Efficacy and safety of human umbilical cord-derived mesenchymal stem cells versus placebo added to second-line therapy in patients with steroid-refractory acute graft-versus-host disease: a multicentre, randomized, double-blind, phase 2 trial

Abstract Background Failure of systemic corticosteroid therapy is common in patients with newly diagnosed acute graft-versus-host disease (aGVHD) above grade II. Mesenchymal stem cells (MSCs) have been used as a tolerable and potentially effective second-line therapy for steroid-refractory aGVHD (SR...

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Main Authors: Erlie Jiang, Kun Qian, Lu Wang, Donglin Yang, Yangliu Shao, Liangding Hu, Yuhang Li, Chen Yao, Mingzhe Han, Xiaoqiang Hou, Daihong Liu
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Language:English
Published: BMC 2024-11-01
Series:BMC Medicine
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Online Access:https://doi.org/10.1186/s12916-024-03782-5
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author Erlie Jiang
Kun Qian
Lu Wang
Donglin Yang
Yangliu Shao
Liangding Hu
Yuhang Li
Chen Yao
Mingzhe Han
Xiaoqiang Hou
Daihong Liu
author_facet Erlie Jiang
Kun Qian
Lu Wang
Donglin Yang
Yangliu Shao
Liangding Hu
Yuhang Li
Chen Yao
Mingzhe Han
Xiaoqiang Hou
Daihong Liu
author_sort Erlie Jiang
collection DOAJ
description Abstract Background Failure of systemic corticosteroid therapy is common in patients with newly diagnosed acute graft-versus-host disease (aGVHD) above grade II. Mesenchymal stem cells (MSCs) have been used as a tolerable and potentially effective second-line therapy for steroid-refractory aGVHD (SR-aGVHD); however, well-designed, prospective, controlled studies are lacking. Methods This multicentre, randomized, double-blind, placebo-controlled, exploratory phase 2 study enrolled patients with SR-aGVHD above grade II from 7 centres. Patients were randomized 1:1 to receive umbilical cord-derived MSCs or placebo added to one centre’s choice of second-line agents (except for ruxolitinib). The agents were infused twice weekly. Patients with complete response (CR), no response (NR), or progression of disease (PD) at d28 received 8 infusions, and those with partial response (PR) received the above infusions for another 4 weeks. The per-protocol population consisted of patients who received ≥ 8 infusions. The primary endpoint was the overall response rate (ORR, CR + PR) at d28, analyzed in the per-protocol and intention-to-treat populations. Results Seventy-eight patients (median age 38, range 13–62) were enrolled: 40 in the MSC group and 38 in the control. Patients in the MSC group received a median of 8 doses, with a median response time of 14 days. In intention-to-treat analysis, ORR at d28 was 60% for MSC group and 50% for control group (p = 0.375). The 2-year cumulative incidence of moderate to severe cGVHD was marginally lower in the MSC group than in the control (13.8% vs. 39.8%, p = 0.067). The 2-year failure-free survival was similar between the MSC and control groups (52.5% vs. 44.4%, p = 0.43). In per-protocol analysis (n = 62), ORR at d28 was significantly greater in the MSC group than in the control group (71.9% vs. 46.7%, p = 0.043). Among patients with gut involvement, ORR at d28 was significantly greater in the MSC group than in the control (66.7% vs. 33.3%, p = 0.031). The adverse events incidences were similar between groups. Conclusions In this exploratory study, there was no superior ORR at d28 demonstrated in the MSC group compared with the control. However, MSCs showed a gradual treatment effect at a median of 2 weeks. Patients who completed 8 infusions may benefit from adding MSCs to one conventional second-line agent, especially those with gut involvement. MSCs was well tolerated in patients with SR-aGVHD. Trial registration chictr.org.cn ChiCTR2000035740.
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spelling doaj-art-678df06a24064f778961d2d6cf38b56f2025-08-20T02:08:19ZengBMCBMC Medicine1741-70152024-11-0122111410.1186/s12916-024-03782-5Efficacy and safety of human umbilical cord-derived mesenchymal stem cells versus placebo added to second-line therapy in patients with steroid-refractory acute graft-versus-host disease: a multicentre, randomized, double-blind, phase 2 trialErlie Jiang0Kun Qian1Lu Wang2Donglin Yang3Yangliu Shao4Liangding Hu5Yuhang Li6Chen Yao7Mingzhe Han8Xiaoqiang Hou9Daihong Liu10School of Medicine, Nankai University, Nankai DistrictSchool of Medicine, Nankai University, Nankai DistrictDepartment of Hematology, theFifth Medical Center of ChineseFengtai District, PLA General HospitalState Key Laboratory of Experimental Hematology, Institute of Hematology & Blood Diseases Hospital, National Clinical Research Center for Blood Diseases, Haihe Laboratory of Cell Ecosystem, Chinese Academy of Medical Sciences & Peking Union Medical CollegeDepartment of Hematology, theFifth Medical Center of ChineseFengtai District, PLA General HospitalDepartment of Hematology, theFifth Medical Center of ChineseFengtai District, PLA General HospitalDepartment of Hematology, theFifth Medical Center of ChineseFengtai District, PLA General HospitalPeking University Clinical Research Institute, Peking University First HospitalState Key Laboratory of Experimental Hematology, Institute of Hematology & Blood Diseases Hospital, National Clinical Research Center for Blood Diseases, Haihe Laboratory of Cell Ecosystem, Chinese Academy of Medical Sciences & Peking Union Medical CollegePlatinumlife Biotechnology (Beijing) Co., Ltd, Beijing Economic-Technological Development AreaSchool of Medicine, Nankai University, Nankai DistrictAbstract Background Failure of systemic corticosteroid therapy is common in patients with newly diagnosed acute graft-versus-host disease (aGVHD) above grade II. Mesenchymal stem cells (MSCs) have been used as a tolerable and potentially effective second-line therapy for steroid-refractory aGVHD (SR-aGVHD); however, well-designed, prospective, controlled studies are lacking. Methods This multicentre, randomized, double-blind, placebo-controlled, exploratory phase 2 study enrolled patients with SR-aGVHD above grade II from 7 centres. Patients were randomized 1:1 to receive umbilical cord-derived MSCs or placebo added to one centre’s choice of second-line agents (except for ruxolitinib). The agents were infused twice weekly. Patients with complete response (CR), no response (NR), or progression of disease (PD) at d28 received 8 infusions, and those with partial response (PR) received the above infusions for another 4 weeks. The per-protocol population consisted of patients who received ≥ 8 infusions. The primary endpoint was the overall response rate (ORR, CR + PR) at d28, analyzed in the per-protocol and intention-to-treat populations. Results Seventy-eight patients (median age 38, range 13–62) were enrolled: 40 in the MSC group and 38 in the control. Patients in the MSC group received a median of 8 doses, with a median response time of 14 days. In intention-to-treat analysis, ORR at d28 was 60% for MSC group and 50% for control group (p = 0.375). The 2-year cumulative incidence of moderate to severe cGVHD was marginally lower in the MSC group than in the control (13.8% vs. 39.8%, p = 0.067). The 2-year failure-free survival was similar between the MSC and control groups (52.5% vs. 44.4%, p = 0.43). In per-protocol analysis (n = 62), ORR at d28 was significantly greater in the MSC group than in the control group (71.9% vs. 46.7%, p = 0.043). Among patients with gut involvement, ORR at d28 was significantly greater in the MSC group than in the control (66.7% vs. 33.3%, p = 0.031). The adverse events incidences were similar between groups. Conclusions In this exploratory study, there was no superior ORR at d28 demonstrated in the MSC group compared with the control. However, MSCs showed a gradual treatment effect at a median of 2 weeks. Patients who completed 8 infusions may benefit from adding MSCs to one conventional second-line agent, especially those with gut involvement. MSCs was well tolerated in patients with SR-aGVHD. Trial registration chictr.org.cn ChiCTR2000035740.https://doi.org/10.1186/s12916-024-03782-5Mesenchymal stem cellsHaematopoietic stem cell transplantationAcute graft-versus-host diseaseSteroid-refractory
spellingShingle Erlie Jiang
Kun Qian
Lu Wang
Donglin Yang
Yangliu Shao
Liangding Hu
Yuhang Li
Chen Yao
Mingzhe Han
Xiaoqiang Hou
Daihong Liu
Efficacy and safety of human umbilical cord-derived mesenchymal stem cells versus placebo added to second-line therapy in patients with steroid-refractory acute graft-versus-host disease: a multicentre, randomized, double-blind, phase 2 trial
BMC Medicine
Mesenchymal stem cells
Haematopoietic stem cell transplantation
Acute graft-versus-host disease
Steroid-refractory
title Efficacy and safety of human umbilical cord-derived mesenchymal stem cells versus placebo added to second-line therapy in patients with steroid-refractory acute graft-versus-host disease: a multicentre, randomized, double-blind, phase 2 trial
title_full Efficacy and safety of human umbilical cord-derived mesenchymal stem cells versus placebo added to second-line therapy in patients with steroid-refractory acute graft-versus-host disease: a multicentre, randomized, double-blind, phase 2 trial
title_fullStr Efficacy and safety of human umbilical cord-derived mesenchymal stem cells versus placebo added to second-line therapy in patients with steroid-refractory acute graft-versus-host disease: a multicentre, randomized, double-blind, phase 2 trial
title_full_unstemmed Efficacy and safety of human umbilical cord-derived mesenchymal stem cells versus placebo added to second-line therapy in patients with steroid-refractory acute graft-versus-host disease: a multicentre, randomized, double-blind, phase 2 trial
title_short Efficacy and safety of human umbilical cord-derived mesenchymal stem cells versus placebo added to second-line therapy in patients with steroid-refractory acute graft-versus-host disease: a multicentre, randomized, double-blind, phase 2 trial
title_sort efficacy and safety of human umbilical cord derived mesenchymal stem cells versus placebo added to second line therapy in patients with steroid refractory acute graft versus host disease a multicentre randomized double blind phase 2 trial
topic Mesenchymal stem cells
Haematopoietic stem cell transplantation
Acute graft-versus-host disease
Steroid-refractory
url https://doi.org/10.1186/s12916-024-03782-5
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