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A National Survey of Ixodidae Ticks on Privately Owned Dogs in Italy

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A National Survey of Ixodidae Ticks on Privately Owned Dogs in Italy Maurelli et al. Parasites & Vectors (2018) 11:420 https://doi.org/10.1186/s13071-018-2994-2 RESEARCH Open Access A national survey of Ixodidae ticks on privately owned dogs in Italy Maria Paola Maurelli1, Paola Pepe1, Liliana Colombo2, Rob Armstrong3* , Elena Battisti4, Maria Elena Morgoglione1, Dimitris Counturis4, Laura Rinaldi1, Giuseppe Cringoli1, Ezio Ferroglio4 and Stefania Zanet4 Abstract Background: The geographical distribution of ticks on companion animals needs to be monitored to develop and plan effective control measures, as suggested by the European Scientific Counsel on Companion Animal Parasites. The aim of this study was to conduct the first Italian national survey of tick distribution on privately owned dogs. Methods: The study was performed over 20 months (February 2016 - September 2017) and involved 153 veterinary practices in 64 different provinces covering 17/20 (85%) Italian regions. Participating practitioners were asked to examine five different dogs per month at random and complete a questionnaire for each dog. Differences in tick infestation associated with: sex, age and hair length (long and short); the dog’s habitat (indoor or outdoor/kennel); and the dog’s environment (urban or rural/sylvatic) were evaluated. The attachment site of ticks on the dog was also recorded. Acaricide efficacy was evaluated for the subset of dogs for which complete information on product used, date of sampling and date of last ectoparasiticide treatment was available. Results: Of the 3026 dogs examined, 1383 (45.7%) were carrying at least one tick. Overall, 2439 tick samples were collected and a total of 14 tick species identified. Rhipicephalus sanguineus group were the most predominant ticks (63.6%), followed by Ixodes ricinus (30.6%) and I. hexagonus (5.6%). Twenty-four dogs had mixed tick infestations. Long-haired dogs had a higher tick infestation risk as did dogs with outdoor and rural/sylvatic lifestyles. Ticks were located on the head (37.4%), the neck (28.8%), the muzzle (15.5%) and the back (15.3%). A higher prevalence of Rhipicephalus was found in the interdigital spaces (10.8%) compared to Ixodes (0.2%). Finally, ectoparasiticide treatments were found significantly protective against tick infestation, especially orally administered formulations. Conclusions: Privately owned dogs in Italy have a high prevalence (45.7%) of infestation with ixodid ticks and this risk varies by dog phenotype and lifestyle. Keywords: Ticks, Dogs, Epidemiology, Risk factors, Seasonal distribution, Italy Background infections commonly referred to as tick-borne diseases In Animal Planet’s list of the top ten most extreme blood- (TBDs) [3]. Although chemical tick control options are suckers on Earth, mosquitoes were sixth, leeches fifth, kis- available, the worldwide incidence of human TBDs is in- sing bugs fourth, bedbugs third, fleas second and ticks first creasing. In Europe, an estimated average of 85,000 people [1, 2]. The literature reports either mosquitoes or ticks as are diagnosed every year with Lyme borreliosis [3]. The in- the most important vectors of pathogens to animals and cidence of human TBDs increased in Italy over the last humans [2]. Hard ticks (Ixodidae) are ectoparasites of do- decade, with 4604 clinical cases and 33 deaths documented mestic and wild animals, as well as humans. Their medical by the Ministry of Health in the period 1998–2002, mainly and veterinary importance is increased by their great cap- in southern and insular regions [3]. acity for transmitting viral, bacterial, protozoan and hel- Tick geographical distribution and abundance are influ- minthic infections to animals, causing a diverse range of enced by biotic and abiotic factors, such as climate, altitude, urbanization and host population dynamics [4]. In recent * Correspondence: [email protected] years, environmental changes, and the movement of people 3MSD Animal Health, Madison, NJ, USA and animals have introduced novel vector species into Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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. Maurelli et al. Parasites & Vectors (2018) 11:420 Page 2 of 10 previously free areas, leading to changes in local epidemi- At the time of the visit, each dog was thoroughly visu- ology of ticks and their associated pathogens [5, 6]. Redu- ally examined for 15–20 min to detect any ticks present. cing and controlling these ectoparasites is extremely Eleven body regions were observed including: head, difficult. Currently, control measures are mainly based on muzzle, neck, armpits, back, abdomen, arts, tail, anus, use of chemicals on animals and in the environment [7]. vagina and interdigital spaces. All ticks found were re- For the multiple reasons mentioned above, it is crucial to moved and preserved in the sample vials at room develop and implement a systematic surveillance system, temperature for submission to the laboratories of Para- based on a comprehensive knowledge of tick species sitology in Turin and Naples. An individual identifica- present in a target geographical area [8, 9]. Companion ani- tion number (ID) was assigned to each animal and mals, especially dogs, may be useful sentinels for monitor- questionnaires and vials were labeled with the same ID. ing tick population distribution and also the pathogens they carry [10, 11]. Many national surveys have been conducted Data handling and tick identification in Europe, based on this assumption, to measure tick abun- Questionnaire and sample vial data were entered into an dance on dogs and to understand their spatial distribution Excel (Microsoft, Redmond, WA, USA) spreadsheet. [9, 10, 12–14]. Italy is a European country with many spe- Ticks were identified to species level, life-stage (i.e. larva, cies of ticks, with about 40 different species reported [3]. nymph or adult) and gender (female or male) under a However, to date, there has been no surveillance program stereomicroscope using appropriate morphological keys in Italy, and information regarding Italian ixodofauna of [22–24]. dogs is limited to local surveys of single tick species and Specimens (86) that were difficult to identify from their pathogens [15], or to ticks collected from the environ- morphological characterization were selected for genetic ment [16–20]. analysis. DNA was extracted using a commercial kit The aim of this study was to conduct the first national (HiPurA™ PCR Product Purification Kit, HiMedia, Mum- Italian survey of ticks in privately owned dogs presented bai, India) in accordance with the manufacturer’s in- to veterinary practices and to develop a spatial distribu- structions. Partial mitochondrial 12S rRNA and 16S tion framework of different tick species. Risk factors as- rRNA gene sequences were generated and analyzed sociated with tick infestation, seasonality and acaricide using primers and PCR conditions as previously de- efficacy were recorded and analyzed. scribed [24, 25]. Amplicons were resolved in ethidium bromide-stained (1.5%) agarose gels (Bio-Rad, Madrid, Methods Spain) and sized by comparison with a marker in the 6X Study design and tick collection DNA Loading Dye (Thermo Fisher Scientific, Waltham, A nationwide survey was performed in Italy from Febru- USA). Gels were photographed using a digital documen- ary 2016 to September 2017. The project involved vol- tation system (Gel Doc 2000, Bio-Rad, Watford, UK). untary participation of veterinary practices in different PCR products (amplicons) were purified (HiPurA™ areas of Italy. The dogs enrolled in the study were Mammalian Genomic DNA Purification Kit, HiMedia) homogeneously distributed across the regions using a and sequenced. Sequences were analyzed using the criterion of proportional allocation, i.e. each region was Chromas version 2.1.1 software and compared with the assigned a number of dogs proportional to the total partial mitochondrial 12S and 16S rRNA gene sequences number of dogs registered in each region [21]. Each vet- in GenBank. erinary practice was provided with a “tick survey pack- age” containing the study protocol, 60 questionnaires, 60 Mapping and statistical analysis sample vials with 70% ethanol and a tick removal hook. The location of positive dogs for each tick genera was The protocol instructed participating vets to examine at geo-referenced using a geographical information system least five dogs per month for ticks over the 20-month (GIS, ArcGIS version 10.3 ESRI), referring to the owner’s study period. Dogs were to be randomly chosen without postcode or, if missing, to the veterinary practice post- prior knowledge of their tick infestation status. The code for the dog. GIS was also used to analyze spatial in- questionnaire requested information on the location of formation on body locations of ticks on examined dogs. the sampled dog (post code of the owner or, if this was Tick infestation differences were analyzed in association not given, the practice postcode), breed, sex, age, hair with dog sex, age, hair length (long and short), habitat (in- length and recent ectoparasiticidal treatment (the last door or outdoor/kennel) and environment (urban or rural/ treatment for ticks and the drug used). Additional sylvatic) using the Chi-square test, with presence or absence questions included: the type of housing (indoor or out- of ticks as dependent variable. Four categories were used door/kennel), the environment in which dog is usually for dog gender: male, female, male neutered and female moved (urban, rural/sylvatic), and the attachment site neutered. Dogs were classed into five groups for the age of ticks if present.
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