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Abstract
Objectives Patients with autoimmune inflammatory rheumatic diseases (AIRD) often have lower vaccination coverage rates compared with the general population, despite being disproportionately affected by infectious complications. We aim to systematically review the literature regarding vaccination willingness and hesitancy in AIRD.
Methods A scoping review was conducted in PubMed, EMBASE and the Cochrane Library in June 2021. Study selection was performed by two independent reviewers and data were extracted using a standardised form. Risk of bias was assessed using instruments from McMaster University. Identified barriers were categorised into the WHO’s measuring behavioural and social drivers (BeSD) of vaccination conceptual model.
Results The search yielded 1644 hits of which 30 publications were included (cross-sectional studies based on interviews (n=27) and intervention studies (n=3)). The majority of studies reported barriers to influenza and pneumococcal vaccination only (n=9) or in combination with another vaccination (n=8) from the patients’ perspective. Only one study assessed the view of rheumatologists. Coverage of domains matched to the BeSD model suggests a lack of awareness of infection risk by both patients and physicians. Patients mainly mentioned behavioural and social factors that negatively influenced their willingness to be vaccinated while physicians mentioned organisational deficits as major barriers.
Conclusions The view on vaccination in patients with AIRD diverges between patients and rheumatologists. Our results show that in-depth counselling on vaccines is important for patients, whereas physicians need support in implementing specific immunisation recommendations. The themes identified provide a starting point for future interventions to improve vaccine rates in patients with AIRD.
- vaccination
- autoimmune diseases
- qualitative research
Data availability statement
Data are available on reasonable 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 about this subject?
Vaccination rates in patients with autoimmune inflammatory rheumatic diseases are low.
Barriers and facilitators are not well studied in this specific population at risk for an increased risk of infections.
What does this study add?
We provided data on barriers and facilitators towards vaccine uptakes from patients’ and physicians’ point of view
How might this impact on clinical practice or future developments?
Patients and physicians need different information to resolve vaccine hesitancy.
Particularly behavioural and social factors could be identified, which negatively influence patients’ willingness to get vaccinated.
Physicians saw organisational deficits and lack of time as major barriers.
Both stakeholders suggest a lack of awareness of infection risk.
Introduction
Patients with autoimmune inflammatory rheumatic diseases (AIRD) have an increased risk of infections compared with the general population. This is due to two main reasons. First, the inflammatory burden of the rheumatic disease itself1 and related comorbidities contribute to an increased risk of infections. Second, the vast majority of patients with AIRD receive therapies with glucocorticoids and disease-modifying antirheumatic drugs with increased risk of infection.1 2
The most effective strategy to prevent infections is vaccination.3 Vaccinations were shown to provide a protective immune response even when patients with AIRD were treated with immunosuppressive agents concomitantly.3 EULAR recommends vaccination for the vast majority of patients with AIRD and an annual check of their vaccination status.4 5 Furthermore, EULAR strongly recommends consideration of influenza and pneumococcal vaccination for the majority of patients with AIRD. Although sufficiently powered safety assessment studies are lacking, most studies show postvaccination a stable disease activity and only mild adverse events.3
Low vaccination rates have been consistently shown in many countries, for example, in an analysis of administrative claims data of outpatient care for the overall population in Germany.6 A few studies have reported a low vaccination uptake in patients with AIRD.7 8 Our own data have demonstrated a low vaccine uptake of 33.4% for influenza and 49.1% for pneumococci in 975 patients with AIRD in a tertiary centre.9
The overall low vaccination rates prompted WHO in 2019 to mark vaccination hesitancy as one of the 10 major threats to global health.10 While low vaccination status has gained further significance with the advent of the current SARS-CoV-2 pandemic, the underlying reasons with respect to facilitators and barriers towards vaccine uptake are not well known. According to WHO, understanding how people think, feel and act is critical to developing strategies for better vaccination acceptance and uptake.11 An expert group has developed a series of tools to measure behavioural and social drivers (BeSD) of vaccination. The BeSD conceptual model measures four domains (figure 1).12 ‘Thinking and feeling’ covers confidence in benefits and safety of vaccines and perceived risks. ‘Social processes’ include external influences like some advice on vaccination by physician. 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’).12
Behavioural and social drivers of vaccination conceptual model.12
The aim of the present review was to systematically review the literature regarding vaccination willingness and hesitancy in patients with AIRD with focus on the perspective of patients and physicians and to close the knowledge gaps to identify facilitators and barriers towards vaccine uptake, and ultimately categorise the identified factors according to the BeSD conceptual model (figure 1).
Methods
This scoping review was conducted using recommendations from the Preferred Reporting Items for Systematic Reviews and Meta-Analyses extension for Scoping Reviews checklist.13 No review protocol was published in advance.
Research questions are:
What are inhibiting and facilitating factors regarding willingness of vaccination in adults with AIRD?
What do physicians perceive as inhibiting and facilitating factors regarding the willingness to vaccinate and vaccination participation among adults with AIRD?
How can the identified factors be classified into the BeSD conceptual model?
Search strategy
A systematic literature search of English and German language publications was carried out in PubMed, EMBASE and the Cochrane Library until 15 June 2021.
The strategy included a list of keywords pertaining three thematic blocks, namely (1) inflammatory rheumatic diseases, (2) vaccinations of interest for patients with AIRD and (3) attitudes of patients and physicians regarding vaccinations. In addition, corresponding Medical Subject Headings (Mesh; Medline and Cochrane Library) and Emtree (EMBASE) were used. Search strategies are described in online supplemental file 1.
Supplemental material
Inclusion criteria
To be included, publications had to consider (1) adult patients with AIRD, (2) vaccination against tetanus, diphtheria, pertussis, poliomyelitis, hepatitis B, pneumococcus, human papillomavirus, influenza, SARS-CoV-2, herpes zoster, meningococcus, measles, mumps, rubella and chickenpox (varicella), (3) factors associated with vaccination willingness. Regarding physicians, the focus was on (1) attitudes and beliefs on the vaccination of patients with AIRD, (2) factors influencing these attitudes, (3) perceived barriers to vaccination. Regarding patients, this includes (1) vaccination willingness and hesitancy and (2) influencing factors.
Publications were excluded if they (1) did not meet the target population, (2) focused on travel vaccinations solely.
Study selection/extraction
After duplicates had been removed, all remaining articles were first scanned on a title and abstract basis according to the prespecified criteria. Also, reference lists from identified literature reviews were screened. At least two of three reviewers (CS, SS, PzN) screened the references independently. In case of disagreement, a third person was consulted.
The following information was extracted from each study: (1) article characteristics; (2) study characteristics; (3) participant information and (4) outcome measure.
Finally, facilitators and barriers regarding vaccination were extracted by two persons (CS, PzN) independently using a standardised form.
Quality assessment
For cross-sectional study designs, the risk of bias instrument for cross-sectional surveys of attitudes and practices from McMaster University was used.14 For interventional studies, a tool to assess risk of bias in longitudinal research studies was used.15 Two researchers conducted the quality assessment independently (SS, PzN). Studies were not excluded based on quality assessment.
Categorisation of factors into the BeSD conceptual model
Identified facilitators and barriers were synthesised by categorising them into BeSD conceptual model. Classification was conducted independently by two researchers (CS, PzN) by using an inductive coding approach based on the content analysis.16 First, each identified factor was coded as facilitating or inhibiting. For example, if ‘fear of adverse reactions’ is associated with lower uptake or intention, it was coded as an inhibitor and assigned to the category ‘fear’.
Allocation of factors depends on the circumstances given in the studies. The circumstances in which a factor is placed are important for interpreting it, for example, to determine whether people’s opinions or their behaviour arise from personal reasons, or from the environment.
For classification, a document elaborated by WHO in which the framework had been applied for the case of SARS-CoV-2 vaccinations was used.12 Identified factors were allocated into categories of the BeSD conceptual model irrespective of frequency of mentions.
Results
The search process identified 1644 publications of which 30 met the inclusion criteria (cross-sectional studies (n=27) and intervention studies (n=3)) (figure 2).
Study selection flow chart.
Study characteristics
A total of 23 full-text publications17–39 and 7 letters to the editor40–46 were included (table 1). All studies were published between 2003 and 2021. Most were conducted in the UK (n=6),36 37 40 41 43 44 Canada (n=3),17 34 46 France (n=3)18 30 31 and Ireland (n=3).24 29 32 One study was carried out in a total of 56 countries.21
Included publications
Table 2 presents study characteristics of the included publications using a cross-sectional design (n=27). In 19 studies questionnaire-based patient surveys,17–20 22 24–26 28 30 31 33 34 36 37 40 42–44 and in 4 studies telephone surveys were used.23 27 35 45 Two studies applied an online patient survey21 39 and one an interview-based survey.46 One study conducted a questionnaire-based physician survey.29 A total of 13 studies were performed in a clinical setting17 18 20 22 24–26 28 30 31 34 36 46 and used interviews/assessments for collecting data. Five publications did not specify the study setting.33 40 42–44
Study characteristics of publications using cross-sectional designs
Nine studies reported survey response rates, which were around 55% in two studies,29 35 between 90% and 99% in five studies19 20 23 26 33 and 100% in two studies.18 24 In total, 26 studies focused on patients17–28 30 31 33–37 39 40 42–46 and 1 rheumatologist practising in Ireland.29 The study population ranged from 44 to 1258 participants. Age of participants is reported very heterogeneous. One study reported an age range of 50–88 years.17 Five studies reported a median between 50 and 62 years.20–23 33 In all studies, the proportion of women was >60%. Overall, four publications displayed no demographic information29 42–44 and one gave information about the participants’ age but no gender-specific information.22
Most studies focused on influenza and pneumococcal vaccine coverage only (n=9),18 24 27 28 30 33 36 37 43 and eight on influenza, pneumococcal and ‘other’ vaccine coverage, including herpes zoster (n=5),17 26 29 34 35 tetanus (n=1),19 diphtheria (n=1),19 meningococcus (n=2)19 29 or hepatitis B virus (n=2).29 34 One study also considered vaccination against COVID-19.21 Eight focused on influenza only,22 23 25 31 40 42 44 46 two on COVID-19 vaccines39 45 and one on pneumococcus only.20
In 24 studies the objectives were to assess vaccination uptake, coverage rate and/or influencing factors.17–20 22–28 30 31 33–37 40 42–46 Two studies analysed patterns of behaviours regarding COVID-19 vaccines, as a proxy to vaccination willingness and to identify actions to increase vaccine coverage in this risk population.21 39 One study investigated the effect of a quality improvement intervention to increase pneumococcal and influenza vaccination rates in rheumatology care.29
Table 3 presents study characteristics of included interventional studies. Both full publications used a prepost interventional design with two survey time points.32 38 Data were collected in 2017 and 201832 and in 2015 and 2019,38 respectively. In the study by Doe et al, data were assessed after an intervention in 2004.41
Study characteristics of publications using interventional designs
All intervention studies examined vaccination coverage rates. Murray et al aimed to assess vaccination coverage rate before and after implementation of a quality intervention and factors influencing it.32 In the study by Valerio et al, differences in vaccination coverage before and after implementation of a multimodal intervention were investigated.38 Doe et al focused on the uptake of influenza and pneumococcal vaccination after an intervention.41 None of the intervention studies reported response rates. The number of included patients ranged from 169 to 425. Murray et al mentioned that 45.6% of the study population were over 60 years of age.32 In the study by Doe et al, 48% of participants were over 65 years of age.41 Valerio et al reported a mean age around 50.8 years (SD=19,4).38 Murray et al and Valerio et al surveyed more women than men at both survey time points, with the proportion of women being >70%.32 38 With a proportion of 48%, Doe et al is the only study with a lower rate of women than men.41
Risk of bias assessment
The risk of bias assessment was limited by the poor reporting quality of most of the included publications. For more details, see online supplemental file 1.
Most frequent facilitators and barriers
In 22 studies, patients’ responses were quantified and provide insight into which factor was most frequently cited.17–27 30–33 35 38–42 44
Fear of adverse reactions were stated as most frequent reason in seven publications. In one study, 21.8% of respondents self-reported developing a flare postvaccination as most important adverse reaction.19 In another study, adverse reactions induced by COVID-19 vaccine were stated by 95.3%.21 Also 27% of participants mentioned previous adverse reactions of vaccines given in the past.41 The rate of patients being afraid of any vaccination ranged from 16% to 48%.25 30 39 42 Sandler et al showed that up to 70% of patients did not trust vaccinations.35 Not feeling safe was stated by 39% of respondents in the study by Figuerra-Parra et al.22 The belief in good health was stated as most frequent reason in three studies (rates 8.9%–36.9%).32 33 41
In one study, lack of awareness was the most common reason for non-vaccination before intervention for both influenza (36.7%) and pneumococcal (PPSV23) (82.1%). After the intervention, these were 34.2% and 76.4%, respectively.32
Unwillingness of patients to receive any vaccination was mentioned in three studies with a rate between 55.0% and 56.5%.17 38 44 Two studies reported that 63% and 72% of patients forgot to get vaccinated.18 23 A lack of recommendation or no offer of vaccination by providers was mentioned by 36%–87% of patients in five studies.20 24 27 31 40
Classification of facilitators and barriers of vaccination willingness
Altogether, 19 categories were identified. Within the domains ‘thinking and feeling’, ‘social processes’, ‘motivation’ and ‘practical issues’, a total of 10, 4, 1 and 4 categories were identified (figure 3).
Allocation of identified categories to the domains of behavioural and social drivers of vaccination concept model.
The results almost exclusively show the patients’ perspective (n=29) (table 4). One study (table 5) examines perceptions of physicians, which is limited to the rheumatologists’ opinions and their attitude towards patient education. Whether rheumatologists know the reasons for their patients’ willingness to be vaccinated could not be answered.
Patients’ point of view
Rheumatologists’ point of view
Identified categories
Regarding behavioural factors the first identified category ‘fear’ is reported in 20 publications and is mentioned as a reason for vaccination hesitancy. The most stated reason in this category is fear of adverse reactions.18–20 23 25 28 30–33 39 40 42 43 In other publications, fear is specifically directed at the development of allergic reactions,17 27 31 36 at experience of flares or relapses of the rheumatic disease,19 25 41 at inefficacy31 and at fear in general.24 Additionally, the category ‘less trust and concerns’ points out that patients mentioned a lack of trust and concerns regarding their vaccines in 11 publications. This lack referred to safety,20 22 23 26–28 35 37 42 to efficacy of the vaccine27 31 42 or to healthcare professionals.21
The category ‘belief that vaccine is ineffective/does not protect’ includes patients who believe that vaccination does not protect,18 19 39 40 who do not perceive any benefit23 and who believe that vaccinations weaken the immune system or that vaccination results in an increased vulnerability to other illnesses.19 22 25
The category ‘belief in good health’ in this domain includes respondents believe in their good health and therefore refuse vaccination.24 26 32 33 38 41 44 Also, the category ‘uncertainties’ illustrates uncertainties based on prior experience. Stated reasons for this are previous ‘sickness with the vaccination’ or ‘negative experience in the past’.17 25 41
Other publications mention that patients believe vaccination is unnecessary,24 26 or that vaccination is only necessary from the age of 65 years onwards.17 Also, the category ‘lack of awareness’ shows that some patients are not aware of the need of vaccination.32 38 44 Lack of perception of personal risk of illness is mentioned as barrier for vaccination uptake in the category ‘no perceived risk’. Patients did not perceive an influenza infection as a serious disease25 or did not assess the risk of infection.30 Moreover, the category ‘prefer alternatives’ demonstrate that some patients preferred alternatives like herbal medicines, traditional medicine or certain foods.22 39
In one study, efforts were mentioned to be too troublesome for patients.26 This factor was assigned to the category ‘perceived burden of getting vaccine’.
Factors that can be assigned to the domain of social processes are assigned to four categories. The first category ‘influence of information source’ shows that the lack of a recommendation, and the failure to offer vaccinations by the rheumatologist or primary care physician20 23–27 30 31 33 35 37 40 43 46 are mentioned reasons in 13 publications for vaccination hesitancy. The willingness to get vaccinated is also negatively influenced if the physician never discussed the importance of vaccination or never mentioned it,20 23–27 30 31 33 35 37 40 43 46 or when patients considered vaccines to be contraindicated,30 36 in one study even after consultation with their physician.30 Additionally, the category ‘missing of scientific results about vaccine’ points out that patients’ vaccination hesitancy results from not knowing the scientific results regarding vaccinations26 or concerns about a technology that has never been used before (eg, RNA vaccine).21 The factor ‘media and social influence’ shows that a negative reputation of the vaccine,45 news of a particular vaccine39 or bad reports41 are negatively influencing factors. Finally, the last category in this domain ‘no access to knowledge’ shows that patients sometimes have no access to knowledge about vaccination.26
In the domain ‘motivation’, the only identified category is ‘willingness’. One publication mentioned that patients would seek influenza or pneumococcal vaccination based on a physician’s recommendation.26 This is the only factor identified as a facilitator in this review.
Regarding the domain ‘practical issues’, the identified category ‘self-organisation’ shows that patients sometimes forgot about vaccinations.18 23 38 The categories ‘costs’, ‘expenditure of time’ and ‘lack of availability’ points out that there are barriers related to costs,26 38 time27 38 and availability of vaccinations.27
In the study which surveyed rheumatologists, three categories could be identified. Respondents in this study mainly stated practical issues, including lack of time with patients as barrier in the category ‘lack of time’ for education about vaccinations.29 In addition, they believe that there are more important issues to be discussed in a specialty hospital29 and that the responsibility to educate is placed in primary care.29 These two factors are assigned to the categories ‘not the task of special rheumatologist clinics’ and ‘responsibility placed in primary care’ (table 5).
Discussion
We identified a variety of barriers that prevent patients with AIRD from getting vaccinated. The fear of adverse reactions was the most frequently reported reason for vaccination hesitancy in seven publications.19 21 25 30 39 41 42 Furthermore, five studies have shown that 36%–87% of patients reported that vaccination was not recommended/not offered by the physician.20 24 27 31 40 In this scoping review only one facilitator was identified, namely the willingness to take vaccines once recommended by the treating physician.
Our scoping review showed clearly that barriers for patients can rather be assigned mainly in behavioural and social areas, less in practical issues. A total of 1817–20 23–25 27 28 30–33 36 39 40 42 43 and 1617 20 23–27 30 31 33 35–37 40 43 46 publications mentioned factors that can be assigned to the categories ‘fear’ and ‘influence of information source’, respectively. A scoping review published in 202047 also searched for vaccine uptake or hesitancy. Also social and contextual factors as well as provider factors as main themes were identified.47 In contrast, by using the BeSD conceptual model, we gained a different insight into understanding vaccination hesitancy among patients.
One publication mentioned that the opposition of some physicians to provide or to suggest vaccinations could have prevented the immunisation.24
We conclude that the physician’s active recommendation for a specific vaccination is strongly influencing the patients’ decision to get vaccinated. This fact is also underlined by the only facilitator showing that the willingness of patients to be vaccinated increases after a recommendation by the physician.26
Although the scoping review identified almost exclusively the patients’ view, our results indicate that the view about vaccination in patients with AIRD diverges between patients and physicians. Interestingly, only one publication29 notes that the rheumatologist’s perspective allocated barriers mostly to practical issues. None of the included studies indicate to what extent physicians have knowledge about the specific recommendations for vaccines in immunocompromised patients. Moreover, insights of rheumatologists or other physicians into vaccine hesitancy of their patients could be helpful to close the immunisation gap, including COVID-19 vaccines, as shown in the study by Tedeschi et al.48 Therefore, in-depth counselling on vaccines is important for patients with AIRD, whereas physicians need support in implementing specific vaccine recommendations. Consequently, the EULAR recommendation for vaccination assigned the responsibility for assessment, education and implementation of the individualised vaccination programme to the treating rheumatologist to improve the uptake of vaccination.4
Finally, recent studies39 45 have also revealed concerns about COVID-19 vaccine. It can be seen that factors such as ‘bad reputation of vaccine’ and ‘type of vaccine’ are mentioned for the first time in connection with COVID-19 vaccinations. Recently published literature on COVID-19 shows misinformation as another factor, the relevance of which will certainly have to be considered in more detail in the future.49 In this regard, the impact of the pandemic on vaccination preparedness is not yet foreseeable.
It cannot be ruled out that the categorisation of factors is subjective. We tried to minimise this risk by carrying out the classification by two persons independently and by using WHO guidance.11 Moreover, systematic search revealed mainly cross-sectional studies with low reporting quality, which is reflected by the results of the risk of bias assessments.
In conclusion, our scoping review provides insights into different barriers to vaccination that prevent patients with AIRD to have a complete vaccine coverage. Interventions to increase vaccine rates should focus on benefit/risk assessments, risk perception and disease-specific vaccine recommendations. Future research should aim to gather more evidence in relation to physicians’ perceptions. In particular, research should focus on capturing what physicians know about their patients in relation to their vaccination coverage.
Data availability statement
Data are available on reasonable request.
Ethics statements
Patient consent for publication
Ethics approval
Not applicable.
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: SN, AN, UK, AW, SS, CS. Acquisition of data: CS, PzN, SS. Analysis and interpretation of data: all authors. Writing of the manuscript: SN, AN, PzN, CS, SS, UK. 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 is fully responsibie for the finished work, had access to the data, and controlled the decision to publish the manuscript.
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.