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1 Stephan Et Al Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2014 Chlamydiaceae and chlamydia-like organisms in free-living small mammals in Europe and Afghanistan Stephan, S ; Guerra, D ; Pospischil, A ; Hilbe, M ; Weissenböck, H ; Novotny, L ; Greub, G ; Croxatto, A ; Teifke, J P ; Ulrich, R G ; Schlegel, M ; Ruhl, S ; Schotte, U ; Binder, A ; Sauer, S ; Borel, N Abstract: Few data are available on the occurrence of chlamydial infections in wild small mammals. Therefore, the present study aimed to investigate the significance of free-living small mammals as reser- voirs or transmission hosts for chlamydiae. In total, 3,664 tissue samples originating from 911 animals were collected in Switzerland, Germany, Austria, the Czech Republic and Afghanistan. Samples included internal organs (n = 3,652) and feces (n = 12) from 679 rodents (order Rodentia) and 232 insectivores (order Eulipotyphla) and were tested by three different TaqMan real-time polymerase chain reactions (PCR) specific for members of the family Chlamydiaceae and selected Chlamydia-like organisms suchas Parachlamydia spp. and Waddlia spp. Only one out of 911 (0.11%) animals exhibited a questionable pos- itive result by Chlamydiaceae specific real-time PCR. Furthermore, five out of 911 animals (0.55%) were positive by specific real-time PCR for Parachlamydia spp. but could not be confirmed by Parachlamydia acanthamoebae secY qPCR. One out of 746 animals (0.13%) showed a positive result by real-time PCR for Waddlia chondrophila. This result was confirmed by Waddlia secY qPCR. This study represents the first detection of Chlamydia-like organisms in small wildlife in Switzerland. Considering previous negative results for Chlamydiaceae in wild ruminant species from Switzerland, these data suggest that wild small mammals are unlikely to be important carriers or transport hosts for Chamydiaceae and Chlamydia-like organisms. DOI: https://doi.org/10.7589/2013-08-194 Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-87383 Journal Article Accepted Version Originally published at: Stephan, S; Guerra, D; Pospischil, A; Hilbe, M; Weissenböck, H; Novotny, L; Greub, G; Croxatto, A; Teifke, J P; Ulrich, R G; Schlegel, M; Ruhl, S; Schotte, U; Binder, A; Sauer, S; Borel, N (2014). Chlamydiaceae and chlamydia-like organisms in free-living small mammals in Europe and Afghanistan. Journal of Wildlife Diseases, 50(2):195-204. DOI: https://doi.org/10.7589/2013-08-194 1 1 Stephan et al. – Chlamydiae in wild small mammals. 2 OCCURRENCE OF CHLAMYDIACEAE AND CHLAMYDIA-LIKE ORGANISMS IN 3 FREE-LIVING SMALL MAMMALS IN EUROPE AND AFGHANISTAN 4 Sarah Stephan1, Diogo Guerra2, Andreas Pospischil1, Monika Hilbe1, Herbert 3 4 5 5 5 Weissenböck , Ladislav Novotný , Gilbert Greub , Antony Croxatto , Jens Peter 6 Teifke6, Rainer G. Ulrich6, Mathias Schlegel6, Silke Ruhl7, Ulrich Schotte7, Alfred 7 Binder7, Sabine Sauer8, Nicole Borel1* 8 1 Institute of Veterinary Pathology, University of Zurich, Vetsuisse Faculty Zurich, 9 Winterthurerstrasse 268, 8057 Zurich, Switzerland 10 2 Institute of Veterinary Parasitology, University of Zurich, Vetsuisse Faculty Zurich, 11 Winterthurerstrasse 266a, 8057 Zurich, Switzerland 12 3 Institute of Pathology and Forensic Veterinary Medicine, Department of Pathobiology, 13 University of Veterinary Medicine Vienna, Veterinärplatz 1, 1210 Vienna, Austria 14 4 Institute of Veterinary Pathology and Parasitology, Faculty of Veterinary Medicine, 15 University of Veterinary and Pharmaceutical Sciences Brno, Palackého 1/3, 61242 Brno, 16 Czech Republic 17 5 Institute of Microbiology, University Hospital Center and University of Lausanne, Rue du 18 Bugnon 48, 1011 Lausanne, Switzerland 19 6 Friedrich-Löffler-Institut, Federal Research Institute for Animal Health, Südufer 10, 17493 20 Greifswald-Insel Riems, Germany 21 7 Central Institute of the Bundeswehr Medical Service Kiel, Department of Veterinary 22 Medicine, Koppenpahler Allee 120, 24119 Kronshagen, Schleswig-Holstein, Germany 23 8 Central Institute of the Bundeswehr Medical Service Munich, Department of Veterinary 24 Medicine, Ingolstädter Landstrasse 102, 85748 Garching, Freistaat Bayern, Germany 25 2 26 Corresponding author: 27 Nicole Borel, DVM, FVH 28 Institute of Veterinary Pathology, Vetsuisse Faculty 29 University of Zurich, Winterthurerstrasse 268 30 CH-8057 Zurich, Switzerland 31 Tel.: +41-44-635-8576 32 Fax.: +41-44-635-8934 33 Email: [email protected] 34 Word count: Abstract: 220; Introduction –Discussion: 3,108 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 3 51 ABSTRACT 52 Few data are available on the occurrence of chlamydial infections in wild small 53 mammals. Therefore, the present study aimed to investigate the significance of free-living 54 small mammals as reservoirs or transmission hosts for chlamydiae. In total, 3,664 tissue 55 samples originating from 911 animals were collected in Switzerland, Germany, Austria, the 56 Czech Republic and Afghanistan. Samples included internal organs (n = 3,652) and feces (n 57 = 12) from 679 rodents (order Rodentia) and 232 insectivores (order Eulipotyphla) and were 58 tested by three different TaqMan real-time polymerase chain reactions (PCR) specific for 59 members of the family Chlamydiaceae and selected Chlamydia-like organisms such as 60 Parachlamydia spp. and Waddlia spp. Only one out of 911 (0.11%) animals exhibited a 61 questionable positive result by Chlamydiaceae specific real-time PCR. Furthermore, five out 62 of 911 animals (0.55%) were positive by specific real-time PCR for Parachlamydia spp. but 63 could not be confirmed by Parachlamydia acanthamoebae secY qPCR. One out of 746 64 animals (0.13%) showed a positive result by real-time PCR for Waddlia chondrophila. This 65 result was confirmed by Waddlia secY qPCR. This study represents the first detection of 66 Chlamydia-like organisms in small wildlife in Switzerland. Considering previous negative 67 results for Chlamydiaceae in wild ruminant species from Switzerland, these data suggest that 68 wild small mammals are unlikely to be important carriers or transport hosts for 69 Chamydiaceae and Chlamydia-like organisms. 70 71 Key words: Chlamydiaceae, Parachlamydia, Real-time PCR, Waddlia, wildlife 72 73 74 4 75 INTRODUCTION 76 Chlamydiae are an important group of obligate intracellular microorganisms which 77 cause a variety of diseases in mammals and birds (Longbottom and Coulter, 2003). 78 Chlamydia muridarum, the agent of the so-called Mouse Pneumonitis (MoPn), was 79 previously classified as a biovar of the species Chlamydia trachomatis. It is composed of 80 two strains, the Nigg strain (MoPn) and the SFPD strain (Zhang et al., 1993; Everett et al., 81 1999). Both have been isolated from laboratory mice and hamsters (Nigg, 1942; Stills et al., 82 1991). While C. trachomatis infects humans, the closely related C. muridarum species 83 naturally occurs in members of the family Muridae, producing a subclinical respiratory 84 infection in young laboratory Albino Swiss mice (Nigg and Eaton, 1944). C. muridarum 85 (MoPn) infection in laboratory mice was observed for the first time by Dochez et al. in 1937. 86 Moreover, as all oculo-genital strains of C. trachomatis are able to infect mice when 87 inoculated with highly infectious material (Storz and Page, 1971), laboratory mice became a 88 widely used animal model for the investigation of human chlamydial infections (Laitinen et 89 al., 1997). Strikingly, there is no report documenting isolation of C. muridarum from wild 90 rodents. In addition, no investigator has ever tried to isolate chlamydiae from wild 91 insectivores such as shrews, hedgehogs and moles. 92 Mouse models are widely used to provide insight into the pathogenesis of Chlamydia 93 abortus, the agent of ovine enzootic abortion (OEA) because mice show the same clinical 94 signs (abortion and pneumonia) as those observed in small ruminants (Caro et al., 2009). In 95 Switzerland, seroprevalence in small ruminants was highest (43%) in the Canton of Grisons 96 (Borel et al., 2004), where even wild ruminants are sporadic carriers of this abortigenic agent 97 (e.g., Holzwarth et al., 2011a,b). As interactions between domestic or wild ruminants and 98 free-living small mammals may occur on Alpine pastures, the role of the latter as reservoirs 99 of C. abortus and other Chlamydiaceae should be considered. 5 100 In the present survey, we also concentrated on a search for Chlamydia-like organisms 101 Parachlamydia acanthamoebae and Waddlia chondrophila. Both are considered to be 102 important emerging pathogens in animals with zoonotic potential (Greub and Raoult, 2002). 103 They might be regarded as new abortigenic agents in Swiss and Scottish cows (e.g., Ruhl et 104 al., 2009; Deuchande et al., 2010). Moreover, P. acanthamoebae has been associated with 105 ocular lesions in naturally infected guinea pigs (Lutz-Wohlgroth et al., 2006) and cats 106 (Richter et al., 2010) and was recently shown to produce pneumonia in an experimental 107 murine lung infection model (Casson et al., 2008b). Furthermore, Parachlamydia and 108 Waddlia DNA has been detected in different ruminant wildlife species in Switzerland 109 (Regenscheit et al., 2012) and even in environmental samples such as cattle drinking- and 110 well water (Wheelhouse et al., 2011; Codony et al., 2012). The potential of wild small 111 mammals being a source of Chlamydia-like organisms has so far not been investigated. 112 Therefore, the aim of the present study was to elucidate the occurrence of 113 Chlamydiaceae, with focus on C. muridarum and C. abortus as well as selected Chlamydia- 114 like organisms such as P. acanthamoebae and W. chondrophila in free-living small 115 mammals of different geographical regions in the Old World such as Switzerland, Germany, 116 Austria, the Czech Republic and Afghanistan. 117 MATERIALS AND METHODS 118 In total, 3,652 tissue samples and 12 fecal samples out of 911 wild small mammals of 119 20 different species were available from Switzerland (n = 490), Afghanistan (n = 379), 120 Germany (n = 29), Austria (n = 8) and the Czech Republic (n = 5) (Table 1).
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