Transmissible spongiform encephalopathies related to bovine spongiform encephalopathy in other domestic and captive wild species

Preferred citation: Anipedia, JAW Coetzer and P Oberem (Directors) In: Infectious Diseases of Livestock, JAW Coetzer, GR Thomson,
NJ Maclachlan and M-L Penrith (Editors). E Vallino-Costassa and T Konold, Transmissible spongiform encephalopathies related to bovine spongiform encephalopathy in other domestic and captive wild species, 2018.
Transmissible spongiform encephalopathies related to bovine spongiform encephalopathy in other domestic and captive wild species

Transmissible spongiform encephalopathies related to bovine spongiform encephalopathy in other domestic and captive wild species

Previous authors: R BRADLEY AND D W VERWOERD

Current authors:
E VALLINO COSTASSA - Doctor in Veterinary Medicine, DVM, PhD, Centre for Animal Encephalopathies (CEA), Istituto Zooprofilattico Sperimentale Piemonte Liguria e Valle d’Aosta, Turin, Italy
T KONOLD - Veterinary Surgeon, Information Officer & Veterinary Research Officer, DrMedVet, PhD, MRCVS, ASU, Pathology Department, APHA Weybridge, Woodham Lane, New Haw, Addlestone, Surrey, KT15 3NB, United Kingdom

Excluding human transmissible spongiform encephalopathies (TSEs) and scrapie, the only naturally occurring animal TSEs known in 1985, i.e. before the advent of bovine spongiform encephalopathy (BSE), were transmissible mink encephalopathy of Mustela vison reported in the United States, Canada, Finland, East Germany and USSR28 and chronic wasting disease (CWD) affecting wild cervids. This latter disease, until 2015, had been restricted to United States, Canada and South Korea. In 2016, a prion disease was reported for the first time in Europe in wild reindeer (Rangifer tarandus)5 which, although reported to be susceptible to oral challenge with CWD prions,31 had not previously been found to be naturally infected. Extended surveillance in Norway led to the detection of more cases in reindeer as well as red deer (Cervus elaphus) and moose (Alces alces).10 A positive moose was subsequently also identified in Finland; however, the pathological phenotype of the moose cases was different from reindeer. Further investigation into these cases are currently ongoing to determine the origin and cause of European cases.

In 1986, just before the first case of BSE was confirmed, a spongiform encephalopathy in a captive nyala (Tragelaphus angasi) in the UK was confirmed by microscopic examination of the brain. This was a prelude to other cases in captive wild members of the family Bovidae, such as greater kudu (Tragelaphus strepsiceros), Arabian oryx (Oryx leucoryx), eland (Taurotragus oryx),  gemsbok (Oryx gazella), nyala (Tragelaphus angasi), scimitar-horned oryx (Oryx dammah) and bison (Bison bison) as well as domestic Ankole cattle identified during the BSE epidemic.20 All these species were presumably exposed to contaminated meat and bone meal (MBM) derived from ruminants. Indeed, experimental transmission of kudu and nyala brain homogenates into mice showed pathology similar to BSE,23 supporting the hypothesis that spongiform encephalopathy in exotic ungulates was related to BSE.

It has been shown that classical BSE can be transmitted to red deer by intracerebral and oral routes. The clinical signs were similar to CWD but – unlike CWD – disease-associated prion protein (PrPSc) was not detected in lymphoid tissue. If BSE cases arose naturally in these animals, they could have been distinguished by the current confirmatory post-mortem tests.27

The possible spread of the BSE agent to small ruminants by feeding contaminated feedstuffs was a major concern in Europe, and TSE surveillance in small ruminants was increased as a consequence. Passage of the BSE agent in ‘new’ hosts may change strain properties and make it difficult to recognize the original strain and thereby increase the risk of epidemic spread. To date, there are no reports of naturally occurring BSE in sheep but since 2005, two natural BSE cases have been reported in goats.12, 38 Experimental studies to better characterize the classical BSE phenotype in the event that it is transmissible to sheep and goats have shown that both species are readily infected with the classical BSE agent and that PrPSc distribution is very similar to that observed in classical scrapie. This results in infectivity in all lymphoid tissues13, 14, 21 with some interspecies variability. Clinical signs were similar to classical scrapie in both species, with pruritus as a consistent finding in sheep.24, 25 Reduced susceptibility was associated with increasing age in sheep,19 and prion protein genotypes that confer resistance to classical scrapie, such as K222 in goats and A136R154R171 in sheep, also appeared to be associated with increased resistance to classical BSE.1, 30 Although classical BSE can be naturally transmitted in an experimental setting, the efficiency to transmit maternally and laterally was low.22 Thus, if individual sheep were infected naturally by consumption of BSE-contaminated meat and bone meal, it probably would not have been passed on sufficiently to other sheep to remain present in the flock.

In 1990, a naturally occurring TSE in a domestic cat was reported for the first time in the UK, soon to be followed by several other reports.15 Since 1990, 89 cases of feline spongiform encephalopathy (FSE) have been recorded in domestic cats in Great Britain, one in Ireland, one in Norway, one in Liechtenstein, one in Italy and two in Switzerland.11 The origin of infection in all cases appears most likely to be feed, but the precise source is unknown because of the varied diets of affected cats. Nevertheless, TSE-infected MBM seems a likely, if unproven, source.

All the cases of FSE described in cats demonstrate that most of the affected animals were male, of common European breed and between 4 and 9 years of age. The first signs consisted of behavioral changes characterized by sudden aggression or shyness...

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