Abstract
Many pathogens causing hemorrhagic fevers of medical and veterinary importance have been identified and isolated from rodents in the Republic of Korea (ROK). We investigated the occurrence of emerging viruses causing hemorrhagic fevers, such as hemorrhagic fever with renal syndrome (HFRS), severe fever with thrombocytopenia syndrome (SFTS), and flaviviruses, from wild rodents. Striped field mice, Apodemus agrarius (n = 39), were captured during 2014–2015 in the south-west of ROK. Using molecular methods, lung samples were evaluated for SFTS virus, hantavirus, and flavivirus, and seropositivity was evaluated in the blood. A high positive rate of hantavirus (46.2%) was detected in A. agrarius lungs by reverse transcription-nested polymerase chain reaction (RT-N-PCR). The monthly occurrence of hantavirus was 16.7% in October, 86.7% in November, and 25% in August of the following year (p < 0.001). Moreover, 17.9% of blood samples were serologically positive for hantavirus antibodies. The most prevalent strain in A. agrarius was Hantaan virus. All samples were positive for neither SFTS virus nor flavivirus. Hantaan virus was detected in 86.7% of A. agrarius in November (autumn), and thus, virus shedding from A. agrarius can increase the risk of humans contracting HFRS. These findings may help to predict and prevent disease outbreaks in ROK.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Amada T, Yoshimatsu K, Yasuda SP, Shimizu K, Koma T, Hayashimoto N, Gamage CD, Nishio S, Takakura A, Arikawa J (2013) Rapid, whole blood diagnostic test for detecting anti-hantavirus antibody in rats. J Virol Methods 193(1):42–49
Baek LJ, Kariwa H, Lokugamage K, Yoshimatsu K, Arikawa J, Takashima I, Kang JI, Moon SS, Chung SY, Kim EJ, Kang HJ (2006) Soochong virus: an antigenically and genetically distinct hantavirus isolated from Apodemus peninsulae in Korea. J Med Virol 78(2):290–297
Dobler G (2010) Zoonotic tick-borne flaviviruses. Vet Microbiol 140(3):221–228
Galeno H, Mora J, Villagra E, Fernandez J, Hernandez J, Mertz GJ, Ramirez E (2002) First human isolate of Hantavirus (Andes virus) in the Americas. Emerg Infect Dis 8(7):657
Goeijenbier M, Wagenaar J, Goris M, Martina B, Henttonen H, Vaheri A, Reusken C, Hartskeerl R, Osterhaus A, Van Gorp E (2013) Rodent-borne hemorrhagic fevers: under-recognized, widely spread and preventable—epidemiology, diagnostics and treatment. Crit Rev Microbiol 39(1):26–42
Heo ST, Yoo JR, Lee KH, Ko KS (2015) The first case of non-retrospective clinical identification of severe fever with thrombocytopenia syndrome patient in 2013 in South Korea. J Bacteriol Virol 45(2):155–158
Holmes EC, Zhang YZ (2015) The evolution and emergence of hantaviruses. Curr Opin Virol 10:27–33
Kim SY, Yun SM, Han MG, Lee IY, Lee NY, Jeong YE, Lee BC, Ju YR (2008) Isolation of tick-borne encephalitis viruses from wild rodents, South Korea. Vector Borne Zoonotic Dis 8(1):7–14
Kim KH, Yi J, Kim G, Choi SJ, Jun KI, Kim NH, Choe PG, Kim NJ, Lee JK, Oh MD (2013) Severe fever with thrombocytopenia syndrome, South Korea, 2012. Emerg Infect Dis 19(11):1892
Klempa B, Fichet-Calvet E, Lecompte E, Auste B, Aniskin V, Meisel H, Denys C, Koivogui L, ter Meulen J, Krüger DH (2006) Hantavirus in African wood mouse, Guinea. Emerg Infect Dis 12(5):838
Korea Centers for Disease control and Prevention (KCDC) (2015) Infectious disease surveillance Yearbook. 2015. Retrieved from. https://is.cdc.go.kr/dstat/index.jsp. Accessed Aug 2017.
Korea Centers for Disease control and Prevention (KCDC) (2016). Infectious disease surveillance Yearbook. 2016. Retrieved from http://www.cdc.go.kr/npt/biz/npp/nppMain.do. Accessed Nov 2018
Krüger DH, Ulrich R, Lundkvist Å (2001) Hantavirus infections and their prevention. Microbes Infect 3(13):1129–1144
Liu K, Cui N, Fang LQ, Wang BJ, Lu QB, Peng W, Li H, Wang LY, Liang S, Wang HY, Zhang YY (2014a) Epidemiologic features and environmental risk factors of severe fever with thrombocytopenia syndrome, Xinyang, China. PLoS Negl Trop Dis 8(5):e2820
Liu Q, He B, Huang SY, Wei F, Zhu XQ (2014b) Severe fever with thrombocytopenia syndrome, an emerging tick-borne zoonosis. Lancet Infect Dis 14(8):763–772
Marty AM, Jahrling PB, Geisbert TW (2006) Viral hemorrhagic fevers. Clin Lab Med 26(2):345–386
Meerburg BG, Singleton GR, Kijlstra A (2009) Rodent-borne diseases and their risks for public health. Crit Rev Microbiol 35(3):221–270
Moureau G, Temmam S, Gonzalez JP, Charrel RN, Grard G, De Lamballerie X (2007) A real-time RT-PCR method for the universal detection and identification of flaviviruses. Vector Borne Zoonotic Dis 7(4):467–477
Ni H, Yang F, Li Y, Liu W, Jiao S, Li Z, Yi B, Chen Y, Hou X, Hu F, Ding Y (2015) Apodemus agrarius is a potential natural host of severe fever with thrombocytopenia syndrome (SFTS)—causing novel bunyavirus. J Clin Virol 71:82–88
Niu G, Li J, Liang M, Jiang X, Jiang M, Yin H, Wang Z, Li C, Zhang Q, Jin C, Wang X (2013) Severe fever with thrombocytopenia syndrome virus among domesticated animals, China. Emerg Infect Dis 19(5):756
Patel P, Landt O, Kaiser M, Faye O, Koppe T, Lass U, Sall AA, Niedrig M (2013) Development of one-step quantitative reverse transcription PCR for the rapid detection of flaviviruses. Virol J 10(1):58
Ryou J, Lee HI, Yoo YJ, Noh YT, Yun SM, Kim SY, Shin EH, Han MG, Ju YR (2011) Prevalence of hantavirus infection in wild rodents from five provinces in Korea, 2007. J Wildl Dis 47(2):427–432
Song JW, Baek LJ, Schmaljohn CS, Yanagihara R (2007a) Thottapalayam virus, a prototype shrewborne Hantavirus. Emerg Infect Dis 13(7):980
Song KJ, Baek LJ, Moon S, Ha SJ, Kim SH, Park KS, Klein TA, Sames W, Kim HC, Lee JS, Yanagihara R (2007b) Muju virus, a novel Hantavirus harboured by the arvicolid rodent Myodes regulus in Korea. J Gen Virol 88(11):3121–3129
Song JW, Hae JK, Se HG, Sung SM, Bennett SN, Song KJ, Luck JB, Kim HC, O’Guinn ML, Chong ST, Klein TA, Yanagihara R (2009) Characterization of Imjin virus, a newly isolated hantavirus from the Ussuri white-toothed shrew (Crocidura lasiura). J Virol 83(12):6184–6191
Viel JF, Lefebvre A, Marianneau P, Joly D, Giraudoux P, Upegui E, Tordo N, Hoen B (2011) Environmental risk factors for haemorrhagic fever with renal syndrome in a French new epidemic area. Epidemiol Infect 139(6):867–874
Wu T, Guo XL, Peng HY, Chen YI, Zhao KCC, Cui LB, Ge Y, Shi ZY, Qi X, Liu DP (2013) Isolation and analysis of genomic sequences of SFTS virus from goat and tick attached to its surface. Jiangsu J of Prey Med 24:7–10
Yun SM, Lee YJ, Choi W, Kim HC, Chong ST, Chang KS, Coburn JM, Klein TA, Lee WJ (2016) Molecular detection of severe fever with thrombocytopenia syndrome and tick-borne encephalitis viruses in ixodid ticks collected from vegetation, Republic of Korea, 2014. Ticks Tick Borne Dis 7(5):970–978
Funding source
This research was supported by a grant from the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI), funded by the Ministry of Health & Welfare, Republic of Korea (grant number: HI15C2891).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflicts of interest to declare.
Statements of compliance
This study was approved from institutional review board (IRB) of Chosun University. All animals were used according to an approved animal use protocol from Chosun University Institutional Animal Care and Use Committee (CIACUC).
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Jalal, S., Jha, B., Kim, CM. et al. Molecular detection of viruses causing hemorrhagic fevers in rodents in the south-west of Korea. J. Neurovirol. 25, 239–247 (2019). https://doi.org/10.1007/s13365-018-0708-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13365-018-0708-3