Seroprevalence of infectious agents affecting the reproductive system of water buffaloes (Bubalus bubalis) in Costa Rica
DOI:
https://doi.org/10.15359/rcv.43-1.1Keywords:
bovine leukosis virus, bovine herpesvirus type 1, bovine viral diarrhea virus, Neospora caninum, seroprevalence, reproductionAbstract
Water buffaloes (Bubalus bubalis) are susceptible to most pathogens affecting cattle, leading to reproductive problems and decreased productivity, which significantly impacts livestock production. So far, the prevalence of brucellosis is the only pathogen that has been determined for this population in Costa Rica. The objective of this study was to determine the seroprevalence of bovine leukosis virus (BLV), bovine herpes virus type 1 (BHV-1), bovine viral diarrhea virus (BVDV), and Neospora caninum in buffaloes in Costa Rica. A total of 372 blood samples were collected from buffaloes older than 15 months across 20 farms in the provinces of Alajuela, Guanacaste, San José, Heredia, Limón, and Puntarenas between May and August 2020. The blood samples were analyzed using commercial enzyme-linked immunosorbent assays (IDvet, Montpellier, France) to determine each agent’s overall and farm-level seroprevalence. The assessed seroprevalences for BHV-1, BVDV, and N. caninum were 54.0%, 41.7%, and 64.3%, respectively. Seropositive individuals for BHV-1, BVDV, and N. caninum were identified in all provinces analyzed. The highest prevalence for BHV-1 was found in Alajuela (65.3%), Heredia (52.8%), and Limón (45.4%); for BVDV in San José (68.2%) and Alajuela (63.9%); and for N. caninum in San José (86.4%), Alajuela (69.4%), Guanacaste (66.6%), and Limón (61.4%). Among the farms analyzed 85.0%, 75.0%, and 100% tested positive for BHV-1, BVDV, and N. caninum, respectively. No BLV-positive animals were detected on any farm. This is the first study to report the prevalence of BHV-1, BVDV, and N. caninum in buffaloes from Costa Rica. These pathogens may contribute to farm reproductive problems, highlighting the need for further investigation into their effects to establish control and prevention programs.
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Ali, S., Rola-Łuszczak, M., Osiński, Z., Bibi, N., & Kuźmak, J. (2021). Bayesian estimation of the true seroprevalence and risk factor analysis of bovine leukemia virus infection in Pakistan. Animals, 11(5), 1404. https://doi.org/10.3390/ani11051404
Alves, M., Fernandes, F. D., Monteiro, F. L., Bräunig, P., Cargnelutti, J. F., Flores, E. F., Weiblen, R., & Vogel, F. S. F. (2020). Co-infection by Neopora caninum and bovine viral diarrhea virus in cattle from Rio Grande do Sul, Brazil, destined to exportation. Pesquisa Veterinaria Brasileira, 40(8), 593–597. https://doi.org/10.1590/1678-5150-pvb-6468
Asadpour, R., & Jafari, R. (2010). Detection of bovine leukosis provirus in blood and semen samples of bulls. Comparative Clinical Pathology, 21(2), 187–191. https://doi.org/10.1007/s00580-010-1083-5
Baker, J. C. (1995). The clinical manifestations of bovine viral diarrhea infection. Veterinary Clinics of North America-food Animal Practice, 11(3), 425–445. https://doi.org/10.1016/s0749-0720(15)30460-6
Barrantes-Guevara, E. (2019) Caracterización de los sistemas de producción bubalina en las zonas agroclimáticas y provincias de Costa Rica. Documento de avance, comunicación personal del autor, Vicerrectoría Investigación, Dirección de Investigación y Transferencia, Sede Atenas, Universidad Técnica Nacional
Bartels, C., Huinink, I., Beiboer, M., Van Schaik, G., Wouda, W., Dijkstra, T., & Stegeman, A. (2007). Quantification of vertical and horizontal transmission of Neospora caninum infection in Dutch dairy herds. Veterinary Parasitology, 148(2), 83–92. https://doi.org/10.1016/j.vetpar.2007,06,004
Brock, K. V. (2004). The many faces of bovine viral diarrhea virus. Veterinary Clinics of North America: Food Animal Practice, 20(1), 1-3. https://doi.org/10.1016/j.cvfa.2003.12,002
Burny, A., Bruck, C., Cleuter, Y., Couez, D., Deschamps, J., Gregoire, D., Ghysdael, J., Kettmann, R., Mammerickx, M., & Marbaix, G. (1985). Bovine leukaemia virus and enzootic bovine leukosis. The Onderstepoort Journal of Veterinary Research, 52(3), 133–144.
Campero, C. M., Pérez, A., Moore, D., Crudeli, G., Benitez, D., Draghi, M. G., Cano, D., Konrad, J. L., & Odeón, A. C. (2007). Occurrence of antibodies against Neospora caninum in water buffaloes (Bubalus bubalis) on four ranches in Corrientes province, Argentina. Veterinary Parasitology, 150(1–2), 155–158. https://doi.org/10.1016/j.vetpar.2007,09,002
Cedeño-Sánchez, H., Burgos-García, B., Zambrano-Aveiga, J., Jurado-Hidalgo, M. E., Zambrano-Moreira, P., Lugo-Almarza, M., Farias, M. E., & Angulo-Cubillán, F. (2022). Bovine Herpesvirus-1 antibodies levels and associated Risk Factors in unvaccinated Dairy Herds from tropical wet weather, Ecuador. Revista Científica, XXXII (single), 1–5. https://doi.org/10.52973/rcfcv-e32088
Chaves, A., Romero, J.J., Romero, L., Pereira, R., Jiménez, C., Haas, L., Greiser-Wilke, I. & Dolz, G. (2008). Genetic typing of bovine viral diarrhea virus isolates from Costa Rica. Cienc. Vet. 26(1), 37-46. https://www.revistas.una.ac.cr/index.php/veterinaria/article/view/4693
Ciuca, L., Borriello, G., Bosco, A., D’Andrea, L. D., Cringoli, G., Ciaramella, P., Maurelli, M. P., Di Loria, A., Rinaldi, L., & Guccione, J. (2020). Seroprevalence and Clinical Outcomes of Neospora caninum, Toxoplasma gondii and Besnoitia besnoiti Infections in Water Buffaloes (Bubalus bubalis). Animals, 10(3), 532. https://doi.org/10.3390/ani10030532
Da Silva, J. B., Nicolino, R. R., Fagundes, G. M., Barbosa, J. D., Reis, A. D. S. B., Da Silva Lima, D. H., De Oliveira, C. a. F., & Da Fonseca, A. H. (2017). Serological survey of Neospora caninum and Toxoplasma gondii in cattle (Bos indicus) and water buffaloes (Bubalus bubalis) in ten provinces of Brazil. Comparative Immunology Microbiology and Infectious Diseases, 52, 30–35. https://doi.org/10.1016/j.cimid.2017,05,005
De Oliveira, C. H., Resende, C. F., De Oliveira, C. a. F., Barbosa, J. C., Fonseca, A. A., Leite, R. C., & Reis, J. K. P. D. (2016). Absence of Bovine leukemia virus (BLV) infection in buffaloes from Amazon and southeast region in Brazil. Preventive Veterinary Medicine. https://doi.org/10.1016/j.prevetmed.2016,05,002
Dhaliwal, G. (2016). Chapter 16: Infectious diseases affecting buffalo reproduction: Causes, diagnosis and control. Herd Health Management of Dairy Buffalo. Central Institute for Research on Buffaloes. Guru Angad Dev Veterinary and Animal Sciences University, India.
Dijkstra, T., Eysker, M., Schares, G., Conraths, F. J., Wouda, W., & Barkema, H. W. (2001). Dogs shed Neospora caninum oocysts after ingestion of naturally infected bovine placenta but not after ingestion of colostrum spiked with Neospora caninum tachyzoites. International Journal for Parasitology, 31(8), 747–752. https://doi.org/10.1016/s0020-7519(01)00230-2
Dubey, J. P., & Schares, G. (2011). Neosporosis in animals—The last five years. Veterinary Parasitology, 180(1–2), 90–108. https://doi.org/10.1016/j.vetpar.2011,05,031
Fagiolo, A., Roncoroni, C., Lai, O., & Borghese, A. (2004). Buffalo pathologies. In A. Borghese (Ed.), Buffalo production and research (pp. 249-296). Food and Agriculture Organization of the United Nations. https://www.researchgate.net/publication/286302484_Buffalo_pathologies
Flórez, J. C. R., Peláez, E. a. P., Marín, N. T., López, J. C. E., & Corrales, J. (2021). Prevalencia del virus de la leucosis bovina en búfalos de agua en la región centro occidental de Colombia. Revista Mexicana De Ciencias Pecuarias, 12(2), 419–436. https://doi.org/10.22319/rmcp.v12i2.5459
Gennari, S. M., Rodrigues, A., Viana, R. B., & Da Cruz Cardoso, E. (2005). Occurrence of anti-Neospora caninum antibodies in water buffaloes (Bubalus bubalis) from the Northern region of Brazil. Veterinary Parasitology, 134(1–2), 169–171. https://doi.org/10.1016/j.vetpar2005,05,064
Gómez, A. (2015). Determinación de la prevalencia de Diarrea Viral Bovina (DVB) y Vulvovaginitis Infecciosa Bovina (VIB) en explotaciones de búfalos (Bubalus bubalis) en la región de Flores, Costa Cuca, Quetzaltenango. (Tesis de grado de licenciatura) Universidad San Carlos de Guatemala.
Gondim, L. F. P., Gao, L., & McAllister, M. M. (2002). Improved production of Neospora caninum oocysts, cyclical oral transmission between dogs and cattle, and in vitro isolation from oocysts. Journal of Parasitology, 88(6), 1159–1163. https://doi.org/10.1645/0022-3395(2002)088
Gondim, L. F. P., McAllister, M. M., Pitt, W. C., & Zemlicka, D. E. (2004). Coyotes (Canis latrans) are definitive hosts of Neospora caninum. International Journal for Parasitology, 34(2), 159–161. https://doi.org/10.1016/j.ijpara.2004,01,001
Grazziotto, N. M., Maidana, S. S., & Romera, S. A. (2020). Susceptibilidad de los búfalos de agua frente a diferentes enfermedades infecciosas. Revista Veterinaria, 31(2), 215. https://doi.org/10.30972/vet.3124750
Hall, C. A., Reichel, M. P., & Ellis, J. (2005). Neospora abortions in dairy cattle: diagnosis, mode of transmission and control. Veterinary Parasitology, 128(3–4), 231–241. https://doi.org/10.1016/j.vetpar.2004.12,012
Hernández-Mora, G., Bonilla-Montoya, R., Barrantes-Granados, O., Esquivel-Suárez, A., Montero-Caballero, D., González-Barrientos, R., Fallas-Monge, Z., Palacios-Alfaro, J. D., Baldi, M., Campos, E., Chanto, G., Barquero-Calvo, E., Chacón-Díaz, C., Chaves-Olarte, E., Verri, C. G., Romero-Zúñiga, J., & Moreno, E. (2017). Brucellosis in mammals of Costa Rica: An epidemiological survey. PLOS ONE, 12(8), e0182644. https://doi.org/10.1371/journal.pone,0182644
Instituto Nacional de Estadistica y Censos (INEC). (2015). VI Censo Nacional Agropecuario 2014. Licencia Renum 2014. https://sistemas.inec.cr/pad5/index.php/catalog/154/data-dictionary/F1?file_name=CRI_CENAGRO_LICENCIA_RENUM_2014_021115
Jara, V. J., Chávez, V. A., Casas, A. E., Sánchez, P. N., Moreno‐López, J., & Mérza, M. (2011). Determinación de anticuerpos contra Neospora caninum en búfalos de agua (Bubalus bubalis) en la Amazonía peruana. Revista De Investigaciones Veterinarias Del Perú, 22(1). https://doi.org/10.15381/rivep.v22i1.123
Johnson, R., & Kaneene, J. B. (1991). Bovine leukemia virus. Part IV. Economic impact and control measures. Compendium On Continuing Education For The Practicing Veterinarian, 13(11), 1727-173417361737.
Kahrs R. (1968). The relationship of bovine viral diarrhea-mucosal disease to abortion in cattle. J Am Vet Med Assoc 1968;153:1652–5.
Lindsay, D. S., Dubey, J. P., & Duncan, R. B. (1999). Confirmation that the dog is a definitive host for Neospora caninum. Veterinary Parasitology, 82(4), 327–333. https://doi.org/10.1016/s0304-4017(99)00054-0
Martínez-Burnes, J., Barrios-García, H., La Fuente, V. C., Corona-González, B., Alvarez, D. O., & Romero-Salas, D. (2024). Viral Diseases in Water Buffalo (Bubalus bubalis): New Insights and Perspectives. Animals, 14(6), 845. https://doi.org/10.3390/ani14060845
Martucciello, A., De Mia, G. M., Giammarioli, M., De Donato, I., Iovane, G., & Galiero, G. (2009). Detection of Bovine Viral Diarrhea Virus from Three Water Buffalo Fetuses (Bubalus Bubalis) in Southern Italy. Journal of Veterinary Diagnostic Investigation, 21(1), 137–140. https://doi.org/10.1177/104063870902100123
McAllister, M. M., Dubey, J. P., Lindsay, D. S., Jolley, W. R., Wills, R. A., & McGuire, A. (1998). Dogs are definitive hosts of Neospora caninum. PubMed, 28(9), 1473–1478. https://pubmed.ncbi.nlm.nih.gov/9770635
McClurkin, A. W., Littledike, E., Cutlip, R. C., Frank, G. H., Coria, M. F., & Bolin, S. R. (1984). Production of cattle immunotolerant to bovine viral diarrhea virus. PubMed, 48(2), 156–161. https://pubmed.ncbi.nlm.nih.gov/6326980
Monti, G. E., Frankena, K., & De Jong, M. C. M. (2007). Transmission of bovine leukaemia virus within dairy herds by simulation modelling. Epidemiology And Infection, 135(5), 722-732. https://doi.org/10.1017/s0950268806007357
Motta Giraldo, Javier Leonardo, Waltero García, Indira, & Abeledo, María Antonia. (2013). Prevalencia de anticuerpos al virus de la diarrea viral bovina, Herpesvirus bovino 1 y Herpesvirus bovino 4 en bovinos y búfalos en el Departamento de Caquetá, Colombia. Revista de Salud Animal, 35(3), 174-181. Recuperado en 05 de agosto de 2024, de http://scielo.sld.cu/scielo.php?script=sci_arttext&pid=S0253-570X2013000300005&lng=es&tlng=es.
Motta Giraldo, J. L. M., Hoyos, J. A. C., García, I. W., & Abeledo, M. A. (2014). Prevalencia de anticuerpos a Brucella abortus, Leptospira sp. y Neospora caninum en hatos bovinos y bubalinos en el Departamento de Caquetá, Colombia. Revista de Salud Animal, 36(2), 80-89. http://scielo.sld.cu/pdf/rsa/v36n2/rsa02214.pdf
Neverauskas, C. E., Nasir, A., & Reichel, M. P. (2015). Prevalence and distribution of Neospora caninum in water buffalo (Bubalus bubalis) and cattle in the Northern Territory of Australia. Parasitology International, 64(5), 392–396. https://doi.org/10.1016/j.parint.2015,05,009
Maidana, S. S., Konrad, J. L., Craig, M. I., Zabal, O., Mauroy, A., Thiry, E., Crudeli, G., & Romera, S. A. (2014). First report of isolation and molecular characterization of bubaline herpesvirus 1 (BuHV1) from Argentinean water buffaloes. Archives of Virology, 159(11), 2917–2923. https://doi.org/10.1007/s00705-014-2146-8
Paixão, S. F., Fritzen, J. T. T., & Alfieri, A. (2017). Virus neutralization technique as a tool to evaluate the virological profile for bovine viral diarrhea virus infection in dairy water buffalo (Bubalus bubalis) herds. Tropical Animal Health and Production, 50(4), 911–914. https://doi.org/10.1007/s11250-017-1503-5
Pastrana, M. E. O., Carrascal-Triana, E. L., Ramos, M. D., & Ortega, D. O. (2022). Seroprevalence and associated factors of viral agents of the bovine respiratory disease complex in buffaloes of Colombia. Ciencia Rural, 52(8). https://doi.org/10.1590/0103-8478cr20210215
Reichel, M. P., McAllister, M. M., Nasir, A., & Moore, D. (2015). A review of Neospora caninum in water buffalo (Bubalus bubalis). Veterinary Parasitology, 212(3–4), 75–79. https://doi.org/10.1016/j.vetpar.2015,08,008
Rosales-Rodríguez, R. (2011). Situación del búfalo de agua en Costa Rica. Revista Tecnología En Marcha, 24(5), pág. 19. https://revistas.tec.ac.cr/index.php/tec_marcha/article/view/162
Romero, J., & Frankena, K. (2003). The effect of the dam–calf relationship on serostatus to Neospora caninum on 20 Costa Rican dairy farms. Veterinary Parasitology, 114(3), 159–171. https://doi.org/10.1016/s0304-4017(03)00135-3
Romero, J. (2006). Neosporosis Bovina (Neospora Caninum) Descripción Impacto Económico y Estrategias para su Control. Ciencias Veterinarias, 24(1), 33-48. https://www.revistas.una.ac.cr/index.php/veterinaria/article/view/4756
Romero-Salas, D., Alvarado-Esquivel, C., Domínguez-Aguilar, G., Cruz-Romero, A., Ibarra-Priego, N., Barrientos-Salcedo, C., Aguilar-Domínguez, M., Canseco-Sedano, R., Espín-Iturbe, L. T., Sánchez-Anguiano, L. F., Hernández-Tinoco, J., & De León, A. A. P. (2017). Seroepidemiology of infection with Neospora caninum, Leptospira, and bovine herpesvirus type 1 in water buffaloes (Bubalus bubalis) in Veracruz, Mexico. European Journal Of Microbiology & Immunology, 7(4), 278-283. https://doi.org/10.1556/1886.2017,00029
Sarangi, L. N., Reddy, R. V. C., Rana, S. K., Naveena, T., Ponnanna, N. M., & Sharma, G. K. (2021). Sero-diagnostic efficacy of various ELISA kits for diagnosis of infectious bovine rhinotracheitis (IBR) in cattle and buffaloes in India. Veterinary Immunology and Immunopathology, 241, 110324. https://doi.org/10.1016/j.vetimm.2021.110324
Salguero-Romero, J. L., Romero-Salas, D., Cruz-Romero, A., Alonso-Díaz, M. A., Aguilar-Domínguez, M., Sánchez-Montes, S., Lammoglia-Villagómez, M. A., Chaparro-Gutiérrez, J. J., Nogueira-Domingues, L., León, A. A. P., & Dubey, J. (2021). Serosurveillance and risk factors for Neospora caninum infection in water buffaloes (B. bubalis) from central and southern Mexico. Veterinary Parasitology Regional Studies And Reports, 26, 100631. https://doi.org/10.1016/j.vprsr.2021.100631
Schwartz, I. K., & Lévy, D. (1994). Pathobiology of bovine leukemia virus. HAL (Le Centre Pour La Communication Scientifique Directe), 25(6), 521–536. https://hal.archives-ouvertes.fr/hal-00902257
Selim, A., Elhaig, M. M., Moawed, S. A., & El-Nahas, E. M. (2018). Modeling the potential risk factors of bovine viral diarrhea prevalence in Egypt using univariable and multivariable logistic regression analyses. Veterinary World, 11(3), 259–267. https://doi.org/10.14202/vetworld.2018.259-267
Soares, L. B. F., Silva, B. P. E., De Melo Borges, J., De Oliveira, J. M. B., De Macêdo, A. A., Aragão, B. B., Nascimento, S. a. D., & Pinheiro, J. B. (2017). Occurrence of Bovine Viral Diarrhea (BVDV) and Bovine Infectious Rhinotracheitis (IBR) Virus Infections in Buffaloes in Pernambuco state - Brazil. Acta Scientiae Veterinariae, 45(1), 8. https://doi.org/10.22456/1679-9216.80181
Thrusfield, M., Ortega, C., De Blas, I., Noordhuizen, J., & Frankena, K. (2001). WIN EPISCOPE 2,0: improved epidemiological software for veterinary medicine. Veterinary Record, 148(18), 567–572. https://doi.org/10.1136/vr.148.18.567
Valas, S., Brémaud, I., Stourm, S., Croisé, B., Mémeteau, S., Ngwa-Mbot, D., Tabouret, M. (2019). Improvement of eradication program for infectious bovine rhinotracheitis in France inferred by serological monitoring of singleton reactors in certified BoHV1-free herds. Preventive veterinary medicine, 171, 104743. https://doi.org/10.1016/j.prevetmed.2019.104743
Valbuena-Carson, R., Valeris, R., Sánchez, E., Ramírez, A., Ochoa, K., Uzcátegui, D., Chacín, E., Simoes, D., Ramirez, R. & Angulo-Cubillán, F. (2013). Detección serológica de Neospora caninum (Aplocomplexa, Sarcocistidae) en Búfalas (Bubalus bubalis) del municipio de Colón, Estado de Zulia, Venezuela. Revista Científica de Facultad de Ciencias Veterinarias, Universidad de Zulia. 23(5), 396-402. https://www.redalyc.org/pdf/959/95928428005.pdf
Waldeck, H. F., Van Duijn, L., Van Den Heuvel-Van Den Broek, K., Mars, M., Santman-Berends, I., Biesheuvel, M. M., & Van Schaik, G. (2021). Risk factors for introduction of bovine herpesvirus 1 (BOHV-1) into cattle herds: a Systematic European Literature review. Frontiers in Veterinary Science, 8. https://doi.org/10.3389/fvets.2021.688935
Wrathall, A. E., Simmons, H. A., & Van Soom, A. (2006). Evaluation of risks of viral transmission to recipients of bovine embryos arising from fertilisation with virus-infected semen. Theriogenology, 65(2), 247–274. https://doi.org/10.1016/j.theriogenology.2005.05.043
Yuan, Y., Kitamura-Muramatsu, Y., Saito, S., Ishizaki, H., Nakano, M., Haga, S., Matoba, K., Ohno, A., Murakami, H., Takeshima, S., & Aida, Y. (2015). Detection of the BLV provirus from nasal secretion and saliva samples using BLV-CoCoMo-qPCR-2: Comparison with blood samples from the same cattle. Virus Research, 210, 248–254. https://doi.org/10.1016/j.virusres.2015,08,013
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