62
Views
0
CrossRef citations to date
0
Altmetric
Review

Treating influenza with neuraminidase inhibitors: an update of the literature

, , ORCID Icon &
Pages 1163-1174 | Received 29 Mar 2024, Accepted 18 Jun 2024, Published online: 27 Jun 2024

References

  • Centers for Disease Control and Prevention (CDC). Key facts about influenza (Flu). [cited 2024 Jun 11]. Available from: https://www.cdc.gov/flu/about/keyfacts.htm
  • WHO. Influenza (seasonal). [cited 2024 Jun 11]. Available from: https://www.who.int/news-room/fact-sheets/detail/influenza-(seasonal)
  • WHO. Guidelines for the clinical management of severe illness from influenza virus infections. Geneva; 2022 [cited 2024 Jun 11]. Available from: https://www.ncbi.nlm.nih.gov/books/NBK579105/
  • Javanian M, Barary M, Ghebrehewet S, et al. A brief review of influenza virus infection. J Med Virol. 2021 Aug;93(8):4638–4646. doi: 10.1002/jmv.26990
  • Toots M, Plemper RK. Next-generation direct-acting influenza therapeutics. Transl Res. 2020 Jun;220:33–42. doi: 10.1016/j.trsl.2020.01.005
  • Smith BJ, Colman PM, Von Itzstein M, et al. Analysis of inhibitor binding in influenza virus neuraminidase. Protein Sci. 2001 Apr;10(4):689–696. doi: 10.1110/ps.41801
  • Davies BE. Pharmacokinetics of oseltamivir: an oral antiviral for the treatment and prophylaxis of influenza in diverse populations. J Antimicrob Chemother. 2010 Apr;Suppl 65(Suppl 2):ii5–ii10. doi: 10.1093/jac/dkq015
  • Moscona A. Neuraminidase inhibitors for influenza. N Engl J Med. 2005 Sep 29;353(13):1363–1373. doi: 10.1056/NEJMra050740
  • Cheng VC, To KK, Tse H, et al. Two years after pandemic influenza A/2009/H1N1: what have we learned? Clin Microbiol Rev. 2012 Apr;25(2):223–263. doi: 10.1128/CMR.05012-11
  • Bantia S, Arnold CS, Parker CD, et al. Anti-influenza virus activity of peramivir in mice with single intramuscular injection. Antiviral Res. 2006 Jan;69(1):39–45. doi: 10.1016/j.antiviral.2005.10.002
  • Chairat K, Tarning J, White NJ, et al. Pharmacokinetic properties of anti-influenza neuraminidase inhibitors. J Clin Pharmacol. 2013 Feb;53(2):119–139. doi: 10.1177/0091270012440280
  • Principi N, Camilloni B, Alunno A, et al. Drugs for influenza treatment: is there significant news? Front Med. 2019;6:109. doi: 10.3389/fmed.2019.00109
  • Uyeki TM, Bernstein HH, Bradley JS, et al. Clinical practice guidelines by the Infectious Diseases Society of America: 2018 update on diagnosis, treatment, chemoprophylaxis, and institutional outbreak management of seasonal influenzaa. Clin Infect Dis. 2019 Mar 5;68(6):895–902. doi: 10.1093/cid/ciy874
  • Muthuri SG, Venkatesan S, Myles PR, et al. Effectiveness of neuraminidase inhibitors in reducing mortality in patients admitted to hospital with influenza a H1N1pdm09 virus infection: a meta-analysis of individual participant data. Lancet Respir Med. 2014 May;2(5):395–404. doi: 10.1016/S2213-2600(14)70041-4
  • Katzen J, Kohn R, Houk JL, et al. Early oseltamivir after hospital admission is associated with shortened hospitalization: a 5-year analysis of oseltamivir timing and clinical outcomes. Clin Infect Dis. 2019 Jun 18;69(1):52–58. doi: 10.1093/cid/ciy860
  • Doll MK, Winters N, Boikos C, et al. Safety and effectiveness of neuraminidase inhibitors for influenza treatment, prophylaxis, and outbreak control: a systematic review of systematic reviews and/or meta-analyses. J Antimicrob Chemother. 2017 Nov 1;72(11):2990–3007. doi: 10.1093/jac/dkx271
  • Engelhard D, Mohty B, de la Camara R, et al. European guidelines for prevention and management of influenza in hematopoietic stem cell transplantation and leukemia patients: summary of ECIL-4 (2011), on behalf of ECIL, a joint venture of EBMT, EORTC, ICHS, and ELN. Transpl Infect Dis. 2013 Jun;15(3):219–232. doi: 10.1111/tid.12054
  • Dobson J, Whitley RJ, Pocock S, et al. Oseltamivir treatment for influenza in adults: a meta-analysis of randomised controlled trials. Lancet. 2015 May 2;385(9979):1729–1737. doi: 10.1016/S0140-6736(14)62449-1
  • Heneghan CJ, Onakpoya I, Thompson M, et al. Zanamivir for influenza in adults and children: systematic review of clinical study reports and summary of regulatory comments. BMJ. 2014 Apr 9;348(apr09 2):g2547. doi: 10.1136/bmj.g2547
  • Thorlund K, Awad T, Boivin G, et al. Systematic review of influenza resistance to the neuraminidase inhibitors. BMC Infect Dis. 2011 May 19;11(1):134. doi: 10.1186/1471-2334-11-134
  • Lackenby A, Hungnes O, Dudman SG, et al. Emergence of resistance to oseltamivir among influenza A(H1N1) viruses in Europe. Euro Surveill. 2008 Jan 31;13(5):3–4. doi: 10.2807/ese.13.05.08026-en
  • Su CP, Chan KA, Huang CT, et al. Inhaled zanamivir vs oral oseltamivir to prevent influenza-related hospitalization or death: a nationwide population-based quasi-experimental study. Clin Infect Dis. [2022 Oct 12];75(8):1273–1279. doi: 10.1093/cid/ciac217
  • Slain D. Intravenous zanamivir: a viable option for critically ill patients with influenza. Ann Pharmacother. 2021 Jun;55(6):760–771. doi: 10.1177/1060028020963616
  • Scott LJ. Peramivir: a review in uncomplicated influenza. Drugs. 2018 Sep;78(13):1363–1370. doi: 10.1007/s40265-018-0981-8
  • Barroso L, Treanor J, Gubareva L, et al. Efficacy and tolerability of the oral neuraminidase inhibitor peramivir in experimental human influenza: randomized, controlled trials for prophylaxis and treatment. Antivir Ther. 2005;10(8):901–910. doi: 10.1177/135965350501000805
  • Whitley R, Laughlin A, Carson S, et al. Single dose peramivir for the treatment of acute seasonal influenza: integrated analysis of efficacy and safety from two placebo-controlled trials. Antivir Ther. 2015;20(7):709–719. doi: 10.3851/IMP2874
  • Kohno S, Kida H, Mizuguchi M, et al. Efficacy and safety of intravenous peramivir for treatment of seasonal influenza virus infection. Antimicrob Agents Chemother. 2010 Nov;54(11):4568–4574. doi: 10.1128/AAC.00474-10
  • Kohno S, Yen MY, Cheong HJ, et al. Phase III randomized, double-blind study comparing single-dose intravenous peramivir with oral oseltamivir in patients with seasonal influenza virus infection. Antimicrob Agents Chemother. 2011 Nov;55(11):5267–5276. doi: 10.1128/AAC.00360-11
  • Ikematsu H, Kawai N. Laninamivir octanoate: a new long-acting neuraminidase inhibitor for the treatment of influenza. Expert Rev Anti Infect Ther. 2011 Oct;9(10):851–857. doi: 10.1586/eri.11.112
  • Yamashita M. Laninamivir and its prodrug, CS-8958: long-acting neuraminidase inhibitors for the treatment of influenza. Antiviral Chem Chemother. 2010;21(2):71–84. doi: 10.3851/IMP1688
  • Kubo S, Tomozawa T, Kakuta M, et al. Laninamivir prodrug CS-8958, a long-acting neuraminidase inhibitor, shows superior anti-influenza virus activity after a single administration. Antimicrob Agents Chemother. 2010 Mar;54(3):1256–1264. doi: 10.1128/AAC.01311-09
  • Sugaya N, Ohashi Y. Long-acting neuraminidase inhibitor laninamivir octanoate (CS-8958) versus oseltamivir as treatment for children with influenza virus infection. Antimicrob Agents Chemother. 2010 Jun;54(6):2575–2582. doi: 10.1128/AAC.01755-09
  • Watanabe A, Chang SC, Kim MJ, et al. Long-acting neuraminidase inhibitor laninamivir octanoate versus oseltamivir for treatment of influenza: A double-blind, randomized, noninferiority clinical trial. Clin Infect Dis. 2010 Nov 15;51(10):1167–1175. doi: 10.1086/656802
  • Jing X, Ma C, Ohigashi Y, et al. Functional studies indicate amantadine binds to the pore of the influenza a virus M2 proton-selective ion channel. Proc Natl Acad Sci USA. 2008 Aug 5;105(31):10967–10972. doi: 10.1073/pnas.0804958105
  • Ison MG. Antiviral treatments. Clin Chest Med. 2017 Mar;38(1):139–153. doi: 10.1016/j.ccm.2016.11.008
  • Centers for Disease Control and Prevention (CDC). High levels of adamantane resistance among influenza a (H3N2) viruses and interim guidelines for use of antiviral agents – United States, 2005-06 influenza season. MMWR Morb Mortal Wkly Rep. 2006 Jan 20;55(2):44–46.
  • O’Hanlon R, Shaw ML. Baloxavir marboxil: the new influenza drug on the market. Curr Opin Virol. 2019 Apr;35:14–18. doi: 10.1016/j.coviro.2019.01.006
  • Hayden FG, Sugaya N, Hirotsu N, et al. Baloxavir marboxil for uncomplicated influenza in adults and adolescents. N Engl J Med. [2018 Sep 6];379(10):913–923. doi: 10.1056/NEJMoa1716197
  • Ison MG, Portsmouth S, Yoshida Y, et al. Early treatment with baloxavir marboxil in high-risk adolescent and adult outpatients with uncomplicated influenza (CAPSTONE-2): a randomised, placebo-controlled, phase 3 trial. Lancet Infect Dis. 2020 Oct;20(10):1204–1214. doi: 10.1016/S1473-3099(20)30004-9
  • Ringer M, Malinis M, McManus D, et al. Clinical outcomes of baloxavir versus oseltamivir in immunocompromised patients. Transpl Infect Dis. 2024 Apr;26(2):e14249. doi: 10.1111/tid.14249
  • Łagocka R, Dziedziejko V, Kłos P, et al. Favipiravir in therapy of viral infections. J Clin Med. 2021 Jan 13;10(2):273. doi: 10.3390/jcm10020273
  • Hayden FG, Shindo N. Influenza virus polymerase inhibitors in clinical development. Curr Opin Infect Dis. 2019 Apr;32(2):176–186. doi: 10.1097/QCO.0000000000000532
  • Wang Y, Fan G, Salam A, et al. Comparative effectiveness of combined favipiravir and oseltamivir therapy versus oseltamivir monotherapy in critically Ill patients with influenza virus infection. J Infect Dis. 2020 Apr 27;221(10):1688–1698. doi: 10.1093/infdis/jiz656
  • Goldhill DH, Te Velthuis AJW, Fletcher RA, et al. The mechanism of resistance to favipiravir in influenza. Proc Natl Acad Sci USA. 2018 Nov 6;115(45):11613–11618. doi: 10.1073/pnas.1811345115
  • Welliver R, Monto AS, Carewicz O, et al. Effectiveness of oseltamivir in preventing influenza in household contacts: a randomized controlled trial. JAMA. 2001 Feb 14;285(6):748–754. doi: 10.1001/jama.285.6.748
  • Duwe SC, Schmidt B, Gartner BC, et al. Prophylaxis and treatment of influenza: options, antiviral susceptibility, and existing recommendations. GMS Infect Dis. 2021;9:Doc02.
  • Carrat F, Duval X, Tubach F, et al. Effect of oseltamivir, zanamivir or oseltamivir-zanamivir combination treatments on transmission of influenza in households. Antivir Ther. 2012;17(6):1085–1090. doi: 10.3851/IMP2128
  • Boikos C, Caya C, Doll MK, et al. Safety and effectiveness of neuraminidase inhibitors in situations of pandemic and/or novel/variant influenza: a systematic review of the literature, 2009-15. J Antimicrob Chemother. 2017 Jun 1;72(6):1556–1573. doi: 10.1093/jac/dkx013
  • Kumar S, Goicoechea S, Kumar S, et al. Oseltamivir analogs with potent anti-influenza virus activity. Drug Discov Today. 2020 Aug;25(8):1389–1402. doi: 10.1016/j.drudis.2020.06.004
  • Seo S, Englund JA, Nguyen JT, et al. Combination therapy with amantadine, oseltamivir and ribavirin for influenza a infection: safety and pharmacokinetics. Antivir Ther. 2013;18(3):377–386. doi: 10.3851/IMP2475
  • Kim WY, Young Suh G, Huh JW, et al. Triple-combination antiviral drug for pandemic H1N1 influenza virus infection in critically ill patients on mechanical ventilation. Antimicrob Agents Chemother. 2011 Dec;55(12):5703–5709. doi: 10.1128/AAC.05529-11
  • Lampejo T. Influenza and antiviral resistance: an overview. Eur J Clin Microbiol Infect Dis. 2020 Jul;39(7):1201–1208. doi: 10.1007/s10096-020-03840-9
  • Gamino-Arroyo AE, Guerrero ML, McCarthy S, et al. Efficacy and safety of nitazoxanide in addition to standard of care for the treatment of severe acute respiratory illness. Clin Infect Dis. 2019 Nov 13;69(11):1903–1911. doi: 10.1093/cid/ciz100
  • Haffizulla J, Hartman A, Hoppers M, et al. 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 Jul;14(7):609–618. doi: 10.1016/S1473-3099(14)70717-0
  • Govorkova EA, Takashita E, Daniels RS, et al. Global update on the susceptibilities of human influenza viruses to neuraminidase inhibitors and the cap-dependent endonuclease inhibitor baloxavir, 2018-2020. Antiviral Res. 2022 Apr;200:105281. doi: 10.1016/j.antiviral.2022.105281
  • Lee N, Hurt AC. Neuraminidase inhibitor resistance in influenza: a clinical perspective. Curr Opin Infect Dis. 2018 Dec;31(6):520–526. doi: 10.1097/QCO.0000000000000498
  • Hussain M, Galvin HD, Haw TY, et al. Drug resistance in influenza a virus: the epidemiology and management. Infect Drug Resist. 2017;10:121–134. doi: 10.2147/IDR.S105473
  • WHO Global Influenza Programme -Table 1. [cited 2024 Jun 11] Available from: https://cdn.who.int/media/docs/default-source/global-influenza-programme/1.-nai_human_reduced-susceptibility-marker-table-(who)_07.03.23_update.pdf?sfvrsn=eef56b17_1&download=true
  • McAuley JL, Gilbertson BP, Trifkovic S, et al. Influenza virus neuraminidase structure and functions. Front Microbiol. 2019;10:39. doi: 10.3389/fmicb.2019.00039
  • Colman PM, Varghese JN, Laver WG. Structure of the catalytic and antigenic sites in influenza virus neuraminidase. Nature. 1983 May 5–11;303(5912):41–44. doi: 10.1038/303041a0
  • Burmeister WP, Ruigrok RW, Cusack S. The 2.2 a resolution crystal structure of influenza B neuraminidase and its complex with sialic acid. Embo J. 1992 Jan;11(1):49–56. doi: 10.1002/j.1460-2075.1992.tb05026.x
  • Centers for Disease Control and Prevention (CDC). Influenza Antiviral Drug Resistance. [cited 2024 Jun 11]. Available from: https://www.cdc.gov/flu/treatment/antiviralresistance.htm
  • Nguyen HT, Fry AM, Gubareva LV. Neuraminidase inhibitor resistance in influenza viruses and laboratory testing methods. Antivir Ther. 2012;17(1 Pt B):159–173. doi: 10.3851/IMP2067
  • 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 Mar;12(3):240–248. doi: 10.1016/S1473-3099(11)70318-8
  • Ikematsu H, Kawai N, Iwaki N, et al. In vitro neuraminidase inhibitory concentration (IC(50)) of four neuraminidase inhibitors in the Japanese 2016–17 season: Comparison with the 2010–11 to 2015–16 seasons. J Infect Chemother. 2018 Sep;24(9):707–712. doi: 10.1016/j.jiac.2018.04.009
  • Huang W, Cheng Y, Li X, et al. Neuraminidase inhibitor susceptibility profile of human influenza viruses during the 2016–2017 influenza season in Mainland China. J Infect Chemother. 2018 Sep;24(9):729–733. doi: 10.1016/j.jiac.2018.05.003
  • Schade D, Kotthaus J, Riebling L, et al. Development of novel potent orally bioavailable oseltamivir derivatives active against resistant influenza a. J Med Chem. 2014 Feb 13;57(3):759–769. doi: 10.1021/jm401492x
  • Zhao H, Jiang S, Ye Z, et al. Discovery of hydrazide-containing oseltamivir analogues as potent inhibitors of influenza a neuraminidase. Eur J Med Chem. 2021 Oct 5;221:113567. doi: 10.1016/j.ejmech.2021.113567
  • Ai W, Zhang J, Zalloum WA, et al. Discovery of novel “Dual-site” binding oseltamivir derivatives as potent influenza virus neuraminidase inhibitors. Eur J Med Chem. 2020 Apr 1;191:112147. doi: 10.1016/j.ejmech.2020.112147
  • Keil JM, Rafn GR, Turan IM, et al. Sialidase inhibitors with different mechanisms. J Med Chem. 2022 Oct 27;65(20):13574–13593. doi: 10.1021/acs.jmedchem.2c01258
  • McKimm-Breschkin JL, Barrett S, McKenzie-Kludas C, et al. Passaging of an influenza A(H1N1)pdm09 virus in a difluoro sialic acid inhibitor selects for a novel, but unfit I106M neuraminidase mutant. Antiviral Res. 2019 Sep;169:104542. doi: 10.1016/j.antiviral.2019.104542
  • Liu X, Zhang B, Wang Y, et al. A universal dual mechanism immunotherapy for the treatment of influenza virus infections. Nat Commun. 2020 Nov 5;11(1):5597. doi: 10.1038/s41467-020-19386-5
  • Chan RWY, Tao KP, Ye J, et al. Inhibition of influenza virus replication by oseltamivir derivatives. Pathogens. 2022 Feb 11;11(2):237. doi: 10.3390/pathogens11020237
  • Ivachtchenko AV, Ivanenkov YA, Mitkin OD, et al. Novel oral anti-influenza drug candidate AV5080. J Antimicrob Chemother. 2014 Jul;69(7):1892–1902. doi: 10.1093/jac/dku074
  • Dose range study to evaluate the efficacy and safety of AV5080 in patients with influenza. [cited 2024 Jun 11]. Available from: https://www.clinicaltrials.gov/study/NCT05095545
  • Jones JC, Yen HL, Adams P, et al. Influenza antivirals and their role in pandemic preparedness. Antiviral Res. 2023 Feb;210:105499. doi: 10.1016/j.antiviral.2022.105499
  • A study of HNC042 in healthy Chinese subjects to evaluate the safety, tolerability, and pharmacokinetics (NCT04603989). [cited 2024 Jun 11]. Available from: https://clinicaltrials.gov/study/NCT04603989
  • Enkhtaivan G, Kim DH, Park GS, et al. Berberine-piperazine conjugates as potent influenza neuraminidase blocker. Int j biol macromol. 2018 Nov;119:1204–1210. doi: 10.1016/j.ijbiomac.2018.08.047
  • Asadi-Samani M, Altememy D, Saffari-Chaleshtor J, et al. Berberine as a new neuraminidase inhibitor drug: a systematic review [10.34172/jhp.2024.48132]. J Herbmed Pharmacol. 2024;13(1):19–27. doi: 10.34172/jhp.2024.48132
  • Morimoto R, Matsubara C, Hanada A, et al. Effect of structural differences in naringenin, prenylated naringenin, and their derivatives on the anti-influenza virus activity and cellular uptake of their flavanones. Pharmaceuticals (Basel). 2022 Nov 28;15(12):1480. doi: 10.3390/ph15121480

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.