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 Table of Contents  
ORIGINAL ARTICLE
Year : 2014  |  Volume : 27  |  Issue : 2  |  Page : 440-446

Prevalence of quinolones resistance among patients with urinary tract infection at Menoufia


Department of Clinical Pathology, Faculty of Medicine, Menoufia University, Menoufia, Egypt

Date of Submission28-Nov-2013
Date of Acceptance06-Feb-2014
Date of Web Publication26-Sep-2014

Correspondence Address:
Rasha Rashed Mohamed
MBBCh, Department of Clinical Pathology, Faculty of Medicine, Menoufia University, El Bagour, Menoufia
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1110-2098.141724

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  Abstract 

Objective
The aim of the study was to examine the prevalence of quinolone resistance and determine appropriate empiric antibiotics for patients with urinary tract infection (UTI).
Background
UTI is the most common disease of the urinary tract and it is a major cause of morbidity in both hospitals and communities. Most infections arise from Escherichia coli. Quinolones are effective for treatment of UTIs. Therapy against infectious diseases with antimicrobial agents such as quinolones is very dynamic, with high probability for bacterial resistance.
Patients and methods
This study was carried out on 150 patients (80 patients suffering from UTI with positive bacterial growth; 55 patients with mixed growth; and 15 patients with Candida). All studied patients with positive bacterial growth were submitted to complete history taking, clinical examination, urine analysis, biochemical tests, bacterial count, urine culture, and antimicrobial sensitivity of all isolates to quinolone drugs (nalidixic acid, ciprofloxacin, levofloxacin, ofloxacin, and gatifloxacin).
Results
In this study 80 (53%) patients had positive urine culture (54% male and 46% female). The most commonly isolated bacterium was E. coli (52.5%). Individuals over the age of 50 years were more frequently affected by UTI. The sensitivity of male and female patients to ciprofloxacin and levofloxacin showed a highly statistically significant difference (P < 0.001) for each, and sensitivity to ofloxacin, gatifloxacin, and nalidixic acid showed a statistically significant difference (P<0.05). In catheterized patients, prevalence of infection with Enterobacter spp. and Citrobacter spp. was higher, whereas in noncatheterized patients infection with E. coli, Gram-positive cocci, and Klebsiella spp. was high. Antibiotic sensitivity of the isolated pathogens was ascertained, which showed that gatifloxacin was the most effective antibiotic against pathogens and nalidixic acid was the least effective.
Conclusion
UTI is a serious health problem. Random use of quinolones in UTI should be discouraged because of increased antimicrobial resistance.

Keywords: Bacterial resistance, Escherichia coli, quinolones resistance, risk factors, urinary tract infection


How to cite this article:
Kandel SH, El-Hendy AA, Mohamed RR. Prevalence of quinolones resistance among patients with urinary tract infection at Menoufia. Menoufia Med J 2014;27:440-6

How to cite this URL:
Kandel SH, El-Hendy AA, Mohamed RR. Prevalence of quinolones resistance among patients with urinary tract infection at Menoufia. Menoufia Med J [serial online] 2014 [cited 2019 Nov 12];27:440-6. Available from: http://www.mmj.eg.net/text.asp?2014/27/2/440/141724


  Introduction Top


Urinary tract infection (UTI) is the most common disease of the urinary tract and it is a major cause of morbidity in both hospitals and communities. The most common causes of UTI are bacteria such as  Escherichia More Details coli, Staphylococcus saprophyticus, Klebsiella spp., Proteus spp., and Pseudomonas spp. Viruses, yeast, and intracellular microorganisms were less common causes [1].

UTI could be defined as the persistent presence of actively multiplying microorganisms in the urinary tract. It is an infection with more than 100 000 organisms per milliliter in midstream urine samples [2].

UTI is prevalent among men and women, but is more in women especially during pregnancy. Unrecognized UTI in infancy and childhood may have serious long-term effects, and chronic pyelonephritis may occur in adults [3].

The WHO has called antibiotic resistance an emerging disease. The rapid spread of bacterial resistance to antimicrobial agents has led to the search for newer and more potent drugs. Abuse of new drugs causes bacterial resistance. An extensive research confirms that fluoroquinolones are extremely effective for the treatment of UTIs ranging in severity from uncomplicated cystitis to urosepsis [4].

Therapy for infectious diseases with antimicrobial agents such as quinolones is very dynamic and increases the probability of bacterial resistance to antimicrobial agents. Hence, most bacterial infections become more difficult to treat [5].

Urinary catheterization and prior quinolone exposure are associated with a high risk for quinolone resistance. Hence, urine culture and susceptibility testing should be performed to guide definitive therapy for UTI [6].


  Patients and methods Top


Data collection and patients

This study was carried out at the Clinical Pathology Department, Faculty of Medicine, Menoufia University, between July 2011 and July 2012. A total of 150 patients from all age groups suffering from UTI were included in the study, comprising 43 (54%) men and 37 (46%) women. All individuals were subjected to complete history taking and clinical examination.

Microbiological laboratory methods

Midstream urine samples were obtained from the studied patients in sterile containers after instructing them to clean the genital area with soap and tap water. Morning urine samples were obtained whenever possible; in case of catheterized patients, the urine samples were collected after 30 min of clamping the catheter, through a syringe and needle inserted proximal to the site of clamping under aseptic precautions. Urine samples were examined either immediately (within 2 h) or, if not possible, refrigerated at 4°C to be examined within 24 h [7].

Macroscopic examination of urine for its color, turbidity, or frank hematuria was carried out.

Microscopic examination of one loopful of uncentrifuged urine was examined directly without staining using ×10, ×40 lens for the presence of pus cells. Detection of one white blood cell/low-power field corresponds to 3 cells/ml [8].

A drop of uncentrifuged urine was transferred to a slide and spread to make a thin smear; it was allowed to dry, heat fixed and Gram stained. Microscopic examination was conducted first using a ×40 objective lens to see the distribution of material and then with oil immersion objective. Detecting one organism in uncentrifuged urine/oil immersion field indicates UTI (i.e. bacteriuria in excess of 10 5 /ml) [8].

Urine samples were cultured on appropriate media, MacConkey agar or cysteine lactose electrolyte deficient agar plates, and incubated at 37°C for 24-48 h with 0.001 ml calibrated loops. After incubation, the colonies in the plates were counted. The presence of 100 or more colonies was considered as significant bacteriuria; then further identification by colony morphology, Gram-staining films, and biochemical reactions was done [9].

Antimicrobial susceptibility was determined by the disc-diffusion method using Mueller-Hinton agar plates. The antibiotics tested for susceptibility included quinolones (nalidixic acid, ciprofloxacin, ofloxacin, levofloxacin, and gatifloxacin). The diameters of the zones of inhibitions were then measured. Susceptibility (sensitive, intermediate, or resistance) was determined using the British Society for Antimicrobial Chemotherapy [10].

Statistical analyses

Data were analyzed using the SPSS (version 11.0; SPSS Inc., Chicago, Illinois, USA) statistical package.

Quantitative data were expressed as mean ± SD. Qualitative data were expressed as number and percentage and analyzed by the c2 -test. The Student t-test was used for the normally distributed variables and the Mann-Whitney U-test for non-normally distributed variables. All these tests were used as tests of significance at P value less than 0.05.


  Results Top


The studied patients comprised 85 (57%) male and 65 (43%) female. The ages ranged from 4 to 80 years with mean age ± SD of 46.9 ± 16.0 [Table 1].
Table 1: Characteristics of the studied group

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There were 80 patients whose urine cultures showed pure growth; 43 samples were from male patients and 37 from female patients. Patients' ages ranged from 4 to 80 years with a mean age ± SD of 47.7 ± 17.4. There were 55 (69%) midstream samples and 25 (31%) catheter samples. Of the organisms isolated, E. coli growth was seen in 42 (52.5%) patients, Enterobacter spp. in 12 (15%), Klebsiella spp. in seven (8.8%), Gram-positive cocci in seven (8.8%), Citrobacter spp. in four (5%), Pseudomonas spp. in four (5%), Proteus spp. in three (3.8%), and Shigella spp. in one (1.3%) patient [Table 2].
Table 2: Characteristics of the group with pure growth

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A total of 80 patients were studied, falling within the age groups of less than 20, 20-50, and more than 50 years. Age distribution showed that UTI most commonly affected persons aged more than 50 years (42 patients, 52.5%), which was followed by persons aged 20-50 years (32 patients, 40%) and patients less than 20 years (six patients, 7.5%) [Table 3].
Table 3: The percentage of the incidence rate of urinary tract infection according to age and sex

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There was a statistically nonsignificant difference between male and female patients regarding the rate of infection of the isolated organisms (P > 0.05) [Table 4].
Table 4: Comparison between male and female patients according to isolated organisms

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Sensitivity to ciprofloxacin and levofloxacin between male and female patients showed a highly statistically significant difference (P < 0.001) for each, and sensitivity to ofloxacin, gatifloxacin, and nalidixic acid showed a statistically significant difference (P < 0.05) [Table 5].
Table 5: Comparison between male and female patients regarding their sensitivity and resistance to different types of quinolone drugs

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Type of samples (midstream or catheter) showed a statistically nonsignificant difference when compared on the basis of sex (P > 0.05), whereas there was a statistically significant difference when compared on the basis of the different organisms isolated from the urine cultures (P < 0.05) [Table 6].
Table 6: Comparison between types of samples (midstream or catheter) with respect to isolated organisms

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Sensitivity and resistance to different types of quinolone drugs showed a nonsignificant statistical difference when compared on the basis of type of samples (midstream or catheter) in patients with UTI (P > 0.05) [Table 7].
Table 7: Comparison between type of samples (midstream or catheter) regarding sensitivity and resistance to different types of quinolone drugs

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Comparing sensitivity and resistance to different types of quinolone drugs in patients with UTI was nonsignificant statistical difference (P > 0.05) [Table 8].
Table 8: Summary of results of sensitivity/resistance profiles of all quinolone drugs

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E. coli exhibited the highest resistance to all quinolones. Among quinolone drugs, nalidixic acid was the least efficient in preventing the growth of UTI pathogens, whereas gatifloxacin was the most potent [Table 9].
Table 9: Summary of sensitivity and resistance profiles of all identified bacterial isolates to the quinolones

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  Discussion Top


UTI is a serious health problem affecting millions of people each year. Infections of the urinary tract are the second most common type of infections in the body. Most infections arise from E. coli [11].

Antibiotics are the mainstay treatment for all UTIs. A variety of antibiotics are available and choices depend on many factors, including whether the infection is complicated, uncomplicated, primary, or recurrent. Treatment decisions are also based on the type of patient (e.g. man or woman, pregnant or nonpregnant, child, hospitalized or nonhospitalized patient, presence of diabetes) [12].

Fluoroquinolones are potent antimicrobial agents used for the treatment and prophylaxis of infections caused by Gram-negative bacteria, including E. coli [13]. Resistance to quinolones may be related to chromosomal mutations, alterations in efflux mechanisms, or plasmid-mediated [14].

In our study, of the 150 (100%) urine cultures ordered, 80 (53.0%) were positive for bacterial growth, 55 (37.0%) cultures yielded mixed growth, and 15 (10.0%) of the isolates were Candida. This is in agreement with the results of Aypak et al. [1], who found positive bacterial growth in 38.5% of cultures and negative growth in 61.5%. Gram-negative bacteria were found in 76.7% of urine samples and Gram-positive bacteria in 16%; Candida was found in 7.3%.

Behzadi et al. [15] reported urinary tract infections associated with Candida albicans in 6.8% of their patients. The remaining 93.2% of UTIs related to bacterial pathogens.

In the present study, the number of male patients was higher than the number of female patients [43 (54.0%) and 37 (46.0%), respectively]. This was because of random selection of samples and because more number of hospitalized patients in the last 6 months were male and suffered from prostatitis, benign prostatic hyperplasia, or cancer prostate. This is in agreement with the results of Mahesh et al. [16], who conducted a study on 194 patients (116 male and 78 female patients), as well as in agreement with the study by Alakhali et al. [17], who conducted a study on 205 urinary tract-infected patients, of whom 116 (56.6%) were male and 89 (43.4%) were female, indicating that prevalence was higher among male patients than among female patients. Further, Rai et al. [18] documented no significant difference in growth-positive rate between sexes (male: 51.7% and female: 48.3%).

This is in contrast to the results of Janifer et al. [19], who reported that women (47.9%) had a significantly higher prevalence of UTI compared with men (34.1%), and also in contrast to the study by Khawcharoenporn et al. [6], who conducted an investigation on 337 eligible patients among whom 83% women had UTIs. This is also in contrast to the study by Acharya et al. [20], who reported that UTI occurred more in female (61.60%) patients than in male (38.39%) patients.

As regards the causative organism of UTI, this study showed that Gram-negative bacilli were the most common organism. Urine culture results obtained from the urine of patients revealed infection by E. coli in 52.5% of patents, Enterobacter spp. in 15.0%, Klebsiella spp. in 8.8%, Gram-positive cocci in 8.8%, Citrobacter spp. in 5.0%, Pseudomonas spp. in 5.0%, Proteus spp. in 3.8%, and Shigella spp. in 1.3%. E. coli was the most predominant (52.5%). This result was in agreement with that of Barros et al. [21], who found that E. coli (63.08%) was the most frequently seen Gram-negative bacteria and that the most frequently isolated Gram-positive bacteria were S. saprophyticus (4.52%) and Staphylococcus aureus (3.19%).

Amin et al. [22] also documented that E. coli was the most commonly isolated bacteria (59%). The other bacteria were Klebsiella spp. (11.6%), Enterobacter spp. (9.8%), Pseudomonas spp. (7.2%), Proteus spp. (2.9%), Acinetobacter spp. (2.7%), coagulase-positive Staphylococci spp. (2.2%), Coagulase-negative Staphylococci spp. (2.3%), Citrobacter spp. (1.3%), and Streptococci a hemolytic (1.1%).

This is also in agreement with the study by Omigie et al. [4], who found that the percentage of isolates was as follows: E. coli, 45.7%; Proteus spp., 15.0%; Klebsiella spp., 12.3%; Pseudomonas spp., 11.5%; S. aureus, 10.1%; and Streptococcus spp., 5.4%. In the study by Acharya et al. [20] E. coli was found in 68.77% of the total isolates, followed by Enterobacter spp. (13.92%) and Klebsiella spp. (5.90%).

In this study, people aged more than 50 years were more frequently affected by UTI (52.5%), which was followed by people aged 20-50 years (40.0%). Most of the patients were male and complained from benign prostate hypertrophy. This is in agreement with the study by Acharya et al. [20], in whose study 42.85% of isolates were from patients older than 50 years. This is also in agreement with the study by Bouchillon et al. [23], who found that almost half of the isolates were from elderly patients over 65 years of age (49%) and fewer than 10% were from pediatric patients (0-16 years), with a mean age of 58.1 years for all patients represented.

This is in contrast to the study by Omigie et al. [4], in whose study patients aged 20-50 years were more frequently affected by UTI (74.7%), followed by patients younger than 20 years (15%).

In this study, E. coli was more prevalent among female patients (52.5%) than among male patients (51.2%), whereas Klebsiella spp. was more prevalent among male patients (11.6%) than among female patients (8.8%). This is in agreement with the study by Rocha et al. [24], who documented that sex significantly influenced the distribution of urine organisms. Although E. coli, Enterococcus spp., and Klebsiella spp. were the three most prevalent pathogens among both female and male patients, E. coli was more prevalent among females, whereas Klebsiella spp. was more prevalent among males.

In this study there is significant difference between male and female patients in their resistance to quinolone drugs, as resistance to quinolone drugs was higher in male than in female patients. This is in agreement with the results of Ito et al. [25], who reported that resistance to quinolones was higher in men, perhaps because of the association between UTIs and prostatitis, where quinolones are widely used.

As regards the type of samples, in this study there were 69.0% midstream sample isolates and 31.0% urinary catheter isolates. Resistance to quinolones was higher in isolates from the urinary catheter than in midstream sample isolates. This is in agreement with the results of Toukam et al. [26], who documented that 56.3% of isolates from urinary catheters were resistant.

In this study there is a reported difference in the prevalence of various uropathogens between patients with indwelling urinary catheter and noncatheterized patients (midstream samples). It was found that E. coli, Gram-positive cocci, and Klebsiella spp. were more often recovered from noncatheterized patients (midstream samples), whereas Enterobacter spp. and Citrobacter spp. were more often recovered from catheterized patients.

In the study by Abdallah et al. [27] it was found that E. coli, Klebsiella spp., and S. aureus were more often recovered from noncatheterized patients, whereas Enterococcus spp. and Pseudomonas spp. were more often recovered from catheterized patients.

This is in contrast to the study by Lule [28], who reported that there were no statistically significant differences in the isolation frequency of each pathogen between noncatheterized and catheterized patients (P > 0.05). The most frequently isolated species from noncatheterized patients was Klebsiella spp. (40%), followed by E. coli (30%). Among catheterized patients, E. coli and Klebsiella spp. were found to be the most frequently isolated pathogens (each of them accounted for 23%). In addition, Proteus spp., Pseudomonas spp., and coagulase-negative Staphylococci spp. were isolated only from catheterized patients.

In this study there was a nonsignificant difference in the results of sensitivity/resistance profiles among all quinolone drugs. Among the quinolone drugs, nalidixic acid was the least efficient in preventing the growth of UTI pathogens, with 83.8% of pathogens resistant, followed by ofloxacin (77.5%), levofloxacin (75.0%), ciprofloxacin (73.8%), and gatifloxacin (72. 5%). This means that nalidixic acid was the most resistant in preventing the growth of UTI pathogens and gatifloxacin was the most potent.

In the study by Omigie et al. [4] nalidixic acid was found to be the least efficient in preventing the growth of UTI pathogens, with 51.7% of all isolates resistant, whereas ciprofloxacin was found to be the most potent, being able to prevent the growth of 91.2% of all the UTI pathogens tested.

This is in agreement with the results of Alakhali et al., [17] who reported that the resistance was elevated for nalidixic acid, with an average rate of 71.9%, which was much higher than that for ciprofloxacin (41.4%). This is in contrast to the results of Molina-López et al. [29], who reported that drug resistance among uropathogenic strains from Mexico city expressed the highest resistance rates to the following: norfloxacin (60.6%), ofloxacin (60.6%), nalidixic acid (56.4%), and ciprofloxacin (55.5%). The lowest percentage of resistance was for meropenem (0.85%), amikacin (1.7%), nitrofurantoin (5.1%), cefepime (7.6%), ceftazidime (8.5%), and ceftriaxone (10.2%).

In this study the highest resistance rate to ciprofloxacin was reported for E. coli, followed by Enterobacter spp., Gram-positive cocci, Klebsiella spp., Pseudomonas spp., and Citrobacter isolates.

This in contrast to the study by Astal [30], who found that high resistance rates to ciprofloxacin were found among Acinetobacter haemolyticus, S. saprophyticus, Pseudomonas aeruginosa, E. coli, and Enterococcus faecalis isolates.


  Conclusion Top


UTI is a serious health problem. Random use of quinolones in UTI should be discouraged because of increased antimicrobial resistance. Close attention is required to monitor fluoroquinolone susceptibility patterns and the association of multidrug resistance with fluoroquinolone resistance in isolates of E. coli and other bacteria causing UTIs.


  Acknowledgements Top


Conflicts of interest

There are no conflicts of interest.

 
  References Top

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2. Lin CY, Huang SH, Chen TC, Lu PL, Lin WR, Chen YH. Risk factors of ciprofloxacin resistance in urinary Escherichia coli isolates. J Microbiol Immunol Infect 2008; 41:325-331.  Back to cited text no. 2
    
3. Olson RP, Harrell LJ, Kaye KS. Antibiotic resistance in urinary isolates of Escherichia coli from college women with urinary tract infections. Antimicrob Agents Chemother 2009; 53:1285-1286.  Back to cited text no. 3
    
4. Omigie O, Okoror L, Umolu P, Ikuuh G. Increasing resistance to quinolones: A four-year prospective study of urinary tract infection pathogens. Int J Gen Med 2009; 2:171-175.  Back to cited text no. 4
    
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27.Abdallah NM, Elsayed SB, Mostafa MY, El-gohary GM. Biofilm forming bacteria isolated from urinary tract infection, relation to catheterization and susceptibility to antibiotics. Int J Biotechnol Mol Biol Res 2011; 2:172-178.  Back to cited text no. 27
    
28.Lule T. Assessment of bacterial profile and antimicrobial Susceptibility pattern of catheter-associated urinary tract infections in comparison with non-catheterized urinary tract infections in jimma university hospital, Southwest Ethiopia. 2005; 27-35.  Back to cited text no. 28
    
29.Molina-López J, Aparicio-Ozores G, Ribas-Aparicio RM, Gavilanes-Parra S, Chávez-Berrocal ME, Hernández-Castro R, Manjarrez-Hernández HA. Drug resistance, serotypes, and phylogenetic groups among uropathogenic Escherichia coli including O25-ST131 in Mexico City. J Infect Dev Ctries 2011; 5:840-849.  Back to cited text no. 29
    
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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8], [Table 9]



 

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