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The outcomes of polyparasitism in stray cats from Brazilian Midwest assessed by epidemiological, hematological and pathological data

Poliparasitismo em gatos não domiciliados no Centro-Oeste brasileiro avaliado através dos aspectos epidemiológicos, hematológicos e patológicos

Abstract

We evaluated the epidemiological, hematological, and pathological data of Leishmania spp., Toxoplasma gondii, Platynosomum illiciens, feline immunodeficiency virus (FIV), and feline leukemia virus (FeLV) infections and the coinfections in stray cats of an endemic area for leishmaniasis. The diagnosis was performed by serological tests and necropsy. We described gross lesions and histopathological findings. We used immunohistochemistry and chromogenic in situ hybridization for L. infantum detection. We found infection in 27 out of 50 sampled cats, among them, 14 presented coinfections. A strong correlation between splenomegaly and lymphadenomegaly with FeLV, and an association between hepatic lesions and cachexia with parasitism due to P. illiciens were observed. Moreover, we found a significant increase in the monocyte count in the FeLV-infected and a decrease in the red blood cell count in the FIV-infected animals. Amastigote forms of Leishmania spp. and tissue changes were detected in lymphoid organs of an animal coinfected with P. illiciens, T. gondii, and FIV. Polyparasitism recorded in stray cats of the Brazilian Midwest should be considered in effective control strategies for public health diseases. Moreover, stray cats of Campo Grande may be a source of infection of FIV, FeLV and P. illiciens for populations of domiciled cats.

Keywords:
Toxoplasma gondii; Platynosomum illiciens; Feline Immunodeficiency virus; Feline Leukemia virus; in situ hybridization

Resumo

Foi avaliada a epidemiologia, hematologia e patologia das infecções por Leishmania spp., Toxoplasma gondii, Platynosomum illiciens, vírus da imunodeficiência felina (FIV) e vírus da leucemia felina (FeLV) e das coinfecções em gatos não domiciliados em uma área endêmica para leishmaniose. O diagnóstico foi realizado por exames sorológicos e necropsia. Foram descritas lesões macroscópicas e achados histopatológicos. Usaram-se imuno-histoquímica e hibridização cromogênica in situ para detecção de L. infantum. Encontrou-se infecção em 27 dos 50 gatos amostrados, dentre eles, 14 apresentavam coinfecções. Foi observada forte correlação entre esplenomegalia e linfadenomegalia com FeLV, e associação entre lesões hepáticas e caquexia com parasitismo por P. illiciens. Além disso, foi encontrado um aumento significativo na contagem de monócitos nos animais infectados pelo FeLV e uma diminuição na contagem de hemácias nos animais infectados pelo FIV. Formas amastigotas de Leishmania spp. e alterações teciduais foram detectadas em órgãos linfoides de um animal coinfectado com P. illiciens, T. gondii e FIV. O poliparasitismo registrado em gatos errantes do Centro-Oeste brasileiro deve ser considerado nas estratégias de controle de zoonoses. Além disso, gatos errantes de Campo Grande podem ser fontes de infecção de FIV, FeLV e P. illiciens para populações de gatos domiciliados.

Palavras-chave:
Toxoplasma gondii; Platynosomum illiciens; vírus da Imunodeficiência Felina; vírus da Leucemia felina; hibridização in situ

Introduction

Parasitism is an interspecific relationship in which one species finds its ecological niche in another, including viruses and several eukaryotic organisms such as bacteria, protozoa, rickettsiae, helminths, and arthropods (Araújo et al., 2003Araújo A, Jansen AM, Bouchet F, Reinhard K, Ferreira LF. Parasitism, the diversity of life, and paleoparasitology. Mem Inst Oswaldo Cruz 2003; 98(suppl 1): 5-11. http://dx.doi.org/10.1590/S0074-02762003000900003. PMid:12687756.
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Since parasites are globally spread in different ecological niches, representing approximately 40% of all biodiversity, it is expected that animals can be exposed to infections by several parasites simultaneously (coinfections) (Cox, 2001Cox FEG. Concomitant infections, parasites and immune responses. Parasitology 2001;122(Suppl): S23-S38. http://dx.doi.org/10.1017/S003118200001698X. PMid:11442193.
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). Furthermore, records indicated that cats parasitized by Leishmania spp. become more likely to coinfections by feline immunodeficiency virus (FIV), feline leukemia virus (FeLV), and Toxoplasma gondii (Dorny et al., 2002Dorny P, Speybroeck N, Verstraete S, Baeke M, De Becker A, Berkvens D, et al. Serological survey of Toxoplasma gondii of a on feline immunodeficiency virus and feine leukaemia virus in urban stray cats in Belgium. Vet Rec 2002; 151(21): 626-629. http://dx.doi.org/10.1136/vr.151.21.626. PMid:12479298.
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). The association between cats seropositive for Toxoplasma gondii and retrovirus has also been reported in other countries (Dorny et al., 2002Dorny P, Speybroeck N, Verstraete S, Baeke M, De Becker A, Berkvens D, et al. Serological survey of Toxoplasma gondii of a on feline immunodeficiency virus and feine leukaemia virus in urban stray cats in Belgium. Vet Rec 2002; 151(21): 626-629. http://dx.doi.org/10.1136/vr.151.21.626. PMid:12479298.
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; Cong et al., 2016Cong W, Meng Q-F, Blaga R, Villena I, Zhu X-Q, Qian A-D. Toxoplasma gondii, Dirofilaria immitis, feline immunodeficiency virus (FIV), and feline leukemia virus (FeLV) infections in stray and pet cats (Felis catus) in northwest China: co-infections and risk factors. Parasitol Res 2016; 115(1): 217-223. http://dx.doi.org/10.1007/s00436-015-4738-y. PMid:26362646.
http://dx.doi.org/10.1007/s00436-015-473...
). This study aimed to assess the epidemiological, hematological, and pathological data of Leishmania spp., T. gondii, Platynosomum illiciens, FIV, and FeLV infections, and coinfections, in stray cats from the city of Campo Grande in Midwestern Brazil, an endemic area for human and canine visceral leishmaniasis (VL).

Materials and Methods

Animals and sample collection

We sampled 50 adult stray cats (Felis catus) from the Zoonotic Disease Control Center (CCZ) in the municipality of Campo Grande, Mato Grosso do Sul state, an endemic area for visceral leishmaniasis (VL) in Brazil (20º29’19”S, 54º36’20”W). These cats were randomly selected with no limitation for age, sex, and clinical status during January–June 2019. The CCZ is responsible for the development of actions aimed at the control of zoonosis through the control of populations of stray dogs and cats including euthanasia according CCZ protocol, in accordance with the ethical standards established by the Federal Council of Veterinary Medicine published in the Brazilian guide to good practices for euthanasia in animals (CFMV, 2020Conselho Federal de Medicina Veterinária – CFMV. Guia Brasileiro de Boas Práticas para a Eutanásia em Animais [online]. Brasília: CFMV; 2020 [cited 2022 Mar 16]. Available from: https://www.cfmv.gov.br/guia-brasileiro-de-boas-praticas-para-a-eutanasia-em-animais/comunicacao/publicacoes/2020/08/03/#28
https://www.cfmv.gov.br/guia-brasileiro-...
). This study was approved by the Ethics Committee for the Use of Experimental Animals of the Universidade Católica Dom Bosco (UCDB) (protocol number 004/2014).

After the 50 cats had been sedated, whole blood was collected by punction of the jugular vein and placed in tubes containing ethylenediamine tetraacetic acid. Red blood cell (RBC), and white blood cell (WBC) counts were performed using an automated cell counter (Sysmex poch 100iV®). The hematocrit value was detected using the microhematocrit technique, and specific leucometry was performed by counting 100 leukocytes in blood smears stained with Giemsa. Necropsies were performed in the Department of Pathology of UCDB with the purpose of evaluating tissue alterations, including cachexia as a parameter for assessing body condition, as well as the search for P. illiciens, an endemic Trematoda in the study area (Personal communication from Andrade, GB) in the liver parenchyma. After gross evaluation, tissue fragments of the lymph node, spleen, and liver were collected and fixed in buffered formalin (pH 7,3) for 24 h.

Histopathological evaluation

Fragments of liver, spleen, and lymph nodes were processed using the usual histology slide preparation techniques and stained with hematoxylin and eosin (HE) for light microscopy analysis (Luna, 1968Luna LG. Manual of histologic staining methods of the armed forces institute of pathology. New York: McGraw-Hill; 1968.). Histopathology evaluated tissue damage, pattern of inflammation, and the presence of amastigotes of Leishmania spp.

Serological diagnosis

For the detection of IgG antibodies to FIV (96% sensitivity and of 98% specificity) and FeLV p27 antigens (90.70% sensitivity and 97.78% specificity) (Medeiros et al., 2019Medeiros SO, Silva BJA, Carneiro AL, Ferreira Júnior OC, Tanuri A. Avaliação de dois testes sorológicos comerciais para diagnóstico das infecções pelo FIV e pelo FeLV. Arq Bras Med Vet Zootec 2019; 71(2): 447-454. http://dx.doi.org/10.1590/1678-4162-10111.
http://dx.doi.org/10.1590/1678-4162-1011...
) in whole blood, we used Alere FIV Ac and FeLV Ag Test Kit® chromatographic immunoassays according to Feitosa et al. (2021)Feitosa TF, Costa FTR, Ferreira LC, Silva SS, Santos A, Silva WI, et al. High rate of feline immunodeficiency virus infection in cats in the Brazilian semiarid region: Occurrence, associated factors and coinfection with Toxoplasma gondii and feline leukemia virus. Comp Immunol Microbiol Infect Dis 2021; 79: 101718. http://dx.doi.org/10.1016/j.cimid.2021.101718. PMid:34794005.
http://dx.doi.org/10.1016/j.cimid.2021.1...
and in accordance with the manufacturer’s recommendation. The presence of T. gondii and L. infantum antibodies in the serum of sampled animal was detected by the Indirect fluorescent Assay (IFAT), as described previously (André et al., 2010André MR, Adania CH, Teixeira RHF, Silva KF, Jusi MMG, Machado STZ, et al. Antibodies to Toxoplasma gondii and Neospora caninum in captive neotropical and exotic wild canids and felids. J Parasitol 2010; 96(5): 1007-1009. http://dx.doi.org/10.1645/GE-2502.1. PMid:20950109.
http://dx.doi.org/10.1645/GE-2502.1...
; Oliveira et al., 2008Oliveira TM, Furuta PI, de Carvalho D, Machado RZ. Study of cross-reactivity in serum samples from dogs positive for Leishmania sp., Babesia canis and Ehrlichia canis in enzyme-linked immunosorbent assay and indirect fluorescent antibody test. Rev Bras Parasitol Vet 2008; 17(1): 7-11. http://dx.doi.org/10.1590/S1984-29612008000100002. PMid:18554433.
http://dx.doi.org/10.1590/S1984-29612008...
). Toxoplasma gondii RH strain tachyzoites and promastigotes of L. infantum were used as antigens, ten microliters of sera at dilution of 1:40 (cut-off for T. gondii) and 1:40 (cut-off for L. infantum) were placed in wells on antigen slides. Cat serum samples positive and negative for T. gondii and L. infantum (André et al., 2010André MR, Adania CH, Teixeira RHF, Silva KF, Jusi MMG, Machado STZ, et al. Antibodies to Toxoplasma gondii and Neospora caninum in captive neotropical and exotic wild canids and felids. J Parasitol 2010; 96(5): 1007-1009. http://dx.doi.org/10.1645/GE-2502.1. PMid:20950109.
http://dx.doi.org/10.1645/GE-2502.1...
; Braga et al., 2012Braga MSCO, André MR, Jusi MMG, Freschi CR, Teixeira MCA, Machado RZ. Occurrence of anti-Toxoplasma gondii and anti-Neospora caninum antibodies in cats with outdoor access in São Luís, Maranhão, Brazil. Rev Bras Parasitol Vet 2012; 21(2): 107-111. http://dx.doi.org/10.1590/S1984-29612012000200007. PMid:22832749.
http://dx.doi.org/10.1590/S1984-29612012...
), obtained from the serum bank of the Laboratory of Immunoparasitology, Department of Veterinary Pathology of Universidade Estadual Paulista, Jaboticabal, São Paulo, were also used in the serological reactions. Slides were incubated at 37°C in a moist chamber for 45 min, washed three times in phosphate-buffered saline (pH 7.2) for 5 min, and air-dried at room temperature. Immunoglobulin G (IgG) anti-cat conjugate (whole molecule with fluorescein isothiocyanate, dilution of 1:32; SigmaR, St. Louis, Missouri) for domestic feline samples were diluted according to the manufacturer’s instructions and added to each well. These slides were incubated again, washed, dried, and overlaid with buffered glycerin (pH 8.7), covered with glass coverslips, and examined using an epifluorescence microscope (Olympus, Japan).

Immunohistochemical technique for Leishmania spp.

Immunohistochemistry (IHC) for Leishmania spp. was performed in the lymphoid tissues of the five Leishmania spp. seropositive cats. Antigen retrieval was performed with citrate buffer and then incubated in Protein Block® (Thermo Fisher Scientific, Cheshire, UK). Sections of the spleen and lymph nodes were treated with rabbit polyclonal anti-Leishmania antibody (in-house) (Boechat et al., 2016Boechat VC, Mendes AAV Jr, Madeira MF, Ferreira LC, Figueiredo FB, Rodrigues FCC, et al. Occurrence of Leishmania infantum and associated histological alterations in the genital tract and mammary glands of naturally infected dogs. Parasitol Res 2016; 115(6): 2371-2379. http://dx.doi.org/10.1007/s00436-016-4987-4. PMid:26979730.
http://dx.doi.org/10.1007/s00436-016-498...
). The EasyLink One HiDef HRP® detection system was used. The slides were counterstained with hematoxylin and observed under a light microscope. Positive and negative controls were included.

In situ hybridization for Leishmania infantum

Chromogenic in situ hybridization (CISH) was used to identify if the amastigote forms detected in the five positive cats for Leishmania spp. by IHC were those of L. infantum. We used CISH in order to associate tissue reaction with the presence of the parasite. For this purpose, a L. infantum-specific oligonucleotide probe labeled with digoxigenin that targets the minicircle kinetoplast DNA gene of the parasite was used (Menezes et al., 2013Menezes RC, Figueiredo FB, Wise AG, Madeira MF, Oliveira RVC, Schubach TMP, et al. Sensitivity and specificity of In Situ Hybridization for diagnosis of cutaneous infection by Leishmania infantum in dogs. J Clin Microbiol 2013; 51(1): 206-211. http://dx.doi.org/10.1128/JCM.02123-12. PMid:23135932.
http://dx.doi.org/10.1128/JCM.02123-12...
). Five micrometer thick sections were cut from the paraffin blocks and mounted on silanized slides. These sections were processed as previously described (Boechat et al., 2016Boechat VC, Mendes AAV Jr, Madeira MF, Ferreira LC, Figueiredo FB, Rodrigues FCC, et al. Occurrence of Leishmania infantum and associated histological alterations in the genital tract and mammary glands of naturally infected dogs. Parasitol Res 2016; 115(6): 2371-2379. http://dx.doi.org/10.1007/s00436-016-4987-4. PMid:26979730.
http://dx.doi.org/10.1007/s00436-016-498...
), using the ZytoFastPlus chromogenic CISH Implementation Kit AP-NBT/BCIP1 (Zytovision GmbH, Bremerhaven, Germany). The probe was diluted at 1:500 in the hybridization solution H7782 (Sigma-Aldrich Co., St. Louis, MO, USA). Positive and negative controls were included.

Statistical analyses

The Shapiro-Wilk test was performed to verify the normality of the hematological results. When appropriate, the paired t-test (normal distribution) or paired Wilcoxon test (non-normal distribution) was used to compare the means of hematological variables among infected and non-infected animals. The level of significance was set at p <0.05. Generalized linear models (GLM) were used to investigate associations among infections and necropsy findings. The candidate models were compared using the corrected Akaike information criterion (AICc). The model with a lower AICc value was considered the best-fit model (Akaike, 1974Akaike H. A new look at the statistical model identification. IEEE Trans Automat Contr 1974; 19(6): 716-723. http://dx.doi.org/10.1109/TAC.1974.1100705.
http://dx.doi.org/10.1109/TAC.1974.11007...
).

Results

Overall, we found that 54% (27/50) of the sampled cats presented infections, among them 51.8% (14/27) displayed coinfections and 48.1% (13/27) showed infections by retrovirus (six single and seven coinfections) (Table 1). The seroprevalence of T. gondii, FeLV, FIV, and Leishmania spp. was 28% (n=14), 18% (n=9), 12% (n=6), and 10% (n=5), respectively. Furthermore, during the necropsy we found P. illiciens in the hepatic parenchyma of 22% (n=11) of the sampled cats. Single infections by T. gondii and FeLV were observed in six (12%) and five (10%) of the sampled animals, respectively (Table 1). Moreover, we found one cat infected only with Leishmania spp. and one infected only with FIV (Table 1). With respect to coinfection with retroviruses (n=5), we found two cats coinfected with T. gondii and FeLV, two with FIV and P. illiciens, and one with FIV and FeLV. Two of the sampled cats showed coinfection with four infectious agents (Table 1), and in one of these cats L. infantum was detected by CISH (Table 1). We highlight that all cats parasitized with P. illiciens showed concomitant infections.

Table 1
Single infections and coinfections in stray cats of Campo Grande, Midwestern Brazil. Data are expressed by the number of positive samples following by percentage of occurrence.

The Shapiro-Wilk test showed that RBC and hematocrit were normally distributed, while monocyte, lymphocyte, neutrophil, eosinophil, and basophil counts did not display normal distribution. Moreover, our statistical analyses demonstrated a strong correlation between splenomegaly and lymphadenomegaly in FeLV seropositive cats (Table 2). In fact, at necropsy, 88.9% (8/9) of the FeLV seropositive cats presented these findings. Moreover, significant higher monocyte counts (p = 0.01) were detected in FeLV seropositive (2,160/μL) than seronegative animals (513/ μL). Furthermore, a significant decrease in RBC was found in FIV seropositive (6,182,500/μL) compared to seronegative (8,414,500/μL) cats (p<0.05).

Table 2
Associations among necropsy findings and Platynosomum illiciens and feline leukemia virus performed using generalized linear models (GLM) on 50 stray cats from Campo Grande, Mato Grosso do Sul, Brazil.

A significant correlation between hepatic lesions and cachexia with P. illiciens was detected by GLM analysis (Table 2). Indeed, hepatic lesions were observed in 90.9% (10/11) of the necropsied cats parasitized with P. illiciens. These lesions consisted of hepatomegaly, whitish coloration, firm texture of the portal areas, thickness of bile ducts, and fibrosis. Microscopically, we observed cholangioectasis and P. illiciens inside the fibrotic and dilated bile ducts (Figure 1).

Figure 1
Photomicrograph of the liver of a cat naturally infected with Platynosomum illiciens. Cross sections of the parasite (Pi) inside a dilated and fibrous bile duct (BD). HE, 5X Objective.

Among the Leishmania spp. seropositive cats (n=5), the IHC detected amastigote forms of Leishmania spp. inside the macrophages, as well as diffused in the interstitial space of the spleen and lymph nodes of a single animal coinfected with P. illiciens, T. gondii, and FIV (Figure 2A and 2B). In addition, using CISH, infection with L. infantum was confirmed in this animal (Figure 3). Furthermore, the histopathological analysis of this polyparasitized cat demonstrated great disorganization of the white pulp together with the atrophy of the germinal center (Figure 4), with marginal zone and lymphoid follicle atrophy. In the red pulp, histiocytosis, epithelioid cells and Mott cells were also noted. Also, we observed granulomas, plasmacytosis, histiocytosis, and epithelioid cells in the lymph node parenchyma (Figure 5).

Figure 2
Photomicrograph of immunohistochemistry of spleen (A) and lymph node (B) of a cat infected with feline immunodeficiency virus, Toxoplasma gondii, Leishmania spp., and Platynosomum illiciens. Note the amastigote forms (arrows) in the cytoplasm of macrophages and in extracellular space. IHC, 100X Objective.
Figure 3
Photomicrograph of the lymph node of a cat coinfected with feline immunodeficiency virus, Toxoplasma gondii, Leishmania infantum, and Platynosomum illiciens. Chromogenic in situ hybridization showing blue-stained amastigote forms of L. infantum (arrows) inside the cytoplasm of macrophages. CISH, 100X Objective.
Figure 4
Photomicrograph of a spleen of a cat coinfected with feline immunodeficiency virus, Toxoplasma gondii, Leishmania infantum, and Platynosomum illiciens. Note the disorganized white pulp (WP, rectangle) with hypoplastic germinal center (GC, ellipse). HE, 10X Objective.
Figure 5
Photomicrograph of a lymph node of a cat coinfected with feline immunodeficiency virus, Toxoplasma gondii, Leishmania infantum, and Platynosomum illiciens. Note the formation of granuloma (large circle) with the central area of necrosis and the presence of plasma cells (head arrows), histiocytes (small circles) and epithelioid cells (arrows). HE, 20X Objective.

Discussion

Although the seroprevalence of 10% observed here was greater than that found by Braga et al. (2014a)Braga ARC, Corrêa APFL, Camossi LG, da Silva RC, Langoni H, Lucheis SB. Coinfection by Toxoplasma gondii and Leishmania spp. in domestic cats (Felis catus) in State of Mato Grosso do Sul. Rev Soc Bras Med Trop 2014a; 47(6): 796-797. http://dx.doi.org/10.1590/0037-8682-0041-2014. PMid:25626663.
http://dx.doi.org/10.1590/0037-8682-0041...
and Metzdorf et al. (2017)Metzdorf IP, da Costa Lima MS, de Fatima Cepa Matos M, de Souza Filho AF, de Souza Tsujisaki RA, Franco KG, et al. Molecular characterization of Leishmania infantum in domestic cats in a region of Brazil endemic for human and canine visceral leishmaniasis. Acta Trop 2017; 166: 121-125. http://dx.doi.org/10.1016/j.actatropica.2016.11.013. PMid:27851895.
http://dx.doi.org/10.1016/j.actatropica....
in cats from Campo Grande, Mato Grosso do Sul state, the role of this domestic species in the transmission and maintenance of L. infantum in endemic areas of Brazil is not well established (Nascimento et al., 2022Nascimento LFJ, Cirilo TM, Gomes DS, Gomes ACA, Lima VFS, Scher R, et al. Epidemiological and diagnostic aspects of feline leishmaniasis with emphasis on Brazil: a narrative review. Parasitol Res 2022; 121(1): 21-34. http://dx.doi.org/10.1007/s00436-021-07372-9. PMid:34761278.
http://dx.doi.org/10.1007/s00436-021-073...
). Cats seem to have no epidemiological importance in endemic areas for VL since we found only one animal with L. infantum, in accordance with Berenguer et al. (2021)Berenguer LKAR, Gomes CFCA, Nascimento JO, Bernardi JCM, Lima VFS, De Oliveira JB, et al. Leishmania infantum infection in a domestic cat: A real threat or an occasional finding? Acta Parasitol 2021; 66(2): 673-676. http://dx.doi.org/10.1007/s11686-020-00294-z. PMid:33044603.
http://dx.doi.org/10.1007/s11686-020-002...
that detected amastigotes forms in a single cat (1/128) from Pernambuco state. Furthermore, Braga et al. (2014b)Braga ARC, Langoni H, Lucheis S. Evaluation of canine and feline leishmaniasis by the association of blood culture, immunofluorescent antibody test and polymerase chain reaction. J Venom Anim Toxins Incl Trop Dis 2014b; 20(1): 5. http://dx.doi.org/10.1186/1678-9199-20-5. PMid:24565284.
http://dx.doi.org/10.1186/1678-9199-20-5...
did not show amastigotes forms in seropositive cats (15/50) from Campo Grande. Moreover, the infection by L. infantum in cats has demonstrated minimal or limited pathological changes (Solano-Gallego et al., 2007Solano-Gallego L, Iniesta L, Rodríguez-Cortés A, Pastor J, Quintana J, Espada Y, et al. Cross-sectional serosurvey of feline leishmaniasis in ecoregions around the northwestern mediterranean. Am J Trop Med Hyg 2007; 76(4): 676-680. http://dx.doi.org/10.4269/ajtmh.2007.76.676. PMid:17426169.
http://dx.doi.org/10.4269/ajtmh.2007.76....
; Pennisi et al., 2015Pennisi M-G, Cardoso L, Baneth G, Bourdeau P, Koutinas A, Miró G, et al. LeishVet update and recommendations on feline leishmaniosis. Parasit Vectors 2015; 8(1): 302. http://dx.doi.org/10.1186/s13071-015-0909-z. PMid:26041555.
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; Soares et al., 2016Soares CSA, Duarte SC, Sousa SR. What do we know about feline leishmaniosis? J Feline Med Surg 2016; 18(6): 435-442. http://dx.doi.org/10.1177/1098612X15589358. PMid:26116620.
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), in agreement with our results which showed no correlation between Leishmania spp. seropositive cats and gross lesions.

The presence of amastigote forms of L. infantum in the single cat may be related to the coinfection by T. gondii, P. illiciens, and FIV. Indeed, the immunosuppression caused by retrovirus may facilitate parasite survival in macrophages by evading natural killer cells and cytotoxic lymphocyte activity (Dorny et al., 2002Dorny P, Speybroeck N, Verstraete S, Baeke M, De Becker A, Berkvens D, et al. Serological survey of Toxoplasma gondii of a on feline immunodeficiency virus and feine leukaemia virus in urban stray cats in Belgium. Vet Rec 2002; 151(21): 626-629. http://dx.doi.org/10.1136/vr.151.21.626. PMid:12479298.
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; Grevot et al., 2005Grevot A, Jaussaud Hugues P, Marty P, Pratlong F, Ozon C, Haas P, et al. Leishmaniosis due to Leishmania infantum in a FIV and FeIV positive cat with a squamous cell carcinoma diagnosed with histological, serological and isoenzymatic methods. Parasite 2005; 12(3): 271-275. http://dx.doi.org/10.1051/parasite/2005123271. PMid:16218216.
http://dx.doi.org/10.1051/parasite/20051...
; Sobrinho et al., 2012Sobrinho LS, Rossi CN, Vides JP, Braga ET, Gomes AA, de Lima VM, et al. Coinfection of Leishmania chagasi with Toxoplasma gondii, Feline Immunodeficiency Virus (FIV) and Feline Leukemia Virus (FeLV) in cats from an endemic area of zoonotic visceral leishmaniasis. Vet Parasitol 2012; 187(1–2): 302-306. http://dx.doi.org/10.1016/j.vetpar.2012.01.010. PMid:22285010.
http://dx.doi.org/10.1016/j.vetpar.2012....
; Spada et al., 2012Spada E, Proverbio D, Pepa A, Perego R, Baggiani L, DeGiorgi GB, et al. Seroprevalence of feline immunodeficiency virus, feline leukaemia virus and Toxoplasma gondii in stray cat colonies in northern Italy and correlation with clinical and laboratory data. J Feline Med Surg 2012; 14(6): 369-377. http://dx.doi.org/10.1177/1098612X12437352. PMid:22318850.
http://dx.doi.org/10.1177/1098612X124373...
). In fact, the parasite persistence during coinfection by L. infantum and retroviruses was reported in humans as a consequence of the impairment of macrophage function (Rossi & Fasel, 2018Rossi M, Fasel N. How to master the host immune system? Leishmania parasites have the solutions! Int Immunol 2018; 30(3): 103-111. http://dx.doi.org/10.1093/intimm/dxx075. PMid:29294040.
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) and probably contributed to the lymphoid tissue damage recorded in the cat with amastigotes forms of L. infantum, also observed in severe canine VL with high parasite load (Cavalcanti et al., 2015Cavalcanti AS, Ribeiro-Alves M, Pereira LOR, Mestre GL, Ferreira ABR, Morgado FN, et al. Parasite load induces progressive spleen architecture breakage and impairs cytokine mRNA expression in Leishmania infantum-naturally infected dogs. PLoS One 2015; 10(4): e0123009. http://dx.doi.org/10.1371/journal.pone.0123009. PMid:25875101.
http://dx.doi.org/10.1371/journal.pone.0...
). Furthermore, histiocytosis and Mott cells observed in the spleen, as well as increase in plasma cells and granulomas in the lymph node of this animal, suggest a chronic infection (Moreira et al., 2010Moreira PRR, Vieira LM, De Andrade MMC, De Barros Bandarra M, Machado GF, Munari DP, et al. Immune response pattern of the popliteal lymph nodes of dogs with visceral leishmaniasis. Parasitol Res 2010; 107(3): 605-613. http://dx.doi.org/10.1007/s00436-010-1902-2. PMid:20499098.
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; Mossuto et al., 2015Mossuto MF, Ami D, Anelli T, Fagioli C, Doglia SM, Sitia R. Biochemical nature of Russell Bodies. Sci Rep 2015; 5(1): 12585. http://dx.doi.org/10.1038/srep12585. PMid:26223695.
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; Lucas, 2017Lucas SB. Lymph node pathology in infectious diseases. Diagn Histopathol 2017; 23(9): 420-430. http://dx.doi.org/10.1016/j.mpdhp.2017.07.002.
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). The plasmacytosis observed in the lymph node of the cat coinfected by L. infantum, T. gondii, P. illiciens, and FIV is a common finding related to VL (Veress et al., 1977Veress B, Omer A, Satir AA, El Hassan AM. Morphology of the spleen and lymph nodes in fatal visceral leishmaniasis. Immunology 1977; 33(5): 605-610. PMid:590992.; Campos-Neto & Bunn-Moreno, 1982Campos-Neto A, Bunn-Moreno MM. Polyclonal B cell activation in hamsters infected with parasites of the genus Leishmania. Infect Immun 1982; 38(3): 871-876. http://dx.doi.org/10.1128/iai.38.3.871-876.1982. PMid:6759410.
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; Galvão-Castro et al., 1984Galvão-Castro B, Sá Ferreira JA, Marzochi KF, Marzochi MC, Coutinho SG, Lambert PH. Polyclonal B cell activation, circulating immune complexes and autoimmunity in human american visceral leishmaniasis. Clin Exp Immunol 1984; 56(1): 58-66. PMid:6424987.; Bagues et al., 2018Bagues NCT, Pinheiro CGM, Bastos LA, Fraga DBM, Veras PST, Pontes-de-Carvalho LC, et al. Parasitic load and histological aspects in different regions of the spleen of dogs with visceral leishmaniasis. Comp Immunol Microbiol Infect Dis 2018; 56: 14-19. http://dx.doi.org/10.1016/j.cimid.2017.11.003. PMid:29406277.
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; Silva-Barrios et al., 2018Silva-Barrios S, Charpentier T, Stäger S. The deadly dance of B cells with trypanosomatids. Trends Parasitol 2018; 34(2): 155-171. http://dx.doi.org/10.1016/j.pt.2017.10.001. PMid:29089182.
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), and in lentiviral infections (Takano et al., 2012Takano T, Hosoya S, Shibao A, Nagasaki B, Yoshioka H, Satoh R, et al. Comparative study of the plasma globulin level, CD21− B-cell counts and FOXP3 mRNA expression level in CD4+ T-cells for different clinical stages of feline immunodeficiency virus infected cats. Res Vet Sci 2012; 92(1): 157-161. http://dx.doi.org/10.1016/j.rvsc.2010.10.022. PMid:21074227.
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; Magden et al., 2013Magden E, Miller C, MacMillan M, Bielefeldt-Ohmann H, Avery A, Quackenbush SL, et al. Acute virulent infection with feline immunodeficiency virus (FIV) results in lymphomagenesis via an indirect mechanism. Virology 2013; 436(2): 284-294. http://dx.doi.org/10.1016/j.virol.2012.12.003. PMid:23290868.
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).

The polyparasitism was demonstrated in 51.8% (14/27) of the infected cats, in accordance with several reports in the studied area (Braga et al., 2014aBraga ARC, Corrêa APFL, Camossi LG, da Silva RC, Langoni H, Lucheis SB. Coinfection by Toxoplasma gondii and Leishmania spp. in domestic cats (Felis catus) in State of Mato Grosso do Sul. Rev Soc Bras Med Trop 2014a; 47(6): 796-797. http://dx.doi.org/10.1590/0037-8682-0041-2014. PMid:25626663.
http://dx.doi.org/10.1590/0037-8682-0041...
; Sousa et al., 2014Sousa KCM, Herrera HM, Domingos IH, Campos JBV, Santos IMC, Neves HH, et al. Serological detection of Toxoplasma gondii, Leishmania infantum and Neospora caninum in cats from an area endemic for leishmaniasis in Brazil. Rev Bras Parasitol Vet 2014; 23(4): 449-455. http://dx.doi.org/10.1590/s1984-29612014078. PMid:25517522.
http://dx.doi.org/10.1590/s1984-29612014...
; André et al., 2015André MR, Herrera HM, De Jesus FS, De Sousa KCM, Gonçalves LR, Domingos IH, et al. Tick-borne agents in domesticated and stray cats from the city of Campo Grande, state of Mato Grosso do Sul, midwestern Brazil. Ticks Tick Borne Dis 2015; 6(6): 779-786. http://dx.doi.org/10.1016/j.ttbdis.2015.07.004. PMid:26187416.
http://dx.doi.org/10.1016/j.ttbdis.2015....
), in Brazilian semiarid region (Miró et al., 2014Miró G, Rupérez C, Checa R, Gálvez R, Hernández L, García M, et al. Current status of L. infantum infection in stray cats in the Madrid region (Spain): implications for the recent outbreak of human leishmaniosis? Parasit Vectors 2014; 7(1): 112. http://dx.doi.org/10.1186/1756-3305-7-112. PMid:24655361.
http://dx.doi.org/10.1186/1756-3305-7-11...
; Feitosa et al., 2021Feitosa TF, Costa FTR, Ferreira LC, Silva SS, Santos A, Silva WI, et al. High rate of feline immunodeficiency virus infection in cats in the Brazilian semiarid region: Occurrence, associated factors and coinfection with Toxoplasma gondii and feline leukemia virus. Comp Immunol Microbiol Infect Dis 2021; 79: 101718. http://dx.doi.org/10.1016/j.cimid.2021.101718. PMid:34794005.
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), and worldwide (Poli et al., 2002Poli A, Abramo F, Barsotti P, Leva S, Gramiccia M, Ludovisi A, et al. Feline leishmaniosis due to Leishmania infantum in Italy. Vet Parasitol 2002; 106(3): 181-191. http://dx.doi.org/10.1016/S0304-4017(02)00081-X. PMid:12062507.
http://dx.doi.org/10.1016/S0304-4017(02)...
; Ayllón et al., 2012Ayllón T, Diniz PPVP, Breitschwerdt EB, Villaescusa A, Rodríguez-Franco F, Sainz A. Vector-borne diseases in client-owned and stray cats from Madrid, Spain. Vector Borne Zoonotic Dis 2012; 12(2): 143-150. http://dx.doi.org/10.1089/vbz.2011.0729. PMid:22022820.
http://dx.doi.org/10.1089/vbz.2011.0729...
; Sobrinho et al., 2012Sobrinho LS, Rossi CN, Vides JP, Braga ET, Gomes AA, de Lima VM, et al. Coinfection of Leishmania chagasi with Toxoplasma gondii, Feline Immunodeficiency Virus (FIV) and Feline Leukemia Virus (FeLV) in cats from an endemic area of zoonotic visceral leishmaniasis. Vet Parasitol 2012; 187(1–2): 302-306. http://dx.doi.org/10.1016/j.vetpar.2012.01.010. PMid:22285010.
http://dx.doi.org/10.1016/j.vetpar.2012....
; Akhtardanesh et al. 2020Akhtardanesh B, Moeini E, Sharifi I, Saberi M, Sadeghi B, Ebrahimi M, et al. Leishmania infection in cats positive for immunodeficiency virus and feline leukemia virus in an endemic region of Iran. Vet Parasitol Reg Stud Rep 2020; 20: 100387. http://dx.doi.org/10.1016/j.vprsr.2020.100387. PMid:32448520.
http://dx.doi.org/10.1016/j.vprsr.2020.1...
). Sobrinho et al. (2012)Sobrinho LS, Rossi CN, Vides JP, Braga ET, Gomes AA, de Lima VM, et al. Coinfection of Leishmania chagasi with Toxoplasma gondii, Feline Immunodeficiency Virus (FIV) and Feline Leukemia Virus (FeLV) in cats from an endemic area of zoonotic visceral leishmaniasis. Vet Parasitol 2012; 187(1–2): 302-306. http://dx.doi.org/10.1016/j.vetpar.2012.01.010. PMid:22285010.
http://dx.doi.org/10.1016/j.vetpar.2012....
showed a strong association between Leishmania sp., FIV, and T. gondii in naturally infected cats in an endemic area for VL in southwest Brazil. Additionally, Feitosa et al. (2021)Feitosa TF, Costa FTR, Ferreira LC, Silva SS, Santos A, Silva WI, et al. High rate of feline immunodeficiency virus infection in cats in the Brazilian semiarid region: Occurrence, associated factors and coinfection with Toxoplasma gondii and feline leukemia virus. Comp Immunol Microbiol Infect Dis 2021; 79: 101718. http://dx.doi.org/10.1016/j.cimid.2021.101718. PMid:34794005.
http://dx.doi.org/10.1016/j.cimid.2021.1...
reported the correlation between FIV and T. gondii in owned cats of Brazilian semiarid region. However, the outcomes of coinfections on the host environment are still largely neglected.

Our analysis demonstrated that cachexia and hepatopathy were significantly related to parasitism by P. illiciens¸ helminth parasite found in all coinfected cats. Liver impairment as a consequence of chronic cholangiohepatitis observed here has been reported in platynosomiasis (Headley et al., 2012Headley SA, Gillen MA, Sanches AWD, Satti MZ. Platynosomum fastosum- induced chronic intrahepatic cholangitis and Spirometra spp. infections in feral cats from Grand Cayman. J Helminthol 2012; 86(2): 209-214. http://dx.doi.org/10.1017/S0022149X11000265. PMid:21729387.
http://dx.doi.org/10.1017/S0022149X11000...
; Jesus et al., 2015Jesus MFP, Brito JA, Silva VC, Pedroso PMO, Pimentel LA, Macedo JTSA, et al. Natural infection by Platynosomum illiciens in a stray cat in Cruz das Almas, Recôncavo da Bahia, Brazil. Braz J Vet Pathol 2015; 8(1): 25-28.; Ramos et al., 2017Ramos DGS, Santos ARGLO, Freitas LC, Braga ÍA, Silva EP, Soares LMC, et al. Feline platynosomiasis: analysis of the association of infection levels with pathological and biochemical findings. Rev Bras Parasitol Vet 2017; 26(1): 54-59. http://dx.doi.org/10.1590/s1984-29612017009. PMid:28327881.
http://dx.doi.org/10.1590/s1984-29612017...
) and certainly compromises the health of their hosts favoring coinfections. Similarly, T. gondii was found in 57.1% of coinfected cats, and when associated to L. infantum, FIV and/or FeLV may constitute a risk for the health of coinfected animals (Sobrinho et al., 2012Sobrinho LS, Rossi CN, Vides JP, Braga ET, Gomes AA, de Lima VM, et al. Coinfection of Leishmania chagasi with Toxoplasma gondii, Feline Immunodeficiency Virus (FIV) and Feline Leukemia Virus (FeLV) in cats from an endemic area of zoonotic visceral leishmaniasis. Vet Parasitol 2012; 187(1–2): 302-306. http://dx.doi.org/10.1016/j.vetpar.2012.01.010. PMid:22285010.
http://dx.doi.org/10.1016/j.vetpar.2012....
; Feitosa et al., 2021Feitosa TF, Costa FTR, Ferreira LC, Silva SS, Santos A, Silva WI, et al. High rate of feline immunodeficiency virus infection in cats in the Brazilian semiarid region: Occurrence, associated factors and coinfection with Toxoplasma gondii and feline leukemia virus. Comp Immunol Microbiol Infect Dis 2021; 79: 101718. http://dx.doi.org/10.1016/j.cimid.2021.101718. PMid:34794005.
http://dx.doi.org/10.1016/j.cimid.2021.1...
). In fact, although protozoan infection primarily induces a strong immune response, it subsequently fails to clear the infection, leading to a chronic phase (Gigley et al., 2012Gigley JP, Bhadra R, Moretto MM, Khan IA. T cell exhaustion in protozoan disease. Trends Parasitol 2012; 28(9): 377-384. http://dx.doi.org/10.1016/j.pt.2012.07.001. PMid:22832368.
http://dx.doi.org/10.1016/j.pt.2012.07.0...
). In the case of coinfection with FIV and T. gondii, clinical and fatal systemic toxoplasmosis have been recorded (Davidson et al., 1993Davidson MG, Rottman JB, English RV, Lappin MR, Tompkins MB. Feline immunodeficiency virus predisposes cats to acute generalized toxoplasmosis. Am J Pathol 1993; 143(5): 1486-1497. PMid:8238262.), analogous to the reports in people with toxoplasmosis and human immunodeficiency virus (Xavier et al., 2013Xavier GA, Cademartori BG, Cunha Filho NA, Farias NAR. Evaluation of seroepidemiological toxoplasmosis in HIV/AIDS patients in the south of Brazil. Rev Inst Med Trop São Paulo 2013; 55(1): 25-30. http://dx.doi.org/10.1590/S0036-46652013000100005. PMid:23328722.
http://dx.doi.org/10.1590/S0036-46652013...
).

Although anemia has long been related to FeLV (Hartmann, 2011Hartmann K. Clinical aspects of feline immunodeficiency and feline leukemia virus infection. Vet Immunol Immunopathol 2011; 143(3–4): 190-201. http://dx.doi.org/10.1016/j.vetimm.2011.06.003. PMid:21807418.
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; Cavalcante et al., 2018Cavalcante LTF, Muniz CP, Jia H, Augusto AM, Troccoli F, Medeiros SO, et al. Clinical and molecular features of Feline Foamy Virus and Feline Leukemia Virus co-infection in naturally-infected cats. Viruses 2018; 10(12): 702. http://dx.doi.org/10.3390/v10120702. PMid:30544924.
http://dx.doi.org/10.3390/v10120702...
; Abdollahi-Pirbazari et al., 2019Abdollahi-Pirbazari M, Jamshidi S, Nassiri SM, Zamani-Ahmadmahmudi M. Comparative measurement of FeLV load in hemolymphatic tissues of cats with hematologic cytopenias. BMC Vet Res 2019; 15(1): 460. http://dx.doi.org/10.1186/s12917-019-2208-y. PMid:31856815.
http://dx.doi.org/10.1186/s12917-019-220...
; Akhtardanesh et al., 2020Akhtardanesh B, Moeini E, Sharifi I, Saberi M, Sadeghi B, Ebrahimi M, et al. Leishmania infection in cats positive for immunodeficiency virus and feline leukemia virus in an endemic region of Iran. Vet Parasitol Reg Stud Rep 2020; 20: 100387. http://dx.doi.org/10.1016/j.vprsr.2020.100387. PMid:32448520.
http://dx.doi.org/10.1016/j.vprsr.2020.1...
; Gomez-Lucia et al., 2020Gomez-Lucia E, Collado VM, Miró G, Martín S, Benítez L, Doménech A. Clinical and hematological follow-up of long-term oral therapy with type-I interferon in cats naturally infected with Feline Leukemia Virus or Feline Immunodeficiency Virus. Animals (Basel) 2020; 10(9): 1464. http://dx.doi.org/10.3390/ani10091464. PMid:32825496.
http://dx.doi.org/10.3390/ani10091464...
), we found a strong correlation between FIV and low RBC, as reported by Spada et al. (2012)Spada E, Proverbio D, Pepa A, Perego R, Baggiani L, DeGiorgi GB, et al. Seroprevalence of feline immunodeficiency virus, feline leukaemia virus and Toxoplasma gondii in stray cat colonies in northern Italy and correlation with clinical and laboratory data. J Feline Med Surg 2012; 14(6): 369-377. http://dx.doi.org/10.1177/1098612X12437352. PMid:22318850.
http://dx.doi.org/10.1177/1098612X124373...
, suggesting that FIV may compromise the hematopoietic tissues. The association between splenomegaly and FeLV observed in the sampled cats may be linked to extramedullary hematopoiesis response to anemia, described in the late phases of FeLV infection (Shirani et al., 2011Shirani D, Nassiri SM, Aldavood SJ, Seddigh HS, Fathi E. Acute erythroid leukemia with multilineage dysplasia in a cat. Can Vet J 2011; 52(4): 389-393. PMid:21731091.; Hartmann, 2012Hartmann K. Clinical aspects of feline retroviruses: A review. Viruses 2012; 4(11): 2684-2710. http://dx.doi.org/10.3390/v4112684. PMid:23202500.
http://dx.doi.org/10.3390/v4112684...
). The immunosuppression frequently detected in FeLV predisposes to secondary infections resulting in lymphadenomegaly (Quackenbush et al., 1996Quackenbush SL, Dean GA, Mullins JI, Hoover EA. Analysis of FeLV-FAIDS provirus burden and productive infection in lymphocyte subsets in vivo. Virology 1996; 223(1): 1-9. http://dx.doi.org/10.1006/viro.1996.0449. PMid:8806534.
http://dx.doi.org/10.1006/viro.1996.0449...
; Hartmann, 2012Hartmann K. Clinical aspects of feline retroviruses: A review. Viruses 2012; 4(11): 2684-2710. http://dx.doi.org/10.3390/v4112684. PMid:23202500.
http://dx.doi.org/10.3390/v4112684...
; Hartmann & Hofmann-Lehmann, 2020Hartmann K, Hofmann-Lehmann R. What’s new in Feline Leukemia Virus infection. Vet Clin North Am Small Anim Pract 2020; 50(5): 1013-1036. http://dx.doi.org/10.1016/j.cvsm.2020.05.006. PMid:32680664.
http://dx.doi.org/10.1016/j.cvsm.2020.05...
), a condition significatively correlated to FeLV seropositive cats in the present study. Furthermore, monocytosis strongly associated with FeLV were also reported in chronic myelomonocytic leukemia with FeLV infection by Shimoda et al. (2000)Shimoda T, Shiranaga N, Mashita T, Hasegawa A. Chronic myelomonocytic leukemia in a cat. J Vet Med Sci 2000; 62(2): 195-197. http://dx.doi.org/10.1292/jvms.62.195. PMid:10720191.
http://dx.doi.org/10.1292/jvms.62.195...
. We highlight that splenomegaly and lymphadenomegaly in 88.9% of cats seropositive for FeLV should be considered an important indicator of this infection.

Conclusions

This study reported that coinfections by L. infantum, T. gondii, and P. illiciens result in damage to lymphoid tissues and liver, threatening the health of infected animals. Polyparasitism in stray cats of the Brazilian Midwest should be considered in order to assure effective control strategies for public health diseases. Moreover, stray cats of Campo Grande may be a source of infection of FIV, FeLV and P. illiciens for populations of domiciled cats.

  • How to cite: da Silva AR, Andrade GB, Carvalho JKMR, Barreto WTG, Martins Santos F, de Sousa KCM, et al. The outcomes of polyparasitism in stray cats from Brazilian Midwest assessed by epidemiological, hematological and pathological data. Braz J Vet Parasitol 2022; 31(2): e004222. https://doi.org/10.1590/S1984-29612022033

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Publication Dates

  • Publication in this collection
    04 July 2022
  • Date of issue
    2022

History

  • Received
    16 Mar 2022
  • Accepted
    30 May 2022
Colégio Brasileiro de Parasitologia Veterinária FCAV/UNESP - Departamento de Patologia Veterinária, Via de acesso Prof. Paulo Donato Castellane s/n, Zona Rural, , 14884-900 Jaboticabal - SP, Brasil, Fone: (16) 3209-7100 RAMAL 7934 - Jaboticabal - SP - Brazil
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