Parasitology Research

, Volume 118, Issue 2, pp 617–630 | Cite as

Molecular characterization of South Indian field isolates of bovine Babesia spp. and Anaplasma spp.

  • Rangapura Kariyappa Pradeep
  • Murikoli Nimisha
  • Meethalae Koombayil Sruthi
  • Pakideery Vidya
  • Birur Mallappa Amrutha
  • Prashant Somalingappa Kurbet
  • Karapparambu Gopalan Ajith Kumar
  • Anju Varghese
  • Chundayil Kalarikkal Deepa
  • Chemmangattuvalappil Narendranath Dinesh
  • Leena Chandrasekhar
  • Sanis Juliet
  • Puthenparambil Ramakrishnan Pradeepkumar
  • Chintu Ravishankar
  • Srikant Ghosh
  • Reghu RavindranEmail author
Protozoology - Original Paper


Ticks and tick-borne diseases (TTBDs) are considered major causes of economic loss in the livestock sector which incur an annual control cost estimated at US$ 498.7 million in India. Among these diseases, babesiosis, theileriosis and anaplasmosis are listed among the top ten livestock diseases in India and cause significant mortality and morbidity among cattle. However, molecular characterization of bovine Babesia and Anaplasma species are scant; thus, the aim of this study is to perform molecular characterization of field isolates of Babesia spp. and Anaplasma spp. infecting bovines in Kerala, South India. Blood smears and whole blood samples were collected from a total of 199 apparently healthy adult female cattle in Kerala. Based on microscopy, Babesia spp., Theileria orientalis and Anaplasma spp. organisms were detected in 9 (4.5%), 40 (20%) and 6 (3%) samples, respectively. Genus-specific polymerase chain reactions for amplification of 18S rRNA of Babesia spp. and 16S rRNA of Anaplasma spp. revealed positive results with 18 (9%) and 14 (7%) samples. The phylogenetic analysis of 18S rRNA gene sequences of Babesia spp. confirmed the existence of two different populations of Babesia spp. circulating in the blood of infected cattle viz., Babesia bigemina and a Babesia sp. genetically related to Babesia ovata. Further phylogenetic analysis using rap-1a sequences of isolates of B. bigemina revealed higher levels of genetic heterogeneity. However, the field isolates of B. bigemina displayed only slight heterogeneity when the rap-1c gene was examined. Polymerase chain reaction followed by sequencing and phylogenetic analysis of 16S rRNA gene of Anaplasma spp. revealed the existence of Anaplasma marginale, Anaplasma bovis and Anaplasma platys in bovines in South India. Based on msp4 gene sequences, all the field isolates of A. marginale from Kerala were clustered in a single clade with others isolated from around the world. To our knowledge, this study forms the first report on occurrence of B. ovata-like parasites and A. platys in cattle from India.


Babesia bigemina B. ovata like Anaplasma marginale A. platys A. bovis Phylogeny South India 



We thank all the veterinary doctors and local farming community for their cooperation.

Funding information

This work was supported financially by the Indian Council of Agricultural Research (NAIP/C2066, NFBSFARA/BSA-4004/2013-14, NASF/ABA-6015/2016-17), the Kerala State Council for Science, Technology and Environment (022/YIPB/KBC/2013/CSTE, 010-14/ SARD/13/CSTE) and the Department of Animal Husbandry, Kerala [B2.3858/04/Plg(3) dt.2/2/07, B2.8401/08/Plg dt.19/18/2008].


  1. Abd-Rani PAM, Irwin PJ, Coleman GT, Gatne M, Traub RJ (2011) A survey of canine tick-borne diseases in India. Parasit Vectors 4:141–148CrossRefGoogle Scholar
  2. Aguirre E, Tesouro MA, Ruiz L, Amusategui I, Sainz A (2006) Genetic characterization of Anaplasma (Ehrlichia) platys in dogs in Spain. J Vet Med B Infect Dis Vet Public Health 53:197–200CrossRefGoogle Scholar
  3. Aktas M, Altay K, Dumanli N (2011) Molecular detection and identification of Anaplasma and Ehrlichia species in cattle from Turkey. Ticks Tick-borne Dis 2:62–65CrossRefGoogle Scholar
  4. Annual Report (2014–15) Project directorate of animal disease monitoring and surveillance, Indian Council of Agricultural Research, New DelhiGoogle Scholar
  5. Bai Q, Liu GY, Zhang L, Zhang JY (1990) Discovery and isolation of Babesia ovata in China. Chin J Vet Sci Technol 20:2–4Google Scholar
  6. Beaufils JP, Inokuma H, Martin-Granel J, Jumelle P, Barbault-Jumelle M, Brouqui P (2002) Anaplasma platys (Ehrlichia platys) infection in a dog in France: description of the case, and characterization of the agent. Rev Med Vet 153:85–90Google Scholar
  7. Brown GK, Canfield PJ, Dunstan RH, Roberts TK, Martin AR, Brown CS, Irving R (2006) Detection of Anaplasma platys and Babesia canis vogeli and their impact on platelet numbers in free-roaming dogs associated with remote aboriginal communities in Australia. Aust Vet J 84:321–325CrossRefGoogle Scholar
  8. Chang AC, Chang WL, Lin CT, Pan MJ, Lee SC (1996) Canine infectious cyclic thrombocytopenia found in Taiwan. J Vet Med Sci 58:473–476CrossRefGoogle Scholar
  9. Contreras M, Alberdi P, Mateos-Hernández L, Fernández de Mera IG, García-Pérez AL, Vancová M, Villar M, Ayllón N, Cabezas-Cruz A, Valdés JJ, Stuen S, Christian Gortazar C, de la Fuente J (2017) Anaplasma phagocytophilum MSP4 and HSP70 proteins are involved in interactions with host cells during pathogen infection. Front Cell Infect Microbiol 7:307CrossRefGoogle Scholar
  10. Dahmani M, Davoust B, Benterki MS, Fenollar F, Raoult D, Mediannikov O (2015) Development of a new PCR-based assay to detect Anaplasmataceae and the first report of Anaplasma phagocytophilum and Anaplasma platys in cattle from Algeria. Comp. Immunol Microbiol Infect Dis 39:39–45CrossRefGoogle Scholar
  11. de Castro JJ (1997) Sustainable tick and tick-borne disease control in livestock improvement in developing countries. Vet Parasitol 71:77–97CrossRefGoogle Scholar
  12. de la Fuente J, Van Den Bussche RA, Kocan KM (2001) Molecular phylogeny and biogeography of North American isolates of Anaplasma marginale (Rickettsiaceae: Ehrlichieae). Vet Parasitol 97:65–76CrossRefGoogle Scholar
  13. de la Fuente J, Bussche RAVD, Garcia-Garcia JC, Rodríguez SD, García MA, Guglielmone AA, Mangold AJ, Friche Passos LM, Blouin EF, Kocan K (2002) Phylogeography of New World isolates of Anaplasma marginale (Rickettsiaceae: Anaplasmataceae) based on major surface protein sequences. Vet Microbiol 88:275–285CrossRefGoogle Scholar
  14. de la Fuente J, Lew A, Lutz H, Meli ML, Hofmann-Lehmann R, Shkap V, Molad T, Mangold AJ, Almazán C, Naranjo V, Gortázar C, Torina A, Caracappa S, Garcıa-Perez AL, Barral M, Oporto B, Ceci L, Carelli G, Blouin EF, Kocan KM (2005a) Genetic diversity of Anaplasma species major surface proteins and implications for anaplasmosis serodiagnosis and vaccine development. Anim Health Res Rev 6:75–89CrossRefGoogle Scholar
  15. de la Fuente J, Torina A, Caracappa S, Tumeno G, Furla R, Almazan C, Kocan KM (2005b) Serologic and molecular characterization of Anaplasma species infection in farm animals and ticks from Sicily. Vet Parasitol 133:357–362CrossRefGoogle Scholar
  16. de la Fuente J, Torina A, Naranjo V, Nicosia S, Alongi A, La MF, Kocan KM (2006) Molecular characterization of Anaplasma platys strains from dogs in Sicily, Italy. BMC Vet Res 2:24CrossRefGoogle Scholar
  17. Devada K, Saseendranath MR, Abraham MJ, Tresamol PV (1996) Occurrence of Ehrlichia bovis in a cow. J Vet Anim Sci 27:66–67Google Scholar
  18. Donatien A, Lestoquard F (1936) Rickettsia bovis, novelle espece pathogene pour le boeuf. Bull Soc Pathol Exot 29:1057–1061Google Scholar
  19. Dumler JS, Barbet AF, CPJ B, Dasch A, Palmer GH, Ray SC, Rikihisa Y, Rurangirwa FR (2001) Reorganization of the 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 “HE agent” as subjective synonyms of Ehrlichia phagocytophilia. Int J Syst Evol Microbiol 51:2145–2165CrossRefGoogle Scholar
  20. Dyachenko V, Pantchev N, Balzer J, Straubinger RK (2012) First case of Anaplasma platys infection in a dog from Croatia. Parasit Vectors 5:49CrossRefGoogle Scholar
  21. Fahrimal Y, Goff WL, Jasmer DP (1992) Detection of Babesia bovis carrier cattle by using polymerase chain reaction amplification of parasite DNA. J Clin Microbiol 30:1374–1379Google Scholar
  22. Ferreira RF, Figueiredo Cerqueira AM, Pereira AM, Guimaraes CM, Sa AG, Abreu FS, Massard CL, Pereira Almosny NR (2007) Anaplasma platys diagnosis in dogs: comparison between morphological and molecular tests. Int J Appl Res Vet Med 5:113–119Google Scholar
  23. Figueroa JV, Chieves LP, Johnson GS, Buening GM (1992) Detection of Babesia bigemina infected carriers by polymerase chain reaction amplification. J Clin Microbiol 30:2576–2582Google Scholar
  24. French TW, Harvey JW (1983) Serologic diagnosis of infectious cyclic thrombocytopenia in dogs using an indirect fluorescent antibody test. Am J Vet Res 44:2407–2411Google Scholar
  25. Garg R, Banerjee PS, Yadav CL, Garg A (2004) Sub-clinical babesiosis and anaplasmosis in cross bred cattle in an organized farm. J Vet Parasitol 18:151–153Google Scholar
  26. Gautam OP, Chhabra MB (1983) Babesiosis: recent advances with special reference to India. Trop Vet Anim Sci 1:201–207Google Scholar
  27. George N, Bhandari V, Sharma P (2017) Phylogenetic relationship and genotypic variability in Anaplasma marginale strains causing anaplasmosis in India. Inf Genet Evol 48:71–75CrossRefGoogle Scholar
  28. Ghosh S, Azhahianambi P, de la Fuente P (2006) Control of ticks of ruminants, with special emphasis on livestock farming system in India: present and future possibilities for integrated control—a review. Exp Appl Acarol 40:49–66CrossRefGoogle Scholar
  29. Gopinath VR (2004) Clinical investigations on parasitic anaemia in cattle. M.V.Sc. thesis. Kerala Agriculture University, Thrissur. 84pGoogle Scholar
  30. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98Google Scholar
  31. Harish BR, Chandranaik BM, Renukaprasad C, Jayakumar SR, Krishnappa G (2006) Incidence of haemoprotozoan diseases in Karnataka. Indian J Vet Med 26:30–31Google Scholar
  32. Hilpertshauser H, Deplazes P, Meli ML, Hofmann-Lehmann R, Lutz H, Mathis A (2007) Genotyping of Babesia bigemina from cattle from a non-endemic area (Switzerland). Vet Parasitol 145:59–64CrossRefGoogle Scholar
  33. Hua P, Yuhai M, Shide T, Yang S, Bohai W, Xiangrui C (2000) Canine ehrlichiosis caused simultaneously by Ehrlichia canis and Ehrlichia platys. Microbiol Immunol 44:737–739CrossRefGoogle Scholar
  34. Indani JA (1938) Babesia bovis as cause of red water in an Indian buffalo. Indian J Vet Sci Anim Husb 9:99–101Google Scholar
  35. Inokuma H, Raoult D, Brouqui P (2000) Detection of Ehrlichia platys DNA in brown dog ticks (Rhipicephalus sanguineus) in Okinawa Island, Japan. J Clin Microbiol 38:4219–4221Google Scholar
  36. Inokuma H, Fujii K, Matsumoto K, Okuda M, Nakagome K, Kosugi R, Hirakawa M, Onishi T (2002a) Demonstration of Anaplasma (Ehrlichia) platys inclusions in peripheral blood platelets of a dog in Japan. Vet Parasitol 110:145–152CrossRefGoogle Scholar
  37. Inokuma H, Fujii K, Okuda M, Onishi T, Beaufils JP, Raoult D, Brouqui P (2002b) Determination of the nucleotide sequences of heat shock operon groESL and the citrate synthase gene (gltA) of Anaplasma (Ehrlichia) platys for phylogenetic and diagnostic studies. Clin Diagn Lab Immunol 9:1132–1136Google Scholar
  38. Kocan KM, de la Fuente J, Gulielmone AA, Melendez RD (2003) Antigens and alternatives for control of Anaplasma marginale infection in cattle. Clin Microbiol Rev 16:698–712CrossRefGoogle Scholar
  39. Kolte SW, Larcombe SD, Jadhao SG, Magar SP, Warthi G, Kurkure NV, Glass EJ, Shiels BR (2017) PCR diagnosis of tick-borne pathogens in Maharashtra state, India indicates fitness cost associated with carrier infections is greater for crossbreed than native cattle breeds. PLoS ONE 12.
  40. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  41. Lack JB, Reichard MV, Van Den Bussche RA (2012) Phylogeny and evolution of the Piroplasmida as inferred from 18S rRNA sequences. Int J Parasitol 42:353–363CrossRefGoogle Scholar
  42. Minami T, Ishihara T (1980) Babesia ovata sp.n. isolated from cattle in Japan. Natl Inst Anim Health Q (Tokyo) 20:101–113Google Scholar
  43. Minjauw B, McLeod A (2003) Tick-borne diseases and poverty: the impact of ticks and tick-borne diseases on the livelihoods of small-scale and marginal livestock owners in India and eastern and southern Africa. DFID Animal Health Programme, Centre for Tropical Veterinary Medicine, UK, p.124Google Scholar
  44. Molad T, Erster L, Fleiderovitz L, Roth A, Leibovitz B, Wolkomirsky R, Mazuz ML (2015) Molecular characterization of the Israeli Babesia bigemina vaccine strain and field isolates. Vet Parasitol 7675:1–9Google Scholar
  45. Mosqueda J, McElwain TF, Stiller D, Palmer GH (2002) Babesia bovis merozoite surface antigen 1 and rhoptry-associated protein 1 are expressed in sporozoites, and specific antibodies inhibit sporozoite attachment to erythrocytes. Infect Immun 70:1599–1603CrossRefGoogle Scholar
  46. Munderloh UG, Tate CM, Lynch MJ, Howerth EW, Kurtti TJ, Davidson WR (2003) Isolation of an Anaplasma sp. organism from white-tailed deer by tick cell culture. J Clin Microbiol 41:4328–4335CrossRefGoogle Scholar
  47. Muraleedharan K (2015) Babesia and babesiosis in livestock of Karnataka state, India—an overview. Vet Res Int 3:81–88Google Scholar
  48. Muraleedharan K, Ziauddin KS, Swamy KG, Muraleedhar T, Seshadri SJ (1984) Some observations on clinical cases of Babesia bovis (Babes, 1888) Starcovici, 1893, in buffaloes (Bubalus bubalis). Indian Vet J 61:76–77Google Scholar
  49. Muraleedharan K, Ziauddin KS, Hussain PM, Puttabyatappa B, Seshadri SJ (1991) Prevalence of haemoprotozoan parasites among buffaloes. Cheiron 20:79–82Google Scholar
  50. Muraleedharan K, Ziauddin KS, Hussain PM, Puttabyatappa B, Mallikarjuna GB, Seshadri SJ (2005) Incidence of Anaplasma sp., Babesia sp. and Trypanosoma sp. in cattle of Karnataka. J Vet Parasitol 19:135–137Google Scholar
  51. Nair AS (2008) Surveillance of haemoprotozoan and haemorickettsial diseases of cattle of Northern Kerala. M.V.Sc thesis, Kerala Agricultural University, Thrissur, Kerala. 126pGoogle Scholar
  52. Nair AS, Ravindran R, Lakshmanan B, Kumar SS, Tresamol PV, Saseendranath MR, Senthilvel K, Rao JR, Tewari AK, Ghosh S (2011) Haemoprotozoa of cattle in Northern Kerala, India. Trop Biomed 28:68–75Google Scholar
  53. Nair AS, Ravindran R, Lakshmanan B, Sreekumar C, Kumar SS, Remya R, Tresamol PV, Vimalkumar MB, Saseendranath MR (2013) Bovine carriers of Anaplasma marginale and Anaplasma bovis in South India. Trop Biomed 30:105–112Google Scholar
  54. Niu Q, Valentin C, Bonsergent C, Malandrin L (2014) Strong conservation of rhoptry-associated-protein-1 (RAP-1) locus organization and sequence among Babesia isolates infecting sheep from China (Babesia motasi-like phylogenetic group). Infect Genet Evol 28:21–32CrossRefGoogle Scholar
  55. Niu Q, Liu Z, Yu P, Yang J, Abdallah MO, Guan G, Liu G, Luo J, Yin H (2015) Genetic characterization and molecular survey of Babesia bovis, Babesia bigemina and Babesia ovata in cattle, dairy cattle and yaks in China. Parasit Vectors 8:518CrossRefGoogle Scholar
  56. Park HS, Lee JH, Jeong EJ, Park TK, Kim TY, Chae JS, Park JH, Klein TA, Jang WJ, Park KH, Lee SH (2005) Differentiation of Anaplasmataceae through partial groEL gene analysis. Microbiol Immunol 49:655–662CrossRefGoogle Scholar
  57. Parola P, Cornet JP, Sanogo YO, Miller RS, Thien HV, Gonzalez JP, Raoult D, Telford IS, Wongsrichanalai C (2003) Detection of Ehrlichia spp., Anaplasma spp., Rickettsia spp., and other Eubacteria in ticks from the Thai-Myanmar border and Vietnam. J Clin Microbiol 41:1600–1608CrossRefGoogle Scholar
  58. Patnaik MM (1963) A note on bovine anaplasmosis. Indian Vet J 40:655–657Google Scholar
  59. Prasath N, Selvaraj J, Jeyathilakan N, Saravanan M, Saravanan M, Ahamad DB, Sasikala M (2016) Occurrence of Anaplasma bovis (Ehrlichia bovis) with varying morphology in a crossbred cow in Tamilnadu, India. Indian J Vet Pathol 40:165–167CrossRefGoogle Scholar
  60. 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:Article ID 9032085, 18 pages. CrossRefGoogle Scholar
  61. Radostits OM, Gay CC, Blood DC, Hinchkliff HW (2000) Veterinary medicine—a text book of the diseases of cattle, sheep, pigs, goats and horses, Ninth edn. W.B. Saunders Company Ltd., New York, p 1812Google Scholar
  62. Ravindran R, Ghosh S (2017) Botanicals for treatment of babesiosis and theileriosis. Ann Pharmacol Pharm 2:1105Google Scholar
  63. Ravindran R, Mishra AK, Rao JR (2002) On the high seroprevalence of bovine babesiosis in Wayanad district of Kerala. J Appl Anim Res 30:142–145Google Scholar
  64. Ravindran R, Mishra AK, Rao JR (2007) Slide enzyme-linked immunosorbent assay for the diagnosis of Babesia bigemina infection in bovines. Vet Res Commun 30:142–145Google Scholar
  65. Ravindran R, Sreekumar C, Saravanan BC, Udaykumar M, Tewari AK, Kumar S, Rao JR, Mishra AK (2010) Genetic variation among Indian isolates of Babesia bigemina. J Vet Parasitol 24:159–163Google Scholar
  66. Sacchi ABV, Duarte JMB, André MR, Machado RZ (2012) Prevalence and molecular characterization of Anaplasmataceae agents in free-ranging Brazilian marsh deer (Blastocerus dichotomus). Comp Immunol Microbiol Infect Dis 35(4):325–334CrossRefGoogle Scholar
  67. Sanogo YO, Davoust B, Inokuma H, Camicas JL, Parola P, Brouqui P (2003) First evidence of Anaplasma platys in Rhipicephalus sanguineus (Acari: Ixodida) collected from dogs in Africa. J Vet Res 70:205–212Google Scholar
  68. Setty DRL, Rao NSK (1972) The pattern of asexual development of Babesia as seen in peripheral blood of a cow. Mysore J Agric Sci 6:474–480Google Scholar
  69. Sharma A, Singla LD, Tuli A, Kaur P, Bal MS (2015) 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 47:251–257CrossRefGoogle Scholar
  70. Shastri U, Degloorkar N, Kulkarni G (1991) Bovine babesiosis due to Babesia bovis at Parbhani (Maharashtra), India. J Vet Parasitol 5:29–34Google Scholar
  71. Shimada MK, Yamamura MH, Kawasaki P, Tamekuni K, Igarashi M, Vidotto O, Vidotto MC (2004) Detection of Anaplasma marginale DNA in larvae of Boophilus microplus ticks by polymerase chain reaction. New York Acad Sci 1026:95–102CrossRefGoogle Scholar
  72. Silveira JA, Rabelo EM, Ribeiro MF (2012) Molecular detection of tick-borne pathogens of the family Anaplasmataceae in Brazilian brown brocket deer (Mazama gouazoubira, Fischer, 1814) and marsh deer (Blastocerus dichotomus, Illiger, 1815). Transbound Emerg Dis 59:353–360CrossRefGoogle Scholar
  73. Sivakumar T, Tattiyapong M, Okubo K, Suganuma K, Hayashida K, Igarashi I, Zakimi S, Matsumoto K, Inokuma H (2014) PCR detection of Babesia ovata from questing ticks in Japan. Ticks Tick Borne Dis 5:205–310CrossRefGoogle Scholar
  74. Soundararajan C, Rajavelu G (2006) Prevalence of haemoprotozoan among cattle and buffaloes. Indian Vet J 83:1258–1260Google Scholar
  75. Sreekumar C, Anandan R, Balasundaram S, Rajavelu G (1996) Morphology and staining characteristics of Ehrlichia bovis. Comp Immunol Microbiol Infect Dis 19:79–83Google Scholar
  76. Sreekumar C, Anandan R, Balasundaram S, John L (2000) Detection of E. bovis—like organism in cultured buffalo monocytes. Trop Anim Health Prod 32:67–72CrossRefGoogle Scholar
  77. Strik NI, Alleman AR, Barbet AF, Sorenson HL, Wamsley HL, Gaschen FP, Luckschander N, Wong S, Chu F, Foley JE, Bjoersdorff A, Stuen S, Knowles DP (2007) Characterization of Anaplasma phagocytophilum major surface protein 5 and the extent of its cross-reactivity with A. marginale. Clin Vaccine Immunol 14:262–268CrossRefGoogle Scholar
  78. Suarez CE, Palmer GH, Florin-Christensen M, Hines SA, Hötzel I, McElwain TF (2003) Organization transcription, and expression of rhoptry associated protein genes in the Babesia bigemina rap-1 locus. Mol Biochem Parasitol 127:101–112CrossRefGoogle Scholar
  79. Suh MD (1987) Pure isolation and identification of Babesia ovata by morphological characteristics and complement fixation test in Korea. Korean J Vet Res 27:307–316Google Scholar
  80. Suksawat J, Pitulle C, Arraga-Alvarado C, Madrigal K, Hancock SI, Breitschwerdt EB (2001) Coinfection with three Ehrlichia species in dogs from Thailand and Venezuela with emphasis on consideration of 16S ribosomal DNA secondary structure. J Clin Microbiol 39:90–93CrossRefGoogle Scholar
  81. Telford SR, Gorenflot A, Brasseur P, Spielman A (1993) Babesial infection in human and wildlife. In: Kreier JP (ed) Parasitic protozoa, vol 5. Academic Press, San Diego, pp 1–47Google Scholar
  82. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefGoogle Scholar
  83. Thompson C, Baravalle ME, Valentini B, Mangold A, de Echaide TS, Ruybal P, Farber M, Echaide I (2014) Typification of virulent and low virulence Babesia bigemina clones by 18S rRNA and rap-1c. Exp Parasitol 141:98–105CrossRefGoogle Scholar
  84. Tian J, Du J, Yang Z, Liu A, Liu X, Liu G, Yin H (2015) A PCR-RFLP assay targeting RPS8 gene for the discrimination between bovine Babesia and Theileria species in China. Parasit Vectors 8:475CrossRefGoogle Scholar
  85. Ulutas B, Bayramli G, Karagenc T (2007) First case of Anaplasma (Ehrlichia) platys infection in a dog in Turkey. Turk J Vet Anim Sci 31:279–282Google Scholar
  86. Van de Peer Y, Baldauf SL, Doolittle WF, Meyer A (2000) An updated and comprehensive rRNA phylogeny of (crown) eukaryotes based on rate-calibrated evolutionary distances. J Mol Evol 51:565–576CrossRefGoogle Scholar
  87. Vijayalakshmi P, Sreekrishnan R (2005) Occurrence, clinical manifestations and treatment of bovine ehrlichiosis. Indian J Vet Med 25:134–135Google Scholar
  88. Walker GK, Edward JT (1927) Some diseases of cattle in India. Government of India, Calcutta, p 29Google Scholar
  89. Weerasooriya G, Sivakumar T, Lan DTB, Long PT, Takemae H, Igarashi I, Inoue N, Yokoyama N (2016) Epidemiology of bovine hemoprotozoa parasites in cattle and water buffalo in Vietnam. J Vet Med Sci 78:1361–1367CrossRefGoogle Scholar
  90. Yoshinari T, Sivakumar T, Asada M, Battsetseg B, Huang X, Lan DT, Inpankaew T, Ybañez AP, Alhassan A, Thekisoe OM, De Macedo AC, Inokuma H, Igarashi I, Yokoyama N (2013) A PCR based survey of Babesia ovata in cattle from various Asian, African and South American countries. J Vet Med Sci 75:211–214CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Rangapura Kariyappa Pradeep
    • 1
  • Murikoli Nimisha
    • 1
  • Meethalae Koombayil Sruthi
    • 1
  • Pakideery Vidya
    • 1
  • Birur Mallappa Amrutha
    • 1
  • Prashant Somalingappa Kurbet
    • 1
  • Karapparambu Gopalan Ajith Kumar
    • 1
  • Anju Varghese
    • 1
  • Chundayil Kalarikkal Deepa
    • 1
  • Chemmangattuvalappil Narendranath Dinesh
    • 2
  • Leena Chandrasekhar
    • 3
  • Sanis Juliet
    • 4
  • Puthenparambil Ramakrishnan Pradeepkumar
    • 5
  • Chintu Ravishankar
    • 6
  • Srikant Ghosh
    • 7
  • Reghu Ravindran
    • 1
    Email author
  1. 1.Department of Veterinary ParasitologyCollege of Veterinary and Animal SciencesWayanadIndia
  2. 2.Department of Animal Breeding and GeneticsCollege of Veterinary and Animal SciencesWayanadIndia
  3. 3.Department of Veterinary AnatomyCollege of Veterinary and Animal SciencesWayanadIndia
  4. 4.Department of Veterinary Pharmacology and ToxicologyCollege of Veterinary and Animal SciencesWayanadIndia
  5. 5.Department of Animal HusbandryThiruvananthapuramIndia
  6. 6.Department of Veterinary MicrobiologyCollege of Veterinary and Animal SciencesWayanadIndia
  7. 7.Division of ParasitologyIndian Veterinary Research InstituteIzatnagarIndia

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