REVIEW PAPER
The role of companion animals in the environmental circulation of tick-borne bacterial pathogens
 
More details
Hide details
1
Department of Genetics, Faculty of Biology, University of Szczecin, Poland
CORRESPONDING AUTHOR
Bogumiła Skotarczak   

Department of Genetics, Faculty of Biology, University of Szczecin, Felczaka 3c, 71-412 Szczecin, Poland
 
Ann Agric Environ Med. 2018;25(3):473–480
KEYWORDS
TOPICS
ABSTRACT
Ticks are known as vectors of a wide range of pathogens of medical and veterinary importance; some of them of zoonotic concern constitute a hazard for the emergence of tick-borne diseases shared between humans and domestic animals and becoming a part of the ‘One Health’ concept. Canine and feline tick-borne diseases have emerged in recent years, performing an extensive geographic distribution and enlarged global prevalence. The present review focuses on the recent epidemiological studies on the emergence of tick-borne bacterial pathogens in dogs and cats, and the discussion whether pet ownership increases the risk of tick-borne diseases. A lot of data provide confirmation that dogs and cats themselves may substantially contribute to the circulation of the ticks and tick-borne bacterial pathogens in the environment. Molecular diagnostics of tick-borne pathogens infections generates a lot of problems like the choice of molecular methods and molecular markers for the detection of bacterial genomic DNA, but play an important role in the diagnosis of infections. The study provides some insight into molecular diagnostic techniques and new potentially recognized bacterial pathogens of this group. Protecting human and companion animal health from vector-borne infections requires controlling vector populations, containing development of novel, practicable strategies that will limit vectors and transmission of vector-borne disease pathogens.
 
REFERENCES (103)
1.
Beugneta F, Marié J-L. Emerging arthropod-borne diseases of companion animals in Europe. Vet Parasitol. 2009; 163(4): 298–305. doi: 10.1016/j.vetpar.2009.03.028. Epub 2009 Mar 26.
 
2.
Otranto D, Dantas-Torres F. Canine and feline vector-borne diseases in Italy: current situation and perspectives. Parasit Vectors 2010; 3: 2. doi: 10.1186/1756-3305-3-2.
 
3.
Skotarczak B. Babesiosis as a disease of people and dogs. Molecular diagnostics: a review. Vet Med. 2008; 53(5): 229–235.
 
4.
Claerebout E, Losson B, Cochez C, Casaert S, Dalemans AC, De Cat A, et al. Ticks and associated pathogens collected from dogs and cats in Belgium. Parasit Vectors 2013; 6: 183. doi: 10.1186/1756-3305-6-183.
 
5.
Maia C, Ramos C, Coimbra M, Bastos F, Martins Â, Pinto P, Nunes M, Vieira ML, Cardoso L, Campino L. Bacterial and protozoal agents of feline vector-borne diseases in domestic and stray cats from southern Portugal. Parasit Vectors 2014; 7: 115. doi: 10.1186/1756-3305-7-115.
 
6.
Maia C, Almeida B, Coimbra M, Fernandes MC, Cristóvão JM, Ramos C, et al. Bacterial and protozoal agents of canine vector-borne diseases in the blood of domestic and stray dogs from southern Portugal. Parasit Vectors 2015; 23(8): 138. doi: 10.1186/s13071-015-0759-8.
 
7.
Little SE. Future challenges for parasitology: Vector control and one health in the Americas Vet Parasitol. 2013; 195(3-4): 249–255. doi: 10.1016/j.vetpar.2013.04.006.
 
8.
Mencke N. Future challenges for parasitology: Vector control and 'One health' in Europe: The veterinary medicinal view on CVBDs such as tick borreliosis, rickettsiosis and canine leishmaniosis. Vet Parasitol. 2013; 195: 256–271. doi: 10.1016/j.vetpar.2013.04.007. Epub 2013 Apr 6.
 
9.
Day MJ. One health: the importance of companion animal vector-borne diseases. Parasit Vectors 2011; 4: 49. doi: 10.1186/1756-3305-4-49.
 
10.
Kaplan B, Kahn LH, Monath TP, Woodall J. ‘One Health' and parasitology. Parasit Vectors 2009; 2: 36. doi: 10.1186/1756-3305-2-36.
 
11.
Brown C. Emerging diseases: the global express. Vet Pathol. 2010; 47: 9–14. Doi: 10.1177/0300985809354351.
 
12.
Rizzoli A, Silaghi C, Obiegala A, Rudolf I, Hubálek Z, Földvári G, et al. Ixodes ricinus and its transmitted pathogens in urban and peri-urban areas in Europe: new hazards and relevance for public health. Front Pub Health 2014; 2: 251. doi: 10.3389/fpubh.2014.00251. eCollection 2014.
 
13.
Kilpatrick AM, Randolph SE. Drivers, dynamics, and control of emerging vector-borne zoonotic diseases. Lancet 2012; 380: 1946–1955. doi: 10.1016/S0140-6736(12)61151-9.
 
14.
Randolph SE. Tick-borne disease systems emerge from the shadows: the beauty lies in molecular detail, the message in epidemiology. Parasitology 2009; 136: 1403–1413. doi: 10.1017/S0031182009005782. Epub 2009 Apr 14.
 
15.
Pfäffle M, Littwin N, Muders SV, Petney TN. The ecology of tick-borne diseases. Int J Parasitol. 2013; 43(12–13): 1059–1077. doi: 10.1016/j.ijpara.2013.06.009. Epub 2013 Aug 1.
 
16.
Wodecka B, Rymaszewska A, Skotarczak B. Host and pathogen DNA identification in blood meals of nymphal Ixodes ricinus ticks from forest parks and rural forests of Poland. Exp Appl Acarol. 2014; 62: 543–555. doi: 10.1007/s10493-013-9763-x. Epub 2013 Dec 19.
 
17.
Ginsberg HS, Faulde MK. Ticks. In: X. Bonnefoy, H. Kampen and K. Sweeney (Eds.), Public Health Significance of Urban Pests. Copenhagen: World Health Organization 2008; pp. 303–345.
 
18.
Król N, Obiegała A, Pfeffer M, Lonc E, Kiewra D. Detection of selected pathogens in ticks collected from cats and dogs in the Wrocław Agglomeration, South-West Poland. Parasit Vectors 2016; 9(1): 351. doi: 10.1186/s13071-016-1632-0.
 
19.
Little SE, Heise SR, Blagburn BL, Callister SM, Mead PS. Lyme borreliosis in dogs and humans in the USA. Trends Parasitol. 2010; 26(4): 213–218. doi: 10.1016/j.pt.2010.01.006. Epub 2010 Mar 6.
 
20.
Kybicová K, Schánilec P, Hulínská D, Uherková L, Kurzová Z, Spejchalová S. Detection of Anaplasma phagocytophilum and Borrelia burgdorferi sensu lato in dogs in the Czech Republic. Vector Born Zoon Dis. 2009; 9(6): 655–661. doi: 10.1089/vbz.2008.0127.
 
21.
Barth C, Straubinger RK, Sauter-Louis C, Hartmann K. Prevalence of antibodies against Borrelia burgdorferi sensu lato and Anaplasma phagocytophilum and their clinical relevance in dogs in Munich, Germany. Berl. Munch. Tierarztl. Wochenschr. 2012; 125(7-8): 337–344.
 
22.
Ebani VV, Bertelloni F, Torracca B, Cerri D. Serological survey of Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum, and Ehrlichia canis infections in rural and urban dogs in Central Italy. Ann Agric Environ Med. 2014; 21(4): 671–675. doi: 10.5604/12321966.1129912.
 
23.
Skotarczak B, Wodecka B. Molecular evidence of the presence of Borrelia burgdorferi sensu lato in the blood samples taken from dogs in Poland. Ann Agric Environ Med. 2003; 10: 113 – 115.
 
24.
Skotarczak B, Wodecka B. Identification of Borrelia burgdorferi genospecies inducing Lyme disease in dogs from Poland. Acta Vet Hun. 2005; 53: 12–21.
 
25.
Skotarczak B, Wodecka B, Rymaszewska A, Sawczuk M, Maciejewska A, Adamska M, et al. Prevelance of DNA and antibodies to Borrelia burgdorferi sensu lato in dogs suspected of borreliosis. Ann Agric Environ Med. 2005; 12(2): 199–205.
 
26.
Wodecka B, Rymaszewska A, Sawczuk M, Skotarczak B. Detectability of tick-borne agents DNA in the blood of dogs, undergoing treatment for borreliosis. Ann Agric Environ Med. 2009; 16(1): 9–14.
 
27.
Zygner W, Górski P, Wedrychowicz H. Detection of the DNA of Borrelia afzelii: Anaplasma phagocytophilum and Babesia canis in blood samples from dogs in Warsaw. Vet Rec. 2009; 164: 465–467.
 
28.
Skotarczak B. Methods for parasitic protozoans detection in the environmental samples. Parasite 2009; 16: 183–190.
 
29.
Hovius J, Hovius K, Oei A, Houwers D, Dam A. Antibodies against specific proteins of and immobilizing activity against three strains of Borrelia burgdorferi sensu lato can be found in symptomatic but not in infected asymptomatic dogs. J Clin Microbiol. 2000; 38: 2611–2621.
 
30.
Rauter C, Hartung T. Prevalence of Borrelia burgdorferi sensu lato genospecies in Ixodes ricinus ticks in Europe: a metaanalysis. Appl Environ Microbiol. 2005; 71(11): 7203–7216.
 
31.
Wilhelmsson P, Fryland L, Börjesson S, Nordgren J, Bergström S, Ernerudh J, et al. Prevalence and diversity of Borrelia species in ticks that have bitten humans in Sweden. J Clin Microbiol. 2010; 48(11): 4169–4176. doi: 10.1128/JCM.01061-10. Epub 2010 Sep 15.
 
32.
Nijhof AM, Bodaan C, Postigo M, Nieuwenhuijs H, Opsteegh M, Franssen L, et al. Ticks and associated pathogens collected from domestic animals in the Netherlands. Vector Born Zoon Dis. 2007; 7(4): 585–595.
 
33.
Kesteman T, Rossi C, Bastien P, Brouillard J, Avesani V, Olive N, et al. Prevalence and genetic heterogeneity of Borrelia burgdorferi sensu lato in Ixodes ticks in Belgium. Acta Clin Belg. 2010; 65(5): 319–322.
 
34.
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(9): 2923–2931. doi: 10.1128/AEM.03061-09. Epub 2010 Mar 12.
 
35.
Wodecka B, Skotarczak B. First isolation of Borrelia lusitaniae DNA from Ixodes ricinus ticks in Poland. Scan J Infect Dis. 2005; 1: 1–9.
 
36.
Skotarczak B. Why are there several species of Borrelia burgdorferi sensu lato detected in dogs and humans? Infect Gen Evol. 2014; 23: 182–188. doi: 10.1016/j.meegid.2014.02.014. Epub 2014 Mar 5.
 
37.
Pangrácová L, Derdáková M, Pekárik L, Hviščová I, Víchová B, Stanko M, et al. Ixodes ricinus abundance and its infection with the tick-borne pathogens in urban and suburban areas of Eastern Slovakia. Parasit Vectors 2013; 6: 238. doi: 10.1186/1756-3305-6-238.
 
38.
Richter D, Matuschka FR. “Candidatus Neoehrlichia mikurensis”, Anaplasma phagocytophilum, and Lyme disease spirochetes in questing European vector ticks and in feeding ticks removed from people. J Clin Microbiol 2012; 50: 943–947. doi: 10.1128/JCM.05802-11. Epub 2012 Jan 11.
 
39.
Morganti G, Gavaudan S, Canonico C, Ravagnan S, Olivieri E, Diaferia M, et al. Molecular Survey on Rickettsia spp., Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato, and Babesia spp. in Ixodes ricinus ticks infesting dogs in central Italy. Vector Born Zoon Dis. 2017; 17(11): 743–748. doi: 10.1089/vbz.2017.2154. Epub 2017 Oct 12.
 
40.
Ruiz-Fons F, Fernandez-de-Mera IG, Acevedo P, Gortázar C, de la Fuente J. Factors driving the abundance of Ixodes ricinus ticks and the prevalence of zoonotic, I. ricinus-borne pathogens in natural foci. Appl Environ Microbiol. 2012; 78: 2669–2676. doi: 10.1128/AEM.06564-11. Epub 2012 Jan 27.
 
41.
Zygner W, Jaros S, Wedrychowicz H. Prevalence of Babesia canis, Borrelia afzelii, and Anaplasma phagocytophilum infection in hard ticks removed from dogs in Warsaw (central Poland). Vet Parasitol. 2008; 153: 139–142.
 
42.
Skotarczak B, Rymaszewska A, Wodecka B, Sawczuk M. Molecular evidence of coinfection of Borrelia burgdorferi sensu lato, Human Granulocytic Ehlichiosis Agent, and Babesia microti in ticks from northwestern Poland. J Parasitol. 2003; 89: 194–196.
 
43.
Cisak E, Chmielewska-Badora J, Zwoliński J, Wójcik-Fatla A, Polak J, Dutkiewicz J. Risk of tick-borne bacterial diseases among workers of Roztocze National Park (south-eastern Poland). Ann Agric Environ Med. 2005; 12: 127–132.
 
44.
Zwoliński J, Chmielewska-Badora J, Cisak E, Buczek A, Dutkiewicz J. Prevalence of antibodies to Anaplasma phagocytophilum and Borrelia burgdorferi in forestry workers from the Lublin region. (in Polish). Wiad Parazytol. 2004; 50: 221–227.
 
45.
Skotarczak B, Adamska M, Rymaszewska A, Suproń M, Sawczuk M, Maciejewska A. Anaplasma phagocytophilum and protozoans of Babesia genus in dogs from endemic areas of Lyme disease in north-western Poland. (in Polish). Wiad Parazytol. 2004; 50: 555–561.
 
46.
Rymaszewska A, Adamska M. Molecular evidence of vector-borne pathogens coinfecting dogs from Poland. Acta Vet Hung. 2011; 59: 215–223. doi: 10.1556/AVet.2011.008.
 
47.
Welc-Faleciak R, Rodo A, Siński E, Bajer A. Babesia canis and other tick-borne infections in dogs in Central Poland. Vet Parasitol. 2009; 166(3-4): 191–198. doi: 10.1016/j.vetpar.2009.09.038. Epub 2009 Sep 26.
 
48.
Alberti A, Zobba R, Chessa B, Addis MF, Sparagano O, Pinna Parpaglia ML, et al. Equine and canine Anaplasma phagocytophilum strains isolated on the island of Sardinia (Italy) are phylogenetically related to pathogenic strains from the United States. Appl Environ Microbiol. 2005; 71: 6418–6422.
 
49.
Ebani V, Cerri D, Fratini F, Ampola M, Andreani E. Seroprevalence of Anaplasma phagocytophilum in domestic and wild animals from central Italy. New Microbiol. 2008; 31: 371–375.
 
50.
Hamel D, Bodarenko A, Silaghi C, Nolte I, Pfister K. Seroprevalence and bacteremia of Anaplasma phagocytophilum in cats from Bavaria and Lower Saxony (Germany). Berl Münch Tierärztl Wochenschr. 2012; 125: 163–167.
 
51.
Alves AS, Milhano N, Santo-Silva M, Santos AS, Vilhena M, De Sousa R. Evidence of Bartonella spp., Rickettsia spp. and Anaplasma phagocytophilum in domestic, shelter and stray cat blood and fleas, Portugal. Clin Microbiol Infect Dis. 2009; 15: 1–3. doi: 10.1111/j.1469-0691.2008.02636.x. Epub 2009 Mar 26.
 
52.
Krämer F, Schaper R, Schunack B, Połozowski A, Piekarska J, Szwedko A, et al. Serological detection of Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato and Ehrlichia canis antibodies and Dirofilaria immitis antigen in a countrywide survey in dogs in Poland. Parasitol Res. 2014; 113(9): 3229–3239. doi: 10.1007/s00436-014-3985-7. Epub 2014 Jun 29.
 
53.
Welc-Falęciak R, Werszko J, Cydzik K, Bajer A, Michalik J, Behnke JM. Co-infection and genetic diversity of tick-borne pathogens in roe deer from Poland. Vector Born Zoon Dis. 2013; 13: 277–288. doi: 10.1089/vbz.2012.1136. Epub 2013 Mar 8.
 
54.
Hapunik J, Víchová B, Karbowiak G, Wita I, Bogdaszewski M, Pet'ko B. Wild and farm breeding cervids infections with Anaplasma phagocytophilum. Ann Agric Environ Med. 2011; 18(1): 73–77.
 
55.
Krücken J, Schreiber C, Maaz D, Kohn M, Demeler J, Beck S, et al. A novel high-resolution melt PCR assay discriminates Anaplasma phagocytophilum and “Candidatus Neoehrlichia mikurensis”. J Clin Microbiol. 2013; 51: 1958–1961. doi: 10.1128/JCM.00284-13. Epub 2013 Apr 10.
 
56.
Silaghi C, Beck R, Oteo JA, Pfeffer M, Sprong H. Neoehrlichiosis: an emerging tick-borne zoonosis caused by Candidatus Neoehrlichia mikurensis. Exp Appl Acarol. 2015; 68(3): 279–297. doi: 10.1007/s10493-015-9935-y. Epub 2015 Jun 17.
 
57.
Grankvist A, Andersson P-O, Mattsson M, Sender M, Vaht K, Höper L et al. Infections with the tick-borne bacterium “Candidatus Neoehrlichia mikurensis” mimic noninfectious conditions in patients with B cell malignancies or autoimmune diseases. Clin Infect Dis. 2014; 58: 1716–1722. doi: 10.1093/cid/ciu189.
 
58.
Heyman P, Cochez C, Hofhuis A, van der Giessen J, Sprong H, Porter SR, et al. A clear and present danger: tick-borne diseases in Europe. Expert Rev Anti Infect Ther. 2010; 8: 33–50. doi: 10.1586/eri.09.118.
 
59.
Michelet L, Delannoy S, Devillers E, Umhang G, Aspan A, Juremalm M, et al. High-throughput screening of tick-borne pathogens in Europe. Front. Cell Infect Microbiol. 2014; 4: 103. doi: 10.3389/fcimb.2014.00103. eCollection 2014.
 
60.
Diniz PP, Schulz BS, Hartmann K, Breitschwerdt EB. Candidatus Neoehrlichia mikurensis infection in a dog from Germany. J Clin Microbiol. 2011; 49: 2059–2062. doi: 10.1128/JCM.02327-10. Epub 2011 Mar 2.
 
61.
Beck R, Čubrić Čurik V, Račić I, Šprem N, Vujnović A. Identification of Candidatus Neoehrlichia mikurensis and Anaplasma species in wildlife from Croatia. Proceedings of the 1st Conference on Neglected Vectors and Vector-Borne Diseases (EurNegVec) Cluj-Napoca. Parasit Vectors 2014; 7(Suppl 1): O28.
 
62.
Liesner JM, Krücken J, Schaper R, Pachnicke S, Kohn B, Müller E, et al. Vector-borne pathogens in dogs and red foxes from the federal state of Brandenburg, Germany. Vet Parasitol. 2016; 224: 44–51. doi: 10.1016/j.vetpar.2016.05.012. Epub 2016 May 11.
 
63.
Pantchev N, Vrhovec MG, Pluta S, Straubinger RK. Seropositivity of Borrelia burgdorferi in a cohort of symptomatic cats from Europe based on a C6-peptide assay with discussion of implications in disease aetiology. Berl Munch Tierarztl Wochenschr. 2016; 129(7-8): 333–339.
 
64.
Magnarelli LA, Bushmich SL, IJdo JW, Fikrig E. Seroprevalence of antibodies against Borrelia burgdorferi and Anaplasma phagocytophilum in cats. Am J Vet Res. 2005; 66(11): 1895–1899.
 
65.
Pennisi MG, Hofmann-Lehmann R, Radford AD, Tasker S, Belák S, Addie DD, et al. Anaplasma, Ehrlichia and Rickettsia species infections in cats: European guidelines from the ABCD on prevention and management. J Feline Med Surg. 2017; 19(5): 542–548. doi: 10.1177/1098612X17706462.
 
66.
Gracia MJ, Marcen JM, Pinal R, Calvete C, Rodes D. Prevalence of Rickettsia and Bartonella species in Spanish cats and their flea. J Vector Ecol. 2015; 40: 233–239. doi: 10.1111/jvec.12159.
 
67.
Leschnik M, Feiler A, Duscher GG, Joachim A. Effect of owner-controlled acaricidal treatment on tick infestation and immune response to tick-borne pathogens in naturally infested dogs from Eastern Austria Parasit Vectors 2013; 6 (1): 62. doi: 10.1186/1756-3305-6-62.
 
68.
Littman MP, Goldstein RE, Labato MA, Lappin MR, Moore GE. ACVIM small animal consensus statement on Lyme disease in dogs: diagnosis, treatment, and prevention. J Vet Intern Med. 2006; 20(2): 422–434.
 
69.
De Silva AM, Fikrig E. Borrelia burgdorferi genes selectively expressed in ticks and mammals. Parasitol Today 1997; 13(7): 267–270.
 
70.
Hübner P, Waiblinger HU, Pietsch K, Brodmann P. Validation of PCR methods for quantitation of genetically modified plants in food. J AOAC Int. 2001; 84(6): 1855–1864.
 
71.
Miller JC, von Lackum K, Babb K, McAlister JD, Stevenson B. Temporal analysis of Borrelia burgdorferi Erp protein expression throughout the mammal-tick infectious cycle. Infect Immun. 2003; 71(12): 6943–6952.
 
72.
Bil-Lula I, Matuszek P, Pfeiffer T, Woźniak M. Lyme Borreliosis – the utility of improved Real-Time PCR Assay in the detection of Borrelia burgdorferi infection. Adv Clin Exp Med. 2015; 24(4): 663–670. doi: 10.17219/acem/28625.
 
73.
Schreiber C, Krücken J, Beck S, Maaz D, Pachnicke S, Krieger K, et al. Pathogens in ticks collected from dogs in Berlin/Brandenburg, Germany. Parasit Vectors 2014; 7: 535. doi: 10.1186/s13071-014-0535-1.
 
74.
Kierwa D, Zaleśny G. Relationship between temporal abundance of ticks and incidence of Lyme borreliosis in Lower Silesia regions of Poland. J Vector Ecol. 2013; 38 (2): 345–352. doi: 10.1111/j.1948-7134.2013.12050.x.
 
75.
Wodecka B, Leońska A, Skotarczak B. A comparative analysis of molecular markers for the detection and identification of Borrelia spirochetes in Ixodes ricinus. J Med Microbiol. 2010; 59: 309–314. doi: 10.1099/jmm.0.013508-0. Epub 2009 Dec 10.
 
76.
Nunes M, Parreira R, Maia C, Lopes N, Fingerle V, Vieira ML. Molecular identification of Borrelia genus in questing hard ticks from Portugal: Phylogenetic characterization of two novel Relapsing Fever-like Borrelia sp. Infect Genet Evol. 2016; 40: 266–274. doi: 10.1016/j.meegid.2016.03.008. Epub 2016 Mar 11.
 
77.
Wodecka B, Skotarczak B. Differentiation Borrelia species in environmental samples with high-resolution DNA melting analysis. Clin Lab. 2015; 61: 669–676.
 
78.
Dunaj J, Zajkowska JM, Kondrusik M, Gern L, Rais O, Moniuszko A, et al. Borrelia burgdorferi genospecies detection by RLB hybridization in Ixodes ricinus ticks from different sites of North-Eastern Poland. Ann Agric Environ Med. 2014; 21(2): 239–243. doi: 10.5604/1232-1966.1108583.
 
79.
Jahfari S, Hofhuis A, Fonville M, van der Giessen J, van Pelt W, Sprong H. Molecular detection of tick-borne pathogens in humans with tick bites and erythema migrans, in the Netherlands. PLoS Negl Trop Dis. 2016; 10(10): e0005042. doi: 10.1371/journal.pntd.0005042. eCollection 2016 Oct.
 
80.
Hamer SA, Tsao JI, Walker ED, Mansfield LS, Foster ES, Hickling GJ. Use of tick surveys and serosurveys to evaluate pet dogs as a sentinel species for emerging Lyme disease. Am J Vet Res. 2009; 70(1): 49–56. doi: 10.2460/ajvr.70.1.49.
 
81.
Cotte V, Bonnet S, Cote M, Vayssier-Taussat M. Prevalence of five pathogenic agents in questing Ixodes ricinus ticks from western France. Vec Born Zoon Dis. 2010; 10: 723–730. doi: 10.1089/vbz.2009.0066. Epub 2009 Dec 18.
 
82.
Cerar T, Ogrinc K, Cimperman J, Lotric-Furlan S, Strle F, Ruzić-Sabljić E. Validation of cultivation and PCR methods for diagnosis of Lyme neuroborreliosis. J Clin Microbiol. 2008; 46(10): 3375–3379. doi: 10.1128/JCM.00410-08. Epub 2008 Aug 20.
 
83.
Elfving K, Lukinius A, Nilsson K. Life cycle, growth characteristics and host cell response of Rickettsia helvetica in a Vero cell line. Exp Appl Acarol. 2012; 56(2): 179–187. doi: 10.1007/s10493-011-9508-7. Epub 2011 Nov 25.
 
84.
Tijsse-Klasen E, Sprong H, Pandak N. Co-infection of Borrelia burgdorferi sensu lato and Rickettsia species in ticks and in an erythema migrans patient. Parasit Vectors 2013; 10(6): 347. doi: 10.1186/1756-3305-6-347.
 
85.
Koetsveld J, Tijsse-Klasen E, Herremans T, Hovius JW, Sprong H. Serological and molecular evidence for spotted fever group Rickettsia and Borrelia burgdorferi sensu lato co-infections in The Netherlands. Ticks Tick-Borne Dis. 2016; 7(2): 371–377. doi: 10.1016/j.ttbdis.2015.12.010. Epub 2015 Dec 17.
 
86.
Summers BA, Straubinger AF, Jacobson RH, Chang YF, Appel MJ, Straubinger RK. Histopathological studies of experimental lyme disease in the dog. J Comp Pathol. 2005; 133: 1–13.
 
87.
Gerber B, Eichenberger S, Haug K, Wittenbrink MM. The dilemma with Lyme borreliosis in the dog with particular consideration of "Lyme nephritis". Schweiz Arch Tierheilkd. 2009; 151 (10): 479–483. doi: 10.1024/0036-7281.151.10.479.
 
88.
Wölfel R, Essbauer S, Dobler G. Diagnostics of tick-borne rickettsioses in Germany: A modern concept for a neglected disease. Int J Med Microbiol. 2008; 298: 368–374.
 
89.
Skotarczak B, Wodecka B, Rymaszewska A, Adamska M. Molecular evidence for bacterial pathogens in Ixodes ricinus ticks infesting Shetland ponies. Exp Appl Acarol 2016; 69(2): 179–189. doi: 10.1007/s10493-016-0027-4. Epub 2016 Feb 26.
 
90.
Courtney JW, Kostelnik LM, Zeidner NS, Massung RF. Multiplex real-time PCR for detection of Anaplasma phagocytophilum and Borrelia burgdorferi. J Clin Microbiol. 2004; 42: 3164–3168.
 
91.
Jahfari S, Fonville M, Hengeveld P, Reusken C, Scholte EJ, Takken W, Heyman P, Medlock J, Heylen D, Kleve J, Sprong H. Prevalence of Neoehrlichia mikurensis in ticks and rodents from north-west Europe. Parasit Vectors. 2012; 5: 74. doi: 10.1186/1756-3305-5-74.
 
92.
Silaghi C, Woll D, Mahling M, Pfister K, Pfeffer M. Candidatus Neoehrlichia mikurensis in rodents in an area with sympatric existence of the hard ticks Ixodes ricinus and Dermacentor reticulatus. Parasit Vectors. 2012; 5: 285. doi: 10.1186/1756-3305-5-285.
 
93.
Skotarczak B. Canine borreliosis-epidemiology and diagnostics. Ann Agric Environ Med. 2002; 9: 137–140.
 
94.
Jones EH, Hinckley AF, Hook SA, Meek JI, Backenson B, Kugeler KJ, Feldman KA. Pet ownership increases human risk of encountering ticks. Zoon Pub Health 2017; doi: 10.1111/zph.12369.
 
95.
Guerra M, Walker E, Kitron U. Canine surveillance system for Lyme borreliosis in Wisconsin and northern Illinois: geographic distribution and risk factor analysis. Am J Trop Med Hyg. 2001; 65: 546–552.
 
96.
Magnarelli LA, Anderson JF, Johnson RC. Analyses of mammalian sera in enzyme-linked immunosorbend assay with different strains of Borrelia burgdorferi sensu lato. J Wild Dis 1995; 31: 159–165.
 
97.
Magnarelli LA, Ijdo JW, Padula SJ, Flavell RA, Fikrig E. Serologic diagnosis of Lyme borreliosis by using enzyme-linked immunosorbent assays with recombinant antigens. J Clin Microbiol. 2000; 38: 1735–1739.
 
98.
Stefancikova A, Tresova G, Petko B, Skardova I, Sesztakova E. ELISA comparison of theree whole-cell antigens of Borrelia burgdorferi sensu lato in serological study of dogs from area of Kosice, eastern Slovakia. Ann Agric Environ Med. 1998; 5, 25–30.
 
99.
Straubinger RK, Straubinger AF, Harter L, Jacobson RH, Chang YF, Summers BA, et al. Borrelia burgdorferi migrates into joint capsules and causes an up-regulation of interleukin-8 in synovial membranes of dogs experimentally infected with ticks. Infect Immun. 1997; 65: 1273–1285.
 
100.
Skotarczak B, Adamska M, Sawczuk M, Maciejewska A, Wodecka B, Rymaszewska A. Coexistence of tick-borne pathogens in game animals and ticks in western Poland. Vet Med. 2008; 53: 668–675.
 
101.
Goossens HAT, Van Den Bogaard AE, Nohlmans MKE. Dogs as sentinels for human Lyme borreliosis in The Netherlands. J Clin Microbiol. 2001; 39: 844–848.
 
102.
Eng TR, Wilson ML, Spielman A, Lastavica CC. Greater risk of Borrelia burgdorferi infection in dogs than in people. J Infect Dis. 1988; 158: 1410–1411.
 
103.
Vourc'h G, Abrial D, Bord S, Jacquot M, Masséglia S, Poux V, et al. Mapping human risk of infection with Borrelia burgdorferi sensu lato, the agent of Lyme borreliosis, in a periurban forest in France. Ticks Tick-Born Dis. 2016; 7(5): 644–652. doi: 10.1016/j.ttbdis.2016.02.008. Epub 2016 Feb 6.
 
eISSN:1898-2263
ISSN:1232-1966