|Year : 2016 | Volume
| Issue : 2 | Page : 52-58
Bacterial catheter-associated urinary tract infection in the Intensive Care Unit of Assiut University Hospital
Sherine A Aly, Rania A Tawfeek, Ismail S Mohamed
Department of Medical Microbiology and Immunology, Faculty of Medicine, Assiut University, Assiut, Egypt
|Date of Submission||16-Feb-2016|
|Date of Acceptance||04-Jul-2016|
|Date of Web Publication||21-Oct-2016|
Sherine A Aly
Department of Medical Microbiology and Immunology, Faculty of Medicine, Assiut University, Assiut 71516
Source of Support: None, Conflict of Interest: None
The aim of this study was to identify the risk factors and common pathogens associated with catheter-associated urinary tract infection (CAUTI) in the ICUs of Assiut University Hospital, Egypt.
Urine samples were collected from patients suffering from CAUTI according to the case definition of Centers for Disease Control and Prevention. The samples were subjected to culture on different culture media, and all positive colonies were identified according to their biochemical profile and antibiograms. Klebsiella isolates were further tested for extended-spectrum β-lactamase production.
The overall bacterial CAUTI incidence rate was 11% (15/136 patients). Female sex, old age (>60 years old), diabetes mellitus, and prolonged duration of catheterization (>6 days) were found to be risk factors for the development of bacterial CAUTI. Klebsiella was the commonly isolated microorganism (8/16, 50%). All Klebsiella isolates were found to be phenotypically Extended-spectrum β lactamase producers, and five of these isolates contained either blaTEM or blaSHV genes.
This study revealed the high incidence of bacterial CAUTI (11%) in ICUs of Assiut University Hospital. ESBL-producing Klebsiella spp. is responsible for about 50% of bacterial CAUTI cases. All isolated microorganisms were found to be multidrug resistant. Strict implementation of infection control procedures appears to be necessary to control the spread of multidrug resistant organisms.
Keywords: catheter-associated urinary tract infections, ESBL, Klebsiella pneumoniae, risk factors
|How to cite this article:|
Aly SA, Tawfeek RA, Mohamed IS. Bacterial catheter-associated urinary tract infection in the Intensive Care Unit of Assiut University Hospital. Al-Azhar Assiut Med J 2016;14:52-8
|How to cite this URL:|
Aly SA, Tawfeek RA, Mohamed IS. Bacterial catheter-associated urinary tract infection in the Intensive Care Unit of Assiut University Hospital. Al-Azhar Assiut Med J [serial online] 2016 [cited 2017 Oct 17];14:52-8. Available from: http://www.azmj.eg.net/text.asp?2016/14/2/52/192652
| Introduction|| |
Catheter-associated urinary tract infection (CAUTI) is characterized by one of the highest rates of occurrence among hospitalized patients, comprising about 36% of all healthcare-associated infections (HAIs) . CAUTIs are of special concern in ICUs because patients in ICUs often have an indwelling catheter to monitor urine . Identifying risks associated with acquisition of urinary tract infection (UTI) is vital to recommend means to avoid these infections. Large prospective studies have recognized a number of risk factors linked to CAUTIs, such as female sex, duration of catheterization, and microbial colonization of the drainage. However, the most important, potentially modifiable, risk factor recognized in every study is prolonged catheterization . Bacteriuria or funguria are acquired by up to 25% of patients when indwelling urinary catheters are left in place for more than 7 days . Although CAUTI carries a low risk for mortality compared with other HAIs, its overall incidence, patient discomfort, and related costs are high given the high-frequency use of urinary catheter in intensive care settings . CAUTI is the most frequent cause of secondary bloodstream HAI, carrying an ∼10% mortality rate, suggesting that nosocomial CAUTIs are associated with substantially increased institutional death rates, unrelated to the occurrence of urosepsis .
In addition, CAUTIs comprise perhaps the largest institutional reservoir of nosocomial antibiotic-resistant pathogens, the most important of which are multidrug resistant (MDR) Klebsiella, Enterobacter, Proteus, Pseudomonas aeruginosa, Enterococci, Staphylococci, and Candida spp. . Organisms gain access through extraluminal contamination that may occur either by direct inoculation during catheter insertion, or later, by organisms ascending from the perineum. Intraluminal contamination occurs by reflux of microorganisms gaining access to the catheter lumen from failure of closed drainage or contamination of urine in the collection bag .
Most published studies of CAUTI have originated from studies conducted in the developed world, with relatively few data available from the eastern Mediterranean region identifying CAUTI and its underlying risk factors . We carried out a 1-year study of CAUTIs in ICUs in Assiut University Hospital. The study aimed to describe rates of infection, explore important risk factors related to infections, and identify the microorganisms responsible for CAUTIs and their antimicrobial resistance patterns with special reference to extended-spectrum β-lactamase production.
| Methods|| |
Patients and setting
This study was performed in Assiut University Hospital, which is a 2000-bed governmental teaching hospital serving the population living in South Egypt. The study was conducted over a period of 1 year from November 2011 through October 2012 and included patients admitted to adult ICUs. Six ICUs participated in the study: the Coronary ICU, the Chest ICU, the Neurology ICU, the General ICU, the Neurosurgical ICU, and the Trauma ICU. All patients admitted in the selected ICUs had indwelling urinary catheters inserted after ICU admission for 3 or more days. The following patients were excluded: (i) those who had a CAUTI at the start of the study and (ii) those with a urethral catheter in place at admission.
Patients were monitored daily and urine culture was performed whenever the patient developed systemic or local signs of CAUTI according to the Centers for Disease Control and Prevention standard case definition of CAUTI after 48 h of admission to the ICU . These signs included fever (temperature>38°C), dysuria, and suprapubic tenderness. Demographic and clinical data were collected, such as age, sex, date of admission, underlying disease, length of ICU stay, duration of catheterization, and previous antibiotic therapy.
All ethical considerations that protect human rights with regard to consent, keeping secrecy, causing no harm, and all other ethical aspects were carefully adapted. The study was revised and approved by the Institutional Ethics Committee of the Faculty of Medicine of Assiut University.
Urine samples were collected from patients who developed clinical signs and symptoms of UTI (n=65). The urine was aseptically aspirated from the urinary catheter and transferred immediately to the hospital microbiology laboratory.
Culture and identification of pathogens
The urine samples were inspected microscopically and processed using standard microbiologic procedures. Viable bacterial count was performed to calculate the number of viable bacteria/1 ml of urine. Significant bacteriuria was defined as more than or equal to 105 microorganisms/ml of urine with no more than two species of microorganisms .
All urine samples were inoculated on blood, MacConkey’s, eosin methylene blue, mannitol salt, Mueller–Hinton, bile esculin azide, and hicrome UTI agar plates and incubated at 37°C for 24 h. Hicrome UTI agar medium is recommended for the detection of urinary tract pathogens based on the production of specific colors by different microorganisms . All positive colonies were further identified on the basis of their morphology, Gram stain, and the pattern of biochemical reaction using standard procedures .
Enterococci spp. were further identified into vancomycin-resistant Enterococci and non-vancomycin-resistant Enterococci depending on the minimal inhibitory concentration for vancomycin using the standard agar dilution method. The breakpoints of the Clinical Laboratory Standard Institute (CLSI) for vancomycin are less than or equal to 4 μg/ml for susceptible, 8–16 μg/ml for intermediate-level vancomycin resistance, and more than or equal to 32 μg/ml for high-level vancomycin resistance .
Staphylococci spp. were further inoculated on oxacillin-resistant screening agar base media, which are commonly used to identify methicillin-resistant Staphylococcus aureus (MRSA).
Antimicrobial susceptibility test
Antibiotic susceptibility testing was performed using the Kirby–Bauer technique according to the CLSI guidelines . Antibiotics used are listed in [Table 1]. Plates were incubated at 37°C for 24 h and tested afterward. Escherichia coli ATCC 25922 was used as standard strain to check the standardization of the disks.
|Table 1: Antibiotics used in antimicrobial susceptibility tests for isolates|
Click here to view
Detection of extended-spectrum β-lactamases
Selective testing for ESBL production was considered for all Klebsiella isolates.
Screening for ESBL production
Isolates that exhibited reduced susceptibility to one or more of oxyiminocephalosporins [cefpodoxime (30 µg)≤25 mm, ceftazidime (30 µg)≤22 mm, aztreonam (30 µg)≤27 mm, cefotaxime (30 µg)≤22 mm, or ceftriaxone (30 µg)≤25 mm (Oxoid, UK)], were considered as potential producers of ESBL according to the CLSI guidelines .
The combined disk method or the inhibitor-potentiated disc diffusion test: Ceftazidime (30 μg) versus ceftazidime/clavulanic acid (30 μg/10 μg) (Oxoid, UK) were used to perform the ESBL phenotypic confirmatory test . An increase of more than or equal to 5 mm in the zone diameter for ceftazidime tested in combination with β-lactamase inhibitor compared with its zone when tested alone indicates ESBL production.
Double-disk synergy test: Mueller–Hinton agar plate was inoculated with a suspension made from an overnight blood agar culture of the test strain as recommended for a standard disk diffusion susceptibility test. Disks containing the standard 30 μg of ceftazidime, or ceftriaxone, or cefotaxime, or aztreonam were placed 15 mm apart (edge to edge) from amoxicillin–clavulanic acid disk (amoxicillin 20 µg+10 μg of clavulanic acid). Following incubation for 24 h at 37°C, any enhancement of the zone of inhibition between a β-lactamase disk and that containing the β-lactamase inhibitor was indicative of ESBL production .
Determination of the type of β-lactamase using PCR: Klebsiella strains (n=8) were investigated to determine the probable type of β-lactamase enzyme that was responsible for resistance. The isolates were tested for blaTEM and blaSHV genes by means of PCR. Primers used for PCR were as follows: TEM forward: 5′-AAGCCATACCAAACGACGAG-3′, TEM reverse: 5′-ATTGTTGCCGGGAAGCTAGA-3′, and SHV forward: 5′-TCTCCCTGTTAGCCACCCTG-3′, SHV reverse: 5′-CCACTGCAGCAGCTGCCGTT-3′. Multiplex PCR was performed using the following parameters: 95°C for 5 min and 30 cycles at 95°C for 30 s, 60°C for 30 s, and 72°C for 1 min, followed by a final extension step at 72°C for 5 min. The mixture was electrophoretically separated on a 2% agarose gel.
Data on infection rates and risk factors were handled and evaluated using the Microsoft Excel 2007 (Microsoft, Chicago, IL, USA). The relative risk (RR) for acquiring a bacterial CAUTI in catheterized patients with the presence of a possible risk factor as compared with no possible risk factor was calculated by dividing the cumulative incidence of bacterial CAUTIs among those with a possible risk factor by the cumulative incidence among those without the factor. The RR was calculated with 95% confidence intervals (CIs). The Fisher exact test was used to calculate the P value. A P value of less than 0.05 was considered significant.
| Results|| |
During the 1-year surveillance study period, 1702 patients were admitted to six different ICUs at Assiut University Hospitals, and among them 136 patients were catheterized. Of them, 15 (11%) patients developed bacterial CAUTI, 4 male and 11 female. The rate of bacterial CAUTI among catheterized patients at different ICUs is demonstrated and the distribution of bacterial CAUTI at different ICUs per 100 admissions is illustrated in [Table 2].
|Table 2: Rate of bacterial catheter-associated urinary tract infection among different intensive care units patients|
Click here to view
A cohort of 136 patients was used to describe risk factors associated with acquiring bacterial CAUTIs. Of the 136 patients, 32.8% were female, with a mean age of 45.43±20.47 years. Risk factors associated with acquiring bacterial CAUTI are listed in [Table 3]. Female patients were at a significantly higher risk of developing nosocomial bacterial CAUTI (RR: 6.1; 95% CI: 3.9–9.4; P<0.001). Patients older than 60 years were 2.2 times more likely to develop bacterial CAUTI compared with patients younger than 20 years (RR: 2.2; 95% CI: 1.5–3.3; P<0.001). Patients with a history of longer duration of catheterization (>6 vs. <6 days) were at a significantly higher risk of developing bacterial CAUTI (RR: 5.2; 95% CI: 3.4–8.0; P<0.001). Diabetic patients were at a significantly higher risk compared with the nondiabetic patients (RR: 7.3; 95% CI: 4.8–11.3; P<0.001).
|Table 3: Univariate analysis for the risk factors associated with bacterial catheter-associated urinary tract infection|
Click here to view
Microorganisms and antimicrobial susceptibility
The study included 136 patients who were admitted to different ICUs in Assiut University Hospital and had indwelling urinary catheters inserted after ICU admission for three or more days. Sixty-five patients developed nosocomial CAUTI during the period of hospitalization, with an incidence rate of 47%. Of the 65 patients, 16 pathogens were isolated from 15 patients. Most of the infections were monomicrobial; 14 of 15 (93.3%) patients had a single pathogen in comparison with a single (6.7%) patient with two pathogens isolated.
Klebsiella spp. were the most commonly isolated microorganism (8/16, 50%), followed by Enterococci spp. (7/16, 44%) and a single S. aureus isolate. All Klebsiella isolates were found to be phenotypically ESBL (ESBL-KP) producers using the combined disk method and the double-disk synergy test according to the criteria set by CLSI . Of the seven enterococcal isolates, six isolates exhibited vancomycin resistance. The single S. aureus isolate was found to be MRSA.
Antibiotic susceptibility patterns of isolates
Klebsiella isolates showed high resistance levels to ampicillin (100%), ceftazidime (100%), cefpodoxime (100%), ceftriaxone (100%), cefotaxime (100%), nitrofurantoin (100%), and tetracycline (75%) and low resistance to amikacin (37.5%) and norfloxacin (25%). Surprisingly, one isolate was found to be resistant to imipenem (12.5%).
Enterococcal isolates showed high resistance to most of the antibiotics: vancomycin (85.7%), ampicillin (85.7%), ceftazidime (85.7%), cefpodoxime (85.7%), ceftriaxone (85.7%), cefotaxime (85.7%), nitrofurantoin (100%), tetracycline (100%), norfloxacin (57%), and amikacin (57%). Moreover, one isolate was found to be resistant to imipenem (14.3%). The single MRSA isolate was resistant to all tested antimicrobials except for imipenem.
Multiplex PCR for the detection of blaTEM and blaSHV
The multiplex PCR method was used to demonstrate the presence of blaTEM or blaSHV genes in the eight Klebsiella pneumoniae strains that were identified as ESBL producers using phenotypic methods. Genotyping of ESBL-KP isolates demonstrated the presence of blaTEM and blaSHV in five of eight ESBL-KP isolates (four blaSHV and one blaTEM) ([Figure 1]).
|Figure 1: Multiplex PCR of blaTEM and blaSHV. L, ladder; samples 1, 3, 5, and 6, blaSHV (593bp); sample 2, blaTEM (108bp); sample 7, negative sample; sample 8, negative control.|
Click here to view
| Discussion|| |
CAUTI is the most common nosocomial infection representing about 30–40% of all hospital-acquired infection and constitutes a major source of nosocomial septicemia and related mortality in acute care hospitals . Our study examined the rate of bacterial CAUTI in Assiut University Hospital together with testing for the common risk factors and the common pathogens associated with bacterial CAUTI.
In the current study, the rate of CAUTI was found to be 47.8% (65/136), whereas only 11% (15/136) of catheterized patients developed bacterial CAUTI. Other cases of CAUTI are probably due to other infectious agents such as fungi, mycoplasma, and chlamydia ,.
Previous studies demonstrated that ∼26% of patients who have an indwelling urinary catheter in place for 2–10 days will develop bacteriuria, and 25% of those patients will develop a bacterial CAUTI. Our results are somewhat higher than the published rates probably because all patients enrolled in this study were admitted to the ICUs and were suffering from a number of a risk factors that increase the possibility of development of bacterial CAUTI ,.
In the present study, a number of probable risk factors for the development of bacterial CAUTI have been evaluated. Our results revealed that 73% of patients suffering from bacterial CAUTI were female; this is in agreement with that published in other studies ,. The mean age of bacterial CAUTI patients in this study was 45±20 years and it was noticeable that 46% of those patients were above 60 years of age (P<0.001). In parallel to this observation, several studies reported that CAUTI is mostly common in patients 60 years or older . In the current study, diabetes mellitus was found to be a risk factor for the occurrence of bacterial CAUTI. The association between diabetes mellitus and the occurrence of bacterial CAUTI has also been documented in a number of studies .
The most important risk factor for the development of bacterial CAUTI is the duration of catheterization as has been verified in several studies . Increased duration presumably increases the likelihood of microbes ascending to the bladder either around the catheter or through its lumen. Increased duration of catheterization has been a significant factor associated with acquiring CAUTI in this study (>6 days) as has been shown in many other studies ,.
In the current study, about 93.3% of bacterial CAUTI were monomicrobial, which is comparable to that reported in several studies. Recently published nosocomial surveillance studies conducted in ICUs in North America and Europe consistently support E. coli, Klebsiella spp., and Enterococci spp. as the predominant bacterial pathogens causing CAUTI ,. These findings are in agreement with our study in which Klebsiella spp. were the most commonly identified bacteria (8/16, 50%), followed by Enterococci (7/16, 44%). Although E. coli is known to be the most predominant etiology for UTI ,, it was not isolated from any of the patients enrolled in this study. This finding might reflect dissimilarity in bacterial population according to different locality and suggests a role of the environment in shaping the bacterial population in each hospital .
All bacterial pathogens recovered from urine of CAUTI cases were found to be resistant to most of the tested antimicrobials. These results are consistent with previous studies that demonstrated that organisms recovered from ICU patients are often resistant to multiple antibiotics ,. The high rate of MDR among nosocomial pathogens reflects the extensive use of antimicrobials in the hospital in addition to the huge ability of the organism to acquire resistance genes ,. Imipenem was the most active drug against Klebsiella and Enterococci isolated in this study (87.5% sensitivity). However, the sensitivity of Klebsiella spp. isolated from Assiut University Hospitals decreased from 100% in 2008 to 94.4% in 2010 and finally to 87.5% in 2013 ,. This steady increase in carbapenem resistance over time is frightening and creates a hazard to infected patients being the only antimicrobial choice for these MDR isolates.
All Klebsiella pathogens isolated in this study were proved to be phenotypically ESBL producers. In this study, PCR could identify ESBL-production genes in five of eight (blaTEM and blaSHV) of the phenotypically ESBL Klebsiella spp. The absence of blaTEM and blaSHV in three of the phenotypically ESBL Klebsiella isolates suggest other mechanisms of ESBL production such as CTX-M or OXA genes .
| Conclusion|| |
CAUTI remains an important problem in Assiut University Hospital and what complicates the situation is that all causative microorganisms are MDR with few options for therapy. According to our results, third and fourth generation cephalosporins should not be used for empirical treatment due to the high prevalence of extended-spectrum β-lactamase production among Klebsiella isolates.
| Acknowledgements|| |
The authors thank Professor Enas Abdel Maguid Deaf for her material support in this study.
Sherine A. Aly contributed to the concept and design of study, analyzing the data, revising the article, and final approval of the version to be published. Rania A. Tawfeek contributed in the acquisition of data, writing the article, and final approval of the version to be published. Ismail S. Mohamed contributed to the design of study, revising the article, and final approval of the version to be published.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Burton A, Fridkin SK, Gould CV. Trends in catheter-associated urinary tract infections in adult intensive care units − United States, 1990–2007. Infect Control Hosp Epidemiol 2011; 32:748–756.
Tissot E, Limat S, Cornette C, Capellier G. Risk factors for catheter associated bacteriuria in a medical intensive care unit. Eur J Clin Microbiol Infect Dis 2001; 20:260–262.
Wald HL, Kramer AM. Nonpayment for harms resulting from medical care: catheter-associated urinary tract infections. JAMA 2007; 298:2782–2784.
Taiwo SS, Aderounmu AOA. Catheter-associated urinary tract infection: etiologic agents and antimicrobial susceptibility pattern in Ladoke Akintola University Teaching Hospital, Osogbo, Nigeria. Afr J Biomed Res 2006; 9:141–148.
Rebmann T, Greene LR. Preventing catheter-associated urinary tract infections: an executive summary of the Association for Professionals in Infection Control and Epidemiology, Inc, Elimination Guide. Am J Infect Control 2010; 38:644–646.
Maki DG, Tambyah PA. Engineering out the risk for infection with urinary catheters. Emerg Infect Dis 2001; 2:342–347.
Saint S, Chenoweth CE. Biofilms and catheter-associated urinary tract infections Infect Dis Clin North Am 2003; 17:2411–2432.
Talaat M, Hafez S, Saied T, Elfeky R, El-Shoubary W, Pimentel G. Surveillance of catheter-associated urinary tract infection in 4 intensive care units at Alexandria University Hospitals in Egypt. Am J Infect Control 2010; 38:222–228.
Emori TG, Culver DH, Horan TC, Jarvis WR, White JW, Olson DR. National Nosocomial Infections Surveillance System (NNIS): description of surveillance methods. Am J Infect Control 1991; 19:19–35.
McGeachie J, Kennedy AC. Simplified quantitative methods for bacteriuria and pyuria. J Clin Pathol 1963; 16:32–38.
Friedman MP. Detection of urinary tract pathogen by chromogenic differential media. J Clin Microbiol 1991; 29:2385–2389.
Collee JG, Fraser AG, Marmion BP, Simmons A. Tests for identification of bacteria. In: Collee JG, Marmion BP, Fraser AG, Simmons A, editors. Mackie and McCartney practical medical microbiology
. 14th ed. New York, USA: Churchill Livingstone; 1996: 131–149.
Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing; sixteenth informational supplement. CLSI document M100-S18. 2014
. Wayne, PA: Clinical and Laboratory Standards Institute; 2014.
Burke JP, Yeo TW. Nosocomial urinary tract infections. In: Mayhall CG editor. Hospital epidemiology infection control
. 3rd ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2004:267–286.
Erikson H, Iverson B, Aavitsland P. Prevalence of nosocomial infections in hospitals in Norway, 2002 and 2003. J Hosp Infect 2005; 60:40–45.
Bagshaw SM, Laupland KB. Epidemiology of intensive care unit-acquired urinary tract infections. Curr Opin Infect Dis 2006; 19:67–71.
Parlak E, Erol S, Kizilkaya M, Altoparlak U, Parlak M. Nosocomial urinary tract infections in the intensive care unit patients. Mikrobiyol Bul 2007; 41:39–49.
Foxman B. Epidemiology of urinary tract infections: incidence, morbidity, and economic costs. Am J Med 2002; 113:S5–S13.
Laupland KB, Zygun DA, Davies HD, Church DL, Louie TG, Doig CJ. Incidence and risk factors for acquiring nosocomial urinary tract infection in the critically ill. J Crit Care 2002; 17:50–57.
Gaynes R, Edwards JR. Overview of nosocomial infections caused by gram-negative bacilli. Clin Infect Dis 2005; 41:848–854.
Al-Hasan MN, Eckel-Passow JE, Baddour LM. Bacteremia complicating Gram-negative urinary tract infections: a population-based study. J Infect 2010; 60:278–285.
Rashid T, Ebringer A. Ankylosing spondylitis is linked to Klebsiella
− the evidence. Clin Rheumatol 2007; 26:858–864.
Sader HS, Jones RN, Dowzicky MJ, Fritsche TR. Antimicrobial activity of tigecycline tested against nosocomial bacterial pathogens from patients hospitalized in the intensive care unit. Diagn Microbiol Infect Dis 2005; 52:203–208.
Zhanel GG, DeCorby M, Laing N, Weshnoweski B, Vashisht R, Tailor F et al.
Canadian Antimicrobial Resistance Alliance (CARA). Antimicrobial-resistant pathogens in intensive care units in Canada: results of the Canadian National Intensive Care Unit (CAN-ICU) study, 2005–2006. Antimicrob Agents Chemother 2008; 52:1430–1437.
Hsueh PR, Chen WH, Luh KT. Relationships between antimicrobial use and antimicrobial resistance in Gram-negative bacteria causing nosocomial infections from 1991–2003 at a university in Taiwan. Int J Antimicrob Agents 2005; 26:463–472.
Beceiro A, Tomás M, Bou G. Antimicrobial resistance and virulence: a successful or deleterious association in the bacterial world? Clin Microbiol Rev 2013; 26:185–230.
Daef EA, Aly SA, El-Din S, El Sherbiny , El Gendy SM. Phenotypic and genotypic detection of extended spectrum beta lactamase Klebsiella pneumoniae
isolated from intensive care units in Assiut University Hospital. Egypt J Med Microbiol 2009; 18:29–40.
Daef E, Elsherbiny N. Clinical and Microbiological Profile of Nosocomial Infections in Adult Intensive Care Units at Assiut University Hospitals, Egypt. J Am Sci 2012; 8:12–17.
Hernández JR, Martínez-Martínez L, Cantón R, Coque TM, Pascual A. Spanish Group for Nosocomial Infections (GEIH). Nationwide study of Escherichia coli
and Klebsiella pneumoniae
producing extended-spectrum beta-lactamases in Spain. Antimicrob Agents Chemother 2005; 49:2122–2125.
[Table 1], [Table 2], [Table 3]