West Nile Virus and Usutu Virus Co-Circulation in Europe: Epidemiology and Implications
Abstract
:1. Introduction
2. Transmission
3. Virology
3.1. WNV
3.2. USUV
4. Clinical Aspects
4.1. WNV
4.2. USUV
5. Diagnosis
5.1. WNV
5.2. USUV
6. Epidemiology
6.1. WNV
6.2. USUV
7. Vectors
8. WNV and USUV Co-Circulation
Funding
Conflicts of Interest
References
- De Madrid, A.T.; Porterfield, J.S. The flaviviruses (group B arboviruses): A cross-neutralization study. J. Gen. Virol. 1974, 23, 91–96. [Google Scholar] [CrossRef] [PubMed]
- May, F.J.; Davis, C.T.; Tesh, R.B.; Barrett, A.D. Phylogeography of West Nile virus: From the cradle of evolution in Africa to Eurasia, Australia, and the Americas. J. Virol. 2011, 85, 2964–2974. [Google Scholar] [CrossRef] [PubMed]
- Nikolay, B. A review of West Nile and Usutu virus co-circulation in Europe: How much do transmission cycles overlap? Trans. R. Soc. Trop. Med. Hyg. 2015, 109, 609–618. [Google Scholar] [CrossRef] [PubMed]
- Ashraf, U.; Ye, J.; Ruan, X.; Wan, S.; Zhu, B.; Cao, S. Usutu virus: An emerging flavivirus in Europe. Viruses 2015, 7, 219–238. [Google Scholar] [CrossRef] [PubMed]
- Bowen, R.A.; Nemeth, N.M. Experimental infections with West Nile virus. Curr. Opin. Infect. Dis. 2007, 20, 293–297. [Google Scholar] [CrossRef] [PubMed]
- Barbic, L.; Vilibic-Cavlek, T.; Listes, E.; Stevanovic, V.; Gjenero-Margan, I.; Ljubin-Sternak, S.; Pem-Novosel, I.; Listes, I.; Mlinaric-Galinovic, G.; Di Gennaro, A.; et al. Demonstration of Usutu virus antibodies in horses, Croatia. Vector Borne Zoonotic Dis. 2013, 13, 772–774. [Google Scholar] [CrossRef] [PubMed]
- ECDC: Reported Cases of West Nile Fever for the EU and Neighbouring Countries. Transmission Season 2013 and Previous Transmission Seasons; Latest Update: 06/11/2013. Available online: http://ecdc.europa.eu/en/healthtopics/west_nile_fever/West-Nile-fever-maps/pages/index.aspx (accessed on 23 March 2019).
- Fros, J.; Miesen, P.; Vogels, C.; Gaibani, P.; Sambri, V.; Martina, B.E.; Koenraadt, C.J.; van Rij, R.P.; Vlak, J.M.; Takken, W.; et al. Comparative Usutu and West Nile virus transmission potential by local Culex pipiens mosquitoes in north-western Europe. One Health 2015, 1, 31–36. [Google Scholar] [CrossRef] [Green Version]
- Colpitts, T.M.; Conway, M.J.; Montgomery, R.R.; Fikrig, E. West Nile Virus: Biology, transmission, and human infection. Clin. Microbiol. Rev. 2012, 25, 635–648. [Google Scholar] [CrossRef]
- Deubel, V.; Fiette, L.; Gounon, P.; Drouet, M.T.; Khun, H.; Huerre, M.; Banet, C.; Malkinson, M.; Desprès, P. Variations in biological features of West Nile viruses. Ann. N. Y. Acad. Sci. 2001, 951, 195–206. [Google Scholar] [CrossRef]
- Bakonyi, T.; Gould, E.A.; Kolodziejek, J.; Weissenböck, H.; Nowotny, N. Complete genome analysis and molecular characterization of Usutu virus that emerged in Austria in 2001: Comparison with the South African strain SAAR-1776 and other flaviviruses. Virology 2004, 328, 301–310. [Google Scholar]
- Engel, D.; Jöst, H.; Wink, M.; Börstler, J.; Bosch, S.; Garigliany, M.M.; Jöst, A.; Czajka, C.; Lühken, R.; Ziegler, U.; et al. Reconstruction of the evolutionary history and dispersal of Usutu virus, a neglected emerging arbovirus in Europe and Africa. MBio 2016, 7, e01938-15. [Google Scholar] [CrossRef] [PubMed]
- Nikolay, B.; Dupressoir, A.; Firth, C.; Faye, O.; Boye, C.S.; Diallo, M.; Sall, A.A. Comparative full length genome sequence analysis of Usutu virus isolates from Africa. Virol. J. 2013, 10, 217. [Google Scholar] [CrossRef] [PubMed]
- Murray, C.L.; Jones, C.T.; Rice, C.M. Architects of assembly: Roles of Flaviviridae non structural proteins in virion morphogenesis. Nat. Rev. Microbiol. 2008, 6, 699–708. [Google Scholar] [CrossRef] [PubMed]
- Watterson, D.; Modhiran, N.; Young, P.R. The many faces of the flavivirus NS1 protein offer a multitude of options for inhibitor design. Antiviral Res. 2016, 130, 7–18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pauli, G.; Bauerfeind, U.; Blümel, J.; Burger, R.; Drosten, C.; Gröner, A.; Gürtler, L.; Heiden, M.; Hildebrandt, M.; Jansen, B.; et al. Usutu virus. Transfus. Med. Hemother. 2014, 41, 73–82. [Google Scholar]
- Pesko, K.N.; Ebel, G.D. West Nile virus population genetics and evolution. Infect. Genet. Evol. 2012, 12, 181–190. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Petersen, L.R.; Brault, A.C.; Nasci, R.S. West Nile virus: Review of the literature. JAMA 2013, 310, 308–315. [Google Scholar] [CrossRef]
- Rossi, S.; Ross, T.; Evans, J. West Nile virus. Clin. Lab. Med. 2010, 30, 47–65. [Google Scholar] [CrossRef]
- Sambri, V.; Capobianchi, M.; Charrel, R.; Fyodorova, M.; Gaibani, P.; Gould, E.; Niedrig, M.; Papa, A.; Pierro, A.; Rossini, G.; et al. West Nile virus in Europe: Emergence, epidemiology, diagnosis, treatment, and prevention. Clin. Microbiol. Infect. 2013, 19, 699–704. [Google Scholar] [CrossRef]
- Zou, S.; Foster, G.A.; Dodd, R.Y.; Petersen, L.R.; Stramer, S.L. West Nile fever characteristics among viremic persons identified through blood donor screening. J. Infect. Dis. 2010, 202, 1354–1361. [Google Scholar]
- Carson, P.J.; Borchardt, S.M.; Custer, B.; Prince, H.E.; Dunn-Williams, J.; Winkelman, V.; Tobler, L.; Biggerstaff, B.J.; Lanciotti, R.; Petersen, L.R.; et al. Neuroinvasive disease and West Nile virus infection, North Dakota, USA, 1999–2008. Emerg. Infect. Dis. 2012, 18, 684–686. [Google Scholar] [CrossRef] [PubMed]
- Kramer, L.D.; Li, J.; Shi, P.Y. West Nile virus. Lancet Neurol. 2007, 6, 171–181. [Google Scholar] [CrossRef]
- Delbue, S.; Ferrante, P.; Mariotto, S.; Zanusso, G.; Pavone, A.; Chinaglia, M.; L’Erario, R.; Monaco, S.; Ferrari, S. Review of West Nile virus epidemiology in Italy and report of a case of West Nile virus encephalitis. J. Neurovirol. 2014, 20, 437–441. [Google Scholar] [CrossRef]
- Beasley, D.W.; Davis, C.T.; Whiteman, M.; Granwehr, B.; Kinney, R.M.; Barrett, A.D. Molecular determinants of virulence of West Nile virus in North America. Arch. Virol. Suppl. 2004, 18, 35–41. [Google Scholar]
- Papa, A. Emerging arboviral human diseases in Southern Europe. J. Med. Virol. 2017, 89, 1315–1322. [Google Scholar] [CrossRef] [PubMed]
- Patel, H.; Sander, B.; Nelder, M.P. Long-term sequelae of West Nile virus-related illness: A systematic review. Lancet Infect. Dis. 2015, 15, 951–959. [Google Scholar] [CrossRef]
- Chevalier, V.; Tran, A.; Durand, B. Predictive modeling of West Nile virus transmission risk in the Mediterranean Basin: How far from landing? Int. J. Environ. Res. Public Health. 2013, 11, 67–90. [Google Scholar] [CrossRef]
- Vazquez, A.; Jimenez-Clavero, M.; Franco, L.; Donoso-Mantke, O.; Sambri, V.; Niedrig, M.; Zeller, H.; Tenorio, A. Usutu virus: Potential risk of human disease in Europe. Euro Surveill. 2011, 16, 19935. [Google Scholar]
- Pierro, A.; Gaibani, P.; Spadafora, C.; Ruggeri, D.; Randi, V.; Parenti, S.; Finarelli, A.C.; Rossini, G.; Landini, M.P.; Sambri, V. Detection of specific antibodies against West Nile and Usutu viruses in healthy blood donors in northern Italy, 2010–2011. Clin. Microbiol. Infect. 2013, 19, E451–E453. [Google Scholar] [CrossRef]
- Pecorari, M.; Longo, G.; Gennari, W.; Grottola, A.; Sabbatini, A.; Tagliazucchi, S.; Savini, G.; Monaco, F.; Simone, M.; Lelli, R.; et al. First human case of Usutu virus neuroinvasive infection, Italy, August-September 2009. Euro Surveill. 2009, 14, 19446. [Google Scholar]
- Dauphin, G.; Zientara, S. West Nile virus: Recent trends in diagnosis and vaccine development. Vaccine 2007, 25, 5563–5576. [Google Scholar] [CrossRef] [PubMed]
- De Filette, M.; Ulbert, S.; Diamond, M.; Sanders, N.N. Recent progress in West Nile virus diagnosis and vaccination. Vet. Res. 2012, 43, 16. [Google Scholar] [CrossRef] [PubMed]
- Vilibic-Cavlek, T.; Kristofic, B.; Savic, V.; Kolaric, B.; Barbic, L.; Tabain, I.; Peric, L.; Sabadi, D.; Miklausic, B.; Potocnik-Hunjadi, T.; et al. Diagnostic significance of immunoglobulin G avidity in symptomatic and asymptomatic West Nile virus infection. Rev. Soc. Bras. Med. Trop. 2018, 51, 591–595. [Google Scholar] [CrossRef] [PubMed]
- Pierson, T.C.; Diamond, M.S. Molecular mechanisms of antibody-mediated neutralisation of flavivirus infection. Expert. Rev. Mol. Med. 2008, 10, e12. [Google Scholar] [CrossRef] [PubMed]
- Lindsey, H.S.; Calisher, C.H.; Mathews, J.H. Serum dilution neutralization test for California group virus identification and serology. J. Clin. Microbiol. 1976, 4, 503–510. [Google Scholar] [PubMed]
- Monini, M.; Falcone, E.; Busani, L.; Romi, R.; Ruggeri, F.M. West nile virus: Characteristics of an African virus adapting to the third millennium world. Open Virol. J. 2010, 4, 42–51. [Google Scholar] [CrossRef] [PubMed]
- Cavrini, F.; Della Pepa, M.E.; Gaibani, P.; Pierro, A.M.; Rossini, G.; Landini, M.P.; Sambri, V. A rapid and specific real-time RT-PCR assay to identify Usutu virus in human plasma, serum, and cerebrospinal fluid. J. Clin. Virol. 2011, 50, 221–223. [Google Scholar] [CrossRef] [PubMed]
- Nikolay, B.; Weidmann, M.; Dupressoir, A.; Faye, O.; Boye, C.S.; Diallo, M.; Sall, A.A. Development of a Usutu virus specific real-time reverse transcription PCR assay based on sequenced strains from Africa and Europe. J. Virol. Methods. 2014, 197, 51–54. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Scaramozzino, N.; Crance, J.M.; Jouan, A.; DeBriel, D.A.; Stoll, F.; Garin, D. Comparison of Flavivirus universal primer pairs and development of a rapid, highly sensitive heminested reverse transcription-PCR assay for detection of flaviviruses targeted to a conserved region of the NS5 gene sequences. J. Clin. Microbiol. 2001, 39, 1922–1927. [Google Scholar]
- Gaibani, P.; Pierro, A.; Alicino, R.; Rossini, G.; Cavrini, F.; Landini, M.P.; Sambri, V. Detection of Usutu-virus-specific IgG in blood donors from northern Italy. Vector Borne Zoonotic Dis. 2012, 12, 431–433. [Google Scholar] [CrossRef]
- Smithburn, K.C.; Hughes, T.P.; Burke, A.W.; Paul, J.H. A neurotropic virus isolated from the blood of a native of Uganda. Am. J. Trop. Med. 1940, 20, 471–492. [Google Scholar] [CrossRef]
- Bárdo, V.; Adamcová, J.; Dedei, S.; Gjini, N.; Rosicky, B.; Simkova, A. Neutralizing antibodies against some neurotropic viruses determined in human sera in Albania. J. Hyg. Epidemiol. Microbiol. Immunol. 1959, 3, 277–282. [Google Scholar]
- Zeller, H.G.; Schuffenecker, I. West Nile virus: An overview of its spread in Europe and the Mediterranean basin in contrast to its spread in the Americas. Eur. J. Clin. Microbiol. Infect. Dis. 2004, 23, 147–156. [Google Scholar] [CrossRef] [PubMed]
- Tsai, T.F.; Popovici, F.; Cernescu, C.; Campbell, G.L.; Nedelcu, N.I. West Nile encephalitis epidemic in southeastern Romania. Lancet 1998, 352, 767–771. [Google Scholar] [CrossRef]
- Jia, X.Y.; Briese, T.; Jordan, I.; Rambaut, A.; Chi, H.C.; Mackenzie, J.S.; Hall, R.A.; Scherret, J.; Lipkin, W.I. Genetic analysis of West Nile New York 1999 encephalitis virus. Lancet 1999, 354, 1971–1972. [Google Scholar] [CrossRef]
- Barzon, L.; Pacenti, M.; Franchin, E.; Pagni, S.; Lavezzo, E.; Squarzon, L.; Martello, T.; Russo, F.; Nicoletti, L.; Rezza, G.; et al. Large human outbreak of West Nile virus infection in north-eastern Italy in 2012. Viruses 2013, 5, 2825–2839. [Google Scholar] [CrossRef] [PubMed]
- Barzon, L.; Pacenti, M.; Franchin, E.; Lavezzo, E.; Masi, G.; Squarzon, L.; Pagni, S.; Toppo, S.; Russo, F.; Cattai, M.; et al. Whole genome sequencing and phylogenetic analysis of West Nile virus lineage 1 and lineage 2 from human cases of infection, Italy, August 2013. Euro Surveill. 2013, 18, 20591. [Google Scholar] [CrossRef] [Green Version]
- Zehender, G.; Veo, C.; Ebranati, E.; Carta, V.; Rovida, F.; Percivalle, E.; Moreno, A.; Lelli, D.; Calzolari, M.; Lavazza, A.; et al. Reconstructing the recent West Nile virus lineage 2 epidemic in Europe and Italy using discrete and continuous phylogeography. PLoS ONE 2017, 12, e0179679. [Google Scholar] [CrossRef]
- Barzon, L.; Pacenti, M.; Franchin, E.; Squarzon, L.; Lavezzo, E.; Cattai, M.; Cusinato, R.; Palù, G. The complex epidemiological scenario of West Nile virus in Italy. Int. J. Environ. Res. Public. Health. 2013, 10, 4669–4689. [Google Scholar] [CrossRef]
- Chaintoutis, S.; Chaskopoulos, A.; Chassalevris, T.; Koehler, P.G.; Papanastassopoulou, M.; Dovas, C.I. West Nile virus lineage 2 strain in Greece, 2012. Emerg. Infect. Dis. 2013, 1, 827–829. [Google Scholar]
- ECDC. Historical Data by Year—West Nile Fever Seasonal Surveillance. Available online: https://ecdc.europa.eu/en/west-nile-fever/surveillance-and-diseasedata/historical (accessed on 27 March 2019).
- ECDC. Epidemiological Update: West Nile Virus Transmission Season in Europe. 2018. Available online: https://ecdc.europa.eu/en/news-events/epidemiological-update-west-nile-virus-transmission-season-europe-2018 (accessed on 27 March 2019).
- McIntosh, B.M. Usutu (SAAr 1776), nouvel arbovirus du groupe B. Int. Cat. Arboviruses 1985, 3, 1059–1060. [Google Scholar]
- Weissenböck, H.; Bakonyi, T.; Rossi, G.; Mani, P.; Nowotny, N. Usutu virus, Italy, 1996. Emerg. Infect. Dis. 2013, 19, 274–277. [Google Scholar] [CrossRef] [PubMed]
- Nikolay, B.; Diallo, M.; Boye, C.S.; Sall, A.A. Usutu virus in Africa. Vector Borne Zoonotic. Dis. 2011, 11, 1417–1423. [Google Scholar] [CrossRef] [PubMed]
- Gaibani, P.; Rossini, G. An overview of Usutu virus. Microbes Infect. 2017, 19, 382–387. [Google Scholar] [CrossRef] [PubMed]
- Vilibic-Cavlek, T.; Kaic, B.; Barbic, L.; Pem-Novosel, I.; Slavic-Vrzic, V.; Lesnikar, V.; Kurecic-Filipovic, S.; Babic-Erceg, A.; Listes, E.; Stevanovic, V.; et al. First evidence of simultaneous occurrence of West Nile virus and Usutu virus neuroinvasive disease in humans in Croatia during the 2013 outbreak. Infection 2014, 42, 689–695. [Google Scholar] [CrossRef]
- Vilibic-Cavlek, T.; Savic, V.; Sabadi, D.; Peric, L.; Barbic, L.; Klobucar, A.; Miklausic, B.; Tabain, I.; Santini, M.; Vucelja, M.; et al. Prevalence and molecular epidemiology of West Nile and Usutu virus infections in Croatia in the ‘One health’ context, 2018. Transbound Emerg. Dis. 2019. [Google Scholar] [CrossRef] [PubMed]
- Cadar, D.; Maier, P.; Muller, S.; Kress, J.; Chudy, M.; Bialonski, A.; Schlaphof, A.; Jansen, S.; Jöst, H.; Tannich, E.; et al. Blood donor screening for West Nile Virus (WNV) revealed acute Usutu virus (USUV) infection, Germany, September 2016. Euro Surveill. 2017, 22, 30501. [Google Scholar] [CrossRef]
- Simonin, Y.; Sillam, O.; Carles, M.J.; Gutierrez, S.; Gil, P.; Constant, O.; Martin, M.F.; Girard, G.; Van de Perre, P.; Salinas, S.; et al. Human Usutu Virus Infection with Atypical Neurologic Presentation, Montpellier, France, 2016. Emerg. Infect. Dis. 2018, 24, 875–878. [Google Scholar] [CrossRef] [Green Version]
- Gaibani, P.; Pierro, A.M.; Cavrini, F.; Rossini, G.; Landini, M.P.; Sambri, V. False-positive transcription-mediated amplification assay detection of West Nile virus in blood from a patient with viremia caused by an Usutu virus infection. J. Clin. Microbiol. 2010, 48, 3338–3339. [Google Scholar] [CrossRef]
- Carletti, F.; Colavita, F.; Rovida, F.; Percivalle, E.; Baldanti, F.; Ricci, I.; De Liberato, C.; Rosone, F.; Messina, F.; Lalle, E.; et al. Expanding Usutu virus circulation in Italy: Detection in the Lazio region, central Italy, 2017 to 2018. Euro Surveill. 2019, 24, 1800649. [Google Scholar] [CrossRef]
- Aberle, S.W.; Kolodziejek, J.; Jungbauer, C.; Stiasny, K.; Aberle, J.H.; Zoufaly, A.; Hourfar, M.K.; Weidner, L.; Nowotny, N. Increase in human West Nile and Usutu virus infections, Austria, 2018. Euro Surveill. 2018, 23, 1800545. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Percivalle, E.; Sassera, D.; Rovida, F.; Isernia, P.; Fabbi, M.; Baldanti, F.; Marone, P. Usutu virus antibodies in blood donors and healthy forestry workers in the Lombardy Region, Northern Italy. Vector Borne Zoonotic Dis. 2017, 17, 658–661. [Google Scholar] [CrossRef] [PubMed]
- Grottola, A.; Marcacci, M.; Tagliazucchi, S.; Gennari, W.; Di Gennaro, A.; Orsini, M.; Monaco, F.; Marchegiano, P.; Marini, V.; Meacci, M.; et al. Usutu virus infections in humans: A retrospective analysis in the municipality of Modena, Italy. Clin. Microbiol. Infect. 2017, 23, 33–37. [Google Scholar] [CrossRef] [PubMed]
- Fortuna, C.; Remoli, M.E.; Di Luca, M.; Severini, F.; Toma, L.; Benedetti, E.; Bucci, P.; Montarsi, F.; Minelli, G.; Boccolini, D.; et al. Experimental studies on comparison of the vector competence of four Italian Culex pipiens populations for West Nile virus. Parasit. Vectors 2015, 8, 463. [Google Scholar] [CrossRef] [PubMed]
- Balenghien, T.; Vazeille, M.; Reiter, P.; Schaffner, F.; Zeller, H.; Bicout, D.J. Evidence of laboratory vector competence of Culex modestus for West Nile virus. J. Am. Mosq. Control Assoc. 2007, 23, 233–236. [Google Scholar] [CrossRef]
- Fortuna, C.; Remoli, M.E.; Severini, F.; Di Luca, M.; Toma, L.; Fois, F.; Bucci, P.; Boccolini, D.; Romi, R.; Ciufolini, M.G. Evaluation of vector competence for West Nile virus in Italian Stegomyia albopicta (=Aedes albopictus) mosquitoes. Med. Vet. Entomol. 2015, 29, 430–433. [Google Scholar] [CrossRef] [PubMed]
- Blagrove, M.S.C.; Sherlock, K.; Chapman, G.E.; Impoinvil, D.E.; McCall, P.J.; Medlock, J.M.; Lycett, G.; Solomon, T.; Baylis, M. Evaluation of the vector competence of a native UK mosquito Ochlerotatus detritus (Aedes detritus) for dengue, chikungunya and West Nile viruses. Parasit. Vectors 2016, 9, 1–6. [Google Scholar] [CrossRef]
- Engler, O.; Savini, G.; Papa, A.; Figuerola, J.; Groschup, M.H.; Kampen, H.; Medlock, J.; Vaux, A.; Wilson, A.J.; Werner, D.; et al. European surveillance for West Nile virus in mosquito populations. Int. J. Env. Res. Public Health 2013, 10, 4869–4895. [Google Scholar] [CrossRef]
- Bellini, R.; Zeller, H.; Van Bortel, W. A review of the vector management methods to prevent and control outbreaks of West Nile virus infection and the challenge for Europe. Parasit. Vectors. 2014, 7, 323. [Google Scholar] [CrossRef]
- Day, J.F.; Shaman, J. Mosquito-Borne Arboviral Surveillance and the Prediction of Disease Outbreaks. In Flavivirus Encephalitis; Ruzek, D., Ed.; InTech: London, UK, 2011; pp. 125–129. [Google Scholar]
- Chaskopoulou, A.; L’Ambert, G.; Petric, D.; Bellini, R.; Zgomba, M.; Groen, T.A.; Marrama, L.; Bicout, D.J. Ecology of West Nile virus across four European countries: Review of weather profiles, vector population dynamics and vector control response. Parasit. Vectors. 2016, 9, 482. [Google Scholar] [CrossRef]
- Vogels, C.B.; Göertz, G.P.; Pijlman, G.P.; Koenraadt, C.J. Vector competence of European mosquitoes for West Nile virus. Emerg. Microbes. Infect. 2017, 6, e96. [Google Scholar] [CrossRef] [PubMed]
- Garrett-Jones, C. Prognosis for interruption of malaria transmission through assessment of the mosquito’s vectorial capacity. Nature 1964, 204, 1173–1175. [Google Scholar] [CrossRef] [PubMed]
- Kenney, J.; Brault, A. The role of environmental, virological and vector interactions in dictating biological transmission of arthropod-borne viruses by mosquitoes. Adv. Virus Res. 2014, 89, 39–83. [Google Scholar] [PubMed]
- Vogels, C.B.F.; Göertz, G.P.; Pijlman, G.P.; Koenraadt, C.J.M. Vector competence of northern and southern European Culex pipiens pipiens mosquitoes for West Nile virus across a gradient of temperatures. Med. Vet. Entomol. 2017, 31, 358–364. [Google Scholar] [CrossRef] [PubMed]
- Whitfield, S.G.; Murphy, F.A.; Sudia, W.D. St. Louis encephalitis virus: An ultrastructural study of infection in a mosquito vector. Virology 1973, 56, 70–87. [Google Scholar] [CrossRef]
- Osório, H.C.; Zé-Zé, L.; Amaro, F.; Nunes, A.; Alves, M.J. Sympatric occurrence of Culex pipiens (Diptera, Culicidae) biotypes pipiens, molestus and their hybrids in Portugal, Western Europe: Feeding patterns and habitat determinants. Med. Vet. Entomol. 2014, 28, 103–109. [Google Scholar] [CrossRef] [PubMed]
- Reiter, P. West Nile virus in Europe: Understanding the present to gauge the future. Euro Surveill. 2010, 15, 19508. [Google Scholar] [PubMed]
- Walter, M.; Brugger, K.; Rubel, F. Usutu virus induced mass mortalities of songbirds in Central Europe: Are habitat models suitable to predict dead birds in unsampled regions? Prev. Vet. Med. 2018, 159, 162–170. [Google Scholar] [CrossRef]
- Nikolay, B.; Fall, G.; Boye, C.S.; Sall, A.A.; Skern, T. Validation of a structural comparison of the antigenic characteristics of Usutu virus and West Nile virus envelope proteins. Virus Res. 2014, 189, 87–91. [Google Scholar] [CrossRef]
- Oliphant, T.; Nybakken, G.E.; Engle, M.; Xu, Q.; Nelson, C.A.; Sukupolvi-Petty, S.; Marri, A.; Lachmi, B.E.; Olshevsky, U.; Fremont, D.H.; et al. Antibody recognition and neutralization determinants on domains I and II of West Nile Virus envelope protein. J. Virol. 2006, 80, 12149–12159. [Google Scholar] [CrossRef]
- Calisher, C.H.; Karabatsos, N.; Dalrymple, J.M.; Shope, R.E.; Porterfield, J.S.; Westaway, E.G.; Brandt, W.E. Antigenic relationships between flaviviruses as determined by cross-neutralization tests with polyclonal antisera. J. Gen. Virol. 1989, 70, 37–43. [Google Scholar] [CrossRef] [PubMed]
- Anderson, K.B.; Gibbons, R.V.; Thomas, S.J.; Shope, R.E.; Porterfield, J.S.; Westaway, E.G.; Brandt, W.E. Preexisting Japanese encephalitis virus neutralizing antibodies and increased symptomatic dengue illness in a school-based cohort in Thailand. PLoS Negl. Trop. Dis. 2011, 5, e1311. [Google Scholar] [CrossRef] [PubMed]
- Reisen, W.K.; Lothrop, H.D.; Wheeler, S.S.; Kennsington, M.; Gutierrez, A.; Fang, Y.; Garcia, S.; Lothrop, B. Persistent West Nile virus transmission and the apparent displacement St. Louis encephalitis virus in southeastern California, 2003–2006. J. Med. Entomol. 2008, 45, 494–508. [Google Scholar] [PubMed]
- Sinigaglia, A.; Pacenti, M.; Martello, T.; Pagni, S.; Franchin, E.; Barzon, L. West Nile virus infection in individuals with pre-existing Usutu virus immunity, northern Italy, 2018. Euro Surveill. 2019, 24, 1900261. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Salje, H.; Cummings, D.A.T.; Rodriguez-Barraquer, I.; Katzelnick, L.C.; Lessler, J.; Klungthong, C.; Thaisomboonsuk, B.; Nisalak, A.; Weg, A.; Ellison, D.; et al. Reconstruction of antibody dynamics and infection histories to evaluate dengue risk. Nature. 2018, 557, 719–723. [Google Scholar] [CrossRef] [PubMed]
- Barzon, L.; Percivalle, E.; Pacenti, M.; Rovida, F.; Zavattoni, M.; Del Bravo, P.; Cattelan, A.M.; Palù, G.; Baldanti, F. Virus and antibody dynamics in travelers with acute Zika virus infection. Clin. Infect. Dis. 2018, 6, 1173–1180. [Google Scholar] [CrossRef] [PubMed]
Physical Sequelae | |
15%–20% patients | Muscle weakness, fatigue, myalgia |
10%–15% patients | Headache |
5%–10% patients | Balance problems, visual impairment, joint weakness or pain, tremor, neck pain or stiffness |
Cognitive and Psychological Sequelae | |
15%–20% patients | Memory loss |
10%–15% patients | Depression, difficulty concentrating |
5%–10% patients | Agitation or increased sensitivity, confusion, altered mental status, aggressivity or anger, anxiety, emotional lability |
Functional Sequelae | |
40%–50% patients | Difficulty performing daily living activities |
<10% patients | Decreased activity, difficulty ambulating |
Country | Year | Clinical Presentation | N° of Cases |
---|---|---|---|
Central African Republic | 1981 | Fever and rash | 1 |
Burkina Faso | 2004 | Fever | 1 |
Italy | 2008–2009 | Neuroinvasive disease | 15 |
Croatia | 2013–2018 | Neuroinvasive disease | 6 |
Germany | 2016 | None | 1 |
France | 2016 | Neuroinvasive disease | 1 |
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Zannoli, S.; Sambri, V. West Nile Virus and Usutu Virus Co-Circulation in Europe: Epidemiology and Implications. Microorganisms 2019, 7, 184. https://doi.org/10.3390/microorganisms7070184
Zannoli S, Sambri V. West Nile Virus and Usutu Virus Co-Circulation in Europe: Epidemiology and Implications. Microorganisms. 2019; 7(7):184. https://doi.org/10.3390/microorganisms7070184
Chicago/Turabian StyleZannoli, Silvia, and Vittorio Sambri. 2019. "West Nile Virus and Usutu Virus Co-Circulation in Europe: Epidemiology and Implications" Microorganisms 7, no. 7: 184. https://doi.org/10.3390/microorganisms7070184
APA StyleZannoli, S., & Sambri, V. (2019). West Nile Virus and Usutu Virus Co-Circulation in Europe: Epidemiology and Implications. Microorganisms, 7(7), 184. https://doi.org/10.3390/microorganisms7070184