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Department of Biochemistry, University of Agriculture Faisalabad, Faisalabad, Pakistan
Ghulam Mustafa*
Department of Biochemistry, Government College University Faisalabad, Faisalabad, Pakistan
*Address all correspondence to: drghulammustafa@gcuf.edu.pk
1. Introduction to antimicrobial stewardship
Antimicrobial stewardship (AMS) refers to interventions and control programs for the optimization of antibiotic usage. Antimicrobial stewardship is growing fastly in numbers with diverse contexts ranging from hospitals to the veterinary community [1]. Despite much acceptance, the term is still facing many challenges in different communities. There are different ways to view antimicrobial stewardship such as a collection of coordinated interventions, a program, a philosophy, and an ethic [1]. Antimicrobial stewardship policies are mainly focused on the optimization of antibiotic usage to reduce antimicrobial resistance and improvement of patients’ outcomes and hospital hygiene in different healthcare centers. This may involve creating criteria for the use of antibiotics, such as limiting their use to specific indications or restricting certain antibiotics to specific patient populations [2]. Various antimicrobial stewardship strategies have been mentioned in Figure 1.
Figure 1.
Various antimicrobial stewardship strategies used to overcome antimicrobial resistance.
Antimicrobial stewardship programs (ASPs) are typically led by multidisciplinary teams of healthcare professionals, including infectious diseases specialists, pharmacists, and microbiologists. These teams work together to develop and implement strategies for promoting the appropriate use of antimicrobial agents [3]. The primary strategies of ASPs include prospective auditing and feedback, pre-authorization, dose optimization, hospital education, computer monitoring, and antibiotic restriction. Regular evaluation of outcomes of these programs can help identify areas to further improve and ensure that the programs are meeting their desired goals [4].
Antimicrobial stewardship policies are important for promoting the responsible use of antibiotics and reducing the risk of antibiotic resistance. By implementing these policies, healthcare providers can help ensure that antibiotics remain effective for future generations. In this current article, the policies to cope with the ongoing problems with uprising challenges have been discussed for the understanding of the importance of antimicrobial stewardship in the medical sector for the management of antibiotic resistance.
Antimicrobial resistance is the ability of microorganisms to withstand the effects of antimicrobial drugs and it develops when an antibiotic loses its ability to effectively stop microbial growth. Antibiotic resistance is a growing global health concern, as it can lead to longer hospital stays, higher healthcare costs, and increased mortality rates. When antibiotics are overused or misused, bacteria are exposed to drugs unnecessarily, and those that survive develop resistance to the antibiotics used [5]. Antimicrobial resistance (AMR) jeopardizes not only public health but also economic growth and security. Based on high-level predictions and global reports, AMR has the potential to result in 10 million fatalities worldwide by 2050 [6]. The Centers for Disease Control and Prevention (CDC) has estimated that antibiotic resistance increases direct healthcare expenditures in the United States by $20 billion annually, excluding the estimated $35 billion in productivity losses [7].
The wide spread of antimicrobials has resulted in the expression of resistance to these antimicrobial agents. Resistance-encoding genes have been probably present for thousands of years, either as a defense against antibiotics or for unknown purposes, and the incorporation of these genes by human commensal and pathogenic flora has been quickly followed [8]. The mass production of antimicrobials has provided humanity with a temporary advantage in the battle against microorganisms however, if the current rate of increase in antimicrobial resistance continues, we may enter the postantibiotic era [8].
Various programs and strategies have been developed over the years to reduce antimicrobial resistance and promote the proper and effective use of antibiotics [9]. The antimicrobial stewardship programs (ASPs) have attracted a lot of attention as one of the most important strategies for combating AMR. Antimicrobial stewardship is a coordinated approach to promote the appropriate use of antibiotics and other antimicrobial agents in healthcare settings [3].
Since the 1940s, different educational programs, management strategies, clinical protocols, and guidelines have been developed by infectious-disease organizations to control and prevent microbial infections in various sectors [10]. In the United States, the Centers for Disease Control and Prevention (CDC) launched the first educational program in 2009 to advocate for the rational use of antibiotics in acute-care settings, and improved antibiotic use as a strategy was adopted in 2013 to address the problem [11]. In 2015, World Health Organization (WHO) issued a global action plan (GAP) on the appropriate use and effects of antibiotics on humans and animals along with the validity of antibiotics for future generations as the main aim of GAP [12].
AMS has a positive impact in hospitals with shorter lengths of stay, shorter treatment duration without an increase in mortality, and a decrease in colonization and infection with resistant bacteria. Many studies have been conducted on interventions aimed at outpatient prescribers proving the prominent reduction in antibiotic prescriptions and resistance rates [11, 13]. The government urged in 2017 that all hospitals include stewardship programs in their organizational mandates. In 2017, European Commission issued reports that highlighted the successful implementation of AMS in clinical communities of different countries [14].
Antimicrobial resistance has been increased by the indiscriminate and injudicious use of antibiotics. Bacterial strains are adapted to new resistance mechanisms due to the abuse of sophisticated antibiotics. Bacteria have developed innovative strategies to combat the currently available antibiotics. Many antibiotics have become ineffective due to the modification of penicillin-binding proteins, and the development of beta-lactamases [15]. The term antimicrobial stewardship refers to appropriate measures and a set of coordinated guidelines for the optimization and selection of antimicrobial usage. The professionals should know the duration and type of antibiotics based on pathogenic identification. The chemists, microbiological labs, and infection control agents should work together to guide and assist decision-making persons about antibiotics, dose, and administration routes for maximum output. The global interdisciplinary committee has been trying to optimize the consumption of antibiotics through different antimicrobial stewardship programs to restrict resistance patterns [16].
Antimicrobial stewardship consists of two main strategies and the most effective programs typically combine both of them. The first pre-prescription approach includes the strict authorization and prescription of certain antimicrobials by a selected group of clinicians. These antimicrobial drugs need special approval and a specific time duration which depends on local microbial resistance patterns in different microbial infections. The other post-prescription approach mainly deals with perspective feedback and reviews for prescribed antibiotics to observe the outcomes for dose optimization (Table 1). Based on the available microbiology data and the clinical aspects of different cases, the antimicrobial steward analyses current antimicrobial treatments and offers clinicians the to continue, modify, change, or stop the medication [18].
Policies
Description
Leadership commitment
Senior management and clinicians who can make decisions regarding the allocation of resources and program implementation.
Accountability and drug expertise
A designated individual or team should be responsible for implementing and managing the antibiotic stewardship program. The team should have expertise in infectious diseases, clinical microbiology, and pharmacology.
Implementing evidence-based policies
Policies and guidelines that reflect evidence-based practices for appropriate antibiotic use. These policies should include recommendations for antibiotic selection, dosing, and duration of therapy.
Antibiotic monitoring and tracking
Antibiotic use and resistance patterns should be monitored to identify areas for improvement and outcomes of interventions should be tracked to evaluate the effectiveness of the stewardship program.
Education and communication
Regular education and communication with healthcare providers, patients, and families are essential to promote appropriate antibiotic use and reduce unnecessary prescribing.
Antimicrobial stewardship interventions
The stewardship program should include interventions such as prospective audits and feedback, clinical guidelines, pathways for antimicrobial order sets, and educational programs for healthcare providers.
Reporting and feedback
Antibiotic use and resistance data should be regularly reported to clinicians and healthcare leaders to promote transparency and accountability for antibiotic prescribing practices.
Table 1.
Core approaches for antimicrobial stewardship programs [17].
Patient risk factors and subjectivity should be considered as the major factor for the prescription of antibiotics. Antimicrobial stewardship needs to be followed up and assessed using relevant and acceptable outcome indicators such as intensity of antibiotics consumption, antibiotics resistance and consumption rate, financial condition, and morbidity and mortality rates [19].
Recent meta-analyses and systematic reviews on antimicrobial stewardship policies show the possibility of lowering comparable outcomes in a variety of healthcare settings (Table 2).
Country
Settings
Design
Duration
interventions
Measured results
Reference
China
Secondary and tertiary hospitals
Retrospective observational study
2010–2016
AMS campaign
Antibiotic consumption, prescriptions and expense rate, Resistance rates
Prospective quasi-experimental, Interrupted time-series study
2014 and 2017
Non-restrictive ASP
Antibiotic prescriptions and cost, mean LOS, CDI incidence rate, and mortality rate in the group of patients who were transferred from emergency rooms to medical wards
The purpose of antimicrobial stewardship programs is to optimize the use of antimicrobial drugs in healthcare facilities such as hospitals, long-term care homes, and outpatient clinics. These initiatives aim to raise patients’ outcomes, control the spread of antibiotic resistance, and cut back on medical expenses.
7.1 Healthcare facility
A list of core components for healthcare facilities has been developed to assist facility management in creating the frameworks required to implement sustainable AMS programs. The core elements are comprised of financial funding, a multidisciplinary dedicated team, health professionals, up-to-date standard treatment recommendations, regular feedback and reviews, and an AMS action plan that sets priorities, evaluates performance, and establishes accountability, collaboration with other programs, a list for healthcare facilities that include a list of restricted antibiotics, basic training for optimal antibiotics use, monitoring quality, susceptibility, types, and resistance rate of antibiotics and medical records and prescription records for the institution (Figure 2).
Figure 2.
Core elements of the healthcare facility for antimicrobial stewardship programs.
7.2 AMS planning programs
AMS programs should be interlinked with other programs for the optimization of antibiotic usage. A large tertiary hospital with many different specialties will have a larger and more sophisticated AMS program than a local hospital. The deployment of an AMS program is a dynamic and step-by-step process where each facility is built on the infrastructure that already exists [26]. AMS programs conduct situational analysis and faculty action plans based on core elements to identify the missing elements. The situational analysis consists of opportunities, barriers, and enablers at different levels for the participation of clinical professionals. The AMS committee can function independently or it can be integrated into an existing framework such as the infection control, patient safety, drugs and therapeutics committee to define the scope of the work. An infectious disease specialist with interest and experience in infectious illnesses can give expertise to the infection management team. This individual serves as the primary hand for the AMS team for helping with drug prescription, diagnosis, and patient management for the optimization of antibiotics to treat infections [27].
Patients care should be taken by nurses and expert staff of hospitals because they know the entire first-hand disease history of the patients [28]. This AMS team member should be focused on the timely administration of antibiotics without delaying any dose, therapeutic drug monitoring, high-quality microbiological sampling, and results discussion to promote the accurate prescription of antibiotics. Moreover, nurses should cooperate to monitor the patient’s clinical progress, antibiotic consumption intensity, and identify the conditions to shift the route of antibiotics from intravenous (IV) to oral, educate patients, and handle the data collection for feedback and reviews [17].
7.3 Selection and dosing of appropriate antibiotics
The infectious disease workers should recommend the correct duration of treatment with an optimized drug dosage to secure the target more accurately in the shortest period with minimal toxicity. The IV drugs should be shifted to the oral route of administration to shorten the patient’s stay at the hospital to avoid catheter-associated infections. The infectious diseases team should follow evidence-based recommendations for the duration of the treatment. The treatment plan for gram-positive and gram-negative bacteria is also established based on the identified pathogen(s) to avoid unnecessary prolonged treatments [29].
Understanding and utilizing pharmacokinetics and pharmacodynamics by hospital and clinical pharmacists is necessary for choosing appropriate antibiotic doses that can help to reduce the use of unnecessary drugs for double therapy. Nursing staff can help explore alternative medicines by accurately documenting and updating antibiotic allergies on a regular basis [30].
The antimicrobial stewardship program is challenging due to limited human resources, formal programs, and policies. Antimicrobial stewardship programs require a significant investment of time, money, and resources to implement and maintain.
8.1 Healthcare challenges
The healthcare sector faces major challenges due to lack of equipment, improper infrastructure, large patient burden, and shortage of hospital facilities. These challenges were frequently reported in rural areas due to irrelevant antibiotic prescriptions and malpractices in the healthcare system [31]. In developed countries, hospitals have special antibiotics committees that monitor the antibiotics usage, treatment plans, and evaluate the implementation of hospital’s stewardship interventions [32].
8.2 Diagnostic challenges
High burden of infectious diseases has limited the availability of microbiology diagnostic laboratories [33]. There is a dire need for necessary equipment, standard operating protocols, well-trained staff, and quality control systems in diagnostic laboratories [34]. Correct pathogen identification and susceptibility testing are difficult due to the large number of antibiotics that could potentially be tested, the multiple techniques and media needed, and the analysis and validation of unlikely resistance profiles. High testing threshold, lack of experienced microbiologists, and habitat culture media are the main crises due to financial constraints [35].
8.3 Educational challenges
The lack of professional clinical staff has been recorded as the main problem in the path of antimicrobial stewardship practice. In rural areas, antibiotics are prescribed and/or provided in many cases by a diverse group of people including healthcare workers with different learning backgrounds (e.g., nurses, dispensers, chemists, and midwives) as well as local vendors. Many healthcare providers may not have adequate education and training on appropriate antimicrobial use. This can make it difficult for them to make informed decisions about prescribing antimicrobials [36].
Antimicrobial stewardship should be a core element for healthcare workers to fully access over risks of antibiotic misuse and its outcomes for the patients. The development of protocols and guidelines is a mandatory step for the education of medical students and clinical workers. Providers may be educated on the principles of antimicrobial stewardship, appropriate prescribing practices, and the risks associated with inappropriate antibiotic use [13].
8.4 Limited access to antibiotics
Many underdeveloped countries have poor access to different antibiotics in rural and remote areas due to a lack of financial aid, transport, storage, and reliable drug supply system. Limited access to antibiotics can lead to increased morbidity and mortality rates, as well as the spread of infectious diseases [37]. The widespread of non-prescribed antibiotics is another potentially challenging threat for the public sector. Many drugs may be difficult to trace in terms of their sources, quality, and supply chain and the pharmaceutical corporations’ influence is frequently neither visible nor regulated [38]. Moreover, US Food and Drug Administration and the European Medicines Agencies have little or no medical access in low- and middle-income countries [39].
The World Health Organization (WHO) has set different roadmaps to monitor the establishment of antimicrobial stewardship policies. The necessity for monitoring and investigation, infection prevention, and control strategies such as immunization and the development of an economic argument for long-term investment in antibiotics have all been mentioned by them as being important components of a complete approach. The availability of affordable and high-quality diagnostic kits and tools, continuous surveillance, and equal distribution of antibiotics is urgently needed as core elements of AMS [12].
The WHO provides a framework for creating National Action Plans (NAP) and analysis systems for a country’s progress evaluation. The US Center for Disease Dynamics, Economics and Policy (CDDEP) is funding the establishment of multisectoral national-level working groups in low- and middle-income countries to comprehend and document antibiotic use in human and animal populations in the national context as well as of developing evidence-based interventions [13].
The global action plan extends current efforts on smart drug use and national medicines policy including the use of essential pharmaceutical lists, concerning the regulation of antibiotic availability, quality, and use at the national level. For instance, despite increasing antibiotic resistance in many countries, national essential drug lists in many underdeveloped countries still do not include specific antibiotics such as carbapenems, glycopeptides, or polymyxins. Moreover, programs such as the Global Antibiotic Research and Development Partnership (GARDP), which aims to use partnership models rather than a pharmaceutical industry-driven strategy to create novel antibiotic treatments may be capable of ensuring ethical use and unlimited access to different antibiotics [40].
Targeted strategies such as shifting from intravenous to dosage form, improving surgical antibiotic prophylaxis, and introducing standard antibiotic formulations might be taken into consideration. Improving antibiotic hang time is another easy approach to improving patients’ outcomes [41].
Hospital-based antimicrobial stewardship programs (ASPs) use several coordinated strategies to optimize the use of antibiotics. Verma et al., [42] have reported pre- and post-intervention study designs that compared the outcomes of AMS on patients admitted from November 2017 to January 2018. Daily assessments and feedbacks, restrictions on the use of antibiotics, daily bedside evaluations, and educational activities to raise awareness among residents and nurses were part of the ASP interventions. The study involved the prescription of 1331 antibiotics to 695 patients. Prophylactic antibiotic use was decreased by 11% (p = 0.001) in this period. In terms of length, choice, indication, and method of administration, the prescription pattern was considerably improved in the intervention phase compared to the pre-intervention phase by 8%, 14%, 2%, and 8%, respectively. The outcomes of this study indicated positive feedback on the implementation of AMS in hospital units for the optimization of antibiotic dosage.
Jones et al., [43] presented the hypothesis of the positive relationship of professional healthcare workers with the success of AMS. During six months intervention period, antibiotic consumption was lowered by 6.5% compared to previous years’ reports. A daily review of antibiotics prescription and administration documentation was significantly improved.
Similarly, [44] conducted telehealth-based antimicrobial stewardship programs in two hospitals. In six months duration, 1419 proposals were presented and 1262 (88.9%) of them were followed through with a 24.4% decrease in broad-spectrum antibiotic consumption. Antimicrobial expenses were estimated to save $1,42,629.83 annually. An intensive ASP strategy enabled in the community hospital context via telehealth resulted in a lower broad-spectrum antibiotic usage and minimum antimicrobial expenses.
11. Conclusion
The rising frequency of antibiotic resistance in hospitals as well as communities is an urgent issue as hospitalized patients become more difficult to treat. To address the problem(s) of AMR, it is important to promote the appropriate use of antimicrobial drugs, develop new and more effective drugs, and improve infection prevention and control practices in healthcare settings and the community. Antimicrobial stewardship practices, concepts, and interventions are the key stages in the prevention and control of antimicrobial resistance. Antimicrobial stewardship may offer every professional the tools they need to use valuable resources.
References
1.Dyar O et al. What is antimicrobial stewardship? Clinical Microbiology and Infection. 2017;23(11):793-798
2.Schuts EC et al. Current evidence on hospital antimicrobial stewardship objectives: A systematic review and meta-analysis. The Lancet Infectious Diseases. 2016;16(7):847-856
3.Ababneh MA, Nasser SA, Rababa’h AM. A systematic review of antimicrobial stewardship program implementation in middle eastern countries. International Journal of Infectious Diseases. 2021;105:746-752
4.Barlam TF et al. Implementing an antibiotic stewardship program: Guidelines by the Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America. Clinical Infectious Diseases. 2016;62(10):e51-e77
5.Nadeem SF et al. Antimicrobial resistance: More than 70 years of war between humans and bacteria. Critical Reviews in Microbiology. 2020;46(5):578-599
6.Nathwani D et al. Value of hospital antimicrobial stewardship programs [ASPs]: A systematic review. Antimicrobial Resistance & Infection Control. 2019;8:1-13
7.Dadgostar P. Antimicrobial resistance: Implications and costs. Infection and drug resistance. 2019;12:3903-3910
8.MacDougall C, Polk RE. Antimicrobial stewardship programs in health care systems. Clinical Microbiology Reviews. 2005;18(4):638-656
9.Pollack LA, Srinivasan A. Core elements of hospital antibiotic stewardship programs from the Centers for Disease Control and Prevention. Clinical Infectious Diseases. 2014;59(suppl_3):S97-S100
10.Rosenblatt-Farrell N. The landscape of antibiotic resistance. Environmental Health Perspectives. 2009;117(6):A244-A250
11.Davey P, et al. Interventions to improve antibiotic prescribing practices for hospital inpatients. Cochrane Database of Systematic Reviews. 2017;2:14651858
12.World Health Organization. Global action plan on antimicrobial resistance. Geneva, Switzerland: World Health Organization; 2015. ISBN 978 924 1509763
13.Cox JA et al. Antibiotic stewardship in low-and middle-income countries: The same but different? Clinical Microbiology and Infection. 2017;23(11):812-818
14.Majumder MAA et al. Antimicrobial stewardship: Fighting antimicrobial resistance and protecting global public health. Infection and drug resistance. 2020;13:4713-4738
15.Rice LB. Antimicrobial stewardship and antimicrobial resistance. Medical Clinics. 2018;102(5):805-818
16.Sahra S, Jahangir, De Chavez V. Antimicrobial stewardship: A review for internal medicine physicians. Cureus. 2021;13(4):e14385
17.World Health Organization. Antimicrobial Stewardship Programmes in Health-Care Facilities in Low- and Middle-Income Countries. Geneva, Switzerland: A Who Practical Toolkit; 2019. ISBN 978-92-4-151548-1
18.Doron S, Davidson LE. Antimicrobial stewardship. Mayo Clinic Proceedings. 2011;86(11):1113-1123
19.Horikoshi Y et al. Sustained pediatric antimicrobial stewardship program with consultation to infectious diseases reduced carbapenem resistance and infection-related mortality. International Journal of Infectious Diseases. 2017;64:69-73
20.Xiao Y et al. Change in antibiotic use in secondary and tertiary hospitals nationwide after a national antimicrobial stewardship campaign was launched in China, 2011–2016: An observational study. The Journal of Infectious Diseases. 2020;221(Supplement_2):S148-S155
21.Mardani M, Abolghasemi S, Shabani S. Impact of an antimicrobial stewardship program in the antimicrobial-resistant and prevalence of clostridioides difficile infection and amount of antimicrobial consumed in cancer patients. BMC Research Notes. 2020;13(1):1-5
22.Savoldi A et al. Impact of implementing a non-restrictive antibiotic stewardship program in an emergency department: A four-year quasi-experimental prospective study. Scientific Reports. 2020;10(1):1-8
23.Wee LE et al. Who listens and who doesn’t? Factors associated with adherence to antibiotic stewardship intervention in a Singaporean tertiary hospital. Journal of Global Antimicrobial Resistance. 2020;22:391-397
24.Abubakar U, Syed Sulaiman SA, Adesiyun AG. Impact of pharmacist-led antibiotic stewardship interventions on compliance with surgical antibiotic prophylaxis in obstetric and gynecologic surgeries in Nigeria. PLoS One. 2019;14(3):e0213395
25.Wang H et al. Impact of antimicrobial stewardship managed by clinical pharmacists on antibiotic use and drug resistance in a Chinese hospital, 2010–2016: A retrospective observational study. BMJ Open. 2019;9(8):e026072
26.Mendelson M et al. How to start an antimicrobial stewardship programme in a hospital. Clinical Microbiology and Infection. 2020;26(4):447-453
27.Goff DA, Rybak MJ. Global antimicrobial stewardship: challenges and successes from frontline stewards. 2015;4(Suppl 1):S1S3
28.Brink AJ et al. Passing the baton to pharmacists and nurses: New models of antibiotic stewardship for South Africa?: Guest editorial. South African Medical Journal. 2016;106(10):947-948
29.Sampathkumar P. Reducing catheter-associated urinary tract infections in the ICU. Current Opinion in Critical Care. 2017;23(5):372-377
30.Satterfield J, Miesner A, Percival K. The role of education in antimicrobial stewardship. Journal of Hospital Infection. 2020;105(2):130-141
31.Zhang C et al. The professional status of infectious disease physicians in China: A nationwide cross-sectional survey. Clinical Microbiology and Infection. 2018;24(1):82. e5-82. e10
32.Howard P et al. An international cross-sectional survey of antimicrobial stewardship programmes in hospitals. Journal of Antimicrobial Chemotherapy. 2015;70(4):1245-1255
33.Feikin DR et al. The burden of common infectious disease syndromes at the clinic and household level from population-based surveillance in rural and urban Kenya. PLoS One. 2011;6(1):e16085
34.Barbé B et al. Implementation of quality management for clinical bacteriology in low-resource settings. Clinical Microbiology and Infection. 2017;23(7):426-433
35.Om C et al. “If it’sa broad spectrum, it can shoot better”: Inappropriate antibiotic prescribing in Cambodia. Antimicrobial Resistance & Infection Control. 2016;5(1):1-8
36.Morgan DJ et al. Non-prescription antimicrobial use worldwide: A systematic review. The Lancet Infectious Diseases. 2011;11(9):692-701
37.Pulcini C et al. Ensuring universal access to old antibiotics: A critical but neglected priority. Clinical Microbiology and Infection. 2017;23(9):590-592
38.Parry J. Former Head of GSK China Is Charged with Bribery. British Medical Journal Publishing Group; 2014
39.Collignon P, et al. Antimicrobial resistance: the major contribution of poor governance and corruption to this growing problem. PloS one. 2015;10(3):e0116746
40.World Health Organization. WHO Model List of Essential Medicines, 20th List (March 2017, Amended August 2017). Geneva, Switzerland: World Health Organization; 2017
41.Messina AP, van den Bergh D, Goff DA. Antimicrobial stewardship with pharmacist intervention improves timeliness of antimicrobials across thirty-three hospitals in South Africa. Infectious Diseases and Therapy. 2015;4:5-14
42.Verma M et al. Antimicrobial stewardship programme in a trauma Centre of a tertiary care hospital in North India: Effects and implementation challenges. Journal of Global Antimicrobial Resistance. 2019;17:283-290
43.Jones AS, et al. Impact of positive feedback on antimicrobial stewardship in a pediatric intensive care unit: A quality improvement project. Pediatric quality & safety. 2019;4(5):e206
44.Shively NR et al. Impact of a telehealth-based antimicrobial stewardship program in a community hospital health system. Clinical Infectious Diseases. 2020;71(3):539-545
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