Borna disease outbreak with high mortality in an alpaca herd in a previously unreported endemic area in Germany

Abstract

Borna disease virus 1 (BoDV‐1) is the causative agent of Borna disease, an often fatal neurologic condition of domestic mammals, including New World camelids, in endemic areas in Central Europe. Recently, BoDV‐1 gained further attention by the confirmation of fatal zoonotic infections in humans. Although Borna disease and BoDV‐1 have been described already over the past decades, comprehensive reports of Borna disease outbreaks in domestic animals employing state‐of‐the‐art diagnostic methods are missing. Here, we report a series of BoDV‐1 infections in a herd of 27 alpacas (Vicugna pacos) in the federal state of Brandenburg, Germany, which resulted in eleven fatalities (41%) within ten months. Clinical courses ranged from sudden death without previous clinical signs to acute or chronic neurologic disease with death occurring after up to six months. All animals that underwent necropsy exhibited a non‐suppurative encephalitis. In addition, six apparently healthy seropositive individuals were identified within the herd, suggesting subclinical BoDV‐1 infections. In infected animals, BoDV‐1 RNA and antigen were mainly restricted to the central nervous system and the eye, and sporadically detectable in large peripheral nerves and neuronal structures in other tissues. Pest control measures on the farm resulted in the collection of a BoDV‐1‐positive bicoloured white‐toothed shrew (Crocidura leucodon), while all other trapped small mammals were negative. A phylogeographic analysis of BoDV‐1 sequences from the alpacas, the shrew and BoDV‐1‐positive equine cases from the same region in Brandenburg revealed a previously unreported endemic area of BoDV‐1 cluster 4 in North‐Western Brandenburg. In conclusion, alpacas appear to be highly susceptible to BoDV‐1 infection and display a highly variable clinical picture ranging from peracute death to subclinical forms. In addition to horses and sheep, they can serve as sensitive sentinels used for the identification of endemic areas.

Astrovirus-Associated Polioencephalomyelitis in an Alpaca

“…Histopathology of the spinal cord and brain revealed a non-suppurative polioencephalomyelitis with neuronal necrosis and gliosis, and a viral etiology was considered to be most likely the cause of disease. Rabies and borna disease are among possible viral agents for non-suppurative encephalitis in alpacas, and were first ruled out by IHC [27][28][29]. When performing IHC on the brain and spinal cord against two different epitopes of BoAstV-CH13/NeuroS1, cells morphologically compatible with neurons were distinctly stained, demonstrating the presence of a virus with similar or identical antigenetic structure to BoAstV-CH13/NeuroS1.…”

Investigation of fatal human Borna disease virus 1 encephalitis outside the previously known area for human cases, Brandenburg, Germany – a case report

“…A possible BoDV-1 etiology of this cryptic encephalitis case was retrospectively investigated 3 years post mortem, triggered by media reports on zoonotic BoDV-1 infections [ 2 ] and by recent BoDV-1 infections reported from alpacas at a farm near to the patient’s home [ 9 ]. Neither serum nor CSF of the patient were available for serological examination.…”

“…1 A). Cluster 3 is known to be endemic in parts of the neighboring federal states of Saxony-Anhalt and Saxony, whereas known BoDV-1 sequences from alpacas and horses in Brandenburg so far belonged to cluster 4 [ 9 ] (Fig. 1 A and B).…”

“…Cluster designations, host and geographic origin are indicated according to previously published work [ 1 – 3 , 7 , 9 – 13 ]. B The human case reported in this study is presented together with previously published BoDV-1 infections of alpacas and horses in Brandenburg and sequence-confirmed BoDV-1 infections of shrews (triangles), domestic mammals (circles) and humans (squares) with available geographic localization in known endemic regions [ 1 – 3 , 7 , 9 – 13 ]. Colors represent regional BoDV-1 sequence clusters (see Figure 1A).…”

“…The likely place of infection lies on the northern fringe of the geographical area known to be endemic for BD on the North German plains. In March 2020, BoDV-1 infections were reported from an alpaca farm and two horses within a 35 km radius surrounding the patient’s home [ 9 ].…”