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Identification of blaOXA−51−23−58, blaVIM, blaNDM, and blaIMP carbapenemase genes in Acinetobacter baumannii isolates from hospitalized patients

BMC Research Notes volume 17, Article number: 392 (2024) Cite this article

Abstract

Objective

The increase of multidrug-resistant (MDR) strains of Acinetobacter baumannii (A. baumannii), especially carbapenem-resistant strains, is challenging for treating infections. This study investigated the antibiotic resistance pattern and frequency of carbapenem resistance genes (oxacillinase and metallo-beta-lactamase) in A. baumannii.

Results

In this study, 100 bacterial isolates were collected from clinical samples from different hospitals in Isfahan, central of Iran. Of 100 samples of bloodstream, urine, cerebrospinal fluid (CSF), wound, and trachea, 60 bacteria were identified as A. baumannii. The results showed that 100% of the selected isolates were resistant to cefotaxime, ceftazidime, ciprofloxacin, piperacillin-tazobactam, and meropenem. Based on the antibiotic resistance pattern, 25 isolates were chosen for PCR analysis targeting blaOXA−51, blaOXA−23, blaOXA−58, blaNDM, blaIMP, and blaVIM genes PCR results revealed that among the selected isolates, 15 (60.0%) harbored the blaOXA−23 gene, 23 (92.0%) contained the blaOXA−51 gene, and 1 (4.0%) isolate carried the blaNDM gene. Based on MLST analysis, two colistin-resistant Acinetobacter baumannii isolates were categorized as ST2. The ST2 clone represents the predominant sequence type within the CC2 or international clone two. The results showed that the best antibiotic against isolates was colistin. blaOXA−51 and blaOXA−23 genes (oxacillinase genes) were dominant genes, but blaIMP and blaOXA−58 were not local carbapenem resistant genes in Isfahan.

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Introduction

Acinetobacter baumannii, a Gram-negative bacterium, recognized as a formidable nosocomial pathogen, posing a substantial burden on healthcare systems globally due to its propensity for antibiotic resistance [1]. In some regions, A. baumannii accounts for a significant proportion of healthcare-associated infections, including ventilator-associated pneumonia, bloodstream infections, urinary tract infections, and surgical site infections. Its ability to persist in the hospital environment, survive on surfaces via biofilm formation, and develop resistance to multiple antibiotics contributes to its prevalence and challenges in infection control [2, 3]. Among the key contributors to A. baumannii multidrug-resistant (MDR), various oxacillinase and metallo-β-lactamases gene encoding enzymes play a crucial role [4, 5]. These enzymes confer resistance by hydrolyzing β-lactam antibiotics, such as carbapenems, rendering them ineffective in treating A. baumannii infections [6, 7].

While OXA-type β-lactamases predominantly target carbapenems, VIM-type, IMP-type, and NDM-type metallo-β-lactamases exhibit broad-spectrum activity against various β-lactam antibiotics [8, 9].

A variety of methodologies exist to enhance our understanding of the geographical distribution of Acinetobacter, including Multilocus Sequence Typing (MLST) and Random Amplification of Polymorphic DNA (RAPD) [10, 11]. MLST serves as a robust tool for investigating the global epidemiology of A. baumannii, utilizing conserved regions from seven housekeeping genes [12]. Epidemiological research on clinical isolates of Acinetobacter across the globe has revealed significant genetic diversity, with most infections attributed to specific isolates. Additionally, studies conducted in Iran indicate that the majority of identified sequence types (STs) in the country fall under clonal complex 92, which is associated with ICL-2 [13].

The presence of metallo-β-lactamase genes in A. baumannii strains highlights the urgent need for effective infection control measures, antimicrobial stewardship programs, and the development of alternative treatment strategies to combat MDR infections caused by this opportunistic pathogen. In this study, we investigated the prevalence of carbapenem resistance genes (oxacillinase and metallo-beta-lactamase), including blaOXA−23, blaOXA−51, blaOXA−58, blaVIM, blaNDM, and blaIMP, and molecular characterization of colistin resistant isolates of A. baumannii isolated from hospitalized patients from different hospitals, Isfahan, Iran.

Methods and materials

Study Design and bacterial isolation

In this study, 100 samples of urine, cerebrospinal fluid (CSF), respiratory system, bloodstream, and wound (surgery or burns) from hospitalized patients in different wards of hospitals in Isfahan (two teaching hospitals and one central private laboratory), Iran, over nine months from December 2021 to July 2022, were collected. All bacterial isolates were confirmed for A. baumannii using biochemical tests, including Gram-staining, TSI, Urease, Oxidase, SIM, MRVP, Simon citrate, ONPG, and Dnase [14].

Antibiotic susceptibility test

The antibiotic susceptibility test followed the Kirby-Bauer protocol according to the Clinical and Laboratory Standards Institute (CLSI) [15]. Administrated antibiotics were included cefepime (30 µg), ampicillin sulbactam (20 µg), cotrimoxazole (1.25/23.75 µg), amikacin (30 µg), ceftazidime (30 µg), meropenem (10 µg), gentamicin (10 µg), ciprofloxacin (5 µg), colistin (10 µg), cefotaxime (30 µg), and piperacillin tazobactam (10/100 µg) (Padtan-Teb, Iran [16](.

Minimum inhibitory concentration (MIC)

Colistin MIC was evaluated through colistin broth disk elution (CBDE) with 1, 2, and 4 µg/mL concentrations [15]. Carbapenem resistance test via MIC was conducted using Etest containing meropenem. MIC ≤ 2 µg/mL was considered intermediate resistance, and MIC ≥ 4 µg/mL was resistant. All tests were performed in triplicate to ensure reproducibility of results [15].

Phenotypic investigate of resistance to Carbapenem

Since metallo-β-lactamase enzymes are inhibited by dipicolinic acid (DPA) and EDTA, the combined disc method employed a combination test of DPA and meropenem. The zone of growth inhibition around the combined disc of meropenem and this compound was compared with the zone around the meropenem disc alone. An increase in the diameter of the inhibition zone by more than 5 mm with the combined discs compared to meropenem alone indicates the presence of metallo-β-lactamase enzymes [15].

Carbapenemase Gene identification

Genomic DNA from A. baumannii isolates was extracted using a simple boiling method, as described previously [17]. To evaluate the presence of carbapenemase genes (blaVIM, blaNDM, and blaIMP), the polymerase chain reaction (PCR) test was performed with final reaction volume of 25 µl Master Mix RED (Ampliqon, Denmark), and designed primers (Table 1S1). PCR was evaluated using the following cycling conditions: one cycle for initial denaturation at 94 °C for 10 min, followed by 36 cycles consisting of denaturation at 94 °C for 30 s, annealing at 52 °C for 40 s, and extension at 72 °C for 50 s; and finally, one cycle for the final extension at 72 °C for 5 min. The presence of blaOXA51, blaOXA−23, and blaOXA−58 genes was evaluated using the following cycling conditions: one cycle for initial denaturation at 94 °C for 5 min, followed by 30 cycles consisting of denaturation at 94 °C for 25 s, annealing at 52 °C for 40 s, and extension at 72 °C for 50 s; and finally, one cycle for the final extension at 72 °C for 6 min [7].

Table 1 Antibiotic susceptibility results for Acinetobacter Baumanni isolates
Full size table

Multilocus sequence typing (Mlst)

MLST was conducted to evaluate the two colistin-resistant isolates in accordance with the Pasteur scheme. This involved the amplification of seven housekeeping genes: fusA, gltA, pyrG, recA, cpn60, rplB, and rpoB, as detailed on the MLST website (http://pubmlst.org/abaumannii/), which provides information on PCR conditions and primers. The allelic numbers and sequence types (STs) for each strain were established by comparing their nucleotide sequences against the A. baumannii PubMLST database [13].

Genes sequencing

After the PCR test, the selected genes were sent to Pishgaman Biotech company for sequencing and were registered at the NCBI database.

Statistical analysis

Data were reported by number, percentages, and mean ± standard division (SD).

Results

Bacterial isolation and identification

Of 100 clinical samples from hospitalized patients, 60 isolates from 23 (38.4%) females and 37 (61.6%) males were diagnosed with A. baumannii, which 20 (33.3%) isolates were obtained from bloodstream, 10 (16.6%) from wounds, 7 (11.6%) from urine samples, 5 (8.3%) from tracheal samples, 4 (6.6%) from respiratory samples, 2 (3.3%) from sputum samples, and 2 (3.3%) from CSF. Additionally, 2 (3.3%) isolates were obtained from secretion samples, while one isolate from each bronchial (1.6%), pleural (1.6%), and throat (1.6%) samples were collected.

Antibiotic resistance pattern

The results of antibiotic susceptibility testing for A. baumannii isolates reveal high rates of resistance to several antibiotics. Broad-spectrum cephalosporins, including cefepime (98.3%), ceftazidime (100%), and cefotaxime (100%), exhibited resistance. Aminoglycosides, such as amikacin (96.7%) and gentamicin (95.0%), also demonstrated limited effectiveness against the isolates, with the majority showing resistance. Similarly, fluoroquinolones like ciprofloxacin exhibited complete resistance (100%). However, polymyxins, particularly colistin, showed notable efficacy, with the most sensitive isolates (96.7%). Beta-lactam combination agents, such as piperacillin-tazobactam and ampicillin-sulbactam, displayed limited effectiveness, with most isolates showing resistance (100%). Trimethoprim-sulfamethoxazole demonstrated moderate sensitivity (3.3%). Carbapenem, represented by meropenem, showed complete resistance across all isolates (100%) (Table 1).

MIC results

Among the 60 carbapenem-resistant A. baumannii strains, 2 strains (3.3%) had turbidity at a 4 µg/ml MIC that were considered resistant to colistin. No turbidity was observed for 58 strains (96/6%) at MICs of 1 µg/ml, 2 µg/ml, and 4 µg/ml. Therefore, MIC was 1 µg/ml, indicating isolates were sensitive to colistin.

Antibiotic resistant genes

Based on the antibiotic resistance pattern, 25 isolates were chosen for PCR analysis targeting blaOXA−51, blaOXA−23, blaOXA−58, blaNDM, blaIMP, and blaVIM genes. PCR results revealed that among the selected isolates, 15 (60.0%) harbored the blaOXA−23 gene, 23 (92.0%) contained the blaOXA−51 gene, and 1 (4.0%) isolate carried the blaNDM gene. Also, blaIMP,blaVIM and blaOXA−58 genes were not detected.

MLST analysis

MLST analysis of colistin-resistant isolates identified that the two isolates were assigned to ST2. Overall, using the goeBURST algorithm, STs were belonged to one CCs including CC2(ST2) (Table 2).

Table 2 Charecterization of two colistin resistant A. baumannii isolates according to MLST profile, clinical sample and antibiotic resistant pattern
Full size table

Genes sequencing

Three blaOXA−51, blaOXA−23, and blaNDM genes from five isolates after the PCR test were sequenced and were deposited in the NCBI database with the accession numbers LC723919, LC723916, LC723917, LC723918, and LC723920 (Table 2S1).

Discussion

In this study, A. baumannii strains were commonly isolated from males, wound specimens, urine, bloodstream, and respiratory secretions. Akbarpour et al. reported that among 248 isolates of A. baumannii, all were MDR and isolated from the upper respiratory tract. In contrast, the urinary tract exhibited the lowest prevalence of A. baumannii. They reported that the highest contamination rate occurred in males and patients in the ICU [18]. In another study, Gharaibeh et al. found a high prevalence of MDR A. baumannii isolates among ICU patients [19]. Furthermore, significant risk factors associated with a poor prognosis in A. baumannii bacteremia encompass underlying medical conditions, pneumonia as the source of bacteremia, surgical procedures, invasive operations, mechanical ventilation, ICU stay, and length of hospitalization.

Most studies isolated A. baumannii strains from respiratory samples [20, 21]. The prevalence of tracheal infections was higher than other respiratory samples in the current study. Similarly, Bardbari et al. reported that A. baumannii strains isolated from tracheal aspirate specimens were the most common respiratory isolates [22]. Most of the A. baumannii strains isolated from our samples were from the bloodstream.

We observed the highest resistance to broad-spectrum cephalosporins and colistin sensitivity. Colistin, or polymyxin E, is an antibiotic used as a last-line treatment for MDR Gram-negative infections, including pneumonia. Lupo et al. demonstrated that A. baumannii and Pseudomonas aeruginosa (P. aeruginosa) could both acquire multiple resistance beta-lactamases or carbapenemases [23].

Another study illustrated that all A. baumannii isolates were MDR, and minocycline and tigecycline were the most effective drugs against A. baumannii [24]. The primary cause of carbapenem resistance typically involves either a decrease in drug accumulation levels or an elevation in the expression levels of efflux pumps [25, 26]. The utilization of colistin for A. baumannii infections has resulted in the emergence of resistant bacterial strains. These strains have also acquired resistance to antimicrobial compounds naturally produced by the human immune system [27, 28]. In the current study, 60.0% harbored the blaOXA−23 gene, 92.0% contained the blaOXA−51 gene, and 4.0% isolate carried the blaNDM gene, while we did not find any isolated with blaIMP,blaVIM and blaOXA−58 genes. The blaOXA−51−like genes have been reported to be present in A. baumannii chromosomes [29].

Jiang et al. found that most carbapenemase-resistant genes blaOXA−23, blaTEM−1, and blaOXA−66 were detected the most A. baumannii every year from 2008 to 2019 [30]. Feizabadi et al. demonstrated a broad range of blaOXA genes present among A. baumannii strains in Iran and reported that identifying bla(OXA-51-like) can serve as a straightforward and dependable means to distinguish A. baumannii strains from other species [31]. Another study by Leungtongkam et al. showed that blaIMP and blaVIM genes were not found among A. baumannii isolates, while blaNDM−1 was detected in some isolates and only one isolate expressed blaOXA−23-blaOXA−58-blaNDM−1 [32]. The main contributor to carbapenem-resistant A. baumannii is regarded as carbapenemase production, particularly by OXA genes, notably blaOXA−23 [32].

The escalating resistance of clinical strains of A. baumannii to antibiotics presents a significant challenge in healthcare settings. These resilient strains, characterized by their rapid proliferation, exacerbate the complex landscape of infection treatment. Consequently, the efficacy of various antibiotic treatments is compromised, resulting in prolonged illnesses, heightened healthcare costs, and increased mortality rates. The advent of nanotechnology has led to a substantial rise in the application of nanoparticles (NPs) across diverse domains, including the management of antimicrobial resistance [33, 34].

ST2 was assigned to two colistin-resistant A. baumannii isolates based on the MLST analysis. The ST2 clone, which represents the predominant sequence type within the CC2 or international clone two, has been identified as the most widespread sequence type in several countries, including Italy, Greece, Turkey, Lebanon, and Algeria, according to data from Iran [9, 35,36,37,38,39,40].

Although various ST clones have been identified in Iran, recent studies by Piran et al., Hojabri et al., Rezaei et al., and Hajihashemi et al. indicate that the ST2 clone is currently the most prevalent. Additionally, ST2 has been widely distributed in clinical settings among Iranian patients, representing approximately 62–90% of isolates [9, 39,40,41].

Conclusion

A. baumannii isolates demonstrated high resistance to multiple antibiotics commonly used in clinical practice, including broad-spectrum cephalosporins, aminoglycosides, fluoroquinolones, and carbapenems. However, colistin showed notable efficacy against the majority of isolates. We identified the presence of carbapenemase-producing strains, particularly those harboring the blaOXA−23 gene, indicating the importance of vigilant monitoring and infection control measures to combat the spread of MDR A. baumannii infections in hospital settings.

The MLST analysis indicates colistin-resistant isolates belonged to ST2 and is endemic in Iran.

Limitations

While we comprehensively investigated the genes associated with carbapenemase genes among clinical isolates, our study had limitations in sample size and the rigorous methodology employed, which may limit the generalizability of our findings to broader populations or geographical regions.

Data availability

No datasets were generated or analysed during the current study.

Abbreviations

MDR:

Multidrug-resistant

MLST:

Multilocus Sequence Typing

RAPD:

Random Amplification of Polymorphic DNA

STs:

Sequence types

CSF:

Cerebrospinal fluid

CBDE:

Colistin broth disk elution

DPA:

Dipicolinic acid

PCR:

Polymerase chain reaction

SD:

Standard division

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Acknowledgements

We would like to thank Shahid Ashrafi Esfahani University, Isfahan, Iran.

Funding

Self-funding.

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Authors and Affiliations

  1. Department of Microbiology, Faculty of Biological Sciences and Technology Shahid Ashrafi, Shahid Ashraf Esfahani University, Isfahan, Iran

    Kosar Salmani Nasrabadi & Seyed Mahdi Ghasemi

  2. Department of Microbiology, Kish International Branch of Islamic Azad University, Kish, Iran

    Yasaman Ahmadi

  3. Nosocomial Infection Research Center, Isfahan University of Medical Sciences, Isfahan, Iran

    Dariush Shokri

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  1. Kosar Salmani Nasrabadi
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Contributions

Conceived and designed the experiments: KSN, DSh, and SGh, Performed the experiments: KSN, YA and SGh, performed statistical and spatial analyses and interpreted all the results. KSN, DSh, and SGh, contributed to the writing of the manuscript and revised the final version manuscript: KSN, YA and SGh. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Dariush Shokri.

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This study was approved by the Research Ethics Committee of Babol University of Medical Sciences; Babol, Iran. However, consent to participate was waived by Research Ethics Committee of Shahid Ashrafi Esfahani University, Isfahan, Iran, due to bacteria isolated from clinical samples in the clinical microbiology laboratory routinely.

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The authors declare no competing interests.

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Nasrabadi, K.S., Ahmadi, Y., Ghasemi, S.M. et al. Identification of blaOXA−51−23−58, blaVIM, blaNDM, and blaIMP carbapenemase genes in Acinetobacter baumannii isolates from hospitalized patients. BMC Res Notes 17, 392 (2024). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s13104-024-07047-5

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  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s13104-024-07047-5

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BMC Research Notes

ISSN: 1756-0500

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