Neuraminidase inhibitor susceptibility surveillance of influenza viruses circulating worldwide during the 2011 Southern Hemisphere season

Influenza and other Respiratory Viruses

Volumn 7, Issue 5, 2013, Pages 645-658

  Okomo Adhiambo, Margaret ^a   Sleeman, Katrina ^a   Lysén, Colleen ^a,b   Nguyen, Ha T ^a,b   Xu, Xiyan ^a   Li, Yan ^c   Klimov, Alexander I ^a   Gubareva, Larisa V ^a  

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

^b BATTELLE MEMORIAL INSTITUTE   (United States)

^c PUBLIC HEALTH AGENCY OF CANADA   (Canada)

Author keywords

Influenza; Neuraminidase inhibitor; Oseltamivir; Peramivir; Southern Hemisphere; Zanamivir

Indexed keywords

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

ANTIVIRAL SUSCEPTIBILITY; ARTICLE; DRUG SURVEILLANCE PROGRAM; INFLUENZA VIRUS A; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H3N2; INFLUENZA VIRUS B; NONHUMAN; PRIORITY JOURNAL; SOUTHERN HEMISPHERE;

INFLUENZA; NEURAMINIDASE INHIBITOR; OSELTAMIVIR; PERAMIVIR; SOUTHERN HEMISPHERE; ZANAMIVIR;

AFRICA; ANTIVIRAL AGENTS; CYCLOPENTANES; DRUG RESISTANCE, VIRAL; ENZYME INHIBITORS; GUANIDINES; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA B VIRUS; INFLUENZA, HUMAN; NEURAMINIDASE; OCEANIA; OSELTAMIVIR; SEASONS; SENTINEL SURVEILLANCE; SOUTH AMERICA; WORLD HEALTH; ZANAMIVIR;

EID: 84882611877     PISSN: 17502640     EISSN: 17502659     Source Type: Journal    
DOI: 10.1111/irv.12113     Document Type: Article

References (49)

1. Pinto LH, Lamb RA. The M2 proton channels of influenza A and B viruses. J Biol Chem 2006; 281:8997-9000.
2. CDC. High levels of adamantane resistance among influenza A (H3N2) viruses and interim guidelines for use of antiviral agents-United States, 2005-2006 influenza season. MMWR Morb Mortal Wkly Rep 2006; 55:44-46.
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 2013; 7:1-3.
7. Monto AS, McKimm-Breschkin JL, Macken C et al. Detection of influenza viruses resistant to neuraminidase inhibitors in global surveillance during the first 3 years of their use. Antimicrob Agents Chemother 2006; 50:2395-2402.
8. Mungall BA, Xu X, Klimov A. Surveillance of influenza isolates for susceptibility to neuraminidase inhibitors during the 2000-2002 influenza seasons. Virus Res 2004; 103:195-197.
9. CDC. Influenza activity-United States and worldwide, May 18-September 19, 2008. MMWR Morb Mortal Wkly Rep 2008; 57:1046-1049.
10. 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.
11. Hauge SH, Dudman S, Borgen K, Lackenby A, Hungnes O. Oseltamivir-resistant influenza viruses A (H1N1), Norway, 2007-2008. Emerg Infect Dis 2009; 15:155-162.
12. Lackenby A, Hungnes O, Dudman SG et al. Emergence of resistance to oseltamivir among influenza A(H1N1) viruses in Europe. Euro Surveill 2008; 13:pii-8026.
13. Besselaar TG, Naidoo D, Buys A et al. Widespread oseltamivir resistance in influenza A viruses (H1N1), South Africa. Emerg Infect Dis 2008; 14:1809-1810.
14. CDC. Update: influenza activity-United States, September 28, 2008-April 4, 2009, and composition of the 2009-2010 influenza vaccine. MMWR Morb Mortal Wkly Rep 2009; 58:369-374.
15. 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.
16. 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.
17. Storms AD, Gubareva LV, Su S et al. Oseltamivir-resistant pandemic (H1N1) 2009 virus infections, United States, 2010-2011. Emerg Infect Dis 2012; 18:308-311.
18. Hurt AC, Hardie K, Wilson NJ et al. Community transmission of oseltamivir-resistant A(H1N1)pdm09 influenza. N Engl J Med 2011a; 365:2541-2542.
19. 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.
20. Hope-Simpson RE. The role of season in the epidemiology of influenza. J Hyg (Lond) 1981; 86:35-47.
21. 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.
22. 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.
23. 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.
24. 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 2010a; 85:381-388.
25. Deyde VM, Gubareva LV. Influenza genome analysis using pyrosequencing method: current applications for a moving target. Expert Rev Mol Diagn 2009; 9:493-509.
26. 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.
27. 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.
28. 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.
29. 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.
30. WHO. Available at http://www.who.int/influenza/resources/documents/manual_diagnosis_surveillance_influenza/en/index.html
31. Okomo-Adhiambo M, Sleeman K, Ballenger K et al. Neuraminidase inhibitor susceptibility testing in human influenza viruses: a laboratory surveillance perspective. Viruses 2010b; 2:2269-2289.
32. Depoortere E, Mantero J, Lenglet A, Kreidl P, Coulombier D. Influenza A(H1N1)v in the southern hemisphere-lessons to learn for Europe? Euro Surveill 2009; 14:pii-19246.
33. Simonsen L. The global impact of influenza on morbidity and mortality. Vaccine 1999; 17(Suppl 1):S3-S10.
34. Finkelman BS, Viboud C, Koelle K, Ferrari MJ, Bharti N, Grenfell BT. Global patterns in seasonal activity of influenza A/H3N2, A/H1N1, and B from 1997 to 2005: viral coexistence and latitudinal gradients. PLoS ONE 2007; 2:e1296.
35. Kenah E, Chao DL, Matrajt L, Halloran ME, Longini IM Jr. The global transmission and control of influenza. PLoS ONE 2011; 6:e19515.
36. WHO. Available at http://www.who.int/influenza/vaccines/virus/recommendations/201202_recommendation.pdf
37. CDC. Available at http://www.cdc.gov/flu/weekly/
38. Yamashita M. Laninamivir and its prodrug, CS-8958: long-acting neuraminidase inhibitors for the treatment of influenza. Antivir Chem Chemother 2010; 21:71-84.
39. Tashiro M, McKimm-Breschkin JL, Saito T et al. Surveillance for neuraminidase-inhibitor-resistant influenza viruses in Japan, 1996-2007. Antivir Ther 2009; 14:751-761.
40. Hurt AC, Barr IG, Hartel G, Hampson AW. Susceptibility of human influenza viruses from Australasia and South East Asia to the neuraminidase inhibitors zanamivir and oseltamivir. Antiviral Res 2004; 62:37-45.
41. McKimm-Breschkin J, Trivedi T, Hampson A et al. Neuraminidase sequence analysis and susceptibilities of influenza virus clinical isolates to zanamivir and oseltamivir. Antimicrob Agents Chemother 2003; 47:2264-2272.
42. Hurt AC, Lee RT, Leang SK et al. 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 2011b; 16:pii-19884.
43. Rota PA, Hemphill ML, Whistler T, Regnery HL, Kendal AP. Antigenic and genetic characterization of the haemagglutinins of recent cocirculating strains of influenza B virus. J Gen Virol 1992; 73:2737-2742.
44. Rota PA, Wallis TR, Harmon MW, Rota JS, Kendal AP, Nerome K. Cocirculation of two distinct evolutionary lineages of influenza type B virus since 1983. Virology 1990; 175:59-68.
45. Xu X, Lindstrom SE, Shaw MW et al. Reassortment and evolution of current human influenza A and B viruses. Virus Res 2004; 103:55-60.
46. Higgins RR, Beniprashad M, Chong-King E et al. Recovery of influenza B Virus with the H273Y point mutation in the neuraminidase active site from a human patient. J Clin Microbiol 2012; 50:2500-2.
47. Tisdale M. Monitoring of viral susceptibility: new challenges with the development of influenza NA inhibitors. Rev Med Virol 2000; 10:45-55.
48. 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.
49. Gubareva LV, Webster RG, Hayden FG. Detection of influenza virus resistance to neuraminidase inhibitors by an enzyme inhibition assay. Antiviral Res 2002; 53:47-61.