Oseltamivir-resistant influenza A (H1N1) virus strain with an H274Y mutation in neuraminidase persists without drug pressure in infected mallards

Applied and Environmental Microbiology

Volumn 81, Issue 7, 2015, Pages 2378-2383

  Gillman, Anna ^a   Muradrasoli, Shaman ^a,b   Söderström, Hanna ^c   Holmberg, Fredrik ^a   Latorre Margalef, Neus ^d,f   Tolf, Conny ^d   Waldenström, Jonas ^d   Gunnarsson, Gunnar ^e   Olsen, Björn ^a   Järhult, Josef D ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^c UMEÅ UNIVERSITY   (Sweden)

^d LINNAEUS UNIVERSITY   (Sweden)

^e KRISTIANSTAD UNIVERSITY   (Sweden)

^f UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIRDS; CARBOXYLATION; HEALTH RISKS; RESERVOIRS (WATER); SEWAGE TREATMENT;

FECAL SAMPLES; INFLUENZA A VIRUS; INFLUENZA PANDEMICS; NEURAMINIDASE; OSELTAMIVIR CARBOXYLATE; VIRAL FITNESS; VIRAL VARIANTS; VIRUS STRAINS;

VIRUSES;

BIRD; CONCENTRATION (COMPOSITION); DISEASE TRANSMISSION; DRUG; DRUG RESISTANCE; GENE EXPRESSION; INFLUENZA; MUTATION; VIRUS; WILD POPULATION;

ANAS; ANAS PLATYRHYNCHOS; ANATIDAE; AVES; INFLUENZA A VIRUS;

ANTIVIRUS AGENT; MUTANT PROTEIN; NA PROTEIN, INFLUENZA A VIRUS; OSELTAMIVIR; SIALIDASE; VIRAL PROTEIN;

AMINO ACID SUBSTITUTION; ANIMAL; ANTIVIRAL RESISTANCE; AVIAN INFLUENZA; DRUG EFFECTS; DUCK; FECES; GENETIC SELECTION; GENETICS; INFLUENZA A VIRUS (H1N1); ISOLATION AND PURIFICATION; MISSENSE MUTATION; VIROLOGY;

AMINO ACID SUBSTITUTION; ANIMALS; ANTIVIRAL AGENTS; DRUG RESISTANCE, VIRAL; DUCKS; FECES; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA IN BIRDS; MUTANT PROTEINS; MUTATION, MISSENSE; NEURAMINIDASE; OSELTAMIVIR; SELECTION, GENETIC; VIRAL PROTEINS;

EID: 84925379512     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.04034-14     Document Type: Article

References (35)

1. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. 1992. Evolution and ecology of influenza A viruses. Microbiol Rev 56:152-179.
2. Olsen B, Munster VJ, Wallensten A, Waldenström J, Osterhaus AD, Fouchier RA. 2006. Global patterns of influenza A virus in wild birds. Science 312:384-388. http://dx.doi.org/10.1126/science.1122438.
3. Brockwell-Staats C, Webster RG, Webby RJ. 2009. Diversity of influenza viruses in swine and the emergence of a novel human pandemic influenza A (H1N1). Influenza Other Respir Viruses 3:207-213. http://dx.doi.org /10.1111/j.1750-2659.2009.00096.x.
4. Latorre-Margalef N, Gunnarsson G, Munster VJ, Fouchier RA, Osterhaus AD, Elmberg J, Olsen B, Wallensten A, Haemig PD, Fransson T, Brudin L, Waldenström J. 2009. Effects of influenza A virus infection on migrating mallard ducks. Proc Biol Sci 276:1029-1036. http://dx.doi.org /10.1098/rspb.2008.1501.
5. Dugan VG, Chen R, Spiro DJ, Sengamalay N, Zaborsky J, Ghedin E, Nolting J, Swayne DE, Runstadler JA, Happ GM, Senne DA, Wang R, Slemons RD, Holmes EC, Taubenberger JK. 2008. The evolutionary genetics and emergence of avian influenza viruses in wild birds. PLoS Pathog 4:e1000076. http://dx.doi.org/10.1371/journal.ppat.1000076.
6. Liu D, Shi W, Shi Y, Wang D, Xiao H, Li W, Bi Y, Wu Y, Li X, Yan J, Liu W, Zhao G, Yang W, Wang Y, Ma J, Shu Y, Lei F, Gao GF. 2013. Origin and diversity of novel avian influenza A H7N9 viruses causing human infection: phylogenetic, structural, and coalescent analyses. Lancet 381:1926-1932. http://dx.doi.org/10.1016/S0140-6736(13)60938-1.
7. Patel A, Gorman SE. 2009. Stockpiling antiviral drugs for the next influenza pandemic. Clin Pharmacol Ther 86:241-243. http://dx.doi.org/10.1038/clpt.2009.142.
8. Wan Po AL, Farndon P, Palmer N. 2009. Maximizing the value of drug stockpiles for pandemic influenza. Emerg Infect Dis 15:1686-1687. http: //dx.doi.org/10.3201/eid1510.090844.
9. World Health Organization. 2012. Meetings of the WHO working group on surveillance of influenza antiviral susceptibility-Geneva, November 2011 and June 2012. Wkly Epidemiol Rec 87:369-374.
10. Samson M, Pizzorno A, Abed Y, Boivin G. 2013. Influenza virus resistance to neuraminidase inhibitors. Antiviral Res 98:174-185. http://dx.doi.org/10.1016/j.antiviral.2013.03.014.
11. Kiso M, Mitamura K, Sakai-Tagawa Y, Shiraishi K, Kawakami C, Kimura K, Hayden FG, Sugaya N, Kawaoka Y. 2004. Resistant influenza A viruses in children treated with oseltamivir: descriptive study. Lancet 364:759-765. http://dx.doi.org/10.1016/S0140-6736(04)16934-1.
12. de Jong MD, Tran TT, Truong HK, Vo MH, Smith GJ, Nguyen VC, Bach VC, Phan TQ, Do QH, Guan Y, Peiris JS, Tran TH, Farrar J. 2005. Oseltamivir resistance during treatment of influenza A (H5N1) infection. N Engl J Med 353:2667-2672. http://dx.doi.org/10.1056/NEJMoa054512.
13. Hu Y, Lu S, Song Z, Wang W, Hao P, Li J, Zhang X, Yen HL, Shi B, Li T, Guan W, Xu L, Liu Y, Wang S, Zhang X, Tian D, Zhu Z, He J, Huang K, Chen H, Zheng L, Li X, Ping J, Kang B, Xi X, Zha L, Li Y, Zhang Z, Peiris M, Yuan Z. 2013. Association between adverse clinical outcome in human disease caused by novel influenzaAH7N9virus and sustained viral shedding and emergence of antiviral resistance. Lancet 381:2273-2279. http://dx.doi.org/10.1016/S0140-6736(13)61125-3.
14. Moscona A. 2009. Global transmission of oseltamivir-resistant influenza. N Engl J Med 360:953-956. http://dx.doi.org/10.1056/NEJMp0900648.
15. Butler J, Hooper KA, Petrie S, Lee R, Maurer-Stroh S, Reh L, Guarnaccia T, Baas C, Xue L, Vitesnik S, Leang SK, McVernon J, Kelso A, Barr IG, McCaw JM, Bloom JD, Hurt AC. 2014. Estimating the fitness advantage conferred by permissive neuraminidase mutations in recent oseltamivir-resistant A(H1N1)pdm09 influenza viruses. PLoS Pathog 10: e1004065. http://dx.doi.org/10.1371/journal.ppat.1004065.
16. Fick J, Lindberg RH, Tysklind M, Haemig PD, Waldenström J, Wallensten A, Olsen B. 2007. Antiviral oseltamivir is not removed or degraded in normal sewage water treatment: implications for development of resistance by influenza A virus. PLoS One 2:e986. http://dx.doi.org/10.1371/journal.pone.0000986.
17. Ghosh GC, Nakada N, Yamashita N, Tanaka H. 2010. Occurrence and fate of oseltamivir carboxylate (Tamiflu) and amantadine in sewage treatment plants. Chemosphere 81:13-17. http://dx.doi.org/10.1016/j.chemosphere.2010.07.023.
18. Takanami R, Ozaki H, Giri RR, Taniguchi S, Hayashi S. 2010. Detection of antiviral drugs oseltamivir phosphate and oseltamivir carboxylate in Neya River, Osaka, Japan. J Water Environ Technol 8:363-372. http://dx.doi.org/10.2965/jwet.2010.363.
19. Söderström H, Järhult JD, Olsen B, Lindberg RH, Tanaka H, Fick J. 2009. Detection of the antiviral drug oseltamivir in aquatic environments. PLoS One 4:e6064. http://dx.doi.org/10.1371/journal.pone.0006064.
20. Azuma T, Nakada N, Yamashita N, Tanaka H. 2012. Synchronous dynamics of observed and predicted values of anti-influenza drugs in environmental waters during a seasonal influenza outbreak. Environ Sci Technol 46:12873-12881. http://dx.doi.org/10.1021/es303203c.
21. Järhult JD. 21 June 2012. Oseltamivir (Tamiflu®) in the environment, resistance development in influenza A viruses of dabbling ducks and the risk of transmission of an oseltamivir-resistant virus to humans-a review. Infect Ecol Epidemiol 2:10.3402/iee.v2i0.18385. http://dx.doi.org /10.3402/iee.v2i0.18385.
22. Monto AS, Webster RG. 2013. Influenza pandemics: history and lessons learned, p 20-34. In Webster RG, Monto AS, Braciale TJ, Lamb RA (ed), Textbook of influenza, 2nd ed. John Wiley & Sons, Ltd, Oxford, United Kingdom.
23. Järhult JD, Muradrasoli S, Wahlgren J, Söderström H, Orozovic G, Gunnarsson G, Bröjer C, Latorre-Margalef N, Fick J, Grabic R, Lennerstrand J, Waldenström J, Lundkvist A, Olsen B. 2011. Environmental levels of the antiviral oseltamivir induce development of resistance mutation H274Y in influenza A/H1N1 virus in mallards. PLoS One 6:e24742. http://dx.doi.org/10.1371/journal.pone.0024742.
24. Gillman A, Muradrasoli S, Söderström H, Nordh J, Bröjer C, Lindberg RH, Latorre-Margalef N, Waldenström J, Olsen B, Järhult JD. 2013. Resistance mutation R292K is induced in influenza A(H6N2) virus by exposure of infected mallards to low levels of oseltamivir. PLoS One 8:e71230. http://dx.doi.org/10.1371/journal.pone.0071230.
25. Achenbach JE, Bowen RA. 2013. Effect of oseltamivir carboxylate consumption on emergence of drug-resistant H5N2 avian influenza virus in mallard ducks. Antimicrob Agents Chemother 57:2171-2181. http://dx.doi.org/10.1128/AAC.02126-12.
26. Reed LJ, Muench H. 1938. A simple method of estimating fifty percent endpoints. Am J Hyg 27:493-497.
27. Spackman E, Suarez DL. 2008. Type A influenza virus detection and quantitation by real-time RT-PCR. Methods Mol Biol 436:19-26. http: //dx.doi.org/10.1007/978-1-59745-279-3_4.
28. Potier M, Mameli L, Belisle M, Dallaire L, Melancon SB. 1979. Fluorometric assay of neuraminidase with a sodium (4-methylumbelliferyl-α-DGillman N-acetylneuraminate) substrate. Anal Biochem 94:287-296. http://dx.doi.org/10.1016/0003-2697(79)90362-2.
29. Russell CA, Fonville JM, Brown AE, Burke DF, Smith DL, James SL, Herfst S, van Boheemen S, Linster M, Schrauwen EJ, Katzelnick L, Mosterin A, Kuiken T, Maher E, Neumann G, Osterhaus AD, Kawaoka Y, Fouchier RA, Smith DJ. 2012. The potential for respiratory droplettransmissible A/H5N1 influenza virus to evolve in a mammalian host. Science 336:1541-1547. http://dx.doi.org/10.1126/science.1222526.
30. Bröjer C, Järhult JD, Muradrasoli S, Söderström H, Olsen B, Gavier-Widen D. 2013. Pathobiology and virus shedding of low-pathogenic avian influenza virus (A/H1N1) infection in mallards exposed to oseltamivir. J Wildl Dis 49:103-113. http://dx.doi.org/10.7589/2011-11-335.
31. Bloom JD, Gong LI, Baltimore D. 2010. Permissive secondary mutations enable the evolution of influenza oseltamivir resistance. Science 328: 1272-1275. http://dx.doi.org/10.1126/science.1187816.
32. Duan S, Govorkova EA, Bahl J, Zaraket H, Baranovich T, Seiler P, Prevost K, Webster RG, Webby RJ. 2014. Epistatic interactions between neuraminidase mutations facilitated the emergence of the oseltamivirresistant H1N1 influenza viruses. Nat Commun 5:5029. http://dx.doi.org /10.1038/ncomms6029.
33. Pizzorno A, Abed Y, Bouhy X, Beaulieu E, Mallett C, Russell R, Boivin G. 2012. Impact of mutations at residue I223 of the neuraminidase protein on the resistance profile, replication level, and virulence of the 2009 pandemic influenza virus. Antimicrob Agents Chemother 56:1208-1214. http://dx.doi.org/10.1128/AAC.05994-11.
34. Huang L, Cao Y, Zhou J, Qin K, Zhu W, Zhu Y, Yang L, Wang D, Wei H, Shu Y. 2014. A conformational restriction in the influenza A virus neuraminidase binding site by R152 results in a combinational effect of I222T and H274Y on oseltamivir resistance. Antimicrob Agents Chemother 58:1639-1645. http://dx.doi.org/10.1128/AAC.01848-13.
35. Azuma T, Nakada N, Yamashita N, Tanaka H. 2013. Mass balance of anti-influenza drugs discharged into the Yodo River system, Japan, under an influenza outbreak. Chemosphere 93:1672-1677. http://dx.doi.org/10.1016/j.chemosphere.2013.05.025.