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

Volumn 117, Issue , 2015, Pages 10-19

  Baranovich, Tatiana ^a   Bahl, Justin ^b,c   Marathe, Bindumadhav M ^a   Culhane, Marie ^d   Stigger Rosser, Evelyn ^a   Darnell, Daniel ^a   Kaplan, Bryan S ^a   Lowe, James F ^e   Webby, Richard J ^a   Govorkova, Elena A ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b UNIVERSITY OF TEXAS SCHOOL OF PUBLIC HEALTH   (United States)

^c DUKE NUS MEDICAL SCHOOL   (Singapore)

^d UNIVERSITY OF MINNESOTA   (United States)

^e UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

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

Indexed keywords

ADAMANTANE; MOLECULAR MARKER; OSELTAMIVIR; PERAMIVIR; SIALIDASE INHIBITOR; ZANAMIVIR; ANTIVIRUS AGENT; CYCLOPENTANE DERIVATIVE; ENZYME INHIBITOR; GUANIDINE DERIVATIVE; SIALIDASE; VIRAL PROTEIN;

AMINO ACID SUBSTITUTION; ANTIVIRAL RESISTANCE; ANTIVIRAL SUSCEPTIBILITY; ANTIVIRAL THERAPY; ARTICLE; AVIAN INFLUENZA VIRUS; CONTROLLED STUDY; DATA BASE; DRUG MONITORING; EC50; IC50; INFLUENZA A; INFLUENZA VIRUS A; NONHUMAN; PHENOTYPIC VARIATION; PHYLOGENY; PRIORITY JOURNAL; SWINE INFLUENZA VIRUS; UNITED STATES; VIRUS ISOLATION; ANIMAL; ANTAGONISTS AND INHIBITORS; DOG; DRUG EFFECTS; GENETICS; GENOTYPE; INFLUENZA A VIRUS; INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H1N2); INFLUENZA A VIRUS (H3N2); MDCK CELL LINE; MISSENSE MUTATION; NUCLEOTIDE SEQUENCE; ORTHOMYXOVIRIDAE INFECTIONS; PHENOTYPE; PIG; SWINE DISEASE; TIME FACTOR; VETERINARY; VIROLOGY;

AVES; INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE; SUIDAE; SUS; SWINE INFLUENZA VIRUS;

ADAMANTANE; AMINO ACID SUBSTITUTION; ANIMALS; ANTIVIRAL AGENTS; BASE SEQUENCE; CYCLOPENTANES; DOGS; DRUG RESISTANCE, VIRAL; ENZYME INHIBITORS; GENOTYPE; GUANIDINES; INFLUENZA A VIRUS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H1N2 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; MADIN DARBY CANINE KIDNEY CELLS; MUTATION, MISSENSE; NEURAMINIDASE; ORTHOMYXOVIRIDAE INFECTIONS; OSELTAMIVIR; PHENOTYPE; PHYLOGENY; SWINE; SWINE DISEASES; TIME FACTORS; UNITED STATES; VIRAL PROTEINS; ZANAMIVIR;

EID: 84923809006     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2015.02.004     Document Type: Article

References (50)

1. Y. Abed, N. Goyette, and G. Boivin Generation and characterization of recombinant influenza A (H1N1) viruses harboring amantadine resistance mutations Antimicrob. Agents chemother. 49 2005 556 559 10.1128/AAc.49.2.556-559.2005
2. T.K. Anderson, M.I. Nelson, P. Kitikoon, S.L. Swenson, J.A. Korslund, and A.L. Vincent Population dynamics of cocirculating swine influenza A viruses in the United States from 2009 to 2012 Influenza Other Respir. Viruses 7 Suppl. 4 2013 42 51 10.1111/irv.12193
3. A. Balish, R. Garten, A. Klimov, and J. Villanueva Analytical detection of influenza A(H3N2)v and other A variant viruses from the USA by rapid influenza diagnostic tests Influenza Other Respir. Viruses 7 2013 491 496 10.1111/irv.12017
4. N. Bastien, N.A. Antonishyn, K. Brandt, c.E. Wong, K. chokani, N. Vegh, G.B. Horsman, S. Tyler, M.R. Graham, F.A. Plummer, P.N. Levett, and Y. Li Human infection with a triple-reassortant swine influenza A(H1N1) virus containing the hemagglutinin and neuraminidase genes of seasonal influenza virus J. Infect. Dis. 201 2010 1178 1182 10.1086/651507
5. K. Bauer, R. Dürrwald, M. Schlegel, K. Pfarr, D. Topf, N. Wiesener, H.-M. Dahse, P. Wutzler, and M. Schmidtke Neuraminidase inhibitor susceptibility of swine influenza A viruses isolated in Germany between 1981 and 2008 Med. Microbiol. Immunol. (Berl.) 201 2012 61 72 10.1007/s00430-011-0206-1
6. K. Bauer, c. Schrader, J. Suess, P. Wutzler, and M. Schmidtke Neuraminidase inhibitor susceptibility of porcine H3N2 influenza A viruses isolated in Germany between 1982 and 1999 Antiviral Res. 75 2007 219 226 10.1016/j.antiviral.2007.03.007
7. W.J. Bean, S.c. Threlkeld, and R.G. Webster Biologic potential of amantadine-resistant influenza A virus in an avian model J. Infect. Dis. 159 1989 1050 1056
8. J.D. Bloom, L.I. Gong, and D. Baltimore Permissive secondary mutations enable the evolution of influenza oseltamivir resistance Science 328 2010 1272 1275 10.1126/science.1187816
9. R.A. Bright, M. Medina, X. Xu, G. Perez-Oronoz, T.R. Wallis, X.M. Davis, L. Povinelli, N.J. cox, and A.I. Klimov Incidence of adamantane resistance among influenza A (H3N2) viruses isolated worldwide from 1994 to 2005: a cause for concern Lancet 366 2005 1175 1181 10.1016/S0140-6736(05)67338-2
10. J. Butler, K.A. Hooper, S. Petrie, R. Lee, S. Maurer-Stroh, L. Reh, T. Guarnaccia, c. Baas, L. Xue, S. Vitesnik, S.-K. Leang, J. McVernon, A. Kelso, I.G. Barr, J.M. Mccaw, J.D. Bloom, and A.c. Hurt Estimating the fitness advantage conferred by permissive neuraminidase mutations in recent oseltamivir-resistant A(H1N1)pdm09 influenza viruses PLoS Pathog. 10 2014 e1004065 10.1371/journal.ppat.1004065
11. c.A. corzo, M. culhane, K. Juleen, E. Stigger-Rosser, M.F. Ducatez, R.J. Webby, and J.F. Lowe Active surveillance for influenza A virus among swine, midwestern United States, 2009-2011 Emerg. Infect. Dis. 19 2013 954 960 10.3201/eid1906.121637
12. F.S. Dawood, L. Dong, F. Liu, D.M. Blau, P.J. Peebles, X. Lu, L. Wagers, B. Oakland, M. Zielenski, R. Daly, V. Horan, S.L. Swenson, B.J. Schmitt, K. Hancock, J.M. Katz, c. Bridges, L. Kightlinger, and L. Finelli A pre-pandemic outbreak of triple-reassortant swine influenza virus infection among university students, South Dakota, 2008 J. Infect. Dis. 204 2011 1165 1171 10.1093/infdis/jir502
13. S. Duan, E.A. Govorkova, J. Bahl, H. Zaraket, T. Baranovich, P. Seiler, K. Prevost, R.G. Webster, and R.J. Webby Epistatic interactions between neuraminidase mutations facilitated the emergence of the oseltamivir-resistant H1N1 influenza viruses Nat. commun. 5 2014 5029 10.1038/ncomms6029
14. M.F. Ducatez, B. Hause, E. Stigger-Rosser, D. Darnell, c. corzo, K. Juleen, R. Simonson, c. Brockwell-Staats, A. Rubrum, D. Wang, A. Webb, J.-c. crumpton, J. Lowe, M. Gramer, and R.J. Webby Multiple reassortment between pandemic (H1N1) 2009 and endemic influenza viruses in pigs, United States Emerg. Infect. Dis. 17 2011 1624 1629 10.3201/eid1709.110338
15. Z. Feng, J.A. Baroch, L.-P. Long, Y. Xu, F.L. cunningham, K. Pedersen, M.W. Lutman, B.S. Schmit, A.S. Bowman, T.J. Deliberto, and X.-F. Wan Influenza A subtype H3 viruses in feral swine, United States, 2011-2012 Emerg. Infect. Dis. 20 2014 843 846 10.3201/eid2005.131578
16. R. Gao, B. cao, Y. Hu, Z. Feng, D. Wang, W. Hu, J. chen, Z. Jie, H. Qiu, K. Xu, X. Xu, H. Lu, W. Zhu, Z. Gao, N. Xiang, Y. Shen, Z. He, Y. Gu, Z. Zhang, Y. Yang, X. Zhao, L. Zhou, X. Li, S. Zou, Y. Zhang, X. Li, L. Yang, J. Guo, J. Dong, Q. Li, L. Dong, Y. Zhu, T. Bai, S. Wang, P. Hao, W. Yang, Y. Zhang, J. Han, H. Yu, D. Li, G.F. Gao, G. Wu, Y. Wang, Z. Yuan, and Y. Shu Human infection with a novel avian-origin influenza A (H7N9) virus N. Engl. J. Med. 368 2013 1888 1897 10.1056/NEJMoa1304459
17. R.J. Garten, c.T. Davis, c.A. Russell, B. Shu, S. Lindstrom, A. Balish, W.M. Sessions, X. Xu, E. Skepner, V. Deyde, M. Okomo-Adhiambo, L. Gubareva, J. Barnes, c.B. Smith, S.L. Emery, M.J. Hillman, P. Rivailler, J. Smagala, M. de Graaf, D.F. Burke, R.A.M. Fouchier, C. Pappas, c.M. Alpuche-Aranda, H. López-Gatell, H. Olivera, I. López, c.A. Myers, D. Faix, P.J. Blair, c. Yu, K.M. Keene, P.D. Dotson, D. Boxrud, A.R. Sambol, S.H. Abid, K. St George, T. Bannerman, A.L. Moore, D.J. Stringer, P. Blevins, G.J. Demmler-Harrison, M. Ginsberg, P. Kriner, S. Waterman, S. Smole, H.F. Guevara, E.A. Belongia, P.A. clark, S.T. Beatrice, R. Donis, J. Katz, L. Finelli, c.B. Bridges, M. Shaw, D.B. Jernigan, T.M. Uyeki, D.J. Smith, A.I. Klimov, and N.J. cox Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans Science 325 2009 197 201 10.1126/science.1176225
18. E.A. Govorkova, T. Baranovich, P. Seiler, J. Armstrong, A. Burnham, Y. Guan, M. Peiris, R.J. Webby, and R.G. Webster Antiviral resistance among highly pathogenic influenza A (H5N1) viruses isolated worldwide in 2002-2012 shows need for continued monitoring Antiviral Res. 98 2013 297 304 10.1016/j.antiviral.2013.02.013
19. R.-X. Gu, L.A. Liu, and D.-Q. Wei Structural and energetic analysis of drug inhibition of the influenza A M2 proton channel Trends Pharmacol. Sci. 34 2013 571 580 10.1016/j.tips.2013.08.003
20. F.G. Hayden Amantadine and rimantadine-clinical aspects D.D. Richman, Antiviral drug resistance 1996 John Wiley & Sons Ltd. New York, N.Y. 59 77
21. E.c. Holmes Helping the resistance Science 328 2010 1243 1244 10.1126/science.1190994
22. L.J. Holsinger, D. Nichani, L.H. Pinto, and R.A. Lamb Influenza A virus M2 ion channel protein: a structure-function analysis J. Virol. 68 1994 1551 1563
23. A.c. Hurt, S.K. Leang, D.J. Speers, I.G. Barr, and S. Maurer-Stroh Mutations I117V and I117M and oseltamivir sensitivity of pandemic (H1N1) 2009 viruses Emerg. Infect. Dis. 18 2012 109 112 10.3201/eid1801.111079
24. A.c. Hurt, P. Selleck, N. Komadina, R. Shaw, L. Brown, and I.G. Barr Susceptibility of highly pathogenic A(H5N1) avian influenza viruses to the neuraminidase inhibitors and adamantanes Antiviral Res. 73 2007 228 231 10.1016/j.antiviral.2006.10.004
25. N.A. Ilyushina, J.P. Seiler, J.E. Rehg, R.G. Webster, and E.A. Govorkova Effect of neuraminidase inhibitor-resistant mutations on pathogenicity of clade 2.2 A/Turkey/15/06 (H5N1) influenza virus in ferrets PLoS Pathog. 6 2010 e1000933 10.1371/journal.ppat.1000933
26. T. Ito, J.N. couceiro, S. Kelm, L.G. Baum, S. Krauss, M.R. castrucci, I. Donatelli, H. Kida, J.c. Paulson, R.G. Webster, and Y. Kawaoka Molecular basis for the generation in pigs of influenza A viruses with pandemic potential J. Virol. 72 1998 7367 7373
27. J.A.L. Ives, J.A. carr, D.B. Mendel, c.Y. Tai, R. Lambkin, L. Kelly, J.S. Oxford, F.G. Hayden, and N.A. Roberts The H274Y mutation in the influenza A/H1N1 neuraminidase active site following oseltamivir phosphate treatment leave virus severely compromised both in vitro and in vivo Antiviral Res. 55 2002 307 317 10.1016/S0166-3542(02)00053-0
28. A. Krumbholz, M. Schmidtke, S. Bergmann, S. Motzke, K. Bauer, J. Stech, R. Dürrwald, P. Wutzler, and R. Zell High prevalence of amantadine resistance among circulating European porcine influenza A viruses J. Gen. Virol. 90 2009 900 908 10.1099/vir.2008.007260-0
29. S. Lindstrom, R. Garten, A. Balish, B. Shu, S. Emery, L. Berman, N. Barnes, K. Sleeman, L. Gubareva, J. Villanueva, and A. Klimov Human infections with novel reassortant influenza A(H3N2)v viruses, United States, 2011 Emerg. Infect. Dis. 18 2012 834 837 10.3201/eid1805.111922
30. R.K. Nelli, S.V. Kuchipudi, G.A. White, B.B. Perez, S.P. Dunham, and K.-c. chang comparative distribution of human and avian type sialic acid influenza receptors in the pig BMc Vet. Res. 6 2010 4 10.1186/1746-6148-6-4
31. M.I. Nelson, A.L. Vincent, P. Kitikoon, E.c. Holmes, and M.R. Gramer Evolution of novel reassortant A/H3N2 influenza viruses in North American swine and humans, 2009-2011 J. Virol. 86 2012 8872 8878 10.1128/JVI.00259-12
32. c.K. Nfon, Y. Berhane, T. Hisanaga, S. Zhang, K. Handel, H. Kehler, O. Labrecque, N.S. Lewis, A.L. Vincent, J. copps, S. Alexandersen, and J. Pasick characterization of H1N1 swine influenza viruses circulating in canadian pigs in 2009 J. Virol. 85 2011 8667 8679 10.1128/JVI.00801-11
33. H.T. Nguyen, A.M. Fry, and L.V. Gubareva Neuraminidase inhibitor resistance in influenza viruses and laboratory testing methods Antivir. Ther. 17 2012 159 173 10.3851/IMP2067
34. c.W. Olsen, S. carey, L. Hinshaw, and A.I. Karasin Virologic and serologic surveillance for human, swine and avian influenza virus infections among pigs in the north-central United States Arch. Virol. 145 2000 1399 1419
35. P.N.Q. Pascua, M.-S. Song, J.H. Lee, Y.H. Baek, H. Kwon, S.-J. Park, E.H. choi, G.-J. Lim, O.-J. Lee, S.-W. Kim, c.-J. Kim, M.H. Sung, M.H. Kim, S.-W. Yoon, E.A. Govorkova, R.J. Webby, R.G. Webster, and Y.-K. choi Virulence and transmissibility of H1N2 influenza virus in ferrets imply the continuing threat of triple-reassortant swine viruses Proc. Natl. Acad. Sci. U.S.A. 109 2012 15900 15905 10.1073/pnas.1205576109
36. c. Scholtissek, H. Bürger, O. Kistner, and K.F. Shortridge The nucleoprotein as a possible major factor in determining host specificity of influenza H3N2 viruses Virology 147 1985 287 294
37. K. Sleeman, V.P. Mishin, Z. Guo, R.J. Garten, A. Balish, A.M. Fry, J. Villanueva, J. Stevens, and L.V. Gubareva Antiviral susceptibility of variant influenza A(H3N2)v viruses isolated in the United States from 2011 to 2013 Antimicrob. Agents chemother. 58 2014 2045 2051 10.1128/AAc.02556-13
38. R.B. Squires, J. Noronha, V. Hunt, A. García-Sastre, c. Macken, N. Baumgarth, D. Suarez, B.E. Pickett, Y. Zhang, c.N. Larsen, A. Ramsey, L. Zhou, S. Zaremba, S. Kumar, J. Deitrich, E. Klem, and R.H. Scheuermann Influenza research database: an integrated bioinformatics resource for influenza research and surveillance Influenza Other Respir. Viruses 6 2012 404 416 10.1111/j.1750-2659.2011.00331.x
39. T.D. Stoner, S. Krauss, R.M. DuBois, N.J. Negovetich, D.E. Stallknecht, D.A. Senne, M.R. Gramer, S. Swafford, T. DeLiberto, E.A. Govorkova, and R.G. Webster Antiviral susceptibility of avian and swine influenza virus of the N1 neuraminidase subtype J. Virol. 84 2010 9800 9809 10.1128/JVI.00296-10
40. R. Takano, M. Kiso, M. Igarashi, Q.M. Le, M. Sekijima, K. Ito, A. Takada, and Y. Kawaoka Molecular mechanisms underlying oseltamivir resistance mediated by an I117V substitution in the neuraminidase of subtype H5N1 avian influenza A viruses J. Infect. Dis. 207 2013 89 97 10.1093/infdis/jis633
41. S.c. Trock, S.A. Burke, and N.J. cox Development of an influenza virologic risk assessment tool Avian Dis. 56 2012 1058 1061
42. D. Vijaykrishna, L.L.M. Poon, H.c. Zhu, S.K. Ma, O.T.W. Li, c.L. cheung, G.J.D. Smith, J.S.M. Peiris, and Y. Guan Reassortment of pandemic H1N1/2009 influenza A virus in swine Science 328 2010 1529 10.1126/science.1189132
43. A. Vincent, L. Awada, I. Brown, H. chen, F. claes, G. Dauphin, R. Donis, M. culhane, K. Hamilton, N. Lewis, E. Mumford, T. Nguyen, S. Parchariyanon, J. Pasick, G. Pavade, A. Pereda, M. Peiris, T. Saito, S. Swenson, K. Van Reeth, R. Webby, F. Wong, and J. ciacci-Zanella Review of influenza A virus in swine worldwide: a call for increased surveillance and research Zoonoses Public Health 61 2014 4 17 10.1111/zph.12049
44. A.L. Vincent, W. Ma, K.M. Lager, B.H. Janke, and J.A. Richt Swine influenza viruses a North American perspective Adv. Virus Res. 72 2008 127 154 10.1016/S0065-3527(08)00403-X
45. J. Wang, c. Ma, J. Wang, H. Jo, B. canturk, G. Fiorin, L.H. Pinto, R.A. Lamb, M.L. Klein, and W.F. DeGrado Discovery of novel dual inhibitors of the wild-type and the most prevalent drug-resistant mutant, S31N, of the M2 proton channel from influenza A virus J. Med. chem. 56 2013 2804 2812 10.1021/jm301538e
46. J. Wang, Y. Wu, c. Ma, G. Fiorin, J. Wang, L.H. Pinto, R.A. Lamb, M.L. Klein, and W.F. Degrado Structure and inhibition of the drug-resistant S31N mutant of the M2 ion channel of influenza A virus Proc. Natl. Acad. Sci. U.S.A. 110 2013 1315 1320 10.1073/pnas.1216526110
47. T. Watanabe, S. Watanabe, H. Ito, H. Kida, and Y. Kawaoka Influenza A virus can undergo multiple cycles of replication without M2 ion channel activity J. Virol. 75 2001 5656 5662 10.1128/JVI.75.12.5656-5662.2001
48. R.J. Webby, S.L. Swenson, S.L. Krauss, P.J. Gerrish, S.M. Goyal, and R.G. Webster Evolution of swine H3N2 influenza viruses in the United States J. Virol. 74 2000 8243 8251
49. WHO 28 September 2012, vol. 87, 39 (pp. 369-380) < http://www.who.int/wer/2012/wer8739/en/ > (accessed 10.16.14).
50. WHO November 2012, Laboratory methodologies for testing the antiviral susceptibility of influenza viruses: Neuraminidase inhibitor (NAI). < http://www.who.int/influenza/gisrs