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Genetic Diversity and Evolution

Continual Reintroduction of Human Pandemic H1N1 Influenza A Viruses into Swine in the United States, 2009 to 2014

Martha I. Nelson, Jered Stratton, Mary Lea Killian, Alicia Janas-Martindale, Amy L. Vincent
R. M. Sandri-Goldin, Editor
Martha I. Nelson
aFogarty International Center, National Institutes of Health, Bethesda, Maryland, USA
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Jered Stratton
bVirus and Prion Research Unit, National Animal Disease Center, USDA-ARS, Ames, Iowa, USA
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Mary Lea Killian
cDiagnostic Virology Laboratory, National Veterinary Services Laboratories, Science, Technology and Analysis Services, Veterinary Services, USDA-APHIS, Ames, Iowa, USA
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Alicia Janas-Martindale
cDiagnostic Virology Laboratory, National Veterinary Services Laboratories, Science, Technology and Analysis Services, Veterinary Services, USDA-APHIS, Ames, Iowa, USA
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Amy L. Vincent
bVirus and Prion Research Unit, National Animal Disease Center, USDA-ARS, Ames, Iowa, USA
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R. M. Sandri-Goldin
Roles: Editor
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DOI: 10.1128/JVI.00459-15
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  • FIG 1
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    FIG 1

    Phylogenetic relationships between pandemic H1 segments. The time-scaled Bayesian MCC tree was inferred for the HA (H1) sequences of 933 viruses collected from swine and humans in the United States from 2009 to 2014, including 173 viruses from swine and 760 viruses from humans. The branches are color coded by host and time (U.S. influenza epidemic) of collection (September to August). sw09-10, swine viruses collected during the 2009-2010 epidemic; sw10-11, swine viruses collected during the 2010-2011 epidemic; sw11-12, swine viruses collected during the 2011-2012 epidemic; sw12-13, swine viruses collected during the 2012-2013 epidemic; sw13-14, swine viruses collected during the 2013-2014 epidemic. The clade of human viruses from the 2013-2014 epidemic is highlighted in the box shaded orange. Posterior probabilities of >0.90 are provided for key nodes. An identical phylogeny with tip strain name labels is provided in Fig. S2 in the supplemental material.

  • FIG 2
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    FIG 2

    Heat map of virus transmission between humans and swine. Markov jump counts measure the number of inferred location state transitions, modeled by a continuous-time Markov chain process, that occur along the branches of the phylogeny. The intensity of the color (red, high; white, low) reflects the number of Markov jump counts between one temporally defined host population (y axis) and another (x axis), which have been abbreviated (e.g., hu08-09, viruses collected in humans during the 2008-2009 epidemic; sw08-09, swine viruses collected during the 2008-2009 epidemic). The results are presented separately for the NA (a) and NP (b) segments. For clarity, each heat map has been divided into four quadrants that represent linkages between human viruses from a seasonal epidemic and human viruses from a different (usually preceding) epidemic (i.e., human-to-human transmission) (I), linkages between swine viruses from a seasonal epidemic and human viruses from a different (usually preceding) epidemic (i.e., human-to-swine transmission) (II), linkages between human viruses and swine viruses (i.e., swine-to-human transmission) (III), and linkages between swine viruses and swine viruses from a different (usually preceding) epidemic (i.e., swine-to-swine transmission) (IV).

  • FIG 3
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    FIG 3

    Numbers of viruses with each of the eight pandemic segments. Of 444 viruses with whole-genome sequences (not including fair pigs or viruses with all eight segments of pandemic origin), the numbers that contain PB2, PB1, PA, HA, NP, NA, MP, and NS segments of pandemic origin are shown. The frequency of each segment indicates the extent of reassortment and onward maintenance of the pH1N1 internal genes in U.S. swine, with the loss of the HA and NA genes outside wholly pandemic viruses.

  • FIG 4
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    FIG 4

    Association between human-to-swine virus transmission and pH1N1 activity in humans. (a) Proportion of total influenza virus specimens that were positive for pH1N1 virus calculated for each week from the beginning of the pandemic in the United States (week 35 of 2009) to the most recent report (week 39 of 2014), as reported by CDC FluView (http://www.cdc.gov/flu/weekly). (b) Heat map of the number of Markov jump counts between one temporally defined host population (y axis) and another (x axis). The labeling of the heat map is similar to that in Fig. 2 except that, for simplicity, all human viruses from 2009 to 2014 were consolidated into a single category, “human.”

Tables

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  • TABLE 1

    Characteristics of 20 H1-pdm viruses from U.S. swine collected during 2014a

    GenBank accession no.Virus nameCollection date (mo/day/yr)Evolutionary origin
    PB2PB1PAHANPNAMPNS
    KJ437560A/swine/Illinois/A01411340/2014/H1N11/−/14pdmpdm
    KJ493356A/swine/Illinois/A01411419/2014/H1N12/−/14pdmpdm
    KJ206094A/swine/Illinois/A01490609/2014 H1N11/8/14pdmpdmpdmpdmpdmpdmpdmpdm
    KJ528259A/swine/Illinois/A01492501/2014 H1N12/12/14pdmpdmpdmpdmpdmpdmpdmpdm
    KJ701784A/swine/Illinois/A01493472/2014 H1N13/26/14pdmpdmpdmpdmpdmpdmpdmpdm
    KJ701853A/swine/Iowa/A01410472/2014 H1N13/3/14pdmpdmpdmpdmpdmpdmpdmpdm
    KJ907733A/swine/Kansas/A01377299/2014 H1N14/30/14pdmpdmpdmpdmpdmpdmpdmpdm
    KJ605091A/swine/Kansas/A01410327/2014 H1N12/7/14pdmpdmpdmpdmpdmpdmpdmpdm
    KJ417899A/swine/Minnesota/A01491447/2014 H1N11/27/14pdmpdmpdmpdmpdmpdmpdmpdm
    KJ417893A/swine/Minnesota/A01491451/2014/H1N11/27/14pdmpdm
    KJ417884A/swine/Minnesota/A01491464/2014/H1N11/27/14pdmpdm
    KJ493336A/swine/Minnesota/A01491704/2014 H1N12/4/14pdmpdmpdmpdmpdmpdmpdmpdm
    KJ667964A/swine/Missouri/A01492887/2014 H1N12/10/14pdmpdmpdmpdmpdmpdmpdmpdm
    KJ206223A/swine/Nebraska/A01366774/2014 H1N11/17/14pdmpdmpdmpdmpdmpdmpdmpdm
    KJ417890A/swine/Nebraska/A01491300/2014 H1N11/27/14pdmpdmpdmpdmpdmpdmpdmpdm
    KJ417881A/swine/Nebraska/A01491382/2014/H1N11/27/14pdmpdm
    KJ493342A/swine/Nebraska/A01491508/2014/H1N11/30/14pdmpdm
    KJ588390A/swine/Nebraska/A01492657/2014 H1N12/27/14pdmpdmpdmpdmpdmpdmpdmpdm
    KJ809095A/swine/Nebraska/A01509523/2014/H1N14/24/14pdmpdm
    KJ739422A/swine/North Carolina/A01410573/2014 H1N13/21/14pdmpdmpdmpdmpdmpdmpdmpdm
    • ↵a The virus name, collection date, and GenBank accession number (HA segment) are provided for the 20 HA and NA segments of pandemic origin (pdm) that were collected from swine in the United States in 2014. The evolutionary origins of HA and NA for all 20 viruses and the evolutionary origins of all eight segments for the 13 viruses that were whole-genome sequenced are provided.

Additional Files

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  • Supplemental material

    • Supplemental file 1 -

      Fig. S1 (Maximum likelihood tree of human and swine pandemic H1 segments.)

      Fig. S2 (Phylogenetic relationships between pandemic H1 segments.)

      Fig. S3 (Phylogenetic relationships between pandemic N1 segments.)

      Fig. S4 (Heat map of viral transmissions between humans and swine for HA segment.)

      Fig. S5 (Phylogenetic relationships between pandemic NP segments.)

      Fig. S6 (Phylogenetic relationships between pandemic PB2 segments.)

      Table S1 (One hundred HA sequences from human H1N1 pandemic viruses from 2014 obtained from the GISAID Epiflu database.)

      Table S2 (Pandemic H1N1 influenza A virus sequences (HA segment) used in this analysis (Fig. 1).)

      Table S3 (Pandemic H1N1 influenza A virus sequences (NA segment) used in this analysis (Fig. S3).)

      Table S4 (Pandemic H1N1 influenza A virus sequences (NP segment) used in this analysis (Fig. S5).)

      Table S5 (Estimated transitions between humans and swine on HA MCC phylogeny, represented by “Markov jumps.”)

      Table S6 (Estimated transitions between humans and swine on NA MCC phylogeny, represented by “Markov jumps.”)

      Table S7 (Estimated transitions between humans and swine on NP MCC phylogeny, represented by “Markov jumps.”)

      Table S8 (Evolutionary origins of each genome segment for 444 U.S. swine viruses collected from 2009 to 2014.)

      PDF, 3.7M

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Continual Reintroduction of Human Pandemic H1N1 Influenza A Viruses into Swine in the United States, 2009 to 2014
Martha I. Nelson, Jered Stratton, Mary Lea Killian, Alicia Janas-Martindale, Amy L. Vincent
Journal of Virology May 2015, 89 (12) 6218-6226; DOI: 10.1128/JVI.00459-15

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Continual Reintroduction of Human Pandemic H1N1 Influenza A Viruses into Swine in the United States, 2009 to 2014
Martha I. Nelson, Jered Stratton, Mary Lea Killian, Alicia Janas-Martindale, Amy L. Vincent
Journal of Virology May 2015, 89 (12) 6218-6226; DOI: 10.1128/JVI.00459-15
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