A broad spectrum screening of Schmallenberg virus antibodies in wildlife animals in Germany

Mouchantat et al. Veterinary Research (2015) 46:99 DOI 10.1186/s13567-015-0232-x SHORT REPORT VETERINARY RESEARCH Open Access A broad spectrum screening of Schmallenberg virus antibodies in wildlife animals in Germany Susan Mouchantat1, Kerstin Wernike2*, Walburga Lutz3, Bernd Hoffmann2, Rainer G. Ulrich4, Konstantin Börner5, Ulrich Wittstatt6 and Martin Beer2 Abstract To identify native wildlife species possibly susceptible to infection with Schmallenberg virus (SBV), a midge-transmitted orthobunyavirus that predominantly infects domestic ruminants, samples from various free-living ruminants, but also carnivores, small mammals and wild boar were analyzed serologically. Before 2011, no SBV-specific antibodies were detectable in any of the tested species, thereafter, a large proportion of the ruminant population became seropositive, while every sample taken from carnivores or small mammals tested negative. Surprisingly, SBV-specific-antibodies were also present in a large number of blood samples from wild boar during the 2011/2012 and 2012/2013 hunting seasons. Hence, free-ranging artiodactyls may play a role as wildlife host. Introduction, methods and results Schmallenberg virus, a midge-transmitted orthobunyavirus, was initially detected in domestic ruminants near the German/Dutch border in late 2011 [1]. Since then, the virus spread very rapidly among European livestock. After the first vector season a very high seroprevalence of approximately 70% to nearly 100% was observed in domestic ruminants in the centre of the epidemic in North-Western Germany, the Netherlands and Belgium [2-5]. In the following vector season, SBV still circulated in that area, but at a much lower level [6], and in 2013, cases of viral genome detection were reported only sporadically to the German Animal Disease Reporting System (TSN). However, in summer and autumn 2014, SBV reappeared to a greater extent [7] and the reasons for that observation are not completely elucidated until now. One possible explanation could be the existence of transient reservoir hosts for the virus apart from the major target species. Until now, viral genome or specific antibodies were detected predominantly in domestic and wild ruminants, such as cattle, sheep, goats, mouflon, bison, moose, alpacas, buffalos, bison, and deer [8-12]. However, antibodies were also found in a dog in Sweden [13], and type I interferon receptor knock-out mice are * Correspondence: 2 Institute of Diagnostic Virology, Friedrich-Loeffler-Institut (FLI), Südufer 10, 17493 Greifswald, Insel Riems, Germany Full list of author information is available at the end of the article susceptible to an experimental SBV-infection [14]. To examine whether free-living carnivores or small mammals, i.e. rodents and shrews, may be infected by SBV, 339 blood samples from a variety of carnivores (red fox Vulpes vulpes, raccoon dog - Nyctereutes procyonoides, raccoon - Procyon lotor, marten - Martes spp.) as well as 195 samples from small mammals (members of the families Muridae, Cricetidae and Soricidae; approved by the competent authority, LANUV NRW, ref. 8.8751.05.20.09.210) were collected between 2011 and 2012 and tested for the presence of SBV-specific antibodies. Though the detection of specific antibodies does not inevitably reflect a productive infection, the short viraemia of only a few days [1,15] makes the detection of anti-SBV antibodies to a much more promising diagnostic test system than the detection of the virus itself, especially for epidemiological investigations. Wild boar (Sus scrofa), considered as a reservoir for several viruses of livestock and humans, is the second most abundant ungulate in Europe. Based on official hunting statistics Germany is one of the countries with the highest population densities of wild boar in Europe [16]. In previous investigations neutralizing antibodies against Akabane virus, a member of the Simbu sero-group of the genus Orthobunyavirus, were detected in warthogs and bush pigs in Africa [17,18] and in pigs in Taiwan [19]. © 2015 Mouchantat et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Mouchantat et al. Veterinary Research (2015) 46:99 Page 2 of 5 To investigate whether wild boar are susceptible to an SBV-infection and may serve as a reservoir, a total of 2077 blood samples taken post mortem in 2006 and between August 2010 and December 2013 was analyzed for the presence of SBV-specific antibodies. 1646 of the 2077 samples were collected in North Rhine-Westphalia, the German federal state where the first case of SBVinfection was detected [1]. In the 2013/2014 hunting seasons, predominantly young animals (<1 year) were sampled. In addition, samples from European mouflon (Ovis orientalis musimon), as a wild sheep the only freeliving wild form of susceptible domestic animals in Germany, and further free-living ruminants such as roe deer (Capreolus capreolus), fallow deer (Dama dama), red deer (Cervus elaphus), and sika deer (Cervus nippon) were analyzed (Table 1). Blood samples from deer and mouflon as well as wild boar and carnivores were collected in cooperation with local hunters according to the appropriate German legislation. No ethical/welfare authority approval was required as samples were collected post-mortem by the hunters. All blood samples were examined with an indirect or a competitive commercially available SBV-antibody ELISA (ID Screen® Schmallenberg virus Indirect or ID Screen® Schmallenberg virus Competition, both IDvet, Grabels, France) according to the manufacturer’s recommendations. In the indirect ELISA kit an Anti-multi-species IgG-HRP conjugate is included. Samples with a doubtful ELISA result as well as a representative number of samples from each species with positive and negative ELISA results were retested Table 1 Serological results of German wildlife screening for Schmallenberg virus infection Species Mouflon Deera Carnivoresb c Small mammals Hunting season Samples Positive or time period (%) Negative (%) 2011/2012 4 4 (100) 0 2012/2013 31 26 (83.87) 5 (16.13) 2013/2014 9 3 (33.33) 6 (66.67) 2000/2001 134 0 134 (100) 2011/2012 136 41 (30.15) 95 (69.85) 2012/2013 760 278 (36.58) 482 (63.42) 2013/2014 324 65 (20.06) 259 (79.94) 2014/2015 4 2 (50) 2 (50) 2011/2012 281 0 281 (100) 2012/2013 58 0 58 (100) 2011-2012 195 0 195 (100) The results are divided by species and hunting seasons (hunt (...truncated)