Abstract
An increasing number of studies reveal that ticks and their hosts are infected with multiple pathogens, suggesting that coinfection might be frequent for both vectors and wild reservoir hosts. Whereas the examination of associations between coinfecting pathogen agents in natural host–vector–pathogen systems is a prerequisite for a better understanding of disease maintenance and transmission, the associations between pathogens within vectors or hosts are seldom explicitly examined. We examined the prevalence of pathogen agents and the patterns of associations between them under natural conditions, using a previously unexamined host–vector–pathogen system—green lizards Lacerta viridis, hard ticks Ixodes ricinus, and Borrelia, Anaplasma, and Rickettsia pathogens. We found that immature ticks infesting a temperate lizard species in Central Europe were infected with multiple pathogens. Considering I. ricinus nymphs and larvae, the prevalence of Anaplasma, Borrelia, and Rickettsia was 13.1% and 8.7%, 12.8% and 1.3%, and 4.5% and 2.7%, respectively. The patterns of pathogen prevalence and observed coinfection rates suggest that the risk of tick infection with one pathogen is not independent of other pathogens. Our results indicate that Anaplasma can play a role in suppressing the transmission of Borrelia to tick vectors. Overall, however, positive effects of Borrelia on Anaplasma seem to prevail as judged by higher-than-expected Borrelia–Anaplasma coinfection rates.
Similar content being viewed by others
References
Alekseev AN, Burenkova LA, Vasil’eva IS, Dubinina EV, Chunikhin SP (1996) The functioning of foci of mixed tick-borne infections on Russian territory. Med Parazitol 4:9–16 (In Russian)
Amore G, Tomassone L, Grego E, Ragagli C, Bertolotti L, Nebbia P, Rosati S, Mannelli A (2007) Borrelia lusitaniae in immature Ixodes ricinus (Acari: Ixodidae) feeding on common wall lizards in Tuscany, Central Italy. J Med Entomol 44:303–307
Barbour A (2004) Specificity of Borrelia-tick vector relationships. In: Gillespie SH, Smith GL, Osbourn A (eds) Microbe–vector interactions in vector-borne diseases. Cambridge University Press, Cambridge, pp 75–90
Barnard SM, Durden LA (2000) A veterinary guide to the parasites of reptiles, vol. 2. Arthropods (excluding mites). Krieger, Malabar
Belongia EA (2002) Epidemiology and impact of coinfections acquired from Ixodes ticks. Vector-Borne Zoonot Dis 2:265–273
Brambor T, Clark WR, Golder M (2005) Understanding interaction models: improving empirical analyses. Polit Anal 13:1–20
Casher LE, Lane RS, Barrett RH, Eisen L (2002) Relative importance of lizards and mammals as hosts for ixodid ticks in northern California. Exp Appl Acarol 26:127–143
Daniel M, Černý V (1971) Klíč zvířeny ČSSR. Československá Akademie Vied, Praha
De Carvalho IL, Fonseca JE, Marques JG, Ullmann A, Hojgaard A, Zeidner N, Núncio MS (2008) Vasculitis-like syndrome associated with Borrelia lusitaniae infection. Clin Rheumatol 27:1587–1591
De Michelis S, Sewell HS, Collares-Pereira M, Santos-Reis M, Schouls LM, Benes V, Holmes EC, Kurtenbach K (2000) Genetic diversity of Borrelia burgdorferi sensu lato in ticks from mainland Portugal. J Clin Microbiol 38:2128–2133
Dib L, Bitam I, Tahri M, Bensouilah M, De Meeûs T (2008) Competitive exclusion between Piroplasmosis and Anaplasmosis agents within Cattle. PloS Pathog 4:e7
Dsouli N, Younsi-Kabachii H, Postic D, Nouira S, Gern L, Bouattour A (2006) Reservoir role of lizard Psammodromus algirus in transmission cycle of Borrelia burgdorferi sensu lato (Spirochaetaceae) in Tunisia. J Med Entomol 43:737–742
Dumler JS, Choi K-S, Garcia-Garcia JC, Barat NS, Scorpio DG, Garyu JW, Grab DJ, Bakken JS (2005) Human granulocytic Anaplasmosis and Anaplasma phagocytophilum. Emerg Infect Dis 11:1828–1834
Ginsberg HS (2008) Potential effects of mixed infections in ticks on transmission dynamics of pathogens: comparative analysis of published records. Exp Appl Acarol 46:29–41
Graves S, Stenos J (2003) Rickettsia honei: a spotted fever group rickettsia on three continents. Ann New York Acad Sci 990:62–66
Gronesova P, Ficova M, Mizakova A, Kabat P, Trnka A, Betakova T (2008) Prevalence of avian influenza viruses, Borrelia garinii, Mycobacterium avium, and Mycobacterium avium subsp. paratuberculosis in waterfowl and terrestrial birds in Slovakia, 2006. Avian Pathol 37:537–543
Hanincová K, Schäfer SM, Etti S, Sewell H-S, Taragelová V, Ziak D, Labuda M, Kurtenbach K (2003) Association of Borrelia afzelii with rodents in Europe. Parasitol 126:11–20
Hanincová K, Taragelová V, Koci J, Schäfer SM, Hails R, Ullmann AJ, Piesman J, Labuda M, Kurtenbach K (2003) Association of Borrelia garinii and B. valaisiana with songbirds in Slovakia. Appl Environ Microbiol 69:2825–2830
Holden K, Hodzic E, Feng S, Freet KJ, Lefebvre RB, Barthold SW (2005) Coinfection with Anaplasma phagocytophilum alters Borrelia burgdorferi population distribution in C3H/HeN mice. Infect Immun 73:3440–3444
Ishiguro F, Takada N, Masuzawa T, Fukui T (2000) Prevalence of Lyme disease Borrelia spp. in ticks from migratory birds on the Japanese mainland. Appl Environ Microbiol 66:982–986
Jado I, Escuerdo R, Gil H, Jiménez-Alonso MI, Sousa R, García-Pérey AL, Rodréguey-Vargas M, Lobo B, Anda P (2006) Molecular method for identification of Rickettsia species in clinical and environmental samples. J Clin Microbiol 44:4572–4576
Krause PJ (2002) Babesiosis. Med Clin N Am 86:361–373
Kuo MM, Lane RS, Giclas PC (2000) A comparative study of mammalian and reptilian alternative pathway of complement-mediated killing of the Lyme disease spirochete (Borrelia burgdorferi). J Parasitol 86:1223–1228
Kurtenbach K, Peacey M, Rijpkema SG, Hoodless AN, Nuttall PA, Randolph SE (1998) Differential transmission of the genospecies of Borrelia burgdorferi sensu lato by game birds and small rodents in England. Appl Environ Microbiol 64:1169–1174
Kurtenbach K, De Michelis S, Sewell H-S, Etti S, Schäfer M, Hails R, Collares-Pereira M, Hanincová K, Labuda M, Bormane A, Donaghy M (2001) Distinct combinations of Borrelia burgdorferi sensu lato genospecies found in individual questing ticks from Europe. Appl Environ Microbiol 67:4926–4929
Levin ML (2007) Effects of coinfection with Borrelia burgdorferi and Anaplasma phagocytophilum in vector ticks and vertebrate hosts. In: van Nitch P (ed) Research on Lyme disease. Nova, New York, pp 1–34
Levin ML, Fish D (2000) Acquisition of coinfection and simultaneous transmission of Borrelia burgdorferi and Ehrlichia phagocytophila by Ixodes scapularis ticks. Infect Immun 68:2183–2186
Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) SAS® for mixed models, 2nd edn. SAS Institute Inc, Cary
Majláthová V, Majláth I, Derdáková M, Víchová B, Peťko B (2006) Borrelia lusitaniae and green lizards (Lacerta viridis), Karst Region, Slovakia. Emerg Infect Dis 12:1895–1901
Mather TN, Piesman J, Spielman A (1987) Absence of spirochetes (Borrelia burgdorferi) and piroplasms (Babesia microti) in deer ticks (Ixodes dammini) parasitized by chalcid wasps (Hunterellus hookeri). Med Vet Entomol 1:3–8
Murray PR, Rosenthal KS, Pfaller MA (2009) Medical microbiology, 6th edn. Mosby, Philadelphia
Nieto NC, Foley JE (2009) 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 9:93–102
Nieto NC, Foley JE, Bettaso J, Lane RS (2009) Reptile infection with Anaplasma phagocytophilum, the causative agent of granulocytic anaplasmosis. J Parasitol 95:1165–1170
Nowak M, Cienuch S, Stańczak J, Siuda K (2010) Detection of Anaplasma phagocytophilum in Amblyomma flavomaculatum ticks (Acari: Ixodidae) collected from lizard Varanus exanthematicus imported to Poland. Exp Appl Acarol 51:363–371
Origgi F (2007) Reptile immunology. In: Jacobson ER (ed) Infectious diseases and pathology of reptiles. Color atlas and text. CRC, Boca Raton, pp 131–166
Pachner A, Steiner I (2007) Lyme neuroborreliosis: infection, immunity, and inflammation. Lancet Neurol 6:544–552
Parola P, Roux V, Camicas JL, Baradji I, Brouqui P, Raoult D (2000) Detection of Ehrlichiae in African ticks by PCR. Trans R Soc Trop Med Hyg 94:707–708
Penchenier L, Simo G, Grébaut P, Nkinin S, Laveissière C, Herder S (2000) Diagnosis of human trypanosomiasis, due to Trypanosoma brucei gambiense in central Africa, by the polymerase chain reaction. Trans R Soc Trop Med Hyg 94:392–394
Postic D, Assous MV, Grimont PA, Baranton G (1994) Diversity of Borrelia burgdorferi sensu lato evidenced by restriction fragment length polymorphism of rrf (5S)–rrl (23S) intergenic spacer amplicons. Int J Sys Bacteriol 44:743–752
Quinn GP, Keough MJ (2007) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
Reeves WK, Durden LA, Dasch GA (2006) A spotted fever group Rickettsia from an exotic tick species, Amblyoma exornatum (Acari: Ixodidae), in a reptile breeding facility in the United States. J Med Entomol 43:1099–1101
Richter D, Matuschka FR (2006) Perpetuation of the Lyme disease spirochete Borrelia lusitaniae by lizards. Appl Environ Microbiol 72:4627–4632
Rooney AA (2005) Reptiles: the research potential of an overlooked taxon in immunotoxicology. In: Tryphonas H, Fournier M, Blakley BR, Smits J, Brousseau P (eds) Investigative immunotoxicology. CRC Press, Boca Raton, pp 107–128
Roux V, Rydkina E, Eremeeva M, Raoult D (1997) Citrate synthase gene comparison, a new tool for phylogenetic analysis, and its application for the Rickettsiae. Int J Sys Bacteriol 47:252–261
Swanson SJ, Neitzel D, Reed KD, Belongia EA (2006) Coinfections acquired from Ixodes ticks. Clin Microbiol Rev 19:708–727
Tarageľová V, Koči J, Hanincová K, Kurtenbach K, Derdáková M, Ogden NH, Literák I, Kocianová E, Labuda M (2008) Blacbirds and song thrushes constitute a key reservoir of Borrelia garinii, the causative agent of borreliosis in Central Europe. Appl Environ Microbiol 74:1289–1293
Thompson C, Spielman A, Krause PJ (2001) Coinfecting deer-associated zoonoses: Lyme disease, babesiosis, and ehrlichiosis. Clin Infect Dis 33:676–685
Tijsse-Klasen E, Fonville M, Reimerink JHJ, Spitzen A, Sprong H (2010) Role of sand lizards in the ecology of Lyme and other tick-borne diseases in the Netherlands. Parasit Vectors 3:42
Václav R, Prokop P, Fekiač V (2007) Expression of breeding coloration in European Green Lizards (Lacerta viridis): variation with morphology and tick infestation. Can J Zool 85:1199–1206
Wielinga PR, Gaasenbeek C, Fonville M, de Boer A, de Vries A, Dimmers W, Akkerhuis OP, Jagers G, Schouls LM, Borgsteede F, van der Giessen JW (2006) Longitudinal analysis of tick densities and Borrelia, Anaplasma, and Ehrlichia infections of Ixodes ricinus ticks in different habitat areas in The Netherlands. Appl Environ Microbiol 72:7594–601
Whitworth T, Popov V, Han V, Bouyer D, Stenos J, Graves S, Ndip L, Walker D (2003) Ultrastructural and genetic evidence of a reptilian tick, Aponomma hydrosauri, as a host of Rickettsia honei in Australia—possible transovarial transmission. Ann N Y Acad Sci 990:67–74
Zeidner NS, Dolan MC, Massung R, Piesman J, Fish D (2000) Coinfection with Borrelia burgdorferi and the agent of human granulocytic ehrlichiosis suppresses IL-2 and IFN γ production and promotes an IL-4 response in C3H/HeJ mice. Parasite Immunol 22:581–588
Acknowledgments
We thank Dr. Ján Krištofík for tick determination. Milan Olekšák and the directive of the Slovak Karst National Park provided logistic support. This study was funded by the VEGA grants no. 2/7080/27 and 1/0207/08. The study was conducted under approval from the Ministry of Environment of the Slovak Republic (license no. 1430/467/04-5.1).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Václav, R., Ficová, M., Prokop, P. et al. Associations Between Coinfection Prevalence of Borrelia lusitaniae, Anaplasma sp., and Rickettsia sp. in Hard Ticks Feeding on Reptile Hosts. Microb Ecol 61, 245–253 (2011). https://doi.org/10.1007/s00248-010-9736-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-010-9736-0