1887

Journal of Medical Microbiology logo

Volume 71, Issue 9

Antimicrobial resistance and molecular characterization of gene cassettes from class 1 integrons in strains Open Access

Abstract

The emergence of antibiotic-resistant isolates is a global concern and has been attributed to the indiscriminate use of antibiotics in humans and animals. Integrons are mobile gene elements closely related to bacterial drug resistance. Among them, class 1 integrons containing various resistance gene cassettes could play an important role in disseminating and maintaining antibiotic resistance in isolates.

. class 1 integrons have a relationship with drug resistance.

. This study aims to investigate the distribution of class 1 integrons and their variable regional molecular characteristics, as well as the diversity of the promoters and drug sensitivity among strains.

. A total of 111 strains, collected between 2018 and 2020, underwent fully automated bacterial identification using the VITEK 2 Compact system and an antibiotic sensitivity test. PCR was employed to screen class 1 integrase genes () and integron variable regions, while promoter type and variable region gene cassette characteristics were determined using sequencing analysis.

. A total of 24 -positive strains were detected in 111 strains. Moreover, -positive strains exhibited statistically significant resistance to ceftazidime, ciprofloxacin, levofloxacin ceftriaxone, trimethoprim/sulfamethoxazole and azithromycin compared to integron-negative strains (<0.05). The multidrug resistance rate of -positive strains was significantly higher than that of negative strains. Variable regions were observed in 6 of the 24 -positive strains. Four gene cassettes were detected, namely , , and . Finally, 3 types of class 1 integron variable region promoters were identified in 24 strains, including PcW, PcH1 and PcW; they are all relatively weak promoters.

. The integron and the drug resistance genes carried by integron have a certain relationship with drug resistance.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): antibiotic resistance , class 1 integron , promoters and Salmonella
Funding
This study was supported by the:
  • Health Commission of Weifang (Award No. wfwsjk-2020-031)
    • Principle Award Recipient: MiLiu
  • Health Commission of Weifang (Award wfwsjk-2020-035)
    • Principle Award Recipient: JieMa
© 2022 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001574
2022-09-07
2024-04-29
Loading full text...

Full text loading...

/deliver/fulltext/jmm/71/9/jmm001574.html?itemId=/content/journal/jmm/10.1099/jmm.0.001574&mimeType=html&fmt=ahah

References

  1. White AE, Ciampa N, Chen Y, Kirk M, Nesbitt A et al. Characteristics of Campylobacter and Salmonella infections and acute gastroenteritis in older adults in Australia, Canada, and the United States. Clin Infect Dis 2019; 69:1545–1552 [View Article]
     [Google Scholar]
  2. Marchello CS, Carr SD, Crump JA. A systematic review on antimicrobial resistance among Salmonella Typhi worldwide. Am J Trop Med Hyg 2020; 103:2518–2527 [View Article]
     [Google Scholar]
  3. Mazel D, Dychinco B, Webb VA, Davies J. A distinctive class of integron in the Vibrio cholerae genome. Science 1998; 280:605–608 [View Article]
     [Google Scholar]
  4. Mazel D. Integrons: agents of bacterial evolution. Nat Rev Microbiol 2006; 4:608–620 [View Article]
     [Google Scholar]
  5. Hall RM, Collis CM, Kim MJ, Partridge SR, Recchia GD et al. Mobile gene cassettes and integrons in evolution. Ann N Y Acad Sci 1999; 870:68–80 [View Article] [PubMed]
     [Google Scholar]
  6. Stokes HW, Hall RM. A novel family of potentially mobile DNA elements encoding site-specific gene-integration functions: integrons. Mol Microbiol 1989; 3:1669–1683 [View Article] [PubMed]
     [Google Scholar]
  7. Hall RM, Collis CM. Mobile gene cassettes and integrons: capture and spread of genes by site-specific recombination. Mol Microbiol 1995; 15:593–600 [View Article] [PubMed]
     [Google Scholar]
  8. Cambray G, Guerout AM, Mazel D. Integrons. Annu Rev Genet 2010; 44:141–166 [View Article]
     [Google Scholar]
  9. Ozoline ON, Deev AA, Arkhipova MV. Non-canonical sequence elements in the promoter structure. Cluster analysis of promoters recognized by Escherichia coli RNA polymerase. Nucleic Acids Res 1997; 25:4703–4709 [View Article]
     [Google Scholar]
  10. Jové T, Da Re S, Denis F, Mazel D, Ploy MC. Inverse correlation between promoter strength and excision activity in class 1 integrons. PLoS Genet 2010; 6:e1000793 [View Article] [PubMed]
     [Google Scholar]
  11. Wei Q, Jiang X, Li M, Chen X, Li G et al. Transcription of integron-harboured gene cassette impacts integration efficiency in class 1 integron. Mol Microbiol 2011; 80:1326–1336 [View Article] [PubMed]
     [Google Scholar]
  12. Clinical and Laboratory Standards Institute Perfor-mance Standards for Antimicrobial Susceptibility Testing, 28th edn. Wayne, PA: CLSI; 2018
     [Google Scholar]
  13. Hsu Y-M, Tang C-Y, Lin H, Chen Y-H, Chen Y-L et al. Comparative study of class 1 integron, ampicillin, chloramphenicol, streptomycin, sulfamethoxazole, tetracycline (ACSSuT) and fluoroquinolone resistance in various Salmonella serovars from humans and animals. Comp Immunol Microbiol Infect Dis 2013; 36:9–16 [View Article] [PubMed]
     [Google Scholar]
  14. Hsu SC, Chiu TH, Pang JC, Hsuan-Yuan CH, Chang GN et al. Characterisation of antimicrobial resistance patterns and class 1 integrons among Escherichia coli and Salmonella enterica serovar Choleraesuis strains isolated from humans and swine in Taiwan. Int J Antimicrob Agents 2006; 27:383–391 [View Article] [PubMed]
     [Google Scholar]
  15. Hsueh P-R, Teng L-J, Tseng S-P, Chang C-F, Wan J-H et al. Ciprofloxacin-resistant Salmonella enterica Typhimurium and Choleraesuis from pigs to humans, Taiwan. Emerg Infect Dis 2004; 10:60–68 [View Article] [PubMed]
     [Google Scholar]
  16. Cabrera R, Ruiz J, Marco F, Oliveira I, Arroyo M et al. Mechanism of resistance to several antimicrobial agents in Salmonella clinical isolates causing traveler’s diarrhea. Antimicrob Agents Chemother 2004; 48:3934–3939 [View Article] [PubMed]
     [Google Scholar]
  17. Ke B, Sun J, He D, Li X, Liang Z et al. Serovar distribution, antimicrobial resistance profiles, and PFGE typing of Salmonella enterica strains isolated from 2007-2012 in Guangdong, China. BMC Infect Dis 2014; 14:338 [View Article] [PubMed]
     [Google Scholar]
  18. Chen H-M, Wang Y, Su L-H, Chiu C-H. Nontyphoid Salmonella infection: microbiology, clinical features, and antimicrobial therapy. Pediatr Neonatol 2013; 54:147–152 [View Article] [PubMed]
     [Google Scholar]
  19. Gunell M, Kotilainen P, Jalava J, Huovinen P, Siitonen A et al. In vitro activity of azithromycin against nontyphoidal Salmonella enterica. Antimicrob Agents Chemother 2010; 54:3498–3501 [View Article] [PubMed]
     [Google Scholar]
  20. Malik N, Ahmed M. In vitro effect of new antibiotics against clinical isolates of Salmonella Typhi. J Coll Physicians Surg Pak 2016; 26:288–292 [PubMed]
     [Google Scholar]
  21. Medalla F, Hoekstra RM, Whichard JM, Barzilay EJ, Chiller TM et al. Increase in resistance to ceftriaxone and nonsusceptibility to ciprofloxacin and decrease in multidrug resistance among Salmonella strains, United States, 1996-2009. Foodborne Pathog Dis 2013; 10:302–309 [View Article] [PubMed]
     [Google Scholar]
  22. Peters ED, Leverstein-van Hall MA, Box AT, Verhoef J, Fluit AC. Novel gene cassettes and integrons. Antimicrob Agents Chemother 2001; 45:2961–2964 [View Article] [PubMed]
     [Google Scholar]
  23. Cameron FH, Groot Obbink DJ, Ackerman VP, Hall RM. Nucleotide sequence of the AAD(2’’) aminoglycoside adenylyltransferase determinant aadB. Evolutionary relationship of this region with those surrounding aadA in R538-1 and dhfrII in R388. Nucleic Acids Res 1986; 14:8625–8635 [View Article]
     [Google Scholar]
  24. Randall LP, Cooles SW, Osborn MK, Piddock LJV, Woodward MJ. Antibiotic resistance genes, integrons and multiple antibiotic resistance in thirty-five serotypes of Salmonella enterica isolated from humans and animals in the UK. J Antimicrob Chemother 2004; 53:208–216 [View Article] [PubMed]
     [Google Scholar]
  25. Rowe-Magnus DA, Guerout A-M, Mazel D. Bacterial resistance evolution by recruitment of super-integron gene cassettes. Mol Microbiol 2002; 43:1657–1669 [View Article] [PubMed]
     [Google Scholar]
  26. Japoni-Nejad A, Farshad S, van Belkum A, Ghaznavi-Rad E. Novel cassette array in a class 1 integron in clinical isolates of Acinetobacter baumannii from central Iran. Int J Med Microbiol 2013; 303:645–650 [View Article]
     [Google Scholar]
  27. Sunde M, Simonsen GS, Slettemeås JS, Böckerman I, Norström M et al. Integron, Plasmid and Host Strain Characteristics of Escherichia coli from Humans and Food Included in the Norwegian Antimicrobial Resistance Monitoring Programs. PLoS One 2015; 10:e0128797 [View Article]
     [Google Scholar]
  28. Ali T, Ur Rahman S, Zhang L, Shahid M, Zhang S et al. ESBL-Producing Escherichia coli from Cows Suffering Mastitis in China Contain Clinical Class 1 Integrons with CTX-M Linked to ISCR1. Front Microbiol 2016; 7:1931 [View Article] [PubMed]
     [Google Scholar]
  29. Zhang C-M, Xu L-M, Mou X, Xu H, Liu J et al. Characterization and evolution of antibiotic resistance of Salmonella in municipal wastewater treatment plants. J Environ Manage 2019; 251:109547 [View Article] [PubMed]
     [Google Scholar]
  30. Nesvera J, Hochmannová J, Pátek M. An integron of class 1 is present on the plasmid pCG4 from gram-positive bacterium Corynebacterium glutamicum. FEMS Microbiol Lett 1998; 169:391–395 [View Article]
     [Google Scholar]
  31. Rowe-Magnus DA, Guerout A-M, Mazel D. Bacterial resistance evolution by recruitment of super-integron gene cassettes. Mol Microbiol 2002; 43:1657–1669 [View Article] [PubMed]
     [Google Scholar]
  32. Guérin E, Jové T, Tabesse A, Mazel D, Ploy M-C. High-level gene cassette transcription prevents integrase expression in class 1 integrons. J Bacteriol 2011; 193:5675–5682 [View Article] [PubMed]
     [Google Scholar]
  33. Liu M, Ma J, Jia W, Li W. Antimicrobial resistance and molecular characterization of gene cassettes from class 1 integrons in Pseudomonas aeruginosa strains. Microb Drug Resist 2020; 26:670–676 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.001574
Loading
Antimicrobial resistance and molecular characterization of gene cassettes from class 1 integrons in Salmonella strains
J. Med. Microbiol. 71, 001574 (2022); https://doi.org/10.1099/jmm.0.001574
/content/journal/jmm/10.1099/jmm.0.001574
/content/journal/jmm/10.1099/jmm.0.001574
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error