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Ticks and Tick-borne Diseases
journal homepage: www.elsevier.com/locate/ttbdis
Evaluation of the vector competence of six ixodid tick species for Rangelia
vitalii (Apicomplexa, Piroplasmorida), the agent of canine rangeliosis
João F. Soares
a,1
, Francisco B. Costa
a,2
, Aline Girotto-Soares
b
, Aleksandro S. Da Silva
c
,
Raqueli T. França
d
, Sueli A. Taniwaki
a
, Bruno Dall’Agnol
b
, José Reck
b
, Mitika K. Hagiwara
a
,
Marcelo B. Labruna
a,
⁎
a
Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, São Paulo, SP, Brazil
b
Instituto de Pesquisas Veterinárias Desidério Finamor, Eldorado do Sul, RS, Brazil
c
Universidade do Estado de Santa Catarina, Chapecó, SC, Brazil
d
Universidade de Caxias do Sul, Caxias do Sul, RS, Brazil
ARTICLE INFO
Keywords:
Ixodidae
Amblyomma aureolatum
Amblyomma spp.
Rhipicephalus sanguineus s.l.
Transstadial perpetuation
Transovarial transmission
Canine piroplasmosis
ABSTRACT
Rangelia vitalii is the etiologic agent of canine rangeliosis, a severe piroplasmosis that affects domestic dogs in
Brazil, Uruguay and Argentina. While R. vitalii is one of the most pathogenic tick-borne pathogens for dogs in the
world, its tick vector has remained unknown. The present study evaluated the vector competence of
Rhipicephalus sanguineus sensu lato (both tropical and temperate species), Amblyomma aureolatum, Amblyomma
ovale, Amblyomma tigrinum, and Amblyomma sculptum for R. vitalii. These six tick species were selected for the
study because they comprise the main tick species infesting dogs within the distribution area of canine range-
liosis in South America. Acquisition feeding of the above six tick species was performed on domestic dogs
showing clinical signs of canine rangeliosis, after being experimentally infected through intravenous inoculation
or infestation with R. vitalii-infected ticks. Thereafter, engorged ticks were evaluated for transstadial and
transovarial passages of R. vitalii through molecular analysis after molting or oviposition and egg hatching. The
resultant ticks were evaluated for their competence to transmit R. vitalii to susceptible dogs. Among the six tick
species, only A. aureolatum was able to acquire and perpetuate R. vitalii by transstadial and transovarial passages,
as demonstrated by > 5% infection rates of ticks after hatching or molting. When exposed to transmission
feeding, only A. aureolatum ticks were competent to transmit R. vitalii to dogs, which became severely ill, and the
results confirmed by molecular methods and blood smear examination to have acquired rangeliosis. Results of
the present study, coupled with epidemiological data, indicate that A. aureolatum is a natural vector of R. vitalii.
Our results also indicate that R. vitalii is the first Piroplasmorida agent to be transovarially transmitted in
Amblyomma ticks.
1. Introduction
Rangelia vitalii is the etiologic agent of canine rangeliosis, a severe
piroplasmosis that affects domestic dogs in Brazil, Uruguay and
Argentina (Soares et al., 2011, 2015; Lemos et al., 2012; Eiras et al.,
2014; Lemos et al., 2017; Rivero et al., 2017), in addition to native wild
canids in Brazil (Soares et al., 2014; Fredo et al., 2015; Quadros et al.,
2015; Silveira et al., 2016). For reasons today understood, the disease
was mistakenly confused with other diseases for nearly a century, until
the completion of the first molecular detection and phylogeny of R.
vitalii (Soares et al., 2011). This hemoparasite was described by Pestana
(1910) as Piroplasma vitalii, and then reclassified by Carini and Maciel
(1914) as Rangelia vitalii due to unique phenotypic characters, such as
its ability to parasitize canine leukocytes and vascular endothelium.
Paradoxically, these unique characters, coupled with morphological
similarities between intraerythrocytic forms of R. vitalii and Babesia
vogeli (reported as B. canis), led subsequent authors to doubt the validity
of the taxon R. vitalii. Wenyon (1926) hypothesized that the schizontic
forms found by Carini and Maciel (1914) were actually a Toxoplasma
gondii infection concomitant with a parasitemia by Babesia canis. Three
https://doi.org/10.1016/j.ttbdis.2018.05.004
Received 7 March 2018; Received in revised form 27 April 2018; Accepted 3 May 2018
⁎
Corresponding author at: Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, Av. Prof. Orlando Marques de Paiva 87, Cidade Universitária, São Paulo, SP,
05508-270, Brazil.
1
Present address: Faculdade de Veterinária, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil.
2
Present address: Faculdade de Medicina Veterinária, Universidade Estadual do Maranhão, São Luís, MA, Brazil.
E-mail address: labruna@usp.br (M.B. Labruna).
Ticks and Tick-borne Diseases xxx (xxxx) xxx–xxx
1877-959X/ © 2018 Elsevier GmbH. All rights reserved.
Please cite this article as: Soares, J.F., Ticks and Tick-borne Diseases (2018), https://doi.org/10.1016/j.ttbdis.2018.05.004