Global Epidemiology and Antimicrobial Resistance of Metallo-β-Lactamase (MBL)-Producing Acinetobacter Clinical Isolates: A Systematic Review

Abstract

This systematic review assessed the global epidemiology of metallo-β-lactamase (MBL)-producing Acinetobacter clinical isolates and the associated antimicrobial resistance. A total of 475 relevant articles from the Cochrane Library, Google Scholar, PubMed, Scopus, and Web of Science were identified and screened as potentially eligible articles. Data from 85 articles were extracted for the analysis. Most reports on MBL-producing Acinetobacter clinical isolates originated from Asia [68/85 (80%) studies] and Africa [14/85 (16.5%) studies]. There were also scarce reports from Europe and America. The bla_VIM (in 31 studies), bla_IMP (in 29 studies), and bla_NDM (in 21 studies) genes were the most commonly identified genes. In 22 out of 28 (78.6%) studies with comparable data, the proportions of MBL-producing pathogens detected using phenotypic methods were numerically higher than those using genotypic methods. MBL-producing Acinetobacter isolates showed high resistance (up to 100%) to several antibiotic classes, including carbapenems, cephalosporins, fluoroquinolones, and monobactams. However, they showed low resistance to colistin [ranging from 0% (in six studies) to 14.3% (in one study)] and to tigecycline [0% (in three studies)]. No risk of bias assessment was conducted. The findings emphasize the global spread of MBL-producing Acinetobacter and the need for enhanced antimicrobial stewardship, infection control measures, and surveillance.

1. Introduction

Pathogens resistant to antimicrobial agents are increasing worldwide and pose a threat to public health because they cause significant mortality, morbidity, and increased healthcare costs [1]. Many of the most frequently encountered resistant isolates belong to the so-called ‘ESKAPE’ pathogens (Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacterales), for which the treatment options are limited [2,3].

Among these, Acinetobacter baumannii infections are particularly associated with advanced antimicrobial resistance [4]. Such infections are usually healthcare associated, but may also be community acquired [5]. Moreover, patients with Acinetobacter baumannii infections experience high mortality [6], especially when caused by carbapenem-resistant strains [7].

The World Health Organization (WHO) has designated carbapenem-resistant Acinetobacter baumannii as a critical priority pathogen and has called for the development of new therapeutic options to treat these infections [8]. Furthermore, the resistance of Acinetobacter clinical isolates to carbapenems is increasing worldwide, driven by various mechanisms, including the production of β-lactamases [9].

Beta-lactamases inactivate β-lactam antibiotics by hydrolyzing the β-lactam ring. According to the Ambler classification, β-lactamases are divided into four molecular classes: A, B, C, and D [10,11]. Classes A, C, and D have an active serine site, whereas class B [also called metallo-β-lactamases (MBLs)] uses zinc as a cofactor [12,13]. Metal ion chelators like ethylene-diamine-tetra-acetic acid (EDTA) inhibit MBL activity [12], a property utilized in phenotypic tests to detect MBL production [14]. MBLs can hydrolyze almost all β-lactam antibiotics, including carbapenems, with the notable exception of monobactams [15,16].

Previous studies are limited in scope: some examined the regional prevalence of carbapenemase-producing Acinetobacter [17,18,19,20], while others focused specifically on Acinetobacter isolates carrying the bla_NDM gene [21]. However, a gap remains in understanding the global epidemiology of MBL-producing Acinetobacter. The therapeutic options for such infections are limited, as these pathogens are often resistant to most antibiotics. Potential therapeutic options include carbapenems (imipenem and meropenem), polymyxins (colistin and polymyxin B), tigecycline, and new β-lactamase inhibitor combinations (sulbactam–durlobactam and aztreonam–avibactam) [22,23,24,25]. Also, there are antibiotics in the pipeline for treating patients with these infections that could potentially be used as alternatives to the available agents, but currently they are under development in clinical trials [26]. Thus, as it is useful to evaluate the global epidemiology of MBL-producing Acinetobacter, this systematic review aims to address the knowledge gap by assessing the data on this clinically important issue.

2. Methods

2.1. Objectives

The objective of this review was to assess the global epidemiology of MBL-producing Acinetobacter clinical isolates and their resistance profiles in regard to various antimicrobial agents.

2.2. Eligibility Criteria

We included all the research articles reporting on Acinetobacter clinical isolates, with no restrictions in terms of the language, publication date, journal, region, patient demographics (adult or pediatric), or setting (inpatient or outpatient). We excluded gray literature (e.g., conference abstracts and industry reports) and any studies analyzing fewer than 5 Acinetobacter isolates.

We included studies that detected MBLs using genotypic methods [polymerase chain reaction (PCR)] and/or phenotypic methods [combined disk test (CDT), double-disk synergy test (DDST), or E-test]. Both CDT and DDST methods use imipenem plus EDTA disks in different settings to test for MBL production, as EDTA inhibits the action of MBLs. Thus, imipenem can act against the growth of MBL-producing strains [27,28]. For the CDT, a zone of inhibition more than 7 mm around the EDTA–imipenem-containing disk is considered a positive result for the production of MBL [27,29]. For the DDST, inhibition between the imipenem and EDTA disks, placed at a 10 mm distance, is a positive result [28,29]. For the E-test, a strip containing imipenem and EDTA is used [30]. We extracted antimicrobial susceptibility data from the studies that used antibiotic diffusion or microdilution methods for antimicrobial susceptibility testing.

2.3. Search Strategy

We searched five databases on 5 February 2025 (the Cochrane Library, Google Scholar, PubMed, Scopus, and Web of Science), using specific search strings (see Supplementary Table S1). Additionally, we screened the reference lists of the included studies for any further relevant articles.

2.4. Selection of Articles

Two investigators (DSK and MZ) conducted the searches. In Google Scholar, only the first 1000 results were accessible, and no bulk export option is available; therefore, we screened the Google Scholar results by title/abstract manually, before deduplication. All the citations from the Cochrane Library, PubMed, Scopus, and Web of Science were exported into Zotero version 7.0.11 (citation management software). These, combined with the Google Scholar selections, were deduplicated using the SR Accelerator tool. Two reviewers (DSK and MZ) independently screened the articles first based on the title and/or abstract and then by reviewing the full text. Any disagreements were resolved by consensus, during scientific meetings with a senior author (MEF).

2.5. Data Extraction

Two investigators (DSK and MZ) independently extracted and tabulated the key data from each study, including first author and publication year; study location (continent and country); patient population characteristics (e.g., age group, inpatient vs. outpatient); hospital/department setting; specimen type from which Acinetobacter isolates were obtained; identified Acinetobacter species; and the MBL genes tested. The main text was translated, using a web software program, if the studies were in a language other than English. For each study, we evaluated the proportion of Acinetobacter isolates that were MBL producers, as determined by genotypic and/or phenotypic methods. The studies were grouped based on the continent and country where the isolates were detected. If multiple data points were provided in a study regarding the isolation of MBL-producing Acinetobacter isolates, they were all extracted and presented separately (e.g., per isolation period). We also noted the proportion of MBL-producing isolates that were non-susceptible to various antibiotics, when such antimicrobial susceptibility data were available.

2.6. Adherence to the PRISMA Guidelines

This systematic review complies with the most recent “Preferred Reporting Items for Systematic Reviews and Meta-Analyses” (PRISMA) guidelines, and any omission is explicitly reported in the discussion section of this study. The study research protocol was not registered in a database. The PRISMA checklists for the abstract and full-text review are provided in Supplementary Tables S2 and S3, respectively.

3. Results

Identification of Relevant Articles

Figure 1 presents a PRISMA flow diagram on the identification, selection, and inclusion of articles included in this systematic review. In total, our searches yielded 73 articles from Google Scholar and 622 from the other sources. After removing duplicates, 475 articles remained for screening. Ultimately, 85 studies met the inclusion criteria and were included in our analysis, and nine articles were excluded after a full-text evaluation (Figure 1). Three studies did not present data specifically for MBL production in Acinetobacter isolates, three studies reported the isolation of less than five Acinetobacter pathogens, one study reported the isolation of pathogens from surfaces and healthcare workers, one study was a dissertation, and one study was a conference abstract. Sixty-eight of the included studies originated from Asia [31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98], fourteen from Africa [99,100,101,102,103,104,105,106,107,108,109,110,111,112], two from America [113,114], and one from Europe [115].

Table 1 presents the proportions of MBL-producing Acinetobacter isolates identified using genotypic and phenotypic methods, sorted by continent and country. In summary, 68 studies reported clinical Acinetobacter strains isolated from patients in countries in Asia (26 in India, 14 in Iran, 9 in Nepal, 5 in Iraq, 5 in Pakistan, 2 in Japan, 1 in Bangladesh, China, Lebanon, Malaysia, Saudi Arabia, South Korea, Taiwan), 14 in Africa (7 in Egypt, 1 in Algeria, Ghana, Libya, Morocco, South Africa, Sudan, Uganda), 2 in America (1 in Canada and the USA, 1 in Colombia), and 1 in Europe (1 in Romania). Seventy-eight studies included clinical isolates from hospitalized patients, six from both hospitalized patients and outpatients, and only one from outpatients [76]. The isolates were obtained from a variety of clinical specimens, most frequently respiratory sources (e.g., sputum and other respiratory secretions) [in 64 of 76 (84.2%) studies with available relevant data], blood [in 56/76 (73.7%)], and urine [in 50/76 (65.8%)]. Wound swabs were the next most common [in 34/76 (44.7%)], followed by cerebrospinal fluid [in 18/76 (23.7%)], pleural fluid [in 9/76 (11.8%)], burn wound samples [in 3/76 (3.9%)], and other sources.

In the 85 included studies, the most commonly identified Acinetobacter species were Acinetobacter baumannii [in 63/85 (74.1%)], followed by Acinetobacter baumannii–calcoaceticus complex [in 6/85 (7.1%)], and Acinetobacter hemolyticus [in 5/85 (5.9%)]. Other Acinetobacter species were also reported in 12 studies. However, 18/85 (21.2%) studies did not specify the isolated Acinetobacter species.

Forty-seven of the 85 studies included in our analysis (55.3%) employed genotypic methods (PCR) to detect MBL genes. In total, bla_VIM was tested in 31 studies, bla_IMP in 29, bla_NDM in 21, bla_SPM in 7, bla_GIM in 7, bla_SIM in 5, and bla_DIM in 1 study. In Africa, 10/13 (76.9%) studies tested for bla_NDM, 6/13 (46.2%) for bla_VIM, and 5/13 (38.5%) for bla_IMP. However, in Asia, 23/31 (74.2%) studies tested for bla_IMP, 22/31 (71%) for bla_VIM, and 11/31 (35.5%) for bla_NDM. In America, two studies tested for bla_VIM, and 1/2 (50%) studies tested for bla_NDM, bla_VIM, and bla_IMP. In Europe, the one relevant study tested for bla_VIM. Only 8 of the 85 studies (9%) included in our analysis reported data on clones of Acinetobacter baumannii isolates.

Seventy of the 85 studies (82.4%) employed phenotypic tests (CDT, DDST, and/or E-test) for MBL detection. Notably, six studies used modified versions of these tests [52,77,79,80,109,117]. Thirty-two studies (37.6%) used both genotypic and phenotypic methods. In four of those thirty-two studies [55,59,79,112], the data were not directly comparable because the number of isolates tested using each method differed. Thus, 28 studies had directly comparable results between genotypic and phenotypic detection and were analyzed for concordance.

In 22 of the 28 studies (78.6%), phenotypic methods detected a higher proportion of MBL-producing Acinetobacter isolates than genotypic methods. Of those twenty-two studies, eight relied solely on the CDT for phenotypic testing [50,62,65,72,73,102,103,107], six used only the E-test [63,67,68,98,111,117], and three used only the DDST [53,57,64] method. One study used all the CDT, DDST, and E-test methods [100], and two studies used both CDT and E-test methods [51,61]. In one of the last studies, the E-test method had a lower proportion of phenotypic MBL-production detection [117/172 (68.0%)] than the genotypic method [139/172 (80.8%)] in contrast to the CDT method [144/172 (83.7%)] [51]. Also, one study used a modified CDT method, with an increase of more than 10 mm in the zone of inhibition for a positive result [80], and one used the EDTA-modified carbapenem inactivation method [117].

In 4/28 (14.3%) studies, the proportion of MBL-producing Acinetobacter detected was higher using genotypic than phenotypic methods. Among these four studies, two used only the DDST method [39,94], one used only the CDT method [101], and one used both CDT and DDST methods [69]. Finally, in 2/28 (7.1%) studies, the proportion of MBL-producing Acinetobacter detected was equal using the genotypic and phenotypic methods. One study used the CDT [31] and one used the DDST phenotypic method [99].

Table 2 presents data on the antimicrobial resistance of the studied clinical isolates. Among the 33 studies that reported antimicrobial susceptibility data for MBL-producing Acinetobacter, the resistance rates were as high as 100% in regard to most of the tested antibiotics, including carbapenems, cephalosporins, and fluoroquinolones. In five studies, MBL-producing pathogens showed resistance to monobactams too. Notably, in six of seven studies (85.7%) that evaluated colistin (six using antibiotic diffusion methods [34,36,55,66,71,84] and one using the agar dilution method [101]), no colistin resistance was detected among the MBL-producing isolates [34,36,55,66,71,84]. In the remaining study, colistin resistance was 14.3% (6 of 42 MBL-producing isolates) [101]. In addition, in all three studies that evaluated tigecycline, no tigecycline resistance was detected [34,44,87].

4. Discussion

The objective of this study was the assessment of the global epidemiology of MBL-producing Acinetobacter isolates and their resistance to various antimicrobial agents. Our main finding confirms that these isolates have now spread worldwide, with most reported cases coming from Asia and Africa. In most studies, MBL-producing Acinetobacter isolates were 100% resistant to most of the tested antibiotics, including all carbapenems. Interestingly, although MBLs do not hydrolyze monobactams, the studies that tested for aztreonam susceptibility showed high resistance to this agent. This finding implies that these isolates were co-producing other types of lactamases (such as extended-spectrum β-lactamases), thus making them resistant to aztreonam, a monobactam antibiotic.

Colistin was the only agent that retained activity against the majority of these isolates (as most studies reported 0% resistance to colistin). However, all six studies that reported 0% resistance to colistin used disk diffusion methods for antimicrobial susceptibility testing. According to the joint Clinical and Laboratory Standards Institute (CLSI)/European Committee on Antimicrobial Susceptibility Testing (EUCAST) guidelines on colistin susceptibility testing, broth and agar microdilution methods are recommended over diffusion methods [118]. Thus, colistin resistance could be underestimated in these studies, with more false-susceptible pathogens reported, and the 0% percentage of resistance to colistin could have been higher if microdilution methods had been used.

In most studies with comparable data (78.6%), MBL-producing Acinetobacter was more frequently detected using phenotypic methods, specifically the CDT, followed by the DDST and E-test methods. This finding indicates that the genes encoding MBLs in the isolates from these studies possibly differed from those included in the PCR assay. The fact that the CDT detected more MBL-producing isolates compared to the other phenotypic methods is in keeping with results from previous studies demonstrating that this method is more sensitive than the DDST or E-test in regard to identifying MBL-producing pathogens [119,120,121]. Moreover, in Africa, most studies tested for the presence of the bla_NDM, whereas in Asia most studies tested for bla_IMP and bla_VIM, highlighting the different prevalence of MBL genes between these geographical regions. Only a small proportion of studies reported data on the clones of Acinetobacter baumannii isolates.

Data from the included studies were heterogeneous, as patients were in different settings (ICU, other clinical departments, or outpatients) and had various infections. Also, the sources of isolation varied from study to study. These limitations made the analyses and synthesis of the data in the subgroups challenging and, thus, only a descriptive evaluation was conducted.

Antimicrobial resistance (AMR) is a growing global threat in regard to the treatment of infectious diseases. In response to rising AMR, standardized definitions for multidrug-resistant (MDR), extensively drug-resistant (XDR), and pandrug-resistant (PDR) bacteria have been adopted [122]. Briefly, MDR organisms are non-susceptible to ≥1 agent in at least three antibiotic categories, XDR organisms are resistant to all but one or two available categories, and PDR organisms are resistant to all categories [122].

Gram-negative bacteria have emerged as the most problematic causes of MDR/XDR/PDR infections from a public health perspective. In particular, Acinetobacter baumannii, once dismissed as a harmless colonizer, is now understood to cause severe infections. Numerous studies have demonstrated that Acinetobacter baumannii infections lead to considerable morbidity, prolonged hospital stays, higher healthcare costs, and attributable mortality [6,123]. Today, the need for immediate interventions and targeted research initiatives related to Acinetobacter baumannii infections is more urgent than ever. There is an urgent need for immediate interventions and targeted research to address Acinetobacter baumannii infections. Developing new antimicrobials, implementing personalized therapeutic approaches, and strengthening infection prevention and control programs are all crucial strategies to stem this crisis.

The global spread of MDR, XDR, and PDR Acinetobacter baumannii infections, including those caused by MBL-producing isolates, is not solely a consequence of antibiotic misuse and overuse, due to a lack of adherence to antimicrobial stewardship policies. Multiple factors, including inadequate infection control in hospitals and transmission via contaminated medical devices, also drive the spread [124]. Additionally, the genetic flexibility of Acinetobacter baumannii enables it to acquire and maintain resistance genes, complicating efforts to eradicate the bacteria [125]. The increasing use of invasive medical procedures, exposure to disinfectants, and heavy metals, further promote the persistence of resistant strains. Particularly concerning is the spread of MBL-producing strains, facilitated by horizontal gene transfer, plasmids, and resistance islands [125].

Extensive antibiotic resistance dramatically limits treatment options, making the management of patients with MDR Acinetobacter infections extremely challenging. The remaining therapeutic choices, such as polymyxins, tigecycline, and sulbactam, come with significant drawbacks, including nephrotoxicity, gastrointestinal disturbances, and limited effectiveness in certain cases [124,126,127,128]. Also, there are limited data on the clinical use of new antibiotics (cefiderocol and sulbactam–durlobactam) that may have activity against MDR Acinetobacter isolates. Cefiderocol was demonstrated to have considerable antimicrobial activity against Gram-negative bacterial isolates, including Acinetobacter baumannii [129]. Although higher mortality was observed in patients who received cefiderocol in a randomized controlled clinical trial for Acinetobacter baumannii infection, subsequent observational studies suggested better clinical outcomes in patients with Acinetobacter baumannii infection treated with this new siderophore, cephalosporin [130,131,132]. In addition, a non-inferiority randomized controlled trial comparing sulbactam–durlobactam with colistin (both combined with imipenem–cilastatin) in patients with carbapenem-resistant Acinetobacter baumannii infection showed promising results for this new combination of two β-lactamase inhibitors [133,134]. Notably, sulbactam may have activity against Acinetobacter baumannii isolates and has been used in high doses for patients with such infections [135]. This underscores the complexity of managing such infections, highlighting the urgent need for stricter surveillance, enhanced infection control programs, and the development of new therapeutic strategies [126].

Our analysis has several limitations. First, most of the included studies were from single hospitals or limited geographic areas rather than broad multicenter surveillance efforts, which may limit the generalizability of their findings. Second, there was inconsistency in the phenotypic MBL detection methods used among the studies, some used modified tests with different zone diameter cut-offs, which complicates direct comparisons of the MBL rates. Third, our analysis did not include data on some of the newest antimicrobials (e.g., recently developed β-lactam/β-lactamase inhibitor combinations), since most of the included studies were published before those agents became available. In addition, we did not perform a formal quality assessment of the included studies, sensitivity analyses, statistical methods to assess the heterogeneity of the studies, and publication bias (e.g., a tendency to report outbreaks or unusually resistant cases), which might have influenced the literature available. These factors should be kept in mind when interpreting our results.

5. Conclusions

The assessed data show that MBL-producing Acinetobacter strains that cause infections have spread globally. These isolates are associated with advanced antimicrobial resistance and pose a critical therapeutic challenge, with important consequences for global public health. These findings underscore the urgent need for a multifaceted approach, including enhanced antimicrobial stewardship, strengthened infection control measures, and sustained global surveillance, to mitigate the spread of MBL-producing Acinetobacter isolates.

Author Contributions

M.E.F. had the idea for the article. All authors contributed to the methodology used in the article. D.S.K. and M.Z. conducted the literature search, data extraction, and tabulation. M.E.F., D.S.K. and M.Z. contributed to the first version of the manuscript. C.F. and G.S.T. revised the manuscript. All authors have read and agreed to the published version of the manuscript.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data used in the conduction of this study are available upon request.

Conflicts of Interest

The authors declare that there are no conflicts of interest.

Abbreviations

AMR	Antimicrobial resistance
CDT	Combined disk test
CLSI	Clinical and Laboratory Standards Institute
DDST	Double-disk synergy test
EDTA	Ethylene-diamine-tetra-acetic acid
EUCAST	European Committee on Antimicrobial Susceptibility Testing
MBL	Metallo-β-lactamase
MDR	Multidrug resistant
PCR	Polymerase chain reaction
PDR	Pandrug resistant
PRISMA	Preferred Reporting Items for Systematic Reviews and Meta-Analyses
WHO	World Health Organization
XDR	Extensively drug resistant

Footnotes

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Figure and Tables

Figure 1 “Preferred Reporting Items for Systematic Reviews and Meta-Analyses” (PRISMA) flow diagram for identification, screening, and inclusion of articles. ⁱ Even though 16,300 results were retrieved with the Google Scholar search, only the first 1000 results could be accessed. Source: Page MJ, et al. BMJ 2021;372:n71. doi: 10.1136/bmj.n71 [116]. This work is licensed under CC BY 4.0. To view a copy of this license, visit https://creativecommons.org/licenses/by/4.0/ (accessed on 6 February 2025).

Table 1

Proportion of phenotypic and genotypic detection of MBLs in various Acinetobacter species.

Author, Year	Continent	Country	Population, Department, Hospital	Isolate Sources [n/N (%)]	Isolates (n)	Genes (n)	Genotypic Detection; Genes, n/N (%)	Phenotypic Detection; n/N (%), Method
Mesli, 2013 [99]	Africa	Algeria	Three different hospitals in western Algeria, hospital environment and patients admitted to ICU, hematology, surgery, and neurosurgery wards	Tracheal aspirate, urine, rectal swab, wound	A. baumannii (106)A. radioresistens (1)A. nosocomialis (2)A. pittii (4)	bla NDM-1	5/113 (4.4)	5/113 (4.4), DDST
Abd El-Glil, 2015 [100]	Africa	Egypt	ICU patients, Benha University, and Benha Teaching hospitals	Sputum [11/40 (17.5)], exudates [9/10 (22.5)], BAL [7/40 (17.5)], blood [6/40 (15)], urine [3/40 (7.5)]	A. baumannii (40)	bla NDM-1	5/40 (12.5)	26/40 (65), E-test25/40 (62.5), CDT 22/40 (55.0), DDST
Elbrolosy, 2019 [101]	Africa	Egypt	Patients with VAP in different ICUs in Menoufia and Kasr Al Ainy University Hospitals	Tracheal aspirate [64/64 (100)]	A. baumannii (37)A. calcoaceticus (15)A. baumannii–calcoaceticus complex (12)	bla NDM-1	42/64 (65.6)	22/64 (34.4), CDT
El-Din, 2014 [102]	Africa	Egypt	Hospitalized patients, Tanta University Hospital	Diabetic ulcers [26/26 (100)]	A. baumannii (26)	bla VIM bla IMP	Total 6/26 (23.1)blaVIM 4/26 (15.4)blaIMP 2/26 (7.7)	9/26 (34.6), CDT
Fattouh, 2014 [103]	Africa	Egypt	ICU patients, Microbiology Department, Sohag University	Endotracheal secretion [7/21 (33.3)], urine [6/21 (28.6)], blood [4/21 (19)], pus [4/21 (19)]	A. baumannii (21)	bla IMP-1 bla VIM-1	0/21 (0)	13/21 (61.9), CDT
Fouad, 2013 [104]	Africa	Egypt	ICU patients, three hospitals (6th October hospital, MUST hospital, National Cancer Institute)	Respiratory tract [24/53 (45.3)], wound [22/53 (41.5)], urine [6/53 (11.3)], blood [1/53 (1.9)]	A. baumannii (53)	bla VIM	1/53 (1.9)	NR
Hassan, 2021 [105]	Africa	Egypt	Hospitalized and ICU patients, Kasr Al-Aini hospital	Wound [77/206 (37.4)], respiratory secretions [56/206 (27.2), blood [37/206 (18)], urine [27/206 (13.1)], body fluid and drains [9/206 (4.4)]	A. baumannii (206)	bla VIM bla IMP bla GIM bla SPM bla SIM-1 bla NDM-1	Total 39/206 (18.9)blaNDM-1 24/106 (11.7)blaSPM 13/206 (6.3)blaVIM 1/206 (0.5)blaSIM-1 1/206 (0.5)	NR
Wasfi, 2021 [106]	Africa	Egypt	Cancer patients at the National Cancer Institute, Giza, Egypt,	Blood [48/48 (100)]	A. baumannii (48)	bla NDM bla GIM bla SPM bla SIM bla IMP	31/48 (63.6)	NR
Olu-Taiwo, 2020 [107]	Africa	Ghana	Clinical isolates, patients over 50 years old, Korle-Bu Teaching Hospital	Wound [(45/87 (51.7)], urine [25/87 (28.7)], ear swabs [8/87 (9.2)], eye swabs [6/48 (6.9)] aspirates [3/48 (3.5)]	Acinetobacter spp. (87)	bla NDM	7/87 (8)	23/87 (26.4), CDT
Mathlouthi, 2016 [108]	Africa	Libya	Clinical isolates, Tripoli Medical Center and Burn and Plastic Surgery Hospital in Tripoli	Wound [15/36 (41.6)], catheter [3/36 (8.3)], septum [3/36 (8.3)], swab [3/36 (8.3)], urine [3/36 (8.3)], blood [2/36 (5.6)], CSF [2/36 (5.6)], chest tube [1/36 (2.8)], endotracheal tube [1/36 (2.8)], GT tube [1/36 (2.8)], mouth [1/36 (2.8)], throat [1/36 (2.8)]	A. baumannii (36)	bla NDM-1	7/36 (22.2)	NR
Kabbaj, 2013 [109]	Africa	Morocco	Hospitalized patients, ICU, neurosurgery ward, neurology ward, Rabat Specialty Hospital	Respiratory tract (69), urine (22), surgical site infection (5), CSF (4)	A. baumannii (47)	NR	NR	20/47 (24.6) i
Nogbou, 2021 [110]	Africa	South Africa	Clinical isolates, teaching hospital in Pretoria	NR ii	A. baumannii (70)	bla VIM bla IMP-5 bla NDM bla SIM-1	blaVIM 60/70 (85.7)blaNDM 41/70 (58.6)blaIMP-5 5/70 (7.1)blaSIM-1 2/70 (2.9)	NR
Elbadawi, 2021 [111]	Africa	Sudan	Children and adults, neonatal ICU, medicine, pediatric, and surgery wards, ICU, renal unit, Soba University Hospital	Blood (36), wound (24), urine (21), body fluids (7), catheter tips (6), sputum (6)	A. baumannii (36)	bla NDM	17/36 (47.2)	19/36 (52.8), E-test
Kateete, 2016 [112]	Africa	Uganda	Hospitalized patients, hospital environment, Mulago Hospital in Kampala	Hospital environment [11/40 (27.5)], tracheal aspirate [9/40 (22.5)], ear swabs [8/40 (20)], pus [4/40 (10)], blood [4/40 (10)], sputum [2/40 (5)], body fluids [1/40 (2.5)]	A. baumannii (40)	bla VIM-1	2/15 (40)	3/40 (7.5), DDST
Rakhi, 2019 [31]	Asia	Bangladesh	Clinical isolates, Dhaka Medical College Hospital	Blood, pleural fluid, pus, tracheal aspirate, urine, vaginal swab, wound	A. baumannii (4)	bla NDM	blaNDM + blaOXA-48 1/4 (25)	1/4 (25), CDT
Li, 2013 [32]	Asia	China	Medical and surgical wards, ICU, burn department, teaching hospital in Guangzhou	Respiratory tract [35/42 (83.3)], blood [3/42 (7.1)], wound [2/42 (4.8)], urine [1/42 (2.4)], CSF [1/42 (2.4)]	A. baumannii (42)	NR	NR	1/42 (2.4), E-test
Ahir, 2012 [33]	Asia	India	Hospitalized patients, tertiary care teaching hospital, Gujarat	Swab [40/78 (51.3)], urine [8/78 (10.3)], sputum [7/78 (9)], pleural fluid [7/78 (9)], pus [5/78 (6.4)], blood [67.7)], other body fluid [5/78 (6.4)] iii	A. baumannii (40)A. lwoffii (20)A. hemolyticus (10)A. calcoaceticus (8)	NR	NR	78/750 (10.4), CDT and DDST
Archana Rao, 2024 [34]	Asia	India	Pediatrics, medical, surgery, ENT, and gynecology wards, Raja Rajeswari Medical College tertiary care hospital	Sputum [14/25 (56)], pus [4/25 (16)], urine [3/25 (12)], ear discharge [2/25 (8)], blood [2/25 (8)]	Acinetobacter spp. (25)	NR	NR	5/25 (20), CDT
Banerjee, 2015 [35]	Asia	India	Clinical isolates, Mayo Institute of Medical Sciences and Hospital, Barabanki	Endotracheal tube [17/67 (25.4)], sputum [16/67 (23.9)], pus [13/67 (19.4)], blood [9/67 (13.4)], urine [7/67 (10.4)], ascitic fluid [5/67 (7.5)]	Acinetobacter spp. (67)	NR	NR	16/67 (23.9), CDT
Binnani, 2018 [36]	Asia	India	Clinical isolates, Tertiary Care Institute in the North West Region of Rajasthan, India	Urine [6/21 (28.6)], sputum and respiratory tract specimens [8/21 (38.1)], blood [5/21 (23.8)], pus and other wounddischarges [2/21 (9.5)]	Acinetobacter spp. (21)	NR	NR	8/21 (38.1), CDT
De, 2010 [37]	Asia	India	Adults, children, intensive care areas in Lokmanya Tilak Municipal Medical College and Hospital	Blood, endotracheal secretions	Acinetobacter spp. (25)	ΝR	NR	9/25 (36), DDST
Gautam, 2023 [38]	Asia	India	Hospitalized and outpatients, children and adults, Central Referral Hospital located in Gangtok, Sikkim	Endotracheal tube, sputum, pus, urine, blood, catheter tips, urogenital swabs	A. baumannii (307)	bla IMP-1 bla VIM-1	blaIMP-1 4/100 (4)blaVIM-1 8/100 (8)	NR
Girija, 2018 [39]	Asia	India	Patients with severe urinary tract infections	Urine [73/73 (100)]	A. baumannii (73)	bla VIM bla GIM	Total 37/73 (50.7)blaVIM 25/73 (34.2)blaGIM 12/73 (16.4)	31/73 (42.5), DDST
Goel, 2017 [40]	Asia	India	ICU patients, teaching tertiary care hospital	Transtracheal or bronchoscopic aspirates [88/88 (100)]	A. baumannii (88)	NR	NR	28/37 (75.7), DDST iv
Hodiwala, 2013 [41]	Asia	India	Clinical isolates	Blood, catheter tips, CSF, endotracheal secretions, pus, sputum, urine, various body fluids (synovial, ascitic, pleural)	A. baumannii (68)	NR	NR	9/68 (13.2), CDT and DDST
Jena, 2014 [42]	Asia	India	Outpatients, ICU, neonatal ICU, IMS and SUM Hospital in Bhubaneswar	Blood, urine, stool, pus, sputum, wound, tracheal aspiration, CSF, high vaginal swab	Acinetobacter spp. (66)	NR	NR	23/66 (34.8), DDST
Jethwa, 2013 [43]	Asia	India	Clinical isolates, tertiary care hospital	Swab [334/854 (39.1)], blood [278/854 (32.6)], body fluids [94/854 (11)], sputum [65/854 (7.6)], pus [39/854 (4.6)], urine [35/854 (4.1)], other [9/854 (1.1)]	Acinetobacter spp. (854)	NR	NR	68/854 (8), CDT
John, 2011 [44]	Asia	India	Clinical isolates, ICU patients	Urine, blood, sputum, pus, endotracheal aspirates, bronchial secretions, wound swabs, vaginal swabs	A. baumannii (242)	NR	NR	36/242 (14.8), DDST
Kaur, 2014 [45]	Asia	India	Clinical isolates, microbiology department	Respiratory samples, pus, blood, others, urine	A. baumannii (389)	NR	NR	313/389 (80.5), CDT
Kaur, 2018 [46]	Asia	India	Clinical isolates, ICU and medical wards, Microbiology Department, Adesh Institute of Medical Sciences and Research, Bathinda	Endotracheal tube secretions [34/116 (29.3)], tracheal aspirate [28/116 (24.1)], pus [29/116 (25)], urine [9/116 (7.8)], sputum [7/116 (6)], blood [6/116 (5.2)], various body fluids [3/116 (2.6)]	A. baumannii (116)	NR	NR	52/116 (44.8), CDT
Kumar, 2013 [47]	Asia	India	Clinical isolates, tertiary care hospital	NR ii	Acinetobacter spp. (180)	NR	NR	43/180 (29.3), DDST
Pandya, 2016 [48]	Asia	India	Clinical isolates, medical wards including ICU, Teaching Hospital in rural Gujarat	Endotracheal secretions [26/81 (32.1)], pus [16/81 (19.8)], tracheostomy secretions [12/81 (14.8)], blood [6/81 (7.4)], sputum [6/81 (7.4)], urine [6/81 (7.4)], broncho-alveolar lavage [3/81 (3.7)], central venous catheter tip [2/81 (2.5)], ascitic fluid [1/81 (1.2)], catheter tip [1/81 (1.2)], drain [1/81 (1.2)], pleural fluid [1/81 (1.2)]	A. baumannii (81)	NR	NR	24/81 (29.6), CDT
Patil, 2021 [49]	Asia	India	Clinical isolates, patients with VAP, ICU, tertiary care hospital	Respiratory tract [246/246 (100)]	Total (188)A. baumannii (156)A. lwoffii (15)A. calcoaceticus (9)A. hemotyticus (5)A. baumannii–calcoaceticus complex (3)	NR	NR	146/188 (77.7), CDT141/188 (75), DDST152/188 (80.9), E-test
Rynga, 2015 [50]	Asia	India	ICU (28%), burns (15%), respiratory (15%), surgery (14%), burns ICU (10%), gynecology (9%), orthopedic (5%) wards, respiratory medicine outpatient department (2%)	Endotracheal aspirate [31/100 (31)], pus [28/100 (28)], wound [25/100 (25)], sputum [14/100 (14)], drain fluid [1/100 (1)], high vaginal swab [1/100 (1)]	A. baumannii (100)	bla VIM bla GIM bla SIM bla IMP	Total 18/100 (18)blaVIM 9/100 (9)blaGIM 6/100 (6)blaSIM 2/100 (2)blaIMP 1/100 (1)	25/100 (25), CDT
Saikia, 2023 [51]	Asia	India	Hospitalized patients, ICU, internal medicine wards, Dibrugarh University	NR ii	A. baumannii (172)	bla NDM bla IMP bla VIM	Total 139/172 (80.8)blaNDM 121/172 (70.3)blaIMP 88/172 (51.2)blaVIM 42/172 (24.4)	144/172 (83.7), CDT117/172 (68), E-test
Singla, 2013 [52]	Asia	India	Outpatients, hospitalized patients, adults and children, tertiary care hospital	Blood, BAL, CSF, endotracheal aspirates, high vaginal swabs, pus, sputum, throat swabs, urine, wound, other body fluids	Total (70)A. baumannii (66)A. lwoffii (4)	NR	NR	A. baumannii 38/66 (57.6)A. lwoffii 1/4 (25), modified CDT method v
Sinha, 2013 [53]	Asia	India	Hospitalized patients, tertiary care center	Pus [52/140 (37.1)], blood [32/140 (22.6)], urine [19/140 (13.6)]	Total (140)A. baumannii (129)A. lwoffii (9)A. hemolyticus (2)	bla IMP-1 bla VIM-1 bla VIM-2	10/140 (7.1)	16/140 (11.4), DDST
Sugumaran, 2019 [54]	Asia	India	Hospitalized patients (81.2%), outpatients (18.8%), Mahatma Gandhi Medical College and Research Institute, Puducherry	Aspirates, central line catheter tip, ear swab, endotracheal tube, groin swab, pus, sputum, synovial fluid, tissue, urine, wound	A. baumannii (19)	NR	NR	10/19 (90.9), imipenem CDT10/19 (90.9), imipenem DDST13/19 (68.9), ceftazidime CDT13/19 (68.9), ceftazidime DDST
Thakar, 2021 [55]	Asia	India	Hospitalized patients, outpatients, tertiary care hospital	Pus [30/72 (41.7)], respiratory tract [16/72 (22.2)], urine [16/72 (22.2)], blood [6/72 (8.3)], others [4/72 (5.6)]	Acinetobacter spp. (72)	bla VIM	15/15 (100)	32/72 (44.4), CDT
Tripathi, 2013 [56]	Asia	India	Clinical isolates, microbiology department	NR ii	Acinetobacter spp. (46)	NR	NR	40/46 (87), CDT
Uma Karthika, 2009 [57]	Asia	India	ICU, acute medical care units, Pondicherry Institute of Medical Sciences tertiary care hospital	Blood, CSF, endotracheal tube, urine, wound	A. baumannii (36)	bla IMP-1 bla VIM-2	Total 23/54 (42.6)blaIMP-1 23/54 (42.6)blaVIM-2 0/54 (0)	39/54 (72.2), DDST
Vamsi, 2021 [58]	Asia	India	Hospitalized patients, SVS Medical College, Hospital in Mahabubnagar	Endotracheal tube [12/17 (70.6)], pus [2/17 (11.8)], blood [1/17 (5.9)], CSF [1/17 (5.9)], urine [1/17 (5.9)]	Acinetobacter spp. (23)	NR	NR	17/23 (73.9) vi
Aghamiri, 2016 [59]	Asia	Iran	Hospitalized patients, 11 hospitals in Tehran	Wound [59/176 (33.5)], tracheal aspirate [34/176 (19.3)], urine [24/176 (13.6)], body fluids [20/176 (11.4)], sputum [11/176 (6.3)], catheter [10/176 (5.7)], blood [18/176 (1)]	A. baumannii (176)	bla IMP bla VIM	123/176 (69.9)	165/169 (97.6), DDST
Jahantigh, 2023 [60]	Asia	Iran	Hospitalized patients, Ali Ebne Abitaleb Hospital in Zahedan, Iran	Blood (39.5), endotracheal tube (34.4), wound (20.7)	A. baumannii (372)	NR	NR	352/372 (94.6), CDT
Khaledi, 2019 [61]	Asia	Iran	Hospitalized patients, Kashani and Hajar Hospitals in Shahrekord	Blood, CSF, pleural effusion, trachea, urine, wound	A. baumannii (100)	bla VIM-1 bla IMP-1	Total 26/100 (26)blaVIM-1 23/100 (23)blaIMP-1 3/100 (3)	65/100 (65), E-test59/100 (59), CDT
Maspi, 2016 [62]	Asia	Iran	Hospitalized patients, Baqiyatallah hospitals	Wound, pleural effusion, urine, blood, tracheal aspirate, BAL, sputum, ascites, abscess	A. baumannii (86)	bla IMP bla SPM bla VIM bla GIM bla SIM	Total 23/86 (26.7)blaIMP 13/86 (15.1)blaSPM 4/86 (4.7)blaVIM 2/86 (2.3)blaGIM 2/86 (2.3)blaSIM 2/86 (2.3)	44/86 (51.2), CDT
Moghadam, 2016 [63]	Asia	Iran	Hospitalized patients, Nemazee and Faghihi hospitals	Sputum [35/98 (35.7)], wound (15/98 (15.3)], body fluids [13/98 (13.3)], blood [9/98 (9.2)], urine [9/98 (9.2)], endotracheal tube [8/98 (8.2)], CSF [5/98 (5.1)], BAL [2/98 (2)], axillary swab [1/98 (1)], eye swab [1/98 (1)]	A. baumannii (96)	bla IMP bla VIM bla SPM	Total 37/96 (38.5)blaIMP 23/96 (24)blaVIM 14/96 (14.6)blaSPM 0/96 (0)	43/96 (44.8), E-test
Moulana, 2020 [64]	Asia	Iran	Clinical isolates, units at Babol University of Medical Sciences affiliated hospitals	Endotracheal aspirates, sputum [30/50 (60)], ulcers [12/50 (24)], urinary specimens [6/50 (12)], blood [2/50 (4)]	A. baumannii (50)	bla VIM	13/50 (26)	15/50 (30), DDST
Noori, 2014 [65]	Asia	Iran	Hospitalized patients, Loghman Hakim and Milad hospitals	Tracheal tube [57/108 (52.8)], urine [29/108 (26.9)], blood [8/108 (7.4)], pleural fluid [8/108 (7.4)], wound [4/108 (3.7)], other [2/108 (1.9)]	A. baumannii (108)	bla IMP bla SPM	Total 3/108 (2.8)blaIMP 3/108 (2.8)blaSPM 0/108 (0)	86/108 (88.9), CDT
Owlia, 2012 [66]	Asia	Iran	Hospitalized patients, burn unit in Motahari Hospital, Tehran	Burns [126/126 (100)]	A. baumannii (126)	NR	NR	42/126 (33.3), DDST
Peymani, 2011 [67]	Asia	Iran	Hospitalized patients, tertiary care teaching hospital	Tracheal aspirate [37/100 (37)], urine [21/100 (21)], sputum [9/100 (9)], blood [7/100 (7)], catheter [6/100 (6)], bronchial washings [6/100 (6)], wound [5/100 (5)], abscess [3/100 (3)], CSF [2/100 (2)], ascites [2/100 (2)], pleural effusion [2/100 (2)]	A. baumannii (100)	bla IMP bla VIM	Total 28/100 (28)blaIMP 19/100 (19)blaVIM 9/100 (9)	31/100 (31), E-test
Ranjbar, 2019 [68]	Asia	Iran	Patients with burns, three major hospital centers	Burns [163/163 (100)]	A. baumannii (163)	bla IMP bla VIM	111/163 (68.1)	147/163 (90.2), E-test
Rezaei, 2018 [69]	Asia	Iran	ICU patients, three teaching hospitals located in Isfahan	Tracheal aspirate (68/100 (68)], CSF [10/100 (10)], wound [9/100 (9)], sputum [3/100 (3)], blood [3/100 (3)], catheters [2/100 (2)], other samples [5/100 (5)]	A. baumannii (100)	bla IMP-1 bla VIM-1 bla VIM-2 bla IMP-2	Total 38/100 (38)blaIMP-1 21/100 (21)blaVIM-1 7/100 (7)blaVIM-2 6/100 (6)blaIMP-2 4/100 (4)	36/100 (36), CDT21/100 (21), DDST
Safari, 2013 [70]	Asia	Iran	Hospitalized patients, ICU, three educational hospitals in Hamadan city	Tracheal aspirate [74/100 (74)], blood [16/100 (16)], urine [5/100 (5)], sputum [4/100 (4)], wound [1/100 (1)]	A. baumannii (100)	NR	NR	99/100 (99), E-test
Soltani, 2018 [71]	Asia	Iran	Hospitalized patients, Nemazee tertiary care hospital	Respiratory tract [61/92 (66.3)], blood [11/92 (12)], skin [8/92 (8.7)], urine [5/92 (5.4)], body fluids [5/92 (5.4)], eyes [2/92 (2.2)]	A. baumannii (92)	bla VIM bla IMP bla SPM	76/92 (82.6)	NR
Vala, 2014 [72]	Asia	Iran	Hospitalized patients, burn unit at Shahid Motahari Hospital	Wound [28/28 (100)]	A. baumannii (28)	bla SPM bla IMP bla VIM bla DIM bla NDM bla GIM	blaSPM 1/28 (3.6)	12/28 (42.9), CDT
Al Marjani, 2013 [73]	Asia	Iraq	Clinical isolates, medical centers in Baghdad	NR ii	A. baumannii (17)	bla IMP-1	3/17 (42.8)	7/17 (41.1), CDT
Anoar, 2014 [74]	Asia	Iraq	Clinical isolate, Burn and Plastic Surgery Hospital in Sulaimani city	Wound [44/44 (100)]	Acinetobacter spp. (44)	bla IMP bla VIM	blaIMP 19/44 (43.2)blaVIM 5/44 (11.4)	NR
Numan, 2022 [75]	Asia	Iraq	Hospitalized patients, four hospitals in Baghdad	Sputum [35/69 (50.7)], blood [21/69 (30.4)], urine [9/69 (13)], CSF [2/69 (2.9)], wound [2/69 (2.9)]	A. baumannii (69)	NR	NR	51/69 (74), CDT
Radhi, 2019 [76]	Asia	Iraq	Outpatients, Hillah Teaching Hospital and Babylon Teaching Hospital for Maternity and Pediatrics	Burns [24/30 (80)], blood [4/30 (13.3)], urine [1/30 (3.3)], wound [1/30 (3.3)]	A. baumannii (30)	NR	NR	22/30 (73.3), E-test
Smail, 2019 [77]	Asia	Iraq	Hospitalized patients, ICU, three educational hospitals in Hamadan city	Blood, CSF, pleural fluid, pus, sputum, urine, wound	A. baumannii (112)	NR	NR	112/112 (100) vii
Kishii, 2014 [78]	Asia	Japan	Clinical isolates, two university hospitals	Blood [123/123 (100)]	Acinetobacter spp. (123)	bla IMP	3/123 (2.4)	NR
Yamamoto, 2013 [79]	Asia	Japan	Clinical isolates, three university hospitals, two city hospitals in Kyoto and Shiga Prefecture	NR ii	Acinetobacter spp. (82)	bla IMP bla VIM bla NDM-1	48/54 (88.9)	44/82 (53.7) viii
Soudeiha, 2018 [80]	Asia	Lebanon	Hospitalized patients, Saint George Hospital University Medical Center	Respiratory tract [62/100 (62)], wound [21/100 (21)], urine [10/100 (10)], blood [4/100 (4)], catheters [3/100 (3)]	Total (100)A. baumannii–calcoaceticus complex (95)A. hemolyticus (3)A. radioresistens (1)A. junii (1)	bla VIM bla IMP bla NDM	0/100 (0)	Total 4/100 (4) ix
Maziz, 2021 [81]	Asia	Malaysia	Clinical isolates, Selayang Hospital, Kuala Lumpur	Urine [16/50 (38)], blood [14/50 (26)], pus [7/50 (14)], skin [5/50 (10)], respiratory secretions [3/50 (6)] and sputum [3/50 (6)]	Acinetobacter spp. (50)	NR	NR	0/50 (0), DDST and E-test
Koirala, 2017 [82]	Asia	Nepal	Clinical isolates, B&B Hospital Kathmandu	Pus [36/109 (33)], suction tip [23/109 (21.1)], sputum [19/109 (17.4)], tracheostomy [16/109 (14.7)], catheter tip [7/109 (6.4)], central venous catheter [6/109 (5.5)], body fluids [1/109 (0.9)], urine [1/109 (0.9)]	Acinetobacter spp. (109)	NR	NR	48/109 (44), CDT
Kumari, 2021 [117]	Asia	Nepal	Clinical isolates, Koirala Institute of Health Sciences	Blood, pus, urine, sputum, endotracheal aspirate, exudate body fluid, central venous catheter, CSF, high vaginal swab, nasal swab, tissue, semen	Total (324)A. baumannii–calcoaceticus complex (167)A. lwoffii (83)A. hemolyticus (38)A. radioresistens (30)A. junii (6)	bla NDM-1	Total 33/324 (10.2)A. baumannii–calcoaceticus complex 28/167 (16.8)A. junii 1/6 (16.7)A. hemolyticus 2/38 (5.2)A. lwoffii 2/83 (2.4)	Total 70/324 (21.6)A. baumannii–calcoaceticus complex 56/167 (33.5)A. lwoffii 3/83 (3.6)A. hemolyticus 7/38 (18.4)A. radioresistens 3/30 (10.0)A. junii 1/6 (16.7), EDTA-modified carbapenem inactivation method
Mishra, 2012 [84]	Asia	Nepal	Clinical isolates, bacteriology laboratory at Tribhuvan University Teaching Hospital	Lower respiratory tract [60/60 (100)]	Total (62)A. baumannii–calcoaceticus complex (60)A. lwoffii (2)	NR	NR	3/62 (4.8), CDT and DDST
Pandey, 2021 [85]	Asia	Nepal	Clinical isolates, 100-bed hospital in the capital city of Nepal	Sputum [25/39 (64.1)], urine [9/39 (23.1)], pus [2/39 (5.1)], catheters and tubes [2/39 (5.1)], blood [1/39 (2.6)]	A. baumannii (39)	NR	NR	4/39 (10.3), CDT and E-test
Pathak, 2017 [86]	Asia	Nepal	Clinical isolates, Shahid Gangalal National Heart Centre, Kathmandu, Nepal	Urine [5/11 (45.5)], endotracheal tube [2/11 (18.2)], suction tip [2/11 (18.2)], central venous catheter tip [1/11 (9.1)], pericardial fluid [1/11 (9.1)]	Acinetobacter spp. (11)	NR	NR	1/11 (9.1), CDT
Sakuma, 2024 [87]	Asia	Nepal	Clinical isolates, university hospital in Nepal	Respiratory tract [28/66 (42.4)], pus [16/66 (24.2)], blood [9/66 (13.6)], wound [7/66 (10.6)], urine [3/66 (4.5)], body fluids [3/66 (4.5)]	A. baumannii (66)	bla NDM-1	26/66 (39.4)	NR
Shrestha, 2015 [88]	Asia	Nepal	Hospitalized patients, Tribhuvan University Teaching Hospital	Respiratory tract [60/122 (49.2)], pus [31/122 (25.4)], urine [13/122 (10.7)]	A. baumannii (122)	NR	NR	50/122 (41), CDT
Thapa, 2017 [89]	Asia	Nepal	Hospitalized and outpatients, Nepal Medical College, Kathmandu	Pus [21/58 (36.2)], urine [21/58 (36.2], sputum [10/58 17.2)], body fluids [6/58 (10.3)]	A. baumannii–calcoaceticus complex (58)	NR	NR	18/58 (31), CDT
Yadav, 2020 [90]	Asia	Nepal	Hospitalized patients, Tribhuvan University Teaching Hospital	Respiratory tract [76/161 (47.2)], pus [44/161 (27.3)], CSF [18/161 (11.1)], urine [11/161 (6.8)], blood [10/161 (6.2)], catheters [2/161 (1.2)]	A. baumannii (161)	ΝR	NR	109/161 (67.7), CDT
Anwar, 2016 [91]	Asia	Pakistan	Clinical isolates, children, Children’s Hospital and Institute of Child Health Lahore	Blood, body fluids, pus, sputum, tracheal secretions, urine	A. baumannii (66)	NR	NR	63/66 (95.5), CDT51/66 (72.3), DDST
Hasan, 2014 [92]	Asia	Pakistan	Clinical isolates, patients with secondary or nosocomial infections from different hospitals in Pakistan	Catheters and tubes [5/19 (26.3)], tracheal aspirate [4/19 (21.1)], blood [4/19 (21.1)], pus [2/19 (10.5)], wound [2/19 (10.5)], body fluids [1/19 (5.3)]	A. baumannii (90)	bla NDM-1	1/90 (1.1)	NR
Irfan, 2008 [93]	Asia	Pakistan	Clinical isolates, Aga Khan University Hospital	Blood, respiratory secretions, urine, wound	Acinetobacter spp. (90)	NR	NR	83/90 (92.2), CDT
Rashid, 2020 [94]	Asia	Pakistan	Clinical isolates, tertiary care referral hospitals	Blood, CSF, pus, sputum, urine, vaginal swab	A. baumannii (12)	bla NDM-1	2/12 (16.7)	(5), DDST
Sajjad, 2019 [95]	Asia	Pakistan	Clinical isolates, Lahore General Hospital	NR ii	A. baumannii (13)A. junii (1)	NR	NR	A. baumannii 11/13 (84.6), DDSTA. junii 0/1 (0), DDST
Shah, 2019 [96]	Asia	Saudi Arabia	Clinical isolates, King Abdulaziz University Hospital, an 845-bed major territory care hospital in Jeddah	Tracheal aspirate [29/135 (21.5)], blood [28/135 (20.7)], wound [19/135 (14.1), urine [19/135 (14.1)], body fluids [7/135 (5.2)], catheters and tubes [9/135 (6.7)], skin [5/135 (3.7)], others [19/135 (14.1)]	A. baumannii (135)	bla IMP bla VIM bla NDM	blaIMP 113/135 (83.7)blaVIM 25/135 (18.5)blaNDM 2/135 (1.5)	NR
Sung, 2015 [97]	Asia	South Korea	Clinical isolates, university hospital in Daejeon	Urine [18/21 (85.7)], sputum [2/21 (9.5)], wound [1/21 (4.8)]	A. pittii (21)	bla IMP-1 bla NDM-1	blaIMP-1 19/21 (90.5)blaNDM-1 2/21 (9.5)	NR
Lee, 2008 [98]	Asia	Taiwan	Clinical isolates, Kaohsiung Medical University Hospital	NR ii	Total (185)A. baumannii (184)A. hemolyticus (1)	bla VIM-2 bla VIM-3 bla VIM-11 bla IMP-8	Total 79/185 (42.7)A. hemolyticus 1/1 (100)A. baumannii 78/184 (42.3)	Total 80/185 (43.2), E-testA. baumannii 79/184 (42.9)A. hemolyticus 1/1 (100)
Mereuţă, 2013 [115]	Europe	Romania	Clinical isolates, five university hospitals in Iasi	Urine [5/16 (31.3)], pus [5/16 (31.3)], sputum [3/16 (18.8)], tracheal aspirate [1/16 (6.3)], blood [1/16 (6.3)], CSF [1/16 (6.3)]	A. baumannii (16)	bla VIM	2/16 (12.5)	3/16 (18.8), E-test
Takemura, 2023 [113]	North America	Canada	Clinical specimens	NR ii	A. baumannii (20)	bla IMP bla VIM bla NDM bla GIM	blaNDM 1/20 (5)	NR
Takemura, 2023 [113]	North America	USA	Clinical isolates, SIDERO-WT surveillance studies	NR ii	A. baumannii (20)	blaIMP blaVIM blaNDM blaGIM	blaNDM 2/20 (10)	NR
Hernández-Gómez, 2014 [114]	South America	Colombia	Adult, pediatric, and neonatal ICU patients, 23 clinics and hospitals	Blood, urine, respiratory tract, other	A. baumannii (241)	bla VIM	0/241 (0)	NR

Abbreviations: MBL, metallo-β-lactamase; DDST, double-disk synergy test; BAL, bronchoalveolar lavage; CDT combined disk test; VAP, ventilator-associated pneumonia; CSF, cerebrospinal fluid. Notes: ⁱ >17 mm zone of inhibition positive for MBL production; ⁱⁱ not available data for the specific sources of isolation; ⁱⁱⁱ information available only for MBL-producing strains; ^iv 37 meropenem-resistant isolates were tested for MBL production; ^v 30 μg ceftazidime, 10 μg imipenem, 0.5 M EDTA, ceftazidime with ≥5 mm zone of inhibition, and/or meropenem with ≥7 mm zone of inhibition positive for MBL production; ^vi does not specify which test produced the specific results for Acinetobacter spp. (CDT, DDST, or E-test); ^vii modified CDT method: meropenem, imipenem, 0.35 M EDTA, ≥2 mm zone of inhibition considered positive for MBL production; ^viii modified CDT method: two disks 30 μg ceftazidime, one disk 3 mg sodium mercaptoacetic acid, ≥5 mm zone of inhibition considered positive for MBL production; ^ix modified CDT method: meropenem and imipenem, 5 mM EDTA, ≥10 mm zone of inhibition considered positive for MBL production.

Table 2

Proportion of the studied resistant MBL-producing Acinetobacter clinical isolates to various antimicrobial agents.

Author, Year	Continent	Country	Isolates (n)	Resistance n/N (%) to Antimicrobial Agent(s) i
Abd El-Glil, 2015 [100]	Africa	Egypt	A. baumannii (40)	5/5 (100) imipenem, meropenem, piperacillin, cefotaxime, ceftazidime, cefepime, aztreonam, ciprofloxacin4/5 (80) amikacin3/5 (60) gentamicin
Elbrolosy, 2019 [101]	Africa	Egypt	A. baumannii (37), A. calcoaceticus (15), A. baumannii–calcoaceticus complex (12)	42/42 (100) imipenem, meropenem, cefotaxime, ceftriaxone, ceftazidime, cefepime, cotrimoxazole, piperacillin–tazobactam, tetracycline, aztreonam, ciprofloxacin, amikacin6/42 (14.3) colistin
Olu-Taiwo, 2020 [107]	Africa	Ghana	Acinetobacter spp. (87)	23/23 (100) ampicillin, cefotaxime, ceftazidime, cefuroxime, meropenem22/23 (95.7) amoxicillin–clavulanate, levofloxacin21/23 (91.3) gentamicin20/23 (87) ciprofloxacin17/23 (73.9) cotrimoxazole14/23 (60.9) nitrofurantoin8/23 (34.8) amikacin
Kateete, 2016 [112]	Africa	Uganda	A. baumannii (40)	3/3 (100) ciprofloxacin, imipenem, meropenem, piperacillin–tazobactam2/3 (66.7) gentamicin, ceftazidime, aztreonam, amikacin
Archana Rao, 2024 [34]	Asia	India	Acinetobacter spp. (25)	0/5 (0) colistin, tigecycline5/5 imipenem and/or meropenem
Binnani, 2018 [36]	Asia	India	Acinetobacter spp. (21)	8/8 (100) ceftazidime, doxycycline, imipenem, meropenem, nitrofurantoin7/8 (87.5) ceftriaxone, ciprofloxacin5/8 (62.5) amikacin0/8 (0) colistin, polymyxin B
De, 2010 [37]	Asia	India	Acinetobacter spp. (25)	9/9 (100) imipenem, gentamicin, amikacin, netilmicin, amoxicillin–clavulanic acid, cefotaxime, ceftriaxone, ceftazidime, cefepime, ciprofloxacin, ofloxacin, piperacillin, piperacillin–tazobactam
John, 2011 [44]	Asia	India	A. baumannii (242)	36/36 (100) ciprofloxacin, piperacillin, gentamicin, ceftazidime0/36 (0) tigecycline
Kaur, 2014 [45]	Asia	India	Total (1017), A. baumannii (964), A. lwoffii (48), A. hemolyticus (5)	A. baumannii: ii313/313 (100) imipenem309/313 (98.7) ceftazidime307/313 (98.1) ciprofloxacin305/313 (97.4) cotrimoxazole304/313 (97.1) cefepime295/313 (94.2) gentamicin285/313 (91.1) piperacillin273/313 (87.2) amikacin209/313 (66.8) netilmicin 179/313 (57.2) piperacillin–tazobactam
Pandya, 2016 [48]	Asia	India	A. baumannii (81)	24/24 (100) ampicillin–sulbactam, ceftazidime, ciprofloxacin, gentamicin, ticarcillin–clavulanic acid, ceftriaxone, piperacillin
Patil, 2021 [49]	Asia	India	Total (188), A. baumannii (156), A. lwoffii (15), A. calcoaceticus (9), A. hemotyticus (5), A. baumannii–calcoaceticus complex (3)	164/164 (100) piperacillin, piperacillin–tazobactam, ciprofloxacin, ceftazidime, cefepime, imipenem, meropenem162/164 (98.8) ceftriaxone152/164 (92.7) tetracycline147/164 (89.6) doxycycline143/164 (87.2) gentamicin137/164 (83.5) amikacin131/164 (79.9) cotrimoxazole
Singla, 2013 [52]	Asia	India	Total (70), A. baumannii (66), A. lwoffii (4)	39/39 (100) cefepime, ceftriaxone, imipenem38/39 (97.4) amoxicillin–clavulanic acid, ticarcillin–clavulanic acid37/39 (94.8) cefotaxime, ceftazidime35/39 (89.7) cotrimoxazole34/39 (87.1) gentamicin33/39 (84.6) doxycycline30/39 (76.9) amikacin, ciprofloxacin27/39 (69.2) netilmicin25/39 (64.1) piperacillin–tazobactam
Thakar, 2021 [55]	Asia	India	Acinetobacter spp. (72)	32/32 (100) ampicillin–sulbactam, carbapenem, third and fourth generation cephalosporins29/32 (90.6) fluoroquinolones28/32 (87.5) amikacin0/32 (0) colistin
Khaledi, 2019 [61]	Asia	Iran	A. baumannii (100)	65/65 (100) imipenem, meropenem
Owlia, 2012 [66]	Asia	Iran	A. baumannii (126)	42/42 (100) cefotaxime, ceftazidime, piperacillin–tazobactam, aztreonam, ciprofloxacin, amikacin, imipenem, piperacillin, ticarcillin, ticarcillin–clavulanic acid, kanamycin 12/42 (28.6) tobramycin, gentamicin0/42 (0) colistin
Soltani, 2018 [71]	Asia	Iran	A. baumannii (92)	76/76 (100) cotrimoxazole, ciprofloxacin, imipenem, meropenem, ticarcillin–clavulanic acid, levofloxacin0/76 (0) colistin, polymyxin B
Al-Marjani, 2013 [73]	Asia	Iraq	A. baumannii (17)	7/7 (100) cefoxitin, ceftriaxone, amoxicillin–clavulanic acid, cefepime, aztreonam
Kishii, 2014 [78]	Asia	Japan	Acinetobacter spp. (123)	3/3 (100) imipenem, meropenem2/3 (66.7) levofloxacin, ciprofloxacin1/3 (33.3) amikacin
Mishra, 2012 [84]	Asia	Nepal	A. baumannii–calcoaceticuscomplex (60)	2/3 (66.7) imipenem, meropenem0/3 (0) colistin, polymyxin B
Pandey, 2021 [85]	Asia	Nepal	A. baumannii (39)	4/4 (100) imipenem0/4 (0) polymyxin B
Sakuma, 2024 [87]	Asia	Nepal	A. baumannii (66)	26/26 (100) imipenem, meropenem, ceftazidime, cefotaxime, amikacin, ciprofloxacin0/26 (0) tigecycline
Irfan, 2008 [93]	Asia	Pakistan	Acinetobacter spp. (90)	83/83 (100) imipenem

Notes: ⁱ defined as the proportion of resistant MBL-producing Acinetobacter isolates to specific antimicrobial agents among all the studied MBL-producing Acinetobacter isolates; ⁱⁱ only 313 Acinetobacter baumannii isolates were tested for antimicrobial susceptibility.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/pathogens14060557/s1, Table S1: Search strings for each resource; Table S2: “Preferred Reporting Items for Systematic Reviews and Meta-Analyses” (PRISMA) checklist for the abstract; Table S3: “Preferred Reporting Items for Systematic Reviews and Meta-Analyses” (PRISMA) checklist for the full-text review.

References

1. Oliveira, M.; Antunes, W.; Mota, S.; Madureira-Carvalho, Á.; Dinis-Oliveira, R.J.; Dias da Silva, D. An Overview of the Recent Advances in Antimicrobial Resistance. Microorganisms; 2024; 12, 1920. [DOI: https://dx.doi.org/10.3390/microorganisms12091920] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/39338594]

2. Salam, M.A.; Al-Amin, M.Y.; Salam, M.T.; Pawar, J.S.; Akhter, N.; Rabaan, A.A.; Alqumber, M.A.A. Antimicrobial Resistance: A Growing Serious Threat for Global Public Health. Healthcare; 2023; 11, 1946. [DOI: https://dx.doi.org/10.3390/healthcare11131946] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/37444780]

3. Miller, W.R.; Arias, C.A. ESKAPE pathogens: Antimicrobial resistance, epidemiology, clinical impact and therapeutics. Nat. Rev. Microbiol.; 2024; 22, pp. 598-616. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/38831030][DOI: https://dx.doi.org/10.1038/s41579-024-01054-w]

4. De Oliveira, D.M.P.; Forde, B.M.; Kidd, T.J.; Harris, P.N.A.; Schembri, M.A.; Beatson, S.A.; Paterson, D.L.; Walker, M.J. Antimicrobial Resistance in ESKAPE Pathogens. Clin. Microbiol. Rev.; 2020; 33, e00181-19. [DOI: https://dx.doi.org/10.1128/CMR.00181-19]

5. Falagas, M.E.; Karveli, E.A.; Kelesidis, I.; Kelesidis, T. Community-acquired Acinetobacter infections. Eur. J. Clin. Microbiol. Infect. Dis.; 2007; 26, pp. 857-868. [DOI: https://dx.doi.org/10.1007/s10096-007-0365-6]

6. Falagas, M.E.; Rafailidis, P.I. Attributable mortality of Acinetobacter baumannii: No longer a controversial issue. Crit. Care Lond. Engl.; 2007; 11, 134. [DOI: https://dx.doi.org/10.1186/cc5911] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/17543135]

7. Lemos, E.V.; de la Hoz, F.P.; Einarson, T.R.; McGhan, W.F.; Quevedo, E.; Castañeda, C.; Kawai, K. Carbapenem resistance and mortality in patients with Acinetobacter baumannii infection: Systematic review and meta-analysis. Clin. Microbiol. Infect. Infect. Dis.; 2014; 20, pp. 416-423. [DOI: https://dx.doi.org/10.1111/1469-0691.12363]

8. World Health Organization. WHO Bacterial Priority Pathogens List, 2024: Bacterial Pathogens of Public Health Importance, to Guide Research, Development and Strategies to Prevent and Control Antimicrobial Resistance; World Health Organization: Geneva, Switzerland, 2024; Available online: https://iris.who.int/handle/10665/376776 (accessed on 6 February 2025).

9. Wong, D.; Nielsen, T.B.; Bonomo, R.A.; Pantapalangkoor, P.; Luna, B.; Spellberg, B. Clinical and Pathophysiological Overview of Acinetobacter Infections: A Century of Challenges. Clin. Microbiol. Rev.; 2017; 30, pp. 409-447. [DOI: https://dx.doi.org/10.1128/CMR.00058-16]

10. Ambler, R.P.; Baddiley, J.; Abraham, E.P. The structure of β-lactamases. Philos. Trans. R. Soc. Lond. B Biol. Sci.; 1997; 289, pp. 321-331. [DOI: https://dx.doi.org/10.1098/rstb.1980.0049]

11. Bush, K. Past and Present Perspectives on β-Lactamases. Antimicrob. Agents Chemother.; 2018; 62, e01076-18. [DOI: https://dx.doi.org/10.1128/AAC.01076-18]

12. Nagshetty, K.; Shilpa, B.M.; Patil, S.A.; Shivannavar, C.T.; Manjula, N.G. An Overview of Extended Spectrum Beta Lactamases and Metallo Beta Lactamases. Adv. Microbiol.; 2021; 11, pp. 37-62. [DOI: https://dx.doi.org/10.4236/aim.2021.111004]

13. Samaha-Kfoury, J.N.; Araj, G.F. Recent developments in β lactamases and extended spectrum β lactamases. BMJ; 2003; 327, pp. 1209-1213. [DOI: https://dx.doi.org/10.1136/bmj.327.7425.1209]

14. Franklin, C.; Liolios, L.; Peleg, A.Y. Phenotypic Detection of Carbapenem-Susceptible Metallo-β-Lactamase-Producing Gram-Negative Bacilli in the Clinical Laboratory. J. Clin. Microbiol.; 2006; 44, pp. 3139-3144. [DOI: https://dx.doi.org/10.1128/JCM.00879-06] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/16954239]

15. Bebrone, C. Metallo-beta-lactamases (classification, activity, genetic organization, structure, zinc coordination) and their superfamily. Biochem. Pharmacol.; 2007; 74, pp. 1686-1701. [DOI: https://dx.doi.org/10.1016/j.bcp.2007.05.021] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/17597585]

16. Palzkill, T. Metallo-β-lactamase structure and function. Ann. N. Y. Acad. Sci.; 2013; 1277, pp. 91-104. [DOI: https://dx.doi.org/10.1111/j.1749-6632.2012.06796.x]

17. Yu, H.; Ezpeleta-Lobato, G.; Han, X.; Carmona-Cartaya, Y.; Quiñones-Pérez, D. Carbapenamase-Producing Acinetobacter baumannii in China, Latin America and the Caribbean. MEDICC Rev.; 2022; 24, pp. 59-69. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/35157640][DOI: https://dx.doi.org/10.37757/MR2022.V24.N1.8]

18. Kindu, M.; Derseh, L.; Gelaw, B.; Moges, F. Carbapenemase-Producing Non-Glucose-Fermenting Gram-Negative Bacilli in Africa, Pseudomonas aeruginosa and Acinetobacter baumannii: A Systematic Review and Meta-Analysis. Int. J. Microbiol.; 2020; 2020, 9461901. [DOI: https://dx.doi.org/10.1155/2020/9461901]

19. Hsu, L.-Y.; Apisarnthanarak, A.; Khan, E.; Suwantarat, N.; Ghafur, A.; Tambyah, P.A. Carbapenem-Resistant Acinetobacter baumannii and Enterobacteriaceae in South and Southeast Asia. Clin. Microbiol. Rev.; 2017; 30, pp. 1-22. [DOI: https://dx.doi.org/10.1128/CMR.00042-16]

20. Djahmi, N.; Dunyach-Remy, C.; Pantel, A.; Dekhil, M.; Sotto, A.; Lavigne, J.-P. Epidemiology of carbapenemase-producing Enterobacteriaceae and Acinetobacter baumannii in Mediterranean countries. BioMed Res. Int.; 2014; 2014, 305784. [DOI: https://dx.doi.org/10.1155/2014/305784]

21. Hajikhani, B.; Sameni, F.; Ghazanfari, K.; Abdolali, B.; Yazdanparast, A.; Asarehzadegan Dezfuli, A.; Nasiri, M.J.; Goudarzi, M.; Dadashi, M. Prevalence of blaNDM-producing Acinetobacter baumannii strains isolated from clinical samples around the world; a systematic review. Gene Rep.; 2023; 30, 101728. [DOI: https://dx.doi.org/10.1016/j.genrep.2022.101728]

22. Vardakas, K.Z.; Mavroudis, A.D.; Georgiou, M.; Falagas, M.E. Intravenous colistin combination antimicrobial treatment vs. monotherapy: A systematic review and meta-analysis. Int. J. Antimicrob. Agents; 2018; 51, pp. 535-547. [DOI: https://dx.doi.org/10.1016/j.ijantimicag.2017.12.020] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/29288723]

23. Kwa, A.L.; Falagas, M.E.; Michalopoulos, A.; Tam, V.H. Benefits of aerosolized colistin for ventilator-associated pneumonia: Absence of proof versus proof of absence?. Clin. Infect. Dis. Off. Publ. Infect. Dis. Soc. Am.; 2011; 52, pp. 1278–1279; author reply 1279–1280. [DOI: https://dx.doi.org/10.1093/cid/cir134] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/21507926]

24. Falagas, M.E.; Kyriakidou, M.; Voulgaris, G.L.; Vokos, F.; Politi, S.; Kechagias, K.S. Clinical use of intravenous polymyxin B for the treatment of patients with multidrug-resistant Gram-negative bacterial infections: An evaluation of the current evidence. J. Glob. Antimicrob. Resist.; 2021; 24, pp. 342-359. [DOI: https://dx.doi.org/10.1016/j.jgar.2020.12.026]

25. Falagas, M.E.; Vardakas, K.Z.; Tsiveriotis, K.P.; Triarides, N.A.; Tansarli, G.S. Effectiveness and safety of high-dose tigecycline-containing regimens for the treatment of severe bacterial infections. Int. J. Antimicrob. Agents; 2014; 44, pp. 1-7. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/24602499][DOI: https://dx.doi.org/10.1016/j.ijantimicag.2014.01.006]

26. Katsarou, A.; Stathopoulos, P.; Tzvetanova, I.D.; Asimotou, C.-M.; Falagas, M.E. β-Lactam/β-Lactamase Inhibitor Combination Antibiotics Under Development. Pathogens; 2025; 14, 168. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/40005543][DOI: https://dx.doi.org/10.3390/pathogens14020168]

27. Yong, D.; Lee, K.; Yum, J.H.; Shin, H.B.; Rossolini, G.M.; Chong, Y. Imipenem-EDTA Disk Method for Differentiation of Metallo-β-Lactamase-Producing Clinical Isolates of Pseudomonas spp. and Acinetobacter spp. J. Clin. Microbiol.; 2002; 40, pp. 3798-3801. [DOI: https://dx.doi.org/10.1128/JCM.40.10.3798-3801.2002]

28. Lee, K.; Chong, Y.; Shin, H.B.; Kim, Y.A.; Yong, D.; Yum, J.H. Modified Hodge and EDTA-disk synergy tests to screen metallo-β-lactamase-producing strains of Pseudomonas and Acinetobactet species. Clin. Microbiol. Infect.; 2001; 7, pp. 88-91. [DOI: https://dx.doi.org/10.1046/j.1469-0691.2001.00204.x] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/11298149]

29. Shivaprasad, A.; Antony, B.; Shenoy, P. Comparative Evaluation of Four Phenotypic Tests for Detection of Metallo-β-Lactamase and Carbapenemase Production in Acinetobacter baumannii. J. Clin. Diagn. Res. JCDR; 2014; 8, pp. DC05-DC08. [DOI: https://dx.doi.org/10.7860/JCDR/2014/6447.4317]

30. Behera, B.; Mathur, P.; Das, A.; Kapil, A.; Sharma, V. An evaluation of four different phenotypic techniques for detection of metallo-beta-lactamase producing Pseudomonas aeruginosa. Indian J. Med. Microbiol.; 2008; 26, pp. 233-237. [DOI: https://dx.doi.org/10.1016/S0255-0857(21)01868-5]

31. Rakhi, N.N.; Alam, A.S.M.R.U.; Sultana, M.; Rahaman, M.M.; Hossain, M.A. Diversity of carbapenemases in clinical isolates: The emergence of blaVIM-5 in Bangladesh. J. Infect. Chemother.; 2019; 25, pp. 444-451. [DOI: https://dx.doi.org/10.1016/j.jiac.2019.01.010]

32. Li, Y.J.; Pan, C.Z.; Zhao, Z.W.; Zhao, Z.X.; Chen, H.L.; Lu, W.B. Effects of a combination of amlodipine and imipenem on 42 clinical isolates of Acinetobacter baumannii obtained from a teaching hospital in Guangzhou, China. BMC Infect. Dis.; 2013; 13, 548. [DOI: https://dx.doi.org/10.1186/1471-2334-13-548] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/24238357]

33. Ahir, H.R.; Patel, P.H.; Berry, R.A.; Parmar, R.; Soni, S.T.; Shah, P.K.; Vegad, M.M.; Patil, S. Prevalence of metallo-β-lactamases producing Pseudomonas and Acinetobacter species in tertiary care teaching hospital, Gujarat. Int. J. Microbiol. Res.; 2012; 4, pp. 322-325. [DOI: https://dx.doi.org/10.9735/0975-5276.4.9.322-325]

34. Archana Rao, K.; Aradita, C.; Lakshminarayana, S. Detection of metallo-beta-lactamase (MBL) producing Pseudomonas aeruginosa and Acinetobacter spp. from a Tertiary Care Hospital. J. Res. Appl. Basic Med Sci.; 2024; 10, pp. 72-79. [DOI: https://dx.doi.org/10.61186/rabms.10.1.72]

35. Banerjee Molay, C.B.L. Prevalence of ESBL and MBL in Acinetobacter Species Isolated from Clinical Samples in Tertiary Care Hospital. Int. J. Sci. Res. IJSR; 2015; 4, pp. 1183-1186.

36. Binnani, A.; Bishnoi, B.R.; Meena, S.; Singh, D. Study of Prevalence and Antimicrobial Susceptibility Pattern of Matello-Beta-Lactamase Producing Acinetobacter spp. Isolated at a Tertiary Care Institute in North West Region of Rajasthan. Int. J. Curr. Microbiol. Appl. Sci.; 2018; 7, pp. 2521-2526. [DOI: https://dx.doi.org/10.20546/ijcmas.2018.709.313]

37. De, A.S.; Kumar, S.H.; Baveja, S.M. Prevalence of metallo-β-lactamase producing Pseudomonas aeruginosa and Acinetobacter species in intensive care areas in a tertiary care hospital. Indian J. Crit. Care Med. Peer-Rev. Off. Publ. Indian Soc. Crit. Care Med.; 2010; 14, pp. 217-219. [DOI: https://dx.doi.org/10.4103/0972-5229.76089]

38. Gautam, D.; Dolma, K.G.; Khandelwal, B.; Goyal, R.K.; Mitsuwan, W.; Pereira, M.d.L.G.; Klangbud, W.K.; Gupta, M.; Wilairatana, P.; Siyadatpanah, A. . Acinetobacter baumannii in suspected bacterial infections: Association between multidrug resistance, virulence genes, & biofilm production. Indian J. Med. Res.; 2023; 158, 439. [DOI: https://dx.doi.org/10.4103/ijmr.ijmr_3470_21] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/38006347]

39. Girija, S.A.; Jayaseelan, V.P.; Arumugam, P. Prevalence of VIM- and GIM-producing Acinetobacter baumannii from patients with severe urinary tract infection. Acta Microbiol. Immunol. Hung.; 2018; 65, pp. 539-550. [DOI: https://dx.doi.org/10.1556/030.65.2018.038]

40. Goel, N.; Punia, P.; Chaudhary, U. Prevalence of ESBL, MBL and Amp C producing XDR Acinetobacter isolates from lower respiratory tract specimens. Int. J. Contemp. Med. Res.; 2017; 4, pp. 2091-2095.

41. Hodiwala, A.; Dhoke, R.; Urhekar, A. Incidence of metallo-betalactamase producing pseudomonas, acinetobacter & enterobacterial isolates in hospitalised patients. Int. J. Pharamcy Biol. Sci.; 2013; 3, pp. 79-83.

42. Jena, J.; Sahoo, R.K.; Subudhi, E.; Debata, N. Prevalence of ESBL, MBL and Ampc-b-lactamases producing multidrug resistance gram negative bacteria in a tertiary care hospital. J. Pure Appl. Microbiol.; 2014; 8, pp. 4099-4105.

43. Jethwa, D.K.; Vegad, M. Phenotypic Detection & Prevalence of Metallo-β-lactamases in Acinetobacter spp. in Clinical Isolates at Tertiary Care Hospital. Med. Sci.; 2013; 2, pp. 270-271.

44. John, S.; Balagurunathan, R. Metallo beta lactamase producing Pseudomonas aeruginosa and Acinetobacter baumannii. Indian J. Med. Microbiol.; 2011; 29, pp. 302-304. [DOI: https://dx.doi.org/10.4103/0255-0857.83918]

45. Kaur, A.; Gupta, V.; Chhina, D. Prevalence of metalo- β-lactamase-producing (MBL) Acinetobacter species in a tertiary care hospital. Iran. J. Microbiol.; 2014; 6, pp. 22-25. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/25954487]

46. Kaur, A.; Singh, S. Prevalence of Extended Spectrum Betalactamase (ESBL) and Metallobetalactamase (MBL) Producing Pseudomonas aeruginosa and Acinetobacter baumannii Isolated from Various Clinical Samples. J. Pathog.; 2018; 2018, 6845985. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/30473888][DOI: https://dx.doi.org/10.1155/2018/6845985]

47. Kumar, E.; Usha, K.; Ramana, B.; Chaudhury, A.; GOPAL, D. Prevalence of various β-lactamase (ESBL, AmpC and MBL) producing multidrug-resistant clinical isolates of Acinetobacter spp. in a tertiary care hospital. Asian J. Pharm. Clin. Res.; 2013; 6, pp. 28-31.

48. Pandya, Y.; Singh, S.; Badodariya, D.; Shethwala, N. Metallo-β-Lactamase Producing Clinical Isolates Of Acinetobacter Baumannii And Pseudomonas Aeruginosa In A Teaching Hospital Of Rural Gujarat-India.: Metallo-β-Lactamase Producing Clinical Isolates Of Acinetobacter Baumannii And Pseudomonas Aeruginosa. Natl. J. Integr. Res. Med.; 2016; 7, pp. 29-33.

49. Patil, H.V.; Mohite, S.T.; Patil, V.C. Metallo-beta-lactamase-producing multidrug-resistant acinetobacter isolates in patients with ventilator-associated pneumonia. J. Nat. Sci. Biol. Med.; 2021; 12, 64. [DOI: https://dx.doi.org/10.4103/jnsbm.JNSBM_54_20]

50. Rynga, D.; Shariff, M.; Deb, M. Phenotypic and molecular characterization of clinical isolates of Acinetobacter baumannii isolated from Delhi, India. Ann. Clin. Microbiol. Antimicrob.; 2015; 14, 40. [DOI: https://dx.doi.org/10.1186/s12941-015-0101-5]

51. Saikia, S.; Gogoi, I.; Oloo, A.; Sharma, M.; Puzari, M.; Chetia, P. Co-production of metallo-β-lactamase and OXA-type β-lactamases in carbapenem-resistant Acinetobacter baumannii clinical isolates in North East India. World J. Microbiol. Biotechnol.; 2024; 40, 167. [DOI: https://dx.doi.org/10.1007/s11274-024-03977-1]

52. Singla, P.; Sikka, R.; Deep, A.; Chaudhary, U. Phenotypic detection and prevalence of metallo β-lactamases (MBLs) in carbapenem resistant isolates of acinetobacter species at a tertiary care hospital in north India. Int. J. Pharm. Med. Bio Sci.; 2013; 2, pp. 85-91.

53. Sinha, N.; Agarwal, J.; Srivastava, S.; Singh, M. Analysis of carbapenem-resistant Acinetobacter from a tertiary care setting in North India. Indian J. Med. Microbiol.; 2013; 31, pp. 60-63. [DOI: https://dx.doi.org/10.4103/0255-0857.108724] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/23508431]

54. Sugumaran, S.; Devi, S.U. Prevalence of Metallo-Beta-Lactamase Producers among Non-Fermenting Gram Negative Bacilli. IOSR J. Dent. Med. Sci.; 2019; 18, pp. 32-41. [DOI: https://dx.doi.org/10.9790/0853-1810133241]

55. Thakar, V.H.; Chakraborthy, A.; Modak, M.; Krunal, L. Detection of Metallo-β-lactamase production amongst Acinetobacter species from a tertiary care hospital. J. Acad. Clin. Microbiol.; 2021; 23, pp. 63-68. [DOI: https://dx.doi.org/10.4103/jacm.jacm_64_21]

56. Tripathi, P.; Gajbhiye, S. Prevalence of multidrug resistance, ESBL and MBL production in Acinetobacter spp. Int. J. Recent. Trends Sci. Technol.; 2013; 6, pp. 139-143.

57. Uma Karthika, R.; Srinivasa Rao, R.; Sahoo, S.; Shashikala, P.; Kanungo, R.; Jayachandran, S.; Prashanth, K. Phenotypic and genotypic assays for detecting the prevalence of metallo-beta-lactamases in clinical isolates of Acinetobacter baumannii from a South Indian tertiary care hospital. J. Med. Microbiol.; 2009; 58, pp. 430-435. [DOI: https://dx.doi.org/10.1099/jmm.0.002105-0]

58. Vamsi, K.S.; Moorthy, S.R.; Murali, T.; Hemiliamma, M.; Reddy, Y.; Reddy, B.; Kumar, J.S. Phenotypic Methods for the Detection of Metallo-Beta-Lactamase Production by Gram-negative Bacterial Isolates from Hospitalized Patients in A Tertiary Care Hospital in India. J. Pure Appl. Microbiol.; 2021; 15, pp. 2019-2026. [DOI: https://dx.doi.org/10.22207/JPAM.15.4.23]

59. Aghamiri, S.; Amirmozafari, N.; Fallah Mehrabadi, J.; Fouladtan, B.; Hanafi Abdar, M. Antibiotic resistance patterns and a survey of metallo-β-lactamase genes including bla-IMP and bla-VIM types in Acinetobacter baumannii isolated from hospital patients in Tehran. Chemotherapy; 2016; 61, pp. 275-280. [DOI: https://dx.doi.org/10.1159/000443825] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/27058056]

60. Jahantigh, M.; Javadi, R.; Bameri, Z.; Dehvari, A. Evaluation of Antibiotic Susceptibility, Carbapenemase and Metallobetalactamase-producing Strains of Acinetobacter baumannii Isolated from Hospitalized Patients in Zahedan During 2019–2022. Int. J. Infect.; 2024; 10, e143968. [DOI: https://dx.doi.org/10.5812/iji-143968]

61. Khaledi, M.; Shahini Shams Abadi, M.; Validi, M.; Zamanzad, B.; Vafapour, R.; Gholipour, A. Phenotypic and genotypic detection of metallo-β-lactamases in A. baumanii isolates obtained from clinical samples in Shahrekord, southwest Iran. BMC Res. Notes; 2019; 12, 597. [DOI: https://dx.doi.org/10.1186/s13104-019-4636-y]

62. Maspi, H.; Mahmoodzadeh Hosseini, H.; Amin, M.; Imani Fooladi, A.A. High prevalence of extensively drug-resistant and metallo beta-lactamase-producing clinical Acinetobacter baumannii in Iran. Microb. Pathog.; 2016; 98, pp. 155-159. [DOI: https://dx.doi.org/10.1016/j.micpath.2016.07.011]

63. Moghadam, M.; Motamedifar, M.; Sarvari, J.; Ebrahim-Saraie, H.S.; Same, M.M.; Moghadam, F. Emergence of multidrug resistance and metallo-beta-lactamase producing Acinetobacter baumannii isolated from patients in Shiraz, Iran. Ann. Med. Health Sci. Res.; 2016; 6, pp. 162-167. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/27398247]

64. Moulana, Z.; Babazadeh, A.; Eslamdost, Z.; Shokri, M.; Ebrahimpour, S. Phenotypic and genotypic detection of metallo-beta-lactamases in Carbapenem resistant Acinetobacter baumannii. Casp. J. Intern. Med.; 2020; 11, pp. 171-176. [DOI: https://dx.doi.org/10.22088/cjim.11.2.171]

65. Noori, M.; Karimi, A.; Fallah, F.; Hashemi, A.; Alimehr, S.; Goudarzi, H.; Aghamohammad, S. High Prevalence of Metallo-beta-lactamase Producing Acinetobacter. Arch. Pediatr.; 2014; 2, e15439.

66. Owlia, P.; Azimi, L.; Gholami, A.; Asghari, B.; Lari, A.R. ESBL- and MBL-mediated resistance in Acinetobacter baumannii: A global threat to burn patients. Infez. Med.; 2012; 20, pp. 182-187. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/22992558]

67. Peymani, A.; Nahaei, M.-R.; Farajnia, S.; Hasani, A.; Mirsalehian, A.; Sohrabi, N.; Abbasi, L. High prevalence of metallo-beta-lactamase-producing acinetobacter baumannii in a teaching hospital in Tabriz, Iran. Jpn. J. Infect. Dis.; 2011; 64, pp. 69-71. [DOI: https://dx.doi.org/10.7883/yoken.64.69]

68. Ranjbar, R.; Farahani, A. Study of genetic diversity, biofilm formation, and detection of Carbapenemase, MBL, ESBL, and tetracycline resistance genes in multidrug-resistant Acinetobacter baumannii isolated from burn wound infections in Iran. Antimicrob. Resist. Infect. Control; 2019; 8, 172. [DOI: https://dx.doi.org/10.1186/s13756-019-0612-5]

69. Rezaei, A.; Fazeli, H.; Halaji, M.; Moghadampour, M.; Faghri, J. Prevalence of metallo-beta-lactamase producing Acinetobacter baumannii isolated from intensive care unit in tertiary care hospitals. Ann. Ig. Med. Prev. E Comunita; 2018; 30, pp. 330-336. [DOI: https://dx.doi.org/10.7416/ai.2018.2224]

70. Safari, M.; Saidijam, M.; Bahador, A.; Jafari, R.; Alikhani, M.Y. High prevalence of multidrug resistance and metallo-beta-lactamase (MbetaL) producing Acinetobacter baumannii isolated from patients in ICU wards, Hamadan, Iran. J. Res. Health Sci.; 2013; 3, pp. 162-167.

71. Soltani, B.; Heidari, H.; Ebrahim-Saraie, H.S.; 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. Riv. Period. Eziologia Epidemiol. Diagn. Clin. E Ter. Patol. Infett.; 2018; 26, pp. 67-76.

72. Vala, M.H.; Hallajzadeh, M.; Hashemi, A.; Goudarzi, H.; Tarhani, M.; Tabrizi, M.S.; Bazmi, F. 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.

73. Al Marjani, M.; Al-Ammar, M.; Kadhem, E. Occurrence of ESBL and MBL genes in Pseudomonas aeruginosa and Acinetobacter baumannii isolated from Baghdad, Iraq. Int. J. Curr. Res.; 2013; 5, pp. 2482-2486.

74. Anoar, K.A.; Ali, F.A.; Omer, S.A. Detection of metallo beta-lactamase enzyme in some gram negative bacteria isolated from burn patients in sulaimani city, Iraq. Eur. Sci. J.; 2014; 10, pp. 485-496.

75. Numan, S.; Al-Saedi, F.; Burhan, I. Prevalence of Extended Spectrum Betalactamase and Metallobetalactamase Producing Acinetobacter baumannii Isolated from Different Infections in Baghdad City of Iraq. Int. J. Drug Deliv. Technol.; 2022; 12, pp. 1742-1747. [DOI: https://dx.doi.org/10.25258/ijddt.12.4.41]

76. Radhi, S.H.; Al-Charrakh, A.H. Occurrence of MBLs and Carbapenemases among MDR and XDR Acinetobacter baumannii Isolated from Hospitals in Iraq. Indian J. Public Health Res. Dev.; 2019; 10, 668. [DOI: https://dx.doi.org/10.5958/0976-5506.2019.01651.6]

77. Smail, S.B.; Al-Otrachi, K.I. Phenotypic Characterization of Extended-Spectrum Beta-Lactamases and Metallo-Beta-Lactamase of Multi Drug Resistant Acinetobacter baumannii Causing Nosocomial Infections in Erbil City. Al-Mustansiriyah J. Sci.; 2019; 30, pp. 51-56. [DOI: https://dx.doi.org/10.23851/mjs.v30i4.671]

78. Kishii, K.; Kikuchi, K.; Yoshida, A.; Okuzumi, K.; Uetera, Y.; Yasuhara, H.; Moriya, K. Antimicrobial susceptibility profile of Acinetobacter species isolated from blood cultures in two Japanese university hospitals. Microbiol. Immunol.; 2014; 58, pp. 142-146. [DOI: https://dx.doi.org/10.1111/1348-0421.12117]

79. Yamamoto, M.; Nagao, M.; Matsumura, Y.; Hotta, G.; Matsushima, A.; Ito, Y.; Takakura, S.; Ichiyama, S. Regional dissemination of Acinetobacter species harbouring metallo-β-lactamase genes in Japan. Clin. Microbiol. Infect. Infect. Dis.; 2013; 19, pp. 729-736. [DOI: https://dx.doi.org/10.1111/1469-0691.12013] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/23009350]

80. Hajjar Soudeiha, M.; Dahdouh, E.; Daoud, Z.; Sarkis, D.K. Phenotypic and genotypic detection of β-lactamases in Acinetobacter spp. isolates recovered from Lebanese patients over a 1-year period. J. Glob. Antimicrob. Resist.; 2018; 12, pp. 107-112. [DOI: https://dx.doi.org/10.1016/j.jgar.2017.09.016]

81. Maziz, M.N.H.; Chakravarthi, S. ESBL and MBL detection in clinical isolates of Acinetobacter species. MAHSA Int. J. Health Med.; 2021; 1, pp. 21-28.

82. Koirala, A.; Agrahari, G.; Dahal, N.; Ghimire, P. ESBL and MBL mediated resistance in clinical isolates of nonfermentating Gram negative bacilli (NFGNB) in Nepal. J. Microb. Antimicrob. Agents; 2017; 3, pp. 18-24.

83. Kumari, M.; Bhattarai, N.R.; Rai, K.; Pandit, T.K.; Khanal, B. Multidrug-Resistant Acinetobacter: Detection of ESBL, MBL, blaNDM-1 Genotype, and Biofilm Formation at a Tertiary Care Hospital in Eastern Nepal. Int. J. Microbiol.; 2022; 2022, 8168000. [DOI: https://dx.doi.org/10.1155/2022/8168000] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/36536809]

84. Mishra, S.K.; Acharya, J.; Kattel, H.P.; Koirala, J.; Rijal, B.P.; Pokhrel, B.M. Metallo-beta-lactamase producing gram-negative bacterial isolates. J. Nepal Health Res. Counc.; 2012; 10, pp. 208-213. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/23281453]

85. Pandey, R.; Mishra, S.K.; Shrestha, A. Characterisation of ESKAPE Pathogens with Special Reference to Multidrug Resistance and Biofilm Production in a Nepalese Hospital. Infect. Drug Resist.; 2021; 14, pp. 2201-2212. [DOI: https://dx.doi.org/10.2147/IDR.S306688]

86. Pathak, P.; Jaishi, N.; Yadav, B.K.; Shah, P.K. Prevalence of extended spectrum beta lactamases (ESBL) and metallo beta lactamases (MBL) mediated resistance in gram negative bacterial pathogens. Tribhuvan Univ. J. Microbiol.; 2017; 4, pp. 49-54. [DOI: https://dx.doi.org/10.3126/tujm.v4i0.21677]

87. Sakuma, M.; Tohya, M.; Hishinuma, T.; Sherchand, J.B.; Kirikae, T.; Tada, T. Molecular epidemiology of multidrug-resistant Acinetobacter baumannii isolates from a hospital in Nepal. J. Glob. Antimicrob. Resist.; 2024; 38, pp. 363-367. [DOI: https://dx.doi.org/10.1016/j.jgar.2024.07.017]

88. Shrestha, S.; Tada, T.; Shrestha, B.; Ohara, H.; Kirikae, T.; Rijal, B.; Pokhrel, B.; Sherchand, J. Phenotypic characterization of multidrug-resistant Acinetobacter baumannii with special reference to metallo-β-lactamase production from the hospitalized patients in a tertiary care hospital in Nepal. J. Inst. Med. Nepal; 2015; 37, pp. 3-10. [DOI: https://dx.doi.org/10.59779/jiomnepal.694]

89. Thapa, P.; Bhandari, D.; Shrestha, D.; Parajuli, H.; Chaudhary, P.; Amatya, J.; Amatya, R. A hospital based surveillance of metallo-beta-lactamase producing gram negative bacteria in Nepal by imipenem-EDTA disk method. BMC Res. Notes; 2017; 10, 322. [DOI: https://dx.doi.org/10.1186/s13104-017-2640-7]

90. Yadav, S.K.; Bhujel, R.; Hamal, P.; Mishra, S.K.; Sharma, S.; Sherchand, J.B. Burden of Multidrug-Resistant Acinetobacter baumannii Infection in Hospitalized Patients in a Tertiary Care Hospital of Nepal. Infect. Drug Resist.; 2020; 13, pp. 725-732. [DOI: https://dx.doi.org/10.2147/IDR.S239514]

91. Anwar, M.; Ejaz, H.; Zafar, A.; Hamid, H. Phenotypic Detection of Metallo-Beta-Lactamases in Carbapenem Resistant Acinetobacter baumannii Isolated from Pediatric Patients in Pakistan. J. Pathog.; 2016; 2016, 8603964. [DOI: https://dx.doi.org/10.1155/2016/8603964]

92. Hasan, B.; Perveen, K.; Olsen, B.; Zahra, R. Emergence of carbapenem-resistant Acinetobacter baumannii in hospitals in Pakistan. J. Med. Microbiol.; 2014; 63, pp. 50-55. [DOI: https://dx.doi.org/10.1099/jmm.0.063925-0] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/24085817]

93. Irfan, S.; Zafar, A.; Guhar, D.; Ahsan, T.; Hasan, R. Metallo-β-Lactamase-Producing Clinical Isolates Of Acinetobacter Species And Pseudomonas Aeruginosa From Intensive Care Unit Patients Of A Tertiary Care Hospital. Indian J. Med. Microbiol.; 2008; 26, pp. 243-245. [DOI: https://dx.doi.org/10.1016/S0255-0857(21)01871-5] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/18695323]

94. Rashid, F.; Masood, R.; Faiz, M. Prevalence of New Delhi metallo beta-lactamase (NDM) producing Gram-negative bacteria from different tertiary care hospitals in Lahore, Pakistan. Pak. J. Zool.; 2020; 52, 1209. [DOI: https://dx.doi.org/10.17582/journal.pjz/20190201050207]

95. Sajjad, A.; Malik, M.; Javed, I.; Mushtaq, S.; Imran, F.; Jameel, R. Detection of metallo beta lactamase production in imipenem resistant gram negative bacilli non fermenters isolated in a Tertiary Care Hospital. Prof. Med. J.; 2019; 26, pp. 2080-2084. [DOI: https://dx.doi.org/10.29309/TPMJ/2019.26.12.3073]

96. Shah, M.W.; Yasir, M.; Farman, M.; Jiman-Fatani, A.A.; Almasaudi, S.B.; Alawi, M.; El-Hossary, D.; Azhar, E.I. Antimicrobial Susceptibility and Molecular Characterization of Clinical Strains of Acinetobacter baumannii in Western Saudi Arabia. Microb. Drug Resist.; 2019; 25, pp. 1297-1305. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/31216221][DOI: https://dx.doi.org/10.1089/mdr.2019.0018]

97. Sung, J.Y.; Koo, S.H.; Kim, S.; Kwon, G.C. Emergence of Acinetobacter pittii harboring New Delhi metallo-β-lactamase genes in Daejeon, Korea. Ann. Lab. Med.; 2015; 35, 531. [DOI: https://dx.doi.org/10.3343/alm.2015.35.5.531]

98. Lee, M.-F.; Peng, C.-F.; Hsu, H.-J.; Chen, Y.-H. Molecular characterisation of the metallo-β-lactamase genes in imipenem-resistant Gram-negative bacteria from a university hospital in southern Taiwan. Int. J. Antimicrob. Agents; 2008; 32, pp. 475-480. [DOI: https://dx.doi.org/10.1016/j.ijantimicag.2008.07.009]

99. Mesli, E.; Berrazeg, M.; Drissi, M.; Bekkhoucha, S.N.; Rolain, J.-M. Prevalence of carbapenemase-encoding genes including New Delhi metallo-β-lactamase in Acinetobacter species, Algeria. Int. J. Infect. Dis.; 2013; 17, pp. e739-e743. [DOI: https://dx.doi.org/10.1016/j.ijid.2013.02.024]

100. Abd El-Glil, R. New Delhi Metallo-β-lactamase 1 (NDM-1) producing Acinetobacter baumannii in Egyptian hospitals. Int. J. Adv. Res.; 2015; 3, pp. 470-478.

101. Elbrolosy, A.M.; Labeeb, A.Z.; Hassan, D.M. New Delhi metallo-β-lactamase-producing Acinetobacter isolates among late-onset VAP patients: Multidrug-resistant pathogen and poor outcome. Infect. Drug Resist.; 2019; 12, pp. 373-384. [DOI: https://dx.doi.org/10.2147/IDR.S186924]

102. El-Din, R.A.A.; El-Bassat, H.; El-Bedewy, M.; El-Mohamady, H. Prevalence of metallo-β-lactamases producers among carbapenem-resistant Acinetobacter baumannii strains isolated from diabetic foot ulcers. Afr. J. Microbiol. Res.; 2014; 8, pp. 1580-1585. [DOI: https://dx.doi.org/10.5897/AJMR2013.6548]

103. Fattouh, M.; El-Din, A. Emergence of carbapenem-resistant Acinetobacter baumannii in the intensive care unit in Sohag University Hospital, Egypt. Int. J. Curr. Microbiol. Appl. Sci.; 2014; 3, pp. 732-744.

104. Fouad, M.; Attia, A.S.; Tawakkol, W.M.; Hashem, A.M. Emergence of carbapenem-resistant Acinetobacter baumannii harboring the OXA-23 carbapenemase in intensive care units of Egyptian hospitals. Int. J. Infect. Dis. IJID Off. Publ. Int. Soc. Infect. Dis.; 2013; 17, pp. e1252-e1254. [DOI: https://dx.doi.org/10.1016/j.ijid.2013.07.012] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/24084245]

105. Hassan, R.M.; Salem, S.T.; Hassan, S.I.M.; Hegab, A.S.; Elkholy, Y.S. Molecular characterization of carbapenem-resistant Acinetobacter baumannii clinical isolates from Egyptian patients. PLoS ONE; 2021; 16, e0251508. [DOI: https://dx.doi.org/10.1371/journal.pone.0251508]

106. Wasfi, R.; Rasslan, F.; Hassan, S.S.; Ashour, H.M.; Abd El-Rahman, O.A. Co-Existence of carbapenemase-encoding genes in Acinetobacter baumannii from cancer patients. Infect. Dis. Ther.; 2021; 10, pp. 291-305. [DOI: https://dx.doi.org/10.1007/s40121-020-00369-4]

107. Olu-Taiwo, M.A.; Opintan, J.A.; Codjoe, F.S.; Obeng Forson, A. Metallo-Beta-Lactamase-Producing Acinetobacter spp. from Clinical Isolates at a Tertiary Care Hospital in Ghana. BioMed Res. Int.; 2020; 2020, 3852419. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/33029505][DOI: https://dx.doi.org/10.1155/2020/3852419]

108. Mathlouthi, N.; El Salabi, A.A.; Ben Jomàa-Jemili, M.; Bakour, S.; Al-Bayssari, C.; Zorgani, A.A.; Kraiema, A.; Elahmer, O.; Okdah, L.; Rolain, J.-M. . Early detection of metallo-β-lactamase NDM-1- and OXA-23 carbapenemase-producing Acinetobacter baumannii in Libyan hospitals. Int. J. Antimicrob. Agents; 2016; 48, pp. 46-50. [DOI: https://dx.doi.org/10.1016/j.ijantimicag.2016.03.007]

109. Kabbaj, H.; Seffar, M.; Belefquih, B.; Akka, D.; Handor, N.; Amor, M.; Alaoui, A.E. Prevalence of metallo-β-Lactamases Producing Acinetobacter baumannii in a Moroccan Hospital. Int. Sch. Res. Not.; 2013; 2013, 154921. [DOI: https://dx.doi.org/10.5402/2013/154921]

110. Nogbou, N.-D.; Phofa, D.T.; Nchabeleng, M.; Musyoki, A.M. Investigating multi-drug resistant Acinetobacter baumannii isolates at a tertiary hospital in Pretoria, South Africa. Indian J. Med. Microbiol.; 2021; 39, pp. 218-223. [DOI: https://dx.doi.org/10.1016/j.ijmmb.2021.03.005]

111. Elbadawi, H.S.; Elhag, K.M.; Mahgoub, E.; Altayb, H.N.; Ntoumi, F.; Elton, L.; McHugh, T.D.; Tembo, J.; Ippolito, G.; Osman, A.Y. . Detection and characterization of carbapenem resistant Gram-negative bacilli isolates recovered from hospitalized patients at Soba University Hospital, Sudan. BMC Microbiol.; 2021; 21, 136. [DOI: https://dx.doi.org/10.1186/s12866-021-02133-1]

112. Kateete, D.P.; Nakanjako, R.; Namugenyi, J.; Erume, J.; Joloba, M.L.; Najjuka, C.F. Carbapenem resistant Pseudomonas aeruginosa and Acinetobacter baumannii at Mulago Hospital in Kampala, Uganda (2007–2009). SpringerPlus; 2016; 5, 1308. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/27547682][DOI: https://dx.doi.org/10.1186/s40064-016-2986-7]

113. Takemura, M.; Wise, M.G.; Hackel, M.A.; Sahm, D.F.; Yamano, Y. In vitro activity of cefiderocol against MBL-producing Gram-negative bacteria collected in North America and Europe in five consecutive annual multinational SIDERO-WT surveillance studies (2014–2019). J. Antimicrob. Chemother.; 2023; 78, pp. 2019-2027. [DOI: https://dx.doi.org/10.1093/jac/dkad200] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/37390312]

114. Hernández Gómez, C.; Blanco, V.M.; Motoa, G.; Correa, A.; Maya, J.J.; de la Cadena Vivas, E.; Perenguez, M.; Rojas, L.; Hernández, A.; Vallejo, M. . Evolución de la resistencia antimicrobiana de bacilos Gram negativos en unidades de cuidados intensivos en Colombia. Bioméd. Rev. Inst. Nac. Salud; 2014; 34, pp. 91-100. [DOI: https://dx.doi.org/10.7705/biomedica.v34i0.1667]

115. Mereuţă, A.I.; Bădescu, A.C.; Dorneanu, O.S.; Iancu, L.S.; Tuchiluş, C.G. Spread of VIM-2 metallo-beta-lactamase in Pseudomonas aeruginosa and Acinetobacter baumannii clinical isolates from Iaşi, Romania. Rev. Romana Med. Lab.; 2013; 21, pp. 423-430. [DOI: https://dx.doi.org/10.2478/rrlm-2013-0035]

116. Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E. . The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ; 2021; 372, n71. [DOI: https://dx.doi.org/10.1136/bmj.n71] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/33782057]

117. Kumari, M.; Verma, S.; Venkatesh, V.; Gupta, P.; Tripathi, P.; Agarwal, A.; Siddiqui, S.S.; Arshad, Z.; Prakash, V. Emergence of blaNDM-1 and blaVIM producing Gram-negative bacilli in ventilator-associated pneumonia at AMR Surveillance Regional Reference Laboratory in India. PLoS ONE; 2021; 16, e0256308. [DOI: https://dx.doi.org/10.1371/journal.pone.0256308] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/34495985]

118. Matuschek, E.; Ahman, J.; Webster, C.; Kahlmeter, G. Antimicrobial susceptibility testing of colistin—Evaluation of seven commercial MIC products against standard broth microdilution for Escherichia coli, Klebsiella pneumoniae, Pseudomonas aeruginosa, and Acinetobacter spp. Clin. Microbiol. Infect.; 2018; 24, pp. 865-870. [DOI: https://dx.doi.org/10.1016/j.cmi.2017.11.020]

119. Galani, I.; Rekatsina, P.D.; Hatzaki, D.; Plachouras, D.; Souli, M.; Giamarellou, H. Evaluation of different laboratory tests for the detection of metallo-β-lactamase production in Enterobacteriaceae. J. Antimicrob. Chemother.; 2008; 61, pp. 548-553. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/18222954][DOI: https://dx.doi.org/10.1093/jac/dkm535]

120. Daef, E.A.; Mohamed, I.S.; Ahmed, A.S.; Elsherbiny, N.M.; Sayed, I.M. Evaluation of different phenotypic assays for the detection of metallo-β-lactamase production in carbapenem susceptible and resistant Acinetobacter baumannii isolates. J. Am. Sci.; 2012; 8, pp. 292-299.

121. Pandya, N.P.; Nirav, P.; Pandya, S.B.P. Evaluation of various methods for detection of metallo-β-lactamase (mbl) production in gram negative bacilli. Int. J. Biol. Med. Res.; 2011; 2, pp. 775-777.

122. Magiorakos, A.-P.; Srinivasan, A.; Carey, R.B.; Carmeli, Y.; Falagas, M.E.; Giske, C.G.; Harbarth, S.; Hindler, J.F.; Kahlmeter, G.; Olsson-Liljequist, B. . 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, pp. 268-281. [DOI: https://dx.doi.org/10.1111/j.1469-0691.2011.03570.x] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/21793988]

123. Falagas, M.E.; Bliziotis, I.A.; Siempos, I.I. Attributable mortality of Acinetobacter baumannii infections in critically ill patients: A systematic review of matched cohort and case-control studies. Crit. Care Lond. Engl.; 2006; 10, R48. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/16563184][DOI: https://dx.doi.org/10.1186/cc4869]

124. Falagas, M.E.; Kopterides, P. Risk factors for the isolation of multi-drug-resistant Acinetobacter baumannii and Pseudomonas aeruginosa: A systematic review of the literature. J. Hosp. Infect.; 2006; 64, pp. 7-15. [DOI: https://dx.doi.org/10.1016/j.jhin.2006.04.015]

125. Poirel, L.; Bonnin, R.A.; Nordmann, P. Genetic basis of antibiotic resistance in pathogenic Acinetobacter species. IUBMB Life; 2011; 63, pp. 1061-1067. [DOI: https://dx.doi.org/10.1002/iub.532]

126. Jain, R.; Danziger, L.H. Multidrug-resistant Acinetobacter infections: An emerging challenge to clinicians. Ann. Pharmacother.; 2004; 38, pp. 1449-1459. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/15280512][DOI: https://dx.doi.org/10.1345/aph.1D592]

127. Karageorgopoulos, D.E.; Kelesidis, T.; Kelesidis, I.; Falagas, M.E. Tigecycline for the treatment of multidrug-resistant (including carbapenem-resistant) Acinetobacter infections: A review of the scientific evidence. J. Antimicrob. Chemother.; 2008; 62, pp. 45-55. [DOI: https://dx.doi.org/10.1093/jac/dkn165] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/18436554]

128. Poulikakos, P.; Tansarli, G.S.; Falagas, M.E. Combination antibiotic treatment versus monotherapy for multidrug-resistant, extensively drug-resistant, and pandrug-resistant Acinetobacter infections: A systematic review. Eur. J. Clin. Microbiol. Infect. Dis.; 2014; 33, pp. 1675-1685. [DOI: https://dx.doi.org/10.1007/s10096-014-2124-9] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/24832022]

129. Falagas, M.E.; Skalidis, T.; Vardakas, K.Z.; Legakis, N.J. Hellenic Cefiderocol Study Group. Activity of cefiderocol (S-649266) against carbapenem-resistant Gram-negative bacteria collected from inpatients in Greek hospitals. J. Antimicrob. Chemother.; 2017; 72, pp. 1704-1708. [DOI: https://dx.doi.org/10.1093/jac/dkx049]

130. Oliva, A.; Liguori, L.; Covino, S.; Petrucci, F.; Cogliati-Dezza, F.; Curtolo, A.; Savelloni, G.; Comi, M.; Sacco, F.; Ceccarelli, G. . Clinical effectiveness of cefiderocol for the treatment of bloodstream infections due to carbapenem-resistant Acinetobacter baumannii during the COVID-19 era: A single center, observational study. Eur. J. Clin. Microbiol. Infect. Dis.; 2024; 43, pp. 1149-1160. [DOI: https://dx.doi.org/10.1007/s10096-024-04833-8]

131. Calò, F.; Onorato, L.; De Luca, I.; Macera, M.; Monari, C.; Durante-Mangoni, E.; Massa, A.; Gentile, I.; Di Caprio, G.; Pagliano, P. . Outcome of patients with carbapenem-resistant Acinetobacter baumannii infections treated with cefiderocol: A multicenter observational study. J. Infect. Public Health; 2023; 16, pp. 1485-1491. [DOI: https://dx.doi.org/10.1016/j.jiph.2023.06.009]

132. Bassetti, M.; Echols, R.; Matsunaga, Y.; Ariyasu, M.; Doi, Y.; Ferrer, R.; Lodise, T.P.; Naas, T.; Niki, Y.; Paterson, D.L. . Efficacy and safety of cefiderocol or best available therapy for the treatment of serious infections caused by carbapenem-resistant Gram-negative bacteria (CREDIBLE-CR): A randomised, open-label, multicentre, pathogen-focused, descriptive, phase 3 trial. Lancet Infect. Dis.; 2021; 21, pp. 226-240. [DOI: https://dx.doi.org/10.1016/S1473-3099(20)30796-9] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/33058795]

133. Sargianou, M.; Stathopoulos, P.; Vrysis, C.; Tzvetanova, I.D.; Falagas, M.E. New β-Lactam/β-Lactamase Inhibitor Combination Antibiotics. Pathogens; 2025; 14, 307. [DOI: https://dx.doi.org/10.3390/pathogens14040307] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/40333039]

134. Kaye, K.S.; Shorr, A.F.; Wunderink, R.G.; Du, B.; Poirier, G.E.; Rana, K.; Miller, A.; Lewis, D.; O’Donnell, J.; Chen, L. . Efficacy and safety of sulbactam-durlobactam versus colistin for the treatment of patients with serious infections caused by Acinetobacter baumannii-calcoaceticus complex: A multicentre, randomised, active-controlled, phase 3, non-inferiority clinical trial (ATTACK). Lancet Infect. Dis.; 2023; 23, pp. 1072-1084. [DOI: https://dx.doi.org/10.1016/S1473-3099(23)00184-6] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/37182534]

135. Rafailidis, P.I.; Ioannidou, E.N.; Falagas, M.E. Ampicillin/sulbactam: Current status in severe bacterial infections. Drugs; 2007; 67, pp. 1829-1849. [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/17722953][DOI: https://dx.doi.org/10.2165/00003495-200767130-00003]