SUPPLEMENT ARTICLE
Consequences of Inaction:
Importance of Infection Control Practices
John M. Boyce
Division of Infectious Diseases, Hospital of Saint Raphael, New Haven, Connecticut
The increasing prevalence of antimicrobial-resistant pathogens in health care facilities is due in large part to
overuse of antibiotics and poor compliance with recommended infection control practices. To control the
spread of such pathogens, health care facilities must reduce overuse and abuse of antibiotics, and they must
implement new multidisciplinary programs to improve hand hygiene practices among health care workers
and improve compliance with recommended barrier precautions.
Earlier papers presented at this conference have dis-
cussed antimicrobial resistance from a global prospec-
tive. As a practicing hospital epidemiologist, I will focus
on antimicrobial resistance in health care settings.
Dr. Levy briefly mentioned some of the costs associ-
ated with antimicrobial resistance in health care settings.
Numerous studies have documented that infections
caused by multidrug-resistant pathogens often result in
prolonged hospital stays and excess hospital costs [1].
Increased per diem costs, and, to a lesser extent, phar-
macy and laboratory costs are important contributors to
excess hospital expenditures attributable to infections
caused by resistant pathogens. In a few instances, the
antibiotics required to treat patients with resistant path-
ogens may be more expensive. Potential costs of anti-
microbial resistance that have not been well quantified
might include loss of productivity of the affected patients
and other quality-of-life issues associated with infections
that are either difficult to treat or untreatable. On a na-
tional basis, projected costs of antimicrobial resistance
in health care settings have been estimated to range from
1 million dollars to 30 billion dollars, with the best es-
timate being 4 billion dollars annually in the United
Reprints or correspondence: Dr. John M. Boyce, Division of Infectious Diseases,
Hospital of Saint Raphael, 1450 Chapel St., New Haven, CT 06511 (Jboyce@srhs
.org).
Clinical Infectious Diseases 2001; 33(Suppl 3):S133–7
 2001 by the Infectious Diseases Society of America. All rights reserved.
1058-4838/2001/3306S3-0007$03.00
States (Office of Technology Assessment, 1995). Clearly,
the economic impact of antimicrobial resistance in health
care settings is substantial.
Resistant organisms of special epidemiologic impor-
tance in health care settings include methicillin-resis-
tant Staphylococcus aureus (MRSA), vancomycin-resis-
tant enterococci (VRE), and gram-negative rods that
produce extended spectrum b-lactamases (ESBLs).
Clostridium difficile, which is usually not included in
discussions of multidrug-resistant bacteria, is also an
important pathogen resistant to many antimicrobial
agents. Recently, vancomycin-intermediate S. aureus
(VISA) infections have been documented in several pa-
tients, and there is concern that such strains will be-
come more prevalent [2].
Data from the Centers for Disease Control and Pre-
vention (CDC) National Nosocomial Infection Sur-
veillance (NNIS) system have documented the pro-
gressive increase in the prevalence of MRSA. By 1997,
more than 35% of nosocomial staphylococcal infections
in large hospitals were caused by MRSA [3]. In me-
dium-sized and smaller hospitals, 30% and 25% of such
infections, respectively, were caused by MRSA in 1997.
Unfortunately, the dramatic increase in the prevalence
of MRSA occurred during the 1980s and early 1990s,
when virtually all hospitals in the United States had
written guidelines for infection control. One must con-
clude that either the guidelines in use at that time did
Infection Control Practices • CID 2001:33 (Suppl 3) • S133
not take into account all patterns of transmission, or that the
poor compliance of health care workers with recommended
practices permitted continued spread of MRSA. I suspect that
poor compliance (an example of inaction) has played an im-
portant role in the emergence of MRSA.
The NNIS system has also documented a dramatic increase
in the percent of nosocomial enterococcal infections that are
caused by VRE. By 1997, 22% of nosocomial enterococcal in-
fections in intensive care units (ICUs), and 15% of those in non-
ICU wards were caused by VRE [3]. There is little doubt that
the increasing use of vancomycin for management of MRSA and
methicillin-resistant coagulase-negative staphylococci, and, per-
haps, frequent use of oral vancomycin for C. difficile-related dis-
ease set the stage for the dramatic increase in VRE.
One issue that has not received enough attention, in my
opinion, is that there is too little careful epidemiological analysis
of sources of transmission and modes of transmission or re-
sistant pathogens in many hospitals. The importance of estab-
lishing local transmission patterns is illustrated by the following
example. Epidemiological analysis of a hospital-wide outbreak
of nosocomial MRSA infection in one hospital revealed that a
respiratory therapist who had chronic MRSA sinusitis was the
source of the outbreak [4]. Failure to identify such an individual
as a source would lead to poor control, despite implementation
of other general control measures, such as isolating patients,
use of recommended barrier precautions, and appropriate hand
washing. In this example, the outbreak of infection was ter-
minated only after the respiratory therapist, who was the source
of the outbreak, was treated appropriately.
As mentioned by previous speakers, overuse and abuse of
antibiotics is also a major factor in contributing to the problem
of antimicrobial resistance in health care settings. For example,
a study conducted by Pestotnik et al. [5] found that antibiotic
use has changed dramatically in hospitals during the past 10
to 15 years. The study revealed that the percentage of hospi-
talized patients who have received antibiotics increased from
32% in 1988 to 53% in 1994. The percentage of such patients
receiving broad-spectrum antibiotics increased from 24% in
1988 to 47% in 1994. Similar trends in antimicrobial use are
likely to have occurred in many other hospitals.
In 1996, CDC and the National Foundation for Infectious
Diseases published guidelines for improving antimicrobial use
in hospitals [6]. Some of the strategies recommended in the
guideline are the following:
1. Optimize perioperative prophylaxis
2. Improve both the choice and duration of empiric ther-
apy, and
3. Use both educational and administrative measures to
improve antimicrobial prescribing practices of physicians.
Examples of administrative measures include use of an an-
S134 • CID 2001:33 (Suppl 3) • Boyce
tibiotic order sheet to guide selection of antibiotics, or imple-
mentation of computerized physician order entry to provide
physicians with guidance on antibiotics selection [5]. The
guideline recommended that hospitals monitor both antimi-
crobial use and antimicrobial resistance. Unfortunately, despite
publication of these guidelines in 1996, there are many hospitals
that perform on very rudimentary, if any, monitoring of an-
timicrobial use. Many facilities do not express the use of in-
dividual antimicrobial agents as grams per 1000 patient-days
or defined daily doses (DDDs) per 1000 patient-days. Express-
ing antimicrobial use in such a fashion facilitates comparison
of rates of use in different hospital services or wards, and per-
mits comparison of use patterns between facilities of varying
size [7]. Hospitals and other health care facilities, such as long-
term care facilities, that have not monitored antimicrobial use
in this manner are strongly encouraged to do so.
Additional guidelines for improving the use of antimicrobial
agents in hospitals have also been published jointly by the
Infectious Diseases Society of America and the Society for
Healthcare Epidemiology of America [8]. Implementation of
clinical practice guidelines is one of several recommendations
made to improve use of antimicrobial agents. For example,
many hospitals have adopted the Hospital Infection Control
Practices Advisory Committee (HICPAC) guideline for appro-
priate use of vancomycin [9]. Educational efforts, such as lec-
tures dealing with appropriate use of antimicrobial agents, are
still recommended, although a number of studies have dem-
onstrated that periodic lectures often have little long-term im-
pact on physician prescribing practices. For this reason, hos-
pitals also should seriously consider utilizing administrative
measures (such as those mentioned earlier as well as antibiotic
stop orders), having pharmacists interact with physicians in
patient wards, or forming a multidisciplinary antibiotic man-
agement team. Selective reporting of antibiotic susceptibility
test results by clinical microbiology laboratories is another ex-
ample of an administrative measure that can affect physician
choice of antimicrobial agents.
Some hospitals require an infectious disease physician to
approve the use of restricted antibiotics. For example, White
et al. [10] implemented a program that was designed to reduce
antibiotic costs and antimicrobial resistance. The program re-
quired that infectious disease attending physicians approve the
use of certain antimicrobial agents, including ceftazidime, ami-
kacin, ticarcillin-clavulanate, aztreonam, and intravenous cip-
rofloxacin. Outcome measures included the level of suscepti-
bility of gram-negative bacilli, patient survival, and duration of
hospital stay. The investigators found that the percentage of
isolates of Escherichia coli, Pseudomonas, Enterobacter cloacae,
and Acinetobacter species that are resistant to ceftazidime de-
creased significantly in an ICU after the intervention. Similar
decreases in the prevalence of antimicrobial resistance were
Table 1. Compliance of health care workers with recom- actual compliance of health care workers remains suboptimal
mended handwashing practices. in many hospitals. For example, in 3 hospitals where VRE was
endemic or epidemic, the compliance of health care workers
Rate of
Author [reference] Clinical setting compliance, % with recommended to barrier precautions ranged from 28% to
71% (table 2) [25–27]. Such poor compliance with recom-
Preston et al. [11] Open ward 16
mended infection control practices is another example of how
ICU 30
inaction on the part of hospitals is likely to have contributed
Albert et al. [12] ICUs 41
to the spread of resistant pathogens.
ICUs 28
In intensive care units, where the incidence of infections
Larson [13] All wards 44
caused by resistant organisms continues to be high despite
Donowitz [14] PICU 30
implementation of recommended control measures, some in-
Graham [15] ICU 32
vestigators have recommended “universal glove use.” This strat-
Dubbert et al. [16] ICU 81
egy requires that every health care worker wear gloves when
Pettinger et al. [17] SICU 51
caring for every patient in the unit, regardless of whether or
Larson et al. [18] NICU/others 29
not the patient has been identified as having a resistant organ-
Doebbeling et al. [19] ICUs 40
ism. Reports by Hartstein et al. [28] and others [29] suggest
Zimakoff et al. [20] ICUs 40
that universal glove use has contributed to the control of out-
Meengs et al. [21] Emergency department 32
breaks of MRSA and VRE.
Pittet et al. [22] All wards 48
Because colonized and infected patients represent the major
NOTE. ICU, intensive care unit; NICU, neonatal intensive care unit; PICU,
pediatric intensive care unit; SICU, surgical intensive care unit.
reservoir for many resistant pathogens encountered in health
care settings, administering decolonization therapy to affected
patients is another strategy that has been useful in some settings
noted for other antimicrobial agents as well. No increase in
[30]. In hospitals where MRSA has been highly endemic or
patient mortality was noted during the study period, and there
epidemic, treating colonized patients with intranasal mupirocin
was no adverse effect on the duration of the patient’s stay.
ointment, when combined with other infection-control barri-
Although it is widely accepted that most multidrug-resistant
ers, appears to have contributed to the control of nosocomial
pathogens are spread in hospitals via the hands of health care
MRSA on a number of occasions.
workers, many studies performed during the past 10 to 15 years
Unfortunately, in the late 1980s and early 1990s, when the
have demonstrated that the compliance of health care workers
prevalence of MRSA increased substantially, health care workers
with recommended hand washing practices is unacceptably low.
and administrators in some hospitals adopted the attitude that
Table 1 demonstrates that the percentage of health care workers
it was impossible to control transmission of the organism, and
who comply with recommended handwashing practices has
they abandoned many of their efforts to control the spread of
varied from 16% to 80%, with an average of rate of compliance
MRSA. In more recent years, a similar attitude has been adopted
of 40%. The increasing spread of resistant nosocomial patho-
in many hospitals where VRE has become prevalent. However,
gens should serve as an impetus for hospitals to develop in-
there are a number of examples demonstrating that appropriate
novative methods to improve hand hygiene among health care
surveillance and barrier precautions can limit the spread of
workers [23].
VRE. In a hospital where VRE had not yet become endemic,
In 1996, HICPAC published guidelines for isolation precau-
focal outbreaks of vanB-type VRE and vanA-type VRE were
tions in hospitals. These guidelines are summarized briefly [24]:
controlled by performing frequent culture surveys of patients
and by requiring the use of gloves and gowns by health care
1. Place patient in private room, or cohort patients workers who entered the rooms of patients with VRE [31, 32].
2. Wear gloves to enter room Anglim et al. [33] reported successful control of VRE by using
3. Wear gown if substantial contact with the patient or the a combination of aggressive barrier precautions, culture surveys
patient’s environment is anticipated
4. Remove gloves (and gown) upon leaving room Table 2. Compliance of personnel with barrier pre-
cautions for vancomycin-resistant enterococci.
5. Wash hands with antimicrobial soap or waterless an-
tiseptic agent Personnel Rate of
6. Dedicate noncritical medical equipment to patient’s Author [reference] observed, no. compliance, %
room, and Morris et al. [25] 56 56
7. Limit transport of patient to essential purposes. Shay et al. [26] 25 25
Slaughter et al. [27] 4364 71
Despite publication of the guideline more than 3 years ago,

Infection Control Practices • CID 2001:33 (Suppl 3) • S135

of high-risk patients, and decreased use of vancomycin. More
recently, Montecalvo et al. [34] reported that a combination
of surveillance cultures, patient and nurse cohorting, wearing
of gloves and gowns for entering VRE patient rooms, and mon-
itoring of compliance with recommended procedures resulted
in a significant reduction in the incidence of VRE bloodstream
infections. Similar success has been reported in several other
institutions where VRE had become endemic [35, 36].
In summary, controlling the spread of antimicrobial resis-
tance in health care settings requires improved infection control
practices and more prudent use of antibiotics. Infection control
efforts must include ongoing laboratory-based surveillance,
identifying colonized patients and placing them in isolation,
and improving compliance of health care workers with rec-
ommended barrier precautions and hand hygiene practices.
Hospitals administrators and department heads must provide
visible support for infection control policies, and must provide
the necessary resources for improving use of antimicrobial
agents. Inaction will lead to continued emergence of multidrug-
resistant pathogens in health care settings.
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