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Evaluation of Miltefosine for the Treatment of Dogs Naturally Infected

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Evaluation of Miltefosine for the Treatment of Dogs Naturally Infected Veterinary Parasitology 181 (2011) 83–90 View metadata, citation and similar papers at core.ac.uk brought to you by CORE Contents lists available at ScienceDirect provided by Elsevier - Publisher Connector Veterinary Parasitology jo urnal homepage: www.elsevier.com/locate/vetpar Evaluation of miltefosine for the treatment of dogs naturally infected with L. infantum (=L. chagasi) in Brazil a,∗ b b b b H.M. Andrade , V.P.C.P. Toledo , M.B. Pinheiro , T.M.P.D. Guimarães , N.C. Oliveira , c c c c c c c J.A. Castro , R.N. Silva , A.C. Amorim , R.M.S.S. Brandão , M. Yoko , A.S. Silva , K. Dumont , d d c M.L. Ribeiro Jr. , W. Bartchewsky , S.J.H. Monte a Universidade Federal de Minas Gerais, Instituto de Ciências Biológicas, Departamento de Parasitologia, Belo Horizonte, MG, Brazil b Universidade Federal de Minas Gerais, Faculdade de Farmácia, Departamento de Análises Clínicas, Belo Horizonte, MG, Brazil c Universidade Federal do Piauí, Centro de Ciências da Saúde, Departamento de Parasitologia e Microbiologia, Teresina, PI, Brazil d Universidade São Francisco, Braganc¸ a Paulista, São Paulo, Brazil a r t i c l e i n f o a b s t r a c t Article history: Dogs naturally infected with Leishmania Infantum (=L. chagasi) were treated with miltefos- Received 4 February 2011 ine using different therapeutic regimens. The animals were evaluated for clinical evolution, Received in revised form 6 May 2011 biochemical parameters, parasite load (by real-time PCR), cytokine levels and humoral Accepted 9 May 2011 response. After treatment and during the following 24 months, there was progressive clin- ical improvement and complete recovery in 50% (7/14) of the treated animals. There was Keywords: a decrease in the smear positivity of the bone marrow after treatment, and there was also Visceral Leishmaniasis a gradual and constant decrease in positive cultures at the end of the follow-up period. Treatment Dogs However, the PCR detection of parasite DNA remained positive. In general, all animals pre- ␥ Miltefosine sented a significant increase in parasite load 6 months after treatment. The IFN- levels in all the groups tended to increase during follow-up period, regardless of the miltefosine dose administered. The IL-4 and IL-10 levels of the animals tended to decrease during follow-up, except after 300 days when only IL-10 increased. The serum antibodies identified antigens that ranged from 116 kDa to less than 29 kDa in the Western blot assay. Furthermore, 300 days after treatment, qualitative and quantitative differences in the antigen profiles were observed. Antigens of 97 and 46 kDa were the most intensely recognized. Higher levels of antigen-specific Leishmania IgG were detected before and 300 days after treatment in all groups. Taking together, the improvement in the clinical symptoms was not followed by parasitological clearance, suggesting that treatment with miltefosine is not recommended, especially in endemic areas like Brazil, where children are the major victims and dogs are involved in the maintenance of the parasite cycle. © 2011 Elsevier B.V. Open access under the Elsevier OA license. 1. Introduction Depending on the species of Leishmania and the immune response of the host, there are several clinical manifesta- Leishmaniasis infects approximately 12 million indi- tions of the disease: cutaneous, mucocutaneous, diffuse, viduals in 88 countries, and 350 million people are at and visceral. Visceral leishmaniasis (VL), a more severe dis- risk of contracting the infection (http://www.who.int/en/). ease, is considered to be an anthroponosis in India and Central Africa and a zoonosis in the Mediterranean and the Americas. The zoonotic VL caused by L. infantum (also ∗ known as L. chagasi) accounts for 20% of the global human Corresponding author. Tel.: +55 3134093010; fax: +55 3132235841. visceral leishmaniasis (100,000 cases per year), and its inci- E-mail addresses: [email protected], [email protected] (H.M. Andrade). dence is increasing in urban and peri-urban areas of the 0304-4017 © 2011 Elsevier B.V. Open access under the Elsevier OA license. doi:10.1016/j.vetpar.2011.05.009 84 H.M. Andrade et al. / Veterinary Parasitology 181 (2011) 83–90 tropics (Dye, 1996). The domestic dog is considered to be The diagnosis of Leishmania infection was confirmed by the primary reservoir and plays a central role in transmit- serological tests (IFA—cut off 1:80), conventional PCR and ting the parasite to humans and sand flies. the detection of amastigotes in smears of bone marrow. Brazil has the highest incidence of zoonotic VL in the Before beginning the treatment schedule, the dogs were world, with about 3000 new cases per year. Moreover, the treated for parasites (endo and exo) and clinically inspected number of areas with incidences that favor a widespread for other possible co-infections (Babesiosis, Erlichiosis and epidemic, which could affect young people or individuals dermatosis). They were kept in a kennel protected by an with co-morbidities and cause a high number of deaths, anti-sand fly screen with water and food “ad libitum” dur- is increasing. The mortality rate of VL has increased from ing the treatment and throughout the follow-up period. 3.6% in 1994 to 6.7% in 2003, which represents an inflation Three different miltefosine treatment schedules were of 85% (Ministério da Saúde, 2006). The control measures administered as described below: adopted include the diagnosis of canine and human cases, which is followed by the treatment of infected humans Group 1 (n = 5): 100 mg miltefosine/animal, administered and euthanasia of infected dogs. The euthanasia of animals daily over a period of 28 days. is a controversial measure, and alternatives for treatment Group 2 (n = 5): 200 mg miltefosine/animal, administered are highly desirable. There is, however, a lack of obvious daily for 28 days. alternatives for the treatment of human and canine VL. Group 3 (n = 4): 100 mg miltefosine/animal, administered Miltefosine has just become available in India for the daily for 45 days. treatment of human VL. This drug is an alkyphospholipid that was originally developed as an oral antineoplastic 2.2. Clinical evaluation agent (Sundar et al., 1998). Miltefosine is a simple, very sta- ble, relatively safe, and highly efficient molecule. Currently Before, immediately after, and at 3-month intervals in clinical trials, it has become the first oral drug available over a period of 2 years after treatment, the animals for the treatment of human visceral and cutaneous leish- were evaluated for the presence of clinical symptoms of maniasis. Miltefosine is toxic for Leishmania parasites, and VL, such as dermatitis, skin ulceration, alopecia, ocular it enhances both T cell and macrophage activation and the lesions, lymphadenopathy, weight loss, epistaxis, diar- production of microbicidal reactive nitrogen and oxygen rhoea, and onychogryphosis. For each assessment, blood intermediates (Soto et al., 2006). samples were collected for laboratory analysis. At the end Few studies have been conducted using miltefosine of these analyses, all animals were sacrificed according for the treatment of Canine Visceral Leishmaniasis (CVL). to resolution no. 714 of the Federal Council of Veterinary Recently, it was shown that treatment with miltefosine Medicine (CFMV) and submitted to necropsy. A spleen alone reduced Leishmania replication, and the parasite was fragment was collected for Leishmania isolation, and the eradicated from the blood, although it was not removed parasite load was determined by q-PCR (quantitative PCR from the lymph nodes (Manna et al., 2008a). This phe- using real time-PCR). nomenon may be a potential reason for the recurrence of the disease. Furthermore, clinical information on the effi- 2.3. Biochemical evaluation cacy and action of miltefosine for the treatment of canine leishmaniasis is limited. The alanine aminotransferase (ALAT), aspartate amino- The objective of the current study was to treat dogs transferase (ASAT), total protein, albumin, globulin, naturally infected with L. Infantum in Brazil endemic area direct/indirect bilirubin, urea, and creatinine levels were using different protocols. The animals were evaluated for determined in blood samples collected from each exper- clinical evolution, biochemistry, parasite load (by real-time imental group at the intervals mentioned above. An ® PCR), cytokine levels and humoral response. To the authors’ automated biochemical analyzer (Ciba Express 550) and ® knowledge, this is the most complete study concerning the the compatible, commercial reagents (Labtest ) were treatment of CVL with miltefosine in Americas. employed. The samples were processed by the kinetic enzymatic method according to the manufacturer’s recom- mendations. All of the tests were performed in the Clinical 2. Materials and methods Pathology Laboratory of the Veterinary Hospital of the Fed- eral University of Piauí. 2.1. Animals 2.4. Parasitological evaluation The study protocol was approved by the Research Ethics committee of the Federal University of Piauí. The presence of Leishmania was investigated in bone Fourteen mongrel animals (Canis familiaris) of unknown marrow samples obtained by sternal puncture from ani- ages were diagnosed by seroepidemiology for CVL, which mals under sedation. Giemsa smears were obtained from was performed during the control program by the Zoonoses these samples and evaluated by microscopy. An aliquot of Control Center of the municipality of Teresina, Piauí, Brazil. the bone marrow aspirate was transferred to the NNN- ◦ The animals were diagnosed with an indirect immunoflu- LIT culture medium, which was maintained at 25 C and orescence assay (IFA). The seropositive dogs were donated examined weekly for 30 days. to the kennel of the Federal University of Piauí to be used The parasite loads in the bone marrow and spleen sam- in the experiments. ples were evaluated by q-PCR. The DNA in the samples was H.M. Andrade et al. / Veterinary Parasitology 181 (2011) 83–90 85 extracted with phenol–chloroform, as described by Silva milliliter of cell suspension was added to two wells of a et al.
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