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 Table of Contents  
ORIGINAL ARTICLE
Year : 2018  |  Volume : 5  |  Issue : 3  |  Page : 135-141

Catheterization-associated urinary tract infections: Epidemiology and incidence from tertiary care hospital in Haryana


1 Department of Microbiology, BPS GMC for Women, Khanpur Kalan, Sonepat, Haryana, India
2 MBBS Student, BPS GMC for Women, Khanpur Kalan, Sonepat, Haryana, India
3 Department of Forensic Medicine, BPS GMC for Women, Khanpur Kalan, Sonepat, Haryana, India

Date of Submission03-Apr-2018
Date of Acceptance01-Nov-2018
Date of Web Publication24-Dec-2018

Correspondence Address:
Dr. Raminder Sandhu
Department of Microbiology, BPS GMC for Women, Khanpur Kalan, Sonipat, Haryana
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jhrr.jhrr_19_18

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  Abstract 

Background: Urinary tract infections (UTIs) attributed to the use of an indwelling catheter is one of the most common infections acquired by patients in health-care facilities. This infection is associated with varied microbiological etiology. This along with existing underlying condition increases hospitalization, medication, morbidity, and also adds to the financial burden. Aims and Objectives: The aim of the study was to provide a baseline information in the context of incidence of catheter-associated UTI (CAUTI), to identify the associated microbial, and to determine their susceptibility pattern to commonly used antimicrobial agents for prophylactic and empiric therapy in this group of patients. Materials and Methods: This prospective study was done on nonrepetitive urine samples from catheterized patients. Semi-quantitative bacterial culture was performed, and isolates were identified by standard biochemical tests. Antimicrobial sensitivity tests were carried out by disc diffusion technique using Mueller-Hinton Agar as recommended by Clinical Laboratory Standard Institute. Results: Significant bacteriuria was observed among 17/161 (10.55%) urine samples. Among bacterial isolates, Gram-negative bacilli predominates. Escherichia coli 7/17 (41.17%) being the most common isolate. The incidence of UTI/1000 catheter days and urinary catheter utilization ratio observed in our study was 4.41 and 18.05, 0.673 and 0.066 for intensive care unit and wards, respectively. Conclusion: Burden of CAUTIs is vast with regards to incidence, patient outcomes, cost, reimbursement, and suffering. Our study underscores the pressing need for the development of antimicrobial urinary catheters and also we strove to minimize the effect of exogenous factors on the incidences of CAUTI and regarding the development of protocols and checklists on the insertion and management of indwelling urinary catheters based on the UTI prevention guideline.

Keywords: Escherichia coli, urinary catheters, urinary tract infections, uropathogens


How to cite this article:
Sandhu R, Sayal P, Jakkhar R, Sharma G. Catheterization-associated urinary tract infections: Epidemiology and incidence from tertiary care hospital in Haryana. J Health Res Rev 2018;5:135-41

How to cite this URL:
Sandhu R, Sayal P, Jakkhar R, Sharma G. Catheterization-associated urinary tract infections: Epidemiology and incidence from tertiary care hospital in Haryana. J Health Res Rev [serial online] 2018 [cited 2019 Aug 19];5:135-41. Available from: http://www.jhrr.org/text.asp?2018/5/3/135/248443


  Introduction Top


Urinary tract infection (UTI) is one of the most common infections in humans, accounting for more than 150 million cases worldwide. In addition to being the most common bacterial infection, UTIs also account for 36% of all healthcare-associated infections. Of these 36% infections, 80% of them are estimated to be catheter associated. Beyond the initial urinary infection, catheter-associated UTIs (CAUTIs) can lead to complications including bacteremia, endocarditis, osteomyelitis, septic arthritis, and meningitis. These pathologies collectively result in prolonged hospital stays and increased morbidity and mortality.[1] As per Center for disease prevention (CDC) and control, CAUTI is where an indwelling urinary catheter (IUC) was in place for >2 calendar days on the date of the event, with a day of device placement being Day 1 and an IUC was in place on the date of the event or the day before. If an IUC was in place for >2 calendar days and then removed, the date of event for UTI must be the day of discontinuation or the next day for the UTI to be catheter-associated.[2]

The susceptibility of an individual to CAUTI is mediated by several risk factors, including older age, female gender, diabetes, and impaired immunity. However, the most important risk factor is the use of an indwelling catheter and the duration of catheterization. The CDC estimates that approximately 12%–16% of adult hospital inpatients will have an indwelling catheter at some point during their hospitalization and that the risk for developing a CAUTI increases by 3%–7% with each additional day of catheterization. This increased susceptibility in catheterized patients is due to the ability of the catheter to bypass several host defenses and thereby enable bacterial entry into the urinary tract. In intubated patients, bacteria can ascend from the urethral meatus into the bladder by migrating between the mucosal and catheter surfaces. Further, contamination of the drainage bag or disruption in the tubing junction may also result in bacterial migration via the drainage system. In addition, the presence of an indwelling device favors the persistence of the etiological agent in the urinary tract, thereby increasing the risk for CAUTI. UTIs, including CAUTIs, can be caused by several bacterial species, including uropathogenic  Escherichia More Details coli (UPEC), Staphylococcus saprophyticus, Klebsiella pneumoniae, Enterococcus faecalis, Group B Streptococcus, Staphylococcus aureus, Proteus mirabilis, Pseudomonas aeruginosa, and Enterobacter spp. However, the most common causative agent for UTI and CAUTI is UPEC. It is estimated that UPEC is responsible for approximately 80% of all UTIs.[1]

Diagnosing CAUTI is often a diagnosis of exclusion. Fever without localizing findings is the usual presentation. Localizing signs or symptoms such as catheter obstruction, acute hematuria, recent trauma, suprapubic pain, or costovertebral angle pain or tenderness are helpful to identify a urinary source of fever but are present in only a minority of episodes of presumed symptomatic infection. If localizing genitourinary findings are not present, fever in bacteriuric patients should be attributed to urinary infection only when there are no other potential sources.[3]

Aims and objectives

  1. The aim of the study was to provide a baseline information in the context of incidence of CAUTI in tertiary care hospital wards and adult intensive care units (ICUs)
  2. To identify the microbial pathogens associated with UTI in catheterized patients and to determine their susceptibility pattern to commonly used antimicrobial agents for prophylactic and empiric therapy in this group of patients
  3. To know about the burden in terms of increase in the length of stay in the health-care settings and to develop a consistent methodology for incidence surveys which will represent a baseline to start from and shall aid in planning the measures needed to reduce the burden of CAUTI.



  Materials and Methods Top


The present study is a cross-sectional interviewer-administered questionnaire-based prospective study, carried out in the Department of Microbiology, BPS Govt. Medical College for Women, Khanpur Kalan, Sonepat, for 2 months' duration from August to September 2016. This teaching institute is a tertiary care center catering to a wide population of North West region of Haryana and neighboring states. Both adult males and females were included in the study group. Before starting the study, the purpose of the study was explained to the subjects, and informed consent was obtained. Approvals and formal authentications were acquired from the Ethical and Scientific Committee to whom proposal and detailed research methodology were presented and agreed on, according to the Declaration of Helsinki roles and policies. The Ethical clearance was granted wide letter no. BPSGMCW/RC158/IEC/16 on 14.5.2016. Patients admitted to Neonatal ICU, pediatrics, ophthalmology, and obstetrics/gynecology ward and those who remained unwilling for participation were excluded. A questionnaire was used to investigate about the demographic detail, provisional diagnosis; predisposing factors as well as risk factors, treatment details along with the date of catheter insertion and removal were as per CDC criteria. CAUTI was diagnosed as per CDC criteria with the presence of at least two of the following features with no other recognized cause: fever, urgency of micturition, dysuria or suprapubic tenderness, and pyuria or positive urine culture. To monitor the occurrence of CAUTIs, the following were calculated once a month: (1) Device Utilization Ratio (DUR): Determining the percentage of patients with urinary catheters urinary catheter utilization-R = number of indwelling catheter-days/total number of patient-days × 100 (2) Incidence rate = dividing the number of new CAUTI case(s) by the number of catheter days and multiplying the result by 1000.[4]

Inclusion criteria

Patients above 15 years of age who were catheterized and admitted to various wards and ICU s were included. UTI was diagnosed as per CDC definition. The presence of at least two of the following features with no other recognized cause: fever, urgency of micturition, dysuria or suprapubic tenderness, and pyuria or positive urine culture.[4] If urine culture is negative, then the patient should have two of the above-mentioned symptoms with one of the seven criteria defined by CDC.[5]

Exclusion criteria

Patients below 15 years of age and patients admitted to neonatal ICU, pediatrics, ophthalmology, obstetrics/gynecology wards as well as those who were unwilling to participate were excluded from the study.

Specimen collection and microbiological procedures

The samples were collected randomly from different clinical wards and ICUs after obtaining the informed consent of the patients. Blood and urine samples of these patients were collected and sent to the microbiology laboratory for culture and antibiotic sensitivity testing, to know the spectrum and resistance pattern of isolated organisms.

Urine sample collection and identification of organisms

Before catheter change or removal from each patient, urine samples were collected aseptically using a sterile needle and syringe from the distal edge of catheter tube into the sterile universal container and transported to the microbiology laboratory for analysis with minimum delay. The samples were processed by the routine standard laboratory procedure. This included microscopy, culture identification, and antibiotic susceptibility testing. Urine microscopy was performed on centrifuged catheter urine specimen. The culture was set up on Blood Agar and MacConkey Agar for isolating all kind of urinary pathogens. Semiquantitative method of urine culture was followed. A sterile calibrated wire loop was used to deliver a loopful (0.01 ml) of urine onto each culture media. All the culture plates were incubated at 37°C aerobically for 18–24 h and the culture-positive isolates were identified by their colony morphology, Gram-staining, and characterized biochemically for species identification.[6] Isolate suggestive of the yeast were subcultured on Sabouraud dextrose agar with further identification by the demonstration of germ tube; sporulation on cornmeal agar, sugar fermentation, and assimilation and CHROME agar.

Blood sample collection and identification of organisms

Blood samples from adults and geriatrics patients were collected by trained nursing staff at the request of clinician. Blood samples were collected after thorough cleaning of the venous site with 70% alcohol and subsequently followed by povidone iodine. Under the aseptic conditions, 5 ml of blood was drawn by venipuncture and transferred into two culture bottles each containing 50 ml of 0.5% bile broth and glucose broth. Both the bottles were incubated aerobically at 37°C for 10 days. Routine subculture was done on Blood agar and MacConkey agar after 24 h, 48 h, 7th day, and 15th day. The growth of microorganism was considered pathogenic if the same microorganism was isolated from both the broths and contaminated if either the growth was obtained in only one bottle or a mixed growth was obtained. In cases where the microorganisms obtained were coagulase-negative staphylococci, a repeat blood culture was performed. Organisms were identified by cultural characters, morphology, and standard biochemical tests.[6]

Antibiotic susceptibility testing

Antimicrobial susceptibility testing for aerobic bacterial isolates was done by Kirby-Bauer disk-diffusion method on Mueller-Hinton agar as per Clinical and Laboratory Standards Institute guidelines.[7] The antimicrobial drugs tested were as follows: cotrimoxazole (1.25/23.75 μg), amoxyclav (20:10 μg), cefuroxime (30 μg), cefoxitin (30 μg), cefazolin (30 μg), cefotaxime (30 μg), ceftazidime (30 μg), gentamicin (10 μg), amikacin (30 μg), ciprofloxacin (5 μg), nitrofurantoin (300 μg), azithromycin (15 μg), vancomycin (30 μg), and linezolid (30 μg).


  Results Top


The present study comprised 161 catheterized urine samples and blood samples collected with proper aseptic precautions. Demographic details of patients are discussed in [Table 1]. Maximum number of catheterized patients were males 97 (60.24%) and 64 (39.75%) were females. Maximum number of catheterized samples were from medicine department 88 (54.66%) followed by orthopedics department 36 (22.36%) and surgery 20 (12.42%). Significant bacteriuria was observed among 17/161 (10.55%) patients. [Table 2] and [Table 3] depict the distribution of blood samples and culture results. Several risk factors also have been cited to be associated with UTI. Predisposing factors observed [Table 4]. The incidence rate of CAUTI and catheter utilization ratio observed in our study was 4.41 and 18.05/1000 catheter days and 0.673 and 0.066 in ICU and ward, respectively. The data regarding CAUTI incidence, DUR, and number of catheter days over the study period are shown in [Table 5]. The observations based on bacteriological profile and antimicrobial sensitivity testing of isolated organisms is shown in [Figure 1] and [Table 6].
Table 1: Age and gender distribution of patients

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Table 2: Distribution of urinary samples according to location

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Table 3: Distribution of blood samples according to location

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Table 4: Predisposing factors for catheter-associated urinary tract infections

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Table 5: Analysis of incidence of aerobic bacterial urinary tract infection, catheter utilization, and catheter days

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Figure 1: Uropathogenic profile among catheter-associated urinary tract infection patients

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Table 6: Antimicrobial susceptibility profile of bacterial uropathogens

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Statistical analysis

Descriptive statistics expressed as percentages were used to evaluate the incidence of CAUTI in tertiary care hospital wards and adult ICUs and to define the resistance pattern of isolated organisms.


  Discussion Top


The presence of indwelling catheter predisposes to a symptomatic infection because it provides a surface for the attachment of microbial adhesion. Symptomatic infection can lead to ascending infection of bladder, ureters, and kidney, with subsequent need for antimicrobial agents. CAUTIs is a huge reservoir of resistant pathogens with the risk of cross-infection of other patients.[8]

Thus, our study was undertaken in the Department of Microbiology, BPS, GMC for Women Khanpur Kalan to determine the incidence of CAUTI in a tertiary care hospital, antibiotic susceptibility pattern of isolates in a trail to help the clinicians make a precise decision regarding treatment of such infections and to determine its burden on health-care facilities. Demographic characteristics of the study showed that among 161 patients, 97 (60.24%) were male and 64 (39.75%) female. These results were in concordance with Verma et al., where the majority of catheterized patients were male (62.58%) and (37.42%) were female.[8] However, this is contradictory to Kakaria et al., who observed a higher incidence of CAUTI in females (56.46%) as compared to males (43.54%). This increased risk in women is likely to be due to easier access of the perineal flora to the bladder along the outside of the catheter as it traverses the shorter female urethra. In addition, a woman's urethra is closer to anus. This makes it easier for bacteria to spread into her urethra and cause an infection.[9]

Many other authors have also failed to find female gender a risk factor for CAUTI. Moreover, less number of female patients in our study group could be a possible reason for this result.

UTIs are most often caused by ascending colonization, hematogenous dissemination secondary to organisms in the bloodstream is another possible route to the development of UTI. In the present study, blood samples were collected with proper aseptic precautions to understand the role of undetected hematogenous seeding of the urinary tract. Maximum samples of 88 (54.65% urine + blood samples) were from the medicine department, followed by orthopedics department had 36 (22.36%) and surgery had 20 (12.42%). As most of the patients admitted to these wards had serious underlying disease or other invasive procedures done, and in most of them, IUCs were present. Apisarnthanarak et al. suggested catheter utilization ratio in medicine 0.52, in surgery 0.24, and the ICUs 0.32. Our study emphasizes the need for careful evaluation of the initial reason for urinary catheterization and the continual reassessment of the need for continued catheter use. Educating physicians on the risk of unnecessary urinary catheterization to their patients is critical. Careful attention to this aspect of medical care may reduce IUC use and CAUTIs by at least one in six of these patients.[10] In our set up also, the higher number of catheterized patients were from medicine ward which could also be the outcome of inappropriate urinary catheters usage in our tertiary care center.

Several risk factors have been cited to be associated with UTI. We included the previous history of catheterization/UTI, associated comorbid condition as diabetes and obstructive uropathy as potential risk factors in our study. These findings were similar to Kakaria et al., who identified three risk factors associated with CAUTI: female gender, diabetes mellitus, and duration of catheterization.[9] A nested case–control study in a multicenter cohort conducted by Clec'h et al., also found that diabetes is a risk factor for CAUTI.[11] The low infection rate among predisposed patients in our study can be explained by a limited number of the sample due to the short duration of the study. Among 716 patients treated in the ICU during 6698 person-days of hospitalization, UTIs were diagnosed in 17 patients. The incidence rate of CAUTI and catheter utilization ratio was 4.41 and 18.05/1000 catheter days and 0.673 and 0.066 in ICU and ward, respectively. The incidence of CAUTIs as observed in other studies, 1.9 − 2.4/1000 catheter-days in Polish ICUs;[12],[13] 6.4 − 12/1000 catheter-days according to the SPIN-UTI Project of the Italian Nosocomial Infections Surveillance in ICUs[14] and 1.46 − 0.57/1000 catheter-days reported by the Krankenhaus Infections Surveillance System.[15]

Uropathogens isolated in the present study include Candida spp. 7 (41.18%), E. coli 7 (41.18%), K. pneumoniae 1 (5.88%), Citrobacter freundii 1 (5.88%), and S. aureus 1 (5.88%). Thus, Gram-negative bacteria (GNB) were most among bacterial isolates 09/10 (90.00%). Our findings were in accordance with Deorukhkar et al., who reported E. coli (33.8%) followed by K. pneumoniae (22.1%) among bacterial isolates and predominance of NAC (77.42%) over Candida albicans (22.58%).[16] In our study, E. coli was most commonly isolated among catheterized patients 9/10 (90.00%), followed by K. pneumoniae 1/10 (5.88%) and C. freundii 1/10 (5.88%). This is in accordance with Santhose et al., who reported E. coli (39.00%) as the predominant organism followed by Klebsiella spp. (28.00%).[17] E. coli is responsible for more than 80% of the UTIs, and it causes both symptomatic UTIs and Asymptomatic bacteriuria. Similarly to the bacterial spectrum of uncomplicated UTIs, E. coli is the most common pathogen in the presence of a catheter as well. The persistence of E. coli strains is related to the presence of Type 1 pili, an adhesin for uroepithelium as well as the Tamm–Horsfall protein. Colonising E. coli strains lack P fimbriae in most cases of catheter-associated infections.[18]

In the present study, bacterial isolates were tested against 10 antimicrobial agents, and their susceptibility pattern was observed. Most of the GNB isolates were sensitive to amikacin (77.78%) followed by cefazolin and ceftazidime (66.67%) but decreased sensitivity was observed to nitrofurantoin, cefuroxime, and cefotaxime (55.56%). These findings are similar to Jafari et al., who also observed amikacin (91%) as the most effective drug against uropathogens.[19] In the present study, the prevalence of resistance was high to cotrimoxazole (88.89%) and ciprofloxacin (88.89%). This is in accordance with Bhani et al., where CAUTIs due to GNB were significantly resistant to norfloxacin (81.25%) and levofloxacin (73.44%) but susceptible to nitrofurantoin (73.4%).[20] Teshager et al. observed the intermediate level of resistance (48%–68%) to amoxicillin-clavulanic acid, gentamicin, cotrimoxazole, and low level of resistance (16%–24%) was observed to amikacin, ciprofloxacin, and nitrofurantoin.[21] In the present study, Gram-positive bacteria were sensitive to vancomycin (100.00%), followed by linezolid (100.00%) and Amikacin (100.00%). A similar pattern of susceptibility was observed in a study by Bhani et al., where all the Gram-positive isolates were susceptible to vancomycin and linezolid (100%).[20] Gram-positive isolates were resistant to cotrimoxazole (100.00%), gentamicin (100.00%), ciprofloxacin (100.00%), and nitrofurantoin (100.00%).

Progress in the area of prevention of urinary catheter-associated infections is very limited, and the preventive procedures used nowadays rather only prolong the “abacterial window” than really prevent the infection. There are only few effective preventive strategies available for prevention of CAUTIs. These include avoiding unnecessary catheterization, selecting alternative catheterization procedures, maintaining the closed drainage system, and eliminating bacterial colonization of the patient. The prolongation of the catheterization or even unnecessary catheterization is the first steps which can be changed in the course of prevention of the CAUTIs. More attention to the selective and limited catheter use can lead to a reduction of the number of CAUTIs.[3] Known measures to prevent CAUTI are catheter insertion in the operating room or another clean environment, training for catheter insertion and early catheter removal. Antimicrobial indwelling urethral catheters mixed or coated with antibacterial agents, including silver hydrogel and nitrofural, are considered effective in preventing CAUTI because of suppression of bacterial growth on the catheter surface.[22]

[TAG:2]Conclusion [/TAG:2]

Catheterized urinary tract provides ideal conditions for bacterial adherence inducing complications in patients' care. Second, treating physicians should carefully evaluate the indications for usage of urinary catheter and avoid unnecessary catheterization to their patients. The present study helped us to generate institutional data regarding CAUTI. The development of universal resistance among uropathogens to antibacterial agents is clinically important and has to be considered when instigating antibiotic therapy for symptomatic infections. Replacing the old catheters before antibiotic treatment is a sensible option. The treatment should be based on the susceptibility of organisms that are isolated from urine aspirated from the new catheter, as samples collected from the old catheter can contain different species and greater numbers of organisms. Thus, the study underscores the pressing need for the development of antimicrobial urinary catheters and their deployment when longer durations of catheter access are required. We strove to minimize the effect of the exogenous factors on the incidences of CAUTI and regarding the development of protocols and checklists on the insertion and management of IUCs based on the UTI prevention guideline.

Acknowledgment

This study was part of Short-Term Student 2016 Programme of ICMR.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Narayanan A, Nair MS, Muyyarikkandy MS, Amalaradjou MA. Inhibition and inactivation of uropathogenic Escherichia coli biofilms on urinary catheters by sodium selenite. Int J Mol Sci 2018;19. pii: E1703.  Back to cited text no. 1
    
2.
Device Associated Module-UTI, NHSN Patient Safety Component Manual, Center for Disease Prevention & Control; January, 2016. Available from: http://www.cdc.gov/nhsn/PS-Analysis-resources/reference-guides.html. [Last accessed on 2017 May 04].  Back to cited text no. 2
    
3.
Nicolle LE. Catheter associated urinary tract infections. Antimicrob Resist Infect Control 2014;3:23.  Back to cited text no. 3
    
4.
Centre for Disease Control and Prevention. Protocol for Reporting Catheter-Associated Urinary Tract Infections to the National Healthcare Safety Network. Centre for Disease Control and Prevention; January, 2016. Available from: http://www.cdc.gov/hai/pdfs/NHSN/7pscCAUTISAMPLE.pdf. [Last accessed on 2017 May 04].  Back to cited text no. 4
    
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Garner JS, Jarvis WR, Emori TG, Horan TC, Hughes JM. CDC definitions for nosocomial infections, 1988. Am J Infect Control 1988;16:128-40.  Back to cited text no. 5
    
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Collee JG, Miles RS, Watt B. Test for identification of bacteria. In: Collee JG, Fraser AG, Marmion BP, Simmons A, editors. Mackie and McCartney Practical Medical Microbiology. 14th ed. New York: Churchill Livingstone; 1996. p. 131-49.  Back to cited text no. 6
    
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Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Second Informational Supplement. CLSI document M100-S21. Wayne, PA: Clinical and Laboratory Standards Institute; 2012.  Back to cited text no. 7
    
8.
Verma S, Naik SA, Deepak TS. Etiology and risk factors of catheter associated urinary tract infections in ICU patients. Int J Med Microbiol Trop Dis 2017;3:65-70.  Back to cited text no. 8
    
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Kakaria BA, Ashish K, Raghuwanshi T. Study of incidence and risk factors of urinary tract infection in catheterized patients admitted at tertiary care. Int J Res Med Sci 2018;6:1730-33.  Back to cited text no. 9
    
10.
Apisarnthanarak A, Rutjanawech S, Wichansawakun S, Ratanabunjerdkul H, Patthranitima P, Thongphubeth K, et al. Initial inappropriate urinary catheters use in a tertiary-care center: Incidence, risk factors, and outcomes. Am J Infect Control 2007;35:594-9.  Back to cited text no. 10
    
11.
Clec'h C, Schwebel C, Français A, Toledano D, Fosse JP, Garrouste-Orgeas M, et al. Does catheter-associated urinary tract infection increase mortality in critically ill patients? Infect Control Hosp Epidemiol 2007;28:1367-73.  Back to cited text no. 11
    
12.
Rutkowska K, Przybyła M, Misiołek H. Health-care associated infection in the newly-opened Intensive Care Unit. Anaesthesiol Intensive Ther 2013;45:62-6.  Back to cited text no. 12
    
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Wałaszek M, Wolak Z, Dobroś W. Nosocomial infection in patients hospitalized in 2005-2011. The St. Lukas district hospital in tarnów. Przegl Epidemiol 2012;66:617-21.  Back to cited text no. 13
    
14.
Agodi A, Barchitta M. Epidemiology and control of urinary tract infections in intensive care patients. In: Nikibakhsh A, editor. Clinical Management of Complicated Urinary Tract Infection. InTech; 2011. p. 1-18.  Back to cited text no. 14
    
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Gastmeier P, Behnke M, Schwab F, Geffers C. Benchmarking of urinary tract infection rates: Experiences from the Intensive Care Unit component of the German national nosocomial infections surveillance system. J Hosp Infect 2011;78:41-4.  Back to cited text no. 15
    
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Deorukhkar SC, Saini S, Raytekar NA, Sebastian MD. Catheter associated urinary tract candida infections in Intensive Care Unit patients. J Clin Microbiol Biochem Technol 2016;2:15-7.  Back to cited text no. 16
    
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Bharathi Santhose N, Mythily N, Ashok Kumar C. Study on biofilm producing bacterial isolates in catheter associated urinary tract infection. IOSR J Dent Med Sci 2018;17:50-3.  Back to cited text no. 17
    
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Köves B, Magyar A, Tenke P. Spectrum and antibiotic resistance of catheter-associated urinary tract infections. GMS Infect Dis 2017;5:Doc06.  Back to cited text no. 18
    
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Jafari HM, Saffar MJ, Nemate I, Saffar H, Khalilian AR. Increasing antibiotic resistance among uropathogens isolated during years 2006-2009: Impact on the empirical management. Int Braz J Urol 2012;38:25-32.  Back to cited text no. 19
    
20.
Bhani D, Bachhiwal R, Sharma R, Maheshwari RK. Microbial profile and antimicrobial susceptibility pattern of uropathogens isolated from catheter associated urinary tract infection (CAUTI). Int J Curr Microbiol Appl Sci 2017;6:2446-53.  Back to cited text no. 20
    
21.
Teshager L, Asrat D, Gebre-Selassie S, Tamiru S. Catheterized and non-catheterized urinary tract infections among patients attended at Jimma University teaching hospital, Southwest, Ethiopia. Ethiop Med J 2008;46:55-62.  Back to cited text no. 21
    
22.
Muramatsu K, Fujino Y, Kubo T, Otani M, Fushimi K, Matsuda S, et al. Efficacy of antimicrobial catheters for prevention of catheter-associated urinary tract infection in acute cerebral infarction. J Epidemiol 2018;28:54-8.  Back to cited text no. 22
    


    Figures

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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]



 

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