Virology Journal | |
Molecular and epidemiological characterization of avian influenza viruses from gulls and dabbling ducks in Norway | |
Anna G Hauge2  Espen Rimstad1  Elisabeth F Hansen1  Monika J Hjortaas2  Christine M Jonassen2  Anja B Kristoffersen2  Ragnhild Tønnessen3  | |
[1] Department of Food Safety & Infection Biology, Norwegian School of Veterinary Science, P. O. Box 8146 Dep N-0033, Oslo, Norway;Norwegian Veterinary Institute, P. O. Box 750 Sentrum, N-0106, Oslo, Norway;Present address: Norwegian Veterinary Institute, P. O. Box 750 Sentrum, N-0106, Oslo, Norway | |
关键词: Reassortment; Epidemiology; Gulls; Dabbling ducks; Avian influenza virus; | |
Others : 1150926 DOI : 10.1186/1743-422X-10-112 |
|
received in 2012-08-26, accepted in 2013-04-03, 发布年份 2013 | |
【 摘 要 】
Background
Wild aquatic birds constitute the natural reservoir for avian influenza viruses (AIVs). Separate Eurasian and American AIV gene pools exist. Here, the prevalence and diversity of AIVs in gulls and dabbling ducks in Norway were described. The influence of host species and temporal changes on AIV prevalence was examined. Five AIVs from Norway, including three from common gull (Larus canus), were analyzed along with 10 available AIV genomes from gulls in Eurasia to search for evidence of intracontinental and intercontinental reassortment of gene segments encoding the internal viral proteins.
Methods
Swabs collected from 2417 dabbling ducks and gulls in the south-west of Norway during five ordinary hunting seasons (August-December) in the period 2005–2010 were analyzed for presence of AIV. Multivariate linear regression was used to identify associations between AIV prevalence, host species and sampling time. Five AIVs from mallard (Anas platyrhynchos) (H3N8, H9N2) and common gull (H6N8, H13N2, H16N3) were full-length characterized and phylogenetically analyzed together with GenBank reference sequences.
Results
Low pathogenic AIVs were detected in 15.5% (CI: 14.1–17.0) of the samples. The overall AIV prevalence was lower in December compared to that found in August to November (p = 0.003). AIV was detected in 18.7% (CI: 16.8–20.6) of the dabbling ducks. A high AIV prevalence of 7.8% (CI; 5.9–10.0) was found in gulls. A similar temporal pattern in AIV prevalence was found in both bird groups. Thirteen hemagglutinin and eight neuraminidase subtypes were detected. No evidence of intercontinental reassortment was found. Eurasian avian (non H13 and H16) PB2 or PA genes were identified in five reference Eurasian gull (H13 and H16) AIV genomes from GenBank. The NA gene from the Norwegian H13N2 gull isolate was of Eurasian avian origin.
Conclusions
The similar temporal pattern in AIV prevalence found in dabbling ducks and gulls, the relatively high virus prevalence detected in gulls and the evidence of intracontinental reassortment in AIVs from gulls indicate that gulls that interact with dabbling ducks are likely to be mixing vessels for AIVs from waterfowl and gulls. Our results support that intercontinental reassortment is rare in AIVs from gulls in Eurasia.
【 授权许可】
2013 Tønnessen et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20150406004243482.pdf | 926KB | download | |
Figure 4. | 88KB | Image | download |
Figure 3. | 29KB | Image | download |
Figure 2. | 36KB | Image | download |
Figure 1. | 33KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
Figure 4.
【 参考文献 】
- [1]Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y: Evolution and ecology of influenza A viruses. Microbiol Rev 1992, 56:152-179.
- [2]Fouchier RAM, Munster V, Wallensten A, Bestebroer TM, Herfst S, Smith D, Rimmelzwaan GF, Olsen B, Osterhaus ADME: Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J Virol 2005, 79:2814-2822.
- [3]Jourdain E, van RD, Munster VJ, Kuiken T, Waldenstrom J, Olsen B, Ellstrom P: The pattern of influenza virus attachment varies among wild bird species. PLoS One 2011, 6:e24155.
- [4]Webster RG, Yakhno M, Hinshaw VS, Bean WJ, Murti KG: Intestinal influenza: replication and characterization of influenza viruses in ducks. Virology 1978, 84:268-278.
- [5]Brown JD, Goekjian G, Poulson R, Valeika S, Stallknecht DE: Avian influenza virus in water: infectivity is dependent on pH, salinity and temperature. Vet Microbiol 2009, 136:20-26.
- [6]Nazir J, Haumacher R, Ike AC, Marschang RE: Persistence of avian influenza viruses in lake sediment, duck feces, and duck meat. Appl Environ Microbiol 2011, 77:4981-4985.
- [7]Munster VJ, Baas C, Lexmond P, Waldenstrom J, Wallensten A, Fransson T, Rimmelzwaan GF, Beyer WE, Schutten M, Olsen B: Spatial, temporal, and species variation in prevalence of influenza A viruses in wild migratory birds. PLoS Pathog 2007, 3:e61.
- [8]Olsen B, Munster VJ, Wallensten A, Waldenstrom J, Osterhaus AD, Fouchier RA: Global patterns of influenza a virus in wild birds. Science 2006, 312:384-388.
- [9]Gaidet N, Ould El Mamy AB, Cappelle J, Caron A, Cumming GS, Grosbois V, Gil P, Hammoumi S, de Almeida RS, Fereidouni SR: PLoS One. 2012, 7:e46049.
- [10]Velarde R, Calvin SE, Ojkic D, Barker IK, Nagy E: Avian influenza virus H13 circulating in ring-billed gulls (Larus delawarensis) in southern Ontario, Canada. Avian Dis 2010, 54:411-419.
- [11]Tønnessen R, Valheim M, Rimstad E, Jonassen CM, Germundsson A: Experimental incoulation of chickens with gull-derived low pathogenic avian influenza virus subtype H16N3 causes limited infection. Avian Dis 2011, 55:680-685.
- [12]Wallensten A, Munster VJ, Elmberg J, Osterhaus AD, Fouchier RA, Olsen B: Multiple gene segment reassortment between Eurasian and American lineages of influenza A virus (H6N2) in Guillemot (Uria aalge). Arch Virol 2005, 150:1685-1692.
- [13]Lebarbenchon C, Chang CM, Gauthier-Clerc M, Thomas F, Renaud F, van der Werf S: H9N2 avian influenza virus in a Mediterranean gull. J Mol Genet Med 2008, 3:121-123.
- [14]Krauss S, Obert CA, Franks J, Walker D, Jones K, Seiler P, Niles L, Pryor SP, Obenauer JC, Naeve CW: Influenza in migratory birds and evidence of limited intercontinental virus exchange. PLoS Pathog 2007, 3:e167.
- [15]Koehler AV, Pearce JM, Flint PL, Franson JC, Ip HS: Genetic evidence of intercontinental movement of avian influenza in a migratory bird: the northern pintail (Anas acuta). Mol Ecol 2008, 17:4754-4762.
- [16]Dugan VG, Chen R, Spiro DJ, Sengamalay N, Zaborsky J, Ghedin E, Nolting J, Swayne DE, Runstadler JA, Happ GM: The evolutionary genetics and emergence of avian influenza viruses in wild birds. PLoS Pathog 2008, 4:e1000076.
- [17]Manzoor R, Sakoda Y, Mweene A, Tsuda Y, Kishida N, Bai GR, Kameyama K, Isoda N, Soda K, Naito M: Phylogenic analysis of the M genes of influenza viruses isolated from free-flying water birds from their Northern Territory to Hokkaido, Japan. Virus Genes 2008, 37:144-152.
- [18]Ramey AM, Pearce JM, Ely CR, Sheffield Guy LM, Irons DB, Derksen DV, Ip HS: Transmission and reassortment of avian influenza viruses at the Asian-North American interface. Virology 2010, 406:352-359.
- [19]Wille M, Robertson GJ, Whitney H, Bishop MA, Runstadler JA, Lang AS: Extensive geographic mosaicism in avian influenza viruses from gulls in the northern hemisphere. PLoS One 2011, 6:e20664.
- [20]Wille M, Robertson GJ, Whitney H, Ojkic D, Lang AS: Reassortment of American and Eurasian genes in an influenza A virus isolated from a great black-backed gull (Larus marinus), a species demonstrated to move between these regions. Arch Virol 2011, 156:107-115.
- [21]zu Dohna H, Li J, Cardona CJ, Miller J, Carpenter TE: Invasions by Eurasian avian influenza virus H6 genes and replacement of the virus’ North American clade. Emerg Infect Dis 2009, 15:1040-1045.
- [22]Hinshaw VS, Air GM, Gibbs AJ, Graves L, Prescott B, Karunakaran D: Antigenic and genetic characterization of a novel hemagglutinin subtype of influenza A viruses from gulls. J Virol 1982, 42:865-872.
- [23]Van Borm S, Rosseel T, Vangeluwe D, Vandenbussche F, van den Berg T, Lambrecht B: Phylogeographic analysis of avian influenza viruses isolated from Charadriiformes in Belgium confirms intercontinental reassortment in gulls. Arch Virol 2012, 157:1509-1522.
- [24]Jonassen CM, Handeland K: Avian influenza virus screening in wild waterfowl in Norway, 2005. Avian Dis 2007, 51:425-428.
- [25]Germundsson A, Madslien KI, Hjortaas MJ, Handeland K, Jonassen CM: Prevalence and subtypes of influenza A viruses in wild waterfowl in Norway 2006-2007. Acta Vet Scand 2010, 52:28. BioMed Central Full Text
- [26]Slomka MJ, Pavlidis T, Banks J, Shell W, McNally A, Essen S, Brown IH: Validated H5 Eurasian real-time reverse transcriptase-polymerase chain reaction and its application in H5N1 outbreaks in 2005-2006. Avian Dis 2007, 51:373-377.
- [27]Phipps LP, Essen SC, Brown IH: Genetic subtyping of influenza A viruses using RT-PCR with a single set of primers based on conserved sequences within the HA2 coding region. J Virol Methods 2004, 122:119-122.
- [28]Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR: Universal primer set for the full-length amplification of all influenza A viruses. Arch Virol 2001, 146:2275-2289.
- [29]WHO Manual of Animal Influenza Diagnosis and Surveillance. http://www.who.int/vaccine_research/diseases/influenza/WHO_manual_on_animal-diagnosis_and_surveillance_2002_5.pdf webcite
- [30]BLAST: Basic local alignment search tool. http://blast.ncbi.nlm.nih.gov/ webcite
- [31]Influenza virus resource. http://www.ncbi.nlm.nih.gov/genomes/FLU/Database/nph-select.cgi?go=genomeset webcite
- [32]Bui VN, Ogawa H, Xininigen , Karibe K, Matsuo K, Awad SS, Minoungou GL, Yoden S, Haneda H, Ngo LH: H4N8 subtype avian influenza virus isolated from shorebirds contains a unique PB1 gene and causes severe respiratory disease in mice. Virology 2012, 423:77-88.
- [33]Tamura K, Dudley J, Nei M, Kumar S: MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599.
- [34]R Core Team: R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2012.
- [35]Pearce JM, Ramey AM, Ip HS, Gill RE Jr: Limited evidence of trans-hemispheric movement of avian influenza viruses among contemporary North American shorebird isolates. Virus Res 2010, 148:44-50.
- [36]Wallensten A, Munster VJ, Latorre-Margalef N, Brytting M, Elmberg J, Fouchier RA, Fransson T, Haemig PD, Karlsson M, Lundkvist A: Surveillance of influenza A virus in migratory waterfowl in northern Europe. Emerg Infect Dis 2007, 13:404-411.
- [37]Hill NJ, Takekawa JY, Cardona CJ, Ackerman JT, Schultz AK, Spragens KA, Boyce WM: Waterfowl ecology and avian influenza in California: do host traits inform us about viral occurrence? Avian Dis 2010, 54:426-432.
- [38]Bakken V, Runde O, Tjørve E: Norwegian bird ringing atlas. Divers - Auks. Stavanger Museum: Stavanger; 2003.
- [39]Toennessen R, Germundsson A, Jonassen CM, Haugen I, Berg K, Barrett RT, Rimstad E: Virological and serological surveillance for type A influenza in the black-legged kittiwake (Rissa tridactyla). Virol J 2011, 8:21. BioMed Central Full Text
- [40]Spackman E, Swayne DE, Gilbert M, Joly DO, Karesh WB, Suarez DL, Sodnomdarjaa R, Dulam P, Cardona C: Characterization of low pathogenicity avian influenza viruses isolated from wild birds in Mongolia 2005 through 2007. Virol J 2009, 6:190. BioMed Central Full Text