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Tick Infestations of Wildlife and Companion Animals in Ontario, Canada, with Detection of Human Pathogens in Ixodes Scapularis Ticks T

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Tick Infestations of Wildlife and Companion Animals in Ontario, Canada, with Detection of Human Pathogens in Ixodes Scapularis Ticks T Ticks and Tick-borne Diseases 10 (2019) 72–76 Contents lists available at ScienceDirect Ticks and Tick-borne Diseases journal homepage: www.elsevier.com/locate/ttbdis Original article Tick infestations of wildlife and companion animals in Ontario, Canada, with detection of human pathogens in Ixodes scapularis ticks T Kathryn A. Smitha,b, Paul T. Oesterlea,b, Claire M. Jardinea,b, Antonia Dibernardoc, Chris Huynhc, ⁎ Robbin Lindsayc, David L. Pearld, Nicole M. Nemetha,b, ,1 a Department of Pathobiology, University of Guelph, Guelph, ON, Canada b Canadian Wildlife Health Cooperative, University of Guelph, Guelph, ON, Canada c National Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, MB, Canada d Department of Population Medicine, University of Guelph, Guelph, ON, Canada ARTICLE INFO ABSTRACT Keywords: The growing risk of transmission of tick-borne zoonotic pathogens to humans in Ontario, Canada, warrants Anaplasma phagocytophilum investigations into regional tick distribution, tick burdens of local peridomestic animals, and prevalence of tick- Borrelia burgdorferi sensu stricto borne pathogens. The objectives of this study were to investigate the geographic distribution and magnitude of Ixodes scapularis tick infestations in opportunistically sampled mammalian wildlife and companion animals (i.e., dogs) in Canada southern Ontario and to test these ticks for evidence of zoonotic tick-borne pathogens. Ticks collected from Ticks wildlife carcasses, live-trapped wildlife and companion animals (2015–2016), as well as wildlife diagnostic cases Wildlife (2011–2013), were identified to species and life stage. Ixodes scapularis ticks were tested by real-time PCR for Anaplasma phagocytophilum, Babesia microti, Borrelia miyamotoi and Borrelia burgdorferi sensu stricto (s.s.). Amblyomma americanum ticks were tested for Ehrlichia chaffeensis. A total of 1687 ticks of six species were collected from 334 animals, including 224 raccoons (n = 1381 ticks) and 50 dogs (n = 67 ticks). The most common tick species collected from parasitized raccoons were Ixodes texanus (n = 666 ticks) and Dermacentor variabilis (n = 600 ticks), which were removed from 58.5% (median: 2 ticks; range: 1–36) and 49.1% (median: 2 ticks; range: 1–64) of raccoons, respectively. Of I. scapularis tested, 9.3% (4/43) were positive for Bo. burgdorferi s.s. and 2.3% (1/43) for A. phagocytophilum. These results reveal that numerous tick species parasitize common, peridomestic wildlife and that at least two zoonotic, tick-borne pathogens circulate in southern Ontario. Host- tick vector-pathogen dynamics should continue to be monitored in the face of global climate change, landscape alterations and expanding human populations. 1. Introduction that tick-borne pathogens will pose an even greater public health threat in the future (Estrada-Peña and de la Fuente, 2014; Ogden et al., Hard ticks (Acari: Ixodidae) are vectors of numerous zoonotic pa- 2006a). thogens with transmission cycles that involve wildlife and companion Global climate change is likely contributing to shifts in the eco- animal hosts (Dantas-Torres et al., 2012). These hosts often live in close epidemiology of vector-borne pathogens, including increased vulner- proximity to humans, contributing to public health risk and associated ability of regions such as southern Ontario, Canada to the influx and economic burden (Jongejan and Uilenberg, 2009). Further, the geo- potential establishment of tick vectors (Estrada-Peña and de la Fuente, graphic distribution of many tick-borne pathogens is expanding 2014). For example, the northward expansion of Ixodes scapularis ticks northward in the northern hemisphere due to increasingly favorable has led to a higher incidence of Lyme disease, caused by Borrelia environments for ticks and their hosts (Clow et al., 2017b). This on- burgdorferi sensu stricto (s.s.), among humans in Ontario (Bouchard going expansion has been associated with rising incidence of human et al., 2015; Ogden et al., 2006a). Ixodes scapularis may also transmit a tick-borne disease in northern latitudes and led to mounting concern variety of other zoonotic pathogens, including Anaplasma ⁎ Corresponding author. E-mail addresses: [email protected] (K.A. Smith), [email protected] (P.T. Oesterle), [email protected] (C.M. Jardine), [email protected] (A. Dibernardo), [email protected] (C. Huynh), [email protected] (R. Lindsay), [email protected] (D.L. Pearl), [email protected] (N.M. Nemeth). 1 Present address: Southeastern Cooperative Wildlife Disease Study, University of Georgia, Athens, GA, USA. https://doi.org/10.1016/j.ttbdis.2018.08.018 Received 21 June 2018; Received in revised form 15 August 2018; Accepted 29 August 2018 Available online 03 September 2018 1877-959X/ Crown Copyright © 2018 Published by Elsevier GmbH. All rights reserved. K.A. Smith et al. Ticks and Tick-borne Diseases 10 (2019) 72–76 phagocytophilum, Borrelia miyamotoi, and Babesia microti (Lindquist precluded the sex determination of a small proportion of adult ticks. et al., 2016). However, few studies have assessed the geographic dis- tribution and prevalence of tick-borne pathogens in southern Ontario, 2.3. Pathogen detection Canada to identify potentially important regional tick vectors and vertebrate reservoir hosts (Clow et al., 2016a; Nelder et al., 2014; Ticks removed from the same host animal were sorted into pools of Werden et al., 2015). up to 10 conspecific adults or up to 25 nymphs (Dupuis et al., 2013). The present study was carried out to assess common, peridomestic DNA was extracted by using QIAGEN DNeasy 96 tissue kits (Qiagen mammalian wildlife and to a lesser extent, companion animals (i.e., Inc., Mississauga, Canada). dogs; Canis lupus familiaris) for tick infestations in southern Ontario. Amblyomma americanum ticks were tested for E. chaffeensis using Our objectives were to: 1) investigate the geographic distribution and real-time polymerase chain reaction (PCR) targeting the 16S ribosomal tick burdens of parasitized mammalian wildlife (e.g., raccoons, striped RNA (rRNA) gene as previously described (Loftis et al., 2003). Ixodes skunks, and groundhogs) and dogs; and 2) test I. scapularis ticks for scapularis ticks were screened by a duplex real-time PCR assay that evidence of zoonotic tick-borne pathogens, including A. phagocyto- targeted the 23S rRNA gene of Borrelia spp. (including all members of philum, Bo. burgdorferi s.s., Bo. miyamotoi and Ba. microti; and the Bo. burgdorferi sensu lato complex) and the msp2 gene of A. pha- Amblyomma americanum ticks for Ehrlichia chaffeensis. gocytophilum (Courtney et al., 2004). Samples that tested positive for Borrelia spp. were subjected to a confirmatory ospA real-time PCR assay 2. Materials and methods for Bo. burgdorferi s.s. and a glpQ real-time PCR assay for Bo. miyamotoi (Dibernardo et al., 2014; Ullmann et al., 2005). In addition, DNA ex- 2.1. Tick collection from animals tracts from I. scapularis ticks were tested for Ba. microti by a real-time PCR assay targeting the cctƞ gene (Nakajima et al., 2008). All real-time Ticks were opportunistically collected from wildlife carcasses col- PCR testing was performed at the National Microbiology Laboratory lected in Ontario, Canada and donated to the Canadian Wildlife Health (Public Health Agency of Canada, Winnipeg, Manitoba, Canada) as Cooperative (CWHC) from May-December of 2015 and 2016; archived previously described (Dibernardo et al., 2014). ticks from previous CWHC diagnostic cases from 2011 to 2013 were also included. Carcasses were examined for ticks over a 5-min period 2.4. Data and statistical analysis with a focus on less densely haired regions (e.g., inguinal and axillary areas, and ventrum, pinnae) as well as the face. Ticks opportunistically Data for each animal from which ticks were collected included: date collected from dogs at seven veterinary clinics within a 7 km radius of of death (carcass) or tick removal (live animals), host species, number Guelph, Ontario from May 2015 to May 2017 also were contributed to of ticks removed, geographic coordinates of the location where found the study. (wildlife) or town center of the veterinary clinic (dogs) and reported In addition, ticks were collected from live-trapped (and released) travel history outside of Ontario (dogs). In addition, for wild mammals, wildlife during June-October 2016 in Guelph, Hamilton and sex and age (i.e., immature < 1 year and adult ≥1 year) were recorded; Peterborough, Ontario. Wild mammals were trapped using Tomahawk the latter was determined by the animals’ weight. traps (sizes 106 and 108; Tomahawk Live Trap Co. Tomahawk, WI, The prevalence, median, and exact 95% confidence intervals of tick- ® USA). Raccoon (Procyon lotor) and striped skunk (Mephitis mephitis) borne pathogens for each host species were estimated using STATA14 trapping was conducted by the Ontario Ministry Natural Resources and Intercooled (StataCorp, College Station, TX, USA). Forestry (OMNRF). Baited (anchovies, cat food) traps were set in the evening and checked the following dawn. Raccoons and skunks were 3. Results anesthetized with medetomidine (40–50 u g/kg) and tiletamine (1–2 mg/kg) with atipamezole hydrochloride (0.2-0.25 mg/kg) as a A total of 1687 ticks, comprised of six species, were collected from reversal agent. Baited (fruit, oats, peanut butter) traps for groundhogs wildlife and companion animals in southern Ontario. This included (Marmota monax) and eastern gray squirrels (Sciurus carolinensis) were 1580 ticks
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