Influenza A viruses of swine circulating in the United States during 2009-2014 are susceptible to neuraminidase inhibitors but show lineage-dependent resistance to adamantanes

Tatiana Baranovich; Justin Bahl; Bindumadhav M. Marathe; Marie Culhane; Evelyn Stigger-Rosser; Daniel Darnell; Bryan S. Kaplan; James F. Lowe; Richard J. Webby; Elena A. Govorkova

doi:10.1016/j.antiviral.2015.02.004

Influenza A viruses of swine circulating in the United States during 2009-2014 are susceptible to neuraminidase inhibitors but show lineage-dependent resistance to adamantanes

Tatiana Baranovich, Justin Bahl, Bindumadhav M. Marathe, Marie Culhane, Evelyn Stigger-Rosser, Daniel Darnell, Bryan S. Kaplan, James F. Lowe, Richard J. Webby, Elena A. Govorkova

Veterinary Population Medicine

Research output: Contribution to journal › Article › peer-review

11 Scopus citations

Abstract

Antiviral drug susceptibility is one of the evaluation criteria of pandemic potential posed by an influenza virus. Influenza A viruses of swine (IAV-S) can play an important role in generating novel variants, yet limited information is available on the drug resistance profiles of IAV-S circulating in the U.S. Phenotypic analysis of the IAV-S isolated in the U.S. (2009-2011) (n ≥ 105) revealed normal inhibition by the neuraminidase (NA) inhibitors (NAIs) oseltamivir, zanamivir, and peramivir. Screening NA sequences from IAV-S collected in the U.S. (1930-2014) showed 0.03% (1/3396) sequences with clinically relevant H274Y-NA substitution. Phenotypic analysis of IAV-S isolated in the U.S. (2009-2011) confirmed amantadine resistance caused by the S31N-M2 and revealed an intermediate level of resistance caused by the I27T-M2. The majority (96.7%, 589/609) of IAV-S with the I27T-M2 in the influenza database were isolated from pigs in the U.S. The frequency of amantadine-resistant markers among IAV-S in the U.S. was high (71%), and their distribution was M-lineage dependent. All IAV-S of the Eurasian avian M lineage were amantadine-resistant and possessed either a single S31N-M2 substitution (78%, 585/747) or its combination with the V27A-M2 (22%, 162/747). The I27T-M2 substitution accounted for 43% (429/993) of amantadine resistance in classic swine M lineage. Phylogenetic analysis showed that both S31N-M2 and I27T-M2 emerged stochastically but appeared to be fixed in the U.S. IAV-S population. This study defines a drug-susceptibility profile, identifies the frequency of drug-resistant markers, and establishes a phylogenetic approach for continued antiviral-susceptibility monitoring of IAV-S in the U.S.

Original language	English (US)
Pages (from-to)	10-19
Number of pages	10
Journal	Antiviral Research
Volume	117
DOIs	https://doi.org/10.1016/j.antiviral.2015.02.004
State	Published - May 2015

Bibliographical note

Funding Information:
This work was supported by the National Institute of Allergy and Infectious Diseases of the National Institutes of Health , under contract numbers HHSN266200700005C and HHSN272201400006C and by ALSAC . The authors thank Jianling Armstrong, Jeri Carol Crumpton, Adam Rubrum, and Kristi Ann Prevost for technical support and Angela J. McArthur for scientific editing the manuscript. The NAIs oseltamivir carboxylate (oseltamivir) and zanamivir were provided by Hoffmann-La Roche, Ltd. (Basel, Switzerland). The NAI peramivir was provided by BioCryst Pharmaceuticals (Birmingham, AL).

Publisher Copyright:
© 2015 Elsevier B.V. All rights reserved.

Keywords

Amantadine
Antiviral resistance
Neuraminidase inhibitors
Oseltamivir
Porcine influenza virus
Swine influenza virus

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10.1016/j.antiviral.2015.02.004

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Baranovich, T., Bahl, J., Marathe, B. M., Culhane, M., Stigger-Rosser, E., Darnell, D., Kaplan, B. S., Lowe, J. F., Webby, R. J., & Govorkova, E. A. (2015). Influenza A viruses of swine circulating in the United States during 2009-2014 are susceptible to neuraminidase inhibitors but show lineage-dependent resistance to adamantanes. Antiviral Research, 117, 10-19. https://doi.org/10.1016/j.antiviral.2015.02.004

Baranovich, T, Bahl, J, Marathe, BM, Culhane, M, Stigger-Rosser, E, Darnell, D, Kaplan, BS, Lowe, JF, Webby, RJ & Govorkova, EA 2015, 'Influenza A viruses of swine circulating in the United States during 2009-2014 are susceptible to neuraminidase inhibitors but show lineage-dependent resistance to adamantanes', Antiviral Research, vol. 117, pp. 10-19. https://doi.org/10.1016/j.antiviral.2015.02.004

@article{664e583679174507afbb302158cb33eb,

title = "Influenza A viruses of swine circulating in the United States during 2009-2014 are susceptible to neuraminidase inhibitors but show lineage-dependent resistance to adamantanes",

abstract = "Antiviral drug susceptibility is one of the evaluation criteria of pandemic potential posed by an influenza virus. Influenza A viruses of swine (IAV-S) can play an important role in generating novel variants, yet limited information is available on the drug resistance profiles of IAV-S circulating in the U.S. Phenotypic analysis of the IAV-S isolated in the U.S. (2009-2011) (n ≥ 105) revealed normal inhibition by the neuraminidase (NA) inhibitors (NAIs) oseltamivir, zanamivir, and peramivir. Screening NA sequences from IAV-S collected in the U.S. (1930-2014) showed 0.03% (1/3396) sequences with clinically relevant H274Y-NA substitution. Phenotypic analysis of IAV-S isolated in the U.S. (2009-2011) confirmed amantadine resistance caused by the S31N-M2 and revealed an intermediate level of resistance caused by the I27T-M2. The majority (96.7%, 589/609) of IAV-S with the I27T-M2 in the influenza database were isolated from pigs in the U.S. The frequency of amantadine-resistant markers among IAV-S in the U.S. was high (71%), and their distribution was M-lineage dependent. All IAV-S of the Eurasian avian M lineage were amantadine-resistant and possessed either a single S31N-M2 substitution (78%, 585/747) or its combination with the V27A-M2 (22%, 162/747). The I27T-M2 substitution accounted for 43% (429/993) of amantadine resistance in classic swine M lineage. Phylogenetic analysis showed that both S31N-M2 and I27T-M2 emerged stochastically but appeared to be fixed in the U.S. IAV-S population. This study defines a drug-susceptibility profile, identifies the frequency of drug-resistant markers, and establishes a phylogenetic approach for continued antiviral-susceptibility monitoring of IAV-S in the U.S.",

keywords = "Amantadine, Antiviral resistance, Neuraminidase inhibitors, Oseltamivir, Porcine influenza virus, Swine influenza virus",

author = "Tatiana Baranovich and Justin Bahl and Marathe, {Bindumadhav M.} and Marie Culhane and Evelyn Stigger-Rosser and Daniel Darnell and Kaplan, {Bryan S.} and Lowe, {James F.} and Webby, {Richard J.} and Govorkova, {Elena A.}",

note = "Funding Information: This work was supported by the National Institute of Allergy and Infectious Diseases of the National Institutes of Health , under contract numbers HHSN266200700005C and HHSN272201400006C and by ALSAC . The authors thank Jianling Armstrong, Jeri Carol Crumpton, Adam Rubrum, and Kristi Ann Prevost for technical support and Angela J. McArthur for scientific editing the manuscript. The NAIs oseltamivir carboxylate (oseltamivir) and zanamivir were provided by Hoffmann-La Roche, Ltd. (Basel, Switzerland). The NAI peramivir was provided by BioCryst Pharmaceuticals (Birmingham, AL). Publisher Copyright: {\textcopyright} 2015 Elsevier B.V. All rights reserved.",

year = "2015",

month = may,

doi = "10.1016/j.antiviral.2015.02.004",

language = "English (US)",

volume = "117",

pages = "10--19",

journal = "Antiviral Research",

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TY - JOUR

T1 - Influenza A viruses of swine circulating in the United States during 2009-2014 are susceptible to neuraminidase inhibitors but show lineage-dependent resistance to adamantanes

AU - Baranovich, Tatiana

AU - Bahl, Justin

AU - Marathe, Bindumadhav M.

AU - Culhane, Marie

AU - Stigger-Rosser, Evelyn

AU - Darnell, Daniel

AU - Kaplan, Bryan S.

AU - Lowe, James F.

AU - Webby, Richard J.

AU - Govorkova, Elena A.

N1 - Funding Information: This work was supported by the National Institute of Allergy and Infectious Diseases of the National Institutes of Health , under contract numbers HHSN266200700005C and HHSN272201400006C and by ALSAC . The authors thank Jianling Armstrong, Jeri Carol Crumpton, Adam Rubrum, and Kristi Ann Prevost for technical support and Angela J. McArthur for scientific editing the manuscript. The NAIs oseltamivir carboxylate (oseltamivir) and zanamivir were provided by Hoffmann-La Roche, Ltd. (Basel, Switzerland). The NAI peramivir was provided by BioCryst Pharmaceuticals (Birmingham, AL). Publisher Copyright: © 2015 Elsevier B.V. All rights reserved.

PY - 2015/5

Y1 - 2015/5

N2 - Antiviral drug susceptibility is one of the evaluation criteria of pandemic potential posed by an influenza virus. Influenza A viruses of swine (IAV-S) can play an important role in generating novel variants, yet limited information is available on the drug resistance profiles of IAV-S circulating in the U.S. Phenotypic analysis of the IAV-S isolated in the U.S. (2009-2011) (n ≥ 105) revealed normal inhibition by the neuraminidase (NA) inhibitors (NAIs) oseltamivir, zanamivir, and peramivir. Screening NA sequences from IAV-S collected in the U.S. (1930-2014) showed 0.03% (1/3396) sequences with clinically relevant H274Y-NA substitution. Phenotypic analysis of IAV-S isolated in the U.S. (2009-2011) confirmed amantadine resistance caused by the S31N-M2 and revealed an intermediate level of resistance caused by the I27T-M2. The majority (96.7%, 589/609) of IAV-S with the I27T-M2 in the influenza database were isolated from pigs in the U.S. The frequency of amantadine-resistant markers among IAV-S in the U.S. was high (71%), and their distribution was M-lineage dependent. All IAV-S of the Eurasian avian M lineage were amantadine-resistant and possessed either a single S31N-M2 substitution (78%, 585/747) or its combination with the V27A-M2 (22%, 162/747). The I27T-M2 substitution accounted for 43% (429/993) of amantadine resistance in classic swine M lineage. Phylogenetic analysis showed that both S31N-M2 and I27T-M2 emerged stochastically but appeared to be fixed in the U.S. IAV-S population. This study defines a drug-susceptibility profile, identifies the frequency of drug-resistant markers, and establishes a phylogenetic approach for continued antiviral-susceptibility monitoring of IAV-S in the U.S.

AB - Antiviral drug susceptibility is one of the evaluation criteria of pandemic potential posed by an influenza virus. Influenza A viruses of swine (IAV-S) can play an important role in generating novel variants, yet limited information is available on the drug resistance profiles of IAV-S circulating in the U.S. Phenotypic analysis of the IAV-S isolated in the U.S. (2009-2011) (n ≥ 105) revealed normal inhibition by the neuraminidase (NA) inhibitors (NAIs) oseltamivir, zanamivir, and peramivir. Screening NA sequences from IAV-S collected in the U.S. (1930-2014) showed 0.03% (1/3396) sequences with clinically relevant H274Y-NA substitution. Phenotypic analysis of IAV-S isolated in the U.S. (2009-2011) confirmed amantadine resistance caused by the S31N-M2 and revealed an intermediate level of resistance caused by the I27T-M2. The majority (96.7%, 589/609) of IAV-S with the I27T-M2 in the influenza database were isolated from pigs in the U.S. The frequency of amantadine-resistant markers among IAV-S in the U.S. was high (71%), and their distribution was M-lineage dependent. All IAV-S of the Eurasian avian M lineage were amantadine-resistant and possessed either a single S31N-M2 substitution (78%, 585/747) or its combination with the V27A-M2 (22%, 162/747). The I27T-M2 substitution accounted for 43% (429/993) of amantadine resistance in classic swine M lineage. Phylogenetic analysis showed that both S31N-M2 and I27T-M2 emerged stochastically but appeared to be fixed in the U.S. IAV-S population. This study defines a drug-susceptibility profile, identifies the frequency of drug-resistant markers, and establishes a phylogenetic approach for continued antiviral-susceptibility monitoring of IAV-S in the U.S.

KW - Amantadine

KW - Antiviral resistance

KW - Neuraminidase inhibitors

KW - Oseltamivir

KW - Porcine influenza virus

KW - Swine influenza virus

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Influenza A viruses of swine circulating in the United States during 2009-2014 are susceptible to neuraminidase inhibitors but show lineage-dependent resistance to adamantanes

Abstract

Bibliographical note

Keywords

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