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Keywords:

  • Bacteraemia;
  • blood cultures;
  • catheter-related bloodstream infection;
  • catheter-related infections;
  • central line-associated bloodstream infection;
  • vascular catheter

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Authors’ Contribution
  9. Transparency Declaration
  10. References
  11. Supporting Information

Clin Microbiol Infect

Abstract

The incidence of central-line-associated bloodstream infection (CLA-BSI) is reported per 1000 days of catheter exposure, mainly in the intensive care unit (ICU), because recording exposure throughout an institution is not always feasible. Confirmation of catheter-related bloodstream infection (CR-BSI) requires specific laboratory testing that identifies the catheter as the source of infection. This information is available in microbiology laboratories and can be assessed using a denominator of 1000 admissions. We evaluated recent trends in the incidence and aetiology of CR-BSI and compared adult ICUs with the remaining areas of the hospital in a retrospective cohort analysis of all confirmed CR-BSIs. During the 8-year study period, we recorded 1208 episodes (8.2% of BSIs) of CR-BSI. After adjusting for the blood cultures drawn, a significant reduction in incidence was observed in adult ICUs (47%), where care bundles had been applied. The reduction was similar irrespective of whether CLA-BSI or CR-BSI was assessed. We recorded a significant reduction in the incidence of Staphylococcus aureus CR-BSI, and a significant increase in the incidence of CR-BSI caused by Enterococcus sp., Gram-negative microorganisms and fungi. The microbiology department may complement CLA-BSI/1000 catheter-days by providing CR-BSI when days of exposure are not available, because both figures are parallel. We demonstrated a significant reduction in the incidence of CR-BSI in recent years in the population admitted to adult ICUs but not in the remaining areas of the hospital. A shift in the aetiological spectrum of CR-BSI may be occurring.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Authors’ Contribution
  9. Transparency Declaration
  10. References
  11. Supporting Information

Evolution of the incidence of central-line-associated bloodstream infection (CLA-BSI) has been assessed mainly in adult intensive care units (ICUs) where care bundles have been implemented in recent years [1–3]. However, a significant number of CLA-BSI episodes occur outside the ICU, in areas where quality control programmes are not always implemented. Information regarding the evolution of CLA-BSI throughout an institution is scarce, probably due to the difficulty in determining the number of days of exposure to a catheter. Furthermore, confirmation of CLA-BSI does not require microbiological laboratory testing; therefore, the problem may be overestimated, and infection could be attributed to other causes [4]. New and easier methods to report hospital-wide trends are clearly required [5].

By contrast, catheter-related bloodstream infection (CR-BSI) requires specific laboratory testing that more thoroughly identifies the catheter as the source of infection. This information is always available in the microbiology department and can be reported against the denominator of 1000 admissions or 1000 days of stay, both of which are readily available in hospitals.

Data regarding secular trends in the incidence and aetiology of CR-BSI in general hospitals are very scarce [6], and most findings are biased by the selection of specific units and patients or short study periods [7–9].

The aim of our study was to assess secular trends in the incidence and aetiology of CR-BSI in a large general hospital using the microbiology laboratory as a watchtower. We also compared CR-BSI in the adult ICUs with the remaining areas of the hospital.

Material and Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Authors’ Contribution
  9. Transparency Declaration
  10. References
  11. Supporting Information

Our hospital is a general teaching institution serving a population that ranged from 704 030 to 806 769 inhabitants during the study period (January 2003–December 2010). The number of beds available decreased from 2500 to approximately 1550 during this period as a result of the opening of new primary care hospitals to absorb less complex patients. Our hospital provides all the services of a general teaching hospital. We included all blood and catheter samples sent for bacterial and fungal culture to our laboratory during the study period.

Blood culture systems

Our institution recommends extraction of three blood samples for evaluation of all episodes of suspected bacteraemia or fungaemia. Blood cultures were processed using BACTEC 9240 (Becton Dickinson Microbiology Systems, Maryland, DE, USA). Methods for processing positive blood cultures were standard [10].

Catheter cultures

In our hospital we followed CDC Guidelines for sending vascular catheter tips from patients with clinical suspicion of sepsis for culture in the Microbiology Department [4]. All catheter tips were cultured immediately according to the semi-quantitative roll-plate technique [11]. All microorganisms present in counts ≥15 colony-forming units (CFUs) were identified to genus and species level, and information on antimicrobial susceptibility was recorded.

Definitions

An episode of ‘significant’ bloodstream infection was defined as an episode of bacteraemia or fungaemia, in which those pathogens were present in ≥1 blood cultures. We considered commensal microorganisms [coagulase negative Staphylococci (CNS), Corynebacterium sp. (except C. jeikeium), Lactobacillus sp., Bacillus sp. and Propionibacterium sp., or viridans group Streptococcus isolates and C. perfringens] as probable pathogens when they were recovered in ≥2 blood cultures. In the case of neonates, due to the difficulty in obtaining blood from these patients and following standard recommendations, we accepted as significant the presence of CNS or other potential contaminants in both bottles of a single venous puncture. Only the number of patients—not the number of blood cultures—was taken into consideration. All microorganisms isolated from blood from the same patient within 1 week were considered a single episode.

The definitions for catheter infections are those detailed in the Clinical Practice Guidelines for the Diagnosis and Management of Intravascular Catheter-Related Infection [4]. In summary, CR-BSI was defined as those episodes in which the same microorganism was recovered from blood and a catheter segment with an interval of <8 days, provided that there was no infection at another site. Other CR-BSI episodes diagnosed by quantitative blood cultures or differential time to positivity (DTTP) were excluded. Central-line-associated bloodstream infection (CLA-BSI) was defined as having a primary bloodstream infection (BSI) in a patient with a central line in place within a 48-h period before onset of the BSI that was not related to infection at another site.

Microorganisms recovered from blood or catheters were identified using the automated MicroScan system with the POS Combo Panel Type 2S and NEG Combo Panel Type 1S (DADE Behring, Sacramento, CA, USA).

Implementation of catheter care bundles

In 2009, our institution joined a national programme to implement a catheter care bundle in adult ICUs, with the intention of reaching zero incidence of CLA-BSI. This consisted of incorporating the following five evidence-based procedures recommended by the CDC: hand hygiene, using full-barrier precautions during the insertion of central venous catheters, cleaning the skin with chlorhexidine, avoiding the femoral site if possible, and removing unnecessary catheters [3].

Statistical analysis

The database of episodes of significant BSI was prospectively updated on a daily basis by the same member of staff of the microbiology laboratory from the beginning of the study. This database also included all endovascular catheters during the study period.

The global incidence of BSI and CR-BSI is expressed as episodes per 1000 admissions.

Overall trends in rate per month over time were adjusted using Poisson regression analysis to estimate the incidence rate ratio (IRR) with a 95% confidence interval (95% CI) adjusted for the number of monthly blood cultures. In order to analyse the evolution of our series, we estimated the IRR, for which the reference year was 2003. Evolution of microorganisms was expressed as the annual IRR.

In order to compare trends in the evolution of catheter-related infections (CLA-BSI/1000 days of exposure vs. CR-BSI/1000 admissions), we estimated the slope in one of the adult ICUs on which both sets of data were available throughout the study period. The slope of annual IRR compared with 2003 was adjusted using linear regression. These slopes are presented with a 95% CI.

All analyses were performed using SPSS v.14 for Windows e (SPSS Inc, Chicago, IL, USA) and STATA v.11.

Statistical significance was set at p <0.05.

Ethics committee approval

This study has been approved by our local ethics committee.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Authors’ Contribution
  9. Transparency Declaration
  10. References
  11. Supporting Information

Correlation between CR-BSI obtained from microbiology laboratory data and epidemiological CLA-BSI data recorded at the bedside

Our institution had 479 710 admissions during the study period (mean, 59 964 admissions/year). We received a total of 356 497 and 17 642 blood culture samples and catheter tips for culture, respectively (Table 1a). The total number of significant episodes of BSI was 14 713 (30.67 episodes/1000 admissions). Of these, 1208 episodes (8.2%) had a simultaneous catheter with a positive culture with the same microorganism and were considered CR-BSI. The remaining 13 505 BSI episodes were those without concomitant or negative catheter tip cultures. The incidence of CR-BSI ranged from 1.9 to 3.6 episodes/1000 admissions (mean, 2.5 episodes/1000 admissions). As for location, 35.5% of CR-BSIs occurred in adult ICUs, 27% in paediatric ICUs, and the remaining 37.5% occurred in other units.

Table 1. Evolution of CR-BSI during the study period
(a) Global data
YearOverall admissionsTotal BSI (per 1000 admissions)Episodes of BSI without concomitant or negative TC (per 1000 admissions)No. of received BCsNo. of received CTs
2003 54 7811613 (29.44)   26.6938 796    2143
2004 61 2991642 (26.79)   24.9140 713    2406
2005 62 7731773 (28.24)   25.9544 187    2399
2006 65 6812040 (31.06)   28.7847 101    2044
2007 67 8822232 (32.88)   30.4951 753    1910
2008 58 7241944 (33.10)   30.3847 338    1815
2009 53 4331825 (34.15)   30.6046 659    2545
2010 55 1371644 (29.82)   27.3539 950    2380
Total (annual average)479 710 (59 964)14 713 (30.67)   28.14356 497   17 642
(b) Specific data
YearEpisodes of CR-BSI (per 1000 admissions)% CR-BSIAdult ICUsAll other units
AdmissionsEpisodes of CR-BSI (per 1000 admissions)AdmissionsEpisodes of CR-BSI (per 1000 admissions)
  1. BSI, bloodstream infections; BCs, blood cultures; TC, tip culture; CTs, catheters; CR-BSI, catheter-related bloodstream infection; ICUs, intensive care units.

2003   151 (2.8)  9.4   353851 (14.41) 51 243100 (1.95)
2004   115 (1.9)  7.0   362940 (11.02) 57 67075 (1.30)
2005   144 (2.3)  8.1   376046 (12.23) 59 01398 (.66)
2006   150 (2.3)  7.4   399574 (18.52) 61 68676 (1.23)
2007   162 (2.4)  7.3   395963 (15.91) 63 92398 (1.55)
2008   160 (2.7)  8.2   392849 (12.47) 54 796111 (2.03)
2009   190 (3.6) 10.4   372671 (19.06) 49 707119 (2.39)
2010   136 (2.5)  8.3   370636 (9.71) 51 431101 (1.94)
Total (annual average)  1208 (2.5)  8.2  30 241 (3780)430 (14.22)449 462 (56 183)778 (1.73)

When data were analysed on a monthly basis, we detected significant variations in CR-BSI from month to month. However, no significant overall reduction in the adjusted incidence of CR-BSI was detected from the beginning to the end of the study period (p 0.598) (Fig. 1a).

image

Figure 1.  (a) Evolution of the incidence rate ratio of microbiologically confirmed CR-BSI/1000 admissions. (b) Evolution of incidence rate ratio of the CR-BSI/1000 admissions in adult ICUs compared with the remaining hospital units. Ad, admissions; ICUs, intensive care units.

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We compared trends in the incidence of CR-BSI in adult ICUs with those for other departments (Table 1b). In adult ICUs, the IRR was 45% after adjusting for the number of blood cultures drawn (95% CI, 15–65%; p 0.007). In the remaining areas of the institution, where care bundles had not been implemented, there were no significant differences from the 2003 reference values (Fig. 1b).

In order to assess the parallelism between CLA-BSI/1000 days of exposure and CR-BSI/1000 admissions, we selected an ICU in which the monthly CLA-BSI data were available throughout the study period. The correlation between both methods of assessment showed clear parallelism, with a slope of episodes/1000 admissions of 0.92 (95% CI, 0.84–1.00; p 0.046) for CR-BSI vs. a slope of 0.91 (95% CI, 0.83–0.99; p 0.055) for CLA-BSI. The comparison between both IRR graphs also showed no statistically significant differences (p 0.879) (Fig. 2).

image

Figure 2.  Comparison of the incidence rate ratio of CLA-BSI/1000 catheter days (cd) in an adult ICU and episodes of CR-BSI/1000 admissions (ad). MIC, microbiology laboratory; ICU, intensive care unit; a, admissions; cd, catheter days. *The slope of annual IRR compared with 2003 was adjusted using linear regression. These slopes are presented with a 95% CI. **Grade matching was performed by the Poisson model.

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Aetiology and evolution of CR-BSI

During the study period, 1255 microorganisms from 1208 episodes of CR-BSI were identified from blood and catheter tips simultaneously.

CR-BSI was caused by Gram-positive bacteria in 67% of episodes, and the remaining episodes were caused by aerobic or facultative Gram-negative bacteria (17%) and fungi (16%).

The evolution of the incidence of different microorganisms throughout the study period is represented in Table 2 and Fig. 3.

Table 2. Evolution of the incidence of microorganisms during the study period
N (incidence per 1000 admissions)Year
20032004200520062007200820092010Total
  1. CoNS, coagulase-negative staphylococci; MS, methicillin susceptible; MR, methicillin resistant.

Gram (+)117 (2.14)90 (1.47)106 (1.69)91 (1.39)105 (1.55)101 (1.72)133 (2.49)88 (1.60)831 (1.73)
 CoNS65 (1.19)57 (0.93)70 (1.12)61 (0.93)63 (0.94)70 (1.19)87 (1.63)60 (1.09)534 (1.11)
 S. aureus45 (0.82)30 (0.49)22 (0.35)23 (0.35)31 (0.46)20 (0.34)24 (0.45)18 (0.33)213 (0.44)
 MS S. aureus21 (0.38)13 (0.21)13 (0.21)9 (0.14)11 (0.16)9 (0.15)17 (0.32)9 (0.16)102 (0.21)
 MR S. aureus24 (0.44)17 (0.28)9 (0.14)14 (0.21)20 (0.29)11 (0.19)7 (0.13)9 (0.16)111 (0.23)
 Enterococcus spp.5 (0.09)3 (0.05)15 (0.24)5 (0.08)9 (0.13)9 (0.15)21 (0.39)12 (0.22)79 (0.16)
 Other3 (0.054)02 (0.031)3 (0.045)2 (0.029)3 (0.051)2 (0.037)1 (0.018)16 (0.033)
Gram (−)18 (0.33)15 (0.24)31 (0.49)33 (0.50)23 (0.34)27 (0.46)35 (0.66)27 (0.49)209 (0.44)
 E. coli1 (0.02)4 (0.07)3 (0.05)1 (0.02)2 (0.03)9 (0.15)6 (0.07)3 (0.05)29 (0.06)
 Klebsiella spp.2 (0.04)5 (0.08)7 (0.11)7 (0.11)5 (0.07)3 (0.05)4 (0.07)7 (0.13)40 (0.08)
 Enterobacter spp.7 (0.13)2 (0.03)2 (0.03)8 (0.12)6 (0.09)7 (0.12)5 (0.09)2 (0.04)39 (0.08)
 Serratia spp.3 (0.05)1 (0.02)7 (0.11)4 (0.06)4 (0.06)1 (0.02)2 (0.04)3 (0.05)25 (0.05)
 Proteus spp.02 (0.03)03 (0.05)01 (0.02)3 (0.06)4 (0.07)13 (0.03)
 Pseudomonas spp.4 (0.07)06 (0.010)5 (0.08)3 (0.04)3 (0.05)9 (0.17)5 (0.09)35 (0.07)
Yeasts15 (0.27)13 (0.21)12 (0.19)28 (0.43)37 (0.55)34 (0.58)29 (0.54)26 (0.47)194 (0.40)
 Candida14 (0.26)13 (0.21)12 (0.19)27 (0.41)37 (0.55)34 (0.58)27 (0.51)26 (0.47)190 (0.40)
 C. albicans5 (0.09)3 (0.05)5 (0.08)10 (0.15)19 (0.28)11 (0.19)14 (0.26)16 (0.29)83 (0.17)
 C. parapsilosis6 (0.11)8 (0.13)7 (0.11)15 (0.23)14 (0.21)15 (0.26)10 (0.19)5 (0.09)80 (0.17)
 C. glabrata1 (0.02)2 (0.03)002 (0.03)3 (0.05)2 (0.04)3 (0.05)13 (0.03)
 C. tropicalis2 (0.04)001 (0.02)1 (0.01)3 (0.05)1 (0.02)1 (0.02)9 (0.02)
image

Figure 3.  Evolution of incidence rate ratio of episodes of Gram-positive, Gram-negative and fungal CR-BSIs.

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Our data show a 25% overall reduction in the incidence of Gram-positive agents (831 episodes) when 2010 is compared with the reference year of 2003 (95% CI, 1–44%; p 0.04).

The mean annual incidence of Gram-negative CR-BSI in our institution was 0.44 episodes/1000 admissions, with a significant increase of 8.9% per year (95% CI, 2.6–15.7%; p 0.005).

Episodes of fungal CR-BSI and the associated trends during the study period are summarized in Fig. 3. The incidence increased progressively from 2003 to 2010 at an annual rate of 14% (95% CI, 6–21%; p <0.001).

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Authors’ Contribution
  9. Transparency Declaration
  10. References
  11. Supporting Information

Our results show that the microbiology department could prove to be an excellent complementary watchtower for monitoring the incidence and aetiology of CR-BSI in hospitals or units where collection of days of catheter exposure is not feasible. We demonstrated a significant reduction in the incidence of CR-BSI in patients admitted to adult ICUs, but not in the remaining hospital areas. We also observed a potentially ongoing shift in the aetiological spectrum of CR-BSI, with a progressive decrease in the incidence of Gram-positive CR-BSI and a significant increase in that of Gram-negative agents and Candida.

CLA-BSI is a major healthcare problem that is associated with significant morbidity and mortality and increases in costs [4,12–14]. There are few data on secular trends in the incidence of this infection [6].

Moreover, data regarding the role of the microbiologist in monitoring CR-BSI trends are scarce. It has been recently reported that conducting surveillance for CLA-BSI by laboratory-based methods was better than it being carried out by infection preventionists [15].

The most common way to report CLA-BSI is as incidence density associated with days/patient of vascular catheter exposure. Using this denominator is common practice in most ICUs, although it is more difficult to assess for the whole population of a general hospital [16]. In contrast, CR-BSI requires microbiological confirmation of origin in a colonized catheter [4].

Continuous monitoring of CR-BSI in non-ICU areas is essential, although assessment of the days of exposure to catheters in a large hospital is not always feasible [6]. We are not suggesting that CLA-BSI be replaced by CR-BSI, because we are convinced of the utility of incidence density determination. We merely stress that, where monitoring of catheter days is not feasible, CR-BSI may be used as a complementary procedure to estimate bloodstream infections related to catheters in a whole institution based on the number of admissions or other available denominators. We chose number of admissions as our denominator because it was easier to obtain than number of patient days, which is submitted to political and administrative pressures for reducing hospital days. Moreover, when the denominator was patient days we obtained a parallel graph to that of admissions (see Supporting Information). Such an approach would allow benchmarking of larger areas of the hospital, thus extending the possibility of implementing catheter-care bundles in non-ICU units.

Future studies comparing CLA-BSI/1000 days with CR-BSI/1000 admissions should clarify the relationship between these figures. We compared secular trends in the incidence of CLA-BSI and CR-BSI in one of our adult ICUs and found a good correlation between both parameters, namely, a decrease in incidence. The closeness of both curves is justified by the characteristics of most ICUs, in which the number of device-days is almost equal to the number of patient-days.

Our study also points to a shift in the aetiological spectrum of CR-BSI in recent years. Reports on recent trends in the aetiology of CR-BSI are scarce [6] and usually refer to particular types of patients or specific types of catheters [17–22]. In our institution, Gram-positive agents continue to be the main cause of CR-BSI; however, a significant reduction in the incidence of S. aureus was observed during the study period. We believe that the infection control measures for MRSA introduced in 2004 may partially explain this evolution. In contrast, Enterococcus spp. seems to be an emerging cause of CR-BSI, and its incidence is increasing significantly [23].

A change in the epidemiology of central venous catheter-related bloodstream infections, with increasing prevalence of Gram-negative pathogens, has already been reported [6,21,24]. We found an increased incidence of Gram-negative CR-BSI in recent years in an unselected population in a large hospital.

The role of Candida spp. and other yeasts as a cause of CR-BSI is becoming more evident [25,26]. In our institution, the incidence of fungal CR-BSI more than doubled during the study period. Probably the increasing complexity of our patients could explain this, because neither a new haematology-oncology ward nor bone marrow transplantation unit was created, nor was a change of antibiotic recommendations introduced.

Our study is limited in that data were collected in a single institution and may not necessarily be extrapolated to other centres. The approach we applied would be impossible in institutions that do not perform catheter cultures and that only rely on DTTP. Regarding this issue, as we did not include the CR-BSI episodes that were only detected by DTTP, we missed 406 episodes from 2005 to 2010. Moreover, in hospitals with large cohorts of patients with long-term catheters, the infection rates per 1000 patients would be much higher than the BSI rates per 1000 catheter-days. Another limitation was that some variables associated with CLA-BSI, such as APACHE score and catheter site, were not controlled. Finally, using a patient denominator may not take account of changes in device-days, and this possibility would have to be monitored in units where both figures are available, such as ICUs. However, we believe that this potential drawback is outweighed by the benefit of having sequential figures of catheter infection in areas where catheter-days are neither routinely collected nor feasibly obtained on a regular basis.

In summary, our data suggest that the microbiology department can provide data on CR-BSI from blood culture and catheter tip records. These data can complement CLA-BSI reports from ICUs and provide a hospital-wide view of the problem. We detected a shift in the aetiological spectrum of CR-BSI, which may have implications for empirical therapeutic decisions.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Authors’ Contribution
  9. Transparency Declaration
  10. References
  11. Supporting Information

We thank Cristina Fernández for her help with the statistical analysis and Lawrence J. C. Baron for his help in the preparation of the manuscript.

Authors’ Contribution

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Authors’ Contribution
  9. Transparency Declaration
  10. References
  11. Supporting Information

EB and MRC contributed to the design of the study. MRC, PMR, EC and MG were responsible for data retrieval. MRC, EB and PM were responsible for data analysis. EB, MRC and PM were responsible for writing of the manuscript. All authors approved the final manuscript.

Transparency Declaration

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Authors’ Contribution
  9. Transparency Declaration
  10. References
  11. Supporting Information

The authors have no conflicts of interest to declare. No funding was received for this article.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Authors’ Contribution
  9. Transparency Declaration
  10. References
  11. Supporting Information
  • 1
    Marra AR, Cal RG, Durao MS et al. Impact of a program to prevent central line-associated bloodstream infection in the zero tolerance era. Am J Infect Control2010; 38: 434439.
  • 2
    Raad II. Commentary: zero tolerance for catheter-related bloodstream infections: the unnegotiable objective. Infect Control Hosp Epidemiol2008; 29: 951953.
  • 3
    Pronovost P, Needham D, Berenholtz S et al. An intervention to decrease catheter-related bloodstream infections in the ICU. N Engl J Med2006; 355: 27252732.
  • 4
    Mermel LA, Allon M, Bouza E et al. Clinical practice guidelines for the diagnosis and management of intravascular catheter-related infection: 2009 Update by the Infectious Diseases Society of America. Clin Infect Dis2009; 49: 145.
  • 5
    Teplick R. Caveats for comparing catheter-associated bloodstream infection rates. Crit Care Med2011; 39: 392394.
  • 6
    Marcos M, Soriano A, Inurrieta A et al. Changing epidemiology of central venous catheter-related bloodstream infections: increasing prevalence of Gram-negative pathogens. J Antimicrob Chemother2012; 66: 21192125.
  • 7
    Marschall J, Leone C, Jones M, Nihill D, Fraser VJ, Warren DK. Catheter-associated bloodstream infections in general medical patients outside the intensive care unit: a surveillance study. Infect Control Hosp Epidemiol2007; 28: 905909.
  • 8
    Zingg W, Sax H, Inan C et al. Hospital-wide surveillance of catheter-related bloodstream infection: from the expected to the unexpected. J Hosp Infect2009; 73: 4146.
  • 9
    Dudeck MA, Horan TC, Peterson KD et al. National Healthcare Safety Network (NHSN) Report, data summary for 2010, device-associated module. Am J Infect Control2011; 39: 798816.
  • 10
    Baron EJ, Weinstein MP, Dunne WM, Yagupsky P, Welch DF, Wilson DM. Blood cultures IV. Washington DC: American Society for Microbiology, 2005.
  • 11
    Maki DG, Weise CE, Sarafin HW. A semiquantitative culture method for identifying intravenous-catheter-related infection. N Engl J Med1977; 296: 13051309.
  • 12
    Pittet D, Tarara D, Wenzel RP. Nosocomial bloodstream infection in critically ill patients. Excess length of stay, extra costs, and attributable mortality. JAMA1994; 271: 15981601.
  • 13
    Warren DK, Quadir WW, Hollenbeak CS, Elward AM, Cox MJ, Fraser VJ. Attributable cost of catheter-associated bloodstream infections among intensive care patients in a nonteaching hospital. Crit Care Med2006; 34: 20842089.
  • 14
    Blot SI, Depuydt P, Annemans L et al. Clinical and economic outcomes in critically ill patients with nosocomial catheter-related bloodstream infections. Clin Infect Dis2005; 41: 15911598.
  • 15
    Mayer J, Greene T, Howell J et al. Agreement in classifying bloodstream infections among multiple reviewers conducting surveillance. Clin Infect Dis2012; 55: 364370.
  • 16
    Garner JS, Jarvis WR, Emori TG, Horan TC, Hughes JM. [CDC definitions for nosocomial infections 1988]. Z Arztl Fortbild (Jena) 1991; 85: 818827.
  • 17
    Gunst M, Matsushima K, Vanek S, Gunst R, Shafi S, Frankel H. Peripherally inserted central catheters may lower the incidence of catheter-related blood stream infections in patients in surgical intensive care units. Surg Infect (Larchmt)2011; 12: 279282.
  • 18
    Zingg W, Imhof A, Maggiorini M, Stocker R, Keller E, Ruef C. Impact of a prevention strategy targeting hand hygiene and catheter care on the incidence of catheter-related bloodstream infections. Crit Care Med2009; 37: 21672173; quiz 80.
  • 19
    Vandijck DM, Labeau SO, Brusselaers N, De Wandel D, Vogelaers DP, Blot SI. Impact of a prevention strategy targeting hand hygiene and catheter care on the incidence of catheter-related bloodstream infections. Crit Care Med2009; 37: 29982999; author reply 9.
  • 20
    Lorente L, Jimenez A, Roca I, Martin MM, Mora ML. Influence of tracheostomy on the incidence of catheter-related bloodstream infection in the catheterization of jugular vein by posterior access. Eur J Clin Microbiol Infect Dis2011; 30: 10491051.
  • 21
    Bouza E, San Juan R, Munoz P, Pascau J, Voss A, Desco M. A European perspective on intravascular catheter-related infections: report on the microbiology workload, aetiology and antimicrobial susceptibility (ESGNI-005 Study). Clin Microbiol Infect2004; 10: 838842.
  • 22
    Kim JT, Oh TY, Chang WH, Jeong YK. Clinical review and analysis of complications of totally implantable venous access devices for chemotherapy. Med Oncol2012; 29: 13611364.
  • 23
    Reigadas E, Rodríguez-Créixems M, Guembe M, Sánchez-Carrillo C, Martín-Rabadán P, Bouza E. Catheter-related bloodstream infection caused by Enterococcus spp.Clin Microbiol Infect2013; 19: 457461.
  • 24
    Munoz P, Bouza E, San Juan R, Voss A, Pascau J, Desco M. Clinical-epidemiological characteristics and outcome of patients with catheter-related bloodstream infections in Europe (ESGNI-006 Study). Clin Microbiol Infect2004; 10: 843845.
  • 25
    Nucci M, Anaissie E, Betts RF et al. Early removal of central venous catheter in patients with candidemia does not improve outcome: analysis of 842 patients from 2 randomized clinical trials. Clin Infect Dis2010; 51: 295303.
  • 26
    Raad I, Hanna H, Boktour M et al. Management of central venous catheters in patients with cancer and candidemia. Clin Infect Dis2004; 38: 11191127.

Supporting Information

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Authors’ Contribution
  9. Transparency Declaration
  10. References
  11. Supporting Information

Data S1. CRBSI/admissions vs. CRBSl/catheter days.

Data S2. CLABSI/admissions vs. CLABSI/catheter days.

FilenameFormatSizeDescription
clm12050_sm_dataS1.jpg47KSupporting info item
clm12050_sm_dataS2.jpg47KSupporting info item

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