1. bookVolume 68 (2018): Issue 3 (September 2018)
Journal Details
License
Format
Journal
eISSN
1820-7448
First Published
25 Mar 2014
Publication timeframe
4 times per year
Languages
English
access type Open Access

Molecular Evidence of Q Fever Agent Coxiella Burnetii in Ixodid Ticks Collected from Stray Dogs in Belgrade (Serbia)

Published Online: 03 Oct 2018
Volume & Issue: Volume 68 (2018) - Issue 3 (September 2018)
Page range: 257 - 268
Received: 04 Jun 2018
Accepted: 13 Jul 2018
Journal Details
License
Format
Journal
eISSN
1820-7448
First Published
25 Mar 2014
Publication timeframe
4 times per year
Languages
English
Abstract

Q fever is a zoonotic disease caused by Coxiella burnetii, a gram-negative coccobacillus, which has been detected in a wide range of animal species, mostly domestic ruminants, but also in wild mammals, pets, birds, reptiles, arthropods (especially ticks), as well as in humans. Although the exposure to domestic animals in rural areas is regarded as the most common cause of the disease in humans, recent studies have shown that the role of pets in the epidemiology of Q fever has been increasingly growing. Although the primary route of infection is inhalation, it is presumed that among animals the infection circulates through ticks and that they are responsible for heterospecifi c transmission, as well as spatial dispersion among vertebrates. The aim of this study was to determine the presence and prevalence of C. burnetii in ticks removed from stray dogs, as well as to examine the distribution of tick species parasitizing dogs on the territory of Belgrade city. A PCR protocol targeting IS1111 repetitive transposon-like region of C. burnetii was used for the detection of C. burnetii DNA in ticks and the results were confi rmed by sequence analysis. In total, 316 ticks were collected from 51 stray dogs - 40 females (78.43%) and 11 males (21.57%). Three species of ticks were identifi ed: Rhipicephalus s anguineus (72.15%), Ixodes ricinus (27.53%) and Dermacentor reticulatus (0.32%). Out of 316 examined ticks, C. burnetii DNA was detected only in the brown dog tick R. sanguineus, with a total prevalence of 10.53% (24/228) . The high prevalence of C. burnetii in R. sanguineus, which is primarily a dog tick, indicates the importance of dogs in the epidemiology of Q fever in the territory of Belgrade.

Keywords

1. Babudieri B: Q fever: a zoonosis. Adv Vet Sci 1959, 5:81-154.Search in Google Scholar

2. Scott GH, McCaul TF, Williams JC: Inactivation of Coxiella burnetii by Gamma Irradiation. Microbiology 1989, 135:3263-70.10.1099/00221287-135-12-3263Search in Google Scholar

3. Scott GH, Williams JC: Susceptibility of Coxiella burnetii to chemical disinfectants. Ann N Y Acad Sci 1990, 590:291-6.10.1111/j.1749-6632.1990.tb42235.xSearch in Google Scholar

4. Rousset E, Berri M, Durand B, Dufour P, Prigent M, Delcroix T, Touratier A, Rodolakis A: Coxiella burnetii shedding routes and antibody response after outbreaks of Q fever-induced abortion in dairy goat herds. Appl Environ Microbiol 2009, 75:428-33.10.1128/AEM.00690-08Search in Google Scholar

5. Maurin M, Raoult D: Q fever. Clin Microbiol Rev 1999, 12:518-53.10.1128/CMR.12.4.518Search in Google Scholar

6. Rodolakis A: Q Fever in Dairy Animals. Ann N Y Acad Sci 2009, 1166:90-3.10.1111/j.1749-6632.2009.04511.xSearch in Google Scholar

7. Joulié A, Laroucau K, Bailly X, Prigent M, Gasqui P, Lepetitcolin E, Blanchard B, Rousset E, Sidi-Boumedine K, Jourdain E: Circulation of Coxiella burnetii in a naturally infected fl ock of dairy sheep: Shedding dynamics, environmental contamination, and genotype diversity. Appl Environ Microbiol 2015, 81:7253-60.10.1128/AEM.02180-15Search in Google Scholar

8. Marrie TJ: Epidemiology of Q fever. In: Q fever, Vol. I. Florida, USA: Boca Raton, CRC Press; 1990, 49-70.Search in Google Scholar

9. Buhariwalla F, Cann B, Marrie TJ: A dog-related outbreak of Q fever. Clin Infect Dis 1996, 23:753-5.10.1093/clinids/23.4.753Search in Google Scholar

10. Laughlin T, Waag D, Williams J, Marrie T: Q fever: from deer to dog to man. Lancet (London, England) 1991, 337:676-7.10.1016/0140-6736(91)92494-MSearch in Google Scholar

11. Komiya T, Sadamasu K, Toriniwa H, Kato K, Arashima Y, Fukushi H, Hirai K, Arakawa Y: Epidemiological survey on the route of Coxiella burnetii infection in an animal hospital. J Infect Chemother 2003, 9:151-5.10.1007/s10156-003-0237-712825114Search in Google Scholar

12. Mantovani A, Benazzi P: The isolation of Coxiella burnetii from Rhipicephalus sanguineus on naturally infected dogs. J Am Vet Med Assoc 1953, 122:117-8.Search in Google Scholar

13. Smith DJW, Derrick EH: Studies in the Epidemiology of Q Fever. I. The Isolation of Six Strains of Rickettsia burneti from the Tick Haemaphysalis humerosa. Aust J Exp Biol Med Sci 1940, 18:1-8.10.1038/icb.1940.1Search in Google Scholar

14. Philip CB: Observations on Experimental Q Fever. J Parasitol 1948, 34:457.10.2307/3273312Search in Google Scholar

15. Duron O, Sidi-Boumedine K, Rousset E, Moutailler S, Jourdain E: The Importance of Ticks in Q Fever Transmission: What Has (and Has Not) Been Demonstrated? Trends Parasitol 2015, 31:536-52.10.1016/j.pt.2015.06.014Search in Google Scholar

16. Eldin C, Mélenotte C, Mediannikov O, Ghigo E, Million M, Edouard S, Mege JL, Maurin M, Raoult D: From Q Fever to Coxiella burnetii Infection: a Paradigm Change. Clin Microbiol Rev 2017, 30:115-90.10.1128/CMR.00045-16Search in Google Scholar

17. Estrada-Peña A, Bouattour A, Camicas J, Walker AR: Ticks of Domestic Animals in the Mediterranean Region A guide to identifi cation of species. 2004.Search in Google Scholar

18. Berri M, Laroucau K, Rodolakis A: The detection of Coxiella burnetii from ovine genital swabs, milk and fecal samples by the use of a single touchdown polymerase chain reaction. Vet Microbiol 2000, 72:285-93.10.1016/S0378-1135(99)00178-9Search in Google Scholar

19. Thompson JD, Higgins DG, Gibson TJ: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specifi c gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22:4673-80.10.1093/nar/22.22.46733085177984417Search in Google Scholar

20. Duron O: The IS1111 insertion sequence used for detection of Coxiella burnetii is widespread in Coxiella-like endosymbionts of ticks. FEMS Microbiol Lett 2015, 362:fnv132.10.1093/femsle/fnv13226269380Search in Google Scholar

21. Tomanović S, Chochlakis D, Radulović Ž, Milutinović M, Ćakić S, Mihaljica D, Tselentis Y, Psaroulaki A: Analysis Analysis of pathogen co-occurrence in host-seeking adult hard ticks from Serbia. Exp Appl Acarol 2013, 59:367-76.10.1007/s10493-012-9597-y22773070Search in Google Scholar

22. Sukara R, Chochlakis D, Ćirović D, Penezić A, Mihaljica D, Ćakić S, Valčić M, Tselentis Y, Psaroulaki A, Tomanović S: Golden jackals (Canis aureus) as hosts for ticks and tick-borne pathogens in Serbia. Ticks Tick Borne Dis 2018. doi:10.1016/J.TTBDIS.2018.04.003.Search in Google Scholar

23. Sprong H, Tijsse-Klasen E, Langelaar M, De Bruin A, Fonville M, Gassner F, Takken W, Van Wieren S, Nijhof A, Jongejan F, Maassen CB, Sholte EJ, Hovius JW, Emil Hovius JW, Spitalská E, Van Duynhoven YT: Prevalence of Coxiella burnetii in ticks after a large outbreak of Q Fever. Zoonoses Public Health 2012, 59:69-75.10.1111/j.1863-2378.2011.01421.x21824373Search in Google Scholar

24. Reye AL, Hübschen JM, Sausy A, Muller CP: Prevalence and seasonality of tick-borne pathogens in questing ixodes ricinus ticks from Luxembourg. Appl Environ Microbiol 2010, 76:2923-31.10.1128/AEM.03061-09286342720228110Search in Google Scholar

25. Pluta S, Hartelt K, Oehme R, Mackenstedt U, Kimmig P: Prevalence of Coxiella burnetii and Rickettsia spp. in ticks and rodents in southern Germany. Ticks Tick Borne Dis 2010, 1:145-7.10.1016/j.ttbdis.2010.04.00121771522Search in Google Scholar

26. Spitalská E, Kocianová E: Detection of Coxiella burnetii in ticks collected in Slovakia and Hungary. Eur J Epidemiol 2003, 18:263-6.10.1023/A:1023330222657Search in Google Scholar

27. Barandika JF, Hurtado A, García-Esteban C, Gil H, Escudero R, Barral M, Jado I, Juste RA, Anda P, Gárcia-Pérez: Tick-borne zoonotic bacteria in wild and domestic small mammals in northern Spain. Appl Environ Microbiol 2007, 73:6166-71.10.1128/AEM.00590-07207500817693556Search in Google Scholar

28. Barandika JF, Hurtado A, García-Sanmartín J, Juste RA, Anda P, García-Pérez AL: Prevalence of Tick-Borne Zoonotic Bacteria in Questing Adult Ticks from Northern Spain. Vector-Borne Zoonotic Dis 2008, 8:829-36.10.1089/vbz.2008.002318759563Search in Google Scholar

29. Bessas A, Leulmi H, Bitam I, Zaidi S, Ait-Oudhia K, Raoult D, Parola P Molecular evidence of vector-borne pathogens in dogs and cats and their ectoparasites in Algiers, Algeria. Comp Immunol Microbiol Infect Dis 2016, 45:23-8.10.1016/j.cimid.2016.01.00227012917Search in Google Scholar

30. Andoh M, Andoh R, Teramoto K, Komiya T, Kaneshima T, Takano A, Hayashidani H, Ando S: Survey of Coxiella burnetii in Ticks Collected from Dogs in Japan. J Vet Med Sci 2013, 75:3-5.10.1292/jvms.12-057023558956Search in Google Scholar

31. Bolaños-Rivero M, Carranza-Rodríguez C, Rodríguez NF, Gutiérrez C, Pérez-Arellano J-L: Detection of Coxiella burnetii DNA in Peridomestic and Wild Animals and Ticks in an Endemic Region (Canary Islands, Spain). Vector-Borne Zoonotic Dis 2017, 17:630-4.10.1089/vbz.2017.212028759337Search in Google Scholar

32. Toledo A, Jado I, Olmeda AS, Casado-Nistal MA, Gil H, Escudero R, Anda P: Detection of Coxiella burnetii in Ticks Collected from Central Spain. Vector-Borne Zoonotic Dis 2009, 9:465-8.10.1089/vbz.2008.007018945192Search in Google Scholar

33. Satta G, Chisu V, Cabras P, Fois F, Masala G: Pathogens and symbionts in ticks: A survey on tick species distribution and presence of tick-transmitted micro-organisms in Sardinia, Italy. J Med Microbiol 2011, 60:63-8.10.1099/jmm.0.021543-020884769Search in Google Scholar

34. Spyridaki I, Psaroulaki A, Loukaides F, Antoniou M, Hadjichristodolou C, Tselentis Y: Isolation of Coxiella burnetii by a centrifugation shell-vial assay from ticks collected in Cyprus: Detection by nested polymerase chain reaction (PCR) and by PCR-restriction fragment length polymorphism analyses. Am J Trop Med Hyg 2002, 66:86-90.10.4269/ajtmh.2002.66.8612135275Search in Google Scholar

35. Psaroulaki A, Hadjichristodoulou C, Loukaides F, Soteriades E, Konstantinidis A, Papastergiou P, Ioannidou MC, Tselentis Y: Epidemiological study of Q fever in humans, ruminant animals, and ticks in Cyprus using a geographical information system. Eur J Clin Microbiol Infect Dis 2006, 25:576-86.10.1007/s10096-006-0170-716915398Search in Google Scholar

36. Psaroulaki A, Chochlakis D, Angelakis E, Ioannou I, Tselentis Y: Coxiella burnetii in wildlife and ticks in an endemic area. Trans R Soc Trop Med Hyg 2014, 108:625-31.10.1093/trstmh/tru13425163752Search in Google Scholar

37. Dantas-Torres F: The brown dog tick, Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae): From taxonomy to control. Vet Parasitol 2008, 152:173-85.10.1016/j.vetpar.2007.12.03018280045Search in Google Scholar

38. Little SE, Hostetler J, Kocan KM: Movement of Rhipicephalus sanguineus adults between cohoused dogs during active feeding. Vet Parasitol 2007, 150:139-45.10.1016/j.vetpar.2007.08.02917904292Search in Google Scholar

39. Estrada-Peña A, Jongejan F: Ticks feeding on humans: A review of records on humanbiting Ixodoidea with special reference to pathogen transmission. Exp Appl Acarol 1999, 23:685-715.10.1023/A:1006241108739Search in Google Scholar

40. Demma LJ, Traeger MS, Nicholson WL, Paddock CD, Blau DM, Eremeeva ME, Dasch GA, Levin ML, 442 Singleton J Jr, Zaki SR, Cheek JE, Swerdlow DL, McQuiston JH: Rocky Mountain Spotted Fever from an Unexpected Tick Vector in Arizona. N Engl J Med 2005, 353:587-94.10.1056/NEJMoa05004316093467Search in Google Scholar

41. Dantas-Torres F, Figueredo LA, Brandão-Filho SP: Rhipicephalus sanguineus (Acari: Ixodidae), the brown dog tick, parasitizing humans in Brazil. Rev Soc Bras Med Trop 2006, 39:64-7.10.1590/S0037-8682200600010001216501769Search in Google Scholar

42. Beaman MH, Hung J: Pericarditis associated with tick-borne Q fever. Aust N Z J Med 1989, 19:254-6.10.1111/j.1445-5994.1989.tb00258.x71656952775046Search in Google Scholar

43. Rolain JM, Gouriet F, Brouqui P, Larrey D, Janbon F, Vene S, Jarnestrom V, Raoult D: Concomitant or Consecutive Infection with Coxiella burnetii and Tickborne Diseases. Clin Infect Dis 2005, 40:82-8.10.1086/42644015614696Search in Google Scholar

44. Nett RJ, Book E, Anderson AD: Q Fever with unusual exposure history: a classic presentation of a commonly misdiagnosed disease. Case Rep Infect Dis 2012, 2012:916142.10.1155/2012/916142340556322848855Search in Google Scholar

Recommended articles from Trend MD

Plan your remote conference with Sciendo