Neuraminidase inhibitor resistance in influenza: a clinical perspective

Current Opinion in Infectious Diseases

Volumn 31, Issue 6, 2018, Pages 520-526

  Lee, Nelson ^a   Hurt, Aeron C ^b,c  

^a UNIVERSITY OF ALBERTA   (Canada)

^b VICTORIAN INFECTIOUS DISEASES REFERENCE LABORATORY   (Australia)

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

Author keywords

Antiviral resistance; Influenza virus; Neuraminidase inhibitors

Indexed keywords

OSELTAMIVIR; PERAMIVIR; SIALIDASE INHIBITOR; ZANAMIVIR; ANTIVIRUS AGENT; ENZYME INHIBITOR; SIALIDASE; VIRAL PROTEIN;

ANTIVIRAL RESISTANCE; ANTIVIRAL THERAPY; DRUG EXPOSURE; HUMAN; IMMUNOCOMPROMISED PATIENT; INFLUENZA; INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H3N2); INFLUENZA A VIRUS (H7N9); INFLUENZA B VIRUS; NONHUMAN; PRIORITY JOURNAL; PROPHYLAXIS; REVIEW; RISK FACTOR; TREATMENT RESPONSE; VIRUS LOAD; VIRUS STRAIN; DRUG EFFECT; INFLUENZA A VIRUS;

ANTIVIRAL AGENTS; DRUG RESISTANCE, VIRAL; ENZYME INHIBITORS; HUMANS; INFLUENZA A VIRUS; INFLUENZA B VIRUS; INFLUENZA, HUMAN; NEURAMINIDASE; VIRAL PROTEINS;

EID: 85055824940     PISSN: 09517375     EISSN: 14736527     Source Type: Journal    
DOI: 10.1097/QCO.0000000000000498     Document Type: Review

References (58)

1. Hurt AC, Chotpitayasunondh T, Cox NJ, et al. Antiviral resistance during the 2009 influenza A H1N1 pandemic: Public health, laboratory, and clinical perspectives. Lancet Infect Dis 2012; 12:240–248.
2. Li TC, Chan MC, Lee N. Clinical implications of antiviral resistance in influenza. Viruses 2015; 7:4929–4944.
3. Leung K, Lipsitch M, Yuen KY, Wu JT. Monitoring the fitness of antiviral-resistant influenza strains during an epidemic: a mathematical modelling study. Lancet Infect Dis 2017; 17:339–347.
4. Gubareva LV, Besselaar TG, Daniels RS, et al. Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors. Antiviral Res 2017; 146:12–20. This study reports the latest results of the WHO global surveillance program on NAI resistance.
5. Lina B, Boucher C, Osterhaus A, et al. Five years of monitoring for the emergence of oseltamivir resistance in patients with influenza A infections in the Influenza Resistance Information Study. Influenza Other Respir Viruses 2018; 12:267–278.
6. Centers for Disease Control and Prevention (CDC). Influenza Antiviral Drug Resistance. https://www.cdc.gov/flu/about/qa/antiviralresistance.htm. [Accessed 15 August 2018].
7. Public Health England (PHE). PHE guidance on use of antiviral agents for the treatment and prophylaxis of seasonal influenza. Version 8.0; September 2017. https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/648758/PHE_guidance_antivirals_influenza_201718_FINAL.pdf. [Accessed 15 August 2018].
8. Kelso A, Hurt AC. The ongoing battle against influenza: drug-resistant influenza viruses: why fitness matters. Nat Med 2012; 18:1470–1471.
9. Bloom JD, Gong LI, Baltimore D. Permissive secondary mutations enable the evolution of influenza oseltamivir resistance. Science 2010; 328:1272–1275.
10. Butler J, Hooper KA, Petrie S, et al. Estimating the fitness advantage conferred by permissive neuraminidase mutations in recent oseltamivir-resistant A(H1N1)pdm09 influenza viruses. PLoS Pathog 2014; 10:e1004065.
11. Tamura D, DeBiasi RL, Okomo-Adhiambo M, et al. Emergence of multidrug-resistant influenza A(H1N1)pdm09 virus mutants in an immunocompromised child treated with oseltamivir and zanamivir. J Infect Dis 2015; 212:1209–1213.
12. L’Huillier AG, Abed Y, Petty TJ, et al. E119D neuraminidase mutation conferring pan-resistance to neuraminidase inhibitors in an A(H1N1)pdm09 isolate from a stem-cell transplant recipient. J Infect Dis 2015; 212:1726–1734.
13. Trebbien R, Pedersen SS, Vorborg K, et al. Development of oseltamivir and zanamivir resistance in influenza A(H1N1)pdm09 virus, Denmark, 2014. Euro Surveill 2017; 22:30445.
14. Abed Y, Boivin G. A review of clinical influenza A and B infections with reduced susceptibility to both oseltamivir and zanamivir. Open Forum Infect Dis 2017; 4:ofx105.
15. Oh DY, Panozzo J, Vitesnik S, et al. Selection of multidrug resistant influenza A and B viruses under zanamivir pressure and their replication fitness in ferrets. Antivir Ther 2017. doi: 10.3851/IMP3135 [Epub ahead of print].
16. Yates PJ, Raimonde DS, Zhao HH, et al. Phenotypic and genotypic analysis of influenza viruses isolated from adult subjects during a phase II study of intravenous zanamivir in hospitalised subjects. Antiviral Res 2016; 134:144–152.
17. de Jong MD, Ison MG, Monto AS, et al. Evaluation of intravenous peramivir for treatment of influenza in hospitalized patients. Clin Infect Dis 2014; 59:e172–e185.
18. Babady NE, Laplante JM, Tang YW, St George K. Detection of a transient R292K mutation in influenza A/H3N2 viruses shed for several weeks by an immunocompromised patient. J Clin Microbiol 2015; 53:1415–1418.
19. Chaudhry A, Bastien N, Li Y, et al. Oseltamivir resistance in an influenza A (H3N2) virus isolated from an immunocompromised patient during the 2014-2015 influenza season in Alberta, Canada. Influenza Other Respir Viruses 2016; 10:532–535.
20. Gaymard A, Charles-Dufant A, Sabatier M, et al. Impact on antiviral resistance of E119V, I222L and R292K substitutions in influenza A viruses bearing a group 2 neuraminidase (N2, N3, N6, N7 and N9). J Antimicrob Chemother 2016; 71:3036–3045.
21. Lee N, Hui DS, Zuo Z, et al. A prospective intervention study on higher-dose oseltamivir treatment in adults hospitalized with influenza a and B infections. Clin Infect Dis 2013; 57:1511–1519.
22. Farrukee R, Leang SK, Butler J, et al. Influenza viruses with B/Yamagata- and B/Victoria-like neuraminidases are differentially affected by mutations that alter antiviral susceptibility. J Antimicrob Chemother 2015; 70: 2004–2012.
23. Uyeki TM, Katz JM, Jernigan DB. Novel influenza A viruses and pandemic threats. Lancet 2017; 389:2172–2174.
24. Quan C, Shi W, Yang Y, et al. New threats from H7N9 influenza virus: spread and evolution of high- and low-pathogenicity variants with high genomic diversity in wave five. J Virol 2018; 92:e00301–e318. This study reports the revolution of H7N9 virus and the threat of NAI resistant variants.
25. Hu Y, Lu S, Song Z, et al. Association between adverse clinical outcome in human disease caused by novel influenza A H7N9 virus and sustained viral shedding and emergence of antiviral resistance. Lancet 2013; 381:2273–2279.
26. Zou X, Guo Q, Zhang W, et al. CAP-China Network. Dynamic variation and reversion in the signature amino acids of H7N9 virus during human infection. J Infect Dis 2018. doi: 10.1093/infdis/jiy217 [Epub ahead of print].
27. Gubareva LV, Sleeman K, Guo Z, et al. Drug susceptibility evaluation of an influenza A(H7N9) virus by analyzing recombinant neuraminidase proteins. J Infect Dis 2017; 216(Suppl_4):S566–S574.
28. Kiso M, Iwatsuki-Horimoto K, Yamayoshi S, et al. Emergence of oseltamivir-resistant H7N9 influenza viruses in immunosuppressed cynomolgus macaques. J Infect Dis 2017; 216:582–593.
29. Ke C, Mok CKP, Zhu W, et al. Human infection with highly pathogenic avian influenza A(H7N9) virus, China. Emerg Infect Dis 2017; 23:1332–1340.
30. Yang L, Zhu W, Li X, et al. Genesis and spread of newly emerged highly pathogenic H7N9 avian viruses in mainland China. J Virol 2017; 91:e01277–e1317.
31. McKimm-Breschkin JL, Barrett S, Wong FYK, et al. Identification of Indonesian clade 2.1 highly pathogenic influenza A(H5N1) viruses with N294S and S246N neuraminidase substitutions which further reduce oseltamivir susceptibility. Antiviral Res 2018; 153:95–100.
32. Choi WS, Jeong JH, Kwon JJ, et al. Screening for neuraminidase inhibitor resistance markers among avian influenza viruses of the N4, N5, N6, and N8 neuraminidase subtypes. J Virol 2017; 92:e01580–e1617.
33. Okomo-Adhiambo M, Mishin VP, Sleeman K, et al. Standardizing the influenza neuraminidase inhibition assay among United States public health laboratories conducting virological surveillance. Antiviral Res 2016; 128:28–35.
34. Gubareva LV, Fallows E, Mishin VP, et al. Monitoring influenza virus susceptibility to oseltamivir using a new rapid assay, iART. Euro Surveill 2017; 22:30529. This study describes a novel assay for rapid detection of oseltamivir resistance.
35. Wang W, Song Z, Guan W, et al. PCR for detection of oseltamivir resistance mutation in influenza A(H7N9) virus. Emerg Infect Dis 2014; 20:847–849.
36. Pichon M, Gaymard A, Josset L, et al. Characterization of oseltamivir-resistant influenza virus populations in immunosuppressed patients using digital-droplet PCR: Comparison with qPCR and next generation sequencing analysis. Antiviral Res 2017; 145:160–167. This study reports a new method to detect emergence of oseltamivir-resistant virus subpopulations.
37. Whale AS, Bushell CA, Grant PR, et al. Detection of rare drug resistance mutations by digital PCR in a human influenza A virus model system and clinical samples. J Clin Microbiol 2016; 54:392–400.
38. Tamura D, Okomo-Adhiambo M, Mishin VP, et al. Application of a seven-target pyrosequencing assay to improve the detection of neuraminidase inhibitor-resistant Influenza A(H3N2) viruses. Antimicrob Agents Chemother 2015; 59:2374–2379.
39. Lee N, Leo YS, Cao B, et al. Neuraminidase inhibitors, superinfection and corticosteroids affect survival of influenza patients. Eur Respir J 2015; 45:1642–1652.
40. Koszalka P, Tilmanis D, Hurt AC. Influenza antivirals currently in late-phase clinical trial. Influenza Other Respir Viruses 2017; 11:240–246.
41. Marty FM, Vidal-Puigserver J, Clark C, et al. Intravenous zanamivir or oral oseltamivir for hospitalised patients with influenza: an international, randomised, double-blind, double-dummy, phase 3 trial. Lancet Respir Med 2017; 5:135–146.
42. Kobayashi M, Kodama M, Noshi T, et al. Therapeutic efficacy of peramivir against H5N1 highly pathogenic avian influenza viruses harboring the neuraminidase H275Y mutation. Antiviral Res 2017; 139:41–48.
43. McKimm-Breschkin JL, Jiang S, Hui DS, et al. Prevention and treatment of respiratory viral infections: presentations on antivirals, traditional therapies and host-directed interventions at the 5th ISIRV Antiviral Group conference. Antiviral Res 2018; 149:118–142.
44. Delang L, Abdelnabi R, Neyts J. Favipiravir as a potential countermeasure against neglected and emerging RNA viruses. Antiviral Res 2018; 153:85–94.
45. Takashita E, Ejima M, Ogawa R, et al. Antiviral susceptibility of influenza viruses isolated from patients pre and postadministration of favipiravir. Antiviral Res 2016; 132:170–177.
46. Heo YA. Baloxavir: first global approval. Drugs 2018; 78:693–697.
47. Portsmouth S, Kawaguchi K, Arai M, et al. Cap-dependent endonuclease inhibitor S-033188 for the treatment of influenza: results from a phase 3, randomized, double-blind, placebo- and active-controlled study in otherwise healthy adolescents and adults with seasonal influenza [abstract no. LB-2]. Open Forum Infect Dis 2017; 4(Suppl 1):S734.
48. Jones JC, Kumar G, Barman S, et al. Identification of the I38T PA substitution as a resistance marker for next-generation influenza virus endonuclease inhibitors. MBio 2018; 9:e00430–e518.
49. Fu Y, Gaelings L, Söderholm S, et al. JNJ872 inhibits influenza A virus replication without altering cellular antiviral responses. Antiviral Res 2016; 133:23–31.
50. Trevejo JM, Asmal M, Vingerhoets J, et al. Pimodivir treatment in adult volunteers experimentally inoculated with live influenza virus: a phase IIa, randomized, double-blind, placebo-controlled study. Antivir Ther 2017. doi: 10.3851/IMP3212 [Epub ahead of print].
51. Haffizulla J, Hartman A, Hoppers M, et al., US Nitazoxanide Influenza Clinical Study Group. Effect of nitazoxanide in adults and adolescents with acute uncomplicated influenza: a double-blind, randomised, placebo-controlled, phase 2b/3 trial. Lancet Infect Dis 2014; 14:609–618.
52. Zenilman JM, Fuchs EJ, Hendrix CW, et al. Phase 1 clinical trials of DAS181, an inhaled sialidase, in healthy adults. Antiviral Res 2015; 123:114–119.
53. Dunning J, Baillie JK, Cao B, Hayden FG. Antiviral combinations for severe influenza. Lancet Infect Dis 2014; 14:1259–1270.
54. Marathe BM, Wong SS, Vogel P, et al. Combinations of Oseltamivir and T-705 Extend the Treatment Window for Highly Pathogenic Influenza A(H5N1) Virus Infection in Mice. Sci Rep 2016; 6: 26742.
55. Kiso M, Lopes TJS, Yamayoshi S, et al. Combination therapy with neuraminidase and polymerase inhibitors in nude mice infected with influenza virus. J Infect Dis 2018; 217:887–896.
56. Belardo G, Cenciarelli O, La Frazia S, et al. Synergistic effect of nitazoxanide with neuraminidase inhibitors against influenza A viruses in vitro. Antimicrob Agents Chemother 2015; 59:1061–1069.
57. Beigel JH, Bao Y, Beeler J, et al., IRC003 Study Team. Oseltamivir, amantadine, and ribavirin combination antiviral therapy versus oseltamivir monotherapy for the treatment of influenza: a multicentre, double-blind, randomised phase 2 trial. Lancet Infect Dis 2017; 17:1255–1265.
58. Lee N, Hui DSC. Potential and challenges of serotherapy for severe influenza. Lancet Respir Med 2017; 5:e27.