A model for chronic bovine besnoitiosis: Parasite stage and inoculation route are key factors.
Besnoitia besnoiti
bradyzoites
chronic besnoitiosis
in vivo model
inoculation routes
Journal
Transboundary and emerging diseases
ISSN: 1865-1682
Titre abrégé: Transbound Emerg Dis
Pays: Germany
ID NLM: 101319538
Informations de publication
Date de publication:
Jan 2020
Jan 2020
Historique:
received:
29
03
2019
revised:
21
08
2019
accepted:
21
08
2019
pubmed:
5
9
2019
medline:
27
5
2020
entrez:
5
9
2019
Statut:
ppublish
Résumé
In this work, an experimental model for chronic besnoitiosis in bovine was developed and characterized. Using a previously established calf model, two new variables (parasite stage and inoculation route) were combined and used. Twelve Holstein Friesian 3-month-old male calves were randomly divided into four groups of three animals each. Bradyzoites were obtained from a chronically infected bull and used for inoculation via three different inoculation routes. Three groups were inoculated with 10
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
234-249Subventions
Organisme : Ministerio de Economía y Competitividad
ID : AGL2013- 46442-R; AGL2016-75202-R
Organisme : Ministerio de Economía y Competitividad
ID : BES-2014-069839
Organisme : Comunidad de Madrid
ID : PLATESA 2-CM
Organisme : Comunidad de Madrid
ID : P2018/BAA- 4370
Organisme : Ministerio de Educación, Cultura y Deporte
ID : FPU 13/05481
Informations de copyright
© 2019 Blackwell Verlag GmbH.
Références
Álvarez-García, G., Frey, C. F., Mora, L. M., & Schares, G. (2013). A century of bovine besnoitiosis: An unknown disease re-emerging in Europe. Trends in Parasitology, 29(8), 407-415. https://doi.org/10.1016/j.pt.2013.06.002
Álvarez-García, G., García-Lunar, P., Gutiérrez-Expósito, D., Shkap, V., & Ortega-Mora, L. M. (2014). Dynamics of Besnoitia besnoiti infection in cattle. Parasitology, 141(11), 1419-1435. https://doi.org/10.1017/S0031182014000729
Arranz-Solís, D., Benavides, J., Regidor-Cerrillo, J., Horcajo, P., Castaño, P., del Carmen Ferreras, M., … Ortega-Mora, L. M. (2016). Systemic and local immune responses in sheep after Neospora caninum experimental infection at early, mid and late gestation. Veterinary Research, 47(1), 1-13. https://doi.org/10.1186/s13567-015-0290-0
Basso, W., Lesser, M., Grimm, F., Hilbe, M., Sydler, T., Trösch, L., … Deplazes, P. (2013). Bovine besnoitiosis in Switzerland: Imported cases and local transmission. Veterinary Parasitology, https://doi.org/10.1016/j.vetpar.2013.09.013
Basson, P. A., McCully, R. M., & Bigalke, R. D. (1970). Observations on the pathogenesis of bovine and antelope strains of Besnoitia besnoiti (Marotel, 1912) infection in cattle and rabbits. The Onderstepoort Journal of Veterinary Research, 37(2), 105-126.
Benavides, J., Collantes-fernández, E., Ferre, I., Pérez, V., Campero, C., Mota, R., … Ortega-mora, L. M. (2014). Experimental ruminant models for bovine neosporosis: What is known and what is needed. Parasitology, 141(11), 1471-1488. https://doi.org/10.1017/S0031182014000638
Bigalke, R. D. (1968). New concepts on the epidemiological features of bovine besnoitiosis as determined by laboratory and field investigations. The Onderstepoort Journal of Veterinary Research., 35(1), 3-137.
Bigalke, R. D., Schoeman, J. H., & 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. The Onderstepoort Journal of Veterinary Research, 41(1), 1-5.
Cervantes-Valencia, M. E., Hermosilla, C., Alcala-Canto, Y., Tapia, G., Taubert, A., & Silva, L. M. (2018). Antiparasitic efficacy of curcumin against Besnoitia besnoiti tachyzoites in vitro. Frontiers in Veterinary Science, 5, 333. https://doi.org/10.3389/fvets.2018.00333
Collantes-Fernandez, E., Arrighi, R. B. G., Álvarez-García, G., Weidner, J. M., Regidor-Cerrillo, J., Boothroyd, J. C., … Barragan, A. (2012). Infected dendritic cells facilitate systemic dissemination and transplacental passage of the obligate intracellular parasite Neospora caninum in mice. PLoS ONE, 7(3), e321-e323. https://doi.org/10.1371/journal.pone.0032123
Cortes, H. C., Muller, N., Boykin, D., Stephens, C. E., & Hemphill, A. (2011). In vitro effects of arylimidamides against infection in vero cells. Parasitology, 138(5), 583-592. https://doi.org/10.1017/S0031182011000114
Cortes, H. C., Reis, Y., Gottstein, B., Hemphill, A., Leitao, A., & Muller, N. (2007). Application of conventional and real-time fluorescent ITS1 rDNA PCR for detection of Besnoitia besnoiti infections in bovine skin biopsies. Veterinary Parasitology, 146(3-4), 352-356. https://doi.org/10.1016/j.vetpar.2007.03.003
Diesing, L., Heydorn, A. O., Matuschka, F. R., Bauer, C., Pipano, E., de Waal, D. T., & Potgieter, F. T. (1988). Besnoitia besnoiti: Studies on the definitive host and experimental infections in cattle. Parasitology Research, 75(2), 114-117. https://doi.org/10.1007/BF00932710
Diezma-Díaz, C., Ferre, I., Re, M., Jiménez-Meléndez, A., Tabanera, E., González-Huecas, M., … Álvarez-García, G. (2019). The route of Besnoitia besnoiti tachyzoites inoculation does not influence the clinical outcome of the infection in calves. Veterinary Parasitology, 267, 21-25. https://doi.org/10.1016/j.vetpar.2019.02.001
Diezma-Díaz, C., Jiménez-Meléndez, A., Fernández, M., Gutiérrez-Expósito, D., García-Lunar, P., Ortega-Mora, L., … Álvarez-García, G. (2017). Bovine chronic besnoitiosis in a calf: Characterization of a novel Besnoitia besnoiti isolate from an unusual case report. Veterinary Parasitology, 247, 10-18.
Diezma-Díaz, C., Jiménez-Meléndez, A., Re, M. T., Ferre, I., Ferreras, M., & d. C., Gutiérrez-Expósito, D., … Álvarez-García, G., (2018). Effect of parasite dose and host age on the infection with Besnoitia besnoiti tachyzoites in cattle. Transboundary and Emerging Diseases, 65(6), 1979-1990. https://doi.org/10.1111/tbed.12980
Esteban-Gil, A., Jacquiet, P., Florentin, S., Decaudin, A., Berthelot, X., Ronsin, P., … Picard-Hagen, N. (2016). Does bovine besnoitiosis affect the sexual function of chronically infected bulls? Theriogenology, 86(5), 1325-1332. https://doi.org/10.1016/j.theriogenology.2016.04.074
European Food Safety Authority (2010). Scientific statement on bovine besnoitiosis. Available at http://www.efsa.europa.eu/sites/default/files/scientific/output/files/main_documents/1499.pdf accessed 19 January 2018.
Fernández-García, A., Álvarez-García, G., Marugan-Hernandez, V., García-Lunar, P., Aguado-Martinez, A., Risco-Castillo, V., & 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(8), 999-1008. https://doi.org/10.1017/S003118201300036X
Fernández-García, A., Risco-Castillo, V., Pedraza-Díaz, S., Aguado-Martínez, A., Álvarez-García, G., Gómez-Bautista, M., … Ortega-Mora, L. M. (2009). First isolation of Besnoitia besnoiti from a chronically infected cow in Spain. The Journal of Parasitology, 95(2), 474-476. https://doi.org/10.1645/GE-1772.1
Frenkel, J., & Wilson, H. (1972). Effects of radiation on specific cellular immunities: Besnoitiosis and a herpesvirus infection of hamsters. Journal of Infectious Diseases, 125(3), 216-230. https://doi.org/10.1093/infdis/125.3.216
Frey, C. F., Gutiérrez-Expósito, D., Ortega-Mora, L. M., Benavides, J., Marcén, J. M., Castillo, J. A., … Álvarez-García, G. (2013). Chronic bovine besnoitiosis: Intra-organ parasite distribution, parasite loads and parasite-associated lesions in subclinical cases. Veterinary Parasitology, 197(1-2), 95-103. https://doi.org/10.1016/j.vetpar.2013.04.023
García-Lunar, P., Ortega-Mora, L., Schares, G., Diezma-Díaz, C., & Álvarez-García, G. (2017). A new lyophilized tachyzoite based ELISA to diagnose besnoitia spp. infection in bovids and wild ruminants improves specificity. Veterinary Parasitology, 244, 176-182. https://doi.org/10.1016/j.vetpar.2017.07.029
García-Lunar, P., Regidor-Cerrillo, J., Gutiérrez-Expósito, D., Ortega-Mora, L., & Álvarez-García, G. (2013). First 2-DE approach towards characterising the proteome and immunome of Besnoitia besnoiti in the tachyzoite stage. Veterinary Parasitology, 195(1-2), 24-34. https://doi.org/10.1016/j.vetpar.2012.12.040
Gazzonis, A. L., Alvarez Garcia, G., Maggioni, A., Zanzani, S. A., Olivieri, E., Compiani, R., … Manfredi, M. T. (2017). Serological dynamics and risk factors of Besnoitia besnoiti infection in breeding bulls from an endemically infected purebred beef herd. Parasitology Research, 116(4), 1383-1393. https://doi.org/10.1007/s00436-017-5418-x
Gentile, A., Militerno, G., Schares, G., Nanni, A., Testoni, S., Bassi, P., & 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(2-4), 108-115. https://doi.org/10.1016/j.vetpar.2011.09.014
Gollnick, N. S., Scharr, J. C., Schares, G., & Langenmayer, M. C. (2015). Natural Besnoitia besnoiti infections in cattle: Chronology of disease progression. BMC Veterinary Research, 11, 35-015-0344-6. https://doi.org/10.1186/s12917-015-0344-6
Gutiérrez-Expósito, D., Arnal, M. C., Martínez-Durán, D., Regidor-Cerrillo, J., Revilla, M., L Fernández de Luco, D., … Álvarez-García, G. (2016). The role of wild ruminants as reservoirs of Besnoitia besnoiti infection in cattle. Veterinary Parasitology, 223, 7-13. https://doi.org/10.1016/j.vetpar.2016.04.005
Gutiérrez-Expósito, D., Ferre, I., Ortega-Mora, L. M., & Álvarez-García, G. (2017). Advances in the diagnosis of bovine besnoitiosis: Current options and applications for control. International Journal for Parasitology, 47(12), 737-751. https://doi.org/10.1016/j.ijpara.2017.08.003
Hemphill, A., & Gottstein, B. (2006). Neospora caninum and neosporosis- recent achievements in host and parasite cell biology and treatment. Acta Parasitologica, 51(1), 15-25. https://doi.org/10.2478/s11686-006-0002-z
Hornok, S., Fedak, A., Baska, F., Hofmann-Lehmann, R., & Basso, W. (2014). Bovine besnoitiosis emerging in Central-Eastern Europe, Hungary. Parasites & Vectors, 7, 20-3305-7-20. https://doi.org/10.1186/1756-3305-7-20
Hunsaker, B. D., & Perino, L. J. (2001). Efficacy of intradermal vaccination. Veterinary Immunology and Immunopathology, 79(1-2), 1-13. https://doi.org/10.1016/S0165-2427(01)00244-6
Janitschke, K., De Vos, A. J., & Bigalke, R. D. (1984). Serodiagnosis of bovine besnoitiosis by ELISA and immunofluorescence tests. The Onderstepoort Journal of Veterinary Research, 51(4), 239-243.
Jeffers, V., Tampaki, Z., Kim, K., & Sullivan, W. J. (2018). A latent ability to persist: Differentiation in Toxoplasma gondii. Cellular and Molecular Life Sciences, 75(13), 2355-2373. https://doi.org/10.1007/s00018-018-2808-x
Jiménez-Meléndez, A., Ojo, K. K., Wallace, A. M., Smith, T. R., Hemphill, A., Balmer, V., … Álvarez-García, G. (2017). In vitro efficacy of bumped kinase inhibitors against Besnoitia besnoiti tachyzoites. International Journal for Parasitology, 47(12), 811-821. https://doi.org/10.1016/j.ijpara.2017.08.005
Jiménez-Meléndez, A., Rico-San Román, L., Hemphill, A., Balmer, V., Ortega-Mora, L. M., & Álvarez-García, G. (2018). Repurposing of commercially available anti-coccidials identifies diclazuril and decoquinate as potential therapeutic candidates against Besnoitia besnoiti infection. Veterinary Parasitology, 261, 77-85. https://doi.org/10.1016/j.vetpar.2018.08.015
Jiménez-Ruiz, E., Bech-Sabat, G., Álvarez-García, G., Regidor-Cerrillo, J., Hinojal-Campana, L., & Ortega-Mora, L. M. (2013). Specific antibody responses against Neospora caninum recombinant rNcGRA7, rNcSAG4, rNcBSR4 and rNcSRS9 proteins are correlated with virulence in mice. Parasitology, 140(5), 569-579. https://doi.org/10.1017/S0031182012002041
Joachim, A., Altreuther, G., Bangoura, B., Charles, S., Daugschies, A., Hinney, B., … Sotiraki, S. (2018). WAAVP guideline for evaluating the efficacy of anticoccidials in mammals (pigs, dogs, cattle, sheep). Veterinary Parasitology, 253, 102-119. https://doi.org/10.1016/j.vetpar.2018.02.029
Kabashima, K., Honda, T., Ginhoux, F., & Egawa, G. (2018). The immunological anatomy of the skin. Nature Reviews Immunology, 19(1), 19-30. https://doi.org/10.1038/s41577-018-0084-5
Kumi-Diaka, J., Wilson, S., Sanusi, A., Njoku, C. E., & Osori, D. I. (1981). Bovine besnoitiosis and its effect on the male reproductive system. Theriogenology, 16(5), 523-530. https://doi.org/10.1016/0093-691X(81)90037-6
Lambert, H., Hitziger, N., Dellacasa, I., Svensson, M., & Barragan, A. (2006). Induction of dendritic cell migration upon Toxoplasma gondii infection potentiates parasite dissemination. Cellular Microbiology, 8(10), 1611-1623. https://doi.org/10.1111/j.1462-5822.2006.00735.x
Langenmayer, M. C., Gollnick, N. S., Majzoub-Altweck, M., Scharr, J. C., Schares, G., & Hermanns, W. (2015). Naturally acquired bovine besnoitiosis: Histological and immunohistochemical findings in acute, subacute, and chronic disease. Veterinary Pathology, 52(3), 476-488. 0300985814541705
Liénard, E., Pop, L., Prevot, F., Grisez, C., Mallet, V., Raymond-Letron, I., … Jacquiet, P. (2015). Experimental infections of rabbits with proliferative and latent stages of Besnoitia besnoiti. Parasitology Research, 114(10), 3815-3826. https://doi.org/10.1007/s00436-015-4612-y
Lyons, R. E., McLeod, R., & Roberts, C. W. (2002). Toxoplasma gondii tachyzoite-bradyzoite interconversion. Trends in Parasitology, 18(5), 198-201. https://doi.org/10.1016/S1471-4922(02)02248-1
Madubata, C., Dunams-Morel, D. B., Elkin, B., Oksanen, A., & Rosenthal, B. M. (2012). Evidence for a recent population bottleneck in an apicomplexan parasite of caribou and reindeer, besnoitia tarandi. Infection, Genetics and Evolution : Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases, 12(8), 1605-1613. https://doi.org/10.1016/j.meegid.2012.06.007.
Manuali, E., Lepri, E., Salamida, S., D’Avino, N., Mangili, P., Vitellozzi, G., … Filippini, G. (2011). An outbreak of bovine besnoitiosis in beef cattle born in central Italy. Transboundary and Emerging Diseases, 58(5), 464-467. https://doi.org/10.1111/j.1865-1682.2011.01220.x
McCully, R. M., Basson, P. A., Van Niekerk, J. W., & Bigalkie, R. D. (1966). Observations on Besnoitia cysts in the cardiovascular system of some wild antelopes and domestic cattle. Onderstepoort Journal of Veterinary Research, 33(2), 245-276.
Müller, J., Manser, V., & Hemphill, A. (2018). In vitro treatment of Besnoitia besnoiti with the naphto-quinone buparvaquone results in marked inhibition of tachyzoite proliferation, mitochondrial alterations and rapid adaptation of tachyzoites to increased drug concentrations. Parasitology, 146(1), 112-120. https://doi.org/10.1017/S0031182018000975
Nieto-Rodríguez, J. M., Calero-Bernal, R., Álvarez-García, G., Gutiérrez-Expósito, D., Redondo-García, E., Fernández-García, J. L., & Martínez-Estéllez, M. Á. H. (2016). Characterization of an outbreak of emerging bovine besnoitiosis in southwestern Spain. Parasitology Research, 115(7), 2887-2892. https://doi.org/10.1007/s00436-016-5050-1
Nobel, T. A., Neumann, M., Klopper, U., & Perl, S. (1981). Cysts of Besnoitia besnoiti in genital organs of the cow. Bulletin De L'académie Vétérinaire De France, 50, 569-574.
Pols, J. W. (1960). Studies on bovine besnoitiosis with special reference to the aetiology. Onderstepoort Journal of Veterinary Research, 28(3), 265-356.
Regidor-Cerrillo, J., Díez-Fuertes, F., García-Culebras, A., Moore, D. P., González-Warleta, M., Cuevas, C., … Ortega-Mora, L. M. (2013). Genetic diversity and geographic population structure of bovine Neospora caninum determined by microsatellite genotyping analysis. PLoS ONE, 8(8), e72678. https://doi.org/10.1371/journal.pone.0072678
Regidor-Cerrillo, J., Gómez-Bautista, M., Del Pozo, I., Jiménez-Ruiz, E., Aduriz, G., & Ortega-Mora, L. M. (2010). Influence of Neospora caninum intra-specific variability in the outcome of infection in a pregnant BALB/c mouse model. Veterinary Research, 41(4), 52. https://doi.org/10.1051/vetres/2010024
Rojo-Montejo, S., Collantes-Fernández, E., López-Pérez, I., Risco-Castillo, V., Prenafeta, A., & Ortega-Mora, L. M. (2012). Evaluation of the protection conferred by a naturally attenuated Neospora caninum isolate against congenital and cerebral neosporosis in mice. Veterinary Research, 43(1), 43-62. https://doi.org/10.1186/1297-9716-43-62
Romani, N., Thurnher, M., Idoyaga, J., Steinman, R. M., & Flacher, V. (2010). Targeting of antigens to skin dendritic cells: Possibilities to enhance vaccine efficacy. Immunology and Cell Biology, 88(4), 424-430. https://doi.org/10.1038/icb.2010.39
Ryan, E. G., Lee, A., Carty, C., O'Shaughnessy, J., Kelly, P., Cassidy, J. P., … de Waal, T. (2016). Bovine besnoitiosis (Besnoitia besnoiti) in an Irish dairy herd. The Veterinary Record, 178(24), 608. https://doi.org/10.1136/vr.103683
Sánchez-Sánchez, R., Ferre, I., Re, M., Vázquez, P., Ferrer, L. M., Blanco-Murcia, J., … Ortega-Mora, L. M. (2018). Safety and efficacy of the bumped kinase inhibitor BKI-1553 in pregnant sheep experimentally infected with Neospora caninum tachyzoites. International Journal for Parasitology: Drugs and Drug Resistance, 8(1), 112-124. https://doi.org/10.1016/j.ijpddr.2018.02.003
Schares, G., Maksimov, A., Basso, W., Moré, G., Dubey, J. P., Rosenthal, B., … Gollnick, N. S. (2011). Quantitative real time polymerase chain reaction assays for the sensitive detection of Besnoitia besnoiti infection in cattle. Veterinary Parasitology, 178(3-4), 208-216. https://doi.org/10.1016/j.vetpar.2011.01.038
Shkap, V. (1986). Antigenicity of Besnoitia besnoiti with special reference to prophylactic immunization. Doctoral thesis. Hebrew University, Jerusalem, Israel.
Shkap, V., Pipano, E., & Ungar-Waron, H. (1987). Besnoitia besnoiti: Chemotherapeutic trials in vivo and in vitro. Revue D'elevage Et De Medecine Veterinaire Des Pays Tropicaux, 40(3), 259-264.
Umeshappa, C. S., Singh, K. P., Channappanavar, R., Sharma, K., Nanjundappa, R. H., Saxena, M., … Sharma, A. K. (2011). A comparison of intradermal and intravenous inoculation of bluetongue virus serotype 23 in sheep for clinico-pathology, and viral and immune responses. Veterinary Immunology and Immunopathology, 141(3-4), 230-238. https://doi.org/10.1016/j.vetimm.2011.03.005
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 Diergeneeskundig Tijdschrift, 84(4), 205-211.
Verma, S., Ajzenberg, D., Rivera-Sánchez, A., Su, C., & Dubey, J. (2015). Genetic characterization of Toxoplasma gondii isolates from Portugal, Austria and Israel reveals higher genetic variability within the type II lineage. Parasitology, 142(7), 948-957.