MAJOR ARTICLE

Antimicrobial Resistance Prevalence Rates

in Hospital Antibiograms Reflect Prevalence
Rates among Pathogens Associated

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with Hospital-Acquired Infections
Scott K. Fridkin,1 Jonathan R. Edwards,1 Fred C. Tenover,1 Robert P. Gaynes,1 John E. McGowan, Jr.,2
for the Intensive Care Antimicrobial Resistance Epidemiology (ICARE) Project and the National Nosocomial
Infections Surveillance (NNIS) System Hospitals
1
Hospital Infections Program, National Center for Infectious Diseases, Centers for Disease Control and Prevention, and 2Department
of Epidemiology, Rollins School of Public Health, Emory University, Atlanta

To determine whether routine antibiograms (summaries reporting resistance of all tested isolates) reflect resistance
rates among pathogens associated with hospital-acquired infections, we compared data collected from 2 different
surveillance components in the same 166 intensive care units (ICUs). ICUs reported data during the same months
to both the infection-based surveillance and the laboratory-based surveillance. Paired comparisons of the per-
centage of isolates resistant were made between systems within each ICU. No significant differences existed
(P 1 .05) between the percentage of isolates resistant from the infection-based system and laboratory-based system
for all antimicrobial-resistant organisms studied, except methicillin resistance in Staphylococcus species. The
mean difference in percentage resistance was higher from the infection-based system than the laboratory-based
system for S. aureus (mean difference, +8%, P ! .001 ) and coagulase-negative staphylococci (mean difference,
+9%, P ! .001). Overall, hospital antibiograms reflected susceptibility patterns among isolates associated with
hospital-acquired infections. Hospital antibiograms may underestimate the relative frequency of methicillin
resistance among Staphylococcus species when associated with hospital-acquired infections.

Susceptibility statistics, consisting of the cumulative and
ongoing summary of the patterns of antimicrobial sus-
ceptibility of clinically important bacteria, are impor-
Received 2 October 2000; revised 7 December 2000; electronically published
21 June 2001.
Financial support: Grants to the Rollins School of Public Health of Emory
University for phase 2 and 3 of Project ICARE by AstraZeneca Pharmaceuticals
(Wilmington, DE) and Pfizer, Inc. (New York, NY). Full sponsors: Roche Laboratories
(Nutley, NJ). Partial sponsors: Aventis Pharma (formerly Rhone-Poulenc Rorer;
Collegeville, PA), the National Foundation for Infectious Diseases (Bethesda, MD),
the American Society for Health Systems Pharmacists Research and Education
Foundation (Bethesda, MD), Kimberly-Clark Corporation (Roswell, GA), and Bayer
Corporation, Pharmaceuticals Division (West Haven, CT).
Reprints or correspondence: Dr. Scott K. Fridkin, Hospital Infections Program,
MS E-A35, Centers for Disease Control and Prevention, 1600 Clifton Rd., Atlanta,
GA 30333 (skf0@cdc.gov).
Clinical Infectious Diseases 2001; 33:324–30
 2001 by the Infectious Diseases Society of America. All rights reserved.
1058-4838/2001/3303-0009$03.00
tant to various health care practitioners, including phy-
sicians, pharmacists, infection control personnel, and
microbiologists [1, 2]. Currently there are no standards
by which isolates should be included in these summary
data, although such guidelines are in development by
the National Committee for Clinical Laboratory Stan-
dards (NCCLS). Many issues regarding generating these
reports, such as handling duplicate isolates, incorpo-
ration of only select sites of cultures, or isolates from
only confirmed infections are currently being discussed
by NCCLS (J. Hindler, personal communication). The
frequency of antimicrobial resistance among isolates
from patients with infections acquired in the health care
setting may be different from that among all isolates
processed by the clinical microbiology laboratory [3].
If such differences were observed, then separate sum-
mary reports would be needed for hospital-acquired

324 • CID 2001:33 (1 August) • Fridkin et al.


Figure 1. Diagram of sources, type, and eligible data from the 2 surveillance systems: the ICU component of the National Nosocomial Infections
Surveillance (NNIS) system, or the Intensive Care Antimicrobial Resistance Epidemiology (ICARE) component of NNIS. ICU, intensive care unit; MICU,
medical ICU; PICU, pediatric ICU; SICU, general surgical ICU.
infections and community infections to best aid in empiric
therapy decisions. Such reports would be difficult to generate
by many clinical microbiology laboratories. Validating the clin-
ical relevance of “all-isolate” summaries for health
care–acquired infections would provide support for the current
widespread practice of using a single summary report in most
hospitals.
To augment surveillance for antimicrobial resistance at hos-
pitals in the United States, the Hospital Infections Program at
Centers for Disease Control and Prevention (CDC), in collab-
oration with the Rollins School of Public Health of Emory
University, began Project ICARE (Intensive Care Antimicrobial
Resistance Epidemiology) in 1996 at a subset of hospitals par-
ticipating in CDC’s National Nosocomial Infections Surveil-
lance (NNIS) system. Project ICARE hospitals reported data
on all strains of selected bacteria tested in the clinical micro-
biology laboratory. These data allowed for determination of
prevalence rates of resistance similar to the routine hospital
cumulative antibiogram. The cumulative antibiogram or cu-
mulative susceptibility test data report is the percentage of iso-
lates of a given species tested in a given institution, or specific
areas of the institution, that are susceptible or resistant to each
of the antimicrobial agents routinely tested. We used data gath-
ered from hospitals participating in our study to study differ-
ences in the prevalence of resistance in participating intensive
care units (ICUs) among bacteria reported through laboratory-
based surveillance (as reported through Project ICARE) to the
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prevalence of resistance among isolates associated with hospital-
acquired infections reported through infection-based surveil-
lance (pathogens reported through the NNIS-ICU component).
Validation of the clinical relevance of the routine hospital anti-
biogram would increase the confidence level among clinicians
that laboratory-based data can guide empiric therapy for pa-
tients with hospital-acquired infections.
METHODS
Surveillance data and sites. Hospitals that participate in the
ICU surveillance component of the NNIS-ICU system were
invited to participate in Project ICARE (NNIS-ICARE), and 61
hospitals representing 171 ICUs submitted data to Project
ICARE and the ICU component of the NNIS system during
the study period January 1996–April 2000. The surveillance
methodology and definitions of the NNIS system [4, 5] and
Project ICARE [6] have been described elsewhere.
Infection-based reports. Participating hospitals reported
monthly hospital-acquired infection data from at least one ICU
to NNIS-ICU. The NNIS-ICU data include information on all
hospital-acquired infections (infections occurring at any site)
detected in patients during the month in which active sur-
veillance occurred in the ICU (figure 1). The susceptibility in-
terpretation (susceptible, intermediate, resistant) for drugs
tested against each pathogen associated with the hospital-ac-
quired infection is reported according to NCCLS breakpoint
definitions [7–9]. This allows for determining the cumulative
Cumulative Susceptibility Data • CID 2001:33 (1 August) • 325
susceptibility report, or antibiogram, of all pathogens associated
with hospital-acquired infections during that month (hospital-
acquired infection–based cumulative antibiogram). As partic-
ipants in the NNIS system, hospital personnel had previously
categorized each ICU at their hospital by the types of patients
served: coronary, medical, general surgical, cardiothoracic,
combined medical-surgical (units where !80% of patients can
be classified into a single unit type), neurosurgical, respiratory,
trauma, or burn. A proficiency testing of Project ICARE clinical
microbiology laboratories determined that despite different
methodologies, testing produced accurate results to 6 challenge
organisms [10].
Laboratory-based reports. As part of NNIS-ICARE, hos-
pitals also reported susceptibility data on select organisms from
clinical specimens (e.g., blood, urine, sputum, and wound)
obtained from patients in these same ICUs, whether associated
with hospital-acquired or community-acquired infection or
colonization (figure 1). Duplicate isolates were excluded; these
were defined as isolates of the same organism with the same
antimicrobial resistance pattern recovered from the same pa-
tient, regardless of the site of isolation, during the same calendar
month. This allowed for determining the cumulative suscep-
tibility report, or antibiogram, of all organisms processed from
clinical specimens submitted to the clinical microbiology lab-
oratory (laboratory-based cumulative antibiogram).
Data analysis. Data were analyzed by SAS version 6.12
software (SAS). For each ICU, only months in which data were
reported to both NNIS-ICU and NNIS-ICARE were selected
for analysis (eligible unit-months; figure 1). For all of the el-
igible unit-months, pooled data (aggregate data combining all
eligible unit-months for each ICU) about each organism were
compared between the laboratory-based and infection-based
reporting systems within each ICU. The testing rates (number
of isolates tested against a specified antimicrobial per month)
and prevalence rates of resistance (percentage of isolates tested
that were resistant) were calculated for each reporting system.
Prevalence rates of resistance were calculated only if ⭓10 isolates
were tested to the specified antimicrobial in the pooled data, and
included rates for methicillin-resistant Staphylococcus aureus
(MRSA); methicillin-resistant coagulase-negative staphylococci;
vancomycin-resistant Enterococcus species, ciprofloxacin-resistant
or ofloxacin-resistant Escherichia coli; ceftazidime-resistant, ce-
fotaxime-resistant, or ceftriaxone (third-generation cephalospo-
rin)–resistant E. coli; third-generation cephalosporin-resistant
Klebsiella pneumoniae; third-generation cephalosporin-resistant
Enterobacter species; piperacillin-resistant Pseudomonas aerugi-
nosa; ceftazidime-resistant P. aeruginosa; imipenem-resistant P.
aeruginosa, and ciprofloxacin-resistant or ofloxacin-resistant P.
aeruginosa.
Further analysis included pairwise comparisons of the av-
erage number of isolates tested per month and the average
326 • CID 2001:33 (1 August) • Fridkin et al.
difference in resistance rate (infection-based rate minus labo-
ratory-based rate). Pairwise comparisons were performed to
measure the difference between reporting systems (laboratory
based vs. infection based) within each ICU. A x2 test was per-
formed to test the homogeneity of the differences among all
ICUs. These comparisons were aggregated to determine statis-
tical significance. If the differences were homogeneous, a
weighted mean was calculated and tested against zero by means
of a Z test to determine a P value. In case of nonhomogeneity,
the average difference was also tested against zero by means of
a Z test. Additionally, to test for absence of mean effect both.
Wilcoxon signed rank and paired t tests were also used to
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confirm the above analyses (data not shown).
RESULTS
Sites. During the study period, 61 hospitals followed the
NNIS-ICARE surveillance protocol and reported a median of
12 months of data from all isolates tested in 166 ICUs, for a
total of 2669 ICU-months of laboratory-based susceptibility
data. During the study period, these hospitals reported 12,398
hospital-acquired infections from the same ICUs, providing a
total of 2080 ICU-months of infection-based susceptibility data
during months overlapping with the laboratory-based suscep-
tibility data (for some months, no infections were reported).
Hospitals were in 26 states (4 New England, 15 mid-Atlantic,
19 south Atlantic, 13 east-central, 6 west-central, and 4 Pacific
hospitals) and had a median of 385 hospital beds (range,
147–1206 beds); 30 (50%) reported a major affiliation with a
teaching institution (major teaching centers), and 6 (10%) were
Veterans Affairs Medical Centers. The ICUs included 45 med-
ical-surgical ICUs, 28 medical ICUs, 26 general surgical ICUs,
22 CCUs, 18 cardiothoracic ICUs, 12 pediatric ICUs, 9 neu-
rosurgical ICUs, 3 trauma ICUs, 2 burn ICUs, and 1 respiratory
ICU.
Frequency of organism testing. For the 11 antimicrobial-
resistant organisms evaluated, the ICU-specific average number
of organisms tested for susceptibility varied by organism, anti-
microbial agent tested, and reporting system. In the laboratory-
based system, the testing rate for S. aureus and coagulase-neg-
ative staphylococci tested to methicillin group agents was
highest (median values of 3.1 and 3.3 organisms tested per
month, respectively), whereas Enterobacter species tested for
third-generation cephalosporin susceptibility was lowest (me-
dian value of 1.4 organisms per month). In contrast, the average
testing rate by the infection-based system (organisms associated
with a hospital-acquired infection) was consistently ⭐1 per
month. Therefore, the testing rate of the laboratory-based sys-
tem was ∼4-fold higher than for the infection-based reporting
(table 1).
Prevalence of resistance to antimicrobial agents. The
prevalence of resistance to antimicrobial agents from the study
hospitals reporting to the infection-based system (table 2) was
 Table 1. Testing rates of select organisms to specific antimicrobial agents and the ratio
of testing rates among intensive care units (ICUs).

Median
b c
testing rate Ratio of testing rates
Antimicrobial
Organism agenta IBRS LBRS Median 25th–75th percentile
Staphylococcus aureus Oxacillin 1.0 3.1 4.0 2.8–7.2
Enterococcus species Vancomycin 1.0 2.2 4.9 2.9–6.4
Coagulase-negative staphylococci Oxacillin 0.8 3.3 5.5 4.1–9.3
Klebsiella pneumoniae Ceftazidimed 0.6 1.5 3.4 2.1–3.8
Escherichia coli Ceftazidimed 0.6 2.1 4.3 2.7–8.0
E. coli Quinolone 0.6 2.2 4.8 3.5–7.2

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Enterobacter species Ceftazidimed 0.7 1.4 2.7 2.1–3.9
Pseudomonas aeruginosa Imipenem 0.8 2.3 3.0 2.4–6.2
P. aeruginosa Ceftazidime 0.8 2.6 3.8 2.3–6.2
P. aeruginosa Quinolone 0.8 2.3 3.6 2.4–5.1
P. aeruginosa Piperacillin 0.8 2.3 3.6 2.5–6.2

NOTE. ICUs reported testing ⭓10 isolates to both the National Nosocomial Infections Surveillance System, ICU component
(infection-based reporting system) or National Nosocomial Infections Surveillance–Intensive Care Antimicrobial Resistance Ep-
idemiology (laboratory-based reporting system), January 1996–April 2000. IBRS, infection-based reporting system; LBRS, lab-
oratory-based reporting system.
a
Quinolone indicates ofloxacin or ciprofloxacin.
b
Testing rate is the average number of isolates tested against a specified antimicrobial per month for all data in an ICU.
c
Median and 25th–75th percentiles of all testing ratios (number of isolates tested by laboratory-based system divided by
the number tested by infection-based system) for the organism listed.
d
Organism tested against ceftazidime, ceftriaxone, or cefotaxime.

similar to that previously reported from the all NNIS hospitals
reporting data from ICU patients (http://www.cdc.gov/ncidod/
hip/surveill/nnis.htm) [11]. For the 11 antimicrobial-resistant
organisms evaluated, the number of ICUs testing ⭓10 organ-
isms was consistently higher when we used data from the lab-
oratory-based reporting system (median value, 110, range,
96–132 ICUs) than the infection-based system (median value,
26, range, 10–44 ICUs). Therefore, comparisons between the
2 reporting systems is limited to those ICUs that reported sus-
ceptibility results on a sufficient numbers of organisms by the
infection-based system.
The prevalence rates of resistance to antimicrobial agents
among all ICUs were usually higher among isolates reported
to the infection-based system than among isolates reported to
the laboratory-based system (table 2). However, these differ-
ences were rarely statistically significant when we used the pair-
wise comparisons, which takes into account the differences
observed within each ICU and the consistency with which these
differences were observed. There were 2 notable exceptions. By
use of the pairwise comparisons, infection-based prevalence of
resistance was significantly higher than laboratory-based prev-
alence for MRSA (average difference, ⫹7.9%; P ! .001) and
methicillin-resistant coagulase-negative staphylococci (mean
difference, ⫹8.7%; P ! .001; table 2). Similar comparisons for
the other organisms evaluated identified no additional signif-
icant differences. Similar analysis comparing the percentage of
isolates susceptible to the antimicrobial revealed similar results.
It is of note that the mean difference in the prevalence of
vancomycin-susceptible enterococci between the 2 systems was
11%, although this difference still did not reach statistical
significance.
DISCUSSION
Aggregating cumulative susceptibility data is a common prac-
tice among clinical microbiology laboratories, but the best
methodology to analyze and present these data has not been
determined. The most common use of the hospital antibio-
grams data is probably for assisting clinicians with empiric
therapy for suspected infections [2]. Our study suggests cu-
mulative susceptibility data (laboratory-based reporting) that
clinicians use to guide empiric treatment of hospital-acquired
infections usually will be representative of the organisms fre-
quently encountered among hospital-acquired infections. Our
study evaluated select patterns of resistance to antimicrobial
agents among the organisms most frequently associated with
hospital-acquired infections and compared the resistance rates
reported to a laboratory-based monitoring system (NNIS-
ICARE) to rates reported to an infection-based monitoring
system (NNIS-ICU). With 2 exceptions, the resistance rates
among isolates associated with only hospital-acquired infec-
tions were similar to rates among isolates associated with in-
fection (both community and hospital acquired), colonization,
and contaminants.
The 2 organisms associated with significantly higher rates of

Cumulative Susceptibility Data • CID 2001:33 (1 August) • 327

 Table 2. Pooled mean prevalence of resistance to antimicrobial agents among select isolates from
patients treated in intensive care units (ICUs).

Pooled mean, %R Pairwise

No.
(no. tested) difference, %R
of
Antimicrobial-resistant organism ICUs IBRS LBRS Meana Pb
Methicillin-resistant Staphylococcus aureus 44 44.6 (1639) 38.4 (9813) ⫹7.9 !.001
Vancomycin-resistant enterococci 25 19.2 (907) 16.1 (6208) ⫹0.5 .36
Methicillin-resistant coagulase-negative staphylococci 33 83.7 (1241) 74.4 (8602) ⫹8.7 !.001
c
Ceftazidime-resistant Klebsiella pneumonia 10 12.0 (515) 6.7 (3718) ⫺0.1 .63
c
Ceftazidime-resistant Escherichia coli 22 4.4 (768) 1.7 (5451) ⫹0.4 .30
Quinolone-resistant E. coli 20 1.7 (754) 2.8 (5185) 0.0 .50

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Ceftazidime-resistant Enterobacter speciesc 25 30.9 (868) 26.2 (3831) ⫹3.2 .06
Imipenem-resistant Pseudomonas aeruginosa 20 15.9 (622) 15.8 (6064) ⫺2.8 .94
Ceftazidime-resistant P. aeruginosa 39 8.6 (1260) 11.8 (7075) ⫺1.9 .99
Quinolone-resistant P. aeruginosa 37 17.5 (1234) 23.1 (7053) ⫺2.5 .97
Piperacillin-resistant P. aeruginosa 32 12.0 (942) 14.6 (6012) ⫺1.5 .88

NOTE. Included are data from ICUs that reported sufficient data (⭓10 isolates) to both laboratory-based and infection-
based reporting systems and the average difference in prevalence by reporting system, National Nosocomial Infections Sur-
veillance System, January 1996–April 2000. IBRS, infection-based reporting system; LBRS, laboratory-based reporting system;
%R, prevalence of resistance.
a
Weighted mean difference for all organisms except S. aureus and coagulase-negative staphylococci (arithmetic mean).
b
P value by Z test of weighted mean difference among paired resistance rates, except S. aureus and coagulase-negative
staphylococci, by Z test of mean difference. Paired t test and Wilcoxon signed-rank test resulted in similar P values (data not
shown).
c
Denotes nonsusceptibility (E. coli or Klebsiella pneumoniae) or resistance (Enterobacter species) to ceftazidime, ceftriaxone,
or cefotaxime.

resistance among isolates reported to the infection-based system
compared with the laboratory-based system were MRSA and
methicillin-resistant coagulase-negative staphylococci. Although
several other organisms tended to be associated with higher re-
sistance rates in the infection-based system, these differences were
not statistically significant. We would expect that resistance to
antimicrobial agents is more frequently encountered among
organisms associated with hospital-acquired infections com-
pared with community-infections for several reasons. First, pre-
vious analysis of data from Project ICARE demonstrated that,
with a few exceptions (i.e, Streptococcus pneumoniae), organ-
isms with onset of disease in the community (from the out-
patient or emergency department setting) are less likely to be
resistant to antimicrobial agents than are those encountered in
the inpatient setting [6]. Second, patients with longer hospital
stays are at increased risk to become infected with antimicro-
bial-resistant pathogens, and these isolates would be more rep-
resented in a infection-based system (i.e., nosocomial infection)
than the laboratory-based system [3, 12–14]. Third, there would
be potential for reporting bias if infection control practitioners
were more likely to report hospital-acquired infections when
they were associated with an antimicrobial-resistant pathogen,
although this seems unlikely. Some of these hypotheses may
explain the significantly higher resistance rates observed in data
from infection-based reporting compared with that from lab-
oratory-based reporting among MRSA and methicillin-resistant
coagulase-negative staphylococci. However, the impact of these
factors does not appear strong enough to consistently create
differences in measured resistance prevalence of any magnitude
worthy of clinical importance. If the sample of data were larger,
we might have identified more significant differences in the
reporting systems. However, the relative differences in resis-
tance prevalence observed were small (!10%) and unlikely to
have any clinical impact, even if differences were to become
statistically significant.
We limited our study to ICUs because our surveillance data
for hospital-acquired infections were limited to the ICU. Cur-
rently, the NNIS system does not receive reports from hospital-
wide surveillance, making comparisons to the non-ICU areas
impossible. Although this study involved data from only ICU
patients, its conclusions may be applicable to hospital-wide
data. This is because we evaluated the differences in reported
resistance rates within the same ICUs, and we suspect these
differences would be of similar magnitude and statistical sig-
nificance in the non-ICU areas. The major differences between
these patient groups in terms of resistance to antimicrobial
agents are higher severity of illness and higher rates of resistance
to antimicrobial agents [6]. With this lower prevalence of re-
sistance to antimicrobial agents in the non-ICU areas, we may
expect any observed differences in the prevalence by reporting
system in these hospital areas to be smaller than that observed
in our study. A second limitation of our study is the exclusion

328 • CID 2001:33 (1 August) • Fridkin et al.

of many ICUs from some analysis because !10 isolates of a
particular organism had been reported to NNIS-ICU during
the study period. This may reflect a very low hospital-acquired
infection rate overall or a paucity of infections caused by the
particular organism under study. Finally, our hypothesis was
tested in only select organisms and may not hold true for the
less frequently encountered pathogens. Those chosen reflect
pathogens thought to have the greatest clinical importance at
the inception of Project ICARE. However, comparisons of re-
sistance prevalence among other pathogens of clinical concern
(i.e., Acinetobacter species, S. pneumoniae) may not show sim-
ilar results to our study. For example, others have reported that
infections with MRSA that arise outside of the hospital setting
(i.e., community-onset MRSA) are frequently associated with
MRSA that is susceptible to clindamycin. This is in contrast to
the MRSA typically associated with hospital-acquired disease
[15–17].
These limitations do not detract from the observations that
differences between reporting systems were small and not clin-
ically relevant, and mostly insignificant. The findings of com-
parability of data from the 2 systems have several implications.
Analysis of these data supports the aggregation of cumulative
susceptibility data from both hospital-acquired infections and
other isolates, which may include isolates from community-
acquired infections, colonization, or contaminants, into one
summary report for use in guiding empiric therapy in hospi-
talized patients. Clinicians should be aware that the MRSA and
methicillin-resistant coagulase-negative staphylococci preva-
lence rates presented in such summary tables may underrep-
resent to a small degree their actual prevalence among path-
ogens associated with hospital-acquired infections. The small
magnitude of this difference means that it should rarely affect
decisions about drug choice. Therefore, producing one sum-
mary report should provide useful relevant data to the clinician
and minimize the need for additional efforts to produce more
detailed reports on subgroups. However, in some settings, re-
porting of separate cumulative susceptibility data from ICU
areas combined may be useful to clinicians [6]. Likewise, sep-
arate reports for specific patient populations (e.g., patients un-
dergoing dialysis or patients with cystic fibrosis) may be helpful
as well. Additional studies to identify effective methodologies
for providing clinicians with appropriate and valid decision
support will be crucial to improving appropriate use of and
reducing resistance to antimicrobial agents in health care
settings.
Acknowledgments
We thank the infection control, pharmacy, and microbiology
personnel from the participating ICARE hospitals of NNIS for
reporting the data for this study. In addition, we recognize the
contributions of Rachel Lawton, MPH, for coordinating the
submission and processing of data from the participating
hospitals.
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