Abstract
The environment, human, and animals play an important role in the spread of antibiotic-resistant bacteria. Enterococci are members of the gastrointestinal tracts of humans and animals and represent important reservoirs of antibiotic resistance genes. Until today, few studies have examined antibiotic susceptibility in enterococci isolated from primates. Therefore, the present study investigated species distribution, antibiotic susceptibility, and resistance genes in enterococci isolated from wild and captive black capuchins monkeys (Sapajus nigritus) in Rio Grande do Sul, South Brazil. A total of 24 swabs/fecal samples were collected, including 19 from wild monkeys living in two forest fragments [São Sebastião do Caí (SSC) and Santa Cruz do Sul (SCS)], and five in captive [Parque Zoológico da Fundação Zoobotânica (ZOO)], between August 2016 and November 2017. Fifteen colonies were randomly selected from each sample. Enterococci were identified by MALDI-TOF, tested for susceptibility to 12 antibiotics; and screened for tet(S), tet(M), tet(L), msrC, and erm(B) genes by PCR. Two-hundred ninety-six enterococci were isolated (SSC n = 137; SCS n = 86; ZOO n = 73) and differences in Enterococcus species distribution were detected on three monkey groups, with low abundance in SCS (1 - D = 0.2), followed by ZOO (1 - D = 0.68), and SSC (1 - D = 0.73). The enterococci frequently recovered include the following: Enterococcus faecalis (42.6%), E. hirae (29.1%), and E. faecium (15.9%). Antibiotic-nonsusceptible was observed in 202 (67.9%) strains. The rate of non-susceptibility to rifampicin, tetracycline, erythromycin, nitrofurantoin, chloramphenicol, and ampicillin was 46%, 26%, 22% and 19%, 13%, 0.3%, and 0.3%, respectively. All strains were susceptible to vancomycin, streptomycin, gentamycin, and linezolid. Forty-three (14.52%) isolates were identified as multidrug resistant (MDR), and the highest number of MDR enterococci were E. faecium recovered from wild monkeys living close to a hospital and water treatment plant. Elevated rates of antibiotic resistance genes msrC and tet(L) were isolates from ZOO. In conclusion, differences in the frequency of enterococci species, antibiotic-nonsusceptible and antibiotic resistance genes in all groups of monkeys were identified. These data suggest that anthropogenic activities could have an impact in the resistome of primate gut enterococci communities.
Highlights
Brazil has the greatest biodiversity on the planet, comprising approximately 103,870 different animal species and the highest diversity of Primates, around 77 species, including the howler monkey, the capuchin monkey, the marmoset, and the tamarin (Brazilian Society of Primatology [SBP], 2016)
E. faecalis (42.6%; n = 126), E. hirae (29.1%; n = 86), and E. faecium (15.9%; n = 47) were detected in all groups of monkeys; and E. durans (6.8%; n = 20), E. casseliflavus (4.4%; n = 13), E. raffinosus (0.3%; n = 1), E. avium (0.3%; n = 1), E. gallinarum (0.3%; n = 1), and Enterococcus sp. (0.3%; n = 1) were occasionally detected in the animals
Whereas E. hirae (47.9%; n = 35), E. faecium (26.0%; n = 19), and E. durans (17.8%; n = 13) were the most abundant species isolated in fecal samples of captive monkeys
Summary
Brazil has the greatest biodiversity on the planet, comprising approximately 103,870 different animal species and the highest diversity of Primates, around 77 species, including the howler monkey, the capuchin monkey, the marmoset, and the tamarin (Brazilian Society of Primatology [SBP], 2016). Sapajus nigritus (black-horned capuchin or black capuchin monkeys) are part of the Cebidae family, characterized as robust capuchin monkeys with adornments or tufts on the head (Rylands et al, 2012) They are considered the largest omnivorous Neotropical primate, which is able to adapt its diet according to food availability, bringing them into contact with a wide diversity of microorganisms. The black capuchin monkeys (S. nigritus) live in different habitats, from large remnants or continuous to small forests fragments Outside of their natural environment, they can be found in zoological, rehabilitation, or research centers, and even in urban and rural environments. Rolland et al (1985) observed that wild baboons (Papio cynocephalus) that fed on human debris, maintained a high proportion of antibiotic-resistant enteric bacteria than those without human contact
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