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Antimicrobial-Resistant Pathogens Associated with Healthcare-Associated Infections: Summary of Data Reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2009–2010

Dawn M. Sievert PhD, Philip Ricks PhD, Jonathan R. Edwards MS, Amy Schneider MPH, Jean Patel PhD, Arjun Srinivasan MD, Alex Kallen MD, Brandi Limbago PhD, Scott Fridkin MD and for the National Healthcare Safety Network (NHSN) Team and Participating NHSN Facilities
Infection Control and Hospital Epidemiology
Vol. 34, No. 1 (January 2013), pp. 1-14
DOI: 10.1086/668770
Stable URL: http://www.jstor.org/stable/10.1086/668770
Page Count: 14
Subjects: Health Sciences Public Health
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NHSN Update

Antimicrobial-Resistant Pathogens Associated with Healthcare-Associated Infections: Summary of Data Reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2009–2010

Dawn M. Sievert, PhD,1
Philip Ricks, PhD,1
Jonathan R. Edwards, MS,1
Amy Schneider, MPH,1
Jean Patel, PhD,1
Arjun Srinivasan, MD,1
Alex Kallen, MD,1
Brandi Limbago, PhD,1
Scott Fridkin, MD,1 and
for the National Healthcare Safety Network (NHSN) Team and Participating NHSN Facilities
1. Division of Healthcare Quality Promotion, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia
    Address correspondence to Scott Fridkin, MD, MS A-35, CDC, 1600 Clifton Road NE, Atlanta, GA 30333 ().

Objective. To describe antimicrobial resistance patterns for healthcare-associated infections (HAIs) reported to the National Healthcare Safety Network (NHSN) during 2009–2010.

Methods. Central line–associated bloodstream infections, catheter-associated urinary tract infections, ventilator-associated pneumonia, and surgical site infections were included. Pooled mean proportions of isolates interpreted as resistant (or, in some cases, nonsusceptible) to selected antimicrobial agents were calculated by type of HAI and compared to historical data.

Results. Overall, 2,039 hospitals reported 1 or more HAIs; 1,749 (86%) were general acute care hospitals, and 1,143 (56%) had fewer than 200 beds. There were 69,475 HAIs and 81,139 pathogens reported. Eight pathogen groups accounted for about 80% of reported pathogens: Staphylococcus aureus (16%), Enterococcus spp. (14%), Escherichia coli (12%), coagulase-negative staphylococci (11%), Candida spp. (9%), Klebsiella pneumoniae (and Klebsiella oxytoca; 8%), Pseudomonas aeruginosa (8%), and Enterobacter spp. (5%). The percentage of resistance was similar to that reported in the previous 2-year period, with a slight decrease in the percentage of S. aureus resistant to oxacillins (MRSA). Nearly 20% of pathogens reported from all HAIs were the following multidrug-resistant phenotypes: MRSA (8.5%); vancomycin-resistant Enterococcus (3%); extended-spectrum cephalosporin–resistant K. pneumoniae and K. oxytoca (2%), E. coli (2%), and Enterobacter spp. (2%); and carbapenem-resistant P. aeruginosa (2%), K. pneumoniae/oxytoca (<1%), E. coli (<1%), and Enterobacter spp. (<1%). Among facilities reporting HAIs with 1 of the above gram-negative bacteria, 20%–40% reported at least 1 with the resistant phenotype.

Conclusion. While the proportion of resistant isolates did not substantially change from that in the previous 2 years, multidrug-resistant gram-negative phenotypes were reported from a moderate proportion of facilities.

The National Healthcare Safety Network (NHSN) began collecting data in 2005 as a national voluntary reporting system for patient and healthcare personnel safety surveillance data, managed by the Centers for Disease Control and Prevention (CDC). It is designed to allow for surveillance of selected healthcare-associated infection (HAI) data in intensive care units, as well as other location types, in hospitals and other types of healthcare facilities. Reporting of pathogens and the antimicrobial susceptibility test results of pathogens associated with HAIs is critically important for understanding the scope and magnitude of emerging and established antimicrobial-resistant infections in the United States. Analysis of these data produces summary measures of the prevalence of antimicrobial resistance among select pathogens in different patient care settings. Such measures should help inform decisions involving infection prevention practice, antimicrobial development, and public policy regarding efforts to detect and prevent transmission of resistant strains and/or their resistance determinants, especially those with phenotypes having the fewest viable treatment options.

This report is the second summary report of NHSN data, and it summarizes the antimicrobial susceptibility data reported to NHSN for the 2-year period 2009–2010. This time period coincides with an increased use of NHSN by acute care state mandates and early adoption of the reporting rules for participation in Centers for Medicare and Medicaid Services (CMS) Prospective Payment System. This report builds on the methodology of the first report,1 with additional evaluation of some temporal changes and degree of spread among reporting facilities.

Methods

We analyzed data that hospitals reported for 2009–2010 to the Patient Safety Component of NHSN.2 Data included those reported for central line–associated bloodstream infections (CLABSIs), catheter-associated urinary tract infections (CAUTIs), ventilator-associated pneumonia (VAP), and surgical site infections (SSIs). These data were compared to data reported from HAIs occurring during 2007–2008. Postprocedure pneumonia (which accounts for <1% of all HAIs reported) was excluded. NHSN methodology has been reported elsewhere2 and is summarized in the first NHSN antimicrobial resistance report.1

Pathogen and antimicrobial susceptibility data reported to NHSN are provided by the facility’s designated clinical microbiology laboratory. Up to 3 organisms can be reported per HAI. There is a select group of pathogens and antimicrobials for which susceptibility test results must be reported if testing was performed and reported to the clinician. Laboratories are expected to use Clinical and Laboratory Standards Institute standards for antimicrobial susceptibility testing.3 Results for each pathogen were reported to NHSN using the category interpretations “susceptible” (S), “intermediate” (I), “resistant” (R), and “not tested.” Because laboratories may test different antimicrobial agents within a class, for some phenotypes, resistance was defined using data from at least 1 of several agents within the same antimicrobial class. To be defined as resistant to extended-spectrum cephalosporins, organisms were reported as I or R either to ceftazidime or cefepime (Pseudomonas aeruginosa) or to ceftazidime, cefepime, ceftriaxone, or cefotaxime (Enterobacteriaceae). Carbapenem resistance was defined for all organisms as a result of I or R to imipenem or meropenem. Fluoroquinolone resistance was defined as a result of I or R either to ciprofloxacin or levofloxacin (P. aeruginosa) or to ciprofloxacin, levofloxacin, or moxifloxacin (Escherichia coli). Aminoglycoside resistance in P. aeruginosa was defined as a result of I or R to gentamicin, amikacin, or tobramycin. Finally, for some of the pathogens, definitions of multidrug resistance were used that required a report of I or R for at least 1 of the agents within a class—thus establishing nonsusceptibility to the class—and nonsusceptibility to at least 3 of the specified classes. For Klebsiella pneumoniae, Klebsiella oxytoca, E. coli, Enterobacter spp., and P. aeruginosa, 5 classes were included: extended-spectrum cephalosporins, fluoroquinolones, aminoglycosides, carbapenems, and piperacillin or piperacillin/tazobactam. A sixth class, ampicillin/sulbactam, was included for Acinetobacter baumannii. These criteria approximated, as best as possible, interim standard definitions for defining multidrug resistance.4 For the purpose of this report, “Klebsiella spp.” refers to results for K. pneumoniae and K. oxytoca combined, with the exclusion of other species of Klebsiella, which were extremely rare.

Statistical analysis. Data were analyzed with SAS software, version 9.3 (SAS Institute). For reporting hospitals and all reported HAIs, absolute frequencies and distributions are described by hospital type, size, and region. Absolute frequencies and distributions of pathogens by location or procedure were calculated. For each HAI type, pooled mean percent resistance (ie, the pooled proportion of bacteria resistant to antimicrobial agents) was calculated for the pathogen–antimicrobial agent combinations by pooling data from all NHSN hospitals for the specified time period (sum of pathogens testing resistant, divided by the sum of pathogens tested for susceptibility, multiplied by 100). Pooled mean percent resistance is reported by HAI type. Differences in pooled percent resistance were compared across HAI types by means of the χ2 test for independence (lowest vs highest percent resistance for device-associated HAIs and device-associated HAI pooled percent resistance vs SSI percent resistance). Percent resistance was found to differ in most cases across the device-associated infections for a specific pathogen-antimicrobial combination; thus, device-associated pooled percent resistance values are not reported. Because of the historical association between higher prevalence of antimicrobial resistance and specimen collection from patients in critical care locations, the pathogen percent resistance was stratified by location. Differences in pooled percent resistance were compared by location (critical care locations vs non–critical care locations) with log-binomial regression analysis for CLABSI and CAUTI. Statistical significance was determined at a P value of .05.

To highlight significant changes in percent resistance reported for the 4 HAI types between the 2009–2010 and 2007–2008 reports, the pooled mean percent resistance was compared between the two time periods for each of the evaluated pathogen-antimicrobial combinations described above, separately by each of the HAI types. To evaluate changes in percent resistance over time for each of the selected pathogen-antimicrobial combinations by HAI type, log-binomial regression analysis was conducted to compare the pooled mean percent resistances from 2009–2010 and 2007–2008. Confidence intervals, overall change, and P values are presented to indicate any significant increase or decrease in a specific percent resistance between the 2 time periods. To provide a measure that reflects the degree of spread of these antimicrobial-resistant pathogens among the reported HAIs, we calculated the number and proportion of facilities, among those reporting at least 1 occurrence of a pathogen-HAI combination, that reported a phenotype resistant to a particular antimicrobial for that HAI.

Results

Distribution of Infections by Hospital or Location Types

From January 2009 through December 2010, 69,475 HAIs were reported to NHSN from 2,039 hospitals. The relative proportions of HAIs reported varied by hospital type, bed size category, and region of the United States (Table 1), where more infections were reported from regions or groupings with more facilities participating in surveillance. Of these infections, 40% were CLABSIs, 27% were CAUTIs, 10% were VAP, and 23% were SSIs. The distribution by category was similar for the 2 reporting periods (Tables 1, 2).

Table 1. 
Characteristics of Hospitals Reporting Healthcare-Associated Infections (HAIs) to the National Healthcare Safety Network, by Time Period, 2007–2010
No. (%) of hospitals reporting No. (%) of HAIs reported
Characteristic2007–2008 (n = 1,172)2009–2010 (n = 2,039)2007–2008 (n = 47,582)2009–2010 (n = 69,475)
Type of hospital
 Children’s33 (2.8)46 (2.3)1,559 (3.3)2,238 (3.2)
 General1,029 (87.8)1,749 (85.8)43,734 (91.9)61,364 (88.3)
 Military6 (0.5)16 (0.8)103 (0.2)425 (0.6)
 Veterans Affairs27 (2.3)22 (1.1)648 (1.4)431 (0.6)
 Long-term acute care33 (2.8)122 (6.0)755 (1.6)3,382 (4.9)
 Othera44 (3.8)84 (4.1)783 (1.6)1,635 (2.4)
Size of hospital, beds
 <200592 (50.5)1,143 (56.1)8,837 (18.6)16,375 (23.6)
 200–499450 (38.4)717 (35.2)19,310 (40.6)28,851 (41.5)
 500–999127 (10.8)174 (8.5)18,836 (39.6)23,442 (33.7)
 ≥1,0003 (0.3)5 (0.2)599 (1.3)807 (1.2)
Location typeb
 Non–critical care386 (29.0)956 (38.3)8,935 (24.3)18,667 (34.9)
 Critical care946 (71.0)1,538 (61.7)27,869 (75.7)34,789 (65.1)
Region
 Region 1c84 (7.2)123 (6.0)888 (1.9)2,704 (3.9)
 Region 2d209 (17.8)248 (12.2)8,833 (18.6)10,190 (14.7)
 Region 3e307 (26.2)371 (18.2)14,043 (29.5)18,603 (26.8)
 Region 4f184 (15.7)339 (16.6)10,010 (21.0)12,915 (18.6)
 Region 5g123 (10.5)265 (13.0)4,758 (10.0)7,686 (11.1)
 Region 6h47 (4.0)135 (6.6)1,602 (3.4)3,091 (4.4)
 Region 7i21 (1.8)55 (2.7)1,274 (2.7)1,648 (2.4)
 Region 8j55 (4.7)71 (3.5)925 (1.9)1,576 (2.3)
 Region 9k93 (7.9)333 (16.3)3,676 (7.7)8,427 (12.1)
 Region 10l49 (4.2)99 (4.9)1,573 (3.3)2,635 (3.8)
Table 2. 
Types of Healthcare-Associated Infections (HAIs) Reported to the National Healthcare Safety Network by HAI Type, by Time Period, 2007–2010
EventNo. (%) of events reported
2007–2008 (n = 47,582)
No. (%) of events reported
2009–2010 (n = 69,475)
CLABSI18,651 (39.2)27,766 (40.0)
CAUTI11,863 (24.9)19,058 (27.4)
VAP6,290 (13.2)6,632 (9.5)
SSI10,778 (22.7)16,019 (23.1)

Overall, 6,505 locations were represented in the surveillance data, including 12 different general categories of critical care location types and 11 different general categories of non–critical care location types (Table 3). Roughly 65% of the device-associated HAIs reported were from critical care locations (Table 1), including mostly medical-surgical combined units and medical, surgical, and neonatal units (Table 3). The other 35% of HAIs were reported from non–critical care locations (Table 1), including mostly inpatient adult medical wards, medical-surgical wards, and long-term acute care locations (Table 3). The majority of procedure-associated HAIs were identified on inpatient surgical wards (data not shown), and most were associated with 1 of the 3 most commonly tracked major procedure types: cardiac surgeries (22%), abdominal surgeries (23%), and orthopedic surgeries (41%), which in this report includes spinal fusion/refusion and laminectomy (Table 4).

Table 3. 
Distribution of Device-Associated Infections Reported to the National Healthcare Safety Network, by Type of Location, 2009–2010
No. (%) of HAIs
LocationNo. of units reporting (n = 6,505)OverallCLABSICAUTIVAP
Critical care
 Burn42792 (1.5)389 (1.4)216 (1.1)187 (2.8)
 Cardiothoracic surgical2512,242 (4.2)1,098 (4.0)703 (3.7)441 (6.7)
 Medical3584,660 (8.7)2,403 (8.7)1,572 (8.2)685 (10.3)
 Medical cardiac2572,106 (3.9)1,086 (3.9)772 (4.1)248 (3.7)
 Medical-surgical1,32911,023 (20.6)5,796 (20.9)3,523 (18.5)1,704 (25.7)
 Neonatal3773,294 (6.2)2,902 (10.5)392 (5.9)
 Neurologic24393 (0.7)98 (0.4)185 (1.0)110 (1.7)
 Neurosurgical921,529 (2.9)418 (1.5)837 (4.4)274 (4.1)
 Pediatrica2032,025 (3.8)1,431 (5.2)342 (1.8)252 (3.8)
 Respiratory976 (0.1)34 (0.1)35 (0.2)7 (0.1)
 Surgical2513,776 (7.1)1,486 (5.4)1,271 (6.7)1,019 (15.4)
 Trauma962,873 (5.4)836 (3.0)963 (5.1)1,074 (16.2)
Non–critical care
 Bone marrow transplantb55939 (1.8)909 (3.3)29 (0.2)1 (0.0)
 Hematology/oncologyc1441,584 (3.0)1,364 (4.9)218 (1.1)2 (0.0)
 Inpatient acute dialysisd35 (0.0)5 (0.0)
 Long-term acute caree1673,554 (6.6)1,778 (6.4)1,630 (8.6)146 (2.2)
 Solid-organ transplantf15178 (0.3)135 (0.5)42 (0.2)1 (0.0)
 Long-term careg22135 (0.3)44 (0.2)91 (0.5)
 Inpatient adult wardsh1,2715,398 (10.1)2,297 (8.3)3,074 (16.1)27 (0.4)
 Inpatient pediatric wardsi109421 (0.8)360 (1.3)60 (0.3)1 (0.0)
 Medical-surgical ward1,0994,647 (8.7)2,074 (7.5)2,561 (13.4)12 (0.2)
 Mixed acuityj1316 (0.0)9 (0.0)6 (0.0)1 (0.0)
 Step-down unitsk3181,790 (3.3)814 (2.9)928 (4.9)48 (0.7)
Total6,50553,456 (100)27,766 (100)19,058 (100)6,632 (100)
Table 4. 
Distribution of Procedure-Associated Infections Reported to the National Healthcare Safety Network, by Type of Surgery, 2009–2010
Type of surgeryNo. (%) of SSIs
Orthopedica6,486 (40.5)
Abdominalb3,598 (22.5)
Cardiacc3,508 (21.9)
Ob/gynd1,543 (9.6)
Neurologicale386 (2.4)
Vascularf245 (1.5)
Transplantg160 (1.0)
Breasth64 (0.4)
Necki14 (0.1)
Otherj15 (0.1)
Total16,019 (100)

Pathogen Distribution

Overall, 81,139 pathogens were reported from the 69,475 HAIs; overall, 90% were bacteria and 10% were fungi (Table 5). Roughly 82% of pathogens were from 1 of 8 main pathogen groups: Staphylococcus aureus (15.6%), Enterococcus spp. (13.9%), E. coli (11.5%), Coagulase-negative staphylococci (11.4%), Candida spp. (9.5%), Klebsiella spp. (8%), P. aeruginosa (7.5%), or Enterobacter spp. (4.7%); other common pathogens included Proteus spp. (2.5%), Serratia spp. (2.1%), and A. baumannii (1.8%). The remaining (roughly 12%) of reported pathogens included a very wide variety of organisms (an additional table can be found at the CDC website, http://www.cdc.gov/nhsn/dataStat.html). For the 21,100 pathogens reported among SSIs, the pathogen distribution varied by type of surgery (Table 6). Coagulase-negative staphylococci and S. aureus were the most prevalent SSI pathogens for most types of surgery, but gram-negative rods were more prevalent in abdominal surgeries. Enterococci were associated with approximately one-third of SSIs following transplant surgery.

Table 5. 
Distribution of Rank Order of Selected Pathogens Associated with Healthcare-Associated Infections (HAIs) Reported to the National Healthcare Safety Network, by Type of HAI, 2009–2010
OverallCLABSICAUTIVAPSSI
PathogenNo. (%) of pathogensRankNo. (%) of pathogensRankaNo. (%) of pathogensRankaNo. (%) of pathogensRankaNo. (%) of pathogensRanka
Staphylococcus aureus12,635 (15.6)13,735 (12.3)2442 (2.1)2,043 (24.1)16,415 (30.4)1
Escherichia coli9,351 (11.5)21,206 (4.0)95,660 (26.8)1504 (5.9)61,981 (9.4)3
Coagulase-negative staphylococci9,261 (11.4)36,245 (20.5)1467 (2.2)72 (0.9)2,477 (11.7)2
Klebsiella (pneumoniae/oxytoca)6,470 (8.0)42,407 (7.9)52,365 (11.2)3854 (10.1)3844 (4.0)7
Pseudomonas aeruginosa6,111 (7.5)51,166 (3.8)102,381 (11.3)21,408 (16.6)21,156 (5.5)5
Enterococcus faecalis5,484 (6.8)62,680 (8.8)31,519 (7.2)545 (0.5)1,240 (5.9)4
Candida albicans4,275 (5.3)71,974 (6.5)71,887 (8.9)4147 (1.7)267 (1.3)
Enterobacter spp.3,821 (4.7)81,365 (4.5)8880 (4.2)8727 (8.6)4849 (4.0)6
Other Candida spp. or NOS3,408 (4.2)92,465 (8.1)4811 (3.8)936 (0.4)96 (0.5)
Enterococcus faecium3,314 (4.1)102,118 (7.0)6654 (3.1)1025 (0.3)517 (2.5)
Enterococcus spp.2,409 (3.0)11703 (2.3)121,010 (4.8)711 (0.1)685 (3.2)8
Proteus spp.2,031 (2.5)12232 (0.8)1,013 (4.8)6119 (1.4)667 (3.2)9
Serratia spp.1,737 (2.1)13762 (2.5)11204 (1.0)386 (4.6)7385 (1.8)
Acinetobacter baumannii1,490 (1.8)14629 (2.1)13185 (0.9)557 (6.6)5119 (0.6)
Othera9,304 (11.5)2,762 (9.1)1,633 (7.7)1,510 (17.8)3,399 (16.1)
Total81,139 (100)30,454 (100)21,111 (100)8,474 (100)21,100 (100)
Table 6. 
Distribution of Selected Pathogens Associated with Surgical Site Infections Reported to the National Healthcare Safety Network, by Type of Surgery, 2009–2010
No. (%) of pathogens, by type of surgerya
PathogenOverall, nAbdominal (n = 5,617)Breast (n = 83)Cardiac (n = 4,453)Neck (n = 20)Neurological (n = 433)Ob/gyn (n = 2,124)Orthopedic (n = 7,765)Transplant (n = 250)Vascular (n = 333)Other (n = 22)
Staphylococcus aureus6,415648 (11.5)31 (37.3)1,368 (30.7)3 (15.0)160 (37.0)418 (19.7)3,656 (47.1)17 (6.8)109 (32.7)5 (22.7)
Escherichia coli1,9811,043 (18.6)3 (3.6)283 (6.4)12 (2.8)274 (12.9)314 (4.0)24 (9.6)25 (7.5)3 (13.6)
Coagulase-negative staphylococci2,477288 (5.1)16 (19.3)743 (16.7)1 (5.0)99 (22.9)189 (8.9)1,073 (13.8)39 (15.6)27 (8.1)2 (9.1)
Klebsiella (pneumoniae/oxytoca)844305 (5.4)4 (4.8)261 (5.9)3 (15.0)15 (3.5)63 (3.0)159 (2.0)18 (7.2)15 (4.5)1 (4.5)
Pseudomonas aeruginosa1,156316 (5.6)7 (8.4)350 (7.9)2 (10.0)14 (3.2)83 (3.9)341 (4.4)16 (6.4)26 (7.8)1 (4.5)
Enterococcus faecalis1,240524 (9.3)1 (1.2)136 (3.1)2 (10.0)15 (3.5)176 (8.3)354 (4.6)16 (6.4)15 (4.5)1 (4.5)
Candida albicans267153 (2.7)1 (1.2)59 (1.3)7 (1.6)16 (0.8)22 (0.3)8 (3.2)1 (0.3)
Enterobacter spp.849254 (4.5)5 (6.0)228 (5.1)1 (5.0)31 (7.2)58 (2.7)238 (3.1)13 (5.2)20 (6.0)1 (4.5)
Other Candida spp. or NOS9648 (0.9)20 (0.4)2 (0.5)4 (0.2)14 (0.2)6 (2.4)1 (0.3)1 (4.5)
Enterococcus faecium517313 (5.6)51 (1.1)5 (1.2)26 (1.2)76 (1.0)38 (15.2)8 (2.4)
Enterococcus spp.685334 (5.9)4 (4.8)76 (1.7)1 (5.0)2 (0.5)87 (4.1)154 (2.0)13 (5.2)11 (3.3)3 (13.6)
Acinetobacter baumannii11916 (0.3)36 (0.8)6 (1.4)8 (0.4)51 (0.7)1 (0.3)1 (4.5)
Streptococcus spp.1,028305 (5.4)1 (1.2)93 (2.1)1 (5.0)12 (2.8)162 (7.6)433 (5.6)9 (3.6)11 (3.3)1 (4.5)
Proteus spp.667135 (2.4)5 (6.0)190 (4.3)4 (0.9)86 (4.0)231 (3.0)4 (1.6)12 (3.6)
Serratia spp.38526 (0.5)1 (1.2)216 (4.9)1 (5.0)9 (2.1)21 (1.0)98 (1.3)3 (1.2)10 (3.0)
Otherb2,374909 (16.2)4 (4.8)343 (7.7)5 (35.0)40 (9.2)453 (21.3)551 (7.1)26 (10.4)41 (12.3)2 (9.1)
Total21,1005,617 (100)83 (100)4,453 (100)20 (100)433 (100)2,124 (100)7,765 (100)250 (100)333 (100)22 (100)

Percent Resistance

Antimicrobial susceptibility testing data were received on most pathogens reported, although the percentage of pathogens with testing data varied by specific agent, pathogen, and HAI type. As in the previous NHSN report, the highest reported testing frequencies (ie, >90% of isolates reported had testing results reported) were for S. aureus susceptibility to oxacillin, Enterococcus faecium and Enterococcus faecalis susceptibility to vancomycin, P. aeruginosa and E. coli susceptibility to fluoroquinolones, and P. aeruginosa and Enterobacter spp. susceptibility to extended-spectrum cephalosporins (Table 7). Although the value varied by HAI type, hospitals reported lower frequencies of testing Klebsiella spp. and E. coli susceptibility to carbapenems (range 64.3%–77.2% and 63.2%–77.2%, respectively). Pooled mean percent resistance for the pathogen-antimicrobial combinations is shown in Table 7. Pathogen percent resistance overall was generally lower for each resistance phenotype among SSIs, compared to that among device-associated HAIs. For most other pathogens, percent resistance differed only slightly between device-associated infection types. Notably, carbapenem resistance in CAUTIs and CLABSIs was very similar for Klebsiella spp. (12.5% and 12.8%, respectively) and E. coli (2.3% and 1.9%, respectively).

Table 7. 
Percentage of Pathogenic Isolates Resistant to Selected Antimicrobial Agents, National Healthcare Safety Network, 2009–2010
CLABSICAUTIVAPSSI
Pathogen, antimicrobialaNo. of isolates reportedNo. (%) of isolates testedResistance, %No. of isolates reportedNo. (%) of isolates testedResistance, %No. of isolates reportedNo. (%) of isolates testedResistance, %No. of isolates reportedNo. (%) of isolates testedResistance, %
Staphylococcus aureus3,7354422,0436,415
 OX/METH3,611 (96.7)54.6438 (99.1)58.71,974 (96.6)48.46,304 (98.3)43.7
Enterococcus spp.
E. faecium2,11865425517
  VAN2,069 (97.7)82.6639 (97.7)82.523 (92)82.6509 (98.5)62.3
E. faecalis2,6801,519451,240
  VAN2,578 (96.2)9.51,446 (95.2)8.441 (91.1)9.81,187 (95.7)6.2
Klebsiella (pneumoniae/oxytoca)2,4072,365854844
 ESC42,109 (87.6)28.81,998 (84.5)26.9747 (87.5)23.8710 (84.1)13.2
 Carbapenems1,858 (77.2)12.81,520 (64.3)12.5617 (72.2)11.2582 (69.0)7.9
 MDR11,932 (80.3)16.81,650 (69.8)16.1658 (77.0)13.4621 (73.6)6.8
Escherichia coli1,2065,6605041,981
 ESC41,067 (88.5)19.04,656 (82.3)12.3429 (85.1)16.31,627 (82.1)10.9
 FQ31,137 (94.3)41.85,513 (97.4)31.2466 (92.5)35.21,876 (94.7)25.3
 Carbapenems931 (77.2)1.93,579 (63.2)2.3344 (68.3)3.51,330 (67.1)2.0
 MDR1992 (82.3)3.73,929 (69.4)2.0365 (72.4)3.31,390 (70.2)1.6
Enterobacter spp.1,365880727849
 ESC41,309 (95.9)37.4818 (93.0)38.5690 (94.9)30.1816 (96.1)27.7
 Carbapenems1,041 (76.3)4.0614 (69.8)4.6530 (72.9)3.6594 (70.0)2.4
 MDR11,123 (82.3)3.7667 (75.8)4.8579 (79.6)1.4648 (76.3)1.7
Pseudomonas aeruginosa1,1662,3811,4081,156
 AMINOS819 (70.2)10.01,495 (62.8)10.9920 (65.3)11.3664 (57.4)6.0
 ESC21,120 (96.1)26.12,294 (96.3)25.21,355 (96.2)28.41,097 (94.9)10.2
 FQ21,114 (95.5)30.52,337 (98.2)33.51,378 (97.9)32.71,111 (96.1)16.9
 Carbapenems982 (84.2)26.11,883 (79.1)21.31,162 (82.5)30.2872 (75.4)11.0
 PIP/PIPTAZ809 (69.4)17.41,792 (75.3)16.61,059 (75.2)19.1818 (70.8)6.8
 MDR21,096 (94)15.42,250 (94.5)14.01,342 (95.3)17.71,053 (91.1)5.3
Acinetobacter baumannii629185557119
 Carbapenems522 (83)62.6128 (69.2)74.2449 (80.6)61.2102 (85.7)37.3
 MDR3617 (98.1)67.6183 (98.9)77.6552 (99.1)63.4114 (95.8)43.9

For the majority of resistant phenotypes evaluated, the percent resistance did not significantly differ by critical care location status (Table 8). Some differences did border on statistical significance, including higher values in the critical care areas for carbapenem resistance among A. baumannii or Klebsiella spp. and lower values in critical care units for S. aureus resistance to oxacillins (ie, MRSA) and E. coli resistance to fluoroquinolones. Because of the lack of consistent evidence that critical care locations are associated with higher percent resistance, data from all location types were combined, and changes in percent resistance for select resistant phenotypes are presented in Tables 912. Among CLABSIs, there was no significant change in percent resistance between the 2 time periods for most phenotypes. Exceptions include increases in extended-spectrum cephalosporin resistance among E. coli (and a corresponding increase in multidrug-resistant E. coli) and carbapenem resistance among A. baumannii (although this organism caused <2% of all HAIs reported). Similar patterns were observed among pathogens associated with CAUTIs. Among pathogens associated with VAP (Table 11) and SSI (Table 12), the percent resistance for MRSA declined slightly in the current period, compared to the earlier period.

Table 8. 
Percentage of Pathogenic Isolates Resistant to Selected Antimicrobial Agents, by Location of Patient Reported to the National Healthcare Safety Network, 2009–2010
CLABSICAUTI
Pathogen, antimicrobial agentsaICUNon-ICUICUNon-ICU
Staphylococcus aureus, oxacillins51.559.352.063.3
Enterococcus species
E. faecium, vancomycin83.680.781.883.1
E. faecalis, vancomycin9.49.55.511.8
Klebsiella (pneumoniae/oxytoca)
 ES cephalosporins 429.727.724.629.0
 Carbapenems14.210.912.412.6
 Multidrug resistant 119.113.715.217.0
Escherichia coli
 ES cephalosporins 418.619.511.513.2
 Fluoroquinolones 336.547.129.133.5
 Carbapenems1.92.01.72.9
 Multidrug resistant 13.44.01.62.3
Enterobacter species
 ES cephalosporins 438.036.238.838.2
 Carbapenems4.92.25.53.5
 Multidrug resistant 14.03.14.65.0
Pseudomonas aeruginosa
 Aminoglycosides11.67.511.89.9
 ES cephalosporins 228.322.622.528.3
 Fluoroquinolones 230.330.831.835.5
 Carbapenems26.824.920.622.3
 Piperacillin/tazobactam19.613.816.117.1
 Multidrug resistant 216.813.312.615.6
Acinetobacter baumannii
 Carbapenems64.556.173.875.0
 Multidrug resistant 369.760.478.676.1
Table 9. 
Changes in Resistance Percentage among Pathogens Associated with CLABSIs Reported to the National Healthcare Safety Network, 2007–2010, from both Critical Care and Non–Critical Care Locations
Pathogen, antimicrobial agentsaResistance percentage, 2007–2008, % (95% CI)Resistance percentage, 2009–2010, % (95% CI) Overall change, %P value
Staphylococcus aureus
 Oxacillins55.5 (53.5, 57.6)54.6 (53.0, 56.2)−1.7.49
Enterococcus species
E. faecium, vancomycin80.6 (78.4, 82.8)82.6 (81.0, 84.2)2.5.15
E. faecalis, vancomycin8.8 (7.4, 10.1)9.5 (8.3, 10.6)8.1.43
Klebsiella (pneumoniae/oxytoca)
 ES cephalosporins 431.7 (29.3, 34.2)28.8 (26.9, 30.8)−9.2.07
 Carbapenems13.2 (11.3, 15.1)12.8 (11.2, 14.3)−3.3.73
 Multidrug resistant 118.1 (16.0, 20.2)16.8 (15.1, 18.4)−7.4.32
Escherichia coli
 ES cephalosporins 412.3 (9.7, 15.0)19.0 (16.7, 21.4)54.3<.001
 Fluoroquinolones 337.7 (33.8, 41.5)41.8 (38.9, 44.6)10.9.10
 Carbapenems1.9 (0.7, 3.1)1.9 (1.0, 2.8)0.9.98
 Multidrug resistant 11.5 (0.5, 2.5)3.7 (2.6, 4.9)150.8.02
Enterobacter species
 ES cephalosporins 440.2 (37.0, 43.5)37.4 (34.8, 40.1)−7.0.19
 Carbapenems3.1 (1.8, 4.3)4.0 (2.8, 5.2)31.2.29
 Multidrug resistant 13.2 (2.0, 4.5)3.7 (2.6, 4.8)15.3.57
Pseudomonas aeruginosa
 Aminoglycosides7.4 (5.1, 9.6)10.0 (8.0, 12.1)36.2.10
 ES cephalosporins 227.6 (24.2, 31.0)26.1 (23.5, 28.6)−5.6.48
 Fluoroquinolones 231.4 (27.9, 35.0)30.5 (27.8, 33.2)−2.9.69
 Carbapenems26.8 (23.2, 30.4)26.1 (23.3, 28.8)−2.8.74
 Piperacillin/tazobactam21.1 (17.4, 24.7)17.4 (14.8, 20.0)−17.2.11
 Multidrug resistant 217.5 (14.5, 20.4)15.4 (13.3, 17.6)−11.7.26
Acinetobacter baumannii
 Carbapenems50.0 (45.6, 54.4)62.6 (58.5, 66.8)25.3<.0001
 Multidrug resistant 361.7 (57.6, 65.7)67.6 (63.9, 71.3)9.6.04
Table 10. 
Changes in Percent Resistance among Pathogens Associated with CAUTIs Reported to the National Healthcare Safety Network, 2007–2010, from Critical Care and Non–Critical Care Locations
Resistant pathogen, antimicrobial agentsaResistance percentage, 2007–2008, % (95% CI)Resistance percentage, 2009–2010, % (95% CI)Overall change, %P value
Staphylococcus aureus
 Oxacillins65.3 (59.6, 71.0)58.7 (54.1, 63.3)−10.2.07
Enterococcus species
E. faecium, vancomycin79.9 (76.0, 83.8)82.5 (79.5, 85.4)3.2.30
E. faecalis, vancomycin5.6 (4.1, 7.2)8.4 (7.0, 9.9)49.9.02
Klebsiella (pneumoniae/oxytoca)
 ES cephalosporins 427.1 (24.6, 29.6)26.9 (24.9, 28.8)−0.7.91
 Carbapenems11.7 (9.6, 13.8)12.5 (10.8, 14.2)6.9.56
 Multidrug resistant 116.0 (13.8, 18.3)16.1 (14.3, 17.9)0.5.96
Escherichia coli
 ES cephalosporins 410.6 (9.5, 11.7)12.3 (11.4, 13.3)16.3.02
 Fluoroquinolones 327.0 (25.5, 28.5)31.2 (30.0, 32.5)15.6<.0001
 Carbapenems2.9 (2.2, 3.7)2.3 (1.8, 2.8)−23.0.13
 Multidrug resistant 11.8 (1.2, 2.3)2.0 (1.5, 2.4)11.0.59
Enterobacter species
 ES cephalosporins 440.6 (36.4, 44.9)38.5 (35.2, 41.8)−5.2.44
 Carbapenems3.7 (1.7, 5.7)4.6 (2.9, 6.2)22.4.54
 Multidrug resistant 13.0 (1.3, 4.7)4.8 (3.2, 6.4)58.3.17
Pseudomonas aeruginosa
 Aminoglycosides10.7 (8.7, 12.7)10.9 (9.3, 12.5)1.9.88
 ES cephalosporins 224.3 (22.0, 26.5)25.2 (23.4, 27.0)3.9.53
 Fluoroquinolones 235.2 (32.7, 37.6)33.5 (31.6, 35.4)−4.7.29
 Carbapenems21.8 (19.3, 24.3)21.3 (19.5, 23.2)−1.9.80
 Piperacillin/tazobactam14.5 (12.3, 16.7)16.6 (14.9, 18.3)14.4.16
 Multidrug resistant 213.4 (11.6, 15.2)14.0 (12.6, 15.4)4.4.62
Acinetobacter baumannii
 Carbapenems63.5 (54.7, 72.3)74.2 (66.6, 81.8)16.9.08
 Multidrug resistant 382.1 (75.8, 88.5)77.6 (71.6, 83.6)−5.5.31
Table 11. 
Changes in Percent Resistance among Pathogens Associated with VAPs Reported to the National Healthcare Safety Network, 2007–2010
Resistant pathogen, antimicrobial agentsaResistance percentage, 2007–2008, % (95% CI)Resistance percentage, 2009–2010, % (95% CI)Overall change, %P value
Staphylococcus aureus
 Oxacillins51.9 (49.6, 54.1)48.4 (46.2, 50.6)−6.7.03
Enterococcus species
E. faecium, vancomycin82.4 (64.2, 100.5)82.6 (67.1, 98.1)0.3.98
E. faecalis, vancomycin6.4 (−0.6, 13.4)9.8 (0.7, 18.8)52.8.56
Klebsiella (pneumoniae/oxytoca)
 ES cephalosporins 421.5 (18.5, 24.5)23.8 (20.8, 26.9)10.9.29
 Carbapenems9.9 (7.5, 12.4)11.2 (8.7, 13.7)12.6.48
 Multidrug resistant 111.8 (9.3, 14.4)13.4 (10.8, 16.0)13.0.41
Escherichia coli
 ES cephalosporins 414.2 (10.6, 17.9)16.3 (12.8, 19.8)14.5.43
 Fluoroquinolones 333.3 (28.6, 38.1)35.2 (30.9, 39.5)5.6.57
 Carbapenems3.0 (1.0, 5.1)3.5 (1.5, 5.4)15.1.75
 Multidrug resistant 11.7 (0.2, 3.1)3.3 (1.5, 5.1)95.9.20
Enterobacter species
 ES cephalosporins 434.6 (30.9, 38.3)30.1 (26.7, 33.6)−13.0.08
 Carbapenems 24.6 (2.7, 6.6)3.6 (2.0, 5.2)−22.7.41
 Multidrug resistant 12.5 (1.1, 3.8)1.4 (0.4, 2.3)−43.8.20
Pseudomonas aeruginosa
 Aminoglycosides10.8 (8.9, 12.7)11.3 (9.3, 13.4)4.6.73
 ES cephalosporins 228.5 (26.1, 30.8)28.4 (26.0, 30.8)−0.2.98
 Fluoroquinolones 232.7 (30.3, 35.2)32.7 (30.3, 35.2)0.0.99
 Carbapenems 231.1 (28.4, 33.8)30.2 (27.6, 32.8)−2.8.65
 Piperacillin/tazobactam19.2 (16.8, 21.6)19.1 (16.7, 21.4)−0.8.93
 Multidrug resistant 216.6 (14.7, 18.6)17.7 (15.6, 19.7)6.2.48
Acinetobacter baumannii
 Carbapenems56.7 (52.8, 60.6)61.2 (56.7, 65.8)8.1.13
 Multidrug resistant 367.4 (63.9, 71.0)63.4 (59.4, 67.4)−6.0.14
Table 12. 
Changes in Percent Resistance among Pathogens Associated with SSIs Reported to the National Healthcare Safety Network, 2007–2010
Resistant pathogen, antimicrobial agentsaResistance percentage, 2007–2008, % (95% CI)Resistance percentage, 2009–2010, % (95% CI)Overall change, %P value
Staphylococcus aureus
 Oxacillins48.0 (46.5, 49.5)43.7 (42.5, 44.9)−9.0<.0001
Enterococcus species
E. faecium, vancomycin65.2 (60.6, 69.7)62.3 (58.1, 66.5)−4.4.36
E. faecalis, vancomycin4.6 (3.1, 6.2)6.2 (4.9, 7.6)34.7.14
Klebsiella (pneumoniae/oxytoca)
 ES cephalosporins 419.4 (15.9, 22.9)13.2 (10.7, 15.7)−31.7<.01
 Carbapenems9.6 (6.7, 12.5)7.9 (5.7, 10.1)−17.7.35
 Multidrug resistant 110.9 (7.9, 13.8)6.8 (4.8, 8.7)−37.8.02
Escherichia coli
 ES cephalosporins 49.1 (7.5, 10.7)10.9 (9.4, 12.5)20.2.11
 Fluoroquinolones 327.2 (24.8, 29.5)25.3 (23.3, 27.2)−7.0.23
 Carbapenems1.5 (0.7, 2.2)2.0 (1.3, 2.8)38.2.31
 Multidrug resistant 11.1 (0.5, 1.7)1.6 (0.9, 2.2)41.8.33
Enterobacter species
 ES cephalosporins 430.6 (26.8, 34.5)27.7 (24.6, 30.8)−9.5.24
 Carbapenems2.8 (1.2, 4.3)2.4 (1.1, 3.6)−14.4.69
 Multidrug resistant 11.5 (0.4, 2.7)1.7 (0.7, 2.7)10.6.83
Pseudomonas aeruginosa
 Aminoglycosides4.4 (2.5, 6.3)6.0 (4.2, 7.8)37.7.23
 ES cephalosporins 213.6 (11.1, 16.0)10.2 (8.4, 12.0)−24.8.03
 Fluoroquinolones 215.8 (13.2, 18.4)16.9 (14.7, 19.1)7.2.51
 Carbapenems11.2 (8.7, 13.8)11.0 (8.9, 13.1)−2.1.89
 Piperacillin/tazobactam6.8 (4.7, 8.8)6.8 (5.1, 8.6)1.3.95
 Multidrug resistant 24.9 (3.3, 6.5)5.3 (4.0, 6.7)8.4.70
Acinetobacter baumannii
 Carbapenems38.6 (28.5, 48.8)37.3 (27.9, 46.6)−3.6.85
 Multidrug resistant 349.5 (39.6, 59.3)43.9 (34.8, 53.0)−11.4.41

There was great variation in the degree of spread of antimicrobial-resistant infections (additional figures can be found on the CDC website, http://www.cdc.gov/nhsn/dataStat.html). Of the 2,039 facilities that reported at least 1 HAI to NHSN during 2009–2010, 1,637 reported at least 1 CLABSI. Among facilities reporting 1 or more CLABSIs with a bacterial pathogen of interest (regardless of resistance), the proportion reporting a resistant phenotype was very high for MRSA (76%) and vancomycin-resistant E. faecium (89%); it was very low for E. coli or Enterobacter spp. resistant to carbapenems, 4% and 7%, respectively. It was modest for the other resistant pathogens. For example, 20% of facilities reporting a CLABSI with Klebsiella spp. reported at least 1 as carbapenem resistant.

Among the 871 facilities reporting 1 or more CAUTIs with a select bacterial pathogen (regardless of resistance), the proportion reporting a resistant phenotype was very high for vancomycin-resistant E. faecium (86%) and fluoroquinolone-resistant E. coli (67%); it was lower for E. coli resistant to carbapenems (8%). Similar to data for CLABSIs, 20% of facilities reporting a CAUTI with Klebsiella spp. reported at least 1 as carbapenem resistant. Among the 570 facilities reporting at least 1 VAP with a bacterial pathogen, the proportion reporting a resistant phenotype was very high for MRSA (77%) and carbapenem-resistant A. baumannii (56%); 16% of facilities reporting a VAP with Klebsiella spp. reported at least 1 as carbapenem resistant. The proportions of facilities reporting CAUTI or VAP pathogens resistant to select antimicrobials are summarized on the CDC website (http://www.cdc.gov/nhsn/dataStat.html).

Among the 1,029 facilities reporting 1 or more SSIs, the pattern was very different. Most (77%) facilities reporting an SSI with S. aureus reported at least 1 as MRSA, similar to results for other HAI types. However, the proportion of facilities reporting SSIs with resistant phenotypes was overall quite low among those pathogens most commonly associated with SSIs.

Discussion

These data present a high-level overview of the antimicrobial resistance problem challenging clinicians and affecting patients who develop HAIs in US hospitals. From these data, we can make several observations that will help advance our understanding of the pathogenesis, preventability, and treatment options of these infections. First, pooled mean percent resistance for certain high-profile resistance phenotypes has decreased. Most notably, we observed a slightly lower percent resistance among device-associated HAIs for MRSA, with relative decreases of 1.7% among CLABSIs, 10.2% among CAUTIs, 6.7% among VAP, and 9% among SSIs (the latter 2 being statistically significant decreases). The changes in MRSA are consistent with recent findings from different surveillance programs focused on MRSA.5,6 Although this decrease in percent resistance is noteworthy, the reasons for it are not known with certainty and are likely multifactorial.

Second, among gram-negative bacteria, there were no consistent trends but some reason for concern.7-10 Although they are a less common cause of HAIs, both multidrug resistance and carbapenem resistance were reported in more than 60% of Acinetobacter spp. among most HAI types, and 70%–80% of facilities reporting an HAI with Acinetobacter spp. reported at least one multidrug-resistant strain. Carbapenem resistance among Klebsiella spp. was stable between time periods (about 13%), but almost 1 in 5 hospitals reporting CLABSIs or CAUTIs with Klebsiella spp. have reported a carbapenem-resistant phenotype as the cause of the infection. This suggests that the problem of highly resistant gram-negative bacteria causing HAIs is not limited to just a small subset of hospitals, and it reinforces the need for prevention efforts designed to prevent the further emergence and spread of these pathogens.8 The fact that carbapenem-resistant Enterobacteriaceae (CRE) are not routinely identified from HAIs from a large proportion of hospitals reporting to NHSN highlights that in many places the identification of CRE from a clinical culture should prompt an aggressive response to prevent further transmission. CDC’s updated CRE prevention recommendations are highlighted at http://www.cdc.gov/HAI/organisms/cre/index.html.

Third, there have been some changes in the distribution of pathogens reported in these device- and procedure-associated HAIs: coagulase-negative staphylococci are a less prominent cause of HAIs in the more recent years, and Candida spp. are slightly more common. This latter observation is subtle, because the current data exclude asymptomatic CAUTI, which is no longer reported to NHSN as of 2009, when the NHSN changed the case definition of CAUTI to exclude asymptomatic bacteriuria (http://www.cdc.gov/nhsn/library.html). Among CLABSIs, these changes suggest that recent prevention efforts may preferentially prevent certain pathogenesis of infection over others. Another possibility for the observed change is less frequent reporting of CLABSIs associated with certain pathogens because of suboptimal implementation of case-finding and reporting methodology.11

Participation in NHSN during the time period covered in this report was a combination of voluntary and mandatory reporting; participation in NHSN related to the CMS Hospital Inpatient Quality Reporting Program was not in effect until 2011 for CLABSIs among critical care patients and 2012 for CAUTIs or SSIs among patients undergoing abdominal hysterectomies or colon surgery. As reporting becomes more comprehensive across the United States, tracking the degree of spread of these and other emerging resistant pathogens will improve and will allow more accurate assessments of how widespread any one resistant phenotype is and how successful facilities and states have been in curtailing or reversing the spread of specific phenotypes across hospitals in the United States.

Direct comparisons of these resistance data with those reported in other studies and even with prior NHSN data have limitations. The patient population may not be representative of the US patient population as a whole; although the data in this report are not from a comprehensive set of hospitals, they represent the largest group of hospitals reporting antimicrobial susceptibility data related to clinically relevant infections. Of note, the majority of hospitals (56.1%) contributing data to this report had fewer than 200 beds; the changing demographics of hospital participation in NHSN toward inclusion of more small hospitals may explain some of the new observations noted in this report. Most US hospitals will expand reporting of HAIs to comply with federal pay-for-reporting programs in 2011–2013. Analysis of data reported from 2011 and beyond will be more representative of all US hospitals and will lead to more informed guidance regarding treatment or prophylaxis strategies. An additional limitation of this report is the use of antimicrobial susceptibility testing data from laboratories servicing the hospitals and not from a single referral laboratory. Related to this fact is that facilities may perform selective testing (cascade testing) of broad-spectrum agents or have systems that have suppression rules in place preventing testing results from being readily available to NHSN users entering data, resulting in some selection bias; inasmuch as more than 80% of isolates had testing results for most phenotypes, any inflation of proportions is likely to be small. In addition, as NHSN captures only the interpretation (S, I, or R) and not the measured minimum inhibitory concentration, the interpretations of susceptibility by individual hospital might vary slightly.

However, despite these limitations, these data represent a current assessment of the prevalence of antimicrobial-resistant phenotypes associated with HAIs in patients across approximately 2,000 hospitals in the United States. Several of the resistant phenotypes assessed are not limited to a small subset of hospitals, which should alert the infection control community to the need for vigilance in identification and implementation of appropriate infection control as they address these challenges in coming years.

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, who tirelessly support 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. 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.

References

  1. 1. Hidron AI, Edwards JR, Patel J, et al. 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. Infect Control Hosp Epidemiol 2008;29(11):996–1011. Erratum in Infect Control Hosp Epidemiol 2009;30(1):107.
  2. 2. CDC. The National Healthcare Safety Network (NHSN) Manual. Patient Safety Component Protocol. Centers for Disease Control and Prevention website. http://www.cdc.gov/ncidod/dhqp/pdf/nhsn/NHSN_Manual_PatientSafetyProtocol_CURRENT.pdf. Published 2008.
  3. 3. Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing—sixteenth informational supplement. Wayne, PA: CLSI, 2008. CLSI document M100-S18.
  4. 4. Magiorakos A-P, Srinivasan A, Carey RB, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012;18(3):268–281.
  5. 5. Landrum ML, Neumann C, Cook C, et al. Epidemiology of Staphylococcus aureus blood and skin and soft tissue infections in the US military health system, 2005–2010. JAMA 2012;308(1):50–59.
  6. 6. Kallen AJ, Mu Y, Bulens S, et al; Health care–associated invasive MRSA infections, 2005–2008. JAMA 2010;304(6):641–648.
  7. 7. Kallen AJ, Hidron AI, Patel J, Srinivasan A. Multidrug resistance among gram-negative pathogens that caused healthcare-associated infections reported to the National Healthcare Safety Network, 2006–2008. Infect Control Hosp Epidemiol 2010;31(5):528–531.
  8. 8. Bradley JS, Guidos R, Baragona S, et al. Anti-infective research and development: problems, challenges, and solutions. Lancet 2007;7:68–78.
  9. 9. Lewis JS II, 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.
  10. 10. 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.
  11. 11. Sexton DJ, Chen LF, Anderson DJ. Current definitions of central line–associated bloodstream infection: is the emperor wearing clothes? Infect Control Hosp Epidemiol 2010;31(12):1286–1289.

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, who tirelessly support 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. 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.

References

  1. 1. Hidron AI, Edwards JR, Patel J, et al. 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. Infect Control Hosp Epidemiol 2008;29(11):996–1011. Erratum in Infect Control Hosp Epidemiol 2009;30(1):107.
  2. 2. CDC. The National Healthcare Safety Network (NHSN) Manual. Patient Safety Component Protocol. Centers for Disease Control and Prevention website. http://www.cdc.gov/ncidod/dhqp/pdf/nhsn/NHSN_Manual_PatientSafetyProtocol_CURRENT.pdf. Published 2008.
  3. 3. Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing—sixteenth informational supplement. Wayne, PA: CLSI, 2008. CLSI document M100-S18.
  4. 4. Magiorakos A-P, Srinivasan A, Carey RB, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012;18(3):268–281.
  5. 5. Landrum ML, Neumann C, Cook C, et al. Epidemiology of Staphylococcus aureus blood and skin and soft tissue infections in the US military health system, 2005–2010. JAMA 2012;308(1):50–59.
  6. 6. Kallen AJ, Mu Y, Bulens S, et al; Health care–associated invasive MRSA infections, 2005–2008. JAMA 2010;304(6):641–648.
  7. 7. Kallen AJ, Hidron AI, Patel J, Srinivasan A. Multidrug resistance among gram-negative pathogens that caused healthcare-associated infections reported to the National Healthcare Safety Network, 2006–2008. Infect Control Hosp Epidemiol 2010;31(5):528–531.
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