Antimicrobial stewardship programs-A review for the formulary decision-maker


Antimicrobial stewardship programs are being implemented in a variety of settings to assist with the challenges associated with the management of infectious diseases. Here's a review of ASPs from the perspective of a formulary decision-maker.

The spread of antimicrobial resistance, lack of novel antimicrobial agents in development, and challenges to the drug discovery process are of significant global concern today.1-7 The state of this crisis is emphasized by published literature denoting the need for action on multiple levels as we move towards a second pre-antibiotic era or post-antibiotic era.8-12 Antimicrobial Stewardship Programs (ASPs) have become a particular area of focus as healthcare practitioners aim to combat these issues within institutions. In 2007 the Infectious Diseases Society of America (IDSA) and Society for Healthcare Epidemiology of America (SHEA) published guidelines for developing an institutional program to enhance antimicrobial stewardship.13 Since that time, a plethora of original research articles in this area as well as various reviews have been published.14-21 In 2010 a national survey conducted by the American Society of Health-System Pharmacists (ASHP) found that 246 of 566 (43.5%) responding American hospitals had an ASP, reflecting the wide-scale utilization of these programs.22 More recently, interest has developed in the role of ASPs within long-term acute care hospitals (LTACHs) and long-term care facilities (LTCFs).23-26  The value of each element and strategy employed by ASPs continues to be understood within various practice settings. As such, the focus of this article is to review the current state of ASPs from the perspective of a formulary decision-maker and raise awareness regarding the complex related issues.

Description of Antimicrobial Stewardship Programs

The goals of an ASP are to improve patient care and health outcomes.13 This may be accomplished through targeting inappropriate or suboptimal antimicrobial selection, progression of antimicrobial resistance, drug toxicity, or costs. The 2 core strategies of an ASP ([1] prospective audit with feedback and intervention and [2] formulary restriction) may be used in combination with the many potential supplemental elements of an ASP (eg, intravenous to oral conversion) to achieve individual or numerous program objectives (Table 1, page 8). Ideally, ASPs are co-directed by a physician and a pharmacist with specialty training in the area of infectious diseases (ID). These 2 core members work with epidemiologists, infection control specialists, microbiologists, information technology specialists, institutional administrators and other healthcare professionals to compose a multidisciplinary ASP team. Implementation of an Anti-Infective Subcommittee that reports to the Pharmacy and Therapeutics Committee, may be used for managing the interventions and activities of the ASP in this interdisciplinary fashion.

Antimicrobial Stewardship in Practice

For an ASP to maximize its potential benefits, incorporating a pharmacist with advanced training (residency or fellowship), extensive experience, or related certifications in the field of antimicrobial stewardship and ID is invaluable.13,18,27 Unfortunately, realization of such positions is limited by difficulties securing funding and a lack of specialized pharmacists.18,27 This leaves many of the more than 5,700 American hospitals in a unique position.28 In current practice, ASP support from a department of pharmacy is being derived from several avenues, leading to great inconsistencies in how each is organized and managed.16,29 Such diversity is reflective of, among other factors, variations in institution types, sizes, politics, affiliations, patient populations and obtainable financial or personnel resources. From the personnel standpoint, pharmacy students completing an introductory pharmacy practice experience or an advanced pharmacy practice experience, post-graduate year-1 or year-2 pharmacy residents, pharmacy fellows, non-ID pharmacists and pharmacy faculty members have all demonstrated the capacity to actively participate in ASP activities.29-32 As such, institutions are getting creative. For example, a 236-bed community hospital in Bethesda, Md., implemented an ASP without a dedicated on-site ID specialist pharmacist or ID specialist physician and successfully demonstrated significant cost savings and a significant decrease in antimicrobial utilization.33

The uniqueness of each practice location must be considered to achieve the greatest return on investment for delegated ASP resources.  When key players select which intervention(s) to pursue, motivating factors such as patient safety, the spread of antimicrobial resistance, hospital length of stay, spectrum of antimicrobial activity and costs are potential targets.13,34,35 As a healthcare practitioner, patient care universally comes before all else; however, as a formulary decision-maker with administrative responsibilities, financial considerations are of particular interest.36 Fortunately, interventions fueled by economic motivations (eg, decreasing daptomycin expenditures) should inherently contribute to additional ASP targets (eg, inappropriate use) when implemented correctly.29

Drug Expenditures and Economic Impacts

During the first 9 months of 2011 within non-federal American hospitals, $2.15 billion of a total $21 billion in drug expenditures was due to systemic anti-infectives.37 Of the top 15 individual drug expenditures, antimicrobial agents levofloxacin (2007), piperacillin-tazobactam (2007-2011), linezolid (2008-2011), and daptomycin (2009-2011) have all made the list during this same period each year from 2007 through 2011.37-41 In recent years, daptomycin has gained particular notoriety for its financial successes.  From 2010 to 2011, 9-month daptomycin expenditures experienced an increase of 21.9% (a percentage increase second only to the chemotherapeutic agent oxaliplatin) to reach $305 million.37 Moreover, in 2010, it was noted to be the most financially successful intravenous antibiotic in American history (in nominal dollars of sales).42 As administrators look to contain drug expenditures and sustain excellent patient care within their institutions, various ASP strategies have been shown to be effective.13,34,43 Recently, Beardsley et al documented an average annual ASP cost reduction (defined as antimicrobial expenditures minus labor costs) at an 880-bed academic teaching medical center of between $920,070 and $2,064,441 (dependent upon the method of calculation of inflation that was used).44 The noted example from Michaels et al. in Maryland occurred at a much smaller (230-bed) community hospital and produced a two-year drug cost reduction of up to $290,000.33 Such examples reflect the capacity for an ASP to generate cost savings in a variety of settings.

Formulary Restriction and Preauthorization

The core ASP strategy of formulary restriction and preauthorization has shown to contribute to immediate and significant reductions in drug cost and use, earning it an A-II recommendation in the 2007 Stewardship Guideline.13 This strategy may be implemented in a number of ways, including controlling antimicrobial agents in a prospective or retrospective authorization process enforced either intermittently or 24-hours per day, 7-days per week. The target for this strategy may be an individual drug (eg, linezolid) or a selected formulary agent within a drug class (eg, doripenem as the antipseudomonal carbapenem of choice).21,43 Target selection is dependent upon the numerous previously noted institution-specific characteristics.

Recently, Goff et al. investigated potential ASP “low-hanging fruit,” or selecting the most feasible targets given sparse resources.21 The authors found formulary restriction to contribute to early program successes and significant cost savings, but noted the requirement of more resources than other strategies (eg, therapeutic substitution).  This led the researchers to reject formulary restriction as a low-hanging fruit. Prior to their investigation, survey data from members from the IDSA Emerging Infections Network documented a shift over a10-year period (1999 to 2009) away from formulary restriction alone to a tailored set of strategies.36 Such findings seem fitting, particularly in light of the lack of resources (including sufficiently trained personnel) institutions are faced with today.18,27

In the setting of an LTACH or LTCF, recognizing the difficulties of maintaining formulary standards when receiving patients from outside facilities with various formulary practices is a challenge for preserving continuity of care.15 To this end, ASPs in these settings may or may not choose to incorporate the strategy of formulary restriction.24,25

Looking forward, formulary restriction will undoubtedly remain an integral part of ASPs, but may be more effective when used in combination with other elements or in a bundled approach to influencing practice.34,45 As such, 2 possible occurrences to be aware of when incorporating formulary restriction into an ASP are stealth prescribing and squeezing of the balloon. Stealth prescribing refers to situations in which prescribers work around the hours of the restriction program, writing for restricted drugs when their orders will not be subject to the traditional approval process.46 Squeezing of the balloon refers to restriction of 1 antimicrobial drug or class, which in turn increases the use of another antimicrobial drug or class.47 A classic case of this was documented by Rahal et al., who found that total cephalosporin restriction led to greater imipenem-cilastatin use and increased imipenem-cilastatin resistance in Pseudomonas aeruginosa.48

Supplemental Strategies for Antimicrobial Stewardship

There are numerous supplemental strategies an ASP may employ (Table 1, page 8), of which many have demonstrated an impact on financial endpoints.13,44 A complete review of these is beyond the scope of this article, but several will be noted here.

Intravenous (IV) to oral (PO) conversion of antimicrobial agents is a commonly practiced intervention that has consistently shown to be safe and effective. Additionally, it can be performed by personnel who do not require extensive training.13,21 In 2001, Wong-Beringer et al provided a description of how an IV to PO program can be implemented, which new ASPs may find useful.49 They suggest selecting drugs that are commonly used and for which there are substantial cost differences between the IV and PO formulations, reflecting the importance of considering the uniqueness of each institution when making decisions. With regard to financial outcomes, there have been extensive publications in this area. Recently, in 2012, Jones et al reported a potential cost savings from 2006 through 2010 of up to $4,000,000 through elimination of avoidable IV fluoroquinolone use in 128 Veterans Affairs Hospitals.50 Although such promise is noteworthy and drug costs are not the only benefit to IV to PO transition, it is also important to recognize long-term drug cost benefits may be hampered by changes in factors such as acquisition costs (eg, levofloxacin transitioning to generic).

Dose optimization of antimicrobials refers to ensuring drug treatment is tailored to the individual patient, causative organism, infection site, and/or drug-specific characteristics (pharmacokinetic/pharmacodynamic [PK/PD] properties).13 Numerous interventions fall under this element, including use of PK/PD services (eg, for IV vancomycin) and extended- or continuous-infusions for drugs with time-dependant killing (eg, select beta-lactams).15 Implementation of a piperacillin-tazobactam extended-infusion protocol has become a specific area of interest in recent years, as more publications supporting its favorable safety and financial impact have come to light.51-55 Utilizing a more prolonged infusion time allows for maximization of antimicrobial killing and a reduction in total daily doses (eg, 3.375 g every 6 hours infused over 30 minutes versus 3.375 g every 8 hours infused over 4 hours), thus preserving patient care and lowering drug costs. Three separate studies of piperacillin-tazobactam extended-infusion protocol implementation have documented financial outcomes to include annual expenditure reductions of up to 18%, $108,529, and $135,750.53-55 Implementing this intervention has the potential to have a similar benefit at other institutions, particularly when considering that piperacillin-tazobactam has consistently been of significant cost to non-federal American hospitals for several years.37-41

As previous points are considered, implementation of interventions targeting utilization of specific high-cost agents is likely to appear a rational starting point, particularly when there are multiple such drugs available and the goal is to establish sustainable ASP activities. While this is undoubtedly true in the short-term, McGowan notes that long-term cost savings are not supported by as robust data and that future evaluation methods are an area of concern if convincing evidence for the continuation of ASPs is to be produced.56 As implementation and continuation of sustainable ASPs remains a challenge, nonpharmacy costs, such as those associated with increased length of hospitalization, hospital readmission, drug toxicities, and acquiring an infection with an antimicrobial resistant organism should also be kept in mind.6,21,57,58

Patient Safety and the Progression of Antimicrobial Resistance

The primary goal of an ASP is the optimization of clinical outcomes.13 To achieve this, use of interdisciplinary strategies and active accounting for institution-specific outcome measures (eg, antimicrobial resistance, length of stay, 30-day readmissions, etc.) are crucial. As patient safety and antimicrobial resistance are addressed, common ground can be observed. For example, when a patient acquires an infection due to an antimicrobial-resistant organism, use of a drug with significant toxicities (eg, colistin) may become necessary.59 The effect of resistant organisms on mortality was investigated by Neidell et al, who recently found higher death rates in patients infected with antimicrobial-resistant organisms versus antimicrobial-susceptible organisms.58 Although this is not entirely surprising, it is tremendously concerning in light of current issues relating to antimicrobial development and resistance worldwide.1-12

When considering these issues, collateral damage is a term worth noting. This refers to the unfavorable ecological effects of using antimicrobial therapy.60 Two possible forms of collateral damage are selection for organisms harboring antimicrobial resistance and colonization with an antimicrobial-resistant organism. Cephalosporins (the second and third generations in particular) and fluoroquinolones are two areas of concern regarding these negative implications.60-62 Focusing on Clostridium difficile infection, Dubberke recently published an article reviewing the scope of this significant and wide-spread health problem.63 Here, the author reviews the impact on morbidity, mortality, and costs and denotes an increase in the incidence, severity, virulence, and treatment failures. As healthcare practitioners attempt to address this issue, agents associated with collateral damage may be found to be antagonistic to their efforts. One example of the impact fluoroquinolone and cephalosporin use can have may be derived from an incident that occurred in a hospital in The Netherlands.61 At this institution, an outbreak of C difficile did not end until use of cephalosporins was restricted and fluoroquinolones were completely banned. More recent literature has supported this finding, noting the restriction of these antibiotics (referred to as “high-risk antibiotics”) to contribute to a reduction in their use and the incidence of C difficile infection.62  Although agents within these 2 drug classes (eg, ceftriaxone and ciprofloxacin) are not typically of particularly high cost from the drug acquisitions perspective, it is clear that they do have considerable cost implications to the healthcare system.64

The occurrence and evolution of infections due to antimicrobial-resistant organisms will inevitably continue to impact patient safety. Therapeutic options in the antimicrobial arsenal become more limited when organisms acquire resistance mechanisms, often resulting in choices which carry a different set of toxicities. This is of particular concern for a set of organisms termed the “ESCAPE” pathogens (previously the “ESKAPE” pathogens), which have the ability to “escape” actions of available antibiotics.2,3 This acronym stands for Enterococcus faecium, Staphylococcus aureus, C difficile, Acinetobacter baumannii, P aeruginosa, and Enterobacteriaceae.3 Agents used to treat infections caused by these pathogens (select adverse drug reaction(s) [ADRs] noted in parentheses), such as tigecycline (nausea and vomiting), daptomycin (creatinine phosphokinase [CPK] elevation), linezolid (neuropathies and bone marrow suppression), dalfopristin-quinupristin (infusion reactions and arthralgias) and colistin (nephrotoxicity and neurotoxicity) require specific consideration in regards to their tolerability.64 Fortunately, several ASP activities exist which can help to control and prevent ADRs. One example comes from Tran et al., who investigated the impact of an institutional protocol to improve daptomycin dosing for infections caused by vancomycin-resistant enterococci (VRE). Their results demonstrated that a multidisciplinary ASP team improved the rate of safety monitoring, as CPK assessment at baseline rose from 43% to 64% (P<.05).65 With multidrug-resistant organisms on the rise, an increase in the utilization of aforementioned medications is inevitable, thus incorporation of monitoring parameters for ADRs into ASP activities should be considered.

Antimicrobial Stewardship Resources

Numerous resources are available to healthcare practitioners looking to acquire more information about antimicrobial stewardship. The websites of organizations such as the World Health Organization, Centers for Disease Control and Prevention (CDC), and local departments of health have an enormous amount of information. The CDC in particular hosts a “Get Smart for Healthcare” campaign available at: (accessed November 19, 2012), whose goal is to optimize antimicrobial use in the inpatient healthcare settings. Guidelines and resources published by the IDSA, SHEA and other major organizations are extensive and many are available for free online. Further, the ASHP initiative Lead Stewardship website available at: (accessed November 19, 2012) hosts an array of resources. 

Available from the literature, a publication by Pagani et al in 2009 provides a review of online resources.66 Here, researchers describe results of a search for antimicrobial stewardship resources for healthcare institutions, with a goal of identifying high-quality and readily accessible resources, such as comprehensive websites, institutional websites, and websites from societies or other organizations. Their findings present a wide array of available resources, which may be useful for anyone involved in ASP activities. More recently, Goff provided a review of medical applications (commonly referred to as “apps”) ASPs may use on the iPhone or iPad.67 Descriptions of 17 apps are provided, which fall under a medical category of drug information, education, calculators, references, epidemiology, or news.

For practitioners looking to acquire training and exposure within the area of ID or antimicrobial stewardship, beyond completing post-graduate pharmacy residency or fellowship training, a few avenues exist. The Society of Infectious Diseases Pharmacists has an Antibiotic Stewardship Certificate Training Program, with details available at: (accessed November 19, 2012). The group Making a Difference in ID Pharmacotherapy (MAD ID) also has a training program, with details available at: (accessed November 19, 2012). For practitioners looking to become distinguished among their peers, the Board of Pharmacy Specialties (BPS) offers Added Qualifications in the area of ID for Board Certified Pharmacotherapy Specialists with criteria available at: (accessed November 19, 2012). Further, the creation of an independent BPS ID specialty is in the works.68

Future Directions and Conclusion

Undoubtedly, antimicrobial stewardship will remain a subject of interest for healthcare practitioners across a variety of settings for years to come. Appelbaum provides a thorough summary of what can be done to address the many concerns at hand, during which he notes the importance of education, public awareness, regulatory collaboration, and funding.1 Goff et al noted future Medicare payment penalties relating to readmissions and the Affordable Care Act, which is likely to become of great interest.21,69 Such discussion supports the notion that improving outcomes, ASP longevity, institution-specific considerations, and other factors will remain a noteworthy challenge as we continue to attempt to hit the moving target of implementing effective antimicrobial stewardship strategies. Importantly, formulary decision-makers should continue to stay abreast of changes as further information comes to light and as we better understand how the decisions of today impact the issues of tomorrow. ■


1. Appelbaum P. 2012 and beyond: potential for the start of a second pre-antibiotic era? J Antimicrob Chemother. 2012;67:2062-2068.

2. Boucher HW, Talbot GH, Bradley JS, et al. Bad bugs, no drugs: no ESKAPE! an update from the infectious diseases society of America. Clin Infect Dis. 2009;48:1-12.

3. Peterson LR. Bad bugs, no drugs: no ESCAPE revisited. Clin Infect Dis. 2009;49:992.

4. Wise R. The urgent need for new antibacterial agents. J Antimicrob Chemother. 2011;66:1939-1940.

5. Piddock LJ. The crisis of no new antibiotics-what is the way forward? Lancet Infect Dis. 2012;12:249-253.

6. White AR. Effective antibacterials: at what cost? the economics of antibacterial resistance and its control. J Antimicrob Chemother. 2011;66:1948–1953.

7. Spellberg B, Brass EP, Bradley JS, et al. White paper: recommendations on the conduct of superiority and organism-specific clinical trials of antibacterial agents for the treatment of infections caused by drug-resistant bacterial pathogens. Clin Infect Dis. 2012;55(8):1031–1046.

8. Alanis AJ. Resistance to antibiotics: are we in the post-antibiotic era? Arch Med Res. 2005;36:697–705.

9. Bush K, Courvalin P, Dantas G, et al. Tackling antibiotic resistance. Nat Rev Microbiol. 2011;9:894–896.

10. Bartlett JG. A call to arms: the imperative for antimicrobial stewardship. Clin Infect Dis. 2011;53(S1):S4–S7.

11. Spelberg B, Guidos R, Bradley J, et al. The epidemic of antibiotic-resistant infections: a call to action for the medical community from the infectious diseases society of America. Clin Infect Dis. 2008;46:155–164.

12. Savard P, Perl TM. A call for action: managing the emergence of multidrug-resistant Enterobacteriaceae in the acute care setting. Curr Opin Infect Dis. 2012;25:371–377.

13. Dellit TH, Owens RC, McGowan JE, 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;44:159–177.

14. Louie T. Antimicrobial stewardship: a review. Infect Dis Clin Pract. 2011;19(6):382–387.

15. Doron S, Davidson L. Antimicrobial stewardship. Mayo Clin Proc. 2011;86(11):1113–1123.

16. Ohl CA, Luther VP. Antimicrobial stewardship for inpatient facilities. J Hosp Med. 2011;6(S1):S4–S15.

17. Lesprit P, Brun-Buisson C. Hospital antibiotic stewardship. Curr Opin Infect Dis. 2008;21:344–349.

18. Drew RH, White R, MacDougall C, Hermsen ED, Owens RC. Insights from the society of infectious diseases pharmacists on antimicrobial stewardship guidelines from the infectious diseases society of America and the society for healthcare epidemiology of America. Pharmacother. 2009;29(5):593–607.

19. Drew RH. Antimicrobial stewardship programs: how to start and steer a successful program. J Manag Care Pharm. 2009;15(S2):S18–S23.

20. Patel D, MacDougall C. How to make antimicrobial stewardship work: practical considerations for hospitals of all sizes. Hosp Pharm. 2010;45(S1):S10–18.

21. Goff DA, Bauer KA, Reed EE, Stevenson KB, Taylor JJ, West JE. Is the “low-hanging fruit” worth picking for antimicrobial stewardship programs? Clin Infect Dis. 2012;55(4):587–592.

22. Pedersen CA, Schneider PJ, Scheckelhoff DJ. ASHP national survey of pharmacy practice in hospital settings: prescribing and transcribing-2010. Am J Health-Syst Pharm. 2011;68:669–688.

23. Daneman N, Gruneir A, Newman A, et al. Antibiotic use in long-term care facilities. J Antimicrob Chemother. 2011;66:2856–2863.

24. Pate PG, Storey DF, Baum DL. Implementation of an antimicrobial stewardship program at a 60-bed long-term acute care hospital. Infect Control Hosp Epidemiol. 2012;33(44):405–408.

25. Van Schooneveld T, Miller H, Sayles H, Watkins K, Smith PW. Survey of antimicrobial stewardship practices in Nebraska long-term care facilities. Infect Control Hosp Epidemiol. 2011;32(7):732–734.

26. Smith PW, Bennett G, Bradley S, et al. SHEA/APIC guideline: infection prevention and control in the long-term care facility. Am J Infect Control. 2008;36:504–535.

27. Owens RC, Shorr AF, Deschambeault AL. Antimicrobial stewardship: shepherding precious resources. Am J Health-Syst Pharm. 2009;66(S4):S15–S22.

28. American Hospital Association website. Available from Updated January 3, 2012. Accessed November 19, 2012.

29. Ohl CA, Dodds Ashley ES. Antimicrobial stewardship programs in community hospitals: the evidence base and case studies. Clin Infect Dis. 2011;53(S1):S23–S28.

30. Bird ML, Dunn RL, Hagemann TM, Burton M, Britton ML, St. Cyr MB. Collaboration between a college of pharmacy and a for-profit health system at an academic medical center. Am J Health-Syst Pharm. 2012;69:1150–1156.

31. Palmer HR, Weston J, Gentry L, et al. Improving patient care through implementation of an antimicrobial stewardship program. Am J Health-Syst Pharm. 2011;68:2170-2174.

32. Camins BC, King MD, Wells JB, et al. Impact of an antimicrobial utilization program on antimicrobial use at a large teaching hospital: a randomized control trial. Infect Control Hosp Epidemiol. 2009;30:931–938.

33. Michaels K, Mahdavi M, Krug A, Kuper K, et al. Implementation of an antimicrobial stewardship program in a community hospital: results of a three-year analysis. Hosp Pharm. 2012;47(8):608–616.

34. Nowak MA, Nelson RE, Breidenbach JL, Thompson PA, Carson PJ. Clinical and economic outcomes of a prospective antimicrobial stewardship program. Am J Health-Syst Pharm. 2012;69:1500–1508.

35. MacDougall C, Polk RE. Antimicrobial stewardship programs in health care systems. Clin Microbiol Rev. 2005;18(4):638–656.

36. Johannsson B, Beekmann SE, Srinivasan A, Hersh AL, Laxminarayan R, Polgreen PM. Improving antimicrobial stewardship: the evolution of programmatic strategies and barriers. Infect Control Hosp Epidemiol. 2011;32(4):367–374.

37. Hoffman JM, Li E, Doloresco F, et al. Projecting future drug expenditures-2012. Am J Health-Syst Pharm. 2012;69:e5-e21.

38. Doloresco F, Fominaya C, Schumock GT, et al. Projecting future drug expenditures-2011. Am J Health-Syst Pharm. 2011;68:e1-e12.

39. Hoffman JM, Doloresco F, Vermeulen LC, et al. Projecting future drug expenditures-2010. Am J Health-Syst Pharm. 2010;67:919–928.

40. Hoffman JM, Shah ND, Vermeulen LC, et al. Projecting future drug expenditures-2009. Am J Health-Syst Pharm. 2009;66:237–257.

41. Hoffman JM, Shah ND, Vermeulen LC, et al. Projecting future drug expenditures-2008. Am J Health-Syst Pharm. 2008;65:234–253.

42. Eisenstein BI, Oleson FB, Baltz RH. Daptomycin: from the mountain to the clinic, with essential help from Francis Tally, MD. Clin Infect Dis. 2010;50(S1):S10–S15.

43. Po JL, Nguyen BQ, Carling PC. The impact of an infectious diseases specialist-directed computerized physician order entry antimicrobial stewardship program targeting linezolid use. Infect Control Hosp Epidemiol. 2012;33:434–435.

44. Beardsley JR, Williamson JC, Johnson JW, Luther VP, Wrenn RH, Ohl CC. Show me the money: long-term financial impact of an antimicrobial stewardship program. Infect Control Hosp Epidemiol. 2012;33(4):398–400.

45. Toth NR, Chambers RM, Davis SL. Implementation of a care bundle for antimicrobial stewardship. Am J Health-Syst Pharm. 2010;67:746–749.

46. LaRosa LA, Fishman NO, Lautenbach E, Koppel R, Morales KH, Linkin DR. Evaluation of antimicrobial therapy orders circumventing an antimicrobial stewardship program: investigating the strategy of “stealth dosing”. Infect Control Hosp Epidemiol. 2007;28:551–556.

47. Peterson LR. Squeezing the antibiotic balloon: the impact of antimicrobial classes on emerging resistance. Clin Microbiol Infect. 2005;11(S5):S4–S16.

48. Rahal JJ, Urban C, Horn D, et al. Class restriction of cephalosporin use to control total cephalosporin resistance in nosocomial Klebsiella. JAMA. 1998;280:1233–1237.

49. Wong-Beringer A, Nguyen K, Razeghi J. Implementing a program for switching from i.v. to oral antimicrobial therapy. Am J Health-Syst Pharm. 2001;58:1146–1149.

50. Jones M, Huttner B, Madaras-Kelly K, et al. Parenteral to oral conversion of fluoroquinolones: low-hanging fruit for antimicrobial stewardship programs? Infect Control Hosp Epidemiol. 2012;33(4):362–367.

51. Kaufman SE, Donnell RW, Hickey SW. Rationale and evidence for extended infusion of piperacillin-tazobactam. Am J Health-Syst Pharm. 2011;68:1521–1526.

52. Yost RJ, Cappalletty DM, et al. The retrospective cohort of extended-infusion piperacillin-tazobactam (RECIEPT) study: a multicenter study. Pharmacother. 2011;31(8):767–775.

53. Xamplas RC, Itokazu GS, Glowacki RC, Grasso AE, Caquelin C, Schwartz DN. Implementation of an extended-infusion piperacillin-tazobactam program at an urban teaching hospital. Am J Health-Syst Pharm. 2010;67:622–628.

54. Heinrich LS, Tokumaru S, Clark NM, Garofalo J, Paek JL, Grim SA. Development and implementation of a piperacillin-tazobactam extended infusion guideline. J Pharm Pract. 2011;24:571–576.

55. Lodise TP, Lomaestro B, Drusano GL. Piperacillin-tazobactam for Pseudomonas aeruginosa infection: clinical implications of an extended-infusion dosing strategy. Clin Infect Dis. 2007;44:357–363.

56. McGowan JE. Antimicrobial stewardship-the state of the art in 2011: focus on outcome and methods. Infect Control Hosp Epidemiol. 2012;33(4):331–337.

57. Dryden M, Saeed K, Townsend R, et al. Antibiotic stewardship and early discharge from hospital: impact of a structured approach to antimicrobial management. J Antimicrob Chemo. 2012;67:2289–2296.

58. Neidell MJ, Cohen B, Furuya Y, et al. Costs of health-care and community-associated infections with antimicrobial resistant versus antimicrobial-susceptible organisms. Clin Infect Dis. 2012;55(6):807–815.

59. Lim LM, Ly B, Anderson D, et al. Resurgence of colistin use: a review of resistance, toxicity, pharmacodynamics, and dosing. Pharmacother. 2010;30(12):1279–1291.

60. Paterson DL. “Collateral damage” from cephalosporin or quinolone antibiotic therapy. Clin Infect Dis. 2004;38(S4):S341–S345.

61. Debast SB, Vassen N, Choudry A, Wiegers-Ligvoet EAJ, Van Den Berg RJ, Kuijper EJ. Successful combat of an outbreak due to Clostridium difficile PCR ribotype 027 and recognition of specific risk factors. Clin Microbiol Infect. 2009;15:427–434.

62. Aldeyab MA, Kearney MP, Scott MG, et al. An evaluation of the impact of antibiotic stewardship on reducing the use of high-risk antibiotics and its effect on the incidence of Clostridium difficile infection in the hospital setting. J Antimicrob Chemother. 2012 Aug 16:[Epub ahead of print].

63. Dubberke E. Clostridium difficile infection: the scope of the problem. J Hosp Med. 2012;7(S3):S1–S4.

64. Lexi-Comp, Inc. (Lexi-DrugsTM). Hudson, OH: Lexi-Comp, Inc.; v1.10.0(159), October 12, 2012.

65. Tran TT, Palmer HR, Weston J, et al. Evaluation of a daptomycin dose-optimization protocol. Am J Health-Syst Pharm. 2012;69:979–984.

66. Pagani L, Gyssens IC, Huttner B, Nathwani D, Harbarth S. Navigating the web in search of resources on antimicrobial stewardship in health care institutions. Clin Infect Dis. 2009;48:626–632.

67. Goff DA. iPhones, iPads, and medical applications for antimicrobial stewardship. Pharmacother. 2012;32(7):657–661.

68. American College of Clinical Pharmacy Website. Available from Accessed November 19, 2012.

69. website. Available from Accessed November 19, 2012.

Related Videos
Related Content
© 2024 MJH Life Sciences

All rights reserved.