Abstract
University students, especially those in healthcare sciences, are of particular importance in COVID-19 vaccine views since their future careers will allow them to educate citizens regarding vaccination. The study examined COVID-19 immunisation coverage, behaviours, and attitudes towards COVID-19 vaccines among students in Bulgarian medical universities. A prospective cross-sectional study was undertaken in September 2021- January 2022. Demographics, university programme, year of study, general vaccine attitudes and behaviour, and personal experience with COVID-19 and vaccines were collected. The chi-square test was used to test for associations and binominal logistic regression to identify possible predictors for vaccination. A total of 3050 students with a median age of 22 years, predominantly female participated. Three-quarters of the students (73.5%) have been vaccinated against COVID-19. An association was found between COVID-19 vaccination and influenza vaccination in the previous season (χ2 = 67.15, p < 0.001) as well as the intention to receive the flu vaccine in the current season (χ2 = 142.83, p < 0.001). Vaccine hesitation mainly stemmed from fear of side effects and safety concerns, but non-vaccinated students voiced them more often. Respondents who were less likely to be vaccinated considered themselves to have: (a) limited access to sufficient information to allow them to make an informed decision to vaccinate against COVID-19; (b) lack of public awareness and education campaigns about COVID-19 vaccines; (c) insufficient information about COVID-19 vaccines during university education that would allow them to make an informed decision to vaccinate; and (d) had a positive COVID-19 diagnosis. Informational initiatives that emphasise vaccine safety will boost COVID-19 immunisation coverage.
Introduction
Four years after the World Health Organization (WHO) declared the Coronavirus Disease 2019 (COVID-19) a pandemic, as of February 11, 2024, worldwide confirmed cases are 774,631,444, including 7,031,216 deaths (0.90%) [Citation1]. The WHO European Region ranks first in terms of registered cases (275,774,521) and second regarding the number of deaths (2,245,481) (lethality 0.81%) [Citation1]. For the same period in Bulgaria, which belongs to upper middle-income countries, the registered number of cases is 1,309,601 with 38,442 deaths or 2.93% lethality [Citation2].
Antiviral medications show promise in preventing severe illness. However, the most effective solution is the development and implementation of safe vaccines through a vaccination programme [Citation3].
The immunization campaign in Bulgaria started on December 27, 2020, with the participation of publicly known personalities with a view to a more significant impact on the population regarding the choice of vaccination. Since the end of the summer of 2021, COVID-19 vaccines have been freely available to the population. Despite this, the country still has the lowest immunization coverage among European countries (30.1% of the population has completed a vaccination course, or 2,080,272 persons) [Citation4], and the total number of vaccines administered from the beginning of the immunization campaign until July 20 2023 was 4,613,280 [Citation2]. The variables associated with the success of an immunization program are vaccine safety and patient adherence [Citation5], and according to the WHO, vaccination hesitancy ranks among the top ten threats to human health globally [Citation6].
University students, particularly those in the healthcare disciplines, are a group of individuals who warrant special attention due to their potential to assume a crucial professional role in disseminating information and educating the public about vaccination. Undoubtedly, the favorable perspective held by university students offers considerable potential to have a substantial impact on societal patterns [Citation7, Citation8].
Vaccine hesitancy poses a persistent and ongoing challenge to public health, potentially impeding the achievement of herd immunity through vaccination. Despite the substantial body of data regarding the advantages of immunization, there persists a widespread amount of misunderstanding and skepticism surrounding the information pertaining to the effectiveness and safety of vaccines [Citation8]. Key barriers to vaccination are insufficient knowledge and confidence, limited vaccine accessibility, concerns about the efficacy and safety of vaccines, and religious beliefs [Citation9]. A number of conspiracy theories, which are widespread on social media, serve to further bolster these challenges [Citation10]. In 2018, Gallup International and the King Baodoin Foundation surveyed 28,782 respondents from 28 EU member states. In this study, Bulgaria is the country in which agreement with the statement that vaccines are safe is expressed by the smallest relative share of respondents (66%) [Citation11].
Vaccine hesitancy is present among healthcare professionals, which is unexpected. Vaccinating healthcare workers is crucial for reducing the spread of viruses because they are well-equiped to address patient concerns, provide information and explain the importance and benefits of vaccination clearly and effectively [Citation10,Citation12]. Nevertheless, an increasing number of research investigations have documented a notable decline in the acceptance rates and a significant increase in the degrees of hesitancy toward COVID-19 immunization among healthcare professionals, encompassing medical doctors, nurses, dentists, and other relevant healthcare providers who are directly involved in administering vaccinations to patients [Citation13, Citation14].
The aim of this study was to examine the COVID-19 vaccination coverage among students enrolled in different degree programs at medical universities in Bulgaria and to investigate behaviors and attitudes towards COVID-19 vaccination. Furthermore, the study aimed to identify potential predictors that may influence students' decisions regarding vaccination.
Materials and methods
A cross-sectional study using a semi-structured anonymous questionnaire was conducted among students in Bulgarian medical universities in the period September 2021– January 2022. The questionnaire was distributed to the students enrolled in the universities via the online teaching platform of each university.. Participants ≥18 years old and currently full-time students enrolled in one of the medical universities in Bulgaria (Medical University of Sofia, Medical University of Plovdiv, Medical university of Varna, Medical University of Pleven, Trakia University, Stara Zagora, Faculty of Medicine, Sofia University “St. Kliment Ohridski”) were enrolled. A total of 3050 students participated in the study.
The questionnaire was prepared both in Bulgarian and in English using Google Forms, and it consisted of four panels. The front page of the questionnaire included a description of the study and consent forms with an opt-out option if the respondent was not willing to continue further.
The first panel of the questionnaire gathered information about the demographics of the participants: age, sex, place of residence, university, main subject of study, and year of study. In the first section of the questionnaire, the respondents were asked whether they had been vaccinated against COVID-19 and, if so, what type of vaccine they had received.
The second section of the questionnaire collected information regarding the general attitudes and practices of the participants toward vaccines - vaccination with mandatory vaccines included in the immunization calendar and vaccination with recommended vaccines, more specifically influenza vaccine.
The third panel consisted of questions examining the attitudes of the participants toward COVID-19 vaccines, such as personal opinions on the importance of vaccination with a COVID-19 vaccine, drivers for vaccine hesitancy such as fear of possible undesirable adverse events, and the tendency to believe conspiracy theories.
The fourth section of the questionnaire consisted of questions exploring the personal experience of the respondents with COVID-19, such as having been infected with the virus and personal experience with COVID-19-related disease or death of close relatives and friends.
The questions exploring the attitudes of students toward mandatory vaccines and COVID-19 vaccines were 5-point Likert-type agreement items: from 0 (strongly disagree) to 4 (strongly agree).
A group of professionals with expertise in biostatistics and ethics [one biostatistician (with postgraduate specialties in “Medical Informatics and Health Management” and “Health Economics”); four epidemiologists (with postgraduate specialties in “Epidemiology”); and one MD (with a postgraduate specialty in “Social Medicine and Public Health”)] adapted the questionnaire following a thorough examination of relevant literature [Citation15–17]. The team also discussed whether the questions were acceptable and understandable, taking into account the training type and level of the students who would sign up.
The questionnaire was disseminated through the cloud-based team collaboration software part of Microsoft 365-MS Teams and reached all students in the Medical Universities in the country (approx. 10,000 students). During the research period, universities utilized this platform to online teaching. During the first and third weeks following the initial distribution of the questionnaire, two sets of reminders were dispatched to the student participants. To exclude duplicate responses, the format of the response form of the questionnaire was restricted to one response per person. The response rate in our study was determined to be 30%.
Statistical analysis
Descriptive statistics was used for: (1) quantitative variables, which are presented as mean (standard deviation) and median (25th percentile; 75th percentile) when variables lack normal distribution; and (2) qualitative variables, which are presented as frequencies and percentages (n and %). Continuous variables were tested for normality of statistical distribution by the Kolmogorov-Smirnov test. Comparative analysis between the medians of two groups was perfrormed with the Mann-Whitney test for independent samples and between two groups' proportions with the z-test. Based on the independent variables introduced in the model with a p < 0.10 identified by univariate analysis, binominal logistic regression was used to estimate the probability that an observation falls into one of two categories of a dichotomous dependent variable—COVID-19 vaccination—based on multiple independent variables. Odds ratios [OR] and 95% confidence intervals [95% CI] for the fixed effects were calculated. The systematization, processing and analysis of the data were performed using SPSS v.26 for Windows (IBM Corp., Released 2019; Armonk, NY: IBM Corp.).
Ethical considerations
The study received approval from the Ethical Committee of the Medical University of Plovdiv, Bulgaria (R651-2022/01/Dec/2021). The research was conducted in full accordance with the principles of the Declaration of Helsinki [Citation18]. The present study was performed following the Strengthening and Reporting of Observational studies in Epidemiology (STROBE) guidelines [Citation19].
Results
In the present study, 3050 students filled out the questionnaire (). The median age was 22 years (25th percentile 20 y.o; 75th percentile 24 y.o). The female respondents predominated (n = 2056, 67.4%). The substantial share of international students enrolled in English-based degree programs at medical universities in Bulgaria required the development of a bilingual questionnaire survey tool. There were 814 (26.7%) responses from English-speaking students. A significant proportion of participants were enrolled in the Medical University of Plovdiv. (n = 1669, 54.7%). There was an almost equal distribution of students regarding the year of study, whereas more than half of them responded that they were studying medicine (n = 1748, 57.3%).
Table 1. Demographic characteristics of the respondents (n = 3050).
Almost three-quarters of the students had been vaccinated against COVID-19 (n = 2241, 73.5%). There were statistically significant differences among the vaccinated and unvaccinated respondents concerning their enrolment in language-based degree programs, year of study, and degree programs ().
General attitudes and practices towards vaccines
Of all respondents, 487 (16%) had received the influenza vaccine in the previous season, and the majority of them were studying medicine (n = 335, 68.8%) (). When further asked whether they planned to receive the flu vaccine in the flu season (2021/2022), 743 (24.4%) gave a positive response. Additionally, the proportion of students who had received the influenza vaccine and had chosen to receive the COVID-19 vaccine was significantly higher than that of the COVID-19 non-vaccinated ones (19.2% for COVID-19 vaccinated vs. 6.9% for COVID-19 non-vaccinated, p < 0.0001).
Table 2. Personal vaccination behavior and general attitudes of the respondents toward vaccines.
Personal experience with COVID-19 and COVID-19 vaccines attitudes
Almost half of the respondents reported having been infected with COVID-19 (n = 1340, 43.9%) (). In both groups of vaccinated and non-vaccinated students, there was a high share who personally knew someone who had had a COVID-19 infection history and someone who had died of COVID-19. When exploring the attitudes of the respondents regarding the COVID-19 vaccines, we could clearly identify a difference between the two groups. A very small share of the unvaccinated students believed that the COVID-19 vaccines were important for them as future healthcare providers and that they should be mandatory for healthcare workers (HCW) (n = 72, 8.9%, and n = 58, 7.2%, respectively). Additionally, the non-vaccinated respondents tended to believe in conspiracy theories to a greater extent, such as that the COVID-19 vaccines have been developed too quickly (n = 324; 14.4% for COVID-19 vaccinated vs. n = 555, 68.6% for COVID-19 non-vaccinated respondents respectively Pearson χ2 test = 1035.10, p = 0.000) and that they might be part of a conspiracy plan (n = 163; 7.2% for COVID-19 vaccinated vs. n = 294, 36.3% for COVID-19 non-vaccinated respectively Pearson χ2 test = 706.91, p = 0.384). The main reasons for vaccine hesitancy in both groups of students were the fear of side effects and the doubts about the safety of the vaccines, although non-vaccinated students significantly more frequently express those fears. When it comes to the main source of information in regard to COVID-19 vaccines, the vaccinated students showed a significantly more pronounced trend to rely on official sources (Ministry of Health (MOH), World Health Organization, Center for Disease Control and Prevention(CDC)) (n = 2008, 89.6% vs. n = 522, 64.6% Pearson χ2 test = 264.35, p < 0.001), and university teachers (n = 942, 42.0% vs. n = 281, 34.8% Pearson χ2 test = 13.19, p < 0.001) compared to non-vaccinated students.
Table 3. Personal experience with COVID-19 and COVID-19 vaccines attitudes.
Logistic regression to identify potential variables that influence students' decisions regarding vaccination
A binomial logistic regression was performed to predict the probability that an observation falls into one of two categories of a dichotomous dependent variable. COVID-19 vaccine vaccination is based on multiple independent variables (). The model was statistically significant: χ2 (42) = 2074.65, p = 0.000. The model explained 72.0% based on Nagelkerke R2 and 50% based on Cox and Snell R2 of the variance in COVID-19 vaccination and correctly classified 89.6% of cases. The model adequately fitted the data: χ2 (8) = 9.70, p = 0.286 (Hosmer and Lemeshow test).
Table 4. Binominal logistic regression model for COVID-19 vaccination.
Bulgarian students were less likely to have received the COVID-19 vaccine compared to international students (odds ratio [OR] 0.42, 95% confidence interval [CI] 0.27–0.68). Medical students were more likely to be vaccinated in comparison with students in the following degree programs : Health care management (OR = 0.31, 95% CI 0.06–0.98), rehabilitation, wellness and SPA (OR = 0.12, 95% CI 0.01–0.98), Assistant pharmacist (OR = 0.17, 95% CI 0.07–0.73), dental technician (OR = 0.31, 95% CI 0.10–0.93), physical therapist (OR = 0.29, 95% CI 0.13–0.66), medical cosmetics (OR = 0.34, 95% CI 0.14–0.84), Medical laboratory assistant (OR = 0.30, 95% CI 0.11–0.83).
Students who felt responsible, as future healthcare professionals to be familiar with the types of vaccines for the patients' wellbeing, were more likely to be vaccinated than those who did not recognize themselves in that role (I neither agree nor disagree: OR = 1.72, 95% CI 1.07–2.76); I agree OR = 1.44, 95% CI 1.17–2.06). Compared to the students who highly valued the importance of COVID-19 vaccines, all the rest were less likely to undergo vaccination. Students who did not agree that the COVID-19 vaccination should be mandatory for medical personnel were less likely to receive such a vaccine. Concerns about possible side effects from the administration of the COVID-19 vaccine were reflected in the lower likelihood of vaccination in almost all categories. Students who did not believe vaccines were part of a conspiracy plan to reduce the population and that the virus was artificially created for this purpose were more likely to have a vaccination (OR = 1.82, 95% CI 1.14–2.92). Respondents who considered themselves to have (a) lack of access to sufficient information to inform about COVID-19 vaccination; (b) lack of public awareness and education campaigns about the effectiveness and safety of COVID-19 vaccines; (c) insufficient information about COVID-19 vaccines during university education; and (d) had a positive COVID-19 diagnosis were less likely to be vaccinated. Students who have not completed the mandatory immunization cycle according to the country's schedule were also less likely to have completed the COVID-19 vaccination.
Discussion
This study included students who were currently enrolled in various health degree programs at medical universities in Bulgaria. The focus of the study was on the acceptance of COVID-19 vaccines among these students, as well as the predictors that might indicate their likelihood of getting vaccinated. Considering the higher level of health literacy in our sample, the results of 73.5% vaccination coverage with the COVID-19 vaccine correspond to previous studies conducted in our country [Citation20]. These results are in line with the study of Gallè among undergraduate students from Central and Southern Italy [Citation21] as well as with international data on students in healthcare disciplines [Citation22–24]. A recent survey among medical students in Japan, found that 89.1% of participants had completed the administration of the second dose of the COVID-19 vaccination. Additionally, a significant majority of 90.7% expressed their willingness to receive the vaccine in the future [Citation22].
There was a discrepancy between the rates of COVID-19 vaccination among the students who took part in our study and the general population. According to the latest data in Bulgaria, the coverage with at least one of the COVID-19 vaccines is 30.1% in the general population, compared to 73.5% of students in our study [Citation4]. These results indicate that the towards COVID-19 vaccines was more positive among students enrolled in various health degree programs at medical universities than in the general population in Bulgaria.
Several studies conducted in Bulgaria highlight that one of the reasons for hesitancy among the general population is distrust in the healthcare system [Citation25, Citation26]. One of the potential causes of this issue could be attributed to the challenges faced by healthcare professionals in effectively disseminating vaccine-related information to their patients, as well as the communication barriers they may experience in the process.
A broader analysis of vaccine information sources on the Internet shows that claims often combine concerns about vaccine safety with expressions of varying degrees of mistrust of medicine in general, as well as specific strategies such as misinterpretation of scientific results and attacks on vaccine advocates [Citation27, Citation28]. University students can assist in spotting and correcting misinformation regarding COVID-19, especially misinformation about immunization. The significance of this role is particularly pronounced in the context of social media platforms, given the prevalence of younger demographics among social media users.
The higher relative share of those vaccinated among the foreign students can be attributed to two factors. Firstly, during the initial two years of the pandemic, there were specific requirements for a COVID travel certificate, which necessitated vaccination. Secondly, this trend can be seen as a reflection of the overall higher confidence in and immunization coverage of COVID-19 vaccines in Western and Central European countries compared to Balkan and Eastern European countries, including Bulgaria [Citation29].
In our study, the respondents studying medicine were more likely to be vaccinated compared to nursing or rehabilitator students, for instance, and the university program was one of the predictors of the intention of vaccination. Multiple studies indicate that medical students are more inclined to get vaccinated compared to the general public [Citation30,Citation31] as well as, students attending nursing schools, and dental students for an instance [Citation32–34]. This might be explained by the more advanced levels of education of medical students in epidemiology, immunology, and infectious diseases, which might result in a better understanding of COVID-19 research, the impact of vaccination, and higher resistance to conspiracy theories.
The respondents who were of the opinion that they had not received enough information regarding COVID-19 vaccines in order to make an informed choice for vaccination were less likely to have received the vaccine in our study. In order to enhance the overall confidence of healthcare workers (HCWs) in vaccinations, it is important to further improve their training and knowledge regarding vaccination. One of the findings of our study provides support for the significance of training and an enhanced informational campaign pertaining to COVID-19 vaccines among students in medical universities.
Several studies [Citation35, Citation36] have found that men are more likely to be vaccinated. This corresponds with our study—statistically significantly higher rates of COVID-19 vaccination were reported in males (n = 822, 82.7% for males vs. n = 1419, 69.0% for females, Pearson χ2 test = 64.329, p < 0.001), although it did not prove to be a predictor for possible vaccination.
A significant determinant for vaccination is any previous history of recommended vaccination (e.g. against influenza) [Citation37–39]. Prior research has indicated a potential association between vaccination intention and behavior across several vaccinations, as evidenced by the correlation found between the likelihood of receiving an influenza vaccination and the likelihood of receiving a COVID-19 immunization. [Citation40–42]. In our study, a statistically significantly higher number of COVID-19 vaccinated students had chosen to receive the influenza vaccine compared to the COVID-19 non-vaccinated respondents. On the other hand, one variable that was negatively associated with the likelihood of COVID-19 vaccination was the lack of a completed immunization cycle with mandatory vaccines according to the country's immunization schedule. These observations indicate that the likelihood of a new vaccine being widely accepted and adopted upon its release may be anticipated based on the favorable views of healthcare workers (HCWs) and the general public toward vaccines, whether they are compulsory or recommended.
The students who had a previous COVID-19 infection were less likely to be vaccinated, which might be due to the lower perceived risk of a subsequent infection and the false sense of protection against the virus. These results correspond to other studies [Citation43], although there are studies indicating that a history of COVID-19 infection is associated with a higher probability of vaccination [Citation44].
In our study, the concerns of possible side effects due to the COVID-19 vaccines and the lack of enough information about the vaccines were negatively associated with the likelihood of vaccination. Several similar studies [Citation45–47] reported that vaccine hesitancy was a result of concerns about the safety and possible adverse effects of the vaccine and a lack of reliable information. Contrary to this, the main reported adverse events in Bulgaria after the COVID-19 vaccination are mild to moderate pain at the injection spot, fatigue, headache, and muscle pains, which resolved in several days [Citation48]. These results correspond to studies regarding the adverse events after COVID-19 vaccines in other countries [Citation49, Citation50].
Lack of advanced vaccination knowledge and inaccurate vaccine information can cause worry, which can lead to an overestimation of potential side effects [Citation41]. This highlights the significance of providing healthcare workers with scientific information about the safety and efficacy of vaccines. To enhance healthcare workers' (HCWs) confidence in the COVID-19 vaccination and subsequently increase its acceptance among both HCWs and the general public, it is imperative to establish targeted communication strategies for the dissemination of safety information.
Interestingly, two variables that were predictive of a higher likelihood of vaccination were the perceived importance of the COVID-19 vaccines to stop the transmission of the disease and other related negative consequences, and the personal perception that it is important for students to be aware of the vaccines in general and the recommendations for vaccination as future HCWs. The results indicate that views about vaccination are shaped by factors beyond only information, including ethical considerations like moral obligation to society, consistent with previous research [Citation23].
Vaccination is a critical aspect of public health, and understanding the factors that influence it is essential for the development of effective vaccination strategies. To advance the understanding of vaccination, future research efforts should employ a multidisciplinary framework that considers the intricate interrelationships among social, cultural, economic, and psychological aspects. By considering these study directions, it is possible to enhance the efficacy of vaccination strategies that are specifically designed for various groups, therefore leading to better public health outcomes. In order for future HCWs to be better equipped to respond to the concerns and doubts of their patients regarding vaccination interventions, it would be beneficial for the curricula to aim to increase their knowledge, and to introduce teaching methods for successful communication (such as motivational interviewing). On the other hand, it is necessary to engage professionals in the field of digital communications to assist in the development and implementation of a professional, well-targeted communication strategy for the coming years, which will counter the misleading information circulating on the Internet.
Strengths and limitations
To the best of our knowledge, this is the first study to investigate the potential drivers of COVID-19 vaccination among Bulgarian students enrolled in various health degree programmes at medical universities in Bulgaria. The target group for our study is anticipated to have very high health literacy levels and frequently act as community opinion leaders in regards to vaccines and vaccination recommendations. The current study may shed light on the variations among health sciences students in terms of gender, academic year, and university programme with relation to COVID-19 vaccines and the motivations for vaccination. As with any survey-based study, non-respondents may have been reluctant to receive the recommended vaccinations, which can overstate the true rate of vaccine reluctance among this group of students. The study's snapshot scope inevitably limits it as a cross-sectional study, but because vaccine hesitancy levels have been constantly changing over time, prospective cohort studies are suitable for tracking these developments.
Although the questionnaire had been adopted and adapted to the psychometric characteristics, its validity may be questionable because of the lack of validity procedures for the Bulgarian population. Furthermore, we have examined self-reported attitudes, and it is important to consider the subjective nature of the responses.
Conclusions
The students in our study showed an overall positive attitude toward the COVID-19 vaccines and a higher rate of administration of the vaccine compared to the general Bulgarian population. There were discrepancies in the vaccination coverage between the students in different university programmes, which indicated the necessity of increasing the knowledge of health sciences students in the field of vaccines. Safety and quality issues with the vaccination were frequently raised. For these reasons, we supported the suggestion that promoting informational campaigns that emphasize the vaccine's safety will be more effective than emphasizing the disease's severity.
Author contributions
Conceptualization, VR and AK; methodology, VR, MB, and NI; software, RR; validation, VR, RR, MB, and AK; formal analysis, VR; investigation, VR, TP, and MK; resources, VR, TP, and MK; data curation, SS and NP; writing—original draft preparation, VR; writing—review and editing, VR, RR, AK, and NI; visualization, VR; supervision, RR and AK; project administration, VR. All authors have read and agreed to the published version of the manuscript.
Institutional Review Board statement
The study was conducted in accordance with the Declaration of Helsinki and approved by the Institutional Review Board of the Medical University of Plovdiv, Bulgaria (R651-2022/01/Dec/2022).
Consent form
Informed consent was obtained from all subjects involved in the study.
Disclosure statement
The authors reported no potential conflicts of interest.
Data availability
The data that support the findings of this study are available from the corresponding author, V.R., upon reasonable request.
Additional information
Funding
References
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