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Blood, Vol. 94 No. 4 (August 15), 1999:
pp. 1465-1470
Risk Factors for Acute Graft-Versus-Host Disease After Allogeneic Blood
Stem Cell Transplantation
By
Donna Przepiorka,
Terry L. Smith,
Jody Folloder,
Issa Khouri,
Naoto T. Ueno,
Rakesh Mehra,
Martin Körbling,
Yang O. Huh,
Sergio Giralt,
James Gajewski,
Michele Donato,
Karen Cleary,
David Claxton,
Ira Braunschweig,
Koen van Besien,
Borje S. Andersson,
Paolo Anderlini, and
Richard Champlin
From the Departments of Blood and Marrow Transplantation,
Biomathematics, Laboratory Medicine and Pathology, University of Texas
M.D. Anderson Cancer Center, Houston, TX
 |
ABSTRACT |
We evaluated demographic characteristics and graft composition as
risk factors for acute graft-versus-host disease (GVHD) in 160 adult
recipients of HLA-identical allogeneic blood stem cell transplants. The
patients received a median nucleated cell dose of 7.9 × 108/kg and median C34+ cell dose of 5.6 × 106/kg. GVHD prophylaxis consisted of cyclosporine (CSA)
and steroids, tacrolimus (FK506) and steroids, or FK506 and
methotrexate. Grades 2 to 4 GVHD occurred in 31% (95% CI, 23% to
39%), and grades 3 to 4 GVHD in 14% (95% CI, 8% to 20%). In
univariate analyses, GVHD prophylaxis with CSA and high
CD34+ cell doses were significant risk factors for grades
2 to 4 GVHD, but diagnosis, age, use of total body irradiation, donor
sex, female donor for male recipient, donor parity, donor
alloimmunization, viral serology, nucleated cell dose,
CD3+ cell dose, and CD56+ cell dose did not
alter the incidence of GVHD significantly. With a CD34+
cell dose less than 8 × 106 CD34+ cells/kg,
the risk of grades 2 to 4 GVHD was significantly higher for those who
received CSA (39%, 95% CI, 21% to 47%) in comparison with those on
FK506 (18%, 95% CI, 10% to 26%) (P = .03), but GVHD prophylaxis regimen had less impact with a higher CD34+
cell dose (overall grades 2 to 4 GVHD rate 52%, 95% CI, 37% to 67%). GVHD prophylaxis and CD34+ cell dose are
independent risk factors for acute GVHD after allogeneic blood stem
cell transplantation.
© 1999 by The American Society of Hematology.
| |
INTRODUCTION |
WHETHER THE HIGH number of lymphocytes in
blood stem cell grafts would increase the risk of acute
graft-versus-host disease (GVHD) after primary allogeneic
transplantation was initially a topic of intense debate. Concern
diminished when the first reports by Russell et al1 and
Sasaki et al2 showed that engraftment of allogeneic blood
stem cells was successful without fatal GVHD, and the feasibility of
this approach was further supported by several case
series.3-5 Comparisons to historical control marrow recipients6-11 and one randomized Phase II
study12 further suggested that the risk of acute GVHD was
no greater with blood stem cell grafts than with marrow grafts from
HLA-identical donors, and randomized Phase III studies to address this
issue are currently ongoing. Interestingly, the rates of grades 2 to 4 GVHD reported have ranged from 14% to 70% for allogeneic blood stem
cell transplant recipients with HLA-identical donors,6-18
and the reason for this wide range is unclear.
Although histoincompatibility remains the strongest risk factor for
acute GVHD, within the subset of patients receiving
non-T-cell-depleted marrow transplants from HLA-matched related
donors, a number of other variables have been associated with an
increased incidence of acute GVHD. These include diagnosis,
recipient-donor sex mismatch, recipient age, female donor-male
recipient pair, alloimmunized and/or parous donor, increased dose of
total body irradiation (TBI), lower intensity of GVHD prophylaxis, and
viral seropositivity of recipient or donor.19-24 Herein, we
have investigated whether such variables are also risk factors for GVHD
after allogeneic blood stem cell transplantation.
| |
PATIENTS AND METHODS |
Patients.
Over a consecutive 44-month period, 160 adults received a myeloablative
preparative regimen and an unmanipulated blood stem cell graft from an
HLA-matched related donor. Patient characteristics are shown in
Table 1. All patients had hematologic
malignancies or solid tumors. Details of the peritransplant care and
administration of the preparative regimens have been described
previously.4,9,25-28 "Minitransplant" recipients and
recipients of T-cell-depleted blood stem cell transplants were not
included. Written informed consent was obtained from each patient, and
all protocols were approved by the Institutional Review Board of the
M.D. Anderson Cancer Center (Houston, TX).
Donors and blood stem cell collection.
Donor characteristics are shown in Table 2.
Details of filgrastim administration and blood stem cell collection
have been published.29 The target CD34+ cell
dose was 4 × 106/kg, but the actual cell
dose infused depended on the result of apheresis and processing. Blood
stem cell collections were assessed for CD34+,
CD3+, and CD56+ cells by flow cytometry on the
day of collection before cryopreservation.29 The absolute
number of a particular subset in the apheresis component was calculated
by multiplying the ungated percentage of that subset of cells times the
total number of cells in the component. On the day of transplantation,
the component was thawed and, in some cases, washed before infusion. An
aliquot of the infusion was used to determine the number of cells
infused. The absolute numbers of CD34+, CD3+,
and CD56+ cells infused were calculated by multiplying the
percentage of cells recovered after thawing and processing times the
absolute number of the subset in the cryopreserved component. The
median recovery of total nucleated cells was 82% (range, 45% to
100%). Characteristics of the blood stem cell grafts are summarized in Table 2. There was a weak association between CD34+ and
CD3+ or total nucleated cell dose (Spearman correlation
coefficient 0.26 and 0.39, respectively).
GVHD prophylaxis, monitoring, and grading.
Patients received one of three GVHD prophylaxis regimens depending on
the standard at the time of transplantation or the requirement of the
transplant protocol. Prophylaxis consisted of cyclosporine (CSA) and
methylprednisolone (MP), tacrolimus (FK506) and MP, or FK506 and
micromethotrexate (MTX). CSA was administered at 3 mg/kg/day IV
continuous infusion from day  2, and doses were adjusted to maintain whole blood steady state or trough levels at 250 ng/mL to 350 ng/mL by radioimmunoassay (RIA) for parent drug. FK506 was
administered at 0.03 mg/kg/day IV by continuous infusion from day
2, and doses were adjusted to maintain whole blood steady state
or trough levels at 5 to 15 ng/mL by IMx assay. After
engraftment when the patient was able to eat, CSA or FK506 was
converted to oral, continued through day 180, and tapered off
thereafter. MTX was administered at 5 mg/m2 IV on days 1, 3, and 6. MP was administered at 1.0 mg/kg/day from days 5 to 28 with a
taper thereafter. Patients were observed prospectively for development
of acute GVHD. The diagnosis of GVHD was based on clinical evidence
with histologic confirmation,30 and GVHD was graded
according to the consensus criteria.31
Statistical considerations.
Minimum follow-up at the time of analysis was 180 days after
transplantation. Estimates of the incidence of GVHD and
treatment-related mortality were calculated by the method of Kaplan and
Meier.32 Cause-specific failure rates for GVHD were also
computed,33 and these were nearly identical to Kaplan-Meier
estimates. Potential prognostic factors are listed in Tables
3 and 4. In considering the
association of GVHD rates with continuously measured covariates, patients were grouped approximately into quartiles based on covariate values (age, log cell dose). Comparisons of categorical data were by
chi-square test, and associations of factors with GVHD rates were
analyzed using log-rank tests and proportional hazards regression modeling.34 In the case of CD34+ cell dose, a
graphical method based on residuals from a proportional hazards
model35 was used to further evaluate the association.
| |
RESULTS |
Incidence of acute GVHD.
Forty-eight patients developed grades 2 to 4 GVHD for a cumulative
incidence of 31% (95% CI, 23% to 39%). Twenty-one patients developed grades 3 to 4 GVHD for a cumulative incidence of 14% (95%
CI, 8% to 20%).
Risk factors for acute GVHD.
Patient and donor demographics as well as characteristics of the
grafts were evaluated as potential risk factors for grades 2 to 4 and
grades 3 to 4 GVHD. Higher rates of grades 2 to 4 GVHD occurred in
patients who were older or who had solid tumors, but GVHD prophylaxis
regimen was the only demographic factor identified as statistically
significant (Table 3). Use of TBI, donor sex, patient-donor sex
mismatch, donor parity, donor alloimmunization, and cytomegalovirus
(CMV)-seronegativity had no correlation with the risk of grades 2 to 4 GVHD. No demographic factor or graft characteristic correlated
significantly with grades 3 to 4 GVHD, although trends generally
corresponded to findings for grades 2 to 4 GVHD (Tables 3 and 4).
There was a trend for increasing rates of grades 2 to 4 GVHD with
increasing numbers of total nucleated cells, CD34+ cells,
CD3+ cells, or CD56+ cells transplanted, but
CD34+ cell dose was the only graft characteristic that
correlated significantly with grades 2 to 4 GVHD. The rate of GVHD
remained fairly stable with increasing numbers of CD34+
cells transfused except at the highest quartile (Table 4). The correlation between CD34+ cell dose and GVHD risk was
verified in a plot of regression residuals,35 which
suggested a sharp increase in risk of GVHD in a range of 6.3 to 10.0 × 106 CD34+ cells/kg with constant risks
both above and below that range. A cutpoint of 8 × 106 CD34+ cells/kg was selected for further
analysis, because it fell at approximately the midpoint of this range.
A proportional hazards model for grades 2 to 4 acute GHVD was fitted
including the two indicator covariates (GVHD prophylaxis and
CD34+ cell dose), the interaction factor (GVHD prophylaxis
by CD34+ cell dose), age (years), and diagnosis
(hematologic disorder or solid tumor). Use of CSA and a
CD34+ cell dose greater than 8 × 106
CD34+ cells/kg remained independent risk factors
(Table 5).
Correlation between risk factors and outcomes.
Estimates of GVHD rates suggested that FK506 provided better
prophylaxis than CSA for those patients transplanted with less than 8 × 106 CD34+ cell/kg (P = .03);
the rate of grades 2 to 4 GVHD was 39% (95% CI, 21% to 57%) for the
32 patients who received CSA and 18% (95% CI, 10% to 26%) for the
85 patients who received FK506 (Fig 1A). Rates of grades 2 to 4 GVHD were higher (52%, 95% CI, 37% to 67%) for patients transplanted with  8 × 106
CD34+ cell/kg and were similar for all GVHD regimens (49%
to 56%) (Fig 1B).
View larger version (26K):
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| Fig 1.
Incidence of grades 2 to 4 GVHD after transplantation of
less than 8 × 106 CD34+ cells/kg (A) or
greater than 8 × 106 CD34+ cells/kg (B)
using CSA/MP (solid line), FK506/MP (dashed line), or FK506/MTX (dotted
line) as GVHD prophylaxis.
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Of the 48 patients who developed grades 2 to 4 GVHD, 21 (44%) had skin
involvement alone, 37 (77%) had skin with or without visceral GVHD, 9 (19%) had liver involvement, and 26 (54%) had gut involvement. The
distribution of organ involvement did not differ significantly by GVHD
prophylaxis or CD34+cell dose group
(Table 6).
For all patients, treatment-related mortality was 30% (95% CI, 23%
to 37%) at day 180 posttransplant. The day-180 treatment-related mortality was 42% (95% CI, 25% to 59%) for patients on CSA who received the low CD34+ cell dose, 24% (95% CI, 15% to
33%) for patients on FK506 who received the low CD34+ cell
dose, and 37% (95% CI, 22% to 52%) for those who received the high
CD34+ cell dose. The differences in treatment-related
mortality were not significant.
| |
DISCUSSION |
In our evaluation of risk factors for acute GVHD after allogeneic blood
stem cell transplantation, we found that the incidence of GVHD was
affected by the immunoprophylaxis regimen and by the CD34+
cell dose. The GVHD prophylaxis regimen has long been known to be an
important risk factor for GVHD,22,26 and recent studies have shown that FK506 is more potent than CSA for prevention of acute
GVHD after allogeneic marrow transplantation,36,37 so our
results for GVHD prophylaxis were not unexpected. The correlation between CD34+ cell dose and risk of GVHD has not been noted
previously with allogeneic marrow transplantation, but the high
CD34+ cell doses as we have collected here from
filgrastim-mobilized donors are rarely achieved in a single marrow
harvest,4,10,12 so such an association would probably not
be identified easily with marrow transplantation.
Of the demographic descriptors evaluated, both we here and Schmitz et
al15 noted a trend for increasing risk of acute GVHD with
increasing age of patient, but it was not significant in either
analysis. None of the other patient-donor variables was found to be
significant. This may be due to the fact that donor selection criteria
at our center already takes into account known characteristics that
increase GVHD risk, potentially biasing the analysis against detection
of significance. With improvement in GVHD prophylaxis, however, others
have also reported that widely accepted demographic risk factors for
acute GVHD may no longer apply for HLA-identical marrow transplant
recipients.22,23
In nonrandomized comparisons, the incidence of grades 2 to 4 GVHD in
marrow transplant recipients did not vary when using MP or MTX with
CSA.38,39 Similarly, in our study of stem cell recipients,
when stratified by CD34+ cell dose, patients receiving
FK506 had the same risk of GVHD whether used in conjunction with MP or
MTX. Bensinger et al7 and Schmitz et al15 also
did not find a significant difference in the incidence of acute GVHD
comparing MP to MTX used with CSA after allogeneic stem cell
transplantation. However, the use of MP in GVHD prophylaxis regimens
has been associated with a higher risk of infection and
treatment-related mortality after marrow transplantation,17,38,40 so MTX may be the preferred second drug to use in combination regimens.
In large multivariate analyses, total nucleated cell dose has not been
identified as an independent risk factor for GVHD after HLA-identical
marrow transplantation.19,20,23,24 In one early study,
nucleated cell dose was associated with an increased survival, but this
was related to a reduction in the incidence of interstitial pneumonitis
and early treatment-related complications other than GVHD.41 We also found that nucleated cell dose did not
affect acute GVHD incidence in the allogeneic blood stem cell recipients.
For our patients, there was no significant correlation between the
incidence of acute GVHD and CD3+ or CD56+ cell
dose. The relative lack of severe GVHD despite the high numbers of
lymphocytes infused into these patients has been ascribed to a
reduction in function of T and NK cells in filgrastim-treated normal
donors.42,43 Impaired functions of T cells from blood stem
cell donors measured in vitro include a decrease in alloantigen and
mitogen proliferative responses, and a lower induction of the CD28
response complex by TCR stimulation.42,44,45 The hyporesponsiveness is thought to be mediated by interleukin-10 (IL-10)
produced by monocytes.46 This observation may be an in
vitro epiphenomenon, however, because high IL-10 levels in vivo have
been associated with increased transplant-related
complications,47,48 and sorted CD4+ cells from
filgrastim-treated normal donors are not consistently hyporesponsive.42 Others have reported that filgrastim
treatment results in a Th2 polarization in vivo,49-51 and
in an animal model, this correlated with a reduction in the incidence
of acute GVHD,52 but the mechanism by which filgrastim
induces the Th2 polarization is unknown.
The association between CD34+ cell dose and GVHD risk has
not been reported previously, although CSA-based prophylaxis has been
used for most other allogeneic blood stem cell transplant recipients,
and even in our study population, the difference in risk of acute GVHD
by CD34+ cell dose is minimal for the CSA subgroup alone.
The truly striking difference occurs in the FK506 subgroup, in which
the risk of GVHD was lower than with CSA only with the low
C34+ cell dose. The lack of FK506-responsiveness at high
CD34+ cell doses suggests that GVHD in this circumstance
may not be mediated totally by lymphocytes. Instead, GVHD at high
CD34+ cell doses may be exacerbated by cytokines released
by the markedly expanding myeloid population at the time of
engraftment. In support of this hypothesis, Hägglund et
al23 reported that early engraftment independently
predicted development of acute GVHD after allogeneic marrow
transplantation. Tumor necrosis factor  (TNF) has been proposed
as the cytokine responsible for this effect,53,54 and high
levels of TNF have been found in peripheral blood monocytes at the
time of engraftment.55 Cytokine release from myeloid cells
would clearly not be ameliorated by FK506 or CSA.
The ultimate objective of a risk factor analysis is to identify the
important variables that may improve outcome when controlled in
practice. We have found that the risk of moderate-to-severe acute GVHD
after HLA-identical blood stem cell transplantation is increased by
high CD34+ cells doses and use of CSA rather than FK506.
Although there was a trend for differences in treatment-related
mortality when patients were grouped by CD34+ cell dose and
GVHD prophylaxis, the differences did not achieve statistical
significance, albeit the power of the analysis may have been limited by
the small number of patients studied. Nevertheless, given the
association of increased risk of acute GVHD with CD34+ cell
dose and immunoprophylaxis regimen, these factors should be taken into
consideration in any analysis of GVHD after allogeneic blood stem cell
transplantation and in the design of new treatment protocols. We
caution, however, that the critical cutpoint for CD34+ cell
dose may differ between institutions due to the variability in the
techniques for measuring CD34+ cell numbers.
| |
FOOTNOTES |
Submitted October 9, 1998; accepted April 11, 1999.
Supported in part by The Tony Anderson Fund, Fujisawa USA, and the
Cancer Center Core Grant (No. CA-16672) from the National Institutes of Health.
The publication costs of this
article were defrayed in part by
page charge payment. This article
must therefore be hereby marked
"advertisement"
in accordance with 18 U.S.C. section
1734 solely to indicate this fact.
Address correspondence to Donna Przepiorka, MD, PhD, Baylor College of
Medicine, Center for Cell and Gene Therapy, 6565 Fannin St, M964,
Houston, TX 77030; email: donnap{at}bcm.tmc.edu.
| |
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ABSTRACT
INTRODUCTION