University Students’ Antibiotic Use and Knowledge of Antimicrobial Resistance: What Are the Common Myths?

We aimed to assess antibiotic usage and knowledge regarding antibiotics and antimicrobial resistance (AMR) among undergraduate students of the Universiti Brunei Darussalam (UBD), public university located in Brunei Darussalam. A cross-sectional study was performed using a self-administered questionnaire. The questionnaire was adapted from the World Health Organization’s (WHO) “Antibiotic resistance: Multi-country public awareness” survey distributed online. Students at the UBD were invited to participate in the online survey through internal email. The questionnaire consisted of five sections: demographic information, antibiotic usage, knowledge on antibiotics, antibiotic resistance (AMR), and use of antibiotics in agriculture. The data were analyzed descriptively and appropriate inferential statistics were used accordingly. A total of 130 students returned a completed questionnaire. The result of the study found that 51% (n = 66) of the students had good level of knowledge of antibiotic and antimicrobial resistance with a mean total knowledge score of nine out of 14. Of note, 76% (n = 99) of the respondents mistakenly believed that antibiotic resistance is the result of the body becoming resistant to antibiotics. Only 14% (n = 18) of the respondents were found to have poor knowledge on antibiotics and antimicrobial resistance in the study. Misconceptions in regards to the use of antibiotics for conditions related to viral illnesses like cold and flu (41%, n = 53) were noticed among the respondents in our study. Thus, improving knowledge on antibiotics is crucial to address these beliefs.


Introduction
The abuse and excessive utilization of antibiotics have led to the rise of antimicrobial resistance (AMR) which poses a major threat to individual health globally [1]. At least 700,000 deaths globally a year are caused by drug-resistant diseases and the rate of mortality has been predicted to grow to 10 million deaths per year by 2050 [2,3]. In Asia alone, an estimated 4.73 million deaths annually will be attributed to antimicrobial resistance by 2050 [4].
Antimicrobial drugs can be defined as a group of drugs that are effective against microorganisms and comprise antibiotics, antifungals, antivirals, and antiparasitic drugs, whereas an antibacterial agent is any agent that is directed against bacteria [5]. Bacterial infections can be prevented and treated with medicines called antibiotics [6]. An antibacterial agent only acts upon bacteria, but antibiotics can work on both bacteria and fungi. students in Sri Lanka revealed that senior students had good knowledge of antibiotics and antimicrobial resistance, although some had misconceptions about antibiotic use for viral illnesses [26]. A similar study in Malaysia also reported students had average knowledge in relation to antibiotics and good awareness of antibiotic resistance, although the study found that some respondents actually believed that antibiotics were useful in viral conditions [26]. This showed that despite having good knowledge of antibiotics and being aware of the essential information about antimicrobial resistance, the misunderstanding on the use of antibiotics in conditions related to viral infections was evident among undergraduate students.
To the best knowledge of the author, there are no documented Bruneian studies assessing the knowledge and perception of antibiotics. The Ministry of Health of Brunei often relies on the data of the neighboring countries as a yardstick in planning the public health campaign. Thus, this study is aimed to explore antibiotic usage and knowledge regarding antibiotics and antimicrobial resistance (AMR) among the Bruneian population, targeting specifically undergraduate students. This study could provide baseline data for future interventions and public health campaigning on antibiotic usage and antimicrobial resistance.

Study Design
This was a cross-sectional online survey study conducted from March to April 2020. The study involved undergraduate students from the Universiti Brunei Darussalam. The criteria of eligibility for the study were as follows: (i) adult (over 18 years old) and (ii) able to read and understand the Malay or English language. The students who were not willing to participate were excluded from the study.
An e-mail invitation was initially mailed to the Academic Registrar at the Institute of Health Sciences, then it was forwarded to all the Registrars from various faculties at the Universiti Brunei Darussalam. The data were collected from an online survey questionnaire. E-mail invitations for participation containing the online survey link and the information sheet for participants were disseminated to the targeted participants. To increase the response rate, reminder e-mails were forwarded twice to the contact persons following a two weeks interval. Other than reminder emails, the survey was also distributed among the students through WhatsApp application as a reminder.

Sample Size Calculation
Raosoft website was used to calculate the sample size with a confidence level set to 95% and the 5% margin of error [34]. Assuming a minimum population of 244, a sample of 150 participants was sought. The number required was calculated based on the proportional ratio.

Study Instrument
The questionnaire was adapted from the questionnaire based on the World Health Organization's (WHO) "Antibiotic resistance: Multi-country public awareness" survey [35]. This questionnaire was preferred for the study, because it had been used previously by the WHO and contains relevant topics which cover the use of antibiotics and knowledge of antibiotics and antimicrobial resistance. The permission for reprinting and reproducing the survey was acquired from the WHO.
The online questionnaire was displayed in English, which is the medium of instruction at the university, and the questions were mostly close-ended. The questionnaire consisted of the following 5 sections: A: basic demographic data of the participants, including age, gender, nationality, years of study, and faculty; B: antibiotic use: 3 questions on the prior use of antibiotics, advice received, and the place of obtaining them; C: knowledge of antibiotics: 4 questions about the treatment duration, knowledge of sharing of antibiotics, disease conditions which require antibiotics; D: knowledge of antibiotic resistance: 5 questions on the commonly used terms related to AMR; 8 true/false statements regarding knowledge of AMR; 8 statements related to AMR measured using a five-point "Likert scale" of agreement, where 1 denotes "Disagree strongly", 2 stands for "Disagree slightly", 3-for "Neither agree nor disagree", 4-for "Agree slightly", and 5-for "Agree strongly"; E: antibiotic use in the community: one question on antibiotic use in agriculture and food products. The questions from the section on the knowledge of antibiotics and the true/false statements from the "Knowledge of antibiotic resistance" section were scored as follows: 1 for each correct answer and 0 for an incorrect one or "Do not know". The knowledge scores for the questionnaire comprised of 12 questions with 14 correct answers were then categorized into "Good" (≥10 correct answers), "Moderate" (6-9 correct answers), and "Poor" (<6 correct answers).

Pilot Test
The questionnaire underwent preliminary pilot testing with subsequent revisions conducted among 15 respondents for initial validation. Necessary adjustments were made based on the feedback received from the respondents before finalizing the questionnaire. Three questions about obtaining antibiotics from a physician or nurse, vaccination, and washing hands from the original World Health Organization's (WHO) "Antibiotic resistance: Multi-country public awareness" survey were omitted, as most antibiotics can only be obtained from a medical practitioner and the latter were found to be out of the research topic. The face validity of the online questionnaire was also assessed for readability, length, and relevance of the questions by two pharmacists with postgraduate qualifications at the Institute of Health Sciences, UBD.
The internal consistency of the survey questions was determined using the Cronbach's alpha coefficient. The Cronbach's alpha values of the section on antibiotic use and knowledge were 0.66 and 0.86, respectively, i.e., satisfactory.

Data Analysis
The data collected in the web-based survey's database were exported into Microsoft Excel or other appropriate software. Data analysis was done using R statistical software (version 3.6) and Microsoft Excel. The data were summarized using descriptive statistics, which includes percentages, frequencies, and also means. Appropriate inferential statistics was also used according to the data distribution.

Ethical Approval
The study received ethical approval from the Research Ethics Committee of Pengiran Anak Puteri Rashidah Sa'adatul Bolkiah Institute of Health Sciences, Universiti Brunei Darussalam. All the participants were notified about the aims of the study, all the data collected were to remain anonymous, and confidentiality was strictly maintained. A written consent form was provided in the survey by ticking an option placed at the end of the cover letter prior to the distribution of the questionnaire. The study was conducted on a voluntary basis and respondents had the freedom to not participate in the online survey.

Antibiotic Usage
The results obtained for antibiotic use ( Table 2) showed that 69% (n = 90) of the students reported having previously used antibiotics. More than half of the students obtained directions to take antibiotics from a healthcare professional (81%, n = 98) and 12% (n = 14) did not get advice. Antibiotics were mostly acquired from public (58%, n = 70) and private hospitals (31%, n = 37) or health clinics, as they can only be prescribed by a physician. However, few of the students reported getting antibiotics from a friend or family member (4%, n = 5) and 3% (n = 4) of them had the antibiotics saved up from the previous use. Table 2. Experience of study participants in antibiotic usage.

Statements Frequency (n) Percentage (%)
When did you last take antibiotics?
In the last month 23 18 In the last 6 months 23 18 In the last year 16 12 More than a year ago 28 22 Can't remember 31 24 Did you get advice from a physician, nurse, or pharmacist on how to take them?

Knowledge about Antibiotics and Antimicrobial Resistance
More than half of the students (51%, n = 66) showed a good level of knowledge (score more than 10) on antibiotics and antimicrobial resistance with a mean total knowledge score of 9 out of 14.
Only 14% (n = 18) of the students scored below 6. Fisher exact test revealed that level of knowledge of the students was significantly different in relation to age (p = 0.001) and faculty (p < 0.001) but not between gender, nationality, place of resident, and year of study (Table 3). Good knowledge was found in students aged between 18 and 21 years old (p = 0.001) and in Health Sciences faculty (p < 0.001). School of Business and Economics (SBE) 0 3 (7) 5 (28) Almost all the students, 92% (n = 119), agreed that antibiotics should be taken as a full course as directed. The frequency and the percentage of students for the statements regarding antibiotic use are presented in Table 4. It is okay to use antibiotics that were given to a friend or family member as long as they were used to treat the same illness Do not know 13 10 A large number of students correctly identified that antibiotics are used to treat bladder or urinary infections (UTI) (72%, n = 93), skin or wound infections (67%, n = 87), and gonorrhea (39%, n = 51) ( Figure 1) [35]. Moreover, students incorrectly classified cold and flu (41%, n = 53) and fever (40%, n = 52) as conditions that can be treated with antibiotics. Similarly, the use of antibiotics was also reported to be appropriate for sore throat (47%, n = 61) and diarrhea (28%, n = 37).

Question/statements Frequency (n) Percentage (%) When do you think you should stop taking antibiotics once you have begun treatment
When you feel better 10 8 When you have taken all of the antibiotics as directed 119 92 Do not know 1 1 It is okay to use antibiotics that were given to a friend or family member as long as they were used to treat the same illness A large number of students correctly identified that antibiotics are used to treat bladder or urinary infections (UTI) (72%, n = 93), skin or wound infections (67%, n = 87), and gonorrhea (39%, n = 51) ( Figure 1) [35]. Moreover, students incorrectly classified cold and flu (41%, n = 53) and fever (40%, n = 52) as conditions that can be treated with antibiotics. Similarly, the use of antibiotics was also reported to be appropriate for sore throat (47%, n = 61) and diarrhea (28%, n = 37).

Knowledge about Antibiotic Use in Agriculture and Food-Producing Animals
Only few of the students (25%, n = 33) reported that they were aware about the use of antibiotics in agriculture and food products in the country, and more than half (69%, n = 90) of them were unsure about it.

Discussion
This study assessed the knowledge of antibiotics and antimicrobial resistance of the students. To the extent of the author's knowledge, this is the first study carried out among Bruneian university students.
A quite high degree of antibiotic consumption was evident in the study. Sources of antibiotics were mostly public and private hospitals or health clinics, as all antimicrobials in Brunei are classified as prescription-only medicines. This is unlike many developing countries where antibiotics can be acquired without a valid prescription, which is commonly practiced among university students in China, India, and Nigeria [23,36,37]. The greater antibiotic consumption could be due to the easy access of healthcare in Brunei, which may cause excessive prescribing of antibiotics, and this correlates with a study in Malaysia where the rates of antibiotic prescribing were indeed high in both public and private primary care settings [38]. Thus, the first National Antibiotic Prescribing guidance published in 2019 was expected to minimize the unnecessary prescribing of antibiotics and to be adopted as a standard practice among all healthcare providers. This in part shares principles of the WHO's systematic approach to the good prescribing practice in general, which can help minimize poor-quality and incorrect prescribing [39]. This can also be used as a referral for the prescribers to practice and ensure appropriateness of antimicrobial use. Further, Brunei also initiated a national strategic plan for 2019-2023 to tackle antimicrobial resistance follow the World Health Organization (WHO). This was implemented to ensure appropriate education and awareness is provided to the public and reduce the growth of resistance in the country.
Moreover, there were only few respondents found who had not received advice on how to take antibiotics and the need to complete the full course. Those who did not obtain advice are more likely to stop taking antibiotics when they feel better, which eventually leads to the growth of resistance in the community. Respondents also reported obtaining antibiotics from the previous use, but the rate was lower than in the previous studies in Malaysia (46/204), Qatar (161/596), China (1,965/11,192), and Saudi Arabia (165/347) [25][26][27][28]. There were more female students than male in this study, which is comparable to many other studies [8,25,29]. Similarly, a few respondents shared antibiotics with their friends or family members, which was also reported in Nigeria (5/400), the UK (3/242), and Jordan (76/1,158) [30,31,37]. The use of leftover antibiotics and antibiotic sharing by the respondents portrayed the non-compliance with antibiotic therapy and showed that the knowledge on antibiotic use is still lacking. Hence, it is important for healthcare providers to highlight the importance of taking antibiotics for the full course and advise patients not to stop taking antibiotics when the condition is better. Healthcare professionals can also recommend the public to return leftover antibiotics to prevent future use, which is unsafe and hence should be hindered. A pharmacist, too, can play a role in counselling patients on the possible risk if the course of antibiotic therapy is incomplete.
Furthermore, most of the students demonstrated good knowledge of antibiotics and antimicrobial resistance. The majority correctly identified conditions that can be treated with antibiotics, namely, bladder or urinary infections, skin or wound infections, and gonorrhea as suggested by the WHO in the antibiotic resistance survey. However, the misconceptions regarding the use of antibiotics for viral infections were also noted in the study, which was consistent with findings from other studies. The proportion was lower than in Jordan (527/1158), and Jatinangor, Indonesia (145/250), but higher than in Italy (210/1050) [31][32][33]. Sore throat and diarrhea were also reported appropriate for antibiotic use. Sore throat is a self-limiting viral illness which does not require the use of antibiotics and can usually be managed easily [40]. Lack of understanding on the difference between bacterial and viral infections could be the reason for the choices and this inappropriate choice can cause development of resistance if the erroneous belief is not addressed. In addition, respondents were aware of the terminology used related to antimicrobial resistance, but not the acronym AMR and superbugs. The reason for this is not known, but most likely because the acronym is rarely used to describe antibiotic or antimicrobial resistance in Brunei and the word "bug" is also not commonly used to identify germs, bacteria, or viruses. Pre-university and university lectures were the main source where the students heard about the term. There was a difference in the students from science and non-science faculties in recognizing terminology, since most of the respondents were from science faculties, namely, the Faculty of Science and the Institute of Health Sciences, so they were more exposed to the terminology than the non-science students. As for the knowledge of antimicrobial resistance, more than half of the respondents mistakenly believed that antibiotic resistance occurs due to the body becoming resistant to antibiotics, when in fact these are the bacteria that are resistant to antibiotics, and this was also seen in a study in Sri Lanka [41].
This study has several limitations. The results of the study may not be extrapolated to other universities, since it was conducted at one university. Other limitations of the study include the risk of response bias, as the findings of the survey were solely based on the self-reported data.

Conclusions
Although a good level of knowledge was found in this study, there are still gaps in areas of antibiotic use, especially the part on the appropriate antibiotic use for certain disease conditions, as some mistakenly considered antibiotic therapy for viral conditions. The current study findings provide baseline data for future research studies. However, further research is needed on this topic, especially to assess the attitudes and practice of antibiotic use among the students and not just focus on knowledge so that appropriate interventions can be carried out. Awareness of the proper use of antibiotics among the students is greatly required to correct their misconceptions and prevent the rise of antimicrobial resistance.