Babesia Species of Domestic Cats: Molecular Characterization Has Opened Pandora's Box

Abstract

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.

Keywords: Babesia canis presentii; Babesia felis; Babesia hongkongensis; Babesia lengau; Babesia leo; Babesia species cat Western Cape; Babesia vogeli; feline babesiosis.

Figure 1

Maximum likelihood tree showing the evolutionary relationships of the published near-full-length Babesia 18S rDNA sequences. Babesias described from domestic cats are indicated in dark blue. Sequence accession numbers are shown in parentheses. The evolutionary history was inferred by using the maximum likelihood method based on the Hasegawa–Kishino–Yano model (HKY + G + I) substitution model (59). The tree with the highest log likelihood (−6,143.13) is shown. The percentage of trees in which the associated taxa clustered together is shown next to the branches. Initial tree(s) for the heuristic search were obtained automatically by applying Neighbor-Join and BioNJ algorithms to a matrix of pairwise distances estimated using the maximum composite likelihood approach and then selecting the topology with superior log likelihood value. A discrete gamma distribution was used to model evolutionary rate differences among sites [five categories (+G, parameter = 0.4871)]. The rate variation model allowed for some sites to be evolutionarily invariable [(+I), 55.35% sites]. The tree is drawn to scale, with branch lengths measured in the number of substitutions per site. All positions containing gaps and missing data were eliminated. There were a total of 1,351 positions in the final data set. Evolutionary analyses were conducted in MEGA7 (60).

Figure 2

Molecular phylogenetic analysis showing relationships between representative B. vogeli and B. gibsoni partial 18S RNA gene sequences described from cats with the published Babesia 18S rDNA sequences. Babesias described from domestic cats are indicated in dark blue. The B. vogeli and B. gibsoni sequences described from domestic cats are indicated in dark green. Sequence accession numbers are shown in parentheses. The evolutionary history was inferred by using the maximum likelihood method based on the Tamura 3-parameter model (62). The tree with the highest log likelihood (−1,898.16) is shown. The percentage of trees in which the associated taxa clustered together is shown next to the branches. A discrete gamma distribution was used to model evolutionary rate differences among sites [five categories (+G, parameter = 0.3970)]. The rate variation model allowed for some sites to be evolutionarily invariable [(+I), 38.96% sites]. The tree is drawn to scale, with branch lengths measured in the number of substitutions per site. All positions containing gaps and missing data were eliminated. There were a total of 312 positions in the final data set. Evolutionary analyses were conducted in MEGA7 (60).