Cowpox Virus Outbreak in Banded Mongooses (Mungos mungo) and Jaguarundis (Herpailurus yagouaroundi) with a Time-Delayed Infection to Humans

et al. (2009) Cowpox Virus Outbreak in Banded Mongooses (Mungos mungo) and Jaguarundis (Herpailurus yagouaroundi) with a Time-Delayed Infection to Humans. PLoS ONE 4(9): e6883. doi:10.1371/journal.pone.0006883 Cowpox Virus Outbreak in Banded Mongooses (Mungos mungo ) and Jaguarundis (Herpailurus yagouaroundi ) with a Time-Delayed Infection to Humans Andreas Kurth 0 Martin Straube 0 Annette Kuczka 0 Anton Josef Dunsche 0 Hermann Meyer 0 Andreas 0 Art F. Y. Poon, University of California San Diego, United States of America 0 1 German Consultant Laboratory for Poxviruses, Robert Koch Institute , Berlin, Germany, 2 Zoo Krefeld, Krefeld, Germany, 3 Chemisches- und Veterina runtersuchungsamt Rhein-Ruhr-Wupper, Krefeld, Germany, 4 Sta dtisches Klinikum Karlsruhe, Karlsruhe, Germany , 5 Bundeswehr Institute of Microbiology , Munich , Germany Background: Often described as an extremely rare zoonosis, cowpox virus (CPXV) infections are on the increase in Germany. CPXV is rodent-borne with a broad host range and contains the largest and most complete genome of all poxviruses, including parts with high homology to variola virus (smallpox). So far, most CPXV cases have occurred individually in unvaccinated animals and humans and were caused by genetically distinguishable virus strains. Methodology/Principal Findings: Generalized CPXV infections in banded mongooses (Mungos mungo) and jaguarundis (Herpailurus yagouaroundi) at a Zoological Garden were observed with a prevalence of the affected animal group of 100% and a mortality of 30%. A subsequent serological investigation of other exotic animal species provided evidence of subclinical cases before the onset of the outbreak. Moreover, a time-delayed human cowpox virus infection caused by the identical virus strain occurred in a different geographical area indicating that handling/feeding food rats might be the common source of infection. Conclusions/Significance: Reports on the increased zoonotic transmission of orthopoxviruses have renewed interest in understanding interactions between these viruses and their hosts. The list of animals known to be susceptible to CPXV is still growing. Thus, the likely existence of unknown CPXV hosts and their distribution may present a risk for other exotic animals but also for the general public, as was shown in this outbreak. Animal breeders and suppliers of food rats represent potential multipliers and distributors of CPXV, in the context of increasingly pan-European trading. Taking the cessation of vaccination against smallpox into account, this situation contributes to the increased incidence of CPXV infections in man, particularly in younger age groups, with more complicated courses of clinical infections. - Attention was first drawn to poxviruses infecting exotic zoo animals in 1960, when, still in the era of smallpox vaccination, two captive Asian elephants died at the Zoological Garden in Leipzig/ Germany [1]. At that time, the causative agent was believed to be vaccinia virus (VACV) that was most probably transmitted by recently vaccinated children to the elephants. However, this hypothesis was never proven. The fact that mandatory smallpox vaccination was abolished in Europe in 1980 with poxvirus outbreaks still occurring in Continental European and British zoos and circuses argues against VACV as their causative agent. To date, more than 30 outbreaks have been reported, affecting various species (Table 1). Virus isolates obtained from these outbreaks have been retrospectively characterized as cowpox virus (CPXV). CPXV belong to the genus Orthopoxvirus (OPV) of the family Poxviridae. Virions are brick-shaped with a size of around 200 nm in diameter and 350 nm in length and carries its genome of approx. 230 kbp in a single, linear, double-stranded segment of DNA [2]. Several often fatal infections among zoo and circus elephants have been reported mainly from Germany (Table 1). As a consequence, elephants are routinely vaccinated with the attenuated modified vaccinia virus Ankara (MVA) strain of vaccinia virus [3,4]. For other exotic zoo animals, very little is known about successful vaccination and immune response to a vaccinia cowpox infection. The most dramatic outbreaks in exotic animals known so far occurred in the Moscow Zoo in 1973 and 1974, causing serious illness in six different species of the family Felidae [5]. Virus was recovered from 18/19 animals examined. Based on large intracellular eosinophilic A-type inclusion bodies and the appearance of hemorrhagic pocks on the chorioallantoic membrane of embryonated hens eggs, it was characterized as CPXV. The origin of this virus appears to have been epizootics of poxvirus infections in colonies of white rats which were used as food for the carnivores [6]. In those epizootics a case-fatality rate exceeding No of animals with clinical signs Essbauer unpublished 2007 Asian elephant (Elephas maximus) African elephant (Loxodonta africana) Lion (Panthera leo) Black panther (Panthera padus) Cheetah (Acinonyx jubatus) Puma (Felis concolor) Jaguar (Felis onca) Ocelot (Felis pardalis) Far eastern cat (Felis bengalis) Okapi (Okapia johnstoni) Anteater (Myrmecophaga tridactyla) Black rhinoceros (Diceros bicornis) White rhinoceros (Ceratotherium s. simum) Llama (Lama glama pacos) Red panda (Ailurus fulgens) Beaver (Castor fibor canadensis) Macaques (Macaca spec.) nk: not known. doi:10.1371/journal.pone.0006883.t001 Patagonian cavy (Dolichotis patagonum) Geographic origin (outbreaks) 30% could be observed. It was assumed that the white rats were infected by accidental contact with wild Norwegian rats (Rattus norvegicus). Experiments performed by Maiboroda demonstrated that Norwegian rats could be productively infected with CPXV and could shed significant amounts of virus, especially if under stress [7]. A potential role of rats as part of the chain of transmission has been emphasized from an outbreak in a circus in Northern Germany, where all virus isolates obtained from asymptomatic rats, the deceased elephant and the locally infected animal care taker had an identical sequence of the hemagglutinin gene [8]. CPXV occurs naturally in several species of rodents in Europe and Western parts of Russia [2]. Although serological surveys demonstrated a high proportion of seropositive bank voles (Clethrionomys glareolus), field voles (Microtus agrestis) and wood mice (Apodemus sylvaticus) [912], no virus isolate has been obtained from these species so far. Experimental CPXV infection in bank voles, one of the main reservoir hosts, yielded only low infectious titers of CPXV [13]. This points to a co-evolution of virus and host over years. On the other hand, the fatal outcome in large felids, elephants and other exotic species indicates that these species are highly susceptible hosts. In this respect, the role of rats has not yet been elucidated. Wild rats could be either a primary reservoir or an amplifying host. Little is also known about the (...truncated)