Detection and risk factors associated with the transmissionof Anaplasma marginale in dairy buffalo herds
Detección y factores de riesgo asociados a la transmisión de Anaplasma Marginale en rebaños bufalinos lecheros
Keywords:
Anaplasma marginale, buffaloes, risk factors, PCR
Abstract
Anaplasma marginale is an intracellular rickettsia transmitted by ticks and hematophagous insects that infect the mature erythrocytes of ruminants, being considered as the hemotropic of greater economic impact in the dairy farms of the world. The findings of A. marginale in buffalo (Bubalus bubalis) have shown that it is an important reservoir of the pathogen for cattle where they coexist. In order to detect A. marginale in lactating buffaloes as well as the risk factors (RF) associated with its transmission, twelve production units located in the Eje Panamericano, Sur del Lago de Maracaibo-Venezuela were visited. Collected 120 blood samples from the jugular vein using vacuum tubes with anticoagulant ethylenediamine tetraacetic acid (EDTA). The DNA
obtained was purified according to the method of proteinase K and phenol-chloroform to identify by means of the Polymerase Chain Reaction (PCR) technique, a specific gene (msp1) for A. marginale. On the other hand, the presence of the pathogen was visualized through the blood smear under a microscope (100X) with Giemsa stain, and an epizootiological questionnaire was applied to register the epidemiological elements related to the transmission of the rickettsial microorganism. PCR revealed the presence of a specific amplicon for A. marginale of approximately 400 bp in 80% (96/120) of the total of buffaloes sampled; however, by extended blood only 30% (36/120) of the animals were diagnosed as positive. Among the FR studied, the presence of ticks (Rhipicephalus microplus) represented the highest negative impact (Odds ratio (OR) = 3.23), while the use of acaricide baths was a protection practice (OR = 0.83) for A. marginale. In conclusion, PCR proved to be a sensitive and specific diagnostic tool compared to the extended blood to find A. marginale. The high positivity among herds demand the adoption of sanitary strategies for the control of A. marginale in B. bubalis.
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References
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HOSMER, D.; LEMESHOW, S. Estimation of odds ratios in the presence of interaction. In: Applied logistic regression. 2nd Ed. Wiley Interscience, EUA. Pp. 74-79. 2000.
JACOBO, R.; CIPOLINI, M.; STORANI, C.; MARTÍNEZ,.; MARTÍNEZ, E. Infección con el complejo tristeza del bovino en búfalos. Rev. Med. Vet. 85(5): 203-204. 2004.
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KHAN, M.; ZAHOOR, A.; JAHANGIR, M.; ASHRAF, M. Prevalence of blood parasites in cattle and buffaloes. Pakistan Vet. J. 24(4):193-195. 2004.
KISPOTTA, S.; ISLAM, F.; HOQUE, F.; RAHMAN, S.; BORMAN, A.; HAQUE, A.; RAHMAN, R. Study of prevalence and associated risk factors of anaplasmosis and theileriasis in cattle. Asian J. Med. Biol. Res. 2(4): 567-576. 2016.
KOCAN, K. Targeting ticks for control of selected hemoparasitic diseases of cattle. Vet. Parasitol. 57(1-3): 121-151. 1995.
KOCAN, K.; STILLER, D.; GOFF, W.; CLAYPOOL, P.; EDWARDS, W.; EWING, S.; MCGUIRE, T.; HAIR, J.; BARRON, S. Development of Anaplasma marginale in male Dermacentor andersoni transferred from parasitemic to susceptible cattle. Amer. J. Vet. Res. 53(4): 499-507. 1992.
MEDINA-NARANJO, V.; REYNA-BELLO, A.; TAVARES- MARQUES, L.; CAMPOS, A.; RON-ROMÁN, J.; MOYANO, J.; JARRÍN-PORRAS, E.; SANDOVAL-MOREJÓN,.; CHÁVEZ-LARREA, M. Diagnóstico de los hemotrópicos Anaplasma marginale, Trypanosoma spp. y Babesia spp. mediante las técnicas de ELISAi y PCR en tres fincas ganaderas de la Provincia de Pastaza, Ecua- dor. Rev. Científ. FCV-LUZ. XXVII(3): 162-171. 2017.
MUÑOZ-GUARNIZO, T.; AYORA-FERNÁNDEZ, P.; LUZURIAGA-NEIRA, A.; CORONA-GONZÁLEZ, B.; MARTÍNEZ-MARRERO, S. Prevalencia de Anaplasma marginale en bovinos de la provincia Zamora Chinchipe, Ecuador. Rev. Salud Anim. 39(1): 68-74. 2017.
NÉO, T. Níveis de infecção de Babesia bovis, B. bigemina e Anaplasma marginale em búfalos criados no estado de São Paulo. Universidade Federal de São Carlos. São Carlos-Brasil. Tese de Grado. 93 pp. 2016.
NOGUERA, E.; ABREU, O.; AZÓCAR, R.; ACOSTA, R. Comportamiento reproductivo de un rebaño mestizo indefinido en El Guayabo, Estado Zulia. Rev. Fac. Agron. (LUZ). 10:537-547. 1993.
OBREGÓN, D.; CORONA, B.; DE LA FUENTE, J.; CA- BEZAS, A.; GONÇALVES, L.; MATOS, C.; ARMAS, Y.; HINOJOSA, Y.; ALFONSO, P.; OLIVEIRA, M.; MACHADO,,R. Molecular evidence of the reservoir competence of water buffalo (Bubalus bubalis) for Anaplasma marginale in Cuba. Vet. Parasitol. Reg. Stud. Rep. 13:180-187. 2018.
OBREGÓN, D.; RODRÍGUEZ, J.; ROQUE, E.; ALEMÁN, Y. Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) en búfalo (Bubalus bubalis), en Cuba. Rev. Salud Anim. 32(2): 132-134. 2010.
REINBOLD, J.; COETZEE, J.; HOLLIS, L.; NICKELL, J.; RIEGEL, C.; CHRISTOPHER, J.; GANTA, R. Comparison of iatrogenic transmission of Anaplasma marginale in Holstein steers via needle and needle-free injection techniques. Am. J. Vet. Res. 71(10): 1178-1188. 2010.
SAETIEW, N.; SIMKING, P.; INPANKAEW, T.; WONGPANIT, K.; KAMYINGKIRD, K.; WONGNAKPHET, S.; STICH, R.; JITTAPALAPONG, S. Prevalence and genetic diversity of Anaplasma marginale infections in water buffaloes in North-east Thailand. J. Trop. Med. Parasitol. 38(1): 9-16. 2015.
SAMBROOK, J.; RUSSELL, D. In vitro amplification of DNA by the polymerase chain reaction. In: Molecular cloning: a laboratory manual. 3rd. Ed. Cold Spring Habor Laboratory Press, New York-EUA. 2344 pp. 2001.
SHARMA, A.; SINGLA, L.; TULI, A.; KAUR, P.; BAL, M. Detection and assessment of risk factors associated with natural concurrent infection of Trypanosoma evansi and Anaplasma marginale in dairy animals by duplex PCR in eastern Punjab. Trop. Anim. Health Prod. 47(1): 252-257. 2015.
SILVA,J.;LOPEZ,C.;SOUZA,M.;GIBSON,A.;VINHOTE,W.; FONSECA, A.; ARAUJO, F.; BARBOSA-NETO, J. Detecção sorológica e molecular de Anaplasma marginale em búfalos na Ilha de Marajó, Pará. Pesq. Vet. Bras. 34(1):11-14. 2014.
SOUZA-AMORIN, L.; ARIAS, A.; SANTOS, F.; SOUZA-CARNEIRO, P.; RÊGO, G. Bovine babesiosis and anaplasmosis complex: diagnosis and evaluation of the risk factors from Bahia, Brazil. Braz. J. Vet. Parasitol. Jaboticabal. 23(3): 328-336. 2014.
STICH, R.; BANTLE, J.A.; KOCAN, K.M.; FEKETE, A. Detection of Anaplasma marginale (Rickettsiales:Anaplasmataceae) in hemolymph of Dermacentor andersoni (Acari:Ixodidae) with the Polymerase Chain Reaction. J. Med. Entomol. 30(4):781-788. 1993.
TAMASAUKAS, R.; AGUDO-CASTELLANOS, L.; SIL- VA-RAVELO, A.; FLORIO-LUIS, J.; VINTIMILLA-TAMASAUKAS, M.; RIVERA-PIRELA, S. Hemoparasitosis en ganadería doble propósito venezolana, diagnóstico y control: una revisión. Agron. Mesoamerican. 21(2): 367-381. 2010.
TORIONI, S.; KNOWLES, D.; MCGUIRE, T.; PALMER, G.; SUÁREZ, C.; MCELWAIN, T. Detection of cattle naturally infected with Anaplasma marginale in a region of endemicity by nested PCR and a competitive enzyme-linked immunosorbent assay using recombinant major surface protein 5. J . Clin. Microbiol. 36 (3):777-782. 1998.
TRAMUTA, C.; LACERENZA, D.; ZOPPI, S.; GORIA, M.; DONDO, A.; FERROGLIO, E.; NEBBIA, P.; ROSATI, S. Development of a set of multiplex standard polymerase chain reaction assays for the identification of infectious agents from aborted bovine clinical samples. J. Vet. Diag. Inv. 23(4): 657-664. 2011.
VENEZIANO, V.; SANTANIELLO, M.; CARBONE, S.; PENNACCHIO, S.; MORGOGLIONE, M.; SCHIOPPI, M.; CONDOLEO, R.; CRINGOLI, G. Lice (Haematopinus tuberculatus) in water buffalo farms from central Itlay. Ital. J. Anim. Sci. 6(Suppl. 2): 926-927. 2007.
AÑEZ-ROJAS, N.; ROMERO, O.; VALBUE- NA, H.; CRISANTE, G.; ROJAS, A.; BOLÍVAR, A.; AÑEZ, N. Detección de transmisión transplacentaria de Anaplasma marginale en bovinos asintomáticos. Rev. Científ. FCV-LUZ. XX(4):377–382. 2010.
ASHUMA, S.; SINGLA, L.; KAUR, P.; BAL, M: BATT, B.; JUYAL, P. Prevalence and haemato-biochemical prolife of Anaplasma marginale infection in dairy animals of Punjab (India). Asian Pac. J. Trop. Med. 6(2):139-144. 2013.
AUBRY, P.; GEALE, D. A review of bovine anaplas- mosis. Transbound Emerg. Dis. 58(1): 1-30. 2011.
BARBOSA DA SILVA, J.; VINHOTE, W.; OLIVEIRA, C.; ANDRÉ, M.; MACHADO, R.; DA FONSECA, A.; BARBOSA, J. Molecular and serological prevalence of Anaplasma marginale in water buffaloes in northern Brazil. Ticks Tick Borne Dis. 5(2): 100-104. 2014.
BATISTA, H.; SARTURI, C.; STELMACHTCHUK, F.; RO- CHA, D.; CAROPREZO, A.; GENNARI, S.; MARCILI, A.; NIERI, F.; SOARES, L.; HAMAD, A. Prevalence and risk factors associated with ectoparasite infestation of buffaloes in an Amazonian ecosystem. Parasit. Vectors. 11(1): 1-9. 2018.
BOLÍVAR, A.; PÉREZ, C. Confirmación microbiológica y evaluación hematológica para Anaplasma marginale y Babesia spp. en ganadería bovina de altura en los andes venezolanos. Rev. Med. Vet. 34: 45-53. 2017.
BOLÍVAR, A.; ROJAS, A.; ROSALES, D.; TORRES, Y.; GARCÍA-LUGO, P. Detección de agentes hemotrópicos en una explotación ganadera utilizando PCR y DGGE. Rev. Salud Anim. 36(1): 53-57. 2014.
CORONA, B.; MARTÍNEZ, S. Detección de Anaplasma marginale en bovinos, mediante la amplificación por PCR del gen msp5. Rev. Salud Anim. 33(1):24-31. 2011.
CORONA, B.; OBREGON, D.; MARTÍNEZ, S.; ESPINIZA, I.; HENRIQUE-FONSECA, A.; ROQUE, E. Detección por PCR de Anaplasma marginale en búfalos de la región occidental de Cuba. Rev. Salud Anim. 34(1): 11-18. 2012.
CORRÊA, F.; COSTA, N.; PASSOS, C.; HENRIQUE, A. Ticks on buffaloes (Bubalus bubalis) in the state of Rio de Janeiro, Brazil. Rev. Bras. Parasitol. Vet. Jaboticabal 21(3): 313-314. 2012.
DA SILVA, A.; LOPES, L.; STUMPFS, J.; TONIN, A.; MOURA, L.; NUNES, D. Lice outbreak in buffaloes: evidence of Anaplasma marginale transmission by sucking lice Haematopinus tuberculatus. J. Parasitol. 99(3): 546-547. 2013.
DA SILVA, M. Prevalência e fatores associados à infecção por Anaplasma marginale, Babesia bovis e Babesia bigemina em bovinos da raça crioula lageana. Universidade do Estado de Santa Catarina. Lages-Brasil. Trabalho de graduação. 130 pp. 2017.
EL-HARIRI, M.; ELHELW, R.; HAMZA, D.; SOLIMAN, D. Molecular detection of Anaplasma marginale in the egyptian water buffaloes (Bubalus bubalis) based on major surface protein 1α. J. Egypt. Soc. Parasitol. 47(2): 247-252. 2017.
ERIKS, I.; PALMER, G.; MCGUIRE, T.; BARBET, A. Detection and quantification of Anaplasma marginale in carrier by using a nucleic acid probe. J. Clin. Microb. 27(2):279-284. 1989.
FIGUEIREDO, M.; SILVA, D.; MANRIQUE, W.; GUERRA, R. Infestación y distribución de Haematopinus tuberculatus en bubalinos de São Luís, estado do Maranhão, Brasil. The Biologist. 11(1): 167-172. 2013.
FIGUEROA, V.; CHIEVES, P.; JOHNSON, S.; BUENING, M. Multiplex polymerase chain reaction based assay for the detection of Babesia bigemina, Babesia bovis and Anaplasma marginale DNA in bovine blood. Vet. Parasitol. 50(1-2):69-81. 1993.
GONZÁLEZ, J.; MELÉNDEZ, R. Seroprevalencia de la Tripanosomosis y Anaplasmosis bovina en el municipio Juan José Mora del estado Carabobo, Venezuela, mediante la técnica de ELISA. Rev. Científ. FCV-LUZ. XVII(5): 449-455. 2007.
GREEN, M.; SAMBROOK, J. Quantitation of DNA and RNA by Real-Time Polymerase Chain Reaction. In: Molecular cloning: a laboratory manual. 4th. Ed. Cold Spring Harbor Laboratory Press. Pp. 633-638. 2012.
HOSMER, D.; LEMESHOW, S. Estimation of odds ratios in the presence of interaction. In: Applied logistic regression. 2nd Ed. Wiley Interscience, EUA. Pp. 74-79. 2000.
JACOBO, R.; CIPOLINI, M.; STORANI, C.; MARTÍNEZ,.; MARTÍNEZ, E. Infección con el complejo tristeza del bovino en búfalos. Rev. Med. Vet. 85(5): 203-204. 2004.
JAIMES-DUEÑEZ, J.; TRIANA, O.; MEJÍA, A. Genetic, host and environmental factors associated with a high prevalence of Anaplasma marginale. Ticks Tick Borne Dis. 9(5): 1286-1295. 2018.
KESSLER, R. Considerações sobre a transmissão de Anaplasma marginale. Pesq. Vet. Bras. 21(4): 177-179. 2001.
KHAN, M.; ZAHOOR, A.; JAHANGIR, M.; ASHRAF, M. Prevalence of blood parasites in cattle and buffaloes. Pakistan Vet. J. 24(4):193-195. 2004.
KISPOTTA, S.; ISLAM, F.; HOQUE, F.; RAHMAN, S.; BORMAN, A.; HAQUE, A.; RAHMAN, R. Study of prevalence and associated risk factors of anaplasmosis and theileriasis in cattle. Asian J. Med. Biol. Res. 2(4): 567-576. 2016.
KOCAN, K. Targeting ticks for control of selected hemoparasitic diseases of cattle. Vet. Parasitol. 57(1-3): 121-151. 1995.
KOCAN, K.; STILLER, D.; GOFF, W.; CLAYPOOL, P.; EDWARDS, W.; EWING, S.; MCGUIRE, T.; HAIR, J.; BARRON, S. Development of Anaplasma marginale in male Dermacentor andersoni transferred from parasitemic to susceptible cattle. Amer. J. Vet. Res. 53(4): 499-507. 1992.
MEDINA-NARANJO, V.; REYNA-BELLO, A.; TAVARES- MARQUES, L.; CAMPOS, A.; RON-ROMÁN, J.; MOYANO, J.; JARRÍN-PORRAS, E.; SANDOVAL-MOREJÓN,.; CHÁVEZ-LARREA, M. Diagnóstico de los hemotrópicos Anaplasma marginale, Trypanosoma spp. y Babesia spp. mediante las técnicas de ELISAi y PCR en tres fincas ganaderas de la Provincia de Pastaza, Ecua- dor. Rev. Científ. FCV-LUZ. XXVII(3): 162-171. 2017.
MUÑOZ-GUARNIZO, T.; AYORA-FERNÁNDEZ, P.; LUZURIAGA-NEIRA, A.; CORONA-GONZÁLEZ, B.; MARTÍNEZ-MARRERO, S. Prevalencia de Anaplasma marginale en bovinos de la provincia Zamora Chinchipe, Ecuador. Rev. Salud Anim. 39(1): 68-74. 2017.
NÉO, T. Níveis de infecção de Babesia bovis, B. bigemina e Anaplasma marginale em búfalos criados no estado de São Paulo. Universidade Federal de São Carlos. São Carlos-Brasil. Tese de Grado. 93 pp. 2016.
NOGUERA, E.; ABREU, O.; AZÓCAR, R.; ACOSTA, R. Comportamiento reproductivo de un rebaño mestizo indefinido en El Guayabo, Estado Zulia. Rev. Fac. Agron. (LUZ). 10:537-547. 1993.
OBREGÓN, D.; CORONA, B.; DE LA FUENTE, J.; CA- BEZAS, A.; GONÇALVES, L.; MATOS, C.; ARMAS, Y.; HINOJOSA, Y.; ALFONSO, P.; OLIVEIRA, M.; MACHADO,,R. Molecular evidence of the reservoir competence of water buffalo (Bubalus bubalis) for Anaplasma marginale in Cuba. Vet. Parasitol. Reg. Stud. Rep. 13:180-187. 2018.
OBREGÓN, D.; RODRÍGUEZ, J.; ROQUE, E.; ALEMÁN, Y. Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) en búfalo (Bubalus bubalis), en Cuba. Rev. Salud Anim. 32(2): 132-134. 2010.
REINBOLD, J.; COETZEE, J.; HOLLIS, L.; NICKELL, J.; RIEGEL, C.; CHRISTOPHER, J.; GANTA, R. Comparison of iatrogenic transmission of Anaplasma marginale in Holstein steers via needle and needle-free injection techniques. Am. J. Vet. Res. 71(10): 1178-1188. 2010.
SAETIEW, N.; SIMKING, P.; INPANKAEW, T.; WONGPANIT, K.; KAMYINGKIRD, K.; WONGNAKPHET, S.; STICH, R.; JITTAPALAPONG, S. Prevalence and genetic diversity of Anaplasma marginale infections in water buffaloes in North-east Thailand. J. Trop. Med. Parasitol. 38(1): 9-16. 2015.
SAMBROOK, J.; RUSSELL, D. In vitro amplification of DNA by the polymerase chain reaction. In: Molecular cloning: a laboratory manual. 3rd. Ed. Cold Spring Habor Laboratory Press, New York-EUA. 2344 pp. 2001.
SHARMA, A.; SINGLA, L.; TULI, A.; KAUR, P.; BAL, M. Detection and assessment of risk factors associated with natural concurrent infection of Trypanosoma evansi and Anaplasma marginale in dairy animals by duplex PCR in eastern Punjab. Trop. Anim. Health Prod. 47(1): 252-257. 2015.
SILVA,J.;LOPEZ,C.;SOUZA,M.;GIBSON,A.;VINHOTE,W.; FONSECA, A.; ARAUJO, F.; BARBOSA-NETO, J. Detecção sorológica e molecular de Anaplasma marginale em búfalos na Ilha de Marajó, Pará. Pesq. Vet. Bras. 34(1):11-14. 2014.
SOUZA-AMORIN, L.; ARIAS, A.; SANTOS, F.; SOUZA-CARNEIRO, P.; RÊGO, G. Bovine babesiosis and anaplasmosis complex: diagnosis and evaluation of the risk factors from Bahia, Brazil. Braz. J. Vet. Parasitol. Jaboticabal. 23(3): 328-336. 2014.
STICH, R.; BANTLE, J.A.; KOCAN, K.M.; FEKETE, A. Detection of Anaplasma marginale (Rickettsiales:Anaplasmataceae) in hemolymph of Dermacentor andersoni (Acari:Ixodidae) with the Polymerase Chain Reaction. J. Med. Entomol. 30(4):781-788. 1993.
TAMASAUKAS, R.; AGUDO-CASTELLANOS, L.; SIL- VA-RAVELO, A.; FLORIO-LUIS, J.; VINTIMILLA-TAMASAUKAS, M.; RIVERA-PIRELA, S. Hemoparasitosis en ganadería doble propósito venezolana, diagnóstico y control: una revisión. Agron. Mesoamerican. 21(2): 367-381. 2010.
TORIONI, S.; KNOWLES, D.; MCGUIRE, T.; PALMER, G.; SUÁREZ, C.; MCELWAIN, T. Detection of cattle naturally infected with Anaplasma marginale in a region of endemicity by nested PCR and a competitive enzyme-linked immunosorbent assay using recombinant major surface protein 5. J . Clin. Microbiol. 36 (3):777-782. 1998.
TRAMUTA, C.; LACERENZA, D.; ZOPPI, S.; GORIA, M.; DONDO, A.; FERROGLIO, E.; NEBBIA, P.; ROSATI, S. Development of a set of multiplex standard polymerase chain reaction assays for the identification of infectious agents from aborted bovine clinical samples. J. Vet. Diag. Inv. 23(4): 657-664. 2011.
VENEZIANO, V.; SANTANIELLO, M.; CARBONE, S.; PENNACCHIO, S.; MORGOGLIONE, M.; SCHIOPPI, M.; CONDOLEO, R.; CRINGOLI, G. Lice (Haematopinus tuberculatus) in water buffalo farms from central Itlay. Ital. J. Anim. Sci. 6(Suppl. 2): 926-927. 2007.
Published
2019-08-18
How to Cite
1.
Uzcátegui-Varela JP, Briceño-Rangel A de J, Rosales MC, Márquez EE, Uzcátegui-Lara R. Detection and risk factors associated with the transmissionof Anaplasma marginale in dairy buffalo herds: Detección y factores de riesgo asociados a la transmisión de Anaplasma Marginale en rebaños bufalinos lecheros. Rev. Cient. FCV-LUZ [Internet]. 2019Aug.18 [cited 2025Jul.15];29(4):265-73. Available from: https://mail.produccioncientificaluz.org/index.php/cientifica/article/view/36549
Section
Veterinary Medicine
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