First evidence of transovarial transmission of Kyasanur Forest disease virus in Haemaphysalis and Rhipicephalus ticks in the wild

Abstract Background Kyasanur forest disease virus (KFDV) is a tick-borne flavivirus causing debilitating and potentially fatal disease in people in the Western Ghats region of India. The transmission cycle is complex, involving multiple vector and host species, but there are significant gaps in ecol...

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Main Authors: Sarah J. Burthe, Bhimanagoud Kumbar, Stefanie M. Schäfer, Bethan V. Purse, Abi T. Vanak, Natrajan Balakrishnan, Richard Hassall, Subhash L. Hoti, Darshan Narayanaswamy, Santoshkumar Potadar, Mujeeb Rahman, Mohammed Mudassar Chanda
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Language:English
Published: BMC 2025-01-01
Series:Parasites & Vectors
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Online Access:https://doi.org/10.1186/s13071-024-06643-5
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author Sarah J. Burthe
Bhimanagoud Kumbar
Stefanie M. Schäfer
Bethan V. Purse
Abi T. Vanak
Natrajan Balakrishnan
Richard Hassall
Subhash L. Hoti
Darshan Narayanaswamy
Santoshkumar Potadar
Mujeeb Rahman
Mohammed Mudassar Chanda
author_facet Sarah J. Burthe
Bhimanagoud Kumbar
Stefanie M. Schäfer
Bethan V. Purse
Abi T. Vanak
Natrajan Balakrishnan
Richard Hassall
Subhash L. Hoti
Darshan Narayanaswamy
Santoshkumar Potadar
Mujeeb Rahman
Mohammed Mudassar Chanda
author_sort Sarah J. Burthe
collection DOAJ
description Abstract Background Kyasanur forest disease virus (KFDV) is a tick-borne flavivirus causing debilitating and potentially fatal disease in people in the Western Ghats region of India. The transmission cycle is complex, involving multiple vector and host species, but there are significant gaps in ecological knowledge. Empirical data on pathogen-vector-host interactions and incrimination have not been updated since the last century, despite significant local changes in land use and the expansion of KFD to new areas. Mathematical models predict that transovarial transmission, whereby adult female ticks pass KFDV infections to their offspring, plays an important role in the persistence of KFD, but this has not been shown in the wild. Here we set out to establish whether transovarial transmission of KFDV was occurring under natural field conditions by assessing whether host-seeking larvae were positive for KFDV. Methods Ticks were sampled by dragging and flagging across a broad range of habitats within the agro-forest matrix at 49 sites in two districts: Shivamogga, Karnataka and Wayanad, Kerala (September 2018-March 2019), and larvae were tested for KFDV by PCR. Results In total, larval ticks from 7 of the 49 sites sampled tested positive for KFDV, indicating that transovarial transmission is occurring. Of the 13 KFDV-positive larval samples, 3 came from around houses and gardens, 5 from crops (3 from harvested rice paddy and 2 from areca plantation), 1 from teak plantation and 4 (2 from 1 transect) from forests. Five different tick species were found to have KFDV-positive larvae: Haemaphysalis spinigera, H. bispinosa, Rhipicephalus annulatus, R. microplus and an unidentifiable species of Haemaphysalis (no close match in GenBank). Conclusions Our empirical confirmation of transovarial transmission has important implications for understanding and predicting KFD dynamics, suggesting that ticks may act as a reservoir for KFDV. Moreover, small mammals and cattle may play crucial roles in transmission if small mammals are the main hosts for larvae infected via transovarial transmission, and cattle support large numbers of infected female adult ticks. This first report of transovarial transmission of KFDV, and within a hitherto undescribed range of vectors and habitats, will help disease managers improve KFD surveillance and mitigation strategies, ultimately leading to communities becoming more resilient to the risk of this tick-transmitted disease. Graphical Abstract
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spelling doaj-art-9a5717561d3f42b6b0475e6c7324e86c2025-01-19T12:12:11ZengBMCParasites & Vectors1756-33052025-01-0118111010.1186/s13071-024-06643-5First evidence of transovarial transmission of Kyasanur Forest disease virus in Haemaphysalis and Rhipicephalus ticks in the wildSarah J. Burthe0Bhimanagoud Kumbar1Stefanie M. Schäfer2Bethan V. Purse3Abi T. Vanak4Natrajan Balakrishnan5Richard Hassall6Subhash L. Hoti7Darshan Narayanaswamy8Santoshkumar Potadar9Mujeeb Rahman10Mohammed Mudassar Chanda11UK Centre for Ecology & HydrologyICAR-National Institute of Veterinary Epidemiology and Disease InformaticsUK Centre for Ecology & HydrologyUK Centre for Ecology & HydrologyAshoka Trust for Research in Ecology and the EnvironmentICAR-National Institute of Veterinary Epidemiology and Disease InformaticsUK Centre for Ecology & HydrologyICMR-Vector Control Research CentreVirus Diagnostic Laboratory, Department of Health and Family Welfare Services, Government of KarnatakaICMR-National Institute of Traditional MedicineAshoka Trust for Research in Ecology and the EnvironmentICAR-National Institute of Veterinary Epidemiology and Disease InformaticsAbstract Background Kyasanur forest disease virus (KFDV) is a tick-borne flavivirus causing debilitating and potentially fatal disease in people in the Western Ghats region of India. The transmission cycle is complex, involving multiple vector and host species, but there are significant gaps in ecological knowledge. Empirical data on pathogen-vector-host interactions and incrimination have not been updated since the last century, despite significant local changes in land use and the expansion of KFD to new areas. Mathematical models predict that transovarial transmission, whereby adult female ticks pass KFDV infections to their offspring, plays an important role in the persistence of KFD, but this has not been shown in the wild. Here we set out to establish whether transovarial transmission of KFDV was occurring under natural field conditions by assessing whether host-seeking larvae were positive for KFDV. Methods Ticks were sampled by dragging and flagging across a broad range of habitats within the agro-forest matrix at 49 sites in two districts: Shivamogga, Karnataka and Wayanad, Kerala (September 2018-March 2019), and larvae were tested for KFDV by PCR. Results In total, larval ticks from 7 of the 49 sites sampled tested positive for KFDV, indicating that transovarial transmission is occurring. Of the 13 KFDV-positive larval samples, 3 came from around houses and gardens, 5 from crops (3 from harvested rice paddy and 2 from areca plantation), 1 from teak plantation and 4 (2 from 1 transect) from forests. Five different tick species were found to have KFDV-positive larvae: Haemaphysalis spinigera, H. bispinosa, Rhipicephalus annulatus, R. microplus and an unidentifiable species of Haemaphysalis (no close match in GenBank). Conclusions Our empirical confirmation of transovarial transmission has important implications for understanding and predicting KFD dynamics, suggesting that ticks may act as a reservoir for KFDV. Moreover, small mammals and cattle may play crucial roles in transmission if small mammals are the main hosts for larvae infected via transovarial transmission, and cattle support large numbers of infected female adult ticks. This first report of transovarial transmission of KFDV, and within a hitherto undescribed range of vectors and habitats, will help disease managers improve KFD surveillance and mitigation strategies, ultimately leading to communities becoming more resilient to the risk of this tick-transmitted disease. Graphical Abstracthttps://doi.org/10.1186/s13071-024-06643-5Monkey FeverZoonotic diseasesTick-borne pathogenEmerging infection
spellingShingle Sarah J. Burthe
Bhimanagoud Kumbar
Stefanie M. Schäfer
Bethan V. Purse
Abi T. Vanak
Natrajan Balakrishnan
Richard Hassall
Subhash L. Hoti
Darshan Narayanaswamy
Santoshkumar Potadar
Mujeeb Rahman
Mohammed Mudassar Chanda
First evidence of transovarial transmission of Kyasanur Forest disease virus in Haemaphysalis and Rhipicephalus ticks in the wild
Parasites & Vectors
Monkey Fever
Zoonotic diseases
Tick-borne pathogen
Emerging infection
title First evidence of transovarial transmission of Kyasanur Forest disease virus in Haemaphysalis and Rhipicephalus ticks in the wild
title_full First evidence of transovarial transmission of Kyasanur Forest disease virus in Haemaphysalis and Rhipicephalus ticks in the wild
title_fullStr First evidence of transovarial transmission of Kyasanur Forest disease virus in Haemaphysalis and Rhipicephalus ticks in the wild
title_full_unstemmed First evidence of transovarial transmission of Kyasanur Forest disease virus in Haemaphysalis and Rhipicephalus ticks in the wild
title_short First evidence of transovarial transmission of Kyasanur Forest disease virus in Haemaphysalis and Rhipicephalus ticks in the wild
title_sort first evidence of transovarial transmission of kyasanur forest disease virus in haemaphysalis and rhipicephalus ticks in the wild
topic Monkey Fever
Zoonotic diseases
Tick-borne pathogen
Emerging infection
url https://doi.org/10.1186/s13071-024-06643-5
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