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.
Similar content being viewed by others
Change history
17 December 2019
Due to an unfortunate error during the processing of the article, the given name and family name of all authors were interchanged. The original article has been corrected.
References
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
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
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
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
Procajło A, Mikulska Skupień E, Bladowski M, Lew S (2011) Monocytic ehrlichiosis in dogs. Pol J Vet Sci 14:515–520 (PMID: 21957751)
Perez M, Rikihisa Y, Bohai W (1996) Ehrlichia canis—like agent isolated from a man in Venezuela: antigenic and genetic characterization. J Clin Microbiol 34:2133–2139
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
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
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
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
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
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
Rezaei M, Khalili M, Akhtardanesh B, Shahheidaripour S (2016) Q fever in dogs: an emerging infectious disease in Iran. J Med Bacteriol 5:1–6
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
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
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
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
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
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
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 0372-5480
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
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 50
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: 341
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
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
Lausevic D (2001) Prevalence of Coxiella burnetii antibodies in sheep in the territory of Montenegro. Acta Vet 51:149–156
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The original version of this article was revised: Due to an unfortunate error during the processing of the article, the given name and family name of all authors were interchanged.
Rights and permissions
About this article
Cite this article
Laušević, D., Ilić, T., Nenadović, K. et al. Seroprevalences of Rickettsia conorii, Ehrlichia canis and Coxiella burnetii in Dogs from Montenegro. Acta Parasit. 64, 769–778 (2019). https://doi.org/10.2478/s11686-019-00098-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.2478/s11686-019-00098-w