Table 1.
Characteristics and Outcomes of the Included Studies
| Author | Country | Year | Patient numbers and description | Control numbers and description | Age of patients, median (y) | Sex of patients (% females) | Cases, concomitant biologics/DMARDs | Cases, concomitant steroids | Type of vaccine | No. of patients receiving 1 dose | No. of patients receiving 2 doses |
|---|---|---|---|---|---|---|---|---|---|---|---|
| Damiani | Italy | 2021 Letter | 4 (psoriasis 100%) | None | 46.8 | 25 | 100% (secukinumab 50%, ixekizumab 25%, risankizumab 25%) | NA | BNT162b2 (Pfizer-BioNTech) 100% | 0 | 4 |
| Deepak | United States | 2021 Preprint | 133 (CD 16.5%, UC 13.5%, RA 28.6%, SpA 15%, SLE 11.3%, Sjögren’s syndrome 6.0%, MS 6.8%, etc) | 53 (HCW and patients) | Cases 45.5,Controls 43.4 | Cases 74.4%,Controls 54.7% | 93.20% (methotrexate 21.8%, hydroxychloroquine 22.6%, MMF 6.8%, AZA 3.0%, leflunomide 1.5%, sulfasalazine 5.3%, JAK inhibitors 8.3%, TNFi 28.6%, etc) | 12.8% | BNT162b2 (Pfizer-BioNTech) NA%, mRNA-1273 (Moderna) NA% | 0 | 133 |
| Geisen | Germany | 2021 Full-text article | 26 (RA 31%, psoriasis/PsA 23%, spondyloarthropathy 12%, SLE 8%, CD 8%, etc) | 42 (HCW) | Cases 50.5 (range 24–89), Controls 37.5 (range 22–61) | Cases 64.3%,Controls 69.2% | 92.3% (cDMARDs 30.8%, bDMARDs 76.9%, both 11.5%) | 26.9% | BNT162b2 (Pfizer-BioNTech) 92.6%, mRNA-1273 (Moderna) 7.3% | 0 | 68 |
| Kennedy | United Kingdom | 2021 Full-text article | 1293 (UC 57.2%, CD 42.8%) | None | 43.8 (32.8–57.6) | 49.2% | 100% (infliximab 66.9%, vedolizumab 33.1%, immunomodulators 48.5%, mesalazine, 25.9%) | 4.8% | AZD1222 (Oxford-AstraZeneca) 54.4%, BNT162b2 (Pfizer-BioNTech) 45.6% |
1293 | 27 |
| Wong | United States | 2021 Full-text article | 48 (UC 52%, CD 48%) | 43 (HCW and volunteers) | Cases 48.8, HCW 35.2, Volunteers 31.5 | Cases 50%,HCW 50%, Volunteers 39% | 85% (TNFi 33%, vedolizumab monotherapy 42%, vedolizumab combination therapy with thiopurine 6%, ustekinumab 8%, guselkumab 2%) | 6% | BNT162b2 (Pfizer-BioNTech) 59%, mRNA-1273 (Moderna) 41% | 36 (22 IBD, 0 HCW, 14 volunteers) | 66 (26 IBD, 14 HCW, 26 volunteers) |
| Boyarsky | United States | 2021 Letter | 123 (inflammatory arthritis 28%, SLE 20%, Sjögren’s syndrome 13%, overlap connective tissue diseases 29%) | None | 50 | 95% | 72% (csDMARDs 19%, bDMARDs 14%, combination therapy 37%) | 3% | BNT162b2 (Pfizer-BioNTech) 52%, mRNA-1273 (Moderna) 48% | 123 | 0 |
| Kappelman | United States | 2021 Full-text article | 317 (IBD 100%) | None | Mean 50.9 | 75.1% | 95.2% (TNFi monotherapy 34.1%, TNFi combination therapy 7.6%, 6MP/AZA/MTX alone 6.3%, mesalazine, sulfasalazine, budesonide, or no medication 20.5%, vedolizumab monotherapy 14.5%, ustekinumab monotherapy 12.3%) | 4.1% | BNT162b2 (Pfizer-BioNTech) 54.6%, mRNA-1273 (Moderna) 45.4% | 0 | 317 |
| Furer | Israel | 2021 Full-text article | 686 (RA 38.3%, PsA 24.1%, AxSpA, 9.9%, SLE 14.7%, AAV 3.8%, etc) | 121 (mainly HCWs) | Cases mean: 56.76, Controls mean: 50.76 | Cases 69.2%, Controls 64.5% | 95.2% (MTX 25.7%, TNFi 25.1%, IL6 inhibitors 5.4%, Anti-CD20 12.7%, abatacept 2.3%, JAK inhibitors 7.1%, IL17 inhibitors 7.0%, MMF 4.1%) | 18.95% | BNT162b2 (Pfizer-BioNTech) 100% | 0 | 807 |
| Shenoy | India | 2021 Preprint | 102 (RA 37.2%, palindromic rheumatism 16.7%, inflammatory polyarthritis 15.7%, spondyloarthropathies 12.7%, SLE 8.8%, vasculitis 5.9%, scleroderma 2.9%, myositis 1.0%) |
60 (Volunteers) | Cases mean: autoimmune 52, other RMD 54.12, Controls mean: ChAdOx1 43.60, BBV152 44.20 | Cases 77.2%, Controls 93.3% | 100% (MTX 56.9%, sulfasalazine 19.6%, leflunomide 8.8%, hydroxychloroquine 69.6%, tofacitinib 5.9%, rituximab 5.9%, MMF 4.9%, etc) | 19.9% | AZD1222 (Oxford-AstraZeneca) 75.9%, BBV152 (Covaxin) 24.1% | 0 | 162 |
| Haidar | United States | 2021 Preprint | 160 (IBD 38.1%, rheumatologic tdiseases 45.6%, other 16.3%) | 107 (HCWs) | Cases mean: 54.2, Controls mean: 43.7 | Cases 70%, Controls 72.0% | 48.1% (TNFi 45%, anti-CD20 3.1%) | NA | Overall population: mRNA-1273 (Moderna) 48.5%, BNT162b2 (Pfizer-BioNTech) 49.7%, Ad26.COV2.S (Janssen/Johnson & Johnson) 1.8% | 0 | 267 |
| Haberman | United States | 2021 Full-text article | 26 (psoriasis/PsA 47.1%, RA 43.1%, other (vasculitis, dermatomyositis, adult-onset Still’s disease, sarcoidosis and polymyalgia rheumatica) 9.8%) | 51 (Healthy subjects) | Cases No MTX mean: 49.1, MTX mean: 63.2, Controls mean: 49.2 | Cases 70.6%, Controls 61.5% | 100% (MTX 49.0%, TNFi 39.2%, other anticytokines/JAK inhibitors 19.6%, immunomodulators 25.5%) | 5.9% | BNT162b2 (Pfizer-BioNTech) 100% | 0 | 77 |
| Mahil | United Kingdom | 2021 Full-text article | 84 (Psoriasis 100%) | 17 (Volunteers) | 43.0 (IQR 31.0–52.0) | 44.5% | 100% (MTX 20.2%, TNFi 32.1%, IL17 inhibitors 17.9%, IL23 inhibitors 29.8%) | 0% | BNT162b2 (Pfizer-BioNTech) 100% | 94 | 0 |
| Simon | Germany | 2021 Full-text article | 84 (SpA 32.1%, RA 29.8%, IBD 9.5%, psoriasis 9.5%, systemic 19.1%) | 182 (Clinic patients) | Cases mean 53.1, Controls mean 40.8 | Cases 65.5%, Controls 57.1% | 66.7% (csDMARDs monotherapy 23.9%, bDMARDs/tsDMARDs 42.9%) | 11.9% | BNT162b2 (Pfizer-BioNTech) 100% | NA | 266 |
| Al-Janabi | United Kingdom | 2021 Letter | 120 (psoriasis 89.2%, PsA 20.8%, RA 8.3%, SLE 0.83%, CD 2.5%) | None | 53 (IQR 33–73) | 40.8% | 74.2% (biologics 67.5%, immunomodulators 25.8%, biologic and immunomodulator 6.7%) | 2.5% | BNT162b2 (Pfizer-BioNTech) 50%, AZD1222 (Oxford-AstraZeneca) 50% | 120 | 0 |
| Bugatti | Italy | 2021 Letter | 120 (RA 57.5%, PsA 21.7%, SpA 20.8%) | None | Mean 56.7 | 67.5% | 100% (csDMARDs 55.8%, b/tsDMARDs 100%) | 39.2% | BNT162b2 (Pfizer-BioNTech) 100% | 120 | 0 |
| Braun-Moscovici | Israel | 2021 Full-text article | 264 (inflammatory arthritis 57.8%, connective tissue diseases 33.0%, vasculitis 7.2%, other 2.3%) | None | Mean 57.6 | 76% | 100% (csDMARDs 60.6%, b/tsDMARDs 67.4%, colchicine 2.3%, nintedanib 1.1%, combination therapy 36.0%) | 34.8% | BNT162b2 (Pfizer-BioNTech) 100% | 0 | 156 |
| Demoulin | Belgium | 2021 Letter | 11 (AAV 63.6%,Minimal change disease/focal and segmental glomerulosclerosis 27.3%, membranous nephropathy 9.1%) | None | 38 (IQR 36–61) | 45.5% | 100% (rituximab monotherapy 100%) | 0% | BNT162b2 (Pfizer-BioNTech) 100% | 0 | 11 |
| Seyahi | Turkey | 2021 Full-text article | 104 (RA 18.3%, SLE 8.7%, Sjögren’s syndrome 6.7%, polymyositis 1.0%, ankylosing spondylitis 16.3%, psoriasis/PsA 6.7%, IBD 4.8%, vasculitis 6.7%, MS 4.8%, etc) | 347 (HCWs, elderly patients) | Cases HCWs mean 42.2, Elderly patients mean 71.4, Controls HCWs mean 41.7, Elderly patients mean 70.9 |
Cases 66.3%, Controls 62.5% | 68.3% (biologics 30.8%, csDMARDs 26.0%, colchicine 15.4%, hydroxychloroquine 11.5%) | 16.3% | CoronaVac (Sinovac) 100% | 0 | 451 |
| Ruddy | United States | 2021 Letter | 404 (inflammatory diseases 44.6%, SLE 21.5%, Sjögren’s syndrome 4.7%, myositis 5.9%, SSc 0.5%, vasculitis 2.0%, overlap connective tissue disease 20.8%) |
None | 44 (IQR 36–57) | 95.3% | 100% (hydroxychloroquine 42.1%, MTX 23.3%, TNFi 24.3%, belimumab 13.9%, mycophenolate 10.1%, AZA 8.7%, IL inhibitors 7.7%, etc) | 29.0% | BNT162b2 (Pfizer-BioNTech) 49.0%, mRNA-1273 (Moderna) 51.0% | 0 | 404 |
| Mrak | Austria | 2021 Full-text article | 74 (IgG4-related disease 2.7%, Connective tissue diseases 29.7%, RA 44.6%, Vasculitis 23.0%) | 10 (Healthy blood donors) | Mean 61.7 | 77.0% | 100% (rituximab 100%, MTX 32.4%, MMF 10.8%, Hydroxychloroquine 9.5%, AZA 6.8%, Leflunomide 5.4%, Sulfasalazine 1.4%, Ig therapy 4.1%) | 29.7% | Cases BNT162b2 (Pfizer-BioNTech) 82.4%, mRNA-1273 (Moderna) 17.6%, Controls BNT162b2 (Pfizer-BioNTech) 100% |
0 | 84 |
| Chung | United States | 2021 Correspondence | 15 (AAV 26.7%, RA 26.7%, SSc 20%, SLE 13.3%, IgG4-related disease 6.7%, IgA vasculitis 6.7%) | None | 57 (IQR 46-65) | 66.7% | 100% (rituximab 93.3%, belimumab 6.7%, MTX 20%, MMF 20%, hydroxychloroquine 13.3%) | 40% | mRNA vaccines (BNT162b2 or mRNA-1273) 93.3%, Ad26.COV2.S (Janssen/Johnson & Johnson) 6.7% | 0 | 15 |
| Spiera | United States | 2021 Letter | 89 (RA 25.8%, SLE 10.1%, Sjögren’s syndrome 11.2%, SSc 5.6%, PsA 6.7%, granulomatosis with polyangiitis 13.5%, giant cell arteritis 2.2%, etc) | None | Mean 61.3 | 76.4% | 100% (csDMARDs 62.9%, bDMARDs 52.6%) | 19.1% | BNT162b2 (Pfizer-BioNTech) 57.3%, mRNA-1273 (Moderna) 42.7% | 6 | 83 |
| Ammitzbøll | Denmark | 2021 Report | 134 (RA 54.5%, SLE 45.5%) | None | SLE 60.2 (IQR 46.3–67.1), RA 70.3 (IQR 66.9–73.5) |
67.2% | RA 100%, SLE 91.8% | 27.6% | BNT162b2 (Pfizer-BioNTech) 100% | 0 | 134 |
| Medeiros-Ribeiro | Brazil | 2021 Full-text article | 910 (chronic inflammatory arthritis (RA, AxSpA, PsA) 49.6%, other ARD (SLE, primary vasculitis, SSc, pSS, IIM, PAPS) 50.4%) | 182 (HCWs) | Cases 51 (IQR 40–60), Controls (50, IQR 41–60) | Cases 76.9%, Controls 76.9% | 100% (Biologics 35.3%, Immunosuppressive drugs 63.0%, Hydroxychloroquine 29.6%, Sulfasalazine 8.0%) | 38.2% | CoronaVac (Sinovac) 100% | 0 | 1038 |
| Dailey | United States | 2021 Preprint | 29 (IBD 100%) | None | Entire study Mean 17.0 (range 2–26), Vaccinated IBD patients NA |
Entire study 42.0%, Vaccinated IBD cohort NA |
100% (vedolizumab monotherapy [4, 13.8%], infliximab monotherapy [22, 75.9%], infliximab + MTX [3, 10.3%]) | NA | mRNA vaccines (BNT162b2 or mRNA-1273) 82.8%, Ad26.COV2.S (Janssen/Johnson & Johnson) 17.2% | 0 | 29 |
| Author | Test used to check antibody response | Timing of test | After 1 dose |
After 2 doses |
||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Cases responders | Controls responders | Cases Ab titers | Controls Ab titers | Cases responders | Controls responders | Cases Ab titers | Controls Ab titers | |||
| Damiani | Anti-S1-receptor binding domain IgG against SARS-CoV-2 | After the second vaccination (days not specified) | … | … | … | … | 100% (4/4) | … | … | … |
| Deepak | Anti-S IgG quantification performed using enzyme-linked immunosorbent assay | 1–2 weeks post-vaccination (mean 8.5 days) | … | … | … | … | Overall 88.7% (118/133), 92% in cases not taking steroids (107/116), 65% in cases taking steroids (11/17) | 98% (52/53) | 33% compared to controls | NA |
| Geisen | IgG antibodies against the SARS-CoV-2 S1 antigen (EUROIMMUN QuantiVac) | 7 days after the second vaccination | … | … | … | … | 100% (26/26) | 100% (42/42) | 2053 ± 1218 (binding antibody units) | 2685 ± 1102 (binding antibody units) |
| Kennedy | Antibodies (including IgG) to the SARS-CoV-2 spike (S) protein receptor binding domain (Roche Elecsys Anti-SARS-CoV-2 S) | 3–10 weeks after the first vaccination | Total 38.2% (494/1293) ADZ1222 33.0% (232/704) BNT162b2 44.5% (262/589) | … | BNT162b2: infliximab GMT 191 U/mL (SD 12.5), vedolizumab GMT 1865 U/mL (SD 8.0), ADZ1222: Infliximab GMT 185 U/mL (SD 9.3), vedolizumab GMT 752 U/mL (SD 12.5) | … | BNT162b2 85.2% (23/27) | … | 158 U/mL in infliximab, 562 U/mL in vedolizumab | - |
| Wong | Siemens Healthineers COV2T and sCOVG assays which test for total immunoglobulins (Igs) and IgG to the receptor binding domain of the SARS-CoV-2 S protein, Roche assay for antibodies to nucleocapsid protein, In-house ELISA testing for IgG against full-length S protein | IBD patients: 14 (3–28) days after the first vaccination, 18 (2–36) days after the second vaccination HCW: 30 (7–37) days after second the vaccination Volunteers: 9 (1–40) days after the first vaccination, 8 (6–18) days after the second vaccination |
67% (6/9) | NA | NA | NA | 100% (26/26) | 100% (40/40) | Similar titers to controls | NA |
| Boyarsky | Antibodies (including IgG) to the SARS-CoV-2 spike (S) protein receptor binding domain (Roche Elecsys Anti-SARS-CoV-2 S) | 22 (18–26) days after the first vaccination | 74.0% (91/123) | … | … | … | … | … | … | … |
| Kappelman | LabCorp Cov2Quant IgG assay | Median 64.0 days (IQR 59.0–2.5) after second vaccination | … | … | … | … | 94.6% (300/317) | … | Median: 17.0 μg/mL (IQR 7.8–30.0) Mean: 28.6 μg/mL (SD 47.5) |
… |
| Furer | DiaSorin LIAISON SARS-CoV-2 anti-S1/S2 IgG assay | 2–6 weeks after second vaccination | … | … | … | … | 86.0% (590/686) | 100% (121/121) | Mean 132.9 BAU/mL (SD 91.7) | Mean 218.6 BAU/mL (SD 82.06) |
| Shenoy | Roche commercial chemiluminescent assay | Cases: Mean 27.6 days (SD 11.7) after second vaccination; Controls: Mean 43 days (SD 10.6) after second vaccination` | … | … | … | … | Total 90.2% (92/102), AZD1222 93.5% (87/93), BBV152 55.6% (5/9) |
ADZ1222 100% (30/30), BBV152 76.7% (23/30) |
Median 223.60 (IQR 53.06–656.40) | ADZ1222 Median 278 (IQR 205–603.12), BBV152 Median 73.89 (IQR 0.85–306.25) |
| Haidar | Beckman Coulter SARS-CoV-2 Spike RBD IgG platform | Median 78 days (IQR 58–105) after second vaccination | … | … | … | … | 83.8% (134/160) | 98.1% (105/107) | Mean antibody level: 8.2 (SD 8.3) | Mean antibody level: 10.1 (SD 8.7) |
| Haberman | Direct ELISA | 1 week after second vaccination | … | … | … | … | 42/51 | 25/26 | No MTX Median 113,608 (range 25–737,310), MTX Median 46,901 units (range 25–694,528) |
Median 104,354 (141–601,185) |
| Mahil | SARS-CoV-2 Spike-specific IgG ELISA | 28 days (±2 days) after first vaccination | 77.9% (60/77) | 100% (17/17) | Responder Median EC50: 43 (IQR 25–162) | Responder Median EC50: 101 (IQR 55–200) | … | … | … | … |
| Simon | Euroimmun anti-S1 IgG ELISA | More than 10 days before serum collection | … | … | … | … | 94.0% (79/84) | 100% (182/182) | Mean optical density 6.47 (SD 3.14) | Mean optical density 9.36 (SD 1.85) |
| Al-Janabi | Roche Diagnostics Elecsys Anti-SARS-CoV-2 S immunoassay | Median: 34 days (IQR 23–46) | 85% (102/120), ADZ1222 78.3% (47/60), BNT162b2 91.7% (55/60) |
… | NA | … | … | … | … | … |
| Bugatti | DiaSorin LIAISON SARS-CoV-2 S1/S2 IgG chemiluminescent assay | 21 days after first vaccination | 55% (66/120) | … | NA | … | … | … | … | … |
| Braun-Moscovici | Abbott SARS-Cov-2 IgG II Quant chemiluminescent microparticle immunoassay (CMIA) | 4–6 weeks after second vaccination | … | … | … | … | 86.0% (227/264) | … | Mean 5830.8 AU/mL (SD 8937) | … |
| Demoulin | Roche Diagnostics SARS-CoV-2 anti-RBD electrochemiluminescent immunoassay | 28 days after second vaccination | … | … | … | … | 45.5% (5/11) | … | Median <0.8 U/mL | … |
| Seyahi | Roche Diagnostics Elecsys Anti-SARS-CoV-2 assay | 30.7 ± 9.0 days after second vaccination | … | … | … | … | 89.4% (93/104) | 99.4% (345/347) | NA | NA |
| Ruddy | Roche Elecsys anti-SARS-CoV-2 S enzyme immunoassay | Median 29 days after second vaccination | … | … | … | … | 93.6% (378/404) | … | >250 U/mL | … |
| Mrak | Roche Diagnostics Elecsys Anti-SARS-CoV-2 S immunoassay | Median 21.9 days (Range 7–49) after second vaccination | … | … | … | … | 39.2% (29/74) | 100% (10/10) | Median 64.9 U/mL (IQR 16.2–2161.0) | NA |
| Chung | Euroimmun IgG binding SARS-CoV-2 spike protein S1 assay (14, 93.3%), DiaSorin Liaison SARS-CoV-2 S1/S2 IgG assay (1, 6.7%) | Median 39 days (IQR 17.5–59.5) after second vaccination | … | … | … | … | 0% (0/15) | … | NA | … |
| Spiera | Roche Elecsys anti-SARS-CoV-2 (84, 94.4%), Siemens healthineers SARS-CoV-2 Total Assay Atellica IM or ADVIA Centaur XP/XPT‡ (5, 5.6%) | NA | … | … | … | … | 76.4% (68/89) | … | NA | … |
| Ammitzbøll | Ortho Clinical Diagnostics VITROS Immunodiagnostic Products Anti-SARS-CoV-2 Total test | 1 week after second vaccination | … | … | … | … | 76.9% (103/134) | … | NA | … |
| Medeiros-Ribeiro | DiaSorin LIAISON SARS-CoV-2 S1/S2 IgG chemiluminescent assay | 28 and 69 days after second vaccination | … | … | … | … | Day 28 18.7% (161/859), Day 69 70.4% (605/859) |
Day 28 34.6% (62/179), Day 69 95.5% (171/179) |
Day 28 geometric mean titer: 5.1 AU/mL (4.7–5.5) Day 69 geometric mean titer: 10.3 AU/mL (8.5–12.5) |
Day 28 geometric mean titer: 10.3 AU/mL (8.5–12.5) Day 69 geometric mean titer: 67.0 AU/mL (59.8–74.9) |
| Dailey | Fluorescent bead-based immunoassay, flow cytometry | mRNA vaccines: mean 3.3 weeks (range 1–10) after second vaccination, adenovirus vector vaccine: mean 3.1 weeks (range 1.6–3.6) after second vaccination |
… | … | … | … | 29/29 | … | NA | … |
6MP, 6-mercaptopurine; AAV, antineutrophil cytoplasmic antibody (ANCA)-associated vasculitis; Ab, antibody; ARD, autoimmune rheumatic diseases; AxSpA, axial spondyloarthritis; AZA, azathioprine; CD, Crohn’s disease; DMARD, disease-modifying antirheumatic drug; ELISA, enzyme-linked immunosorbent assay; HCW, health care worker; Ig, immunoglobulin; IIM, idiopathic inflammatory myopathy; IQR, interquartile range; JAK, Janus kinase; MMF, mycophenolate mofetil; MS, multiple sclerosis; MTX, methotrexate; NA, not available; PAPS, primary antiphospholipid syndrome; PsA, psoriatic arthritis; pSS, primary Sjögren’s syndrome; RA, rheumatoid arthritis; SD, standard deviation; SLE, systemic lupus erythematosus; SpA, spondyloarthritis; SSc, systemic sclerosis; TNFi, TNF inhibitors; UC, ulcerative colitis.