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| Year : 2014 | Volume
: 57
| Issue : 2 | Page : 244-248 |
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| Molecular detection of ESBLs production and antibiotic resistance patterns in Gram negative bacilli isolated from urinary tract infections |
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Mehdi Kargar1, Mohammad Kargar2, Mohammad Zareian Jahromi2, Akram Najafi3, Sadegh Ghorbani-Dalini1
1 Department of Microbiology, Jahrom Branch, Young Researcher's and Elit Club, Jahrom, Iran
2 Department of Microbiology, Jahrom Branch, Islamic Azad University, Jahrom, Iran
3 Department of Marine Microbiology, The Persian Gulf Marine Biotechnolohy Research Center, Bushehr University of Medical Sciences, Bushehr, Iran
Click here for correspondence address and email
| Date of Web Publication | 19-Jun-2014 |
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 Abstract | | |
Background: β-lactam resistance is more prevalent in Gram negative bacterial isolates worldwide, particularly in developing countries. In order to provide data relating to antibiotic therapy and resistance control, routine monitoring of corresponding antibiotic resistance genes is necessary. Aims: The aim of this study was the characterization of β-lactam resistance genes and its plasmid profile in bacteria isolated from urinary tract infection samples. Materials and Methods: In this study, 298 Gram negative bacteria isolated from 6739 urine specimens were identified by biochemical standard tests. Antimicrobial susceptibility testing was performed by the disk diffusion method. Extended-spectrum β-lactamase (ESBL)-producing strains were also detected by the double-disk synergy test. The presence of blaTEM and blaSHV genes in the strains studied was ascertained by polymerase chain reaction. Results: Of all Gram negative bacteria, Escherichia coli (69.1%) was the most common strain, followed by Klebsiella sp. (12.1%), Enterobacter sp. (8.4%), Proteus sp. (4.4%), Citrobacter (4%) and Pseudomonas sp. (2%). The most antibiotic resistance was shown to tetracycline (95.16%), nalidixic acid (89.78%) and gentamycin (73.20%) antibiotics. Among all the strains tested, 35 isolates (11.75%) expressed ESBL activity. The prevalence of TEM and SHV positivity among these isolates was 34.29%, followed by TEM (31.43%), TEM and SHV negativity (20.0%) and SHV (14.29%), respectively. Conclusions: Regular monitoring of antimicrobial drug resistance seems necessary to improve our guidelines in the use of the empirical antibiotic therapy. Keywords: Antibiotic resistance, blaSHV , blaTEM , ESBLs
How to cite this article:
Kargar M, Kargar M, Jahromi MZ, Najafi A, Ghorbani-Dalini S. Molecular detection of ESBLs production and antibiotic resistance patterns in Gram negative bacilli isolated from urinary tract infections. Indian J Pathol Microbiol 2014;57:244-8 |
How to cite this URL:
Kargar M, Kargar M, Jahromi MZ, Najafi A, Ghorbani-Dalini S. Molecular detection of ESBLs production and antibiotic resistance patterns in Gram negative bacilli isolated from urinary tract infections. Indian J Pathol Microbiol [serial online] 2014 [cited 2023 Mar 30];57:244-8. Available from: https://www.ijpmonline.org/text.asp?2014/57/2/244/134688 |
| Introduction | |  |
Among Gram negative pathogens in Iran, the incidence of resistance to extended-spectrum β-lactamase (ESBL) is becoming a major problem. Production of β-lactamase is the most common mechanism responsible for resistance to β-lactam antibiotics among the members of the Enterobacteriaceae family. Generally, β-lactamases are divided into four classes (A-D) according to their amino acid sequence homology. Plasmid-mediated class A β-lactamases derived from TEM (named for a patient called Temoniera) and SHV (named for sulfhydryl variables) enzymes have most frequently been reported. [1] For the first time in 1965, Datta and Kontomichalou reported that TEM-1 (classical TEM-type β-lactamase) shows a high level of resistance to penicillins (ampicillin and piperacillin) and early cephalosporins (cephalosporin). Later, it was reported that TEM-1 (classical TEM-type β-lactamase) confers little resistance to oxyiminocephalosporins, monobactams and carbapenems. [2]
TEM-1-derived ESBLs appeared in the beginning of the 1980s when β-lactam antibiotics were introduced into the field of medicine. In most of the cases ESBLs are plasmid mediated, and most of them are mutant forms of TEM-1 enzymes in which one or more amino acids have been substituted. These amino acids are located around the active site. [3]
As a result of these changes, some of ESBLs such as cephalosporins (ceftazidime and cefotaxime) and monobactams (aztreonam), which remain stable to TEM-1 enzymes, will hydrolyze. [4] In their study, Hall and Barlow reported that TEM β-lactamases probably diverged around 400 million years ago (before the antibiotic era). [5] Since the introduction of broad-spectrum antibiotics, the importance of Gram negative bacteria has increased. The reason is that these organisms often carry multiple antibiotic resistances. [6]
Epidemiological studies conducted in different geographical regions of the world have indicated that ESBLs producing Gram negative bacteria are responsible for 23-51% of the community/hospital-acquired infections. [7],[8],[9] Also, previous population-based investigations in Iran have revealed that these strains are caused by 14-56% of ESBL production in this region. [10],[11],[12],[13],[14] In this study, in addition to the evaluation of antibiotic resistance patterns and the plasmid profile of the bacterial agents in urinary tract infection (UTI), plasmid-mediated ESBLs are evaluated using bla TEM and bla SHV genes.
| Materials and methods | | |
Isolation and identification of bacteria
A total of 6739 urine specimens were collected from the suspect patient with UTI admitted to the hospitals and clinical laboratories in Jahrom, Iran, during 2011-2012. All the samples were transported to the Microbiology Laboratory of the Islamic Azad University of Jahrom for greater evaluation under sterile conditions.
The samples were cultured on standard media, including Blood agar, MacConkey's agar and Eosin methylene blue (Merck, Darmstadt, Germany) and incubated at 37°C for 24 h. The isolation and identification of Gram negative bacteria were performed by catalase, oxidase and routine biochemical tests, i.e. indole, motility, methyl red, Voges-Proskauer, lysine decarboxylase, Simmon citrate agar, urease, OD, PD and triple sugar iron agar (TSI). All the isolates were stored in trypticase soy broth (Merck, Darmstadt, Germany) with 25% sterile glycerol at –70°C.
The study was approved by the Ethical and Research Committee of the Jahrom University of Medical Sciences, Iran.
Antibiogram
The isolates on Luria-Bertani (L.B.) broth were incubated at 37°C for 24 h. The number of bacteria per milliliter was accessed according to a 0.5 Mac Farland standard (1.5 × 10 8 cfu/mL). Bacteria were grown on Mueller Hinton agar (Merck, Darmstadt, Germany) using the Lown method.
Antimicrobial susceptibility was determined by disc diffusion tests according to the Clinical Laboratory Standards Institute (CLSI) guidelines. [15] The antimicrobial drugs used were ampicillin (10 μg), amikacin (30 μg), tobramycin (30 μg), gentamicin (10 μg), tetracycline (30 μg), chloramphenicol (30 μg), nalidixic acid (30 μg) and cotrimoxazole (sulfamethoxazole 23.75 μg + trimethoprim 1.75 μg) (Padtan Teb, Tehran, Iran).
E. coli ATCC 25922 was used as the positive control. Making use of the double disk synergy test (DDST), ESBL identification was achieved. Resistant isolates to gentamycin‚ trimethoporim-sulphamethoxazole‚ tetracycline‚ nalidixic acid‚ amikacin‚ ampicilin‚ tobramycin and chloramphenicol were grown on a Mueller-Hinton broth and subsequently incubated at 37°C for 24 h to yield turbidity equal to a 0.5 Mac Farland standard. Three discs with ceftazidime (30 μg), cefotaxime (30 μg) and Co-amoxyclave (10 μg) were placed on the Mueller-Hinton agar (Merck, Darmstadt, Germany) with a disc spacing of 20 mm (center to center).
The ESBL-producing phenotype was screened through characteristic distortion of the inhibition zones. The DDST was used to evaluate ESBL-producing strains that showed resistance to one or more third-generation cephalosporins. The ESBL production is inferred when the cephalosporin inhibition zone is expanded and enlarged by clavulanic acid (>5 mm). [16]
Plasmid extraction
ESBL-producing bacterial strains that were resistant to gentamycin‚ trimethoporim-sulphamethoxazole‚ tetracycline‚ nalidixic acid‚ amikacin‚ ampicilin‚ tobramycin and chloramphenicol antibiotics were grown on L.B. broth at 37°C for 24 h. Plasmid extraction was performed according to the Kado and Liu method. [17] Plasmid size was determined by agarose gel electrophoresis on 0.8% agarose gel (Merck, Darmstadt, Germany) stained with ethidium bromide.
Polymerase chain reaction (PCR)
TEM-1 and SHV-1 genes were amplified by PCR using the following specific primers: TEM-1-F (5΄-TTGGGTGCACGAGTGGGTTA-3΄) and TEM-1-R (5΄-TAATTGTTGCCGGGAAGCTA-3΄) for the TEM-1 gene and SHV-1-F (5΄-CGCCGGGTTATTCTTATTTGTCGC-3΄) and SHV-1-R (5΄-TCTTTCCGATGCCGCCGCCAGTCA-3΄) for the SHV-1 gene. [18],[19]
PCR amplification was carried out in volume of 25 μL containing 0.5 μM of each primer, 1.5 mM MgCl 2 , 250 μM dNTPs, 1X PCR buffer (Fermentase), 5 μL of extracted plasmid and 2U Taq DNA polymerase (Fermentase). Following an initial denaturation at 94°C for 3 min, the samples were subjected to 30 cycles of 1 min denaturation at 94°C, 1 min annealing at 55°C, 1 min extension at 72°C and a final extension at 72°C for 10 min. PCR products were visualized by staining with ethidium bromide on 1.2% agarose gel (Merck, Darmstadt, Germany).
Statistical analysis
The data were statistically analyzed by SPSS version 15 (SPSS Inc., Chicago, IL, USA). The chi-square test or the Fisher exact test was provided to compare categorical variables. P-value <0.05 was considered statistically significant.
| Results | | |
Gram negative bacteria were detected in 4.42% (298/6739) of all the evaluated urine samples as follows: E. coli (69.1%), Klebsiella sp. (12.1%), Enterobacter sp. (8.4%), Proteus sp. (4.4%), Citrobacter sp. (4%) and Pseudomonas sp. (2%). The distribution of gender in positive cases was 207 (66.46%) in females and 91 (30.54%) in males [Table 1]. All the suspect patients with UTI were classified between less than 6 to more than 50 years of age groups. The most Gram negative bacteria were detected in the 20-50 years age group, accounting for 44.3% of the infected patients [Table 1]. | Table 1: Distribution of gender and age groups among ESBL-positive and -negative strains
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The resistance of the isolated bacteria to antimicrobial agents is shown in [Table 2]. The most antibiotic resistance was shown to tetracycline (95.16%), nalidixic acid (89.78%) and gentamycin (73.20%) antibiotics. Also, the lowest antibiotic resistance was observed to co-amoxyclave (25.75%) and ampicillin (27.34%).
In the present study, of the 298 isolates of Gram negative bacteria, 35 (11.75%) were detected as ESBL producers and 263 (88.25%) were detected as non-ESBL producers. [Table 3] shows the genotypic resistance patterns of the isolated strains. The prevalence of both TEM- and SHV-positive genes among the Gram negative bacteria was 34.29%, followed by TEM (31.43%), both TEM and SHV negative (20.0%) and SHV (14.29%).
In this study, the isolated strains revealed different plasmids including 18, 16.5, 14, 12, 9.8, 9.5, 9, 8.5 and 3.4 kb. As shown in [Figure 1], plasmids of different molecular sizes were extracted among which the largest amount is 18 kb and the least is 3.4 kb. | Figure 1: Bacterial isolates' plasmid extraction on 0.8% agarose gel. Lanes (1) E. coli showing plasmid of 18 and 6.5 Kb; (2) Citrobacter sp. showing plasmids of 16.5 and 9 Kb; (3) E. coli6 showing plasmid of 9.8 and 8.5 Kb; (4) E. coli11 showing plasmids 1.8 and 1.5 Kb; (5) E. coli13 showing plasmid of 12 Kb; (6) E. coli18 showing plasmid of 9.5 Kb M molecular size marker of 1 Kb; (7) E. coli36 showing no plasmid; (8) E. coli49 showing no plasmid; (9) E. coli52 showing plasmids of 14 and 18Kb; (10) E. coli56 showing plasmid of 3.4 Kb
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| Discussion | | |
Nosocomial infections can cause infections of the urinary tract and other parts of the body. Many types are difficult to attack with antibiotics, and antibiotic resistance is spreading to Gram negative bacteria that can infect people outside the hospital. ESBL-producing members of the Enterobacteriaceae family have played a leading role among nosocomially acquired multidrug-resistant organisms during the past decade. Also, ESBL-producing bacteria should be considered in the etiology of nosocomial infections in patients with risk factors. [20]
This study provides data about the problem of resistance in Enterobacteriaceae obtained from patients handled in an outpatient facility from a hospital and in a municipal health unit.
In the present study, E. coli was the most common isolated Gram negative bacteria causing UTI, which is in accordance with other reviewed studies from Iran [10],[13] and other developed and developing countries. [21],[22],[23],[24]
In this study, the frequency of ESBL-producing bacteria was 11.75%, which is consistent with those reported in 13 European countries [25] and Poland. [26] But, our results were much lower than those published in other developing countries. [27],[28],[29],[30] Some Iranian surveys, conducted in five Iranian hospitals, found a 14-56% prevalence of ESBL-positive pathogens, [10],[11],[12],[13],[14] which is more than that observed in our study. On the other hand, the largest amount of ESBL-producing organisms were demonstrated to be E. coli isolates, with a frequency of 48.57%, and the least amount were shown to be Proteus isolates, which demonstrated no ESBL.
The identification of ESBL genotypes revealed that majority of the ESBL-producing isolates carried both TEM and SHV in contrast to TEM or SHV alone. Among the single gene carrier strains, the proportion of TEM was higher than the proportion of SHV. Many molecular epidemiological studies from around the world have shown that the TEM gene is the most common ESBL genotype, [12],[14],[31],[32] whereas TEM was the second identified type in our study.
In 2009, a community-based study demonstrated that the most prevalent ESBL gene was bla SHV among ESBL-producing Enterobacteriaceae. [33] Also, bla SHV is known to be a predominant genotype in other conducted studies, [34],[35] whereas in our study bla SHV had the lowest frequency among the identified types.
The spread of ESBL-producing bacteria has been expanding rapidly worldwide, indicating that continuous monitoring systems and effective infection control measures are absolutely required. Therapeutic options against infections due to ESBL producers have also become increasingly limited. Health care interactions including the use of antibiotics, particularly oxyiminocephalosporins, and hospital transfers are among the well-defined risk factors for the acquisition of ESBL-producing bacteria. [36]
The isolates had the most resistance against tetracycline (95.16%) and nalidixic acid (89.78%) antibiotics. The rates observed in the present study for antibiotic-resistant isolates are in agreement with those reported by other researchers in antimicrobial surveillance studies in developing countries including some from Iran [37] and Pakistan. [38] On the other hand, the least resistance was shown to ampicillin (27.34%). This finding contrasts with previous reports in Portugal [35] and Italy. [32] Our finding revealed that among the isolated bacteria, E. coli have high rates of resistance to the commonly used antibiotics. Assessment of antimicrobial resistance patterns will help physicians to administer drugs more effectively and treat diseases sooner. Therefore, performing antimicrobial resistance tests is suggested for all patients with hospital infections, especially those with UTIs.
| Conclusion | | |
The present study indicates that the prevalence of ESBL genes in the investigated area is in accordance with other parts of Iran. But, these findings are different from other parts of the world like Egypt and Austria, where CTX-M is predominant. [16] Also, considering the similar profile of the detected plasmids in the isolates, the prevalence of ESBL genes among different members of the Enterobacteriaceae family is confirmed. This subject can specify the importance of more attention to therapeutic regime, especially for high-risk patients. Therefore, limitation in taking broad-spectrum and third-generation cephalosporins seems to be essential for infection control program.
| Acknowledgment | | |
All authors are grateful to the Islamic Azad University, Jahrom branch for their executive support of this project
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Correspondence Address:
Mohammad Kargar
Department of Microbiology, Jahrom Branch, Islamic Azad University, Jahrom
Iran
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/0377-4929.134688
[Figure 1]
[Table 1], [Table 2], [Table 3] |
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