Prevalence of Cotrimoxazole Resistance Uropathogenic Bacteria in Iran: A Systematic Review and Meta-Analysis

AUTHORS

Mostafa Rezaei-Tavirani 1 , Sobhan Ghafourian 2 , Fatemeh Sayehmiri 2 , Reza Pakzad 3 , 4 , Saeid Safiri 5 , 6 , Iraj Pakzad 2 , 7 , *

1 Proteomics Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran

2 Department of Microbiology, Faculty of Medicine, Ilam University of Medical Sciences, Ilam, Iran

3 Noor Research Center for Ophthalmic Epidemiology, Noor Eye Hospital, Tehran, Iran

4 Department of Epidemiology, Faculty of Health, Ilam University of Medical Sciences, Ilam, Iran

5 Managerial Epidemiology Research Center, Department of Public Health, School of Nursing and Midwifery, Maragheh University of Medical Sciences, Maragheh, Iran

6 Department of Epidemiology and Biostatistics, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran

7 Clinical Microbiology Research Center, Ilam University of Medical Sciences, Ilam, Iran

How to Cite: Rezaei-Tavirani M, Ghafourian S , Sayehmiri F , Pakzad R , Safiri S, et al. Prevalence of Cotrimoxazole Resistance Uropathogenic Bacteria in Iran: A Systematic Review and Meta-Analysis, Arch Clin Infect Dis. 2018 ; 13(5):e63256. doi: 10.5812/archcid.63256.

ARTICLE INFORMATION

Archives of Clinical Infectious Diseases: 13 (5); e63256
Published Online: August 6, 2018
Article Type: Review Article
Received: August 19, 2016
Revised: October 25, 2017
Accepted: October 29, 2017
Crossmark

Crossmark

CHEKING

READ FULL TEXT
Abstract

Context: Cotrimoxazole is one of the antibiotics commonly used to treat urinary tract infections. The widespread use of this drug has led to increased resistance to cotrimoxazole among urinary tract pathogens. This study aimed to investigate the cotrimoxazole resistance pattern of uropathogenic bacteria by a systematic review and meta-analysis method.

Evidence Acquisition: Several databases including PubMed, Web of Science, Scopus, Google Scholar, Iran Medex, Magiran, IranDoc, MedLib, and SID were searched. From a total of 171 papers published from different regions of Iran from 1992 to May 2015, 67 were included in this study. To assess the quality of the study, the STROBE (strengthening the reporting of observational studies in epidemiology) checklist was employed. The I2 index was used to determine heterogeneity and a random effects model to analyze the data.

Results: The results showed that the prevalence of urinary tract infection was several times higher in women than in men. The most common pathogens causing urinary tract infections were E. coli 64%, Klebsiella 12%, Staphylococcus 10%, and Enterobacter (6%). The prevalence of cotrimoxazole resistance was as follows: E. coli 62% (95%CI: 60 - 65), Klebsiella 54% (95% CI: 45 - 62), Staphylococcus 55% (95% CI: 47 - 63), and Enterobacter 52% (95% CI: 33 - 70). Cotrimoxazole resistance in different studies varied from 22% in Arak to 88% in Ahvaz.

Conclusions: Gram-negative bacilli, particularly Escherichia coli, were the most common bacteria causing urinary tract infections. The majority of strains were resistant to cotrimoxazole. According to the findings, cotrimoxazole is not recommended as the first-line drug for the treatment of urinary tract infections in Iran.

Keywords

Urinary Tract Infections Gram-Negative Bacteria Gram-Positive Bacteria Cotrimoxazole, Antimicrobial Resistance Meta-Analysis

Copyright © 2018, Archives of Clinical Infectious Diseases. This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License (http://creativecommons.org/licenses/by-nc/4.0/) which permits copy and redistribute the material just in noncommercial usages, provided the original work is properly cited.

1. Context

Urinary tract infection (UTI) is the most common bacterial infection with the high economic burden that affects a large number of populations. The range of clinical symptoms of the infection is different from asymptomatic bacteriuria to bladder inflammation, pyelonephritis, septic shock, and defects in several organs (1, 2). Both hospital-acquired and community-acquired urinary tract infections can lead to serious complications such as urinary tract disorders, uremia, hypertension, and even death (3). It is the most common infection among patients admitted to hospitals and laboratories. It can be observed in all age groups and in both genders although it is more likely to occur among young women (4). Studies have indicated that about 50% of women and 12% of men suffer from urinary tract infection throughout their life (5). Moreover, 20 - 30% of women experience a recurrence of this infection during 6 - 12 months (5, 6). Therefore, this is a major public health problem (7). Throughout the world, about 150 million people are diagnosed with a UTI each year (8). In most cases, bacterial agents, especially Gram-negative bacteria such as E. coli, are the cause of this infection. Other Gram-negative bacteria include Klebsiella, Proteus, Pseudomonas, Serratia, and Enterobacter, which are involved in a small percentage of urinary tract infections (4, 9). Isolated urinary pathogens vary depending on age, gender, catheterization, hospitalization, and previous use of antibiotics (10). Due to the acquisition of antibiotic resistance genes by the bacteria over time in different geographical areas, on the one hand, and the change in the susceptibility patterns of bacteria to antibiotics, on the other hand, the selection of the appropriate antibiotics for treatment has become a challenge and it is more based on the information obtained from determining the pattern of antimicrobial resistance in the given area (3).

Cotrimoxazole is made from a combination of two antibiotics including trimethoprim and sulfamethoxazole, both of which disrupt folic acid metabolism in bacteria through different mechanisms. Moreover, it is the first antibiotic prescribed for the treatment of urinary tract infection (11). Folic acid producing bacteria are sensitive to this medicine; therefore, the drug stops their proliferation (12-14).

The widespread use of this drug due to the low cost, fewer side effects, and availability have led to increased resistance to cotrimoxazole among urinary pathogens (15).

The treatment of urinary tract infections can be often done on an experimental basis. An important principle in the treatment of such infections is the use of the results of the bacterial resistance patterns causing the infection. Furthermore, because of the continuous rise of antibiotic resistance, the regular monitoring of antibiotic resistance is necessary for improving the empirical antibiotic treatment guidelines (16). According to numerous studies conducted on the prevalence of resistance to cotrimoxazole among the urinary pathogenic bacteria, a meta-analysis seemed necessary in order to validate the results of these studies.

2. Evidence Acquisition

2.1. Search Strategy

A systematic review and meta-analysis was conducted in Persian and English by searching the national and international databases including SID, Magiran, IranDoc, IranMedex, MedLib, PubMed, ISI, Web of Science, Scopus, and Google Scholar to find studies published from 1992 to 2015 concerning the patterns of drug resistance to cotrimoxazole in microbial strains isolated from urinary tract infections. These databases were investigated using keywords in Persian (urinary tract infections, Gram-negative bacteria, Gram-positive bacteria, cotrimoxazole, and antibiotic resistance) and their English equivalent, with all the possible combinations including important, original, and sensitive words. In addition, the reference list of the selected articles was used to find additional resources.

2.2. Study Selection

All group or cross-sectional studies were considered among those reporting the prevalence of bacterial resistance to cotrimoxazole in urinary tract infections. Two researchers (S-Gh, R-P) independently took the responsibility for selecting the articles and assessing their validity. Any discrepancy between the two raters was resolved by a third reviewer (I-P). The current study applied a blinding and task separation to the study selection. The inter-rater reliability was calculated based on kappa statistics, which was obtained at 85%.

The selection of papers for the study was completed based on three stages including title, abstract, and full text. Studies with insufficient information, non-cross-sectional designs, studies in conjunction with other non-UTI infections, review studies, abstracts of conference proceedings, published papers in languages other than English and Persian, meta-analyses, systematic, and repetitive studies were excluded from the analysis.

2.3. Data Extraction and Quality Assessment

First, the title of all articles was reviewed for screening the eligibility criteria. Every paper, which was inconsistent with the eligibility criteria, was excluded. Afterward, the abstracts were checked and then, the full text of articles was assessed to identify the inclusion criteria. Those articles that did not satisfy the inclusion criteria nor had a weak correlation with the objectives of the study were excluded. Then, all the articles included in the final stage of analysis were assessed by using checklists to extract the following data: first author, year of publication, year of study, study location, sample size, mean age, gender, type of isolation, prevalence of urinary pathogens, bacterial pathogens resistant to cotrimoxazole, and standard methods for determining antibiotic susceptibility to antibiotics (Table 1).

Table 1. General Specifications and Data of Articles Reviewed in the Meta-Analysis
First Author (Reference)Publication YearStudy LocationSample SizeThe Prevalence of Pathogens and Their Drug Resistance to Cotrimoxazole
E. coli (%)Klebsiella (%)Staphylococcus (%)
PrevalenceResistanceSusceptibilityPrevalenceResistanceSusceptibilityPrevalenceResistanceSusceptibility
Sharifi (16)2014Yasouj120-62.537.5------
Molazadeh (17)2012Gaharbi Azerbaijan190039.360.329.8------
Mohajeri (18)2011Kermanshah11147558.736.7------
Molazadeh (17)2012Fasa248476.359.440.616.651.748.3---
Mosavian (19)2004Ahvaz383435.364.720--1433.350
Madani (20)2008Kermanshah181545.461.127.7------
Sorkhi (21)2005Babol18859.58119------
Ghutaslou (22)2005Tabriz20137964.735.310.3-----
Nourozi (23)2000Tehran31353.578224.6--3.2--
Alaei (24)2008Tehran5107266349--6.1--
Borji (25)2001Zahedan429-80.516.7------
Torabi (26)2007Zanjan11848.457.442.617.3--15.971.128.9
Hajizade (27)2003Tehran150507228107030195545
Eghbalian (28)2005Hamedan15682.134.465.62.6--5.1--
Barati (29)2011Kolaleh360-4748.1------
Farshad (30)2009Jahrom90-7624------
Jarsiah (4)2014Tehran20873.165.525.46.7-----
Mirmostafa (31)2013Karaj1008359413-----
Tajvidi (32)2014Tehran372-5147------
Asgharian (33)2011Tenkabon35784.68317------
Sharif (34)1999Kashan15752564414.757.842.2---
Rahimi (35)2014Isfahan30164.570297.3316911.3--
Ranjbaran (36)2013Arak50-8812-7030---
Mokhtarian (37)2006Gokabad3536662.216.77.9--21.8--
Beheshti (38)2005Tabriz103-76.128.4------
Assefzadeh (39)2009Ghazvin22461.261.538.58.964.335.77.245.554.5
Tarhani (40)2003Khoramabad12773.254.345.749.47.192.9---
Hamid-Farahani (41)2012Tehran45660.33761.513--22.1--
Mohammadi (42)2006Falavarjan20954.163.435.915.8--17.2--
Langarizadeh (43)2010Tabriz72----95.82.8---
Fahimi (44)2004Tehran17061.175.319.42.92.8--
Babaie Kasmaei (45)2012Tehran123-93.36.7------
Arbab Soleimani (46)2014Semnan100704258------
Tashkori (47)2011Rafsanjan146-62.337.7-----
Moulana (48)2013Babol77048.669.330.717.9--8--
Heidari- Soureshojani (49)2013Chaharmahal va Bakhtiari7470.342.451.5---20.3--
Soltan Dallal (50)2011Tabriz400476535------
Sharifi Yazdi (51)2013Tehran300------77.765.143.9
Fesharakinia (52)2012Birjand1007569.920.5------
Jalalpour (53)2009Isfahan9184.659.240.815.45050---
Fallah (54)2012Tehran200-67.732.3------
Khodadoost (55)2013Kermanshah140-62.137.3------
Ghadiri (56)2009Kermanshah87-72.419.5------
Sahebnasagh (57)2015Tehran11235061.438.6------
Safkhani (58)2014Tehran13651.56037.311.843.856.213.2--
Barari Sawadkouhi (59)2013Babol1288962.337.73.15050-0100
Akya (60)2015Kermanshah200-57.542.5------
Dezfolimanesh (61)2013Kermanshah100-55.634.9------
Isvand (62)2014Dezfoul16063.311.288.820.6--4.4-
Esmaeli (63)2013Hamedan141612873---8.566.733.3
Sedighi (64)2014Hamedan50-7028------
Hosseini (65)2014Ghazvin12041.61485210.64357---
Bagheri (66)2014Gorgan111---40.51.319.68---
Molazadeh (17)2012Fasa28364.35.6626.75.141.471.444.69.427.35
Molazadeh (17)2012Fasa248464.77.6831.39.234.606.39---
Molaabaszadeh (67)2013Tabriz570158.49.6333------
Ahangarkani (68)2015Babol128786722------
Neamati (69)2015Kashan150-7.647.32------
Sedighi (64)2014Hamedan100-7026------
Nasiri Moghadam (70)2000Birjand111656535------
Savadkoohi (71)2007Babol160706733---6.57.663.33
Emam Ghoreishi (72)2014Jahrom108-4.716.28------
Esmaeili (73)2005Mashhad1661.748.752.242.73.337.663.4--
Sedighi (74)2010Hamedan100-7026------
Zamanzad (75)2005Shahrkord100422.768.23387.843.1512--
Zamanzad (75)2005Shahrkord100585.655.341675257--
Norouzi (76)2006Jahrom35680.3511.4110.7--84--
Nakhaie Moghadam (77)2010Mashhad109-1.559.44------

To evaluate the quality of the studies, seven items on the STROBE (strengthening the reporting of observational studies in epidemiology) checklist were considered: meticulous references based on the framework of the study, setting of the study, inclusion and exclusion criteria, definition of UTI and criteria, identification and measurement methods of UTI and criteria, reporting the main outcome, the number of study population, and the target population of the study.

The studies, which adhered to all seven items on the STROBE checklist, were labeled as high quality while those observing six items were of medium quality. The studies that did not meet two or more items on the STROBE checklist were classified as low-quality studies.

2.4. Statistical Analysis

Given that in each article, the prevalence of antibiotic resistance and the number of samples were extracted, a binomial distribution was used to calculate the variance of each study and average weight was applied to combine the prevalence of different studies. A weight was given to every study inversely proportional to its variance. According to a large difference in prevalence rates between different studies (heterogeneity of studies) and based on the significant heterogeneity index (I2 = 95%), a random-effects model was used in the meta-analysis. A funnel plot was used to detect the publication bias graphically. It is a bivariate scatter plot (x, y) of the study sample size versus the study estimate of treatment difference or effect size. There is a formal test for publication bias based on the linear regression analysis. It includes both intercept and slope parameters given as yi = α + βxi + εi, for i = 1, ..., r, where r is the number of studies, yi is the ‘standardized estimate’, xi is the ‘precision’ of studies and εi the error term.

3. Results

In the initial search, 171 full papers and abstracts were obtained. In the next phase, 23 papers and abstracts were removed because of mismatch and insufficient contents of abstracts. Then, 34 other repetitive reviews were excluded from the study. After evaluation of articles, 47 ones were deleted because of failure to mention the drug resistance to cotrimoxazole and finally, after a thorough review of the selected articles, 67 studies, which were published between 1995 and 2015, entered into the meta-analysis (Figure 1). Based on the quality assessment, 42 studies were classified as high quality and 25 as moderate quality. General specifications and data from articles are shown in Table 1.

The flowchart of study selection in the systematic review and meta-analysis
Figure 1. The flowchart of study selection in the systematic review and meta-analysis

In all the studies included in this meta-analysis, the middle urine samples were cultured on the appropriate media and the bacteria were identified by standard methods. The results obtained from these studies showed that 29399 cases among the total number of samples had a urinary tract infection, 78.40% of which were related to women while 21.60% of these samples were found in men and the highest proportion (59.40%) was associated with outpatients. The most common bacteria that caused urinary tract infection and their prevalence are indicated in Table 2. As can be seen, the most common pathogen responsible for urinary tract infection was E. coli with the frequency of 64% (Figure 2). Klebsiella with a frequency of 12%, Staphylococcus with a frequency of 10%, and Enterobacter with a frequency of 6% were in the next ranks. In addition, other bacteria responsible for urinary tract infection included Enterococci, Citrobacter, Acinetobacter, Pseudomonas, Proteus, and Enterobacter with an overall frequency of 8% that had marginal roles in the development of urinary tract infections (Table 2).

Table 2. The Frequency Distribution of Bacterial Agents of Urinary Tract Infection in Terms of the Number of Studies Included in the Meta-Analysis
Bacteria TypeThe Number of StudiesPrevalenceConfidence Interval (CI%95)Heterogeneity Index I2 (%)P-Value
E. coli4564%68 - 6097.6< 0.001
Klebsiella3112%9 - 1596.6< 0.001
Staphylococcus2410%7 - 1293.3< 0.001
Enterobacter236%5 - 788.9< 0.001
Other species348%2 - 1259.2< 0.001
The prevalence of E. coli in urinary tract infections based on random effects model (The midpoint of each line segment shows estimated prevalence rate, the length of line segment indicates a confidence interval of 95% in each study and diamond mark illustrates the prevalence in the whole country for all studies)
Figure 2. The prevalence of E. coli in urinary tract infections based on random effects model (The midpoint of each line segment shows estimated prevalence rate, the length of line segment indicates a confidence interval of 95% in each study and diamond mark illustrates the prevalence in the whole country for all studies)

Kirby-Bauer disk diffusion test was used to determine the bacterial susceptibility to cotrimoxazole in all studies included in the meta-analysis.

According to the results shown in Table 3, the resistance rate of the most common strains causing urinary tract infection to cotrimoxazole was as follows: E. coli, 62% (with confidence interval: 60 - 65) (Figure 2), Klebsiella, 54% (with confidence interval: 45 - 62), Staphylococcus, 55% (with confidence interval: 47 - 63), and Enterobacter, 52% (with confidence interval: 33 - 70).

Table 3. The Prevalence of Bacterial Resistance to Cotrimoxazole with a 95% Confidence Interval
Bacteria TypeThe Number of StudiesSensitive (95% CI)Semi-Sensitive (95% CI)Resistant (95% CI)
E. coli6635 (32 - 389) 3 (1 - 5)62 (60 - 65)
Klebsiella1846 (37 - 55)054 (45 - 62)
Staphylococcus940 (34 - 64)5 (3 - 8)55 (47 - 63)
Enterobacter946 (28 - 65)2 (0 - 4)52 (33 - 70)

Since the rate of resistance to cotrimoxazole was highest in E. coli strains in most of the studies included in the meta-analysis, the most common agent causing urinary tract infection was E. coli. Therefore, the ratio of resistance to cotrimoxazole in E. coli strains was studied in different geographical areas of the country. The results showed that the ratio of resistance in the majority of the five regions and cities in the country was high (above 60%) and there were no significant differences between these areas (Tables 4 and 5). It should be noted that the highest resistance rate (88%) was reported in Arak while the lowest rate (22%) was found in Ahvaz.

Table 4. The Prevalence of Resistance to Cotrimoxazole in E. coli With 95% Confidence Interval in Different Cities of Iran
CityThe Number of StudiesThe Prevalence of Resistance%Confidence Interval (CI%95)
Tehran136657 - 74
Isfahan46365 - 70
Ghazvin25441 - 68
ShahrKord36243 - 80
Arak18879 - 97
Kermanshah66158 - 63
Hamedan65438 - 70
Gharbi Azerbaijan16063 - 58
Zanjan26947 - 92
Tabriz66463 - 65
Ahvaz2221 - 46
Shiraz36558 - 71
Yasouj16354 - 71
Jahrom36649 - 83
Rafsanjan16354 - 70
Mashhad26645 - 86
Semnan14232 - 52
Birjand26761 - 74
Table 5. The Prevalence of Resistance to Cotrimoxazole in E. coli with a 95% Confidence Interval in Different Regions of Iran
RegionThe Number of StudiesThe Prevalence of ResistanceConfidence Interval (CI%95)Heterogeneity Index I2 (%)P-Value
Central226458 - 7196.3< 0.001
North96759 - 7594.7< 0.001
West196057 - 6389.8< 0.001
South105746 - 6798.3< 0.001
East66554 - 7693.2< 0.001

According to the publication bias figure, the effect of bias in these studies was not significant. In fact, most studies were located inside the funnel plot, demonstrating that the results of the most relevant studies performed in Iran were included in the analysis (Figure 3). The interpretation of meta-regression represented that there was no significant relationship between the prevalence of E. coli and year of study (P = 0.15) (Figure 4).

Begg’s funnel plot for publication bias in the risk difference (RD) analysis
Figure 3. Begg’s funnel plot for publication bias in the risk difference (RD) analysis
The association between the prevalence of E. coli and year using meta-regression
Figure 4. The association between the prevalence of E. coli and year using meta-regression

4. Discussion

In the present study, the ratio of urinary tract infection was several times higher in females than in males (78.40% vs. 21.60%, respectively). In other parts of the world, similar results were reported in several studies. For example, Dipiro et al. in New York (78), Boucher et al. in America (79), Linhares et al. in Portugal (80), Garcia-Morua et al. in Mexico (81), Oladeinde et al. and Dibua et al. in Nigeria (82, 83), Chen et al. in Taiwan (84), George et al. in India (85), and Kalsoom et al. in Pakistan (86) have found that the prevalence of urinary tract infection was higher in females. A reason for this issue can be the structure and anatomy of the female genital-urinary tract; the shorter urethra and the proximity of urethral to vaginal and anus in females are the main causes of urinary tract infections in this group (87, 88).

In our society, due to the absence of the culture of correct consumption of antibiotics, most of the patients’ urine cultures were negative because of the previous self-curing. Thus, in many cases, the treatment takes place based on the most prevalent strains of urinary tract infection and their antibiotic susceptibility pattern (63). The results of this research suggest that the bacteria of the Enterobacteriaceae family in most cases are the most prevalent causes of urinary tract infections. Among the members of this family, E. coli is most frequently assigned. These results were consistent with studies conducted in other parts of the world (80, 85, 89-96). In addition, in this study, Klebsiella was the most prevalent one after Escherichia coli, which is in line with other studies (86, 97-100). In most of these studies, in line with the present study, Enterobacteriaceae have been reported as the cause of 90% of the genital-urinary tract infections, with Escherichia coli as the main pathogen, followed by other members of the Enterobacteriaceae family and Gram-positive cocci, especially Staphylococcus. The reason for the higher prevalence of the Enterobacteriaceae family is the presence of these bacteria in the stool and the possibility of urinary tract infection in this way (101). Microorganisms can be compatible with environmental changes in different ways, among which is drug resistance (32). In this study, the most prevalent uropathogens (Escherichia, Klebsiella, Staphylococcus, and Enterobacter) were resistant to cotrimoxazole. Escherichia coli with 62% resistance rate ranked first, followed by other microorganisms. Recent studies show that E. coli isolated from humans is an important pathogen with increased antibiotic resistance to most antimicrobial drugs (49); therefore, the present study focused on the investigation and interpretation of the results of E. coli resistance to cotrimoxazole.

E. coli resistance to cotrimoxazole in most developing countries demonstrated similar results. For example, this resistance has been reported 68.1% in Senegal (46), 58% in Turkey (98), 53% in Lebanon (102), 55% in Brazil (103), and 60% in Mexico (104). E. coli in Bangladesh showed the lowest susceptibility (20 - 27%) to cotrimoxazole (105). In addition, this sensitivity was 33.3% in Ethiopia (100). The results of these studies were consistent with those of the present study and showed the high resistance of E. coli to cotrimoxazole. The susceptibility of E. coli to cotrimoxazole has been reported as 49% in Taiwan (84) and 49.1% in India (85). Comparing the results of the mentioned studies with our findings shows that the prevalence of resistance to cotrimoxazole was higher in our country than in other countries. In all studies cited, empirical treatment with this drug was not satisfactory and it was not recommended to use.

Unlike the present study, the low resistance to cotrimoxazole in E. coli isolates has been reported in some studies, especially in developed countries. For example, the ratio of resistance was 27.1% in Italy (106), 22% in Canada (107), 20.59% in Croatia (108), 21.3% in America (24), 14.5% in Australia (104), 64.1% South Korea (99), and 21% to 36% in several European countries (101). In general, antibiotic resistance in Iran is high compared to some developed countries like the United States (19). The difference could be due to the strains of microorganisms, self-medication by patients, not completing the full course of treatment, inappropriate prescription of antibiotics by physicians, inadequate dose of the drug, drug quality according to the manufacturers, action limited to empirical treatment without regard to culture and susceptibility patterns, poor hygiene, and low social and economic status of life in dirty and crowded environments. According to the high levels of E. coli resistance to cotrimoxazole in this study and similar studies, it seems the phenomenon of drug resistance is increasing in developing countries rapidly. Therefore, accurate strategies by clinical practitioners should be in line with infection control and prevention from the spread of resistance.

The study results conducted in Iran revealed that a low resistance to cotrimoxazole in E. coli strains only was reported in Ahvaz (46, 62) and Semnan (109), which may be due to avoiding the prescription of cotrimoxazole or because of the small number of studies reported in these areas. In all cities in other parts of the country, a high resistance to cotrimoxazole has been reported in E. coli strains. Given these similarities, in the case of the high resistance to cotrimoxazole in different regions of the country, it can be concluded that prescribing patterns and drug use in the country were the same. However, in the past decade, inappropriate use of cotrimoxazole has led to increased resistance to this medication. In most instances, due to the indiscriminate and arbitrary use of antibiotics, many cases of drug resistance can be observed in pathogens leading to treatment failures and many complications, despite the high cost of care. The results of this research are not compatible with the treatment regimen published in 2007 by the world health organization that introduced cotrimoxazole as the first-line drug for the treatment of urinary tract infection (17). According to the results of this study and other studies, it seems that these guidelines need to be revised and even it is suggested developing the first-line treatments specifically for every area based on epidemiological studies. Therefore, according to the results of this study, it can be said that cotrimoxazole is ineffective and its use is not recommended as the first-line antibiotic therapy.

There are several limitations to this study. First, publications from certain provinces were exceedingly high and it might affect the total estimation. Another limitation of this study was a failure to account for the ratio of resistance to cotrimoxazole in strains causing urinary tract infections separately for males and females. Only in a limited number of studies, the resistance was separately calculated for the two genders. Moreover, age is listed among the factors affecting the level of resistance while because of failure to separate the age groups in a number of studies and due to the absence of similar age groups in a number of other studies, we could not calculate the level of resistance in terms of age. In addition, inability to account for the ratio of resistance according to the type of admission was another constraint of the current study since there was no such information in numerous studies. However, our study was the first study that assessed the prevalence of cotrimoxazole resistance in uropathogenic bacteria in Iran and the results of our study are useful in health planning.

4.1. Conclusion

According to the present research, the ratio of urinary tract infections is several times higher in females than in males. E. coli is the most common cause of urinary tract infections, followed by Klebsiella, Staphylococcus, Enterobacter, and other species with slight differences in different geographical areas. All bacteria were resistant to cotrimoxazole. According to the findings of this study, cotrimoxazole is not recommended as the first-line medicine for the treatment of urinary tract infections in Iran.

Acknowledgements

Footnotes

References

  • 1.

    Eshetie S, Unakal C, Gelaw A, Ayelign B, Endris M, Moges F. Multidrug resistant and carbapenemase producing Enterobacteriaceae among patients with urinary tract infection at referral Hospital, Northwest Ethiopia. Antimicrob Resist Infect Control. 2015;4:12. doi: 10.1186/s13756-015-0054-7. [PubMed: 25908966]. [PubMed Central: PMC4407313].

  • 2.

    Agarwal J, Srivastava S, Singh M. Pathogenomics of uropathogenic Escherichia coli. Indian J Med Microbiol. 2012;30(2):141-9. doi: 10.4103/0255-0857.96657. [PubMed: 22664427].

  • 3.

    Molazade A, Shahi A, Najafipour S, Mobasheri F, Norouzi F, Abdollahi Kheirabadi S, et al. [Antibiotic resistance pattern of bacteria causing urinary tract infections in children of Fasa during the years 2012 and 2014]. J Fasa Univ Med Sci. 2015;4(4):493-9. Persian.

  • 4.

    Jarsiah P, Alizadeh A, Mehdizadeh E, Ataee R, Khanalipour N. [Evaluation of antibiotic resistance model of Escherichia coli in urine culture samples at Kian hospital lab in Tehran, 2011-2012]. J Mazandaran Univ Med Sci. 2014;24(111):78-83. Persian.

  • 5.

    Brumbaugh AR, Mobley HL. Preventing urinary tract infection: progress toward an effective Escherichia coli vaccine. Expert Rev Vaccines. 2012;11(6):663-76. doi: 10.1586/erv.12.36. [PubMed: 22873125]. [PubMed Central: PMC3498450].

  • 6.

    Akoachere JF, Yvonne S, Akum NH, Seraphine EN. Etiologic profile and antimicrobial susceptibility of community-acquired urinary tract infection in two Cameroonian towns. BMC Res Notes. 2012;5:219. doi: 10.1186/1756-0500-5-219. [PubMed: 22564344]. [PubMed Central: PMC3528744].

  • 7.

    Tarchouna M, Ferjani A, Ben-Selma W, Boukadida J. Distribution of uropathogenic virulence genes in Escherichia coli isolated from patients with urinary tract infection. Int J Infect Dis. 2013;17(6):e450-3. doi: 10.1016/j.ijid.2013.01.025. [PubMed: 23510539].

  • 8.

    Lee JB, Neild GH. Urinary tract infection. Medicine. 2007;35(8):423-8. doi: 10.1016/j.mpmed.2007.05.009.

  • 9.

    Cybulski Z, Schmidt K, Grabiec A, Talaga Z, Bociag P, Wojciechowicz J, et al. Usability application of multiplex polymerase chain reaction in the diagnosis of microorganisms isolated from urine of patients treated in cancer hospital. Radiol Oncol. 2013;47(3):296-303. doi: 10.2478/raon-2013-0044. [PubMed: 24133395]. [PubMed Central: PMC3794886].

  • 10.

    Moges AF, Genetu A, Mengistu G. Antibiotic sensitivities of common bacterial pathogens in urinary tract infections at Gondar Hospital, Ethiopia. East Afr Med J. 2002;79(3):140-2. [PubMed: 12389960].

  • 11.

    Gupta K, Scholes D, Stamm WE. Increasing prevalence of antimicrobial resistance among uropathogens causing acute uncomplicated cystitis in women. JAMA. 1999;281(8):736-8. [PubMed: 10052444].

  • 12.

    Wormser GP, Keusch GT, Heel RC. Co-trimoxazole (trimethoprim-sulfamethoxazole): an updated review of its antibacterial activity and clinical efficacy. Drugs. 1982;24(6):459-518. [PubMed: 6759092].

  • 13.

    Stegeman CA, Tervaert JW, de Jong PE, Kallenberg CG. Trimethoprim-sulfamethoxazole (co-trimoxazole) for the prevention of relapses of Wegener's granulomatosis. Dutch Co-Trimoxazole Wegener Study Group. N Engl J Med. 1996;335(1):16-20. doi: 10.1056/NEJM199607043350103. [PubMed: 8637536].

  • 14.

    Guerrant RL, Van Gilder T, Steiner TS, Thielman NM, Slutsker L, Tauxe RV, et al. Practice guidelines for the management of infectious diarrhea. Clin Infect Dis. 2001;32(3):331-51. doi: 10.1086/318514. [PubMed: 11170940].

  • 15.

    Jafari S, Najafipour S, Kargar M, Abdollahi A, Mardaneh J, Fasihy Ramandy M, et al. [Phenotypical evaluation of multi-drug resistant Acinetobacter baumannii]. J Fasa Univ Med Sci. 2013;2(4):254-8. Persian.

  • 16.

    Sharifi A, Khoramrooz SS, Khosravani SA, Yazdanpanah M, Gharibpour F, Malekhoseini Malekhoseini AA, et al. [Antimicrobial resistance pattern of Escherichia coli isolated from patients with urinary tract infection (UTI) in Yasuj city during 1391-1392]. Armaghane danesh. 2014;19(4):337-46. Persian.

  • 17.

    Molazadeh M, Zadeh HMA, Zadeh NM. The pattern of sensitivity and resistance antibiotics in E. coli strains isolated from urine samples of pregnant women in Khoy and Salmas in West Azerbaijan province. Sci J Micro Biotech Islamic Azad Univ. 2012;4(12):13-20.

  • 18.

    Mohajeri P, Izadi B, Naghshi N. Evaluation of Antibiotic sensitivity of E.coli Isolated from Urinary infections patients referred to Kermanshah Central Laboratory in 2008. Behbood. Bimon J Kermanshah Univ Med Sci. 2011;15(1):51-6.

  • 19.

    Mosavian SM, Mashali K. [Study of bacterial urinary tract infection after catheterization and determine antibiotic resistance of bacteria isolated from patients]. Sci J Hamedan Univ Med Sci. Persian.

  • 20.

    Madani S, Khazaee S, Kanani M, Shahi M. [Antibiotic resistance pattern of E. coli isolated from urine culture in Imam Reza Hospital Kermanshah-2006]. J Kermanshah Univ Med Sci. 2008;12(3). Persian.

  • 21.

    Sorkhi H, Jabbarian AA, Askarian A. [Escherichia coli and drug sensitivity in children with urinary tract infection]. J Guilan Univ Med Sci. 2005;14(54):23-8. Persian.

  • 22.

    Ghutaslou R, Abdoli O, Mesri A. The in vitro activity of ciprofloxacin on isolated organisms from urinary tract infections in a pediatric hospital. Pharm Sci. 2005:29-32.

  • 23.

    Nourozi J, Mirjalili A, Azhdari A. Urinary infection in residents of Kahrizak Charity Foundation in Tehran during 1998. Feyz: J Kashan Univ Med Sci. 2000;13:104-9.

  • 24.

    Alaie V, Saleh Zadeh F. [Clinical protests and antibiogram results in 510 children with urinary tract infection]. J Ardebil Univ Med Sci. 2008;8(3):274-80. Persian.

  • 25.

    Borji A, Shahraki Zahedani S, Moradi A. [Drug resistant E.coli isolated from urinary tract infections in Zahedan during 2000-2001]. Sci J Zanjan Univ Med Sci. 2001;37:28-32. Persian.

  • 26.

    Torabi SZ, Falak-ul-Aflaki B, Moezzi F. In vitro Antimicrobial Drug-Resistance of Urinary Tract Pathogens in Patients Admitted to Vali-e-Asr Hospital Wards. ZUMS J. 2007;15(61):79-88.

  • 27.

    Hajizade N, Daneshjo K. Evaluation of in vitro antimicrobial drug-resistance in Imam Khomini hospital. Iran J Pediatr. 2003;13(2):133-40.

  • 28.

    Eghbalian F, Yousefi Mashouf R . [Determining the frequency of the bacterial agents in urinary tract infection in hospitalized patients under 18 years old in Ekbatan Hospital]. J Army Univ Med Sci. 2005;3(11):635-70. Persian.

  • 29.

    Barati L, Ghezelsofla F, Azarhoush R, Heidari F, Noora M. [Antibiotic sensitivity of isolated E. coli from pregnant women urine]. J Gorgan Univ Med Sci. 2011;13(3):101-7. Persian.

  • 30.

    Farshad S, Anvarinejad M, Mehrabi Tavana A, Japoni A, Hoseini M, Shahidi M. [Molecular Epidemiology of E. coli strains isolated from urinary Tract Infections in Children]. J Jahrom Uni Med Sci. 2009;7(1):15-27. Persian.

  • 31.

    Mirmostafa M, Hadadi A, Mozafari Sabet N. Plasmid Profiles and antibiotic resistance in clinical isolates of Escherichia coli isolated from patients in different parts of the city of Karaj. NCMBJ. 2013;3(12):93-7.

  • 32.

    Tajvidi N, Mahbod SA, Shokoh SGH, Naseh I, Tajvidi MA. [In-vitro Resistance Pattern of Escherichia coli Isolated from Patients with Urinary Tract Infection in Tehran]. J Army Univ Med Sci. 2014;11(4):330-4. Persian.

  • 33.

    Asgharian A. Investigation of antibiotic susceptibility pattern of E. coli isolated from urinary culture related to patients in the west of the Mazandaran province, during from September 2010 to September 2011. Sci J Exp Anim Biol. 2011;1(3):13-25.

  • 34.

    Sharif A, Adib M, Mousavi G, Sharif M, Ghavoshi G. The antibiotic resistance in bacterial agents of urinary tract infections in Kashan during 1995- 1997. Feyz: J Kashan Univ Med Sci. 1999;9:41-5.

  • 35.

    Rahimi MK, Falsafi S, Taiebi Z, Maesoumi M, Farasat Pour MR, Mirzaie A. The pattern of antimicrobial susceptibility of bacteria to human pathogens isolated from patients with urinary tract infection. NCMBJ. 2014;4(15):83-9.

  • 36.

    Ranjbaran M, Zolfaghari M, Japoni-Nejad A, Amouzandeh-Nobaveh A, Abtahi H, Nejad M, et al. [Molecular investigation of integrons in Escherichia coli and Klebsiella pneumoniae isolated from urinary tract infections]. J Mazandaran Univ Med Sci. 2013;23(105):2. Persian.

  • 37.

    Mokhtarian H, Ghahramani M, Nourzad H. A study of antibiotic resistance of Escherichia coli isolated from urinary tract infection. Quart J Horiz Med Sci. 2006;12(3):5-10.

  • 38.

    Beheshti F, Rahmati A, Akhi MT. [Compare minimum inhibitory concentration of common antibiotics on E. coli strains isolated from urinary tract infections in outpatient and inpatient]. J Tabriz Univ Med Sci. 2005;27(3):27-31. Persian.

  • 39.

    Assefzadeh M, Hagmanochehri F, Mohammadi N, Tavakoli N. [Prevalence of pathogens and antimicrobial susceptibility patterns in urine cultures of patients referred to Avesina medical center in Qazvin]. J Qazvin Univ Med Sci. 2009;13(2):30-4. Persian.

  • 40.

    Tarhani F, Kazemi AH, Abedini MR, Rashidi R. Antibiotic resistance in urinary tract infections in children hospitalized in Shahid Madani hospital khorramabad during 2001-2002. Quart Res J Lorestan Univ Med Sci. 2003;5(17):39-44.

  • 41.

    Hamid-Farahani R, Tajik AR, Noorifard M, Keshavarz A, Taghipour N, Hossieni-Shokouh J. Antibiotic resistance pattern of E. coli isolated from urine culture in 660 Army clinical laboratory center in Tehran 2008. Ann Mil Health Sci Res. 2012;10(1):45-9.

  • 42.

    Mohammadi M, Mohammadi M. Antibiotic susceptibility of bacteria isolated from urinary tract infections. Med Sci J Azad Univ. 2006;16(2):95-9.

  • 43.

    Langarizade N, Ahangarzade R, Aghazade M, Hasani A. Comparison of the prevalence of multidrug resistant Klebsiella pneumoniae in children and adults with urinary tract infection admitted to hospitals in Tabriz. Quart J Biolog Sci. 2010;12(4):9-17.

  • 44.

    Fahimi D, Rahbari Manesh A, Seifolahi A, Rezaei N. [The survey of microorganisms causing urinary tract infections and their susceptibility to antibiotics in children referred to Bahrami pediatrics hospital, during 1996-2003]. J Army Univ Med Sci. 2004;1(4):223-7. Persian.

  • 45.

    Babaie Kasmaei Z, Mozafari N, Forohesh Tehrani H, Arashkia A, Mahdavi S, Bahrami A. Determine the antimicrobial susceptibility of E. coli with multiple drug resistance in outpatients with urinary tract infection in Tehran. Iran J Med Microbiol. 2012;6(9):37-44.

  • 46.

    Arbab Soleimani N, Amini Z, Tajbakhsh E. [The study of attachment factor and biofilm formation of uropathogenic Escherichia coli isolated from patient with urinary tract infection of Semnan Province]. Pajoohandeh J. 2014;18(6):332-6. Persian.

  • 47.

    Tashkori M, Farokhnia M, Zia Sheikhaleslami N, Mirzaei T, Yosefi H, Mokhtari F, et al. [Evaluation of Producing Extended Spectrum β-lactamase among Isolated Escherchia coli from Patients Suffering from Urinary Tract Infections:(Short Report)]. J Rafsanjan Univ Med Sci. 2011;10(1):62-8. Persian.

  • 48.

    Moulana Z, Asgharpour F, Ramezani T. [Frequency of the Bacterial Causing Agents in Urinary Tract Infection and Antibiotic Pattern Samples Sent to Razi Laboratory, Babol 2008-2009: A Short Report]. J Rafsanjan Univ Med Sci. 2013;12(6):489-94. Persian.

  • 49.

    Heidari-Soureshjani E, Heidari M, Doosti A. [Epidemiology of urinary tract infection and antibiotic resistance pattern of E. coli in patients referred to Imam Ali hospital in Farokhshahr, Chaharmahal va Bakhtiari, Iran]. J Shahrekord Univ Med Sci. 2013;15(2):9-15. Persian.

  • 50.

    Soltan Dallal MM, Azarsa M, Shirazi MH, Rastegar Lari A, Owlia P, Fallah Mehrabadi J, et al. The prevalence of extended-spectrum beta-lactamases and CTX-M-1 producing Escherichia coli in urine samples collected at Tabriz city Hospitals. Tehran Univ Med J. 2011;69(5):273-8.

  • 51.

    Sharifi Yazdi K, Soltan Dallal MM. Prevalence study of enterococus and staphylococci resistance to vancomycin isolated from urinary tract infections. Tehran Univ Med J. 2013;71(4):250-8.

  • 52.

    Fesharakinia A, Malekaneh M, Hooshyar H, Aval M, Gandomy-Sany F. [The survey of bacterial etiology and their resistance to antibiotics of urinary tract infections in children of Birjand city]. J Birjand Univ Med Sci. 2012;19(2):208-15. Persian.

  • 53.

    Jalalpour S, Mobasherizade S. The prevalence of ESBLs and antibiotic resistance in Escherichia coli and Klebsia pneumoniae strains isolated from inpatients and outpatients urinary tract infection in Isfahan in 2009-2010. JMW. 2009;2(2):105-11.

  • 54.

    Fallah F, Karimi A, Goudarzi M, Shiva F, Navidinia M, Jahromi MH, et al. Determination of integron frequency by a polymerase chain reaction-restriction fragment length polymorphism method in multidrug-resistant Escherichia coli, which causes urinary tract infections. Microb Drug Resist. 2012;18(6):546-9. doi: 10.1089/mdr.2012.0073. [PubMed: 22816551].

  • 55.

    Khodadoost M, Akya A, Taha A, Mansour S, Adabagher S. [The frequency of antibiotic resistance and CTX-M gene in Escherichia coli isolated from Urinary Tract Infections of out- patients in Kermanshah]. Urmia Med J. 2013;24(5):318-28. Persian.

  • 56.

    Ghadiri K, Ahmadi P, Abiri R, Saidzade S, Babaei H, Salehi A, et al. The MIC Study of Antibiotics Used in the Treatment of Children with Urinary Tract Infections caused by E. coli using E-test and ts Comparison with Disk Diffusion. ZUMS J. 2009;17(67):89-98.

  • 57.

    Sahebnasagh R, Saderi H, Boroumandi S. [Comparison of antibiotic resistance in Escherichia coli isolated from urine of adult patients with regard to gender, age and kind of admission]. Daneshvar Med J(Sci-Res J Shahed Univ). 2015;114:47-55. Persian.

  • 58.

    Safkhani E, Saderi H, Boroumandi S, Faghihzadeh E, Akhavi Rad SM, Moosavi SM. [Bacteria isolated from urine of children with different sex and ages]. Daneshvar Med J(Sci-Res J Shahed Univ). 2014;113:63-71. Persian.

  • 59.

    Barari Sawadkouhi R, Pournasrollah M, Babazadeh N. [Antibiotic Resistance of Bacteria Causing Urinary Tract Infections in Children Hospitalized in Amirkola Children Hospital during 2010-2011]. J Babol Univ Med Sci. 2013;15(5):89-94. Persian.

  • 60.

    Akya A, Gheisari H, Mohammadi G, Khodadost M. [The pattern of plasmids and antibiotic resistance of E. coli isolated from urinary tract infection in outpatient patients]. Sci J Kordestan Univ Med Sci. 2015;20:89-96. Persian.

  • 61.

    Dezfolimanesh Z, Pourmirza Kalhori R, Tohidnia MR. The prevalence and pattern of antibiotic resistance of E. coli producer ESBL in urinary tract infections Imam Reza Kermanshah hospital 2011. Iranian J Infect Dis Trop Med. 2013;18(61):27-32.

  • 62.

    Isvand A, Yahyavi M, Asadi-Samani M, Kooti W, Davoodi-Jouneghani Z. [The study of bacteriological factors and antibiotic resistance in women with UTI referred to the Razi laboratory in Dezful]. J Ilam Univ Med Sci. 2014;22(4):199-205. Persian.

  • 63.

    Esmaeili R, Hashemi H, Moghadam shakib M, Alikhani M, Sohrabi Z. [Bacterial Etiology of Urinary Tract Infections and Determining their Antibiotic Resistance in Adults Hospitalized in or Referred to the Farshchian Hospital in Hamadan]. J Ilam Univ Med Sci. 2014;21(7):281-7. Persian.

  • 64.

    Sedighi I, Solgi A, Amanati A, Alikhani MY. Choosing the correct empirical antibiotic for urinary tract infection in pediatric: Surveillance of antimicrobial susceptibility pattern of Escherichia coli by E-Test method. Iran j microbiol. 2014;6(6):387.

  • 65.

    Hosseini M, Farhangara E, Yousefi Masheof R, Parsavash P. Prevalence and determining of antibiotic-resistant bacteria isolated from urine culture of patients hospitalized (Qazvin). Med Lab J. 2014;8(4):78-81.

  • 66.

    Bagheri H, Najfi F, Behnam Pour N, Gjaemi E. Prevalence of multiple drug resistance in Gram-negative bacteria isolated from urinary tract infections in Gorgan 2011-2012. Med Lab J. 2014;8(4):95-102.

  • 67.

    Molaabaszadeh H, Hajisheikhzadeh B, Mollazadeh M, Eslami K, Mohammadzadeh Gheshlaghi N. [Study of sensibility and antimicrobial resistance in Escherichia coli isolated from urinary tract infection in Tabriz city]. J Fasa Univ Med Sci. 2013;3(2):149-54. Persian.

  • 68.

    Ahangarkani F, Rajabnia R, Shahandashti EF, Bagheri M, Ramez M. Frequency of class 1 integron in Escherichia coli strains isolated from patients with urinary tract infections in north of iran. Mater Sociomed. 2015;27(1):10-2. doi: 10.5455/msm.2014.27.10-12. [PubMed: 25870523]. [PubMed Central: PMC4384837].

  • 69.

    Neamati F, Firoozeh F, Saffari M, Zibaei M. Virulence Genes and Antimicrobial Resistance Pattern in Uropathogenic Escherichia coli Isolated From Hospitalized Patients in Kashan, Iran. Jundishapur J Microbiol. 2015;8(2). e17514. doi: 10.5812/jjm.17514. [PubMed: 25825647]. [PubMed Central: PMC4376973].

  • 70.

    Nasiri Moghadam Z. Sarvey on the sensitivity of E. coli to Amoxicillin and C-otrimoxazole in urinary infections. Asrar-J Sabzevar Univ Med Sci. 2000;7(2):38-42.

  • 71.

    Savadkoohi R, Sorkhi H, Poyrnasrollah M, Khalilian E, Mahdi Pour E. Antibiotics resistance of bacteria causing urinary tract infection in hospitalized patients in University hospital Amirkola – Babol between 84-1381. Iran J Infect Dis Tropical Med. 2007;12(39):25-8.

  • 72.

    Emam Ghoreishi F, Kohanteb J. [Antibiotic resistance pattern of E. coli cause urinary tract infections]. Sci J Jahrom Univ Med Sci. 2014;4(4):1-9. Persian.

  • 73.

    Esmaeili M. Antibiotics for causative microorganisms of urinary tract infections. Iran J Pediatr. 2005;15(2):165-73.

  • 74.

    Sedighi I, Salagi A, Alikhani MY, Emad Momtaz H, Mahini F. [Comparison of two agar disk diffusion methods with Iranian and foreign disks for determining the susceptibility of strains of E. coli isolated from children with urinary tract infection]. Sci J Hamedan Univ Med Sci. 2010;17(1):17-20. Persian.

  • 75.

    Zamanzad B, Naseri F. Comparison of the causative bacteria and antibacterial susceptibility pattern of nosocomial and community-acquired urinary tract pathogens in 13-35 years old women, Shahrekord, 2004. Arak Med Univ J. 2005;8(4):23-30.

  • 76.

    Norouzi J, Kargar M, Pourshahian F, Kamali M. [Study on the prevalence of urinary tract infection by E.coli, antibiotic resistance and plasmid profile of isolated bacteria in Jahrom city]. J Army Univ Med Sci. 2006;4(13):746-50. Persian.

  • 77.

    Nakhaie Moghadam M, Moshrefi S. [Determine the prevalence of antibiotic resistance in urinary isolates of E. coli and ESBLs among them]. J Sabzevar Univ Med Sci. 2010;16(4):228-33. Persian.

  • 78.

    Dipiro J, Talbert R, Yee G, Matzke G, Wells B, Posey L. Pharmacotherapy: A Pathphysiologic Approach. 8 ed. New York: McGraw-HILL; 2011.

  • 79.

    Boucher HW, Talbot GH, Bradley JS, Edwards JE, Gilbert D, Rice LB, et al. Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin Infect Dis. 2009;48(1):1-12. doi: 10.1086/595011. [PubMed: 19035777].

  • 80.

    Linhares I, Raposo T, Rodrigues A, Almeida A. Frequency and antimicrobial resistance patterns of bacteria implicated in community urinary tract infections: a ten-year surveillance study (2000-2009). BMC Infect Dis. 2013;13:19. doi: 10.1186/1471-2334-13-19. [PubMed: 23327474]. [PubMed Central: PMC3556060].

  • 81.

    Garcia-Morua A, Hernandez-Torres A, Salazar-de-Hoyos JL, Jaime-Davila R, Gomez-Guerra LS. Community-acquired urinary tract infection etiology and antibiotic resistance in a Mexican population group. Rev Mex Urol. 2009;69(2):45-8.

  • 82.

    Oladeinde BH, Omoregie R, Olley M, Anunibe JA. Urinary tract infection in a rural community of Nigeria. N Am J Med Sci. 2011;3(2):75-7. doi: 10.4297/najms.2011.375. [PubMed: 22540069]. [PubMed Central: PMC3336890].

  • 83.

    Dibua UM, Onyemerela IS, Nweze EI. Frequency, urinalysis and susceptibility profile of pathogens causing urinary tract infections in Enugu State, southeast Nigeria. Rev Inst Med Trop Sao Paulo. 2014;56(1):55-9. doi: 10.1590/S0036-46652014000100008. [PubMed: 24553609]. [PubMed Central: PMC4085832].

  • 84.

    Chen LF, Chiu CT, Lo JY, Tsai SY, Weng LS, Anderson DJ, et al. Clinical Characteristics and Antimicrobial Susceptibility Pattern of Hospitalized Patients with Community Acquired Urinary Tract Infections at a Regional Hospital in Taiwan. Health Infect. 2013;19(1):20-5. doi: 10.1071/HI13033. [PubMed: 25580164]. [PubMed Central: PMC4288472].

  • 85.

    George CE, Norman G, Ramana GV, Mukherjee D, Rao T. Treatment of uncomplicated symptomatic urinary tract infections: Resistance patterns and misuse of antibiotics. J Family Med Prim Care. 2015;4(3):416-21. doi: 10.4103/2249-4863.161342. [PubMed: 26288784]. [PubMed Central: PMC4535106].

  • 86.

    Kalsoom B, Jafar K, Begum H, Munir S, ul AKBAR N, Ansari JA, et al. Patterns of antibiotic sensitivity of bacterial pathogens among urinary tract infections (UTI) patients in a Pakistani population. Afr J Microbiol Res. 2012;6(2):414-20.

  • 87.

    Cohen R, Gillet Y, Faye A. [Synthesis of management of urinary tract infections in children]. Arch Pediatr. 2012;19:S124-8. French. doi: 10.1016/s0929-693x(12)71285-x.

  • 88.

    Kothari A, Sagar V. Antibiotic resistance in pathogens causing community-acquired urinary tract infections in India: a multicenter study. J Infect Dev Ctries. 2008;2(5):354-8. [PubMed: 19745502].

  • 89.

    Kader AA, Kumar A, Dass SM. Antimicrobial resistance patterns of gram-negative bacteria isolated from urine cultures at a general hospital. Saudi J Kidney Dis Transpl. 2004;15(2):135-9. [PubMed: 17642764].

  • 90.

    Yolbas I, Tekin R, Kelekci S, Tekin A, Okur MH, Ece A, et al. Community-acquired urinary tract infections in children: pathogens, antibiotic susceptibility and seasonal changes. Eur Rev Med Pharmacol Sci. 2013;17(7):971-6. [PubMed: 23640446].

  • 91.

    Lee DS, Choe HS, Lee SJ, Bae WJ, Cho HJ, Yoon BI, et al. Antimicrobial susceptibility pattern and epidemiology of female urinary tract infections in South Korea, 2010-2011. Antimicrob Agents Chemother. 2013;57(11):5384-93. doi: 10.1128/AAC.00065-13. [PubMed: 23959315]. [PubMed Central: PMC3811252].

  • 92.

    Abejew AA, Denboba AA, Mekonnen AG. Prevalence and antibiotic resistance pattern of urinary tract bacterial infections in Dessie area, North-East Ethiopia. BMC Res Notes. 2014;7:687. doi: 10.1186/1756-0500-7-687. [PubMed: 25280498]. [PubMed Central: PMC4195856].

  • 93.

    Majumder MI, Ahmed T, Hossain D, Begum SA. Bacteriology and antibiotic sensitivity patterns of urinary tract infections in a tertiary hospital in Bangladesh. Mymensingh Med J. 2014;23(1):99-104. [PubMed: 24584381].

  • 94.

    Stratchounski LS, Rafalski VV. Antimicrobial susceptibility of pathogens isolated from adult patients with uncomplicated community-acquired urinary tract infections in the Russian Federation: two multicentre studies, UTIAP-1 and UTIAP-2. Int J Antimicrob Agents. 2006;28 Suppl 1:S4-9. doi: 10.1016/j.ijantimicag.2006.05.015. [PubMed: 16829055].

  • 95.

    Hickerson AD, Carson CC. The treatment of urinary tract infections and use of ciprofloxacin extended release. Expert Opin Investig Drugs. 2006;15(5):519-32. doi: 10.1517/13543784.15.5.519. [PubMed: 16634690].

  • 96.

    Lo DS, Shieh HH, Ragazzi SL, Koch VH, Martinez MB, Gilio AE. Community-acquired urinary tract infection: age and gender-dependent etiology. J Bras Nefrol. 2013;35(2):93-8. doi: 10.5935/0101-2800.20130016. [PubMed: 23812565].

  • 97.

    Kamenski G, Wagner G, Zehetmayer S, Fink W, Spiegel W, Hoffmann K. Antibacterial resistances in uncomplicated urinary tract infections in women: ECO.SENS II data from primary health care in Austria. BMC Infect Dis. 2012;12:222. doi: 10.1186/1471-2334-12-222. [PubMed: 22989349]. [PubMed Central: PMC3520812].

  • 98.

    Renuart AJ, Goldfarb DM, Mokomane M, Tawanana EO, Narasimhamurthy M, Steenhoff AP, et al. Microbiology of urinary tract infections in Gaborone, Botswana. PLoS One. 2013;8(3). e57776. doi: 10.1371/journal.pone.0057776. [PubMed: 23469239]. [PubMed Central: PMC3587627].

  • 99.

    Mukherjee M, BaSu S, MuKherjee SK, MajuMder M. Multidrug-Resistance and Extended Spectrum Beta-Lactamase Production in Uropathogenic E. coli which were Isolated from Hospitalized Patients in Kolkata, India. J CLIN DIAGNOs RES. 2013. doi: 10.7860/jcdr/2013/4990.2796.

  • 100.

    Hoban DJ, Nicolle LE, Hawser S, Bouchillon S, Badal R. Antimicrobial susceptibility of global inpatient urinary tract isolates of Escherichia coli: results from the Study for Monitoring Antimicrobial Resistance Trends (SMART) program: 2009-2010. Diagn Microbiol Infect Dis. 2011;70(4):507-11. doi: 10.1016/j.diagmicrobio.2011.03.021. [PubMed: 21767706].

  • 101.

    Lutter SA, Currie ML, Mitz LB, Greenbaum LA. Antibiotic resistance patterns in children hospitalized for urinary tract infections. Arch Pediatr Adolesc Med. 2005;159(10):924-8. doi: 10.1001/archpedi.159.10.924. [PubMed: 16203936].

  • 102.

    Daoud Z, Afif C. Escherichia coli Isolated from Urinary Tract Infections of Lebanese Patients between 2000 and 2009: Epidemiology and Profiles of Resistance. Chemotherapy Res Pract. 2011;2011:1-6. doi: 10.1155/2011/218431.

  • 103.

    Guidoni EB, Berezin EN, Nigro S, Santiago NA, Benini V, Toporovski J. Antibiotic resistance patterns of pediatric community-acquired urinary infections. Braz J Infect Dis. 2008;12(4):321-3. [PubMed: 19030734].

  • 104.

    Arredondo-Garcia JL, Soriano-Becerril D, Solorzano-Santos F, Arbo-Sosa A, Coria-Jimenez R, Arzate-Barbosa P. Resistance of uropathogenic bacteria to first-line antibiotics in mexico city: A multicenter susceptibility analysis. Curr Ther Res Clin Exp. 2007;68(2):120-6. doi: 10.1016/j.curtheres.2007.03.005. [PubMed: 24678125]. [PubMed Central: PMC3966000].

  • 105.

    Sharmin S, Alamgir F, Fahmida M, Saleh AA. Antimicrobial sensitivity pattern of uropathogens in children. Bangladesh J Med Microbiol. 2010;3(2):18-22. doi: 10.3329/bjmm.v3i2.5322.

  • 106.

    Magliano E, Grazioli V, Deflorio L, Leuci AI, Mattina R, Romano P, et al. Gender and age-dependent etiology of community-acquired urinary tract infections. Sci World J. 2012;2012:349597. doi: 10.1100/2012/349597. [PubMed: 22629135]. [PubMed Central: PMC3351074].

  • 107.

    Karlowsky JA, Lagace-Wiens PR, Simner PJ, DeCorby MR, Adam HJ, Walkty A, et al. Antimicrobial resistance in urinary tract pathogens in Canada from 2007 to 2009: CANWARD surveillance study. Antimicrob Agents Chemother. 2011;55(7):3169-75. doi: 10.1128/AAC.00066-11. [PubMed: 21537027]. [PubMed Central: PMC3122429].

  • 108.

    Barisic, Z , Babic-Erceg, A , Borzic, E , Zoranic, V , Kaliterna, V , Carev, M . Urinary tract infections in South Croatia: aetiology and antimicrobial resistance. Int J Antimicrob Ag. 2003;22:61-4. doi: 10.1016/s0924-8579(03)00233-4.

  • 109.

    Wolff O, Maclennan C. Evidence behind the WHO guidelines: hospital care for children: what is the appropriate empiric antibiotic therapy in uncomplicated urinary tract infections in children in developing countries? J Trop Pediatr. 2007;53(3):150-2. doi: 10.1093/tropej/fmm030. [PubMed: 17517816].

  • COMMENTS

    LEAVE A COMMENT HERE: