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antibiotics
Article
Assessment of Adherence to the Core Elements of Hospital
Antibiotic Stewardship Programs: A Survey of the Tertiary Care
Hospitals in Punjab, Pakistan
Naeem Mubarak 1, * , Asma Sarwar Khan 1, Taheer Zahid 1, Umm e Barirah Ijaz 1, Muhammad Majid Aziz 1,
Rabeel Khan 1, Khalid Mahmood 2, Nasira Saif-ur-Rehman 1,* and Che Suraya Zin 3,*
Citation: Mubarak, N.; Khan, A.S.;
Zahid, T.; Ijaz, U.e.B.; Aziz, M.M.;
Khan, R.; Mahmood, K.;
Saif-ur-Rehman, N.; Zin, C.S.
Assessment of Adherence to the Core
Elements of Hospital Antibiotic
Stewardship Programs: A Survey of
the Tertiary Care Hospitals in Punjab,
Pakistan. Antibiotics 2021,10, 906.
https://doi.org/10.3390/
antibiotics10080906
Academic Editor: Marc Maresca
Received: 30 May 2021
Accepted: 22 July 2021
Published: 24 July 2021
Publisher’s Note: MDPI stays neutral
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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/).
1Department of Pharmacy Practice, Lahore Medical & Dental College, University of Health Sciences,
Lahore 54600, Pakistan; asma.sarwar@lmdc.edu.pk (A.S.K.); taheerzahid21@gmail.com (T.Z.);
bariraaijazz@gmail.com (U.e.B.I.); majid.aziz@lmdc.edu.pk (M.M.A.); rabeel.khan74@gmail.com (R.K.)
2
Institute of Information Management, University of the Punjab, Lahore 54000, Pakistan; khalid.im@pu.edu.pk
3Kulliyyah of Pharmacy, International Islamic University Malaysia, Kuantan 25200, Malaysia
*Correspondence: naeem.mubarak@lmdc.edu.pk (N.M.); dean.lpc@lmdc.edu.pk (N.S.-u.-R.);
chesuraya@iium.edu.my (C.S.Z.)
Abstract: Background:
To restrain antibiotic resistance, the Centers for Disease Control and Preven-
tion (CDC), United States of America, urges all hospital settings to implement the Core Elements
of Hospital Antibiotic Stewardship Programs (CEHASP). However, the concept of hospital-based
antibiotic stewardship programs is relatively new in Low- and Middle-Income Countries.
Aim:
To
appraise the adherence of the tertiary care hospitals to seven CEHASPs.
Design and Setting:
A cross-
sectional study in the tertiary care hospitals in Punjab, Pakistan.
Method:
CEHASP assessment tool,
(a checklist) was used to collect data from the eligible hospitals based on purposive sampling. The
check list had 19 statements to cover seven CEHASPs: Hospital Leadership Commitment, Accountability,
Pharmacy Expertise, Action (Implement Interventions to Improve Antibiotic Use), Tracking Antibiotic Use
and Outcomes, Reporting Antibiotic Use and Outcomes, and Education. For each statement, a response of
“YES”, “NO” or “Under Process” constituted a score of 2, 0 and 1, respectively, where the higher the
scores the better the adherence. Categorical variables were described through descriptive statistics,
while independent t-test computed group differences.
Result
: A total of 68 hospitals (n= 33 public,
n= 35 private) participated with a response rate of 79.1%. No hospital demonstrated “Perfect”
adherence. Roughly half private (48.6%) and more than half public (54.5%) sector hospitals were
“Poor“ in adherence. Based on the mean score, there was no significant difference between the
private and the public hospitals in terms of comparison of individual core elements. The two most
neglected core elements emerged as top priority area were: Reporting Antibiotic Use and Outcomes and
Tracking Antibiotic Use and Outcomes.
Conclusion:
The current response of Pakistan to implement
hospital-based antibiotic stewardship programs is inadequate. This study points out significant gaps
of practice both in public and private tertiary care hospitals. A majority of the core elements of
antibiotic stewardship are either absent or ”Under Process”. The deficiency/priority areas mentioned
require immediate attention of the concerned stakeholders in Pakistan.
Keywords:
antibiotic stewardship; antimicrobial stewardship; hospitals; tertiary care; Pakistan; core
elements; CDC; health policy; rational drug use; AMR; LMIC; resistance
1. Background
The struggle for survival is one of the basic instincts of living organisms, including
bacteria, who have evolved different mechanisms to resist the lethal actions of antibiotics—
once considered “magical bullets”. This situation has led to one of the inescapable crises of
21st century called “antibiotic resistance”, i.e., the situation in which antibiotics would no
longer be effective against bacteria. These resistant bacteria make even ordinary infections
Antibiotics 2021,10, 906. https://doi.org/10.3390/antibiotics10080906 https://www.mdpi.com/journal/antibiotics
Antibiotics 2021,10, 906 2 of 14
more difficult to treat and surgical procedure riskier to perform. Centuries of progress in
improving health and economy is at stake due to antibiotic resistance [
1
,
2
]. If healthcare sys-
tems do not implement systematic interventions, by 2050, antibiotic resistance may inflict
10 million deaths per year around the globe and an economic loss of USD 100 trillion [
3
].
The World Health Organization (WHO) recorded grave concerns on the continuous rife in
antibiotic resistance and warned of the possibilities of a “post antibiotic era” [2].
Multiple factors are responsible for accelerating antibiotic resistance, however, there
exists a strong correlation between the development of resistance and overuse or over
prescribing of antibiotics [
4
,
5
]. To optimize the use of antibiotics, the WHO placed the
implementation of hospital based antibiotic stewardship programs (ASPs) at the heart of
its Global Action Plan to curb antibiotic resistance [
6
]. Antibiotic Stewardship includes
“coordinated interventions designed to improve and measure the appropriate use of [antibiotic] agents
by promoting the selection of the optimal [antibiotic] drug regimen including dosing, duration of
therapy, and route of administration” [
7
]. Thus, the WHO urges hospitals and other healthcare
settings (at all levels, i.e., primary, secondary, and tertiary care) to implement some form of
ASPs based on local or international guidelines. Subsequently, many high-income countries
shifted the focus of public health policy and implemented ASPs in hospitals and other
related settings. At the forefront, for instance, the United States Centers for Diseases Control
and Prevention (CDC) chartered the Core Elements of Hospital Antibiotic Stewardship
Programs (CEHASP) in 2016, updated in 2019, and demanded its implementation in all
hospitals across the country [8].
Antibiotic resistance is no longer only a problem of high-income countries, for instance,
five Low- and Middle-Income Countries (LMICs) bear more than half (52%) of the burden
of mortalities caused by neonatal sepsis associated with resistant strains of bacteria. In
some cases, bacteria are resistant to up to 90% of antibiotics [
1
,
2
]. Over prescribing, limited
surveillance or regulatory framework, and rampant poor practices of infection prevention
and control incite a faster spread of resistant bacteria in LMIC. A recent estimate of the
prevalence of antibiotic resistance in different regions has raised many red flags and
revealed that Asia is home to 70% of emerging resistance, making this region an important
focus of ASPs [
9
]. However, the concept of hospital-based ASPs has gained recent attention
in LMICs, and various governments have recorded commitments to take initiatives to
implement ASPs in hospitals. Nevertheless, translating national or local commitment into
action represents a formidable implementation challenge [10,11].
Pakistan, a country in South Asia, belongs to the World Bank strata of LMICs with
a population 216.5 million. In terms of healthcare infrastructure, Punjab is the most de-
veloped province that accommodates more than 65% of the population of Pakistan [
1
,
12
].
Healthcare is provided by a rapidly expanding network of private hospitals and heavily
subsidized public hospitals where the latter fulfils the healthcare needs of the majority of
the population [
13
]. Antibiotic consumption rate is alarmingly high and reportedly Pak-
istan has the third highest antibiotic consumption in LMICs [
14
]. Recent point prevalence
surveys on antibiotic use in hospitals of Punjab also depict a gloomy situation where pa-
tients receive unnecessary antibiotics [15,16]. Furthermore, various studies have reported
pervasive infections caused by multidrug resistant and extensively drug resistant bacte-
ria [
1
]. Rampant inappropriate prescribing requires systematic interventions to change the
physician’s attitude, and, in this context, ASPs can play a formidable role to optimize the
antibiotic use in hospitals. Pakistan’s National Action Plan (2017) recognizes antibiotic
resistance as a key challenge in Pakistan and urges hospitals nationwide to develop and
implement ASPs to curtail the continuous surge of resistant infections [
17
]. However, to
what extent standardized ASPs have been instituted in hospitals remains unknown, and
there is a paucity of key implementation data and facts on the roll out of ASPs, especially
in tertiary care settings. Hence, this study aims to appraise the current adherence levels of
tertiary care hospitals to the CEHASPs. It also implies underlying subgroup analysis to
identify differences in adherence to CEHASPs in private and public hospitals. The evidence
base generated may potentially contribute to the formulation of national or local policies to
Antibiotics 2021,10, 906 3 of 14
implement ASPs in hospitals with a prime focus on the gaps and priority areas identified
in this study.
2. Methods
2.1. Study Design, Survey Instrument and Setting
This was a cross-sectional study to collect hospitals’ data on the validated CDC “An-
tibiotic stewardship program assessment tool” [
18
]. Compared with other ASP assessment
tools, the CDC assessment tool offers a valuable advantage, i.e., a universal applicability,
as it can be used to evaluate any setting (resource rich or resource poor). The survey
instrument comprised of two parts.
Part one enquired about the demographic details of the hospital, such as name, owner-
ship (public/private), name of the administrative division of Punjab in which the hospital
was located, and designation and sign and stamp of the hospital representative providing
the information. Part two was comprised of the CDC assessment tool enlisting seven core
elements of hospital ASPs. A core element was a broad category of action or strategy that
covered a main aspect of antibiotic stewardship (e.g., commitment or education). The seven
core elements are: Hospital Leadership Commitment, Accountability, Pharmacy Expertise, Action
(Implement Interventions to Improve Antibiotic Use), Tracking Antibiotic Use and Outcomes,
Reporting Antibiotic Use and Outcomes, and Education. Generally, three to four statements
(items) covered a unique core element. On a summative scale, for each statement of a
core element, a response of “YES”, “NO” or “Under Process” constituted a score of 2, 0
and 1, respectively. There were a total 19 statements covering the seven core elements of
hospital ASP (please see the Survey Instrument CDC assessment tool for core elements of
hospital antibiotic stewardship programs in Table S1 in Supplementary Materials). Thus, a
maximum score of 38 could be possible for a given hospital where the higher the scores the
better the adherence. Furthermore, as the seven core elements had a different number of
sub-statements, to normalize the data, we used mean in order to compare the individual
core element in a standardized way.
A list of tertiary care hospitals was obtained from the Specialized Healthcare & Medical
Education Department, government of Punjab, and hospitals were recruited based on the
purposive sampling.
2.2. Data Collection
Data were collected in a personal meeting with the representative of the adminis-
tration of the hospitals willing to participate in the survey from 3 December 2019 to 15
January 2020. Any of the following representatives of the hospital administration was
eligible to fill the survey: Medical Superintendent, Deputy Medical Superintendent, As-
sistant Medical Superintendent, Manager/Head of Pharmacy, or Chief Pharmacist. These
representatives were chosen because all of them belong to hospital administration, hence,
are better aware of the policies and practices in a given hospital. Furthermore, the outcome
(survey responses) could not change with the change of the designation, as all are part of
the administration team in a hierarchy. The team of data collectors—11 Pharm-D final year
students—aimed to reach tertiary care hospitals located in all the nine administrative divi-
sions of the Punjab, and Islamabad, the capital territory. The data collection team remained
present throughout the meeting for any query related to the CEHASP. As compared to a
survey sent through mail or email, the in-person, self-administration of the survey was
opted to ensure quick and high response rate, and an error-free recording of the responses.
Final analysis added only those responses which were signed and stamped by any of the
earlier mentioned representatives.
2.3. Inclusion and Exclusion Criteria
All tertiary care hospitals (both in the public and private sector) located in Punjab
and Islamabad were eligible to participate in the survey. For this study, a tertiary care
hospital was defined as any hospital enlisted by the Punjab government as an access point
Antibiotics 2021,10, 906 4 of 14
for tertiary care, or any teaching or non-teaching hospital in the private or public sector
with distinct specialties and facilities, such as ICU, CCU, dialysis, ventilators, in-house
lab testing and pharmacy services, etc., and general specialties like surgery, medicine,
orthopedics, pediatrics, and gynecology.
Primary care facilities and small secondary care hospitals (<30 beds) were excluded.
2.4. Data Management and Statistical Analysis
Statistical Package for Social Sciences (SPSS) (version 22 IBM, Armonk, NY„ USA) was
used to manage and analyze data. Descriptive statistics were used to evaluate the extent
of adherence, while mean difference between private and public hospitals was analyzed
with the help of t-tests for each of the core elements mentioned earlier with a pvalue < 0.05
considered significant.
Here, an important point to mention was about the nature of variables. For a particular
core element, the score of 2, 1 or 0 against “YES”, “Under Process”, and “NO”, respectively,
was taken as numerical variable because the scores were given as real numbers similar to
scores in an exam where one point is given on a correct answer leading to a total score. This
type of data is not dichotomous and hence may not be confused just because of ”YES/NO”.
Thus, mean scores would be based on a summative scale, if choose to answer “YES” for all
the statements of the survey, a hospital could achieve a maximum score of 38. The mean
scores of hospitals would be related to adherence where the higher the score, the better
the adherence to the CEHASP. To assess level of adherence of participating tertiary care
hospitals, the total score obtained by the hospitals was assigned a category, for instance, a
total score range of 0–11.9, 12–23.9, 24–34.9, and 35–38 was defined as “Poor”, “Moderate”,
“Good”, and “Perfect”, respectively.
2.5. Ethics
The ethical approval was granted by the Research Ethics Committee, Lahore Phar-
macy College, Lahore Medical & Dental College (ref#
ETH/LPC/
10/08/19). Before taking
consent, project information was shared with the representative of all participating hos-
pitals to detail the background, aims, and how the data would be utilized. To ensure
the anonymity of hospitals, an individual identification number was allocated to each
participating hospital. Data were stored in a password protected computer.
3. Results
A total of n= 68 hospitals (n= 33 public, n= 35 private) participated with a response
rate of 79.1% (12 private and 6 public hospitals declined due to lack of willingness to
share data). Mainly, the respondents were Chief Pharmacist/Director of Pharmacy Ser-
vices/Manager of Pharmacy Services (36.8%, n= 25), followed by Medical Superintendents
(29.3%, n= 20), Assistant Medical Superintendents (22%, n= 15), and Deputy Medical
Superintendents (11.8%, n= 8).
The survey reached to diversely located hospitals in all official administrative divisions
of Punjab, i.e., Lahore, Rawalpindi, Dera Ghazi Khan, Bahawalpur, Sahiwal, Sargodha
Faisalabad, Multan, and Gujranwala, and additionally, the Islamabad Capital Territory
(the federal capital), and three other cities in Punjab, Sialkot, Sheikhupura, and Rahim
Yar Khan (Table 1). No public or private hospital was in “perfect” compliance with all
the seven core elements (Figure 1). The majority of the hospitals, in both the private and
public sector, were poorly adherent to the CEHASP. In subgroup analysis, among the
public hospitals, only 9.4% hospitals scored high enough to fall in the “Good” category of
adherence, while more than half (54.5%) were in the “Poor” category, as depicted in the
Figure 1. The situation was more or less the same in the private sector. Among the private
hospitals, roughly half (48.6%) were in the “Poor” category, while 14.3% hospital were
in the “Good” category of adherence. Furthermore, private and public hospitals had no
significant difference in mean scores for adherence to the CEHASP.
Antibiotics 2021,10, 906 5 of 14
Table 1. Number of public and private hospitals that participated from each division of Punjab.
Name of Division No. of Public Hospitals No. of Private Hospitals
Lahore 14 12
Islamabad 2 2
Rawalpindi 2 2
Faisalabad 3 3
Gujranwala 2 3
Sialkot 1 2
Sheikhupura 1 1
Sargodha 2 2
Multan 2 3
Bahawalpur 1 1
Rahim Yar Khan 1 1
Dera Ghazi Khan 1 1
Sahiwal 1 2
Total 33 35
Antibiotics 2021, 10, x FOR PEER REVIEW 5 of 13
situation was more or less the same in the private sector. Among the private hospitals,
roughly half (48.6%) were in the “Poor” category, while 14.3% hospital were in the “Good”
category of adherence. Furthermore, private and public hospitals had no significant dif-
ference in mean scores for adherence to the CEHASP.
Table 1. Number of public and private hospitals that participated from each division of Punjab.
Name of Division No. of Public Hospitals No. of Private Hospitals
Lahore 14 12
Islamabad 2 2
Rawalpindi 2 2
Faisalabad 3 3
Gujranwala 2 3
Sialkot 1 2
Sheikhupura 1 1
Sargodha 2 2
Multan 2 3
Bahawalpur 1 1
Rahim Yar Khan 1 1
Dera Ghazi Khan 1 1
Sahiwal 1 2
Total 33 35
Figure 1. Percentage of public and private tertiary care hospitals in each defined category of adherence for core elements.
In the context of individual core elements, a major lacking was observed in the core
element Reporting Antibiotic Use and Outcomes, that received the lowest mean in both pri-
vate and public hospitals, followed by Tracking Antibiotic Use and Outcomes.
In subgroup analysis, comparatively, private hospitals performed well (higher mean
score) in almost all core elements, however, the difference was not statistically significant
as mentioned in Table 2. Nevertheless, public hospitals scored higher in Tracking Antibiotic
Use and Outcomes (but the difference was not significant, Table 2).
Figure 1. Percentage of public and private tertiary care hospitals in each defined category of adherence for core elements.
In the context of individual core elements, a major lacking was observed in the core
element Reporting Antibiotic Use and Outcomes, that received the lowest mean in both private
and public hospitals, followed by Tracking Antibiotic Use and Outcomes.
In subgroup analysis, comparatively, private hospitals performed well (higher mean
score) in almost all core elements, however, the difference was not statistically significant
as mentioned in Table 2. Nevertheless, public hospitals scored higher in Tracking Antibiotic
Use and Outcomes (but the difference was not significant, Table 2).
Antibiotics 2021,10, 906 6 of 14
Table 2. Core elements of hospital antibiotics stewardship.
Sr. Mean (SD)
Subgroup Analysis
Public Hospitals
Mean (SD)
Private Hospitals
Mean (SD)
t*
(p-Value)
Core Elements of
Antibiotic
Stewardship
1.
Hospital Leadership
Commitment 0.76 (0.71) 0.74 (0.69) 0.78 (0.73)
−0.21
(0.835)
2.
Accountability 1.34 (0.80) 1.33 (0.89) 1.34 (0.73)
−0.05
(0.961)
3.
Pharmacy Expertise 1.10 (0.77) 1.09 (0.75) 1.10 (0.79)
−0.05
(0.962)
4.
Action: Implement
Interventions to Improve
Antibiotic Use
0.69 (0.52) 0.66 (0.50) 0.71 (0.54)
−0.45
(0.651)
5.
Tracking Antibiotic Use
and Outcomes 0.44 (0.37) 0.45 (0.36) 0.44 (0.38)
−0.21
(0.834)
6.
Reporting Antibiotic Use
and Outcomes 0.20 (0.30) 0.14 (0.25) 0.26 (0.33)
−1.61
(0.113)
7.
Education 1.29 (0.73) 1.26 (0.82) 1.33 (0.65)
−0.40
(0.693)
Total mean score 0.72 (0.39) 0.70 (0.41) 0.74 (0.38)
−0.42
(0.678)
Notes: * Independent t-test. Abbreviation: SD, standard deviation.
Item level analysis and the scores of the individual statements of each core element
in the survey can be found in the Table 3, while corresponding SPSS data is provided in
Table S2 of the Supplementary Materials.
Table 3. Item level analysis of core elements of antibiotics stewardship programs.
Statements Mean
(SD)
Subgroup Analysis
Public Hospitals
Mean
Private Hospitals
Mean
t
(p-Value)
Hospital
Leadership
Commitment
Does facility leadership provide
stewardship program leader(s)
dedicated time to manage the
program and conduct daily
stewardship interventions?
1.00
(0.96) 1.03 (0.95) 0.97 (0.99) 0.25
(0.362)
Does facility leadership provide
stewardship program leader(s) with
resources (e.g., IT support, training)
to effectively operate the program?
0.31
(0.55) 0.27 (0.52) 0.34 (0.59)
−0.52
(0.315)
Does your antibiotic stewardship
program have a senior executive that
serves as a point of contact or
“champion” to help ensure the
program has resources and support
to accomplish its mission?
1.13
(0.86) 1.12 (0.89) 1.14 (0.85)
−0.10
(0.496)
Do stewardship program leader(s)
have regularly scheduled meetings
with facility leadership and/or the
hospital board to report and discuss
stewardship activities, resources and
outcomes?
0.60
(0.90) 0.55 (0.87) 0.66 (0.94)
−0.51
(0.250)
Antibiotics 2021,10, 906 7 of 14
Table 3. Cont.
Statements Mean
(SD)
Subgroup Analysis
Public Hospitals
Mean
Private Hospitals
Mean
t
(p-Value)
Accountability
Does your facility have a leader or
co-leaders responsible for program
management and outcomes of
stewardship activities?
1.34
(0.80) 1.33 (0.89) 1.34 (0.73)
−0.05
(0.041)
Pharmacy
Expertise
Does your facility have a
pharmacist(s) responsible for leading
implementation efforts to improve
antibiotic use?
1.35
(0.86) 1.36 (0.86) 1.34 (0.88) 0.10
(0.840)
Does your pharmacist(s) leading
implementation efforts have specific
training and/or experience in
antibiotic stewardship?
0.84
(0.80) 0.82 (0.81) 0.86 (0.81)
−0.198
(0.931)
Action: Implement
Interventions to
Improve Antibiotic
Use
Does your facility perform
prospective audit and feedback for
specific antibiotic agents?
0.88
(0.89) 0.88 (0.89) 0.89 (0.90)
−0.03
(0.904)
Does your facility perform
preauthorization for specific
antibiotic agents?
0.56
(0.58) 0.55 (0.62) 0.57 (0.56)
−0.18
(0.430)
Does your facility have
facility-specific treatment
recommendations, based on national
guidelines and local pathogen
susceptibilities, to assist with
antibiotic selection for common
clinical conditions?
0.62
(0.52) 0.55 (0.51) 0.69 (0.53)
−1.12
(0.532)
Tracking Antibiotic
Use and Outcomes
Does your antibiotic stewardship
program track antibiotic use by
submitting to the
national/provisional/international
center Antimicrobial Use (AU)
Option?
0.29
(0.46) 0.42 (0.50) 0.17 (0.38) 2.33
(0.000)
Does your antibiotic stewardship
program monitor prospective audit
and feedback interventions by
tracking the types of interventions
and acceptance of recommendations?
0.54
(0.72) 0.58 (0.75) 0.51 (0.70) 0.35
(0.563)
Does your antibiotic stewardship
program monitor preauthorization
interventions by tracking which
agents are being requested for which
conditions?
0.40
(0.55) 0.33 (0.54) 0.46 (0.56)
−0.93
(0.294)
Does your stewardship program
monitor adherence to facility-specific
treatment recommendations?
0.54
(0.53) 0.48 (0.51) 0.60 (0.55)
−0.89
(0.65)
Antibiotics 2021,10, 906 8 of 14
Table 3. Cont.
Statements Mean
(SD)
Subgroup Analysis
Public Hospitals
Mean
Private Hospitals
Mean
t
(p-Value)
Reporting
Antibiotic Use and
Outcomes
Does your antibiotic stewardship
program share facility and/or
individual prescriber-specific reports
on antibiotic use with prescribers?
0.03
(0.17) 0.00 (0.00) 0.06 (0.24)
−1.40
(0.004)
Does your antibiotic stewardship
program report adherence to
treatment recommendations to
prescribers (e.g., results from
medication use evaluations, etc.)?
0.31
(0.47) 0.24 (0.44) 0.37 (0.49)
−1.15
(0.026)
Has your facility distributed a current
antibiogram to prescribers?
0.26
(0.51) 0.18 (0.47) 0.34 (0.54)
−1.32
(0.029)
Education
Does your stewardship program
provide education to prescribers and
other relevant staff on optimal
prescribing, adverse reactions from
antibiotics, and antibiotic resistance?
1.49
(0.82) 0.33 (0.89) 1.57 (0.74)
−1.20
(0.035)
Does your stewardship program
provide education to prescribers as
part of the prospective audit and
feedback process (sometimes called
“handshake stewardship”)?
1.13
(0.75) 1.18 (0.81) 1.09 (0.70) 0.52
(0.104)
Precisely, one of the statements that covered the core element of Action, “Does your
facility have facility-specific treatment recommendations, based on national guidelines
and local pathogen susceptibilities, to assist with antibiotic selection for common clinical
conditions?”, was reported as the most “Under Process” intervention to improve stew-
ardship in more than half (58.8%) of all the participating hospitals (54.5% public, 62.9%
private). It was followed by the statement that covered the core element of Tracking of
Antibiotic Use and Outcomes: “Does your stewardship program monitor adherence to
facility- specific treatment recommendations?”. It received the status of “Under Process” by
51.5% of the participating hospitals (48.5% public, 54.3% of private). This trend is depicted
in the Figure 2.
Antibiotics 2021,10, 906 9 of 14
Antibiotics 2021, 10, x FOR PEER REVIEW 8 of 13
Figure 2. Percentage of hospitals which reported “Under Process” interventions for individual statements of each core
element. LC1 to LC4 = statements 1 to 4 of the core element Hospital Leadership and Commitment. A = statement of the core
element Accountability. PE1 to PE2 = statements 1 to 2 of the core element Pharmacy Expertise. A1 to A3 = statements 1 to 3
of the core element Action. T1 to T4 = statements 1 to 4 of the core element Tracking Antibiotics Use and Outcomes. R1 to R3
= statements 1 to 3 of the core element Reporting Antibiotics Use and Outcomes. E1 to E2 = statements 1 to 2 of the core
element Education.
4. Discussion
This study explored the current state of implementation and roll out of ASPs in the
tertiary care hospitals of Punjab, Pakistan. Tertiary care represents an advance setting,
however, given the findings, unfortunately the majority of the CEHASPs are yet to be
implemented in the hospitals. For instance, Reporting and Tracking of Antibiotic Use and
Outcomes are at the heart of any ASPs, however, emerged as the top two most neglected
core elements both in private and public hospitals that participated in this study. A pos-
sible reason of this implementation failure could be the general absence of a compelling
narrative to link the ASPs as the core national health priority to convince the political will.
Similarly, response on the four statements that cover Tracking Antibiotic Use and Outcomes
revealed that preauthorization and prospective audits were evidently absent in an over-
whelming majority of the hospitals, especially in private sector. Furthermore, hospitals do
not track and document antibiotic use to submit to a provincial/national or international
database. Many studies have reported the impact of prospective audits and formular as
being most effective measurer [19]. Nevertheless, these two core elements implied two
major gaps in practice for any future intervention and may be taken as a top priority.
Similarly, Hospital Leadership Commitment was notably lacking and indicated another gap
in practice. Leadership commitment in a hospital is actually a direct function of the extent
of the implementation of ASPs. Hospital Leadership Commitment was evaluated through
four statements, however, data reveal that not all statements for this core element received
high scores. The most underscored statement among the four was, “Does facility leader-
ship provide stewardship program leader(s) with resources (e.g., IT support, training) to
effectively operate the program?”. This highlights the lack of resources hospitals have in
this part of the world.
Two encouraging findings of this study are related to the two core elements Account-
ability and Education of the prescribers, which received the highest mean score in both
private and public hospitals. Literature also supports that a small investment on these
LC1 LC2 LC3 LC4 A PE1 PE2 A1 A2 A3 T1 T2 T3 T4 R1 R2 R3 E1 E2
Public Hospitals 12.1 21.2 21.2 6.1 12.1 15.2 33.3 21.2 42.4 54.5 42.4 27.3 27.3 48.5 0.0 24.2 12.1 12.1 33.3
Private Hospitals 5.7 22.9 28.6 2.9 37.1 14.3 34.3 20.0 51.4 62.9 17.1 28.6 40.0 54.3 5.7 37.1 28.6 14.3 51.4
Total Hospitals 8.8 22.1 25.0 4.4 25.0 14.7 33.8 20.6 47.1 58.8 29.4 27.9 33.8 51.5 2.9 30.9 20.6 13.2 42.6
0.0
10.0
20.0
30.0
40.0
50.0
60.0
70.0
Percentage of hospitals (%)
Individual statements of CEHASPs reported as "Under Process"
Public Hospitals Private Hospitals
Figure 2.
Percentage of hospitals which reported “Under Process” interventions for individual statements of each core
element. LC1 to LC4 = statements 1 to 4 of the core element Hospital Leadership and Commitment. A = statement of the core
element Accountability. PE1 to PE2 = statements 1 to 2 of the core element Pharmacy Expertise. A1 to A3 = statements 1 to 3 of
the core element Action. T1 to T4 = statements 1 to 4 of the core element Tracking Antibiotics Use and Outcomes. R1 to R3 =
statements 1 to 3 of the core element Reporting Antibiotics Use and Outcomes. E1 to E2 = statements 1 to 2 of the core element
Education.
4. Discussion
This study explored the current state of implementation and roll out of ASPs in the
tertiary care hospitals of Punjab, Pakistan. Tertiary care represents an advance setting,
however, given the findings, unfortunately the majority of the CEHASPs are yet to be
implemented in the hospitals. For instance, Reporting and Tracking of Antibiotic Use and
Outcomes are at the heart of any ASPs, however, emerged as the top two most neglected
core elements both in private and public hospitals that participated in this study. A
possible reason of this implementation failure could be the general absence of a compelling
narrative to link the ASPs as the core national health priority to convince the political
will. Similarly, response on the four statements that cover Tracking Antibiotic Use and
Outcomes revealed that preauthorization and prospective audits were evidently absent
in an overwhelming majority of the hospitals, especially in private sector. Furthermore,
hospitals do not track and document antibiotic use to submit to a provincial/national or
international database. Many studies have reported the impact of prospective audits and
formular as being most effective measurer [
19
]. Nevertheless, these two core elements
implied two major gaps in practice for any future intervention and may be taken as a
top priority. Similarly, Hospital Leadership Commitment was notably lacking and indicated
another gap in practice. Leadership commitment in a hospital is actually a direct function
of the extent of the implementation of ASPs. Hospital Leadership Commitment was evaluated
through four statements, however, data reveal that not all statements for this core element
received high scores. The most underscored statement among the four was, “Does facility
leadership provide stewardship program leader(s) with resources (e.g., IT support, training)
to effectively operate the program?”. This highlights the lack of resources hospitals have in
this part of the world.
Two encouraging findings of this study are related to the two core elements Account-
ability and Education of the prescribers, which received the highest mean score in both
Antibiotics 2021,10, 906 10 of 14
private and public hospitals. Literature also supports that a small investment on these
basic core elements can substantially improve the outcome [
20
]. The next logical step is to
translate commitment into action. Likewise, Education of the prescriber and other related
healthcare professionals received the second highest score in the CEHASPs, particularly in
private sector. It is a positive development as compared to previously reported studies and
indicates that more hospitals are providing continuous education to healthcare profession-
als and are making them accountable for stewardship interventions and programs [
21
]. Be
that as it may, though continuous education seems to be part of practice in the hospitals, it
should be improved to the next level as it requires the least resources. One way to improve
this deficiency is to engage hospital pharmacists in the stewardship teams. The addition
of pharmacists in ASPs has shown to improve the outcomes of antibiotic stewardship
interventions, and a recent example may be cited from Africa [
9
,
22
]. This is of particular
relevance for LMICs like Pakistan, where only a few physicians are available for a huge
population of patients, and therefore dissemination of a meaningful education to patients
is often compromised. Pakistan also needs to engage its underutilized workforce of phar-
macists in hospitals for the same purpose [
12
,
16
]. Thus, utilizing pharmacy expertise in
antibiotic stewardship activities beyond simple dispensing and procurement is a need in
Pakistan. Survey results on utilization and training of hospital pharmacist expertise show
moderate progress in adoption of pharmacist expertise in tertiary care hospitals.
Finally, a promising finding of the study is related to those core elements which were
reported “Under Process”, i.e., not implemented at the time of study. For instance, more
than half of tertiary care hospitals are in the process of implementing treatment guidelines
for local susceptible pathogens, as well as tracking the antibiotic use in wards as shown in
Figure 2. Furthermore, 33.8% of the participating hospitals are in the process of training
and involving pharmacists in ASPs. This shows that an increasing number of hospitals
(especially in the private sector) have been sensitized on the issue at hand, and one may
expect an action for the implementation soon.
4.1. Comparison with the Existing Literature
The findings of this study are in agreement with the results of a previous similar study
conducted in outpatient settings of tertiary care hospitals in Punjab [
23
]. Reporting Antibiotic
Use and Outcomes and Tracking Antibiotic Use and Outcomes remain the top deficiency areas
reported in both studies. This state of affairs indicates a lack of action and too-slow
implementation process, hence, requires immediate attention of the health authorities.
Our study results may be broadly comparable to the findings of a qualitative study
that explored physicians’ views for implementation of the ASPs in public hospitals of
Punjab and mentioned that physicians endorsed the implementation of stricter policies
on antibiotics surveillance [
19
]. This is in line with our results of the core element that
judged Accountability to implement ASPs and received one of the highest scores among
the seven CEHASPs. At the same time, our data contradict the findings of the same study
that poor familiarity of ASPs exists among the physicians in the hospitals surveyed. One
possible reason could be the differences in the sample and data collection time of the
two studies. The mentioned study had participating physicians mainly from the public
hospitals, while our study included physicians (MS/AMS/DMS) and pharmacists from
both private and public sector hospitals in proportion in 2020. Another study conducted
in Karachi, a city in the province of Sindh, Pakistan, identified similar gaps in practice of
antibiotic stewardship in hospitals [
24
]. This study reported a serious lack of leadership
commitment and reporting antibiotic use in the 44 hospitals that participated, which is in
line with our results. However, our study took a step further and reported new findings on
various ASPs which were “Under Process” in different hospitals. Furthermore, comparing
these two studies, our study findings were based on a diverse sample of the hospitals and
thus reported more reliable data. Nevertheless, both studies point out serious lacking in
two different provinces of Pakistan (Punjab and Sindh) and collectively portrays a general
absence of policies in place.
Antibiotics 2021,10, 906 11 of 14
Compared to other LMICs internationally, the findings of this study imply a poor
to moderate adoption and implementation of the core elements of ASPs in hospitals.
Substantial progress has been reported, for instance, in African regions where Antibiotic
Surveillance and Stewardship Programs have been implemented in a majority of the
hospitals and routine surveillance and audits are being performed. These programs
have resulted in improving the prescribing habits of not only physicians, but surgeons
as well, and improved awareness of the public and professionals. With the inclusion of
hospital pharmacists in the stewardship team to lead the stewardship activities, significant
reductions in the misuse of antibiotics have been observed [
22
,
25
,
26
]. Similarly, another
study conducted in Jordan also aimed to evaluate the adherence of hospitals to the core
elements of antibiotic stewardship and reported slow adoption and poor implementation
of interventions in the country [
27
]. However, the data was obtained in 2017 and there
could have been improvements in stewardship activities in the meantime.
In the region, Pakistan can learn some lessons from China, which has achieved sub-
stantial success in implementation of ASPs in the tertiary care setting, especially in terms
of Leadership Commitment and Tracking Antibiotic Use. Data of 116 hospitals from
all provinces and municipalities revealed that 94% of the hospitals had formal teams for
antibiotic stewardship interventions which ensure tracking of antibiotics use through preau-
thorization and post prescription reviews with feedback [
28
]. Thus, in Asia, many countries
have started implementing various core elements of hospital-based ASPs, however, in
Pakistan the pace is comparatively slow.
4.2. Implications for Policy and Practice and Further Research
Periodic cross-sectional audits are mandatory to keep a check on the progress of the
implementation of the stewardship activities in hospitals. The results of this study warrant
more in-depth quantitative research into core elements that scored low in order to fully
understand the quality of antibiotic stewardship in the tertiary care setting. Pakistan has
partnered with a US program, Global Antimicrobial Resistance Partnership, and made
commitments to curb antibiotic resistance [
29
]. It is also in parallel to Pakistan’s first
National Action Plan (2017) that aims to rationalize the use of antibiotics with a prime
focus on ASPs in hospitals. However, the findings of this study voice apprehensions over
the implementation failure of translating political commitment into action. Thus, our
findings serve as a reminder to expediate the process of the implementation of ASPs in
healthcare settings. The gaps identified in this study are more relevant as a broader outline
to refine the plan into action. Based on the findings, the current study suggests following
implications for policy, practice and further research:
(a)
The deficiency areas highlighted in this study, such as the core elements of Tracking
and Reporting of Antibiotic Use, should be prioritized in any future policy shift and
must be given due weight.
(b)
Concerned ministry should take a step forward and enforce a low hang intervention
of tertiary care hospitals. Here, the concept of low hang intervention refers to interven-
tions that require least resources but yield high outcomes, for instance, Education of
the prescriber is directly correlated with the improved prescribing habits and patient
education.
(c) Hospital pharmacists should be engaged in antibiotic stewardship activities in the hos-
pitals, beyond merely dispensing or procurement of medicines. As of now pharmacy
expertise is an official requirement in the CDC proffered CEHASP.
(d)
Similar studies need to be conducted in other provinces of Pakistan to draw a holistic
picture of the situation to keep a check on the progress of implementation of the ASPs.
4.3. Limitations and Strength of the Study
We noted the following limitations and strengths of the study. We only covered tertiary
care hospitals in Punjab and ICT, hence, results may be interrupted with caution in terms
of generalizability to other provinces of Pakistan. The sample of tertiary care hospitals
Antibiotics 2021,10, 906 12 of 14
was, though diverse and large, still purposive, and the participation was voluntary and
not an obligation as the case of government funded audits. We did not collect detailed
demographic data of the hospitals, such as the number of beds, wards, lab facilities, etc.
However, this kind of data were of lesser significance and unrelated to the objectives set in
this research.
To the best of our knowledge, this is the first study that extensively covered tertiary
care hospitals in Punjab and the Islamabad Capital Territory to appraise the rollout of
some form of ASP against a standard, i.e., the CEHASP in Punjab. Additionally, our study
aimed to minimize recruitment bias as the data collectors did not opt for a convenient
sample of the hospitals in Lahore only, but rather to reach out to hospitals diversely located
in different divisions of Punjab. In terms of impact, the study reported specific gaps in
ASPs in hospitals in Punjab for future policy. These findings are equally useful for other
LMICs from an introspective point of view and urge healthcare stakeholders to encourage
hospitals to implement a minimum set of ASPs.
5. Conclusions
The current response of Pakistan to implement hospital-based antibiotic stewardship
programs is inadequate. The findings of this study further imply a too-slow implementa-
tion and adoption of the stewardship programs in the tertiary care hospitals of the most
developed province of Pakistan, i.e., Punjab. Despite the grandiose infrastructure and
resources private hospitals have in Pakistan, there was no significant difference between
the two groups in terms of adherence. While two core elements indicated an encouraging
situation, i.e., Accountability and Education, nevertheless, overall findings are disappointing
and there is still much more that needs to be done. The majority of the core elements of
antibiotic stewardship are either absent or ”Under Process” and indicate significant gaps
in the practice of antibiotic stewardship. If left unattended, these gaps will inflict immense
harm and ultimately affect the appropriate use of antibiotics in hospitals. The findings
of this study further point out some urgent priority areas to focus on for action, such as
Tracking and Reporting of Antibiotic Use and Outcomes in hospitals. These priority areas
should be given special emphasis in future policy for hospital-based antibiotic stewardship
programs. This study urges relevant stakeholders to expediate the implementation of
antibiotic stewardship programs in hospitals to curb the growing antibiotic resistance and
optimize antibiotic therapy. A significant impact is only possible if a majority of the hospi-
tals in Pakistan implement uniform stewardship programs. We are running our time out
for antibiotics, and if implementation of stewardship interventions is further delayed, the
resistant infections will have disastrous impact on the healthcare sector and the country’s
economy.
Supplementary Materials:
The following are available online at https://www.mdpi.com/article/10
.3390/antibiotics10080906/s1, Table S1: Survey Instrument CDC assessment tool for core elements of
hospital antibiotic stewardship programs; Table S2: Individual hospital response SPSS file.
Author Contributions:
Conceptualization, N.M.; methodology, N.M., N.S.-u.-R., C.S.Z. and K.M.;
software, T.Z., U.e.B.I., R.K., A.S.K. and K.M.; validation, C.S.Z. and N.S.-u.-R.; formal analysis, N.M.
and K.M.; investigation, A.S.K., T.Z., U.e.B.I. and R.K.; resources, N.S.-u.-R., M.M.A. and C.S.Z.; data
curation, A.S.K., T.Z., U.e.B.I. and R.K.; writing—original draft preparation, N.M.; writing—review
and editing, N.S.-u.-R., M.M.A. and C.S.Z.; visualization, A.S.K., T.Z., U.e.B.I. and R.K.; supervision,
N.M., N.S.-u.-R., C.S.Z. and MMA; project administration, N.M., A.S.K., T.Z., U.e.B.I. and R.K. All
authors have read and agreed to the published version of the manuscript.
Funding: This study received no financial support for the research, authorship, and/or publication
of this article.
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/10/08/19).
Antibiotics 2021,10, 906 13 of 14
Informed Consent Statement:
Informed consent was obtained from all subjects involved in the
study for participation and later publication of this paper.
Data Availability Statement: All the data have been provided in the supplementary information.
Acknowledgments:
We extend our heartfelt thanks to Javaid Asgher and Asad Ahmad Khan for the
valuable contacts to acquire data in various hospitals in the province.
Conflicts of Interest: The authors declare no conflict of interest.
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