Molecular Detection of Anaplasma, Bartonella, and Borrelia theileri in Raccoon Dogs (Nyctereutes procyonoides) in Korea

Jun-Gu Kang Laboratory of Veterinary Internal Medicine, Research Institute BK21 Program for Veterinary Science and College of Veterinary Medicine, Seoul National University, Seoul, Korea;

Search for other papers by Jun-Gu Kang in
Current site
Google Scholar
PubMed
Close
,
Jeong-Byoung Chae Laboratory of Veterinary Internal Medicine, Research Institute BK21 Program for Veterinary Science and College of Veterinary Medicine, Seoul National University, Seoul, Korea;

Search for other papers by Jeong-Byoung Chae in
Current site
Google Scholar
PubMed
Close
,
Yoon-Kyoung Cho Laboratory of Veterinary Internal Medicine, Research Institute BK21 Program for Veterinary Science and College of Veterinary Medicine, Seoul National University, Seoul, Korea;

Search for other papers by Yoon-Kyoung Cho in
Current site
Google Scholar
PubMed
Close
,
Young-Sun Jo Laboratory of Veterinary Internal Medicine, Research Institute BK21 Program for Veterinary Science and College of Veterinary Medicine, Seoul National University, Seoul, Korea;

Search for other papers by Young-Sun Jo in
Current site
Google Scholar
PubMed
Close
,
Nam-Shik Shin Laboratory of Zoo and Wildlife Medicine, Research Institute and BK21 Program for Veterinary Science and College of Veterinary Medicine, Seoul National University, Seoul, Korea;

Search for other papers by Nam-Shik Shin in
Current site
Google Scholar
PubMed
Close
,
Hang Lee College of Veterinary Medicine, Seoul National University, Seoul, Korea;

Search for other papers by Hang Lee in
Current site
Google Scholar
PubMed
Close
,
Kyoung-Seong Choi College of Ecology and Environmental Science, Kyungpook National University, Sangju, Korea;

Search for other papers by Kyoung-Seong Choi in
Current site
Google Scholar
PubMed
Close
,
Do-Hyeon Yu Institute of Animal Medicine, College of Veterinary Medicine, Gyeongsang National University, Jinju, Korea;

Search for other papers by Do-Hyeon Yu in
Current site
Google Scholar
PubMed
Close
,
Jinho Park College of Veterinary Medicine, Chonbuk National University, Iksan, Korea;

Search for other papers by Jinho Park in
Current site
Google Scholar
PubMed
Close
,
Bae-Keun Park Research Institute of Veterinary Medicine and College of Veterinary Medicine, Chungnam National University, Daejeon, Korea

Search for other papers by Bae-Keun Park in
Current site
Google Scholar
PubMed
Close
, and
Joon-Seok Chae Laboratory of Veterinary Internal Medicine, Research Institute BK21 Program for Veterinary Science and College of Veterinary Medicine, Seoul National University, Seoul, Korea;

Search for other papers by Joon-Seok Chae in
Current site
Google Scholar
PubMed
Close
Restricted access

Anaplasmosis, cat-scratch disease, and Lyme disease are emerging vector-borne infectious diseases in Korea. Although the prevalence of vector-borne pathogens (VBPs) in domestic animals and vector arthropods has been documented, there is limited information on the presence of VBPs in wild animals. The raccoon dog (Nyctereutes procyonoides), a wild canid found in East Asia and Europe, represents a potential wildlife reservoir for zoonotic diseases. To investigate the prevalence of VBPs in raccoon dogs, 142 carcasses and 51 blood samples from captured raccoon dogs were collected from 2003 to 2010 and from 2008 to 2009, respectively, in Korea. In addition, 105 Haemaphysalis flava (14 larvae, 43 nymphs, 32 males, and 16 females) and nine Haemaphysalis longicornis (all female) were collected from three raccoon dogs. Samples of the spleen and blood were tested for the presence of VBPs by using nested polymerase chain reaction. Among the samples collected from 193 raccoon dogs and 114 ticks, two samples were positive for Anaplasma phagocytophilum, four for Anaplasma bovis, two for Borrelia theileri, and two for Bartonella henselae. To the best of our knowledge, this study is the largest survey of raccoon dogs aimed at the analysis of VBPs in this species. Moreover, the present study represents the first identification of A. phagocytophilum, B. henselae, and B. theileri in raccoon dogs in their native habitat (East Asia).

Author Notes

Address correspondence to Joon-seok Chae, Laboratory of Veterinary Internal Medicine, Research Institute BK21 Program for Veterinary Science and College of Veterinary Medicine, Seoul National University, 1 Gwanak-ro, Gwanak-gu, Seoul 08826, Korea. E-mail: jschae@snu.ac.kr

Financial support: This work was supported by the “Cooperative Research Program for Agriculture Science & Technology Development (project number PJ010092),” Rural Development Administration, the Republic of Korea, and a National Research Foundation of Korea Grant funded by the Korean Government (NRF-2014R1A1A2056207).

Authors’ addresses: Jun-Gu Kang, Veterinary Internal Medicine, College of Veterinary Medicine, Seoul National University, Seoul, Korea, E-mail: herculess@snu.ac.kr. Jeong-Byoung Chae, Yoon-Kyoung Cho, Young-Sun Jo, and Joon-Seok Chae, College of Veterinary Medicine, Seoul National University, Seoul, Korea, E-mails: jbchae117@gmail.com, hmhm0410@naver.com, joy85@snu.ac.kr, and jschae@snu.ac.kr. Nam-Shik Shin, Laboratory of Zoo and Wildlife Medicine, Research Institute and BK21 Program for Veterinary Science and College of Veterinary Medicine, Seoul National University, Seoul, Korea, E-mail: nsshin@snu.ac.kr. Hang Lee, Conservation Genome Resource Bank for Korean Wildlife and Research Institute for Veterinary Science, Seoul National University College of Medicine, Seoul, Korea, E-mail: hanglee@snu.ac.kr. Kyoung-Seong Choi, College of Ecology and Environmental Science, Kyungpook National University, Daegu, Korea, E-mail: kschoi3@knu.ac.kr. Do-Hyeon Yu, Institute of Animal Medicine, College of Veterinary Medicine, Gyeongsang National University, Jinju, Gyeongsangnam-do, E-mail: yudh@gnu.ac.kr. Jinho Park, College of Veterinary Medicine, Chonbuk National University, Iksan, Jeollabuk-do, Korea, E-mail: jpark@jbnu.ac.kr. Bae-Keun Park, College of Veterinary Medicine, Chungnam National University, Daejeon, Korea, E-mail: bkpark@cnu.ac.kr.

  • 1.

    Ward OG, Wurster-Hill DH, 1990. Mammalian Species: Nyctereutes procyonoides. Oxford, United Kingdom: Oxford University Press.

  • 2.

    Hyun BH, Lee KK, Kim IJ, Lee KW, Park HJ, Lee OS, An SH, Lee JB, 2005. Molecular epidemiology of rabies virus isolates from South Korea. Virus Res 114: 113125.

    • Search Google Scholar
    • Export Citation
  • 3.

    Oh SY, Kim SA, Kim JY, Yoo HS, Lee KK, Shin NS, 2012. Detection of antibodies against the rabies virus in Korean raccoon dogs (Nyctereutes procyonoides koreensis). J Zoo Wildl Med 43: 174176.

    • Search Google Scholar
    • Export Citation
  • 4.

    Härtwig V, von Loewenich FD, Schulze C, Straubinger RK, Daugschies A, Dyachenko V, 2014. Detection of Anaplasma phagocytophilum in red foxes (Vulpes vulpes) and raccoon dogs (Nyctereutes procyonoides) from Brandenburg, Germany. Ticks Tick Borne Dis 5: 277280.

    • Search Google Scholar
    • Export Citation
  • 5.

    Wodecka B, Michalik J, Lane RS, Nowak-Chmura M, Wierzbicka A, 2016. Differential associations of Borrelia species with European badgers (Meles meles) and raccoon dogs (Nyctereutes procyonoides) in western Poland. Ticks Tick Borne Dis 7: 10101016.

    • Search Google Scholar
    • Export Citation
  • 6.

    Han YJ, Park JH, Lee YS, Chae JS, Yu DH, Park BK, Kim HC, Choi KS, 2017. Molecular identification of selected tick-borne pathogens in wild deer and raccoon dogs from the Republic of Korea. Vet Parasitol Reg Stud Rep 7: 2531.

    • Search Google Scholar
    • Export Citation
  • 7.

    Sato S, Kabeya H, Miura T, Suzuki K, Bai Y, Kosoy M, Sentsui H, Kariwa H, Maruyama S, 2012. Isolation and phylogenetic analysis of Bartonella species from wild carnivores of the suborder Caniformia in Japan. Vet Microbiol 161: 130136.

    • Search Google Scholar
    • Export Citation
  • 8.

    Chen SM, Dumler JS, Bakken JS, Walker DH, 1994. Identification of a granulocytotropic Ehrlichia species as the etiologic agent of human disease. J Clin Microbiol 32: 589595.

    • Search Google Scholar
    • Export Citation
  • 9.

    Kim CM et al. 2006. Tick-borne rickettsial pathogens in ticks and small mammals in Korea. Appl Environ Microbiol 72: 57665776.

  • 10.

    Oh JY, Moon BC, Bae BK, Shin EH, Ko YH, Kim YJ, Park YH, Chae JS, 2009. Genetic identification and phylogenetic analysis of Anaplasma and Ehrlichia species in Haemaphysalis longicornis collected from Jeju Island, Korea. J Bacteriol Virol 39: 111.

    • Search Google Scholar
    • Export Citation
  • 11.

    Dugat T, Lagrée AC, Maillard R, Boulouis HJ, Haddad N, 2015. Opening the black box of Anaplasma phagocytophilum diversity: current situation and future perspectives. Front Cell Infect Microbiol 5: 61.

    • Search Google Scholar
    • Export Citation
  • 12.

    Kang JG, Ko S, Kim YJ, Yang HJ, Lee H, Shin NS, Choi KS, Chae JS, 2011. New genetic variants of Anaplasma phagocytophilum and Anaplasma bovis from Korean water deer (Hydropotes inermis argyropus). Vector Borne Zoonotic Dis 11: 929938.

    • Search Google Scholar
    • Export Citation
  • 13.

    Kang JG, Kim HC, Choi CY, Nam HY, Chae HY, Chong ST, Klein TA, Ko S, Chae JS, 2013. Molecular detection of Anaplasma, Bartonella, and Borrelia species in ticks collected from migratory birds from Hong-do Island, Republic of Korea. Vector Borne Zoonotic Dis 13: 215225.

    • Search Google Scholar
    • Export Citation
  • 14.

    Seong G, Han YJ, Chae JB, Chae JS, Yu DH, Lee YS, Park J, Park BK, Yoo JG, Choi KS, 2015. Detection of Anaplasma sp. in Korean native goats (Capra aegagrus hircus) on Jeju Island, Korea. Korean J Parasitol 53: 765769.

    • Search Google Scholar
    • Export Citation
  • 15.

    Lee SH, VanBik D, Kim NH, Park SJ, Kwon OD, Kim TH, Kwak D, 2016. First molecular detection and genetic analysis of Anaplasma phagocytophilum in shelter cats in Seoul, Korea. Infect Genet Evol 46: 7173.

    • Search Google Scholar
    • Export Citation
  • 16.

    Lee S, Lee SH, VanBik D, Kim NH, Kim KT, Goo YK, Rhee MH, Kwon OD, Kwak D, 2016. First molecular detection and phylogenetic analysis of Anaplasma phagocytophilum in shelter dogs in Seoul, Korea. Ticks Tick Borne Dis 7: 945950.

    • Search Google Scholar
    • Export Citation
  • 17.

    Kim KH, Yi J, Oh WS, Kim NH, Choi SJ, Choe PG, Kim NJ, Lee JK, Oh MD, 2014. Human granulocytic anaplasmosis, South Korea, 2013. Emerg Infect Dis 20: 17081711.

    • Search Google Scholar
    • Export Citation
  • 18.

    Chomel BB, Boulouis HJ, Maruyama S, Breitschwerdt EB, 2006. Bartonella spp. in pets and effect on human health. Emerg Infect Dis 12: 389394.

  • 19.

    Kang JG, Ko S, Smith WB, Kim HC, Lee IY, Chae JS, 2016. Prevalence of Anaplasma, Bartonella and Borrelia species in Haemaphysalis longicornis collected from goats in North Korea. J Vet Sci 17: 207216.

    • Search Google Scholar
    • Export Citation
  • 20.

    Kang JG et al. 2016. Prevalence of Anaplasma and Bartonella spp. in ticks collected from Korean water deer (Hydropotes inermis argyropus). Korean J Parasitol 54: 8791.

    • Search Google Scholar
    • Export Citation
  • 21.

    Kim YS, Seo KW, Lee JH, Choi EW, Lee HW, Hwang CY, Shin NS, Youn HJ, Youn HY, 2009. Prevalence of Bartonella henselae and Bartonella clarridgeiae in cats and dogs in Korea. J Vet Sci 10: 8587.

    • Search Google Scholar
    • Export Citation
  • 22.

    Ko S, Kim SJ, Kang JG, Won S, Lee H, Shin NS, Choi KS, Youn HY, Chae JS, 2013. Molecular detection of Bartonella grahamii and B. schoenbuchensis-related species in Korean water deer (Hydropotes inermis argyropus). Vector Borne Zoonotic Dis 13: 415418.

    • Search Google Scholar
    • Export Citation
  • 23.

    Kang JG, Won S, Kim HW, Kim BJ, Park BK, Park TS, Seo HY, Chae JS, 2016. Molecular detection of Bartonella spp. in terrestrial leeches (Haemadipsa rjukjuana) feeding on human and animal blood in Gageo-do, Republic of Korea. Parasit Vectors 9: 326.

    • Search Google Scholar
    • Export Citation
  • 24.

    Cotté V, Bonnet S, Le Rhun D, Le Naour E, Chauvin A, Boulouis HJ, Lecuelle B, Lilin T, Vayssier-Taussat M, 2008. Transmission of Bartonella henselae by Ixodes ricinus. Emerg Infect Dis 14: 10741080.

    • Search Google Scholar
    • Export Citation
  • 25.

    Im JH, Baek JH, Lee HJ, Lee JS, Chung MH, Kim M, Lee SM, Kang JS, 2013. First case of Bartonella henselae bacteremia in Korea. Infect Chemother 45: 446450.

    • Search Google Scholar
    • Export Citation
  • 26.

    Burgdorfer W, Barbour AG, Hayes SF, Benach JL, Grunwaldt E, Davis JP, 1982. Lyme disease-a tick-borne spirochetosis? Science 216: 13171319.

  • 27.

    Margos G, Vollmer SA, Ogden NH, Fish D, 2011. Population genetics, taxonomy, phylogeny and evolution of Borrelia burgdorferi sensu lato. Infect Genet Evol 11: 15451563.

    • Search Google Scholar
    • Export Citation
  • 28.

    Elbir H, FotsoFotso A, Diatta G, Trape JF, Arnathau C, Renaud F, Durand P, 2015. Ubiquitous bacteria Borrelia crocidurae in western African ticks Ornithodoros sonrai. Parasit Vectors 8: 477.

    • Search Google Scholar
    • Export Citation
  • 29.

    Barbour AG, Maupin GO, Teltow GJ, Carter CJ, Piesman J, 1996. Identification of an uncultivable Borrelia species in the hard tick Amblyomma americanum: possible agent of a Lyme disease-like illness. J Infect Dis 173: 403409.

    • Search Google Scholar
    • Export Citation
  • 30.

    Fukunaga M, Takahashi Y, Tsuruta Y, Matsushita O, Ralph D, McClelland M, Nakao M, 1995. Genetic and phenotypic analysis of Borrelia miyamotoi sp. nov., isolated from the ixodid tick Ixodes persulcatus, the vector for Lyme disease in Japan. Int J Syst Bacteriol 45: 804810.

    • Search Google Scholar
    • Export Citation
  • 31.

    Theiler A, 1904. Spirillosis of cattle. J Comp Pathol Ther 17: 4755.

  • 32.

    Park KH, Lee SH, Won WJ, Jang WJ, Chang WH, 1992. Isolation of Borrelia burgdorferi, the causative agent of Lyme disease, from Ixodes ticks in Korea. J Korean Soc Microbiol 27: 307312.

    • Search Google Scholar
    • Export Citation
  • 33.

    Jung BY, Gebeyehu EB, Seo MG, Byun JW, Kim HY, Kwak D, 2012. Prevalence of vector-borne diseases in shelter dogs in Korea. Vet Rec 171: 249.

  • 34.

    Lee SH, Yun SH, Choi E, Park YS, Lee SE, Cho GJ, Kwon OD, Kwak D, 2016. Serological detection of Borrelia burgdorferi among horses in Korea. Korean J Parasitol 54: 97101.

    • Search Google Scholar
    • Export Citation
  • 35.

    Yamaguti N, Tipton VJ, Keegan HL, Toshioka S, 1971. Ticks of Japan, Korea and the Ryukyu Islands. Sci Bull Biol Ser 15: 1227.

  • 36.

    Renesto P, Gouvernet J, Drancourt M, Roux V, Raoult D, 2001. Use of rpoB gene analysis for detection and identification of Bartonella species. J Clin Microbiol 39: 430437.

    • Search Google Scholar
    • Export Citation
  • 37.

    Zeaiter Z, Fournier PE, Ogata H, Raoult D, 2002. Phylogenetic classification of Bartonella species by comparing groEL sequences. Int J Syst Evol Microbiol 52: 165171.

    • Search Google Scholar
    • Export Citation
  • 38.

    Park HS, Lee JH, Jeong EJ, Koh SE, Park TK, Jang WJ, Park KH, Kim BJ, Kook YH, Lee SH, 2004. Evaluation of groEL gene analysis for identification of Borrelia burgdorferi sensu lato. J Clin Microbiol 42: 12701273.

    • Search Google Scholar
    • Export Citation
  • 39.

    Cheng WY, Zhao GH, Jia YQ, Bian QQ, Du SZ, Fang YQ, Qi MZ, Yu SK, 2013. Characterization of Haemaphysalis flava (Acari: Ixodidae) from Qingling subspecies of giant panda (Ailuropoda melanoleuca qinlingensis) in Qinling Mountains (central China) by morphology and molecular markers. PLoS One 8: e69793.

    • Search Google Scholar
    • Export Citation
  • 40.

    Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R, 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3: 294299.

    • Search Google Scholar
    • Export Citation
  • 41.

    Slaska B, Grzybowska-Szatkowska L, 2011. Analysis of the mitochondrial haplogroups of farm and wild-living raccoon dogs in Poland. Mitochondrial DNA 22: 105110.

    • Search Google Scholar
    • Export Citation
  • 42.

    Lee M, Yu D, Yoon J, Li Y, Lee J, Park J, 2009. Natural co-infection of Ehrlichia chaffeensis and Anaplasma bovis in a deer in South Korea. J Vet Med Sci 71: 101103.

    • Search Google Scholar
    • Export Citation
  • 43.

    Kim BJ et al. 2013. First report for the seasonal and annual prevalence of flea-borne Bartonella from rodents and soricomorphs in the Republic of Korea. Vector Borne Zoonotic Dis 13: 457467.

    • Search Google Scholar
    • Export Citation
  • 44.

    Moon S, Hong Y, Hwang KJ, Kim S, Eom J, Kwon D, Park JH, Youn SK, Sohn A, 2015. Epidemiological features and clinical manifestations of Lyme borreliosis in Korea during the period 2005–2012. Jpn J Infect Dis 68: 14.

    • Search Google Scholar
    • Export Citation
  • 45.

    Jilintai, Seino N, Hayakawa D, Suzuki M, Hata H, Kondo S, Matsumoto K, Yokoyama N, Inokuma H, 2009. Molecular survey for Anaplasma bovis and Anaplasma phagocytophilum infection in cattle in a pastureland where sika deer appear in Hokkaido, Japan. Jpn J Infect Dis 62: 7375.

    • Search Google Scholar
    • Export Citation
  • 46.

    Engel P et al. 2011. Parallel evolution of a type IV secretion system in radiating lineages of the host-restricted bacterial pathogen Bartonella. PLoS Genet 7: e1001296.

    • Search Google Scholar
    • Export Citation
  • 47.

    Callow LL, 1967. Observations on tick-transmitted spirochaetes of cattle in Australia and South Africa. Br Vet J 123: 492497.

  • 48.

    Khoo JJ, Lim FS, Tan KK, Chen FS, Phoon WH, Khor CS, Pike BL, Chang LY, AbuBakar S, 2017. Detection in Malaysia of a Borrelia sp. from Haemaphysalis hystricis (Ixodida: Ixodidae). J Med Entomol 54: 14441448.

    • Search Google Scholar
    • Export Citation
  • 49.

    Smith RD, Miranpuri GS, Adams JH, Ahrens EH, 1985. Borrelia theileri: isolation from ticks (Boophilus microplus) and tick-borne transmission between splenectomized calves. Am J Vet Res 46: 13961398.

    • Search Google Scholar
    • Export Citation
  • 50.

    Lee WK, Lim JW, Lee SY, Lee IY, 1997. Redescription of Haemaphysalis flava and Ixodes tanuki collected from a raccoon dog in Korea. Korean J Parasitol 35: 18.

    • Search Google Scholar
    • Export Citation
  • 51.

    Kim HC et al. 2011. Ticks collected from selected mammalian hosts surveyed in the Republic of Korea during 2008–2009. Korean J Parasitol 49: 331335.

    • Search Google Scholar
    • Export Citation
  • 52.

    Angelakis E, Billeter SA, Breitschwerdt EB, Chomel BB, Raoult D, 2010. Potential for tick-borne Bartonellosis. Emerg Infect Dis 16: 385391.

Past two years Past Year Past 30 Days
Abstract Views 64 64 31
Full Text Views 737 220 2
PDF Downloads 248 63 3
 
Membership Banner
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save