetic diversity of H3N2 circulating in U.S. swine after 2009, with important implications for the control of IAV for the swine industry. Because H1N1pdm09 is also highly adapted to humans, these swine viruses pose a potential risk to public health if swine-adapted viruses with H1N1pdm09 genes also have an increased risk for human infection.

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Reassortment between Swine H3N2 and 2009 Pandemic H1N1 in the United States Resulted in Influenza A Viruses with Diverse Genetic Constellations with Variable Virulence in Pigs

Rajão

Walia

Campbell

et al. 2017

J Virol

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“…Since pigs may facilitate the introduction of avian viruses or viral genes to humans, transmission of avian H9N2 viruses to pigs raises concerns over the possible generation of human pandemic influenza strains (9). This has been heightened since the emergence of the swine-origin 2009 H1N1 pandemic influenza virus (28,29) and the subsequent rapid expansion of the genetic diversity of swine influenza viruses (30,31).…”

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confidence: 99%

Infectivity and Transmissibility of Avian H9N2 Influenza Viruses in Pigs

Wang

Hong

et al. 2016

J Virol

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The H9N2 influenza viruses that are enzootic in terrestrial poultry in China pose a persistent pandemic threat to humans. To investigate whether the continuous circulation and adaptation of these viruses in terrestrial poultry increased their infectivity to pigs, we conducted a serological survey in pig herds with H9N2 viruses selected from the aquatic avian gene pool (Y439 lineage) and the enzootic terrestrial poultry viruses (G1 and Y280 lineages). We also compared the infectivity and transmissibility of these viruses in pigs. It was found that more than 15% of the pigs sampled from 2010 to 2012 in southern China were seropositive to either G1 or Y280 lineage viruses, but none of the sera were positive to the H9 viruses from the Y439 lineage. Viruses of the G1 and Y280 lineages were able to infect experimental pigs, with detectable nasal shedding of the viruses and seroconversion, whereas viruses of the Y439 lineage did not cause a productive infection in pigs. Thus, adaptation and prevalence in terrestrial poultry could lead to interspecies transmission of H9N2 viruses from birds to pigs. Although H9N2 viruses do not appear to be continuously transmissible among pigs, repeated introductions of H9 viruses to pigs naturally increase the risk of generating mammalian-adapted or reassorted variants that are potentially infectious to humans. This study highlights the importance of monitoring the activity of H9N2 viruses in terrestrial poultry and pigs. IMPORTANCEH9N2 subtype of influenza viruses has repeatedly been introduced into mammalian hosts, including humans and pigs, so awareness of their activity and evolution is important for influenza pandemic preparedness. However, since H9N2 viruses usually cause mild or even asymptomatic infections in mammalian hosts, they may be overlooked in influenza surveillance. Here, we found that the H9N2 viruses established in terrestrial poultry had higher infectivity in pigs than those from aquatic birds, which suggests that adaptation of the H9N2 viruses in terrestrial poultry might have increased the infectivity of the virus to mammals. Therefore, monitoring the prevalence and evolution of H9 viruses prevalent in terrestrial birds and conducting risk assessment of their threat to mammals are critical for evaluating the pandemic potential of this virus.

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“…In the United States, the TRIG lineage was the predominant lineage prior to 2009. Recent records have shown that the H1N1pdm09 viruses have reassorted extensively with other co-circulating swine IAV in both H1 and H3 subtypes [9,22,23,26] and gradually replaced the dominant TRIG lineage internal genes, especially the pdm-lineage M gene [23,24,27]. All eight pdm-lineage genes were detected in our study in various combinations with TRIG-lineage genes.…”

Section: Discussionmentioning

confidence: 59%

“…The introduction of human seasonal IAV to swine and reassortment has been associated with subsequent antigenic evolution in multiple swine IAV lineages, including in southern China [24] and Europe [25]. Multiple internal Table 1.…”

Section: Discussionmentioning

confidence: 99%

The genomic evolution of H1 influenza A viruses from swine detected in the United States between 2009 and 2016

Gao

Anderson

Walia

et al. 2017

Journal of General Virology

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Transmission of influenza A virus (IAV) from humans to swine occurs with relative frequency and is a critical contributor to swine IAV diversity. Subsequent to the introduction of these human seasonal lineages, there is often reassortment with endemic viruses and antigenic drift. To address whether particular genome constellations contributed to viral persistence following the introduction of the 2009 H1N1 human pandemic virus to swine in the USA, we collated and analysed 616 whole genomes of swine H1 isolates. For each gene, sequences were aligned, the best-known maximum likelihood phylogeny was inferred, and each virus was assigned a clade based upon its evolutionary history. A time-scaled Bayesian approach was implemented for the haemagglutinin (HA) gene to determine the patterns of genetic diversity over time. From these analyses, we observed an increase in genome diversity across all H1 lineages and clades, with the H1-g and H1-d1 genetic clades containing the greatest number of unique genome patterns. We documented 74 genome patterns from 2009 to 2016, of which 3 genome patterns were consistently detected at a significantly higher level than others across the entire time period. Eight genome patterns increased significantly, while five genome patterns were shown to decline in detection over time. Viruses with genome patterns identified as persisting in the US swine population may possess a greater capacity to infect and transmit in swine. This study highlights the emerging genetic diversity of US swine IAV from 2009 to 2016, with implications for swine and public health and vaccine control efforts.

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Expansion of Genotypic Diversity and Establishment of 2009 H1N1 Pandemic-Origin Internal Genes in Pigs in China

Cited by 88 publications

References 44 publications

Reassortment between Swine H3N2 and 2009 Pandemic H1N1 in the United States Resulted in Influenza A Viruses with Diverse Genetic Constellations with Variable Virulence in Pigs

Reassortment between Swine H3N2 and 2009 Pandemic H1N1 in the United States Resulted in Influenza A Viruses with Diverse Genetic Constellations with Variable Virulence in Pigs

Infectivity and Transmissibility of Avian H9N2 Influenza Viruses in Pigs

The genomic evolution of H1 influenza A viruses from swine detected in the United States between 2009 and 2016

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