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SALMONELLA SPP. VIRULENT AND RESISTANT MULTIDRUG

RECOVERED FROM CHICKEN CARCASSES IN BRAZIL

ORIGINAL ARTICLE

MELO, Nataly Sayonara da Silva1, SILVA Maria Goretti Varejão da2, ALMEIDA,
Anna Carolina Soares3, MEDEIROS, Anna Karolyne de Araujo4, SILVA, Daniel Dias
da5, SOUZA, Paula Mariana Salgueiro de6, SILVA, Marcela Oliveira da7,
SOARES Anísio Francisco8, MENDONÇA, Marcelo9, MEDEIROS, Elizabeth
Sampaio de10

MELO, Nataly Sayonara da Silva, et al. Salmonella spp. virulent and resistant
multidrug recovered from chicken carcasses in Brazil. Revista Científica
Multidisciplinar Núcleo do Conhecimento. Year. 08, Ed. 04, Vol. 01, pp. 92-114. April
2023. ISSN: 2448-0959, Access link:
https://www.nucleodoconhecimento.com.br/biology/salmonella-spp, DOI:
10.32749/nucleodoconhecimento.com.br/biology/salmonella-spp

ABSTRACT

The aim of this study was to evaluate the biofilm production, the susceptibility profile
and the detection of resistance genes present in Salmonella spp isolates from fresh
chicken carcasses sold in a Brazilian metropolis. From a total of 61 samples of fresh
poultry carcasses, 21 were positive for the presence of Salmonella spp. Regarding
the antimicrobial susceptibility test, (13/21) isolates tested were resistant to at least
one antibiotic, corresponding to 61.9%, and 38% (08/21) were Resistant to Multiple
Drugs. At least two resistance genes were identified in all isolates, especially the
genes related to β-lactamases and Quinolones resistance. It was also observed that
some Salmonella spp isolates showed identical genetic patterns. And all 21 isolates
were able to form biofilm. The identification of Salmonella spp. biofilm forming and
carrying different β-lactamase genes and determinants of resistance to quinolones
demonstrates the capacity of these bacteria to accumulate various mechanisms of
virulence and resistance to antimicrobials. Therefore, the spread of different clonal
groups of Salmonella spp. MDR in poultry meat carcasses expressed in this attest
to the need for effective controls to contain this microorganism, which besides being
a risk to public health, is also responsible for considerable economic losses.

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Keyword: Beta-lactams, Food poisoning, PCR, Public market.

INTRODUCTION

Salmonellosis is a foodborne disease caused by pathogenic Salmonella spp strains.

Cases of Salmonellosis in humans occur mainly through the consumption of
contaminated food or water. In most cases, food of animal origin, especially those
from poultry, are the major sources of Salmonella spp. infections. The symptoms of
the enteric infection are nausea, vomit, non-bloody diarrhea, fever, cold, abdominal
pain, myalgia and headaches, and in immunodepressed patients it can lead to
bacteremia, endocarditis, and death (GRIMONT and WEILL, 2007).

According to the Centres for diseases, control and prevention (CDC), 1.2 million
cases of infections, 23.000 hospitalizations, and 450 deaths per year in the United
States of America are caused by Salmonella spp, approximately. And the infections
related to the ingestion of contaminated food represents 1.0 million of the cases,
approximately (CDC, 2020). In Brazil, according to the Ministry of Health, a total of
12.660 cases of foodborne illness was reported between 2000 and 2017, and
Salmonella spp. was one of the major agents reported in these cases, which
represents a total of 35% of the cases reported (BRASIL, 2019).

In most salmonellosis cases, healthy individuals do not need treatment. However,

immunodepressed patients need to go through treatment (SERENO et al., 2017).
Nevertheless, the indiscriminate use of antimicrobials, especially in animal
production has led to an increased number of microorganisms resistant to
therapeutic agents, leading to a limited number of antimicrobial options, which can
result in treatment failures (ALEKSHUN and LEVY, 2007; PENG et al., 2014). Over
the years, there has been an increase in the prevalence of Salmonella strains
multiple drugs resistant, mainly in poultry products, such as poultry meat
(AZEVEDO, 2014; BAPTISTA et al., 2018; DUARTE et al., 2009; FITCH et al., 2016;

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BONI et al., 2011; REZENDE et al., 2005; RIBEIRO et al., 2007; THRELFALL,
2002).

Therefore, the emergence of multidrug-resistant Salmonella (MDR) is a worldwide

concern, due to the increased hospitalization rates and death. This phenomenon is
a consequence of the extensive use of antibiotics by humans, and also in animal
production.

Moreover, Salmonella species have the ability to form biofilm, where cells
microorganisms are embedded in an extracellular matrix, so these microorganisms
can adhere to biotic or abiotic surfaces (DAVEY and O’TOOLE, 2000; FLEMMING
et al., 2016). The complex matrices of the biofilm keep the microbial cells protected
from the action of sanitation process and antimicrobial agents, therefore, when
pathogenic microorganisms are involved in the biofilm, there is a huge risk to
contaminate the food, which leads to a public health problem. (KASNOWSKY et al.,
2010).

Hence, the aim of this study was to characterize the determinants of antibiotic
resistance, and to evaluate the production of biofilm in Salmonella spp. strains
recovered from fresh poultry meat sold in a Brazilian metropolis.

METHODS

Sampling and identification of the poultry carcasses

A total of 61 poultry meat carcasses were purchased from 07 different public markets
in the city of Recife in the state of Pernambuco, Brazil, between 2018 to 2019 (figure
1 and table 1). The samples were sent to the Meat and Milk Inspection Laboratory
(LICAL), of the Department of Veterinary Medicine in the Federal Rural University of
Pernambuco (UFRPE).

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At the laboratory, the surface of each poultry carcasses pack was wiped with 70
percent alcohol. Then, 25g of the carcases were randomly taken and placed in
individual sterile stomacher bags with 225 ml of Buffered Peptone Water (Kasvi,
Brazil), and homogenized in stomacher for 2 min (Kasvi, Brazil) and incubated at 37
°C for 24 hours for the pre-enrichment stage. For the enrichment stage, 0.1 ml of the
pre-enriched broth was transferred into 10 ml of Tetrathionate broth (Merck e pais)
and then incubated at 41.5 °C for 24 hours, and 1.0 ml of the pre-enriched broth was
also transferred into 10 ml of Rappaport and incubated at 37 °C for 24 hours for
selective enrichment. After the incubation, one loopful of the TT broth and Rappaport
cultures were streaked onto Xylose Lysine Agar (XLD) (Kasvi, Brazil) and Hektoen
Enteric Agar (HE) (Kasvi, Brazil) plates and incubated at 37 °C for 24h. Three
presumptive Salmonella colonies on the plates were selected and streaked onto
Nutrient agar (Merck, pais-) and incubated at 37.8 °C for 24 hours. Then, colonies
from the Nutrient agar were submitted to biochemical and serological tests (ISO,
657912017).

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Figure 1: Public markets where the samples were acquired

Source: Google Earth.

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Table 1: Number of samples acquired in different public markets in the city of Recife – Pernambuco,
Brazil

Public Market Samples acquired

A 1, 2, 3 22, 23, 24, 25, 26
B 4, 5, 6, 7, 8, 9, 27, 28, 29
C 30, 31, 32
D 10, 33, 34, 35, 36,
E 11, 37, 38, 39, 40, 41
F 12, 13, 14, 15, 16, 17, 18, 45, 46,47, 48, 49, 50, 51, 52, 53, 54, 55, 56, 57, 58, 59,
60, 61
G 18, 20, 21, 42, 43, 44

Source: Authors.

Susceptibility profile to antimicrobials

The susceptibility profile test was done by the agar disc-diffusion method with the
following antimicrobial agents: ampicillin, chloramphenicol, ciprofloxacin,
ceftriaxone, sulfamethoxazole-trimethoprim, imipenem, amoxicillin-clavulanic acid,
ceftazidime, cefotaxime and aztreonam, according to the Clinical and Laboratory
Standards Institute (CLSI) (CLSI, 2018).

Detection of resistance genes

The DNA used in the molecular analyses was obtained from bacterial suspensions
made up of fresh colonies, which were previously grown for 16-18 hours in Luria
Bertani agar and inoculated in approximately 300 μL ultrapure water free of nuclease
homogenized with the aid of a vortex tube shaker (Vision Scientific).

The investigation of genes to β-lactams and quinolones resistance was performed

by PCR. The thermal cycling conditions were those described by the authors listed
in the primer table.

Table 2: Primers used to detect the β-lactamases genes

Primer 5’ 3’ Sequences Target Gene Product References

KPC F TGTCACTGTATCGCCGTC blaKPC 1011pb (Bratu et al., 2005)
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R CTCAGTGCTCTACAGAAAACC
CTX- F SCSATGTGCAGYACCAGTAA blaCTXM 500pb (Cao et al., 2002)
M R CCGCRATATGRTTGGTGGTG
TEM F TCGGGGAAATGTGCGCG blaTEM 700pb
R TGCTTAATCAGTGAGGCACC
SHV F TTATCTCCCTGTTAGCCACC blaSHV 900pb
R GATTTGCTGATTTCGCTCGG
R AAGCAGACTTGACCTGA
qnrA F AGA GGA TTT CTC ACG CCA GG qnrA 580pb (Cattoir et al.,
2007).
R TGC CAG GCA CAG ATC TTG AC
qnrB F GGM ATH GAA ATT CGC CAC T qnrB 264pb
R TTT GCY GYY CGC CAG TCG AA
qnrC F GGG TTG TAC ATT TAT TGA ATC qnrC 447pb (Wang et al., 2009)
R TCC ACT TTA CGA GGT TCT
qnrD F CGA GAT CAA TTT ACG GGG AAT A qnrD 582pb (Cavaco et al.,
2009).

Source: Authors.

Analysis of the genetic profile of the isolates

The comparison and identification of genetic variations in the content of bacterial

strains was performed by ERIC-PCR. The primers used for the reaction were ERIC-
1R (5' ATGTAAGCTCCTGGGGATTCAC-3') and ERIC2
(5'AAGTAAGTGACTGGGGGGGCCG-3') (Sigma Aldrich) according to
(VERSALOVIC et al., 1991), with modification described by (FENDRI et al., 2013).

Biofilm production capacity

The biofilm forming capacity was evaluated according to the methodology proposed
by (STEPANOVIĆ et al., 2000; STEPANOVIĆ et al., 2007). Each strain was diluted
to 108CFU/mL (0.5 in the MacFarland scale) using Trypticase Soy Broth (TSB)
(Merck), and 200μL were cultured in three wells of the 96-well flat-bottom
polystyrene microplate (Nest®). A total of 69 wells were used to test 21 strains; the
other 3 wells received the Salmonella Typhimurim ATCC 14028 as positive control,
and 3 wells received the negative control (non-inoculated culture medium). The
plates containing Salmonella spp. strains and controls were incubated at 35ºC for
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96 hours. The plate was washed three times with phosphate buffered saline (PBS
pH 7.2) and stained with crystal violet at 1% for 15 minutes. After washing three
times with distilled water and drying at room temperature, absorbance was read in a
Polaris (Celer®) microplate reader at 492 nm wavelength (SERENO et al., 2017).

The optical density (OD) of each Salmonella spp. strain was obtained by the
arithmetic mean of the absorbance of three wells and this value was compared with
the mean absorbance of negative controls (ODnc). After that, the strains were
classified in no biofilm producer (OD≤ODnc); weak biofilm producer
(ODnc<ODs≤2.ODnc); moderate biofilm producer (2.ODnc<ODs≤4.ODnc); and
strong biofilm production (4.ODnc<ODs) classification given according to
(STEPANOVIĆ et al., 200; STEPANOVIĆ et al., 2007).

RESULTS

Prevalence of Salmonella spp. in poultry meat carcass samples

From the 61 samples of poultry meat carcasses collected in the public markets, 34%
(21) were contaminated by Salmonella spp. The prevalence of Salmonella spp. on
each public market is expressed in figure 3, and the data is detailed in table 3.

Figure 2: Prevalence of Salmonella spp. isolates from each public market in the city of Recife –
Pernambuco, Brazil

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Source: Authors.

Table 3: Salmonella spp. isolates from each public market in the city of Recife – Pernambuco, Brazil

Isolates Public market Year

1 A 2018
2 2019
3 2019
4 B 2018
5 2018
6 2018
7 2018
8 2018
9 2018
10 D 2019
11 E 2019
12 F 2019
13 2019
14 2019
15 2019
16 2019
17 2019
18 2019
19 G 2018
20 2019
21 2019

Source: Authors.
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Figure 3: Antimicrobial resistance to individual antimicrobial agents among Salmonella spp. isolates
from poultry carcasses sold in public markets in the city of Recife – Brazil

Source: Authors.

Susceptibility perfil

From the 21 isolates, 13 (61,9%) were resistant to at least one antimicrobial agent.
The antimicrobial resistance to individual antimicrobial agents among Salmonella
isolates is expressed in figure.3. The detailed data from the antimicrobial
susceptibility test is expressed in table 4.

Table 4. Antimicrobial susceptibility profile of Salmonella spp. isolates from chicken carcasses
acquired in public markets in the city of Recife - PE, between 2018 and 2019

Isolate AMP AMC CRO CTX CAZ IPM ATM CLO CIP SUT
1 R S R S S S S S R R
2 S S S S S S S S I S
3 S S S S S S S S R R
4 R S I S S S S S S S
5 S S S S S S S S I S
6 S S I S S S S S R S
7 S S I S S S S S I S

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8 S S S S S S S S R S
9 S S I S S S S S I S
10 S S S S S S S S I S
11 S S S S S S S S I S
12 R S R S S S S S I R
13 R S R S S S S S I R
14 S S S S S S S S I S
15 R S R S S S S R S R
16 R S R S S S S R S R
17 R S R S S S S R S R
18 R S R S S S S S S R
19 S S S S S S S S S S
20 R S R S S S S S S R
21 R S R R S S S S R R

AMP - Ampicillin, CLO - Chloramphenicol, CIP - Ciprofloxacin, CRO- Ceftriaxone, SUT -

Sulfamethoxazole-trimethoprim, IPM - Imipenem, AMC - amoxicillin-clavulanic acid, CAZ -
Ceftazidime, CTX- Cefotaxime and ATM - Aztreonam, S – Sensitive; R- Resistant; I-. Intermediate.
Source: Authors.

At least two resistance genes were identified in all isolates, among which the
presence of resistance genes encoding β-lactamases (bla) and resistance genes
encoding quinolones (qnr) were observed in the molecular tests carried out in the
present study, and the results are detailed in table 3.

Table 5: Resistance genes detected in each Salmonella spp isolate, recovered from poultry carcasses
acquired in public markets in the city of Recife - Pernambuco between the years 2018 and 2019

β-lactams resistant Quinolones resistants

Isolates BlaTEM-like BlaSHV- BlaCTX-M- BlaKPC-2 qnrA qnrB qnrC qnrD
like like
1 + - - - + + - -
2 + - - - + + - -
3 + - - - + + - +
4 + - - - + + - -
5 + - - - + + - +
6 + - - - + + - +
7 + - - - + + - +
8 + - - - + + - +
9 + - - - + + - +
10 + - + - - + - -
11 + - - - - + - -
12 + - + - - + - -
13 + - + - - + - -
14 + - + - - + - -
15 + - + - - + - -
16 + - + - - + - +
17 - - + - - + - +

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18 + - + - - + - +
19 + - - - - + - +
20 + - - - - + - +
21 + - - - + + - +

Source: Authors.

Clonal relationship

The isolates showed a pattern ranging from 3 to 9 strips, which revealed the
presence of different genotypes pattern indistinguishable from each other and others
whose standard is different for only one or two bands. Some isolates of Salmonella
spp. showed identical genetic patterns (2, 3, 4, 5, 6 and 7). Samples 9, 11, 19, 20
and 21 were closely related genetically, as they have a similar pattern of strips,
differing only in one (9, 21) or two strips (11 and 20).

Biofilm forming

All the 21 Salmonella spp. isolates tested were biofilm producers, and these isolates
were classified as weak biofilm producers according to (STEPANOVIĆ et al., 2000;
STEPANOVIĆ et al., 2007).

DISCUSSION

This work identified Salmonella spp. contaminating chicken carcasses sold in public
markets in a Brazilian metropolis. In addition, we detected the resistance
mechanisms present in these bacterial isolates and confirmed that they were all
biofilm producers. The results that are presented here showed several isolates with
a genetic proximity and revealed that the others are clones.

Isolates 2, 3, 4 and 5 have an identical genetic profile, although they were collected
in two different markets, Market A and Market B, which are about 5 km apart from
each other. This finding indicates that the sellers may have the same supplier, where
the contamination by Salmonella MDR started. Market F presented a greater number
of strains characterised as clones (12, 14, 15, 16 and 18). In addition to the possibility
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of the same supplier, according to a set of failures in hygienic conditions, such as

the exposure of products to dust and insects and the inappropriate sharing of utensils
such as knives and containers between traders, they can contribute to the
contamination of the carcasses, which results in the dissemination of isogenic
isolates (AZEVEDO, 2014).

The presence of Salmonella spp. in poultry meat was also observed in the studies
done by (BAPTISTA et al., 2018; MELO et al., 2020; YIN et al., 2021). However, our
findings differ from these studies due to the higher prevalence of Salmonella spp
isolates.

The contamination by Salmonella spp. detected in the samples may have been due
to previous contamination in the slaughterhouse itself, because of failures in the
process of slaughtering (LOPES et al., 2007; VON RÜCKERT et al., 2009). It was
also observed that traders removed the carcasses from the original packaging and
placed them in plastic bowls and later sold them at room temperature (88 ºF), which
is considered a fraud. This temperature promotes the multiplication of Salmonella
spp., as these microorganisms can multiply at temperatures around 5°C to 45°C
(MAHMOUD, 2012) This problem related to the temperature was also noticed in the
studies done by (KHAN et al., 2018; JARQUIN et al., 2015).

Therefore, this practice increases the risk of product contamination, mainly due to
inadequate handling practices and inadequate sanitary hygienic conditions and to
what is observed in these public markets, as it was found that tables and benches
were not cleaned in 59% (36/61) of the places. Regarding the handlers, it was
observed that 100% did not have their nails well cut and clean. In addition, the same
employee who took care of the meat was the same one in the checkout counter.
Consequently, these flaws in the processes of good handling practices observed in
these markets can contribute to the contamination and spread of Salmonella spp. in
this product. This transference can occur between various interactions between

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man, food and the environment. Therefore, cross-contamination is the basis for the
spread of Salmonella spp.

From the results from the susceptibility test against antimicrobials agents in the
present study, it was observed that 38% (08/21) of the Salmonella spp strains were
Resistant to Multiple Drugs (MDR), that is, bacteria that are resistant to at least three
classes of antimicrobial agents (MAGIORAKOS et al., 2011).

The occurrence of Salmonella spp strains resistant to multiple antimicrobials in

poultry meat in Brazil is a growing reality, due to the data reported in the present
study, and other researches done by (ZIECH, 2015; BAPTISTA et al., 2018). It might
happen because of the intensive use of antimicrobial agents in the animal production
to treat the animals, and also to improve the production.

The greatest implication regarding the dissemination of multidrug resistant zoonotic

strains is related to therapeutic failures in the face of several conditions, both in
human and animal cases. In addition, this reality leads to losses in animal herds,
since when present, these resistant strains are difficult to eliminate. The permanence
of pathogenic and multidrug resistant strains in the poultry production is even more
worrying, since the animal density is higher, and consequently, there is a greater
spread of the microorganisms in a shorter period of time.

It was observed that only 4.28% (03/21) of the isolates were resistant to
Chloramphenicol. This result may reflect the ban on the use of this agent as a
therapeutic agent and growth promoter in animal production in Brazil (PACHECO-
SILVA et al., 2014).

On the other hand, 42.85% (09/21) of the isolates were resistant to Ceftriaxone, 3rd
generation cephalosporin. The use of this drug in animal production is prohibited in
Brazil (MION et al., 2014). Therefore, this result indicates that this drug or others
from the same antimicrobial class is still being used in animal production in Brazil.

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In addition, 42.85 (9/21) of the isolates were resistant to three or more antimicrobial
drugs. Then, when comparing the resistant profile with the markets, it was noticed
that isolates number 13, 15, 16, 17, 18, which were resistant to up to three drugs
were from the same public market (public market F). It suggests that there may have
been cross contamination at the market, or that these chicken carcasses may have
suffered previous contamination in the poultry slaughterhouse.

Hence, the occurrence of Salmonella MDR strains in food animal origin is increasing
in Brazil (BAPTISTA et al., 2018; MELO et al., 2020; VOSS-RECH et al., 2015).
Infections related to multidrug resistant strains are associated with high morbidity
and mortality, compared to the sensitive ones, since these microorganisms
represent a barrier in the treatment of human and animal diseases.

The presence of such resistance genes detected in Salmonella spp. isolates from
food of animal origin represents a serious threat to public health, since the horizontal
transmission of resistance genes occurs mainly by plasmids encoding β-lactamases
(GYLES, 2008). In addition, these genes are considered from community origin, and
are common in hospital environments (SUN et al., 2013). Thus, the dissemination of
resistant strains points out the importance of the Salmonella spp control in poultry
meat (BORGES et al., 2019; SIVASANKAR et al., 2020).

The presence of biofilm-forming strains of Salmonella spp. observed in the present

study points out the risk that this finding may bring to the food industry and the public
health. The ability to form biofilm protected the microorganisms inside the biofilm,
and thus less susceptible to external factors, such as the action of antimicrobial
agents (ZIECH, 2015; SERENO et al., 2017; BORGES et al., 2018).

In addition, biofilms promote the permanence of pathogenic and spoilage

microorganisms, which cause illnesses to consumers, and the depreciation of the
final product due to physical-chemical and sensory changes (KASNOWSKY et al.,
2010; SINGH et al., 2017).

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Finally, this investigation showed that the identification of Salmonella spp. producer
of biofilm and carrying different β-lactamase genes and determinants of resistance
to quinolones demonstrates the ability of these bacteria to accumulate various
mechanisms of virulence and resistance to antimicrobials. The selective pressure is
exerted by the indiscriminate use of antibiotics in agriculture is an important factor
for the acquisition of different mechanisms of resistance and dissemination of these
strains. Furthermore, the spread of different clonal groups of Salmonella spp. MDR,
in chicken carcasses, shown in this study attests to the need for effective controls to
contain this microorganism, which besides being a risk to public health, is also
responsible for considerable economic losses.

FINANCIAL SUPPORT

The authors thank the Coordenação de Aperfeiçoamento de Pessoal de Nível

Superior (CAPES) for the scholarship provided.

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Sent: March 27, 2023.

Approved: April 08, 2023.

1 Doctoral student of the Graduate Program in Animal Bioscience. ORCID: 0000-0003-0698-6125.

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2 Doctoral student of the Graduate Program in Animal Bioscience. ORCID: 0000-0001-9410-7631.

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3 PhD in Genetics. ORCID: 0000-0003-0698-6125. CURRÍCULO LATTES:

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4 Graduate in Veterinary Medicine. ORCID: 0000-0001-9273-5204. CURRÍCULO LATTES:

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LATTES: http://lattes.cnpq.br/6281410502740086.
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8 PhD in Biochemistry and Physiology, Master in Physiology, Biologist. ORCID: 0000-0003-1493-

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9 Doctor. ORCID: 0000-0002-1993-0350.
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