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Canine babesiosis: A Brazilian perspective
Veterinary Parasitology 141 (2006) 197–203 www.elsevier.com/locate/vetpar
Review
Canine babesiosis: A Brazilian perspective Filipe Dantas-Torres a,*, Luciana Aguiar Figueredo b a
Departamento de Imunologia, Centro de Pesquisas Aggeu Magalha˜es, Fundac¸a˜o Oswaldo Cruz, C.P. 7472, Recife 50670-420, Pernambuco, Brazil b Departamento de Medicina Veterina´ria, Universidade Federal Rural de Pernambuco, Rua Dom Manoel de Medeiros, s/n Dois Irma˜os, Recife 52171-900, Pernambuco, Brazil Received 1 April 2006; received in revised form 19 June 2006; accepted 24 July 2006
Abstract Canine babesiosis is highly endemic in Brazil, caused by Babesia canis and Babesia gibsoni, both transmitted by Rhipicephalus sanguineus ticks. The present review argues for a more adequate method of characterizing the Babesia species infecting dogs and cats in different Brazilian endemic zones. It advocates for a comprehensive understanding of the biology of R. sanguineus ticks under Brazilian conditions in order to define the more effective preventive strategies against canine babesiosis and calls for partnerships between the public and private sectors for research on canine babesiosis and other vector-borne diseases in Brazil. # 2006 Elsevier B.V. All rights reserved. Keywords: Canine babesiosis; Babesia canis vogeli; Babesia gibsoni; Rhipicephalus sanguineus; Brazil
Contents 1. 2. 3. 4. 5. 6. 7. 8.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Geographical distribution, prevalence and risk factors . . . . . . . Etiological agents and tick species involved in the transmission Clinical and laboratory findings . . . . . . . . . . . . . . . . . . . . . . . Diagnosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Treatment and management. . . . . . . . . . . . . . . . . . . . . . . . . . Prevention. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Future research needs and conclusions . . . . . . . . . . . . . . . . . . Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction Canine babesiosis is a life-threatening disease that is caused by intraerythrocytic protozoan parasites of the * Corresponding author. Tel.: +55 81 21012640; fax: +55 81 34532449. E-mail address: [email protected] (F. Dantas-Torres). 0304-4017/$ – see front matter # 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.vetpar.2006.07.030
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genus Babesia. The infection is transmitted by ixodid (hard) ticks of different genera and species. Canine babesiosis is one of the most important tick-borne diseases of dogs worldwide (Boozer and Macintire, 2003; Miyama et al., 2005; Bourdoiseau, 2006; Garcia, 2006; Jacobson, 2006; Kjemtrup and Conrad, 2006). The importance of babesiosis for different animal species has prompted the realization of the first
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International Forum on Babesiosis that took place from 4 to 6 November 2004, in Nice, France. This Forum brought together specialists from many parts of the world. They discussed several aspects of babesiosis in different animal species, particularly dogs. Unfortunately, no emphasis was given to the occurrence of babesiosis in Latin American countries, such as Brazil. Nor was Brazil cited as an area of risk for canine babesiosis (Bourdoiseau, 2006; Garcia, 2006; Jacobson, 2006; Vial and Gorenflot, 2006). Canine babesiosis is a disease of great veterinary importance in Brazil; it is endemic in the whole country and its prevalence is increasing in certain areas (Bastos et al., 2004). Despite this, the disease has been little studied and many aspects of its natural history remains to be further addressed. In the present paper, the state of the art of canine babesiosis in Brazil is reviewed in the light of recent research as well as the authors’ personal experiences.
2. Geographical distribution, prevalence and risk factors Cases of canine babesiosis have been reported in many Brazilian states, such as Rio Grande do Sul (Braccini et al., 1992), Sa˜o Paulo (Dell’Porto et al., 1993), Pernambuco (Dantas-Torres et al., 2004a), Rio de Janeiro (Guimara˜es et al., 2004), Minas Gerais (Bastos et al., 2004), and Parana´ (Trapp et al., 2006). Although canine babesiosis is widely spread in Brazil, the prevalence of Babesia infection in dogs in most of the areas where the disease is endemic is largely unknown. Serological surveys revealed that the prevalence of antibodies to Babesia parasites in dogs varies from 35.7% (Trapp et al., 2006) to 66.9% (Ribeiro et al., 1990). Parasitological investigations showed that the prevalence of Babesia infection ranges from 1.9% (Soares et al., 2006) to 42.0% (Bastos et al., 2004). The
results of parasitological and serological surveys conducted in Brazil are shown in Table 1. Little is known about the possible risk factors for canine babesiosis in Brazil. A hospital population based-study revealed that dogs older than 1 year, living in urban areas and presented with superficial bleeding are more likely to present antibodies to Babesia canis vogeli (Trapp et al., 2006). In the authors’ experience, canine babesiosis has been seen more frequently in dogs older than 2 years, though young dogs with a recent history of visiting a beach and first exposure to ticks have also been seen affected by the disease. No significant gender or breed predilections have been observed (Ribeiro et al., 1990; Guimara˜es et al., 2002; Bastos et al., 2004; Trapp et al., 2006). 3. Etiological agents and tick species involved in the transmission Most of the cases of canine babesiosis have been attributed to B. canis sensu lato. However, antibodies to Babesia gibsoni have been detected in a dog with a history of traveling to Brazil (Gothe and Wegerdt, 1991). In fact, B. gibsoni was implicated in some cases of canine babesiosis in Rio Grande do Sul (Braccini et al., 1992), Sa˜o Paulo (Lucidi et al., 2004) and Parana´ (Trapp et al., in press). An experimental model of canine babesiosis previously suggested that the B. canis vogeli is the causal agent of the disease, at least in Minas Gerais (Bicalho et al., 2002). More recently, infection by B. canis vogeli in dogs has been confirmed for the first time not only in Brazil, but also in South America (Passos et al., 2005). The 18S rDNA gene sequence of the Brazilian strains of B. canis vogeli has been established as being very similar to those from Egypt, Spain, France, Japan, Australia and South Africa. Perhaps, B. canis vogeli was introduced in Brazil concomitantly
Table 1 Results of parasitological and serological surveys conducted in Brazil Reference
Region
Sample size
Method of investigation
Prevalence (%)
Soares et al. (2006) Trapp et al. (2006) Bastos et al. (2004) Rodrigues et al. (2002) O’Dwyer et al. (2001) Dell’Porto et al. (1993)
Minas Gerais State Parana´ State Minas Gerais State Minas Gerais State Rural areas of Rio de Janeiro State Sa˜o Paulo State
51 381 145 104 250 106
Ribeiro et al. (1990)
Minas Gerais State
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Stained IFATa Stained Stained Stained IFAT Stained IFAT
1 136 61 28 13 45 11 85
a
Indirect fluorescent antibody test.
blood smears blood smears blood smears blood smears blood smears
(1.9%) (35.7%) (42.0%) (26.9%) (5.2%) (42.4%) (10.3%) (66.9%)
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observed that R. sanguineus ticks are more abundant during the dry season with the incidence of canine babesiosis increasing slightly during this period, as has also been observed in Minas Gerais (Guimara˜es et al., 2002).
with the introduction of Rhipicephalus sanguineus ticks from the Afrotropical region during the European colonization. In Brazil, up to the beginning of the past century, the area of occurrence of R. sanguineus was very restricted (Araga˜o, 1911). Nowadays, this tick can be found in the whole country (Araga˜o and Fonseca, 1961). There has been recent evidence of the presence of Babesia-like inclusions in Brazilian cats (Gazeta et al., 2004; Mendes-de-Almeida et al., 2005). We have found Babesia-like inclusions in a cat from Pernambuco, with no previous history of tick exposure. We observed small, pleomorphic intraerythrocytic inclusions that appeared as bipolar ‘‘safety pins’’ or round ‘‘dots’’. These inclusions are similar to those described by Gazeta et al. (2004). It is interesting to note that there are few reports regarding tick infestations in Brazilian cats (Araga˜o, 1911; Araga˜o and Fonseca, 1961), which appears to be a rare event in our area. Further molecular studies are needed to determine the taxonomic position of the piroplasms of Brazilian cats. Babesia parasites are transmitted to a susceptible dog through the saliva of an infected tick while it is feeding (Fig. 1). In 1936, it was demonstrated that R. sanguineus ticks were able to transmit B. canis vogeli from a naturally infected dog to an uninfected one (Regendanz and Muniz, 1936). R. sanguineus, which is also a major vector of B. gibsoni, is the most common ixodid tick in Brazil (Araga˜o and Fonseca, 1961; Labruna and Pereira, 2001; Dantas-Torres et al., 2004b) and it is invariably present in areas where canine babesiosis is endemic. In certain areas, R. sanguineus is the sole tick species known to parasitize dogs (Dantas-Torres et al., 2004b) and cases of human parasitism by this tick have also been reported (Dantas-Torres et al., 2006). In Pernambuco, we have
The clinical picture presented by Brazilian dogs suffering from babesiosis is diverse, though most of the dogs display apathy (Fig. 2), anemia, fever, anorexia (Guimara˜es et al., 2002; Bastos et al., 2004), and pale mucous membranes (Guimara˜es et al., 2004). Although hemorrhage has been previously reported as a clinical sign of canine babesiosis (Guimara˜es et al., 2002, 2004), the possibility of coinfection with Ehrlichia canis should be considered if hemorrhage is present. Dehydration, loss of weight (also shown in Fig. 2), abdominal pain, and kidney sensitivity to palpation may also be observed (Bastos et al., 2004). In a study conducted with 500 dogs from Rio de Janeiro, the most common laboratory findings in those with proven Babesia infection were: normocytic– hypochromic anemia, polychromasia, anisocytosis, neutrophil leukocytosis, monocytosis, lymphopenia, and thrombopenia (Guimara˜es et al., 2004). Hemograms available to us in our private diagnosis laboratory have typically revealed regenerative hemolytic anemia, decreased packed cell volume, and thrombopenia. The severity of the anemia may vary widely. In some cases, the erythrocyte cell count is markedly decreased and values may be as low as 1.7 106/mm3. The leukocyte count might be increased or decreased, as observed elsewhere (Hagiwara and Holzchuh, 1987; Dell’Porto et al., 1993).
Fig. 1. A female cocker Spaniel dog highly infested by R. sanguineus ticks.
Fig. 2. A female German sheep dog suffering from babesiosis with severe loss of weight and prostration.
4. Clinical and laboratory findings
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5. Diagnosis The diagnosis of canine babesiosis is often based on physical examination and patient history. But whenever possible, the microscopic examination of stained peripheral blood smears has been carried out to confirm the infection (Guimara˜es et al., 2002). During the parasitaemia, intraerythrocytic inclusions of Babesia are easily found in stained peripheral blood smears, especially in febrile dogs (Guimara˜es et al., 2004). This method is the most widely used in the veterinary medicine daily routine due to its many advantages, such as simplicity, high specificity and low cost. Sometimes, particularly in chronic or sub clinical cases (Dell’Porto et al., 1993), the parasitological confirmation of the infection is not readily achieved. Serological tests are useful to identify asymptomatic carrier dogs and to diagnose chronic infections, in which the level of parasitaemia might be low and not detectable in stained peripheral blood smears. It is important to note, however, that even after chemosterilization dogs may remain seropositive for long periods. Thus, the diagnostic value of serological tests is poor in the absence of clinical signs and patient’s data. The indirect fluorescent antibody test (IFAT) and the enzyme-linked immunosorbent assay (ELISA) are considered to be highly sensitive and moderately specific tools for detection of antibodies to Babesia parasites in dogs (Dell’Porto et al., 1993; Yamane et al., 1993; Furuta et al., 2004). However, the sensitivity, specificity, and predictive values of these methods have not been previously stated. Molecular-based methods, particularly the polymerase chain reaction (PCR), are promising tools for diagnosis of many parasitic diseases (Gasser, 2006). PCR has been shown to be a useful tool for detection of Babesia DNA in canine blood samples (Birkenheuer et al., 2003; Inokuma et al., 2005), with specificity and sensitivity of 100% as determined in a cohort of 55 dogs (Martin et al., 2006). The disadvantages of PCR are the requirement for specialized laboratory equipment and well-trained laboratory personnel. In Brazil, the PCR is currently restricted to research (Passos et al., 2005; Trapp et al., in press) and its utility for the diagnosis of Babesia infection in Brazilian dogs should be further evaluated. 6. Treatment and management Diminazene diaceturate and imidocarb dipropionate are the drugs of choice for treatment of canine babesiosis in Brazil. A single injection of diminazene
diaceturate at 2.5–3.5 mg/kg given subcutaneously or intramuscularly is reputed to be effective; in B. gibsoni infections an additional injection after 24 h may be required (Branda˜o and Hagiwara, 2002). Undesirable effects of this drug include depression, ataxia and convulsion. Two injections of imidocarb dipropionate at 5–7 mg/kg given subcutaneously or intramuscularly at an interval of 2 weeks are effective (Branda˜o and Hagiwara, 2002). Undesirable effects of imidocarb include painful injection, vomiting, colic, diarrhea, and ptyalismis. The administration of atropine at 0.04 mg/ kg, 10 min before application of imidocarb can prevent adverse cholinergic effects. The exact mode of action of current babesiacides is uncertain. The diminazene diaceturate appears to interfere with aerobic glycolysis and synthesis of DNA in the parasite. The imidocarb interferes with the production and/or utilization of polyamines, or prevention of entry of inositol into infected erythrocytes (Branda˜o and Hagiwara, 2002; Vial and Gorenflot, 2006). A study of the pharmacokinetics of imidocarb showed that the plasma half-life was 207 min and 80% was eliminated in 8 h in dogs given an intravenous bolus (Abdullah and Baggot, 1983). It seems to be eliminated through the urine and faeces. The highest concentrations of residues were found in liver and in kidney. Suspicious cases of canine babesiosis with a history of recent tick exposure should be treated, even in the absence of a parasitological confirmation. Depending on the severity of the illness, supportive therapy such as intravenous fluids and blood transfusion may be required (Guimara˜es et al., 2002). The decision to transfuse should always be based on clinical signs and hematological testing. The presence of clinical signs such as tachycardia, tachypnea, water-hammer pulse, weakness and collapse may indicate the need for blood transfusion. Transfusion should also be considered if the hematocrit is 15% and always be performed when it is 10%. In certain cases, the use of prednisolone at 1–2 mg/ kg/day for up to 1 week may benefit to inhibit immunopathological phenomena inducing or accentuating glomerulonephritis (Bourdoiseau, 2006). 7. Prevention As expected for a tick-borne disease, the prevention of canine babesiosis is not an easy task. In contrast to what occurs in France (Bourdoiseau, 2006), there is no vaccine against canine babesiosis available in Brazil and thus all attempts to prevent this disease have concentrated on avoiding tick infestations (Branda˜o and
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Hagiwara, 2002; Vidotto and Trapp, 2004). The Brazilian climate is perfect for R. sanguineus ticks, facilitating the development of up to four generations per year. Thus, owners should be instructed to keep their dogs free of ticks by means of regular tick removal and acaricide treatment. The control of ticks is generally carried out by the use of acaricides (spot-on, pour-on or spray-on) on dogs and in the environment. Fipronil and amitraz are among the active ingredients most used (Labruna and Pereira, 2001). Regular physical inspections should also be conducted to remove all attached ticks. In areas where tick-borne diseases such as Rocky Mountain spotted fever are endemic, special care must be taken when removing a tick from the dog’s skin. As there is risk of Rickettsia rickettsii infection by contact with crushed tick’s tissues and fluids, proper tick removal procedures (e.g., use of gloves) must be adopted (Gammons and Salam, 2002). In Pernambuco State, we have noted that from December to February (holidays for some) many pet dogs go to the beach with their owners and return to the city infested by ticks. A significant number of these dogs will suffer from babesiosis in a short period of time, especially the young ones that have never been exposed to tick bites. Chemoprophylaxis, which consists of the use of acaricides associated to an intramuscular injection of imidocarb at high dosage, may be useful to prevent these cases. Imidocarb at 4–6 mg/kg protects dogs from B. canis infection for 2–6 weeks (Vercammen et al., 1996a; Bourdoiseau, 2006). Doxycycline at 20 mm/kg (10 mg/ kg BID), during 11 consecutive days, is reputed to be effective in preventing clinical disease, but not infection (Vercammen et al., 1996b). As Babesia parasites can be transmitted through blood transfusion (Freeman et al., 1994), it is important that donors are free of infection. The education of dog owners is also essential. They must be aware about their role in maintaining their dogs free of ticks without an indiscriminate use of acaricides in the environment. The indiscriminate use of acaricides may cause serious undesirable effects, such as environmental pollution and development of acaricide resistance in the ticks. 8. Future research needs and conclusions The identification of the causal agent involved in each case of canine babesiosis is important to define treatment planning and prognosis (Boozer and Macintire, 2003). Further studies aiming to identify all representative species of Babesia infecting dogs (and
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also cats) in different Brazilian regions are needed. These studies should be based on a combination of morphological and molecular methods. Case-control studies should be helpful to identify risk factors associated with Babesia infection and outcome of canine babesiosis. There appears to be an increasing risk of acquiring the infection during the dry season in certain areas (e.g., Pernambuco). This hypothesis should be investigated more fully. It is known that a comprehensive understanding of vector biology and ecology is important to define and implement appropriate prevention and control strategies. The biology of R. sanguineus ticks under Brazilian conditions should be addressed in future research. Diagnostic tools other than the parasitological examination should be encouraged to be used in Brazil. The IFATand the ELISA methods should be standardized and included in the diagnosis routine. In this perspective, the sensitivity, specificity, positive and negative predictive values of both methods should be assessed. Canine babesiosis has been little studied in Brazil, owing to the low investment in clinical veterinary research, which has impeded the development of further molecular and field investigations. Public–private partnerships should be encouraged to support future research on canine babesiosis and other vector-borne diseases in Brazil. Acknowledgements The authors dedicate this review to Professor Maria Aparecida da Gloria Faustino in recognition of her outstanding contributions to teaching and research in veterinary parasitology in Brazil. Thanks to Sidney Pratt for English revision and also to the anonymous referees of Veterinary Parasitology for their helpful comments on a draft of this manuscript. The first author is receiving a scholarship from the National Council of Technological and Scientific Development (CNPq). References Abdullah, A.S., Baggot, J.D., 1983. Pharmacokinetics of imidocarb in normal dogs and goats. J. Vet. Pharmacol. Ther. 6, 195–199. Araga˜o, H., 1911. Notas sobre ixo´didas brazileiros. Mem. Inst. Oswaldo Cruz 3, 145–195. Araga˜o, H., Fonseca, F., 1961. Notas de ixodologia VIII Lista e chave para representantes da fauna ixodolo´gica brasileira. Mem. Inst. Oswaldo Cruz 59, 115–129. Bastos, C.V., Moreira, S.M., Passos, L.M., 2004. Retrospective study (1998–2001) on canine babesiosis in Belo Horizonte, Minas Gerais, Brazil. Ann. N. Y. Acad. Sci. 1026, 158–160.
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Inokuma, H., Okuda, M., Yoshizaki, Y., Hiraoka, H., Miyama, T., Itamoto, K., Une, S., Nakaichi, M., Taura, Y., 2005. Clinical observations of Babesia gibsoni infection with low parasitaemia confirmed by PCR in dogs. Vet Rec. 156, 116–118. Jacobson, L.S., 2006. The South African form of severe and complicated canine babesiosis: clinical advances 1994–2004. Vet. Parasitol. 138, 126–139. Kjemtrup, A.M., Conrad, P.A., 2006. A review of the small canine piroplasms from California: Babesia conradae in the literature. Vet. Parasitol. 138, 112–117. Labruna, M., Pereira, M.C., 2001. Carrapatos em ca˜es no Brasil. Clin. Vet. 11, 24–32. Lucidi, C.A., Angerami, J.T.S., Rodrigues, R.R., Takahira, R.K., 2004. Primeira ocorreˆncia de Babesia gibsoni no Estado de Sa˜o Paulo: nota preliminar. Rev. Bras. Parasitol. Vet. 13 (Suppl. 1), 231. Martin, A.R., Dunstan, R.H., Roberts, T.K., Brown, G.K., 2006. Babesia canis vogeli: a novel PCR for its detection in dogs in Australia. Exp. Parasitol. 112, 63–65. Mendes-de-Almeida, F., Faria, M.C., Branco, A.S., Serrao, M.L., Souza, A.M., Almosny, N., Charme, M., Labarthe, N., 2005. Sanitary conditions of a colony of urban feral cats (Felis catus Linnaeus, 1758) in a zoological garden of Rio de Janeiro, Brazil. Rev. Inst. Med. Trop. Sao Paulo 46, 269–274. Miyama, T., Sakata, Y., Shimada, Y., Ogino, S., Watanabe, M., Itamoto, K., Okuda, M., Verdida, R.A., Xuan, X., Nagasawa, H., Inokuma, H., 2005. Epidemiological survey of Babesia gibsoni infection in dogs in eastern Japan. J. Vet. Med. Sci. 67, 467–471. O’Dwyer, L.H., Massard, C.L., de Souza, J.C.P., 2001. Hepatozoon canis infection associated with dog ticks of rural areas of Rio de Janeiro State, Brazil. Vet. Parasitol. 94, 143–150. Passos, L.M., Geiger, S.M., Ribeiro, M.F., Pfister, K., Zahler-Rinder, M., 2005. First molecular detection of Babesia vogeli in dogs from Brazil. Vet. Parasitol. 127, 81–85. Regendanz, P., Muniz, J., 1936. O Rhipicephalus sanguineus como transmissor da piroplasmose canina no Brasil. Mem. Inst. Oswaldo Cruz 31, 81–84. Ribeiro, M.F.B., Lima, J.D., Passos, L.M.F., Guimara˜es, A.M., 1990. Frequ¨eˆncia de anticorpos fluorescentes anti-Babesia canis em ca˜es de Belo Horizonte, Minas Gerais. Arq. Bras. Med. Vet. Zootec. 42, 511–517. Rodrigues, A.F.S.F., D’Agosto, M., Daemon, E., 2002. Babesia canis (Piana & Galli-Valerio, 1895) (Apicomplexa: Babesiidae) em ca˜es de rua do Municı´pio de Juiz de Fora, MG. Rev. Bras. Med. Vet. 24, 17–21. Soares, A.O., Souza, A.D., Feliciano, E.A., Rodrigues, A.F., D’agosto, M., Daemon, E., 2006. Avaliac¸a˜o ectoparasitolo´gica e hemoparasitolo´gica em ca˜es criados em apartamentos e casas com quintal na cidade de Juiz de Fora, MG. Rev. Bras. Parasitol. Vet. 15, 13–16. Trapp, S.M., Dagnone, A.S., Vidotto, O., Freire, R.L., Amude, A.M., Morais, H.S., 2006. Seroepidemiology of canine babesiosis and ehrlichiosis in a hospital population. Vet. Parasitol. 140, 223–230. Trapp, S.M., Messick, J.B., Vidotto, O., Jojima, F.S., Morais, H.S., in press. Babesia gibsoni genotype Asia in dogs from Brazil. Vet. Parasitol. Vercammen, F., De Deken, R., Maes, L., 1996a. Prophylactic activity of imidocarb against experimental infection with Babesia canis. Vet. Parasitol. 63, 195–198. Vercammen, F., De Deken, R., Maes, L., 1996b. Prophylactic treatment of experimental canine babesiosis (Babesia canis) with doxycycline. Vet. Parasitol. 66, 251–255.
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Review
Canine babesiosis: A Brazilian perspective Filipe Dantas-Torres a,*, Luciana Aguiar Figueredo b a
Departamento de Imunologia, Centro de Pesquisas Aggeu Magalha˜es, Fundac¸a˜o Oswaldo Cruz, C.P. 7472, Recife 50670-420, Pernambuco, Brazil b Departamento de Medicina Veterina´ria, Universidade Federal Rural de Pernambuco, Rua Dom Manoel de Medeiros, s/n Dois Irma˜os, Recife 52171-900, Pernambuco, Brazil Received 1 April 2006; received in revised form 19 June 2006; accepted 24 July 2006
Abstract Canine babesiosis is highly endemic in Brazil, caused by Babesia canis and Babesia gibsoni, both transmitted by Rhipicephalus sanguineus ticks. The present review argues for a more adequate method of characterizing the Babesia species infecting dogs and cats in different Brazilian endemic zones. It advocates for a comprehensive understanding of the biology of R. sanguineus ticks under Brazilian conditions in order to define the more effective preventive strategies against canine babesiosis and calls for partnerships between the public and private sectors for research on canine babesiosis and other vector-borne diseases in Brazil. # 2006 Elsevier B.V. All rights reserved. Keywords: Canine babesiosis; Babesia canis vogeli; Babesia gibsoni; Rhipicephalus sanguineus; Brazil
Contents 1. 2. 3. 4. 5. 6. 7. 8.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Geographical distribution, prevalence and risk factors . . . . . . . Etiological agents and tick species involved in the transmission Clinical and laboratory findings . . . . . . . . . . . . . . . . . . . . . . . Diagnosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Treatment and management. . . . . . . . . . . . . . . . . . . . . . . . . . Prevention. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Future research needs and conclusions . . . . . . . . . . . . . . . . . . Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction Canine babesiosis is a life-threatening disease that is caused by intraerythrocytic protozoan parasites of the * Corresponding author. Tel.: +55 81 21012640; fax: +55 81 34532449. E-mail address: [email protected] (F. Dantas-Torres). 0304-4017/$ – see front matter # 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.vetpar.2006.07.030
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genus Babesia. The infection is transmitted by ixodid (hard) ticks of different genera and species. Canine babesiosis is one of the most important tick-borne diseases of dogs worldwide (Boozer and Macintire, 2003; Miyama et al., 2005; Bourdoiseau, 2006; Garcia, 2006; Jacobson, 2006; Kjemtrup and Conrad, 2006). The importance of babesiosis for different animal species has prompted the realization of the first
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International Forum on Babesiosis that took place from 4 to 6 November 2004, in Nice, France. This Forum brought together specialists from many parts of the world. They discussed several aspects of babesiosis in different animal species, particularly dogs. Unfortunately, no emphasis was given to the occurrence of babesiosis in Latin American countries, such as Brazil. Nor was Brazil cited as an area of risk for canine babesiosis (Bourdoiseau, 2006; Garcia, 2006; Jacobson, 2006; Vial and Gorenflot, 2006). Canine babesiosis is a disease of great veterinary importance in Brazil; it is endemic in the whole country and its prevalence is increasing in certain areas (Bastos et al., 2004). Despite this, the disease has been little studied and many aspects of its natural history remains to be further addressed. In the present paper, the state of the art of canine babesiosis in Brazil is reviewed in the light of recent research as well as the authors’ personal experiences.
2. Geographical distribution, prevalence and risk factors Cases of canine babesiosis have been reported in many Brazilian states, such as Rio Grande do Sul (Braccini et al., 1992), Sa˜o Paulo (Dell’Porto et al., 1993), Pernambuco (Dantas-Torres et al., 2004a), Rio de Janeiro (Guimara˜es et al., 2004), Minas Gerais (Bastos et al., 2004), and Parana´ (Trapp et al., 2006). Although canine babesiosis is widely spread in Brazil, the prevalence of Babesia infection in dogs in most of the areas where the disease is endemic is largely unknown. Serological surveys revealed that the prevalence of antibodies to Babesia parasites in dogs varies from 35.7% (Trapp et al., 2006) to 66.9% (Ribeiro et al., 1990). Parasitological investigations showed that the prevalence of Babesia infection ranges from 1.9% (Soares et al., 2006) to 42.0% (Bastos et al., 2004). The
results of parasitological and serological surveys conducted in Brazil are shown in Table 1. Little is known about the possible risk factors for canine babesiosis in Brazil. A hospital population based-study revealed that dogs older than 1 year, living in urban areas and presented with superficial bleeding are more likely to present antibodies to Babesia canis vogeli (Trapp et al., 2006). In the authors’ experience, canine babesiosis has been seen more frequently in dogs older than 2 years, though young dogs with a recent history of visiting a beach and first exposure to ticks have also been seen affected by the disease. No significant gender or breed predilections have been observed (Ribeiro et al., 1990; Guimara˜es et al., 2002; Bastos et al., 2004; Trapp et al., 2006). 3. Etiological agents and tick species involved in the transmission Most of the cases of canine babesiosis have been attributed to B. canis sensu lato. However, antibodies to Babesia gibsoni have been detected in a dog with a history of traveling to Brazil (Gothe and Wegerdt, 1991). In fact, B. gibsoni was implicated in some cases of canine babesiosis in Rio Grande do Sul (Braccini et al., 1992), Sa˜o Paulo (Lucidi et al., 2004) and Parana´ (Trapp et al., in press). An experimental model of canine babesiosis previously suggested that the B. canis vogeli is the causal agent of the disease, at least in Minas Gerais (Bicalho et al., 2002). More recently, infection by B. canis vogeli in dogs has been confirmed for the first time not only in Brazil, but also in South America (Passos et al., 2005). The 18S rDNA gene sequence of the Brazilian strains of B. canis vogeli has been established as being very similar to those from Egypt, Spain, France, Japan, Australia and South Africa. Perhaps, B. canis vogeli was introduced in Brazil concomitantly
Table 1 Results of parasitological and serological surveys conducted in Brazil Reference
Region
Sample size
Method of investigation
Prevalence (%)
Soares et al. (2006) Trapp et al. (2006) Bastos et al. (2004) Rodrigues et al. (2002) O’Dwyer et al. (2001) Dell’Porto et al. (1993)
Minas Gerais State Parana´ State Minas Gerais State Minas Gerais State Rural areas of Rio de Janeiro State Sa˜o Paulo State
51 381 145 104 250 106
Ribeiro et al. (1990)
Minas Gerais State
127
Stained IFATa Stained Stained Stained IFAT Stained IFAT
1 136 61 28 13 45 11 85
a
Indirect fluorescent antibody test.
blood smears blood smears blood smears blood smears blood smears
(1.9%) (35.7%) (42.0%) (26.9%) (5.2%) (42.4%) (10.3%) (66.9%)
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observed that R. sanguineus ticks are more abundant during the dry season with the incidence of canine babesiosis increasing slightly during this period, as has also been observed in Minas Gerais (Guimara˜es et al., 2002).
with the introduction of Rhipicephalus sanguineus ticks from the Afrotropical region during the European colonization. In Brazil, up to the beginning of the past century, the area of occurrence of R. sanguineus was very restricted (Araga˜o, 1911). Nowadays, this tick can be found in the whole country (Araga˜o and Fonseca, 1961). There has been recent evidence of the presence of Babesia-like inclusions in Brazilian cats (Gazeta et al., 2004; Mendes-de-Almeida et al., 2005). We have found Babesia-like inclusions in a cat from Pernambuco, with no previous history of tick exposure. We observed small, pleomorphic intraerythrocytic inclusions that appeared as bipolar ‘‘safety pins’’ or round ‘‘dots’’. These inclusions are similar to those described by Gazeta et al. (2004). It is interesting to note that there are few reports regarding tick infestations in Brazilian cats (Araga˜o, 1911; Araga˜o and Fonseca, 1961), which appears to be a rare event in our area. Further molecular studies are needed to determine the taxonomic position of the piroplasms of Brazilian cats. Babesia parasites are transmitted to a susceptible dog through the saliva of an infected tick while it is feeding (Fig. 1). In 1936, it was demonstrated that R. sanguineus ticks were able to transmit B. canis vogeli from a naturally infected dog to an uninfected one (Regendanz and Muniz, 1936). R. sanguineus, which is also a major vector of B. gibsoni, is the most common ixodid tick in Brazil (Araga˜o and Fonseca, 1961; Labruna and Pereira, 2001; Dantas-Torres et al., 2004b) and it is invariably present in areas where canine babesiosis is endemic. In certain areas, R. sanguineus is the sole tick species known to parasitize dogs (Dantas-Torres et al., 2004b) and cases of human parasitism by this tick have also been reported (Dantas-Torres et al., 2006). In Pernambuco, we have
The clinical picture presented by Brazilian dogs suffering from babesiosis is diverse, though most of the dogs display apathy (Fig. 2), anemia, fever, anorexia (Guimara˜es et al., 2002; Bastos et al., 2004), and pale mucous membranes (Guimara˜es et al., 2004). Although hemorrhage has been previously reported as a clinical sign of canine babesiosis (Guimara˜es et al., 2002, 2004), the possibility of coinfection with Ehrlichia canis should be considered if hemorrhage is present. Dehydration, loss of weight (also shown in Fig. 2), abdominal pain, and kidney sensitivity to palpation may also be observed (Bastos et al., 2004). In a study conducted with 500 dogs from Rio de Janeiro, the most common laboratory findings in those with proven Babesia infection were: normocytic– hypochromic anemia, polychromasia, anisocytosis, neutrophil leukocytosis, monocytosis, lymphopenia, and thrombopenia (Guimara˜es et al., 2004). Hemograms available to us in our private diagnosis laboratory have typically revealed regenerative hemolytic anemia, decreased packed cell volume, and thrombopenia. The severity of the anemia may vary widely. In some cases, the erythrocyte cell count is markedly decreased and values may be as low as 1.7 106/mm3. The leukocyte count might be increased or decreased, as observed elsewhere (Hagiwara and Holzchuh, 1987; Dell’Porto et al., 1993).
Fig. 1. A female cocker Spaniel dog highly infested by R. sanguineus ticks.
Fig. 2. A female German sheep dog suffering from babesiosis with severe loss of weight and prostration.
4. Clinical and laboratory findings
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5. Diagnosis The diagnosis of canine babesiosis is often based on physical examination and patient history. But whenever possible, the microscopic examination of stained peripheral blood smears has been carried out to confirm the infection (Guimara˜es et al., 2002). During the parasitaemia, intraerythrocytic inclusions of Babesia are easily found in stained peripheral blood smears, especially in febrile dogs (Guimara˜es et al., 2004). This method is the most widely used in the veterinary medicine daily routine due to its many advantages, such as simplicity, high specificity and low cost. Sometimes, particularly in chronic or sub clinical cases (Dell’Porto et al., 1993), the parasitological confirmation of the infection is not readily achieved. Serological tests are useful to identify asymptomatic carrier dogs and to diagnose chronic infections, in which the level of parasitaemia might be low and not detectable in stained peripheral blood smears. It is important to note, however, that even after chemosterilization dogs may remain seropositive for long periods. Thus, the diagnostic value of serological tests is poor in the absence of clinical signs and patient’s data. The indirect fluorescent antibody test (IFAT) and the enzyme-linked immunosorbent assay (ELISA) are considered to be highly sensitive and moderately specific tools for detection of antibodies to Babesia parasites in dogs (Dell’Porto et al., 1993; Yamane et al., 1993; Furuta et al., 2004). However, the sensitivity, specificity, and predictive values of these methods have not been previously stated. Molecular-based methods, particularly the polymerase chain reaction (PCR), are promising tools for diagnosis of many parasitic diseases (Gasser, 2006). PCR has been shown to be a useful tool for detection of Babesia DNA in canine blood samples (Birkenheuer et al., 2003; Inokuma et al., 2005), with specificity and sensitivity of 100% as determined in a cohort of 55 dogs (Martin et al., 2006). The disadvantages of PCR are the requirement for specialized laboratory equipment and well-trained laboratory personnel. In Brazil, the PCR is currently restricted to research (Passos et al., 2005; Trapp et al., in press) and its utility for the diagnosis of Babesia infection in Brazilian dogs should be further evaluated. 6. Treatment and management Diminazene diaceturate and imidocarb dipropionate are the drugs of choice for treatment of canine babesiosis in Brazil. A single injection of diminazene
diaceturate at 2.5–3.5 mg/kg given subcutaneously or intramuscularly is reputed to be effective; in B. gibsoni infections an additional injection after 24 h may be required (Branda˜o and Hagiwara, 2002). Undesirable effects of this drug include depression, ataxia and convulsion. Two injections of imidocarb dipropionate at 5–7 mg/kg given subcutaneously or intramuscularly at an interval of 2 weeks are effective (Branda˜o and Hagiwara, 2002). Undesirable effects of imidocarb include painful injection, vomiting, colic, diarrhea, and ptyalismis. The administration of atropine at 0.04 mg/ kg, 10 min before application of imidocarb can prevent adverse cholinergic effects. The exact mode of action of current babesiacides is uncertain. The diminazene diaceturate appears to interfere with aerobic glycolysis and synthesis of DNA in the parasite. The imidocarb interferes with the production and/or utilization of polyamines, or prevention of entry of inositol into infected erythrocytes (Branda˜o and Hagiwara, 2002; Vial and Gorenflot, 2006). A study of the pharmacokinetics of imidocarb showed that the plasma half-life was 207 min and 80% was eliminated in 8 h in dogs given an intravenous bolus (Abdullah and Baggot, 1983). It seems to be eliminated through the urine and faeces. The highest concentrations of residues were found in liver and in kidney. Suspicious cases of canine babesiosis with a history of recent tick exposure should be treated, even in the absence of a parasitological confirmation. Depending on the severity of the illness, supportive therapy such as intravenous fluids and blood transfusion may be required (Guimara˜es et al., 2002). The decision to transfuse should always be based on clinical signs and hematological testing. The presence of clinical signs such as tachycardia, tachypnea, water-hammer pulse, weakness and collapse may indicate the need for blood transfusion. Transfusion should also be considered if the hematocrit is 15% and always be performed when it is 10%. In certain cases, the use of prednisolone at 1–2 mg/ kg/day for up to 1 week may benefit to inhibit immunopathological phenomena inducing or accentuating glomerulonephritis (Bourdoiseau, 2006). 7. Prevention As expected for a tick-borne disease, the prevention of canine babesiosis is not an easy task. In contrast to what occurs in France (Bourdoiseau, 2006), there is no vaccine against canine babesiosis available in Brazil and thus all attempts to prevent this disease have concentrated on avoiding tick infestations (Branda˜o and
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Hagiwara, 2002; Vidotto and Trapp, 2004). The Brazilian climate is perfect for R. sanguineus ticks, facilitating the development of up to four generations per year. Thus, owners should be instructed to keep their dogs free of ticks by means of regular tick removal and acaricide treatment. The control of ticks is generally carried out by the use of acaricides (spot-on, pour-on or spray-on) on dogs and in the environment. Fipronil and amitraz are among the active ingredients most used (Labruna and Pereira, 2001). Regular physical inspections should also be conducted to remove all attached ticks. In areas where tick-borne diseases such as Rocky Mountain spotted fever are endemic, special care must be taken when removing a tick from the dog’s skin. As there is risk of Rickettsia rickettsii infection by contact with crushed tick’s tissues and fluids, proper tick removal procedures (e.g., use of gloves) must be adopted (Gammons and Salam, 2002). In Pernambuco State, we have noted that from December to February (holidays for some) many pet dogs go to the beach with their owners and return to the city infested by ticks. A significant number of these dogs will suffer from babesiosis in a short period of time, especially the young ones that have never been exposed to tick bites. Chemoprophylaxis, which consists of the use of acaricides associated to an intramuscular injection of imidocarb at high dosage, may be useful to prevent these cases. Imidocarb at 4–6 mg/kg protects dogs from B. canis infection for 2–6 weeks (Vercammen et al., 1996a; Bourdoiseau, 2006). Doxycycline at 20 mm/kg (10 mg/ kg BID), during 11 consecutive days, is reputed to be effective in preventing clinical disease, but not infection (Vercammen et al., 1996b). As Babesia parasites can be transmitted through blood transfusion (Freeman et al., 1994), it is important that donors are free of infection. The education of dog owners is also essential. They must be aware about their role in maintaining their dogs free of ticks without an indiscriminate use of acaricides in the environment. The indiscriminate use of acaricides may cause serious undesirable effects, such as environmental pollution and development of acaricide resistance in the ticks. 8. Future research needs and conclusions The identification of the causal agent involved in each case of canine babesiosis is important to define treatment planning and prognosis (Boozer and Macintire, 2003). Further studies aiming to identify all representative species of Babesia infecting dogs (and
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also cats) in different Brazilian regions are needed. These studies should be based on a combination of morphological and molecular methods. Case-control studies should be helpful to identify risk factors associated with Babesia infection and outcome of canine babesiosis. There appears to be an increasing risk of acquiring the infection during the dry season in certain areas (e.g., Pernambuco). This hypothesis should be investigated more fully. It is known that a comprehensive understanding of vector biology and ecology is important to define and implement appropriate prevention and control strategies. The biology of R. sanguineus ticks under Brazilian conditions should be addressed in future research. Diagnostic tools other than the parasitological examination should be encouraged to be used in Brazil. The IFATand the ELISA methods should be standardized and included in the diagnosis routine. In this perspective, the sensitivity, specificity, positive and negative predictive values of both methods should be assessed. Canine babesiosis has been little studied in Brazil, owing to the low investment in clinical veterinary research, which has impeded the development of further molecular and field investigations. Public–private partnerships should be encouraged to support future research on canine babesiosis and other vector-borne diseases in Brazil. Acknowledgements The authors dedicate this review to Professor Maria Aparecida da Gloria Faustino in recognition of her outstanding contributions to teaching and research in veterinary parasitology in Brazil. Thanks to Sidney Pratt for English revision and also to the anonymous referees of Veterinary Parasitology for their helpful comments on a draft of this manuscript. The first author is receiving a scholarship from the National Council of Technological and Scientific Development (CNPq). References Abdullah, A.S., Baggot, J.D., 1983. Pharmacokinetics of imidocarb in normal dogs and goats. J. Vet. Pharmacol. Ther. 6, 195–199. Araga˜o, H., 1911. Notas sobre ixo´didas brazileiros. Mem. Inst. Oswaldo Cruz 3, 145–195. Araga˜o, H., Fonseca, F., 1961. Notas de ixodologia VIII Lista e chave para representantes da fauna ixodolo´gica brasileira. Mem. Inst. Oswaldo Cruz 59, 115–129. Bastos, C.V., Moreira, S.M., Passos, L.M., 2004. Retrospective study (1998–2001) on canine babesiosis in Belo Horizonte, Minas Gerais, Brazil. Ann. N. Y. Acad. Sci. 1026, 158–160.
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