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Review Articles

Risk of resistant avian influenza A virus in wild waterfowl as a result of environmental release of oseltamivir

, MD, PhD
Article: 32870 | Received 12 Jul 2016, Accepted 13 Sep 2016, Published online: 11 Oct 2016

References

  • Fields BN, Knipe DM, Howley PM. Fields’ virology. 2007; 5th ed, Philadelphia, PA: Lippincott Williams & Wilkins.
  • Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev. 1992; 56: 152–79.
  • Olsen B, Munster VJ, Wallensten A, Waldenström J, Osterhaus AD, Fouchier RA. Global patterns of influenza A virus in wild birds. Science. 2006; 312: 384–8.
  • Brockwell-Staats C, Webster RG, Webby RJ. Diversity of influenza viruses in swine and the emergence of a novel human pandemic influenza A (H1N1). Influenza Other Respir Viruses. 2009; 3: 207–13.
  • Cox NJ, Subbarao K. Global epidemiology of influenza: past and present. Annu Rev Med. 2000; 51: 407–21.
  • Monto AS, Webster RG. Webster RG, Monto AS, Braciale TJ, Lamb RA. Influenza pandemics: history and lessons learned. Textbook of influenza. 2013; 2nd ed, Oxford, UK: Wiley. 20–34.
  • To KK, Chan JF, Chen H, Li L, Yuen KY. The emergence of influenza A H7N9 in human beings 16 years after influenza A H5N1: a tale of two cities. Lancet Infect Dis. 2013; 13: 809–21.
  • Abdel-Ghafar AN, Chotpitayasunondh T, Gao Z, Hayden FG, Nguyen DH, de Jong MD, etal. Update on avian influenza A (H5N1) virus infection in humans. N Engl J Med. 2008; 358: 261–73.
  • Tanner WD, Toth DJ, Gundlapalli AV. The pandemic potential of avian influenza A(H7N9) virus: a review. Epidemiol Infect. 2015; 143: 3359–74.
  • Fiore AE, Uyeki TM, Broder K, Finelli L, Euler GL, Singleton JA, etal. Prevention and control of influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2010. MMWR Recomm Rep. 2010; 59: 1–62.
  • Partridge J, Kieny MP. Global production of seasonal and pandemic (H1N1) influenza vaccines in 2009–2010 and comparison with previous estimates and global action plan targets. Vaccine. 2010; 28: 4709–12.
  • Nguyen-Van-Tam JS, Bresee J. Webster RG, Monto AS, Braciale TJ, Lamb RA. Pandemic preparedness and response. Textbook of influenza. 2013; 2nd ed, Oxford, UK: Wiley. 453–69.
  • Webster RG, Govorkova EA. Continuing challenges in influenza. Ann N Y Acad Sci. 2014; 1323: 115–39.
  • WHO. Meetings of the WHO working group on surveillance of influenza antiviral susceptibility – Geneva, November 2011 and June 2012. Wkly Epidemiol Rec. 2012; 87: 369–74.
  • Hurt AC, Besselaar TG, Daniels RS, Ermetal B, Fry A, Gubareva L, etal. Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2014–2015. Antiviral Res. 2016; 132: 178–85.
  • Ison MG, Hay A. Webster RG, Monto AS, Braciale TJ, Lamb RA. Antivirals: targets and use. Textbook of influenza. 2013; 2nd ed, Oxford, UK: Wiley. 392–418.
  • Patel A, Gorman SE. Stockpiling antiviral drugs for the next influenza pandemic. Clin Pharmacol Ther. 2009; 86: 241–3.
  • Wan Po AL, Farndon P, Palmer N. Maximizing the value of drug stockpiles for pandemic influenza. Emerg Infect Dis. 2009; 15: 1686–7.
  • Smith JR, Rayner CR, Donner B, Wollenhaupt M, Klumpp K, Dutkowski R. Oseltamivir in seasonal, pandemic, and avian influenza: a comprehensive review of 10-years clinical experience. Adv Ther. 2011; 28: 927–59.
  • Russell RJ, Haire LF, Stevens DJ, Collins PJ, Lin YP, Blackburn GM, etal. The structure of H5N1 avian influenza neuraminidase suggests new opportunities for drug design. Nature. 2006; 443: 45–9.
  • Russel RJ, Gamblin SJ, Skehel JJ. Webster RG, Monto AS, Braciale TJ, Lamb RA. Influenza glycoproteins: hemagglutinin and neuraminidase. Textbook of influenza. 2013; 2nd ed, Oxford, UK: Wiley. 67–100.
  • Samson M, Pizzorno A, Abed Y, Boivin G. Influenza virus resistance to neuraminidase inhibitors. Antiviral Res. 2013; 98: 174–85.
  • McKimm-Breschkin JL. Influenza neuraminidase inhibitors: antiviral action and mechanisms of resistance. Influenza Other Respir Viruses. 2013; 7(Suppl 1): 25–36.
  • Colman PM, Hoyne PA, Lawrence MC. Sequence and structure alignment of paramyxovirus hemagglutinin-neuraminidase with influenza virus neuraminidase. J Virol. 1993; 67: 2972–80.
  • Ferraris O, Lina B. Mutations of neuraminidase implicated in neuraminidase inhibitors resistance. J Clin Virol. 2008; 41: 13–19.
  • Tai CY, Escarpe PA, Sidwell RW, Williams MA, Lew W, Wu H, etal. Characterization of human influenza virus variants selected in vitro in the presence of the neuraminidase inhibitor GS 4071. Antimicrob Agents Chemother. 1998; 42: 3234–41.
  • Gubareva LV, Robinson MJ, Bethell RC, Webster RG. Catalytic and framework mutations in the neuraminidase active site of influenza viruses that are resistant to 4-guanidino-Neu5Ac2en. J Virol. 1997; 71: 3385–90.
  • McKimm-Breschkin JL, Sahasrabudhe A, Blick TJ, McDonald M, Colman PM, Hart GJ, etal. Mutations in a conserved residue in the influenza virus neuraminidase active site decreases sensitivity to Neu5Ac2en-derived inhibitors. J Virol. 1998; 72: 2456–62.
  • Kiso M, Mitamura K, Sakai-Tagawa Y, Shiraishi K, Kawakami C, Kimura K, etal. Resistant influenza A viruses in children treated with oseltamivir: descriptive study. Lancet. 2004; 364: 759–65.
  • Whitley RJ, Boucher CA, Lina B, Nguyen-Van-Tam JS, Osterhaus A, Schutten M, etal. Global assessment of resistance to neuraminidase inhibitors, 2008–2011: the Influenza Resistance Information Study (IRIS). Clin Infect Dis. 2013; 56: 1197–205.
  • Gubareva LV, Kaiser L, Matrosovich MN, Soo-Hoo Y, Hayden FG. Selection of influenza virus mutants in experimentally infected volunteers treated with oseltamivir. J Infect Dis. 2001; 183: 523–31.
  • De Jong MD, Tran TT, Truong HK, Vo MH, Smith GJ, Nguyen VC, etal. Oseltamivir resistance during treatment of influenza A (H5N1) infection. N Engl J Med. 2005; 353: 2667–72.
  • Hu Y, Lu S, Song Z, Wang W, Hao P, Li J, etal. Association between adverse clinical outcome in human disease caused by novel influenza A H7N9 virus and sustained viral shedding and emergence of antiviral resistance. Lancet. 2013; 381: 2273–9.
  • Eshaghi A, Shalhoub S, Rosenfeld P, Li A, Higgins RR, Stogios PJ, etal. Multiple influenza A (H3N2) mutations conferring resistance to neuraminidase inhibitors in a bone marrow transplant recipient. Antimicrob Agents Chemother. 2014; 58: 7188–97.
  • Thorlund K, Awad T, Boivin G, Thabane L. Systematic review of influenza resistance to the neuraminidase inhibitors. BMC Infect Dis. 2011; 11: 134.
  • Van der Vries E, Stelma FF, Boucher CA. Emergence of a multidrug-resistant pandemic influenza A (H1N1) virus. N Engl J Med. 2010; 363: 1381–2.
  • Moscona A. Global transmission of oseltamivir-resistant influenza. N Engl J Med. 2009; 360: 953–6.
  • Storms AD, Gubareva LV, Su S, Wheeling JT, Okomo-Adhiambo M, Pan CY, etal. Oseltamivir-resistant pandemic (H1N1) 2009 virus infections, United States, 2010–11. Emerg Infect Dis. 2012; 18: 308–11.
  • Lackenby A, Moran Gilad J, Pebody R, Miah S, Calatayud L, Bolotin S, etal. Continued emergence and changing epidemiology of oseltamivir-resistant influenza A(H1N1)2009 virus, United Kingdom, winter 2010/11. Euro Surveill. 2011; 16: 1–16
  • Takashita E, Kiso M, Fujisaki S, Yokoyama M, Nakamura K, Shirakura M, etal. Characterization of a large cluster of influenza A(H1N1)pdm09 viruses cross-resistant to oseltamivir and peramivir during the 2013–2014 influenza season in Japan. Antimicrob Agents Chemother. 2015; 59: 2607–17.
  • Hurt AC, Hardie K, Wilson NJ, Deng YM, Osbourn M, Gehrig N, etal. Community transmission of oseltamivir-resistant A(H1N1)pdm09 influenza. N Engl J Med. 2011; 365: 2541–2.
  • Stoner TD, Krauss S, Turner JC, Seiler P, Negovetich NJ, Stallknecht DE, etal. Susceptibility of avian influenza viruses of the N6 subtype to the neuraminidase inhibitor oseltamivir. Antiviral Res. 2012; 93: 322–9.
  • Orozovic G, Orozovic K, Järhult JD, Olsen B. Study of oseltamivir and zanamivir resistance-related mutations in influenza viruses isolated from wild mallards in Sweden. PLoS One. 2014; 9: e89306.
  • Stoner TD, Krauss S, DuBois RM, Negovetich NJ, Stallknecht DE, Senne DA, etal. Antiviral susceptibility of avian and swine influenza virus of the N1 neuraminidase subtype. J Virol. 2010; 84: 9800–9.
  • LIFproduktresumé. Produktresumé FASS Relenza. 2015; LIF: Läkemedelsindustriföreningens Service AB. Available from: http://www.fass.se/LIF/product?userType=0&nplId=19990209000018&docType=3 [cited 18 January 2015]..
  • Fick J, Lindberg RH, Tysklind M, Haemig PD, Waldenström J, Wallensten A, etal. Antiviral oseltamivir is not removed or degraded in normal sewage water treatment: implications for development of resistance by influenza A virus. PLoS One. 2007; 2: e986.
  • Jain S, Kumar P, Vyas RK, Pandit P, Dalai AK. Occurrence and removal of antiviral drugs in environment: a review. Water Air Soil Pollut. 2013; 224: 1–19.
  • Azuma T, Nakada N, Yamashita N, Tanaka H. Synchronous dynamics of observed and predicted values of anti-influenza drugs in environmental waters during a seasonal influenza outbreak. Environ Sci Technol. 2012; 46: 12873–81.
  • Leknes H, Sturtzel IE, Dye C. Environmental release of oseltamivir from a Norwegian sewage treatment plant during the 2009 influenza A (H1N1) pandemic. Sci Total Environ. 2012; 414: 632–8.
  • Singer AC, Järhult JD, Grabic R, Khan GA, Lindberg RH, Fedorova G, etal. Intra- and inter-pandemic variations of antiviral, antibiotics and decongestants in wastewater treatment plants and receiving rivers. PLoS One. 2014; 9: e108621.
  • Ghosh GC, Nakada N, Yamashita N, Tanaka H. Oseltamivir carboxylate, the active metabolite of oseltamivir phosphate (Tamiflu), detected in sewage discharge and river water in Japan. Environ Health Perspect. 2010; 118: 103–7.
  • Prasse C, Schlusener MP, Schulz R, Ternes TA. Antiviral drugs in wastewater and surface waters: a new pharmaceutical class of environmental relevance?. Environ Sci Technol. 2010; 44: 1728–35.
  • Azuma T, Ishiuchi H, Inoyama T, Teranishi Y, Yamaoka M, Sato T, etal. Detection of peramivir and laninamivir, new anti-influenza drugs, in sewage effluent and river waters in Japan. PLoS One. 2015; 10: e0131412.
  • Tashiro M, McKimm-Breschkin JL, Saito T, Klimov A, Macken C, Zambon M, etal. Surveillance for neuraminidase-inhibitor-resistant influenza viruses in Japan, 1996–2007. Antivir Ther. 2009; 14: 751–61.
  • Hoffman-La-RocheINC. Pediatric Advisory Committee Briefing Document for Tamiflu® (RO 64-0796) PAC Briefing Document. 2007; Nutley, New Jersey: Hoffmann-La Roche Inc.
  • Söderström H, Järhult JD, Olsen B, Lindberg RH, Tanaka H, Fick J. Detection of the antiviral drug oseltamivir in aquatic environments. PLoS One. 2009; 4: e6064.
  • Takanami R, Ozaki H, Giri RR, Taniguchi S, Hayashi S. Detection of antiviral drugs oseltamivir phosphate and oseltamivir carboxylate in Neya River, Osaka Japan. J Water Environ Technol. 2010; 8: 363–72.
  • Takanami R, Ozaki H, Giri RR, Taniguchi S, Hayashi S. Antiviral drugs zanamivir and oseltamivir found in wastewater and surface water in Osaka, Japan. J Water Environ Technol. 2012; 10: 57–68.
  • Ghosh GC, Nakada N, Yamashita N, Tanaka H. Occurrence and fate of oseltamivir carboxylate (Tamiflu) and amantadine in sewage treatment plants. Chemosphere. 2010; 81: 13–17.
  • Azuma T, Nakada N, Yamashita N, Tanaka H. Mass balance of anti-influenza drugs discharged into the Yodo River system, Japan, under an influenza outbreak. Chemosphere. 2013; 93: 1672–7.
  • Singer AC, Järhult JD, Grabic R, Khan GA, Fedorova G, Fick J, etal. Compliance to oseltamivir among two populations in Oxfordshire, United Kingdom affected by influenza A(H1N1)pdm09, November 2009 – a waste water epidemiology study. PLoS One. 2013; 8: e60221.
  • Goncalves C, Perez S, Osorio V, Petrovic M, Alpendurada MF, Barcelo D. Photofate of oseltamivir (Tamiflu) and oseltamivir carboxylate under natural and simulated solar irradiation: kinetics, identification of the transformation products, and environmental occurrence. Environ Sci Technol. 2011; 45: 4307–14.
  • Chen WY, Lin CJ, Liao CM. Assessing exposure risks for aquatic organisms posed by Tamiflu use under seasonal influenza and pandemic conditions. Environ Pollut. 2014; 184: 377–84.
  • Straub JO. An environmental risk assessment for oseltamivir (Tamiflu) for sewage works and surface waters under seasonal-influenza- and pandemic-use conditions. Ecotoxicol Environ Saf. 2009; 72: 1625–34.
  • Singer AC, Johnson AC, Anderson PD, Snyder SA. Reassessing the risks of Tamiflu use during a pandemic to the Lower Colorado River. Environ Health Perspect. 2008; 116: A285–6.
  • Singer AC, Nunn MA, Gould EA, Johnson AC. Potential risks associated with the proposed widespread use of Tamiflu. Environ Health Perspect. 2007; 115: 102–6.
  • Bartels P, von Tumpling W Jr. The environmental fate of the antiviral drug oseltamivir carboxylate in different waters. Sci Total Environ. 2008; 405: 215–25.
  • Boreen AL, Arnold WA, McNeill K. Photodegradation of pharmaceuticals in the aquatic environment: a review. Aquat Sci. 2003; 65: 320–41.
  • Accinelli C, Sacca ML, Fick J, Mencarelli M, Lindberg R, Olsen B. Dissipation and removal of oseltamivir (Tamiflu) in different aquatic environments. Chemosphere. 2010; 79: 891–7.
  • Accinelli C, Caracciolo AB, Grenni P. Degradation of the antiviral drug oseltamivir carboxylate in surface water samples. Int J Environ Anal Chem. 2007; 87: 579–87.
  • Slater FR, Singer AC, Turner S, Barr JJ, Bond PL. Pandemic pharmaceutical dosing effects on wastewater treatment: no adaptation of activated sludge bacteria to degrade the antiviral drug oseltamivir (Tamiflu(R)) and loss of nutrient removal performance. FEMS Microbiol Lett. 2011; 315: 17–22.
  • Sacca ML, Accinelli C, Fick J, Lindberg R, Olsen B. Environmental fate of the antiviral drug Tamiflu in two aquatic ecosystems. Chemosphere. 2009; 75: 28–33.
  • Accinelli C, Saccà ML, Batisson I, Fick J, Mencarelli M, Grabic R. Removal of oseltamivir (Tamiflu) and other selected pharmaceuticals from wastewater using a granular bioplastic formulation entrapping propagules of Phanerochaete chrysosporium. Chemosphere. 2010; 81: 436–43.
  • Mestankova H, Schirmer K, Escher BI, von Gunten U, Canonica S. Removal of the antiviral agent oseltamivir and its biological activity by oxidative processes. Environ Pollut. 2012; 161: 30–5.
  • Fedorova G, Grabic R, Nyhlen J, Järhult JD, Söderström H. Fate of three anti-influenza drugs during ozonation of wastewater effluents – degradation and formation of transformation products. Chemosphere. 2016; 150: 723–30.
  • Munster VJ, Baas C, Lexmond P, Waldenström J, Wallensten A, Fransson T, etal. Spatial, temporal, and species variation in prevalence of influenza A viruses in wild migratory birds. PLoS Pathog. 2007; 3: e61.
  • Krauss S, Walker D, Pryor SP, Niles L, Chenghong L, Hinshaw VS, etal. 2004. Influenza A viruses of migrating wild aquatic birds in North America. Vector Borne Zoonotic Dis. 2004; 4: 177–89.
  • Fouchier RAM, Guan Y. Webster RG, Monto AS, Braciale TJ, Lamb RA. Ecology and evolution of influenza viruses in wild and domesticated birds. Textbook of influenza. 2013; Oxford, UK: Wiley. 175–89.
  • Latorre-Margalef N, Tolf C, Grosbois V, Avril A, Bengtsson D, Wille M, etal. Long-term variation in influenza A virus prevalence and subtype diversity in migratory mallards in northern Europe. Proc Biol Sci. 2014; 281: 20140098.
  • Gaidet N, Ould El Mamy AB, Cappelle J, Caron A, Cumming GS, Grosbois V, etal. Investigating avian influenza infection hotspots in old-world shorebirds. PLoS One. 2012; 7: e46049.
  • Krauss S, Stallknecht DE, Negovetich NJ, Niles LJ, Webby RJ, Webster RG. Coincident ruddy turnstone migration and horseshoe crab spawning creates an ecological ‘hot spot’ for influenza viruses. Proc Biol Sci. 2010; 277: 3373–9.
  • Jourdain E, Gunnarsson G, Wahlgren J, Latorre-Margalef N, Bröjer C, Sahlin S, etal. Influenza virus in a natural host, the mallard: experimental infection data. PLoS One. 2010; 5: e8935.
  • Latorre-Margalef N, Gunnarsson G, Munster VJ, Fouchier RA, Osterhaus AD, Elmberg J, etal. Effects of influenza A virus infection on migrating mallard ducks. Proc Biol Sci. 2009; 276: 1029–36.
  • Wallensten A, Munster VJ, Karlsson M, Lundkvist Å, Brytting M, Stervander M, etal. High prevalence of influenza A virus in ducks caught during spring migration through Sweden. Vaccine. 2006; 24: 6734–5.
  • Hill NJ, Takekawa JY, Ackerman JT, Hobson KA, Herring G, Cardona CJ, etal. Migration strategy affects avian influenza dynamics in mallards (Anas platyrhynchos). Mol Ecol. 2012; 21: 5986–99.
  • Lewis NS, Verhagen JH, Javakhishvili Z, Russell CA, Lexmond P, Westgeest KB, etal. Influenza A virus evolution and spatio-temporal dynamics in Eurasian wild birds: a phylogenetic and phylogeographical study of whole-genome sequence data. J Gen Virol. 2015; 96: 2050–60.
  • Dugan VG, Chen R, Spiro DJ, Sengamalay N, Zaborsky J, Ghedin E, etal. The evolutionary genetics and emergence of avian influenza viruses in wild birds. PLoS Pathog. 2008; 4: e1000076.
  • Chen R, Holmes EC. Hitchhiking and the population genetic structure of avian influenza virus. J Mol Evol. 2010; 70: 98–105.
  • Russell CA, Fonville JM, Brown AE, Burke DF, Smith DL, James SL, etal. The potential for respiratory droplet-transmissible A/H5N1 influenza virus to evolve in a mammalian host. Science. 2012; 336: 1541–7.
  • Chen R, Holmes EC. Avian influenza virus exhibits rapid evolutionary dynamics. Mol Biol Evol. 2006; 23: 2336–41.
  • Forrest HL, Webster RG. Perspectives on influenza evolution and the role of research. Anim Health Res Rev. 2010; 11: 3–18.
  • Järhult JD, Muradrasoli S, Wahlgren J, Söderström H, Orozovic G, Gunnarsson G, etal. Environmental levels of the antiviral oseltamivir induce development of resistance mutation H274Y in influenza A/H1N1 virus in mallards. PLoS One. 2011; 6: e24742.
  • Achenbach JE, Bowen RA. Effect of oseltamivir carboxylate consumption on emergence of drug-resistant H5N2 avian influenza virus in Mallard ducks. Antimicrob Agents Chemother. 2013; 57: 2171–81.
  • Gillman A, Muradrasoli S, Söderström H, Nordh J, Bröjer C, Lindberg RH, etal. Resistance mutation R292K is induced in influenza A(H6N2) virus by exposure of infected mallards to low levels of oseltamivir. PLoS One. 2013; 8: e71230.
  • Gillman A, Nykvist M, Muradrasoli S, Söderström H, Wille M, Daggfeldt A, etal. Influenza A(H7N9) virus acquires resistance-related neuraminidase I222T substitution when infected mallards are exposed to low levels of oseltamivir in water. Antimicrob Agents Chemother. 2015; 59: 5196–202.
  • Gillman A, Muradrasoli S, Söderström H, Holmberg F, Latorre-Margalef N, Tolf C, etal. Oseltamivir-resistant influenza A (H1N1) virus strain with an H274Y mutation in neuraminidase persists without drug pressure in infected mallards. Appl Environ Microbiol. 2015; 81: 2378–83.
  • Gillman A, Muradrasoli S, Mardnas A, Söderström H, Fedorova G, Lowenthal M, etal. Oseltamivir resistance in influenza A(H6N2) caused by an R292K substitution in neuraminidase is not maintained in mallards without drug pressure. PLoS One. 2015; 10: e0139415.
  • Bloom JD, Gong LI, Baltimore D. Permissive secondary mutations enable the evolution of influenza oseltamivir resistance. Science. 2010; 328: 1272–5.
  • Duan S, Govorkova EA, Bahl J, Zaraket H, Baranovich T, Seiler P, etal. Epistatic interactions between neuraminidase mutations facilitated the emergence of the oseltamivir-resistant H1N1 influenza viruses. Nat Commun. 2014; 5: 5029.
  • Butler J, Hooper KA, Petrie S, Lee R, Maurer-Stroh S, Reh L, etal. Estimating the fitness advantage conferred by permissive neuraminidase mutations in recent oseltamivir-resistant A(H1N1)pdm09 influenza viruses. PLoS Pathog. 2014; 10: e1004065.