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antibiotics
Article
How Are We Educating Future Physicians and Pharmacists in
Pakistan? A Survey of the Medical and Pharmacy Student’s
Perception on Learning and Preparedness to Assume Future
Roles in Antibiotic Use and Resistance
Naeem Mubarak 1, * , Sara Arif 2, Mahnoor Irshad 1, Rana Muhammad Aqeel 1, Ayesha Khalid 1,
Umm e Barirah Ijaz 1, Khalid Mahmood 3, Shazia Jamshed 4, * , Che Suraya Zin 5, * and Nasira Saif-ur-Rehman 1
Citation: Mubarak, N.; Arif, S.;
Irshad, M.; Aqeel, R.M.; Khalid, A.;
Ijaz, U.e.B.; Mahmood, K.; Jamshed,
S.; Zin, C.S.; Saif-ur-Rehman, N. How
Are We Educating Future Physicians
and Pharmacists in Pakistan? A
Survey of the Medical and Pharmacy
Student’s Perception on Learning and
Preparedness to Assume Future Roles
in Antibiotic Use and Resistance.
Antibiotics 2021,10, 1204. https://
doi.org/10.3390/antibiotics10101204
Academic Editors: Xiaolin Wei,
Rebecca King and Leonardo Pagani
Received: 29 August 2021
Accepted: 30 September 2021
Published: 3 October 2021
Publisher’s Note: MDPI stays neutral
with regard to jurisdictional claims in
published maps and institutional affil-
iations.
Copyright: © 2021 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
1Lahore Medical & Dental College, University of Health Sciences, Lahore 54600, Pakistan;
mahnoorirshad6901@gmail.com (M.I.); ranaaqeel1996@gmail.com (R.M.A.);
ayeshakhalid294@gmail.com (A.K.); bariraaijazz@gmail.com (U.eB.I.); dean.lpc@lmdc.edu.pk (N.S.-u.-R.)
2Jinnah Burn and Reconstructive Surgery Center, Allama Iqbal Medical College, Lahore 54000, Pakistan;
saraarif@jbrsc-aimc.edu.pk
3
Institute of Information Management, University of the Punjab, Lahore 54000, Pakistan; khalid.im@pu.edu.pk
4Department of Clinical Pharmacy and Practice, Faculty of Pharmacy, Universiti Sultan Zainal Abidin,
Terengganu 22200, Malaysia
5Kulliyyah of Pharmacy, International Islamic University Malaysia, Kuantan 25200, Malaysia
*Correspondence: naeem.mubarak@lmdc.edu.pk (N.M.); shaziajamshed@unisza.edu.my (S.J.);
chesuraya@iium.edu.my (C.S.Z.)
Abstract:
Background: Medical and pharmacy students are future healthcare professionals who
will be on the forefront in dealing with antibiotics in hospitals or community settings. Whether
the current medical and pharmacy education in Pakistan prepares students to take future roles in
antibiotic use remains an under-researched area. Aim: This study aims to compare medical and
pharmacy students’ perceived preparedness, learning practices and usefulness of the education
and training on antibiotic use and resistance imparted during undergraduate studies in Pakistan.
Design and Setting: It was amulti-centre cross-sectional survey of medical and pharmacy colleges
in Punjab, Pakistan. Method: A self-administered questionnaire was used to collect data from final
year medical and pharmacy students. Descriptive statistics were used for categorical variables while
independent t-test and One-way ANOVA computed group differences. Result: Nine hundred forty-
eight respondents (526 medical and 422 pharmacy students) completed the survey from 26 medical
and 19 pharmacy colleges. Majority (76.1%) of the pharmacy students had not completed a clinical
rotation in infectious diseases. The top three most often used sources of learning antibiotic use
and resistance were the same among the medical and the pharmacy students; included textbooks,
Wikipedia, and smart phone apps. Overall self-perceived preparedness scores showed no significant
difference between pharmacy and medical students.. The least prepared areas by medical and
pharmacy students included transition from intravenous to oral antibiotics and interpretation of
antibiograms. Both medical and pharmacy students found problem solving sessions attended by a
small group of students to be the most useful (very useful) teaching methodology to learn antibiotic
use and resistance. Conclusions: Differences exist between medical and pharmacy students in
educational resources used, topics covered during undergraduate degree. To curb the growing
antibiotic misuse and resistance, the concerned authorities should undertake targeted educational
reforms to ensure that future physicians and pharmacists can play a pivotal role in rationalizing the
use of antibiotics.
Keywords:
antibiotic resistance; pharmacy education; medical education; educational policy; antibi-
otic use; Pakistan
Antibiotics 2021,10, 1204. https://doi.org/10.3390/antibiotics10101204 https://www.mdpi.com/journal/antibiotics
Antibiotics 2021,10, 1204 2 of 14
1. Background
Antibiotic resistance—the capability of bacteria to surpass the effects of antibiotics—
has emerged as one of the top ten challenges of 21st century. It means the resource pool of
antibiotics will lose its effectiveness leading to its partial or complete depletion. Nowadays,
antibiotic resistance (ABR) is termed a “tragedy of commons” because of the irreversible
fallouts on society including incurable or long-standing common infections and significant
rise in mortality, healthcare cost and hospital stays [1].
A growing body of evidence warns of the dramatic spread of ABR in low- and
middle-income countries (LMICs) in the Asian region [
2
]. One of the established reasons
behind this continuous surge in bacterial resistance is pervasive misuse of antibiotics
in hospitals and community settings in Asia. This misuse of antibiotics emanates from
fallacies in the choice of antibiotic, posology, route of administration, duration of therapy,
over prescribing and unauthorized sale of antibiotics [
2
,
3
]. Multiple factors cause the
malpractices of overprescribing and sale of antibiotics without prescription; however,
inadequate knowledge and training of health care professionals have been dubbed as the
fons et origo of the two malpractices [3].
The World Health Organization’s Global Action Plan emphasizes the education and
training of the prescriber and other healthcare professionals as one of five priority interven-
tions to clampdown growing bacterial resistance and optimize the use of antibiotics [
4
].
Education of healthcare professionals is a continuous process, however, the undergraduate
level of medical, pharmacy or any other allied health discipline is the first step to acquire
related knowledge and build a strong foundation for any further specialty [
5
]. Notably,
medical and pharmacy students are future healthcare professionals who will be dealing
with antibiotics in hospitals, primary care and community settings. On one hand, medical
students will be the future prescribers, and on the other hand, pharmacy students will
advise on the rational use of antibiotics in hospitals at the conveniently accessible location
of a community pharmacy somewhere [
6
,
7
]. Hence, future management of the challenges
associated with bacterial resistance or misuse of antibiotics depends upon the quality of
education, training and skills learnt at an undergraduate level and this accentuates the
pivotal value of undergraduate studies for the upcoming years. Nevertheless, during early
education of health care professionals, different countries deploy different pedagogical
approaches to teach optimal antibiotic use [7].
Pakistan, an LMIC in South Asia, is an important region for interventions to reduce the
growing ABR owing to its huge population of 216 million inhabitants [
8
]. Officially, there
are 62 medical colleges (19 public, 43 private) in Punjab and Islamabad [
9
]. The Pakistan
Medical Commission (PMC), formerly known as Pakistan Medical & Dental Council, and
the Higher Education Commission (HEC), are the regulatory bodies with a mandate to
set and implement a uniform curriculum for the five-year degree program Bachelor of
Medicine and Bachelor of Surgery (MBBS), as well as accrediting medical colleges across the
country. Meanwhile, The Pharmacy Council of Pakistan (PCP) accredits pharmacy colleges,
registers pharmacists, and sets standards of pharmacy education and training across the
country. A five-year curriculum, developed and approved by the HEC in consultation with
PCP, leads to the degree of Doctor of Pharmacy (Pharm D). At the moment, 49 pharmacy
colleges (10 public, 39 private) are approved by the PCP to offer a Pharm D degree program
in Punjab [10].
Studies have warned of pervasive overprescribing by physicians in hospitals and the
sale of antibiotics without prescription in community settings in Pakistan [
11
]. Significant
gaps exist in the continuous education of healthcare professionals on optimal antibiotic
use and growing resistance in tertiary care hospitals [
8
,
12
]. Whether these gaps originate
from a lack of training and education at the beginning (during the undergraduate degree
program, such as MBBS or Pharm D) or during professional practices, remains a debatable
issue. Meanwhile, different studies report sub-optimal knowledge on the part of pharmacy
and medical students regarding antibiotics use, resistance, and stewardship [
13
]. Despite
antibiotic resistance being a significant threat in Pakistan, few studies have shed light on the
Antibiotics 2021,10, 1204 3 of 14
nature of the contents of the training and education that students have undergone during
MBBS and Pharm D degrees in Pakistan. Nevertheless, hardly any study has evaluated and
compared preparedness or perception of the quality of medical and pharmacy education
and training. Thus, an in-depth analysis of the quality of training and education at an
undergraduate level is notably absent. A greater understanding is required about how the
principals of appropriate antibiotics use are taught, at which level students are introduced
to these concepts, and whether teaching made students confident enough to translate these
concepts into practice. Therefore, this study aims to understand the perception of medical
and pharmacy students about their education and training imparted during undergraduate
studies on the appropriate antibiotic use and resistance in Pakistan. The findings of this
study will recognize current trends in academic practices in medical and pharmacy colleges
and may be used to urge action to improve future teaching practices and curriculum design
for pharmacy and medical undergraduate degree programs.
2. Methods
2.1. Study Design, Sample and Setting
A cross-sectional, multicentre survey was designed to collect data of final year MBBS
and Pharm D students in medical and pharmacy colleges in the province of Punjab and
Islamabad Capital Territory in Pakistan. Lists of the approved medical and pharmacy
colleges were obtained from the official websites of PMC and PCP respectively.
An online freely available software, Raosoft, calculated the sample size independently
for pharmacy (n= 257) and for medical (n= 373) with a 5% margin of error, 95% confidence
interval and assuming a maximum possible population of 20,000 for each discipline at a
response distribution of 50%.
2.2. Survey Instrument, Data Collection and Analysis
The survey instrument was adopted from the questionnaire used in a previous
study [14]. It was comprised of five sections in English language:
1.
Demographics of the respondent (e.g., sex, name of college, ownership of college,
previous training before the formal degree etc.).
2.
The topics covered related to responsible antibiotic use and resistance during the
undergraduate degree program.
3. The resources preferred by the students to learn about antibiotic use and resistance.
4.
Perceived usefulness of different teaching methods deployed to teach antibiotic use
and resistance.
5.
Perceived preparedness of the students to take future roles in antibiotic use and
resistance.
Researchers deployed four data collection teams, each one consisting of five Doctor of
Pharmacy (final year) students. We trained data collection teams for two days on topics,
such as aims of the study, items in the survey, possible queries, and ensuring completeness
of the questionnaire filled. Data were collected on paper, self-administered, over a period
of three months (17 October 2019, to 15 January 2020). After permission from the concerned
authorities in the participating colleges, data collectors were escorted to final year students.
Data collector teams first introduced the aims and objective of the study to students and
then distributed the survey. Data on paper were later exported in Statistical Package Social
Sciences SPSS (version 23 IBM, Armonk, NY, USA) for analysis. Categorical data were
reported using frequencies and percentages, while continuous variables were described
using mean and standard deviation. Student t-test was used to commute two group
differences while one way ANOVA was used to evaluate more than two group differences.
The rank order of different resources used by the students was computed based on the
mean score value where the higher the mean score was, higher the rank (‘1’ = the highest).
Antibiotics 2021,10, 1204 4 of 14
2.3. Inclusion and Exclusion Criteria
Final year enrolled students from any medical or pharmacy college in Punjab and
Islamabad were eligible to participate (subject to willingness) in the survey. Researchers
surveyed final year students of both professions because students in final year have mainly
completed all the subjects related to the topic of this study.
Non-final year students in medical and pharmacy disciplines were excluded because
they had not completed all the necessary subjects related to the topic of this study, hence,
their experience might lead to a bias. Recently accredited/approved medical or pharmacy
colleges were excluded because these colleges had initial classes and lacked final year
students. Finally, the study excluded medical and pharmacy colleges which were not
recognized by the PMC and PCP, respectively; because that indicated a lack of compliance
to the minimum set standards of education and training.
2.4. Ethics
Research Ethics Committee, Lahore Pharmacy College, Lahore Medical & Dental Col-
lege granted ethical approval to carry out this study (ref: ETH/LPC/15/07/19). Informed
consent was taken from the respective administrative head of the participating college,
after detailing them about the aims of the study and how the data would be used for
publication in later stages. The research team assured the anonymity of data and responses
during the publication process. For this purpose, the research team assigned individual
identification numbers to colleges. Afterwards, data were stored in a password-protected
computer.
3. Results
3.1. Demographic Data and Response Rate
A total of 948 respondents (526 medical and 422 pharmacy students) completed the
survey from twenty-six medical colleges (institutional response rate 76.5%) and nineteen
pharmacy colleges (institutional response rate. 70.40%). Based on the exclusion criteria,
20 pharmacy
and 4 medical colleges were excluded. The mean age of the respondents
was 23.3 years and majority of the respondents were females in both medical (53.2%)
and pharmacy colleges (63%). A vast majority (76.1%) of the pharmacy students had not
completed a clinical rotation in infectious diseases, compared with 57% of the medical
students who reported completion of a clinical rotation in infectious diseases. Detailed
demographics are provided in Supplementary file (Table S1).
3.2. Topics Covered on Responsible Antibiotic Use and Resistance
Disappointingly, a vast majority of the medical (83%) and pharmacy students (78%)
were not familiar with the term antimicrobial stewardship. Less than half of the students
in both disciplines had attended lectures on the rational use of antibiotics in general.
Compared with medical students, more pharmacy students acknowledged receiving formal
lectures on selection of the correct antibiotic dose and right duration of treatment for specific
infections and the difference was statistically significant. Table 1lists various topics covered
during the degree programs.
3.3. Educational Resources
Both medical and pharmacy students reported a variety of resources for learning
optimal antibiotic use and resistance. The top three most often used sources of learning
antibiotic use and resistance were the same among the medical and the pharmacy students
and included textbooks or study guides, followed by Wikipedia and smart phone apps.
However, there was a considerable variability in ranking of medical and pharmacy stu-
dents. For instance, peer learning was popular among medical students who ranked it the
fourth most often used resource, while pharmacy students ranked consultation with the
hospital/clinical pharmacist as the fourth most used source. Notably, neither pharmacy
nor medical students preferred any kind of infectious disease guidelines (ranked 14th, the
Antibiotics 2021,10, 1204 5 of 14
least consulted source) Table 2compares the rankings of different sources of learning by
medical and pharmacy students.
Table 1. Have you attended any formal lecture(s) that address the following topics during medical/pharmacy College?
Statements Status No
n(%)
Yes
n(%)
I don’t Remember
n(%)
χ2
(p-Value)
Rational use of antibiotics in general P 192 (45.5) 199 (47.2) 31 (7.3) 1.79
M 218 (41.4) 262 (49.8) 46 (8.7) (0.408)
When to start antibiotics P 112 (26.5) 265 (62.8) 45 (10.7) 3.51
M 169 (32.1) 306 (58.2) 51 (9.7) (0.173)
How to select the correct dosage? P 119 (28.2) 257 (60.9) 46 (10.9) 18.62
M 217 (41.3) 252 (47.9) 57 (10.8) (0.000) *
How to select the duration of
treatment for specific infections?
P 125 (29.6) 237 (56.2) 60 (14.2) 7.26
M 199 (37.8) 266 (50.6) 61 (11.6) (0.027) *
Are you familiar with the term
antimicrobial stewardship (AMS)?
P 331 (78.4) 37 (8.8) 54 (12.8) 9.03
M 437 (83.1) 52 (9.9) 37 (7.0) (0.011) *
n= number, % = percentage, χ2 = Chi-square test, P = pharmacy students, M = medical students. * p≤0.05 (significant difference).
Table 2. How do you use each of the following sources to learn about antimicrobials use and resistance?
Statements Medical Students Pharmacy Students t
Mean (SD) Rank Mean (SD) Rank (p-Value)
Textbooks or study guides 3.17 (0.95) 13.24 (0.89) 11.23
(0.221)
Wikipedia 3.01 (0.98) 23.07 (0.95) 30.19
(0.849)
iPhone or smartphone apps 2.94 (1.02) 33.02 (0.99) 22.13
(0.034) *
Peers (other students) 2.89 (1.05) 43.01 (0.91) 7−0.21 **
(0.833)
Others used often 2.89 (1.08) 42.96 (1.01) 60.01
(0.996)
Up to Date 2.87 (1.01) 52.89 (1.12) 51.38
(0.168)
Infectious Diseases specialists 2.86 (1.02) 62.87 (1.04) 70.20
(0.844)
Hospital/ clinical Pharmacists 2.76 (0.97) 72.87 (0.97) 44.13
(0.000) *
Medical Journals 2.67 (0.99) 82.86 (1.02) 92.39
(0.017) *
Other Guidelines by professional organizations 2.63 (1.00) 92.83 (0.99) 10 2.96
(0.003) *
Non-infectious diseases physicians 2.61 (0.97) 10 2.82 (0.98) 14 −1.58 **
(0.113)
Pharmaceutical representatives 2.58 (1.05) 11 2.68 (1.08) 84.02
(0.000) *
Johns Hopkins Antibiotic guide 2.57 (1.08) 12 2.59 (1.14) 12 0.24
(0.811)
Sanford guide 2.55 (1.08) 13 2.55 (1.14) 13 −0.02 **
(0.988)
Infectious Diseases Society of America Guidelines 2.53 (1.00) 14 2.50 (0.99) 11 2.20
(0.027) *
SD = standard deviation, t= independent t-test. * p
≤
0.05 (significant difference).** In statistics, a negative t-value elaborates that the
direction of the effect under study is being reversed; this value has no impact on the significance of difference between groups of data.
Pharmacy students’ rank was italicized to differentiate from the rank given by the medical students.
Antibiotics 2021,10, 1204 6 of 14
3.4. Perceived Usefulness of Teaching Methodology
Both medical and pharmacy students found problem solving sessions attended by a
small group of students as the most useful (very useful) teaching methodology to learn
antibiotic use and resistance, followed by the grand round’s lectures i.e., discussion of
clinical cases. Interestingly, classroom lectures were rated very useful by only 8.2% of
medical and 11.1% of pharmacy students and thus indicate a lack of effectiveness.
Table 3
contrasts the perceived usefulness of different teaching methods among the pharmacy
and medical students in Punjab, Pakistan. Furthermore, as a whole, only 19.8% medical
and 17.1% pharmacy students rated their education and training on appropriate use of
antibiotics as very useful (Figure 1).
3.5. Perceived Preparedness
The overall mean score on perceived preparedness was higher among pharmacy
students as compared to medical students; however, the difference was not statistically
significant (p= 0.15). Among the pharmacy students, based on the mean score, the top three
least prepared individual curriculum items included; interpretation of antibiograms (mean,
2.96, p= 0.48), followed by transition from intravenous to oral antibiotics (mean, 3.03,
p= 0.04
), and how to streamline or deescalate antibiotics therapy (mean, 3.09,
p= 0.03
) as
mentioned in Table 4. Whereas, among the medical students, the top three topics perceived
as least prepared included; lack of competency to decide the transition from intravenous to
oral antibiotics (mean score, 2.91, p= 0.04) followed by how to select the best antimicrobial
for a specific infection (mean, 2.94, p= 0.00), and how to interpret the antibiograms (mean,
3.02, p= 0.48) (Table 4). While, both medical and pharmacy students well understand the
basic mechanisms of antimicrobial resistance (mean, 3.44 and 3.56 respectively, p= 0.06).
Table 4presents a comparison of the preparedness of medical vs. pharmacy students on
various topics related to optimal antibiotic use.
Finally, results of analysis of variance reveal that public medical colleges were better
prepared as compared to private medical colleges and the difference was statistically
significant. Supplementary file (Table S2) offers comparison of the mean of four subgroups
in the sample.
Antibiotics 2021,10, 1204 7 of 14
Table 3. If made available to you, please rate the usefulness of each of the following options for learning about antimicrobial use and resistance?
Statements Status Not at all Useful
n(%)
Not Useful
n(%)
Neutral
n(%)
Useful
n(%)
Very Useful
n(%)
Median
(IQR)
Grand rounds lecture P 18 (4.3) 41 (9.7) 126 (29.9) 154 (36.5) 83 (19.7) 4 (1)
M 43 (8.2) 53 (10.1) 100 (19.0) 182 (34.6) 148 (28.1) 4 (2)
Classroom lectures P 28 (6.6) 206 (48.8) 85 (20.1) 56 (13.3) 47 (11.1) 2 (1)
M 45 (8.6) 227 (43.2) 21 (4.0) 190 (36.1) 43 (8.2) 2 (2)
Lecture series of medical and pharmacy students. P 29 (6.9) 34 (8.1) 116 (27.5) 161 (38.3) 82 (19.4) 4 (1)
M 39 (7.4) 75 (14.3) 182 (34.6) 154 (29.3) 76 (14.4) 3 (1)
Interactive patient oriented problem-solving modules on
the internet.
P 30 (7.1) 41 (9.7) 156 (37.0) 118 (28.0) 77 (18.2) 3 (1)
M 35 (6.7) 60 (11.4) 171 (32.5) 134 (25.5) 126 (24) 3 (1)
Interactive patient oriented problem-solving modules on
CD-ROM.
P 38 (9.0) 46 (10.9) 138 (32.7) 147 (34.8) 53 (12.6) 3 (1)
M 33 (6.3) 70 (13.3) 163 (31.0) 57 (29.8) 103 (19.6) 3 (1)
Problems solving sessions attended by small groups of
medical/pharmacy students and residency or faculty.
P 25 (5.9) 39 (9.2) 84 (19.9) 136 (32.2) 138 (32.7) 4 (2)
M 31 (5.9) 55 (10.5) 100 (19.0) 185 (35.2) 155 (29.5) 4 (2)
Role playing sessions dealing with patients demanding
antimicrobial therapy.
P 28 (6.6) 40 (9.5) 155 (36.7) 121 (28.7) 78 (18.5) 3 (1)
M 59 (11.2) 97 (18.4) 90 (17.1) 142 (27.0) 138 (26.2) 4 (3)
n= number, % = percentage, IQR = interquartile range, P = pharmacy students, M = medical students.
Antibiotics 2021,10, 1204 8 of 14
Antibiotics 2021, 10, x FOR PEER REVIEW 6 of 15
Johns Hopkins Antibiotic guide 2.57 (1.08) 12 2.59 (1.14) 12 0.24
(0.811)
Sanford guide 2.55 (1.08) 13 2.55 (1.14) 13 −0.02 **
(0.988)
Infectious Diseases Society of America
Guidelines 2.53 (1.00) 14 2.50 (0.99) 11 2.20
(0.027) *
SD = standard deviation, t = independent t-test. * p ≤ 0.05 (significant difference).** In statistics, a negative t-value elaborates
that the direction of the effect under study is being reversed; this value has no impact on the significance of difference
between groups of data. Pharmacy students’ rank was italicized to differentiate from the rank given by the medical stu-
dents.
3.4. Perceived Usefulness of Teaching Methodology
Both medical and pharmacy students found problem solving sessions attended by a
small group of students as the most useful (very useful) teaching methodology to learn
antibiotic use and resistance, followed by the grand round’s lectures i.e., discussion of
clinical cases. Interestingly, classroom lectures were rated very useful by only 8.2% of
medical and 11.1% of pharmacy students and thus indicate a lack of effectiveness. Table 3
contrasts the perceived usefulness of different teaching methods among the pharmacy
and medical students in Punjab, Pakistan. Furthermore, as a whole, only 19.8% medical
and 17.1% pharmacy students rated their education and training on appropriate use of
antibiotics as very useful (Figure 1).
Figure 1. Overall usefulness of education regarding appropriate use of antimicrobials.
3.5. Perceived Preparedness
The overall mean score on perceived preparedness was higher among pharmacy stu-
dents as compared to medical students; however, the difference was not statistically sig-
nificant (p = 0.15). Among the pharmacy students, based on the mean score, the top three
least prepared individual curriculum items included; interpretation of antibiograms
(mean, 2.96, p = 0.48), followed by transition from intravenous to oral antibiotics (mean,
Figure 1. Overall usefulness of education regarding appropriate use of antimicrobials.
Table 4.
How well do you feel that your medical/pharmacy education has prepared you to do the following upon
graduation?
Statements
Medical Students Pharmacy Students t
(p-Value)
Mean
(SD)
Mean
(SD)
To know when to start antimicrobial therapy 3.30 3.36 1.01
(0.97) (0.99) (0.314)
How to select the best antimicrobial for a specific infection? 2.94 3.18 0.28
(1.13) (1.03) (0.001) *
To describe the correct spectrum of antimicrobial therapy for
different antimicrobials (what is covered by each drug)
3.32 3.28 −0.51 **
(1.00) (1.04) (0.613)
Understand the basic mechanisms of antimicrobial resistance 3.44 3.56 1.89
(1.01) (0.97) (0.059) *
How to streamline or de-escalate antimicrobial therapy? 3.23 3.09 −2.24 **
(0.99) (0.95) (0.025) *
How to interpret antibiograms? 3.02 2.96 −0.71 *
(1.11) (1.10) (0.481)
How to find reliable sources of information to treat infections? 3.24 3.42 2.68
(1.05) (1.01) (0.008) *
How to transition from intravenous to oral antibiotics (IV to PO
switch)?
2.91 3.03 2.02
(0.96) (0.88) (0.044) *
How to handle a patient who demands antimicrobial therapy that
is not indicated?
3.23 3.31 1.12
(1.13) (1.07) (0.262)
Overall Score 3.18 3.24 1.44
(0.70) (0.68) (0.152)
SD = standard deviation, t= independent t-test, IV = intravenous, PO = per oral. * p
≤
0.05 (significant difference). ** In statistics, a negative
t-value elaborates that the direction of the effect under study is being reversed, this value has no impact on the significance of difference
between groups of data.
Antibiotics 2021,10, 1204 9 of 14
4. Discussion
This study assessed medical and pharmacy students’ self-reported preparedness,
usefulness of different learning methods, range of topics covered, and common educational
resources preferred for antibiotic use and resistance. Our study noted several important
findings:
First, some major principles on prudent antibiotic use were perceived poorly pre-
pared which implies various areas where both pharmacy and medical students require
more training. For instance, medical students feel unprepared on the complexities in
selection of the best antimicrobial for a specific infection in daily practice, transition from
intravenous to oral, and finding a reliable source of information. These gaps in training
during undergraduate studies may also be correlated with the shortcomings identified
in antibiotics prescriptions in hospitals in Punjab where duration of antibiotic therapy or
doses of antibiotics and switch from intravenous to oral or route of administration were
absent or wrongly mentioned on the prescriptions [
15
,
16
]. A key consideration of these
findings would be that the low prepared areas should now be prioritized for improvement
during teaching planning.
Second, in terms of practical exposure, a vast majority of pharmacy students report lack
of clinical rotation in infectious diseases, which is worrying as it will limit the participation
of pharmacists in any future antibiotic stewardship role [
7
]. A number of studies have
mentioned participation in clinical rotation as the strongest predictor of greater knowledge
in students and concluded that clinical rotation in infectious diseases improves knowledge
of appropriate antibiotic use as compared to absentee students in clinical rotation [17,18].
Third, our findings reveal that passive forms of learning, such as classical classroom
lectures were not perceived as useful or popular in today’s generation in Pakistan. Many
universities have adopted problem based learning and improved students understanding.
A number of studies support the idea that active/interactive forms of learning have higher
and longer-term influence on prescribing habits later in professional life [
19
,
20
]. A study
in Nepal highlighted the successful teaching of antimicrobials through a problem-solving
approach as part of pharmacology lectures [
20
]. Furthermore, in terms of adult learning
behaviour, it is always beneficial to teach concepts from a disease-oriented approach
(e.g., urinary tract infections) or problem-oriented approach (e.g., antimicrobial resistance)
rather than a drug-oriented approach (e.g., cramming classification of antibiotics) or a
pathogen-oriented approach (e.g., methicillin-resistant Staphylococcus aureus) [5,18].
Many developed countries have recognized the importance of undergraduate training
and education and its impact on professional practice and attitude. For instance, in the
UK, a Specialist Advisory Committee on Antimicrobial Resistance has proposed a robust
framework for developing curricula to learn the rational use of antibiotics [
21
]. This
framework is based on developing core-learning outcomes (statements that define what
a student should know or be able to perform by the end of an educational intervention).
Teaching resources based on clinical case scenarios (vignettes) and problem-based learning
would be used to ensure that the learning outcomes were achieved. The learning outcomes
may be translated later into competencies that can be objectively measured by a concerned
body for the accreditation purposes. Similarly, in the United States, a new curriculum
on antimicrobial stewardship has been jointly designed by the U.S. Centres for Disease
Control and Prevention and the Association of American Medical Colleges [
5
,
21
]. While,
in Pakistan, conversion of a Bachelor of Pharmacy (a four years degree program) to Doctor
of Pharmacy (a five years degree program) happened in 2003 with an aim to inculcate a
more patient-oriented (clinical) curricula to pharmacy students. Pharm D curricula was last
updated in 2013, however, the clinical focus remained deficient and our study also reports
that a vast majority of the students have not received any clinical rotation in infectious
diseases [10].
Fourth, a vast majority of medical and pharmacy students were not familiar with the
term antibiotic stewardship. This finding is in line with the results reported in the study by
Hayat et al. [
13
]. Antibiotics use, resistance and mechanisms are part of the curriculum of
Antibiotics 2021,10, 1204 10 of 14
both Pharm D and MBBS degree programs, however, specifically, principals of antibiotics
stewardship and its concept is relatively new and grossly absent in both curricula.
Fifth, although the top three learning resources used in both disciplines were more
or less the same, both medical and pharmacy students did not consult any professional
guidelines as a preferred source of learning rational antibiotic use. This behaviour may
have resulted from a lack of focus on guidelines within the curricula, which does not bind
students or teachers to develop these habits. Research has shown that students who use the
Infectious Diseases Society of America (IDSA) guidelines demonstrate better and structured
knowledge of antibiotic use than those who do not use guidelines. Furthermore, students
who consulted guidelines during undergraduate studies are more likely to practice rational
use of antibiotics later in professional practice [14,22]
Sixth, lack of inter-professional collaboration between medical and pharmacy students
was evident. Students did not prefer to consult pharmacist or infectious disease physician
for knowledge exchange, even though both disciplines will assume the future role of a
patient educator, especially the pharmacist working in a community pharmacy, and will
formidably influence consumer behaviour on irrational and unauthorized purchase of
antibiotics without prescription.
Finally, various studies have concluded that it is easier to shape behaviours during
early education and training than changing established habits later during professional
life [
5
,
22
]. While, traditionally, a major focus of education has been on the experienced
prescribers and pharmacists, students or residents received little attention. This despite the
idea that they may otherwise benefit more from educational interventions, being in an early
phase of habit development. Research supports the idea that better training of students
and residents may result in long lasting antibiotics stewardship habits [
19
]. Furthermore,
for a resource limited setting i.e., low- and middle-income countries, a focus on education
may be the least resource consuming interventions to reduce antibiotic overuse [3].
4.1. Comparison with Existing Literature
The findings regarding the choice of educational resources by medical and pharmacy
students reported in our study are in line with a previous study conducted in Punjab [
23
].
Both studies found that medical and pharmacy students prefer to use textbooks to learn
antibiotic use. However, there exists methodological differences in terms of data analysis in
addition to the larger and diverse sample size in our study which may yield a comparatively
more reliable and generalizable result. However, our findings regarding self-perceived
preparedness are not in consonance with the mentioned study that reported no significant
difference between pharmacy and medical students except on the statement that asked to
describe the correct spectrum of antimicrobial therapy. These differences in findings may be
linked with the lack of diversity or inclusiveness in terms of the number of colleges in the
sample recruited to report the results (only two institutions participated in the study). While
we reported mixed findings and concluded significant differences in preparedness between
medical and pharmacy students based on a diverse sample. Pharmacy students were
poorly prepared in how to de-escalate antibiotic therapy and transition from intravenous
antibiotics to oral. While pharmacy students were better prepared to find a reliable source
of information to treat infections, and to select the best antimicrobial. Interestingly, these
findings are in line with the results of a multicentre survey conducted in three Asian
countries (Indonesia, Malaysia, and Pakistan) that reported similar results on self-perceived
confidence of pharmacy students to perform the tasks mentioned [
7
]. Another study in
Bangladesh reported similar lacks in the preparedness of medical students on antibiotic
use and resistance as reported in our study and suggested an upgrade of curricula on
antimicrobial stewardship as educational interventions [24].
A recent study conducted in seven pharmacy institutes in Pakistan concluded average
knowledge of the students on certain aspects of the antibiotic use and only 21.6% of
students were familiar with the antibiotic stewardship program [
13
]. These results are in
line with the results of our study that involved a comparatively larger sample. However,
Antibiotics 2021,10, 1204 11 of 14
our study contradicts the findings of this study that report that public university students
had a superior knowledge and reported no significant differences between the knowledge
of pharmacy students from private or public institutions in any contexts. The possible
reason could be the different statements used to develop a construct to cover antibiotic use
and resistance.
Comparing at a regional level, a multicentre survey in five Asian countries (Malaysia,
Thailand, Singapore, Indonesia, and the Philippines), reports that 87% of the schools use
interactive teaching formats and mainly deliver the knowledge through small group dis-
cussion (93%) vs. clinical case studies (69%), lectures (69%) and role-play (21%). Interactive
learning has improved many aspect of student learning on antibiotic use [
25
]. This state of
affairs implies that in the region, various other countries are steps ahead as compared to
Pakistan in terms of teaching methods. While, our study reports pervasive classical lectures
format and less interactive learning in both medical and pharmacy schools. Another study
conducted in central China revealed similar gaps in the teaching of medical education to
those in our study and highlighted the need for educational reform on medical education
in developing countries. Particularly, our results in the educational resources used among
medical students in Pakistan are quite similar and indicate the need for a change in the
teaching practices in the region [26].
4.2. Implications for Policy and Practice and Further Research
Based on the findings, the current study suggests the following implications for policy,
practice, and further research:
First, in order to boost students’ knowledge of optimal antibiotic use and prescribing;
reforms in the concerned undergraduate curriculum are inevitable. Curricula are being
revised worldwide; hence, a strong foundation within the existing curriculum is crucial
to prepare future healthcare professionals who can rationalize antibiotic use in hospitals
and in the community. It is time that PMC and PCP also revise respective curricula in
consultation with HEC toward antibiotic stewardship and optimal antibiotic use. For this,
the authors suggest integrating dedicated modules on antibiotic stewardship in the subject
of Pharmacology or Clinical Pharmacy. Second, clinical rotation in infectious diseases
should be a priority in future curricula reforms especially in the pharmacy. Third, given
the gaps in teaching methods, curricula should focus more on active (interactive) learning
techniques such as patient case studies and problem-based learning involving small groups
to deliver key concepts of prudent antibiotic use. Fourth, the addition of inter-professional
workshops right at the start of undergraduate training to overcome future barriers in
working as a team.
Fifth, there should be a change in educational resources and students should practice
the use of standard guidelines. Finally, there is a crucial need for further research to
understand how students’ self-perceived preparedness reflects observed preparedness
and how this in turn translates into clinical practice. A natural extension of this study
may involve a systematic comparison of the formal medical and pharmacy curricula and
pedagogical and assessment methods used in medical and pharmacy colleges in Pakistan
with internationally agreed upon sets of competencies in antimicrobial stewardship to
identify and address potential lacunas in training. Meanwhile, we expect that our results
provide useful insight for faculty currently teaching the rational use of antibiotics to
pharmacy and medical students in Pakistan.
4.3. Limitations and Strengths of the Study
We noted the following limitations/strengths of the study.
(a)
Our study did not recruit students or colleges based on random sampling; however,
we do not believe it will have introduced significant selection bias given the topic of
the study and the lack of incentives to participate. Moreover, this study collected data
from a majority of the medical and pharmacy colleges in the province and thus we
anticipate that results are likely to represent the overall scenario in the country.
Antibiotics 2021,10, 1204 12 of 14
(b)
Colleges under the auspices of Pakistan Armed Forces were not included in the sam-
ple because a time taking procedure to seek permission was required from General
Headquarters. However, based on the diversity of the sample, since students partic-
ipated from a large majority of the colleges, results appear to be generalizable and
more likely to represent the overall scenario in the country.
(c) Another limitation of this study was assessment bias. The questions in the survey may
not have necessarily covered all the dimensions of preparedness or educational re-
sources or teaching practices on antibiotic resistance, antibiotic therapy, and antibiotic
stewardship.
(d)
As some of the questions required the respondents to recall certain information, the
possibilities of the risk of recall bias could be there.
Strengths
(a) To our knowledge, this is the first comprehensive comparative study to report current
practices and perceived preparedness of the medical and pharmacy students on
antibiotic use.
(b)
Our study was free of recruitment bias as the data collectors did not opt for a con-
venient sample of the colleges but included medical and pharmacy colleges in nine
administrative divisions of Punjab Pakistan.
(c)
Furthermore, since students participated from nearly all medical and pharmacy
colleges results likely to be highly relevant to all institutions in the country.
(d)
Study reported specific gaps in teaching, and identified poorly prepared areas related
to prudent antibiotic use.
5. Conclusions
Significant differences exist between medical and pharmacy students in educational re-
sources used, topics covered during undergraduate degrees, and perceived preparedness to
take future roles in antibiotic use. Both medical and pharmacy students demonstrated low
self-perceived preparedness and require more training in selection of antibiotic, posology,
duration and de-escalation and transition from intravenous to oral delivery of the antibiotic
therapy. Both medical and pharmacy students did not find lecture-based learning useful
for learning antibiotics use. There is a strong reason for action and we urge educational
policy makers in Pakistan to take a step forward to upgrade the decade old curricula of
the Pharm D and MBBS degree program to one that uses problem-based learning with
increased practical exposure. This sort of education should start at an early stage, during
the undergraduate curriculum, to ensure maximal effect and to foster the right attitudes.
The problem does exist at the beginning at least in this part of the world, hence,
scientists alone cannot tackle the looming crisis of antibiotic resistance, and we need educa-
tionist too. To curb growing antibiotic misuse and resistance, the concerned stakeholders
in Pakistan should undertake targeted educational reforms to ensure that medical and
pharmacy students leave the college with confidence to play a pivotal role in rationalizing
the use of antibiotics in hospitals and community settings.
Supplementary Materials:
The following are available online at https://www.mdpi.com/article/10
.3390/antibiotics10101204/s1, Table S1: Demographics of respondents, Table S2: How well do you
feel that your medical/ pharmacy education has prepared you to do the following upon graduation?
Author Contributions:
Conceptualization, N.M.; methodology, N.M., N.S.-u.-R., C.S.Z., S.J. and
K.M.; software, S.A., U.eB.I., M.I., R.M.A., A.K. and K.M.; validation, N.M., C.S.Z. and N.S.-u.-R.;
formal analysis, N.M. and K.M.; investigation, S.A., M.I., R.M.A., A.K. and U.eB.I.; resources, N.S.-
u.-R., S.J. and C.S.Z.; data curation, S.A., M.I., R.M.A., A.K. and U.eB.I.; writing—original draft
preparation, N.M.; writing—review and editing, N.S.-u.-R., S.J., K.M. and C.S.Z.; visualization, S.A.,
M.I., R.M.A., A.K. and U.eB.I.; supervision, N.M., N.S.-u.-R., C.S.Z. and S.J.; project administration,
N.M., S.A., M.I., R.M.A., A.K. and U.eB.I. All authors have read and agreed to the published version
of the manuscript.
Antibiotics 2021,10, 1204 13 of 14
Funding: This research received no external funding.
Institutional Review Board Statement:
The study was conducted according to the guidelines of
the Declaration of Helsinki, and approved by the Institutional Review Board/Ethics Committee of
Lahore Pharmacy College, Lahore Medical & Dental College (ref: ETH/LPC/15/07/19).
Informed Consent Statement:
Written Informed consent was obtained from all medical and phar-
macy colleges involved in the study for participation and later publication of this paper.
Data Availability Statement:
Research team has made all the underlying data available to the public
in the supplementary files. Furthermore, the corresponding authors may be contacted for any further
clarifications.
Acknowledgments:
Many thanks to Lilian Abbo, M.D. FIDSA, Chief Infection Control & Antimicro-
bial Stewardship, Jackson Health System, Professor of Infectious Diseases, Department of Medicine
& Miami Transplant Institute, University of Miami Miller School of Medicine; for the generous
permission to use the survey. We extend our heartfelt thanks to Javaid Asgher (CEO, Lahore Medical
& Dental College) and Asad Ahmad Khan (Company Secretary, Lahore Medical & Dental College)
for the valuable contacts to acquire data in various medical and pharmacy colleges in Punjab and
Islamabad. All individuals included in this section have consented to the acknowledgement.
Conflicts of Interest: The authors declare no conflict of interest.
Disclaimer:
Some of the initial findings of this study were presented as oral presentation in In-
ternational Conference on Pharmaceutical Research and Pharmacy Practice cum 14th IIUM-MPS
Pharmacy Scientific Conference, Malaysia and later published as conference proceedings in the
Journal of Pharmacy & Bio-allied Sciences.
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