A comparison between allogeneic stem cell transplantation from unmanipulated haploidentical and unrelated donors in acute leukemia
Piemontese et al. Journal of Hematology & Oncology
A comparison between allogeneic stem cell transplantation from unmanipulated haploidentical and unrelated donors in acute leukemia
Simona Piemontese 0 1
F. Ciceri 0 1
M. Labopin 0
N. C. Gorin 0
M. Mohty 0
A. Nagler 0
on behalf of
0 EBMT ALWP Office, Hospital Saint Antoine , Paris , France
1 Hematology and Bone Marrow Transplant Unit, San Raffaele Scientific Institute , Milan , Italy
Background: In the absence of a HLA-matched related or matched unrelated donor, allogeneic stem cell transplantation (allo-SCT) from mismatched unrelated donors or haploidentical donors are potential alternatives for patients with acute leukemia with an indication to allo-SCT. The objective of this study was to compare the outcome of allo-SCT from T cell-replete haploidentical (Haplo) versus matched (MUD 10/10) or mismatched unrelated donor at a single HLA-locus (MMUD 9/10) for patients with acute leukemia in remission. Methods: Two hundred sixty-five adult patients with de novo acute leukemia in first or second remission that received a Haplo-SCT between January 2007 and December 2013 were compared with 2490 patients receiving a MUD 10/10 and 813 receiving a MMUD 9/10. Propensity score weighted analysis was conducted in order to control for disease risk imbalances between the groups. Results: The weighted 3-year non-relapse mortality and relapse incidence were 29 and 30% for Haplo, 21 and 29% for MUD 10/10, and 29 and 25% for MMUD 9/10, respectively. The weighted 3-year leukemia-free survival (LFS) and overall survival (OS) were 41 and 46% for Haplo, 50 and 56% for MUD 10/10, and 46 and 48% for MMUD 9/10, respectively. Using weighted Cox model, both LFS and OS were significantly higher in transplants from MUD 10/10 compared from those in Haplo but not different between transplants from MMUD 9/10 and Haplo. The type of donor was not significantly associated with neither acute nor chronic graft-versus-host disease. Conclusions: Patients with acute leukemia in remission have better outcomes if transplanted from a MUD 10/10. We did not find any significant difference in outcome between transplants from MMUD 9/10 and Haplo, suggesting that both can be equally used in the absence of a 10/10 MUD. Key point 1: Better outcomes using fully (10/10) matched unrelated donor for allo-SCT in acute leukemia in remission. Key point 2: Similar outcomes after allo-SCT from unmanipulated haploidentical graft or mismatched (9/10) unrelated donor in acute leukemia in remission.
Allogeneic stem cell transplantation (allo-SCT)
represents the only possible cure for most adult acute
leukemias (AL). HLA-matched related (MRD) or unrelated
donors (MUD) are usually considered the preferable
donors, but they are not available for all the patients
with an indication for allo-SCT. In the absence of a
HLA-matched donor, allo-SCT from mismatched
unrelated donors (MMUD), cord blood units (CB), or
haploidentical (Haplo) donors are potential alternatives.
A Haplo donor is available for virtually all AL patients,
enabling minimal delay and access to repeated stem cell
(SC) donations or donor lymphocyte infusions, if needed.
These are the main reasons for the increasing numbers of
Haplo-SCT for AL in recent years. Unmanipulated (non
ex vivo T-depleted) grafts from Haplo donors, in
comparison to T-depleted ones, result in lower incidence of
serious infections due to faster immune reconstitution
and stronger graft versus leukemia effect [1, 2]. In
addition, the introduction of more effective regimens for
graft-versus-host disease (GvHD) prophylaxis for
Treplete Haplo-SCT contributed to reduce GvHD incidence
and to increase the use of unmaniplated grafts for the
Haplo setting [3–10].
Recently, several reports have shown comparable
allo-SCT outcomes between Haplo and historical
MRD, MUD, and MMUD series [11–15]. However,
these are mostly but one  single center studies
with limited number of patients [11, 12, 15] in
various disease categories and status. For these reasons,
we decided to perform a large, registry-based study,
using the European Society of Bone Marrow
Transplantation (EBMT)-Acute Leukemia Working Party
(ALWP) registry, comparing T-replete Haplo-SCT to
transplants from MUD and MMUD for AL patients
in first or second remission.
In order to be included in the study, the patients had to
fulfill all the following criteria: age ≥18 years; de novo
AL; disease status at transplant: complete remission 1
(CR1) or 2 (CR2); family donor with host/donor number
of HLA mismatches ≥2 (Haplo), or MUD 10/10 or
MMUD 9/10 (patients and donors should have HLA A,
B, C, and DRB1 and DQB1 allelic typing performed);
peripheral blood (PB) or bone marrow (BM) or both as
source of SC; no ex vivo T cell depletion; and first
alloSCT (previous autologous SCT was allowed). All
patients underwent transplantation between January 2007
and December 2013. We were able to verify the
inclusion criteria for 265 Haplo-SCT, 2490 MUD 10/10-SCT,
and 813 MMUD 9/10-SCT. This was a retrospective
multicenter analysis. Data were provided and approved
for this study by the ALWP of the EBMT group registry.
The EBMT is a non-profit, scientific society representing
more than 600 transplant centers mainly in Europe. The
EBMT promotes all activity aiming to improve stem cell
transplantation or cellular therapy, which includes
registering all the activity relating to stem cell transplants.
Data are entered, managed, and maintained in a central
database with internet access; each EBMT center is
represented in this database. There are no restrictions
on centers for reporting data, except for those required
by the law on patient consent, data confidentiality, and
accuracy. Quality control measures included several
independent systems: confirmation of validity of the
entered data by the reporting team, selective comparison
of the survey data with minimum essential data A
(MED-A) data sets in the EBMT registry database,
cross-checking with the National Registries, and regular
in-house and external data audits. Since 1990, patients
have provided informed consent authorizing the use of
their personal information for research purposes.
Definitions and statistical analysis
The primary endpoints were leukemia-free survival
(LFS) and overall survival (OS). The secondary
endpoints were engraftment, acute and chronic GVHD
(aGVHD and cGVHD), relapse incidence (RI),
nonrelapse mortality (NRM), and graft-versus-host
relapsefree survival (GRFS) . LFS was defined as time to
death or relapse, whichever came first. OS was defined
as time to death from all causes. NRM was defined as
death without evidence of relapse. Engraftment was
defined as the first of three consecutive days with an
absolute neutrophil count > 0.5 × 109/L. Acute GVHD
was graded according to the modified Seattle-Glucksberg
criteria  and cGVHD according to the revised Seattle
We used propensity scores (PS) weighting to control
for pre-treatment imbalances on observed variables. The
following factors were included in the PS model: patient
age, time from diagnosis to transplantation, year of
transplant, diagnosis (AML versus ALL), status at
transplant (CR1 versus CR2), cytogenetics group, donor/
patient CMV serology, conditioning (RIC versus MAC),
and sex matching (female donor to male recipient versus
other). The estimation of propensity score was performed
using generalized boosted models .
As the study question was whether Haplo could replace
10/10 or 9/10 MUD, we weighted the groups receiving
either MUD 10/10- and MMUD 9/10-HSCT to match the
characteristics of patients receiving Haplo-SCT, by
estimating the average treatment effect among the treated
(ATT); Haplo-HSCT being the treated group. The ATT
weights equal one for Haplo-HSCT, and it equals the ratio
of the propensity score to one minus the propensity score
in the two UD-HSCT groups. Therefore, UD patients that
were significantly different from average haplo-grafted
patients had a low contribution in the comparisons. We
checked the balance between the groups looking to ATT
weighted means. Then, we used pairwise ATTs to fit the
weighted Kaplan-Meier and Cox models separately for
Haplo- versus MUD 10/10-HSCT and Haplo- versus
The type I error rate was fixed at 0.05 for
determination of factors associated with time to event. Analyses
were performed using the R statistical software version
3.2.3 (R Development Core Team, Vienna, Austria);
propensity score analysis was performed using the mnps
function of the Twang package and weighted analyses
using the survey package .
Patients’ and donors’ characteristics
Patient’s and host/donors’ characteristics are showed in
Table 1. Regimens, stem cell source, and GvHD
prophylaxis are described in Table 2. Anti-thymocyte globulin
(ATG) was used for in vivo T cell depletion in 120/265
Haplo (45%), 1457/2490 (59%) 10/10 MUD, and 550/813
(82%) 9/10 MMUD. Campath was used in 6/265 Haplo
(1%), 302/2490 (12%) MUD, and 124/813 (18%) MMUD.
PT-Cy was used in 107/265 Haplo (40%), 27/2490 (1%)
MUD, and 12/813 (1%) MMUD. Among patients
receiving a MMUD 9/10, 204 (25%) were mismatched in locus
A, 115 (14%) in locus B, 275 (34%) in locus C, 62 (8%)
in locus DRB1, and 157 (19%) in locus DQB1. Allelic
typing for locus A, B, C, DRB1, and DQB1 was available
for all patients and donors.
The 30-day CI of engraftment was 95% (92–97%) for
Haplo, 97% (93–98%) for MUD 10/10, and 92% (88–
95%) for MMUD 9/10. In weighted Cox model, CI of
engraftment resulted to be lower in Haplo versus MUD
10/10 (p = 0.015) but not different between Haplo and
MMUD 9/10 (p = 0.62).
Non-relapse mortality, acute and chronic GvHD
The weighted CI of NRM at 3 years was 29% (23–34%),
21% (15–26%), and 29% (23–35%) for Haplo , MUD 10/
10, and MMUD 9/10 (Fig. 1a), respectively. In weighted
Cox model, NRM was lower in MUD 10/10 as compared
in Haplo, but not different from that in MMUD 9/10
(Table 3). The percentage of grades II–IV aGvHD was
28% (22–33%), 25% (18–31%), and 27% (21–33%) for
Haplo, MUD 10/10, and MMUD 9/10, respectively. The
frequency of grades III–IV aGvHD was 10% (6–13%) for
Haplo, 7% (3–10%) for MUD 10/10, and 11% (6–15%)
for MMUD 9/10. The 3-year CI of overall cGvHD and
extensive cGvHD was 34% (28–40%) and 15% (10–20%),
40% (33–47%) and 22% (15–28%), and 33% (26–39%)
and 18% (12–23%) for Haplo, MUD 10/10, and MMUD
9/10, respectively. Neither grades II–IV aGvHD nor
chronic GvHD incidences differed between Haplo versus
MUD 10/10 and Haplo versus MMUD 9/10 in weighted
Cox analysis (Table 3).
The weighted CI of relapse at 3 years was 30% (24–
35%), 29% (22–35%), and 25% (19–31%) for Haplo,
MUD 10/10, and MMUD 9/10, respectively (Fig. 1b).The
type of donor was not a predictive factor for relapse in
weighted Cox model (Table 3).
LFS, OS, and GRFS
The median follow-up among survivors was 34 (range,
3–84) months for Haplo, 36 (range, 1–103) for MUD
10/10, and 36 (range, 1–102) for MMUD 9/10,
respectively. The weighted probability of LFS at 3 years was
41% (35–48%), 50% (43–58%), and 46% (39–53%) for
Haplo, 10/10 MUD, and 9/10 MMUD, respectively
(Fig. 2).The weighted probability of 3-year OS was 46%
(40–53%), 56% (49–64%), and 48% (41–56%) (Fig. 2).The
3-year GRFS was 33% (28–40%), 36% (29–44%), and
34% (28–41%) for Haplo, 10/10 MUD, and 9/10 MMUD,
respectively (Fig. 2). In the weighted Cox analysis, LFS
and OS resulted to be better for MUD 10/10 compared
with Haplo, but no statistical difference comparing
Haplo with MUD 9/10. No statistical differences were
found in GRFS according to the type of donor in the
weighted Cox analysis (Table 3).
In the absence of a MRD for allo-SCT in acute leukemia,
the ideal donor still remains to be determined. The
current report represents a large registry study
comparing the outcome between transplants from Haplo and
MUD 10/10 or MMUD 9/10 for adult patients with de
novo AL in remission.
As a recent ALWP-EBMT survey on
unmanipulated haploidentical transplantation in AL showed a
lower incidence of aGvHD in patients receiving
PTCy but no significant statistical differences in either
LFS or OS , in our study we included all the
non T-depleted Haplo-SCT registered in the EBMT
Previous reports described worse outcomes after
MMUD in comparison to MUD [22–26], and this
finding was in accordance to our preliminary data and to a
recent ALWP publication .
We did not find any differences in terms of LSF and
OS in the 813 MMUD-SCT according to HLA-DQ
mismatch in univariate analysis (p = 0.35). Therefore, we
decided to compare separately MUD 10/10 and MMUD
9/10 transplants with Haplo.
MUD 10/10 vs Haplo
MMUD 9/10 vs Haplo
Table 2 Conditioning regimens, stem cell source, and in vivo T cell depletion
MUD 10/10 vs Haplo
MMUD 9/10 vs Haplo
Stem cell source
In vivo T cell depletion
See text for abbreviations
The 30-day CI of engraftment proved to be lower in
Haplo than in MUD 10/10 but not different between
Haplo and MMUD 9/10. In addition to the type of
donor, the number and type of chemotherapy cycles
pretransplant and/or early post-transplant infections, in
particular viral, could have had an impact on differences
in engraftment. A lower incidence of engraftment in
Haplo compared in UD was previously reported in both
reduced intensity  and myeloablative conditioning
Notably, we did not find any difference in the
incidence of either aGvHD > II or cGvHD according to
donor type in line with similar comparisons in
literature. This was true also for grades III–IV aGvHD and
extensive cGvHD. In the recent report comparing
Haplo using PT-Cy to UD from the Center for
International Blood and Marrow Transplant Research
(CIBMTR), the authors describe a lower incidence of
acute and cGvHD in Haplo on univariate analysis
, but most of the Haplo were performed using
BM as stem cell source, and most of the UD using
PB without receiving any in vivo T cell depletion. Of
note, they did not find any difference in the 3-year
cGvHD incidence according to donor type when
analyzing only patients receiving BM. The role of stem
cell source as risk factor for cGvHD after Haplo-SCT
remains to be determined. While some reports do not
show any difference in terms of cGvHD between PB
and BM in haploidentical transplantations using
Cy [28, 29], a recent comparison from CIBMTR
Fig. 1 Weighted CI of relapse and non-relapse mortality according to donor type. a Weighted CI of relapse. b Weighted CI of NRM
Table 3 Weighted Cox model for NRM, RI, LFS, OS, and GRFS
Day 30 PMN engraftment
See text for abbreviations
concludes for a high incidence of cGvHD using PB
instead of BM . Notable, in the context of UD,
cGvHD has been shown to be higher using PBSC 
especially if not using in vivo T cell depletion .
The 3-year NRM was higher using Haplo (29%)
compared with MUD 10/10 (21%) but identical
compared with MMUD (29%), in contrast with other
reports on similar comparisons where the authors did
not find any difference [11–15]. This higher NRM in
Haplo compared in MUD 10/10 could be in part due
to the use of in vivo T cell depletion other than
PTCy in the 45% of our Haplo . In addition to the
type of in vivo T cell depletion, also, differences in
conditioning regimens could explain our finding .
Patients’ comorbidities, mostly unknown in
restrospective study, could also have influenced NRM. The
3-year CI of relapse was not different between the
The lower NRM in MUD 10/10 resulted in both a
higher 3-year LFS and OS compared in Haplo but
no difference in GRFS. No differences in either OS,
LFS, or GRFS were observed between Haplo and
MMUD 9/10. Analyzing separately patients with
AML and ALL, we found no differences of GRFS in
Haplo compared in MUD 10/10 and compared in
MMUD 9/10, higher LFS and OS in MUD 10/10
compared in Haplo but no differences between
Haplo and MMUD 9/10 in terms of LFS and OS
(Additional file 1).
Based on these results, we can assert that patients with
acute leukemia in remission showed better outcomes if
transplanted from a MUD 10/10. We did not find any
significant difference in outcome between MMUD 9/10
and Haplo, suggesting that both can be equally used in
the absence of a MUD 10/10 and that other factors, such
as urgency of transplant and center expertise should
dictate the choice between these two alternative donor
Ongoing and future prospective clinical studies,
including transplants from CBU, will ultimately be
required to determine the best alternative donor for adult
AL patients who lack an HLA-matched sibling one.
Years post transplantation Years post transplantation
Fig. 2 Weighted probability of leukemia-free survival and overall survival according to donor type. a Weighted probability of leukemia-free
survival. b Weighted probability of overall survival
Additional file 1: Table AML and ALL. (DOCX 18 kb)
Additional file 2: Participating centers’ Table. (DOCX 37 kb)
AL: Acute leukemia; ALL: Acute lymphoblastic leukemia; AML: Acute myeloid
leukemia; ATG: Anti-thymocyte globulin; ATT: Average treatment effect
among the treated; BM: Bone marrow; CB: Cord blood;
CMV: Cytomegalovirus; CR: Complete remission; GRFS: Graft-versus-host
relapse-free survival; GVHD: Graft-versus-host disease (acute aGvHD or
chronic cGvHD); HAPLO: Haploidentical donor; LFS: Leukemia-free survival;
MAC: Myeloablative conditioning regimen; MMUD: Mismatched unrelated
donor; MRD: Matched related donor; MUD: Matched unrelated donor;
NRM: Non-relapse mortality; OS: Overall survival; PB: Peripheral blood;
PMN: Polymorphonuclear cells; PS: Propensity score; PT-Cy: Post-transplant
cyclophosphamide; RI: Relapse incidence; RIC: Reduced intensity
conditioning regimen; SC: Stem cell; SCT: Stem cells transplantation;
The authors thank all allogeneic transplantation centers of the EBMT group
for reporting to the registry the data included in this analysis. A list of the
participating EBMT centers appears in the Additional file 2. We thank Pr J.V.
Melo for the critical reading of the manuscript.
Availability of data and materials
Data are entered, managed, and maintained in a central database with
Internet access; each EBMT center is represented in this database.
SP, ML, and FC designed the research. SP collected and checked the data
and contacted the transplantation centers. SP and ML analyzed the data. SP,
ML, FC, MM, AN, and N-CG wrote the paper. FC, MM, AN, AW, K-KS, SS, HH,
BD, CC, GZ, and BA provided the data. The results of this study were partially
presented as an oral presentation at the EBMT 2014 annual meeting and as
a poster presentation at the ASH 2014 meeting. All authors read and
approved the final manuscript.
The authors declare that they have no competing interests.
Consent for publication
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