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Acta Parasitologica

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Volume 62, Issue 4

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

Rika Umemiya-Shirafuji
  • Corresponding author
  • National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-Cho, Obihiro, Hokkaido 080-8555, Japan
  • Research Center for Global Agromedicine, Obihiro University of Agriculture and Veterinary Medicine, Inada-Cho, Obihiro, Hokkaido 080-8555, Japan
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Takeshi Hatta
  • Kitasato University School of Medicine, Kitasato 1-15-1, Sagamihara, Kanagawa, 252-0374, Japan
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/ Kazuhiro Okubo
  • National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-Cho, Obihiro, Hokkaido 080-8555, Japan
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/ Moeko Sato
  • National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-Cho, Obihiro, Hokkaido 080-8555, Japan
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/ Hiroki Maeda
  • Kitasato University School of Medicine, Kitasato 1-15-1, Sagamihara, Kanagawa, 252-0374, Japan
  • Department of Pathological and Preventive Veterinary Science, The United Graduate School of Veterinary Science, Yamaguchi University, Yoshida, Yamaguchi 753-8515, Japan
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/ Aiko Kume
  • National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-Cho, Obihiro, Hokkaido 080-8555, Japan
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/ Naoaki Yokoyama
  • National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-Cho, Obihiro, Hokkaido 080-8555, Japan
  • Research Center for Global Agromedicine, Obihiro University of Agriculture and Veterinary Medicine, Inada-Cho, Obihiro, Hokkaido 080-8555, Japan
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/ Ikuo Igarashi
  • National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-Cho, Obihiro, Hokkaido 080-8555, Japan
  • Research Center for Global Agromedicine, Obihiro University of Agriculture and Veterinary Medicine, Inada-Cho, Obihiro, Hokkaido 080-8555, Japan
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/ Naotoshi Tsuji
  • Kitasato University School of Medicine, Kitasato 1-15-1, Sagamihara, Kanagawa, 252-0374, Japan
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/ Kozo Fujisaki
  • National Agricultural and Food Research Organization, Kannondai 3-1-5, Tsukuba, Ibaraki 305-0856, Japan
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/ Noboru Inoue
  • Obihiro University of Agriculture and Veterinary Medicine, Inada-Cho, Obihiro, Hokkaido 080-8555, Japan
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/ Hiroshi Suzuki
  • National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-Cho, Obihiro, Hokkaido 080-8555, Japan
  • Research Center for Global Agromedicine, Obihiro University of Agriculture and Veterinary Medicine, Inada-Cho, Obihiro, Hokkaido 080-8555, Japan
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Published Online: 2017-10-15 | DOI: https://doi.org/10.1515/ap-2017-0100

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

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. CrossrefWeb of ScienceGoogle 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. CrossrefPubMedGoogle Scholar

  • 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. CrossrefPubMedGoogle Scholar

  • 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

  • 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, 513–515CrossrefPubMedGoogle Scholar

  • 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. CrossrefPubMedWeb of ScienceGoogle Scholar

  • 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.CrossrefPubMedWeb of ScienceGoogle Scholar

  • 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

  • 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. CrossrefGoogle Scholar

  • 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. CrossrefPubMedGoogle Scholar

  • 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. CrossrefPubMedWeb of ScienceGoogle Scholar

  • 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. CrossrefWeb of SciencePubMedGoogle Scholar

  • 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

  • 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. CrossrefPubMedGoogle Scholar

  • 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. CrossrefPubMedGoogle Scholar

  • 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. CrossrefWeb of SciencePubMedGoogle Scholar

  • Sivakumar T., Igarashi I., Yokoyama N. 2016. Babesia ovata: Taxonomy, phylogeny and epidemiology. Veterinary Parasitology, 229, 99–106. CrossrefWeb of SciencePubMedGoogle Scholar

  • 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. CrossrefWeb of SciencePubMedGoogle Scholar

  • 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. CrossrefPubMedWeb of ScienceGoogle Scholar

  • 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. CrossrefPubMedGoogle Scholar

  • Watts J.G., Playford M.C., Hickey K.L. 2016. Theileria orientalis: a review. The New Zealand Veterinary Journal, 64, 3–9. CrossrefGoogle Scholar

About the article


Received: 2017-01-29

Revised: 2017-08-04

Accepted: 2017-08-16

Published Online: 2017-10-15

Published in Print: 2017-12-20


Citation Information: Acta Parasitologica, Volume 62, Issue 4, Pages 836–841, ISSN (Online) 1896-1851, ISSN (Print) 1230-2821, DOI: https://doi.org/10.1515/ap-2017-0100.

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