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Detection of Babesia Odocoilei in Ixodes Scapularis Ticks Collected from Songbirds in Ontario and Quebec, Canada

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Detection of Babesia Odocoilei in Ixodes Scapularis Ticks Collected from Songbirds in Ontario and Quebec, Canada pathogens Article Detection of Babesia odocoilei in Ixodes scapularis Ticks Collected from Songbirds in Ontario and Quebec, Canada John D. Scott *, Emily L. Pascoe , Muhammad S. Sajid and Janet E. Foley Department of Medicine and Epidemiology, School of Veterinary Medicine, University of California Davis, Davis, CA 95616, USA; [email protected] (E.L.P.); [email protected] (M.S.S.); [email protected] (J.E.F.) * Correspondence: [email protected] Received: 19 August 2020; Accepted: 16 September 2020; Published: 24 September 2020 Abstract: Songbirds widely disperse ticks that carry a diversity of pathogens, some of which are pathogenic to humans. Among ticks commonly removed from songbirds, the blacklegged tick, Ixodes scapularis, can harbor any combination of nine zoonotic pathogens, including Babesia species. From May through September 2019, a total 157 ticks were collected from 93 songbirds of 29 species in the Canadian provinces of Ontario and Québec. PCR testing for the 18S gene of Babesia species detected Babesia odocoilei in 12.63% of I. scapularis nymphs parasitizing songbirds in Ontario and Québec; none of the relatively small numbers of Ixodes muris, Ixodes brunneus, or Haemaphysalis leporispalustris were PCR-positive. For ticks at each site, the prevalence of B. odocoilei was 16.67% in Ontario and 8.89% and 5.26% in Québec. Of 31 live, engorged I. scapularis larvae and nymphs held to molt, 25 ticks completed the molt; five of these molted ticks were positive for B. odocoilei. PCR-positive ticks were collected from six bird species—namely, Common Yellowthroat, Swainson’s Thrush, Veery, House Wren, Baltimore Oriole, and American Robin. Phylogenetic analysis documented the close relationship of B. odocoilei to Babesia canis canis and Babesia divergens, the latter a known pathogen to humans. For the first time in Canada, we confirm the transstadial passage of B. odocoilei in I. scapularis molting from larvae to nymphs. A novel host record reveals I. scapularis on a Palm Warbler. Our findings show that B. odocoilei is present in all mobile life stages of I. scapularis, and it is widely dispersed by songbirds in Ontario and Québec. Keywords: Babesia odocoilei; piroplasm; human babesiosis; songbirds; ticks; Ixodes scapularis; parasitism; Canada 1. Introduction Ticks carry a wide spectrum of disease-causing microorganisms that cycle between vectors and hosts, including humans. Some of these ectoparasites are laden with tick-borne zoonotic pathogens, including Babesia spp. (Apicomplexa: Piroplasmida: Babesiidae). These malaria-like piroplasms, which invade red blood cells, were first discovered by the Romanian researcher Victor Babes in 1888 [1–3]. The first description of human babesiosis was a fatal case in a splenectomized farmer in Croatia [4]. Although ticks were identified as vectors shortly after the discovery of the pathogen [5], more recently, this apicomplexan microorganism has also been found to be transmitted to humans by blood transfusion [6,7], by organ transplantation [8], and by maternal–fetal transmission [9,10]. Babesia species are typically host-specific and, globally, they infect a wide range of vertebrate hosts. These Babesia spp. often result in reduced fitness and mortality in wildlife and domestic animals, producing economic losses with low productivity and added mortality. Epidemiologically, they also cause morbidity and mortality in humans worldwide [2–4,11–16]. Human babesiosis is reported in Pathogens 2020, 9, 781; doi:10.3390/pathogens9100781 www.mdpi.com/journal/pathogens Pathogens 2020, 9, 781 2 of 13 Canada and the United States, sometimes with fatal outcomes [11,17]. Babesia species that bring about pathogenicity in humans include B. microti, B. crassa, B. duncani, B. venatorum, B. divergens, Babesia divergens-like MO-1, Babesia sp. KO-1, Babesia sp. XXB/HangZhou, and Babesia spp. CA1, CA3, and CA4 [11,17–19]. Migratory songbirds (Passeriformes) disperse ticks and tick-borne pathogens across regional and transcontinental areas. These migrants occasionally support the establishment of ticks and pathogens in new foci [20,21]. Some songbirds, such as the American Robin, are reservoirs of the Lyme disease bacterium, Borrelia burgdorferi sensu lato [22]; however, passerine species are not known to be reservoir-competent hosts of Babesia spp. Even if birds are refractory to infection with a tick-borne pathogen, they can host ticks that are already infected with disease-producing microbes. For example, the blacklegged tick, Ixodes scapularis (Acari: Ixodidae), an important human-biting tick in eastern and central North America, can harbor any combination of nine different zoonotic pathogens, including Babesia species [23]. A nymphal I. scapularis, which parasitized a spring-migrating Veery in southeastern New York state, was triple co-infected with B. burgdorferi sensu lato, Babesia microti, and Anaplasma phagocytophilum [24]. Certain cervids (i.e., caribou, deer, elk) are reservoirs of Babesia odocoilei, while I. scapularis ticks are vectors of this babesial infection. In many parts of eastern and central North America, I. scapularis ticks and cervine hosts co-habitat in nature to maintain B. odocoilei. Passerine birds are common incidental hosts of I. scapularis larvae and nymphs, and occasionally, these ticks are infected with B. odocoilei. Based on current knowledge, cervids and I. scapularis form a collective hub for the enzootic transmission cycle of B. odocoilei. Although B. odocoilei has been investigated as a pathogen of cervids, it has not been examined closely as a potential source of human babesiosis. The aim of this study was to detect and identify, to species, any Babesia DNA in ticks collected from migratory songbirds in two provinces in Canada. 2. Materials and Methods 2.1. Collection of Ticks from Songbirds Bird banders and wildlife rehabilitators collected ixodid ticks from songbirds captured at five locations (Figure1) between 23 April and 30 September 2019. They removed ticks using fine-pointed hardened stainless steel, #5, superfine-tipped forceps (BioQuip Products, Rancho Dominguez, CA, USA). There were three collection sites in Ontario (Ruthven Park, Long Point, and Toronto) and two in Québec (Ste-Anne-de-Bellevue and Montée Biggar). These technicians and collectors placed live ticks into transparent 8.5 mL, 15.7 mm 75 mm, round-bottomed polypropylene tubes (Sarstedt, Montréal, × Québec, Canada); each tube contained ticks from a single host. In order to prevent ticks from escaping and provide ventilation, a 3 cm piece of tulle netting was placed over the mouth of the tube, and a push cap, which had a 7 mm hole, was inserted into the tube opening. All ticks were promptly mailed in a double-zipper plastic bag with a moistened paper towel to the laboratory (JDS) for identification. Partially and fully engorged larval and nymphal ticks were held to molt to the next developmental life stage at a long-day photoperiod of 16:8 (L:D) h at room temperature in humidity from 90% to 95%. For the statistical analyses, molted ticks were designated the life stage at the time of collection. Taxonomic keys and descriptions were utilized for identification [25–29]. Pathogens 2020, 9, 781 3 of 13 Pathogens 2020, 9, x FOR PEER REVIEW 3 of 14 Figure 1. Map ofFigure Ontario 1. Map of Ontario and Quand Québecébec showing showing tick collection tick collection sites. (1) McGill sites.Bird Observatory, (1) McGill Ste-Anne- Bird Observatory, de-Bellevue, Québec; 45.43N, 73.94W. (2) Montée Biggar, Québec; 45.09N, 74.22W. (3) Fatal Light Awareness Ste-Anne-de-Bellevue,Program, QuToronto,ébec; Ontario; 45.43 43.74N, N, 73.94 79.37W. W. (4) (2)Ruthven Mont Parké eNational Biggar, Historic Qu éSitebec; Banding 45.09 Station, N, 74.22 W. (3) Fatal Light AwarenessHaldimand Program, Bird Toronto,Observatory, Ontario;Cayuga, Ontario; 43.74 42.97N, N, 79.3779.87W. W.(5) Long (4) Point Ruthven Bird Observatory, Park National Long Historic Site Point (Port Rowan), Ontario; 42.52N, 80.17W. Banding Station, Haldimand Bird Observatory, Cayuga, Ontario; 42.97 N, 79.87 W. (5) Long Point Bird Observatory,2.2. Long DNA Point Extraction (Port and PCR Rowan), Ontario; 42.52 N, 80.17 W. Unfed ticks were subjected to an ammonium hydroxide DNA extraction protocol as described previously [30], whereas DNA from fed ticks was extracted using the Qiagen DNeasy Blood and Tissue Kit 2.2. DNA Extraction(Qiagen, and Valencia, PCR CA, USA) following the manufacturer’s protocol for animal tissue. Ticks were initially pooled according to bird host; however, upon discovering the relatively high prevalence, we decided to Unfed ticksprocess were ticks subjected individually to. DNA an was ammonium stored at −20 °C hydroxideuntil PCR was performed. DNAextraction Conventional PCR protocol was as described previously [30], whereasused to detect DNA the from18S ribosomal fed ticks RNA was(rRNA) extracted gene of the usinggenus Babesia the Qiagen, with 25 µL DNeasy reaction mixes Blood and Tissue Kit containing 2.5 µL each of 5 µM primers BJ1 (5′-GTC-TTG-TAA-TTG-GAA-TGA-TGG-3′) and BN2 (5′-TAG- (Qiagen, Valencia,TTT-ATG-GTT-AGG-ACT-ACG-3 CA, USA) following the′) [31], manufacturer’s 5 µL nuclease-free water, protocol 12.5 µL for Green animal Go Taq tissue. (Promega, Ticks were initially Madison, WI, USA), and 2.5 µL of DNA at 8–10 ng/µL. PCR was performed under thermal cycling pooled accordingconditions to bird of host;initial denaturation however, at 94 upon °C for 10 discovering min, 35 cycles of the94 °C relativelyfor 1 min, 55 °C high for 1 min, prevalence, and 72 we decided to process ticks individually.°C for 2 min with a DNAfinal extension was at stored 72 °C for at5 min,20 and◦ thenC untilheld at 4 PCR °C. Amplified wasperformed. DNA was visualized Conventional PCR with UV transillumination of a 1% agarose gel containing− GelStar nucleic acid stain (Lonza, Rockland, ME, was used to detectUSA). the Amplicons 18S ribosomalof 400–500 base pairs RNA (bp) (rRNA)were excised genefrom the of gel theand prep genusared forBabesia DNA sequencing, with 25 µL reaction using a gel extraction kit (QIAamp DNA Kit, Qiagen, Valencia, CA, USA).
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