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Frontiers of Medicine

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Front. Med.    2019, Vol. 13 Issue (2) : 238-249    https://doi.org/10.1007/s11684-017-0599-3
RESEARCH ARTICLE
Interferon-α salvage treatment is effective for patients with acute leukemia/myelodysplastic syndrome with unsatisfactory response to minimal residual disease-directed donor lymphocyte infusion after allogeneic hematopoietic stem cell transplantation
Xiaodong Mo1, Xiaohui Zhang1, Lanping Xu1, Yu Wang1, Chenhua Yan1, Huan Chen1, Yuhong Chen1, Wei Han1, Fengrong Wang1, Jingzhi Wang1, Kaiyan Liu1, Xiaojun Huang1,2()
1. Peking University People’s Hospital, Peking University Institute of Hematology, Beijing Key Laboratory of Hematopoietic Stem Cell Transplantation, Beijing 100044, China
2. Peking-Tsinghua Center for Life Sciences, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing 100044, China
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Abstract

The efficacy of salvage interferon-α (IFN-α) treatment was investigated in patients with unsatisfactory response to minimal residual disease (MRD)-directed donor lymphocyte infusion (DLI) (n=24). Patients who did not become MRD-negative at 1 month after DLI were those with unsatisfactory response and were eligible to receive salvage IFN-α treatment within 3 months of DLI. Recombinant human IFN-α-2b injections were subcutaneously administered 2–3 times a week for 6 months. Nine (37.5%), 6 (25.0%), and 3 (12.5%) patients became MRD-negative at 1, 2, and>2 months after the salvage IFN-α treatment, respectively. Two-year cumulative incidences of relapse and non-relapse mortality were 35.9% and 8.3%, respectively. Two-year probabilities of event-free survival, disease-free survival, and overall survival were 51.6%, 54.3%, and 68.0%, respectively. Outcomes of patients subjected to salvage IFN-α treatment after DLI were significantly better than those with persistent MRD without IFN-α treatment. Moreover, clinical outcomes were comparable between the salvage DLI and IFN-α treatment groups. Thus, salvage IFN-α treatment may help improve the outcome of patients with unsatisfactory responses to MRD-directed DLI and could be a potential salvage treatment for these patients after allogeneic hematopoietic stem cell transplantation.
Keywords interferon-α      hematopoietic stem cell transplantation      minimal residual disease      donor lymphocyte infusion     
Corresponding Author(s): Xiaojun Huang   
Just Accepted Date: 12 February 2018   Online First Date: 16 April 2018    Issue Date: 28 March 2019
 Cite this article:   
Xiaodong Mo,Xiaohui Zhang,Lanping Xu, et al. Interferon-α salvage treatment is effective for patients with acute leukemia/myelodysplastic syndrome with unsatisfactory response to minimal residual disease-directed donor lymphocyte infusion after allogeneic hematopoietic stem cell transplantation[J]. Front. Med., 2019, 13(2): 238-249.
 URL:  
https://academic.hep.com.cn/fmd/EN/10.1007/s11684-017-0599-3
https://academic.hep.com.cn/fmd/EN/Y2019/V13/I2/238
Fig.1  Patients enrolled in this study. Patients who were minimal residual disease (MRD) (+) at 1 month after MRD-directed DLI were eligible to receive salvage interventions within 3 months of donor lymphocyte infusion (DLI), with consent, if they had no active graft-versus-host disease (GVHD) or active infection. Salvage interventions included treatment with IFN-α and DLI, and this intervention was primarily based on the physicians’ and patients’ intentions.
Fig.2  Cumulative incidence of relapse at 2 years based on the (A) underlying disease (42.5% vs. 31.3%, P=0.969) and (B) MRD status after salvage treatment with IFN-α (20.5% vs. 51.3%, P=0.131).
Characteristics MRD (–) group (n=26) MRD (+) IFN-α (+) group (n =24) MRD (+) IFN-α (–) group (n=17) P value
Median age at allo-HSCT, years (range) 28 (8–58) 23 (3–48) 28 (2–50) 0.478
Median time from allo-HSCT to DLI, days (range) 177 (79–821) 242 (63–1239) 214 (73–1552) 0.444
Underlying disease, n (%)
?Acute myeloid leukemia 13 (50.0) 15 (62.5) 11 (64.8) 0.338
?Acute lymphoblastic leukemia 7 (26.9) 8 (33.3) 3 (17.6)
?Myelodysplastic syndrome 6 (23.1) 1 (4.2) 3 (17.6)
Disease risk at diagnosis, n (%)
?Low risk 2 (7.7) 3 (12.5) 1 (5.9) 0.484
?Intermediate risk 18 (69.2) 19 (79.2) 15 (88.2)
?High risk 6 (23.1) 2 (8.3) 1 (5.9)
Sex, n (%)
?Male 14 (53.8) 14 (58.3) 11 (64.7) 0.779
?Female 12 (46.2) 10 (41.7) 16 (35.3)
Donor–recipient sex match, n (%)
?Female–male 6 (23.1) 7 (29.2) 2 (11.8) 0.430
?Others 20 (76.9) 17 (70.8) 15 (88.2)
ABO matched, n (%)
?Matched 15 (57.7) 12 (50.0) 10 (58.8) 0.811
?Mismatched 11 (42.3) 12 (50.0) 7 (41.2)
Donor–recipient relationship, n (%)
?Father–child 9 (34.6) 9 (37.5) 7 (41.2) 0.675
?Mother–child 1 (3.8) 3 (12.5) 0 (0.0)
?Sibling–sibling 13 (50.0) 11 (45.8) 9 (52.9)
?Other related donor 3 (11.6) 0 (0.0) 0 (0.0)
?Unrelated donor 0 (0.0) 1 (4.2) 1 (5.9)
Donor type, n (%)
?HLA-identical sibling donor 8 (30.8) 6 (25.0) 6 (35.3) 0.734
?HLA-haploidentical related donor 18 (69.2) 17 (70.8) 10 (58.8)
?HLA-unrelated donor 0 (0.0) 1 (4.2) 1 (5.9)
Number of HLA-A, HLA-B, HLA-DR mismatches, n (%)
?0 8 (30.8) 7 (29.2) 6 (35.3) 0.878
?1 2 (7.7) 0 (0.0) 1 (5.8)
?2 2 (7.7) 2 (8.3) 2 (11.8)
?3 14 (53.8) 15 (62.5) 8 (47.1)
MRD prior to preemptive DLI, n (%)
?Genetic markerpositive twice 15 (57.7) 11 (45.8) 5 (29.4) 0.175
?LAIPs positive twice 2 (7.7) 0 (0.0) 1 (5.9)
?Genetic marker and LAIPs positive simultaneous 9 (34.6) 13 (54.2) 11 (64.7)
High-level MRD prior to DLI, n (%) a 21 (80.8) 17 (70.8) 15 (88.2) 0.411
Late onset MRD, n (%) b 18 (69.2) 16 (66.7) 13 (76.5) 0.789
Discontinuing immunosuppressions before DLI, n (%) 16 (61.5) 13 (54.2) 6 (35.3) 0.235
GVHD prophylaxis, n (%)
?Cyclosporine A 26 (100.0) 23 (95.8) 16 (94.1) 0.518
?Methotrexate 0 (0.0) 1 (4.2) 1 (5.9)
Subtypes of cells for DLI
?Median mononuclear cells, ×108/kg (range) 1.0
(1.0–2.3)		 1.0
(0.8–1.8)		 1.0
(0.8–2.0)		 0.558
?Median CD3+ counts, ×107/kg (range) 3.6
(0.7–7.5)		 3.3
(0.2–7.7)		 3.5
(0.5–7.4)		 0.565
?Median CD34+ counts, ×106/kg (range) 0.3
(0.1–0.6)		 0.4
(0.1–1.2)		 0.5
(0.1–1.5)		 0.064
Acute GVHD after DLI, n (%) 8 (30.8) 4 (16.6) 5 (29.4) 0.459
?Grade I to II 5 (19.2) 2 (8.3) 3 (17.6) 0.570
?Grade III to IV 3 (11.6) 2 (8.3) 2 (11.8) 1.000
Chronic GVHD after DLI, n (%) 19 (73.1) 9 (37.5) 7 (41.2) 0.024
?Mild to moderate 7 (26.9) 5 (20.8) 5 (29.4) 0.824
?Severe 12 (46.2) 4 (16.7) 2 (11.8) 0.021
Median follow-up after DLI, d (range) 532 (90–1231) 557 (62–1336) 190 (16–867) 0.017
Tab.1  Patient characteristics
Fig.3  Clinical outcomes of patients with and without exposure to salvage IFN-α treatment at 2 years after MRD-directed DLI. (A) Relapse: MRD (+) IFN (+) group vs. MRD (+) IFN (–) group: 35.9% vs. 64.7%, P=0.007; MRD (+) IFN (+) group vs. MRD (–) group: 35.9% vs. 3.8%, P=0.011; MRD (+) IFN (–) group vs. MRD (–) group: 64.7% vs. 3.8%, P<0.001. (B) NRM: MRD (+) IFN (+) group vs. MRD (+) IFN (–) group: 8.3% vs. 5.9%, P=0.888; MRD (+) IFN (+) group vs. MRD (–) group: 8.3% vs. 21.3%, P=0.233; MRD (+) IFN(–) group vs. MRD (–) group: 5.9% vs. 21.3%, P=0.298. (C) DFS: MRD (+) IFN (+) group vs. MRD (+) IFN (–) group: 54.3% vs. 29.4%, P=0.004; MRD (+) IFN (+) group vs. MRD (–) group: 54.3% vs. 74.9%, P=0.206; MRD (+) IFN (–) group vs. MRD (–) group: 29.4% vs. 74.9%, P<0.001. (D) OS: MRD (+) IFN (+) group vs. MRD (+) IFN (–) group: 68.0% vs. 41.7%, P=0.076; MRD (+) IFN (+) group vs. MRD (–) group: 68.0% vs. 78.8%, P=0.441; MRD (+) IFN (–) group vs. MRD (–) group: 41.7% vs. 78.8%, P=0.015.
HR 95% CI P
Relapse
?MRD (+) after DLI, without IFN-α 1.00
?MRD (+) after DLI, received IFN-α 0.28 0.11–0.70 0.007
?MRD (−) after DLI 0.03 0.01–0.25 0.001
Treatment failure as defined by DFS
?MRD (+) after DLI, without IFN-α 1.00
?MRD (+) after DLI, received IFN-α 0.30 0.13–0.71 0.006
?MRD (−) after DLI 0.14 0.05–0.39 <0.001
Treatment failure as defined by OS
?MRD (+) after DLI, without IFN-α 1.00
?MRD (+) after DLI, received IFN-α 0.41 0.15–1.13 0.085
?MRD (−) after DLI 0.26 0.09–0.81 0.020
Tab.2  Multivariate analyses for 2-year clinical outcomes after DLI
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