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Table 2 Summary of vaccine-related characteristics of the included studies

From: Immunologic responses to the third and fourth doses of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccines in cell therapy recipients: a systematic review and meta-analysis

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