The Abundance of Plasmid-Mediated Quinolone Resistance Genes in <i>Enterobacter cloacae</i> Strains Isolated from Clinical Specimens in Kermanshah, Iran

Afsharian, Mandana; Asadi, Somayeh; Danesh, Camellia; Sedighi, Reza; Karimi, Kohsar; Miladi, Nooshin; Miladi, Ronak; Azizi, Mohsen; Madadi-Goli, Nahid; Ahmadi, Kamal; Zamanian, Mohammad Hossein

doi:https://doi.org/10.1155/2024/8849097

Canadian Journal of Infectious Diseases and Medical Microbiology

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Abstract Introduction Materials and Methods Results Discussion Conclusions Data Availability Conflicts of Interest Authors’ Contributions Acknowledgments Supplementary Materials References Copyright Related Articles

Research Article | Open Access

Volume 2024 | Article ID 8849097 | https://doi.org/10.1155/2024/8849097

The Abundance of Plasmid-Mediated Quinolone Resistance Genes in Enterobacter cloacae Strains Isolated from Clinical Specimens in Kermanshah, Iran

Mandana Afsharian,¹Somayeh Asadi,²Camellia Danesh,²Reza Sedighi,²Kohsar Karimi,³Nooshin Miladi,⁴Ronak Miladi,¹Mohsen Azizi,⁵Nahid Madadi-Goli,⁶Kamal Ahmadi,^5,6and Mohammad Hossein Zamanian¹

Academic Editor: Mohsin Khurshid

Received06 Nov 2023

Revised07 Mar 2024

Accepted23 Mar 2024

Published08 Apr 2024

Abstract

Background. Enterobacter cloacae (E. cloacae) is one of the most common Enterobacteriaceae causing nosocomial infections. Plasmid-mediated quinolone resistance (PMQR) determinants have been considered recently. This study evaluated the abundance of PMQR genes in strains of E. cloacae obtained from clinical samples in Kermanshah, Iran. Methods. In this descriptive cross-sectional study, after collecting 113 isolates of E. cloacae, their identity was confirmed using specific biochemical tests. After determining their drug resistance patterns using disc diffusion, the phenotypic frequency of extended-spectrum beta-lactamase (ESBL)-producing isolates was measured by the double-disk synergy test (DDST) method. The isolates were examined for the presence of qnrA, qnrB, qnrS, and aac(6′)-Ib-cr genes by the polymerase chain reaction (PCR) assay. Results. The antibiotic resistance rate of E. cloacae isolates varied from 9.7% to 60.2%; among them, 78% were multidrug-resistant (MDR). The highest quinolone resistance was observed in ESBL-producing strains of E. cloacae. The frequency of positive isolates for PMQR and ESBL was 79.6% and 57.5%, respectively. The genes aac(6′)-ib-cr (70.8%) and qnrB (38.1%) had the highest frequency among other genes. The number of isolates simultaneously carrying 2 and 3 genes was 64 and 5 isolates, respectively. Conclusion. The obtained results indicate a high degree of quinolone resistance among ESBL-producing E. cloacae strains. Nevertheless, there was a significant relationship between the PMQR gene and ESBL-positive isolates. Therefore, special attention should be paid to molecular epidemiological studies on antibiotic resistance to quinolones and beta-lactamases in these strains.

1. Introduction

Enterobacter is one of the causes of nosocomial infections and belongs to the family Enterobacteriaceae. It exists as saprophytes everywhere and is part of the natural flora in the human intestine [1]. E. cloacae and Enterobacter aerogenes have been identified as major nosocomial pathogens among these bacterial species. E. cloacae is responsible for over 70% of these bacterial infections [2]. Due to various virulence factors, such as biofilm-forming ability, toxins, cytotoxicity, and hemolysin release, this bacterium can lead to several nosocomial infections, including pneumonia, urinary tract infections, surgical wounds, skin and soft tissue infections, and bacteremia [3, 4]. Inappropriate antibiotic prescribing, overuse, and the underdevelopment of new antibiotics have rapidly caused antibiotic-resistant bacteria to emerge, causing nearly 700,000 deaths annually [5]. Many broad-spectrum antibiotics are used to treat bacterial infections, and their improper use has led to widespread resistance, reducing the effectiveness of these antibiotics. Recent studies have reported cases of increased drug resistance in Enterobacter strains and the emergence of multidrug-resistant (MDR) strains of this bacterium [6, 7]. Enterobacter strains are often associated with the MDR phenotype due to their ability to acquire mobile genetic factors containing resistance genes and adaptability to the hospital environment. These bacteria are intrinsically resistant to ampicillin, amoxicillin, first-generation cephalosporins, and cefoxitin due to the expression of AmpC beta-lactamase. Additionally, extended-spectrum beta-lactamase (ESBL) production in these bacteria makes them challenging to treat [8]. Quinolones and fluoroquinolones are highly applied for the treatment of various bacterial infections. Resistance to quinolones can be caused by chromosomal mutations in bacterial genes encoding quinolone target proteins, mutations that cause decreased drug accumulation due to decreased uptake or increased efflux, or plasmid-localized genes associated with quinolone resistance [9, 10]. Three classes of plasmid-mediated quinolone resistance (PMQR) genes have been identified based on their mode of action, including qnr proteins, the aac(6′)-Ib-cr genes, and efflux pump genes oqxA, oqxB, and qepA [11]. The qnr genes are one of the major PMQR factors, increasing drug resistance in bacteria due to their location on genetic factors [12]. In addition to inducing quinolone resistance, PMQR might play an important role in resistance to other antibiotics, particularly aminoglycosides and beta-lactamases [13]. Currently, seven groups of qnr genes have been identified, including qnrA, qnrB, qnrS, qnrC, qnrD, and qnrVC [14]. The qnr gene induces quinolone resistance by blocking deoxyribonucleic acid (DNA) gyrase and topoisomerase IV. Quinolone resistance is also induced by an aminoglycoside acetyltransferase called aac(6)-ib-cr, which reduces sensitivity to ciprofloxacin. Additionally, the aac(6)-ib-cr gene, besides causing aminoglycoside resistance, confers resistance to fluoroquinolones [15]. Quinolones are the most important antibiotics used in the treatment of various bacterial infections. Unfortunately, PMQR-mediated resistance has been widely reported in Enterobacteriaceae worldwide in recent decades. On the other hand, the presence of PMQR determinants can increase QRDR mutations, which increases fluoroquinolone resistance [16]. As a result, determining the frequency of PMQR genes in different species of Enterobacteriaceae can provide important information to determine the epidemiology and understand the abundance and distribution of PMQRs to prevent the irrational use of these antibiotics and the spread of drug resistance. Considering that there is no study on the frequency of PMQR genes in Enterobacter strains isolated in this province, the present study evaluated the frequency of PMQR genes in E. cloacae strains collected from patient samples in Kermanshah City, Iran.

2. Materials and Methods

2.1. Bacterial Isolates

In this cross-sectional study conducted from February 2020 to January 2021, we prepared 113 nonreplicating clinical isolates of E. cloacae from patients referred to Imam Reza Hospital in Kermanshah. Clinical samples included urine, wound, blood, trachea, sputum, cerebrospinal fluid (CSF), bronchoalveolar lavage (BAL), and catheter specimens. This study focused exclusively on E. cloacae isolates from the clinical samples of hospitalized patients, excluding other Enterobacter species and environmental samples. The present research was approved by the Ethics Committee of Kermanshah University of Medical Sciences (No. IR.KUMS.REC.1399.754), and informed consent was obtained from all patients. Initially, the collected specimens were cultured on eosin methylene blue agar (EMB) and McConkey agar (Merck, Germany) under sterile conditions. Subsequently, specific tests, including culture in IMVIC and triple sugar iron (TSI) agar medium, Simmons citrate agar (HiMedia Co., India), and indole test, were employed to identify E. cloacae. The E. cloacae samples identified in tryptic soy broth (TSB) were then preserved with 15% glycerol at −70°C.

2.2. Antimicrobial Susceptibility Assessment

Antibiotic sensitivity testing of the isolates was conducted following Clinical and Laboratory Standards Institute (CLSI) guidelines, using 17 antibiotic discs (MAST, UK) that included ciprofloxacin (5 μg), nalidixic acid (30 μg), norfloxacin (10 μg), gatifloxacin (5 μg), levofloxacin (5 μg), ceftazidime (30 μg), ofloxacin (5 μg), cefotaxime (30 μg), aztreonam (30 μg), ceftriaxone (30 μg), imipenem (10 μg), nitrofurantoin (30 μg), colistin (10 μg), chloramphenicol (10 μg), gentamicin (10 μg), tobramycin (10 μg), and amikacin (30 μg). The Kirby–Bauer method was used for this test, with the standard concentration of McFarland 0.5 (1.5 × 10⁸) of bacteria applied for antimicrobial sensitivity testing. Escherichia coli strain ATCC 25922 served as a control for the antibiogram test, and isolates resistant to three or more types of antibiotics were classified as MDR E. cloacae strains.

2.3. Extended-Spectrum Beta-Lactamases Detection

The isolates characterized by minimum inhibition zone diameters of 22, 25, and 27 mm for ceftazidime, ceftriaxone, and cefotaxime, respectively, were evaluated for ESBL genes. To confirm ESBL production, the combined disk (CD) approach was used, employing 30 μg ceftazidime and cefotaxime disks impregnated with 10 μg clavulanic acid (MAST, UK) on Mueller–Hinton agar (HiMedia Co., India), following the disk diffusion method. After 24 hours of incubation at 37°C, strains with a minimum inhibition zone diameter of ≥5 mm compared to a single disc of the same antibiotic were considered ESBL producers.

2.4. Detection of PMQR Genes

The isolates’ genomes were extracted through boiling, and the frequency of the target genes (Supplementary file (available here)) was determined using their specific primers (Tekapo Biot Company, Iran) via polymerase chain reaction (PCR) [12, 17]. The level of extracted DNA specimens was measured at 260 nm using a Nanodrop Synergy HTX (BioTek Instrument, Inc. USA), resulting in a concentration of 34 pmol/uL. The purity of the DNA extracted at 280/260 nm wavelength was 1.82. The PCR reaction, with a volume of 25 μL, included Master Mix (12.5 μL) (Sinocloon Company, Iran), 1 μL of primer, bacterial DNA (2 μL), and sterilized distilled water up to 25 μL. The PCR procedure comprised initial denaturation (94°C/5 min), 35 basic cycles, and extension (10 min/72°C). In this study, in addition to using E. coli J53 strains containing pMG252, pMG298, and pMG306 as positive controls for qnrA, qnrB, and qnrS genes, respectively, we also used isolates carrying quinolone resistance genes from a previous study. The final products were detected through electrophoresis on 1% agarose gel (70 V, 1 h) with ethidium bromide (0.5 μg/mL) in the Tris-EDTA buffer. An ultraviolet illuminator (ProteinSimple, USA) was employed to observe the gel, with distilled water serving as a negative control for each PCR.

2.5. Statistical Analysis

The data were analyzed using SPSS software (version 20) with the chi-square and Fisher’s exact tests. A value less than 0.05 was considered significant.

3. Results

A total of 113 clinical strains of E. cloacae were collected from 113 patients, including 47 (41.6%) male and 66 (58.4%) female subjects, with a mean age of 36.42 ± 11.59 years, ranging from 16 to 72 years. These strains were obtained from patients at Imam Reza Hospital in Kermanshah, Iran. The highest and lowest frequencies of E. cloacae isolates were found in urine samples (43 : 38.1%) and BAL samples (5 : 4.4%), respectively. Furthermore, most isolates were obtained from the urology, intensive care unit (ICU), and outpatient wards (Table 1). The results of the antibiotic resistance pattern of E. cloacae indicated that the highest antibiotic resistance was observed for nalidixic acid (68 : 60.2%) and ciprofloxacin (66 : 58.4%); however, the highest sensitivity was found for colistin (11 : 9.7%). The frequency of MDR strains was 78% (89 isolates). Among the 113 isolates, the frequency of quinolone-resistant isolates was determined to be 53.7%, with the highest and lowest levels of resistance to nalidixic acid (60.2%) and gatifloxacin (33.6%), respectively. Notably, quinolone-resistant isolates exhibited significantly higher drug resistance than quinolone-sensitive isolates, particularly against cephalosporins and aminoglycosides (Table 2). Based on the results of the double-disk synergy test (DDST) method, the frequencies of positive and negative ESBL isolates were determined to be 65 (57.5%) and 48 (42.5%), respectively. A high degree of resistance to all tested quinolones was observed in ESBL-producing isolates compared to non-ESBL-producing isolates. Statistically, there was a significant relationship between the drug resistance properties of ESBL-positive and ESBL-negative strains (Table 3). The frequency of PMQR in the 113 E. cloacae isolates was 77% (87 cases), and among these strains positive for ESBL, it was 93.8% (61/65 cases). The highest frequency of quinolone resistance genes was identified for the aac(6′)-Ib-cr gene (80 : 70.8%). The frequencies of the remaining genes were 20 (17.7%) and 43 (38.1%) for qnrS and qnrB genes, respectively. None of the strains possessed the qnrA gene. The frequency of the qnrB gene was the highest in the age group of 16–30 years (14/19 cases: 73.7%), which was statistically significant. However, in other cases, there was no significant relationship between the PMQR gene frequency and patient gender or different age groups (). The frequencies of isolates with two concurrent genes included 35.4%, 4.4%, and 13.8% for qnrB + aac(6′)-Ib-cr, qnrB + qnrS, and qnrS + aac(6′)-Ib-cr, respectively. In addition, 5 isolates simultaneously possessed 3 genes: qnrB + qnrS + aac(6′)-Ib-cr. The highest frequency of ESBL- and PMQR-positive strains was related to E. cloacae isolates obtained from clinical urine and blood samples in the urology and hospitalized wards (Table 2). From a statistical point of view, there was a significant relationship between the presence of the studied resistance genes and the drug resistance patterns () (Supplementary file (available here)). The majority of the genes studied were detected in the ESBL strains, and in some cases, this relationship was statistically significant (Table 4). Figure 1 shows the PCR results for the qnrB, qnrS, and aac(6′)-Ib-cr genes.

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(b)

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4. Discussion

In recent years, there has been a global increase in infections caused by MDR E. cloacae strains [18]. The highest frequency of identified strains was isolated from urine and wound samples. Previous studies have also reported isolating many strains of these bacteria from urine samples [2, 5, 19]. However, Liu et al. reported the highest frequency of E. cloacae isolation from sputum samples [20]. Among the studied strains, the highest resistance was observed against nalidixic acid (60.2%), ciprofloxacin, and tobramycin (58.4%). The overall resistance rates to quinolones, cephalosporins, and aminoglycosides were determined to be 53.7%, 50.4%, and 49.2%, respectively. Of 113 E. cloacae isolates, 89 (78%) exhibited multidrug resistance. The frequency of MDR E. cloacae isolates has been reported to range from 69.9% to 75% in other studies [3, 7, 21]. In Uzunović et al.’s study, over 66% and 28% of E. cloacae isolates were resistant to cephalosporins and aminoglycosides, respectively [22]. In 2022, the resistance rates to cephalosporins, gentamicin, ciprofloxacin, and imipenem in these isolates were 100%, 82.3%, 60.8%, and 7.5%, respectively [23]. Colistin (9.7%) and imipenem (14.2%) exhibited the lowest drug resistance rates among the isolates in this study. Other studies have reported lower antibiotic resistance rates in E. cloacae isolates against imipenem and colistin [20–23]. However, in Ebomah and Okoh survey, more than 70% of these bacterial strains were resistant to carbapenems [24]. Differences in resistance outcomes across studies might be attributed to variations in bacterial populations, their prevalence in hospital settings, the distribution of resistance genes, variations in antibiotic use patterns, and patient management practices. The frequency of ESBL production among E. cloacae strains in this study was determined to be 57.5%. The ESBL-positive isolates of this bacterium have been reported at rates ranging from 59.1% to 100% in other studies [6, 7, 25]. In ESBL-producing isolates, higher drug resistance was observed for all tested quinolones (). Azargun et al. reported a significant relationship between ESBL activity and fluoroquinolone resistance [26]. Discrepancies in these findings might be due to prolonged hospital stays and inappropriate and increased antibiotic use.

The frequency of PMQR in E. cloacae strains and ESBL-positive strains in this study was 77% and 93.8%, respectively. The high prevalence of PMQR and ESBL genes in this study can be indicative of the indiscriminate use of various antibiotics, including quinolones and beta-lactamases, followed by the spread of antibiotic resistance among bacterial isolates, which was consistent with the results of the drug resistance patterns. The highest frequency of the qnr gene was found in E. cloacae strains related to the aac(6′)-Ib-cr gene (70.8%). Given the location of the qnr gene in plasmids containing many resistant genes, including beta-lactamases, the higher frequency of quinolone-resistant isolates in ESBL-producing E. cloacae strains in the present study might be reasonable. Markovska et al. reported a PMQR gene frequency of 59% in Enterobacter strains [27]. In Azargon et al.’s study, similar to the results of the present study, the highest PMQR gene frequencies were found in ESBL-producing isolates. They also observed a significant correlation between the PMQR gene frequency and ESBL-positive isolates, which is consistent with the results of the present study [26]. In another study performed in 2020, the highest PMQR gene frequency among ESBL-producing Klebsiella pneumoniae strains was linked to aac(6′)-Ib-cr (55.6%) and qnrB (34.9%) [12]. The aforementioned results suggest a high frequency of quinolone-resistant genes, the presence of resistant bacterial strains, and the widespread prevalence of resistant genes among them. In Huang et al.’s study, 68.8% of E. cloacae isolates had the PMQR gene. They reported that the highest frequency of PMQR-positive and aac(6′)-Ib-cr-positive isolates was among the ESBL-producing isolates of this bacterium, which is consistent with the results of the current study [25]. Previous studies have shown that the presence of the PMQR gene is significantly associated with other antibiotic-resistant genes, including the ESBL gene, in bacterial isolates [28]. The present study’s most common qnr gene was qnrB (38.1%). Other studies have also reported qnrB as the most frequently detected qnr gene, similar to the findings of the current study. For instance, in Bolourchi et al.’s study, 3 of 4 isolates of E. cloacae carried this gene [29]. Markovska et al. reported the frequency of qnrB as 90% [27]. Among 113 strains of E. cloacae, the frequency of qnrS was determined to be 17.7%. In other studies, the frequency of this gene was reported as 24.1% and 37.1%, respectively [19, 25]. In Guillard et al.’s study, of the 31 PMQR-harboring E. cloacae isolates, 13 (42%) carried qnr only, and 17 (55%) carried both qnr and aac(6′)-Ib-cr [30]. In another study, the frequency of E. cloacae isolates carrying the qnr gene was reported at 60.3%, with qnrB1 being the most common (38.8%), followed by qnrS1 (24.1%). None of the isolates of the present study contained qnrA, which is consistent with studies conducted in Iran [10, 19]. However, in a study conducted in China, all 4 strains of E. cloacae had this gene [25]. In the current study, only 4.4% of isolates simultaneously possessed both qnrB and qnrS genes. In Peymani et al.’s study, there was a higher frequency (8.6%) of these isolates containing these genes together [19]. This is the first study on the prevalence of quinolone resistance mediated by the plasmid aac(60)-Ib-cr in E. cloacae in Kermanshah City. According to the results of a previous study and the findings of this study, it was shown that the frequency of the aac(6′)-Ib-cr gene was higher than that of the qnr gene in isolated Enterobacteriaceae strains. The main limitations of this study were the lack of research on other quinolone resistance mechanisms and the lack of plasmid DNA analysis.

5. Conclusions

In the present study, a high level of antibiotic resistance was observed in E. cloacae strains capable of producing PMQR and ESBL. This resistance can be attributed to the presence of plasmids in ESBL-producing isolates, which often carry various resistance genes. Considering the significant prevalence of the PMQR gene in ESBL-producing isolates among the samples in the current study, it is essential to emphasize the rational and appropriate use of various fluoroquinolones in the treatment of bacterial infections. The dissemination of PMQR and ESBL gene-containing plasmids is a cause for concern, as it can facilitate the selection and proliferation of MDR strains within the community. Therefore, conducting regular and comprehensive studies to gather more information about isolated E. cloacae strains in this context is imperative.

Data Availability

All data supporting the results are contained in the manuscript.

Conflicts of Interest

The authors declare that there are no conflicts of interest.

Authors’ Contributions

All authors contributed to the study conception and design, data acquisition, analysis, interpretation, and drafting and revising of the manuscript. The authors have read and approved the final version of the manuscript and agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. Mohsen Azizi, Nahid Madadi-Goli, and Kamal Ahmadi contributed equally to this work.

Acknowledgments

This research was supported by a grant (Grant No. 4000251) from Kermanshah University of Medical Sciences, Kermanshah, Iran. The authors of the manuscript would like to express their gratitude to the Vice Chancellor’s Office for Research and Technology and the Clinical Research Development Unit at Imam Reza Hospital of Kermanshah University of Medical Sciences, Kermanshah, Iran, for their cooperation in conducting this study.

Supplementary Materials

The primers and temperature cycles used in the PCR reaction to check the genes studied in this study are listed in the table primers (supplementary file). From a statistical point of view, there was a significant relationship between the presence of the studied resistance genes and the drug resistance patterns (). Of these, the most statistically significant correlation was observed between the presence of the aac(6′)-Ib-cr gene and resistance to most of the antibiotics studied, including quinolones, cephalosporins, and aminoglycosides (supplementary file). (Supplementary Materials)

References

A. Godmer, Y. Benzerara, A. C. Normand et al., “Revisiting species identification within the Enterobacter cloacae complex by matrix-assisted laser desorption ionization-time of flight mass spectrometry,” Microbiology Spectrum, vol. 9, no. 1, Article ID e0066121, 2021.
View at: Publisher Site | Google Scholar
S. H. Mortazavi, F. Mansouri, M. Azizi et al., “Prevalence of class I and II integrons among MDR Enterobacter cloacae isolates obtained from clinical samples of children in Kermanshah, Iran,” Journal of Clinical and Diagnostic Research, vol. 12, no. 12, 2018.
View at: Publisher Site | Google Scholar
M. Mishra, S. Panda, S. Barik, A. Sarkar, D. V. Singh, and H. Mohapatra, “Antibiotic resistance profile, outer membrane proteins, virulence factors and genome sequence analysis reveal clinical isolates of Enterobacter are potential pathogens compared to environmental isolates,” Frontiers in Cellular and Infection Microbiology, vol. 10, p. 54, 2020.
View at: Publisher Site | Google Scholar
A. Mustafa, M. Ibrahim, M. A. Rasheed et al., “Genome-wide analysis of four Enterobacter cloacae complex type strains: insights into virulence and niche adaptation,” Scientific Reports, vol. 10, no. 1, p. 8150, 2020.
View at: Publisher Site | Google Scholar
J. Intra, D. Carcione, R. M. Sala, C. Siracusa, P. Brambilla, and V. Leoni, “Antimicrobial resistance patterns of Enterobacter cloacae and Klebsiella aerogenes strains isolated from clinical specimens: a twenty-year surveillance study,” Antibiotics, vol. 12, no. 4, p. 775, 2023.
View at: Publisher Site | Google Scholar
M. K. Annavajhala, A. Gomez-Simmonds, and A. C. Uhlemann, “Multidrug-resistant Enterobacter cloacae complex emerging as a global, diversifying threat,” Frontiers in Microbiology, vol. 10, p. 44, 2019.
View at: Publisher Site | Google Scholar
M. Hemmati, S. Vaziri, M. Afsharian et al., “Molecular investigation of extended-spectrum β-lactamase and patterns of antibiotic resistance in Enterobacter cloacae isolates from teaching hospitals in Kermanshah, Iran,” Journal of Clinical and Diagnostic Research, vol. 13, no. 9, 2019.
View at: Publisher Site | Google Scholar
A. Davin-Regli, J. P. Lavigne, and J. M. Pagès, “Enterobacter spp.: update on taxonomy, clinical aspects, and emerging antimicrobial resistance,” Clinical Microbiology Reviews, vol. 32, no. 4, pp. e00002–e00019, 2019.
View at: Publisher Site | Google Scholar
Y. Long, X. Lu, X. Ni et al., “High carriage rate of the multiple resistant plasmids harboring quinolone resistance genes in Enterobacter spp. isolated from healthy individuals,” Antibiotics, vol. 11, no. 1, p. 15, 2021.
View at: Publisher Site | Google Scholar
A. Majlesi, R. K. Kakhki, A. S. Mozaffari Nejad et al., “Detection of plasmid-mediated quinolone resistance in clinical isolates of Enterobacteriaceae strains in Hamadan, West of Iran,” Saudi Journal of Biological Sciences, vol. 25, no. 3, pp. 426–430, 2018.
View at: Publisher Site | Google Scholar
M. B. Amin, S. R. Saha, M. R. Islam et al., “High prevalence of plasmid-mediated quinolone resistance (PMQR) among E. coli from aquatic environments in Bangladesh,” PLoS One, vol. 16, no. 12, Article ID e0261970, 2021.
View at: Publisher Site | Google Scholar
S. Vaziri, M. Afsharian, F. Mansouri et al., “Frequency of qnr and aac(6’)Ib-cr genes among ESBL-producing Klebsiella pneumoniae strains isolated from burn patients in Kermanshah, Iran,” Jundishapur Journal of Microbiology, vol. 13, no. 7, Article ID e100348, 2020.
View at: Publisher Site | Google Scholar
J. M. Rodríguez-Martínez, J. Machuca, M. E. Cano, J. Calvo, L. Martínez-Martínez, and A. Pascual, “Plasmid-mediated quinolone resistance: two decades on,” Drug Resistance Updates, vol. 29, pp. 13–29, 2016.
View at: Publisher Site | Google Scholar
G. B. Kraychete, L. A. B. Botelho, P. V. Monteiro-Dias et al., “qnrVC occurs in different genetic contexts in Klebsiella and Enterobacter strains isolated from Brazilian coastal waters,” Journal of Global Antimicrobial Resistance, vol. 31, pp. 38–44, 2022.
View at: Publisher Site | Google Scholar
K. Kariuki, M. M. Diakhate, S. Musembi et al., “Plasmid-mediated quinolone resistance genes detected in Ciprofloxacin non-susceptible Escherichia coli and Klebsiella isolated from children under five years at hospital discharge, Kenya,” BMC Microbiology, vol. 23, no. 1, p. 129, 2023.
View at: Publisher Site | Google Scholar
D. N. Kotb, W. K. Mahdy, M. S. Mahmoud, and R. M. M. Khairy, “Impact of co-existence of PMQR genes and QRDR mutations on fluoroquinolones resistance in Enterobacteriaceae strains isolated from community and hospital acquired UTIs,” BMC Infectious Diseases, vol. 19, no. 1, p. 979, 2019.
View at: Publisher Site | Google Scholar
F. Amereh, M. R. Arabestani, and L. Shokoohizadeh, “Relationship of OqxAB efflux pump to antibiotic resistance, mainly fluoroquinolones in Klebsiella pneumoniae, isolated from hospitalized patients,” Iranian Journal of Basic Medical Sciences, vol. 26, no. 1, pp. 93–98, 2023.
View at: Publisher Site | Google Scholar
T. B. Lima, O. N. Silva, K. C. de Almeida et al., “Antibiotic combinations for controlling colistin-resistant Enterobacter cloacae,” Journal of Antibiotics, vol. 70, no. 2, pp. 122–129, 2017.
View at: Publisher Site | Google Scholar
A. Peymani, T. N. Farivar, R. Najafipour, and S. Mansouri, “High prevalence of plasmid-mediated quinolone resistance determinants in Enterobacter cloacae isolated from hospitals of the Qazvin, Alborz, and Tehran provinces, Iran,” Revista da Sociedade Brasileira de Medicina Tropical, vol. 49, no. 3, pp. 286–291, 2016.
View at: Publisher Site | Google Scholar
L. Liu, J. Yu, M. Tang, and J. Liu, “Mechanisms of resistance in clinical isolates of Enterobacter cloacae that are less susceptible to cefepime than to ceftazidime,” Annals of Clinical Laboratory Science, vol. 48, no. 3, pp. 355–362, 2018.
View at: Google Scholar
J. Sumbana, A. Santona, M. Fiamma et al., “Polyclonal emergence of MDR Enterobacter cloacae complex isolates producing multiple extended spectrum beta-lactamases at Maputo Central Hospital, Mozambique,” Rendiconti Lincei, vol. 33, no. 1, pp. 39–45, 2022.
View at: Publisher Site | Google Scholar
S. Uzunović, A. Ibrahimagić, and B. Bedenić, “Antibiotic resistance in Enterobacter cloacae strains with derepressed/partly derepressed/inducible AmpC and extendedspectrum beta-lactamases in Zenica-Doboj Canton, Bosnia and Herzegovina,” Medicinski Glasnik, vol. 15, no. 1, pp. 37–45, 2018.
View at: Publisher Site | Google Scholar
S. Manandhar, Q. Nguyen, T. Nguyen Thi Nguyen et al., “Genomic epidemiology, antimicrobial resistance and virulence factors of Enterobacter cloacae complex causing potential community-onset bloodstream infections in a tertiary care hospital of Nepal,” JAC-Antimicrobial Resistance, vol. 4, no. 3, 2022.
View at: Publisher Site | Google Scholar
K. E. Ebomah and A. I. Okoh, “Enterobacter cloacae harbouring blaNDM-1, blaKPC, and blaOXA-48-like carbapenem-resistant genes isolated from different environmental sources in South Africa,” International Journal of Environmental Studies, vol. 78, no. 1, pp. 151–164, 2021.
View at: Publisher Site | Google Scholar
S. Huang, W. Dai, S. Sun, X. Zhang, and L. Zhang, “Prevalence of plasmid-mediated quinolone resistance and aminoglycoside resistance determinants among carbapeneme non-susceptible Enterobacter cloacae,” PLoS One, vol. 7, no. 10, Article ID e47636, 2012.
View at: Publisher Site | Google Scholar
R. Azargun, M. R. Sadeghi, M. H. Soroush Barhaghi et al., “The prevalence of plasmid-mediated quinolone resistance and ESBL-production in Enterobacteriaceae isolated from urinary tract infections,” Infection and Drug Resistance, vol. 11, pp. 1007–1014, 2018.
View at: Publisher Site | Google Scholar
R. Markovska, T. Stoeva, D. Dimitrova et al., “Quinolone resistance mechanisms among third-generation cephalosporin resistant isolates of Enterobacter spp. in a Bulgarian university hospital,” Infection and Drug Resistance, vol. 12, pp. 1445–1455, 2019.
View at: Publisher Site | Google Scholar
L. Yan, D. Liu, X. H. Wang et al., “Bacterial plasmid-mediated quinolone resistance genes in aquatic environments in China,” Scientific Reports, vol. 7, no. 1, Article ID 40610, 2017.
View at: Publisher Site | Google Scholar
N. Bolourchi, C. G. Giske, S. Nematzadeh et al., “Comparative resistome and virulome analysis of clinical NDM-1-producing carbapenem-resistant Enterobacter cloacae complex,” Journal of Global Antimicrobial Resistance, vol. 28, pp. 254–263, 2022.
View at: Publisher Site | Google Scholar
T. Guillard, P. Cholley, A. Limelette et al., “Fluoroquinolone resistance mechanisms and population structure of Enterobacter cloacae non-susceptible to ertapenem in north-eastern France,” Frontiers in Microbiology, vol. 6, p. 1186, 2015.
View at: Publisher Site | Google Scholar

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Copyright © 2024 Mandana Afsharian et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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