Skip to main content
SpringerLink
Log in

Meteorological factors affecting seroconversion of Akabane disease in sentinel calves in the subtropical Okinawa Islands of Japan

  • Short Communications
  • Published:
Tropical Animal Health and Production Aims and scope Submit manuscript

Abstract

Akabane virus, the pathogen-causing Akabane disease, is an arthropod-borne virus (arbovirus) transmitted by the Culicoides biting midge. A nationwide serological surveillance program for bovine arboviral diseases, including Akabane disease, has been established in Japan to monitor the circulation of arboviruses by targeting sentinel calves. Okinawa, which is located in the southwestern-most region of Japan, is a high-risk area for incursion of arboviruses. The aim of the present study was to identify the meteorological factors related to farm-level seroconversion of Akabane virus by analyzing the serological surveillance data for sentinel calves collected in Okinawa between 2007 and 2015. Rainfall in winter, spring, and autumn was positively associated with seroconversion. Adequate rainfall seems to keep the soil in a suitably moist state for growth and survival of biting midges. Maximum temperature in winter was also positively associated with seroconversion in sentinel calves. The warmer temperatures in winter may provide conditions suitable for shortening the larval development cycle and increase production of adult midges. Our findings indicate that meteorological factors such as temperature and rainfall may be important factors that produce circumstances conducive to effective transmission of the virus between vectors and the host. The results of this study provide a better understanding of the circulation of arboviruses and offer suggestions for developing better surveillance and measures to prevent arboviral disease.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

References

  • Akaike, H. 1998. Information theory and an extension of the maximum likelihood principle. In: Selected Papers of Hirotugu Akaike. (Springer, New York), 199–213.

  • Bellis, G., Dyce, A., Gopurenko, D., Yanase, T., Garros, C., Labuschagne, K. and Mitchell, A., 2014. Revision of the Culicoides (Avaritia) Imicola complex Khamala & Kettle (Diptera: Ceratopogonidae) from the Australasian region, Zootaxa, 3768, 401–427

    Article  Google Scholar 

  • Bellis, G., Halling, L. and Anderson, S.J., 2015. Pictorial key to adult female Culicoides Latreille, 1809 (Diptera: Ceratopogonidae) from the Northern Territory, Western Australia and South Australia, Australian Journal of Entomology, 54, 28–59

    Article  Google Scholar 

  • Bishop, A.L., McKenzie, H.J., Barchia, I.M. and Harris, A.M., 1996. Effect of temperature regimes on the development, survival and emergence of Culicoides brevitarsis Kieffer (Diptera: Ceratopogonidae) in bovine dung, Australian Journal of Entomology, 35, 361–368

    Article  Google Scholar 

  • Braverman, Y., 1992. Host detection, hourly activity, and preferred landing sites of Culicoides imicola (Diptera: Ceratopogonidae) on a calf in Israel. In: T.E. Walton and B.I. Osburn (eds), Bluetongue, African horse sickness, and related orbiviruses. Proceedings of the 2nd international symposium. Boca Raton, FL, USA, CRC Press

  • Braverman, Y. and Galun R., 1973. The occurrence of Culicoides in Israel with reference to the incidence of bluetongue, Refuah Veterinarith, 30, 121–127

    Google Scholar 

  • Della-Porta A.J., White J.R., Gard G.P. and Kirkland P.D., 1993. Akabane disease. In: Corner L.A. and Bagust T.J, (eds), Australian standard diagnostic techniques for animal diseases, CSIRO, for the Standing Committee on Agriculture and Resource Management, Melbourne, Australia, pp. 1–11.

  • Elbers, A.R.W., Koenraadt, C.J.M. and Meiswinkel, R., 2015. Mosquitoes and Culicoides biting midges: vector range and the influence of climate change, Scientific and Technical Review of the Office International des Epizooties (Paris), 34, 123–137

    Article  CAS  Google Scholar 

  • Hoshino, C., 1985. Notes on biting midges collected by light traps at a cowshed in Ishigaki-jima, Ryukyu Islands. (In Japanese with English summary), Medical Entomology and Zoology, 36, 55–58

    Article  Google Scholar 

  • Inaba, Y. and Matumoto, M., 1990. Akabane virus. In: Dinter Z. and Morein B. (eds), Virus infections of ruminants. Amsterdam, The Netherlands, Elsevier Science Publishers, 467–480

    Chapter  Google Scholar 

  • Kato, T., Yanase, T., Suzuki, M., Katagiri, Y., Ikemiyagi, K., Takayoshi, K., Shirafuji, H., Ohashi, S., Yoshida, K., Yamakawa, M. and Tsuda, T., 2016. Monitoring for bovine arboviruses in the most southwestern islands in Japan between 1994 and 2014, BMC Veterinary Research, 12, 125

    Article  Google Scholar 

  • Kettle, D.S., 1957. Preliminary observations on weather conditions and the activity of biting flies, Proceedings of the Royal Entomological Society of London Series A, 32, 13–20

    Article  Google Scholar 

  • Kettle, D.S., 1995. Ceratopogonidae (biting midges). In: Medical and Veterinary Entomology. 2nd ed. CABI Publishing, Cambridge, 152–176

    Google Scholar 

  • Kettle, D.S. and Linley, J.R., 1969. The biting habits of some Jamaican Culicoides. I. C. barbosai Wirth & Blanton, Bulletin of Entomological Research, 58, 729–753

    Article  CAS  Google Scholar 

  • Kirkland, P.D., 2015. Akabane virus infection, Scientific and Technical Review of the Office International des Epizooties (Paris), 34, 403–410.

  • Kono, R., Hirata, M., Kaji, M., Goto, Y., Ikeda, S., Yanase, T., Kato, T., Tanaka, S., Tsutsui, T., Imada, T. and Yamakawa, M., 2008. Bovine epizootic encephalomyelitis caused by Akabane virus in southern Japan, BMC Veterinary Research 4, 20

    Article  Google Scholar 

  • Lühken, R., Steinke, S., Hoppe, N. and Kiel, E., 2015. Effect of temperature and photoperiod on the development of overwintering immature Culicoides chiopterus and Culicoides dewulfi, Veterinary Parasitology, 214, 195–199

    Article  Google Scholar 

  • Mellor, P.S., Boorman, J. and Baylis, M., 2000. Culicoides biting midges: their role as arbovirus vectors, Annual Review of Entomology, 45, 307–340.

    Article  CAS  Google Scholar 

  • Ministry of Agriculture, Forestry, and Fisheries (MAFF). Data on animal hygiene. 2015a (in Japanese), http://www.maff.go.jp/j/syouan/douei/kansi_densen/kansi_densen.html Accessed on 6 Mar 2017

  • Ministry of Agriculture, Forestry, and Fisheries (MAFF). Statistics on Livestock. 2015b (in Japanese). http://www.maff.go.jp/j/tokei/kouhyou/tikusan/index.html. Accessed on 6 Mar 2017

  • Miyazato, S., Miura, Y., Hase, M., Kubo, M., Goto, Y. and Kono, Y., 1989. Encephalitis of cattle caused by Iriki isolate, a new strain belonging to Akabane virus, Nihon Juigaku Zasshi 51, 128–136

    Article  CAS  Google Scholar 

  • Moran, P.A.P., 1950. Notes on continuous stochastic phenomena, Biometrika, 37, 17–23

    Article  CAS  Google Scholar 

  • Murray, M.D., 1991. The seasonal abundance of female biting-midges, Culicoides brevitarsis. Kieffer (Diptera: Ceratopogonidae), in coastal south-eastern Australia, Australian Journal of Zoology, 39, 333–342

    Article  Google Scholar 

  • Murray, M.D., 1995. Influences of vector biology on transmission of arboviruses and outbreaks of disease: the Culicoides brevitarsis model, Veterinary Microbiology, 46, 91–99

    Article  CAS  Google Scholar 

  • Nelson, R.L. and Bellamy, R.E., 1971. Patterns of flight activity of Culicoides variipennis (Coquillett) (Diptera: Ceratopogonidae), Journal of Medical Entomology, 8, 283–291

    Article  CAS  Google Scholar 

  • Purse, B.V., Carpenter, S., Venter, G.J., Bellis, G. and Mullens, B.A., 2015. Bionomics of temperate and tropical Culicoides midges: knowledge gaps and consequences for transmission of Culicoides-borne viruses, Annual Review of Entomology, 60, 373–392

    Article  CAS  Google Scholar 

  • Tsuda, T., Yoshida, K., Ohashi, S., Yanase, T., Sueyoshi, M., Kamimura, S., Misumi, K., Hamana, K., Sakamoto, H. and Yamakawa, M., 2004. Arthrogryposis, hydranencephaly and cerebellar hypoplasia syndrome in neonatal calves resulting from intrauterine infection with Aino virus. Veterinary Research, 35, 531–538

    Article  Google Scholar 

  • Wittmann, E.J. and Baylis, M., 2000. Climate change: effects on Culicoides-transmitted viruses and implications for the UK, The Veterinary Journal, 160, 107–117

    Article  CAS  Google Scholar 

  • Wittmann, E.J., Mellor, P.S. and Baylis, M., 2001. Using climate data to map the potential distribution of Culicoides imicola (Diptera: Ceratopogonidae) in Europe, Scientific and Technical Review of the Office International des Epizooties (Paris), 20, 731–740

    Article  CAS  Google Scholar 

  • Yanase, T., Kato, T., Katagiri, Y., Aizawa, M., Nakamura, K., Kokuba, T., Araki, M., Shirafuji, H., Yamakawa, M. and Tsuda, T., 2010. Isolation and characterization of bluetongue virus from Culicoides brevitarsis (Diptera: Ceratopogonidae) in Okinawa, Medical Entomology and Zoology, 61, 85–91

    Article  Google Scholar 

  • Yanase, T., Matsumoto, Y., Matsumori, Y., Aizawa, M., Hirata, M., Kato, T., Shirafuji, H., Yamakawa, M., Tsuda, T. and Noda, H., 2013. Molecular identification of field-collected Culicoides larvae in the southern part of Japan, Journal of Medical Entomology, 50, 1105–1110

    Article  Google Scholar 

Download references

Funding information

This study was supported by the Research Project for Improving Food Safety and Animal Health of the Ministry of Agriculture, Forestry and Fisheries (Tokyo, Japan).

Author information

Authors and Affiliations

  1. Viral Disease and Epidemiology Research Division, National Institute of Animal Health, National Agriculture and Food Research Organization, 3-1-5 Kannondai, Tsukuba, Ibaraki, 305-0856, Japan

    Yoko Hayama, Takehisa Yamamoto, Sota Kobayashi, Kiyokazu Murai & Toshiyuki Tsutsui

  2. Kyushu Research Station, National Institute of Animal Health, National Agriculture and Food Research Organization, Kagoshima, Japan

    Tohru Yanase

  3. Okinawa Prefectural Institute of Animal Health, Okinawa, Japan

    Moemi Suzuki

  4. Okinawa Prefectural Hokubu Livestock Hygiene Service Center, Okinawa, Japan

    Kazuhiko Unten

  5. Okinawa Prefectural Chuo Livestock Hygiene Service Center, Okinawa, Japan

    Hisayuki Tomochi

  6. Okinawa Prefectural Miyako Livestock Hygiene Service Center, Okinawa, Japan

    Mayu Kakehi

  7. Okinawa Prefectural Yaeyama Livestock Hygiene Service Center, Okinawa, Japan

    Yukina Shono

Authors
  1. Yoko Hayama
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tohru Yanase
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Moemi Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kazuhiko Unten
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hisayuki Tomochi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mayu Kakehi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yukina Shono
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Takehisa Yamamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Sota Kobayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Kiyokazu Murai
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Toshiyuki Tsutsui
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yoko Hayama.

Ethics declarations

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

ESM 1

(PDF 67 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hayama, Y., Yanase, T., Suzuki, M. et al. Meteorological factors affecting seroconversion of Akabane disease in sentinel calves in the subtropical Okinawa Islands of Japan. Trop Anim Health Prod 50, 209–215 (2018). https://doi.org/10.1007/s11250-017-1404-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11250-017-1404-7

Keywords

Search

Navigation