Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2015–2016

Antiviral Research

Volumn 146, Issue , 2017, Pages 12-20

  Gubareva, Larisa V ^a   Besselaar, Terry G ^b   Daniels, Rod S ^c   Fry, Alicia ^a   Gregory, Vicki ^c   Huang, Weijuan ^d   Hurt, Aeron C ^e,f   Jorquera, Patricia A ^a   Lackenby, Angie ^g   Leang, Sook Kwan ^e   Lo, Janice ^h   Pereyaslov, Dmitriy ^b   Rebelo de Andrade, Helena ^i,j   Siqueira, Marilda M ^k   Takashita, Emi ^l   Odagiri, Takato ^l   Wang, Dayan ^d   Zhang, Wenqing ^b   Meijer, Adam ^m  

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

^b WORLD HEALTH ORGANIZATION   (Switzerland)

^c THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^d National Institute for Viral Disease Control and Prevention   (China)

^e PETER DOHERTY INSTITUTE FOR INFECTION AND IMMUNITY   (Australia)

^f UNIVERSITY OF MELBOURNE   (Australia)

^g PUBLIC HEALTH ENGLAND   (United Kingdom)

^h Public Health Laboratory Centre   (China)

ⁱ NATIONAL INSTITUTE OF HEALTH DR RICARDO JORGE   (Portugal)

^j RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

^k INSTITUTO OSWALDO CRUZ   (Brazil)

^l NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

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

more..

Author keywords

Inhibitor; Markers; Neuraminidase; Resistance; Surveillance; Susceptibility

Indexed keywords

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

AMINO ACID SUBSTITUTION; ANTIVIRAL SUSCEPTIBILITY; ARTICLE; HUMAN; IC50; INFLUENZA A VIRUS; INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H3N2); INFLUENZA B VIRUS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SEQUENCE DATABASE; WORLD HEALTH ORGANIZATION; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; ANTIVIRAL RESISTANCE; DRUG EFFECT; ENZYMOLOGY; EPIDEMIOLOGICAL MONITORING; GENETICS; GLOBAL HEALTH; INFLUENZA; MICROBIAL SENSITIVITY TEST; SEASON; VIROLOGY;

AMINO ACID SUBSTITUTION; ANTIVIRAL AGENTS; CYCLOPENTANES; DRUG RESISTANCE, VIRAL; ENZYME INHIBITORS; EPIDEMIOLOGICAL MONITORING; GLOBAL HEALTH; GUANIDINES; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA B VIRUS; INFLUENZA, HUMAN; INHIBITORY CONCENTRATION 50; MICROBIAL SENSITIVITY TESTS; NEURAMINIDASE; OSELTAMIVIR; SEASONS; WORLD HEALTH ORGANIZATION; ZANAMIVIR;

EID: 85027542792     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2017.08.004     Document Type: Article

References (37)

1. Baranovich, T., Vongphrachanh, P., Ketmayoon, P., Sisouk, T., Chomlasack, K., Khanthamaly, V., Nguyen, H., Mishin, V., Marjuki, H., Barnes, J., Garten, R., Stevens, J., Wentworth, D., Gubareva, L., Antiviral drug–resistant influenza B viruses carrying H134N substitution in neuraminidase, Laos, February 2016. Emerg. Infect. Dis., 23, 2017.
2. Bright, R.A., Medina, M.J., Xu, X., Perez-Oronoz, G., Wallis, T.R., Davis, X.M., Povinelli, L., Cox, N.J., Klimov, A.I., Incidence of adamantane resistance among influenza A (H3N2) viruses isolated worldwide from 1994 to 2005: a cause for concern. Lancet 366 (2005), 1175–1181.
3. Farrukee, R., Leang, S.K., Butler, J., Lee, R.T., Maurer-Stroh, S., Tilmanis, D., Sullivan, S., Mosse, J., Barr, I.G., Hurt, A.C., Influenza viruses with B/Yamagata- and B/Victoria-like neuraminidases are differentially affected by mutations that alter antiviral susceptibility. J. Antimicrob. Chemother. 70 (2015), 2004–2012.
4. FDA, The FDA Approves First Generic Version of Widely Used Influenza Drug, Tamiflu. 2016.
5. Fujisaki, S., Imai, M., Takashita, E., Taniwaki, T., Xu, H., Kishida, N., Yokoyama, M., Sato, H., Tashiro, M., Odagiri, T., Mutations at the monomer-monomer interface away from the active site of influenza B virus neuraminidase reduces susceptibility to neuraminidase inhibitor drugs. J. Infect. Chemother. 19 (2013), 891–895.
6. Fujisaki, S., Takashita, E., Yokoyama, M., Taniwaki, T., Xu, H., Kishida, N., Sato, H., Tashiro, M., Imai, M., Odagiri, T., A single E105K mutation far from the active site of influenza B virus neuraminidase contributes to reduced susceptibility to multiple neuraminidase-inhibitor drugs. Biochem. Biophys. Res. Commun. 429 (2012), 51–56.
7. Garg, S., Moore, Z., Lee, N., McKenna, J., Bishop, A., Fleischauer, A., Springs, C.B., Nguyen, H.T., Sheu, T.G., Sleeman, K., Finelli, L., Gubareva, L., Fry, A.M., 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 (2013), 966–973.
8. Garten, R.J., Davis, C.T., Russell, C.A., Shu, B., Lindstrom, S., Balish, A., Sessions, W.M., Xu, X., Skepner, E., Deyde, V., Okomo-Adhiambo, M., Gubareva, L., Barnes, J., Smith, C.B., Emery, S.L., Hillman, M.J., Rivailler, P., Smagala, J., de Graaf, M., Burke, D.F., Fouchier, R.A., Pappas, C., Alpuche-Aranda, C.M., Lopez-Gatell, H., Olivera, H., Lopez, I., Myers, C.A., Faix, D., Blair, P.J., Yu, C., Keene, K.M., Dotson, P.D. Jr., Boxrud, D., Sambol, A.R., Abid, S.H., St George, K., Bannerman, T., Moore, A.L., Stringer, D.J., Blevins, P., Demmler-Harrison, G.J., Ginsberg, M., Kriner, P., Waterman, S., Smole, S., Guevara, H.F., Belongia, E.A., Clark, P.A., Beatrice, S.T., Donis, R., Katz, J., Finelli, L., Bridges, C.B., Shaw, M., Jernigan, D.B., Uyeki, T.M., Smith, D.J., Klimov, A.I., Cox, N.J., Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325 (2009), 197–201.
9. Hooper, K.A., Bloom, J.D., A mutant influenza virus that uses an N1 neuraminidase as the receptor-binding protein. J. Virol. 87 (2013), 12531–12540.
10. Hooper, K.A., Crowe, J.E. Jr., Bloom, J.D., Influenza viruses with receptor-binding N1 neuraminidases occur sporadically in several lineages and show no attenuation in cell culture or mice. J. Virol. 89 (2015), 3737–3745.
11. Hurt, A.C., Besselaar, T.G., Daniels, R.S., Ermetal, B., Fry, A., Gubareva, L., Huang, W., Lackenby, A., Lee, R.T., Lo, J., Maurer-Stroh, S., Nguyen, H.T., Pereyaslov, D., Rebelo-de-Andrade, H., Siqueira, M.M., Takashita, E., Tashiro, M., Tilmanis, D., Wang, D., Zhang, W., Meijer, A., Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2014-2015. Antivir. Res. 132 (2016), 178–185.
12. Hurt, A.C., Lee, R.T., Leang, S.K., Cui, L., Deng, Y.M., Phuah, S.P., Caldwell, N., Freeman, K., Komadina, N., Smith, D., Speers, D., Kelso, A., Lin, R.T., Maurer-Stroh, S., Barr, I.G., Increased detection in Australia and Singapore of a novel influenza A(H1N1)2009 variant with reduced oseltamivir and zanamivir sensitivity due to a S247N neuraminidase mutation. Euro Surveill., 16, 2011.
13. Hurt, A.C., Okomo-Adhiambo, M., Gubareva, L.V., The fluorescence neuraminidase inhibition assay: a functional method for detection of influenza virus resistance to the neuraminidase inhibitors. Methods Mol. Biol. 865 (2012), 115–125.
14. Ison, M.G., Antiviral treatments. Clin. Chest Med. 38 (2017), 139–153.
15. Kawai, N., Ikematsu, H., Iwaki, N., Kondou, K., Hirotsu, N., Kawashima, T., Maeda, T., Tanaka, O., Doniwa, K., Kashiwagi, S., Clinical effectiveness of oseltamivir for influenza A(H1N1) virus with H274Y neuraminidase mutation. J. Infect. 59 (2009), 207–212.
16. Kelso, A., Hurt, A.C., The ongoing battle against influenza: drug-resistant influenza viruses: why fitness matters. Nat. Med. 18 (2012), 1470–1471.
17. Kubo, S., Tomozawa, T., Kakuta, M., Tokumitsu, A., Yamashita, M., Laninamivir prodrug CS-8958, a long-acting neuraminidase inhibitor, shows superior anti-influenza virus activity after a single administration. Antimicrob. Agents Chemother. 54 (2010), 1256–1264.
18. Leang, S.K., Kwok, S., Sullivan, S.G., Maurer-Stroh, S., Kelso, A., Barr, I.G., Hurt, A.C., Peramivir and laninamivir susceptibility of circulating influenza A and B viruses. Influenza Other Respir. Viruses 8 (2014), 135–139.
19. Little, K., Leang, S.K., Butler, J., Baas, C., Harrower, B., Mosse, J., Barr, I.G., Hurt, A.C., Zanamivir-resistant influenza viruses with Q136K or Q136R neuraminidase residue mutations can arise during MDCK cell culture creating challenges for antiviral susceptibility monitoring. Euro Surveill., 20, 2015.
20. Mandal, R.S., Panda, S., Das, S., In silico prediction of drug resistance due to S247R mutation of Influenza H1N1 neuraminidase protein. J. Biomol. Struct. Dyn., 2017, 1–43.
21. McKimm-Breschkin, J.L., Influenza neuraminidase inhibitors: antiviral action and mechanisms of resistance. Influenza Other Respir. Viruses 7:Suppl. 1 (2013), 25–36.
22. Meijer, A., Rebelo-de-Andrade, H., Correia, V., Besselaar, T., Drager-Dayal, R., Fry, A., Gregory, V., Gubareva, L., Kageyama, T., Lackenby, A., Lo, J., Odagiri, T., Pereyaslov, D., Siqueira, M.M., Takashita, E., Tashiro, M., Wang, D., Wong, S., Zhang, W., Daniels, R.S., Hurt, A.C., Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2012-2013. Antivir. Res. 110 (2014), 31–41.
23. Mishin, V.P., Sleeman, K., Levine, M., Carney, P.J., Stevens, J., Gubareva, L.V., The effect of the MDCK cell selected neuraminidase D151G mutation on the drug susceptibility assessment of influenza A(H3N2) viruses. Antivir. Res. 101 (2014), 93–96.
24. Naesens, L., Stevaert, A., Vanderlinden, E., Antiviral therapies on the horizon for influenza. Curr. Opin. Pharmacol. 30 (2016), 106–115.
25. Nelson, M.I., Simonsen, L., Viboud, C., Miller, M.A., Holmes, E.C., The origin and global emergence of adamantane resistant A/H3N2 influenza viruses. Virology 388 (2009), 270–278.
26. Nguyen, H.T., Nguyen, T., Mishin, V.P., Sleeman, K., Balish, A., Jones, J., Creanga, A., Marjuki, H., Uyeki, T.M., Nguyen, D.H., Nguyen, D.T., Do, H.T., Klimov, A.I., Davis, C.T., Gubareva, L.V., Antiviral susceptibility of highly pathogenic avian influenza A(H5N1) viruses isolated from poultry, Vietnam, 2009-2011. Emerg. Infect. Dis. 19 (2013), 1963–1971.
27. Nguyen, H.T., Trujillo, A.A., Sheu, T.G., Levine, M., Mishin, V.P., Shaw, M., Ades, E.W., Klimov, A.I., Fry, A.M., Gubareva, L.V., Analysis of influenza viruses from patients clinically suspected of infection with an oseltamivir resistant virus during the 2009 pandemic in the United States. Antivir. Res. 93 (2012), 381–386.
28. Samson, M., Abed, Y., Desrochers, F.M., Hamilton, S., Luttick, A., Tucker, S.P., Pryor, M.J., Boivin, G., Characterization of drug-resistant influenza virus A(H1N1) and A(H3N2) variants selected in vitro with laninamivir. Antimicrob. Agents Chemother. 58 (2014), 5220–5228.
29. Sheu, T.G., Deyde, V.M., Okomo-Adhiambo, M., Garten, R.J., Xu, X., Bright, R.A., Butler, E.N., Wallis, T.R., Klimov, A.I., Gubareva, L.V., Surveillance for neuraminidase inhibitor resistance among human influenza A and B viruses circulating worldwide from 2004 to 2008. Antimicrob. Agents Chemother. 52 (2008), 3284–3292.
30. Sleeman, K., Sheu, T.G., Moore, Z., Kilpatrick, S., Garg, S., Fry, A.M., Gubareva, L.V., Influenza B viruses with mutation in the neuraminidase active site, North Carolina, USA, 2010-11. Emerg. Infect. Dis. 17 (2011), 2043–2046.
31. Takashita, E., Fujisaki, S., Shirakura, M., Nakamura, K., Kishida, N., Kuwahara, T., Shimazu, Y., Shimomura, T., Watanabe, S., Odagiri, T., Influenza Virus Surveillance Group of, J. Influenza A(H1N1)pdm09 virus exhibiting enhanced cross-resistance to oseltamivir and peramivir due to a dual H275Y/G147R substitution, Japan, March 2016. Euro Surveill., 21, 2016.
32. Takashita, E., Kiso, M., Fujisaki, S., Yokoyama, M., Nakamura, K., Shirakura, M., Sato, H., Odagiri, T., Kawaoka, Y., Tashiro, M., Characterization of a large cluster of influenza A(H1N1)pdm09 viruses cross-resistant to oseltamivir and peramivir during the 2013-2014 influenza season in Japan. Antimicrob. Agents Chemother. 59 (2015), 2607–2617.
33. Takashita, E., Meijer, A., Lackenby, A., Gubareva, L., Rebelo-de-Andrade, H., Besselaar, T., Fry, A., Gregory, V., Leang, S.K., Huang, W., Lo, J., Pereyaslov, D., Siqueira, M.M., Wang, D., Mak, G.C., Zhang, W., Daniels, R.S., Hurt, A.C., Tashiro, M., Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2013-2014. Antivir. Res. 117 (2015), 27–38.
34. Van der Vries, E., Collins, P.J., Vachieri, S.G., Xiong, X., Liu, J., Walker, P.A., Haire, L.F., Hay, A.J., Schutten, M., Osterhaus, A.D., Martin, S.R., Boucher, C.A., Skehel, J.J., Gamblin, S.J., H1N1 2009 pandemic influenza virus: resistance of the I223R neuraminidase mutant explained by kinetic and structural analysis. PLoS Pathog., 8, 2012, e1002914.
35. WHO, Meetings of the WHO working group on surveillance of influenza antiviral susceptibility - Geneva, November 2011 and June 2012. Wkly. Epidemiol. Rec. 87 (2012), 369–374.
36. World Health Organization, Manual for the Laboratory Diagnosis and Virological Surveillance of Influenza. 2011, World Health Organization, Geneva.
37. Zhong, J., Liang, L., Huang, P., Zhu, X., Zou, L., Yu, S., Zhang, X., Zhang, Y., Ni, H., Yan, J., Genetic mutations in influenza H3N2 viruses from a 2012 epidemic in Southern China. Virol. J., 10, 2013, 345.