Lab Med Online.  2019 Oct;9(4):201-209. 10.3343/lmo.2019.9.4.201.

Distribution of adeG, adeB, adeE, adeY, abeM, and adeJ Efflux Pump Genes in Clinical Isolates of Acinetobacter Species from Korea

• Choi IS
• Choi JA
• Jang SJ
• Park G
• Jeong SH
• Kim CM
• Lee OJ
• Kang SH
• Moon DS

• KMID: 2458679
• DOI: http://doi.org/10.3343/lmo.2019.9.4.201

Abstract

BACKGROUND
The aim of the present study was to determine the frequency of six efflux pump genes in Acinetobacter clinical isolates collected from South Korean hospitals.
METHODS
In this study, we used a total of 339 Acinetobacter strains, comprising 279 Acinetobacter calcoaceticus-Acinetobacter baumannii (ACB) complex and 60 non-ACB complex strains. We performed specific PCR assays to detect adeG, adeB, adeE, adeY, abeM, and adeJ, transporter genes of the multidrug efflux pumps AdeFGH, AdeABC, AdeDE, AdeXYZ, AbeM, and AdeIJK, respectively.
RESULTS
Frequencies of six efflux pump genes varied according to the species of Acinetobacter. Frequencies of adeE, abeM, and adeJ between A. baumannii group and A. nosocomialis group were found to be significantly different. Significant differences were found in the frequencies of adeB, adeE, adeY, and adeJ among the susceptible A. baumannii (SAB), multidrug-resistant A. baumannii (MDRAB), and extensively drug-resistant A. baumannii (XDRAB) groups within the 154 strains of A. baumannii. The frequencies of efflux pump genes in imipenem-susceptible and imipenem-nonsusceptible groups were significantly different for adeB, adeY, and adeJ. The frequencies of efflux pump genes in ciprofloxacin-susceptible and ciprofloxacin-nonsusceptible groups were significantly different for adeB and adeY. No significant difference was found in the frequency of efflux pump genes among groups sampled from different regions of Korea, across 86 strains of A. baumannii collected in 2012.
CONCLUSIONS
The frequencies of six efflux pump genes obtained in this study demonstrate the fundamental epidemiological feature of efflux pump genes in Korean Acinetobacter clinical isolates.

Keyword

Gene frequency; Multidrug efflux pump genes; Resistance-nodulation-cell division-type efflux pump; Acinetobacter; adeB; abeM

MeSH Terms

Acinetobacter*
Gene Frequency
Genes, MDR
Korea*
Polymerase Chain Reaction

Reference

1. Coyne S, Courvalin P, Périchon B. Efflux-mediated antibiotic resistance in Acinetobacter spp. Antimicrob Agents Chemother. 2011; 55:947–953.

2. Hernando-Amado S, Blanco P, Alcalde-Rico M, Corona F, Reales-Calderón JA, Sánchez MB, et al. Multidrug efflux pumps as main players in intrinsic and acquired resistance to antimicrobials. Drug Resist Updat. 2016; 28:13–27.

3. Yoon EJ, Chabane YN, Goussard S, Snesrud E, Courvalin P, Dé E, et al. Contribution of resistance-nodulation-cell division efflux systems to antibiotic resistance and biofilm formation in Acinetobacter baumannii. MBio. 2015; 6:e00309–e00315.

4. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012; 18:268–281.

5. Higgins PG, Wisplinghoff H, Krut O, Seifert H. A PCR-based method to differentiate between Acinetobacter baumannii and Acinetobacter genomic species 13TU. Clin Microbiol Infect. 2007; 13:1199–1201.

6. Higgins PG, Lehmann M, Wisplinghoff H, Seifert H. gyrB multiplex PCR to differentiate between Acinetobacter calcoaceticus and Acinetobacter genomic species 3. J Clin Microbiol. 2010; 48:4592–4594.

7. La Scola B, Gundi VA, Khamis A, Raoult D. Sequencing of the rpoB gene and flanking spacers for molecular identification of Acinetobacter species. J Clin Microbiol. 2006; 44:827–832.

8. Woodford N, Ellington MJ, Coelho JM, Turton JF, Ward ME, Brown S, et al. Multiplex PCR for genes encoding prevalent OXA carbapenemases in Acinetobacter spp. Int J Antimicrob Agents. 2006; 27:351–353.

9. Lee MJ, Jang SJ, Li XM, Park G, Kook JK, Kim MJ, et al. Comparison of rpoB gene sequencing, 16S rRNA gene sequencing, gyrB multiplex PCR, and the VITEK2 system for identification of Acinetobacter clinical isolates. Diagn Microbiol Infect Dis. 2014; 78:29–34.

10. Li XM, Choi JA, Choi IS, Kook JK, Chang YH, Park G, et al. Development and evaluation of species-specific PCR for detection of nine Acinetobacter species. Ann Clin Lab Sci. 2016; 46:270–278.

11. Coyne S, Rosenfeld N, Lambert T, Courvalin P, Périchon B. Overexpression of resistance-nodulation-cell division pump AdeFGH confers multidrug resistance in Acinetobacter baumannii. Antimicrob Agents Chemother. 2010; 54:4389–4393.

12. Magnet S, Courvalin P, Lambert T. Resistance-nodulation-cell division-type efflux pump involved in aminoglycoside resistance in Acinetobacter baumannii strain BM4454. Antimicrob Agents Chemother. 2001; 45:3375–3380.

13. Chau SL, Chu YW, Houang ET. Novel resistance-nodulation-cell division efflux system AdeDE in Acinetobacter genomic DNA group 3. Antimicrob Agents Chemother. 2004; 48:4054–4055.

14. Chu YW, Chau SL, Houang ET. Presence of active efflux systems AdeABC, AdeDE and AdeXYZ in different Acinetobacter genomic DNA groups. J Med Microbiol. 2006; 55:477–478.

15. Su XZ, Chen J, Mizushima T, Kuroda T, Tsuchiya T. AbeM, an H+-coupled Acinetobacter baumannii multidrug efflux pump belonging to the MATE family of transporters. Antimicrob Agents Chemother. 2005; 49:4362–4364.

16. Damier-Piolle L, Magnet S, Brémont S, Lambert T, Courvalin P. AdeIJK, a resistance-nodulation-cell division pump effluxing multiple antibiotics in Acinetobacter baumannii. Antimicrob Agents Chemother. 2008; 52:557–562.

17. Lin L, Ling BD, Li XZ. Distribution of the multidrug efflux pump genes, adeABC, adeDE and adeIJK, and class 1 integron genes in multiple-antimicrobial-resistant clinical isolates of Acinetobacter baumannii-Acinetobacter calcoaceticus complex. Int J Antimicrob Agents. 2009; 33:27–32.

18. Nowak J, Seifert H, Higgins PG. Prevalence of eight resistance-nodulation-division efflux pump genes in epidemiologically characterized Acinetobacter baumannii of worldwide origin. J Med Microbiol. 2015; 64:630–635.

19. Wieczorek P, Sacha P, Czaban S, Hauschild T, Ojdana D, Kowalczuk O, et al. Distribution of AdeABC efflux system genes in genotypically diverse strains of clinical Acinetobacter baumannii. Diagn Microbiol Infect Dis. 2013; 77:106–109.

20. Nemec A, Maixnerová M, van der Reijden TJ, van den Broek PJ, Dijkshoorn L. Relationship between the AdeABC efflux system gene content, netilmicin susceptibility and multidrug resistance in a genotypically diverse collection of Acinetobacter baumannii strains. J Antimicrob Chemother. 2007; 60:483–489.

21. Huys G, Cnockaert M, Vaneechoutte M, Woodford N, Nemec A, Dijk¬shoorn L, et al. Distribution of tetracycline resistance genes in genotypically related and unrelated multiresistant Acinetobacter baumannii strains from different European hospitals. Res Microbiol. 2005; 156:348–355.

22. Pagdepanichkit S, Tribuddharat C, Chuanchuen R. Distribution and expression of the Ade multidrug efflux systems in Acinetobacter baumannii clinical isolates. Can J Microbiol. 2016; 62:794–801.

23. Hou PF, Chen XY, Yan GF, Wang YP, Ying CM. Study of the correlation of imipenem resistance with efflux pumps AdeABC, AdeIJK, AdeDE and AbeM in clinical isolates of Acinetobacter baumannii. Chemotherapy. 2012; 58:152–158.