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Besnoitiosis is caused by different species of intracellular protozoan parasites belonging to the family Sarcocystidae and affecting multiple host species worldwide
ten species are described infecting animals
donkeys and zebras and was described in Africa and in the USA where donkey besnoitiosis is considered as an emerging disease
A two-year-old male donkey was purchased in May 2016 in poor body condition (cachexia
alopetic areas and pruritus mainly on neck and head) by the present owner in Le Roeulx (Belgium) from a milk producing donkey farm in Frasnes-lez-Buissenal (Belgium)
hyperkeratosis (both flanks and neck) anorexia and cachexia
A treatment with phoxim was given with no improvement
A cutaneous biopsy of hyperkeratotic skin was performed in July
It showed a perivascular eosinophilic infiltrate with a large thick walled cyst located in the dermis containing numerous bradyzoites
This was highly suggestive of besnoitiosis
Several skin biopsy samples were obtained for qPCR analysis and confirmed the presence of Besnoitia spp
Further laboratory diagnosis tests were performed (western blot and rDNA sequencing) confirming Besnoitia bennetti aetiology for the male
haematology and qPCR were negatives but the western blot showed the presence of antibodies directed to Besnoitia spp
Further clinical examination performed in August highlighted scleral pinhead sized cysts (pearl) in the right eye and between nares
Another ten-year-old female donkey purchased in France and sharing the same accommodation showed a good clinical condition
but a thorough clinical examination showed the presence of numerous cysts on the inner face of upper labial mucosa
A daily treatment based on sulfamethaxzole and trimethoprim (Emdotrim 60% Mix®
30 mg/kg) was given orally and some improvement was noticed
This is the first evidence of Besnoitia bennetti infection (Protozoa: Apicomplexa) in donkeys (Equus asinus) in Belgium
we describe two cases of besnoitiosis in donkeys
a private veterinarian referred a donkey characterised by poor body condition and chronic skin lesions to the Faculty of Veterinary Medicine of Liège (Belgium)
Patient’s skin lesions: a alopetic and crusty area on the right shoulder
Shortly after its purchase, the animal was shorn revealing crusts and hyperkeratosis (on both flanks and the neck). The animal was anorexic and in poor body condition. A closer clinical examination in August highlighted scleral pinhead sized cysts (pearl) in the right eye and between nares (Fig. 2). The rest of the examination was unremarkable.
Scleral pin-head sized cysts (pearl; red arrow) between nares
Another ten year old female donkey (Grand noir du Berry breed)
purchased several years ago in France (Loire region) by the same owner and sharing the same accommodation
further clinical examination showed the presence of numerous cysts on the inner face of upper labial mucosa
The two donkeys were kept in a fenced area (below 1 ha)
The animals were fed a standard donkey food regimen composed of hay
supplemented with protein-containing grain (oats) and occasional fruits and vegetables
Previous medical treatments included routine vaccinations and prophylactic deworming (based on ivermectin)
chickens and rodents) had free access to the farm and the paddock buildings
Numerous flies were observed in the paddocks (Stomoxys calcitrans and Musca spp.)
Skin scrapings were performed in different places (mainly flanks and neck where the lesions were the most obvious) on both animals
A culture on Sabouraud dextrose agar-chloramphenicol (0.5 per 1000 m/w for three weeks at 37°C) yielded a negative result for ringworm
Microscopic examination of the hair revealed neither fungal spores nor ectoparasites
A Giemsa staining of an impression smear also gave negative results
Several skin biopsies were taken using an 8 mm biopsy punch
Histopathology and DNA extraction for qPCR and PCR were performed on those skin samples
the material was stored in 10% phosphate-buffered formalin for histological examination and in 70% ethanol for molecular analyses
The formalin-fixed sample was bisected and embedded in paraffin wax at 56 °C
cut and stained with haematoxylin and eosin for routine evaluation
This technique was performed by a veterinary diagnostic laboratory (Medvet
Histopathological preparation from the male donkey showing a cyst full of bradyzoites (haematoxylin eosin; 10×)
Several blood samples were taken for haematology and biochemistry analysis from both patients
A blood sample from the male gave unremarkable results except a light anaemia [haemoglobin 10.1 d/l (normal range 11–19 d/l)
red blood cells 5.22 106/mm3 (normal range 6.5–12.5 106/mm3)
an eosinophilia [15.5%; 1631/mm3 (normal range < 5% and < 500/mm3
respectively)] and an increased gamma globulin fraction [32.8%; 23.9 g/l (normal range 13–21% and 5.5–19 g/l
A blood sample from the female revealed only an eosinophilia (12.7%
Lane -: sera from uninfected cattle; Lane +: sera from infected cattle; Lane 1: sera from uninfected donkey; Lane 2: male serum (4/8/2016); Lane 3: female serum (4/8/2016); Lane 4: male serum (9/9/2016); Lane 5: female serum (9/9/2016)
The skin sample from the male was highly positive with a Ct of 25 but no Besnoitia DNA was detected in skin sample from the female
Phylogenetic tree based on 938 bp rDNA sequence (containing complete sequences of 5.8S gene and ITS1 and ITS2 fragments and partial sequences of 18S and 28S genes) reconstructed using NJ/MP/ML methods showing the position of the isolated Belgian strain (GenBank: MG652473) and other Besnoitia from cattle and goat deposited in the GenBank database
Bootstrap support (1000 replicates) is shown at each node as NJ/MP/ML; bootstrap values below 60% are not shown
The scale-bar indicates the number of substitutions per site
bennetti isolated from the equid host (donkey) was a distinct species to Besnoitia species (B
Taking all these results a diagnosis of besnoitiosis was established in both animals
A daily treatment based on sulfamethoxazole and trimethoprim (Emdotrim 60% Mix®
30 mg/kg) was given orally to the affected animal and some improvement was noticed
the affected animal was treated for four months with sulfamethoxazole and trimethoprim alongside a discontinued hepatoprotective treatment (Sédochol®)
The animal gained weight and no more skin conditions were visible
besnoiti will perhaps provide new molecular targets useful for species phylogeny and genetic population structure
very little data exists in the literature and these parameters do not seem to be of valuable assistance for diagnosis
it could be useful for a correct evaluation of renal function before sulfamethoxazole-trimethoprim treatment
neither isolation of parasites nor further molecular genotyping were achieved to determine the accurate Besnoitia species involved in these three studies
This first report of besnoitiosis in donkeys in Belgium suggests an urgent need for an extensive serological survey to assess prevalence in not only Belgian donkey populations but also in France
due to the geographical origin of the mare
Difficulties in confirming diagnoses and the absence of efficient treatment options are probably responsible for the underreporting of besnoitiosis in European donkeys
This report aimed to highlight to clinicians the necessity to include besnoitiosis in the differential diagnosis of chronic dermatitis unresponsive to routine topical and systemic treatments
Whether this finding represents an unusual cluster of infections or reflects a wider distribution of subclinical infections which have largely gone undetected to date requires further study
Donkeys are increasing in number and particularly in developing countries [36]
Widespread distribution of this infection would be of international concern and veterinary medical importance
This case report is the first unequivocal report of B
bennetti infection of donkey in Europe based on clinical
Further investigations are necessary to unravel the phylogeny of B
bennetti and its epidemiology in Europe and elsewhere
Bovine besnoitiosis: an emerging disease in Europe
taxonomy and epidemiology of Besnoitia species (Protozoa: Sarcocystidae)
A century of bovine besnoitiosis: an unknown disease re-emerging in Europe
The role of wild ruminants as reservoirs of Besnoitia besnoiti infection in cattle
Comparative evaluation of immunofluorescent antibody and new immunoblot tests for the specific detection of antibodies against Besnoitia besnoiti tachyzoites and bradyzoites in bovine sera
A review on bovine besnoitiosis: a disease with economic impact in herd health management
caused by Besnoitia besnoiti (Franco and Borges)
Genetic characterization of the causative agent of besnoitiosis in goats in Iran on the basis of internal transcribed spacer rDNA and its comparison with Besnoitia species of other hosts
First confirmed case of bovine besnoitiosis in an imported bull in Belgium
A peculiar equine Sarcosporidium in the Anglo-Egyptian Sudan
Globidosis - a cause of dermatitis in horses
Serological diagnosis of Besnoitia bennetti infection in donkeys (Equus asinus)
Besnoitia bennetti infection in miniature donkeys: an emerging protozoan of increasing concern
Investigation of an outbreak of besnoitiosis in donkeys in northeastern Pennsylvania
Immunodiagnosis of Besnoitia besnoiti infection by ELISA and Western blot
Experimental infections of rabbits with proliferative and latent stages of Besnoitia besnoiti
Development of a protocol testing the ability of Stomoxys calcitrans (Linnaeus
1758) (Diptera: Muscidae) to transmit Besnoitia besnoiti (Henry
MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets
Redescription of Besnoitia bennetti (Protozoa: Apicomplexa) from the donkey (Equus asinus)
Studies on besnoitiosis bennetti in miniature donkeys
Outbreak of besnoitiosis in donkeys (Equus asinus) in the south of Spain
Phylogenetic congruence of Sarcocystis neurona Dubey et al.
1991 (Apicomplexa: Sarcocystidae) in the United States based on sequence analysis and restriction fragment length polymorphism (RFLP)
Naturally acquired bovine besnoitiosis: histological and immunohistochemical findings in acute
An outbreak of besnoitiosis in miniature donkeys
A serosurvey of selected cystogenic coccidia in Spanish equids: first detection of anti-Besnoitia spp
Evidence for a recent population bottleneck in an apicomplexan parasite of caribou and reindeer
Traité de protozoologie médicale et vétérinaire
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for her kindness and help in handling the patients
and Amelia Coggon for review and improvement of the English language
The datasets used and/or analysed during the current study are available from the corresponding author upon reasonable request
Laboratoire de Parasitologie et Maladies Parasitaires
Caroline Vanvinckenroye & Yannick Caron
FP and SS performed serology and molecular biology
IT and CV performed the clinical part of the study
SV performed the histopathological part of the study
BL and MF read and improved the manuscript
All authors read and approved the final manuscript
The authors declare that they have no competing interests
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DOI: https://doi.org/10.1186/s13071-018-2993-3
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