Skip to main content
Log in

Relationship between antibiotic resistance with class 1 integron and SmeDEF efflux pump encoding genes in clinical isolates of Stenotrophomonas maltophilia

  • Microbial Genetics • Original Paper
  • Published:
Journal of Applied Genetics Aims and scope Submit manuscript

Abstract

Stenotrophomonas maltophilia is an emerging multidrug-resistant organism with an increasing frequency of hospital-acquired infections predominantly in developing countries. The purpose of this study was to determine the antibiotic resistance and frequency of the smeD, class 1 integron, and sul1 genes in clinical isolates of S. maltophilia in two Iranian provinces. From January 2020 to September 2021, 38 clinical isolates of S. maltophilia were collected from patients in hospitals in Tabriz and Sanandaj provinces of Iran. S. maltophilia isolates were confirmed by standard bacteriological tests and 16S rRNA gene PCR. Disk diffusion and the MIC test strip methods were used to determine the antibiotic resistance patterns. PCR was performed to investigate the presence of smeD, class 1 integron, and sul1 genes. The antimicrobial test for the isolated S. maltophilia showed a high level of sensitivity against most of the antibiotics used. Maximum sensitivity was recorded for ciprofloxacin (100% (38/38)) and levofloxacin 100% (38/38), followed by ceftazidime (97.36% (37/38)), trimethoprim-sulfamethoxazole (81.57% (31/38)), ticarcillin-clavulanate (60.52% (23/38)), and piperacillin-tazobactam (55.26% (21/38)). We observed a high prevalence of smeD (100% (38/38)) and class 1 integron (94.73% (36/38)) genes in the isolates, and none of the isolates carried the sul1 gene. The findings from this study indicate that resistance to trimethoprim-sulfamethoxazole was not observed, and still, trimethoprim-sulfamethoxazole is the best drug with desirable antimicrobial effect in the treatment of nosocomial infections caused by S. maltophilia strains. Despite the observation of a high number of class 1 integron, the sul1 gene was not observed, which indicates the role of this gene in high-level trimethoprim-sulfamethoxazole resistance and not having a role in low-level resistance. Based on our results, clinical microbiology laboratories need continuous surveillance of resistance rates to trimethoprim-sulfamethoxazole, because of the possibility of S. maltophilia acquiring trimethoprim-sulfamethoxazole-resistance by mobile gen elements.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this published article. The datasets used and/or analyzed during the current study are available from the corresponding authors on reasonable request.

References

  • Alonso A, Martinez JL (2000) Cloning and characterization of SmeDEF, a novel multidrug efflux pump from Stenotrophomonas maltophilia. Antimicrob Agents Chemother 44(11):3079–3086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Azimi A et al (2021) Emergence of fluoroquinolone resistance and possible mechanisms in clinical isolates of Stenotrophomonas maltophilia from Iran. Sci Rep 11(1):9582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barbolla R et al (2004) Class 1 integrons increase trimethoprim-sulfamethoxazole MICs against epidemiologically unrelated Stenotrophomonas maltophilia isolates. Antimicrob Agents Chemother 48(2):666–669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baseri Z et al (2021) Prevalence of resistance genes and antibiotic resistance profile among Stenotrophomonas maltophilia isolates from hospitalized patients in Iran. New Microbes New Infect 44:100943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Betts J et al (2014) Activity of colistin in combination with tigecycline or rifampicin against multidrug-resistant Stenotrophomonas maltophilia. Eur J Clin Microbiol Infect Dis 33(9):1565–1572

    Article  CAS  PubMed  Google Scholar 

  • Bostanghadiri N et al (2019) Characterization of phenotypic and genotypic diversity of Stenotrophomonas maltophilia strains isolated from selected hospitals in Iran. Front Microbiol 10:1191. https://doi.org/10.3389/fmicb.2019.0119110

  • Chong SY et al (2017) Levofloxacin efflux and smeD in clinical isolates of Stenotrophomonas maltophilia. Microb Drug Resist 23(2):163–168

    Article  CAS  PubMed  Google Scholar 

  • Chung HS et al (2015b) The sul1 gene in Stenotrophomonas maltophilia with high-level resistance to trimethoprim/sulfamethoxazole. Ann Lab Med 35(2):246–249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chung H-S et al (2015a) The sul1 gene in Stenotrophomonas maltophilia with high-level resistance to trimethoprim/sulfamethoxazole. Ann Lab Med 35(2):246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crossman LC et al (2008) The complete genome, comparative and functional analysis of Stenotrophomonas maltophilia reveals an organism heavily shielded by drug resistance determinants. Genome Biol 9(4):R74

    Article  PubMed  PubMed Central  Google Scholar 

  • Denton M, Kerr KG (1998) Microbiological and clinical aspects of infection associated with Stenotrophomonas maltophilia. Clin Microbiol Rev 11(1):57–80

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ebrahim-Saraie HS et al (2019) Prevalence of antibiotic resistance and integrons, sul and Smqnr genes in clinical isolates of Stenotrophomonas maltophilia from a tertiary care hospital in Southwest Iran. Iran J Basic Med Sci 22(8):872

    PubMed  PubMed Central  Google Scholar 

  • EUCAST (2015) The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters, Version 5.0. http://www.eucast.org

  • Fu et al (2022) Characteristics and influencing factors for Stenotrophomonas maltophilia infection in a tertiary general hospital of Sanya City and drug resistance from 2016 to 2020. Chin J Nosocomiology 32(10):1464–1467

  • Gordon N, Wareham D (2010) Novel variants of the Sm qnr family of quinolone resistance genes in clinical isolates of Stenotrophomonas maltophilia. J Antimicrob Chemother 65(3):483–489

    Article  CAS  PubMed  Google Scholar 

  • Gould VC, Avison MB (2006) SmeDEF-mediated antimicrobial drug resistance in Stenotrophomonas maltophilia clinical isolates having defined phylogenetic relationships. J Antimicrob Chemother 57(6):1070–1076

    Article  CAS  PubMed  Google Scholar 

  • Gozel MG, Celik C, Elaldi N (2015) Stenotrophomonas maltophilia infections in adults: primary bacteremia and pneumonia. Jundishapur J Microbiol 8(8):e23569

  • Hu LF et al (2011a) Stenotrophomonas maltophilia resistance to trimethoprim/sulfamethoxazole mediated by acquisition of sul and dfrA genes in a plasmid-mediated class 1 integron. Int J Antimicrob Agents 37(3):230–234

    Article  CAS  PubMed  Google Scholar 

  • Hu L-F et al (2011b) Stenotrophomonas maltophilia resistance to trimethoprim/sulfamethoxazole mediated by acquisition of sul and dfrA genes in a plasmid-mediated class 1 integron. Int J Antimicrob Agents 37(3):230–234

    Article  CAS  PubMed  Google Scholar 

  • Hu L-F et al (2016) Increase in the prevalence of resistance determinants to trimethoprim/sulfamethoxazole in clinical Stenotrophomonas maltophilia isolates in China. PloS One 11(6):e0157693

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang Y-W et al (2015) The contribution of class 1 integron to antimicrobial resistance in Stenotrophomonas maltophilia. Microb Drug Resist 21(1):90–96

    Article  CAS  PubMed  Google Scholar 

  • Huang Y-W et al (2017) Overexpression of SmeDEF efflux pump decreases aminoglycoside resistance in Stenotrophomonas maltophilia. Antimicrob Agents Chemother 61(5):e02685–e02616

    Article  PubMed  PubMed Central  Google Scholar 

  • Ince N et al (2020) An evaluation of six-year Stenotrophomonas maltophilia infections in a university hospital. Afr Health Sci 20(3):1118–1123

    Article  PubMed  PubMed Central  Google Scholar 

  • Insuwanno W, Kiratisin P, Jitmuang A (2020) Stenotrophomonas maltophilia infections: clinical characteristics and factors associated with mortality of hospitalized patients. Infect Drug Resist 13:1559–1566

  • Jamali F et al (2011) Minimal inhibitory concentration of ceftazidime and co-trimoxazole for Stenotrophomonas maltophilia using E-test. J Glob Infect 3(3):254

    Article  CAS  Google Scholar 

  • Jia W et al (2015) Resistance of Stenotrophomonas maltophilia to fluoroquinolones: prevalence in a university hospital and possible mechanisms. Int J Environ Res Public Health 12(5):5177–5195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang X-M et al (2015) Genome-wide identification of genes necessary for biofilm formation by nosocomial pathogen Stenotrophomonas maltophilia reveals that orphan response regulator FsnR is a critical modulator. Appl Environ Microbiol 81(4):1200–1209

    Article  PubMed  PubMed Central  Google Scholar 

  • Liaw SJ, Lee YL, Hsueh PR (2010) Multidrug resistance in clinical isolates of Stenotrophomonas maltophilia: roles of integrons, efflux pumps, phosphoglucomutase (SpgM), and melanin and biofilm formation. Int J Antimicrob Agents 35(2):126–130

    Article  CAS  PubMed  Google Scholar 

  • Looney WJ, Narita M, Mühlemann K (2009a) Stenotrophomonas maltophilia: an emerging opportunist human pathogen. Lancet Infect Dis 9(5):312–323

    Article  CAS  PubMed  Google Scholar 

  • Looney WJ, Narita M, Muhlemann K (2009b) Stenotrophomonas maltophilia: an emerging opportunist human pathogen. Lancet Infect Dis 9(5):312–323

    Article  CAS  PubMed  Google Scholar 

  • Millar BC et al (2000) A simple and sensitive method to extract bacterial, yeast and fungal DNA from blood culture material. J Microbiol Methods 42(2):139–147

    Article  CAS  PubMed  Google Scholar 

  • Namaei MH et al (2021) High prevalence of multidrug-resistant non-fermentative Gram-negative bacilli harboring blaIMP-1 and blaVIM-1 metallo-beta-lactamase genes in Birjand, south-east Iran. Iran J Microbiol 13(4):470

    PubMed  PubMed Central  Google Scholar 

  • Pak TR et al (2015) Whole-genome sequencing identifies emergence of a quinolone resistance mutation in a case of Stenotrophomonas maltophilia bacteremia. Antimicrob Agents Chemother 59(11):7117–7120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Papadimitriou-Olivgeris M et al (2022) Clonal dissemination and resistance genes among Stenotrophomonas maltophilia in a Greek University Hospital during a four-year period. AIMS Microbiology 8(3):292

    Article  PubMed  PubMed Central  Google Scholar 

  • Performance C (2017) Standards for antimicrobial susceptibility testing. CLSI Supplement M100:29

    Google Scholar 

  • Pinot C et al (2011) Identification of Stenotrophomonas maltophilia strains isolated from environmental and clinical samples: a rapid and efficient procedure. J Appl Microbiol 111(5):1185–1193

    Article  CAS  PubMed  Google Scholar 

  • Sanchez MB, Hernandez A, Martinez JL (2009) Stenotrophomonas maltophilia drug resistance. Future Microbiol 4(6):655–660

    Article  CAS  PubMed  Google Scholar 

  • Sánchez MB et al (2016) Antimicrobial drug efflux pumps in Stenotrophomonas maltophilia. In: Xian-Zhi L (ed) Efflux-mediated antimicrobial resistance in bacteria, 1st edn. Springer, pp 401–416. https://doi.org/10.1007/978-3-319-39658-3

  • Srivastava S et al (2022) Infection trends, susceptibility pattern, and treatment options for Stenotrophomonas maltophilia infections in trauma patients: a retrospective study. J Lab Physicians 15(1):106–109. https://doi.org/10.1055/s-0042-1757413

  • Tan C-K et al (2008) Extensively drug-resistant Stenotrophomonas maltophilia in a tertiary care hospital in Taiwan: microbiologic characteristics, clinical features, and outcomes. Diagn Microbiol Infect Dis 60(2):205–210

    Article  CAS  PubMed  Google Scholar 

  • Toleman MA et al (2007) Global emergence of trimethoprim/sulfamethoxazole resistance in Stenotrophomonas maltophilia mediated by acquisition of sul genes. Emerg Infect Dis 13(4):559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watson L et al (2018) Sulfamethoxazole/trimethoprim versus fluoroquinolones for the treatment of Stenotrophomonas maltophilia bloodstream infections. J Glob Antimicrob Resist 12:104–106

    Article  PubMed  Google Scholar 

  • Zhang L, Li XZ, Poole K (2001) SmeDEF multidrug efflux pump contributes to intrinsic multidrug resistance in Stenotrophomonas maltophilia. Antimicrob Agents Chemother 45(12):3497–3503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to thank all the members of the microbiology laboratory of Hamadan, Tabriz and Sanandaj University of medical sciences, Iran.

Funding

The design of the study and collection, analysis, interpretation of data, and writing the manuscript was supported by a grant (grant number: 9612228413) from Vice chancellor of research and Technology of Hamadan University of Medical Sciences, Hamadan, Iran.

Author information

Authors and Affiliations

Authors

Contributions

MYA conceived and designed the experiments, SBZ and MN performed the experiments, and MYA and RYM and HS analyzed the data. MYA and SB wrote the manuscript. All authors reviewed and approved the manuscript.

Corresponding authors

Correspondence to Mohammad Yousef Alikhani or Safar Farajnia.

Ethics declarations

Consent to participate was not applicable to this study because the isolates in the study were obtained from existing clinical collections routinely collected as part of tertiary hospital laboratory practices. Clinical strains of S. maltophilia were obtained with the permission of the head of the hospital laboratory.

Ethics approval

The current study was approved by the research ethics committee of Hamadan University of Medical Sciences, Hamadan, Iran (ID: IR.UMSHA. REC.1396.918).

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Communicated by: Agnieszka Szalewska-Palasz

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bafandeh Zamanpour, S., Yousefi Mashouf, R., Salimizand, H. et al. Relationship between antibiotic resistance with class 1 integron and SmeDEF efflux pump encoding genes in clinical isolates of Stenotrophomonas maltophilia. J Appl Genetics 64, 591–597 (2023). https://doi.org/10.1007/s13353-023-00776-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13353-023-00776-6

Keywords

Navigation