• Users Online: 628
  • Print this page
  • Email this page


 
 
Table of Contents
ORIGINAL ARTICLE
Year : 2018  |  Volume : 9  |  Issue : 1  |  Page : 11-16

Extended-Spectrum beta-lactamase production and antimicrobial susceptibility pattern of uropathogens in a Tertiary Hospital in Northwestern Nigeria


1 Department of Medical Microbiology, Faculty of Basic Clinical Sciences, College of Health Sciences, Ahmadu Bello University, Zaria, Nigeria
2 Department of Medical Microbiology, Faculty of Clinical Sciences, College of Medicine, Kaduna State University, Kaduna, Nigeria
3 Cluster Coordinator, WHO FCT Office, Abuja, Nigeria
4 Department of Medical Microbiology, Ahmadu Bello University Teaching Hospital, Zaria, Nigeria

Date of Web Publication11-Jun-2018

Correspondence Address:
Fatima Jummai Giwa
Department of Medical Microbiology, Faculty of Basic Clinical Sciences, College of Health Sciences, Ahmadu Bello University, Samaru Zaria, Kaduna State
Nigeria
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/atp.atp_39_17

Get Permissions

  Abstract 

Background: Globally, there is a changing trend in the antibiotic susceptibility pattern of Gram-negative uropathogens to the conventional drugs used in the treatment of urinary tract infections due to the production of extended-spectrum beta-lactamases (ESBLs). Aim: This study aimed to determine ESBL production and antimicrobial susceptibility pattern in uropathogens. Materials and Methods: Five hundred urine samples submitted to the Medical Microbiology Department of Ahmadu Bello University Teaching Hospital from January to June 2012 were analyzed by conventional methods. Modified standardized Kirby-Bauer disc diffusion method was used for antimicrobial susceptibility testing. ESBL production by Escherichia coli and Klebsiella pneumoniae isolates was screened for using the Clinical and Laboratory Standards Institute guidelines 2012 and confirmed by the double-disc synergy tests. Results: Five hundred samples were analyzed. Of these, a total of 175 Gram-negative isolates were obtained. Isolation rates were E. coli – 56%, K. pneumoniae – 20%, Proteus mirabilis – 16%, and Pseudomonas aeruginosa – 4%. ESBL production was observed in 34.3% of all the isolates. Fifty percent (50%) of E. coli and 40% of K. pneumoniae were identified as ESBL producers and were found to be resistant to multiple antimicrobial agents. Imipenem and nitrofurantoin had sensitivity of 100% and 70%, respectively, while susceptibility to ciprofloxacin and gentamicin was low at 35% and 30%, respectively, although 96% sensitivity was observed with amikacin. ESBL producers and nonproducers showed a high level of resistance of over 95% to ampicillin, amoxycillin, and trimethoprim-sulfamethoxazole. Conclusion: This study found a high rate of ESBL production (34.4%) among uropathogens with multidrug resistance. Clinical microbiology laboratories should routinely incorporate ESBL detection methods in their laboratory procedures for continuous surveillance of multidrug-resistant isolates and antibiograms to guide empirical therapy.

Keywords: Antimicrobial susceptibility pattern, extended-spectrum beta-lactamases, northwestern Nigeria, tertiary hospital, uropathogens


How to cite this article:
Giwa FJ, Ige OT, Haruna DM, Yaqub Y, Lamido TZ, Usman SY. Extended-Spectrum beta-lactamase production and antimicrobial susceptibility pattern of uropathogens in a Tertiary Hospital in Northwestern Nigeria. Ann Trop Pathol 2018;9:11-6

How to cite this URL:
Giwa FJ, Ige OT, Haruna DM, Yaqub Y, Lamido TZ, Usman SY. Extended-Spectrum beta-lactamase production and antimicrobial susceptibility pattern of uropathogens in a Tertiary Hospital in Northwestern Nigeria. Ann Trop Pathol [serial online] 2018 [cited 2018 Nov 19];9:11-6. Available from: http://www.atpjournal.org/text.asp?2018/9/1/11/234155


  Introduction Top


Urinary tract infections (UTIs) are among the most common bacterial infections leading patients to seek medical care [1] and are the most common hospital-acquired infections accounting for 40% of nosocomial infections.[2] More than 80% of these infections are attributable to the use of indwelling urethral catheters.[3] The hospital environment plays an important role in determining the organisms involved in UTIs. Hospitalized patients are more likely to be infected with  Escherichia More Details, Klebsiella, Proteus, Staphylococci, Pseudomonas, Enterococci, and Candida spp.[4] These strains are more drug resistant and carry a higher morbidity and mortality index, especially for multidrug-resistant Gram-negative bacteria which produce extended-spectrum beta-lactamases (ESBLs).

Originally, ESBL-producing strains were confined to hospital settings, but lately, these organisms are becoming prevalent in the community,[5] leading to high resistance rates of antimicrobials used in the treatment of UTIs worldwide and the spread of ESBLs.[6],[7]

ESBLs are primarily produced by the Enterobacteriaceae family of Gram-negative organisms with particular reference to Klebsiella pneumoniae, Klebsiella oxytoca, Escherichia coli, and Proteus spp.[6],[8] ESBLs are also found in nonfermentative Gram-negative bacteria, such as Pseudomonas aeruginosa and Acinetobacter baumannii.[9]

ESBLs are enzymes capable of hydrolyzing the penicillins, first-, second-, and third-generation cephalosporins and aztreonam but not the cephamycins or carbapenems and are inhibited by beta-lactamase inhibitors such as clavulanic acid.[7] ESBLs are often located on plasmids that are transferable from strain to strain and between bacterial species.[10]

The prevalence of ESBLs is increasingly being reported worldwide, and it varies according to geographic location and is directly linked to the use and misuse of antibiotics.[11] In Africa, ESBL-producing organisms have been reported in Egypt, Morocco, Tunisia, Senegal, and South Africa.[12] In Nigeria, prevalence rates range from 5% to 44.3% as shown in several studies by Olowe and Aboderin, Yusha'u et al., Akujobi and Ewuru, Mohammed et al., Olonitola et al., and Ogefere et al.[13],[14],[15],[16],[17],[18] in Ogun, Kano, Nnewi, Maiduguri, Zaria, and Benin, respectively. In many parts of the world, 10%–40% of strains of E. coli and K. pneumoniae express ESBLs.[10] The Study for Monitoring Antimicrobial Resistance Trends (SMART) study, conducted in the Asian Pacific in 2007, reported the prevalence of ESBL production in Enterobacteriaceae to be highest in India. ESBL production among E. coli was 79.0%.[19]

Numerous outbreaks of infection due to ESBL-producing organisms have been described on every continent of the globe and pose challenging infection control issues. Some initial outbreaks of infection have been supplanted by endemicity leading to increased patient morbidity and mortality.[20],[21] Incidentally, the laboratory detection of ESBLs can be complex and is not routinely performed in most laboratories.

The presence of ESBLs gives limited therapeutic options for treatment since plasmids responsible for ESBL production simultaneously carry multiple resistant genes to other antimicrobial classes such as aminoglycosides, fluoroquinolones, trimethoprim, chloramphenicol, tetracyclines, and cotrimoxazole giving rise to the development of multidrug resistance.[21],[22]

Currently, the drugs of choice for the treatment of infections caused by ESBL-producing organisms are the carbapenems. The use of carbapenems, however, has also been associated with the emergence of carbapenem-resistant organisms.[10]

Colistin, polymyxin B, tigecycline, and fosfomycin have been shown to have substantial antimicrobial activity against ESBL-producing Enterobacteriaceae and merit further evaluation.[8] Temocillin also showed very promising effects.[23],[24] These drugs are, however, not available in most developing countries.

This study aimed to determine ESBL production in uropathogens and their antibiotic susceptibility pattern in a tertiary health facility in northwestern Nigeria.


  Materials and Methods Top


This was a prospective study conducted on 500 nonrepetitive urine samples submitted to the Medical Microbiology Department of Ahmadu Bello University Teaching Hospital, Shika-Zaria, from January to June 2012 from in-and out-patients with suspected UTI. These samples were processed within 1 h of collection. The ethical committee of the institution approved the study.

Urine microscopy was done using a drop of uncentrifuged urine to determine significant pyuria. The urine sediment was also examined microscopically.[25]

The samples were inoculated on Cysteine Lactose Electrolyte Deficient and Blood Agars and incubated at 37°C for 18–24 h under aerobic conditions. A significant bacteriuria count was also done using a calibrated wire loop on a blood agar plate. Discrete colonies were picked from the plate and a secondary Gram-staining was done. Further identification was done by using standard biochemical tests such as oxidase, motility, triple sugar iron, urease, citrate, and indole tests.[25]

Antimicrobial susceptibility testing

This test was done using the modified Kirby-Bauer disc diffusion method on Mueller-Hinton agar as described by the Clinical and Laboratory Standards Institute (CLSI 2012) guidelines.[26]

The Modified Kirby-Bauer standardized disc diffusion testing was done using the direct colony suspension method. A suspension was made from a 24 h growth of the organism in saline to match the 0.5 McFarland turbidity standard. This was seeded on the entire surface of a Mueller-Hinton agar plate while rotating the plate at an angle of 60° three times. The following antibiotic discs (Oxoid UK) with potencies were used: ceftazidime (30 μg), ceftriaxone (30 μg), ampicillin (30 μg), amoxicillin, nitrofurantoin (300 μg), Augmentin (20 mg amoxicillin and 10 mg clavulanic acid), trimethoprim-sulfamethoxazole (1.25/23.75 μg), gentamicin (10 μg), amikacin (30 μg), imipenem (10 μg), and ciprofloxacin (30 μg). The Mueller-Hinton agar plate was then incubated at (35°C–37°C) in an aerobic atmosphere for 18–24 h, after which the diameter of the zones of growth inhibition around the discs was measured with a ruler. A similar procedure was done using E. coli ATCC 25922 strain and K. pneumoniae ATCC 700603 as negative and positive controls. These results were further interpreted using the Performance Standards for Antimicrobial Susceptibility Testing, CLSI 2012.[26]

Extended-spectrum beta-lactamase screening test

All Gram-negative isolates were subjected to screening tests using ceftazidime (30 μg) and ceftriaxone (30 μg) discs. Those isolates with ceftazidime zone <22 mm and ceftriaxone zone <25 mm were then subjected to confirmatory tests.[26]

Double-disc synergy test

The double-disc synergy test as described by Jarlier et al.[11] was used to confirm ESBL production. Plates were inoculated for routine drug susceptibility using the modified Kirby-Bauer standardized disc diffusion method. Ceftazidime (30 μg) and ceftriaxone (30 μg) discs were placed on either side of co-amoxiclav (20 + 10 μg) 15 mm apart. ESBL-positive strains showed an expansion of the zone of inhibition of either cephalosporin toward the clavulanate giving a dumbbell shape. This expansion occurred because the clavulanic acid present in the Augmentin disc inactivated the ESBL produced by the test organism.

Statistical analysis

Data analysis was carried out using the Statistical Package for the Social Sciences (SPSS) version 20 (Armonk, New York: IBM Corp). Results were presented as charts, tables, and figures as appropriate.


  Results Top


During the study period, a total of 500 urine specimens from patients suspected with UTIs were processed. Most of the patients were females, i.e.,285 (57%), male: female ratio was 1:1.32, while age range was between 1 and 75 years. Majority were outpatients and isolation rates were higher in patients on admission in Intensive Care Unit (ICU) and surgical wards.

Out of the 500 samples, 175 (35%) were characterized as Gram-negatives, 265 (53%) had no growth, mixed growth was seen in 30 (6%) samples, while 40 (8%) were Gram-positives.

Isolation rates were found to be 56%, 20%, 16%, and 8% for E. coli, K. pneumoniae, Proteus mirabilis, and P. aeruginosa, respectively [Figure 1].
Figure 1: Distribution of Gram-negative uropathogens

Click here to view


ESBL production was observed in 34.3% of all the isolates. Fifty percent (50%) of E. coli (46) and 40% (14) of K. pneumoniae were identified as ESBL producers and were found to be resistant to multiple antibiotics.

Antibiotic sensitivity to these ESBL isolates were 100% and 70%, respectively, for imipenem and nitrofurantoin while susceptibility to ciprofloxacin and gentamicin was low at 35% and 30%, respectively, while 96% sensitivity was observed with amikacin. ESBL producers and nonproducers showed a high level of resistance of over 95% to ampicillin, amoxycillin, and trimethoprim-sulfamethoxazole [Figure 2].
Figure 2: Antibiotic susceptibility pattern of ESBL-producing uropathogens

Click here to view



  Discussion Top


The findings in this study showed higher isolation rates in female inpatients compared with males and outpatients. Studies have shown that uncomplicated UTIs usually occur more in females than in males with an increase in age and sexual activity.[27],[28],[29] A study by Ben-Ami et al.[30] which examined risk factors for UTIs caused by ESBLs identified male sex, age >65 years, recent antibiotic use, recent hospitalization, and residence in a long-term care facility as independent predictors of risk of ESBL positivity by multivariate analysis. Similar findings were found in studies by Briongos-Figuero et al.[31] and Sammon et al.[32] which were in contrast to findings in this study.

The predominant isolate in this study was E. coli followed by K. pneumoniae, P. mirabilis, and P. aeruginosa with isolation rates of 56%, 20%, 16%, and 8%, respectively. Literature and several studies on uropathogens showed E. coli as the most frequently isolated uropathogen followed by K. pneumoniae.[33],[34],[35]

ESBL production was observed in 34.3% of all the isolates. This was similar to findings of Bajpai et al., Aggarwal et al., and Babypadmin and Appalaraju [36],[37],[38] where ESBL production was found to be 36.8, 36%, and 39.9%, respectively. Other workers like Ogefere et al., Azekhueme et al., Tankhiwale et al., and Mathur et al.[18],[33],[39],[40] in Calabar, Benin, Nagpur, and New Delhi in India found higher rates of ESBL production of 47.1%, 44.3%, 48.3%, and 58% among Gram-negative isolates. This was, however, in contrast to findings of Akujobi and Ewuru, Mohammed et al., and Khurana et al.[15],[16],[41] in Maiduguri, Nnewi, and India who found lower ESBL production rates of 23.6%, 16%, and 26.6%, respectively.

These observed variances may be attributed to differences in study design and patient selection and differing patterns of antibiotic stewardship in the various centers.[16],[42] Moreover, geographical differences occur in clinical isolates which are also rapidly changing with time.[36]

Fifty percent (46) of E. coli and 40% (14) of K. pneumoniae were identified as ESBL producers and were found to be resistant to multiple antibiotics. This trend has been observed in several studies where ESBL production was found to be highest in E. coli followed by K. pneumoniae.[15],[33],[36],[43] The SMART study which was conducted in the Asian Pacific in 2007 found ESBL production in Enterobacteriaceae to be highest in India (79%) and in E. coli.[19]

The antimicrobial susceptibility pattern to ESBL isolates in this study were 100% and 70%, respectively, for imipenem and nitrofurantoin while susceptibility to ciprofloxacin and gentamicin was low at 35% and 30% respectively, while 96% sensitivity was observed with amikacin.

Carbapenems are regarded as the antibiotic of choice and mainstay of treatment used against infections caused by ESBLs.[7],[8] This is consistent with findings in this study which showed a 100% susceptibility to imipenem which is similar to results from other studies [44],[45] In contrast, resistance to carbapenems has been seen in some strains of K. pneumoniae and E. coli species, in the form of carbapenemases (Klebsiella-producing carbapenemases and New Delhi metallo-β-lactamases). A study by Bajpai et al.[36] showed a high resistance (52.1%) to meropenem, due to the presence of carbapenemase-producing isolates as a result of excessive use of carbapenems in ICUs. A similar study by Gupta et al.[45] also showed a resistance of 22.16% and 17.32% to meropenem and imipenem, respectively, mainly from isolates in ICUs. This is alarming and gives rise to an increasing concern over the judicious use of carbapenems in our health facilities.[46],[47]

The susceptibility pattern of nitrofurantoin on ESBLs was found to be 70% in this study. Nitrofurantoin is a synthetic nitrofuran antimicrobial agent that has been in use for more than 50 years and continues to be effective for the treatment of uncomplicated UTIs in the ambulatory setting.[48] A persisting low prevalence of resistance to nitrofurantoin (1.9%–7.7%) was found among urinary E. coli isolates, including those resistant to trimethoprim-sulfamethoxazole or ciprofloxacin.[48] Surveys in the USA and Canada on E. coli urinary isolates found 1.1% resistance [49] which is similar to the resistance rate in France which was 1.8% among E. coli urinary isolates.[50] The low resistance to nitrofurantoin may be attributed to its ability to achieve very high urine concentrations.[51] Studies done have also found it effective in vitro against E. coli strains, including ESBL producers.[48],[52] This corroborates the findings in this study and that of a study done in Europe where it was found that among 115 clinical isolates of E. coli ESBL producers, 71.3% were sensitive to nitrofurantoin.[53] In a similar vein, a study done in a tertiary care facility in Turkey showed resistance rates of 6.6% and 23.2% in ESBL-negative and ESBL-producing E. coli.[52] These results suggest that nitrofurantoin is a suitable, effective, and cheap alternative drug in the treatment of ESBL-producing E. coli-related lower UTI.[54]

ESBL producers and nonproducers in this study showed a high level of resistance of >95% to ampicillin, amoxycillin, and trimethoprim-sulfamethoxazole which are the routinely used drugs for the treatment of UTIs. This trend was also observed in studies conducted by Manjunath and Aboderin et al.,[55],[56] in India and Nigeria, which suggests that these drugs may no longer be used routinely as empirical treatment ascribed to their widespread use, with resistance developing to such a level that using them would lead to treatment failure.[55],[56]

Susceptibility results of ciprofloxacin and gentamicin seen in this study were low at 35% and 30%, respectively, while 96% sensitivity was observed with amikacin. The quinolones are increasingly becoming resistant due to their excessive use in the treatment of various infections resulting in high selective pressure, prevalent in an environment in which antibiotics are freely available without restrictions.[55],[57] Moreover, resistance to third-generation cephalosporins as exhibited by ESBLs often coexists with resistance to other antibiotics. Such associated resistance was also seen with gentamicin and cotrimoxazole that showed low sensitivities. The sensitivity of amikacin in this study was quite high (96%). Similar studies done have suggested the use of amikacin in cases of drug-resistant Enterobacteriaceae[58],[59] due to its high sensitivity, and it has been found to be generally more active against ESBL-producing and quinolone-resistant E. coli than other aminoglycosides.[59],[60],[61] Due to its property of being refractory to most aminoglycoside-modifying enzymes, amikacin has been successfully used to treat otherwise aminoglycoside-resistant infections, and it is the most widely used semisynthetic aminoglycoside.[62],[63] Results from the SMART study carried out from 2009 to 2011 in the United States [61] indicate that the most effective drug against ESBL-producing uropathogens after the carbapenems is amikacin. A study by Sung-Yeon et al.,[64] which evaluated the outcome of amikacin used as outpatient parenteral antibiotic therapy for UTIs caused by ESBL-producing E. coli, found an 88.9% cure rate while a study by Al Zahrouni et al.[65] showed 100% susceptibility. The benefit derived by patients with the use of amikacin is the attainment of high urinary concentrations because 94%–98% of the unchanged drug is recovered in the urine at 24 h.[66] These findings suggest that amikacin may be a valuable treatment option for ESBL-producing uropathogens.


  Conclusion Top


This study found a high rate of ESBL production (34.4%) in uropathogens with multidrug resistance. Clinical microbiology laboratories should routinely incorporate ESBL detection methods for continuous surveillance of multidrug-resistant isolates and antibiograms to guide empirical therapy. Effective hospital-based infection prevention and control and antibiotic stewardship programs aimed at limiting the spread and emergence of resistant isolates should be instituted in our health-care facilities.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
  References Top

1.
Shakibaie MR, Adeli S, Salehi MH. Antimicrobial susceptibility pattern and ESBL production among uropathogenic Escherichia coli isolated from UTI children in pediatric unit of a hospital in Kerman, Iran. Br Microbiol Res J 2014;4:262-71.  Back to cited text no. 1
    
2.
Kalsi J, Arya M, Wilson P, Mundy A. Hospital-acquired urinary tract infection. Int J Clin Pract 2003;57:388-91.  Back to cited text no. 2
    
3.
Weinstein JW, Mazon D, Pantelick E, Reagan-Cirincione P, Dembry LM, Hierholzer WJ Jr., et al. A decade of prevalence surveys in a tertiary-care center: Trends in nosocomial infection rates, device utilization, and patient acuity. Infect Control Hosp Epidemiol 1999;20:543-8.  Back to cited text no. 3
    
4.
Forbes BA, Sahm DF, Weissfeld AS, editors. Bailey and Scott's Diagnostic Microbiology. International 12th Edition. Philadelphia, USA: Mosby Elsevier; 2007.  Back to cited text no. 4
    
5.
Datta P, Gupta V, Sidhu S. Extended spectrum beta-lactamase positive uropathogenic E. coli – Epidemiological factors and resistance. BJMP 2014;7:a718.  Back to cited text no. 5
    
6.
Bradford PA. Extended-spectrum beta-lactamases in the 21st century: Characterization, epidemiology, and detection of this important resistance threat. Clin Microbiol Rev 2001;14:933-51.  Back to cited text no. 6
    
7.
Pitout JD, Nordmann P, Laupland KB, Poirel L. Emergence of Enterobacteriaceae producing extended-spectrum β-lactamases (ESBLs) in the community. J Antimicrob Chemother 2005;56:52-9.  Back to cited text no. 7
    
8.
Falagas ME, Karageorgopoulos DE. Extended-spectrum beta-lactamase-producing organisms. J Hosp Infect 2009;73:345-54.  Back to cited text no. 8
    
9.
Jacoby GA, Munoz-Price LS. The new beta-lactamases. N Engl J Med 2005;352:380-91.  Back to cited text no. 9
    
10.
Rupp ME, Fey PD. Extended spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae: Considerations for diagnosis, prevention and drug treatment. Drugs 2003;63:353-65.  Back to cited text no. 10
    
11.
Jarlier V, Nicolas MH, Fournier G, Philippon A. Extended broad-spectrum beta-lactamases conferring transferable resistance to newer beta-lactam agents in Enterobacteriaceae: Hospital prevalence and susceptibility patterns. Rev Infect Dis 1988;10:867-78.  Back to cited text no. 11
    
12.
Blomberg B, Jureen R, Manji KP, Tamim BS, Mwakagile DS, Urassa WK, et al. High rate of fatal cases of pediatric septicemia caused by gram-negative bacteria with extended-spectrum beta-lactamases in Dar es Salaam, Tanzania. J Clin Microbiol 2005;43:745-9.  Back to cited text no. 12
    
13.
Olowe OA, Aboderin BW. Detection of extended spectrum beta lactamase producing strains of Escherichia coli and Klebsiella species in a tertiary health centre in Ogun state. Int J Trop Med 2010;5:62-4.  Back to cited text no. 13
    
14.
Yusha'u MM, Aliyu HM, Kumurya AS, Suleiman L. Prevalence of extended spectrum beta-lactamases among Enterobacteriaceae in Murtala Muhammad Specialist Hospital, Kano, Nigeria. Bajopas 2010;3:169-77.  Back to cited text no. 14
    
15.
Akujobi CN, Ewuru CP. Detection of extended spectrum beta-lactamases in gram negative bacilli from clinical specimens in a teaching hospital in South Eastern Nigeria. Niger Med J 2010;51:141-6.  Back to cited text no. 15
  [Full text]  
16.
Mohammed Y, Gadzama GB, Zailani SB, Aboderin AO. Characterization of extended-spectrum beta-lactamase from Escherichia coli and Klebsiella species from North Eastern Nigeria. J Clin Diagn Res 2016;10:DC07-10.  Back to cited text no. 16
    
17.
Olonitola OS, Olayinka AT, Inabo HI, Shuaibu AM. Production of extended spectrum beta lactamases of urinary isolates of Escherichia coli and Klebsiella pneumoniae in Ahmadu Bello University Teaching Hospital, Zaria, Nigeria. Int J Biol Chem Sci 2007;1:181-5.  Back to cited text no. 17
    
18.
Ogefere HO, Aigbiremwen PA, Omoregie R. Extended-spectrum beta-lactamase (ESBL)-producing gram-negative isolates from urine and wound specimens in a tertiary health facility in Southern Nigeria. Trop J Pharm Res 2015;14:1089-94.  Back to cited text no. 18
    
19.
Hawser SP, Bouchillon SK, Hoban DJ, Badal RE, Hsueh PR, Paterson DL. Emergence of high levels of extended-spectrum-{beta}-lactamase producing gram-negative bacilli in the Asia Pacific region: Data from the Study for Monitoring Antimicrobial Resistance Trends (SMART) Program, 2007. Antimicrob Agents Chemother 2009;53:3280-4.  Back to cited text no. 19
    
20.
Paterson DL, Bonomo RA. Extended spectrum β-lactamases: A clinical update. Clin Microbiol Rev 2005;18:657-86.  Back to cited text no. 20
    
21.
Nathisuwan S, Burgess DS, Lewis JS. Extended spectrum β-lactamases: Epidemiology, detection and treatment. Pharmacotherapy 2001;21:920-8.  Back to cited text no. 21
    
22.
Jacoby GA, Sutton L. Properties of plasmids responsible for production of extended spectrum β-lactamases. Antimicrob Agents Chemother 1991;35:164-9.  Back to cited text no. 22
    
23.
Dhillon RH, Clark J. ESBLs: A clear and present danger? Crit Care Res Pract 2012;2012.  Back to cited text no. 23
    
24.
Livermore DM, Warner M, Mushtaq S, Doumith M, Zhang J, Woodford N, et al. What remains against carbapenem-resistant Enterobacteriaceae? Evaluation of chloramphenicol, ciprofloxacin, colistin, fosfomycin, minocycline, nitrofurantoin, temocillin and tigecycline. Int J Antimicrob Agents 2011;37:415-9.  Back to cited text no. 24
    
25.
Winn W Jr., Allen S, Janda W, Koneman E, Procop G, Schreckenberger P, et al., editors. Koneman's Color Atlas and Textbook of Diagnostic Microbiology. 6th ed. Philadelphia, USA: Lippincott Wiilliams and Wilkins; 2006. p. 212-301.  Back to cited text no. 25
    
26.
Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility: Twenty Second Informational Supplement. Vol. 32. Wayne, PA, USA: CLSI; 2012. p. M100-S22.  Back to cited text no. 26
    
27.
Rahn DD. Urinary tract infections: Contemporary management. Urol Nurs 2008;28:333-41.  Back to cited text no. 27
    
28.
Foxman B, Barlow R, D'Arcy H, Gillespie B, Sobel JD. Urinary tract infection: Self-reported incidence and associated costs. Ann Epidemiol 2000;10:509-15.  Back to cited text no. 28
    
29.
Foxman B. Epidemiology of urinary tract infections: Incidence, morbidity, and economic costs. Am J Med 2002;113:5-11S.  Back to cited text no. 29
    
30.
Ben-Ami R, Rodríguez-Baño J, Arslan H, Pitout JD, Quentin C, Calbo ES, et al. A multinational survey of risk factors for infection with extended-spectrum beta-lactamase-producing Enterobacteriaceae in nonhospitalized patients. Clin Infect Dis 2009;49:682-90.  Back to cited text no. 30
    
31.
Briongos-Figuero LS, Gómez-Traveso T, Bachiller-Luque P, Domínguez-Gil González M, Gómez-Nieto A, Palacios-Martín T, et al. Epidemiology, risk factors and comorbidity for urinary tract infections caused by extended-spectrum beta-lactamase (ESBL)-producing enterobacteria. Int J Clin Pract 2012;66:891-6.  Back to cited text no. 31
    
32.
Sammon JD, Sharma P, Rahbar H, Roghmann F, Ghani KR, Sukumar S, et al. Predictors of admission in patients presenting to the emergency department with urinary tract infection. World J Urol 2014;32:813-9.  Back to cited text no. 32
    
33.
Azekhueme I, Moses AE, Abbey SD. Extended spectrum beta-lactamases in clinical isolates of Escherichia coli and Klebsiella pneumoniae from University of Uyo Teaching Hospital, Uyo-Nigeria. J Adv Med Pharm Sci 2005;2:117-25.  Back to cited text no. 33
    
34.
Ramesh N, Sumathi CS, Balasubramanian V, Palaniappan KR, Kannan VR. Urinary tract infections and antimicrobial susceptibility pattern of extended spectrum of beta lactamase producing clinical isolates. Adv Biol Res 2008;2:78-82.  Back to cited text no. 34
    
35.
Gales AC, Sader HS, Jones RN; SENTRY Participants Group (Latin America). Urinary tract infection trends in Latin American hospitals: Report from the SENTRY antimicrobial surveillance program (1997-2000). Diagno Microbiol Infect Dis 2002;44:289-99.  Back to cited text no. 35
    
36.
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.  Back to cited text no. 36
[PUBMED]  [Full text]  
37.
Aggarwal R, Chaudhary U, Sikka R. Detection of extended spectrum β-lactamase production among uropathogens. J Lab Physicians 2009;1:7-10.  Back to cited text no. 37
[PUBMED]  [Full text]  
38.
Babypadmini S, Appalaraju B. Extended spectrum -lactamases in urinary isolates of Escherichia coli and Klebsiella pneumoniae – Prevalence and susceptibility pattern in a tertiary care hospital. Indian J Med Microbiol 2004;22:172-4.  Back to cited text no. 38
[PUBMED]  [Full text]  
39.
Tankhiwale SS, Jalgaonkar SV, Ahamad S, Hassani U. Evaluation of extended spectrum beta lactamase in urinary isolates. Indian J Med Res 2004;120:553-6.  Back to cited text no. 39
    
40.
Mathur P, Kapil A, Das B, Dhawan B. Prevalence of extended spectrum β–lactamase producing gram negative bacteria in a tertiary care hospital. Indian J Med Res 2002;115:153-7.  Back to cited text no. 40
    
41.
Khurana S, Taneja N, Sharma M. Extended spectrum beta-lactamase mediated resistance in urinary tract isolates of family Enterobacteriaceae. Indian J Med Res 2002;116:145-9.  Back to cited text no. 41
    
42.
Krishnakumar S, Rajan RA, Babu MM, Bai VD. Antimicrobial susceptibility pattern of extended spectrum of beta lactamase (ESBL) producing uropathogens from pregnant women. Indian J Med Healthc 2012;1:188-92.  Back to cited text no. 42
    
43.
Sharma M, Pathak S, Srivastava P. Prevalence and antibiogram of extended spectrum β-lactamase (ESBL) producing gram negative bacilli and further molecular characterization of ESBL producing Escherichia coli and Klebsiella spp. J Clin Diag Res 2013;7:2173-7.  Back to cited text no. 43
    
44.
Sasirekha B. Prevalence of ESBL, AMPC B-lactamases and MRSA among uropathogens and its antibiogram. EXCLI J 2013;12:81-8.  Back to cited text no. 44
    
45.
Gupta E, Mohanty S, Sood S, Dhawan B, Das BK, Kapil A, et al. Emerging resistance to carbapenems in a tertiary care hospital in North India. Indian J Med Res 2006;124:95-8.  Back to cited text no. 45
[PUBMED]  [Full text]  
46.
Kumarasamy KK, Toleman MA, Walsh TR, Bagaria J, Butt F, Balakrishnan R, et al. Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: A molecular, biological, and epidemiological study. Lancet Infect Dis 2010;10:597-602.  Back to cited text no. 46
    
47.
Yong D, Toleman MA, Giske CG, Cho HS, Sundman K, Lee K, et al. Characterization of a new metallo-β-lactamase gene, bla, and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrobial Agents Chemother 2009;53:5046-54.  Back to cited text no. 47
    
48.
Hooper D. Urinary tract agents: Nitrofurantoin and methenamine. In: Mandell GL, Bennet JE, Dolin R, editors. Principles and Practice of Infectious Diseases. 6th ed. Philadelphia: Elsevier; 2005. p. 473-8.  Back to cited text no. 48
    
49.
Zhanel GG, Hisanaga TL, Laing NM, DeCorby MR, Nichol KA, Palatnik LP, et al. Antibiotic resistance in Escherichia coli outpatients urinary tract infection isolates: Final results from the North American Urinary Tract Infection Collaborative Alliance (Nautica). Int J Antimicrob Agents 2006;27:468-75.  Back to cited text no. 49
    
50.
Honderlick P, Cahen P, Gravisse J, Vignon D. Uncomplicated urinary tract infections, what about fosfomycin and nitrofurantoin in 2006? Pathol Biol (Paris) 2006;54:462-6.  Back to cited text no. 50
    
51.
Rajesh KR, Mathavi S, Indra RP. Prevalence of antimicrobial resistance in uropathogens and determining empirical therapy for UTI's. Int J Basic Med Sci 2011;1:260-3.  Back to cited text no. 51
    
52.
Pullukcu H, Aydemir S, Tasbakan S, Sipahi OR, Cilli F, Ulusoy S.In vitro efficacy of nitrofurantoin on Escherichia coli strains isolated from urine cultures. Turk J Infect 2007;21:197-200.  Back to cited text no. 52
    
53.
Puerto AS, Fernandez JG, del Castillo J, Pino MJ, Angulo JP.In vitro activity of beta-lactam and non-betalactam antibiotics in extended spectrum beta-lactamaseproducing clinical isolates of Escherichia coli. Diagn Microbiol Infect Dis 2006;54:135-9.  Back to cited text no. 53
    
54.
Tasbakan MI, Pullukcu H, Sipahi OR, Yamazhan T, Ulusoy S. Nitrofurantoin in the treatment of extended-spectrum β-lactamase-producing Escherichia coli-related lower urinary tract infection. Int J Antimicrob Agents 2012;40:554-6.  Back to cited text no. 54
    
55.
Manjunath GN, Prakash R, Vamseedhar A, Shetty K. Changing trends in the spectrum of antimicrobial drug resiatance pattern of uropathogens isolated from hospitals and community patients with urinary tract infections in Tumkur and Bangalore. Int J Biol Med Res 2011;2:504-7.  Back to cited text no. 55
    
56.
Aboderin OA, Abdu AR, Odetoyin BW, Lamikanra A. Antimicrobial resistance in Escherichia coli strains from urinary tract infections. J Natl Med Assoc 2009;101:1268-73.  Back to cited text no. 56
    
57.
Babalola OO, Lamikanra A. Pattern of antibiotic purchases in community pharmacies in South Western Nigeria. J Soc Adm Pharm 2002;19:33-8.  Back to cited text no. 57
    
58.
Craig WA. Optimizing aminoglycoside use. Crit Care Clin 2011;27:107-21.  Back to cited text no. 58
    
59.
Hanberger H, Edlund C, Furebring M, G Giske C, Melhus A, Nilsson LE, et al. Rational use of aminoglycosides – Review and recommendations by the Swedish Reference Group for Antibiotics (SRGA). Scand J Infect Dis 2013;45:161-75.  Back to cited text no. 59
    
60.
Lu PL, Liu YC, Toh HS, Lee YL, Liu YM, Ho CM, et al. Epidemiology and antimicrobial susceptibility profiles of gram-negative bacteria causing urinary tract infections in the Asia-Pacific region: 2009-2010 results from the study for monitoring antimicrobial resistance trends (SMART). Int J Antimicrob Agents 2012;40 Suppl: S37-43.  Back to cited text no. 60
    
61.
Bouchillon SK, Badal RE, Hoban DJ, Hawser SP. Antimicrobial susceptibility of inpatient urinary tract isolates of gram-negative bacilli in the United States: Results from the study for monitoring antimicrobial resistance trends (SMART) program: 2009-2011. Clin Ther 2013;35:872-7.  Back to cited text no. 61
    
62.
Marsot A, Guilhaumou R, Riff C, Blin O. Amikacin in critically ill patients: A Review of population pharmacokinetic studies. Clin Pharmacokinet 2017;56:127-38.  Back to cited text no. 62
    
63.
Ramirez MS, Tolmasky ME. Amikacin: Uses, resistance, and prospects for inhibition. Molecules 2017;22. pii: E2267.  Back to cited text no. 63
    
64.
Sung-Yeon C, Su-Mi C, Sun Hee P, Dong-Gun L, Jung-Hyun C, Jin-Hong Y. Amikacin therapy for urinary tract infections caused by extended spectrum B lactamase producing Escherichia coli. Korean J Internal Med 2016;31:156-61.  Back to cited text no. 64
    
65.
Al-Zarouni M, Senok A, Rashid F, Al-Jesmi SM, Panigrahi D. Prevalence and antimicrobial susceptibility pattern of extended-spectrum beta-lactamase-producing Enterobacteriaceae in the United Arab Emirates. Med Princ Pract 2008;17:32-36.  Back to cited text no. 65
    
66.
Salvatore DJ, Resman-Targoff BH. Treatment options for urinary tract infections caused by extended spectrum B – Lactamase producing Escherichia coli and Klebsiella pneumoniae. Am J Hosp Med 2015;7.  Back to cited text no. 66
    


    Figures

  [Figure 1], [Figure 2]



 

Top
 
  Search
 
    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Access Statistics
    Email Alert *
    Add to My List *
* Registration required (free)  

 
  In this article
Abstract
Introduction
Materials and Me...
Results
Discussion
Conclusion
Introduction
Materials and Me...
Results
Discussion
Conclusion
References
Article Figures

 Article Access Statistics
    Viewed796    
    Printed91    
    Emailed0    
    PDF Downloaded154    
    Comments [Add]    

Recommend this journal