Analyze Diet
Irish veterinary journal2024; 77(1); 2; doi: 10.1186/s13620-024-00263-2

First report of Besnoitia bennetti in Irish donkeys: an emerging parasitic disease in Europe.

Abstract: This is the first report of Besnoitia bennetti in donkeys in Ireland. B. bennetti, an apicomplexan protozoan parasite specific to equids, is an emerging pathogen in Europe. This parasite forms chronic intracytoplasmic cysts in cells of the mesenchymal lineage, mainly fibroblasts, in the skin, sclera and mucosa. Clinical signs in affected equine hosts vary from mild to severe debilitating disease. Little is known of the phylogeny, epidemiology or transmission of B. bennetti infection in donkeys, mules or horses. Methods: Two cases of besnoitiosis in donkeys are presented. Both donkeys were born and raised in theSouthwest of Ireland. The first case was a 2.5-year-old donkey that had a suspect sarcoid removed, while the second case,a 2-year-old donkey, had a biopsy of nodular dermatitis of the muzzle. Diagnosis was made by histopathology and the parasite species, B. bennetti, was confirmed by PCR followed by sequencing and microsatellite analysis. Both donkeys had high antibody titres against Besnoitia spp. Small (0.5 mm) scleral, conjunctival and dermal cysts over the muzzle were subsequently observed in both animals. Treatment with trimethoprim sulfadiazine for 30 days did not lead to clinical resolution. The findings are compared to the cases of besnoitiosis in donkeys reported in the past 10 years throughout Europe. Conclusions: Besnoitiosis should be considered as a differential diagnosis for chronic skin disease particularly in cases of cutaneous masses, non-pruritic dermatitis, and dermatitis that is not responsive to treatment in donkeys and other equids. Future studies are needed to investigate the prevalence of the disease in Irish donkeys, the spread of the disease and the potential impact on the health and welfare of the donkeys.
Publication Date: 2024-02-14 PubMed ID: 38355717PubMed Central: PMC10865628DOI: 10.1186/s13620-024-00263-2Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research article describes the first known cases of a parasitic disease, caused by Besnoitia bennetti, in Irish donkeys. This emerging pathogen, which mainly affects fibroblasts in the skin and mucosa, has been identified in other regions of Europe and is now confirmed in Ireland.

Background and Objectives

  • The main aim of the research was to identify and study the presence of Besnoitia bennetti, an apicomplexan protozoan parasite, in Irish donkeys.
  • The article focusses on the clinical signs in affected equine hosts which may range from mild to severe debilitating disease.
  • The investigators wanted to shed more light on the phylogeny, epidemiology, and transmission of this less understood infection in donkeys, mules, and horses.

Methodology

  • Two donkeys from the Southwest of Ireland were the subject of this study, with both suffering from skin conditions leading to suspicion of besnoitiosis.
  • Diagnosis was made through histopathology, after which the specific species of B. bennetti was confirmed through PCR, sequencing, and microsatellite analysis.
  • The studied donkeys also showed high antibody titres against Besnoitia spp., further confirming the presence of the infection.

Findings

  • The study was successful in diagnosing the first cases of besnoitiosis in Irish donkeys.
  • Small (0.5 mm) scleral, conjunctival, and dermal cysts were observed in both animals as a result of the Besnoitia infection.
  • Treatment through trimethoprim sulfadiazine administered over 30 days failed to bring about a clinical resolution, indicating the stubborn nature of the disease.

Comparison and Conclusion

  • Findings from this research were compared with similar besnoitiosis cases across Europe within the past decade.
  • It was concluded that besnoitiosis should be considered when diagnosing chronic skin diseases in donkeys and other equines, especially in cases exhibiting non-responsive dermatitis and cutaneous masses.
  • The paper suggests further studies to analyze the prevalence of this disease in Ireland, as well as the potential health and welfare impacts on the donkey population.

Cite This Article

APA
Tinkler SH, Villa L, Manfredi MT, Walshe N, Jahns H. (2024). First report of Besnoitia bennetti in Irish donkeys: an emerging parasitic disease in Europe. Ir Vet J, 77(1), 2. https://doi.org/10.1186/s13620-024-00263-2

Publication

ISSN: 2046-0481
NlmUniqueID: 0100762
Country: Ireland
Language: English
Volume: 77
Issue: 1
Pages: 2
PII: 2

Researcher Affiliations

Tinkler, Stacy H
  • Veterinary Department, The Donkey Sanctuary Ireland, Hannigan's Farm, Liscarroll, Mallow Co. Cork, Ireland.
Villa, Luca
  • Department of Veterinary Medicine and Animal Sciences, Università Degli Studi Di Milano, Via Dell'Università, 6, 26900, Lodi, Italy.
Manfredi, Maria Teresa
  • Department of Veterinary Medicine and Animal Sciences, Università Degli Studi Di Milano, Via Dell'Università, 6, 26900, Lodi, Italy.
Walshe, Nicola
  • Pathobiology Section, School of Veterinary Medicine, University College Dublin, Belfield, Dublin, D04W6F6, Ireland.
Jahns, Hanne
  • Pathobiology Section, School of Veterinary Medicine, University College Dublin, Belfield, Dublin, D04W6F6, Ireland. Hanne.jahns@ucd.ie.

Conflict of Interest Statement

The authors declare no competing interests.

References

This article includes 50 references
  1. Dubey JP, Sreekumar C, Donovan T, Rozmanec M, Rosenthal BM, Vianna MC. Redescription of Besnoitia bennetti (Protozoa: Apicomplexa) from the donkey (Equus asinus). Int J Parasitol 2005;35(6):659–672.
    doi: 10.1016/j.ijpara.2005.01.004pubmed: 15862579google scholar: lookup
  2. Ellis JT, Holmdahl OJ, Ryce C, Njenga JM, Harper PA, Morrison DA. Molecular phylogeny of Besnoitia and the genetic relationships among Besnoitia of cattle, wildebeest and goats. Protist 2000;151(4):329–336.
    doi: 10.1078/S1434-4610(04)70031-0pubmed: 11212893google scholar: lookup
  3. Alvarez-García G, Frey CF, Mora LM, Schares G. A century of bovine besnoitiosis: an unknown disease re-emerging in Europe. Trends Parasitol 2013;29(8):407–415.
    doi: 10.1016/j.pt.2013.06.002pubmed: 23830145google scholar: lookup
  4. Gutiérrez-Expósito D, Arnal MC, Martínez-Durán D, Regidor-Cerrillo J, Revilla M, de Luco DL. The role of wild ruminants as reservoirs of Besnoitia besnoiti infection in cattle. Vet Parasitol 2016;223:7–13.
    doi: 10.1016/j.vetpar.2016.04.005pubmed: 27198769google scholar: lookup
  5. Ness SL, Peters-Kennedy J, Schares G, Dubey JP, Mittel LD, Mohammed HO. Investigation of an outbreak of besnoitiosis in donkeys in northeastern Pennsylvania. J Am Vet Med Assoc 2012;240(11):1329–1337.
    doi: 10.2460/javma.240.11.1329pubmed: 22607601google scholar: lookup
  6. Bigalke RD. Besnoitiosis and Globidiosis. 1981.
  7. Ramakrishnan C, Krishnan A, Francisco S, Schmid MW, Russo G, Leitão A. Dissection of Besnoitia besnoiti intermediate host life cycle stages: From morphology to gene expression. PLoS Pathog 2022;18(11):e1010955.
  8. Velásquez ZD, Lopez-Osorio S, Pervizaj-Oruqaj L, Herold S, Hermosilla C, Taubert A. Besnoitia besnoiti-driven endothelial host cell cycle alteration. Parasitol Res 2020;119(8):2563–2577.
    doi: 10.1007/s00436-020-06744-xpmc: PMC7366594pubmed: 32548739google scholar: lookup
  9. Authority EFS. Bovine Besnoitiosis: An emerging disease in Europe. EFSA J 2010;8(2):1499.
  10. Elsheikha HM. Besnoitia bennetti infection in miniature donkeys: an emerging protozoan of increasing concern. Vet parasitol 2007;145(3–4):390–391.
    doi: 10.1016/j.vetpar.2007.01.004pubmed: 17317014google scholar: lookup
  11. Olias P, Schade B, Mehlhorn H. Molecular pathology, taxonomy and epidemiology of Besnoitia species (Protozoa: Sarcocystidae). Infect Genet Evol 2011;11(7):1564–1576.
    doi: 10.1016/j.meegid.2011.08.006pubmed: 21906696google scholar: lookup
  12. Cortes H, Leitão A, Gottstein B, Hemphill A. A review on bovine besnoitiosis: a disease with economic impact in herd health management, caused by Besnoitia besnoiti (Franco and Borges). Parasitology 2014;141(11):1406–1417.
    doi: 10.1017/S0031182014000262pubmed: 24694568google scholar: lookup
  13. Bigalke RD. The artificial transmission of Besnoitia besnoiti (Marotel, 1912) from chronically infected to susceptible cattle and rabbits. Onderstepoort J Vet Res 1967;34(2):303–316.
    pubmed: 5583772
  14. Liénard E, Salem A, Grisez C, Prévot F, Bergeaud JP, Franc M. A longitudinal study of Besnoitia besnoiti infections and seasonal abundance of Stomoxys calcitrans in a dairy cattle farm of southwest France. Vet parasitol 2011;177(1–2):20–27.
    doi: 10.1016/j.vetpar.2010.11.030pubmed: 21185653google scholar: lookup
  15. Bennett SCJ. A Peculiar Equine Sarcosporidium in the Anglo-Egyptian Sudan. Vet J (1900) 1927;83(6):297–304.
  16. Bigalke RD. Studies on Equine Besnoitiosis. J Parasitol 1970;56(4):29.
  17. Schulz K, Thorburn J. Globidiosis-a cause of dermatitis in horses. J S Afr Vet Assoc 1955;26(1):39–44.
  18. van Heerden J, Els HJ, Raubenheimer EJ, Williams JH. Besnoitiosis in a horse. J S Afr Vet Assoc 1993;64(2):92–95.
    pubmed: 8410950
  19. Terrell TG, Stookey JL. Besnoitia bennetti in two Mexican burros. Vet Pathol 1973;10(2):177–184.
    doi: 10.1177/030098587301000210pubmed: 4203448google scholar: lookup
  20. Davis WP, Peters DF, Dunstan RW. Besnoitiosis in a miniature donkey. Vet Dermatol 1997;8(2):139–143.
  21. Elsheikha HM, Mackenzie CD, Rosenthal BM, Marteniuk JV, Steficek B, Windsor S. An outbreak of besnoitiosis in miniature donkeys. J Parasitol 2005;91(4):877–881.
    doi: 10.1645/GE-3277.1pubmed: 17089758google scholar: lookup
  22. Pols J, Alexander RA, Clark R, Louw JG, De Kock VE. Studies on bovine besnoitiosis with special reference to the aetiology. Onderstepoort J Vet Res 1960;28(3):265.
  23. Elsheikha HM, Schares G, Paraschou G, Sullivan R, Fox R. First record of besnoitiosis caused by Besnoitia bennetti in donkeys from the UK. Parasit Vectors 2020;13(1):279.
    doi: 10.1186/s13071-020-04145-8pmc: PMC7267762pubmed: 32493413google scholar: lookup
  24. Liénard E, Nabuco A, Vandenabeele S, Losson B, Tosi I, Bouhsira É. First evidence of Besnoitia bennetti infection (Protozoa: Apicomplexa) in donkeys (Equus asinus) in Belgium. Parasit Vectors 2018;11(1):427.
    doi: 10.1186/s13071-018-2993-3pmc: PMC6052696pubmed: 30021659google scholar: lookup
  25. Villa L, Gazzonis AL, Diezma-Díaz C, Perlotti C, Zanzani SA, Ferrucci F, Álvarez-García G, Manfredi MT. Besnoitiosis in donkeys: an emerging parasitic disease of equids in Italy. Parasitol Res 2021;120:1811–1819.
    doi: 10.1007/s00436-021-07089-9pmc: PMC8084774pubmed: 33723661google scholar: lookup
  26. Jacquiet P, Liénard E, Franc M. Bovine besnoitiosis: epidemiological and clinical aspects. Vet parasitol 2010;174(1–2):30–36.
    doi: 10.1016/j.vetpar.2010.08.013pubmed: 20850933google scholar: lookup
  27. Ness SL, Schares G, Peters-Kennedy J, Mittel LD, Dubey JP, Bowman DD. Serological diagnosis of Besnoitia bennetti infection in donkeys (Equus asinus). J Vet Diagn Invest 2014;26(6):778–782.
    doi: 10.1177/1040638714550180pubmed: 25227418google scholar: lookup
  28. Zafra Leva R, Soria-López N, Díez de Castro E, Jáber Mohamad JR, Mozos E, Pérez J. Outbreak of besnoitiosis in donkeys (Equus asinus) in the south of Spain. J Comp Path 2013;148(1):81.
  29. Gondim LFP, Mineo JR, Schares G. Importance of serological cross-reactivity among Toxoplasma gondii, Hammondia spp., Neospora spp. Sarcocystis spp. and Besnoitia besnoiti. Parasitology 2017;144(7):851–68.
    doi: 10.1017/S0031182017000063pmc: PMC5471829pubmed: 28241894google scholar: lookup
  30. Villa L, Gazzonis AL, Álvarez-García G, Diezma-Díaz C, Zanzani SA, Manfredi MT. First detection of anti-Besnoitia spp. specific antibodies in horses and donkeys in Italy. Parasitol Int 2018;67(5):640–3.
    doi: 10.1016/j.parint.2018.06.008pubmed: 29935266google scholar: lookup
  31. Villa L, Gazzonis AL, Zanzani SA, Perlotti C, Sironi G, Manfredi MT. Bovine besnoitiosis in an endemically infected dairy cattle herd in Italy: serological and clinical observations, risk factors, and effects on reproductive and productive performances. Parasitol Res 2019;118(12):3459–3468.
    doi: 10.1007/s00436-019-06501-9pubmed: 31659452google scholar: lookup
  32. García-Lunar P, Ortega-Mora LM, Schares G, Gollnick NS, Jacquiet P, Grisez C. An inter-laboratory comparative study of serological tools employed in the diagnosis of Besnoitia besnoiti infection in bovines. Transbound Emerg Dis 2013;60(1):59–68.
  33. Cortes HC, Reis Y, Gottstein B, Hemphill A, Leitão A, Müller N. Application of conventional and real-time fluorescent ITS1 rDNA PCR for detection of Besnoitia besnoiti infections in bovine skin biopsies. Vet parasitol 2007;146(3–4):352–356.
    doi: 10.1016/j.vetpar.2007.03.003pubmed: 17418951google scholar: lookup
  34. Madubata C, Dunams-Morel DB, Elkin B, Oksanen A, Rosenthal BM. Evidence for a recent population bottleneck in an Apicomplexan parasite of caribou and reindeer. Besnoitia tarandi. Infect Genet Evol 2012;12(8):1605–1613.
    doi: 10.1016/j.meegid.2012.06.007pubmed: 22742966google scholar: lookup
  35. Ryan EG, Lee A, Carty C, O'Shaughnessy J, Kelly P, Cassidy JP. Bovine besnoitiosis (Besnoitia besnoiti) in an Irish dairy herd. Vet Rec 2016;178(24):608.
    doi: 10.1136/vr.103683pubmed: 27122500google scholar: lookup
  36. Rhodes V, Hayes CJ, Sánchez-Miguel C, O'Donovan J, Ryan EG. An investigation into bovine besnoitiosis (Besnoitia besnoiti) in an Irish pedigree Aberdeen Angus herd. Vet Rec Case Rep 2022;10(3):e379.
    doi: 10.1002/vrc2.379google scholar: lookup
  37. Langenmayer MC, Gollnick NS, Majzoub-Altweck M, Scharr JC, Schares G, Hermanns W. Naturally Acquired Bovine Besnoitiosis: Histological and Immunohistochemical Findings in Acute, Subacute, and Chronic Disease. Vet Pathol 2015;52(3):476–488.
    doi: 10.1177/0300985814541705pubmed: 25096291google scholar: lookup
  38. Dubey JP, van Wilpe E, Blignaut DJ, Schares G, Williams JH. Development of early tissue cysts and associated pathology of Besnoitia besnoiti in a naturally infected bull (Bos taurus) from South Africa. J Parasitol 2013;99(3):459–466.
    doi: 10.1645/12-128.1pubmed: 23327488google scholar: lookup
  39. Villa L, Gazzonis AL, Zanzani SA, Mazzola S, Giordano A, Manfredi MT. Exploring alterations in hematological and biochemical parameters, enzyme activities and serum cortisol in Besnoitia besnoiti naturally infected dairy cattle. Parasit Vectors 2021;14(1):154.
    doi: 10.1186/s13071-021-04626-4pmc: PMC7962361pubmed: 33722267google scholar: lookup
  40. Sundberg JP, Burnstein T, Page EH, Kirkham WW, Robinson FR. Neoplasms of Equidae. J Am Vet Med Assoc 1977;170(2):150–152.
    pubmed: 576219
  41. Diezma-Díaz C, Tabanera E, Ferre I, Pizarro-Díaz M, González-Huecas M, Blanco-Murcia J. Histological findings in experimentally infected male calves with chronic besnoitiosis. Vet parasitol 2020;281:109120.
    doi: 10.1016/j.vetpar.2020.109120pubmed: 32361525google scholar: lookup
  42. Christen G, Gerber V, Dolf G, Burger D, Koch C. Inheritance of equine sarcoid disease in Franches-Montagnes horses. Vet J 2014;199(1):68–71.
    doi: 10.1016/j.tvjl.2013.09.053pubmed: 24152383google scholar: lookup
  43. Wilson AD, Hicks C. Both tumour cells and infiltrating T-cells in equine sarcoids express FOXP3 associated with an immune-supressed cytokine microenvironment. Vet Res 2016;47(1):55.
    doi: 10.1186/s13567-016-0339-8pmc: PMC4862206pubmed: 27160146google scholar: lookup
  44. García-Lunar P, Moré G, Campero L, Ortega-Mora LM, Álvarez-García G. Anti-Neospora caninum and anti-Sarcocystis spp. specific antibodies cross-react with Besnoitia besnoiti and influence the serological diagnosis of bovine besnoitiosis. Vet Parasitol 2015;214(1–2):49–54.
    doi: 10.1016/j.vetpar.2015.09.011pubmed: 26386830google scholar: lookup
  45. Gutiérrez-Expósito D, García-Bocanegra I, Howe DK, Arenas-Montes A, Yeargan MR, Ness SL. A serosurvey of selected cystogenic coccidia in Spanish equids: first detection of anti-Besnoitia spp. specific antibodies in Europe. BMC Vet Res 2017;13(1):128.
    doi: 10.1186/s12917-017-1046-zpmc: PMC5424396pubmed: 28490374google scholar: lookup
  46. Waap H, Volkart de Oliveira U, Nunes T, Gomes J, Gomes T, Bärwald A. Serological survey of Neospora spp. and Besnoitia spp in horses in Portugal. Vet Parasitol Reg Stud Rep 2020;20:100391.
    pubmed: 32448546
  47. González-Barrio D, Köster PC, Habela MA, Martín-Pérez M, Fernández-García JL, Balseiro A. Molecular survey of Besnoitia spp. (Apicomplexa) in faeces from European wild mesocarnivores in Spain. Transbound Emerg Dis 2021;68(6):3156–66.
    doi: 10.1111/tbed.14206pubmed: 34174029google scholar: lookup
  48. Millán J, Sobrino R, Rodríguez A, Oleaga A, Gortazar C, Schares G. Large-scale serosurvey of Besnoitia besnoiti in free-living carnivores in Spain. Vet parasitol 2012;190(1–2):241–245.
    doi: 10.1016/j.vetpar.2012.06.014pubmed: 22770702google scholar: lookup
  49. Seltmann A, Schares G, Aschenborn OHK, Heinrich SK, Thalwitzer S, Wachter B. Species-specific differences in Toxoplasma gondii, Neospora caninum and Besnoitia besnoiti seroprevalence in Namibian wildlife. Parasit Vectors 2020;13(1):7.
    doi: 10.1186/s13071-019-3871-3pmc: PMC6950991pubmed: 31915056google scholar: lookup
  50. Saegerman C, Evrard J, Houtain JY, Alzieu JP, Bianchini J, Mpouam SE, Schares G, Liénard E, Jacquiet P, Villa L, Álvarez-García G, Gazzonis AL, Gentile A, Delooz L. First expert elicitation of knowledge on drivers of emergence of bovine besnoitiosis in Europe. Pathogens 2022;11(7):753.
    doi: 10.3390/pathogens11070753pmc: PMC9323894pubmed: 35889998google scholar: lookup

Citations

This article has been cited 1 times.
  1. Turra N, Conejeros I, Hermosilla C, Burgos RA, Taubert A. Besnoitia besnoiti-Induced Neutrophil Extracellular Traps (NETs): Metabolic Signature, Signaling Pathways, Receptors and Implications on Pathogenesis. Animals (Basel) 2025 Nov 18;15(22).
    doi: 10.3390/ani15223326pubmed: 41302033google scholar: lookup