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Table 1 Characteristics of the included studies

From: Serologic response and safety of COVID-19 vaccination in HSCT or CAR T-cell recipients: a systematic review and meta-analysis

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

  1. Age is expressed as median (range) or median ± quartile
  2. 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