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Revista Brasileira de Parasitologia Veterinária

Print version ISSN 0103-846XOn-line version ISSN 1984-2961

Rev. Bras. Parasitol. Vet. vol.28 no.1 Jaboticabal Jan./Mar. 2019  Epub Feb 14, 2019

https://doi.org/10.1590/s1984-296120180096 

Original Article

Occurrence of zoonotic Enterocytozoon bieneusi in cats in Brazil

Ocorrência de Enterocytozoon bieneusi zoonótico em gatos no Brasil

Jamille Batista Faria Prado1 

Carlos Alberto do Nascimento Ramos2 
http://orcid.org/0000-0002-3084-172X

Vagner Ricardo da Silva Fiuza3 

Veronica Jorge Babo Terra2 

1 Programa de Pós-graduação em Ciências Veterinárias, Faculdade de Medicina Veterinária e Zootecnia, Universidade Federal de Mato Grosso do Sul – UFMS, Campo Grande, MS, Brasil

2 Faculdade de Medicina Veterinária e Zootecnia, Universidade Federal de Mato Grosso do Sul – UFMS, Campo Grande, MS, Brasil

3 Instituto de Biociências, Universidade Federal de Mato Grosso do Sul – UFMS, Cidade Universitária - Pioneiros, Campo Grande, MS, Brasil


Abstract

Enterocytozoon bieneusi is an opportunistic intestinal pathogen that infects humans and a wide variety of animals worldwide. Our aim in this study was to investigate the occurrence of E. bieneusi in a domestic cat population in Campo Grande, Mato Grosso do Sul, Brazil. Sixty fecal samples from diarrheic cats were subjected to polymerase chain reaction (PCR) and the amplicons were sequenced for identification. E. bieneusi was detected in two samples (3.3%), both identified as genotype D. This genotype has already been reported in animals and humans and is considered a zoonotic genotype. Our findings represent the first report of E. bieneusi in domestic cats in Brazil, reinforcing the importance of identifying this agent as a source of infection in animals and humans.

Keywords:  Microsporidia; zoonosis; felines; diagnosis; PCR

Resumo

Enterocytozoon bieneusi é um patógeno intestinal oportunista que infecta humanos e uma variedade de animais em todo o mundo. O objetivo no presente estudo foi investigar a ocorrência de E. bieneusi em uma população de gatos domésticos em Campo Grande, Mato Grosso do Sul, Brasil. Sessenta amostras fecais de gatos diarréicos foram submetidas a reação em cadeia da polimerase (PCR) e os produtos de amplificação foram sequenciados para identificação molecular. E. bieneusi foi detectado em duas amostras (3,3%), ambos identificados como genótipo D. Esse genótipo tem sido relatado em animais e humanos e é considerado um genótipo zoonótico. Nossos resultados representam a primeira descrição de E. bieneusi em gatos domésticos no Brasil, reforçando a importância desse agente como fonte de infecção para animais e humanos.

Palavras-chave:  Microsporídeo; zoonose; felinos; diagnóstico; PCR

Introduction

Microsporidia are obligate intracellular fungi. Currently between 1300 and 1500 different species have already been described, infecting a wide variety of invertebrate and vertebrate hosts, including humans ( VÁVRA & LUKEŠ, 2013 ; SANTÍN, 2015 ). However, only 17 species are known to be pathogenic to humans, among which Enterocytozoon bieneusi is considered the most common disease-causing species ( FAYER & SANTÍN, 2014 ; MATHIS et al., 2005 ). It is an opportunistic pathogen, which infects mainly immunocompromised individuals whose CD4+ cell counts are lower than 100 cels/mm3 ( ESPERN et al., 2007 ), causing clinical signs of chronic diarrhea associated with abdominal pain, fever and weight loss ( AKINBO et al., 2012 ; BRASIL et al., 2000 ). Transmission occurs through the fecal-oral route by the accidental ingestion of spores eliminated within feces from infected animals or humans or by the ingestion of contaminated water and/or food ( SANTÍN, 2015 ).

E. bieneusi was first identified in 1985 in enterocytes from an HIV positive human ( DESPORTES et al., 1985 ). In animals, E. bieneusi was first reported in pig feces in 1996 ( DEPLAZES et al., 1996 ), and since then it has been detected in the feces and intestinal tissue of 236 different animal species ( MATHIS et al., 2005 ; SANTÍN & FAYER, 2011 ; WANG et al., 2018 ). Information about the occurrence of E. bieneusi in cats is scanty; a few studies have been conducted in Asian and European countries, and a single study in South America. Most of these studies have identified zoonotic E. bieneusi genotypes, which includes cats as dispersing agents and a potential source of infection in humans. Given the absence of studies on E. bieneusi in cats in Brazil, the purpose of our research was to investigate the occurrence of E. bieneusi in diarrheic domestic cats in the city of Campo Grande, state of Mato Grosso do Sul, mid west Brazil.

Material and Methods

Samples

This study was approved by the Ethics Committee on Animal Use of the Federal University of Mato Grosso do Sul (Protocol no. 787/2016).

Fecal samples from 60 diarrheic cats were carefully collected from the ground immediately after defecation, between September 2016 and May 2017. The fecal samples were collected in private residences and veterinary clinics. The cats ages varied from 45 days to 17 years old. All the samples (approximately 8 grams each) were placed in clean containers and immediately sent for processing at the laboratory of molecular biology at veterinary hospital facilities. Aliquots of the samples (approximately 1g) were transferred to 1.5 mL polypropylene tubes containing 500 μL of 0.9% sterile saline solution, and stored at -20 °C until DNA extraction. The classification of feces as diarrheic was based on a scoring system presented by Queen et al. (2012) , in which score 1 was considered very firm, score 2 was considered well-formed, score 3 was considered soft-formed, and score 4 was considered watery. Only specimens with scores 3 or 4 were included in the diarrheic group.

DNA extraction

Three hundred microliters of the fecal suspensions stored in microtubes were centrifuged (10,000 x g for 10 minutes). After discarding the supernatant, the pellet was suspended in 500 μL of 20% SDS (Sodium Dodecyl Sulfate), and 10 μL of Proteinase K (20 mg/mL) were added. The suspension was homogenized in a vortex mixer and incubated at 65 °C for 10 minutes. Then, 400 μL of chloroform was added and the suspension was vortexed again, after which 300 μL of protein precipitation solution (5M potassium acetate, 11% glacial acetic acid) was added. The microtubes were centrifuged (10,000 x g for 10 minutes) and the supernatant transferred to a new 1.5 mL microtube. One mL of ethanol was then added for DNA precipitation. After another centrifugation step (10,000 x g for 5 minutes), the supernatant was discarded and the pellet washed with 1 mL of 70% ethanol. The samples were centrifuged for 2 min (10,000 x g ), and the pellets were allowed to dry at room temperature. Then, 100 μL of nuclease free water was added for DNA elution. An analysis of the material in an BioPhotometer Plus spectrophotometer (Eppendorf) indicated that all the samples showed a DNA concentration equal to or greater than 25 ng/μL and a ratio of 260/280nm equal to or greater than 1.75.

PCR and sequencing

The molecular identification of E. bieneusi was performed using a nested protocol, as described by Buckholt et al. (2002) . The primers for the first PCR were EBITS3 (5' GGT CAT AGG GAT GAA GAG 3') and EBITS4 (5' TCG AGT TCT TTC GCG CTC 3'). The second reaction was performed with the primers EBITS1 (5' GCT CTG AAT ATC TAT GGC T 3') and EBITS2.4 (5' ATC GCC GAC GGA TCC AAG TG 3'), amplifying a 392bp DNA fragment comprising part of the internal transcribed spacer (ITS) region of the E. bieneusi rRNA gene. Reactions were performed in a final volume of 25 μL containing 1.5 mM MgCl2, 50 mM KCl, 20 mM Tris-HCl (pH 9.0), 0.2 mM dNTPs, 1 μM of each primer, and 2.5 U of Taq DNA polymerase (Ludwig Biotec). The conditions for the first reaction was 94 °C for 3 min, followed by 35 cycles of denaturation at 94 °C for 30s, annealing at 57 °C for 30s, and extension at 72 °C for 40s, followed by a final extension at 72 °C for 10 min. The procedure for the second reaction was similar to the first, except the annealing temperature (55 °C), and the number of PCR cycles (30 cycles). E. bieneusi positive controls obtained from cattle from a previous study conducted in Brazil (FIUZA et al., 2016b), as well as negative controls (ultra-pure water), were included in all the reactions.

Amplification products were visualized in agarose gel (2%) stained with GelRed® (Biotium) under ultraviolet light after gel electrophoresis. Positive samples were purified using CleanSweep® PCR Purification (Applied Biosystems), following the manufacturer’s protocol, and were sequenced in both directions by the Sanger method ( SANGER et al., 1977 ). The resulting sequences were aligned with reference sequences downloaded from GenBank using the MEGA v. 7 program ( KUMAR et al., 2016 ) for genotype identification.

Results

Positive E. bieneusi PCR amplifications were observed in 2 (3.3%) of the 60 fecal samples. The samples came from a 3-month-old and a 5-year-old cat living in two different households. Both PCR products were successfully purified and sequenced, and presented 100% similarity with genotype D. The nucleotide sequences obtained in the present study were deposited in the GenBank database under accession nos. MH161409 and MH161410.

Discussion

This is the first report of presence of E. bieneusi in domestic cats in Brazil. Indeed, E. bieneusi was previously identified through PCR in feces from cats in Asia: China ( KARIM et al., 2014a ; LI et al., 2015 ; XU et al., 2016b ), Japan ( ABE et al., 2009 ), Iran ( JAMSHIDI et al., 2012 ) and Thailand ( MORI et al., 2013 ); Europe: Germany ( DENGJEL et al., 2001 ), Switzerland ( MATHIS et al., 1999 ), Portugal ( LOBO et al., 2006 ) and Poland ( PIEKARSKA et al., 2017 ); and in South America: Colombia ( SANTÍN et al., 2006 ), with prevalence rates varying from 5 to 31.3% in studies involving 40 or more samples. The prevalence rate found in this study was 3.3%. In a study conducted in South America ( SANTÍN et al., 2006 ), 46 cats from 15 days to 10 years of age were euthanized in Colombia and fecal samples were collected directly from the rectum and ileum; eight (17%) animals were considered E. bieneusi positive after molecular analysis.

E. bieneusi DNA has already been identified in fecal samples in Brazil collected from humans ( FENG et al., 2011 ), cattle (FIUZA et al., 2016b), birds (CUNHA et al., 2016 , 2017 ; LALLO et al., 2012 ), pigs ( FIUZA et al., 2015 ) and sheep (FIUZA et al., 2016a). In addition, microsporidium was also detected in a sample of treated effluent water collected in the region of Campinas, São Paulo, demonstrating the significant possibility of dispersion of this agent even after sewage treatment ( YAMASHIRO et al., 2017 ). However, epidemiologic factors and the occurrence of clinical disease in the country are still uncertain and need further clarification.

No clinical symptomatology has been associated with domestic animals in Brazil. In the state of Rio de Janeiro, Fiuza et al. (2016b) compared the feces consistency and body condition score of cattle of different age groups, but were unable to correlate the parameters with the occurrence of E. bieneusi.

In this study, all the fecal samples collected from cats were diarrheic. However, due to the low prevalence rate and the non-comprehensive diagnosis of other parasitic, bacterial and viral etiological agents wich are expected to cause diarrhea, we could not correlate the presence of E. bieneusi with this clinical manifestation. Similarly, Dengjel et al. (2001) , who analyzed fecal samples from 60 diarrheic cats in Germany, found only three samples positive for E. bieneusi. Piekarska et al. (2017) analyzed fecal samples from 44 domestic cats (nine diarrheic) in Poland and found four E. bieneusi positive samples, only one of which was diarrheic. None of these studies was able to correlate the presence of E. bieneusi DNA with diarrhea in the cats.

E. bieneusi genotyping contributes as an essential information to a better knowledge on this microorganism, indicating both possible species-specific genotypes as well as those already found in more than one animal species. Genotypes found in humans and animals are considered zoonotic, even when clinical disease is not evident. The presence of DNA of this organism in feces suggests the presence of infection and the possibility of spore dissemination through feces.

Among more than 200 known E. bieneusi genotypes, 12 are considered specific to cats ( Table 1 ), whereas two others have been reported in cats and other animals ( Table 2 ). Hence, these genotypes are considered non-zoonotic. On the other hand, six genotypes that have been found in cats are considered zoonotic, since they have also been observed in humans ( Table 3 ). Genotypes D and Type IV are of major importance and have been described in several countries in humans and in a wide variety of animal species ( Table 3 ). In this study, both positive cats had the genotype D. This genotype was described in cats for the first time by Mori et al. (2013) in Thailand, where it was detected in 22 out of 25 E. bieneusi positive animals, demonstrating that domestic cats may play an important role in the propagation of zoonotic microsporidiosis caused by this genotype. Since that first description, genotype D has also been identified in cats by Karim et al. (2014a) , Li et al. (2015) and Xu et al. (2016b) , in researches carried out in China. Therefore, this is the first report of genotype D in cats outside the Asian continent. In Brazil, genotype D has already been found in fecal samples from humans ( FENG et al., 2011 ), cattle (FIUZA et al., 2016b) and birds ( CUNHA et al., 2016 , 2017 ), suggesting the possible risk of zoonotic transmission in this country. In a study conducted in birds by Cunha et al. (2016) in the state of Minas Gerais, genotype D was the most prevalent, and was found in 58.3% of analyzed fecal samples from chickens purchased in public markets. In the other single research in cats in the Americas, Santín et al. (2006) , using molecular methods, found 17% of 46 cats tested positive for E. bieneusi in Colombia, and also found four other genotypes (Type IV, WL11, Peru10 and D-like).

Table 1 Enterocytozoon bieneusi genotypes found only in cats.  

Genotype (Synonym) Host Geographic distribution (Reference)
EbfelA Cat Switzerland ( Mathis et al., 1999 )
L Cat Germany ( Dengjel et al. 2001 )
Portugal ( Lobo et al., 2006 )
PtEb III Cat Portugal ( Lobo et al., 2006 )
PtEb IV Cat Portugal ( Lobo et al., 2006 )
D-like Cat Colombia ( Santín et al., 2006 )
ETMK2 Cat Thailand ( Mori et al., 2013 )
ETMK3 Cat Thailand ( Mori et al., 2013 )
ETMK4 Cat Thailand ( Mori et al., 2013 )
CC1 Cat China ( Karim et al., 2014a )
CC2 Cat China ( Karim et al., 2014a )
CC3 Cat China ( Karim et al., 2014a )
eb52 Cat Poland ( Piekarska et al., 2017 )

Table 2 Enterocytozoon bieneusi genotypes found in cats and other hosts.  

Genotype (Synonym) Host Geographic distribution (Reference)
CC4 Cat China ( Karim et al., 2014a )
Cattle China ( Qi et al., 2017 )
PtEb IX Cat China ( Karim et al., 2014a )
Dog Poland ( Piekarska et al., 2017 )
Switzerland ( Mathis et al., 1999 )
Portugal ( Lobo et al., 2006 )
Japan ( Abe et al., 2009 )
Colombia ( Santín et al., 2008 )
United States of America ( Feng et al., 2011 )
China ( Xu et al., 2016b )

Table 3 Enterocytozoon bieneusi genotypes found in cats and humans (and some genotypes also in other hosts).  

Genotype (Synonym) Host Geographic distribution (Reference)
D (PigEBITS 9, WL8, Peru9, CEbC, PTEb VI) Human Cameroon ( Breton et al., 2007 )
Gabon ( Breton et al., 2007 )
Peru ( Bern et al., 2005 ; Cama et al., 2007 ; Sulaiman et al., 2003a )
England ( Sadler et al., 2002 )
Niger, Vietnan ( Espern et al., 2007 )
Nigeria ( Akinbo et al., 2012 ; Ayinmode et al., 2011 ; Maikai et al., 2012 )
Malawi, Netherlands ( ten Hove et al., 2009 )
Iran ( Agholi et al., 2013a ; Agholi et al., 2013b )
Thailand ( Leelayoova et al., 2006 ; Prasertbun et al., 2017 ; Saksirisampant et al., 2009 )
Russia ( Sokolova et al., 2011 )
Congo ( Wumba et al., 2012 )
China ( Wang et al., 2013a , b )
Portugal ( Lobo et al., 2012 )
Tunisia ( Chabchoub et al., 2012 )
Poland ( Kicia et al., 2014 )
India ( Li et al., 2013 )
Democratic Republic of São Tomé and Príncipe ( Lobo et al., 2014 )
Brazil ( Feng et al., 2011 )
Spain ( Galván et al., 2011 )
Cat China ( Karim et al., 2014a ; Li et al., 2015 ; Xu et al., 2016b )
Thailand ( Mori et al., 2013 )
Brazil (this study)
Wild boar Czech Republic ( Němejc et al., 2014 )
Slovak Republic ( Němejc et al., 2014 )
Pig United States of America ( Buckholt et al., 2002 )
Japan ( Abe and Kimata, 2010 )
Thailand ( Prasertbun et al., 2017 )
China ( Li et al., 2014a ; Zhao et al., 2014b )
Czech Republic ( Sak et al., 2008 )
Cattle South Africa (Abu Samra et al., 2012 )
China ( Li et al., 2016a ; Qi et al., 2017 ; Zhao et al., 2015c )
Argentina ( Del Coco et al., 2014 )
Brazil (Fiuza et al., 2016b)
Korea ( Lee 2007 , 2008 )
Sheep China ( Zhao et al., 2015b )
Goat China ( Shi et al., 2016 ; Zhao et al., 2015b )
Takin China ( Zhao et al., 2015a )
Beaver United States of America ( Sulaiman et al., 2003b )
Fox United States of America ( Sulaiman et al., 2003b )
Spain ( Galván-Díaz et al., 2014 )
China ( Yang et al., 2015 ; Zhao et al., 2015d )
Muskrat United States of America ( Sulaiman et al., 2003b )
Northern raccoon China ( Li et al., 2016b )
River otter United States of America ( Guo et al., 2014 )
Raccoon United States of America ( Sulaiman et al., 2003b )
China ( Xu et al., 2016a ; Yang et al., 2015 ; Zhao et al., 2015d )
Falcon Abu Dhabi (Muller et al., 2008)
Rabbit Spain ( Galván-Díaz et al., 2014 )
Horse Czech Republic (Wagnerova et al., 2012)
Algeria ( Laatamna et al., 2015 )
China ( Qi et al., 2016 )
Colombia ( Santín et al., 2010 )
African lion China ( Li et al., 2016b )
Asian golden cat China ( Li et al., 2016b )
Dog Portugal ( Lobo et al., 2006 )
China ( Karim et al., 2014a ; Xu et al., 2016b )
Pigeon Iran ( Pirestani et al., 2013 )
Mice Czech Republic ( Sak et al., 2011 )
Germany ( Sak et al., 2011 )
Birds Brazil ( Cunha et al., 2016 , 2017 )
Northern white cheeked gibbon China ( Li et al., 2016b )
Golden snub-nosed monkey China ( Li et al., 2016b )
Olive baboon China ( Li et al., 2016b )
Primate China ( Karim et al., 2015 ; Karim et al. 2014b , c )
Baboon Kenya ( Li et al., 2011 )
Macaque United States of America ( Chalifoux et al., 2000 )
China ( Ye et al., 2014 )
Type IV (K, Peru2, BEB5, CMITS1, BEB-var, PtEB III) Human Cameroon ( Breton et al., 2007 ; Sarfati et al., 2006 )
Gabon ( Breton et al., 2007 )
Peru ( Bern et al., 2005 ; Cama et al., 2007 ; Sulaiman et al., 2003a )
England ( Sadler et al., 2002 )
Uganda ( Tumwine et al., 2002 )
Niger ( Espern et al., 2007 )
Iran ( Agholi et al., 2013a )
China ( Wang et al., 2013b )
Nigeria ( Akinbo et al., 2012 ; Ayinmode et al., 2011 ; Maikai et al., 2012 )
Portugal ( Lobo et al., 2012 )
France (Liguory et al., 1998 , 2001 )
Democratic Republic of São Tomé and Príncipe ( Lobo et al., 2014 )
Malawi ( ten Hove et al., 2009 )
Netherland ( ten Hove et al., 2009 )
Cat Germany ( Dengjel et al., 2001 )
Portugal ( Lobo et al., 2006 )
China ( Li et al., 2015 ; Xu et al., 2016b )
Japan ( Abe et al., 2009 )
Colombia ( Santín et al., 2006 )
Cattle United States of America ( Santín et al., 2012 ; Sulaiman et al., 2004 )
Korea ( Lee, 2008 )
Chipmunk United States of America ( Guo et al., 2014 )
Woodchuck United States of America ( Guo et al., 2014 )
Meadow vole United States of America ( Guo et al., 2014 )
Squirrel United States of America ( Guo et al., 2014 )
Black bear United States of America ( Guo et al., 2014 )
Primate China ( Karim et al. 2014b , c )
Ostriches Spain ( Galván-Díaz et al., 2014 )
Birds Brazil ( Cunha et al., 2016 )
Snake China ( Karim et al., 2014d )
Monkey China ( Karim et al., 2015 )
Rhesus monkeys China ( Ye et al., 2012 )
Dog China ( Karim et al., 2014a )
Colombia ( Santín et al., 2008 )
I (BEB2, CEbE) Human China ( Zhang et al., 2011 )
Cat China ( Karim et al., 2014a )
Cattle Germany ( Dengjel et al., 2001 ; Rinder et al., 2000 )
Czech Republic ( Juránková et al., 2013 )
Korea ( Lee, 2007 , 2008 )
China ( Jiang et al., 2015 ; Li et al., 2016a ; Ma et al., 2015b ; Qi et al., 2017 ; Zhang et al., 2011 ; Zhao et al., 2015c )
Argentina ( Del Coco et al., 2014 )
Brazil (Fiuza et al., 2016b)
South Africa (Abu Samra et al., 2012 )
United States of America ( Fayer et al. 2007 , 2012 ; Santín et al., 2012 ; Santín and Fayer, 2009 ; Santín et al., 2005 ; Sulaiman et al., 2004 )
Algeria ( Baroudi et al., 2017 )
Primate China ( Karim et al., 2014b )
White tailed deer United States of America ( Santín and Fayer, 2015 )
Yak China ( Ma et al., 2015a )
Pig Spain ( Galván-Díaz et al., 2014 )
BEB6 (SH5) Human China ( Wang et al., 2013b )
Cat China ( Karim et al., 2014a )
Sheep Brazil (Fiuza et al., 2016a)
China ( Jiang et al., 2015 ; Li et al., 2014b ; Shi et al., 2016 ; Ye et al., 2015 ; Zhao et al., 2015b )
Sweden ( Stensvold et al., 2014 )
Cattle United States of America ( Fayer et al., 2007 )
Hog deer China ( Li et al., 2016b )
Alpaca China ( Li et al., 2016b )
Sika deer China ( Li et al., 2016b ; Zhao et al., 2014a )
Red deer China ( Li et al., 2016b )
Primate China (Karim et al., 2014B, 2015)
Horse China ( Qi et al., 2016 )
Goat Peru ( Feng et al., 2011 )
China ( Shi et al., 2016 ; Ye et al., 2015 ; Zhao et al., 2015b )
Peru10 Human Peru ( Bern et al., 2005 ; Cama et al., 2007 ; Sulaiman et al., 2003a )
Cat Colombia ( Santín et al., 2006 )
WL11 (Peru5) Human Peru ( Bern et al., 2005 ; Cama et al., 2007 ; Sulaiman et al., 2003a )
Cat Colombia ( Santín et al. 2006 )
Dog Colombia ( Santín et al. 2008 )
Fox United States ( Sulaiman et al. 2003b )

Our findings reveal the presence of E. bieneusi infection by a zoonotic genotype in domestic cats in Brazil. Cats, along with dogs, are the most common companion pets that live inside homes around the world, in very close contact with humans of all ages and health conditions. The detection of a zoonotic genotype emphasizes the risk of human infection, since cats can contribute to the direct and indirect transmission of this parasite through the contamination of water and food with feces containing E. bieneusi spores. This study imputes cats as potential dispersing agents of zoonotic genotype D in Brazil. However, further studies should be carried out to confirm this hypothesis.

Knowledge about and identification of possible pathogenic agents transmitted by these animals is of major public health importance, especially to immunocompromised patients. Thus, to gain a better understanding of the zoonotic transmission of E. bieneusi in Brazil, new epidemiological investigations on cats and other animals are needed, as well as simultaneous studies on animals and humans living together in the same house.

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Received: September 06, 2018; Accepted: December 10, 2018

* Corresponding author: Carlos Alberto do Nascimento Ramos. Faculdade de Medicina Veterinária e Zootecnia, Universidade Federal de Mato Grosso do Sul – UFMS, Av. Senador Filinto Muller, 2443, CEP 79074-460, Campo Grande, MS, Brasil. e-mail: carlos.nascimento@ufms.br

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