Detection of Beta-Lactam-Resistant Escherichia coli and Toxigenic Clostridioides difficile Strains in Wild Boars Foraging in an Anthropization Gradient

Abstract

Disease transmission among wild boars, domestic animals and humans is a public health concern, especially in areas with high wild boar densities. In this study, fecal samples of wild boars (n = 200) from different locations of the Metropolitan Area of Barcelona were analyzed by PCR to explore the frequency of β-lactamases and extended cephalosporin and carbapenem resistance genes (ESBLs) in Escherichia coli strains and the presence of toxigenic Clostridioides difficile. The prevalence of genes conferring resistance to β-lactam antimicrobials was 8.0% (16/200): blaCMY-2 (3.0%), blaTEM-1b (2.5%), blaCTX-M-14 (1.0%), blaSHV-28 (1.0%), blaCTX-M-15 (0.5%) and blaCMY-1 (0.5%). Clostridioides difficile TcdA+ was detected in two wild boars (1.0%), which is the first report of this pathogen in wild boars in Spain. Moreover, the wild boars foraging in urban and peri-urban locations were more exposed to AMRB sources than the wild boars dwelling in natural environments. In conclusion, the detection of E. coli carrying ESBL/AmpC genes and toxigenic C. difficile in wild boars foraging in urban areas reinforces the value of this game species as a sentinel of environmental AMRB sources. In addition, these wild boars can be a public and environmental health concern by disseminating AMRB and other zoonotic agents. Although this study provides the first hints of the potential anthropogenic sources of AMR, further efforts should be conducted to identify and control them.

Extended-Spectrum β-Lactam Resistant Klebsiella pneumoniae and Escherichia coli in Wild European Hedgehogs (Erinaceus europeus) Living in Populated Areas

“…Regarding the bacterial isolates, a total of 90 bacterial isolates were identified from those 67 analysed animals, and AMR genes were detected in 52 isolates. Thus, in line with other studies [28,29], we observed that some of the AMRB did not have any of the AMR genes. This could be explained by the possible existence of other mechanisms of resistance such as chromosomal mechanisms that were not included as a target of this study.…”

“…The presence of β-lactamase resistance genes has been historically analysed using E. coli as a marker in livestock [34] and wildlife [35][36][37]. Regarding wildlife, the presence of ESBL genes has been reported principally in wild birds [38][39][40], but also in other species such as bats [41], wild boars [29], and fish [42]. The most commonly detected ESBL genes are CTX-M-1, CTX-M-14, and CTX-M-15, which are also found frequently in hospital settings, suggesting a relationship between bacteria from wildlife and health-care facilities [33].…”

Resistance Patterns, mcr-4 and OXA-48 Genes, and Virulence Factors of Escherichia coli from Apennine Chamois Living in Sympatry with Domestic Species, Italy

“…The phenotypic resistance to cephalosporins has been investigated worldwide and the host taxa that carry cephalosporinases in Europe include birds, mammals, reptiles, fish, and mollusks [ 8 ]. Considering wild mammals, the bla SHV has been reported in Gram-negative bacteria with reduced susceptibility to third-generation cephalosporins from wild boars, European hedgehogs, beech marten, and European badgers in Spain and Italy [ 42 , 43 , 44 ]. The blaTEM gene was reported in resistant E. coli from wild boars in Portugal, Poland, and Spain and it was considered by some authors the most frequent gene conferring resistance to β-lactams [ 43 , 45 , 46 ].…”

“…Considering wild mammals, the bla SHV has been reported in Gram-negative bacteria with reduced susceptibility to third-generation cephalosporins from wild boars, European hedgehogs, beech marten, and European badgers in Spain and Italy [ 42 , 43 , 44 ]. The blaTEM gene was reported in resistant E. coli from wild boars in Portugal, Poland, and Spain and it was considered by some authors the most frequent gene conferring resistance to β-lactams [ 43 , 45 , 46 ]. Otherwise, in Italy, a low prevalence of bla TEM was reported in resistant isolates from wild boars collected in Emilia Romagna and Lombardy regions [ 18 , 44 ].…”

“…Otherwise, in Italy, a low prevalence of bla TEM was reported in resistant isolates from wild boars collected in Emilia Romagna and Lombardy regions [ 18 , 44 ]. Previously, the bla CMY-1 was mainly detected in avian wildlife [ 42 ] and with a low prevalence in resistant E. coli from wild boars in Spain [ 43 ]. Regarding bla CMY-2, it was earlier reported in hedgehogs, roe deer, and American minks in Spain [ 42 ], while in Italy the bla CMY-2 gene was found in wild boars, badgers, wolves, foxes, and mouflons [ 18 , 28 , 44 ].…”