Circulation of a Meaban-like virus in yellow-legged gulls and seabird ticks in the Western Mediterranean Basin

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Arnal, Audrey ^a,b   Gómez Díaz, Elena ^c   Cerdà Cuéllar, Marta ^d,e   Lecollinet, Sylvie ^f   Pearce Duvet, Jessica ^a   Busquets, Núria ^e   García Bocanegra, Ignacio ^h   Pagès, Nonito ^e   Vittecoq, Marion ^b   Hammouda, Abdessalem ⁱ   Samraoui, Boudjéma ^j,k   Garnier, Romain ^a   Ramos, Raül ^a   Selmi, Slaheddine ⁱ   González Solís, Jacob ^g   Jourdain, Elsa ^l   Boulinier, Thierry ^a  

^a CNRS   (France)

^b STATION BIOLOGIQUE DE LA TOUR DU VALAT   (France)

^c UNIVERSITAT POMPEU FABRA   (Spain)

^d IRTA   (Spain)

^e UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^f ANSES   (France)

^g UNIVERSITY OF BARCELONA   (Spain)

^h UNIVERSITY OF CÓRDOBA   (Spain)

ⁱ UNIVERSITY OF GABES   (Tunisia)

^j UNIVERSITY OF GUELMA   (Algeria)

^k KING SAUD UNIVERSITY   (Saudi Arabia)

^l EPIA   (France)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ENVELOPE PROTEIN;

ANTIBODY DETECTION; ANTIBODY SPECIFICITY; ARTICLE; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME LINKED IMMUNOSORBENT ASSAY; FLAVIVIRUS; GENE AMPLIFICATION; IMMUNE RESPONSE; LARUS MICHAHELLIS; MARINE ENVIRONMENT; MEABAN LIKE VIRUS; MEDITERRANEAN SEA; NESTING; NONHUMAN; ORGANISM COLONY; ORNITHODOROS; ORNITHODOROS MARITIMUS; PATHOGENICITY; POLYMERASE CHAIN REACTION; SEABIRD; SEROLOGY; TICK BORNE FLAVIVIRUS; VIRUS IDENTIFICATION; VIRUS ISOLATION; VIRUS NEUTRALIZATION; WEST NILE FLAVIVIRUS; ALGERIA; ANIMAL; CHARADRIIFORMES; FLAVIVIRUS INFECTION; FRANCE; GEOGRAPHY; OOCYTE; PREVALENCE; SERODIAGNOSIS; SOUTHERN EUROPE; SPAIN; STATISTICAL MODEL; TICK; TRANSMISSION; TUNISIA; VETERINARY; VIROLOGY; WILD ANIMAL;

ALGERIA; ANIMALS; ANIMALS, WILD; CHARADRIIFORMES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLAVIVIRUS; FLAVIVIRUS INFECTIONS; FRANCE; GEOGRAPHY; LIKELIHOOD FUNCTIONS; MEDITERRANEAN REGION; NEUTRALIZATION TESTS; OVUM; PREVALENCE; SPAIN; TICKS; TUNISIA;

EID: 84898746195     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0089601     Document Type: Article

References (90)

1. Morens DM, Folkers GK, Fauci AS (2004) The challenge of emerging and reemerging infectious diseases. Nature 430: 242-249. (Pubitemid 38902437)
2. Meslin FX (1997) Global aspects of emerging and potential zoonoses: a WHO perspective. Emerg Infect Dis 3: 223-228.
3. Woolhouse M, Gaunt E (2007) Ecological origins of novel human pathogens. Crit Rev Microbiol 33: 231-242. (Pubitemid 350146703)
4. Reed KD, Meece JK, Henkel JS, Shukla SK (2003) Birds, migration and emerging zoonoses: west nile virus, lyme disease, influenza A and enteropathogens. Clin Med Res 1: 5-12.
5. Murphy FA (1998) Emerging zoonoses. Emerg Infect Dis 4: 429-435.
6. Jourdain E, Gauthier-Clerc M, Bicout DJ, Sabatier P (2007) Bird migration routes and risk for pathogen dispersion into western Mediterranean wetlands. Emerg Infect Dis 13: 365-372. (Pubitemid 46348122)
7. Rappole JH, Derrickson SR, Hubalek Z (2000) Migratory birds and spread of West Nile virus in the Western Hemisphere. Emerg Infect Dis 6: 319-328. (Pubitemid 30643651)
8. LaDeau SL, Kilpatrick AM, Marra PP (2007) West Nile virus emergence and large-scale declines of North American bird populations. Nature 447: 710-713. (Pubitemid 46889724)
9. Lanciotti RS, Roehrig JT, Deubel V, Smith J, Parker M, et al. (1999) Origin of the West Nile virus responsible for an outbreak of encephalitis in the northeastern United States. Science 286: 2333-2337. (Pubitemid 30016893)
10. Webster RG, Krauss S, Hulse-Post D, Sturm-Ramirez K (2007) Evolution of influenza a viruses in wild birds. J Wildl Dis 43: S1-S6. (Pubitemid 47342966)
11. Gauthier-Clerc M, Lebarbenchon C, Thomas F (2007) Recent expansion of highly pathogenic avian influenza H5N1: a critical review. Ibis 149: 202-214. (Pubitemid 46525262)
12. Weissenboeck H, Hubalek Z, Bakonyi T, Nowotny N (2010) Zoonotic mosquito-borne flaviviruses: worldwide presence of agents with proven pathogenicity and potential candidates of future emerging diseases. Vet Microbiol 140: 271-280.
13. Gould EA, Lamballerie Xd, Zanotto PMdA, Holmes EC (2003) Origins, evolution, and vector/host coadaptations within the genus Flavivirus. Adv Virus Res 59: 277: 277-314.
14. Porterfield JS (1975) Basis of arbovirus classification. Med Biol 53: 400-405.
15. Mansfield KL, Johnson N, Phipps LP, Stephenson JR, Fooks AR, et al. (2009) Tick-borne encephalitis virus - a review of an emerging zoonosis. J Gen Virol 90: 1781-1794.
16. Lundström JO (1999) Mosquito-borne viruses in western Europe: a review. J Vector Ecol 24: 1-39.
17. Berthold P, editor(2001) Bird migration: a general survey. Second Edition ed: Oxford University Press. 272 p.
18. Jourdain E, Schuffenecker I, Korimbocus J, Reynard S, Murri S, et al. (2007) West Nile virus in wild resident birds, Southern France, 2004. Vector-Borne Zoonotic Dis 7: 448-452. (Pubitemid 47536190)
19. Murgue B, Murri S, Zientara S, Durand B, Durand JP, et al. (2001) West Nile outbreak in horses in Southern France, 2000: the return after 35 years. Emerg Infect Dis 7: 692-696. (Pubitemid 32845261)
20. Jimenez-Clavero MA, Llorente F, Sotelo E, Soriguer R, Gomez-Tejedor C, et al. (2010) West Nile virus serosurveillance in horses in Donana, Spain, 2005 to 2008. Vet Rec 167: 379-380.
21. Figuerola J, Soriguer R, Rojo G, Tejedor CG, Jimenez-Clavero MA (2007) Seroconversion in wild birds and local circulation of West Nile virus, Spain. Emerg Infect Dis 13: 1915-1917. (Pubitemid 350248497)
22. Bofill D, Domingo C, Cardenosa N, Zaragoza J, de Ory F, et al. (2006) Human West Nile virus infection, Catalonia, Spain. Emerg Infect Dis 12: 1163-1164. (Pubitemid 44061296)
23. Vazquez A, Sanchez-Seco M-P, Palacios G, Molero F, Reyes N, et al. (2012) Novel flaviviruses detected in different species of mosquitoes in Spain. Vector- Borne Zoonotic Dis 12: 223-229.
24. EpiSouth (2010) West Nile virus circulation in the EpiSouth countries and neighbouring areas (Hungary and Russia) - Update 6th of October 2010. 5 p.
25. Vazquez A, Jimenez-Clavero M, Franco L, Donoso-Mantke O, Sambri V, et al. (2011) Usutu virus: potential risk of human disease in Europe. Euro Surveill 16.
26. Höfle U, Gamino V, Fernández de Mera IG, Mangold AJ, Ortíz J-A, et al. (2000) Usutu Virus in Migratory Song Thrushes, Spain. Emerging Infectious Diseases 267: 1741-1744.
27. Agüero M, Fernandez-Pinero J, Buitrago D, Sanchez A, Elizalde M, et al. (2011) Bagaza virus in partridges and pheasants, Spain, 2010. Emerg Infect Dis 17: 1498-1501.
28. Gaunt MW, Sall AA, de Lamballerie X, Falconar AKI, Dzhivanian TI, et al. (2001) Phylogenetic relationships of flaviviruses correlate with their epidemiology, disease association and biogeography. J Gen Virol 82: 1867-1876. (Pubitemid 32707550)
29. Labuda M, Nuttall PA (2004) Tick-borne viruses. Parasitology 129: S221-S245. (Pubitemid 40780697)
30. Heinze DM, Gould EA, Forrester NL (2012) Revisiting the clinal concept of evolution and dispersal for the tick-borne flaviviruses by using phylogenetic and biogeographic analyses. J Virol 86: 8663-8671.
31. Cramp S, Simmons KEL, editors (1983) Handbook of the birds of Europe, the Middle East and North Africa: the birds of the Western Paleartic. 1st ed: Oxford University Press. 913 p.
32. Oro D, Martinez-Abrain A (2007) Deconstructing myths on large gulls and their impact on threatened sympatric waterbirds. Anim Conserv 10: 117-126. (Pubitemid 46189186)
33. Bosch M, Figuerola J (1999) Detrimental effects of ticks Ornithodoros maritimus on the growth of yellow-legged gull Larus michahellis chicks. Ardea 87: 83-89. (Pubitemid 29492464)
34. Dietrich M, Gómez-Díaz E, McCoy KD (2011) Worldwide distribution and diversity of seabird ticks: implications for the ecology and epidemiology of tickborne pathogens. Vector-Borne Zoonotic Dis 11: 453-470.
35. Baaloudj A, Samraoui F, Laouar A, Benoughidene M, Hasni D, et al. (2012) Dispersal of yellow-legged gulls Larus michahellis ringed in Algeria: a preliminary analysis. Ardeola 59: 137-144.
36. Hars J, Cuge P, Chavernac D, Balanca G, Keck N, et al. (2004) Surveillance de l'infection de l'avifaune camarguaise par le virus West Nile. Faune Sauvage 261: 54-58.
37. Malkinson M, Banet C, Weisman Y, Pokamunski S, King R, et al. (2002) Introduction of West Nile virus in the Middle East by migrating white storks. Emerg Infect Dis 8: 392-397. (Pubitemid 34415201)
38. Monaco F, Savini G, Calistri P, Polci A, Pinoni C, et al. (2011) 2009 West Nile disease epidemic in Italy: first evidence of overwintering in Western Europe? Res Vet Sci 91: 321-326.
39. Hubalek Z, Wegner E, Halouzka J, Tryjanowski P, Jerzak L, et al. (2008) Serologic survey of potential vertebrate hosts for West Nile virus in Poland. Viral Immunol 21: 247-253. (Pubitemid 351873372)
40. Alba A, Allepuz A, Napp S, Soler M, Selga I, et al. (2013) Ecological surveillance for West Nile in Catalonia (Spain), learning from a five-year period of follow-up. Zoonoses Pub Hlth: doi: 10.1111/zph.12048
41. Komar N, Langevin S, Hinten S, Nemeth N, Edwards E, et al. (2003) Experimental infection of north American birds with the New York 1999 strain of West Nile virus. Emerg Infect Dis 9: 311-322. (Pubitemid 36330872)
42. Jourdain E, Toussaint Y, Leblond A, Bicout DJ, Sabatier P, et al. (2007) Bird species potentially involved in introduction, amplification, and spread of West Nile virus in a Mediterranean wetland, the Camargue (Southern France). Vector-Borne Zoonotic Dis 7: 15-33. (Pubitemid 46626687)
43. Calistri P, Giovannini A, Hubalek Z, Ionescu A, Monaco F, et al. (2010) Epidemiology of West Nile in Europe and in the Mediterranean Basin. Open Virol J 4: 29-37.
44. Calzolari M, Bonilauri P, Bellini R, Albieri A, Defilippo F, et al. (2010) Evidence of simultaneous circulation of West Nile and Usutu viruses in mosquitoes sampled in Emilia-Romagna region (Italy) in 2009. PLoS ONE 5: e14324-e14324.
45. Vidal E, Medail F, Tatoni T (1998) Is the yellow-legged gull a superabundant bird species in the Mediterranean? Impact on fauna and flora, conservation measures and research priorities. Biodivers Conserv 7: 1013-1026. (Pubitemid 29020091)
46. Peruski LF, Peruski AH (2003) Rapid diagnostic assays in the genomic biology era: detection and identification of infectious disease and biological weapon agents. Biotechniques 35: 840-846.
47. Arens M (1999) Methods for subtyping and molecular comparison of human viral genomes. Clin Microbiol Rev 12: 612-626.
48. Huhtamo E, Hasu E, Uzcategui NY, Erra E, Nikkari S, et al. (2010) Early diagnosis of dengue in travelers: comparison of a novel real-time RT-PCR, NS1 antigen detection and serology. J Clin Virol 47: 49-53.
49. Pedersen AB, Babayan SA (2011) Wild immunology. Mol Ecol 20: 872-880.
50. Boulinier T, Staszewski V (2008) Maternal transfer of antibodies: raising immuno-ecology issues. Trends Ecol Evol 23: 282-288. (Pubitemid 351626205)
51. Gasparini J, McCoy KD, Haussy C, Tveraa T, Boulinier T (2001) Induced maternal response to the Lyme disease spirochaete Borrelia burgdorferi sensu lato in a colonial seabird, the kittiwake Rissa tridactyla. P Roy Soc B-Biol Sci 268: 647-650.
52. Gasparini J, McCoy KD, Tveraa T, Boulinier T (2002) Related concentrations of specific immunoglobulins against the Lyme disease agent Borrelia burgdorferi sensu lato in eggs, young and adults of the kittiwake (Rissa tridactyla). Ecol Lett 5: 519-524. (Pubitemid 34824911)
53. Hammouda A, Pearce-Duvet J, Chokri MA, Arnal A, Gauthier-Clerc M, et al. (2011) Prevalence of Influenza A antibodies in yellow-legged gull (Larus michahellis) eggs and adults Southern Tunisia. Vector-Borne Zoonotic Dis 11: 1583-1590.
54. Pearce-Duvet JMC, Gauthier-Clerc M, Jourdain E, Boulinier T (2009) Maternal antibody transfer in yellow-legged gulls. Emerg Infect Dis 15: 1147-1149.
55. Gibbs SEJ, Hoffman DM, Stark LM, Marlenee NL, Blitvich BJ, et al. (2005) Persistence of antibodies to West Nile virus in naturally infected rock pigeons (Columba livia) . Clin Diag Lab Immunol 12: 665-667. (Pubitemid 41184729)
56. Nemeth NM, Oesterle PT, Bowen RA (2009) Humoral immunity to West Nile virus is long-lasting and protective in the house sparrow (Passer domesticus). Am J Trop Med Hyg 80: 864-869.
57. Sol D, Arcos JM, Senar JC (1995) The influence of refuse tips on the winter distribution of yellow-legged gulls Larus cachinnans . Bird Study 42: 216-221.
58. Ramos R, Ramirez F, Sanpera C, Jover L, Ruiz X (2009) Feeding ecology of yellow-legged gulls Larus michahellis in the Western Mediterranean: a comparative assessment using conventional and isotopic methods. Mar Ecol-Prog Ser 377: 289-297.
59. Jupp PG, McIntosh BM, Dickinson DB (1972) Quantitative experiments on the vector capability of Culex (Culex) theileri theobald with West Nile and Sindbis viruses. J Med Entomol 9: 393-395.
60. Dauphin G, Zientara S (2007) West Nile virus: recent trends in diagnosis and vaccine development. Vaccine 25: 5563-5576. (Pubitemid 47031364)
61. Oliphant T, Diamond MS (2007) The molecular basis of antibody-mediated neutralization of West Nile virus. Expert Opin Biol Th 7: 885-892. (Pubitemid 46954434)
62. Beck C, Jimenez-Clavero M, Leblond A, Durand B, Nowotny N, et al. (2013) Flaviviruses in Europe: Complex Circulation Patterns and Their Consequences for the Diagnosis and Control of West Nile Disease. International Journal of Environmental Research and Public Health 10: 6049-6083.
63. Hobson-Peters J (2012) Approaches for the development of rapid serological assays for surveillance and diagnosis of infections caused by zoonotic flaviviruses of the Japanese encephalitis virus serocomplex. J Biomed Biotech 2012: 379738-379738.
64. Figuerola J, Jimenez-Clavero MA, Rojo G, Gomez-Tejedor C, Soriguer R (2007) Prevalence of West Nile virus neutralizing antibodies in colonial aquatic birds in Southern Spain. Avian Pathol 36: 209-212.
65. Garnier R, Ramos R, Staszewski V, Militao T, Lobato E, et al. (2012) Maternal antibody persistence: a neglected life-history trait with implications from albatross conservation to comparative immunology. P Roy Soc B-Biol Sci 279: 2033-2041.
66. Rangel TF, Diniz-Filho JAF, Bini LM (2010) SAM: a comprehensive application for Spatial Analysis in Macroecology. Ecography 33: 46-50.
67. Sanchez-Seco MP, Rosario D, Domingo C, Hernandez L, Valdes K, et al. (2005) Generic RT-nested-PCR for detection of flaviviruses using degenerated primers and internal control followed by sequencing for specific identification. J Virol Methods 126: 101-109. (Pubitemid 40558749)
68. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
69. Cook S, Holmes EC (2006) A multigene analysis of the phylogenetic relationships among the flaviviruses (Family : Flaviviridae) and the evolution of vector transmission. Arch Virol 151: 309-325. (Pubitemid 43130590)
70. Grard G, Moureau G, Charrel RN, Lemasson J-J, Gonzalez J-P, et al. (2007) Genetic characterization of tick-borne flaviviruses: New insights into evolution, pathogenetic determinants and taxonomy. Virology 361: 80-92. (Pubitemid 46566451)
71. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
72. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25: 1253-1256.
73. Chastel C, Le Lay G, Legrand-Quillien MC, Le Goff F (1988) Distribution inégale des arbovirus transmis par des tiques dans les colonies d'oiseaux de mer du nord et du sud de la France. CR Acad Sci 307: 479-484.
74. Arizaga J, Herrero A, Galarza A, Hidalgo J, Aldalur A, et al. (2010) First-year movements of yellow-legged gull (Larus michahellis lusitanius) from the Southeastern Bay of Biscay. Waterbirds 33: 444-450.
75. McCoy KD, Boulinier T, Tirard C (2005) Comparative host-parasite population structures: disentangling prospecting and dispersal in the black-legged kittiwake Rissa tridactyla. Molecular Ecology 14: 2825-2838. (Pubitemid 41576964)
76. Gómez-Díaz E, Morris-Pocock JA, Gonzalez-Solis J, McCoy KD (2012) Trans-oceanic host dispersal explains high seabird tick diversity on Cape Verde islands. Biol Lett 8: 616-619.
77. Garcia-Bocanegra I, Busquets N, Napp S, Alba A, Zorrilla I, et al. (2011) Serosurvey of West Nile virus and other flaviviruses of the Japanese encephalitis antigenic complex in birds from Andalusia, Southern Spain. Vector-Borne Zoonotic Dis 11: 1107-1113.
78. Llorente F, Perez-Ramirez E, Fernandez-Pinero J, Soriguer R, Figuerola J, et al. (2013) Flaviviruses in game birds, Southern Spain, 2011-2012. Emerg Infect Dis 19: 1023-1025.
79. Sotelo E, Fernandez-Pinero J, Llorente F, Aguero M, Hoefle U, et al. (2009) Characterization of West Nile virus isolates from Spain: new insights into the distinct West Nile virus eco-epidemiology in the Western Mediterranean. Virology 395: 289-297.
80. Vazquez A, Ruiz S, Herrero L, Moreno J, Molero F, et al. (2011) West Nile and Usutu viruses in mosquitoes in Spain, 2008-2009. Am J Trop Med Hyg 85: 178-181.
81. Murgue B, Murri S, Triki H, Deubel V, Zeller HG (2001) West Nile in the Mediterranean basin: 1950-2000. In: White DJ, Morse DL, editors. West Nile Virus: Detection, Surveillance, and Control. pp. 117-126. (Pubitemid 34060038)
82. Chastel C, Main AJ, Guiguen C, Lelay G, Quillien MC, et al. (1985) The isolation of Meaban virus, a new Flavivirus from the seabird tick Ornithodoros (Alectorobius) maritimus in France. Arch Virol 83: 129-140. (Pubitemid 15162600)
83. EstradaPena A, Bosch M, Pedrocchi V (1996) First record of Ornithodoros (Alectorobius) maritimus Vermeil & Marguet (Acari: Argasidae) in Spain. Acarologia 37: 19-21.
84. Oro D (2008) Living in a ghetto within a local population: an empirical example of an ideal despotic distribution. Ecology 89: 838-846.
85. Gómez-Díaz E, Boulinier T, Sertour N, Cornet M, Ferquel E, et al. (2011) Genetic structure of marine Borrelia garinii and population admixture with the terrestrial cycle of Lyme borreliosis. Environmental Microbiology 13: 2453-2467.
86. Chastel C, Guiguen C, Lelay G, Monnat JY, Quillien MC, et al. (1983) Are the Arboviruses from seabirds colonies in Brittany able to infect man. Rev Epidémiol Santé Publique 31: 445-457. (Pubitemid 14157482)
87. Dobler G (2010) Zoonotic tick-borne flaviviruses. Vet Microbiol 140: 221-228.
88. Mackenzie JS, Williams DT (2009) The zoonotic flaviviruses of Southern, South- Eastern and Eastern Asia, and Australasia: the potential for emergent viruses. Zoonoses Pub Hlth 56: 338-356.
89. Nuttall PA, Kelly TC, Carey D, Moss SR, Harrap KA (1984) Mixed infections with tick-borne viruses in a seabird colony in Eire. Arch Virol 79: 35-44. (Pubitemid 14177946)
90. Gómez-Díaz E, Doherty PF Jr, Duneau D, McCoy KD (2010) Cryptic vector divergence masks vector-specific patterns of infection: an example from the marine cycle of Lyme borreliosis. Evol Appl 3: 391-401.