Introduction
Method and materials
Search strategy
Eligibility criteria
Population
Intervention
Comparison
Outcome
Study design
Risk of bias assessment
Data extraction
Statistical analysis
Results
Study selection
Characteristics of the included studies
No. | Author/ Year | Country | Design | Cell Therapy | Group | Number of Patients | Age, years | Female (%) | Background Diseases |
---|---|---|---|---|---|---|---|---|---|
1 | Abid, M. B./ 2022 [63] | United States | Prospective | Allogeneic | 26 | 68 [31–81] | 33.33 | N/R | |
Autologous | 30 | ||||||||
CAR-T cell | 10 | ||||||||
2 | Albiol, N./ 2023 [33] | Spain | Prospective | Allogeneic | G1: 3–24 months since HSCT | 49 | 56 [26–73] | 49 | AML/ MDS and other myeloid malignancies/ ALL/ Lymphomas and lymphoproliferative syndromes/ MM |
G2: > 24 months since HSCT | 19 | 60 [25–70] | 36.8 | AML/ MDS and other myeloid malignancies/ ALL/ Lymphomas and lymphoproliferative syndromes | |||||
3 | Attolico, I./ 2022 [64] | Italy | Prospective | Allogeneic | 42 | 56.5 [32–68] | 42.86 | AML/ ALL/ SAA/ CML/ MDS/ NHL/ MM/ CMML/ CLL/ HL | |
Autologous | 21 | 57 [20–71] | 47.62 | MM/ NHL/ HL | |||||
4 | Barkhordar, M./ 2023 [24] | Iran | Non-randomized clinical trial | Allogeneic | 36 | 42.42 ± 15.84 | 41.7 | AML/ ALL | |
5 | Canti, L./ 2022 [28] | Belgium | Non-randomized clinical trial | Allogeneic | 38 | 60 [54–70] | 50 | N/R | |
6 | Chevallier, P./ 2022 [65] | France | Prospective | Allogeneic | 124 | 58 [20–77] | 40.43 | Myeloid/ Lymphoid | |
7 | Debie, Y./ 2021 [27] | Belgium | Non-randomized clinical trial | Allogeneic | 10 | N/R | N/R | CLL and Lymphoma/ Myeloid malignancies/ Other | |
8 | Einarsdottir, S./ 2022 [34] | Sweden | Non-randomized clinical trial | Allogeneic | 37 | 61.5 [19–78] | N/R | AML/ ALL/ MDS/ MF/ CML/ ACML/ Myeloma/ CLL/ HL | |
9 | Fatobene, G./ 2023 [30] | Brazil | Non-randomized clinical trial | Allogeneic + Autologous | 30 | 38 [20–66] | 30 | HL/ AML/ NHL | |
10 | Federico, L./ 2023 [66] | Norway | Prospective | Allogeneic | 3rd-dose | 12 | 49 [21–73] | 50 | AML/ MDS/ ALL/ AA/ Other |
4th-dose | 12 | ||||||||
11 | Gössi, S./ 2022 [49] | Switzerland | Retrospective | CAR-T cell | 3rd-dose | 23 | 64 [18–80] | 39.13 | Primary (de novo) DLBCL/ Secondary or transformed DLBCL/ MCL/ B-ALL |
4th-dose | 3 | ||||||||
12 | Haggenburg, S./ 2022 [32] | The Netherlands | Prospective | Allogeneic | 100 | Mean: 56 | 36 | N/R | |
Autologous | 69 | Mean: 60 | 30.43 | Lymphoma/ MM | |||||
CAR-T cell | 43 | Mean: 60 | 27.91 | N/R | |||||
13 | Henig, I./ 2023 [31] | Israel | Prospective | Allogeneic | 39 | 55 [20–74] | 53 | AML/ ALL/ MDS/ MPN/ Lymphoma | |
14 | Hütter-Krönke, M. L./ 2023 [55] | Germany | Retrospective | Allogeneic | 103 | 59 [22–81] | 44 | AML/ MPN/ MDS/ NHL/ ALL/ Others | |
15 | Khan, Q. J./ 2022 [67] | United States | Prospective | Allogeneic + Autologous | 53 | 59.5 [19–78] | 44 | AML + MDS/ MM/ ALL/ CLL + Lymphoma | |
16 | Kimura, M./ 2022 [38] | Canada | Prospective | Allogeneic | 64 | 57 [45–64] | 50.8 | AML/ MDS/ ALL/ MF/ CML/ CMML/ NHL/ MPAL/ HL/ AA/ CLL/ Others | |
17 | Kokogho, A./ 2023 [35] | United States | Retrospective | Allogeneic + Autologous | 3rd-dose | 55 | 62 [50–68] | 46.1 | AML and other acute leukemias/ CML and other chronic leukemias/ ALL/ Lymphomas (HL/ NHL)/ Anemias and Hemoglobinopathies/ MDS and MF/ MMs |
4th-dose | 10 | ||||||||
18 | Le Bourgeois, A./ 2021 [68] | France | Retrospective | Allogeneic | 80 | 57 [20–75] | 43.75 | Myeloid/ Lymphoid/ Others | |
19 | Liga, M./ 2022 [69] | Greece | Prospective | Allogeneic | 5 | 48 [21–76] | 45.71 | AML/ ALL/ CML/ MF/ HL/ NHL | |
20 | Loubet, P./ 2023 [70] | France | Prospective | Allogeneic + Autologous | 46 | 54.7 [39.5–65.6] | 40.2 | N/R | |
21 | Majcherek, M./ 2023 [71] | Poland | Prospective | Allogeneic | 47 | 52 [20–68] | 48 | AML/ MDS/ ALL/ NHL/ HL/ Other | |
Autologous | 21 | 58 [26–69] | 45 | NHL/ HL/ MM | |||||
22 | Maillard, A./ 2022 [54] | France | Retrospective | Allogeneic | 181 | 60.5 [49.5–66.9] | 39.23 | Myeloid malignancy/ Lymphoid malignancy | |
23 | Marco, I./ 2022 [36] | Italy | Prospective | Allogeneic | 14 | 47 [39–59] | 42.86 | ALL/ AML/ MDS/ T-ALL/ AA/ MF | |
24 | Mittal, A./ 2023 [62] | Canada | Prospective | Allogeneic | 3rd-dose | 54 | 59.5 [53.5–65.5] | 39 | AML/ ALL/ MDS/ NHL HL/ CLL/ SAA/ CMML/ MPAL/ Thalassemia/ MF |
4th-dose | 54 | ||||||||
25 | Nikoloudis, A./ 2023 [72] | Austria | Retrospective | Allogeneic | 3rd-dose | 30 | 58.10 [23.40–76.60] | 43.1 | N/R |
4th-dose | 16 | ||||||||
26 | Piñana, J. L./ 2023 [50] | Spain | Prospective | Allogeneic | 56 | 55 [16–78] | 42.7 | AML/ MDS/ NHL/ MM/ CLL/ HD/ MPN/ ALL/ Others | |
Autologous | 18 | 61 [19–79] | 43 | AML/ NHL/ MM/ HL | |||||
CAR-T cell | 3 | 59 [26–78] | 41 | NHL/ MM/ CLL/ ALL | |||||
27 | Ram, R./ 2022 [29] | Israel | Non-randomized clinical trial | Allogeneic | 10 | 66 [33–78] | 31.25 | AML/ Other lymphoma/ MPN | |
CAR-T cell | 6 | 68 [23–80] | 33 | ALL/ DLBCL | |||||
28 | Sharifi Aliabadi, L./ 2023 [25] | Iran | Randomized clinical trial | Autologous | Homologous | 30 | 51 ± 11 | 40 | Lymphoma/ MM |
Heterologous | 29 | 50 ± 11 | 26 | Lymphoma/ MM | |||||
29 | Thümmler, L./ 2022 [37] | Germany | Prospective | Allogeneic + Autologous | 18 | 61 [21–71] | 44.44 | N/R | |
30 | Tsoutsoukis, M./ 2023 [26] | United Kingdom | Retrospective | Allogeneic | 3rd-dose | 75 | N/R | N/R | N/R |
4th-dose | 75 | ||||||||
31 | Vanlerberghe, B./ 2023 [73] | Belgium | Prospective | Allogeneic + Autologous | 58 | 58 ± 14 | 34.7 | N/R | |
32 | Watanabe, M./ 2022 [74] | Japan | Prospective | Allogeneic | 22 | 56 [23–71] | 45 | AML/ ALL/ Malignant lymphoma/ Others |
No. | Author/ Year | Received Dose | Time since Cell Therapy to 1st Dose | Primary Vaccine | Additional Vaccine | Time since 2nd to 3rd Dose/ 3rd to 4th Dose | Antibody Detection Method; Criteria for Determining Seropositivity |
---|---|---|---|---|---|---|---|
1 | Abid, M. B./ 2022 [63] | 3 | N/R | BNT162b2/ mRNA-1273 | BNT162b2/ mRNA-1273/ mix-and-match | At least 28 days | AdviseDx SARS-CoV-2 IgG II assay; ≥ 50 AU/mL |
2 | Albiol, N./ 2023 [33] | 3 | G1: Median: 14 [range 3–24] months G2: Median: 43 [range 30–90] months | mRNA-1273 | mRNA-1273 | 5–6 months | SARS-CoV-2 IgG II Quant test (Abbott, Illinois, USA); ≥ 0.417 AU |
3 | Attolico, I./ 2022 [64] | 3 | G1: ≤ 1 year G2:1–5 years G3 ≥ 5 years | BNT162b2 | BNT162b2 | N/R | Abbott immunoassay; ≥ 50 AU/ml |
4 | Barkhordar, M./ 2023 [24] | 3 | Median: 133 days [IQR 107.5–228] | Receptor-binding domain (RBD)–tetanus toxoid (TT)-conjugated SARS-CoV-2 vaccine (Soberana 2) | Receptor-binding domain (RBD)–tetanus toxoid (TT)-conjugated SARS-CoV-2 vaccine (Soberana 2) | 1 month | ChemoBind SARS-CoV-2 Neutralizing Antibody Test Kit (ChemoBind, Tehran, Iran); > 1.1 ISR |
5 | Canti, L./ 2022 [28] | 3 | Median: 31 months [IQR 14–42] | BNT162b2 | BNT162b2 | 14–26 weeks | WANTAI SARS-Cov-2 Ab ELISA (Beijing Wantai Biological Pharmacy Enterprise, Beijing, China) |
6 | Chevallier, P./ 2022 [65] | 3 | Median: 33.5 months [range 3–282] | BNT162b2 | BNT162b2 | Median: 44 [range 20–205] days | Roche S tAb/ Abbott S IgG/ DiaSorin TriS/ Atellica/ Novalisa |
7 | Debie, Y./ 2021 [27] | 3 | N/R | BNT162b2 | BNT162b2 | 183 ± 10 days | Wantai SARS-CoV-2 IgG ELISA (Quantitative); CE-marked; WS-1396; lot NCOG120210301; Beijing Wantai Biological Pharmacy Enterprise Co., Ltd., China |
8 | Einarsdottir, S./ 2022 [34] | 3 | N/R | BNT162b2/ mRNA-1273 | BNT162b2/ mRNA-1273 | Median: 127 days [range 56–174] | SARS-CoV-2 IgG II Quant (Abbott, Illinois, USA); ≥ 14 BAU/mL |
9 | Fatobene, G./ 2023 [30] | 3 | Median: 5 [range: 1–212] months | CoronaVac | BNT162b2 | ≥ 28 days | N/R |
10 | Federico, L./ 2023 [66] | 3 & 4 | Median: 14 [range 3–82] months | BNT162b2/ mRNA-1273 | BNT162b2/ mRNA-1273 | N/R | Multiplexed bead-based assay; > 70 AU/mL |
11 | Gössi, S./ 2022 [49] | 3 & 4 | Median: 286 days [range 23–975] | BNT162b2/ mRNA-1273 | BNT162b2/ mRNA-1273 | N/R | Anti-SARSCoV-2 IgG indirect chemiluminescence immuno assay (CLIA) (Liaison® XL by DiaSorin, Saluggia, Italy); > 12 AU/mL |
12 | Haggenburg, S./ 2022 [32] | 3 | N/R | mRNA-1273 | mRNA-1273 | 5 months | Multiplex bead-based immune assay; > 10 BAU/mL |
13 | Henig, I./ 2023 [31] | 3 | G1:< 6 months G2: 6–12 months G3:> 12 months | BNT162b2 | BNT162b2 | > 5 months | SARS-CoV-2 IgG II Quant (Abbott©, Chicago, IL, USA) assay; > 150 AU/mL |
14 | Hütter-Krönke, M. L./ 2023 [55] | 3 | Median: 750 days [range 40–10,566] | BNT162b2/ ChAdOx1-S/ mRNA-1273/ JNJ-78436735/ Mixed vaccination (mostly ChAdOx1-S followed by an mRNA-vaccine) | BNT162b2/ mRNA-1273 | Median: 173 [range 14–285] days | IgG ELISA assay (Euroimmun) or an EIA Assay (Roche); ≥ 0.8 U/ml |
15 | Khan, Q. J./ 2022 [67] | 3 | Median: 440 days | BNT162b2/ mRNA-1273/ JNJ-78436735 | BNT162b2/ mRNA-1273 | Median: 154 days | Roche Elecsys anti-SARS-CoV-2 S enzyme immunoassay; ≥ 0.8 U/ml |
16 | Kimura, M./ 2022 [38] | 3 | Median: 185 [IQR 115–524] days | BNT162b2/ mRNA-1273/ Mixed | BNT162b2/ mRNA-1273/ Mixed | N/R | Roche Elecsys anti-SARS-CoV-2 S enzyme immunoassay; > 0.8 U/mL |
17 | Kokogho, A./ 2023 [35] | 3 & 4 | Median: 140.5 [range − 48-254] days | BNT162b2/ mRNA-1273/ JNJ-78436735 | BNT162b2/ mRNA-1273 | N/R | Roche Elecsys Anti-SARS-CoV-2 spike immunoassay; ≥ 0.8 U/mL |
18 | Le Bourgeois, A./ 2021 [68] | 3 | Median: 719 [range 91–6198] days | BNT162b2 | BNT162b2 | N/R | Roche Elecsys (Rotkreuz, Switzerland); ≥ 0.8 U/ml |
19 | Liga, M./ 2022 [69] | 3 | Median: 913.5 days [range: 137–4086] | BNT162b2/ ChAdOx1-S | N/R | N/R | Abbott SARS-CoV-2 IgG II Quant assay; ≥ 50 AU/mL |
20 | Loubet, P./ 2023 [70] | 3 | N/R | BNT162b2/ mRNA-1273 | BNT162b2/ mRNA-1273/ mix-and-match | Median: 4.1 [IQR 4.0–4.9] weeks | QuantiVac ELISA kit from Euroimmun® (Lubeck, Germany); a ratio of optic density (OD) of the sample to that of a calibratorof ≥1.1 |
21 | Majcherek, M./ 2023 [71] | 3 | Allo-G: Median: 23 [range 3–112] months Auto-G: Median: 10 [range 4–38] months | BNT162b2 | BNT162b2 | 168 [range 144–244] days | Chemiluminescent microparticle immunoassay (CMIA) “Alinity I” from Abbott Diagnostic |
22 | Maillard, A./ 2022 [54] | 3 | Median: 18.5 [IQR 10.1–42.6] months | BNT162b2/ mRNA-1273 | BNT162b2/ mRNA-1273 | Median: 54.0 [IQR 34.0–73.8] days | Abbott SARS-CoV-2 IgG II Quant-test (Abbott S IgG); ≥ 50 AU/mL/ Roche Elecsys anti-SARS-CoV-2 S (Roche S tAb); ≥ 0.8 U/ml/ DiaSorin Liaison SARS-CoV-2 TrimericS IgG (DiaSorin TriS IgG); ≥ 13 AU/ml/ Siemens SARS-CoV-2 IgG (Siemens sCOVG); ≥ 1.0 U/ml/ Wantai SARS-CoV-2 IgG ELISA (Wantai S IgG); ≥ 0.75 AU/ml |
23 | Marco, I./ 2022 [36] | 3 | N/R | BNT162b2 | BNT162b2 | N/R | N/A |
24 | Mittal, A./ 2023 [62] | 3 & 4 | N/R | BNT162b2/ mRNA-1273 | BNT162b2/ mRNA-1273 | 2nd to 3rd: N/R | Roche Elecsys anti-SARS-CoV-2 S enzyme immunoassay; ≥ 0.8 U/mL |
3rd to 4th: Median: 135.5 [IQR 121.7–161.5] days | |||||||
25 | Nikoloudis, A./ 2023 [72] | 3 & 4 | Median: 30.89 [range 2.53–215.07] months | BNT162b2/ mRNA-1273 | BNT162b2/ mRNA-1273 | 2nd to 3rd: Median: 189 [range 56–273] days | SARS-CoV-2 IgG II Quant assay (Abbott, Ireland); ≥ 7.1 BAU/mL |
3rd to 4th: Median: 110 days | |||||||
26 | Piñana, J. L./ 2023 [50] | 3 | Allo-G: Median: 33 [range: 2–317] months Auto-G: Median: 36 [range: 3–305] months CAR-T-G: Median: 9.6 [range: 4.4–23.5] months | BNT162b2/ mRNA-1273/ Adenoviral vector-based | BNT162b2/ mRNA-1273 | Allo-G: Median: 161 [range 31–390] days Auto-G: Median: 149 [range 69–538] days CAR-T-G: Median: 182 [range 122–253] days | Architect SARS-CoV-2 IgG Quant II chemiluminescent microparticle immunoassay (Abbott Diagnostics, Ill, USA)/ Liaison SARS-CoV-2 S1/S2 IgG chemiluminescent assay (DiaSorin S.p.A., Saluggia, Italy)/ MAGLUMI 2019-nCoV IgG chemiluminescent assay (SNIBE—Shenzhen New Industries Biomedical Engineering Co., Ltd., Shenzhen, China)/ Elecsys anti-SARS-CoV-2 S (Roche Diagnostics (Pleasanton, CA, USA))/ Atellica SARS-CoV-2 (Siemmens, Germany) |
27 | Ram, R./ 2022 [29] | 3 | Allo-G: Median: 31 [range 11–65] months CAR-T-G: Median: 14 [range 8–17] months | BNT162b2 | BNT162b2 | Median: 5.2 [range 5.1–5.6] months | SARS-CoV-2 IgG II Quant, Cat no. 6S60; Abbott Ireland; > 150 AU/mL |
28 | Sharifi Aliabadi, L./ 2023 [25] | 3 | Homologous arm: Median: 206 [IQR 178–265] days Hetrologous arm: Median: 219 [IQR 178–277] days | Receptor-binding domain (RBD)–tetanus toxoid (TT)-conjugated SARS-CoV-2 vaccine (Soberana 2) | Receptor-binding domain (RBD)–tetanus toxoid (TT)-conjugated SARS-CoV-2 vaccine (Soberana 2)/ CoronaVac | 1 month | ChemoBind SARS-CoV-2 Neutralizing Antibody Test Kit (ChemoBind, Tehran, Iran); > 1.1 ISR |
29 | Thümmler, L./ 2022 [37] | 3 | Median: 4.1 years [range 0.5–24] | N/R | N/R | N/R | CE-marked anti-SARSCoV- 2 IgG semiquantitative ELISA (Euroimmun, Lübeck, Germany) and a quantitative ELISA (anti-SARS-CoV-2-QuantiVac-ELISA, Euroimmun, Lübeck, Germany)- |
30 | Tsoutsoukis, M./ 2023 [26] | 3 & 4 | Median: 145 days [range 79–700] | BNT162B2/ mRNA-1273/ ChAdOx1-S | BNT162B2/ mRNA-1273 | N/R | N/R |
31 | Vanlerberghe, B./ 2023 [73] | 3 | N/R | BNT162b2/ mRNA-1273/ ChAdOx1-S/ JNJ-78436735 | BNT162b2/ mRNA-1273 | N/R | Abbot’s SARS-CoV-2 IgG II Quant anti-S chemiluminescent immunoassays (CLIA); ≥ 50 AU/mL |
32 | Watanabe, M./ 2022 [74] | 3 | N/R | BNT162b2 | BNT162b2/ mRNA-1273 | Median: 219 [range 194–258] days | QuaResearch COVID-19 Human IgM IgG ELISA kit (Cellspect, Inc., RCOEL961S1, Iwate, Japan); The optimal optical density (O.D.) of anti-S1 > 0.26 |