Advertisement

Acta Parasitologica

, Volume 64, Issue 4, pp 769–778 | Cite as

Seroprevalences of Rickettsia conorii, Ehrlichia canis and Coxiella burnetii in Dogs from Montenegro

  • Dejan Laušević
  • Tamara Ilić
  • Katarina NenadovićEmail author
  • Dragan Bacić
  • Sonja Obrenović
Original Paper
  • 35 Downloads

Abstract

Purpose

The incidence of vector-borne zoonoses has been increasing in Europe as a result of global climate change, and rickettsioses are a significant etiologic entity among these infections. The objective of this study was to investigate the seroprevalences of Rickettsia conorii, Ehrlichia canis and Coxiella burnetii in dogs in Montenegro.

Methods

The seroepidemiological study covered 259 dogs, of which 155 were owned dogs suspected of infection with agents of rickettsial aetiology from the continental (Podgorica) or five coastal municipalities of Montenegro (Budva, Herceg Novi, Kotor, Ulcinj and Bar), and 104 dogs were from a public shelter in Podgorica. The presence of specific IgG antibodies against R. conorii was analysed using a commercial indirect enzyme-linked immunosorbent assay (ELISA) test, and the presence of antibodies against E. canis and C. burnetii was analysed using commercial indirect immunofluorescence tests (IFAT).

Results

Seroprevalences of 73.36, 19.3 and 1.16% were determined for R. conorii, E. canis and C. burnetii, respectively. R. conorii was significantly more prevalent (χ2 = 14.53; p < 0.001) in owned dogs (81.93%) than in dogs from the public shelter (60.6%), while E. canis was more prevalent (χ2 = 12.31; p < 0.001) in dogs from the public shelter (29.81%) than in owned dogs (12.26%). Coinfection with two pathogens was determined in 40 (15.44%) dogs, and the prevalence of R. conorii/E. canis (χ2 = 4.23; p < 0.05) was greater in dogs from the public shelter (20.19%) than in owned dogs (10.97%).

Conclusion

The prevailing evidence from this study shows that dogs from Montenegro are exposed to pathogens of veterinary and public health importance. This calls for the One Health approach to sensitise the public on the risks of zoonoses from dogs and to formulate policies and strategies to mitigate their spread and safeguard public health.

Keywords

Rickettsia conorii Ehrlichia canis Coxiella burnetii Dog Antibodies Montenegro 

Notes

Acknowledgements

We would like to express our gratitude to all the veterinarians and the managers of the public dog shelter in Podgorica who provided dog blood samples for this study.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

References

  1. 1.
    Biggs HM, Behravesh BC, Bradley KK, Dahlgren SF, Drexler NA, Dumler SJ, Folk SM, Kato CY, Lash RR, Levin ML, Massung RF, Nadelman RB, Nicholson WL, Paddock CD, Pritt SB, Traeger MS (2016) Diagnosis and management of tickborne rickettsial diseases: rocky mountain spotted fever and other spotted fever group rickettsioses, ehrlichioses, and anaplasmosis—United States. A practical guide for health care and public health professionals. MMWR Recomm Rep 65:1–44.  https://doi.org/10.15585/mmwr.rr6502a1 CrossRefPubMedGoogle Scholar
  2. 2.
    Parola P, Paddock CD, Socolovschi C, Labruna MB, Mediannikov O, Kernif T, Abdad MY, Stenos J, Bitam I, Fournier PE, Raoult D (2013) Update on tick-borne rickettsioses around the world: a geographic approach. Clin Microbiol Rev 26:657–702.  https://doi.org/10.1128/CMR.00032-13 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Barradas FP, Vilhena H, Oliveira AC, Granada S, Amorim I, Ferreira P, Cardoso L, Gärtner F, de Sousa R (2017) Serological and molecular detection of spotted fever group Rickettsia in a group of pet dogs from Luanda, Angola. Parasite Vector 10:271.  https://doi.org/10.1186/s13071-017-2216-3 CrossRefGoogle Scholar
  4. 4.
    Nicholson W, Allen K, McQuiston E (2010) The increasing recognition of rickettsial pathogens in dogs and people. Trends Parasitol 26:205–212.  https://doi.org/10.1016/j.pt.2010.01.007 CrossRefPubMedGoogle Scholar
  5. 5.
    Procajło A, Mikulska Skupień E, Bladowski M, Lew S (2011) Monocytic ehrlichiosis in dogs. Pol J Vet Sci 14:515–520 (PMID: 21957751) CrossRefGoogle Scholar
  6. 6.
    Perez M, Rikihisa Y, Bohai W (1996) Ehrlichia canis—like agent isolated from a man in Venezuela: antigenic and genetic characterization. J Clin Microbiol 34:2133–2139PubMedPubMedCentralGoogle Scholar
  7. 7.
    Bouza-Mora L, Dolz G, Solórzano-Morales A, Romero-Zuñiga JJ, Salazar-Sánchez L, Labruna MB, Aguiar DM (2017) Novel genotype of Ehrlichia canis detected in samples of human blood bank donors in Costa Rica. Ticks Tick Borne Dis 8:36–40.  https://doi.org/10.1016/j.ttbdis.2016.09.012 CrossRefPubMedGoogle Scholar
  8. 8.
    Perez M, Bodor M, Zhang C, Xiong Q, Rikihisa Y (2006) Human infection with Ehrlichia canis accompanied by clinical signs in Venezuela. Ann N Y Acad Sci 1078:110–117.  https://doi.org/10.1196/annals.1374.016 CrossRefPubMedGoogle Scholar
  9. 9.
    Bolaños-Rivero M, Carranza-Rodríguez C, Rodríguez NF, Gutiérrez C, Pérez-Arellano JL (2017) Detection of Coxiella burnetii DNA in peridomestic and wild animals and ticks in an endemic region (Canary Island, Spain). Vector-Borne Zoonot 17:630–634.  https://doi.org/10.1089/vbz.2017.2120 CrossRefGoogle Scholar
  10. 10.
    Ceylan E, Berktas M, Keles I, Agaoglu Z (2009) Seroprevalence of Q fever in cattle and sheep in the east of Turkey. Asian J Anim Vet Adv 4:114–121.  https://doi.org/10.3923/ajava.2009.114.121 CrossRefGoogle Scholar
  11. 11.
    Tozer SJ, Lambert SB, Strong CL, Field HE, Sloots TP, Nissen MD (2014) Potential animal and environmental sources od Q fever infection for humans in Queensland. Zoonoses Public Health 61:105–112.  https://doi.org/10.1111/zph.12051 CrossRefPubMedGoogle Scholar
  12. 12.
    Esmailnejad A, Abbaszadeh Hasiri M (2016) Serological evidence of Coxiella burnetii infection among companion dogs in Fars province, South Iran. Bulg J Vet Med Online First 20:377–384.  https://doi.org/10.15547/bjvm.1016 CrossRefGoogle Scholar
  13. 13.
    Rezaei M, Khalili M, Akhtardanesh B, Shahheidaripour S (2016) Q fever in dogs: an emerging infectious disease in Iran. J Med Bacteriol 5:1–6Google Scholar
  14. 14.
    Eldin C, Mélenotte C, Mediannikov O, Ghigo E, Million M, Edouard S, Mege J, Maurin M, Raoult D (2017) From Q fever to Coxiella burnetii infection: a paradigm change. Clin Microbiol Rev 30:115–190.  https://doi.org/10.1128/CMR.00045-16 CrossRefPubMedGoogle Scholar
  15. 15.
    Otranto D, Dantas-Torres F (2010) Canine and feline vector-borne diseases in Italy: current situation and perspectives. Parasite Vector 3:2.  https://doi.org/10.1186/1756-3305-3-2 CrossRefGoogle Scholar
  16. 16.
    Latrofa SM, Angelou A, Giannelli A, Annoscia G, Ravagnan S, Dantas-Torres F, Capelli G, Halos L, Beugnet F, Papadopoulos E, Otranto D (2017) Ticks and associated pathogens in dogs from Greece. Parasite Vector 10:301.  https://doi.org/10.1186/s13071-017-2225-2 CrossRefGoogle Scholar
  17. 17.
    Socolovschi C, Kernif T, Raoult D, Parola P (2012) Borrelia, Rickettsia, and Ehrlichia species in bat ticks, France. Emerg Infect Dis 18:1966–1975.  https://doi.org/10.3201/eid1812.111237 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Marquez FJ (2008) Spotted fever group Rickettsia in ticks from southeastern Spain natural parks. Exp Appl Acarol 45:185–194.  https://doi.org/10.3201/eid1907.130005 CrossRefPubMedGoogle Scholar
  19. 19.
    Vilibic-Cavlek T, Kucinar J, Ljubin-Sternak S, Kolaric B, Kaic B, Lazaric-Stefanovic L, Hunjak B, Mlinaric-Galinovic G (2012) Prevalence of Coxiella burnetii antibodies among febrile patients in Croatia, 2008–2010. Vector-Borne Zoonotic Dis 12:293–296.  https://doi.org/10.1089/vbz.2011.068 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Krčmar SJ, Ferizbegović J, Lonić E, Kamberović J (2014) Hard tick infestation of dogs in the Tuzla area (Bosnia and Herzegovina). Vet Arhiv 84:177–182. ISSN 0372-5480Google Scholar
  21. 21.
    Schüle C, Rehbein S, Shukullari E, Rapti D, Reese S, Silaghi C (2016) Police dogs from Albania as indicators of exposure risk to Toxoplasma gondii, Neospora caninum and vector-borne pathogens of zoonotic and veterinary concern. Vet Parasitol 1–2:35–46.  https://doi.org/10.1016/j.vprsr.2016.03.004 CrossRefGoogle Scholar
  22. 22.
    Vuković M (1997) Distribution/Fauna of ticks in the central and southern region of SR Montenegro, specialist work. Faculty of Veterinary Medicine, University of Belgrade, Serbia, p 50Google Scholar
  23. 23.
    Andrić B, Lako B, Vučinić N, Janković S, Komatina G, Boljević B, Drašković D, Lalović S (1996) Tick born typhus was registered for the first time in Montenegro. In: 8th European Congress of clinical Microbiology and Infectious diseases 3, 2: 341Google Scholar
  24. 24.
    Andric B, Mijovic G, Terzic D, Dupanovic B (2012) Vector borne transmissible zoonozes in Montenegro. J IMAB 18:220–225.  https://doi.org/10.5272/jimab.2012181.220 CrossRefGoogle Scholar
  25. 25.
    Andrić B (2014) Diagnostic evaluation of Ehrlichia canis human infections. Open J Med Microbiol 4:132–139.  https://doi.org/10.4236/ojmm.2014.42015 CrossRefGoogle Scholar
  26. 26.
    Lausevic D (2001) Prevalence of Coxiella burnetii antibodies in sheep in the territory of Montenegro. Acta Vet 51:149–156Google Scholar
  27. 27.
    Solano-Gallego L, Caprì A, Pennisi GM, Caldin M, Furlanello T, Trotta M (2015) Acute febrile illness is associated with Rickettsia spp. infection in dogs. Parasite Vector 8:216.  https://doi.org/10.1186/s13071-015-0824-3 CrossRefGoogle Scholar
  28. 28.
    Pennisi MG, Capri A, Solano-Gallego L, Lombardo G, Torina A, Masucci M (2012) Prevalence of antibodies against Rickettsia conorii, Babesia canis, Ehrlichia canis, and Anaplasma phagocytophilum antigens in dogs from the Stretto di Messina area (Italy). Ticks Tick Borne Dis 3:315–318.  https://doi.org/10.1016/j.ttbdis.2012.10.026 CrossRefPubMedGoogle Scholar
  29. 29.
    Punda-Polic V, Leko-Grbic J, Radulovic S (1995) Prevalence of antibodies to rickettsiae in the north-western part of Bosnia and Herzegovina. Eur J Epidemiol 11:697–699 PMID: 8861855 CrossRefGoogle Scholar
  30. 30.
    Lj Spasojević Kosić, Savić S, Potkonjak A, Vračar V (2015) Retrospective analysis of clinical and laboratory findings in hunting dogs with serologic reactions to tick-borne pathogens (Anaplasma phagocytophilum, Borrelia burgdorferi, Babesia canis, Ehrlichia canis, Rickettsia conorii). Vet Glasnik 69:231–244.  https://doi.org/10.2298/VETGL1504219S CrossRefGoogle Scholar
  31. 31.
    Harrus S, Waner T (2011) Diagnosis of canine monocytotropic ehrlichiosis (Ehrlichia canis): an overview. Vet J 187:292–296.  https://doi.org/10.1016/j.tvjl.2010.02.001 CrossRefPubMedGoogle Scholar
  32. 32.
    Cardenas AM, Doyle CK, Zhang X, Nethery K, Corstvet RE, Walker DH, McBride JW (2007) Enzyme-linked immunosorbent assay with conserved immunoreactive glycoproteins gp36 and gp19 has enhanced sensitivity and provides species-specific immunodiagnosis of Ehrlichia canis infection. Clin Vaccine Immunol 14:123–128.  https://doi.org/10.1128/cvi.00361-06 CrossRefPubMedGoogle Scholar
  33. 33.
    Sainz A, Roura X, Miró G, Estrada-Peña A, Kohn B, Harrus S, Solano-Gallego L (2015) Guideline for veterinary practitioners on canine ehrlichiosis and anaplasmosis in Europe. Parasite Vector 8:75.  https://doi.org/10.1186/s13071-015-0649-0 CrossRefGoogle Scholar
  34. 34.
    Harrus S, Kass PH, Klement E, Waner T (1997) Canine monocytic ehrlichiosis: a retrospective study of 100 cases, and an epidemiological investigation of prognostic indicators for the disease. Vet Rec 141:360–363 PMID: 9351185 CrossRefGoogle Scholar
  35. 35.
    Kottadamane RM, Dhaliwal SP, Singla DL, Bansal KB, Uppal KS (2017) Clinical and hematobiochemical response in canine monocytic ehrlichiosis seropositive dogs of Punjab. Vet World 10:255–261.  https://doi.org/10.14202/vetworld.2017.255-261 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Cardoso L, Mendao C, Madeira de Carvalho L (2012) Prevalence of Dirofilaria immitis, Ehrlichia canis, Borrelia burgdorferi sensu lato, Anaplasma spp. and Leishmania infantum in apparently healthy and CVBD-suspect dogs in Portugal-a national serological stud. Parasite Vector 5:62.  https://doi.org/10.1186/1756-3305-5-62 CrossRefGoogle Scholar
  37. 37.
    Batmaz H, Nevo E, Waner T, Senturk S, Yilmaz Z, Harrus S (2001) Seroprevalence of Ehrlichia canis antibodies among dogs in Turkey. Vet Rec 148:665–666 PMID: 11400989 CrossRefGoogle Scholar
  38. 38.
    Geromichalou A, Faixová Z (2017) Haematopathological changes in dogs affected with Ehrlichia canis in Lesvos. Folia Vet 61:44–49.  https://doi.org/10.1515/fv-2017-0017 CrossRefGoogle Scholar
  39. 39.
    Amusategui I, Tesouro MA, Kakoma I, Sainz A (2008) Serological reactivity to Ehrlichia canis, Anaplasma phagocytophilum, Neorickettsia risticii, Borrelia burgdorferi and Rickettsia conorii in dogs from northwestern Spain. Vector Borne Zoonotic Dis 8:797–803.  https://doi.org/10.1089/vbz.2007.0277 CrossRefPubMedGoogle Scholar
  40. 40.
    Farkas R, Gyurkovszky M, Lukacs Z, Aladics B, Solymosi N (2014) Seroprevalence of some vector-borne infections of dogs in Hungary. Vector Borne Zoonotic Dis 14:256–260.  https://doi.org/10.1089/vbz.2013.1469 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Pantchev N, Schaper R, Limousin S, Norden N, Weise M, Lorentzen L (2009) Occurrence of Dirofilaria immitis and tick-borne infections caused by Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato and Ehrlichia canis in domestic dogs in France: results of a countrywide serologic survey. Parasitol Res 105:S101–S114.  https://doi.org/10.1016/j.pt.2010.01.007 CrossRefPubMedGoogle Scholar
  42. 42.
    Perez Vera C, Kapiainen S, Junnikkala S, Aaltonen K, Spillmann T, Vapalahti O (2014) Survey of selected tick-borne diseases in dogs in Finland. Parasite Vector 7:285.  https://doi.org/10.1186/1756-3305-7-285 CrossRefGoogle Scholar
  43. 43.
    Mircean V, Dumitrache MO, Gyorke A, Pantchev Jodies R, Mihalca AD, Cozma V (2012) Seroprevalence and geographic distribution of Dirofilaria immitis and tick-borne infections (Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato, and Ehrlichia canis) in dogs from Romania. Vector Borne Zoonotic Dis 12:595–604.  https://doi.org/10.1089/vbz.2011.0915 CrossRefPubMedGoogle Scholar
  44. 44.
    Hamel D, Rohrig E, Pfister K (2011) Canine vector-borne disease in travelled dogs in Germany a retrospective evaluation of laboratory data from the years 2004–2008. Vet Parasitol 181:31–36.  https://doi.org/10.1016/j.vetpar.2011.04.020 CrossRefPubMedGoogle Scholar
  45. 45.
    Bogićević N, Elezović Radovanović M, Vasić A, Manić M, Marić J, Vojinović D, Rogožarski D, Gligić A, Valčić M (2017) Seroprevalence of Ehrlichia canis infection in stray dogs from Serbia. Mac Vet Rev 40:37–42.  https://doi.org/10.1515/macvetrev-2016-0096 CrossRefGoogle Scholar
  46. 46.
    Bessas A, Leulmi H, Bitam I, Zaidi S, Ait-Oudhia K, Raoult D, Parola P (2016) Molecular evidence of vector-borne pathogens in dogs and cats and their ectoparasites in Algiers, Algeria. Comp Immunol Microb 45:23–28.  https://doi.org/10.1016/j.cimid.2016.01.002 CrossRefGoogle Scholar
  47. 47.
    Cooper A, Hedlefs R, Ketheesan N, Govan B (2011) Serological evidence of Coxiella burnetii infection in dogs in a regional centre. Aust Vet J 89:385–387.  https://doi.org/10.1111/j.1751-0813.2011.00819.x CrossRefPubMedGoogle Scholar
  48. 48.
    Shapiro AJ, Norris JM, Heller J, Brown G, Malik R, Bosward KL (2016) Seroprevalence of Coxiella burnetii in Australian dogs. Zoonoses Public Health 63:458–466.  https://doi.org/10.1111/zph.12250 CrossRefPubMedGoogle Scholar
  49. 49.
    Boni M, Davoust B, Tissot-Dupont H, Raoult D (1998) Survey of seroprevalence of Q fever in dogs in the southeast of France, French Guyana, Martinique, Senegal and the Ivory Coast. Vet Microbiol 64:1–5 PMID: 9874098 CrossRefGoogle Scholar

Copyright information

© Witold Stefański Institute of Parasitology, Polish Academy of Sciences 2019
corrected publication 2019

Authors and Affiliations

  1. 1.PI Diagnostic Veterinary Laboratory in PodgoricaPodgoricaMontenegro
  2. 2.Department of Parasitology, Faculty of Veterinary MedicineUniversity of BelgradeBelgradeSerbia
  3. 3.Department of Animal Hygiene, Faculty of Veterinary MedicineUniversity of BelgradeBelgradeSerbia
  4. 4.Department of Infectious Animal Diseases and Bee Diseases, Faculty of Veterinary MedicineUniversity of BelgradeBelgradeSerbia

Personalised recommendations