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Die Rolle Des Europäischen Igels (Erinaceus Europaeus)

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Die Rolle Des Europäischen Igels (Erinaceus Europaeus) Die Rolle des Europäischen Igels ( Erinaceus europaeus ) in der Epidemiologie zeckenübertragener Krankheiten -Borrelia spp., Anaplasma spp., Rickettsia spp. und FSME-Viren- Zur Erlangung des akademischen Grades eines DOKTORS DER NATURWISSENSCHAFTEN (Dr. rer. nat.) Fakultät für Chemie und Biowissenschaften Karlsruher Institut für Technologie (KIT)-Universitätsbereich genehmigte DISSERTATION von Jasmin Desirée Skuballa aus Karlsruhe Dekan: Prof. Dr. Martin Bastmeyer Referent: Prof. Dr. Horst Taraschewski 1.Korreferent: Prof. Dr. Dr. Peter Kimmig 2. Korreferent: Prof. Dr. Doris Wedlich Tag der mündlichen Prüfung: 18.10.2011 Meiner Familie Teile dieser Arbeit wurden bereits veröffentlicht: Skuballa J, Petney TN, Pfäffle M, Oehme R, Hartelt K, Fingerle V, Kimmig P, Taraschewski H (2011) Occurrence of different Borrelia burgdorferi sensu lato genospecies including B. afzelii, B. bavariensis and B. spielmanii in hedgehogs ( Erinaceus spp.) in Europe. Ticks and Tick-borne Diseases (in press). Skuballa J, Pfäffle M, Petney TN, Taraschewski H (2010) Molecular detection of Anaplasma phagocytophilum in the European hedgehog ( Erinaceus europaeus ) and its ticks. Vector-Borne and Zoonotic Diseases 10: 1055-1057. Skuballa J, Oehme R, Hartelt K, Petney T, Bücher T, Kimmig P, Taraschewski H (2007) European hedgehogs as hosts for Borrelia spp., Germany. Emerging Infectious Diseases 13: 952-953. Diese Arbeit wurde in Kooperation mit dem Landesgesundheitsamt Baden-Württemberg durchgeführt und gefördert durch: ein Stipendium der Landesgraduiertenförderung Baden-Württemberg und ein Stipendium der Grimminger-Stiftung für Zoonosenforschung, Stuttgart. Zusammenfassung Zusammenfassung Vektorübertragene Erreger zirkulieren in der Natur innerhalb vielfältiger Transmissionszyklen zwischen blutsaugenden Arthropoden und Wirbeltieren und können letztendlich auch den Menschen erreichen. Grundlegende Untersuchungen zur Erreger-Vektor-Wirts-Beziehung sind daher notwendig, um die komplexen epidemiologischen Zusammenhänge zu verstehen. In der vorliegenden Arbeit wurde die Stellung von Igeln, insbesondere der Art Erinaceus europaeus , im Kreislauf von zeckenassoziierten Erregern in West- und Mitteleuropa untersucht. Der Schwerpunkt der Studie lag dabei auf Borrelien des Borrelia burgdorferi s.l. Komplexes, aber auch zur Epidemiologie von Anaplasmen, Rickettsien und des FSME-Virus konnten neue Daten gewonnen werden. Für die molekularbiologische Untersuchung auf die genannten Erreger wurden Organproben von Sektionsigeln und von Igeln abgesammelte Zecken ( Ixodes hexagonus und Ixodes ricinus ) verwendet. Des Weiteren wurden Blutproben von lebenden Igeln mithilfe eines modifizierten ELISAs und Immunblots auf spezifische Antikörper gegen Borrelien getestet. Ergänzt wurde die B. burgdorferi s.l. Untersuchung durch Xenodiagnose an experimentell und natürlich infizierten Igeln. Die hier vorgestellten Ergebnisse demonstrieren deutlich, dass Igel eine nicht zu unterschätzende Rolle im Kreislauf von zeckenübertragenen Erregern mit humanpathogenem Potential einnehmen. Anhand der gewonnenen Daten zeigt sich das Reservoirpotential des Igels für Borrelien ( Borrelia afzelii, Borrelia bavariensis und Borrelia spielmanii ), was auch durch Xenodiagnose bestätigt werden konnte. Insbesondere juvenile Igel und Igelindividuen mit einem schlechten Allgemeinbefinden scheinen empfänglich für eine Infektion zu sein. Demgegenüber stehen der hohe IgG-Titer gegen spezifische Borrelia -Antigene und die niedrige Transmissionsrate von Borrelien auf Zecken bei adulten Tieren, was auf eine Verringerung der Reservoirkompetenz durch eine erworbene Immunität hindeutet. Auch im Kreislauf von Anaplasma phagocytophilum nehmen Igel eine wichtige Position ein. Die vorliegenden Ergebnisse zeigen, dass Igel für eine „igelspezifische“ A. phagocytophilum -Variante, aber auch für weitere Genotypen empfänglich sind. An der Verbreitung von Rickettsien sind Igel ebenfalls deutlich beteiligt. Rickettsien wurden sowohl in einer Hautprobe als auch in allen 3 Entwicklungsstadien von in I. ricinus und I. hexagonus nachgewiesen. Die Sequenzierung bestätigte die Infektion beider Zeckenarten mit Rickettsia helvetica. Die 3 genannten Erreger wurden nicht nur in I. ricinus, sondern auch i Zusammenfassung in I. hexagonus gefunden , was auch für die Involvierung von wirtsspezifischen Zecken in der Epidemiologie dieser Erreger spricht. Der molekularbiologische Nachweis von FSME-Viren im Nierengewebe eines Tieres beweist, dass Igel auch für virale Erreger anfällig sind. Im Rahmen der vorliegenden Studie wurde nur ein kleines Repertoire an zeckenassoziierten Erregern untersucht. Es muss jedoch davon ausgegangen werden, dass Igel durch einen häufigen und starken Ektoparasitenbefall auch an der Verbreitung weiterer vektorübertragener Erreger (z.B. Babesia spp., Bartonella spp. und Francisella spp.) beteiligt sind. Die gewonnenen Daten sollten daher als Grundlage und Ausgangsbasis für weitere Untersuchungen dienen, um einerseits Schutzstrategien für den Igel zu entwickeln, aber auch andererseits auf die zoonotische Bedeutung aufmerksam zu machen. ii Summary Summary Title: The role of the European hedgehog ( Erinaceus europaeus ) in the epidemiology of tick-borne diseases ( Borrelia spp., Anaplasma spp., Rickettsia spp. and TBE-virus). Vector-borne pathogens circulate in nature between blood-sucking arthropods and vertebrate hosts via a variety of transmission cycles through which they can also reach humans. Basic investigations on the pathogen-vector-host relationship are therefore necessary in order to understand such a complex epidemiological situation. The work presented focuses on the role of hedgehogs, notably Erinaceus europaeus , in the circulation of tick-borne pathogens in Western and Central Europe. New data are presented particularly with regard to various genospecies of the Borrelia burgdorferi s.l. complex, but also involving the epidemiology of Anaplasma species, Rickettsia species and tick-borne encephalitis (TBE) virus. For the molecular investigation of these pathogens, organs of dissected animals, as well as ticks ( Ixodes hexagonus and Ixodes ricinus ) removed from hedgehogs, were used. In addition blood samples from living animals were tested by a modified ELISA and an immunoblot for specific antibodies against Borrelia genospecies. The B. burgdorferi s.l. investigation was supplemented by xenodiagnosis on experimentally and naturally infected hedgehogs. The results obtained demonstrate that hedgehogs play a significant role in the circulation of tick-borne pathogens with pathogenic potential for humans. The data acquired prove the reservoir potential of hedgehogs for certain Borrelia genospecies ( Borrelia afzelii, Borrelia bavariensis and Borrelia spielmanii ). In particular juvenile hedgehogs or individuals with a reduced health status seem to be susceptible to infection. In contrast to this, high IgG-titers against specific Borrelia antigens and the low transmission rate from adult animals to ticks indicate a reduction in the reservoir competence of hedgehogs presumably caused by adaptive immunity. Hedgehogs are also involved in the circulation of Anaplasma phagocytophilum . My results show that they are susceptible to a specific “hedgehog variant”, but also to other genotypes. In a similar way, hedgehogs play a role in the epidemiology of Rickettsia species. Rickettsial DNA could be detected in a skin sample of one animal, as well as in all life history stages of iii Summary I. hexagonus and I. ricinus ticks. Sequencing confirmed the presence of Rickettsia helvetica in both tick species. Finding the pathogens not only in I. ricinus , but also in I. hexagonus , indicates the involvement of both species in the circulation of these pathogens. The molecular detection of TBE-virus in the kidney of one animal confirms the susceptibility of hedgehogs to viral infections. In this study a limited repertoire of tick-borne pathogens was examined. However, it has to be assumed that hedgehogs with a high burden of different ectoparasites are also involved in the spreading of other vector-borne pathogens (e.g. Babesia, Bartonella and Francisella ). Hence, the data obtained should serve as a baseline for further investigations, and should help in the development of conservation strategies for hedgehogs, as well as calling attention to the zoonotic potential. iv Inhaltsverzeichnis Inhaltsverzeichnis Zusammenfassung.....................................................................................................................i Summary..................................................................................................................................iii Inhaltsverzeichnis..................................................................................................................... v 1 Einleitung.......................................................................................................................... 1 1.1 Fragestellung und Zielsetzung ................................................................................ 4 2 Literaturübersicht............................................................................................................ 5 2.1 Zur Biologie und Ökologie von Igeln (Erinaceidae) ............................................. 5 2.1.1 Systematik und Verbreitung.................................................................... 5 2.1.2 Kleinohrigel ( Erinaceus spp.)................................................................... 5 2.1.3 Zur Biologie und Ökologie
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