Analysis of exotic squirrel trade and detection of human infections with variegated squirrel bornavirus 1, Germany, 2005 to 2018

摘要

Following the discovery in 2015 of the variegated squirrel bornavirus 1 (VSBV-1) in fatal encephalitis cases among exotic squirrel breeders and a zoo animal caretaker in Germany, a case definition was developed. It was employed during trace-back animal trade investigations and sero-epidemiological studies among breeders and zoo animal caretakers of holdings with VSBV-1 infected squirrels. During the investigation, two possible human cases who had died of encephalitis were identified retrospectively among the squirrel breeders. Moreover, one probable human case was detected among the breeders who had a positive memory T-cell response to VSBV-1 antigen and antibodies against VSBV-1. The low rate of seropositivity found among living persons in risk groups that handle exotic squirrels privately or at zoos may reflect rareness of exposure to VSBV-1 during animal contact, a high lethality of infection or a combination of these factors. As a precaution against human exposure, testing of exotic squirrels for VSBV-1 infection and/or avoiding direct contact with exotic squirrels in zoos and private holdings is strongly advised. Keywords: exotic pets, animal trade, variegated squirrel bornavirus 1, case definition, serology, epidemiology, viral infections, encephalitis, viral encephalitis, surveillance, laboratoryBackgroundIn 2015, the variegated squirrel bornavirus 1 (VSBV-1, species Mammalian 2 orthobornavirus ) was discovered as an emerging zoonotic pathogen responsible for three cases of fatal encephalitis among private breeders of exotic squirrels in Germany [1]. All three were male, resident in the state of Saxony-Anhalt (Cases A, B, C) and had succumbed to encephalitis between 2011 and 2013. All had kept variegated squirrels ( Sciurus variegatoides ), an exotic squirrel species from Central America. Recently, in early 2018, the virus was retrospectively detected also in the brain of a zoo animal caretaker from the German state of Schleswig-Holstein (Case D). This female patient had had occupational contact to an infected Prevost’s squirrel ( Callosciurus prevostii ), an exotic species from Southeast Asia. She had died of limbic encephalitis in 2013 [2]. VSBV-1 has been tentatively classified as a biosafety level 3 pathogen. The incubation time and the mode of transmission have not been determined. Animal scratches and bites are considered the main risk factor [1].Following the retrospective detection in 2015 of the VSBV-1 encephalitis cluster among the breeders of variegated squirrels [1], the European Centre for Disease Prevention and Control (ECDC) issued a rapid risk assessment. It stressed the need for investigations into the natural hosts, reservoirs and transmission route of the virus owing due to the novel nature of the event [3]. As a precautionary measure, direct contact to exotic squirrels should be avoided. Since then, molecular testing for VSBV-1 infection among exotic squirrel species has been performed in Germany in private holdings and zoos and has been recommended as a standard measure to reduce the risk of human infection. VSBV-1-positive exotic squirrels and/or humans were identified at seven private holdings (including the holdings of Cases A, B and C) and four zoos (including the zoo where Case D had worked) between 2015 and 2017 [4,5]. Testing of exotic squirrels in Germany is continuously ongoing.Here, we report an epidemiological investigation of the exotic squirrel trade between private holdings, the detection of additional human fatalities linked to VSBV-1 among squirrel breeders, and a serological study of past VSBV-1 infections among private squirrel breeders and zoo animal caretakers in Germany.MethodsEpidemiology and human case findingTrace-back interviews about exotic squirrel trading were conducted between 2015 and 2018 in the private holdings of the three squirrel breeders who had died of VSBV-1 encephalitis [1] and in four further holdings where VSBV-1-infected squirrels had been found previously [4,5]. We contacted squirrel breeders and holders identified by the tracing of the animal trade, as well as their household members, by telephone or email. In systematic questionnaire-based interviews, the participants were asked about the history of their holdings, their general husbandry management, trading contacts and animal exchange with others (squirrel species, year of trade), and rate of contact to the animals (regularly, occasionally, rarely). We identified contact holdings and offered them diagnostic testing of their squirrels, accompanied with a questionnaire-based interview. Because there was no registry of squirrel owners or documentation on the individual animal exchanges between the holdings, the data on the trading contacts were based on the participants’ memories. Interview participants were also asked to take part in a serosurvey for past VSBV-1 infection.Zoos were informed, by the federal states’ authorities and by scientific lectures at meetings of the German Zoolog