Journal Pre-proof

Perception and Practice of Community Pharmacist towards

Antimicrobial Stewardship in Lahore, Pakistan

Zunaira Akbar , Zikria Saleem , Arooj Shaukat ,

Muhammad Junaid Farrukh

PII: S2213-7165(21)00079-5
DOI: https://doi.org/10.1016/j.jgar.2021.03.013
Reference: JGAR 1529

To appear in: Journal of Global Antimicrobial Resistance

Received date: 13 November 2020

Revised date: 2 February 2021
Accepted date: 2 March 2021

Please cite this article as: Zunaira Akbar , Zikria Saleem , Arooj Shaukat ,
Muhammad Junaid Farrukh , Perception and Practice of Community Pharmacist towards Antimi-
crobial Stewardship in Lahore, Pakistan, Journal of Global Antimicrobial Resistance (2021), doi:
https://doi.org/10.1016/j.jgar.2021.03.013

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 1 Perception and Practice of Community Pharmacist towards Antimicrobial Stewardship in Lahore, Pakistan

2 Zunaira Akbara,*, Zunaira.akbar@hotmail.com, Zikria Saleemb, xikria@gmail.com, Arooj Shaukatc, aroojshaukat1@gmail.com,

3 Muhammad Junaid Farrukhd, junaid@ucsiuniversity.edu.my

4
a
5 Riphah Institute of Pharmaceutical Sciences, Riphah International University, Lahore, Pakistan
b
6 Faculty of Pharmacy, The University of Lahore, Pakistan
c
7 Fatima Jinnah Medical University, Lahore, Pakistan
d
8 Department of Clinical Pharmacy, Faculty of Pharmaceutical Sciences, UCSI University Kuala Lumpur, Malaysia

9
*
10 Corresponding Author

11

12

13 Abstract

14 Study Objective: Antimicrobial resistance (AMR) is a major health concern worldwide. To rationalize antibiotic use, community
15 pharmacist plays an important role. This study aimed to evaluate the perceptions and practices of community pharmacists regarding
16 antimicrobial stewardship (AMS) in Lahore, Pakistan.

17 Method: A descriptive cross-sectional study was conducted among community pharmacists in Lahore, Pakistan from November 1,
18 2017, to December 31, 2017. A self-administered questionnaire was used for data collection. Nonprobability convenient sampling was
19 done to select community pharmacies. Descriptive statistics were applied and Mann–Whitney U tests and Kruskal–Wallis tests were
20 performed to compare independent groups by using SPSS version 20.0.P-value less than0.05 was considered statistically significant.

1
21 Perception and practice scores were determined to access community pharmacist knowledge regarding antimicrobial stewardship. The
22 score of 0.5-1 was considered to be very good.

23 Results:The overall response rate was 71 %. Gender, age, work experience and education level did not significantly influence the
24 perception and practices of the community pharmacist. Experienced pharmacist showed better response towards antibiotic
25 stewardship. Majority of the pharmacists strongly agreed that they educate patients on the use of antimicrobial and resistance-related
26 issues.

27 Conclusion: It was concluded that community pharmacists in Lahore, Pakistan, have good perception regarding AMS and they are
28 practicing it well. But there are few gaps in their practices that must be filled such as dispensing without prescription and dispensing
29 for duration more than prescribed. In addition, there should be strict implantation of guidelines for dispensing antibiotics in order to
30 rationalize antibiotic use and decreasing antibiotic resistance.

31 Keywords

32 Antimicrobial stewardship (AMS), Community Pharmacist, Perception, Practice, Antimicrobial Resistance, Pakistan

33 Introduction

34 Antimicrobial resistance (AMR) is an undeniably general medical problem which can be reduced by using antimicrobial agents only
35 when necessary (1).AMR prolongs hospital stay and increases morbidity and mortality rate, thus increases the burden on the health
36 care system (2).Antimicrobial stewardship program (ASP) plans to improve patient outcomes while limiting unintended outcomes, for
37 example, generating untoward impacts of the resistant organism on the individual patient (3, 4)..Implementation of ASP reduces the
38 emergence and transmission of antimicrobial-resistant pathogens (3, 5, 6).The emergence of new infections made antibiotic regimen
39 more complex thus increases the pharmacist role in combating and preventing infection. Moreover, the sale of medicines at
40 community pharmacies without prescription is a very important factor that mainly depends upon personal traits and polices of the
41 country. The study conducted in Karachi, Pakistan showed that almost 15.2 % antibiotics are dispensed without prescription which
42 results in increased resistance due to self-medication (7).Antibiotic self-medication, particularly for upper respiratory tract infection
43 (URTI), is a major health concern because of increased resistance. A study conducted in universities of Lahore showed that 62% of
44 antibiotics are used without prescriptions in URTI(8). Pharmacist-directed antimicrobial stewardship programs have increased over

2
45 the past decade(9, 10).Community pharmacists can play a crucial role in the development and execution of AMS programs in
46 community settings.

47 The aim of this study was to assess pharmacists’ knowledge about antibiotics and their perceptions and practices regarding AMS in
48 community pharmacy settings.

49 Method

50 Study design

51 This descriptive, cross-sectional study was done to investigate the perception and practice of community pharmacists towards
52 antimicrobial stewardship program. Registered pharmacists working at community pharmacies of Lahore were included in this study.

53 Study population and sampling method

54 Nonprobability convenient sampling was done for selection of community pharmacists in Lahore. Lahore is Pakistan’s second most
55 populated &wealthiest city with an estimated GDP of $58.14 billion as of 2015. For the provision of health care services, many
56 community pharmacies are established and working in Lahore.They are involved in patient counseling on prescribed medicines,
57 promoting rational use of antibiotics, guiding patients regarding immunization schedules and control of serious communicable
58 diseases like Tuberculosis, AIDS, hepatitis, and polio. They also provide online services like home-delivery of medicines, drug
59 information, vaccines and guide patients about nutrition intake according to requirement and disease. These pharmacies also promote
60 health education through pamphlets and advertisements.

61 Sample size and data collection

62 A total of 141 registered community pharmacists were approached in a period of 2 months (November 1, 2017, to December 31, 2017)
63 for the data collection. Out of 141, only 100 pharmacists responded completely giving a response rate of 71%.

64 Survey items

65 Available literature was reviewed to design a data collection tool (11-13).Initially, the questionnaire was subjected to content and face
66 validity. The content was evaluated by the opinions of two experts and necessary changes were made. A pilot study was then done by
3
67 including 15 community pharmacists in order to reduce ambiguities in the questionnaire. The recommended changes were
68 incorporated. The reliability of the questionnaire was assessed by determining Cronbach’s α which was 0.65 for perception and 0.56
69 for practice. The final questionnaire contained three sections: The first section had 4 questions on the demographic history of
70 participants, the second section had 10 questions about the perception of community pharmacist about antimicrobial stewardship, and
71 the third portion had 11 questions about the practice of community pharmacists towards the antimicrobial stewardship. A 5 point
72 Likert scale was used for scoring statements regarding the perception and practice of community pharmacists. Point 1 was used for
73 strongly disagree, point 2 for disagree, point 3 for neutral, point 4 for agree and point 5 for strongly disagree. Overall scoring for
74 perception and practice was done in such a way that 0.5–1 was assigned “very good”, 1.5–2 “good”,2.5–3 “acceptable”, 3.5–4 “poor”,
75 and 4.5–5 “very poor”. Data were collected by using this supervised self-administered questionnaire (14).

76 Ethical approval

77 The study was approved from the research ethical committee of Riphah Institute of Pharmaceutical Sciences with reference number
78 REC/RIPS-LHR/2017/10.

79 Consent for Participation and Publication

80 Verbal consent was taken from the participants. They were informed about the purpose of study. Research ethical committee of
81 Riphah institute of Pharmaceutical sciences approved this consent because it was knowledge based study and did not involve any
82 participant’s personal/identifying information.

83 Data analysis

84 Data were entered and analyzed using SPSS version 20. Descriptive statistics (Frequencies, percentages, and medians) were used to
85 analyze data. Independent-sample Mann–Whitney U tests were employed to assess differences in perception and practices regarding
86 AMS between gender and education level. Independent-sample Kruskal–Wallis tests were used to check differences among age
87 groups and experience of the community pharmacists with regard to perceptions and practices regarding AMS. P<0.05 was used for
88 statistical significance of differences.

89 Results

4
 90 Out of 100 respondents, the majority were male pharmacist (57%), aged between 26-35 years (51%), qualification Pharm.d (77%) and
91 working experience of most of the pharmacists were less than 1year (43%) as shown in Table 1.

92 A large number of participants strongly agree that they keep in mind side effects while dispensing antibiotics, experienced pharmacist
93 show more response towards AMS and continued educational activities are required to enhance the understanding of antimicrobial
94 stewardship that indicates very good perception of Community pharmacist towards AMS (Median score

95 =1) shown in table 2.

96 When practices of community pharmacist were evaluated, Majority showed positive response when patients enquire about antibiotic
97 use, do not dispense antibiotics without prescription and also educate patients about antibiotic resistance related issues thus focuses on
98 the importance of antibiotic treatment course. Overall, community pharmacists showed good practices (Median xscore=2) shown in
99 table 3.

100 Gender, age, qualification and experience of the participants did not significantly affected their median scores with respect to their
101 perceptions. Median scores of participants about their perceptions and practices of antimicrobial stewardship are tabularized in Table
102 4.

103 Discussion

104 The rational use of antibiotics is essential for controlling infectious diseases. The rate of antibiotic resistance is high where antibiotics
105 are sold without prescription. The nonprescription use of antibiotic is associated with the inappropriate drug, dose, and duration of
106 treatment (15, 16).Many factors are associated with the dispensing of antibiotics without prescription such as less knowledge of
107 pharmacist, customers pressure and business oriented pharmacies (17). Therefore, there is a need to enhance the pharmacist
108 knowledge regarding rational use of drugs so that Pharmacists can play an important role in AMS and infection control program. This
109 study evaluated the perception and practices of community pharmacist towards AMS. Overall, the response rate was 71%. The current
110 study highlighted that community Pharmacists have good perceptions regarding antimicrobial use (perception score 1) and practicing
111 AMS (practice score 2) as well in Lahore, Pakistan. Participants were familiar with the importance of antimicrobial stewardship as the
112 majority agreed that it decreases the emergence of resistance thus improves patient care. Similar findings were reported previously in
113 Malaysia (14). Antibiotics are prescribed inappropriately and AMS can effectively change prescribing patterns of antibiotics resulting
114 in improved patient care(18).
5
115 In our study, gender, qualification, experience and age did not significantly influence the perception and practice of community
116 pharmacist regarding the rational use of antibiotics. The findings were different from previous literature (11). Majority of the
117 pharmacist had an opinion that antibiotics are more used in elderly patients as compared to adults. This may be due to the fact that
118 elderly patients are more prone to infections because of age-related change in physiological processes (19).

119 Majority of the community pharmacist consider their responsibility to guide patients on antibiotic use because pharmacists are
120 involved in processing medication orders (20). Patient counselling during dispensing not only decreases medication errors but also
121 improve patient adherence and make them more compliant towards the regimen (21). A large number of pharmacists strongly agree
122 that AMS should be introduced at the community level. Sufficient education should be provided to community pharmacist on AMS;
123 for that purpose, conference and workshops should be arranged in order to enhance understanding of AMS thus promoting rational use
124 of antibiotics. Pharmacist being the part of the health care team can effectively promote rational use of antibiotics and there is great
125 evidence that AMS should be inculcated at the community level. This will definitely decrease antibiotic resistance (22).In this study,
126 the majority of community pharmacist strongly agree that 60% of population self-medicate with antibiotics which is the major reason
127 for developing antibiotic resistance. Overuse or misuse of antibiotics causes poor control of infection as pathogens become immune
128 against antibiotic (23). Community pharmacies are the main source of antibiotics, although most of these drugs are prescription only
129 medicines. Implementing strong prescription policies and law enforcement can minimize self medication and ultimately reduces
130 antibacterial resistance (15).

131 The results indicated that community pharmacist shows positive response if any patient asks a question about antibiotic use. Almost
132 half of the respondents disagree that they dispense antibiotics without a prescription. The results were encouraging because their
133 positive attitudes make them more confident in appropriate dispensing of antibiotics. This finding was different from the study
134 conducted in Malaysia, Saudia, and China where majority pharmacist dispense antibiotics without prescription because of their
135 business requirement (11, 24, 25). Majority pharmacists were strongly agreed that they do recommend medicines other than antibiotics
136 for the minor ailment because people prefer to ask the pharmacist about medicine for their minor problems rather than visiting
137 hospitals or clinics. Pharmacist because of having clinical expertise can recommend therapies for minor ailments. By Implementing
138 pharmaceutical care at community level, Pharmacist are in better position to provide a primary care for minor ailment (15). Majority
139 of pharmacist strongly agreed that they screen antibiotics prescription with local guidelines and take history from the patient about
140 previous allergies in order to prevent irrational prescribing and minimize the chances of adverse drug reactions. They also
141 communicate with prescribers if they are unsure about the appropriateness of antibiotic prescriptions. This will also decrease the

6
142 emergence of antibiotic resistance. The findings were different from the study conducted previously that stated gap in communication
143 is also the major reason for irrational antibiotic use (14). A large proportion of pharmacist stated that they do not dispense antibiotic
144 for a duration more than that is prescribed, however, few agreed that dispense antibiotic for a longer duration. Previous studies showed
145 that prolonged antibiotic duration serves as a mean of antibiotic resistance (26). Many of the pharmacists stated that they follow the
146 guidelines for dispensing antibiotics but still there is a need for strict implementation of guidelines for dispensing antibiotics. Majority
147 of the pharmacist strongly agreed that they ask for the patient’s age, possible allergies and purpose of medicine prior to dispensing
148 thus rationalizing the use of antibiotics. At present, there is no well-established AMS program but community pharmacists of Lahore
149 are well aware of the AMS program and its purpose. Thus there is a need for stabling effective AMS programs at the community level
150 in to promote rational use of antibiotics.

151 Conclusion

152 It is concluded that Community Pharmacist in Lahore, Pakistan have good perception regarding AMS and they are practicing it well.
153 But there are few gaps in their practices that must be filled such dispensing without a prescription and dispensing for duration more
154 than prescribed. In addition, there should be strict implantation of guidelines for dispensing antibiotics in order to rationalize antibiotic
155 use and decreasing antibiotic resistance.

156 Competing interest

157 The authors declare that they have no competing interests.

158 Funding

159 No funding support was acquired for this study.

160 Contributor ship

161 Zikria Saleem designed and supervised the project and applied statistical methods to analyze the data. Zunaira Akbar wrote the
162 manuscript. Arooj Shaukat collected data. Muhammad Junaid Farrukh reviewed the manuscript.

163 Data sharing statement

7
164 No additional data

165 Acknowledgment

166 The authors would like to thank Riphah Institute of Pharmaceutical Sciences, Riphah International University, Township campus,
167 Lahore, Pakistan for their support.

168 References

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219 26. Nasrin D. Effect of β-lactam antibiotic use in children on pneumococcal resistance to penicillin: morospective cohort study. British
220 Medical Jounal. 2002;5:324-8.

221

222

223

224

225

226 Table 1. Participants Characteristics

Variable Frequency n=100 Percentage %

Gender

Male 57 57

Female 43 43

Age(years)

10
 <25 40 40

26-35 52 52

36-45 6 6

>45 2 2

Qualification

Pharm D 77 77

M.Phil 23 23

Experience ( years)

<1year 43 43

1-3 38 38

4-6 10 10

>6 9 9

227

228

229 Table 2. Perception of Pharmacists towards Antimicrobial Stewardships

Participants Responses* Variables

Statements SA A N DA SD Median Gender Age Qualification Experience
(IQR)
11
Do you keep in 62(60.8) 30(29.4) 4(3.9) 3(2.9) 1(1.0) 1(1) NS 0.057 NS NS
mind the side
effects while
dispensing
antibiotics?
Do you think the 26(25.5) 50(49.0) 23(22.5) 1(1) 33(32.4) 2(1) NS NS NS NS
use of
antimicrobials is
more common in
aged persons than
younger?
Do you think 28(27.5) 33(32.4) 14(13.7) 21(20.6) 4(3.9) 2(3) 0.057 NS NS NS
guidance about
antimicrobial agents
is the only
responsibility of a
pharmacist?
Does experienced 54(52.9) 36(35.3) 7(6.9) 2(2) 1(1) 1(1) NS NS 0.001 NS
pharmacist show
more response
towards antibiotic
stewardship?
Do you think 56(54.9) 38(37.3) 5(4.9) 1(1.0) 0(0) 1(1) NS NS NS NS
antimicrobial
stewardship should
be introduced at
community

12
pharmacy level?

Do you feel proud 69(67.6) 25(24.5) 6(5.9) 0(0) 0(0) 1(1) NS NS NS NS

while giving
information about
the use of
antibiotics?
Does guidance 45(44.1) 39(38.2) 10(9.8) 4(3.9) 2(2) 2(1) NS NS NS 0.031
about antibiotic use
decreases the
percentage of
resistance in
patients?
Does sufficient 60(58.8) 32(31.4) 6(5.9) 2(2) 0(0) 1(1) NS NS NS NS
education on
antimicrobial
stewardship should
be given to
community
pharmacists?
Do you think, about 44(43.1) 40(39.2) 10(9.8) 5(4.9) 1(1) 2(1) NS NS NS NS
60% of people use
antimicrobials as
self-medication(in
case of minor
infections)?
Does relevant 63(61.8) 28(27.5) 7(6.9) 1(1) 1(1) 1(1) NS NS NS NS
conferences,
13
 workshops and
other education
activity are required
to enhance the
understanding of
antimicrobial
stewardship?
Perception score 1.0(1)
overall
230 *SD = Strongly Disagree, D = Disagree, N=Neutral, A = Agree, SA = Strongly Agree. Note: Perception was assessed by giving 1 to
231 SD, 2 to D, 3 to N, 4 to A, 5 to SA, NS=non significant
232

233

234

235 Table 3.Practice of community pharmacists towards antimicrobial stewardships

Participants Responses* Variables

Statements SA A N DA SD Median Gender Age Qualification Experience
(IQR)
Do you show a 60(58.8) 37(36.3) 2(2) 1(1) 0(0) 1(1) NS NS NS NS
positive response
if someone asks a
question about
antibiotic use?
Do you dispense 9(8.8) 25(24.5) 17(16.4) 16(15.7) 33(32.4) 3(3) 0.045 0.029 NS NS

14
antimicrobials
without
prescription?
Do you dispense 47(46.1) 34(33.3) 13(12.7) 5(4.9) 1(1) 1(1) NS NS NS NS
antimicrobial on
prescription with
complete clinical
information?
Do you 36(35.3) 46(45.1) 11(10.8) 7(6.9) 0(0) 2(1) NS NS NS NS
recommend
therapies other
than
antimicrobials for
minor ailments?
Do you educate 56(54.9) 38(37.3) 6(5.9) 0(0) 0(0) 1(1) NS NS NS NS
patients on use of
antimicrobial and
resistance related
issues?
Before 19(18.6) 55(53.9) 18(17.6) 6(5.9) 2(2) 2(1) NS NS NS NS
dispensing, do
you screen the
antimicrobial
prescription with
local guidelines?
Do you 38(37.3) 38(37.3) 12(11.8) 10(9.8) 2(2) 2(1) NS NS NS NS
communicate
15
with prescribers
if you are unsure
about the
appropriateness
of an antibiotic
prescription?
Do you dispense 5(4.9) 34(33.3) 17(16.7) 20(19.6) 24(23.5) 3(2) NS NS NS NS
antimicrobials for
duration more
than prescribed
by a physician on
patient’s request?
Do you know 24(23.5) 60(58.8) 13(12.7) 3(2.9) 0(0) 2(0) NS NS NS NS
how to handle a
patient who
demands
antimicrobial
therapy that is not
indicated?
While dispensing 51(50) 39(39.2) 5(4.9) 4(3.9) 1(1) 1(1) NS NS NS NS
antibiotics, do
you ask for the
age, possible
allergies and
purpose of
medicines from
the patient?

16
 Do you 40(39.2) 38(37.3) 15(14.7) 6(5.9) 1(1) 2(1) 0.026 NS NS NS
participate in
communication
with prescriber
for antimicrobial?
Practice score 2(1)
overall
236 *SD = strongly Disagree, D = Disagree, N=Neutral, A = Agree, SA = Strongly Agree. Note: Practice was assessed by giving 1 to SD,
237 2 to D, 3 to N, 4 to A, 5 to SA, NS=non significant.
238

239

240

241

242

243 Table 4: Median Score of Participants about their perception and practice of antimicrobial stewardship

Variable Perception Rank p value Practice Rank p value

Score Score
(Median) (Median)

Gender*

Male 1.6 54.21 0.111 1.7 52.32 0.418

Female 1.4 45.58 1.6 48.08

17
 Age (years)**

<25 1.6 53.91 1.7 53.18

25-35 1.4 47.76 0.746 1.5 48.02 0.709

36-45 1.6 52.25 2 56.58

>45 1.5 48.25 1.5 43.25

Qualification*

Pharm D 1.7 49.77 0.617 1.6 49.91 0.677

M.Phil 1.5 52.96 1.7 52.48

Experience
(years)**

<1
1.6 51.65 1.6 47.62
1-3
1.4 48.28 0.802 1.7 51.00 0.704
4-6
1.5 47.95 1.9 55.90
>6
1.6 57.22 1.7 56.17

244 *Mann Whitney Test

245 ** Kruskal Wallis Test

246

18