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Establishment of Babesia vulpes n. sp. (Apicomplexa: Babesiidae), a piroplasmid species pathogenic for domestic dogs.

ABSTRACT: BACKGROUND:Canine babesiosis is a severe disease caused by several Babesia spp. A number of names have been proposed for the canine-infecting piroplasmid pathogen initially named Theileria annae Zahler, Rinder, Schein & Gothe, 2000. It was shown to be a member of the Babesia (sensu lato) group infecting carnivores and is also closely related to the Babesia microti group. Subsequently, the same parasite species was reclassified as a member of the genus Babesia and the name Babesia vulpes Baneth, Florin-Christensen, Cardoso & Schnittger, 2015 was proposed for it. However, both names do not meet the requirements of the International Code of Zoological Nomenclature (no accompanying descriptions, no deposition of type-specimens) and cannot be recognized as available names from the nomenclatural point of view. The purpose of this study was to further characterize this parasite in order to confirm its validity, to provide its description and to introduce zoological nomenclature for it with the name Babesia vulpes n. sp. RESULTS:Morphological description of the parasite in canine erythrocytes demonstrated that it takes the shape of small (1.33?×?0.98 µm), round to oval forms reminiscent of the pyriform and ring shapes of other small canine Babesia spp., such as Babesia gibsoni Patton, 1910 and Babesia conradae Kjemtrup, Wainwright, Miller, Penzhorn & Carreno, 2006. However, these parasite forms were overall smaller than those measured for the latter two species and no tetrad (Maltese cross) form was reported. Furthermore, phylogenetic analysis using the cytochrome c oxidase subunit 1 (COX1) amino acid sequences substantiates the species identity of this parasite as previously demonstrated based on phylogenetic analysis of the 18S rRNA and ?-tubulin genes. The holotype of the parasite species was designated and deposited in an accessible public collection. CONCLUSIONS:This study ratifies the name Babesia vulpes n. sp. proposed for the parasite previously referred to as Theileria annae Zahler, Rinder, Schein & Gothe, 2000, Babesia annae (Zahler, Rinder, Schein & Gothe, 2000) or Babesia vulpes Baneth, Florin-Christensen, Cardoso & Schnittger, 2015, or mentioned as "Babesia microti-like piroplasm", "Babesia Spanish dog isolate" and Babesia cf. microti.

SUBMITTER: Baneth G

PROVIDER: S-EPMC6434798 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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Establishment of Babesia vulpes n. sp. (Apicomplexa: Babesiidae), a piroplasmid species pathogenic for domestic dogs.

Baneth Gad G Cardoso Luís L Brilhante-Simões Paula P Schnittger Leonhard L

Parasites & vectors 20190326 1

<h4>Background</h4>Canine babesiosis is a severe disease caused by several Babesia spp. A number of names have been proposed for the canine-infecting piroplasmid pathogen initially named Theileria annae Zahler, Rinder, Schein & Gothe, 2000. It was shown to be a member of the Babesia (sensu lato) group infecting carnivores and is also closely related to the Babesia microti group. Subsequently, the same parasite species was reclassified as a member of the genus Babesia and the name Babesia vulpes ...[more]

PMID: 30909951

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Project description:BackgroundBabesiosis is a tick-borne infection caused by piroplasmid protozoa and associated with anemia and severe disease in humans, domestic animals and wildlife. Domestic cats are infected by at least six Babesia spp. that cause clinical disease.MethodsInfection with a piroplasmid species was detected by microscopy of stained blood smears in three sick cats from Israel. Genetic characterization of the piroplasmid was performed by PCR amplification of the 18S rRNA, cytochorme B (CytB) and heat shock protein 70 (HSP70) genes and the internal transcribed spacer (ITS) locus, DNA sequencing and phylogenetic analysis. In addition, Haemaphysalis adleri ticks collected from two cats were analyzed by PCR for piroplasmids.ResultsThe infected cats presented with anemia and thrombocytopenia (3/3), fever (2/3) and icterus (1/3). Comparison of gene and loci sequences found 99-100% identity between sequences amplified from different cats and ticks. Constructed phylogenetic trees and DNA sequence comparisons demonstrated a previously undescribed Babesia sp. belonging to the Babesia sensu stricto (clade X). The piroplasm forms detected included pear-shaped merozoite and round-to-oval trophozoite stages with average sizes larger than those of Babesia felis, B. leo and B. lengau and smaller than canine Babesia s.s. spp. Four of 11 H. adleri adult ticks analyzed from cat # 3 were PCR positive for Babesia sp. with a DNA sequence identical to that found in the cats. Of these, two ticks were PCR positive in their salivary glands, suggesting that the parasite reached these glands and could possibly be transmitted by H. adleri.ConclusionsThis study describes genetic and morphological findings of a new Babesia sp. which we propose to name Babesia galileei sp. nov. after the Galilee region in northern Israel where two of the infected cats originated from. The salivary gland PCR suggests that this Babesia sp. may be transmitted by H. adleri. However, incriminating this tick sp. as the vector of B. galilee sp. nov. would require further studies.

Project description:IntroductionBabesiosis is a protozoan tick-borne infection associated with anemia and life-threatening disease in humans, domestic and wildlife animals. Dogs are infected by at least six well-characterized Babesia spp. that cause clinical disease. Infection with a piroplasmid species was detected by light microscopy of stained blood smears from five sick dogs from Israel and prompted an investigation on the parasite's identity.MethodsGenetic characterization of the piroplasmid was performed by PCR amplification of the 18S rRNA and the cytochrome c oxidase subunit 1 (cox1) genes, DNA sequencing and phylogenetic analysis. Four of the dogs were co-infected with Borrelia persica (Dschunkowsky, 1913), a relapsing fever spirochete transmitted by the argasid tick Ornithodoros tholozani Laboulbène & Mégnin. Co-infection of dogs with B. persica raised the possibility of transmission by O. tholozani and therefore, a piroplasmid PCR survey of ticks from this species was performed.ResultsThe infected dogs presented with fever (4/5), anemia, thrombocytopenia (4/5) and icterus (3/5). Comparison of the 18S rRNA and cox1 piroplasmid gene sequences revealed 99-100% identity between sequences amplified from different dogs and ticks. Phylogenetic trees demonstrated a previously undescribed species of Babesia belonging to the western group of Babesia (sensu lato) and closely related to the human pathogen Babesia duncani Conrad, Kjemtrup, Carreno, Thomford, Wainwright, Eberhard, Quick, Telfrom & Herwalt, 2006 while more moderately related to Babesia conradae Kjemtrup, Wainwright, Miller, Penzhorn & Carreno, 2006 which infects dogs. The piroplasm forms detected included tetrads (Maltese cross), merozoite and trophozoite stages whose average size was larger than stages of other canine Babesia spp. belonging to the Babesia (s.l.) and B. gibsoni Patton, 1910, and smaller than other canine Babesia (sensu stricto) spp. Of 212 O. tholozani ticks surveyed, 11 (5.2%) harbored DNA of the new species of Babesia.ConclusionsBabesia negevi n. sp. is described based on morphological and genetic characterization and phylogenetic analyses. The species is named after the Negev desert of southern Israel, where the first infected dog originated from. Despite co-infection in four dogs, the fifth dog had fatal disease attesting that B. negevi n. sp. infection requires clinical attention. Incriminating O. tholozani or another tick species as the vector of Babesia negevi n. sp., would require additional studies.

Project description:BackgroundTheileria annae is a tick-transmitted small piroplasmid that infects dogs and foxes in North America and Europe. Due to disagreement on its placement in the Theileria or Babesia genera, several synonyms have been used for this parasite, including Babesia Spanish dog isolate, Babesia microti-like, Babesia (Theileria) annae, and Babesia cf. microti. Infections by this parasite cause anemia, thrombocytopenia, and azotemia in dogs but are mostly subclinical in red foxes (Vulpes vulpes). Furthermore, high infection rates have been detected among red fox populations in distant regions strongly suggesting that these canines act as the parasite's natural host. This study aims to reassess and harmonize the phylogenetic placement and binomen of T. annae within the order Piroplasmida.MethodsFour molecular phylogenetic trees were constructed using a maximum likelihood algorithm based on DNA alignments of: (i) near-complete 18S rRNA gene sequences (n = 76 and n = 93), (ii) near-complete and incomplete 18S rRNA gene sequences (n = 92), and (iii) tubulin-beta gene sequences (n = 32) from B. microti and B. microti-related parasites including those detected in dogs and foxes.ResultsAll phylogenetic trees demonstrate that T. annae and its synonyms are not Theileria parasites but are most closely related with B. microti. The phylogenetic tree based on the 18S rRNA gene forms two separate branches with high bootstrap value, of which one branch corresponds to Babesia species infecting rodents, humans, and macaques, while the other corresponds to species exclusively infecting carnivores. Within the carnivore group, T. annae and its synonyms from distant regions segregate into a single clade with a highly significant bootstrap value corroborating their separate species identity.ConclusionPhylogenetic analysis clearly shows that T. annae and its synonyms do not pertain to Theileria and can be clearly defined as a separate species. Based on the facts that T. annae and its synonyms have not been shown to have a leukocyte stage, as expected in Theileria, do not infect humans and rodents as B. microti, and cluster phylogenetically as a separate species, this study proposes to name this parasite Babesia vulpes sp. nov., after its natural host, the red fox V. vulpes.

Project description:BackgroundThe Babesia microti-like parasite is an emerging tick-borne piroplasm that has been detected in a range of hosts worldwide. Babesia vulpes, which is found in dogs and foxes, has been reclassified from B. microti-like parasites. The relationships among these B. microti-like parasites and B. vulpes with respect to host range and geographical origin have not been elucidated.MethodsBlood samples were collected from 27 raccoon dogs in South Korea and used to screen for B. microti-like parasites based on a PCR assay targeting the 18S rRNA gene of Babesia. For comparative purposes, in addition to 18S rRNA sequences from nine raccoon dogs, we also analyzed 18S rRNA sequences from B. microti-like parasites infecting hosts in different geographical regions worldwide obtained from the GenBank database, giving 123 sequences in total. The genetic variation and evolutionary relationships among these sequences were examined based on analyses using DnaSP, MEGA, Arlequine, and BEAST software.ResultsBabesia microti-like parasites were identified in nine raccoon dogs and found to be related to B. vulpes obtained from Spanish dogs. Among the 123 sequences from 14 countries and various hosts, we identified 43 haplotypes with high genetic variance. Based on the genetic variance and phylogenetic analyses, we established that the B. microti-like parasites isolated in different geographical regions and from hosts belonging to five orders showed higher among-population variation than within-population variation. Babesia vulpes parasites infecting carnivore hosts, including raccoon dogs, foxes, skunks and dogs, appear to be genetically distinct from B. microti-like parasites infecting hosts belonging to the other orders.ConclusionsOur study demonstrated the genetic variation and evolutionary relationships among 18S rRNA sequences obtained from blood samples collected from various hosts and different geographical regions. Babesia vulpes was identified from raccoon dogs in South Korea. In addition, higher genetic variations were observed among populations of different hosts and geographical origins and, in particular, low connectivity was observed among host populations in the order Carnivora and those in other orders. These results suggest the B. vulpes, a piroplasmid species pathogenic in domestic dogs and wild canines, is genetically and evolutionarily different from B. microti-like parasites.

Project description:This is the first comprehensive review of the literature pertaining to Babesia species reported from domestic cats. Description of the four species (Babesia felis, Babesia cati, Babesia herpailuri, and Babesia pantherae) named based on morphology and/or host specificity is documented. Feline babesiosis is of major veterinary concern only in South Africa. Reports of the rare occurrence of feline babesiosis cases in Europe (France, Germany, Poland, and Spain) and Asia (Israel, India, and Pakistan) are documented. Molecular characterization has revealed that cats can harbor a variety of Babesia species. The previous practice of referring to all piroplasms, especially small ones, seen on feline blood smears as B. felis is therefore no longer tenable. The near-full-length 18S rRNA gene sequences entered into GenBank in 2001 (accession no. AF244912) are designated as definitive for B. felis sensu stricto. All published literature relating to molecular characterization of feline Babesia species that could be traced was critically assessed. Four Babesia species are now known to be involved in causing feline babesiosis in South Africa: the closely related B. felis s.s. and Babesia leo (clade I), Babesia lengau (clade II), and Babesia species cat Western Cape (clade VI, Babesia s.s.). Clade VI also includes Babesia canis presentii and Babesia hongkongensis reported from cats in Asia. Six other Babesia species have been reported from domestic cats: the dog-associated B. canis s.s., Babesia gibsoni, and B. vogeli, as well as Babesia lohae, Babesia microti, and Babesia vulpes. Phylogenetic relationships of all named species were assessed and are presented as trees. The relatively high prevalence of B. vogeli in clinically healthy cats (16% in Brazil, 13% on St Kitts, and 8.1% in Portugal) suggests that immunocompetent cats can harbor the infection with no discernible untoward effects. Reports of occurrence of B. felis and other Babesia species in domestic cats should be accepted only if they are supported by credible molecular provenance.

Dataset Information

Establishment of Babesia vulpes n. sp. (Apicomplexa: Babesiidae), a piroplasmid species pathogenic for domestic dogs.

Publications

Establishment of Babesia vulpes n. sp. (Apicomplexa: Babesiidae), a piroplasmid species pathogenic for domestic dogs.

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