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Front. Microbiol. | doi: 10.3389/fmicb.2019.01191

Characterization of Phenotypic and Genotypic diversity of Stenotrophomonas maltophilia Strains Isolated from Selected Hospitals in Iran

Narjess Bostanghadiri1, Zohreh Ghalavand1, Fatemeh Fallah1,  Abbas Yadegar1,  Samira Tarashi2, Abazar Pournajaf3, Jalal Mardaneh4, Saeed Shams5, Abdollah Ardebili6 and  Ali Hashemi1*
  • 1Foodborne and Waterborne Diseases Research Center, Research Institute for Gastroenterology and Liver Diseases, Shahid Beheshti University of Medical Sciences, Iran
  • 2Department of Mycobacteriology and Pulmonary Research, Pasteur Institute of Iran (PII), Iran
  • 3Department of Microbiology, School of Medicine, Babol University of Medical Sciences, Iran
  • 4Microbiology Department, School of Medicine, Gonabad University of Medical Sciences, Iran
  • 5Cellular & Molecular Research Center, Qom University of Medical Sciences, Iran
  • 6Department of Microbiology, Faculty of Medicine, Golestan University of Medical Sciences, Iran

The purpose of this study was to determine the phenotypic and genotypic characterization of S. maltophilia isolates recovered from patients referred to several hospitals. A total of 164 clinical isolates of S. maltophilia were collected from hospitals in various regions in Iran between 2016 and 2017. Antibiotic susceptibility testing was performed by disc diffusion method and E-test assay according to the Clinical and Laboratory Standards Institute(CLSI) guideline. The ability of biofilm formation was assessed with crystal violet staining and then, biofilm-associated genes were investigated by PCR-sequencing method. The presence of L1 (a metallo-β-lactamase), L2(a clavulanic acid-sensitive cephalosporinase), sul1 and sul2 (resistance to Trimethoprim/Sulfamethoxazole),Smqnr (intrinsic resistance to quinolones) and dfrA genes (dihydrofolate reductase enzyme that contributes to trimethoprim resistance) was also examined by PCR-sequencing. Relative gene expression of smeDEF efflux pump was assessed by real-time PCR. Genotyping was performed using the multi-locus sequencing typing (MLST) and repetitive extragenic palindromic-PCR (Rep-PCR).Isolates were resistant to imipenem (100%),meropenem (96 %),doripenem (96%),and ceftazidime (36.58%). Notably, 5 (3.04%) isolates showed resistant to trimethoprim-sulfamethoxazole (TMP-SMX), an alarming trend of decreased susceptibility to TMP-SMX in Iran. Minocycline and levofloxacin exhibited the highest susceptibility of 91.46% and 99.39%, respectively. Using the crystal violet staining, 157(95.73%) isolates had biofilm phenotype: 49 (29.87%), 63 (38.41%), and 45 (27.43%) isolates were categorized as strong-, moderate- and weak-biofilm producer while 7 isolates (4.26%) were identified a non-biofilm producer. Biofilm genes had an overall prevalence of 145(88.41%), 137(83.53%),and 164(100%) of rmlA, rpfF and spgM, respectively. L1, L2, Smqnr, sul1, and sul2 resistance genes were detected in 145(88.41%), 156(96.12%), 103(62.80%), 89 (54.26%), 92 (56.09%) isolates, respectively. None of the S. maltophilia isolates were positive for dfrA12, dfrA17, and dfrA27 genes. Gene expression analysis showed that smeD efflux system was overexpressed in 2 out of the 5 clinical isolates (40%) that showed resistance to TMP-SMX. Most of the isolates were genetically unrelated. Two new sequence types(ST139 and ST259) were determined. Our results showed that TMP-SMX was still an effective antibiotic against S. maltophilia. The findings of the current study revealed an increasing prevalence of antibiotic resistance and biofilm genes in clinical S. maltophilia isolates in Iran.

Keywords: Stenotrophomonas maltophilia, Trimethoprim-sulfamethoxazole (TMP-SMX), Biofilm, antibiotic resistance genes, efflux pump, sequence type

Received: 17 Mar 2018; Accepted: 10 May 2019.

Edited by:

Gilberto Igrejas, University of Trás-os-Montes and Alto Douro, Portugal

Reviewed by:

Xu Jia, Chengde Medical College, China
Leila Vali, Kuwait University, Kuwait
Jason Sahl, Northern Arizona University, United States  

Copyright: © 2019 Bostanghadiri, Ghalavand, Fallah, Yadegar, Tarashi, Pournajaf, Mardaneh, Shams, Ardebili and Hashemi. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: PhD. Ali Hashemi, Shahid Beheshti University of Medical Sciences, Foodborne and Waterborne Diseases Research Center, Research Institute for Gastroenterology and Liver Diseases, Tehran, Iran, ali.hashemi@sbmu.ac.ir