George and Morris Critical Care 2010, 14:205

http://ccforum.com/content/14/1/205

REVIEW

Pro/con debate: Should antimicrobial stewardship

programs be adopted universally in the intensive
care unit?
Philip George1 and Andrew M Morris2*

while producing the fewest possible side effects and the

Abstract
lowest risk for subsequent resistance [2]. Antimicrobial
You are director of a large multi-disciplinary ICU. stewardship programs may contain a variety of inter-
You have recently read that hospital-wide antibiotic ventions that are complementary to effective infection
stewardship programs have the potential to improve prevention and control programs.
the quality and safety of care, and to reduce the Inappropriate antimicrobial usage is a significant
emergence of multi-drug resistant organisms and problem, with approximately 50% of antimicrobial usage
overall costs. You are considering starting one of being unnecessary or suboptimal in hospital, community
these programs in your ICU, but are concerned about or ambulatory settings [3,4]. A recent study showed that
the associated infrastructure costs. You are debating approximately 20% of patients admitted to the ICU with
whether it is worth bringing the concept forward to Clostridium difficile-associated diarrhoea were receiving
your hospital’s administration to consider investing in. antibiotics without any obvious evidence of infection,
with an accompanying 28% in-hospital mortality [5]. As a
consequence of indiscriminate antibiotic use, there are
Statement for debate reported increases in the incidence of infections caused
Antibiotic stewardship programs improve patient out- by resistant organisms. A significant correlation was
comes and cost-effectiveness in critically ill patients in demonstrated between the increase in fluoroquinolone
the ICU. prescriptions in Canada from 0.8 to 5.5 per 100 persons
per year and increased ciprofloxacin-resistant Streptococcus
Introduction pneumoniae from 0% to 1.7% [6]. Twelve percent of
Antibiotic stewardship programs are multidisciplinary patients previously exposed to piperacillin-tazobactam
initiatives whose primary aim is to optimize antibiotic were colonized with strains of enterobacteriaceae resis-
usage. The Infectious Disease Society of America (IDSA) tant to this antibiotic [7] and the use of third generation
and the Society for Health Care Epidemiology of America cephalosporins is associated with higher rates of
(SHEA) published guidelines for antimicrobial steward- vancomycin-resistant enterococci and extended-spectrum
ship in 2007 aimed at providing information on how to β-lactamase-producing organisms [8]. Antimicrobial
establish such programs within health care institutions resistance emerging in response to the selective pressure
[1]. Because antibiotics are used heavily in the ICU, exerted by antibiotics is also a clinical phenomenon, with
stewardship programs appear particularly applicable to outbreaks of antibiotic-resistant Pseudomonas aeuroginosa
this setting. Antimicrobial stewardship is broadly defined and Acinetobacter baumanii-calcoaceticus occurring in
as a practice that ensures the optimal selection, dose and ICUs, where a huge antimicrobial pressure is present
duration of antimicrobials and leads to the best clinical [9-11].
outcome for the treatment or prevention of infection Although they are often life-saving, antibiotics can also
cause serious harm to patients, including Clostridium
difficile-associated diarrhoea, antibiotic-resistant infec-
*Correspondence: amorris@mtsinai.on.ca tions and invasive candidiasis [12-14]. Antibiotics also
2
Division of Infectious Diseases, Department of Medicine, Mount Sinai Hospital
and University Health Network, Mount Sinai Hospital, 600 University Avenue,
result in dangerous drug interactions, life-threatening
Suite 415, Toronto, ON M5G 1X5, Canada hypersensitivity reactions, nephrotoxicity, and QT pro-
Full list of author information is available at the end of the article longation, to name a few. Inappropriate antibiotic use
also contributes to rising drug and hospitalisation costs,
© 2010 BioMed Central Ltd © 2010 BioMed Central Ltd and the need to preserve our current antibiotic arsenal
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has assumed greater importance with the paucity of new from an infectious disease fellow and a clinical pharma-
antibiotic development [15]. cist resulted in 1.6 fewer days of parenteral therapy and
cost savings with no adverse effects on clinical response
Pro: There is justification for implementing [23]. Another study demonstrated a sustained decrease in
antibiotic stewardship programs in the ICU parenteral antibiotics over a 7-year period following
Clinicians have long been aware of the risks of antibiotic introduction of a prospective audit with interaction and
resistance associated with inappropriate antibiotic use, feedback [26].
but nonetheless very few effective antibiotic policies have Multiple studies using healthcare information tech-
been implemented, and the problem appears to be even nology, such as computer-assisted decision support
worsening [16]. The costs associated with antibiotic designed to provide treatment recommendations, have
usage are also escalating, with systemic antibiotics being shown significant reductions in the use of antibiotics and
the single most costly drug class over the past decade in greater de-escalation to narrow-spectrum antimicrobials.
non-federal hospitals in the United States. In 2007, Improvements in cost and efficiency of existing steward-
systemic antibiotics accounted for 11.2% of the pharmacy ship programs, and improved physician knowledge
budget of non-federal hospitals [17]. In addition to direct regarding treatment and pathogen prediction were also
pharmacy costs, hospitalisation and other infrastructure noted [27-29]. In addition to improving antimicrobial use
costs are also increased, ultimately resulting in a greater and patient care (including tracking of antibiotic resis-
strain on the healthcare system. Saving antibiotics will tance patterns), such systems can improve surveillance of
save money, and there are a variety of methods to do so. hospital-acquired infections and adverse drug events
Education is the cornerstone of any antibiotic steward- when compared to manual surveillance methods [30,31].
ship program, with prescriber education and implemen- In a 15-month study using a web-based antimicrobial
tation of guidelines and clinical pathways improving approval system linked to national antibiotic guidelines, a
antimicrobial prescribing behaviour. For example, studies sustained reduction in third-generation cephalosporin
using algorithms to shorten the course of antimicrobial prescriptions were accompanied by increased concor-
therapy in ventilator-associated pneumonia led to signifi- dance with antibiotic guidelines [32]. These benefits have
cantly lower antimicrobial therapy usage with reduction also been noted in an ICU-based study, where
in costs, antimicrobial resistance, and super-infections investigators used computerised anti-infective programs
without adversely affecting the length of stay or mortality and were able to document significant reductions in the
[18,19]. The absence of formal antimicrobial stewardship use of excessive drug dosage, adverse drug events and
training programs for infectious diseases fellows, board- length of hospital stay and costs [33].
certified physicians, and pharmacists has recently been a Standardized pre-printed or computer-generated
challenge to the education imperative, however [20]. physician order sets can improve the efficiency of
Preauthorisation (also known as formulary restriction) antibiotic stewardship programs. In a study looking into
requires approval by a pharmacist or physician prior to their benefits in the management of patients with septic
clinical use of an antimicrobial. Although preauthoriza- shock in an emergency department, order sets were
tion is thought to be the most effective method of found to improve initial fluid resuscitation, use of appro-
controlling antimicrobial use, it does not alter the priate antibiotics and 28-day mortality [34]. A recent
duration of therapy or the decision to give or withhold study to evaluate the hospital-wide impact of a standard-
antibiotics. The main benefits of this strategy are the ized order set for the management of severe bacteraemic
supervision of antibiotic use by experts and substantial sepsis has shown that a greater number of patients
cost savings (with some studies demonstrating cost received appropriate initial antibiotic therapy with
savings upwards of US$800,000) [21,22]. decreased incidence of organ failure and improved
Through prospective audit with interaction and survival [35].
feedback, antimicrobial use is reviewed after antimicro- A survey of 670 US hospitals found that implementa-
bial therapy has been initiated and recommendations are tion of guideline-recommended practices to control
made with regard to their appropriateness in terms of antimicrobial use and optimize the duration of empirical
selection, dose, route and duration. Prospective audit therapy was associated with less antimicrobial resistance,
with feedback avoids delays in initiation of therapy and including methicillin-resistant Staphylococcus aureus,
maintenance of prescribers’ autonomy, and can be imple- vancomycin-resistant enterococci, fluoroquinolone-
mented in health care facilities of varying sizes [23,24]. A resistant Escherichia coli and ceftazidime-resistant
large teaching hospital reported a 37% reduction in the Klebsiella species [36]. Given the relationship between
number of days of unnecessary antibiotics use by antimicrobial use and antimicrobial resistance, anti-
decreasing the duration of treatment and by reducing microbial stewardship appears to be a logical first step in
new starts [25]. In another study, antimicrobial suggestions the effort to control antimicrobial resistance.
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The efficacy of antimicrobial stewardship programs has Antibiotic use in ICUs may be the consequence rather
been the subject of a recent Cochrane systematic review, than the cause of resistance, and there is a risk that
examining 66 studies from 1980 to 2003 [37]. The main stewardship, with its emphasis on decreased antibiotic
interventions analyzed in the review were targeted to use, could lead to a substantial increase in patient risk. It
decrease treatment (57 studies), increase treatment is also important to note that neither the published
(6 studies) or both (3 studies). The interventions guidelines nor the important stewardship articles identify
addressed the antibiotic regimen (61 studies), the safety as an endpoint.
duration of treatment (10 studies), the timing of first dose Another potentially adverse consequence of antibiotic
(6 studies), or the decision to prescribe antibiotics restriction is the emergence of new resistance patterns
(1 study). Optimization of antibiotic use was seen in 81% replacing the old ones. A study documenting the
of the studies aimed at improving antimicrobial introduction of new guidelines that restricted cephalo-
utilization. Significant improvements in microbiological sporin use was primarily aimed at reducing the incidence
outcome (for example, prevalence of antibiotic-resistant of cephalosporin-resistant Klebsiella spp. Even though
bacteria) and clinical outcomes (for example, mortality the primary aim was achieved, this occurred at the
and length of hospital stay) were also noted in some expense of increased imipenem usage with the subse-
studies. Recent observational studies (subsequent to the quent increase in incidence of imipenem-resistant
Cochrane review) have demonstrated that reducing P. aeuroginosa by about 69% [46]. Thus, formulary
antimicrobial pressure correlates with improved anti- restriction does not necessarily prevent the potential
microbial susceptibility of pathogens [38,39]. overuse of available broad spectrum antibiotics in routine
Antimicrobial stewardship programs using the methods practice [47]. Rather, a significant change in clinical
described above will promote the optimal use of anti- thinking to reduce our dependence on and abuse of
microbial therapy, leading to the best clinical outcome antibiotics is needed.
for patients. The relative paucity of outcome data Antimicrobial stewardship programs form only one
demonstrating the benefits of antimicrobial stewardship strategy for minimizing the incidence of resistance, and
is likely due to its infancy: antimicrobial stewardship must partner with infection control measures, including
programs today are where infection control programs surveillance, outbreak investigation, disinfection and
were roughly 30 years ago [40,41]. Because antimicrobials sterilization, and environmental hygiene. Of the studies
are widely prescribed in the ICU, with an apparent reported to be beneficial, it remains unclear as to whether
mortality benefit with appropriate therapy [42], using the the reported improvements in resistance rates are related
best available methods to optimize their use through to antimicrobial stewardship programs, infection control
antimicrobial stewardship is crucial. measures or both.
Although healthcare information technology is believed
Con: The evidence for effectiveness of to be a key component of antimicrobial stewardship
antimicrobial stewardship is lacking programs, detailed information on the resources required
Despite the publication of guidelines for improving the to implement and maintain these sophisticated computer
use of antimicrobial agents in the United States, a great programs is not widely available. It is also not clear
deal of scepticism about the effectiveness and accepta- whether the reported cost-effectiveness of many of these
bility of antimicrobial stewardship programs persists. In stewardship programs takes into account the overall cost
a survey conducted by the United States Centers for of these interventions above and beyond the pharmacy-
Disease Control and Prevention’s National Nosocomial related costs and expenses associated with development
Infections Surveillance Systems, only 40% of selected and distribution of educational materials.
hospitals had antibiotic restriction policies and 60% used Another challenge to implementing antimicrobial
stop orders [43]. Antimicrobial stewardship programs are stewardship in the ICU deals with the confidence inten-
also 50% less likely to be implemented in community sivists have in the clinical judgement of the stewardship
hospitals compared to academic hospitals [44]. Two years physician. A junior physician might be a less effective
after the publication of the IDSA/SHEA antibiotic antimicrobial stewardship team member because of a
stewardship guidelines [1] only 48% of survey respon- perceived or real lack of knowledge and experience [48],
dents stated that their hospital had a program [41]. but may be utilized because the ‘price is right’. In the
Reduction in the incidence of bacterial resistance is survey by Pope and colleagues [41], personnel shortages
touted as the main advantage of antimicrobial steward- (55%), financial considerations (36%), and resistance from
ship programs, but lacks scientific evidence to support it. administration (14%) were frequent barriers to establishing
In a recent survey of 33 US hospitals, there was no antimicrobial stewardship programs. Opposition from
significant correlation between antibiotic guideline prescribing physicians was a barrier to establishing an
adherence by physicians and resistance rates [45]. antimicrobial stewardship program in about 27% of cases.
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While antimicrobial stewardship programs have rather adverse consequences. All ICUs should have an anti-
consistently shown significant improvement in anti- microbial stewardship program accompanied by a system
microbial utilization, there are very few studies examin- to monitor clinically meaningful outcomes such as
ing meaningful clinical outcome measures such as mortality and length of stay. Monitoring such outcomes
duration of hospitalization, mortality rates, or even presents an excellent opportunity for infection control
quality indicators such as patient satisfaction. In the and other patient quality and safety initiatives, whose
systematic review by the Cochrane Collaboration on aims include prevention of healthcare-associated infec-
antibiotic stewardship programs, clinical outcomes such tions and control of antibiotic-resistant organisms. In the
as mortality and length of hospital stay were reported in absence of such monitoring, antimicrobial stewardship
only 15% of the studies [37]. In the 2008 survey by Pope programs are nothing more than programs to reduce
and colleagues [41], only 25% of respondents reported antimicrobial use with a largely unproven effect on
clinical outcomes. Also, none of the studies report any patient care. Close collaboration between critical care,
significant reduction in antimicrobial side effects as a infectious disease, infection control, medical informatics,
result of these interventions. microbiology, and pharmacy staff are needed for the
success of an antimicrobial stewardship program. From
Conclusion our experience, leadership and a culture that embraces
Hospitals are increasingly implementing antimicrobial change is critical to implementation of a successful
stewardship programs in response to increasing anti- antimicrobial stewardship program.
microbial resistance (despite aggressive infection control
practices), coupled with fewer novel antimicrobials and Abbreviations
IDSA = Infectious Diseases Society of America; SHEA = Society for Healthcare
increasing antimicrobial costs. There is little question Epidemiology of America.
that antimicrobial use is causally related to antimicrobial
resistance, and there is growing evidence that steward- Author details
1
Division of Critical Care, Department of Medicine, Mount Sinai Hospital and
ship measures aimed at optimizing antimicrobial use can University Health Network, Mount Sinai Hospital, 600 University Avenue, Suite
reduce antimicrobial resistance while reducing associated 18-206, Toronto, ON M5G 1X5, Canada
costs. Being major foci of antimicrobial resistance and 2
Division of Infectious Diseases, Department of Medicine, Mount Sinai Hospital
and University Health Network, Mount Sinai Hospital, 600 University Avenue,
the largest consumers of antimicrobials in most hospitals, Suite 415, Toronto, ON M5G 1X5, Canada
ICUs can expect to benefit most from antimicrobial
stewardship programs. Competing interests
Full implementation of antibiotic stewardship programs AMM is Director of the Antimicrobial Stewardship Program at Mount Sinai
Hospital and University Health Network in Toronto. He receives salary support
requires significant investment, however. In the present for his work in this capacity. There are no other competing interests.
economic climate, barriers to implementing such
programs include personnel shortages, financial cutbacks, Published: 25 February 2010
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Cite this article as: George P, Morris AM: Pro/con debate: Should
infectious diseases specialist consultant on the appropriateness of
antimicrobial stewardship programs be adopted universally in the
antimicrobial therapy prescription in an intensive care unit. Am J Infect
intensive care unit? Critical Care 2010, 14:205.
Control 2008, 36:283-290.