Absence of intestinal colonization by vancomycin-resistant enterococci in nonhuman primates

Abstract

The animal reservoirs of vancomycin-resistant enterococci (VRE) have important role in the epidemiology of the bacteria and resistant genes. The present work searched fecal samples taken off nonhuman primates for the presence of VRE. Resistance profiles, virulence traits, and genetic variability among enterococci isolates were also analyzed. The samples included Capuchin monkeys (Cebus apella, n=28) and Common marmoset (Callithrix penicillata, n=37) housed in the Primate Center of the University of Brasília, Brazil. Most individuals were captive monkeys from the Central-West and South-East regions of Brazil (n=48). We collected rectal swabs and carried out selective isolation followed by multiplex Polymerase Chain Reaction (PCR) to identify species and resistance genes. No vanA or vanB-containing enterococci were found. The carriage rates ranged from 1.5% for the VanC-type E. casseliflavus and E. gallinarum until 12.3% (n=8) for Enterococcus faecalis. All E. faecalis isolates showed susceptibility to vancomycin, teicoplanin, ampicillin, gentamicin, and streptomycin. The virulence genes ace and esp were prevalent (100.0%, 87.5%). Multilocus variable number of tandem repeats (MLVA) revealed diversity in the number of repeats among E. faecalis isolates and targets, which was higher for espC, efa5, and efa6. We identified six different MLVA genotypes that were divergent from those described in human beings. Also, they were clustered into two genogroups that showed host-specificity for the species Cebus apella or Callithrix penicillata. In conclusion, no vanA-or vanB-containing enterococci were found colonizing those primate individuals. This finding suggested that the primate individuals investigated in our study are not directly involved in the epidemiological chain of high-level vancomycin-resistant genes vanA or vanB in Brazil. Our study also showed that E. faecalis isolated from nonhuman primates carry virulence traits and have ability to spread their lineages among different individuals.

Antimicrobial Resistance Profiles in Enterococcus spp. Isolates From Fecal Samples of Wild and Captive Black Capuchin Monkeys (Sapajus nigritus) in South Brazil

“…Among the species identified in the present study, E. faecalis was predominant. This species was also the most prevalent species in fecal samples of captive capuchin monkeys, common marmoset, domesticated mammals, birds, and wildlife feces, described in previous studies ( Lanthier et al, 2010 ; Xavier et al, 2010 ). Nevertheless, it is important to highlight that some species could be underestimated in the present study due to the limitation of the method on used for enterococci isolation based on culturable methods.…”

“…To date, only a few studies have investigated the distribution of enterococci species in the fecal samples/rectal swabs of wild and captive black capuchin monkeys. The genus Enterococcus was first reported in fecal samples from captive capuchin monkeys ( Cebus apella ) and common marmoset ( Callithrix penicillata ) in the Primate Center of the University of Brasília, Brazil ( Xavier et al, 2010 ). Thereafter, Glover (2014) identified the genus Enterococcus in the fecal samples from the baboons ( Papio ) and vervet monkeys ( Chlorocebus pygerythrus ) in two rehabilitation centers in South Africa.…”

“…The genus Enterococcus consists of over 50 diverse species, and Enterococcus faecalis , E. faecium , E. hirae , E. durans , E. casseliflavus , E. gallinarum , and E. mundtii are the most frequently encountered in the gastrointestinal tracts of animals ( Poeta et al, 2005 ; Cassenego et al, 2011 ; Lozano et al, 2016 ; Medeiros et al, 2017 ). However, the species evaluation in the gastrointestinal tract of primates remains little known ( Xavier et al, 2010 ; Glover, 2014 ). The species distribution, as well as their proportions in the different niche can change according to the host and its age, diet, underlying diseases, and prior antimicrobial therapy ( Lebreton et al, 2014 ).…”

“…To date, few studies have examined the presence of enterococci in monkeys, and these studies have focused primarily on captive animals, perhaps due to the inherent difficulty in obtaining samples from free-living wild animals ( Xavier et al, 2010 ; Glover, 2014 ; Woods et al, 2017 ). The investigation of the persistence of enterococci in these animals highlights the impact of human activities on the environment.…”

Comparison of Multilocus Variable-Number Tandem-Repeat Analysis with Multilocus Sequence Typing and Pulsed-Field Gel Electrophoresis for Enterococcus faecalis

“…a single isolate was negative). For the other five loci espC, espA, efa2, efa3 and efa5, typability was 73.9%, 68.0%, 50.3%, 46.4% and 86.3%, respectively; such incomplete MLVA profiles were found also in other studies on E. faecalis (Titze- de-Almeida et al, 2004;Wałecka et al, 2009;Xavier et al, 2010). Interestingly, the complete MLVA profiles were observed mostly for isolates from infections than from carriage or hospital environment (Fisher exact one-tailed test, p = 0.035), which is in agreement with the fact that the former isolates are enriched in virulence factors (Shankar et al, 1999).…”