|Year : 2020 | Volume
| Issue : 2 | Page : 122-129
Knowledge and perceptions of antimicrobial stewardship program among health-care students in Saudi Arabia
Rina Tripathi1, Ahmed A Albarraq1, Hafiz A Makeen1, Saad S Alqahtani1, Pankaj Tripathi2, Shyam Sunder Pancholi3
1 Department of Clinical Pharmacy, Pharmacy Practice Research Unit (PPRU), College of Pharmacy, Jazan University, Jazan, Kingdom of Saudi Arabia
2 Department of Pharmacology, College of Pharmacy, Jazan University, Jazan, Kingdom of Saudi Arabia
3 Department of Pharmaceuitcs, College of Pharmacy, Jazan University, Jazan, Kingdom of Saudi Arabia
|Date of Submission||11-Nov-2019|
|Date of Decision||27-Jun-2020|
|Date of Acceptance||22-Jul-2020|
|Date of Web Publication||19-Aug-2020|
Department of Pharmacology, College of Pharmacy, Jazan University, Jazan
Kingdom of Saudi Arabia
Source of Support: None, Conflict of Interest: None
Background: National antimicrobial stewardship program (AMS) is an initiative to prevent antibiotic misadventures. Currently, AMS is not compulsory as part of the undergraduate health-care students in Saudi Arabia. Identifying gaps in knowledge and a better understanding of their perceptions about AMS could assist in recommendations for appropriate changes to the curricula that may lead to more appropriate use of antimicrobials within the multidisciplinary team. Objective: The objective of this study was to assess the AMS knowledge and perceptions among health-care students – pharmacy, medicine, dental, nursing, and microbiology. Methods: A cross-sectional, descriptive survey was conducted among health-care students of different colleges of Jazan University, Saudi Arabia. Collected data were analyzed using SPSS version 23. Results: A questionnaire was supplied to 563 students and 390 (69.27%) responded. AMS was known to 71% of the participants, while 50.3% were familiar with AMS in Saudi Arabia, with a significant difference among students of different health-care colleges. The broad appreciation of AMS goals, team members, and role of pharmacist was more among dental, microbiology, and pharmacy students as against nursing and general medicine. All health-care students possess good knowledge about causes of antimicrobial resistance (AMR). Formal training on AMS was received by merely 48.97% of the participants. A clear majority (80.8%) opined that better understanding of antimicrobial use is important for career, and 79.0% registered a need of incorporating AMS training in curricula. Conclusions: Concepts of AMS need to be included in the undergraduate health-care curricula to promote the rational use of antimicrobials and minimize incidences of AMR to improve clinical outcomes.
Keywords: Antimicrobial resistance, antimicrobial stewardship, health-care students, Jazan University, Saudi Arabia
|How to cite this article:|
Tripathi R, Albarraq AA, Makeen HA, Alqahtani SS, Tripathi P, Pancholi SS. Knowledge and perceptions of antimicrobial stewardship program among health-care students in Saudi Arabia. Saudi J Health Sci 2020;9:122-9
|How to cite this URL:|
Tripathi R, Albarraq AA, Makeen HA, Alqahtani SS, Tripathi P, Pancholi SS. Knowledge and perceptions of antimicrobial stewardship program among health-care students in Saudi Arabia. Saudi J Health Sci [serial online] 2020 [cited 2020 Sep 30];9:122-9. Available from: http://www.saudijhealthsci.org/text.asp?2020/9/2/122/292644
| Introduction|| |
The introduction of antimicrobials for treatment marked an era of unprecedented advances in medical and societal history. However, recently irrational use of antimicrobials has been increased leading to emergence and spread of new antimicrobial resistance (AMR) mechanisms globally. The rise in prevalence of AMR is intimidating our ability to cure infections. There is a consequential increase in the cost of health care, incidences of prolonged illness, disability, and death. As per the World Health Organization (WHO), the AMR has attained such a grievous scale that it should be considered as a major threat to basic human health. The annual global deaths attributable to AMR are estimated to be 700,000 as per a 2016 study, commissioned by the UK government, and this may approach to 10 million annual deaths by 2050 if an urgent action is not taken to handle the situation with appropriate remedial measures. AMR is likely to rank number one among the principal causes of death, and this can have an economic impact of up to 100 trillion US dollars. Despite the continuous efforts made by the WHO to curb the menace of irrational use of antimicrobials, the share of antimicrobial drugs purchased without prescription is estimated to be highest in Asia (58%), followed by Southern Europe (47%), Middle East (39%), Eastern Europe (30%), and South America (25%).
Relatively high incidences of self-medication of antibiotics (up to 48%) have been reported among Saudis as per a 2012 study, and thus, the Kingdom of Saudi Arabia (KSA) ranks highest among all Gulf Cooperation Council (GCC) countries regarding the prevalence of AMR. In Riyadh city of KSA, as per a cross-sectional study, around 79% of the participants purchased at least one antibiotic without a prescription. Further, antimicrobial utilization is suboptimal in Saudi Arabia. Thus, recognizing the urgency to improve antibiotic utilization in hospitals, the Centers for Disease Control and Prevention has issued a recommendation that AMS shall be implemented in all acute care hospitals. Globally, most of the countries have established AMS to address the critical problem of AMR.,,,,,,
The term antimicrobial stewardship refers to coordinated efforts aimed to minimize the incidences of AMR by means of improving the selection of optimal antimicrobial drug, dose, duration of therapy, and route of administration., Antimicrobial stewardship interventions can only be successful if they meet the specific needs of the health-care institutions with a coordinated effort of dedicated multifaceted, multidisciplinary team (pharmacists, physicians, and nurses), administrators, and policy-makers.
Antimicrobial stewardship programs (AMSs) are still in their infancy in the Middle East, but the efforts are currently being put forth to further develop these programs. From the year 2012, the pharmacy strategic plan was implemented by general administration of pharmaceutical care at the Ministry of Health (MOH) in Saudi Arabia, with more than thirty national programs of pharmacy practice started during the period 2012–2015 – one among them is National AMS., At MOH, in late 2014, a memorandum was sent by a Central Committee to start the AMS at every hospital in KSA, and this memo got activated in early 2015. A recent prospective study on stepwise implementation of AMS in a tertiary care university hospital of Saudi Arabia suggested that it is a safe and cost-effective strategy for improving the practice of prescribing antibiotics and to minimize the occurrence of multidrug resistance. Meanwhile, MOH has also implemented the Executive Regulations of Health Practice Law that prohibits the antibiotic uses without a prescription.
The WHO aims to avert potential AMRs by putting a restrain on irrational antimicrobial prescribing and has recommended the need of making the health-care team aware about AMS., Limited data are available about the extent and effectiveness of the AMS education among Saudi health-care students. This study was, therefore, planned to assess the extent of knowledge and perception about concepts of antimicrobial stewardship among final-year health-care students of Jazan University, including pharmacy, general medicine, dental, nursing, and microbiology. The study aims to identify the gaps in curricular knowledge and practice needed for implementation of effective AMS and attempts to provide appropriate recommendations for improvement in undergraduate curricula. A special training may be highly prioritized to ensure that future health-care professionals stick to appropriate use of antimicrobials. Further, there may be a need of new policy formulation or modification of the prevailing policy to address the unique needs of AMS.
| Methods|| |
Study design and population
A cross-sectional, descriptive survey was conducted among 390 health-care students of MBBS (medical), BDS (dental), Pharm D, BSc (Nursing), and microbiology programs offered at different colleges of Jazan University, Saudi Arabia, during academic session 2017–2018. All students enrolled at the university for final year of the degree or undergoing internship, representing the future generation of health-care professionals, and showing willingness to participate were included in the survey. In each class, after a regular lecture, the students were briefed about the purpose of the research. The questionnaires were then distributed to those who volunteered for participation. Participation was voluntary, and no exclusion was made on any ground.
We used denial equation to calculate required sample size. The sample size estimated was 323 based on the 95% confidence interval, 50% prevalence, and a 5% margin of error. In order to minimize error and account for nonresponders, an additional sample was included in the study.
A standardized (structured, precoded, and validated) questionnaire was developed that consisted of two parts. The first part inquires about sociodemographic information, and the second part was based on to assess the knowledge and perception of target population about (i) role of pharmacist in AMS; (ii) goals, objectives, and members of AMS; (iii) antimicrobial dispensing and development of resistance; and (iv) need of AMS education. The questionnaire used in the study was adopted from similar studies done by Abbo et al. in medical students of the USA and Burger et al. in pharmacy students of South Africa with few modifications. The prevalidation of questionnaire for readability, length, and relevance of the questions was done by administering the same to five pharmacy interns who participated voluntarily, and the language of questions was revised based on the feedback to simplify understanding.
Data collection and statistical analysis
Data were collected using a convenience sampling method and analyzed using the IBM Statistical Package for the Social Science (SPSS) version 23.0 software for windows (Armonk, NY, USA, IBM Corp.). For categorical variables, data were presented as frequencies and percentages. The differences between the responses of respondents of different healthcare departments were analyzed using a Chisquared test and were considered statistically significant for P ≤ 0.05.
The study was granted ethics approval by the “Scientific Research Ethics Committee-Jazan University” vide its letter no. 5103/702/1439, and consent for conduct of survey was obtained from the heads of each health-care college involved. Informed consent was obtained from all individual participants included before the study.
| Results|| |
The questionnaire was distributed to 563 students pursuing final year of their degree course or doing internship in respective health-care stream, namely pharmacy (A), general medicine (B), dental (C), nursing (D) and microbiology (E) during the survey period at Jazan University, out of which 390 students responded to the survey. The final-year Pharm D students contributed to 26.9% of the sample population, followed by microbiology department (25.9%) of science college, nursing (23.6%), dental BDS program (13.6%), and general medicine MBBS program (10%). The gender distribution of participants in the study was in favor of females (76.9%). The overall response rate was 69.27%, ranging from 36.55% to 99.01% for different programs and highest for microbiology, as depicted in [Table 1].
Awareness about antimicrobial stewardship
The awareness about “AMSs in KSA” was not found to be very profound among prospective health-care professionals and only half (50.3%) of the respondent population nodded in yes to the question, whether they had heard about this earlier, however, a significant difference was observed between awareness levels in different health-care colleges (47.6% A, 59% B, 71.7% C, 47.8% D, and 40.6% E; P < 0.004), as shown in [Table 2]. Majority (74.4%) agreed that implementation of AMSs in Jazan, KSA, was much desired, with responses ranging from 51.3% to 86.8% (P < 0.001), highest being for dental students. The prescribing and use of antimicrobials in Jazan were considered appropriate by only 53.1% of the total respondents, with a range from 42.6% to 69.8% (P < 0.018), and microbiology group gave least of favorable responses. There appeared an adequate understanding and concordance among majority of the participants (78.7%) that chances of AMR will be reduced by appropriate use of antimicrobials, and an affirmative response was obtained from as high as 92.5% for dental stream and lowest (46.2%) for medical school (P < 0.001), as shown in [Table 2].
|Table 2: Background knowledge, perceptions, and role of pharmacist in antimicrobial stewardship|
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Majority of the participants were able to appreciate the significance of the pharmacist's role in antimicrobial stewardship that includes education of other health-care professionals (79.2%), assembling and leading the core team of AMS (78.2%), work with therapeutic committees (75.1%), and promoting optimal use of antimicrobial agents (69.5%). However, 60.3% of the respondents considered that pharmacist was responsible for “over-the-counter (OTC)” dispensing of antimicrobial agents to the patients.
Antimicrobial stewardship goals, activities, and team members
Most (85.9%) agreed that the main goal of AMS is to reduce AMR. Additional objectives of AMS were also appreciated such as minimizing toxicity and other adverse effects (78.5%) and reducing the hospital stay (62.8%). Some respondents also selected incorrect options such as the increase in duration of therapy (50.3%), increase in use of broad-spectrum antibiotics (52.3%), and as such increase in antimicrobial use (51.3%) indicating poor level of understanding of AMS in entirety. The responses of the students of different health-care schools varied significantly. Almost three-fourth of the respondents were aware that AMS involves appropriate selection of antibiotics (73.6%), appropriate dosing and route of administration (78.2%), appropriate duration of therapy (74.6%), and study of antimicrobial effectiveness (70.8%). Statistically significant differences were found between responses of students of different health-care colleges (P < 0.05), as summarized in [Table 3].
|Table 3: Knowledge and perception on goals, objectives, and members of antimicrobial stewardship|
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The knowledge about the constitution of AMS team was fair, and a good number of respondents opined that clinical pharmacist (86.7%), infectious disease physicians (81.8%), and infection control staff (72.8%) are part of the AMS team. However, respondents also considered occupational therapist (76.4%) and hospital cleaning staff (67.7%) as AMS team members. Thus, awareness among different health-care students regarding AMS team members was found to differ significantly (P < 0.001), as mentioned in [Table 3].
Antimicrobial resistance and intervention
Among the factors contributing to AMR, the overuse of antimicrobials ranked as the highest (80.3%; P < 0.03), followed by broad-spectrum antimicrobial use when an alternative narrow-spectrum antibiotic is available (72.3%; P < 0.003). Further, some respondents considered that the AMR is prompted by poor medication adherence by patient (71.3%; P < 0.001) and poor handwashing practice (64.1%; P < 0.04). Responses from the different health-care colleges differed significantly in most cases, except in the case of the use of substandard quality of antimicrobials, as indicated by overall agreement by 68.2% of the respondents [Table 4].
|Table 4: Perceptions of health-care students about antimicrobial prescribing, resistance, and development strategies|
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Respondents show reasonable agreement in the matter of interventions that can possibly combat AMR that include strong knowledge and education of antimicrobial therapy (80.8%), appropriate use of antibiotics (79.7%), antimicrobial usage policies (78.5%), antimicrobial drug use guidelines needs to be developed (79.7%), and followed establishing national AMR surveillance (77.7%).
Most troublesome organisms
The overall students' responses regarding most troublesome bacteria in KSA with regard to contribution to development of AMR in decreasing sequence of importance are as follows: Enterococcus (70%), Pseudomonas aeruginosa (extended-spectrum beta-lactamases [ESBLs]) (68.7%), Salmonella enterica serovar Typhi (62.1%), methicillin-resistant Staphylococcus aureus (57.2%), β-lactamase (ESBL)-producing Klebsiella pneumoniae (52.8%), ESBL-producing Escherichia coli (51.3%), and Acinetobacter baumannii (49.0%), however, the responses of different health-care students differed significantly (P = 0.001), as shown in [Table 4].
Education on antimicrobial stewardship
[Table 5] displays the perception of different health-care students about the quality and adequacy of education they possess regarding AMS. Overall, only 191 (48.97%) had received a formal training on AMS, with the highest percentage from dentistry (77.3%). Clear majority of the respondents (79%) indicated that they would like to undergo more training and education on AMS as also suggested by the fact that majority of the respondents rated their knowledge on AMS, between average and poor.
|Table 5: Perceptions of health-care students for education on antimicrobial stewardship|
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| Discussion|| |
National AMS in Saudi Arabia optimizes the usage of antimicrobials for improvement of patient outcomes and prevention of AMR-related problems since the second half of 2014. Better understanding of AMS by health-care students could be considered as an indicator of its effectiveness in their future professional practices. In this context, the present study offers an insight into the existing state of awareness among final-year and internship students from different health-care colleges of Jazan University and indicates the scope of improvement in education and training needs. This study appears to be the first of its kind that ponders on various aspects of AMS such as knowledge, attitudes, and perceptions of health-care students of Jazan University regarding AMS and the level of their understanding.
The response rate of health-care students at Jazan University for this study was found to be relatively better than other similar studies in the South Africa region from June 2015 to August 2015, due to continued efforts over the study period. In this study, more than half of the respondents were familiar with AMS. In addition, the students of dental and general medicine were significantly more aware as compared to other health-care students. The awareness about AMS was reported 40% among US medical students, 71.9% in South African final-year pharmacy students, and 41% in Australian health-care professionals. The significant level of differences in the responses among the students of different health-care colleges of Jazan University can be attributed to the differences in requirements of curriculum of various health-care programs included in the study, and probably, the extracurricular efforts for AMS awareness made by individual schools were of different level.
Majority of the respondents believed that prescription practices and use of antimicrobials were appropriate which are in contrast with South African and Ethiopian studies. This can be attributed to a better level of training to the health-care team members or may conversely be due to the insufficient knowledge of respondent population to appreciate the problem. However, nearly three-fourth of the participants in our study concurred with the suggestion that implementation of AMS was essential in Jazan.
In this survey, the majority of the health-care workers were aware of pharmacist's role in AMS, but there was a misconception too that OTC distribution of antimicrobial is the responsibility of pharmacist. Nevertheless, it is against the law to dispense antibiotics without prescription. The present study revealed that more clarity existed among dental, microbiology, and pharmacy students regarding the role of pharmacist compared to general medicine and nursing students. Majority of the participants felt that a pharmacist can have an important role in promoting awareness about adequate use of antibiotics and in prevention of AMR. This provides an insight to the attitude of other health-care professionals that they rely on pharmacists' contribution to curb the menace of AMR. Rizvi et al. also reported that pharmacist in Tasmania perceived that inappropriate use of antibiotics can be reduced by implementing AMS. Surprisingly, awareness about components of AMS, namely selection of appropriate antibiotics, properly monitored dosing, correct route of administration, appropriate duration of therapy, and education about antibiotic usage, was higher among nonmedical respondents. On the other hand, a lot of inconsistency was observed regarding understanding of AMS and its team members. This may be because AMS is not a curricular component of health-care program and the awareness merely dependents on subjective efforts.
As per guidelines, core members of AMS team are infectious diseases physician (leader), clinical pharmacist having training in infectious diseases (coordinator), clinical microbiologist, an information system specialist, an infection control professional, and hospital epidemiologist. Majority of the dental and microbiology participants of the survey had appropriate knowledge about composition of the core team of AMS as compared to nursing, pharmacy, and general medicine students. Further, few unfortunate misconceptions existed among few students of all health-care colleges such as occupational therapist, and hospital cleaning staff are also AMS team members.
The universal prevalence of AMR is a serious issue,,, and the major causes surfaced in our study include extensive antimicrobial overuse, poor patient adherence to schedule, duration of prescribed antimicrobials, and use of broad-spectrum antimicrobials even when narrow spectrum is available as a better choice. The studies of this kind conducted in Australia, Ethiopia, France, Scotland, South Africa, Spain, and Saudi Arabia suggest that principal reasons for development of AMR are availability of numerous broad-spectrum antimicrobials, increasing number of prescriptions with antibiotics, and improper duration of therapy.,,,, Dental, microbiology, and pharmacy students were found more aware about causes of AMR.
Strong knowledge of antimicrobials, development of institutional guidelines, and policies followed by education on antimicrobial therapy and establishment of national AMR surveillance can possibly help to combat ever-increasing incidences of AMR. Majority of the nursing, pharmacy, and general medicine students were aware of the most troublesome microorganisms and were able to appreciate the relative significance of different pathogens contributing to AMR.
The responses from different health-care students regarding adequacy of education and training on AMS during their course varied significantly. More percentage of dental and microbiology students had received some sort of training on AMS. The respondents in vast majority perceived a need for including AMS in curriculum. A willingness to receive more education on AMS was also reported in similar studies on students of a US medical school and students of pharmacy in South Africa.
The studies from Saudi Arabia, and survey from GCC states, those which have implemented AMS, reported a significant impact on the reduction in use of broad-spectrum antibiotics, antibiotic utilization, hospital-acquired and associated infections, length of stay or mortality metrics, inappropriate prescribing, AMR, and direct antibiotic cost. These findings suggest a promising opportunity to enhance the efficiency of existing AMS implementation through sharing of best practices and supporting the development of region-specific guidelines for better awareness across Saudi Arabia. On the other hand, the self-assessment of knowledge on AMS among different undergraduate health-care participants revealed that the level of knowledge they possessed was average to poor, which establishes a need to stipulate uniform AMS training during undergraduate or internship level in order to meet AMS goals in Saudi Arabia.
Limitations and strength
The scope of the present study was restricted to views of only final-year health-care students enrolled at Jazan University. Further, recruitment being voluntary in nature, only self-motivated students participated that might have contributed to possible bias. The response rate was low, especially among dental and medical students; therefore, the views, opinions, and responses may not be generalized. The demographic information of target population of students could not be collected to test for bias between responders and nonresponders, and as such, the investigators could not figure out whether there were any important differences between them. The study did not include any detail regarding contents of the study curriculum that relates to antimicrobial therapy, and it is difficult to correlate the awareness on AMS to the curricular requirements of each specialization. In contrast, a few specific strengths of the study include that target population from a diverse group of health-care specializations gives an opportunity to understand the extent of appreciation of others' contribution to AMS for a better coordination before they join duties as a professional in their respective fields. As such, this is the first study in Saudi Arabia that attempts to assess knowledge and perceptions among health-care students about AMS across different specializations.
| Conclusions|| |
The outcomes of the present study indicate that the future professionals of different health-care disciplines have a considerable understanding and theoretical knowledge on concept of AMR and cautious use of antimicrobials, but they lack awareness about current practices and the guidelines regarding AMS. This underlines the requirement for a coordinated effort to provide for structured education about AMS with nutshell information to achieve goals of improving antimicrobial use and checking the fierce spread of AMR. Significant differences in the responses regarding certain aspects of AMS warrant for a uniform training to be designed and conducted across the health-care programs to appraise them about each other's role and responsibility, so that they can work as a team for effective implementation of the AMS.
The authors are thankful to Majdah AG, Wejdan OH, Zinab AS, Mariam MAB, Njood SA, Jana AO, and Mariam MA, the Pharm D internship students, College of Pharmacy, Jazan University, for their assistance in fieldwork for collecting data. The authors would like to acknowledge all the health-care students who participated in the survey. The authors also like to thank colleges of pharmacy, medicine, dental, nursing, and microbiology, Jazan University, for their cooperation and unbiased volunteering in this survey.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Laxminarayan R, Matsoso P, Pant S, Brower C, Røttingen JA, Klugman K, et al
. Access to effective antimicrobials: A worldwide challenge. Lancet 2016;387:168-75.
Shallcross LJ, Howard SJ, Fowler T, Davies SC. Tackling the threat of antimicrobial resistance: From policy to sustainable action. Philos Trans R Soc Lond B Biol Sci 2015;370:20140082.
Morgan DJ, Okeke IN, Laxminarayan R, Perencevich EN, Weisenberg S. Non-prescription antimicrobial use worldwide: A systematic review. Lancet Infect Dis 2011;11:692-701.
Aly M, Balkhy HH. The prevalence of antimicrobial resistance in clinical isolates from Gulf Corporation Council countries. Antimicrob Resist Infect Control 2012;1:26.
Al Rasheed A, Yagoub U, Alkhashan H, Abdelhay O, Alawwad A, Al Aboud A, et al
. Prevalence and predictors of self-medication with antibiotics in Al Wazarat Health Center, Riyadh City, KSA. Biomed Res Int 2016;2016:1-8.
Nasr Z, Paravattil B, Wilby KJ. The impact of antimicrobial stewardship strategies on antibiotic appropriateness and prescribing behaviours in selected countries in the Middle East: A systematic review. East Mediterr Health J 2017;23:430-40.
Fridkin SK, Baggs J, Fagan R, Magill S, Pollack LA, Malpiedi P, et al
. Vital signs: Improving antibiotic use among hospitalized patients. Cent Dis Cont Prev MMWR 2014;63:194-200.
Pogorzelska-Maziarz M, Herzig CT, Larson EL, Furuya EY, Perencevich EN, Stone PW. Implementation of antimicrobial stewardship policies in U.S. hospitals: Findings from a national survey. Infect Control Hosp Epidemiol 2015;36:261-4.
Howard P, Pulcini C, Levy HG, West RM, Gould IM, Harbarth S, et al
. An international cross-sectional survey of antimicrobial stewardship programs in hospitals. J Antimicrob Chemother 2015;70:1245-55.
Trivedi KK, Dumartin C, Gilchrist M, Wade P, Howard P. Identifying best practices across three countries: Hospital antimicrobial stewardship in the United Kingdom, France, and the United States. Clin Infect Dis 2014;59 Suppl 3:S170-8.
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.
Center for Disease Control and Prevention. CDC's campaign to prevent antimicrobial resistance in health-care settings. Morb Mortal Wkly Rep 2002;51:343.
Goff DA, Rybak MJ. Global antimicrobial stewardship: Challenges and successes from Frontline Stewards. Infect Dis Ther 2015;4:1-3.
Drew RH. Antimicrobial stewardship programs: How to start and steer a successful program. J Manag Care Pharm 2009;15:S18-23.
Alomi YA. National antimicrobial stewardship program in Saudi Arabia: Experiences and future vision. 3rd
International Conference on Clinical Pharmacy. Clin Pharmacol Biopharm 2015:4:49.
Alomi YA. National antimicrobial stewardship program in Saudi Arabia; initiative and the future. Open Access J Surg 2017;4:1-7.
Alawi MM, Darwesh BM. A stepwise introduction of a successful antimicrobial stewardship program. Experience from a tertiary care university hospital in Western, Saudi Arabia. Saudi Med J 2016;37:1350-8.
Vickers H. International antibiotic resistance crisis. Better training needed to maintain therapeutic arsenal. Student BMJ 2011;342.
Danial WW. Biostatics: A Foundation for Analysis in the Health Sciences. 7th
ed. New York: John Wiley & Sons; 1999.
Abbo LM, Cosgrove SE, Pottinger PS, Pereyra M, Sinkowitz-Cochran R, Srinivasan A, et al
. Medical students' perceptions and knowledge about antimicrobial stewardship: How are we educating our future prescribers? Clin Infect Dis 2013;57:631-8.
Burger M, Fouriea J, Lootsa D, Mnisia T, Schellacka N, Bezuidenhouta S, et al
. Knowledge and perceptions of antimicrobial stewardship concepts among final year pharmacy students in pharmacy schools across South Africa. South Afr J Infect Dis 2016;31:84-90.
Cotta MO, Robertson MS, Tacey M, Marshall C, Thursky KA, Liew D, et al
. Attitudes towards antimicrobial stewardship: Results from a large private hospital in Australia. Healthc Infect 2014;19:89-94.
Abera B, Kibret M, Mulu W. Knowledge and beliefs on antimicrobial resistance among physicians and nurses in hospitals in Amhara Region, Ethiopia. BMC Pharmacol Toxicol 2014;15:26.
Al-Jedai A, Qaisi S, Al-Meman A. Pharmacy practice and the health care system in Saudi Arabia. Can J Hosp Pharm 2016;69:231-7.
Rizvi T, Thompson A, Williams M, Zaidi ST. Perceptions and current practices of community pharmacists regarding antimicrobial stewardship in Tasmania. Int J Clin Pharm 2018;40:1380-7.
Alghadeer S, Aljuaydi K, Babelghaith S, Alhammad A, Alarifi MN. Self-medication with antibiotics in Saudi Arabia. Saudi Pharm J 2018;26:719-24.
Navarro-San Francisco C, Del Toro MD, Cobo J, De Gea-García JH, Vañó-Galván S, Moreno-Ramos F, et al
. Knowledge and perceptions of junior and senior Spanish resident doctors about antibiotic use and resistance: Results of a multicenter survey. Enferm Infecc Microbiol Clin 2013;31:199-204.
Pulcini C, Williams F, Molinari N, Davey P, Nathwani D. Junior doctors' knowledge and perceptions of antibiotic resistance and prescribing: A survey in France and Scotland. Clin Microbiol Infect 2011;17:80-7.
Minen MT, Duquaine D, Marx MA, Weiss D. A survey of knowledge, attitudes, and beliefs of medical students concerning antimicrobial use and resistance. Microb Drug Resist 2010;16:285-9.
Amer MR, Akhras NS, Mahmood WA, Al-Jazairi AS. Antimicrobial stewardship program implementation in a medical intensive care unit at a tertiary care hospital in Saudi Arabia. Ann Saudi Med 2013;33:547-54.
Al Awdah L, AlShahrani D, AlShehri M, AlFawaz T, ElSidig N, AlAwfi A. Antimicrobial stewardship program in a pediatric intensive care unit of a tertiary care children's hospital in Saudi Arabia – A pilot study. Antimicrob Resist Infect Control 2015;4:173.
Enani MA. The antimicrobial stewardship program in Gulf Cooperation Council (GCC) states: Insights from a regional survey. J Infect Prev 2016;17:16-20.
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]