Genomic monitoring to understand the emergence and spread of Usutu virus in the Netherlands, 2016-2018.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
18 02 2020
Historique:
received: 15 10 2019
accepted: 31 01 2020
entrez: 20 2 2020
pubmed: 20 2 2020
medline: 20 11 2020
Statut: epublish

Résumé

Usutu virus (USUV) is a mosquito-borne flavivirus circulating in Western Europe that causes die-offs of mainly common blackbirds (Turdus merula). In the Netherlands, USUV was first detected in 2016, when it was identified as the likely cause of an outbreak in birds. In this study, dead blackbirds were collected, screened for the presence of USUV and submitted to Nanopore-based sequencing. Genomic sequences of 112 USUV were obtained and phylogenetic analysis showed that most viruses identified belonged to the USUV Africa 3 lineage, and molecular clock analysis evaluated their most recent common ancestor to 10 to 4 years before first detection of USUV in the Netherlands. USUV Europe 3 lineage, commonly found in Germany, was less frequently detected. This analyses further suggest some extent of circulation of USUV between the Netherlands, Germany and Belgium, as well as likely overwintering of USUV in the Netherlands.

Identifiants

pubmed: 32071379
doi: 10.1038/s41598-020-59692-y
pii: 10.1038/s41598-020-59692-y
pmc: PMC7029044
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2798

Références

Pauli, G. et al. Usutu virus. Transfus. Med. Hemother. 41, 73–82 (2014).
pubmed: 24659950 pmcid: 24659950
Camp, J. V., Kolodziejek, J. & Nowotny, N. Targeted surveillance reveals native and invasive mosquito species infected with Usutu virus. Parasit. Vectors 12, 46 (2019).
pubmed: 30665453 pmcid: 6341546 doi: 10.1186/s13071-019-3316-z
Fros, J. J. et al. Comparative Usutu and West Nile virus transmission potential by local Culex pipiens mosquitoes in north-western Europe. One Heal. 1, 31–36 (2015).
doi: 10.1016/j.onehlt.2015.08.002
Cadar, D. et al. Usutu virus in bats, Germany, 2013. Emerg. Infect. Dis. 20, 1771–3 (2014).
pubmed: 25271769 pmcid: 4193186 doi: 10.3201/eid2010.140909
Diagne, M. et al. Usutu Virus Isolated from Rodents in Senegal. Viruses 11, 181 (2019).
pmcid: 6409855 doi: 10.3390/v11020181
Williams, M. C., Simpson, D. I. H., Haddow, A. J. & Knight, E. M. The Isolation of West Nile Virus from Man and of Usutu Virus from the Bird-Biting Mosquito Mansonia Aurites (Theobald) in the Entebbe Area of Uganda. Ann. Trop. Med. Parasitol. 58, 367–374 (1964).
pubmed: 14212897 doi: 10.1080/00034983.1964.11686258 pmcid: 14212897
Nikolay, B., Diallo, M., Boye, C. S. B. & Sall, A. A. Usutu Virus in Africa. Vector-Borne Zoonotic Dis. 11, 1417–1423 (2011).
pubmed: 21767160 doi: 10.1089/vbz.2011.0631 pmcid: 21767160
Weissenböck, H. et al. Emergence of Usutu virus, an African Mosquito-Borne Flavivirus of the Japanese Encephalitis Virus Group, Central Europe. Emerg. Infect. Dis. 8, 652–656 (2002).
pubmed: 12095429 pmcid: 2730324 doi: 10.3201/eid0807.020094
Weissenböck, H., Bakonyi, T., Rossi, G., Mani, P. & Nowotny, N. Usutu Virus, Italy, 1996. Emerg. Infect. Dis. 19, 274–277 (2013).
pubmed: 23347844 pmcid: 3559058 doi: 10.3201/eid1902.121191
Cheng, Y. et al. Evaluating the risk for Usutu virus circulation in Europe: comparison of environmental niche models and epidemiological models. Int J Heal. Geogr 17, 35 (2018).
doi: 10.1186/s12942-018-0155-7
Lühken, R. et al. Distribution of Usutu Virus in Germany and Its Effect on Breeding Bird Populations. Emerg. Infect. Dis. 23, 1994–2001 (2017).
pubmed: 29148399 pmcid: 5708248 doi: 10.3201/eid2312.171257
Pierro, A. et al. Detection of specific antibodies against West Nile and Usutu viruses in healthy blood donors in northern Italy, 2010–2011. Clin. Microbiol. Infect. 19, E451–E453 (2013).
pubmed: 23663225 doi: 10.1111/1469-0691.12241 pmcid: 23663225
Cadar, D. et al. Blood donor screening for West Nile virus (WNV) revealed acute Usutu virus (USUV) infection, Germany, September 2016. Eurosurveillance 22, 30501 (2017).
pubmed: 28422005 pmcid: 5388121 doi: 10.2807/1560-7917.ES.2017.22.14.30501
Bakonyi, T. et al. Usutu virus infections among blood donors, Austria, July and August 2017 – Raising awareness for diagnostic challenges. Eurosurveillance 22, (2017).
Zaaijer, H. L., Slot, E., Molier, M., Reusken, C. B. E. M. & Koppelman, M. H. G. M. Usutu virus infection in Dutch blood donors. Transfusion trf.15444. https://doi.org/10.1111/trf.15444 (2019).
pubmed: 31270821 doi: 10.1111/trf.15444 pmcid: 31270821
Pecorari, M. et al. First human case of Usutu virus neuroinvasive infection, Italy, August-September 2009. Euro Surveill. 14, (2009).
Cavrini, F. et al. Usutu virus infection in a patient who underwent orthotropic liver transplantation, Italy, August-September 2009. Euro Surveill. 14, (2009).
Cavrini, F. et al. A rapid and specific real-time RT-PCR assay to identify Usutu virus in human plasma, serum, and cerebrospinal fluid. J. Clin. Virol. 50, 221–223 (2011).
pubmed: 21156352 doi: 10.1016/j.jcv.2010.11.008
Grottola, A. et al. Usutu virus infections in humans: a retrospective analysis in the municipality of Modena, Italy. Clin. Microbiol. Infect. 23, 33–37 (2017).
pubmed: 27677699 doi: 10.1016/j.cmi.2016.09.019
Simonin, Y. et al. Human Usutu Virus Infection with Atypical Neurologic Presentation, Montpellier, France, 2016. Emerg. Infect. Dis. 24, 875–878 (2018).
pubmed: 29664365 pmcid: 5938765 doi: 10.3201/eid2405.171122
Santini, M. et al. First cases of human Usutu virus neuroinvasive infection in Croatia, August–September 2013: clinical and laboratory features. J. Neurovirol. 21, 92–97 (2015).
pubmed: 25361698 doi: 10.1007/s13365-014-0300-4 pmcid: 25361698
Zaaijer, H. L., Slot, E., Molier, M., Reusken, C. B. E. M. & Koppelman, M. H. G. M. Usutu virus infection in Dutch blood donors. Transfusion trf.15444. https://doi.org/10.1111/trf.15444 (2019).
pubmed: 31270821 doi: 10.1111/trf.15444 pmcid: 31270821
Aberle, S. W. et al. Increase in human West Nile and Usutu virus infections, Austria, 2018. Eurosurveillance 23, 1800545 (2018).
pmcid: 6208007 doi: 10.2807/1560-7917.ES.2018.23.43.1800545
Calzolari, M. et al. Co-circulation of two Usutu virus strains in Northern Italy between 2009 and 2014. Infect. Genet. Evol. 51, 255–262 (2017).
pubmed: 28341546 doi: 10.1016/j.meegid.2017.03.022 pmcid: 28341546
Sieg, M. et al. Outbreak and Cocirculation of Three Different Usutu Virus Strains in Eastern Germany. https://doi.org/10.1089/vbz.2016.2096 .
pubmed: 28816628 doi: 10.1089/vbz.2016.2096 pmcid: 28816628
Michel, F. et al. Evidence for West Nile Virus and Usutu Virus Infections in Wild and Resident Birds in Germany, 2017 and 2018. Viruses 11, 674 (2019).
pmcid: 6669720 doi: 10.3390/v11070674
Eiden, M. et al. Emergence of two Usutu virus lineages in Culex pipiens mosquitoes in the Camargue, France, 2015. Infect. Genet. Evol. 61, 151–154 (2018).
pubmed: 29592838 doi: 10.1016/j.meegid.2018.03.020 pmcid: 29592838
Cadar, D. et al. Widespread activity of multiple lineages of Usutu virus, Western Europe, 2016. Eurosurveillance 22, (2017).
Engel, D. et al. Reconstruction of the Evolutionary History and Dispersal of Usutu Virus, a Neglected Emerging Arbovirus in Europe and Africa. MBio 7, e01938–15 (2016).
pubmed: 26838717 pmcid: 4742707
Rijks, J. M. et al. Widespread Usutu virus outbreak in birds in The Netherlands, 2016. Eurosurveillance 21, (2016).
Faria, N. R. et al. Zika virus in the Americas: Early epidemiological and genetic findings. Science 352, 345–349 (2016).
pubmed: 27013429 pmcid: 4918795 doi: 10.1126/science.aaf5036
Hill, S. C. et al. Early Genomic Detection of Cosmopolitan Genotype of Dengue Virus Serotype 2, Angola, 2018. Emerg. Infect. Dis. 25, 784–787 (2019).
pubmed: 30882320 pmcid: 6433006 doi: 10.3201/eid2504.180958
Faria, N. R. et al. Genomic and epidemiological monitoring of yellow fever virus transmission potential. Science (80-.). 361, 894–899 (2018).
pmcid: 6874500 doi: 10.1126/science.aat7115
Naveca, F. G. et al. Genomic, epidemiological and digital surveillance of Chikungunya virus in the Brazilian Amazon. PLoS Negl. Trop. Dis. 13, e0007065 (2019).
pubmed: 30845267 pmcid: 6424459 doi: 10.1371/journal.pntd.0007065
Faria, N. R. et al. Establishment and cryptic transmission of Zika virus in Brazil and the Americas. Nature 546, 406–410 (2017).
pubmed: 28538727 pmcid: 5722632 doi: 10.1038/nature22401
Oude Munnink, B. B. et al. Towards high quality real-time whole genome sequencing during outbreaks using Usutu virus as example. Infect. Genet. Evol. 73, 49–54 (2019).
pubmed: 31014969 doi: 10.1016/j.meegid.2019.04.015 pmcid: 31014969
Han, A. X., Parker, E., Scholer, F., Maurer-Stroh, S. & Russell, C. A. Phylogenetic Clustering by Linear Integer Programming (PhyCLIP). bio Rxiv 446716. https://doi.org/10.1101/446716 (2019).
Reusken, C. et al. No proof for usutuvirus as cause of death in songbirds in the Netherlands (fall 2012). Tijdschr. Diergeneeskd. 139, 28–30 (2014).
pubmed: 24701786 pmcid: 24701786
Lim, S. M. et al. Serologic evidence of West Nile virus and Usutu virus infections in Eurasian coots in the Netherlands. Zoonoses Public Health 65, 96–102 (2018).
pubmed: 28688117 doi: 10.1111/zph.12375 pmcid: 28688117
Mühlemann, B. et al. Ancient hepatitis B viruses from the Bronze Age to the Medieval period. Nature 557, 418–423 (2018).
pubmed: 29743673 doi: 10.1038/s41586-018-0097-z pmcid: 29743673
Mannasse, B. et al. Usutu Virus RNA in Mosquitoes, Israel, 2014–2015. Emerg. Infect. Dis. 23, 1699–1702 (2017).
pubmed: 28930008 pmcid: 5621534 doi: 10.3201/eid2310.171017
Nikolay, B. A review of West Nile and Usutu virus co-circulation in Europe: how much do transmission cycles overlap? https://doi.org/10.1093/trstmh/trv066 .
pubmed: 26286946 doi: 10.1093/trstmh/trv066 pmcid: 26286946
OIE. OIE-West Nile Fever. Available at: http://www.oie.int/wahis_2/public/wahid.php/Reviewreport/Review?page_refer=MapFullEventReport&reportid=27744 . (Accessed: 13th November 2018) (2018).
Nikolay, B. et al. Development of a Usutu virus specific real-time reverse transcription PCR assay based on sequenced strains from Africa and Europe. J. Virol. Methods 197, 51–54 (2014).
pubmed: 24036076 doi: 10.1016/j.jviromet.2013.08.039 pmcid: 24036076
Jöst, H. et al. Isolation of usutu virus in Germany. Am. J. Trop. Med. Hyg. 85, 551–3 (2011).
pubmed: 21896821 pmcid: 3163883 doi: 10.4269/ajtmh.2011.11-0248
Watson, S. J. et al. Viral population analysis and minority-variant detection using short read next-generation sequencing. Philos Trans. R. Soc L. B. Biol. Sci. 368, 20120205 (2013).
doi: 10.1098/rstb.2012.0205
Kearse, M. et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649 (2012).
pubmed: 22543367 pmcid: 3371832 doi: 10.1093/bioinformatics/bts199
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).
pubmed: 2231712 pmcid: 2231712 doi: 10.1016/S0022-2836(05)80360-2
Benson, D. A., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J. & Sayers, E. W. GenBank. Nucleic Acids Res. 38, D46–51 (2010).
pubmed: 19910366 doi: 10.1093/nar/gkp1024 pmcid: 19910366
Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).
pubmed: 15034147 pmcid: 390337 doi: 10.1093/nar/gkh340
Nguyen, L. T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol 32, 268–274 (2015).
pubmed: 25371430 doi: 10.1093/molbev/msu300 pmcid: 25371430
Gill, M. S. et al. Improving Bayesian population dynamics inference: a coalescent-based model for multiple loci. Mol. Biol. Evol. 30, 713–24 (2013).
pubmed: 23180580 doi: 10.1093/molbev/mss265 pmcid: 23180580
Rambaut, A. FigTree. Available at: http://tree.bio.ed.ac.uk/software/figtree/ (2016).

Auteurs

B Bas Oude Munnink (BB)

ErasmusMC, Department of Viroscience, WHO collaborating centre for arbovirus and viral hemorrhagic fever Reference and Research, Rotterdam, the Netherlands. b.oudemunnink@erasmusmc.nl.

E Münger (E)

ErasmusMC, Department of Viroscience, WHO collaborating centre for arbovirus and viral hemorrhagic fever Reference and Research, Rotterdam, the Netherlands.

D F Nieuwenhuijse (DF)

ErasmusMC, Department of Viroscience, WHO collaborating centre for arbovirus and viral hemorrhagic fever Reference and Research, Rotterdam, the Netherlands.

R Kohl (R)

ErasmusMC, Department of Viroscience, WHO collaborating centre for arbovirus and viral hemorrhagic fever Reference and Research, Rotterdam, the Netherlands.

A van der Linden (A)

ErasmusMC, Department of Viroscience, WHO collaborating centre for arbovirus and viral hemorrhagic fever Reference and Research, Rotterdam, the Netherlands.

C M E Schapendonk (CME)

ErasmusMC, Department of Viroscience, WHO collaborating centre for arbovirus and viral hemorrhagic fever Reference and Research, Rotterdam, the Netherlands.

H van der Jeugd (H)

Vogeltrekstation - Dutch Centre for Avian Migration and Demography, NIOO-KNAW, Wageningen, the Netherlands.

M Kik (M)

Dutch Wildlife Health Centre, University of Utrecht, Utrecht, the Netherlands.
Department of Pathobiology, Pathology, Faculty of Veterinary Medicine, Utrecht University, Utrecht, the Netherlands.

J M Rijks (JM)

Dutch Wildlife Health Centre, University of Utrecht, Utrecht, the Netherlands.

C B E M Reusken (CBEM)

ErasmusMC, Department of Viroscience, WHO collaborating centre for arbovirus and viral hemorrhagic fever Reference and Research, Rotterdam, the Netherlands.
Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, the Netherlands.

M Koopmans (M)

ErasmusMC, Department of Viroscience, WHO collaborating centre for arbovirus and viral hemorrhagic fever Reference and Research, Rotterdam, the Netherlands.

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