Skip to main content
Log in

Absence of antibodies specific to Besnoitia spp. in European sheep and goats from areas in Spain where bovine besnoitiosis is endemic

  • Short Communication
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Besnoitia besnoiti and B. caprae, which infect bovids (cattle and antelopes) and goats, respectively, are responsible for besnoitiosis, a chronic and debilitating disease. Bovine besnoitiosis is considered to be a reemerging disease in Central and Western Europe. In addition, infection by Besnoitia spp. has been reported in reindeer from Sweden and Finland. Recently, the parasite was also detected in roe deer and red deer from Spain, where an interconnection between the domestic and sylvatic cycles of B. besnoiti has been presumed. In contrast, caprine besnoitiosis seems to be enzootic to Kenya and Iran. The presence of Besnoitia spp. in small domestic ruminants has never been explored in Europe, and the role that these species might play in the epidemiology of bovine besnoitiosis, as intermediate hosts or reservoirs of B. besnoiti, remains unknown. Herein, the first serosurvey conducted in European sheep and goats from areas in Spain where bovine besnoitiosis is endemic is described. Convenience sampling was conducted of 1943 sheep and 342 goats close to cattle from the Pyrenees and Central Spain that were infected with endemic Besnoitia spp. Serum samples were first analyzed by ELISA and then by confirmatory Western blot. Specific antibodies were not found in any sampled animal. Thus, sheep are unlikely to play a role in the epidemiology of bovine besnoitiosis, at least in the sampled areas. A larger serosurvey is necessary to determine whether goats might be a putative reservoir. To confirm the results of this study, sheep and goats should be further studied in other European countries and regions where their numbers are high and where bovine besnoitiosis is spreading.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

References

  • Alvarez-García G, Frey CF, Ortega-Mora LM, Schares G (2013) A century of bovine besnoitiosis: an unknown disease re-emerging in Europe. Trends Parasitol 29:407–415. doi:10.1016/j.pt.2013.06.002

    Article  PubMed  Google Scholar 

  • Alvarez-García G, García-Lunar P, Gutiérrez-Expósito D, Shkap V, Ortega-Mora LM (2014) Dynamics of Besnoitia besnoiti infection in cattle. Parasitology 141:1419–1435. doi:10.1017/S0031182014000729

    Article  PubMed  Google Scholar 

  • Arnal MC, Gutiérrez-Expósito D, Martínez-Durán D, Regidor-Cerrillo J, Revilla M, Fernández de Luco D, Jiménez-Meléndez A, Ortega-Mora LM, Álvarez-García G (2016) Systemic besnoitiosis in a juvenile roe deer (Capreolus capreolus). Transbound Emerg Dis. doi:10.1111/tbed.12514

    PubMed  Google Scholar 

  • Baldacchino F, Gardes L, De Stordeur E, Jay-Robert P, Garros C (2014) Blood-feeding patterns of horse flies in the French Pyrenees. Vet Parasitol 199:283–288. doi:10.1016/j.vetpar.2013.10.009

    Article  CAS  PubMed  Google Scholar 

  • Beck R, Stoković I, Pleadin J, Beck A (2013) Bovine besnoitiosis in Croatia, Proccedings Apicompexa congress., p 64

    Google Scholar 

  • Bigalke RD (1968) New concepts on the epidemiological features of bovine besnoitiosis as determined by laboratory and field investigations. Onderstepoort J Vet Res 35:3–137

    CAS  PubMed  Google Scholar 

  • Buxton D (1998) Protozoan infections (Toxoplasma gondii, Neospora caninum and Sarcocystis spp.) in sheep and goats: recent advances. Vet Res 29:289–310

    CAS  PubMed  Google Scholar 

  • Bwangamoi O, Carles AB, Wandera JG (1989) An epidemic of besnoitiosis in goats in Kenya. Vet Rec 125:461

    Article  CAS  PubMed  Google Scholar 

  • Cheema AH, Toofanian F (1979) Besnoitiosis in wild and domestic goats in Iran. Cornell Vet 69:159–168

    CAS  PubMed  Google Scholar 

  • Dubey JP (2009) Toxoplasmosis in sheep-the last 20 years. Vet Parasitol 163:1–14. doi:10.1016/j.vetpar.2009.02.026

    Article  CAS  PubMed  Google Scholar 

  • Ellis JT, Holmdahl OJ, Ryce C, Njenga JM, Harper PA, Morrison DA (2000) Molecular phylogeny of Besnoitia and the genetic relationships among Besnoitia of cattle, wildebeest and goats. Protist 151:329–336. doi:10.1078/S1434-4610(04)70031-0

    Article  CAS  PubMed  Google Scholar 

  • European Food Safety Authority (2010) Scientific statement on bovine besnoitiosis. https://www.efsa.europa.eu/de/efsajournal/pub/1499. Accessed 25 July 2016. doi: 10.2903/j.efsa.2010.1499

  • Eurostat (2015) Agriculture, forestry and fishery statistics. http://ec.europa.eu/eurostat/documents/3217494/7158355/KS-FK-15-101-EN N.pdf/79470e8c-abf3-43d3-8cd4-84880962cdd. Accessed 25 July 2016.

  • Fernández-García A, Alvarez-García G, Risco-Castillo V, Aguado-Martínez A, Marcen JM, Rojo-Montejo S, Castillo JA, Ortega-Mora LM (2010) Development and use of an indirect ELISA in an outbreak of bovine besnoitiosis in Spain. Vet Rec 166:818–822. doi:10.1136/vr.b4874

    Article  PubMed  Google Scholar 

  • García-Lunar P, Ortega-Mora LM, Rojo-Montejo S, Castillo JA, Álvarez-García G (2010) Actuación del veterinario antes un brote de besnoitiosis bovina, Proceedings XV Congreso Internacional Anembe de Medicina Bovina., pp 229–231

    Google Scholar 

  • García-Lunar P, More G, Campero L, Ortega-Mora LM, Alvarez-García G (2015) Anti-Neospora caninum and anti-Sarcocystis spp. specific antibodies cross-react with Besnoitia besnoiti and influence the serological diagnosis of bovine besnoitiosis. Vet Parasitol 214:49–54. doi:10.1016/j.vetpar.2015.09.011

    Article  PubMed  Google Scholar 

  • Gazzonis AL, Alvarez-García G, Zanzani SA, Garippa G, Rossi L, Maggiora M, Dini V, Invernizzi A, Luini M, Tranquillo VM, Ortega-Mora LM, Manfredi MT (2014) Besnoitia besnoiti among cattle in insular and northwestern Italy: endemic infection or isolated outbreaks? Parasit Vectors 7:585. doi:10.1186/s13071-014-0585-4

    Article  PubMed  PubMed Central  Google Scholar 

  • Gazzonis AL, Veronesi F, Di Cerbo AR, Zanzani SA, Molineri G, Moretta A, Piergili Fioretti D, Invernizzi A, Manfredi MT (2015) Toxoplasma gondii in small ruminants in Northern Italy—prevalence and risk factors. Ann Agric Environ Med 22:62–68. doi:10.5604/12321966.1141370

    Article  PubMed  Google Scholar 

  • González-Warleta M, Castro-Hermida JA, Regidor-Cerrillo J, Benavides J, Alvarez-García G, Fuertes M, Ortega-Mora LM, Mezo M (2014) Neospora caninum infection as a cause of reproductive failure in a sheep flock. Vet Res 45:88. doi:10.1186/s13567-014-0088-5

    PubMed  PubMed Central  Google Scholar 

  • Gutiérrez-Expósito D, Ortega-Mora LM, Gajadhar AA, García-Lunar P, Dubey JP, Alvarez-García G (2012) Serological evidence of Besnoitia spp. infection in Canadian wild ruminants and strong cross-reaction between Besnoitia besnoiti and Besnoitia tarandi. Vet Parasitol 190:19–28. doi:10.1016/j.vetpar.2012.06.017

    Article  PubMed  Google Scholar 

  • Gutiérrez-Expósito D, Ortega-Mora LM, Marco I, Boadella M, Gortazar C, San Miguel-Ayanz JM, García-Lunar P, Lavin S, Alvarez-García G (2013) First serosurvey of Besnoitia spp. infection in wild European ruminants in Spain. Vet Parasitol 197:557–564. doi:10.1016/j.vetpar.2013.05.017

    Article  PubMed  Google Scholar 

  • Gutiérrez-Expósito D, Esteban-Gil A, Ortega-Mora LM, García-Lunar P, Castillo JA, Marcen JM, Alvarez-García G (2014) Prevalence of Besnoitia besnoiti infection in beef cattle from the Spanish Pyrenees. Vet J 200:468–470. doi:10.1016/j.tvjl.2014.02.008

    Article  PubMed  Google Scholar 

  • Gutiérrez-Expósito D, Arnal MC, Martínez-Durán D, Regidor-Cerrillo J, Revilla M, Ortega-Mora LM, Fernández de Luco D, Jiménez-Meléndez A, Calero-Bernal R, Habela Martínez-Estéllez MA, García-Bocanegra I, Arenas-Montes A, Álvarez-García G (2016) The role of wild ruminants as reservoirs of Besnoitia besnoiti infection in cattle. Vet Parasitol 223:7–13. doi:10.1016/j.vetpar.2016.04.005

    Article  PubMed  Google Scholar 

  • Hornok S, Fedak A, Baska F, Hofmann-Lehmann R, Basso W (2014) Bovine besnoitiosis emerging in Central-Eastern Europe, Hungary. Parasit Vectors 7:20. doi:10.1186/1756-3305-7-20

    Article  PubMed  PubMed Central  Google Scholar 

  • Krcmar S, Mikuska A, Merdic E (2006) Response of Tabanidae (Diptera) to different natural attractants. J Vector Ecol 31:262–265

    Article  PubMed  Google Scholar 

  • Krcmar S, Radolic V, Lajos P, Lukacevic I (2014) Efficiency of colored modified box traps for sampling of tabanids. Parasite 21:67. doi:10.1051/parasite/2014068

    Article  PubMed  PubMed Central  Google Scholar 

  • Lesser M, Braun U, Deplazes P, Gottstein B, Hilbe M, Basso W (2012) First cases of besnoitiosis in cattle in Switzerland. Schweiz Arch Tierheilkd 154:469–474. doi:10.1024/0036-7281/a000389

    Article  CAS  PubMed  Google Scholar 

  • Millán J, Sobrino R, Rodríguez A, Oleaga Á, Gortazar C, Schares G (2012) Large-scale serosurvey of Besnoitia besnoiti in free-living carnivores in Spain. Vet Parasitol 190:241–245. doi:10.1016/j.vetpar.2012.06.014

    Article  PubMed  Google Scholar 

  • Moreno B, Collantes-Fernández E, Villa A, Navarro A, Regidor-Cerrillo J, Ortega-Mora LM (2012) Occurrence of Neospora caninum and Toxoplasma gondii infections in ovine and caprine abortions. Vet Parasitol 187:312–318. doi:10.1016/j.vetpar.2011.12.034

    Article  CAS  PubMed  Google Scholar 

  • Namazi F, Oryan A, Sharifiyazdi H (2011) 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. Parasitol Res 108:633–638. doi:10.1007/s00436-010-2107-4

    Article  PubMed  Google Scholar 

  • Ness SL, Peters-Kennedy J, Schares G, Dubey JP, Mittel LD, Mohammed HO, Bowman DD, Felippe MJ, Wade SE, Shultz N, Divers TJ (2012) Investigation of an outbreak of besnoitiosis in donkeys in northeastern Pennsylvania. J Am Vet Med Assoc 240:1329–1337. doi:10.2460/javma.240.11.1329

    Article  PubMed  Google Scholar 

  • Njenga J, Bwangamoi O, Mutiga E, Kangethe E, Mugera G (1993) Preliminary findings from an experimental study of caprine besnoitiosis in Kenya. Vet Res Commun 17:203–208

    Article  CAS  PubMed  Google Scholar 

  • Njenga M, Munyua S, Bwangamoi O, Kangethe E, Mugera G, Mutiga E, Wamukoya J (1999) Prevalence of besnoitiosis in domestic ruminants in Kenya: a preliminary survey. J S Afr Vet Assoc 70:151–153

    CAS  PubMed  Google Scholar 

  • Olias P, Schade B, Mehlhorn H (2011) Molecular pathology, taxonomy and epidemiology of Besnoitia species (Protozoa: Sarcocystidae). Infect Genet Evol 11:1564–1576. doi:10.1016/j.meegid.2011.08.006

    Article  CAS  PubMed  Google Scholar 

  • Oryan A, Silver IA, Sadoughifar R (2014) Caprine besnoitiosis: an emerging threat and its relationship to some other infections of ungulates by Besnoitia species. Res Vet Sci 97:1–7. doi:10.1016/j.rvsc.2014.06.004

    Article  CAS  PubMed  Google Scholar 

  • Pols JW (1960) Studies on bovine besnoitiosis with special reference to the aetiology. Onderstepoort J Vet Res 28:265–356

    Google Scholar 

  • Ryan EG, Lee A, Carty C, O’Shaughnessy J, Kelly P, Cassidy JP, Sheehan M, Johnson A, de Waal T (2016) Bovine besnoitiosis (Besnoitia besnoiti) in an Irish dairy herd. Vet Rec 178:608. doi:10.1136/vr.103683

    Article  CAS  PubMed  Google Scholar 

  • Vanhoudt A, Pardon B, De Schutter P, Bosseler T, Sarre C, Vercruysse J, Deprez P (2015) First confirmed case of bovine besnoitiosis in an imported bull in Belgium. Vlaams Diergeneeskd Tijdschr 84:205–211

    Google Scholar 

  • Waap H, Nunes T, Cortes H, Leitao A, Vaz Y (2014) Prevalence and geographic distribution of Besnoitia besnoiti infection in cattle herds in Portugal. Parasitol Res 113:3703–3711. doi:10.1007/s00436-014-4035-1

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a research project from the Spanish Ministry of Economy and Competitiveness (AGL 2010-20561), Ciencia y Teconología para el Desarrollo (CYTED) (Thematic Network 113RT0469 Protozoovac), and by the Community of Madrid (PLATESA S20137ABI-2906). Daniel Gutiérrez Expósito has been financially supported by the Ministry of Economy and Competitiveness (grant no. BES-2011-043753). We wish to acknowledge Paula García-Lunar, Alba Pablos-Tanarro, and Alejandro Jiménez-Meléndez for their excellent technical assistance and the farmers of the herds for their help.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gema Álvarez-García.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gutiérrez-Expósito, D., Ortega-Mora, L.M., Ara, V. et al. Absence of antibodies specific to Besnoitia spp. in European sheep and goats from areas in Spain where bovine besnoitiosis is endemic. Parasitol Res 116, 445–448 (2017). https://doi.org/10.1007/s00436-016-5311-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-016-5311-z

Keywords

Navigation