Summary of study characteristics and outcomes for patients with hematologic malignancies by overall cohort and specific underlying disease
| Study . | Type/location . | Study population/comparator . | No. of participants analyzed/controls . | Median age, y (range or IQR) . | M/F . | Vaccine type . | Analysis . | Seropositivity . | Rate of positive nAb/cellular response . | AEs . |
|---|---|---|---|---|---|---|---|---|---|---|
| Mixed-group | ||||||||||
| Addeo et al23 | Multicenter prospective cohort study Europe, North America | Hem Solid tumor | 25 106 | NR for hem | NR for hem | BNT162b2, mRNA-1273, NR for hem | SARS-CoV-2 spike, IgG Roche (≥0.8 IU/mL = positive) | Hem: 3-4 weeks after first dose, 18 (72%) of 25; 3-4 weeks after second dose, 17 (77%) of 22. Solid tumor: first dose, 80 (83%) of 96; second dose, 99 (98%) of 101 | NR | NR |
| Agha et al24 | Single-center retrospective cohort study/ United States | Hem | 67 | 71 (IQR, 65-77) | 35/32 | BNT162b2, mRNA-1273, 51%; 42%; unknown, 7% | SARS-CoV-2 spike, IgG Beckman Coulter (≥1.00 = positive) | 21 days after second dose, 36 (54%) of 67 | NR | NR |
| Benda et al25 | Single-center prospective cohort study/ Austria | Hem Solid tumor | 123 34% myeloma, 38% CLL/lymphoma/WM, 28% AML/MDS/MPNs 136 | NR for hem | NR for hem | BNT162b2 | SARS-CoV-2 spike, IgG Roche (≥0.8 IU/mL = positive) | 21 days after first dose, 53 (43%) of 123; 28 days after second dose, 85 (71%) of 119 | NR | NR for hem |
| Cohen et al26 | Single-center retrospective study/Israel | Hem | 54 | 69 (IQR, 61-77) | 32/22 | BNT162b2 | SARS-CoV-2 spike, IgG Roche (≥0.8 IU/mL = positive) | 2-3 weeks after second dose, 34 (63%) of 54 | NR | NR |
| Gavriatopoulou et al27 | Single-center prospective cohort study/ Greece | Hem Control group | 58 48% WM, 38% CLL, 14% NHL 213 | 75 (40-88) | 28/30 | BNT162b2, 76%; ChAdOx1, 24% | nAb GenScript (≥30% = positive; ≥50% = clinically relevant inhibition) | 22 days after first dose, ≥30%, 8 (14%) of 58 patients vs 114 (54%) of 213 controls | 22 days after first dose, ≥50%, 3 (5%) of 58 patients vs 50 (24%) of 213 controls | NR |
| Greenberger et al28 | Multicenter prospective cohort study/ United States | Hem | 1445: 45% CLL, 25% NHL, 5% HL, 15% MM, 4% acute leukemia, 2% CML, 2% MPNs, 2% other | 68 (16-110) | 574/871 | BNT162b2, 55%; mRNA-1273, 45% | SARS-CoV-2 spike, IgG Roche (≥0.8 IU/mL = positive) | >14days after second dose, 1088 (75%) of 1445 | NR | NR |
| Herzog Tzarfati et al29 | Single-center prospective cohort study/ Israel | Hem Matched healthy controls | 315 22% MPNs, 17% myeloma, 16% aggressive NHL, 13% indolent NHL, 11% CLL, 7% CML, 5% HL, 5% acute leukemia, 5% MDS 108 | 70 (IQR, 61-77) | 223/200 | BNT162b2 | SARS-CoV-2 spike, IgG DiaSorin (≥12 AU/mL = positive) | 30-60 days after second dose, 235 (75%) of 315 vs 107 (99%) of 108 controls | NR | NR |
| Iacano et al30 | Single-center prospective cohort study/ Italy | Hem ≥80 y; health care worker controls ≥66 y (results NR) | 10 | NR for hem | NR for hem | BNT162b2 | SARS-CoV-2 spike, IgG Abbott (≥50 AU/mL = positive) | 28 days after second dose, 4 (40%) of 10 | NR | NR |
| Jurgens et al31 | Single-center prospective cohort study/ United States | Hem Health care worker controls | 67 31% CLL, 63% NHL, 6% HL 35 | 71 (24-90) | 36/31 | BNT162b2, 46%; mRNA-1273, 54% | SARS-CoV-2 spike, IgG in-house (OD 450 ≥3 = positive) | 21 days after second dose, 41 (61%) of 67 vs 35 (100%) of 35 controls | NR | NR |
| Maneikis et al32 | Multicenter prospective cohort study/ Europe | Hem Health care worker controls | 857 68 | 65 (IQR, 54-72) | 404/453 | BNT162b2 | SARS-CoV-2 spike, IgG Abbott (≥50 AU/mL = positive) | 7-21days after first dose, 481 (56%) of 857; NR for control group | NR | At least 1 AE; dose 1, 56 (9%) of 575; dose 2, 72 (13%) of 575 |
| Malard et al33 | Single-center retrospective cohort study/ France | Hem Healthy controls | 195 27% myeloma, 23% NHL, 3% HL, 13% CLL, 16% AML, 2% ALL, 9% MPNs, 7% other 30 | 69 (22-92) | 117/78 | BNT162b2 | SARS-CoV-2 spike, IgG Abbott (≥50 AU/mL = positive; ≥3100 AU/mL = neutralization >30%; SARS-CoV-2 T-cell response, ELISPOT ≥10 spot-forming cells per 106 PBMCs and ratio 2.5 = positive) | ≥3100 AU/mL threshold*; 28 days after first dose, 3 (2%) of 195; 14 days after second dose, 91 (47%) of 196 vs 26 (87%) of 30 controls | Cellular response 14 days after second dose, 36 (53%) of 68 | At least 1 AE; dose 1, 88 (57%) of 154; dose 2, 55 (34%) of 163 |
| Monin et al34 | Multicenter prospective cohort study/ United Kingdom | Hem Health care worker controls | 56: 68% B-cell malignancies, 9% T-cell malignancies, 18% myeloid or acute leukemia, 5% other 54 | 73 (IQR, 65-80) | NE for hem | BNT162b2 | SARS-CoV-2 spike, IgG (≥70 EC50 = positive); SARS-CoV-2–specific T-cells secreting IFN-γ and/or IL-2 >7 cytokine-secreting cells per 106 PBMCs = positive) | 21 days after first dose, 8 (18%) of 44 vs 32 (94%) of 34 controls; 35 days after first dose, 4 (11%) of 36 vs 18 (86%) of 21 controls; 35 days after first dose (with second dose), 3 (60%) of 5 vs 12 (100%) of 12 controls | Cellular response 21 days after first dose, 9 (50%) of 18 vs 14 (82%) of 17 controls; 35 days after first dose, 6 (33%) of 18 vs 9 (69%) of 13 controls; 35 days after first dose (with second dose), 3 (75%) of 4 vs 3 (100%) of 3 controls | NE for hem patients |
| Ollila et al35 | Single-center retrospective cohort study/ United States | Hem | 160: 36% aggressive and 21% indolent lymphoma, 15% plasma cell leukemia, 12% CLL, 9% other lymphoma, 6% myeloid leukemia | 72 (65-79) | 86/74 | BNT162b2, 60%; mRNA-1273, 31%; Ad26, 7%; ND, 1% | SARS-CoV-2 spike, IgG Abbott (signal/cutoff ratio ≥1.4 = positive) | 56 days after first dose, 63 (39%) of 160 | NR | NR |
| Pimpinelli et al36 | Single-center prospective study/ Italy | Hem Older age (>80 y) control group | 92 46% myeloma, 54% MPN 36 | 73 (47-78)/ 70 (28-80) | Myeloma: 23/19; MPN: 26/24 | BNT162b2 | SARS-CoV-2 spike, IgG DiaSorin (≥15 AU/mL = positive) | 21 days after first dose, 9 (21%) of 42; myeloma, 26 (52%) of 50 MPNs vs 19 (53%) of 36 controls; 14 days after second dose, 33 (79%) of 42; myeloma 44 (88%) of 50 MPNs vs 36 (100%) of 36 controls; ≥80 AU/mL threshold*: 14 days after second dose, 23 (55%) of 42; myeloma 42 (84%) of 50 MPNs vs 34 (97%) of 36 controls | NR | Reported with different patient numbers |
| Re et al37 | Multicenter retrospective cohort study/ France | Hem | 102: 45% lymphoma, 22% myeloma, 13% MDS/AML, 10% CLL, 10% MPNs | 76 (33-93) | 67/35 | BNT162b2, 93%; mRNA-1273, 7% | SARS-CoV-2 spike, IgG; range of commercial kits using their own threshold | 21-28 days after second dose, 64 (62%) of 102 | NR | NR |
| Thakkar et al38 | Single-center prospective and retrospective cohort study/ United States | Hem Solid tumors Healthy controls | 6639% lymphoid malignancies, 27% myeloid malignancies, 33% plasma cell leukemia 134 26 | NR for hem | NR for hem | BNT162b2, 58%; mRNA-1273, 31%; Ad26, 10%; mRNA type unknown, 2% | SARS-CoV-2 spike, IgG Abbott (≥50 AU/mL = positive) | >7 days after second dose, 56 (85%) of 66 vs 131 (98%) of 134 solid tumors; rate NR for controls | NR | NR for hem |
| Myeloma-specific | ||||||||||
| Avivi et al39 | Single-center prospective cohort study/ Israel | Myeloma Healthy volunteers | 171 64 | 70 (38-94) | 96/75 | BNT162b2 | SARS-CoV-2 spike, IgG Roche (≥0.8 IU/mL = positive) | 14-21 days after second dose, 133 (78%) of 171 vs 63 (98%) of 64 controls | NR | At least 1 AE; 90 (53%) of 161 vs 29 (55%) of 53 controls |
| Bird et al40 | Single-center retrospective cohort study/ United Kingdom | Myeloma | 93 | 67 (47-87) | 55/38 | BNT162b2, 52%; ChAdOx1, 48% | SARS-CoV-2 spike, IgG Ortho clinical (≥1 signal/cutoff = positive) | ≥21 days after first dose, 52 (56%) of 93 | NR | NR |
| Ghandili et al41 | Single-center prospective cohort study/ Germany | Myeloma | 82 | 68 (40-85) | 49/33 | BNT162b2, 77%; ChAdOx1, 23% | SARS-CoV-2 spike, IgG DiaSorin (≥34 AU/mL = positive) | 21 days after first dose, 17 (23%) of 74 | NR | NR |
| Ramasamy et al42 | Multicenter web-based prospective cohort study/ United Kingdom | Myeloma | 105-28 patients sampled | 63 | 67/42 | BNT162b2, 42%; ChAdOx1, 58% | SARS-CoV-2 spike, IgG Abbott (COV ≥50 = positive) | >21 days after first dose, 17 (61%) of 28 | NR | NR |
| Stampfer et al43 | Single-center prospective cohort study/ United States | Myeloma Healthy controls Pre-COVID-19 controls | 103 31 34 | 68 (35-88) | 61/42 | BNT162b2, 50%; mRNA-1273, 50% | SARS-CoV-2 spike, IgG in-house (50-250 IU/mL = positive partial response) (>250 IU/mL = clinically relevant response) | 14-21 days after first dose, 20 (21%) of 96; 14-21 days after second dose, 64 (67%) of 96 vs 31 (100%) of 31 controls; >250 IU/mL: 14-21 days after first dose, 2 (2%) of 96; 14-21 days after second dose, 45 (46%) of 96 vs 29 (94%) of 31 controls | NR | NR |
| Terpos et al44 | Single-center prospective cohort study/ Greece | Myeloma Matched controls | 48 102 | 83 (59-92) | 29/19 | BNT162b2 | SARS-CoV-2 nAb GenScript (≥30% = positive; ≥50% = clinically relevant) | ≥30%: 22 days after first dose, 12 (25%) of 48 vs 57 (55%) of 102 controls | ≥50%: 22 days after first dose, 4 (8%) of 48 vs 21 (20%) of 102 controls | NR |
| Terpos et al45 | Single-center prospective cohort study/ Greece | Myeloma Matched controls | 276 77% myeloma, 14% sMM, 9% MGUS 226 | 74 (62-80) | 151/125 | BNT162b2, 78%; ChAdOx1, 22% | SARS-CoV-2 nAb GenScript (≥30% = positive; ≥50% = clinically relevant) | ≥30%; day 22 after first dose, 117 (42%) of 276 vs 145 (64%) of 226 controls; day 50 after first dose, 196 (71%) of 276 vs 204 (90%) of 226 controls | ≥50%; day 22 after first dose, 55 (20%) of 276 vs 73 (32%) of 226 controls; day 50 after first dose, 158 (57%) of 276 vs 183 (81%) of 226 controls | First dose of BNT162b2, 71 (33%) of 215 local reaction; 28 (13%) of 215 systemic reaction; ChAdOx1, 20 (33%) of 61 local reaction. Second dose of BNT162b2, 68 (32%) of 215 local reaction; 45 (21%) of 215 systemic reaction |
| Van Oekelen et al46 | Single-center prospective and retrospective cohort study/ United States | Myeloma Matched health care worker controls | 320 260 sampled 67 | 68 (38-93) | 185/135 | BNT162b2, 69%; mRNA-1273, 27%; unknown, 4% | SARS-CoV-2 spike, IgG in-house (≥5 AU/mL = positive) | 51 days after second dose, 219 (84%) of 260 vs 67 (100%) of 67 controls | NR | NR |
| CLL-specific | ||||||||||
| Benjamini et al47 | Multicenter prospective cohort study/ Israel | CLL patients | 373 | 70 (40-89) | 222/151 | BNT162b2 | SARS-CoV-2 spike, IgG DiaSorin (≥15 AU/mL = positive); Abbott (>50 U/mL = positive); in-house (>1.1 = positive) | 14-21 days after second dose, 160 (43%) of 373 | nAb 14-21 days after second dose, 27 (60%) of 45 | At least 1 AE; 151 (47%) of 331 |
| Del Poeta et al48 | Single-center prospective cohort study/ Italy | CLL patients | 46 | NR | 29/17 | BNT162b2 | SARS-CoV-2 spike, IgG MAGLUMI (≥1.1 = positive) | 14-21 days after second dose, 25 (54%) of 46 | NR | NR |
| Herishanu et al49 | Single-center prospective cohort study/ Israel | CLL patients Age- and sex-matched controls | 167 52 | 71 (63-76) | 112/55 | BNT162b2 | SARS-CoV-2 spike, IgG Roche (≥0.8 IU/mL = positive) | 14-21 days after second dose, 66 (40%) of 167 patients vs 52 (100%) of 52 controls | NR | First dose, 52 (31%) of 167 local reaction; 21 (13%) of 167 systemic reaction. Second dose, 56 (34%) of 167 local reaction; 21 (23%) of 167 systemic reaction |
| Parry et al50 | Single-center prospective cohort study/ United Kingdom | CLL patients Healthy age-matched controls | 299 93 | 69 (IQR, 63-74) | 159/140 | BNT162b2, 52%; ChAxOd1, 48% | SARS-CoV-2 spike, IgG Roche (≥0.8 IU/mL = positive); dried blood sampling Roche (ratio ≥1.0 = positive) | 43 days after first dose, serum 29 (34%) of 86 vs 89 (94%) of 95 controls; dried blood* 63 (24%) of 267 vs 66 (71%) of 93 controls; 18 days after second dose, serum 9 (75%) of 12 vs 59 (100%) of 59 controls; dried blood* 39 (71%) of 55 vs 36 (97%) of 37 controls | NR | NR |
| Roeker et al51 | Single-center retrospective cohort study United States | CLL patients | 44 | 71 (37-89) | 23/21 | BNT162b2, 57%; mRNA-1273, 43% | SARS-CoV-2 spike, IgG DiaSorin (≥15 AU/mL = positive) | 21 days after second dose, 23 (52%) of 44 | NR | NR |
| Tadmor et al52 | Multicenter prospective observation study/ Israel | CLL patients | 84 | 69 (44-87) | 53/29 | BNT162b2 | SARS-CoV-2 spike, IgG Abbott (≥50 U/mL = positive); SARS-CoV-2 RBD IgG (>1.1 = positive) | 22 days after second dose, 49 (58%) of 84 | NR | NR |
| Lymphoma-specific | ||||||||||
| Ghione et al53 | Single-center prospective cohort study/ United States | B-cell lymphoma Nursing home controls Health care worker controls | 86 47 154 | 70 (35-91) | 45/41 | BNT162b2, 47%; mRNA-1273, 52%; Ad26, 1% | SARS-CoV-2 spike, IgG BioRad (≥1.0 = positive) | 14-56 days after completion of vaccination, 36 (42%) of 86 patients vs 43 (92%) of 47 nursing home controls, 154 (100%) of 154 health care worker controls | NR | NR |
| Gurion et al54 | Multicenter prospective cohort study/ Israel | Lymphoma | 162: 88% NHL, 12% HL | 65 (52-73) | 89/73 | BNT162b2 | SARS-CoV-2 spike, IgG Abbott (≥50 IU/mL = positive) | 28 days after second dose, 83 (51%) of 162 | NR | NR |
| Lim et al55 | Multicenter prospective cohort study interim analysis/ United Kingdom | Lymphoma Healthy controls | 129 recruited, 119 analyzed/ 150: 66% indolent B-cell NHL, 29% aggressive B-cell NHL, 10% HL, 3% other | 69 (IQR, 57-74) | 81/48 | BNT162b2, ChAdOx1 | SARS-CoV-2 spike, IgG Meso Scale Discovery (>0.55 BAU/mL = positive); RBD IgG (>0.73 BAU/mL = positive) | 14 days after first dose, 32 (54%) of 59 patients vs 65 (100%) of 65 controls; 14-28 days after second dose, 61 (71%) of 86 patients vs 85 (100%) of 85 controls | NR | NR |
| Perry et al56 | Single-center prospective cohort study/ Israel | Lymphoma, B-cell NHL Healthy controls | 149 53% indolent NHL, 47% aggressive NHL 65 | 64 (20-92) | 88/61 | BNT162b2 | SARS-CoV-2 spike, IgG Roche (≥0.8 IU/mL = positive) | 14-21 days after second dose, 73 (49%) of 149 vs 64 (99%) of 65 controls; 38 (48%) of 80 indolent NHL; 34 (49%) of 69 aggressive NHL | NR | At least 1 AE; 60 (51%) of 118; 44 (37%) of 118 local AE; 23 (20%) of 118 systemic AE |
| HCT-specific | ||||||||||
| Easdale et al57 | Single-center retrospective cohort study/ United Kingdom | Allo-HCT >3 months | 55 | 50 (18-73) | 34/21 | BNT162b2, 38%; ChAdOx1, 62% | SARS-CoV-2 spike, IgG Ortho clinical (≥1 signal/cutoff = positive) | 42 days after first dose, 21 (38%) of 55 | NR | NR |
| Redjoul et al58 | Single-center retrospective cohort study/ France | Allo-HCT | 88 | NR | 47/41 | BNT162b2 | SARS-CoV-2 spike, IgG Abbott (>21 AU/mL = positive; >4160 AU/mL = neutralization) | 28 days after second dose, 69 (78%) of 88; >4160 AU/mL 28 days after second dose, 52 (59%) of 88 | NR | NR |
| Ram et al59 | Single-center prospective cohort study/ Israel | Allo-HCT and CAR T cells >3 months | 80: 83% allo-HCT, 17% CAR T cells | 65 (23-83) | 44/37 | BNT162b2 | SARS-CoV-2 spike, IgG Roche (≥0.8 U/mL = positive); SARS-CoV-2–specific cells ELISPOT (IFN, IL-2) (4 spots per well = positive) | 7-14 days after second dose, 47 (75%) of 63 allo-HCT; 5 (36%) of 14 CAR T cells | Cellular response 7-14 days after second dose, 7 (19%) of 37 allo-HCT; 6 (50%) of 12 CAR T cells | At least 1 AE; first dose, 11 (14%) of 80, 3 (4%) of 80 GVHD; second dose, 18 (24%) of 74, 3 (4%) of 74 GVHD |
| Dhakal et al60 | Single-center retrospective cohort study/ United States | Auto-HCT, allo-HCT, CAR T cells | 130: 45 auto-HCT, 71 allo-HCT, 14 CAR T cells | Auto-HCT, 65 (45-75); allo-HCT, 64 (25-77); CAR T cells, NR | NR | BNT162b2, 59%; mRNA-1273, 36%; Ad26, 5% | SARS-CoV-2 spike, IgG EUROIMMUN (≥1.1 signal/cutoff = positive) | 14 days after completion of vaccination, 27 (60%) of 45 auto-HCT; 49 (38%) of 71 allo-HCT; 3 (21%) of 14 CAR T cells | NR | NR |
| MPN- and CML-specific | ||||||||||
| Caocci et al61 | Single-center prospective cohort study/ Italy | MPN | 20: 65% MF, 30% ET, 5% PV | 66 (48-82) | NR | BNT162b2 | SARS-CoV-2 spike, IgG DiaSorin (≥15 AU/mL = positive) | 42 days after second dose, 13 (65%) of 20 | NR | NR |
| Chowdhury et al62 | Single-center retrospective cohort/ United Kingdom | CML and MPN Health care workers age >60 years | 59 232 | 62 (IQR, 52-73) | 27/32 | BNT162b2, 37%; ChAdOx1, 63% | SARS-CoV-2 spike, IgG Abbott (≥50 AU/mL = positive) | ≥2 weeks after first dose, 34 (57%) of 59 vs 224 (97%) of 232 controls | NR | NR |
| Guglielmelli et al63 | Single-center prospective cohort study/ Italy | MPN Healthy controls | 30 43% MF, 33% PV, 23% ET 14 | NR overall | 10/20 | BNT162b2, 83%; mRNA-1273, 17% | SARS-CoV-2 spike/RBD IgG (NS) | 21 to 28 days after first dose, 18 (60%) of 30 vs 14 (100%) of 14 controls | nAb, 21-28 days after first dose, 13 (43%) of 30 vs 14 (100%) of 14 controls | NR |
| Harrington et al64 | Single-center prospective cohort study/ United Kingdom | CML | 16 | 45 (23-74) | 12/4 | BNT162b2 | SARS-CoV-2 spike, IgG in-house (1:25 = positive); SARS-CoV-2 neutralizing in-house (ID50 = positive); SARS-CoV-2 T cells ICA (IFN, IL-2) (threefold increase = positive) | 21 days after first dose, 14 (88%) of 16 | nAb 21 days after first dose, 6 (38%) of 16; cellular response, 14 (80%) of 15 | Local AEs, 8 (50%) of 16; systemic AEs, 9 (56%) of 16 |
| Harrington et al65 | Single-center prospective cohort study/ United Kingdom | MPN | 21 | 58 (36-72) | 7/21 | BNT162b2 | SARS-CoV-2 spike, IgG in-house (1:25 = positive); SARS-CoV-2 neutralizing in-house (ID50 = positive); SARS-CoV-2 T cells ICA (IFN, IL-2) (threefold increase = positive) | 21 days after first dose, 16 (76%) of 21 | nAb 21 days after first dose, 18 (86%) of 21; cellular response (CD4), 15 (75%) of 20 | At least 1 AE; 12 (57%) of 21 local; 10 (48%) of 21 systemic |
| Pimpinelli et al66 | Single-center prospective cohort study/ Italy | MPN | 42: 40% ET, 36% PV, 24% MF | 72 (52-82) | 20/22 | BNT162b2 | SARS-CoV-2 spike, IgG DiaSorin (≥15 AU/mL = positive) | 21 days after first dose, 23 (55%) of 42; 14 days after second dose, 36 (86%) of 42 | NR | NR |
| Study . | Type/location . | Study population/comparator . | No. of participants analyzed/controls . | Median age, y (range or IQR) . | M/F . | Vaccine type . | Analysis . | Seropositivity . | Rate of positive nAb/cellular response . | AEs . |
|---|---|---|---|---|---|---|---|---|---|---|
| Mixed-group | ||||||||||
| Addeo et al23 | Multicenter prospective cohort study Europe, North America | Hem Solid tumor | 25 106 | NR for hem | NR for hem | BNT162b2, mRNA-1273, NR for hem | SARS-CoV-2 spike, IgG Roche (≥0.8 IU/mL = positive) | Hem: 3-4 weeks after first dose, 18 (72%) of 25; 3-4 weeks after second dose, 17 (77%) of 22. Solid tumor: first dose, 80 (83%) of 96; second dose, 99 (98%) of 101 | NR | NR |
| Agha et al24 | Single-center retrospective cohort study/ United States | Hem | 67 | 71 (IQR, 65-77) | 35/32 | BNT162b2, mRNA-1273, 51%; 42%; unknown, 7% | SARS-CoV-2 spike, IgG Beckman Coulter (≥1.00 = positive) | 21 days after second dose, 36 (54%) of 67 | NR | NR |
| Benda et al25 | Single-center prospective cohort study/ Austria | Hem Solid tumor | 123 34% myeloma, 38% CLL/lymphoma/WM, 28% AML/MDS/MPNs 136 | NR for hem | NR for hem | BNT162b2 | SARS-CoV-2 spike, IgG Roche (≥0.8 IU/mL = positive) | 21 days after first dose, 53 (43%) of 123; 28 days after second dose, 85 (71%) of 119 | NR | NR for hem |
| Cohen et al26 | Single-center retrospective study/Israel | Hem | 54 | 69 (IQR, 61-77) | 32/22 | BNT162b2 | SARS-CoV-2 spike, IgG Roche (≥0.8 IU/mL = positive) | 2-3 weeks after second dose, 34 (63%) of 54 | NR | NR |
| Gavriatopoulou et al27 | Single-center prospective cohort study/ Greece | Hem Control group | 58 48% WM, 38% CLL, 14% NHL 213 | 75 (40-88) | 28/30 | BNT162b2, 76%; ChAdOx1, 24% | nAb GenScript (≥30% = positive; ≥50% = clinically relevant inhibition) | 22 days after first dose, ≥30%, 8 (14%) of 58 patients vs 114 (54%) of 213 controls | 22 days after first dose, ≥50%, 3 (5%) of 58 patients vs 50 (24%) of 213 controls | NR |
| Greenberger et al28 | Multicenter prospective cohort study/ United States | Hem | 1445: 45% CLL, 25% NHL, 5% HL, 15% MM, 4% acute leukemia, 2% CML, 2% MPNs, 2% other | 68 (16-110) | 574/871 | BNT162b2, 55%; mRNA-1273, 45% | SARS-CoV-2 spike, IgG Roche (≥0.8 IU/mL = positive) | >14days after second dose, 1088 (75%) of 1445 | NR | NR |
| Herzog Tzarfati et al29 | Single-center prospective cohort study/ Israel | Hem Matched healthy controls | 315 22% MPNs, 17% myeloma, 16% aggressive NHL, 13% indolent NHL, 11% CLL, 7% CML, 5% HL, 5% acute leukemia, 5% MDS 108 | 70 (IQR, 61-77) | 223/200 | BNT162b2 | SARS-CoV-2 spike, IgG DiaSorin (≥12 AU/mL = positive) | 30-60 days after second dose, 235 (75%) of 315 vs 107 (99%) of 108 controls | NR | NR |
| Iacano et al30 | Single-center prospective cohort study/ Italy | Hem ≥80 y; health care worker controls ≥66 y (results NR) | 10 | NR for hem | NR for hem | BNT162b2 | SARS-CoV-2 spike, IgG Abbott (≥50 AU/mL = positive) | 28 days after second dose, 4 (40%) of 10 | NR | NR |
| Jurgens et al31 | Single-center prospective cohort study/ United States | Hem Health care worker controls | 67 31% CLL, 63% NHL, 6% HL 35 | 71 (24-90) | 36/31 | BNT162b2, 46%; mRNA-1273, 54% | SARS-CoV-2 spike, IgG in-house (OD 450 ≥3 = positive) | 21 days after second dose, 41 (61%) of 67 vs 35 (100%) of 35 controls | NR | NR |
| Maneikis et al32 | Multicenter prospective cohort study/ Europe | Hem Health care worker controls | 857 68 | 65 (IQR, 54-72) | 404/453 | BNT162b2 | SARS-CoV-2 spike, IgG Abbott (≥50 AU/mL = positive) | 7-21days after first dose, 481 (56%) of 857; NR for control group | NR | At least 1 AE; dose 1, 56 (9%) of 575; dose 2, 72 (13%) of 575 |
| Malard et al33 | Single-center retrospective cohort study/ France | Hem Healthy controls | 195 27% myeloma, 23% NHL, 3% HL, 13% CLL, 16% AML, 2% ALL, 9% MPNs, 7% other 30 | 69 (22-92) | 117/78 | BNT162b2 | SARS-CoV-2 spike, IgG Abbott (≥50 AU/mL = positive; ≥3100 AU/mL = neutralization >30%; SARS-CoV-2 T-cell response, ELISPOT ≥10 spot-forming cells per 106 PBMCs and ratio 2.5 = positive) | ≥3100 AU/mL threshold*; 28 days after first dose, 3 (2%) of 195; 14 days after second dose, 91 (47%) of 196 vs 26 (87%) of 30 controls | Cellular response 14 days after second dose, 36 (53%) of 68 | At least 1 AE; dose 1, 88 (57%) of 154; dose 2, 55 (34%) of 163 |
| Monin et al34 | Multicenter prospective cohort study/ United Kingdom | Hem Health care worker controls | 56: 68% B-cell malignancies, 9% T-cell malignancies, 18% myeloid or acute leukemia, 5% other 54 | 73 (IQR, 65-80) | NE for hem | BNT162b2 | SARS-CoV-2 spike, IgG (≥70 EC50 = positive); SARS-CoV-2–specific T-cells secreting IFN-γ and/or IL-2 >7 cytokine-secreting cells per 106 PBMCs = positive) | 21 days after first dose, 8 (18%) of 44 vs 32 (94%) of 34 controls; 35 days after first dose, 4 (11%) of 36 vs 18 (86%) of 21 controls; 35 days after first dose (with second dose), 3 (60%) of 5 vs 12 (100%) of 12 controls | Cellular response 21 days after first dose, 9 (50%) of 18 vs 14 (82%) of 17 controls; 35 days after first dose, 6 (33%) of 18 vs 9 (69%) of 13 controls; 35 days after first dose (with second dose), 3 (75%) of 4 vs 3 (100%) of 3 controls | NE for hem patients |
| Ollila et al35 | Single-center retrospective cohort study/ United States | Hem | 160: 36% aggressive and 21% indolent lymphoma, 15% plasma cell leukemia, 12% CLL, 9% other lymphoma, 6% myeloid leukemia | 72 (65-79) | 86/74 | BNT162b2, 60%; mRNA-1273, 31%; Ad26, 7%; ND, 1% | SARS-CoV-2 spike, IgG Abbott (signal/cutoff ratio ≥1.4 = positive) | 56 days after first dose, 63 (39%) of 160 | NR | NR |
| Pimpinelli et al36 | Single-center prospective study/ Italy | Hem Older age (>80 y) control group | 92 46% myeloma, 54% MPN 36 | 73 (47-78)/ 70 (28-80) | Myeloma: 23/19; MPN: 26/24 | BNT162b2 | SARS-CoV-2 spike, IgG DiaSorin (≥15 AU/mL = positive) | 21 days after first dose, 9 (21%) of 42; myeloma, 26 (52%) of 50 MPNs vs 19 (53%) of 36 controls; 14 days after second dose, 33 (79%) of 42; myeloma 44 (88%) of 50 MPNs vs 36 (100%) of 36 controls; ≥80 AU/mL threshold*: 14 days after second dose, 23 (55%) of 42; myeloma 42 (84%) of 50 MPNs vs 34 (97%) of 36 controls | NR | Reported with different patient numbers |
| Re et al37 | Multicenter retrospective cohort study/ France | Hem | 102: 45% lymphoma, 22% myeloma, 13% MDS/AML, 10% CLL, 10% MPNs | 76 (33-93) | 67/35 | BNT162b2, 93%; mRNA-1273, 7% | SARS-CoV-2 spike, IgG; range of commercial kits using their own threshold | 21-28 days after second dose, 64 (62%) of 102 | NR | NR |
| Thakkar et al38 | Single-center prospective and retrospective cohort study/ United States | Hem Solid tumors Healthy controls | 6639% lymphoid malignancies, 27% myeloid malignancies, 33% plasma cell leukemia 134 26 | NR for hem | NR for hem | BNT162b2, 58%; mRNA-1273, 31%; Ad26, 10%; mRNA type unknown, 2% | SARS-CoV-2 spike, IgG Abbott (≥50 AU/mL = positive) | >7 days after second dose, 56 (85%) of 66 vs 131 (98%) of 134 solid tumors; rate NR for controls | NR | NR for hem |
| Myeloma-specific | ||||||||||
| Avivi et al39 | Single-center prospective cohort study/ Israel | Myeloma Healthy volunteers | 171 64 | 70 (38-94) | 96/75 | BNT162b2 | SARS-CoV-2 spike, IgG Roche (≥0.8 IU/mL = positive) | 14-21 days after second dose, 133 (78%) of 171 vs 63 (98%) of 64 controls | NR | At least 1 AE; 90 (53%) of 161 vs 29 (55%) of 53 controls |
| Bird et al40 | Single-center retrospective cohort study/ United Kingdom | Myeloma | 93 | 67 (47-87) | 55/38 | BNT162b2, 52%; ChAdOx1, 48% | SARS-CoV-2 spike, IgG Ortho clinical (≥1 signal/cutoff = positive) | ≥21 days after first dose, 52 (56%) of 93 | NR | NR |
| Ghandili et al41 | Single-center prospective cohort study/ Germany | Myeloma | 82 | 68 (40-85) | 49/33 | BNT162b2, 77%; ChAdOx1, 23% | SARS-CoV-2 spike, IgG DiaSorin (≥34 AU/mL = positive) | 21 days after first dose, 17 (23%) of 74 | NR | NR |
| Ramasamy et al42 | Multicenter web-based prospective cohort study/ United Kingdom | Myeloma | 105-28 patients sampled | 63 | 67/42 | BNT162b2, 42%; ChAdOx1, 58% | SARS-CoV-2 spike, IgG Abbott (COV ≥50 = positive) | >21 days after first dose, 17 (61%) of 28 | NR | NR |
| Stampfer et al43 | Single-center prospective cohort study/ United States | Myeloma Healthy controls Pre-COVID-19 controls | 103 31 34 | 68 (35-88) | 61/42 | BNT162b2, 50%; mRNA-1273, 50% | SARS-CoV-2 spike, IgG in-house (50-250 IU/mL = positive partial response) (>250 IU/mL = clinically relevant response) | 14-21 days after first dose, 20 (21%) of 96; 14-21 days after second dose, 64 (67%) of 96 vs 31 (100%) of 31 controls; >250 IU/mL: 14-21 days after first dose, 2 (2%) of 96; 14-21 days after second dose, 45 (46%) of 96 vs 29 (94%) of 31 controls | NR | NR |
| Terpos et al44 | Single-center prospective cohort study/ Greece | Myeloma Matched controls | 48 102 | 83 (59-92) | 29/19 | BNT162b2 | SARS-CoV-2 nAb GenScript (≥30% = positive; ≥50% = clinically relevant) | ≥30%: 22 days after first dose, 12 (25%) of 48 vs 57 (55%) of 102 controls | ≥50%: 22 days after first dose, 4 (8%) of 48 vs 21 (20%) of 102 controls | NR |
| Terpos et al45 | Single-center prospective cohort study/ Greece | Myeloma Matched controls | 276 77% myeloma, 14% sMM, 9% MGUS 226 | 74 (62-80) | 151/125 | BNT162b2, 78%; ChAdOx1, 22% | SARS-CoV-2 nAb GenScript (≥30% = positive; ≥50% = clinically relevant) | ≥30%; day 22 after first dose, 117 (42%) of 276 vs 145 (64%) of 226 controls; day 50 after first dose, 196 (71%) of 276 vs 204 (90%) of 226 controls | ≥50%; day 22 after first dose, 55 (20%) of 276 vs 73 (32%) of 226 controls; day 50 after first dose, 158 (57%) of 276 vs 183 (81%) of 226 controls | First dose of BNT162b2, 71 (33%) of 215 local reaction; 28 (13%) of 215 systemic reaction; ChAdOx1, 20 (33%) of 61 local reaction. Second dose of BNT162b2, 68 (32%) of 215 local reaction; 45 (21%) of 215 systemic reaction |
| Van Oekelen et al46 | Single-center prospective and retrospective cohort study/ United States | Myeloma Matched health care worker controls | 320 260 sampled 67 | 68 (38-93) | 185/135 | BNT162b2, 69%; mRNA-1273, 27%; unknown, 4% | SARS-CoV-2 spike, IgG in-house (≥5 AU/mL = positive) | 51 days after second dose, 219 (84%) of 260 vs 67 (100%) of 67 controls | NR | NR |
| CLL-specific | ||||||||||
| Benjamini et al47 | Multicenter prospective cohort study/ Israel | CLL patients | 373 | 70 (40-89) | 222/151 | BNT162b2 | SARS-CoV-2 spike, IgG DiaSorin (≥15 AU/mL = positive); Abbott (>50 U/mL = positive); in-house (>1.1 = positive) | 14-21 days after second dose, 160 (43%) of 373 | nAb 14-21 days after second dose, 27 (60%) of 45 | At least 1 AE; 151 (47%) of 331 |
| Del Poeta et al48 | Single-center prospective cohort study/ Italy | CLL patients | 46 | NR | 29/17 | BNT162b2 | SARS-CoV-2 spike, IgG MAGLUMI (≥1.1 = positive) | 14-21 days after second dose, 25 (54%) of 46 | NR | NR |
| Herishanu et al49 | Single-center prospective cohort study/ Israel | CLL patients Age- and sex-matched controls | 167 52 | 71 (63-76) | 112/55 | BNT162b2 | SARS-CoV-2 spike, IgG Roche (≥0.8 IU/mL = positive) | 14-21 days after second dose, 66 (40%) of 167 patients vs 52 (100%) of 52 controls | NR | First dose, 52 (31%) of 167 local reaction; 21 (13%) of 167 systemic reaction. Second dose, 56 (34%) of 167 local reaction; 21 (23%) of 167 systemic reaction |
| Parry et al50 | Single-center prospective cohort study/ United Kingdom | CLL patients Healthy age-matched controls | 299 93 | 69 (IQR, 63-74) | 159/140 | BNT162b2, 52%; ChAxOd1, 48% | SARS-CoV-2 spike, IgG Roche (≥0.8 IU/mL = positive); dried blood sampling Roche (ratio ≥1.0 = positive) | 43 days after first dose, serum 29 (34%) of 86 vs 89 (94%) of 95 controls; dried blood* 63 (24%) of 267 vs 66 (71%) of 93 controls; 18 days after second dose, serum 9 (75%) of 12 vs 59 (100%) of 59 controls; dried blood* 39 (71%) of 55 vs 36 (97%) of 37 controls | NR | NR |
| Roeker et al51 | Single-center retrospective cohort study United States | CLL patients | 44 | 71 (37-89) | 23/21 | BNT162b2, 57%; mRNA-1273, 43% | SARS-CoV-2 spike, IgG DiaSorin (≥15 AU/mL = positive) | 21 days after second dose, 23 (52%) of 44 | NR | NR |
| Tadmor et al52 | Multicenter prospective observation study/ Israel | CLL patients | 84 | 69 (44-87) | 53/29 | BNT162b2 | SARS-CoV-2 spike, IgG Abbott (≥50 U/mL = positive); SARS-CoV-2 RBD IgG (>1.1 = positive) | 22 days after second dose, 49 (58%) of 84 | NR | NR |
| Lymphoma-specific | ||||||||||
| Ghione et al53 | Single-center prospective cohort study/ United States | B-cell lymphoma Nursing home controls Health care worker controls | 86 47 154 | 70 (35-91) | 45/41 | BNT162b2, 47%; mRNA-1273, 52%; Ad26, 1% | SARS-CoV-2 spike, IgG BioRad (≥1.0 = positive) | 14-56 days after completion of vaccination, 36 (42%) of 86 patients vs 43 (92%) of 47 nursing home controls, 154 (100%) of 154 health care worker controls | NR | NR |
| Gurion et al54 | Multicenter prospective cohort study/ Israel | Lymphoma | 162: 88% NHL, 12% HL | 65 (52-73) | 89/73 | BNT162b2 | SARS-CoV-2 spike, IgG Abbott (≥50 IU/mL = positive) | 28 days after second dose, 83 (51%) of 162 | NR | NR |
| Lim et al55 | Multicenter prospective cohort study interim analysis/ United Kingdom | Lymphoma Healthy controls | 129 recruited, 119 analyzed/ 150: 66% indolent B-cell NHL, 29% aggressive B-cell NHL, 10% HL, 3% other | 69 (IQR, 57-74) | 81/48 | BNT162b2, ChAdOx1 | SARS-CoV-2 spike, IgG Meso Scale Discovery (>0.55 BAU/mL = positive); RBD IgG (>0.73 BAU/mL = positive) | 14 days after first dose, 32 (54%) of 59 patients vs 65 (100%) of 65 controls; 14-28 days after second dose, 61 (71%) of 86 patients vs 85 (100%) of 85 controls | NR | NR |
| Perry et al56 | Single-center prospective cohort study/ Israel | Lymphoma, B-cell NHL Healthy controls | 149 53% indolent NHL, 47% aggressive NHL 65 | 64 (20-92) | 88/61 | BNT162b2 | SARS-CoV-2 spike, IgG Roche (≥0.8 IU/mL = positive) | 14-21 days after second dose, 73 (49%) of 149 vs 64 (99%) of 65 controls; 38 (48%) of 80 indolent NHL; 34 (49%) of 69 aggressive NHL | NR | At least 1 AE; 60 (51%) of 118; 44 (37%) of 118 local AE; 23 (20%) of 118 systemic AE |
| HCT-specific | ||||||||||
| Easdale et al57 | Single-center retrospective cohort study/ United Kingdom | Allo-HCT >3 months | 55 | 50 (18-73) | 34/21 | BNT162b2, 38%; ChAdOx1, 62% | SARS-CoV-2 spike, IgG Ortho clinical (≥1 signal/cutoff = positive) | 42 days after first dose, 21 (38%) of 55 | NR | NR |
| Redjoul et al58 | Single-center retrospective cohort study/ France | Allo-HCT | 88 | NR | 47/41 | BNT162b2 | SARS-CoV-2 spike, IgG Abbott (>21 AU/mL = positive; >4160 AU/mL = neutralization) | 28 days after second dose, 69 (78%) of 88; >4160 AU/mL 28 days after second dose, 52 (59%) of 88 | NR | NR |
| Ram et al59 | Single-center prospective cohort study/ Israel | Allo-HCT and CAR T cells >3 months | 80: 83% allo-HCT, 17% CAR T cells | 65 (23-83) | 44/37 | BNT162b2 | SARS-CoV-2 spike, IgG Roche (≥0.8 U/mL = positive); SARS-CoV-2–specific cells ELISPOT (IFN, IL-2) (4 spots per well = positive) | 7-14 days after second dose, 47 (75%) of 63 allo-HCT; 5 (36%) of 14 CAR T cells | Cellular response 7-14 days after second dose, 7 (19%) of 37 allo-HCT; 6 (50%) of 12 CAR T cells | At least 1 AE; first dose, 11 (14%) of 80, 3 (4%) of 80 GVHD; second dose, 18 (24%) of 74, 3 (4%) of 74 GVHD |
| Dhakal et al60 | Single-center retrospective cohort study/ United States | Auto-HCT, allo-HCT, CAR T cells | 130: 45 auto-HCT, 71 allo-HCT, 14 CAR T cells | Auto-HCT, 65 (45-75); allo-HCT, 64 (25-77); CAR T cells, NR | NR | BNT162b2, 59%; mRNA-1273, 36%; Ad26, 5% | SARS-CoV-2 spike, IgG EUROIMMUN (≥1.1 signal/cutoff = positive) | 14 days after completion of vaccination, 27 (60%) of 45 auto-HCT; 49 (38%) of 71 allo-HCT; 3 (21%) of 14 CAR T cells | NR | NR |
| MPN- and CML-specific | ||||||||||
| Caocci et al61 | Single-center prospective cohort study/ Italy | MPN | 20: 65% MF, 30% ET, 5% PV | 66 (48-82) | NR | BNT162b2 | SARS-CoV-2 spike, IgG DiaSorin (≥15 AU/mL = positive) | 42 days after second dose, 13 (65%) of 20 | NR | NR |
| Chowdhury et al62 | Single-center retrospective cohort/ United Kingdom | CML and MPN Health care workers age >60 years | 59 232 | 62 (IQR, 52-73) | 27/32 | BNT162b2, 37%; ChAdOx1, 63% | SARS-CoV-2 spike, IgG Abbott (≥50 AU/mL = positive) | ≥2 weeks after first dose, 34 (57%) of 59 vs 224 (97%) of 232 controls | NR | NR |
| Guglielmelli et al63 | Single-center prospective cohort study/ Italy | MPN Healthy controls | 30 43% MF, 33% PV, 23% ET 14 | NR overall | 10/20 | BNT162b2, 83%; mRNA-1273, 17% | SARS-CoV-2 spike/RBD IgG (NS) | 21 to 28 days after first dose, 18 (60%) of 30 vs 14 (100%) of 14 controls | nAb, 21-28 days after first dose, 13 (43%) of 30 vs 14 (100%) of 14 controls | NR |
| Harrington et al64 | Single-center prospective cohort study/ United Kingdom | CML | 16 | 45 (23-74) | 12/4 | BNT162b2 | SARS-CoV-2 spike, IgG in-house (1:25 = positive); SARS-CoV-2 neutralizing in-house (ID50 = positive); SARS-CoV-2 T cells ICA (IFN, IL-2) (threefold increase = positive) | 21 days after first dose, 14 (88%) of 16 | nAb 21 days after first dose, 6 (38%) of 16; cellular response, 14 (80%) of 15 | Local AEs, 8 (50%) of 16; systemic AEs, 9 (56%) of 16 |
| Harrington et al65 | Single-center prospective cohort study/ United Kingdom | MPN | 21 | 58 (36-72) | 7/21 | BNT162b2 | SARS-CoV-2 spike, IgG in-house (1:25 = positive); SARS-CoV-2 neutralizing in-house (ID50 = positive); SARS-CoV-2 T cells ICA (IFN, IL-2) (threefold increase = positive) | 21 days after first dose, 16 (76%) of 21 | nAb 21 days after first dose, 18 (86%) of 21; cellular response (CD4), 15 (75%) of 20 | At least 1 AE; 12 (57%) of 21 local; 10 (48%) of 21 systemic |
| Pimpinelli et al66 | Single-center prospective cohort study/ Italy | MPN | 42: 40% ET, 36% PV, 24% MF | 72 (52-82) | 20/22 | BNT162b2 | SARS-CoV-2 spike, IgG DiaSorin (≥15 AU/mL = positive) | 21 days after first dose, 23 (55%) of 42; 14 days after second dose, 36 (86%) of 42 | NR | NR |
AEs, adverse events; ALL, acute lymphocytic leukemia; AML, acute myeloid leukemia; BAU, binding antibody unit; CLL, chronic lymphotic leukemia; COV, cut-off value; EC50, median effective concentration; ET, essential thrombocythemia; F, female; GVHD, graft-versus-host disease; hem, hematology; HL, Hodgkin lymphoma; ICA, intracellular cytokine assay; ID50, median infective dose; IFN-γ, interferon-γ; IL-2, interleukin-2; IQR, interquartile range; M, male; MF, myelofibrosis; MGUS, monoclonal gammopathy of unknown significance; MM, multiple myeloma; ND, not determined; NE, not extractable; NHL, non-Hodgkin lymphoma; NR, not reported; OD, optical density; PBMC, peripheral blood mononuclear cell; PV, polycythemia vera; RBD, receptor-binding domain; SMM, smoldering multiple myeloma; WM, Waldenström macroglobulinemia.
Excluded from meta-analysis.