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Abstract
Introduction To identify facilitators and barriers towards vaccination in general and specifically against pneumococci, influenza and SARS-CoV-2 in patients with rheumatic musculoskeletal diseases (RMD).
Methods Between February and April 2021, consecutive patients with RMD were asked to complete a structured questionnaire on general knowledge about vaccination, personal attitudes and perceived facilitators and barriers towards vaccination. General facilitators (n=12) and barriers (n=15) and more specific ones for vaccination against pneumococci, influenza and SARS-CoV-2 were assessed. Likert scales had four response options: from 1 (completely disagree) to 4 (completely agree). Patient and disease characteristics, their vaccination records and attitudes towards vaccination against SARS-CoV-2 were assessed.
Results 441 patients responded to the questionnaire. Knowledge about vaccination was decent in ≥70% of patients, but <10% of patients doubted its effectiveness. Statements on facilitators were generally more favourable than on barriers. Facilitators for SARS-CoV-2 vaccination were not different from vaccination in general. Societal and organisational facilitators were more often named than interpersonal or intrapersonal facilitators. Most patients indicated that recommendations of their healthcare professional would encourage them to be vaccinated—without preference for general practitioner or rheumatologists. There were more barriers towards SARS-CoV-2 vaccination than to vaccination in general. Intrapersonal issues were most frequently reported as a barrier. Statistically significant differences in response patterns to nearly all barriers between patients classified as definitely willing, probably willing and unwilling to receive SARS-CoV-2 vaccines were noted.
Discussion Facilitators towards vaccination were more important than barriers. Most barriers against vaccination were intrapersonal issues. Societal facilitators identified support strategies in that direction.
- Vaccination
- Autoimmune Diseases
- COVID-19
- Health services research
- Outcome Assessment, Health Care
Data availability statement
Data are available on reasonable request. Data are avilable on reasonoable request.
This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/.
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WHAT IS ALREADY KNOWN ON THIS TOPIC
Uptake of influenza and pneumococcal vaccines in patients with rheumatic musculoskeletal diseases (RMD) is relatively low despite the fact of an increased risk for infections in this population.
Studies about willingness to receive vaccines showed a large heterogeneity which are based in parts on different patterns of behaviours towards vaccines.
Almost no data exist to understand this gap in immunisation status in patients with RMD, and knowledge on facilitators and barriers of vaccine uptake in patients with RMD is limited.
WHAT THIS STUDY ADDS
Facilitators were rated more frequently than barriers without differences between vaccination against pneumococci, influenza and SARS-CoV-2.
Societal and organisational facilitators were more often named than interpersonal or intrapersonal facilitators.
Barriers against vaccination were less frequently mentioned with intrapersonal issues as the most frequent barrier, especially in patients unwilling to receive SARS-CoV-2 vaccines.
HOW THIS STUDY MIGHT AFFECT RESEARCH, PRACTICE OR POLICY
High number of societal and organisational facilitators identified supports the implementation of proactive strategies to increase vaccination rates.
In-depth counselling on vaccines is important for patients with RMD, whereas physicians need support in implementing specific immunisation recommendations.
Introduction
Patients with inflammatory rheumatic musculoskeletal diseases (RMD) carry an increased risk of infections compared with the general population.1 Therapy with disease-modifying antirheumatic drugs (DMARDs) is essential for patients with RMD to achieve remission. Although the degree of immunosuppression varies substantially between the different drugs, most are associated with an increased risk of infection.2–4
One of the most effective strategies to prevent infections is vaccination. The European Alliance of Associations for Rheumatology (EULAR) has recommended vaccination including an annual check of the vaccination status for patients with RMD.5 6 No flares of disease activity and only mild adverse events comparable to healthy controls have been reported after vaccination.7 In addition, the German federal authority for protection against infectious diseases has published guidance on vaccination for patients with RMD.8 Accordingly, vaccination against influenza and pneumococcal is advised for patients with RMD.9 Infections with the SARS-CoV-2 in patients with RMD were reported to be associated with higher rates of hospitalisation and death, especially in high-risk populations.10–12 Risk–benefit analyses have consistently shown that the benefits of vaccination outweigh the risks.13
Uptake of influenza and pneumococcal vaccines in patients with RMD has been reported to be relatively low and variable.6 14 Indeed, less than 50% of patients with RMD had been vaccinated against pneumococci and influenza in a recent study.15 Gaps in vaccine uptake were also reported in other German cohorts.16 Low vaccination rates prompted the WHO in 2019 to mark vaccination hesitancy as 1 of the 10 major threats to global health.17
The situation for SARS-CoV-2 vaccination has not been very clear in that regard. Frequent reasons for the vaccination hesitancy in patients with RMD were the paucity of safety and efficacy data of SARS-CoV-2 vaccines along to the new mode of action for some of the SARS-CoV-2 vaccines and also the transient shortage of vaccines.18 19 Preliminary studies about the willingness of patients with RMD to receive SARS-CoV-2 vaccines showed a large heterogeneity.20 21 Almost no data exist to understand this gap in immunisation status of patients with RMD.
Accordingly, little is known about facilitators and barriers of vaccine uptake in patients with RMD and about their attitudes towards SARS-CoV-2 vaccines compared with other vaccines. Research on the determinants of vaccine uptake has focused largely on intrapersonal determinants such as perceived risk, past vaccine acceptance and beliefs about vaccine safety, and on physician recommendation. COVID-19 pandemic has shown us that other factors like availability of vaccine, influence of public opinion through social media or protective measures for high-risk patients also might influence vaccine uptake.22 23 Given the complex interplay between individuals, relationship, community and societal factors a health model is needed that assess factors beyond attitude of patients at the intrapersonal level. Contrary to most health behaviour theories, the Social Ecological Model, argues that individual behaviour is shaped by facilitators and barriers at multiple levels, including institutional, community and policy levels in addition to intrapersonal and interpersonal levels.24 In this study, we aimed to identify facilitators and barriers towards vaccines in general and specifically against pneumococci, influenza and SARS-CoV-2 based on the Social Ecological Model in patients with RMD.
Methods
Patients with RMD presenting to our tertiary rheumatology hospital were consecutively recruited between February and April 2021. Patients were eligible when been diagnosed with an inflammatory RMDs and provided written informed consent prior to study start. Patients were excluded if they did not speak German. All patients underwent a standardised assessment including patient and disease characteristics and the history of vaccine uptake. A detailed description of the cohort has been previously reported.21
All patients completed a structured questionnaire assessing their knowledge about vaccination in general. Vaccination willingness, confidence and safety concerns towards SARS-CoV-2 vaccines were assessed with a Numerical Rating Scale (NRS) ranging from 0 to 10 (fully agree). Responses between 0 and 4 were classified as ‘unwilling’, between 5 and 6 as ‘probably willing’ and ≥7 as ‘definitely willing’. Attitudes towards vaccinations in general and in particular for pneumococci, influenza and SARS-CoV-2 were assessed using 27 statements. Content were based on the Social Ecological Model which conceptualised health in four domains that are relevant to describe the complex interplay between individuals, relationship, community and societal factors which are relevant for understanding health promotion.24 In addition to this generic framework, we applied the WHO framework of behavioural and social drivers (BeSD) tool of vaccination which is a tool to measure behavioural and social drivers of vaccination.25 26 The BeSD conceptual model measures four domains whereas the domain ‘thinking and feeling’ covers confidence in benefits and safety of vaccines and perceived risks, the domain ‘social processes’ includes external influences like advice on vaccination. These two domains then constitute the ‘motivation’, defined as the intention to get or willingness to recommend a vaccination, which only leads to successful vaccination if the vaccine is available and accessible (‘practical issues’). The questions were tailored to 12 facilitators and 15 barriers. Items were categorised into societal (eg, maintenance of public life), organisational (eg, lack of time or resources), intrapersonal (eg, safety concerns, influence of vaccines on disease status) and interpersonal (eg, negative attitudes of family) factors. Items were phrased by the investigators and one patient. Responses were collected by a 4-point Likert scale with a response option from 1 (completely disagree) to 4 (completely agree) (table 1). Response options to 3 or 4 were categorised as an agreement. Questionnaire was not field tested.
Allocation of facilitators and barriers to statement, term and domain
Statistics
Descriptive data are presented with means and SDs or the median and IQR when referring to quantitative variables and as absolute frequencies and percentages (%) when referring to qualitative ones. Group comparisons of patients stratified by vaccination willingness were performed using Pearson’s χ2 tests or Fisher’s exact tests.
Results
Demographics
A totl of 441 out of 514 patients with inflammatory RMDs fully completed the questionnaire about attitudes to vaccines (85.8%). Patients had a mean age of 54.1 years, a mean disease duration of 9.8 (8.9) years and 61.7% were women (table 2). Rheumatoid arthritis (RA, n=156) and spondyloarthritis (SpA, n=181) were the most common RMDs (337 patients; 76.4%). The remainder had a connective tissue disease or a vasculitis. DMARDs were taken by 425 patients (96.4%). bDMARDs were most frequently used (n=280; 63.5%). No difference in response pattern was observed between patients with different DMARDs groups except the fact that patients with tsDMARDs more frequently assigned themselves as belonging to a risk group (tsDMARDs 83.6% vs csDMARD 69.2% (online supplemental 1). Hypertension was the most common comorbidity (49.9%), followed by obesity (26.1%) and lung disease (19.3%). Patients had moderate disease activity and some impairment of physical function (table 2). The 73 patients with missing responses to the questionnaire about attitudes to vaccines did not deviate substantially from the 441 patients with complete data (online supplemental 2). Patients with missing responses were more often diagnosed with RA, used more often tsDMARDs and less often bDMARDS, had no prior COVID infection in the past and received less often influenza vaccine in the past. Although mean values of willingness to receive SARS-CoV-2 vaccines were not different (complete group 8.6 (2.5) vs missing responses 8.4 (2.8)), responses to the willingness question of patients with missing responses were shifted towards a larger proportion of patients who are unwilling to receive SARS-CoV-2 vaccine (complete group 7.5% vs missing responses 9.0%).
Supplemental material
Patient and disease characteristics
Statements related to COVID-19 infection
Patients were worried about contracting COVID-19 (NRS 6.2 (3.0)) and rated their individual risk to get a worse COVID-19 infection course high (NRS 7.1 (2.5)). A total of 330 patients (74.8%) assigned themselves to a risk group. Only 22 patients (5.0%) reported a prior COVID-19 infection. The willingness to be vaccinated against SARS-CoV-2 was high (NRS 8.6 (2.5)). A total of 357 (81.5%), 48 (11.0%) and 33 (7.5%) patients were definitely or probably willing or unwilling to receive SARS-CoV-2 vaccines, respectively. The confidence in the safety and concerns about side effects of SARS-CoV-2 vaccines was 6.8 (2.8) and 5.4. (3.3), respectively.
Statements related to past vaccine uptake
Self-reported vaccine uptake against pneumococci and seasonal influenza was present in 225 (51.0%) and 279 (63.3%). Several patients stated that they never had been asked to be vaccinated against pneumococci (n=65; 14.7%) or influenza (n=36; 8.2%). Twenty-nine patients (6.6%) had already been vaccinated against SARS-COV-2.
Statements related to knowledge about vaccinations
Most patients reported to have decent knowledge about vaccines in general (78.8%), and about vaccination against influenza (82.3%), pneumococci (73.7%) and SARS-CoV-2 (66.6%) in particular. A minority of patients doubted the effectiveness of vaccines in general (5.9%), against influenza (8.7%), pneumococci (5.9%) and SARS-CoV-2 in particular (14.7%). More than one-third of patients were open to receive more detailed information on vaccines (38.6% in general, 37.9% influenza, 39.2% pneumococci, 42.4% SARS-CoV-2).
Facilitator towards vaccinations
Positive attitudes towards vaccination were frequently indicated, and patients rated statements about facilitators better than statements about barriers (figures 1 and 2, table 3). Societal and organisational facilitators were more often reported than interpersonal or intrapersonal facilitators. Protection of high-risk patients was the most frequently cited facilitator next to maintenance of public life (figure 1). Most patients indicated that they were likely to be vaccinated if their healthcare professional would recommend it—without a strong preference for general practitioners (GPs) or rheumatologists (figure 1). Moreover, a regular check of the vaccine status was appreciated by most patients. Public vaccine campaigns or vaccine campaigns organised by the employer were rated as facilitators by approximately one-third of patients. Many patients stated that they would need comprehensible information about vaccines and especially for SARS-CoV-2 vaccines to decide and even more patients stated that positive information on vaccination in media would support vaccination. Support of family or friends seemed less important. Facilitators did not differ between statements on vaccination in general, and against influenza, pneumococci or SARS-CoV-2 in particular (table 3).
Facilitators towards vaccinations among patients with RMD stratified by willingness to receive SARS-CoV-2 vaccines
Facilitators (A) and barriers (B) of vaccine uptake in general and for SARS-CoV-2. Responses to vaccine uptake in general and SARS-CoV-2 are depicted graphically. Response options to ‘agree’ and ‘completely agree’ were categorised as agreement and depicted in horizontal bars.
Vaccination perceptions among patients with RMD stratified by willingness to receive SARS-CoV-2 vaccines. Percentages were based on the total number of patients for whom the question was applicable. Facilitators are presented in A and barriers in B. RMD, rheumatic musculoskeletal disease.
Barriers towards vaccinations
Patients were less likely to agree to statements about barriers than to statements about facilitators. Specifically, barrier and facilitators statements to vaccination in general ranged between 0%–31% (majority<20%) and 11%–63% (majority>30%), respectively. More barriers towards SARS-CoV-2 and pneumococci vaccination were reported in comparison to vaccination in general or influenza, respectively (figures 1–2). Patients frequently indicated intrapersonal issues as barriers (table 4). Many patients worried about worsening of their disease after vaccination (table 4, figure 1B). Concerns about safety were more prominent for vaccinations against SARS-CoV-2 but lower for vaccinations in general, influenza and pneumococci, respectively (table 4). Importantly, inadequate risk perception was frequently stated for SARS-CoV-2 vaccines but less often for other vaccinations. Negative attitudes of family or friends and lack of time were infrequently stated (table 4). Lack of resources were more often mentioned for SARS-CoV-2 vaccines compared with other vaccines in general. Negative opinions regarding specific vaccines coming from social media were rarely declared by patients.
Barriers towards vaccinations among patients with RMD stratified by willingness to receive SARS-CoV-2 vaccines
Differences in attitudes towards SARS-CoV-2 vaccines between unwilling, probably and definitely willing patients
Statistically significant differences in response patterns to almost all barriers but to a lesser extent to facilitators were noted between patients classified as unwilling, probably or definitely willing (tables 3 and 4, figure 2). Especially statements about barriers to SARS-CoV-2 vaccines were answered differently. Many unwilling patients doubted SARS-CoV-2 vaccine effectiveness, expressed concerns about safety, expressed fear of flares or denied vaccination because of negative reports in media. Patients with probable willingness to receive SARS-CoV-2 vaccines lacked knowledge about SARS-CoV-2 vaccines and expressed the need for information more often compared with definitely willing patients (p=0.039). A minority of unwilling and probably willing patients stated that vaccination is complicated and that family and friends and even physicians advised against SARS-CoV-2 vaccination—and this was not the case for definitely willing patients (all p≤0.001). Interestingly, the risk perception of unwilling, probably or definitely willing patients was not much different (p=0.09). Frequency of barriers towards vaccination against pneumococci was almost similar to barriers towards SARS-CoV-2 vaccination—with the exception that neither doctor nor family/friends advised against vaccination. Differences in response patterns to barriers for vaccination in general and against influenza in particular were seen for statements about perceived lack of benefit (p=0.045) and inadequate access (p<0.001) between unwilling/probably willing patients compared with definitely willing patients. Irrespective of vaccination, patients with a probable willingness to receive SARS-CoV-2 vaccines agreed to facilitators such as knowledge on vaccines more often compared with unwilling patients (p=0.01). Probably and definitely willing patients saw vaccine campaigns (p=0.025), maintenance of public life (p=0.017) and protection for high-risk patients (p=0.003) more often as facilitating compared with unwilling patients.
Discussion
In this study, we identified attitudes towards vaccine uptake of patients with RMD and we show that facilitators were more important than barriers. Societal and organisational facilitators were considered more relevant compared with interpersonal or intrapersonal facilitators—and this was different for barriers. Intrapersonal barriers were addressed more frequently compared with societal and organisational barriers but importantly also at lower rates compared with facilitators. Patients did not recognise differences with respect to attitudes between vaccination in general, influenza, pneumococci and SARS-CoV-2, and also not between GPs and rheumatologists.
Self-reported vaccine uptake was moderate for pneumococci and influenza in this cohort but it was higher compared with our previous report.15 This may potentially be a success of vaccination campaigns in the last years. Importantly, more than 80% of patients were definitely willing to be vaccinated against SARS-CoV-2.21 This high agreement to receive a SARS-CoV-2 vaccine is reflected by the fact that 78% of the population in Germany have received so far vaccinations against SARS-CoV-2 which is one of the highest coverage rate within Europe.27 An increase in vaccine acceptancy was also observed from 2020 until 2022 in 23 countries worldwide.28 Acceptance to vaccination was particularly high among patients who had already received at least one vaccination.
The study also shows that most patients have limited knowledge about vaccination in general and that more than one-third of patients were open to receive more detailed information on vaccines. Consequently, comprehensible positive information about vaccines and on vaccination in media was consistently named as facilitators. Decent knowledge about vaccination is especially relevant for patients with probable willingness to receive SARS-CoV-2 vaccines. Identification of sources of information is of special interest to overcome vaccine hesitancy. Accordingly, using non-traditional health information was associated with the greatest vaccination hesitancy in a US cohort.29 Healthcare and medical science, personal relationships, news and social media were reported as trusted sources of information on COVID-19 vaccines in another US study.30 Thus, future public health campaigns can potentially increase the vaccination rate of hesitant patients.
Provaccination campaigns were rated as facilitators by one-third of patients and again, more often by patients with probable willingness to receive SARS-CoV-2 vaccines. Thus, societal facilitators are an important domain to increase vaccination rates. However, the individual recommendation of vaccinations by physicians is also relevant, since a recent study showed that training on vaccination alone did not change patient behaviour.31 Although knowledge and risk perception increased significantly in the intervention group, the participants did not show a higher willingness to be vaccinated. The authors concluded that interventions on knowledge are effective only if patients are directly vaccinated on site. Moreover, as recently shown, interventions were most successful if tailored to specific populations and their individual concerns.32 Multifactorial and dialogue-based interventions were also more effective.32
Physician interaction was also rated important according to our study results. Patients strongly agreed with the facilitator that their doctor regularly checks their vaccine status. However, some patients reported that doctors have advised against vaccination in the past. This was fortunately rare but it is an area where physician education is still much needed to improve quality of care. Germany’s vaccination strategy is based on a good cooperation between GPs and specialists. However, we have previously shown that this strategy does not seem to work very well.15 33 One reason might be that GPs have limited knowledge about vaccine strategies in patients with RMD and they may be more concerned about side effects in this population at risk. As shown recently by our group, in-depth counselling on vaccines is important for patients with RMD, whereas physicians need support in implementing specific immunisation recommendations.34
Intrapersonal issues were most frequently cited as barriers. Especially unwilling patients often doubt vaccine effectiveness, express concerns about safety and fear flares. This was more often mentioned regarding SARS-CoV-2 vaccination. Other studies about willingness to receive SARS-CoV-2 vaccination have shown heterogeneous results.35 As reported by the COVID-19 Global Rheumatology Alliance almost all unsure or unwilling respondents expressed concerns about side effects and safety.19 Data from EULAR Coronavirus Vaccine (COVAX) physician-reported registry have shown that safety profiles of SARS-CoV-2 vaccines in patients with RMD were reassuring and comparable with other patients.36
Inadequate risk perception was frequently stated for SARS-CoV-2 vaccines but less often for vaccinations in general but did not differ in our study between unwilling, probably and definitely willing patients. It has been shown that complacent individuals do not feel threatened by infectious diseases, and therefore, general involvement in the decision to get vaccines is low37 The WHO-SAGE vaccine hesitancy working group claimed that complacency, lack of confidence and convenience issues impede vaccination rates.38 Consequently, these three most important factors for vaccine hesitancy were identified as barriers to influenza vaccine uptake in risk groups.39 However, recent data from Germany showed that there are also relevant aspects beyond confidence and that structural changes to reduce practical barriers are also important.40
This study has several limitations. Our study is monocentric, and only patients treated in our specialised tertiary centre, the Rheumazentrum Ruhrgebiet, were included in the study. Therefore, we lack generalisability and it might be possible that patients with a more severe course and higher disease activity were included which could have led to selection bias. Patient selection may also have an impact on the high willingness to receive SARS-CoV-2 vaccines. Furthermore, we have assessed the vaccination willingness using the questionnaire developed by us that has not been validated. However, we are not aware of a validated instrument for patients with RMD in this regard. As a methodological basis for developing the questions on barriers and facilitators, we chose two models, Social Ecological Model and BeSD model, which conceptualised health in a broad way. Moreover, the barriers and facilitators assessed in our questionnaire have recently been found as relevant in a scoping review on vaccine uptake.41 Another limitation might be that we have set arbitrary cut-offs for definite and possible vaccination willingness. Employing an NRS had the advantage to use an instrument that was familiar and easy to use for both patients and physicians. Lastly, willigness to vaccination might not generalizeable today, given the nature of the pandemic has changed and many patients have received multiple vaccination since the time of this survey.
In conclusion, facilitators were generally found to be more important than barriers. The most important barriers against vaccination were intrapersonal issues. The high number of societal and organisational facilitators identified supports the implementation of proactive strategies to increase vaccination rates.
Data availability statement
Data are available on reasonable request. Data are avilable on reasonoable request.
Ethics statements
Patient consent for publication
Ethics approval
This study involves human participants and the study was approved by the Ethical Committee of the Ruhr-Universität Bochum, Germany (Nr: 20-7143). Participants gave informed consent to participate in the study before taking part.
Acknowledgments
We thank the patients for their participation in the trial.
References
Supplementary materials
Supplementary Data
This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.
Footnotes
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Contributors Study concept and design: UK, IA and JB. Acquisition of data: all authors. Analysis and interpretation of data: all authors. Writing of the manuscript: all authors. Critical revision of the manuscript for important intellectual content: all authors. All authors had access to the data, commented on the report drafts and approved the final submitted version. UK accepts full responsibility for the work and/or the conduct of the study, had access to the data, and controlled the decision to publish.
Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.
Competing interests None declared.
Provenance and peer review Not commissioned; externally peer reviewed.
Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.