Abstract
Borna disease (BD) is a sporadic neurologic disease of horses and sheep caused by mammalian Borna disease virus (BDV). Its unique epidemiological features include: limited occurrence in certain endemic regions of central Europe, yearly varying disease peaks, and a seasonal pattern with higher disease frequencies in spring and a disease nadir in autumn. It is most probably not directly transmitted between horses and sheep. All these features led to the assumption that an indigenous virus reservoir of BDV other than horses and sheep may exist. The search for such a reservoir had been unsuccessful until a few years ago five BDV-infected shrews were found in a BD-endemic area in Switzerland. So far, these data lacked further confirmation. We therefore initiated a study in shrews in endemic areas of Germany. Within five years 107 shrews of five different species were collected. BDV infections were identified in 14 individuals of the species bicolored white-toothed shrew (Crocidura leucodon, HERMANN 1780), all originating from BD-endemic territories. Immunohistological analysis showed widespread distribution of BDV antigen both in the nervous system and in epithelial and mesenchymal tissues without pathological alterations. Large amounts of virus, demonstrated by presence of viral antigen in epithelial cells of the oral cavity and in keratinocytes of the skin, may be a source of infection for natural and spill-over hosts. Genetic analyses reflected a close relationship of the BDV sequences obtained from the shrews with the regional BDV cluster. At one location a high percentage of BDV-positive shrews was identified in four consecutive years, which points towards a self-sustaining infection cycle in bicolored white-toothed shrews. Analyses of behavioral and population features of this shrew species revealed that the bicolored white-toothed shrew may indeed play an important role as an indigenous host of BDV.
Highlights
Borna disease viruses (BDVs) are nonsegmented negative stranded RNA viruses of the family Bornaviridae within the order Mononegavirales which replicate and transcribe in the nucleus of infected cells and use cellular splicing for generating some mRNAs [1,2,3]
The possibility of infections of humans with BDV was hypothesized over years based on antibody findings and later putative BDV sequences obtained from human specimens, but this has been questioned recently since reported human-derived BDV sequences proved to be inadvertent laboratory artefacts [23,24] and psychiatric syndromes could not be linked to BDV antibodies [25]; the specificity of antibodies against BDV in humans remains questionable since they have been found to be more frequent in patient groups with chronic diseases [26,27] which points towards a high percentage of immunological cross-reactivity not linked with BDV
This study provides evidence that C. leucodon, the bicolored white-toothed shrew, can harbor BDV without tissue damage in territories endemic for BD, whose BDV sequences fit to the epidemiological sequence cluster of the corresponding region
Summary
Borna disease viruses (BDVs) are nonsegmented negative stranded RNA viruses of the family Bornaviridae within the order Mononegavirales which replicate and transcribe in the nucleus of infected cells and use cellular splicing for generating some mRNAs [1,2,3]. The possibility of infections of humans with BDV was hypothesized over years based on antibody findings and later putative BDV sequences obtained from human specimens, but this has been questioned recently since reported human-derived BDV sequences proved to be inadvertent laboratory artefacts [23,24] and psychiatric syndromes could not be linked to BDV antibodies [25]; the specificity of antibodies against BDV in humans remains questionable since they have been found to be more frequent in patient groups with chronic diseases [26,27] which points towards a high percentage of immunological cross-reactivity not linked with BDV. The epidemiological pattern of BD as well as the geographic clustering indicates an existence of reservoir species for BDV [19]. It was a major breakthrough when BDV infections in bicolored white-toothed shrews (Crocidura leucodon) were reported from Switzerland [35,36]. The shrews had been trapped near locations where BD in horses had been reported in the years before
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