New World camelids are sentinels for the presence of Borna disease virus

Abstract

Borna disease (BD), a frequently fatal neurologic disorder caused by Borna disease virus 1 (BoDV-1), has been observed for decades in horses, sheep, and other mammals in certain regions of Europe. The bicoloured white-toothed shrew (Crocidura leucodon) was identified as a persistently infected species involved in virus transmission. Recently, BoDV-1 attracted attention as a cause of fatal encephalitis in humans. Here, we report investigations on BoDV-1-infected llamas from a farm in a BD endemic area of Switzerland, and alpacas from holdings in a region of Germany where BD was last seen in the 1960s but not thereafter. All New World camelids showed apathy and abnormal behaviour, necessitating euthanasia. Histologically, severe non-suppurative meningoencephalitis with neuronal Joest-Degen inclusion bodies was observed. BoDV-1 was confirmed by immunohistology, RT-qPCR, and sequencing in selected animals. Analysis of the llama herd over 20 years showed that losses due to clinically suspected BD increased within the last decade. BoDV-1 whole-genome sequences from one Swiss llama and one German alpaca and-for comparison-from one Swiss horse and one German shrew were established. They represent the first published whole-genome sequences of BoDV-1 clusters 1B and 3, respectively. Our analysis suggests that New World camelids may have a role as a sentinel species for BoDV-1 infection, even when symptomatic cases are lacking in other animal species.

Borna disease virus 1 infection in alpacas: Comparison of pathological lesions and viral distribution to other dead-end hosts

“…42,43,61 Thereby, the virus can be transmitted not only within its reservoir species but also to other mammals, including horses, sheep, New World camelids, and humans. 8,34,41,47,52 In addition, singular cases of natural BoDV-1 infections have been reported and confirmed in cats, dogs, cattle, and goats. 5,9,62 For these spillover hosts, an intranasal route of entry was suspected, followed by a spread to the central nervous system (CNS) in which high viral loads were detectable.…”

“…10,21,60,61,63 However, a mortality rate of roughly 40% was recently reported in an alpaca herd in a novel endemic area in Brandenburg, a federal state of Germany, 52 and New World camelids are discussed as a sentinel species for BoDV-1 infections. 34 To date, only single reports have described BD in New World camelids, 26,27,34 and a comprehensive study of respective histopathological lesions of BD in this species is lacking.…”

Borna Disease Virus 1 (BoDV-1): Aktueller Stand und Perspektiven

“…Die BoDV-1-Sequenzen von Spitzmäusen und Fehlwirten clustern regional, was am Ehesten für eine Übertragung des Virus von Spitzmäusen, möglicherweise über ihre Ausscheidungen, auf die Fehlwirte ("Spill-over") spricht [16]. Die Fehlwirte selbst, zu denen neben Pferden, Schafen und Alpakas [27,28] auch in seltenen Fällen Haussäugetiere wie Hund und Katze sowie Zoosäugetiere zählen, gehören dagegen nicht zu den Überträgern des Virus.…”

Lamas und Alpakas – der neurologische Patient

“…Unter den viral bedingten Enzephalopathien kommt derzeit unter den Neuweltkamelen dem Borna Disease Virus 1 (BoDV-1) die größte Bedeutung zu 19 , 21 . Das BoDV-1 ist gegenwärtig endemisch in bestimmten Regionen der Schweiz, Deutschland, Liechtenstein und Österreich 20 , 21 . Der letzte größere Ausbruch betraf mehrere Alpakas in einer Region Ostdeutschlands, die klinisch eine Verhaltensänderung, Ataxien, Kreisbewegungen Opisthotonus, Krämpfe oder Tremor zeigten 21 .…”

“…Eine in Österreich durchgeführte Seroprävalenzstudie verdeutlichte den stattfindenden Kontakt von Lamas und Alpakas mit dem Virus 27 . Als geeigneter Nachweis einer Infektion am lebenden Tier gilt die Antikörper-Titerbestimmung; der direkte Nachweis von Virus-RNA gelingt beim toten Tier aus Anteilen des ZNS 20 , 21 .…”