Introduction
Health science students are exposed to a variety of vaccine-preventable diseases (VPDs) through clinical encounters during their undergraduate training, e.g. varicella zoster virus (VZV), hepatitis B virus (HBV) and influenza.(1,2) Infected students may transmit infections to their patients, colleagues and the community.(2) Nosocomial outbreaks of VPDs have serious implications for health-care facilities, such as additional staff time and expenses for investigating and controlling these outbreaks. More importantly, these outbreaks have severe consequences for hospitalized patients, such as prolonged length of stay, increased morbidity and even mortality. Pathogen transmission to other susceptible health-care workers may result in staff absences, service disruption and increased workload for the remaining staff. From the students’ perspective, occupationally acquired VPDs may cause disruption to their academic studies through ill health and enforced absence.(3)
Health-care workers’ vaccination is a critical component of occupational health and safety and infection prevention and control programmes at health-care facilities.(1–5) Whereas comprehensive health-care workers’ vaccination is mandatory in most high-income countries, implementation and enforcement of such programmes in low-middle- income countries are low or absent.(4) In 2017, the World Health Organization (WHO) recommendations for health-care workers’ vaccination in low-middle-income countries included HBV, measles, rubella, influenza, polio, diphtheria, VZV and meningococcus (for high-risk groups).(6) The United States of America's Advisory Committee on Immunization Practices (ACIP) recommends that all health-care students receive and complete vaccination for VPD before commencing their clinical training.(1) Electronic records of vaccinations and serological proof of immunity are also recommended by ACIP for students and health-care workers in an effort to increase adherence to vaccination policies.(1–3)
In South Africa, HBV vaccination is recommended for health-care workers but not enforced. A study in Gauteng Province found that 67.9% of health-care workers had received one dose of HBV vaccination, but only 19.9% of health-care workers were fully vaccinated.(7) Another study among health science students in Greece also found significant immunity gaps against VPDs and that education about immunization and a formal system for coordinating vaccination of students was necessary.(8) Similarly, the recommendations and requirements for the vaccination of health science students at South African higher education institutions are not uniformly established or enforced.(4) This suggests a need for a uniform national policy for the prevention of HBV in health-care workers. At Stellenbosch University Faculty of Medicine and Health Sciences (SU-FMHS), only HBV vaccination is mandatory.(9) A recent study at SU-FMHS found that first-year medical students have insufficient immunity against five VPDs (hepatitis A virus, HBV, measles, rubella and VZV) and recommended the implementation of immunity screening and vaccination (booster) programmes.(10)
Given the need to develop a more robust health science student vaccination programme at SU-FMHS, a survey was conducted of health science students’ knowledge, attitudes and practices (KAP) regarding vaccination and preferences for the delivery of a student vaccination programme.
Methods
Study design, participants and analysis
SU-FMHS students who were registered for any of the five undergraduate health science degree programmes (MBChB, Physiotherapy, Occupational Therapy, Dietetics and Speech-Language and Hearing Therapy) in 2017 (n = 2472) were invited via email to participate in an anonymous electronic KAP survey. The survey was hosted on the university's Research Electronic Data Capture (REDCap) (11) platform; two invitations to participate were sent to students using the undergraduate students’ email lists between November 2017 and January 2018 of the university. The survey was developed by the study investigators and pilot tested by seven undergraduate students to ensure comprehensibility and relevance. Quantitative survey elements included questions related to participants’ demographics (n = 4), vaccination knowledge (n = 10), attitudes (n = 7), practices (n = 3) and preferences (n = 5), with some question responses allowing for multiple possible answers, and most attitude questions using a five-option Likert scale. Responses to three open-ended questions were data coded by two independent researchers to identify emerging themes using framework analysis. Survey responses from the REDCap platform were exported into an Excel spreadsheet for data cleaning. The STATA Statistical Software version 13.0 IC (StataCorp LP, College Station, TX) was used to analyse the data. The study population demographics were described using frequencies and proportions. Mean scores for overall vaccination-related knowledge (K), attitudes (A), practices (P) and preferences (Pref) were normally distributed on the Shapiro–Wilk test (i.e. >0.05) and were compared between medical and allied health students using a Student's t-test. For question K3 and question A1 (each with several sub-questions), the average score was calculated to produce a maximum score weight of 1. Responses to individual KAP questions were compared between medical and allied health students using the Pearson χ2 test. A p-value of ≤0.05 was considered statistically significant.
The approval for the study was granted by the Stellenbosch University Health Research Ethics Committee. All survey participants provided individual electronic consent.
Results
Demographics
A total of 403/2472 (16.3%) eligible undergraduate health science students completed the survey. By degree type, the survey response rates were MBChB 320/1789 (17.9%), Physiotherapy 31/233 (9.6%), Occupational Therapy 33/198 (16.7%), Dietetics 14/129 (10.9%) and Speech-Language and Hearing Therapy 3/123 (2.4%). Two participants omitted several questions and were removed from the study sample. The participants had a mean age of 21.5 years [standard deviation (SD) 2.3], were predominantly women (76.6%), and studied either medicine (79.8%) or an allied health professional course (20.2%) (Table 1). Most participants were in the clinical phase (practical training in hospital from year 3 onwards) of their studies (61.6%). Overall, 26.4% of respondents had participated in one or both of the previous vaccination activities for undergraduate students at SU-FMHS [a seroprevalence study (10) of students’ immunity to VPD in 2015 and two mass influenza peer vaccination sessions for the fourth year medical students in 2016 and 2017].
Survey participants’ demographics (n = 401).
| Variable | Frequency | % | ||
|---|---|---|---|---|
| Medical students | 320 | 79.8 | ||
| Course | Allied health students | Physiotherapy | 31 | 7.7 |
| Dietetics | 14 | 3.5 | ||
| Speech-Language and Hearing Therapy | 3 | 0.8 | ||
| Occupational Therapy | 33 | 8.2 | ||
| Total Allied Health students | 81 | 20.2 | ||
| Phase of study* | Pre-clinical | 154 | 38.4 | |
| Clinical | 247 | 61.6 | ||
| Gender (female) | 307 | 76.6 | ||
| Age in years, mean (SD†) | 21.5 | SD 19.2–23.8 | ||
Pre-clinical = years 1 and 2, clinical > year 2.
SD = standard deviation.
Knowledge
Participants scored a mean of 6.7 (SD 1.2) out of 10 questions regarding knowledge of health-care workers’ vaccination, with no significant difference between the scores of medical vs allied health students (p = 0.998) (Table 2). Most participants knew that vaccinations form part of standard infection prevention precautions (79.6%). More medical students knew that serological test results are an acceptable form of evidence of immunity to VPDs [290/320 (90.6%) vs 58/81 (71.6%); p < 0.001], whilst more allied health students regarded documentation from a vaccine provider as acceptable evidence of immunity [65/81 (90.2%) vs 196/320 (61.3%); p = 0.001]. Students were aware of the fact that they had to submit proof of HBV immunity (96.5%), but a few number of students knew by when (99/401; 24.7%) and where (117/401; 29.2%) the proof of immunity should be submitted.
Health science students’ knowledge of vaccination (n = 401)
| Knowledge questions (n = 10) | Total (n = 401) | Medical (n = 320) | Allied health (n = 81) | p-value + |
|---|---|---|---|---|
| Total Knowledge score, mean (SD) | 6.7 (5.5-7.9) | 6.8 (5.6-8.0) | 6.4 (5.3-7.5) | 0.998‡ |
| 1. Do vaccinations form part of standard precautions for healthcare workers? (Yes*) | 319 (79.6) | 254 (79.4) | 65 (80.2) | 0.862 |
| 2. Does receiving a vaccine mean that you are immune to the targeted disease? (No*) | 226 (56.4) | 174 (54.4) | 52 (64.2) | 0.111 |
| 3. For which diseases does the World Health Organization recommend routine vaccination for health-care workers (6) in 2017†? (Diphtheria, HBV, Influenza, Measles, Meningococcus, Polio, Rubella, Varicella Zoster) | 205 (51.1) | 171 (53.4) | 34 (42.1) | 0.081 |
| 4. Is self-report of vaccination acceptable as evidence of immunity to a disease? (No*) | 370 (92.3) | 296 (92.5) | 74 (91.4) | 0.731 |
| 5. Are parents’ reports of childhood illness acceptable as evidence of immunity to a disease? (No*) | 360 (89.8) | 290 (90.6) | 70 (86.4) | 0.264 |
| 6. Are serological tests acceptable as evidence of immunity to a disease? (Yes*) | 348 (86.8) | 290 (90.6) | 58 (71.6) | <0.001 |
| 7. Is documentation from a vaccine provider acceptable as evidence of immunity to a disease? (Yes*) | 261 (65.1) | 196 (61.3) | 65 (80.2) | 0.001 |
| 8. Are Stellenbosch University health science students required to submit proof of Hepatitis B immunity? (Yes*) | 387 (96.5) | 309 (96.6) | 78 (96.3) | 0.907 |
| 9. When should proof of immunity be submitted to Stellenbosch University? (End of year 1*) | 99 (24.7) | 85 (26.6) | 14 (17.3) | <0.001 |
| 10. Where should proof of immunity be submitted? (Campus health clinic*) | 117 (29.2) | 110 (34.4) | 7 (8.6) | <0.001 |
For question K3, the average score of several sub-questions was calculated to produce a maximum score weight of 1. Medical = Bachelor of Medicine and Bachelor of Surgery, Standard precautions = minimum infection prevention practices that apply to all patient care in any setting where healthcare is delivered,(12) HBV = hepatitis B virus.
Pearson's χ 2 test.
t-Test comparing medical and allied health students.
Correct response.
Including health science students.(6)
Attitudes
Participants provided desired attitude responses for a mean of 4.1 (SD 1.3) out of 7 questions, with similar scores for medical and allied health students (Table 3). A few number of students felt that they had received adequate information regarding recommended vaccinations (39.4%). The majority (93.5%) of students believed that it is necessary to test for HBV immunity after primary immunization. Most thought it should be compulsory to submit evidence of immunity for mandated vaccinations (91.3%). However, only 30.3% of students considered it their own responsibility to determine which vaccines they still required. More allied health (59.3%) than medical (44.8%) students felt that non-immune students should be excluded from clinical rotations.
Health science students’ attitudes and practices regarding vaccination (n = 401).
| Attitude questions (n = 7) | Total (n = 401) | Medical (n = 320) | Allied health (n = 81) | p-Value+ |
|---|---|---|---|---|
| Total attitude score, mean (SD) | 4.1 (2.8–5.4) | 4.1 (2.8–5.4) | 4.2 (3.0–5.4) | 0.301‡ |
| 1. Which of the following vaccines do you believe should be mandatory for Stellenbosch University health science students? (Yes, I believe it should be mandatory*) | 225 (56) | 186 (58.2) | 38 (47.3) | 0.079 |
| 1a. Diphtheria | 85 (21.2) | 78 (24.4) | 7 (8.6) | |
| 1b. Hepatitis A | 300 (74.8) | 230 (71.9) | 70 (86.4) | |
| 1c. Hepatitis B | 388 (96.8) | 313 (97.8) | 75 (92.6) | |
| 1d. Influenza | 240 (59.9) | 215 (67.2) | 25 (30.9) | |
| 1e. MMR (measles, mumps, rubella) | 239 (59.6) | 195 (60.9) | 44 (4.9) | |
| 1f. Polio | 136 (33.9) | 105 (32.8) | 31 (38.3) | |
| 1g. Varicella zoster | 184 (45.9) | 168 (52.5) | 16 (19.8) | |
| 2. Should health science students be required to check their immune status to hepatitis B following primary immunization? (Yes*) | 375 (93.5) | 302 (94.4) | 73 (90.1) | 0.165 |
| 3. I received adequate information about which vaccine/s are compulsory prior to my clinical rotations? (Strongly agree or agree*) | 242 (60.3) | 193 (60.3) | 49 (60.5) | 0.976 |
| 4. I received adequate information about which vaccine/s are recommended prior to clinical rotations? (Strongly agree or agree*) | 158 (39.4) | 128 (40) | 30 (37.0) | 0.626 |
| 5. Should the university make/keep it compulsory to submit evidence of immunity to diseases for which vaccination is compulsory before clinical rotations? (Yes*) | 366 (91.3) | 289 (90.3) | 77 (95.1) | 0.176 |
| 6. Whose responsibility is it to determine which vaccines a health science student still requires (i.e. for diseases they are non-immune to)? (Student's responsibility*) | 121 (30.3) | 91 (28.6) | 30 (37) | 0.132 |
| 7. Should students who have not received the required vaccines be excluded from clinical rotations until they can demonstrate immunity? (Yes*) | 190 (47.4) | 142 (44.8) | 48 (59.3) | 0.017 |
| Practice questions (n = 3) | Total (n = 401) | Medical (n = 320) | Allied health (n = 81) | p-Value+ |
| Total practice score, mean (SD) | 2.4 (1.6–3.2) | 2.4 (1.6–3.2) | 2.5 (1.7–3.3) | 0.158‡ |
| 1. I possess at least one form of evidence of immunity against a vaccine-preventable disease. (Yes*) | 350 (87.3) | 276 (86.3) | 74 (91.4) | 0.218 |
| 2. Did you complete the 3-dose primary hepatitis B vaccination series? (Yes or in progress*)† | 361 (90.0) | 287 (89.7) | 74 (91.4) | 0.654 |
| 3. If you were not immunized at the campus health clinic, did you provide Stellenbosch University with proof of immunity to hepatitis B? (Yes*)# | 242 (60.3) | 191 (59.7) | 51 (63.0) | 0.590 |
For question A1 the average score of several sub-questions was calculated to produce a maximum score weight of 1. SD = standard deviation.
Pearson's χ2 test.
t-Test comparing medical and allied health students.
Desired response.
Of the 44 (11%) participants in the process of completing the series, 17 (4%) were still in year 1 and were only required to submit evidence of immunity at the end of year 1.
Yes responses include students immunized at the campus health clinic as well as those who were immunized elsewhere and provided SU with proof of immunity. This indicates the total amount of students for which proof of immunity was available.
Practices
Mean p scores were high in both the groups [mean 2.4 (SD 0.8) of three questions] (Table 3). Most students (87.3%) possessed at least one form of evidence of immunity to a VPD. Although 90% had completed (or were in the process of completing) the primary HBV immunization series, only 60.3% of students had provided the proof of immunization to the university.
Preferences
More medical students (81.6%) indicated that they would participate in a peer vaccination session compared to only 50.6% of the allied health students (261/320 vs 41/81; p <0.001) (Table 4). Medical (92.8%) and allied health students (82.7%) were supportive of developing a webpage or mobile application to assist students with scheduling of vaccinations (297/320 vs 67/81; p = 0.005).
Health science students’ preferences regarding vaccination (n = 401).
| Preference questions (n = 5) | Total (n = 401) | Medical (n = 320) | Allied health (n = 81) | p-Value+ |
|---|---|---|---|---|
| 1. Would you participate in a class demonstration and peer vaccination session? | <0.001 | |||
| Yes | 302 (75.3) | 261 (81.6) | 41 (50.6) | |
| No | 65 (16.2) | 33 (10.3) | 32 (39.5) | |
| Unsure | 34 (8.5) | 26 (8.1) | 8 (9.9) | |
| 2. Would you use a webpage or app to guide you regarding scheduling of required and recommended vaccinations? | 0.005 | |||
| Yes | 364 (90.8) | 297 (92.8) | 67 (82.7) | |
| No | 18 (4.5) | 13 (4.1) | 5 (6.2) | |
| Unsure | 19 (4.7) | 10 (3.1) | 9 (11.1) | |
| 3. Would you prefer having vaccine costs charged to your student account? | 0.697 | |||
| Yes | 255 (63.6) | 205 (64.1) | 50 (61.7) | |
| No | 142 (35.4) | 111 (34.7) | 31 (38.3) | |
| Unsure | 4 (1) | 4 (1.3) | 0 (0) | |
| 4. Who should bear the cost of the vaccinations required for undergraduate health science students? | NA | |||
| The Department of Health | 228 (56.9) | 188 (58.8) | 40 (49.4) | |
| Stellenbosch University | 120 (29.9) | 99 (30.9) | 21 (25.9) | |
| The students themselves | 39 (9.7) | 23 (7.2) | 16 (19.8) | |
| Academic Hospitals | 11 (2.7) | 7 (2.2) | 4 (4.9) | |
| Unsure | 3 (0.7) | 3 (0.9) | 0 (0) | |
| 5. Where do you think SU health science students should receive their required vaccinations?† | NA | |||
| Campus health clinic | 219 (54.6) | 171 (53.4) | 48 (59.3) | |
| Mass vaccination sessions in the skills laboratory | 147 (36.7) | 127 (39.7) | 20 (24.7) | |
| Hospital occupational health clinic | 14 (3.5) | 10 (3.1) | 4 (4.9) | |
| Private pharmacy or general practitioner | 13 (3.2) | 8 (2.5) | 5 (6.1) | |
| Other | 8 (2.0) | 4 (1.2) | 4 (4.9) |
Responses converted to binary output (yes vs no/unsure) and compared between medical and allied health students using a Pearson's χ2 test.
Participants could only select one option.
Other = missing, could be vaccinated anywhere.
Students’ reported experience of vaccination services
Only 2/159 students (1.3%) who had not provided evidence of HBV immunity reported being contacted by the university to follow up on their immunization status. Of the 232 students vaccinated at the campus health clinic, 76 (32.8%) received an adult vaccination card as evidence of vaccination. Shortages of vaccines at the campus health clinic were reported by 148 (36.9%) students, with the most common vaccines out of stock being HBV (n = 80), VZV (n = 42) and Hepatitis A Virus (HAV) (n = 33) partly owing to national vaccine shortages in recent years. Most students’ parents funded their vaccinations (56.4%), followed by medical insurance (38.7%), own funds (29.4%) and bursaries (1.2%).
Qualitative data
Three open-ended questions were included in the survey: (i) to probe students’ reasons for not completing HBV vaccination, (ii) opinion on whether non-immune students should be excluded from clinical rotations and (iii) to obtain additional comments on the topic of student vaccination.
Participants reported various reasons for non-completion of HBV vaccination, including vaccine unavailability, lack of funds or lack of awareness regarding the importance of vaccination.
There were conflicting opinions as to whether non-immune students should be excluded from clinical rotations. Reasons for exclusion included that it is to protect the student from disease and prevent infection transmission. Participants also believed that it would emphasize the seriousness of the matter and increase vaccination uptake among students.
On the other hand, some students felt that it would be unjustified to exclude those who had not received the required vaccines for various reasons, including affordability, availability, differences in immune response to vaccination, missing academic time and that vaccination remains the student's own choice and responsibility.
When students were asked for comments regarding vaccinations, affordability emerged as a major factor once more. There were conflicting views as to whose responsibility it should be to ensure and fund student vaccination with some believing that it should be included in student fees and others suggesting that vaccination costs should be covered by the university or the Department of Health.
Besides affordability, students pointed out that accessibility and vaccine stock shortages were also a barrier to vaccination uptake. Furthermore, participants commented on the importance of vaccination and the risk of disease, missing academic time and transmitting infection to patients and colleagues.
Students felt that the university was not giving enough attention to vaccinations. In general, participants felt uninformed but were enthusiastic to gain more knowledge and made some suggestions on how to engage students on the topic.
Students supported the idea of mass class vaccination sessions or a mobile application to help keep vaccinations up to date.
Discussion
There is a clear need to develop a more robust health science student vaccination programme at South African higher education institutions and to increase education and advocacy for health-care workers vaccination among students. Similar conclusions were drawn following findings of significant lack of knowledge regarding vaccination and immunity gaps against VPDs amongst Greek medical students.(8) The Greek study strongly recommended improving education of health-care students and suggested consideration for mandatory vaccinations.(8)
In the current study, medical students had higher knowledge scores. This may reflect a greater inclusion of vaccination teaching in their curriculum as opposed to that of the allied health students’ curriculum. Most students knew that vaccinations form part of standard precautions but were unaware that receiving a vaccine does not equate to immunity. Participants did not know what vaccines were recommended by the WHO in 2017 (6) [except for HBV, most likely due to the fact that HBV vaccination is required by SU-FMHS (9)] and did not think them important enough to make vaccination compulsory. A few number of participants felt that they received adequate information regarding compulsory vaccines and even fewer felt they had received enough information regarding recommended vaccines. Dedicated information sessions for all students during their first year of study and reminders during their clinical rotations can potentially address this shortcoming.
Most students had completed or were in the process of completing their HBV vaccination series. Although participants knew that they were required to submit evidence of HBV immunity, there was confusion as to whom and by when this evidence should be submitted. This indicates a clear need for the university to improve communication regarding recommended and mandatory vaccines and to have a formal student vaccination follow-up system.
Students did not feel that it should be their responsibility to determine their immunity to VPDs and thus which vaccines they still required. This suggests that an undergraduate vaccination programme at South African institutions will need to advocate for and motivate students to take responsibility for their own health and vaccinations, until there is an implementation of a formal vaccination program through the university or the Department of Health.
The cost of vaccines emerged as a significant barrier for some students. Most students felt the Department of Health or the university should carry the cost of vaccines. Thus methods of lowering costs should be investigated; students suggested that the inclusion of vaccination costs in study fees or student accounts to ensure the payment of these costs by bursaries.
Increasing access to vaccines is important, as shortages at the campus health clinic (driven largely by national vaccine stock shortages) compromised on timeous vaccination. Mass class or peer vaccination sessions could be an option to ensure vaccination uptake amongst students and were widely supported by medical students, most likely as vaccination technique forms part of their required clinical skill set. A study at another South African university also found that students were positive about practising immunization techniques on their peers.(13) Allied health students at SU-FMHS were not very supportive of peer or mass vaccination, possibly as they are less familiar with administering vaccines.
The follow-up of students’ immunity forms a crucial part of a vaccination programme.(1,3) Almost half of the students believed that non-immune students should be excluded from clinical training until they can prove immunity. Arguments for excluding students included that they are at the risk of contracting the disease and missing out on academic time, as well as the possibility of spreading it to other patients, colleagues and the community. The fact that not all students can afford vaccines was by far the most common argument as to why students should not be excluded. Also many felt that it would be unjustified to exclude students who had not received vaccines for reasons beyond their control, e.g. due to a shortage of vaccines or being non-immune even after vaccination.
Students should be informed about compulsory and recommended vaccines from the first year of study and access to more information should be available at all times. Vaccination booklets are underutilized and could be used as a guide and reminder to students of required vaccinations. Participants supported the idea of a webpage or a mobile application for recording and scheduling of vaccinations. Although there is currently no national guideline on health-care worker vaccination, health science students should as a minimum be encouraged to obtain vaccination for HBV, influenza, diphtheria and pertussis and serological testing to determine their immunity to measles, rubella, VZV and HBV.(1,6,10) In addition, for students born after 1997, the HBV three-dose series may potentially be reduced to a single dose, followed by hepatitis B surface antibody testing to confirm protective immunity levels.
There are limited published studies regarding vaccination of undergraduate health science students at higher education institutions in Africa. Although the study surveyed a large sample of multi-disciplinary students in different phases of their studies, the study is limited by the low participation rate (16.3%), with disproportionally more medical than allied health students partaking, resulting in bias towards medical students. It is also limited by the inclusion of self-reported vaccination practices and self- selection bias.
Conclusion
A comprehensive vaccination policy and student-centric vaccination programme are needed for undergraduate health science students in South Africa. Although undergraduate health science students at SU-FMHS have reasonable knowledge regarding vaccination for health-care workers, the barriers to an effective vaccination programme include the lack of adequate information, lack of vaccines and importantly affordability of vaccines. Additional educational content, vaccine accessibility and affordability are important issues to consider in the development of a successful national undergraduate health science student vaccination programme in South Africa.