Assessment of influenza A (H1N1, H3N2) oseltamivir resistance during 2017-2019 in Iran
-
Amytis Gholami
,
Nazanin Zahra Shafiei-Jandaghi
,
Nastaran Ghavami
,
Forough Tavakoli
,
Jila Yavarian
,
Talat Mokhtari-Azad
Abstract
Background and Objectives: Neuraminidase inhibitors (NAIs) as an imperative antiviral for influenza prophylaxis and treatment are being consumed worldwide. Increasing use of these antivirals might be associated with drug resistance. Regarding the significance of these variations, this study aimed to investigate the mutations occurring in the NA gene of influenza A viruses leading to oseltamivir resistance during 2017-2019 in Iran.
Materials and Methods: In this cross-sectional study, 40 influenza A (H1N1, H3N2) strains, isolated in National Influenza Center (NIC) from patients with Severe Acute Respiratory Infection (SARI) during 2017-2019 were subjected to RT-PCR and sequencing of NA complete gene. The frequency of oseltamivir resistance and variation of NA amino acids in these strains were investigated.
Results: No significant mutation conferring oseltamivir resistance was detected. However, NA antigenic sites in these strains depicted minor changes compared to the vaccine strains. Among H3N2 isolates, mutations at 329, 344, 346 and 385 and among H1N1 isolates mutations at 143 and 188 residues occurred in NA antigenic regions.
Conclusion: Evaluation of NA gene sequences, showed no resistant viruses to oseltamivir. Given that the viruses in the present study were the last viruses circulating in Iran before COVID-19 pandemic, the results will be beneficial to have a worthy comparison with the strains circulating after the pandemic. Constant monitoring for the emergence of drug-resistant variants and antigenic changes are crucial for all countries.
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4. Jackson ML, Chung JR, Jackson LA, Phillips CH, Benoit J, Monto AS, et al. Influenza vaccine effectiveness in the United States during the 2015–2016 season. N Engl J Med 2017; 377: 534-543.
5. Bassetti M, Castaldo N, Carnelutti A. Neuraminidase inhibitors as a strategy for influenza treatment: pros, cons and future perspectives. Expert Opin Pharmacother 2019; 20: 1711-1718.
6. Paules CI, Sullivan SG, Subbarao K, Fauci AS. Chasing seasonal influenza-the need for a universal influenza vaccine. N Engl J Med 2018; 378: 7-9.
7. Sautto GA, Kirchenbaum GA, Ross TM. Towards a universal influenza vaccine: different approaches for one goal. Virol J 2018; 15: 17.
8. 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: 913-923.
9. Heo Y-A. Baloxavir: first global approval. Drugs 2018; 78: 693-697.
10. Han N, Oh JM, Kim I-W. Assessment of adverse events related to anti-influenza neuraminidase inhibitors using the FDA adverse event reporting system and online patient reviews. Sci Rep 2020; 10: 3116.
11. Rashidi O, Moattari A, Pirbonyeh N, Emami A, Kadivar MR, Tavakoli Movaghar N, et al. Investigation of genetic variation: Neuraminidase gene of influenza A virus H1N1/pdm09, Shiraz, Iran (2015–2016). J Med Virol 2021; 93: 4763-4772.
12. Holmes EC, Hurt AC, Dobbie Z, Clinch B, Oxford JS, Piedra PA. Understanding the impact of resistance to influenza antivirals. Clin Microbiol Rev 2021; 34(2): e00224-20.
13. Zhang W, Xu H, Guan S, Wang C, Dong G. Frequency and distribution of H1N1 influenza A viruses with oseltamivir‐resistant mutations worldwide before and after the 2009 pandemic. J Med Virol 2022; 94: 4406-4416.
14. Liu S-S, Jiao X-Y, Wang S, Su W-Z, Jiang L-Z, Zhang X, et al. Susceptibility of influenza A (H1N1)/pdm2009, seasonal A (H3N2) and B viruses to Oseltamivir in Guangdong, China between 2009 and 2014. Sci Rep 2017; 7: 8488.
15. Lampejo T. Influenza and antiviral resistance: an overview. Eur J Clin Microbiol Infect Dis 2020; 39: 1201-1208.
16. Momeni P, Abedin Dargoosh S, Sedehzadeh AA, Bagheri G, Mohammadi M, Poosashkan L, et al. Neuraminidase Gene Variations in Influenza A (H1N1) pdm09 Virus among Patients Admitted to Refferal Pulmonary Hospital, Tehran, Iran in 2009–2013. Tanaffos 2017; 16: 99-106.
17. Moasser E, Behzadian F, Moattari A, Fotouhi F, Zaraket H. Characterization of the neuraminidase genes from human influenza A viruses circulating in Iran from 2010 to 2015. Arch Virol 2018; 163: 391-400.
18. Khodadad N, Moattari A, Shamsi Shahr Abadi M, Kadivar MR, Sarvari J, Tavakoli F, et al. Prevalence of influenza A (H1N1) pdm09 virus resistant to oseltamivir in Shiraz, Iran, during 2012-2013. Jundishapur J Microbiol 2015; 8(8): e23690.
19. Moradi A, Nadji SA, Tabarsi P, Hashemian SM, Marjani M, Sigaroodi A, et al. Prevalence of oseltamivir-resistant 2009 H1N1 influenza virus among patients with pandemic 2009 H1N1 influenza infection in NRITLD, Tehran, Iran. Tanaffos 2011; 10: 8-11.
20. Koel BF, Vigeveno RM, Pater M, Koekkoek SM, Han AX, Tuan HM, et al. Longitudinal sampling is required to maximize detection of intrahost A/H3N2 virus variants. Virus Evol 2020; 6:veaa088.
21. Takashita E, Daniels RS, Fujisaki S, Gregory V, Gubareva LV, Huang W, et al. Global update on the susceptibilities of human influenza viruses to neuraminidase inhibitors and the cap-dependent endonuclease inhibitor baloxavir, 2017–2018. Antiviral Res 2020; 175: 104718.
22. Akand EH, Downard KM. Mechanisms of antiviral resistance in influenza neuraminidase revealed by a mass spectrometry based phylonumerics approach. Mol Phylogenet Evol 2019; 135: 286-296.
23. Pires De Mello CP, Drusano GL, Adams JR, Shudt M, Kulawy R, Brown AN. Oseltamivir-zanamivir combination therapy suppresses drug-resistant H1N1 influenza A viruses in the hollow fiber infection model (HFIM) system. Eur J Pharm Sci 2018; 111: 443-449.
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: 449-457.
25. Job ER, Schotsaert M, Ibañez LI, Smet A, Ysenbaert T, Roose K, et al. Antibodies directed toward neuraminidase N1 control disease in a mouse model of influenza. J Virol 2018; 92(4): e01584-17.
26. Sedova ES, Scherbinin DN, Lysenko AA, Alekseeva SV, Artemova EA, Shmarov MM. Non-neutralizing antibodies directed at conservative influenza antigens. Acta Naturae 2019; 11: 22-32.
27. McMillan CLD, Young PR, Watterson D, Chappell KJ. The next generation of influenza vaccines: Towards a universal solution. Vaccines (Basel) 2021; 9: 26.
28. Yavarian J, Shafiei Jandaghi NZ, Naseri M, Mokhtari Azad T. Characterization of variations in PB2, NS1, M, neuraminidase and hemagglutinin of influenza A (H3N2) viruses in Iran. Jundishapur J Microbiol 2014; 7(3): e9089.
29. Liang L, Huang P, Wen M, Ni H, Tan S, Zhang Y, et al. Epitope peptides of influenza H3N2 virus neuraminidase gene designed by immunoinformatics. Acta Biochim Biophys Sin (Shanghai) 2012; 44: 113-118.
30. Kaplan BS, Anderson TK, Chang J, Santos J, Perez D, Lewis N, et al. Evolution and antigenic advancement of N2 neuraminidase of swine influenza A viruses circulating in the United States following two separate introductions from human seasonal viruses. J Virol 2021; 95(20): e0063221.
31. Liu B, Wang Y, Liu Y, Chen Y, Liu Y, Cong X, et al. Molecular evolution and characterization of hemagglutinin and neuraminidase of influenza A (H1N1) pdm09 viruses isolated in Beijing, China, during the 2017–2018 and 2018–2019 influenza seasons. Arch Virol 2021; 166: 179-189.
32. Mohan T, Nguyen HT, Kniss K, Mishin VP, Merced-Morales AA, Laplante J, et al. Cluster of Oseltamivir-Resistant and Hemagglutinin Antigenically Drifted Influenza A (H1N1) pdm09 Viruses, Texas, USA, January 2020. Emerg Infect Dis 2021; 27: 1953-1957.
33. Lee N, Hurt AC. Neuraminidase inhibitor resistance in influenza: a clinical perspective. Curr Opin Infect Dis 2018; 31: 520-526.
34. Principi N, Camilloni B, Alunno A, Polinori I, Argentiero A, Esposito S. Drugs for influenza treatment: is there significant news? Front Med (Lausanne) 2019; 6: 109.
35. Bai Y, Jones JC, Wong S-S, Zanin M. Antivirals targeting the surface glycoproteins of Influenza virus: Mechanisms of action and resistance. Viruses 2021; 13: 624.
36. Yavarian J, Mokhtari-Azad T, Nadji SA, Zeraati H, Naseri M. Analysis of the hemagglutinin and neuraminidase genes of human Influenza A/H3N2 viruses circulating in iran between 2005 and 2007: antigenic and phylogenetic relationships to vaccine strains. Intervirology 2010; 53: 133-140.
37. Simon P, Holder BP, Bouhy X, Abed Y, Beauchemin CA, Boivin G. 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.
38. Okomo-Adhiambo M, Demmler-Harrison GJ, Deyde VM, Sheu TG, Xu X, Klimov AI, 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.
39. Van Poelvoorde LAE, Saelens X, Thomas I, Roosens NH. Next-generation sequencing: an eye-opener for the surveillance of antiviral resistance in influenza. Trends Biotechnol 2020; 38: 360-367.
40. McGinnis J, Laplante J, Shudt M, George KS. Next generation sequencing for whole genome analysis and surveillance of influenza A viruses. J Clin Virol 2016; 79: 44-50.
41. McAuley JL, Gilbertson BP, Trifkovic S, Brown LE, McKimm-Breschkin JL. Influenza virus neuraminidase structure and functions. Front Microbiol 2019; 10: 39.
42. Powell H, Pekosz A. Neuraminidase antigenic drift of H3N2 clade 3c. 2a viruses alters virus replication, enzymatic activity and inhibitory antibody binding. PLoS Pathog 2020; 16(6): e1008411.
43. Wan H, Gao J, Yang H, Yang S, Harvey R, Chen Y-Q, et al. The neuraminidase of A (H3N2) influenza viruses circulating since 2016 is antigenically distinct from the A/Hong Kong/4801/2014 vaccine strain. Nat Microbiol 2019; 4: 2216-2225.
44. Zost SJ, Parkhouse K, Gumina ME, Kim K, Diaz Perez S, Wilson PC, et al. Contemporary H3N2 influenza viruses have a glycosylation site that alters binding of antibodies elicited by egg-adapted vaccine strains. Proc Natl Acad Sci U S A 2017; 114: 12578-12583.
45. Bashir Aamir U, Badar N, Mehmood MR, Nisar N, Suleman RM, Shaukat S, et al. Molecular epidemiology of influenza A (H1N1) pdm09 viruses from Pakistan in 2009–2010. PLoS One 2012; 7(8): e41866.
46. Jandaghi NZ, Azad TM, Naseri M, Yavarian J, Nategh R. Molecular and genetic characteristics of hemagglutinin and neuraminidase in Iranian 2009 pandemic influenza A (H1N1) viruses. Arch Virol 2010; 155: 717-721.
47. Al Khatib HA, Al Thani AA, Gallouzi I, Yassine HM. Epidemiological and genetic characterization of pH1N1 and H3N2 influenza viruses circulated in MENA region during 2009–2017. BMC Infect Dis 2019; 19: 314.
48. Isakova-Sivak I, Stepanova E, Mezhenskaya D, Matyushenko V, Prokopenko P, Sychev I, et al. Influenza vaccine: Progress in a vaccine that elicits a broad immune response. Expert Rev Vaccines 2021; 20: 1097-1112.
2. Souquette A, Thomas PG. Past life and future effects-How heterologous infections alter immunity to influenza viruses. Front Immunol 2018; 9: 1071.
3. Tavakoli F, Moattari A, Shamsi Shahr Abadi M, Kadivar MR, Khodadad N, Pirbonyeh N, et al. Antigenic Variation of the Haemagglutinin Gene of the Influenza A (H1N1) pdm09 Virus Circulating in Shiraz, February-April 2013. Iran J Immunol 2015; 12: 198-208.
4. Jackson ML, Chung JR, Jackson LA, Phillips CH, Benoit J, Monto AS, et al. Influenza vaccine effectiveness in the United States during the 2015–2016 season. N Engl J Med 2017; 377: 534-543.
5. Bassetti M, Castaldo N, Carnelutti A. Neuraminidase inhibitors as a strategy for influenza treatment: pros, cons and future perspectives. Expert Opin Pharmacother 2019; 20: 1711-1718.
6. Paules CI, Sullivan SG, Subbarao K, Fauci AS. Chasing seasonal influenza-the need for a universal influenza vaccine. N Engl J Med 2018; 378: 7-9.
7. Sautto GA, Kirchenbaum GA, Ross TM. Towards a universal influenza vaccine: different approaches for one goal. Virol J 2018; 15: 17.
8. 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: 913-923.
9. Heo Y-A. Baloxavir: first global approval. Drugs 2018; 78: 693-697.
10. Han N, Oh JM, Kim I-W. Assessment of adverse events related to anti-influenza neuraminidase inhibitors using the FDA adverse event reporting system and online patient reviews. Sci Rep 2020; 10: 3116.
11. Rashidi O, Moattari A, Pirbonyeh N, Emami A, Kadivar MR, Tavakoli Movaghar N, et al. Investigation of genetic variation: Neuraminidase gene of influenza A virus H1N1/pdm09, Shiraz, Iran (2015–2016). J Med Virol 2021; 93: 4763-4772.
12. Holmes EC, Hurt AC, Dobbie Z, Clinch B, Oxford JS, Piedra PA. Understanding the impact of resistance to influenza antivirals. Clin Microbiol Rev 2021; 34(2): e00224-20.
13. Zhang W, Xu H, Guan S, Wang C, Dong G. Frequency and distribution of H1N1 influenza A viruses with oseltamivir‐resistant mutations worldwide before and after the 2009 pandemic. J Med Virol 2022; 94: 4406-4416.
14. Liu S-S, Jiao X-Y, Wang S, Su W-Z, Jiang L-Z, Zhang X, et al. Susceptibility of influenza A (H1N1)/pdm2009, seasonal A (H3N2) and B viruses to Oseltamivir in Guangdong, China between 2009 and 2014. Sci Rep 2017; 7: 8488.
15. Lampejo T. Influenza and antiviral resistance: an overview. Eur J Clin Microbiol Infect Dis 2020; 39: 1201-1208.
16. Momeni P, Abedin Dargoosh S, Sedehzadeh AA, Bagheri G, Mohammadi M, Poosashkan L, et al. Neuraminidase Gene Variations in Influenza A (H1N1) pdm09 Virus among Patients Admitted to Refferal Pulmonary Hospital, Tehran, Iran in 2009–2013. Tanaffos 2017; 16: 99-106.
17. Moasser E, Behzadian F, Moattari A, Fotouhi F, Zaraket H. Characterization of the neuraminidase genes from human influenza A viruses circulating in Iran from 2010 to 2015. Arch Virol 2018; 163: 391-400.
18. Khodadad N, Moattari A, Shamsi Shahr Abadi M, Kadivar MR, Sarvari J, Tavakoli F, et al. Prevalence of influenza A (H1N1) pdm09 virus resistant to oseltamivir in Shiraz, Iran, during 2012-2013. Jundishapur J Microbiol 2015; 8(8): e23690.
19. Moradi A, Nadji SA, Tabarsi P, Hashemian SM, Marjani M, Sigaroodi A, et al. Prevalence of oseltamivir-resistant 2009 H1N1 influenza virus among patients with pandemic 2009 H1N1 influenza infection in NRITLD, Tehran, Iran. Tanaffos 2011; 10: 8-11.
20. Koel BF, Vigeveno RM, Pater M, Koekkoek SM, Han AX, Tuan HM, et al. Longitudinal sampling is required to maximize detection of intrahost A/H3N2 virus variants. Virus Evol 2020; 6:veaa088.
21. Takashita E, Daniels RS, Fujisaki S, Gregory V, Gubareva LV, Huang W, et al. Global update on the susceptibilities of human influenza viruses to neuraminidase inhibitors and the cap-dependent endonuclease inhibitor baloxavir, 2017–2018. Antiviral Res 2020; 175: 104718.
22. Akand EH, Downard KM. Mechanisms of antiviral resistance in influenza neuraminidase revealed by a mass spectrometry based phylonumerics approach. Mol Phylogenet Evol 2019; 135: 286-296.
23. Pires De Mello CP, Drusano GL, Adams JR, Shudt M, Kulawy R, Brown AN. Oseltamivir-zanamivir combination therapy suppresses drug-resistant H1N1 influenza A viruses in the hollow fiber infection model (HFIM) system. Eur J Pharm Sci 2018; 111: 443-449.
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: 449-457.
25. Job ER, Schotsaert M, Ibañez LI, Smet A, Ysenbaert T, Roose K, et al. Antibodies directed toward neuraminidase N1 control disease in a mouse model of influenza. J Virol 2018; 92(4): e01584-17.
26. Sedova ES, Scherbinin DN, Lysenko AA, Alekseeva SV, Artemova EA, Shmarov MM. Non-neutralizing antibodies directed at conservative influenza antigens. Acta Naturae 2019; 11: 22-32.
27. McMillan CLD, Young PR, Watterson D, Chappell KJ. The next generation of influenza vaccines: Towards a universal solution. Vaccines (Basel) 2021; 9: 26.
28. Yavarian J, Shafiei Jandaghi NZ, Naseri M, Mokhtari Azad T. Characterization of variations in PB2, NS1, M, neuraminidase and hemagglutinin of influenza A (H3N2) viruses in Iran. Jundishapur J Microbiol 2014; 7(3): e9089.
29. Liang L, Huang P, Wen M, Ni H, Tan S, Zhang Y, et al. Epitope peptides of influenza H3N2 virus neuraminidase gene designed by immunoinformatics. Acta Biochim Biophys Sin (Shanghai) 2012; 44: 113-118.
30. Kaplan BS, Anderson TK, Chang J, Santos J, Perez D, Lewis N, et al. Evolution and antigenic advancement of N2 neuraminidase of swine influenza A viruses circulating in the United States following two separate introductions from human seasonal viruses. J Virol 2021; 95(20): e0063221.
31. Liu B, Wang Y, Liu Y, Chen Y, Liu Y, Cong X, et al. Molecular evolution and characterization of hemagglutinin and neuraminidase of influenza A (H1N1) pdm09 viruses isolated in Beijing, China, during the 2017–2018 and 2018–2019 influenza seasons. Arch Virol 2021; 166: 179-189.
32. Mohan T, Nguyen HT, Kniss K, Mishin VP, Merced-Morales AA, Laplante J, et al. Cluster of Oseltamivir-Resistant and Hemagglutinin Antigenically Drifted Influenza A (H1N1) pdm09 Viruses, Texas, USA, January 2020. Emerg Infect Dis 2021; 27: 1953-1957.
33. Lee N, Hurt AC. Neuraminidase inhibitor resistance in influenza: a clinical perspective. Curr Opin Infect Dis 2018; 31: 520-526.
34. Principi N, Camilloni B, Alunno A, Polinori I, Argentiero A, Esposito S. Drugs for influenza treatment: is there significant news? Front Med (Lausanne) 2019; 6: 109.
35. Bai Y, Jones JC, Wong S-S, Zanin M. Antivirals targeting the surface glycoproteins of Influenza virus: Mechanisms of action and resistance. Viruses 2021; 13: 624.
36. Yavarian J, Mokhtari-Azad T, Nadji SA, Zeraati H, Naseri M. Analysis of the hemagglutinin and neuraminidase genes of human Influenza A/H3N2 viruses circulating in iran between 2005 and 2007: antigenic and phylogenetic relationships to vaccine strains. Intervirology 2010; 53: 133-140.
37. Simon P, Holder BP, Bouhy X, Abed Y, Beauchemin CA, Boivin G. 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.
38. Okomo-Adhiambo M, Demmler-Harrison GJ, Deyde VM, Sheu TG, Xu X, Klimov AI, 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.
39. Van Poelvoorde LAE, Saelens X, Thomas I, Roosens NH. Next-generation sequencing: an eye-opener for the surveillance of antiviral resistance in influenza. Trends Biotechnol 2020; 38: 360-367.
40. McGinnis J, Laplante J, Shudt M, George KS. Next generation sequencing for whole genome analysis and surveillance of influenza A viruses. J Clin Virol 2016; 79: 44-50.
41. McAuley JL, Gilbertson BP, Trifkovic S, Brown LE, McKimm-Breschkin JL. Influenza virus neuraminidase structure and functions. Front Microbiol 2019; 10: 39.
42. Powell H, Pekosz A. Neuraminidase antigenic drift of H3N2 clade 3c. 2a viruses alters virus replication, enzymatic activity and inhibitory antibody binding. PLoS Pathog 2020; 16(6): e1008411.
43. Wan H, Gao J, Yang H, Yang S, Harvey R, Chen Y-Q, et al. The neuraminidase of A (H3N2) influenza viruses circulating since 2016 is antigenically distinct from the A/Hong Kong/4801/2014 vaccine strain. Nat Microbiol 2019; 4: 2216-2225.
44. Zost SJ, Parkhouse K, Gumina ME, Kim K, Diaz Perez S, Wilson PC, et al. Contemporary H3N2 influenza viruses have a glycosylation site that alters binding of antibodies elicited by egg-adapted vaccine strains. Proc Natl Acad Sci U S A 2017; 114: 12578-12583.
45. Bashir Aamir U, Badar N, Mehmood MR, Nisar N, Suleman RM, Shaukat S, et al. Molecular epidemiology of influenza A (H1N1) pdm09 viruses from Pakistan in 2009–2010. PLoS One 2012; 7(8): e41866.
46. Jandaghi NZ, Azad TM, Naseri M, Yavarian J, Nategh R. Molecular and genetic characteristics of hemagglutinin and neuraminidase in Iranian 2009 pandemic influenza A (H1N1) viruses. Arch Virol 2010; 155: 717-721.
47. Al Khatib HA, Al Thani AA, Gallouzi I, Yassine HM. Epidemiological and genetic characterization of pH1N1 and H3N2 influenza viruses circulated in MENA region during 2009–2017. BMC Infect Dis 2019; 19: 314.
48. Isakova-Sivak I, Stepanova E, Mezhenskaya D, Matyushenko V, Prokopenko P, Sychev I, et al. Influenza vaccine: Progress in a vaccine that elicits a broad immune response. Expert Rev Vaccines 2021; 20: 1097-1112.
| Files | ||
| Issue | Vol 14 No 4 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v14i4.10241 | |
| Keywords | ||
| Influenza A viruses; Neuraminidase; Oseltamivir; Antiviral drug; Iran | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Gholami A, Shafiei-Jandaghi NZ, Ghavami N, Tavakoli F, Yavarian J, Mokhtari-Azad T. Assessment of influenza A (H1N1, H3N2) oseltamivir resistance during 2017-2019 in Iran. Iran J Microbiol. 2022;14(4):545-553.
