Abstract
Aims:
To evaluate the effect of biomedical students' ongoing education, we assessed their knowledge and attitudes toward antimicrobial use.
Study Design:
A cross-sectional study was carried out among the students of four study programs: Medicine in Croatian, Medicine in English, Dental medicine, and Pharmacy. The anonymous questionnaire was distributed to students who attended classes from April to May 2018.
Results:
A total of 947 (86%) out of 1,107 students enrolled at the University of Split School of Medicine participated in this study. A third of dental students (51/159) and a quarter of medical (113/458) and pharmacy students (32/130) believed that paracetamol was an antibiotic that reduces pain. However, the percentage significantly decreased from the first to the final years. Only 31% of the final year dental medicine students (5/16) named a correct guideline for the usage of antimicrobial drugs, 23% of medical students (18/78), and none in the English program. Pharmacy students were the most informed, since 76% of the final year students (16/21) named Intersectoral Coordination Mechanism for the Control of Antimicrobial Resistance (ISKRA) guidelines.
Conclusion:
The students showed poor knowledge on the use of guidelines for antibiotic use, highlighting the need for changes in the existing curricula, including a more effective course on antimicrobial prescribing.
Introduction
The ability to treat infectious diseases with antimicrobial drugs is considered as an essential component of medical training. Unlike many other drugs prescribed by a limited number of well-trained specialists in a given field, antimicrobial drugs are prescribed by all medical and dental practitioners in different areas of practice, regardless of their training or knowledge.1–3 Educational initiatives on the prudent prescription of antimicrobial drugs, for both health care professionals and students, as well as the general population, should be promoted.4,5 Particularly, the focus should be directed toward the next generations of future prescribers. 6 Effective education on appropriate antimicrobial use has been achieved to varying degrees in different countries.1,4,7
According to the database of the European Center for Disease Prevention and Control (ECDC) from 2017, Croatia is in the middle among European Union countries with respect to consumption of antimicrobials for systemic use in the community (primary care) and hospital sector. 8
The University of Split School of Medicine (USSM) is one of four medical and dental schools in Croatia, with one of three medical studies in English and one of two pharmacy studies, which makes our student body a representative sample of future medical professionals in the entire country. In addition, students enrolled in our English medical program return to practice medicine in their home country (e.g., Germany and Scandinavian countries) after graduation. According to Cars et al., 9 the education of the future health care professionals on rational antimicrobial prescribing is an integral part of all antimicrobial resistance containment activities; therefore, we find it crucial to focus on the students of these professions. The objective of our study was to evaluate and compare the knowledge, attitudes, and behaviors of all years of the medical, dental, and pharmacy students at the USSM on antibiotic usage and antibiotic resistance.
Materials and Methods
Study design
A cross-sectional study was carried out among the students of four study programs: Medical studies in Croatian, Medical studies in English, Dental medicine, and Pharmacy, enrolled at the USSM in Split, Croatia. All students enrolled into one of the four studies were eligible as participants. Four hundred fifty-eight out of 514 medical students in Croatian, 200 out of 247 medical students in English, 159 out of 197 dental students, and 130 out of 149 pharmacy students participated in this study.
Participants
The questionnaires were administered to students of all academic years (1–6 for medical studies and dental medicine and 1–5 for pharmacy), attending regular classes during the period of 2 months, April and May of 2018. The participation was voluntary, anonymous, and without compensation. A total of 947 students out of 1,107 enrolled at the USSM participated in this study.
Questionnaire and variables
The background and the aim of the research were explained in the first part of the questionnaire.
The questionnaire was composed of three parts, developed according to previously validated surveys from similar studies.1,4 It was translated into the Croatian language for Croatian students in the medical, dental, and pharmacy programs.
For the first part of the questionnaire the students provided their general data: sociodemographic characteristics such as age, gender, study program, and year of the study. Students also stated whether they had the relatives working in a health-related field and if they consumed any antibiotics within the last year. They also answered whether they were aware of the guidelines on the usage and prescription of antimicrobials and, if yes, which one(s).
In the second part, students' practices and knowledge on the usage and resistance to antimicrobials were addressed with 11 questions, and dichotomous answers (yes/no) were given.
The third part evaluated students' attitudes and knowledge on antibiotic usage, resistance, and adverse effects through 16 statements, using a 5-point Likert scale (from minimum 1 to maximum 5) with responses ranging from “Strongly disagree” to “Strongly agree.” 4
Statistical analysis
The results were analyzed using the Microsoft Office Excel 2016 program and JASP 0.9.2.0.
A descriptive analysis was conducted, with the results expressed in frequencies and percentages for dichotomous variables and as mean with standard deviation (SD) for continuous variables, which were initially tested for normality using the Kolmogorov–Smirnov test.
The outcomes on the attitudes and knowledge were described with absolute numbers and percentages. The percentages were calculated for every outcome. Nonparametric chi-square test was used to assess differences between groups and correlations between variables. For this purpose, the answers from the 5-point Likert scale were then divided into two groups to create dichotomous variables, grouping the “totally agree” and “agree” (as agree) and “totally disagree” and “disagree” (as disagree).
Ethical approval
The study was approved by the Ethics committee of the USSM (Approval No.: 2181-198-03/0001). The authors confirm that the research has been conducted in full accordance with the World Medical Association Declaration of Helsinki.
Results
In this study, 947 (85.6%) out of 1,107 students from four programs participated: 458 (89.1%) from Medical studies in Croatian, 200 (81%) from Medical studies in English, 159 (80.7%) students from Dental medicine, and 139 (93.3%) Pharmacy students. Among the students, 72.2% were females. The mean age of the participants was 21.9 (SD ±2.2), with a range from 18 to 41 years. A total number of 482 (50.9%) students declared to have relatives working in a health-related field, and 39.4% stated to have taken antibiotics in the last year. There was a significant difference between the students from four different studies when it comes to having relatives in a health-related field (χ 2 = 39.44, p < 0.001), but no statistical difference in taking the antibiotics within the last year (Table 1).
General Characteristics of the Students Enrolled at University of Split School of Medicine in 2018
We found no correlation between the students with a relative in a health-related field and a lower likelihood of taking antibiotics only when prescribed. However, there was a correlation between students having health worker relatives and keeping the leftover antibiotics (χ 2 = 43.26, p < 0.001), since 44.4% of the students with relatives in a health-related field stated that they kept leftovers at home, unlike 24.1% of the students without relatives in that field that kept leftover antibiotics (data not shown).
In total, 43.2% of students stated that they were familiar with the guidelines for the usage of antimicrobial drugs (Table 1). However, most of the students from the first to final academic year of all studies under guidelines named the following: “we shouldn't stop taking antibiotics if we feel better,” “antibiotics should not be mixed with alcohol,” and “antibiotics should be taken with food and dairy products” and other similar claims. Fourth, fifth, and sixth year students correctly named domestic or international guidelines, including 37 students from Medical studies in Croatian, 2 students from Medical studies in English, 7 students from Dental medicine, and 16 Pharmacy students. Significant differences were found between the students of these four study programs concerning their familiarity with the guidelines (χ 2 = 37.51, p < 0.001) (Table 2). There was no significant difference between male and female students.
The Students' Familiarity with the Guidelines for Antimicrobial Drugs and Naming the Specific Guidelines by Their Study Program and Academic Year at University of Split School of Medicine in 2018
When it comes to practices and knowledge on antibiotic usage, 17% of students used antibiotics for a sore throat and 8.6% for fever. About 20% of students reported to have stopped taking antibiotics upon feeling better, with 34.4% stating to have leftover antibiotics and 13.7% reported to have used leftovers, without consulting a physician. About 26% of students used antibiotics after a phone call to a physician, without examination. Twenty-four percent of students answered that paracetamol was an antibiotic, which reduces the pain and inflammation (Table 3). However, the largest percentage of students that provided this answer were first or second year students (around 50% of the first year medical studies in Croatian and dental medicine), and these percentages decreased toward the final years. Interestingly, around 5% of final years' students (fifth and sixth for medicine and dental medicine and fourth and fifth for pharmacy) believed that paracetamol was an antibiotic (data not shown). Moreover, around 5% of medical students in Croatian and pharmacy students did not agree with the statement that amoxicillin or penicillin were antibiotics (data not shown). Significant differences were found among the students from four different studies and their practices and knowledge on antibiotic usage and antibiotic resistance (Table 3).
Students' Practices and Knowledge on Antibiotic usage and Antibiotic Resistance from University of Split School of Medicine Four Study Programs: Medical Studies in Croatian, Medical Studies in English, Dental Medicine, and Pharmacy in 2018
Chi-square test.
Students' attitudes and knowledge on antimicrobial usage, prescription, and antibiotic resistance by study program at the USSM are summarized in Table 4. Students agreed that the usage of antimicrobials is frequently uncritical, over exaggerated, and unnecessary (73%) that antimicrobial resistance is a great global issue (86%) and that rational/critical use of antimicrobials can reduce resistance problems (89%). Five percent of students believed that viral infections are cured by antibiotics and 19% that fungal infections are cured by antibiotics. The respondents disagreed with the statement that antimicrobial resistance causes problems only in hospital environments (72%) and that the usage of antimicrobials in every oral inflammatory process treatment is justified (70%). Forty-three percent considered their knowledge to be quite satisfactory. Students also reported that they need continuous education on antimicrobial drugs (77%) (Table 4). There were statistically significant differences between the four school programs concerning the following statements: the usage of antimicrobials is frequently uncritical, over exaggerated, and unnecessary; viral infections are cured by antibiotics; fungal infections are cured by antibiotics; and my knowledge about antimicrobial drugs is quite satisfactory (p < 0.001) (Table 4).
Students' Attitudes and Knowledge on Antibiotic Usage and Antibiotic Resistance from University of Split School of Medicine Four Study Programs: Medical Studies in Croatian, Medical Studies in English, Dental Medicine, and Pharmacy in 2018
Chi-square test.
Discussion
In this study, we aimed to assess the knowledge, practices, and attitudes of medical, dental, and pharmacy students at the University of Split on antibiotic usage and antibiotic resistance.
In general, the students recognized the importance of appropriate antimicrobial usage; however, they did not always practice according to what they learned. The students showed poor knowledge on the use of guidelines for antimicrobial drugs.
Although almost half of the students stated that they were familiar with the guidelines for the usage of antimicrobial drugs, when it came to naming them, the results were unsatisfactory. The correct guidelines were named only by fourth, fifth, and sixth year students in very low percentages: 18% students from Medical studies in Croatian, 3% of students from Medical studies in English, 9.5% from Dental medicine, and 32% of fourth and fifth year Pharmacy students. Pharmacy students were the most familiar with the guidelines, which included the Intersectoral Coordination Mechanism for the Control of Antimicrobial Resistance (ISKRA), MEDIATELY, Centor criteria, Swedish strategic programme against antibiotic resistance (STRAMA), Infectious Diseases Society of America (IDSA), and American Heart Association (AHA). ISKRA guidelines represent Croatian national guidelines from several branches of medicine where antimicrobial therapy plays a significant role in treatment. In their study, Abbo et al. found that fourth year medical students at three universities in the United States reported the use of IDSA by 24–41% of respondents, and 35–57% of students used guidelines by other professional organizations. 1
In our study, about 40% of students stated to have used antibiotics in the last year. Seventeen percent of students took antibiotics for a sore throat and 8.6% for fever. In a similar study, about one-tenth of dental students stated that antibiotics can be used for the flu (7%) and common cold (11%). 10 Huang et al. reported that 13.6% of students took antimicrobials for the common cold, 11 and Khan et al. reported that 38% of students stated that antibiotics should be taken when developing a cold and 60% believed that taking antibiotics for a cold made them feel better more quickly. 12
Our results showed that 5% of students believed that viral infections were cured by antibiotics and 19% that fungal infections are cured by antibiotics. The results of Scaioli et al. showed that as much as 16% of students considered antibiotics appropriate for viral infections. 4 Scaioli et al. 4 also showed that medical students in Torino with relatives in a medical field would more often use antibiotics without a prescription from a health professional. Although Italy and Croatia belong to the similar Mediterranean cultural region, our results were somewhat different. Namely, we found no correlation between the students with a relative in a medical field and a lower likelihood of taking antibiotics only when prescribed; however, we did find a correlation between students having the health worker relatives and keeping the leftover antibiotics at home.
A large percentage (87–99%) of students took antibiotics only if prescribed by a physician. It is interesting that older students are more likely to take antibiotics if they are not prescribed by a physician, and the largest number of such students was in the last year of all study programs. Almost half of medical students in the English program and one third of Croatian medical students have antibiotic reserves at home, if needed. Our data are in accordance with the study conducted on the final year medical and pharmacy students where 36% of students kept a stock of antibiotics. 13 This practice has been demonstrated in other studies; however, the behavior can be associated with cultural characteristics in countries such as India and Jordan where students often share drugs with roommates and friends.12,14,15
The highest percentage of students, almost one-fourth, was medical students in Croatian that reported to have stopped taking antibiotics when starting to feel better, before the end of therapy, followed by one fifth of dental students. Although these numbers decrease toward higher academic years, the numbers of students in the final years are still relatively high, with 15% of students in the fifth year and the same percentage in the sixth year. Even more worrying is the percentage of students in the sixth year of dental medicine, where 25% of students practice this kind of behavior.
Our findings are similar to results from students in Italy where more than 15% declared to stop taking antibiotics when symptoms improve and to use leftover antibiotics without consulting a physician. 4
About a quarter of all students reported advising the family members or friends about starting antibiotic treatment, even from the early years of their studies.
A third of dental students and quarter of students in medicine and pharmacy believed that paracetamol is an antibiotic that relieves pain. This percentage significantly decreased from the first to the final years in all studies. Still, around 5% of final years' students (fifth and sixth or fourth and fifth for pharmacy) believed that paracetamol was an antibiotic.
About half of medical and pharmacy students and a third of students of medicine in English and dental medicine thought that their knowledge was satisfactory, and this percentage was exceptionally high for the last 2 years of all studies. However, about three-quarters reported that they still need continuing education on antimicrobial drugs, which is in line with attitudes of students from other studies.4,16–18
This study highlighted the problem that students encounter after graduation, which is the lack of knowledge on the guidelines for prescribing antimicrobials.
Our students take several different courses on antimicrobial drugs during their studies, for example, Pharmacology, Infectology, Medical Microbiology and Parasitology courses, and endodontics in dental medicine, which discuss the subject in more detail. In addition, a few lectures involving the antimicrobial drugs are given during the Surgery, Epidemiology, Otorhinolaryngology, Urology, and Gynecology courses in the fifth year. Pharmacy students take Pharmaceutical Microbiology in the second year, Special Pharmacology in the fourth year, and Clinical Pharmacology, Clinical Pharmacy, and Pharmacotherapy in the fifth year. However, our results emphasize the need to revise and improve the curricula with the introduction of an additional course that would integrate all the knowledge and provide practical advice and guidance on antimicrobials, such as Clinical Pharmacology or Rational Pharmacotherapy. In contrast to the USSM, it is indeed already a part of the curricula in some biomedical studies in the region. Because students as future medical practitioners still heavily rely upon senior colleagues for information and advice on antimicrobial usage, given the students' responses, it would be helpful to provide continuous education lasting throughout their studies and into medical practice.
The main strength of our study is that we are the first to investigate this issue among the whole health care professional student body in one of four universities with medical, dental, and pharmacy studies in Croatia, allowing a representative sample with a large number of our future biomedical experts and prescribers. Furthermore, we had a high rate of responses comprising a sample size that was 86% of the population.
The limitations include the fact that we did not collect formal data on curricula in either of the studies regarding antimicrobial use and resistance. A self-administered questionnaire instead of an interview with each student is also considered a limitation of the study. There is a possible recall bias due to all measures being based on self-reporting.
Conclusion
Our study provides an important insight into the knowledge, attitudes, practices, and perceptions of medical, dental, and pharmacy students in Split, Croatia, in regard to antimicrobial use and resistance. Even though the students have satisfactory theoretical knowledge, they do not always follow the learned facts and apply them in everyday life.
Given that these students will soon become practitioners and prescribe antimicrobial drugs, it is essential that they are not only properly instructed but also that they behave accordingly, to be a good role model for other members of society.
The students showed poor knowledge about the use of guidelines and it would be advisable to introduce changes to the existing curricula, such as continuous education and a more effective course on antimicrobial prescribing for students in the final years of their study program.
Footnotes
Disclosure Statement
No competing financial interests exist.
Funding Information
No funding was received for this article.
