Online first
Current issue
Archive
Special Issues
About the Journal
Publication Ethics
Anti-Plagiarism system
Instructions for Authors
Instructions for Reviewers
Editorial Board
Editorial Office
Contact
Reviewers
All Reviewers
2023
2022
2021
2020
2019
2018
2017
2016
General Data Protection Regulation (RODO)
Prevalence of infections and co-infections with 6 pathogens in Dermacentor reticulatus ticks collected in eastern Poland
1
Department of Health Biohazards and Parasitology, Institute of Rural Health, Lublin, Poland
2
Department of Parasitology and Invasive Diseases, National Veterinary Research Institute, Pulawy, Poland
3
Chair and Department of Biology and Parasitology, Medical University, Lublin, Poland
Corresponding author
Angelina Wójcik-Fatla
Department of Health Biohazards and Parasitology, Institute of Rural Health, Lublin, Poland
Department of Health Biohazards and Parasitology, Institute of Rural Health, Lublin, Poland
Ann Agric Environ Med. 2017;24(1):26-32
KEYWORDS
Dermacentor reticulatusco-infectionsTBE virusAnaplasma phagocytophilumRickettsia raoultiiBorrelia burgdorferi sensu latoBabesia sppToxoplasma gondii
ABSTRACT
Occurrence of co-infections with various pathogens in ixodid ticks creates a risk of increased severity of tick-borne diseases in humans and animals exposed to bite of the ticks carrying multiple pathogens. Accordingly, co-infections in ticks were subject of numerous analyses, but almost exclusively with regard to Ixodes ricinus complex whereas potential tick vectors belonging to other genera were much less studied. Taking into consideration the role of Dermacentor reticulatus in the transmission of various pathogens, we carried out for the first time the comprehensive statistical analysis of co-infections occurring in this tick species. An attempt was made to determine the significance of the associations between 6 different pathogens occurring in D. reticulatus (Tick-borne encephalitis virus = TBEV, Anaplasma phagocytophilum, Rickettsia raoultii, Borrelia burgdorferi s. l., Babesia spp., Toxoplasma gondii), using 2 statistical methods: determination of Odds Ratios (ORs) and the Fisher’s exact test. 634 questing Dermacentor reticulatus ticks (370 females and 264 males) were collected in 2011– 2013 by flagging the lower vegetation in 3 localities in the area of Łęczyńsko-Włodawskie Lakeland, situated in the Lublin region of eastern Poland. The presence of individual pathogens was detected by PCR. Ticks were infected most often with Rickettsia raoultii (43.8%), less with TBEV (8.5%), and much less with Babesia spp., Toxoplasma gondii, Borrelia burgdorferi s.l., and Anaplasma phagocytophilum (2.5%, 2.1%, 1.6% and 1.1%, respectively). The locality-dependent variability proved to be significant for TBEV (χ2=11.063; P=0.004) and Toxoplasma gondii (χ2=11.298; P=0.0035), but not for other pathogens. Two hundred seventy (42.6%) of the examined ticks were infected only with a single pathogen, and 54 (8.5%) showed the presence of dual co-infections, each with 2 pathogens. The most common were dual infections with participation of Rickettsia raoultii (7.41%); next, those with participation of the TBEV (5.21%), Toxoplasma gondii (1.58%), Borrelia burgdorferi s.l. (1.26%), Anaplasma phagocytophilum (0.95%), and Babesia spp. (0.63%). On the total number of 15 possible associations, in 9 cases co-infections occurred whereas in 6 cases they were not detected. The most noteworthy were positive co-infections with the participation of TBEV, which proved to be weakly significant (0.05Toxoplasma gondii and Anaplasma phagocytophilum, with Odds Ratios over 3.3 and 4.4, respectively. The values of Odds Ratios exceeded 3.0 also at the co-infections of Rickettsia raoultii with B. burgdorferi s.l., and T. gondii with Babesia spp., but these associations did not attain a significance level. The co-infections of Rickettsia raoultii with Babesia spp. appeared not to be significant (0.05<P<0.1) with OR below 0.3. In conclusion, co-infections with various pathogens in D. reticulatus ticks seem to be relatively rare and mostly not significant.
REFERENCES (68)
1.
Swanson SJ, Neitzel D, Reed KD, Belongia EA. Coinfections acquired from Ixodes ticks. Clin Microbiol Rev. 2006; 19: 708–727.
2.
Belongia EA. Epidemiology and impact of coinfections acquired from Ixodes ticks. Vector Borne Zoonotic Dis. 2002; 2: 265–273.
3.
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.
4.
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: 93–102.
5.
Lommano E, Bertaiola L, Dupasquier C, Gern L. Infections and coinfections of questing Ixodes ricinus ticks by emerging zoonotic pathogens in Western Switzerland. Appl Environ Microbiol. 2012; 78: 4606–4612.
6.
Chitimia-Dobler L. Spatial distribution of Dermacentor reticulatus in Romania. Vet Parasitol. 2015; 214: 219–223.
7.
Karbowiak G. The occurrence of the Dermacentor reticulatus tick – its expansion to new areas and possible causes. Ann Parasitol. 2014; 60: 37–47.
8.
Rubel F, Brugger K, Pfeffer M, Chitimia-Dobler L, Didyk YM, Leverenz S, Dautel H, Kahl O. Geographical distribution of Dermacentor marginatus and Dermacentor reticulatus in Europe. Ticks Tick Borne Dis. 2016; 7: 224–233.
9.
Estrada-Peňa A, Jongejan F.Ticks feeding on humans: a review of records on human-biting Ixodoidea with special reference to pathogen transmission. Exp. Appl. Acarol. 1999; 23: 685–715.
10.
Bartosik K, Wiśniowski L, Buczek A. Abundance and seasonal activity of adult Dermacentor reticulatus (Acari: Amblyommidae) in eastern Poland in relation to meteorological conditions and the photoperiod. Ann Agric Environ Med. 2011; 18: 340–344.
11.
Buczek A, Bartosik K. Ticks (Ixodida: Ixodidae, Amblyommidae) in south-eastern Poland and their medical and epidemiological importance. Zdr Publ. 2011; 121: 392–397.
12.
Bartosik K, Wiśniowski L, Buczek A. Questing behavior of Dermacentor reticulatus adults (Acari: Amblyommidae) during diurnal activity periods in eastern Poland. J Med Entomol. 2012; 49: 859–864.
13.
Buczek A, Bartosik K, Wiśniowski L, Tomasiewicz K. Changes in population abundance of adult Dermacentor reticulatus (Acari: Amblyommidae) in long-term investigations in eastern Poland. Ann Agric Environ Med. 2013; 20: 269–272.
14.
Buczek A, Bartosik K, Zając Z. Changes in the activity of adult stages of Dermacentor reticulatus (Ixodida: Amblyommidae) induced by weather factors in eastern Poland. Parasit Vectors. 2014; 7: 245.
15.
Mierzejewska EJ, Alsarraf M, Behnke JM, Bajer A. The effect of changes in agricultural practices on the density of Dermacentor reticulatus ticks. Vet Parasitol. 2015; 211: 259–265.
16.
Mierzejewska EJ, Estrada-Peña A, Alsarraf M, Kowalec M, Bajer A. Mapping of Dermacentor reticulatus expansion in Poland in 2012–2014. Ticks Tick Borne Dis. 2016; 7: 94–106.
17.
Zając Z, Bartosik K, Buczek A. Factors influencing the distribution and activity of Dermacentor reticulatus (F.) ticks in an anthropopressure-unaffected area in central-eastern Poland. Ann Agric Environ Med. 2016; 23: 270–275. doi: 10.5604/12321966.1203889.
18.
Földvári G, Široký P, Szekeres S, Majoros G, Sprong H. Dermacentor reticulatus: a vector on the rise. Parasit Vectors. 2016; 9: 314.
19.
Kahl O, Janetzki C, Gray JS, Stein J, Bauch RJ. Tick infection rates with Borrelia: Ixodes ricinus versus Haemaphysalis concinna and Dermacentor reticulatus in two locations in eastern Germany. Med Vet Entomol. 1992; 6: 363–366.
20.
Rar VA, Fomenko NV, Dobrotvorsky AK, Livanova NN, Rudakova SA, Fedorov EG, Astanin VB, Morozova OV. Tickborne pathogen detection, Western Siberia, Russia. Emerg Infect Dis. 2005; 11: 1708–1715.
21.
Dautel H, Dippel C, Oehme R, Hartelt K, Schetter E. Evidence for increased geographical distribution of Dermacentor reticulatus in Germany and detection of Rickettsia sp. RpA4. Int J Microbiol. 2006; 296 (Suppl. 40): 149–156.
22.
Stańczak J. Detection of spotted fever group (SFG) rickettsiae in Dermacentor reticulatus (Acari: Ixodidae) in Poland. Int J Med Microbiol. 2006; 296: 144–148.
23.
Biaduń W, Rzymowska J, Stępień-Rukasz H, Niemczyk M, Chybowski J. Occurrence of Borrelia burgdorferi sensu lato in Ixodes ricinus and Dermacentor reticulatus ticks collected from roe deer and deer shot in the south-east of Poland. Bull Vet Inst Pulawy. 2007; 51: 213–217.
24.
Wójcik-Fatla A, Cisak E, Zając V, Zwoliński J, Dutkiewicz J. Prevalence of tick-borne encephalitis virus in Ixodes ricinus and Dermacentor reticulatus ticks collected from the Lublin region (eastern Poland). Ticks Tick Borne Dis. 2011; 2: 16–19.
25.
Wójcik-Fatla A, Bartosik K, Buczek A, Dutkiewicz J. Babesia microti in adult Dermacentor reticulatus ticks from eastern Poland. Vector Borne Zoonotic Dis. 2012; 12: 841–843.
26.
Földvári G, Rigó K, Lakos A. Transmission of Rickettsia slovaca and Rickettsia raoultii by male Dermacentor marginatus and Dermacentor reticulatus ticks to humans. Diagn Microbiol Infect Dis. 2013; 76: 387–389.
27.
Reye AL, Stegniy V, Mishaeva NP, Velhin S, Hübschen JM. Ignatyev G, Muller CP. Prevalence of tick-borne pathogens in Ixodes ricinus and Dermacentor reticulatus ticks from different geographical locations in Belarus. PLOS ONE 2013; 8, e54476.
28.
Tomanović S, Chochlakis D, Radulović Ž, Milutinović M, Ćakić S, Mihaljica D, Tselentis Y, Psaroulaki A. Analysis of pathogen co-occurrence in host-seeking adult hard ticks from Serbia. Exp Appl Acarol. 2013; 59: 367–376.
29.
Wójcik-Fatla A, Cisak E, Zając V, Sroka J, Sawczyn A, Dutkiewicz J. Study on tick-borne rickettsiae in eastern Poland. I. Prevalence in Dermacentor reticulatus (Acari: Amblyommidae). Ann Agr Env Med. 2013; 20: 276–279.
30.
Mierzejewska EJ, Pawełczyk A, Radkowski M, Welc-Falęciak R, Bajer A. Pathogens vectored by the tick, Dermacentor reticulatus, in endemic regions and zones of expansion in Poland. Parasit Vectors. 2015; 8: 490.
31.
Wójcik-Fatla A, Zając V, Sawczyn A, Cisak E, Dutkiewicz J. Babesia spp. in questing ticks from eastern Poland: prevalence and species diversity. Parasitol. Res. 2015; 114: 3111–3116.
32.
Wójcik-Fatla A, Zając V, Sawczyn A, Cisak E, Sroka J, Dutkiewicz J. Occurrence of Francisella spp. in Dermacentor reticulatus and Ixodes ricinus ticks collected in eastern Poland. Ticks Tick Borne Dis. 2015; 6: 253–257.
33.
Heile C, Heydorn AO, Schein E. Dermacentor reticulatus (Fabricius, 1794) – distribution, biology and vector for Babesia canis in Germany. Berl Munch Tierarztl Wochenschr. 2006; 119: 330–334 (in German).
34.
Beelitz P, Schumacher S, Marholdt F, Pfister K, Silaghi C. The prevalence of Babesia canis canis in marsh ticks (Dermacentor reticulatus) in the Saarland. Berl. Munch. Tierarztl. Wochenschr. 2012; 125: 168–171 (in German).
35.
Biernat B, Karbowiak G, Werszko J, Stańczak J. Prevalence of tick-borne encephalitis virus (TBEV) RNA in Dermacentor reticulatus ticks from natural and urban environment, Poland. Exp Appl Acarol. 2014; 64: 543–551.
36.
Wójcik-Fatla A, Zając V, Sawczyn A, Sroka J, Cisak E, Dutkiewicz J. Infections and mixed infections with the selected species of Borrelia burgdorferi sensu lato complex in Ixodes ricinus ticks collected in eastern Poland: a significant increase in the course of 5 years. Exp Appl Acarol. 2016; 68: 197–2012.
37.
Dubey JP. Toxoplasmosis of Animals and Humans. 2 nd Ed. CRC Press, Boca Raton, FL 2010.
38.
Wójcik-Fatla A, Sroka J, Zając V, Sawczyn A, Cisak E, Dutkiewicz J. Toxoplasma gondii (Nicolle et Manceaux, 1908) detected in Dermacentor reticulatus (Fabricius) (Ixodidae). Folia Parasit. 2015; 62: 2015.055.
39.
Sroka J, Chmielewska-Badora., Dutkiewicz J. Ixodes ricinus as a potential vector of Toxoplasma gondii. Ann Agric Environ Med. 2003; 10: 121–123.
40.
Sroka J, Wójcik-Fatla A, Zwoliński J, Zając V, Sawczuk M, Dutkiewicz J. Preliminary study on the occurrence of Toxoplasma gondii in Ixodes ricinus ticks from north-western Poland with the use of PCR. Ann Agric Environ Med. 2008; 15: 333–338.
41.
Asman M, Solarz K, Cuber P, Gąsior T, Szilman P, Szilman E, Tondaś E, Matzullok A, Kusion N, Florek K. Detection of protozoans Babesia microti and Toxoplasma gondii and their co-existence in ticks (Acari: Ixodida) collected in Tarnogórski district (Upper Silesia, Poland). Ann Agric Environ Med. 2015; 22: 80–83.
42.
Zhou Y, Zhang H, Cao J, Gong H, Zhou J. Epidemiology of toxoplasmosis: role of the tick Haemaphysalis longicornis. Infect Dis Poverty. 2016; 5: 14.
43.
Rijpkema S, Golubic D, Moelkenboer M, Verbeek-De Kruif N, Schellekens J. Identification of four genomic groups of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks collected in a Lyme borreliosis endemic region of northern Croatia. Exp Appl Acarol. 1996; 20: 23–30.
44.
Massung RF, Slater K, Owens JH, Nicholson WL, Mather TN, Solberg VB, Olson JG. Nested PCR assay for detection of granulocytic ehrlichiae. J Clin Microbiol. 1998; 36: 1090–1095.
45.
Regnery RL, Spruill CL, Plikyatis BD. Genotypic identification of rickettsiae and estimation of interspecies sequence divergence for portions of two rickettsial genes. J Bacteriol. 1991; 173: 1576–1589.
46.
Stańczak J, Kubica-Biernat B, Acewicz M, Kruminis-Łozowska W, Kur J. Detection of three genospecies of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks collected in different regions of Poland. Int J Med Microbiol. 2000; 290: 559–566.
47.
Wodecka B, Sawczuk M. Occurrence of pathogenic genospecies of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks collected from north-western Poland. Wiad. Parazytol. 2004; 50: 545–553.
48.
Persing DH, Mathiesen D, Marshall WF, Telford SR, Apielman A, Thomford JW, Conrad PA. Detection of Babesia microti by polymerase chain reaction. J Clin Microbiol. 1992; 30: 2097–2103.
49.
Hilpertshauser H, Deplazes P, Schnyder M, Gern L, Mathis A. Babesia spp. identified by PCR in ticks collected from domestic and wild ruminants in southern Switzerland. Appl Environ Microbiol. 2006; 72: 6503–6507.
50.
Grigg ME, Boothroyd JC. Rapid identification of virulent type I strains of the protozoan pathogen Toxoplasma gondii by PCR restriction fragment length polymorphism analysis at the B1 gene. J. Clin. Microbiol. 2001; 39: 398–400.
51.
Schrader C, Süss J. A nested RT-PCR for the detection of tick-borne encephalitis virus (TBEV) in ticks in natural foci. Zbl. Bakteriol. 1999; 289: 319–328.
54.
Ionita M, Silaghi C, Mitrea IL, Edouard S, Parola P, Pfister K. Molecular detection of Rickettsia conorii and other zoonotic spotted fever group rickettsiae in ticks, Romania. Ticks Tick Borne Dis. 2016; 7: 150–153.
55.
Steiner FE, Pinger RR, Vann CN, Grindle N, Civitello D, Clay K, Fuqua C. Infection and co-infection rates of Anaplasma phagocytophilum variants, Babesia spp., Borrelia burgdorferi, and the rickettsial endosymbiont in Ixodes scapularis (Acari: Ixodidae) from sites in Indiana, Maine, Pennsylvania, and Wisconsin. J Med Entomol. 2008; 45: 289–297.
56.
Tokarz R, Jain K, Bennett A, Briese T, Lipkin WA. Assessment of polymicrobial infections in ticks in New York state. Vector Borne Zoonotic Dis. 2010; 10: 217–221.
57.
Reis C, Cote M, Paul RE, Bonnet S. Questing ticks in suburban forest are infected by at least six tick-borne pathogens. Vector Borne Zoonotic Dis.2011; 11: 907–916.
58.
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.
59.
Dzięgiel B, Kubrak T, Adaszek Ł, Dębiak P, Wyłupek D, Bogucka-Kocka A, Lechowsk, J, Winiarczyk S. Prevalence of Babesia canis, Borrelia burgdorferi sensu lato, and Anaplasma phagocytophilum in hard ticks collected from meadows of Lubelskie Voivodship (eastern Poland). Bull Vet Inst Pulawy. 2014; 58: 29–33.
60.
Alekseev AN, Semenov AV, Dubinina HV. Evidence of Babesia microti infection in multi-infected Ixodes persulcatus ticks in Russia. Exp Appl Acarol. 2003; 29: 345–353.
61.
Siński E. Effect of coinfections in Ixodidae ticks on transmission of blood microparasites. Wiad Parazytol. 2009; 55: 341–347 (in Polish).
62.
Wójcik-Fatla A, Szymańska 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.
63.
Prusinski MA, Kokas JE, Hukey KT, Kogut SJ, Lee J, Backenson PB. Prevalence of Borrelia burgdorferi (Spirochaetales: Spirochaetaceae), Anaplasma phagocytophilum (Rickettsiales: Anaplasmataceae), and Babesia microti (Piroplasmida: Babesiidae) in Ixodes scapularis (Acari: Ixodidae) collected from recreational lands in the Hudson Valley Region, New York. State J Med Entomol. 2014; 51: 226–236.
64.
Danielová V, Holubová J, Pejcoch M., Daniel M. Potential significance of transovarial transmission in the circulation of tick-borne encephalitis virus. Folia Parasitol. (Praha) 2002; 49: 323–325.
65.
Pal U, Li X, Wang T, Montgomery RR, Ramamoorthi N, Desilva AM, Bao F, Yang X, Pypaert M, Pradhan D, Kantor FS, Telford S, Anderson JF, Fikrig E. TROSPA, an Ixodes scapularis receptor for Borrelia burgdorferi. Cell. 2004; 119: 457–468.
66.
Antunes S., Galindo R., Almazan C, Rudenko N, Golovchenko M, Grubhoffer L, Shkap V, do Rosário V, de la Fuente J, Domingos A. Functional genomics studies of Rhipicephalus (Boophilus) annulatus ticks in response to infection with the cattle protozoan parasite, Babesia bigemina. Int J Parasitol. 2012; 42: 187–195.
67.
Moniuszko A, Rückert C, Alberdi MP, Barry G, Stevenson B, Fazakerley JK, Kohl A, Bell-Sakyi L. Coinfection of tick cell lines has variable effects on replication of intracellular bacterial and viral pathogens. Ticks Tick Borne Dis. 2014; 5: 415–422.
68.
Levin ML, Fish D. Acquisition of coinfection and simultaneous transmission of Borrelia burgdorferi and Ehrlichia phagocytophila by Ixodes scapularis ticks. Infect. Immun. 2000; 68: 2183–2186.
Share
RELATED ARTICLE
| eISSN: | 1898-2263 |
| ISSN: | 1232-1966 |
Improvement of visual identification of the journal - task financed under the agreement No. 618/P-DUN/2019 by the Minister of Science and Higher Education allocated to the activities of disseminating science.
Generation of the DOI (Digital Object Identifier) - task financed under the agreement No. 618/P-DUN/2019 by the Minister of Science and Higher
© 2006-2024 Journal hosting platform by Bentus
We process personal data collected when visiting the website. The function of obtaining information about users and their behavior is carried out by voluntarily entered information in forms and saving cookies in end devices. Data, including cookies, are used to provide services, improve the user experience and to analyze the traffic in accordance with the Privacy policy. Data are also collected and processed by Google Analytics tool (more).
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
