Annals of Laboratory Medicine

Korean Society for Laboratory Medicine (대한진단검사의학회)
권호 표지
DOI QR코드

DOI QR Code

Molecular Epidemiology of Integron-Associated Antimicrobial Gene Cassettes in the Clinical Isolates of Acinetobacter baumannii from Northern Taiwan

  • Lin, Ming-Feng (Department of Medicine, National Taiwan University Hospital Chu-Tung Branch) ;
  • Liou, Ming-Li (Department of Computer Science and Information Engineering, Providence University) ;
  • Tu, Chi-Chao (Department of Medical Laboratory Science and Biotechnology, Yuanpei University) ;
  • Yeh, Hui-Wen (Laboratory Medicine Division, National Taiwan University Hospital Hsin-Chu Branch) ;
  • Lan, Chung-Yu (Institute of Molecular and Cellular Biology, National Tsing Hua University)
  • Published : 2013.07.01
⟨ Previous Next ⟩

Abstract

Background: The aims of this study were to understand the molecular epidemiology of integron-associated gene cassettes in Acinetobacter baumannii across four hospitals in northern Taiwan and to clarify the relationship between the presence of integrons and antibiotic-resistant phenotypes. Methods: Sixty-five A. baumannii isolates, collected from the patients of four regional hospitals in northern Taiwan in 2009, were tested for the presence of integrons and their associated gene cassettes. The susceptibility difference between integron-positive and integron-negative A. baumannii strains was analyzed. Antibiotic-resistant phenotypes among A. baumannii with different types of gene cassette array combinations were also compared. Results: Around 72% of the A. baumannii isolates carried class 1 integrase genes. Despite this, only three gene cassette arrays were found in the integrons. Integron-positive strains were significantly more resistant to all the tested antibiotics than the integrase-negative strains. All the four types of A. baumannii with different gene cassette array combinations were multidrug-resistant in nature. Gene cassette array aacA4-catB8-aadA1 existed in all the integron-positive A. baumannii isolates. Repetitive-sequence-based PCR (rep-PCR) results revealed the prevalence of one major cluster of imipenem-resistant A. baumannii strains (84%) in the four regional hospitals. Conclusions: The presence of integrons with associated antimicrobial resistance gene cassettes can be used as a representative marker of multidrug resistance in A. baumannii. Some prevalent gene cassette arrays may exist among epidemiologically unrelated A. baumannii strains.

Keywords

References

  1. Perez F, Hujer AM, Hujer KM, Decker BK, Rather PN, Bonomo RA. Global challenge of multidrug-resistant Acinetobacter baumannii. Antimicrob Agents Chemother 2007;51:3471-84. https://doi.org/10.1128/AAC.01464-06
  2. Peleg AY, Seifert H, Paterson DL. Acinetobacter baumannii: emergence of a successful pathogen. Clin Microbiol Rev 2008;21:538-82. https://doi.org/10.1128/CMR.00058-07
  3. Valenzuela JK, Thomas L, Partridge SR, van der Reijden T, Dijkshoorn L, Iredell J. Horizontal gene transfer in a polyclonal outbreak of carbapenem-resistant Acinetobacter baumannii. J Clin Microbiol 2007;45:453-60. https://doi.org/10.1128/JCM.01971-06
  4. Carattoli A. Importance of integrons in the diffusion of resistance. Vet Res 2001;32:243-59. https://doi.org/10.1051/vetres:2001122
  5. Mazel D. Integrons: agents of bacterial evolution. Nat Rev Microbiol 2006;4:608-20. https://doi.org/10.1038/nrmicro1462
  6. Gu B, Tong M, Zhao W, Liu G, Ning M, Pan S, et al. Prevalence and characterization of class I integrons among Pseudomonas aeruginosa and Acinetobacter baumannii isolates from patients in Nanjing, China. J Clin Microbiol 2007;45:241-3. https://doi.org/10.1128/JCM.01318-06
  7. Huang LY, Chen TL, Lu PL, Tsai CA, Cho WL, Chang FY, et al. Dissemination of multidrug-resistant, class 1 integron-carrying Acinetobacter baumannii isolates in Taiwan. Clin Microbiol Infect 2008;14:1010-9. https://doi.org/10.1111/j.1469-0691.2008.02077.x
  8. Turton JF, Kaufmann ME, Glover J, Coelho JM, Warner M, Pike R, et al. Detection and typing of integrons in epidemic strains of Acinetobacter baumannii found in the United Kingdom. J Clin Microbiol 2005;43:3074-82. https://doi.org/10.1128/JCM.43.7.3074-3082.2005
  9. Chen TL, Siu LK, Wu RC, Shaio MF, Huang LY, Fung CP, et al. Comparison of one-tube multiplex PCR, automated ribotyping and intergenic spacer (ITS) sequencing for rapid identification of Acinetobacter baumannii. Clin Microbiol Infect 2007;13:801-6. https://doi.org/10.1111/j.1469-0691.2007.01744.x
  10. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Disk Susceptibility Tests. Approved Standards-Tenth edition, M02-A10. Wayne, PA: Clinical and Laboratory Standards Institute, 2009.
  11. Koeleman JG, Stoof J, Van Der Bijl MW, Vandenbroucke-Grauls CM, Savelkoul PH. Identification of epidemic strains of Acinetobacter baumannii by integrase gene PCR. J Clin Microbiol 2001;39:8-13. https://doi.org/10.1128/JCM.39.1.8-13.2001
  12. Vincze T, Posfai J, Roberts, R.J. NEBcutter: a program to cleave DNA with restriction enzymes. Nucleic Acids Res 2003;31:3688-91. https://doi.org/10.1093/nar/gkg526
  13. Misbah S, AbuBakar S, Hassan H, Hanifah YA, Yusof MY. Antibiotic susceptibility and REP-PCR fingerprints of Acinetobacter spp. isolated from a hospital ten years apart. J Hosp Infect 2004;58:254-61. https://doi.org/10.1016/j.jhin.2004.07.007
  14. Gaur A, Prakash P, Anupurba S, Mohapatra TM. Possible role of integrase gene polymerase chain reaction as an epidemiological marker: study of multidrug-resistant Acinetobacter baumannii isolated from nosocomial infections. Int J Antimicrob Agents 2007;29:446-50. https://doi.org/10.1016/j.ijantimicag.2006.11.014
  15. Gallego L and Towner KJ. Carriage of class 1 integrons and antibiotic resistance in clinical isolates of Acinetobacter baumannii from northern Spain. J Med Microbiol 2001;50:71-7.
  16. Gombac F, Riccio ML, Rossolini GM, Lagatolla C, Tonin E, Monti-Bragadin C, et al. Molecular characterization of integrons in epidemiologically unrelated clinical isolates of Acinetobacter baumannii from Italian hospitals reveals a limited diversity of gene cassette arrays. Antimicrob Agents Chemother 2002;46:3665-8. https://doi.org/10.1128/AAC.46.11.3665-3668.2002
  17. Sung JY, Kwon KC, Cho HH, Koo SH. Antimicrobial resistance determinants in imipenem-nonsusceptible Acinetobacter calcoaceticus-baumannii complex isolated in Daejeon, Korea. Korean J Lab Med 2011;31:265-70. https://doi.org/10.3343/kjlm.2011.31.4.265
  18. Seifert H, Dolzani L, Bressan R, van der Reijden T, van Strijen B, Stefanik D, et al. Standardization and interlaboratory reproducibility assessment of pulsed-field gel electrophoresis-generated fingerprints of Acinetobacter baumannii. J Clin Microbiol 2005;43:4328-35. https://doi.org/10.1128/JCM.43.9.4328-4335.2005
  19. Bartual SG, Seifert H, Hippler C, Luzon MA, Wisplinghoff H, Rodriguez-Valera F. Development of a multilocus sequence typing scheme for characterization of clinical isolates of Acinetobacter baumannii. J Clin Microbiol 2005;43:4382-90. https://doi.org/10.1128/JCM.43.9.4382-4390.2005
  20. Higgins PG, Hujer AM, Hujer KM, Bonomo RA, Seifert H. Interlaboratory reproducibility of DiversiLab rep-PCR typing and clustering of Acinetobacter baumannii isolates. J Med Microbiol 2012;61:137-41. https://doi.org/10.1099/jmm.0.036046-0
  21. Higgins PG, Janssen K, Fresen MM, Wisplinghoff H, Seifert H. Molecular epidemiology of Acinetobacter baumannii bloodstream isolates obtained in the United States from 1995 to 2004 using rep-PCR and multilocus sequence typing. J Clin Microbiol 2012;50:3493-500. https://doi.org/10.1128/JCM.01759-12
  22. Lin MF, Chang KC, Yang CY, Yang CM, Xiao CC, Kuo HY, et al. Role of integrons in antimicrobial susceptibility patterns of Acinetobacter baumannii. Jpn J Infect Dis 2010;63:440-3.
  23. Zhong Q, Xu W, Wu Y, Xu H. Clonal spread of carbapenem non-susceptible Acinetobacter baumannii in an intensive care unit in a teaching hospital in China. Ann Lab Med 2012;32:413-9. https://doi.org/10.3343/alm.2012.32.6.413
  24. Nemec A, Dolzani L, Brisse S, van den Broek P, Dijkshoorn L. Diversity of aminoglycoside-resistance genes and their association with class 1 integrons among strains of pan-European Acinetobacter baumannii clones. J Med Microbiol 2004;53:1233-40. https://doi.org/10.1099/jmm.0.45716-0
  25. Lee YT, Huang LY, Chen TL, Siu LK, Fung CP, Cho WL, et al. Gene cassette arrays, antibiotic susceptibilities, and clinical characteristics of Acinetobacter baumannii bacteremic strains harboring class 1 integrons. J Microbiol Immunol Infect 2009;42:210-9.
  26. Su CH, Wang JT, Hsiung CA, Chien LJ, Chi CL, Yu HT, et al. Increase of carbapenem-resistant Acinetobacter baumannii infection in acute care hospitals in Taiwan: association with hospital antimicrobial usage. PLoS One 2012;7:e37788. https://doi.org/10.1371/journal.pone.0037788
  27. Chen YS, Lin HH, Wu CH, Hsiao YS, Hsu NS, Chen YL. Colonization of a medical center in Southern Taiwan by epidemic strains of carbapenem- and multidrug-resistant Acinetobacter baumannii and the genetic organization of their integrons. Jpn J Infect Dis 2009;62:155-7.
  28. Lin MF, Chang KC, Lan CY, Chou JL, Kuo JW, Chang CK, et al. Molecular epidemiology and antimicrobial resistance determinants of multidrug-resistant Acinetobacter baumannii among five proximal hospitals in Taiwan. Jpn J Infect Dis 2011;64:222-7.
  29. Iacono M, Villa L, Fortini D, Bordoni R, Imperi F, Bonnal RJ, et al. Wholegenome pyrosequencing of an epidemic multidrug-resistant Acinetobacter baumannii strain belonging to the European clone II group. Antimicrob Agents Chemother 2008;52:2616-25. https://doi.org/10.1128/AAC.01643-07

Cited by

  1. Tracing the emergence of multidrug-resistant Acinetobacter baumannii in a Taiwanese hospital by evaluating the presence of integron gene intI1 vol.13, pp.1, 2013, https://doi.org/10.1186/1477-5751-13-15
  2. Correlation of Ciprofloxacin Resistance with the AdeABC Efflux System in Acinetobacter baumannii Clinical Isolates vol.34, pp.6, 2013, https://doi.org/10.3343/alm.2014.34.6.433
  3. Antimicrobial resistance inAcinetobacter baumannii: From bench to bedside vol.2, pp.12, 2013, https://doi.org/10.12998/wjcc.v2.i12.787
  4. Prevalence and Characterization of Integrons in Multidrug Resistant Acinetobacter baumannii in Eastern China: A Multiple-Hospital Study vol.12, pp.8, 2013, https://doi.org/10.3390/ijerph120810093
  5. DNA fingerprinting and antimicrobial susceptibility pattern of clinical and environmentalAcinetobacter baumanniiisolates: a multicentre study vol.28, pp.4, 2016, https://doi.org/10.1080/1120009x.2016.1175706
  6. Molecular characterization and antimicrobial susceptibility of Acinetobacter baumannii isolates obtained from two hospital outbreaks in Los Angeles County, California, USA vol.16, pp.None, 2016, https://doi.org/10.1186/s12879-016-1526-y
  7. Biology of Acinetobacter baumannii : Pathogenesis, Antibiotic Resistance Mechanisms, and Prospective Treatment Options vol.7, pp.None, 2013, https://doi.org/10.3389/fcimb.2017.00055
  8. Comparative genomic analysis of Myroides odoratimimus isolates vol.8, pp.2, 2019, https://doi.org/10.1002/mbo3.634
  9. Copy Number of an Integron-Encoded Antibiotic Resistance Locus Regulates a Virulence and Opacity Switch in Acinetobacter baumannii AB5075 vol.11, pp.5, 2013, https://doi.org/10.1128/mbio.02338-20