Standardizing the influenza neuraminidase inhibition assay among United States public health laboratories conducting virological surveillance

Antiviral Research

Volumn 128, Issue , 2016, Pages 28-35

  Okomo Adhiambo, M ^a   Mishin, V P ^a   Sleeman, K ^a   Saguar, E ^b   Guevara, H ^b   Reisdorf, E ^c   Griesser, R H ^c   Spackman, K J ^d   Mendenhall, M ^d   Carlos, M P ^e   Healey, B ^e   St George, K ^f   Laplante, J ^f   Aden, T ^g   Chester, S ^g   Xu, X ^a   Gubareva, L V ^a  

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

^b CALIFORNIA DEPARTMENT OF PUBLIC HEALTH   (United States)

^c WISCONSIN STATE LABORATORY OF HYGIENE   (United States)

^d Unified State Laboratories: Public Health (USLPH)   (United States)

^e MARYLAND DEPARTMENT OF HEALTH AND MENTAL HYGIENE   (United States)

^f WADSWORTH CENTER   (United States)

^g ASSOCIATION OF PUBLIC HEALTH LABORATORIES   (United States)

Author keywords

Assay standardization; Neuraminidase inhibition; Oseltamivir; Peramivir; Zanamivir

Indexed keywords

OSELTAMIVIR; PERAMIVIR; SIALIDASE INHIBITOR; VIRUS SIALIDASE; ZANAMIVIR; SIALIDASE;

ANTIVIRAL SUSCEPTIBILITY; ARTICLE; DISEASE SURVEILLANCE; ENZYME INHIBITION ASSAY; FLUORESCENCE ANALYSIS; IC50; INFLUENZA; INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H3N2); INFLUENZA B VIRUS; LABORATORY; NEURAMINIDASE INHIBITION ASSAY; PRIORITY JOURNAL; STANDARDIZATION; ANTAGONISTS AND INHIBITORS; ANTIVIRAL RESISTANCE; ENZYME ASSAY; ENZYMOLOGY; EPIDEMIOLOGICAL MONITORING; HUMAN; INFLUENZA, HUMAN; PUBLIC HEALTH SERVICE; STANDARDS; UNITED STATES;

CENTERS FOR DISEASE CONTROL AND PREVENTION (U.S.); DRUG RESISTANCE, VIRAL; ENZYME ASSAYS; EPIDEMIOLOGICAL MONITORING; HUMANS; INFLUENZA, HUMAN; INHIBITORY CONCENTRATION 50; NEURAMINIDASE; UNITED STATES;

EID: 84958211533     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2016.01.009     Document Type: Article

References (31)

1. CDC Website. Fluview http://www.cdc.gov/flu/weekly/. (accessed 09.10.15.).
2. Clinical Trials.Gov Website https://clinicaltrials.gov/show/NCT01231620. (accessed 09.10.15.).
3. V.M. Deyde, and L.V. Gubareva Influenza genome analysis using pyrosequencing method: current applications for a moving target Expert Rev. Mol. Diagn. 9 5 2009 493 509
4. V.M. Deyde, X. Xu, R.A. Bright, M. Shaw, C.B. Smith, Y. Zhang, Y. Shu, L.V. Gubareva, N.J. Cox, and A.I. Klimov Surveillance of resistance to adamantanes among influenza A(H3N2) and A(H1N1) viruses isolated worldwide J. Infect. Dis. 196 2 2007 249 257
5. 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
6. IRR Website. http://www.influenzareagentresource.org/Catalog.aspx. (accessed 09.10.15.).
7. ISIRV Antiviral Group Website. http://www.isirv.org/site/index.php/reference-panel. (accessed 30.11.15.).
8. J. McKimm-Breschkin, T. Trivedi, A. Hampson, A. Hay, A. Klimov, M. Tashiro, F. Hayden, and M. Zambon Neuraminidase sequence analysis and susceptibilities of influenza virus clinical isolates to zanamivir and oseltamivir Antimicrob. Agents Chemother. 47 7 2003 2264 2272
9. J.L. McKimm-Breschkin, and S. Barrett Neuraminidase mutations conferring resistance to laninamivir lead to faster drug binding and dissociation Antivir. Res. 114 2014 62 66
10. 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 Antivir. Res. 110 2014 31 41
11. V.P. Mishin, K. Sleeman, M. Levine, P.J. Carney, J. Stevens, and L.V. Gubareva 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
12. A.S. Monto, J.L. McKimm-Breschkin, C. Macken, A.W. Hampson, A. Hay, A. Klimov, M. Tashiro, R.G. Webster, M. Aymard, F.G. Hayden, and M. Zambon Detection of influenza viruses resistant to neuraminidase inhibitors in global surveillance during the first 3 years of their use Antimicrob. Agents Chemother. 50 7 2006 2395 2402
13. B.A. Mungall, X. Xu, and A. Klimov Surveillance of influenza isolates for susceptibility to neuraminidase inhibitors during the 2000-2002 influenza seasons Virus Res. 103 1-2 2004 195 197
14. H.T. Nguyen, T.G. Sheu, V.P. Mishin, A.I. Klimov, and L.V. Gubareva Assessment of pandemic and seasonal influenza A (H1N1) virus susceptibility to neuraminidase inhibitors in three enzyme activity inhibition assays Antimicrob. Agents. Chemother. 54 9 2010 3671 3677
15. M. Okomo-Adhiambo, A.M. Fry, S. Su, H.T. Nguyen, A.A. Elal, E. Negron, J. Hand, R.J. Garten, J. Barnes, X. Xiyan, J.M. Villanueva, L.V. Gubareva 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
16. M. Okomo-Adhiambo, H.T. Nguyen, A. Abd Elal, K. Sleeman, A. Fry, and L.V. Gubareva Drug susceptibility surveillance of influenza viruses circulating in the United States in 2011-2012: Application of WHO antiviral working group criteria Influenza Other Respir. Viruses 8 2 2014 258 265
17. M. Okomo-Adhiambo, K. Sleeman, C. Lysen, H.T. Nguyen, X. Xu, Y. Li, A.I. Klimov, and L.V. Gubareva Neuraminidase inhibitor susceptibility surveillance of influenza viruses circulating worldwide during the 2011 Southern Hemisphere season Influenza Other Respir. Viruses 7 5 2013 645 658
18. ®: when, why and how Proc. South East SAS Users Group Conference: Paper TU04 2004
19. A.K. Shetty, and L.A. Peek Peramivir for the treatment of influenza Expert Rev. Anti. Infect. Ther. 10 2 2012 123 143
20. T.G. Sheu, V.M. Deyde, M. Okomo-Adhiambo, R.J. Garten, X. Xu, R.A. Bright, E.N. Butler, T.R. Wallis, A.I. Klimov, and L.V. Gubareva Surveillance for neuraminidase inhibitor resistance among human influenza A and B viruses circulating worldwide from 2004 to 2008 Antimicrob. Agents Chemother. 52 9 2008 3284 3292
21. K. Sleeman, Z. Guo, J. Barnes, M. Shaw, J. Stevens, and L.V. Gubareva R292K substitution and drug susceptibility of influenza A(H7N9) viruses Emerg. Infect. Dis. 19 9 2013 1521 1524
22. 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 4 2014 2045 2051
23. 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
24. E. Takashita, M. Kiso, S. Fujisaki, M. Yokoyama, K. Nakamura, M. Shirakura, H. Sato, T. Odagiri, Y. Kawaoka, and M. Tashiro 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 5 2015 2607 2617
25. E. Takashita, A. Meijer, A. Lackenby, L. Gubareva, H. Rebelo-de-Andrade, T. Besselaar, A. Fry, V. Gregory, S.K. Leang, W. Huang, J. Lo, D. Pereyaslov, M.M. Siqueira, D. Wang, G.C. Mak, W. Zhang, R.S. Daniels, A.C. Hurt, and M. Tashiro Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2013-2014 Antivir. Res. 117 2015 27 38
26. D. Tamura, H. Nguyen, K. Sleeman, M. Levine, V. Mishin, H. Yang, Z. Guo, M. Okomo-Adhiambo, X. Xu, J. Stevens, and L. Gubareva Cell culture-selected substitutions in influenza A(H3N2) neuraminidase affect drug susceptibility assessment Antimicrob. Agents Chemother. 57 12 2013 6141 6146
27. M. Tisdale Monitoring of viral susceptibility: New challenges with the development of influenza NA inhibitors Rev. Med. Virol. 10 1 2000 45 55
28. Tocris Website http://www.tocris.com/molarityCalculator.php. (accessed 09.10.15.).
29. N.T. Wetherall, T. Trivedi, J. Zeller, C. Hodges-Savola, J.L. McKimm-Breschkin, M. Zambon, and F.G. Hayden Evaluation of neuraminidase enzyme assays using different substrates to measure susceptibility of influenza virus clinical isolates to neuraminidase inhibitors: Report of the neuraminidase inhibitor susceptibility network J. Clin. Microbiol. 41 2 2003 742 750
30. 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
31. M. Yamashita, T. Tomozawa, M. Kakuta, A. Tokumitsu, H. Nasu, and S. Kubo CS-8958, a prodrug of the new neuraminidase inhibitor R-125489, shows long-acting anti-influenza virus activity Antimicrob. Agents Chemother. 53 1 2009 186 192