Ixodes ricinus as potential vector for Usutu virus

Usutu virus (USUV) is an emerging flavivirus that is maintained in an enzootic cycle with mosquitoes as vectors and birds as amplifying hosts. In Europe, the virus has caused mass mortality of wild birds, mainly among Common Blackbird ( Turdus merula ) populations. While mosquitoes are the primary v...

Full description

Saved in:
Bibliographic Details
Published inPLoS neglected tropical diseases Vol. 18; no. 7; p. e0012172
Main Authors Bakker, Julian W., Münger, Emmanuelle, Esser, Helen J., Sikkema, Reina S., de Boer, Willem F., Sprong, Hein, Reusken, Chantal B. E. M., de Vries, Ankje, Kohl, Robert, van der Linden, Anne, Stroo, Arjan, van der Jeugd, Henk, Pijlman, Gorben P., Koopmans, Marion P. G., Munnink, Bas B. Oude, Koenraadt, Constantianus J. M.
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 10.07.2024
Public Library of Science (PLoS)
Subjects
Animals
Arachnid Vectors - physiology
Arachnid Vectors - virology
Biology and Life Sciences
Bird Diseases - transmission
Bird Diseases - virology
Birds - virology
Disease transmission
Entomology
Female
Flavivirus - genetics
Flavivirus - physiology
Flavivirus Infections - transmission
Flavivirus Infections - veterinary
Flavivirus Infections - virology
Insects as carriers of disease
Ixodes - physiology
Ixodes - virology
Medicine and Health Sciences
Netherlands
Nymph - virology
Netherlands
Online AccessGet full text

Cover

Abstract Usutu virus (USUV) is an emerging flavivirus that is maintained in an enzootic cycle with mosquitoes as vectors and birds as amplifying hosts. In Europe, the virus has caused mass mortality of wild birds, mainly among Common Blackbird ( Turdus merula ) populations. While mosquitoes are the primary vectors for USUV, Common Blackbirds and other avian species are exposed to other arthropod ectoparasites, such as ticks. It is unknown, however, if ticks can maintain and transmit USUV. We addressed this question using in vitro and in vivo experiments and field collected data. USUV replicated in IRE/CTVM19 Ixodes ricinus tick cells and in injected ticks. Moreover, I . ricinus nymphs acquired the virus via artificial membrane blood-feeding and maintained the virus for at least 70 days. Transstadial transmission of USUV from nymphs to adults was confirmed in 4.9% of the ticks. USUV disseminated from the midgut to the haemocoel, and was transmitted via the saliva of the tick during artificial membrane blood-feeding. We further explored the role of ticks by monitoring USUV in questing ticks and in ticks feeding on wild birds in the Netherlands between 2016 and 2019. In total, 622 wild birds and the Ixodes ticks they carried were tested for USUV RNA. Of these birds, 48 (7.7%) carried USUV-positive ticks. The presence of negative-sense USUV RNA in ticks, as confirmed via small RNA-sequencing, showed active virus replication. In contrast, we did not detect USUV in 15,381 questing ticks collected in 2017 and 2019. We conclude that I . ricinus can be infected with USUV and can transstadially and horizontally transmit USUV. However, in comparison to mosquito-borne transmission, the role of I . ricinus ticks in the epidemiology of USUV is expected to be minor.
AbstractList Usutu virus (USUV) is an emerging flavivirus that is maintained in an enzootic cycle with mosquitoes as vectors and birds as amplifying hosts. In Europe, the virus has caused mass mortality of wild birds, mainly among Common Blackbird (Turdus merula) populations. While mosquitoes are the primary vectors for USUV, Common Blackbirds and other avian species are exposed to other arthropod ectoparasites, such as ticks. It is unknown, however, if ticks can maintain and transmit USUV. We addressed this question using in vitro and in vivo experiments and field collected data. USUV replicated in IRE/CTVM19 Ixodes ricinus tick cells and in injected ticks. Moreover, I. ricinus nymphs acquired the virus via artificial membrane blood-feeding and maintained the virus for at least 70 days. Transstadial transmission of USUV from nymphs to adults was confirmed in 4.9% of the ticks. USUV disseminated from the midgut to the haemocoel, and was transmitted via the saliva of the tick during artificial membrane blood-feeding. We further explored the role of ticks by monitoring USUV in questing ticks and in ticks feeding on wild birds in the Netherlands between 2016 and 2019. In total, 622 wild birds and the Ixodes ticks they carried were tested for USUV RNA. Of these birds, 48 (7.7%) carried USUV-positive ticks. The presence of negative-sense USUV RNA in ticks, as confirmed via small RNA-sequencing, showed active virus replication. In contrast, we did not detect USUV in 15,381 questing ticks collected in 2017 and 2019. We conclude that I. ricinus can be infected with USUV and can transstadially and horizontally transmit USUV. However, in comparison to mosquito-borne transmission, the role of I. ricinus ticks in the epidemiology of USUV is expected to be minor.
Usutu virus (USUV) is an emerging flavivirus that is maintained in an enzootic cycle with mosquitoes as vectors and birds as amplifying hosts. In Europe, the virus has caused mass mortality of wild birds, mainly among Common Blackbird (Turdus merula) populations. While mosquitoes are the primary vectors for USUV, Common Blackbirds and other avian species are exposed to other arthropod ectoparasites, such as ticks. It is unknown, however, if ticks can maintain and transmit USUV. We addressed this question using in vitro and in vivo experiments and field collected data. USUV replicated in IRE/CTVM19 Ixodes ricinus tick cells and in injected ticks. Moreover, I. ricinus nymphs acquired the virus via artificial membrane blood-feeding and maintained the virus for at least 70 days. Transstadial transmission of USUV from nymphs to adults was confirmed in 4.9% of the ticks. USUV disseminated from the midgut to the haemocoel, and was transmitted via the saliva of the tick during artificial membrane blood-feeding. We further explored the role of ticks by monitoring USUV in questing ticks and in ticks feeding on wild birds in the Netherlands between 2016 and 2019. In total, 622 wild birds and the Ixodes ticks they carried were tested for USUV RNA. Of these birds, 48 (7.7%) carried USUV-positive ticks. The presence of negative-sense USUV RNA in ticks, as confirmed via small RNA-sequencing, showed active virus replication. In contrast, we did not detect USUV in 15,381 questing ticks collected in 2017 and 2019. We conclude that I. ricinus can be infected with USUV and can transstadially and horizontally transmit USUV. However, in comparison to mosquito-borne transmission, the role of I. ricinus ticks in the epidemiology of USUV is expected to be minor.Usutu virus (USUV) is an emerging flavivirus that is maintained in an enzootic cycle with mosquitoes as vectors and birds as amplifying hosts. In Europe, the virus has caused mass mortality of wild birds, mainly among Common Blackbird (Turdus merula) populations. While mosquitoes are the primary vectors for USUV, Common Blackbirds and other avian species are exposed to other arthropod ectoparasites, such as ticks. It is unknown, however, if ticks can maintain and transmit USUV. We addressed this question using in vitro and in vivo experiments and field collected data. USUV replicated in IRE/CTVM19 Ixodes ricinus tick cells and in injected ticks. Moreover, I. ricinus nymphs acquired the virus via artificial membrane blood-feeding and maintained the virus for at least 70 days. Transstadial transmission of USUV from nymphs to adults was confirmed in 4.9% of the ticks. USUV disseminated from the midgut to the haemocoel, and was transmitted via the saliva of the tick during artificial membrane blood-feeding. We further explored the role of ticks by monitoring USUV in questing ticks and in ticks feeding on wild birds in the Netherlands between 2016 and 2019. In total, 622 wild birds and the Ixodes ticks they carried were tested for USUV RNA. Of these birds, 48 (7.7%) carried USUV-positive ticks. The presence of negative-sense USUV RNA in ticks, as confirmed via small RNA-sequencing, showed active virus replication. In contrast, we did not detect USUV in 15,381 questing ticks collected in 2017 and 2019. We conclude that I. ricinus can be infected with USUV and can transstadially and horizontally transmit USUV. However, in comparison to mosquito-borne transmission, the role of I. ricinus ticks in the epidemiology of USUV is expected to be minor.
Usutu virus (USUV) is an emerging flavivirus that is maintained in an enzootic cycle with mosquitoes as vectors and birds as amplifying hosts. In Europe, the virus has caused mass mortality of wild birds, mainly among Common Blackbird ( Turdus merula ) populations. While mosquitoes are the primary vectors for USUV, Common Blackbirds and other avian species are exposed to other arthropod ectoparasites, such as ticks. It is unknown, however, if ticks can maintain and transmit USUV. We addressed this question using in vitro and in vivo experiments and field collected data. USUV replicated in IRE/CTVM19 Ixodes ricinus tick cells and in injected ticks. Moreover, I . ricinus nymphs acquired the virus via artificial membrane blood-feeding and maintained the virus for at least 70 days. Transstadial transmission of USUV from nymphs to adults was confirmed in 4.9% of the ticks. USUV disseminated from the midgut to the haemocoel, and was transmitted via the saliva of the tick during artificial membrane blood-feeding. We further explored the role of ticks by monitoring USUV in questing ticks and in ticks feeding on wild birds in the Netherlands between 2016 and 2019. In total, 622 wild birds and the Ixodes ticks they carried were tested for USUV RNA. Of these birds, 48 (7.7%) carried USUV-positive ticks. The presence of negative-sense USUV RNA in ticks, as confirmed via small RNA-sequencing, showed active virus replication. In contrast, we did not detect USUV in 15,381 questing ticks collected in 2017 and 2019. We conclude that I . ricinus can be infected with USUV and can transstadially and horizontally transmit USUV. However, in comparison to mosquito-borne transmission, the role of I . ricinus ticks in the epidemiology of USUV is expected to be minor. Usutu virus (USUV) is a virus primarily circulating between birds and mosquitoes. Other blood-feeding arthropods, such as ticks, feed on birds. However, it is unknown whether ticks can be infected with USUV and transmit the virus to birds or other animals. Therefore, we infected a tick cell line and ticks collected from the field with USUV. We showed that the virus replicates in tick cells, as well as in field-collected ticks. Moreover, we showed that USUV disseminated through the tick body and was excreted with the saliva of ticks during artificial feeding. We further investigated if ticks are infected with USUV while feeding on wild birds and when searching for a host in the vegetation. We found that 7.7% of tick-infested birds carried USUV positive ticks, while USUV was not detected in questing ticks. Our findings provide evidence that ticks can be infected with USUV and might transmit the virus to another host, but the role of ticks in the transmission of USUV is expected to be minor.
Usutu virus (USUV) is an emerging flavivirus that is maintained in an enzootic cycle with mosquitoes as vectors and birds as amplifying hosts. In Europe, the virus has caused mass mortality of wild birds, mainly among Common Blackbird ( Turdus merula ) populations. While mosquitoes are the primary vectors for USUV, Common Blackbirds and other avian species are exposed to other arthropod ectoparasites, such as ticks. It is unknown, however, if ticks can maintain and transmit USUV. We addressed this question using in vitro and in vivo experiments and field collected data. USUV replicated in IRE/CTVM19 Ixodes ricinus tick cells and in injected ticks. Moreover, I . ricinus nymphs acquired the virus via artificial membrane blood-feeding and maintained the virus for at least 70 days. Transstadial transmission of USUV from nymphs to adults was confirmed in 4.9% of the ticks. USUV disseminated from the midgut to the haemocoel, and was transmitted via the saliva of the tick during artificial membrane blood-feeding. We further explored the role of ticks by monitoring USUV in questing ticks and in ticks feeding on wild birds in the Netherlands between 2016 and 2019. In total, 622 wild birds and the Ixodes ticks they carried were tested for USUV RNA. Of these birds, 48 (7.7%) carried USUV-positive ticks. The presence of negative-sense USUV RNA in ticks, as confirmed via small RNA-sequencing, showed active virus replication. In contrast, we did not detect USUV in 15,381 questing ticks collected in 2017 and 2019. We conclude that I . ricinus can be infected with USUV and can transstadially and horizontally transmit USUV. However, in comparison to mosquito-borne transmission, the role of I . ricinus ticks in the epidemiology of USUV is expected to be minor.
Audience Academic
Author Esser, Helen J.
Kohl, Robert
Bakker, Julian W.
Münger, Emmanuelle
de Boer, Willem F.
Munnink, Bas B. Oude
Sprong, Hein
Reusken, Chantal B. E. M.
van der Linden, Anne
Stroo, Arjan
van der Jeugd, Henk
Koenraadt, Constantianus J. M.
Pijlman, Gorben P.
Koopmans, Marion P. G.
de Vries, Ankje
Sikkema, Reina S.
AuthorAffiliation 7 Laboratory of Virology, Wageningen University & Research, Wageningen, the Netherlands
6 Centre for Monitoring of Vectors, Netherlands Food and Consumer Product Safety Authority (NVWA), Wageningen, the Netherlands
4 Vogeltrekstation, Dutch Centre for Avian Migration and Demography, NIOO-KNAW, Wageningen, the Netherlands
1 Laboratory of Entomology, Wageningen University & Research, Wageningen, the Netherlands
Faculty of Science, Ain Shams University (ASU), EGYPT
2 Department of Viroscience, Erasmus MC, Rotterdam, the Netherlands
5 National Institute of Public Health and the Environment (RIVM), Utrecht, the Netherlands
3 Wildlife Ecology and Conservation Group, Wageningen University & Research, Wageningen, the Netherlands
AuthorAffiliation_xml – name: 3 Wildlife Ecology and Conservation Group, Wageningen University & Research, Wageningen, the Netherlands
– name: 5 National Institute of Public Health and the Environment (RIVM), Utrecht, the Netherlands
– name: 7 Laboratory of Virology, Wageningen University & Research, Wageningen, the Netherlands
– name: 2 Department of Viroscience, Erasmus MC, Rotterdam, the Netherlands
– name: 4 Vogeltrekstation, Dutch Centre for Avian Migration and Demography, NIOO-KNAW, Wageningen, the Netherlands
– name: Faculty of Science, Ain Shams University (ASU), EGYPT
– name: 1 Laboratory of Entomology, Wageningen University & Research, Wageningen, the Netherlands
– name: 6 Centre for Monitoring of Vectors, Netherlands Food and Consumer Product Safety Authority (NVWA), Wageningen, the Netherlands
Author_xml – sequence: 1
  givenname: Julian W.
  orcidid: 0000-0002-1084-7729
  surname: Bakker
  fullname: Bakker, Julian W.
– sequence: 2
  givenname: Emmanuelle
  surname: Münger
  fullname: Münger, Emmanuelle
– sequence: 3
  givenname: Helen J.
  surname: Esser
  fullname: Esser, Helen J.
– sequence: 4
  givenname: Reina S.
  surname: Sikkema
  fullname: Sikkema, Reina S.
– sequence: 5
  givenname: Willem F.
  surname: de Boer
  fullname: de Boer, Willem F.
– sequence: 6
  givenname: Hein
  surname: Sprong
  fullname: Sprong, Hein
– sequence: 7
  givenname: Chantal B. E. M.
  surname: Reusken
  fullname: Reusken, Chantal B. E. M.
– sequence: 8
  givenname: Ankje
  surname: de Vries
  fullname: de Vries, Ankje
– sequence: 9
  givenname: Robert
  surname: Kohl
  fullname: Kohl, Robert
– sequence: 10
  givenname: Anne
  surname: van der Linden
  fullname: van der Linden, Anne
– sequence: 11
  givenname: Arjan
  surname: Stroo
  fullname: Stroo, Arjan
– sequence: 12
  givenname: Henk
  surname: van der Jeugd
  fullname: van der Jeugd, Henk
– sequence: 13
  givenname: Gorben P.
  surname: Pijlman
  fullname: Pijlman, Gorben P.
– sequence: 14
  givenname: Marion P. G.
  surname: Koopmans
  fullname: Koopmans, Marion P. G.
– sequence: 15
  givenname: Bas B. Oude
  surname: Munnink
  fullname: Munnink, Bas B. Oude
– sequence: 16
  givenname: Constantianus J. M.
  surname: Koenraadt
  fullname: Koenraadt, Constantianus J. M.
BackLink https://www.ncbi.nlm.nih.gov/pubmed/38985837$$D View this record in MEDLINE/PubMed
BookMark eNp9kl2LEzEUhoOsuB_6D0QGBPGmNcmZTGa8kWXxo7DgjXsdMvloU9KkJpmi_97UdqUVkSHMkDzvM-eQc40uQgwGoZcEzwlw8m4dpxSkn29D0XOMCSWcPkFXZAA2oxzYxcn3JbrOeY0xG1hPnqFL6Iee9cCvEF38iNrkJjnlwpQbmZttLCYUJ32zM6rE1Ni6HvJUpmbn0pSfo6dW-mxeHN836OHTx293X2b3Xz8v7m7vZ4pxKDPLLR5GCpxDS9U4Gt5ro1sLHdGApSZGEQV2ZIRQ2tmWqZHpdtCd1JaMeIQbtDh4dZRrsU1uI9NPEaUTvzdiWgqZilPeCAb1T5RLMNi0lo8DgOQaV5kZKFakuj4cXNtp3BitaoNJ-jPp-UlwK7GMO1GLg45iVg1vj4YUv08mF7FxWRnvZTBxygIw7zlpB9ZV9PUBXcpamws2VqXa4-K2x8D6ykCl5v-g6qPNxql619bV_bPAm5PAykhfVjn6qbgY8jn46rTZP10-3noF3h8AlWLOyVihXJF7Ty3BeUGw2I-YOI6Y2I-YOI5YDbd_hR_9_439Argh2A0
CitedBy_id crossref_primary_10_1111_zph_13213
crossref_primary_10_1099_jgv_0_002041
crossref_primary_10_3389_fmicb_2025_1548538
Cites_doi 10.1016/j.onehlt.2023.100572
10.1093/jmedent/31.1.1
10.1016/S0022-2836(05)80360-2
10.4269/ajtmh.2011.11-0248
10.1002/wrna.1361
10.3390/v11020181
10.1016/j.pt.2007.07.009
10.1080/22221751.2024.2321992
10.1371/journal.pntd.0008217
10.3201/eid2812.220552
10.1093/ve/vew033
10.1007/s00436-016-5022-5
10.3390/v12121441
10.3390/v15010077
10.1017/S0031182004004925
10.2807/1560-7917.ES.2020.25.41.2001732
10.1080/22221751.2020.1854623
10.32614/RJ-2017-066
10.1038/s41598-020-71920-z
10.1016/j.pt.2015.09.009
10.1603/0022-2585-40.4.528
10.1016/j.prevetmed.2008.01.006
10.3390/v13122463
10.1016/j.meegid.2019.04.015
10.1093/bioinformatics/btab705
10.4269/ajtmh.18-0134
10.1093/oxfordjournals.aje.a118408
10.1016/j.virol.2015.03.033
10.3201/eid2312.171257
10.1089/vbz.2005.5.65
10.2807/1560-7917.ES.2016.21.45.30391
10.1038/s41598-020-59692-y
10.1093/jme/tjv241
10.3201/eid1902.121191
10.1093/molbev/msu300
10.1016/j.jviromet.2013.08.039
10.1016/j.vetmic.2011.03.036
10.14411/fp.2021.024
10.1089/vbz.2012.1190
10.1093/nar/gku657
10.1186/s13071-017-2399-7
10.1128/JVI.80.8.4099-4113.2006
10.1016/j.pt.2007.07.010
10.3390/pathogens9100780
10.1371/journal.pone.0109905
10.1016/j.onehlt.2015.08.002
10.1186/1471-2105-5-113
10.1134/S0013873810020090
10.1016/j.cois.2022.100875
10.1016/j.vetmic.2007.01.029
10.1016/j.ttbdis.2022.102114
10.1007/s10493-019-00375-3
10.1186/s13071-017-2000-4
10.1101/gr.4086505
10.3389/fcimb.2017.00236
10.1186/1471-2199-10-26
10.3390/pathogens9090699
10.3390/v7010219
10.1134/S1062359014040086
10.1016/S0264-410X(02)00812-5
10.1093/nar/gkp1024
10.1186/s13071-019-3316-z
10.1093/bioinformatics/bty560
ContentType Journal Article
Copyright Copyright: © 2024 Bakker et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
COPYRIGHT 2024 Public Library of Science
2024 Bakker et al 2024 Bakker et al
Copyright_xml – notice: Copyright: © 2024 Bakker et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
– notice: COPYRIGHT 2024 Public Library of Science
– notice: 2024 Bakker et al 2024 Bakker et al
DBID AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
7X8
5PM
DOA
DOI 10.1371/journal.pntd.0012172
DatabaseName CrossRef
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
MEDLINE - Academic
PubMed Central (Full Participant titles)
DOAJ Open Access Full Text
DatabaseTitle CrossRef
MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
MEDLINE - Academic
DatabaseTitleList
MEDLINE
MEDLINE - Academic



CrossRef
Database_xml – sequence: 1
  dbid: DOA
  name: DOAJ Directory of Open Access Journals
  url: https://www.doaj.org/
  sourceTypes: Open Website
– sequence: 2
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 3
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
DeliveryMethod fulltext_linktorsrc
Discipline Medicine
DocumentTitleAlternate Ixodes ricinus as a potential vector for Usutu virus
EISSN 1935-2735
ExternalDocumentID oai_doaj_org_article_539b227a3e0e4f7b933a7d09d6e920c1
PMC11236205
A803585633
38985837
10_1371_journal_pntd_0012172
Genre Journal Article
GeographicLocations Netherlands
GeographicLocations_xml – name: Netherlands
GrantInformation_xml – fundername: ;
– fundername: ;
  grantid: No. 874735 (VEO)
– fundername: ;
  grantid: 109986
– fundername: ;
  grantid: 522003004
GroupedDBID ---
123
29O
2WC
53G
5VS
7X7
88E
8C1
8FI
8FJ
AAFWJ
AAUCC
AAWOE
AAYXX
ABDBF
ABUWG
ACGFO
ACIHN
ACPRK
ACUHS
ADBBV
AEAQA
AENEX
AEUYN
AFKRA
AFPKN
AFRAH
AHMBA
ALIPV
ALMA_UNASSIGNED_HOLDINGS
AOIJS
BAWUL
BCNDV
BENPR
BPHCQ
BVXVI
BWKFM
CCPQU
CITATION
CS3
DIK
DU5
E3Z
EAP
EAS
EBD
ECGQY
EMOBN
ESX
F5P
FPL
FYUFA
GROUPED_DOAJ
GX1
HMCUK
HYE
IAO
IHR
IHW
ITC
KQ8
M1P
M48
O5R
O5S
OK1
OVT
P2P
PGMZT
PHGZM
PHGZT
PIMPY
PQQKQ
PROAC
PSQYO
PV9
RNS
RPM
RZL
SV3
TR2
TUS
UKHRP
3V.
ADRAZ
CGR
CUY
CVF
ECM
EIF
H13
IPNFZ
M~E
NPM
RIG
WOQ
PMFND
7X8
PPXIY
5PM
PJZUB
PUEGO
ID FETCH-LOGICAL-c573t-f7f09b2377342cbbe78ded4f361d30ad1ec1c3fb511226f45cb5d49d6adf1b0b3
IEDL.DBID M48
ISSN 1935-2735
1935-2727
IngestDate Wed Aug 27 01:30:19 EDT 2025
Thu Aug 21 18:32:20 EDT 2025
Thu Jul 10 22:40:56 EDT 2025
Tue Jun 17 22:05:53 EDT 2025
Tue Jun 10 21:06:08 EDT 2025
Thu May 22 21:24:00 EDT 2025
Wed Feb 19 02:04:40 EST 2025
Tue Jul 01 00:44:54 EDT 2025
Thu Apr 24 22:56:08 EDT 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 7
Language English
License Copyright: © 2024 Bakker et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c573t-f7f09b2377342cbbe78ded4f361d30ad1ec1c3fb511226f45cb5d49d6adf1b0b3
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
BBOM and CJMK also contributed equally to this work.
The authors have declared that no competing interests exist.
ORCID 0000-0002-1084-7729
OpenAccessLink https://doaj.org/article/539b227a3e0e4f7b933a7d09d6e920c1
PMID 38985837
PQID 3078714956
PQPubID 23479
ParticipantIDs doaj_primary_oai_doaj_org_article_539b227a3e0e4f7b933a7d09d6e920c1
pubmedcentral_primary_oai_pubmedcentral_nih_gov_11236205
proquest_miscellaneous_3078714956
gale_infotracmisc_A803585633
gale_infotracacademiconefile_A803585633
gale_healthsolutions_A803585633
pubmed_primary_38985837
crossref_citationtrail_10_1371_journal_pntd_0012172
crossref_primary_10_1371_journal_pntd_0012172
ProviderPackageCode CITATION
AAYXX
PublicationCentury 2000
PublicationDate 20240710
PublicationDateYYYYMMDD 2024-07-10
PublicationDate_xml – month: 7
  year: 2024
  text: 20240710
  day: 10
PublicationDecade 2020
PublicationPlace United States
PublicationPlace_xml – name: United States
– name: San Francisco, CA USA
PublicationTitle PLoS neglected tropical diseases
PublicationTitleAlternate PLoS Negl Trop Dis
PublicationYear 2024
Publisher Public Library of Science
Public Library of Science (PLoS)
Publisher_xml – name: Public Library of Science
– name: Public Library of Science (PLoS)
References FS Flores (pntd.0012172.ref019) 2019; 100
IG Korobitsyn (pntd.0012172.ref022) 2021; 68
JD Oliver (pntd.0012172.ref028) 2016; 53
K Liebig (pntd.0012172.ref057) 2020; 10
D Cadar (pntd.0012172.ref011) 2023; 15
C Klaus (pntd.0012172.ref014) 2016; 115
MM Diagne (pntd.0012172.ref066) 2019; 11
JM Rijks (pntd.0012172.ref004) 2016; 21
OW Lwande (pntd.0012172.ref023) 2013; 13
R Lühken (pntd.0012172.ref010) 2017; 23
I Rudolf (pntd.0012172.ref069) 2017; 10
C Răileanu (pntd.0012172.ref020) 2020; 9
G Cheng (pntd.0012172.ref003) 2016; 32
JF Anderson (pntd.0012172.ref018) 2003; 40
U Ashraf (pntd.0012172.ref007) 2015; 7
JW Bakker (pntd.0012172.ref030) 2024; 13
EV Chausov (pntd.0012172.ref073) 2010; 90
PA Nuttall (pntd.0012172.ref062) 1994; 31
H Jöst (pntd.0012172.ref002) 2011; 85
BB Oude Munnink (pntd.0012172.ref040) 2019; 73
SI Bonnet (pntd.0012172.ref058) 2017; 7
N Moskvitina (pntd.0012172.ref075) 2008; 42
J Kolodziejek (pntd.0012172.ref021) 2014; 9
T Vilibic-Cavlek (pntd.0012172.ref006) 2020; 9
G Savini (pntd.0012172.ref009) 2011; 151
JV Camp (pntd.0012172.ref013) 2019; 12
AT Ciota (pntd.0012172.ref064) 2015; 482
FG Sauer (pntd.0012172.ref072) 2023; 16
IV Llopis (pntd.0012172.ref026) 2016; 40
H Wang (pntd.0012172.ref032) 2020; 9
AJ Folly (pntd.0012172.ref005) 2020; 25
pntd.0012172.ref041
B Giardine (pntd.0012172.ref035) 2005; 15
O Folmer (pntd.0012172.ref038) 1994; 3
A Bergman (pntd.0012172.ref070) 2020; 12
J. Allaire (pntd.0012172.ref053) 2012
ND Grubaugh (pntd.0012172.ref061) 2016; 2
RM Kofler (pntd.0012172.ref063) 2006; 80
F Mancini (pntd.0012172.ref025) 2013; 36
H. Li (pntd.0012172.ref043) 2021; 37
NS Moskvitina (pntd.0012172.ref024) 2014; 41
KY Mumcuoglu (pntd.0012172.ref074) 2005; 5
R core team (pntd.0012172.ref052) 2021
SE Randolph (pntd.0012172.ref016) 2004; 129
L Bell-Sakyi (pntd.0012172.ref027) 2007; 23
T Kröber (pntd.0012172.ref031) 2007; 23
IA Azarova (pntd.0012172.ref017) 2002
DA Benson (pntd.0012172.ref044) 2010; 38
RC Edgar (pntd.0012172.ref045) 2004; 5
S Kurscheid (pntd.0012172.ref060) 2009; 10
M Drehmann (pntd.0012172.ref065) 2019; 78
HJ Esser (pntd.0012172.ref048) 2022; 28
LJ Reed (pntd.0012172.ref033) 1938; 27
S Chen (pntd.0012172.ref042) 2018; 34
pntd.0012172.ref049
SR Abbo (pntd.0012172.ref034) 2020; 14
pntd.0012172.ref054
H Weissenböck (pntd.0012172.ref001) 2013; 19
JM Rijks (pntd.0012172.ref047) 2019; 25
pntd.0012172.ref051
E Schnettler (pntd.0012172.ref055) 2014; 42
S Chvala (pntd.0012172.ref008) 2007; 122
B Nikolay (pntd.0012172.ref037) 2014; 197
ME Brooks (pntd.0012172.ref050) 2017; 9
EP Caragata (pntd.0012172.ref059) 2022; 50
LT Nguyen (pntd.0012172.ref046) 2015; 32
O Kahl (pntd.0012172.ref067) 2023; 14
ERGR Aguiar (pntd.0012172.ref056) 2016; 7
C Krull (pntd.0012172.ref029) 2017; 10
J Süss (pntd.0012172.ref015) 2003; 21
SF Altschul (pntd.0012172.ref039) 1990; 215
JJ Fros (pntd.0012172.ref012) 2015; 1
F Rubel (pntd.0012172.ref068) 2008; 85
H Kampen (pntd.0012172.ref071) 2021; 13
BB Oude Munnink (pntd.0012172.ref036) 2020; 10
References_xml – volume: 16
  start-page: 100572
  year: 2023
  ident: pntd.0012172.ref072
  article-title: Overwintering Culex torrentium in abandoned animal burrows as a reservoir for arboviruses in Central Europe
  publication-title: One Health
  doi: 10.1016/j.onehlt.2023.100572
– volume: 31
  start-page: 1
  year: 1994
  ident: pntd.0012172.ref062
  article-title: Adaptations of arboviruses to ticks
  publication-title: Journal of Medical Entomology
  doi: 10.1093/jmedent/31.1.1
– volume: 215
  start-page: 403
  year: 1990
  ident: pntd.0012172.ref039
  article-title: Basic local alignment search tool
  publication-title: Journal of Molecular Biology
  doi: 10.1016/S0022-2836(05)80360-2
– volume: 85
  start-page: 551
  year: 2011
  ident: pntd.0012172.ref002
  article-title: Isolation of Usutu virus in Germany
  publication-title: American Journal of Tropical Medicine and Hygiene
  doi: 10.4269/ajtmh.2011.11-0248
– volume: 7
  start-page: 824
  year: 2016
  ident: pntd.0012172.ref056
  article-title: Virus-derived small RNAs: molecular footprints of host—pathogen interactions
  publication-title: Wiley Interdisciplinary Reviews: RNA
  doi: 10.1002/wrna.1361
– volume: 11
  start-page: 181
  year: 2019
  ident: pntd.0012172.ref066
  article-title: Usutu virus isolated from rodents in Senegal
  publication-title: Viruses
  doi: 10.3390/v11020181
– volume: 23
  start-page: 450
  year: 2007
  ident: pntd.0012172.ref027
  article-title: Tick cell lines: tools for tick and tick-borne disease research
  publication-title: Trends in Parasitology
  doi: 10.1016/j.pt.2007.07.009
– volume: 13
  start-page: 2321992
  year: 2024
  ident: pntd.0012172.ref030
  article-title: Differential susceptibility of geographically distinct Ixodes ricinus populations to tick-borne encephalitis virus and louping ill virus
  publication-title: Emerging Microbes & Infections
  doi: 10.1080/22221751.2024.2321992
– start-page: 27
  volume-title: Ecology, Biodiversity and Role of Blood Sucking Insects and Ticks in the Ecosystems of Russia Proc II Resp ScI Conf V Novgorod
  year: 2002
  ident: pntd.0012172.ref017
– volume: 14
  start-page: e0008217
  year: 2020
  ident: pntd.0012172.ref034
  article-title: The invasive asian bush mosquito Aedes japonicus found in the Netherlands can experimentally transmit Zika virus and Usutu virus
  publication-title: PLoS Neglected Tropical Diseases
  doi: 10.1371/journal.pntd.0008217
– volume: 28
  start-page: 2416
  year: 2022
  ident: pntd.0012172.ref048
  article-title: Continued circulation of tick-borne encephalitis virus variants and detection of novel transmission foci, the Netherlands
  publication-title: Emerging Infectious Diseases
  doi: 10.3201/eid2812.220552
– volume: 2
  start-page: 1
  year: 2016
  ident: pntd.0012172.ref061
  article-title: Transmission bottlenecks and RNAi collectively influence tick-borne flavivirus evolution
  publication-title: Virus Evolution
  doi: 10.1093/ve/vew033
– volume: 115
  start-page: 2729
  year: 2016
  ident: pntd.0012172.ref014
  article-title: Tick infestation in birds and prevalence of pathogens in ticks collected from different places in Germany
  publication-title: Parasitology Research
  doi: 10.1007/s00436-016-5022-5
– volume-title: R Foundation for Statistical Computing
  year: 2021
  ident: pntd.0012172.ref052
– volume: 12
  start-page: 1441
  year: 2020
  ident: pntd.0012172.ref070
  article-title: Sindbis virus Infection in non-blood-fed hibernating Culex pipiens mosquitoes in Sweden
  publication-title: Viruses
  doi: 10.3390/v12121441
– volume: 15
  start-page: 77
  year: 2023
  ident: pntd.0012172.ref011
  article-title: Human Usutu Virus Infections in Europe: A New Risk on Horizon?
  publication-title: Viruses
  doi: 10.3390/v15010077
– volume: 129
  start-page: 37
  year: 2004
  ident: pntd.0012172.ref016
  article-title: Tick ecology: Processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors
  publication-title: Parasitology
  doi: 10.1017/S0031182004004925
– volume: 25
  start-page: 2001732
  year: 2020
  ident: pntd.0012172.ref005
  article-title: Detection of Usutu virus infection in wild birds in the United Kingdom, 2020
  publication-title: Eurosurveillance
  doi: 10.2807/1560-7917.ES.2020.25.41.2001732
– volume: 9
  start-page: 2642
  year: 2020
  ident: pntd.0012172.ref032
  article-title: Competition between Usutu virus and West Nile virus during simultaneous and sequential infection of Culex pipiens mosquitoes
  publication-title: Emerging Microbes and Infections
  doi: 10.1080/22221751.2020.1854623
– volume: 9
  start-page: 378
  year: 2017
  ident: pntd.0012172.ref050
  article-title: glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling
  publication-title: R Journal
  doi: 10.32614/RJ-2017-066
– volume: 3
  start-page: 294
  year: 1994
  ident: pntd.0012172.ref038
  article-title: DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates
  publication-title: Molecular marine biology and biotechnology
– volume: 10
  start-page: 15478
  year: 2020
  ident: pntd.0012172.ref057
  article-title: Tick populations from endemic and non-endemic areas in Germany show differential susceptibility to TBEV
  publication-title: Scientific Reports
  doi: 10.1038/s41598-020-71920-z
– volume: 32
  start-page: 177
  year: 2016
  ident: pntd.0012172.ref003
  article-title: Mosquito defense strategies against viral infection
  publication-title: Trends in Parasitology
  doi: 10.1016/j.pt.2015.09.009
– volume: 40
  start-page: 528
  year: 2003
  ident: pntd.0012172.ref018
  article-title: Transstadial transfer of West Nile virus by three species of ixodid ticks (Acari: Ixodidae)
  publication-title: Journal of Medical Entomology
  doi: 10.1603/0022-2585-40.4.528
– volume: 85
  start-page: 166
  year: 2008
  ident: pntd.0012172.ref068
  article-title: Explaining Usutu virus dynamics in Austria: Model development and calibration
  publication-title: Preventive Veterinary Medicine
  doi: 10.1016/j.prevetmed.2008.01.006
– volume: 13
  start-page: 2463
  year: 2021
  ident: pntd.0012172.ref071
  article-title: First evidence of West Nile virus overwintering in mosquitoes in Germany
  publication-title: Viruses
  doi: 10.3390/v13122463
– start-page: 165
  volume-title: RStudio: integrated development environment for R
  year: 2012
  ident: pntd.0012172.ref053
– volume: 73
  start-page: 49
  year: 2019
  ident: pntd.0012172.ref040
  article-title: Towards high quality real-time whole genome sequencing during outbreaks using Usutu virus as example
  publication-title: Infection, Genetics and Evolution
  doi: 10.1016/j.meegid.2019.04.015
– volume: 37
  start-page: 4572
  year: 2021
  ident: pntd.0012172.ref043
  article-title: New strategies to improve minimap2 alignment accuracy
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btab705
– volume: 100
  start-page: 1230
  year: 2019
  ident: pntd.0012172.ref019
  article-title: Vector competence for West Nile virus and St. Louis encephalitis virus (flavivirus) of three tick species of the genus Amblyomma (Acari: Ixodidae)
  publication-title: American Journal of Tropical Medicine and Hygiene
  doi: 10.4269/ajtmh.18-0134
– volume: 27
  start-page: 493
  year: 1938
  ident: pntd.0012172.ref033
  article-title: A simple method of estimating fifty percent endpoints
  publication-title: American journal of epidemiology
  doi: 10.1093/oxfordjournals.aje.a118408
– volume: 482
  start-page: 128
  year: 2015
  ident: pntd.0012172.ref064
  article-title: West Nile virus adaptation to ixodid tick cells is associated with phenotypic trade-offs in primary hosts
  publication-title: Virology
  doi: 10.1016/j.virol.2015.03.033
– volume: 23
  start-page: 1991
  year: 2017
  ident: pntd.0012172.ref010
  article-title: Distribution of Usutu virus in Germany and its effect on breeding bird populations
  publication-title: Emerging Infectious Diseases
  doi: 10.3201/eid2312.171257
– volume: 5
  start-page: 66
  year: 2005
  ident: pntd.0012172.ref074
  article-title: Argasid ticks as possible vectors of West Nile Virus in Israel
  publication-title: Vector borne and zoonotic diseases
  doi: 10.1089/vbz.2005.5.65
– volume: 21
  start-page: 30391
  year: 2016
  ident: pntd.0012172.ref004
  article-title: Widespread Usutu virus outbreak in birds in The Netherlands, 2016
  publication-title: Eurosurveillance
  doi: 10.2807/1560-7917.ES.2016.21.45.30391
– volume: 10
  start-page: 2798
  year: 2020
  ident: pntd.0012172.ref036
  article-title: Genomic monitoring to understand the emergence and spread of Usutu virus in the Netherlands, 2016–2018
  publication-title: Scientific Reports
  doi: 10.1038/s41598-020-59692-y
– volume: 36
  start-page: 433
  year: 2013
  ident: pntd.0012172.ref025
  article-title: Virus investigation in ticks from migratory birds in Italy
  publication-title: New Microbiologica
– volume: 53
  start-page: 409
  year: 2016
  ident: pntd.0012172.ref028
  article-title: Infection of immature Ixodes scapularis (Acari: Ixodidae) by membrane feeding
  publication-title: Journal of Medical Entomology
  doi: 10.1093/jme/tjv241
– volume: 42
  start-page: 210
  year: 2008
  ident: pntd.0012172.ref075
  article-title: Detection of the West Nile Virus and its genetic typing in ixodid ticks (Parasitiformes: Ixodidae) in Tomsk City and its suburbs
  publication-title: Parazitologiia
– volume: 19
  start-page: 274
  year: 2013
  ident: pntd.0012172.ref001
  article-title: Usutu virus, Italy, 1996
  publication-title: Emerging Infectious Diseases
  doi: 10.3201/eid1902.121191
– volume: 32
  start-page: 268
  year: 2015
  ident: pntd.0012172.ref046
  article-title: IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies
  publication-title: Molecular Biology and Evolution
  doi: 10.1093/molbev/msu300
– volume: 197
  start-page: 51
  year: 2014
  ident: pntd.0012172.ref037
  article-title: Development of a Usutu virus specific real-time reverse transcription PCR assay based on sequenced strains from Africa and Europe
  publication-title: Journal of Virological Methods
  doi: 10.1016/j.jviromet.2013.08.039
– volume: 151
  start-page: 264
  year: 2011
  ident: pntd.0012172.ref009
  article-title: Usutu virus in Italy: An emergence or a silent infection?
  publication-title: Veterinary Microbiology
  doi: 10.1016/j.vetmic.2011.03.036
– volume: 68
  start-page: 1
  year: 2021
  ident: pntd.0012172.ref022
  article-title: Detection of tick-borne pathogens in wild birds and their ticks in Western Siberia and high level of their mismatch
  publication-title: Folia Parasitologica
  doi: 10.14411/fp.2021.024
– ident: pntd.0012172.ref054
– volume: 13
  start-page: 637
  year: 2013
  ident: pntd.0012172.ref023
  article-title: Isolation of tick and mosquito-borne arboviruses from ticks sampled from livestock and wild animal hosts in Ijara District, Kenya
  publication-title: Vector-Borne and Zoonotic Diseases
  doi: 10.1089/vbz.2012.1190
– volume: 42
  start-page: 9436
  year: 2014
  ident: pntd.0012172.ref055
  article-title: Induction and suppression of tick cell antiviral RNAi responses by tick-borne flaviviruses
  publication-title: Nucleic Acids Research
  doi: 10.1093/nar/gku657
– volume: 40
  start-page: 56
  year: 2016
  ident: pntd.0012172.ref026
  article-title: Investigation into Usutu and West Nile viruses in ticks from wild birds in Northwestern Italy, 2012–2014
  publication-title: New Microbiologica
– volume: 10
  start-page: 452
  year: 2017
  ident: pntd.0012172.ref069
  article-title: West Nile virus in overwintering mosquitoes, central Europe
  publication-title: Parasites and Vectors
  doi: 10.1186/s13071-017-2399-7
– volume: 80
  start-page: 4099
  year: 2006
  ident: pntd.0012172.ref063
  article-title: Functional analysis of the tick-borne encephalitis virus cyclization elements indicates major differences between mosquito-borne and tick-borne Flaviviruses
  publication-title: Journal of Virology
  doi: 10.1128/JVI.80.8.4099-4113.2006
– volume: 23
  start-page: 445
  year: 2007
  ident: pntd.0012172.ref031
  article-title: In vitro feeding assays for hard ticks
  publication-title: Trends in Parasitology
  doi: 10.1016/j.pt.2007.07.010
– volume: 9
  start-page: 780
  year: 2020
  ident: pntd.0012172.ref020
  article-title: Transstadial transmission and replication kinetics of West Nile virus lineage 1 in laboratory reared Ixodes ricinus ticks
  publication-title: Pathogens
  doi: 10.3390/pathogens9100780
– volume: 9
  start-page: e0109905
  year: 2014
  ident: pntd.0012172.ref021
  article-title: The complete sequence of a West Nile virus lineage 2 strain detected in a Hyalomma marginatum tick collected from a song thrush (Turdus philomelos) in Eastern Romania in 2013 revealed closest genetic relationship to strain Volgograd 2007
  publication-title: PLoS ONE
  doi: 10.1371/journal.pone.0109905
– volume: 1
  start-page: 31
  year: 2015
  ident: pntd.0012172.ref012
  article-title: Comparative Usutu and West Nile virus transmission potential by local Culex pipiens mosquitoes in north-western Europe
  publication-title: One Health
  doi: 10.1016/j.onehlt.2015.08.002
– volume: 5
  start-page: 1
  year: 2004
  ident: pntd.0012172.ref045
  article-title: MUSCLE: a multiple sequence alignment method with reduced time and space complexity
  publication-title: BMC bioinformatics
  doi: 10.1186/1471-2105-5-113
– volume: 90
  start-page: 240
  year: 2010
  ident: pntd.0012172.ref073
  article-title: Genetic diversity of tick-borne pathogenes in Tomsk and environs
  publication-title: Entomological Review
  doi: 10.1134/S0013873810020090
– volume: 50
  start-page: 100875
  year: 2022
  ident: pntd.0012172.ref059
  article-title: Vector microbiota and immunity: modulating arthropod susceptibility to vertebrate pathogens
  publication-title: Current Opinion in Insect Science
  doi: 10.1016/j.cois.2022.100875
– ident: pntd.0012172.ref049
– volume: 25
  start-page: 181386
  year: 2019
  ident: pntd.0012172.ref047
  article-title: Tick-borne encephalitis virus antibodies in roe deer, th Netherlands
  publication-title: Emerging Infectious Diseases
– ident: pntd.0012172.ref051
– volume: 122
  start-page: 237
  year: 2007
  ident: pntd.0012172.ref008
  article-title: Monitoring of Usutu virus activity and spread by using dead bird surveillance in Austria, 2003–2005
  publication-title: Veterinary Microbiology
  doi: 10.1016/j.vetmic.2007.01.029
– volume: 14
  start-page: 102114
  year: 2023
  ident: pntd.0012172.ref067
  article-title: The biology of Ixodes ricinus with emphasis on its ecology
  publication-title: Ticks and Tick-borne Diseases
  doi: 10.1016/j.ttbdis.2022.102114
– volume: 78
  start-page: 79
  year: 2019
  ident: pntd.0012172.ref065
  article-title: Ixodes frontalis: a neglected but ubiquitous tick species in Germany
  publication-title: Experimental and Applied Acarology
  doi: 10.1007/s10493-019-00375-3
– volume: 10
  start-page: 60
  year: 2017
  ident: pntd.0012172.ref029
  article-title: Optimization of an artificial tick feeding assay for Dermacentor reticulatus
  publication-title: Parasites and Vectors
  doi: 10.1186/s13071-017-2000-4
– volume: 15
  start-page: 1451
  year: 2005
  ident: pntd.0012172.ref035
  article-title: Galaxy: a platform for interactive large-scale genome analysis
  publication-title: Genome research
  doi: 10.1101/gr.4086505
– volume: 7
  start-page: 236
  year: 2017
  ident: pntd.0012172.ref058
  article-title: The tick microbiome: Why non-pathogenic microorganisms matter in tick biology and pathogen transmission
  publication-title: Frontiers in Cellular and Infection Microbiology
  doi: 10.3389/fcimb.2017.00236
– volume: 10
  start-page: 26
  year: 2009
  ident: pntd.0012172.ref060
  article-title: Evidence of a tick RNAi pathway by comparative genomics and reverse genetics screen of targets with known loss-of-function phenotypes in Drosophila
  publication-title: BMC Molecular Biology
  doi: 10.1186/1471-2199-10-26
– volume: 9
  start-page: 699
  year: 2020
  ident: pntd.0012172.ref006
  article-title: Epidemiology of usutu virus: The european scenario
  publication-title: Pathogens
  doi: 10.3390/pathogens9090699
– volume: 7
  start-page: 219
  year: 2015
  ident: pntd.0012172.ref007
  article-title: Usutu virus: An emerging flavivirus in Europe
  publication-title: Viruses
  doi: 10.3390/v7010219
– volume: 41
  start-page: 387
  year: 2014
  ident: pntd.0012172.ref024
  article-title: The role of birds in the maintenance of tick-borne infections in the Tomsk anthropurgic foci
  publication-title: Biology Bulletin
  doi: 10.1134/S1062359014040086
– volume: 21
  start-page: 19
  year: 2003
  ident: pntd.0012172.ref015
  article-title: Epidemiology and ecology of TBE relevant to the production of effective vaccines
  publication-title: Vaccine
  doi: 10.1016/S0264-410X(02)00812-5
– volume: 38
  start-page: D46
  year: 2010
  ident: pntd.0012172.ref044
  article-title: GenBank
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gkp1024
– ident: pntd.0012172.ref041
– volume: 12
  start-page: 46
  year: 2019
  ident: pntd.0012172.ref013
  article-title: Targeted surveillance reveals native and invasive mosquito species infected with Usutu virus
  publication-title: Parasites and Vectors
  doi: 10.1186/s13071-019-3316-z
– volume: 34
  start-page: i884
  year: 2018
  ident: pntd.0012172.ref042
  article-title: Fastp: An ultra-fast all-in-one FASTQ preprocessor
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/bty560
SSID ssj0059581
Score 2.4372246
Snippet Usutu virus (USUV) is an emerging flavivirus that is maintained in an enzootic cycle with mosquitoes as vectors and birds as amplifying hosts. In Europe, the...
SourceID doaj
pubmedcentral
proquest
gale
pubmed
crossref
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
Enrichment Source
StartPage e0012172
SubjectTerms Animals
Arachnid Vectors - physiology
Arachnid Vectors - virology
Biology and Life Sciences
Bird Diseases - transmission
Bird Diseases - virology
Birds - virology
Disease transmission
Entomology
Female
Flavivirus - genetics
Flavivirus - physiology
Flavivirus Infections - transmission
Flavivirus Infections - veterinary
Flavivirus Infections - virology
Insects as carriers of disease
Ixodes - physiology
Ixodes - virology
Medicine and Health Sciences
Netherlands
Nymph - virology
SummonAdditionalLinks – databaseName: DOAJ Open Access Full Text
  dbid: DOA
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1Lb9QwELZQD4gLgvJKaSFISJzSOnYcO8eCqApSObFSb5afohLKrjZJxc9nxvGuNuLQC8eNJyvN5xl7xvF8Q8hHI4xRHM81LLVV00ZYB6WllbLOW-awwTXWO9_8aK9XzfdbcXvQ6gvvhM30wDNwF4J3ljFpeKChidJCAm6kp51vQ8eoS4kP7Hm7ZGpeg0UnUntSiE6w4orJXDTHZX2R5-h804_-PFGaSbbYlBJ3_78r9MEWtbw-ebAfXT0jT3MgWV7OCjwnj0J_TB7f5E_lLwj79mftw1Bu8fc0lGYoN-sR7wbBW_fprL6EgLVcDdM4lfd322l4SVZXX39-ua5yg4TKCcnHKspIAR0uJW-YszZI5YNvImDvOTW-Dq52PFoMqlgbG-Gs8A1AZ3ysYW74K3LUr_vwhpTGNKoDf2yjgQDJt13rWcu5VKHG_w4F4TuEtMvs4djE4rdOn8QkZBGz3hpx1RnXglT7tzYze8YD8p8R_L0scl-nB2AROluEfsgiCvIep07PhaR7D9aXinJIjkCrgnxKEujDoIQzuRQBoEA2rIXk6UISfM8thj_szEPjEF5Y68N6GjQsnZCKYvZZkNezuey1ghhRCcVlQdTCkBZqL0f6u1-J-rtGshxGxcn_AOotecIgRMOT6pqekqNxO4UzCLFG-y55018LIyOW
  priority: 102
  providerName: Directory of Open Access Journals
Title Ixodes ricinus as potential vector for Usutu virus
URI https://www.ncbi.nlm.nih.gov/pubmed/38985837
https://www.proquest.com/docview/3078714956
https://pubmed.ncbi.nlm.nih.gov/PMC11236205
https://doaj.org/article/539b227a3e0e4f7b933a7d09d6e920c1
Volume 18
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwhR1ra9RAcKgtlH4R30brGUHwU44km2Q3H0Ta0lKFKyIe3Lewr2ihJGcepf57Z_Ligha_BJKdDczszM5jd2YA3stYSsEorqF85UVJjvsgV74nlDYq1NTgmvKdV1fJ5Tr6sok3ezD2bB0IWP_TtaN-UuvqZnn36_cnFPiPXdcGHoyTltuiMcuuSBnHTfkAdRMnUV1F07lCnMYiGBLo7pt5BIeoxEUsqDX6jq7qSvr_vXHvaK75rcodNXXxCB4O9qV70jPEY9izxRM4XA0n6E8h_HxXGlu7Fb23tStrd1s2dGUIZ912IXwX7Vh3XbdN695eV239DNYX59_PLr2hb4KnY84aL-e5n6qQcc6iUCtluTDWRDkuiWG-NIHVgWa5IlsrTPIo1io2UWoSafIAl4w9h_2iLOxLcKWMRIpimuQS7SaTpIkJE8a4sAH92zrARgpleigqTr0tbrLupIyjc9HjnRGJs4HEDnjTrG1fVOM_8KdE_AmWSmJ3H8rqRzZIWBYzxDnkklnfRjlXKWOSGx_Rsmno68CBt7R0WZ9fOgl2diJ8hj4TYuXAhw6CmA2R0HLIUEBSUJGsGeTxDBJFUs-G343skdEQ3WMrbNnWGe6o6KGSU-rAi55dJqxGrnNAzBhphvZ8pLj-2VUED6iGTujHr-796Ws4CtEco6h04B_DflO19g2aU41awAO-4fgUZ8ECDk7Pr75-W3ShiUUnO38A0RUjhw
linkProvider Scholars Portal
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Ixodes+ricinus+as+potential+vector+for+Usutu+virus&rft.jtitle=PLoS+neglected+tropical+diseases&rft.au=Bakker%2C+Julian+W&rft.au=M%C3%BCnger%2C+Emmanuelle&rft.au=Esser%2C+Helen+J&rft.au=Sikkema%2C+Reina+S&rft.date=2024-07-10&rft.eissn=1935-2735&rft.volume=18&rft.issue=7&rft.spage=e0012172&rft_id=info:doi/10.1371%2Fjournal.pntd.0012172&rft_id=info%3Apmid%2F38985837&rft.externalDocID=38985837
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1935-2735&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1935-2735&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1935-2735&client=summon