Advertisement

High co-infection rates of Babesia bovis, Babesia bigemina, and Anaplasma marginale in water buffalo in Western Cuba

  • Dasiel ObregónEmail author
  • Alejandro Cabezas-Cruz
  • Yasmani Armas
  • Jenevaldo B. Silva
  • Adivaldo H. Fonseca
  • Marcos R. André
  • Pastor Alfonso
  • Márcia C.S. Oliveira
  • Rosangela Z. Machado
  • Belkis Corona-González
Protozoology - Original Paper

Abstract

Water buffalo is important livestock in several countries in the Latin American and Caribbean regions. This buffalo species can be infected by tick-borne hemoparasites and remains a carrier of these pathogens which represent a risk of infection for more susceptible species like cattle. Therefore, studies on the epidemiology of tick-borne hemoparasites in buffaloes are required. In this study, the prevalence of Babesia bovis, Babesia bigemina, and Anaplasma marginale were determined in water buffalo herds of western Cuba. To this aim, a cross-sectional study covering farms with large buffalo populations in the region was performed. Eight buffalo herds were randomly selected, and blood samples were collected from 328 animals, including 63 calves (3–14 months), 75 young animals (3–5 years), and 190 adult animals (> 5 years). Species-specific nested PCR and indirect ELISA assays were used to determine the molecular and serological prevalences of each hemoparasite, respectively. The molecular and serological prevalence was greater than 50% for the three hemoparasites. Differences were found in infection prevalence among buffalo herds, suggesting that local epidemiological factors may influence infection risk. Animals of all age groups were infected, with a higher molecular prevalence of B. bigemina and A. marginale in young buffalo and calves, respectively, while a stepwise increase in seroprevalence of B. bovis and B. bigemina from calves to adult buffaloes was found. The co-infection by the three pathogens was found in 12% of animals, and when analyzed by pair, the co-infections of B. bovis and B. bigemina, B. bigemina and A. marginale, and B. bovis and A. marginale were found in 20%, 24%, and 26%, respectively, underlying the positive interaction between these pathogens infecting buffaloes. These results provide evidence that tick-borne pathogen infections can be widespread among water buffalo populations in tropical livestock ecosystems. Further studies should evaluate whether these pathogens affect the health status and productive performance of water buffalo and infection risk of these pathogens in cattle cohabiting with buffalo.

Keywords

Water buffalo Tick-borne pathogens Prevalence Co-infections nPCR iELISA 

Notes

Acknowledgments

This work was supported by funding from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq-474648/210-9), Brazil; Empresa Brasileira de Pesquisa Agropecuária (Embrapa Pecuária Sudeste); Fundacão de Amparo à Pesquisa do Estado de São Paulo (FAPESP), Brazil (Process 2012/21371-4); Coordination for the Improvement of Higher Education Personnel (Capes/MES- Projetos. Process 089110); and National Priority Program for Animal and Plant Health, Ministry of Agriculture (MINAGRI-P131LH003007), Cuba. Dasiel Obregon wishes to acknowledge the Coordination for the Improvement of Higher Education Personnel (CAPES), Brazil, for his sandwich Ph.D. grant (Capes/MES- Docentes, 2013). We are grateful to Leonhard Schnittger, PhD. for their exhaustive review, which greatly improved this paper.

Compliance with ethical standards

The procedures involving animals in this work were according to the principles established by The International Guiding Principles for Biomedical Research Involving Animals (2012). Consequently, the committee on ethics and animal welfare at CENSA approved the experimental design of this research. The Frontier Veterinary Service of the Institute of Veterinary Medicine under the Ministry of Agriculture of the Republic of Cuba authorized the export of the DNA samples used in this work, under the Zoosanitary Export Certification number R.S.1522010.

Conflicts of interest

The authors declare that they have no conflict of interest.

Supplementary material

436_2018_6194_Fig5_ESM.png (254 kb)
Supplementary Fig SF1

Limit of detection (LOD) of nPCR assays for molecular diagnosis of B. bovis (A), B. bigemina (B), and A. marginale (C). Ten-fold serial dilutions of DNA positive controls were used as template in the first round PCR, no-template reactions were used as negative controls. Lanes 1–7 correspond to the quantities of DNA 10 to 10−6 ng, respectively and M: DNA ladder. The LOD of nPCR assays of B. bovis and B. bigemina were established at 10−5 ng of DNA template, however, the LOD of the nPCR assay for A. marginale was in 10−6 ng. The size (base pair, bp) of the generated bands is indicated. (PNG 254 kb)

436_2018_6194_MOESM1_ESM.tif (1.3 mb)
High resolution image (TIF 1296 kb)

References

  1. Abbasi F, Abbasi IHR, Nissa TF, Bhutto ZA, Arain MA, Soomro RN, Siyal FA, Fazlani SA (2017) Epidemiological study of tick infestation in buffalo of various regions of district Khairpur, Pakistan. Vet World 10:688–694.  https://doi.org/10.14202/vetworld.2017.688-694 CrossRefGoogle Scholar
  2. Alonso M, Arellano-Sota C, Cereser VH et al (1992) Epidemiology of bovine anaplasmosis and babesiosis in Latin America and the Caribbean. Int J Epidemiol 11:713–733Google Scholar
  3. Aubry P, Geale DW (2011) A review of Bovine anaplasmosis. Transbound Emerg Dis 58:1–30.  https://doi.org/10.1111/j.1865-1682.2010.01173.x CrossRefGoogle Scholar
  4. Benitez D, Cetrá B, Florin-christensen M (2012) Rhipicephalus (Boophilus ) microplus ticks can complete their life cycle on the water buffalo (Bubalus bubalis). J Buffalo Sci 1:193–197.  https://doi.org/10.6000/1927-520X.2012.01.02.11 Google Scholar
  5. Benitez D, Mesplet M, Echaide I, Torioni de Echaide S, Schnittger L, Florin-Christensen M (2018) Mitigated clinical disease in water buffaloes experimentally infected with Babesia bovis. Ticks Tick Borne Dis 9:0–1.  https://doi.org/10.1016/j.ttbdis.2018.04.012 CrossRefGoogle Scholar
  6. CENCOP National Livestock Registration Center (2015) Existencia de bufalos al cierre del año. Ministry of Agriculture of the Republic of Cuba, HavanaGoogle Scholar
  7. Chauvin AC, Oreau EM, Onnet SB et al (2009) Babesia and its hosts: adaptation to long-lasting interactions as a way to achieve efficient transmission. Vet Res 40:37.  https://doi.org/10.1051/vetres/2009020 CrossRefGoogle Scholar
  8. Corona B, Muñoz ML, Hernández M, Martínez S (2004) Use of random amplified polymorphic DNA markers for the detection of genetic variation in Anaplasma marginale isolates. Rev Salud Anim 26:29–34Google Scholar
  9. Corona B, Rodríguez M, Martínez S (2005) Bovine anaplasmosis. Rev Electrónica Vet VI:1–27Google Scholar
  10. Corona B, Obregón D, Martínez S et al (2012) Detección por PCR de Anaplasma marginale en búfalos de la región occidental de Cuba. Rev Salud Anim 34:11–18Google Scholar
  11. Corrêa FN, Cunha NC, Rangel CP, Fonseca AH (2012) Ticks on buffaloes (Bubalus bubalis) in the state of Rio de Janeiro, Brazil. Brazilian J Vet Parasitol 21:313–314.  https://doi.org/10.1590/S1984-29612012000300026 CrossRefGoogle Scholar
  12. Diuk-Wasser MA, Vannier E, Krause PJ (2016) Coinfection by ixodes tick-borne pathogens: ecological, epidemiological, and clinical consequences. Trends Parasitol 32:30–42.  https://doi.org/10.1016/j.pt.2015.09.008 CrossRefGoogle Scholar
  13. FAO (2014) La alimentación y la agricultura en América Latina y el Caribe. In: Anuario Estadístico de la FAO. FAO, Santigo de Chile, pp 1689–1699Google Scholar
  14. Ferreri L, Benitez D, Dominguez M, Rodriguez A, Asenzo G, Mesplet M, Florin-Christensen M, Schnittger L (2008) Water Buffalos as carriers of Babesia bovis in Argentina. Ann N Y Acad Sci 1149:149–151.  https://doi.org/10.1196/annals.1428.036 CrossRefGoogle Scholar
  15. García Y, Fraga L, Guzmán G et al (2012) Evaluation of dairy performance of crossbred (Buffalypso x Carabao ) buffalo cows. Cuba J Agric Sci 46:357–363Google Scholar
  16. Gondard M, Cabezas-Cruz A, Charles RA, Vayssier-Taussat M, Albina E, Moutailler S (2017) Ticks and tick-borne pathogens of the Caribbean: current understanding and future directions for more comprehensive surveillance. Front Cell Infect Microbiol 7:490.  https://doi.org/10.3389/fcimb.2017.00490 CrossRefGoogle Scholar
  17. Graham AL (2008) Ecological rules governing helminth microparasite coinfection. Proc Natl Acad Sci 105:566–570.  https://doi.org/10.1073/pnas.0707221105 CrossRefGoogle Scholar
  18. Guerrero FD, Bendele KG, Davey RB, George JE (2007) Detection of Babesia bigemina infection in strains of Rhipicephalus (Boophilus) microplus collected from outbreaks in south Texas. Vet Parasitol 145:156–163.  https://doi.org/10.1016/j.vetpar.2006.11.014 CrossRefGoogle Scholar
  19. Guglielmone AA (1995) Epidemiology of babesiosis and anaplasmosis in South and Central America. Vet Parasitol 57:109–119CrossRefGoogle Scholar
  20. He L, Feng HH, Zhang WJ, Zhang QL, Fang R, Wang LX, Tu P, Zhou YQ, Zhao JL, Oosthuizen MC (2011) Occurrence of Theileria and Babesia species in water buffalo (Bubalus babalis, Linnaeus, 1758) in the Hubei province, South China. Vet Parasitol 186:490–496.  https://doi.org/10.1016/j.vetpar.2011.11.021 CrossRefGoogle Scholar
  21. Hindahl MS, Iglewski BH (1986) Outer membrane proteins from Legionella pneumophila serogroups and other Legionella species. Infect Immun 51:94–101Google Scholar
  22. Hofmann-Lehmann R, Meli ML, Dreher UM, et al (2004) Concurrent infections with vector-borne pathogens associated with fatal hemolytic anemia in a cattle herd in Switzerland. J Clin Microbiol 42:3775–3780.  https://doi.org/10.1128/JCM.42.8.3775-3780.2004
  23. Ibrahim HM, Adjou Moumouni PF, Mohammed-Geba K, Sheir SK, Hashem ISY, Cao S, Terkawi MA, Kamyingkird K, Nishikawa Y, Suzuki H, Xuan X (2013) Molecular and serological prevalence of Babesia bigemina and Babesia bovis in cattle and water buffalos under small-scale dairy farming in Beheira and Faiyum Provinces, Egypt. Vet Parasitol 198:187–192CrossRefGoogle Scholar
  24. Jirapattharasate C, Adjou Moumouni PF, Cao S, Iguchi A, Liu M, Wang G, Zhou M, Vudriko P, Efstratiou A, Changbunjong T, Sungpradit S, Ratanakorn P, Moonarmart W, Sedwisai P, Weluwanarak T, Wongsawang W, Suzuki H, Xuan X (2017) Molecular detection and genetic diversity of bovine Babesia spp., Theileria orientalis, and Anaplasma marginale in beef cattle in Thailand. Parasitol Res 116:751–762.  https://doi.org/10.1007/s00436-016-5345-2 CrossRefGoogle Scholar
  25. Jonsson NN, Bock RE, Jorgensen WK, Morton JM, Stear MJ (2012) Is endemic stability of tick-borne disease in cattle a useful concept? Trends Parasitol 28:85–89.  https://doi.org/10.1016/j.pt.2011.12.002 CrossRefGoogle Scholar
  26. Kocan KM, de la Fuente J, Blouin EF, Coetzee JF, Ewing SA (2010) The natural history of Anaplasma marginale. Vet Parasitol 167:95–107.  https://doi.org/10.1016/j.vetpar.2009.09.012 CrossRefGoogle Scholar
  27. Li Y, Luo Y, Cao S, Terkawi MA, Lan DT, Long PT, Yu L, Zhou M, Gong H, Zhang H, Zhou J, Yokoyama N, Suzuki H, Xuan X (2014) Molecular and seroepidemiological survey of Babesia bovis and Babesia bigemina infections in cattle and water buffaloes in the central region of Vietnam. Trop Biomed 31:406–413.  https://doi.org/10.1207/S15328015TLM1301 Google Scholar
  28. LNP (National Parasitology Laboratory) (2014) Serie histórica de la anaplasmosis y babesiosis en Cuba. Ministry of Agriculture of the Republic of Cuba, HavanaGoogle Scholar
  29. Machado RZ, McElwain TF, Suarez CE et al (1993) Babesia bigemina: isolation and characterization of merozoite rhoptries. Exp Parasitol 77:315–325.  https://doi.org/10.1006/expr.1993.1089 CrossRefGoogle Scholar
  30. Machado RZ, Valadão CA, Melo WR, Alessi AC (1994) Isolation of Babesia bigemina and Babesia bovis merozoites by ammonium chloride lysis of infected erythrocytes. Braz J Med Biol Res 27:2591–2598Google Scholar
  31. Machado RZ, Montassier HJ, Pinto AA et al (1997) An enzyme-linked immunosorbent assay ( ELISA ) for the detection of antibodies against Babesia bovis in cattle. Vet Microbiol 71:17–26Google Scholar
  32. Mahmmod Y (2014) Natural Babesia bovis infection in water buffaloes (Bubalus bubalis) and crossbred cattle under field conditions in Egypt : a preliminary study. J Arthropod-Borne Dis 8:1–9Google Scholar
  33. Mahmoud MS, Kandil OM, Nasr SM, Hendawy S, Habeeb S, Mabrouk D, Silva M, Suarez C (2015) Serological and molecular diagnostic surveys combined with examining hematological profiles suggests increased levels of infection and hematological response of cattle to babesiosis infections compared to native buffaloes in Egypt. Parasit Vectors 8:1–15.  https://doi.org/10.1186/s13071-015-0928-9 CrossRefGoogle Scholar
  34. Marcelino I, de Almeida AM, Ventosa M, Pruneau L, Meyer DF, Martinez D, Lefrançois T, Vachiéry N, Coelho AV (2012) Tick-borne diseases in cattle: applications of proteomics to develop new generation vaccines. J Proteome 75:4232–4250.  https://doi.org/10.1016/j.jprot.2012.03.026 CrossRefGoogle Scholar
  35. Mitat AOB (2009) Búfalos de agua en Cuba: origen y evolución. Rev ACPA 3:45–48Google Scholar
  36. Nari A (1995) Strategies for the control of one-host ticks and relationship with tick-borne diseases in South America. Vet Parasitol 57:153–165.  https://doi.org/10.1016/0304-4017(94)03117-F CrossRefGoogle Scholar
  37. Néo TA, Giglioti R, Obregón D, Bilhassi TB, Oliveira HN, Machado RZ, Aníbal FF, Brito LG, Malagó Jr W, Bressani FA, Oliveira MCS (2016) Detection of Babesia bovis and B. bigemina in Water buffaloes (Bubalus bubalis) in endemic areas of São Paulo State, Brazil. Open J Vet Med 6:75–84.  https://doi.org/10.4236/ojvm.2016.65009 CrossRefGoogle Scholar
  38. Nithikathkul C, Polseela P, Changsap B, Leemingsawat S (2002) Ixodid ticks on domestic animals in Samut Prakan Province, Thailand. Southeast Asian J Trop Med Public Health 33:41–44Google Scholar
  39. Obregón D, Rodríguez JD, Roque E, Alemán Y (2010) Rhipicephalus (Boophilus) microplus (acari: ixodidae) en búfalos (Bubalus bubalis), en Cuba. Rev Salud Anim 32:132–134Google Scholar
  40. Obregón D, Rabelo MD, Giglioti R et al (2016) Standardization of a SYBR green based real-time PCR system for detection and molecular quantification of Babesia bovis and B. bigemina in water buffaloes (Bubalus bubalis). J Buffalo Sci 5:44–52.  https://doi.org/10.6000/1927-520x.2016.05.02.4 CrossRefGoogle Scholar
  41. Obregón D, Corona BG, Cabezas-cruz A et al (2018) Molecular evidence of the reservoir competence of water buffalo (Bubalus bubalis) for Anaplasma marginale in Cuba. Vet Parasitol Reg Stud Reports 13:180–187.  https://doi.org/10.1016/j.vprsr.2018.06.007 CrossRefGoogle Scholar
  42. Ochirkhuu N, Konnai S, Mingala CN, Okagawa T, Villanueva M, R. Pilapil FMI, Murata S, Ohashi K (2015) Molecular epidemiological survey and genetic analysis of vector-borne infections of cattle in Luzon Island, the Philippines. Vet Parasitol 212:161–167.  https://doi.org/10.1016/j.vetpar.2015.05.019 CrossRefGoogle Scholar
  43. Rehman A, Nijhof AM, Sauter-Louis C, Schauer B, Staubach C, Conraths FJ (2017) Distribution of ticks infesting ruminants and risk factors associated with high tick prevalence in livestock farms in the semi-arid and arid agro-ecological zones of Pakistan. Parasit Vectors 10:1–15.  https://doi.org/10.1186/s13071-017-2138-0 CrossRefGoogle Scholar
  44. Romero-Salas D, Mira A, Mosqueda J, García-Vázquez Z, Hidalgo-Ruiz M, Vela NAO, de León AAP, Florin-Christensen M, Schnittger L (2016) Molecular and serological detection of Babesia bovis- and Babesia bigemina-infection in bovines and water buffaloes raised jointly in an endemic field. Vet Parasitol 217:101–107.  https://doi.org/10.1016/j.vetpar.2015.12.030 CrossRefGoogle Scholar
  45. Silva JB, André MR, da Fonseca AH et al (2013) Molecular and serological prevalence of Babesia bovis and Babesia bigemina in water buffaloes in the north region of Brazil. Vet Parasitol 197:678–681.  https://doi.org/10.1016/j.vetpar.2013.05.020 CrossRefGoogle Scholar
  46. Silva JB, Cabezas-Cruz A, Fonseca AH, Barbosa JD, de la Fuente J (2014a) Infection of water buffalo in Rio de Janeiro Brazil with Anaplasma marginale strains also reported in cattle. Vet Parasitol 205:730–734.  https://doi.org/10.1016/j.vetpar.2014.09.009 CrossRefGoogle Scholar
  47. Silva JB, Dos Santos PN, Santana-Castro GN et al (2014b) Prevalence Survey of selected bovine pathogens in water buffaloes in the North Region of Brazil. J Parasitol Res 2014(603484):4Google Scholar
  48. Silva JB, Marcelo W, Vinhote S et al (2014c) Molecular and serological prevalence of Anaplasma marginale in water buffaloes in northern Brazil. Ticks Tick Borne Dis 5:100–104.  https://doi.org/10.1016/j.ttbdis.2013.09.007 CrossRefGoogle Scholar
  49. Silveira JAG, de Oliveira CHS, Silvestre BT, Albernaz TT, Leite RC, Barbosa JD, Oliveira CMC, Ribeiro MFB (2016) Molecular assays reveal the presence of Theileria spp. and Babesia spp. in Asian water buffaloes (Bubalus bubalis, Linnaeus, 1758) in the Amazon region of Brazil. Ticks Tick Borne Dis 7:1017–1023.  https://doi.org/10.1016/j.ttbdis.2016.05.009 CrossRefGoogle Scholar
  50. Sivakumar T, Tattiyapong M, Fukushi S, Hayashida K, Kothalawala H, Silva SSP, Vimalakumar SC, Kanagaratnam R, Meewewa AS, Suthaharan K, Puvirajan T, de Silva WK, Igarashi I, Yokoyama N (2014) Genetic characterization of Babesia and Theileria parasites in water buffaloes in Sri Lanka. Vet Parasitol 200:24–30.  https://doi.org/10.1016/j.vetpar.2013.11.029 CrossRefGoogle Scholar
  51. Suarez CE, Noh S (2011) Emerging perspectives in the research of bovine babesiosis and anaplasmosis. Vet Parasitol 180:109–125.  https://doi.org/10.1016/j.vetpar.2011.05.032 CrossRefGoogle Scholar
  52. Terkawi MA, Huyen NX, Shinuo C, Inpankaew T, Maklon K, Aboulaila M, Ueno A, Goo YK, Yokoyama N, Jittapalapong S, Xuan X, Igarashi I (2011) Molecular and serological prevalence of Babesia bovis and Babesia bigemina in water buffaloes in the northeast region of Thailand. Vet Parasitol 178:201–207.  https://doi.org/10.1016/j.vetpar.2011.01.041 CrossRefGoogle Scholar
  53. Thrusfield M (2006) Types of sampling. In: Thrusfield M (ed) Veterinary epidemiology, 3rd edn. Blackwell Science Ltd, Oxford, pp 230–246Google Scholar
  54. Torioni de Echaide S, Knowles DP, Guire TCMC et al (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 36:777–782Google Scholar
  55. Trindade HI, Silva GRA, Teixeira MC et al (2010) Detection of antibodies against Babesia bovis and Babesia bigemina in calves from the region of Araguaína, State of Tocantins, Brazil. Rev Bras Parasitol Vet 19:169–173.  https://doi.org/10.1590/S1984-29612010000300008 CrossRefGoogle Scholar
  56. Valle MR, Mèndez L, Valdez M et al (2004) Integrated control of Boophilus microplus ticks in Cuba based on vaccination with the anti-tick vaccine Gavac™. Exp Appl Acarol 34:375–382.  https://doi.org/10.1007/s10493-004-1389-6 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Dasiel Obregón
    • 1
    • 2
    Email author
  • Alejandro Cabezas-Cruz
    • 3
  • Yasmani Armas
    • 1
  • Jenevaldo B. Silva
    • 4
  • Adivaldo H. Fonseca
    • 4
  • Marcos R. André
    • 5
  • Pastor Alfonso
    • 2
  • Márcia C.S. Oliveira
    • 6
  • Rosangela Z. Machado
    • 5
  • Belkis Corona-González
    • 2
  1. 1.Universidad Agraria de La HabanaSan José de Las LajasCuba
  2. 2.Centro Nacional de Sanidad AgropecuariaSan José de Las LajasCuba
  3. 3.UMR BIPAR, INRA, ANSES, Ecole Nationale Vétérinaire d’AlfortUniversité Paris-EstMaisons-AlfortFrance
  4. 4.Universidade Federal Rural do Rio de JaneiroSeropédica - RJBrazil
  5. 5.Universidade Estadual Paulista-Campus de JaboticabalJaboticabalBrazil
  6. 6.Embrapa Pecuária SudesteSão CarlosBrazil

Personalised recommendations