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  • 1.
    Avril, Alexis
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Grosbois, Vladimir
    CIRAD, France.
    Latorre-Margalef, Neus
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Univ Georgia, USA.
    Gaidet, Nicolas
    CIRAD, France.
    Tolf, Conny
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Olsen, Björn
    Uppsala University.
    Waldenström, Jonas
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Capturing individual-level parameters of influenza A virus dynamics in wild ducks using multistate models2016In: Journal of Applied Ecology, ISSN 0021-8901, E-ISSN 1365-2664, Vol. 53, no 4, p. 1289-1297Article in journal (Refereed)
    Abstract [en]

    Disease prevalence in wildlife is governed by epidemiological parameters (infection and recovery rates) and response to infection, both of which vary within and among individual hosts. Studies quantifying these individual-scale parameters and documenting their source of variation in wild hosts are fundamental for predicting disease dynamics. Such studies do not exist for the influenza A virus (IAV), despite its strong impact on the global economy and public health. Using capture-recaptures of 3500 individual mallards Anas platyrhynchos during seven migration seasons at a stopover site in southern Sweden, we provide the first empirical description of the individual-based mechanisms of IAV dynamics in a wild reservoir host. For most years, prevalence and risk of IAV infection peaked at a single time during the autumn migration season, but the timing, shape and intensity of the infection curve showed strong annual heterogeneity. In contrast, the seasonal pattern of recovery rate only varied in intensity across years. Adults and juveniles displayed similar seasonal patterns of infection and recovery each year. However, compared to adults, juveniles experienced twice the risk of becoming infected, whereas recovery rates were similar across age categories. Finally, we did not find evidence that infection influenced the timing of emigration.Synthesis and applications. Our study provides robust empirical estimates of epidemiological parameters for predicting influenza A virus (IAV) dynamics. However, the strong annual variation in infection curves makes forecasting difficult. Prevalence data can provide reliable surveillance indicators as long as they catch the variation in infection risk. However, individual-based monitoring of infection is required to verify this assumption in areas where surveillance occurs. In this context, monitoring of captive sentinel birds kept in close contact with wild birds is useful. The fact that infection does not impact the timing of migration underpins the potential for mallards to spread viruses rapidly over large geographical scales. Hence, we strongly encourage IAV surveillance with a multistate capture-recapture approach along the entire migratory flyway of mallards.

  • 2.
    Ellström, Patrik
    et al.
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Latorre-Margalef, Neus
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Griekspoor, Petra
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Waldenström, Jonas
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Olofsson, Jenny
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Wahlgren, John
    Ctr Microbiol Preparedness KCB, Swedish Inst Infect Dis Control SMI, SE-17182 Solna, Sweden.
    Olsen, Björn
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Sampling for low-pathogenic avian influenza A virus in wild Mallard ducks: Oropharyngeal versus cloacal swabbing2008In: Vaccine, ISSN 0264-410X, E-ISSN 1873-2518, Vol. 26, no 35, p. 4414-4416Article in journal (Refereed)
  • 3.
    Gillman, Anna
    et al.
    Uppsala University.
    Muradrasoli, Shaman
    Swedish University of Agricultural Sciences.
    Söderstrom, Hanna
    Umeå University.
    Nordh, Johan
    Uppsala University.
    Bröjer, Caroline
    Swedish University of Agricultural Sciences.
    Lindberg, Richard H.
    Umeå University.
    Latorre-Margalef, Neus
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Waldenström, Jonas
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Olsen, Björn
    Uppsala University.
    Järhult, Josef D.
    Uppsala University.
    Resistance Mutation R292K Is Induced in Influenza A(H6N2) Virus by Exposure of Infected Mallards to Low Levels of Oseltamivir2013In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 8, no 8, article id e71230Article in journal (Refereed)
    Abstract [en]

    Resistance to neuraminidase inhibitors (NAIs) is problematic as these drugs constitute the major treatment option for severe influenza. Extensive use of the NAI oseltamivir (Tamiflu(R)) results in up to 865 ng/L of its active metabolite oseltamivir carboxylate (OC) in river water. There one of the natural reservoirs of influenza A, dabbling ducks, can be exposed. We previously demonstrated that an influenza A(H1N1) virus in mallards (Anas platyrhynchos) exposed to 1 mu g/L of OC developed oseltamivir resistance through the mutation H274Y (N2-numbering). In this study, we assessed the resistance development in an A(H6N2) virus, which belongs to the phylogenetic N2 group of neuraminidases with distinct functional and resistance characteristics. Mallards were infected with A(H6N2) while exposed to 120 ng/L, 1.2 mu g/L or 12 mu g/L of OC in their sole water source. After 4 days with 12 mu g/L of OC exposure, the resistance mutation R292K emerged and then persisted. Drug sensitivity was decreased approximate to 13,000-fold for OC and approximate to 7.8-fold for zanamivir. Viral shedding was similar when comparing R292K and wild-type virus indicating sustained replication and transmission. Reduced neuraminidase activity and decrease in recovered virus after propagation in embryonated hen eggs was observed in R292K viruses. The initial, but not the later R292K isolates reverted to wild-type during egg-propagation, suggesting a stabilization of the mutation, possibly through additional mutations in the neuraminidase (D113N or D141N) or hemagglutinin (E216K). Our results indicate a risk for OC resistance development also in a N2 group influenza virus and that exposure to one NAI can result in a decreased sensitivity to other NAIs as well. If established in influenza viruses circulating among wild birds, the resistance could spread to humans via re-assortment or direct transmission. This could potentially cause an oseltamivir-resistant pandemic; a serious health concern as preparedness plans rely heavily on oseltamivir before vaccines can be mass-produced.

  • 4.
    Gillman, Anna
    et al.
    Uppsala University.
    Muradrasoli, Shaman
    Uppsala University;Swedish University of Agricultural Sciences.
    Söderström, Hanna
    Umeå University.
    Holmberg, Fredrik
    Uppsala University.
    Latorre-Margalef, Neus
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Tolf, Conny
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Waldenström, Jonas
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Gunnarsson, Gunnar
    Kristianstad University.
    Olsen, Björn
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Uppsala University.
    Jarhult, Josef D.
    Uppsala University.
    Oseltamivir-Resistant Influenza A (H1N1) Virus Strain with an H274Y Mutation in Neuraminidase Persists without Drug Pressure in Infected Mallards2015In: Applied and Environmental Microbiology, ISSN 0099-2240, E-ISSN 1098-5336, Vol. 81, no 7, p. 2378-2383Article in journal (Refereed)
    Abstract [en]

    Influenza A virus (IAV) has its natural reservoir in wild waterfowl, and emerging human IAVs often contain gene segments from avian viruses. The active drug metabolite of oseltamivir (oseltamivir carboxylate [OC]), stockpiled as Tamiflu for influenza pandemic preparedness, is not removed by conventional sewage treatment and has been detected in river water. There, it may exert evolutionary pressure on avian IAV in waterfowl, resulting in the development of resistant viral variants. A resistant avian IAV can circulate among wild birds only if resistance does not restrict viral fitness and if the resistant virus can persist without continuous drug pressure. In this in vivo mallard (Anas platyrhynchos) study, we tested whether an OC-resistant avian IAV (H1N1) strain with an H274Y mutation in the neuraminidase (NA-H274Y) could retain resistance while drug pressure was gradually removed. Successively infected mallards were exposed to decreasing levels of OC, and fecal samples were analyzed for the neuraminidase sequence and phenotypic resistance. No reversion to wild-type virus was observed during the experiment, which included 17 days of viral transmission among 10 ducks exposed to OC concentrations below resistance induction levels. We conclude that resistance in avian IAV that is induced by exposure of the natural host to OC can persist in the absence of the drug. Thus, there is a risk that human-pathogenic IAVs that evolve from IAVs circulating among wild birds may contain resistance mutations. An oseltamivir-resistant pandemic IAV would pose a substantial public health threat. Therefore, our observations underscore the need for prudent oseltamivir use, upgraded sewage treatment, and surveillance for resistant IAVs in wild birds.

  • 5.
    Gunnarsson, Gunnar
    et al.
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Jourdain, Elsa
    Waldenström, Jonas
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Helander, Björn
    Lindberg, Peter
    Elmberg, Johan
    Latorre-Margalef, Neus
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Olsen, Björn
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Zero prevalence of influenza A virus two raptor species by standard screeing.2009In: Vector Borne and Zoonotic Diseases, ISSN 1530-3667, E-ISSN 1557-7759, Vol. 10, no 4, p. 387-390Article in journal (Refereed)
    Abstract [en]

    Disease can have severe impact on animal populations, especially in rare species. Baseline data for atypical host species are missing for a range of infectious diseases, although such hosts are potentially more affected than the normal vectors and reservoir species. If highly pathogenic avian influenza strikes rare birds of prey, this may have crucial impact on the predator species itself, but also on the food web in which it interacts. Here we present the first large-scale screening of raptors that regularly consume birds belonging to the natural reservoir of influenza A viruses. Influenza A virus prevalence was studied in two rare raptors, the white-tailed sea eagle (Haliaeetus albicilla) and the peregrine falcon (Falco peregrinus). Nestlings were screened for active (181 white-tailed sea eagles and 168 peregrine falcons) and past (123 white-tailed sea eagles and 6 peregrine falcons) infection in 2006–2007, and an additional 20 succumbed adult white-tailed sea eagles were sampled in 2003–2006. Neither high- nor low-pathogenic influenza infections were found in our sample, but this does not rule out that the former may have major impact on rare raptors and their food webs.

  • 6.
    Gunnarsson, Gunnar
    et al.
    Kristianstad University.
    Latorre-Margalef, Neus
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Hobson, K. A.
    Environment Canada, Saskatoon, Canada.
    Van Wilgenburg, S. L.
    Environment Canada, Saskatoon, Canada.
    Elmberg, Johan
    Kristianstad University.
    Olsen, Björn
    Uppsala University Hospital.
    Fouchier, R. A. M.
    Erasmus Medical Center, The Netherlands.
    Waldenström, Jonas
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Disease Dynamics and Bird Migration – Linking Mallards Anas platyrhynchos and subtype diversity of Influenza A Virus in Time and Space2012In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 7, no 4, article id e35679Article in journal (Refereed)
    Abstract [en]

    The mallard Anas platyrhynchos is a reservoir species for influenza A virus in the northern hemisphere, with particularly high prevalence rates prior to as well as during its prolonged autumn migration. It has been proposed that the virus is brought from the breeding grounds and transmitted to conspecifics during subsequent staging during migration, and so a better understanding of the natal origin of staging ducks is vital to deciphering the dynamics of viral movement pathways. Ottenby is an important stopover site in southeast Sweden almost halfway downstream in the major Northwest European flyway, and is used by millions of waterfowl each year. Here, mallards were captured and sampled for influenza A virus infection, and positive samples were subtyped in order to study possible links to the natal area, which were determined by a novel approach combining banding recovery data and isotopic measurements (d2 H) of feathers grown on breeding grounds. Geographic assignments showed that the core natal areas of studied mallards were in Estonia, southern and central Finland, and northwestern Russia. This study demonstrates a clear temporal succession of latitudes of natal origin during the course of autumn migration. We also demonstrate a corresponding and concomitant shift in virus subtypes. Acknowledging that these two different patterns were based in part upon different data, a likely interpretation worth further testing is that the early arriving birds with more proximate origins have different influenza A subtypes than the more distantly originating late autumn birds. If true, this knowledge would allow novel insight into the origins and transmission of the influenza A virus among migratory hosts previously unavailable through conventional approaches.

  • 7.
    Jourdain, Elsa
    et al.
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences. INRA, France.
    Gunnarsson, Gunnar
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences. Kristianstad University.
    Wahlgren, John
    Karolinska Institutet ; Swedish Institute for Infectious Disease Control.
    Latorre-Margalef, Neus
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Bröjer, Caroline
    National Veterinary Institute ; University of Agricultural Sciences.
    Sahlin, Sofie
    Karolinska Institutet ; Swedish Institute for Infectious Disease Control.
    Svensson, Lovisa
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Waldenström, Jonas
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Lundkvist, Åke
    Swedish Institute for Infectious Disease Control.
    Olsen, Björn
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences. Uppsala University.
    Influenza Virus in a Natural Host, the Mallard: Experimental Infection Data2010In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 5, no 1, article id e8935Article in journal (Refereed)
    Abstract [en]

    Wild waterfowl, particularly dabbling ducks such as mallards (Anas platyrhynchos), are considered the main reservoir of low-pathogenic avian influenza viruses (LPAIVs). They carry viruses that may evolve and become highly pathogenic for poultry or zoonotic. Understanding the ecology of LPAIVs in these natural hosts is therefore essential. We assessed the clinical response, viral shedding and antibody production of juvenile mallards after intra-esophageal inoculation of two LPAIV subtypes previously isolated from wild congeners. Six ducks, equipped with data loggers that continually monitored body temperature, heart rate and activity, were successively inoculated with an H7N7 LPAI isolate (day 0), the same H7N7 isolate again (day 21) and an H5N2 LPAI isolate (day 35). After the first H7N7 inoculation, the ducks remained alert with no modification of heart rate or activity. However, body temperature transiently increased in four individuals, suggesting that LPAIV strains may have minor clinical effects on their natural hosts. The excretion patterns observed after both reinoculations differed strongly from those observed after the primary H7N7 inoculation, suggesting that not only homosubtypic but also heterosubtypic immunity exist. Our study suggests that LPAI infection has minor clinically measurable effects on mallards and that mallard ducks are able to mount immunological responses protective against heterologous infections. Because the transmission dynamics of LPAIVs in wild populations is greatly influenced by individual susceptibility and herd immunity, these findings are of high importance. Our study also shows the relevance of using telemetry to monitor disease in animals.

  • 8.
    Järhult, Josef D.
    et al.
    Uppsala University.
    Muradrasoli, Shaman
    Swedish University of Agricultural Sciences.
    Wahlgren, John
    Swedish Institute for Infectious Disease Control ; Karolinska Institutet.
    Söderström, Hanna
    Umeå University.
    Orozovic, Goran
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Gunnarsson, Gunnar
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences. Kristianstad University.
    Bröjer, Caroline
    National Veterinary Institute ; Swedish University of Agricultural Sciences.
    Latorre-Margalef, Neus
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Fick, Jerker
    Umeå University.
    Grabic, Roman
    Umeå University ; University of South Bohemia in Ceske Budejovice, Czech Republic.
    Lennerstrand, Johan
    Uppsala University.
    Waldenström, Jonas
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Lundkvist, Ake
    Swedish Institute for Infectious Disease Control ; Karolinska Institutet.
    Olsen, Björn
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences. Uppsala University.
    Environmental levels of the antiviral oseltamivir induce development of resistance mutation H274Y in influenza A/H1N1 virus in mallards2011In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 6, no 9, article id e24742Article in journal (Refereed)
    Abstract [en]

    Oseltamivir (Tamiflu®) is the most widely used drug against influenza infections and is extensively stockpiled worldwide as part of pandemic preparedness plans. However, resistance is a growing problem and in 2008-2009, seasonal human influenza A/H1N1 virus strains in most parts of the world carried the mutation H274Y in the neuraminidase gene which causes resistance to the drug. The active metabolite of oseltamivir, oseltamivir carboxylate (OC), is poorly degraded in sewage treatment plants and surface water and has been detected in aquatic environments where the natural influenza reservoir, dabbling ducks, can be exposed to the substance. To assess if resistance can develop under these circumstances, we infected mallards with influenza A/H1N1 virus and exposed the birds to 80 ng/L, 1 µg/L and 80 µg/L of OC through their sole water source. By sequencing the neuraminidase gene from fecal samples, we found that H274Y occurred at 1 µg/L of OC and rapidly dominated the viral population at 80 µg/L. IC₅₀ for OC was increased from 2-4 nM in wild-type viruses to 400-700 nM in H274Y mutants as measured by a neuraminidase inhibition assay. This is consistent with the decrease in sensitivity to OC that has been noted among human clinical isolates carrying H274Y. Environmental OC levels have been measured to 58-293 ng/L during seasonal outbreaks and are expected to reach µg/L-levels during pandemics. Thus, resistance could be induced in influenza viruses circulating among wild ducks. As influenza viruses can cross species barriers, oseltamivir resistance could spread to human-adapted strains with pandemic potential disabling oseltamivir, a cornerstone in pandemic preparedness planning. We propose surveillance in wild birds as a measure to understand the resistance situation in nature and to monitor it over time. Strategies to lower environmental levels of OC include improved sewage treatment and, more importantly, a prudent use of antivirals.

  • 9.
    Kraus, Robert H. S.
    et al.
    Wageningen University, The Netherlands.
    van Hooft, Pim
    Wageningen University, The Netherlands.
    Waldenström, Jonas
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Latorre-Margalef, Neus
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Ydenberg, Ronald C.
    Wageningen University, The Netherlands ; Simon Fraser University, Canada.
    Prins, Herbert H. T.
    Wageningen University, The Netherlands.
    Avian influenza surveillance with FTA cards: field methods, biosafety, and transportation issues solved2011In: Journal of Visualized Experiments, ISSN 1940-087X, E-ISSN 1940-087X, no 54, article id 2832Article in journal (Refereed)
    Abstract [en]

    Avian Influenza Viruses (AIVs) infect many mammals, including humans(1). These AIVs are diverse in their natural hosts, harboring almost all possible viral subtypes(2). Human pandemics of flu originally stem from AIVs(3). Many fatal human cases during the H5N1 outbreaks in recent years were reported. Lately, a new AIV related strain swept through the human population, causing the 'swine flu epidemic'(4). Although human trading and transportation activity seems to be responsible for the spread of highly pathogenic strains(5), dispersal can also partly be attributed to wild birds(6, 7). However, the actual reservoir of all AIV strains is wild birds. In reaction to this and in face of severe commercial losses in the poultry industry, large surveillance programs have been implemented globally to collect information on the ecology of AIVs, and to install early warning systems to detect certain highly pathogenic strains(8-12). Traditional virological methods require viruses to be intact and cultivated before analysis. This necessitates strict cold chains with deep freezers and heavy biosafety procedures to be in place during transport. Long-term surveillance is therefore usually restricted to a few field stations close to well equipped laboratories. Remote areas cannot be sampled unless logistically cumbersome procedures are implemented. These problems have been recognised(13, 14) and the use of alternative storage and transport strategies investigated (alcohols or guanidine)(15-17). Recently, Kraus et al.(18) introduced a method to collect, store and transport AIV samples, based on a special filter paper. FTA cards(19) preserve RNA on a dry storage basis(20) and render pathogens inactive upon contact(21). This study showed that FTA cards can be used to detect AIV RNA in reverse-transcription PCR and that the resulting cDNA could be sequenced and virus genes and determined. In the study of Kraus et al.(18) a laboratory isolate of AIV was used, and samples were handled individually. In the extension presented here, faecal samples from wild birds from the duck trap at the Ottenby Bird Observatory (SE Sweden) were tested directly to illustrate the usefulness of the methods under field conditions. Catching of ducks and sample collection by cloacal swabs is demonstrated. The current protocol includes up-scaling of the work flow from single tube handling to a 96-well design. Although less sensitive than the traditional methods, the method of FTA cards provides an excellent supplement to large surveillance schemes. It allows collection and analysis of samples from anywhere in the world, without the need to maintaining a cool chain or safety regulations with respect to shipping of hazardous reagents, such as alcohol or guanidine.

  • 10.
    Latorre-Margalef, Neus
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Univ Georgia, USA.
    Avril, Alexis
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Tolf, Conny
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Olsen, Björn
    Uppsala University.
    Waldenström, Jonas
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    How Does Sampling Methodology Influence Molecular Detection and Isolation Success in Influenza A Virus Field Studies?2016In: Applied and Environmental Microbiology, ISSN 0099-2240, E-ISSN 1098-5336, Vol. 82, no 4, p. 1147-1153Article in journal (Refereed)
    Abstract [en]

    Wild waterfowl are important reservoir hosts for influenza A virus (IAV) and a potential source of spillover infections in other hosts, including poultry and swine. The emergence of highly pathogenic avian influenza (HPAI) viruses, such as H5N1 and H5N8, and subsequent spread along migratory flyways prompted the initiation of several programs in Europe, North America, and Africa to monitor circulation of HPAI and low-pathogenicity precursor viruses (low-pathogenicity avian influenza [LPAI] viruses). Given the costs of maintaining such programs, it is essential to establish best practice for field methodologies to provide robust data for epidemiological interpretation. Here, we use long-term surveillance data from a single site to evaluate the influence of a number of parameters on virus detection and isolation of LPAI viruses. A total of 26,586 samples (oropharyngeal, fecal, and cloacal) collected from wild mallards were screened by real-time PCR, and positive samples were subjected to isolation in embryonated chicken eggs. The LPAI virus detection rate was influenced by the sample type: cloacal/fecal samples showed a consistently higher detection rate and lower cycle threshold (Ct) value than oropharyngeal samples. Molecular detection was more sensitive than isolation, and virus isolation success was proportional to the number of RNA copies in the sample. Interestingly, for a given Ct value, the isolation success was lower in samples from adult birds than in those from juveniles. Comparing the results of specific real-time reverse transcriptase (RRT)-PCRs and of isolation, it was clear that coinfections were common in the investigated birds. The effects of sample type and detection methods warrant some caution in interpretation of the surveillance data.

  • 11.
    Latorre-Margalef, Neus
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Grosbois, Vladimir
    International Research Center in Agriculture for Development, France.
    Wahlgren, John
    Karolinska Institutet.
    Munster, Vincent J.
    Erasmus Medical Center, The Netherlands ; National Institutes of Health, USA.
    Tolf, Conny
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Fouchier, Ron A. M.
    Erasmus Medical Center, The Netherlands.
    Osterhaus, Albert D. M. E.
    Erasmus Medical Center, The Netherlands.
    Olsen, Björn
    Uppsala University.
    Waldenström, Jonas
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Heterosubtypic Immunity to Influenza A Virus Infections in Mallards May Explain Existence of Multiple Virus Subtypes2013In: PLoS Pathogens, ISSN 1553-7366, E-ISSN 1553-7374, Vol. 9, no 6, article id e1003443Article in journal (Refereed)
    Abstract [en]

    Wild birds, particularly duck species, are the main reservoir of influenza A virus (IAV) in nature. However, knowledge of IAV infection dynamics in the wild bird reservoir, and the development of immune responses, are essentially absent. Importantly, a detailed understanding of how subtype diversity is generated and maintained is lacking. To address this, 18,679 samples from 7728 Mallard ducks captured between 2002 and 2009 at a single stopover site in Sweden were screened for IAV infections, and the resulting 1081 virus isolates were analyzed for patterns of immunity. We found support for development of homosubtypic hemagglutinin (HA) immunity during the peak of IAV infections in the fall. Moreover, re-infections with the same HA subtype and related prevalent HA subtypes were uncommon, suggesting the development of natural homosubtypic and heterosubtypic immunity (p-value = 0.02). Heterosubtypic immunity followed phylogenetic relatedness of HA subtypes, both at the level of HA clades (p-value = 0.04) and the level of HA groups (p-value = 0.05). In contrast, infection patterns did not support specific immunity for neuraminidase (NA) subtypes. For the H1 and H3 Clades, heterosubtypic immunity showed a clear temporal pattern and we estimated within-clade immunity to last at least 30 days. The strength and duration of heterosubtypic immunity has important implications for transmission dynamics of IAV in the natural reservoir, where immune escape and disruptive selection may increase HA antigenic variation and explain IAV subtype diversity.

  • 12.
    Latorre-Margalef, Neus
    et al.
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Gunnarsson, Gunnar
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Munster, V J
    Fouchier, R A M
    Osterhaus, A D M E
    Elmberg, J
    Olsen, Björn
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Wallensten, Anders
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Fransson, T
    Brudin, Lars
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Waldenström, Jonas
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Does Influenza A affect body condition of wild mallard ducks, or vice versa? A reply to Flint & Franson2009In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 276, no 1666, p. 2347-2349Article in journal (Refereed)
  • 13.
    Latorre-Margalef, Neus
    et al.
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Gunnarsson, Gunnar
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Munster, V.J.
    Fouchier, R.A.M.
    Osterhaus, A.D.M.E.
    Elmberg, Johan
    Olsen, Björn
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Wallensten, Anders
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Haemig, Paul D.
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Fransson, Thord
    Brudin, Lars
    University of Kalmar, School of Pure and Applied Natural Sciences. Kalmar County Hospital.
    Waldenström, Jonas
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Effects of influenza A virus infection on migrating mallard ducks2009In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 276, no 1659, p. 1029-1036Article in journal (Refereed)
    Abstract [en]

    The natural reservoir of influenza A virus is waterfowl, particularly dabbling ducks (genus Anas). Although it has long been assumed that waterfowl are asymptomatic carriers of the virus, a recent study found that low-pathogenic avian influenza (LPAI) infection in Bewick's swans (Cygnus columbianus bewickii) negatively affected stopover time, body mass and feeding behaviour. In the present study, we investigated whether LPAI infection incurred ecological or physiological costs to migratory mallards (Anas platyrhynchos) in terms of body mass loss and staging time, and whether such costs could influence the likelihood for long-distance dispersal of the avian influenza virus by individual ducks. During the autumn migrations of 2002-2007, we collected faecal samples (n = 10 918) and biometric data from mallards captured and banded at Ottenby, a major staging site in a flyway connecting breeding and wintering areas of European waterfowl. Body mass was significantly lower in infected ducks than in uninfected ducks (mean difference almost 20 g over all groups), and the amount of virus shed by infected juveniles was negatively correlated with body mass. There was no general effect of infection on staging time, except for juveniles in September, in which birds that shed fewer viruses stayed shorter than birds that shed more viruses. LPAI infection did not affect speed or distance of subsequent migration. The data from recaptured individuals showed that the maximum duration of infection was on average 8.3 days (s.e. 0.5), with a mean minimum duration of virus shedding of only 3.1 days (s.e. 0.1). Shedding time decreased during the season, suggesting that mallards acquire transient immunity for LPAI infection. In conclusion, deteriorated body mass following infection was detected, but it remains to be seen whether this has more long-term fitness effects. The short virus shedding time suggests that individual mallards are less likely to spread the virus at continental or intercontinental scales.

  • 14.
    Latorre-Margalef, Neus
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Univ Georgia, Dept Populat Hlth, Coll Vet Med, Southeastern Cooperat Wildlife Dis Study, Athens, GA 30602 USA.
    Tolf, Conny
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Grosbois, Vladimir
    Int Res Ctr Agr Dev CIRAD UPR AGIRs, Anim & Integrate Risk Management, F-34398 Montpellier, France.
    Avril, Alexis
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Bengtsson, Daniel
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Wille, Michelle
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Osterhaus, Albert D M E
    Erasmus MC, Dept Virol, Rotterdam, Netherlands.
    Fouchier, Ron A M
    Erasmus MC, Dept Virol, Rotterdam, Netherlands.
    Olsen, Björn
    Uppsala Univ.
    Waldenström, Jonas
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Long-term variation in influenza A virus prevalence and subtype diversity in migratory mallards in northern Europe.2014In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 281, no 1781, p. Article ID: UNSP 20140098-Article in journal (Refereed)
    Abstract [en]

    Data on long-term circulation of pathogens in wildlife populations are seldom collected, and hence understanding of spatial-temporal variation in prevalence and genotypes is limited. Here, we analysed a long-term surveillance series on influenza A virus (IAV) in mallards collected at an important migratory stopover site from 2002 to 2010, and characterized seasonal dynamics in virus prevalence and subtype diversity. Prevalence dynamics were influenced by year, but retained a common pattern for all years whereby prevalence was low in spring and summer, but increased in early autumn with a first peak in August, and a second more pronounced peak during October-November. A total of 74 haemagglutinin (HA)/neuraminidase (NA) combinations were isolated, including all NA and most HA (H1-H12) subtypes. The most common subtype combinations were H4N6, H1N1, H2N3, H5N2, H6N2 and H11N9, and showed a clear linkage between specific HA and NA subtypes. Furthermore, there was a temporal structuring of subtypes within seasons based on HA phylogenetic relatedness. Dissimilar HA subtypes tended to have different temporal occurrence within seasons, where the subtypes that dominated in early autumn were rare in late autumn, and vice versa. This suggests that build-up of herd immunity affected IAV dynamics in this system.

  • 15.
    Lewis, Nicola S.
    et al.
    Univ Cambridge, UK.
    Verhagen, Josanne H.
    Erasmus MC, Netherlands.
    Javakhishvili, Zurab
    Ilia State Univ, Rep of Georgia.
    Russell, Colin A.
    Univ Cambridge, UK.
    Lexmond, Pascal
    Erasmus MC, Netherlands.
    Westgeest, Kim B.
    Erasmus MC, Netherlands.
    Bestebroer, Theo M.
    Erasmus MC, Netherlands.
    Halpin, Rebecca A.
    J Craig Venter Inst, USA.
    Lin, Xudong
    J Craig Venter Inst, USA.
    Ransier, Amy
    J Craig Venter Inst, USA.
    Fedorova, Nadia B.
    J Craig Venter Inst, USA.
    Stockwel, Timothy B.
    J Craig Venter Inst, USA.
    Latorre-Margalef, Neus
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Univ Georgia, USA.
    Olsen, Björn
    Uppsala Univ.
    Smith, Gavin
    Duke NUS Grad Med Sch, Singapore.
    Bahl, Justin
    Duke NUS Grad Med Sch, Singapore ; Univ Texas Houston, USA..
    Wentworth, David E.
    Waldenström, Jonas
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Fouchier, Ron A. M.
    Erasmus MC, Netherlands.
    de Graaf, Miranda
    Erasmus MC, Netherlands.
    Influenza A virus evolution and spatio-temporal dynamics in Eurasian wild birds: a phylogenetic and phylogeographical study of whole-genome sequence data2015In: Journal of General Virology, ISSN 0022-1317, E-ISSN 1465-2099, Vol. 96, p. 2050-2060Article in journal (Refereed)
    Abstract [en]

    Low pathogenic avian influenza A viruses (IAVs) have a natural host reservoir in wild waterbirds and the potential to spread to other host species. Here, we investigated the evolutionary, spatial and temporal dynamics of avian IAVs in Eurasian wild birds. We used whole-genome sequences collected as part of an intensive long-term Eurasian wild bird surveillance study, and combined this genetic data with temporal and spatial information to explore the virus evolutionary dynamics. Frequent reassortment and co-circulating lineages were observed for all eight genomic RNA segments over time. There was no apparent species-specific effect on the diversity of the avian IAVs. There was a spatial and temporal relationship between the Eurasian sequences and significant viral migration of avian lAVs from West Eurasia towards Central Eurasia. The observed viral migration patterns differed between segments. Furthermore, we discuss the challenges faced when analysing these surveillance and sequence data, and the caveats to be borne in mind when drawing conclusions from the apparent results of such analyses.

  • 16.
    Nykvist, Marie
    et al.
    Uppsala University.
    Gillman, Anna
    Uppsala University.
    Söderström Lindström, Hanna
    Umeå University.
    Tang, Chaojun
    Umeå University.
    Fedorova, Ganna
    University of South Bohemia in Ceske Budejovice, Czech Republic.
    Lundkvist, Åke
    Uppsala University.
    Latorre-Margalef, Neus
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Wille, Michelle
    Uppsala University.
    Järhult, Josef D.
    Uppsala University.
    In vivo mallard experiments indicate that zanamivir has less potential for environmental influenza A virus resistance development than oseltamivir2017In: Journal of General Virology, ISSN 0022-1317, E-ISSN 1465-2099, Vol. 98, no 12, p. 2937-2949Article in journal (Refereed)
    Abstract [en]

    Neuraminidase inhibitors are a cornerstone of influenza pandemic preparedness before vaccines can be mass-produced and thus a neuraminidase inhibitor-resistant pandemic is a serious threat to public health. Earlier work has demonstrated the potential for development and persistence of oseltamivir resistance in influenza A viruses exposed to environmentally relevant water concentrations of the drug when infecting mallards, the natural influenza reservoir that serves as the genetic base for human pandemics. As zanamivir is the major second-line neuraminidase inhibitor treatment, this study aimed to assess the potential for development and persistence of zanamivir resistance in an in vivo mallard model; especially important as zanamivir will probably be increasingly used. Our results indicate less potential for development and persistence of resistance due to zanamivir than oseltamivir in an environmental setting. This conclusion is based on: (1) the lower increase in zanamivir IC50 conferred by the mutations caused by zanamivir exposure (2–17-fold); (2) the higher zanamivir water concentration needed to induce resistance (at least 10 µg l−1); (3) the lack of zanamivir resistance persistence without drug pressure; and (4) the multiple resistance-related substitutions seen during zanamivir exposure (V116A, A138V, R152K, T157I and D199G) suggesting lack of one straight-forward evolutionary path to resistance. Our study also adds further evidence regarding the stability of the oseltamivir-induced substitution H275Y without drug pressure, and demonstrates the ability of a H275Y-carrying virus to acquire secondary mutations, further boosting oseltamivir resistance when exposed to zanamivir. Similar studies using influenza A viruses of the N2-phylogenetic group of neuraminidases are recommended.

  • 17.
    Olson, Sarah H.
    et al.
    Wildlife Conservation Society, USA.
    Parmley, Jane
    University of Guelph, Canada.
    Soos, Catherine
    Environment Canada, Canada.
    Gilbert, Martin
    Wildlife Conservation Society, USA.
    Latorre-Margalef, Neus
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. University of Georgia, USA.
    Hall, Jeffrey S.
    National Wildlife Health Center, USA.
    Hansbro, Phillip M.
    University of Newcastle, Australia ; Hunter Medical Research Institute, Australia.
    Leighton, Frederick
    University of Saskatchewan, Canada.
    Munster, Vincent
    National Institutes of Health, USA.
    Joly, Damien
    Metabiota, Canada.
    Sampling Strategies and Biodiversity of Influenza A Subtypes in Wild Birds2014In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 9, no 3, article id e90826Article in journal (Refereed)
    Abstract [en]

    Wild aquatic birds are recognized as the natural reservoir of avian influenza A viruses (AIV), but across high and low pathogenic AIV strains, scientists have yet to rigorously identify most competent hosts for the various subtypes. We examined 11,870 GenBank records to provide a baseline inventory and insight into patterns of global AIV subtype diversity and richness. Further, we conducted an extensive literature review and communicated directly with scientists to accumulate data from 50 non-overlapping studies and over 250,000 birds to assess the status of historic sampling effort. We then built virus subtype sample-based accumulation curves to better estimate sample size targets that capture a specific percentage of virus subtype richness at seven sampling locations. Our study identifies a sampling methodology that will detect an estimated 75% of circulating virus subtypes from a targeted bird population and outlines future surveillance and research priorities that are needed to explore the influence of host and virus biodiversity on emergence and transmission.

  • 18.
    Orozovic, Goran
    et al.
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Latorre-Margalef, Neus
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Wahlgren, John
    Muradrasoli, Shaman
    Olsen, Björn
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Degenerate primers for PCR amplification and sequencing of the avian influenza A neuraminidase gene2010In: Journal of Virological Methods, ISSN 0166-0934, E-ISSN 1879-0984, Vol. 170, no 1-2, p. 94-98Article in journal (Refereed)
    Abstract [en]

    This study describes the design of degenerate primers and their use for synthesis of full-length avian influenza A neuramindase (NA). Each reaction was performed using either two forward primers and one reverse primer, or one forward primer and one reverse primer. Both primer combinations had comparable amplification efficiencies for all NA subtypes (1-9). A total of 11 virus strains, including both field isolates and reference strains, were amplified successfully using these degenerate primer sets. Of the sequences amplified, 108 strains (93.9%) resulted in near full-length NA cDNAs after two readings with one forward primer and one reverse primer. Of the remaining sequences, five strains (4.3%) yielded reads with enough information for subtype categorization by BLAST although they were of insufficient quality for assembly. One strain (0.9%) yielded different subtypes from both sequence reads whereas the other one (0.9%) was not possible to assemble and subtype. This successful demonstration of these degenerate primers for the amplification and sequencing of all avian NA subtypes suggests that these primers could be employed in the avian influenza surveillance program as well as studies of antiviral resistance, virus ecology or viral phylogeny.

  • 19.
    Tolf, Conny
    et al.
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Bengtsson, Daniel
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Rodrigues, David
    Instituto Politécnico de Coimbra, Portugal.
    Latorre-Margalef, Neus
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Wille, Michelle
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Figueiredo, Maria Ester
    Instituto Politécnico de Coimbra, Portugal.
    Jankowska-Hjortaas, Monika
    Norwegian Veterinary Institute, Norway.
    Germundsson, Anna
    Norwegian Veterinary Institute, Norway.
    Duby, Pierre-Yves
    Instituto Politécnico de Coimbra, Portugal.
    Lebarbenchon, Camille
    Universite de La Reunion, France.
    Gauthier-Clerc, Michel
    Centre de Recherche de la Tour du Valat, France.
    Olsen, Björn
    Uppsala University.
    Waldenström, Jonas
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Birds and viruses at a crossroad: surveillance of influenza a virus in portuguese waterfowl2012In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 7, no 11, article id e49002Article in journal (Refereed)
    Abstract [en]

    During recent years, extensive amounts of data have become available regarding influenza A virus (IAV) in wild birds in northern Europe, while information from southern Europe is more limited. Here, we present an IAV surveillance study conducted in western Portugal 2008-2009, analyzing 1653 samples from six different species of waterfowl, with the majority of samples taken from Mallards (Anas platyrhynchos). Overall 4.4% of sampled birds were infected. The sampling results revealed a significant temporal variation in the IAV prevalence, including a pronounced peak among predominantly young birds in June, indicating that IAV circulate within breeding populations in the wetlands of western Portugal. The H10N7 and H9N2 subtypes were predominant among isolated viruses. Phylogenetic analyses of the hemagglutinin and neuraminidase sequences of H10N7, H9N2 and H11N3 virus showed that sequences from Portugal were closely related to viral sequences from Central Europe as well as to IAVs isolated in the southern parts of Africa, reflecting Portugal's position on the European-African bird migratory flyway. This study highlights the importance of Portugal as a migratory crossroad for IAV, connecting breeding stationary waterfowl with birds migrating between continents which enable transmission and spread of IAV.

  • 20.
    Tolf, Conny
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Latorre-Margalef, Neus
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Wille, Michelle
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Bengtsson, Daniel
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Gunnarsson, Gunnar
    Kristianstad University.
    Grosbois, Vladimir
    Centre de coopération Internationale en Recherche Agronomique pour le Développement (CIRAD), France.
    Hasselquist, Dennis
    Lund University.
    Olsen, Björn
    Uppsala University.
    Elmberg, Johan
    Kristianstad University.
    Waldenström, Jonas
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Individual Variation in Influenza A Virus Infection Histories and Long-Term Immune Responses in Mallards2013In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 8, no 4, article id e61201Article in journal (Refereed)
    Abstract [en]

    Wild dabbling ducks (genus Anas) are the main reservoir for influenza A virus (IAV) in the Northern Hemisphere. Current understanding of disease dynamics and epidemiology in this virus-host system has primarily been based on population-level surveillance studies and infection experiments conducted in laboratory settings. Using a combined experimental-natural approach with wild-strain captive mallards (Anas platyrhynchos), we monitored individual IAV infection histories and immunological responses of 10 birds over the course of 15 months. This is the first detailed study to track natural IAV infection histories over several seasons amongst the same individuals growing from juvenile to adults. The general trends in the infection histories of the monitored birds reflected seasonal variation in prevalence at the population level. However, within the study group there were significant differences between individuals in infection frequency as well as in short and long term anti-IAV antibody response. Further observations included individual variation in the number of infecting virus subtypes, and a strong tendency for long-lasting hemagglutinin-related homosubtypic immunity. Specifically, all infections in the second autumn, except one, were of different subtypes compared to the first autumn. The variation among birds concerning these epidemiologically important traits illustrates the necessity for IAV studies to move from the level of populations to examine individuals in order to further our understanding of IAV disease and epidemiology.

  • 21. Wallensten, Anders
    et al.
    Munster, V
    Latorre-Margalef, Neus
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Brytting, M
    Elmberg, J
    Fouchier, R A M
    Fransson, Thord
    Haemig, Paul D
    Karlsson, Malin
    Lundkvist, Åke
    Osterhaus, A D M E
    Stervander, M
    Waldenström, Jonas
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Olsen, Björn
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Surveillance of Influenza A Virus in Migratory Waterfowl in Northern Europe2007In: Emerging Infectious Diseases, ISSN 1080-6040, E-ISSN 1080-6059, Vol. 13, no 3, p. 404-411Article in journal (Refereed)
  • 22. Wallensten, Anders
    et al.
    Munster, Vincent J.
    Latorre Margalef, Neus
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Brytting, Mia
    Elmberg, Johan
    Fouchier, Ron A.M.
    Fransson, Thord
    Haemig, Paul
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Karlsson, Malin
    Lundkvist, Åke
    Osterhaus, Albert D.M.E.
    Stervander, Martin
    Waldenström, Jonas
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Olsen, Björn
    University of Kalmar, School of Pure and Applied Natural Sciences.
    Surveillance of the Influenza A virus in migratory waterfowl in Northern Europe2007In: Emerging Infectious Diseases, ISSN 1080-6040, E-ISSN 1080-6059, Vol. 13, p. 404-411Article in journal (Refereed)
  • 23.
    Wille, Michelle
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Peter Doherty Inst Infect & Immun, Australia.
    Latorre-Margalef, Neus
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Lund University.
    Tolf, Conny
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Halpin, Rebecca
    J Craig Venter Inst, USA.
    Wentworth, David
    J Craig Venter Inst, USA.
    Fouchier, Ron A. M.
    Erasmus MC, Netherlands.
    Raghwani, Jayna
    Univ Oxford, UK.
    Pybus, Oliver G.
    Univ Oxford, UK.
    Olsen, Bjorn
    Uppsala University.
    Waldenström, Jonas
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Where do all the subtypes go?: Temporal dynamics of H8-H12 influenza A viruses in waterfowl2018In: Virus Evolution, E-ISSN 2057-1577, Vol. 4, no 2, article id vey025Article in journal (Refereed)
    Abstract [en]

    Influenza A virus (IAV) is ubiquitous in waterfowl. In the northern hemisphere IAV prevalence is highest during the autumn and coincides with a peak in viral subtype diversity. Although haemagglutinin subtypes H1-H12 are associated with waterfowl hosts, subtypes H8-H12 are detected very infrequently. To better understand the role of waterfowl in the maintenance of these rare subtypes, we sequenced H8-H12 viruses isolated from Mallards (Anas platyrhynchos) from 2002 to 2009. These rare viruses exhibited varying ecological and phylodynamic features. The Eurasian clades of H8 and H12 phylogenies were dominated by waterfowl sequences; mostly viruses sequenced in this study. H11, once believed to be a subtype that infected charadriiformes (shorebirds), exhibited patterns more typical of common virus subtypes. Finally, subtypes H9 and H10, which have maintained lineages in poultry, showed markedly different patterns: H10 was associated with all possible NA subtypes and this drove HA lineage diversity within years. Rare viruses belonging to subtypes H8-H12 were highly reassorted, indicating that these rare subtypes are part of the broader IAV pool. Our results suggest that waterfowl play a role in the maintenance of these rare subtypes, but we recommend additional sampling of non-traditional hosts to better understand the reservoirs of these rare viruses.

  • 24.
    Wille, Michelle
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Uppsala University.
    Latorre-Margalef, Neus
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. University of Georgia, USA.
    Tolf, Conny
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Stallknecht, D. E.
    University of Georgia, USA.
    Waldenström, Jonas
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    No evidence for homosubtypic immunity of influenza H3 in Mallards following vaccination in a natural experimental system2017In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 26, no 5, p. 1420-1431Article in journal (Refereed)
    Abstract [en]

    The Mallard (Anas platyrhynchos) is an important reservoir species for influenza A viruses (IAV), and in this host, prevalence and virus diversity are high. Studies have demonstrated the presence of homosubtypic immunity, where individuals are unlikely to be reinfected with the same subtype within an autumn season. Further, evidence for heterosubtypic immunity exists, whereby immune responses specific for one subtype offer partial or complete protection against related HA subtypes. We utilized a natural experimental system to determine whether homo- or heterospecific immunity could be induced following experimental vaccination. Thirty Mallards were vaccinated with an inactivated H3, H6 or a sham vaccine and after seroconversion were exposed to naturally infected wild conspecifics. All ducks were infected within 2days and had both primary and secondary infections. Overall, there was no observable difference between groups; all individuals were infected with H3 and H10 IAV. At the cessation of the experiment, most individuals had anti-NP antibodies and neutralizing antibodies against H10. Not all individuals had H3 neutralizing antibodies. The isolated H3 IAVs revealed genetic dissimilarity to the H3 vaccine strain, specifically substitutions in the vicinity of the receptor-binding site. There was no evidence of vaccine-induced homosubtypic immunity to H3, a likely result of both a poor H3 immune response in the ducks and H3 immune escape. Likewise, there was no observed heterosubtypic protection related to H6 vaccination. This study highlights the need for experimental approaches to assess how exposure to pathogens and resulting immune processes translates to individual and population disease dynamics.

  • 25.
    Wille, Michelle
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Latorre-Margalef, Neus
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Tolf, Conny
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Stallknecht, D.
    Waldenström, Jonas
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Putative escape and poor humoral response to inactivatedvaccine in Mallards results in no homo- or heterosubtypic immunity againstH3 influenza A in a natural-experimental system.Manuscript (preprint) (Other academic)
  • 26.
    Wille, Michelle
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Tolf, Conny
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Avril, Alexis
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. CIRAD, Campusinternational de Baillarguet, Montpellier 34398, France.
    Latorre-Margalef, Neus
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Wallerström, Sofie
    Karolinska institutet.
    Olsen, Björn
    Uppsala universitet.
    Waldenström, Jonas
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Frequency and patterns of reassortment in natural influenza A virus infection in a reservoir host2013In: Virology, ISSN 0042-6822, E-ISSN 1096-0341, Vol. 443, no 15, p. 150-160Article in journal (Refereed)
    Abstract [en]

    Influenza A viruses (IAV) can dramatically alter both genotype and phenotype at a rapid rate as a product of co-infection and reassortment Avian IAV exhibit high levels of phylogenetic incongruence, suggesting high levels of reassortment in the virus reservoir. Using a natural-experimental system, we reconstructed relationships amongst 92 viruses across 15 subtypes from 10 Mallards in an autumn season. Phylogenetic analyses estimated that 56% of the isolated viruses were reassorted. Network analysis demonstrated different patterns of reassortment and limited exchange of segments between primary and secondary infections. No clear patterns of linkage between segments were found, and patterns within a season were likely the consequence of continued introduction ofnew constellations, high viral load and diversity in the wild bird reservoir, and co-infections. This is the first IAV study to implement multiple tools available for elucidating factors governing reassortment patterns in naturally infected Mallards.

  • 27.
    Wille, Michelle
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Tolf, Conny
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Latorre-Margalef, Neus
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Fouchier, R. A. M.
    Halpin, R. A.
    Wentworth, D. E.
    Ragwani, J.
    Pybus, O.
    Olsen, Björn
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Waldenström, Jonas
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Limited diffusion of genome constellations and pervasive reassortment arefeatures of long-term circulation of H4N6 influenza A in European waterfowlManuscript (preprint) (Other academic)
1 - 27 of 27
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