• 1.

    Ladner JT et al. 2015. Evolution and spread of Ebola virus in Liberia, 2014–2015. Cell Host Microbe 18: 659669.

  • 2.

    Korea Centers for Disease Control and Prevention, 2015. Middle east respiratory syndrome coronavirus outbreak in the Republic of Korea, 2015. Osong Public Health Res Perspect 6: 269278.

    • Search Google Scholar
    • Export Citation
  • 3.

    Faria NR et al. 2016. Zika virus in the Americas: early epidemiological and genetic findings. Science 352: 345349.

  • 4.

    Fill MA et al. 2017. Notes from the field: multiple cases of Seoul virus infection in a household with infected pet rats—Tennessee, December 2016–April 2017. MMWR Morb Mortal Wkly Rep 66: 10811082.

    • Search Google Scholar
    • Export Citation
  • 5.

    Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P, 2008. Global trends in emerging infectious diseases. Nature 451: 990993.

  • 6.

    Karesh WB et al. 2012. Ecology of zoonoses: natural and unnatural histories. Lancet 380: 19361945.

  • 7.

    Meerburg BG, Singleton GR, Kijlstra A, 2009. Rodent-borne diseases and their risks for public health. Crit Rev Microbiol 35: 221270.

  • 8.

    Lee HW, Lee PW, Johnson KM, 1978. Isolation of the etiologic agent of Korean hemorrhagic fever. J Infect Dis 190: 17111721.

  • 9.

    Taylor AJ, Paris DH, Newton PN, 2015. A systematic review of mortality from untreated scrub typhus (Orientia tsutsugamushi). PLoS Negl Trop Dis 9: e0003971.

    • Search Google Scholar
    • Export Citation
  • 10.

    Chae JS, Kim CM, Kim EH, Hur EJ, Klein TA, Kang TK, Lee HC, Song JW, 2003. Molecular epidemiological study for tick-borne disease (Ehrlichia and Anaplasma spp.) surveillance at selected U.S. military training sites/installations in Korea. Ann NY Acad Sci 990: 118125.

    • Search Google Scholar
    • Export Citation
  • 11.

    Kim CM et al. 2005. Detection of Bartonella species from ticks, mites and small mammals in Korea. J Vet Sci 6: 327334.

  • 12.

    Firth C et al. 2014. Detection of zoonotic pathogens and characterization of novel viruses carried by commensal Rattus norvegicus in New York City. MBio 5: e01933e14.

    • Search Google Scholar
    • Export Citation
  • 13.

    Lee HW, Baek LJ, Johnson KM, 1982. Isolation of Hantaan virus, the etiologic agent of Korean hemorrhagic fever, from wild urban rats. J Infect Dis 146: 638644.

    • Search Google Scholar
    • Export Citation
  • 14.

    Lee HW, Johnson KM, 1982. Laboratory-acquired infections with Hantaan virus, the etiologic agent of Korean hemorrhagic fever. J Infect Dis 146: 645651.

    • Search Google Scholar
    • Export Citation
  • 15.

    Vaheri A, Strandin T, Hepojoki J, Sironen T, Henttonen H, Makela S, Mustonen J, 2013. Uncovering the mysteries of hantavirus infections. Nat Rev Microbiol 11: 539550.

    • Search Google Scholar
    • Export Citation
  • 16.

    Kim YS, Ahn C, Han JS, Kim S, Lee JS, Lee PW, 1995. Hemorrhagic fever with renal syndrome caused by the Seoul virus. Nephron 71: 419427.

  • 17.

    Klempa B, 2009. Hantaviruses and climate change. Clin Microbiol Infect 15: 518523.

  • 18.

    Yan L, Fang LQ, Huang HG, Zhang LQ, Feng D, Zhao WJ, Zhang WY, Li XW, Cao WC, 2007. Landscape elements and Hantaan virus-related hemorrhagic fever with renal syndrome, People’s Republic of China. Emerg Infect Dis 13: 13011306.

    • Search Google Scholar
    • Export Citation
  • 19.

    Gracia JR, Schumann B, Seidler A, 2015. Climate variability and the occurrence of human puumala hantavirus infections in Europe: a systematic review. Zoonoses Public Health 62: 465478.

    • Search Google Scholar
    • Export Citation
  • 20.

    Schwarz AC, Ranft U, Piechotowski I, Childs JE, Brockmann SO, 2009. Risk factors for human infection with Puumala virus, southwestern Germany. Emerg Infect Dis 15: 10321039.

    • Search Google Scholar
    • Export Citation
  • 21.

    Madsen T, Shine R, 1999. Rainfall and rats: climatically-driven dynamics of a tropical rodent population. Aust J Ecol 24: 8089.

  • 22.

    Engelthaler DM et al. 1999. Climatic and environmental patterns associated with hantavirus pulmonary syndrome, Four Corners region, United States. Emerg Infect Dis 5: 8794.

    • Search Google Scholar
    • Export Citation
  • 23.

    Hjelle B, Glass GE, 2000. Outbreak of hantavirus infection in the Four Corners region of the United States in the wake of the 1997–1998 El Nino-southern oscillation. J Infect Dis 181: 15691573.

    • Search Google Scholar
    • Export Citation
  • 24.

    Pettersson L, Boman J, Juto P, Evander M, Ahlm C, 2008. Outbreak of Puumala virus infection, Sweden. Emerg Infect Dis 14: 808810.

  • 25.

    Tersago K, Verhagen R, Servais A, Heyman P, Ducoffre G, Leirs H, 2009. Hantavirus disease (nephropathia epidemica) in Belgium: effects of tree seed production and climate. Epidemiol Infect 137: 250256.

    • Search Google Scholar
    • Export Citation
  • 26.

    Hornfeldt B, Hipkiss T, Eklund U, 2005. Fading out of vole and predator cycles? Proc Biol Sci 272: 20452049.

  • 27.

    Bi P, Tong S, Donald K, Parton K, Ni J, 2002. Climatic, reservoir and occupational variables and the transmission of haemorrhagic fever with renal syndrome in China. Int J Epidemiol 31: 189193.

    • Search Google Scholar
    • Export Citation
  • 28.

    Zhang WY et al. 2010. Climate variability and hemorrhagic fever with renal syndrome transmission in northeastern China. Environ Health Perspect 118: 915920.

    • Search Google Scholar
    • Export Citation
  • 29.

    Zhang WY et al. 2009. Predicting the risk of hantavirus infection in Beijing, People’s Republic of China. Am J Trop Med Hyg 80: 678683.

  • 30.

    Haredasht SA et al. 2013. Model-based prediction of nephropathia epidemica outbreaks based on climatological and vegetation data and bank vole population dynamics. Zoonoses Public Health 60: 461477.

    • Search Google Scholar
    • Export Citation
  • 31.

    Song JW et al. 2009. Characterization of Imjin virus, a newly isolated hantavirus from the Ussuri white-toothed shrew (Crocidura lasiura). J Virol 83: 61846191.

    • Search Google Scholar
    • Export Citation
  • 32.

    Edgar RC, 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 17921797.

  • 33.

    Tamura K, Stecher G, Peterson D, Filipski A, Kumar S, 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30: 27252729.

    • Search Google Scholar
    • Export Citation
  • 34.

    Song KJ, Luck Ju B, Yong Ju L, 1994. Sequence analysis and mutation rate of Hantaan virus in the natural condition. J Korean Soc Microbiol 29: 675683.

    • Search Google Scholar
    • Export Citation
  • 35.

    Lee HW, Chu YK, Kang BN, 1986. Isolation of Hantaan-like virus from wild urban rats in Incheon. J Korean Soc Virol 16: 99104.

  • 36.

    Lee HW, Chu YK, Koo IH, 1986. Seroepidemiologic survey of Hantaan virus infection among USArmy soldiers stationed in Korea and wild rats captured at the USArmy installations in Seoul. J Korean Soc Virol 16: 105111.

    • Search Google Scholar
    • Export Citation
  • 37.

    Bi P, Wu X, Zhang F, Parton KA, Tong S, 1998. Seasonal rainfall variability, the incidence of hemorrhagic fever with renal syndrome, and prediction of the disease in low-lying areas of China. Am J Epidemiol 148: 276281.

    • Search Google Scholar
    • Export Citation
  • 38.

    Fang LQ et al. 2010. Spatiotemporal trends and climatic factors of hemorrhagic fever with renal syndrome epidemic in Shandong Province, China. PLoS Negl Trop Dis 4: e789.

    • Search Google Scholar
    • Export Citation
  • 39.

    Li CP et al. 2013. Association between hemorrhagic fever with renal syndrome epidemic and climate factors in Heilongjiang Province, China. Am J Trop Med Hyg 89: 10061012.

    • Search Google Scholar
    • Export Citation
  • 40.

    Song DH et al. 2017. Sequence-independent, single-primer amplification next-generation sequencing of Hantaan virus cell culture-based isolates. Am J Trop Med Hyg 96: 389394.

    • Search Google Scholar
    • Export Citation
  • 41.

    Klempa B, Witkowski PT, Popugaeva E, Auste B, Koivogui L, Fichet-Calvet E, Strecker T, Ter Meulen J, Kruger DH, 2012. Sangassou virus, the first hantavirus isolate from Africa, displays genetic and functional properties distinct from those of other murinae-associated hantaviruses. J Virol 86: 38193827.

    • Search Google Scholar
    • Export Citation
  • 42.

    Kim HC, Chong ST, Collier BW, Yi SC, Song KJ, Baek LJ, Song J-W, 2007. Seroepidemiological survey of rodents collected at a U.S. military installation, Yongsan Garrison, Seoul, Republic of Korea. Mil Med 172: 759764.

    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 3 3 3
Full Text Views 1501 203 2
PDF Downloads 135 44 3
 
 
 
 
 
 
 
 
 
 
 

Urban Rodent Surveillance, Climatic Association, and Genomic Characterization of Seoul Virus Collected at U.S. Army Garrison, Seoul, Republic of Korea, 2006–2010

Heung-Chul KimMedical Command Activity-Korea, 65th Medical Brigade, Unit 15281, APO AP 96271-5281;

Search for other papers by Heung-Chul Kim in
Current site
Google Scholar
PubMed
Close
,
Won-Keun KimDepartment of Microbiology, College of Medicine, Korea University, Seoul, Republic of Korea;

Search for other papers by Won-Keun Kim in
Current site
Google Scholar
PubMed
Close
,
Jin Sun NoDepartment of Microbiology, College of Medicine, Korea University, Seoul, Republic of Korea;

Search for other papers by Jin Sun No in
Current site
Google Scholar
PubMed
Close
,
Seung-Ho LeeDepartment of Microbiology, College of Medicine, Korea University, Seoul, Republic of Korea;

Search for other papers by Seung-Ho Lee in
Current site
Google Scholar
PubMed
Close
,
Se Hun Gu5th R&D Institute, Agency for Defense Development, Daejeon, Republic of Korea

Search for other papers by Se Hun Gu in
Current site
Google Scholar
PubMed
Close
,
Sung-Tae ChongMedical Command Activity-Korea, 65th Medical Brigade, Unit 15281, APO AP 96271-5281;

Search for other papers by Sung-Tae Chong in
Current site
Google Scholar
PubMed
Close
,
Terry A. KleinMedical Command Activity-Korea, 65th Medical Brigade, Unit 15281, APO AP 96271-5281;

Search for other papers by Terry A. Klein in
Current site
Google Scholar
PubMed
Close
, and
Jin-Won SongDepartment of Microbiology, College of Medicine, Korea University, Seoul, Republic of Korea;

Search for other papers by Jin-Won Song in
Current site
Google Scholar
PubMed
Close
View More View Less
Restricted access

Rodent-borne pathogens pose a critical public health threat in urban areas. An epidemiological survey of urban rodents was conducted from 2006 to 2010 at the U.S. Army Garrison (USAG), Seoul, Republic of Korea (ROK), to determine the prevalence of Seoul virus (SEOV), a rodent-borne hantavirus. A total of 1,950 rodents were captured at USAG, Yongsan, near/in 19.4% (234/1,206) of the numbered buildings. Annual mean rodent infestation rates were the highest for food service facilities, e.g., the Dragon Hill Lodge complex (38.0 rodents) and the Hartell House (18.8 rodents). The brown rat, Rattus norvegicus, accounted for 99.4% (1,939/1,950) of all the rodents captured in the urban area, whereas only 0.6% (11/1,950) of the rodents was house mice (Mus musculus). In November 2006, higher numbers of rats captured were likely associated with climatic factors, e.g., rainfall and temperatures as rats sought harborage in and around buildings. Only 4.7% (34/718) of the rodents assayed for hantaviruses was serologically positive for SEOV. A total of 8.8% (3/34) R. norvegicus were positive for SEOV RNA by reverse transcription polymerase chain reaction, of which two SEOV strains were completely sequenced and characterized. The 3′ and 5′ terminal sequences revealed incomplete complementary genomic configuration. Seoul virus strains Rn10-134 and Rn10-145 formed a monophyletic lineage with the prototype SEOV strain 80-39. Seoul virus Medium segment showed the highest evolutionary rates compared with the Large and Small segments. In conclusion, this report provides significant insights into continued rodent-borne disease surveillance programs that identify hantaviruses for analysis of disease risk assessments and development of mitigation strategies.

Author Notes

Address correspondence to Jin-Won Song, Department of Microbiology, College of Medicine, Korea University, 3 Incheon-ro, Seongbuk-gu, Seoul 02841, Republic of Korea. E-mail: jwsong@korea.ac.kr

Financial support: Funding for portions of this work was provided by the AFHSB-GEIS and a grant from the ADD (UD160022ID). This research was also supported by Research Program To Solve Social Issues of the National Research Foundation of Korea (NRF) funded by the Ministry of Science and ICT (NRF-2017M3A9E4061992).

Ethical approval: All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

Authors’ addresses: Heung-Chul Kim, Sung-Tae Chong, and Terry A. Klein, Medical Command Activity-Korea, 65th Medical Brigade, Unit 15281, E-mails: hungchol.kim2.ln@mail.mil, sungtae.chong.ln@mail.mil, and terry.a.klein2.civ@mail.mil. Won-Keun Kim, Jin Sun No, Seung-Ho Lee, and Jin-Won Song, Department of Microbiology, College of Medicine, Korea University, Seoul, Republic of Korea, E-mails: wkkim1061@korea.ac.kr, dybono@korea.ac.kr, leeds1104@korea.ac.kr, and jwsong@korea.ac.kr. Se Hun Gu, 5th R&D Institute, Agency for Defense Development, Daejeon, Republic of Korea, E-mails: sehungu@add.re.kr.

These authors contributed equally to this study.

Save