Antiviral therapy in seasonal influenza and 2009 H1N1 pandemic influenza: Korean experiences and perspectives

Expert Review of Anti-Infective Therapy

Volumn 13, Issue 11, 2015, Pages 1361-1372

  Song, Joon Young ^a,b   Noh, Ji Yun ^a,b   Choi, Won Suk ^a,b   Cheong, Hee Jin ^a,b   Kim, Woo Joo ^a,b  

^a Korea University College of Medicine   (South Korea)

^b TEPIK   (South Korea)

Author keywords

Antiviral agents; drug resistance; epidemics; influenza; Republic of Korea

Indexed keywords

AMANTADINE; ANTIVIRUS AGENT; CR 8020; DAS 181; DIRIDAVUMAB; FAVIPIRAVIR; FGI 101 1A6; LANINAMIVIR OCTANOATE; MED 18852; MONOCLONAL ANTIBODY; NAVIVUMAB; NITAZOXANIDE; OSELTAMIVIR; PERAMIVIR; PLACEBO; RIBAVIRIN; TCN 032; UNCLASSIFIED DRUG; VIS410; ZANAMIVIR; AMIDE; CYCLOPENTANE DERIVATIVE; GUANIDINE DERIVATIVE; LANINAMIVIR; PYRAZINE DERIVATIVE;

2009 H1N1 INFLUENZA; ANTIVIRAL THERAPY; DISEASE SURVEILLANCE; DRUG DOSE ESCALATION; DRUG EFFICACY; DRUG ELIMINATION; DRUG HALF LIFE; DRUG MEGADOSE; DRUG POTENTIATION; DRUG SAFETY; EPIDEMIC; HUMAN; INFLUENZA A; KOREAN (PEOPLE); MORBIDITY; MORTALITY; NONHUMAN; PANDEMIC INFLUENZA; RECOMMENDED DRUG DOSE; REVIEW; SEASONAL INFLUENZA; SEVERE ACUTE RESPIRATORY SYNDROME; SINGLE DRUG DOSE; TREATMENT DURATION; VIRUS STRAIN; WINTER; ANALOGS AND DERIVATIVES; ANTIVIRAL RESISTANCE; CLINICAL TRIAL (TOPIC); DRUG EFFECTS; HOSPITALIZATION; INFLUENZA A VIRUS (H1N1); INFLUENZA, HUMAN; SOUTH KOREA;

AMIDES; ANTIVIRAL AGENTS; CLINICAL TRIALS AS TOPIC; CYCLOPENTANES; DRUG RESISTANCE, VIRAL; GUANIDINES; HOSPITALIZATION; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA, HUMAN; OSELTAMIVIR; PYRAZINES; REPUBLIC OF KOREA; ZANAMIVIR;

EID: 84945448542     PISSN: 14787210     EISSN: 17448336     Source Type: Journal    
DOI: 10.1586/14787210.2015.1076334     Document Type: Review

References (87)

1. Nicholson KG. Human influenza. In: Nicholson KG, Webster RG, Hay AJ., Editors. Textbook of influenza. Oxford: Blackwell Science; 1998; 219-64
2. Song JY, Cheong HJ, Choi SH, et al. Hospital-based influenza surveillance in Korea: hospital-based influenza morbidity and mortality study group. J Med Virol 2013; 85: 910-17
3. Samson M, Pizzorno A, Abed Y, Boivin G. Influenza virus resistance to neuraminidase inhibitors. Antiviral Res 2013; 98: 174-85
4. Thompson WW, Shay DK, Weintraub E, et al. Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 2003; 289: 179-86
5. National Evidence-based Healthcare Collaborating Agency. Disease burden of seasonal influenza and vaccine effectiveness in Korea. 2010. Available from: www.neca.re.kr/center/researcher/report-view.jsp?boardNo=GA&seq=7&q=626f6172644e6f3d4741. [Last accessed 2015]
6. Suh M, Kang DR, Lee DH, et al. Socioeconomic burden of influenza in the Republic of Korea, 2007-2010. PLoS One 2013; 8: e84121
7. Lee JS, Shin KC, Na BK, et al. Influenza surveillance in Korea: establishment and first results of an epidemiological and virological surveillance scheme. Epidemiol Infect 2007; 135: 1117-23
8. Seo YB, Song JY, Cheong HJ, et al. Hospital-based influenza morbidity and mortality surveillance system for influenza-like illnesses: a comparison with national influenza surveillance systems. Influenza Other Respir Viruses 2014; 8: 17-20
9. Korea Center for Disease Control and Prevention (KCDC). Influenza A(H1N1) virus resistance to oseltamivir-Fourth quarter 2008 to 31 January 2009. Public Health Weekly Report 2009; 2: 220-1
10. Korea Center for Disease Control and Prevention (KCDC). Korean Influenza Sentinel Surveillance Report, 2013-2014. Public Health Weekly Report 2014; 7: 1089-98
11. Lee DH, Shin SS, Jun BY, Lee JK. [National level response to pandemic (H1N1) 2009]. J Prev Med Public Health 2010; 43: 99-104
12. Choi WS, Kim WJ, Cheong HJ. [The evaluation of policies on 2009 influenza pandemic in Korea]. J Prev Med Public Health 2010; 43: 105-8
13. Choi K, Cho SI, Hashizume M, Kim H. Epidemiological characteristics of novel influenza A (H1N1) in antiviral drug users in Korea. PLoS One 2012; 7: e47634
14. Kim JH, Yoo HS, Lee JS, et al. The spread of pandemic H1N1 2009 by age and region and the comparison among monitoring tools. J Korean Med Sci 2010; 25: 1109-12
15. Garske T, Legrand J, Donnelly CA, et al. Assessing the severity of the novel influenza A/H1N1 pandemic. BMJ 2009; 339: b2840
16. 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; 2: 395-404
17. Hong SB, Choi EY, Kim SH, et al. Epidemiological analysis of critically ill adult patients with pandemic influenza A(H1N1) in South Korea. Epidemiol Infect 2013; 141: 1070-9
18. Kang SJ, Park KH, Kee SJ, et al. Virological clearance rate of high-dose oseltamivir or triple-combination antiviral therapy in complicated 2009 pandemic influenza A (H1N1) infection. Jpn J Infect Dis 2013; 66: 425-7
19. Kim HS, Kim JH, Shin SY, et al. Fatal cases of 2009 pandemic influenza A (H1N1) in Korea. J Korean Med Sci 2011; 26: 22-7
20. Song JY, Cheong HJ, Heo JY, et al. Clinical, laboratory and radiologic characteristics of 2009 pandemic influenza A/H1N1 pneumonia: primary influenza pneumonia versus concomitant/secondary bacterial pneumonia. Influenza Other Respir Viruses 2011; 5: e535-43
21. Ko JH, Kim JH, Kang JH, et al. Characteristics of hospitalized children with 2009 pandemic influenza A (H1N1): a multicenter study in Korea. J Korean Med Sci 2012; 27: 408-15
22. Lee E, Seo JH, Kim HY, et al. Clinical characteristics and outcomes among pediatric patients hospitalized with pandemic influenza A/H1N1 2009 infection. Korean J Pediatr 2011; 54: 329-34
23. Rhim JW, Lee KY, Youn YS, et al. Epidemiological and clinical characteristics of childhood pandemic 2009 H1N1 virus infection: an observational cohort study. BMC Infect Dis 2011; 11: 225
24. 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: 1511-19
25. 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; 55: 5703-9
26. Smee DF, Hurst BL, Wong MH, et al. Effects of double combinations of amantadine, oseltamivir, and ribavirin on influenza A (H5N1) virus infections in cell culture and in mice. Antimicrob Agents Chemother 2009; 53: 2120-8
27. Hata A, Akashi-Ueda R, Takamatsu K, Matsumura T. Safety and efficacy of peramivir for influenza treatment. Drug Des Devel Ther 2014; 8: 2017-38
28. Choi WS, Lee J, Lee H-Y, et al. Clinical practice guideline for antiviral treatment and chemoprophylaxis of seasonal influenza. Infect Chemother 2012; 44: 233-49
29. Choi WS, Noh JY, Song JY, et al. Comparison of clinical effectiveness of oseltamivir and peramivir against seasonal influenza in Korean adults. In: 2014 Congress of the Korean Society for Chemotherapy &The Korean Society of Infectious Diseases. The Korean Society of Infectious Diseases, Seoul: 2014
30. Choi WS, Baek JH, Seo YB, et al. Severe influenza treatment guideline. Korean J Intern Med 2014; 29: 132-47
31. Yang SG, Cao B, Liang LR, et al. Antiviral therapy and outcomes of patients with pneumonia caused by influenza a pandemic (H1N1) virus. PLoS One 2012; 7: e29652
32. South East Asia Infectious Disease Clinical Research Network. Effect of double dose oseltamivir on clinical and virological outcomes in children and adults admitted to hospital with severe influenza: double blind randomised controlled trial. BMJ 2013; 346: f3039
33. Fiore AE, Fry A, Shay D, et al. Antiviral agents for the treatment and chemoprophylaxis of influenza-recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2011; 60: 1-24
34. Escuret V, Cornu C, Boutitie F, et al. Oseltamivir-zanamivir bitherapy compared to oseltamivir monotherapy in the treatment of pandemic 2009 influenza A(H1N1) virus infections. Antiviral Res 2012; 96: 130-7
35. Duval X, van der Werf S, Blanchon T, et al. Efficacy of oseltamivir-zanamivir combination compared to each monotherapy for seasonal influenza: a randomized placebo-controlled trial. PLoS Med 2010; 7: e1000362
36. Fraaij PL, van der Vries E, Beersma MF, et al. Evaluation of the antiviral response to zanamivir administered intravenously for treatment of critically ill patients with pandemic influenza A (H1N1) infection. J Infect Dis 2011; 204: 777-82
37. Petersen E, Keld DB, Ellermann-Eriksen S, et al. Failure of combination oral oseltamivir and inhaled zanamivir antiviral treatment in ventilator-and ECMO-treated critically ill patients with pandemic influenza A (H1N1)v. Scand J Infect Dis 2011; 43: 495-503
38. 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; 54: 1256-64
39. Ishizuka H, Yoshiba S, Okabe H, Yoshihara K. Clinical pharmacokinetics of laninamivir, a novel long-acting neuraminidase inhibitor, after single and multiple inhaled doses of its prodrug, CS-8958, in healthy male volunteers. J Clin Pharmacol 2010; 50: 1319-29
40. Samson M, Abed Y, Desrochers FM, et al. Characterization of drug-resistant influenza virus A(H1N1) and A(H3N2) variants selected in vitro with laninamivir. Antimicrob Agents Chemother 2014; 58: 5220-8
41. Yamashita M, Tomozawa T, Kakuta M, et al. CS-8958, a prodrug of the new neuraminidase inhibitor R-125489, shows long-acting anti-influenza virus activity. Antimicrob Agents Chemother 2009; 53: 186-92
42. 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; 51: 1167-75
43. 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; 54: 2575-82
44. Ikematsu H, Kawai N, Iwaki N, Kashiwagi S. Continued effectiveness of laninamivir octanate hydrate for influenza treatment in Japan: comparison between the 2011-2012 and 2012-2013 influenza seasons. J Infect Chemother 2014; 20: 799-803
45. Meijer A, Rebelo-de-Andrade H, Correia V, et al. Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2012-2013. Antiviral Res 2014; 110: 31-41
46. Takashita E, Meijer A, Lackenby A, et al. Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2013-2014. Antiviral Res 2015; 117: 27-38
47. Furuta Y, Takahashi K, Shiraki K, et al. T-705 (favipiravir) and related compounds: Novel broad-spectrum inhibitors of RNA viral infections. Antiviral Res 2009; 82: 95-102
48. Sidwell RW, Barnard DL, Day CW, et al. Efficacy of orally administered T-705 on lethal avian influenza A (H5N1) virus infections in mice. Antimicrob Agents Chemother 2007; 51: 845-51
49. Kiso M, Takahashi K, Sakai-Tagawa Y, et al. T-705 (favipiravir) activity against lethal H5N1 influenza A viruses. Proc Natl Acad Sci USA 2010; 107: 882-7
50. Park S, Kim JI, Lee I, et al. Combination effects of peramivir and favipiravir against oseltamivir-resistant 2009 pandemic influenza A(H1N1) infection in mice. PLoS One 2014; 9: e101325
51. Smee DF, Tarbet EB, Furuta Y, et al. Synergistic combinations of favipiravir and oseltamivir against wild-type pandemic and oseltamivir-resistant influenza A virus infections in mice. Future Virol 2013; 8: 1085-94
52. Hayden FG. Newer influenza antivirals, biotherapeutics and combinations. Influenza Other Respir Viruses 2013; 7 (Suppl 1): 63-75
53. Toyama Chemical Co. The new drug application approval of "AVIGAN® Tablet 200mg" in Japan for the anti-influenza virus drug. 2014. Available from: www.toyama-chemical.co.jp/eng/news/news140324e.html. [Last accessed 25 Mar 2015]
54. Malakhov MP, Aschenbrenner LM, Smee DF, et al. Sialidase fusion protein as a novel broad-spectrum inhibitor of influenza virus infection. Antimicrob Agents Chemother 2006; 50: 1470-9
55. Triana-Baltzer GB, Gubareva LV, Nicholls JM, et al. Novel pandemic influenza A(H1N1) viruses are potently inhibited by DAS181, a sialidase fusion protein. PLoS One 2009; 4: e7788
56. Marjuki H, Mishin VP, Chesnokov AP, et al. An investigational antiviral drug, DAS181, effectively inhibits replication of zoonotic influenza A virus subtype H7N9 and protects mice from lethality. J Infect Dis 2014; 210: 435-40
57. Belser JA, Lu X, Szretter KJ, et al. DAS181, a novel sialidase fusion protein, protects mice from lethal avian influenza H5N1 virus infection. J Infect Dis 2007; 196: 1493-9
58. Chan RW, Chan MC, Wong AC, et al. DAS181 inhibits H5N1 influenza virus infection of human lung tissues. Antimicrob Agents Chemother 2009; 53: 3935-41
59. Moss RB, Hansen C, Sanders RL, et al. A phase II study of DAS181, a novel host directed antiviral for the treatment of influenza infection. J Infect Dis 2012; 206: 1844-51
60. Triana-Baltzer GB, Sanders RL, Hedlund M, et al. Phenotypic and genotypic characterization of influenza virus mutants selected with the sialidase fusion protein DAS181. J Antimicrob Chemother 2011; 66: 15-28
61. Rossignol JF, La Frazia S, Chiappa L, et al. Thiazolides, a new class of anti-influenza molecules targeting viral hemagglutinin at the post-translational level. J Biol Chem 2009; 284: 29798-808
62. Rossignol JF. Nitazoxanide: a first-in-class broad-spectrum antiviral agent. Antiviral Res 2014; 110: 94-103
63. 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; 14: 609-18
64. Safety and efficacy study of nitazoxanide in the treatment of acute uncomplicated influenza. Available from: https://clinicaltrials.gov/ct2/show/NCT01610245
65. 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: 1061-9
66. Noh JY, Kim WJ. Influenza vaccines: unmet needs and recent developments. Infect Chemother 2013; 45: 375-86
67. Clementi N, Criscuolo E, Castelli M, Clementi M. Broad-range neutralizing anti-influenza A human monoclonal antibodies: new perspectives in therapy and prophylaxis. New Microbiol 2012; 35: 399-406
68. Corti D, Voss J, Gamblin SJ, et al. A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 2011; 333: 850-6
69. Dreyfus C, Laursen NS, Kwaks T, et al. Highly conserved protective epitopes on influenza B viruses. Science 2012; 337: 1343-8
70. Celltrion. Celltrion announces positive data from phase 1 trial of a novel therapeutic antibody CT-P27. 2013. Available from: www.celltrion.com/en/COMPANY/notice-view.asp?idx=414&code=ennews&intNowPage=1&menu-num=&align-year=all. [Last accessed 30 Mar 2015]
71. Song A, Myojo K, Laudenslager J, et al. Evaluation of a fully human monoclonal antibody against multiple influenza A viral strains in mice and a pandemic H1N1 strain in nonhuman primates. Antiviral Res 2014; 111: 60-8
72. Wang R, Song A, Levin J, et al. Therapeutic potential of a fully human monoclonal antibody against influenza A virus M2 protein. Antiviral Res 2008; 80: 168-77
73. Ozawa T, Jin A, Tajiri K, et al. Characterization of a fully human monoclonal antibody against extracellular domain of matrix protein 2 of influenza A virus. Antiviral Res 2011; 91: 283-7
74. Ramos EL, Mitcham JL, Koller TD, et al. Efficacy and safety of treatment with an anti-m2e monoclonal antibody in experimental human influenza. J Infect Dis 2015; 211: 1038-44
75. Takashita E, Ejima M, Fujisaki S, et al. A community cluster of influenza A(H1N1)pdm09 virus exhibiting cross-resistance to oseltamivir and peramivir in Japan, November 2013 to February 2014. In: The Fifth ESWI Influenza Conference, 16 September 2014, Riga, Latvia
76. Pascua PN, Choi YK. Zoonotic infections with avian influenza A viruses and vaccine preparedness: a game of "mix and match". Clin Exp Vaccine Res 2014; 3: 140-8
77. Safety study of anti-influenza virus monoclonal antibody to treat Influenza. Available from: https://clinicaltrials.gov/ct2/show/NCT01390025
78. Influenza virus challenge study to test monoclonal antibody TCN-032 as a treatment for influenza. Available from: https://clinicaltrials.gov/ct2/show/NCT01719874
79. Assessment of CR6261, a monoclonal antibody against the influenza a virus. Available from: https://clinicaltrials.gov/ct2/show/NCT01406418
80. Assessment of CR8020, a monoclonal antibody against influenza a viruses. Available from: https://clinicaltrials.gov/ct2/show/NCT01756950
81. Assessment of efficacy of CR8020 and CR6261, monoclonal antibodies, against influenza infection. Available from: https://clinicaltrials.gov/ct2/show/NCT01992276
82. Evaluation of the protective efficacy and safety of CR8020 in an influenza challenge. Available from: https://clinicaltrials.gov/ct2/show/NCT01938352
83. Study in healthy volunteers to evaluate the efficacy and safety of CR6261 in an H1N1 influenza healthy human challenge model. Available from: https://clinicaltrials.gov/ct2/show/NCT02371668
84. To Evaluate the efficacy and safety of CT-P27 in an influenza challenge model. Available from: https://clinicaltrials.gov/ct2/show/NCT02071914
85. Safety and pharmacokinetics study of human monoclonal antibody (FGI-101-1A6). Available from: https://clinicaltrials.gov/ct2/show/NCT01299142
86. A study of VIS410 to assess safety and pharmacokinetics. Available from: https://clinicaltrials.gov/ct2/show/NCT02045472
87. Phase 1 placebo-controlled,dose-escalation study to evaluate the safety and pharmacokinetics of MEDI8852 in adults. Available from: https://clinicaltrials.gov/ct2/show/NCT02350751