- Email: [email protected]
Influenza vaccination status in rheumatoid arthritis and spondyloarthritis patients receiving biologic DMARDs
G Model
ARTICLE IN PRESS
BONSOI-4191; No. of Pages 2
Joint Bone Spine xxx (2015) xxx–xxx
Available online at
ScienceDirect www.sciencedirect.com
Letter to the Editor Influenza vaccination status in rheumatoid arthritis and spondyloarthritis patients receiving biologic DMARDs
a r t i c l e
i n f o
Keywords: Biologics Chronic inflammatory rheumatic disease (CIRD) Disease-modifying antirheumatic drugs (DMARDs) Influenza vaccination Patient information
Biologic disease-modifying antirheumatic drugs (bDMARDs) are effective treatment for chronic inflammatory rheumatic disease (CIRD) but increase the risk of infections [1]. French and international rheumatology organizations recommend influenza vaccination yearly for patients with CIRD receiving immunosuppressive therapy, bDMARDs or glucocorticoid at immunosuppressive dose [2]. We performed a study to evaluate the influenza vaccination rate in patients with CIRD on intravenous (IV) bDMARD and identify factors influencing such vaccination. We questioned 161 consecutive patients about influenza vaccination status in 2013–4. We also noted socio-demographics and clinical data, previous influenza vaccination status, reasons for nonvaccination and information received. The most common diagnosis were rheumatoid arthritis (86/161) and spondyloarthritis (73/161). bDMARDs used were abatacept (22% of patients), infliximab (87%), rituximab (5%) and tocilizumab (34%). Conventional DMARDs (cDMARD) and glucocorticoid were used by 55.3% and 17.4% of patients, respectively. The 2013–4 winter influenza vaccination was given to 42.2% of patients. Age over 65, prior influenza vaccination status and information about benefits of influenza vaccination were significantly associated with the current vaccination status (Table 1). Rheumatologist, general practitioner (GP) and nurse were the main persons who informed patients. Barriers to vaccine uptake were fear of vaccine side effects (32.6%), lack of awareness of infection risk (31.5%), concern about vaccine’s effectiveness and lack of recommendation by a physician (Table 2). However, limitations to our results must be specified: the lack of control of patient vaccination status by evaluation of immunization and the absence of control group. According to us, this is the first published study on influenza vaccination status in patients with CIRD on IV bDMARDs since 2009. Between 2004 and 2009, influenza vaccination rates in patients with CIRD on cDMARDs and/or subcutaneous or IV bDMARDs were reported between 13% and 69.2% in European and US countries [3–8]. These studies found the same predictive factors of vaccination and barriers to vaccination as our study [4–8]. It
Table 1 Influence of socio-demographical, clinical and biological factors on influenza vaccination in 2013/2014. Factors Gender Female (vs. male) Home Urban (vs. rural) Age Age > 65 (vs. age < 65) Tobacco consumption No (vs. Yes) Alcohol consumptiona No (vs. Yes) Living with a person under 18 at home Yes (vs. No) Study level High school certificate completed (vs. not completed) Additional risk factorsb Yes (vs. No) Rheumatologist practice Public hospital (vs. private practice) Diagnosis RA (vs. SpA) Disease duration (months) [12–36] [36–60] [60–120] ≥ 120 bDMARDs continuation rate (months) < 12 [12–36] [36–60] [60–120] ≥ 120 Additional immunosuppressantc Yes (vs. No) Previous bDMARDs Yes (vs. No) HAQ > 1 (vs. < 1) DAS28 < 2.6 [2.6–3.2] [3.2–5.1] ≥ 5.1 Erosion Yes (vs. no) BASDAI [0–4] [4–6] [6–10] Influenza vaccination status in 2012/2013 Vaccinated (vs. non vaccinated)
OR
95% CI
P
0.5
[0.3–1.1]
0.08
0.6
[0.3–1.2]
0.17
2.4
[1.1–5.2]
0.03
1.1
[0.5–2.1]
0.85
1.1
[0.6–2]
0.69
0.5
[0.2–1]
0.07
1.1
[0.6–2.1]
0.81
1.7
[0.9–3.2]
0.12
1.7
[0.3–11.4]
0.57
0.8
[0.4–1.45]
0.43
1 0.5 0.96 0.9
[0.1–4.9] [0.1–6.4] [0.1–5.4]
0.58 0.96 0.88
1 0.98 1.1 2 1.2
[0.4–2.3] [0.4–3] [0.7–5.8] [0.3–4.4]
0.95 0.8 0.19 0.8
0.8
[0.4–1.5]
0.51
0.8
[0.4–1.6]
0.5
1.1
[0.5–2.1]
0.95
1 0.3 0.996 3
[0.9–1.3] [0.4–2.6] [0.3–30]
0.11 0.99 0.34
2.1
[0.7–6.2]
0.18
1 0.5 1.1
[0.2–1.4] [0.2–4.5]
0.20 0.94
26.8
[11.3–63.5]
< 0.05
Data were generated by logistic regression, and expressed as odds ratio (OD) and confidence interval (CI); BASDAI: bath ankylosing spondylitis disease activity index; bDMARDS: biologic disease-modifying antirheumatic drugs; DAS28: Disease Activity Score; HAQ: Health Assessment Questionnaire; RA: rheumatoid arthritis; SpA: spondyloarthritis. a At least one glass a day. b Additional risk factors requiring influenza vaccination according to the French Haut Conseil de Santé publique recommendations in 2013 [2] c Considering treatment: azathioprine, corticosteroids, hydroxychloroquine, leflunomide, methotrexate.
http://dx.doi.org/10.1016/j.jbspin.2015.02.016 1297-319X/© 2015 Published by Elsevier Masson SAS on behalf of the Société Française de Rhumatologie.
Please cite this article in press as: Michel M, et al. Influenza vaccination status in rheumatoid arthritis and spondyloarthritis patients receiving biologic DMARDs. Joint Bone Spine (2015), http://dx.doi.org/10.1016/j.jbspin.2015.02.016
G Model BONSOI-4191; No. of Pages 2
ARTICLE IN PRESS Letter to the Editor / Joint Bone Spine xxx (2015) xxx–xxx
2 Table 2 Reasons for non-influenza-vaccination in CIRD patients.
Disclosure of interest
Reasons
CIRD (n = 92)
Fear of side effects, n (%) Fever, stiffness, fatigue Allergy Other disease Disease flare Other Do not need vaccination, n (%) Already had the flu, hence cannot be infected again, n (%) Influenza vaccine is not efficient and does not protect from the flu, n (%) Influenza vaccine is not recommended, according to, n (%) Media Internet General practitioner Rheumatologist Friends and family Others patients Other Lack of time, n (%) No medical prescription, n (%) Nobody told him/her to be vaccinated, n (%) Vaccine is expensive, n (%) Do not want to, without any explanation, n (%) Patient prefers alternative/holistic approach, n (%) Homeopathy Essential oils Not defined NR
30 (32.6) 11 (11.9) 4 (4.3) 17 (18.4) 8 (8.7) 2 (2.2) 29 (31.5)
The authors declare that they have no conflicts of interest concerning this article. Acknowledgments The authors wish to thank the clinical staff of the department of Rheumatology of Caen hospital, as well as the patients. We thank Dr. Kim Murphy for critical appraisal of the manuscript.
3 (3.3)
References 10 (10.9)
19 (20.6)
3 (3.3) 3 (3.3) 7 (7.6) 6 (6.5) 4 (4.3) 4 (4.3) 0 (0) 8 (8.7) 14 (15.2) 17 (18.5) 2 (2.2) 28 (30.4) 10 (10.9)
3 (3.3) 1 (1.1) 6 (6.5) 7 (7.6)
Data are expressed as number (percentage); several answers could be selected; CIRD: chronic inflammatory rheumatic disease; N/A: not applicable; NR: no response.
suggests a lack of awareness of infection risk by both patients and physicians and a critical role of information to improve vaccination rate [4,5,7,8]. Patients should benefit didactic sessions emphasizing the risk of infection during bDMARDs and the benefits of influenza vaccination [5–8]. Rheumatologists should request patient vaccination status prior induction of bDMARDs, routinely control and update it and work more closely with GPs and nurses [6]. In summary, influenza vaccination rate was low in this cohort. Disease management strategies focused on factors influencing vaccination should involve primary care. Future longitudinal prospective studies are needed to assess benefits of such interventions on CIRD patients’ influenza vaccination rate.
[1] Furst DE. The risk of infections with biologic therapies for rheumatoid arthritis. Semin Arthritis Rheum 2010;39:327–46. [2] Santé MdAsedl. Calendrier vaccinal et recommandations vaccinales 2013 du ministère des Affaires sociales et de la Santé, selon l’avis du Haut Conseil de la santé publique; 2013. [3] Ledwich LJ, Harrington TM, Ayoub WT, et al. Improved influenza and pneumococcal vaccination in rheumatology patients taking immunosuppressants using an electronic health record best practice alert. Arthritis Rheum 2009;61:1505–10. [4] Pradeep J, Watts R, Clunie G. Audit on the uptake of influenza and pneumococcal vaccination in patients with rheumatoid arthritis. Ann Rheum Dis 2007;66:837–8. [5] Haroon M, Adeeb F, Eltahir A, et al. The uptake of influenza and pneumococcal vaccination among immunocompromised patients attending rheumatology outpatient clinics. Joint Bone Spine 2011;78:374–7. [6] Sowden E, Mitchell WS. An audit of influenza and pneumococcal vaccination in rheumatology outpatients. BMC Musculoskelet Disord 2007;8:58. [7] Lanternier F, Henegar C, Mouthon L, et al. Factors influencing influenzavaccination in adults under immunosuppressive therapy for a systemic inflammatory disease. Med Mal Infect 2009;39:247–51. [8] McCarthy EM, de Barra E, Bergin C, et al. Influenza and pneumococcal vaccination and varicella status in inflammatory arthritis patients. Ir Med J 2011;104:208–11.
Murielle Michel a,∗ Fabien B. Vincent b Simon Rio a Nathalie Leon a,1 Christian Marcelli a,1 a Department of Rheumatology, University Hospital Centre of Caen, avenue de la Côte-de-Nacre, 14033 Caen cedex 9, France b Department of Immunology, Monash University, Central Clinical School, Alfred Medical Research and Education Precinct (AMREP), 89 Commercial Road, Melbourne, Victoria 3004, Australia ∗ Corresponding author. E-mail address: [email protected] (M. Michel) 1
Equal contributors.
Accepted 4 February 2015 Available online xxx
Please cite this article in press as: Michel M, et al. Influenza vaccination status in rheumatoid arthritis and spondyloarthritis patients receiving biologic DMARDs. Joint Bone Spine (2015), http://dx.doi.org/10.1016/j.jbspin.2015.02.016
ARTICLE IN PRESS
BONSOI-4191; No. of Pages 2
Joint Bone Spine xxx (2015) xxx–xxx
Available online at
ScienceDirect www.sciencedirect.com
Letter to the Editor Influenza vaccination status in rheumatoid arthritis and spondyloarthritis patients receiving biologic DMARDs
a r t i c l e
i n f o
Keywords: Biologics Chronic inflammatory rheumatic disease (CIRD) Disease-modifying antirheumatic drugs (DMARDs) Influenza vaccination Patient information
Biologic disease-modifying antirheumatic drugs (bDMARDs) are effective treatment for chronic inflammatory rheumatic disease (CIRD) but increase the risk of infections [1]. French and international rheumatology organizations recommend influenza vaccination yearly for patients with CIRD receiving immunosuppressive therapy, bDMARDs or glucocorticoid at immunosuppressive dose [2]. We performed a study to evaluate the influenza vaccination rate in patients with CIRD on intravenous (IV) bDMARD and identify factors influencing such vaccination. We questioned 161 consecutive patients about influenza vaccination status in 2013–4. We also noted socio-demographics and clinical data, previous influenza vaccination status, reasons for nonvaccination and information received. The most common diagnosis were rheumatoid arthritis (86/161) and spondyloarthritis (73/161). bDMARDs used were abatacept (22% of patients), infliximab (87%), rituximab (5%) and tocilizumab (34%). Conventional DMARDs (cDMARD) and glucocorticoid were used by 55.3% and 17.4% of patients, respectively. The 2013–4 winter influenza vaccination was given to 42.2% of patients. Age over 65, prior influenza vaccination status and information about benefits of influenza vaccination were significantly associated with the current vaccination status (Table 1). Rheumatologist, general practitioner (GP) and nurse were the main persons who informed patients. Barriers to vaccine uptake were fear of vaccine side effects (32.6%), lack of awareness of infection risk (31.5%), concern about vaccine’s effectiveness and lack of recommendation by a physician (Table 2). However, limitations to our results must be specified: the lack of control of patient vaccination status by evaluation of immunization and the absence of control group. According to us, this is the first published study on influenza vaccination status in patients with CIRD on IV bDMARDs since 2009. Between 2004 and 2009, influenza vaccination rates in patients with CIRD on cDMARDs and/or subcutaneous or IV bDMARDs were reported between 13% and 69.2% in European and US countries [3–8]. These studies found the same predictive factors of vaccination and barriers to vaccination as our study [4–8]. It
Table 1 Influence of socio-demographical, clinical and biological factors on influenza vaccination in 2013/2014. Factors Gender Female (vs. male) Home Urban (vs. rural) Age Age > 65 (vs. age < 65) Tobacco consumption No (vs. Yes) Alcohol consumptiona No (vs. Yes) Living with a person under 18 at home Yes (vs. No) Study level High school certificate completed (vs. not completed) Additional risk factorsb Yes (vs. No) Rheumatologist practice Public hospital (vs. private practice) Diagnosis RA (vs. SpA) Disease duration (months) [12–36] [36–60] [60–120] ≥ 120 bDMARDs continuation rate (months) < 12 [12–36] [36–60] [60–120] ≥ 120 Additional immunosuppressantc Yes (vs. No) Previous bDMARDs Yes (vs. No) HAQ > 1 (vs. < 1) DAS28 < 2.6 [2.6–3.2] [3.2–5.1] ≥ 5.1 Erosion Yes (vs. no) BASDAI [0–4] [4–6] [6–10] Influenza vaccination status in 2012/2013 Vaccinated (vs. non vaccinated)
OR
95% CI
P
0.5
[0.3–1.1]
0.08
0.6
[0.3–1.2]
0.17
2.4
[1.1–5.2]
0.03
1.1
[0.5–2.1]
0.85
1.1
[0.6–2]
0.69
0.5
[0.2–1]
0.07
1.1
[0.6–2.1]
0.81
1.7
[0.9–3.2]
0.12
1.7
[0.3–11.4]
0.57
0.8
[0.4–1.45]
0.43
1 0.5 0.96 0.9
[0.1–4.9] [0.1–6.4] [0.1–5.4]
0.58 0.96 0.88
1 0.98 1.1 2 1.2
[0.4–2.3] [0.4–3] [0.7–5.8] [0.3–4.4]
0.95 0.8 0.19 0.8
0.8
[0.4–1.5]
0.51
0.8
[0.4–1.6]
0.5
1.1
[0.5–2.1]
0.95
1 0.3 0.996 3
[0.9–1.3] [0.4–2.6] [0.3–30]
0.11 0.99 0.34
2.1
[0.7–6.2]
0.18
1 0.5 1.1
[0.2–1.4] [0.2–4.5]
0.20 0.94
26.8
[11.3–63.5]
< 0.05
Data were generated by logistic regression, and expressed as odds ratio (OD) and confidence interval (CI); BASDAI: bath ankylosing spondylitis disease activity index; bDMARDS: biologic disease-modifying antirheumatic drugs; DAS28: Disease Activity Score; HAQ: Health Assessment Questionnaire; RA: rheumatoid arthritis; SpA: spondyloarthritis. a At least one glass a day. b Additional risk factors requiring influenza vaccination according to the French Haut Conseil de Santé publique recommendations in 2013 [2] c Considering treatment: azathioprine, corticosteroids, hydroxychloroquine, leflunomide, methotrexate.
http://dx.doi.org/10.1016/j.jbspin.2015.02.016 1297-319X/© 2015 Published by Elsevier Masson SAS on behalf of the Société Française de Rhumatologie.
Please cite this article in press as: Michel M, et al. Influenza vaccination status in rheumatoid arthritis and spondyloarthritis patients receiving biologic DMARDs. Joint Bone Spine (2015), http://dx.doi.org/10.1016/j.jbspin.2015.02.016
G Model BONSOI-4191; No. of Pages 2
ARTICLE IN PRESS Letter to the Editor / Joint Bone Spine xxx (2015) xxx–xxx
2 Table 2 Reasons for non-influenza-vaccination in CIRD patients.
Disclosure of interest
Reasons
CIRD (n = 92)
Fear of side effects, n (%) Fever, stiffness, fatigue Allergy Other disease Disease flare Other Do not need vaccination, n (%) Already had the flu, hence cannot be infected again, n (%) Influenza vaccine is not efficient and does not protect from the flu, n (%) Influenza vaccine is not recommended, according to, n (%) Media Internet General practitioner Rheumatologist Friends and family Others patients Other Lack of time, n (%) No medical prescription, n (%) Nobody told him/her to be vaccinated, n (%) Vaccine is expensive, n (%) Do not want to, without any explanation, n (%) Patient prefers alternative/holistic approach, n (%) Homeopathy Essential oils Not defined NR
30 (32.6) 11 (11.9) 4 (4.3) 17 (18.4) 8 (8.7) 2 (2.2) 29 (31.5)
The authors declare that they have no conflicts of interest concerning this article. Acknowledgments The authors wish to thank the clinical staff of the department of Rheumatology of Caen hospital, as well as the patients. We thank Dr. Kim Murphy for critical appraisal of the manuscript.
3 (3.3)
References 10 (10.9)
19 (20.6)
3 (3.3) 3 (3.3) 7 (7.6) 6 (6.5) 4 (4.3) 4 (4.3) 0 (0) 8 (8.7) 14 (15.2) 17 (18.5) 2 (2.2) 28 (30.4) 10 (10.9)
3 (3.3) 1 (1.1) 6 (6.5) 7 (7.6)
Data are expressed as number (percentage); several answers could be selected; CIRD: chronic inflammatory rheumatic disease; N/A: not applicable; NR: no response.
suggests a lack of awareness of infection risk by both patients and physicians and a critical role of information to improve vaccination rate [4,5,7,8]. Patients should benefit didactic sessions emphasizing the risk of infection during bDMARDs and the benefits of influenza vaccination [5–8]. Rheumatologists should request patient vaccination status prior induction of bDMARDs, routinely control and update it and work more closely with GPs and nurses [6]. In summary, influenza vaccination rate was low in this cohort. Disease management strategies focused on factors influencing vaccination should involve primary care. Future longitudinal prospective studies are needed to assess benefits of such interventions on CIRD patients’ influenza vaccination rate.
[1] Furst DE. The risk of infections with biologic therapies for rheumatoid arthritis. Semin Arthritis Rheum 2010;39:327–46. [2] Santé MdAsedl. Calendrier vaccinal et recommandations vaccinales 2013 du ministère des Affaires sociales et de la Santé, selon l’avis du Haut Conseil de la santé publique; 2013. [3] Ledwich LJ, Harrington TM, Ayoub WT, et al. Improved influenza and pneumococcal vaccination in rheumatology patients taking immunosuppressants using an electronic health record best practice alert. Arthritis Rheum 2009;61:1505–10. [4] Pradeep J, Watts R, Clunie G. Audit on the uptake of influenza and pneumococcal vaccination in patients with rheumatoid arthritis. Ann Rheum Dis 2007;66:837–8. [5] Haroon M, Adeeb F, Eltahir A, et al. The uptake of influenza and pneumococcal vaccination among immunocompromised patients attending rheumatology outpatient clinics. Joint Bone Spine 2011;78:374–7. [6] Sowden E, Mitchell WS. An audit of influenza and pneumococcal vaccination in rheumatology outpatients. BMC Musculoskelet Disord 2007;8:58. [7] Lanternier F, Henegar C, Mouthon L, et al. Factors influencing influenzavaccination in adults under immunosuppressive therapy for a systemic inflammatory disease. Med Mal Infect 2009;39:247–51. [8] McCarthy EM, de Barra E, Bergin C, et al. Influenza and pneumococcal vaccination and varicella status in inflammatory arthritis patients. Ir Med J 2011;104:208–11.
Murielle Michel a,∗ Fabien B. Vincent b Simon Rio a Nathalie Leon a,1 Christian Marcelli a,1 a Department of Rheumatology, University Hospital Centre of Caen, avenue de la Côte-de-Nacre, 14033 Caen cedex 9, France b Department of Immunology, Monash University, Central Clinical School, Alfred Medical Research and Education Precinct (AMREP), 89 Commercial Road, Melbourne, Victoria 3004, Australia ∗ Corresponding author. E-mail address: [email protected] (M. Michel) 1
Equal contributors.
Accepted 4 February 2015 Available online xxx
Please cite this article in press as: Michel M, et al. Influenza vaccination status in rheumatoid arthritis and spondyloarthritis patients receiving biologic DMARDs. Joint Bone Spine (2015), http://dx.doi.org/10.1016/j.jbspin.2015.02.016