Int J Clin Pharm DOI 10.1007/s11096-014-9960-7
RESEARCH ARTICLE
A qualitative study of pharmacists’ perceptions of, and recommendations for improvement of antibiotic use in Qatar Emily Black • Andrea Cartwright • Sumaia Bakharaiba Eman Al-Mekaty • Dima Alsahan
•
Received: 2 December 2013 / Accepted: 19 May 2014 Koninklijke Nederlandse Maatschappij ter bevordering der Pharmacie 2014
Abstract Background Use of antibiotics has been correlated with increasing rates of resistance. Pharmacists are ideally positioned as front line health care providers to limit indiscriminate antibiotic use and promote the safe and effective administration of these medications. Objective The aim of this project was to assess pharmacists’ opinions relating to antibiotic utilization in the community setting. Setting Doha, Qatar. Method Community and primary care pharmacists were invited to participate in one of three focus groups or a semi-structured interview at Qatar University or at their site of employment. A total of 22 community and primary care pharmacists participated in this study. Interviews were facilitated using a focus group guide, were recorded, and later transcribed. Transcripts were reviewed for recurring themes and coded using Nvivo software for qualitative research. Main outcome measure Pharmacists’ perceptions. Results Five major themes emerged from a series of focus groups and interviews. Themes which recurred across interview groups included: misconceptions and inappropriate practices by patients and healthcare providers, currently implemented strategies, perceived barriers, ways to overcome perceived barriers, and targets for improvement of antibiotic use in Qatar. The greatest need, as identified by pharmacists in this study was increased knowledge of the general population about appropriate antibiotic use through various educational interventions. Conclusion Pharmacists report a number of E. Black (&) S. Bakharaiba E. Al-Mekaty D. Alsahan College of Pharmacy, Qatar University, PO Box 2713, Doha, Qatar e-mail: [email protected] A. Cartwright Pharmacy Department, Sidra Medical and Research Center, PO Box 26999, Doha, Qatar
misconceptions and inappropriate practices relating to antibiotic use in Qatar by patients and healthcare providers. Education to improve knowledge of appropriate antibiotic use is needed. Despite recognition of these issues, barriers are preventing pharmacists from implementing strategies to improve antibiotic use in Qatar. Keywords Antibiotics Community pharmacy General public Pharmacist Pharmacist opinion Qatar
Impact of research findings • •
•
A lack of knowledge by the general population contributes to inappropriate antibiotic use Pharmacists perceive that patient demand is one of the greatest barriers to improving antibiotic utilization by community pharmacists Educational interventions by community pharmacists and other healthcare providers using a variety of formats are needed to improve knowledge of the general population
Introduction Antimicrobial resistance is increasing at an alarming rate worldwide [1–5] and there is evidence to suggest that as a consequence patients are failing first line antibiotic therapies [6]. Additionally, patients are requiring longer and more expensive treatment courses, and most notably, these drug resistant infections are putting patients at an increased risk of death [3, 6, 7]. The development of antibiotic resistance is a natural phenomenon resulting from the exposure of microorganisms
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to antibacterial agents that can be accelerated by the widespread use of antibiotics [8]. While the advent of antimicrobials has significantly decreased morbidity and mortality associated with many infectious diseases, indiscriminant use threatens to increase the risk of death from previously curable infections [9]. Although rates of antimicrobial resistance are increasing [1], few novel antibiotics are currently being developed. This has resulted in concern from the global medical community about a return to the ‘‘pre-antibiotic’’ infectious disease era [10]. The inappropriate use of antibiotic drug therapy has been identified by the World Health Organization as a risk factor for antimicrobial resistance [8]. An increase in antibiotic consumption has been correlated with development of resistance [11–13]. Costelloe et al. [11] found a significant association between any antibiotic use in individual patients and subsequent antibiotic resistance within the following 12 months. The prevalent use of fluoroquinolones has also been shown to be associated with increased rates of fluoroquinolone resistant Escherichia coli [12]. Additionally, longer duration and multiple courses of antibiotics were also associated with higher rates of resistance [11]. Given the positive association between antibiotic consumption and resistance rates, it is not surprising that decreasing antibiotic usage can result in a corresponding decrease in the incidence of antibiotic resistant pathogens. In Finland, a reduction in the use of macrolide antibiotics was followed by a significant decrease in group A streptococcus erythromycin resistance rates from 16.5 to 8.6 % over a 4 year period [14]. In another study, Hicks et al. [15] found that higher rates of outpatient antibiotic prescribing was associated with a greater proportion of non-susceptible invasive pneumococcal disease isolates as compared to areas with lower prescribing rates. Antibiotics are commonly prescribed to community dwelling patients. In a survey by Al-Niemat et al. [16] over 35 % of prescribed medications from an outpatient clinic were for antibiotics. A similar rate of prescribing was found in a survey of antibiotic consumption in a community setting in New Delhi, with 43 % of patients visiting a private clinic being prescribed at least one antibiotic [17]. Given this high rate of antibiotic use in the community setting, improving the judicious use of antibiotics in this population may have a significant impact on altering antibiotic resistance rates. Due to a high volume of antibiotic prescribing in the community setting, pharmacists may be ideally positioned as front line health care providers to limit indiscriminate antibiotic use and promote the safe and effective administration of these medications. In Qatar, patients receive medications from private community pharmacies, dispensaries affiliated with
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primary care clinics, and outpatient dispensaries in hospitals. Currently, regulations require a prescription prior to dispensing antimicrobial agents in Qatar. Beyond fulfilling legal requirements, it is unknown what, if any strategies have been implemented to improve antibiotic use in the community and no study has evaluated pharmacists’ perception of potential areas for improvement in antibiotic utilization. In order to implement effective strategies, specific targets for improving antibiotic use must be identified.
Aim of the study The aim of this project was to assess pharmacists’ opinions about antibiotic utilization in the community practice setting.
Ethical approval This study was reviewed and received research ethics exemption by the Qatar University Institutional Review board (QU-IRB 155-E/12).
Methods Study design A series of three focus groups and two small group interviews with a total of 22 participants were completed by study investigators in order to determine suggested strategies for improving antibiotic use in the community. A qualitative study design was chosen to explore rationale for limited implemented services, perceived barriers to implementing services, and to determine pharmacists’ perceptions of patient and healthcare provider educational needs in Qatar. Focus groups were defined as group discussions consisting of 4–10 participants facilitated by a study investigator. For invited participants who were not able to attend scheduled focus groups, alternative dates for individual or small group (2–3 participants) interviews were offered. Participants Community and primary care pharmacists were recruited to participate in one of three focus groups or, had the option to complete an individual or small group interview at their convenience. All community pharmacists and primary care pharmacists were invited to participate through email invitations send through the Qatar
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University continuing professional development database. To identify pharmacists who may not have received the email invitations, pharmacists attending continuing professional development events at the university received a written invitation. In addition, managers of several community pharmacy chains were asked to notify their pharmacists of the project. Any community or primary care pharmacists who spoke English and were currently practicing in Qatar were eligible to participate. Community pharmacists in Qatar practice in privately owned retail pharmacies while primary care pharmacists work in dispensaries or clinics attached to a healthcare center. Pharmacists who had previously practiced in Qatar as a community pharmacist and those who had completed at least 2 months of structured practical experiential training as pharmacy students in a community pharmacy setting in Qatar were also included in this study. To ensure participants were willing to openly discuss experiences, pharmacists were grouped to a focus group or interview based on their specific practice environment (community, primary care, or former students who had completed at least 2 months of structured practical experiential training). Three focus groups consisting of 4, 5, and 8 participants respectively, and two small group interviews consisting of 2 and 3 participants respectively took place. Pharmacists who had not practiced in a community or primary care setting in Qatar were excluded.
Table 1 Focus group and interview guide Community pharmacist focus group and interview questions 1. In your practice, what are the most common types of infectious diseases you encounter? 2. What are some common misconceptions or inappropriate practices patients may have relating to treatment of infections or appropriate antibiotic use? 3. Which strategies should be considered highest priority to resolve from the perspective of healthcare providers? 4. What are some actions you currently use to improve antibiotic use in your area of practice? 5. In your opinion, what are some services community pharmacists could offer to improve appropriate use of antibiotics by the general population in the community? 6. Do you feel community pharmacists need additional training to implement suggested strategies? 7. What are some barriers to implementing interventions you have suggested to improve antibiotic use at your practice site? 8. What are some strategies to overcome barriers which would allow community pharmacists to provide services relating to improving antibiotic use at your practice site? 9. Is there anything else you would like to say about improving antibiotic use in the community through pharmacist lead interventions?
the participants’ place of employment in Doha, Qatar. The duration of focus groups and interviews ranged from 45 to 90 min. Each focus group or interview was audio-recorded to allow for transcription after the session took place.
Data collection Analysis All focus groups and interviews were facilitated by a member of the research team (EB). Other research team members (undergraduate and graduate pharmacy students) assisted to take notes when academic schedules would allow. Notes were used as a backup in the event that the recorder failed and to document facial expressions and emotions of participants. Sessions were facilitated using an interview guide consisting of nine open-ended questions. Questions were developed by study investigators based on objectives of this study and two previously completed surveys of the general population’s knowledge of appropriate antibiotic use in Qatar and pharmacists’ perceptions of currently implemented antimicrobial stewardship activities and barriers to implementation of services in Qatar. Every discussion began with an engagement question followed by a series of exploratory questions and ended with an exit question. Questions included in the interview guide are outlined in Table 1. Focus groups and interviews took place until no new ideas were generated. The saturation point was met after completing three focus groups and two small group interviews. Sessions were conducted at Qatar University or at
Data were analyzed using the Framework method as described by Gale et al. [18] with assistance of Nvivo software for qualitative research. Themes were identified inductively from the data as described by Patton in ‘‘Qualitative Research and Evaluation Methods’’. Inductive analysis should permit patterns to emerge as data is collected rather than defining specific research hypotheses prior to performing interviews [19]. While focus groups and interviews were completed with an interview guide, investigators began analysis during data collection with research team members listening for themes and prompting participants to elaborate outside the interview guide (if relevant) during the course of the discussions. To ensure an inductive approach was used, open-ended questions were asked allowing participants to determine the direction of the discussion. After each focus group or interview, the research team members present during the discussions met to review specific observations. Emerging patterns were also identified. Transcription of recorded discussions took place shortly after the focus group session by members of the
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A total of 22 pharmacists from community and primary care settings participated. The majority of pharmacists were female (72.7 %) and practiced in the primary care setting (59.1 %). Baseline characteristics of pharmacists are outlined in Table 2. Five major themes relating to antibiotic use were identified throughout interview sessions and are discussed below. Themes included: misconceptions and inappropriate practices, implemented strategies, perceived barriers, ways to overcome perceived barriers, and targets for improvement of antibiotic use in Qatar. All interview questions were addressed and coded under the above themes with the exception of the question ‘‘Which strategies should be considered highest priority to resolve from the perspective of healthcare providers’’. When asked this question, pharmacists quickly shifted to discussing barriers limiting implementation of strategies.
self-limiting illnesses. Non-compliance with prescribed directions was also reported by most groups. Pharmacistreported rationale for patient non-compliance included discontinuation of antibiotics prematurely due to resolution of symptoms and use of higher doses of antibiotics with the perception that the patient would get better faster. One participant highlighted that ‘‘when they have a prescription, they will just ask for half of it when the doctor has prescribed a week of the prescription but they will just take half of it and say I am fine in 2 or 3 days (Interviewee 1, Community Pharmacist)’’. Participants also reported the general population had a lack of awareness relating to development of resistance, adverse effects of antibiotics, and antibiotic allergies. Inappropriate practices by healthcare providers were also identified. Pharmacists practicing in community-based settings reported that antibiotics are being dispensed over the counter in some community pharmacies despite laws requiring a prescription to dispense. One participant indicated, ‘‘if the patient or customer is a friend of the pharmacist, he give them antibiotic but it is a prescribed medicine (Interviewee 4, Community Pharmacist)’’. Pharmacists from primary care settings felt this was less of a concern due to internal policies which reinforced national dispensing laws and regulations. Some participants also reported a lack of patient counseling by pharmacists and limited interdisciplinary communication between pharmacists and physicians. Both community and primary care pharmacists reported suboptimal prescribing resulting in overuse of antibiotics for self-limiting illnesses, broad-spectrum antibiotic selection, and lack of patient assessment by physicians. One participant stated ‘‘Cephalosporin for example, the third generation cephalosporins. I used to get this prescription from one doctor. Different patients but the same prescription (Interviewee 2, Community Pharmacist)’’. Another participant commented, ‘‘From the doctor himself, he doesn’t follow the procedures of prescribing an antibiotic. Some manufacturers will go for him and ask him to write this antibiotic and he will get a journey to some Middle East or some gift like that (Interviewee 4, Community Pharmacist)’’.
Misconceptions and inappropriate practices
Current strategies to improve antibiotic use
Participants reported a wide range of misconceptions and inappropriate practices with regards to antibiotic use by the general population in Qatar. All groups indicated that the general population had a low level of knowledge relating to the appropriate use of antibiotics. The majority of participants discussed frequent desire of patients to use antibiotics when not indicated, and the occasional use of antibiotics when not prescribed to treat viral and other
Most groups identified few ongoing strategies to promote appropriate antibiotic use in community and primary care settings. Where strategies exist, the most commonly reported initiative was patient education in the form of patient counseling at the time of dispensing. One respondent commented, ‘‘if there is a side effect, pharmacists are highlighting side effects from this antibiotic’’ (Interviewee 20, Primary Care). Primary care pharmacists reported internal
Table 2 Baseline characteristics (N = 22) Characteristics
N (%)
Female
16 (72.7)
Primary area of practice Community pharmacy
4 (18.2)
Primary care pharmacy
13 (59.1)
Former practice in a community pharmacy Pharmacists completing entry-to-practice degree and experiential training in Qatar
5 (22.7) 4 (18.2)
research team. Transcripts were recorded verbatim. Transcriptions were then reviewed and an initial codebook was constructed by the research team based on emerging patterns. Using the codebook, two of more study investigators independently coded transcripts for recurring themes using nodes in Nvivo. After initial coding, themes were then reviewed for similarity and grouped together. Subthemes were identified and coded as child nodes in Nvivo. Consensus was achieved through face-to-face discussions with the research team.
Results
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antibiotic guidelines were available; however, groups acknowledged limited implementation in routine patient care. A small number of pharmacists reported interacting with physicians when drug related problems such as prescribing of duplicate therapy arose. While current strategies to improve antibiotic use were briefly outlined in all groups, pharmacists quickly shifted to lengthy discussions about ongoing barriers to improving antibiotic use. Barriers to improving antibiotic use All groups extensively discussed current barriers to improving antibiotic use in the community and primary care settings. Many participants highlighted that the number of barriers was overwhelming and before interventions could be developed, pharmacists must work collaboratively with government regulatory authorities, the College of Pharmacy at Qatar University, and other healthcare providers to overcome these barriers. Primary subthemes that emerged during discussion of barriers included: patient demand, low level of knowledge by healthcare providers, poor perception of pharmacists, and business model of community pharmacy practice. One of the most common barriers to improving antibiotic use in both the community and primary care settings was patient demand to prescribe and dispense antibiotics. One pharmacist stated ‘‘but what is the use? From the doctor itself, the patient ask them, I want you to write me this. They know what they want. They are dictating (Interviewee 1, Community Pharmacist)’’. Another pharmacist highlighted burden on pharmacists through the statement ‘‘sometimes the pharmacist refuse to give them antibiotic but they wait in the pharmacy and argue to get the antibiotic (Interviewee 4, Community Pharmacist)’’. Another common barrier was level of healthcare provider knowledge. Participants primarily focused on level of knowledge of pharmacists. During discussions about the level of knowledge of the pharmacist, one participant reported, ‘‘we are not aware anymore what’s the latest medicines, vaccines, and antibiotics, and the side effects (Interviewee 3, Community Pharmacist)’’. In addition to improvement in the level of knowledge regarding pharmacotherapy, participants also highlighted the need to improve critical appraisal and communication skills as evident by the statement ‘‘how to discuss evidence based practice, the communication skills, these all need to be the training for the pharmacist (Interviewee 8, Former Student)’’. Furthermore, participants reported poor perception of pharmacists by the public and healthcare providers. Referring to the perception of the general population, one participant reported, ‘‘they think the pharmacist is only a store keeper in a grocery shop (Interviewee 5, Community Pharmacist)’’. Another pharmacist stated, ‘‘the perception,
Table 3 Perceived barriers to improving antibiotic use and suggestions to overcome barriers of interviewed pharmacists (N = 22) Barrier
Suggestion
Patient demand
Patient education Development and enforcement of laws and regulations pertaining to prescribing and dispensing of antibiotics
Knowledge of healthcare providers
Mandatory continuing professional development Development of specialty training programs for pharmacists
Poor perception of pharmacists
Education about the role of the pharmacist
Time
Increase staffing in pharmacies
Develop a pharmacist society Allow pharmacists to read educational materials during working hours Business model of pharmacy practice
Development and enforcement of laws and regulations pertaining to dispensing of medications
Lack of resources
Provision of internet access and up-to-date resources
Lack of clear laws and regulations guiding prescribing and dispensing of medications
Development and enforcement of laws and regulations pertaining to prescribing and dispensing of medications in Qatar
Lack of motivation
Provide monetary incentives for pharmacists
Communication
None suggested
even from our families they [pharmacists] are educated sellers (interviewee 8, Former Student)’’. Poor perception by physicians was also perceived as outlined by the statement ‘‘Sometimes the doctors, they don’t approve of the intervention (Interviewee 11, Primary Care Pharmacist)’’. Furthermore, the most lengthy discussions regarding barriers experienced by community pharmacists related to the current business model of community pharmacy practice and lack of comprehensive laws and regulations relating to prescribing and dispensing of medications. Participants highlighted that individuals without a pharmacy degree typically own community pharmacies. Concern was raised with respect to an emphasis on sales as opposed to provision of patient care. Dissatisfaction with the current business model of community pharmacy practice was summarized in the statement ‘‘So the owner is thinking for the business and getting more money and the pharmacist is under pressure to sell and to get more profit (Interviewee 5, Community Pharmacist)’’. Pharmacists practicing in primary care clinics did not report these concerns as the dispensary is owned and operated by
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primary health care centers. All perceived barriers reported by focus group participants are outlined in Table 2. Ways to overcome barriers Pharmacists recommended a number of strategies to overcome the discussed barriers, which would enable pharmacists and other health care providers to improve antibiotic use in the community setting. All groups extensively discussed the need for education of patients and health care providers through various means. One participant highlighted ‘‘Education for doctor, education for patient, education for pharmacists (Interviewee 15, Primary Care Pharmacist)’’. While less of a concern for primary care pharmacists, updating and enforcing laws and regulations pertaining to prescribing and dispensing of medications was a common suggestion across groups who practiced in community pharmacy settings. One participant stated ‘‘I think for myself, I don’t even know the Qatari laws (Interviewee 7, Former Student)’’. Another pharmacists referring to practice in community settings in Qatar commented ‘‘I want to implement a protocol. A very strong protocol for the community pharmacy. A strategy, how to dispense the antibiotic and under which circumstances you can dispense an antibiotic (Interviewee 5, Community Pharmacist)’’. Other strategies to overcome identified barriers are outlined in Table 3. Targets for improvement Despite a wide range of listed barriers and suggestions for improvement, all groups discussed the need to improve the knowledge of the general population about appropriate antibiotic use. Pharmacists felt the general population should be educated through various means including education in the media, awareness campaigns at public venues, as well as routine counseling and education in community and primary care pharmacies. Other suggested targets to improve antibiotic use included interdisciplinary communication between healthcare providers as highlighted by one pharmacists who indicated ‘‘communication and intervention is very important between the pharmacists and the doctors (Interviewee 10, Primary Care Pharmacist)’’, development of clinical practice guidelines based on local patterns of resistance, and further practice-based research to assess the success of implemented strategies.
Discussion This is the first qualitative study to evaluate community pharmacist perceptions of antibiotic use in Qatar. Pharmacists participating in this study suggested ongoing need
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for improvement in prescribing and dispensing by healthcare providers in addition to increased awareness of appropriate antibiotic utilization by patients. While pharmacists recognize these issues, barriers are preventing implementation of interventions to improve antibiotic utilization. Pharmacists participating in this study perceived that a lack of knowledge by patients resulted in inappropriate use of antibiotics. A lack of knowledge and resultant misuse of antibiotics has been documented internationally [20–22]. A low level of antibiotic knowledge consequently has been shown to correlate with non-adherence [20]. Multiple educational interventions targeted at patients and healthcare providers to improve overall knowledge and use of antibiotics have been recommended by study participants in Qatar and is consistent with those previously recommended in the literature [23–25]. Pharmacists working in community practice settings are the most accessible healthcare providers and are ideally positioned to provide educational interventions [26]. A survey by El-Hajj and Colleagues completed with the general population in Qatar demonstrated that 52 % of respondents visit a community pharmacy monthly. Despite frequent visits to community pharmacies, 50 % of respondents reported physicians as their first contact to answer drug related questions [27]. In a systematic review of community pharmacist involvement in health promotion, mixed findings from general population on pharmacist participation were reported. For those who experienced health promotion interventions by pharmacist, the overall perception was positive. The authors concluded that with increased exposure to health promotion activities, attitudes towards pharmacists participation in health promotion activities by the general population would improve. The authors suggested pharmacists needed to be more proactive in offering services and may need additional training to increase confidence in order to change attitudes [28]. Similarly, our findings indicate limited ongoing education and health promotion activities by community pharmacists. Despite these findings, pharmacists believe they can play an important role in public health promotion by educating the public about appropriate antibiotic use in Qatar. In order to increase utilization of community and primary care pharmacists in health promotion, barriers should be overcome. Currently, several barriers are preventing pharmacists from providing services to improve antibiotic utilization. Concerns outlined by community pharmacists in Qatar have been echoed by pharmacists internationally [25, 29, 30]. A qualitative study completed in India identified inappropriate prescribing and dispensing as an area of concern and notably, patient demand was thought to be a major contributing factor [25]. Roque et al. [29] also reported patient demand on pharmacists to dispense and
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physicians to prescribe antibiotics. Pharmacists in Portugal have identified that patient self-medication with leftovers from previous treatments, non-compliance with prescribed dosages, suboptimal prescribing by physicians, and use of antibiotics in animals for human consumption are major factors contributing to development of resistance in their country [29]. In addition, an American study reported time constraints, fear of harming relations with physicians, and lack of educational material as barriers to engaging in antibiotic campaigns [30]. Finally, a study completed in the United Kingdom reported poor perception of the pharmacist’s competencies by the general population and other health care providers as a significant obstacle to pharmacists providing public health services [31]. Local inappropriate practices and barriers to improving antibiotic use must be considered during the process of developing a health promotion strategy. Interventions to improve knowledge of the general population and health care providers are needed in Qatar. Currently, no pharmacist associations or societies in the country exist. All medical and healthcare provider licensing and regulation is overseen by the national Supreme Council of Health who are responsible for quality and effectiveness of services delivered in private and public sectors of healthcare [32]. Development of a professional pharmacist’s society may assist in supporting an expanded scope of practice for pharmacists and improving the general population’s perception of community pharmacists. In addition, clarity and enforcement of laws and regulations pertaining to prescribing and dispensing of antibiotics is needed. Our findings provide valuable insight pharmacists’ perceptions of antibiotic use and strategies for improvement in Qatar; however, in considering results, a number of limitations should be noted. While perceptions of pharmacists participating in the interviews and focus groups were consistent, our findings represent input from a small sample of community and primary care pharmacists in Qatar. The exact number of pharmacists in Qatar is unknown; however it is estimated from our continuing professional development database that 1,000 pharmacists work in community, primary care, academic, or hospital settings. In addition, interview sessions were completed in English while the majority of participants spoke English as a second language, which may have resulted in misunderstanding of interview guide questions. To overcome this barrier, the facilitator rephrased questions when concern arose. The facilitator of the focus groups was a pharmacist, which may have impacted responses and contributed to social desirability however; we believe this bias has been minimized as the facilitator refrained from sharing their own perceptions. In addition, the facilitator was a faculty member who did not work in community practice. Furthermore, due to an extension in timeline of
the research project, collaborators assisting in data collection during the final two focus groups were not available to assist in note taking due to other commitments. To overcome this barrier, all sessions were recorded and at least two collaborators reviewed transcripts. Finally, results from this study represent perceptions of community and primary care pharmacists in Qatar and cannot be generalized to pharmacists practicing in other countries or in the inpatient setting.
Conclusion Community and primary care pharmacists recognize a lack of knowledge and inappropriate practices relating to antibiotic use by the general population and healthcare providers in Qatar. Barriers are limiting ongoing initiatives to promote judicious use of antibiotics. Interventions targeting the general population, health care providers, and regulatory authorities are needed to combat indiscriminant use of antibiotics and development of resistance. Acknowledgments The authors of this manuscript would like to thank the Qatar Petroleum Health and Wellness Center pharmacy department for their contributions to this project. Funding This study was completed with funding from an Internal Student Grant from Qatar University. Conflicts of interest The authors of this paper report no conflicts of interest.
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RESEARCH ARTICLE
A qualitative study of pharmacists’ perceptions of, and recommendations for improvement of antibiotic use in Qatar Emily Black • Andrea Cartwright • Sumaia Bakharaiba Eman Al-Mekaty • Dima Alsahan
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Received: 2 December 2013 / Accepted: 19 May 2014 Koninklijke Nederlandse Maatschappij ter bevordering der Pharmacie 2014
Abstract Background Use of antibiotics has been correlated with increasing rates of resistance. Pharmacists are ideally positioned as front line health care providers to limit indiscriminate antibiotic use and promote the safe and effective administration of these medications. Objective The aim of this project was to assess pharmacists’ opinions relating to antibiotic utilization in the community setting. Setting Doha, Qatar. Method Community and primary care pharmacists were invited to participate in one of three focus groups or a semi-structured interview at Qatar University or at their site of employment. A total of 22 community and primary care pharmacists participated in this study. Interviews were facilitated using a focus group guide, were recorded, and later transcribed. Transcripts were reviewed for recurring themes and coded using Nvivo software for qualitative research. Main outcome measure Pharmacists’ perceptions. Results Five major themes emerged from a series of focus groups and interviews. Themes which recurred across interview groups included: misconceptions and inappropriate practices by patients and healthcare providers, currently implemented strategies, perceived barriers, ways to overcome perceived barriers, and targets for improvement of antibiotic use in Qatar. The greatest need, as identified by pharmacists in this study was increased knowledge of the general population about appropriate antibiotic use through various educational interventions. Conclusion Pharmacists report a number of E. Black (&) S. Bakharaiba E. Al-Mekaty D. Alsahan College of Pharmacy, Qatar University, PO Box 2713, Doha, Qatar e-mail: [email protected] A. Cartwright Pharmacy Department, Sidra Medical and Research Center, PO Box 26999, Doha, Qatar
misconceptions and inappropriate practices relating to antibiotic use in Qatar by patients and healthcare providers. Education to improve knowledge of appropriate antibiotic use is needed. Despite recognition of these issues, barriers are preventing pharmacists from implementing strategies to improve antibiotic use in Qatar. Keywords Antibiotics Community pharmacy General public Pharmacist Pharmacist opinion Qatar
Impact of research findings • •
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A lack of knowledge by the general population contributes to inappropriate antibiotic use Pharmacists perceive that patient demand is one of the greatest barriers to improving antibiotic utilization by community pharmacists Educational interventions by community pharmacists and other healthcare providers using a variety of formats are needed to improve knowledge of the general population
Introduction Antimicrobial resistance is increasing at an alarming rate worldwide [1–5] and there is evidence to suggest that as a consequence patients are failing first line antibiotic therapies [6]. Additionally, patients are requiring longer and more expensive treatment courses, and most notably, these drug resistant infections are putting patients at an increased risk of death [3, 6, 7]. The development of antibiotic resistance is a natural phenomenon resulting from the exposure of microorganisms
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to antibacterial agents that can be accelerated by the widespread use of antibiotics [8]. While the advent of antimicrobials has significantly decreased morbidity and mortality associated with many infectious diseases, indiscriminant use threatens to increase the risk of death from previously curable infections [9]. Although rates of antimicrobial resistance are increasing [1], few novel antibiotics are currently being developed. This has resulted in concern from the global medical community about a return to the ‘‘pre-antibiotic’’ infectious disease era [10]. The inappropriate use of antibiotic drug therapy has been identified by the World Health Organization as a risk factor for antimicrobial resistance [8]. An increase in antibiotic consumption has been correlated with development of resistance [11–13]. Costelloe et al. [11] found a significant association between any antibiotic use in individual patients and subsequent antibiotic resistance within the following 12 months. The prevalent use of fluoroquinolones has also been shown to be associated with increased rates of fluoroquinolone resistant Escherichia coli [12]. Additionally, longer duration and multiple courses of antibiotics were also associated with higher rates of resistance [11]. Given the positive association between antibiotic consumption and resistance rates, it is not surprising that decreasing antibiotic usage can result in a corresponding decrease in the incidence of antibiotic resistant pathogens. In Finland, a reduction in the use of macrolide antibiotics was followed by a significant decrease in group A streptococcus erythromycin resistance rates from 16.5 to 8.6 % over a 4 year period [14]. In another study, Hicks et al. [15] found that higher rates of outpatient antibiotic prescribing was associated with a greater proportion of non-susceptible invasive pneumococcal disease isolates as compared to areas with lower prescribing rates. Antibiotics are commonly prescribed to community dwelling patients. In a survey by Al-Niemat et al. [16] over 35 % of prescribed medications from an outpatient clinic were for antibiotics. A similar rate of prescribing was found in a survey of antibiotic consumption in a community setting in New Delhi, with 43 % of patients visiting a private clinic being prescribed at least one antibiotic [17]. Given this high rate of antibiotic use in the community setting, improving the judicious use of antibiotics in this population may have a significant impact on altering antibiotic resistance rates. Due to a high volume of antibiotic prescribing in the community setting, pharmacists may be ideally positioned as front line health care providers to limit indiscriminate antibiotic use and promote the safe and effective administration of these medications. In Qatar, patients receive medications from private community pharmacies, dispensaries affiliated with
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primary care clinics, and outpatient dispensaries in hospitals. Currently, regulations require a prescription prior to dispensing antimicrobial agents in Qatar. Beyond fulfilling legal requirements, it is unknown what, if any strategies have been implemented to improve antibiotic use in the community and no study has evaluated pharmacists’ perception of potential areas for improvement in antibiotic utilization. In order to implement effective strategies, specific targets for improving antibiotic use must be identified.
Aim of the study The aim of this project was to assess pharmacists’ opinions about antibiotic utilization in the community practice setting.
Ethical approval This study was reviewed and received research ethics exemption by the Qatar University Institutional Review board (QU-IRB 155-E/12).
Methods Study design A series of three focus groups and two small group interviews with a total of 22 participants were completed by study investigators in order to determine suggested strategies for improving antibiotic use in the community. A qualitative study design was chosen to explore rationale for limited implemented services, perceived barriers to implementing services, and to determine pharmacists’ perceptions of patient and healthcare provider educational needs in Qatar. Focus groups were defined as group discussions consisting of 4–10 participants facilitated by a study investigator. For invited participants who were not able to attend scheduled focus groups, alternative dates for individual or small group (2–3 participants) interviews were offered. Participants Community and primary care pharmacists were recruited to participate in one of three focus groups or, had the option to complete an individual or small group interview at their convenience. All community pharmacists and primary care pharmacists were invited to participate through email invitations send through the Qatar
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University continuing professional development database. To identify pharmacists who may not have received the email invitations, pharmacists attending continuing professional development events at the university received a written invitation. In addition, managers of several community pharmacy chains were asked to notify their pharmacists of the project. Any community or primary care pharmacists who spoke English and were currently practicing in Qatar were eligible to participate. Community pharmacists in Qatar practice in privately owned retail pharmacies while primary care pharmacists work in dispensaries or clinics attached to a healthcare center. Pharmacists who had previously practiced in Qatar as a community pharmacist and those who had completed at least 2 months of structured practical experiential training as pharmacy students in a community pharmacy setting in Qatar were also included in this study. To ensure participants were willing to openly discuss experiences, pharmacists were grouped to a focus group or interview based on their specific practice environment (community, primary care, or former students who had completed at least 2 months of structured practical experiential training). Three focus groups consisting of 4, 5, and 8 participants respectively, and two small group interviews consisting of 2 and 3 participants respectively took place. Pharmacists who had not practiced in a community or primary care setting in Qatar were excluded.
Table 1 Focus group and interview guide Community pharmacist focus group and interview questions 1. In your practice, what are the most common types of infectious diseases you encounter? 2. What are some common misconceptions or inappropriate practices patients may have relating to treatment of infections or appropriate antibiotic use? 3. Which strategies should be considered highest priority to resolve from the perspective of healthcare providers? 4. What are some actions you currently use to improve antibiotic use in your area of practice? 5. In your opinion, what are some services community pharmacists could offer to improve appropriate use of antibiotics by the general population in the community? 6. Do you feel community pharmacists need additional training to implement suggested strategies? 7. What are some barriers to implementing interventions you have suggested to improve antibiotic use at your practice site? 8. What are some strategies to overcome barriers which would allow community pharmacists to provide services relating to improving antibiotic use at your practice site? 9. Is there anything else you would like to say about improving antibiotic use in the community through pharmacist lead interventions?
the participants’ place of employment in Doha, Qatar. The duration of focus groups and interviews ranged from 45 to 90 min. Each focus group or interview was audio-recorded to allow for transcription after the session took place.
Data collection Analysis All focus groups and interviews were facilitated by a member of the research team (EB). Other research team members (undergraduate and graduate pharmacy students) assisted to take notes when academic schedules would allow. Notes were used as a backup in the event that the recorder failed and to document facial expressions and emotions of participants. Sessions were facilitated using an interview guide consisting of nine open-ended questions. Questions were developed by study investigators based on objectives of this study and two previously completed surveys of the general population’s knowledge of appropriate antibiotic use in Qatar and pharmacists’ perceptions of currently implemented antimicrobial stewardship activities and barriers to implementation of services in Qatar. Every discussion began with an engagement question followed by a series of exploratory questions and ended with an exit question. Questions included in the interview guide are outlined in Table 1. Focus groups and interviews took place until no new ideas were generated. The saturation point was met after completing three focus groups and two small group interviews. Sessions were conducted at Qatar University or at
Data were analyzed using the Framework method as described by Gale et al. [18] with assistance of Nvivo software for qualitative research. Themes were identified inductively from the data as described by Patton in ‘‘Qualitative Research and Evaluation Methods’’. Inductive analysis should permit patterns to emerge as data is collected rather than defining specific research hypotheses prior to performing interviews [19]. While focus groups and interviews were completed with an interview guide, investigators began analysis during data collection with research team members listening for themes and prompting participants to elaborate outside the interview guide (if relevant) during the course of the discussions. To ensure an inductive approach was used, open-ended questions were asked allowing participants to determine the direction of the discussion. After each focus group or interview, the research team members present during the discussions met to review specific observations. Emerging patterns were also identified. Transcription of recorded discussions took place shortly after the focus group session by members of the
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A total of 22 pharmacists from community and primary care settings participated. The majority of pharmacists were female (72.7 %) and practiced in the primary care setting (59.1 %). Baseline characteristics of pharmacists are outlined in Table 2. Five major themes relating to antibiotic use were identified throughout interview sessions and are discussed below. Themes included: misconceptions and inappropriate practices, implemented strategies, perceived barriers, ways to overcome perceived barriers, and targets for improvement of antibiotic use in Qatar. All interview questions were addressed and coded under the above themes with the exception of the question ‘‘Which strategies should be considered highest priority to resolve from the perspective of healthcare providers’’. When asked this question, pharmacists quickly shifted to discussing barriers limiting implementation of strategies.
self-limiting illnesses. Non-compliance with prescribed directions was also reported by most groups. Pharmacistreported rationale for patient non-compliance included discontinuation of antibiotics prematurely due to resolution of symptoms and use of higher doses of antibiotics with the perception that the patient would get better faster. One participant highlighted that ‘‘when they have a prescription, they will just ask for half of it when the doctor has prescribed a week of the prescription but they will just take half of it and say I am fine in 2 or 3 days (Interviewee 1, Community Pharmacist)’’. Participants also reported the general population had a lack of awareness relating to development of resistance, adverse effects of antibiotics, and antibiotic allergies. Inappropriate practices by healthcare providers were also identified. Pharmacists practicing in community-based settings reported that antibiotics are being dispensed over the counter in some community pharmacies despite laws requiring a prescription to dispense. One participant indicated, ‘‘if the patient or customer is a friend of the pharmacist, he give them antibiotic but it is a prescribed medicine (Interviewee 4, Community Pharmacist)’’. Pharmacists from primary care settings felt this was less of a concern due to internal policies which reinforced national dispensing laws and regulations. Some participants also reported a lack of patient counseling by pharmacists and limited interdisciplinary communication between pharmacists and physicians. Both community and primary care pharmacists reported suboptimal prescribing resulting in overuse of antibiotics for self-limiting illnesses, broad-spectrum antibiotic selection, and lack of patient assessment by physicians. One participant stated ‘‘Cephalosporin for example, the third generation cephalosporins. I used to get this prescription from one doctor. Different patients but the same prescription (Interviewee 2, Community Pharmacist)’’. Another participant commented, ‘‘From the doctor himself, he doesn’t follow the procedures of prescribing an antibiotic. Some manufacturers will go for him and ask him to write this antibiotic and he will get a journey to some Middle East or some gift like that (Interviewee 4, Community Pharmacist)’’.
Misconceptions and inappropriate practices
Current strategies to improve antibiotic use
Participants reported a wide range of misconceptions and inappropriate practices with regards to antibiotic use by the general population in Qatar. All groups indicated that the general population had a low level of knowledge relating to the appropriate use of antibiotics. The majority of participants discussed frequent desire of patients to use antibiotics when not indicated, and the occasional use of antibiotics when not prescribed to treat viral and other
Most groups identified few ongoing strategies to promote appropriate antibiotic use in community and primary care settings. Where strategies exist, the most commonly reported initiative was patient education in the form of patient counseling at the time of dispensing. One respondent commented, ‘‘if there is a side effect, pharmacists are highlighting side effects from this antibiotic’’ (Interviewee 20, Primary Care). Primary care pharmacists reported internal
Table 2 Baseline characteristics (N = 22) Characteristics
N (%)
Female
16 (72.7)
Primary area of practice Community pharmacy
4 (18.2)
Primary care pharmacy
13 (59.1)
Former practice in a community pharmacy Pharmacists completing entry-to-practice degree and experiential training in Qatar
5 (22.7) 4 (18.2)
research team. Transcripts were recorded verbatim. Transcriptions were then reviewed and an initial codebook was constructed by the research team based on emerging patterns. Using the codebook, two of more study investigators independently coded transcripts for recurring themes using nodes in Nvivo. After initial coding, themes were then reviewed for similarity and grouped together. Subthemes were identified and coded as child nodes in Nvivo. Consensus was achieved through face-to-face discussions with the research team.
Results
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antibiotic guidelines were available; however, groups acknowledged limited implementation in routine patient care. A small number of pharmacists reported interacting with physicians when drug related problems such as prescribing of duplicate therapy arose. While current strategies to improve antibiotic use were briefly outlined in all groups, pharmacists quickly shifted to lengthy discussions about ongoing barriers to improving antibiotic use. Barriers to improving antibiotic use All groups extensively discussed current barriers to improving antibiotic use in the community and primary care settings. Many participants highlighted that the number of barriers was overwhelming and before interventions could be developed, pharmacists must work collaboratively with government regulatory authorities, the College of Pharmacy at Qatar University, and other healthcare providers to overcome these barriers. Primary subthemes that emerged during discussion of barriers included: patient demand, low level of knowledge by healthcare providers, poor perception of pharmacists, and business model of community pharmacy practice. One of the most common barriers to improving antibiotic use in both the community and primary care settings was patient demand to prescribe and dispense antibiotics. One pharmacist stated ‘‘but what is the use? From the doctor itself, the patient ask them, I want you to write me this. They know what they want. They are dictating (Interviewee 1, Community Pharmacist)’’. Another pharmacist highlighted burden on pharmacists through the statement ‘‘sometimes the pharmacist refuse to give them antibiotic but they wait in the pharmacy and argue to get the antibiotic (Interviewee 4, Community Pharmacist)’’. Another common barrier was level of healthcare provider knowledge. Participants primarily focused on level of knowledge of pharmacists. During discussions about the level of knowledge of the pharmacist, one participant reported, ‘‘we are not aware anymore what’s the latest medicines, vaccines, and antibiotics, and the side effects (Interviewee 3, Community Pharmacist)’’. In addition to improvement in the level of knowledge regarding pharmacotherapy, participants also highlighted the need to improve critical appraisal and communication skills as evident by the statement ‘‘how to discuss evidence based practice, the communication skills, these all need to be the training for the pharmacist (Interviewee 8, Former Student)’’. Furthermore, participants reported poor perception of pharmacists by the public and healthcare providers. Referring to the perception of the general population, one participant reported, ‘‘they think the pharmacist is only a store keeper in a grocery shop (Interviewee 5, Community Pharmacist)’’. Another pharmacist stated, ‘‘the perception,
Table 3 Perceived barriers to improving antibiotic use and suggestions to overcome barriers of interviewed pharmacists (N = 22) Barrier
Suggestion
Patient demand
Patient education Development and enforcement of laws and regulations pertaining to prescribing and dispensing of antibiotics
Knowledge of healthcare providers
Mandatory continuing professional development Development of specialty training programs for pharmacists
Poor perception of pharmacists
Education about the role of the pharmacist
Time
Increase staffing in pharmacies
Develop a pharmacist society Allow pharmacists to read educational materials during working hours Business model of pharmacy practice
Development and enforcement of laws and regulations pertaining to dispensing of medications
Lack of resources
Provision of internet access and up-to-date resources
Lack of clear laws and regulations guiding prescribing and dispensing of medications
Development and enforcement of laws and regulations pertaining to prescribing and dispensing of medications in Qatar
Lack of motivation
Provide monetary incentives for pharmacists
Communication
None suggested
even from our families they [pharmacists] are educated sellers (interviewee 8, Former Student)’’. Poor perception by physicians was also perceived as outlined by the statement ‘‘Sometimes the doctors, they don’t approve of the intervention (Interviewee 11, Primary Care Pharmacist)’’. Furthermore, the most lengthy discussions regarding barriers experienced by community pharmacists related to the current business model of community pharmacy practice and lack of comprehensive laws and regulations relating to prescribing and dispensing of medications. Participants highlighted that individuals without a pharmacy degree typically own community pharmacies. Concern was raised with respect to an emphasis on sales as opposed to provision of patient care. Dissatisfaction with the current business model of community pharmacy practice was summarized in the statement ‘‘So the owner is thinking for the business and getting more money and the pharmacist is under pressure to sell and to get more profit (Interviewee 5, Community Pharmacist)’’. Pharmacists practicing in primary care clinics did not report these concerns as the dispensary is owned and operated by
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primary health care centers. All perceived barriers reported by focus group participants are outlined in Table 2. Ways to overcome barriers Pharmacists recommended a number of strategies to overcome the discussed barriers, which would enable pharmacists and other health care providers to improve antibiotic use in the community setting. All groups extensively discussed the need for education of patients and health care providers through various means. One participant highlighted ‘‘Education for doctor, education for patient, education for pharmacists (Interviewee 15, Primary Care Pharmacist)’’. While less of a concern for primary care pharmacists, updating and enforcing laws and regulations pertaining to prescribing and dispensing of medications was a common suggestion across groups who practiced in community pharmacy settings. One participant stated ‘‘I think for myself, I don’t even know the Qatari laws (Interviewee 7, Former Student)’’. Another pharmacists referring to practice in community settings in Qatar commented ‘‘I want to implement a protocol. A very strong protocol for the community pharmacy. A strategy, how to dispense the antibiotic and under which circumstances you can dispense an antibiotic (Interviewee 5, Community Pharmacist)’’. Other strategies to overcome identified barriers are outlined in Table 3. Targets for improvement Despite a wide range of listed barriers and suggestions for improvement, all groups discussed the need to improve the knowledge of the general population about appropriate antibiotic use. Pharmacists felt the general population should be educated through various means including education in the media, awareness campaigns at public venues, as well as routine counseling and education in community and primary care pharmacies. Other suggested targets to improve antibiotic use included interdisciplinary communication between healthcare providers as highlighted by one pharmacists who indicated ‘‘communication and intervention is very important between the pharmacists and the doctors (Interviewee 10, Primary Care Pharmacist)’’, development of clinical practice guidelines based on local patterns of resistance, and further practice-based research to assess the success of implemented strategies.
Discussion This is the first qualitative study to evaluate community pharmacist perceptions of antibiotic use in Qatar. Pharmacists participating in this study suggested ongoing need
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for improvement in prescribing and dispensing by healthcare providers in addition to increased awareness of appropriate antibiotic utilization by patients. While pharmacists recognize these issues, barriers are preventing implementation of interventions to improve antibiotic utilization. Pharmacists participating in this study perceived that a lack of knowledge by patients resulted in inappropriate use of antibiotics. A lack of knowledge and resultant misuse of antibiotics has been documented internationally [20–22]. A low level of antibiotic knowledge consequently has been shown to correlate with non-adherence [20]. Multiple educational interventions targeted at patients and healthcare providers to improve overall knowledge and use of antibiotics have been recommended by study participants in Qatar and is consistent with those previously recommended in the literature [23–25]. Pharmacists working in community practice settings are the most accessible healthcare providers and are ideally positioned to provide educational interventions [26]. A survey by El-Hajj and Colleagues completed with the general population in Qatar demonstrated that 52 % of respondents visit a community pharmacy monthly. Despite frequent visits to community pharmacies, 50 % of respondents reported physicians as their first contact to answer drug related questions [27]. In a systematic review of community pharmacist involvement in health promotion, mixed findings from general population on pharmacist participation were reported. For those who experienced health promotion interventions by pharmacist, the overall perception was positive. The authors concluded that with increased exposure to health promotion activities, attitudes towards pharmacists participation in health promotion activities by the general population would improve. The authors suggested pharmacists needed to be more proactive in offering services and may need additional training to increase confidence in order to change attitudes [28]. Similarly, our findings indicate limited ongoing education and health promotion activities by community pharmacists. Despite these findings, pharmacists believe they can play an important role in public health promotion by educating the public about appropriate antibiotic use in Qatar. In order to increase utilization of community and primary care pharmacists in health promotion, barriers should be overcome. Currently, several barriers are preventing pharmacists from providing services to improve antibiotic utilization. Concerns outlined by community pharmacists in Qatar have been echoed by pharmacists internationally [25, 29, 30]. A qualitative study completed in India identified inappropriate prescribing and dispensing as an area of concern and notably, patient demand was thought to be a major contributing factor [25]. Roque et al. [29] also reported patient demand on pharmacists to dispense and
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physicians to prescribe antibiotics. Pharmacists in Portugal have identified that patient self-medication with leftovers from previous treatments, non-compliance with prescribed dosages, suboptimal prescribing by physicians, and use of antibiotics in animals for human consumption are major factors contributing to development of resistance in their country [29]. In addition, an American study reported time constraints, fear of harming relations with physicians, and lack of educational material as barriers to engaging in antibiotic campaigns [30]. Finally, a study completed in the United Kingdom reported poor perception of the pharmacist’s competencies by the general population and other health care providers as a significant obstacle to pharmacists providing public health services [31]. Local inappropriate practices and barriers to improving antibiotic use must be considered during the process of developing a health promotion strategy. Interventions to improve knowledge of the general population and health care providers are needed in Qatar. Currently, no pharmacist associations or societies in the country exist. All medical and healthcare provider licensing and regulation is overseen by the national Supreme Council of Health who are responsible for quality and effectiveness of services delivered in private and public sectors of healthcare [32]. Development of a professional pharmacist’s society may assist in supporting an expanded scope of practice for pharmacists and improving the general population’s perception of community pharmacists. In addition, clarity and enforcement of laws and regulations pertaining to prescribing and dispensing of antibiotics is needed. Our findings provide valuable insight pharmacists’ perceptions of antibiotic use and strategies for improvement in Qatar; however, in considering results, a number of limitations should be noted. While perceptions of pharmacists participating in the interviews and focus groups were consistent, our findings represent input from a small sample of community and primary care pharmacists in Qatar. The exact number of pharmacists in Qatar is unknown; however it is estimated from our continuing professional development database that 1,000 pharmacists work in community, primary care, academic, or hospital settings. In addition, interview sessions were completed in English while the majority of participants spoke English as a second language, which may have resulted in misunderstanding of interview guide questions. To overcome this barrier, the facilitator rephrased questions when concern arose. The facilitator of the focus groups was a pharmacist, which may have impacted responses and contributed to social desirability however; we believe this bias has been minimized as the facilitator refrained from sharing their own perceptions. In addition, the facilitator was a faculty member who did not work in community practice. Furthermore, due to an extension in timeline of
the research project, collaborators assisting in data collection during the final two focus groups were not available to assist in note taking due to other commitments. To overcome this barrier, all sessions were recorded and at least two collaborators reviewed transcripts. Finally, results from this study represent perceptions of community and primary care pharmacists in Qatar and cannot be generalized to pharmacists practicing in other countries or in the inpatient setting.
Conclusion Community and primary care pharmacists recognize a lack of knowledge and inappropriate practices relating to antibiotic use by the general population and healthcare providers in Qatar. Barriers are limiting ongoing initiatives to promote judicious use of antibiotics. Interventions targeting the general population, health care providers, and regulatory authorities are needed to combat indiscriminant use of antibiotics and development of resistance. Acknowledgments The authors of this manuscript would like to thank the Qatar Petroleum Health and Wellness Center pharmacy department for their contributions to this project. Funding This study was completed with funding from an Internal Student Grant from Qatar University. Conflicts of interest The authors of this paper report no conflicts of interest.
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