Molecular screening for Bartonella henselae and Borrelia burgdorferi sensu lato co-existence within Ixodes ricinus populations in central and eastern parts of Poland
More details
Hide details
University of Natural Sciences and Humanities, Siedlce, Poland
W. Stefański Institute of Parasitology of the Polish Academy of Sciences, Warsaw, Poland
Corresponding author
Hubert Sytykiewicz   

University of Natural Sciences and Humanities, Siedlce, Poland
Ann Agric Environ Med. 2012;19(3):451-456
The presented study aimed at establishing the prevalence and co-infection rates of Bartonella henselae and Borrelia burgdorferi sensu lato in Ixodes ricinus ticks collected from the central and eastern parts of Poland. The common tick individuals were gathered in the years 2008-2009. Questing ticks were sampled by dragging a white woollen flag over lower vegetation at 17 localities within diverse types of habitats: urban recreational green areas (city parks and squares), suburban forests and rural woodlands throughout the investigated regions of Poland. Detection of B. henselae in tested tick specimens was based on PCR amplification of the citrate synthase (gltA) gene, while screening for the presence of B. burgdorferi s.l. DNA was carried out by analyzing fragments of two genes: the flagellin (fla) and outer surface protein A (ospA). A total number of 1,571 I. ricinus ticks were sampled: 865 (55.1%) nymphs, 377 females (24.0%) and 329 males (20.9%). The application of PCR assays revealed that 76 (4.8%) tick samples were B. henselae-positive, B. burgdorferi s.l. DNA was detected in 194 specimens (12.3%), whereas the co-existence of these pathogens was evidenced in 22 tested ticks (1.4%). Furthermore, the occurrence of bartonellae and co-circulation of analysed microorganisms in I. ricinus was affirmed only within adult individuals, while presence of the screened spirochetes was ascertained in both nymphal and adult ticks. It should be stressed that the suburban woods of Warsaw and rural forests in Warsaw County characterized the highest prevalence levels of dual infection with investigated tick-borne pathogens, whereas the lowest co-infection rates were recorded in tick populations inhabiting rural forests in Płock County and forested areas in Korczew-Mogielnica (within the Nadbużański Landscape Park).
Florin TA, Zaoutis TE, Zaoutis LB. Beyond cat scratch disease: widening spectrum of Bartonella henselae infection. Pediatrics 2008; 121: e1413-1425. DOI: 10.1542/peds.2007-1897.
Franz B, Kempf VAJ. Adhesion and host cell modulation: critical pathogenicity determinants of Bartonella henselae. Parasit Vectors 2011; 4:54. DOI: 10.1186/1756-3305-4-54.
Breitschwerdt EB, Maggi RG, Lantos PM, Woods CW, Hegarty BC, Bradley JM. Bartonella vinsonii subsp. berkhoffii and Bartonella henselae bacteremia in a father and daughter with neurological disease. Parasit Vectors 2010; 3:29. DOI: 10.1186/1756-3305-3-29.
Scheidegger F, Quebatte M, Mistl C, Dehio C. The Bartonella henselae VirB/Bep system interferes with vascular endothelial growth factor (VEGF) signalling in human vascular endothelial cells. Cell Microbiol. 2011; 13: 419-431.
Truttmann MC, Guye P, Dehio C. BID-F1 and BID-F2 domains of Bartonella henselae effector protein BepF trigger together with BepC the formation of invasome structures. PLoS ONE 2011; 6 (10): e25106. DOI: 10.1371/journal.pone.0025106.
Chomel BB, Kasten RW. Bartonellosis, an increasingly recognized zoonosis. J Appl Microbiol. 2010; 109: 743-750.
Liu Q, Eremeeva ME, Li D. Bartonella and Bartonella infections in China: from the clinic to the laboratory. Comp Immunol Microbiol Infect Dis. 2012; 35 (2): 93-102. DOI: 10.1016/j.cimid.2012.01.002.
Kaçar N, Taşli L, Demirkan N, Ergin C, Ergin S. HIV-negative case of bacillary angiomatosis with chronic hepatitis B. J Dermatol. 2010; 37(8): 722-725.
Dehio C. Recent progress in understanding Bartonella-induced vascular proliferation. Curr Opin Microbiol. 2003; 6: 61-65.
Mosepele M, Mazo D, Cohn J. Bartonella infection in immunocompromised hosts: immunology of vascular infection and vasoproliferation. Clin Dev Immunol. 2012; Article ID 612809. DOI: 10.1155/2012/612809.
Pulliainen AT, Dehio C. Persistence of Bartonella spp. stealth pathogens: from subclinical infections to vasoproliferative tumor formation. FEMS Microbiol Rev. 2012; 36(3): 563-599.
McCord AM, Resto-Ruiz SI, Anderson BE. Autocrine role for interleukin-8 in Bartonella henselae-induced angiogenesis. Infect Immun. 2006; 74(9): 5185-5190.
Deng H, Le Rhun DC, Cotte V, Buffet JP, Read A, Birtles RJ, Vayssier-Taussat M. Strategies of exploitation of mammalian reservoirs by Bartonella species. Vet Res. 2012, 43(1): 15. DOI: 10.1186/1297-9716-43-15.
Pitassi LHU, Magalhães RF, Barjas-Castro ML, de Paula EV, Ferreira MRM, Velho PENF. Bartonella henselae infects human erythrocytes. Ultrastruct Pathol. 2007; 31(6): 369-372.
Billeter SA, Levy MG, Chomel BB, Breitschwerdt EB. Vector transmission of Bartonella species with emphasis on the potential for tick transmission. Med Vet Entomol. 2008; 22: 1-15.
Harms A, Dehio C. Intruders below the radar: molecular pathogenesis of Bartonella spp. Clin Microbiol Rev. 2012; 25(1): 42-78.
Cotté V, Bonnet S, Le-Rhun D, Le Naour E, Chauvin A, Boulouis HJ. Transmission of Bartonella henselae by Ixodes ricinus. Emerg Infect Dis. 2008; 14: 1074-1080.
Sanogo YO, Zeaiter Z, Caruso G, Merola F, Shpynov S, Brouqui P, Raoult D. Bartonella henselae in Ixodes ricinus ticks (Acari: Ixodida) removed from humans, Belluno province, Italy. Emerg Infect Dis. 2003; 9: 329-332.
Angelakis E, Pulcini C, Waton J, Imbert P, Socolovschi C, Edouard S, Dellamonica P, Raoult D. Scalp eschar and neck lymphadenopathy caused by Bartonella henselae after tick bite. Clin Infect Dis. 2010; 50: 549-551.
Eskow E, Rao RV, Mordechai E. Concurrent infection of the central nervous system by Borrelia burgdorferi and Bartonella henselae: evidence for a novel tick-borne disease complex. Arch Neurol. 2001; 58: 1357-1363.
Podsiadly E, Chmielewski T, Tylewska-Wierzbanowska S. Bartonella henselae and Borrelia burgdorferi infections of the central nervous system. Ann N Y Acad Sci. 2003; 990: 404-406.
Chang CC, Chomel BB, Kasten RW, Romano V, Tietze N. Molecular evidence of Bartonella spp. in questing adult Ixodes pacificus ticks in California. J Clin Microbiol. 2001; 39: 1221-1226.
Chang CC, Hayashidani H, Pusterla N, Kasten RW, Madigan JE, Chomel BB. Investigation of Bartonella infection in Ixodid ticks from California. Comp Immunol Microbiol Infect Dis. 2002; 25: 229-236.
Kim CM, Kim JY, Yi YH, Lee MJ, Cho MR, Shah DH, Klein TA, Kim HC, Song JW, Chong ST, O’Guinn ML, Lee JS, Lee IY, Park JH, Chae JS. Detection of Bartonella species from ticks, mites and small mammals in Korea. J Vet Sci. 2005; 6: 327-334.
Zając V, Wójcik-Fatla A, Szymańska J. Infection of Ixodes ricinus ticks with Bartonella spp. in the Lublin macroregion. Zdr Publ. 2009; 119(4): 403-407.
Parola P, Shpynov S, Montoya M, Lopez M, Houpikian P, Zeaiter Z, Guerra H, Raoult D. First molecular evidence of new Bartonella spp. in fleas and a tick from Peru. Am J Trop Med Hyg. 2002; 67(2): 135-136.
Halos L, Jamal T, Maillard R, Beugnet F, Le Menach A, Boulouis HJ, 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.
Skotarczak B, Adamska M. Detection of Bartonella DNA in roe deer (Capreolus capreolus) and in ticks removed from deer. Eur J Wildl Res. 2005; 51: 287-290.
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(12): 668-675.
Mietze A, Strube C, Beyerbach M, Schnieder T, Goethe R. Occurrence of Bartonella henselae and Borrelia burgdorferi sensu lato co-infections in ticks collected from humans in Germany. Clin Microbiol Infect. 2011; 17(6): 918-920.
Norman AF, Regnery R, Jameson P, Greene C, Krause DC. Differentiation of Bartonella-like isolates at the species level by PCR-restriction fragment length polymorphism in the citrate synthase gene. J Clin Microbiol. 1995; 33(7): 1797-1803.
Skotarczak B, Wodecka B, Cichocka A. Coexistence DNA of Borrelia burgdorferi sensu lato and Babesia microti in Ixodes ricinus ticks from north-western Poland. Ann Agric Environ Med. 2002; 9 (1): 25-28.
Nocton JJ, Dressler F, Rutledge BJ, Rys PN, Persing DH, Steere AC. Detection of Borrelia burgdorferi DNA by polymerase chain reaction in synovial fluid from patients with Lyme arthritis. N Engl J Med. 1994; 330(4): 229-234.
Gray JS, Dautel H, Estrada-Peña A, Kahl O, Lindgren E. Effects of climate change on ticks and tick-borne diseases in Europe. Interdiscip Perspect Infect Dis. 2009; Article ID 593232, DOI: 10.1155/2009/593232.
Jaenson TGT, Lindgren E. The range of Ixodes ricinus and the risk of contracting Lyme borreliosis will increase northwards when the vegetation period becomes longer. Ticks Tick Borne Dis. 2011; 2(1): 44-49.
Jaenson TGT, Jaenson DGE, Eisen L, Petersoon E, Lindgren E. Changes in the geographical distribution and abundance of the tick Ixodes ricinus during the past 30 years in Sweden. Parasit Vectors 2012; 5:8. DOI: 10.1186/1756-3305-5-8.
Estrada-Peña A, Ayllón N, de la Fuente J. Impact of climate trends on tick-borne pathogen transmission. Front Physiol. 2012; 3:64. DOI: 10.3389/fphys.2012.00064.
Kjelland V, Ytrehus B, Stuen S, Skarpaas T, Slettan A. Prevalence of Borrelia burgdorferi in Ixodes ricinus ticks collected from moose (Alces alces) and roe deer (Capreolus capreolus) in southern Norway. Ticks Tick Borne Dis. 2011; 2(2): 99-103.
Stańczak J, Gabre RM, Kruminis-Łozowska W, Racewicz 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.
Komoń T, Sytykiewicz H. Occurrence of Borrelia burgdorferi s.l. in selected Ixodes ricinus populations within Nadbuzański Landscape Park. Wiad Parazytol. 2007; 53(4): 309-317.
Gern L. Life cycle of Borrelia burgdorferi sensu lato and transmission to humans. Curr Probl Dermatol. 2009; 37: 18-30.
Podsiadły E, Chmielewski T, Karbowiak G, Kędra E, Tylewska-Wierzbanowska S. The occurrence of spotted fever rickettsioses and other tick-borne infections in forest workers in Poland. Vector Borne Zoonotic Dis. 2011; 11(7): 985-989.
Welc-Falęciak R, Hildebrandt A, Siński E. Co-infection with Borrelia species and other tick-borne pathogens in humans: two cases from Poland. Ann Agric Environ Med. 2010; 17(2): 309-313.
Lotric-Furlan S, Ruzic-Sabljic E, Strle F. Concomitant human granulocytic anaplasmosis and Lyme neuroborreliosis. Clin Microbiol Infect. 2009; 15 (Suppl 2): 28-29.
Ruiz-Fons F, Fernández-de-Mera IG, Acevedo P, Gortázar C, de la Fuente J. Factors driving the abundance of Ixodes ricinus and the prevalence of zoonotic I. ricinus-borne pathogens in natural foci. Appl Environ Microbiol. 2012; 78(8): 2669-2676.
Grzeszczuk A, Puzanowska B, Zirako S. Anaplasma phagocytophilum infection in patients with early Lyme borreliosis, erythema migrans, in north-eastern Poland. Clin Microbiol Infect. 2009; 15 (Suppl 2): 17-18.
Swanson SJ, Neitzel D, Reed KD, Belongia EA. Coinfections acquired from Ixodes ticks. Clin Microbiol Rev. 2006; 19: 708-727.
Sytykiewicz H, Karbowiak G, Hapunik J, Szpechciński A, Supergan-Marwicz M, Goławska S, Sprawka I, Czerniewicz P. Molecular evidence of Anaplasma phagocytophilum and Babesia microti co-infections in Ixodes ricinus ticks in central-eastern region of Poland. Ann Agric Environ Med. 2012; 19(1): 45-49.
Wójcik-Fatla A, Szymańska J, Wdowiak L, Buczek A, DutkiewiczJ. 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.
Hildebrandt A, Schmidt KH, Wilske B, Dorn W, Straube E, Fingerle V. Prevalence of four species of Borrelia burgdorferi sensu lato and coinfection with Anaplasma phagocytophila in Ixodes ricinus ticks in central Germany. Eur J Clin Microbiol Infect Dis. 2003; 22(6): 364-367.
Halos L, Bord S, Cotté V, Gasqui P, Abrial D, Barnouin J, Boulouis HJ, 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(13): 4413-4420.
Holden K, Boothby JT, Kasten RW, Chomel BB. Co-detection of Bartonella henselae, Borrelia burgdorferi, and Anaplasma phagocytophilum in Ixodes pacificus ticks from California, USA. Vector Borne Zoonotic Dis. 2006; 6: 99-102.
Ginsberg HS. Potential effects of mixed infections in ticks on transmission dynamics of pathogens: comparative analysis of published records. Exp Appl Acarol. 2008; 46: 29-41.
Milutinović M, Masuzawa T, Tomanović S, Radulović Z, Fukui T, Okamoto Y. Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum, Francisella tularensis and their co-infections in host-seeking Ixodes ricinus ticks collected in Serbia. Exp Appl Acarol. 2008; 45(3-4): 171-183.
Podsiadły E, Chmielewski T, Marczak R, Sochon E, Tylewska-Wierzbanowska S. Bartonella henselae in the human environment in Poland. Scand J Infect Dis. 2007; 39: 956-962.
Tijsse-Klasen E, Fonville M, Gassner F, Nijhof AM, Hovius EKE, Jongejan F, Takken W, Reimerink JR, Overgaauw PAM, Sprong H. Absence of zoonotic Bartonella species in questing ticks: First detection of Bartonella clarridgeiae and Rickettsia felis in cat fleas in the Netherlands. Parasit Vectors 2011; 4:61. DOI: 10.1186/1756-3305-4-61.
Telford III SR, Wormser GP. Bartonella spp. transmission by ticks not established. Emerg Infect Dis. 2010; 16(3): 379-384.
Mosbacher ME, Klotz S, Klotz J, Pinnas JL. Bartonella henselae and the potential for arthropod vector-borne transmission. Vector Borne Zoonotic Dis. 2011; 11(5): 471-477.
Journals System - logo
Scroll to top