Comparison of outcomes in hematological malignancies treated with haploidentical or HLA-identical sibling hematopoietic stem cell transplantation following myeloablative conditioning: A meta-analysis
Comparison of outcomes in hematological malignancies treated with haploidentical or HLA-identical sibling hematopoietic stem cell transplantation following myeloablative conditioning: A meta-analysis
Dangui Chen 0 1
Di Zhou 1
Dan Guo 0 1
Peipei Xu 1
Bing Chen 0 1
0 Department of Hematology, Nanjing Drum Tower Hospital Clinical College of Nanjing Medical University , Nanjing , People's Republic of China, 2 Department of Hematology, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School , Gulou district, Nanjing , People's Republic of China
1 Editor: Senthilnathan Palaniyandi, University of Kentucky , UNITED STATES
Haploidentical and human leukocyte antigen (HLA)-identical sibling hematopoietic stem transplantation are two main ways used in allogeneic hematopoietic stem cell transplantation (allo-HSCT). In recent years, remarkable progress has been made in haploidentical allo-HSCT (HID-SCT), and some institutions found HID-SCT had similar outcomes as HLAidentical sibling allo-HSCT (ISD-SCT). To clarify if HID-SCT has equal effects to ISD-SCT in hematologic malignancies, we performed this meta-analysis. Relevant articles published prior to February 2017 were searched on PubMed. Two reviewers assessed the quality of the included studies and extracted data independently. Odds ratio (OR) and 95% confidence intervals (CIs) were calculated for statistical analysis.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
Funding: This work is supported by Peak of Six
Talent in Jiangsu Province (2015-WSN-075).
Competing interests: The authors have declared
that no competing interests exist.
Seven studies including 1919 patients were included. The rate of platelet engraftment is
significantly lower after HID-SCT versus ISD-SCT while there is no difference in neutrophil
engraftment (OR = 2.58, 95% CI = 1.70±3.93, P < 0.00001). The risk of acute
graft-versushost disease (GVHD) is significantly higher after HID-SCT versus ISD-SCT (OR = 1.88,
95% CI = 1.42±2.49, P < 0.00001), but the relapse rate is lower in HID-SCT group (OR =
0.70, 95% CI = 0.55±0.90, P = 0.005). The incidence rates of overall survival (OS) and
disease-free-survival/leukemia-free survival/relapse-free survival (DFS/LFS/RFS) after
ISDSCT are all significantly superior to HID-SCT (OR = 1.32, 95% CI = 1.08±1.62, P = 0.006;
OR = 1.25, 95% CI = 1.03±1.52, P = 0.02). There is no significant difference in
transplantation related mortality (TRM) rate after HID-SCT and ISD-SCT.
After myeloablative conditioning, patients receiving ISD-SCT have a faster engraftment,
lower acute GVHD and longer life expectancy compared to HID-SCT with GVHD
prophylaxis (cyclosporine A, methotrexate, mycophenolate mofetil and antithymoglobulin; CsA +
MTX + MMF + ATG). Currently, HID-SCT with GVHD prophylaxis (CsA + MTX + MMF +
ATG) may not replace ISD-SCT when HLA-identical sibling donor available.
Allogeneic hematopoietic stem cell transplantation (allo-HSCT) with human leukocyte antigen
(HLA)-identical sibling or unrelated donor is the main way for treatment for high-risk
hematological malignancies. For patients without a suitable donor, especially those in urgent need
of transplantation, haploidentical allo-HSCT (HID-SCT) is an option [
]. HID-SCT was
unsuccessful for many years because of graft rejection and high incidence of acute
graft-versus-host disease (GVHD), but the progress in GVHD prophylaxis and conditioning regimen
has made HID-SCT possible [
]. A multicenter phase-2 study from the Chinese Bone
Marrow Transplant Cooperative Group (CBMTCG) showed that the combination of cyclosporine
A, methotrexate, mycophenolate mofetil (CsA + MTX + MMF) for GVHD prophylaxis signifi
cantly decreased the incidence of acute GVHD without an increase in relapse or any adverse
impact on survival in standard-risk patients compared with historical controls in ISD-SCT [
Similarly, ATG deletes T lymphocytes chronically in vivo, and prevents GVHD without
increasing the risks of relapse [
]. Some institutions demonstrated HID-SCT using
conditioning regimen including ATG yielded similar outcomes to ISD-SCT for hematological
]. Some studies also indicated similar outcomes after HID-SCT compared to
HLA-identical allo-HSCT [
]. At present, HID-SCT has been accepted by many
transplantation centers. Over the past decades, much progress has been made to improve the outcomes
of transplantation, including in the conditioning regimen; prophylaxis; lower cumulative
incidence rates of GVHD, transplantation-related mortality/ no-relapse mortality (TRM/NRM)
and relapse; higher rates of OS and DFS/LFS/PFS. However, there haven't been well-controlled
studies to compare the efficacy of HID-SCT and ISD-SCT. Therefore, our meta-analysis aims
to investigate whether HID-SCT has similar outcomes compared with ISD-SCT.
Identification and study selection
Two reviews independently identified relevant studies by searching PubMed. Search terms
included ªhaploidentical stem cell transplantationº, ªhaploidenticalº and ªidenticalº. All
studies published prior to February 2017 were eligible. The title and abstracts of all potentially
relevant publications were reviewed. Studies that met the inclusion criteria were selected for the
analysis. The reference lists from the selected articles were then hand-searched to identify
further relevant trials.
Inclusion and exclusion criteria
This meta-analysis included hematologic malignancies who received HSCT (HID-SCT or
ISD-SCT). T cell replete HID-SCT for hematologic malignancies using GVHD prophylaxis (CsA + MMF + MTX + ATG) was included. Studies with data concerning grades 3±4 acute
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GVHD were included if no suitable data of grades 2±4 acute GVHD were available. The inclu
sion criteria were as follows: randomized/nonrandomized studies that compared the outcomes
of HID-SCT versus ISD-SCT; the key outcomes including engraftment, OS, DFS/LFS/RFS,
acute/chronic-GVHD, relapse and NRM/TRM; myeloablative conditioning regimens and
HID group GVHD prophylaxis (CsA + MMF + MTX + ATG).
We excluded ongoing studies or studies with data inaccessible. If the same authors had more than one publication based on same population, only the most recent or most complete report was included.
Two reviewers independently assessed the quality of the included studies using Newcastle
Ottawa scale . Studies scoring more than 5 stars were considered acceptable. Data were independently abstracted by each reviewer. Any disagreement between the two reviewers was solved by a third person who extracted the data again.
The extracted information was analyzed on the Cochrane statistical program Review Manager
5.3. For the key outcomes, odds ratio (OR) and 95% confidence intervals (CI) were calculated
for each trial. Dichotomous outcomes were determined by the number of participants with
events and the total number of participants in HID-SCT and ISD-SCT. Heterogeneity was
checked by Q-test and defined as P < 0.1. Heterogeneity was quantified using the I2 metric
(I2<50% acceptable level of heterogeneity; I2>50%, large or extreme). We performed
metaanalysis using a fixed or random effect model (Mantel±Haenszel method for dichotomous
data). A funnel plot was applied to detect the presence of publication bias.
Description of included studies
A total of 187 potentially relevant publications were retrieved from our initial search (Fig 1).
Among these, 46 publications were excluded for review, 120 studies were excluded for not ful
filling the inclusion criteria and 16 were excluded for meeting the exclusion criteria.
Additionally, 2 articles were included through searching the reference lists. Finally, 7 studies including
1919 patients were included [7,8,12±16] (Table 1). Specifically, 936 patients were treated with
HID-SCT and 983 patients received ISD-SCT. Both non-randomized and non-blinded com
parative studies were included. All data from the comparative studies of HID-SCT versus
ISD-SCT were clinical trials. The key outcomes were neutrophil and platelet engraftment, OS,
DFS/LFS/RFS, acute/chronic-GVHD, relapse and NRM/TRM, myeloablative conditioning regimen and HID group with GVHD prophylaxis (CsA + MMF + MTX + ATG) were also included.
Characteristics of the included studies and subgroups
The characteristics of all included studies are shown in Table 2. Different hematologic diseases
were included, such as acute myelogenous leukiemia (AML), acute lymphocytic leukemia
(ALL), myelodysplastic syndromes (MDS), chronic myelogenous leukemia (CML), and
lymphoma. Subgroups were divided by the follow up time 3 year and 4 year. The outcomes of
each study are shown in Table 3.
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Fig 1. Flowchart of selection of studies for inclusion in meta-analysis.
Effects of interventions
Neutrophil and platelet engraftment
Five studies reported neutrophil and platelet engraftment rates, including 705 HID-SCT
treated patients and 672 ISD-SCT-treated patients. For neutrophil engraftment, a fixed effect
model was used. There were no significances differences in the incidence rates of neutrophil
engraftment between the two groups (OR = 0.83, 95% CI = 0.37±1.89, P = 0.66, I2 = 0). The
platelet engraftment was significantly faster following ISD-SCT than HID-SCT (OR = 2.58,
95% CI = 1.70±3.93, P < 0.00001, I 2 = 30%) (Fig 2).
There is a significant difference between HID-SCT and ISD-SCT regarding the incidence rates of acute GVHD, but not chronic GVHD. We extracted data regarding acute GVHD from seven studies including 1919 patients. The fixed effect model was used, results showed the risk
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A study can be awarded a maximum of one star for each numbered item within the Selection and Outcome categories if it meets the criteria. A maximum of two stars
can be given for Comparability.
Selection: 1) Representativeness of the exposed cohort: truly/somewhat representative of the average in the community; 2) Selection of the non exposed cohort: drawn
from the same community as the exposed cohort; 3) Ascertainment of exposure: secure record (eg surgical records) or structured interview; 4) Demonstration that
outcome of interest was not present at start of study.
Comparability: 1) Comparability of cohorts on the basis of the design or analysis: a) stdy controls for; b) study controls for additional factor.
Outcome: 1) Assessment of outcome: independent blind assessment or record linkage; 2) The follow-up was long enough for outcomes to occur; 3) Adequacy of follow
up of cohorts: complete follow up±all subjects accounted for, or subjects lost to follow up unlikely to introduce bias.
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d = day, m = month, y = year, NRM = no relapse mortality, DFS = diseae free survival, LFS = leukemia free survival, RFS = relapse free survival, TRM =
treatmentrelated mortality, OS = overall survival, GVHD = graft versus host disease
of acute GVHD after HID-SCT was significantly higher than ISD-SCT (OR = 1.88, 95%
CI = 1.42±2.49, P < 0.00001, I2 = 37%). No significant difference was found in the incidence
rates of chronic GVHD between HID-SCT and ISD-SCT (OR = 1.25, 95% CI = 0.68±2.30,
P = 0.48, I2 = 89%) (Fig 3).
Relapse and NRM/TRM
Seven studies regarding relapse involving 1919 patients were analyzed with the fixed effect
model. The risk of relapse after HID-SCT was significantly lower than ISD-SCT (OR = 0.70,
95% CI = 0.55±0.90, P = 0.005, I2 = 30%). Four studies reported the NRM rates and three
reported TRM rates, respectively. The risk of TRM was not significantly different between
HID-SCT-treated and ISD-SCT-treated patients (OR = 1.29, 95% CI = 0.85±1.98, P = 0.23, I2 =
0). Significant difference in TRM was found, but it was unreliable because of unacceptable
heterogeneity (OR = 2.33, 95% CI = 2.16±4.30, P = 0.007, I2 = 68%) (Fig 4).
DFS/LFS/RFS and OS
All seven studies reported DFS/LFS/RFS and OS. Fixed effect model showed the heterogeneity
of outcomes was acceptable. The rates of DFS/LFS/RFS after HID-SCT were significantly
lower compared with ISD-SCT (OR = 1.25, 95% CI = 1.03±1.52, P = 0.02, I2 = 0). Significant
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Fig 2. Forest plot of comparisons between HID-SCT and ISD-SCT: Neutrophil and platelet engraftment.
differences in OS and longer life expectancy were found between ISD-SCT-treated and
HID-SCT-treated group (OR = 1.32, 95% CI = 1.08±1.62, P = 0.006, I2 = 31%) (Fig 5).
Meta regression and subgroup analysis
As mentioned above, we found significant heterogeneity in chronic GVHD and NRM rates.
Thus, subgroup analysis by follow-up time was performed to further investigate NRM. It was
found the cumulative incidence rates of NRM for HID-SCT and ISD-SCT were similar at 3
year, but not at 4year (P = 0.13, I2 = 0; P = 0.01, I 2 = 77%) (Table 4). For chronic GVHD,
publication bias might cause the heterogenity(Fig 6).
To our knowledge, this is the first meta-analysis that compares HID-SCT with ISD-SCT in an
unselected population of hematological malignancies. The results indicate that HID-SCT is
associated with a higher risk for acute GVHD, a lower rate of platelets engraftment, and worse
OS and DFS/LFS/RFS. No significant difference was found in TRM rate and neutrophil
engraftment. Previous studies reported that HID-SCThad lower neutrophil engraftment rate
which led to higher TRM. Also the median time to engraftment after HID-SCT was
significantly longer than after ISD-SCT [
]. HID-SCT without ATG resulted in similar
median time for neutrophil engraftment, and longer platelet engraftment compared with
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Fig 3. Forest plot of comparisons between HID-SCT and ISD-SCT: Acute GVHD and chronic GVHD.
]. ATG is associated with delayed immune reconstitution, which is often
accompanied by severe infections and higher TRM. But we found no significant difference in
neutrophil engraftment (according to the follow-up time (30 days)) or cumulative incidence of TRM
between the two groups. Although the median time to engraftment in HID-SCT group was
significantly longer than in the ISD-SCT group, it may indicate neutrophil engraftment within
30d, did not increase the risk of TRM. For platelet engraftment, whatever median time or 100d
cumulative incidence, HID-SCT was thought to have lower engraftment rate than ISD-SCT
[7,12,14±16]. Our meta-analysis indicates HID-SCT is associated with a higher risk of acute
GVHD. However, the reduced intensity transplantation (RIC) with HID-SCT
(post-transplantation cyclophosphamide PT-Cy) has showed similar risks of severe acute GVHD and 3-year
rates of NRM, relapse, OS and PFS compared with ISD-SCT [
]. Similarly, HID-SCT (T-cell
depleted grafts or CsA + MMF + Cyclophosphamide) was associated with a similar risk of
severe acute GVHD [
]. However, some studies reported a higher risk of grade 3±4 of
acute GVHD following HID-SCT with ATG compared to ISD-SCT [
] while some other
studies found a similar risk of grade 3±4 of GVHD between HID-SCT with ATG and ISD-SCT
]. Our meta-analysis indicates HID-SCT with ATG has a higher risk of serious acute
GVHD than ISD-SCT. Further studies are needed to uncover whether ATG can reduce the
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Fig 4. Forest plot of comparisons between HID-SCT and ISD-SCT: Relapse and NRM/TRM.
risk of severe acute GVHD compared with T-cell depleted grafts or PT-Cy. Higher risk for
GVHD is associated with more mortality, correspondingly, the low rate of relapse is supposed
to improve DFS/LFS/RFS, even OS. It should be mentioned that relevant studies also suggested
in high risk acute leukemia, HID-SCT has lower relapse rate and longer OS than ISD-SCT
]. Many studies showed the cumulative risk of relapse was similar or lower after HID-ISD
than ISD-SCT [7,8,12,14±16]. However, this finding is not fully consistent with the
conclusions of our meta-analysis. We found a lower risk for relapse after HID-SCT, but did not find
higher rates for DFS/LFS/RFS or OS. HID-SCT may be superior to ISD-SCT in terms of high
risk acute leukemia but no evidence suggests the low risk of relapse could lead to better DFS/
LFS/RFS or OS.
For the incidence rates of NRM after HID-SCT and ISD-SCT, the outcomes of NRM were opposite between the follow up durations 3 years and 4 years. We did not find significant differences between the two groups at the follow up time 3 years. Related research also showed no significant differences in the incidence of NRM at one year . However, the
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Fig 5. Forest plot of comparisons between HID-SCT and ISD-SCT: DFS/LFS/RFS and OS.
2-year incidence of NRM was significantly lower among haploidentical related recipients com
pared to HLA-matched related recipients for relapsed or refractory Hodgkin Lymphoma [
Over the past decades, new approaches (such as GVHD prophylaxis, conditioning regimen)
were applied to HID-SCT which have effectively controlled intense alloreactivity, resulting in
improved outcomes, but our results indicate ISD-SCT is still the preferred option in all
transplantations, and other promising HID-SCT strategies should be pursued.
Our meta-analysis has some limitations, such as different risk status and diagnosis among the included studies, long time interval, and different follow up durations. To obtain better conclusion, we need more randomized controlled studies.
NRM = transplantation related mortality, OR = odds ratio, CI = confidence intervals
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Fig 6. Funnel plot of comparisons between HID-SCT and ISD-SCT: Chronic GVHD.
S1 Table. PRISMA checklist 2009.
Data curation: Dan Guo, Peipei Xu.
Methodology: Dan Guo, Peipei Xu.
Project administration: Bing Chen.
Software: Dan Guo, Peipei Xu.
Writing ± original draft: Dangui Chen, Bing Chen.
Writing ± review & editing: Dangui Chen, Di Zhou, Bing Chen.
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