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Article contents

A review on bovine besnoitiosis: a disease with economic impact in herd health management, caused by Besnoitia besnoiti (Franco and Borges, 1916)

Published online by Cambridge University Press:  02 April 2014

HELDER CORTES
Affiliation:
Victor Caeiro Laboratory of Parasitology, ICAAM – Instituto de Ciências Agrárias e Ambientais Mediterrânicas – Universidade de Évora – Núcleo da Mitra, Ap. 94, 7002-554, Évora, Portugal
ALEXANDRE LEITÃO*
Affiliation:
Instituto de Investigação Científica Tropical, CVZ, CIISA Faculdade de Medicina Veterinária, Universidade de Lisboa, Av. Universidade Técnica, 1300-447 Lisboa, Portugal
BRUNO GOTTSTEIN
Affiliation:
Institute of Parasitology, Vetsuisse Faculty, University of Bern, Länggass-Strasse 122, CH-3012 Bern, Switzerland
ANDREW HEMPHILL*
Affiliation:
Institute of Parasitology, Vetsuisse Faculty, University of Bern, Länggass-Strasse 122, CH-3012 Bern, Switzerland
*
*Corresponding authors: Institute of Parasitology, Vetsuisse Faculty, University of Bern, Länggass-Strasse 122, CH-3012 Bern, Switzerland. E-mail: andrew.hemphill@vetsuisse.unibe.ch; Alexandre Leitão, Instituto de Investigação Científica Tropical, CVZ, CIISA Faculdade de Medicina Veterinária, Universidade de Lisboa, 1300-447 Lisboa, Portugal. E-mail: alexandre@fmv.ulisboa.pt
*Corresponding authors: Institute of Parasitology, Vetsuisse Faculty, University of Bern, Länggass-Strasse 122, CH-3012 Bern, Switzerland. E-mail: andrew.hemphill@vetsuisse.unibe.ch; Alexandre Leitão, Instituto de Investigação Científica Tropical, CVZ, CIISA Faculdade de Medicina Veterinária, Universidade de Lisboa, 1300-447 Lisboa, Portugal. E-mail: alexandre@fmv.ulisboa.pt

Summary

Bovine besnoitiosis is caused by the largely unexplored apicomplexan parasite Besnoitia besnoiti. In cows, infection during pregnancy often results in abortion, and chronically infected bulls become infertile. Similar to other apicomplexans B. besnoiti has acquired a largely intracellular lifestyle, but its complete life cycle is still unknown, modes of transmission have not been entirely resolved and the definitive host has not been identified. Outbreaks of bovine besnoitiosis in cattle were described in the 1990s in Portugal and Spain, and later several cases were also detected in France. More cases have been reported recently in hitherto unaffected countries, including Italy, Germany, Switzerland, Hungary and Croatia. To date, there is still no effective pharmaceutical compound available for the treatment of besnoitiosis in cattle, and progress in the identification of novel targets for intervention through pharmacological or immunological means is hampered by the lack of molecular data on the genomic and transcriptomic level. In addition, the lack of an appropriate small animal laboratory model, and wide gaps in our knowledge on the host-parasite interplay during the life cycle of this parasite, renders vaccine and drug development a cost- and labour-intensive undertaking.

Type
Special Issue Article
Copyright
Copyright © Cambridge University Press 2014 

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References

Alvarez-Garcia, G., Frey, C., Ortega-Mora, L. M. and Schares, G. (2013). A century of bovine besnoitiosis: an unknown disease re-emerging in Europe. Trends in Parasitology 29, 407415. doi: 10.1016/j.pt.2013.06.002.CrossRefGoogle Scholar
Alzieu, J. P., Cortes, H., Gottstein, B., Jacquiet, P., Dorchies, P., Schelcher, F. and L'Hostis, M. (2007). La besnoitiose bovine: actualités épidémiologiques et diagnostiques. Bulletin des G.T.V. – Hors-série parasitisme des bovins, 4149.Google Scholar
Ayroud, M., Leighton, F. A. and Tessaro, S. V. (1995). The morphology and pathology of Besnoitia sp. in reindeer (Rangifer tarandus tarandus). Journal of Wildlife Diseases 31, 319326. doi: 10.7589/0090-3558-31.3.319.CrossRefGoogle Scholar
Basso, W., Schares, G., Gollnick, N. S., Rütten, M. and Deplazes, P. (2011). Exploring the life cycle of Besnoitia besnoiti – experimental infection of putative definitive and intermediate host species. Veterinary Parasitology 178, 223234. doi: 10.1016/j.vetpar.2011.01.027.CrossRefGoogle ScholarPubMed
Basson, P. A., van Niekerk, J. W., McCully, R. M. and Bigalke, R. D. (1965). Besnoitiosis in South African antelopes: a preliminary note on the occurrence of Besnoitia cysts in the cardiovascular system. Journal of the South African Veterinary Medical Association 36, 578.Google Scholar
Basson, P. A., McCully, R. M. and Bigalke, R. D. (1970). Observations on the pathogenesis of bovine and antelope strains of Besnoitia besnoiti (Marotel, 1912) infection in cattle and rabbits. Onderstepoort Journal of Veterinary Research 37, 105126.Google ScholarPubMed
Besnoit, C. and Robin, V. (1912). Sarcosporidioses cutanée chez une vache. Revue Vétérinaire 37, 649663.Google Scholar
Bigalke, R. D. (1960). Preliminary observation on the mechanical transmission of cyst organisms of Besnoitia besnoiti (Marotel, 1912) from a chronically infected bull to rabbits by Glossina brevipalpis Newstead, 1910. Journal of the South African Veterinary Association 31, 3744.Google Scholar
Bigalke, R. D. (1968). New concepts on the epidemiological features of bovine besnoitiosis as determined by laboratory and field investigations. Onderstepoort Journal of Veterinary Research 35, 3138.Google ScholarPubMed
Bigalke, R. D. and Naude, T. W. (1962). The diagnostic value of cysts in the scleral conjunctiva in bovine besnoitiosis. Journal of the South African Veterinary Medical Association XXXIII, 2127.Google Scholar
Bigalke, R. D. and Prozesky, L. (2004). Besnoitiosis. In Infectious Diseases of Livestock, Vol. 1 (ed. Coetzer, J. A. W. and Tustin, R. C.), pp. 331359. Oxford University Press, Cape Town, South Africa.Google Scholar
Bigalke, R. D., van Niekerk, J. W., Basson, P. A. and McCully, R. M. (1967). Studies on the relationship between Besnoitia of blue wildebeest and impala, and Besnoitia besnoiti of cattle. Onderstepoort Journal of Veterinary Research 34, 728.Google ScholarPubMed
Bigalke, R. D., Schoeman, J. H. and McCully, R. M. (1974). Immunization against bovine besnoitiosis with a live vaccine prepared from a blue wildebeest strain of Besnoitia besnoiti grown in cell cultures. 1. Studies on rabbits. Onderstepoort Journal of Veterinary Research 41, 15.Google ScholarPubMed
Cadéac, C. (1884). Identit‚ de l‚Elephantiasis et de l'anasarque du boeuf. Description de cette maladie. Revue Vétérinaire 521, 521540.Google Scholar
Coleman, A. W. and Mai, J. C. (1997). Ribosomal DNA ITS-1 and ITS-2 sequence comparisons as a tool for predicting genetic relatedness. Journal of Molecular Evolution 45, 168177. doi: 10.1007/PL00006217.CrossRefGoogle ScholarPubMed
Cortes, H., Ferreira, M. L., Silva, J. F., Vidal, R., Serra, P. and Caeiro, V. (2003). Contribuição para o estudo da besnoitiose bovina em Portugal. Revista Portuguesa de Ciências Veterinárias 98, 4346.Google Scholar
Cortes, H., Leitão, A., Vidal, R., Vila-Vicosa, M. J., Ferreira, M. L., Caeiro, V. and Hjerpe, C. A. (2005). Besnoitiosis in bulls in Portugal. Veterinary Record 157, 262264. doi: 10.1136/vr.157.9.262.CrossRefGoogle ScholarPubMed
Cortes, H. C. E., Nunes, S., Reis, Y., Staubli, D., Vidal, R., Sager, H., Leitão, A. and Gottstein, B. (2006 a). Immunodiagnosis of Besnoitia besnoiti infection by ELISA and Western blot. Veterinary Parasitology 141, 216225. doi: 10.1016/j.vetpar.2006.05.023.CrossRefGoogle ScholarPubMed
Cortes, H., Chagas e Silva, J., Baptista, M. C., Pereira, R. M., Leitão, A., Horta, A. E. M., Vasques, M. I., Barber, J. and Marques, C. C. (2006 b). Besnoitia besnoiti impact on fertility of cattle exploited in mediterranean pastures (Alentejo). In EAAP Publication 119 (ed. Ribeiro, J. M. R.), pp. 323329. Wageningen Academic Press, Wageningen, the Netherlands.Google Scholar
Cortes, H. C., Reis, Y., Waap, H., Vidal, R., Soares, H., Marques, I., da Pereira, F., Fazendeiro, I., Ferreira, M. L., Caeiro, V., Shkap, V., Hemphill, A. and Leitão, A. (2006 c). Isolation of Besnoitia besnoiti from infected cattle in Portugal. Veterinary Parasitology 141, 226233. doi: 10.1016/j.vetpar.2006.05.022.CrossRefGoogle ScholarPubMed
Cortes, H. C. E., Reis, Y., Gottstein, B., Hemphill, A., Leitão, A. and Müller, N. (2007 a). Application of conventional and real-time fluorescent ITS1 rDNA PCR for detection of Besnoitia besnoiti infections in bovine skin biopsies. Veterinary Parasitology 146, 352356. doi: 10.1016/j.vetpar.2007.03.003.CrossRefGoogle ScholarPubMed
Cortes, H. C. E., Mueller, N., Esposito, M., Leitão, A., Naguleswaran, A. and Hemphill, A. (2007 b). In vitro efficacy of nitro- and bromo-thiazolyl-salicylamide compounds (thiazolides) against Besnoitia besnoiti infection in Vero cells. Parasitology 134, 975985. doi: 10.1017/S0031182007002417.CrossRefGoogle ScholarPubMed
Cortes, H. C., Muller, N., Boykin, D., Stephens, C. E. and Hemphill, A. (2011). In vitro effects of arylimidamides against Besnoitia besnoiti infection in Vero cells. Parasitology 138, 583592. doi: 10.1017/S0031182011000114.CrossRefGoogle ScholarPubMed
Debache, K., Guionaud, C., Alaeddine, F. and Hemphill, A. (2010). Intraperitoneal and intra-nasal vaccination of mice with three distinct recombinant Neospora caninum antigens results in differential effects with regard to protection against experimental challenge with Neospora caninum tachyzoites. Parasitology 137, 229240. doi: 10.1017/S0031182009991259.CrossRefGoogle ScholarPubMed
Diesing, L., Heydorn, A. O., Matuschka, F. R., Bauer, C., Pipano, E., de Waal, D. T. and Potgieter, F. T. (1988). Besnoitia besnoiti: studies on the definitive host and experimental infections in cattle. Parasitology Research 75, 114117. doi: 10.1007/BF00932710.CrossRefGoogle ScholarPubMed
Dubey, J. P. (1976). A review of Sarcocystis of domestic animals and of other coccidia of cats and dogs. Journal of the American Veterinary Medical Association 169, 10611078.Google Scholar
Dubey, J. P., Shkap, V., Pipano, E., Fish, L. and Fritz, D. L. (2003). Ultrastructure of Besnoitia besnoiti tissue cysts and bradyzoites. Journal of Eukaryotic Microbiology 50, 240244. doi: 10.1111/j.1550-7408.2003.tb00127.x.CrossRefGoogle ScholarPubMed
Dubey, J. P., Sreekumar, C., Rosenthal, B. M., Vianna, M. C. B., Nylund, M., Nikander, S. and Oksanen, A. (2004). Redescription of Besnoitia tarandi (Protozoa: Apicomplexa) from the reindeer (Rangifer tarandus). International Journal for Parasitology 34, 12731287. doi: 10.1016/j.ijpara.2004.07.002.CrossRefGoogle Scholar
Dubey, J. P., van Wilpe, E., Blignaut, D. J. C., Schares, G. and Williams, J. H. (2013). Development of early tissue cysts and associated pathology of Besnoitia besnoiti in a naturally infected bull (Bos taurus) from South Africa. Journal of Parasitology 99, 459466. doi: 10.1645/12-128.1.CrossRefGoogle Scholar
Ducrocq, J., Beauchamp, G., Kutz, S., Simard, M., Elkin, B., Croft, B., Taillon, J., Cote, S. D., Brodeur, V., Campbell, M., Cooley, D., Cuyler, C. and Lair, S. (2012). Comparison of gross visual and microscopic assessment of four anatomic sites to monitor Besnoitia tarandi in barren-ground caribou (Rangifer tarandus). Journal of Wildlife Diseases 48, 732738. doi: 10.7589/0090-3558-48.3.732.CrossRefGoogle Scholar
EFSA Journal (2010). Bovine besnoitiosis: an emerging disease in Europe. EFSA Journal 8, 1499 [15 pp.]. doi: 10.2903/j.efsa.2010.1499.CrossRefGoogle Scholar
Elsheikha, H. M., Mackenzie, C. D., Rosenthal, B. M., Marteniuk, J. V., Steficek, B., Windsor, S., Saeed, A. M. and Mansfield, L. S. (2005). An outbreak of besnoitiosis in miniature donkeys. Journal of Parasitology 91, 877881. doi: 10.1645/GE-3277.1.CrossRefGoogle ScholarPubMed
Fernandez-Garcia, A., Risco-Castillo, V., Pedraza-Diaz, S., Aguado-Martinez, A., Alvarez-Garcia, G., Gomez-Bautista, M., Collantes-Fernandez, E. and Ortega-Mora, L. M. (2009 a). First isolation of Besnoitia besnoiti from a chronically infected cow in Spain. Journal of Parasitology 95, 474476.CrossRefGoogle ScholarPubMed
Fernandez-Garcia, A., Alvarez-Garcia, G., Risco-Castillo, V., Aguado-Martinez, A., Marugan-Hernandez, V. and Ortega-Mora, L. M. (2009 b). Pattern of recognition of Besnoitia besnoiti tachyzoite and bradyzoite antigens by naturally infected cattle. Veterinary Parasitology 164, 104110. doi: 10.1016/j.vetpar.2009.06.020.CrossRefGoogle ScholarPubMed
Fernandez-Garcia, A., Alvarez-Garcia, G., Risco-Castillo, V., Aguado-Martinez, A., Marcen, J. M., Rojo-Montejo, S., Castillo, J. A. and Ortega-Mora, L. M. (2010). Development and use of an indirect ELISA in an outbreak of bovine besnoitiosis in Spain. Veterinary Record 166, 818822. doi: 10.1136/vr.b4874.CrossRefGoogle Scholar
Fernandez-García, A., Alvarez-García, G., Marugán-Hernández, V., García-Lunar, P., Aguado-Martínez, A., Risco-Castillo, V. and Ortega-Mora, L. M. (2013). Identification of Besnoitia besnoiti proteins that showed differences in abundance between tachyzoite and bradyzoite stages by difference gel electrophoresis. Parasitology 140, 9991008. doi: 10.1017/S003118201300036X.CrossRefGoogle ScholarPubMed
Franco, E. E. and Borges, I. (1916). Sur la sarcosporidiose Bovine. Arquivos do Instituto Bacteriologico Câmara Pestana 4, 269289.Google Scholar
Frey, C. F., Gutiérrez-Expósito, D., Ortega-Mora, L. M., Benavides, J., Marcén, J. M., Castillo, J. A., Casasús, I., Sanz, A., García-Lunar, P., Esteban-Gil, A. and Álvarez-García, G. (2013). Chronic bovine besnoitiosis: intra-organ parasite distribution, parasite loads and parasite-associated lesions in subclinical cases. Veterinary Parasitology 197, 95103. doi: 10.1016/j.vetpar.2013.04.023.CrossRefGoogle ScholarPubMed
Fulton, J. D. and Turk, J. L. (1959). Direct agglutination test for Toxoplasma gondii . Lancet 2, 10681069.CrossRefGoogle ScholarPubMed
Garcia-Lunar, P., Ortega-Mora, L. M., Schares, G., Gollnick, N. S., Jacquiet, P., Grisez, C., Prevot, F., Frey, C. F., Gottstein, B. and Alvarez-Garcia, G. (2013 a). An inter-laboratory comparative study of serological tools employed in the diagnosis of Besnoitia besnoiti infection in bovines. Transboundary and Emerging Diseases 60, 5968. doi: 10.1111/j.1865-1682.2012.01318.x.CrossRefGoogle Scholar
Garcia-Lunar, P., Regidor-Cerrillo, J., Gutiérrez-Expósito, D., Ortega-Mora, L. and Alvarez-García, G. (2013 b). First 2-DE approach towards characterising the proteome and immunome of Besnoitia besnoiti in the tachyzoite stage. Veterinary Parasitology 195, 2434. doi: 10.1016/j.vetpar.2012.12.040.CrossRefGoogle ScholarPubMed
Gentile, A., Militerno, G., Schares, G., Nanni, A., Testoni, S., Bassi, P. and Gollnick, N. S. (2012). Evidence for bovine besnoitiosis being endemic in Italy – first in vitro isolation of Besnoitia besnoiti from cattle born in Italy. Veterinary Parasitology 184, 108115. doi: 10.1016/j.vetpar.2011.09.014.CrossRefGoogle ScholarPubMed
Gollnick, N. S., Gentile, A. and Schares, G. (2010). Diagnosis of bovine besnoitiosis in a bull born in Italy. Veterinary Record 166, 599. doi: 10.1136/vr.b4874.CrossRefGoogle Scholar
Gutiérrez-Expósito, D., Ortega-Mora, L. M., Gajadhar, A. A., García-Lunar, P., Dubey, J. P. and Alvarez-García, G. (2012). Serological evidence of Besnoitia spp. infection in Canadian wild ruminants and strong cross-reaction between Besnoitia besnoiti and Besnoitia tarandi . Veterinary Parasitology 190, 1928. doi: 10.1016/j.vetpar.2012.06.017.CrossRefGoogle ScholarPubMed
Gutiérrez-Expósito, D., Ortega-Mora, L. M., Marco, I., Boadella, M., Gortázar, C., San Miguel-Ayanz, J. M., García-Lunar, P., Lavín, S. and Alvarez-García, G. (2013). First serosurvey of Besnoitia spp. infection in wild European ruminants in Spain. Veterinary Parasitology 197, 557564. doi: 10.1016/j.vetpar.2013.05.017.CrossRefGoogle ScholarPubMed
Henry (1912). Sarcosporidiose cutanée chez une Vache. Recueil de médecine vétérinaire XC, 327.Google Scholar
Herin, V. V. (1952). Bovine globidiosis in Ruanda-Urundi. Annales de la Société Belge de Médecine Tropicale 32, 155159.Google ScholarPubMed
Hornok, S., Fedák, A., Baska, F., Hofmann-Lehmann, R. and Basso, W. (2014). Bovine besnoitiosis emerging in Central-Eastern Europe, Hungary. Parasites and Vectors 7, 20. doi: 10.1186/1756-3305-7-20.CrossRefGoogle ScholarPubMed
Irigoien, M., Del Cacho, E., Gallego, M., López-Bernad, F., Quílez, J. and Sánchez-Acedo, C. (2000). Immunohistochemical study of the cyst of Besnoitia besnoiti . Veterinary Parasitology 91, 16. doi: 10.1016/S0304-4017(00)00260-0.CrossRefGoogle ScholarPubMed
Jacquiet, P., Liénard, E. and Franc, M. (2010). Bovine besnoitiosis: epidemiological and clinical aspects. Veterinary Parasitology 174, 3036. doi: 10.1016/j.vetpar.2010.08.013.CrossRefGoogle ScholarPubMed
Janitschke, K., De Vos, A. J. and Bigalke, R. D. (1984). Serodiagnosis of bovine besnoitiosis by ELISA and immunofluorescence tests. Onderstepoort Journal of Veterinary Research 51, 239243.Google ScholarPubMed
Johnson, A. M. (1997). Speculation on possible life cycles for the clonal lineages in the genus Toxoplasma . Parasitology Today 13, 393397.CrossRefGoogle ScholarPubMed
Juste, R. A., Cuervo, L. A., Marco, J. C. and Oregui, L. M. (1990). La besnoitiosis bovina: desconocida en España? Medicina Veterinária 7, 613618.Google Scholar
Kiehl, E., Heydorn, A. O., Schein, E., Al-Rasheid, K. A. S., Selmair, J., Abdel-Ghaffar, F. and Mehlhorn, H. (2010). Molecular biological comparison of different Besnoitia species and stages from different countries. Parasitology Research 106, 889894. doi: 10.1007/s00436-010-1770-9.CrossRefGoogle ScholarPubMed
Kumi-Diaka, J., Wilson, S., Sannusi, A., Njoku, C. E. and Osoru, D. I. K. (1981). Bovine besnoitiosis and its effect on the male reproductive system. Theriogenology 16, 523530. doi: 10.1016/0093-691X(81)90037-6.CrossRefGoogle ScholarPubMed
Liao, M., Ma, L., Bannai, H., Lee, E.-G., Xie, Z., Tang, X., Zhang, H., Xuan, X. and Fujisaki, K. (2006). Identification of a protein disulfide isomerase of Neospora caninum in excretory-secretory products and its IgA binding and enzymatic activities. Veterinary Parasitology 139, 4756. doi: 10.1016/j.vetpar.2006.02.029.CrossRefGoogle ScholarPubMed
Liénard, E., Salem, A., Grisez, C., Prévot, F., Bergeaud, J. P., Franc, M., Gottstein, B., Alzieu, J. P., Lagalisse, Y. and Jacquiet, P. (2011). A longitudinal study of Besnoitia besnoiti infections and seasonal abundance of Stomoxys calcitrans in a dairy cattle farm of southwest France. Veterinary Parasitology 177, 2027. doi: 10.1016/j.vetpar.2010.11.030.CrossRefGoogle Scholar
Liénard, E., Salem, A., Jacquiet, P., Grisez, C., Prévot, F., Blanchard, B., Bouhsira, E. and Franc, M. (2013). Development of a protocol testing the ability of Stomoxys calcitrans (Linnaeus, 1758) (Diptera: Muscidae) to transmit Besnoitia besnoiti (Henry, 1913) (Apicomplexa: Sarcocystidae). Parasitology Research 112, 479486. doi: 10.1007/s00436-012-3157-6.CrossRefGoogle Scholar
Marcelino, E., Martins, T. M., Morais, J. B., Nolasco, S., Cortes, H., Hemphill, A., Leitão, A. and Novo, C. (2011). Besnoitia besnoiti protein disulfide isomerase (BbPDI): molecular characterization, expression and in silico modelling. Experimental Parasitology 129, 164174. doi: 10.1016/j.exppara.2011.06.012.CrossRefGoogle ScholarPubMed
Marotel, M. (1912). Discussion of paper by Besnoit and Robin. Bullet Mémoires de la Société de Sciences Veterinaires de Lyon et de la Société de Medicine Veterinaire de Lyon et du Sud-Est 15, 196217.Google Scholar
McCully, R. M., Basson, P. A., van Niekerk, J. W. and Bigalke, R. D. (1966). Observations on Besnoitia cysts in the cardiovascular system of some wild antelopes and domestic cattle. Onderstepoort Journal of Veterinary Research 33, 245276.Google Scholar
Meek, B., Back, J. W., Klaren, V. N., Speijer, D. and Peek, R. (2002 a). Protein disulfide isomerase of Toxoplasma gondii is targeted by mucosal IgA antibodies in humans 470. FEBS Letters 522, 104108. doi: 10.1016/S0014-5793(02)02911-3.CrossRefGoogle Scholar
Meek, B., Back, J. W., Klaren, V. N. A., Speijer, D. and Peek, R. (2002 b). Conserved regions of protein disulfide isomerase are targeted by natural IgA antibodies in humans. International Immunology 14, 12911301. doi: 10.1093/intimm/dxf091.CrossRefGoogle ScholarPubMed
Mehlhorn, H., Klimpel, S., Schein, E., Heydorn, A. O., Al-Quraishy, S. and Selmair, J. (2009). Another African disease in Central Europe: Besnoitiosis of cattle. I. Light and electron microscopical study. Parasitology Research 104, 861868. doi: 10.1007/s00436-008-1267-y.CrossRefGoogle ScholarPubMed
Millan, J., Sobrino, R., Rodriguez, A., Oleaga, A., Gortazar, C. and Schares, G. (2012). Large-scale serosurvey of Besnoitia besnoiti in free-living carnivores in Spain. Veterinary Parasitology 190, 241245. doi: 10.1016/j.vetpar.2012.06.014.CrossRefGoogle ScholarPubMed
Naguleswaran, A., Alaeddine, F., Guionaud, C., Vonlaufen, N., Sonda, S., Jenoe, P., Mevissen, M. and Hemphill, A. (2005). Neospora caninum protein disulfide isomerase is involved in tachyzoite-host cell interaction. International Journal for Parasitology 35, 14591472. doi: 10.1016/j.ijpara.2005.06.006.CrossRefGoogle ScholarPubMed
Nasir, A., Lanyon, S. R., Schares, G., Anderson, M. L. and Reichel, M. P. (2012). Sero-prevalence of Neospora caninum and Besnoitia besnoiti in South Australian beef and dairy cattle. Veterinary Parasitology 186, 480485. doi: 10.1016/j.vetpar.2011.11.032.CrossRefGoogle ScholarPubMed
Neuman, M. (1962). The experimental infection of the gerbil (Meriones tristrami shanii) with Besnoitia besnoiti . Refuah Veterinarith 19, 184188.Google Scholar
Neuman, M. (1972). Serological survey of Besnoitia besnoiti (Marotel 1912) infection in Israel by immunofluorescence. Zentralblatt Veterinarmedizin Reihe B 19, 391396.CrossRefGoogle ScholarPubMed
Ng'ang'a, C. J. and Kasigazi, S. (1994). Caprine besnoitiosis: studies on the experimental intermediate hosts and the role of the domestic cat in transmission. Veterinary Parasitology 52, 207210. doi: 10.1016/0304-4017(94)90112-0.CrossRefGoogle ScholarPubMed
Njagi, O. N., Entzeroth, R., Nyaga, P. N. and Musoke, A. J. (2004). Monoclonal antibodies identify two neutralization-sensitive epitopes in Besnoitia besnoiti endocytes. Parasitology Research 94, 247253. doi: 10.1007/s00436-004-1210-9.CrossRefGoogle ScholarPubMed
Olias, P., Schade, B. and Mehlhorn, H. (2011). Molecular pathology, taxonomy and epidemiology of Besnoitia species (Protozoa: Sarcocystidae). Infection, Genetics and Evolution 11, 15641576. doi: 10.1016/j.meegid.2011.08.006.CrossRefGoogle Scholar
Packham, A. E., Sverlow, K. W., Conrad, P. A., Loomis, E. F., Rowe, J. D., Anderson, M. L., Marsh, A. E., Cray, C. and Barr, B. C. (1998). A modified agglutination test for Neospora caninum: development, optimization, and comparison to the indirect fluorescent-antibody test and enzyme-linked immunosorbent assay. Clinical and Diagnostic Laboratory Immunology 5, 467473.Google ScholarPubMed
Peteshev, V. M., Galuzo, I. G. and Polomoshov, A. P. (1974). Cats – definitive hosts Besnoitia (Besnoitia besnoiti) (in Russian). Izvestiae Akademii Nauk Kazakheskan SSR B, 3338.Google Scholar
Pipano, E. (1997). Vaccines against hemoparasitic diseases in Israel with special reference to quality assurance. Tropical Animal Health and Production 29, 86S90S.CrossRefGoogle ScholarPubMed
Pols, J. W. (1954). The artificial transmission of Globidium besnoiti Marotel, 1912, to cattle and rabbits. Journal of the South African Veterinary Medical Association 25, 3744.Google Scholar
Pols, J. W. (1960). Studies on bovine besnoitiosis with special reference to the aetiology. Onderstepoort Journal of Veterinary Research 28, 265356.Google Scholar
Reis, Y., Cortes, H., Viseu, M. L., Fazendeiro, I., Leitão, A. and Soares, H. (2006). Microtubule cytoskeleton behavior in the initial steps of host cell invasion by Besnoitia besnoiti . FEBS Letters 580, 46734682. doi: 10.1016/j.febslet.2006.07.050.CrossRefGoogle ScholarPubMed
Rinaldi, L., Maurelli, M. P., Musella, V., Bosco, A., Cortes, H. and Cringoli, G. (2013). First cross-sectional serological survey on Besnoitia besnoiti in cattle in Italy. Parasitology Research 112, 18051807. doi: 10.1007/s00436-012-3241-y.CrossRefGoogle ScholarPubMed
Rinder, H., Rausch, R. L., Takahashi, K., Kopp, H., Thomschke, A. and Loscher, T. (1997). Limited range of genetic variation in Echinococcus multilocularis . Journal of Parasitology 83, 10451050.CrossRefGoogle ScholarPubMed
Romand, S., Thulliez, P. and Dubey, J. P. (1998). Direct agglutination test for serologic diagnosis of Neospora caninum infection. Parasitology Research 84, 5053. doi: 10.1007/s004360050355.CrossRefGoogle ScholarPubMed
Rommel, M. (1989). Recent advances in the knowledge of the biology of the cyst-forming coccidian. Angewandte Parasitologie 30, 173183.Google Scholar
Rostaher, A., Mueller, R. S., Majzoub, M., Schares, G. and Gollnick, N. S. (2010). Bovine besnoitiosis in Germany. Veterinary Dermatology 21, 329334. doi: 10.1111/j.1365-3164.2009.00813.x.Google ScholarPubMed
Sannusi, A. (1991). A simple field diagnostic smear test for bovine besnoitiosis. Veterinary Parasitology 39, 185188. doi: 10.1016/0304-4017(91)90073-5.CrossRefGoogle ScholarPubMed
Schares, G., Basso, W., Majzoub, M., Cortes, H. C. E., Rostaher, A., Selmair, J., Hermanns, W., Conraths, F. J. and Gollnick, N. S. (2009). First in vitro isolation of Besnoitia besnoiti from chronically infected cattle in Germany. Veterinary Parasitology 163, 315322. doi: 10.1016/j.vetpar.2009.04.033.CrossRefGoogle ScholarPubMed
Schares, G., Basso, W., Majzoub, M., Rostaher, A., Scharr, J. C., Langenmayer, M. C., Selmair, J., Dubey, J. P., Cortes, H. C., Conraths, F. J. and Gollnick, N. S. (2010). Comparative evaluation of immunofluorescent antibody and new immunoblot tests for the specific detection of antibodies against Besnoitia besnoiti tachyzoites and bradyzoites in bovine sera. Veterinary Parasitology 171, 3240. doi: 10.1016/j.vetpar.2010.03.017.CrossRefGoogle ScholarPubMed
Schares, G., Basso, W., Majzoub, M., Rostaher, A., Scharr, J. C., Langenmayer, M. C., Selmair, J., Dubey, J. P., Cortes, H. C., Conraths, F. J., Haupt, T., Pürro, M., Raeber, A., Buholzer, P. and Gollnick, N. S. (2011 a). Evaluation of a commercial ELISA for the specific detection of antibodies against Besnoitia besnoiti . Veterinary Parasitology 175, 5259. doi: 10.1016/j.vetpar.2010.09.024.CrossRefGoogle ScholarPubMed
Schares, G., Maksimov, A., Basso, W., Moré, G., Dubey, J. P., Rosenthal, B., Majzoub, M., Rostaher, A., Selmair, J., Langenmayer, M. C., Scharr, J. C., Conraths, F. J. and Gollnick, N. S. (2011 b). Quantitative real time polymerase chain reaction assays for the sensitive detection of Besnoitia besnoiti infection in cattle. Veterinary Parasitology 178, 208216. doi: 10.1016/j.vetpar.2011.01.038.CrossRefGoogle ScholarPubMed
Schares, G., Langenmayer, M. C., Scharr, J. C., Minke, L., Maksimov, P., Maksimov, A., Schares, S., Bärwald, A., Basso, W., Dubey, J. P., Conraths, F. J. and Gollnick, N. S. (2013). Novel tools for the diagnosis and differentiation of acute and chronic bovine besnoitiosis. International Journal for Parasitology 43, 143154. doi: 10.1016/j.ijpara.2012.10.011.CrossRefGoogle ScholarPubMed
Schulz, K. C. A. (1960). A report on naturally acquired besnoitiosis in bovines with special reference to its pathology. Journal of the South African Veterinary Medical Association 31, 2135.Google Scholar
Shin, Y., Lee, E., Shin, G., Kim, Y., Lee, E., Kim, J., Jang, H., Gershwin, L. J., Kim, D., Kim, Y., Kim, G. S., Suh, M. D. and Jung, T. S. (2004). Identification of antigenic proteins from Neospora caninum recognized by bovine immunoglobulins M, E, A and G using immunoproteomics. Proteomics 4, 36003609. doi: 10.1002/pmic.200400963.CrossRefGoogle Scholar
Shin, Y.-S., Shin, G.-W., Kim, Y.-R., Lee, E.-Y., Yang, H.-H., Palaksha, K. J., Youn, H.-J., Kim, J.-H., Kim, D.-Y., Marsh, A. E., Lakritz, J. and Jung, T. S. (2005). Comparison of proteome and antigenic proteome between two Neospora caninum isolates. Veterinary Parasitology 134, 4152. doi: 10.1016/j.vetpar.2005.06.021.CrossRefGoogle ScholarPubMed
Shkap, V., Ungar-Waron, H., Pipano, E. and Greenblatt, C. (1984). Enzyme linked immunosorbent assay for detection of antibodies against Besnoitia besnoiti in cattle. Tropical Animal Health and Production 16, 233238.CrossRefGoogle ScholarPubMed
Shkap, V., Ungar-Waron, H., Pipano, E. and Greenblatt, C. (1985 a). Specific antibodies to Besnoitia besnoiti precipitated from serum of cattle by live parasites and by soluble antigen. Veterinary Immunology and Immunopathology 9, 5357.CrossRefGoogle ScholarPubMed
Shkap, V., De Waal, D. T. and Potgieter, F. T. (1985 b). Chemotherapy of experimental Besnoitia besnoiti infection in rabbits. Onderstepoort Journal of Veterinary Research 52, 289.Google ScholarPubMed
Shkap, V., Pipano, E. and Ungar-Waron, H. (1987 a). Besnoitia besnoiti: chemotherapeutic trials in vivo and in vitro . Revue d’Élevage et de Médecine Vétérinaire des Pays Tropicaux 40, 259264.Google ScholarPubMed
Shkap, V., Pipano, E. and Greenblatt, C. (1987 b). Cultivation of Besnoitia besnoiti and evaluation of susceptibility of laboratory animals to cultured parasites. Veterinary Parasitology 23, 169178.CrossRefGoogle ScholarPubMed
Shkap, V., Ungar-Waron, H. and Pipano, E. (1989). Soluble antigens from culture-grown Besnoitia besnoiti endozoites. Veterinary Parasitology 34, 165170.CrossRefGoogle ScholarPubMed
Shkap, V., Ungar-Waron, H. and Pipano, E. (1990). Identification and partial purification of soluble antigens from culture-grown Besnoitia besnoiti endozoites. Revue d’Élevage et de Médecine Vétérinaire des Pays Tropicaux 43, 6368.Google ScholarPubMed
Shkap, V., Pipano, E., Marcus, S. and Krigel, Y. (1994). Bovine besnoitiosis: transfer of colostral antibodies with observations possibly relating to natural transmission of the infection. Onderstepoort Journal of Veterinary Research 61, 273275.Google ScholarPubMed
Shkap, V., Reske, A., Pipano, E., Fish, L. and Baszler, T. (2002). Immunological relationship between Neospora caninum and Besnoitia besnoiti . Veterinary Parasitology 106, 3543.CrossRefGoogle ScholarPubMed
Soulsby, E. J. L. (1982). Helminths, Arthropods and Protozoa of Domesticated Animals. Baillière Tindall, London, UK.Google Scholar
Tenter, A. M. and Johnson, A. M. (1997). Phylogeny of the tissue cyst-forming coccidia. Advances in Parasitology 39, 69139. doi: 10.1016/S0065-308X(08)60045-7.CrossRefGoogle ScholarPubMed
Van Heerden, J., Els, H. J., Raubenheimer, E. J. and Williams, J. H. (1993). Besnoitiosis in a horse. Journal of the South African Veterinary Association 64, 9295.Google ScholarPubMed
Waap, H., Cardoso, R., Marcelino, E., Malta, J., Cortes, H. and Leitão, A. (2011). A modified agglutination test for the diagnosis of Besnoitia besnoiti infection. Veterinary Parasitology 178, 217222. doi: 10.1016/j.vetpar.2011.01.035.CrossRefGoogle Scholar
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A review on bovine besnoitiosis: a disease with economic impact in herd health management, caused by Besnoitia besnoiti (Franco and Borges, 1916)
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