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original article
objective. To estimate the proportion of healthcare-associated infections (HAIs) in US hospitals that are reasonably preventable,
along with their related mortality and costs.
methods. To estimate preventability of catheter-associated bloodstream infections (CABSIs), catheter-associated urinary tract infections
(CAUTIs), surgical site infections (SSIs), and ventilator-associated pneumonia (VAP), we used a federally sponsored systematic review of
interventions to reduce HAIs. Ranges of preventability included the lowest and highest risk reductions reported by US studies of moderate
to good quality published in the last 10 years. We used the most recently published national data to determine the annual incidence of
HAIs and associated mortality. To estimate incremental cost of HAIs, we performed a systematic review, which included costs from studies
in general US patient populations. To calculate ranges for the annual number of preventable infections and deaths and annual costs, we
multiplied our infection, mortality, and cost figures with our ranges of preventability for each HAI.
results. As many as 65%70% of cases of CABSI and CAUTI and 55% of cases of VAP and SSI may be preventable with current
evidence-based strategies. CAUTI may be the most preventable HAI. CABSI has the highest number of preventable deaths, followed by
VAP. CABSI also has the highest cost impact; costs due to preventable cases of VAP, CAUTI, and SSI are likely less.
conclusions. Our findings suggest that 100% prevention of HAIs may not be attainable with current evidence-based prevention
strategies; however, comprehensive implementation of such strategies could prevent hundreds of thousands of HAIs and save tens of
thousands of lives and billions of dollars.
Infect Control Hosp Epidemiol 2011;32(2):101-114
CABSI, CAUTI, and SSI. VAP is being considered for inclusion in an expanded list scheduled for release in 2011.6
Although nonpayment for treatment of HAIs may be an
effective incentive for hospitals and physicians to reduce the
incidence of HAIs, some have asserted that not all HAIs are
preventable and that this new incentive may be a challenge
for hospitals that care for patients at high risk for HAIs.5,6 To
inform discussions regarding the preventability of HAIs, we
estimated the proportion of HAIs that are reasonably preventable in US hospitals, as well as their associated mortality
rates and costs.
methods
HAI Incidence, Associated Mortality, and Risk Reduction
An accurate estimation of the annual number of preventable
HAIs requires accurate estimates of 2 underlying values: the
current total annual number of HAIs and the proportion of
Affiliations: 1. Center for Evidence-Based Practice, University of Pennsylvania, Philadelphia, Pennsylvania; 2. Center for Clinical Epidemiology and
Biostatistics, University of Pennsylvania, Philadelphia, Pennsylvania; 3. Department of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania;
4. Office of the Chief Medical Officer, University of Pennsylvania, Philadelphia, Pennsylvania.
Received May 12, 2010; accepted August 10, 2010; electronically published January 14, 2011.
2011 by the Society for Healthcare Epidemiology of America. All rights reserved. 0899-823X/2011/3202-0001$15.00. DOI: 10.1086/657912
102
results
Number of HAIs and Associated Mortality
A comprehensive estimate of annual incidence of the mortality rates associated with HAIs in US hospitals was reported
in 2007 (Appendix Table A1).2 These data suggest that CABSI
and VAP cause more than two-thirds of the deaths resulting
from HAIs and that they are 5 times as deadly as the other
HAIs.
103
Intervention
Intervention period: 0
cases per 1,000 CDs;
control period: 1.6
cases per 1,000 CDs
4.51 cases per 1,000 CDs 2.92 cases per 1,000 CDs
10.8 cases per 1,000 CDs 3.7 cases per 1,000 CDs
Intervention period:
11.3 cases per 1,000
CDs; control period:
5.7 cases per 1,000
CDs
After intervention
table 1. Summaries of Studies of Prevention of Healthcare-Associated Infections Included in the Present Analysis
35%
66%
57%
42%
18%
28%b
66%a
Reduction
Before-after study;
ICU patients
Before-after study;
ICU patients
Before-after study;
ICU patients
Before-after study;
type of patients
not reported
Preventive: Appropriate use of perioperative antibiotics; decreased use of preoperative shaving; improvement in perioperative glucose control
QI: Audit and feedback; clinician education; clinician reminder
Preventive: Improvement in perioperative
glucose control
QI: Audit and feedback; clinician education; patient education
Preventive: Appropriate use of perioperative antibiotics; decreased use of preoperative shaving; improvement in perioperative glucose control
QI: Clinician education, clinician reminder
2.1%
7.58%
2.3%
1.5%
3.47%
1.7%
Preventive: Hand hygiene; head of bed an- 8.75 cases per 1,000 VDs 4.74 cases per 1,000 VDs
gle 130; daily interruption of sedation
QI: Clinician education
Preventive: Head of bed angle 130
12.6 cases per 1,000 VDs 5.7 cases per 1,000 VDs
QI: Clinician education
29%
54%
26%
SICU: 17%;
MICU: 29%;
CICU: 45%
69%
SICU: 38%;
MICU: 48%
55%
46%
note. CABSI, catheter-associated bloodstream infection; CAUTI, catheter-associated urinary tract infection; CD, catheter-day; ICU, intensive care unit; CICU, cardiology ICU;
MICU, medical ICU; QI, quality initiative; SICU, surgical ICU; SSI, surgical site infection; VAP, ventilator-associated pneumonia; VD, ventilator-day.
a
Reported risk reduction resulting from interrupted time-series modeling.
b
Risk reduction calculated by taking the difference between the risk reductions of the intervention arm and the control arm.
Before-after study;
type of patients
not reported
Before-after study;
type of patients
not reported
Before-after study;
ICU patients
St. Louis, MO
Surgical and medical ICU
41
Primary
Cost identification
By infection control team using CDC
criteria
Cost identification
Not reported
Warren et al11
Pittsburgh, PA
Medical and coronary ICU
54
Primary
Shannon et al10
Baltimore, MD
Surgical ICU
86
Primary
Dimick et al12
Ann Arbor, MI
Medical ICU
68
Secondary
DiGiovine et al8
note. Costs were converted to 2009 dollars using the Consumer Price Index (CPI) for Hospital Services (US Bureau of Labor Statistics), except for DiGiovine et al,8 for which costs were converted
using the CPI for Medical Services, since the hospital index was not calculated before 1997. APACHE II, Acute Physiology and Chronic Health Evaluation II; CD, catheter-day; CDC, Centers for Disease
Control and Prevention; CFU, colony-forming unit; CI, confidence interval; ICU, intensive care unit; LOS, length of stay; SD, standard deviation; VD, ventilator-day.
a
No. of patients with infection; excludes matched control subjects.
Cost identification
Cost identification
Colonization of catheter (115 CFU) By infection control team using
with organism found in periphCDC criteria
eral blood specimen
Control group
None
ICU patients without infection
ICU patients without infection
Matched control subjects; matching
based on predicted mortality,
sex, age, race, admitting diagnosis, and chronic health
Method of determining cost
Clinicians retrospective review of charts,
Multiple linear regression model
Multiple linear regression model
By LOS and by total direct costs;
bills, and payments
which costs were reported is not
stated
Source of cost data (baseline year) Hospital cost reports, 20022005 dollars
Hospital cost accounting database, 2000 Hospital charges converted to costs, Hospital cost accounting database,
dollars
1998 dollars
19941996 dollars
Costs measured
Line item costs of care attributable to CABSI All costs in hospital accounting database, All costs in hospital billing database; Cost analysis methods ambiguous;
(eg, additional hospital days, antibiotics,
including overhead costs
overhead costs not reported
it appears that only direct costs
and tests) and/or its complications (eg,
for ICU care were considered
exploratory laparotomy, hemodialysis)
Perspective
Hospital
Hospital
Hospital
Hospital
Time horizon
Inpatient stay
Inpatient stay
Inpatient stay
ICU component of stay
Main economic outcome
Mean incremental direct cost per hospitali- Adjusted mean incremental total cost
Adjusted mean incremental total
Mean incremental ICU cost attribzation attributable to the CABSI
per hospitalization attributable to the
cost per hospitalization attributautable to the CABSI
CABSI
ble to the CABSI
Multivariate adjustment made to No
Yes; regression model controlled for
Yes; regression model controlled for No
cost estimates
APACHE II score, heart failure, heAPACHE III score and age
modialysis, ventilator-days, and corticosteroid use
Unadjusted results (as published) Mean, $40,179 (SD not reported)
Median, $63,572 (75th95th quartile
Median, $62,652 (75th95th quartile All patients: mean, $23,751;
range, $39,314$84,871)
range, $17,439$170,799)
survivors: mean, $34,508 (SDs
not reported)
Adjusted results (as published)
No multivariate analysis
Mean, $11,971 (95% CI, $6,732
Mean, $56,167 (95% CI, $11,523
No multivariate analysis
$18,352)
$165,735)
Unadjusted results (2009 dollars) Mean, $56,000 (SD not reported)
Median, $113,700 (75th95th quartile
Median, $123,600 (75th95th quar- All patients: mean, $41,900;
range, $70,300$151,700)
tile range, $34,400$337,000)
survivors: mean, $60,900
(SDs not reported)
Adjusted results (2009 dollars)
No multivariate analysis
Mean, $21,400 (95% CI, $12,000
Mean, $110,800 (95% CI, $22,700 No multivariate analysis
$32,800)
$327,000)
Comments
Three clinician reviewers had to agree costs
Separate analyses done for all pawere attributable to the CABSI or its
tients and for patients who surcomplications for costs to be included;
vived to discharge
average loss to hospital, $26,885
City
Type of patients, by hospital site
No. of patientsa
Cost analysis primary or
secondary aim?
Purpose of economic analysis
Method of defining infection
Variable
table 2. Summary of 4 Studies of the Costs Associated with Catheter-Associated Bloodstream Infection (CABSI)
Houston, TX
Trauma ICU
70
Primary
Cost identification
By infection control team using
NNIS criteria
Matched control subjects: matching
based on age and Injury Severity
Score
Cost identification
By infection control team using NNIS
criteria
Patients in same ICU without
infection
Cocanour et al41
Kansas City, MO
Trauma ICU
13
Secondary
Lansford et al13
Cost identification
By infection control team using NNIS
criteria
Patients in same ICU without infection
St. Louis, MO
Surgical and medical ICUs
127
Primary
Warren et al14
Cost identification
Not reported
Nationwide
ICU
816
Secondary
Rello et al42
note. Costs were converted to 2009 dollars using the Consumer Price Index for Hospital Services (US Bureau of Labor Statistics). CDC, Centers for Disease Control and Prevention; CFU,
colony-forming unit; CI, confidence interval; ICU, intensive care unit; NNIS, National Nosocomial Infections Surveillance.
a
No. of patients with infection; excludes matched control subjects.
Control group
City
Type of patients, by hospital site
No. of patientsa
Cost analysis primary or
secondary aim?
Purpose of economic analysis
Method of defining infection
Variable
table 3. Summary of 4 Studies of the Costs Associated with Ventilator-Associated Pneumonia (VAP)
Seattle, WA
Inpatients
No cases
Secondary
Cost estimation
No cases
Cost identification
Bacteria or fungi at concentration of
11,000 CFU/mL
No control
Clinicians retrospective review of
charts and bills
Saint et al16
Madison, WI
Inpatients
123
Secondary
Tambyah et al15
Estimate, $2,471
No multivariate analysis
Estimate, $4,700
No multivariate analysis
Part of a multicenter study; cost analysis for just
1 hospital; ignored treatment, other costs; selected low estimate so as not to overestimate
impact of prevention measures
No
Hospital
Fixed as 1 additional inpatient day
Cost of ICU stay and diagnostic workup used in
management of CAUTI
No control
Investigators estimate of additional length of
stay and testing needed
Cost estimation
No cases
Philadelphia, PA
ICU
No cases
Secondary
Bologna et al17
note. Costs were converted to 2009 dollars using the Consumer Price Index for Hospital Services (US Bureau of Labor Statistics). CFU, colony-forming unit; ICU,
intensive care unit.
a
No. of patients with infection; excludes matched control subjects.
No control
Investigators estimate of additional
length of stay, testing, and treatment
needed
Source of cost data (baseline year) Not reported; 1998 dollars
Standard hospital charge multiplied by
cost/charge ratio; 1998 dollars
Costs measured
Lab test costs and medication costs
0.5-day inpatient stay, urine analysis,
urine culture, and sensitivity testing;
antimicrobial therapy
Perspective
Hospital
Hospital
Time horizon
Diagnostic and treatment period
Fixed as 0.5 additional inpatient day
Main economic outcome
Cost of lab tests and medications used Cost of hospital stay, laboratory tests, and
in management of CAUTI
medications used in management of
CAUTI
Multivariate adjustment made to No
No
cost estimates
Unadjusted results (as published) Mean, $589
Estimate, $2,041
Adjusted results (as published)
No multivariate analysis
No multivariate analysis
Unadjusted results (2009 dollars) Estimate, $1,200
Estimate, $4,000
Adjusted results (2009 dollars)
No multivariate analysis
No multivariate analysis
Comments
Ignored additional physician and
Ignored all other costs, such as
nursing costs and cost of bloodnursing and physician costs; selected
stream infections
low estimates of costs
Control group
Method of determining cost
City
Type of patients, by hospital site
No. of patientsa
Cost analysis primary or
secondary aim?
Purpose of economic analysis
Method of defining infection
Variable
table 4. Summary of 3 Studies of the Costs Associated with Catheter-Associated Urinary Tract Infection (CAUTI)
255
Primary
Durham, NC
All surgery
Kirkland et al44
No multivariate analysis
Mean, $6,700 (95% CI, $2,600
$10,800)
No multivariate analysis
Mean, $2,200 (95% CI, $600$3,900)
Most cases of SSI are diagnosed after Infectious complications included 41
discharge
wound infections, 10 cases of sepsis,
24 cases of wound dehiscence
No
Cost identification
Using NSQIP criteria
75
Primary
Ann Arbor, MI
General or vascular surgery
Dimick et al46
Cost identification
By investigator, using NNIS criteria
267
Primary
Boston, MA
All surgery
Perencevich et al45
note. Costs were converted to 2009 dollars using the Consumer Price Index (CPI) for Hospital Services (US Bureau of Labor Statistics), except for Kirkland et al,44 for which costs were converted
using the CPI for Healthcare Services, because the hospital services component was not calculated before 1997. CDC, Centers for Disease Control and Prevention; CFU, colony-forming unit; CI,
confidence interval; ICU, intensive care unit; LOS, length of stay; NNIS, National Nosocomial Infections Surveillance; NSQIP, National Surgical Quality Improvement Program.
a
No. of patients with infection; excludes matched control subjects.
b
Depending on the type of surgery and whether the infection was fatal.
Cost identification
By independent physicians, using CDC
criteria
Patients in same hospital without
infection
Iowa City, IA
General, cardiothoracic surgery, or
neurosurgery
316
Secondary
Herwaldt et al43
Cost identification
By infection control nurse, using
NNIS criteria
Control group
Matched control subjects: matching
based on NNIS risk index, type of
procedure, age, date of surgery,
and surgeon
Method of determining cost
Median total costs for patients with SSI Mean total costs for patients with SSI
vs patients without SSI
vs patients without SSI
Source of cost data (baseline year) Hospital financial department, details
Cost accounting database; 19911995
not reported; 19951998 dollars
dollars
Costs measured
All hospital costs excluding physicians Direct costs: overhead excluded, defees, overhead not reported
tails not reported
Perspective
Hospital
Hospital
Time horizon
30 days after operation
30 days after operation
Main economic outcome
Total postoperative costs attributable to Mean incremental direct cost per
the SSI
hospitalization associated with the
SSI
Multivariate adjustment made to Yes, but results reported only as perNo
cost estimates
centages; regression model controlled
for Karnofsky score, NNIS risk index, number of comorbidities, obesity, preoperative LOS, and age
Unadjusted results (as published) Median, $3,343
Initial stay: mean, $3,089 (95% CI,
$2,139$4,163); with readmission:
mean, $5,038 (95% CI, $4,020
$6,289)
Adjusted results (as published)
Increase of 25%106%b
No multivariate analysis
Unadjusted results (2009 dollars) Median, $5,600
Initial stay: mean, $6,000 (95% CI,
$4,200$8,100); with readmission:
mean, $9,800 (95% CI, $7,900
$12,300)
Adjusted results (2009 dollars)
Increase of 25%106%b
No multivariate analysis
Comments
Cost methods given in separate
report47
No. of patientsa
Cost analysis primary or
secondary aim?
Purpose of economic analysis
Method of defining infection
City
Type of patients, by hospital site
Variable
table 5. Summary of 4 Studies of the Costs Associated with Surgical Site Infection (SSI)
110
discussion
Past studies have estimated the number of infections prevented or lives saved if hospitals followed best practices in
infection prevention and control. The Centers for Disease
Control and Preventions Study on the Efficacy of Nosocomial
Infection Control (SENIC) project made such an estimate in
1975.19 Its estimate considered that 30%35% of most HAIs
were preventable with effective surveillance and control programs, including 22% of cases of pneumonia. In a 1985 follow-up survey,20 the SENIC project found that only a fraction
of those infections were actually being prevented, because
many hospitals still had not implemented recommended infection control measures. This was still the case in the present
decade.21 Our estimated ranges of potential reductions in
HAIs are in line with the most recent estimates by Kaye et al.22
The considerable uncertainty in our estimates of preventable HAIs and the associated mortality and costs stems from
both the component numbers and the calculations themselves. First, while our estimates of the annual numbers of
HAIs and associated deaths are based on broad national surveillance systems,2 those data are more than 5 years old and
do not capture the possibly lower infection and mortality
rates resulting from improved care practices implemented
since 2002. If care has improved since that time, the current
number of infections and deaths would be lower than those
observed in 2002. That would continue the trend observed
since 19751976, when the total number of HAIs estimated
by the SENIC project was 2.15 million.19 Second, there is no
definite way to attribute a death to an HAI, because patient
deaths frequently have multiple causes, and the role of infection may not always be clear. Klevens et al2 attempted to
address this by only including deaths for which an infection
preventionist determined that the HAI caused or directly contributed to the death, but this may overstate the number of
deaths of patients with HAI who may have actually died of
other causes. However, for some infectionsspecifically,
CABSIother investigators have provided higher estimates
of attributable mortality than Klevens et al.2 Pittet and colleagues23 estimated an attributable mortality of 35% in surgical ICU patients. For other HAIs, such as VAP, recent systematic reviews of the literature have highlighted difficulty of
quantifying the attributable mortality.24 Therefore, for most
HAIs additional studies are needed to determine the attributable mortality.
Certainty in the estimate of the proportion of HAIs that
are reasonably preventable is limited by the quality of the
HAI reduction studies. None of the studies was randomized,
and few were controlled, limiting the validity of reported risk
reductions. Most utilized a simple before-after design, comparing outcomes before and after an intervention to reduce
the incidence of HAIs, a design that cannot control for other
changes in patient care between the control period and the
intervention period and makes it difficult to attribute the
results to the intervention rather than to random variation,
patient selection, or other uncontrolled variables. To address
this limitation, we only included studies of good or moderate
quality in which causality could reasonably be attributed to
the intervention. In addition, some of the published studies
included in the AHRQ EPC report3 date back a decade or
more; infection prevention and control practices examined
in these older studies may be standard practice currently,
making large HAI reductions resulting from these interventions less likely in modern hospitals. To address this limitation, our analyses only included studies published in the past
decade.
Another source of uncertainty is generalizing from the results of studies in specialized populations, such as ICU patients, to patients on general hospital wards. In our review,
all but one of the CABSI, VAP, and CAUTI studies were
carried out in an ICU. The one study not performed in an
ICU examined CAUTI on a general medical ward.36 If that
study were discounted, the upper limit for the percentage of
HAIs that were reasonably preventable would fall from 69%
to 45%, which corresponds to 134,800 fewer preventable infections, 3,100 fewer preventable deaths, and $160 million to
$630 million less in costs.
The key uncertainty in estimating reasonably preventable
HAI deaths is the fact that the studies we reviewed did not
directly measure death as an outcome. Instead, we extrapolated reductions in death rates from the estimates of reductions in the number of HAIs, which have their own limitations. In addition, in multiplying the estimated fraction of
HAIs that are preventable by the estimated number of HAIrelated deaths, we assume that the proportion of deaths that
are preventable is the same as the proportion of infections
that are preventable. The true effect on deaths could be larger
or smaller, depending on the extent to which preventive measures affect the severity of HAIs and the extent to which
preventive measures work for the kinds of patients who are
more susceptible to fatal HAIs. In addition, this review focused on HAIs associated with invasive devices and surgical
procedures but did not capture data on morbidity and mortality associated with other infections, such as Clostridium
difficile infection.
Cost estimates are also limited, mostly by the poor design
of the available studies. In general, 2 types of cost analyses
were available in the published literature. The first was a raw
comparison of costs between patients with the HAI in question and patients without an infection (unadjusted results).
Some of these studies attempted to control for confounding
variables, such as patient age and disease severity, by selecting
uninfected matched control patients for each infected case
patient. Others simply compared mean or median costs for
111
comprehensive evidence-based interventions, it may be appropriate to consider reimbursement strategies that encourage hospitals to reduce the incidence of HAIs while also accounting for hospitals case mix indices. For example,
reimbursement based on a percentage reduction in the incidence of an HAI or a reduction of the number of cases of
an HAI below a threshold set according to the case mix.
In conclusion, our findings suggest that the goal of preventing 100% of HAIs may not be attainable even with use
of current evidence-based HAI prevention strategies; however, comprehensive implementation of such strategies could
prevent hundreds of thousands of HAIs and save tens of
thousands of lives and billions of dollars. Given their limitations, the figures in our study should not be used as a basis
for policy decisions but should prompt future studies with
robust designs to measure accurately the impact of HAI reduction strategies and the incremental cost of HAIs.
acknowledgments
We thank our colleague David Goldmann, MD, at the University of Pennsylvania, for reviewing the manuscript and for his many thoughtful
suggestions.
Potential conflicts of interest. P.J.B. reports that he is chair of the Healthcare Infection Control Practices Advisory Committee of the Centers for
Disease Control and Prevention and past president of SHEA. The authors
report no other potential conflicts of interest.
Address reprint requests to Craig A. Umscheid, MD, MSCE, Assistant
Professor of Medicine and Epidemiology, Director, Center for Evidence-Based
Practice, University of Pennsylvania, 3535 Market Street, Mezzanine, Suite
50, Philadelphia, PA 19104 (craig.umscheid@uphs.upenn.edu
This study was originally performed for the Society for Healthcare Epidemiology of America (SHEA) and was included in its written testimony to
the Committee on Oversight and Government Reform in its Hearing on
Healthcare-Associated Infections: A Preventable Epidemic, chaired by Henry
A. Waxman on April 16, 2008, in Washington, DC. Findings from the manuscript were subsequently presented at the 19th Annual Scientific Meeting
of SHEA in San Diego, California, in 2009.
112
appendix a
table a1.
Type of infection
No. of
infections
No. of deaths
from infection
Case fatality
rate, %
248,678
250,205
561,667
290,485
386,090
1,737,125
30,665
35,967
13,088
8,205
11,062
98,987
12.3
14.4
2.3
2.8
2.9
5.7
note.
CABSI
VAP
CAUTI
SSI
2
1
6
2
8
19
0
0
3
4
5
12
3
0
0
6
1
10
4
2
1
6
15
28
10
0
0
2
7
5
1
1
2
3
1
3
2
2
2
15
3
2
5
3
note. Data are from the AHRQ report by Ranji et al.3 CABSI, catheter-associated
bloodstream infection; CAUTI, catheter-associated urinary tract infection; EPC, evidence-based practice center; SSI, surgical site infection; VAP, ventilator-associated pneumonia; US, United States.
references
1. Kohn LT, Corrigan JM, Donaldson MS, eds. To err is human:
building a safer health system. National Academy of Sciences,
2000.
2. Klevens RM, Edwards JR, Richards CL Jr, et al. Estimating health
care-associated infections and deaths in US hospitals, 2002. Public Health Rep 2007;122(2):160166.
3. Ranji SR, Shetty K, Posley KA, et al. Volume 6: prevention of
healthcare-associated infections. Rockville, MD: Agency for
Healthcare Research and Quality; 2007 January 2007. AHRQ
publication 04(07)-0051-6.
4. Yokoe DS, Mermel LA, Anderson DJ, et al. A compendium of
strategies to prevent healthcare-associated infections in acute
care hospitals. Infect Control Hosp Epidemiol 2008;29(suppl 1):
S12S21.
5. Wald HL, Kramer AM. Nonpayment for harms resulting from
medical care: catheter-associated urinary tract infections. JAMA
2007;298(23):27822784.
6. Pronovost PJ, Goeschel CA, Wachter RM. The wisdom and
justice of not paying for preventable complications. JAMA
2008;299(18):21972199.
7. Brown A, Wells P, Jaffey J, et al. Point-of-care monitoring devices
for long-term oral anticoagulation therapy: clinical and cost
effectiveness. Ottawa: Canadian Agency for Drugs and Technologies in Health, 2007. Technology report 72.
8. DiGiovine B, Chenoweth C, Watts C, Higgins M. The attributable mortality and costs of primary nosocomial bloodstream
infections in the intensive care unit. Am J Respir Crit Care Med
1999;160(3):976981.
9. Harbarth S, Sax H, Gastmeier P. The preventable proportion of
nosocomial infections: An overview of published reports. J Hosp
Infect 2003;54(4):258266.
10. Shannon RP, Patel B, Cummins D, Shannon AH, Ganguli G,
Lu Y. Economics of central lineassociated bloodstream infections. Am J Med Qual 2006;21(suppl 6):7S-16S.
11. Warren DK, Quadir WW, Hollenbeak CS, Elward AM, Cox MJ,
Fraser VJ. Attributable cost of catheter-associated bloodstream
infections among intensive care patients in a nonteaching hospital. Crit Care Med 2006;34(8):20842089.
12. Dimick JB, Pelz RK, Consunji R, Swoboda SM, Hendrix CW,
Lipsett PA. Increased resource use associated with catheter-related bloodstream infection in the surgical intensive care unit.
Arch Surg 2001;136(2):229234.
13. Lansford T, Moncure M, Carlton E, et al. Efficacy of a pneumonia prevention protocol in the reduction of ventilator-associated pneumonia in trauma patients. Surg Infect (Larchmt)
2007;8(5):505510.
14. Warren DK, Shukla SJ, Olsen MA, et al. Outcome and attributable cost of ventilator-associated pneumonia among intensive
care unit patients in a suburban medical center. Crit Care Med
2003;31(5):13121317.
15. Tambyah PA, Knasinski V, Maki DG. The direct costs of nosocomial catheter-associated urinary tract infection in the era of
managed care. Infect Control Hosp Epidemiol 2002;23(1):2731.
16. Saint S, Veenstra DL, Sullivan SD, Chenoweth C, Fendrick AM.
The potential clinical and economic benefits of silver alloy urinary catheters in preventing urinary tract infection. Arch Intern
Med 2000;160(17):26702675.
17. Bologna RA, Tu LM, Polansky M, Fraimow HD, Gordon DA,
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.
33.
113
Whitmore KE. Hydrogel/silver ion-coated urinary catheter reduces nosocomial urinary tract infection rates in intensive care
unit patients: a multicenter study. Urology 1999;54(6):982987.
Dimick JB, Chen SL, Taheri PA, Henderson WG, Khuri SF,
Campbell DA Jr. Hospital costs associated with surgical complications: a report from the private-sector national surgical
quality improvement program. J Am Coll Surg 2004;199(4):531
537.
Haley RW, Culver DH, White JW, Morgan WM, Emori TG. The
nationwide nosocomial infection rate: a new need for vital statistics. Am J Epidemiol 1985;121(2):159167.
Haley RW, Culver DH, White JW, et al. The efficacy of infection
surveillance and control programs in preventing nosocomial
infections in US hospitals. Am J Epidemiol 1985;121(2):182205.
Braun BI, Kritchevsky SB, Wong ES, et al. Preventing central
venous catheter-associated primary bloodstream infections:
characteristics of practices among hospitals participating in the
evaluation of processes and indicators in infection control
(EPIC) study. Infect Control Hosp Epidemiol 2003;24(12):926
935.
Kaye KS, Engemann JJ, Fulmer EM, Clark CC, Noga EM, Sexton
DJ. Favorable impact of an infection control network on nosocomial infection rates in community hospitals. Infect Control
Hosp Epidemiol 2006;27(3):228232.
Pittet D, Harbarth S. What techniques for diagnosis of ventilator-associated pneumonia? [see comment]. Lancet 1998;
352(9122):8384.
Melsen WG, Rovers MM, Bonten MJ. Ventilator-associated
pneumonia and mortality: a systematic review of observational
studies. Crit Care Med 2009;37(10):27092718.
Perencevich EN, Stone PW, Wright SB, et al. Raising standards
while watching the bottom line: making a business case for
infection control. Infect Control Hosp Epidemiol 2007;28(10):
11211133.
Pronovost P, Needham D, Berenholtz S, et al. An intervention
to decrease catheter-related bloodstream infections in the ICU.
N Engl J Med 2006;355(26):27252732.
Berenholtz SM, Pronovost PJ, Lipsett PA, et al. Eliminating catheter-related bloodstream infections in the intensive care unit.
Crit Care Med 2004;32(10):20142020.
Coopersmith CM, Zack JE, Ward MR, et al. The impact of
bedside behavior on catheter-related bacteremia in the intensive
care unit. Arch Surg 2004;139(2):131136.
Warren DK, Zack JE, Mayfield JL, et al. The effect of an education program on the incidence of central venous catheterassociated bloodstream infection in a medical ICU. Chest 2004;
126(5):16121618.
Warren DK, Zack JE, Cox MJ, Cohen MM, Fraser VJ. An educational intervention to prevent catheter-associated bloodstream infections in a nonteaching, community medical center.
Crit Care Med 2003;31(7):19591963.
Coopersmith CM, Rebmann TL, Zack JE, et al. Effect of an
education program on decreasing catheter-related bloodstream
infections in the surgical intensive care unit. Crit Care Med 2002;
30(1):5964.
Sherertz RJ, Ely EW, Westbrook DM, et al. Education of physicians-in-training can decrease the risk for vascular catheter
infection. Ann Intern Med 2000;132(8):641648.
Babcock HM, Zack JE, Garrison T, et al. An educational intervention to reduce ventilator-associated pneumonia in an inte-
114
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
45.
46.
47.
Prevention of postoperative mediastinitis: a clinical process improvement model. J Healthc Qual 2004;26(1):2227.
Cocanour CS, Ostrosky-Zeichner L, Peninger M, et al. Cost of
a ventilator-associated pneumonia in a shock trauma intensive
care unit. Surg Infect (Larchmt) 2005;6(1):6572.
Rello J, Ollendorf DA, Oster G, et al. Epidemiology and outcomes of ventilator-associated pneumonia in a large US database. Chest 2002;122(6):21152121.
Herwaldt LA, Cullen JJ, Scholz D, et al. A prospective study of
outcomes, healthcare resource utilization, and costs associated
with postoperative nosocomial infections. Infect Control Hosp
Epidemiol 2006;27(12):12911298.
Kirkland KB, Briggs JP, Trivette SL, Wilkinson WE, Sexton DJ.
The impact of surgical-site infections in the 1990s: attributable
mortality, excess length of hospitalization, and extra costs. Infect
Control Hosp Epidemiol 1999;20(11):725730.
Perencevich EN, Sands KE, Cosgrove SE, Guadagnoli E, Meara
E, Platt R. Health and economic impact of surgical site infections
diagnosed after hospital discharge. Emerg Infect Dis 2003;9(2):
196203.
Dimick JB, Pronovost PJ, Cowan JA, Lipsett PA. Complications
and costs after high-risk surgery: where should we focus quality
improvement initiatives? J Am Coll Surg 2003;196(5):671678.
Herwaldt LA, Swartzendruber SK, Edmond MB, et al. The epidemiology of hemorrhage related to cardiothoracic operations.
Infect Control Hosp Epidemiol 1998;19(1):916.