Two decades of Lloviu virus in Europe: knowns and unknowns about the European filovirus

Introduction: The Lloviu cuevavirus (LLOV) was the first filovirus identified in Europe and at the temperate climate region. Its first discovery was associated with a massive die-off event of Schreibers's bats in Spain. Since its discovery this virus became the second filovirus ever isolated di...

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Main Authors: Dr Gábor Kemenesi, Dr Zsófia Lanszki, Ágota Ábrahám, Dr Sándor A Boldogh, Dr Simon Scott, professor Nigel Temperton, Dr Edward Wright, Dr Pierre Nouvellet, Dr Stefania Leopardi, Dr Paola Di Benedictis, Dr Adam Hume, Dr Elke Mühlberger, Levente Sipos-Szabó, Dr Dávid Bajusz, Dr Heliana Dundarova, Dr Szilárd L Bücs, Dr Branka Bajić, Dr Ivana Budinski, Dr Štefan Matis, Dr Tamás Görföl
Format: Article
Language:English
Published: Elsevier 2025-03-01
Series:International Journal of Infectious Diseases
Online Access:http://www.sciencedirect.com/science/article/pii/S1201971224008270
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author Dr Gábor Kemenesi
Dr Zsófia Lanszki
Ágota Ábrahám
Dr Sándor A Boldogh
Dr Simon Scott
professor Nigel Temperton
Dr Edward Wright
Dr Pierre Nouvellet
Dr Stefania Leopardi
Dr Paola Di Benedictis
Dr Adam Hume
Dr Elke Mühlberger
Levente Sipos-Szabó
Dr Dávid Bajusz
Dr Heliana Dundarova
Dr Szilárd L Bücs
Dr Branka Bajić
Dr Ivana Budinski
Dr Štefan Matis
Dr Tamás Görföl
author_facet Dr Gábor Kemenesi
Dr Zsófia Lanszki
Ágota Ábrahám
Dr Sándor A Boldogh
Dr Simon Scott
professor Nigel Temperton
Dr Edward Wright
Dr Pierre Nouvellet
Dr Stefania Leopardi
Dr Paola Di Benedictis
Dr Adam Hume
Dr Elke Mühlberger
Levente Sipos-Szabó
Dr Dávid Bajusz
Dr Heliana Dundarova
Dr Szilárd L Bücs
Dr Branka Bajić
Dr Ivana Budinski
Dr Štefan Matis
Dr Tamás Görföl
author_sort Dr Gábor Kemenesi
collection DOAJ
description Introduction: The Lloviu cuevavirus (LLOV) was the first filovirus identified in Europe and at the temperate climate region. Its first discovery was associated with a massive die-off event of Schreibers's bats in Spain. Since its discovery this virus became the second filovirus ever isolated directly from bats. Initial in vitro experiments have suggested that this virus could be a potentially zoonotic filovirus and further experiments suggested an apathogenic nature in humans. During the last decades, several more die-off events in bats were associated with the virus, which therefore might be one of the few viruses pathogenic to bats under certain circumstances. Methods & Materials: We initiated a complex monitoring program for Lloviu virus in 2013. During the last decade we collected and screened more than 2000 blood samples with PCR and serology from eight countries. In addition to blood samples, we screened urine, faeces, swab and ectoparasites from these animals. Using a mobile laboratory approach, we collected fresh blood samples from infected animals on-site to facilitate in vitro isolation experiments. We used the SuBK12-08 cell line for the establishment of novel isolates. In parallel we analysed the ectoparasite samples with sequencing and histology to get a better understanding about their potential vector role. Results: We detected the viral RNA in all sample types, except oral swabs. We generated more than 20 novel viral genomic sequences, covering the whole coding region of the virus. We established four in vitro isolates. Using the sequence data, we generated throughout the years we performed molecular modelling to understand the temporal variation regarding its receptor affinity to bats and found no evidence of adaptation to better receptor binding. Additionally, we were able to calculate the molecular evolution of the virus, describe its mutational landscape and phylogenetic tree. Discussion: Over a decade of research activities, we now possess data that allow us to evaluate the hypothesis concerning the emerging versus enzootic nature of this virus in Europe. Based on the surveillance and sequence data we believe that this virus is endemic in the whole range of this bat species. We established a hypothesis about the potential connection of die-off events, Lloviu virus infection and hibernation of these animals. Conclusion: Although we generated significant amount of data regarding the ecology and zoonotic nature of this virus, several key questions remained to be solved. These include the investigation of potential spillover hosts, other potential bat host species and the role of ectoparasites in the natural transmission cycle. In conclusion, our efforts may lead to a deeper understanding of temperate climate filoviruses and, as a model, provide insights into the ecology and spillover mechanisms of highly pathogenic African filoviruses.
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spelling doaj-art-b5c4b5f3d2f5401cab5250eac168ac372025-08-20T02:54:52ZengElsevierInternational Journal of Infectious Diseases1201-97122025-03-0115210775210.1016/j.ijid.2024.107752Two decades of Lloviu virus in Europe: knowns and unknowns about the European filovirusDr Gábor Kemenesi0Dr Zsófia Lanszki1Ágota Ábrahám2Dr Sándor A Boldogh3Dr Simon Scott4professor Nigel Temperton5Dr Edward Wright6Dr Pierre Nouvellet7Dr Stefania Leopardi8Dr Paola Di Benedictis9Dr Adam Hume10Dr Elke Mühlberger11Levente Sipos-Szabó12Dr Dávid Bajusz13Dr Heliana Dundarova14Dr Szilárd L Bücs15Dr Branka Bajić16Dr Ivana Budinski17Dr Štefan Matis18Dr Tamás Görföl19National Laboratory Of Virology, Szentágothai Research Centre, University Of Pécs, Hungary; Faculty of Sciences, Institute of Biology, University of PécsNational Laboratory Of Virology, Szentágothai Research Centre, University Of Pécs, Hungary; Faculty of Sciences, Institute of Biology, University of PécsNational Laboratory Of Virology, Szentágothai Research Centre, University Of Pécs, HungaryAggtelek National Park DirectorateViral Pseudotype Unit, Medway School of Pharmacy, Chatham Maritime, Universities of Kent & GreenwichViral Pseudotype Unit, Medway School of Pharmacy, Chatham Maritime, Universities of Kent & GreenwichViral Pseudotype Unit, School of Life Sciences, University of SussexSchool of Life SciencesOIE Collaborating Centre and National Reference Centre for Infectious Diseases at the Animal‑Human Interface, Istituto Zooprofilattico Sperimentale delle VenezieOIE Collaborating Centre and National Reference Centre for Infectious Diseases at the Animal‑Human Interface, Istituto Zooprofilattico Sperimentale delle VenezieDepartment of Virology, Immunology and Microbiology, Boston University Chobanian & Avedisian School of MedicineDepartment of Virology, Immunology and Microbiology, Boston University Chobanian & Avedisian School of MedicineMedicinal Chemistry Research Group, HUN-REN Research Centre for Natural SciencesMedicinal Chemistry Research Group, HUN-REN Research Centre for Natural SciencesInstitute of Biodiversity and Ecosystem ResearchCentre for Bat Research and ConservationDepartment of Genetic Research, Institute for Biological Research “Siniša Stanković” – National Institute of the Republic of Serbia, University of BelgradeDepartment of Genetic Research, Institute for Biological Research “Siniša Stanković” – National Institute of the Republic of Serbia, University of BelgradeNational Park Slovak Karst DirectorateNational Laboratory Of Virology, Szentágothai Research Centre, University Of Pécs, HungaryIntroduction: The Lloviu cuevavirus (LLOV) was the first filovirus identified in Europe and at the temperate climate region. Its first discovery was associated with a massive die-off event of Schreibers's bats in Spain. Since its discovery this virus became the second filovirus ever isolated directly from bats. Initial in vitro experiments have suggested that this virus could be a potentially zoonotic filovirus and further experiments suggested an apathogenic nature in humans. During the last decades, several more die-off events in bats were associated with the virus, which therefore might be one of the few viruses pathogenic to bats under certain circumstances. Methods & Materials: We initiated a complex monitoring program for Lloviu virus in 2013. During the last decade we collected and screened more than 2000 blood samples with PCR and serology from eight countries. In addition to blood samples, we screened urine, faeces, swab and ectoparasites from these animals. Using a mobile laboratory approach, we collected fresh blood samples from infected animals on-site to facilitate in vitro isolation experiments. We used the SuBK12-08 cell line for the establishment of novel isolates. In parallel we analysed the ectoparasite samples with sequencing and histology to get a better understanding about their potential vector role. Results: We detected the viral RNA in all sample types, except oral swabs. We generated more than 20 novel viral genomic sequences, covering the whole coding region of the virus. We established four in vitro isolates. Using the sequence data, we generated throughout the years we performed molecular modelling to understand the temporal variation regarding its receptor affinity to bats and found no evidence of adaptation to better receptor binding. Additionally, we were able to calculate the molecular evolution of the virus, describe its mutational landscape and phylogenetic tree. Discussion: Over a decade of research activities, we now possess data that allow us to evaluate the hypothesis concerning the emerging versus enzootic nature of this virus in Europe. Based on the surveillance and sequence data we believe that this virus is endemic in the whole range of this bat species. We established a hypothesis about the potential connection of die-off events, Lloviu virus infection and hibernation of these animals. Conclusion: Although we generated significant amount of data regarding the ecology and zoonotic nature of this virus, several key questions remained to be solved. These include the investigation of potential spillover hosts, other potential bat host species and the role of ectoparasites in the natural transmission cycle. In conclusion, our efforts may lead to a deeper understanding of temperate climate filoviruses and, as a model, provide insights into the ecology and spillover mechanisms of highly pathogenic African filoviruses.http://www.sciencedirect.com/science/article/pii/S1201971224008270
spellingShingle Dr Gábor Kemenesi
Dr Zsófia Lanszki
Ágota Ábrahám
Dr Sándor A Boldogh
Dr Simon Scott
professor Nigel Temperton
Dr Edward Wright
Dr Pierre Nouvellet
Dr Stefania Leopardi
Dr Paola Di Benedictis
Dr Adam Hume
Dr Elke Mühlberger
Levente Sipos-Szabó
Dr Dávid Bajusz
Dr Heliana Dundarova
Dr Szilárd L Bücs
Dr Branka Bajić
Dr Ivana Budinski
Dr Štefan Matis
Dr Tamás Görföl
Two decades of Lloviu virus in Europe: knowns and unknowns about the European filovirus
International Journal of Infectious Diseases
title Two decades of Lloviu virus in Europe: knowns and unknowns about the European filovirus
title_full Two decades of Lloviu virus in Europe: knowns and unknowns about the European filovirus
title_fullStr Two decades of Lloviu virus in Europe: knowns and unknowns about the European filovirus
title_full_unstemmed Two decades of Lloviu virus in Europe: knowns and unknowns about the European filovirus
title_short Two decades of Lloviu virus in Europe: knowns and unknowns about the European filovirus
title_sort two decades of lloviu virus in europe knowns and unknowns about the european filovirus
url http://www.sciencedirect.com/science/article/pii/S1201971224008270
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