Tick-Borne Encephalitis Virus (TBEV) Infection in Two Horses.
Abstract: A final diagnosis in a horse with clinical signs of encephalopathy can be challenging despite the use of extensive diagnostics. Clinical signs are often not pathognomonic and need to be interpreted in combination with (specific) laboratory results and epidemiological data of the geographical region of the origin of the case(s). Here we describe the diagnostic pathway of tick-borne encephalitis virus infection in two horses using established molecular diagnostic methods and a novel in situ hybridization technique to differentiate between regionally important/emerging diseases for central Europe: (i) hepatoencephalopathy, (ii) Borna disease virus, and (iii) West Nile virus infections.
Publication Date: 2021-09-06 PubMed ID: 34578356PubMed Central: PMC8472121DOI: 10.3390/v13091775Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Case Reports
- Journal Article
- Borna Disease Virus
- Case Reports
- Clinical Signs
- Diagnosis
- Diagnostic Technique
- Disease Diagnosis
- Encephalitis
- Epidemiology
- Equine Health
- Horses
- In Situ Hybridization
- Infection
- Infectious Disease
- Laboratory Methods
- Molecular biology
- Neurological Diseases
- Tick-Borne Diseases
- Veterinary Medicine
- Virology
- Virus
- West Nile Virus
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
This research aims to describe how two horse cases, presenting with brain inflammation symptoms, were eventually diagnosed with Tick-Borne Encephalitis Virus (TBEV) infection. This was achieved using existing diagnostic methods and introducing a new one, in situ hybridization, to differentiate TBEV from other regionally prevalent neurological diseases in Central Europe.
Diagnostic Challenge in Encephalopathy Cases in Horses
- Healthcare professionals struggle to give a conclusive diagnosis when a horse exhibits symptoms of encephalopathy, the condition typified by altered brain functions or structures.
- The clinical signs often do not match precisely with any one disease and must be combined with specific lab results and epidemiological data collected from the geographic origin of the case(s).
TBEV Diagnosis in Two Horses
- The researchers set about diagnosing two horses displaying symptoms of encephalopathy.
- They employed standard molecular diagnostic techniques and a newly introduced procedure called in situ hybridization, which enables them to locate specific DNA or RNA sequences in tissues using labeled probes.
- This procedure was instrumental in differentiating Tick-Borne Encephalitis Virus (TBEV) infection from other similar diseases common in the central Europe region, such as hepatoencephalopathy, Borna disease virus, and West Nile virus infections.
Noteworthy Outcomes
- With these methods, both cases were found to be suffering from TBEV infection.
- The success of this diagnostic pathway underscores the potential of techniques like in situ hybridization in identifying diseases that usually pose a diagnostic challenge, like encephalopathies in horses.
Cite This Article
APA
Conze TM, Bagó Z, Revilla-Fernández S, Schlegel J, Goehring LS, Matiasek K.
(2021).
Tick-Borne Encephalitis Virus (TBEV) Infection in Two Horses.
Viruses, 13(9), 1775.
https://doi.org/10.3390/v13091775 Publication
Researcher Affiliations
- Equine Medicine and Reproduction, Centre for Clinical Veterinary Medicine, Faculty of Veterinary Medicine, Ludwig-Maximilians University Munich, Veterinärstraße 13, 80539 Munich, Germany.
- Institute for Veterinary Disease Control Mödling, Austrian Agency for Health and Food Safety GmbH (AGES), IVET, 2340 Mödling, Austria.
- Institute for Veterinary Disease Control Mödling, Austrian Agency for Health and Food Safety GmbH (AGES), IVET, 2340 Mödling, Austria.
- Department of Neuropathology, Institute of Pathology, School of Medicine, Technical University Munich, Trogerstraße 18, 81675 Munich, Germany.
- Equine Medicine and Reproduction, Centre for Clinical Veterinary Medicine, Faculty of Veterinary Medicine, Ludwig-Maximilians University Munich, Veterinärstraße 13, 80539 Munich, Germany.
- Section of Clinical and Comparative Neuropathology, Centre for Clinical Veterinary Medicine, Ludwig-Maximilians University, Veterinärstraße 13, 80539 Munich, Germany.
MeSH Terms
- Animals
- Austria
- Brain / pathology
- Brain / virology
- Encephalitis Viruses, Tick-Borne / genetics
- Encephalitis, Tick-Borne / diagnosis
- Encephalitis, Tick-Borne / epidemiology
- Encephalitis, Tick-Borne / pathology
- Encephalitis, Tick-Borne / virology
- Germany
- Horse Diseases / diagnosis
- Horse Diseases / epidemiology
- Horse Diseases / pathology
- Horse Diseases / virology
- Horses
- In Situ Hybridization
- Ixodes / virology
- West Nile Fever / epidemiology
- West Nile Fever / virology
- West Nile virus / genetics
Conflict of Interest Statement
The authors declare no conflict of interest.
References
This article includes 64 references
- Böhm B, Schade B, Bauer B, Hoffmann B, Hoffmann D, Ziegler U, Beer M, Klaus C, Weissenböck H, Böttcher J. Tick-borne encephalitis in a naturally infected sheep.. BMC Vet Res 2017 Aug 22;13(1):267.
- Schneider H. Über epidemische akute ‘Meningitis serosa’. Wien. Klin. Wochenschr. 1931;44:350–352.
- Slávik I, Mayer V, Mrena E. Morphologyof purified tick-borne encephalitis virus.. Acta Virol 1967 Jan;11(1):66.
- Beauté J, Spiteri G, Warns-Petit E, Zeller H. Tick-borne encephalitis in Europe, 2012 to 2016.. Euro Surveill 2018 Nov;23(45).
- Holzmann H, Aberle SW, Stiasny K, Werner P, Mischak A, Zainer B, Netzer M, Koppi S, Bechter E, Heinz FX. Tick-borne encephalitis from eating goat cheese in a mountain region of Austria.. Emerg Infect Dis 2009 Oct;15(10):1671-3.
- Suss J. Tick-borne encephalitis in Europe and beyond--the epidemiological situation as of 2007.. Euro Surveill 2008 Jun 26;13(26).
- Kaiser R. The clinical and epidemiological profile of tick-borne encephalitis in southern Germany 1994-98: a prospective study of 656 patients.. Brain 1999 Nov;122 ( Pt 11):2067-78.
- Gustafson R, Svenungsson B, Forsgren M, Gardulf A, Granström M. Two-year survey of the incidence of Lyme borreliosis and tick-borne encephalitis in a high-risk population in Sweden.. Eur J Clin Microbiol Infect Dis 1992 Oct;11(10):894-900.
- . Epidemiological Situation of Tick-Borne Encephalitis in the European Union and European Free Trade Association Countries. European Centre for Disease Prevention and Control .
- Robert-Koch-Institute. FSME: Risikogebiete in Deutschland [TBE risk areas in Germany]. Epid. Bull. 2018;17:161–176.
- Boelke M, Bestehorn M, Marchwald B, Kubinski M, Liebig K, Glanz J, Schulz C, Dobler G, Monazahian M, Becker SC. First Isolation and Phylogenetic Analyses of Tick-Borne Encephalitis Virus in Lower Saxony, Germany.. Viruses 2019 May 21;11(5).
- Österreichischer Verband der Impfstoffhersteller. [(accessed on 5 October 2020)]. Available online: https://oevih.at/
- Reiner B, Fischer A. Frühsommer-Meningoenzephalitis (FSME) beim Hund in Deutschland: Zwei Fallberichte. Kleintierpraxis 1998;43:255–269.
- Weissenböck H, Suchy A, Holzmann H. Tick-borne encephalitis in dogs: neuropathological findings and distribution of antigen.. Acta Neuropathol 1998 Apr;95(4):361-6.
- Süss J, Gelpi E, Klaus C, Bagon A, Liebler-Tenorio EM, Budka H, Stark B, Müller W, Hotzel H. Tickborne encephalitis in naturally exposed monkey (Macaca sylvanus).. Emerg Infect Dis 2007 Jun;13(6):905-7.
- Waldvogel A, Matile H, Wegmann C, Wyler R, Kunz C. [Tick-borne encephalitis in the horse].. Schweiz Arch Tierheilkd 1981 May;123(5):227-33.
- Luckschander N, Kölbel S, Enzesberger O, Zipko H.T., Thalhammer J.G. Frühsommermeningoenzepahlitis-(FSME)Infektion in einer österreichischen Pferdepopulation. Tierarztl Prax Aus G Grosstiere Nutztiere 1999;27:235–238.
- Janitza-Futterer D. Seroepidemiological Investigation of Endemic TBE Infection in A Horse and Dog Population in Southwestern Germany. Ph.D. Thesis. Ludwig-Maximilians University; Munich, Germany: 2013.
- Mayhew I.G.. Neurologic Evaluation. Large Animal Neurology Lea and Febiger; Philadelphia, PE, USA: 1989.
- Pease A, Behan A, Bohart G. Ultrasound-guided cervical centesis to obtain cerebrospinal fluid in the standing horse.. Vet Radiol Ultrasound 2012 Jan-Feb;53(1):92-5.
- Bitschi ML, Bagó Z, Rosati M, Reese S, Goehring LS, Matiasek K. A Systematic Approach to Dissection of the Equine Brain-Evaluation of a Species-Adapted Protocol for Beginners and Experts.. Front Neuroanat 2020;14:614929.
- Scaramozzino N, Crance JM, Jouan A, DeBriel DA, Stoll F, Garin D. Comparison of flavivirus universal primer pairs and development of a rapid, highly sensitive heminested reverse transcription-PCR assay for detection of flaviviruses targeted to a conserved region of the NS5 gene sequences.. J Clin Microbiol 2001 May;39(5):1922-7.
- Kolodziejek J, Marinov M, Kiss BJ, Alexe V, Nowotny N. The complete sequence of a West Nile virus lineage 2 strain detected in a Hyalomma marginatum marginatum tick collected from a song thrush (Turdus philomelos) in eastern Romania in 2013 revealed closest genetic relationship to strain Volgograd 2007.. PLoS One 2014;9(10):e109905.
- Liesche F, Ruf V, Zoubaa S, Kaletka G, Rosati M, Rubbenstroth D, Herden C, Goehring L, Wunderlich S, Wachter MF, Rieder G, Lichtmannegger I, Permanetter W, Heckmann JG, Angstwurm K, Neumann B, Märkl B, Haschka S, Niller HH, Schmidt B, Jantsch J, Brochhausen C, Schlottau K, Ebinger A, Hemmer B, Riemenschneider MJ, Herms J, Beer M, Matiasek K, Schlegel J. The neuropathology of fatal encephalomyelitis in human Borna virus infection.. Acta Neuropathol 2019 Oct;138(4):653-665.
- Schindler AR, Vögtlin A, Hilbe M, Puorger M, Zlinszky K, Ackermann M, Ehrensperger F. Reverse transcription real-time PCR assays for detection and quantification of Borna disease virus in diseased hosts.. Mol Cell Probes 2007 Feb;21(1):47-55.
- Kolodziejek J, Dürrwald R, Herzog S, Ehrensperger F, Lussy H, Nowotny N. Genetic clustering of Borna disease virus natural animal isolates, laboratory and vaccine strains strongly reflects their regional geographical origin.. J Gen Virol 2005 Feb;86(Pt 2):385-398.
- Goehring L.S., van Winden S.C., van Maanen C., Sloet van Oldruitenborgh-Oosterbaan M.M.. Equine herpesvirus type 1-associated myeloencephalopathy in The Netherlands: A four-year retrospective study (1999–2003). J. Vet. Intern. Med. 2006;24:1176–1183.
- Richt JA, Grabner A, Herzog S. Borna disease in horses.. Vet Clin North Am Equine Pract 2000 Dec;16(3):579-95, xi.
- Hilbe M, Herrsche R, Kolodziejek J, Nowotny N, Zlinszky K, Ehrensperger F. Shrews as reservoir hosts of borna disease virus.. Emerg Infect Dis 2006 Apr;12(4):675-7.
- Sauder C, Staeheli P. Rat model of borna disease virus transmission: epidemiological implications.. J Virol 2003 Dec;77(23):12886-90.
- Bilzer T, Stitz L. Brain cell lesions in Borna disease are mediated by T cells.. Arch Virol Suppl 1993;7:153-8.
- Weissenböck H, Bagó Z, Kolodziejek J, Hager B, Palmetzhofer G, Dürrwald R, Nowotny N. Infections of horses and shrews with Bornaviruses in Upper Austria: a novel endemic area of Borna disease.. Emerg Microbes Infect 2017 Jun 21;6(6):e52.
- Grabner A, Herzog S, Lange-Herbst H, Frese K. Die Intra-vitam-Diagnose der Bornaschen Krankheit (BD) bei Equiden. Pferdeheilkunde 2002;18:579–586.
- Lange H, Herzog S, Herbst W, Schließer T. Seroepidemiologische Untersuchungen zur Bornaschen Krankheit (Ansteckende Gehirn- und Rückenmarksentzündung der Pferde). Tierärztl Umschau 1987;12:938–946.
- Stickle JE, McKnight CA, Williams KJ, Carr EA. Diarrhea and hyperammonemia in a horse with progressive neurologic signs.. Vet Clin Pathol 2006 Jun;35(2):250-3.
- Kosenko E, Kaminsky Y, Grau E, Miñana MD, Marcaida G, Grisolía S, Felipo V. Brain ATP depletion induced by acute ammonia intoxication in rats is mediated by activation of the NMDA receptor and Na+,K(+)-ATPase.. J Neurochem 1994 Dec;63(6):2172-8.
- Kosenko E, Kaminsky Y, Kaminsky A, Valencia M, Lee L, Hermenegildo C, Felipo V. Superoxide production and antioxidant enzymes in ammonia intoxication in rats.. Free Radic Res 1997 Dec;27(6):637-44.
- Albrecht J, Jones EA. Hepatic encephalopathy: molecular mechanisms underlying the clinical syndrome.. J Neurol Sci 1999 Nov 30;170(2):138-46.
- Divers T.J., Barton M.H.. Disorders of the Liver. Equine Internal Medicine 4th ed. Elsevier; St. Louis, MO, USA: 2018.
- Müller J.M.V., Schulze M., Herder V., Lautenschläger I., Baumgärtner W., Feige K. Ataxia and weakness as uncommon primary manifestations of hepatic encephalopathy in a 15-year-old trotter gelding. Equine Vet. Educ. 2011;23:5.
- Labuda M, Austyn JM, Zuffova E, Kozuch O, Fuchsberger N, Lysy J, Nuttall PA. Importance of localized skin infection in tick-borne encephalitis virus transmission.. Virology 1996 May 15;219(2):357-66.
- Nuttall PA, Labuda M. Dynamics of infection in tick vectors and at the tick-host interface.. Adv Virus Res 2003;60:233-72.
- 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.
- 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.
- Dörrbecker B, Dobler G, Spiegel M, Hufert FT. Tick-borne encephalitis virus and the immune response of the mammalian host.. Travel Med Infect Dis 2010 Jul;8(4):213-22.
- Haglund M, Günther G. Tick-borne encephalitis--pathogenesis, clinical course and long-term follow-up.. Vaccine 2003 Apr 1;21 Suppl 1:S11-8.
- Růžek D, Salát J, Singh SK, Kopecký J. Breakdown of the blood-brain barrier during tick-borne encephalitis in mice is not dependent on CD8+ T-cells.. PLoS One 2011;6(5):e20472.
- Bílý T, Palus M, Eyer L, Elsterová J, Vancová M, Růžek D. Electron Tomography Analysis of Tick-Borne Encephalitis Virus Infection in Human Neurons.. Sci Rep 2015 Jun 15;5:10745.
- Hayasaka D, Nagata N, Fujii Y, Hasegawa H, Sata T, Suzuki R, Gould EA, Takashima I, Koike S. Mortality following peripheral infection with tick-borne encephalitis virus results from a combination of central nervous system pathology, systemic inflammatory and stress responses.. Virology 2009 Jul 20;390(1):139-50.
- Růzek D, Salát J, Palus M, Gritsun TS, Gould EA, Dyková I, Skallová A, Jelínek J, Kopecký J, Grubhoffer L. CD8+ T-cells mediate immunopathology in tick-borne encephalitis.. Virology 2009 Feb 5;384(1):1-6.
- Del Piero F., Robertson J.L.. The Basics of Equine Neuropathology. Equine Neurology 2nd ed. Wiley Blackwell; Ames, IA, USA: 2015.
- Gelpi E, Preusser M, Garzuly F, Holzmann H, Heinz FX, Budka H. Visualization of Central European tick-borne encephalitis infection in fatal human cases.. J Neuropathol Exp Neurol 2005 Jun;64(6):506-12.
- Holzmann H. Diagnosis of tick-borne encephalitis.. Vaccine 2003 Apr 1;21 Suppl 1:S36-40.
- Long M.T.. Mosquito-Borne Infections Affecting the Central Nervous System. Equine Neurology 2nd ed. Wiley Blackwell; Ames, IA, USA: 2015.
- Smithburn K.C., Hughes T.P., Burke A.W., Paul J.H.. A neurotropic virus isolated from the blood of a native of Uganda. Am. J. Trop. Med. Hyg. 1940;20:471–473.
- Tierseuchengeschehen Friedrich-Löffler-Institute. [(accessed on 8 October 2020)]. Available online: https://www.fli.de/de/aktuelles/tierseuchengeschehen/west-nil-virus/
- Bunning ML, Bowen RA, Cropp CB, Sullivan KG, Davis BS, Komar N, Godsey MS, Baker D, Hettler DL, Holmes DA, Biggerstaff BJ, Mitchell CJ. Experimental infection of horses with West Nile virus.. Emerg Infect Dis 2002 Apr;8(4):380-6.
- Guthrie AJ, Howell PG, Gardner IA, Swanepoel RE, Nurton JP, Harper CK, Pardini A, Groenewald D, Visage CW, Hedges JF, Balasuriya UB, Cornel AJ, MacLachlan NJ. West Nile virus infection of Thoroughbred horses in South Africa (2000-2001).. Equine Vet J 2003 Sep;35(6):601-5.
- Porter MB, Long MT, Getman LM, Giguère S, MacKay RJ, Lester GD, Alleman AR, Wamsley HL, Franklin RP, Jacks S, Buergelt CD, Detrisac CJ. West Nile virus encephalomyelitis in horses: 46 cases (2001).. J Am Vet Med Assoc 2003 May 1;222(9):1241-7.
- Cantile C, Di Guardo G, Eleni C, Arispici M. Clinical and neuropathological features of West Nile virus equine encephalomyelitis in Italy.. Equine Vet J 2000 Jan;32(1):31-5.
- Ziegler U, Seidowski D, Angenvoort J, Eiden M, Müller K, Nowotny N, Groschup MH. Monitoring of West Nile virus infections in Germany.. Zoonoses Public Health 2012 Sep;59 Suppl 2:95-101.
- Holzmann H. Pitfalls in modern TBE sero-diagnosis. Zent. Bakteriol. 1999;289:548–549.
- 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.
- Rockstroh A, Moges B, Berneck BS, Sattler T, Revilla-Fernández S, Schmoll F, Pacenti M, Sinigaglia A, Barzon L, Schmidt-Chanasit J, Nowotny N, Ulbert S. Specific detection and differentiation of tick-borne encephalitis and West Nile virus induced IgG antibodies in humans and horses.. Transbound Emerg Dis 2019 Jul;66(4):1701-1708.
Citations
This article has been cited 3 times.- 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).
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists