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  Table of Contents    
Year : 2014  |  Volume : 57  |  Issue : 3  |  Page : 407-412
Prevalence of extended spectrum beta-lactamase producing uropathogens and their antibiotic resistance profile in patients visiting a tertiary care hospital in central India: Implications on empiric therapy

1 Department of Microbiology, Sri Aurobindo Institute of Medical Sciences Medical College and PG Institute, Indore, Madhya Pradesh, India
2 Department of Biochemistry, IGNOU, New Delhi, India
3 Department of Biochemistry, Sri Aurobindo Institute of Medical Sciences Medical College and PG Institute, Indore, Madhya Pradesh, India

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Date of Web Publication14-Aug-2014


Context: Antimicrobial resistance showed by different uropathogens is one of the barricades that might hinder a successful treatment. Detection of extended spectrum beta-lactamase (ESBL) production among uropathogens is an important marker of endemicity. Aims: The present prospective study was done to identify the trends of uropathogens, to find the prevalence of ESBL isolates and to study the antibiotic resistance profile of the ESBL and non-ESBL uropathogenic isolates. Materials and Methods: This study was conducted in the Department of Microbiology of a teaching tertiary care hospital from July 2013 to September 2013. All the uropathogenic isolates were identified up to species level by conventional methods. The prevalence of potential ESBL producers was explored. Antibiotic resistance test of the urinary isolates was done by disc-diffusion method and the results were interpreted according to Clinical Laboratory Standards Institute-2013 guidelines. Results: A total of 670 urine samples from male and female patients visiting the outpatient department (OPD) and inpatient department (IPD) of our hospital were collected. A significantly higher number of IPD and OPD males (55.1% and 55.5%) were found to be culture positive. Escherichia coli (55.3%) was the most frequently isolated uropathogen followed by Klebsiella pneumoniae (23%). However, strains of Escherichia coli (41.6%) were the highest ESBL producing isolates followed by Pseudomonas aeruginosa (36.1%). ESBL producing isolates were found to be multidrug-resistant when compared to non-ESBL producers. However, excessive drug-resistance among non-ESBL producing isolates can't be ignored. Conclusion: Our study confirms a global trend toward increased resistance to beta-lactam antibiotics. We emphasize on the formulation of antibiotic policy for a particular geographical area.

Keywords: Beta-lactam antibiotics, extended spectrum beta-lactamase, uropathogens

How to cite this article:
Bajpai T, Pandey M, Varma M, Bhatambare GS. Prevalence of extended spectrum beta-lactamase producing uropathogens and their antibiotic resistance profile in patients visiting a tertiary care hospital in central India: Implications on empiric therapy. Indian J Pathol Microbiol 2014;57:407-12

How to cite this URL:
Bajpai T, Pandey M, Varma M, Bhatambare GS. Prevalence of extended spectrum beta-lactamase producing uropathogens and their antibiotic resistance profile in patients visiting a tertiary care hospital in central India: Implications on empiric therapy. Indian J Pathol Microbiol [serial online] 2014 [cited 2023 May 31];57:407-12. Available from:

   Introduction Top

Extended spectrum beta-lactamase (ESBL) producing organisms are those that hydrolyze the oxyimino beta-lactams and monobactams, but have no effect on the cephamycins and carbapenems. [1] They are increasing rapidly and becoming a major problem in the area of infectious diseases. Problems associated with ESBL producing isolates are difficult to be detected or treated, thereby causing increased mortality of patients. [2] The prevalence of ESBL producing organisms among clinical isolates vary greatly worldwide and is rapidly changing over time. ESBL producers have been steadily increasing after their initial detection in the mid 1980's in Western Europe. The outbreaks of infection in various hospitals globally have been supplanted by endemicity of ESBL producers. This may lead to increased patient mortality when antibiotics inactive against ESBL producers are used. [3] Unfortunately, the ESBL producers often also have resistance determinants to other antibiotic groups, leaving an extremely limited range of effective agents. A delay in appropriate therapy can cause severe complications. [1] Detection of ESBL producers from sample such as urine may be of utmost importance because this represents an epidemiologic marker of colonization and therefore there is potential for transfer of such organisms to other patients. [3] The rapid increase of resistance to broad spectrum beta lactams among uropathogens has recently become a major problem globally. It leads to antibiotic ineffectiveness, increased severity of illness and cost of treatment. [4] The serious increase in the prevalence of ESBL's worldwide creates a need for effective and easy to perform screening methods for detection. [5]

This study was designed to identify the changing etiological trends of urinary tract infections (UTI), detect the prevalence of ESBL producing uropathogens and study their antibiotic resistance profile.

   Materials and methods Top

The present prospective study was carried out from July 2013 to September 2013 in the Department of Microbiology of a teaching tertiary care hospital. The study protocol was approved by the Institutional Ethical Committee. A total of 670 non-repetitive (midstream, catheterized, supra-pubic, and nephrostomy) urine samples were collected in sterile containers. The samples were processed within 1 h of collection. Semi-quantitative culture of urine was done by a calibrated loop method [6] on a UTI chromogenic media [7] The culture plates were incubated at 37°C for 18-24 h under aerobic conditions. Identification of bacterial growth was confirmed by standard microbiological and biochemical techniques. [6],[8]

Antibiotic sensitivity testing (AST) was performed by the Kirby-Bauer disc-diffusion method on Mueller-Hinton agar. [9] For this test, a culture medium, specifically the Mueller-Hinton agar, was uniformly and aseptically inoculated with the test organism and then filter paper discs, which were impregnated with a specific concentration of a particular antibiotic, were placed on the medium. If the organism was susceptible to a specific antibiotic, there was no growth around the disc containing the antibiotic. Thus, a "zone of inhibition" was observed and measured to determine the susceptibility to an antibiotic for that particular organism. The following antibiotics were tested: Amikacin (30 mcg), gentamycin (10 mcg), ampicillin (10 mcg), piperacillin (100 mcg), ticarcillin (75 mcg), levofloxacin (5 mcg), norfloxacin (10 mcg), nitrofurantoin (300 mcg), tetracycline (30 mcg), co-trimoxazole (1.25/23.75 mcg), aztreonam (5 mcg), cefazolin (30 mcg), cefotaxime (30 mcg), ceftazidime (30 mcg), cefepime (30 mcg), cefoxitin (30 mcg) piperacillin-tazobactum (100/10 mcg), colistin (10 mcg), imipenem (10 mcg) and meropenem (10 mcg). Dehydrated media and antibiotic discs were procured from Hi-Media, Mumbai, India. The control strains used during the study were Escherichia coli ATCC 25922 and Pseudomonas aeruginosa ATCC 27853. The selection of antibiotics and interpretation of inhibition zone sizes was done according to Clinical Laboratory Standards Institute-2013 guidelines. [10]

Extended spectrum beta-lactamase confirmatory tests were also included in the routine susceptibility test. [11] While performing AST, ceftazidime plus clavulanic acid (30/10 mcg) and cefotaxime plus clavulanic acid (30/10 mcg) discs were also included along with ceftazidime (30 mcg) and cefotaxime (30 mcg) discs on Muller-Hinton agar. Organism was considered as ESBL producer if there was an increase of ≥5 mm in the zone diameter of ceftazidime/clavulanic acid disc with respect to that of ceftazidime disc alone and or ≥5 mm increase in the zone diameter of cefotaxime/clavulanic acid disc with respect to that of cefotaxime disc alone. Escherichia coli 25922 and a known in-house ESBL producer were used as negative and positive controls respectively [Figure 1]. Once the ESBL producers were isolated, their antibiotic resistance profile were prepared and evaluated.
Figure 1: Phenotypic expression of extended spectrum beta-lactamase production (zone sizes of cefotaxime(ctx)/clavulanic acid(cac) and ceftazidime(ctz)/clavulanic acid(cec) ≥5 mm. than the zone sizes of cefotaxime and ceftazidime respectively)

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   Results and discussion Top

A total of 670 urine samples were collected from male and female patients visiting the outpatient departments (OPD) and inpatient departments (IPD) of a teaching tertiary care hospital [Table 1]. Significant bacteriurea was observed in 257 samples (38.3%) from which a total of 281 uropathogenic isolates were identified. This was because 24 samples were detected to bear two pathogens which were again confirmed by testing the second sample. Out of 281 isolates, 217 (77.2%) isolates were characterized as Gram-negative, 29 (10.32%) were characterized as Gram-positive while 35 (12.4%) were identified as Candida species. Among the 217 Gram-negative isolates, 80 (36.8%) were found to be ESBL producers [Table 2].
Table 1: Gender-wise and department-wise distribution of uropathogens

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Table 2: The various uropathogenic isolates and distribution of ESBL's among various GN isolates

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In our study, 356 (53.1%) male patients were suspected of UTI as compared to 314 (46.8%) female patients. Furthermore, more male patients that is, 142 (39.8%) were found to be culture positive as compared to 115 (36.6%) female patients. In our case, 460 (68.6%) IPD samples were collected as compared to 210 (31.3%) OPD samples. Furthermore, more IPD samples that is, 194 (42.1%) were found to be positive as compared to 63 (30%) OPD samples. Also more IPD and OPD males that is, 107 and 35(55.1% and 55.5%) were found to be positive as compared to 87 and 28 (44.8% and 44.4%) IPD females, respectively. The difference was significant between male and female positive cases but was not influenced by, whether it is from IPD or OPD. The findings were against the studies made by Sasirekha, Manjunath et al. and Sood and Gupta. [12],[13],[14]

Of the total 281 uropathogen isolates, Escherichia coli was found in maximum number of isolates that is, 120 (42.7%) followed by Klebsiella pneumoniae (50 [17.7%] and P. aeruginosa (26 [9.2%] with no significant differences in both male and female patients. However, few rare pathogens like Proteus mirabilis, Providencia rettgeri , Acinetobacter baumanii, Enterobacter cloacae, and Morganella morganii were isolated only from male patients. This may be because more males were IPD patients and would have acquired UTI nosocomially. Non-Escherichia coli infections are common in complicated UTI's involving structural abnormalities of urinary tract, diabetes or in case of catheterization. This can be correlated to more culture positive male IPD patients in our study. [15]

In the current study, 120 (55.3%) of the 217 Gram-negative isolates were identified as Escherichia coli followed by 50 (23%) K. pneumoniae and 26 (16.5%) P. aeruginosa. Of these, maximum ESBL isolates were among Escherichia coli that is, 50 (41.6%) followed by P. aeruginosa (13 [36.1%] and K. pneumoniae (13 [26%]. Most of the studies have also revealed that Escherichia coli as the most frequently isolated uropathogen followed by Klebsiella [12],[16],[17],[18],[19] However, in our case, P. aeruginosa has been found to be a second most frequent ESBL producer unlike studies of Sasirekha, Aruna and Mobashshera et al., Gales et al. and Mathur et al. Our study resembles that of Ramesh et al. who reported P. aeruginosa as the second most frequent ESBL producer followed by Klebsiella. [16]

Our study reported 36.8% ESBL producers unlike the studies made by Khurana et al. (26.6%) and Tankhiwale et al. (48.3%). [20],[21] Our study reported 41.66% Escherichia coli ESBL isolates resembling those reported by Kumar et al. (39%) and Taneja et al. (40.2%) [22],[23] and unlike those reported by Ramesh et al. (60.7%), Aruna and Mobashshera (49.32%), Tankhiwale et al. (49.8%), Singhal et al. (62%), Kesavaram et al. (59.1%), Maya et al. (75.5%) and Gururajan et al. (47%). [16],[17],[21],[24],[25],[26],[27] The reports presented by different authors clearly indicate that the prevalence of ESBL producing organisms among clinical isolates vary greatly geographically and rapidly changing over time. [2],[28]

Antibiotic resistance showed by different uropathogens is one of the barricades that might hinder a successful treatment. Widespread antibiotic usage exerts a selective pressure that acts as a driving force in the development of antibiotic resistance. The detailed insight of antibiotic resistance pattern has been illustrated in [Figure 2]. Constant survey of antibiotic resistance plays a very important role in empiric treatment of UTI.
Figure 2: Graphical representation of the antibiotic resistance profile of various extended spectrum beta-lactamase (ESBL) and non-ESBL uropathogenic isolates

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The antibiogram of the Gram-negative isolates revealed that the ESBL producers possessed a high degree of resistance toward antibiotics that are routinely prescribed against UTI's as compared to non-ESBL producing isolates. These findings are similar to those reported by other authors like Sasirekha, Ndugulile et al. and Mehrgan et al. [12],[29],[30] This observation can be explained by the fact that ESBL are plasmid-mediated enzymes, which are transferable between one bacterium to another and such transferable plasmids also code for resistance determinants to antimicrobial agents other than beta-lactams. [31]

A low degree of resistance to amikacin (12.5% and 36.8%) and gentamycin (31.3% and 51.5%) (aminoglycoside drug) was observed for both ESBL and non-ESBL producers respectively and hence may be helpful in combating severe infections. [12],[32] Aminoglycosides being injectables are used restrictively in the community care setting and hence have showed lesser resistance rates. [14]

Resistance to antibiotics like ampicillin (100% and 85.3%), piperacillin (89.6% and 70.6%) and co-trimoxazole (98% and 78%) among ESBL producers and nonproducers, respectively has been developed to such a level that prescribing them would lead to treatment failure. This can be predicted due to their widespread use. [13]

An individual is at a significantly higher risk of being infected by ESBL producing uropathogens if he/she is exposed to antibiotics for a long period, suffers from serious illness, undergoes instrumentation or catherization or is a resident of nursing home or an institute which frequently use third generation cephalosporins. [32] Under such circumstances fluoroquinolenes become a drug of choice. Higher rate of resistance exhibited by ESBL producers and non-producers, respectively toward oral antibiotics, like norfloxacin (83.4% and 78%) and levofloxacin (68.8% and 73.6%) in our study indicated an increased quinolone resistance in our institute. This finding is consistent with previous studies. [13],[33] Since, they are ubiquitously prescribed, it accounts for the emergence of resistance against them. Fluoroquinolones show varied side effects when prescribed in high doses; hence, its extensive use should be avoided. Our findings indicate that urgent strategies to counteract increased resistance to these drugs must be developed or their use in uncomplicated infections should be strictly curtailed.

Another oral antibiotic nitrofurantoin (31.3% and 51.5% resistance among ESBL and non-ESBL's) was found to be more effective in treatment of UTI in our case and the findings are in agreement with similar surveillance studies by Sasirekha and Khameneh [12],[34] and other Indian studies, which have demonstrated nitrofurantoin as an appropriate agent for first line treatment of community-acquired UTI. [14] Low antimicrobial resistance for nitrofurantoin can be attributed to its localized action on urinary tract and not being exposed outside urinary tract. [35]

Resistance to piperacillin-tazobactum (27.1% and 41.2% resistance among ESBL and non-ESBL's) was low in our case, probably reflecting their low usage for treatment of community-acquired infections. Not only ESBL producing isolates (resistance towards cefazolin, cefotaxime, ceftazidime, cefepime and aztreonam in the range of 89-94%) but also ESBL nonproducers (cefazolin: 78%; cefotaxime: 67.7%; ceftazidime: 72.1%; cefepime: 69.2%; aztreonam: 67.7%) exhibited high degrees of resistance toward third and fourth generation cephalosporins and mono-bactam. Such findings are attributed to excessive use of antibiotics in both community and hospital settings, uncontrolled prescription practices and incomplete dosage consumption by patients.

Resistance to imipenem, which is used as last resort drugs in the health-care settings was found to be 6.3% and 17.7% among ESBL producers and non-producers, respectively. Resistance to meropenem (52.1% and 55.9% exhibited by ESBL and non-ESBL producers respectively) in our study is quite alarming. Carbapenem resistance is usually multifactorial. Resistance to carbapenems occurs through bacterial production of beta-lactamase enzymes that hydrolyze the antibacterial agent or through porin changes in the bacterial cell wall that reduce the permeability of the drug into the organism. In addition, upregulation of efflux pumps result into reduced susceptibility of organisms toward meropenem. [36] Most studies showed 100% sensitivity toward imipenem. [17],[28],[37],[38] Incidences of meropenem resistance higher than that of imipenem among nosocomial pathogens was observed by Gupta et al. [39] The resistance exhibited in our case is due to existence of carbapenemase producing isolates in our setting. This may be because patients in Intensive Care Unit are directly being treated with carbapenems that has led to development of such multidrug-resistant isolates in our health-care setting.

The sensitivity pattern of microorganisms to various antibiotics varies over time and among different geographical locations. Therefore, continuous analysis of the antibiotic resistance pattern acts as a guide in initiating the empirical treatment of UTI and the therapy must be started only after the gold-standard test like urine culture and sensitivity have been done. It helps in avoiding the treatment failure and rapid dissemination of the antibiotic resistance and its mechanism can be prevented. Our study suggests amikacin to be prescribed as the empirical treatment for UTI in hospital and nitrofurantoin in case of community-acquired infections. We advocate that carbapenem should be used as a last line antibiotic to prevent occurrence of carbapenem resistance. Hence, they should not be given for empirical treatment. Since the advent of new mighty drugs is highly difficult, proper use of currently available antimicrobial agents should be initiated.

   Acknowledgment Top

The authors would like to thank the Chairperson and Dean of the institute for providing laboratory facilities and healthy working atmosphere during the study period. The authors are also thankful to the technical staff of the institute for providing necessary helping hand during the endeavor.

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Correspondence Address:
Trupti Bajpai
Asst. Prof., Department of Microbiology, Sri Aurobindo Institute of Medical Sciences Medical College and PG Institute, MR-10 Crossing, Indore-Ujjain Highway, Indore, Madhya Pradesh
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0377-4929.138733

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