(Chest. 2001;119:405S-411S.)
© 2001
American College of Chest Physicians
Implementation of Strategies to Control Antimicrobial Resistance*
Rekha Murthy, MD
*
From the Division of Infectious Diseases, Cedars-Sinai Medical Center, University of California, Los Angeles, Los Angeles, CA.
Correspondence to: Rekha Murthy, MD, Director, Hospital Epidemiology, Cedars-Sinai Medical Center, 8700 Beverly Blvd, Room: MOT 1130E, Los Angeles, CA 90048
 |
Abstract
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Antimicrobial resistance has emerged as a major public health issue
in recent years. A steady increase in resistance continues despite the
introduction of new antibiotics, and resistant bacteria have been
associated with increased patient morbidity and mortality as well as
with increased costs. Addressing the problem of antimicrobial
resistance requires both infection control and regulation of antibiotic
use; addressing either alone is insufficient. Mounting evidence shows
that control of the use of broad-spectrum antibiotics (especially
vancomycin and third-generation cephalosporins) and implementation of
infection control measures can result in decreased incidence of
antibiotic-resistant bacteria such as vancomycin-resistant enterococci
and extended-spectrum ß-lactamase–producing Escherichia
coli and Klebsiella. Recent reports from professional
organizations and a consensus of experts have outlined strategies for
the control of resistance in hospitals, with specific measures
identified for antibiotic control and infection control. These reports
have emphasized the importance of a multidisciplinary approach in
tackling this problem in hospitals and have suggested that a
quality-improvement model be used to address antimicrobial resistance.
A close collaboration among the disciplines of infectious diseases,
microbiology, hospital epidemiology, pharmacy, and nursing, with
particular emphasis in ICUs, and with strong support from hospital
leadership, can result in an effective program that can be readily
incorporated into the quality-improvement goals of any health-care
organization.
Key Words: antibiotics • drug resistance • ICUs • vancomycin
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Introduction
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Antimicrobial
resistance has emerged as a major public health concern in the United
States during the past decade.1
2
Indeed, despite the
continuing development and introduction of new antibiotics,
antimicrobial resistance has increased steadily. Over 70% of bacterial
pathogens found in US hospitals are resistant to at least one
antibiotic.3
Nosocomial infections, which are important
factors of morbidity and mortality in US hospitals and nursing homes,
are increasingly caused by such microorganisms. The increase in
vancomycin-resistant enterococci (VRE), the emergence of
methicillin-resistant Staphylococcus aureus), (MRSA) strains
possessing a decreased susceptibility to vancomycin
(glycopeptide-intolerant S aureus), and the emergence of new
patterns of resistance in Gram-negative bacteria (including
Pseudomonas aeruginosa, Enterobacter species,
Escherichia coli, and Klebsiella pneumoniae,
among others) have the potential for major public health consequences
as existing antibiotics are rendered ineffective. Patients with
resistant infections are twice as likely to require hospitalization, to
need longer hospitalizations, and to die as a result of their
infections.4
5
Furthermore, the cost of caring for
patients with infections caused by resistant bacteria is much higher
than for those with antibiotic-sensitive organisms, with national costs
of antimicrobial resistance in the United States estimated between $100
million and $30 billion annually.5
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Factors Involved in Emerging Resistance
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Surveillance data from the Centers for Disease Control and
Prevention (CDC) confirm that resistance to commonly used
broad-spectrum antibiotics (including vancomycin, third-generation
cephalosporins, carbapenems, and quinolones) is increasing in both
Gram-negative (E coli, P aeruginosa) and
Gram-positive bacteria (VRE and MRSA).6
The increase in
antimicrobial resistance is most marked in ICUs; according to CDC data,
rates of nosocomial infections in ICUs in the United States due to
selected resistant organisms have increased dramatically over the past
decade. For example, 1998 rates of ICU infections due to resistant
organisms, when compared with the previous 5 years, indicate an 89%
increase in quinolone-resistant P aeruginosa, a 55%
increase in VRE, and an approximate 30% increase in MRSA and
imipenem-resistant P aeruginosa.6
There are several factors contributing to the increase in antimicrobial
resistance (Table 1
). Some are related to host factors, such as a sicker inpatient
population, a larger immunocompromised population, and new procedures
and instrumentation that have resulted in new sites or types of
infection. Other factors are related to increases in antibiotic
pressure (both in the community and health-care institutions) and
lapses in infection-control compliance in health-care settings. While
little opportunity exists to modify the former, mounting evidence
suggests that improving antibiotic practices and compliance with
infection control precautions can result in decreased antimicrobial
resistance. Emerging multidrug-resistant pathogens in both community
and health-care settings and complacency among the public and medical
community regarding antibiotic use have also contributed to the
problem.
Postulated mechanisms for the appearance and spread of antimicrobial
resistance in hospitals include the following: (1) introduction of a
resistant organism to a previously susceptible population, (2)
acquisition of resistance by a susceptible strain (via spontaneous
mutation or genetic transfer), (3) expression of regulated resistance
already present in the population, (4) selection of a resistant
subpopulation, and (5) dissemination or spread of resistant
organisms.7
ICUs provide a unique setting, facilitating
the emergence and spread of resistance for several reasons: (1)
close quarters and high frequency of staff-to-patient contact can
increase patient-to-patient contact; (2) cross-transmission of
pathogens due to lack of hand washing (and hand-washing rates decline
with increased workload)8
; (3) heavy selection pressure by
broad-spectrum antibiotic use; and (4) environmental contamination
providing further opportunity for cross-transmission of pathogens via
contaminated equipment and hands of health-care workers.
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Problem Pathogens
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The most common mechanism of antimicrobial resistance in
Gram-negative bacteria involves the production of ß-lactamase enzymes
that can inactivate commonly used antibiotics. Some
resistance-conferring genes are intrinsic to bacteria (ie,
chromosomally based, such as in P aeruginosa)9
;
others are carried on plasmids and can be particularly problematic
because they enable transfer of resistance between different bacterial
species.10
New types of plasmid-mediated resistant mutants
(SHV or TEM) have been characterized that are capable of producing
extended-spectrum ß-lactamases (ESBLs).10
Strains
producing ESBLs are able to inactivate third-generation cephalosporins
(such as cefoperazone, cefotaxime, ceftazidime, and ceftizoxime) and
monobactams and may only be sus-ceptible to carbapenems, amikacin,
quinolones, cefepime (a fourth-generation cephalosporin) or
ß-lactam/ß-lactamase–inhibitor combination antibiotics, such as
piperacillin/tazobactam and ticarcillin/clavulanate.10
11
Under high selective pressure through cephalosporin antibiotic use,
ESBL-producing strains can emerge, with resistance spreading to other
bacteria. Furthermore, these strains may be inaccurately identified by
the automated susceptibility-testing methods used in most microbiology
laboratories, leading to ineffective therapeutic choices.
Some resistant Gram-negative species possess inducible, chromosomally
mediated ß-lactamase expression that can result in high-level
production of the enzymes sufficient to render the organism fully
resistant to ß-lactams, including third-generation
cephalosporins.12
Such bacterial strains, including some
species of Enterobacter, Citrobacter, Serratia, and Pseudomonas, may be
susceptible to extended-spectrum penicillins, carbapenems, quinolones,
cefepime, and amikacin; susceptibility data should be verified for
individual cases. The emergence of strains of resistant Enterobacter
species has been associated with the overuse of second-generation and
third-generation cephalosporins.12
Finally, infections
with resistant Enterobacter and ESBLs have been associated with
increased mortality, indicating the importance of appropriate initial
therapy as well as for measures to address emergence of these pathogens
in institutions, particularly in the ICU.11
12
At many hospitals, strains of MRSA are endemic and difficult to
control,13
having spread from tertiary medical centers to
community hospitals and residential-care facilities. Until recently,
vancomycin was the only antibiotic effective for therapy of infections
with these MRSA strains,13
leading to increased use of
this antibiotic and the potential for emergence of vancomycin-resistant
bacteria. The recent emergence of strains of MRSA
(glycopeptide-intolerant S aureus) and
methicillin-resistant Staphylococcus epidermidis with
elevated minimum inhibitory concentrations to vancomycin have raised
concerns about the potential for an increased incidence of infections
caused by these resistant microbes.14
15
Incidence rates of VRE infection in ICU patients have increased
steadily in the United States, from <1% in 19893
to
> 25% in 1999.6
Risk factors for the acquisition of VRE
in hospitalized patients include immunosuppression, admission to the
ICU, prolonged length of hospital stay, prolonged duration of
broad-spectrum antimicrobial use, and lapses in infection
control.16
17
18
Uses of vancomycin, clindamycin, and
third-generation cephalosporins have also been identified as additional
risk factors.16
19
20
Until recently, no uniformly
effective antimicrobial therapies were available for serious infections
with VRE.21
Two new agents, quinupristin/dalfopristin and
linezolid, recently added to the antimicrobial armamentarium offer new
options for therapy of infections with some strains of Gram-positive
bacteria that are resistant to vancomycin.22
|
Antibiotic Control and Infection Control: The Two Sides of
the Resistance "Coin"
|
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Overuse of antimicrobial agents and poor compliance with
infection-control measures have been identified as the major reasons
for increasing trends in antimicrobial resistance. More than half of
all hospitalized patients receive antibiotics, and such drugs can
account for up to 50% of hospital pharmacy budgets.23
Of
greater concern are estimates that 25 to 50% of all antibiotic
prescriptions are inappropriate as a result of incorrect choices in
drug, dose, or duration.23
24
25
Two uses of antimicrobial agents that deserve special attention with
regard to resistance are empiric antibiotic therapy, defined as
treatment initiated before confirmation of infection is available, and
prophylactic antibiotic use, especially before surgical procedures.
Waiting for the full details of an infection to be known is often
imprudent. Physicians should, however, use broad-spectrum antibiotics
for the shortest duration possible; if antibiotic therapy is
begun for coverage of a possible infection of unknown type, such
agents should be changed to those with the narrowest spectrum of
activity based on microbiological results of culture and
susceptibility.25
Furthermore, when making choices regarding antibiotic therapy, the
physician should have good working knowledge of the most common
infections and the most appropriate drugs for use. Procedures have been
developed to maximize the efficacy of such decisions, including
restrictive formularies, prospective antibiotic monitoring programs,
and computer-assisted management support.23
25
Evans and
colleagues26
demonstrated that providing real-time
information feedback to physicians at the time of order entry resulted
in improved antibiotic selection.
The overuse of antibiotics for surgical prophylaxis may lead to
increased resistance, toxicity, and cost. Recent CDC guidelines for
surgical prophylaxis recommend that in most clean-contaminated
procedures, a single, well-timed (within 2 h of incision) dose of
antibiotic is effective in reducing the risk of postoperative
infection, and that further doses do not provide additional
benefit.27
Hospitals have considerable potential for the spread of antimicrobial
resistance. Poor compliance with basic infection-control techniques is
largely responsible for the dissemination of resistant organisms.
Caregivers, for example, may not wash their hands or wear and discard
gloves appropriately, and efforts to modify caregiver behavior in this
regard have proved unsuccessful over the long term. Understaffing, high
intensity of care, and high workload also contribute to noncompliance
with hand washing.8
28
Environmental contamination with
organisms such as VRE also adds to the problem of resistance control. A
large reservoir of patients colonized with resistant organisms may be
difficult to identify in the absence of costly surveillance
measurements, unless they have an active infection, which would then
further increase the likelihood of person-to-person spread in the
hospital setting.
Despite these critical concerns with resistance, evidence is
growing to show that the problem can be effectively managed and
controlled. For some pathogens, such as MRSA, infection-control
techniques appear to have the most impact, whereas for other organisms,
such as ESBL-producing species or Enterobacter, antibiotic-control
measures may be more effective.29
For other groups, such
as VRE, a combination of both strategies may be required for successful
control.
Studies have documented the role of these measures in controlling
specific resistance problems. In a study by Bamberger and
Dahl,30
enforcement of antibiotic-usage restrictions led
to decreases in resistance in Enterobacter cloacae and
P aeruginosa within 6 months. In another
study,31
a formulary change from ceftazidime to cefepime
in an ICU resulted in improvement in resistant E cloacae.
Quale et al32
reported on the impact of a formulary change
that restricted cefotaxime and vancomycin use and added
ß-lactam/ß-lactamase–inhibitor combination antibiotics
(ampicillin/sulbactam and piperacillin/tazobactam) to replace
third-generation cephalosporins. Over 18 months, a significant
reduction in the prevalence of VRE colonization, from 47% to 15% of
patients, was documented.32
Other
studies33
34
have demonstrated a correlation between
decreased cephalosporin use and reduced rates of resistance to
ceftazidime in ESBL-producing isolates of K pneumoniae.
The importance of infection-control measures has been demonstrated
repeatedly, primarily in the control of outbreaks. Such measures
include implementation of CDC guidelines on isolation and barrier
precautions, cohorting of patients, hand-washing awareness campaigns,
and use of waterless hand-disinfection systems.35
Thus, to
successfully combat antimicrobial resistance in the clinical setting,
both effective infection control and restrictions governing antibiotic
use are required; addressing either issue alone is inadequate.
|
Strategies for the Control of Antimicrobial Resistance
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Two reports36
37
include consensus statements
on the importance of prevention and control of antimicrobial-resistant
microorganisms in the hospital setting, along with guidelines for
hospitals to handle this dilemma. The Society for Healthcare
Epidemiology of America and the Infectious Diseases Society of America
identified the importance of addressing antimicrobial resistance by
developing consensus within hospitals. Table 2
outlines the recommendations of these societies.36
A model
for implementation was proposed in which hospital committees use
external guidelines, such as those of the CDC or Infectious Diseases
Society of America, to develop local policies based on the specific
resistance issues of the institution. The hospital administration
should then assume responsibility for putting these policies into
practice and ensuring staff compliance. Under this model, data from the
programs would be analyzed for outcomes and quality assessment and used
both internally to improve processes further and may also be provided
to outside agencies, such as local and state health departments and the
CDC. The authors further proposed that oversight agencies, such as the
Joint Commission on the Accreditation of Hospitals, incorporate into
their hospital reviews the priority that specific hospitals give to
resistance control, the policies implemented, and the effectiveness of
such plans.36
Another report37
from a multidisciplinary workshop of
experts outlined 10 strategic goals for hospitals to consider in
addressing antimicrobial resistance, 5 of which target antibiotic use
and 5 that relate to infection control. The goals that target
antibiotic use are to (1) optimize prophylactic antimicrobial use prior
to surgical procedures, (2) optimize choice and duration of empiric
antimicrobial use, (3) improve antimicrobial prescribing practices
through educational and administrative means, (4) establish a system
that monitors and provides feedback regarding the occurrence of
resistance, and (5) define and implement guidelines for antimicrobial
use. The goals that target infection control measures are to (1)
develop a means of recognizing significant changes in resistance and
reporting these shifts to staff with a need to know, (2) develop a
system for rapid detection and reporting of resistant organisms in
individual patients so that their caregivers and treating staff are
well informed, (3) increase compliance with basic infection-control
techniques, including hand hygiene and barrier methods, (4) incorporate
detection, prevention, and control of antimicrobial resistance into the
strategic goals of the institution, and (5) develop a plan for
appropriately treating, transferring, discharging, and readmitting
patients known to be colonized with resistant organisms. These 10 goals
can provide a useful map in developing programs to combat antimicrobial
resistance in hospitals.
Through quality-improvement teams, the aforementioned workshop also
outlined processes which hospitals can apply toward specific goals and
measure, with specific outcome measures that can be monitored for each
strategic goal (Table 3
).37
The authors concluded that a "multidisciplinary,
systems-oriented approach, catalyzed by hospital leadership, is
required" to control antimicrobial resistance.37
Specific measures to manage antimicrobial resistance by modifying
patterns of antibiotic use may include restriction of certain classes
of antibiotics, rotating or cycling classes of antibiotics
periodically, or open formularies. Physician education is a critical
component of any successful program to manage antibiotic use, whether
by a restricted formulary, use of antibiotic order forms, requirement
of approval by an infectious disease specialist, or prospective
educational intervention programs. Computerized physician order entry
with decision support and real-time feedback to physicians has been
shown to be an efficient means of antibiotic management.23
A program to address emerging antimicrobial resistance was
implemented at our institution using a multidisciplinary,
quality-improvement approach with support from the hospital
administration and medical staff leadership (Fig 1
). Antibiotic-control and infection-control measures were implemented,
with process and outcome measures for monitoring progress. Education
was followed by application of empiric antibiotic treatment guidelines
and daily prospective antibiotic monitoring (including daily rounds
with review of broad-spectrum antibiotics by infectious disease
physicians and pharmacists in ICU and in non-ICU patients),
surveillance for selected resistant organisms and for nosocomial
infections with these organisms, hand-washing campaigns, and isolation
precautions. These efforts were accompanied by improved utilization of
vancomycin (per CDC criteria) and broad-spectrum antibiotics, and
improved compliance with infection control precautions, followed by a
decrease in the incidence of nosocomial VRE infections and
ß-lactam–resistant Gram-negative bacteria over the subsequent year.
In conclusion, a hospital-wide effort to properly manage antimicrobial
use using a quality-improvement model, with strong institutional
support, can be effective in controlling antimicrobial resistance in
the hospital setting. Education-based strategies with process and
outcome measures and continuous feedback are important for sustaining
support from clinicians, administrators, and other health-care
professionals.
|
Footnotes
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Abbreviations:
CDC = Centers for Disease Control and Prevention;
ESBL = extended-spectrum ß-lactamase;
MRSA = methicillin-resistant Staphylococcus aureus;
VRE = vancomycin-resistant enterococci
|
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TOP
Abstract
Introduction
