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Published in: BMC Infectious Diseases 1/2021

Open Access 01-12-2021 | Imipenem | Research

Comparative analysis of carbapenemases, RND family efflux pumps and biofilm formation potential among Acinetobacter baumannii strains with different carbapenem susceptibility

Authors: Yanpeng Zhang, Bing Fan, Yong Luo, Zhiyuan Tao, Yongbo Nie, Yongtao Wang, Fanglin Ding, Yanwu Li, Dayong Gu

Published in: BMC Infectious Diseases | Issue 1/2021

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Abstract

Aim

This study has conducted a comparative analysis of common carbapenemases harboring, the expression of resistance-nodulation-cell division (RND) family efflux pumps, and biofilm formation potential associated with carbapenem resistance among Acinetobacter baumannii (A. baumannii) strains with different carbapenem susceptibility. Methods: A total of 90 isolates of A. baumannii from two tertiary hospitals of China were identified and grouped as carbapenem susceptible A. baumannii (CSAB) strains and carbapenem non-susceptible A. baumannii (CnSAB) strains based on the susceptibility to imipenem. Harboring of carbapenemase genes, relative expression of RND family efflux pumps and biofilm formation potential were compared between the two groups. Result: Among these strains, 12 (13.3 %) strains were divided into the CSAB group, and 78 (86.7 %) strains into the CnSAB group. Compared with CSAB strains, CnSAB strains increased distribution of blaOXA−23 (p < 0.001) and ISAba1/blaOXA−51−like (p = 0.034) carbapenemase genes, and a 6.1-fold relative expression of adeB (p = 0.002), while CSAB strains led to biofilm formation by 1.3-fold than CnSAB strains (p = 0.021).

Conclusions

Clinically, harboring more blaOXA−23−like and ISAba1/blaOXA−51−like complex genes and overproduction of adeABC are relevant with carbapenem resistance, while carbapenem susceptible strains might survive the stress of antibiotic through their ability of higher biofilm formation.
Literature
1.
go back to reference Antunes LCS, Visca P, Towner KJ. Acinetobacter baumannii: Evolution of a global pathogen. Pathog Dis. 2014;71:292–301.CrossRef Antunes LCS, Visca P, Towner KJ. Acinetobacter baumannii: Evolution of a global pathogen. Pathog Dis. 2014;71:292–301.CrossRef
2.
go back to reference Peleg AY, Seifert H, Paterson DL. Acinetobacter baumannii: Emergence of a successful pathogen. Clin Microbiol Rev. 2008;21:538–82.CrossRef Peleg AY, Seifert H, Paterson DL. Acinetobacter baumannii: Emergence of a successful pathogen. Clin Microbiol Rev. 2008;21:538–82.CrossRef
3.
go back to reference Holmes CL, Anderson MT, Mobley HLT, Bachman MA. Pathogenesis of gram-negative bacteremia. Clin Microbiol Rev. 2021;34:1. Holmes CL, Anderson MT, Mobley HLT, Bachman MA. Pathogenesis of gram-negative bacteremia. Clin Microbiol Rev. 2021;34:1.
4.
go back to reference Lima WG, Silva Alves GC, Sanches C, Antunes Fernandes SO, de Paiva MC. Carbapenem-resistant Acinetobacter baumannii in patients with burn injury: a systematic review and meta-analysis. Burns. 2019;45:1495–508.CrossRef Lima WG, Silva Alves GC, Sanches C, Antunes Fernandes SO, de Paiva MC. Carbapenem-resistant Acinetobacter baumannii in patients with burn injury: a systematic review and meta-analysis. Burns. 2019;45:1495–508.CrossRef
5.
go back to reference Ayobami O, Willrich N, Harder T, Okeke IN, Eckmanns T, Markwart R. The incidence and prevalence of hospital-acquired (carbapenem-resistant) Acinetobacter baumannii in Europe, Eastern Mediterranean and Africa: a systematic review and meta-analysis. Emerg Microb Infect. 2019;8:1747–59.CrossRef Ayobami O, Willrich N, Harder T, Okeke IN, Eckmanns T, Markwart R. The incidence and prevalence of hospital-acquired (carbapenem-resistant) Acinetobacter baumannii in Europe, Eastern Mediterranean and Africa: a systematic review and meta-analysis. Emerg Microb Infect. 2019;8:1747–59.CrossRef
6.
go back to reference Durante-Mangoni E, Zarrilli R. Global spread of drug-resistant Acinetobacter baumannii: molecular epidemiology and management of antimicrobial resistance. Fut Microbiol. 2011;6:407–22.CrossRef Durante-Mangoni E, Zarrilli R. Global spread of drug-resistant Acinetobacter baumannii: molecular epidemiology and management of antimicrobial resistance. Fut Microbiol. 2011;6:407–22.CrossRef
7.
go back to reference Doi Y. Treatment options for carbapenem-resistant gram-negative bacterial infections. Clin Infect Dis. 2019;69(Suppl 7):S565–75.CrossRef Doi Y. Treatment options for carbapenem-resistant gram-negative bacterial infections. Clin Infect Dis. 2019;69(Suppl 7):S565–75.CrossRef
8.
go back to reference Gundi VAKB, Dijkshoorn L, Burignat S, Raoult D, La Scola B. Validation of partial rpoB gene sequence analysis for the identification of clinically important and emerging Acinetobacter species. Microbiology. 2009;155:2333–41.CrossRef Gundi VAKB, Dijkshoorn L, Burignat S, Raoult D, La Scola B. Validation of partial rpoB gene sequence analysis for the identification of clinically important and emerging Acinetobacter species. Microbiology. 2009;155:2333–41.CrossRef
9.
go back to reference La Scola B, Gundi VAKB, Khamis A, Raoult D. Sequencing of the rpoB gene and flanking spacers for molecular identification of Acinetobacter species. J Clin Microbiol. 2006;44:827–32.CrossRef La Scola B, Gundi VAKB, Khamis A, Raoult D. Sequencing of the rpoB gene and flanking spacers for molecular identification of Acinetobacter species. J Clin Microbiol. 2006;44:827–32.CrossRef
10.
go back to reference Zhang Y, Li Z, He X, Ding F, Wu W, Luo Y, et al. Overproduction of efflux pumps caused reduced susceptibility to carbapenem under consecutive imipenem-selected stress in Acinetobacter baumannii. Infect Drug Resist. 2018;11:457–67.CrossRef Zhang Y, Li Z, He X, Ding F, Wu W, Luo Y, et al. Overproduction of efflux pumps caused reduced susceptibility to carbapenem under consecutive imipenem-selected stress in Acinetobacter baumannii. Infect Drug Resist. 2018;11:457–67.CrossRef
12.
go back to reference Yang YS, Chen HY, Hsu WJ, Chou YC, Perng CL, Shang HS, et al. Overexpression of AdeABC efflux pump associated with tigecycline resistance in clinical Acinetobacter nosocomialis isolates. Clin Microbiol Infect. 2019;25:512.e1-512.e6.CrossRef Yang YS, Chen HY, Hsu WJ, Chou YC, Perng CL, Shang HS, et al. Overexpression of AdeABC efflux pump associated with tigecycline resistance in clinical Acinetobacter nosocomialis isolates. Clin Microbiol Infect. 2019;25:512.e1-512.e6.CrossRef
13.
go back to reference Turton JF, Ward ME, Woodford N, Kaufmann ME, Pike R, Livermore DM, et al. The role of ISAba1 in expression of OXA carbapenemase genes in Acinetobacter baumannii. FEMS Microbiol Lett. 2006;258:72–7.CrossRef Turton JF, Ward ME, Woodford N, Kaufmann ME, Pike R, Livermore DM, et al. The role of ISAba1 in expression of OXA carbapenemase genes in Acinetobacter baumannii. FEMS Microbiol Lett. 2006;258:72–7.CrossRef
14.
go back to reference Krzyściak P, Chmielarczyk A, Pobiega M, Romaniszyn D, Wójkowska-Mach J. Acinetobacter baumannii isolated from hospital-acquired infection: biofilm production and drug susceptibility. APMIS. 2017;125:1017–26.CrossRef Krzyściak P, Chmielarczyk A, Pobiega M, Romaniszyn D, Wójkowska-Mach J. Acinetobacter baumannii isolated from hospital-acquired infection: biofilm production and drug susceptibility. APMIS. 2017;125:1017–26.CrossRef
15.
go back to reference Schooley RT, Biswas B, Gill JJ, Hernandez-Morales A, Lancaster J, Lessor L, et al. Development and use of personalized bacteriophage-based therapeutic cocktails to treat a patient with a disseminated resistant Acinetobacter baumannii infection. Antimicrob Agents Chemother. 2017;61:1.CrossRef Schooley RT, Biswas B, Gill JJ, Hernandez-Morales A, Lancaster J, Lessor L, et al. Development and use of personalized bacteriophage-based therapeutic cocktails to treat a patient with a disseminated resistant Acinetobacter baumannii infection. Antimicrob Agents Chemother. 2017;61:1.CrossRef
16.
go back to reference Xiao J, Zhang C, Ye S. Acinetobacter baumannii meningitis in children: a case series and literature review. Infection. 2019;47:643–9.CrossRef Xiao J, Zhang C, Ye S. Acinetobacter baumannii meningitis in children: a case series and literature review. Infection. 2019;47:643–9.CrossRef
17.
go back to reference Yamasmith E, Chongtrakool P, Chayakulkeeree M. Isolated pulmonary fusariosis caused by Neocosmospora pseudensiformis in a liver transplant recipient: A case report and review of the literature. Transpl Infect Dis. 2020;22:e13344.CrossRef Yamasmith E, Chongtrakool P, Chayakulkeeree M. Isolated pulmonary fusariosis caused by Neocosmospora pseudensiformis in a liver transplant recipient: A case report and review of the literature. Transpl Infect Dis. 2020;22:e13344.CrossRef
18.
go back to reference Aykota MR, Sari T, Yilmaz S. Successful treatment of extreme drug resistant Acinetobacter baumannii infection following a liver transplant. J Infect Dev Ctries. 2020;14:408–10.CrossRef Aykota MR, Sari T, Yilmaz S. Successful treatment of extreme drug resistant Acinetobacter baumannii infection following a liver transplant. J Infect Dev Ctries. 2020;14:408–10.CrossRef
19.
go back to reference Xu A, Zhu H, Gao B, Weng H, Ding Z, Li M, et al. Diagnosis of severe community-acquired pneumonia caused by Acinetobacter baumannii through next-generation sequencing: a case report. BMC Infect Dis. 2020;20:45.CrossRef Xu A, Zhu H, Gao B, Weng H, Ding Z, Li M, et al. Diagnosis of severe community-acquired pneumonia caused by Acinetobacter baumannii through next-generation sequencing: a case report. BMC Infect Dis. 2020;20:45.CrossRef
20.
go back to reference Dijkshoorn L, Nemec A, Seifert H. An increasing threat in hospitals: multidrug-resistant Acinetobacter baumannii. Nat Rev Microbiol. 2007;5:939–51.CrossRef Dijkshoorn L, Nemec A, Seifert H. An increasing threat in hospitals: multidrug-resistant Acinetobacter baumannii. Nat Rev Microbiol. 2007;5:939–51.CrossRef
21.
go back to reference Jia W, Li C, Zhang H, Li G, Liu X, Wei J. Prevalence of genes of OXA-23 carbapenemase and AdeABC efflux pump associated with multidrug resistance of Acinetobacter baumannii isolates in the ICU of a comprehensive hospital of Northwestern China. Int J Environ Res Public Health. 2015;12:10079–92.CrossRef Jia W, Li C, Zhang H, Li G, Liu X, Wei J. Prevalence of genes of OXA-23 carbapenemase and AdeABC efflux pump associated with multidrug resistance of Acinetobacter baumannii isolates in the ICU of a comprehensive hospital of Northwestern China. Int J Environ Res Public Health. 2015;12:10079–92.CrossRef
22.
go back to reference Sun H, Xiao G, Zhang J, Pan Z, Chen Y, Xiong F. Rapid simultaneous detection of blaoxa-23, Ade-B, int-1, and ISCR-1 in multidrug-resistant Acinetobacter baumannii using single-tube multiplex PCR and high resolution melting assay. Infect Drug Resist. 2019;12:1573–81.CrossRef Sun H, Xiao G, Zhang J, Pan Z, Chen Y, Xiong F. Rapid simultaneous detection of blaoxa-23, Ade-B, int-1, and ISCR-1 in multidrug-resistant Acinetobacter baumannii using single-tube multiplex PCR and high resolution melting assay. Infect Drug Resist. 2019;12:1573–81.CrossRef
23.
24.
go back to reference Leungtongkam U, Thummeepak R, Wongprachan S, Thongsuk P, Kitti T, Ketwong K, et al. Dissemination of blaOXA-23, blaOXA-24, blaOXA-58, and blaNDM-1 Genes of Acinetobacter baumannii Isolates from Four Tertiary Hospitals in Thailand. Microb Drug Resist. 2018;24:55–62.CrossRef Leungtongkam U, Thummeepak R, Wongprachan S, Thongsuk P, Kitti T, Ketwong K, et al. Dissemination of blaOXA-23, blaOXA-24, blaOXA-58, and blaNDM-1 Genes of Acinetobacter baumannii Isolates from Four Tertiary Hospitals in Thailand. Microb Drug Resist. 2018;24:55–62.CrossRef
25.
go back to reference Hou C, Yang F. Drug-resistant gene of blaOXA-23, blaOXA-24, blaOXA-51 and blaOXA-58 in Acinetobacter baumannii. Int J Clin Exp Med. 2015;8:13859–63.PubMedPubMedCentral Hou C, Yang F. Drug-resistant gene of blaOXA-23, blaOXA-24, blaOXA-51 and blaOXA-58 in Acinetobacter baumannii. Int J Clin Exp Med. 2015;8:13859–63.PubMedPubMedCentral
28.
go back to reference Fernández L, Hancock REW. Adaptive and mutational resistance: role of porins and efflux pumps in drug resistance. Clin Microbiol Rev. 2012;25:661–81.CrossRef Fernández L, Hancock REW. Adaptive and mutational resistance: role of porins and efflux pumps in drug resistance. Clin Microbiol Rev. 2012;25:661–81.CrossRef
29.
go back to reference Adabi M, Talebi-Taher M, Arbabi L, Afshar M, Fathizadeh S, Minaeian S, et al. Spread of efflux pump overexpressing-mediated fluoroquinolone resistance and multidrug resistance in Pseudomonas aeruginosa by using an efflux pump inhibitor. Infect Chemother. 2015;47:98–104.CrossRef Adabi M, Talebi-Taher M, Arbabi L, Afshar M, Fathizadeh S, Minaeian S, et al. Spread of efflux pump overexpressing-mediated fluoroquinolone resistance and multidrug resistance in Pseudomonas aeruginosa by using an efflux pump inhibitor. Infect Chemother. 2015;47:98–104.CrossRef
30.
go back to reference 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;58:152–8.CrossRef 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;58:152–8.CrossRef
31.
go back to reference Yoon EJ, Courvalin P, Grillot-Courvalin C. RND-type efflux pumps in multidrug-resistant clinical isolates of Acinetobacter baumannii: Major role for AdeABC overexpression and aders mutations. Antimicrob Agents Chemother. 2013;57:2989–95.CrossRef Yoon EJ, Courvalin P, Grillot-Courvalin C. RND-type efflux pumps in multidrug-resistant clinical isolates of Acinetobacter baumannii: Major role for AdeABC overexpression and aders mutations. Antimicrob Agents Chemother. 2013;57:2989–95.CrossRef
32.
go back to reference Chen Y, Ai L, Guo P, Huang H, Wu Z, Liang X, et al. Molecular characterization of multidrug resistant strains of Acinetobacter baumannii isolated from pediatric intensive care unit in a Chinese tertiary hospital 11 Medical and Health Sciences 1108 Medical Microbiology. BMC Infect Dis. 2018;18:1–7.CrossRef Chen Y, Ai L, Guo P, Huang H, Wu Z, Liang X, et al. Molecular characterization of multidrug resistant strains of Acinetobacter baumannii isolated from pediatric intensive care unit in a Chinese tertiary hospital 11 Medical and Health Sciences 1108 Medical Microbiology. BMC Infect Dis. 2018;18:1–7.CrossRef
33.
go back to reference Dahdouh E, Orgaz B, Gómez-Gil R, Mingorance J, Daoud Z, Suarez M, et al. Patterns of biofilm structure and formation kinetics among Acinetobacter baumannii clinical isolates with different antibiotic resistance profiles. Med Chem Comm. 2016;7:1.CrossRef Dahdouh E, Orgaz B, Gómez-Gil R, Mingorance J, Daoud Z, Suarez M, et al. Patterns of biofilm structure and formation kinetics among Acinetobacter baumannii clinical isolates with different antibiotic resistance profiles. Med Chem Comm. 2016;7:1.CrossRef
34.
go back to reference Perez LRR. Acinetobacter baumannii displays inverse relationship between meropenem resistance and biofilm production. J Chemother. 2015;27:13–6.CrossRef Perez LRR. Acinetobacter baumannii displays inverse relationship between meropenem resistance and biofilm production. J Chemother. 2015;27:13–6.CrossRef
Metadata
Title
Comparative analysis of carbapenemases, RND family efflux pumps and biofilm formation potential among Acinetobacter baumannii strains with different carbapenem susceptibility
Authors
Yanpeng Zhang
Bing Fan
Yong Luo
Zhiyuan Tao
Yongbo Nie
Yongtao Wang
Fanglin Ding
Yanwu Li
Dayong Gu
Publication date
01-12-2021
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2021
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-021-06529-2

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