Antimicrobial susceptibility of Staphylococcus sp. and Escherichia coli isolated from captive Amazonian manatee (Trichechus inunguis)

Isolamento e sensibilidade antimicrobiana de Staphylococcus sp. e Escherichia coli de peixe-boi-da-amazônia (Trichechus inunguis) em cativeiro

ABSTRACT:

The Amazonian manatee (Trichechusinunguis) is an aquatic mammal threatened with extinction. However, few studies have investigated the pathogens in this species, which may affect both animal and human health. This study aimed to evaluate the frequency, distribution, and patterns of antimicrobial susceptibility of Staphylococcus spp. and Escherichiacoli colonizing the nasal and rectal cavities of Amazonian manatees kept in captivity at the National Institute for Amazonian Research (INPA) in the state of Amazonas, Brazil. Rectal and nasal swabs from 44 manatees of different ages were used in this study. The genus Staphylococcus was isolated from the nasal swabs of 32 (72.7%) animals, with two individuals harboring more than one species of Staphylococcus. S. sciuri was the most commonly isolated species. Resistance to penicillin was observed in 13 (40.6%) isolates, more frequent than the other antimicrobials tested (P = 0.01). E. coli was isolated from the rectal swabs of all animals, with phylogroup B1 being the most frequent among the strains obtained (P = 0.0008). Four isolates (6.8%) were positive for virulence factors, three of which were classified as enterotoxigenicE. coli (ETEC) and one as enteropathogenicE. coli (EPEC). To our knowledge, this is the first study to evaluate Staphylococcus spp. and E. coli in Amazonian manatee samples. This study revealed nasal colonization by Staphylococcus spp., mainly S. sciuri, and diarrheagenicE. coli isolates, including antimicrobial-resistant strains.

Key words:
Enterobacteriaceae; Trichechidae; Manatins

RESUMO:

O peixe-boi amazônico (Trichechus inunguis) é um mamífero aquático ameaçado de extinção. Apesar disso, poucos estudos investigaram patógenos nessa espécie que podem impactar a saúde animal e humana. O objetivo deste estudo foi avaliar a frequência, distribuição e padrões de suscetibilidade antimicrobiana de Staphylococcus sp. e Escherichia coli pertencentes à microbiota nasal e retal de peixes-bois da Amazônia mantidos em cativeiro no Instituto Nacional de Pesquisas da Amazônia (INPA) (Amazonas, Brasil). Foram utilizados suabes retais e nasais de 44 peixes-boi de diferentes idades. O gênero Staphylococcus foi isolado do swab nasal de 32 (72,7%) animais, sendo que dois indivíduos apresentaram mais de uma espécie de Staphylococcus. S. sciuri foi a espécie mais comumente isolada. A resistência à penicilina foi observada em 13 (40,6%) isolados, sendo mais frequente do que os outros antimicrobianos testados (P = 0,01). Escherichia coli foi isolada dos suabes retais de todos os animais, sendo o filogrupo B1 o mais frequente entre as cepas obtidas (P = 0,0008). Quatro isolados (6,8%) foram positivos para fatores de virulência, três dos quais foram classificados como E. coli enterotoxigênica (ETEC) e um isolado como E. coli enteropatogênica (EPEC). Este é o primeiro estudo a avaliar Staphylococcus spp. e E. coli de amostras de peixe-boi da Amazônia. O estudo revelou colonização nasal por Staphylococcus sp., principalmente S. sciuri, e por isolados diarreiogênicos de E. coli, incluindo cepas resistentes a antimicrobianos.

Palavras-chave:
Enterobacteriaceae; Trichechidae; peixe-boi

INTRODUCTION:

Manatees (Trichechus spp.) are aquatic mammals classified as “vulnerable” by the International Union for Conservation of Nature (IUCN) (MARMONTEL et al., 2016). There are two species of the manatee in Brazil, the American manatee (T. manatus) and the Amazonian manatee (T. inunguis), both of which are threatened by hunting, accidental capture, and destruction of their natural habitats (BARRETO et al., 2021; CABALLERO et al., 2021; SIDRIM et al., 2015). To reduce the impact of these threats, orphaned American manatee calves, victims of poaching, or those accidentally caught in fishing nets were rescued at various locations in Amazonas State (Brazil) and rehabilitated at the National Institute for Amazonian Research (INPA). These animals remain in captivity for up to 10 years until they meet the requirements for release back into the wild.

Staphylococci are gram-positive, coccoid bacteria that are commensals of several species, but they can also be the cause of a wide variety of diseases in animals and humans (LISOWSKA-ŁYSIAK et al., 2021; SANTANA et al., 2022a; WALTHER et al., 2017; WIELER et al., 2011). There is little knowledge about the species of Staphylococcus that colonize animals of wild species, with most studies being case reports of infection (GARCÊS et al., 2019; LUZZAGO et al., 2014; SAHIN-TÓTH et al., 2022).

Escherichia coli is also a commensal bacterial agent in humans and animals, but it can cause a range of conditions, from mild enteric conditions to infections in various organs and potentially fatal sepsis (ALFURAIJI et al., 2022; KOLENDA et al., 2015; SONG et al., 2022). Some animals also act as carriers of E. coli potentially pathogenic to humans (ABREHAM et al., 2019; KOLODZIEJEK et al., 2022; PIÉRARD et al., 2012); however, the role of wild animals as reservoirs of E. coli and its relevance to public health is still not well understood (MERKER BREYER et al., 2022; TORRES et al., 2022).

In addition to the pathogenic potential of E. coli and Staphylococcus bacteria, there is increasing concern regarding their potential for antimicrobial resistance in humans and animals (AWORH et al., 2021; RASMI et al., 2022; RAUBER et al., 2016; VIEGAS et al., 2022). Evidence shows that wild animals can act as reservoirs and disseminators of resistant microorganisms (BESSALAH et al., 2021; ROTH et al., 2019; SUAY-GARCÍA et al., 2019).

Therefore, this study aimed to evaluate the frequency, distribution, and patterns of antimicrobial susceptibility of E. coli and Staphylococcus spp. found in the nasal and rectal cavities of Amazonian manatees held in captivity at the INPA, Amazonas, Brazil.

MATERIALS AND METHODS:

Samples

A one-year study was conducted using non-probability sampling, where all available animals were sampled. A total of 44 Amazonian manatees, of different age groups and sexes, from the INPA were included in this study (Table 1). A total of 76 nasal and rectal swabs were collected, of which 21 were from calves (47.7%), 14 were from juveniles (31.8%), and nine were from adults (20.4%), with the majority being female. The time spent in captivity by the sampled calves varied from 3 days to 40 months, with an average of 15 months. The juveniles in captivity were from 29 to 70 months of age, with a mean age of 56. All sampled adults were in captivity for over five years, with a maximum of 36 years (mean = 19 years).

Table 1
Collected samples, animal age category, and culture results for Escherichia coli and Staphylococcus spp. in captive Amazonian manatee (Trichechusinunguis).

Age group	--Nasal swab (%)--	--Rectal swab (%)--	----TOTAL (%)----	---------------------Culture---------------------
				E. coli	Staphylococcus spp.
Adult	9 (20.4)	5 (15.6)	14 (18.4)	5 (20)	7 (21.8)
Juvenile	14 (31.8)	13 (40.6)	27 (35.5)	8 (32)	7 (21.8)
Calf	21 (47.7)	14 (43.7)	35 (46)	12 (48)	18 (56.2)
TOTAL (%)	44 (100)	32 (100)	76 (100)	25 (100)	32 (100)

Calves were housed in circular fiberglass tanks with 636 m³ freshwater, whereas juveniles were kept in oval fiberglass tanks filled with 2,268 m³ freshwater. Calves were fed exclusively on an artificial milk formula (water, whole milk powder, canola oil, Aminomix (Vetnil, Brazil), soybean meal, rolled oats, and corn flour) four times per day (MADURO et al., 2020). A combination of milk formula with mixed cultivated vegetables and grasses (carrots, lettuce, pumpkin, cabbage, Brachiariamutica, and Eichhorniacrassipes) was offered to the juveniles thrice daily. The adults were fed once daily, exclusively on a mixture of cultivated vegetables and grass.

For sampling, the animals were physically restrained and placed over a sponge mattress outside the water. All individuals were clinically monitored and considered healthy when samples were collected. Nasal and rectal swabs were collected in Stuart medium (Olen^®, China) and were refrigerated and sent to the Laboratory of Bacterioses and Anaerobe Research at the Veterinary School of the Federal University of Minas Gerais (Belo Horizonte, Brazil) to be processed within four days.

Staphylococcus sp. and detection of mecA

Swabs were seeded onto saline mannitol agar (MSA; Difco, USA) and incubated at 37 °C for 24 h to isolate Staphylococcus spp. Presumptive colonies from each sample were plated on Müller Hinton agar (MH; Difco, USA) and identified by matrix-assisted laser desorption/ionization time-of-flight (MALDI-TOF) mass spectrometry, as previously described (ASSIS et al., 2017) using a FlexControlMicroFlex LT mass spectrometer (Bruker Daltonics, USA) with a 60-Hz nitrogen laser, in which up to 240 laser shots were used. Parameters for mass range detection were defined to allow the identification from 1,960 to 20,137 m/z, where Ion source 1 was 19.99 kV, Ion source 2 was 18.24 kV, and the lens voltage was 6.0 kV for data acquisition. Prior to measurement, calibration was performed using a standard control (Escherichia coli DH5 alpha; Bruker Daltonics, USA). The real-time (RT) identification score criteria were those recommended by the manufacturer: a score ≥ 2.3 indicated a species-level identification. Isolates with MALDI-TOF, scores under 2.300 were submitted to sequencing the rpoB gene (MELLMANN et al., 2006).

Antimicrobial susceptibility tests were performed using the disk diffusion method on agar according to the Institute of Clinical and Laboratory Standards Institute (CLSI) guidelines M100-S30 and VET01S (CLSI, 2020a; CLSI, 2020b). The antimicrobials tested were based on the recommendations of CLSI (CLSI, 2020a; CLSI, 2020b) and considered one representative compound from each antimicrobial class commonly used in human and veterinary medicine: cefoxitin (CFO:30 µg), penicillin G (PEN:10 IU), tetracycline (TET:30 µg), trimethoprim/sulfamethoxazole (SUT:25 µg), chloramphenicol (CLO:30 µg), erythromycin (ERI:5 µg), clindamycin (CLI:2 µg), gentamicin (GEN:10 µg), rifampicin (RIF:5 µg), and ciprofloxacin (CIP:5 µg) (DME, BRA). Staphylococcus aureus ATCC 25923 was used as the control. Isolates were considered multidrug resistant (MDR) if they were resistant to three or more classes of antimicrobials (SWEENEY et al., 2018). In addition, Staphylococcus spp. isolates were tested by polymerase chain reaction (PCR) to determine whether they carried the mecA gene (MURAKAMI et al., 1991).

Escherichia coli

For E. coli isolation, nasal and fecal swabs were plated on MacConkey agar (MC; Difco, USA) and incubated for 24 h at 37 ºC. Up to three selected lactose-producing colonies from each sample were subjected to species-specific PCR, as previously described (MCDANIEL et al., 1996) and using the following primers: 5ʹ-ACCTGCGTTGCGTAAATA-3ʹ forward and 5ʹ-GGGCGGGAGAAGTTGATG-3ʹ reverse. The E. coli isolates were then classified into one of the following phylogroups: A, B1, B2, C, D, E, F, or Clade I (CLERMONT et al., 2013). The presence of virulence genes associated with enterotoxigenicE. coli (ETEC: sta, stb, lt, f5, f18, f41, f4, and 987p), enteropathogenicE. coli (EPEC: eae, bfpA, iha, toxB, and efa1), Shiga toxin-producing E. coli (STEC: stx1, stx2, ehxA, and saa), enterohemorrhagicE. coli (EHEC: eae, iha, toxB, efa1, stx1, stx2, ehxA, and saa), E. colinecrotoxic (NTEC: cnf1, cnf2, and f17), enteroaggregativeE. coli (EAEC: astA, aggR, aaf, and pet) and enteroinvasiveE. coli (EIEC: ipaH) were screened using PCR (RAMOS et al., 2019).

One E. coli isolate per animal was subjected to antimicrobial susceptibility testing. Two isolates were tested for animals that were positive for more than one E. coliphylogroup. Antimicrobial susceptibility tests were performed using disk diffusion on agar according to the Institute of Clinical and Laboratory Standards guideline VET01S (CLSI, 2020a). The following antimicrobials were tested: trimethoprim/sulfamethoxazole (SUT:25 µg), enrofloxacin (ENO:5 µg), gentamicin (GEN:10 µg), neomycin (NEO:30 µg), ceftiofur (CFT:30 µg), amoxicillin/clavulanic acid (AMC:30 µg), ampicillin (AMP:10 µg), florfenicol (FLF:30 µg), doxycycline (DOX:30 µg), oxytetracycline (OT:30 µg) (zones of inhibition were interpreted according to CLSI, 2020), and ciprofloxacin (CIP:5 µg) (zones of inhibition were interpreted according to EUCAST, 2022) (DME, BRA). E. coli ATCC 25922 was used as the control.

RESULTS AND DISCUSSION:

Bacteria of the genus Staphylococcus were isolated from nasal swabs of 32 (72.7%) individuals. S. sciuri was the most commonly isolated species in this study (Table 2). There was no association between the isolation of Staphylococcus species and animal categories (P> 0.05).

Table 2
Distribution of Staphylococcus spp. isolates in nasal swabs of captive Amazonian manatees (Trichechusinunguis) (n= 44).

Species	----------------------------------------------------------------Total (%)----------------------------------------------------------------
S. sciuri	17 (38.6)
S. kloosii	4 (9)
S. haemolyticus	3 (6.8)
S. warneri	2 (4.5)
S. gallinarum	2 (4.5)
S. xylosus	1 (2.3)
S.pseudoxylosus	1 (2.3)
S.pasteuri	1 (2.3)
S. hominis	1 (2.3)
Negatives	12 (27.3)
Total	44 (100)

Resistance to penicillin and tetracycline was observed in 13 (40.6%) and three (9.3%) isolates, respectively (Figure 1). Two isolates (6.2%) exhibited simultaneous resistance to both antimicrobials. The highest resistance rate among the tested strains (P = 0.0111) was for penicillin, whereas all isolates were sensitive to cefoxitin, rifampicin, chloramphenicol, ciprofloxacin, and gentamicin.

Figure 1
Overall frequency of antimicrobial resistance among Staphylococcus spp. (A) and Escherichia coli isolates (B) from captive Amazonian manatee (Trichechusinunguis), Brazil. Legend: R - Resistant; I - Intermediate Resistance; S -Susceptible; cefoxitin (CFO), penicillin (PEN), tetracycline (TET), trimethoprim/sulfamethoxazole (SUT), chloramphenicol (CLO), erythromycin (ERI), clindamycin (CLI), gentamicin (GEN), rifampicin (RIF), and ciprofloxacin (CIP), enrofloxacin (ENO), neomycin (NEO), ceftiofur (CFT), amoxicillin/clavulanic acid (AMC), ampicillin (AMP), florfenicol (FLF), doxycycline (DOX).

Twenty-five (25/44, 56.8%) animals tested positive for E. coli, and a total of 59 isolates were obtained from rectal swabs. Of the total number of isolates, 39 (66.1%) were classified as phylogroup B1 (Table 3), which had more isolates than the others (P = 0.0008). Four isolates (6.8%) were positive for virulence factors, three of which were classified as ETEC (positive for LT and 937p virulence factors), and one isolate was classified as EPEC (positive for the eae gene, which codes for intimin) (Table 4).

Table 3
Number of isolates and frequency of Clermont phylogroups of Escherichia coli identified from rectal swabs of 25 captive Amazonian manatees (Trichechusinunguis).

Phylogroup	--------------------------------------------------------Total positive isolates (%)--------------------------------------------------------
B1	39 (66.1)
D	9 (15.2)
A	7 (11.8)
F	3 (5.1)
E	1 (1.7)
Total	59 (100)

Table 4
Frequency of E. coli virulence genes in strains isolated from rectal swabs of captive Amazonian manatees (Trichechusinunguis) and their respective phylogroups and antimicrobial resistance.

Animal identification	------Category------	-----Phylogroup-----	Pathotype(virulence factors)	--Antimicrobial resistance--
233	Juvenile	A	ETEC (K88 and LT)	-
242	Juvenile	B1	EPEC(eae)	SUT
278	Calf	B1	ETEC (937p)	AMP
281	Calf	A	ETEC (K99)	AMC; SUT

• SUT - sulfamethoxazole/trimethoprim; AMP - ampicillin; AMC - amoxicillin/clavulanic acid.

Almost one-third (11/37 = 29.7%) of the isolates were resistant to at least one antimicrobial class, and two isolates (2/37 = 5.4%) were multidrug-resistant (Figure 1). Resistance to ampicillin and trimethoprim/sulfamethoxazole was most frequent among E. coli isolates, whereas resistance to ceftiofur and gentamicin was not detected in the present study.

Few studies have been conducted on commensal microorganisms and bacterial pathogens in wild animals, particularly endangered species (DE OLIVEIRA et al., 2021; LONCARIC et al., 2019). Among animals belonging to the order Sirenia, the manatee (genus Trichechus, specifically the species Trichechusinunguis) stands out. Studying this species in the wild is difficult due to its habitat and behavior, as it can camouflage itself in the dark waters of the Amazon rivers, avoiding contact with humans as much as possible (ARÉVALO - SANDI; et al., 2016). To date, studies on Staphylococcus and E. coli in animals of the order Sirenia have been limited to case reports, and few studies have evaluated the colonization and antimicrobial sensitivity of the pathogens affecting these animals (SUZUKI et al., 2019; SILVA et al., 2017; VERGARA-PARENTE et al., 2003).

The Staphylococcus genus has recently become a major concern due to increasing antimicrobial resistance and frequent reports of infection in a variety of hosts, including wild animals (FEBLER et al., 2018; GARCÍA et al., 2020; MATIAS et al., 2018; WENDLANDT et al., 2013). Recent studies have suggested an interconnection between humans, animals, and the environment, with non-domestic animals potentially serving as carriers of staphylococci and antimicrobial resistance genes located in mobile genetic elements (ABDULLAHI et al., 2021; ROSSI et al., 2020). In the present study, S. sciuri was the most common species in the three animal categories studied and was found in almost half of the animals (40.9%). S. sciuri is known to colonize a wide range of hosts (GARCÍA et al., 2020; HAUSCHILD et al., 2007; SARAIVA et al., 2021) and is frequently described as an opportunistic pathogen in several animals species and humans (CARVALHO et al., 2022; NEMEGHAIRE et al., 2014; SANTANA et al., 2022a).

Other species of the genus Staphylococcus identified in this study have also been reported. S. kloosii, S. haemolyticus, and S. warneri have been reported to infect humans and colonize various animals, such as birds of prey, bats, and trout, as well as some domestic species (FOUNTAIN et al., 2019; DOS SANTOS et al., 2018; SIGLER; HENSLEY, 2013; SOUSA et al., 2016). S. haemolyticus is a notable pathogen frequently associated with human infections, particularly that of neonates (CZEKAJ et al., 2015; ELTWISY et al., 2022; PEREIRA et al., 2014; WESTBERG; et al., 2022).

Thirteen (40.6%) Staphylococcus isolates showed resistance to at least one antimicrobial agent, a frequency similar to that observed in previous studies on some wild animals (SANTANA et al., 2022a, 2022b; SOUSA et al., 2014). This higher frequency of penicillin resistance is consistent with the results of previous studies on various animals, such as tortoises and wild birds (RUIZ-RIPA et al., 2019; SANTANA et al., 2022a). Some authors have hypothesized that this frequency of resistant isolates is due to the widespread use of beta-lactams, particularly penicillin, in both human and veterinary medicine (COLLIGNON et al., 2016; MCEWEN & COLLIGNON, 2018). It is worth noting that the use of antimicrobials in these animals is rare, which suggests indirect dissemination of resistance mechanisms and/or resistance (REBELO et al., 2021; VERSTRAETE et al., 2022).

It is not surprising that most animals tested positive for E. coli, as this microorganism is commensal in animals (BLOUNT, 2015; LAGERSTROM & HADLY, 2021; LEIMBACH et al., 2013; MURPHY et al., 2021; TENAILLON et al., 2010). Among the isolates, phylogroup B1 was the most prevalent, corroborating studies on several animal species that showed a high prevalence of this phylogroup in their gastrointestinal microbiota (LAGERSTROM & HADLY, 2021; RAMOS et al., 2019; TENAILLON et al., 2010; XAVIER et al., 2022). Phylogroups A and D were detected in approximately 27% of the animals. These two phylogroups are more common in humans (BAILEY et al., 2010) and have been reported at lower frequencies in some animal species than those found in this study (KILANI et al., 2017; XAVIER et al., 2022). This detection raises two hypotheses: either isolates from phylogroups A and D are part of the microbiota of these animals, unlike some wild species already studied (CRISTÓVÃO et al., 2017; ZURFLUH et al., 2019), or there is external influence, such as contamination of riverbeds by human and domestic animal waste or transmission by contaminated feed (AMARSY et al., 2019; GUENTHER et al., 2011; KARAKAYA et al., 2022).

Four E. coli isolates were positive for virulence factors and were classified as ETEC or EPEC. These virulence factors are commonly associated with enteric colibacillosis in cattle and pigs (AWAD et al., 2020; DUBREUIL; ISAACSON; SCHIFFERLI, 2016). These findings suggest that Amazonian manatees may host diarrheagenic strains of E. coli and, combined with the detection of strains of phylogroups A and D, further supports the hypothesis that colonization is secondary to indirect contact with domestic animal waste.

Interestingly, almost one-third of the tested E. coli isolates were resistant to at least one antimicrobial, and resistance to ampicillin, sulfamethoxazole/trimethoprim, and tetracycline was the most common. Notably, these are the antimicrobials most commonly used in human and veterinary medicine (BOECKEL et al., 2019; VITTECOQ et al., 2016).

Similar to that of Staphylococcus spp., few studies on E. coli in animals belonging to the order Sirenia make comparisons difficult. These results suggest that manatees may spread resistance genes through the water in which they live, which could constitute environmental pollution (GUENTHER et al., 2011).

In conclusion, this study suggests that Amazonian manatees in captivity are commonly colonized by Staphylococcus spp., mainly S. sciuri, and diarrheagenicE. coli isolates, including multidrug resistant strains. Future studies may clarify the possible influence of riverbed contamination on microbial colonization. In addition, sampling of free-living animals is necessary to better understand the influence of captivity on the microbiota of Amazonian manatees.

ACKNOWLEDGMENTS

This work was supported by funds from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES - Prêmio CAPES 2015 - 0774/2017 and Brasil - Finance code 001), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq - 406402/2018-3, PCI-DB 301484/2020-1, 301297/2021-5 and 02132/2021-0), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG - APQ-00524-17), Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM - UNIVERSAL AMAZONAS - 062.00891/2019) and Pró-Reitoria de Pesquisa da Universidade Federal de Minas Gerais (PRPq/UFMG).

REFERENCES

• ABDULLAHI, I. N. et al. Wild animals Procuraruniformizar re Reservoirs and Sentinels of Staphylococcus aureus and MRSA Clones: A Problem with “One Health” Concern. Antibiotics (Basel, Switzerland), v.10, n.12, p.1556, 20 dez. 2021. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/34943768 >. Accessed: Nov. 18, 2022. doi: 10.3390/antibiotics10121556.
  » https://doi.org/10.3390/antibiotics10121556.» https://pubmed.ncbi.nlm.nih.gov/34943768
• ABREHAM, S. et al. Escherichia coli O157:H7: distribution, molecular characterization, antimicrobial resistance patterns and source of contamination of sheep and goat carcasses at an export abattoir, Mojdo, Ethiopia. BMC microbiology, v.19, n.1, p.215, 12 sept. 2019. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/31510932 >. Accessed: Jan. 8, 2023. doi: 10.1186/s12866-019-1590-8.
  » https://doi.org/10.1186/s12866-019-1590-8.» https://pubmed.ncbi.nlm.nih.gov/31510932
• ALFURAIJI, N. et al. UropathogenicEscherichia coli virulence characteristics and antimicrobial resistance amongst pediatric urinary tract infections. Journal of Medicine and Life, v.15, n.5, p.650-654, maio 2022. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/35815089 >. Accessed: Jan. 8, 2023. doi: 10.25122/jml-2021-0148.
  » https://doi.org/10.25122/jml-2021-0148.» https://pubmed.ncbi.nlm.nih.gov/35815089
• AMARSY, R. et al. Determination of Escherichia coliphylogroups in elderly patients with urinary tract infection or asymptomatic bacteriuria. Clinical Microbiology and Infection: The Official Publication of the European Society of Clinical Microbiology and Infectious Diseases, v.25, n.7, p.839-844, jul. 2019. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/30648603 >. Accessed: Jan. 8, 2023. doi: 10.1016/j.cmi.2018.12.032.
  » https://doi.org/10.1016/j.cmi.2018.12.032.» https://pubmed.ncbi.nlm.nih.gov/30648603
• ARÉVALO-SANDI, A. R.; CASTELBLANCO-MARTÍNEZ, D. N. Interactions between calves of Amazonian manatees in Peru: a study case. Acta Biológica Colombiana, v.21, n.2, p.355-364, maio 2016. Available from: <Available from: http://www.scielo.org.co/scielo.php?script=sci_abstract&pid=S0120-548X2016000200004&lng=en&nrm=iso&tlng=en >. Accessed: Sept. 12, 2022. doi: 10.15446/abc.v21n2.48675.
  » https://doi.org/10.15446/abc.v21n2.48675.» http://www.scielo.org.co/scielo.php?script=sci_abstract&pid=S0120-548X2016000200004&lng=en&nrm=iso&tlng=en
• ASSIS, G. B. N. et al. Use of MALDI-TOF Mass spectrometry for the fast identification of Gram-Positive fish pathogens. Frontiers in Microbiology, v.8, p.1492, 2017. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/28848512 >. Accessed: Nov. 11, 2022. doi: 10.3389/fmicb.2017.01492.
  » https://doi.org/10.3389/fmicb.2017.01492.» https://pubmed.ncbi.nlm.nih.gov/28848512
• AWAD, W. S. et al. Molecular characterization of pathogenic Escherichia coli isolated from diarrheic and in-contact cattle and buffalo calves. Tropical Animal Health and Production, v.52, n.6, p. 3173-3185, nov. 2020. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/32647966 >. Accessed: Jan. 8, 2023. doi: 10.1007/s11250-020-02343-1.
  » https://doi.org/10.1007/s11250-020-02343-1.» https://pubmed.ncbi.nlm.nih.gov/32647966
• AWORH, M. K. et al. Genetic relatedness of multidrug resistant Escherichia coli isolated from humans, chickens and poultry environments. Antimicrobial Resistance and Infection Control, v.10, n.1, p.58, 23 mar. 2021. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/33757589 >. Accessed: Jan. 8, 2023. doi: 10.1186/s13756-021-00930-x.
  » https://doi.org/10.1186/s13756-021-00930-x.» https://pubmed.ncbi.nlm.nih.gov/33757589
• BAILEY, J. K. et al. Distribution of human commensal Escherichia coli phylogenetic groups. Journal of Clinical Microbiology, v.48, n.9, p.3455-3456, sept. 2010. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/20610687 >. Accessed: Nov. 11, 2022. doi: 10.1128/JCM.00760-10.
  » https://doi.org/10.1128/JCM.00760-10.» https://pubmed.ncbi.nlm.nih.gov/20610687
• BARRETO, U. H. A. et al. Abdominal ultrasound in Amazonian manatee (Trichechusinunguis) (Natterer, 1883). Brazilian Journal of Biology = RevistaBrasleira De Biologia, v.83, p.e247609, 2021. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/34468528 >. Accessed: Nov. 21, 2022. doi: 10.1590/1519-6984.247609.
  » https://doi.org/10.1590/1519-6984.247609.» https://pubmed.ncbi.nlm.nih.gov/34468528
• BESSALAH, S. et al. Characterization and antimicrobial susceptibility of Escherichia coli isolated from healthy farm animals in Tunisia. Animal Biotechnology, v.32, n.6, p.748-757, dez. 2021. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/32293994 >. Accessed: Nov. 21, 2022. doi: 10.1080/10495398.2020.1752702.
  » https://doi.org/10.1080/10495398.2020.1752702» https://pubmed.ncbi.nlm.nih.gov/32293994
• BLOUNT, Z. D. The unexhausted potential of E. coli eLife, v.4, 25 mar. 2015. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/25807083 >. Accessed: Nov. 20, 2022. doi: 10.7554/eLife.05826.
  » https://doi.org/10.7554/eLife.05826.» https://pubmed.ncbi.nlm.nih.gov/25807083
• BOECKEL, T. P. V. et al. Global trends in antimicrobial resistance in animals in low- and middle-income countries. Science, 20 sept. 2019. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/31604207 >. Accessed: Nov. 10, 2022. doi: 10.1126/science.aaw1944.
  » https://doi.org/10.1126/science.aaw1944.» https://pubmed.ncbi.nlm.nih.gov/31604207
• CABALLERO, S. et al. Mitochondrial genetic diversity, population structure and detection of Antillean and Amazonian Manatees in Colombia: New Areas and New Techniques. Frontiers in Genetics, v.12, p.726916, 2021. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/34899829 >. Accessed: Nov. 21, 2022. doi: 10.3389/fgene.2021.726916.
  » https://doi.org/10.3389/fgene.2021.726916.» https://pubmed.ncbi.nlm.nih.gov/34899829
• CARVALHO, T. P. et al. Mammaliicoccus (Staphylococcus) sciuri-induced suppurative meningoencephalitis and bacteremia in an infant western lowland gorilla (Gorilla gorilla gorilla). Journal of Medical Primatology, v.51, n.6, p.396-399. 2022 Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/35570384 >. Accessed: May, 29, 2023. doi: 10.1111/jmp.12597.
  » https://doi.org/10.1111/jmp.12597.» https://pubmed.ncbi.nlm.nih.gov/35570384
• CLERMONT, O. et al. The Clermont Escherichia coliphylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environmental Microbiology Reports, v.5, n.1, p.58-65, fev. 2013. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/23757131 >. Accessed: Nov. 20, 2022. doi: 10.1111/1758-2229.12019.
  » https://doi.org/10.1111/1758-2229.12019.» https://pubmed.ncbi.nlm.nih.gov/23757131
• CLINICAL AND LABORATORY STANDARDS INSTITUTE. (CLSI). Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated From Animals. 5th ed. CLSI supplement VET01S (ISBN 978-1-68440-092-8 [Print]; ISBN 978-1-68440-093-5 [Electronic]). Clinical and Laboratory Standards Institute, 950 West Valley Road, Suite 2500, Wayne, Pennsylvania 19087 USA, 2020a.
• CLINICAL AND LABORATORY STANDARDS INSTITUTE (CLSI). Wayne, PA, USA. Performance Standards for Antimicrobial Susceptibility Testing. 30th ed. CLSI supplement M100, 19087, 2020b.
• COLLIGNON, P. C. et al. World Health Organization ranking of antimicrobials according to their importance in human medicine: A Critical step for developing risk management strategies to control antimicrobial resistance from food animal production. Clinical Infectious Diseases, v.63, n.8, p.1087-1093, 15 out. 2016. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/27439526 >. Accessed: Nov. 10, 2022. doi: 10.1093/cid/ciw475.
  » https://doi.org/10.1093/cid/ciw475.» https://pubmed.ncbi.nlm.nih.gov/27439526
• CRISTÓVÃO, F. et al. Clonal diversity of extended-spectrum beta-lactamase producing Escherichia coli isolates in fecal samples of wild animals. FEMS microbiology letters, v.364, n.5, 1 mar. 2017. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/28364731 >. Accessed: Jan. 8, 2023. doi: 10.1093/femsle/fnx039.
  » https://doi.org/10.1093/femsle/fnx039.» https://pubmed.ncbi.nlm.nih.gov/28364731
• CZEKAJ, T.; et al. Staphylococcus haemolyticus - an emerging threat in the twilight of the antibiotics age. Microbiology (Reading, England), v.161, n.11, p.2061-2068, nov. 2015. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/26363644/ >. Accessed: Nov. 18, 2022. doi: 10.1099/mic.0.000178.
  » https://doi.org/10.1099/mic.0.000178.» https://pubmed.ncbi.nlm.nih.gov/26363644/
• DE OLIVEIRA, T. M. et al. TLR4 and TLR8 variability in Amazonian and West Indian manatee species from Brazil. Genetics and Molecular Biology, v.44, n.2, p.e20190252, 9 abr. 2021. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/33847701 >. Accessed: Nov. 19, 2022. doi: 10.1590/1678-4685-GMB-2019-0252.
  » https://doi.org/10.1590/1678-4685-GMB-2019-0252.» https://pubmed.ncbi.nlm.nih.gov/33847701
• DUBREUIL, J. D.; ISAACSON, R. E.; SCHIFFERLI, D. M. Animal enterotoxigenicEscherichia coli EcoSal Plus, v.7, n.1, out. 2016. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/27735786 >. Accessed: Jan. 8, 2023. doi: 10.1128/ecosalplus.ESP-0006-2016.
  » https://doi.org/10.1128/ecosalplus.ESP-0006-2016.» https://pubmed.ncbi.nlm.nih.gov/27735786
• ELTWISY, H. O. et al. Clinical infections, antibiotic resistance, and pathogenesis of Staphylococcus haemolyticus Microorganisms, v.10, n.6, p.1130, 31 maio 2022. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/35744647 >. Accessed: Nov. 18, 2022. doi: 10.3390/microorganisms10061130.
  » https://doi.org/10.3390/microorganisms10061130.» https://pubmed.ncbi.nlm.nih.gov/35744647
• EUCAST - The European Committee on Antimicrobial Susceptibility Testing (EUCAST). Breakpoint tables for interpretation of MICs and zone diameters. In: European Society of Clinical Microbiology and Infectious Diseases Basel, 2022.
• FEβLER, A. T. et al. Phenotypic and genotypic characteristics of Staphylococcus aureus isolates from zoo and wild animals. Veterinary Microbiology, v.218, p.98-103, maio 2018. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/29685228 >. Accessed: Nov. 7, 2022. doi: 10.1016/j.vetmic.2018.03.020.
  » https://doi.org/10.1016/j.vetmic.2018.03.020.» https://pubmed.ncbi.nlm.nih.gov/29685228
• FOUNTAIN, K. et al. Diversity of staphylococcal species cultured from captive livingstone’s fruit bats (Pteropuslivingstonii) and their environment. Journal of Zoo and Wildlife Medicine: Official Publication of the American Association of Zoo Veterinarians, v.50, n.1, p.266-269, 1 mar. 2019. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/31120689 >. Accessed: Nov. 18, 2022. doi: 10.1638/2018-0121.
  » https://doi.org/10.1638/2018-0121» https://pubmed.ncbi.nlm.nih.gov/31120689
• GARCÊS, A. et al. Pyometra Caused by Staphylococcus lentus in a Wild European Hedgehog (Erinaceuseuropaeus). Journal of Wildlife Diseases, v.55, n.3, p.724-727, jul. 2019. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/30628855 >. Accessed: Nov. 7, 2022. doi: 10.7589/2018-06-158.
  » https://doi.org/10.7589/2018-06-158.» https://pubmed.ncbi.nlm.nih.gov/30628855
• GARCÍA, L. A. et al. Staphylococcus spp. from wild mammals in Aragón (Spain): Antibiotic Resistance Status. Journal of Veterinary Research, v.64, n.3, p.373-379, 16 sept. 2020. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/32984626 >. Accessed: Nov. 18, 2022. doi: 10.2478/jvetres-2020-0057.
  » https://doi.org/10.2478/jvetres-2020-0057.» https://pubmed.ncbi.nlm.nih.gov/32984626
• GUENTHER, S.; EWERS, C.; WIELER, L. H. Extended-spectrum beta-lactamases Producing E. coli in Wildlife, yet Another Form of Environmental Pollution? Frontiers in Microbiology, v.2, p.246, 2011. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/22203818 >. Accessed: Nov. 20, 2022. doi: 10.3389/fmicb.2011.00246.
  » https://doi.org/10.3389/fmicb.2011.00246.» https://pubmed.ncbi.nlm.nih.gov/22203818
• HAUSCHILD, T. et al. Tetracycline resistance and distribution of tet genes in members of the Staphylococcus sciurigroup isolated from humans, animals and different environmental sources. International Journal of Antimicrobial Agents, v.29, n.3, p.356-358, mar. 2007. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/17229556 >. Accessed: Nov. 7, 2022. doi: 10.1016/j.ijantimicag.2006.10.002.
  » https://doi.org/10.1016/j.ijantimicag.2006.10.002.» https://pubmed.ncbi.nlm.nih.gov/17229556
• KARAKAYA, E. et al. Escherichia coli in different animal feces: phylotypes and virulence genes. World Journal of Microbiology & Biotechnology, v.39, n.1, p.14, 16 nov. 2022. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/36383288 >. Accessed: Jan. 8, 2022. doi: 10.1007/s11274-022-03451-w.
  » https://doi.org/10.1007/s11274-022-03451-w.» https://pubmed.ncbi.nlm.nih.gov/36383288
• KILANI, H. et al. Diverse Escherichia colipathovars of phylogroups B2 and D isolated from animals in Tunisia. Journal of Infection in Developing Countries, v.11, n.7, p.549-556, 31 jul. 2017. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/31071064/ >. Accessed: Jan. 8, 2022. doi: 10.3855/jidc.8579.
  » https://doi.org/10.3855/jidc.8579» https://pubmed.ncbi.nlm.nih.gov/31071064/
• KOLENDA, R.; BURDUKIEWICZ, M.; SCHIERACK, P. A systematic review and meta-analysis of the epidemiology of pathogenic Escherichia coli of calves and the role of calves as reservoirs for human pathogenic E. coli. Frontiers in Cellular and Infection Microbiology, v.5, p.23, 2015. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/25815276 >. Accessed: Jan. 8, 2022. doi: 10.3389/fcimb.2015.00023.
  » https://doi.org/10.3389/fcimb.2015.00023.» https://pubmed.ncbi.nlm.nih.gov/25815276
• KOLODZIEJEK, A. M.; MINNICH, S. A.; HOVDE, C. J. Escherichia coli 0157:H7 virulence factors and the ruminant reservoir. Current Opinion in Infectious Diseases, v.35, n.3, p.205-214, 1 jun. 2022. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/35665714/ >. Accessed: Jan. 8, 2023. doi: 10.1097/QCO.0000000000000834.
  » https://doi.org/10.1097/QCO.0000000000000834.» https://pubmed.ncbi.nlm.nih.gov/35665714/
• LAGERSTROM, K. M.; HADLY, E. A. The under-investigated wild side of Escherichia coli: genetic diversity, pathogenicity and antimicrobial resistance in wild animals. Proceedings of the Royal Society B: Biological Sciences, v.288, n.1948, p.20210399, 2021. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/33849316 >. Accessed: Nov. 18, 2022. doi: 10.1098/rspb.2021.0399.
  » https://doi.org/10.1098/rspb.2021.0399» https://pubmed.ncbi.nlm.nih.gov/33849316
• LEIMBACH, A.; HACKER, J.; DOBRINDT, U. E. coli as an all-rounder: the thin line between commensalism and pathogenicity. Current Topics in Microbiology and Immunology, v.358, p.3-32, 2013. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/23340801 >. Accessed: Nov. 20, 2022. doi: 10.1007/82_2012_303.
  » https://doi.org/10.1007/82_2012_303.» https://pubmed.ncbi.nlm.nih.gov/23340801
• LISOWSKA-ŁYSIAK, K. et al. Epidemiology and pathogenesis of Staphylococcus bloodstream infections in humans: a review. Polish Journal of Microbiology, v.70, n.1, p.13-23, mar. 2021. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/33815523 >. Accessed: Nov. 21, 2022. doi: 10.33073/pjm-2021-005.
  » https://doi.org/10.33073/pjm-2021-005.» https://pubmed.ncbi.nlm.nih.gov/33815523
• LONCARIC, I. et al. Characterization of mecC gene-carrying coagulase-negative Staphylococcus spp. isolated from various animals. Veterinary Microbiology, v.230, p.138-144, mar. 2019. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/30827379 >. Accessed: Nov. 7, 2022. doi: 10.1016/j.vetmic.2019.02.014.
  » https://doi.org/10.1016/j.vetmic.2019.02.014.» https://pubmed.ncbi.nlm.nih.gov/30827379
• LUZZAGO, C. et al. Clonal diversity, virulence-associated genes and antimicrobial resistance profile of Staphylococcus aureus isolates from nasal cavities and soft tissue infections in wild ruminants in Italian Alps. Veterinary Microbiology, v.170, n.1-2, p.157-161, 14 maio 2014. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/24565474 >. Accessed: Jan. 8, 2023. doi: 10.1016/j.vetmic.2014.01.016.
  » https://doi.org/10.1016/j.vetmic.2014.01.016» https://pubmed.ncbi.nlm.nih.gov/24565474
• MADURO A. H. P. et al. Metabolic profile of captive Amazonian manatee calves (Trichechusinunguis), fed different substitutes for maternal milk. Arq Bras Med Vet Zootec. 2020;72(5):1830-1838. Available from: <Available from: https://www.scielo.br/j/abmvz/a/9z3bcFJMv97rprrpsWswcPF/?format=html⟨=pt >. Accessed: Jan. 14, 2022. doi: 10.1590/1678-4162-11415.
  » https://doi.org/10.1590/1678-4162-11415.» https://www.scielo.br/j/abmvz/a/9z3bcFJMv97rprrpsWswcPF/?format=html⟨=pt
• MARMONTEL, M.; KENDALL, S.; SOUZA, D. DE. IUCN Red list of threatened Species: Trichechusinunguis IUCN Red List of Threatened Species, 28 fev. 2016. Available from: <Available from: https://www.iucnredlist.org/en >. Accessed: Nov. 22, 2022. doi: 10.2305/IUCN.UK.2016-2.RLTS.T22102A43793736.en.
  » https://doi.org/10.2305/IUCN.UK.2016-2.RLTS.T22102A43793736.en.» https://www.iucnredlist.org/en
• DOS SANTOS, A. C. et al. Complete genome Sequences of the Potential Zoonotic Pathogens Staphylococcus felis and Staphylococcus kloosii Genome Announcements, v.6, n.20, p.e00404-18, 17 maio 2018. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/29773625 >. Accessed: Nov. 12, 2022. doi: 10.1128/genomeA.00404-18.
  » https://doi.org/10.1128/genomeA.00404-18.» https://pubmed.ncbi.nlm.nih.gov/29773625
• MATIAS, C. A. R. et al. Staphylococcus spp. isolated from wild birds apprehended in the local illegal trade in Rio de Janeiro, Brazil, and relevance in public health. Letters in Applied Microbiology, v.67, n.3, p.292-298, sept. 2018. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/29924392 >. Accessed: Nov. 7, 2022. doi: 10.1111/lam.13035.
  » https://doi.org/10.1111/lam.13035.» https://pubmed.ncbi.nlm.nih.gov/29924392
• MCEWEN, S. A.; COLLIGNON, P. J. Antimicrobial resistance: a One Health Perspective. Microbiology Spectrum, v.6, n.2, mar. 2018. Available from <Available from https://pubmed.ncbi.nlm.nih.gov/29600770 >. Accessed: Nov. 18, 2022. doi: 10.1128/microbiolspec.ARBA-0009-2017.
  » https://doi.org/10.1128/microbiolspec.ARBA-0009-2017» https://pubmed.ncbi.nlm.nih.gov/29600770
• MELLMANN, A. et al. Sequencing and staphylococci identification. Emerging Infectious Diseases, v.12, n.2, p.333-336, fev. 2006. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/16494767 >. Accessed: Nov. 7, 2022. doi: 10.3201/eid1202.050962.
  » https://doi.org/10.3201/eid1202.050962.» https://pubmed.ncbi.nlm.nih.gov/16494767
• MERKER BREYER, G. et al. Wild capybaras as reservoir of shiga toxin-producing Escherichia coli in urban Amazonian Region. Letters in Applied Microbiology, v.75, n.1, p.10-16, jul. 2022. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/35285057 >. Accessed: Jan. 8, 2023. doi: 10.1111/lam.13694.
  » https://doi.org/10.1111/lam.13694.» https://pubmed.ncbi.nlm.nih.gov/35285057
• MURAKAMI, K. et al. Identification of methicillin-resistant strains of staphylococci by polymerase chain reaction. J ClinMicrobiol. 1991;29(10):2240-2244. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/1939577/ >. Accessed: May, 29, 2023. doi: 10.1128/jcm.29.10.2240-2244.1991.
  » https://doi.org/10.1128/jcm.29.10.2240-2244.1991.» https://pubmed.ncbi.nlm.nih.gov/1939577/
• MURPHY, R. et al. Genomic epidemiology and evolution of Escherichia coli in Wild Animals in Mexico. mSphere, v.6, n.1, p.e00738-20, 6 jan. 2021. Available from <Available from https://pubmed.ncbi.nlm.nih.gov/33408222/ >. Accessed: Nov. 20, 2022. doi: 10.1128/mSphere.00738-20.
  » https://doi.org/10.1128/mSphere.00738-20» https://pubmed.ncbi.nlm.nih.gov/33408222/
• NEMEGHAIRE, S. et al. The ecological importance of the Staphylococcus sciurispecies group as a reservoir for resistance and virulence genes. Veterinary Microbiology, v.171, n.3-4, p.342-356, 16 jul. 2014. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/24629775 >. Accessed: Nov. 20, 2022. doi: 10.1016/j.vetmic.2014.02.005.
  » https://doi.org/10.1016/j.vetmic.2014.02.005» https://pubmed.ncbi.nlm.nih.gov/24629775
• PEREIRA, P. M. A. et al. Staphylococcus haemolyticus disseminated among neonates with bacteremia in a neonatal intensive care unit in Rio de Janeiro, Brazil. Diagnostic Microbiology and Infectious Disease, v.78, n.1, p.85-92, jan. 2014. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/24176549 >. Accessed: Nov. 18, 2022. doi: 10.1016/j.diagmicrobio.2013.06.026.
  » https://doi.org/10.1016/j.diagmicrobio.2013.06.026.» https://pubmed.ncbi.nlm.nih.gov/24176549
• PIÉRARD, D. et al. O157:H7 and O104:H4 Vero/Shiga toxin-producing Escherichia coli outbreaks: respective role of cattle and humans. Veterinary Research, v.43, n.1, p.13, 13 fev. 2012. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/22330148 >. Accessed: Jan. 8, 2023. doi: 10.1186/1297-9716-43-13.
  » https://doi.org/10.1186/1297-9716-43-13.» https://pubmed.ncbi.nlm.nih.gov/22330148
• RAMOS, C. P. et al. Identification and characterization of Escherichia coli, Salmonella spp., Clostridium perfringens, and C. difficile Isolates from Reptiles in Brazil. BioMed Research International, v.2019, p.9530732, 2019. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/31263711 >. Accessed: Nov. 20, 2022. doi: 10.1155/2019/9530732.
  » https://doi.org/10.1155/2019/9530732.» https://pubmed.ncbi.nlm.nih.gov/31263711
• RASMI, A. H. et al. Virulence genes distributed among Staphylococcus aureus causing wound infections and their correlation to antibiotic resistance. BMC infectious diseases, v.22, n.1, p.652, 28 jul. 2022. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/35902813 >. Accessed: Jan. 8, 2023. doi: 10.1186/s12879-022-07624-8.
  » https://doi.org/10.1186/s12879-022-07624-8» https://pubmed.ncbi.nlm.nih.gov/35902813
• RAUBER, J. M. et al. Multidrug-resistant Staphylococcusspp and its impact on patient outcome. American Journal of Infection Control, v.44, n.11, p.e261-e263, 1 nov. 2016. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/27639754 >. Accessed: Jan. 8, 2023. doi: 10.1016/j.ajic.2016.07.015.
  » https://doi.org/10.1016/j.ajic.2016.07.015» https://pubmed.ncbi.nlm.nih.gov/27639754
• REBELO, J. S. et al. Bacterial persistence is essential for susceptible cell survival in indirect resistance, mainly for lower cell densities. PloS One, v.16, n.9, p.e0246500, 2021. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/34473689 >. Accessed: Jan. 8, 2023. doi: 10.1371/journal.pone.0246500.
  » https://doi.org/10.1371/journal.pone.0246500.» https://pubmed.ncbi.nlm.nih.gov/34473689
• ROSSI, C. C.; et al. Underrated Staphylococcus species and their role in antimicrobial resistance spreading. Genetics and Molecular Biology, v.43, n.1 suppl 2, p.e20190065, 2020. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/32052827 >. Accessed: Nov. 18, 2022. doi: 10.1590/1678-4685-GMB-2019-0065.
  » https://doi.org/10.1590/1678-4685-GMB-2019-0065.» https://pubmed.ncbi.nlm.nih.gov/32052827
• ROTH, N. et al. The application of antibiotics in broiler production and the resulting antibiotic resistance in Escherichia coli: A global overview. Poultry Science, v.98, n.4, p.1791-1804, 1 abr. 2019. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/30544256 >. Accessed: Nov. 21, 2022. doi: 10.3382/ps/pey539.
  » https://doi.org/10.3382/ps/pey539.» https://pubmed.ncbi.nlm.nih.gov/30544256
• RUIZ-RIPA, L. et al. Diversity of Staphylococcus aureus clones in wild mammals in Aragon, Spain, with detection of MRSA ST130-mecC in wild rabbits. Journal of Applied Microbiology, v.127, n.1, p.284-291, jul. 2019. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/31063623 >. Accessed: Nov. 7, 2022. doi: 10.1111/jam.14301.
  » https://doi.org/10.1111/jam.14301.» https://pubmed.ncbi.nlm.nih.gov/31063623
• SAHIN-TÓTH, J. et al. Prevalence of Staphylococcus aureus in wild hedgehogs (Erinaceuseuropaeus) and first report of mecC-MRSA in Hungary. The Science of the Total Environment, v.815, p.152858, 1 abr. 2022. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/34995585 >. Accessed: Jan. 8, 2023. doi: 10.1016/j.scitotenv.2021.152858.
  » https://doi.org/10.1016/j.scitotenv.2021.152858.» https://pubmed.ncbi.nlm.nih.gov/34995585
• SANTANA, J. A. et al. Isolation and antimicrobial resistance of coagulase-negative staphylococci recovered from healthy tortoises in Minas Gerais, Brazil. Ciência Rural, v.52, 5 jan. 2022a. Available from: <Available from: https://www.scielo.br/j/cr/a/g4xkgQ3fDHGGZDQc9p3mRfK/abstract/?lang=en >. Accessed: Nov. 20, 2022. doi: 10.1590/0103-8478cr20210354.
  » https://doi.org/10.1590/0103-8478cr20210354» https://www.scielo.br/j/cr/a/g4xkgQ3fDHGGZDQc9p3mRfK/abstract/?lang=en
• SANTANA, J. A. et al. Clostridioides difficile and multi-drug-resistant staphylococci in free-living rodents and marsupials in parks of Belo Horizonte, Brazil. Brazilian Journal of Microbiology, v.53, n.1, p.401-410, 1 mar. 2022b. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/34761356 >. Accessed: Nov. 20, 2022. doi: 10.1007/s42770-021-00640-x.
  » https://doi.org/10.1007/s42770-021-00640-x.» https://pubmed.ncbi.nlm.nih.gov/34761356
• SARAIVA, M. DE M. S. et al. Staphylococcus sciuri as a Reservoir of mecA to Staphylococcus aureus in Non-Migratory Seabirds from a Remote Oceanic Island. Microbial Drug Resistance (Larchmont, N.Y.), v.27, n.4, p.553-561, abr. 2021. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/32816627 >. Accessed: Nov. 7, 2022. doi: 10.1089/mdr.2020.0189.
  » https://doi.org/10.1089/mdr.2020.0189.» https://pubmed.ncbi.nlm.nih.gov/32816627
• SIDRIM, J. J. C. et al. Yeast microbiota of natural cavities of manatees (Trichechusinunguisand Trichechusmanatus) in Brazil and its relevance for animal health and management in captivity. Canadian Journal of Microbiology, v.61, n.10, p.763-769, out. 2015. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/26308797 >. Accessed: Nov. 19, 2022. doi: 10.1139/cjm-2015-0341.
  » https://doi.org/10.1139/cjm-2015-0341.» https://pubmed.ncbi.nlm.nih.gov/26308797
• SIGLER, V.; HENSLEY, S. Persistence of mixed staphylococci assemblages following disinfection of hospital room surfaces. The Journal of Hospital Infection, v.83, n.3, p.253-256, mar. 2013. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/23374288 >. Accessed: Jan. 12, 2023. doi: 10.1016/j.jhin.2012.12.009.
  » https://doi.org/10.1016/j.jhin.2012.12.009.» https://pubmed.ncbi.nlm.nih.gov/23374288
• SILVA, M. C. O. et al. Identification of bacteria in blood cultures from clinically ill captive antillean manatees (Trichechusmanatusmanatus). Journal of Zoo and Wildlife Medicine: Official Publication of the American Association of Zoo Veterinarians, v.48, n.1, p.13-17, mar. 2017. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/28363079 >. Accessed: Nov. 20, 2022. doi: 10.1638/2015-0094.1.
  » https://doi.org/10.1638/2015-0094.1.» https://pubmed.ncbi.nlm.nih.gov/28363079
• SONG, K. et al. Factors associated with in-hospital mortality in adult sepsis with Escherichia coli infection. BMC infectious diseases, v.22, n.1, p.197, 28 fev. 2022. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/35227247 >. Accessed: Jan. 8, 2023. doi: 10.1186/s12879-022-07201-z.
  » https://doi.org/10.1186/s12879-022-07201-z.» https://pubmed.ncbi.nlm.nih.gov/35227247
• SOUSA, M. et al. Antimicrobial resistance determinants in Staphylococcus spp. recovered from birds of prey in Portugal. Veterinary Microbiology, v.171, n.3-4, p.436-440, 16 jul. 2014. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/24679961 >. Accessed: Nov. 20, 2022. doi: 10.1016/j.vetmic.2014.02.034.
  » https://doi.org/10.1016/j.vetmic.2014.02.034.» https://pubmed.ncbi.nlm.nih.gov/24679961
• SOUSA, M. et al. Genetic diversity and antibiotic Resistance Among Coagulase-Negative Staphylococci Recovered from Birds of Prey in Portugal. Microbial Drug Resistance (Larchmont, N.Y.), v.22, n.8, p.727-730, dez. 2016. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/26990729 >. Accessed: Nov. 18, 2022. doi: 10.1089/mdr.2015.0266.
  » https://doi.org/10.1089/mdr.2015.0266.» https://pubmed.ncbi.nlm.nih.gov/26990729
• SUAY-GARCÍA, B. et al. Detection and Characterization of Extended-Spectrum Beta-Lactamases-Producing Escherichia coli in Animals. Vector Borne and Zoonotic Diseases (Larchmont, N.Y.), v.19, n.2, p.115-120, fev. 2019. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/30129883 >. Accessed: Nov. 21, 2022. doi: 10.1089/vbz.2018.2333.
  » https://doi.org/10.1089/vbz.2018.2333.» https://pubmed.ncbi.nlm.nih.gov/30129883
• SUZUKI, A. et al. Fecal microbiota of captive Antillean manateeTrichechusmanatusmanatus FEMS Microbiology Letters, v.366, n.11, p.fnz134, 1 jun. 2019. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/31210263 >. Accessed: Nov. 19, 2022. doi: 10.1093/femsle/fnz134.
  » https://doi.org/10.1093/femsle/fnz134.» https://pubmed.ncbi.nlm.nih.gov/31210263
• SWEENEY, M. T. et al. Applying definitions for multidrug resistance, extensive drug resistance and pandrug resistance to clinically significant livestock and companion animal bacterial pathogens. The Journal of Antimicrobial Chemotherapy, v.73, n.6, p.1460-1463, 1 jun. 2018. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/29481657 >. Accessed: Nov. 20, 2022. doi: 10.1093/jac/dky043.
  » https://doi.org/10.1093/jac/dky043.» https://pubmed.ncbi.nlm.nih.gov/29481657
• TENAILLON, O. et al. The population genetics of commensal Escherichia coli Nature Reviews. Microbiology, v.8, n.3, p.207-217, mar. 2010. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/20157339 >. Accessed: Nov. 20, 2022. doi: 10.1038/nrmicro2298.
  » https://doi.org/10.1038/nrmicro2298.» https://pubmed.ncbi.nlm.nih.gov/20157339
• TORRES, R. T. et al. A walk on the wild side: Wild ungulates as potential reservoirs of multidrug resistant bacteria and genes, including Escherichia coliharbouring CTX-M beta-lactamases. Environmental Pollution (Barking, Essex: 1987), v.306, p.119367, 1 ago. 2022. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/35489528 >. Accessed: Jan. 8, 2023. doi: 10.1016/j.envpol.2022.119367.
  » https://doi.org/10.1016/j.envpol.2022.119367.» https://pubmed.ncbi.nlm.nih.gov/35489528
• VERGARA-PARENTE, J. et al. Bacterial flora of upper respiratory tract of captive Antillean manatees.Aquatic Mammals, v.29, p.124, 1 jan. 2003. Available from: <Available from: https://www.icmbio.gov.br/cma/images/stories/Publica%C3%A7%C3%B5es/Vergara-Parente_et_al._2003.pdf >. Accessed: Nov. 20, 2022. doi: 10.1578/016754203101023979.
  » https://doi.org/10.1578/016754203101023979.» https://www.icmbio.gov.br/cma/images/stories/Publica%C3%A7%C3%B5es/Vergara-Parente_et_al._2003.pdf
• VERSTRAETE, L. et al. Ecology and evolution of antibiotic persistence. Trends in Microbiology, v.30, n.5, p.466-479, maio 2022. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/34753652 >. Accessed: Jan. 8, 2023. doi: 10.1016/j.tim.2021.10.001.
  » https://doi.org/10.1016/j.tim.2021.10.001.» https://pubmed.ncbi.nlm.nih.gov/34753652
• VIEGAS, F. M. et al. Occurrence and characterization of methicillin-resistant Staphylococcus spp. in diseased dogs in Brazil. PloS One, v.17, n.6, p.e0269422, 2022. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/35657980 >. Accessed: Sept. 15, 2022. doi: 10.1371/journal.pone.0269422.
  » https://doi.org/10.1371/journal.pone.0269422» https://pubmed.ncbi.nlm.nih.gov/35657980
• VITTECOQ, M. et al. Antimicrobial resistance in wildlife. Journal of Applied Ecology, v.53, n.2, p.519-529, 2016. Available from: <Available from: https://besjournals.onlinelibrary.wiley.com/doi/full/10.1111/1365-2664.12596 >. Accessed: Nov. 18, 2022. doi: 10.1111/1365-2664.12596.
  » https://doi.org/10.1111/1365-2664.12596.» https://besjournals.onlinelibrary.wiley.com/doi/full/10.1111/1365-2664.12596
• WALTHER, B.; TEDIN, K.; LÜBKE-BECKER, A. Multidrug-resistant opportunistic pathogens challenging veterinary infection control. Veterinary Microbiology, v.200, p.71-78, fev. 2017. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/27291944 >. Accessed: Nov. 21, 2022. doi: 10.1016/j.vetmic.2016.05.017.
  » https://doi.org/10.1016/j.vetmic.2016.05.017.» https://pubmed.ncbi.nlm.nih.gov/27291944
• WENDLANDT, S. et al. The diversity of antimicrobial resistance genes among staphylococci of animal origin. International journal of medical microbiology: IJMM, v.303, n.6-7, p. 338-349, ago. 2013. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/23499306 >. Accessed: Nov. 7, 2022. doi: 10.1016/j.ijmm.2013.02.006.
  » https://doi.org/10.1016/j.ijmm.2013.02.006.» https://pubmed.ncbi.nlm.nih.gov/23499306
• WESTBERG, R.; STEGGER, M.; SÖDERQUIST, B. Molecular Epidemiology of Neonatal-Associated Staphylococcus haemolyticusReveals Endemic Outbreak. Microbiology Spectrum, p.e0245222, 31 out. 2022. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/36314976 >. Accessed: Nov. 18, 2022. doi: 10.1128/spectrum.02452-22.
  » https://doi.org/10.1128/spectrum.02452-22» https://pubmed.ncbi.nlm.nih.gov/36314976
• WIELER, L. H. et al. Methicillin-resistant staphylococci (MRS) and extended-spectrum beta-lactamases (ESBL)-producing Enterobacteriaceae in companion animals: nosocomial infections as one reason for the rising prevalence of these potential zoonotic pathogens in clinical samples. International journal of medical microbiology: IJMM, v.301, n.8, p.635-641, dez. 2011. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/22000738 >. Accessed: Nov. 21, 2022. doi: 10.1016/j.ijmm.2011.09.009.
  » https://doi.org/10.1016/j.ijmm.2011.09.009.» https://pubmed.ncbi.nlm.nih.gov/22000738
• XAVIER, R. G. C. et al. Characterization of Escherichia coli in Dogs with Pyometra and the Influence of Diet on the Intestinal Colonization of Extraintestinal Pathogenic E. coli (ExPEC). Veterinary Sciences, v.9, n.5, p.245, 22 maio 2022. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/35622773 >. Accessed: Nov. 20, 2022. doi: 10.3390/vetsci9050245.
  » https://doi.org/10.3390/vetsci9050245.» https://pubmed.ncbi.nlm.nih.gov/35622773
• ZURFLUH, K. et al. Antimicrobial resistant and extended-spectrum β-lactamase producing Escherichia coli in common wild bird species in Switzerland. MicrobiologyOpen, v.8, n.11, p.e845, nov. 2019. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/31006991 >. Accessed: Jan. 8, 2023. doi: 10.1002/mbo3.845.
  » https://doi.org/10.1002/mbo3.845» https://pubmed.ncbi.nlm.nih.gov/31006991

• CR-2023-0140.R2

BIOETHICS AND BIOSECURITY COMMITTEE APPROVAL

• This study was conducted with permission from the Instituto Chico Mendes de Conservação da Biodiversidade, (ICMBio-SISBIO) permit 72503-2. In addition, the study satisfied the ethics and animal welfare criteria of the Comitê de ÉticaemExperimentação Animal da União Federal Instituto do Amazonas.

Edited by

Editors: Rudi Weiblen (0000-0002-1737-9817) Juliana FelipettoCargnelutti (0000-0002-3160-3643)

Publication Dates

• Publication in this collection
  01 Mar 2024
• Date of issue
  2024

History

• Received
  09 Mar 2023
• Accepted
  14 Sept 2023
• Reviewed
  27 Dec 2023