Abstract
Bovine besnoitiosis is an emerging disease in Europe, presenting quick spread toward central and southern Spain. Characterization of an outbreak in a free-ranging Limousin and Avileña beef cattle herd from southwestern Spain territories is attempted. Serological survey in the herd revealed increase of number of infected animals, from 34.3 % on first diagnoses/exams on December 2013 to 42.5 % in the second on April 2014. Blood analysis and serum biochemistry showed important alterations like leukocytosis (+33.2 % of mean value), with lymphocytosis (+205.3 %) and increase of LDH (+25.1 %), associated with tissue damage. Clinical cases were only observed in Limousin animals. Along with typical lesions of acute and chronic besnoitiosis, inflammatory and degenerative processes and parasitic cysts were present in the corpus cavernosum and the corpus spongiosum of penis. By using polymerase chain reaction (PCR) sequencing of 18S rDNA, Besnoitia besnoiti was confirmed as causative agent; microsatellite sequence analyses showed the homology of isolates with previously studied strains.
References
Álvarez-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
Álvarez-García G, Fernández-García A, Gutiérrez-Expósito D, Ruíz-Santa Quiteria JA, Aguado-Martínez A, Ortega-Mora LM (2014) Seroprevalence of Besnoitia besnoiti infection and associated risk factors in cattle from an endemic region in Europe. Vet J 200:328–331. doi:10.1016/j.tvjl.2014.02.013
Cortes H, Leitão A, Gottstein B, Hemphill A (2014) A review on bovine besnoitiosis: a disease with economic impact in herd health management, caused by Besnoitia besnoiti (Franco and Borges). Parasitology 141:1406–1417. doi:10.1017/s0031182014000262
Dubey JP, van Wilpe E, Blignaut DJC, Schares G, Williams JH (2013) Development of early tissue cysts and associated pathology of Besnoitia besnoiti in a naturally infected bull (Bos taurus) from South Africa. J Parasitol 99:459–466. doi:10.1645/12-128.1
EFSA (2010) Bovine besnoitiosis: an emerging disease in Europe. EFSA J 8(1499):15. doi:10.2903/jefsa20101499
Esteban-Gil A, Grisez C, Prevot F, Florentin S, Decaudin A, Picard-Hagen N, Berthelot X, Ronsin P, Alzieu JP, Marois M, Corboz N, Peglion M, Vilardell C, Liénard E, Bouhsira E, Castillo JA, Franc M, Jacquiet P (2014) No detection of Besnoitia besnoiti DNA in the semen of chronically infected bulls. Parasitol Res 113:2355–2362. doi:10.1007/s00436-014-3894-9
Fernández-García A, Risco-Castillo V, Pedraza-Díaz S, Aguado-Martínez A, Álvarez-García G, Gómez-Bautista M, Collantes-Fernández E, Ortega-Mora LM (2009) First isolation of Besnoitia besnoiti from a chronically infected cow in Spain. J Parasitol 95:474–476. doi:10.1645/ge-1772.1
Fernández-García A, Álvarez-García G, Risco-Castillo V, Aguado-Martínez A, Marcén 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
Frey CF, Gutiérrez-Expósito D, Ortega-Mora LM, Benavides J, Marcén JM, Castillo JA, Casasús I, Sanz A, García-Lunar P, Esteban-Gil A, Álvarez-García G (2013) Chronic bovine besnoitiosis: Intra-organ parasite distribution, parasite loads and parasite-associated lesions in subclinical cases. Vet Parasitol 197:95–103. doi:10.1016/j.vetpar.2013.04.023
García-Lunar P, Ortega-Mora LM, Schares G, Gollnick NS, Jacquiet P, Grisez C, Prevot F, Frey CF, Gottstein B, Álvarez-García G (2013) An inter-laboratory comparative study of serological tools employed in the diagnosis of Besnoitia besnoiti infection in bovines. Transbound Emerg Dis 60:59–68. doi:10.1111/j.1865-1682.2012.01318.x
Gollnick NS, Scharr JC, Schares G, Langenmayer MC (2015) Natural Besnoitia besnoiti infections in cattle: chronology of disease progression. BMC Vet Res 11:35. doi:10.1186/s12917-015-0344-6
Gutiérrez-Expósito D, Ortega-Mora LM, Marco I, Boadella M, Gortázar C, San Miguel-Ayanz JM, García-Lunar P, Lavin S, Álvarez-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
Gutiérrez-Expósito D, Esteban-Gil A, Ortega-Mora LM, García-Lunar P, Castillo JA, Marcén JM, Álvarez-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
Gutiérrez-Expósito D, Ortega-Mora LM, García-Lunar P, Rojo-Montejo S, Zabala J, Serrano M, Alvarez-García G (2015) Clinical and serological dynamics of Besnoitia besnoiti infection in three endemically infected beef cattle herds. Transbound Emerg Dis. doi:10.1111/tbed.12402
Hornok S, Fedák A, Baska F, Hofmann-Lehmann R, Basso W (2014) Bovine besnoitiosis emerging in central-eastern Europe, Hungary. Parasitol Vector 7:20. doi:10.1186/1756-3305-7-20
Hornok S, Fedák A, Baska F, Basso W, Dencső L, Tóth G, Szeredi L, Abonyi T, Dénes B (2015) Vector-borne transmission of Besnoitia besnoiti by blood-sucking and secretophagous flies: epidemiological and clinicopathological implications. Parasitol Vector 8:450. doi:10.1186/s13071-015-1058-0
Kiehl E, Heydorn AO, Schein E, Al-Rasheid KA, Selmair J, Abdel-Ghaffar F, Mehlhorn H (2010) Molecular biological comparison of different Besnoitia species and stages from different countries. Parasitol Res 106:889–894. doi:10.1007/s00436-010-1770-9
Kumi-Diaka J, Wilson S, Sanusi A, Njoku CE, Osori DI (1981) Bovine besnoitiosis and its effect on the male reproductive system. Theriogenology 16:523–530
Langenmayer MC, Gollnick NS, Majzoub-Altweck M, Scharr JC, Schares G, Hermanns W (2015a) Naturally acquired bovine besnoitiosis: histological and immunohistochemical findings in acute, subacute, and chronic disease. Vet Pathol 52:476–488. doi:10.1177/0300985814541705
Langenmayer MC, Scharr JC, Sauter-Louis C, Schares G, Gollnick NS (2015b) Natural Besnoitia besnoiti infections in cattle: hematological alterations and changes in serum chemistry and enzyme activities. BMC Vet Res 11:32. doi:10.1186/s12917-015-0326-8
Madubata C, Dunams-Morel DB, Elkin B, Oksanen A, Rosenthal BM (2012) Evidence for a recent population bottleneck in an Apicomplexan parasite of caribou and reindeer, Besnoitia tarandi. Infect Genet Evol 12:1605–1613. doi:10.1016/j.meegid.2012.06.007
Mehlhorn H, Klimpel S, Schein E, Heydorn AO, Al-Quraishy S, Selmair J (2009) Another African disease in central Europa: besnoitiosis of cattle. I. Light and electron microscopical study. Parasitol Res 104:861–868. doi:10.1007/s00436-008-1267-y
Miller SA, Dykes DD, Polesky HF (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16:1215
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
Pedraza-Díaz S, Marugán-Hernández V, Collantes-Fernández E, Regidor-Cerrillo J, Rojo-Montejo S, Gómez-Bautista M, Ortega-Mora LM (2009) Microsatellite markers for the molecular characterization of Neospora caninum: application to clinical samples. Vet Parasitol 166:38–46. doi:10.1016/j.vetpar.2009.07.043
Schares G, Maksimov A, Basso W, Moré G, Dubey JP, Rosenthal B, Majzoub M, Rostaher A, Selmair J, Langenmayer MC, Scharr JC, Conraths FJ, Gollnick NS (2011) Quantitative real time polymerase chain reaction assays for the sensitive detection of Besnoitia besnoiti infection in cattle. Vet Parasitol 178:208–216. doi:10.1016/j.vetpar.2011.01.038
Smith BP (2009) Large animal internal medicine, 4th edn. St. Louis, Missouri
Waap H, Nunes T, Cortes H, Leitão 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
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Authors thank Jesús López Casablanca (INVET, Cáceres) and Alejandro Tovar Cebrián for their excellent technical assistance.
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Nieto-Rodríguez, J.M., Calero-Bernal, R., Álvarez-García, G. et al. Characterization of an outbreak of emerging bovine besnoitiosis in southwestern Spain. Parasitol Res 115, 2887–2892 (2016). https://doi.org/10.1007/s00436-016-5050-1
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DOI: https://doi.org/10.1007/s00436-016-5050-1