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. 2011 Oct 12;2011:218431. doi: 10.1155/2011/218431

Escherichia coli Isolated from Urinary Tract Infections of Lebanese Patients between 2000 and 2009: Epidemiology and Profiles of Resistance

Ziad Daoud 1,*, Claude Afif 2
PMCID: PMC3263611  PMID: 22295204

Abstract

The purpose of this study was to investigate the bacterial etiology of urinary tract infections in one of the busiest hospitals of Lebanon and to examine the epidemiologic and microbiologic properties of Escherichia coli isolated from urinary tract infections of Lebanese patients over a 10-year period. Methods. This retrospective study analyzed the data generated between 2000 and 2009 (10,013 Gram-positive and Gram-negative bacteria). Bacterial identification was based on standard culture and biochemical characteristics of isolates. Antimicrobial susceptibility was tested by the disk diffusion method, and ESBL production was detected by synergy with third-generation cephalosporins and amoxiclav. Results. E. coli was the most frequent isolate throughout the ten years (60.64% of the total isolates). It was followed by Klebsiella pneumoniae and Proteus sp., Pseudomonas aeruginosa, Enterococcus sp., and Streptococcus agalactiae. E. coli occurred more frequently in women (69.8%) than in men (61.4%). The lowest percentage of susceptibility of E. coli was manifested against piperacillin and ampicillin. An increase in the production of ESBL was observed (2.3% in 2000 to 16.8% in 2009). Conclusions. The etiology of urinary tract infections and their susceptibility profiles are important to be evaluated in countries like Lebanon where a severe misuse of antibiotics at all levels is observed.

1. Introduction

Urinary tract infections (UTIs) are one of the most common infectious diseases [1–3]. They may be symptomatic or asymptomatic, and either type of infection can result in serious sequelae if not appropriately treated [4]. Although different causative agents can be responsible for UTIs, bacteria are the major cause being responsible for more than 95% of UTI cases [5]. In this context, E. coli is the most prevalent organism and is solely responsible for the majority of these infections. An accurate and prompt diagnosis is important in shortening the disease course and for preventing the ascent of the infection to the upper urinary tract [6]. Treatment of UTI is often started empirically. UTIs are often treated with different broad-spectrum antibiotics when one with a narrow spectrum of activity may be appropriate because of concerns about infection with resistant organisms, and antimicrobial susceptibility testing of the urinary pathogens constitutes the basis for antibiotic therapy. However, in view of the increasing bacterial resistance, regular monitoring of resistance patterns is necessary to improve guidelines for empirical antibiotic therapy [6–8]. The present study aims at analyzing the infectious epidemiology of UTIs in a general university hospital located in Beirut over a period of ten years. In addition, it examines the susceptibility profiles of E. coli between 2000 and 2009.

2. Material and Methods

2.1. Study Design

This is a retrospective study conducted at the Microbiology section of the Medical Laboratories of the Saint George Hospital-University Medical Center in Beirut and covering ten years (2000 to 2009). The population included all in- and outpatients with documented UTI. This included 10,013 different Gram-positive and Gram-negative bacteria in addition to Candida albicans and Candida sp. There were 6,708 (66.99%) samples from female patients and 3,305 (33.01%) from male patients. Adult patients were sampled by clean catch midstream urine, and children aged less than 3 years were sampled using sterile urine bags. Only a single positive culture per patient was included in the analysis within the period of three months.

2.2. Isolation and Identification of Organisms

Samples for urine culture were tested within half an hour of sampling. All samples were inoculated on blood agar as well as Mac Conckey agar and incubated at 37°C for 24 hours, and for 48 hours in negative cases. A specimen was considered positive for UTI in the light of the number of yielded colonies (≥105 cfu/mL) and the cytology of the urine through microscopic detection of bacteriuria and PMNs (≥8 leukocytes/mm3). However, lower colony counts associated with significant pyuria or low PMN count associated with significant colony counts was considered and analyzed in the light of the clinical picture and the patient's immunological status. Bacterial identification was based on standard culture and biochemical characteristics of isolates.

Gram-negative bacteria were identified by standard biochemical tests [5, 6]. Gram-positive microorganisms were identified with the corresponding recommended laboratory tests.

2.3. Susceptibility Testing

Antimicrobial susceptibility of E. coli was tested by the disk diffusion method according to the CLSI recommendations, using the Mueller-Hinton agar [6]. Antimicrobial agents tested were ampicillin, amoxicillin-clavulanic acid, aztreonam, cephalothin, cefoxitin, cefuroxime, cefotaxime, ceftriaxone, ceftazidime, cefipime, piperacillin, piperacillin-tazobactam, imipenem, gentamycin, tobramycin, norfloxacin, ciprofloxacin, trimethoprim-sulfamethoxazole, and tetracycline. The CLSI-ESBL phenotypic confirmatory test with ceftazidime, cefotaxime, ceftriaxone, and cefixime was performed for all the isolates by disk diffusion method on the Mueller-Hinton agar plates with and without 10 μg of amoxiclav. Susceptibility test results were interpreted according to the criteria established by the Clinical & Laboratory Standard Institute (CLSI). A minimum of 5 mm increase in the zone of diameter of third-generation cephalosporins, tested in combination with amoxiclav versus its zone when tested alone, was considered indicative of ESBL production. E. coli ATCC 25922 was used as ESBL-negative and K. pneumoniae 700603 was used as ESBL-positive reference strain. Statistical analysis: variables were expressed as percentages.

3. Results

Over a 10-year period, a total of 10,013 positive urine isolates including 6,071 E. coli were analyzed.

Tables 1 and 2 show the microorganisms most frequently isolated from these positive urine cultures. As expected, E. coli was the most frequent isolate throughout the ten years (average of 60.64% of the total isolates). It was followed by Klebsiella pneumoniae where rate of isolation ranged between 6.1 and 9.9%. The next most frequently isolated bacteria were Proteus sp., Pseudomonas aeruginosa, Enterococcus sp., and Streptococcus agalactiae. Candida albicans and Candida sp. were commonly isolated; however, their clinical significance was not always evident. If Candida and minor bacterial isolates are not included, Gram-negative bacteria accounted for 92% of the UTI, while Gram-positive infections were responsible only for 8%.

Table 1.

The organisms most commonly isolated from Lebanese patients with UTI between 2000 and 2004 at Saint George Hospital University Medical Center, Beirut.

The microorganisms most commonly isolated from Lebanese patients with UTI between 2000 and 2004
2000 2001 2002 2003 2004
Nb % Nb % Nb % Nb % Nb %
Acinetobacter sp. 3 0.5 4 0.5 2 0.2 0 0.0 14 1.3
Candida albicans 15 2.4 12 1.6 23 2.4 26 2.4 31 2.9
Candida sp. 16 2.5 22 2.9 28 2.9 47 4.3 34 3.1
Citrobacter sp. 6 0.9 11 1.5 19 2.0 17 1.5 15 1.4
Enterobacter sp. 4 0.6 12 1.6 14 1.5 6 0.5 16 1.5
Enterococcus faecalis 17 2.7 18 2.4 28 2.9 48 4.4 20 1.9
Enterococcus faecium 6 0.9 18 2.4 20 2.1 30 2.7 35 3.2
Escherichia coli 395 62.5 440 58.3 575 59.8 637 57.9 661 61.1
Klebsiella sp. 48 7.6 75 9.9 59 6.1 85 7.7 79 7.3
Morganella morganii 5 0.8 4 0.5 11 1.1 14 1.3 14 1.3
Proteus sp. 45 7.1 50 6.6 72 7.5 74 6.7 65 6.0
Pseudomonas aeruginosa 30 4.7 38 5.0 45 4.7 35 3.2 51 4.7
Pseudomonas sp. 0 0.0 2 0.3 1 0.1 1 0.1 0 0.0
Staphylococcus aureus 3 0.5 6 0.8 3 0.3 7 0.6 9 0.8
Staphylococcus saprophyticus 6 0.9 7 0.9 5 0.5 2 0.2 3 0.3
Streptococcus agalactiae 20 3.2 15 2.0 14 1.5 25 2.3 18 1.7
Streptococcus, Group D 1 0.2 2 0.3 4 0.4 1 0.1 6 0.6
Other minor organisms 12 1.9 19 2.5 38 4.0 45 4.1 10 0.9
Total isolates 632 755 961 1100 1081
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Table 2.

The organisms most commonly isolated from Lebanese patients with UTI between 2000 and 2004 at Saint George Hospital University Medical Center, Beirut.

The microorganisms most commonly isolated from Lebanese patients with UTI between 2005 and 2009
2005 2006 2007 2008 2009
Nb % Nb % Nb % Nb % Nb %
Acinetobacter sp. 19 1.9 14 1.2 18 1.6 16 1.3 5 0.5
Candida albicans 14 1.4 37 3.3 27 2.4 29 2.4 25 2.5
Candida sp. 29 2.9 57 5.1 34 3.0 31 2.6 35 3.5
Citrobacter sp. 15 1.5 18 1.6 19 1.7 16 1.3 9 0.9
Enterobacter sp. 16 1.6 22 2.0 14 1.2 19 1.6 6 0.6
Enterococcus faecalis 14 1.4 15 1.3 20 1.8 14 1.2 15 1.5
Enterococcus faecium 32 3.2 25 2.2 34 3.0 34 2.8 6 0.6
Escherichia coli 609 60.2 711 63.4 688 60.7 727 60.0 628 62.5
Klebsiella sp. 92 9.1 84 7.5 100 8.8 118 9.7 90 9.0
Morganella morganii 13 1.3 6 0.5 10 0.9 24 2.0 7 0.7
Proteus sp. 57 5.6 53 4.7 70 6.2 73 6.0 63 6.3
Pseudomonas aeruginosa 39 3.9 27 2.4 40 3.5 44 3.6 41 4.1
Pseudomonas sp. 0 0.0 6 0.5 0 0.0 6 0.5 3 0.3
Staphylococcus aureus 7 0.7 4 0.4 6 0.5 4 0.3 10 1.0
Staphylococcus saprophyticus 0 0.0 5 0.4 1 0.1 2 0.2 3 0.3
Streptococcus agalactiae 27 2.7 14 1.2 16 1.4 16 1.3 8 0.8
Streptococcus, Group D 1 0.1 1 0.1 1 0.1 0 0.0 1 0.1
Other minor organisms 28 2.8 23 2.0 36 3.2 38 3.1 50 5.0
Total isolates 1012 1122 1134 1211 1005
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Analysis of the results according to patient gender (not shown) indicated that although E. coli is the predominant isolated pathogen from both sexes, it occurred more frequently in women (69.8% in women compared to 61.4% in men.) The trend of infectious etiology in the population did not really differ over the 10-year period.

The percentages of susceptibility (and subsequently of nonsusceptibility including both resistant and intermediately resistant strains) of E. coli isolates to the panel of antibiotics which are commonly used to treat Escherichia infections are shown in Table 3. The lowest percentage of susceptibility was manifested against piperacillin (between 9 and 24%) followed by ampicillin (between 26 and 38%), whereas an absolute susceptibility was observed with imipenem (100%). In general, the urinary isolates showed a slightly better susceptibility profile in comparison to all the hospital isolates of E. coli. Over the successive years, the susceptibility to cephalosporins, including generations 3 and 4, tends to decrease; this is coupled by an increase in the production of ESBL as shown in Table 4 where ESBL production goes from 2.3% in 2000 to 16.8% in 2009 for the urinary isolates.

Table 3.

Susceptibility profiles of urinary and nonurinary isolates of E. coli collected from Lebanese patients between 2000 and 2009 at Saint George Hospital University Medical Center, Beirut.

Percentages of susceptibility of E. coli isolated from Lebanese patients
Year Site of isolation Number Antibacterial Agent
Ampicillin Amox-Clav Aztreonam Cephalothin Cefoxitin Cefuroxime Cefotaxim Ceftriaxone Ceftazidime Cefepime Piperacillin Pipera-Tazo Imipenem Gentamycin Tobramycin Norfloxacin Ciprofloxacin Trimeth-Sulfa
2000 General 620 37 58 95 54 92 89 96 96 95 97 20 93 100 89 88 75 78 51
Urinary 395 38 59 98 57 97 95 96 96 97 99 24 94 100 92 89 88 83 54
Nonurinary 225 35 56 91 52 81 82 95 95 94 96 17 93 100 85 88 59 70 52
2001 General 697 28 56 92 49 91 82 93 93 92 95 18 93 100 89 88 75 78 48
Urinary 440 32 63 94 51 92 88 96 96 97 97 22 94 100 92 89 88 83 51
Nonurinary 257 22 49 91 47 89 74 91 89 87 92 13 91 100 87 86 61 73 45
2002 General 901 30 62 92 60 96 84 94 94 92 96 12 96 100 83 79 64 76 50
Urinary 699 34 69 94 62 97 90 96 97 97 97 16 97 100 86 80 77 81 53
Nonurinary 202 26 54 89 56 93 77 90 91 87 94 7 93 100 81 77 50 73 45
2003 General 1221 28 58 81 54 96 83 83 83 82 83 13 95 100 78 74 60 77 48
Urinary 637 32 65 83 56 97 89 89 90 89 90 17 96 100 81 75 73 82 51
Nonurinary 516 24 50 78 51 94 77 76 80 74 77 10 94 100 75 74 48 72 44
2004 General 1094 28 65 52 59 95 77 82 82 82 82 9 99 100 78 81 62 65 64
Urinary 661 32 72 54 61 96 83 88 89 89 89 13 100 100 81 82 75 70 67
Nonurinary 433 25 59 50 56 93 71 75 75 75 74 7 97 100 78 79 52 63 60
2005 General 998 26 61 53 49 95 76 80 80 80 81 10 98 100 76 99 58 62 51
Urinary 609 30 68 55 51 96 82 86 87 87 88 14 99 100 79 100 71 67 54
Nonurinary 389 24 55 51 48 93 72 75 73 72 74 8 97 100 74 99 51 60 49
2006 General 1072 29 64 79 54 95 80 83 83 83 83 10 99 100 79 99 43 71 49
Urinary 711 33 71 81 56 96 86 89 90 90 90 14 100 100 82 100 56 76 52
Nonurinary 361 25 60 79 55 94 75 79 78 78 78 8 99 100 76 99 39 74 48
2007 General 1049 29 65 81 59 95 78 81 81 81 81 10 99 100 80 99 44 48 47
Urinary 688 34 72 83 61 96 84 87 88 88 88 14 100 100 83 100 57 53 50
Nonurinary 361 23 60 80 58 93 73 78 77 77 77 7 99 100 78 99 36 45 44
2008 General 1098 28 66 77 55 89 73 78 80 80 80 9 99 100 75 93 42 47 45
Urinary 727 30 67 80 55 96 78 82 88 88 89 15 99 100 82 98 62 52 51
Nonurinary 371 25 65 76 54 84 69 75 73 73 73 5 98 100 70 89 39 45 40
2009 General 1011 26 60 79 46 96 76 79 79 79 79 13 98 100 79 99 44 46 47
Urinary 628 31 69 81 47 96 84 86 86 87 53 18 99 100 83 99 63 52 51
Nonurinary 383 23 53 79 45 96 69 74 74 75 80 11 99 100 76 99 35 41 44
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Table 4.

ESBL production in E. coli collected from Lebanese patients between 2000 and 2009 at the Saint George Hospital University Medical Center, Beirut. U: urinary isolates, NU: nonurinary isolates.

ESBL production in E. coli isolated between 2000 and 2009
2000 2001 2002 2003 2004
Isolates All U NU All U NU All U NU All U NU All U NU
Number of isolates 620 395 225 697 440 257 901 699 202 1221 637 584 1094 661 433
% of ESBL 2.3 2.1 2.3 4 3.9 4.3 9.8 9.9 9.5 13.6 14.5 12.1 12.9 11.0 14.1
2005 2006 2007 2008 2009
Isolates All U NU All U NU All U NU All U NU All U NU
Number of isolates 998 609 389 1072 711 361 1049 688 361 1098 727 371 1011 628 383
% of ESBL 20.3 15.7 26.1 17.4 15.6 19.1 19.45 19.2 19.8 19.4 17.1 22.0 18.6 16.8 21.8
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Table 5 shows the susceptibility profiles of ESBL producing E. coli to families of antibiotics other than beta-lactams. Tigecycline, amikacin, and piperacillin-tazobactam seem to have the highest antibacterial activity on these organisms.

Table 5.

Susceptibility profiles of ESBL producing E. coli collected from Lebanese patients between 2005 and 2009 at the Saint George Hospital-University Medical Center, Beirut.

Percentages of susceptibility of ESBL producing E. coli
Antibacterial agent
Year Isolates Amikacin Cefoxitin Gentamycin Pip + Tazo TSM Tigecycline Ciprofloxacin
2005 All 90.5 85.6 29.8 97.6 39.4 ND 21.1
Urinary 92.3 87.6 35.2 97.5 41.1 ND 16.4
Nonurinary 88.2 83.5 25.1 97.8 37.1 ND 17.9
2006 All 97.9 80.7 27.3 93.3 24.1 ND 17.6
Urinary 95.6 84.4 33.5 94.1 40.8 ND 18.8
Nonurinary 98.3 76.9 22.1 93.5 18.9 ND 16.5
2007 All 93.6 81.4 30.1 92.2 23.5 89.6 23.1
Urinary 91.2 87.5 22.4 89.9 36.8 91.2 25.7
Nonurinary 90.2 75.6 36.8 95.4 41.3 93.2 19.1
2008 All 94.2 80.6 27.8 94.1 25.6 87.4 18.8
Urinary 89.1 82.4 24.4 87.9 26.6 91.4 21.1
Nonurinary 97.3 77.1 32.2 98.8 23.9 82.1 15.5
2009 All 93.6 83.4 30.8 94.2 19.5 91.6 19.6
Urinary 94.6 84.5 36.1 96.6 25.4 94.4 19.5
Nonurinary 91.8 82.2 26.3 92.2 10.6 89.9 19.2
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Table 6 shows the percentages of simultaneous resistance in the urinary isolates of E. coli to various families of antimicrobial agents.

Table 6.

Multiple resistance of urinary isolates of E. coli.

Percentage of resistance profiles
Resistance profile of urinary E. coli 2005 2006 2007 2008 2009
Resistant to aminoglycosides and fluoroquinolones 3.2 2.6 3.1 3 3.7
Resistant to 3rd-Generation cephalosporins and fluoroquinolones 3.6 3 4.9 8.2 9.6
Resistant to 3rd-Generation cephalosporins and aminoglycosides 3.9 3.4 3.5 2.5 3.1
Resistant to 3rd-Generation cephalosporins, aminoglycosides, and fluoroquinolones 8.7 9 9.8 13.8 7.3
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4. Discussion

This study shows the distribution of microbial species and antibiotic susceptibility patterns of E. coli isolated from Lebanese patients with UTIs. Saint George Hospital is a 300-bed hospital located in Beirut; however, it is one of the busiest hospitals in the country and receives patients from different areas of Lebanon. In this retrospective study, no clinical data are provided, and this constitutes by itself a limitation. Subsequently, important information related to symptomatic versus asymptomatic, complicated versus uncomplicated UTI, and health-care-associated versus catheter-related UTIs could not be addressed and discussed. The majority of pathogens were isolated from women (69.8%). It has been extensively reported that adult women have a higher prevalence of UTI than men, principally owing to anatomic and physical factors [9].

Antibiotic resistance is a major clinical problem in treating infections caused by these microorganisms. The resistance to the antimicrobials has increased over the years. Resistance rates vary from country to country [10]. In Lebanon, there is an evidence for increase in ESBL producing Enterobacteriaceae. This was previously reported in our hospital as well as in other institutions in the country [11–15]

In this study, E. coli accounted for approximately 61% of all clinically significant urinary isolates and 76.8% of all Enterobacteriaceae. This is consistent with the findings of previous studies in which E. coli was the predominant pathogen isolated from patients with UTIs [16, 17]. The rate of isolation of Klebsiella pneumoniae might be described as high when compared to other studies [16, 17]; however, this can be explained by the fact that our study includes both hospital and acquired UTI.

E. coli isolates from urinary infections show a similar pattern of susceptibility to those isolated from all body site infections although with a more enhanced susceptibility percentages. Aminopenicillins do not constitute a therapeutic option in this population; even the combination amoxicillin-clavulanic acid does not seem to offer important alternative for treatment. In view of the increasing ESBL production, all cephalosporins activities are affected and challenged by these inactivating enzymes. Imipenem remains the only antibiotic with 100% of susceptibility.

It is pretty alarming to note that between 7.3 and 13.8% of the urinary isolates of E. coli show simultaneous resistance to third-generation cephalosporins, aminoglycosides, and fluoroquinolones. A genetic investigation on these isolates should be performed in order to identify the mechanisms of resistance and discover whether they are correlated to each other or independently occurring.

Conflict of Interests

The authors declare that they have no conflict of interests.

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