Table 1.
Characteristics of the included studies
| Study | Country/Year | Number of doses | Total number of patients (Number of patients with serologic response data) | Number of control group (Number of controls with serologic response data) | Underlying disease | Age | Gender (%female) | Type of vaccine received | Time to serologic response evaluation post vaccination | Antibody detection method; criteria for determining seropositivity (if avaliable) |
|---|---|---|---|---|---|---|---|---|---|---|
| Agnieszka Matkowska-Kocjan [23] | Poland/2021 | 2 | 65 (57) Allo-HSCT | No | ALL, CML, AML, AA, MDS, HL, others | 21 (18–31) | 40.0% | BNT162b2 | 14–21 days |
Anti-SARS-CoV-2 QuantiVac ELISA IgG test (Euroimmun/PerkinElmer subsidiary, Waltham, MA, USA); ≥ 35.2 BAU/mL |
| Alexis Maillard [45] | France/2022 | 2 | 687 (687) Allo-HSCT | No | myeloid malignancies, lymphoid malignancies, nonmalignant disease | 59 (46–66) | 41.0% |
BNT162b2; mRNA-1273 |
33 days (27–52) |
1. Abbott SARS-CoV-2 IgG II Quant-test (Abbott S IgG); ≥ 50AU/ml 2. Roche Elecsys anti-SARS-CoV-2 S (Roche S tAb); ≥ 0.8U/ml |
| 3 | 181 (181) Allo-HSCT | 60.5 (49.5–66.9) | 39.4% | Not reported |
3. DiaSorin Liaison SARS-CoV-2 TrimericS IgG (DiaSorin TriS IgG) ≥ 13AU/ml 4. Siemens SARS-CoV-2 IgG (Siemens sCOVG); ≥ 1.0 U/ml 5. Wantai SARS-CoV-2 IgG ELISA (Wantai S IgG) ≥ 0.75 AU/ml |
|||||
| Amandine Le Bourgeois [46] | France/2021 | 2 | 117 (117) Allo-HSCT | No | AML, MDS, MF, MDS/MF, CML, BPDCN, NHL, HL, ALL, MM, NNAA, porphyria | 57 (20–75) | 40.0% | BNT162b2 | 35 (18–77) days |
Elecsys anti–SARS-CoV-2-S (Roche Elecsys, Rotkreuz, Switzerland); ≥ 0.8 U/mL |
| Amandine Le Bourgeois-2 [44] | France/2021 | 3 | 80 (80) Allo-HSCT | 25 (25) Healthy controls | myeloid, lymphoid, others | 57 (20–75) | 43.8% | BNT162b2 | 94.5 (55–220) days |
Elecsys anti–SARS-CoV-2-S (Roche Elecsys, Rotkreuz, Switzerland); ≥ 0.8 U/mL |
| Anne-Claire Mamez [43] | Switzerland/2021 | 2 | 63 (63) Allo-HSCT | No | Acute leukemia, MDS/MPS, lymphoid diseases, hemoglobinopathie | 54 (18–78) | 38.0% | BNT162b2; mRNA-1273 | 38 (13–98) days |
Semi-quantitative Elecsys ® Anti-SARSCoV-2 immunoassay (Roche); ≥ 0.8 U/mL |
| Binod Dhakal [47] | US/2021 | 1, 2 |
71 (71) Allo-HSCT; 45 (45) Auto-HSCT; 14 (14) CAR T |
No | lymphoma, myeloma, some were not reported | 25–77 | not reported | BNT162b2; mRNA-1273; Ad26.COV2.S | ≥ 2 weeks | Enzyme immunoassay testing antibodies to the S1 domain of the SARS-CoV-2 spike protein (EUROIMMUN) |
| Caroline Pabst [24] | Germany/2022 | 1, 2 | 167 (167) Allo-HSCT | 134 (134) Healthy controls | AML, MDS, MPN, AA, ALL, MM, lymphoma | 60 (19–79) | 38.9% | BNT162b2; mRNA-1273; ChAdOx1 | Not reported | Surrogate virus neutralization test (Medac, Wedel, Germany) |
| José Luis Piñana[25] | Spain/2021 | 2 |
311 (311) Allo-HSCT 86 (86) Auto-HSCT |
No | AML, MDS, NHL, MM, CLL, HD, MPN, ALL, others |
Allo: 56.7 (18–80) Auto: 64.6 (19–78) |
Allo: 40.0% Auto: 43.0% |
mRNA-1273; BNT162b2; ChAdOx1; Ad26.COV2.S |
3–6 weeks |
1. Abbott Architect SARS-CoV-2 IgG Quant II chemiluminescent microparticle immunoassay (Abbott, Sligo, Ireland) 2. Liaison SARS-CoV-2 S1/S2 IgG chemiluminescent assay (DiaSorin S.p.A., Saluggia, Italy) 3. Euroimmun SARS-CoV-2 IgG ELISA (Euroimmun, Lübeck, Germany) 4. MAGLUMI 2019-nCoV IgG chemiluminescent assay (SNIBE—Shenzhen New Industries Biomedical Engineering Co., Ltd., Shenzhen, China) 5. COVID-19 ELISA IgG (Vircell Spain S.L.U., Granada, Spain) |
| Kalpana Parvathaneni [41] | US/2021 | 2 | 12 (12) CAR T | 8 (8) Healthy controls | B-ALL, DLBCL, NHL, MCL, CLL | 53 (16–74) | 25.0% | BNT162b2; mRNA-1273 | Up to 28 days | Not reported |
| Katie Healy [35] | Sweden/2021 | 2 | 74 (69) Allo-HSCT/CAR T | 82 (82) Healthy controls | Not reported | 60 (51–67) | 45.0% | BNT162b2 | 14 days |
Elecsys® Anti-SARS-CoV-2 S assay (Roche Diagnostics); ≥ 0.80 U/mL |
| Lorenzo Canti [26] | Belgium/2021 | 1 | 40 (37) Allo-HSCT | 40 (40) Healthy controls | Not reported | 60 (26–76) | 52.5% | BNT162b2 | 21 days | WANTAI SARS-Cov-2 Ab ELISA (Beijing Wantai Biological Pharmacy Enterprise, Beijing, China) |
| 2 | 40 (37) Allo-HSCT | 40 (40) Healthy controls | 28 days | |||||||
| Lorenzo Canti-2 [39] | Belgium/2022 | 3 | 38 (38) Allo-HSCT | No | Not reported | 60 (26–76) | 50.0% | BNT162b2 | 28 days | WANTAI SARS-Cov-2 Ab ELISA (Beijing Wantai Biological Pharmacy Enterprise, Beijing, China) |
| Martina Chiarucci [27] | Italy/2021 | 2 | 12 (12) Allo-HSCT; 38 (38) Auto-HSCT | 45 (0) Healthy controls | Auto-HSCT: MM, NHL, HL; Allo-HSCT: AML, ALL, MDS | 61 (21–72) | 44.0% | BNT162b2 | 30 days | Anti-SARSCoV-2 IgG CLIA (LIAISON ® SARS-CoV-2 TrimericS IgG assay, Diasorin, Saluggia, Italy) |
| Marika Watanabe [28] | Japan/2022 | 2 | 25 (25) Allo-HSCT | 19 (19) Healthy controls | AML, ALL, malignant lymphoma, others |
55 (23–71) |
44.0% | BNT162b2 | 14 days (+ / − 7 days) |
QuaResearch COVID-19 Human IgM IgG ELISA kit (Spike Protein-S1) (Cellspect, Inc., RCOEL961S1, Iwate, Japan); > 0.26 (optical density value) |
| Maciej Majcherek [29] | Poland/2022 | 2 |
64 (63) Allo-HSCT; 29 (26) Auto-HSCT; |
No | AML, MM, NHL, HL, MDS, ALL |
Allo-HSCT: 52 (20–68); Auto-HSCT: 58 (26–69) |
Allo-HSCT: 45.0%; Auto-HSCT: 48.0% |
BNT162b2 | 2–4 weeks | Chemiluminescent microparticle immunoassay (CMIA) “Alinity I” (Abbott Diagnostics) |
| Monika Lindemann [30] | Germany/2021 | 2 | 117 (117) Allo-HSCT | 35 (35) Healthy controls | Acute leukemia, MDS, MPN, lymphoma, others | 59 (21–77) | 52.1% |
BNT162b2; mRNA-1273; ChAdOx1 |
31 (11–137) days | CE marked Anti-SARS-CoV-2 IgG semi-quantitative ELISA (Euroimmun, Lübeck, Germany); |
| Muhammad Bilal Abid [48] | US/2022 | 3 |
26 (26) Allo-HSCT; 30 (30) Auto-HSCT; 10 (10) CAR T |
No | Lymphoma, myeloma | 31–81 | 32.0% |
BNT162b2; mRNA-1273; |
At least 14 days |
AdviseDx SARS-CoV-2 IgG II assay; > 50.0 AU/mL |
| Noga Shem-Tov [31] | Israel/2021 | 2 | 176 (152) Allo-HSCT |
272 (272) Healthy controls |
AML, MDS, MPD, ALL, NHL, HL, CLL, AA | 58.4 ± 14.0 (mean ± SD) | 36.8% | BNT162b2 | 2–4 weeks | Mount Sinai Hospital Clinical Laboratory SARS-CoV-2 IgG Antibody Test; |
| Patrice Chevallier [32] | France/2021 | 1 | 112 (112) Allo-HSCT | 26 (26) Healthy controls | AML, MDS, MF, MDS/MF, CML, BPDCN, NHL, HL, ALL, MM, AA, porphyria | 57 (20–75) | 40.2% | BNT162b2 | 16–35 days |
Roche Elecsys; ≥ 0.8 U/ml |
| Peter Bergman [49] | Sweden/2021 | 2 |
87 (70) Allo-HSCT; 3 (2) CAR T |
90 (78) Healthy controls | not reported | 74% < 65 | 47.0% | BNT162b2 | 14 days |
Elecsys ® AntiSARS-CoV-2 S (Roche Diagnostics); ≥ 0.8 U/ml |
| Rabah Redjoul [37] | France/2021 | 2 | 88 (88) Allo-HSCT | No |
Myeloid malignancy, lymphoid malignancy and nonmalignant |
26–77 | 46.6% | BNT162b2 | 28 (IQR 26–31) days | IgG II Quant Assay (Abbot Laboratories, Wiesbaden, Germany); |
| Ron Ram [36] | Israel/2021 | 2 |
66 (57) Allo-HSCT; 14 (14) CAR T |
No | AML, MDS, ALL, DLBCL, other lymphoma, MPN, others | 65 (23–83) | 45.0% | BNT162b2 | 7–14 days |
Elecsys Anti-SARS-CoV-2 S assay on the Cobas e411 (Roche Diagnostics, Basel, Switzerland); ≥ 0.80 U/mL |
| Roni Tamari [33] | US/2021 | 1 |
149 (149) Allo-HSCT; 61 (61) Auto-HSCT; 7 (7) CAR T |
69 (54) Healthy controls | Acute leukemia, MDS/MPN, chronic leukemia, MM and amyloid, lymphoma, AA, SA, BPDCN | 66.4 (25.8–84.1) | 40.6% | BNT162b2; mRNA-1273 | 3 months |
AdviseDx SARS-CoV-2 IgG II assay; > 50.0 AU/mL |
| Sandra Easdale [34] | UK/2021 | 1 | 55 (55) Allo-HSCT | No | ALL, AML, AA, MDS, NHL, HL, MF | 50 (18–73) | 38.2% | BNT162b2; ChAdOx1 | 14–84 days | Ortho Clinical Diagnostic Anti-SARS-CoV-2 IgG antibody methods (Ortho Clinical Diagnostics, USA); |
| Saurabh Dahiya [40] | US/2022 | 2 | 14 (14) CAR T | 4 (4) Healthy controls | LBCL, MCL, FL | 50.5 (24–87) | 33.0% | BNT162b2; mRNA-1273 | 4 weeks | |
| 3 | 6 (6) CAR T | No | Not reported | Not reported | ~ 1 month | |||||
| Thomas A. Fox [42] | UK/2021 | 2 | 11 (11) CAR T | No | B-ALL, NHL, CLL, WM | Not reported | Not reported |
BNT162b2; ChAdOx1 |
1 month |
Quantitative double-antigen sandwich immunoassays (Roche, Basel, Switzerland); > 0.4 µ/ml |
| Thomas Gastinne [38] | France/2021 | 1, 2 | 23 (23) CAR T | 25 (25) Healthy controls | Lymphoma, ALL | 62 (21–79) | 39.1% | BNT162b2 | 29 (16–32) days after 1st dose and 52 (21–99) days after 2nd dose | Several serological techniques but mainly the Roche Elecsys assay |
Age is expressed as median (range) or median ± quartile
AA aplastic anemia, AML acute myeloid leukemia, ALL acute lymphoblastic leukemia, B-ALL B-cell acute lymphoblastic leukemia, BPDCN blastic plasmacytoid dendritic cell neoplasm, CML chronic myelomonocytic leukemia, DLBCL diffuse large B cell lymphoma, NHL non-Hodgkin lymphoma, HL Hodgkin lymphoma, LBCL large B-cell lymphoma, MCL mantle cell lymphoma, FL follicular lymphoma, MM multiple myeloma, MDS myelodysplastic syndrome, MF myelofibrosis, MPN myeloproliferative neoplasia, MPS Myeloproliferative syndrome, NNAA nonlymphoid and nonmyeloid aplastic anemia, SA systemic mastocytosis, WM Waldenstrom macroglobulinaemia