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Ticks and accompanying pathogens of domestic and wild animals of Kerala, South India

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Abstract

The objective of the present study was to detect the chosen nucleotide DNA or RNA sequences of the pathogens in ticks of domestic and wild animals of Kerala, South India based on molecular techniques. Among 602 ticks collected, 413 were from bovines (cattle and buffalo), 26 from goats, 101 from dogs and 62 from wild animals. Amblyomma integrum, Am. gervaisi, Dermacentor auratus, Haemaphysalis bispinosa, Ha. intermedia, Ha. shimoga, Ha. spinigera, Rhipicephalus annulatus, Rh. microplus, Rh. haemaphysaloides and Rh. sanguineus s.l. were identified from various domestic and wild animals of Kerala. The cDNA synthesized from the RNA isolated from fully or partially engorged adult female/nymphal ticks was used as template for the specific polymerase chain reactions (PCR). Out of 602 ticks examined, nucleotide sequences of pathogens were detected in 28 ticks (4.65%). The nucleotide sequences of tick-borne pathogens like Theileria orientalis, Babesia vogeli, Hepatozoon canis, Anaplasma marginale, An. bovis, Rickettsia sp. closely related to Ri. raoultii, Ri. massiliae, Ri. africae and Ri. slovaca were detected. The identification of the previously unreported nucleotide sequences of rickettsial pathogens from India is of particular interest due to their zoonotic significance. The phylogenetic analysis of the major piroplasm surface protein (MPSP) gene of T. orientalis amplified from Rh. annulatus ticks revealed that they were genetically close to type 7, which belong to the highly pathogenic Ikeda group.

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References

  • Abdigoudarzi M (2013) Detection of naturally infected vector ticks (Acari: Ixodidae) by different species of Babesia and Theileria agents from three different enzootic parts of Iran. J Arthropod Borne Dis 7:164–172

    PubMed  PubMed Central  Google Scholar 

  • Abd-Rani PAM, Irwin PJ, Coleman GT, Gatne M, Traub RJ (2011) A survey of canine tick-borne diseases in India. Parasit Vectors 4:141–148

    Article  PubMed  PubMed Central  Google Scholar 

  • Annual Report (2015–2016) National Institute of Veterinary Epidemiology and Disease Informatics (NIVEDI-ICAR), Bangalore

  • Aparna M, Ravindran R, Vimalkumar MB, Lakshmanan B, Rameshkumar P, Ajithkumar KG, Promod K, Ajithkumar S, Ravishankar C, Devada K, Subramanian H, George AJ, Ghosh S (2011) Molecular characterization of Theileria orientalis causing fatal infection in crossbred adult bovines of South India. Parasitol Int 60:524–529

    Article  CAS  PubMed  Google Scholar 

  • Aparna M, Vimal Kumar MB, Varghese S, Sentilvel K, Ajithkumar KG, Raji K, Syamala K, Priya MN, Deepa CK, Jyothimol G, Juliet S, Chandrasekhar L, Ravindran R (2013) Phylogenetic analysis of bovine Theileria spp. isolated in south India. Trop Biomed 30:281–290

    CAS  PubMed  Google Scholar 

  • Araujo AC, Silveira JAG, Azevedo SS, Nieri-Bastos FA, Ribeiro MFB, Labruna MB, Horta MC (2015) Babesia canis vogeli infection in dogs and ticks in the semiarid region of Pernambuco, Brazil. Pesq Vet Bras 35:456–461

    Article  Google Scholar 

  • Auffenberg W, Auffenberg T (1990) The reptile tick Aponomma gervaisi (Acarina: Ixodidae) as a parasite of monitor lizard in Pakistan and India. Biol Sci 35:1–34

    Google Scholar 

  • Augustine S, Sabu L, Lakshmanan B (2017) Molecular identification of Babesia spp. in naturally infected dogs of Kerala. J Parasit Dis 41:459–462

    Article  PubMed  Google Scholar 

  • Baneth G, Samish M, Alekseev E, Aroch I, Shkap V (2001) Transmission of Hepatozoon canis to dogs by naturally-fed or percutaneously-injected Rhipicephalus sanguineus ticks. J Parasitol 87:606–611

    Article  CAS  PubMed  Google Scholar 

  • Crampton A, McKay I, Barker S (1996) Phylogeny of ticks (Ixodida) inferred from nuclear ribosomal DNA. Int J Parasitol 26:511–517

    Article  CAS  PubMed  Google Scholar 

  • Devada K, Abraham MJ, Ajithkumar S, Balakrishnan VS (1996) Hepatozoon canis in a pup-case report. J Vet Anim Sci 27:173–174

    Google Scholar 

  • Esteves E, Bastos CV, Zivkovic Z, de La Fuente J, Kocan K, Blouin E, Ribeiro MFB, Passos LMF, Daffre S (2009) Propagation of a Brazilian isolate of Anaplasma marginale with appendage in a tick cell line (BME26) derived from Rhipicephalus (Boophilus) microplus. Vet Parasitol 161:150–153

    Article  CAS  PubMed  Google Scholar 

  • Estrada-Peña A, Gray JS, Kahl O, Lane RS, Nijhof AM (2013) Research on the ecology of ticks and tick-borne pathogens—methodological principles and caveats. Front Cell Infect Microbiol 3:29

    Article  PubMed  PubMed Central  Google Scholar 

  • Fukumoto S, Hiroshi S, Igarashi I, Xuan X (2005) Fatal experimental transplacental Babesia gibsoni infections in dogs. Int J Parasitol 35:1031–1035

    Article  PubMed  Google Scholar 

  • Geevarghese G, Mishra AC (2011) Haemaphysalis ticks of India, 1st edn. Elsevier, New York

    Google Scholar 

  • Ghosh S, Nagar G (2014) Problem of ticks and tick-borne diseases in India with special emphasis on progress in tick control research: a review. J Vector Dis 51:259–270

    Google Scholar 

  • Ghosh S, Azhahianambi P, de la Fuente J (2006) Control of ticks of ruminants, with special emphasis on livestock farming systems in India: present and future possibilities for integrated control—a review. Exp Appl Acarol 40:49–66

    Article  CAS  PubMed  Google Scholar 

  • Ghosh S, Azhahianambi P, Yadav MP (2007) Upcoming and future strategies of tick control: a review. J Vector Borne Dis 44:79–89

    CAS  PubMed  Google Scholar 

  • Giannelli A, Ramos RAN, Paola GD, Mencke N, Dantas-Torres F, Baneth G, Otranto D (2013) Transstadial transmission of Hepatozoon canis from larvae to nymphs of Rhipicephalus sanguineus. Vet Parasitol 196:1–5

    Article  PubMed  Google Scholar 

  • 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 38:4219–4221

    CAS  PubMed  PubMed Central  Google Scholar 

  • Inokuma H, Okuda M, Ohno K, Shimoda K, Onishi T (2002) Analysis of the 18S rRNA gene sequence of a Hepatozoon detected in two Japanese dogs. Vet Parasitol 106:265–271

    Article  CAS  PubMed  Google Scholar 

  • Inokuma H, Yoshizaki Y, Shimada Y, Sakata Y, Okuda M, Onishi T (2003) Epidemiological survey of Babesia species in Japan performed with specimens from ticks collected from dogs and detection of new Babesia DNA closely related to Babesia odocoilei and Babesia divergens DNA. J Clin Microbiol 41:3494–3498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jefferies R, Ryan UM, Jardine J, Broughton DK, Robertson ID, Irwin PJ (2007) Blood, Bull Terriers and Babesiosis: further evidence for direct transmission of Babesia gibsoni in dogs. Aust Vet J 85:459–463

    Article  CAS  PubMed  Google Scholar 

  • Joshi HS, Thomas M, Warrier A, Kumar S (2012) Gangrene in cases of spotted fever: a report of three cases. BMJ Case Rep 2012:bcr2012007295

    Article  PubMed  PubMed Central  Google Scholar 

  • Kahl O, Gern L, Eisen L, Lane RS (2002) Ecological research on Borrelia burgdorferi sensu lato: terminology and some methodological pitfalls. In: Gray J, Kahl O, Lane RS, Stanek G (eds) Lyme borreliosis: biology, epidemiology and control. CABI Publishing, New York, pp 29–46

    Chapter  Google Scholar 

  • Kakati P, Sarmah PC, Ray D, Bhattacharjee K, Sharma RK, Barkalita LM, Sarma DK, Baishya BC, Borah P, Stanley B (2015) Emergence of oriental theileriosis in cattle and its transmission through Rhipicephalus (Boophilus) microplus in Assam, India. Vet World 8:1099–1104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamani J, Baneth G, Mumcuoglu KY, Waziri NE, Eyal O, Guthmann Y, Harrus S (2013) Molecular detection and characterization of tick-borne pathogens in dogs and ticks from Nigeria. PLoS Negl Trop Dis 7:e2108. https://doi.org/10.1371/journal.pntd.0002108

    Article  PubMed  PubMed Central  Google Scholar 

  • Kariyappa PR, Ravindran R, Nimisha M, Amrutha BM, Kurbet PS, Kumar KGA, Varghese A, Deepa CK, Dinesh CN (2017) Prevalence of bovine babesiosis and theileriosis in Kerala, India. Int J Curr Microbiol Appl Sci 6:2310–2314

    Article  Google Scholar 

  • Kawahara M, Rikihisa Y, Lin Q, Isogai E, Tahara K, Itagaki A, Hiramitsu Y, Tajima T (2006) Novel genetic variants of Anaplasma phagocytophilumA. bovisA. centrale, and a Novel Ehrlichia sp. in wild deer and ticks on two major islands in Japan. Appl Environ Microbiol 72:1102–1109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khukhuu A, Lan DTB, Long PT, Ueno A, Li Y, Luo Y, Macedo ACC, Matsumoto K, Inokuma H, Kawazu SI, Igarashi I, Xuan X, Yokoyama N (2011) Molecular epidemiological survey of Theileria orientalis in Thua Thien Hue province, Vietnam. J Vet Med Sci 73:701–705

    Article  PubMed  Google Scholar 

  • 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. https://doi.org/10.1371/journal.pone.0174595

    Article  PubMed  PubMed Central  Google Scholar 

  • Kumar R, Paul S, Kumar S, Sharma AK, Gupta S, Rawat AKS, Chaudhuri P, Ray DD, Ghosh S (2011) Nucleotide specific changes in the hypervariable region of 16S rDNA gene as possible marker to differentiate the tick genera. Indian J Anim Sci 81:1204–1207

    CAS  Google Scholar 

  • Kumar KGA, Ravindran R, Ghosh S (2012) First report of Dermacentor auratus Supino, 1897 (Acarina, Ixodidae) from Wayanad, Kerala. Indian J Med Res 135:435–436

    Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar KGA, Ravindran R, Johns J, Chandy G, Rajagopal K, Chandrasekhar L, George AJ, Ghosh S (2018) Ixodid tick vectors of wild mammals and reptiles of southern India. J Arthropod Borne Dis 12:276–285

    Google Scholar 

  • Kuo-Fan T (1991) Acari: Ixodidae. Econ Insect Fauna China 39:1–359

    Google Scholar 

  • Labruna MB, Whitworth T, Mauricio CH, Bouyer H, McBridge JW, Pinter A, Popov V, Gennari SM, Walker DH (2004) Rickettsia species infecting Amblyomma cooperi ticks from an area in the state of Sao Paulo, Brazil, where Brazilin spotted fever is endemic. J Clin Microbiol 42:90–98

    Article  PubMed  PubMed Central  Google Scholar 

  • Lakshmanan B, Jose KJ, George A, Usha NP, Devada K (2018) Molecular detection of Hepatozoon canis in dogs from Kerala. J Parasit Dis 42:287–290

    Article  PubMed  PubMed Central  Google Scholar 

  • Latrofa MS, Torres FD, Giannelli A, Otranto D (2014) Molecular detection of tick-borne pathogens in Rhipicephalus sanguineus group ticks. Ticks Tick Borne Dis 5:943–946

    Article  PubMed  Google Scholar 

  • Mahalingaiah MKC, Asoor M, Thimmaiah RP, Narayanaswamy HD, Mukartal SY, Elattuvalappil AM, Chikkahonnaiah N, Gupta S, Singh S (2017) Prevalence of canine babesiosis in different breeds of dogs in and around Bengaluru. Adv Anim Vet Sci 5:140–144

    Article  Google Scholar 

  • Manjunathachar HV, Saravanan BC, Kesavan M, Karthik K, Rathod P, Gopi M, Tamilmahan P, Balaraju BL (2014) Economic importance of ticks and their effective control strategies. Asian Pac J Trop Dis 4:770–779

    Article  Google Scholar 

  • Matjila PT, Penzhorn BL, Bekker CPJ, Nijhof AM, Jongejan F (2004) Confirmation of occurrence Babesia canis vogeli in domestic dogs in South Africa. Vet Parasitol 122:119–125

    Article  CAS  PubMed  Google Scholar 

  • Mediannikov OY, Sideonikov Y, Ivanov L, Mokressova E, Fournier PE, Tarasevich I, Raoult D (2004) Acute tick borne rickettsiosis, caused by Rickettsia heilongjiangensis variant in the Russian Far East. Emerg Infect Dis 10:810–817

    Article  PubMed  PubMed Central  Google Scholar 

  • Naicke PR (2011) The impact of climate change and other factors on zoonotic diseases. Arch Clin Microbiol 2:1–5

    Google Scholar 

  • 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 28:68–75

    CAS  PubMed  Google Scholar 

  • Nair AS, Ravindran R, Lakshmanan B, Sreekumar C, Kumar SS, Raju Remya, Tresamol PV, Vimalkumar MB, Saseendranath MR (2013) Bovine carriers of Anaplasma marginale and Anaplasma bovis in South India. Trop Biomed 30:105–112

    CAS  PubMed  Google Scholar 

  • Nimisha M, Pradeep RK, Kurbet PS, Amrutha BM, Varghese A, Deepa CK, Priya MN, Lakshmanan B, Kumar KGA, Ravindran R (2017) Parasitic diseases of domestic and wild animals in northern Kerala: a retrospective study based on clinical samples. Int J Curr Microbiol Appl Sci 6:2381–2392

    Article  Google Scholar 

  • Palomar AM, Portillo A, Santibáñez P, Mazuelas D, Roncero L, García-Álvarez L, Santibáñez S, Gutiérrez Ó, Oteo JA (2015) Detection of tick-borne Anaplasma bovis, A. phagocytophilum and A. centrale in Spain. Med Vet Entomol 29:349–353

    Article  CAS  PubMed  Google Scholar 

  • Parola P, Paddock CD, Raoult D (2005) Tick-borne rickettsioses around the world: emerging diseases challenging old concepts. Clin Microbiol Rev 18:719–756

    Article  PubMed  PubMed Central  Google Scholar 

  • Parola P, Paddock CD, Socolovschi C, Labruna MB, Mediannikov O, Kernif T, Abdad MY, Stenos J, Bitam I, Fournier P, Raoult D (2013) Update on tick-borne rickettsioses around the world: a geographic approach. Clin Microbiol Rev 26:657–702

    Article  PubMed  PubMed Central  Google Scholar 

  • Ponnudurai G, Larcombe S, Velusamy R, Rani N, Kolte SW, Rubinibala B, Alagesan A, Rekha B, Shiels B (2017) Prevalence of tick-borne pathogens in co-grazed dairy bovines differs by region and host-type in Tamil Nadu, India. J Adv Dairy Res 5:177

    Google Scholar 

  • Pradeep RK, Nimisha M, Sruthi MK, Pakideery V, Amrutha BM, Kurbet PS, Kumar KGA, Varghese A, Deepa CK, Dinesh CN, Chandrasekhar L, Juliet S, Pradeepkumar PR, Ravishankar C, Ghosh S, Ravindran R (2019) Molecular characterization of South Indian field isolates of bovine Babesia spp. and Anaplasma spp. Parasitol Res 118:617–630

    Article  PubMed  Google Scholar 

  • Rathi N, Rathi A (2010) Rickettsial infections: Indian perspective. Indian Pediatr 47:157–164

    Article  PubMed  Google Scholar 

  • Ravindran R, Mishra AK, Rao JR (2002) On the high seroprevalence of bovine babesiosis in Wayanad district of Kerala. J Appl Anim Res 22:43–48

    Article  Google Scholar 

  • René-Martellet M, Moro CV, Chêne J, Bourdoiseau G, Chabanne L, Mavingui P (2015) Update on epidemiology of canine babesiosis in Southern France. BMC Vet Res 11:223–233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roux V, Raoult D (1995) Phylogenetic analysis of the genus Rickettsia by 16S rDNA sequencing. Res Microbiol 146:385–396

    Article  CAS  PubMed  Google Scholar 

  • Roux V, Raoult D (1999) Body lice as tools for diagnosis and surveillance of reemerging diseases. J Clin Microbiol 37:596–599

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ruiz-Fons F, Gilbert L (2010) The role of deer as vehicles to move ticks Ixodes ricinus between contrasting habitats. Int J Parasitol 40:1013–1020

    Article  PubMed  Google Scholar 

  • Sahu A, Mohanty B, Panda MR, Sardar KK (2014) Incidence of haemoprotozoan parasites in dogs in and around Bhubaneswar, Odisha. Indian Vet J 91:93–95

    Google Scholar 

  • Shayan P, Hooshmand E, Rahbari S (2007) Determination of Rhipicephalus spp. as vectors for Babesia ovis in Iran. Parasitol Res 101:1029–1033

    Article  PubMed  Google Scholar 

  • Shyma KP, Stanley B, Ray DD, Ghosh S (2013) Prevalence of cattle and buffalo ticks in northern Kerala. J Vet Parasitol 27(1):55–56

    Google Scholar 

  • Smitha JP, Thushara MR, Vijayakumar K, Saseedranath MR, Baby PG (2003) Concurrent infection of Ehrlichia sp. and Hepatozoon canis in a dog- a case report. Indian Vet J 80:1059–1060

    Google Scholar 

  • Soundararajan C, Nagarajan K, Prakash MA (2018) Tick infestation in human beings in the Nilgiris and Kancheepuram District of Tamil Nadu, India. J Parasit Dis 42:50–54

    Article  CAS  PubMed  Google Scholar 

  • Stegeman JR, Birkenheuer AJ, Kruger JM, Breitschwerdt EB (2003) Transfusion-associated Babesia gibsoni infection in a dog. J Am Vet Med Assoc 222:959–963

    Article  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trapido H, Varma MGR, Rajagopalan PK, Singh KRP, Rebello MJ (1964) A guide to the identification of all stages of the Haemaphysalis ticks of South India. Bull Entomol Res 55:249–270

    Article  Google Scholar 

  • Voltzit OV, Keirans JE (2002) A review of Asian Amblyomma species (Acari: Ixodida). Acarina 10:95–136

    Google Scholar 

  • Yokoyama N, Ueno A, Mizuno D, Kuboki N, Khukhuu A, Igarashi I, Miyahara T, Shiraishi T, Kudo R, Oshiro M, Zakimi S, Sugimoto C, Matsumoto K, Inokuma H (2011) Genotypic diversity of Theileria orientalis detected from cattle grazing in Kumamoto and Okinawa prefectures of Japan. J Vet Med Sci 73:305–312

    Article  PubMed  Google Scholar 

  • Yoshimoto K, Matsuyama Y, Matsuda H, Sakamoto L, Matsumoto K, Yokoyama N, Inokuma H (2010) Detection of Anaplasma bovis and A. phagocytophilum DNA from Haemaphysalis megaspinosa in Hokkaido, Japan. Vet Parasitol 168:170–172

    Article  PubMed  Google Scholar 

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Acknowledgements

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

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Nimisha, M., Devassy, J.K., Pradeep, R.K. et al. Ticks and accompanying pathogens of domestic and wild animals of Kerala, South India. Exp Appl Acarol 79, 137–155 (2019). https://doi.org/10.1007/s10493-019-00414-z

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