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SHABANGU Et Al. 2021.Pdf Veterinary Parasitology 291 (2021) 109381 Contents lists available at ScienceDirect Veterinary Parasitology journal homepage: www.elsevier.com/locate/vetpar A shared pathogen: Babesia rossi in domestic dogs, black-backed jackals (Canis mesomelas) and African wild dogs (Lycaon pictus) in South Africa Ntji Shabangu a, Barend L. Penzhorn a,b,c, Marinda C. Oosthuizen a,b, Ilse Vorster a, O. Louis van Schalkwyk d, Robert F. Harrison-White e, P. Tshepo Matjila a,* a Vectors and Vector-borne Diseases Programme, Department of Veterinary Tropical Diseases, Faculty of Veterinary Science, University of Pretoria, Private Bag X04, Onderstepoort, 0110, South Africa b Centre for Veterinary Wildlife Studies, Faculty of Veterinary Science, University of Pretoria, South Africa c National Zoological Garden, South African National Biodiversity Institute, P.O. Box 754, Pretoria, 0001, South Africa d Office of the State Veterinarian, Skukuza, Kruger National Park, 1350, South Africa e Wildlife Damage – Research and Management, P.O. Box 783540, Sandton, 2146, South Africa ARTICLE INFO ABSTRACT Keywords: In sub-Saharan Africa, babesiosis in domestic dogs is caused primarily by Babesia rossi. Black-backed jackals African wild dog (Canis mesomelas), which are subclinical carriers of B. rossi, were a likely reservoir host from which infection Babesia rossi passed to domestic dogs. The role of other indigenous canids, e.g. African wild dogs (Lycaon pictus), as reservoirs Black-backed jackal of B. rossi has not been elucidated. The question also arises whether genetic differences have arisen between Canis mesomelas B. rossi infecting domestic dogs and “ancestral” B. rossi in jackals. In a previous study we found that nearly one- Lycaon pictus Reservoir host third (27 of 91) of jackals were infected with B. rossi; this was confirmedby 18S rDNA sequence analysis. In this South Africa study, the near full-length B. rossi 18S rRNA gene was successfully amplified from 6 domestic dogs and 3 black- backed jackals. The obtained recombinant sequences were identical (100 %) to previously described B. rossi sequences of black-backed jackals in South Africa, and 99 % similar to B. rossi from dogs in South Africa and the Sudan. Although blood specimens from 5 (10 %) of 52 free-ranging African wild dogs (from Kruger National Park, South Africa, reacted with the B. rossi probe on RLB hybridisation, the presence of B. rossi could not be confirmed by amplification and sequencing, nor by multiplex, real-time PCR. Although African wild dogs they can be infected with B. rossi without showing clinical signs, our findings suggest that they are apparently not important reservoir hosts of B. rossi. 1. Introduction while adult ticks prefer carnivores, both canid and felid (Horak et al., 2018). Adult female H. elliptica, which ingest B. rossi when engorging on In sub-Saharan Africa, babesiosis in domestic dogs is caused pri­ an infected canid host, pass the infection transovarially; B. rossi is marily by Babesia rossi (Matjila et al., 2008a; Penzhorn, 2020). transmitted only by adult ticks of the subsequent generation (Lounsbury, Black-backed jackals (Canis mesomelas), which occur in two discrete 1904; Lewis et al., 1996). In areas where its off-host ecological re­ geographic ranges in southwestern and northeastern Africa (Kingdon quirements are met, H. elliptica is the most prevalent tick in black-backed and Hoffmann, 2013), harbour B. rossi without showing any clinical jackal populations (Penzhorn et al., 2020). These jackals are therefore signs (Neitz and Steyn, 1947; van Heerden, 1980). In a previous study likely reservoirs from which domestic dogs initially became infected we found that nearly one-third (27 of 91) of a free-ranging black-backed with B. rossi (Penzhorn, 2011; Penzhorn et al., 2017) jackal population was subclinically infected with B. rossi (Penzhorn Dogs are not native to sub-Saharan Africa, but have been present for et al., 2017). many centuries (Mitchell, 2015). It is postulated that through natural Haemaphysalis elliptica, the only confirmed vector of B. rossi, occurs selection, African dog types such as Africanis have developed the ability commonly in the more mesic parts of southern Africa (Theiler and to cope with B. rossi infection, while exotic dog breeds are highly sus­ Robinson, 1953). Immature stages feed primarily on murid rodents, ceptible (Penzhorn, 2011). Once established, infections can be * Corresponding author. E-mail address: [email protected] (P.T. Matjila). https://doi.org/10.1016/j.vetpar.2021.109381 Received 29 July 2020; Received in revised form 2 February 2021; Accepted 3 February 2021 Available online 14 February 2021 0304-4017/© 2021 Elsevier B.V. All rights reserved. N. Shabangu et al. Veterinary Parasitology 291 (2021) 109381 maintained in domestic dog populations in the absence of jackals clinical signs of babesiosis and B. rossi recovered form black-backed (Morters et al., 2020). The questions arises, therefore, whether genetic jackals; and (b) the prevalence of B. rossi in free-ranging African wild differences have arisen between B. rossi infecting domestic dogs and dogs, through molecular detection. “ancestral” B. rossi in jackals. In a previous study conducted in our laboratory, blood specimens 2. Materials and methods from 33 (30.8 %) of 107 black-backed jackals reacted with the B. rossi probe on Reverse Line Blot (RLB) assay (Penzhorn et al., 2017). To 2.1. Sample collection confirm the RLB results, two of the positive specimens were analysed further. After amplification and cloning of near full-length 18S rRNA Blood was collected into Ethylenediaminetetra-acetic acid (EDTA) gene from these two samples, six recombinants yielded sequences vacutainer tubes from the cephalic vein, refrigerated and transported to identical to that of B. rossi (L19079) in GenBank and differing by two the Department of Veterinary Tropical Diseases. As part of a previous base pairs from B. rossi (DQ111760). There were 1,502 positions in the study, blood samples (n = 75) were collected over a six-year period final dataset. The original specimens were still available. More of the (2000–2006) from dogs presented at the Outpatients Clinic of the positive specimens could therefore be analysed further, to give a clearer Onderstepoort Veterinary Academic Hospital (OVAH) (Matjila et al., indication of possible genetic variation. 2008a) (Fig. 1). Blood samples from free-ranging (n = 91) and captive (n For comparison, blood specimens from 75 dogs presented to the = 6) black-backed jackals had been collected at Mogales Gate Biodi­ Outpatients Clinic of the Onderstepoort Veterinary Academic Hospital versity Centre, northwestern Gauteng, in 2012 and 2014 and at S.A. (OVAH) and tentatively diagnosed as suffering from babesiosis were Lombard Nature Reserve near Bloemhof, North West Province, South available. These specimens had been used in a previous study (Matjila Africa (Penzhorn et al., 2017) (Fig. 1). African wild dog blood samples (n et al., 2008a). = 52) were collected from a free-ranging population, primarily in the Occurrence and prevalence of B. rossi infection in other indigenous southern half of the KNP (Fig. 1). Additional blood samples from captive canid species has not been well documented. Some captive African wild African wild dogs (n = 6) were obtained from the biobank at the Na­ dogs (Lycaon pictus) have been shown to be infected (Matjila et al., tional Zoological Garden, South African National Biodiversity Institute, 2008b), but reports from free-ranging wild dogs are meagre (Peirce Pretoria, South Africa (Fig. 1). et al., 1995; van Heerden et al., 1995). Mortality due to babesiosis has been recorded in a zoo-born pup (Colly and Nesbit, 1992). On the other 2.2. DNA extraction hand, three 6-month-old African wild dogs infected intravenously with heparinised blood from a terminally sick domestic dog developed par­ Genomic DNA was extracted from 200 μL of EDTA anticoagulated ◦ asitaemias but showed no clinical signs of infection (van Heerden, whole blood (stored at 20 C) using the QIAamp®DNA mini kit (Qia­ 1980). Blood collected from individual African wild dogs on Day 29 after gen, Southern Cross Biotechnology, Hilden, Germany), following man­ infection and injected intravenously into three different domestic dogs ufacturer’s instructions. resulted in severe clinical signs, suggesting that African wild dogs could be reservoirs of infection (van Heerden, 1980). A general health survey 2.3. Reverse line blot hybridisation of the African wild dog population in the southern half of the Kruger National Park (KNP) where both black-backed jackals and H. elliptica The Reverse Line Blot (RLB) hybridization assay, as previously occur, offered the opportunity of examining a large set of blood speci­ described by Gubbels et al. (1999), was performed on all samples. The mens for the presence of haemoprotozoa. oligonucleotide probes and their sequences used for detecting pathogen The objectives of this study were to determine (a) whether there DNA with PCR-RLB hybridization are listed in Table 1. Babesia bovis and were genetic differences between B. rossi in domestic dogs showing Anaplasma centrale known positives were used as positive control to Fig. 1. Map of the north-eastern part of South Africa, indicating the origins of the various blood specimens included in the study: (1) S.A. Lombard Nature Reserve, near Bloemhof, North West Province; (2) Mogale’s Gate Biodiversity Centre, Gauteng; Pretoria, Gauteng (Onderstepoort Veterinary Academic Hospital and National Zoological Garden; (4) Kruger National Park, Mpumalanga and Limpopo Provinces. 2 N. Shabangu et al. Veterinary Parasitology 291 (2021) 109381 Table 1 Table 1 (continued ) List of oligonucleotide probes and their sequences used for detecting pathogen 0 0 Oligonucleotide probes Sequences (5 -3 ) Reference DNA with PCR-RLB hybridization. R = A / G, W = A / T are the symbols used to indicate degenerate positions. Babesia vogeli AGC GTG TTC GAG TTT Matjila et al. (2004) GCC 0 0 Oligonucleotide probes Sequences (5 -3 ) Reference Ehrlichia / Anaplasma genus- GGG GGA AAG ATT TAT Bekker et al.
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