hematol transfus cell ther.

2 0 1 9;4 1(1):1–6

Hematology, Transfusion and Cell Therapy

www.rbhh.org

Original article

Assessing the impact of ABO incompatibility on

major allogeneic hematopoietic stem cell
transplant outcomes: a prospective, single-center,
cohort study

José Alfreu Soares Júnior, Glaucia Helena Martinho, Antonio Vaz de Macedo,
Marisa Ribeiro Verçosa, Vandack Nobre, Gustavo Machado Teixeira ∗
Hospital das Clínicas da Universidade Federal de Minas Gerais (HC UFMG), Belo Horizonte, MG, Brazil

a r t i c l e i n f o a b s t r a c t

Article history: Background: ABO blood group incompatibility between donor and recipient is associated with
Received 18 September 2017 a number of immunohematological complications, but is not considered a major contraindi-
Accepted 3 May 2018 cation to allogeneic hematopoietic stem cell transplantation. However, available evidence
Available online 10 July 2018 from the literature seems to be conflicting as to the impact of incompatibility on overall sur-
vival, event-free survival, transplant-related mortality, graft-versus-host disease, and time
Keywords: to neutrophil and platelet engraftment.
ABO incompatibility Methods: This single-center, prospective, cohort study included patients with hematological
Hematopoietic stem cell transplant malignancies who underwent a first allogeneic hematopoietic stem cell transplantation
Outcomes of bone marrow between 2008 and 2014. Patients receiving umbilical cord blood as the stem cell source were
transplantation excluded from this analysis. The impact of ABO incompatibility was evaluated in respect
to overall survival, event-free survival, transplant-related mortality, acute graft-versus-host
disease and engraftment.
Results: A total of 130 patients were included of whom 78 (60%) were males. The median
age at transplant was 36 (range: 2–65) years, 44 (33%) presented ABO incompatibility, 75
(58%) had acute leukemia, 111 (85%) had a related donor, 100 (77%) received peripheral blood
hematopoietic stem cells as graft source and 99 (76%) underwent a myeloablative condition-
ing regimen. There was no statistically significant association between ABO incompatibility
and overall survival, event-free survival, transplant-related mortality, grade II–IV acute graft-
versus-host disease, neutrophil or platelet engraftment in multivariate analysis.
Conclusion: These results show that ABO incompatibility does not seem to influence these
parameters in patients undergoing allogeneic hematopoietic stem cell transplantation.
© 2018 Associação Brasileira de Hematologia, Hemoterapia e Terapia Celular. Published
by Elsevier Editora Ltda. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).

∗
Corresponding author at: Programa de residência médica em hematologia e hemoterapia do Hospital das Clínicas da Universidade
Federal de Minas Gerais (HC UFMG), Av. Professor Alfredo Balena, 110, Santa Efigênia, Belo Horizonte, MG CEP: 30.130-100, Brazil.
E-mail address: [email protected] (G.M. Teixeira).
https://doi.org/10.1016/j.htct.2018.05.007
2531-1379/© 2018 Associação Brasileira de Hematologia, Hemoterapia e Terapia Celular. Published by Elsevier Editora Ltda. This is an
open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
2 hematol transfus cell ther. 2 0 1 9;4 1(1):1–6

weight and intravenous melphalan at a dose equal to or

Introduction less than 140 mg/m2 /body surface area.
b. Myeloablative conditioning (MAC): use of oral busulfan and
Allogeneic hematopoietic stem cell transplantation
intravenous melphalan doses greater than 9 mg/kg/body
(alloHSCT) constitutes a potentially curative approach to
weight and 140 mg/m2 /body surface area, respectively.
a number of malignant and non-malignant hematological
diseases. During the past few decades, results of alloHSCT
ABO compatibility
have improved considerably, particularly with advances in
donor selection, hematopoietic stem cell source, supportive
Transplants were classified according to ABO compatibility
measures, management of post-transplant complications,
between donor and recipient, as follows:
and development of less toxic conditioning regimens, as
well as novel post-transplant treatment platforms. This (a) ABO iso-group: donor and recipient had the same ABO
improvement has broadened alloHSCT indications sig- blood group;
nificantly worldwide and has expanded the number of (b) Minor ABO incompatibility: when the donor had iso-
transplant-eligible patients.1,2 hemagglutinins against recipient red blood cell antigens;
Donor-recipient ABO blood group incompatibility (ABOi) (c) Major ABO incompatibility: when the recipient had iso-
is not a contraindication to alloHSCT. ABOi is observed in hemagglutinins directed against donor red blood cell
30–40% of human leukocyte antigen (HLA)-matched trans- antigens; this group also included bidirectional ABO
plants, since ABO genetic inheritance is independent to that incompatibility (i.e., when there were iso-hemagglutinins
of HLA haplotypes. Several complications related to ABOi against both donor and recipient red blood cell antigens).
have been described in studies, such as acute and chronic
hemolytic transfusion reactions,3–5 pure red cell aplasia,6–8
Clinical outcome definitions
delayed engraftment,9,10 and increased incidence of acute
graft-versus-host disease (GvHD),11,12 but this has not been
Neutrophil engraftment: the first of three consecutive
confirmed in others.13–15 Conflicting results seem to be more
days with a neutrophil count equal to or greater than
prominent with regard to the occurrence of GvHD in this
0.5 × 109 cells/L. For this analysis, the incidence of neutrophil
setting.16,17
engraftment was considered within the first 30 days post-
Considering the conflicting evidence as to the real impact
transplant.
of ABOi on alloHSCT outcomes, this study aimed to assess
Platelet engraftment: the first of seven consecutive days
the impact of ABOi on major outcomes in patients with
with a platelet count equal to or greater than 20 × 109 /L with-
hematological malignancies undergoing a first alloHSCT at a
out transfusion support. The incidence of platelet engraftment
transplant referral center in Brazil.
was considered within the first 100 days post-transplant.
Transplant-related mortality: death associated with
alloHSCT complications and not related to relapse. The
Methods cumulative incidence of transplant-related mortality was
assessed at one year post-transplant.
This was a prospective, single-center, cohort study, com-
Event-free survival: probability of being alive after trans-
prising patients with hematological malignancies (acute
plant without having any events during the first two years
leukemia, myelodysplastic syndrome, primary myelofibrosis,
post-transplant. For this analysis, ‘event’ was defined as death
chronic myeloid leukemia, lymphoma, and multiple myeloma)
or relapse.
undergoing a first related or unrelated alloHSCT at Hos-
Overall survival: probability of being alive at two years post-
pital das Clínicas, Universidade Federal de Minas Gerais,
transplant.
Brazil, between the 1st April, 2008 and 31st December, 2014.
Acute GvHD was classified and graded according to the
Patients receiving umbilical cord blood as stem cell source
Glucksberg-Seattle criteria.20 The cumulative incidences of
and those undergoing haploidentical transplantation were
grade II–IV and grade III–IV acute GvHD were assessed within
excluded from this analysis. This study was approved by
the first 100 days post-transplant.
the institutional Research Ethics Committee, which abides by
the Declaration of Helsinki principles for research in human
Statistical analysis
beings, and an informed consent form was obtained from all
study participants.
Frequency (n) and proportion measures were used for categor-
ical variables and median, minimum and maximum values
Conditioning regimen were considered for continuous variables. Transplant-related
mortality was defined as death from all causes not related
The conditioning regimens administered in the included to relapse. Event-free survival was defined as the interval
patients were classified according to the National Marrow between transplant and death or relapse, whereas overall sur-
Donor Program (NMDP) and the Center for International Blood vival comprised the interval between transplant and death
and Marrow Transplant Research (CIBMTR), as follows18,19 : from all causes. Event-free and overall survival were esti-
mated using the Kaplan–Meier method and the log-rank test
a. Reduced intensity conditioning (RIC): use of an oral busulfan was used to compare these survival curves in the univari-
formulation at a dose equal to or less than 9 mg/kg/body ate analysis. Data was censored at the time of death or of
 hematol transfus cell ther. 2 0 1 9;4 1(1):1–6 3

last follow-up. The Gray method was used for the analyses of
Table 1 – Characteristics of the population studied
competing events: in the analyses of neutrophil and platelet (n = 130).
engraftment and of acute GvHD cumulative incidences, death
Characteristic
was considered a competing event, whereas, in the analysis
of the cumulative incidence of transplant-related mortality, Gender: male – n (%) 78 (60.0)
relapse was considered as a competing event. A significance Age at transplant (years) – median (range) 36 (2–65)
level of 5% (p-value = 0.05) with a 95% confidence interval (95% ABO incompatibility (ABOi) classification – n (%)
CI) was used for the hazard ratio (HR) estimates. Cox’s propor- ABO iso-group 86 (66.1)
tional hazards model was used for the multivariate analyses Minor ABOi 20 (15.3)
of overall and event-free survival, and the Fine and Gray mul- Major ABOi 20 (15.3)
Bidirectional ABOi 4 (3.3)
tivariate method for competing events was applied for the
analyses of cumulative incidence of transplant-related mor- Primary disease – n (%)
tality, neutrophil and platelet engraftment, and acute GvHD. AML 46 (35.4)
The following variables were included in the univariate anal- ALL 29 (22.3)
CML 20 (15.4)
ysis: source of hematopoietic stem cells, type of conditioning
HL 4 (3.1)
regimen, type of donor, and type of ABOi. Variables with a p- NHL 11 (8.5)
value ≤0.30 in the univariate analysis, as well as the type of MM 1 (0.8)
ABOi were included in the multivariate analysis. All statistical MDS 12 (9.2)
analyses were performed using the Easy R software package. PMF 7 (5.1)

Graft source – n (%)

BMHSC 30 (23.1)
Results PBHSC 100 (76.9)

Conditioning regimen – n (%)

Patients
MAC 98 (75.4)
RIC 32 (24.6)
A total of 130 patients were included, of whom 86 (66%) were
Type of donor – n (%)
ABO iso-group with their donors, 20 (15.3%) had minor ABOi,
Related 111 (85.4)
20 (15.3%) had major ABOi, and four (3%) had bidirectional
Unrelated 19 (14.6)
ABOi. There was a predominance of males (60.0% of cases).
The median age at transplant was 36 (range: 2–65) years. Acute ABOi: ABO blood group incompatibility; ALL: acute lymphoblastic
myeloid leukemia (AML) and acute lymphoblastic leukemia leukemia; AML: acute myeloid leukemia; BMHSC: bone mar-
(ALL) were the main primary hematological diseases, compris- row hematopoietic stem cells; CML: chronic myeloid leukemia;
HL: Hodgkin lymphoma; MAC: myeloablative conditioning; MDS:
ing 46 (35.3%) and 29 (22.3%) cases, respectively. Patients’ main
myelodysplastic syndrome; MM: multiple myeloma; NHL: Non-
characteristics are shown in Table 1. Hodgkin’s lymphoma; PBHSC: peripheral blood hematopoietic
stem cells; PMF: primary myelofibrosis; RIC: reduced intensity
Neutrophil and platelet engraftment conditioning.

The cumulative incidence of neutrophil engraftment at 30

days was 83.8% (median: 19 days; range: 3–30 days). In uni- analysis, neither the type of ABOi nor the other studied vari-
variate analysis (Table 2), type of ABOi was associated with an ables were associated with the cumulative incidence of grade
increase in the time to neutrophil engraftment (88.4% of neu- III–IV acute GvHD (Table 3).
trophil engraftment in the ABO iso-group versus 62.5% in the
major/bidirectional ABOi transplants; p-value = 0.02). Neither Transplant-related mortality
the type of ABOi nor the other studied variables showed any
statistically significant predictive association with neutrophil The cumulative incidence of transplant-related mortality dur-
engraftment in the multivariate analysis. Regarding the cumu- ing the first year of transplant was 38.5%. Neither the type
lative incidence of platelet engraftment, it occurred in 76.2% of ABOi nor the other studied variables showed any statisti-
of cases during the first 100 days post-transplant (median: 21 cally significant predictive association with transplant-related
days; range: 3–100 days). None of the studied variables showed mortality in either the univariate or the multivariate analyses
any predictive association with platelet engraftment (Table 2 (Tables 2 and 3, respectively).
and Table 3).
Event-free and overall survival
Graft-versus-host disease
The estimated event-free and overall survival at two years
The cumulative incidences of grade II–IV and grade III–IV acute post-transplant were 32.0% (95% CI: 21.3–36.9%) and 35.4%
GvHD during the first 100 days post-transplant were 33.1% and (95% CI: 26.3–42.6%), respectively. Univariate (Table 2) and
7.7%, respectively. Neither the type of ABOi nor the other stud- multivariate (Table 3) analyses did not show any statis-
ied variables showed any statistically significant association tically significant association between ABOi (p-value = 0.46)
with the cumulative incidence of grade II–IV and grade III–IV or the other studied variables with event-free or overall
acute GvHD in the univariate analysis (Table 2). In multivariate survival.
4 hematol transfus cell ther. 2 0 1 9;4 1(1):1–6

Table 2 – Univariate analysis of the main post-transplant outcomes of 130 patients submitted to hematopoietic stem cell
transplant at a single center in Brazil.
OS EFS TRM aGVHD II-IV NE PE

% p % p % p % p % p % p

Classification
ABO iso-group 37.2 0.42 33.7 0.46 37.2 0.29 38.4 0.17 88.4 0.02 79.1 0.27
Minor ABOi 40.0 36.8 30.0 25.0 85.0 75.0
Major/bidirectional ABOi 25.0 21.7 50.0 20.8 62.0 58.3

Graft source
BM HSC 40.0 0.51 34.5 0.92 30.0 0.29 36.7 0.62 90.0 0.41 76.7 0.96
PBHSC 34.0 31.3 41.0 32.0 82.0 75.0

Gender
Male 33.8 0.83 31.5 0.79 41.6 0.40 35.1 0.48 81.8 0.08 76.6 0.67
Female 37.7 32.7 34.0 30.2 86.8 75.5

Conditioning regimen
MAC 35.4 0.61 31.6 0.87 41.9 0.69 33.3 0.93 83.8 0.12 75.8 0.10
RIC 35.5 33.3 37.4 32.3 83.9 77.4

Type of donor
Related 38.7 0.13 34.9 0.27 36.0 0.23 31.5 0.47 82.9 0.78 77.5 0.36
Unrelated 15.8 15.8 52.6 42.1 84.2 63.2

ABOi: ABO blood group incompatibility; BM HSC: bone marrow hematopoietic stem cells; PBHSC: peripheral blood hematopoietic stem cells;
MAC: myeloablative conditioning; RIC: reduced intensity conditioning; OS: overall survival; EFS: event-free survival; TRM: transplant-related
mortality; aGHVD: acute graft-versus-host disease; NE: neutrophil engraftment; PE: platelet engraftment.
Significance set for a p-value <0.05.

Table 3 – Multivariate analysis of the main post-transplant outcomes in 130 patients undergoing hematopoietic stem cell
transplant at a single center in Brazil.
Outcome Variable Hazard ratio (95% CI) p-Value

OS ABOi Minor 1.25 (0.72–2.17) 0.41

Major/bidirectional 0.87 (0.48–1.58) 0.66
Type of donor Unrelated 1.43 (0.81–2.52) 0.21
EFS ABOi Minor 1.28 (0.73–2.23) 0.37
Major/bidirectional 1.00 (0.55–1.80) 0.99
Type of donor Unrelated 1.24 (0.70–2.19) 0.45
TRM ABOi Minor 1.47 (0.73–2.97) 0.47
Major/bidirectional 1.29 (0.64–2.59) 0.42
Type of donor Unrelated 0.71 (0.31–1.61) 0.19

aGVHD II-IV
ABOi Major/bidirectional 1.19 (0.25–5.63) 0.82
Type of regimen MAC 0.33 (0.04–2.64) 0.30
NE ABOi Minor 0.50 (0.30–0.90) 0.20
Major/bidirectional 1.11 (0.65–1.89) 0.69
Recipient sex Female 1.31 (0.89–1.92) 0.17
Type of regimen MAC 1.30 (0.78–2.15) 0.31
PE ABOi Minor 0.67 (0.39–1.16) 0.16
Major/bidirectional 1.12 (0.62–2.01) 0.70
Type of donor Unrelated 1.37 (0.80–2.33) 0.25

ABOi: ABO blood group incompatibility; OS: overall survival; EFS: event-free survival; TRM: transplant-related mortality; aGHVD II–IV: acute grade
II–IV graft-versus-host disease; MAC: myeloablative conditioning; NE: neutrophil engraftment; PE: platelet engraftment; 95% CI: 95% confidence
interval.
Significance set for a p-value <0.05.
 hematol transfus cell ther. 2 0 1 9;4 1(1):1–6 5

transplants, among which 22.5% had major ABOi, 16.8% had

Discussion minor ABOi, and 5.6% had bidirectional ABOi within donor-
recipient pairs. These authors did not observe any statistically
The present study evaluated both the presence and the clin- significant differences in the incidence of transplant-related
ical relevance of ABOi in alloHSCT. No significant impact of mortality, acute GvHD, neutrophil engraftment and platelet
ABOi was found on overall and event-free survival, nor on engraftment between the ABOi and the ABO iso-group trans-
the cumulative incidence of transplant-related mortality, neu- plants, which is in accordance with the findings of the present
trophil and platelet engraftment, and grade II–IV and grade study.
III–IV acute GvHD. In another retrospective study which included a larger
The proportion of patients stratified as having ABOi in number of patients (562) with hematological malignancies
this study is in accordance with that of the medical lit- (mainly acute leukemia), 35.8% of cases had ABOi (27.0% had
erature, where 30–50% of allogeneic transplants are ABO minor ABOi, 23.7% had major ABOi, and 4.7% had bidirectional
incompatible.21 ABOi). In contrast to the findings herein, this study noted a sig-
Goldman et al.,22 in a retrospective study including nificant association between minor ABOi transplants and the
153 alloHSCT recipients with hematological malignancies, incidence of low-grade acute GvHD, but no differences were
showed, as in the current study, that the presence of ABOi observed in respect to the incidence of moderate or severe
does not influence overall survival. Their cohort study differs (II–IV) acute GvHD.25
from this study due to its retrospective design and the fact that In keeping with most of the aforementioned studies, no
patients with both Hodgkin’s and non-Hodgkin lymphoma differences were observed with regard to overall survival and
and multiple myeloma were excluded from the analysis. to transplant-related mortality, nor to the incidence of acute
Moreover, these authors showed a greater proportion of donor- GvHD, between the ABO groups in the current study.
recipient pairs with ABOi (45.1% versus 33.9%), with a different The major drawbacks of this study were that it was lim-
distribution of ABOi subtypes: minor ABOi accounted for 18.9% ited to a single-center cohort, patients were enrolled based
of cases compared to 15.3% in this study; major ABOi repre- on convenience sampling during a pre-specified time period
sented 22.9% (versus 15.3%) and bidirectional ABOi comprised and included a relatively small number of subjects with
3.3% of cases (which is equal to the 3.3% observed in this ABOi (20 minor ABOi transplants, 20 major ABOi cases, and
study). only four bidirectional ABOi donor-recipient pairs). This may
On the other hand, the results of a Japanese marrow donor have masked potentially significant differences in outcomes
program that retrospectively analyzed data from 5549 allo- between ABOi subgroups. Likewise, due to the relatively small
geneic transplants with unrelated donors for the treatment number of patients who had ABOi and survived after Day 100
of malignant and non-malignant hematological diseases post-transplant (i.e., only 13 patients), it was not possible to
showed that transplants with minor or major ABOi had worse analyze the potential association of ABOi with the occurrence
overall survival as compared to ABO iso-group transplants. of chronic GvHD in this population. Moreover, since most of
In that study, no significant difference was noted in overall the patients received transfusions at different centers during
survival for bidirectional ABOi transplants when compared to the late post-transplant period, we were unable to analyze the
iso-group ones. However, worse transplant-related mortality, probable implications of ABOi regarding transfusion depen-
delayed neutrophil and platelet engraftment, and greater inci- dence and burden (due to a lack of reliable data from the
dence of grade III–IV acute GvHD were observed in both major centers).
and minor ABOi groups. That study also observed a greater
proportion of HLA-mismatched transplants in the major,
minor and bidirectional ABOi groups (43.9% HLA-mismatched Conclusions
transplants in the major ABOi group, 23.1% in the minor ABOi
group, and 2.8% in the bidirectional group) in comparison to This prospective, single-center, cohort study found that ABOi
the ABO iso-group (30.2%) pairs (p-value <0.001). Such discrep- does not seem to influence overall and event-free survival, nor
ancy between the proportion of HLA mismatch in the ABO the incidence of transplant-related mortality, acute GvHD, or
iso-group cases and that of the ABOi groups may have influ- neutrophil and platelet engraftment in HLA-identical, related
enced the overall survival, transplant-related mortality and and unrelated, alloHSCT patients. Multicenter studies, with a
acute GvHD estimates found by those authors.23 Moreover, greater number of patients with ABOi, may help to shed light
when compared to this study, important differences emerge on the effects of ABOi on these and other clinically relevant
with regard to the characteristics of the population studied, post-transplant outcomes in this population.
such as those related to the type of primary disease (malignant
and benign disease versus only malignant hematological dis- Conflicts of interest
ease in this study), the type of donor (100% unrelated donors
versus 14.6% in this study), and the proportion of patients with The authors declare no conflicts of interest.
ABOi (49.2% in the Kimura et al.,22 study versus 33.9% in this
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