Pharmacy: Antibiotic Stewardship in Community Pharmacies: A Scoping Review
Pharmacy: Antibiotic Stewardship in Community Pharmacies: A Scoping Review
Pharmacy: Antibiotic Stewardship in Community Pharmacies: A Scoping Review
Review
Antibiotic Stewardship in Community Pharmacies: A
Scoping Review
Shazia Jamshed 1, * ID , Fadzlan Padzil 1 , Siti Hadijah Shamsudin 1 , Siti Halimah Bux 1 ,
Abdul Aziz Jamaluddin 1 , Akshaya Srikanth Bhagavathula 2 ID , Saira Azhar 3 and
Mohamed Azmi Hassali 4
1 Department of Pharmacy Practice, International Islamic University, Kuantan Pahang 25200, Malaysia;
[email protected] (F.P.); [email protected] (S.H.S.); [email protected] (S.H.B.);
[email protected] (A.A.J.)
2 Department of Internal Medicine, College of Medicine and Health Sciences, United Arab
Emirates University, Al Ain, Abu Dhabi 15551, UAE; [email protected]
3 College of Pharmacy, Princess Nourah Binti Abdul Rahman University, Riyadh 11671, Saudi Arabia;
[email protected]
4 Discipline of Social and Administrative Pharmacy, School of Pharmaceutical Sciences, Universiti Sains
Malaysia, Penang 11800, Malaysia; [email protected]
* Correspondence: [email protected] or [email protected]; Tel.: +60-1-7470-3692
Received: 31 March 2018; Accepted: 14 August 2018; Published: 23 August 2018
Abstract: The increase in antibiotic resistance has frequently been linked to unrestrained antibiotic
dispensing. This review was conducted to mainly assess the perception and attitudes of community
pharmacists towards antibiotic dispensing. This scoping review was performed between June 2016
and September 2016 to identify published studies related to the perception and attitudes of community
pharmacists towards antibiotic dispensing. The combination of terms such as ‘antibiotic dispensing’,
‘antimicrobial resistance’, ‘community pharmacy’, and ‘community pharmacists’ were searched in
electronic databases such as PubMed, ProQuest, Google Scholar, and Science Direct. Only published
articles within the last 12 years were included. A total of 13 studies were identified. In general,
community pharmacists have good awareness and knowledge of antibiotic dispensing. However,
the majority of them are still selling antibiotics to their customers and/or patients for unjustified
reasons. The community pharmacists seem well aware of the antimicrobial resistance crisis and
considered it a significant health issue. However, many embraced the concept that dispensing
antibiotics without medical prescription (DAwMP) can be one of the key features in the dissemination
of multidrug resistant bacteria.
1. Introduction
Increased prevalence of drug-resistant bacteria leads to an upsurge in morbidity and
mortality from bacterial infections [1]. Infection thrives due to drug-resistant bacteria and claims
thousands of lives each year [2]. A few commonly-encountered bacterial strains that develop
resistance to antimicrobials are Escherichia coli (E. coli), Klebsiella pneumoniae, Streptococcus pneumonia,
and methicillin-resistant Staphylococcus aureus (MRSA) [3].
Globally, one of the key issues in tuberculosis (TB) treatment is drug resistance. The statistics on
anti-TB drug resistance highlighted 123,000 patients with MDR-TB or rifampicin-resistant tuberculosis
(RR-TB) and around three-fourths were located in India, South Africa, China, and European regions [4].
The report from the Centre for Disease Dynamics, Economics, and Policy (CDDEP) outlined an
interesting scenario for MRSA.
During 2014 and 2015 it was reported that the incidence for MRSA was declined in United States
(44%), Europe (18%) Canada (16%), and South Africa (28%) but it gained momentum in India (40%),
Latin America (90%), Australia, and sub-Saharan Africa [5–9].
E. coli emerged as difficult-to-treat extended-spectrum betalactamase (ESBL) producers exhibiting
resistance to newer third-generation cephalosporins. In 2013, 17 European countries reported the
majority of E. coli isolates (85–100%) as ESBL-positive [6]. In the Asian region, 11 countries reported 28%
of the E. coli family as ESBL-positive (UTIs) followed by resistance to both third- and fourth-generation
cephalosporins [10]. Related to Enterobacteriaceae, five countries of Europe reported having increased
incidence of Carbapenem-resistant Enterobacteriaceae (CRE) in 2013 [6], while in the United States,
11% of K. pneumoniae and 2% of E. coli were resistant to carbapenem [2].
The root cause of this problem is multifactorial and stems from the overuse of antibiotics,
inappropriate antibiotic prescribing and dispensing, extensive use in agriculture and veterinary sectors,
lack of new antibiotics, and weak regulatory barriers [11]. There is no denying that the problem of
antimicrobial resistance is burdening both the developed and developing regions, being further
aggravated by the nonprescription use of antibiotics [12–14]. Likewise, the problem of dispensing of
antibiotics without prescription is also observed in many regions, except for US, Canada, and Northern
Europe [13,15]. It is difficult to ascertain the comprehensive effect of antimicrobial resistance, but in
the middle- and lower-income regions judicious sale of antibiotics is always a question mark [16–28].
An amalgamation of program elements focused on attitude and behavior changes is vital to
achieve optimal health outcomes in a population. Antimicrobial stewardship (AMS) is an intervention
program directed to improve and sustain appropriate antibiotic use in the absence of antimicrobial
resistance and strengthen patient safety in a cost-effective manner [29]. The American Society of
Health System Pharmacists outlined pharmacists as appropriate antimicrobial stewards who can
responsibly acquire projected roles in antimicrobial stewardship programs and can exercise profound
influence through participatory action in infection prevention and control measures [30]. Precisely,
the successful execution and maintenance of this program depend on the knowledge and attitudes of
the pharmacists working in both hospital and community settings. Globally, community pharmacists
are well-documented to maintain reinforced care and services with customers and/or patients and,
thus, are in well-placed positions to implement interventions related to stewardship and medication
management in both minor and major conditions.
This scoping review focused on the perception and attitude of community pharmacists towards
antibiotic dispensing without prescription and the related factors and facilitators with most sought-after
antibiotics in different diseases. The review is also expected to highlight research gaps followed by
recommendations of interventions and health education.
(a) What are the perceptions of community pharmacists towards antibiotic dispensing?
(b) What are the attitudes of community pharmacists towards antibiotic dispensing?
(c) How frequently did community pharmacists sell antibiotics in community pharmacies?
(d) How often did customers demand antibiotics in community pharmacies?
(e) What is the suitability of antibiotics that were dispensed from community pharmacies?
3. Results
A total of 507 references were identified from the electronic searches of four databases after
duplicates were removed. A total of 478 identified studies were excluded based on the titles and
Pharmacy 2018, 6, 92 4 of 11
abstracts. From the 29 research articles retrieved for detailed examination 16 were excluded (Figure 1).
Pharmacy 2018, 6, x FOR PEER REVIEW 4 of 11
A total of 13 full-text articles were finally decided to be included in the review.
Figure 1. Quorum
Figure flow
1. Quorum chart.
flow chart.
3.1.3.1. Awareness
Awareness andand Perception
Perception towards
towards Antibiotic
Antibiotic Dispensing
Dispensing
In In general,
general, community
community pharmacists
pharmacists showed
showed appropriate
appropriate knowingness
knowingness andand perception
perception towards
towards
antibioticdispensing
antibiotic dispensingwithout
without prescription
prescription andandallall
identified this this
identified as growing public public
as growing health issue
health [16–
18,25,28].
issue This is followed
[16–18,25,28]. by diminished
This is followed efficacy efficacy
by diminished of antibiotics and treatment
of antibiotics failure [17]
and treatment leading
failure [17] to
increased
leading resistance
to increased [18]. According
resistance to DilliptoetDillip
[18]. According al., a large
et al., majority perceived
a large majority their outlets
perceived their as a place
outlets
as for the customers
a place to obtaintomedical
for the customers servicesservices
obtain medical and devices
and which
devicesmotivate them to dispense
which motivate antibiotics
them to dispense
to the customers
antibiotics [17]. The
to the customers research
[17]. evidence
The research from from
evidence SpainSpain
acknowledged
acknowledged patient gratification
patient gratificationover
potential
over potential AMR,
AMR, andand
preferred to dispense
preferred to dispenseantibiotics
antibioticsdespite their
despite proper
their perception
proper towards
perception towardsAMR
AMR[19].[19].
However,
However,most of the
most community
of the community pharmacists
pharmacistsagreed thatthat
agreed irrational antibiotics
irrational usage
antibiotics is one
usage is of
onethe
of main causes
the main of increased
causes antibiotic
of increased resistance,
antibiotic andand
resistance, thatthat
all healthcare professionals
all healthcare need
professionals to think
need to
rationally
think rationallyandand
stopstop
prescribing andand
prescribing dispensing
dispensingantibiotic excessively.
antibiotic excessively.
3.2.3.2.
Attitudes of Pharmacists
Attitudes towards
of Pharmacists Antibiotic
towards Dispensing
Antibiotic Dispensing
The
Theattitudes
attitudesof of
thethe
majority of of
majority thethe
pharmacists
pharmacistsdiddid
notnot
parallel with
parallel withtheir awareness
their awareness and and
perception
perceptionand, interestingly,
and, dispensing
interestingly, dispensing without
withoutmedical
medicalprescription
prescription(DAwMP)
(DAwMP) is an extensive
is an extensive
phenomenon
phenomenon seen in many
seen community
in many community settings [16–28].
settings There
[16–28]. is a plethora
There of facilitators
is a plethora that seem
of facilitators to
that seem
be to
involved in DAwMP and the most important ones are highlighted
be involved in DAwMP and the most important ones are highlighted below: below:
3.2.1. Patient/Customer
3.2.1. Demand
Patient/Customer Demand
The community
The community pharmacists
pharmacists putput
thethe
onus on on
onus customers/patients
customers/patients forfor
nonprescription
nonprescription dispensing
dispensing
irrespective of which strata of society they are from [16,17]. Community pharmacists also
irrespective of which strata of society they are from [16,17]. Community pharmacists also underlined underlined
that those
that patients
those who
patients whopreviously
previously benefitted
benefittedfrom
fromany antibiotic
any and
antibiotic considered
and considered it ait“panacea
a “panacea forfor
all”, or require it as “travel medicine”, or are not able to pay the consultation fees of the
all”, or require it as “travel medicine”, or are not able to pay the consultation fees of the doctors were doctors
were generally
generally moremore concerned
concerned in getting
in getting antibiotics
antibiotics [16,17,25,28].
[16,17,25,28]. A fewAalso
fewcited
alsoapprehensions
cited apprehensions
of losing
of losing their loyal clientele if not succumbing to the demands/requests of their
their loyal clientele if not succumbing to the demands/requests of their customers [17,18]. customers [17,18].
Complacency of patients was also reported in a couple of studies as the motivational factor to
dispense without prescription [19,25,28].
Pharmacy 2018, 6, 92 5 of 11
Complacency of patients was also reported in a couple of studies as the motivational factor to dispense
without prescription [19,25,28].
Study Participants
Study Type Conclusion
Author, Year, [Ref.] Study Site Aims/Objectives Study Findings
Study Tool Limitation
Sampling
Accredited drug dispensing outlet
Good knowledge but low
(ADDO) owners and dispensers; Exploring attitudes towards Positive influence of ADDO Program
implementation;
Qualitative; Tanga and Ruvuma; antibiotic dispensing; but absence of translation into practice;
Dillip, 2015, [17] Customer demand
In-depth interviews Tanzania Accreditation influence on Nongeneralizable sample
Profit margin;
purposive dispensing Social desirability bias
Habit to follow doctors’ prescriptions
interviews (7)
286 Community
Cross-sectional Positive relationship with DAwMP; Strong relationship with DAwMP;
pharmacists (CPs) Interpretation of knowledge
Zapata, 2014, [19] Self-administered Indifferent attitude, complacency; Nonresponse bias;
Spain and attitudes for DAwMP
questionnaire Insufficient knowledge Inappropriate validity criterion
Exhaustive sampling
OTC antibiotic sales-common practice;
Phenomenological qualitative; Frequent DAwMP;
Five CPs Exploring reasons—OTC Strict regulatory enforcement;
Gebretekle, 2016, [16] In-depth interviews Weak enforcement regulation;
Ethiopia antibiotics sales Educational campaigns;
Observation Customer demand, profit margin
Non-generalizable sample
Insufficient knowledge of legality;
Knowledgeable of consequences Ignorant of DAwMP as illegal
Cross-sectional; Exploring knowledge, of DAwMP Educational interventions;
189 CPs
Hadi, 2015, [18] Self-administered attitude, practices towards Patient unwillingness to Single study setting (Makkah);
Makkah, Saudi Arabia
questionnaire DAwMP consult doctors; Non-generalizable;
Unaffordability of doctors’ Social desirability bias
consultations
Unnecessary dispensing for sore throat
Assessing knowledge of viral and UTI;
Prospective design; 202 pharmacies Absence of abidance of national
Almaytah, 2015, [20] symptoms; Insufficient knowledge of duration
Five clinical scenarios (SPs) Jordan regulation
DAwMP of treatment;
Antibiotic dispensing refusal
Exploring the attitude for
Unnecessary dispensing for sore throat Though illegal DAwMP observed;
Prospective design; 197 pharmacies DAwMP;
Llor, 2009, [21] and acute bronchitis; Not confirmed whether community
Three clinical scenarios (SPs) Spain Quantifying the extent of
Recommended consultation pharmacist dispensing
DAwMP
Despite implementation of restriction
Huge and easy dispensing
Prospective design; 174 pharmacies Quantifying the extent of ciprofloxacin dispensed;
Plachouras, 2010, [22] Amoxicillin/clavulanate and
21 voluntary collaborators Greece DAwMP Educational strategies for pharmacists;
ciprofloxacin largely requested
Need of strong regulation enforcement
327 pharmacies DAwMP observed without patients’ DAwMP routinely observed;
Cross-sectional; Exploring DAwMP;
Abdulhak, 2011, [23] Saudi Arabia requests for sore throat and diarrhea; Requirement of stringent enforcement
SPs Exploring associated risks
Quasi-random Improper history-taking and compliance to regulations
Pharmacy 2018, 6, 92 7 of 11
Table 1. Cont.
Study Participants
Study Type Conclusion
Author, Year, [Ref.] Study Site Aims/Objectives Study Findings
Study Tool Limitation
Sampling
Investigating antibiotic
50 pharmacies Irrational antibiotic dispensing;
Cross-sectional; dispensing for (upper Noncompliance rational use of drug
Alabid, 2014, [27] Malaysia Polypharmacy;
SPs respiratory tract infections) concept (RUD) by WHO
Convenient Nonrepresentative sample
URTIs
Highly inappropriate treatment;
DAwMP with antimotility agents
Cross-sectional; 164 pharmacies Investigating treatment of Actual treatment under-dispensed;
Diwan, 2015, [24] and probiotics;
Simulated clients (SCs) India childhood diarrhea Not confirmed whether community
Actual treatment (oral rehydration salt)
pharmacist dispensing
Frequent DAwMP; Highly undesirable DAwMP;
Cross-sectional; 261 pharmacies Exploring frequency of
Shet, 2015, [26] Inappropriate management for URTI Not confirmed whether community
Two clinical scenarios (SPs) India DAwMP
and self-limiting illnesses pharmacist dispensing
Knowledgeable about rational Fair improvement chances;
Exploratory
dispensing and antibiotic resistance; Behavioral intention for
qualitative; 32 CPs Exploring the knowledge,
Roque, 2013, [25] Factors: Physicians and patients and expected change;
Semi-structured interviews Portugal perception and attitude
veterinary consumption for Non-generalizable sample;
(six focus groups)
antibiotic resistance Chances of bias in FGD
Frequent DAwMP-dental ailments Attitudes promotes DAwMP;
Cross-sectional;
770 CPs Evaluating DAwMP; and UTIs; Educational interventions;
Roque, 2015, [28] Self-administered
Portugal Attitude towards DAwMP Factors: Patient satisfaction, Nonresponse bias;
questionnaire
precaution, and fear for DAwMP Social desirability
Pharmacy 2018, 6, 92 8 of 11
4. Discussion
Based on the review undertaken, most of the community pharmacists presented appropriate
awareness towards AMR [16–23], but the majority reflected unacceptable attitudes towards
dispensing and preferred to perform DAwMP in minor ailments and self-limiting conditions [16–28].
The majority of the papers included in the review identified several enablers that promote
DAwMP, such as indifference on the part of pharmacists, fulfilment of the demands of
patients/clients/customers, external responsibility, and insufficient knowledge of the consumer
and/or patient [16–27]. The knowledge and awareness of pharmacists on disease management
was predictably outstanding [16,18] since they are considered experts with respect to medicines.
Additionally, the pharmacists need to be continually vigilant not only towards the development and
issues in healthcare for providing the best treatment to their customers, but also towards the preventive
measures that can intervene with the patient’s recovery, such as AMR. Inappropriate knowledge,
understanding, and awareness on AMR can increase unnecessary antibiotic dispensing [19], and further
worsen AMR. A steady knowledge and consistent understanding on the antibiotics and AMR among
the community pharmacists pave the way towards reduced AMR progression through improved
adherence towards antibiotic usage and reducing self-medication [18,34], and also channelize the
injudicious demands of antibiotics from the community pharmacy [16].
URTI, the most commonly reported case at primary care institutions, are mostly of viral
origin. In the current review the URTI scenarios used viral cough as the presented problem and
the community pharmacists always dispensed penicillin or penicillin plus penicillinase inhibitor
as the treatment [20,21,23,26,27]. The staggering fact is that in these cases community pharmacists
dispensed antibiotics. On the other hand, UTIs stem from bacterial infection more frequently in women.
Community pharmacists dispensed fluoroquinolones to their simulated patients/clients [20,21,23]
without proper history-taking. The importance of history-taking in community pharmacies cannot be
denied as this can help in evading common pitfalls, such as in the case of category C medicines,
like fluoroquinolones, which have teratogenic effects and must be dispensed with caution in
women [35]. We observed in our review that most of the pharmacists did not assess the simulated
patients (SPs) precisely and dispensed antibiotics as per their demand.
Otitis media is one such condition in which antibiotic intervention is generally not
recommended [36]. Nevertheless, the common action observed among community pharmacists
was to dispense amoxicillin/clavulanic acid and chloramphenicol [20,23]. For diarrhea, the nature of
the problem needs to be diagnosed based on patient’s history as its etiology is frequently attributed to
food poisoning and, therefore, antimotility agents are therapeutically effective. The frequent usage of
antibiotics in paediatric diarrhea can be a potential contributory factor to AMR [24].
The current review reported a liberal attitude of community pharmacists towards antibiotic
dispensing in all the simulated clinical scenarios. Especially in case of URTI, it was observed that
antibiotics were given mostly without emphasizing the demand from the SPs [20–23,26].
A recently published commentary pinned high hopes on community pharmacists and positioned
them as antibiotic stewards in upper respiratory tract infections [37]. Likewise, both the studies from
Portugal [25,28] highlighted that attitudes of community pharmacists towards DAwMP are driven by
patient-related factors and educational interventions directed towards improved patient–pharmacist
interactive sessions are needed for exercising appropriate and rational use of antibiotics.
Unlike the current scoping review, the systematic review by McCullough et al. [38] focused mainly
on clinicians and reported that clinicians considered antimicrobial resistance a thought-provoking
matter, but the responsibility mainly lies on patients or other healthcare providers.
5. Conclusions
The majority of the community pharmacists reflected necessary knowledge and appropriate
perceptions toward antibiotic dispensing and resistance. The majority acknowledged that antimicrobial
resistance is the culmination of injudicious and excessive antibiotic dispensing and irrational usage.
Pharmacy 2018, 6, 92 9 of 11
However, antibiotics are still dispensed freely in a community setting and, thus galvanizing widespread
antibiotic resistance. The authorities should reflect intensified mindfulness towards this problem by
strengthening the implementation of current regulations, followed by brainstorming new alternatives
to curb this menace.
Finally, community pharmacists can work as collaborators between the prescribers and patients,
educating patients on ‘where’, ‘when’, and ‘how’ to use antibiotics effectively, as well as to remind
prescribers to follow guidelines, and furnishing them with up-to-date information about different
therapeutic categories. Mass media campaigns voiced over by community pharmacists on the disposal
of unused antibiotics can be one such future strategy which needs to be implemented soon in lower-
and middle-income countries.
Author Contributions: All authors have significantly contributed to this review. Author F.P. conducted the initial
search, identification, screening, and tabulation, analyzed the articles, and completed the first draft. S.J. searched
and provided related articles, provided the framework for writing the review, and strengthened the whole review
until the final phase. All of the authors analyzed the articles and endorsed the inclusion of relevant studies. All the
authors contributed to the final draft and the checking and reviewing of the manuscript.
Funding: This work is under the grant EDW B13-086-0971.
Acknowledgments: This review was supported by the Research Management Centre, International Islamic
University Malaysia (IIUM) (project no. EDW B13-086-0971).
Conflicts of Interest: The authors declare no conflicts of interest.
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