Cross-Sectional Study on the Prevalence and Factors Influencing Occurrence of Tick-Borne Encephalitis in Horses in Lithuania.
Abstract: Various animal species have been evaluated in depth for their potential as Tick-borne encephalitis virus (TBEV) sentinel species, although evidence for equine capacity is incomplete. Therefore, a comprehensive cross-sectional stratified serosurvey and PCR analysis of selected horses ( = 301) were performed in TBEV endemic localities in Lithuania. Attached and moving ticks ( = 241) have been collected from aforementioned hosts to evaluate natural infectivity of TBEV vectors () in the recreational environments surrounding equestrian centers. All samples were screened for TBEV IgG and positive samples were confirmed by virus neutralization test (VNT). 113 (37.5%) horses from all counties of Lithuania tested positive for TBEV IgG, revealing age and sex indifferent results of equine seroprevalence that were significantly dependent on pedigree: horses of mixed breed were more susceptible to infection possibly due to their management practices. TBEV prevalence in equine species corresponded to TBEV-confirmed human cases in the precedent year. As much as 3.9% of horses were viraemic with TBEV-RNA with subsequent confirmation of TBEV European subtype. 4/38 of tested tick pools were positive for TBEV-RNA (Minimal infectious rate 1.2%). Several unknown microfoci were revealed during the study indicating areas of extreme risk close to popular human entertainment sites. The study provides important evidence in favor of horses' usage as sentinel species, as equines could provide more detailed epidemiological mapping of TBEV, as well as more efficient collection of ticks for surveillance studies.
Publication Date: 2021-01-31 PubMed ID: 33572628PubMed Central: PMC7911650DOI: 10.3390/pathogens10020140Google Scholar: Lookup
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- Journal Article
Summary
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The research paper focuses on the investigation and analysis of the prevalence of Tick-Borne Encephalitis Virus (TBEV) in horses, and how these animals could potentially be used as indicator or “sentinel” species for monitoring the spread of the disease.
Study Design and Procedure
- This is a cross-sectional study that examined and tested 301 horses from various TBEV-endemic localities in Lithuania. They also investigated 241 ticks that were either attached to or found moving on these horses. The research was aimed at evaluating the natural infectivity of TBEV vectors (i.e., ticks).
- The horses and ticks were tested for the presence of TBEV Immunoglobulin G (IgG) antibodies and those that were positive were further confirmed by a virus neutralization test (VNT).
Study Findings
- The study revealed that 37.5% of the horses from all counties in Lithuania tested positive for TBEV IgG. The susceptibility of horses to the infection did not depend on their age or sex, but was significantly tied to their breed. Specifically, the study found that mixed breed horses were more predisposed to TBEV infection, possibly due to their management practices.
- The research also found that the prevalence of TBEV in horses corresponded with the number of confirmed human TBEV cases in the previous year, indicating that the virus is similarly distributed in both human and equine populations.
- Additionally, the study revealed that 3.9% of the horses were viremic, meaning they had the virus in their bloodstream. The TBEV present was confirmed as the European subtype.
- Of the tested tick pools, 4 out of 38 were positive for TBEV, indicating an infection rate of 1.2%. The study also uncovered several unknown microfoci of TBEV, which are areas of extreme risk that are close to human entertainment sites.
Implications of the findings
- The findings indicate that horses can be used as sentinel species for TBEV. By monitoring equine populations, scientists could develop a more detailed and localized epidemiological map of TBEV and track its spread in real-time.
- On top of that, the use of horses for tick collection could make surveillance studies more effective and efficient.
Cite This Article
APA
Pautienius A, Armonaite A, Simkute E, Zagrabskaite R, Buitkuviene J, Alpizar-Jara R, Grigas J, Zakiene I, Zienius D, Salomskas A, Stankevicius A.
(2021).
Cross-Sectional Study on the Prevalence and Factors Influencing Occurrence of Tick-Borne Encephalitis in Horses in Lithuania.
Pathogens, 10(2), 140.
https://doi.org/10.3390/pathogens10020140 Publication
Researcher Affiliations
- Virology Laboratory, Institute of Microbiology and Virology, Faculty of Veterinary Medicine, Lithuanian University of Health Sciences, Tilzes str. 18, LT-47181 Kaunas, Lithuania.
- Laboratory of Immunology, Department of Anatomy and Physiology, Faculty of Veterinary Medicine, Lithuanian University of Health Sciences, Tilzes str. 18, LT-47181 Kaunas, Lithuania.
- Laboratory of Immunology, Department of Anatomy and Physiology, Faculty of Veterinary Medicine, Lithuanian University of Health Sciences, Tilzes str. 18, LT-47181 Kaunas, Lithuania.
- Laboratory of Immunology, Department of Anatomy and Physiology, Faculty of Veterinary Medicine, Lithuanian University of Health Sciences, Tilzes str. 18, LT-47181 Kaunas, Lithuania.
- National Food and Veterinary Risk Assessment Institute, J. Kairiukscio Str. 10, LT-08409 Vilnius, Lithuania.
- National Food and Veterinary Risk Assessment Institute, J. Kairiukscio Str. 10, LT-08409 Vilnius, Lithuania.
- Research Center in Mathematics and Applications (CIMA-UE), Institute for Advanced Studies and Research, Department of Mathematics, School of Science and Technology, University of Évora, Rua Romão Ramalho 59, 7000-671 Évora, Portugal.
- Virology Laboratory, Institute of Microbiology and Virology, Faculty of Veterinary Medicine, Lithuanian University of Health Sciences, Tilzes str. 18, LT-47181 Kaunas, Lithuania.
- Laboratory of Immunology, Department of Anatomy and Physiology, Faculty of Veterinary Medicine, Lithuanian University of Health Sciences, Tilzes str. 18, LT-47181 Kaunas, Lithuania.
- Laboratory of Immunology, Department of Anatomy and Physiology, Faculty of Veterinary Medicine, Lithuanian University of Health Sciences, Tilzes str. 18, LT-47181 Kaunas, Lithuania.
- Department of Veterinary Pathobiology, Faculty of Veterinary Medicine Lithuanian University of Health Sciences, Tilzes str. 18, LT-47181 Kaunas, Lithuania.
- Department of Veterinary Pathobiology, Faculty of Veterinary Medicine Lithuanian University of Health Sciences, Tilzes str. 18, LT-47181 Kaunas, Lithuania.
- Laboratory of Immunology, Department of Anatomy and Physiology, Faculty of Veterinary Medicine, Lithuanian University of Health Sciences, Tilzes str. 18, LT-47181 Kaunas, Lithuania.
Grant Funding
- MT-18-5 / Funded by Ministry of Agriculture of the Republic Lithuania
Conflict of Interest Statement
The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.
References
This article includes 37 references
- Süss J. Tick-borne encephalitis 2010: epidemiology, risk areas, and virus strains in Europe and Asia-an overview.. Ticks Tick Borne Dis 2011 Mar;2(1):2-15.
- Radzišauskienė D, Žagminas K, Ašoklienė L, Jasionis A, Mameniškienė R, Ambrozaitis A, Jančorienė L, Jatužis D, Petraitytė I, Mockienė E. Epidemiological patterns of tick-borne encephalitis in Lithuania and clinical features in adults in the light of the high incidence in recent years: a retrospective study.. Eur J Neurol 2018 Feb;25(2):268-274.
- European Centre for Disease Prevention and Control. Tick-Borne Encephalitis—Annual Epidemiological Report for 2018. 2019.
- European Centre for Disease Prevention and Control. Country Profile: Lithuania. Tick-Borne Encephalitis (TBE). 2012.
- Lindquist L. Tick-borne encephalitis.. Handb Clin Neurol 2014;123:531-59.
- Imhoff M, Hagedorn P, Schulze Y, Hellenbrand W, Pfeffer M, Niedrig M. Review: Sentinels of tick-borne encephalitis risk.. Ticks Tick Borne Dis 2015 Jul;6(5):592-600.
- Gerth HJ, Grimshandl D, Stage B, Döller G, Kunz C. Roe deer as sentinels for endemicity of tick-borne encephalitis virus.. Epidemiol Infect 1995 Oct;115(2):355-65.
- Achazi K, Růžek D, Donoso-Mantke O, Schlegel M, Ali HS, Wenk M, Schmidt-Chanasit J, Ohlmeyer L, Rühe F, Vor T, Kiffner C, Kallies R, Ulrich RG, Niedrig M. Rodents as sentinels for the prevalence of tick-borne encephalitis virus.. Vector Borne Zoonotic Dis 2011 Jun;11(6):641-7.
- Knap N, Korva M, Dolinšek V, Sekirnik M, Trilar T, Avšič-Županc T. Patterns of tick-borne encephalitis virus infection in rodents in Slovenia.. Vector Borne Zoonotic Dis 2012 Mar;12(3):236-42.
- Klaus C, Beer M, Saier R, Schau U, Moog U, Hoffmann B, Diller R, Süss J. Goats and sheep as sentinels for tick-borne encephalitis (TBE) virus--epidemiological studies in areas endemic and non-endemic for TBE virus in Germany.. Ticks Tick Borne Dis 2012 Feb;3(1):27-37.
- Klaus C, Hoffmann B, Beer M, Müller W, Stark B, Bader W, Stiasny K, Heinz FX, Süss J. Seroprevalence of tick-borne encephalitis (TBE) in naturally exposed monkeys (Macaca sylvanus) and sheep and prevalence of TBE virus in ticks in a TBE endemic area in Germany.. Ticks Tick Borne Dis 2010 Sep;1(3):141-4.
- Lindhe KE, Meldgaard DS, Jensen PM, Houser GA, Berendt M. Prevalence of tick-borne encephalitis virus antibodies in dogs from Denmark.. Acta Vet Scand 2009 Dec 29;51(1):56.
- Duscher GG, Wetscher M, Baumgartner R, Walder G. Roe deer sera used for TBE surveillance in Austria.. Ticks Tick Borne Dis 2015 Jun;6(4):489-93.
- Klaus C, Hörügel U, Hoffmann B, Beer M. Tick-borne encephalitis virus (TBEV) infection in horses: clinical and laboratory findings and epidemiological investigations.. Vet Microbiol 2013 May 3;163(3-4):368-72.
- Rushton JO, Lecollinet S, Hubálek Z, Svobodová P, Lussy H, Nowotny N. Tick-borne encephalitis virus in horses, Austria, 2011.. Emerg Infect Dis 2013 Apr;19(4):635-7.
- Müller K, König M, Thiel HJ. [Tick-borne encephalitis (TBE) with special emphasis on infection in horses].. Dtsch Tierarztl Wochenschr 2006 Apr;113(4):147-51.
- Setia MS. Methodology Series Module 3: Cross-sectional Studies.. Indian J Dermatol 2016 May-Jun;61(3):261-4.
- . VIII-500 Lietuvos Respublikos Gyvūnų Gerovės ir Apsaugos Įstatymas. Žin. 2012, Nr. 122-6126.
- Holzmann H, Kundi M, Stiasny K, Clement J, McKenna P, Kunz C, Heinz FX. Correlation between ELISA, hemagglutination inhibition, and neutralization tests after vaccination against tick-borne encephalitis.. J Med Virol 1996 Jan;48(1):102-7.
- Schwaiger M, Cassinotti P. Development of a quantitative real-time RT-PCR assay with internal control for the laboratory detection of tick borne encephalitis virus (TBEV) RNA.. J Clin Virol 2003 Jul;27(2):136-45.
- Puchhammer-Stöckl E, Kunz C, Mandl CW, Heinz FX. Identification of tick-borne encephalitis virus ribonucleic acid in tick suspensions and in clinical specimens by a reverse transcription-nested polymerase chain reaction assay.. Clin Diagn Virol 1995 Dec;4(4):321-6.
- Sumilo D, Bormane A, Asokliene L, Vasilenko V, Golovljova I, Avsic-Zupanc T, Hubalek Z, Randolph SE. Socio-economic factors in the differential upsurge of tick-borne encephalitis in Central and Eastern Europe.. Rev Med Virol 2008 Mar-Apr;18(2):81-95.
- Sumilo D, Bormane A, Asokliene L, Lucenko I, Vasilenko V, Randolph S. Tick-borne encephalitis in the Baltic States: identifying risk factors in space and time.. Int J Med Microbiol 2006 May;296 Suppl 40:76-9.
- Jaenson TG, Hjertqvist M, Bergström T, Lundkvist A. Why is tick-borne encephalitis increasing? A review of the key factors causing the increasing incidence of human TBE in Sweden.. Parasit Vectors 2012 Aug 31;5:184.
- Sikutová S, Hornok S, Hubálek Z, Dolezálková I, Juricová Z, Rudolf I. Serological survey of domestic animals for tick-borne encephalitis and Bhanja viruses in northeastern Hungary.. Vet Microbiol 2009 Mar 30;135(3-4):267-71.
- Stefanoff P, Pfeffer M, Hellenbrand W, Rogalska J, Rühe F, Makówka A, Michalik J, Wodecka B, Rymaszewska A, Kiewra D, Baumann-Popczyk A, Dobler G. Virus detection in questing ticks is not a sensitive indicator for risk assessment of tick-borne encephalitis in humans.. Zoonoses Public Health 2013 May;60(3):215-26.
- Gäumann R, Mühlemann K, Strasser M, Beuret CM. High-throughput procedure for tick surveys of tick-borne encephalitis virus and its application in a national surveillance study in Switzerland.. Appl Environ Microbiol 2010 Jul;76(13):4241-9.
- Sidorenko M, Radzijevskaja J, Mickevičius S, Bratčikovienė N, Paulauskas A. Prevalence of tick-borne encephalitis virus in questing Dermacentor reticulatus and Ixodes ricinus ticks in Lithuania.. Ticks Tick Borne Dis 2021 Jan;12(1):101594.
- Belova OA, Burenkova LA, Karganova GG. Different tick-borne encephalitis virus (TBEV) prevalences in unfed versus partially engorged ixodid ticks--evidence of virus replication and changes in tick behavior.. Ticks Tick Borne Dis 2012 Sep;3(4):240-6.
- Balling A, Plessow U, Beer M, Pfeffer M. Prevalence of antibodies against tick-borne encephalitis virus in wild game from Saxony, Germany.. Ticks Tick Borne Dis 2014 Oct;5(6):805-9.
- Klaus C, Ziegler U, Kalthoff D, Hoffmann B, Beer M. Tick-borne encephalitis virus (TBEV) - findings on cross reactivity and longevity of TBEV antibodies in animal sera.. BMC Vet Res 2014 Apr 1;10:78.
- Klaus C, Beer M, Saier R, Schubert H, Bischoff S, Süss J. Evaluation of serological tests for detecting tick-borne encephalitis virus (TBEV) antibodies in animals.. Berl Munch Tierarztl Wochenschr 2011 Nov-Dec;124(11-12):443-9.
- Pacilly FC, Benning ME, Jacobs F, Leidekker J, Sprong H, Van Wieren SE, Takken W. Blood feeding on large grazers affects the transmission of Borrelia burgdorferi sensu lato by Ixodes ricinus.. Ticks Tick Borne Dis 2014 Oct;5(6):810-7.
- Rizzoli A, Hauffe HC, Tagliapietra V, Neteler M, Rosà R. Forest structure and roe deer abundance predict tick-borne encephalitis risk in Italy.. PLoS One 2009;4(2):e4336.
- Bolzoni L, Rosà R, Cagnacci F, Rizzoli A. Effect of deer density on tick infestation of rodents and the hazard of tick-borne encephalitis. II: population and infection models.. Int J Parasitol 2012 Apr;42(4):373-81.
- Hofmeester TR, Sprong H, Jansen PA, Prins HHT, van Wieren SE. Deer presence rather than abundance determines the population density of the sheep tick, Ixodes ricinus, in Dutch forests.. Parasit Vectors 2017 Sep 19;10(1):433.
- Gassner F, Verbaarschot P, Smallegange RC, Spitzen J, Van Wieren SE, Takken W. Variations in Ixodes ricinus density and Borrelia infections associated with cattle introduced into a woodland in The Netherlands.. Appl Environ Microbiol 2008 Dec;74(23):7138-44.
Citations
This article has been cited 15 times.- Gothe LMR, Ganzenberg S, Ziegler U, Obiegala A, Lohmann KL, Sieg M, Vahlenkamp TW, Groschup MH, Hörügel U, Pfeffer M. Horses as Sentinels for the Circulation of Flaviviruses in Eastern-Central Germany. Viruses 2023 Apr 30;15(5).
- Fracasso G, Grillini M, Grassi L, Gradoni F, Rold GD, Bertola M. Effective Methods of Estimation of Pathogen Prevalence in Pooled Ticks. Pathogens 2023 Apr 5;12(4).
- Trozzi G, Adjadj NR, Vervaeke M, Matthijs S, Sohier C, De Regge N. Comparison of Serological Methods for Tick-Borne Encephalitis Virus-Specific Antibody Detection in Wild Boar and Sheep: Impact of the Screening Approach on the Estimated Seroprevalence. Viruses 2023 Feb 6;15(2).
- Cavalleri JV, Korbacska-Kutasi O, Leblond A, Paillot R, Pusterla N, Steinmann E, Tomlinson J. European College of Equine Internal Medicine consensus statement on equine flaviviridae infections in Europe. J Vet Intern Med 2022 Nov;36(6):1858-1871.
- Magouras I, Schoster A, Fouché N, Gerber V, Groschup MH, Ziegler U, Fricker R, Griot C, Vögtlin A. Neurological disease suspected to be caused by tick-borne encephalitis virus infection in 6 horses in Switzerland. J Vet Intern Med 2022 Nov;36(6):2254-2262.
- Ganzenberg S, Sieg M, Ziegler U, Pfeffer M, Vahlenkamp TW, Hörügel U, Groschup MH, Lohmann KL. Seroprevalence and Risk Factors for Equine West Nile Virus Infections in Eastern Germany, 2020. Viruses 2022 May 30;14(6).
- Da Rold G, Obber F, Monne I, Milani A, Ravagnan S, Toniolo F, Sgubin S, Zamperin G, Foiani G, Vascellari M, Drzewniokova P, Castellan M, De Benedictis P, Citterio CV. Clinical Tick-Borne Encephalitis in a Roe Deer (Capreolus capreolus L.). Viruses 2022 Jan 31;14(2).
- Pautienius A, Dudas G, Simkute E, Grigas J, Zakiene I, Paulauskas A, Armonaite A, Zienius D, Slyzius E, Stankevicius A. Bulk Milk Tank Samples Are Suitable to Assess Circulation of Tick-Borne Encephalitis Virus in High Endemic Areas. Viruses 2021 Sep 5;13(9).
- Fouché N, Oesch S, Ziegler U, Gerber V. Clinical Presentation and Laboratory Diagnostic Work-Up of a Horse with Tick-Borne Encephalitis in Switzerland. Viruses 2021 Jul 28;13(8).
- Kloster H, Stormo C, Haaland AH, Stuen S, Kjelland V. Seroprevalence of IgG Antibodies Against Borrelia burgdorferi Sensu Lato, Anaplasma phagocytophilum, and Tick-Borne Encephalitis (TBE) Virus in Horses in Southern Norway. Microorganisms 2025 Mar 28;13(4).
- Simkute E, Pautienius A, Grigas J, Sidorenko M, Radzijevskaja J, Paulauskas A, Stankevicius A. The Prevalence of Tick-Borne Encephalitis Virus in Wild Rodents Captured in Tick-Borne Encephalitis Foci in Highly Endemic Lithuania. Viruses 2024 Mar 13;16(3).
- Vilibic-Cavlek T, Krcmar S, Bogdanic M, Tomljenovic M, Barbic L, Roncevic D, Sabadi D, Vucelja M, Santini M, Hunjak B, Stevanovic V, Boljfetic M, Bjedov L, Masovic V, Potocnik-Hunjadi T, Lakoseljac D, Al-Mufleh M, Savic V. An Overview of Tick-Borne Encephalitis Epidemiology in Endemic Regions of Continental Croatia, 2017-2023. Microorganisms 2024 Feb 13;12(2).
- Sidorenko M, Radzijevskaja J, Mickevičius S, Bratchikov M, Mardosaitė-Busaitienė D, Sakalauskas P, Paulauskas A. Phylogenetic characterisation of tick-borne encephalitis virus from Lithuania. PLoS One 2024;19(2):e0296472.
- Simkute E, Pautienius A, Grigas J, Urbute P, Stankevicius A. The Prevalence, Seroprevalence, and Risk Factors of Tick-Borne Encephalitis Virus in Dogs in Lithuania, a Highly Endemic State. Viruses 2023 Nov 17;15(11).
- de Heus P, Bagó Z, Weidinger P, Lale D, Trachsel DS, Revilla-Fernández S, Matiasek K, Nowotny N. Severe Neurologic Disease in a Horse Caused by Tick-Borne Encephalitis Virus, Austria, 2021. Viruses 2023 Sep 29;15(10).
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