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Competence of the Vector Restricting Tick-Borne Encephalitis Virus Spread

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Competence of the Vector Restricting Tick-Borne Encephalitis Virus Spread University of Veterinary Medicine Hannover Institute for Parasitology Competence of the vector restricting tick-borne encephalitis virus spread THESIS Submitted in partial fulfilment of the requirements for the degree of Doctor of Natural Sciences Doctor rerum naturalium (Dr. rer. nat.) awarded by the University of Veterinary Medicine Hannover by Katrin Liebig from Rheda-Wiedenbrück Hannover, Germany 2020 Supervisor: Prof. Dr. rer. nat. Stefanie Becker Supervision Group: Prof. Dr. rer. nat. Stefanie Becker Prof. Dr. rer. nat. Klaus Jung PD Dr. med. habil. Gerhard Dobler 1st Evaluation: Prof. Dr. rer. nat. Stefanie Becker Institute for Parasitology and Research Center for Emerging Infections and Zoonoses University of Veterinary Medicine Hannover, Foundation Prof. Dr. rer. nat. Klaus Jung Institute for Animal Breeding and Genetics University of Veterinary Medicine Hannover, Foundation PD Dr. med. habil. Gerhard Dobler Institute for Microbiology of the Bundeswehr Parasitology Unit, University of Hohenheim 2nd Evaluation: Prof. Dr. med. vet. Martin Pfeffer Institute of Animal Hygiene and Veterinary Public Health University of Leipzig Date of final exam: 29.10.2020 This work was funded by the German research foundation and the TBENAGER consortium. Parts of the present thesis have been either accepted for publication or prepared for submission Accepted for publication Liebig, K., Boelke, M., Grund, D., Schicht, S., Springer, A. Strube, C., Chitimia-Dobler, L., Dobler, G. Jung, K., Becker, S. Tick populations from endemic and non-endemic areas in Germany show differential susceptibility to TBEV. Sci Rep 10, 15478 (2020). https://doi.org/10.1038/s41598-020-71920-z Prepared for submission Liebig, K., Boelke, M., Grund, D., Schicht, S., Bestehorn-Willmann, M., Chitimia-Dobler, L., Dobler, G. Jung, K., Becker, S.The stable matching problem in TBEV enzootic circulation: the importance of the perfect tick-virus match. Table of content Table of content I List of abbreviations II List of figures IV Summary V Zusammenfassung VI Introduction 1 Tick-borne encephalitis (TBE) 1 Tick-borne encephalitis virus (TBEV) 2 Distribution 4 Transmission 5 Ixodes ricinus 7 Life cycle 7 Spread 8 Vector competence 9 In vitro feeding 10 Aim of the study 11 Publications 12 Tick populations from endemic and non-endemic areas in Germany show differential susceptibility to TBEV. 12 Abstract 13 The stable matching problem in TBEV enzootic circulation: the importance of the perfect tick- virus match. 14 Abstract 15 Introduction 15 Materials and Methods 16 Results 18 Discussion 20 Conclusion 23 Supplementary material 24 References 25 Material and Methods 29 Discussion 30 Conclusion 41 References 42 I List of abbreviations % Percent ++ssRNA positive-sense single-stranded RNA °C Degree Celsius µl Microliter A. Anaplasma aa Amino acids Ae. Aedes Arbovirus Arthropode-borne virus B. Borrelia BSL3 Biosafety level three C Capsid CHIKV Chikungunya virus CNS Central nervous system CO2 Carbon dioxide D. Dermacentor DEET N,N-diethyl-meta-toluamide DENV Dengue virus E Envelope et al. Et ali; and others FSMEV Frühsommer-Meningoenzephalitis-Virus H. Haemaphysalis I. Ixodes IMD Immune deficiency IOL Indian Ocean Lineage JAK-STAT Janus kinase/signal transducers and activators of transcription JEV Japanese encephalitis virus M Membrane MAPK Mitogen-activated protein kinase min. Minutes II mm Milimetre NS Non-structural proteins prM Precursor of protein M R. Rickettsia RdRp RNA-dependent RNA-polymerase RH Relative humidity RNA Ribonucleic acid RNAi RNA interference s.l. Sensu lato; in the broad sense spp. Species pluralis; multiple species TBE Tick-borne encephalitis TBEV Tick-borne encephalitis virus TBV Tick-borne viruses VEEV Venezuelan equine encephalitis virus WNV West Nile virus YFV Yellow fever virus ZIKV Zika virus III List of figures Figure 1 Schematic model of a flavivirus particle (Vratskikh et al. 2013). 2 Figure 2 Phylogenetic tree of TBEV (Dai et al. 2018), modified. 3 Figure 3 TBEV transmission and I. ricinus life cycle. 6 Figure 4 Single components of the in vitro feeding chamber. 29 Figure 5 Fully assembled in vitro feeding chamber, containing bovine blood. 29 Figure 6 Schematic dissection of I. ricinus 29 IV Summary Summary Competence of the vector restricting tick-borne encephalitis virus spread Katrin Liebig The tick-borne encephalitis virus (TBEV) is a flavivirus, circulating between ticks and vertebrates. It is considered a major health risk in Germany with 1028 reported human cases in 2018 and 2019. Risk areas of TBEV are mainly located in the south of Germany, primarily in the states of Bavaria and Baden- Wuerttemberg. In contrast to this focal distribution, the main vector of TBEV in Germany, Ixodes (I.) ricinus, as well as host species are spread countrywide, indicating that other factors apart from the presence of suitable vectors and hosts are important for enzootic circulation of TBEV. The current state of knowledge concerning the vector competence of geographically separated I. ricinus populations for the TBEV is incomplete. Therefore, experimental infection studies using Ixodes ticks of different populations, distributed across Germany, and different TBEV isolates were conducted to investigate possible population-based differences in infection susceptibility. To achieve this goal, an artificial feeding system has been used to infect field collected I. ricinus nymphs with different TBEV strains. Over three seasons, the susceptibility to TBEV infection have been analyzed involving different impact factors as seasonality, natural co-infection and the correlation of tick population with a respective TBEV strain. Ixodes ricinus nymphs were collected in four TBEV endemic foci as well as one non-endemic area. To investigate specific virus isolate/tick population relationships, ticks were exposed to different virus isolates by in vitro feeding and compared regarding their feeding behavior as well as their infection susceptibility for the respective TBEV strains. Differences in the intrinsic susceptibility of the I. ricinus tick vector to TBEV infection seem to be related to genetic pairings of vector and virus. Furthermore, infection with Borrelia spp. may influence the ability of tick populations to spread TBEV. These findings can help to deepen the understanding of TBEV focal transmission cycle as it is critical for predicting and mitigating human disease risk. V Zusammenfassung Zusammenfassung Untersuchung einer möglichen vektorbedingten Kompetenzbeeinträchtigung bei der Ausbreitung des Erregers der Frühsommer-Meningoenzephalitis Katrin Liebig Das Frühsommer-Meningoenzephalitis-Virus (FSMEV) ist ein zwischen Zecken und Vertebraten zirkulierendes Flavivirus. Mit 1028 gemeldeten Humanfällen in den Jahren 2018 und 2019, wird es als erhebliches Gesundheitsrisiko in Deutschland betrachtet. Risikogebiete von FSMEV sind hauptsächlich in Süddeutschland lokalisiert, vorrangig in Bayern und Baden-Württemberg. Im Gegensatz zu dieser fokalen Verbreitung in Deutschland, kommen der Hauptvektor Ixodes (I.) ricinus sowie die Wirtsarten gleichmäßig im Land vor. Dies weist darauf hin, dass neben dem Vorkommen von Vektor und Wirt, noch andere Faktoren für den sylvatischen Zyklus von FSMEV wichtig sind. Der derzeitige Wissensstand bezüglich der Vektorkompetenz von geografisch separierten I. ricinus Populationen für FSMEV ist unvollständig. Um mögliche Populations-basierte Unterschiede in der Empfänglichkeit für eine Infektion zu untersuchen, wurden experimentelle Infektionsstudien mit Ixodes Zecken aus unterschiedlichen Populationen Deutschlands und verschiedenen FSMEV Isolaten durchgeführt. Ein künstliches Fütterungssystem wurde verwendet, um I. ricinus Nymphen aus natürlichen Habitaten mit unterschiedlichen FSMEV Stämmen zu infizieren. Die Empfänglichkeit für eine FSMEV Infektion wurde über drei Saisons analysiert. Dabei wurden unterschiedliche Einflussfaktoren wie die Saisonalität, natürliche Koinfektionen und die Korrelation zwischen Zeckenpopulation mit einem bestimmten FSMEV Stamm einbezogen. Die I. ricinus Nymphen wurden in vier FSMEV endemischen und einem FSMEV nicht endemischen Gebiet gesammelt. Um spezifische Beziehungen zwischen Virus und Zeckenpopulationen zu untersuchen, wurden die Zecken mit verschiedenen Virusisolaten über die in vitro Fütterung infiziert und hinsichtlich ihres Fütterungsverhaltens sowie ihrer Empfänglichkeit für eine Infektion mit einem bestimmten FSMEV Stammes verglichen. Unterschiede in der spezifischen Empfänglichkeit des I. ricinus Zeckenvektors für eine FSMEV Infektion scheinen mit der genetischen Paarung von Vektor und Virus in Verbindung zu stehen. Darüber hinaus könnte eine Infektion mit Borrelia spp. die Fähigkeit von Zeckenpopulationen FSMEV zu verbreiten beeinflussen. Diese Erkenntnisse können zu einem besseren Verständnis des fokalen FSMEV Übertragungszyklus beitragen, welches für die Vorhersage und Minderung des Erkrankungsrisikos für den Menschen entscheidend ist. VI Introduction Introduction Worldwide over 500 arboviruses are described (Weaver and Reisen 2010; Gubler 2001) of which at least 38 viral species are transmitted by ticks (Labuda and Nuttall 2004). The ongoing geographical expansion of zoonotic diseases like Chikungunya, Dengue, Yellow fever and Zika virus poses a considerable global health threat. Besides mosquitos, ticks are the most important vectors for transmitting arboviruses (de la Fuente et al. 2008). Due to globalization and climate change, new arthropod vector species are spread and introduced in formerly
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