Epidemic IncX3 plasmids spreading carbapenemase genes in the United Arab Emirates and worldwide

Shaimaa F Mouftah; Tibor Pál; Dania Darwish; Akela Ghazawi; Laura Villa; Alessandra Carattoli; Ágnes Sonnevend

doi:10.2147/IDR.S210554

Epidemic IncX3 plasmids spreading carbapenemase genes in the United Arab Emirates and worldwide

Infect Drug Resist. 2019 Jun 21:12:1729-1742. doi: 10.2147/IDR.S210554. eCollection 2019.

Authors

Shaimaa F Mouftah^#¹, Tibor Pál^#¹, Dania Darwish¹, Akela Ghazawi¹, Laura Villa², Alessandra Carattoli³, Ágnes Sonnevend^{1

4}

Affiliations

¹ Department of Medical Microbiology and Immunology, College of Medicine and Health Sciences, United Arab Emirates University, Al Ain, United Arab Emirates.
² Department of Infectious Diseases, Istituto Superiore di Sanitá, Rome, Italy.
³ Department of Molecular Microbiology, University of Rome La Sapienza, Rome, Italy.
⁴ Department of Medical Microbiology and Immunology, Medical School, University of Pécs, Pécs, Hungary.

^# Contributed equally.

Abstract

Purpose: Plasmids of the incompatibility group X type 3 (IncX3) were described carrying various carbapenemase genes in carbapenemase-producing Enterobacteriaceae (CPE) worldwide and in the United Arab Emirates (UAE), as well. To understand the driving force behind the emergence of such plasmids in the UAE, the relationship between IncX3 plasmids encountered locally and globally was investigated.

Methods: CPE strains isolated in the UAE during 2009-2014 were screened by X3 PCR-based replicon typing. The clonal relationship of CPE carrying IncX3 plasmids was determined by multi-locus sequence typing (MLST) and pulsed-field gel electrophoresis (PFGE). Complete sequence of selected IncX3 plasmids was determined. Phylogenetic relationship between the carbapenemase carrying IncX3 plasmids from the UAE and of those reported worldwide was established by comparing the plasmid backbones.

Results: 10.2% of the 295 CPE tested were identified to carry IncX3 plasmids: 13 Escherichia coli, 13 Klebsiella pneumoniae, two Enterobacter cloacae, one Citrobacter freundii and one Morganella morganii isolate, respectively. Most of them were non-clonal; with small clusters of triplets and pairs of E. coli and K. pneumoniae, and a cluster of five K. pneumoniae ST11 exhibiting >90% similar PFGE patterns, respectively. The 30 isolates harbored either bla _NDM-1, bla _NDM-4, bla _NDM-5, bla _NDM-7, bla _OXA-181 or bla _KPC-2 carbapenemase genes on IncX3 plasmids. Phylogenetic analysis of the backbone region of IncX3 plasmids carrying various beta-lactamase genes from the UAE (n=23) and that of North-America, Europe, Asia and Australia (n=35) revealed three clusters based on the carbapenemase genes carried: plasmids harboring bla _OXA-181 and bla _NDM-5 formed two distinct groups, whereas backbones of plasmids with bla _NDM-1, bla _NDM-4 and bla _NDM-7 clustered together. Each cluster contained plasmids of diverse geographical origin.

Conclusion: The findings suggest that different carbapenemase gene carrying IncX3 plasmids encountered in the UAE do not evolve locally, rather are subtypes of this epidemic plasmid emerging in this country due to international transfer.

Keywords: Enterobacterales; IncX3 plasmid; Middle-East; carbapenemase genes.