Scandinavian Journal of Infectious Diseases, 2012; 44: 344–349
ORIGINAL ARTICLE
Factors associated with catheter-associated urinary tract infections and the effects of other concomitant nosocomial infections in intensive care units
EKREM TEMIZ1, NIHAL PISKIN2, HANDE AYDEMIR2, NEFISE OZTOPRAK2, DENIZ AKDUMAN2, GUVEN CELEBI2 & FURUZAN KOKTURK3
From the 1Departments of Infectious Diseases and Clinical Microbiology, Bitlis Government Hospital, Bitlis, 2Departments of Infectious Diseases and Clinical Microbiology, and 3Department of Biostatistics, School of Medicine, Zonguldak Karaelmas University, Zonguldak,Turkey
Abstract
Background: Catheter-associated urinary tract infections (CAUTIs) are the most common nosocomial infections in inten- sive care units (ICUs). The objectives of this study were to describe the incidence, aetiology, and risk factors of CAUTIs in ICUs and to determine whether concomitant nosocomial infections alter risk factors. Methods: Between April and Octo- ber 2008, all adult catheterized patients admitted to the ICUs of Zonguldak Karaelmas University Hospital were screened daily, and clinical and microbiological data were collected for each patient. Results: Two hundred and four patients were included and 85 developed a nosocomial infection. Among these patients, 22 developed a CAUTI alone, 38 developed a CAUTI with an additional nosocomial infection, either concomitantly or prior to the onset of the CAUTI, and 25 devel- oped nosocomial infections at other sites. The CAUTI rate was 19.02 per 1000 catheter-days. A Cox proportional hazard model showed that in the presence of other site nosocomial infections, immune suppression (hazard ratio (HR) 3.73, 95% CI 1.47–9.46; p0.006), previous antibiotic usage (HR 2.06, 95% CI 1.11–3.83; p0.023), and the presence of a noso- comial infection at another site (HR 1.82, 95% CI 1.04–3.20; p0.037) were the factors associated with the acquisition of CAUTIs with or without a nosocomial infection at another site. When we excluded the other site nosocomial infections to determine if the risk factors differed depending on the presence of other nosocomial infections, female gender (HR 2.67, 95% CI 1.03–6.91; p0.043) and duration of urinary catheterization (HR 1.07 (per day), 95% CI 1.01–1.13; p0.019) were found to be the risk factors for the acquisition of CAUTIs alone. Conclusions: Our results showed that the presence of nosocomial infections at another site was an independent risk factor for the acquisition of a CAUTI and that their pres- ence alters risk factors.
Keywords: Urinary tract infection, intensive care unit, incidence, risk factors
Introduction
Urinary tract infections (UTIs) are the most frequently encountered infections in intensive care units (ICUs), leading to significant morbidity and mortality and increased hospital costs. UTIs are of special concern in ICUs because most patients in ICUs receive an indwelling urinary catheter to monitor urine output or manage urine retention, and the presence of the indwelling catheter has been identified as the most important risk factor in the development of UTIs
[1,2]. Despite their importance, there have only been very limited studies focusing on catheter-associated UTIs (CAUTIs) in the critically ill, and in most of the published studies, the presence of other concomitant nosocomial infections, as a possible confounding fac- tor, was not taken into account [3–6]. The aim of this prospective study was to assess the incidence, aetiol- ogy, and risk factors of CAUTIs in ICUs and to deter- mine whether these risk factors differ based on the presence of other concomitant nosocomial infections.
Correspondence: N. Piskin, Zonguldak Karaelmas Üniversitesi, Tıp Fakültesi, Enfeksiyon Hastalıkları ve Klinik Mikrobiyoloji Anabilim Dalı, 67600 Kozlu, Zonguldak,Turkey.Tel:90 372 261 32 00. Fax:90 372 261 02 64. E-mail: nihal_piskin@yahoo.com
(Received 23 March 2011; accepted 2 November 2011)
ISSN 0036-5548 print/ISSN 1651-1980 online © 2012 Informa Healthcare DOI: 10.3109/00365548.2011.639031
Materials and methods
This study was conducted at Zonguldak Karaelmas University Hospital, a 524-bed referral and tertiary hospital.Two ICUs participated in the study: the gen- eral ICU (23 beds), which admits surgical, medical, and trauma patients, and the chest ICU (6 beds). All adult patients admitted to the selected ICUs between 1 April and 1 October 2008 and who were in the ICU for at least 48 h were included in this study. The hos- pital ethics committee approved the study.
Patients were catheterized upon admission or during their stay in one of the ICUs, and all patients were screened daily for the acquisition of CAUTIs. A quantitative urine culture was performed upon admission and then once per week or at the time that clinical manifestations of a CAUTI were observed (fever38°C, dysuria, and suprapubic tenderness). Patients with a positive urine culture upon admission and patients with asymptomatic bacteriuria were not included. To ensure sterile conditions, urethral cath- eters were inserted by physicians employing standard techniques. Silicone Foley catheters were used and each catheter was connected to a closed drainage system. Routine meatal and perineal hygiene was performed daily using povidone–iodine. The urine specimen was aspirated aseptically from the sampling port of the catheter, and it was taken immediately to the microbiology laboratory. Standard culture and bacteriological techniques were used to identify any isolated organisms. A CAUTI was defined as a quan- titative culture containing 105 colony-forming units (CFU)/ml of 1 or 2 organisms, according to the cri- teria of the US Centers for Disease Control and Pre- vention [7]. If more than 2 microorganisms were isolated, the sample was considered to be contami- nated. Standardized surveillance forms were used for all patients who met the inclusion criteria. Each day, the infectious diseases staff discussed positive physi- cal and bacteriological examinations that indicated the acquisition of a CAUTI or any other nosocomial infection. When a patient was discharged from the ICU, screening was continued for 7 days. Clinical, radiological, and microbiological data were collected for each patient. Clinical data included age, sex, diag- nosis on admission, presence of an infection on admission (except UTI), underlying diseases, antibi- otic use in the previous 3 months, Acute Physiology and Chronic Health Evaluation (APACHE II) score on admission, type of ICU, length of ICU stay, pres- ence of invasive procedures, and mortality.
Statistical analysis
The statistical analysis was performed using SPSS version 13.0 statistical software (SPSS Inc., Chicago,
IL, USA). A p-value of0.05 was considered to be significant in the analysis. Univariate analysis was performed to determine the risk factors for ICU- acquired CAUTI. The Chi-square test or Fisher’s exact test was used for categorical variables. Con- tinuous variables were tested using the Student’s t-test. The Cox proportional hazard model was per- formed to assess the independent factors for ICU- acquired CAUTI.
Results
During the study period, 259 patients were admitted to the 2 selected ICUs.The 46 patients who were not catheterized during their ICU stay, 4 patients with a positive urine culture on admission, and 5 patients with asymptomatic bacteriuria were all excluded from the study. Of the 204 patients who met the inclusion criteria, 85 (41.6%) developed an ICU- acquired infection. Among these 85 patients, 22 developed a CAUTI alone (CAUTI-A), 38 devel- oped a CAUTI along with an accompanying noso- comial infection (CAUTI-NI), either concomitantly or prior to UTI, and 25 developed a nosocomial infection alone, not related to the CAUTI (NI-A) (Figure 1).The accompanying nosocomial infections were as follows: pneumonia in 22 patients, intravas- cular catheter-related bacteraemia in 10 patients, and surgical site infections (SSI) in 6 patients. The iso- lated pathogens from these accompanying infections were: Acinetobacter spp. in 20 patients, Pseudomo- nas aeruginosa in 8 patients, coagulase-negative Staphylococcus in 4 patients, Escherichia coli in 4 patients, and methicillin-resistant Staphylococcus aureus in 2 patients.
A total of 66 ICU-acquired CAUTI episodes occurred among 60 (24%) patients. The CAUTI rate was 19.02 per 1000 catheter-days. The isolated patho- gens were Candida spp. (33.3%), E. coli (24.2%), Enterococcus spp. (15.2%), Klebsiella pneumoniae (10.6%), P. aeruginosa (9.1%), Proteus spp. (4.5%), Acinetobacter spp. (1.5%), and Enterobacter cloacae (1.5%). None of the UTI episodes were polymicrobial. Of the 38 CAUTI-NI patients, 17 developed a CAUTI following treatment of the nosocomial infection, 6 patients were diagnosed concomitantly, and 15 patients were on antibiotic treatment for the nosocomial infec- tion at another site when the CAUTI was diagnosed. In 6 of these 15 patients, Candida spp. were isolated and in the remaining patients the isolated pathogens were also resistant to the antibiotics prescribed to treat them, including 3 penicillin-resistant enterococci, 3 extended-spectrum beta-lactamase (ESBL)-producing E. coli, and 3 ESBL-producing K. pneumoniae. The mean infection development time after admission for
Factors associated with CAUTIs in ICUs 345
346 E. Temiz et al.
Exclusion criteria:
Patients who were not catheterized (n = 46) Patients with a positive urine culture on admission (n = 4)
Patients with asymptomatic bacteriuria (n = 5)
Patients acquired CAUTI n = 60
Total patients n = 259
Patients included in the risk factor analysis n = 204
1st control group (patients who did not acquire CAUTI) n = 144
Patients acquired CAUTI + other site NI (CAUTI-NI) n = 38
Patients acquired CAUTI alone (CAUTI-A) n = 22
2nd control group (patients who did not acquire any NI) n = 119
Patients acquired other site NI alone (NI-A) n = 25
Figure 1. Patient groups according to their infection status (CAUTI, catheter-associated urinary tract infection; NI, nosocomial infection). accompanying nosocomial infections was 5.13 2.94 days and the mean CAUTI development time was 15.72 17.06 days. The delay between the develop- ment of other nosocomial infection and a CAUTI epi- sode was 15.89 18.16 days.The CAUTI development time after admission was 14.816.2 days in women and 16.718.2 days in men (p0.761)
A cohort of 204 patients was used to describe the risk factors associated with acquiring a CAUTI, and we performed the analysis in the presence or absence of nosocomial infections at other anatomical sites. A total of 144 patients; 119 patients did not acquire any nosocomial infections and these patients along with the NI-A group (n=25), served as the first con- trol group. Control group 1 was compared to the 60 patients who acquired a CAUTI with or without an accompanying nosocomial infection at another ana- tomical site (CAUTI-A and CAUTI-NI). We per- formed a subgroup analysis by excluding patients who developed nosocomial infections at other sites, and 119 patients who did not develop any nosoco- mial infections served as the second control group, which was compared to the 22 CAUTI-A patients (Figure 1). The results of the univariate analysis are presented in Table I.
We used a Cox proportional hazard model, taking into account the time at which CAUTIs and other nosocomial infections occurred, to determine the risk factors for these infections. Age, gender, type of ICU, presence of an infection on admission, presence of underlying diseases (diabetes mellitus, renal failure, chronic obstructive pulmonary disease, congestive heart failure, malignancy, immune suppression, and recent surgery), previous antibiotic usage, presence of mechanical ventilation and central venous catheter, duration of urinary catheterization, APACHE II score on admission, and the presence of other site nosoco- mial infections were included in the model. The haz- ard rates of CAUTIs stratified by the presence of other nosocomial infections are presented in Table II.
Discussion
This study evaluated the incidence, aetiology, and risk factors of CAUTIs in the ICUs of a university hos- pital.The CAUTI rate was higher at this hospital than the rates in the USA described by the National Noso- comial Infections Surveillance study (3.9 per 1000 catheter-days) [8]. However, our rates were similar to those identified in the ICUs of Argentina and Egypt (15.7–18.5 per 1000 catheter-days) [6,9]. The factors affecting high infection rates in the ICUs in develop- ing countries have already been described in previ- ously published studies, and some of these factors include over-crowded wards, a shortage of trained personnel, and insufficient supplies, which may also explain the high rates observed in this study [10].
There are several published studies based on catheterized patients that identify risk factors for the acquisition of CAUTIs. The most important inde- pendent risk factor identified in every study is the duration of urinary catheterization [2–6]. Female gender is another common risk factor associated with an increased risk of CAUTI [2–4], but in other stud- ies, this has not always been reported as an indepen- dent risk factor [5,6].The literature also suggests that other risk factors, such as severity of illness at admis- sion, unit of admission, length of ICU stay, prior antibiotic exposure, and attention to catheter care are associated with the CAUTI risk, but the relationship
Factors associated with CAUTIs in ICUs 347 Table I. Risk factors associated with acquiring CAUTIs in the presence or absence of other site nosocomial infections(univariate analysis). Variables
Age, mean SD
Female sex
Medical ICU
Presence of infection on admission Underlying diseases
DM
Renal failure
COPD
Chronic heart failure Malignancy
Immune suppression CVD
Recent surgery
Previous antibiotic usage Invasive procedures
Central venous catheterization
Mechanical ventilation
Duration of urinary catheterization, mean SD
Length of hospital stay, mean SD
Length of ICU stay, mean SD
APACHE II score on admission, meanSD
Patients who acquired a CAUTI with or without
First control (patients who did not acquire a CAUTI)
(n 144)
63.43 17.06 64 (44.4) 88 (61.1) 59 (41.0)
14 (9.7) 9 (6.3)
24 (16.7) 12 (8.3) 32 (22.2)
1 (0.7) 16 (11.1) 38 (26.4) 8 (5.6)
45 (31.3)
52 (36.1) 8.19 5.54
16.86 12.33 10.62 8.77 12.75.1
Patients who acquired a CAUTI alone
(n 22)
69.77 15.77 16 (72.7)
17 (77.3)
9 (40.9)
2 (9.1) 2 (9.1) 5 (22.7) 5 (22.7) 5 (22.7) 3 (13.6) 3 (13.6) 4 (18.2) 5 (22.7)
9 (40.9)
9 (40.9) 13.68 6.73
19.64 8.35 13.14 8.24 13.09 5.61
Second control (patients who did not acquire any NI)
(n 119)
63.97 16.66 54 (45.4) 71 (59.7) 48 (40.3)
12 (10.1) 9 (7.6) 21 (17.6)
10 (8.4) 26 (21.8)
1 (0.8) 12 (10.1) 31 (26.1) 7 (5.9)
37 (31.1) 40 (33.6)
7.39 4.7 15.16 11.32
9.61 7.92 12.74 5.02
an accompanying (n60)
69.08 15.32 32 (53.3) 50 (83.3) 26 (43.3)
9 (15.0) 2 (3.3) 8 (13.3)
10 (16.7) 12 (20.0) 5 (8.3) 14 (23.3) 11 (18.3) 13 (21.7)
33 (55.0)
32 (53.3) 32.9336.23
37.9835.25 31.8036.94 13.84.7
NI
Results are n(%) unless otherwise stated.
CAUTI, catheter-associated urinary tract infection; NI, nosocomial infection; SD, standard deviation; ICU, intensive care unit; DM, diabetes mellitus; COPD, chronic obstructive pulmonary disease; CVD, cerebrovascular disease. between these risk factors and the acquisition of CAUTIs is controversial [2–6,11]. These contradic- tory results are possibly related to the heterogeneity of the selected study populations or the effect of including the other site infections in the risk factor
Table II. Results of Cox proportional hazards model.
Variable Variable
In the presence of other site NIa Presence of immune suppression Previous antibiotic usage Presence of other site NI
In the absence of other site NIb Female sex Duration of urinary catheterization (per day) p-Value 0.027
0.246 0.003 0.755
0.399 0.514 0.700 0.133 0.869 0.009 0.042 0.295 0.001
0.001
0.023 0.001 0.001 0.001 0.157 p-Value 0.103
0.034 0.185 1.000
1.000 0.682 0.557 0.060 1.000 0.012 0.705 0.606 0.022
0.513
0.677 0.001
0.005 0.009 0.741
analysis. In particular, among critically ill patients, it was not uncommon to develop infections at more than 1 site; however, none of the previously published studies evaluating ICU-acquired CAUTIs mentioned whether the patients had an accompanying other site
HR 95% CI 3.73 1.47–9.46
2.06 1.11–3.83 1.82 1.04–3.20 2.67 1.03–6.9 1.07 1.01–1.13 p-Value 0.006
0.023 0.037 0.043 0.019
NI, nosocomial infection; HR, hazard ratio; CI, confidence interval. aThe model included 144 patients who did not acquire a CAUTI (first control group) and 60 patients who acquired a CAUTI and an accompanying other site NI. bThe model included 119 patients who did not acquire any NI (second control group) and 22 patients who acquired a CAUTI alone.
348 E. Temiz et al. infection [2,6]. In fact, the presence of other active sites of infection was only reported as a risk factor for CAUTIs in a single study by Maki and Tambyah [11]. In another study that aimed to define the clin- ical features and symptoms of CAUTIs, other site nosocomial infections were excluded as a confound- ing factor, but the authors did not perform a risk factor analysis [12].
In the present study, we performed a risk factor analysis for 2 groups, including patients who acquired a CAUTI with or without another accompanying nosocomial infection and patients who only acquired a CAUTI, to determine the possible confounding effect of other site nosocomial infections. In the uni- variate analysis, duration of catheterization was found to be a significant risk factor in both groups, which is consistent with other published studies [2–6,11,13]. Age, type of ICU, the presence of central venous catheterization, mechanical ventilation, and underly- ing cerebrovascular disease were not found to be significant risk factors for the development of CAUTIs alone; however, these factors were found to be associated with the development of CAUTIs with or without an accompanying nosocomial infection. In contrast, female gender was only associated with the development of CAUTIs alone.
The contradictory results of the univariate anal- ysis strengthened our hypothesis, and in an attempt to determine the effect of other site nosocomial infections more definitively, we used the Cox regres- sion model. When we entered the presence of other nosocomial infections as an indicator into the Cox model, the presence of immune suppression, previ- ous antibiotic usage, and the presence of other site nosocomial infections were found to be the indepen- dent risk factors for the acquisition of CAUTIs with or without an accompanying nosocomial infection at another site. The presence of immune suppression suggests a reduced health status and a compromised immune system, and these conditions might render patients susceptible to infection. Although we found that previous antibiotic usage was an independent risk factor, the relationship between the use of anti- biotics and CAUTI has been controversial, and in some studies, the antibiotic usage has been reported as a risk factor, whereas in other studies, it has been reported as a protective factor [3,4]. In a systematic review of the subject, it was stated that the protective effect of antibiotic use was for short-term catheter- izations, but that antibiotics select for infections caused by multidrug-resistant Gram-negative bacilli, enterococci, and yeasts [11]. These microorganisms were the leading pathogens in the present study, and the patients in this study required prolonged cath- eterization, so this could be an explanation as to why antibiotic usage was found to be a risk factor. The presence of other site nosocomial infections was also found to be an independent risk factor for the acqui- sition of CAUTIs, increasing the risk by 1.82-fold. The antibiotic usage for the other site nosocomial infections, and the reduced health status as an out- come of prior nosocomial infections, may facilitate the acquisition of a CAUTI. Maki and Tambyah also reported that patients with other active sites of infec- tion had an increased risk for CAUTIs (risk ratio 2.3–2.4), but there are no other published studies that have focused on the presence of other site noso- comial infections [11]. In the second Cox model that we performed excluding the patients who acquired other site nosocomial infections, the duration of uri- nary catheterization and female gender were found to be independently associated with the acquisition of a CAUTI alone. The ascending route of infection and the shorter female urethra make contamination more likely, and as a result, UTIs are much more common in women than in men [13]. However, there was no known predisposition of gender for the acquisition of any other nosocomial infections, so we could not find a significant association with gender in the first group. Although duration of catheteriza- tion is the most important and well-known risk fac- tor for the acquisition of CAUTIs [2–6,11,13], it was not found as an independent risk factor in the first group but only in the second group, probably because of the confounding effect of other site noso- comial infections.
The present study had several limitations. A quantitative urine culture was performed only once per week or when clinical manifestations of a CAUTI occurred; therefore, the duration of catheterization before the onset of infection may be overestimated. Catheter care violations, which have been identified as a risk factor, were not taken into account. The small number of patients may be inadequate to determine more definitive results of the confound- ing effects of other accompanying nosocomial infections.
Although the development of concomitant noso- comial infections frequently occurs in the ICU set- ting, this is the first report evaluating the risk factors for the acquisition of CAUTIs in the presence or absence of other accompanying nosocomial infec- tions. Larger studies are needed to improve our understanding of the role of the accompanying noso- comial infections. Our results also underline the necessity of reducing the duration of catheterization to avoid the development of CAUTIs in ICU patients.
Declaration of interest: All authors report no con- flict of interest relevant to this article.
References
[1] Laupland KB, Zygun DA, Davies HD, Church DL, Louie TJ, Doig CJ. Incidence and risk factors for acquiring noso- comial urinary tract infection in the critically ill. J Crit Care 2002;17:50–7.
[2] Bagshaw SM, Laupland KB. Epidemiology of intensive care unit-acquired urinary tract infections. Curr Opin Infect Dis 2006;19:67–71.
[3] Leone M, Albanèse J, Garnier F, Sapin C, Barrau K, Bimar MC, et al. Risk factors of nosocomial catheter-associated urinary tract infection in a polyvalent intensive care unit. Intensive Care Med 2003;29:1077–80.
[4] 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;20:260–2.
[5] Laupland KB, Bagshaw SM, Gregson DB, Kirkpatrick AW, Ross T, Church DL. Intensive care unit-acquired urinary tract infections in a regional critical care system. Crit Care 2005;9:60–5.
[6] Talaat M, Hafez S, Saied T, Elfeky R, El-Shoubary W, Pimen- tel G. Surveillance of catheter-associated urinary tract infection in 4 intensive care units at Alexandria university hospitals in Egypt. Am J Infect Control 2010;38:222–8.
[7] Garner JS, Jarvis WR, Emori TG, Horan TC, Hughes JM. CDC definitions for nosocomial infections, 1988. Am J Infect Control 1988;16:128–40.
[8] Centers for Disease Control and Prevention. National Noso- comial Infections surveillance (NNIS) system report, data summary from January 1992 through June 2004, issued October 2004. Am J Infect Control 2004;32:470–85.
[9] Rosenthal VD, Guzmán S, Crnich C. Device-associated nosocomial infection rates in intensive care units of Argen- tina. Infect Control Hosp Epidemiol 2004;25:251–5.
[10] Leblebicioglu H, Rosenthal VD, Arikan OA, Ozgültekin A,Yal- cin AN, Koksal I, et al.; Turkish Branch of INICC. Device- associated hospital-acquired infection rates in Turkish intensive care units. Findings of the International Nosocomial Infection Control Consortium (INICC). J Hosp Infect 2007;65:251–7.
[11] Maki DG,Tambyah PA. Engineering out the risk of infection with urinary catheters. Emerg Infect Dis 2001;7:2–6.
[12] Tambyah PA, Maki DG. Catheter-associated urinary tract infection is rarely symptomatic: a prospective study of 1,497 catheterized patients. Arch Intern Med 2000;160:678–82.
[13] Sobell JD, Kaye D. Urinary tract infections. In: Mandell GL, Bennett JE, Dolin R, editors. Principles and practices of infectious diseases. 7th ed. Philadelphia: Churchill Living- stone Elsevier; 2010. pp. 958–85.