1887
Surveillance Open Access
Like 0

Abstract

Background

Usutu virus (USUV) is a flavivirus with an enzootic cycle between birds and mosquitoes; humans are incidental dead-end hosts. In Europe, the virus was first detected in Italy in 1996; since then, it has spread to many European countries.

Aim

We aimed to report on the epidemiology, surveillance, diagnosis and prevention of USUV infection in humans, mosquitoes and other animals in the European Union/European Economic Area (EU/EEA) from 2012 to 2021.

Methods

We collected information through a literature review, an online survey and an expert meeting.

Results

Eight countries reported USUV infection in humans (105 cases, including 12* with neurological symptoms), 15 countries in birds and seven in mosquitoes. Infected animals were also found among pets, wild and zoo animals. Usutu virus was detected primarily in but also in six other mosquito species. Detection of USUV infection in humans is notifiable only in Italy, where it is under surveillance since 2017 and now integrated with surveillance in animals in a One Health approach. Several countries include USUV infection in the differential diagnosis of viral encephalitis and arbovirus infections. Animal USUV infection is not notifiable in any EU/EEA country.

Conclusion

Human USUV infections, mainly asymptomatic and, less frequently, with a febrile illness or a neuroinvasive disease, have been reported in several EU/EEA countries, where the virus is endemic. Climate and environmental changes are expected to affect the epidemiology of USUV. A One Health approach could improve the monitoring of its evolution in Europe.

Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2023.28.33.2200929
2023-08-17
2024-04-27
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2023.28.33.2200929
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/28/33/eurosurv-28-33-1.html?itemId=/content/10.2807/1560-7917.ES.2023.28.33.2200929&mimeType=html&fmt=ahah

References

  1. Weissenböck H, Bakonyi T, Rossi G, Mani P, Nowotny N. Usutu virus, Italy, 1996. Emerg Infect Dis. 2013;19(2):274-7.  https://doi.org/10.3201/eid1902.121191  PMID: 23347844 
  2. Zecchin B, Fusaro A, Milani A, Schivo A, Ravagnan S, Ormelli S, et al. The central role of Italy in the spatial spread of USUTU virus in Europe. Virus Evol. 2021;7(1):veab048.  https://doi.org/10.1093/ve/veab048  PMID: 34513027 
  3. Scaramozzino P, Carvelli A, Bruni G, Cappiello G, Censi F, Magliano A, et al. West Nile and Usutu viruses co-circulation in central Italy: outcomes of the 2018 integrated surveillance. Parasit Vectors. 2021;14(1):243.  https://doi.org/10.1186/s13071-021-04736-z  PMID: 33962673 
  4. Rijks JM, Kik ML, Slaterus R, Foppen R, Stroo A, IJzer J, et al. Widespread Usutu virus outbreak in birds in the Netherlands, 2016. Euro Surveill. 2016;21(45):30391.  https://doi.org/10.2807/1560-7917.ES.2016.21.45.30391  PMID: 27918257 
  5. Störk T, de le Roi M, Haverkamp AK, Jesse ST, Peters M, Fast C, et al. Analysis of avian Usutu virus infections in Germany from 2011 to 2018 with focus on dsRNA detection to demonstrate viral infections. Sci Rep. 2021;11(1):24191.  https://doi.org/10.1038/s41598-021-03638-5  PMID: 34921222 
  6. Bakonyi T, Jungbauer C, Aberle SW, Kolodziejek J, Dimmel K, Stiasny K, et al. Usutu virus infections among blood donors, Austria, July and August 2017 - Raising awareness for diagnostic challenges. Euro Surveill. 2017;22(41):17-00644.  https://doi.org/10.2807/1560-7917.ES.2017.22.41.17-00644  PMID: 29043962 
  7. Percivalle E, Sassera D, Rovida F, Isernia P, Fabbi M, Baldanti F, et al. Usutu virus antibodies in blood donors and healthy forestry workers in the Lombardy region, northern Italy. Vector Borne Zoonotic Dis. 2017;17(9):658-61.  https://doi.org/10.1089/vbz.2017.2126  PMID: 28759350 
  8. Zaaijer HL, Slot E, Molier M, Reusken CBEM, Koppelman MHGM. Usutu virus infection in Dutch blood donors. Transfusion. 2019;59(9):2931-7.  https://doi.org/10.1111/trf.15444  PMID: 31270821 
  9. Faggioni G, De Santis R, Pomponi A, Grottola A, Serpini GF, Meacci M, et al. Prevalence of Usutu and West Nile virus antibodies in human sera, Modena, Italy, 2012. J Med Virol. 2018;90(10):1666-8.  https://doi.org/10.1002/jmv.25230  PMID: 29797606 
  10. Constant O, Gil P, Barthelemy J, Bolloré K, Foulongne V, Desmetz C, et al. One Health surveillance of West Nile and Usutu viruses: a repeated cross-sectional study exploring seroprevalence and endemicity in Southern France, 2016 to 2020. Euro Surveill. 2022;27(25):2200068.  https://doi.org/10.2807/1560-7917.ES.2022.27.25.2200068  PMID: 35748300 
  11. Pecorari M, Longo G, Gennari W, Grottola A, Sabbatini A, Tagliazucchi S, et al. First human case of Usutu virus neuroinvasive infection, Italy, August-September 2009. Euro Surveill. 2009;14(50):19446.  https://doi.org/10.2807/ese.14.50.19446-en  PMID: 20070936 
  12. Cavrini F, Gaibani P, Longo G, Pierro AM, Rossini G, Bonilauri P, et al. Usutu virus infection in a patient who underwent orthotropic liver transplantation, Italy, August-September 2009. Euro Surveill. 2009;14(50):19448.  https://doi.org/10.2807/ese.14.50.19448-en  PMID: 20070935 
  13. Santini M, Vilibic-Cavlek T, Barsic B, Barbic L, Savic V, Stevanovic V, et al. First cases of human Usutu virus neuroinvasive infection in Croatia, August-September 2013: clinical and laboratory features. J Neurovirol. 2015;21(1):92-7.  https://doi.org/10.1007/s13365-014-0300-4  PMID: 25361698 
  14. Simonin Y, Sillam O, Carles MJ, Gutierrez S, Gil P, Constant O, et al. Human Usutu virus infection with atypical neurologic presentation, Montpellier, France, 2016. Emerg Infect Dis. 2018;24(5):875-8.  https://doi.org/10.3201/eid2405.171122  PMID: 29664365 
  15. Pacenti M, Sinigaglia A, Martello T, De Rui ME, Franchin E, Pagni S, et al. Clinical and virological findings in patients with Usutu virus infection, northern Italy, 2018. Euro Surveill. 2019;24(47):1900180.  https://doi.org/10.2807/1560-7917.ES.2019.24.47.1900180  PMID: 31771697 
  16. Vilibic-Cavlek T, Savic V, Sabadi D, Peric L, Barbic L, Klobucar A, 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;66(5):1946-57.  https://doi.org/10.1111/tbed.13225  PMID: 31067011 
  17. Percivalle E, Cassaniti I, Sarasini A, Rovida F, Adzasehoun KMG, Colombini I, et al. West Nile or Usutu virus? A three-year follow-up of humoral and cellular response in a group of asymptomatic blood donors. Viruses. 2020;12(2):157.  https://doi.org/10.3390/v12020157  PMID: 32013152 
  18. Aberle SW, Kolodziejek J, Jungbauer C, Stiasny K, Aberle JH, Zoufaly A, et al. Increase in human West Nile and Usutu virus infections, Austria, 2018. Euro Surveill. 2018;23(43):1800545.  https://doi.org/10.2807/1560-7917.ES.2018.23.43.1800545  PMID: 30376913 
  19. Nagy A, Mezei E, Nagy O, Bakonyi T, Csonka N, Kaposi M, et al. Extraordinary increase in West Nile virus cases and first confirmed human Usutu virus infection in Hungary, 2018. Euro Surveill. 2019;24(28):1900038.  https://doi.org/10.2807/1560-7917.ES.2019.24.28.1900038  PMID: 31311619 
  20. Allering L, Jöst H, Emmerich P, Günther S, Lattwein E, Schmidt M, et al. Detection of Usutu virus infection in a healthy blood donor from south-west Germany, 2012. Euro Surveill. 2012;17(50):20341.  https://doi.org/10.2807/ese.17.50.20341-en  PMID: 23241231 
  21. Bakonyi T, Erdélyi K, Brunthaler R, Dán Á, Weissenböck H, Nowotny N. Usutu virus, Austria and Hungary, 2010-2016. Emerg Microbes Infect. 2017;6(10):e85. PMID: 29018253 
  22. Weidinger P, Kolodziejek J, Bakonyi T, Brunthaler R, Erdélyi K, Weissenböck H, et al. Different dynamics of Usutu virus infections in Austria and Hungary, 2017-2018. Transbound Emerg Dis. 2020;67(1):298-307.  https://doi.org/10.1111/tbed.13351  PMID: 31505099 
  23. Benzarti E, Sarlet M, Franssen M, Cadar D, Schmidt-Chanasit J, Rivas JF, et al. Usutu virus epizootic in Belgium in 2017 and 2018: evidence of virus endemization and ongoing introduction events. Vector Borne Zoonotic Dis. 2020;20(1):43-50.  https://doi.org/10.1089/vbz.2019.2469  PMID: 31479400 
  24. Hönig V, Palus M, Kaspar T, Zemanova M, Majerova K, Hofmannova L, et al. Multiple lineages of Usutu virus (Flaviviridae, Flavivirus) in blackbirds (Turdus merula) and mosquitoes (Culex pipiens, Cx. modestus) in the Czech Republic (2016-2019). Microorganisms. 2019;7(11):568.  https://doi.org/10.3390/microorganisms7110568  PMID: 31744087 
  25. Höfle U, Gamino V, de Mera IG, Mangold AJ, Ortíz JA, de la Fuente J. Usutu virus in migratory song thrushes, Spain. Emerg Infect Dis. 2013;19(7):1173-5.  https://doi.org/10.3201/eid1907.130199  PMID: 23764143 
  26. Guerrero-Carvajal F, Bravo-Barriga D, Martín-Cuervo M, Aguilera-Sepúlveda P, Ferraguti M, Jiménez-Clavero , et al. Serological evidence of co-circulation of West Nile and Usutu viruses in equids from western Spain. Transbound Emerg Dis. 2021;68(3):1432-44.  https://doi.org/10.1111/tbed.13810  PMID: 32853452 
  27. Michel F, Sieg M, Fischer D, Keller M, Eiden M, Reuschel M, et al. Evidence for West Nile virus and Usutu virus infections in wild and resident birds in Germany, 2017 and 2018. Viruses. 2019;11(7):674.  https://doi.org/10.3390/v11070674  PMID: 31340516 
  28. Ziegler U, Bergmann F, Fischer D, Müller K, Holicki CM, Sadeghi B, et al. Spread of West Nile virus and Usutu virus in the German bird population, 2019-2020. Microorganisms. 2022;10(4):807.  https://doi.org/10.3390/microorganisms10040807  PMID: 35456857 
  29. Oude Munnink BB, Münger E, Nieuwenhuijse DF, Kohl R, van der Linden A, Schapendonk CME, et al. Genomic monitoring to understand the emergence and spread of Usutu virus in the Netherlands, 2016-2018. Sci Rep. 2020;10(1):2798.  https://doi.org/10.1038/s41598-020-59692-y  PMID: 32071379 
  30. Cadar D, Lühken R, van der Jeugd H, Garigliany M, Ziegler U, Keller M, et al. Widespread activity of multiple lineages of Usutu virus, western Europe, 2016. Euro Surveill. 2017;22(4):30452.  https://doi.org/10.2807/1560-7917.ES.2017.22.4.30452  PMID: 28181903 
  31. Michel F, Fischer D, Eiden M, Fast C, Reuschel M, Müller K, et al. West Nile virus and Usutu virus monitoring of wild birds in Germany. Int J Environ Res Public Health. 2018;15(1):171.  https://doi.org/10.3390/ijerph15010171  PMID: 29361762 
  32. Llopis IV, Rossi L, Di Gennaro A, Mosca A, Teodori L, Tomassone L, et al. Further circulation of West Nile and Usutu viruses in wild birds in Italy. Infect Genet Evol. 2015;32:292-7.  https://doi.org/10.1016/j.meegid.2015.03.024  PMID: 25818400 
  33. Lauriano A, Rossi A, Galletti G, Casadei G, Santi A, Rubini S, et al. West Nile and Usutu viruses’ surveillance in birds of the province of Ferrara, Italy, from 2015 to 2019. Viruses. 2021;13(7):1367.  https://doi.org/10.3390/v13071367  PMID: 34372573 
  34. Constant O, Bollore K, Clé M, Barthelemy J, Foulongne V, Chenet B, et al. Evidence of exposure to USUV and WNV in zoo animals in France. Pathogens. 2020;9(12):1005.  https://doi.org/10.3390/pathogens9121005  PMID: 33266071 
  35. Kvapil P, Račnik J, Kastelic M, Bártová E, Korva M, Jelovšek M, et al. A sentinel serological study in selected zoo animals to assess early detection of West Nile and Usutu virus circulation in Slovenia. Viruses. 2021;13(4):626.  https://doi.org/10.3390/v13040626  PMID: 33917545 
  36. Cano-Terriza D, Guerra R, Lecollinet S, Cerdà-Cuéllar M, Cabezón O, Almería S, et al. Epidemiological survey of zoonotic pathogens in feral pigeons (Columba livia var. domestica) and sympatric zoo species in Southern Spain. Comp Immunol Microbiol Infect Dis. 2015;43:22-7.  https://doi.org/10.1016/j.cimid.2015.10.003  PMID: 26616657 
  37. Camp JV, Kolodziejek J, Nowotny N. Targeted surveillance reveals native and invasive mosquito species infected with Usutu virus. Parasit Vectors. 2019;12(1):46.  https://doi.org/10.1186/s13071-019-3316-z  PMID: 30665453 
  38. Klobucar A, Savic V, Curman Posavec M, Petrinic S, Kuhar U, Toplak I, et al. Screening of mosquitoes for West Nile virus and Usutu virus in Croatia, 2015-2020. Trop Med Infect Dis. 2021;6(2):45.  https://doi.org/10.3390/tropicalmed6020045  PMID: 33918386 
  39. Čabanová V, Tichá E, Bradbury RS, Zubriková D, Valentová D, Chovancová G, et al. Mosquito surveillance of West Nile and Usutu viruses in four territorial units of Slovakia and description of a confirmed autochthonous human case of West Nile fever, 2018 to 2019. Euro Surveill. 2021;26(19):2000063.  https://doi.org/10.2807/1560-7917.ES.2021.26.19.2000063  PMID: 33988125 
  40. Barzon L, Montarsi F, Quaranta E, Monne I, Pacenti M, Michelutti A, et al. Early start of seasonal transmission and co-circulation of West Nile virus lineage 2 and a newly introduced lineage 1 strain, northern Italy, June 2022. Euro Surveill. 2022;27(29):2200548.  https://doi.org/10.2807/1560-7917.ES.2022.27.29.2200548  PMID: 35866436 
  41. Folly AJ, Lawson B, Lean FZ, McCracken F, Spiro S, John SK, et al. Detection of Usutu virus infection in wild birds in the United Kingdom, 2020. Euro Surveill. 2020;25(41):2001732.  https://doi.org/10.2807/1560-7917.ES.2020.25.41.2001732  PMID: 33063656 
  42. Folly AJ, Sewgobind S, Hernández-Triana LM, Mansfield KL, Lean FZX, Lawson B, et al. Evidence for overwintering and autochthonous transmission of Usutu virus to wild birds following its redetection in the United Kingdom. Transbound Emerg Dis. 2022;69(6):3684-92.  https://doi.org/10.1111/tbed.14738  PMID: 36217722 
  43. Steinmetz HW, Bakonyi T, Weissenböck H, Hatt JM, Eulenberger U, Robert N, et al. Emergence and establishment of Usutu virus infection in wild and captive avian species in and around Zurich, Switzerland--genomic and pathologic comparison to other central European outbreaks. Vet Microbiol. 2011;148(2-4):207-12.  https://doi.org/10.1016/j.vetmic.2010.09.018  PMID: 20980109 
  44. Kemenesi G, Buzás D, Zana B, Kurucz K, Krtinic B, Kepner A, et al. First genetic characterization of Usutu virus from Culex pipiens mosquitoes Serbia, 2014. Infect Genet Evol. 2018;63:58-61.  https://doi.org/10.1016/j.meegid.2018.05.012  PMID: 29778766 
  45. Capobianchi MR, Sambri V, Castilletti C, Pierro AM, Rossini G, Gaibani P, et al. Retrospective screening of solid organ donors in Italy, 2009, reveals unpredicted circulation of West Nile virus. Euro Surveill. 2010;15(34):19648.  https://doi.org/10.2807/ese.15.34.19648-en  PMID: 20807488 
  46. Costa AN, Capobianchi MR, Ippolito G, Palù G, Barzon L, Piccolo G, et al. West Nile virus: the Italian national transplant network reaction to an alert in the north-eastern region, Italy 2011. Euro Surveill. 2011;16(41):19991. PMID: 22008198 
  47. Benzarti E, Sarlet M, Franssen M, Desmecht D, Schmidt-Chanasit J, Garigliany MM. New insights into the susceptibility of immunocompetent mice to Usutu Virus. Viruses. 2020;12(2):189.  https://doi.org/10.3390/v12020189  PMID: 32046265 
  48. Clé M, Barthelemy J, Desmetz C, Foulongne V, Lapeyre L, Bolloré K, et al. Study of Usutu virus neuropathogenicity in mice and human cellular models. PLoS Negl Trop Dis. 2020;14(4):e0008223.  https://doi.org/10.1371/journal.pntd.0008223  PMID: 32324736 
  49. Riccetti S, Sinigaglia A, Desole G, Nowotny N, Trevisan M, Barzon L. Modelling West Nile virus and Usutu virus pathogenicity in human neural stem cells. Viruses. 2020;12(8):882.  https://doi.org/10.3390/v12080882  PMID: 32806715 
  50. Blázquez A-B, Escribano-Romero E, Martín-Acebes MA, Petrovic T, Saiz J-C. Limited susceptibility of mice to Usutu virus (USUV) infection and induction of flavivirus cross-protective immunity. Virology. 2015;482:67-71.  https://doi.org/10.1016/j.virol.2015.03.020  PMID: 25827530 
  51. Kuchinsky SC, Hawks SA, Mossel EC, Coutermarsh-Ott S, Duggal NK. Differential pathogenesis of Usutu virus isolates in mice. PLoS Negl Trop Dis. 2020;14(10):e0008765.  https://doi.org/10.1371/journal.pntd.0008765  PMID: 33044987 
  52. Escribano-Romero E, Jiménez de Oya N, Camacho MC, Blázquez AB, Martín-Acebes MA, Risalde MA, et al. Previous Usutu virus exposure partially protects magpies (Pica pica) against West Nile virus disease but does not prevent horizontal transmission. Viruses. 2021;13(7):1409.  https://doi.org/10.3390/v13071409  PMID: 34372622 
  53. Reemtsma H, Holicki CM, Fast C, Bergmann F, Groschup MH, Ziegler U. A prior Usutu virus infection can protect geese from severe West Nile disease. Pathogens. 2023;12(7):959.  https://doi.org/10.3390/pathogens12070959 
  54. Santos PD, Michel F, Wylezich C, Höper D, Keller M, Holicki CM, et al. Co-infections: Simultaneous detections of West Nile virus and Usutu virus in birds from Germany. Transbound Emerg Dis. 2022;69(2):776-92.  https://doi.org/10.1111/tbed.14050  PMID: 33655706 
  55. Wang H, Abbo SR, Visser TM, Westenberg M, Geertsema C, Fros JJ, et al. Competition between Usutu virus and West Nile virus during simultaneous and sequential infection of Culex pipiens mosquitoes. Emerg Microbes Infect. 2020;9(1):2642-52.  https://doi.org/10.1080/22221751.2020.1854623  PMID: 33215969 
  56. Salgado R, Hawks SA, Frere F, Vázquez A, Huang CY, Duggal NK. West Nile virus vaccination protects against Usutu virus disease in mice. Viruses. 2021;13(12):2352.  https://doi.org/10.3390/v13122352  PMID: 34960621 
  57. Holicki CM, Scheuch DE, Ziegler U, Lettow J, Kampen H, Werner D, et al. German Culex pipiens biotype molestus and Culex torrentium are vector-competent for Usutu virus. Parasit Vectors. 2020;13(1):625.  https://doi.org/10.1186/s13071-020-04532-1  PMID: 33380339 
  58. Puggioli A, Bonilauri P, Calzolari M, Lelli D, Carrieri M, Urbanelli S, et al. Does Aedes albopictus (Diptera: Culicidae) play any role in Usutu virus transmission in Northern Italy? Experimental oral infection and field evidences. Acta Trop. 2017;172:192-6.  https://doi.org/10.1016/j.actatropica.2017.05.006  PMID: 28495404 
  59. Abbo SR, Visser TM, Wang H, Göertz GP, Fros JJ, Abma-Henkens MHC, et al. The invasive Asian bush mosquito Aedes japonicus found in the Netherlands can experimentally transmit Zika virus and Usutu virus. PLoS Negl Trop Dis. 2020;14(4):e0008217.  https://doi.org/10.1371/journal.pntd.0008217  PMID: 32282830 
/content/10.2807/1560-7917.ES.2023.28.33.2200929
Loading

Data & Media loading...

Supplementary data

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error