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Abstract

Background

West Nile virus (WNV), found in Berlin in birds since 2018 and humans since 2019, is a mosquito-borne virus that can manifest in humans as West Nile fever (WNF) or neuroinvasive disease (WNND). However, human WNV infections and associated disease are likely underdiagnosed.

Aim

We aimed to identify and genetically characterise WNV infections in humans and mosquitoes in Berlin.

Methods

We investigated acute WNV infection cases reported to the State Office for Health and Social Affairs Berlin in 2021 and analysed cerebrospinal fluid (CSF) samples from patients with encephalitis of unknown aetiology (n = 489) for the presence of WNV. Mosquitoes were trapped at identified potential exposure sites of cases and examined for WNV infection.

Results

West Nile virus was isolated and sequenced from a blood donor with WNF, a symptomatic patient with WNND and a WNND case retrospectively identified from testing CSF. All cases occurred in 2021 and had no history of travel 14 days prior to symptom onset (incubation period of the disease). We detected WNV in mosquitoes sampled at the exposure site of one case in 2021, and in 2022. Genome analyses revealed a monophyletic Berlin-specific virus clade in which two enzootic mosquito-associated variants can be delineated based on tree topology and presence of single nucleotide variants. Both variants have highly identical counterparts in human cases indicating local acquisition of infection.

Conclusion

Our study provides evidence that autochthonous WNV lineage 2 infections occurred in Berlin and the virus has established an endemic maintenance cycle.

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/content/10.2807/1560-7917.ES.2023.28.48.2300258
2023-11-30
2024-12-22
/content/10.2807/1560-7917.ES.2023.28.48.2300258
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References

  1. Ciota AT. West Nile virus and its vectors. Curr Opin Insect Sci. 2017;22:28-36.  https://doi.org/10.1016/j.cois.2017.05.002  PMID: 28805636 
  2. Hurlbut HS, Rizk F, Taylor RM, Work TH. A study of the ecology of West Nile virus in Egypt. Am J Trop Med Hyg. 1956;5(4):579-620.  https://doi.org/10.4269/ajtmh.1956.5.579  PMID: 13354882 
  3. Petersen LR, Brault AC, Nasci RS. West Nile virus: review of the literature. JAMA. 2013;310(3):308-15.  https://doi.org/10.1001/jama.2013.8042  PMID: 23860989 
  4. Zou S, Foster GA, Dodd RY, Petersen LR, Stramer SL. West Nile fever characteristics among viremic persons identified through blood donor screening. J Infect Dis. 2010;202(9):1354-61.  https://doi.org/10.1086/656602  PMID: 20874087 
  5. Yeung MW, Shing E, Nelder M, Sander B. Epidemiologic and clinical parameters of West Nile virus infections in humans: a scoping review. BMC Infect Dis. 2017;17(1):609.  https://doi.org/10.1186/s12879-017-2637-9  PMID: 28877682 
  6. Harrington T, Kuehnert MJ, Kamel H, Lanciotti RS, Hand S, Currier M, et al. West Nile virus infection transmitted by blood transfusion. Transfusion. 2003;43(8):1018-22.  https://doi.org/10.1046/j.1537-2995.2003.00481.x  PMID: 12869105 
  7. Smithburn KC, Hughes TP, Burke AW, Hall JH. A neurotropic virus isolated from the blood of a native of Uganda. Am J Trop Med Hyg. 1940;20(4):471-2.  https://doi.org/10.4269/ajtmh.1940.s1-20.471 
  8. May FJ, Davis CT, Tesh RB, Barrett AD. Phylogeography of West Nile virus: from the cradle of evolution in Africa to Eurasia, Australia, and the Americas. J Virol. 2011;85(6):2964-74.  https://doi.org/10.1128/JVI.01963-10  PMID: 21159871 
  9. Hernández-Triana LM, Jeffries CL, Mansfield KL, Carnell G, Fooks AR, Johnson N. Emergence of west nile virus lineage 2 in europe: a review on the introduction and spread of a mosquito-borne disease. Front Public Health. 2014;2:271.  https://doi.org/10.3389/fpubh.2014.00271  PMID: 25538937 
  10. Chaintoutis SC, Papa A, Pervanidou D, Dovas CI. Evolutionary dynamics of lineage 2 West Nile virus in Europe, 2004-2018: Phylogeny, selection pressure and phylogeography. Mol Phylogenet Evol. 2019;141:106617.  https://doi.org/10.1016/j.ympev.2019.106617  PMID: 31521822 
  11. Camp JV, Nowotny N. The knowns and unknowns of West Nile virus in Europe: what did we learn from the 2018 outbreak? Expert Rev Anti Infect Ther. 2020;18(2):145-54.  https://doi.org/10.1080/14787210.2020.1713751  PMID: 31914833 
  12. Ziegler U, Lühken R, Keller M, Cadar D, van der Grinten E, Michel F, et al. West Nile virus epizootic in Germany, 2018. Antiviral Res. 2019;162:39-43.  https://doi.org/10.1016/j.antiviral.2018.12.005  PMID: 30550796 
  13. Ziegler U, Santos PD, Groschup MH, Hattendorf C, Eiden M, Höper D, et al. West Nile Virus Epidemic in Germany Triggered by Epizootic Emergence, 2019. Viruses. 2020;12(4):448.  https://doi.org/10.3390/v12040448  PMID: 32326472 
  14. Pietsch C, Michalski D, Münch J, Petros S, Bergs S, Trawinski H, et al. Autochthonous West Nile virus infection outbreak in humans, Leipzig, Germany, August to September 2020. Euro Surveill. 2020;25(46):2001786.  https://doi.org/10.2807/1560-7917.ES.2020.25.46.2001786  PMID: 33213686 
  15. Schneider J, Bachmann F, Choi M, Kurvits L, Schmidt ML, Bergfeld L, et al. Autochthonous West Nile virus infection in Germany: Increasing numbers and a rare encephalitis case in a kidney transplant recipient. Transbound Emerg Dis. 2021. PMID: 34850584 
  16. Kampen H, Holicki CM, Ziegler U, Groschup MH, Tews BA, Werner D. West Nile Virus Mosquito Vectors (Diptera: Culicidae) in Germany. Viruses. 2020;12(5):493.  https://doi.org/10.3390/v12050493  PMID: 32354202 
  17. Fynmore N, Lühken R, Maisch H, Risch T, Merz S, Kliemke K, et al. Rapid assessment of West Nile virus circulation in a German zoo based on honey-baited FTA cards in combination with box gravid traps. Parasit Vectors. 2021;14(1):449.  https://doi.org/10.1186/s13071-021-04951-8  PMID: 34488835 
  18. Engler O, Savini G, Papa A, Figuerola J, Groschup MH, Kampen H, et al. European surveillance for West Nile virus in mosquito populations. Int J Environ Res Public Health. 2013;10(10):4869-95.  https://doi.org/10.3390/ijerph10104869  PMID: 24157510 
  19. 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 
  20. Santos PD, Günther A, Keller M, Homeier-Bachmann T, Groschup MH, Beer M, et al. An advanced sequence clustering and designation workflow reveals the enzootic maintenance of a dominant West Nile virus subclade in Germany. Virus Evol. 2023;9(1):vead013.  https://doi.org/10.1093/ve/vead013  PMID: 37197362 
  21. Robert Koch Institute. Falldefinitionen des RKI 2019. Case definitions of the RKI 2019. Berlin: Robert Kock Institute; 2019. German. Available from: https://www.rki.de/DE/Content/Infekt/IfSG/Falldefinition/Downloads/Falldefinitionen_des_RKI_2019.pdf?__blob=publicationFile
  22. Frank C, Schmidt-Chanasit J, Ziegler U, Lachmann R, Preußel K, Offergeld R. West Nile Virus in Germany: An Emerging Infection and Its Relevance for Transfusion Safety. Transfus Med Hemother. 2022;49(4):192-204.  https://doi.org/10.1159/000525167  PMID: 36159956 
  23. Eiden M, Vina-Rodriguez A, Hoffmann B, Ziegler U, Groschup MH. Two new real-time quantitative reverse transcription polymerase chain reaction assays with unique target sites for the specific and sensitive detection of lineages 1 and 2 West Nile virus strains. J Vet Diagn Invest. 2010;22(5):748-53.  https://doi.org/10.1177/104063871002200515  PMID: 20807934 
  24. Becker N, Petric D, Zgomba M, Boase C, Madon M, Dahl C, et al. Mosquitoes and their control. 2nd ed. Heidelberg: Springer; 2010.
  25. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol. 1994;3(5):294-9. PMID: 7881515 
  26. Guggemos HD, Fendt M, Hieke C, Heyde V, Mfune JKE, Borgemeister C, et al. Simultaneous circulation of two West Nile virus lineage 2 clades and Bagaza virus in the Zambezi region, Namibia. PLoS Negl Trop Dis. 2021;15(4):e0009311.  https://doi.org/10.1371/journal.pntd.0009311  PMID: 33798192 
  27. Reed LJ, Muench H. A simple method of estimating fifty percent endpoints. Am J Hyg. 1938.
  28. Schilling-Loeffler K, Viera-Segura O, Corman VM, Schneider J, Gadicherla AK, Schotte U, et al. Cell Culture Isolation and Whole Genome Characterization of Hepatitis E Virus Strains from Wild Boars in Germany. Microorganisms. 2021;9(11):2302.  https://doi.org/10.3390/microorganisms9112302  PMID: 34835427 
  29. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772-80. . Available from: MAFFT multiple sequence alignment software version 7: improvements in performance and usability. https://doi.org/10.1093/molbev/mst010  PMID: 23329690 
  30. Kampen H, Tews BA, Werner D. First Evidence of West Nile Virus Overwintering in Mosquitoes in Germany. Viruses. 2021;13(12):2463.  https://doi.org/10.3390/v13122463  PMID: 34960732 
  31. Robert Koch Institute (RKI). Survstat. Berlin: Survstat. [Accessed: 12 Apr 2023]. Available from: https://survstat.rki.de/
  32. Vlaskamp DR, Thijsen SF, Reimerink J, Hilkens P, Bouvy WH, Bantjes SE, et al. First autochthonous human West Nile virus infections in the Netherlands, July to August 2020. Euro Surveill. 2020;25(46):2001904.  https://doi.org/10.2807/1560-7917.ES.2020.25.46.2001904  PMID: 33213687 
  33. Holicki CM, Ziegler U, Răileanu C, Kampen H, Werner D, Schulz J, et al. West Nile Virus Lineage 2 Vector Competence of Indigenous Culex and Aedes Mosquitoes from Germany at Temperate Climate Conditions. Viruses. 2020;12(5):561.  https://doi.org/10.3390/v12050561  PMID: 32438619 
  34. Fay RL, Keyel AC, Ciota AT. West Nile virus and climate change. Adv Virus Res. 2022;114:147-93.  https://doi.org/10.1016/bs.aivir.2022.08.002 
  35. Kilpatrick AM, Meola MA, Moudy RM, Kramer LD. Temperature, viral genetics, and the transmission of West Nile virus by Culex pipiens mosquitoes. PLoS Pathog. 2008;4(6):e1000092.  https://doi.org/10.1371/journal.ppat.1000092  PMID: 18584026 
  36. Ruiz MO, Chaves LF, Hamer GL, Sun T, Brown WM, Walker ED, et al. Local impact of temperature and precipitation on West Nile virus infection in Culex species mosquitoes in northeast Illinois, USA. Parasit Vectors. 2010;3(1):19.  https://doi.org/10.1186/1756-3305-3-19  PMID: 20302617 
  37. Aharonson-Raz K, Lichter-Peled A, Tal S, Gelman B, Cohen D, Klement E, et al. Spatial and temporal distribution of West Nile virus in horses in Israel (1997-2013)--from endemic to epidemics. PLoS One. 2014;9(11):e113149.  https://doi.org/10.1371/journal.pone.0113149  PMID: 25402217 
  38. García San Miguel Rodríguez-Alarcón L, Fernández-Martínez B, Sierra Moros MJ, Vázquez A, Julián Pachés P, García Villacieros E, et al. Unprecedented increase of West Nile virus neuroinvasive disease, Spain, summer 2020. Euro Surveill. 2021;26(19):2002010.  https://doi.org/10.2807/1560-7917.ES.2021.26.19.2002010  PMID: 33988123 
  39. Riccardo F, Bella A, Monaco F, Ferraro F, Petrone D, Mateo-Urdiales A, et al. Rapid increase in neuroinvasive West Nile virus infections in humans, Italy, July 2022. Euro Surveill. 2022;27(36):2200653.  https://doi.org/10.2807/1560-7917.ES.2022.27.36.2200653  PMID: 36082685 
  40. Hayes EB, Komar N, Nasci RS, Montgomery SP, O’Leary DR, Campbell GL. Epidemiology and transmission dynamics of West Nile virus disease. Emerg Infect Dis. 2005;11(8):1167-73.  https://doi.org/10.3201/eid1108.050289a  PMID: 16102302 
  41. Heym EC, Kampen H, Krone O, Schäfer M, Werner D. Molecular detection of vector-borne pathogens from mosquitoes collected in two zoological gardens in Germany. Parasitol Res. 2019;118(7):2097-105.  https://doi.org/10.1007/s00436-019-06327-5  PMID: 31154526 
  42. TierSeuchenInformationsSystem (TSIS). Animal disease query. [Accessed: 1 Apr 2022]. German. Available from: https://tsis.fli.de/Reports/Info_SO.aspx?ts=416&guid=dfaef4b7-5934-412f-901b-5a9ddeaa9b32
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