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Blood, Vol. 92 No. 10 (November 15), 1998:
pp. 3515-3520
RAPID COMMUNICATION
Optimizing Outcome After Unrelated Marrow Transplantation by
Comprehensive Matching of HLA Class I and II Alleles in the Donor and
Recipient
By
Effie W. Petersdorf,
Theodore A. Gooley,
Claudio Anasetti,
Paul J. Martin,
Anajane G. Smith,
Eric M. Mickelson,
Ann E. Woolfrey, and
John A. Hansen
From the Division of Clinical Research, Fred Hutchinson Cancer
Research Center and the University of Washington School of Medicine,
Seattle, WA.
 |
ABSTRACT |
In unrelated marrow transplantation, the benefit of matching class
II HLA-DRB1 and DQB1 alleles of the donor and recipient is well
documented. Little is known about the clinical relevance of matching
for class I HLA-A, B, and C alleles. We used DNA-amplification methods
to identify the HLA-A, B, and C alleles of 300 patients and their
donors. The incidence of graft failure was correlated with multiple
class I mismatching in the donor. The risk of grades III-IV acute
graft-versus-host disease was highest with class II mismatching in the
recipient. Mismatching for a single class I or class II allele had no
effect on survival, but mortality was increased by mismatching for more
than one class I allele and by simultaneous mismatching for class I and
class II alleles. We conclude that matching HLA class I and class II
alleles of the donor and recipient can improve outcome after unrelated
marrow transplantation.
© 1998 by The American Society of Hematology.
| |
INTRODUCTION |
MARROW TRANSPLANTATION from an
HLA-matched sibling has been well established as a curative therapy for
a variety of malignant and nonmalignant diseases.1-6 The
establishment of volunteer donor registries has facilitated
transplantation from unrelated donors for patients who lack a suitably
matched related donor.7-13 Current standards for HLA typing
include serological methods for class I HLA-A, HLA-B, and HLA-C
antigens and DNA-based typing for class II HLA-DRB1 and HLA-DQB1
alleles. Molecular analysis has disclosed that the same serologically
defined class I antigen can be encoded by an entire family of alleles.
Among the 24 HLA-A, 50 HLA-B, and 11 HLA-C antigens, more than 86 HLA-A, 185 HLA-B, and 45 HLA-C alleles have been
described.14 With sibling pairs, there is no need to
identify the HLA class I and II alleles of the donor and recipient
because they have inherited identical HLA haplotypes. With unrelated
pairs, typing of HLA alleles is needed to evaluate genetic disparity,
and matching of HLA alleles provides the closest possible approximation
of the compatibility that can be achieved with a related donor.
Donor-recipient identity for HLA-DRB1 and DQB1 alleles reduces the risk
of acute graft-versus-host disease (GVHD) and improves survival after
unrelated marrow transplantation.13,15 However, with
matching for serologically defined HLA-A and B antigens and for
HLA-DRB1 and DQB1 alleles, the risks of acute GVHD, graft failure, and
mortality remain higher with unrelated donors than with HLA-identical
sibling donors. In this study, we tested the hypothesis that the
increased risk of complications after unrelated marrow transplantation
could be caused by mismatching for HLA-A, B, and C alleles of the donor
and recipient. We found that outcome after unrelated donor
transplantation can be optimized by matching the HLA-A, B, C, DRB1, and
DQB1 alleles of the donor and recipient. However, mismatching for a
single allele was well-tolerated. We also present evidence that class I
and class II antigens have biologically different functions in clinical
marrow transplantation. Whereas class I determinants govern graft
acceptance, class II determinants play a role in GVHD.
| |
MATERIALS AND METHODS |
Study population.
Between May 1985 and March 1998, 439 patients received an unrelated
marrow transplant for treatment of chronic myeloid leukemia (CML) in chronic phase (CP), accelerated phase (AP), or
blast phase in remission. In the interest of decreasing the
heterogeneity of factors associated with the risk of acute GVHD, we
restricted the study to patients who received T-cell-replete
marrow16 with methotrexate and cyclosporine as GVHD
prophylaxis17 (n = 402). Samples were sufficient for
complete retrospective typing of HLA-A, B, and C alleles in 300 of the
402 pairs. The 102 pairs lacking DNA were similar to the 300 pairs with
respect to demographic and clinical outcome.
Histocompatibility testing and donor selection criteria.
Before transplantation, HLA-A and HLA-B antigens of the donor and
recipient were typed by the standard two-stage National Institutes of
Health complement-dependent microcytotoxicity test, and HLA-DR and
HLA-DQ antigens were typed by using Dynabead-purified B cells in a
microcytotoxicity assay. Before 1991, donor selection was based on
matching for HLA-A, B, DR, and Dw.18 A single HLA-Dw mismatch with serological matching for HLA-DR or a single HLA-A or
HLA-B mismatch within a serological cross-reactive antigen group was
allowed for patients younger than 36 years of age if an HLA-A, B, DR,
Dw-matched donor could not be identified. After 1991, HLA-DRB1 allele
typing19 superceded Dw typing, and a single HLA-DRB1 allele
mismatch was allowed for patients younger than 36 years of age if an
HLA-DRB1-matched donor could not be identified. In 1992, prospective
HLA-DQB1 allele typing15 was introduced, and
HLA-DQB1-matched donors were selected in preference to
HLA-DQB1-mismatched donors. Beginning in 1996, HLA-C serological
typing was used to select HLA-C-matched donors in preference to
HLA-C-mismatched donors.20 Among the 300 pairs in this
study, 20 were mismatched at HLA-A and 10 were mismatched at HLA-B by
serologic testing.
HLA-A, B, and C alleles were sequenced by using direct automated
fluorescence methods.20 When improved methods for
sequencing became available, HLA-A exons 1-5 were amplified with
5.IN/3.IN21 or A1/A2 primers (Lifecodes, Inc, Stamford,
CT), and introns 1-3 of HLA-C were amplified with primer pair C1/C2
(Lifecodes, Inc). Amplified HLA-A and C templates were sequenced by
using dye-labeled primers21,22 (HLA-A Sequencing Based
Typing Kit; Applied Biosytems, Inc, Foster City, CA). In 133 typings,
class I alleles were assigned by using oligonucleotide probe
hybridization reagents (Lifecodes, Inc). Because most unrelated
transplant pairs are HLA-DPB1 mismatched,23,24 no
consideration was given to HLA-DPB1 matching in this study.
Transplant procedure.
All patients were prepared for transplantation with intravenous
cyclophosphamide (60 mg/kg recipient body weight) administered on each
of 2 successive days followed by total body irradiation (1,200 to 1,575 cGy in 6 to 12 fractions) from dual opposed 60Co sources.
Prophylaxis for CMV, fungal, and Pneumocystis carinii infection
was administered as described.25,26 All protocols were
reviewed and approved by the Institutional Review Board of the Fred
Hutchinson Cancer Research Center. Engraftment and the severity of
acute GVHD were assessed according to criteria previously described.1,20
Statistical methods.
The primary end point of this study was survival after transplantation.
Grades III-IV acute GVHD and graft failure were secondary endpoints.
Associations between type of donor and the hazard appropriate for
survival and GVHD were examined by fitting multivariable proportional hazards regression models. Logistic regression was used to examine the
probability of graft failure. Variables shown from previous studies to
be associated with these end points were included in the multivariable
models.13,20,27 Because the intention of this study was to
assess associations between HLA allele matching and clinical outcome,
parameters for age, gender, pretransplant therapy, stage of disease,
body weight, and time interval from diagnosis to transplant are not
displayed. Associations between these variables and clinical outcome
have been reported elsewhere.
For analysis of each end point, donor and recipient pairs were
categorized as follows: allele match at HLA-A, B, C, DRB1, and DQB1;
mismatch involving only one class I allele; mismatch involving two or
more class I alleles; mismatch involving only one class II allele;
mismatch involving two or more class II alleles; and mismatch involving
at least one class I allele and at least one class II allele. For
analysis of GVHD, mismatching was defined as the presence of recipient
alleles not shared by the donor (recipient disparity). For analysis of
graft failure, mismatching was defined as the presence of donor alleles
not shared by the recipient (donor disparity). For analysis of
survival, mismatching included either type of disparity. The
probability of GVHD was estimated as the cumulative
incidence,28 with death, relapse, and graft failure without
GVHD considered as competing risks. Kaplan-Meier estimates were used to
describe survival.29 All P values resulting from regression models were derived from the Wald test and are two-sided. No
adjustments were made for multiple comparisons.
| |
RESULTS |
HLA matching.
Of the 300 pairs in the study, 142 were matched for HLA-A, B, C, DRB1,
DQB1 alleles. Among the 158 mismatched pairs, 83 were mismatched at
only one HLA locus (21 HLA-A, 11 HLA-B, 26 HLA-C, 9 HLA-DRB1, and 16 HLA-DQB1) and 75 were mismatched at two or more loci. Eighty-three
percent of the transplants were performed from a Caucasian donor for a
Caucasian patient; the patient and donor were of the same race in 85%
of the transplants.
Graft failure.
Graft failure occurred most frequently with donors who were mismatched
for more than one class I allele (Table 1).
Graft failure did not occur with donors who were mismatched only at HLA-DRB1, DQB1, or both. After adjusting for marrow cell dose, the odds
of graft failure was much higher with donors who were mismatched only
for class I alleles than with matched donors (odds ratio, 10.5; 95%
confidence interval, 2.2 to 49.8; P = .003). The odds of graft
failure were also higher with donors who were mismatched both for class
I and class II alleles than with matched donors (odds ratio, 10.0; 95%
confidence interval, 1.7 to 58.4; P = .01). These results
indicate that graft failure was caused primarily by class I disparities
in the donor. We could not evaluate the role of individual class I
loci, because the number of patients with graft failure was too small.
Acute GVHD.
The risk of grades III-IV acute GVHD was influenced by the number and
class of mismatched alleles in the recipient
(Table 2 and
Fig 1). Recipients with a single class I
mismatch did not have an increased hazard of grades III-IV acute GVHD
compared with matched recipients. Those with multiple class I
mismatches appeared to have a higher hazard of severe GVHD than matched
recipients, but the difference was not statistically significant.
Recipients with both class I and class II mismatches had a
significantly increased hazard compared with matched recipients.
Recipients with a single class II mismatch also appeared to have a
higher hazard than matched recipients. Although this difference was not statistically significant, the trend was suggestive, especially considering the relatively small number of patients. With respect to
the development of grades III-IV acute GVHD, class II mismatches caused
more difficulty than class I mismatches.
Survival.
Patients with more than one class I mismatch and patients with both
class I and class II mismatches had significantly lower survival than
matched patients (Table 3 and
Fig 2). In contrast, the survival of
patients with a single class I or class II allele mismatch was similar
to that of matched patients. Three of the seven patients mismatched for
multiple class II alleles died before day 100. The other four remain
alive from 3 to 8 years after transplant. These data demonstrate that a
single class I or class II mismatch is well tolerated, but multiple
class I allele mismatches and simultaneous class I and class II
mismatches should be avoided.
View larger version (18K):
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| Fig 2.
Kaplan-Meier estimates of overall survival according to
donor or recipient disparity. Tick marks indicate patients alive at the
time of last contact. Some patients remain alive more than 8 years
after the transplant, but no deaths have occurred past this time.
|
|
| |
DISCUSSION |
The results of this study demonstrate that survival after
transplantation can be improved by matching HLA-A, B, C, DRB1, DQB1 alleles of the donor and recipient. The presence of multiple class I
disparities in the donor was associated with an increased risk of graft
failure, and the presence of class II disparities in the recipient was
associated with an increased risk of GVHD. Disparity for a single class
I or II allele did not appear to compromise survival. A parallel study
of allele matching in a transplant population has been examined by the
Japanese Marrow Donor Program.30
The presence of HLA class I disparity had important effects on the risk
of graft failure, especially when two or more class I mismatches were
present in the donor. The high risk of graft failure explains the
reduced survival observed in this group of patients. The assessment of
possible qualitative differences between class I loci must await a
larger transplant experience because the numbers of donors with a
single HLA-A, B, or C mismatch were too small for meaningful
comparisons (21 HLA-A, 11 HLA-B, and 26 HLA-C).
The differences between class I and class II disparity in conferring
risks of graft failure and acute GVHD reflect the distinct biologic
functions of class I molecules and class II molecules.31,32 Class I molecules present peptides derived primarily from endogenously synthesized proteins, and the responding T cells express CD8. Class II
molecules present peptides derived primarily from exogenously synthesized proteins, and the responding T cells express CD4. The
peptides that bind respectively to class I and class II molecules differ in length and sequence.33 HLA class I molecules are
further distinguished from class II molecules by their complex
interaction with natural killer (NK) cells.34
Although complete allele matching is desirable, the presence of a
single class I or II allele mismatch had little demonstrable effect on
survival. These results are encouraging particularly for Africans,
Asians, Hispanics, Native Americans, and other ethnic groups who have a
low probability of finding a fully matched donor.35 Increased registry size and recruitment of specific ethnic populations can only partially alleviate this problem. Allowance for a single class
I or II disparity offers access to marrow transplantation for patients
who lack an HLA-A, B, C, DRB1, DQB1 allele-matched donor.
During the past decade, clinical laboratories have focused efforts on
developing methods for prospective typing of HLA-DRB1 and DQB1 alleles
in selecting donors for unrelated marrow
transplantation.36,37 The results of our study provide
further clinical rationale for efforts to develop methods for routine
clinical typing of HLA class I alleles.38-42 The benefits
of prospective class I allele typing will depend on the ability to
identify optimally matched donors. Matching for HLA alleles may be more
feasible for patients with CML than for patients with acute leukemia
where progression of the disease might not allow an extended period of
time for finding a donor. For patients with CML, results of
transplantation are best when the time interval between diagnosis and
transplantation is minimized,13 and a delay in
transplantation introduced by a lengthy search for a donor could be
detrimental.
Two further questions remain to be answered. First, we confined our
current analysis to patients with CML, and the applicability of the
results to patients with other diseases is unknown. For example, graft
failure occurs very rarely in patients with acute leukemia and might
not be associated with class I disparity. Second, the importance of
matching for HLA-DPB1 alleles has not been defined. This question may
be more answerable when the effects of class I disparity are better
understood.
In unrelated marrow transplantation, efforts should be made to match
HLA-A, B, and C alleles as well as HLA-DRB1 and DQB1 alleles of the
donor and recipient. In patients with CML, the presence of a single HLA
class I or class II disparity is well tolerated, but multiple
disparities between the donor and recipient should be avoided wherever
possible.
| |
ACKNOWLEDGMENT |
The authors are indebted to Dr Ji Pei and Leigh Ann Guthrie for sample
procurement; Andrew Yamane, Mari Malkki, Mark Gatterman, and Brenda
Nisperos for technical assistance; Amy Mellon for collection of
clinical data; and Alison Sell for preparation of the manuscript.
| |
FOOTNOTES |
Submitted July 14, 1998;
accepted August 20, 1998.
Supported by Grants No. AI33484, CA18029, and CA72978 from the National
Institutes of Health and the Friends of Allison, Inc.
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 reprint requests to Effie W. Petersdorf, MD, Fred Hutchinson
Cancer Research Center, 1100 Fairview Ave N, PO Box 19024, Seattle, WA
98109-1024.
| |
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Top
Abstract
Introduction