Skip to main content
Log in

Correlation between Rhipicephalus microplus ticks and Anaplasma marginale infection in various cattle breeds in Brazil

  • Published:
Experimental and Applied Acarology Aims and scope Submit manuscript

Abstract

The tick Rhipicephalus microplus is responsible for the transmission of Anaplasma marginale, which causes hemolytic anemia, abortion, decreased production, and mortality in cattle in Brazil. However, A. marginale can also persist in cattle herds without any clinical signs. This study investigated the relationship between the number of ticks present on each cattle and the circulating number of A. marginale msp1β gene copies in the blood of Brangus and Nellore cattle reared in the Brazilian Cerrado through a year period. Twenty-three animals (11 Brangus and 12 Nellore) were raised for 12 months with ticks counted every 18 days, and blood collected every 36 days. Blood sera was used for total antigen iELISA, genomic DNA was extracted from whole blood by the phenol/chloroform method and then analyzed by PCR to confirm A. marginale presence with the msp5 gene. Positive samples were quantified by qPCR using msp1β gene. Brangus cattle presented 4.5 fold more ticks than Nellore group. Although Brangus cattle carried a higher overall A. marginale msp1β gene presence than Nellore cattle, no relationship of tick count and copy number could be achieved due to high variability in copy number. Moreover, both breeds showed similar weight gain and a similar serological pattern throughout the year. None of the animals showed any clinical signs of anaplasmosis during the experimental period, indicating that a low level of tick infestation may be sufficient to maintain a stable enzootic situation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Andrade GM, Machado RZ, Vidotto MC, Vidotto O (2004) Immunization of bovines using a DNA vaccine (pcDNA3.1/MSP1b) prepared from the Jaboticabal strain of Anaplasma marginale. Ann N Y Acad Sci 1026:257–266. https://doi.org/10.1196/annals.1307.040

    Article  CAS  PubMed  Google Scholar 

  • Aguirre DH, Gaido AB, Vinabal AE, De Echaide ST, Guglielmone AA (1994) Transmission of Anaplasma marginale with adult Boophilus microplus ticks fed as nymphs on calves with different levels of rickettsaemia. Parasite 1(4):405–407. https://doi.org/10.1051/parasite/1994014405

    Article  CAS  PubMed  Google Scholar 

  • Almeida MBD, Tortelli FP, Riet-Correa B, Ferreira JLM, Soares MP, Farias NAR et al (2006) Tristeza parasitária bovina na região sul do Rio Grande do Sul: estudo retrospectivo de 1978–2005. Pesquisa Vet Bras 26:237–242. https://doi.org/10.1590/S0100-736X2006000400008

    Article  Google Scholar 

  • Andreotti R, Barros J, Valerio GM, Rodrigues SV, Higa L, Duarte OP et al (2018) Cattle tick infestation in Brangus cattle raised with Nellore in central Brazil. Semina 39(3):1099–1115. https://doi.org/10.5433/1679-0359.2018v39n3p1099

    Article  Google Scholar 

  • Aubry P, Geale DW (2011) A review of bovine anaplasmosis. Transbound Emerg Dis 58(1):1–30. https://doi.org/10.1111/j.1865-1682.2010.01173.x

    Article  CAS  PubMed  Google Scholar 

  • Bianchin I, Catto BJ, Kichel NA, Torres AA, Honer MR (2007) The effect of the control of endo- and ectoparasites on weight gains in crossbred cattle (Bos taurus taurus × Bos taurus indicus) in the central region of Brazil. Trop Anim Health Prod 39(4):287–296. https://doi.org/10.1007/s11250-007-9017-1

    Article  CAS  PubMed  Google Scholar 

  • Bonatte-Junior P, Rodrigues VS, Garcia MV, Higa LOS, Zimmermann NP, Barros JC et al (2019) Economic performance evaluation of Brangus and Nellore cattle breed naturally infested with Rhipicephalus microplus in an extensive production system in Central–West Brazil. Exp Appl Acarol 78:565. https://doi.org/10.1007/s10493-019-00404-1

    Article  Google Scholar 

  • Broom D (2003) Transport stress in cattle and sheep with details of physiological, ethological and other indicators. Dtsch Tierarztl Wochenschr 110(3):83–89

    CAS  PubMed  Google Scholar 

  • Carelli G, Decaro N, Lorusso A, Elia G, Lorusso E, Mari V et al (2007) Detection and quantification of Anaplasma marginale DNA in blood samples of cattle by real-time PCR. Vet Microbiol 124(1–2):107–114. https://doi.org/10.1016/j.vetmic.2007.03.022

    Article  CAS  PubMed  Google Scholar 

  • Carroll JA, Forsberg NE (2007) Influence of stress and nutrition on cattle immunity. Veterinary clinics of North America. Food Anim Pract 23(1):105–149. https://doi.org/10.1016/j.cvfa.2007.01.003

    Article  Google Scholar 

  • Costa SCL, de Magalhães VCS, de Oliveira UV, Carvalho FS, de Almeida CP, Machado RZ et al (2016) Transplacental transmission of bovine tick-borne pathogens: Frequency, co-infections and fatal neonatal anaplasmosis in a region of enzootic stability in the northeast of Brazil. Ticks Tick Borne Dis 7(2):270–275. https://doi.org/10.1016/j.ttbdis.2015.11.001

    Article  PubMed  Google Scholar 

  • Costa VMM, Ribeiro MFB, Duarte GAFP, Soares JF, Azevedo SS, Barros ATM et al (2018) Incidência de Anaplasma marginale, Babesia bigemina e Babesia bovis em bezerros no semiárido paraibano. Pesquisa Vet Bras 38:605–612. https://doi.org/10.1590/1678-5150-pvb-4786

    Article  Google Scholar 

  • De la Fuente J, Bussche VDRA, Garcia-Garcia JC, Rodriguez SD, Garcia MA, Guglielmone AA et al (2002) Phylogeography of new world isolates of Anaplasma marginale based on major surface protein sequences. Vet Microbiol 88:275–285. https://doi.org/10.1016/s0378-1135(02)00122-0

    Article  PubMed  Google Scholar 

  • Di Pietro F, Ortenzi F, Tilio M, Concetti F, Napolioni V (2011) Genomic DNA extraction from whole blood stored from 15- to 30-years at – 20 °C by rapid phenol–chloroform protocol: a useful tool for genetic epidemiology studies. Mol Cell Probes 25(1):44–48. https://doi.org/10.1016/j.mcp.2010.10.003

    Article  CAS  PubMed  Google Scholar 

  • Drummond RO, Ernst SE, Trevino JL, Gladney WJ, Graham OH (1973) Boophilus annulatus and Boophilus microplus: laboratory tests of insecticides. J Econ Entomol 66(1):130–133. https://doi.org/10.1093/jee/66.1.130

    Article  CAS  PubMed  Google Scholar 

  • Dumler JS, Barbet AF, Bekker CP, Dasch GA, Palmer GH, Ray SC et al (2001) Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions of six new species combinations and designation of Ehrlichia equi and ‘HGE agent’ as subjective synonyms of Ehrlichia phagocytophila. Int J Syst Evol Microbiol 51(6):2145–2165. https://doi.org/10.1099/00207713-51-6-2145

    Article  CAS  PubMed  Google Scholar 

  • Echaide AT, Knowles DP, Mcguire TC, Palmer GH, Suarez CE, Mcelwain TF (1998) 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(6):777–782

    Article  Google Scholar 

  • Eriks IS, Stiller D, Palmer GH (1993) Impact of persistent Anaplasma marginale rickettsemia on tick infection and transmission. J Clin Microbiol 31(8):2091–2096

    Article  CAS  Google Scholar 

  • Estrada-Peña A, Acedo CS, Quílez J, Del Cacho E (2005) A retrospective study of climatic suitability for the tick Rhipicephalus (Boophilus) microplus in the Americas. Glob Ecol Biogeogr 14(6):565–573. https://doi.org/10.1111/j.1466-822X.2005.00185.x

    Article  Google Scholar 

  • Flumignan DL, Fietz CR, Comunello E (2015) O clima na região do Bolsão de Mato Grosso do Sul. Dourados: EMBRAPA Agropecuária do Oeste. Documentos EMBRAPA Agropecuária do Oeste, Dourados, p 42

    Google Scholar 

  • Frisch JE (1999) Towards a permanent solution for controlling cattle ticks. Int J Parasitol 29:57–71. https://doi.org/10.1016/S0020-7519(98)00177-5

    Article  CAS  PubMed  Google Scholar 

  • Futse JE, Ueti MW, Knowles DP, Palmer GH (2003) Transmission of Anaplasma marginale by Boophilus microplus: retention of vector competence in the absence of vector-pathogen interaction. J Clin Microbiol 41(8):3829–3834

    Article  Google Scholar 

  • Giglioti R, Oliveira HN, Santana CH, Ibelli AMG, Neo TA, Bilhassi TB et al (2016) Babesia bovis and Babesia bigemina infection levels estimated by qPCR in Angus cattle from an endemic area of Sao Paulo state, Brazil. Ticks Tick Borne Dis 7(5):657–662. https://doi.org/10.1016/j.ttbdis.2016.02.011

    Article  CAS  PubMed  Google Scholar 

  • Giglioti R, Oliveira HN, Ibelli AMG, Bilhassi TB, Neo TA, Santana CH et al (2017) Neither quantification by qPCR nor quantitative Elisa can be used to discriminate Angus cattle for resistance/susceptibility to Babesia bovis. Ticks Tick Borne Dis 8(3):335–340. https://doi.org/10.1016/j.ttbdis.2016.11.008

    Article  PubMed  Google Scholar 

  • Giglioti R, De Oliveira HN, Bilhassi TB, Portilho AI, Okino CH, Marcondes CR et al (2018) Estimates of repeatability and correlations of hemoparasites infection levels for cattle reared in endemic areas for Rhipicephalus microplus. Vet Parasitol 250:78–84. https://doi.org/10.1016/j.vetpar.2017.12.010

    Article  PubMed  Google Scholar 

  • Gomes A, Honer HR, Schenk MAH, Curvo JBE (1988) Populations of cattle tick (Boophilus microplus) on purebred Nellore, Ibage and Nellore × European crossbreds in the Brazilian savannah. Trop Animal Health Prod 21(1):20–24

    Article  Google Scholar 

  • Graça T, Paradiso L, Broschat SL, Noh SM, Palmera GH (2015) Primary structural variation in Anaplasma marginale Msp2 efficiently generates immune escape variants. Infect Immun 83(11):4178–4184. https://doi.org/10.1128/IAI.00851-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grisi L, Leite RC, Martins JR, Barros AT, Andreotti R, Cancado PH, Leon AA et al (2014) Reassessment of the potential economic impact of cattle parasites in Brazil. Rev Bras Parasitol Vet 23(2):150–156. https://doi.org/10.1590/S1984-29612014042

    Article  PubMed  Google Scholar 

  • Higa LOS, Garcia MV, Rodrigues VS, Bonatte-Junior P, Piña FTB, Barros JC, Andreotti R (2019) Effects of cypermethrin, chlorpyrifos and piperonyl butoxide-based pour-on and spray acaricides on controlling the tick Rhipicephalus microplus. Syst App Acarol 24(2):278–286. https://doi.org/10.11158/saa.24.2.10

    Article  Google Scholar 

  • Hornok S, Földvári G, Elek V, Naranjo V, Farkas R, de la Fuente J (2008) Molecular identification of Anaplasma marginale and rickettsial endosymbionts in blood-sucking flies (Diptera: Tabanidae, Muscidae) and hard ticks (Acari: Ixodidae). Vet Parasitol 154(3–4):354–359. https://doi.org/10.1016/j.vetpar.2008.03.019

    Article  CAS  PubMed  Google Scholar 

  • Hulbert LE, Cobb CJ, Carroll JA, Ballou MA (2011) The effects of early weaning on innate immune responses of Holstein calves. J Dairy Sci 94(5):2545–2456. https://doi.org/10.3168/jds.2010-3983

    Article  CAS  PubMed  Google Scholar 

  • IBGE (2017) Pesquisa Agrícola Municipal. Rio de Janeiro: IBGE. Sistema IBGE de Recuperação Automática sidra. Banco de Dados Agregados. http://www.sidra.ibge.gov.br/bda/acervo9.asp. Accessed 05 May 2019

  • Kazimírová M, Štibrániová I (2013) Tick salivary compounds: their role in modulation of host defences and pathogen transmission. Front Cell Infect Microbiol 3:43. https://doi.org/10.3389/fcimb.2013.00043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ke GM, Cheng HL, Ke LY, Ji WT, Chulu JL, Liao MH et al (2006) Development of a quantitative Light cycler real-time RT-PCR for detection of avian reovirus. J Virol Methods 133(1):6–13. https://doi.org/10.1016/j.jviromet.2005.09.011

    Article  CAS  PubMed  Google Scholar 

  • Kessler RH (2001) Considerações sobre a transmissão de Anaplasma marginale. Pesquisa Vet Bras 21(4):177–179

    Article  Google Scholar 

  • Kocan KM, Stiller D, Goff WL, Claypool PL, Edwards W, Ewing SA et al (1992) Development of Anaplasma marginale in male Dermacentor andersoni transferred from parasitemic to susceptible cattle. Am J Vet Res 53(4):499–507

    CAS  PubMed  Google Scholar 

  • Kocan KM, de la Fuente J, Guglielmone AA, Meléndez RD (2003) Antigens and alternatives for control of Anaplasma marginale infection in cattle. Clin Microb Rev 16(4):698–712. https://doi.org/10.1128/CMR.16.4.698-712.2003

    Article  Google Scholar 

  • Kocan KM, de la Fuente J, Blouin EF, Garcia-Garcia JC (2004) Anaplasma marginale (Rickettsiales: Anaplasmataceae): recent advances in defining host-pathogen adaptations of a tick-borne rickettsia. Parasitology 129:S285–S300

    Article  Google Scholar 

  • Korotkov Y, Kozlova T, Kozlovskaya L (2015) Observations on changes in abundance of questing Ixodes ricinus, castor bean tick, over a 35-year period in the eastern part of its range (Russia, Tula region). Med Vet Entomol 29(2):129–136. https://doi.org/10.1111/mve.12101

    Article  PubMed  Google Scholar 

  • Machado RZ, Montassier HJ, Pinto AA, Lemos EG, Machado MR, Valadao IF et al (1997) An enzyme-linked immunosorbent assay (ELISA) for the detection of antibodies against Babesia bovis in cattle. Vet Parasitol 71(1):17–26

    Article  CAS  Google Scholar 

  • Madruga CR, Aycardi EI, Put N (1983) Epidemiologia da anaplasmose e babesiose em bovinos da região do cerrado do Estado de Mato Grosso do Sul. Arq Bras Med Vet Zootec 35(5):631–640

    Google Scholar 

  • Madruga CR, Kessler RH, Gomes A, Schenck MAM, Andrade DE (1985) Níveis de anticorpos e parasitemia de Anaplasma marginale em área enzoótica, nos bezerros da raça Nelore, Ibagé e cruzamentos Nelore. Pesquisa Agro Bras 20(1):135–142

    Google Scholar 

  • Madruga CR, Berne MEA, Kessler RH, Gomes RFC, Lima JG, Schenk MAM (1986) Diagnóstico da tristeza parasitária bovina no estado de Mato Grosso do Sul: inquérito de opinião. Fundação Cargill/EMBRAPA-CNPGC, Campinas, p 32

    Google Scholar 

  • Madruga CR, Honer MR, Schenk MAM, Curvo JBE (1987) Avaliação preliminar de parâmetros epidemiológicos da tristeza parasitáira bovina no Mato Grosso do Sul (Pesquisa em Andamento n. 38). Embrapa-CNPGC, Campo Grande. pp I–7. http://docsagencia.cnptia.embrapa.br/bovinodecorte/pa/pa38/pa38.pdf. Accessed 10 June 2019

  • Mahoney DF, Ross DR (1972) Epizootiological factors in the control of bovine babesiosis. Aust Vet J 48(5):292–298

    Article  CAS  Google Scholar 

  • Perner J, Kropáčková S, Kopáček P, Ribeiro JMC (2018) Sialome diversity of ticks revealed by RNAseq of single tick salivary glands. PLoS Negl Trop Dis 12(4):1–17. https://doi.org/10.1371/journal.pntd.0006410

    Article  CAS  Google Scholar 

  • Piper EK, Jonsson NN, Gondro C, Lew-Tabor AE, Moolhuijzen P, Vance ME et al (2009) Immunological profiles of Bos taurus and Bos indicus cattle infested with the cattle tick, Rhipicephalus (Boophilus) microplus. Clin Vaccine Immunol 16(7):1074–1786. https://doi.org/10.1128/CVI.00157-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quiroz-Castañeda RE, Amaro-Estrada I, Rodríguez-Camarillo SD (2016) Anaplasma marginale: diversity, virulence, and vaccine landscape through a genomics approach. Biomed Res Int 2016:9032085. https://doi.org/10.1155/2016/9032085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramos IAS, Herrera HM, Fernandes SJ, Amaral RB, Zanatto DCS et al (2019) Genetic diversity of Anaplasma marginale in beef cattle in the Brazilian pantanal. Ticks Tick-Borne Dis 10:805–814. https://doi.org/10.1016/j.ttbdis.2019.03.015

    Article  Google Scholar 

  • Raoult D, Roux V (1997) Rickettsioses as paradigms of new or emerging infectious diseases. Clin Microbiol Rev 10(4):694–719

    Article  CAS  Google Scholar 

  • Ratter JA, Ribeiro JF, Bridgewater S (1997) The Brazilian cerrado vegetation and threats to its biodiversity. Ann Bot 80(3):223–230. https://doi.org/10.1006/anbo.1997.0469

    Article  Google Scholar 

  • Ristic M (1977) Bovine anaplasmosis. Parasit Protozoa 4:235–249

    Google Scholar 

  • Silva JB, Gonçalves LR, Varani AM, André MR, Machado RZ (2015) Genetic diversity and molecular phylogeny of Anaplasma marginale studied longitudinally under natural transmission conditions in Rio de Janeiro, Brazil. Ticks Tick-Borne Dis 7:270–275. https://doi.org/10.1016/j.ttbdis.2015.04.002

    Article  Google Scholar 

  • Scoles GA, Broce AB, Lysyk TJ, Palmer GH (2005) Relative efficiency of biological transmission of Anaplasma marginale (Rickettsiales: Anaplasmataceae) by Dermacentor andersoni (Acari: Ixodidae) compared with mechanical transmission by Stomoxys calcitrans (Diptera: Muscidae). J Med Entomol 42:668–675

    Article  Google Scholar 

  • Smith RD, Evans DE, Martins JR, Cereser VH, Correa BL, Petraccia C et al (2000) Babesiosis (Babesia bovis) stability in unstable environments. Ann N Y Acad Sci 916:510–520

    Article  CAS  Google Scholar 

  • Snowball GJ (1956) The effect of self licking by cattle on infestation of cattle tick Boophilus microplus (Canestrini). Aust J Agric Res 7(3):227

    Article  Google Scholar 

  • Sutherst RW, Utech KBW (1981) Controlling livestock parasites with host resistance. CRC Handbook of pest management in agriculture, 2nd edn. CRC Press, Boca Raton, pp 385–407

    Google Scholar 

  • Trunkfield HR, Broom DM (1990) The welfare of calves during handling and transport. Appli Anim Behav Sci 28(1):135–152. https://doi.org/10.1016/0168-1591(90)90050-N

    Article  Google Scholar 

  • Verissimo CJ, D’Agostino SM, Pessoa FF, De Toledo LM, Santos IK (2015) Length and density of filiform tongue papillae: differences between tick-susceptible and resistant cattle may affect tick loads. Parasit Vectors 8:594. https://doi.org/10.1186/s13071-015-1196-4

    Article  PubMed  PubMed Central  Google Scholar 

  • Wharton RH, Utech KBW (1970) The relation between engorgement and dropping of Boophilus microplus (Casnestrini) (Ixodidae) to the assessment of the tick numbers on cattle. J Aust Entomol Soc 9(3):171–182

    Article  Google Scholar 

  • Zucchi RA (1990). In: Crócomo WB (ed) A taxionomia e o manejo de pragas. Manejo integrado de pragas, UNESP, São Paulo, pp 57–69

    Google Scholar 

Download references

Acknowledgements

The authors thank Agropecuária Sanyo and Ernesto Lyo Nakashima. This study was financed in part by the Brazilian Federal Agency for Support and Evaluation of Graduate Education (CAPES) - Finance Code 001”, the Brazilian National Council for Scientific and Technological Development (CNPq), and the Foundation for Support to the Development of Education, Science and Technology of Mato Grosso do Sul (Fundect, MS) – State Government of Mato Grosso do Sul.

Author information

Authors and Affiliations

Authors

Contributions

RA led the study conception and fund raising. All authors contributed to the study design. Material preparation, data collection, and analysis were performed by KRM, LSOH, PBJR, MVG, POD, BGC, and JBC. The first draft of the manuscript was written by KRM, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Renato Andreotti.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Martins, K.R., Garcia, M.V., Bonatte-Junior, P. et al. Correlation between Rhipicephalus microplus ticks and Anaplasma marginale infection in various cattle breeds in Brazil. Exp Appl Acarol 81, 585–598 (2020). https://doi.org/10.1007/s10493-020-00514-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10493-020-00514-1

Keywords

Navigation