Evidence for overwintering and autochthonous transmission of Usutu virus to wild birds following its redetection in the United Kingdom

Arran J. Folly; Sanam Sewgobind; Luis M. Hernández-Triana; Karen L. Mansfield; Fabian Z.X. Lean; Becki Lawson; Katharina Seilern-Moy; Andrew A. Cunningham; Simon Spiro; Ethan Wrigglesworth; Paul Pearce-Kelly; Trent Herdman; Colin Johnston; Morgan Berrell; Alexander G.C. Vaux; Jolyon M. Medlock; Nicholas Johnson

doi:10.1111/tbed.14738

Evidence for overwintering and autochthonous transmission of Usutu virus to wild birds following its redetection in the United Kingdom

Arran J. Folly^*, Sanam Sewgobind, Luis M. Hernández-Triana, Karen L. Mansfield, Fabian Z.X. Lean, Becki Lawson, Katharina Seilern-Moy, Andrew A. Cunningham, Simon Spiro, Ethan Wrigglesworth, Paul Pearce-Kelly, Trent Herdman, Colin Johnston, Morgan Berrell, Alexander G.C. Vaux, Jolyon M. Medlock, Nicholas Johnson

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

Abstract

Usutu virus (USUV) is an emerging zoonotic arbovirus in Europe, where it primarily impacts Eurasian blackbirds (Turdus merula). For mosquito-borne viruses to persist in temperate areas, transovarial transmission in vectors or overwintering in either hosts or diapausing vectors must occur to facilitate autochthonous transmission. We undertook surveillance of hosts and vectors in 2021 to elucidate whether USUV had overwintered in the United Kingdom (UK) following its initial detection there in 2020. From 175 dead bird submissions, we detected 1 case of USUV infection, in a blackbird, from which a full USUV genome was derived. Using a molecular clock analysis, we demonstrate that the 2021 detection shared a most recent common ancestor with the 2020 Greater London, UK, USUV sequence. In addition, we identified USUV-specific neutralizing antibodies in 10 out of 86 serum samples taken from captive birds at the index site, demonstrating in situ cryptic infection and potential sustained transmission. However, from 4966 mosquitoes, we detected no USUV RNA suggesting that prevalence in the vector community was absent or low during sampling. Combined, these results suggest that USUV overwintered in the UK, thus providing empirical evidence for the continued northward expansion of this vector-borne viral disease. Currently, our detection indicates geographically restricted virus persistence. Further detections over time will be required to demonstrate long-term establishment. It remains unclear whether the UK, and by extension other high-latitude regions, can support endemic USUV infection.

Original language	English
Pages (from-to)	3684-3692
Number of pages	9
Journal	Transboundary and Emerging Diseases
Volume	69
Issue number	6
DOIs	https://doi.org/10.1111/tbed.14738
Publication status	Published - Nov 2022
Externally published	Yes

Bibliographical note

Funding Information:
The authors would like to thank members of the public and participants in the British Trust for Ornithology's Garden BirdWatch scheme, who report to the Garden Wildlife Health project (www.gardenwildilfehealth.org); APHA regional laboratories, the Predatory Bird Monitoring Scheme and the Institute of Zoology's Disease Risk Analysis and Health Surveillance project, for wild bird submissions to the GB flavivirus surveillance scheme. The authors would also like to thank Sophie Myers and Sophie Harding for assisting with mosquito collection, histology scientists at APHA for performing IHC and the Protein Expression Facility, University of Queensland, Australia for producing the Kunjin NS1 protein for the generation of polyclonal antiserum. This study was supported by grants SV3045 and SE0560 from Department for Environment, Food & Rural Affairs (Defra) and the Devolved Administrations of Scotland and Wales and the European Union Horizon 2020 Research and Innovation Program under grant agreement No. 871029 EVA-GLOBAL. Financial support for the Garden Wildlife Health project comes in part from the Defra, the Welsh Government and the APHA Diseases of Wildlife Scheme Scanning Surveillance Programme (Project ED1058), and from the Garfield Weston Foundation and the Universities Federation for Animal Welfare. BL and AAC receive financial support from Research England.

Funding Information:
The authors would like to thank members of the public and participants in the British Trust for Ornithology's Garden BirdWatch scheme, who report to the Garden Wildlife Health project ( www.gardenwildilfehealth.org ); APHA regional laboratories, the Predatory Bird Monitoring Scheme and the Institute of Zoology's Disease Risk Analysis and Health Surveillance project, for wild bird submissions to the GB flavivirus surveillance scheme. The authors would also like to thank Sophie Myers and Sophie Harding for assisting with mosquito collection, histology scientists at APHA for performing IHC and the Protein Expression Facility, University of Queensland, Australia for producing the Kunjin NS1 protein for the generation of polyclonal antiserum. This study was supported by grants SV3045 and SE0560 from Department for Environment, Food & Rural Affairs (Defra) and the Devolved Administrations of Scotland and Wales and the European Union Horizon 2020 Research and Innovation Program under grant agreement No. 871029 EVA‐GLOBAL. Financial support for the Garden Wildlife Health project comes in part from the Defra, the Welsh Government and the APHA Diseases of Wildlife Scheme Scanning Surveillance Programme (Project ED1058), and from the Garfield Weston Foundation and the Universities Federation for Animal Welfare. BL and AAC receive financial support from Research England.

Publisher Copyright:
© 2022 The Authors. Transboundary and Emerging Diseases published by Wiley-VCH GmbH.

Keywords

Culex pipiens
Flavivirus
Turdus merula
emerging infectious disease
molecular clock
mosquito-borne disease

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.1111/tbed.14738

Cite this

Folly, A. J., Sewgobind, S., Hernández-Triana, L. M., Mansfield, K. L., Lean, F. Z. X., Lawson, B., Seilern-Moy, K., Cunningham, A. A., Spiro, S., Wrigglesworth, E., Pearce-Kelly, P., Herdman, T., Johnston, C., Berrell, M., Vaux, A. G. C., Medlock, J. M., & Johnson, N. (2022). Evidence for overwintering and autochthonous transmission of Usutu virus to wild birds following its redetection in the United Kingdom. Transboundary and Emerging Diseases, 69(6), 3684-3692. https://doi.org/10.1111/tbed.14738

@article{db2b234e24a54ee9a219778cce64a39b,

title = "Evidence for overwintering and autochthonous transmission of Usutu virus to wild birds following its redetection in the United Kingdom",

abstract = "Usutu virus (USUV) is an emerging zoonotic arbovirus in Europe, where it primarily impacts Eurasian blackbirds (Turdus merula). For mosquito-borne viruses to persist in temperate areas, transovarial transmission in vectors or overwintering in either hosts or diapausing vectors must occur to facilitate autochthonous transmission. We undertook surveillance of hosts and vectors in 2021 to elucidate whether USUV had overwintered in the United Kingdom (UK) following its initial detection there in 2020. From 175 dead bird submissions, we detected 1 case of USUV infection, in a blackbird, from which a full USUV genome was derived. Using a molecular clock analysis, we demonstrate that the 2021 detection shared a most recent common ancestor with the 2020 Greater London, UK, USUV sequence. In addition, we identified USUV-specific neutralizing antibodies in 10 out of 86 serum samples taken from captive birds at the index site, demonstrating in situ cryptic infection and potential sustained transmission. However, from 4966 mosquitoes, we detected no USUV RNA suggesting that prevalence in the vector community was absent or low during sampling. Combined, these results suggest that USUV overwintered in the UK, thus providing empirical evidence for the continued northward expansion of this vector-borne viral disease. Currently, our detection indicates geographically restricted virus persistence. Further detections over time will be required to demonstrate long-term establishment. It remains unclear whether the UK, and by extension other high-latitude regions, can support endemic USUV infection.",

keywords = "Culex pipiens, Flavivirus, Turdus merula, emerging infectious disease, molecular clock, mosquito-borne disease",

author = "Folly, {Arran J.} and Sanam Sewgobind and Hern{\'a}ndez-Triana, {Luis M.} and Mansfield, {Karen L.} and Lean, {Fabian Z.X.} and Becki Lawson and Katharina Seilern-Moy and Cunningham, {Andrew A.} and Simon Spiro and Ethan Wrigglesworth and Paul Pearce-Kelly and Trent Herdman and Colin Johnston and Morgan Berrell and Vaux, {Alexander G.C.} and Medlock, {Jolyon M.} and Nicholas Johnson",

note = "Funding Information: The authors would like to thank members of the public and participants in the British Trust for Ornithology's Garden BirdWatch scheme, who report to the Garden Wildlife Health project (www.gardenwildilfehealth.org); APHA regional laboratories, the Predatory Bird Monitoring Scheme and the Institute of Zoology's Disease Risk Analysis and Health Surveillance project, for wild bird submissions to the GB flavivirus surveillance scheme. The authors would also like to thank Sophie Myers and Sophie Harding for assisting with mosquito collection, histology scientists at APHA for performing IHC and the Protein Expression Facility, University of Queensland, Australia for producing the Kunjin NS1 protein for the generation of polyclonal antiserum. This study was supported by grants SV3045 and SE0560 from Department for Environment, Food & Rural Affairs (Defra) and the Devolved Administrations of Scotland and Wales and the European Union Horizon 2020 Research and Innovation Program under grant agreement No. 871029 EVA-GLOBAL. Financial support for the Garden Wildlife Health project comes in part from the Defra, the Welsh Government and the APHA Diseases of Wildlife Scheme Scanning Surveillance Programme (Project ED1058), and from the Garfield Weston Foundation and the Universities Federation for Animal Welfare. BL and AAC receive financial support from Research England. Funding Information: The authors would like to thank members of the public and participants in the British Trust for Ornithology's Garden BirdWatch scheme, who report to the Garden Wildlife Health project ( www.gardenwildilfehealth.org ); APHA regional laboratories, the Predatory Bird Monitoring Scheme and the Institute of Zoology's Disease Risk Analysis and Health Surveillance project, for wild bird submissions to the GB flavivirus surveillance scheme. The authors would also like to thank Sophie Myers and Sophie Harding for assisting with mosquito collection, histology scientists at APHA for performing IHC and the Protein Expression Facility, University of Queensland, Australia for producing the Kunjin NS1 protein for the generation of polyclonal antiserum. This study was supported by grants SV3045 and SE0560 from Department for Environment, Food & Rural Affairs (Defra) and the Devolved Administrations of Scotland and Wales and the European Union Horizon 2020 Research and Innovation Program under grant agreement No. 871029 EVA‐GLOBAL. Financial support for the Garden Wildlife Health project comes in part from the Defra, the Welsh Government and the APHA Diseases of Wildlife Scheme Scanning Surveillance Programme (Project ED1058), and from the Garfield Weston Foundation and the Universities Federation for Animal Welfare. BL and AAC receive financial support from Research England. Publisher Copyright: {\textcopyright} 2022 The Authors. Transboundary and Emerging Diseases published by Wiley-VCH GmbH.",

year = "2022",

month = nov,

doi = "10.1111/tbed.14738",

language = "English",

volume = "69",

pages = "3684--3692",

journal = "Transboundary and Emerging Diseases",

issn = "1865-1674",

publisher = "wiley",

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Folly, AJ, Sewgobind, S, Hernández-Triana, LM, Mansfield, KL, Lean, FZX, Lawson, B, Seilern-Moy, K, Cunningham, AA, Spiro, S, Wrigglesworth, E, Pearce-Kelly, P, Herdman, T, Johnston, C, Berrell, M, Vaux, AGC , Medlock, JM & Johnson, N 2022, 'Evidence for overwintering and autochthonous transmission of Usutu virus to wild birds following its redetection in the United Kingdom', Transboundary and Emerging Diseases, vol. 69, no. 6, pp. 3684-3692. https://doi.org/10.1111/tbed.14738

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T1 - Evidence for overwintering and autochthonous transmission of Usutu virus to wild birds following its redetection in the United Kingdom

AU - Folly, Arran J.

AU - Sewgobind, Sanam

AU - Hernández-Triana, Luis M.

AU - Mansfield, Karen L.

AU - Lean, Fabian Z.X.

AU - Lawson, Becki

AU - Seilern-Moy, Katharina

AU - Cunningham, Andrew A.

AU - Spiro, Simon

AU - Wrigglesworth, Ethan

AU - Pearce-Kelly, Paul

AU - Herdman, Trent

AU - Johnston, Colin

AU - Berrell, Morgan

AU - Vaux, Alexander G.C.

AU - Medlock, Jolyon M.

AU - Johnson, Nicholas

N1 - Funding Information: The authors would like to thank members of the public and participants in the British Trust for Ornithology's Garden BirdWatch scheme, who report to the Garden Wildlife Health project (www.gardenwildilfehealth.org); APHA regional laboratories, the Predatory Bird Monitoring Scheme and the Institute of Zoology's Disease Risk Analysis and Health Surveillance project, for wild bird submissions to the GB flavivirus surveillance scheme. The authors would also like to thank Sophie Myers and Sophie Harding for assisting with mosquito collection, histology scientists at APHA for performing IHC and the Protein Expression Facility, University of Queensland, Australia for producing the Kunjin NS1 protein for the generation of polyclonal antiserum. This study was supported by grants SV3045 and SE0560 from Department for Environment, Food & Rural Affairs (Defra) and the Devolved Administrations of Scotland and Wales and the European Union Horizon 2020 Research and Innovation Program under grant agreement No. 871029 EVA-GLOBAL. Financial support for the Garden Wildlife Health project comes in part from the Defra, the Welsh Government and the APHA Diseases of Wildlife Scheme Scanning Surveillance Programme (Project ED1058), and from the Garfield Weston Foundation and the Universities Federation for Animal Welfare. BL and AAC receive financial support from Research England. Funding Information: The authors would like to thank members of the public and participants in the British Trust for Ornithology's Garden BirdWatch scheme, who report to the Garden Wildlife Health project ( www.gardenwildilfehealth.org ); APHA regional laboratories, the Predatory Bird Monitoring Scheme and the Institute of Zoology's Disease Risk Analysis and Health Surveillance project, for wild bird submissions to the GB flavivirus surveillance scheme. The authors would also like to thank Sophie Myers and Sophie Harding for assisting with mosquito collection, histology scientists at APHA for performing IHC and the Protein Expression Facility, University of Queensland, Australia for producing the Kunjin NS1 protein for the generation of polyclonal antiserum. This study was supported by grants SV3045 and SE0560 from Department for Environment, Food & Rural Affairs (Defra) and the Devolved Administrations of Scotland and Wales and the European Union Horizon 2020 Research and Innovation Program under grant agreement No. 871029 EVA‐GLOBAL. Financial support for the Garden Wildlife Health project comes in part from the Defra, the Welsh Government and the APHA Diseases of Wildlife Scheme Scanning Surveillance Programme (Project ED1058), and from the Garfield Weston Foundation and the Universities Federation for Animal Welfare. BL and AAC receive financial support from Research England. Publisher Copyright: © 2022 The Authors. Transboundary and Emerging Diseases published by Wiley-VCH GmbH.

PY - 2022/11

Y1 - 2022/11

N2 - Usutu virus (USUV) is an emerging zoonotic arbovirus in Europe, where it primarily impacts Eurasian blackbirds (Turdus merula). For mosquito-borne viruses to persist in temperate areas, transovarial transmission in vectors or overwintering in either hosts or diapausing vectors must occur to facilitate autochthonous transmission. We undertook surveillance of hosts and vectors in 2021 to elucidate whether USUV had overwintered in the United Kingdom (UK) following its initial detection there in 2020. From 175 dead bird submissions, we detected 1 case of USUV infection, in a blackbird, from which a full USUV genome was derived. Using a molecular clock analysis, we demonstrate that the 2021 detection shared a most recent common ancestor with the 2020 Greater London, UK, USUV sequence. In addition, we identified USUV-specific neutralizing antibodies in 10 out of 86 serum samples taken from captive birds at the index site, demonstrating in situ cryptic infection and potential sustained transmission. However, from 4966 mosquitoes, we detected no USUV RNA suggesting that prevalence in the vector community was absent or low during sampling. Combined, these results suggest that USUV overwintered in the UK, thus providing empirical evidence for the continued northward expansion of this vector-borne viral disease. Currently, our detection indicates geographically restricted virus persistence. Further detections over time will be required to demonstrate long-term establishment. It remains unclear whether the UK, and by extension other high-latitude regions, can support endemic USUV infection.

AB - Usutu virus (USUV) is an emerging zoonotic arbovirus in Europe, where it primarily impacts Eurasian blackbirds (Turdus merula). For mosquito-borne viruses to persist in temperate areas, transovarial transmission in vectors or overwintering in either hosts or diapausing vectors must occur to facilitate autochthonous transmission. We undertook surveillance of hosts and vectors in 2021 to elucidate whether USUV had overwintered in the United Kingdom (UK) following its initial detection there in 2020. From 175 dead bird submissions, we detected 1 case of USUV infection, in a blackbird, from which a full USUV genome was derived. Using a molecular clock analysis, we demonstrate that the 2021 detection shared a most recent common ancestor with the 2020 Greater London, UK, USUV sequence. In addition, we identified USUV-specific neutralizing antibodies in 10 out of 86 serum samples taken from captive birds at the index site, demonstrating in situ cryptic infection and potential sustained transmission. However, from 4966 mosquitoes, we detected no USUV RNA suggesting that prevalence in the vector community was absent or low during sampling. Combined, these results suggest that USUV overwintered in the UK, thus providing empirical evidence for the continued northward expansion of this vector-borne viral disease. Currently, our detection indicates geographically restricted virus persistence. Further detections over time will be required to demonstrate long-term establishment. It remains unclear whether the UK, and by extension other high-latitude regions, can support endemic USUV infection.

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KW - Flavivirus

KW - Turdus merula

KW - emerging infectious disease

KW - molecular clock

KW - mosquito-borne disease

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DO - 10.1111/tbed.14738

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JO - Transboundary and Emerging Diseases

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ER -

Evidence for overwintering and autochthonous transmission of Usutu virus to wild birds following its redetection in the United Kingdom

Abstract

Bibliographical note

Keywords

UN SDGs

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