Prevalence of carbapenemases among high-level aminoglycoside-resistant Acinetobacter baumannii isolates in a university hospital in China

Wang,Yanhong; Shen,Min; Yang,Jingni; Dai,Min; Chang,Yaowen; Zhang,Chi; Luan,Guangxin; Ling,Baodong; Jia,Xu

doi:10.3892/etm.2016.3828

Prevalence of carbapenemases among high-level aminoglycoside-resistant Acinetobacter baumannii isolates in a university hospital in China

Authors:
- Yanhong Wang
- Min Shen
- Jingni Yang
- Min Dai
- Yaowen Chang
- Chi Zhang
- Guangxin Luan
- Baodong Ling
- Xu Jia
View Affiliations

Affiliations: Non‑Coding RNA and Drug Discovery Laboratory, Chengdu Medical College, Chengdu, Sichuan 610500, P.R. China, School of Laboratory Medicine, Chengdu Medical College, Chengdu, Sichuan 610500, P.R. China, Small Molecule Drugs Sichuan Key Laboratory, Institute of Materia Medica, Chengdu Medical College, Chengdu, Sichuan 610500, P.R. China
Published online on: October 20, 2016 https://doi.org/10.3892/etm.2016.3828
Pages: 3642-3652
Copyright: © Wang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

The prevalence of aminoglycoside resistant enzymes has previously been reported and extended-spectrum β-lactamase among Acinetobacter baumannii. To track the risk of multidrug‑resistant A. baumannii, the present study aimed to determine the prevalence of carbapenemases in high‑level aminoglycoside resistant A. baumannii over two years. A total of 118 strains of A. baumannii were consecutively collected in the First Affiliated Hospital of Chengdu Medical College, Chengdu, China. These isolates were investigated on the genetic basis of their resistance to aminoglycosides. The results showed that 75 (63.56%) isolates were high‑level resistant to aminoglycosides, including gentamicin and amikacin (minimum inhibitory concentration, ≥256 µg/ml). Aminoglycoside‑resistant genes ant(2

View Figures

View References

1	Sheikh YA, Marie MA, John J, Krishnappa LG and Dabwab KH: Prevalence of 16S rRNA methylase genes among β-lactamase-producing Enterobacteriaceae clinical isolates in Saudi Arabia. Libyan J Med. 9:244322014. View Article : Google Scholar : PubMed/NCBI
2	Belbel Z, Chettibi H, Dekhil M, Ladjama A, Nedjai S and Rolain JM: Outbreak of an armA Methyltransferase-Producing ST39 Klebsiella pneumoniae clone in a pediatric Algerian hospital. Microb Drug Resist. 20:310–315. 2014. View Article : Google Scholar : PubMed/NCBI
3	Liu Z, Ling B and Zhou L: Prevalence of 16S rRNA methylase, modifying enzyme, and extended-spectrum beta-lactamase genes among Acinetobacter baumannii isolates. J Chemother. 27:207–212. 2015. View Article : Google Scholar : PubMed/NCBI
4	Nemec A, Dolzani L, Brisse S, van den Broek P and 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. 53:1233–1240. 2004. View Article : Google Scholar : PubMed/NCBI
5	Labby KJ and Garneau-Tsodikova S: Strategies to overcome the action of aminoglycoside-modifying enzymes for treating resistant bacterial infections. Future Med Chem. 5:1285–1309. 2013. View Article : Google Scholar : PubMed/NCBI
6	Ramirez MS and Tolmasky ME: Aminoglycoside modifying enzymes. Drug Resist Updat. 13:151–171. 2010. View Article : Google Scholar : PubMed/NCBI
7	Cho YJ, Moon DC, Jin JS, Choi CH, Lee YC and Lee JC: Genetic basis of resistance to aminoglycosides in Acinetobacter spp. and spread of armA in Acinetobacter baumannii sequence group 1 in Korean hospitals. Diagn Microbiol Infect Dis. 64:185–190. 2009. View Article : Google Scholar : PubMed/NCBI
8	Bueno MF, Francisco GR, O'Hara JA, de Oliveira Garcia D and Doi Y: Coproduction of 16S rRNA methyltransferase RmtD or RmtG with KPC-2 and CTX-M group extended-spectrum β-lactamases in Klebsiella pneumoniae. Antimicrob Agents Chemother. 57:2397–2400. 2013. View Article : Google Scholar : PubMed/NCBI
9	Galimand M, Courvalin P and Lambert T: RmtF, a new member of the aminoglycoside resistance 16S rRNA N7 G1405 methyltransferase family. Antimicrob Agents Chemother. 56:3960–3962. 2012. View Article : Google Scholar : PubMed/NCBI
10	Huang J, Ye M, Jia X, Yu F and Wang M: Coexistence of armA and genes encoding aminoglycoside-modifying enzymes in Acinetobacter baumannii. Afr J Microbiol Res. 6:5325–5330. 2012.
11	O'Hara JA, McGann P, Snesrud EC, Clifford RJ, Waterman PE, Lesho EP and Doi Y: Novel 16S rRNA methyltransferase RmtH produced by Klebsiella pneumoniae associated with war-related trauma. Antimicrob Agents Chemother. 57:2413–2416. 2013. View Article : Google Scholar : PubMed/NCBI
12	Wachino J and Arakawa Y: Exogenously acquired 16S rRNA methyltransferases found in aminoglycoside-resistant pathogenic Gram-negative bacteria: An update. Drug Resist Updat. 15:133–148. 2012. View Article : Google Scholar : PubMed/NCBI
13	Wachino J, Shibayama K, Kurokawa H, Kimura K, Yamane K, Suzuki S, Shibata N, Ike Y and Arakawa Y: Novel plasmid-mediated 16S rRNA m1A1408 methyltransferase, NpmA, found in a clinically isolated Escherichia coli strain resistantto structurally diverse aminoglycosides. Antimicrob Agents Chemother. 51:4401–4409. 2007. View Article : Google Scholar : PubMed/NCBI
14	Nagasawa M, Kaku M, Kamachi K, Shibayama K, Arakawa Y, Yamaguchi K and Ishii Y: Loop-mediated isothermal amplification assay for 16S rRNA methylase genes in Gram-negative bacteria. J Infect Chemother. 20:635–638. 2014. View Article : Google Scholar : PubMed/NCBI
15	Marques MB, Brookings ES, Moser SA, Sonke PB and Waites KB: Comparative in vitro antimicrobial susceptibilities of nosocomial isolates of Acinetobacter baumannii and synergistic activities of nine antimicrobial combinations. Antimicrob Agents Chemother. 41:881–885. 1997.PubMed/NCBI
16	Wen JT, Zhou Y, Yang L and Xu Y: Multidrug-resistantgenes of aminoglycoside-modifying enzymes and 16S rRNA methylases in Acinetobacter baumannii strains. Genet Mol Res. 13:3842–3849. 2014. View Article : Google Scholar : PubMed/NCBI
17	Chang Y, Luan G, Xu Y, Wang Y, Shen M, Zhang C, Zheng W, Huang J, Yang J, Jia X and Ling B: Characterization of carbapenem-resistant Acinetobacter baumannii isolates in a Chinese teaching hospital. Front Microbiol. 6:9102015. View Article : Google Scholar : PubMed/NCBI
18	Walther-Rasmussen J and Høiby N: OXA-type carbapenemases. J Antimicrob Chemother. 57:373–383. 2006. View Article : Google Scholar : PubMed/NCBI
19	Doi Y, Adams JM, Yamane K and Paterson DL: Identification of 16S rRNA methylase-producing Acinetobacter baumannii clinical strains in North America. Antimicrob Agents Chemother. 51:4209–4210. 2007. View Article : Google Scholar : PubMed/NCBI
20	Kim JW, Heo ST, Jin JS, Choi CH, Lee YC, Jeong YG, Kim SJ and Lee JC: Characterization of Acinetobacter baumannii carrying bla(OXA-23), bla(PER-1) and armA in a Korean hospital. Clin Microbiol Infect. 14:716–718. 2008. View Article : Google Scholar : PubMed/NCBI
21	Zhou H, Du XX, Yang Q, Zhou JY, Yu YS and Li LJ: Study on carbapenemase and 16S rRNA methylase of imipenem-resistant Acinetobacter baumannii. Zhonghua Liu Xing Bing Xue Za Zhi. 30:269–272. 2009.(In Chinese). PubMed/NCBI
22	Adams-Haduch JM, Paterson DL, Sidjabat HE, Pasculle AW, Potoski BA, Muto CA, Harrison LH and Doi Y: Genetic basis of multidrug resistance in Acinetobacter baumannii clinical isolates at a tertiary medical center in Pennsylvania. Antimicrob Agents Chemother. 52:3837–3843. 2008. View Article : Google Scholar : PubMed/NCBI
23	Sung JY, Kwon KC, Cho HH and Koo SH: Antimicrobial resistance determinants in imipenem-nonsusceptible Acinetobacter calcoaceticus-baumannii complex isolated in Daejeon, Korea. Korean J Lab Med. 31:265–270. 2011. View Article : Google Scholar : PubMed/NCBI
24	Karthikeyan K, Thirunarayan MA and Krishnan P: Coexistence of blaOXA-23 with blaNDM-1 and armA in clinical isolates of Acinetobacter baumannii from India. J Antimicrob Chemother. 65:2253–2254. 2010. View Article : Google Scholar : PubMed/NCBI
25	Bonnin RA, Potron A, Poirel L, Lecuyer H, Neri R and Nordmann P: PER-7, an extended-spectrum beta-lactamase with increased activity toward broad-spectrum cephalosporins in Acinetobacter baumannii. Antimicrob Agents Chemother. 55:2424–2427. 2011. View Article : Google Scholar : PubMed/NCBI
26	Strateva T, Markova B, Marteva-Proevska Y, Ivanova D and Mitov I: Widespread dissemination of multidrug-resistant Acinetobacter baumannii producing OXA-23 carbapenemase and ArmA 16S ribosomal RNA methylase in a Bulgarian university hospital. Braz J Infect Dis. 16:307–310. 2012. View Article : Google Scholar : PubMed/NCBI
27	Brigante G, Migliavacca R, Bramati S, Motta E, Nucleo E, Manenti M, Migliorino G, Pagani L, Luzzaro F and Viganò FE: Emergence and spread of a multidrug-resistant Acinetobacter baumannii clone producing both the carbapenemase OXA-23 and the 16S rRNA methylase ArmA. J Med Microbiol. 61:653–661. 2012. View Article : Google Scholar : PubMed/NCBI
28	Saule M, Samuelsen Ø, Dumpis U, Sundsfjord A, Karlsone A, Balode A, Miklasevics E and Karah N: Dissemination of a carbapenem-resistant Acinetobacter baumannii strain belonging to international clone II/sequence type 2 and harboring a novel AbaR4-like resistance island in Latvia. Antimicrob Agents Chemother. 57:1069–1072. 2013. View Article : Google Scholar : PubMed/NCBI
29	Revathi G, Siu LK, Lu PL and Huang LY: First report of NDM-1-producing Acinetobacter baumannii in East Africa. Int J Infect Dis. 17:e1255–e1258. 2013. View Article : Google Scholar : PubMed/NCBI
30	Bakour S, Alsharapy SA, Touati A and Rolain JM: Characterization of Acinetobacter baumannii clinical isolates carrying bla(OXA-23) carbapenemase and 16S rRNA methylase armA genes in Yemen. Microb Drug Resist. 20:604–609. 2014. View Article : Google Scholar : PubMed/NCBI
31	Tada T, Miyoshi-Akiyama T, Shimada K, Shimojima M and Kirikae T: Dissemination of 16S rRNA methylase ArmA-producing Acinetobacter baumannii and emergence of OXA-72 carbapenemase coproducers in Japan. Antimicrob Agents Chemother. 58:2916–2920. 2014. View Article : Google Scholar : PubMed/NCBI
32	Tojo M, Mawatari M, Hayakawa K, Nagamatsu M, Shimada K, Mezaki K, Sugiki Y, Kuroda E, Takeshita N, Kutsuna S, et al: Multidrug-resistant Acinetobacter baumannii isolated from a traveler returned from Brunei. J Infect Chemothe. 21:212–214. 2015. View Article : Google Scholar
33	El-Sayed-Ahmed MA, Amin MA, Tawakol WM, Loucif L, Bakour S and Rolain JM: High prevalence of bla(NDM-1) carbapenemase-encoding gene and 16S rRNA armA methyltransferase among Acinetobacter baumannii clinical isolates, Egypt. Antimicrob Agents Chemother. 59:3602–3605. 2015. View Article : Google Scholar : PubMed/NCBI
34	Zhao WS, Liu GY, Mi ZH and Zhang F: Coexistence of blaOXA-23 with armA and novel gyrA mutation in a pandrug-resistant Acinetobacter baumannii isolate from the blood of a patient with haematological disease in China. J Hosp Infect. 77:278–279. 2011. View Article : Google Scholar : PubMed/NCBI
35	Zhou H, Zhang T, Yu D, Pi B, Yang Q, Zhou J, Hu S and Yu Y: Genomic analysis of the multidrug-resistant Acinetobacter baumannii strain MDR-ZJ06 widely spread in China. Antimicrob Agents Chemother. 55:4506–4512. 2011. View Article : Google Scholar : PubMed/NCBI
36	Liu Z, Ling B and Zhou L: Prevalence of 16S rRNA methylase, modifying enzyme, and extended-spectrum beta-lactamase genes among Acinetobacter baumannii isolates. J Chemother. 27:207–212. 2015. View Article : Google Scholar : PubMed/NCBI
37	Chen TL, Siu LK, Wu RC, Shaio MF, Huang LY, Fung CP, Lee CM and Cho WL: Comparison of one-tube multiplex PCR, automated ribotyping and intergenic spacer (ITS) sequencing for rapid identification of Acinetobacter baumannii. Clin Microbiol Infect. 13:801–806. 2007. View Article : Google Scholar : PubMed/NCBI
38	Li Y, Guo Q, Wang P, Zhu D, Ye X, Wu S and Wang M: Clonal dissemination of extensively drug-resistant Acinetobacter baumannii producing an OXA-23 β-lactamase at a teaching hospital in Shanghai, China. J Microbiol Immunol Infect. 48:101–108. 2015. View Article : Google Scholar : PubMed/NCBI
39	Clinical and Laboratory Standards Institute, . Performance Standards for Antimicrobial Susceptibility Testing. 24th Informational Supplement. CLSI; Wayne, PA, USA: M100, 2014
40	Li Y, Guo Q, Wang P, Zhu D, Ye X, Wu S and Wang M: Clonal dissemination of extensively drug-resistant Acinetobacter baumannii producing an OXA-23 β-lactamase at a teaching hospital in Shanghai, China. J Microbiol Immunol Infect. 48:101–108. 2015. View Article : Google Scholar : PubMed/NCBI
41	Valenzuela JK, Thomas L, Partridge SR, van der Reijden T, Dijkshoorn L and Iredell J: Horizontal gene transfer in a polyclonal outbreak of carbapenem-resistant Acinetobacter baumannii. J Clin Microbiol. 45:453–460. 2007. View Article : Google Scholar : PubMed/NCBI
42	Tsakris A, Pournaras S, Woodford N, Palepou MF, Babini GS, Douboyas J and Livermore DM: Outbreak of infections caused by Pseudomonas aeruginosa producing VIM-1 carbapenemase in Greece. J Clin Microbiol. 38:1290–1292. 2000.PubMed/NCBI
43	Ellington MJ, Kistler J, Livermore DM and Woodford N: Multiplex PCR for rapid detection of genes encoding acquired metallo-beta-lactamases. J Antimicrob Chemother. 59:321–322. 2007. View Article : Google Scholar : PubMed/NCBI
44	Yong D, Toleman MA, Giske CG, Cho HS, Sundman K, Lee K and Walsh TR: Characterization of a new metallo-beta-lactamase gene, bla(NDM-1) and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrob Agents Chemother. 53:5046–5054. 2009. View Article : Google Scholar : PubMed/NCBI
45	Woodford N, Ellington MJ, Coelho JM, Turton JF, Ward ME, Brown S, Amyes SG and Livermore DM: Multiplex PCR for genes encoding prevalent OXA carbapenemases in Acinetobacter spp. Int J Antimicrob Agents. 27:351–353. 2006. View Article : Google Scholar : PubMed/NCBI
46	Fu Y, Zhou J, Zhou H, Yang Q, Wei Z, Yu Y and Li L: Wide dissemination of OXA-23-producing carbapenem-resistant Acinetobacter baumannii clonal complex 22 in multiple cities of China. J Antimicrob Chemother. 65:644–650. 2010. View Article : Google Scholar : PubMed/NCBI
47	Netsvyetayeva I, Sikora M, Golas M, Swoboda-Kopec E, de Walthoffen SW, Dembicka O, Fraczek M, Mlynarczyk A, Pacholczyk M, Chmura A and Mlynarczyk G: Acinetobacter baumannii multidrug-resistant strain occurrence in liver recipients with reference to other high-risk groups. Transplant Proc. 43:3116–3120. 2011. View Article : Google Scholar : PubMed/NCBI
48	Diancourt L, Passet V, Nemec A, Dijkshoorn L and Brisse S: The population structure of Acinetobacter baumannii: Expanding multiresistant clones from an ancestral susceptible genetic pool. PLoS One. 5:e100342010. View Article : Google Scholar : PubMed/NCBI
49	Bartual SG, Seifert H, Hippler C, Luzon MA, Wisplinghoff H and Rodríguez-Valera F: Development of a multilocus sequence typing scheme for characterization of clinical isolates of Acinetobacter baumannii. J Clin Microbiol. 43:4382–4390. 2005. View Article : Google Scholar : PubMed/NCBI
50	PubMLST, . Acinetobacter baumannii MLST Databases. http://pubmlst.org/abaumannii/
51	Feil EJ, Li BC, Aanensen DM, Hanage WP and Spratt BG: eBURST: Inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol. 186:1518–1530. 2004. View Article : Google Scholar : PubMed/NCBI
52	Agadzhanian VV, Semenikhin VA, Iu S Fedorov, Krasulina GP, Gaǐfulina IM and Mironova LA: Experience of health protection center on organization of medical care for coal miners in Kuzbass. Med Tr Prom Ekol. 27–30. 2002.(In Russian). PubMed/NCBI
53	Tada T, Miyoshi-Akiyama T, Kato Y, Ohmagari N, Takeshita N, Hung NV, Phuong DM, Thu TA, Binh NG, Anh NQ, et al: Emergence of 16S rRNA methylase-producing Acinetobacter baumannii and Pseudomonas aeruginosa isolates in hospitals in Vietnam. BMC Infect Dis. 13:2512013. View Article : Google Scholar : PubMed/NCBI
54	Nie L, Lv Y, Yuan M, Hu X, Nie T, Yang X, Li G, Pang J, Zhang J, Li C, et al: Genetic basis of high level aminoglycoside resistance in Acinetobacter baumannii from Beijing, China. Acta Pharm Sin B. 4:295–300. 2014. View Article : Google Scholar : PubMed/NCBI
55	Xiao SZ, Han LZ, Chu HQ, Zhao L, Chen X and Ni YX: Detection of aminoglycoside resistance related genes in multidrug-resistant Acinetobacter baumannii isolated from a single institute of Shanghai, China. Panminerva Med. 57:49–53. 2015.PubMed/NCBI
56	Bakour S, Touati A, Bachiri T, Sahli F, Tiouit D, Naim M, Azouaou M and Rolain JM: First report of 16S rRNA methylase ArmA-producing Acinetobacter baumannii and rapid spread of metallo-β-lactamase NDM-1 in Algerian hospitals. J Infect Chemother. 20:696–701. 2014. View Article : Google Scholar : PubMed/NCBI
57	Azimi L, Talebi M, Pourshafie MR, Owlia P and Lari A Rastegar: Characterization of carbapenemases in extensively drug resistance Acinetobacter baumannii in a burn care center in Iran. Int J Mol Cell Med. 4:46–53. 2015.PubMed/NCBI
58	Jia X, Zhang J, Sun W, He W, Jiang H, Chen D and Murchie AI: Riboswitch control of aminoglycoside antibiotic resistance. Cell. 152:68–81. 2013. View Article : Google Scholar : PubMed/NCBI
59	Haldorsen BC, Simonsen GS, Sundsfjord A and Samuelsen Ø; Norwegian Study Group on Aminoglycoside Resistance, : Increased prevalence of aminoglycoside resistance in clinical isolates of Escherichia coli and Klebsiella spp. in Norway is associated with the acquisition of AAC(3)-II and AAC(6′)-Ib. Diagn Microbiol Infect Dis. 78:66–69. 2014. View Article : Google Scholar : PubMed/NCBI
60	Soleimani N, Aganj M, Ali L, Shokoohizadeh L and Sakinc T: Frequency distribution of genes encoding aminoglycoside modifying enzymes in uropathogenic E. coli isolated from Iranian hospital. BMC Res Notes. 7:8422014. View Article : Google Scholar : PubMed/NCBI
61	Miro E, Grünbaum F, Gomez L, Rivera A, Mirelis B, Coll P and Navarro F: Characterization of aminoglycoside-modifying enzymes in enterobacteriaceae clinical strains and characterization of the plasmids implicated in their diffusion. Microb Drug Resist. 19:94–99. 2013. View Article : Google Scholar : PubMed/NCBI
62	Akers KS, Chaney C, Barsoumian A, Beckius M, Zera W, Yu X, Guymon C, Keen EF III, Robinson BJ, Mende K and Murray CK: Aminoglycoside resistance and susceptibility testing errors in Acinetobacter baumannii-calcoaceticus complex. J Clin Microbiol. 48:1132–1138. 2010. View Article : Google Scholar : PubMed/NCBI
63	Nowak P, Paluchowska PM and Budak A: Co-occurrence of carbapenem and aminoglycoside resistance genes among multidrug-resistant clinical isolates of Acinetobacter baumannii from Cracow, Poland. Med Sci Monit Basic Res. 20:9–14. 2014. View Article : Google Scholar : PubMed/NCBI
64	Hamouda A, Evans BA, Towner KJ and Amyes SG: Characterization of epidemiologically unrelated Acinetobacter baumannii isolates from four continents by use of multilocus sequence typing, pulsed-field gel electrophoresis and sequence-based typing of bla(OXA-51-like) genes. J Clin Microbiol. 48:2476–2483. 2010. View Article : Google Scholar : PubMed/NCBI