Advertisement

Acta Parasitologica

, Volume 62, Issue 4, pp 836–841 | Cite as

Transovarial persistence of Babesia ovata DNA in a hard tick, Haemaphysalis longicornis, in a semi-artificial mouse skin membrane feeding system

  • Rika Umemiya-ShirafujiEmail author
  • Takeshi Hatta
  • Kazuhiro Okubo
  • Moeko Sato
  • Hiroki Maeda
  • Aiko Kume
  • Naoaki Yokoyama
  • Ikuo Igarashi
  • Naotoshi Tsuji
  • Kozo Fujisaki
  • Noboru Inoue
  • Hiroshi Suzuki
Research Note

Abstract

Bovine piroplasmosis, a tick-borne protozoan disease, is a major concern for the cattle industry worldwide due to its negative effects on livestock productivity. Toward the development of novel therapeutic and vaccine approaches, tick-parasite experimental models have been established to clarify the development of parasites in the ticks and the transmission of the parasites by ticks. A novel tick-Babesia experimental infection model recently revealed the time course of Babesia ovata migration in its vector Haemaphysalis longicornis, which is a dominant tick species in Japan. However, there has been no research on the transovarial persistence of B. ovata DNA using this experimental infection model. Here we assessed the presence of B. ovata DNA in eggs derived from parthenogenetic H. longicornis female ticks that had engorged after semi-artificial mouse skin membrane feeding of B. ovata-infected bovine red blood cells. The oviposition period of the engorged female ticks was 21–24 days in the semi-artificial feeding. Total egg weight measured daily reached a peak by day 3 in all female ticks. Nested PCR revealed that 3 of 10 female ticks laid B. ovata DNA-positive eggs after the semi-artificial feeding. In addition, B. ovata DNA was detected at the peak of egg weight during oviposition, indicating that B. ovata exist in the eggs laid a few days after the onset of oviposition in the tick. These findings will contribute to the establishment of B. ovata-infected H. longicornis colonies under laboratory conditions.

Keywords

Tick Haemaphysalis longicornis egg Babesia ovata β-tubulin nested PCR 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bonnet S., Jouglin M., Malandrin L., Becker C., Agoulon A., L’hostis M., Chauvin A. 2007. Transstadial and transovarial persistence of Babesia divergens DNA in Ixodes ricinus ticks fed on infected blood in a new skin-feeding technique. Parasitology, 134, 197–207. DOI: 10.1017/S0031182006001545PubMedCrossRefGoogle Scholar
  2. Büscher G., Friedhoff K.T., El-Allawy T.A. 1988. Quantitative description of the development of Babesia ovis in Rhipicephalus bursa (hemolymph, ovary, eggs). Parasitology Research, 74, 331–339. DOI: 10.1007/BF00539454PubMedCrossRefGoogle Scholar
  3. Cafrune M.M., Aguirre D.H., Mangold A.J., Guglielmone A.A. 1995. Experimental studies of the rate of infection of Boophilus microplus eggs with Babesia bovis. Research in Veterinary Science, 58, 284–285. DOI: 10.1016/0034-5288(95)90119-1PubMedCrossRefGoogle Scholar
  4. Fujisaki K. 1978. Development of acquired resistance precipitating antibody in rabbits experimentally infested with females of Haemaphysalis longicornis (Ixodoidea: Ixodidae). National Institute of Animal Health Quarterly, 18, 27–38PubMedGoogle Scholar
  5. Fujisaki K., Kamio T., Kawazu S., Minami T., Nakamura Y., Shimura K., et al. 1988. Experimental transmission of Theileria sergenti of cattle in Japan by Haemaphysalis mageshimaensis. Annals of Tropical Medicine and Parasitology, 82, 513–515PubMedCrossRefGoogle Scholar
  6. Hatta T., Matsubayashi M., Miyoshi T., Islam K., Alim M.A., Anisuzzaman Yamaji K., et al. 2013. Quantitative PCR-based parasite burden estimation of Babesia gibsoni in the vector tick, Haemaphysalis longicornis (Acari: Ixodidae), fed on an experimentally infected dog. The Journal of Veterinary Medical Science, 75, 1–6. DOI: 10.1292/jvms.12-0175PubMedCrossRefGoogle Scholar
  7. Hatta T., Miyoshi T., Matsubayashi M., Islam M.K., Alim M.A., Anisuzzaman Yamaji K., et al. 2012. Semi-artificial mouse skin membrane feeding technique for adult tick, Haemaphysalis longicornis. Parasites & Vectors, 5, 263. DOI: 10.1186/1756-3305-5-263CrossRefGoogle Scholar
  8. Higuchi S., Hamana M., Etoh K., Kawamura S., Yasuda Y. 1991. Development of Babesia ovata in the ovary and eggs of the tick, Haemaphysalis longicornis. The Kitasato Archives of Experimental Medicine, 64, 133–139PubMedGoogle Scholar
  9. Igarashi I., Avarzed A., Tanaka T., Inoue N., Ito M., Omata Y., et al. 1994. Continuous in vitro cultivation of Babesia ovata. The Journal of protozoology research, 4, 111–118. DOI: 10.1007/s004360000254Google Scholar
  10. Inokuma H., Kemp D.H. 1998. Establishment of Boophilus microplus infected with Babesia bigemina by using in vitro tube feeding technique. The Journal of Veterinary Medical Science, 60, 509–512. DOI: 10.1292/jvms.60.509PubMedCrossRefGoogle Scholar
  11. Maeda H., Hatta T., Alim M.A., Tsubokawa D., Mikami F., Matsubayashi M., et al. 2016. Establishment of a novel tick-Babesia experimental infection model. Scientific Reports, 6, 37039. DOI: 10.1038/srep37039PubMedPubMedCentralCrossRefGoogle Scholar
  12. Marcelino I., de Almeida A.M., Ventosa M., Pruneau L., Meyer D.F., Martinez D., et al. 2012. Tick-borne diseases in cattle: applications of proteomics to develop new generation vaccines. Journal of Proteomics, 75, 4232–4250. DOI: 10.1016/j.jprot.2012.03.026PubMedCrossRefGoogle Scholar
  13. Ohta M., Kawazu S., Terada Y., Kamio T., Tsuji M., Fujisaki K. 1996. Experimental transmission of Babesia ovata oshimensis n. var. of cattle in Japan by Haemaphysalis longicornis. The Journal of Veterinary Medical Science, 58, 1153–115PubMedCrossRefGoogle Scholar
  14. Oliveira M.C., Oliveira-Sequeira T.C., Araujo J.P., Amarante A.F., Oliveira H.N. 2005. Babesia spp. infection in Boophilus microplus engorged females and eggs in Sao Paulo State, Brazil. Veterinary Parasitology, 130, 61–67. DOI: 10.1016/j.vetpar.2005.03.007PubMedCrossRefGoogle Scholar
  15. Shimizu S., Nojiri K., Matsunaga N., Yamane I., Minami T. 2000. Reduction in tick numbers (Haemaphysalis longicornis), mortality and incidence of Theileria sergenti infection in field-grazed calves treated with flumethrin pour-on. Veterinary Parasitology, 92, 129–138. DOI: 10.1016/S0304-4017(00)00278-8PubMedCrossRefGoogle Scholar
  16. Singla L.D., Sumbria D., Mandhotra A., Bal M.S., Kaur P. 2016. Critical analysis of vector-borne infections in dogs: Babesia vogeli, Babesia gibsoni, Ehrlichia canis and Hepatozoon canis in Punjab, India. Acta Parasitol, 61, 697–706. DOI: 10.1515/ap-2016-0098PubMedCrossRefGoogle Scholar
  17. Sivakumar T., Igarashi I., Yokoyama N. 2016. Babesia ovata: Taxonomy, phylogeny and epidemiology. Veterinary Parasitology, 229, 99–106. DOI: 10.1016/j.vetpar.2016.10.006PubMedCrossRefGoogle Scholar
  18. Sivakumar T., Tattiyapong M., Okubo K., Suganuma K., Hayashida K., Igarashi I., et al. 2014. PCR detection of Babesia ovata from questing ticks in Japan. Ticks and Tick-borne Diseases, 5, 305–310. DOI: 10.1016/j.ttbdis.2013.12.006PubMedCrossRefGoogle Scholar
  19. Takeet M.I., Oyewusi A.J., Abakpa S.A., Daramola O.O., Peters S.O. 2017. Genetic diversity among Babesia rossi detected in naturally infected dogs in Abeokuta, Nigeria, based on 18S rRNA gene sequences. Acta Parasitol, 62, 192–198. DOI: 10.1515/ap-2017-002PubMedCrossRefGoogle Scholar
  20. Voigt W.P., Young A.S., Mwaura S.N., Nyaga S.G., Njihia G.M., Mwakima F.N., Morzaria S.P. 1993. In vitro feeding of instars of the ixodid tick Amblyomma variegatum on skin membranes and its application to the transmission of Theileria mutans and Cowdria ruminantium. Parasitology, 107, 257. DOI: 10.1017/S0031182000079233PubMedCrossRefGoogle Scholar
  21. Watts J.G., Playford M.C., Hickey K.L. 2016. Theileria orientalis: a review. The New Zealand Veterinary Journal, 64, 3–9. DOI: 10.1080/00480169.2015.1064792PubMedCrossRefGoogle Scholar

Copyright information

© Witold Stefański Institute of Parasitology, Polish Academy of Sciences 2017

Authors and Affiliations

  • Rika Umemiya-Shirafuji
    • 1
    • 2
    Email author
  • Takeshi Hatta
    • 3
  • Kazuhiro Okubo
    • 1
  • Moeko Sato
    • 1
  • Hiroki Maeda
    • 3
    • 4
  • Aiko Kume
    • 1
  • Naoaki Yokoyama
    • 1
    • 2
  • Ikuo Igarashi
    • 1
    • 2
  • Naotoshi Tsuji
    • 3
  • Kozo Fujisaki
    • 5
  • Noboru Inoue
    • 6
  • Hiroshi Suzuki
    • 1
    • 2
  1. 1.National Research Center for Protozoan DiseasesObihiro University of Agriculture and Veterinary MedicineObihiro, HokkaidoJapan
  2. 2.Research Center for Global AgromedicineObihiro University of Agriculture and Veterinary MedicineObihiro, HokkaidoJapan
  3. 3.Kitasato University School of MedicineSagamihara, KanagawaJapan
  4. 4.Department of Pathological and Preventive Veterinary Science, The United Graduate School of Veterinary ScienceYamaguchi UniversityYamaguchiJapan
  5. 5.National Agricultural and Food Research OrganizationTsukuba, IbarakiJapan
  6. 6.Obihiro University of Agriculture and Veterinary MedicineObihiro, HokkaidoJapan

Personalised recommendations