Maintenance strategies for relapse prevention and treatment

2.

DeFilipp

Z

,

Chen

Y-B

.

How I treat with maintenance therapy after allogeneic HCT

.

Blood

.

2023

;

141

(

1

):

39

-

48

.

3.

Xuan

L

,

Wang

Y

,

Huang

F

, et al.

Sorafenib maintenance in patients with FLT3-ITD acute myeloid leukaemia undergoing allogeneic haematopoietic stem-cell transplantation: an open-label, multicentre, randomised phase 3 trial

.

Lancet Oncol

.

2020

;

21

(

9

):

1201

-

1212

.

4.

Levis

MJ

,

Hamadani

M

,

Logan

B

, et al.

Gilteritinib as posttransplant maintenance for acute myeloid leukemia with internal tandem duplication mutation of FLT3

.

J Clin Oncol

.

2024

;

42

(

15

):

1766

-

1775

.

5.

Fathi

AT

,

Kim

HT

,

Soiffer

RJ

, et al.

Multicenter phase I trial of ivosidenib as maintenance treatment following allogeneic hematopoietic cell transplantation for IDH1-mutated acute myeloid leukemia

.

Clin Cancer Res

.

2023

;

29

(

11

):

2034

-

2042

.

6.

Fathi

AT

,

Kim

HT

,

Soiffer

RJ

, et al.

Enasidenib as maintenance following allogeneic hematopoietic cell transplantation for IDH2-mutated myeloid malignancies

.

Blood Adv

.

2022

;

6

(

22

):

5857

-

5865

.

7.

DeFilipp

Z

,

Ancheta

R

,

Liu

Y

, et al.

Maintenance tyrosine kinase inhibitors following allogeneic hematopoietic stem cell transplantation for chronic myelogenous leukemia: a Center for International Blood and Marrow Transplant Research Study

.

Biol Blood Marrow Transplant

.

2020

;

26

(

3

):

472

-

479

.

8.

Brissot

E

,

Labopin

M

,

Beckers

MM

, et al.

Tyrosine kinase inhibitors improve long-term outcome of allogeneic hematopoietic stem cell transplantation for adult patients with Philadelphia chromosome positive acute lymphoblastic leukemia

.

Haematologica

.

2015

;

100

(

3

):

392

-

399

.

9.

Chen

H

,

Xu

L-P

,

Zhang

X-H

, et al.

Safety and outcomes of maintenance therapy with third-generation tyrosine kinase inhibitor after allogeneic hematopoietic cell transplantation in Philadelphia chromosome positive acute lymphoblastic leukemia patients with T315I mutation

.

Leuk Res

.

2022

;

121

:

106930

.

10.

Pasvolsky

O

,

Saliba

RM

,

Popat

UR

, et al.

Azacitidine posttransplant maintenance improves disease progression in high-risk acute myeloid leukemia and myelodysplastic syndrome

.

Clin Lymphoma Myeloma Leuk

.

2024

;

24

(

5

):

e196

-

e204

.

11.

Oran

B

,

de Lima

M

,

Garcia-Manero

G

, et al.

A phase 3 randomized study of 5-azacitidine maintenance vs observation after transplant in high-risk AML and MDS patients

.

Blood Adv

.

2020

;

4

(

21

):

5580

-

5588

.

12.

Kent

A

,

Schwartz

M

,

McMahon

C

, et al.

Venetoclax is safe and tolerable as posttransplant maintenance therapy for AML patients at high risk for relapse

.

Bone Marrow Transplant

.

2023

;

58

(

8

):

849

-

854

.

13.

Garcia

JS

,

Kim

HT

,

Murdock

HM

, et al.

Prophylactic maintenance with venetoclax/azacitidine after reduced-intensity conditioning allogeneic transplant for high-risk MDS and AML

.

Blood Adv

.

2024

;

8

(

4

):

978

-

990

.

14.

Metheny

LL

,

Sobecks

R

,

Cho

C

, et al.

A multicenter study of posttransplantation low-dose inotuzumab ozogamicin to prevent relapse of acute lymphoblastic leukemia

.

Blood Adv

.

2024

;

8

(

6

):

1384

-

1391

.

15.

Gaballa

MR

,

Banerjee

P

,

Milton

DR

, et al.

Blinatumomab maintenance after allogeneic hematopoietic cell transplantation for B-lineage acute lymphoblastic leukemia

.

Blood

.

2022

;

139

(

12

):

1908

-

1919

.

16.

Kennedy-Nasser

AA

,

Ku

S

,

Castillo-Caro

P

, et al.

Ultra low-dose IL-2 for GVHD prophylaxis after allogeneic hematopoietic stem cell transplantation mediates expansion of regulatory T cells without diminishing antiviral and antileukemic activity

.

Clin Cancer Res

.

2014

;

20

(

8

):

2215

-

2225

.

17.

Magenau

JM

,

Peltier

D

,

Riwes

M

, et al.

Type 1 interferon to prevent leukemia relapse after allogeneic transplantation

.

Blood Adv

.

2021

;

5

(

23

):

5047

-

5056

.

18.

Loke

J

,

McCarthy

N

,

Jackson

A

, et al.

Posttransplant MRD and T-cell chimerism status predict outcomes in patients who received allografts for AML/MDS

.

Blood Adv

.

2023

;

7

(

14

):

3666

-

3676

.

19.

Lindahl

H

,

Vonlanthen

S

,

Valentini

D

, et al.

Lineage-specific early complete donor chimerism and risk of relapse after allogeneic hematopoietic stem cell transplantation for acute myeloid leukemia

.

Bone Marrow Transplant

.

2022

;

57

(

5

):

753

-

759

.

20.

Dekker

SE

,

Rea

D

,

Cayuela

J-M

,

Arnhardt

I

,

Leonard

J

,

Heuser

M.

Using measurable residual disease to optimize management of AML, ALL, and chronic myeloid leukemia

.

Am Soc Clin Oncol Educ Book

.

2023

;

43

:

e390010

.

21.

Vago

L

,

Perna

SK

,

Zanussi

M

, et al.

Loss of mismatched HLA in leukemia after stem-cell transplantation

.

N Engl J Med

.

2009

;

361

(

5

):

478

-

488

.

22.

Crucitti

L

,

Crocchiolo

R

,

Toffalori

C

, et al.

Incidence, risk factors and clinical outcome of leukemia relapses with loss of the mismatched HLA after partially incompatible hematopoietic stem cell transplantation

.

Leukemia

.

2015

;

29

(

5

):

1143

-

1152

.

23.

Rautenberg

C

,

Bergmann

A

,

Germing

U

, et al.

Prediction of response and survival following treatment with azacitidine for relapse of acute myeloid leukemia and myelodysplastic syndromes after allogeneic hematopoietic stem cell transplantation

.

Cancers (Basel)

.

2020

;

12

(

8

).

24.

Craddock

C

,

Jilani

N

,

Siddique

S

, et al.

Tolerability and clinical activity of posttransplantation azacitidine in patients allografted for acute myeloid leukemia treated on the RICAZA trial

.

Biol Blood Marrow Transplant

.

2016

;

22

(

2

):

385

-

390

.

25.

Schroeder

T

,

Rachlis

E

,

Bug

G

, et al.

Treatment of acute myeloid leukemia or myelodysplastic syndrome relapse after allogeneic stem cell transplantation with azacitidine and donor lymphocyte infusions–a retrospective multicenter analysis from the German Cooperative Transplant Study Group

.

Biol Blood Marrow Transplant

.

2015

;

21

(

4

):

653

-

660

.

26.

Schroeder

T

,

Fröbel

J

,

Cadeddu

R-P

, et al.

Salvage therapy with azacitidine increases regulatory T cells in peripheral blood of patients with AML or MDS and early relapse after allogeneic blood stem cell transplantation

.

Leukemia

.

2013

;

27

(

9

):

1910

-

1913

.

27.

Krakow

EF

,

Walter

RB

,

Nathe

JM

, et al.

Intensive chemotherapy for acute myeloid leukemia relapse after allogeneic hematopoietic cell transplantation

.

Am J Hematol

.

2022

;

97

(

6

):

E220

-

E223

.

28.

Joshi

M

,

Cook

J

,

McCullough

K

, et al.

Salvage use of venetoclax-based therapy for relapsed AML post allogeneic hematopoietic cell transplantation

.

Blood Cancer J

.

2021

;

11

(

3

):

49

.

29.

Amit

O

,

On

YB

,

Perez

G

,

Shargian-Alon

L

,

Yeshurun

M

,

Ram

R.

Venetoclax and donor lymphocyte infusion for early relapsed acute myeloid leukemia after allogeneic hematopoietic cell transplantation. A retrospective multicenter trial

.

Ann Hematol

.

2021

;

100

(

3

):

817

-

824

.

30.

Schuler

E

,

Wagner-Drouet

E-M

,

Ajib

S

, et al;

German Cooperative Transplant Study Group

.

Treatment of myeloid malignancies relapsing after allogeneic hematopoietic stem cell transplantation with venetoclax and hypomethylating agents-a retrospective multicenter analysis on behalf of the German Cooperative Transplant Study Group

.

Ann Hematol

.

2021

;

100

(

4

):

959

-

968

.

31.

Aldoss

I

,

Yang

D

,

Aribi

A

, et al.

Efficacy of the combination of venetoclax and hypomethylating agents in relapsed/refractory acute myeloid leukemia

.

Haematologica

.

2018

;

103

(

9

):

e404

-

e407

.

32.

DiNardo

CD

,

Jonas

BA

,

Pullarkat

V

, et al.

Azacitidine and venetoclax in previously untreated acute myeloid leukemia

.

N Engl J Med

.

2020

;

383

(

7

):

617

-

629

.

33.

Zucenka

A

,

Vaitekenaite

V

,

Maneikis

K

, et al.

Venetoclax-based salvage therapy followed by Venetoclax and DLI maintenance vs. FLAG-Ida for relapsed or refractory acute myeloid leukemia after allogeneic stem cell transplantation

.

Bone Marrow Transplant

.

2021

;

56

(

11

):

2804

-

2812

.

34.

Zuanelli Brambilla

C

,

Lobaugh

SM

,

Ruiz

JD

, et al.

Relapse after allogeneic stem cell transplantation of acute myelogenous leukemia and myelodysplastic syndrome and the importance of second cellular therapy

.

Transplant Cell Ther

.

2021

;

27

(

9

):

771.e1

-

771.e10

.

35.

Zhao

P

,

Ni

M

,

Ma

D

, et al.

Venetoclax plus azacitidine and donor lymphocyte infusion in treating acute myeloid leukemia patients who relapse after allogeneic hematopoietic stem cell transplantation

.

Ann Hematol

.

2022

;

101

(

1

):

119

-

130

.

36.

Schmidt

S

,

Liu

Y

,

Hu

Z-H

, et al.

The role of donor lymphocyte infusion (DLI) in post-hematopoietic cell transplant (HCT) relapse for chronic myeloid leukemia (CML) in the tyrosine kinase inhibitor (TKI) Era

.

Biol Blood Marrow Transplant

.

2020

;

26

(

6

):

1137

-

1143

.

37.

DiNardo

CD

,

Stein

EM

,

de Botton

S

, et al.

Durable remissions with ivosidenib in IDH1-mutated relapsed or refractory AML

.

N Engl J Med

.

2018

;

378

(

25

):

2386

-

2398

.

38.

Stein

EM

,

DiNardo

CD

,

Pollyea

DA

, et al.

Enasidenib in mutant IDH2 relapsed or refractory acute myeloid leukemia

.

Blood

.

2017

;

130

(

6

):

722

-

731

.

39.

Mathew

NR

,

Baumgartner

F

,

Braun

L

, et al.

Erratum: sorafenib promotes graft-versus-leukemia activity in mice and humans through IL-15 production in FLT3-ITD-mutant leukemia cells

.

Nat Med

.

2018

;

24

(

4

):

526

.

40.

Zhang

Z

,

Hasegawa

Y

,

Hashimoto

D

, et al.

Gilteritinib enhances graft-versus-leukemia effects against FLT3-ITD mutant leukemia after allogeneic hematopoietic stem cell transplantation

.

Bone Marrow Transplant

.

2022

;

57

(

5

):

775

-

780

.

41.

Xuan

L

,

Wang

Y

,

Chen

J

, et al.

Sorafenib therapy is associated with improved outcomes for FMS-like tyrosine kinase 3 internal tandem duplication acute myeloid leukemia relapsing after allogeneic hematopoietic stem cell transplantation

.

Biol Blood Marrow Transplant

.

2019

;

25

(

8

):

1674

-

1681

.

42.

De Freitas

T

,

Marktel

S

,

Piemontese

S

, et al.

High rate of hematological responses to sorafenib in FLT3-ITD acute myeloid leukemia relapsed after allogeneic hematopoietic stem cell transplantation

.

Eur J Haematol

.

2016

;

96

(

6

):

629

-

636

.

43.

Issa

GC

,

Aldoss

I

,

Thirman

MJ

, et al.

Menin inhibition with revumenib for KMT2A-rearranged relapsed or refractory acute leukemia (AUGMENT-101)

.

J Clin Oncol

.

2024

:

JCO2400826

.

44.

Issa

GC

,

Aldoss

I

,

DiPersio

J

, et al.

The menin inhibitor revumenib in KMT2A-rearranged or NPM1-mutant leukaemia

.

Nature

.

2023

;

615

(

7954

):

920

-

924

.

45.

Collins

RH

Jr,

Shpilberg

O

,

Drobyski

WR

, et al.

Donor leukocyte infusions in 140 patients with relapsed malignancy after allogeneic bone marrow transplantation

.

J Clin Oncol

.

1997

;

15

(

2

):

433

-

444

.

46.

Biederstädt

A

,

Rezvani

K.

How I treat high-risk acute myeloid leukemia using preemptive adoptive cellular immunotherapy

.

Blood

.

2023

;

141

(

1

):

22

-

38

.

47.

Kharfan-Dabaja

MA

,

Labopin

M

,

Polge

E

, et al.

Association of second allogeneic hematopoietic cell transplant vs donor lymphocyte infusion with overall survival in patients with acute myeloid leukemia relapse

.

JAMA Oncol

.

2018

;

4

(

9

):

1245

-

1253

.

48.

Alkhaldi

H

,

Kharfan-Dabaja

M

,

El Fakih

R

,

Aljurf

M.

Safety and efficacy of immune checkpoint inhibitors after allogeneic hematopoietic cell transplantation

.

Bone Marrow Transplant

.

2023

;

58

(

10

):

1075

-

1083

.

49.

Sockel

K

,

Bornhaeuser

M

,

Mischak-Weissinger

E

, et al;

German MDS and Cooperative Transplant Study Group (GCTSG)

.

Lenalidomide maintenance after allogeneic HSCT seems to trigger acute graft-versus-host disease in patients with high-risk myelodysplastic syndromes or acute myeloid leukemia and del(5q): results of the LENAMAINT trial

.

Haematologica

.

2012

;

97

(

9

):

e34

-

e35

.

50.

Craddock

C

,

Slade

D

,

De Santo

C

, et al.

Combination lenalidomide and azacitidine: a novel salvage therapy in patients who relapse after allogeneic stem-cell transplantation for acute myeloid leukemia

.

J Clin Oncol

.

2019

;

37

(

7

):

580

-

588

.

51.

Schroeder

T

,

Stelljes

M

,

Christopeit

M

, et al.

Azacitidine, lenalidomide and donor lymphocyte infusions for relapse of myelodysplastic syndrome, acute myeloid leukemia and chronic myelomonocytic leukemia after allogeneic transplant: the Azalena-trial

.

Haematologica

.

2023

;

108

(

11

):

3001

-

3010

.

52.

Posthuma

EF

,

Marijt

EW

,

Barge

RM

, et al.

Alpha-interferon with very-low-dose donor lymphocyte infusion for hematologic or cytogenetic relapse of chronic myeloid leukemia induces rapid and durable complete remissions and is associated with acceptable graft-versus-host disease

.

Biol Blood Marrow Transplant

.

2004

;

10

(

3

):

204

-

212

.

53.

Henden

AS

,

Varelias

A

,

Leach

J

, et al.

Pegylated interferon-2α invokes graft-versus-leukemia effects in patients relapsing after allogeneic stem cell transplantation

.

Blood Adv

.

2019

;

3

(

20

):

3013

-

3019

.

54.

Christopher

MJ

,

Petti

AA

,

Rettig

MP

, et al.

Immune escape of relapsed AML cells after allogeneic transplantation

.

N Engl J Med

.

2018

;

379

(

24

):

2330

-

2341

.

55.

Toffalori

C

,

Zito

L

,

Gambacorta

V

, et al.

Immune signature drives leukemia escape and relapse after hematopoietic cell transplantation

.

Nat Med

.

2019

;

25

(

4

):

603

-

611

.

56.

Matte-Martone

C

,

Liu

J

,

Zhou

M

, et al.

Differential requirements for myeloid leukemia IFN-γ conditioning determine graft-versus-leukemia resistance and sensitivity

.

J Clin Invest

.

2017

;

127

(

7

):

2765

-

2776

.

57.

Kharfan-Dabaja

MA

,

Reljic

T

,

Yassine

F

, et al.

Efficacy of a second allogeneic hematopoietic cell transplant in relapsed acute myeloid leukemia: results of a systematic review and meta-analysis

.

Transplant Cell Ther

.

2022

;

28

(

11

):

767.e1

-

767767.e11

.

58.

Ruutu

T

,

de Wreede

LC

,

van Biezen

A

, et al;

European Society for Blood and Marrow Transplantation (EBMT)

.

Second allogeneic transplantation for relapse of malignant disease: retrospective analysis of outcome and predictive factors by the EBMT

.

Bone Marrow Transplant

.

2015

;

50

(

12

):

1542

-

1550

.

59.

Yerushalmi

Y

,

Shem-Tov

N

,

Danylesko

I

, et al.

Second hematopoietic stem cell transplantation as salvage therapy for relapsed acute myeloid leukemia/myelodysplastic syndromes after a first transplantation

.

Haematologica

.

2023

;

108

(

7

):

1782

-

1792

.

60.

Bazarbachi

A

,

Schmid

C

,

Labopin

M

, et al.

Evaluation of trends and prognosis over time in patients with AML relapsing after allogeneic hematopoietic cell transplant reveals improved survival for young patients in recent years

.

Clin Cancer Res

.

2020

;

26

(

24

):

6475

-

6482

.

61.

Christopeit

M

,

Kuss

O

,

Finke

J

, et al.

Second allograft for hematologic relapse of acute leukemia after first allogeneic stem-cell transplantation from related and unrelated donors: the role of donor change

.

J Clin Oncol

.

2013

;

31

(

26

):

3259

-

3271

.

62.

Imus

PH

,

Blackford

AL

,

Bettinotti

M

, et al.

Major histocompatibility mismatch and donor choice for second allogeneic bone marrow transplantation

.

Biol Blood Marrow Transplant

.

2017

;

23

(

11

):

1887

-

1894

.

63.

Shimoni

A

,

Labopin

M

,

Finke

J

, et al.

Donor selection for a second allogeneic stem cell transplantation in AML patients relapsing after a first transplant: a study of the Acute Leukemia Working Party of EBMT

.

Blood Cancer J

.

2019

;

9

(

12

):

88

.

64.

Aldoss

I

,

Khaled

SK

,

Wang

Y

, et al.

Donor-derived CD19-targeted chimeric antigen receptor T cells in adult transplant recipients with relapsed/refractory acute lymphoblastic leukemia

.

Blood Cancer J

.

2023

;

13

(

1

):

107

.

65.

Brudno

JN

,

Somerville

RP

,

Shi

V

, et al.

Allogeneic T cells that express an anti-CD19 chimeric antigen receptor induce remissions of B-cell malignancies that progress after allogeneic hematopoietic stem-cell transplantation without causing graft-versus-host disease

.

J Clin Oncol

.

2016

;

34

(

10

):

1112

-

1121

.

66.

Chapuis

AG

,

Egan

DN

,

Bar

M

, et al.

T cell receptor gene therapy targeting WT1 prevents acute myeloid leukemia relapse posttransplant

.

Nat Med

.

2019

;

25

(

7

):

1064

-

1072

.

67.

Lulla

PD

,

Naik

S

,

Vasileiou

S

, et al.

Clinical effects of administering leukemia- specific donor T cells to patients with AML/MDS after allogeneic transplant

.

Blood

.

2021

;

137

(

19

):

2585

-

2597

.

68.

Krakow

EF

,

Brault

M

,

Summers

C

, et al.

HA-1-targeted T cell receptor (TCR) T cell therapy for recurrent leukemia after hematopoietic stem cell transplantation

.

Blood

.

2024

:blood.2024024105.

69.

Guan

F

,

Yang

L

,

Chen

Y

, et al.

Comparison of long-term outcomes between imatinib and dasatinib prophylaxis after allogeneic stem cell transplantation in patients with Philadelphia-positive acute lymphoblastic leukemia: a multicenter retrospective study

.

Cancer

.

2024

;

130

(

12

):

2139

-

2149

.

70.

Cheng

Q

,

Tang

Y

,

Liu

F

,

Li

X

,

Fang

D.

Efficacy and safety in early application of Ruxolinitib for high-risk: acute lymphoblastic leukemia to prevent GVHD and recurrence after allogeneic hematopoietic stem cell transplantation

.

Transpl Immunol

.

2024

;

83

:

101978

.

71.

Fan

J

,

Lu

R

,

Zhu

J

, et al.

Effects of posttransplant maintenance therapy with decitabine prophylaxis on the relapse for acute lymphoblastic leukemia

.

Bone Marrow Transplant

.

2023

;

58

(

6

):

687

-

695

.