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Ticks Infesting Humans in Italy and Associated Pathogens

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Ticks Infesting Humans in Italy and Associated Pathogens Otranto et al. Parasites & Vectors 2014, 7:328 http://www.parasitesandvectors.com/content/7/1/328 RESEARCH Open Access Ticks infesting humans in Italy and associated pathogens Domenico Otranto1*, Filipe Dantas-Torres1,2, Alessio Giannelli1, Maria Stefania Latrofa1, Antonio Cascio3, Stefania Cazzin4, Silvia Ravagnan4, Fabrizio Montarsi4, Sergio Aurelio Zanzani5, Maria Teresa Manfredi5 and Gioia Capelli4 Abstract Background: Ticks may transmit a large variety of pathogens, which cause illnesses in animals and humans, commonly referred to as to tick-borne diseases (TBDs). The incidence of human TBDs in Italy is underestimated because of poor surveillance and the scant amount of studies available. Methods: Samples (n = 561) were collected from humans in four main geographical areas of Italy (i.e., northwestern, northeastern, southern Italy, and Sicily), which represent a variety of environments. After being morphologically identified, ticks were molecularly tested with selected protocols for the presence of pathogens of the genera Rickettsia, Babesia, Theileria, Candidatus Neoehrlichia mikurensis, Borrelia and Anaplasma. Results: Ticks belonged to 16 species of the genera Argas, Dermacentor, Haemaphysalis, Hyalomma, Ixodes and Rhipicephalus,withIxodes ricinus (59.5%) being the species most frequently retrieved, followed by Rhipicephalus sanguineus sensu lato (21.4%). Nymphs were the life stage most frequently retrieved (41%), followed by adult females (34.6%). The overall positivity to any pathogen detected was 18%. Detected microorganisms were Rickettsia spp. (17.0%), Anaplasma phagocytophilum (0.8%), Borrelia afzelii (0.5%), Borrelia valaisiana (0.3%), C. N. mikurensis (0.5%) and Babesia venatorum (0.6%). Conclusions: Results indicate that people living in the Italian peninsula are at risk of being bitten by different tick species, which may transmit a plethora of TBD causing pathogens and that co-infections may also occur. Keywords: Ticks, Pathogens, Humans, Tick-borne diseases, Italy, Distribution Background animals, with a high risk of acquiring infections for Ticks are amongst the most important arthropod parasites humans frequenting tick-infested areas, such as forests, of animals and display a worldwide distribution, being meadow habitats and grasslands [1,3,4]. adapted to different environments and climates and host In spite of the availability of several chemical options species [1]. Hard ticks (order Ixodida, family Ixodidae) for tick control, especially for companion animals and represent the most diverse group, occurring in tropical, livestock, the incidence of human TBDs is increasing temperate and even arctic regions [2]. Their medical and worldwide [1,5]. For example, cases of Lyme borreliosis veterinary importance is mostly due to their great capacity by Borrelia burgdorferi sensu lato are on the rise in the of transmitting viral, bacterial, protozoan and helminthic United States, and are related to the occurrence of its infections to animals, which may cause a diverse range of competent vector Ixodes scapularis. In Europe there is affections, commonly referred to as tick-borne diseases an estimated average of 85,000 cases per year [6]. The (TBDs). Importantly, zoonotic TBDs (e.g., anaplasmosis, development of molecular tools (e.g., reverse-line blotting babesiosis, borreliosis, rickettsioses and tick-borne en- hybridization, pyrosequencing and next generation cephalitis) may be associated with both domestic and wild sequencing), has refined the current understanding of the distribution of TBDs and the role of certain tick species as vectors of these pathogens [1]. Importantly, the immediate * Correspondence: [email protected] 1Department of Veterinary Medicine, University of Bari, 70010 Valenzano, Bari, removal of an attached tick, referral to a qualified Italy physician and tick identification in specialized laboratories, Full list of author information is available at the end of the article © 2014 Otranto et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Otranto et al. Parasites & Vectors 2014, 7:328 Page 2 of 9 http://www.parasitesandvectors.com/content/7/1/328 is pivotal to prompt the diagnosis and the treatment of any Therefore, the present study aimed to identify the TBDs. In addition, the set-up of surveillance programs is species of ticks removed from humans living in required for understanding the risks of transmission of northern, southern and insular Italy, and to molecularly specific infections in certain areas [1]. detect associated pathogens. With about 40 species [7], the tick fauna in Italy is one of the most diverse across Europe, with more species than Methods countries such as Portugal [8] and the United Kingdom Tick collection and identification [9,10]. For example, a recent study confirmed a high Ticks were collected from humans at different time points, species richness and abundance of free-living ticks in from 1995 to 2011, in northwestern (Savona, Liguria region; southern Italy, with up to nine species (i.e., Dermacentor site 1), northeastern (Trentino-Alto Adige, Veneto and marginatus, Haemaphysalis concinna, Haemaphysalis Friuli Venezia Giulia regions; site 2), southern Italy (Apulia inermis, Haemaphysalis parva, Haemaphysalis sulcata, and Basilicata regions; site 3) and Sicily island (site 4) Hyalomma marginatum, Ixodes ricinus, Rhipicephalus (Figure 1). These sites included four main geographical bursa and Rhipicephalus turanicus) collected in a single areas of Italy, representing a variety of natural environments. forested area [11]. Conversely, the species richness in the Most of the inland northern areas are featured by a environment is lower in central and northern Italy where continental humid climate, whereas the coastal areas I. ricinus is the most prevalent species [12-14]. of the Liguria region and most of the peninsula are The incidence of TBDs in humans in Italy is underesti- characterized by a Mediterranean temperate climate, mated because of low rates of notification of cases and with mild winters and hot summers [2,4,7]. scant studies focussing on the detection of pathogens in All specimens were placed in vials containing 70% ticks collected from humans (e.g., ref. [15]). Accordingly, ethanol and sent to the laboratories of the Department of the limited data on ticks, and their associated pathogens Veterinary Medicine of the University of Bari (i.e., ticks infecting humans in Italy may impair the understanding from site 3 and 4), University of Milano (i.e., ticks from of the risk for TBDs in this country. This aspect is particu- site 1) and to the Istituto Zooprofilattico Sperimentale larly important considering that the Italian peninsula has a delle Venezie (i.e., ticks from site 2). Species identification great vocation for tourism, mostly during the spring and was performed using taxonomic keys appropriate for each summer months, which constitute the high-risk period for developmental stage (i.e., larvae, nymphs, females, and tick infestation in some areas. males) [7,15]. Figure 1 Sampling areas and number of positive specimens collected from each site across the Italian peninsula. Otranto et al. Parasites & Vectors 2014, 7:328 Page 3 of 9 http://www.parasitesandvectors.com/content/7/1/328 Amplification of pathogen DNA Foster City, CA, USA), aligned and finally compared with All ticks were tested for the presence of pathogens of representative sequences available in GenBank. the genera Rickettsia, Babesia, Theileria as well as of Candidatus Neoehrlichia mikurensis. In addition, Ixodes Statistical analysis ticks were screened for B. burgdorferi s.l. and Anaplasma The difference in prevalence of different tick and phagocytophilum. pathogen species, according to their provenance and tick DNA was extracted from individual adults, nymphs or life stages were tested using the chi-square test and the larvae, using the All Prep DNA/RNA mini Kit (Qiagen, Fisher’s exact test, when appropriate. GraphPad statistical Inc., Valencia, CA), according to the manufacturer’s software (GraphPad Software, Inc.; www.graphpad.com/ instructions, and then frozen at -20°C. quickcalcs/contingency1/) was used. Differences were Target genes, primers and probes used, along with the considered significant at p < 0.05. methodologies employed for testing each pathogen, are listed in Table 1. Pathogen identity was confirmed by Ethics statement sequencing each amplicon, using a 16-capillary ABI Following the patients’ informed consent, ticks were PRISM 3130 × l Genetic Analyzer (Applied Biosystem, collected by physicians working at the first aid guard and Foster City, CA, USA). Sequence data were assembled and sent, for diagnostic purposes, to the reference laboratories edited with SeqScape software v 2.5 (Applied Biosystem, (see above). As this study was based on tick identification Table 1 Molecular detection of tick-borne pathogens: PCR methods, target genes, primers, nucleotide sequences, amplicon size (base pairs) Species PCR method Target Primer Nucleotide sequence (5′-3′) Amplicon Reference gene size (bp) Anaplasma phagocytophilum duplex RT-PCR
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