Nej Mo A 1306801

The n e w e ng l a n d j o u r na l of m e dic i n e
original article
Multistate Point-Prevalence Survey of Health

CareAssociated Infections
Shelley S. Magill, M.D., Ph.D., Jonathan R. Edwards, M.Stat.,
Wendy Bamberg, M.D., Zintars G. Beldavs, M.S., Ghinwa Dumyati, M.D.,
Marion A. Kainer, M.B., B.S., M.P.H., Ruth Lynfield, M.D., Meghan Maloney, M.P.H.,
Laura McAllister-Hollod, M.P.H., Joelle Nadle, M.P.H., Susan M. Ray, M.D.,
Deborah L. Thompson, M.D., M.S.P.H., Lucy E. Wilson, M.D.,
and Scott K. Fridkin, M.D., for the Emerging Infections Program
Healthcare-Associated Infections and Antimicrobial Use Prevalence Survey Team*
A bs t r ac t
Background
From the Centers for Disease Control Currently, no single U.S. surveillance system can provide estimates of the burden of
and Prevention (S.S.M., J.R.E., L.M.-H., all types of health careassociated infections across acute care patient populations.
S.K.F.) and Emory University School of
Medicine (S.M.R.) both in Atlanta; We conducted a prevalence survey in 10 geographically diverse states to determine
Colorado Department of Public Health the prevalence of health careassociated infections in acute care hospitals and gen-
and Environment, Denver (W.B.); Ore- erate updated estimates of the national burden of such infections.
gon Public Health Authority, Portland
(Z.G.B.); New YorkRochester Emerging Methods
Infections Program and University of
We defined health careassociated infections with the use of National Healthcare
Rochester, Rochester (G.D.); Tennessee
Department of Health, Nashville (M.A.K.); Safety Network criteria. One-day surveys of randomly selected inpatients were performed
Minnesota Department of Health, St. Paul in participating hospitals. Hospital personnel collected demographic and limited
(R.L.); Connecticut Department of Public
clinical data. Trained data collectors reviewed medical records retrospectively to iden-
Health, Hartford (M.M.); California Emerg-
ing Infections Program, Oakland (J.N.); tify health careassociated infections active at the time of the survey. Survey data and
Georgia Emerging Infections Program 2010 Nationwide Inpatient Sample data, stratified according to patient age and length
and the Atlanta Veterans Affairs Medical
of hospital stay, were used to estimate the total numbers of health careassociated
Center, Decatur (S.M.R.); New Mexico De-
partment of Health, Santa Fe (D.L.T.); and infections and of inpatients with such infections in U.S. acute care hospitals in 2011.
Maryland Department of Health and Results
Mental Hygiene, Baltimore (L.E.W.). Ad-
dress reprint requests to Dr. Magill at the Surveys were conducted in 183 hospitals. Of 11,282 patients, 452 had 1 or more
Division of Healthcare Quality Promotion, health careassociated infections (4.0%; 95% confidence interval, 3.7 to 4.4). Of
Centers for Disease Control and Preven-
tion, 1600 Clifton Rd., MS A-24, Atlanta,
504 such infections, the most common types were pneumonia (21.8%), surgical-site
GA 30333, or at [email protected]. infections (21.8%), and gastrointestinal infections (17.1%). Clostridium difficile was
the most commonly reported pathogen (causing 12.1% of health careassociated
*A complete list of members of the
Emerging Infections Program Healthcare-
infections). Device-associated infections (i.e., central-catheterassociated bloodstream
Associated Infections and Antimicrobial infection, catheter-associated urinary tract infection, and ventilator-associated
Use Prevalence Survey Team is in the pneumonia), which have traditionally been the focus of programs to prevent health
Supplementary Appendix, available at
NEJM.org.
careassociated infections, accounted for 25.6% of such infections. We estimated
that there were 648,000 patients with 721,800 health careassociated infections in
N Engl J Med 2014;370:1198-208.
DOI: 10.1056/NEJMoa1306801
U.S. acute care hospitals in 2011.
Copyright 2014 Massachusetts Medical Society. Conclusions
Results of this multistate prevalence survey of health careassociated infections
indicate that public health surveillance and prevention activities should continue to
address C. difficile infections. As device- and procedure-associated infections de-
crease, consideration should be given to expanding surveillance and prevention
activities to include other health careassociated infections.
1198 n engl j med 370;13nejm.orgmarch 27, 2014
The New England Journal of Medicine

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Copyright 2014 Massachusetts Medical Society. All rights reserved.
Prevalence of Health CareAssociated Infections
E
limination of health careassoci- network of 10 state health departments (in Cali-
ated infections is a priority of the Depart- fornia, Colorado, Connecticut, Georgia, Maryland,
ment of Health and Human Services.1 Con- Minnesota, New Mexico, New York, Oregon, and
siderable success in prevention has been reported Tennessee) and academic partners. The current
for some infections, particularly central-catheter survey was also conducted with the EIP.
associated bloodstream infections.2-5 Continued Each EIP site was asked to recruit a total of
improvements in patient safety depend on main- up to 25 general and childrens acute care hospi-
taining a comprehensive understanding of the tals, with the following distribution according to
epidemiology of health careassociated infec- size, if possible: 13 small hospitals (<150 beds),
tions. Currently, no single U.S. surveillance sys- 9 medium-sized hospitals (150 to 399 beds), and
tem can provide estimates of the burden of all 3 large hospitals (400 beds). Eligible hospitals
types of such infections across acute care patient were randomly selected within each size stratum
populations. The most recent estimate produced to participate in a 1-day survey. When a selected
by the Centers for Disease Control and Preven- hospital declined to participate, an alternative
tion (CDC) and published in 2007 1.7 million hospital was used.
health careassociated infections per year re- The CDC determined the survey to be a public
lied on historical data combined with contempo- health surveillance activity. Institutional review
rary hospitalization data.6 The CDC surveillance boards at the state health departments, academic
system for health careassociated infections, the partners, and participating hospitals (where ap-
National Healthcare Safety Network (NHSN), plicable) reviewed the protocol and either deter-
provides information on incidence rates of com- mined that the survey did not constitute human-
mon infections. Most hospitals limit reporting to subjects research or approved the survey with a
device-associated infections, selected surgical-site waiver of the requirement for informed consent.
infections, and infections due to Clostridium diffi-
cile and methicillin-resistant Staphylococcus aureus Patient Selection
(MRSA). Therefore, the NHSN cannot provide Inpatients of any age in acute care hospitals were
national-scale data on the overall burden and eligible for inclusion. Patients in outpatient areas,
distribution of health careassociated infections emergency departments, and psychiatry, skilled
across acute care patient populations. nursing, and rehabilitation units were excluded.
To address this knowledge gap, the CDC be- Each hospital surveyed a random sample of eligi-
gan a three-phase effort in 2009 to develop and ble patients obtained from the morning census on
conduct a multistate prevalence survey of health the survey date: 100 patients in each large hospital
careassociated infections and use of antimicro- and 75 patients (or all eligible patients if <75) in
bial agents. Prevalence surveys have been used in each small or medium-sized hospital (for details,
other countries to describe the scope and mag- see the Supplementary Appendix, available with
nitude of the problem of such infections.7-30 The the full text of this article at NEJM.org).
CDC effort culminated in 2011 in a large-scale
survey that estimated the prevalence of health Training and Data Collection
careassociated infections in acute care hospi- Two teams collected data in each hospital: a pri-
tals, determined the distribution of these infec- mary team of infection preventionists and other
tions according to infection site and pathogen, personnel at the participating hospital and an
and generated updated estimates of the national EIP team of staff members from state health de-
burden of these infections. partments, academic partner institutions, or both.
Both teams received training in survey operations
Me thods and data-collection procedures; the EIP team also
received training in NHSN terms and definitions
for health careassociated infections.
Survey Design and Hospital Selection Primary teams reviewed medical records on
Survey methods were developed in two phases: a the survey date to collect demographic and lim-
single-city pilot in 200931 and a limited-rollout sur- ited clinical information, including whether pa-
vey in 2010 that was performed in collaboration tients were receiving or were scheduled to receive
with the Emerging Infections Programs (EIP), a antimicrobial drugs at the time of the survey.
n engl j med 370;13nejm.orgmarch 27, 2014 1199

Primary teams did not collect detailed anti Statistical Analysis

microbial data or identify health careassociated Data were analyzed with the use of SAS software,
infections. In some cases, EIP teams assisted with version 9.3 (SAS Institute), and OpenEpi software,
or performed the primary-team data collection. versions 2.3.1 and 3.01 (www.openepi.com). The
EIP teams reviewed medical records retrospec- mid-P exact method was used to generate confi-
tively to collect data on antimicrobial therapy and dence intervals for infection prevalence. Compar-
identify active health careassociated infections isons of patients with and those without health
with the use of NHSN surveillance definitions in careassociated infections were performed with
place at that time.32 EIP teams were instructed to the use of chi-square tests for categorical vari-
use only information present in the medical record ables and Wilcoxon rank-sum tests for continu-
on or before the survey date, including results of ous variables.
cultures collected or other testing performed on To generate estimates of the national burden of
or before the survey date. EIP teams used the health careassociated infections, we converted
NHSN definitions of gastrointestinal infections infection prevalence to incidence using the formula
for reporting C. difficile infection when possible; of Rhame and Sudderth33: I=P[LA(LNINT)],
in circumstances in which a patient with a posi- where I denotes incidence, P prevalence, LA the
tive test result for C. difficile infection did not mean length of hospitalization for all patients,
meet the NHSN gastrointestinal definitions, EIP LN the mean length of hospitalization for patients
teams used a prevalence surveyspecific definition who acquired one or more health careassociated
of C. difficile infection (described in the Supple- infections, and INT the mean interval between
mentary Appendix). admission and the onset of the first such infection.
On the basis of pilot data31 and unpublished Numbers of patients with health careassociated
data showing that antimicrobial therapy is a sensi- infections were obtained by multiplying infec-
tive proxy indicator for health careassociated tion incidence by numbers of U.S. hospital dis-
infections (sensitivity, 95 to 100%), EIP teams re- charges, obtained from the 2010 Nationwide
viewed records for active health careassociated Inpatient Sample (NIS).34 This database of hos-
infections only for those patients who were re- pitalizations from a sample of U.S. community
ceiving antimicrobial agents for the treatment of hospitals was developed as part of the Healthcare
active infections or for no documented reason. Cost and Utilization Project of the Agency for
Additional information on the use of data on Healthcare Research and Quality; discharge
antimicrobial therapy to identify patients with weighting allows national estimates to be gener-
active infections is presented in the Supplemen- ated from the sample.
tary Appendix (Methods section and Fig. S1). We sought to improve the precision of the
Active health careassociated infections were burden-estimation process by performing log-
defined as infections not present or incubating binomial regression modeling to identify factors
on admission to the survey hospital (with cer- significantly associated with the prevalence of
tain exceptions, noted below) that met NHSN health careassociated infections. Through a pro-
surveillance definition criteria, with signs or cess described in the Supplementary Appendix,
symptoms of infection present on the survey the results of regression modeling were used to
date or with antimicrobial therapy still being create multiple strata based on patient age and a
given on the survey date. Infections present on proxy measure of the length of the hospital stay.
admission to the survey hospital were consid- Within each stratum, the predicted prevalence of
ered health careassociated infections if they were health careassociated infections was converted
surgical-site infections related to surgery per- to incidence with the use of the median length
formed at the survey hospital within the preced- of the hospital stay for surveyed patients for
ing 30 days (or within 1 year if an implant was whom such information was available (LA in the
in place), C. difficile infections related to a previous formula of Rhame and Sudderth), the median
stay in the survey hospital within 28 days before length of hospital stay for patients with health
specimen collection, or infections related to a careassociated infections (LN), and the median
prior hospitalization in the survey hospital within interval from admission to the onset of the first
the preceding 48 hours. health careassociated infection (INT). Median

rather than mean values were used owing to a survey (Table 1, and Fig. S1 in the Supplemen-
skewed distribution. The incidence in each stra- tary Appendix).
tum of age and length of stay was multiplied by
the total number of U.S. discharges in that stra- Prevalence and Distribution of Health Care
tum (with the use of weighted discharge data Associated Infections
from the NIS), under the assumption that each The medical records of 4504 patients (39.9%)
discharge represented a unique patient, to get those receiving antimicrobial agents for treatment
stratum-specific numbers of patients with health of active infections or for no documented reason
careassociated infections. These stratum-specific were reviewed for health careassociated in-
numbers were summed to obtain an estimate of fections (Fig. S1 in the Supplementary Appendix).
the total number of inpatients with health care A total of 504 such infections were detected in 452
associated infections in U.S. acute care hospitals of 11,282 patients; therefore, 4.0% of patients had
in 2011. Because our estimates of the median at least 1 health careassociated infection (95%
length of the hospital stay for all patients were confidence interval [CI], 3.7 to 4.4). Pneumonia
based on data from patients receiving antimicro- and surgical-site infection were most common,
bial therapy, who may have had a longer median followed by gastrointestinal infection, urinary
length of stay than patients not receiving such tract infection, and primary bloodstream infec-
therapy, we also performed the burden-estimation tion (Table 2). In addition to 50 primary blood
process using data from the NIS for the median stream infections, there were 37 secondary blood-
length of the hospital stay for all patients in the stream infections. Device-associated infections
formula of Rhame and Sudderth. (i.e., ventilator-associated pneumonia, catheter-
Burden estimates for major types of health associated urinary tract infection, and central-
careassociated infection were generated by mul- catheterassociated bloodstream infection) ac-
tiplying the proportion of surveyed patients with counted for 25.6% of all health careassociated
each infection type by the estimated total number infections; together, device-associated infections
of patients with health careassociated infec- and surgical-site infections (21.8%) accounted
tions. The numbers of each major type of infec- for 47.4% of all health careassociated infections
tion were summed to obtain an estimate of the (239 of 504 infections). The remaining 52.6% of
total number of inpatient health careassociated infections were not associated with devices or
infections in U.S. acute care hospitals in 2011. operative procedures.
Overall, 169 of 394 nonsurgical-site infections
R e sult s (42.9%) developed during or within 48 hours after
a stay in a critical care unit; 167 (42.4%) devel-
Hospitals and Patients oped during or within 48 hours after a stay in a
A total of 183 hospitals (79% of the goal of non-nursery ward. The NHSN operative-procedure
232hospitals) participated (Table S1 in the Sup- types associated with the most surgical-site in-
plementary Appendix). Of the 183 hospitals, 93 fections were colon surgeries (accounting for 16
(51%) were small, 68 (37%) were medium-sized, of 110 surgical-site infections [14.5%]), hip arthro-
and 22 (12%) were large proportions that plasties (11 [10.0%]), and small-bowel surgeries
were similar to those for all 406 hospitals in the (7 [6.4%]). Ten surgical-site infections (9.1%) were
10 EIP sites (55% small, 35% medium-sized, and attributed to other, unspecified procedures.
10% large). The median interval from hospital admission to
Overall, 11,290 patients were included in sur- the onset of symptoms of a health careassociated
veys performed between May and September 2011; infection was 6 days (interquartile range, 2 to 13)
data collection was completed for 11,282 patients among 494 patients for whom symptom-onset
(99.9%). The median patient age was 58 years dates were reported. Overall, 98 health care
(interquartile range, 32 to 74). Most patients associated infections (19.4%) were present on
(71.2%) were in non-nursery wards; 15.1% were admission and were therefore related to a previ-
in critical care units. Approximately 51.9% of ous admission to the same hospital. Most infec-
patients were receiving or were scheduled to re- tions present on admission were surgical-site
ceive antimicrobial agents at the time of the infections (66 [67.3%]) and gastrointestinal in-

fections (9 [9.2%]). The outcome was known for Pathogens Causing Health CareAssociated
436 of the 452 patients with health careassociated Infections
infections (96.5%). Fifty of these 436 patients A total of 481 pathogens were reported for 372 of
(11.5%) died during their survey hospitalization. 504 health careassociated infections (73.8%).
Table 1. Demographic and Clinical Characteristics of Surveyed Patients.*
Patients without Patients with

Health Care Health Care
Associated Associated
All Patients Infections Infections P
Characteristic (N=11,282) (N=10,830) (N=452) Value
Sex no. (%) 0.13
Male 5,034 (44.6) 4,813 (44.4) 221 (48.9)
Female 6,236 (55.3) 6,006 (55.5) 230 (50.9)
Missing data 12 (0.1) 11 (0.1) 1 (0.2)
Age no. (%) 0.09
<1 yr 1,151 (10.2) 1,115 (10.3) 36 (8.0)
117 yr 479 (4.2) 460 (4.2) 19 (4.2)
1824 yr 462 (4.1) 448 (4.1) 14 (3.1)
2544 yr 1,686 (14.9) 1,634 (15.1) 52 (11.5)
4564 yr 3,060 (27.1) 2,927 (27.0) 133 (29.4)
6584 yr 3,429 (30.4) 3,269 (30.2) 160 (35.4)
85 yr 1,014 (9.0) 976 (9.0) 38 (8.4)
Missing data 1 (<0.1) 1 (<0.1) 0
Race or ethnic group no. (%) 0.09
American Indian or Alaska Native 119 (1.1) 117 (1.1) 2 (0.4)
Asian 254 (2.3) 244 (2.3) 10 (2.2)
Black 1,905 (16.9) 1,809 (16.7) 96 (21.2)
Multiple races or other unspecified race 254 (2.3) 244 (2.3) 10 (2.2)
Native Hawaiian or other Pacific Islander 20 (0.2) 18 (0.2) 2 (0.4)
White 7,537 (66.8) 7,244 (66.9) 293 (64.8)
Missing data 1,193 (10.6) 1,154 (10.7) 39 (8.6)
Hispanic or Latino ethnic group no. (%) 0.04
Hispanic or Latino 846 (7.5) 826 (7.6) 20 (4.4)
Not Hispanic or Latino 3,715 (32.9) 3,564 (32.9) 151 (33.4)
Missing data 6,721 (59.6) 6,440 (59.5) 281 (62.2)
Hospital size no. (%) <0.001
Small 4,073 (36.1) 3,964 (36.6) 109 (24.1)
Medium 4,995 (44.3) 4,794 (44.3) 201 (44.5)
Large 2,214 (19.6) 2,072 (19.1) 142 (31.4)
Location of patient in hospital on survey date no. (%) <0.001
Critical care unit 1,707 (15.1) 1,551 (14.3) 156 (34.5)
Mixed acuity unit 119 (1.1) 114 (1.1) 5 (1.1)
Newborn or special care nursery 485 (4.3) 482 (4.5) 3 (0.7)
Specialty care area 469 (4.2) 439 (4.1) 30 (6.6)
Step-down unit 466 (4.1) 443 (4.1) 23 (5.1)
Ward, not nursery 8,036 (71.2) 7,801 (72.0) 235 (52.0)

Table 1. (Continued.)
Patients without Patients with

Health Care Health Care
Associated Associated
All Patients Infections Infections P
Characteristic (N=11,282) (N=10,830) (N=452) Value
Central catheter in place on survey date no. (%)
Any 2,121 (18.8) 1,862 (17.2) 259 (57.3) <0.001
Femoral 54 (0.5) 44 (0.4) 10 (2.2)
Peripherally inserted 1,037 (9.2) 878 (8.1) 159 (35.2)
Other known type 1,057 (9.4) 958 (8.8) 99 (21.9)
Unknown type 32 (0.3) 29 (0.3) 3 (0.7)
None 9,140 (81.0) 8,948 (82.6) 192 (42.5)
Missing data 21 (0.2) 20 (0.2) 1 (0.2)
Urinary catheter in place on survey date no. (%) <0.001
Yes 2,659 (23.6) 2,482 (22.9) 177 (39.2)
No 8,594 (76.2) 8,321 (76.8) 273 (60.4)
Missing data 29 (0.3) 27 (0.2) 2 (0.4)
Patient receiving mechanical ventilatory support on survey date <0.001
no. (%)
Yes 527 (4.7) 432 (4.0) 95 (21.0)
No 10,748 (95.3) 10,391 (95.9) 357 (79.0)
Missing data 7 (0.1) 7 (0.1) 0
Patient receiving or scheduled to receive antimicrobial therapy 5,860 (51.9) 5,408 (49.9) 452 (100)
at time of survey no. (%)**
Patient receiving dialysis at time of survey no. (%) 446 (4.0) 410 (3.8) 36 (8.0) <0.001
Interval from admission to survey days
Median 3 2 12 <0.001
Interquartile range 16 15 723
* Percentages may not add up to 100 because of rounding.

P values were calculated with the use of the chi-square test, except where indicated.
Race and ethnic group were determined on the basis of medical-record documentation.
Small hospitals had fewer than 150 beds, medium-sized hospitals had 150 to 399 beds, and large hospitals had 400 or more beds.
Hospital units were defined according to the National Healthcare Safety Network classification. Critical care units included level IIIII and
level III neonatal intensive care units.
Patients could have more than one type of central catheter.
** For four patients without health careassociated infections, information on antimicrobial therapy was not available on the survey date;
medical records of these patients were reviewed retrospectively to collect data on antimicrobial therapy and health careassociated infec-
tions. By definition, all patients with health careassociated infections were receiving antimicrobial agents at the time of the survey.
The P value was calculated with the use of the Wilcoxon rank-sum test.
C.difficile was the most common pathogen, causinglonger at the time of the survey, were in a large
61 health careassociated infections (12.1%) (Ta- hospital, had a central catheter in place, were re-
ble 3). S. aureus was the second most common ceiving mechanical ventilatory support, or were in
pathogen (54 infections [10.7%]), followed by a critical care unit had an increased risk of health
careassociated infection (Table S2 in the Supple-
Klebsiella pneumoniae and K. oxytoca (50 infections
mentary Appendix). The total estimated number
[9.9%]) and Escherichia coli (47 infections [9.3%])
(Table 3). of patients with at least 1 health careassociated
infection in 2011 was 648,000 (95% CI, 246,400 to
Risk Factors for Health CareAssociated 987,300). The use of data on the median length
Infections and Overall U.S. Burden of the hospital stay from the NIS in the burden-
Multivariable regression analysis showed that pa- estimation process, in place of data on the length
tients who were older, had been in the hospital of stay from surveyed patients receiving anti

microbial therapy, did not substantially change stays. The current estimates of the overall burden
the overall burden estimate (582,000 infections; are lower than older estimates, such as those
95% CI, 216,600 to 875,400). Estimated numbers from the Study on the Efficacy of Nosocomial
of selected major types of health careassociated Infection Control in the 1970s (2.1 million infec-
infection are shown in Table 4; summing the tions)36 and those from analyses of National
estimates for each of the 13 major types shown Nosocomial Infections Surveillance system data
in Table 2 yielded an overall total estimate of collected from 1990 through 2002 (1.7 million in-
721,800 infections (95% CI, 214,700 to 1,411,000). fections),6 although it is difficult to draw conclu-
sions from these comparisons because of the
Discussion differences in patient populations, surveillance
definitions of health careassociated infections,
In this survey, 4.0% of inpatients in U.S. acute care and data-collection and analytical methods among
hospitals had at least 1 health careassociated these CDC efforts.31
infection, yielding an estimate of 648,000 inpa- Device-associated infections, which have been
tients with a total of approximately 721,800 such a major focus of infection prevention in recent
infections in 2011. These estimates of the national decades, accounted for only 25.6% of all health
burden of health careassociated infections in careassociated infections detected in the current
acute care hospitals were generated through the survey. Infections not associated with devices or
use of a modeling process that accounted for se- operative procedures including C. difficile infec-
lected predictors of infection prevalence, includ- tions and other gastrointestinal infections and
ing age and length of stay, and application of the nonventilator-associated pneumonia accounted
results of this modeling to the NIS, a nationally for approximately half of all health careassoci-
representative sample of U.S. community-hospital ated infections in the survey. This finding should
expand the public health focus to include these
other types of infections, identifying patients at
Table 2. Distribution of 504 Health CareAssociated Infections.* risk and developing effective prevention measures.
Percentage of All An example is the recent focus of the CDC on sur-
Health Care veillance and prevention of C. difficile infections.37
Associated Gastrointestinal infections, 70.9% of which
No. of Infections
Type of Infection Rank Infections (95% CI) were C. difficile infections, were the third most
common type of health careassociated infection
Pneumonia 1 (tie) 110 21.8 (18.425.6)
in this survey, in contrast to the results of previ-
Surgical-site infection 1 (tie) 110 21.8 (18.425.6)
ous analyses.6,36 Although there is ample evi-
Gastrointestinal infection 3 86 17.1 (14.020.5) dence to support our finding that C. difficile in-
Urinary tract infection 4 65 12.9 (10.216.0) fections are a major contributor to the overall
Primary bloodstream infection 5 50 9.9 (7.512.8) U.S. burden of health careassociated infections
Eye, ear, nose, throat, or mouth 6 28 5.6 (3.87.8) in acute care hospitals,38-41 the high prevalence
infection of C. difficile infections in this survey may be
Lower respiratory tract infection 7 20 4.0 (2.56.0) partially explained by the use of a sensitive defi-
Skin and soft-tissue infection 8 16 3.2 (1.95.0) nition. This definition, as opposed to the more
restrictive NHSN surveillance definitions of gas-
Cardiovascular system infection 9 6 1.2 (0.52.5)
trointestinal infections, was used for reporting
Bone and joint infection 10 5 1.0 (0.42.2)
31 of the 61 cases of C. difficile infection (51%) de-
Central nervous system infection 11 4 0.8 (0.31.9) tected in the survey. It is also likely that nucleic
Reproductive tract infection 12 3 0.6 (0.21.6) acid amplification testing for diagnosis of C.diffi-
Systemic infection 13 1 0.2 (0.011.0) cile infection was used in some participating fa-
cilities, resulting in increased case detection.42
* Infections were defined with the use of National Healthcare Safety Network This survey has important limitations that
criteria. CI denotes confidence interval.
A total of 43 pneumonia events (39.1%) were associated with a mechanical must be considered. First, although we are con-
ventilator. fident that the survey hospitals are representa-
A total of 44 urinary tract infections (67.7%) were associated with a catheter. tive of hospitals within the EIP catchment areas,
A total of 42 primary bloodstream infections (84.0%) were associated with a
central catheter. they may not be representative of all U.S. acute
care hospitals. Only 183 hospitals and 11,282 pa-

Table 3. Reported Causative Pathogens, According to Type of Infection.*
All Health
Care
Associated Surgical-Site GI Bloodstream
Infections Pneumonia Infections Infections UTIs Infections
Pathogen (N=504) (N=110) (N=110) (N=86) (N=65) (N=50)
no. (%) rank number (percent)
Clostridium difficile 61 (12.1) 1 0 0 61 (70.9) 0 0
Staphylococcus aureus 54 (10.7) 2 18 (16.4) 17 (15.5) 1 (1.2) 2 (3.1) 7 (14.0)
Klebsiella pneumoniae or K. oxytoca 50 (9.9) 3 13 (11.8) 15 (13.6) 1 (1.2) 15 (23.1) 4 (8.0)
Escherichia coli 47 (9.3) 4 3 (2.7) 14 (12.7) 1 (1.2) 18 (27.7) 5 (10.0)
Enterococcus species 44 (8.7) 5 2 (1.8) 16 (14.5) 5 (5.8) 11 (16.9) 6 (12.0)
Pseudomonas aeruginosa 36 (7.1) 6 14 (12.7) 7 (6.4) 1 (1.2) 7 (10.8) 2 (4.0)
Candida species 32 (6.3) 7 4 (3.6) 3 (2.7) 3 (3.5) 3 (4.6) 11 (22.0)
Streptococcus species 25 (5.0) 8 7 (6.4) 8 (7.3) 2 (2.3) 2 (3.1) 2 (4.0)
Coagulase-negative staphylococcus 24 (4.8) 9 0 7 (6.4) 0 1 (1.5) 9 (18.0)
species
Enterobacter species 16 (3.2) 10 3 (2.7) 5 (4.5) 0 2 (3.1) 2 (4.0)
Acinetobacter baumannii 8 (1.6) 11, tie 4 (3.6) 2 (1.8) 0 0 0
Proteus mirabilis 8 (1.6) 11, tie 1 (0.9) 5 (4.5) 0 1 (1.5) 0
Yeast, unspecified 8 (1.6) 11, tie 3 (2.7) 0 1 (1.2) 4 (6.2) 0
Stenotrophomonas maltophilia 8 (1.6) 11, tie 6 (5.5) 0 0 2 (3.1) 0
Citrobacter species 6 (1.2) 15, tie 2 (1.8) 1 (0.9) 0 1 (1.5) 0
Serratia species 6 (1.2) 15, tie 2 (1.8) 0 0 2 (3.1) 0
Bacteroides species 6 (1.2) 15, tie 0 5 (4.5) 1 (1.2) 0 0
Haemophilus species 6 (1.2) 15, tie 2 (1.8) 2 (1.8) 0 0 0
Viruses 3 (0.6) 19, tie 1 (0.9) 0 0 0 0
Peptostreptococcus species 3 (0.6) 19, tie 0 2 (1.8) 0 0 1 (2.0)
Klebsiella species other than 2 (0.4) 21, tie 1 (0.9) 0 0 0 1 (2.0)
K.pneumoniae and K. oxytoca
Clostridium species other than 2 (0.4) 21, tie 0 2 (1.8) 0 0 0
C.difficile
Prevotella species 2 (0.4) 21, tie 0 1 (0.9) 0 0 0
Morganella morganii 2 (0.4) 21, tie 0 1 (0.9) 0 1 (1.5) 0
Lactobacillus species 2 (0.4) 21, tie 0 0 1 (1.2) 0 1 (2.0)
Other organisms** 13 (2.6) 1 (0.9) 6 (5.5) 0 1 (1.5) 3 (6.0)
* One or more pathogens were reported for 372 of 504 infections (73.8%). No pathogens were reported for the remaining 132 infections
(26.2%).
Values for all health careassociated infections include those for the 13 major types of infection listed in Table 2.
Enterococcus species include E. faecalis (23 infections), E. faecium (8), other or unspecified enterococci (11), E. faecalis and E. faecium (1),
and E. faecalis and E. avium (1).
Candida species include C. albicans (18 infections), C. parapsilosis (6), C. glabrata (4), other or unspecified candida species (2), and C. albi-
cans and C. dubliniensis (2).
Streptococcus species include S. pneumoniae (7 infections), viridans streptococci (7), group B streptococci (3), other or unspecified strep-
tococci (7), and group G streptococci and S. parasanguis (1).
Viruses include adenovirus (1 infection), herpes simplex virus (1), and parainfluenza virus (1).
** Other organisms include Achromobacter xylosoxidans (1 infection), Aeromonas hydrophila (1), aspergillus species (1), bacillus species (1),
Finegoldia magna (1), fusobacterium species (1), Moraxella catarrhalis (1), propionibacterium species (1), Pseudomonas alcaligenes (1),
Rothia mucilaginosa (1), unspecified gram-negative rods (2), and Acinetobacter lwoffii and micrococcus species (1).
tients were included, of a total of approximately States.43 Second, because our survey was limited
5000 U.S. community hospitals and 34 million to acute care hospitals, we cannot estimate the
annual admissions (2012 data) in the United numbers of health careassociated infections

occurring in other settings, such as skilled nurs- team identified similar proportions of patients
ing facilities. Third, we were not able to validate with health careassociated infections overall,
data across the 10 EIP sites. Data evaluations although there were many discrepancies in pa-
were performed in the previous two phases of tient-level determinations of such an infection.31
survey development; the results showed that the Additional limitations are discussed in the Sup-
primary data-collection team and the evaluation plementary Appendix.
Table 4. Estimated Numbers of Major Types of Health CareAssociated Infection in the United States in 2011.
Surveyed
Infections Patients
Identified with Type of Estimated Infections
Type of Infection in Survey Infection in the United States*
no. % (95% CI) no. (95% CI)
All health careassociated infections
Pneumonia 110 24.3 (20.628.5) 157,500 (50,800281,400)
Surgical-site infection 110 24.3 (20.628.5) 157,500 (50,800281,400)
Gastrointestinal infection 86 19.0 (15.622.8) 123,100 (38,400225,100)
Urinary tract infection 65 14.4 (11.417.9) 93,300 (28,100176,700)
Primary bloodstream infection 50 11.1 (8.414.2) 71,900 (20,700140,200)
Eye, ear, nose, throat, or mouth infection 28 6.2 (4.28.7) 40,200 (10,40085,900)
Lower respiratory tract infection 20 4.4 (2.86.6) 28,500 (690065,200)
Skin and soft-tissue infection 16 3.5 (2.15.6) 22,700 (520055,300)
Cardiovascular system infection 6 1.3 (0.52.7) 8,400 (120026,700)
Bone and joint infection 5 1.1 (0.42.4) 7,100 (100023,700)
Central nervous system infection 4 0.9 (0.32.1) 5,800 (70020,700)
Reproductive tract infection 3 0.7 (0.21.8) 4,500 (50017,800)
Systemic infection 1 0.2 (0.011.1) 1,300 (010,900)
Total 721,800 (214,7001,411,000)
Infections in non-neonatal intensive care units
Catheter-associated urinary tract infection 25 5.5 (3.77.9) 35,600 (910078,000)
Central-catheterassociated primary bloodstream infection 11 2.4 (1.34.2) 15,600 (320041,500)
Ventilator-associated pneumonia 35 7.7 (5.510.5) 49,900 (13,600103,700)
Surgical-site infections attributed to Surgical Care Improvement 46 10.2 (7.613.2) 66,100 (18,700130,300)
Project procedures
Hospital-onset infections caused by specific pathogens
Clostridium difficile infection 56 12.4 (9.615.7) 80,400 (23,700155,000)
MRSA bacteremia 7 1.5 (0.73.0) 9,700 (170029,600)
* Estimates are based on an overall estimate of 648,000 patients (95% CI, 246,400 to 987,300) with at least one health careassociated infec-
tion in 2011. To calculate the numbers of estimated infections, the point estimate of the percentage of patients with a particular type of in-
fection (e.g., 24.3% for pneumonia) was multiplied by the point estimate of the overall number of patients with health careassociated in-
fections. To calculate the 95% CIs, the lower bound of the 95% CI for the percentage of patients with a particular type of infection (e.g.,
20.6% for pneumonia) was multiplied by the lower bound of the 95% CI for the overall number of patients with health careassociated in-
fections, and the upper bound of the 95% CI for the percentage of patients with a particular type of infection (e.g., 28.5% for pneumonia)
was multiplied by the upper bound of the 95% CI for the overall number of patients with health careassociated infections.
There were 110 surgical-site infections in 109 patients. For the purposes of estimating the total number of such infections in the United
States in 2011, we assumed that each of the 110 infections occurred in a unique patient.
There were 28 eye, ear, nose, throat, or mouth infections in 27 patients. For the purposes of estimating the total number of such infections
in the United States in 2011, we assumed that each of the 28 infections occurred in a unique patient.
Surgical Care Improvement Project procedures included those with the following National Healthcare Safety Network procedure codes:
CARD, CBGB, CBGC, AAA, CEA, PVBY, COLO, REC, HYST, VHYS, HPRO, and KPRO.35
C. difficile infection was defined by an onset of symptoms on or after the third day of hospitalization (with the day of admission counted as the first day).
Methicillin-resistant Staphylococcus aureus (MRSA) bacteremia was defined as primary or secondary MRSA bloodstream infection with an
onset of symptoms on or after the third day of hospitalization (with the first day of admission counted as the first day).

Despite these limitations, the national esti- one health careassociated infection. Pneumonia
mates that we generated for selected types of and surgical-site infection were the most common
health careassociated infection are remarkably infection types, and C. difficile was the most com-
similar to estimates from other data sources. mon pathogen. Infections other than those asso-
For example, we estimated that 15,600 central- ciated with central catheters, urinary catheters,
catheterassociated bloodstream infections oc- and ventilators account for the majority of the
curred in 2011 (not including such infections in U.S. burden of health careassociated infections
neonatal intensive care units), and NHSN data and may warrant increased attention. A better
yielded an estimate of 12,400.35 Our estimate of understanding of trends in the epidemiology of
9700 hospital-onset cases of MRSA bacteremia health careassociated infections and prevention
is similar to that obtained from EIP popula- success may be achieved through repeated prev-
tion-based surveillance, in which 71.3% of the alence surveys in which similar methods are used
estimated 14,156 invasive, hospital-onset MRSA each time.
infections, or 10,093 infections, involved bacte- The findings and conclusions in this report are those of the
remia.44 Finally, we estimated that there were authors and do not necessarily represent the official position of
66,100 Surgical Care Improvement Project proce- the Centers for Disease Control and Prevention (CDC) or the
Agency for Toxic Substances and Disease Registry.
dure-associated surgical-site infections, as com- Dr. Kainer reports receiving consulting, lecture, and board mem-
pared with the NHSN estimate of 52,567.35 The bership fees from and owning stock in the Infectious Disease Con-
similarity of these estimates from different data sulting Corporation. Dr. Lynfield reports receiving travel support
from Parexel. No other potential conflict of interest relevant to this
sources bolsters our confidence in the overall article was reported.
estimates of health careassociated infections Disclosure forms provided by the authors are available with
that we have generated, as well as our estimates the full text of this article at NEJM.org.
We thank the staff of each hospital that participated in
of infections for which other data sources do not phases 2 and 3 of the Emerging Infections Program (EIP)
currently exist. Healthcare-Associated Infections and Antimicrobial Use Prev-
In summary, our survey results indicate that alence Survey, our colleagues in the EIP sites and at the CDC
who contributed to this effort (listed in the Supplementary Ap-
on any given day approximately 1 of every 25 in- pendix), and the Healthcare Cost and Utilization Project Data
patients in U.S. acute care hospitals has at least Partners (www.hcup-us.ahrq.gov/db/hcupdatapartners.jsp).
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The n e w e ng l a n d j o u r na l of m e dic i n e

Multistate Point-Prevalence Survey of Health

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The New England Journal of Medicine

n engl j med 370;13nejm.orgmarch 27, 2014 1199

Primary teams did not collect detailed anti Statistical Analysis

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Table 1. Demographic and Clinical Characteristics of Surveyed Patients.*

Patients without Patients with

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Patients without Patients with

* Percentages may not add up to 100 because of rounding.

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Table 3. Reported Causative Pathogens, According to Type of Infection.*

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my nejm in the journal online

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The New England Journal of Medicine

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