Carbapenemase-producing enterobacteriaceae recovered from a Spanish river ecosystem

Abstract

The increasing resistance to carbapenems is an alarming threat in the fight against multiresistant bacteria. The dissemination properties of antimicrobial resistance genes are supported by their detection in a diverse population of bacteria, including strains isolated from the environment. The objective of this study was to investigate the presence of carbapenemase-producing Enterobacteriaceae (CPE) collected from a river ecosystem in the Barcelona metropolitan area (Spain). Identification of β-lactamases and other resistance determinants was determined as was the antimicrobial susceptibility profile. Moreover, screening of virulence factors, plasmid addiction systems, plasmid partition systems and replicon typing was performed. The results identified 8 isolates belonging to different species (Escherichia coli, Enterobacter cloacae, Klebsiella pneumoniae, Klebsiella oxytoca, Raoultella ornithinolytica). The most prevalent enzyme was KPC-2 (n = 6), followed by VIM-1 (n = 2) and IMI-2 (n = 1), whereas no OXA-48-type was detected. In addition, one strain was positive for both KPC-2 and VIM-1 enzymes. All the carbapenemase-encoding plasmids carried at least one plasmid addiction or partition system, being vagCD and parAB the most frequently detected, respectively. E. coli and K. pneumoniae isolates carried a low number of virulence-associated factors and none of the detected clones has previously been identified in the clinical setting. These findings support the high dissemination potential of the carbapanemase-encoding genes and reinforce the idea that the environment is another reservoir that may play an important role in the capture, selection and dissemination of carbapenem resistance genes.

Prevalence and characterization of carbapenem‐resistant bacteria in water bodies in the Los Angeles–Southern California area

“…Of greater concern is the identification of seven E. asburiae isolates carrying the bla IMI‐2 carbapenemase gene. This gene is an inducible plasmid‐encoded carbapenemase gene that was first identified in carbapenem‐resistant E. asburiae isolates from four different U.S. Midwest rivers (Aubron et al., ), and was later found in an Enterobacter cloacae isolate recovered from river sediment in Spain in 2017 (Piedra‐Carrasco et al., ). bla IMI‐2 has also recently been found in clinical isolates of E. asburiae (Czech Republic) (Rotova et al., ), E. cloacae (China) (Yu, Du, Zhou, Chen, & Li, ), Escherichia coli (Spain and China) (Rojo‐Bezares, Martin, Lopez, Torres, & Saenz, ; Zhang et al., ), and Klebsiella variicola (United Kingdom) (Hopkins, Findlay, Doumith, Mather, & Meunier, ).…”

“…bla IMI‐2 has also recently been found in clinical isolates of E. asburiae (Czech Republic) (Rotova et al., ), E. cloacae (China) (Yu, Du, Zhou, Chen, & Li, ), Escherichia coli (Spain and China) (Rojo‐Bezares, Martin, Lopez, Torres, & Saenz, ; Zhang et al., ), and Klebsiella variicola (United Kingdom) (Hopkins, Findlay, Doumith, Mather, & Meunier, ). In both environmental and clinical isolates, bla IMI‐2 was usually found in transposable elements located in transferable plasmids (Aubron et al., ; Hopkins et al., ; Piedra‐Carrasco et al., ; Rojo‐Bezares et al., ; Rotova et al., ; Yu et al., ; Zhang et al., ); however, one E. asburiae clinical isolate carrying the bla IMI‐2 gene in its chromosome (the transposable element was not characterized) was identified in South Africa in 2015 (Gqunta et al., ). Our results show that this acquired carbapenemase gene is also spread outside of clinical and river environments, which may be related to the presence of bla IMI‐2 in transposable elements located in transferable plasmids (Aubron et al., ; Hopkins et al., ; Piedra‐Carrasco et al., ; Rojo‐Bezares et al., ; Rotova et al., ; Yu et al., ; Zhang et al., ).…”

“…In both environmental and clinical isolates, bla IMI‐2 was usually found in transposable elements located in transferable plasmids (Aubron et al., ; Hopkins et al., ; Piedra‐Carrasco et al., ; Rojo‐Bezares et al., ; Rotova et al., ; Yu et al., ; Zhang et al., ); however, one E. asburiae clinical isolate carrying the bla IMI‐2 gene in its chromosome (the transposable element was not characterized) was identified in South Africa in 2015 (Gqunta et al., ). Our results show that this acquired carbapenemase gene is also spread outside of clinical and river environments, which may be related to the presence of bla IMI‐2 in transposable elements located in transferable plasmids (Aubron et al., ; Hopkins et al., ; Piedra‐Carrasco et al., ; Rojo‐Bezares et al., ; Rotova et al., ; Yu et al., ; Zhang et al., ). Further, surveillance is necessary to better characterize the role of freshwater environments as a source of IMI‐2‐producing E. asburiae , which can be both an opportunistic pathogen, as well as a reservoir of this transferable carbapenemase.…”

Plasmid evolution in carbapenemase‐producing Enterobacteriaceae: a review

“…Within this group, three subgroups with similar plasmid scaffolds but less similarity in backbone sequences have been described: IncN1 (R46), IncN2 (p271A), and IncN3 (pN‐Cit); these characteristics might be the reason for their stability and success in disseminating multiple carbapenemases. IncN plasmids are usually medium‐sized conjugative plasmids documented to be associated with bla VIM ‐expressing Enterobacteriaceae and bla KPC ‐expressing K. pneumoniae isolates . Plasmids, including p9 (70.6 kb), p12 (75.6 kb), pKPC‐629 (80.1 kb), pBK31551 (83.7 kb), pKO6 (65.5 kb), and pKp58‐N (69.8 kb), have been documented as carriers of bla KPC .…”

“…Moreover, these plasmid replicon groups are also associated with K. pneumoniae strains producing other carbapenemases. VIM has been only reported by two studies in Italy and Kuwait to be hosted by IncN and A/C …”