Effectiveness of four types of neuraminidase inhibitors approved in Japan for the treatment of influenza

English version

Autoři: Momoko Mawatari ^aff001; Reiko Saito ^aff001; Akinobu Hibino ^aff001; Hiroki Kondo ^aff001; Ren Yagami ^aff001; Takashi Odagiri ^aff001; Ikumi Tanabe ^aff001; Yugo Shobugawa ^aff001;
Působiště autorů: Division of International Health (Public Health), Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan ^aff001; Division of Infectious Diseases and Immunology, Department of Microbiology, School of Medicine, Iwate Medical University, Iwate, Japan ^aff002
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0224683

Souhrn

Background

Neuraminidase inhibitors (NAIs) effectively treat influenza. The clinical effectiveness of four NAIs (oseltamivir, zanamivir, laninamivir, and peramivir) was evaluated against influenza A/H1N1pdm09, A/H3N2, and B viruses. Additionally, fever duration in patients infected with oseltamivir-resistant influenza A/H1N1pdm09 with the H275Y mutation was evaluated.

Methods

Patients aged <20 years who visited outpatient clinics in Japan with influenza-like illnesses were enrolled during 4 influenza seasons from 2012/2013 to 2015/2016. After obtaining informed consent, patients who tested positive for influenza with rapid tests received one of the four NAIs. Patients recorded their body temperature daily for 8 days from the first visit. The influenza strain was identified using real-time polymerase chain reaction. Univariate and multivariable analyses were used to evaluate factors influencing fever duration. In children aged ≤5 years treated with oseltamivir, fever duration in oseltamivir-resistant A/H1N1pdm09-infected patients was compared to that in oseltamivir-sensitive A/H1N1pdm09-infected patients.

Results

Of the 1,368 patients analyzed, 297 (21.7%), 683 (49.9%), and 388 (28.4%) were infected with influenza A/H1N1pdm09, A/H3N2, and B, respectively. In multivariable analysis factors associated with significantly prolonged fever duration included: treatment with laninamivir (hazard ratio [HR]: 0.78, p = 0.006, compared to oseltamivir), influenza B (HR: 0.58, p<0.001, compared to influenza A/H1N1pdm09), and a higher body temperature at the clinic visit (HR: 0.87 per degree Celsius, p<0.001). Increasing age was associated with a significantly shorter duration of fever (HR: 1.31 for 6–9 years old, p<0.001; and HR: 1.65 for 10–19 years old, p<0.001, respectively, compared to 0–5 years old). Following treatment with oseltamivir, fever duration was significantly longer for oseltamivir-resistant A/H1N1pdm09-infected patients (n = 5) than for oseltamivir-sensitive A/H1N1pdm09 infected patients (n = 111) (mean, 89 versus 40 hours, p<0.001).

Conclusions

Our results revealed characteristic information on the effectiveness of the four NAIs and also on oseltamivir-resistant viruses that may affect patients’ clinical care.

Klíčová slova:

Vaccination and immunization – Influenza viruses – Influenza A virus – Age groups – Fevers – Influenza – Japan – Body temperature

Zdroje

1. Murakami Y, Hashimoto S, Kawado M, Ohta A, Taniguchi K, Sunagawa T, et al. Estimated number of patients with influenza A(H1)pdm09, or other viral types, from 2010 to 2014 in Japan. PLoS One. 2016;11: e0146520. Epub 2016/01/20. doi: 10.1371/journal.pone.0146520 26784031.

2. Zaraket H, Saito R. Japanese surveillance systems and treatment for influenza. Current Treat Options Infect Dis. 2016;8: 311–328. Epub 2016/12/31. doi: 10.1007/s40506-016-0085-5 28035195.

3. McKimm-Breschkin JL. Influenza neuraminidase inhibitors: antiviral action and mechanisms of resistance. Influenza Other Resp Viruses. 2013;7 Suppl 1: 25–36. Epub 2013/01/04. doi: 10.1111/irv.12047 23279894.

4. Kawai N, Ikematsu H, Iwaki N, Maeda T, Satoh I, Hirotsu N, et al. A comparison of the effectiveness of oseltamivir for the treatment of influenza A and influenza B: a Japanese multicenter study of the 2003–2004 and 2004–2005 influenza seasons. Clin Infect Dis. 2006;43: 439–444. Epub 2006/07/14. doi: 10.1086/505868 16838232.

5. Sato M, Saito R, Sato I, Tanabe N, Shobugawa Y, Sasaki A, et al. Effectiveness of oseltamivir treatment among children with influenza A or B virus infections during four successive winters in Niigata City, Japan. Tohoku J Exp Med. 2008;214: 113–120. Epub 2008/02/21. doi: 10.1620/tjem.214.113 18285668.

6. Dobson J, Whitley RJ, Pocock S, Monto AS. Oseltamivir treatment for influenza in adults: a meta-analysis of randomised controlled trials. Lancet. 2015;385(9979): 1729–1737. Epub 2015/02/03. doi: 10.1016/S0140-6736(14)62449-1 25640810.

7. Jefferson T, Demicheli V, Rivetti D, Jones M, Di Pietrantonj C, Rivetti A. Antivirals for influenza in healthy adults: systematic review. Lancet. 2006;367(9507):303–313. Epub 2006/01/31. doi: 10.1016/S0140-6736(06)67970-1 16443037.

8. Sugaya N, Tamura D, Yamazaki M, Ichikawa M, Kawakami C, Kawaoka Y, et al. Comparison of the clinical effectiveness of oseltamivir and zanamivir against influenza virus infection in children. Clin Infect Dis. 2008;47(3): 339–345. Epub 2008/06/28. doi: 10.1086/589748 18582202.

9. Hurt AC. The epidemiology and spread of drug resistant human influenza viruses. Curr Opin Virol. 2014;8: 22–29. Epub 2014/05/29. doi: 10.1016/j.coviro.2014.04.009 24866471.

10. Baranovich T, Saito R, Suzuki Y, Zaraket H, Dapat C, Caperig-Dapat I, et al. Emergence of H274Y oseltamivir-resistant A(H1N1) influenza viruses in Japan during the 2008–2009 season. J Clin Virol. 2010;47(1): 23–28. Epub 2009/12/08. doi: 10.1016/j.jcv.2009.11.003 19962344.

11. Hauge SH, Dudman S, Borgen K, Lackenby A, Hungnes O. Oseltamivir-resistant influenza viruses A (H1N1), Norway, 2007–08. Emerg Infect Dis. 2009;15(2): 155–162. Epub 2009/02/06. doi: 10.3201/eid1502.081031 19193257.

12. Matsuzaki Y, Mizuta K, Aoki Y, Suto A, Abiko C, Sanjoh K, et al. A two-year survey of the oseltamivir-resistant influenza A(H1N1) virus in Yamagata, Japan and the clinical effectiveness of oseltamivir and zanamivir. Virol J. 2010;7:53. Epub 2010/03/06. doi: 10.1186/1743-422X-7-53 20202225.

13. Saito R, Sato I, Suzuki Y, Baranovich T, Matsuda R, Ishitani N, et al. Reduced effectiveness of oseltamivir in children infected with oseltamivir-resistant influenza A (H1N1) viruses with His275Tyr mutation. Pediatr Infect Dis J. 2010;29(10): 898–904. Epub 2010/05/06. doi: 10.1097/INF.0b013e3181de9d24 20442686.

14. 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(6): 2575–2582. doi: 10.1128/AAC.01755-09 20368393

15. Lina B, Boucher C, Osterhaus A, Monto AS, Schutten M, Whitley RJ, 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 Resp Viruses. 2018;12(2): 267–278. Epub 2017/12/22. doi: 10.1111/irv.12534 29265727.

16. Wang B, Taylor J, Ratnamohan M, McPhie K, Kesson A, Dixit R, et al. Frequency of oseltamivir resistance in Sydney, during the Newcastle outbreak of community transmitted oseltamivir-resistant influenza A(H1N1)pdm09 virus, Australia, June to August 2011. Eurosurveillance. 2012;17(27): 20210. Epub 2012/07/14. doi: 10.2807/ese.17.27.20210-en 22790606.

17. Takashita E, Ejima M, Itoh R, Miura M, Ohnishi A, Nishimura H, et al. A community cluster of influenza A(H1N1)pdm09 virus exhibiting cross-resistance to oseltamivir and peramivir in Japan, November to December 2013. Eurosurveillance. 2014;19(1): 4–9.

18. Kakuya F, Kinebuchi T, Fujiyasu H, Tanaka R, Okubo H, Kano H. Clinical findings in 10 children with H275Y influenza A(H1N1)pdm09 virus infection. Pediatr Int. 2015;57(5): 888–892. doi: 10.1111/ped.12658 25865177

19. Hibino A, Kondo H, Masaki H, Tanabe Y, Sato I, Takemae N, et al. Community- and hospital-acquired infections with oseltamivir- and peramivir-resistant influenza A(H1N1)pdm09 viruses during the 2015–2016 season in Japan. Virus Genes. 2017;53(1):89–94. Epub 2016/10/08. doi: 10.1007/s11262-016-1396-9 27714496.

20. Dapat IC, Dapat C, Baranovich T, Suzuki Y, Kondo H, Shobugawa Y, et al. Genetic characterization of human influenza viruses in the pandemic (2009–2010) and post-pandemic (2010–2011) periods in Japan. PLoS One. 2012;7(6):e36455. doi: 10.1371/journal.pone.0036455 22761651

21. Suzuki Y, Saito R, Sato I, Zaraket H, Nishikawa M, Tamura T, et al. Identification of oseltamivir resistance among pandemic and seasonal influenza A (H1N1) viruses by an His275Tyr genotyping assay using the cycling probe method. J Clin Microbiol. 2011;49(1): 125–130. Epub 2010/11/19. doi: 10.1128/JCM.01401-10 21084523.

22. Zaraket H, Kondo H, Hibino A, Yagami R, Odagiri T, Takemae N, et al. Full genome characterization of human influenza A/H3N2 isolates from Asian countries reveals a rare amantadine resistance-conferring mutation and novel PB1-F2 polymorphisms. Front Microbiol. 2016;7: 262. doi: 10.3389/fmicb.2016.00262 27014195

23. Kanda Y. Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant. 2013;48(3): 452–458. Epub 2012/12/05. doi: 10.1038/bmt.2012.244 23208313.

24. Ishiguro N, Koseki N, Kaiho M, Ariga T, Kikuta H, Oba K, et al. Clinical effectiveness of four neuraminidase inhibitors (oseltamivir, zanamivir, laninamivir, and peramivir) for children with influenza A and B in the 2014–2015 to 2016–2017 influenza seasons in Japan. J Infect Chemother. 2018;24(6):449–457. Epub 2018/03/01. doi: 10.1016/j.jiac.2018.01.013 29487035.

25. Shobugawa Y, Saito R, Sato I, Kawashima T, Dapat C, Dapat IC, et al. Clinical effectiveness of neuraminidase inhibitors-oseltamivir, zanamivir, laninamivir, and peramivir-for treatment of influenza A(H3N2) and A(H1N1)pdm09 infection: an observational study in the 2010–2011 influenza season in Japan. J Infect Chemother. 2012;18(6):858–864. doi: 10.1007/s10156-012-0428-1 22644080

26. Kawai N, Ikematsu H, Iwaki N, Maeda T, Kawashima T, Hirotsu N, et al. Comparison of the effectiveness of Zanamivir and Oseltamivir against influenza A/H1N1, A/H3N2, and B. Clin Infect Dis. 2009;48(7):996–997. Epub 2009/03/06. doi: 10.1086/597360 19260819.

27. Sugaya N, Mitamura K, Yamazaki M, Tamura D, Ichikawa M, Kimura K, et al. Lower clinical effectiveness of oseltamivir against influenza B contrasted with influenza A infection in children. Clin Infect Dis. 2007;44(2): 197–202. doi: 10.1086/509925 17173216

28. Kondo H, Shobugawa Y, Hibino A, Yagami R, Dapat C, Okazaki M, et al. Influenza Virus Shedding in Laninamivir-Treated Children upon Returning to School. Tohoku J Exp Med. 2016;238(2):113–121. doi: 10.1620/tjem.238.113 26806610

29. Boivin G, Goyette N. Susceptibility of recent Canadian influenza A and B virus isolates to different neuraminidase inhibitors. Antiviral Res. 2002;54(3):143–147. Epub 2002/06/14. doi: 10.1016/s0166-3542(01)00219-4 12062387.

30. Burnham AJ, Baranovich T, Govorkova EA. Neuraminidase inhibitors for influenza B virus infection: efficacy and resistance. Antivir Res. 2013;100(2):520–534. Epub 2013/09/10. doi: 10.1016/j.antiviral.2013.08.023 24013000.

31. Koseki N, Kaiho M, Kikuta H, Oba K, Togashi T, Ariga T, et al. Comparison of the clinical effectiveness of zanamivir and laninamivir octanoate for children with influenza A (H3N2) and B in the 2011–2012 season. Influenza Other Resp Viruses. 2014;8(2):151–158.

32. Hikita T, Hikita H, Hikita F, Hikita N, Hikita S. Clinical effectiveness of peramivir in comparison with other neuraminidase inhibitors in pediatric influenza patients. Int J pediatr. 2012;2012: 834181. Epub 2012/04/21. doi: 10.1155/2012/834181 22518184.

33. Sugaya N, Sakai-Tagawa Y, Bamba M, Yasuhara R, Yamazaki M, Kawakami C, et al. Comparison between virus shedding and fever duration after treating children with pandemic A H1N1/09 and children with A H3N2 with a neuraminidase inhibitor. Antivir Ther. 2015;20(1): 49–55. Epub 2014/05/17. doi: 10.3851/IMP2798 24832015.

34. Yoshi N, Tocino Y, Fujioka M, Kureya Y, Asai K, Kimura T, et al. Comparison of the clinical courses of patients with influenza after neuraminidase inhibitors treatment: A postcard survey of the 2013–2014 influenza season in Osaka. Osaka City Med J. 2016;62(2): 29–38. Epub 2016/12/01. 30550708.

35. Hirotsu N, Saisho Y, Hasegawa T, Shishido T. Clinical and virologic effects of four neuraminidase inhibitors in influenza A virus-infected children (aged 4–12 years): an open-label, randomized study in Japan. Expert Rev Anti Infect Ther. 2018;16(2):173–182. Epub 2017/12/30. doi: 10.1080/14787210.2018.1421945 29284320.

36. Takemoto Y, Asai T, Ikezoe I, Yano T, Ichikawa M, Miyagawa S, et al. Clinical effects of oseltamivir, zanamivir, laninamivir and peramivir on seasonal influenza infection in outpatients in Japan during the winter of 2012–2013. Chemotherapy. 2013;59(5):373–378. doi: 10.1159/000362436 24821568

37. Kawai N, Ikematsu H, Iwaki N, Satoh I, Kawashima T, Maeda T, et al. Factors influencing the effectiveness of oseltamivir and amantadine for the treatment of influenza: a multicenter study from Japan of the 2002–2003 influenza season. Clin Infect Dis. 2005;40(9):1309–1316. Epub 2005/04/13. doi: 10.1086/429241 15825034.

38. Suzuki E, Ichihara K. The course of fever following influenza virus infection in children treated with oseltamivir. J Med Virol. 2008;80(6):1065–1071. Epub 2008/04/23. doi: 10.1002/jmv.21144 18428131.

39. Li CC, Wang L, Eng HL, You HL, Chang LS, Tang KS, et al. Correlation of pandemic (H1N1) 2009 viral load with disease severity and prolonged viral shedding in children. Emerg Infect Dis. 2010;16(8):1265–1272. Epub 2010/08/04. doi: 10.3201/eid1608.091918 20678321.

40. Leekha S, Zitterkopf NL, Espy MJ, Smith TF, Thompson RL, Sampathkumar P. Duration of influenza A virus shedding in hospitalized patients and implications for infection control. Infect Control Hosp Epidemiol. 2007;28(9):1071–1076. Epub 2007/10/13. doi: 10.1086/520101 17932829.

41. Munoz FM. Influenza virus infection in infancy and early childhood. Paediatr Respir Rev. 2003;4(2):99–104. Epub 2003/05/22. 12758046.

42. Kawai N, Ikematsu H, Iwaki N, Maeda T, Kanazawa H, Kawashima T, et al. A comparison of the effectiveness of zanamivir and oseltamivir for the treatment of influenza A and B. J Infection. 2008;56(1):51–57. https://doi.org/10.1016/j.jinf.2007.09.002.

43. Kaiser L, Fritz RS, Straus SE, Gubareva L, Hayden FG. Symptom pathogenesis during acute influenza: interleukin-6 and other cytokine responses. J Med Virol. 2001;64(3):262–268. Epub 2001/06/26. doi: 10.1002/jmv.1045 11424113.

44. Tochino Y, Fujioka M, Sakazaki H, Ikuno Y, Tochino R, Yoshii N, et al. Current usage and effectiveness of influenza medications and factors regarding the time taken to alleviate fever based on postcard questionnaire survey. J Gen Fam Med. 2017;18(6):386–392. Epub 2017/12/22. doi: 10.1002/jgf2.109 29264069.

45. Kawai N, Ikematsu H, Iwaki N, Kondou K, Hirotsu N, Kawashima T, et al. Clinical effectiveness of oseltamivir for influenza A(H1N1) virus with H274Y neuraminidase mutation. J Infection. 2009;59(3):207–212. Epub 2009/07/22. doi: 10.1016/j.jinf.2009.07.002 19619898.

46. Hayden FG, Sugaya N, Hirotsu N, Lee N, de Jong MD, Hurt AC, et al. Baloxavir Marboxil for uncomplicated influenza in adults and adolescents. N Engl J Med. 2018;379(10):913–923. Epub 2018/09/06. doi: 10.1056/NEJMoa1716197 30184455.

47. Hayden FG, Shindo N. Influenza virus polymerase inhibitors in clinical development. Curr Opin Infect Dis. 2019;32(2):176–186. Epub 2019/02/07. doi: 10.1097/QCO.0000000000000532 30724789.