Roles of the Maltese Cross Form of Babesia microti in the Development of Parasitemia in B. microti Infection

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Abstract
Studies of parasite infection involving animal hosts other than humans have contributed significantly to our understand- ing of the disease process, including possible pathogenic mech- anisms of parasites and immunological responses of the hosts. In dogs, it was traditionally assumed that the only Babesia species causing disease were Babesia canis and Babesia gibsoni, but recently published reports (1, 5, 7) demonstrate that a different (Babesia microti-like) piroplasm can parasitize dogs. In the first report (7), molecular phylogenetic analysis indi- cated that the infecting agent was in fact more closely related to B. microti, a Holarctic rodent parasite and the cause of human babesiosis in eastern North America, than to other Babesia species. In an extensive series of case studies from Galicia, Spain (1, 5), the agent was also definitively identified by molecular phylogenetic methods as the B. microti-like par- asite. Analysis of the rDNA sequences indicates that the Span- ish isolate is closely related, but not identical, to the reference B. microti strains isolated in Japan and the United States. Whether the parasite should be referred to as a geographical variant of B. microti or a new species (or subspecies) remains unresolved. This newly recognized piroplasm appears to be hyperen- demic in Galicia, northwest Spain, and associated with the tick Ixodes hexagonus (2). B. microti infection in dogs is frequently associated with pathology. Intense regenerative anemia and thrombocytopenia are common findings among infected dogs, many of which also develop serum biochemistry abnormalities compatible with renal disease (3). In the January 2003 issue of Infection and Immunity, Yokoyama et al. (6) published an important paper that gives clues to a possible protective role of the Maltese cross form of the parasite in the course of B. microti infection in mice and in the development of parasitemia. After this interesting work, between October and December 2003, 945 dogs had blood samples submitted for hematological analysis to a diagnostic laboratory located in Vigo, northwest Spain. All the samples were analyzed by bright field micros- copy of Giemsa-stained thin blood smears, and small ring- shaped piroplasms (B. microti like) were detected in 41 of the samples, with parasitemia within 1 to 30%. The identity of the infecting agents was confirmed by PCR sequencing. The results show the following conclusions. (i) The Maltese cross form is often described as character- istic of B. microti, as well as Babesia (Theileria) equi and Thei- leria parva. In the present study, it was also observed among B. microti-like piroplasm-infected dogs (1%). (ii) In splenectomized dogs with the B. microti-like piro- plasm (4), the Maltese cross form represented approximately 2% of the total merozoite forms. In this case, during the acute febrile phase, the main laboratory finding was the presence of multiple intraerythrocytic merozoites of a small piroplasm in Giemsa-stained thin blood smears observed microscopically. The typical features of ring, binary, and tetrad forms were observed.