International Journal of Current Research and Review
ISSN: 2231-2196 (Print)ISSN: 0975-5241 (Online)
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IJCRR - Vol 05 Issue 17, September, 2013

Pages: 28-35

Date of Publication: 12-Sep-2013


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PHENOTYPIC ASSAYS FOR DETECTION OF ESBL AND MBL PRODUCERS AMONG THE CLINICAL ISOLATES OF MULTIDRUG RESISTANT PSEUDOMONAS AERUGINOSA FROM A TERTIARY CARE HOSPITAL

Author: Kalaivani R., Shashikala P., Sheela Devi C., Prashanth K., Saranathan R.

Category: Healthcare

Abstract:Introduction: Pseudomonas aeruginosa has been a major nosocomial pathogen associated with nosocomial pneumonia, surgical site infections and UTI in patients admitted to intensive care units in the recent past(1). Major risk factors includes prolonged hospitalization, ventilation, underlying immunocompromised state and inadequate or irrational antimicrobial therapy(2). Despite improvements in therapy due to introduction of newer antimicrobials, P. aeruginosa is intrinsically resistant to number of antimicrobials, they aroused a major challenge to overcome the morbidity and mortality caused by multidrug and pan drug resistant P. aeruginosa(3). Drug resistance in turn leads to prolonged hospital stay and increased expenditure, which causes increased cross infections and poorer clinical outcomes. The present study investigated the prevalence of resistance mechanisms among Multi Drug Resistant Pseudomonas aeruginosa (MDRPA) clinical isolates from a tertiary care hospital. Methods: Seventy-five MDRP. aeruginosa isolates were obtained from 226 patients admitted in various wards. Antimicrobial susceptibility testing was performed by disk diffusion method and all these isolates were found to be MDR. All the isolates were subjected to different phenotypic assays to detect the production of enzymes such as ESBL, AmpC and MBL,. MIC determination was done by agar dilution method for Meropenem and Polymyxin B. Further, quantitative evaluation of biofilm production by was carried out by microtitre plate assay, since many studies have shown positive correlation between MDR and biofilm formation. Results: Of the 75 MDR P. aeruginosa, 36% were resistant to imipenem and 80% to meropenem. All the isolates were sensitive to polymyxin B. MBL production (38.67%) was found to be the predominant resistance mechanism followed by ESBL production (26.67%). None of them showed AmpC production. Ninety three percent (93%) of the strains produced abundant biofilms. Conclusion: P. aeruginosa was shown to be predominant nosocomial pathogen showing resistance to most of the available antibiotics including carbapenems. MBL is shown to be predominant mechanism for development of resistance in the present study.

Keywords: MDR, Pseudomonas aeruginosa, ESBL, MBL.

Full Text:

INTRODUCTION

Pseudomonas aeruginosa is one of the significant Gram-negative bacteria causing hospital-associated infections(4). Among the common multidrug resistant (MDR) nosocomial pathogens emerged in medical centers, P. aeruginosa is the most frequent pathogen causing life threatening infections markedly, respiratory tract infections, surgical site and urinary tract infections in patients from intensive care units (ICUs)(5). It has significant role in causing chronic debilitating respiratory infections in cystic fibrosis patients due to mucoid strains, which leads to increased mortality. Prolonged endotracheal intubation, associated with exposure to inappropriate antimicrobial therapies leads to colonization of the upper respiratory tract thereby complicates the eradication (6).

A major challenge has aroused regarding the treatment of infections caused by opportunistic pathogens, predominantly those with pan drug resistant P. aeruginosa and Acinetobacter baumannii strains, which has extreme ability to acquire resistance (7, 8). P.  aeruginosa possesses the ability to acquire resistance genes from the environment as well as from other bacteria (4). High mortality may be attributable to the inherent virulence of the organism as well as the fact that it often occurs with immunosuppression and co morbidity conditions (9, 10). In addition, P aeruginosa is susceptible to a limited number of antimicrobial agents, which increases the likelihood of inappropriate empirical antimicrobial therapy. Reported rates of Multidrug Resistant Pseudomonas aeruginosa (MDRPA) varied from 0.6% - 32% according to various surveillance studies held in different geographic locations (11, 12).  The prevalence of MDRPA has increased over the past decade and has become a major concern among hospitalized patients. Several mechanisms can contribute to resistance in P. aeruginosa, including β-lactamase production, up regulation of efflux systems, biofilm formation and decreased outer membrane permeability.

However, production of β- lactamases such as Metallo- β- lactamases (MBL) and Extended spectrum β-lactamases (ESBL) are the most common resistant mechanisms documented in P. aeruginosa. As carbapenems are the most potent β-lactams against P. aeruginosa, intensive use of carbapenems facilitated the emergence of carbapenem-resistant P. aeruginosa(14).  Resistance to all antibiotics except polymyxins is now a reality in many medical centers. Despite of abundant literature, little is known about the prevalence of these mechanisms among the clinical isolates of P. aeruginosa from India. Hence, this study was carried out to understand the prevailing mechanisms of resistance among the clinical isolates of MDRPA from in-patients of a tertiary care hospital. This possibly will help to prevent the associated morbidity and mortality caused by this organism by implementing proper infection control measures, which can reduce the duration of hospital stay and expenditure.

MATERIALS AND METHODS

Study design                                                   

A descriptive study was conducted during the period of November 2009 to October 2010. Seventy-five MDR P. aeruginosa isolates were obtained from 226 patients admitted in various wards of the hospital. All the clinically significant MDRPA isolates collected in the Department of Clinical Microbiology laboratory from wound swabs, endotracheal aspirates, urine, blood, broncheoalveolar lavage, drain tip and tissue samples were investigated. Repeat isolates were excluded from the study. All the isolates were identified by standard microbiological techniques. ATCC P. aeruginosa 27853 strain was used as quality control reference strain for all experiments with satisfactory results.

Antibiotic susceptibility testing was performed  by Kirby-Bauer disc diffusion method. All these isolates were found to be MDR and were responsible for clinically significant infections. Isolates were also tested for carbapenemase production, if they were found to be intermediate or resistant to either Imipenem or meropenem in disc diffusion method. MIC values were determined by agar dilution method for clinically relevant antibiotics such as meropenem (Astra Zeneca, Bangalore) and polymyxin B (Hi-Media, Mumbai) as per CLSI guidelines.

All the MDR P. aeruginosa were subjected to different phenotypic assays to detect the production of enzymes such as ESBL, AmpC and MBL, which are implicated for causing multiple drug resistance. Phenotypic confirmatory test for ESBL production was performed by placing ceftazidime (30 μg) and ceftazidime + clavulanic acid disc. Detection of Metallo-ß-lactamases was carried out by combined disc diffusion test. AmpC detection was done using AmpC discs method.

Microtitre plate assay for Biofilm production

Since many studies have shown positive correlation between biofilm and multiple drug resistance, quantitative evaluation of biofilm production by P. aeruginosa isolates was carried out by microtitre plate assay (16), (17).  Biofilm negative E. coli isolate from our collection and ATCC P. aeruginosa 27853 were used as negative and positive controls respectively.  Based on the OD values, the extent of biofilm formed by the clinical isolates were classified as follows,

  • OD ≤ ODc   - Non adherent
  • ODc < OD ≤ 2 × ODc- Weakly adherent
  • 2 × ODc < OD4 × ODc- Moderately adherent
  • 4 × ODc < OD - Strongly adherent (20).

RESULTS

Among the seventy-five patients with MDRPA infection, males were found to be more predominant (66.7%) than females (33.3%). MDR P. aeruginosa infections were found to be 34.7% between 21 to 40 years of age group. MDR P. aeruginosa were mainly isolated from wound infections (43%), followed by endotracheal aspirates (19%), urine (16%), and blood (11%), bronchoalveolar lavage (BAL)( 7%,) drain tip (3%) and tissue (1%) respectively(Fig.1). Various risk factors for MDRPA infection were patients with prolonged hospitalization (52%), patients who are on Foley’s catheter (45%), patients with diabetes mellitus (37%), on ventilator (25%), on tracheostomy (21%), post operative patients (16%), on central line catheter (12%) and on steroids (1%). Thirty-three percentage of   patients (n=25) were found to have more than two risk factors.

MDRPA isolates showed markedly high-level resistance towards ciprofloxacin (95%), tobramycin (92%), ceftriaxone and gentamicin, (83%). Forty-four isolates (59%) showed resistance to amikacin and 51% resistance was noticed for piperacillin + tazobactum. Among carbapenems, imipenem showed 36% resistance and meropenem 53% resistance. None of the isolates was resistant to polymyxin B. Among the 75 MDRPA isolates, 13 isolates, which were isolated from urine samples, showed 77% of resistance to norfloxacin and carbenicillin.

MIC for meropenem ranged from 0.5µg/ml to >64µg/ml. Forty out of seventy five (53.33%) isolates of MDRPA were found to be resistant to meropenem. The isolates were categorized resistant if the MIC value was more than 8µg/ml. Thirty two (42.67%) isolates showed sensitive MIC value (≤4µg/ml) and 4% (3) isolates showed intermediate MIC   value (8µg/ml). All the isolates showed lower MIC of 0.5µg/ml to 1µg/ml for polymyxin B (Break point MIC for Pseudomonas aeruginosa ≤2µg/ml to ≥8µg/ml) and none of these isolates showed resistant or intermediate MIC values (Fig.2).

Thirty-nine percent of isolates were found to produce MBL and only, 27% isolates showed ESBL production, none of the isolates showed AmpC production. Twelve percent (9) of isolates were found to be negative for phenotypic production of all β-lactamases (fig.3). Almost all isolates (93%) from our collection were biofilm producers, wherein 75% of the isolates were strongly adherent, 8% moderately adherent and 11% weakly adherent. The percentage of non-adherent cells or biofilm negative isolates was found to be a meager of 7%.

DISCUSSION

P. aeruginosa is a leading cause of nosocomial infections, and it exhibits intrinsic resistance to almost all commercially available antimicrobial agents. However, acquired resistance to anti-pseudomonal β-lactam antibiotics such as ticarcillin, piperacillin, ceftazidime, cefepime, aztreonam and especially carbapenems can be a major challenge in managing MDRPA infections, mostly when it is associated with co-resistance with other classes of drugs namely aminoglycosides and quinolones. Acquired ESBL and metallo-β-lactamases are the major β-lactamases produced by P. aeruginosa.

The prevalence of MDR P. aeruginosa was found to be 33.2% in our investigation, which is in accordance with a similar recent study from India that showed the predominance rate of 44% (18). However, comparatively lesser prevalence of MDRPA (26.7%) responsible for burn wound infections in Iran (19). Likewise, one more investigation from India reported 22% MDRPA and 4% Pandrug resistant P aeruginosa (20), wherein, we recorded a higher level of MDRPA incidence. Factors such as age and sex among MDRPA infection were found to have significant association with MDRPA, wherein the incidence was more among the age groups between 21 and 40 (34.7%) and males being predominant (67%) which is the likely case in earlier reports (21). Possibly, it may be due to high incidence of road traffic accidents among males, leading to hospitalization thereby high incidence of P. aeruginosa infection through catheterization.

Earlier investigations have reported the major source of MDRPA to be sputum, tracheostomy specimen, pus, respiratory tract, surgical sites and endotracheal aspirate (22, 23 24, 25). In the present study, the major source of MDRPA was found to be wound  swabs (43%), followed by endotracheal aspirate (19%) implying that wound  infections and respiratory tract infections are most significant infections caused by MDRPA in most of the hospitals including our setup. The major risk factors were prolonged hospitalization followed by patients on Foleys catheter.  Foot infections and surgical site infections were found to be common source of MDRPA among the diabetic patients.

MDRPA isolates showed markedly high-level resistance towards ciprofloxacin (95%), tobramycin (92%), ceftriaxone and gentamicin, (83%). Forty-four isolates (59%) showed resistance to amikacin and 51% resistance was noticed for piperacillin/ tazobactum combination. Among carbapenems, imipenem and meropenem resistance was observed to be 36% and 53% respectively. None of the isolates were resistant to polymyxin B. Among the 75 MDRPA isolates, 13 isolates, which were isolated from urine samples, showed 77% of resistance to norfloxacin and carbenicillin.

MIC for meropenem ranged from 0.5µg/ml to >64µg/ml. Forty out of seventy five (53.33%) isolates of MDRPA were found to be resistant to meropenem. The isolates were categorized resistant if the MIC value was more than 8µg/ml. Thirty two (42.67%) isolates showed sensitive MIC value (≤4µg/ml) and 4% (3) isolates showed intermediate MIC   value (8µg/ml). All the isolates showed lower MIC of 0.5µg/ml to 1µg/ml for polymyxin B (Break point MIC for Pseudomonas aeruginosa ≤2µg/ml to ≥8µg/ml) and none of these isolates showed resistant or intermediate MIC values.

Among various mechanisms of resistance, MBL and ESBL enzymes were found to be more effective and the incidence of MBL production in P.aeruginosa has been reported to be 10-30% from different clinical setups in India (26). Recent studies have shown a very high incidence of MBL (47%), AmpC (50%) and ESBL (13.3%) among the MDRPA isolates tested (29). In our study, also we have observed a high prevalence of MBL (39%), ESBL (27%) producers and 22% of MDRPA isolates were found to produce both MBL and ESBL, which appears to be significant. Around 12 % of isolates did not show any of the mechanisms studied which might follow altogether different resistance mechanisms like formation of biofilms and/or cell wall permeability defects and efflux pump mechanisms (27)

High  percentage of biofilm  producers  were  observed   in  our  study,  which  may  be  due  to  the  increase  number  of  MDRPA  isolates encountered. Morten Hentzer et al. earlier reported the strong correlation between biofilm formation and multiple drug resistance in Gram-negative pathogens (29). Thus, biofilm formation appears to be one of the mechanisms among these strains to develop multi drug resistance, which is evident from the earlier reports from India (28).

CONCLUSION

In summary, MDR P. aeruginosa is a notable cause of hospital acquired infections and known to cause a wide spectrum of life threatening diseases. These organisms are resistant to almost all commonly available antibiotics with limited treatment options. Thirty-six percent of isolates showed resistance to imipenem and 53% to meropenem, which is an “alarming sign”, since carbepenems were the present drug of choice. Furthermore, 93% of isolates had the ability to form biofilm that might aid in the persistence of MDRPA thereby imparts resistance.

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Best Article Award

A Study by Badritdinova MN et al. entitled "Peculiarities of a Pain in Patients with Ischemic Heart Disease in the Presence of Individual Combines of the Metabolic Syndrome" is awarded Best Article for Vol 12 issue 24
A Study by Sindhu Priya E S et al. entitled "Neuroprotective activity of Pyrazolone Derivatives Against Paraquat-induced Oxidative Stress and Locomotor Impairment in Drosophila melanogaster" is awarded Best Article for Vol 12 issue 23
A Study by Habiba Suhail et al. entitled "Effect of Majoon Murmakki in Dysmenorrhoea (Usre Tams): A Standard Controlled Clinical Study" is awarded Best Article for Vol 12 issue 22
A Study by Ghaffar UB et al. entitled "Correlation between Height and Foot Length in Saudi Population in Majmaah, Saudi Arabia" is awarded Best Article for Vol 12 issue 21
A Study by Leow Jun Xian and Siti Sarah Binti Maidin entitled "Sleep Well: Mobile Application to Address Sleeping Problems" is awarded Best Article for Vol 12 issue 20
A Study by Avijit Singh et al. entitled "Comparison of Post Operative Clinical Outcomes Between “Made in India” TTK Chitra Mechanical Heart Valve Versus St Jude Mechanical Heart Valve in Valve Replacement Surgery" is awarded Best Article for Vol 12 issue 19
A Study by Sonali Banerjee and Mary Mathews N. entitled "Exploring Quality of Life and Perceived Experiences Among Couples Undergoing Fertility Treatment in Western India: A Mixed Methodology" is awarded Best Article for Vol 12 issue 18
A Study by Jabbar Desai et al. entitled "Prevalence of Obstructive Airway Disease in Patients with Ischemic Heart Disease and Hypertension" is awarded Best Article for Vol 12 issue 17
A Study by Juna Byun et al. entitled "Study on Difference in Coronavirus-19 Related Anxiety between Face-to-face and Non-face-to-face Classes among University Students in South Korea" is awarded Best Article for Vol 12 issue 16
A Study by Sudha Ramachandra & Vinay Chavan entitled "Enhanced-Hybrid-Age Layered Population Structure (E-Hybrid-ALPS): A Genetic Algorithm with Adaptive Crossover for Molecular Docking Studies of Drug Discovery Process" is awarded Best article for Vol 12 issue 15
A Study by Varsha M. Shindhe et al. entitled "A Study on Effect of Smokeless Tobacco on Pulmonary Function Tests in Class IV Workers of USM-KLE (Universiti Sains Malaysia-Karnataka Lingayat Education Society) International Medical Programme, Belagavi" is awarded Best article of Vol 12 issue 14, July 2020
A study by Amruta Choudhary et al. entitled "Family Planning Knowledge, Attitude and Practice Among Women of Reproductive Age from Rural Area of Central India" is awarded Best Article for special issue "Modern Therapeutics Applications"
A study by Raunak Das entitled "Study of Cardiovascular Dysfunctions in Interstitial Lung Diseas epatients by Correlating the Levels of Serum NT PRO BNP and Microalbuminuria (Biomarkers of Cardiovascular Dysfunction) with Echocardiographic, Bronchoscopic and HighResolution Computed Tomography Findings of These ILD Patients" is awarded Best Article of Vol 12 issue 13 
A Study by Kannamani Ramasamy et al. entitled "COVID-19 Situation at Chennai City – Forecasting for the Better Pandemic Management" is awarded best article for  Vol 12 issue 12
A Study by Muhammet Lutfi SELCUK and Fatma COLAKOGLU entitled "Distinction of Gray and White Matter for Some Histological Staining Methods in New Zealand Rabbit's Brain" is awarded best article for  Vol 12 issue 11
A Study by Anamul Haq et al. entitled "Etiology of Abnormal Uterine Bleeding in Adolescents – Emphasis Upon Polycystic Ovarian Syndrome" is awarded best article for  Vol 12 issue 10
A Study by Arpita M. et al entitled "Estimation of Reference Interval of Serum Progesterone During Three Trimesters of Normal Pregnancy in a Tertiary Care Hospital of Kolkata" is awarded best article for  Vol 12 issue 09
A Study by Ilona Gracie De Souza & Pavan Kumar G. entitled "Effect of Releasing Myofascial Chain in Patients with Patellofemoral Pain Syndrome - A Randomized Clinical Trial" is awarded best article for  Vol 12 issue 08
A Study by Virendra Atam et. al. entitled "Clinical Profile and Short - Term Mortality Predictors in Acute Stroke with Emphasis on Stress Hyperglycemia and THRIVE Score : An Observational Study" is awarded best article for  Vol 12 issue 07
A Study by K. Krupashree et. al. entitled "Protective Effects of Picrorhizakurroa Against Fumonisin B1 Induced Hepatotoxicity in Mice" is awarded best article for issue Vol 10 issue 20
A study by Mithun K.P. et al "Larvicidal Activity of Crude Solanum Nigrum Leaf and Berries Extract Against Dengue Vector-Aedesaegypti" is awarded Best Article for Vol 10 issue 14 of IJCRR
A study by Asha Menon "Women in Child Care and Early Education: Truly Nontraditional Work" is awarded Best Article for Vol 10 issue 13
A study by Deep J. M. "Prevalence of Molar-Incisor Hypomineralization in 7-13 Years Old Children of Biratnagar, Nepal: A Cross Sectional Study" is awarded Best Article for Vol 10 issue 11 of IJCRR
A review by Chitra et al to analyse relation between Obesity and Type 2 diabetes is awarded 'Best Article' for Vol 10 issue 10 by IJCRR. 
A study by Karanpreet et al "Pregnancy Induced Hypertension: A Study on Its Multisystem Involvement" is given Best Paper Award for Vol 10 issue 09
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List of Awardees

A Study by Alkhansa Mahmoud et al. entitled "mRNA Expression of Somatostatin Receptors (1-5) in MCF7 and MDA-MB231 Breast Cancer Cells" from Vol 13 issue 06 received Emerging Researcher Award


Awardees of COVID-19 Research

Woman Researcher Award

A Study by Neha Garg et al. entitled "Optimization of the Response to nCOVID-19 Pandemic in Pregnant Women – An Urgent Appeal in Indian Scenario" published in Vol 12 issue 09

A Study by Sana Parveen and Shraddha Jain entitled "Pathophysiologic Enigma of COVID-19 Pandemic with Clinical Correlates" published in Vol 12 issue 13

A Study by Rashmi Jain et al. entitled "Current Consensus Review Article on Drugs and Biologics against nCOVID-19 – A Systematic Review" published in Vol 12 issue 09

Emerging Researcher Award

A Study by Madhan Jeyaraman et al. entitled "Vitamin-D: An Immune Shield Against nCOVID-19" published in Vol 12 issue 09

Study by Dheeraj Kumar Chopra et al. entitled "Lipid-Based Solid Dispersions of Azilsartan Medoxomil with Improved Oral Bioavailability: In Vitro and In Vivo Evaluation" published in Vol 12 issue 19


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