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UNIVERSIDADE FEDERAL DE MATO GROSSO
PROGRAMA DE RESIDÊNCIA UNIPROFISSIONAL EM
MEDICINA VETERINÁRIA
LABORATÓRIO DE PARASITOLOGIA E DOENÇAS PARASITÁRIAS
Infection by Sarcocystis neurona and Toxoplasma gondii in dogs in
the northern region of Brazil.
LEODIL DA COSTA FREITAS
Cuiabá
2015
UNIVERSIDADE FEDERAL DE MATO GROSSO
PROGRAMA DE RESIDÊNCIA UNIPROFISSIONAL EM
MEDICINA VETERINÁRIA
LABORATÓRIO DE PARASITOLOGIA E DOENÇAS PARASITÁRIAS
Infection by Sarcocystis neurona and Toxoplasma gondii in dogs in
the northern region of Brazil.
Autor: Leodil da Costa Freitas
Orientador: Prof. Dr. Richard de Campos Pacheco
Trabalho de Conclusão de Curso apresentado ao Curso de
Pós-graduação de Medicina Veterinária da Universidade
Federal de Mato Grosso, como requisito para obtenção do
título de Residência Uniprofissional em Medicina
Veterinária, área de concentração: Medicina Veterinária
Preventiva
Cuiabá
2015
Dados Internacionais de Catalogação na Fonte.
C837i Costa Freitas, Leodil da. Infection by sarcocystis neurona and toxoplasma gondii in dogs in the
northern region of Brazil. / Leodil da Costa Freitas. -- 2015 8 f. ; 30 cm.
Orientador: Richard de Campos Pacheco. Co-orientador: Daniel Moura de Aguiar. TCC (especialização em Medicina Veterinária) - Universidade
Federal de Mato Grosso, Faculdade de Agronomia e Medicina Veterinária, Residência Uniprofissional em Medicina Veterinária, Cuiabá, 2015.
Inclui bibliografia.
1. Sarcocystis neurona. 2. Toxoplasma gondii. 3. Ji- Paraná/Rondônia. 4. Indirect immunofluorescence assay. I. Título.
Ficha catalográfica elaborada automaticamente de acordo com os dados fornecidos pelo(a) autor(a).
Permitida a reprodução parcial ou total, desde que citada a fonte.
UNIVERSIDADE FEDERAL DE MATO GROSSO
PROGRAMA DE RESIDÊNCIA UNIPROFISSIONAL EM MEDICINA
VETERINÁRIA
LABORATÓRIO DE PARASITOLOGIA E DOENÇAS PARASITÁRIAS
Infection by Sarcocystis neurona and Toxoplasma gondii in dogs in the
northern region of Brazil.
BANCA EXAMINADORA
Aprovado: ________ de fevereiro de 2015
__________________________________________
Prof. Dr. Richard de Campos Pacheco
Presidente da Banca - UFMT
__________________________________________
Alice Mamede Costa Marques Borges - UFMT
__________________________________________
Andréia Lima Tomé Melo - UFMT
Trabalho de Conclusão de Curso apresentado ao Curso de Pós-graduação de Medicina
Veterinária da Universidade Federal de Mato Grosso, como requisito para obtenção do
título de Residência Uniprofissional em Medicina Veterinária, área de concentração:
Medicina Veterinária Preventiva.
Infection by sarcocystis neurona and toxoplasma gondii in dogs in the northern region of
Brazil.
Infecção por Sarcocystis neurona e Toxoplasma gondii em cães da região norte do Brasil.
Leodil da Costa Freitas1*; Thábata dos Anjos Pacheco
2; Andréia Lima Tomé Melo
2; Felipe
Wolf Jaune2; Ricardo Vilas Boas
2, Dirceu Guilherme de Souza Ramos
2 Daniel Moura de
Aguiar2, Richard de Campos Pacheco
2
RESUMO
Sarcocystis neurona e Toxoplasma gondii são protozoários do Filo Apicomplexa e família
Sarcocystidae. S. neurona é um protozoário coccídeo formador de cistos teciduais, agente
etiológico da Mieloencefalite Protozoária Equina, uma severa síndrome neurológica que
acomete eqüinos e causa grande impacto econômico nas Américas. Toxoplasmose é uma
zoonose cosmopolita e os cães são considerados sentinelas para este parasita por causa de seu
contato próximo dos seres humanos e gatos. Objetivou-se avaliar a ocorrência de anticorpos
anti-S. neurona e anti-T. gondii em cães de propriedades rurais do município de Ji-
Paraná/Rondônia. Foram analisadas 181 amostras de soro sanguíneo por meio da reação de
imunofluorescência indireta (RIFI). Das amostras testadas, observou-se ocorrência de 57
(31,49%) positivas para T. gondii e 20 (11,04%) para S. neurona, caracterizando a ampla
distribuição dos agentes na região estudada.
Palavras Chaves: Sarcocystis neurona; Toxoplasma gondii; Ji-Paraná/Rondônia;
Imunofluorescência Indireta
ABSTRACT
Sarcocystis neurona and Toxoplasma gondii are protozoa phylum Apicomplexa and
Sarcocystidae family. S. neurona is a coccidium forming tissue cysts, which causes of Equine
1 Discente, Residência Uniprofissional em Medicina Veterinária, UNIPRUV, Universidade Federal de Mato Grosso, UFMT,
Cuiabá, Mato Grosso. 2 Programa de Pós-graduação em Ciências Veterinárias, PPGVET, Universidade Federal de Mato Grosso, UFMT, Cuiabá,
Mato Grosso.
* Autor para correspondência. [email protected]
protozoal myeloencephalitis, a severe neurological syndrome that affects horses and great
economic impact in the Americas. Toxoplasmosis is a cosmopolitan zoonosis and dogs are
sentinels for this parasite because of their close contact with humans and cats. Aimed to
evaluate the occurrence of anti-S. neurona antibodies and anti-T. gondii in dogs from family
farming properties in the city of Ji-Paraná / Rondônia. We analyzed 181 samples of blood
serum by indirect immunofluorescence assay (IFA). Of the samples tested, there was
occurrence of 57 (31.49%) positive for T. gondii and 20 (11.04%) for S. neurona, featuring
the wide distribution of agents in the region studied.
Key Words: Sarcocystis neurona; Toxoplasma gondii; Ji-Paraná/Rondônia; Indirect
immunofluorescence assay.
Sarcocystis neurona and Toxoplasma gondii are related apicomplexans that can cause
systemic illness in many species of animals, including dogs (DUBEY et al., 2006). Equine
protozoal myeloencephalitis (EPM) due to the protozoan parasite, S. neurona continues to be
a serious neurological disease of horses in the Americas. (DUBEY et al., 2015). Toxoplasma
gondii is a widespread zoonotic protozoan that infects most, if not all, species of birds and
mammals, including dogs (DUBEY, 2010). Infection with T. gondii in dogs is also of
epidemiological importance. The prevalence of T. gondii infection in dogs may reflect the
magnitude of parasite contamination in their environment. For this reason, dogs have been
used as sentinel animal for T. gondii infection because of their close contact with people
(SALB et al., 2008). The present study aimed to carry out a serological study on S. neurona
and T. gondii infection among dogs of dairy cattle in rural areas in the municipality of Ji-
Paraná, Rondônia, in the western Brazilian Amazon region.
This study sampled dogs living in farms (i.e., population of dairy cows on family
farms). Dogs were sampled primarily for another project on the epidemiology of neosporosis
(VILAS BOAS et al., 2015) etween September 2012 and November 2013. Blood was
collected from all the dogs (n=181) present on 61 of the 63 farms. The responsible for each
farm answered a questionnaire addressing epidemiological factors relating to handling of
animals (dairy cows and dogs) in each farm.
The immunofluorescent antibody test (IFAT) was performed to detect serum
antibodies (IgG) against S. neurona and T. gondii, using the following antigens: T. gondii RH
strain tachyzoites, as described by CAMARGO (1964) and S. neurona SN37R strain
(SOFALY et al., 2002), as described by DUARTE et al. (2003). The cut-offs adopted were
dilutions of 1:16 for T. gondii and 1:25 for S. neurona, respectively (RIVETTI el al., 2008;
ANDRÉ et al., 2010). Positive and negative control samples were included on each slide, and
a goat anti-cat immunoglobulin G (anti-IgG) labeled with fluorescein isothiocyanate was used
as conjugate. The slides were examined using an epifluorescence microscope. The samples
considered positive were subjected to a two-fold serial dilution to obtain the final titer.
Statistical analyses were performed using the statistical software EPIINFO 7.0. The
associations between dogs positive (S. neurona and/or T. gondii) and the variables were
analyzed by means of the chi-square (2) and Fisher exact tests, with significance of 5%. The
covariate variables analyzed were: presence of dogs; dogs positive for S. neurona and T.
gondii on farm; occurrence of abortion; wild canids nearby; dogs with access to cattle food;
dogs with access to water for cattle; presence of felids; presence of equidae; dogs with access
to remains of dead cattle carcasses; dogs fed with heat-treated food or foodstuffs scrapped
(with uncooked or undercooked meat); cattle grazing with dogs present; destination of the
dead animals; destination of fetuses, when observed; dogs that get stuck or loose; farming
system (extensive or intensive); has recently acquired dog; farrowing of dogs on the property;
age and sex of dogs. Statistical analyses were performed comparing these covariates and
farms with presence of seropositive dogs for S. neurona and T. gondii using the methodology
of generalized linear models (GLM).
The Bioethical Committee for Animal Research of the Federal University of Mato
Grosso approved the present study, under protocol no. 23108.015662/12-5.
Antibodies to S. neurona (titers ≥ 25) were found 11.04% (20/181), with titers ranging
from 25 to 800, while antibodies to S T. gondii (titers ≥ 16) were found 31.49% (57/181), with
titers ranging from 16 to 2,048 (Table 1).
Table 1. Titers frequencies of antibodies against Toxoplasma gondii and Sarcocystis neurona
in dogs by means of the indirect immunofluorescent assay (IFA) of the 63 farms in the
municipality of Ji-Paraná, Rondônia, collected from September 2012 to November 2013.
Sarcocystis neurona Toxoplasma gondii
Titer Positive sample (%) Titer Positive sample (%)
25 1 (5) 16 2 (3,508)
50 2 (10) 32 8 (14,035)
100 5 (25) 64 14 (24,561)
200 6 (30) 128 17 (29,824)
400 5 (25) 256 6 (10,526)
800 1 (5) 512 5 (8,771)
1600 0 (0) 1024 2 (3,508)
3200 0 (0) 2048 3 (5,263)
Total 20 (100) Total 57 (100)
Univariate correlations between examined variables and the presence of seropositive
dogs showed that the kind of food provided to dogs is associated with occurrences of S.
neurona antibodies in the farms studied (p=0,021).
Statistical analysis using the chi-square test for linear tendency was significantly
associated to T. gondii among seropositive dogs and the variable dog age resulting in χ2 =
5.990 and p = 0.014. The odds ratio analysis (OR) obtained, considering the results by age
group, was 0-12 months OR = 1.000; 12-24 months OR = 0.96; 24-36 months OR = 1.56; 36-
48 months OR = 3.44 and above 48 months OR = 2,342. The GLM analyses showed that in
farms with positive dogs to S. neurona and T. gondii was associated with kind of food
provided to dogs (heat-treated food or foodstuffs scrapped with uncooked or undercooked
meat; F-test <0,001) and with dogs that have access to bovine carcass (F-test=0,003),
respectively.
Serological surveys indicate that T. gondii are prevalent worldwide. Approximately
30% of cats and dogs in the United States have T. gondii antibodies (DUBEY et al., 2009).
The occurrence of seropositive dogs (57%) in the study showed wide incidence of the
infectious agent in the rural area of municipality and the human exposure to the disease,
because dogs may reflect the magnitude of parasite contamination in their environment
(SALB et al., 2008).
Anti-T. gondii antibodies and dog age revealed statistically difference by the qui-
square test, with a significant increase in the number of positive animals with age. Group
of dogs at 36 to 48 months age had 3.44 times more the chance to be exposed to T. gondii
infection. The magnitude of titer is not associated with clinical signs, and this occurs because
seroprevalence increases with age due to chance of agent exposure during the lifetime rather
than disease susceptibility (DUBEY et al., 2009).
Dogs that have access to bovine carcass show significant (F-test=0,003) differences of
infection by T. gondii, indicating the possible participation of cattle in the transmission of the
parasite. Among livestock, infection by T. gondii bovines seem to be more resistant to
infection than other animals (DUBEY, 1994), however parasites may remain viable in their
tissues until slaughtering age (DUBEY, 1983), possibly serving as a source of infection.
Despite S. neurona is related apicomplexan that can cause systemic illness in dogs
(DUBEY et al., 2006). Antibodies to S. neurona detected (11.04%) suggest the exposure of
farm dogs and, possibly, other animals, as well as environmental contamination with the
parasite. Therefore, EPM due to the protozoan parasite, S. neurona should be considered in
case of neurological disease of horses in the study area, since in all farms (n=20) with positive
dogs had the presence of equine.
Dogs fed with foodstuffs scrapped showed significant differences of infection by S.
neurona. Sarcocystis species transmission should be relation with ingestion of undercooked
meat, since during their life cycle they requires both an intermediated and a final host, usually
an herbivorous and carnivorous vertebrate animal, respectively (DUBEY et al., 2015).
However, a problem to investigated Sarcocystis species is immunologic cross-reactivity
amongst these parasites (O’DONOGHUE 1990; HAMIR et al., 1993). So, should be
considered an occurrence of infection in farm dogs for others species than S. neurona.
Acknowledgements
To the Technical Assistance and Rural Extension Association of the State of Rondônia. And
Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the scholarships
of A.L.T. Melo, T.A. Pacheco, Ramos, D.G.S., D.M. Aguiar, and R.C. Pacheco.
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10.1. Citação de livro:
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herbívoros. Manaus : INPA, 1979. 95p.
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GORBAMAN, A. A comparative pathology of thyroid. In: HAZARD, J.B.; SMITH, D.E. The thyroid.
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MEWIS, I.; ULRICHS, CH. Action of amorphous diatomaceous earth against different stages of
the stored product pests Tribolium confusum (Coleoptera: Tenebrionidae), Tenebrio molitor
(Coleoptera: Tenebrionidae), Sitophilus granarius (Coleoptera: Curculionidae) and Plodia
interpunctella (Lepidoptera: Pyralidae). Journal of Stored Product Research, Amsterdam
(Cidade opcional), v.37, p.153‐164, 2001. Disponível em:
<http://dx.doi.org/10.1016/S0022‐474X(00)00016‐3>. Acesso em: 20 nov. 2008. doi:
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(1991 ‐ Informe verbal). Ao final do texto, antes das Referências Bibliográficas, citar o endereço
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Ciência Rural
Obrigado por enviar seu manuscrito para Ciência Rural .
Manuscrito ID:
CR20150582
Título: Ocorrência de Sarcocystis neurona e toxoplasma gondii em cães da região norte do Brasil.
Autores:
FREITAS, LEODIL Pacheco, Thabata Melo, Andréia Jaune, Felipe Vilas Boas, Ricardo Ramos, Dirceu Moura de Aguiar, Daniel Pacheco, Richard
F r
eview
Ciência Rural
Occurrence of sarcocystis neurona and toxoplasma gondii in dogs in the northern region of Brazil.
Journal: Ciência Rural
Manuscript ID: CR-2015-0582
Manuscript Type: Note
Keyword:
Sarcocystis neurona, Toxoplasma gondii, Ji-Paraná/Rondônia, Indirect immunofluorescence assay
https://mc04.manuscriptcentral.com/cr-scielo
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Occurrence of anti-Sarcocystis neurona and Toxoplasma gondii antibodies in dogs in the
northern region of Brazil.
Ocorrencia de aticorpos anti Sarcocystis neurona e Toxoplasma gondii em cães na região
norte do Brasil.
- NOTE –
ABSTRACT
This study aimed to evaluate the occurrence of anti-S. neurona and T. gondii antibodies in
dogs from family farming properties in the city of Ji-Paraná/Rondônia. We analyzed 181
samples of blood serum by means indirect fluorescent antibody test (IFAT). We observed the
occurrence of 57 (31.49%) and 20 (11.04%) positive serum samples for T. gondii for S.
neurona, respectively, featuring the wide distribution of agents in the region studied. The
kind of food provided to dogs was associated with occurrences of S. neurona antibodies.
While, dog age and access to bovine carcass were the variables that showed as risk factors for
the presence of T. gondii.
Key Words: Antibodies; Sarcocystis neurona; Toxoplasma gondii; Ji-Paraná/Rondônia;
Indirect immunofluorescence assay.
RESUMO
Neste estudo objetivou-se avaliar a ocorrência de anticorpos anti-S. neurona e T. gondii em
cães de propriedades de agricultura familiar do município de Ji-Paraná/Rondônia. Foram
analisadas 181 amostras de soro sanguíneo por meio da reação de imunofluorescência indireta
(RIFI). Observou-se ocorrência de 57 (31,49%) e 20 (11,04%) amostras de soro positivas para
T. gondii e S. neurona, respectivamente, caracterizando a ampla distribuição dos agentes na
região estudada. O tipo de alimento fornecido aos cães foi associada com a ocorrência de
anticorpos para S. neurona. Enquanto, a idade do cão e o acesso à carcaça de bovinos foram
as variáveis que se mostraram como fatores de risco para a presença de T. gondii.
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Palavras Chaves: Anticorpos; Sarcocystis neurona; Toxoplasma gondii; Ji-
Paraná/Rondônia; Imunofluorescência Indireta
Sarcocystis neurona and Toxoplasma gondii are related apicomplexans that can cause
systemic illness in many species of animals, including dogs (DUBEY et al., 2006). Equine
protozoal myeloencephalitis (EPM), due to the protozoan parasite S. neurona, continues to be
a serious neurological disease of horses in the Americas (DUBEY et al., 2015). Toxoplasma
gondii is a widespread zoonotic protozoan that infects most, if not all, species of birds and
mammals, including dogs (DUBEY, 2010). Dogs have been used as sentinel animal for T.
gondii infection because of their close contact with people and cats (SALB et al., 2008). The
present study aimed to carry out a serological-epidemiological study on S. neurona and T.
gondii infection among dogs of dairy cattle and evaluate risk factors for this infection in rural
areas in the municipality of Ji-Paraná, Rondônia, in the western Brazilian Amazon region.
This study sampled dogs living in farms (i.e., population of dairy cows on family
farms). Dogs were sampled primarily for another project on the epidemiology of neosporosis
(VILAS BOAS et al., 2015) between September 2012 and November 2013. Blood was
collected from all the dogs (n=181) present on 61 of the 63 farms. The responsible for each
farm answered a questionnaire addressing epidemiological factors relating to handling of
animals in each farm.
The levels of S. neurona and T. gondii antibodies were measured by means of the
indirect fluorescent antibody test (IFAT) using the following antigens: T. gondii RH strain
tachyzoites, as described by CAMARGO (1964) and S. neurona SN37R strain (SOFALY et
al., 2002), as described by DUARTE et al. (2003). The cut-offs adopted were dilutions of 1:16
for T. gondii and 1:25 for S. neurona, respectively (RIVETTI el al., 2008; ANDRÉ et al.,
2010). Positive and negative control samples were included on each slide, and a goat anti-cat
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immunoglobulin G (anti-IgG) labeled with fluorescein isothiocyanate was used as conjugate.
Samples considered positive were subjected to a two-fold serial dilution to obtain the final
titer.
Statistical analyses were performed using the statistical software EPIINFO 7.0. The
associations between dogs positive (S. neurona and/or T. gondii) and the variables were
analyzed by means of the chi-square (χ2) and Fisher exact tests, with significance of 5%. The
covariate variables analyzed were: presence of dogs; dogs positive for S. neurona and/or T.
gondii on farm; occurrence of abortion; wild canids nearby; dogs with access to cattle food;
dogs with access to water for cattle; presence of felids; presence of equidae; dogs with access
to remains of dead cattle carcasses; dogs fed with heat-treated food or foodstuffs scrapped
(with uncooked or undercooked meat); cattle grazing with dogs present; destination of the
dead animals; destination of fetuses, when observed; dogs that get stuck or loose; farming
system (extensive or intensive); has recently acquired dog; farrowing of dogs on the property;
age and sex of dogs. Statistical analyses were performed comparing these covariates and
farms with presence of seropositive dogs for S. neurona and T. gondii using the methodology
of generalized linear models (GLM).
Antibodies to S. neurona (titers ≥ 25) were found 11.04% (20/181), with titers ranging
from 25 to 800, while antibodies to T. gondii (titers ≥ 16) were found 31.49% (57/181), with
titers ranging from 16 to 2,048 (Table 1).
Univariate correlations between examined variables and the presence of seropositive
dogs showed that the kind of food provided to dogs is associated with occurrences of S.
neurona antibodies in the farms studied (p=0,021).
Statistical analysis using the chi-square test for linear tendency was significantly
associated to T. gondii among seropositive dogs and the variable dog age resulting in χ2 =
5.990 and p = 0.014. The odds ratio analysis (OR) obtained, considering the results by age
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group, was 0-12 months OR = 1.000; 12-24 months OR = 0.96; 24-36 months OR = 1.56; 36-
48 months OR = 3.44 and above 48 months OR = 2,342. The GLM analyses showed that
farms with positive dogs to S. neurona and T. gondii were associated with kind of food
provided to dogs (heat-treated food or foodstuffs scrapped with uncooked or undercooked
meat; F-test <0,001) and with dogs that have had access to bovine carcass (F-test=0,003),
respectively.
Serological surveys indicate that T. gondii are prevalent worldwide. Approximately
30% of cats and dogs in the United States have T. gondii antibodies (DUBEY et al., 2009).
The occurrence of seropositive dogs (57%) in the study showed wide e high incidence of the
infectious agent in the rural area of municipality, possibly with the human and livestock
exposure to the disease. High seroprevalence in dogs may reflect the magnitude of parasite
contamination in their environment (SALB et al., 2008). Anti-T. gondii antibodies and dog
age revealed statistically difference by the qui-square test, with a significant increase in the
number of positive animals with age. Group of dogs at 36 to 48 months age had 3.44 times
more the chance to be exposed to T. gondii infection. The magnitude of titer is not associated
with clinical signs, and this occurs because seroprevalence increases with age due to chance
of agent exposure during the lifetime rather than disease susceptibility (DUBEY et al., 2009).
Dogs that have had access to bovine carcass showed significant (F-test=0,003)
differences of infection by T. gondii, suggesting the possible participation of cattle in the
transmission of the parasite. Among livestock, bovines seem to be more resistant to infection
by T. gondii than other animals; however, cysts of T. gondii may remain viable in their
tissues until slaughtering age and, possibly serving as a source of infection (DUBEY, 2010).
Despite S. neurona is an apicomplexan that can cause systemic illness in dogs
(DUBEY et al., 2006) there is no serological survey in dogs in Brazil. Antibodies to S.
neurona detected (11.04%), for the first time, suggest the exposure of farm dogs and,
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possibly, other animals, as well as environmental contamination with the parasite. Therefore,
EPM due to the protozoan parasite, S. neurona should be considered in case of neurological
disease of horses in the study area, since in all farms (n=20) with positive dogs had the
presence of equine.
Dogs fed with foodstuffs scrapped showed significant differences of infection by S.
neurona. Sarcocystis species are intracellular protozoan parasites with a requisite two-host
life cycle based on a prey-predator (intermediate-definitive), therefore the transmission of
Sarcocystis species could be related with ingestion of undercooked meat. Despite antibody
titers to the parasite (up to 800) were found in dogs, which is suggestive of true exposure to S.
neurona (MENESES et al., 2014), a problem to research Sarcocystis species is immunologic
cross-reactivity amongst these parasites (HAMIR et al., 1993). So, should be considered an
occurrence of infection in farm dogs for others species than S. neurona.
This study observed the infection and distribution of T. gondii and S. neurona in farm
dogs in the municipality of Ji-Paraná, Rondônia. In addition, kind of food provided to dogs is
associated with occurrences of S. neurona, while dogs with access to bovine carcass and
older are associate with the occurrence of T. gondii.
ACKNOWLEDGEMENTS
ETHICS COMMITTEE AND BIOSAFETY
The Bioethical Committee for Animal Research of the Federal University of XXX
approved the present study, under protocol no. 23108.015662/12-5.
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10 Toxoplasma gondii Sarcocystis neurona
11 12 Titer Positive sample (%) Titer Positive sample (%)
13 14 16 2 (3,51) 25 1 (5) 15 16 17
32 8 (14,03) 50 2 (10)
18 19
64
14 (24,56)
100
5 (25)
20 21
128
17 (29,82)
200
6 (30)
23
256
6 (10,53)
400
5 (25) 24 25 512 5 (8,77) 800 1 (5) 26 27 28
1024 2 (3,51)
29 30
2048
3 (5,27)
31 32
Total
57 (100)
Total
20 (100) 33 34 4 35 36 37 5
1 2 3 1 Table 1. Titers frequencies of antibodies against Toxoplasma gondii and Sarcocystis neurona 4 5 2 in dogs by means of the indirect fluorescent antibody test (IFAT) of the
63 farms in the 6 7 3 municipality of Ji-Paraná, Rondônia, collected from September 2012 to
November 2013. 8 9
22
38 39 40 41 42 43 44 45 46 47 48 49 50 51 52