Incidence Trends in Pathogen-Specific Central Line–Associated Bloodstream Infections in US Intensive Care Units, 1990–2010
Objective. To quantify historical trends in rates of central line–associated bloodstream infections (CLABSIs) in US intensive care units (ICUs) caused by major pathogen groups, including Candida spp., Enterococcus spp., specified gram-negative rods, and Staphylococcus aureus.
Design. Active surveillance in a cohort of participating ICUs through the Centers for Disease Control and Prevention, the National Nosocomial Infections Surveillance system during 1990–2004, and the National Healthcare Safety Network during 2006–2010.
Participants. Patients who were admitted to participating ICUs.
Results. The CLABSI incidence density rate for S. aureus decreased annually starting in 2002 and remained lower than for other pathogen groups. Since 2006, the annual decrease for S. aureus CLABSIs in nonpediatric ICU types was −18.3% (95% confidence interval [CI], −20.8% to −15.8%), whereas the incidence density rate for S. aureus among pediatric ICUs did not change. The annual decrease for all ICUs combined since 2006 was −17.8% (95% CI, −19.4% to −16.1%) for Enterococcus spp., −16.4% (95% CI, −18.2% to −14.7%) for gram-negative rods, and −13.5% (95% CI, −15.4% to −11.5%) for Candida spp.
Conclusions. Patterns of ICU CLABSI incidence density rates among major pathogen groups have changed considerably during recent decades. CLABSI incidence declined steeply since 2006, except for CLABSI due to S. aureus in pediatric ICUs. There is a need to better understand CLABSIs that still do occur, on the basis of microbiological and patient characteristics. New prevention approaches may be needed in addition to central line insertion and maintenance practices.
Central line–associated bloodstream infections (CLABSIs) are among the most common types of healthcare-associated infections (HAIs). A coordinated effort by state and federal agencies, professional societies, and healthcare personnel to implement proven best practices for the insertion of central lines has been associated with an approximately 60% decrease in overall CLABSI incidence rates in US intensive care units (ICUs) during the past decade.1-4 Additionally, population-based surveillance has shown that the incidence of hospital-onset, methicillin-resistant Staphylococcus aureus bloodstream infections decreased approximately 11% per year during 2005–2008.5 However, an estimated 18,000 CLABSIs still occur each year in US ICUs and contribute to poor patient outcomes and increased healthcare costs.1
The Centers for Disease Control and Prevention’s (CDC’s) National Healthcare Safety Network (NHSN) is used to track progress toward meeting federal, state, and facility-level HAI prevention goals. In 2009, the US Department of Health and Human Services announced its Action Plan to Prevent HAIs, which set goals for a 50% decrease in CLABSI incidence and 100% adherence to recommended central line insertion practices by 2013.6,7 Also, the Centers for Medicare and Medicaid Services (CMS) and more than half of all states now require public reporting of CLABSIs by healthcare facility; in most states and nationally, this reporting is being accomplished through use of NHSN. Facility-level CLABSI data reported to CMS via NHSN are now publicly available on the CMS Hospital Compare website. Mandated public reporting of CLABSI data is expected to accelerate progress toward CLABSI elimination.
Previous analyses of NHSN CLABSI surveillance data have tended to focus on overall CLABSI or S. aureus incidence density rates. Additional microbiological information is needed to help direct future CLABSI prevention efforts. A comparison of 2009 versus 2001 CLABSI surveillance data showed greater declines in the incidence of S. aureus CLABSIs than for other pathogen groups.1 This observation suggests that there have been differences in the recent success of CLABSI prevention, depending on the causative pathogen; better description and understanding of CLABSI rate trends could inform new approaches to prevention that may be needed to make an impact on preventing CLABSIs associated with specific pathogens. To further investigate this finding and better understand the historical context concerning the microbiology of CLABSIs in US ICUs, we analyzed 20 years of CDC CLABSI surveillance data to characterize pathogen-specific trends in CLABSI incidence density rates.
CLABSI Surveillance Systems and Reporting Environment
CLABSI data were reported by participating ICUs through the CDC’s National Nosocomial Infections Surveillance (NNIS) system during 1990–2004 and the NHSN during 2006–2010. Data are unavailable from 2005 because of a transition year between the systems. CLABSI reporting was mainly voluntary until several states implemented reporting mandates through NHSN starting in November 2006 and culminated in 21 states and the District of Columbia with CLABSI reporting mandates by October 2010 (C. Rebmann, personal communication, March 2012). Overall, 25 states had at least 1 ICU that participated in CLABSI surveillance in 1990, 41 in 2000, and 50 in 2010. All data included in this analysis were submitted before any CMS CLABSI reporting requirement as a condition of participation in the CMS Hospital Inpatient Quality Reporting Program. We analyzed data from 7 ICU types: cardiothoracic, coronary, medical, surgical, combined medical-surgical units in facilities with a major medical school teaching program affiliation, combined medical-surgical units in facilities without such an affiliation, and nonneonatal pediatric units.8
Definitions and Data Collection
NHSN data are maintained electronically at the CDC. For each month of surveillance, participating hospital units submit microbiologic and other information about all CLABSI events as well as the monthly total of patient-days and central line–days for that location.9 Detailed descriptions of NNIS and NHSN CLABSI surveillance methods and definitions are available.8,10,11 In brief, a CLABSI is a primary bloodstream infection in a patient who had a central line at the time of or within the 48 hours before the onset of the infection.11 For the recognized pathogens included in this analysis, a laboratory-confirmed bloodstream infection means that the pathogen must be cultured from 1 or more blood cultures, and the organism cultured from blood is not related to an infection at another site.11 NHSN CLABSI surveillance methodology distinguishes between recognized pathogens and common commensals (eg, coagulase-negative Staphylococci); because we limited our analysis to recognized pathogens, no correction was needed for a 2008 protocol change that applied only to common commensals.12 The most commonly isolated CLABSI pathogens were grouped into 4 categories: Candida species; S. aureus; Enterococcus species; and gram-negative rods, including Acinetobacter baumanii, Enterobacter species, Escherichia coli, Klebsiella oxytoca, Klebsiella pneumoniae, and Pseudomonas aeruginosa. CLABSIs with more than 1 pathogen could be reported in multiple pathogen categories. In subanalyses, additional pathogen-specific incidence rates were analyzed for Candida albicans, non-albicans Candida spp., Enterococcus faecalis, Enterococcus faecium, and 2 subgroups of gram-negative rods corresponding to Enterobacteriaceae (Enterobacter spp., E. coli, and Klebsiella spp.) or the common environmental organisms A. baumanii and P. aeruginosa.
For each pathogen category included in our study, we calculated the pooled mean CLABSI incidence density rate per 1,000 central line–days per year by ICU type. We also calculated the annual device utilization rate (total central line–days/total patient-days) to assess whether CLABSI trends were related to changes in central line usage.13 We used Poisson regression to model trends in pathogen-specific CLABSI incidence. The NNIS and NHSN periods were modeled separately to more accurately characterize CLABSI trends. The variables year, ICU type, and an interaction term for year and ICU type were included in the preliminary models for each pathogen category. ICU types were subsequently collapsed into mutually exclusive groups if preliminary analyses indicated a similar direction (increase, decrease, or no change) in the CLABSI trend; given a similar direction in trend, ICU types were separated into different groups only if their slope estimates differed at a higher level of statistical significance (). The final ICU groups for the NNIS period were medical-surgical ICUs (with or without major medical school affiliation) and non-medical-surgical ICUs (cardiothoracic, coronary, medical, pediatric, and surgical ICUs) for each pathogen category, except that all ICU types were combined for Enterococcus spp. For the NHSN period, all 7 ICU types were grouped together for each pathogen category, except that pediatric ICUs were analyzed separately from other ICU types for S. aureus.
To evaluate whether our findings could be explained by migration into or out of the surveillance network, a sensitivity analysis was conducted using data from NNIS continuous reporters, defined as ICUs that participated in CLABSI surveillance for at least 1 month in 14 or more of 15 NNIS surveillance years, and NHSN continuous reporters, which participated in CLABSI surveillance for at least 1 month during each of the 5 NHSN years. A participating ICU was defined as one that reported 50 or more central line–days in a given year.
Statistical analyses were performed using SAS (ver. 9.2; SAS Institute). P values are reported at a 2-sided significance level of . The (former) National Center for Preparedness, Detection, and Control of Infectious Diseases, CDC, conducted an ethical review and approved the routine reporting of HAI data to NNIS and NHSN, determining that such reporting constitutes surveillance and not research and therefore is not subject to institutional review board requirements. Our examination of temporal trends in these surveillance data is within the scope of routine surveillance activities and likewise is not subject to further institutional review.
Characteristics of Participating ICUs
The number of participating ICUs grew from 127 in 1990 to 3,474 in 2010, and 89% of that increase occurred after 2006, when some states started to mandate CLABSI reporting. Corresponding growth was observed in the number of facilities, ICU patient-days, and central line–days under surveillance. The overall device utilization rate was 0.51 central line–days per patient-days per year and did not vary considerably across the years (range, 0.49–0.53). When looking at the annual number of participating ICUs and total reported central line–days by ICU type, substantial growth in participation was observed for all ICU types (Table 1). However, the largest relative increase occurred for medical-surgical units without a major medical school affiliation, and the smallest relative increase occurred for surgical units.
|Cardiothoracic||Coronary||Medical||Without major teaching affiliation||With major teaching affiliation||Pediatric||Surgical|
|1990–1994 ()||28 (6)||73 (16)||81 (17)||96 (21)||53 (11)||46 (10)||88 (19)|
|1995–1999 ()||60 (8)||97 (13)||126 (17)||153 (20)||104 (14)||71 (9)||142 (19)|
|2000–2004 ()||59 (9)||80 (12)||116 (17)||136 (20)||114 (17)||64 (9)||122 (18)|
|2006–2010 ()||326 (9)||326 (9)||482 (13)||1,797 (47)||254 (7)||281 (7)||321 (8)|
|Central line–days × 103|
|1990–1994||117 (10)||87 (8)||185 (16)||192 (17)||114 (10)||102 (9)||354 (31)|
|1995–1999||328 (10)||203 (6)||545 (17)||666 (21)||459 (14)||233 (7)||745 (23)|
|2000–2004||388 (10)||235 (6)||631 (16)||942 (23)||805 (20)||312 (8)||746 (18)|
|2006–2010||1,669 (11)||1,142 (8)||2,318 (16)||5,407 (36)||1,571 (11)||1,085 (7)||1,715 (12)|
Pooled Mean CLABSI Incidence Density by Pathogen Category
The pooled mean CLABSI incidence density rate per 1,000 central line–days is shown by pathogen category (Figure 1). The 2010 pooled mean overall ICU CLABSI incidence density rate was 1.3 CLABSIs per 1,000 central line–days. When looking at the distribution of pathogens across time (Figure 1), S. aureus CLABSI incidence had no clear pattern during the majority of the NNIS period but decreased starting in 2002 and remained lower than other pathogen categories. The Candida spp. CLABSI incidence density rate was lower than other groups during much of the NNIS period but converged with gram-negative rod and Enterococcus spp. incidence during NHSN years. The Enterococcus spp. CLABSI incidence density rate increased from the lowest to highest incidence of the 4 categories by 2000 and remained so into 2010. The differences discussed between these pathogen groups are based on analysis of reported surveillance data and were not tested for statistical significance.
The unadjusted 2010 pathogen-specific incidence density rates for Candida spp., Enterococcus spp., gram-negative rods, and S. aureus were 0.25, 0.28, 0.26, and 0.14 CLABSIs per 1,000 central line–days, respectively. In 2010, 42% of Candida spp. CLABSIs were due to C. albicans and 59% to non-albicans Candida spp. Forty-five percent of Enterococcus spp. CLABSIs were due to E. faecalis, 44% to E. faecium, and 13% to other species. Thirty-six percent of gram-negative rod CLABSIs were associated with Klebsiella spp., 22% with P. aeruginosa, 20% with Enterobacter spp., 14% with E. coli, and 12% with A. baumanii.
Pathogen-Specific Trends in CLABSI Incidence Density Rates
For each pathogen and ICU group used in the final analysis, the modeled trend is shown with the reported annual CLABSI incidence density rates for the NNIS and NHSN surveillance periods (Figure 2). Table 2 displays the magnitude of the model-estimated annual percent changes for each pathogen group reflected in Figure 2.
|NNIS (1990–2004)||NHSN (2006–2010)|
|Pathogen-specific ICU grouping||All ICUs||Continuous reporters||All ICUs||Continuous reporters|
|Medical-surgical||−1.2 (−2.6 to 0.1)||3.8 (0.2 to 7.5)|
|Non-medical-surgical||−1.8 (−2.6 to −0.8)||−3.6 (−5.3 to −1.8)|
|Pediatric||−3.3 (−12.2 to 6.7)||−1.5 (−15.8 to 15.1)|
|Nonpediatric||−18.3 (−20.8 to −15.8)||−16.9 (−21.0 to −12.6)|
|Medical-surgical||−2.6 (−4.0 to −1.2)||4.5 (0.7 to 8.5)|
|Non-medical-surgical||0.3 (−0.7 to 1.3)||−0.9 (−2.7 to 0.9)|
|All ICU types||−13.5 (−15.4 to −11.5)||−10.8 (−14.1 to −7.4)|
|Medical-surgical||−4.6 (−5.9 to −3.2)||0.0 (−3.8 to 4.0)|
|Non-medical-surgical||−1.8 (−2.5 to −1.0)||−3.3 (−4.7 to −2.0)|
|All ICU types||−16.4 (−18.2 to −14.7)||−10.1 (−13.2 to −7.0)|
|All ICU types||3.6 (2.8 to 4.4)||4.6 (2.9 to 6.3)||−17.8 (−19.4 to −16.1)||−14.1 (−17.2 to −11.6)|
During the NNIS period, the S. aureus incidence density rate declined in non-medical-surgical ICUs, and Enterococcus spp. incidence increased for all ICU types. For Candida spp. and gram-negative rods, the slight decrease observed among medical-surgical ICUs was not confirmed by the sensitivity analysis among continuously reporting ICUs. In contrast, during the NHSN period, significant and substantial annual decreases were detected within all pathogen and ICU groups except for the S. aureus incidence density rate among pediatric ICUs, which did not change (Table 2). The sensitivity analysis confirmed these findings, although the decreases were somewhat smaller among continuously reporting ICUs than for all reporters. During the NHSN period, the declines were greatest for S. aureus (nonpediatric ICUs) and more modest for gram-negative rods and Candida spp.
Our results demonstrate that historical decreases in pathogen-specific CLABSI rates in US ICUs are largely attributable to steep annual declines that have occurred since 2006. Though overall declines were observed for the major pathogens in our analysis, the relative incidence of CLABSIs due to these pathogens has changed considerably during the past decade. The S. aureus CLABSI incidence density rate has fallen below those of Candida spp., Enterococcus spp., and gram-negative rods, with the exception that S. aureus CLABSI incidence in pediatric ICUs has not decreased. Furthermore, the incidence rates for these non–S. aureus pathogen groups have converged. These changes reflect an evolution in the success of CLABSI prevention measures.
The incidence density rate of CLABSIs caused by Candida spp., Enterococcus spp., and gram-negative rods has remained higher than for S. aureus since 2004. A likely explanation for this finding is that central line insertion practices may be less effective at preventing bloodstream infections caused by Candida spp., Enterococcus spp., and Enterobacteriaceae, because some of these infections occur as a result of contamination of the catheter at the hub or needleless connector, while others arise from the gastrointestinal tract through compromised mucosal barriers.14,15 It may be prudent to turn our attention to infections due to these other pathogen groups that may require different approaches to prevention, for example, optimizing central line maintenance practices.1,8 Changes in NHSN surveillance definitions to allow separate reporting of bloodstream infections likely related to mucosal barrier injury were implemented in January 2013.
The increase in enterococcal CLABSI rates during the late 1990s may reflect the increasing prevalence of vancomycin-resistant enterococci in ICUs during this period.16,17 The subsequent declines in enterococcal CLABSI rates could reflect the effects of targeted environmental decontamination, patient isolation, and improved availability of effective antimicrobial therapy in addition to central line insertion practices.18,19 Although Candida CLABSI incidence density rates were substantially lower than for S. aureus earlier in the study period, they have been higher than for S. aureus since 2004. The effect of central line–based CLABSI prevention strategies on the epidemiology of Candida CLABSIs deserves further study.
The lack of recent improvement in S. aureus CLABSI incidence density rates in pediatric ICUs stands in contrast to other ICU types. It has been reported elsewhere that the incidence of healthcare-associated, invasive methicillin-resistant S. aureus infections has declined in adults but not in children.20 The adoption of central line insertion and maintenance bundles reduces overall CLABSI rates by approximately 40%–60% in pediatric ICUs, but no pediatric study has reported the near elimination of CLABSIs that has been observed with similar interventions in some adult ICUs.21-23 Proposed reasons for this difference include host factors and longer catheter dwell times for pediatric ICU populations versus adults.24 Focused attention on daily maintenance and care of central lines may be required to effect major reductions in CLABSI rates in pediatric ICUs, where maximizing compliance with insertion practices alone is unlikely to significantly reduce CLABSIs.25
Reporting mandates have driven explosive growth in participation in NHSN CLABSI surveillance, especially by smaller, nonacademic hospitals. This growth will provide more representative national surveillance data while also posing challenges to the interpretation of long-term CLABSI and other HAI trends.
The microbiologic categories and ICU groups chosen for this analysis are not intended to be definitive concerning the use of CLABSI data to evaluate pathogen- or healthcare location–specific concerns. Microbiologic CLABSI data are collected at the species level and provide a powerful tool to provide insight into the etiology and preventability of CLABSI or other HAIs reported to NHSN. Likewise, the rapid growth in NHSN CLABSI reporting may support future analyses involving a broader range of ICU types (eg, burn units) as well as hospital wards and specialty care areas, including hematology/oncology units.
Our analysis has several limitations. First, in looking at historical trends, the interpretation of earlier findings is based on the relatively small number of participating ICUs. We thus cannot rule out that migration into or out of the system had a substantial impact on findings. Because of the length of the study period and the need to consider pathogen- and ICU-specific trends, we were unable to identify a substantial cohort of continuous reporters across the entire 20-year surveillance period. Second, though ICU type and medical school teaching affiliation may broadly represent certain patient characteristics, we could not account for patient morbidities or other factors that influence CLABSI risk and are likely to be highly variable across facilities. Thus, our findings may not necessarily reflect trends at the facility or regional level. Third, problems with interobserver reliability could impact the integrity of CLABSI surveillance data. Fourth, CLABSI reporting does not require users to indicate the source of the positive blood culture. Therefore, changes over time may reflect improvements in central line hub management, thereby reducing intraluminal catheter colonization and the likelihood that blood cultures drawn through central lines will be positive. Fifth, we were unable to assess the extent to which recent CLABSI public reporting mandates acted as a negative incentive for facilities to identify and report CLABSIs.
Though overall CLABSI incidence density rates continue to decline, there is a need to better understand CLABSIs that still do occur. Microbiological data submitted to NHSN, such as those presented here, help inform the interpretation of measures of prevention success. For some scenarios, new prevention approaches may be needed in addition to central line insertion and maintenance practices. Also, evaluation is ongoing concerning areas of the current CLABSI definition that may be overly sensitive concerning bloodstream infections that can be acquired through routes other than the central line. Finally, as more and more healthcare facilities achieve excellent compliance with guidelines around central line insertion and maintenance, greater attention may need to be given to healthcare-associated BSIs that are occurring as a result of other primary, non-device-associated HAIs.
We thank Philip Ricks, PhD, Centers for Disease Control and Prevention.
Potential conflicts of interest. All authors report no conflicts of interest relevant to this article. All authors submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest, and the conflicts that the editors consider relevant to this article are disclosed here.
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