## Abstract

Preventing, reducing, and controlling the emergence of antimicrobial-resistant organisms is a major public health challenge requiring the participation of the entire medical community and public health agencies. Antimicrobial stewardship programs (ASPs) have the potential to integrate the many and sometimes disparate individuals and organizations that rely on antimicrobial agents in an effort to better control antimicrobial prescribing, possibly minimizing the emergence of resistant organisms. Developing and implementing ASPs can be a major challenge for community-based hospitals. In addition to specific and localized patterns of resistance—a consideration for every hospital—community hospitals must develop strategies that appropriately conform to their size, staffing, personnel, and infrastructure. This article reviews the ASP strategies and resources currently available to community hospitals for improving if, when, and how antimicrobial agents are prescribed and delivered.

The last several decades have witnessed a worldwide increase in the prevalence of antimicrobial-resistant pathogens [1]. Infections caused by these pathogens result in prolonged hospital stays, higher treatment costs, and, most importantly, substantially worse patient outcomes, including higher mortality rates [2–4]. The Infectious Diseases Society of America (IDSA) has identified Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacter species (the so-called ESKAPE pathogens) as emerging predominant causes of hospital-associated infections that are resistant to multiple antimicrobial agents (Figure 1) [2, 5, 6]. Outside the hospital, community-acquired methicillin-resistant Staphylococcus aureus (MRSA) is now a leading cause of community-acquired skin and soft-tissue infections, including necrotizing fasciitis [7–13], and is also associated with community-acquired bacteremia, urinary tract infection (UTI), and pneumonia [8]. Infection with Clostridium difficile, which is associated with antimicrobial use and resistance in some cases, is also increasing in prevalence [14–16]. Although the phenomenon of antimicrobial resistance and spread of antimicrobial-resistant pathogens can be attributed to many factors within and without the purview of physicians, there is a well-established relationship between antimicrobial prescribing practices and the emergence of antimicrobial-resistant pathogens [17–19].

Figure 1.

Antimicrobial resistance for selected pathogens over time [2]. Reprinted with permission from Wenzel et al.

Figure 1.

Antimicrobial resistance for selected pathogens over time [2]. Reprinted with permission from Wenzel et al.

Preventing, reducing, and controlling the emergence of antimicrobial-resistant organisms in hospitals, long-term-care facilities, and other institutions, as well as in the community, is a major public health challenge requiring the participation of the entire medical community and public health agencies. Antimicrobial stewardship programs (ASPs) have the potential to integrate the many and sometimes disparate individuals and organizations that rely on antimicrobial agents in an effort to better control antibiotic prescribing and improve antimicrobial selection, dosing, and administration, possibly minimizing the emergence of resistant organisms, the spread of infections, and other unintended consequences of antimicrobial use.

Developing and implementing ASPs can be a major logistic, clinical, and sometimes political challenge for any institution, some of which are unique to community-based hospitals. In addition to specific and localized patterns of resistance—a consideration for every hospital—community hospitals must develop strategies that appropriately conform to their size, staffing, personnel, and infrastructure. ASPs must not be viewed strictly as the province of the large-scale hospitals with full-time infectious diseases (ID) physicians and pharmacists. Rather, antimicrobial stewardship should be thought of as a menu of interventions that are adaptable and customizable concepts that can be designed to fit the infrastructure of institutions of any hospital, no matter what the size.

## ANTIMICROBIAL STEWARDSHIP STRATEGIES

In the broadest sense, the goals of an ASP are to prevent or slow the emergence of antimicrobial resistance; optimize selection, dose, and duration of treatment; reduce adverse drug events including secondary infection, and lower rates of morbidity and mortality and length of hospital stay. When such goals are achieved, reductions in health care expenditures are often possible as well. However, cost savings are not, and should not be, the primary ambition of an ASP. Cost savings are a natural consequence of improved and reduced antimicrobial use.

ASP strategies are broadly divided into 2 categories: prior-authorization strategies and prospective audit and feedback strategies (Table 1)[20]. Prior-authorization strategies are based on restricting physician access to some or all antimicrobial agents on formulary [17]. To use an antimicrobial agent, the prescriber must receive approval from an authorizing individual or committee before the agent will be dispensed. Such strategies significantly reduce antimicrobial use and misuse. However, prior-authorization strategies are limited by the availability of authorizing personnel, bureaucracy, and physician willingness to work within the system. One academic medical center with a prior-approval ASP active between 8 AM and 10 PM found that orders for restricted agents increased significantly in the 60 minutes after ASP approvals had ended for the evening (57.0% vs 49.9% during other times, P = 0.02) [21]. Interestingly, these prescriptions were more often discontinued (that is, they were eventually found inappropriate) than were prescriptions filled during the active-ASP time period. The study suggests that physicians were circumventing the prior-approval process to obtain restricted agents and that those agents were frequently inappropriate choices. Other authors have documented inaccuracies in the information provided to restricted-access ASPs [22].

Table 1.

Potential Advantages and Disadvantages of IDSA/SHEA Core Strategies and Supplemental Elements of Antimicrobial Stewardship Programs [20]

 Core strategies Advantages Disadvantages Prospective audit with direct intervention and feedback • May reduce inappropriate antimicrobial use• May serve an educational purpose to modify future prescribing• Allows prescribers to maintain autonomy • Difficulty identifying patients with inappropriate therapy and communicating with prescribers Formulary restriction and preauthorization requirements • May result in immediate and substantial reductions in antimicrobial use and costs • May increase staffing requirements• May delay order implementation while approval is obtained from an authorized prescriber, with the potential for adverse patient outcomes• May increase use of and resistance to alternative antimicrobial agents• Perceived loss of prescriber autonomy Supplemental elements Education • May influence prescribing behavior and promote acceptance of ASP strategies • Only marginally effective in modifying prescribing behavior when used without active intervention Evidence-based guidelines and clinical pathways • May improve antimicrobial use and eliminate practice variations • Adherence may be poor Antimicrobial cycling (not routinely recommended in IDSA/SHEA guidelines) • May minimize resistance by providing diversity in antimicrobial use • Insufficient data available demonstrating long-term effectiveness in reducing antimicrobial resistance• Many patients excluded because of drug allergies, toxicity, or other concerns• Potential of nonadherence due to prescriber lack of awareness of currently scheduled agent• May increase antibiotic costs Antimicrobial order forms • May reduce inappropriate antimicrobial use• May facilitate implementation of guidelines and clinical pathways • Potential for inappropriate interruption in therapy due to automatic stop orders Combination therapy (not routinely recommended in IDSA/SHEA guidelines) • May improve clinical outcomes and prevent resistance in certain types of patients and situations • Often redundant and unnecessary• nsufficient data available demonstrating improved clinical outcomes and prevention of resistance Streamlining or de-escalation of therapy • Reduces antimicrobial exposure, selection of resistant pathogens, and health care costs • Prescriber reluctance to de-escalate therapy when cultures are negative and clinical improvement has been observed Dose optimization • Tailors therapy to patient characteristics, causative organism, site of infection, and pharmacokinetic and pharmacodynamic characteristics of the antimicrobial agent • Nursing staff concerns about incompatibilities when prolonged infusions are used based on pharmacokinetic considerations Parenteral to oral conversion • May decrease length of hospital stay and health care costs• May reduce the risk of complications from intravenous access • Difficulty identifying patients in whom conversion is appropriate
 Core strategies Advantages Disadvantages Prospective audit with direct intervention and feedback • May reduce inappropriate antimicrobial use• May serve an educational purpose to modify future prescribing• Allows prescribers to maintain autonomy • Difficulty identifying patients with inappropriate therapy and communicating with prescribers Formulary restriction and preauthorization requirements • May result in immediate and substantial reductions in antimicrobial use and costs • May increase staffing requirements• May delay order implementation while approval is obtained from an authorized prescriber, with the potential for adverse patient outcomes• May increase use of and resistance to alternative antimicrobial agents• Perceived loss of prescriber autonomy Supplemental elements Education • May influence prescribing behavior and promote acceptance of ASP strategies • Only marginally effective in modifying prescribing behavior when used without active intervention Evidence-based guidelines and clinical pathways • May improve antimicrobial use and eliminate practice variations • Adherence may be poor Antimicrobial cycling (not routinely recommended in IDSA/SHEA guidelines) • May minimize resistance by providing diversity in antimicrobial use • Insufficient data available demonstrating long-term effectiveness in reducing antimicrobial resistance• Many patients excluded because of drug allergies, toxicity, or other concerns• Potential of nonadherence due to prescriber lack of awareness of currently scheduled agent• May increase antibiotic costs Antimicrobial order forms • May reduce inappropriate antimicrobial use• May facilitate implementation of guidelines and clinical pathways • Potential for inappropriate interruption in therapy due to automatic stop orders Combination therapy (not routinely recommended in IDSA/SHEA guidelines) • May improve clinical outcomes and prevent resistance in certain types of patients and situations • Often redundant and unnecessary• nsufficient data available demonstrating improved clinical outcomes and prevention of resistance Streamlining or de-escalation of therapy • Reduces antimicrobial exposure, selection of resistant pathogens, and health care costs • Prescriber reluctance to de-escalate therapy when cultures are negative and clinical improvement has been observed Dose optimization • Tailors therapy to patient characteristics, causative organism, site of infection, and pharmacokinetic and pharmacodynamic characteristics of the antimicrobial agent • Nursing staff concerns about incompatibilities when prolonged infusions are used based on pharmacokinetic considerations Parenteral to oral conversion • May decrease length of hospital stay and health care costs• May reduce the risk of complications from intravenous access • Difficulty identifying patients in whom conversion is appropriate

NOTE. ASP, antimicrobial stewardship program; IDSA, Infectious Diseases Society of America; SHEA, Society for Healthcare Epidemiology of America. [20]

Reprinted with permission of the American Society of Health-System Pharmacists, Inc.

In prospective audit and feedback models for ASPs, pharmacists or ID specialists audit antimicrobial use, and changes and interventions are performed as needed [17]. These ASP strategies tend to be more flexible than are prior-approval strategies and facilitate patient-specific care. Audits are conducted after patients have undergone diagnostic studies and have received empiric therapy, which may facilitate implementation of pathogen-specific treatment strategies, and treatment tailored to individual patient characteristics and responses to initial therapy. Prospective audit and feedback strategies are limited by the logistic challenge of identifying patients receiving inappropriate therapy, the availability of knowledgeable staff to perform the reviews, constructive communication with prescribers, and physician willingness to accept recommendations. It is definitely the more time-consuming of the 2 primary approaches for ASPs.

These strategies and supplemental components, such as education, evidence-based (institution-specific) guidelines and clinical pathways, parenteral to oral strategies, and others (Table 1) [20], are not mutually exclusive, and combinations are possible, depending on local resources, needs, and practices. For example, some hospitals restrict access to specific agents while auditing the use of others. The selection of strategies should conform to the resources of an individual hospital, and ASPs are likely to differ among community hospitals and large-scale tertiary facilities.

## CURRENT STATE OF COMMUNITY HOSPITALS

To understand the potential and challenges for widespread development and implementation of ASPs in community hospitals, it is important to also understand the resources available in today’s community hospitals. The HealthTrust Purchasing Group (HPG), which includes more than 1400 for-profit, nonprofit, teaching, and nonteaching hospitals, the majority of which are community-based institutions, recently conducted a hospital facilities and resources survey focused on antimicrobial use and management [Ed Septimus, MD, unpublished data, 2010].

A total of 568 hospitals participated in the survey, ∼80% of which had between 25 and 300 beds. An overview of hospital resources is detailed in Table 2. Most hospitals, but not all, reported having infection-control committees (80.0%), and 78.3% had on-site microbiology capabilities. Nearly 93% of hospitals produced an antibiogram, but, of these, only 12.1% produced unit-specific antibiograms. In terms of personnel, hospitalists were on staff in 73.4% of hospitals, and 58.8% had an ID specialist.

Table 2.

HealthTrust Purchasing Group Survey Results: Current Antimicrobial Stewardship Program Use and Resources

 Resources Respondents (%) Infection control committee 80.0 Microbiology laboratory 78.3 Hospitalists 73.4 ID specialist 58.8 Clinical pharmacy program 55.0 Pharmacy clinical coordinator 44.1 Intensivists 39.0 Antimicrobial subcommittee 15.4 ID pharmacist 7.0 Other 5.7 Point person for program Pharmacist 64.0 Physician 5.2 Nurse 1.7 Other 0.4 None identified 28.3 Antibiogram 92.7 Unit breakout 12.1 Antimicrobial restriction program (at least 1 agent) 60.0 Intravenous to oral program 72.0 Dose–optimization program 55.7
 Resources Respondents (%) Infection control committee 80.0 Microbiology laboratory 78.3 Hospitalists 73.4 ID specialist 58.8 Clinical pharmacy program 55.0 Pharmacy clinical coordinator 44.1 Intensivists 39.0 Antimicrobial subcommittee 15.4 ID pharmacist 7.0 Other 5.7 Point person for program Pharmacist 64.0 Physician 5.2 Nurse 1.7 Other 0.4 None identified 28.3 Antibiogram 92.7 Unit breakout 12.1 Antimicrobial restriction program (at least 1 agent) 60.0 Intravenous to oral program 72.0 Dose–optimization program 55.7

NOTE. ID, infectious diseases.

Only 15.4% of respondents reported having an antimicrobial committee, a figure that appears consistent with international surveys, which found antimicrobial committees in up to ∼18% of hospitals [23, 24]. Pharmacists served as the point person for 64.0% of the antimicrobial committees. Only 5.2% of responding hospitals reported that a physician was the point person for an antimicrobial committee, and 28.3% did not identify a point person. Independent of who serves as the coordinating party for ASPs, it is essential to have involvement from physicians, pharmacists, and microbiologists alike in order to ensure program success.

In the HPG survey, access to at least some antimicrobial agents was restricted in 60.0% of hospitals. Agents with activity against MRSA were the most commonly restricted (72%). Programs for converting intravenous to oral therapy were active in 72.0% of hospitals, but only 55.7% had dose-optimization programs.

Dose-optimization programs are an important strategy in improving how antimicrobial agents are administered. These strategies are based on pharmacokinetic and pharmacodynamic (PK/PD) principles and seek to optimize dosing by maximally exploiting the time-dependent or concentration-dependent activity of antimicrobial agents [25]. In clinical trials, PK/PD-based strategies have produced cure rates comparable to those of standard dosing strategies but with reductions in the total duration of treatment and drug exposure, factors that may help reduce or prevent the emergence of antimicrobial-resistant pathogens [26, 27]. Even more importantly, dose optimization is a key patient safety function when antibiotics with narrow therapeutic to toxicity ratios are used.

Overall, the survey results indicate a diversity of resources in community hospitals, and all hospitals included in the survey had at least some resources at their disposal to implement ASPs and better manage how antimicrobial agents are used. The small number of antimicrobial committees suggests that, although select agents may be restricted, antimicrobial use largely goes unmonitored and unaudited in community hospitals and that even minimal education and audit strategies could produce substantial improvements in antimicrobial use. Data are limited in terms of what is effective and how to measure outcomes.

## PIVOTAL ROLE OF THE PHARMACIST

Several key elements are needed to make ASPs work in community hospitals. First and foremost is strong buy-in and support from senior leadership and the administration, and an effective and local “champion”—the physician, pharmacist, or hospitalist who takes ownership of the mission for building an ASP. Hospitalists now care for 20%–30% of inpatients and are already in position to liaise among various specialists, hospital wards, and ASPs [28]. The champion could be any physician, pharmacist, or hospitalist with a basic knowledge of antimicrobial agents, good interpersonal and leadership skills, and a visible and strong commitment to ASPs.

The 2007 IDSA ASP guidelines suggest that ASPs be administered by either ID specialists and/or ID pharmacists [17]. Unfortunately, there are too few ID specialists, and, as seen in the HPG survey, more than 40% of community hospitals do not have an ID specialist on staff. ID pharmacists, too, are in limited supply, and, often, community hospitals cannot support a full-time ID pharmacist. Moreover, there are simply not enough pharmacists trained in antimicrobial stewardship, which is itself a specialized pharmacy practice. Consequently, as the survey also showed, most often the point person for antimicrobial committees is a pharmacist, a role that is encouraged and endorsed by the American Society of Health-System Pharmacists [20, 29]. For pharmacists willing to take on the mantle of ASP leader with the provisions of adequate time, resources, and compensation, a variety of educational opportunities are available, as are ASP certification programs designed to help pharmacists who have not trained formally in antimicrobial stewardship (Table 3) [20].

Table 3.

Informal Infectious Diseases (ID) Educational Opportunities for Hospital Pharmacists [20]

 Identify a mentor with ID expertise for case discussions Attend rounds with an ID physician “Shadow” a clinical microbiologist Join ID professional organizations Attend ID professional meetings Participate in ID-related continuing education programs Subscribe to ID list-servs Sign up for electronic alerts with tables of contents for ID-related periodicals Read basic primers, review articles, and practice guidelines on ID topics Conduct or participate in an ID journal club Attend ID-related morbidity and mortality case reviews
 Identify a mentor with ID expertise for case discussions Attend rounds with an ID physician “Shadow” a clinical microbiologist Join ID professional organizations Attend ID professional meetings Participate in ID-related continuing education programs Subscribe to ID list-servs Sign up for electronic alerts with tables of contents for ID-related periodicals Read basic primers, review articles, and practice guidelines on ID topics Conduct or participate in an ID journal club Attend ID-related morbidity and mortality case reviews

NOTE. Reprinted with permission of the American Society of Health-System Pharmacists, Inc.

The responsibilities of the pharmacist ASP leader, in the broadest sense, are to encourage the optimal use of antimicrobial agents by promoting interdisciplinary collaboration within the hospital and auditing and guiding the selection, dosing, timing, de-escalation, and discontinuation of antimicrobial therapy [20, 29]. The pharmacist ASP administrator should be directly involved with infection-prevention and infection-control strategies and play a role in the education of physicians and health care workers, patients, and the public.

Multiple studies have documented improved antimicrobial use and patient outcomes with pharmacist-led ASPs [30–32]. Gross and coworkers [30] compared antimicrobial use recommendations of pharmacist-led ASP and those made by ID fellows and found that the ASP performed significantly better, with higher rates of appropriate antimicrobial use (87% vs 47%, respectively; P < 0.001), higher cure rates (64% vs 42%, respectively; P = 0.007), and a lower incidence of treatment failures (15% vs 28%, respectively; P = 0.03). There was no difference in economic outcomes between strategies. Investigators noted several possible explanations for the findings. First, the program director, who had extensive knowledge of antimicrobial agents, provided pharmacists with frequent support and guidance, and the program was the primary responsibility of a pharmacist whose recommendations were considered in performance evaluations. The ID fellows did not have the same vested interest. ID fellows considered the program burdensome, distracting, and of little educational value.

Other studies have documented improved clinical and economic outcomes with pharmacist-led ASPs [31, 32]. A 2005 study from Bond and coworkers [32] reported aminoglycoside and vancomycin use in 199,082 Medicare patients treated in 961 hospitals with and without pharmacist-led ASPs. In hospitals without pharmacist-led ASPs, mortality rates were 6.7% higher (P < 0.001) and length of hospital stay 12.3% longer (mean, 13 vs 11.6 days; P < 0.001) than in hospitals with pharmacist-led treatment (Figure 2) [32]. Respective rates of hearing loss and renal impairment—2 serious adverse events associated with aminoglycoside use—were 46.4% and 34.0% higher, respectively, in hospitals without pharmacist leadership (P < 0.001) (Figure 2). In economic terms, total Medicare, drug, and laboratory charges were all significantly higher in hospitals without pharmacist-led treatment (6.3%, 8.2%, and 7.8% higher, respectively; P < 0.001). In total, hospitals without pharmacist-led ASPs had $140,745,924 in excess total Medicare charges. Figure 2. Clinical outcomes for patients treated with aminoglycosides or vancomycin in hospitals with and without a pharmacist-led antimicrobial stewardship program [32]. Figure 2. Clinical outcomes for patients treated with aminoglycosides or vancomycin in hospitals with and without a pharmacist-led antimicrobial stewardship program [32]. Similar outcomes were reported when comparing antimicrobial prophylaxis in 242,704 Medicare patients requiring surgery in 860 hospitals with and without pharmacist-led ASPs (19% vs 81%, respectively) [31]. In this study, too, pharmacist management was associated with significantly lower overall mortality rates, shorter hospital stays, fewer complications, and overall lower costs (Table 4). Table 4. Clinical and Economic Outcomes in Surgical Patients in Hospitals With and Without a Pharmacist-Led Antimicrobial Stewardship Program (ASP) [31]  ASP No ASP Increase (%) P value Death, % 2.7 4.1 52.1 <.001 No. of patient days 456 698 1 644 596 10.2 <.001 Mean total Medicare charges,$ 31 580 32 560 3.1 <.001 Mean total drug charges, $4029 4321 7.2 .005 Mean laboratory charges,$ 2721 2795 2.7 .0056 Postoperative infections, % 1.13 1.72 34.3 <.001
 ASP No ASP Increase (%) P value Death, % 2.7 4.1 52.1 <.001 No. of patient days 456 698 1 644 596 10.2 <.001 Mean total Medicare charges, $31 580 32 560 3.1 <.001 Mean total drug charges,$ 4029 4321 7.2 .005 Mean laboratory charges, \$ 2721 2795 2.7 .0056 Postoperative infections, % 1.13 1.72 34.3 <.001

NOTE. Originally published in Bond CA, Raehl CL. Clinical and economic outcomes of pharmacist-managed antimicrobial prophylaxis in surgical patients. Am J Health Syst Pharm. 2007;64:1935–1942. © 2007, American Society of Health-System Pharmacists, Inc. All rights reserved. Reprinted with permission. (R1105)

## ROLE OF PUBLIC HEALTH AGENCIES

Antimicrobial agents are a shared resource and, perhaps, the only drugs where use in one patient can impact the effectiveness in another. When used inappropriately, society, not just a single patient, suffers the consequences. Public health agencies therefore also have a role in the development of ASPs in community hospitals and other institutions and bring unique capabilities to planning and implementation.

ASPs are necessarily multidisciplinary endeavors that, in addition to physicians, pharmacists, infection preventionists, and microbiologists, include nurses, allied health professionals, payers, researchers, and government agencies. Government agencies have the resources and clout to bring together these key players and promote collaboration; they also have the resources and knowledge base to develop best practices and widely disseminate information. Importantly, government agencies may be the only institutions with the authority to institute mandates, control regulations, and moderate/control reporting practices.

Several government-sponsored programs designed to improve antimicrobial use in the community hospitals have already been conducted. The current initiative of the Centers for Disease Control and Prevention (CDC) is Get Smart for Healthcare (www.cdc.gov/getsmart/healthcare/)—a multidisciplinary approach to improving antimicrobial use in hospitals by facilitating the widespread development and implementation of antimicrobial stewardship interventions. An initial multidisciplinary expert panel identified several key goals for the program. These included incorporating in-hospital infection prevention and infection-control initiatives into ASPs, convincing administrators/payers of the importance of ASPs, making ASPs easier to implement, and maximizing the involvement of physicians and pharmacists.

The initiative’s goals for improving antimicrobial measurement include switching from defined daily doses to days of therapy and enabling individual hospitals to perform in-hospital and interhospital benchmarking. To facilitate this, the CDC has revised the Antibiotic Use and Resistance module of the National Healthcare Safety Network to allow electronic submission of use data. This not only will facilitate monitoring of use at individual facilities but also will be a first step toward national use benchmarking. Additionally, it should be remembered that the primary focus of ASPs is improving patient outcomes. With Accountable Care Organization philosophies, institutions will be “at risk” for poor outcomes as a result of choosing the wrong antimicrobial, the wrong dose, or wrong duration of administration. Readmission rates for failed antimicrobial therapy will not be acceptable. Using more expensive antimicrobials that may reduce failure rates or reduce length of stay should be considered, instead of shelved, in spite the fact that they may increase pharmacy expenses. Cost cutting does not equate, by definition, to antimicrobial stewardship. Looking across the continuum of health care, our current paradigm of evaluating costs in relation to “silos” could result in “anti-stewardship”. We should remember that the most expensive therapy is the one that does not work.

## CONCLUSIONS

For ASPs to successfully improve antimicrobial use and thereby delay and/or prevent the emergence of antimicrobial-resistant pathogens, it is important that ASPs be developed on a broad scale. Stewardship programs are not just strategies for large-scale hospitals; ASPs are needed and viable in community hospitals as well. With clear and focused leadership from an ID specialist or pharmacist or, more often, a nonspecialist pharmacist, implementation of ASPs is feasible and effective.

Supplement sponsorship.  This article was published as part of a supplement entitled “Antimicrobial Stewardship for the Community Hospital: Practical Tools and Techniques for Implementation,” jointly sponsored by the University of Cincinnati and Rockpointe Corporation, ACPE credit provided by Potomac Center for Medical Education, and supported by an educational grant from Ortho-McNeil.

Potential conflicts of interest.  Both authors received financial support from Ortho-McNeil Janssen for preparation of this manuscript. E. S. has received institutional grant support from AHRQ and the CDC and received payment for lectures from Cubist.

All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed in the Acknowledgments section.

## References

1.
Talbot
GH
J
Edwards
JE
Jr
Gilbert
D
Scheld
M
Bartlett
JG
Bad bugs need drugs: an update on the development pipeline from the Antimicrobial Availability Task Force of the Infectious Diseases Society of America
Clin Infect Dis
,
2006
, vol.
42
(pg.
657
-
68
)
2.
Wenzel
RP
Bearman
G
Edmond
MB
Screening for MRSA: a flawed hospital infection control intervention
Infect Control Hosp Epidemiol
,
2008
, vol.
29
(pg.
1012
-
8
)
3.
Vincent
JL
Rello
J
Marshall
J
, et al.  .
International study of the prevalence and outcomes of infection in intensive care units
JAMA
,
2009
, vol.
302
(pg.
2323
-
9
)
4.
European Centre for Disease Prevention and Control, European Medicines Agency
ECDC/EMEA Joint Technical Report: the bacterial challenge: time to react

5.
Rice
LB
Federal funding for the study of antimicrobial resistance in nosocomial pathogens: no ESKAPE
J Infect Dis
,
2008
, vol.
197
(pg.
1079
-
81
)
6.
Boucher
HW
Talbot
GH
JS
, et al.  .
Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America
Clin Infect Dis
,
2009
, vol.
48
(pg.
1
-
12
)
7.
Miller
LG
Perdreau-Remington
F
Rieg
G
, et al.  .
Necrotizing fasciitis caused by community-associated methicillin-resistant Staphylococcus aureus in Los Angeles
N Engl J Med
,
2005
, vol.
352
(pg.
1445
-
53
)
8.
Fridkin
SK
Hageman
JC
Morrison
M
, et al.  .
Methicillin-resistant Staphylococcus aureus disease in three communities
N Engl J Med
,
2005
, vol.
352
(pg.
1436
-
44
)
9.
Kaplan
SL
Hulten
KG
Gonzalez
BE
, et al.  .
Three-year surveillance of community-acquired Staphylococcus aureus infections in children
Clin Infect Dis
,
2005
, vol.
40
(pg.
1785
-
91
)
10.
King
MD
Humphrey
BJ
Wang
YF
Kourbatova
EV
Ray
SM
Blumberg
HM
Emergence of community-acquired methicillin-resistant Staphylococcus aureus USA 300 clone as the predominant cause of skin and soft-tissue infections
Ann Intern Med
,
2006
, vol.
144
(pg.
309
-
17
)
11.
Moran
GJ
Amii
RN
Abrahamian
FM
Talan
DA
Methicillin-resistant Staphylococcus aureus in community-acquired skin infections
Emerg Infect Dis
,
2005
, vol.
11
(pg.
928
-
30
)
12.
Moran
GJ
A
Gorwitz
RJ
, et al.  .
Methicillin-resistant S. aureus infections among patients in the emergency department
N Engl J Med
,
2006
, vol.
355
(pg.
666
-
74
)
13.
Liu
C
Bayer
A
Cosgrove
SE
, et al.  .
Clinical practice guidelines by the infectious diseases society of America for the treatment of methicillin-resistant Staphylococcus aureus infections in adults and children
Clin Infect Dis
,
2011
, vol.
52
(pg.
285
-
92
)
14.
Wilcox
MH
Mooney
L
Bendall
R
Settle
CD
Fawley
WN
A case-control study of community-associated Clostridium difficile infection
J Antimicrob Chemother
,
2008
, vol.
62
(pg.
388
-
96
)
15.
Rabatsky-Ehe
T
Purviance
K
Mlynarski
D
, et al.  .
Surveillance for community-associated Clostridium difficile–Connecticut, 2006
MMWR Morb Mortal Wkly Rep
,
2008
, vol.
57
(pg.
340
-
3
)
16.
Delaney
JA
Dial
S
Barkun
A
Suissa
S
Antimicrobial drugs and community-acquired Clostridium difficile–associated disease, UK
Emerg Infect Dis
,
2007
, vol.
13
(pg.
761
-
3
)
17.
Dellit
TH
Owens
RC
McGowan
JE
Jr.
, et al.  .
Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America guidelines for developing an institutional program to enhance antimicrobial stewardship
Clin Infect Dis
,
2007
, vol.
44
(pg.
159
-
77
)
18.
Neuhauser
MM
Weinstein
RA
Rydman
R
Danziger
LH
Karam
G
Quinn
JP
Antibiotic resistance among gram-negative bacilli in US intensive care units: implications for fluoroquinolone use
JAMA
,
2003
, vol.
289
(pg.
885
-
8
)
19.
Hecker
MT
Aron
DC
Patel
NP
Lehmann
MK
Donskey
CJ
Unnecessary use of antimicrobials in hospitalized patients: current patterns of misuse with an emphasis on the antianaerobic spectrum of activity
Arch Intern Med
,
2003
, vol.
163
(pg.
972
-
8
)
20.
Rapp
RP
Kaye
KS
Canon
SB
Hermsen
ED
DePestel
DD
A hospital pharmacist’s guide to antimicrobial stewardship programs

21.
LaRosa
LA
Fishman
NO
Lautenbach
E
Koppel
RJ
Morales
KH
DR
Evaluation of antimicrobial therapy orders circumventing an antimicrobial stewardship program: investigating the strategy of “stealth dosing”
Infect Control Hosp Epidemiol
,
2007
, vol.
28
(pg.
551
-
6
)
22.
DR
Paris
S
Fishman
NO
Metlay
JP
Lautenbach
E
Inaccurate communications in telephone calls to an antimicrobial stewardship program
Infect Control Hosp Epidemiol
,
2006
, vol.
27
(pg.
688
-
94
)
23.
Larson
EL
Quiros
D
Giblin
T
Lin
S
Relationship of antimicrobial control policies and hospital and infection control characteristics to antimicrobial resistance rates
Am J Crit Care
,
2007
, vol.
16
(pg.
110
-
20
)
24.
Shlaes
DM
Gerding
DN
John
JF
Jr.
, et al.  .
Society for Healthcare Epidemiology of America and Infectious Diseases Society of America Joint Committee on the Prevention of Antimicrobial Resistance: guidelines for the prevention of antimicrobial resistance in hospitals
Infect Control Hosp Epidemiol
,
1997
, vol.
18
(pg.
275
-
91
)
25.
Calbo
E
Garau
J
Application of pharmacokinetics and pharmacodynamics to antimicrobial therapy of community-acquired respiratory tract infections
Respiration
,
2005
, vol.
72
(pg.
561
-
71
)
26.
Dunbar
LM
Wunderink
RG
Habib
MP
, et al.  .
High-dose, short-course levofloxacin for community-acquired pneumonia: a new treatment paradigm
Clin Infect Dis
,
2003
, vol.
37
(pg.
752
-
60
)
27.
Noreddin
AM
Hoban
DJ
Zhanel
GG
Comparison of gatifloxacin and levofloxacin administered at various dosing regimens to hospitalised patients with community-acquired pneumonia: pharmacodynamic target attainment study using North American surveillance data for Streptococcus pneumoniae
Int J Antimicrob Agents
,
2005
, vol.
26
(pg.
120
-
5
)
28.
Ford
W
New strategies in antimicrobial stewardship: managing patient care

29.
ASHP statement on the pharmacist's role in antimicrobial stewardship and infection prevention and control
Am J Health Syst Pharm
,
2010
, vol.
67
(pg.
575
-
7
)
30.
Gross
R
Morgan
AS
Kinky
DE
Weiner
M
Gibson
GA
Fishman
NO
Impact of a hospital-based antimicrobial management program on clinical and economic outcomes
Clin Infect Dis
,
2001
, vol.
33
(pg.
289
-
95
)
31.
Bond
CA
Raehl
CL
Clinical and economic outcomes of pharmacist-managed antimicrobial prophylaxis in surgical patients
Am J Health Syst Pharm
,
2007
, vol.
64
(pg.
1935
-
42
)
32.
Bond
CA
Raehl
CL
Clinical and economic outcomes of pharmacist-managed aminoglycoside or vancomycin therapy
Am J Health Syst Pharm
,
2005
, vol.
62
(pg.
1596
-
605
)

## Author notes

a
Clinical Scientific Director, Medical Affairs, Cubist Pharmaceuticals, Lexington, Massachusetts.