Neuraminidase inhibitor resistance in influenza viruses and laboratory testing methods

Antiviral Therapy

Volumn 17, Issue 1 PART B, 2012, Pages 159-173

  Nguyen, Ha T ^a,b,c   Fry, Alicia M ^a   Gubareva, Larisa V ^a  

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

^b ATLANTA RESEARCH AND EDUCATION FOUNDATION   (United States)

^c BATTELLE MEMORIAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

A 315675; ADAMANTANE DERIVATIVE; INFLUENZA VACCINE; LANINAMIVIR; N ACETYLNEURAMINIC ACID; OSELTAMIVIR; PERAMIVIR; SIALIDASE INHIBITOR; UNCLASSIFIED DRUG; VIRUS SIALIDASE; ZANAMIVIR;

2009 H1N1 INFLUENZA; AMINO ACID SUBSTITUTION; ANTIVIRAL RESISTANCE; ANTIVIRAL SUSCEPTIBILITY; AVIAN INFLUENZA; CELL CULTURE; CHEMOLUMINESCENCE; CROSS RESISTANCE; DRUG STRUCTURE; FLUORESCENCE ANALYSIS; GENETIC REASSORTMENT; GENOTYPE; HOSPITAL INFECTION; HUMAN; INFECTION CONTROL; INFLUENZA; INFLUENZA A (H1N1); INFLUENZA A (H3N2); INFLUENZA VIRUS; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H3N2; LABORATORY TEST; MEDICAL DECISION MAKING; NONHUMAN; PANDEMIC INFLUENZA; PATIENT MONITORING; PRIORITY JOURNAL; PUBLIC HEALTH SERVICE; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SEASONAL INFLUENZA; VIRUS MUTATION; VIRUS TRANSMISSION; VIRUS VIRULENCE;

ANTIVIRAL AGENTS; DRUG RESISTANCE, VIRAL; HUMANS; INFLUENZA, HUMAN; NEURAMINIDASE; ORTHOMYXOVIRIDAE; PANDEMICS;

EID: 84860334106     PISSN: 13596535     EISSN: None     Source Type: Journal    
DOI: 10.3851/IMP2067     Document Type: Review

References (135)

1. Bright RA, Medina MJ, Xu X, et al. Incidence of adamantane resistance among influenza A (H3N2) viruses isolated worldwide from 1994 to 2005: a cause for concern. Lancet 2005; 366:1175-1181. (Pubitemid 41393595)
2. World Health Organization. Influenza A(H1N1) virus resistance to oseltamivir - 2008/2009 influenza season, northern hemisphere, 18 March 2009. (Accessed 21 August 2011.) Available from http://www.who.int/influenza/ resources/documents/H1N1webupdate20090318-ed-ns.pdf
3. Dharan NJ, Gubareva LV, Meyer JJ, et al. Infections with oseltamivir-resistant influenza A(H1N1) virus in the United States. JAMA 2009; 301:1034-1041.
4. Novel Swine-Origin Influenza 1 (H1N1) Virus Investigation Team. Emergence of a novel swine-origin influenza A (H1N1) virus in humans. N Engl J Med 2009; 360:2605-2615.
5. Escuret V, Frobert E, Bouscambert-Duchamp M, et al. Detection of human influenza A (H1N1) and B strains with reduced sensitivity to neuraminidase inhibitors. J Clin Virol 2008; 41:25-28.
6. Reece PA. Neuraminidase inhibitor resistance in influenza viruses. J Med Virol 2007; 79:1577-1586. (Pubitemid 47328747)
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. (Pubitemid 43993177)
8. World Health Organization. Influenza A virus resistance to oseltamivir and other antiviral medicines. 2010. (Accessed 21 August 2011.) Available from http://www.who.int/csr/disease/influenza/2008-9nhemisummaryreport/en/index.html
9. Sheu TG, Fry AM, Garten RJ, et al. Dual resistance to adamantanes and oseltamivir among seasonal influenza A(H1N1) viruses: 2008-2010. J Infect Dis 2011; 203:13-17.
10. Zhou J, Zou L, Zhang X, et al. Adamantane- and oseltamivirresistant seasonal A(H1N1) and pandemic A(H1N1) 2009 influenza viruses in Guangdong, China, during 2008 and 2009. J Clin Microbiol 2011; 49:2651-2655.
11. World Health Organization. Number of specimens positive for influenza by subtypes from week no. 17 (2009) to 21 (2010). (Accessed 21 August 2011.) Available from http://www.who.int/csr/disease/swineflu/Virologicaldata2010-06- 11.pdf
12. Garten RJ, Davis CT, Russell CA, et al. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 2009; 325:197-201.
13. Pada S, Tambyah PA. Overview/reflections on the 2009 H1N1 pandemic. Microbes Infect 2011; 13:470-478.
14. Centers for Disease Control and Prevention. High levels of resistance to the adamantanes (amantadine and rimantadine) persist among 2009 influenza A (H1N1) and A (H3N2) viruses currently circulating. MMWR Morb Mortal Wkly Rep 2011; 60:175-181.
15. Gamblin SJ, Skehel JJ. Influenza hemagglutinin and neuraminidase membrane glycoproteins. J Biol Chem 2010; 285:28403-28409.
16. Wagner R, Matrosovich M, Klenk HD. Functional balance between haemagglutinin and neuraminidase in influenza virus infections. Rev Med Virol 2002; 12:159-166. (Pubitemid 34516947)
17. Gubareva LV. Molecular mechanisms of influenza virus resistance to neuraminidase inhibitors. Virus Res 2004; 103:199-203. (Pubitemid 38649080)
18. McKimm-Breschkin JL, Sahasrabudhe A, Blick TJ, et al. Mutations in a conserved residue in the influenza virus neuraminidase active site decreases sensitivity to Neu5Ac2en-derived inhibitors. J Virol 1998; 72:2456-2462. (Pubitemid 28100807)
19. McKimm-Breschkin JL, McDonald M, Blick TJ, et al. Mutation in the influenza virus neuraminidase gene resulting in decreased sensitivity to the neuraminidase inhibitor 4-guanidino-Neu5Ac2en leads to instability of the enzyme. Virology 1996; 225:240-242. (Pubitemid 26390073)
20. Yang JR, Lin YC, Huang YP, et al. Reassortment and mutations associated with emergence and spread of oseltamivir-resistant seasonal influenza A/H1N1 viruses in 2005-2009. PLoS ONE 2011; 6:e18177.
21. Bloom JD, Gong LI, Baltimore D. Permissive secondary mutations enable the evolution of influenza oseltamivir resistance. Science 2010; 328:1272-1275.
22. Rameix-Welti MA, Munier S, Le Gal S, et al. Neuraminidase of 2007-2008 influenza A(H1N1) viruses shows increased affinity for sialic acids due to the D344N substitution. Antivir Ther 2011; 16:597-603.
23. 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.
24. 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.
25. Writing Committee of the WHO Consultation on Clinical Aspectsof Pandemic (H1N1) 2009. Influenza clinical aspects of pandemic 2009 influenza A (H1N1) virus infection. N Engl J Med 2010; 362:1708-1719.
26. Centers for Disease Control and Prevention. Update: drug susceptibility of swine-origin influenza A (H1N1) viruses, April 2009. MMWR Morb Mortal Wkly Rep 2009; 58:433-435.
27. World Health Organization. Weekly update on oseltamivir resistance of influenza A (H1N1) 2009 virus 01 June 2011. (Accessed 21 August 2011.) Available from http://www.who.int/csr/disease/influenza/2011-06-03-weekly-web-update- oseltamivir-resistance.pdf
28. Centers for Disease Control and Prevention. Update: influenza activity - United States, 2010-11 season, and composition of the 2011-12 influenza vaccine. MMWR Morb Mortal Wkly Rep 2011; 60:705-712.
29. Euroflu. Europe influenza surveillance (week 5: 31/01/2011-06/02/2011). (Accessed 21 August 2011.) Available from http://www.euroflu.org/cgi-files/ bulletin-v2.cgi?display=1&code=388&bulletin=388
30. World Health Organization. Review of the 2010-2011 winter influenza season, northern hemisphere. Wkly Epidemiol Rec 2011; 86:222-227.
31. Le QM, Wertheim HF, Tran ND, et al. A community cluster of oseltamivir-resistant cases of 2009 H1N1 influenza. N Engl J Med 2010; 362:86-87.
32. Centers for Disease Control and Prevention. Oseltamivir-Resistant 2009 Pandemic influenza A (H1N1) virus infection in two summer campers receiving prophylaxis - North Carolina, 2009. MMWR Morb Mortal Wkly Rep 2009; 58:969-972.
33. Chen LF, Dailey NJ, Rao AK, et al. Cluster of oseltamivirresistant 2009 pandemic influenza A (H1N1) virus infections on a hospital ward among immunocompromised patients - North Carolina, 2009. J Infect Dis 2011; 203:838-846.
34. Mandelboim M, Hindiyeh M, Meningher T, et al. Possible transmission of pandemic (HIN1) 2009 virus with oseltamivir resistance. Emerg Infect Dis 2010; 16:873-874.
35. Moore C, Galiano M, Lackenby A, et al. Evidence of person-to-person transmission of oseltamivir-resistant pandemic influenza A(H1N1) 2009 virus in a hematology unit. J Infect Dis 2011; 203:18-24.
36. Wolfe C, Greenwald I, Chen L. Pandemic (H1N1) 2009 and oseltamivir resistance in hematology/oncology patients. Emerg Infect Dis 2010; 16:1809-1811.
37. Lackenby A, Moran Gilad J, Pebody R, et al. Continued emergence and changing epidemiology of oseltamivirresistant influenza A(H1N1) 2009 virus, United Kingdom, winter 2010/11. Euro Surveill 2011; 16: pii 19784.
38. European Centre for Disease Prevention and Control. Rapid risk assessment: oseltamivir-resistant influenza A(H1N1)2009 cluster in Australia. Technical reports - 06 September 2011. (Accessed 20 September 2011.) Available from http://ecdc.europa.eu/en/publications/Publications/110906-TER-Rapid-Risk- Assessment-Oseltamivir-resistant%20influenza%20A.pdf
39. Hatakeyama S, Sugaya N, Ito M, et al. Emergence of influenza B viruses with reduced sensitivity to neuraminidase inhibitors. JAMA 2007; 297:1435-1442. (Pubitemid 46556469)
40. Stephenson I, Democratis J, Lackenby A, et al. Neuraminidase inhibitor resistance after oseltamivir treatment of acute influenza A and B in children. Clin Infect Dis 2009; 48:389-396.
41. 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. (Pubitemid 38649079)
42. Hurt AC, Holien JK, Parker MW, et al. Oseltamivir resistance and the H274Y neuraminidase mutation in seasonal, pandemic and highly pathogenic influenza viruses. Drugs 2009; 69:2523-2531.
43. Lackenby A, Democratis J, Siqueira MM, et al. Rapid quantitation of neuraminidase inhibitor drug resistance in influenza virus quasispecies. Antivir Ther 2008; 13:809-820.
44. Ferraris O, Lina B. Mutations of neuraminidase implicated in neuraminidase inhibitors resistance. J Clin Virol 2008; 41:13-19. (Pubitemid 350298978)
45. 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.
46. Abed Y, Baz M, Boivin G. Impact of neuraminidase mutations conferring influenza resistance to neuraminidase inhibitors in the N1 and N2 genetic backgrounds. Antivir Ther 2006; 11:971-976. (Pubitemid 44955172)
47. Hurt AC, Holien JK, Barr IG. In vitro generation of neuraminidase inhibitor resistance in A(H5N1) influenza viruses. Antimicrob Agents Chemother 2009; 53:4433-4440.
48. Zürcher T, Yates PJ, Daly J, et al. Mutations conferring zanamivir resistance in human influenza virus N2 neuraminidases compromise virus fitness and are not stably maintained in vitro. J Antimicrob Chemother 2006; 58:723-732. (Pubitemid 44390944)
49. Gubareva LV, Robinson MJ, Bethell RC, et al. Catalytic and framework mutations in the neuraminidase active site of influenza viruses that are resistant to 4-guanidino-Neu5Ac2en. J Virol 1997; 71:3385-3390. (Pubitemid 27172346)
50. Gubareva LV, Bethell R, Hart GJ, et al. Characterization of mutants of influenza A virus selected with the neuraminidase inhibitor 4-guanidino- Neu5Ac2en. J Virol 1996; 70:1818-1827. (Pubitemid 26062945)
51. Thorlund K, Awad T, Boivin G, et al. Systematic review of influenza resistance to the neuraminidase inhibitors. BMC Infect Dis 2011; 11:134.
52. Moss RB, Davey RT, Steigbigel RT, et al. Targeting pandemic influenza: a primer on influenza antivirals and drug resistance. J Antimicrob Chemother 2010; 65:1086-1093.
53. 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.
54. Hurt AC, Holien JK, Parker M, et al. Zanamivir-resistant influenza viruses with a novel neuraminidase mutation. J Virol 2009; 83:10366-10373.
55. Dapat C, Suzuki Y, Saito R, et al. Rare influenza A (H3N2) variants with reduced sensitivity to antiviral drugs. Emerg Infect Dis 2010; 16:493-496.
56. Okomo-Adhiambo M, Demmler-Harrison GJ, Deyde VM, et al. Detection of E119V and E119I mutations in influenza A (H3N2) viruses isolated from an immunocompromised patient: challenges in diagnosis of oseltamivir resistance. Antimicrob Agents Chemother 2010; 54:1834-1841.
57. Gubareva LV, Matrosovich MN, Brenner MK, et al. Evidence for zanamivir resistance in an immunocompromised child infected with influenza B virus. J Infect Dis 1998; 178:1257-1262.
58. Tamura D, Sugaya N, Ozawa M, et al. Frequency of drug-resistant viruses and virus shedding in pediatric influenza patients treated with neuraminidase inhibitors. Clin Infect Dis 2011; 52:432-437.
59. Boltz DA, Douangngeun B, Phommachanh P, et al. Emergence of H5N1 avian influenza viruses with reduced sensitivity to neuraminidase inhibitors and novel reassortants in Lao People's Democratic Republic. J Gen Virol 2010; 91:949-959.
60. Carr S, Ilyushina NA, Franks J, et al. Oseltamivir-resistant influenza A and B viruses pre- and postantiviral therapy in children and young adults with cancer. Pediatr Infect Dis J 2011; 30:284-288.
61. 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 2011; 16: pii 19884.
62. 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. (Pubitemid 36753582)
63. 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.
64. Ghedin E, Laplante J, DePasse J, et al. Deep sequencing reveals mixed infection with 2009 pandemic influenza A (H1N1) virus strains and the emergence of oseltamivir resistance. J Infect Dis 2011; 203:168-174.
65. Gubareva L, Nguyen H, Sleeman K, et al. Comprehensive assessment of the drug susceptibility of 2009 H1N1 influenza viruses. Options for the Control of Influenza VII. 3-7 September 2010, Hong Kong SAR, China. Abstract O-821.
66. Colman PM. New Antivirals and Drug Resistance. Annu Rev Biochem 2009; 78:95-118.
67. Cooper NJ, Sutton AJ, Abrams KR, et al. Effectiveness of neuraminidase inhibitors in treatment and prevention of influenza A and B: systematic review and meta-analyses of randomised controlled trials. BMJ 2003; 326:1235.
68. Nguyen HT, Sheu TG, Mishin VP, et al. 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.
69. Pizzorno A, Bouhy X, Abed Y, et al. Generation and characterization of recombinant pandemic influenza A(H1N1) viruses resistant to neuraminidase inhibitors. J Infect Dis 2011; 203:25-31.
70. Jackson D, Barclay W, Zurcher T, et al. Characterisation of recombinant influenza B viruses with key neuraminidase inhibitor resistance mutations. J Antimicrob Chemother 2005; 55:162-169. (Pubitemid 40331140)
71. Hurt AC, Iannello P, Jachno K, et al. Neuraminidase inhibitor-resistant and -sensitive influenza B viruses isolated from an untreated human patient. Antimicrob Agents Chemother 2006; 50:1872-1874.
72. Ison MG, Gubareva LV, Atmar RL, et al. Recovery of drug-resistant influenza virus from immunocompromised patients: a case series. J Infect Dis 2006; 193:760-764.
73. Birnkrant D, Cox E. The emergency use authorization of peramivir for treatment of 2009 H1N1 influenza. N Engl J Med 2009; 361:2204-2207.
74. Baz M, Abed Y, Boivin G. Characterization of drug-resistant recombinant influenza A/H1N1 viruses selected in vitro with peramivir and zanamivir. Antiviral Res 2007; 74:159-162. (Pubitemid 46436166)
75. Le QM, Kiso M, Someya K, et al. Avian flu: isolation of drug-resistant H5N1 virus. Nature 2005; 437:1108. (Pubitemid 41509341)
76. Memoli MJ, Hrabal RJ, Hassantoufighi A, et al. Rapid selection of oseltamivir- and peramivir-resistant pandemic H1N1 virus during therapy in 2 immunocompromised hosts. Clin Infect Dis 2010; 50:1252-1255.
77. Babu YS, Chand P, Bantia S, et al. BCX-1812 (RWJ-270201): discovery of a novel, highly potent, orally active, and selective influenza neuraminidase inhibitor through structure-based drug design. J Med Chem 2000; 43:3482-3486.
78. World Health Organization. Antiviral resistance during the 2009 influenza A H1N1 pandemic: public health, laboratory, and clinical perspectives. Lanet Infect Dis 2011; doi: 10.1016/S1473-3099(11)70318-8.
79. Gaur AH, Bagga B, Barman S, et al. Intravenous zanamivir for oseltamivir-resistant 2009 H1N1 influenza. N Engl J Med 2010; 362:88-89.
80. Nguyen HT, Fry AM, Loveless PA, et al. 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 2010; 51:983-984.
81. van der Vries E, Stelma FF, Boucher CA. Emergence of a multidrug-resistant pandemic influenza A (H1N1) virus. N Engl J Med 2010; 363:1381-1382.
82. Eshaghi A, Patel SN, Sarabia A, et al. Multidrug-resistant pandemic (H1N1) 2009 infection in immunocompetent child. Emerg Infect Dis 2011; 17:1472-1474.
83. Baz M, Abed Y, McDonald J, et al. Characterization of multidrug-resistant influenza A/H3N2 viruses shed during 1 year by an immunocompromised child. Clin Infect Dis 2006; 43:1555-1561. (Pubitemid 44901897)
84. Sleeman K, Sheu TG, Moore Z, et al. Influenza B viruses with the I221V substitution in the neuraminidase active site, North Carolina, 2010-2011 influenza season. Emerg Infect Dis 2011; 17:2043-2046.
85. Richard M, Ferraris O, Erny A, et al. Combinatorial effect of two E119V+I222L framework mutations in the neuraminidase active site of H3N2 influenza virus on resistance to oseltamivir. Antimicrob Agents Chemother 2011; 55:2942-2952.
86. Le Goff J, Rousset D, Abou-Jaoude G, et al. Emergence of cross-resistance to oseltamivir and zanamivir in pandemic influenza A (H1N1) 2009 virus. 50th Interscience Conference on Antimicrobials and Chemotherapy. 12-15 September 2010, Boston, MA, USA. Poster V-448d.
87. Rousset D, Le Goff J, Abou-Jaoude G, et al. Emergence of successive mutations in the neuraminidase of the pandemic H1N1 virus respectively associated with oseltamivir resistance and reduced susceptibility to both oseltamivir and zanamivir under treatment with neuraminidase inhibitors. Options for the Control of Influenza VII. 3-7 September 2010, Hong Kong SAR, China. Abstract P-198.
88. Takashita E, Ujike M, Ejima M, et al. Detection and characterization of oseltamivir-resistant pandemic influenza A/H1N1 2009 viruses in the 2009/10 season in Japan. Options for the Control of Influenza VII. 3-7 September 2010, Hong Kong SAR, China. Abstract P-175.
89. Santos L, Correia V, Giria M, et al. Genetic and antiviral drug susceptbility profiles of pandemic A(H1N1)v influenza virus circulating in Portugal. Options for the Control of Influenza VII. 3-7 September 2010, Hong Kong SAR, China. Abstract O-851.
90. Simon P, Holder BP, Bouhy X, et al. The I222V neuraminidase mutation has a compensatory role in replication of an oseltamivir-resistant influenza virus A/H3N2 E119V mutant. J Clin Microbiol 2011; 49:715-717.
91. Bouvier NM, Lowen AC, Palese P. Oseltamivir-resistant influenza A viruses are transmitted efficiently among guinea pigs by direct contact but not by aerosol. J Virol 2008; 82:10052-10058.
92. Simonsen L, Viboud C, Grenfell BT, et al. The genesis and spread of reassortment human influenza A/H3N2 viruses conferring adamantane resistance. Mol Biol Evol 2007; 24:1811-1820. (Pubitemid 47236702)
93. Hayden FG, de Jong MD. Emerging influenza antiviral resistance threats. J Infect Dis 2011; 203:6-10.
94. Peacey M, Hall RJ, Sonnberg S, et al. Pandemic (H1N1) 2009 and seasonal influenza A(H1N1) co-infection, New Zealand, 2009. Emerg Infect Dis 2010; 16:1618-1620.
95. Aoki FY, Boivin G, Roberts N. Influenza virus susceptibility and resistance to oseltamivir. Antivir Ther 2007; 12:603-616. (Pubitemid 47235503)
96. Baz M, Abed Y, Simon P, et al. Effect of the neuraminidase mutation H274Y conferring resistance to oseltamivir on the replicative capacity and virulence of old and recent human influenza A(H1N1) viruses. J Infect Dis 2010; 201:740-745.
97. Tramontana AR, George B, Hurt AC, et al. Oseltamivir resistance in adult oncology and hematology patients infected with pandemic (H1N1) 2009 virus, Australia. Emerg Infect Dis 2010; 16:1068-1075.
98. Tang JW, Shetty N, Lam TT. Features of the new pandemic influenza A/H1N1/2009 virus: virology, epidemiology, clinical and public health aspects. Curr Opin Pulm Med 2010; 16:235-241.
99. Valinotto LE, Diez RA, Barrero PR, et al. Emergence of intratreatment resistance to oseltamivir in pandemic influenza A H1N1 2009 virus. Antivir Ther 2010; 15:923-927.
100. Nguyen HT, Trujillo AA, Sheu TG, et al. Analysis of influenza viruses from patients clinically suspected of infection with an oseltamivir resistant virus during the 2009 pandemic in the United States. Antiviral Res 2012; doi:10.1016/j.antiviral.2012.01.006.
101. Renaud C, Boudreault AA, Kuypers J, et al. H275Y mutant pandemic (H1N1) 2009 virus in immunocompromised patients. Emerg Infect Dis 2011; 17:653-660.
102. Campanini G, Piralla A, Rovida F, et al. First case in Italy of acquired resistance to oseltamivir in an immunocompromised patient with influenza A/H1N1v infection. J Clin Virol 2010; 48:220-222.
103. Brookes DW, Miah S, Lackenby A, et al. Pandemic H1N1 2009 influenza virus with the H275Y oseltamivir resistance neuraminidase mutation shows a small compromise in enzyme activity and viral fitness. J Antimicrob Chemother 2011; 66:466-470.
104. Duan S, Boltz DA, Seiler P, et al. Oseltamivir-resistant pandemic H1N1/2009 influenza virus possesses lower transmissibility and fitness in ferrets. PLoS Pathog 2010; 6:e1001022.
105. Hamelin ME, Baz M, Abed Y, et al. Oseltamivir-resistant pandemic A/H1N1 virus is as virulent as its wild-type counterpart in mice and ferrets. PLoS Pathog 2010;6:e1001015.
106. Kiso M, Shinya K, Shimojima M, et al. Characterization of oseltamivir-resistant 2009 H1N1 pandemic influenza A viruses. PLoS Pathog 2010; 6:e1001079.
107. Yang JR, Huang YP, Lin YC, et al. Early findings of oseltamivir-resistant pandemic (H1N1) 2009 influenza A viruses in Taiwan. Antiviral Res 2010; 88:256-262.
108. Memoli MJ, Davis AS, Proudfoot K, et al. Multidrug-resistant 2009 pandemic influenza A(H1N1) viruses maintain fitness and transmissibility in ferrets. J Infect Dis 2011; 203:348-357.
109. Seibert CW, Kaminski M, Philipp J, et al. Oseltamivir-resistant variants of the 2009 pandemic H1N1 influenza A virus are not attenuated in the guinea pig and ferret transmission models. J Virol 2010; 84:11219-11226.
110. Gerloff NA, Kremer JR, Mossong J, et al. Genomic diversity of oseltamivir-resistant influenza virus A (H1N1), Luxembourg, 2007-08. Emerg Infect Dis 2009; 15:1523-1524.
111. Inoue M, Barkham T, Leo YS, et al. Emergence of oseltamivir-resistant pandemic (H1N1) 2009 virus within 48 hours. Emerg Infect Dis 2010; 16:1633-1636.
112. Gubareva LV, Fry AM. Current challenges in the risk assessment of neuraminidase inhibitor-resistant influenza viruses. J Infect Dis 2010; 201:656-658.
113. Memoli MJ, Hrabal RJ, Hassantoufighi A, et al. Rapid selection of a transmissible multidrug-resistant influenza A/H3N2 virus in an immunocompromised host. J Infect Dis 2010; 201:1397-1403.
114. Yen HL, Herlocher LM, Hoffmann E, et al. Neuraminidase inhibitor-resistant influenza viruses may differ substantially in fitness and transmissibility. Antimicrob Agents Chemother 2005; 49:4075-4084. (Pubitemid 41400949)
115. Tisdale M, Daly J, Gor D. Methods for determining resistance to neuraminidase inhibitors. Int Congr Ser 2001; 1219:879-886.
116. Okomo-Adhiambo M, Ballenger K, Nguyen HT, et al. Neuraminidase Inhibitor Susceptibility Testing in Human Influenza Viruses: A Laboratory Surveillance Perspective. Viruses 2010; 2:2269-2289.
117. Deyde VM, Gubareva LV. Influenza genome analysis using pyrosequencing method: current applications for a moving target. Expert Rev Mol Diagn 2009; 9:493-509.
118. Kawai N, Ikematsu H, Hirotsu N, et al. Clinical effectiveness of oseltamivir and zanamivir for treatment of influenza A virus subtype H1N1 with the H274Y mutation: a Japanese, multicenter study of the 2007-2008 and 2008-2009 influenza seasons. Clin Infect Dis 2009; 49:1828-1835.
119. Kawai N, Ikematsu H, Iwaki N, et al. Clinical effectiveness of oseltamivir for influenza A(H1N1) virus with H274Y neuraminidase mutation. J Infect 2009; 59:207-212.
120. Dharan NJ, Gubareva LV, Klimov AI, et al. 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 2010; 50:621-622.
121. Chidlow GR, Harnett GB, Williams SH, et al. The detection of oseltamivir-resistant pandemic influenza A/H1N1 2009 viruses using a real-time RT-PCR assay. J Virol Methods 2010; 169:47-51.
122. Operario DJ, Moser MJ, St George K. Highly sensitive and quantitative detection of the H274Y oseltamivir resistance mutation in seasonal A/H1N1 influenza virus. J Clin Microbiol 2010; 48:3517-3524.
123. Deng YM, Caldwell N, Hurt A, et al. A comparison of pyrosequencing and neuraminidase inhibition assays for the detection of oseltamivir-resistant pandemic influenza A(H1N1) 2009 viruses. Antiviral Res 2011; 90:87-91.
124. McCullers JA, Wang GC, He S, et al. Reassortment and insertion-deletion are strategies for the evolution of influenza B viruses in nature. J Virol 1999; 73:7343-7348. (Pubitemid 29383217)
125. Colman PM, Hoyne PA, Lawrence MC. Sequence and structure alignment of paramyxovirus hemagglutinin-neuraminidase with influenza virus neuraminidase. J Virol 1993; 67:2972-2980. (Pubitemid 23143664)
126. Hurt AC, Selleck P, Komadina N, et al. Susceptibility of highly pathogenic A(H5N1) avian influenza viruses to the neuraminidase inhibitors and adamantanes. Antiviral Res 2007; 73:228-231.
127. Ilyushina NA, Seiler JP, Rehg JE, et al. Effect of neuraminidase inhibitor-resistant mutations on pathogenicity of clade 2.2 A/Turkey/15/06 (H5N1) influenza virus in ferrets. PLoS Pathog 2010; 6:e1000933.
128. Hurt AC, Lowther S, Middleton D et al. Assessing the development of oseltamivir and zanamivir resistance in A(H5N1) influenza viruses using a ferret model. Antiviral Res 2010; 87:361-366.
129. Naughtin M, Dyason JC, Mardy S, et al. Neuraminidase inhibitor sensitivity and receptor-binding specificity of Cambodian clade 1 highly pathogenic H5N1 influenza virus. Antimicrob Agents and Chemother 2011; 55:2004-2010.
130. Earhart KC, Elsayed NM, Saad MD, et al. Oseltamivir resistance mutation N294S in human influenza A(H5N1) virus in Egypt. J Infect Public Health 2009; 2:74-80.
131. Yen HL, Hoffmann E, Taylor G, et al. Importance of neuraminidase active-site residues to the neuraminidase inhibitor resistance of influenza viruses. J Virol 2006; 80:8787-8795. (Pubitemid 44384887)
132. Kiso M, Mitamura K, Sakai-Tagawa Y, et al. Resistant influenza A viruses in children treated with oseltamivir: descriptive study. Lancet 2004; 364:759-765. (Pubitemid 39165094)
133. Sheu TG, Deyde VM, Garten RJ, et al. Detection of antiviral resistance and genetic lineage markers in influenza B virus neuraminidase using pyrosequencing. Antiviral Res 2010; 85:354-360.
134. Barnett JM, Cadman A, Burrell FM, et al. In vitro selection and characterisation of influenza B/Beijing/1/87 isolates with altered susceptibility to zanamivir. Virology 1999; 265:286-295. (Pubitemid 30022223)
135. Mishin VP, Hayden FG, Gubareva LV. Susceptibilities of antiviral-resistant influenza viruses to novel neuraminidase inhibitors. Antimicrob Agents Chemother 2005; 49:4515-4520. (Pubitemid 41552580)