• Users Online: 95
  • Home
  • Print this page
  • Email this page
Home About us Editorial board Search Ahead of print Current issue Archives Submit article Instructions Subscribe Contacts Login 


 
 Table of Contents  
REVIEW ARTICLE
Year : 2014  |  Volume : 1  |  Issue : 1  |  Page : 4-10

Antimicrobial stewardship: Strategies for a global response


1 Department of Internal Medicine, Division of Infectious Diseases, Henry Ford Hospital, Detroit, USA
2 Department of Public Health Sciences; The Global Health Initiative, Division of Infectious Diseases, Henry Ford Health System, Detroit, Michigan, USA

Date of Web Publication11-Feb-2014

Correspondence Address:
Indira Brar
Department of Internal Medicine, Division of Infectious Diseases, Henry Ford Health System, 2799 West Grand BLVD, CFP 305, Detroit, Michigan 48202
USA
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/2348-3334.126771

Rights and Permissions
  Abstract 

The increasing antimicrobial resistance worldwide, combined with dwindling antimicrobial armamentarium, has resulted in a critical threat to the public health and safety of patients. To combat this hazard, antimicrobial stewardship programs (ASPs) have emerged. Antimicrobial stewardship programs prevent or slow the emergence of antimicrobial resistance by coordinated interventions designed to optimize antimicrobial use to achieve the best clinical outcomes and limiting selective pressures that drive the emergence of resistance. This also reduces excessive costs attributable to suboptimal antimicrobial use. Even though an ideal effective ASP should incorporate more than one element simultaneously, it also requires a multidisciplinary team, which should include an infectious diseases physician, a clinical pharmacist with infectious diseases training, infection control professionals, hospital epidemiologist, a clinical microbiologist and an information specialist. However, for antimicrobial stewardship (AMS) programs to be successful, they must address the specific needs of individual institutions, must be built on available resources, the limitations and advantages of each institution, and the available staffing and technological infrastructure.

Keywords: Antimicrobial resistance, antimicrobial stewardship, antimicrobial utilization, global health, multidrug resistant infection prevention


How to cite this article:
Grunwald J, Zervos J, Zervos M, Brar I. Antimicrobial stewardship: Strategies for a global response. CHRISMED J Health Res 2014;1:4-10

How to cite this URL:
Grunwald J, Zervos J, Zervos M, Brar I. Antimicrobial stewardship: Strategies for a global response. CHRISMED J Health Res [serial online] 2014 [cited 2023 Mar 31];1:4-10. Available from: https://www.cjhr.org/text.asp?2014/1/1/4/126771


  Introduction Top


Antimicrobial resistance is increasing worldwide and there are fewer antimicrobials being developed to treat these resistant organisms. [1],[2],[3],[4],[5],[6],[7] Given the paucity of novel antibiotics being developed, the need to preserve the effectiveness of our current antimicrobial armamentarium has never been greater. There is an urgent requirement to reduce selection pressure on today's agents by more prudent choice of antibiotic, by reducing transmission of multidrug resistant organisms through effective infection control systems to prevent cross transmission of organisms, and by optimizing drug exposure through better adherence to proven treatment regimens. The Centers for Disease Control and Prevention (CDC) estimates that in the United States over 2 million people acquire antibiotic resistant infections each year with an estimated cost of 20 billion dollars (threat report). [8] This is a global problem, with many examples of the rapid spread of new resistances between continents. [1],[9],[10] Unfortunately, we lack the surveillance systems, the policy methods and resources to tackle it. The paucity of basic information about prescribed antibiotic use is compounded by the fact that antibiotics are used across the world in animal feed and without a prescription. Practical strategies of control are particularly needed in low- and middle income countries. Because of increasing resistance rates, morbidity/mortality, and escalating costs, antimicrobial stewardship (AMS) programs are increasingly recognized as an essential practice element for health care institutions. [11],[12],[13],[14],[15],[16],[17],[18],[19],[20],[21],[22],[23],[24],[25],[26] Antimicrobial Stewardship Programs (ASP) have been shown to decrease costs, decrease infection rates with multidrug resistant organisms and C. difficile, decrease length of stay, and improve patient outcomes. Also, effective AMS programs can be financially self- supporting. [27],[28]

Need for antimicrobial stewardship?

In 2013, CDC issued the threat report with a goal to increase public awareness of the danger that multidrug resistant organisms present us and urged that action be taken to address the growing threat of these organisms. The threat report estimates that in the United States more than two million people will acquire an antibiotic resistant infection yearly and 23,000 will die as a result. This costs an estimated 20 billion dollar to the US economy. 250,000 people require hospitalization for C. difficile each year and mortality rose 400% between 2000 and 2007. Rates of multidrug resistant organisms are rising. A 2012 review article by Savard and Perl [29] described the emergence of multidrug resistant (MDR) Enterobacteriaceae as a global health concern. MDR Enterobacteriaceae rates have increased annually in the United States. The emergence of New Delhi Metallo-β-lactamase in multiple countries is well documented. [10] Unfortunately, New Delhi Metallo-β-lactamase organisms have been found in tap water and sewage in India, thus making intestinal colonization possible outside of a hospital setting. While the rates of MDR organisms are rising, the rate of new antibiotics being developed to target these organisms is painfully slow. The Infectious Diseases Society of America (IDSA) has identified Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacter species (ESKAPE) pathogens as a target of new antibiotic initiatives. Because the number of new antibiotics developed continues to decline against these gram negative organisms, the IDSA has launched the 10 × 20 initiative. The IDSA stresses that the antibiotic pipeline crisis can be solved by the collaboration of global leaders to develop creative incentives that will stimulate new antibacterial research and development. The aim is to develop a sustainable global antibacterial drug research and development enterprise in order to develop ten new, safe and efficacious antibiotics by 2020. An update issued by the IDSA in 2013 demonstrated that while some progress is being made in the development of antibiotics targeting gram negative bacteria, overall progress is slow. [7] This reinforces the need to protect current available antibiotics with stewardship and infection prevention measures.

Benefits of antimicrobial stewardship programs

The IDSA defines AMS as coordinated interventions designed to improve and measure the appropriate use of antimicrobials by promoting the selection of optimal antimicrobial drug regimen, dose, duration of therapy, and route of administration. [13] The goal of the intervention is to improve patient outcomes in addition to minimizing antimicrobial resistance, and the collateral injury from the overuse of antibiotics such as C. difficile. IDSA began publishing guidelines for antimicrobial usage in 1988.

Standiford et al., described a successful AMS program that consisted of having an infectious disease (ID) pharmacist and ID physician at a large academic medical center. The goal was to identify ineffective or excessive antibiotic coverage, discontinue unnecessary double coverage, and conversion from IV therapy to oral antibiotics wherever possible. There was a cost reduction of three million dollars within the first three years. However when the program was discontinued, there was a 32% increase in costs within two years. [15] Even in rural hospitals without an infectious diseases specialist, stewardship programs can be successful. Yam et al. described the implementation of AMS program at a rural hospital where an ID physician and an ID pharmacist were not available. A multidisciplinary team was established that identified six antimicrobials with a high potential for misuse. A key part of the program was the participation of a remotely located ID physician specialist in a weekly case review teleconference. A weekly case review teleconference was held with an infectious disease physician. This relatively simple intervention was shown to decrease antibiotic costs, decrease C. difficile infection rates, improvements in infection control. [30] Even a thrice weekly review performed by a pharmacist was found to have 37% reduction in total antimicrobial expenditures. [31]

The IDSA issued guidelines for developing ASM programs in 2012. Among the recommendations was a to build multidisciplinary team consisting of an ID physician and ID trained pharmacist along with using measures such as formulary restriction and preauthorization, de-escalating therapy, dose optimization, parenteral to oral conversion and education. [13] Studies have shown that the absence of a pharmacist from an ASM program resulted in increased use of restricted antibiotics, increased duration of antibiotics, and increased C. difficile infections during the period of absence by the pharmacist. [24],[32]

It has been suggested that when starting an AMS program, try to start with simple obtainable targets such as formulary restriction, parental to oral conversion, selective reporting by the microbiology laboratory and therapeutic substitutions. These measures require few resources and have shown to result in significant cost savings. [33] Goff et al.,[33] showed that in their ASM program, selecting simple attainable targets that included intravenous-to-oral conversions, batching of intravenous antimicrobials, therapeutic substitutions, and formulary restrictions, provided early successes, with a substantial cumulative annual cost savings of $832,590. Other strategies have been, restriction of newer agents or review of antimicrobial management of disease states in which there is potential for overuse, such as management of asymptomatic bacteria because it is often over treated. [34]

Newer techniques for enhancing AMS programs have included the use of molecular methods for rapid and reliable identification of various organisms directly from blood culture bottles within minutes. [35] Perez et al. showed that this technology improved time to optimal therapy. In the study during the intervening period, the average turnaround time for final culture identification and antimicrobial susceptibility results was a full day quicker compared with the pre-intervention study group (24.4 vs. 47.1 hours, respectively; P < 0.001). This resulted in earlier initiation of active, targeted antimicrobial therapy which resulted in improved patient outcomes (decreased length of stay and decreased mortality) and reduced healthcare expenditures. [36]

Strategies for AMS

The strategies are broadly divided into two categories:

(1) Prior authorization strategies: These are based on restricting access to some formulary of antibiotics in an institution. The use of the antibiotics requires prior authorization from an individual or a committee. [13],[37],[38],[39],[40] This strategy can lead to immediate and significant reductions in antimicrobial use and cost and may be beneficial as part of a multifaceted response to a nosocomial outbreak of infection. However, the use of preauthorization requirements as a means of controlling antimicrobial resistance is less clear, and in some circumstances, use may simply shift to an alternative agent with resulting increased resistance. The negative impact of this strategy is the suggestion that physicians, to circumvent the process of seeking prior approval, were using alternative antibiotics that were frequently inappropriate choices. [41] The individual preauthorization of a specific agent to be used in an individual patient is generally done by the Infectious Disease Consultative Service of the institution. The agents restricted are those with potential for overuse or high cost.

(2) Prospective audit and feedback strategies: In this strategy, either an ID physician or pharmacist audits antimicrobial use and performs changes and interventions as needed. This strategy is limited by the logistic challenge of identifying patients receiving inappropriate antibiotics, availability of knowledgeable staff to perform reviews and the physician's willingness to accept recommendations.

In addition to these two core antimicrobial stewardship strategies, the supplementary activities of a successful AMS program include:

  • Education: This is designed to influence prescribing behavior and can provide a foundation of knowledge that will enhance and increase the acceptance of stewardship strategies.
  • Guidelines and clinical pathways: The development of evidence based practice guidelines incorporating local microbiology and resistance patterns can improve antimicrobial utilization. [32],[42],[43],[44],[45],[46]
  • Antimicrobial substitution or cycling: [47],[48],[49],[50],[51] It is a strategy suggested to curb the development of resistant hospital acquired infections. In this strategy, antibiotic classes are switched or alternated over time. This can be compared with a mixing program in which, when given two drugs, half of the physicians prescribe one drug over the other. Chow et al. use a mathematical model of antimicrobial cycling in a hospital population setting to evaluate the efficacy of a cycling program with an emphasis on reducing the emergence and significance of dual resistance. The model also considered the effects of physician compliance and isolating patients harboring dual resistant bacteria. Simulation results showed that the optimal antimicrobial drug usage program in hospital populations depends upon the type of resistance being targeted for treatment; a cycling program is more effective against dual resistance compared with mixing. Patient isolation and high compliance to a cycling program is also shown to dramatically decrease dual resistance in hospitalized populations. The substitution of agents has been shown to reduce resistance to a particular class of drug. However, there is not sufficient data to recommend the routine use of antimicrobial cycling as a means of preventing or reducing antimicrobial resistance over a prolonged period of time.
  • Antimicrobial order forms and electronic monitoring: Antimicrobial order forms can be an effective component of AMS and can facilitate implementation of practice guidelines. With newer electronic medical records, incorporation of alerts for use of drugs is increasingly used as reminders for appropriate use or to trigger monitoring. [44],[52],[53],[54],[55]
  • Combination therapy: There is insufficient data to recommend the routine use of combination therapy to prevent the emergence of resistance. Combination therapy does have a role in certain clinical contexts, including use for empirical therapy for critically ill patients at risk of infection with multidrug-resistant pathogens.
  • Streamlining or de-escalation of therapy: Streamlining or de-escalation of empirical antimicrobial therapy on the basis of culture results and elimination of redundant combination therapy can more effectively target the causative pathogen, resulting in decreased antimicrobial exposure and substantial cost savings. [56],[57],[58],[59],[60],[61]
  • Dose optimization: It is an important part of stewardship to optimize the dosing of antimicrobials.
  • Parenteral to oral conversion: Development of clinical criteria and guidelines to switch to oral agents of antimicrobials with excellent bioavailability, when the patient's condition allows. If the agent is bioavailable and the patient has a functioning gastrointestinal tract, the agent can be safely substituted.
  • Automatic stop orders issued to stop antimicrobial agents used empirically or perioperatively. A "time out" for reconsideration of agents has also been suggested and
  • Allergy de-labeling [62] is an integration of antibiotic allergy de-labeling, as imprecise antibiotic allergy labeling is associated with increased antibiotic costs, antimicrobial use, risk of acute care admission, and mortality.


An ideal effective AMS program should incorporate more than one element simultaneously into the program. It also requires a multidisciplinary team, which should include an ID physician, a clinical pharmacist with ID training, infection control professionals, hospital epidemiologist, a clinical microbiologist and an information specialist. The latter plays an important role in linking the patient's medical record to the pharmacy and microbiology databases, to identify interventions and to perform surveillance activities. However, for AMS programs to be successful, they must address the specific needs of individual institutions and be built on available resources, the limitations and advantages of each institution, and the available staffing and technological infrastructure.

Global impact: The future

Antimicrobial resistance is a global threat. Its emergence rests on antimicrobial overuse in humans and food-producing animals; globalization and suboptimal infection control facilitate its spread. While aggressive measures in some countries have led to the containment of some resistant gram-positive organisms, extensively resistant gram-negative organisms such as carbapenem-resistant enterobacteriaceae, Mycobacterium tuberculosis and pan-resistant Acinetobacter spp. continue their rapid spread. Antimicrobial conservation/stewardship programs have seen some measure of success in reducing antimicrobial overuse in humans, but their reach is limited to acute-care settings in high-income countries. Both horizontal and vertical infection control measures can interrupt transmission, but many of these are costly and essentially limited to high-income countries as well. Novel antimicrobials are urgently needed; however, in recent decades pharmaceutical companies have largely abandoned antimicrobial discovery and development given their high costs and low yield. International and cross-disciplinary collaboration appears to be gaining interest, although specific strategies still need to be defined. Educational programs targeting both antimicrobial prescribers and consumers must be further developed and supported. The general public must continue to be made aware of the current scale of the antimicrobial resistance threat. To address this issue, an improvement to antibiotic stewardship and recognition that this is a global health issue is essential. The prescribing behavior of healthcare practitioners is affected by many factors including demands from patients because the effect of antibiotic use extends beyond individual patients. There is a public health imperative for use to be closely monitored and a balance needs to be struck between limiting the availability of antibiotics and ensuring timely treatment for severe infections. Such a balance is difficult in countries with advanced healthcare systems but is more difficult in resource-limited settings. However, the increasing resistance shown by Enterobacteriaceae, originating in developing countries, shows that resistance is a serious threat not only in these countries but can spread globally. Concerted global action is needed to tackle this problem and, at the same time, ensure equity of access to effective treatments. Strategies in under-resourced countries need to be practical, need to include availability of microbiologic tests, better infection control, education programs for providers and guidelines for use of agents appropriately.

Consequences of stewardship

Cost savings are not and should not be the primary ambition of an AMS program. Cost savings are a natural consequence of improved patient outcomes by decreasing unnecessary antibiotic use, increasing adherence with antimicrobial treatment principles, and improving antimicrobial dose, timing and duration and reduced antimicrobial use. As shown in a study by Moellering, [3] AMS can prevent the selection of antimicrobial resistant bacteria, prevent hospital acquired infection (HAI) such as C. difficile (CDI), lead to improved patient safety and outcomes, and decrease hospital costs.


  Conclusion Top


Antimicrobial resistance is not new and it is not going away. Development of new antimicrobial drugs remains alarmingly slow, while resistance rates are rapidly increasing. Antimicrobial stewardship programs are essential for the maintenance of current antibiotics but have also been shown to decrease infection rates of multidrug resistant organisms and C. difficile, improve patient outcomes and length of stay, as well as reduction of costs. Effective AMS programs can be financially self-supporting and improve patient care. Administrative support and collaboration with other services are key components of an AMS program. The recognition that resistance is a global issue and that we have a shared interest in addressing the problem is crucial. Antimicrobial resistance is as serious a challenge in India, as it is globally. To tackle this problem in India, "A Roadmap to Tackle the Challenge of Antimicrobial Resistance" known as the "Chennai Declaration" was established in 2012 in Chennai, India. This Declaration aims to initiate efforts to formulate a national policy to control the rising trend of antimicrobial resistance (AMR), after consultation with all relevant stakeholders and to take all possible measures to implement the strategy. The aim is to establish an implementable antibiotic policy. This should include in-hospital antibiotic monitoring, audit and feedback of antibiotic use, which should be conducted by an antibiotic stewardship team. Measures should be taken to step up microbiology laboratory and a Hospital Infection Control Committee should be established. This coordinated approach at a national and local level would improve the use of antimicrobial medications and enhance patient health outcomes, reducing resistance to antibiotics, and decreasing unnecessary costs.

 
  References Top

1.World Health Organization. WHO Global Strategy for Containment of Antimicrobial Resistance [Internet]. 2001 Available from: http://who.int/drugresistance/WHO_Global_Strategy_English.pdf [Last accessed on 2013 Dec 16].  Back to cited text no. 1
    
2.Huttner A, Harbarth S, Carlet J, Cosgrove S, Goossens H, Holmes A, et al. Antimicrobial resistance: A global view from the 2013 World Healthcare-Associated Infections Forum. Antimicrob Resist Infect Control 2013;2:31.  Back to cited text no. 2
[PUBMED]    
3.Moellering RC Jr, Graybill JR, McGowan JE Jr, Corey L, American Society for Microbiology. Antimicrobial resistance prevention initiative-an update: Proceedings of an expert panel on resistance. Am J Infect Control 2007;35:S1-26.  Back to cited text no. 3
    
4.Carlet J, Collignon P, Goldmann D, Goossens H, Gyssens IC, Harbarth S, et al. Society's failure to protect a precious resource: Antibiotics. Lancet 2011;378:369-71.  Back to cited text no. 4
[PUBMED]    
5.Hidron AI, Edwards JR, Patel J, Horan TC, Sievert DM, Pollock DA, et al. National Healthcare Safety Network Team; Participating National Healthcare Safety Network Facilities. NHSN annual update: Antimicrobial-resistant pathogens associated with healthcare-associated Infections: Annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006-2007. Infect Control Hosp Epidemiol 2008;29:996-1011.  Back to cited text no. 5
[PUBMED]    
6.Centers for Disease Control and Prevention. Get Smart: Know When Antibiotics Work [Internet]. 2013. Available from: http://www.cdc.gov/getsmart/ [Last accessed on 2013 Dec 16].  Back to cited text no. 6
    
7.Boucher HW, Talbot GH, Benjamin DK Jr, Bradley J, Guidos RJ, Jones RN, et al. Infectious Diseases Society of America. 10 × '20 Progress--development of new drugs active against gram-negative bacilli: An update from the infectious diseases society of America. Clin Infect Dis 2013;56:1685-94.  Back to cited text no. 7
[PUBMED]    
8.Centers for Disease Control and Prevention. Antibiotics Resistance Threats in the United States [Internet]. 2013. Available from: http://www.cdc.gov/drugresistance/threat-report-2013/pdf/ar-threats-2013-508.pdf [Last accessed on 2013 Dec 16].  Back to cited text no. 8
    
9.Cuzon G, Naas T, Truong H, Villegas MV, Wisell KT, Carmeli Y, et al. Worldwide diversity of Klebsiella pneumoniae that produce beta-lactamase blaKPC-2 gene. Emerg Infect Dis 2010;16:1349-56.  Back to cited text no. 9
[PUBMED]    
10.Kumarasamy KK, Toleman MA, Walsh TR, Bagaria J, Butt F, Balakrishnan R, et al. Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: A molecular, biological, and epidemiological study. Lancet Infect Dis 2010;10:597-602.  Back to cited text no. 10
[PUBMED]    
11.Bogan C, Marchaim D. The role of antimicrobial stewardship in curbing carbapenem resistance. Future Microbiol 2013;8:979-91.  Back to cited text no. 11
[PUBMED]    
12.McGowan JE. Antimicrobial Stewardship-the state of the art in 2011: Focus on outcome and methods. Infect Control Hosp Epidemiol 2012;33:331-7.  Back to cited text no. 12
[PUBMED]    
13.Dellit TH, Owens RC, McGowan JE Jr, Gerding DN, Weinstein RA, Burke JP, et al. Infectious Diseases Society of America; Society for Healthcare Epidemiology of America. Infectious Diseases Society of America and the Society for Healthcare of America. 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;44:159-77.  Back to cited text no. 13
    
14.Shlaes DM, Gerding DN, John JF Jr, Craig WA, Bornstein DL, Duncan RA, 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. Clin Infect Dis 1997;25:584-99.  Back to cited text no. 14
[PUBMED]    
15.Standiford HC, Chan S, Tripoli M, Weekes E, Forrest GN. Antimicrobial stewardship at a large tertiary care academic medical center: Cost analysis before, during, and after a 7-year program. Infect Control Hosp Epidemiol 2012;33:338-45.  Back to cited text no. 15
[PUBMED]    
16.Shrestha NK, Bhaskaran A, Scalera NM, Schmitt SK, Rehm SJ, Gordon SM. Antimicrobial stewardship at transition of care from hospital to community. Infect Control Hosp Epidemiol 2012;33:401-4.  Back to cited text no. 16
[PUBMED]    
17.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;33:405-8.  Back to cited text no. 17
[PUBMED]    
18.Society for Healthcare Epidemiology of America, Infectious Diseases Society of America, Pediatric Infectious Diseases Society. Policy Statement on Antimicrobial Stewardship by the Society for Healthcare Epidemiology of America (SHEA), the Infectious Diseases Society of America (IDSA), and the Pediatric Infectious Diseases Society (PIDS). Infect Control Hosp Epidemiol 2012;33:322-7.  Back to cited text no. 18
    
19.Bartlett JG. A call to arms: The imperative for antimicrobial stewardship. Clin Infect Dis 2011;53 Suppl 1:S4-7.  Back to cited text no. 19
[PUBMED]    
20.Ohl CA, Luther VP. Antimicrobial stewardship for inpatient facilities. J Hosp Med 2011;6 Suppl 1:S4-15.  Back to cited text no. 20
[PUBMED]    
21.Septimus EJ, Owens RC Jr. Need and potential of antimicrobial stewardship in community hospitals. Clin Infect Dis 2011;53 Suppl 1:S8-14.  Back to cited text no. 21
[PUBMED]    
22.Carling P, Fung T, Killion A, Terrin N, Barza M. Favorable impact of a multidisciplinary antibiotic management program conducted during 7 years. Infect Control Hosp Epidemiol 2003;24:699-706.  Back to cited text no. 22
    
23.Kaki R, Elligsen M, Walker S, Simor A, Palmay L, Daneman N. Impact of antimicrobial stewardship in critical care: A systematic review. J Antimicrob Chemother 2011;66:1223-30.  Back to cited text no. 23
[PUBMED]    
24.Chambers RM, Davis SL. Expanding the reach of antimicrobial stewardship. Pharmacotherapy 2013;33:118-21.  Back to cited text no. 24
[PUBMED]    
25.Moody J, Cosgrove SE, Olmsted R, Septimus E, Aureden K, Oriola S, et al. Antimicrobial stewardship: A collaborative partnership between infection preventionists and healthcare epidemiologists. Infect Control Hosp Epidemiol 2012;33:328-30.  Back to cited text no. 25
[PUBMED]    
26.The Joint Commission. Assets for Acute Care Hospital Accreditation 2011: Comprehensive Accreditation Manual for Hospitals [Internet]. 2011 Available from: http://www.jointcommission.org/assets/1/6/2011_NPSGs_HAP.pdf [Last accessed on 2013 Dec 16].  Back to cited text no. 26
    
27.Stevenson KB, Balada-Llasat JM, Bauer K, Deutscher M, Goff D, Lustberg M, et al. The economics of antimicrobial stewardship: The current state of the art and applying the business case model. Infect Control Hosp Epidemiol 2012;33:389-97.  Back to cited text no. 27
[PUBMED]    
28.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;33:398-400.  Back to cited text no. 28
[PUBMED]    
29.Savard P, Perl TM. A call for action: Managing the emergence of multidrug-resistant Enterobacteriaceae in the acute care settings. Curr Opin Infect Dis 2012;25:371-7.  Back to cited text no. 29
[PUBMED]    
30.Yam P, Fales D, Jemison J, Gillum M, Bernstein M. Implementation of an antimicrobial stewardship program in a rural hospital. Am J Health Syst Pharm 2012;69:1142-8.  Back to cited text no. 30
[PUBMED]    
31.Vettese N, Hendershot J, Irvine M, Wimer S, Chamberlain D, Massoud N. Outcomes associated with a thrice-weekly antimicrobial stewardship programme in a 253-bed community hospital. J Clin Pharm Ther 2013;38:401-4.  Back to cited text no. 31
[PUBMED]    
32.Toth NR, Chambers RM, Davis SL. Implementation of a care bundle for antimicrobial stewardship. Am J Health Syst Pharm 2010;67:746-9.  Back to cited text no. 32
[PUBMED]    
33.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;55:587-92.  Back to cited text no. 33
[PUBMED]    
34.File TM Jr, Solomkin JS, Cosgrove SE. Strategies for improving antimicrobial use and the role of antimicrobial stewardship programs. Clin Infect Dis 2011;53 Suppl 1:S15-22.  Back to cited text no. 34
[PUBMED]    
35.Trienski TL, Barrett HL, Pasquale TR, DiPersio JR, File TM. Evaluation and use of a rapid Staphylococcus aureus assay by an antimicrobial stewardship program. Am J Health Syst Pharm 2013;70:1908-12.  Back to cited text no. 35
    
36.Perez KK, Olsen RJ, Musick WL, Cernoch PL, Davis JR, Land GA, et al. Integrating Rapid Pathogen Identification and Antimicrobial Stewardship Significantly Decreases Hospital Costs. Arch Pathol Lab Med 2013;137:1247-54.  Back to cited text no. 36
[PUBMED]    
37.Lipworth AD, Hyle EP, Fishman NO, Nachamkin I, Bilker WB, Marr AM, et al. Limiting the emergence of extended-spectrum Beta-lactamase-producing enterobacteriaceae: Influence of patient population characteristics on the response to antimicrobial formulary interventions. Infect Control Hosp Epidemiol 2006;27:279-86.  Back to cited text no. 37
[PUBMED]    
38.Yeo CL, Wu JE, Chung GW, Chan DS, Chen HH, Hsu LY. Antimicrobial stewardship auditing of patients reviewed by infectious diseases physicians in a tertiary university hospital. Antimicrob Resist Infect Control 2013;2:29.  Back to cited text no. 38
[PUBMED]    
39.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;32:367-74.  Back to cited text no. 39
[PUBMED]    
40.White AC Jr, Atmar RL, Wilson J, Cate TR, Stager CE, Greenberg SB. Effects of requiring prior authorization for selected antimicrobials: Expenditures, susceptibilities, and clinical outcomes. Clin Infect Dis 1997;25:230-9.  Back to cited text no. 40
[PUBMED]    
41.LaRosa LA, Fishman NO, Lautenbach E, Koppel RJ, 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;28:551-6.  Back to cited text no. 41
[PUBMED]    
42.Dortch MJ, Fleming SB, Kauffmann RM, Dossett LA, Talbot TR, May AK. Infection reduction strategies including antibiotic stewardship protocols in surgical and trauma intensive care units are associated with reduced resistant gram-negative healthcare-associated infections. Surg Infect 2011;12:15-25.  Back to cited text no. 42
    
43.Chiu CH, Michelow IC, Cronin J, Ringer SA, Ferris TG, Puopolo KM. Effectiveness of a guideline to reduce vancomycin use in the neonatal intensive care unit. Pediatr Infect Dis J 2011;30:273-8.  Back to cited text no. 43
[PUBMED]    
44.Paul M, Andreassen S, Tacconelli E, Nielsen AD, Almanasreh N, Frank U, et al. Improving empirical antibiotic treatment using TREAT, a computerized decision support system: cluster randomized trial. J Antimicrob Chemother 2006;58:1238-45.  Back to cited text no. 44
[PUBMED]    
45.Joo EJ, Kang CI, Ha YE, Park SY, Kang SJ, Wi YM, et al. Impact of inappropriate empiric antimicrobial therapy on outcome in Pseudomonas aeruginosa bacteraemia: a stratified analysis according to sites of infection. Infection 2011;39:309-18.  Back to cited text no. 45
[PUBMED]    
46.Talpaert MJ, Gopal Rao G, Cooper BS, Wade P. Impact of guidelines and enhanced antibiotic stewardship on reducing broad-spectrum antibiotic usage and its effect on incidence of Clostridium difficile infection. J Antimicrob Chemother 2011;66:2168-74.  Back to cited text no. 46
[PUBMED]    
47.Carrico RM, Archibald LK, Bryant K, Dubberke E, Litz Fauerbach L, Garcia JG, et al. Guide to the Elimination of Clostridium difficile in Healthcare Settings [Internet]. 2008 Available from: http://www.apic.org/Resource_/EliminationGuideForm/5de5d1c1-316a-4b5e-b9b4-c3fbeac1b53e/File/APIC-Cdiff-Elimination-Guide.pdf [Last accessed on 2013 Dec 16].  Back to cited text no. 47
    
48.Dubberke ER, Gerding DN, Classen D, Arias KM, Podgorny K, Anderson DJ, et al. Strategies to prevent clostridium difficile infections in acute care hospitals. Infect Control Hosp Epidemiol 2008;29 Suppl 1:S81-92.  Back to cited text no. 48
[PUBMED]    
49.Siegel JD, Rhinehart E, Jackson M, Chiarello L; Healthcare Infection Control Practices Advisory Committee. Management of multidrug-resistant organisms in health care settings, 2006. Am J Infect Control 2007;35 Suppl 10:S165-93.  Back to cited text no. 49
    
50.Valiquette L, Cossette B, Garant MP, Diab H, Pépin J. Impact of a reduction in the use of high-risk antibiotics on the course of an epidemic of Clostridium difficile-associated disease caused by the hypervirulent NAP1/027 strain. Clin Infect Dis 2007;45 Suppl 2:S112-21.  Back to cited text no. 50
    
51.Chow K, Wang X, Curtiss R 3 rd , Castillo-Chavez C. Evaluating the efficacy of antimicrobial cycling programmes and patient isolation on dual resistance in hospitals. J Biol Dyn 2011;5:27-43.  Back to cited text no. 51
    
52.Elligsen M, Walker SA, Pinto R, Simor A, Mubareka S, Rachlis A, et al. Audit and feedback to reduce broad-spectrum antibiotic use among intensive care unit patients: A controlled interrupted time series analysis. Infect Control Hosp Epidemiol 2012;33:354-61.  Back to cited text no. 52
    
53.Cosgrove SE, Seo SK, Bolon MK, Sepkowitz KA, Climo MW, Diekema DJ, et al. Evaluation of postprescription review and feedback as a method of promoting rational antimicrobial use: A multicenter intervention. Infect Control Hosp Epidemiol 2012;33:374-80.  Back to cited text no. 53
[PUBMED]    
54.Cook PP, Rizzo S, Gooch M, Jordan M, Fang X, Hudson S. Sustained reduction in antimicrobial use and decrease in methicillin-resistant Staphylococcus aureus and Clostridium difficile infections following implementation of an electronic medical record at a tertiary-care teaching hospital. J Antimicrob Chemother 2010;66:205-9.  Back to cited text no. 54
[PUBMED]    
55.Gauthier TP, Lantz E, Heyliger A, Francis SM, Smith L. Internet-Based Institutional Antimicrobial Stewardship Program Resources in Leading US Academic Medical Centers. Clin Infect Dis 2014;58:445-6.  Back to cited text no. 55
[PUBMED]    
56.Schulz L, Osterby K, Fox B. The use of best practice alerts with the development of an antimicrobial stewardship navigator to promote antibiotic de-escalation in the electronic medical record. Infect Control Hosp Epidemiol 2013;34:1259-65.  Back to cited text no. 56
    
57.Hayashi Y, Paterson DL. Strategies for reduction in duration of antibiotic use in hospitalized patients. Clin Infect Dis 2011;52:1232-40.  Back to cited text no. 57
[PUBMED]    
58.Pogue JM, Marchaim D, Chopra T, Bheemreddy S, Lee J, Mudegowdra NS, et al. Evaluation of the potential impact of a carbapenem de-escalation program in an academic healthcare system. Journal of Infection and Public Health [Internet]. 2013 Nov; Available from: http://linkinghub.elsevier.com/retrieve/pii/S1876034113001287 [Last accessed on 2013 Dec 3].  Back to cited text no. 58
    
59.Lee SO, Lee ES, Park SY, Kim SY, Seo YH, Cho YK. Reduced use of third-generation cephalosporins decreases the acquisition of extended-spectrum beta-lactamase-producing Klebsiella pneumoniae. Infect Control Hosp Epidemiol 2004;25:832-7.  Back to cited text no. 59
[PUBMED]    
60.Madaras-Kelly KJ, Remington RE, Lewis PG, Stevens DL. Evaluation of an intervention designed to decrease the rate of nosocomial methicillin-resistant Staphylococcus aureus infection by encouraging decreased fluoroquinolone use. Infect Control Hosp Epidemiol 2006;27:155-69.  Back to cited text no. 60
[PUBMED]    
61.Lan CK, Hsueh PR, Wong WW, Fung CP, Lau YT, Yeung JY, et al. Association of antibiotic utilization measures and reduced incidence of infections with extended-spectrum beta-lactamase-producing organisms. J Microbiol Immunol Infect 2003;36:182-6.  Back to cited text no. 61
[PUBMED]    
62.Trubiano J, Phillips E. Antimicrobial stewardship´s new weapon? A review of antibiotic allergy and pathways to "de-labeling". Curr Opin Infect Dis 2013;26:526-37.  Back to cited text no. 62
[PUBMED]    




 

Top
 
 
  Search
 
Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

 
  In this article
Abstract
Introduction
Conclusion
References

 Article Access Statistics
    Viewed5191    
    Printed157    
    Emailed0    
    PDF Downloaded567    
    Comments [Add]    

Recommend this journal


[TAG2]
[TAG3]
[TAG4]