RESEARCH PAPER
Molecular evidence of Anaplasma phagocytophilum and Babesia microti co-infections in Ixodes ricinus ticks in central-eastern region of Poland
 
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1
University of Natural Sciences and Humanities, Siedlce, Poland
2
W. Stefański Institute of Parasitology of the Polish Academy of Sciences, Warsaw, Poland
3
Institute of Tuberculosis and Lung Disease, Warsaw, Poland
4
Medical University, Warsaw, Poland
 
Ann Agric Environ Med. 2012;19(1):45–49
KEYWORDS
ABSTRACT
The aim of the study was to elucidate the distribution of Anaplasma phagocytophilum and Babesia microti co-infection in Ixodes ricinus populations within the central-eastern region of Poland. The prevalence of analysed tick-borne human pathogens in single and polymicrobial infections in I. ricinus ticks were analysed using the conventional and nested PCR techniques. A total number of 1,123 questing tick individuals (291 females, 267 males and 565 nymphs) were collected at different ecosystems (municipal parks, suburban forests, and woodlands). In the presented study, 95 samples of ticks (8.5%) were infected with A.phagocytophilum, 3.1% (n=35) with B. microti, whereas the co-existence status of these human pathogens was detected in 1.8% (n=20) of all tested samples. It has been demonstrated that the prevalence of co-infection status was the highest among females of I. ricinus (11 samples, 3.8%), whereas the lowest within tested nymphs (5 samples, 0.9%). Ticks collected at city parks in Warsaw and suburban areas of this town characterized the highest prevalence of co-infections (3.3 and 4.8%, respectively). Furthermore, it was established that co-infection rates of ticks inhabiting woodlands within Kampinos National Park and Nadbużański Landscape Park were similar and reached the levels of 1.4% (n=5) and 1.1% (n=4), respectively.
 
REFERENCES (41)
1.
Angelakis E, Billeter SA, Breitschwerdt EB, Chomel BB, Raoult D. Potential for tick-borne bartonelloses. Emerg Infect Dis. 2010; 16: 385-391.
 
2.
Castellaw AH, Chenney EF, Varela-Stokes AS. Tick-borne disease agents in various wildlife from Mississippi. Vector Borne Zoonotic Dis. 2011, 11(4): 439-442.
 
3.
Daniel M, Materna J, Hőnig V, Metelka L, Danielová V, Harčarik J, Kligrová S, Grubhoffer L. Vertical distribution of the tick Ixodes ricinus and tick-borne pathogens in the northern Moravian mountains correlated with climate warming (Jeseníky Mts., Czech Republic). Cent Eur J Public Health. 2009; 17: 139-145.
 
4.
Lempereur L, De Cat A, Caron Y, Madder M, Claerebout E, Saegerman C, Losson B. First molecular evidence of potentially zoonotic Babesia microti and Babesia sp. EU1 in Ixodes ricinus ticks in Belgium. Vector Borne Zoonotic Dis. 2011; 11: 125-130.
 
5.
Severinsson K, Jaenson TG, Pettersson J, Falk K, Nilsson K. Detection and prevalence of Anaplasma phagocytophilum and Rickettsia helvetica in Ixodes ricinus ticks in seven study areas in Sweden. Parasit Vectors 2010, 3:66, DOI: 10.1186/1756-3305-3-66.
 
6.
Tokarz R, Jain K, Bennett A, Briese T, Lipkin WI. Assessment of polymicrobial infections in ticks in New York State. Vector Borne Zoonotic Dis. 2010; 10: 217-221.
 
7.
Doudier B, Olano J, Parola P, Brouqui P. Factors contributing to emergence of Ehrlichia and Anaplasma spp. as human pathogens. Vet Parasitol. 2010; 167: 149-159.
 
8.
Heyman P, Cochez C, Hofhuis A, van der Giessen J, Sprong H, Porter SR, Losson B, Saegerman C, Donoso-Mantke O, Niedrig M, Papa A. A clear and present danger: tick-borne diseases in Europe. Expert Rev Anti Infect Ther. 2010; 8: 33-50.
 
9.
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: 2923-2931.
 
10.
Blaschitz M, Narodoslavsky-Gfoller M, Kanzler M, Stanek G, Walochnik J. Babesia species occurring in Austrian Ixodes ricinus ticks. Appl Environ Microbiol. 2008; 74: 4841-4846.
 
11.
Hildebrandt A, Pauliks K, Sachse S, Straube E. Coexistence of Borrelia spp. and Babesia spp. in Ixodes ricinus ticks in middle Germany. Vector Borne Zoonotic Dis. 2010; 10: 831-837.
 
12.
Karbowiak G. Zoonotic reservoir of Babesia microti in Poland. Pol J Microbiol. 2004; 53(Suppl.): 61-65.
 
13.
Sytykiewicz H, Pucyk A. Detection of Babesia sp. DNA in common tick population occuring at Kampinos National Park. In: Buczek A, Błaszak C (Eds): Stawonogi – środowisko, patogeny i żywiciele. Wyd. Koliber, Lublin 2007; 147 152.
 
14.
Siński E. Wpływ konfekcji u kleszczy (Ixodidae) na transmisję mikropasożytów krwi. Wiad Parazytol. 2009; 55: 341-347.
 
15.
Halos L, Bord S, Cotté V, Gasqui P, Abrial D, Barnouin J, Boulouis H-J, Vayssier-Taussat M, Vourc’h G. Ecological factors characterizing the prevalence of bacterial tick-borne pathogens in Ixodes ricinus ticks in pastures and woodlands. Appl Environ Microbiol. 2010; 76: 4413-4420.
 
16.
Dietrich F, Schmidgen T, Maggi RG, Richter D, Matuschka F-R, Vonthein R, Breitschwerdt EB, Kempf VAJ. Prevalence of Bartonella henselae and Borrelia burgdorferi sensu lato DNA in Ixodes ricinus ticks in Europe. Appl Environ Microbiol. 2010; 76: 1395-1398.
 
17.
Aktas M, Vatansever Z, Altay K, Aydin MF, Dumanli N. Molecular evidence for Anaplasma phagocytophilum in Ixodes ricinus from Turkey. Trans R Soc Trop Med Hyg. 2010; 104: 10-15.
 
18.
Franke J, Fritzsch J, Tomaso H, Straube E, Dorn W, Hildebrandt A. Coexistence of pathogens in host-seeking and feeding ticks within a single natural habitat in central Germany. Appl Environ Microbiol. 2010; 76: 6829-6836.
 
19.
Nonaka E, Ebel GD, Wearing HJ. Persistence of pathogens with short infectious periods in seasonal tick populations: the relative importance of three transmission routes. PLoS ONE 2010; 5: e11745.
 
20.
Torina A, Alongi A, Scimeca S, Vicente J, Caracappa S, de la Fuente J. Prevalence of tick-borne pathogens in ticks in Sicily. Transbound Emerg Dis. 2010; 57: 46-48.
 
21.
Václav R, Ficová M, Prokop P, Betáková T. Associations between coinfection prevalence of Borrelia lusitaniae, Anaplasma sp., and Rickettsia sp. in hard ticks feeding on reptile hosts. Microb Ecol. 2011; 61: 245-253.
 
22.
Grzeszczuk A, Stańczak J, Kubica-Biernat B. Serological and molecular evidence of human granulocytic ehrlichiosis focus in the Białowieża Primeval Forest (Puszcza Białowieska), northeastern Poland. Eur J Clin Microbiol Infect Dis. 2002; 21: 6-11.
 
23.
Stańczak J, Gable RM, Kruminis-Łozowska W, Carewicz M, Kubica-Biernat B. Ixodes ricinus as a vector of Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum and Babesia microti in urban and suburban forests. Ann Agric Environ Med. 2004; 11: 109-114.
 
24.
Persing DH, Mathiesen D, Marshall WF, Telford SR, Spielman A, Thomford JW, Conrad PA. Detection of Babesia microti by polymerase chain reaction. J Clin Microbiol. 1992; 30: 2097-2103.
 
25.
Masuzawa T, Kharitonenkov IG, Okamoto Y, Fukui T, Ohashi N. Prevalence of Anaplasma phagocytophilum and its coinfection with Borrelia afzelii in Ixodes ricinus and Ixodes persulcatus ticks inhabiting Tver Province (Russia) – a sympatric region for both tick species. J Med Microbiol. 2008; 57: 986-991.
 
26.
Wójcik-Fatla A, Szamańska J, Wdowiak L, Buczek A, Dutkiewicz J. Coincidence of three pathogens (Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum and Babesia microti) in Ixodes ricinus ticks in the Lublin macroregion. Ann Agric Environ Med. 2009; 16: 151-158.
 
27.
Halos L, Jamal T, Maillard R, Beugnet F, Le Menach A, Boulouis H-J, Vayssier-Taussat M. Evidence of Bartonella sp. in questing adult and nymphal Ixodes ricinus ticks from France and co-infection with Borrelia burgdorferi sensu lato and Babesia sp. Vet Res. 2005; 36: 79-87.
 
28.
Hildebrandt A, Straube E, Neubauer H, Schmoock G. Coxiella burnetii and co-infections in Ixodes ricinus ticks in central Germany. Vector Borne Zoonotic Dis. 2010, DOI:10.1089/vbz.2010.0180 [ahead of print].
 
29.
Koči J, Movila A, Taragel’ová V, Toderas I, Uspenskaia I, Derdáková M, Labuda M. First report of Anaplasma phagocytophilum and its coinfections with Borrelia burgdorferi sensu lato in Ixodes ricinus ticks (Acari: Ixodidae) from Republic of Moldova. Exp Appl Acarol. 2007; 41: 147-152.
 
30.
Nieto NC, Foley JE. Meta-analysis of coinfection and coexposure with Borrelia burgdorferi and Anaplasma phagocytophilum in humans, domestic animals, wildlife, and Ixodes ricinus-complex ticks. Vector Borne Zoonotic Dis. 2009; 9: 93-101.
 
31.
Swanson SJ, Neitzel D, Reed KD, Belongia EA. Coinfections acquired from Ixodes ticks. Clin Microbiol Rev. 2006; 19: 708-727.
 
32.
Toledo Á, Olmeda AS, Escudero R, Jado I, Valcárcel F, Casado-Nistal MA, Rodríguez-Vargas M , Gil H, Anda P. Tick-borne zoonotic bacteria in ticks collected from central Spain. Am J Trop Med Hyg. 2009; 81: 67-74.
 
33.
Vennestrøm J, Egholm H, Jensen PM. Occurrence of multiple infections with different Borrelia burgdorferi genospecies in Danish Ixodes ricinus nymphs. Parasitol Int. 2008; 57: 32-37.
 
34.
Vorou RM, Papavassiliou VG, Tsiodras S. Emerging zoonoses and vector-borne infections affecting humans in Europe. Epidemiol Infect. 2007; 135: 1231-1247.
 
35.
Zygner W, Bąska P, Wiśniewski M, Wędrychowicz H. The molecular evidence of Babesia microti in hard ticks removed from dogs in Warsaw (central Poland). Pol J Microbiol. 2010; 59: 95-97.
 
36.
Hildebrandt A, Hunfeld KP, Baier M, Krumbholz A, Sachse S, Lorenzen T, Kiehntopf M, Fricke HJ, Straube E. First confimed autochtonous case of human Babesia microti infection in Europe. Eur J Clin Microbiol Infect Dis. 2007; 26: 595-601.
 
37.
Becker CA, Bouju-Albert A, Jouglin M, Chauvin A, Malandrin L. Natural transmission of zoonotic Babesia spp. by Ixodes ricinus ticks. Emerg Infect Dis. 2009; 15; 320-322.
 
38.
Bonnet S, Brisseau N, Hermouet A, Jouglin M, Chauvin A. Experimental in vitro transmission of Babesia sp. (EU1) by Ixodes ricinus. Vet Res. 2009; 40: 21-28.
 
39.
Casati S, Sager H, Gern L, Piffaretti JC. Presence of potentially pathogenic Babesia sp. for human in Ixodes ricinus in Switzerland. Ann Agric Environ Med. 2006; 13: 65-70.
 
40.
Häselbarth K, Tenter AM, Brade V, Krieger G, Hunfeld KP. First case of human babesiosis in Germany-clinical presentation and molecular characterisation of the pathogen. Int J Med Microbiol. 2007; 297: 197-204.
 
41.
Hunfeld KP, Brade V. Zoonotic Babesia: possibly emerging pathogens to be considered for tick-infested humans in Central Europe. Int J Med Microbiol. 2004; 293(Suppl. 37): 93-103.
 
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