Abundance of questing ticks and molecular evidence for pathogens in ticks in three parks of Emilia-Romagna region of Northern Italy
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Veterinary practitioner, Modena, Italy
Department of Veterinary Medical Sciences, Alma mater Studiorum - University of Bologna, Italy
University of California Davis, School of Veterinary Medicine, Dept. of Medicine and Epidemiology
Veterinary Practitioner, Forlì- Cesena, Italy
Corresponding author
Roberta Galuppi   

Department of Veterinary Medical Sciences, Alma mater Studiorum - University of Bologna, Italy
Ann Agric Environ Med. 2015;22(3):459-466
Introduction and objective:
Infectious and parasitic diseases transmitted by ticks, such as Lyme diseases, granulocytic anaplasmosis and piroplasmosis, have been frequently reported in Europe, with increasing attention to them as an emerging zoonotic problem. The presented study was performed to assess the distribution and the density of questing ticks in three regional parks of Emilia-Romagna region of Northern Italy, and to seek molecular evidence of potential human pathogens in tick populations.

Material and Methods:
In the period April-October 2010, 8,139 questing ticks were collected: 6,734 larvae, 1,344 nymphs and only a few adults – 28 females and 33 males. The abundance of Ixodes ricinus questing ticks was compared among different sampling sites and related to microclimate parameters. 1,544 out of 8,139 ticks were examined for the presence of pathogens: PCR was used to detect piroplasms DNA and Real time Taqman PCR for Anaplasma phagocytophilum and Borrelia burgdorferi s.l.

The predominant species was I. ricinus (overall abundance 1,075.9/100 m2); more rarely, Dermacentor marginatus (n = 37 – 0.45%), Scaphixodes frontalis (n = 13 – 0.16%), Hyalomma spp. (n = 6 – 0.07%) and Ixodes acuminatus (n = 3 – 0.04%) were also found. 28 out of 324 (8.6%) samples of ticks were PCR-positive for piroplasm DNA. 11 amplicons of 18S rRNA gene were identical to each other and had 100% identity with Babesia EU1 (Babesia venatorum) using BLAST analysis. Real time Taqman PCR gave positive results for A. phagocytophilum in 23 out of 292 samples (7.9%), and for B. burgdorferi s.l. in 78 out of 292 samples (26.7%). I. ricinus was the only species found positive for pathogens by molecular analysis; 16 tick samples were co-infected with at least 2 pathogens.

The peak of nymph presence was in May, and the higher prevalence of pathogens occurred in April-June, most often in nymphs; therefore, spring season could represent the higher risk period for the transmission of pathogens. These data could provide guidelines for the preventions of tick-trasmitted diseases in this region.

Gray JS, Dautel H, Estrada-Peña A, Kahl A, Lindgren. Effects of climate change on ticks and tick-borne diseases in Europe. Interdiscip Perspect Infect Dis. 2009, Article ID 593232, 12 pages, doi:10.1155/2009/593232.
Kjemtrup AM, Conrad PA. Human babesiosis: an emerging tick-borne disease. Intern J Parasit. 2000; 30(12–13): 1323–1337.
Kubiak K, Dziekonska-Rynko J. Seasonal activity of the common European tick, Ixodes ricinus (Linnaeus, 1758), in the forested areas of the city of Olsztyn and its surroundings. Wiad Parazytol. 2006; 52 (1): 59–64.
Kramer VL, Beesley C. Temporal and spatial distribution of Ixodes pacificus and Dermacentor occidentalis (Acari: Ixodidae) and prevalence of Borrelia burgdorferi in Contra Costa county, California. J Med Entomol. 1993; 30 (3): 549–554.
Li X, Dunley JE. Optimal sampling and spatial distribution of Ixodes pacificus , Dermacentor occidentalis and Dermacentor variabilis ticks (Acari: Ixodidae). Exp Appl Acarol. 1998; 22 (4): 233–248.
Manilla G. Fauna d’Italia. Acari Ixodida. Edizioni Calderini, Bologna, Italy, 1998.
Iori A, Di Giulio A, De Felici S. Zecche d’Italia. In: Cringoli G, Iori A, Rinaldi L, Veneziano V, Genchi C (eds.). Mappe parassitologiche: Zecche. Rolando Editore, Napoli 2005.p.52–163.
Schwarz A, Maier WA, Kistemann T, Kampen H. Analysis of the distribution of the tick Ixodes ricinus L. (Acari: Ixodidae) in a nature reserve of western Germany using Geographic Information systems. Int J Hyg Environ Health. 2009; 212(1): 87–96.
Iori A, Gabrielli S, Calderini P, Moretti A, Pietrobelli M, Tampieri M P, Galuppi R, Cancrini G. Tick reservoirs for piroplasms in central and northern Italy. Vet Parasitol. 2010; 170(3–4): 291–296.
Galuppi R, Aureli S, Bonoli C, Caffara M, Tampieri MP. Detection and molecular characterization of Theileria sp. in fallow deer (Dama dama) and ticks from an Italian natural preserve. Res Vet Sci. 2011; 91(1): 110–115.
Drazenovich N, Foley J, Brown RN. Use of Real-Time quantitative PCR targeting the msp2 protein gene to identify cryptic Anaplasma phagocytophilum infections in wildlife and domestic animals. Vector-borne Zoon Dis. 2006, 1(1): 83–90.
Barbour AG, Bunikis J, Travinsky B, Hoen A G, Diuk-Wasser MA, Fish D, Tsao JI. Niche partitioning of Borrelia burgdorferi and Borrelia miyamotoi in the same tick vector and mammalian reservoir species. Am J Trop Med Hyg. 2009; 81(6): 1120–1131.
Barandika JF, Hurtado A, Juste RA, Garcìa-Pérez AL. Seasonal Dynamics of Ixodes ricinus in a 3-Year Period in Northern Spain: First Survey on the Presence of Tick-Borne Encephalitis Virus. Vector-Borne Zoon Dis. 2010; 10(10): 1027–1035.
Maioli G, Pistone D, Bonilauri P, Pajoro M, Barbieri I, Patrizia M, Vicari N, Dottori M. Ethiological agents of rickettsiosis and anaplasmosis in ticks collected in Emilia-Romagna region (Italy) during 2008 and 2009. Exp Appl Acarol. 2012; 57(2): 199–208.
Dantas-Torres F, Otranto D. Seasonal dynamics of Ixodes ricinus on ground level and higher vegetation in a preserved wooded area in southern Europe. Vet Parasitol. 2013; 192(1–3) 253– 258.
Wilson ML. Population ecology of tick vectors: interaction, measurement and analysis. In: Sonenshine DE, Mather TN (eds.). Ecological dynamics of tick-borne zoonoses. Oxford University Press, UK, 1994. p.20–44.
Randolph SE, Green RM, Hoodless AN, Peacey MF. An empirical quantitative framework for the seasonal population dynamics of the tick Ixodes ricinus. Int J Parassitol. 2002; 32: 979–989.
Balashov YS. Bloodsucking ticks (Ixodidea) Vector of diseases of man and animals. Miscellaneous Publications of the Entomological Society of America. 1972; 8: 161–376.
Anderson JF, Magnarelli LA. Biology of Ticks. Infect Dis Clin North Am. 2008; 22: 195–215.
Jensen PM. Host seeking activity of the Ixodes ricinus ticks based on daily consecutive flagging samples. Exp Appl Acarol. 2000; 24: 695–708.
Hartelt K, Oehme R, Frank H, Brockmann SO, Hassler D, Kimming P. Pathogens and symbionts in ticks: prevalence of Anaplasma phagocytophilum (Ehrlichia sp.), Wolbachia sp., Rickettsia sp. and Babesia sp. in southern Germany. Int J Med Microbiol. 2004; 293 (suppl 37): 86–92.
Kuźna-Grygiel W, Bukowska K, Cichocka A, Kosik-Bogacka D, Skotarczak B. The prevalence of piroplasms in a population of Ixodes ricinus (Acari: Ixodidae) from North-Western Poland. Ann Agric Environ Med. 2002; 9(2): 175–178.
Gray JS. Studies on the activity of Ixodes ricinus in relation to the epidemiology of babesiosis in Co Meath, Ireland. Br Vet J. 1980; 136(5): 427–436.
Cassini R, Bonoli C, Montarsi F, Tessarin C, Marcer F, Galuppi R. Detection of Babesia EU1 in Ixodes ricinus ticks in Northen Italy. Vet Parasitol. 2010; 171(1–2): 151–154.
Herwaldt B L, Cacciò S, Gherlinzoni F, Aspock H, Slemenda SD, Piccalunga P, Martinelli G, Edelhofer R, Hollstein U, Poletti G, Pampiglione S, Loschenberger K, Tura S, Pieniazek N. Molecular charcterization of a non-Babesia divergens organism causing zoonotic babesiosis in Europe. Emerg Infect Dis. 2003; 9(8): 942–948.
Corrain R, Drigo M, Fenati M, Menandro ML, Mondin A, Pasotto D, Martini M. Study on ticks and tick-borne zoonoses in public parks in Italy. Zoonoses Public Health. 2012; 59(7): 468–476.
Nazzi F, Martinelli E, Del Fabbro S, Bernardinelli I, Milani N, Iob A, Pischiutti P, Campello C, D’Agaro P. Ticks and Lyme borreliosis in an alpine area in northeast Italy. Med Vet Entomol. 2010; 24(3): 220–226.
Wójcik-Fatla A, Szymańska J, Wdowiak L, Buczek A, Dutkiewicz J. Coincidence of three pathogens (Borrelia burgdorferi, Anaplasma phagocytophilum and Babesia microti) in Ixodes ricinus ticks in the Lublin macroregion. Ann Agric Environ Med. 2009; 16(1): 151–158.
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