Mysterious parasitic disease of equines confirmed in donkeys in Britain

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Besnoitia bennetti cysts in the eye of a 5-year-old donkey. The cysts appear as multiple, up to 1 mm in diameter, round, white and firm nodules (arrow). Photo: Elsheikha et al. https://doi.org/10.1186/s13071-020-04145-8

A chronic and debilitating parasitic equine disease which causes eye lesions and skin lumps has been confirmed in donkeys in Britain for the first time.

Equine besnoitiosis can affect donkeys, horses, zebras and mules.

It was confirmed in 20 donkeys under the care of The Donkey Sanctuary, with researchers saying more work is needed to learn more about its possible occurrence, characteristics, and clinical manifestations in donkeys and other equids.

“At present, it cannot be certain whether Besnoitia infection is confined to the donkey population or whether it has not been identified yet in other equines in the UK,” the research team reported in the journal Parasites & Vectors.

“Further studies to establish whether the cysts are also present in the horse and pony populations are warranted.”

The infected donkeys had never lived outside the UK, except for one who came from Ireland.

All were kept on various Donkey Sanctuary sites in East Devon and a single location in Dorset.

Besnoitiosis was first described in Sudan in the 1920s. In Europe, the parasitic disease was first reported in France in 1922.

The disease is a result of infection with the protozoan parasite Besnoitia bennetti. It typically gives rise to multiple, pinpoint, raised, round, yellow-to-white cysts in the skin over the head and body. Lesions can also develop in the eyes.

Besnoitiosis in donkeys has gone from being a rarely detected parasite to being reported in donkeys in many countries, including the United States, Spain, Belgium, Italy and Portugal.

“This increase in the number of reports of B. bennetti infection in donkeys and other equids is probably attributed to the increasing awareness of the disease,” the researchers, comprising experts from the University of Nottingham and The Donkey Sanctuary, said.

Mysterious disease

There are many unanswered questions around the disease and the parasite that causes it, with little known about its life cycle and route of transmission.

“This raises the question about the source of infection and possible route of transmission in donkeys in the UK,” the study team, led by the university’s Dr Hany Elsheikha, an Associate Professor of Parasitology, said.

“Since its discovery, the route of B. bennetti transmission has not been clearly defined.”

One of the most unique features of besnoitiosis is the development of tiny cysts on the eye surface.

Some infected animals can remain otherwise healthy, while others suffer weight loss, malaise and generalized dry skin.

However, this has not been observed in the British cases, which chiefly involved small skin masses with little involvement of the eyes.

“There was limited health impact on the donkeys concerned,” the study team said.

Although many of the clinical signs associated with besnoitiosis have not been seen in the cases identified in Britain, the study has important clinical relevance.

First case seen in 2013

Besnoitiosis was discovered in 2013 in a donkey with the charity. The animal had skin lumps that were presumed to be sarcoid tumours.

However, microscopic examination of the affected skin tissue revealed cysts similar to those caused by  Besnoitia bennetti.

Since then, 19 other donkeys with skin masses were also found to have Besnoitia cysts. Anti-Besnoitia antibodies were found in some serum samples, and molecular-based testing confirmed the presence of the parasite.

“Since then, Besnoitia cysts have become a routine differential diagnosis for skin masses by the local veterinary team,” the researchers reported.

Besnoitia cysts should now be included as a differential diagnosis for sarcoids in Britain, at least in donkeys, they said.

The first case triggered a collaboration between a team of clinicians from The Donkey Sanctuary and a veterinary parasitologist from the School of Veterinary Medicine and Science at the University of Nottingham.

Dr Rebekah Sullivan, co-author of the report and a vet at the Donkey Sanctuary, said: “Given the relative proximity to other European countries, where clinical besnoitiosis is apparent, our findings will inform British vets of the potential for this emerging disease so that they can better recognise the pattern of clinical signs during clinical examination.”

Dr Elsheikha added: “It is absolutely essential – particularly now – that vets in the UK learn more about besnoitiosis, so they can identify and protect donkeys potentially at risk.

“Knowledge obtained in this study should improve our response to this emerging parasitic disease in donkeys in the UK, especially with the few treatment options and the unknown routes of transmission.”

Several serological methods and screening strategies have been developed to help guide veterinarians to earlier diagnosis and treatment of the disease.

Gereon Schares from the Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, in Germany, and co-author of the report, said: “This study is particularly important because by using a suite of molecular methods we were able to confirm for the first time in Europe that the parasite agent involved in these cases is specifically Besnoitia bennetti and infection can be shown by serological methods.”

The correct identification of Besnoitia cysts in skin biopsies taken from UK donkeys does have a clinical advantage for veterinarians, providing more accurate prognoses where a skin mass has been identified.

“It can no longer be assumed that skin masses are either neoplastic in origin or inflammatory, such as eosinophilic granulomas, for example,” said George Paraschou, co-author and pathologist at the Donkey Sanctuary.

Eight of the 20 donkeys identified with Besnoitia cysts are still alive.

Route of transmission

Since its discovery, the route of B. bennetti transmission has not been clearly defined by scientists, the researchers say.

Attempts to identify the definitive host for B. bennetti have been unsuccessful, precluding researchers from understanding more about the parasite’s life-cycle.

“All the donkeys described in this case series were kept in large groups on sites within a limited geographical range in East Devon and Dorset in England,” they wrote.

It is possible, they said, that some factors specific to this group, such as the potential for transmission by blood-sucking insect vectors, may have aided B. bennetti transmission in these donkeys, similar to Besnoitia infection in cattle.

“However, the role of insect vectors in the transmission of donkey besnoitiosis has yet to be identified.

“Given the large number of donkeys kept on these sites, and the low case incidence, it can be assumed that the transmission rate remains low.

“However, we cannot be certain that we have identified and diagnosed all cases so far.

“Further studies are required to identify potential perpetuating factors, such as underlying disease, co-infection, the presence of potential wildlife reservoirs, or climatic conditions.”

They say that ongoing monitoring and investigation of clinical cases is justified to learn more about any negative impact the presence of Besnoitia cysts may have on the donkeys.

“Given the lack of effective chemotherapeutic treatment for besnoitiosis, further research is required to determine the optimal treatment regimen, if any, for B. bennetti infection affecting donkeys.

“In the cases presented here, it is apparent that symptomatic treatment of associated inflammation is all that has been required.”

They continued: “Given the relative proximity to other European countries, where clinical besnoitiosis is apparent, UK veterinarians should be aware of the potential for this disease and the pattern of clinical signs during clinical examination.”

More effort is also needed, they say, to understand the parasite at a genetic level.

“This will improve the understanding of the epidemiology and the spread of besnoitiosis in donkeys and other equids, which may ultimately impact clinical management of equine besnoitiosis.”

First record of besnoitiosis caused by Besnoitia bennetti in donkeys from the UK
Hany M. Elsheikha, Gereon Schares, Georgios Paraschou, Rebekah Sullivan and Richard Fox
Parasites & Vectors (2020) 13:279 https://doi.org/10.1186/s13071-020-04145-8

The study, published under a Creative Commons License, can be read here

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