Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter October 15, 2017

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

Rika Umemiya-Shirafuji, Takeshi Hatta, Kazuhiro Okubo, Moeko Sato, Hiroki Maeda, Aiko Kume, Naoaki Yokoyama, Ikuo Igarashi, Naotoshi Tsuji, Kozo Fujisaki, Noboru Inoue and Hiroshi Suzuki
From the journal Acta Parasitologica

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.


Present address: Department of Infectious Diseases, Hokkaido Institute of Public Health, North 19, West 12, Kita-ku Sapporo 060-0819, Japan


Acknowledgements

The first author was supported by the Grant-in-Aid for Young Scientists (B) from the Japan Society for the Promotion of Science (16K18794) and The Akiyama Life Science Foundation. This research was also supported by The Japan Agency for Medical Research and Development (AMED)/The Japan International Cooperation Agency (JICA), and the Science and Technology Research Partnership for Sustainable Development (SATREPS).

References

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. 10.1017/S0031182006001545Search in Google Scholar

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. 10.1007/BF00539454Search in Google Scholar PubMed

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. 10.1016/0034-5288(95)90119-1Search in Google Scholar PubMed

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, 27–38Search in Google Scholar PubMed

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, 513–51510.1080/00034983.1988.11812285Search in Google Scholar PubMed

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. 10.1292/jvms.12-0175Search in Google Scholar PubMed

Hatta T., Miyoshi T., Matsubayashi M., Islam M.K., Alim M.A., Anisuzzaman, et al. 2012. Semi-artificial mouse skin membrane feeding technique for adult tick, Haemaphysalis longicornis. Parasites & Vectors, 5, 263.10.1186/1756-3305-5-263Search in Google Scholar PubMed PubMed Central

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, 133–139Search in Google Scholar PubMed

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. 10.1007/s004360000254Search in Google Scholar PubMed

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. 10.1292/jvms.60.509Search in Google Scholar PubMed

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. 10.1038/srep37039Search in Google Scholar PubMed PubMed Central

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. 10.1016/j.jprot.2012.03.026Search in Google Scholar PubMed

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, 1153–11510.1292/jvms.58.11_1153Search in Google Scholar PubMed

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. 10.1016/j.vetpar.2005.03.007Search in Google Scholar PubMed

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. 10.1016/S0304-4017(00)00278-8Search in Google Scholar PubMed

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. 10.1515/ap-2016-0098Search in Google Scholar PubMed

Sivakumar T., Igarashi I., Yokoyama N. 2016. Babesia ovata: Taxonomy, phylogeny and epidemiology. Veterinary Parasitology, 229, 99–106. 10.1016/j.vetpar.2016.10.006Search in Google Scholar PubMed

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. 10.1016/j.ttbdis.2013.12.006Search in Google Scholar PubMed

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. 10.1515/ap-2017-002Search in Google Scholar PubMed

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. 10.1017/S0031182000079233Search in Google Scholar PubMed

Watts J.G., Playford M.C., Hickey K.L. 2016. Theileria orientalis: a review. The New Zealand Veterinary Journal, 64, 3–9. 10.1080/00480169.2015.1064792Search in Google Scholar PubMed

Received: 2017-1-29
Revised: 2017-8-4
Accepted: 2017-8-16
Published Online: 2017-10-15
Published in Print: 2017-12-20

© 2017 W. Stefański Institute of Parasitology, PAS