Risk Factors Associated with Hemoparasites in Dual-Purpose Cattle of Colombia
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Area
2.2. Study Population
2.3. Processing Samples and DNA Extraction
2.4. PCR Technique
2.5. Data Analysis
3. Results
3.1. Prevalence
3.2. Association Analysis
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Vokaty, S.; Desquesnes, M.; Applewhaite, L.; Favre, J.; Lieuw-A-Joe, R.; Parris-Aaron, M.; Bansse-Iisa, L. New Hemoparasite Information Network. Ann. N. Y. Acad. Sci. 1996, 791, 166–171. [Google Scholar] [CrossRef] [PubMed]
- Behar, A.; Yasur-Landau, D.; Leszkowicz-Mazuz, M. Vector-Borne Diseases in Ruminants. Lester M. Shulman 2023, 441, 1–28. [Google Scholar] [CrossRef]
- Mor, N.H.; Tavera, J.V.M.; Tobón, J.C.; Guzmán Barragán, B.L.; López, G.B.; Vargas Duarte, J.J.; Corredor, D.W.S.; Tafur-Gómez, G.A. Hemoparasitism in Grazing Cattle and Risk Factors Associated with Husbandry Management in an Endemic Area of Eastern Colombia. J. Parasit. Dis. 2024, 48, 924–935. [Google Scholar] [CrossRef]
- Ferreira, G.C.M.; Canozzi, M.E.A.; Peripolli, V.; de Paula Moura, G.; Sánchez, J.; Martins, C.E.N. Prevalence of Bovine Babesia Spp., Anaplasma Marginale, and Their Co-Infections in Latin America: Systematic Review-Meta-Analysis. Ticks Tick-Borne Dis. 2022, 13, 101967. [Google Scholar] [CrossRef]
- Corrier, D.E.; Cortes, J.; Thompson, K.; Riaño, H.; Becerra, E.; Rodriguez, R. A Field Survey of Bovine Anaplasmosis, Babesiosis and Tick Vector Prevalence in the Eastern Plains of Colombia. 1978, 10, 91–92. Trop. Anim. Health Prod. 1978, 10, 91–92. [Google Scholar] [CrossRef]
- Jaimes-Dueñez, J.; Tique-Oviedo, M.; Arias-Vega, L.; Castiblanco-Diaz, E.; Rivero-Rodriguez, L.; Marin-Cossio, L.; Gongora-Orjuela, A.; Jimenez-Leaño, A. Epidemiological Assessment of Anaplasma Marginale, Babesia Bigemina, and Babesia Bovis Infections in Colombian Creole Cattle Breeds: A Molecular Survey in Northeastern Colombia. Vet. Parasitol. Reg. Stud. Rep. 2024, 50, 101011. [Google Scholar] [CrossRef] [PubMed]
- Osorio Martínez, F.J.; Patiño Álvarez, A.; Linares Chaparro, C.; Romero González, L.A.; Ortiz Cardozo, J.; Reina Beltrán, J.F.; González, P.M. Colombia Sanidad Animal 2012; ICA: Bogotá, Colombia, 2013. [Google Scholar]
- Cerón, W.L.; Andreoli, R.V.; Kayano, M.T.; Canchala, T.; Ocampo-Marulanda, C.; Avila-Diaz, A.; Antunes, J. Trend Pattern of Heavy and Intense Rainfall Events in Colombia from 1981–2018: A Trend-EOF Approach. Atmosphere 2022, 13, 156. [Google Scholar] [CrossRef]
- Wells, E.; Betancourth, A.; Page, W. The Epidemiology of Bovine Trypanosomiasis in Colombia. Trop. Anim. Health Prod. 1970, 2, 111–125. [Google Scholar] [CrossRef]
- Patarroyo, J.; Villa, O.; Diazgranados, H. Epidemiology of Cattle Anaplasmosis in Colombia: I. Prevalence and Distribution of Agglutinating Antibodies. Trop. Anim. Health Prod. 1978, 10, 171–174. [Google Scholar] [CrossRef] [PubMed]
- Betancourt Echeverri Ph, J.A.; López Valencia MSc, G.; López Sierra MSc, G.A.; Evanoff Ph, E.A.; Berrío Cataño, W.; Gómez Oquendo, J.; Velásquez Arboleda, A.F. Eficacia de La Asociación Oxitetraciclina-Isometamidium En El Control de Anaplasmosis y Tripanosomosis Bovina. CES Med. Vet. Y Zootec. 2020, 15, 49–63. [Google Scholar] [CrossRef]
- Parra Arango, J.L.; Onofre, H.G.; Cassalett Bustillo, E.R. Diagnóstico, Manejo y Control Integrado de Ectoparásitos En Bovinos Doble Propósito Del Piedemonte Llanero; Corporación Colombiana de Investigación Agropecuaria-AGROSAVIA: Bogotá, Colombia, 2018. [Google Scholar]
- Urrea, V.; Ochoa, A.; Mesa, O. Seasonality of Rainfall in Colombia. Water Resour. Res. 2019, 55, 4149–4162. [Google Scholar] [CrossRef]
- Velandia, F.; Nuñez, A.; Marquínez, G. Memoria Explicativa: Mapa Geológico Del Departamento Del Huila. Scale 2001, 1. [Google Scholar]
- Ríos-Tobón, S.; Gutiérrez-Builes, L.A.; Ríos-Osorio, L.A. Assessing Bovine Babesiosis in Rhipicephalus (Boophilus) Microplus Ticks and 3 to 9-Month-Old Cattle in the Middle Magdalena Region, Colombia. Pesqui. Veterinária Bras. 2014, 34, 313–319. [Google Scholar] [CrossRef]
- Böse, R.; Jorgensen, W.; Dalgliesh, R.; Friedhoff, K.; De Vos, A. Current State and Future Trends in the Diagnosis of Babesiosis. Vet. Parasitol. 1995, 57, 61–74. [Google Scholar] [CrossRef] [PubMed]
- Giglioti, R.; Oliveira, H.N.; Ibelli, A.M.G.; Bilhassi, T.B.; Néo, T.A.; Santana, C.H.; Rabelo, M.D.; Machado, R.Z.; de Souza Chagas, A.C.; de Sena Oliveira, M.C. Neither Quantification by qPCR nor Quantitative Elisa Can Be Used to Discriminate Angus Cattle for Resistance/Susceptibility to Babesia Bovis. Ticks Tick-Borne Dis. 2017, 8, 335–340. [Google Scholar] [CrossRef] [PubMed]
- Alvarez, J.A.; Rojas, C.; Figueroa, J.V. Diagnostic Tools for the Identification of Babesia Sp. in Persistently Infected Cattle. Pathogens 2019, 8, 143. [Google Scholar] [CrossRef]
- Betancourt, J.A.; Cassalett, E. Fluctuaciones En El Número de Garrapatas Boophilus Microplus Adultas Parasitando Bovinos En El Valle Del Cauca; Corporación Colombiana de Investigación Agropecuaria: Bogotá, Colombia, 1995. [Google Scholar]
- Díaz Rivera, E.; Benavides Ortiz, E.V.; Parra Trujillo, M.H.; Riveros Escobar, E.; Arcos Dorado, J.C.; Jaramillo, F.; Londoño Arango, J.E. Frecuencia y Distribucion de Garrapatas En La Cuenca Del Alto Magdalena: Recomendaciones Para Su Control; Corporación Colombiana de Investigación Agropecuaria: Bogotá, Colombia, 1999. [Google Scholar]
- Brennan, M.L.; Kemp, R.; Christley, R.M. Direct and Indirect Contacts between Cattle Farms in North-West England. Prev. Vet. Med. 2008, 84, 242–260. [Google Scholar] [CrossRef] [PubMed]
- Bastos, T.S.A.; Faria, A.M.; Madrid, D.M.d.C.; Bessa, L.C.d.; Linhares, G.F.C.; Fidelis, O.L.; Sampaio, P.H.; Cruz, B.C.; Cruvinel, L.B.; Nicaretta, J.E. First Outbreak and Subsequent Cases of Trypanosoma Vivax in the State of Goiás, Brazil. Rev. Bras. Parasitol. Veterinária 2017, 26, 366–371. [Google Scholar] [CrossRef]
- Lozano, M.C.; Arias, D.C. Residuos de Fármacos En Alimentos de Origen Animal: Panorama Actual En Colombia. Rev. Colomb. Cienc. Pecu. 2008, 21, 121–135. [Google Scholar] [CrossRef]
- Benavides Ortiz, E.; Vizcaíno Gerdts, O.; Polanco Palencia, N.; Mestra Pineda, A.; Betancur Hurtado, O.J. Efecto Terapéutico de Un Fármaco Frente a Los Hemoparásitos Del Bovino Babesia Bovis, Babesia Biaemina y Anaplasma Marginale. CES Med. Vet. Zootec. 2012, 7, 33–48. [Google Scholar]
- Shahbazi, P.; Nouri Gharajalar, S.; Mohebbi, K.; Taeb, J.; Hashemzadeh Farhang, H.; Nikvand, A.A.; Norouzi, R. First Survey on the Presence and Distribution of Oxytetracycline-Resistance Genes in Anaplasma Species. Acta Parasitol. 2021, 66, 501–507. [Google Scholar] [CrossRef] [PubMed]
- Sow, A.; Sidibé, I.; Bengaly, Z.; Marcotty, T.; Séré, M.; Diallo, A.; Vitouley, H.S.; Nebié, R.; Ouédraogo, M.; Akoda, G. Field Detection of Resistance to Isometamidium Chloride and Diminazene Aceturate in Trypanosoma Vivax from the Region of the Boucle Du Mouhoun in Burkina Faso. Vet. Parasitol. 2012, 187, 105–111. [Google Scholar] [CrossRef] [PubMed]
- Tuvshintulga, B.; Sivakumar, T.; Yokoyama, N.; Igarashi, I. Development of Unstable Resistance to Diminazene Aceturate in Babesia Bovis. Int. J. Parasitol. Drugs Drug Resist. 2019, 9, 87–92. [Google Scholar] [CrossRef]
- Zambrano, J.C.; Echeverri, J. Genetic and Environmental Variance and Covariance Parameters for Some Reproductive Traits of Holstein and Jersey Cattle in Antioquia (Colombia). Rev. Bras. Zootec. 2014, 43, 132–139. [Google Scholar] [CrossRef]
- Salamanca-Carreño, A.; Tamasaukas, R.; Cesar-Giraldo-Forero, J.; Quintero, A.D.; Hernandez-Rodríguez, M.E. Interacción Entre Factores Ambientales y Raciales Sobre La Prevalencia de Hemotrópicos En Hembras Bovinas Doble Propósito En Sabanas Inundables Araucanas, Colombia. Rev. Científica 2018, 28, 52–62. [Google Scholar]
- Okafor, C.C.; Collins, S.L.; Daniel, J.A.; Harvey, B.; Coetzee, J.F.; Whitlock, B.K. Factors Associated with Seroprevalence of Bovine Anaplasmosis in Texas. Vet. Parasitol. Reg. Stud. Rep. 2018, 14, 32–40. [Google Scholar] [CrossRef] [PubMed]
- Overton, T.; Yasui, T. Practical Applications of Trace Minerals for Dairy Cattle. J. Anim. Sci. 2014, 92, 416–426. [Google Scholar] [CrossRef] [PubMed]
- Goff, J.P. Invited Review: Mineral Absorption Mechanisms, Mineral Interactions That Affect Acid–Base and Antioxidant Status, and Diet Considerations to Improve Mineral Status. J. Dairy Sci. 2018, 101, 2763–2813. [Google Scholar] [CrossRef] [PubMed]
- Ravindran, R.; Juliet, S.; Ajith Kumar, K.; Sunil, A.; Amithamol, K.; Nair, S.; Chandrasekhar, L.; Sujith, S.; Bandyapadhyay, A.; Rawat, A. Effects of Solvents and Surfactants against Haemaphysalis Bispinosa. Trop. Biomed. 2011, 28, 482–486. [Google Scholar] [PubMed]
- Nyahangare, E.T.; Mvumi, B.M.; McGaw, L.J.; Eloff, J.N. Addition of a Surfactant to Water Increases the Acaricidal Activity of Extracts of Some Plant Species Used to Control Ticks by Zimbabwean Smallholder Farmers. BMC Vet. Res. 2019, 15, 404. [Google Scholar] [CrossRef]
- Schimpf, D.J.; Ewert, M.M.; Lai, V.K.; Clarke, B.L. Responses of Ticks to Immersion in Hot Bathing Water: Effect of Surface Type, Water Temperature, and Soap on Tick Motor Control. PLoS ONE 2021, 16, e0261592. [Google Scholar] [CrossRef]
Hemoparasite | Strand | Primer Sequence 5′-3′ |
---|---|---|
Anaplasma spp. | Forward | GTGCTGGTTGTGTGGTTGTC |
Reverse | TGGCTGGGAGGACACATACT | |
Babesia spp. | Forward | AACGTGATTTCAACAATGGTGT |
Reverse | TCTTAACCCAACTCACGTACCA | |
Trypanosoma spp. | Forward | TTGTCGTTTTCAATGGGGGA |
Reverse | GTAAAAATCACGGACGCCCC |
Hemoparasite | Frequency | Prevalence | 95% Confidence Interval | |
---|---|---|---|---|
Lower Limit | Upper Limit | |||
Anaplasma spp. | 145/360 | 40.3 | 0.35 | 0.45 |
Babesia spp. | 151/360 | 41.9 | 0.37 | 0.47 |
Trypanosoma spp. | 162/360 | 45.0 | 0.40 | 0.50 |
Anaplasma spp. + Babesia spp. | 131/360 | 36.4 | 0.31 | 0.41 |
Anaplasma spp. + Trypanosoma spp. | 133/360 | 36.9 | 0.32 | 0.42 |
Babesia spp. + Trypanosoma spp. | 130/360 | 36.1 | 0.31 | 0.41 |
Anaplasma spp. + Babesia spp. + Trypanosoma spp. | 126/360 | 35.0 | 0.30 | 0.40 |
Age | Hemoparasite | Babesia spp. | Trypanosoma spp. | Anaplasma spp. | ||||
---|---|---|---|---|---|---|---|---|
+ | % | + | % | + | % | + | % | |
0 to 45 | 25 | 42.4 | 22 | 37.3 | 21 | 35.6 | 21 | 35.6 |
46 to 65 | 70 | 60.9 | 53 | 46.1 | 57 | 49.6 | 50 | 43.5 |
66 to 85 | 70 | 56.4 | 58 | 46.8 | 62 | 50.0 | 56 | 45.2 |
86 to 104 | 9 | 37.5 | 6 | 25.0 | 9 | 37.5 | 8 | 33.3 |
106 or more | 12 | 40.0 | 9 | 30.0 | 10 | 33.3 | 7 | 23.3 |
undetermined | 3 | 37.5 | 3 | 37.5 | 3 | 37.5 | 3 | 47.5 |
χ2 (5, N = 360) = 11.5, p = 0.048 | χ2 (5, N = 360) = 7.2, p = 0.208 | χ2 (5, N = 360) = 6.71, p = 0.243 | χ2 (5, N = 360) = 6.34, p = 0.274 |
Region | Hemoparasite | Babesia spp. | Trypanosoma spp. | Anaplasma spp. | ||||
---|---|---|---|---|---|---|---|---|
+ | % | + | % | + | % | + | % | |
Southern | 20 | 30.8 | 16 | 24.6 | 20 | 30.8 | 14 | 21.5 |
Central | 43 | 74.1 | 37 | 63.8 | 36 | 62.1 | 33 | 56.9 |
Northern | 96 | 54.2 | 76 | 42.9 | 78 | 44.1 | 76 | 42.9 |
Western | 30 | 50.0 | 22 | 36.7 | 28 | 46.7 | 22 | 36.7 |
χ2 (3, N = 360) = 23.6, p ≤ 0.001 | χ2 (3, N = 360) = 20.1, p ≤ 0.001 | χ2 (3, N = 360) = 6.69, p = 0.006 | χ2 (3, N = 360) = 17.0, p ≤ 0.001 |
Hemoparasites | Babesia spp. | Anaplasma spp. | Trypanosoma spp. |
---|---|---|---|
Babesia spp. | 1 | 0.805 * | 0.702 * |
Anaplasma spp. | 0.805 * | 1 | 0.77 * |
Trypanosoma spp. | 0.702 * | 0.771 * | 1 |
Factor | n | Hemoparasites | Babesia spp. | Trypanosoma spp. | Anaplasma spp. | |||||
---|---|---|---|---|---|---|---|---|---|---|
p-Value | OR | p-Value | OR | p-Value | OR | p-Value | OR | |||
Geographical area | South | 65 | - | - | - | - | - | - | - | - |
Center | 58 | <0.001 * | 6.4 | <0.001 * | 5.4 | <0.001 * | 3.7 | <0.001 * | 4.8 | |
North | 177 | 0.001 * | 2.7 | 0.01 * | 2.3 | 0.063 | 1.8 | 0.003 * | 2.7 | |
West | 60 | 0.03 * | 2.2 | 0.145 | 1.8 | 0.069 | 2.0 | 0.064 | 2.1 | |
Mineral salt supply | No | 82 | - | - | - | - | - | - | - | - |
Yes | 269 | 0.005 * | 0.478 | 0.006 * | 0.5 | <0.001 * | 0.4 | 0.005 * | 0.487 | |
Livestock weight | <350 | 39 | - | - | - | - | - | - | - | - |
351−400 | 66 | 0.397 | 1.4 | 0.668 | 1.2 | 0.183 | 1.8 | 0.83 | 0.9 | |
401−450 | 85 | 0.027 * | 2.4 | 0.07 * | 2.1 | 0.006 * | 3.1 | 0.017 * | 2.7 | |
>451 | 76 | 0.241 | 1.6 | 0.15 | 1.8 | 0.19 | 1.7 | 0.238 | 1.6 | |
Presence of cattle from other owners on the farm | No | 305 | - | - | - | - | - | - | - | - |
Yes | 55 | <0.001 * | 0.3 | 0.001 * | 0.3 | 0.002 * | 0.4 | 0.008 * | 0.4 | |
Purchase of animals for fattening | No | 286 | - | - | - | - | - | - | - | - |
Yes | 74 | 0.035 * | 1.8 | 0.019 * | 1.8 | 0.006 * | 2.1 | 0.001 * | 2.9 | |
Disinfection of clothing after contact with neighbor’s animals | No | 148 | - | - | - | - | - | - | - | - |
Yes | 210 | 0.002 * | 1.9 | <0.001 * | 2.2 | 0.002 * | 1.9 | <0.001 * | 2.5 | |
Self-medication | No | 56 | - | - | - | - | - | - | - | - |
Yes | 303 | 0.017 * | 2 | 0.001 * | 3.1 | <0.001 * | 3.2 | 0.006 * | 2.5 | |
Evidence of joint trauma | No | 315 | - | - | - | - | - | - | - | - |
Yes | 44 | 0.328 | 0.7 | 0.008 * | 0.4 | <0.001 * | 0.3 | 0.005 * | 0.23 | |
Documented milking routine | No | 264 | - | - | - | - | - | - | - | - |
Yes | 95 | 0.256 | 0.8 | 0.036 * | 0.6 | 0.924 | 1 | 0.449 | 0.8 | |
Use of clean clothing | No | 109 | - | - | - | - | - | - | - | - |
Yes | 251 | 0.01 * | 1.8 | 0.002 * | 2.2 | 0.011 * | 1.8 | 0.006 * | 2 | |
Blood sample submission | No | 261 | - | - | - | - | - | - | - | - |
Yes | 98 | 0.049 * | 0.6 | 0.001 * | 0.4 | 0.034 * | 0.6 | <0.001 * | 0.4 | |
Reproductive status | Empty | 287 | - | - | - | - | - | - | - | - |
Pregnant | 64 | 0.041 * | 1.8 | 0.505 | 1.2 | 0.024 * | 1.9 | 0.124 | 1.5 | |
Postparturient | 8 | 0.484 | 1.7 | 0.232 | 2.4 | 0.659 | 1.4 | 0.176 | 2.7 | |
Separation of cattle pens | No | 76 | - | - | - | - | - | - | - | - |
Yes | 284 | 0.076 | 1.6 | 0.818 | 1 | 0.009 * | 2.0 | 0.226 | 1.4 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Murcia-Mono, C.A.; Falla-Tapias, S.; Morales Cabrera, A.F.; Navia Álvarez, L.C.; Rivera-Sánchez, L.; Gómez Vargas, Y.; Burgos-Paz, W.O. Risk Factors Associated with Hemoparasites in Dual-Purpose Cattle of Colombia. Pathogens 2025, 14, 62. https://doi.org/10.3390/pathogens14010062
Murcia-Mono CA, Falla-Tapias S, Morales Cabrera AF, Navia Álvarez LC, Rivera-Sánchez L, Gómez Vargas Y, Burgos-Paz WO. Risk Factors Associated with Hemoparasites in Dual-Purpose Cattle of Colombia. Pathogens. 2025; 14(1):62. https://doi.org/10.3390/pathogens14010062
Chicago/Turabian StyleMurcia-Mono, César A., Sergio Falla-Tapias, Andrés F. Morales Cabrera, Laura C. Navia Álvarez, Leidy Rivera-Sánchez, Yolanda Gómez Vargas, and William O. Burgos-Paz. 2025. "Risk Factors Associated with Hemoparasites in Dual-Purpose Cattle of Colombia" Pathogens 14, no. 1: 62. https://doi.org/10.3390/pathogens14010062
APA StyleMurcia-Mono, C. A., Falla-Tapias, S., Morales Cabrera, A. F., Navia Álvarez, L. C., Rivera-Sánchez, L., Gómez Vargas, Y., & Burgos-Paz, W. O. (2025). Risk Factors Associated with Hemoparasites in Dual-Purpose Cattle of Colombia. Pathogens, 14(1), 62. https://doi.org/10.3390/pathogens14010062