DOI QR코드

DOI QR Code

Serological evidence of Anaplasma spp., Borrelia burgdorferi and Ehrlichia canis in dogs from the Republic of Korea by rapid diagnostic test kits

  • Miranda, Evelyn Alejandra (Laboratory of Veterinary Internal Medicine, BK21 FOUR Future Veterinary Medicine Leading Education and Research Center, Research Institute for Veterinary Science and College of Veterinary Medicine, Seoul National University) ;
  • Han, Sun-Woo (Laboratory of Veterinary Internal Medicine, BK21 FOUR Future Veterinary Medicine Leading Education and Research Center, Research Institute for Veterinary Science and College of Veterinary Medicine, Seoul National University) ;
  • Rim, Ji-Min (Laboratory of Veterinary Internal Medicine, BK21 FOUR Future Veterinary Medicine Leading Education and Research Center, Research Institute for Veterinary Science and College of Veterinary Medicine, Seoul National University) ;
  • Cho, Yoon-Kyoung (Laboratory of Veterinary Internal Medicine, BK21 FOUR Future Veterinary Medicine Leading Education and Research Center, Research Institute for Veterinary Science and College of Veterinary Medicine, Seoul National University) ;
  • Choi, Kyoung-Seong (College of Ecology and Environmental Science, Kyungpook National University) ;
  • Chae, Joon-Seok (Laboratory of Veterinary Internal Medicine, BK21 FOUR Future Veterinary Medicine Leading Education and Research Center, Research Institute for Veterinary Science and College of Veterinary Medicine, Seoul National University)
  • Received : 2021.07.28
  • Accepted : 2021.12.05
  • Published : 2022.03.31

Abstract

Background: Emergent and re-emergent canine tick-borne infections are attracting increasing attention worldwide. The rise in pet ownership and the close relationship between dogs and their owners are the most concerning factors because dogs may act as competent reservoirs for human tick-transmitted infectious agents. Objectives: This study contributes to the epidemiological surveillance of canine tick-transmitted infections with zoonotic risk in the Republic of Korea (ROK) by investigating the seroprevalence of the pathogens, Anaplasma spp., Borrelia burgdorferi, and Ehrlichia canis. Methods: Four hundred and thirty whole blood samples from domestic dogs were collected in seven metropolitan cities and nine provinces in the ROK and tested using SensPERT Ab test kits (VetAll Laboratories®) to detect seroreactive animals. Results: The seroprevalence rates identified were 9.8% (42/430) for Anaplasma spp., 2.8% (12/430) for B. burgdorferi, and 1.4% (6/430) for E. canis. The risk factors evaluated in this study that could be associated with the development of a humoral immune response, such as sex, age, and history of tick exposure, were similar. There was only one exception for dogs seroreactive to Anaplasma spp., where the risk factor "tick exposure" was statistically significant (p = 0.047). Conclusions: This serological survey exhibited the widespread presence of Anaplasma spp., B. burgdorferi, and E. canis throughout the ROK. Hence, dogs may play a key role as the sentinel animals of multiple zoonotic infectious agents in the country.

Keywords

Acknowledgement

The authors wish to thank VetAll Laboratories® for providing the SensPERT Ab Test Kits for this study. Evelyn Alejandra Miranda expresses her deep gratitude to the National Institute of International Education (NIIED) and the Global Korea Scholarship (GKS) program for the scholarship granted for her graduate studies for 2018-2021.

References

  1. Potkonjak A, Zekic-Stosic M. Tick-borne infections of dogs in Serbia: a review of research. Vet Glas. 2020;74(2):107-124. https://doi.org/10.2298/VETGL201103014P
  2. Dantas-Torres F, Otranto D. Best practices for preventing vector-borne diseases in dogs and humans. Trends Parasitol. 2016;32(1):43-55. https://doi.org/10.1016/j.pt.2015.09.004
  3. Sharifah N, Heo CC, Ehlers J, Houssaini J, Tappe D. Ticks and tick-borne pathogens in animals and humans in the island nations of Southeast Asia: a review. Acta Trop. 2020;209:105527. https://doi.org/10.1016/j.actatropica.2020.105527
  4. Chomel B. Tick-borne infections in dogs-an emerging infectious threat. Vet Parasitol. 2011;179(4):294-301. https://doi.org/10.1016/j.vetpar.2011.03.040
  5. Chirek A, Silaghi C, Pfister K, Kohn B. Granulocytic anaplasmosis in 63 dogs: clinical signs, laboratory results, therapy and course of disease. J Small Anim Pract. 2018;59(2):112-120. https://doi.org/10.1111/jsap.12787
  6. Liu J, Eberts M, Bewsey H, O'Connor TP, Chandrashekar R, Breitschwerdt EB. Sensitivity and specificity levels of two rapid assays for antibodies to Anaplasma spp. in dogs. J Vet Diagn Invest. 2018;30(2):290-293. https://doi.org/10.1177/1040638717745932
  7. Silaghi C, Kohn B, Chirek A, Thiel C, Nolte I, Liebisch G, et al. Relationship of molecular and clinical findings on Anaplasma phagocytophilum involved in natural infections of dogs. J Clin Microbiol. 2011;49(12):4413-4414. https://doi.org/10.1128/JCM.06041-11
  8. Lee SH, Kim N, Kwak D. First clinical case of canine granulocytic anaplasmosis in Korea and genotypic analyses of Anaplasma phagocytophilum. Ticks Tick Borne Dis. 2017;8(4):462-465. https://doi.org/10.1016/j.ttbdis.2017.02.003
  9. Harrus S, Aroch I, Lavy E, Bark H. Clinical manifestations of infectious canine cyclic thrombocytopenia. Vet Rec. 1997;141(10):247-250. https://doi.org/10.1136/vr.141.10.247
  10. Volgina NS, Romashov BV, Romashova NB, Shtannikov AV. Prevalence of borreliosis, anaplasmosis, ehrlichiosis and Dirofilaria immitis in dogs and vectors in Voronezh Reserve (Russia). Comp Immunol Microbiol Infect Dis. 2013;36(6):567-574. https://doi.org/10.1016/j.cimid.2013.08.003
  11. Gaunt S, Beall M, Stillman B, Lorentzen L, Diniz P, Chandrashekar R, et al. Experimental infection and co-infection of dogs with Anaplasma platys and Ehrlichia canis: hematologic, serologic and molecular findings. Parasit Vectors. 2010;3(1):33. https://doi.org/10.1186/1756-3305-3-33
  12. Murphy GL, Ewing SA, Whitworth LC, Fox JC, Kocan AA. A molecular and serologic survey of Ehrlichia canis, E. chaffeensis, and E. ewingii in dogs and ticks from Oklahoma. Vet Parasitol. 1998;79(4):325-339. https://doi.org/10.1016/S0304-4017(98)00179-4
  13. Fritz CL. Emerging tick-borne diseases. Vet Clin North Am Small Anim Pract. 2009;39(2):265-278. https://doi.org/10.1016/j.cvsm.2008.10.019
  14. Magnarelli LA, Anderson JF, Schreier AB, Ficke CM. Clinical and serologic studies of canine borreliosis. J Am Vet Med Assoc. 1987;191(9):1089-1094.
  15. Colella V, Nguyen VL, Tan DY, Lu N, Fang F, Zhijuan Y, et al. Zoonotic vectorborne pathogens and ectoparasites of dogs and cats in eastern and Southeast Asia. Emerg Infect Dis. 2020;26(6):1221-1233. https://doi.org/10.3201/eid2606.191832
  16. Lee S, Lee H, Park JW, Yoon SS, Seo HJ, Noh J, et al. Prevalence of antibodies against Anaplasma spp., Borrelia burgdorferi sensu lato, Babesia gibsoni, and Ehrlichia spp. in dogs in the Republic of Korea. Ticks Tick Borne Dis. 2020;11(4):101412. https://doi.org/10.1016/j.ttbdis.2020.101412
  17. Lee S, Lee SH, VanBik D, Kim NH, Kim KT, Goo YK, et al. First molecular detection and phylogenetic analysis of Anaplasma phagocytophilum in shelter dogs in Seoul, Korea. Ticks Tick Borne Dis. 2016;7(5):945-950. https://doi.org/10.1016/j.ttbdis.2016.04.011
  18. Suh GH, Ahn KS, Ahn JH, Kim HJ, Leutenegger C, Shin S. Serological and molecular prevalence of canine vector-borne diseases (CVBDs) in Korea. Parasit Vectors. 2017;10(1):146. https://doi.org/10.1186/s13071-017-2076-x
  19. Bell DR, Berghaus RD, Patel S, Beavers S, Fernandez I, Sanchez S. Seroprevalence of tick-borne infections in military working dogs in the Republic of Korea. Vector Borne Zoonotic Dis. 2012;12(12):1023-1030. https://doi.org/10.1089/vbz.2011.0864
  20. Lim S, Irwin PJ, Lee S, Oh M, Ahn K, Myung B, et al. Comparison of selected canine vector-borne diseases between urban animal shelter and rural hunting dogs in Korea. Parasit Vectors. 2010;3(1):32. https://doi.org/10.1186/1756-3305-3-32
  21. Cui Y, Yan Y, Wang X, Cao S, Zhang Y, Jian F, et al. First molecular evidence of mixed infections of Anaplasma species in dogs in Henan, China. Ticks Tick Borne Dis. 2017;8(2):283-289. https://doi.org/10.1016/j.ttbdis.2016.12.001
  22. Shi K, Li J, Yan Y, Chen Q, Wang K, Zhou Y, et al. Dogs as new hosts for the emerging zoonotic pathogen Anaplasma capra in China. Front Cell Infect Microbiol. 2019;9:394. https://doi.org/10.3389/fcimb.2019.00394
  23. Miranda EA, Han SW, Cho YK, Choi KS, Chae JS. Co-infection with Anaplasma species and novel genetic variants detected in cattle and goats in the Republic of Korea. Pathogens. 2021;10(1):28. https://doi.org/10.3390/pathogens10010028
  24. Zhang J, Liu Q, Wang D, Li W, Beugnet F, Zhou J. Epidemiological survey of ticks and tick-borne pathogens in pet dogs in south-eastern China. Parasite. 2017;24:35. https://doi.org/10.1051/parasite/2017036
  25. Uesaka K, Maezawa M, Inokuma H. Serological survey of Borrelia infection of dogs in Sapporo, Japan, where Borrelia garinii infection was previously detected. J Vet Med Sci. 2016;78(3):463-465. https://doi.org/10.1292/jvms.15-0392
  26. Yu DH, Li YH, Yoon JS, Lee JH, Lee MJ, Yu IJ, et al. Ehrlichia chaffeensis infection in dogs in South Korea. Vector Borne Zoonotic Dis. 2008;8(3):355-358. https://doi.org/10.1089/vbz.2007.0226
  27. Jung BY, Gebeyehu EB, Seo MG, Byun JW, Kim HY, Kwak D. Prevalence of vector-borne diseases in shelter dogs in Korea. Vet Rec. 2012;171(10):249.
  28. Kubo S, Tateno M, Ichikawa Y, Endo Y. A molecular epidemiological survey of Babesia, Hepatozoon, Ehrlichia and Anaplasma infections of dogs in Japan. J Vet Med Sci. 2015;77(10):1275-1279. https://doi.org/10.1292/jvms.15-0079
  29. Shaw SE, Day MJ, Birtles RJ, Breitschwerdt EB. Tick-borne infectious diseases of dogs. Trends Parasitol. 2001;17(2):74-80. https://doi.org/10.1016/S1471-4922(00)01856-0
  30. Beall MJ, Chandrashekar R, Eberts MD, Cyr KE, Diniz PP, Mainville C, et al. Serological and molecular prevalence of Borrelia burgdorferi, Anaplasma phagocytophilum, and Ehrlichia species in dogs from Minnesota. Vector Borne Zoonotic Dis. 2008;8(4):455-464. https://doi.org/10.1089/vbz.2007.0236
  31. Kim CM, Kim MS, Park MS, Park JH, Chae JS. Identification of Ehrlichia chaffeensis, Anaplasma phagocytophilum, and A. bovis in Haemaphysalis longicornis and Ixodes persulcatus ticks from Korea. Vector Borne Zoonotic Dis. 2003;3(1):17-26. https://doi.org/10.1089/153036603765627424
  32. Choe HC, Fudge M, Sames WJ, Robbins RG, Lee IY, Chevalier NA, et al. Tick surveillance of dogs in the Republic of Korea. Syst Appl Acarol. 2011;16(3):215-222. https://doi.org/10.11158/saa.16.3.5
  33. Chong ST, Kim HC, Lee IY, Kollars TM Jr, Sancho AR, Sames WJ, et al. Seasonal distribution of ticks in four habitats near the demilitarized zone, Gyeonggi-do (Province), Republic of Korea. Korean J Parasitol. 2013;51(3):319-325. https://doi.org/10.3347/kjp.2013.51.3.319
  34. Jo YS, Kang JG, Chae JB, Cho YK, Shin JH, Jheong WH, et al. Prevalence of severe fever with thrombocytopenia syndrome virus in ticks collected from national parks in Korea. Vector Borne Zoonotic Dis. 2019;19(4):284-289. https://doi.org/10.1089/vbz.2018.2338
  35. Kang JG, Cho YK, Jo YS, Chae JB, Joo YH, Park KW, et al. Severe fever with thrombocytopenia syndrome virus in dogs, South Korea. Emerg Infect Dis. 2019;25(2):376-378. https://doi.org/10.3201/eid2502.180859