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Antimicrobial‐Resistant Pathogens Associated With Healthcare‐Associated Infections: Annual Summary of Data Reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006–2007

Alicia I. Hidron , MD, Jonathan R. Edwards , MS, Jean Patel , PhD, Teresa C. Horan , MPH, Dawn M. Sievert , PhD, Daniel A. Pollock , MD, Scott K. Fridkin , MD, National Healthcare Safety Network Team and Participating National Healthcare Safety Network Facilities
Infection Control and Hospital Epidemiology
Vol. 29, No. 11 (November 2008), pp. 996-1011
DOI: 10.1086/591861
Stable URL: http://www.jstor.org/stable/10.1086/591861
Page Count: 16
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NHSN Annual Update

Antimicrobial‐Resistant Pathogens Associated With Healthcare‐Associated Infections: Annual Summary of Data Reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006–2007

Alicia I. Hidron, MD ;
Jonathan R. Edwards, MS ;
Jean Patel, PhD ;
Teresa C. Horan, MPH ;
Dawn M. Sievert, PhD ;
Daniel A. Pollock, MD ;
Scott K. Fridkin, MD ; for the
National Healthcare Safety Network Team and
Participating National Healthcare Safety Network Facilities
From the Department of Medicine, Division of Infectious Diseases, Emory University School of Medicine (A.I.H.), and the Centers for Disease Control and Prevention, Division of Healthcare Quality Promotion (J.R.E., J.P., T.C.H., D.M.S., D.A.P., S.K.F.), Atlanta, Georgia.
    Address reprint requests to Dawn M. Sievert, PhD, Surveillance Branch, Division of Healthcare Quality Promotion, Centers for Disease Control and Prevention, 1600 Clifton Road, NE Mailstop A‐24, Atlanta, GA 30333 ().

Objective. 

To describe the frequency of selected antimicrobial resistance patterns among pathogens causing device‐associated and procedure‐associated healthcare‐associated infections (HAIs) reported by hospitals in the National Healthcare Safety Network (NHSN).

Methods. 

Data are included on HAIs (ie, central line–associated bloodstream infections, catheter‐associated urinary tract infections, ventilator‐associated pneumonia, and surgical site infections) reported to the Patient Safety Component of the NHSN between January 2006 and October 2007. The results of antimicrobial susceptibility testing of up to 3 pathogenic isolates per HAI by a hospital were evaluated to define antimicrobial‐resistance in the pathogenic isolates. The pooled mean proportions of pathogenic isolates interpreted as resistant to selected antimicrobial agents were calculated by type of HAI and overall. The incidence rates of specific device‐associated infections were calculated for selected antimicrobial‐resistant pathogens according to type of patient care area; the variability in the reported rates is described.

Results. 

Overall, 463 hospitals reported 1 or more HAIs: 412 (89%) were general acute care hospitals, and 309 (67%) had 200–1,000 beds. There were 28,502 HAIs reported among 25,384 patients. The 10 most common pathogens (accounting for 84% of any HAIs) were coagulase‐negative staphylococci (15%), Staphylococcus aureus (15%), Enterococcus species (12%), Candida species (11%), Escherichia coli (10%), Pseudomonas aeruginosa (8%), Klebsiella pneumoniae (6%), Enterobacter species (5%), Acinetobacter baumannii (3%), and Klebsiella oxytoca (2%). The pooled mean proportion of pathogenic isolates resistant to antimicrobial agents varied significantly across types of HAI for some pathogen‐antimicrobial combinations. As many as 16% of all HAIs were associated with the following multidrug‐resistant pathogens: methicillin‐resistant S. aureus (8% of HAIs), vancomycin‐resistant Enterococcus faecium (4%), carbapenem‐resistant P. aeruginosa (2%), extended‐spectrum cephalosporin‐resistant K. pneumoniae (1%), extended‐spectrum cephalosporin‐resistant E. coli (0.5%), and carbapenem‐resistant A. baumannii, K. pneumoniae, K. oxytoca, and E. coli (0.5%). Nationwide, the majority of units reported no HAIs due to these antimicrobial‐resistant pathogens.

Antimicrobial‐resistant pathogens that cause healthcare‐associated infections (HAIs) pose an ongoing and increasing challenge to hospitals, both in the clinical treatment of patients and in the prevention of the cross‐transmission of these problematic pathogens.14 These pathogens include methicillin‐resistant Staphylococcus aureus (MRSA), vancomycin‐resistant Enterococcus species, extended‐spectrum β‐lactamase–producing Escherichia coli and Klebsiella species, and fluoroquinolone‐ or carbapenem‐resistant Enterobacteriaceae or Pseudomonas aeruginosa.59 Describing the magnitude of the problem with respect to these antimicrobial‐resistant pathogens is challenging, because the levels of antimicrobial resistance vary for different types of healthcare facilities and for different geographic areas, and some resistance phenotypes are difficult for laboratories to detect. However, the findings from such attempts may help the infection control and public health communities target problems and utilize resources more efficiently.

Background

The National Healthcare Safety Network (NHSN) began collecting voluntarily reported data in 2005 as a national surveillance system for patient and healthcare personnel safety; it is managed by the Division of Healthcare Quality Promotion at the Centers for Disease Control and Prevention. It integrates 3 former systems, the National Nosocomial Infections Surveillance (NNIS) system, the Dialysis Surveillance Network, and the National Surveillance System for Healthcare Workers, into a single system. In contrast to the NNIS system, the NHSN is designed to allow for surveillance of selected HAI data at locations other than intensive care units (ICUs), in hospitals and other types of healthcare facilities. Therefore, because of differences in the surveillance methodology of, and in the healthcare facilities reporting to, the NNIS system and the NHSN, the percentage of HAIs caused by antimicrobial‐resistant pathogens reported to each system may not be comparable. A summary of device‐associated infection rates reported to the NHSN has been published.10 The purpose of this report is to describe the scope and magnitude of select antimicrobial‐resistant pathogens among infections reported to the device‐ and procedure‐associated modules of the NHSN.

Methods

We analyzed data that hospitals reported from January 2006 through October 2007 to the device‐ and procedure‐associated modules of the Patient Safety Component of the NHSN.11 HAI data on postprocedure pneumonia were excluded from further analysis because they accounted for less than 1% of the infections reported during this time period.

NHSN Methodology

After completing NHSN training, healthcare facility personnel collect and report data on a monthly basis using standardized methods and definitions specific to the NHSN module(s) selected.11 At least 6 months of data per year compliant with at least 1 module must be submitted to maintain active status in the NHSN.

For the device‐associated module, patients in the selected patient care areas are monitored for 1–3 types of HAI: central line–associated bloodstream infection (CLABSI), catheter‐associated urinary tract infection (CAUTI), or ventilator‐associated pneumonia (VAP). Denominator data from the specific types of patient care areas are also collected. For the procedure‐associated module, patients undergoing the selected surgical procedures are monitored for the development of either surgical site infection (SSI) or postprocedure pneumonia, or both. Procedure‐specific denominator data are collected. HAIs are identified using standardized definitions that combine laboratory, clinical, and radiographic criteria, if applicable.11

Pathogens and Susceptibility Data

Microbiology data provided by the healthcare facility’s designated clinical microbiology laboratory are collected for each HAI identified. The methods used for organism identification and antimicrobial susceptibility testing may vary between laboratories in different facilities. Up to 3 organisms per HAI were reported. Laboratories were expected to use Clinical and Laboratory Standards Institute standards for antimicrobial susceptibility testing;12 data for each pathogenic isolate were reported to the NHSN using the following category interpretations: intermediate, resistant, susceptible, or not tested. In some cases, resistance was defined using data from a single antimicrobial test result (resistance to ceftazidime, amikacin, or cefepime in P. aeruginosa pathogenic isolates; resistance to oxacillin in S. aureus pathogenic isolates; and resistance to either vancomycin or ampicillin in Enterococcus pathogenic isolates). In other cases, because laboratories test different antimicrobial agents within a class of antibiotics, resistance was defined using data from at least one of several agents within the same antibiotic class. Specifically, we defined resistance as follows: for fluoroquinolone resistance among P. aeruginosa and E. coli pathogenic isolates, the organisms were resistant to either ciprofloxacin, levofloxacin, ofloxacin, or moxifloxacin; for piperacillin resistance among P. aeruginosa pathogenic isolates, the organisms were resistant to either piperacillin or piperacillin‐tazobactam; for carbapenem resistance among P. aeruginosa and Acinetobacter baumannii pathogenic isolates, the organisms were resistant to imipenem or meropenem; for carbapenem resistance among E. coli, Klebsiella pneumoniae, and Klebsiella oxytoca pathogenic isolates, the organisms were resistant to imipenem, meropenem, or ertapenem; and for extended‐spectrum cephalosporin resistance among E. coli, K. pneumoniae, K. oxytoca, and A. baumannii pathogenic isolates, the organisms were resistant to either ceftriaxone or ceftazidime. A subset of the organisms listed above were classified as multidrug resistant, including MRSA, vancomycin‐resistant Enterococcus, extended‐spectrum cephalosporin‐resistant K. pneumoniae and E. coli, and carbapenem‐resistant P. aeruginosa, A. baumannii, K. pneumoniae, K. oxytoca, and E. coli. This classification was based on the recognition that the mechanisms of resistance in these phenotypes confer resistance to multiple classes of antimicrobial agents.12 This list is not all‐inclusive but includes pathogens of epidemiologic concern.

Selection of Pathogen‐Antimicrobial Combinations of Concern

Pathogen‐antimicrobial combinations selected for evaluation in this report were chosen on the basis of their greater frequency, their higher degree of clinical importance, and consideration of emerging antimicrobial resistance. To describe the variability in the incidence rates of antimicrobial resistance among specific reporting patient care areas, 4 pathogen‐antimicrobial combinations were selected for each type of device‐associated HAI.

Statistical Analysis

Data were analyzed using SAS software, version 9.1 (SAS). For device‐associated infections, the total number of HAIs and their distribution by type of hospital, patient care area, and procedure were calculated. For procedure‐associated infection, the total number of pathogens and their distribution by type of HAI and surgical procedure were calculated. For each type of HAI, the percentage of pathogenic isolates resistant to antimicrobial agents (hereafter, the resistance percentage) was calculated for the pathogen‐antimicrobial combinations by pooling data from all NHSN hospitals for this time period (ie, the sum of pathogenic isolates that were found to be resistant divided by the sum of pathogenic isolates that were tested, multiplied by 100). If fewer than 30 isolates were tested for antimicrobial susceptibility overall, the data were considered of low accuracy and therefore not reported, consistent with Clinical and Laboratory Standards Institute recommendations.13 The resistance percentage is reported by type of HAI. Additionally, if the resistance percentage did not differ between the types of device‐associated infections for a specific pathogen‐antimicrobial combination, a pooled device‐associated resistance percentage was also reported. Differences in the resistance percentages were compared across types of HAI using the χ2 test for independence (ie, comparing the lowest and highest resistance percentages for device‐associated HAIs, and comparing the pooled device‐associated HAI resistance percentages and SSI resistance percentages).

Location‐specific incidence rates of HAI due to selected antimicrobial‐resistant pathogens were also calculated for MRSA (CLABSI and VAP), vancomycin‐resistant Enterococcus faecium (CLABSI and CAUTI), extended‐spectrum cephalosporin‐resistant K. pneumoniae (CLABSI, CAUTI, and VAP), carbapenem‐resistant A. baumannii (CLABSI, CAUTI, and VAP), and carbapenem‐resistant P. aeruginosa (CAUTI and VAP). For these rates, only locations reporting more than 50 device‐days were included in the calculations. Pooled mean incidence rates for specific patient care areas included data from all healthcare facilities reporting from those patient care areas. The range of incidence rates for a specific patient care area was reported only if more than 20 healthcare facilities reported data for that patient care area.

To estimate the effects of unique recognized antimicrobial resistance patterns reported from certain geographic areas, and state mandatory reporting requirements on data in the current pool, we attempted to determine the relative contribution of facilities from New York on the magnitude of resistance. This was done by comparing the pooled device‐associated HAI resistance percentage while including and excluding data from New York facilities. We focused on data from this state because all New York hospitals were mandated to use the NHSN for reporting HAI data beginning January 2007 and because recent reports have described carbapenemase‐producing Klebsiella species as a problem among some New York hospitals.14

Results

Distribution of Infections

From January 2006 through October 2007, a total of 28,502 HAIs were reported to the NHSN: 10,064 (35.3%) were cases of CLABSI, 8,579 (30.1%) were cases of CAUTI, 4,524 (15.9%) were cases of VAP, 5,291 (18.6%) were cases of SSI, and 44 (0.2%) were cases of postprocedure pneumonia (data not shown). The 463 hospitals that reported 1 or more HAIs to the NHSN during this time period were predominantly large (Table 1): 412 (89%) were general acute care hospitals, 309 (67%) had between 200 and 1,000 beds, and 151 (33%) had less than 200 beds. Hospitals from 42 states were involved in the reporting to the NHSN. Most of the HAIs reported (19,390 [68%] of 28,502) were from hospitals in the northeastern and southern United States, which comprised 73% of the total number of hospitals.

Table 1. 
Characteristics of Hospitals Reporting Antimicrobial‐Resistant Healthcare‐Associated Infections (HAIs) to the National Healthcare Safety Network, January 2006–October 2007
Characteristic No. (%) of hospitals reporting ⩾1 HAI
($n=463$ )
No. (%) of HAIs reported
($n=28,502$ )
Type of hosptial
 Children’s 16 (3.5) 1,060 (3.7)
 General 412 (89.0) 26,767 (93.9)
 Military 5 (1.1) 81 (0.3)
 Veterans Affairs 20 (4.3) 510 (1.8)
 Othera 10 (2.2) 84 (0.3)
Size of hospital
 ⩽200 beds 151 (32.6) 2,270 (8.0)
 200–500 beds 217 (46.9) 10,669 (37.4)
 500–1,000 beds 92 (19.9) 15,079 (52.9)
 ⩾1,000 beds 3 (0.7) 484 (1.7)

Most patients with HAI were adults; 21,576 (85%) of the 25,384 patients were older than 20 years of age. Patients 0–3 years of age were mainly diagnosed with CLABSI (which represented 78% of HAIs for that age group). The HAIs were reported from 1,428 unique locations representing 10 general types of patient care areas within the 463 NHSN hospitals. Most device‐associated HAIs were reported from ICUs: medical‐surgical ICUs (23%), medical ICUs (13%), surgical ICUs (12%), neonatal ICUs (11%), trauma ICUs (7%), cardiothoracic surgical ICUs (6%), medical cardiac ICUs (5%), pediatric ICUs (4%), neurosurgical ICUs (4%), and burn ICUs (3%). The remaining 12% of device‐associated HAIs were reported from specialty care areas (3%) and other inpatient non‐ICU areas (ie, medical‐surgical wards [5%] and other inpatient wards [4%]) (Table 2). The majority of procedure‐associated HAIs were identified on inpatient surgical wards (data not shown), and most were associated with 1 of 4 major procedure types: cardiac surgery (29%), abdominal surgery (26%), orthopedic surgery (18%), and neurosurgery (12%) (Table 3).

Table 2. 
Distribution of Device‐Associated Healthcare‐Associated Infections (HAIs) Reported to the National Healthcare Safety Network, January 2006–October 2007, Stratified by Type of Patient Care Area (PCA)
Type of PCA No. of units reporting
($n=1,040$ a)
No. (%) of HAIs
Overall CLABSI CAUTI VAP
Burn ICU 18 690 (3.0) 271 (2.7) 206 (2.4) 213 (4.7)
Medical cardiac ICU 84 1,135 (4.9) 429 (4.3) 548 (6.4) 158 (3.5)
Cardiothoracic surgical ICU 76 1,299 (5.6) 443 (4.4) 469 (5.5) 387 (8.6)
MICUb 116 2,961 (12.8) 1,204 (12.0) 1,252 (14.6) 505 (11.2)
Medical‐surgical ICU 268 5,260 (22.7) 1,918 (19.0) 2,208 (25.7) 1,134 (25.1)
Medical‐surgical ward 31 1,116 (4.8) 288 (2.9) 827 (9.6) 1 (0.02)
NICUc 127 2,421 (10.5) 2,076 (20.6) 0 (0.00) 345 (7.6)
Neurosurgical ICU 31 867 (3.7) 268 (2.7) 398 (4.6) 201 (4.4)
PICUd 65 958 (4.1) 621 (6.2) 197 (2.3) 140 (3.1)
SCAe 25 631 (2.7) 552 (5.5) 65 (0.8) 14 (0.3)
SICU 100 2,730 (11.8) 1,031 (10.2) 1,005 (11.7) 694 (15.3)
Trauma ICU 27 1,520 (6.6) 448 (4.4) 495 (5.8) 577 (12.8)
Inpatient wardf 37 900 (3.9) 312 (3.1) 579 (6.7) 9 (0.2)
Other location 35 679 (2.9) 203 (2.0) 330 (3.9) 146 (3.2)
 Total 23,167 (100) 10,064 (100) 8,579 (100) 4,524 (100)
Table 3. 
Distribution of Procedure‐Associated Healthcare‐Associated Infections (HAIs) Reported to the National Healthcare Safety Network, January 2006–October 2007, Stratified by Type of Surgery
Type of
surgery
No. of surgeries No. (%) of HAIs
Overall SSI PPP
Abdominala 1,389 1,390 (26.1) 1,377 (26.0) 13 (29.5)
Cardiacb 1,557 1557 (29.2) 1536 (29.0) 21 (47.7)
Neurologicalc 650 650 (12.2) 650 (12.3) 0 (0.0)
Ob/Gynd 335 335 (6.3) 335 (6.3) 0 (0.0)
Orthopedice 969 969 (18.2) 962 (18.2) 7 (15.9)
Transplantf 87 87 (1.6) 86 (1.6) 1 (2.3)
Vascularg 217 217 (4.1) 217 (4.1) 0 (0.0)
Other 130 130 (2.4) 128 (2.4) 2 (4.5)
 Total 5,335 (100) 5,291 (100) 44 (100)

Pathogen Distribution

From 28,502 cases of HAI, a total of 33,848 pathogenic isolates were recovered and reported: 29,448 (87%) were bacteria, and 4,400 (13%) were fungi (Table 4). Overall, 16.4% of infections were polymicrobial and varied slightly by type of HAI: 20% of cases of SSI were polymicrobial, 21% of cases of VAP, 11% of cases of CLABSI, and 8% of cases of CAUTI.

Table 4. 
Distribution and Rank Order of Selected Pathogens Associated With Cases of Healthcare‐Associated Infection (HAI) Reported to the National Healthcare Safety Network, January 2006–October 2007, by Type of HAI
Pathogen Overalla CLABSI CAUTI VAP SSI
No. (%) of pathogenic isolates Rank No. (%) of pathogenic isolates Rank No. (%) of pathogenic isolates Rank No. (%) of pathogenic isolates Rank No. (%) of pathogenic isolates Rank
CoNS 5,178 (15.3) 1 3,900 (34.1) 1 234 (2.5) 7 79 (1.3) 9 965 (13.7) 2
Staphylococcus aureus 4,913 (14.5) 2 1,127 (9.9) 4 208 (2.2) 8 1,456 (24.4) 1 2,108 (30.0) 1
Enterococcus species 3 2 3 10 3
E. faecalis 1,177 (3.5) 627 (5.5) 335 (3.6) 21 (0.4) 194 (2.8)
E. faecium 1,888 (5.6) 942 (8.2) 562 (6.0) 38 (0.6) 345 (4.9)
 NOS 1,028 (3.0) 265 (2.3) 496 (5.3) 18 (0.3) 249 (3.5)
Candida species 4 3 2 7 8
C. albicans 2,295 (6.8) 673 (5.9) 1,361 (14.5) 140 (2.4) 115 (1.6)
 Other Candida spp. or NOS 1,333 (3.9) 669 (5.9) 613 (6.5) 20 (0.3) 30 (0.4)
Escherichia coli 3,264 (9.6) 5 310 (2.7) 8 2,009 (21.4) 1 271 (4.6) 6 671 (9.6) 4
Pseudomonas aeruginosa 2,664 (7.9) 6 357 (3.1) 7 938 (10.0) 4 972 (16.3) 2 390 (5.6) 5
Klebsiella pneumoniae 1,956 (5.8) 7 563 (4.9) 5 722 (7.7) 5 446 (7.5) 5 213 (3.0) 7
Enterobacter species 1,624 (4.8) 8 443 (3.9) 6 384 (4.1) 6 498 (8.4) 3 293 (4.2) 6
Acinetobacter baumannii 902 (2.7) 9 252 (2.2) 9 109 (1.2) 9 498 (8.4) 3 42 (0.6) 9
Klebsiella oxytoca 359 (1.1) 10 99 (0.9) 10 85 (0.9) 10 128 (2.2) 8 47 (0.7) 9
Other 5,267 (15.6) 1,201 (10.5) 1,321 (14.1) 1,375 (23.1) 1,363 (19.4)
 Total 33,848 (100) 11,428 (100) 9,377 (100) 5,960 (100) 7,025 (100)

Overall, the majority of isolates (70%) were either coagulase‐negative staphylococci (15%), S. aureus (15%), Enterococcus species (12%), Candida species (11%), E. coli (10%), or P. aeruginosa (8%) (Table 4). The rank‐order distribution of the selected pathogens varied by type of HAI but did not vary significantly when stratified by patient care area or by criteria used to identify each HAI (except for cases of CLABSI, for which criterion 2 is specific for common skin contaminant; data not shown).11 For cases of SSI, the distribution of pathogens varied only slightly when stratified by type of SSI (superficial incisional, deep incisional, or organ space; data not shown) but varied signficantly when stratified by type of surgery (Table 5). Coagulase‐negative staphylococci and S. aureus were the most prevalent pathogens causing SSI for most types of surgery, but gram‐negative rods and enterococci were the more prevalent pathogens causing SSI following abdominal surgery. Enterococci were associated with approximately one‐third of cases of SSI following transplant surgery.

Table 5. 
Distribution of Selected Pathogens Associated With Cases of Surgical Site Infection Reported to the National Healthcare Safety Network, January 2006–October 2007, by Type of Surgery
Pathogen Total no. of pathogenic isolates No. (%) of pathogenic isolates, by type of surgerya
Abdominal
($n=1,376$ )
Cardiac
($n=1,536$ )
Neurological
($n=650$ )
Ob/Gyn
($n=335$ )
Orthopedic
($n=963$ )
Transplant
($n=86$ )
Vascular
($n=203$ )
Other
($n=142$ )
CoNS 965 135 (6.4) 423 (21.9) 123 (16.2) 59 (12.4) 173 (15.3) 8 (6.4) 24 (7.8) 20 (10.9)
Staphylococcus aureus 2,108 268 (12.7) 627 (32.5) 387 (50.9) 134 (28.3) 548 (48.6) 14 (11.2) 96 (31.3) 34 (18.5)
Enterococcus species
E. faecalis 345 165 (7.8) 52 (2.7) 9 (1.2) 30 (6.3) 57 (5.1) 13 (10.4) 8 (2.6) 11 (6.0)
E. faecium 194 121 (5.7) 17 (0.9) 1 (0.1) 4 (0.8) 13 (1.2) 25 (20.0) 3 (1.0) 10 (5.4)
 NOS 249 114 (5.4) 40 (2.1) 13 (1.7) 14 (3.0) 34 (3.0) 5 (4.0) 19 (6.2) 10 (5.4)
Candida species
C. albicans 115 58 (2.7) 27 (1.4) 3 (0.4) 2 (0.4) 2 (0.2) 9 (7.2) 4 (1.3) 10 (5.4)
 Other Candida spp. or NOS 30 9 (0.4) 10 (0.5) 0 (0.0) 0 (0.0) 2 (0.2) 4 (3.2) 3 (1.0) 2 (1.1)
Escherichia coli 671 395 (18.6) 116 (6.0) 28 (3.7) 45 (9.5) 34 (3.0) 11 (8.8) 26 (8.5) 16 (8.7)
Pseudomonas aeruginosa 390 129 (6.1) 136 (7.1) 32 (4.2) 15 (3.2) 38 (3.4) 3 (2.4) 27 (8.8) 10 (5.4)
Klebsiella pneumoniae 213 80 (3.8) 72 (3.7) 14 (1.8) 9 (1.9) 14 (1.2) 7 (5.6) 8 (2.6) 9 (4.9)
Enterobacter species 293 100 (4.7) 74 (3.8) 35 (4.6) 9 (1.9) 37 (3.3) 10 (8.0) 10 (3.3) 18 (9.8)
Acinetobacter baumannii 42 7 (0.3) 15 (0.8) 6 (0.8) 2 (0.4) 10 (0.9) 0 (0.0) 2 (0.7) 0 (0.0)
Klebsiella oxytoca 47 22 (1.0) 12 (0.6) 3 (0.4) 0 (0.0) 5 (0.4) 1 (0.8) 2 (0.7) 2 (1.1)
 Total no. of pathogenic isolatesb 7,025 2,118 1,929 760 474 1,128 125 307 184

Antimicrobial Resistance Percentages

Antimicrobial susceptibility testing data were received for most of the pathogenic isolates reported; the proportion of pathogenic isolates with test results varied by antimicrobial agent, pathogen, and type of HAI. The pathogen‐antimicrobial combinations with the highest proportion of test results were as follows: S. aureus tested against oxacillin (97%–99.5%); E. faecium and E. faecalis tested against vancomycin (98.4%–99.5% and 91.9%–98.4%, respectively); and P. aeruginosa and E. coli tested against fluoroquinolones (91%–97.9% and 93.2%–95.6%, respectively). The pathogen‐antimicrobial combinations with the lowest proportion of test results were associated with cases of CAUTI, specifically tested against carbapenems for K. pneumoniae (53.7%), K. oxytoca (44.7%), and E. coli (43.4%) (Tables 6 and 7). Pooled mean resistance percentages for the pathogen‐antimicrobial combinations are shown in Tables 6 and 7.

Table 6. 
Antimicrobial Resistance Percentages for Pathogenic Isolates ($n=26,765$ ) Associated With Cases of Device‐Associated Healthcare‐Associated Infection (HAI) Reported to the National Healthcare Safety Network, January 2006–October 2007
Pathogen,
antimicrobial
CLABSI CAUTI VAP Pooleda
No. of pathogenic isolates reported No. (%) of pathogenic isolates tested Resistance percentage, %b No. of pathogenic isolates reported No. (%) of pathogenic isolates tested Resistancepercentage, %b No. of pathogenic isolates reported No. (%) of pathogenic isolates tested Resistance percentage, %b No. of pathogenic isolates reported No. (%) of pathogenic isolates tested Resistance percentage, %b
Staphylococcus aureus 1,127 208 1,456 2,791
 OXA 1,103 (97.9) 56.8 207 (99.5) 65.2 1,426 (97.9) 54.4 2,736 (98.0) 56.2
Enterococcus species
 E. faecium 627 335 21 983
  VAN 617 (98.4) 78.9 331 (98.8) 81.0 NR NR 969 (98.6) 80.0
  AMP 547 (87.2) 90.5 278 (83.0) 89.9 NR NR 845 (86.0) 90.4
E. faecalis 942 562 38 1,542
  VAN 909 (96.5) 7.5 553 (98.4) 6.1 35 (92.1) 2.9 1,497 (97.1) 6.9
  AMP 813 (86.3) 4.2 481 (85.6) 3.1 34 (89.5) 2.9 1,328 (86.1) 3.8
 NOS 265 496
  VAN 219 (82.6) 37.0 401 (80.8) 18.0 18 NR NR
  AMP 172 (64.9) 40.7 267 (53.8) 21.3 NR NR
 All 1,834 1,393 77 3,304
  VAN 1,745 (95.1) 36.4 1,285 (92.2) 29.1 67 (87.0) 32.8 3,097 (93.7) 33.3
Pseudomonas aeruginosa 357 938 972 2,267
 FQs 325 (91.0) 30.5 918 (97.9) 33.8 942 (96.9) 27.8 2,185 (96.4) 30.7
 PIP or PTZ 242 (67.8) 20.2 609 (64.9) 17.1 694 (71.4) 17.0 1545 (68.2) 17.5
 AMK 234 (65.5) 4.3 580 (61.8) 7.9 630 (64.8) 4.9 1,444 (63.7) 6.0
 IMI or MERO 270 (75.6) 23.0 609 (64.9) 25.1 679 (69.9) 26.4 1,558 (68.7) 25.3
 TAZ 289 (81.0) 18.7 745 (79.4) 12.6 755 (77.7) 13.1
 CPM 247 (69.2) 12.6 639 (68.1) 10.8 718 (73.9) 11.1 1604 (70.8) 11.2
Klebsiella pneumoniae 563 722 446
 CTR or TAZ 483 (85.8) 27.1 579 (80.2) 21.2 329 (73.8) 23.7
 IMI, MERO, or ETP 452 (80.3) 10.8 388 (53.7) 10.1 302 (67.7) 3.6
Klebsiella oxytoca 99 85 128 312
 CTR or TAZ 82 (82.8) 15.9 68 (80.0) 17.6 82 (64.1) 17.1 232 (74.4) 16.8
 IMI, MERO, or ETP 63 (63.6) 0.0 38 (44.7) 2.6 80 (62.5) 5.0 181 (58.0) 2.8
Acinetobacter baumannii 252 109 498
 IMI or MERO 219 (86.9) 29.2 82 (75.2) 25.6 427 (85.7) 36.8
Escherichia coli 310 2,009 271
 CTR or TAZ 258 (83.2) 8.1 1,577 (78.5) 5.5 173 (63.8) 11.0
 IMI, MERO, or ETP 226 (72.9) 0.9 871 (43.4) 4.0 163 (60.1) 1.8
 FQs 289 (93.2) 30.8 1,920 (95.6) 24.8 255 (94.1) 22.7
Table 7. 
Antimicrobial Resistance Percentages for Pathogenic Isolates ($n=7,025$ ) Associated With Cases of Surgical Site Infection Reported to the National Healthcare Safety Network, January 2006–October 2007
Pathogen,
antimicrobial
No. of pathogenic isolates reported No. (%) of pathogenic isolates tested No. (%) of pathogenic isolates resistanta
Staphylococcus aureus 2,108
 OXA 2,045 (97.0) 1,006 (49.2)
Enterococcus species
E. faecium 194
  VAN 193 (99.5) 109 (56.5)
  AMP 169 (87.1) 120 (71.0)
E. faecalis 345
  VAN 317 (91.9) 15 (4.7)
  AMP 291 (84.3) 12 (4.1)
 NOS 249
  VAN 179 (71.9) 12 (6.7)
  AMP 175 (70.3) 19 (10.9)
 All 788
  VAN 689 (87.4) 136 (19.7)
Pseudomonas aeruginosa 390
 FQs 377 (96.7) 60 (15.9)
 PIP or PTZ 262 (74.9) 23 (7.9)
 AMK 196 (50.3) 4 (2.0)
 IMI or MERO 279 (71.5) 33 (11.8)
 TAZ 313 (80.3) 23 (7.3)
 CPM 261 (66.9) 15 (5.7)
Klebsiella pneumoniae 213
 CTR or TAZ 162 (76.1) 24 (14.8)
 IMI, MERO, or ETP 153 (71.8) 8 (5.2)
Klebsiella oxytoca 47
 CTR or TAZ 37 (78.7) 3 (8.1)
 IMI, MERO, or ETP NR NR
Acinetobacter baumannii 42
 IMI or MERO 36 (85.7) 11 (30.6)
Escherichia coli 671
 CTR or TAZ 489 (72.9) 26 (5.3)
 IMI, MERO, or ETP 439 (65.4) 11 (2.5)
 FQs 629 (93.7) 143 (22.7)

For 13 of 22 antimicrobial‐resistant phenotypes evaluated, the resistance percentage was comparable between all types of device‐associated HAIs, and an overall pooled device‐associated resistance percentage is presented (Table 6). However, there were some exceptions. Compared with cases of CAUTI, cases of CLABSI had a higher percentage of Enterococcus pathogenic isolates not otherwise specified that were resistant to vancomycin (18% vs 37%) and ampicillin (21.3% vs 40.7%), P. aeruginosa pathogenic isolates resistant to ceftazidime (12.6% vs 18.7%), and K. pneumoniae pathogenic isolates resistant to ceftriaxone or ceftazidime (21.2% vs 27.1%). Compared with cases of VAP, cases of CLABSI had a higher percentage of E. coli pathogenic isolates resistant to fluoroquinolones (22.7% vs 30.8%). Compared with cases of CLABSI and CAUTI, cases of VAP had a lower percentage of K. pneumoniae pathogenic isolates resistant to carbapenems (10.8% and 10.1% vs 3.6%). Compared with cases of CAUTI, cases of VAP had a higher percentage of A. baumannii pathogenic isolates resistant to carbapenems (25.6% vs 36.8%) and a higher percentage of E. coli pathogenic isolates resistant to ceftriaxone or ceftazidime (5.5% vs 11.0%). Compared with cases of CLABSI, cases of CAUTI had a higher percentage of E. coli pathogenic isolates resistant to carbapenems (0.9% vs 4.0%) (Table 6). The resistance percentages were lower for pathogenic isolates recovered from patients with SSI than for pathogenic isolates recovered from patients with device‐associated HAI, and these data are presented separately (Table 7).

When evaluating the relative contribution of the New York hospitals to the pooled data, we found that the pooled resistance percentage for pathogen‐antimicrobial combinations for all device‐associated HAIs combined remained unchanged when healthcare facilities reporting from New York were excluded, with the exception of carbapenem‐resistant K. pneumoniae pathogenic isolates, which changed from 8.7% to 5 % ($P< .001$ ). Because the exclusion of the New York hospitals did not affect the overall results reported, all of the tables include the data from New York.

Variability in the Incidence of HAIs With Select Antimicrobial‐Resistant Pathogens

The pooled mean rates of infection with antimicrobial‐resistant pathogens varied by type of patient care area for cases of CLABSI, CAUTI, and VAP, and these rates are reported separately (Tables 810). Data presented are limited to the more common antimicrobial‐resistant pathogens, including some of the multidrug‐resistant phenotypes; overall, the infection rate was very low. Also, in most cases, the majority of hospitals reported no antimicrobial‐resistant HAIs (ie, the median rate was zero). For example, the median rate of MRSA CLABSI and of MRSA VAP was zero in all types of patient care areas, with the exception of MRSA VAP in trauma ICU and medical ICU (Tables 8 and 10). However, differences in the pooled mean rates were clearly evident by type of patient care area. For example, the rate of MRSA CLABSI (calculated as cases per 1,000 device‐days) was low for inpatient medical‐surgical wards and was average for other ICUs (cardiac, medical, surgical, and trauma ICUs) and inpatient medical wards. The highest MRSA CLABSI rate was reported by burn ICUs (0.93 cases per 1,000 device‐days).

Table 8. 
Rates of Central Line–Associated Bloodstream Infection (CLABSI) Caused by Selected Antimicrobial‐Resistant Pathogens Reported to the National Healthcare Safety Network, January 2006–October 2007, by Type of Patient Care Area (PCA)
Pathogen, type of PCAa No. of units reporting No. of months reported No. of cases of infection No. of
device‐days
No. of infections per 1,000 device‐days Percentage of
units reporting
no resistant cases
Pooled mean Median 75th
percentile
90th
percentile
MRSA
 Burn ICU 19 259 32 34,546 0.93 NR NR NR 52.6
 Medical cardiac ICU 110 1,260 38 142,180 0.27 0.00 0.25 0.97 72.7
 Cardiothoracic surgical ICU 90 1,128 23 217,256 0.11 0.00 0.00 0.32 83.3
 MICU 134 1,622 72 365,378 0.20 0.00 0.24 0.55 69.4
 Medical‐surgical ICU
  Major teaching 100 1,266 50 258,460 0.19 0.00 0.30 0.52 64.0
  All others 296 2,928 63 491,709 0.13 0.00 0.00 0.40 83.8
 Neurosurgical ICU 36 405 9 55,473 0.16 0.00 0.00 0.45 83.3
 PICU 72 898 16 111,087 0.14 0.00 0.00 0.39 83.3
 SICU 118 1,579 65 311,761 0.21 0.00 0.27 0.59 70.3
 Trauma ICU 31 361 25 83,479 0.30 0.00 0.46 0.60 58.1
 Inpatient medical ward 29 289 13 46,349 0.28 0.00 0.17 1.05 72.4
 Inpatient medical‐surgical ward 57 543 19 105,972 0.18 0.00 0.00 0.94 75.4
Vanco‐res E. faecium
 Burn ICU 19 259 2 34,546 0.06 NR NR NR NR
 Medical cardiac ICU 110 1,260 26 142,180 0.18 0.00 0.00 0.70 84.5
 Cardiothoracic surgical ICU 90 1,128 14 217,256 0.06 0.00 0.00 0.23 85.6
 MICU 134 1,622 135 365,378 0.37 0.00 0.57 1.08 58.2
 Medical‐surgical ICU
  Major teaching 100 1,266 46 258,460 0.18 0.00 0.15 0.62 74.0
  All others 296 2,928 64 491,709 0.13 0.00 0.00 0.27 86.8
 Neurosurgical ICU 36 405 5 55,473 0.09 0.00 0.00 0.47 86.1
 PICU 72 898 16 111,087 0.14 0.00 0.00 0.41 81.9
 SICU 118 1,579 45 311,761 0.14 0.00 0.08 0.49 74.6
 Trauma ICU 31 361 12 83,479 0.14 0.00 0.18 0.40 71.0
 Inpatient medical ward 29 289 7 46,349 0.15 0.00 0.00 0.00 93.1
 Inpatient medical‐surgical ward 57 543 14 105,972 0.13 0.00 0.00 0.20 87.7
Carbp‐res A. baumannii
 Burn ICU 19 259 12 34,546 0.35 NR NR NR NR
 Medical cardiac ICU 110 1,260 1 142,180 0.01 0.00 0.00 0.00 99.1
 Cardiothoracic surgical ICU 90 1,128 0 217,256 0.00 0.00 0.00 0.00 100.0
 MICU 134 1,622 20 365,378 0.05 0.00 0.00 0.00 90.3
 Medical‐surgical ICU
  Major teaching 100 1,266 7 258,460 0.03 0.00 0.00 0.00 95.0
  All others 296 2,928 5 491,709 0.01 0.00 0.00 0.00 98.3
 Neurosurgical ICU 36 405 1 55,473 0.02 0.00 0.00 0.00 97.2
 PICU 72 898 1 111,087 0.01 0.00 0.00 0.00 98.6
 SICU 118 1,579 8 311,761 0.03 0.00 0.00 0.00 94.1
 Trauma ICU 31 361 1 83,479 0.01 0.00 0.00 0.00 96.8
 Inpatient medical ward 29 289 1 46,349 0.02 0.00 0.00 0.00 96.6
 Inpatient medical‐surgical ward 57 543 0 105,972 0.00 0.00 0.00 0.00 100.0
ES‐Ceph–res K. pneumoniaeb
 Burn ICU 19 259 9 34,546 0.26 NR NR NR NR
 Medical cardiac ICU 110 1,260 14 142,180 0.20 0.00 0.00 0.25 89.1
 Cardiothoracic surgical ICU 90 1,128 3 217,256 0.01 0.00 0.00 0.00 97.8
 MICU 134 1,622 31 365,378 0.08 0.00 0.00 0.32 84.3
 Medical‐surgical ICU
  Major teaching 100 1,266 11 258,460 0.04 0.00 0.00 0.00 91.0
  All others 296 2,928 17 491,709 0.03 0.00 0.00 0.00 96.3
 Neurosurgical ICU 36 405 4 55,473 0.07 0.00 0.00 0.34 88.9
 PICU 72 898 5 111,087 0.05 0.00 0.00 0.00 93.1
 SICU 118 1,579 14 311,761 0.04 0.00 0.00 0.00 92.4
 Trauma ICU 31 361 1 83,479 0.01 0.00 0.00 0.00 96.8
 Inpatient medical ward 29 289 3 46,349 0.06 0.00 0.00 0.00 93.1
 Inpatient medical‐surgical ward 57 543 2 105,972 0.02 0.00 0.00 0.00 96.5
Table 9. 
Rates of Catheter‐Associated Urinary Tract Infection (CAUTI) Caused by Selected Antimicrobial‐Resistant Pathogens Reported to the National Healthcare Safety Network, January 2006–October 2007, by Type of Patient Care Area (PCA)
Pathogen, type of PCAa No. of units reporting No. of months reported No. of cases of infection No. of
device‐days
No. of infections per 1,000 device‐days Percentage of
units reporting no resistant cases
Pooled mean Median 75th
percentile
90th
percentile
Vanco‐res E. faecium
 Burn ICU 14 171 3 22,977 0.13 NR NR NR NR
 Medical cardiac ICU 54 731 14 119,876 0.12 0.00 0.00 0.50 83.3
 Cardiothoracic surgical ICU 46 680 11 128,736 0.09 0.00 0.00 0.29 84.8
 MICU 66 955 68 285,497 0.24 0.00 0.37 0.76 59.1
 Medical‐surgical ICU
  Major Teaching 56 838 33 232,717 0.14 0.00 0.26 0.54 62.5
  All others 116 1,465 38 410,147 0.09 0.00 0.00 0.42 79.3
 Neurosurgical ICU 19 237 3 59,236 0.05 NR NR NR NR
 PICU 33 481 3 37,071 0.08 0.00 0.00 0.00 90.9
 SICU 63 971 35 244,704 0.14 0.00 0.20 0.45 68.3
 Trauma ICU 20 272 16 86,948 0.18 0.00 0.24 0.81 55.0
 Inpatient medical ward 17 169 14 31,189 0.45 NR NR NR NR
 Inpatient medical‐surgical ward 38 346 6 49,944 0.12 0.00 0.00 0.48 86.8
Carbp‐res P. aeruginosa
 Burn ICU 14 171 16 22,977 0.70 NR NR NR NR
 Medical cardiac ICU 54 731 6 119,876 0.05 0.00 0.00 0.00 92.6
 Cardiothoracic surgical ICU 46 680 11 128,736 0.09 0.00 0.00 0.28 78.3
 MICU 66 955 21 285,497 0.07 0.00 0.00 0.27 80.3
 Medical‐surgical ICU
  Major teaching 56 838 12 232,717 0.05 0.00 0.00 0.20 85.7
  All others 116 1,465 7 410,147 0.02 0.00 0.00 0.00 94.0
 Neurosurgical ICU 19 237 5 59,236 0.08 NR NR NR NR
 PICU 33 481 3 37,071 0.08 0.00 0.00 0.00 90.9
 SICU 63 971 25 244,704 0.10 0.00 0.00 0.22 76.2
 Trauma ICU 20 272 9 86,948 0.10 0.00 0.18 0.47 75.0
 Inpatient medical ward 17 169 3 31,189 0.10 NR NR NR NR
 Inpatient medical‐surgical ward 38 346 4 49,944 0.08 0.00 0.00 0.00 94.7
Carbp‐res A. baumannii
 Burn ICU 14 171 2 22,977 0.09 NR NR NR NR
 Medical cardiac ICU 54 731 0 119,876 0.00 0.00 0.00 0.00 100.0
 Cardiothoracic surgical ICU 46 680 1 128,736 0.01 0.00 0.00 0.00 97.8
 MICU 66 955 5 285,497 0.02 0.00 0.00 0.00 92.4
 Medical‐surgical ICU
  Major teaching 56 838 1 232,717 0.00 0.00 0.00 0.00 98.2
  All others 116 1,465 1 410,147 0.00 0.00 0.00 0.00 99.1
 Neurosurgical ICU 19 237 1 59,236 0.02 NR NR NR NR
 PICU 33 481 1 37,071 0.03 0.00 0.00 0.00 97.0
 SICU 63 971 2 244,704 0.01 0.00 0.00 0.00 96.8
 Trauma ICU 20 272 2 86,948 0.02 0.00 0.00 0.00 95.0
 Inpatient medical ward 17 169 0 31,189 0.00 NR NR NR NR
 Inpatient medical‐surgical ward 38 346 1 49,944 0.02 0.00 0.00 0.00 97.4
ES‐Ceph–res K. pneumoniaeb
 Burn ICU 14 171 7 22,977 0.30 NR NR NR NR
 Medical cardiac ICU 54 731 10 119,876 0.08 0.00 0.00 0.22 88.9
 Cardiothoracic surgical ICU 46 680 6 128,736 0.05 0.00 0.00 0.16 89.1
 MICU 66 955 29 285,497 0.10 0.00 0.00 0.55 75.8
 Medical‐surgical ICU
  Major teaching 56 838 12 232,717 0.05 0.00 0.00 0.16 87.5
  All others 116 1,465 13 410,147 0.03 0.00 0.00 0.00 93.1
 Neurosurgical ICU 19 237 3 59,236 0.05 NR NR NR NR
 PICU 33 481 1 37,071 0.03 0.00 0.00 0.00 97.0
 SICU 63 971 23 244,704 0.09 0.00 0.00 0.35 82.5
 Trauma ICU 20 272 0 86,948 0.00 0.00 0.00 0.00 100.0
 Inpatient medical ward 17 169 1 31,189 0.03 NR NR NR NR
 Inpatient medical‐surgical ward 38 346 0 49,944 0.00 0.00 0.00 0.00 100.0
Table 10. 
Rates of Ventilator‐Associated Pneumonia (VAP) Caused by Selected Antimicrobial‐Resistant Pathogens Reported to the National Healthcare Safety Network, January 2006–October 2007, by Type of Patient Care Area (PCA)
Pathogen, type of PCAa No. of units reporting No. of months reported No. of cases of infection No. of
device‐days
No. of infections per 1,000 device‐days Percentage of
units reporting
no resistant cases
Pooled mean Median 75th
percentile
90th
percentile
MRSA
 Burn ICU 16 208 52 18,683 0.56 NR NR NR NR
 Medical cardiac ICU 66 880 30 69,413 0.43 0.00 0.35 1.68 74.2
 Cardiothoracic surgical ICU 64 902 50 90,696 0.55 0.00 0.47 1.73 71.9
 MICU 84 1,160 106 209,885 0.51 0.10 0.71 1.57 48.8
 Medical‐surgical ICU
  Major teaching 72 975 92 155,178 0.59 0.00 0.97 2.01 52.8
  All others 149 1,928 125 264,805 0.47 0.00 0.59 1.67 61.7
 Neurosurgical ICU 25 287 36 33,468 1.08 0.00 1.10 2.90 60.0
 PICU 43 602 11 64,413 0.17 0.00 0.00 0.60 81.4
 SICU 81 1,163 112 148,455 0.75 0.00 0.68 1.51 55.6
 Trauma ICU 24 301 84 61,714 1.36 0.59 1.63 2.89 37.5
Carbp‐res P. aeruginosa
 Burn ICU 16 208 10 18,683 0.54 NR NR NR NR
 Medical cardiac ICU 66 880 9 69,413 0.13 0.00 0.00 0.00 92.4
 Cardiothoracic surgical ICU 64 902 4 90,696 0.04 0.00 0.00 0.00 93.8
 MICU 84 1,160 44 209,885 0.21 0.00 0.21 0.78 70.2
 Medical‐surgical ICU
  Major teaching 72 975 17 155,178 0.11 0.00 0.00 0.35 81.9
  All others 149 1,928 15 264,805 0.06 0.00 0.00 0.00 90.6
 Neurosurgical ICU 25 287 3 33,468 0.09 0.00 0.00 0.26 88.0
 PICU 43 602 1 64,413 0.02 0.00 0.00 0.00 97.7
 SICU 81 1,163 27 148,455 0.18 0.00 0.00 0.54 81.5
 Trauma ICU 24 301 9 61,714 0.15 0.00 0.08 0.37 75.0
Carbp‐res A. baumannii
 Burn ICU 16 208 33 18,683 1.77 NR NR NR NR
 Medical cardiac ICU 66 880 5 69,413 0.07 0.00 0.00 0.00 93.9
 Cardiothoracic surgical ICU 64 902 4 90,696 0.04 0.00 0.00 0.00 93.8
 MICU 84 1,160 20 209,885 0.10 0.00 0.00 0.55 84.5
 Medical‐surgical ICU
  Major teaching 72 975 21 155,178 0.14 0.00 0.00 0.50 81.9
  All others 149 1,928 8 264,805 0.03 0.00 0.00 0.00 95.3
 Neurosurgical ICU 25 287 3 33,468 0.09 0.00 0.00 0.00 92.0
 PICU 43 602 4 64,413 0.06 0.00 0.00 0.00 95.3
 SICU 81 1,163 24 148,455 0.16 0.00 0.00 0.70 84.0
 Trauma ICU 24 301 24 61,714 0.39 0.00 0.00 0.54 79.2
ES‐Ceph–res K. pneumoniaeb
 Burn ICU 16 208 1 18,683 0.05 NR NR NR NR
 Medical cardiac ICU 66 880 4 69,413 0.06 0.00 0.00 0.00 95.5
 Cardiothoracic surgical ICU 64 902 5 90,696 0.06 0.00 0.00 0.00 93.8
 MICU 84 1,160 18 209,885 0.09 0.00 0.00 0.43 84.5
 Medical‐surgical ICU
  Major teaching 72 975 16 155,178 0.10 0.00 0.00 0.16 86.1
  All others 149 1,928 10 264,805 0.04 0.00 0.00 0.00 96.6
 Neurosurgical ICU 25 287 0 33,468 0.00 0.00 0.00 0.00 100.0
 PICU 43 602 1 64,413 0.02 0.00 0.00 0.00 97.7
 SICU 81 1,163 13 148,455 0.09 0.00 0.00 0.26 87.7
 Trauma ICU 24 301 3 61,714 0.05 0.00 0.00 0.44 87.5

For antimicrobial‐resistant gram‐negative rods causing CLABSI, CAUTI, and VAP, in almost all types of patient care areas, approximately 80% of units or more reported no cases of carbapenem‐resistant A. baumannii or extended‐spectrum cephalosporin‐resistant K. pneumoniae (Tables 810). In all types of patient care areas, 70% of units or more reported no cases of carbapenem‐resistant P. aeruginosa CAUTI or VAP (Tables 9 and 10).

Discussion

This is the first antimicrobial resistance report from the NHSN. We found the pathogen distribution still closely parallels that of the NNIS reports from 1986 to 1999.15,16 The resistance percentages differ only slightly from the percentages found in historical data on ICU infections reported to the NNIS from 1986 to 2003.1518 Compared with the historical NNIS reports, this NHSN report found a slightly lower resistance percentage among device‐associated HAIs for MRSA (60% vs 56% of pathogenic isolates)17 and for extended‐spectrum cephalosporin‐resistant P. aeruginosa (32% vs 13%–19% of pathogenic isolates), but a slightly higher resistance percentage for vancomycin‐resistant Enterococcus (29% vs 33% of pathogenic isolates), extended‐spectrum cephalosporin‐resistant E. coli (6% vs 6%–11% of pathogenic isolates), extended‐spectrum cephalosporin‐resistant K. pneumoniae (21% vs 21%–27% of pathogenic isolates), and carbapenem‐resistant P. aeruginosa (21% vs 25% of pathogenic isolates).18 These current patterns seem to be similar to those found in national and international surveillance studies.1923

For device‐associated infections and SSIs, the most prevalent organisms overall were gram‐positive cocci (S. aureus, enterococci, and coagulase‐negative staphylococci, which were associated with 40% of infections) and Candida species. For cases of CLABSI, CAUTI, and VAP, the ranking of the 4 most common pathogens is almost identical to that of the NNIS report published in 1999.15 One notable exception is for VAP; A. baumannii now equals Enterobacter species, as the third most common pathogen. In contrast, the ranking of pathogens for ICU‐associated HAIs from European studies reveals a greater contribution from E. coli and Pseudomonas species and a less prominent contribution from Enterococcus species22,23 and, in some cases, Candida species.22 These differences may be explained by the use of different surveillance methods (the NHSN limits reports to device‐ and procedure‐associated infections based on specific criteria, whereas other institutions may use any positive clinical culture result, which may represent either colonization or infection) or perhaps by geographic differences.

Overall, compared with studies from other surveillance systems involving ICUs from European and North American countries (including the United States), our pooled mean resistance percentages are similar for MRSA and, in some instances, for P. aeruginosa, but are higher for most other pathogens.9,1925 For MRSA pathogenic isolates, resistance percentages as low as 20% have been reported from Canada21 and as high as 80% from southern European countries,23 but resistance percentages from ICUs in Europe and North America are comparable to ours (50%–60% of pathogenic isolates).19,20,23 For Enterococcus species, the percentages of resistance to vancomycin that we found are higher overall than those from Europe and North America (33% vs 13%–28% of pathogenic isolates),19,20,24,25 as are the percentages we found for vancomycin‐resistant E. faecium pathogenic isolates (80% vs 0.8% reported from France and 24% from Italy).21 For the P. aeruginosa pathogenic isolates tested, the pooled mean resistance percentages for most antimicrobials were comparable with those of other studies in general,9,1921,2326 except for Italy, where a higher percentage of resistance to ceftazidime, cefepime, piperacillin, and fluoroquinolone has been reported.21 However, the carbapenem resistance percentage was higher overall in this NHSN report.9,19,20,22,23

Among Enterobacteriaceae pathogenic isolates, resistance to fluoroquinolones, extended‐spectrum cephalosporins, and carbapenems was generally higher in our report, compared with other isolate‐based testing systems both inside and outside the United States.9,1922,24,25 Among these reports, the notable exceptions included the higher percentage of extended‐spectrum cephalosporin resistance among K. pneumoniae (29% of pathogenic isolates) and K. oxytoca (15% of pathogenic isolates) from Italy.21 Also of note, no carbapenem‐resistant K. oxytoca pathogenic isolates were reported from any of these studies, and, similarly, only one study9 reported any carbapenem‐resistant K. pneumoniae pathogenic isolates. Our observed resistance percentages for carbapenem‐resistant A. baumannii were also considerably higher than those from these other studies (33% vs 2%–21% of pathogenic isolates).9,19,21 The NHSN received reports of this antimicrobial‐resistant pathogen from 5%–25% of locations reporting cases of VAP, with higher percentages of reporting among burn and trauma ICUs (Table 10).

The high percentage of resistance to carbapenems observed among K. pneumoniae pathogenic isolates was of special concern. Previous laboratory‐based surveillance studies evaluating bloodstream infections in hospitalized patients did not identify any pathogenic isolates of carbapenem‐resistant Klebsiella species among a range of 161–765 pathogenic isolates.19,26,27 We observed a range of resistance percentages (ie, 4%–11% of pathogenic isolates) among the different types of HAI, with the highest resistance percentages observed for pathogenic isolates associated with CLABSI. The first reports of carbapenem resistance among Klebsiella species started to appear from New York hospitals around 2004.14 The resistance percentage for pathogenic isolates reported from New York hospitals was 21% and contributed to the percentages observed; however, when excluding the hospitals reporting from New York, the resistance percentage remained high (5% of pathogenic isolates), which suggests that this phenotype may be more widespread and more common than previously recognized (ie, the resistance percentage observed is not due solely to healthcare facilities reporting from a single geographic area).

Identification of some of these emerging resistance patterns should alert the infection control community to potential challenges they may face in coming years. However, although each of these described antimicrobial‐resistant phenotypes is of concern, the frequency with which each causes HAIs is relatively low, compared with all other pathogens. Among all cases of HAI reported, the following multidrug‐resistant pathogens accounted for approximately 16% of infections: MRSA, 8%; vancomycin‐resistant E. faecium, 4%; carbapenem‐resistant P. aeruginosa, 2%; extended‐spectrum cephalosporin‐resistant K. pneumoniae, 1%; extended‐spectrum cephalosporin‐resistant E. coli, less than 1%; and carbapenem‐resistant A. baumannii, K. pneumoniae, K. oxytoca, and E. coli, each less than 1%.

A novel metric included in this report is a device‐associated infection incidence density rate for selected antimicrobial‐resistant pathogens. Data were stratified by type of patient care area, because differences according to hospital location were evident. Further stratification (eg, by the number of beds in the hospital) may be possible as more data become available. The incidence density rate allows for assessment of the variability of antimicrobial resistance among device‐associated infections in different patient care areas, and may provide an additional way to assess the efficacy of infection control practices in the future. In general, antimicrobial‐resistant device‐associated infections due to gram‐positive pathogens was more widespread than infections due to gram‐negative pathogens. However, overall, less than 50% of units reporting to each of the types of patient care areas reported any device‐associated infection due to antimicrobial‐resistant pathogens, suggesting that these types of infections are not represented equally among all reporting hospitals. As the NHSN hospitals continue to report cases of HAI during the next several years, the tracking of this distribution of resistant pathogens is needed to assess the utility of this metric.

Direct comparisons of this resistance‐percentage data with the data reported in other studies and even with prior NNIS reports may not be informative for several reasons. First, the NHSN includes expansion to non‐ICU patient care areas and no minimum bed size criterion for inclusion of a hospital as a member, in contrast to the NNIS system. Second, this NHSN analysis limits reports to device‐ and procedure‐associated HAIs. Third, although the hospitals contributing data to the current report are similar to those that reported to the NNIS system (general, large, acute care hospitals),28 they include more varied types of hospitals and patient care areas. This report and previous NNIS reports have a limitation in common: the patient population may not be representative of the US patient population as a whole, even though hospitals from 42 states are represented.

Additional limitations of this report include the fact that antimicrobial susceptibility testing was performed by laboratories servicing the hospitals, not by a central laboratory of the Centers for Disease Control and Prevention. Also, a few errors were identified in the data. We looked at the frequency of highly unlikely phenotypes and found a number of reports that noted carbapenem resistance in conjunction with extended‐spectrum cephalosporin susceptibility among pathogenic isolates of K. pneumoniae and E. coli. These unlikely phenotypes were reported in only 0.46% of all K. pneumoniae pathogenic isolates, equivalent to 7.5% of the carbapenem‐resistant K. pneumoniae pathogenic isolates reported, but were reported in 1.13% of all E. coli pathogenic isolates, equivalent to 66.7% of the carbapenem‐resistant E. coli pathogenic isolates reported. These errors may be have been due to incorrect data entry and/or laboratory testing. In response to these findings, and to improve the reliability of the data entered into this system, an edit check will be incorporated, to warn if data on carbapenem resistance in conjunction with extended‐spectrum cephalosporin susceptibility are entered. Lastly, accounting for the impact of mandated reporting on this antimicrobial resistance report will be an ongoing challenge. By January 2007, there were 2 states that had required all hospitals to report data to the NHSN, and this number continues to increase. In summary, this first report describes the scope, magnitude, and variability of certain antimicrobial‐resistant pathogens associated with device‐ or procedure‐associated HAIs reported to the Patient Safety Component of the NHSN.

Acknowledgments

We thank the NHSN participants for their ongoing efforts to monitor infections and improve patient safety, and our colleagues in the Division of Healthcare Quality Promotion for their tireless support of this unique public health network.

Financial support. The NHSN surveillance system is supported by the Division of Healthcare Quality Promotion, Centers for Disease Control and Prevention.

Potential conflicts of interest. All authors report no conflicts of interest relevant to this article.

References

  1. 1. 
    Esposito S, Leone S. Antimicrobial treatment for intensive care unit (ICU) infections including the role of the infectious disease specialist. Int J Antimicrob Agents 2007; 29:494–500.
  2. 2. 
    Bradley JS, Guidos R, Baragona S, et al. Anti‐infective research and development—problems, challenges, and solutions. Lancet Infect Dis 2007; 7:68–78.
  3. 3. 
    Huang SS, Yokoe DS, Hinrichsen VL, et al. Impact of routine intensive care unit surveillance cultures and resultant barrier precautions on hospital‐wide methicillin‐resistant Staphylococcus aureus bacteremia. Clin Infect Dis 2006; 43:971–978.
  4. 4. 
    Schwaber MJ, Carmeli Y. Mortality and delay in effective therapy associated with extended‐spectrum β‐lactamase production in Enterobacteriaceae bacteremia: a systematic review and meta‐analysis. J Antimicrob Chemother 2007; 60:913–920.
  5. 5. 
    Chambers HF. Community‐associated MRSA—resistance and virulence converge. N Engl J Med 2005; 352:1485–1487.
  6. 6. 
    Deshpande LM, Fritsche TR, Moet GJ, Biedenbach DJ, Jones RN. Antimicrobial resistance and molecular epidemiology of vancomycin‐resistant enterococci from North America and Europe: a report from the SENTRY antimicrobial surveillance program. Diagn Microbiol Infect Dis 2007; 58:163–170.
  7. 7. 
    Lewis JS 2nd, Herrera M, Wickes B, Patterson JE, Jorgensen JH. First report of the emergence of CTX‐M‐type extended‐spectrum β‐lactamases (ESBLs) as the predominant ESBL isolated in a U.S. health care system. Antimicrob Agents Chemother 2007; 51:4015–4021.
  8. 8. 
    Moland ES, Hanson ND, Black JA, Hossain A, Song W, Thomson KS. Prevalence of newer β‐lactamases in gram‐negative clinical isolates collected in the United States from 2001 to 2002. J Clin Microbiol 2006; 44:3318–3324.
  9. 9. 
    Lockhart SR, Abramson MA, Beekmann SE, et al. Antimicrobial resistance among gram‐negative bacilli causing infections in intensive care unit patients in the United States between 1993 and 2004. J Clin Microbiol 2007; 45:3352–3359.
  10. 10. 
    Edwards JR, Peterson KD, Andrus ML, et al. National Healthcare Safety Network (NHSN) Report, data summary for 2006, issued June 2007. Am J Infect Control 2007; 35:290–301.
  11. 11. 
    CDC. The National Healthcare Safety Network (NHSN) Manual. Patient Safety Component Protocol. Division of Healthcare Quality Promotion. Available at: http://www.cdc.gov/ncidod/dhqp/pdf/nhsn/NHSN_Manual_PatientSafetyProtocol_CURRENT.pdf. Accessed December 12, 2007.
  12. 12. 
    CLSI. Performance standards for antimicrobial susceptibility testing: 16th informational supplement. CLSI document. Wayne, PA: CLSI, 2008:M100‐S18.
  13. 13. 
    CLSI. Analysis and presentation of cumulative antimicrobial susceptibility test data: approved guideline. 2nd ed. Wayne, PA: CLSI, 2006:M39‐A2.
  14. 14. 
    Bradford PA, Bratu S, Urban C, et al. Emergence of carbapenem‐resistant Klebsiella species possessing the class A carbapenem‐hydrolyzing KPC‐2 and inhibitor‐resistant TEM‐30 β‐lactamases in New York City. Clin Infect Dis 2004;39:55–60.
  15. 15. 
    CDC. National Nosocomial Infections Surveillance (NNIS) system report, data summary from January 1990–May 1999, issued June 1999. Am J Infect Control 1999; 27:520–532.
  16. 16. 
    CDC. National Nosocomial Infections Surveillance (NNIS) system report, data summary from October 1986‐April 1998, issued June 1998. Available at: http://www.cdc.gov/ncidod/dhqp/pdf/nnis/sar98net.PDF. Accessed at December 12, 2007.
  17. 17. 
    Klevens RM, Edwards JR, Tenover FC, McDonald LC, Horan T, Gaynes R; National Nosocomial Infections Surveillance System. Changes in the epidemiology of methicillin‐resistant Staphylococcus aureus in intensive care units in US hospitals, 1992–2003. Clin Infect Dis 2006; 42:389–391.
  18. 18. 
    National Nosocomial Infections Surveillance (NNIS) system report, data summary from January 1992 through June 2004, issued October 2004. Am J Infect Control 2004; 32:470–485.
  19. 19. 
    Streit JM, Jones RN, Sader HS, Fritsche TR. Assessment of pathogen occurrences and resistance profiles among infected patients in the intensive care unit: report from the SENTRY Antimicrobial Surveillance Program (North America, 2001). Int J Antimicrob Agents 2004; 24:111–118.
  20. 20. 
    Stephen JM, Jones RN. Assessment of pathogens and resistance (R) patterns among intensive care unit (ICU) patients in North America (NA): initial report from the SENTRY Antimicrobial Surveillance Program (2001). In: Programs and Abstracts of the 42nd Interscience Congress of Antimicrobial Agents and Chemotherapy American Society for Microbiology; September 27–30, 2002; San Diego, CA. Abstract C2‐297.
  21. 21. 
    Jones ME, Draghi DC, Thornsberry C, Karlowsky JA, Sahm DF, Wenzel RP. Emerging resistance among bacterial pathogens in the intensive care unit—a European and North American surveillance study (2000–2002). Ann Clin Microbiol Antimicrob 2004; 3:14.
  22. 22. 
    Fluit AC, Verhoef J, Schmitz FJ. Frequency of isolation and antimicrobial resistance of gram‐negative and gram‐positive bacteria from patients in intensive care units of 25 European university hospitals participating in the European arm of the SENTRY Antimicrobial Surveillance Program 1997–1998. Eur J Clin Microbiol Infect Dis 2001; 20:617–625.
  23. 23. 
    Vincent JL, Bihari DJ, Suter PM, et al. The prevalence of nosocomial infection in intensive care units in Europe. Results of the European Prevalence of Infection in Intensive Care (EPIC) Study. EPIC International Advisory Committee. JAMA 1995; 274:639–644.
  24. 24. 
    Fridkin SK, Steward CD, Edwards JR, et al. Surveillance of antimicrobial use and antimicrobial resistance in United States hospitals: project ICARE phase 2. Project Intensive Care Antimicrobial Resistance Epidemiology (ICARE) hospitals. Clin Infect Dis 1999; 29:245–252.
  25. 25. 
    Fridkin SK, Hill HA, Volkova NV, et al. Temporal changes in prevalence of antimicrobial resistance in 23 US hospitals. Emerg Infect Dis 2002; 8:697–701.
  26. 26. 
    Diekema DJ, Pfaller MA, Jones RN, et al. Survey of bloodstream infections due to gram‐negative bacilli: frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, and Latin America for the SENTRY Antimicrobial Surveillance Program, 1997. Clin Infect Dis 1999; 29:595–607.
  27. 27. 
    Diekema DJ, Pfaller MA, Jones RN, et al.; SENTRY Participants Group. Trends in antimicrobial susceptibility of bacterial pathogens isolated from patients with bloodstream infections in the USA, Canada and Latin America. Int J Antimicrob Agents 2000; 13:257–271.
  28. 28. 
    Richards C, Emori TG, Edwards J, Fridkin S, Tolson J, Gaynes R. Characteristics of hospitals and infection control professionals participating in the National Nosocomial Infections Surveillance System 1999. Am J Infect Control 2001; 29:400–403.

Acknowledgments

We thank the NHSN participants for their ongoing efforts to monitor infections and improve patient safety, and our colleagues in the Division of Healthcare Quality Promotion for their tireless support of this unique public health network.

Financial support. The NHSN surveillance system is supported by the Division of Healthcare Quality Promotion, Centers for Disease Control and Prevention.

Potential conflicts of interest. All authors report no conflicts of interest relevant to this article.

References

  1. 1. 
    Esposito S, Leone S. Antimicrobial treatment for intensive care unit (ICU) infections including the role of the infectious disease specialist. Int J Antimicrob Agents 2007; 29:494–500.
  2. 2. 
    Bradley JS, Guidos R, Baragona S, et al. Anti‐infective research and development—problems, challenges, and solutions. Lancet Infect Dis 2007; 7:68–78.
  3. 3. 
    Huang SS, Yokoe DS, Hinrichsen VL, et al. Impact of routine intensive care unit surveillance cultures and resultant barrier precautions on hospital‐wide methicillin‐resistant Staphylococcus aureus bacteremia. Clin Infect Dis 2006; 43:971–978.
  4. 4. 
    Schwaber MJ, Carmeli Y. Mortality and delay in effective therapy associated with extended‐spectrum β‐lactamase production in Enterobacteriaceae bacteremia: a systematic review and meta‐analysis. J Antimicrob Chemother 2007; 60:913–920.
  5. 5. 
    Chambers HF. Community‐associated MRSA—resistance and virulence converge. N Engl J Med 2005; 352:1485–1487.
  6. 6. 
    Deshpande LM, Fritsche TR, Moet GJ, Biedenbach DJ, Jones RN. Antimicrobial resistance and molecular epidemiology of vancomycin‐resistant enterococci from North America and Europe: a report from the SENTRY antimicrobial surveillance program. Diagn Microbiol Infect Dis 2007; 58:163–170.
  7. 7. 
    Lewis JS 2nd, Herrera M, Wickes B, Patterson JE, Jorgensen JH. First report of the emergence of CTX‐M‐type extended‐spectrum β‐lactamases (ESBLs) as the predominant ESBL isolated in a U.S. health care system. Antimicrob Agents Chemother 2007; 51:4015–4021.
  8. 8. 
    Moland ES, Hanson ND, Black JA, Hossain A, Song W, Thomson KS. Prevalence of newer β‐lactamases in gram‐negative clinical isolates collected in the United States from 2001 to 2002. J Clin Microbiol 2006; 44:3318–3324.
  9. 9. 
    Lockhart SR, Abramson MA, Beekmann SE, et al. Antimicrobial resistance among gram‐negative bacilli causing infections in intensive care unit patients in the United States between 1993 and 2004. J Clin Microbiol 2007; 45:3352–3359.
  10. 10. 
    Edwards JR, Peterson KD, Andrus ML, et al. National Healthcare Safety Network (NHSN) Report, data summary for 2006, issued June 2007. Am J Infect Control 2007; 35:290–301.
  11. 11. 
    CDC. The National Healthcare Safety Network (NHSN) Manual. Patient Safety Component Protocol. Division of Healthcare Quality Promotion. Available at: http://www.cdc.gov/ncidod/dhqp/pdf/nhsn/NHSN_Manual_PatientSafetyProtocol_CURRENT.pdf. Accessed December 12, 2007.
  12. 12. 
    CLSI. Performance standards for antimicrobial susceptibility testing: 16th informational supplement. CLSI document. Wayne, PA: CLSI, 2008:M100‐S18.
  13. 13. 
    CLSI. Analysis and presentation of cumulative antimicrobial susceptibility test data: approved guideline. 2nd ed. Wayne, PA: CLSI, 2006:M39‐A2.
  14. 14. 
    Bradford PA, Bratu S, Urban C, et al. Emergence of carbapenem‐resistant Klebsiella species possessing the class A carbapenem‐hydrolyzing KPC‐2 and inhibitor‐resistant TEM‐30 β‐lactamases in New York City. Clin Infect Dis 2004;39:55–60.
  15. 15. 
    CDC. National Nosocomial Infections Surveillance (NNIS) system report, data summary from January 1990–May 1999, issued June 1999. Am J Infect Control 1999; 27:520–532.
  16. 16. 
    CDC. National Nosocomial Infections Surveillance (NNIS) system report, data summary from October 1986‐April 1998, issued June 1998. Available at: http://www.cdc.gov/ncidod/dhqp/pdf/nnis/sar98net.PDF. Accessed at December 12, 2007.
  17. 17. 
    Klevens RM, Edwards JR, Tenover FC, McDonald LC, Horan T, Gaynes R; National Nosocomial Infections Surveillance System. Changes in the epidemiology of methicillin‐resistant Staphylococcus aureus in intensive care units in US hospitals, 1992–2003. Clin Infect Dis 2006; 42:389–391.
  18. 18. 
    National Nosocomial Infections Surveillance (NNIS) system report, data summary from January 1992 through June 2004, issued October 2004. Am J Infect Control 2004; 32:470–485.
  19. 19. 
    Streit JM, Jones RN, Sader HS, Fritsche TR. Assessment of pathogen occurrences and resistance profiles among infected patients in the intensive care unit: report from the SENTRY Antimicrobial Surveillance Program (North America, 2001). Int J Antimicrob Agents 2004; 24:111–118.
  20. 20. 
    Stephen JM, Jones RN. Assessment of pathogens and resistance (R) patterns among intensive care unit (ICU) patients in North America (NA): initial report from the SENTRY Antimicrobial Surveillance Program (2001). In: Programs and Abstracts of the 42nd Interscience Congress of Antimicrobial Agents and Chemotherapy American Society for Microbiology; September 27–30, 2002; San Diego, CA. Abstract C2‐297.
  21. 21. 
    Jones ME, Draghi DC, Thornsberry C, Karlowsky JA, Sahm DF, Wenzel RP. Emerging resistance among bacterial pathogens in the intensive care unit—a European and North American surveillance study (2000–2002). Ann Clin Microbiol Antimicrob 2004; 3:14.
  22. 22. 
    Fluit AC, Verhoef J, Schmitz FJ. Frequency of isolation and antimicrobial resistance of gram‐negative and gram‐positive bacteria from patients in intensive care units of 25 European university hospitals participating in the European arm of the SENTRY Antimicrobial Surveillance Program 1997–1998. Eur J Clin Microbiol Infect Dis 2001; 20:617–625.
  23. 23. 
    Vincent JL, Bihari DJ, Suter PM, et al. The prevalence of nosocomial infection in intensive care units in Europe. Results of the European Prevalence of Infection in Intensive Care (EPIC) Study. EPIC International Advisory Committee. JAMA 1995; 274:639–644.
  24. 24. 
    Fridkin SK, Steward CD, Edwards JR, et al. Surveillance of antimicrobial use and antimicrobial resistance in United States hospitals: project ICARE phase 2. Project Intensive Care Antimicrobial Resistance Epidemiology (ICARE) hospitals. Clin Infect Dis 1999; 29:245–252.
  25. 25. 
    Fridkin SK, Hill HA, Volkova NV, et al. Temporal changes in prevalence of antimicrobial resistance in 23 US hospitals. Emerg Infect Dis 2002; 8:697–701.
  26. 26. 
    Diekema DJ, Pfaller MA, Jones RN, et al. Survey of bloodstream infections due to gram‐negative bacilli: frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, and Latin America for the SENTRY Antimicrobial Surveillance Program, 1997. Clin Infect Dis 1999; 29:595–607.
  27. 27. 
    Diekema DJ, Pfaller MA, Jones RN, et al.; SENTRY Participants Group. Trends in antimicrobial susceptibility of bacterial pathogens isolated from patients with bloodstream infections in the USA, Canada and Latin America. Int J Antimicrob Agents 2000; 13:257–271.
  28. 28. 
    Richards C, Emori TG, Edwards J, Fridkin S, Tolson J, Gaynes R. Characteristics of hospitals and infection control professionals participating in the National Nosocomial Infections Surveillance System 1999. Am J Infect Control 2001; 29:400–403.