Don't Let Sleeping Dogs Lie: Unravelling the Identity and Taxonomy of Babesia Canis, Babesia Rossi and Babesia Vogeli
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Penzhorn Parasites Vectors (2020) 13:184 https://doi.org/10.1186/s13071-020-04062-w Parasites & Vectors REVIEW Open Access Don’t let sleeping dogs lie: unravelling the identity and taxonomy of Babesia canis, Babesia rossi and Babesia vogeli Barend L. Penzhorn1,2* Abstract For most of the 20th century the causative agent of canine babesiosis, wherever it occurred in the world, was com- monly referred to as Babesia canis. Early research, from the 1890s to the 1930s, had shown that there were three distinctly diferent vector-specifc parasite entities occurring in specifc geographical regions, that host response to infection ranged from subclinical to acute, and that immunity to one stock of the parasite did not necessarily protect against infection with other stocks. This substantial body of knowledge was overlooked or ignored for 50 years. In this review the frst records and descriptions of the disease in four geographical regions were traced: sub-Saharan Africa, Europe, North Africa and Asia. Research leading to identifcation of the specifc tick vector species involved is docu- mented. Evidence is given of the growing realisation that there were substantial biological diferences between stocks originating from diferent geographical regions. Etymological provenance for Babesia vogeli is proposed. Keywords: Babesia canis, Babesia rossi, Babesia vogeli, Canine babesiosis, Dermacentor reticulatus, Haemaphysalis elliptica, History, Rhipicephalus sanguineus Background those of B. canis (sensu lato), it became common prac- Babesiosis, a tick-transmitted disease afecting dogs in tice to refer to either a large or a small Babesia infect- many parts of the world, is caused by various Babesia ing dogs. Molecular characterisation has indicated that spp. Babesia canis (Piana & Galli-Valerio, 1895) (sensu B. gibsoni falls in the same clade as B. canis (s.l.) (Clade stricto) was described and named in 1895 in northern VI: Babesia (s.s.)) [3]. Te two small Babesia spp. that can Italy [1]. During the next three decades, work by numer- also cause disease in dogs, i.e. B. vulpes Baneth, Cardoso, ous researchers indicated clearly that there were three Brilhante-Simoes & Schnittger, 2019 [4, 5] and B. con- distinct, vector-specifc parasite entities lumped under radae Kjemtrup, Wainwright, Miller, Penzhorn & Car- the name B. canis. Clinical manifestation of infection reno, 2006 [6], fall in Clade I (B. microti-like) and Clade II with these parasites also difered markedly in dogs, rang- (Babesia (s.l.)), respectively [3]. Tis review focuses only ing from subclinical to peracute. In 1910 a separate spe- on B. canis (s.l.) cies, Babesia gibsoni (Patton, 1910), was described from For most of the 20th century the proverbial slumber dogs in India [2]. Since the intraerythrocytic trophozoites of canines was not disturbed. Te causative agent of the and meronts of B. gibsoni were generally smaller than disease, wherever it occurred, was commonly referred to as B. canis, even though it had been amply demonstrated that diferent tick vectors were involved, that some para- *Correspondence: [email protected] site stocks were decidedly virulent, while others caused 1 Vectors and Vector-borne Diseases Research Programme, Department of Veterinary Tropical Diseases, Faculty of Veterinary Science, University mild or no clinical signs even in splenectomised dogs, of Pretoria, Private Bag X04, Onderstepoort 0110, South Africa and that immunity to one stock did not necessarily pro- Full list of author information is available at the end of the article tect against another. Tis was the situation until some 30 © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Penzhorn Parasites Vectors (2020) 13:184 Page 2 of 9 years ago, when Uilenberg et al. [7] presented serological infection. Being the most common canine tick-borne dis- evidence and reminded the scientifc community that not ease in the area, babesiosis is a prime candidate. one but three vector-specifc taxa were involved, which Tere is anecdotal evidence of canine babesiosis cases they named B. canis canis, B. canis vogeli and B. canis in the Eastern Cape Province in the 1840s, Cape Town rossi. By 1998 it had been demonstrated that variation area in the 1870s and KwaZulu-Natal in the 1880s [14]. in the 18S rRNA gene segregated genotypes of B. canis Hutcheon, a colonial veterinarian, frst encountered (s.l.) into distinct groups corresponding to the proposed canine babesiosis when posted to Port Elizabeth, Cape subspecies [8]. Opinion varied as to whether these taxa Colony, in 1885 [15]. In 1893 he described in some detail should be regarded as subspecies of B. canis or distinct the clinical signs, including haemoglobinuria, of what he species. Tere is no universally accepted criterion (% called “malignant jaundice or bilious fever” [16]. Te dis- sequence diference) for classifying organisms to species ease was quite common in coastal towns and districts of level based on variation in the 18S rRNA gene. A recent the Cape Colony, but rarer in higher-lying inland regions. proposal was that the genetic distance between proposed He noted that the disease bore a close resemblance to novel species and their closest described relatives should red-water or Texas Fever of cattle. By 1899 Hutcheon [15] be greater than the genetic distance between the next two referred to the local disease as “malignant malarial fever most closely related species [9]. For the purposes of this of the dog” and stated that it was widespread in the Cape review, the three taxa are regarded as species. Te three Colony and adjoining states. taxa are: (i) Babesia canis (s.s.), transmitted by Derma- Working in Cape Town in 1899, Spreull [17] success- centor reticulatus and historically confned to Europe, fully subinoculated the infection by means of intravascu- but recently reported from China [10]; (ii) Babesia rossi lar and subcutaneous injection of blood from a sick dog (Nuttall, 1910), transmitted by Haemaphysalis elliptica to healthy ones. Blood smears were sent to Dr Carrington (and possibly H. leachi) and confned to sub-Saharan Purvis in Grahamstown, Eastern Cape Province, who Africa; and (iii) the cosmopolitan Babesia vogeli (Reiche- confrmed the presence of pyriform intra-erythrocytic now, 1935), transmitted by Rhipicephalus sanguineus. organisms bearing a strong resemblance to the “now Why was the early research that clearly indicated major well-known redwater organism” [17]. Purvis identifed biological diferences between various canine Babesia the same piroplasm on blood smears from a dog at Gra- stocks overlooked or ignored for 50 years? In this review hamstown, showing similar clinical signs [17]. Following early records and descriptions of the disease in Africa, Spreull, Robertson [18] performed numerous inocula- Europe and Asia are traced and identifcation of the spe- tion experiments, by both subcutaneous and intravenous cifc vectors involved is documented. Evidence is also injection of infected blood. given of the growing realisation that there were substan- In 1901 Robertson [18] stated that the causative organ- tial biological diferences between various stocks (fol- ism of the disease in South Africa is without doubt a lowing Uilenberg et al. [7], this term is used rather that double pyrosoma, resembling “Pyrosoma bigeminum”. strain or isolate). Etymological provenance for B. vogeli is By 1904, Lounsbury [14] was referring to the causative proposed. organism as Piroplasma canis. South Africa Te parasite concerned is regarded as B. rossi, although Pathogenicity B. vogeli could also be involved [11]. Concurrent infec- Hutcheon [15] regarded babesiosis the most fatal disease tion with B. rossi and B. vogeli has been reported [12]. afecting dogs in the Cape Colony. Obtaining blood from a sick dog, Robertson [18] successively subinoculated 13 Early records dogs, all of which succumbed to the disease. Citing Rob- Shortly after arriving in Cape Town in May 1797, Lady ertson (1902), Lounsbury [14] stated that “malignant Anne Barnard recorded in her journal that dogs brought jaundice” was the most serious and one of the most com- from England to South Africa and allowed to roam mon diseases afecting dogs in the Cape Colony. Some freely generally did not live long in their new home [13]. dogs die within 24 hours of the onset of clinical signs, In contrast, English dogs that were tied up usually sur- while most succumb after a few days. Te few dogs that vived. Such precautions were not entirely successful, as survive take weeks or months to recover fully. In a more in November 1797 she referred to a Pointer as their “only recent experiment, fve dogs artifcially infected with English dog that survived the ailment which attacks all B. rossi developed parasitaemias usually much higher who arrive here” [14]. Mortalities occurring in newly than 1% and required chemotherapeutic treatment [19]. imported dogs which had roamed in the indigenous In contrast to dogs artifcially infected with B.