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Abstract

Promoting awareness regarding antimicrobial resistance (AMR) and stewardship (AMS) is crucial as it results in treatment failures and an economic burden on a country. This study was conducted to determine the baseline knowledge of healthcare students and the impact of conducting training sessions regarding AMR and AMS on the knowledge of healthcare students. This study was conducted using a quasi-experimental design at Wah Medical College, Pakistan, and its subsidiary institutes in 4 months. Two hundred twenty-six healthcare students were selected via stratified sampling through a proportional allocation from 3 academic student groups. Training sessions were conducted and data were collected using a structured questionnaire. Data analysis was done using Statistical Package for the Social Sciences version 23. The median age of the participants was 22 while most were females (54.9%). There was a significant difference in means of AMR score between BScN and AD-BTM student groups and among AD-BTM and MBBS student groups. In the case of AMS scores, the difference in means was significant among all student groups. The training sessions were found effective as the mean AMR and AMS knowledge scores among all the student groups increased significantly after the intervention.

Keywords

antibiotics antimicrobial resistance Stewardship healthcare students LMICs

What do we already know about this topic?

Policies regarding control of inappropriate use of antimicrobials exist at the global level in the form of the Global Action Plan for AMR and in Pakistan in the form of the National Action Plan for AMR but due to poor awareness, there is a lack of implementation.

How does your research contribute to the field?

This study established the impact of conducting training sessions on the knowledge level of healthcare students regarding Antimicrobial Resistance and Stewardship as it has been suggested by the previous literature that poor prescribing practices can also result from a lack of awareness about these issues at the undergraduate level of healthcare education.

What are your research’s implications for theory, practice, or policy?

Since Antimicrobial Stewardship is not taught as a part of the formal healthcare curriculum in Pakistan, this study attempted to convince the policy-makers and policy implementers of Pakistan that if a course or module is introduced as part of undergraduate curriculums, it will help in curbing the issue of AMR by increasing awareness among the healthcare workforce.

Introduction

AMR has become a leading cause of death globally and can affect anyone irrespective of age, gender or nationality.¹ As published in the Lancet, 1.2 million deaths globally are attributed to antimicrobial resistance.² The World Bank has estimated that globally the gross domestic product (GDP) will reduce by 3.8% by 2050 due to the persistence of this issue worldwide.³ According to the Organization for Economic Co-operation and Development (OECD), the situation regarding antimicrobial resistance is quite worse in the lower and middle-income countries (LMICs) where around 60% of the infections are caused by resistant organisms.⁴ In the last 15 years, a 67% increase in antimicrobial consumption has been reported in Pakistan which has also led to increased antimicrobial resistance rates.⁵ AMR surveillance conducted in the Eastern Mediterranean Region reported Pakistan’s resistance to 5 of 6 superbugs considered for the study.⁶ A systematic review conducted in Pakistan reported that 49% of the total Staphylococcus aureus cases were resistant to methicillin, which establishes AMR as a national health issue.⁷

AMR directly affects patient treatment outcomes and is responsible for the increased burden on a country’s healthcare system.⁸ Antimicrobial resistance often occurs due to inappropriate use of antimicrobials that may result from inadequate knowledge and poor adherence to drug protocols by the prescribers.⁹ Self-medication is an essential contributor toward antimicrobial resistance and this behavior can be addressed by training the healthcare workers on the appropriate use of antimicrobials so that they can work on bringing behavioral change in healthcare workers and the general public as well.¹⁰ Providing competency-based training to future prescribers will also lead them to adapt delayed antimicrobial prescription practices and equip them to educate the general public regarding appropriate antimicrobial consumption practices.¹¹ Global Action Plan on AMR (GAP-AMR) further emphasizes the need to train all healthcare workers on the issue of antimicrobial resistance, which led to the formulation of the National Action Plan on AMR for Pakistan (NAP-AMR) in 2017.^12,13

The concept of antimicrobial stewardship addresses the inappropriateness of antimicrobial prescription to prevent the further emergence of antimicrobial resistance to improve patient treatment outcomes in a low-middle-income country like Pakistan. Implementing this program in our local healthcare settings is very important and so is the knowledge about this program.^14,15

Poor prescribing practices may result from a lack of awareness and understanding about antimicrobial resistance and prescribing practices at the undergraduate level of healthcare education.¹⁶ It was evident from a study conducted among students of different public and private sector universities of Lahore which reported that around 80% of the participants were involved in self-prescribing antimicrobials. It also emphasized the need for educational sessions to promote antimicrobial stewardship practices among healthcare students.¹⁷ The need to encourage educational activities regarding antimicrobial resistance and stewardship among undergraduate and postgraduate healthcare students of Pakistan was also recognized by a study that was conducted to assess the progress of the country related to “AMR national action plan” in 2021.¹⁸

As identified earlier, poor awareness regarding antimicrobial resistance and stewardship among healthcare students poses one of the biggest hurdles in implementing NAP-AMR. Keeping this in view, this study was designed to assess the level of knowledge of undergraduate healthcare students regarding antimicrobial resistance and stewardship and also to assess the impact of conducting training sessions on their knowledge.

Methodology

It was a quantitative study and was conducted using a Quasi-experimental design. The study was conducted at Wah Medical College (WMC) and its subsidiary institutes of Nursing and Allied Health Sciences, located in Wah Cantonment, Pakistan, for 4 months, that is, September 2022 to December 2022. The study population consisted of fourth-year and fifth-year MBBS students, third-year and fourth-year Bachelor of Science in Nursing (BScN) generic students, and first-year and second-year Associate Degree in Blood Transfusion Medicine (AD-BTM) students. Since Wah Medical College is the only organization providing healthcare education for the community of Wah Cantonment, the students with maximum clinical exposure among all the undergraduate healthcare programs were considered for the study. The students were enrolled in the study using stratified sampling through proportional allocation. The participants gave written informed consent.

Sample Size Calculation

Based on the population of 520 students obtained from the student affairs departments of the 3 institutes, MBBS (300), Nursing (120), and AD-BTM (100), the confidence level was set at 95% and the alpha error at 5%, sample size of 226 using Yamane’s formula was calculated.¹⁹

Formula:

n = \frac{N}{1 + N {(e)}^{2}}

Where:

n = sample size required, N = number of people in the population, e = allowable error (%)

n = \frac{520}{1 + 520 \times {(0.05)}^{2}} = 226

Calculation for proportional allocation of students: The target sample size for students of each degree program was calculated through proportional allocation as MBBS (131), Nursing (52), and AD-BTM (43).

For MBBS students =

\frac{300}{520} \times 226 = 131

For BScN students =

\frac{120}{520} \times 226 = 52

For AD-BTM students =

\frac{100}{520} \times 226 = 43

Inclusion Criteria

All the students, studying in the fourth and final year of the MBBS program, the third and final year of the BScN generic program, and first-year and second-year students of the AD-BTM program at WMC and its subsidiary institutes, who gave consent to be included in the study.

Exclusion Criteria

Data Collection

Data collection was initiated in the 3 institutes. A total of 6 training sessions were conducted, that is, one training session regarding antimicrobial resistance and stewardship for each included class. Data was collected in 2 phases for each class. A structured questionnaire was used to collect baseline data on students’ knowledge regarding antimicrobial resistance and stewardship before conducting training sessions. Sessions were conducted using a large group interactive session (LGIS) strategy. After ending the training session for each class, post-intervention data was collected using the same questionnaire. Total scores for knowledge regarding antimicrobial resistance and antimicrobial stewardship were calculated separately for each student pre-intervention and post-intervention.

Data Collection Tool

It was a structured questionnaire constructed after an extensive literature review and contained closed-ended questions. It was divided into 3 parts. The first part comprised demographic information of the participants. The second part included a Likert scale for assessment of students’ knowledge regarding antibiotic resistance. This scale was also used in a study conducted in Nigeria.¹⁹ “It comprised 10 questions with a 5-point Likert scale response option ranging from strongly agree (5) to strongly disagree (1) to evaluate students’ knowledge of antimicrobial resistance. The maximum obtainable score was 50. There were 4 negatively worded knowledge questions (items 2, 3, 9, 10); these questions were reversed scored.” The third section of the questionnaire had the tool for assessment of knowledge regarding antimicrobial stewardship. Knowledge regarding 7 core elements of Hospital Stewardship Programs, that is, hospital leadership commitment, accountability, pharmacy expertise, action, tracking, reporting, and education, was assessed in this portion. This tool was adapted from the “Antibiotic Stewardship Program Assessment Tool for Core Elements of Hospital Antibiotic Stewardship Programs” published by CDC.²⁰ This tool consisted of a Likert scale with options ranging from strongly agree (5) to strongly disagree (1). It contained 15 questions so the maximum obtainable score was 75. The questionnaire used in this study has also been added as Supplemental Material.

The face validity of the questionnaire was conducted by 2 public health experts and a pharmacist and the recommended changes were incorporated. The questionnaire was piloted in 5% of the sample size (12 healthcare students). These 12 students were excluded from the study. A Cronbach’s alpha value of .75 was attained for the antimicrobial resistance knowledge scale while a value of .71 was attained for the antimicrobial stewardship knowledge scale.

Data Analysis

It was carried out using SPSS version 23. Data regarding the socio-demographic profile of the students was entered. Variables were then created for students’ knowledge scores regarding antimicrobial resistance and antimicrobial stewardship pre- and post-intervention, respectively among MBBS, Nursing and AD-BTM students, which were considered as dependent variables while the student group, age of the students and gender of the students were considered as independent variables. A descriptive analysis of the variables was done. One-way ANOVA tests were applied to determine the difference in the mean of antimicrobial resistance and antimicrobial stewardship pre-intervention knowledge scores among MBBS, Nursing and AD-BTM students. After achieving significant results, Tukey’s HSD Test for multiple comparisons was applied. Paired t-tests were used to determine the difference in the mean knowledge scores in MBBS, Nursing and AD-BTM students separately before and after the training sessions.

Results

A total of 226 students enrolled in different healthcare programs at Wah Medical College and its subsidiary institutes of Nursing and Allied Health Sciences gave consent to be included in the study. The median age of the overall students was 22 (2.0) while median ages for BScN, ADBTM and MBBS students were 22 (2.0), 21 (3.0), and 22 (1.0) respectively. Table 1 shows that the majority of the students (54.9%) were females while 58% of the participants were from the MBBS degree program.

Table 1.

Socio-demographic Characteristics of Students.

Characteristics	n (%)
Gender
Male	102 (45.1)
Female	124 (54.9)
Student groups
BscN	52 (23)
Third year	28
Fourth year	24
AD-BTM	43 (19)
First year	23
Second year	20
MBBS	131 (58)
Fourth year	68
Fifth year	63

To assess the difference in mean AMR and AMS knowledge scores among the 3 student groups, One-way ANOVA tests were applied. The tests revealed that there was a statistically significant difference in mean AMR knowledge score between at least 2 groups (F(2, 223) = [17.80], P < .05 while there was also a statistically significant difference in mean AMS knowledge score between at least 2 groups (F(2, 223) = [114.51], P < .05) as can be seen in Table 2.

Table 2.

Results of One-way ANOVA Test for Difference in Mean AMR and AMS Across Student Groups.

Difference in mean AMR knowledge score across student groups
Sr. No.	Student group	Mean antimicrobial resistance knowledge score ± SD	P-value*
1	BScN	35.57 ± 4.46	<.05
2	ADBTM	31.72 ± 3.99
3	MBBS	37.09 ± 5.67
Difference in mean AMS knowledge score across student groups
Sr. No.	Student group	Mean antimicrobial Stewardship knowledge score ± SD	P-value*
1	BScN	43.13 ± 1.95	<.05
2	ADBTM	51.90 ± 6.61
3	MBBS	59.92 ± 8.10

One-way ANOVA test.

To further assess the differences, Tukey’s HSD test for multiple comparisons was applied for both scores. For the AMR knowledge score, it was found that the mean value was significantly different between BScN and AD-BTM groups (P < .05, 95% C.I. = [1.36, 6.35]) and AD-BTM groups and MBBS groups (P < .05, 95% C.I. = [−7.50, −3.25]).

There was no statistically significant difference in mean scores between BScN and MBBS (P > .05). For the AMS knowledge score, the multiple comparisons test found that the mean value was significantly different between all the student groups (P < .05).

To assess the effect of conducting training sessions among healthcare students, paired t-tests were applied to determine the difference in AMR and AMS knowledge scores pre- and post-intervention in each student group. As shown in Table 3, there was a significant increase in the AMR and AMS knowledge scores post-intervention for all the healthcare student groups (P < .05).

Table 3.

Student Group-wise Comparison of Pre-and Post-intervention AMR and AMS Mean Knowledge Score.

Comparison of pre-and post-intervention AMR mean knowledge score
Sr. No.	Student group	Pre-test knowledge mean score ± SD	Post-test knowledge mean score ± SD	P-value*
1	BScN	35.57 ± 4.46	42.23 ± 5.37	<.05
2	AD-BTM	31.72 ± 3.99	35.00 ± 4.13	<.05
3	MBBS	37.09 ± 5.67	40.90 ± 6.06	<.05
Comparison of pre-and post-intervention AMS mean knowledge score
Sr. No.	Student group	Pre-test knowledge mean score ± SD	Post-test knowledge mean score ± SD	P-value*
1	BScN	43.13 ± 1.95	72.75 ± 1.25	<.05
2	AD-BTM	51.91 ± 6.61	61.37 ± 5.74	<.05
3	MBBS	59.92 ± 8.10	68.56 ± 5.92	<.05

Paired t-test.

Discussion

This study was conducted using a quasi-experimental design among 226 healthcare students. The mean age of the participants was 22 (2.0) while most (54.9%) were females. These students were divided into 3 groups based on their degree programs, that is, BScN, AD-BTM and MBBS. The effect of conducting training sessions regarding AMR and AMS has been assessed in all the student groups.

Antimicrobial resistance is a global issue. It is a well-established fact that improving awareness regarding AMR is the most important solution to mitigate this problem. As a result, educational interventions have been carried out among different target populations in different parts of the world and efforts have been made to establish the effect of conducting educational inventions regarding AMR and AMS as these activities require resources.

A cross-sectional study conducted among 994 medical students in Spain established the effect of the inclusion of infectious disease training in the final year curriculum on the knowledge of students regarding antimicrobial stewardship which increased from 9.3% in the first year to 52.2% in the sixth year of the degree program (P < .05).²¹ This study also established that when an intervention like a training session on AMS was conducted among medical students, the mean AMS knowledge score increased from 59.92 ± 8.10 to 68.56 ± 5.92 (P < .05).

A mixed-method study was also designed to assess the change in awareness regarding antimicrobial stewardship among healthcare workers in a tertiary care hospital in Ghana. Data was collected in 2 phases. Pre-test and post-test data were collected using a structured questionnaire at the time of training sessions from 50 participants. After 6 months, in-depth interviews were conducted among 18 healthcare professionals. It was reported that knowledge related to stewardship improved immediately after sessions while the practices improved after 6 months of the intervention.²² In the present study, AMS knowledge also increased among all the student groups (P < .05).

In Egypt, two interventional studies were conducted to establish the effect of conducting training sessions regarding AMS. One study was conducted among 69 healthcare workers (doctors, nurses, and pharmacists) at National Liver Institute²³ and the other study was conducted only among 115 nurses at Ain Shams University.²⁴ In both studies, there was significant improvement in the knowledge, attitudes, and perceptions of healthcare workers regarding antimicrobial stewardship (P < .05, <.05). The current study has also established the effect of conducting educational intervention across all included groups (P < .05).

In the COVID era, the world moved toward online interventions. Such a study was conducted in Jordan where training sessions related to AMR and AMS were conducted online via Zoom platform for 2 days and online pre-test and post-test questionnaires were filled by 100 pharmacists and it demonstrated a positive effect on the knowledge of pharmacists (P < .05).²⁵ The current study showed a similar effect on the knowledge of healthcare students after the intervention (P < .05).

AMR issue can only be addressed if interventions using the One Health approach are adapted. This approach revolves around the fact that misuse of antimicrobials in humans, animals, plants, and the environment leads to the clinical presentation of antimicrobial resistance in humans.²⁶ Success can only be achieved by employing strategies that involve antimicrobial prescribers related to the fields as mentioned earlier.²⁷ A study conducted in Iran among live-stock farmers identified poor knowledge associated with AMR and AMS as one of the factors for inappropriate use of antimicrobials among livestock breeders, other factors being the urge for increased production and marketing strategies used by the pharma industry.²⁸ Similar findings were reported among farmers in Uganda.²⁹ In Croatia, the effect of poor awareness related to AMR and AMS on prescribing practices was also reported among doctors and pharmacists.³⁰ In this context, our study had the shortcoming that knowledge assessment only among healthcare students was carried out as pharmacy and veterinary educational institutes are not present in Wah Cantt. Our study was conducted in only one cantonment of Pakistan so it lacks generalizability. A multi-center study needs to be conducted to provide substantial data for policymaking.

Implementation of antimicrobial stewardship is the best strategy to address the inappropriate use of antimicrobials. In Pakistan, factors like lack of political commitment, lack of infrastructure for antimicrobial usage surveillance and lack of structured educational interventions have been recognized as obstacles to implementing the program.³¹

Conclusion

It can be concluded that the difference in means of AMR score was significant between BScN and AD-BTM student groups and among AD-BTM and MBBS student groups. In the case of AMS scores, the difference in means was significant among all student groups. It can be inferred from the study that conducting training sessions had a positive effect on the knowledge of students as a significant difference in mean AMR and AMS knowledge scores was observed among each student group so the introduction of a course related to AMR and AMS in undergraduate healthcare curriculums can be an effective way to improve awareness regarding AMR and AMS among healthcare workforce in Pakistan.

Supplemental Material

sj-docx-1-inq-10.1177_00469580241228443 – Supplemental material for The Impact of Antimicrobial Resistance and Stewardship Training Sessions on Knowledge of Healthcare Students of Wah Cantonment, Pakistan

Supplemental material, sj-docx-1-inq-10.1177_00469580241228443 for The Impact of Antimicrobial Resistance and Stewardship Training Sessions on Knowledge of Healthcare Students of Wah Cantonment, Pakistan by Saleh Ahmed, Ahmad Hussen Tareq and Doua Ilyas in INQUIRY: The Journal of Health Care Organization, Provision, and Financing

Footnotes

Acknowledgements

I would like to express my gratitude to Prof. Dr. Musarat Ramzan, Dean of Academics at Wah Medical College, for providing me with much needed guidance and for helping me in getting the required permissions from the college and its subsidiary institutes. I would like to specially thank Mr. Asad Ellahi, Biostatistician at Wah Medical College, who guided me during the process of data analysis.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Ethical Consideration

The study was initiated after approval from Institutional Review Committee of HSA granted vide letter no. F.No.000118/HSA/MSPH-2021 dated 8th Sept, 2022 and data collection was started after taking ethical clearance from Institutional Review boards of Wah Medical College granted vide letter no. WMC/ERC/IRB/029, Dated 3rd Oct, 2022 and from Institutes of Nursing and Allied Health Sciences granted vide letter no. 786/DC/27/WMC, Dated 12th Oct, 2022. Participants were enrolled in the study after taking written informed consent. They were explained that their participation in the research was voluntarily and they could drop out of the study whenever they wished. They were assured that their data will only be used for research purposes and it will have no effect on their academic record.

ORCID iD

Saleh Ahmed

Supplemental Material

Supplemental material for this article is available online.

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Supplementary Material

Please find the following supplemental material available below.

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The Impact of Antimicrobial Resistance and Stewardship Training Sessions on Knowledge of Healthcare Students of Wah Cantonment,Pakistan

Abstract

Keywords

Introduction

Methodology

Sample Size Calculation

Inclusion Criteria

Exclusion Criteria

Data Collection

Data Collection Tool

Data Analysis

Results

Discussion

Conclusion

Supplemental Material

sj-docx-1-inq-10.1177_00469580241228443 – Supplemental material for The Impact of Antimicrobial Resistance and Stewardship Training Sessions on Knowledge of Healthcare Students of Wah Cantonment, Pakistan

Footnotes

Acknowledgements

Declaration of Conflicting Interests

Funding

Ethical Consideration

ORCID iD

Supplemental Material

References

Supplementary Material