Epidemiological Assessment of Risk Factors Associated with Bovine Ephemeral Fever Virus Exposure among Sheep and Goats in South Korea

Jeong-Min Hwang, Yun Ji Ga, Jung-Yong Yeh

Abstract


Background: Bovine ephemeral fever virus (BEFV) is an arthropod-borne virus classified as a type species of the genus Ephemerovirus, family Rhabdoviridae. BEFV is the causative agent of bovine ephemeral fever (BEF), a non-contagious disease of acute febrile clinical signs in cattle and water buffalo. Some species might act as reservoir hosts, and antibodies to BEFV have also been found in asymptomatic sheep, goats, pigs, and many wild animals. This study aimed to conduct a retrospective cross-sectional serological screening in South Korea to address BEFV seroprevalence and identify risk factors for becoming seropositive for the virus in sheep and goats. 

Materials, Methods & Results: The apparent prevalence rates were considered to be the animal-level prevalence, defined as the proportion of serum neutralization test (SNT)-positive animals out of the total number of animals tested in the study area, and flock prevalence was defined as the proportion of SNT-positive flocks out of the total number of tested flocks in the area. A flock was classified as positive if at least one animal was SNT-positive. At the national level in 2011, 28 of 177 flocks (15.8%; 95% CI, 11.2−21.9%) and 71 of 498 heads (14.3%, 95% CI: 11.5-17.6%) that were analyzed showed serum neutralizing antibodies against BEFV. Our results revealed that age class, vector control, and geographic location affected seroprevalence to differing extents. In the univariate analysis, older age was a significant risk factor (OR, 2.327; 95% CI, 1.147-4.721; P = 0.017 in adults). The management risk factor attributes showed that preventive measures, such as routine application of insecticides in farms, decreased the odds of seropositivity for BEFV (OR, 0.514; 95% CI, 0.267-0.991; P = 0.044). Vector control was a significant protective factor, while animal species, flock size, and flock structure were not significantly associated. Differences in seroprevalence between variations in the presence of ruminant farms, lakes, or rice paddies within a 1-km radius or type of land use were not statistically significant (P > 0.05). We observed a significant difference in the individual likelihood of being positive in the southern provinces with respect to that in the northern provinces (OR, 2.166; 95% CI, 1.228-3.824; P = 0.007). Differences in seroprevalence between variations in the eastern and western regions were not statistically significant (P > 0.05). The retrospective study results showed that the virus was widely distributed in sheep and goats in South Korea, with seropositive rates ranging from 7.8% to 19.7% between 2003 and 2008.

Discussion: This is the first report of circulating antibodies against BEFV in sheep and goats in South Korea. The serological prevalence of BEFV infection in sheep and goats was significantly different between different age cohorts, vector control, and geographical locations: it was higher in the older group and the southern and western regions of South Korea. Determination of seropositivity rates often leads to an understanding of virus circulation dynamics and is useful in the formulation of disease control measures. Our results demonstrated that vector control was a significant protective factor; therefore, the summer control of vectors could be better implemented in provinces with elevated seropositivity rates. The results of this seroprevalence study may serve as a basis for future epidemiological studies on BEFV infection in South Korea.



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References


Abu-Elzein E.M., Al-Afaleq A.I., Housawi F.M. & Al-Basheir A.M. 2006. A study on bovine ephemeral fever involving sentinel herds and serosurveillance in Saudi Arabia. Revue Scientifique et Technique. 25(3): 1147-1151.

Akakpo A.J. 2015. Three-day fever. Revue Scientifique et Technique. 34(2): 533-538, 525-532.

Almasi S. & Bakhshesh M. 2019. Antigenic variation of bovine ephemeral fever viruses isolated in Iran, 2012-2013. Virus Genes. 55(5): 654-659. DOI: 10.1007/s11262-019-01688-6

Aziz-Boaron O., Brettschneider S., King R., Gelman B. & Klement E. 2015. Seroprevalence of bovine ephemeral fever virus in domesticated and wildlife species during epidemic and inter-epidemic periods (2000-2009) in Israel. Transboundary and Emerging Diseases. 62(2): 183-187. DOI: 10.1111/tbed.12104

Bakhshesh M. & Abdollahi D. 2015. Bovine Ephemeral Fever in Iran: Diagnosis, Isolation and Molecular Characterization. Journal of Arthropod-Borne Diseases. 9(2): 195-203.

Chaisirirat T., Sangthong P., Arunvipas P., Petcharat N., Thangthamniyom N., Chumsing W. & Lekcharoensuk P. 2018. Molecular characterization of bovine ephemeral fever virus in Thailand between 2013 and 2017. Veterinary Microbiology. 227: 1-7. DOI: 10.1016/j.vetmic.2018.10.013

Cybinski D.H. & Zakrzewski H. 1983. The isolation and preliminary characterization of a rhabdovirus in Australia related to bovine ephemeral fever virus. Veterinary Microbiology. 8(3): 221-235. DOI: 10.1016/0378-1135(83)90075-5

Davies F.G., Shaw T. & Ochieng P. 1975. Observations on the epidemiology of ephemeral fever in Kenya. Journal of Hygiene. 75(2): 231-235. DOI: 10.1017/s0022172400047264

Dik B., Muz D., Muz M.N. & Uslu U. 2014. The geographical distribution and first molecular analysis of Culicoides Latreille (Diptera: Ceratopogonidae) species in the Southern and Southeastern Turkey during the 2012 outbreak of bovine ephemeral fever. Parasitology Research. 113(11): 4225-4232. DOI: 10.1007/s00436-014-4098-z

Doherty R.L., Carley J.G., Standfast H.A., Dyce A.L. & Snowdon W.A. 1972. Virus strains isolated from arthropods during an epizootic of bovine ephemeral fever in Queensland. Australian Veterinary Journal. 48(3): 81-86. DOI: 10.1111/j.1751-0813.1972.tb02220.x

Dorey-Robinson D.L.W., Fernandez de Marco M., Hernandez-Triana L.M., Folly A.J., McElhinney L.M., Stokes J.E., Sanders C., Carpenter S., Fooks A.R., Zalesky O., Gelman B., Erster O. & Johnson N. 2019. Complete Genome Sequence of a Bovine Ephemeral Fever Virus Isolate from Israel. Microbiology Resource Announcements. 8(41): DOI: 10.1128/MRA.00822-19

English A.W. 1982. Serological survey of wild fallow deer (Dama dama) in New South Wales, Australia. The Veterinary Record. 110(7): 153-154. DOI: 10.1136/vr.110.7.153

Farag M.A., al-Sukayran A., Mazloum K.S. & al-Bukomy A.M. 1998. Epizootics of bovine ephemeral fever on dairy farms in Saudi Arabia. Revue Scientifique et Technique. 17(3): 713-722. DOI: 10.20506/rst.17.3.1127

Finlaison D.S., Read A.J. & Kirkland P.D. 2010. An epizootic of bovine ephemeral fever in New South Wales in 2008 associated with long-distance dispersal of vectors. Australian Veterinary Journal. 88(8): 301-306. DOI: 10.1111/j.1751-0813.2010.00596.x

Finlaison D.S., Read A.J., Zhang J., Paskin R. & Kirkland P.D. 2014. Application of a real-time polymerase chain reaction assay to the diagnosis of bovine ephemeral fever during an outbreak in New South Wales and northern Victoria in 2009-10. Australian Veterinary Journal. 92(1-2): 24-27. DOI: 10.1111/avj.12139

Gao S., Du J., Tian Z., Niu Q., Zheng F., Huang D., Kang B., Luo J., Liu G. & Yin H. 2017. Complete genome sequence of a bovine ephemeral fever virus JT02L strain in mainland China. Archives of Virology. 162(11): 3555-3558. DOI: 10.1007/s00705-017-3520-0

Geoghegan J.L., Walker P.J., Duchemin J.B., Jeanne I. & Holmes E.C. 2014. Seasonal drivers of the epidemiology of arthropod-borne viruses in Australia. PLOS Neglected Tropical Diseases. 8(11): e3325. DOI: 10.1371/journal.pntd.0003325

Hall W.T., Daddow K.N., Dimmock C.K., George T.D. & Standfast H.A. 1975. The infection of merino sheep with bovine ephemeral fever virus. Australian Veterinary Journal. 51(7): 344-346. DOI: 10.1111/j.1751-0813.1975.tb15943.x

Hayama Y., Moriguchi S., Yanase T., Suzuki M., Niwa T., Ikemiyagi K., Nitta Y., Yamamoto T., Kobayashi S., Murai K. & Tsutsui T. 2016. Epidemiological analysis of bovine ephemeral fever in 2012-2013 in the subtropical islands of Japan. BMC Veterinary Research. 12(47). DOI: 10.1186/s12917-016-0673-0

Hijazeen Z.S., Ismail Z.B. & Al-Majali A. 2020. Prevalence and risk factors of some arthropod-transmitted diseases in cattle and sheep in Jordan. Veterinary World. 13(1): 201-205. DOI: 10.14202/vetworld.2020.201-205

Hsieh Y.C., Chen S.H., Chou C.C., Ting L.J., Itakura C. & Wang F.I. 2005. Bovine ephemeral fever in Taiwan (2001-2002). Journal of Veterinary Medical Science. 67(4): 411-416. DOI: 10.1292/jvms.67.411

Huaman J.L., Pacioni C., Forsyth D.M., Pople A., Hampton J.O., Carvalho T.G. & Helbig K.J. 2020. Serosurveillance and Molecular Investigation of Wild Deer in Australia Reveals Seroprevalence of Pestivirus Infection. Viruses. 12(7): 10.3390/v12070752

Humphry R.W., Cameron A. & Gunn G.J. 2004. A practical approach to calculate sample size for herd prevalence surveys. Preventive Veterinary Medicine. 65(3-4): 173-188. DOI: 10.1016/j.prevetmed.2004.07.003

Kato T., Yanase T., Suzuki M., Katagiri Y., Ikemiyagi K., Takayoshi K., Shirafuji H., Ohashi S., Yoshida K., Yamakawa M. & Tsuda T. 2016. Monitoring for bovine arboviruses in the most southwestern islands in Japan between 1994 and 2014. BMC Veterinary Research. 12(1): 125. DOI: 10.1186/s12917-016-0747-z

Kim Y.H., Kweon C.H., Tark D.S., Lim S.I., Yang D.K., Hyun B.H., Song J.Y., Hur W. & Park S.C. 2011. Development of inactivated trivalent vaccine for the teratogenic Aino, Akabane and Chuzan viruses. Biologicals. 39(3): 152-157. 10.1016/j.biologicals.2011.02.004

Kim Y.H., Oem J.K., Lee E.Y., Lee K.K., Kim S.H., Lee M.H. & Park S.C. 2015. Seroprevalence of five arboviruses in sentinel cattle as part of nationwide surveillance in South Korea, 2009-2012. Journal of Veterinary Medical Science. 77(2): 247-250. DOI: 10.1292/jvms.14-0163

Kun J., Rongrong J., Xiangbin W., Yan Z., Yiping D., Gang L., Pei Z. & Shoujun L. 2020. Genetic characterization of bovine ephemeral fever virus in southern China, 2013-2017. Virus Genes. 56(3): 390-395. DOI: 10.1007/s11262-020-01740-w

Lapira J.E.E., Balbin M.M., Belotindos L.P., Viloria V.V., Abes N.S. & Mingala C.N. 2018. Molecular detection of ephemeral fever virus among large ruminants in the Philippines. VirusDisease. 29(3): 400-404. DOI: 10.1007/s13337-018-0468-y

Lee F. 2019. Bovine Ephemeral Fever in Asia: Recent Status and Research Gaps. Viruses. 11(5): 412. DOI: 10.3390/v11050412

Li Z., Zheng F., Gao S., Wang S., Wang J., Liu Z., Du J. & Yin H. 2015. Large-scale serological survey of bovine ephemeral fever in China. Veterinary Microbiology. 176(1-2): 155-160. DOI: 10.1016/j.vetmic.2014.12.008

Liao Y.K., Inaba Y., Li N.J., Chain C.Y., Lee S.L. & Liou P.P. 1998. Epidemiology of bovine ephemeral fever virus infection in Taiwan. Microbiological Research. 153(3): 289-295. DOI: 10.1016/S0944-5013(98)80014-1

Lim S.I., Kweon C.H., Tark D.S., Kim S.H. & Yang D.K. 2007. Sero-survey on Aino, Akabane, Chuzan, bovine ephemeral fever and Japanese encephalitis virus of cattle and swine in Korea. Journal of Veterinary Science. 8(1): 45-49. DOI: 10.4142/jvs.2007.8.1.45

Lim S.I., Kweon C.H., Yang D.K., Tark D.S. & Kweon J.H. 2005. Apoptosis in Vero cells infected with Akabane, Aino and Chuzan virus. Journal of Veterinary Science. 6(3): 251-254.

Liu D., Li K., Zhang L., Lan Y., Wang X., Zhang H., Wang L., Gui R., Han Z., Jang W., Sizhu S. & Li J. 2017. Seroprevalence investigation of bovine ephemeral fever in yaks in Tibetan Plateau of China from 2012 to 2015. Tropical Animal Health and Production. 49(1): 227-230. DOI: 10.1007/s11250-016-1172-9

Nandi S. & Negi B.S. 1999. Bovine ephemeral fever: a review. Comparative Immunology, Microbiology and Infectious Diseases. 22(2): 81-91. DOI: 10.1016/s0147-9571(98)00027-7

Oguzoglu T.C., Erturk A., Cizmeci S.G., Koc B.T. & Akca Y. 2015. A Report on Bovine Ephemeral Fever Virus in Turkey: Antigenic Variations of Different Strains of EFV in the 1985 and 2012 Outbreaks Using Partial Glycoprotein Gene Sequences. Transboundary and Emerging Diseases. 62(5): e66-70. DOI: 10.1111/tbed.12187

Omar R., Van Schalkwyk A., Carulei O., Heath L., Douglass N. & Williamson A.L. 2020. South African bovine ephemeral fever virus glycoprotein sequences are phylogenetically distinct from those from the rest of the world. Archives of Virology. 165(5): 1207-1210. DOI: 10.1007/s00705-020-04568-9

Pyasi S., Sahu B.P., Sahoo P., Dubey P.K., Sahoo N., Byrareddy S.N. & Nayak D. 2020. Identification and phylogenetic characterization of bovine ephemeral fever virus (BEFV) of Middle Eastern lineage associated with 2018-2019 outbreaks in India. Transboundary and Emerging Diseases. DOI: 10.1111/tbed.13531

Reiczigel J., Foldi J. & Ozsvari L. 2010. Exact confidence limits for prevalence of a disease with an imperfect diagnostic test. Epidemiology and Infection. 138(11): 1674-1678. DOI: 10.1017/S0950268810000385

Sanders C.J., Harrup L.E., Tugwell L.A., Brugman V.A., England M. & Carpenter S. 2017. Quantification of within- and between-farm dispersal of Culicoides biting midges using an immunomarking technique. Journal of Applied Ecology. 54(5): 1429-1439. DOI: 10.1111/1365-2664.12875

St. George T.D. 1988. Bovine ephemeral fever: a review. Tropical Animal Health and Production. 20(4): 194-202. DOI: 10.1007/BF02239980

Tonbak S., Berber E., Yoruk M.D., Azkur A.K., Pestil Z. & Bulut H. 2013. A large-scale outbreak of bovine ephemeral fever in Turkey, 2012. Journal of Veterinary Medical Science. 75(11): 1511-1514. DOI: 10.1292/jvms.13-0085

Walker P.J. & Klement E. 2015. Epidemiology and control of bovine ephemeral fever. Veterinary Research. 46:124. DOI: 10.1186/s13567-015-0262-4

Wang F.I., Hsu A.M. & Huang K.J. 2001. Bovine ephemeral fever in Taiwan. Journal of Veterinary Diagnostic Investigation. 13(6): 462-467. DOI: 10.1177/104063870101300602

Yanase T., Murota K. & Hayama Y. 2020. Endemic and Emerging Arboviruses in Domestic Ruminants in East Asia. Frontiers in Veterinary Science. 7: 168. DOI: 10.3389/fvets.2020.00168

Yang D.K., Hwang I.J., Kim B.H., Kweon C.H., Lee K.W., Kang M.I., Lee C.S. & Cho K.O. 2008. Serosurveillance of viral diseases in Korean native goats (Capra hircus). Journal of Veterinary Medical Science. 70(9): 977-979. DOI: 10.1292/jvms.70.977

Yeruham I., Van Ham M., Stram Y., Friedgut O., Yadin H., Mumcuoglu K.Y. & Braverman Y. 2010. Epidemiological investigation of bovine ephemeral Fever outbreaks in Israel. Veterinary Medicine International. 2010: 290541. DOI: 10.4061/2010/290541

Yeruham I., Yadin H., Abramovitch I. & Shama Z. 2005. Bovine ephemeral fever in a dairy cattle herd in the Jordan Valley. The Veterinary Record. 156(9): 284-286. DOI: 10.1136/vr.156.9.284

Zaghawa A., Housawi F.M., Al-Naeem A., Al-Nakhly H., Kamr A. & Toribio R. 2016. Risk analysis and seroprevalence of bovine ephemeral fever virus in cattle in the Kingdom of Saudi Arabia. Tropical Animal Health and Production. 48(3): 487-492. DOI: 10.1007/s11250-015-0978-1

Zaghawa A.A., Housawi F., Al-Naeem A., Elsify A. & Hegazy Y.M. 2017. Bovine ephemeral fever epidemics in Kingdom Saudi Arabia: clinical, epidemiological and molecular investigation. Journal of Infection in Developing Countries. 11(11): 854-860. DOI: 10.3855/jidc.8201




DOI: https://doi.org/10.22456/1679-9216.111679

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