Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2013-2014

Antiviral Research

Volumn 117, Issue , 2015, Pages 27-38

  Takashita, Emi ^a   Meijer, Adam ^b   Lackenby, Angie ^c   Gubareva, Larisa ^d   Rebelo De Andrade, Helena ^e,f   Besselaar, Terry ^a   Fry, Alicia ^d   Gregory, Vicky ^a   Leang, Sook Kwan ^g   Huang, Weijuan ^a   Lo, Janice ^h   Pereyaslov, Dmitriy ^a   Siqueira, Marilda M ⁱ   Wang, Dayan ^a   Mak, Gannon C ^h   Zhang, Wenqing ^a   Daniels, Rod S ^a   Hurt, Aeron C ^g,j   Tashiro, Masato ^a  

^a WORLD HEALTH ORGANIZATION   (Switzerland)

^b NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^c PUBLIC HEALTH ENGLAND   (United Kingdom)

^d CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^e NATIONAL INSTITUTE OF HEALTH DR RICARDO JORGE   (Portugal)

^f RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

^g VICTORIAN INFECTIOUS DISEASES REFERENCE LABORATORY   (Australia)

^h Public Health Laboratory Center   (Hong Kong)

ⁱ INSTITUTO OSWALDO CRUZ   (Brazil)

^j UNIVERSITY OF MELBOURNE   (Australia)

more..

Author keywords

Antiviral resistance; Global analysis; Influenza virus; Neuraminidase inhibitors; Oseltamivir; Reduced susceptibility

Indexed keywords

LANINAMIVIR; OSELTAMIVIR; PERAMIVIR; VIRUS SIALIDASE; ZANAMIVIR; ANTIVIRUS AGENT; CYCLOPENTANE DERIVATIVE; ENZYME INHIBITOR; GUANIDINE DERIVATIVE; SIALIDASE;

AMINO ACID SUBSTITUTION; ANTIVIRAL SUSCEPTIBILITY; ARTICLE; CHINA; EPIDEMIC; EUROPE; HUMAN; IC50; INFLUENZA VIRUS; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H1N1 PDM09; INFLUENZA VIRUS A H3N2; INFLUENZA VIRUS B; JAPAN; MOLECULAR PHYLOGENY; NONHUMAN; PRIORITY JOURNAL; SEQUENCE DATABASE; UNITED STATES; VIRUS DETECTION; WESTERN HEMISPHERE; WORLD HEALTH ORGANIZATION; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; ANTIVIRAL RESISTANCE; CHEMISTRY; DRUG EFFECTS; EPIDEMIOLOGY; GENETICS; INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H3N2); INFLUENZA B VIRUS; MICROBIAL SENSITIVITY TEST; PHYLOGENY; STATISTICS AND NUMERICAL DATA; TIME;

HUMAN INFLUENZA VIRUS; ORTHOMYXOVIRIDAE;

AMINO ACID SUBSTITUTION; ANTIVIRAL AGENTS; CHINA; CYCLOPENTANES; DISEASE OUTBREAKS; DRUG RESISTANCE, VIRAL; ENZYME INHIBITORS; EUROPE; GUANIDINES; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA B VIRUS; INHIBITORY CONCENTRATION 50; JAPAN; MICROBIAL SENSITIVITY TESTS; NEURAMINIDASE; OSELTAMIVIR; PHYLOGENY; TIME FACTORS; UNITED STATES; WORLD HEALTH ORGANIZATION; ZANAMIVIR;

EID: 84924269303     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2015.02.003     Document Type: Article

References (32)

1. Y. Abed, A. Pizzorno, X. Bouhy, and G. Boivin Role of permissive neuraminidase mutations in influenza A/Brisbane/59/2007-like (H1N1) viruses PLoS Pathog. 7 12 2011 e1002431 10.1371/journal.ppat.1002431
2. Y. Abed, A. Pizzorno, X. Bouhy, C. Rhéaume, and G. Boivin Impact of potential permissive neuraminidase mutations on viral fitness of the H275Y oseltamivir-resistant influenza A(H1N1)pdm09 virus in vitro, in mice and in ferrets J. Virol. 88 3 2014 1652 1658 10.1128/JVI.02681-13
3. J.D. Bloom, L.I. Gong, and D. Baltimore Permissive secondary mutations enable the evolution of influenza oseltamivir resistance Science 328 5983 2010 1272 1275 10.1126/science.1187816
4. N.M. Bouvier, S. Rahmat, and N. Pica Enhanced mammalian transmissibility of seasonal influenza A/H1N1 viruses encoding an oseltamivir-resistant neuraminidase J. Virol. 86 13 2012 7268 7279 10.1128/JVI.07242-12
5. 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 4 2014 e1004065 10.1371/journal.ppat.1004065
6. P.J. Collins, L.F. Haire, Y.P. Lin, J. Liu, R.J. Russell, P.A. Walker, S.R. Martin, R.S. Daniels, V. Gregory, J.J. Skehel, S.J. Gamblin, and A.J. Hay Structural basis for oseltamivir resistance of influenza viruses Vaccine 27 45 2009 6317 6323 10.1016/j.vaccine.2009.07.017
7. C. Dapat, Y. Suzuki, R. Saito, Y. Kyaw, Y.Y. Myint, N. Lin, H.N. Oo, K.Y. Oo, N. Win, M. Naito, G. Hasegawa, I.C. Dapat, H. Zaraket, T. Baranovich, M. Nishikawa, T. Saito, and H. Suzuki Rare influenza A (H3N2) variants with reduced sensitivity to antiviral drugs Emerg. Infect. Dis. 16 3 2010 493 496 10.3201/eid1603.091321
8. N.J. Dharan, L.V. Gubareva, J.J. Meyer, M. Okomo-Adhiambo, R.C. McClinton, S.A. Marshall, K. St George, S. Epperson, L. Brammer, A.I. Klimov, J.S. Bresee, A.M. Fry, and Oseltamivir-Resistance Working Group Infections with oseltamivir-resistant influenza A(H1N1) virus in the United States JAMA 301 10 2009 1034 1041 10.1001/jama.2009.294
9. N.J. Dharan, L.V. Gubareva, A.I. Klimov, A.E. Fiore, J.S. Bresee, and A.M. Fry Antiviral treatment of patients with oseltamivir-resistant and oseltamivir-susceptible seasonal Influenza A (H1N1) infection during the 2007-2008 influenza season in the United States Clin. Infect. Dis. 50 4 2010 621 622 10.1086/650178
10. J. García, M. Sovero, A.L. Torres, J. Gomez, R. Douce, M. Barrantes, F. Sanchez, M. Jimenez, G. Comach, I. de Rivera, R. Agudo, and T. Kochel Antiviral resistance in influenza viruses circulating in Central and South America based on the detection of established genetic markers Influenza Other Respir. Viruses 3 2 2009 69 74 10.1111/j.1750-2659.2009.00072.x
11. S. Garg, Z. Moore, N. Lee, J. McKenna, A. Bishop, A. Fleischauer, C.B. Springs, H.T. Nguyen, T.G. Sheu, K. Sleeman, L. Finelli, L. Gubareva, and A.M. Fry A cluster of patients infected with I221V influenza B virus variants with reduced oseltamivir susceptibility-North Carolina and South Carolina, 2010-2011 J. Infect. Dis. 207 6 2013 966 973 10.1093/infdis/jis776
12. S.H. Hauge, S. Dudman, K. Borgen, A. Lackenby, and O. Hungnes Oseltamivir-resistant influenza viruses A (H1N1), Norway, 2007-08 Emerg. Infect. Dis. 15 2 2009 155 162 10.3201/eid1502.081031
13. A.C. Hurt, J. Ernest, Y.M. Deng, P. Iannello, T.G. Besselaar, C. Birch, P. Buchy, M. Chittaganpitch, S.C. Chiu, D. Dwyer, A. Guigon, B. Harrower, I.P. Kei, T. Kok, C. Lin, K. McPhie, A. Mohd, R. Olveda, T. Panayotou, W. Rawlinson, L. Scott, D. Smith, H. D'Souza, N. Komadina, R. Shaw, A. Kelso, and I.G. Barr Emergence and spread of oseltamivir-resistant A(H1N1) influenza viruses in Oceania, South East Asia and South Africa Antiviral Res. 83 1 2009 90 93 10.1016/j.antiviral.2009.03.003
14. A.C. Hurt, K. Hardie, N.J. Wilson, Y.M. Deng, M. Osbourn, S.K. Leang, R.T. Lee, P. Iannello, N. Gehrig, R. Shaw, P. Wark, N. Caldwell, R.C. Givney, L. Xue, S. Maurer-Stroh, D.E. Dwyer, B. Wang, D.W. Smith, A. Levy, R. Booy, R. Dixit, T. Merritt, A. Kelso, C. Dalton, D. Durrheim, and I.G. Barr Characteristics of a widespread community cluster of H275Y oseltamivir-resistant A(H1N1)pdm09 influenza in Australia J. Infect. Dis. 206 2 2012 148 157 10.1093/infdis/jis337
15. N. Kawai, H. Ikematsu, N. Iwaki, K. Kondou, N. Hirotsu, T. Kawashima, T. Maeda, O. Tanaka, K. Doniwa, and S. Kashiwagi Clinical effectiveness of oseltamivir for influenza A(H1N1) virus with H274Y neuraminidase mutation J. Infect. 59 3 2009 207 212 10.1016/j.jinf.2009.07.002
16. M.E. Kitler, P. Gavinio, and D. Lavanchy Influenza and the work of the World Health Organization Vaccine 15 20 Suppl. 2 2002 S5 S14
17. A. Lackenby, O. Hungnes, S.G. Dudman, A. Meijer, W.J. Paget, A.J. Hay, and M.C. Zambon Emergence of resistance to oseltamivir among influenza A(H1N1) viruses in Europe Euro Surveill. 13 5 2008 pii: 8026
18. Y. Matsuzaki, K. Mizuta, Y. Aoki, A. Suto, C. Abiko, K. Sanjoh, K. Sugawara, E. Takashita, T. Itagaki, Y. Katsushima, M. Ujike, M. Obuchi, T. Odagiri, and M. Tashiro A two-year survey of the oseltamivir-resistant influenza A(H1N1) virus in Yamagata, Japan and the clinical effectiveness of oseltamivir and zanamivir Virol. J. 5 7 2010 53 10.1186/1743-422X-7-53
19. A. Meijer, A. Lackenby, O. Hungnes, B. Lina, S. van-der-Werf, B. Schweiger, M. Opp, J. Paget, J. van-de-Kassteele, A. Hay, M. Zambon, and European Influenza Surveillance Scheme Oseltamivir-resistant influenza virus A (H1N1), Europe, 2007-08 season Emerg Infect Dis. 15 4 2009 552 560 10.3201/eid1504.181280
20. A. Meijer, H. Rebelo-de-Andrade, V. Correia, T. Besselaar, R. Drager-Dayal, A. Fry, V. Gregory, L. Gubareva, T. Kageyama, A. Lackenby, J. Lo, T. Odagiri, D. Pereyaslov, M.M. Siqueira, E. Takashita, M. Tashiro, D. Wang, S. Wong, W. Zhang, R.S. Daniels, and A.C. Hurt Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2012-2013 Antiviral Res. 110 2014 31 41 10.1016/j.antiviral.2014.07.001
21. H.T. Nguyen, A.M. Fry, P.A. Loveless, A.I. Klimov, and L.V. Gubareva Recovery of a multidrug-resistant strain of pandemic influenza A 2009 (H1N1) virus carrying a dual H275Y/I223R mutation from a child after prolonged treatment with oseltamivir Clin. Infect. Dis. 51 8 2010 983 984 10.1086/656439
22. A.J. Oakley, S. Barrett, T.S. Peat, J. Newman, V.A. Streltsov, L. Waddington, T. Saito, M. Tashiro, and J.L. McKimm-Breschkin Structural and functional basis of resistance to neuraminidase inhibitors of influenza B viruses J. Med. Chem. 53 17 2010 6421 6431 10.1021/jm100621s
23. M. Okomo-Adhiambo, A.M. Fry, S. Su, H.T. Nguyen, A.A. Elal, E. Negron, J. Hand, R.J. Garten, J. Barnes, X. Xu, J.M. Villanueva, L.V. Gubareva, and 2013-14 US Influenza Antiviral Working Group Oseltamivir-Resistant Influenza A(H1N1)pdm09 Viruses, United States, 2013-14 Emerg Infect Dis. 21 1 2015 136 141 10.3201/eid2101.141006
24. M. Potier, L. Mameli, M. Bélisle, L. Dallaire, and S.B. Melançon Fluorometric assay of neuraminidase with a sodium (4-methylumbelliferyl-alpha-D-N-acetylneuraminate) substrate Anal. Biochem. 94 2 1979 287 296
25. M.A. Rameix-Welti, S. Munier, S. Le Gal, F. Cuvelier, F. Agou, V. Enouf, N. Naffakh, and S. van der Werf Neuraminidase of 2007-2008 influenza A(H1N1) viruses shows increased affinity for sialic acids due to the D344N substitution Antivir. Ther. 16 4 2011 597 603 10.3851/IMP1804
26. R. Saito, I. Sato, Y. Suzuki, T. Baranovich, R. Matsuda, N. Ishitani, C. Dapat, I.C. Dapat, H. Zaraket, T. Oguma, and H. Suzuki Reduced effectiveness of oseltamivir in children infected with oseltamivir-resistant influenza A (H1N1) viruses with His275Tyr mutation Pediatr. Infect. Dis. J. 29 10 2010 898 904 10.1097/INF.0b013e3181de9d24
27. E. Takashita, M. Ejima, R. Itoh, M. Miura, A. Ohnishi, H. Nishimura, T. Odagiri, and M. Tashiro A community cluster of influenza A(H1N1)pdm09 virus exhibiting cross-resistance to oseltamivir and peramivir in Japan, November to December 2013 Euro Surveill. 19 1 2014 pii: 20666
28. D. Tamura, H.T. Nguyen, K. Sleeman, M. Levine, V.P. Mishin, H. Yang, Z. Guo, M. Okomo-Adhiambo, X. Xu, J. Stevens, and L.V. Gubareva Cell culture-selected substitutions in influenza A(H3N2) neuraminidase affect drug susceptibility assessment Antimicrob. Agents Chemother. 57 12 2013 6141 6146 10.1128/AAC.01364-13
29. H. Tan, K. Wei, J. Bao, and X. Zhou In silico study on multidrug resistance conferred by I223R/H275Y double mutant neuraminidase Mol. BioSyst. 9 11 2013 2764 2774 10.1039/c3mb70253g
30. M. Ujike, K. Shimabukuro, K. Mochizuki, M. Obuchi, T. Kageyama, M. Shirakura, N. Kishida, K. Yamashita, H. Horikawa, Y. Kato, N. Fujita, and M. Tashiro Odagiri T; Working Group for Influenza Virus Surveillance in Japan. Oseltamivir-resistant influenza viruses A (H1N1) during 2007-2009 influenza seasons, Japan Emerg. Infect. Dis. 16 6 2010 926 935 10.3201/eid1606.091623
31. World Health Organization Meetings of the WHO working group on surveillance of influenza antiviral susceptibility-Geneva, November 2011 and June 2012 Wkly Epidemiol. Rec. 87 39 2012 369 374
32. World Health Organization Meeting of the WHO expert working group on surveillance of influenza antiviral susceptibility, Geneva, July 2013 Wkly Epidemiol. Rec. 88 44/45 2013 477 482