Advanced Biomedical Research

Genotypic patterns of multidrug-resistant Acinetobacter baumannii: A systematic review

Authors

Pediatric Infectious Diseases Research Center, Communicable Diseases Institute, Mazandaran University of Medical Sciences, Sari, Iran

Abstract

Acinetobacter baumannii (A. baumannii) is one of the most common bacteria in nosocomial infections. Inappropriate usage of antibiotics has led to expanding emergence resistance to A. baumannii as a multidrug-resistant (MDR) strain. Empirical antibiotic therapy is necessary to evaluate the resistant gene pattern of MDR A. baumannii. For this purpose, the present study evaluated the resistance genes pattern of MDR A. baumannii collected from hospitalized patients using a genotypic diagnostic technique. To find evidence related to the study objectives, databases were searched such as Google Scholar, Web of Science, Science Direct, PubMed, and Scopus from 2000 to 2022, with specified keywords in the title and text of the articles. Articles were included based on inclusion and exclusion criteria. The mentioned database displayed 284 articles. After screening, 65 eligible articles were included. The results showed that various b-lactamases genes, aminoglycoside-modifying enzymes (AMEs) genes, and pump-expressing genes are resistance gene patterns in MDR A. baumannii isolates. MDR A. baumannii has significantly become resistant to b-lactams, carbapenems, and aminoglycosides.

Keywords

1.
Garnacho-Montero J, Ortiz-Leyba C, Fernández-Hinojosa E, Aldabó-Pallás T, Cayuela A, Marquez-Vácaro JA, et al. Acinetobacter baumannii ventilator-associated pneumonia: Epidemiological and clinical findings. Intensive Care Med 2005;31:649-55.  Back to cited text no. 1
    
2.
Rahimzadeh G, Rezai MS. Detection extended-spectrum beta-lactamase- and carbapenemase-producing Enterobacteriaceae isolates from clinical samples; Narrative review. J. Isfahan Med. Sch 2022;40:743-58.  Back to cited text no. 2
    
3.
Medina E, Pieper DH. Tackling threats and future problems of multidrugresistant Bacteria. Curr Top Microbiol Immunol 2016;398:3-33.  Back to cited text no. 3
    
4.
Poirel L, Nordmann P. Carbapenem resistance in Acinetobacter baumannii: Mechanisms and epidemiology. Clin Microbiol Infect 2006;12:826-36.  Back to cited text no. 4
    
5.
Alkasaby NM, El Sayed Zaki M. Molecular study of Acinetobacter baumannii isolates for Metallo-beta-lactamases and extended-spectrum-beta-lactamases genes in intensive care unit, Mansoura University Hospital, Egypt. Int J Microbiol 2017;2017:3925868.  Back to cited text no. 5
    
6.
Gootz TD, Marra A. Acinetobacter baumannii: An emerging multidrugresistant threat. Expert Rev Anti-Infect Ther 2008;6:309-25.  Back to cited text no. 6
    
7.
Karaaslan A, Soysal A, Altinkanat Gelmez G, Kepenekli Kadayifci E, Soyletir G, Bakir M. Molecular characterization and risk factors for carbapenem-resistant gram-negative bacilli colonization in children: Emergence of NDM-producing Acinetobacter baumannii in a newborn intensive care unit in Turkey. J Hosp Infect 2016;92:67-72.  Back to cited text no. 7
    
8.
Roschanski N, Fischer J, Guerra B, Roesler U. Development of a multiplex real-time PCR for the rapid detection of the predominant beta-lactamase genes CTX-M, SHV, TEM and CIT-type AmpCs in Enterobacteriaceae. PLoS One 2014;9:e100956.  Back to cited text no. 8
    
9.
Kaitany KCJ, Klinger NV, June CM, Ramey ME, Bonomo RA, Powers RA, et al. Structures of the class D carbapenemases OXA-23 and OXA-146: Mechanistic basis of activity against carbapenems, extended-spectrum cephalosporins, and aztreonam. Antimicrob Agents Chemother 2013;57:4848-55.  Back to cited text no. 9
    
10.
Corvec S, Poirel L, Naas T, Drugeon H, Nordmann P. Genetics and expression of the carbapenem-hydrolyzing oxacillinase gene blaOXA-23 in Acinetobacter baumannii. Antimicrob Agents Chemother 2007;51:1530-3.  Back to cited text no. 10
    
11.
Turton JF, Ward ME, Woodford N, Kaufmann ME, Pike R, Livermore DM, et al. The role of IS Aba1 in expression of OXA carbapenemase genes in Acinetobacter baumannii. FEMS Microbiol Lett 2006;258:72-7.  Back to cited text no. 11
    
12.
Héritier C, Poirel L, Lambert T, Nordmann P. Contribution of acquired carbapenem-hydrolyzing oxacillinases to carbapenem resistance in Acinetobacter baumannii. Antimicrob Agents Chemother 2005;49:3198-202.  Back to cited text no. 12
    
13.
Povilonis J, Seputiene V, Krasauskas R, Juskaite R, Miskinyte M, Suziedelis K, et al.Spread of carbapenemresistant Acinetobacter baumannii carrying a plasmid with two genes encoding OXA-72 carbapenemase in Lithuanian hospitals. J Antimicrob Chemother 2013;68:1000-6  Back to cited text no. 13
    
14.
Bush K, Jacoby GA. Updated functional classification of beta-lactamases. Antimicrob Agents Chemother 2010;54:969-76.  Back to cited text no. 14
    
15.
Jeong SH, Bae IK, Kwon SB, Lee K, Yong D, Woo GJ, et al. Investigation of a nosocomial outbreak of Acinetobacter baumannii producing PER-1 extended-spectrum β-lactamase in an intensive care unit. J Hosp Infect 2005;59:242-8.  Back to cited text no. 15
    
16.
Lee K, Yum JH, Yong D, Lee HM, Kim HD, Docquier JD, et al. Novel acquired metallo-β-lactamase gene, blaSIM-1, in a Class 1 integron from Acinetobacter baumannii clinical isolates from Korea. Antimicrob Agents Chemother 2005;49:4485-91.  Back to cited text no. 16
    
17.
Hujer KM, Hamza NS, Hujer AM, Perez F, Helfand MS, Bethel CR, et al. Identification of a new allelic variant of the Acinetobacter baumannii cephalosporinase, ADC-7 β-lactamase: Defining a unique family of class C enzymes. Antimicrob Agents Chemother 2005;49:2941-8.  Back to cited text no. 17
    
18.
Jeon JH, Hong MK, Lee JH, Lee JJ, Park KS, Karim AM, et al. Structure of ADC-68, a novel carbapenem hydrolyzing class C extended-spectrum b-lactamase isolated from Acinetobacter baumannii. Acta Crystallogr D Biol Crystallogr 2014;70:2924-36.  Back to cited text no. 18
    
19.
Bou G, Martínez-Beltrán J. Cloning, nucleotide sequencing, and analysis of the gene encoding an AmpC β-lactamase in Acinetobacter baumannii. Antimicrob Agents Chemother 2000;44:428-32.  Back to cited text no. 19
    
20.
Higgins PG, Poirel L, Lehmann M, Nordmann P, Seifert H.OXA-143, a Novel Carbapenem-hydrolyzing class D β-lactamase in Acinetobacter baumannii. Antimicrob Agents Chemother 2009;53:5035-8.  Back to cited text no. 20
    
21.
Higgins PG, Pérez-Llarena FJ, Zander E, Fernández A, Bou G, Seifert H.OXA-235, a novel class D β-lactamase involved in resistance to carbapenems in Acinetobacter baumannii. Antimicrob Agents Chemother 2013;57:2121-6.  Back to cited text no. 21
    
22.
Huang XZ, Cash DM, Chahine MA, Nikolich MP, Craft DW.Development and validation of a multiplex TaqManReal-time PCR for rapid detection of genes encoding four types of class D carbapenemase in Acinetobacter baumannii. J Med Microbiol 2012;61:1532-7.  Back to cited text no. 22
    
23.
Poirel L, Menuteau O, Agoli N, Cattoen C, Nordmann P. Outbreak of extended-spectrum β-lactamase VEB-1-producing isolates of Acinetobacter baumannii in a French hospital. J Clin Microbiol 2003;41:3542-7.  Back to cited text no. 23
    
24.
Adams MD, Goglin K, Molyneaux N, Hujer KM, Lavender H, Jamison JJ, et al. Comparative genome sequence analysis of multidrug-resistant Acinetobacter baumannii. J Bacteriol 2008;190:8053-64.  Back to cited text no. 24
    
25.
Bogaerts P, Naas T, El Garch F, Cuzon G, Deplano A, Delaire T, et al. GES extended-spectrum β-lactamases in Acinetobacter baumannii isolates in Belgium. Antimicrob Agents Chemother 2010;54:4872-8.  Back to cited text no. 25
    
26.
Bonnin RA, Nordmann P, Potron A, Lecuyer H, Zahar JR, Poirel L.Carbapenem-hydrolyzing GES-type extended-spectrum β-lactamase in Acinetobacter baumannii. Antimicrob Agents Chemother 2011;55:349-54.  Back to cited text no. 26
    
27.
Brown S, Young HK, Amyes SGB. Characterisation of OXA-51, a novel class D carbapenemase found in genetically unrelated clinical strains of Acinetobacter baumannii from Argentina. Clin Microbiol Infect 2005;11:15-23.  Back to cited text no. 27
    
28.
Chu YW, Afzal-Shah M, Houang ET, Palepou MI, Lyon DJ, Woodford N, et al. IMP-4, a novel metallo-β-lactamase from nosocomial Acinetobacter spp. collected in Hong Kong between 1994 and 1998. Antimicrob Agents Chemother 2001;45:710-4.  Back to cited text no. 28
    
29.
Dhabaan GN, AbuBakar S, Cerqueira GM, Al-Haroni M, Pang SP, Hassan H. Imipenem treatment induces expression of important genes and phenotypes in a resistant Acinetobacter baumannii isolate. Antimicrob Agents Chemother 2016;60:1370-6.  Back to cited text no. 29
    
30.
Endimiani A, Luzzaro F, Migliavacca R, Mantengoli E, Hujer AM, Hujer KM, et al. Spread in an Italian hospital of a clonal Acinetobacter baumannii strain producing the TEM-92 extended-spectrum β-lactamase. Antimicrob Agents Chemother 2007;51:2211-4.  Back to cited text no. 30
    
31.
Gales AC, Tognim MC, Reis AO, Jones RN, Sader HS. Emergence of an IMP-like metallo-enzyme in an Acinetobacter baumannii clinical strain from a Brazilian teaching hospital. Diagn Microbiol Infect Dis 2003;45:77-9.  Back to cited text no. 31
    
32.
Hamidian M, Holt KE, Hall RM.Genomic Resistance Island AGI1 carrying a complex class 1 integron in a multiply antibiotic-resistant ST25 Acinetobacter baumannii isolate. J Antimicrob Chemother 2015;70:2519-23.  Back to cited text no. 32
    
33.
Sohrabi N, Farajnia S, Akhi MT, Nahaei MR, Naghili B, Peymani A, et al. Prevalence of OXA-Type β-lactamases among Acinetobacter baumannii isolates from Northwest of Iran. Microb Drug Resist 2012;18:385-9.  Back to cited text no. 33
    
34.
Koh TH, Sng LH, Wang GCY, Hsu LY, Zhao Y.IMP-4 and OXA β-lactamases in Acinetobacter baumannii from Singapore. J Antimicrob Chemother2007;59:627-32.  Back to cited text no. 34
    
35.
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.  Back to cited text no. 35
    
36.
AlAmri AM, AlQurayan AM, Sebastian T, AlNimr AM. Molecular surveillance of multidrug-resistant Acinetobacter baumannii. Curr Microbiol2020;77:335-42.  Back to cited text no. 36
    
37.
Genteluci GL, Gomes DBC, Pereira D, Neves MC, de Souza MJ, Rangel K, et al. Multidrug-resistant Acinetobacter baumannii: Differential adherence to HEp-2 and A-549 cells. Braz J Microbiol 2020;51:657-64.  Back to cited text no. 37
    
38.
Raro OHF, Gallo SW, Ferreira CAS, Oliveira SD. Carbapenem-resistant Acinetobacter baumannii contamination in an intensive care unit. Rev Soc Bras Med Trop 2017;50:167-72.  Back to cited text no. 38
    
39.
Hassan R, Tantawy M, Gouda NA, Elzayat MG, Gabra S, Nabih A, et al. Genotypic characterization of multiple drug resistant Escherichia coli isolates from a pediatric cancer hospital in Egypt. Sci Rep 2020;10:4165.  Back to cited text no. 39
    
40.
Qureshi ZA, Paterson DL, Peleg AY, Adams-Haduch JM, Shutt KA, Pakstis DL, et al. Clinical characteristics of bacteremia due to extended-spectrum β-lactamase (ESBL)-producing Enterobacteriaceae in the era of CTX-M and KPC-type β-lactamases. Clin Microbiol Infect 2012;18:887-93.  Back to cited text no. 40
    
41.
Goudarzi M, Fazeli M, Eslami G, Pouriran R, Hajikhani B, Dadashi M. Genetic diversity analysis of methicillin-resistant Staphylococcus aureus strains isolated from intensive care unit in Iran. Oman Med J 2019;34:118-25.  Back to cited text no. 41
    
42.
Yang Q, Rui Y. Two multiplex real-time PCR assays to detect and differentiate Acinetobacterbaumannii and non- baumannii Acinetobacter spp. Carrying blaNDM, blaOXA-23-Like, blaOXA-40-Like, blaOXA-51-Like, and blaOXA-58-Like Genes. PLoS One 2016;11:e0158958.  Back to cited text no. 42
    
43.
Yamamoto M, Nagao M, Matsumura Y, Matsushima A, Ito Y, Takakura S, et al. Interspecies dissemination of a novel class 1 integron carrying bla IMP-19 among Acinetobacter species in Japan. J Antimicrob Chemother 2011;66:2480-3.  Back to cited text no. 43
    
44.
Hakemi Vala M, Hallajzadeh M, Hashemi A, Goudarzi H, Tarhani M, Sattarzadeh Tabrizi M, et al. Detection of Ambler class A, B and D ß-lactamases among Pseudomonas aeruginosa and Acinetobacter baumannii clinical isolates from burn patients. Ann Burns Fire Disasters 2014;27:8-13.  Back to cited text no. 44
    
45.
Tsakris A, Ikonomidis A, Pournaras S, Tzouvelekis LS, Sofianou D, Legakis NJ, et al. VIM-1 metallo-β-lactamase in Acinetobacter baumannii. Emerg Infect Dis 2006;12:981-3.  Back to cited text no. 45
    
46.
Brown S, Amyes SGB. The sequences of seven class D b-lactamases isolated from carbapenem-Resistant Acinetobacter baumannii from four continents. Clin Microbiol Infect 2005;11:326-9.  Back to cited text no. 46
    
47.
Peymani A, Farajnia S, Nahaei MR, Sohrabi N, Abbasi L, Ansarin K, et al. Prevalence of class 1 integron among multidrug-resistant Acinetobacter baumannii in Tabriz, northwest of Iran. Pol J Microbiol 2012;61:57-60.  Back to cited text no. 47
    
48.
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.  Back to cited text no. 48
    
49.
Peymani A, Nahaei MR, Farajnia S, Hasani A, Mirsalehian A, Sohrabi N, et al. High prevalence of metallo-b-lactamase-producing Acinetobacter baumannii in a teaching hospital in Tabriz, Iran. Jpn J Infect Dis2011;64:69-71.  Back to cited text no. 49
    
50.
Yoon EJ, Balloy V, Fiette L, Chignard M, Courvalin P, Grillot-Courvalin C. Contribution of the Ade Resistance-Nodulation-Cell Division-Type Efflux Pumps to Fitness and Pathogenesis of Acinetobacter baumannii.mBio2016;7:e00697-16.  Back to cited text no. 50
    
51.
Khaledi A, Esmaeili D, Jamehdar SA, Esmaeili SA, Neshani A, Bahador A. Expression of MFS efflux pumps among multidrug resistant Acinetobacter baumannii clinical isolates. Der Pharmacia Lettre2016;8:262-7.  Back to cited text no. 51
    
52.
Merkier AK, Centrón D. BlaOXA-51-type β-lactamase genes are ubiquitous and vary within a strain in Acinetobacter baumannii. Int J Antimicrob Agents 2006;28:110-3.  Back to cited text no. 52
    
53.
Naas T, Coignard B, Carbonne A, Blanckaert K, Bajolet O, Bernet C, et al.VEB-1 extended-spectrum β-lactamase–producing Acinetobacter baumannii, France. Emerg Infect Dis 2006;12:1214-22.  Back to cited text no. 53
    
54.
Shahcheraghi F, Abbasalipour M, Feizabadi M, Ebrahimipour G, Akbari N. Isolation and genetic characterization of metallo-β-lactamase and carbapenamase producing strains of Acinetobacter baumannii from patients at Tehran hospitals. Iran J Microbiol2011;3:68-74.  Back to cited text no. 54
    
55.
Yum JH, Yi K, Lee H, Yong D, Lee K, Kim JM, et al. Molecular characterization of metallo-β-lactamase-producing Acinetobacter baumannii and Acinetobacter genomospecies 3 from Korea: Identification of two new integrons carrying the blaVIM-2 gene cassettes. J Antimicrob Chemother 2002;49:837-40.  Back to cited text no. 55
    
56.
Beheshti M, Talebi M, Ardebili A, Bahador A, Lari AR.Detection of AdeABC efflux pump genes in tetracycline-resistant Acinetobacter baumannii isolates from burn and ventilator-associated pneumonia patients. J Pharm Bioallied Sci 2014;6:229-32.  Back to cited text no. 56
    
57.
Ranjbar R, Zayeri S, Afshar D. High Frequency of AdeA, AdeB and AdeC Genes among Acinetobacter baumannii Isolates. Iran J Public Health 2020;49:1539-45.  Back to cited text no. 57
    
58.
Nogbou ND, Nkawane GM, Ntshane K, Wairuri CK, Phofa DT, Mokgokong KK, et al. Efflux pump activity and mutations driving multidrug resistance in Acinetobacter baumannii at a Tertiary Hospital in Pretoria, South Africa. Int J Microbiol 2021;2021:9923816.  Back to cited text no. 58
    
59.
Mobasseri P, Azimi L, Salehi M, Hosseini F, Fallah F. Multi-drug resistance profiles and expression of AdeIJK and AbeM in Acinetobacter baumannii collected from humans by real-time PCR. J Med Bacteriol 2018;7:50-6.  Back to cited text no. 59
    
60.
Angoti G, Bandehpour M, Goudarzi H, Hajizadeh M, Moghaddam MZ, Kouchaki A. Detection of efflux pump genes (adeA, adeB, adeC and abeM) in Acinetobacter baumannii isolated from hospitalize patients, north-west of Iran. Infect Epidemiol Med 2016;2:8-11.  Back to cited text no. 60
    
61.
AlQumaizi KI, Kumar S, Anwer R, Mustafa S. Differential gene expression of efflux pumps and porins in clinical isolates of MDR Acinetobacter baumannii. Life (Basel) 2022;12:419.  Back to cited text no. 61
    
62.
Rafiei E, Shahini Shams Abadi M, Zamanzad B, Gholipour A. The frequency of efflux pump genes expression in Acinetobacter baumannii isolates from pulmonary secretions. AMB Express2022;12:103.  Back to cited text no. 62
    
63.
Rajamohan G, Srinivasan VB, Gebreyes WA.Novel role of Acinetobacter baumannii RND efflux transporters in mediating decreased susceptibility to biocides. J Antimicrob Chemother 2010;65:228-32.  Back to cited text no. 63
    
64.
TahbazSV, AzimiL, Lari AR. Characterization of aminoglycoside resistance mechanisms in Acinetobacter Baumannii isolates from burn wound colonization. Ann Burns Fire Disasters 2019;30:32:115-21.  Back to cited text no. 64
    
65.
Asadollahi K, Taherikalani M, Maleki A, Alizadeh E, Valadbaigi H, Soroush S, et al. Diversity of aminoglycoside modifying enzyme genes among multidrug resistant Acinetobacter baumannii genotypes isolated from nosocomial infections in Tehran hospitals and their association with class 1 integrons. Acta Microbiol Immunol Hung2011;58:359-70.  Back to cited text no. 65
    
66.
Kishk R, Soliman N, Nemr N, Eldesouki R, Mahrous N, Gobouri A, et al. Prevalence of aminoglycoside resistance and aminoglycoside modifying enzymes in Acinetobacter baumannii among intensive care unit patients, Ismailia, Egypt. Infect Drug Resist 2021;14:143-50.  Back to cited text no. 66
    
67.
Rashvand P, Peymani A, Mohammadi M, Karami AA, Samimi R, Hajian S, et al. Molecular survey of aminoglycoside-resistant Acinetobacter baumannii isolated from tertiary hospitals in Qazvin, Iran. New Microbes New Infect 2021;42:100883.  Back to cited text no. 67
    
68.
Hammoudi D, Moubareck CA, Hakime N, Houmani M, Barakat A, Najjar Z, et al. Spread of imipenem-resistant Acinetobacter baumannii co-expressing OXA-23 and GES-11 carbapenemases in Lebanon. Int J Infect Dis 2015;36:56-61.  Back to cited text no. 68
    
69.
Ghaith DM, Zafer MM, Al-Agamy MH, Alyamani EJ, Booq RY, Almoazzamy O. The emergence of a novel sequence type of MDR Acinetobacter baumannii from the intensive care unit of an Egyptian tertiary care hospital. Ann Clin Microbiol Antimicrob 2017;16:34.  Back to cited text no. 69
    
70.
Khalilzadegan S, Sade M, Godarzi H, Eslami G, Hallajzade M, Fallah F, et al. Beta-lactamase encoded genes blaTEM and blaCTX among Acinetobacter baumanniispecies isolated from medical devices of intensive care units in Tehran hospitals. Jundishapur J Microbial 2016;9:e14990.  Back to cited text no. 70
    
71.
Lowe M, Ehlers MM, Ismail F, Peirano G, Becker PJ, Pitout JDD, et al. Acinetobacter baumannii: Epidemiological and beta-lactamase data from two tertiary academic hospitals in Tshwane, South Africa. Front Microbial 2018;9:1280.  Back to cited text no. 71
    
72.
Mak JK, Kim MJ, Pham J, Tapsall J, White PA. Antibiotic resistance determinants in nosocomial strainsof multidrug-resistant Acinetobacter baumannii. J Antimicrob Chemother 2009;63:47-54.  Back to cited text no. 72
    
73.
Yousefi Nojookambari N, Sadredinamin M, Dehbanipour R, Ghalavand Z, Eslami G, Vaezjalali M, et al. Prevalence of β-lactamase-encoding genes and molecular typing of Acinetobacter baumannii isolates carrying carbapenemaseOXA-24 in children. Ann Clin Microbiol Antimicrob 2021;20:75.  Back to cited text no. 73
    
74.
Rynga D, ShariffM, Deb M. Phenotypic and molecular characterization of clinical isolatesof Acinetobacter baumannii isolated from Delhi, India. Ann Clin Microbiol Antimicrob2015;14:40.  Back to cited text no. 74
    
75.
Soltani B, Heidari H, Ebrahim-Saraie HS, Hadi N, Mardaneh J, Motamedifar M. Molecular characteristics of multiple and extensive drug-resistant Acinetobacter baumannii isolates obtained from hospitalized patients in Southwestern Iran. Infez Med 2018;26:67-76.  Back to cited text no. 75
    
76.
Uddin F, McHugh TD, Roulston K, Platt G, Khan TA, Sohail M. Detection of carbapenemases, AmpC and ESBL genes in Acinetobacter isolates from ICUs by DNA microarray. J Microbiol Methods 2018;155:19-23.  Back to cited text no. 76
    
77.
AsaadAM, AnsariS, Ajlan SE, Awad SM. Epidemiology of biofilm producing Acinetobacterbaumannii nosocomial isolates from a tertiary care hospital in Egypt: A cross-sectional study. Infect Drug Resist 2021;14:709-17.  Back to cited text no. 77
    
78.
Behdad R, Pargol M, Mirzaie A, Karizi SZ, Noorbazargan H, Akbarzadeh I. Efflux pump inhibitory activity of biologically synthesized silver nanoparticles against multidrug-resistant Acinetobacter baumannii clinical isolates. J Basic Microbiol 2020;60:494-507.  Back to cited text no. 78
    
79.
Ben RJ, Yang MC, Hsueh JC, Shiang JC, Chien ST. Molecular characterisation of multiple drug-resistant Acinetobacter baumannii isolates in southern Taiwan. Int J Antimicrob Agents 2011;38:403-8.  Back to cited text no. 79
    
80.
Pourhajibagher M, Hashemi FB, Pourakbari B, Aziemzadeh M, Bahador A. Antimicrobial resistance of Acinetobacter baumannii to imipenem in Iran: A systematic review and meta-analysis. Open Microbiol J 2016;10:32-42.  Back to cited text no. 80
    
81.
Eliopoulos GM, Maragakis LL, Perl TM. Acinetobacter baumannii: Epidemiology, antimicrobial resistance, and treatment options. Clin Infect Dis 2008;46:1254-63.  Back to cited text no. 81
    
82.
Manchanda V, Sinha S, Singh NP. Multidrug resistant Acinetobacter.J Global Infect Dis 2010;2:291-304.  Back to cited text no. 82
    
83.
Feizabadi MM, Fathollahzadeh B, Taherikalani M, Rasoolinejad M, Sadeghifard N, Aligholi M, et al. Antimicrobial susceptibility patterns and distribution of blaOXA genes among Acinetobacter spp. Isolated from patients at Tehran hospitals. Jpn J Infect Dis2008;61:274-8.  Back to cited text no. 83
    
84.
Gounden R, Bamford C, van Zyl-Smit R, Cohen K, Maartens G. Safety and effectiveness of colistin compared with tobramycin for multi-drug resistant Acinetobacter baumannii infections. BMC Infect Dis 2009;9:26.  Back to cited text no. 84
    
85.
Ni W, Shao X, Di X, Cui J, Wang R, Liu Y. In vitro synergy of polymyxins with other antibiotics for Acinetobacter baumannii: A systematic review and meta-analysis. Int J Antimicrob Agents 2015;45:8-18.  Back to cited text no. 85
    
86.
Vila J, Martí S, Sánchez-Céspedes J.Porins, efflux pumps and multidrug resistance in Acinetobacter baumannii. J Antimicrob Chemother 2007;59:1210-5.  Back to cited text no. 86
    
87.
Hornsey M, Ellington MJ, Doumith M, Thomas CP, Gordon NC, Wareham DW, et al. AdeABC-mediated efflux and tigecycline MICs for epidemic clones of Acinetobacter baumannii. J Antimicrob Chemother 2010;65:1589-93.  Back to cited text no. 87
    
88.
Poole K. Efflux-mediated multiresistance in Gram-negative bacteria.Clin Microbiol Infect2004;10:12-26.  Back to cited text no. 88
    
89.
Ruzin A, Immermann FW, Bradford PA.RT-PCR and statistical analyses of adeABC expression in clinical isolates of Acinetobacter calcoaceticus-Acinetobacter baumannii complex. Microb Drug Resist 2010;16:87-9.  Back to cited text no. 89
Advanced Biomedical Research
Volume 2023, March
March 2023
Pages 1-15