|Year : 2019 | Volume
| Issue : 3 | Page : 102-109
Bacterial causes of community-acquired and nosocomial urinary tract infection in type 2 diabetes: A comparative approach
E Premprakash Patra1, Sonam Karna1, Dayanidhi Meher2, Srilekha Mishra1
1 Applied Research Laboratory, School of Biotechnology, KIIT Deemed to be University, Bhubaneswar, Odisha, India
2 Department of Endocrinology, Kalinga Institute of Medical Sciences, Bhubaneswar, Odisha, India
|Date of Web Publication||27-Aug-2019|
Dr. Srilekha Mishra
Applied Research Laboratory, School of Biotechnology, KIIT Deemed to be University, Bhubaneswar - 751 023, Odisha.
Source of Support: None, Conflict of Interest: None
Introduction: Urinary tract infection (UTI) in type 2 diabetes (T2D) is one of the most common infectious diseases diagnosed both in community and in hospital. Due to increased prevalence of disease and rising antibiotic resistance among uropathogens, it is important to have local community- and hospital-based knowledge of the organisms causing UTI in T2D and their sensitivity pattern to choose correct treatment regimen. Methodology: Samples were collected from both Outpatient Department (OPD) and Inpatient Department (IPD) of endocrinology, KIMS. The study was selected to compare the prevalence among the bacterial isolates from community-acquired UTI (CUTI) and nosocomial UTI (NUTI) in T2D individuals and compare the antibiogram pattern. Results: Of the total 92 culture-positive samples, 40 were CUTI and 52 were NUTI. Culture positivity was directly proportional to the presence of increased number of pus cell and glycaemic status. The most commonly isolated bacterium was Escherichia coli both in OPD and IPD followed by Enterococcus, Staphylococcus saprophyticus, Staphylococcus aureus, Klebsiella spp., Pseudomonas aeruginosa and Proteus species except the Citrobacter spp. and Candida spp. which were isolated from ward patients. Conclusion: There was no significant difference of resistance pattern between CUTI and NUTI. Inappropriate use of antibiotics results in increase of antibiotic resistance, and hence, proper care should be taken regarding infection treatment guidelines promoting rational antibiotic prescribing in hyperglycaemic UTI cases.
Keywords: Antibiotic resistance, hyperglycaemia, puss cells
|How to cite this article:|
Patra E P, Karna S, Meher D, Mishra S. Bacterial causes of community-acquired and nosocomial urinary tract infection in type 2 diabetes: A comparative approach. J Diabetol 2019;10:102-9
|How to cite this URL:|
Patra E P, Karna S, Meher D, Mishra S. Bacterial causes of community-acquired and nosocomial urinary tract infection in type 2 diabetes: A comparative approach. J Diabetol [serial online] 2019 [cited 2020 Jan 20];10:102-9. Available from: http://www.journalofdiabetology.org/text.asp?2019/10/3/102/265412
| Introduction|| |
Urinary tract infection (UTI) is a common bacterial infection known to affect the different parts of the urinary tract accounting for large antimicrobial drug consumption. About 150 million UTI cases were diagnosed every year., UTI is mainly defined as the colonisation of mixed population of microorganisms colonising in the urinary tract through which the urine flows from the kidneys to bladder to outside. From microbiological perspective, UTI can happen anywhere including the bladder, kidneys, urethra and ureters. UTI can be classified into community acquired and hospital acquired (nosocomial UTI [NUTI]). According to Hackett in 2005, about 70% UTI cases were community acquired. Uncomplicated community-acquired UTI (CUTI) was more common and mainly related to hospital visits and no catheter-associated infection. NUTI is the infection acquired by the patient during hospital stay, which was not present earlier or at the time of admission. NUTI is generally symptomatic and catheter-associated infection. UTI accounts for about 50% nosocomial infections with 80% cases caused due to catheterisation. Increased blood glucose level results in symptomatic and asymptomatic UTI. Type 2 diabetes (T2D) patients are not only community-acquired but also exhibit hospital-acquired infections, particularly catheter associated. T2D is also associated with worse outcomes of UTI, including longer hospitalisations and increased mortality. An observational study of all patients with T2D in the UK general practice research database found that the incidence rate of UTI was 46.9/1000 person-years among diabetic patients and 29.9 for patients without diabetes. Another American database study from 2014 found that a UTI diagnosis was more common in men and women with diabetes than in those without diabetes. The patients suffering from diabetes mellitus are generally more susceptible to infections and these infections are likely to be more severe than in the non-diabetics. T2D is the most common condition of diabetes and the current observation shows that its profile in India is just beginning to emerge. In the present study, the frequency of UTI in diabetic patients of both outpatient department (OPD) and inpatient department (IPD) of various hospitals has been studied. We hypothesise that, in the developing world, factors limiting access to care and those which may increase the likelihood of developing UTI, result in increased morbidity. Due to arising antibiotic resistance, it is important to have local community- and hospital-based knowledge of the organisms causing UTI and their sensitivity pattern to choose correct treatment regimen. The main objectives were to study the quantum and incidence of UTI and antibiogram among the bacterial isolates of both CUTI and NUTI in T2D patients and to evaluate the various factors which predispose to its development.
| Methodology|| |
The study was purely a cross-sectional type and carried out in the Department of Applied research laboratory at KIIT School of Biotechnology, KIIT University.
Selection criteria of study subjects
The patients fulfilling the inclusion criteria were enrolled in the study.
Inclusion criteria for community-acquired urinary tract infection
Clinically suspected CUTI T2D cases were selected on the basis of following cardinal signs/symptoms (CDC criteria) (Savas et al., 2006).
- Urgency, frequency, dysuria, suprapubic tenderness, fever (>100.4°C) and pyuria
- T2D complications such as nephropathy, retinopathy, periodontal and all established T2D individuals with blood sugar level, fasting blood glucose (FBS) >150, post-prandial blood sugar (PPBS) >200 and glycosylated haemoglobin (HbA1c) >7.
Inclusion criteria for nosocomial urinary tract infection
Suspected cases of hospital-acquired T2D UTI were selected on the basis of as follows: (i) patient was not suffering from UTI at the time of hospital admission, (ii) UTI developed at least 72h after admission in hospital and (iii) Patients with indwelling catheter. This also includes inclusion criteria of CUTI.
Exclusion criteria for community-acquired urinary tract infection and nosocomial urinary tract infection
Individuals including chronic smokers and alcoholic, having chronic infection (HIV, hepatitis C virus and hepatitis B virus) and receiving any local or systemic treatment with glucocorticoids or antihistamines within 2 weeks before samples were excluded from the study. Those having immunisation within the past 4 weeks were also excluded from the study.
A total of 400 samples were randomly taken out, of which 200 clinically suspected NUTI and CUTI individuals with established T2D were selected from both OPD and IPD of the hospitals for the study based on the selection criteria. The samples were collected after getting ethical clearance and written consent from the individuals as per instructions from the clinicians. Biochemical and anthropological parameters were obtained from the questionnaires provided to the patients. The study included 100 T2D individuals from OPD and 100 from IPD.
The mid-stream urine samples were collected from patients from both OPD and IPD in urine collection vials. In IPD cases, first 10ml of urine samples were collected because the catheter was pre-attached by the manufacturer to the 10ml specimen collection container with identification label affixed to the specimen container and dated. Urine was collected in specimen vials and kept at room temperature for immediate culture and transported to the laboratory for further processing. In case of any adverse situation, the urine sample collected was kept at 4°C to inhibit further growth of bacteria.
Examination of urine sample
Urine sample was transferred to a microcentrifuge tube and it was centrifuged at 10,000rpm for 5min. The residual part was collected and pipetted out on a clean slide, and a smear was made to find the number of pus cells. The normal value of a puss cell varies from 5 to 8 in male and 10 for women.
A loopful of urine sample was taken and streaked to different types of media such as UTI agar (Himedia), blood agar (Himedia), MacConkey agar (Himedia) and brain–heart infusion agar (Himedia). The colonies on the media were confirmed by Gram staining and biochemical tests., Antimicrobial sensitivity of the isolates was performed using Kirby–Bauer Method. The diagnosis of UTI was made as per the standard procedures. Cultures having colony counts >103–105 CFU/ml and pyuria (>5 pus cells/HPF) were symptomatic and considered as culture positive. Occurrence of a pure colony of a single potential pathogen was also considered to be significant regardless of the colony forming units.
Data were expressed in terms of mean, standard deviation and percentages. Student’s t-test, Z test and Chi-square test were used as required; P < 0.05 was considered statistically significant. Analysis was performed using the Statistical Package for the Social Sciences (SPSS) version 10.0 (SPSS, IBM, USA).
| Results|| |
The study was carried out on urine samples from 200 T2D individuals both from OPD and IPD of different hospitals in and around Bhubaneswar region from January to May 2017. The study population was classified according to glycaemic status with controlled glycaemia (HbA1C <6.5) and uncontrolled glycaemia (HbA1C >7). Main characteristics of the study population are summarised in [Table 1]. A total of 200 (n = 200) UTI cases were studied to isolate bacteria from urine samples, of which 100 were from NUTI and 100 from CUTI cases. Basic parameters such as age, sex, body mass index (BMI), duration of disease and blood sugar level (FBS, PPBS and HbA1C) were also recorded. The mean age group of individuals was equal (49.49 ± 12.5) in both the settings. However, a significant difference was observed between gender groups. Females had a higher percentage of UTI in both CUTI (65%) and NUTI (82%) than the males (P = 0.005). BMI did not exhibit any significant difference between the cohorts, but BMI >25 was increased in NUTI (45%) than CUTI (38%) T2D individuals. However, cases with BMI <25 were increased in NUTI (62%) than CUTI (55%) T2D individuals. T2D individuals admitted to hospitals with uncontrolled sugar level exhibited higher degrees of UTI (86%) than the individuals visiting hospitals (72%) for checkup. A significant difference was observed in glycaemic level (P = 0.012). Ninety-seven (48.5%) cases were newly diagnosed for T2D or <5 years were having UTI. Most of the individuals were nosocomial (58%) with respect to community (39%). 43% were in the range of 5–10 years where 51% of CUTI and 35% of NUTI cases were found. Here, more number of diabetic CUTI cases had infection than NUTI cases. Similarly, 6.5%, 1.5% and 0.5% of cases had infection with 11–15 years, 16–20 years and >20 years of duration of diabetes, respectively. There was also a significant difference between the study groups with duration of diabetes (P = 0.02). Of total 200 culture of T2D patients, 92 (46%) became positive. Of 100 CUTI, 40% were culture positive and of 100 NUTI, 52% were culture positive (0.05). The individuals were found to produce symptoms such as dysuria (11.5%), urgency (13%), pyelonephritis (0.04%), cystitis (0.03%), prostatitis (0.02%) and urethritis (0.06%) while most cases were asymptomatic (59.5%). The frequency was more in nosocomial cases.
The presence of puss cells detects the severity of UTI. [Table 2] shows a relationship between pyuria and culture positivity. Culture positivity was found to be directly proportional to pus cell as well as glycaemic status (P = 0.005).
|Table 2: Relationship between pyuria and urine culture in community-acquired urinary tract infections and nosocomial urinary tract infections type-2 diabetic patients|
Click here to view
[Table 3] shows the culture positivity of UTI among the genders with reference to blood sugar level in CUTI and NUTI individuals. Culture positivity among uncontrolled females was 38% and 17.39% in NUTI and CUTI, respectively, whereas males exhibited 16.3% and 10.8% in CUTI and NUTI. There was a significant difference between the genders of varying glycaemic status.
|Table 3: Age and sex distribution of patients with positive cultures in community-acquired urinary tract infections and nosocomial urinary tract infections individuals according to glycaemic status|
Click here to view
Among the isolated organisms, Escherichia More Details coli was responsible as the leading cause for both the UTI in T2D cases with a higher prevalence of 32.18% in NUTI and 28.8% in CUTI cases [Figure 1]a and [Figure 1]b. Enterococcus was also found to be isolated in high frequency in both the groups (20.6% in NUTI and 22.2% in CUTI). Staphylococcus aureus (CUTI = 11.1% and NUTI = 12.6%), Staphylococcus saprophyticus (NUTI = 8% and CUTI = 1.4%), Klebsiella (NUTI = 16.09% and CUTI = 15.5%) and Proteus (NUTI = 6.8% and CUTI = 4.4%) were common for both UTI. However, Candida (1.1%) and Citrobacter (1.1%) were isolated only in NUTI cases but absent in cultures of CUTI individuals.
|Figure 1: (a) Distribution of bacterial isolates causing urinary tract infection in type-2 diabetes among community-acquired urinary tract infection. Bacteria isolated from community-acquired urinary tract infection were seen. Escherichia coli was the most dominant and prevalent bacteria among the type-2 diabetes patients visiting hospitals followed by Enterococcus, Klebsiella and Staphylococcus aureus. (b) Distribution of bacterial isolates causing urinary tract infection in type-2 diabetes among nosocomial urinary tract infection. Bacteria isolated from nosocomial urinary tract infection were seen. Citrobacter and Candida spp. were also isolated from the ward cases which were absent in outpatient cases. Escherichia coli was also the dominant organism found followed by Enterococcus, Klebsiella and Staphylococcus aureus|
Click here to view
[Table 4] shows the antibiogram resistance pattern of the isolates against different antibiotics. E. coli was less sensitive to commonly used drugs such as cefotaxime, vancomycin, trimethoprim and ciprofloxacin. Tetracycline and erythromycin were the most sensitive against E. coli. Similarly, S. aureus showed multidrug resistance to amoxicillin, trimethoprim, tetracycline and ciprofloxacin. Enterococcus also showed more than 50% resistance to many antibiotics such as amikacin, amoxicillin, tetracycline, erythromycin, ciprofloxacin and trimethoprim. In our study, we found Klebsiella showing more than 50% resistance to more than one drugs and 100% sensitivity to cefotaxime, tetracycline and trimethoprim. Proteus was also found to be the multidrug-resistant (MDR) strain to majority of antibiotics such as amoxicillin, erythromycin and ciprofloxacin. Pseudomonas showed resistance to amoxicillin and vancomycin in both types of UTI. Similarly, Citrobacter was found only in ward patients who showed 100% resistance to most antibiotics such as amoxicillin, vancomycin and trimethoprim. Candida spp. known to be the most common and risk of UTI was found to be resistant to all antibiotics.
|Table 4: Resistance pattern of urinary isolates against antibiotics in community-acquired urinary tract infections and nosocomial urinary tract infections in type-2 diabetic individuals|
Click here to view
| Discussion|| |
Despite the widespread availability of antibiotics, UTI remains the most common bacterial infection in the human population. Although the majority of infections are acute and short lived, they contribute to the significant amount of morbidity in the population.
The clinical characteristics of the study population show that females were more predominant having UTI which is correlated with the previous studies of Al Benwan et al., 2010, thereby confirming adult women have higher rate of UTI than men. BMI and age do not have an effect on UTI in both settings. Furthermore, most of the UTI were found in T2D patients having uncontrolled glycaemia (79%) in agreement of the reports suggesting this trend when comparing diabetic patients and non-diabetic patients with normal glycaemia. This also supports the finding of Wilke et al. who found higher incidence of UTI in T2D patients with poor glycaemic control. Duration of T2D is a specific risk factor for T2D and it also showed a significant difference in NUTI and CUTI. The results were similar to findings of Isikgoz Tasbakan et al. where he found more frequency of UTI in hospital-acquired cases and basically in ICUs.
The rate of culture positivity increases with increasing number of pus cells and glycaemic status. The study was found to be associated with the reports of Anushree and Chandrakanth where 38.4% of cases showed significant bacterial growth. They also suggested pyuria as a good indicator of inflammatory response. Our reports are higher (63.9%) than the studies of Mamun Mahmud et al. where they found 60.82% of culture-positive cases in pyuric diabetic patients.
Our study showed higher percentage (46%) of positive cultures from T2D patients obtained from the community and the hospital than 20%–30% commonly reported in diabetic patients which showed only 35% culture-positive cases.
The male:female ratio was found to be 1:2.7 which is quite higher than the reports of Majeed et al. where the ratio was 1:1.6. In both the UTIs, females were affected more which are in accordance to reports of Tada et al. Men are less prone to UTI than female due to the longer course of the urethra and bacteriostatic properties of prostatic secretions. Uncontrolled glycaemic group has about more incidence of UTI with increase in age as compared to controlled glycaemics. This may be due to poor circulation in T2D reducing the ability of infection-fighting white blood cells to get where they need to go and unable to ingest the offending bacteria. Complicated diabetic patients admitted to hospitals have dysfunctional bladders that contract poorly which allows urine to remain in static pools providing luxurious ponds of bacteria. In our study, we got more number of positive cultures in uncontrolled females admitted to hospitals (38.04%) with predominant age group between 45–54 and 55–60. This supports the finding of Al Benwan et al. confirming the adult women have higher rate of UTI than men in diabetic population. While Linhares et al. suggested higher incidence of female UTI in hospital settings which confirms our finding. The prevalence of NUTI in male group after 50 years might be caused by the higher incidence of urinary tract pathologies such as prostate diseases. As most of the previous studies on UTI in diabetic patients are carried out, there is limited evidence on describing UTI aspects in male with CUTI and NUTI. To the best of our knowledge, this is the first report from eastern part of India to compare effect of glycaemic control on NUTI and CUTI in both genders.
An American study showed that the proposition of E. coli in the current decade has risen significantly, it accounted for trending increase of resistance of E. coli. These findings were in agreement with the study done by Sharmin et al. Another study done by Hasan et al. showed 50.7% incidence of NUTI caused by E. coli, which was nearer to our study. In the prevalence study carried out in Turkey showed that E. coli (32.4%) was mostly responsible for NUTI, and in Anbumani and Mallika study, it was 33%. Enterococccus (22%) and S. aureus (12%) supports the reports of Chihara et al. describing the occurrence of S. aureus bacteraemia in urine cultures to identify patients at high risk of death in hospitalised patients. Enterococcal species in CUTIs agrees to the finding of reports in 2011 by issue of renal and urology news.
Although the spectrum of pathological bacteria isolated from the urine of patients across the globe remained largely unchanged over the past few decades, there have been dramatic changes in the resistance pattern and sensitivity profile in most countries. In our study, antibiogram of urinary pathogens isolated from community and ward patients reveals that E. coli were less sensitive to commonly used drugs such as cefotaxime, vancomycin, trimethoprim and ciprofloxacin. Tetracycline (100%) and erythromycin (100%) were the most sensitive against E. coli that is in agreement with the reports of Abejew et al. who stated E. coli and Pseudomonas to be sensitive to and resistant to various drugs. The results were similar to reports of Sabir et al. where the resistance was about 100% in amoxycillin, 89.7% in cefotaxime and 12.7% to amikacin. The resistance of S. aureus showing 80% multidrug resistance to amoxycillin and trimethoprim, tetracycline and ciprofloxacin was similar to Onanuga and Awhowho who stated that S. aureus isolated by them from the UTI patients showed resistant to tetracycline and vancomycin. S. saprophyticus was the only organism which showed 100% sensitivity to all antibiotics. However, it is supported by other studies where S. saprophyticus was isolated from females of which highest rate, isolation was among female of 18–45 years age group they saw a high rate of sensitivity pattern with different antibiotics. Enterococcus showing more than 50% resistance to many antibiotics used were contrast to studies of Barros et al. which showed Enterococcus sensitive to amoxicillin (78%) and trimethoprim (64%) and 62% resistant to ciprofloxacin and vancomycin. In our study, we found Klebsiella showing more than 50% resistance to more than one drugs and 100% sensitivity to cefotaxime, tetracycline and trimethoprim which are found in the reports of El Bouamri et al. stating 51% resistance to amoxicillin, 86% to cefotaxime and 62% amikacin. According to reports of Manikandan and Amsath, resistance of Klebsiella to amoxycillin was about 88.9% was a contrast to our study. Candida, Proteus and Citrobacter were also found to be the MDR-resistant strain to antibiotics such as amoxicillin, erythromycin and ciprofloxacin which correlate the results of Biswas et al. where resistance to these antibiotics were about 70%–80%. Candida spp. Known to be the most common and risk of UTI was found to be resistant to all antibiotics. However, no studies define the sensitivity of the Candida sp. Instead in some reports, it is recommended to use antifungals like fluconazole.
| Conclusion|| |
In Odisha, E. coli is still the leading cause of UTI in T2D patients, along with its increasing resistance pattern to various antibiotics and is going to be an alarming health hazard. Most other urinary pathogen shows almost the same picture in the present study. It is revealed in our study that the findings of significant number of pus cells are not always the evidence for UTI; rather somewhere pus cell less than significant number is also indicative. The major responsibility goes to catheterisation in various durations causing NUTI by different microorganisms. The changing scenario of resistant pathogen of both the UTIs is the extract of this study. In our study, the difference in the resistance pattern between the NUTI and CUTI is found insignificant. This may be due to resistance of antibiotics in individuals which is carried from community to hospital and vice-versa. Hence, the larger amount of antibiotic consumption and its irrational and indiscriminate use losing even the last weapon to fight against UTI.
The study also gives evidence of differences in the etiological agents in Odisha as compared to other regions which highlight the need for proper use of antibiotics in diabetic patients, particularly. However, despite these limitations, we have also shown clear difference in the correlation between the UTI and age which seem to be directly affected by glycaemic control. Moreover, the resistance pattern and etiological agents and its prevalence vary from that of developed countries also shown in our study. This study has revealed the alarming level of resistance (even ciprofloxacin) achieved by bacteria involved in causing UTI. The truth revealed from the study will help the physicians to prescribe the drugs cautiously for the betterment of the patients. It is one of the few studies comparing the CUTI and NUTI in T2D patients ever done which will act as an evidence for the future research. It is recommended that antibiotics should be used after doing a routine microscopy and culture/sensitivity of urine to inhibit acquisition and spread of drug resistance by the bacteria. Antimicrobial policy should be adopted at both the tertiary level hospital and national level supervised by monitoring cell for taking necessary steps to minimise the drug resistance. Although utmost sincerity and dedication were invested to carry out the study, it could not go beyond limitations as the sample size was not large enough, moreover, the genetic analysis of resistant bacteria that could help finding the actual cause behind the emerging drug resistance, we could not do that due to lack of proper logistic support.
We would like to thank the Department of Biotechnology, Government of India, for providing financial support to carry out this study. We are also thankful to all the study participants as well as staff and management of hospitals where samples were collected.
Financial support and sponsorship
This study was financially supported by Department of Biotechnology, Government of India.
Conflicts of interest
There are no conflicts of interest.
| References|| |
Dias Neto JA, Silva LD, Martins AC, Tiraboschi RB, Domingos AL, Suaid HJ, et al
. Prevalence and bacterial susceptibility of hospital acquired urinary tract infection. Acta Cir Bras 2003;18:36-8.
Akram M, Shahid M, Khan AU. Etiology and antibiotic resistance patterns of community-acquired urinary tract infections in J N M C hospital Aligarh, India. Ann Clin Microbiol Antimicrob 2007;6:4.
Simon H. Urinary Tract Infection in Depth. In Depth Health Articles ADAM, 2006 Review Date; 2006.
Hackett G. 2005 Urinary Tract Infection (UTI). Updated; October 2005.
Tankhiwale SS, Jalgaonkar SV, Ahamad S, Hassani U. Evaluation of extended spectrum beta lactamase in urinary isolates. Indian J Med Res 2004;120:553-6.
Malmartel A, Ghasarossian C. Epidemiology of urinary tract infections, bacterial species and resistances in primary care in France. Eur J Clin Microbiol Infect Dis 2016;35:447-51.doi: 10.1007/s10096-015-2560-1.
Foon R, Toozs-Hobson P, Latthe P. Prophylactic antibiotics to reduce the risk of urinary tract infections after urodynamic studies. Cochrane Database Syst Rev 2012. doi: 10.1002/14651858.CD008224.pub2.
Hammar N, Farahmand B, Gran M, Joelson S, Andersson SW. Incidence of urinary tract infection in patients with type 2 diabetes. Experience from adverse event reporting in clinical trials. Pharmacoepidemiol Drug Saf 2010;19:1287-92.
Hooton TM, Besser R, Foxman B, Fritsche TR, Nicolle LE. Acute uncomplicated cystitis in an era of increasing antibiotic resistance: A proposed approach to empirical therapy. Clin Infect Dis 2004;39:75-80.
Bartholomew JW, Mittwer T. The Gram stain. Bacteriol Rev 1952;16:1-29.
Forbes BA, Daniel F. Sahm DF, Alice S. Weissfeld. St. Louis, Bailey and Scott’s Diagnostic Microbiology, Eleventh Edition. MO: Mosby, 2002, 1069 pp. ISBN 0-323-01678-2.
Bauer AW, Kirby WM, Sherris JC, Turck M. Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 1966;45:493-6.
Saber MH, Barai L, Haq JA, Jilani MS, Begum J. The pattern of organism causing urinary tract infection in diabetic and non diabetic patients in Bangladesh. Bangladesh J Med Microbiol 2010;4:6-8.
Gupta V, Yadav A, Joshi RM. Antibiotic resistance pattern in uropathogens. Indian J Med Microbiol 2002;20:96-8.
] [Full text]
Stamm WE, Kasper DL, Braunwald E, Fauce AS, Hauser S, Longo DL, et al
. Urinary Tract Infection and Pylonepritis in Harrisons Principles of Internal Medicine. 16th
ed. New York: Mc Graw Medical Publishing Division; 2005. p. 1715-9.
Al Benwan K, Al Sweih N, Rotimi VO. Etiology and antibiotic susceptibility patterns of community- and hospital-acquired urinary tract infections in a general hospital in Kuwait. Med Princ Pract 2010;19:440-6.
Wilke T, Boettger B, Berg B, Groth A, Mueller S, Botteman M, et al
. Epidemiology of urinary tract infections in type 2 diabetes mellitus patients: An analysis based on a large sample of 456,586 German T2DM patients. J Diabetes Complications 2015;29:1015-23.
Isikgoz Tasbakan M, Durusoy R, Pullukcu H, Sipahi OR, Ulusoy S; 2011 Turkish Nosocomial Urinary Tract Infection Study Group, et al
. Hospital-acquired urinary tract infection point prevalence in Turkey: Differences in risk factors among patient groups. Ann Clin Microbiol Antimicrob 2013;12:31.
Anushree CN, Chandrakanth VM. Relationship between pyuria and bacteruria in suspected urinary tract infection. Medica 2014;3:65.
Mamun Mahmud H, Qureshi S, Kumar D, Farman S. Pyuric diabetic patients: A tertiary centre experience from Karachi. Pak J Med Sci 2014;30:77-80.
Sewify M, Nair S, Warsame S, Murad M, Alhubail A, Behbehani K, et al
. Prevalence of urinary tract infection and antimicrobial susceptibility among diabetic patients with controlled and uncontrolled glycemia in Kuwait. J Diabetes Res 2016;2016:6573215.
Majeed N, Nair AV. Comparison of bacteriological profile and antibiotic susceptibility pattern of community acquired and nosocomial urinary tract infection. J Dent Med Sci 2017;16:69-72.
Tada DG, Gandhi PJ, Patel KN. A study on antibiotic related resistance in UTI patients: A comparison between community acquired and hospital acquired E. coli
. Natl J Community Med 2012;3:255-8.
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.
Dyer IE, Sankary TM, Dawson JA. Antibiotic resistance in bacterial urinary tract infections, 1991 to 1997. West J Med 1998;169:265-8.
Sharmin S. Use of Chromogenic Media (Urochrom II) for Detection of Uropathogen. M. Phil (Microbiology) Thesis; 2005. p. 55-68.
Hasan AS, Nair D, Kaur J, Baweja G, Deb M, Aggarwal P, et al
. Resistance patterns of urinary isolates in a tertiary Indian hospital. J Ayub Med Coll Abbottabad 2007;19:39-41.
Leblebicioglu H, Esen S, Turkish Nosocomial Urinary Tract Infection Study Group. Hospital-acquired urinary tract infections in Turkey: A nationwide multicenter point prevalence study. J Hosp Infect 2003;53:207-10.
Anbumani N, Mallika M. Antibiotic resistance pattern in uropathogens in a tertiary care hospital. Indian J Pract Doctor 2001;4:204-7.
Chihara S, Popovich KJ, Weinstein RA, Hota B. Staphylococcus aureus
bacteriuria as a prognosticator for outcome of Staphylococcus aureus
bacteremia: A case-control study. BMC Infect Dis 2010;10:225.
Kadri SM, Gash B, Rukhsana A. Antibiotic sensitivity and resistance profile of the micro-organisms responsible for urinary tract infection observed in Kashmir, India. J Indian Med Assoc 2002;100:656, 658-60.
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.
Sabir S, Ahmad Anjum A, Ijaz T, Asad Ali M, Ur Rehman Khan M, Nawaz M, et al
. Isolation and antibiotic susceptibility of E
from urinary tract infections in a tertiary care hospital. Pak J Med Sci 2014;30:389-92.
Onanuga A, Awhowho GO. Antimicrobial resistance of Staphylococcus aureus
strains from patients with urinary tract infections in Yenagoa, Nigeria. J Pharm Bioallied Sci 2012;4:226-30.
Jhora ST, Paul S. Urinary tract Infections caused by Staphylococcus saprophyticus
and their antimicrobial sensitivity pattern in young adult women. Bangladesh J Med Microbiol 2011;5:21-5.
Barros M, Martinelli R, Rocha H. Enterococcal urinary tract infections in a university hospital: Clinical studies. Braz J Infect Dis 2009;13:294-6.
El Bouamri MC, Arsalane L, El Kamouni Y, Zouhair S. Antimicrobial susceptibility of urinary Klebsiella pneumoniae
and the emergence of carbapenem-resistant strains: A retrospective study from a university hospital in Morocco, North Africa. Afr J Urol 2015;21:36-40.
Manikandan C, Amsath A. Antibiotic susceptibility pattern of Klebsiella pneumoniae
isolated from urine samples. Int J Curr Microbiol Appl Sci 2013;2:330-7.
Biswas R, Rabbani R, Ahmed HS, Sarker MA, Zafrin N, Rahman MM. Antibiotic sensitivity pattern of urinary tract infection at a tertiary care hospital. Bangladesh Crit Care J 2014;2:21-4.
[Table 1], [Table 2], [Table 3], [Table 4]