Assays for monitoring susceptibility of influenza viruses to neuraminidase inhibitors

Influenza and other Respiratory Viruses

Volumn 7, Issue 1 SUPPL.1, 2013, Pages 44-49

  Okomo Adhiambo, Margaret ^a   Sheu, Tiffany G ^a   Gubareva, Larisa V ^a  

^a NATIONAL CENTER FOR IMMUNIZATION AND RESPIRATORY DISEASES   (United States)

Author keywords

Functional analysis; Genetic analysis; Influenza antiviral susceptibility; Neuraminidase inhibitors

Indexed keywords

LANINAMIVIR; OSELTAMIVIR; PERAMIVIR; SIALIDASE; SIALIDASE INHIBITOR; ZANAMIVIR;

ANTIVIRAL SUSCEPTIBILITY; CELL CULTURE; ENZYME INHIBITION; GENOTYPE; INFLUENZA VIRUS; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H3N2; MONITORING; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; VIRUS RESISTANCE;

ANTIVIRAL AGENTS; DRUG RESISTANCE, VIRAL; ENZYME INHIBITORS; GENOTYPE; HUMANS; INFLUENZA, HUMAN; MICROBIAL SENSITIVITY TESTS; NEURAMINIDASE; ORTHOMYXOVIRIDAE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA;

EID: 84871833332     PISSN: 17502640     EISSN: 17502659     Source Type: Journal    
DOI: 10.1111/irv.12051     Document Type: Review

References (52)

1. Bright RA, Shay DK, Shu B, Cox NJ, Klimov AI. Adamantane resistance among influenza A viruses isolated early during the 2005-2006 influenza season in the United States. JAMA 2006; 295:891-894.
2. Deyde VM, Xu X, Bright RA et al. Surveillance of resistance to adamantanes among influenza A(H3N2) and A(H1N1) viruses isolated worldwide. J Infect Dis 2007; 196:249-257.
3. Gubareva LV, Trujillo AA, Okomo-Adhiambo M et al. Comprehensive assessment of 2009 pandemic influenza A (H1N1) virus drug susceptibility in vitro. Antivir Ther 2010; 15:1151-1159.
4. Shetty AK, Peek LA. Peramivir for the treatment of influenza. Expert Rev Anti Infect Ther 2012; 10:123-143.
5. Sugaya N, Kohno S, Ishibashi T, Wajima T, Takahashi T. Efficacy, safety, and pharmacokinetics of intravenous peramivir in children with 2009 pandemic H1N1 influenza A virus infection. Antimicrob Agents Chemother 2012; 56:369-377.
6. Sunagawa S, Higa F, Cash HL, Tateyama M, Uno T, Fujita J. Single-dose inhaled laninamivir: registered in Japan and its potential role in control of influenza epidemics. Influenza Other Respi Viruses 2012; DOI: 10.1111/j.1750-2659.2012.00351.x..
7. CDC. Influenza activity - United States and worldwide, May 18-September 19, 2008. MMWR Morb Mortal Wkly Rep 2008; 57:1046-1049.
8. Lackenby A, Hungnes O, Dudman SG et al. Emergence of resistance to oseltamivir among influenza A(H1N1) viruses in Europe. Euro Surveill 2008; 13(5):8026.
9. Hauge SH, Dudman S, Borgen K, Lackenby A, Hungnes O. Oseltamivir-resistant influenza viruses A (H1N1), Norway, 2007-08. Emerg Infect Dis 2009; 15:155-162.
10. CDC. Update: influenza activity - United States, September 28, 2008-April 4, 2009, and composition of the 2009-10 influenza vaccine. MMWR Morb Mortal Wkly Rep 2009; 58:369-374.
11. Baranovich T, Saito R, Suzuki Y et al. Emergence of H274Y oseltamivir-resistant A(H1N1) influenza viruses in Japan during the 2008-2009 season. J Clin Virol 2010; 47:23-28.
12. Graitcer SB, Gubareva L, Kamimoto L et al. Characteristics of patients with oseltamivir-resistant pandemic (H1N1) 2009, United States. Emerg Infect Dis 2011; 17:255-257.
13. Storms AD, Gubareva LV, Su S et al. Oseltamivir-resistant pandemic (H1N1) 2009 virus infections, United States, 2010-11. Emerg Infect Dis 2012; 18:308-311.
14. Hurt AC, Hardie K, Wilson NJ et al. Community transmission of oseltamivir-resistant A(H1N1)pdm09 influenza. N Engl J Med 2011; 365:2541-2542.
15. Hurt AC, Hardie K, Wilson NJ et al. Characteristics of a widespread community cluster of H275Y oseltamivir-resistant A(H1N1)pdm09 influenza in Australia. J Infect Dis 2012; 206:148-157. Epub 2012 May 4.
16. Deyde VM, Gubareva LV. Influenza genome analysis using pyrosequencing method: current applications for a moving target. Expert Rev Mol Diagn 2009; 9:493-509.
17. Sheu TG, Deyde VM, Okomo-Adhiambo M et al. Surveillance for neuraminidase inhibitor resistance among human influenza A and B viruses circulating worldwide from 2004 to 2008. Antimicrob Agents Chemother 2008; 52:3284-3292.
18. Tisdale M. Monitoring of viral susceptibility: new challenges with the development of influenza NA inhibitors. Rev Med Virol 2000; 10:45-55.
19. Hurt AC, Okomo-Adhiambo M, Gubareva LV. The fluorescence neuraminidase inhibition assay: a functional method for detection of influenza virus resistance to the neuraminidase inhibitors. Methods Mol Biol 2012; 865:115-125.
20. Okomo-Adhiambo M, Hurt AC, Gubareva LV. The chemiluminescent neuraminidase inhibition assay: a functional method for detection of influenza virus resistance to the neuraminidase inhibitors. Methods Mol Biol 2012; 865:95-113.
21. Potier M, Mameli L, Belisle M, Dallaire L, Melancon SB. Fluorometric assay of neuraminidase with a sodium (4-methylumbelliferyl-alpha-D-N-acetylneuraminate) substrate. Anal Biochem 1979; 94:287-296.
22. Buxton RC, Edwards B, Juo RR, Voyta JC, Tisdale M, Bethell RC. Development of a sensitive chemiluminescent neuraminidase assay for the determination of influenza virus susceptibility to zanamivir. Anal Biochem 2000; 280:291-300.
23. Nguyen HT, Sheu TG, Mishin VP, Klimov AI, Gubareva LV. Assessment of pandemic and seasonal influenza A (H1N1) virus susceptibility to neuraminidase inhibitors in three enzyme activity inhibition assays. Antimicrob Agents Chemother 2010; 54:3671-3677.
24. Wetherall NT, Trivedi T, Zeller J et al. 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 2003; 41:742-750.
25. Okomo-Adhiambo M, Sleeman K, Ballenger K et al. Neuraminidase inhibitor susceptibility testing in human influenza viruses: a laboratory surveillance perspective. Viruses 2010; 2:2269-2289.
26. Monto AS, McKimm-Breschkin JL, Macken C et al. Detection of influenza viruses resistant to neuraminidase inhibitors in global surveillance during the first 3years of their use. Antimicrob Agents Chemother 2006; 50:2395-2402.
27. ISIRV-AVG. Available at http://www.isirv.org/site/index.php/reference-panel (Accessed 31 October 2012).
28. Hurt AC, Holien JK, Parker M, Kelso A, Barr IG. Zanamivir-resistant influenza viruses with a novel neuraminidase mutation. J Virol 2009; 83:10366-10373.
29. Okomo-Adhiambo M, Nguyen HT, Sleeman K et al. Host cell selection of influenza neuraminidase variants: implications for drug resistance monitoring in A(H1N1) viruses. Antiviral Res 2010; 85:381-388.
30. Deyde VM, Okomo-Adhiambo M, Sheu TG et al. Pyrosequencing as a tool to detect molecular markers of resistance to neuraminidase inhibitors in seasonal influenza A viruses. Antiviral Res 2009; 81:16-24.
31. Deyde VM, Sheu TG, Trujillo AA et al. Detection of molecular markers of drug resistance in 2009 pandemic influenza A (H1N1) viruses by pyrosequencing. Antimicrob Agents Chemother 2010; 54:1102-1110.
32. Sheu TG, Deyde VM, Garten RJ, Klimov AI, Gubareva LV. Detection of antiviral resistance and genetic lineage markers in influenza B virus neuraminidase using pyrosequencing. Antiviral Res 2010; 85:354-360.
33. Bao JR, Huard TK, Piscitelli AE et al. Reverse-transcription polymerase chain reaction/pyrosequencing to characterize neuraminidase H275 residue of influenza A 2009 H1N1 virus for rapid and specific detection of the viral oseltamivir resistance marker in a clinical laboratory. Diagn Microbiol Infect Dis 2011; 71:396-402.
34. Lackenby A, Democratis J, Siqueira MM, Zambon MC. Rapid quantitation of neuraminidase inhibitor drug resistance in influenza virus quasispecies. Antivir Ther 2008; 13:809-820.
35. Duan S, Boltz DA, Li J et al. Novel genotyping and quantitative analysis of neuraminidase inhibitor resistance-associated mutations in influenza a viruses by single-nucleotide polymorphism analysis. Antimicrob Agents Chemother 2011; 55:4718-4727.
36. Levine M, Sheu TG, Gubareva LV, Mishin VP. Detection of hemagglutinin variants of the pandemic influenza A (H1N1) 2009 virus by pyrosequencing. J Clin Microbiol 2011; 49:1307-1312.
37. Medina RA, Rojas M, Tuin A et al. Development and characterization of a highly specific and sensitive SYBR green reverse transcriptase PCR assay for detection of the 2009 pandemic H1N1 influenza virus on the basis of sequence signatures. J Clin Microbiol 2011; 49:335-344.
38. Wong S, Pabbaraju K, Wong A, Fonseca K, Drews SJ. Development of a real-time RT-PCR assay for detection of resistance to oseltamivir in influenza A pandemic (H1N1) 2009 virus using single nucleotide polymorphism probes. J Virol Methods 2011; 173:259-265.
39. Operario DJ, Moser MJ, St GK. Highly sensitive and quantitative detection of the H274Y oseltamivir resistance mutation in seasonal A/H1N1 influenza virus. J Clin Microbiol 2010; 48:3517-3524.
40. Renaud C, Kuypers J, Corey L. Diagnostic accuracy of an allele-specific reverse transcriptase-PCR assay targeting the H275Y oseltamivir resistant mutation in 2009 pandemic influenza A/H1N1 virus. J Clin Virol 2010; 49:21-25.
41. van der Vries E, Jonges M, Herfst S et al. Evaluation of a rapid molecular algorithm for detection of pandemic influenza A (H1N1) 2009 virus and screening for a key oseltamivir resistance (H275Y) substitution in neuraminidase. J Clin Virol 2010; 47:34-37.
42. Bolotin S, Robertson AV, Eshaghi A et al. Development of a novel real-time reverse-transcriptase PCR method for the detection of H275Y positive influenza A H1N1 isolates. J Virol Methods 2009; 158:190-194.
43. Carr MJ, Sayre N, Duffy M, Connell J, Hall WW. Rapid molecular detection of the H275Y oseltamivir resistance gene mutation in circulating influenza A (H1N1) viruses. J Virol Methods 2008; 153:257-262.
44. Tong SY, Dakh F, Hurt AC et al. Rapid detection of the H275Y oseltamivir resistance mutation in influenza A/H1N1 2009 by single base pair RT-PCR and high-resolution melting. PLoS ONE 2011; 6:e21446.
45. Lee HK, Lee CK, Loh TP, Tang JW, Tambyah PA, Koay ES. High-resolution melting approach to efficient identification and quantification of H275Y mutant influenza H1N1/2009 virus in mixed-virus-population samples. J Clin Microbiol 2011; 49:3555-3559.
46. Redlberger-Fritz M, Aberle SW, Strassl R, Popow-Kraupp T. Rapid identification of neuraminidase inhibitor resistance mutations in seasonal influenza virus A(H1N1), A(H1N1)2009, and A(H3N2) subtypes by melting point analysis. Eur J Clin Microbiol Infect Dis 2012; 31:1593-1601.
47. Whiley DM, Jacob K, Nakos J et al. Improved detection of genetic markers of antimicrobial resistance by hybridization probe-based melting curve analysis using primers to mask proximal mutations: examples include the influenza H275Y substitution. J Antimicrob Chemother 2012; 67:1375-1379.
48. Hindiyeh M, Ram D, Mandelboim M et al. Rapid detection of influenza A pandemic (H1N1) 2009 virus neuraminidase resistance mutation H275Y by real-time reverse transcriptase PCR. J Clin Microbiol 2010; 48:1884-1887.
49. Wang B, Dwyer DE, Blyth CC et al. Detection of the rapid emergence of the H275Y mutation associated with oseltamivir resistance in severe pandemic influenza virus A/H1N1 09 infections. Antiviral Res 2010; 87:16-21.
50. Steain MC, Dwyer DE, Hurt AC et al. Detection of influenza A H1N1 and H3N2 mutations conferring resistance to oseltamivir using rolling circle amplification. Antiviral Res 2009; 84:242-248.
51. Guo L, Garten RJ, Foust AS et al. Rapid identification of oseltamivir-resistant influenza A(H1N1) viruses with H274Y mutation by RT-PCR/restriction fragment length polymorphism assay. Antiviral Res 2009; 82:29-33.
52. Nukiwa N, Suzuki A, Furuse Y et al. Simplified screening method for detecting oseltamivir resistant pandemic influenza A (H1N1) 2009 virus by a RT-PCR/restriction fragment length polymorphism assay. J Virol Methods 2010; 170:165-168.