Abstract
Background: Patients with inflammatory rheumatic diseases (IRD) are susceptible to influenza infections and their complications. However, they may avoid vaccination for fear of exacerbating their IRD. This study evaluates the 2023/24 influenza vaccine in IRD patients, aiming to provide recommendations for this group in the upcoming season. Methods: In this prospective, longitudinal study, we assessed the self-reported impact of influenza vaccination on patients with IRD. Participants were recruited nationwide between October and December 2023 and completed an online questionnaire after vaccination as well as at three and six months of follow-up. Results: Among 633 patients, 87.5% were female, with a median age of 50.4 (18–84) years. Post-vaccination, 50% experienced injection site pain; 41% reported no side effects. IRD flares occurred in 5%, with 1% requiring changes to immunomodulation. Among 428 patients with follow-up, influenza infections were reported in 38 patients (8.9%), including 10 (2.3%) with reinfections. No severe cases requiring hospitalization were reported. Spondyloarthritis patients had higher susceptibility to influenza (p = 0.002), accounting for 55.3% of infections. IRD flare-ups in the 12 months before vaccination predicted infections (p = 0.002). Conclusions: The 2023/24 vaccine was well tolerated by IRD patients, with no impact on the course of the disease in 95% of cases. Only 9% of patients reported influenza infections, none of which were severe. In light of these findings, physicians are advised to recommend vaccination to eligible IRD patients prior to or in the respective season.
1. Introduction
Vaccines are among the most effective measures against infectious diseases, yet rising skepticism and misinformation about vaccines and their adjuvants contribute to declining global vaccination rates. No test currently guarantees individual vaccine effectiveness, despite extensive research efforts in this area. While immunogenicity assays, including serologic, neutralization, and cellular tests, indicate immune response, they do not guarantee clinical protection [1,2,3,4].
Influenza vaccination is an effective and affordable preventive strategy. In Germany, the Standing Committee on Vaccination (STIKO) recommends influenza vaccination for patients with inflammatory rheumatic diseases (IRD) on immunosuppressive therapy, with high-dose or adjuvanted vaccines being preferred for individuals aged ≥ 60 years [5]. IRD, like rheumatoid arthritis (RA) and systemic lupus erythematosus (SLE), are linked to an increased risk of influenza infections and complications [1]. Increased susceptibility is due to underlying rheumatic diseases and immunosuppressive therapies used for treatment [6,7]. Furthermore, influenza infections can trigger disease flares in patients with IRD. In SLE, influenza is significantly associated with increased incidence of flares during the first week post-infection, often leading to hospitalization [8].
Given the significant risks associated with influenza infections in patients with IRD, vaccination can effectively reduce the risk of respiratory morbidity and mortality in this population [9]. However, data on influenza vaccine efficacy and safety in IRD remain limited, raising concerns among both patients and physicians. Moreover, the routine exclusion of patients with IRD from vaccine approval trials further contributes to the uncertainty surrounding this issue.
Given these considerations, evaluating the effectiveness and tolerability of influenza vaccination in patients with IRD is essential. This study provides self-reported longitudinal data on these aspects of the 2023/2024 vaccine in IRD. We aim to offer recommendations for this group during the upcoming season to enhance vaccination uptake and address safety and efficacy concerns in this population.
2. Methods
2.1. Study Design and Participants
From 1 October to 31 December 2023, influenza patients receiving the 2023/24 influenza vaccine were invited to participate in a six-month longitudinal survey assessing vaccine effectiveness and tolerability. The inclusion criteria were: (i) age of at least 18 years, (ii) self-reported IRD diagnosis, (iii) influenza vaccination during the study period, and (iv) informed consent. Follow-up surveys were conducted three and six months after vaccination. The follow-up surveys inquired about outcomes occurring between 0–3 months (after the initial survey) and >3–6 months (since the previous survey).
An online questionnaire (www.RheumaVir.de, accessed on 20 December 2025) was developed with two sections.
(a) Demographics: this section collected data on location, age, gender, comorbidities, IRD type, immunomodulatory or immunosuppressive treatment, disease activity, and vaccination history.
(b) Influenza Vaccination: This section assessed participants’ vaccination experiences, its impact on disease activity, confidence in vaccines, perception of risk, and willingness to vaccinate in the future (see Supplementary Materials). The vaccine brand was not assessed. Based on previous studies indicating that patients are often unable to reliably report this information, we decided not to include it in the survey.
2.2. Data Collection
Survey promotion included posters with QR codes, social media, patient organization channels, and direct emails. Representatives from the German League Against Rheumatism were involved throughout the study. Informed consent was obtained before survey access. Participation was voluntary and uncompensated.
The study followed STROBE guidelines for reporting observational research.
2.3. Outcome Measures
The primary outcomes were the frequency and duration of disease flares following the 2023/2024 influenza vaccination. Secondary outcomes included the rate and progression of influenza infections in vaccinated IRD patients, stratified by IRD subtypes.
2.4. Statistical Analysis
Categorical variables are presented as absolute and relative frequencies, and continuous variables as median and range. Group comparisons were performed using χ2, Fisher’s exact, or Kruskal–Wallis tests, depending on variable type and cell sizes. Patients with no, one, or two influenza infections were compared using Fisher’s exact tests for categorical variables and Kruskal–Wallis tests for continuous variables. Wilcoxon–Mann–Whitney tests were used to compare disease activity between two groups. Statistical analyses were conducted using SPSS Statistics (IBM SPSS Statistics, V.26.0) and SAS 9.4 (SAS Institute, Cary, NC, USA).
2.5. Ethics Approval
The study was conducted in accordance with the principles of the Declaration of Helsinki and approved by the ethics committee of the Justus-Liebig-University Giessen (#AZ 19/23, 7 March 2023), Germany. Patient consent for publication was not required according to ethics committee. Informed consent was obtained from all subjects involved in the study.
3. Results
3.1. Patient Characteristics and Baseline Data
A total of 633 patients participated (median age 50.4 years, 87.5% female; Table 1), with rheumatoid arthritis as the most common IRD at 49.8%. Arterial hypertension was the most common comorbidity (26.5%); 41% reported no comorbidities. Two-thirds were treated in rheumatology practices, 28% in hospital outpatient departments, and 6% without rheumatologist care. More than half received glucocorticoids, and 43% were on biologics. Most patients (85.8%) continued their IRD therapy during vaccination; 9.2% discontinued on a physician’s advice, and 5.1% stopped independently (Table 2). Influenza vaccination at baseline was co-administered with another vaccine in 22.4% of cases, primarily coronavirus disease 2019 (COVID-19) vaccines (20.1%), followed by pneumococcal or shingles vaccination (n = 6, 1.0%).
Table 1.
Data of all patients (n = 633). Non-infected patients (n = 380) were compared to once infected (n = 38) and twice infected (n = 10) patients. IRD = inflammatory rheumatic disease, ANCA = Anti-neutrophil cytoplasmic antibodies, IgG4 = immunoglobulin G4, csDMARD = conventional synthetic (cs) disease modifying antirheumatic drug (DMARD), bDMARD = biological disease-modifying antirheumatic drugs, ts = targeted synthetic, TNF-a = tumor necrosis factor alpha, IL = interleukin, GC = glucocorticoid.
Table 2.
Discontinuation of the inflammatory rheumatic disease (IRD) treatment during the administration of the influenza vaccination.
3.2. Vaccination Ever History
Prior to the current influenza vaccination, participants reported the following previous vaccinations: Nearly all participants reported a previous COVID-19 vaccination (92.6%; Table 3). More than half received over four COVID-19 vaccines, 30% received at least three, and 2.8% two. Previous pneumococcal vaccination was reported in 64.9%, followed by measles (41.7%), shingles (40.1%), tuberculosis (15.3%), and respiratory syncytial virus (RSV, 4.3%). Only 2.8% reported no prior vaccinations.
Table 3.
Self-reported history of vaccines ever prior to influenza vaccination 2023/24.
3.3. Tolerability of Influenza Vaccination in IRD Patients
Half of the patients (50.1%) reported pain at the injection site after baseline vaccination, followed by fatigue (20.7%). 5.2% of patients reported an IRD flare post-vaccination. Consequently, four patients (0.6%) were either switched to a new IRD therapy or their existing therapy was supplemented with an additional IRD-related medication (Table 4). In follow-up surveys, 10.8% of the patients reported new onset of vaccine-related side effects since the last survey after three months, and 6.8% after six months. Over 90% of participants expressed willingness to receive an influenza vaccination during the next flu season.
Table 4.
Reported side effects of influenza vaccination and impact on the disease activity of the IRD reported in the first and follow-up surveys. Baseline survey was conducted immediately after influenza vaccination. In the follow-up survey after 3 months and between >3–6 months any changes since the last survey were asked. Regarding side effects, multiple choices were available. AE = adverse event, DSA = disease activity, IRD = inflammatory rheumatic disease.
3.4. Occurrences of Influenza Infection After 2023/2024 Influenza Vaccination and the Impact of the Vaccine on Disease Activity in IRD Patients
No severe influenza infections requiring hospitalization were reported. Among 428 patients with complete data, 38 (8.9%) experienced influenza infections, and 10 (2.3%) were infected twice (Table 1). Influenza infections were more common in patients with spondyloarthritides—including psoriatic, axial, and enteropathic spondyloarthritides—than in patients with other IRD types (55.3% vs. 26.1%; p = 0.002, Table 1). Notably, a greater proportion of men than women had spondyloarthritides (42.6% vs. 24.4%; p = 0.000334).
While age, treatment, and comorbidities did not significantly differ among patients with zero, one, or two infections, IRD flare-ups in the 12 months before vaccination were significant predictors of infections: the median duration of IRD flares was significantly longer in infected patients (45 days, range 0–365) than in non-infected patients (10 days, range 0–365; p = 0.002, Table 1). Subanalyses for IRD subtypes partially confirmed this observation: in patients with RA, those infected with influenza reported a higher number of days with flares in the past year compared to uninfected patients (72 ± 78.8 vs. 36.3 ± 66.3 days; p = 0.034). A similar trend was observed in patients with spondyloarthritides, who reported even more days with flares, aligning with the higher total infection rate compared to other IRD types (90.2 ± 103.9 vs. 53.8 ± 82.8 days; p = 0.018). In contrast, no significant differences were found in patients with connective tissue diseases or concurrent fibromyalgia (Table 5).
Table 5.
Data on the frequency with which disease flares were reported within the 12 months prior to influenza vaccination, categorized by type of inflammatory rheumatic disease and state of influenza infection. The mean values, standard deviations, medians, and ranges are shown. Mann–Whitney test was used to evaluate the results. The calculated p-value is shown.
3.5. Source of Information, Reasons for Receiving Influenza Vaccination, and Concerns
Over half of the participants (n = 370, 58.5%) reported receiving information about influenza vaccination from a physician. Additionally, 23% of the participants (n = 145) referred to various sources such as newspapers, radio, television, online news, social media, and personal online research.
Participants reported several personal reasons for receiving the influenza vaccination, including: (i) belonging to a risk group (n = 533, 84.2%), (ii) the desire to avoid influenza infection (n = 471, 74.4%), (iii) the intention to protect others (n = 175, 27.7%), (iv) employment in the healthcare sector (n = 99, 15.6%), (v) work in critical environments such as schools (n = 58, 9.2%), and (vi) other reasons (n = 28, 4.4%).
Most patients (n = 495; 78.2%) expressed no concerns about the influenza vaccination. The remaining participants reported varying levels of concern: mild (n = 101, 16.0%), moderate (n = 32, 5.1%), and only a small proportion reported high (n = 4, 0.6%) and very high concern (n = 1, 0.1%). Identified concerns included (i) fear of side effects (n = 91, 14.4%), (ii) worries about increased disease activity post-vaccination (n = 64, 10.1%), (iii) perceptions of insufficient efficacy of the vaccination (n = 28, 4.4%), (iv) concerns about long-term side effects (n = 20, 3.2%), (v) potential genomic consequences (n = 6, 1.0%), and (vi) insufficient information related to the vaccination (n = 5, 0.8%). These findings underscore the importance of addressing patient concerns while highlighting the overall effectiveness and tolerability of the influenza vaccination in individuals with IRD.
4. Discussion
In this nationwide study involving over 600 IRD patients in Germany, the 2023/2024 influenza vaccine was well tolerated, with only 8.9% of the patients experiencing influenza infection. No hospitalizations, major disease flares, or severe adverse events were reported. These observations were preserved despite ongoing treatment with disease modifying anti-rheumatic drugs (DMARDs) in the majority of patients, including approximately one-fifth who received concurrent vaccinations.
Retrospective data from 30,788 IRD patients indicate that influenza vaccination in DMARD recipients reduces the incidence of influenza-like illnesses, COPD exacerbations, and pneumonia-related hospitalizations and mortality [9]. Our prospective cohort study confirms these observations, especially concerning the preventative effect of vaccinations on influenza-associated hospitalizations.
It is encouraging that over 90% of participants expressed willingness to receive vaccination in the next season. However, despite clear benefits, many patients remain hesitant and opt out of vaccination. Previous studies identified several key barriers to vaccination uptake among IRD patients, including lack of physician recommendations, younger age, concerns about vaccine safety and efficacy, fear of disease flares, limited awareness or misconceptions regarding vaccination benefits, and mistrust of the medical system or pharmaceutical industry [10,11,12].
Concerns that vaccination may exacerbate underlying IRD and doubts about efficacy due to immunosuppressive therapy were particularly confirmed in our survey. Nakafero et al. found no significant association between inactivated influenza vaccination and rheumatoid arthritis flares, glucocorticoid prescriptions, fever, or new-onset vasculitis. Vaccination was even associated with reduced primary care consultations for joint pain within 90 days post-vaccination [13]. Consistent with these findings, our prospective study observed no significant IRD flares following vaccination (Table 4).
The concern about flares, ranked second in the survey, can be reassuringly addressed by physicians with minimal time investment. In this context, the absence of a direct recommendation from a rheumatologist or general practitioner consistently appears as the most significant predictor of non-vaccination [10,11,12]. However, only 58.5% of participants reported receiving vaccination information from a physician. In contrast, 94% of patients received regular rheumatologist care, highlighting a significant communication gap where rheumatologists fail to address vaccination, which urgently needs improvement. Differing from other studies, limited access to vaccination services and lack of awareness of cost-free vaccines likely play a minor role in the insufficient vaccination rates among IRD patients in Germany [10,11,12,14].
While immune responses may vary by disease type and DMARD treatment, only one participant receiving rituximab—a biological, immunosuppressive agent used primarily for severe RA and systemic IRDs known to cause B-cell depletion—reported influenza in our study [15]. Unexpectedly, participants with connective tissue diseases and other IRD types associated with higher infection susceptibility reported influenza infections less frequently than those with spondyloarthritis. This observation may be linked to previously reported higher infection rates in patients with elevated disease activity prior to vaccination, as also observed in our spondyloarthritis patients [16]. In our study, patients with spondyloarthritis had more days with flares prior to vaccination, aligning with the higher total infection rate compared to other IRD types (Table 5). In contrast, no significant differences were found in patients with fibromyalgia (n = 10) and connective tissue diseases (n = 11) (Table 5). Notably, the statistical test may not have been significant for fibromyalgia because of a smaller sample size. However, it is crucial to consider that sex differences may have influenced the observed outcomes in spondyloarthritides, as men are generally more susceptible to infectious diseases and show weaker vaccine-induced humoral responses than women [17].
To our knowledge, this is the first study to prospectively evaluate the effectiveness of influenza vaccination in reducing infection severity in IRD patients in real-world setting, including reinfection cases. Reassuringly, the reinfection rate of 2.3% falls within the range previously reported in a general population, which varies from 1% in Queensland, Australia and 4% in Guangxi, China [18,19]. Therefore, vaccination has proven effective in preventing severe influenza cases, even in patients experiencing reinfection.
The study’s key strengths include: (i) a substantial sample size; (ii) homogenous data retrieved from a single healthcare system over a defined period, ensuring that all patients received the same standard of medical care and experienced the same influenza season; and (iii) data gathered through a standardized online survey.
This study has several limitations. Only vaccinated IRD patients were invited to participate, and recruitment supported by patient organizations may have introduced selection bias, favoring well-informed individuals who are willing to be vaccinated, as suggested by their higher uptake of other vaccines and reported willingness for future influenza vaccination. Given that this was a very select group of patients who opted to receive the influenza vaccine and enrolled in the study, the results should be considered with certain caution. The educational level and socioeconomic status of the participants were not documented, potentially influencing their knowledge and attitudes toward vaccination. The self-administered questionnaire may have excluded patients who experienced severe side effects or influenza infections from participation. Additionally, information on disease duration, prior medications, vaccine type, and other infectious diseases that could influence IRD flares or the risk of influenza was not recorded. A limitation of the study is that it was not possible to compare the efficacy and tolerability of the vaccine to those of a general population. This is due to the fact that only vaccinated patients and those who voluntarily chose to participate were included in the study.
5. Conclusions
The 2023/24 vaccine was well tolerated by IRD patients, with no impact on the course of the disease in 95% of cases. Only 9% of patients reported influenza infections, none of which were severe. Given the substantial benefits of influenza vaccination for IRD patients, physicians are advised to recommend it to eligible IRD individuals in the upcoming seasons and proactively address potential concerns regarding the influenza vaccination.
Supplementary Materials
The following supporting information can be downloaded at: Online Questionnaire: https://www.mdpi.com/article/10.3390/vaccines14020136/s1. The online questionnaire used for this study is composed of two parts: a baseline questionnaire and a follow-up questionnaire. The questions have been translated into English.
Author Contributions
Conceptualization, K.G., C.F., U.M.-L., H.S.-K., C.S., M.S., K.T. and R.H.; Methodology, E.B., C.F., G.G.-F., N.K. and R.H.; Software, R.H.; Validation, K.G., B.D. and R.H.; Formal analysis, K.G., B.D., N.A.-A., G.R.B., S.C., C.F., G.G.-F., N.K., A.K., U.M.-L., J.R., H.S.-K., C.S., M.S., K.T. and R.H.; Investigation, K.G., B.D., E.B., N.A.-A., G.R.B., S.C., C.F., G.G.-F., N.K., A.K. and R.H.; Resources, R.H.; Data curation, E.B. and R.H.; Writing—original draft, K.G., B.D., E.B. and R.H.; Writing—review & editing, K.G., B.D., E.B., N.A.-A., G.R.B., S.C., C.F., G.G.-F., N.K., A.K., U.M.-L., J.R., H.S.-K., C.S., M.S., K.T. and R.H.; Visualization, K.G. and R.H.; Supervision, K.G., A.K., J.R., C.S., M.S., K.T. and R.H.; Project administration, K.G., B.D., N.A.-A., S.C., C.F., G.G.-F., N.K. and R.H.; Funding acquisition, U.M.-L., H.S.-K., C.S. and R.H. All authors have read and agreed to the published version of the manuscript.
Funding
This study was funded by the Kerckhoff-Foundation (972071), 61231 Bad Nauheim, Germany.
Institutional Review Board Statement
The study was conducted in accordance with the principles of the Declaration of Helsinki and approved by the ethics committee of the Justus-Liebig-University Giessen (#AZ 19/23, 7 March 2023), Germany.
Informed Consent Statement
Informed consent was obtained from all subjects involved in the study.
Data Availability Statement
All data relevant to the study are included in the article.
Acknowledgments
The authors would like to thank all patients who participated in this study and all patients’ organization for their support to spread the study. The authors would also like to thank Alexander Bondar for the technical programming of the survey.
Conflicts of Interest
The authors declare that they have no competing interests.
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