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Article history: Background: The World Health Organization released a Global Action Plan to overcome the threatening
Received 25 April 2019 concerns of antibacterial resistance. One of the cornerstones of this plan is the Antibiotic Stewardship
Received in revised form 23 June 2019 Program (ASP). The study aimed to assess the community pharmacists’ knowledge, perceptions and
Accepted 2 July 2019
current practices regarding ASP.
Methods: A qualitative study was conducted in Bahawalpur, Pakistan, in which data were collected from
Keywords:
the community pharmacists through in-depth, semi-structured interviews. The convenience sampling
Drug regulatory authority of Pakistan
technique was used to recruit the study participants. Interview protocol was pilot tested and the sample
Community pharmacies
Developing countries
size was limited by applying the saturation point criteria. All interviews were audio recorded and tran-
Health education scribed verbatim. The thematic analysis approach was used to analyze the data and draw conclusions
Antibiotic resistance based on study objectives.
Results: A total of fifteen community pharmacists were interviewed. Analysis of the data yielded five
themes and 16 subthemes. All of the respondents had sound knowledge about the irrational use of
antibiotics; however, they were oblivious about the ASP. After explaining the term, the respondents
were of the opinion that these strategies could not be implemented in the current healthcare system
of the country. According to the findings of the study, prescribing and dispensing practices were not
followed. Only a few patients were educated about the antibiotics they were purchasing.
Conclusion: Most of the study participants were unaware of any ASP being offered in the community
pharmacy settings. The study participants agreed to be the antibiotic stewards, but a number of obstacles
were reported. The training of pharmacists, medication reconciliation, the implementation of the good
pharmacy practice guidelines and assurance of pharmacist availability at drug retail outlets were few
suggestions given by the study participants to incorporate the ASP in the community settings.
© 2019 The Authors. Published by Elsevier Limited on behalf of King Saud Bin Abdulaziz University
for Health Sciences. This is an open access article under the CC BY-NC-ND license (http://
creativecommons.org/licenses/by-nc-nd/4.0/).
https://doi.org/10.1016/j.jiph.2019.07.003
1876-0341/© 2019 The Authors. Published by Elsevier Limited on behalf of King Saud Bin Abdulaziz University for Health Sciences. This is an open access article under the
CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
M. Atif et al. / Journal of Infection and Public Health 13 (2020) 118–124 119
of decreased development of new antibacterial drugs continued in the final analysis. The interview guide underwent iterative revi-
[7]. The World Health Organization (WHO) released the Global sion during the study to ensure that evolving themes can be best
Action Plan (GAP) in 2015 to overcome the threatening concerns captured in subsequent interviews [28].
of antibacterial resistance [8]. One of the cornerstones of this GAP
is the Antibiotic Stewardship Program (ASP) which engrosses the Recruitment and data collection
appropriate use of antibiotics in humans as well as in animals [8,9].
The program is aimed to target the optimal clinical outcomes with The study participants were recruited by using the convenience
minimal undesired consequences of antibacterial therapy, includ- sampling technique. In the first step, a list of pharmacies was gen-
ing reduction in toxicity, adverse events and cost of therapy [10,11]. erated where community pharmacists were working. In the second
In Pakistan, the existence of unregistered medical practitioners step, the target participants were approached and conveniently
(quacks), low quality prescriptions, self-medication and easy access selected based on their availability and willingness to participate
to antibiotics at the drug retail outlets are major threats to the in the study. All semi-structured interviews were conducted by
future of antibiotics [12]. Various studies have reported higher than SA. The interviews were conducted at the participants’ workplace
optimal and inappropriate use of antibiotics in Pakistan [13–17]. between October and November 2018. Before conducting the inter-
Consequently, there is an increase in antibiotic resistance in the views, written informed consent to participate in the study was
country which is making the drug therapy complex for infectious obtained from the participants after explaining the nature and
diseases [18]. Considering the need to reduce the unnecessary and objectives of the study to them. Prior to initiating the interview, the
inappropriate use of antibiotics [12,19], the Medical Microbiology participants completed a demographic data collection form which
and Infectious Diseases Society of Pakistan adopted the general recorded the details, including gender, age, qualifications, work-
guidelines provided by the GAP, and initiated the ASP in 2016 ing experience and details of any specific training undertaken on
[12,19]. The plan was implemented successfully in various hospital antimicrobial stewardship. All interviews were conducted in the
settings, but not in community pharmacy settings despite the fact national language of Pakistan (Urdu) and were audio recorded.
that inappropriate antibiotic use is highly prevalent in these set- Observation notes were also taken for all respondents. The sample
tings [16,20]. Data outlining the inappropriate use of antibiotics in size was limited by applying the saturation point criteria [29].
the community justify the extension of ASP in these healthcare set-
tings [16,21]. Community pharmacists can play an important role Data management and analysis
in the implementation of ASP and this advanced role of pharmacists
has been witnessed in earlier studies [22–24]. In Pakistani context, The thematic analysis approach was used to analyze the data
though the community pharmacists are not following the set of ASP [30]. The data were analyzed in six phases; familiarization with the
protocols, but it is important to capture their perceptions and cur- data, generation of initial codes, searching for themes, reviewing
rent practices regarding this program. Therefore, in this study, we themes, defining and naming themes and producing the report [30].
aimed to assess the community pharmacists’ knowledge, percep- Data familiarization was initiated at an early stage when data were
tions and practices regarding ASP in Pakistan. The findings of this listened carefully for several times, transcribed verbatim and trans-
study will not only identify the antibiotic use practices at the com- lated into English. Open coding was commenced by two authors (SA
munity pharmacies in Pakistan, but will also help the policy makers and IM) to generate the initial codes representing the study objec-
to tackle the challenges associated with successful implementation tives. These initial codes were then categorized and arranged to
of ASP in these settings. generate the potential themes. The generated themes were then
reviewed and refined by all authors. Further analysis was per-
formed in next phase to generate clear definitions and phrase for
Methods
each theme. In the final stage, the report was drafted (all authors).
Cross checking of the emergent themes and conclusion was made
Study design and setting
by the research team to ensure the data credibility. In case of any
conflict or disagreement, the decision of the senior authors (MA
In this qualitative study, community pharmacists working in
and IMU) was considered final.
the Bahawalpur district of the Punjab province of Pakistan were
interviewed by using semi-structured interview schema. There are
Results
about 500 drug retail outlets located in various areas of Bahawalpur
[25] but only a few pharmacies provide the services of community A total of 15 interviews were conducted and the interview
pharmacists [26]. Others are run by non-pharmacist proprietors duration ranged from 19 to 47 minutes with a mean duration of
only by hiring the license of qualified pharmacists [26]. Most of the 28 minutes (SD = 8.5 min). Among the participants, 10 were males
pharmacies in Bahawalpur are clustered around the Bahawal Victo- and five were females. The age of interviewed pharmacists ranged
ria Hospital, which is a large tertiary care hospital in the Bahawalpur from 23 to 32 years (mean age = 26.13; SD = 2.41). The participants
district, while others are located near populated areas. Community had mean work experience of two years (SD = 1.4). The demo-
pharmacists willing to participate in the study, registered with the graphic characteristics of the respondents are outlined in Table 1.
Punjab Pharmacy Council and having minimum work experience The analysis of the data yielded five overarching themes, includ-
of at least one year at community drug retail outlets were included ing knowledge about the irrational use of antibiotics, initiatives to
in the study. restrict the irrational use, familiarity with the ASP, current prac-
tices and suggestions for the implementation of the ASP. Themes
Study instrument were characterized by 16 subthemes to best capture the diversity
of participants’ perspectives. The emerged themes, subthemes and
The study instrument was designed by the research team, after exemplar quotations are illustrated in Table 2.
a thorough literature review [4,12,27] to best answer the research
problem and address gaps in the literature. The interview guide was Theme 1: Knowledge about irrational use of antibiotics
modified following piloting with two community pharmacists to
ensure the uniformity, face validity and understandability (please All respondents had the appropriate knowledge about the irra-
refer to Additional File 1). The pilot interviews were not included tional use of antibiotics. The respondents pointed out a number
120 M. Atif et al. / Journal of Infection and Public Health 13 (2020) 118–124
Table 1
Demographic characteristics of participants.
Respondent A Female 24 2 34
Respondent B Male 25 3 29
Respondent C Female 25 1 23
Respondent D Male 26 2 22
Respondent E Male 27 1.5 47
Respondent F Male 24 2 22
Respondent G Female 24 1 23
Respondent H Male 26 2.5 26
Respondent I Female 23 1 26
Respondent J Male 28 2 30
Respondent K Male 27 2 19
Respondent L Male 25 1.5 29
Respondent M Male 30 6 24
Respondent N Female 26 2 24
Respondent O Male 32 5 47
Mean duration 28
of aspects involved in the irrational use of antibiotics, including be devised and implemented effectively. Along with the train-
overuse, underuse, self-medication, improper selection of antibi- ing of pharmacists, the general public should be educated on the
otics and not following the prescription guidelines. appropriate use of medicines. Medication compliance should be
assured by the proper counseling of the patients. Moreover, the
Theme 2: Initiatives to restrict the irrational use of national good pharmacy practice guidelines should be developed
antibiotics and implemented to rationalize the therapy according to the ASP
principles.
Many initiatives were suggested by the respondents to ratio- The participants further stated that the government should
nalize the use of antibiotics, including evidence-based therapy, sponsor the research projects to find the recent trends in antibi-
avoidance of broad-spectrum antibiotics, rationalization of pre- otic use and antibiotic resistance, and the they further stated that
scription and monitoring of antibacterial therapy. According to the the availability of qualified persons (pharmacist) should be assured
respondents, an empiric therapy based on the physicians’ experi- at all community pharmacy settings.
ence should be avoided. Instead, antibiotics should be prescribed
after culture and sensitivity testing.
Discussion
Table 2
Respondents’ views about the Antibiotic Stewardship Program; themes, subthemes and exemplar quotations.
Table 2 (Continued)
Patient education “General public training is necessary. Public can wait at doctor’s clinic even for hours but at pharmacy
if they have to wait for 5 minutes they are about to die”. (Respondent A)
“Patients should be guided about completion of therapy. Blister packing should be stopped and
complete bottle should be dispensed and sold which contain complete course of therapy. When the
patients will purchase medicine by spending money then they tend to complete the therapy as they had
spent money on it”. (Respondent B)
“Patient guidance material can be used such as display cards or pictures to make the patients
understand in better way”. (Respondent E)
National good pharmacy practice guidelines and “Policies and rules at national as well as institutional levels should be devised for good pharmacy
their implementation practice. It may involve existing global antibiotic ASP guidelines or develop their own ones. These rules
should be implanted by the government. Some guidelines are present but these are not implemented. If
these will be implemented then system will improve”. (Respondent D)
“Pharmacy practice guidelines provided by the WHO and other organizations should be introduced at
national level including the supply of quality medicines with appropriate guidance and resolving
economic issue”. (Respondent I)
Medication reconciliation “The concept of prescription assessment and check for errors in prescribed medicines should be
introduced at community pharmacies. Pharmacist is a qualified person to perform these tasks and to
improve the patient health”. (Respondent M)
“Dose, dosing frequency, interactions, side effects and then discussion about these things if there is any
problem with the physician is necessary to perform the monitoring of therapy which is an essential part
of stewardship as you explained” (Respondent J)
Research “I had seen in a report from India that by 2025 the whole India will be resistant to antibiotics. If India is
going to be resistant by 2025 then in Pakistan it will be earlier. We are such a nation which does not
have data that how many patients are resistant to which antibiotics. We must have data. The
government should sponsor the research projects for finding facts about this serious issue. Rules and
regulations should be made and implemented properly”. (Respondent E)
Availability of community pharmacist “Pharmacist should be available at every community set-up. Awareness should be increased among the
community. Campaigns should be arranged. There is an urgent need to educate the general public
about the role of pharmacist and appropriate use of antibiotics”. (Respondent D)
“Pharmacist duty timing should be increased and availability should be assured for all the time when
pharmacy is opened”. (Respondent H)
Awareness of newer trends in antibacterial “Pharmacists should have sound knowledge about ASP. Only then they can take part in tracking and
therapy monitoring strategies for the proper use of antibiotics. Community pharmacists should keep them up-to
date with newer global campaigns and international trends to play their role in effective patient
management”. (Respondent O)
“Community pharmacists should follow the good practice guidelines provided by the international and
national organizations and perform expanded activities of pharmacist at community settings. This will
be helpful in implementation of ASP strategies”. (Respondent I)
The findings of the current study demonstrated a lack of aware- healthcare professionals. This finding indicates that antimicrobial
ness about ASP among the community pharmacists. These findings awareness seminars and workshops were not offered to healthcare
are in line with a study conducted in England, where community professionals in Pakistan. This is contrary to the findings of stud-
pharmacists were generally unaware of any stewardship initiatives ies conducted in many countries where these seminars were held
from within and outside of the community pharmacy settings [33]. regularly [4,9,35,36]. Our respondents advocated the organization
The majority of our study participants had never heard of the term of conferences, workshops and seminars for the community phar-
“antibiotic stewardship”. Despite this lack of awareness, when the macists to build their competency for the active involvement in
term was explained to them, they believed that they had a role the ASP and antibiotic surveillance. These findings are similar to
in monitoring the antimicrobial therapy and in the education of the findings of an Ethiopian study in which 90.5% of pharmacists
the general public about the appropriate use of antibiotics. Simi- suggested such training programs [35].
lar results were shown in a previous study conducted in Malaysia Knowledge of antibiotic resistance patterns, increased aware-
where community pharmacists were eager to take part in ASP and ness about latest treatment guidelines, effective patient counseling
recognized the importance of this program [4]. According to our and monitoring the antibiotic use patterns were the important
study participants, surveillance of antibiotic use practices in Pak- strategies suggested by our respondents as a part of community-
istani community was not possible due to lack of access to patient based ASP. According to them, community pharmacists are suitable
medical records. This might be possibly associated with absence healthcare providers to handle the vast majority of patient-initiated
of medication reconciliation practices in the country [4] and the consultations, and should be more systematically involved in a
same was reported in our study. Improved communication among triage-type role on the front line. The participants of the current
the healthcare professionals could significantly assist in optimiz- study emphasized that the presence of community pharmacists
ing the use of antibiotics and is an essential feature of ASP [34]. should be assured at drug retail outlets so that the patients in the
Similar implications were suggested in a previous Pakistani study community are able to seek advices about their health issues [37].
which stated that the healthcare professionals should work within The strength of the present study is that it highlighted a health
multi-disciplinary teams to reduce the problem of antimicrobial policy issue in which the availability of evidence-based literature is
resistance and improve the quality of life of patients [12]. very limited, especially from developing countries. This study has
Similar to the findings of Rehman et al., our respondents were a few limitations as well. First, we used the convenience sampling
of the opinion that suitable training of community pharmacists is strategy to recruit the study participants. The random selection of
necessary for the successful implementation of ASP [12]. Accord- study participant was not possible because only a limited number of
ing to the respondents, stewardship programs should be initiated pharmacies in Bahawalpur render the services of pharmacists and
in all community pharmacy and institutional settings, and antibi- some of the pharmacists were not willing to talk, possibly because
otic competency and training programs should be offered to the of their lack of knowledge about ASP. Therefore, those who were
M. Atif et al. / Journal of Infection and Public Health 13 (2020) 118–124 123
willing to participate in the study were selected. Second, the find- Ethical approval
ings of this study may not be generalized for the whole of Pakistan
because this study was conducted in one city. However, since a The approval for the conduct of study was obtained by the Phar-
uniform healthcare policy is implemented throughout the country macy Research Ethics Committee (PREC) at the Islamia University
and availability of pharmacists at retail drug outlets is scarce in the Bahawalpur (Reference: 41/S-2018-/PREC, dated May 31, 2018)
country, therefore, our findings provide an insight of what is hap- and permission to conduct research at community pharmacies was
pening in the country. Third, the age of the participants ranged from obtained from the Drug Controller, Bahawalpur.
23 to 32 years with a mean age of 26 years. One might argue that
the study participants are relatively young with little experience. Competing interests
In Pakistan, the concept of the presence of pharmacists at commu-
nity pharmacies is relatively new. Most of the drug retail outlets are None declared.
run without the presence of a pharmacist. For the past few years,
the government is trying to enforce the pharmacy rules. As a result, Availability of data
some of the pharmacy owners have now employed pharmacists
at their businesses. However, because this is a new dimension of The datasets used and analyzed during the current study are
the pharmacy profession in Pakistan, therefore, relatively a young available from the corresponding author on request.
lot of pharmacists are available in community pharmacy settings,
though there could be very few exceptions where senior commu- Acknowledgements
nity pharmacists are available.
We would like to thank the respondents for their participation.
Implications for practice and research
Appendix A. Supplementary data
The study will contribute to the literature by addressing the cur-
rent status and future prospects of ASP at community pharmacies Supplementary material related to this article can be found,
in Pakistan. Besides the implication of this study to literature, the in the online version, at doi:https://doi.org/10.1016/j.jiph.2019.07.
findings warrant the active considerations by policy makers, who 003.
may need to put legislation to introduce the ASP at community
settings in Pakistan. In practice terms, training and involvement of References
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