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Blood, Vol. 92 No. 5 (September 1), 1998:
pp. 1832-1836
Allogeneic Bone Marrow Transplantation for Low-Grade Lymphoma
By
Koen van Besien,
Kathleen A. Sobocinski,
Philip A. Rowlings,
Sandra C. Murphy,
James O. Armitage,
Michael R. Bishop,
Ok-kyong Chaekal,
Robert Peter Gale,
John P. Klein,
Hillard M. Lazarus,
Philip
L. McCarthy Jr,
John M.M. Raemaekers,
Josy Reiffers,
Gordon L. Phillips,
Anton V.M.B. Schattenberg,
Leo F. Verdonck,
Julie M. Vose, and
Mary M. Horowitz
From the Joint Lymphoma Working Committee of the International Bone
Marrow Transplant Registry and the Autologous Blood and Marrow
Transplant Registry, Health Policy Institute, Medical College of
Wisconsin, Milwaukee; the Section of Hematology/Oncology, University of
Illinois, Chicago; the Department of Internal Medicine, University of
Nebraska Medical Center, Omaha; the Division of Bone Marrow and Stem
Cell Transplantation, Salick Health Care, Inc, Los Angeles, CA; the
Department of Medicine, Ireland Cancer Center, University Hospitals of
Cleveland, Case Western Reserve University, Cleveland, OH; the
Department of Medicine, Roswell Park Cancer Institute, Buffalo, NY; the
Division of Hematology, University Hospital St Radboud, Nijmegen, The
Netherlands; Unite de Greffe, Hospital Haut-Leveque, Pessac, France;
Division of Bone Marrow Transplantation, Markey Cancer Center,
University of Kentucky, Lexington, KY; and the Haematology Department,
University Hospital Utrecht, Utrecht, The Netherlands.
 |
ABSTRACT |
Advanced low-grade lymphomas are usually incurable with
conventional-dose chemotherapy. It is uncertain whether
cures are possible with high-dose therapy and bone marrow transplant
from a human leukocyte antigen (HLA)-identical sibling. We sought to determine the outcome of HLA-identical sibling bone marrow transplants in advanced low-grade lymphoma in an observational study of 113 patients conducted at 50 centers participating in the International Bone Marrow Transplant Registry (IBMTR). The median patient age was 38 years (range, 15 to 61). Eighty percent had stage IV disease at the
time of transplantation. The median number of prior chemotherapy regimens was two (range, 0 to 5). Thirty-eight percent had refractory disease and 29% a Karnofsky performance score (KPS) less than 80%.
All patients underwent allogeneic bone marrow transplantation from a
HLA-identical sibling donor. The conditioning regimen included total-body irradiation (TBI) in 82% of patients; cyclosporine was used
for graft-versus-host disease prophylaxis in 74%. Survival, disease-free survival, recurrence rate, treatment-related mortality, and causes of death were determined. Three-year probabilities of
recurrence, survival, and disease-free survival were 16% (95% confidence interval [CI], 9% to 27%), 49% (95% CI, 39% to 60%), and 49% (95% CI, 39% to 59%), respectively. Higher survival was associated with pretransplant KPS  90%, chemotherapy-sensitive disease, use of a TBI-containing conditioning regimen, and age less
than 40 years. We conclude that high-dose therapy followed by
transplantation from a HLA-identical sibling leads to prolonged survival in some patients with advanced low-grade lymphoma. Most mortality is treatment-related, and recurrences are rare.
© 1998 by The American Society of Hematology.
| |
INTRODUCTION |
ADVANCED-GRADE LYMPHOMAS are
relatively indolent, but are incurable with conventional
treatments.1-4 The median survival duration from diagnosis
is 7 to 9 years. High-dose therapy and a blood cell or bone marrow
autotransplant reportedly results in sustained remission in some
patients.5-9 Recurrences are common and there is concern
about posttransplant myelodysplastic syndromes.5,10-12 Prolonged remissions have been reported in small numbers of patients treated with allogeneic bone marrow transplantation.13-19
We studied 113 patients with advanced low-grade lymphoma who received a
bone marrow transplant from a human leukocyte antigen (HLA)-identical sibling.
| |
PATIENTS AND METHODS |
Patients.
We reviewed all HLA-identical sibling transplants for low-grade
lymphoma performed between 1984 and 1995 and reported to the International Bone Marrow Transplant Registry (IBMTR) by 50 centers worldwide. The study included 113 patients with a diagnosis of low-grade lymphoma at diagnosis and at the time of transplant. This
included patients with diffuse well-differentiated lymphocytic lymphoma
(Working Formulation group A), follicular small cleaved-cell lymphoma
(Working Formulation group B), and follicular mixed-cell lymphoma
(Working Formulation group C).20 Patients initially diagnosed with low-grade lymphoma, but whose disease transformed to
intermediate-grade or high-grade lymphoma before transplantation, were
excluded.
Pathology reports confirming the diagnosis of low-grade lymphoma were
reviewed by Koen van Besien. Discrepancies in nomenclature among
centers were resolved using the recent publication on the Revised
European-American Lymphoma (REAL) classification.21
IBMTR.
The IBMTR is a voluntary working group of more than 300 transplant
teams worldwide that contribute detailed data on their allogeneic bone
marrow transplants to the Statistical Center at the Medical College of
Wisconsin. Participants are required to report all consecutive
transplants; compliance is monitored by on-site audits. Approximately
two thirds of all active transplant centers report their data to the
IBMTR. The IBMTR database includes 40% to 45% of all allogeneic
transplant recipients since 1970. Patients are monitored
longitudinally. Computerized error checks, physician review of
submitted data, and on-site audits of participating centers ensure data
quality.
Statistical methods.
Primary outcomes were survival, disease-free survival (survival without
lymphoma posttransplant), recurrence, and treatment-related mortality
(nonrelapse death). For treatment-related mortality, patients were
considered treatment failures at the time of death from any cause in
the first 28 days posttransplant or at time of death in continuous
remission for those surviving more than 28 days posttransplant;
patients with recurrent lymphoma were censored at the time of relapse
and those alive in remission were censored at the last follow-up
evaluation. For disease-free survival, patients were considered
treatment failures at the time of relapse or death from any cause;
patients alive in continuous remission were censored at the last
follow-up evaluation. Patients who never achieved remission were
analyzed as having recurrent lymphoma on day 28.
Other outcomes examined were acute graft-versus-host disease (GVHD),
chronic GVHD, and survival. Acute GVHD was defined as moderate to
severe (grade II to IV) disease using established criteria; patients
surviving more than 21 days with evidence of engraftment were
considered at risk.22 Chronic GVHD was determined by
clinical criteria in patients surviving more than 90 days with evidence
of engraftment.23
Probabilities of outcomes were calculated using the Kaplan-Meier
product-limit estimate and expressed as probabilities with a 95%
confidence interval (CI) computed using the arcsine-square root
transformation. Patient-, disease-, and transplant-related variables
were studied for associations with survival. Univariate comparisons
used the log-rank test. Multivariate analyses used Cox proportional
hazards regression with stepwise forward variable selection. As
disease-free survival was nearly identical to survival, multivariate
analyses were performed only for survival. The incidence of lymphoma
relapse was too low to allow a multivariate analysis of this parameter.
| |
RESULTS |
Patient characteristics.
Patient-, disease-, and transplant-related characteristics are listed
in Table 1.
Fifty-eight percent of patients were male. The median age was 38 years
(range, 15 to 61). Twenty-nine percent had a Karnofsky performance
score (KPS) less than 90%.
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Table 1.
Patient-, Disease-, and Transplant-Related
Characteristics of 113 Recipients of HLA-Identical Sibling Bone
Marrow Transplants for Low-Grade Non-Hodgkin's Lymphoma Reported to
the IBMTR by 50 Centers Worldwide
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Eighteen percent of patients had small lymphocytic lymphoma, 46% had
follicular small cleaved-cell lymphoma, and 36% had follicular mixed-cell lymphoma. Eighty-one percent were diagnosed with stage IV
disease, most commonly due to bone marrow involvement. Only 14% were
in complete remission at transplant. Seventy-one percent had stage IV
disease at transplant, despite a median of two prior chemotherapy
regimens. Diverse chemotherapy regimens were used pretransplant; 37%
of patients were felt to have chemotherapy-resistant lymphoma (ie, they
had achieved less than a partial remission to the last chemotherapy
regimen administered before transplant).
Eighty-four percent of the transplants were performed after 1990. The
median interval from diagnosis to transplant was 24 months (range, 5 to
130). The pretransplant conditioning regimen included total-body
irradiation (TBI) in 82% of cases. Among the 20 patients (18%) not
receiving TBI for conditioning regimens, only three had received prior
radiation. Twenty-two percent of patients received T-cell-depleted
transplants.
Outcomes.
Outcomes are summarized in Table 2. The
median follow-up duration of surviving patients was 25 months (range, 4 to 95). Three-year probabilities of recurrence and treatment-related
mortality were 16% (95% CI, 9% to 27%) and 40% (95% CI, 30% to
50%), respectively (Fig
1). Three-year
probabilities of survival and disease-free survival were both 49%
(95% CI, 39% to 59%) (Fig 2). Among 33 patients monitored for more than 2 years after transplantation, only
one relapse was documented.
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| Fig 1.
Probability of relapse and treatment-related mortality
after HLA-identical sibling bone marrow transplant for low-grade
non-Hodgkin's lymphoma.
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View larger version (10K):
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[in a new window]
| Fig 2.
Probability of survival and disease-free survival after
HLA-identical sibling bone marrow transplant for low-grade
non-Hodgkin's lymphoma.
|
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In multivariate analysis, KPS, chemotherapy-resistance, conditioning
regimen, and age significantly predicted survival (Table 3).
View this table:
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Table 3.
Factors Significantly Associated With Survival in
Multivariate Analysis of 113 Recipients of HLA-Identical Sibling Bone
Marrow Transplants for Low-Grade Non-Hodgkin's Lymphoma Reported to
the IBMTR by 50 Centers Worldwide
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Fifty-one patients died; causes of death are summarized in Table
4. Pulmonary complications were most
common, including interstitial pneumonitis (n = 7), acute respiratory
distress syndrome (n = 5), and pulmonary hemorrhage (n = 1). Two
patients died of acute GVHD and three of chronic GVHD.
View this table:
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[in a new window]
|
Table 4.
Causes of Death of 51 Recipients of HLA-Identical
Sibling Bone Marrow Transplants for Low-Grade Non-Hodgkin's
Lymphoma
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| |
DISCUSSION |
This report evaluates the outcome of HLA-identical sibling bone marrow
transplants for advanced low-grade lymphomas among centers reporting
consecutive patients to the IBMTR. Not surprisingly, the data indicate
that transplants are mainly offered to younger patients with advanced
disease. Most patients in this study received extensive prior therapy.
Many had chemotherapy-resistant disease and low performance scores.
Most were not candidates for autotransplants because of extensive bone
marrow involvement. Characteristics of these patients and their
outcomes are consistent with those reported in three smaller
single-institution series.13,18,19 Only 22 of the patients
in this study were included in those series. Given the unfavorable
characteristics of this population, the observed lymphoma-free and
overall survival rates of 49% and the recurrence rate of only 16% are
encouraging.
Interestingly, there was only one recurrence among 33 patients
monitored for more than 2 years. This seems lower than has been
reported for autotransplants and is consistent with other recent
reports.24,25 The low recurrence rate, if true, may be due
to graft-versus-lymphoma effects as suggested by some,26-28 or, alternatively, to lack of tumor contamination of the allogeneic graft.29,30 Our results should be interpreted cautiously.
Although we tried to obtain current information on all patients,
follow-up methods and accuracy of restaging varies considerably among
reporting centers; failure to detect early recurrences may at least
partially explain the results.
Multivariate analyses identified poor KPS and chemotherapy-resistance
as adverse prognostic factors. Better patient selection and earlier
transplants could improve outcome. Use of TBI for pretransplant
conditioning was also associated with better survival. Radiation is
effective in low-grade lymphoma and is frequently used in
autotransplant conditioning regimens. However, in a recent analysis of
autotransplants for low-grade lymphoma, there was a trend
(P = .09 in multivariate analysis) for poorer survival among
patients receiving TBI.31 Only 18% of the patients in this
series received non-TBI regimens and it is possible that such patients
differed for unknown but important (latent) covariates.
The 3-year probability of treatment-related mortality was 40% (95%
CI, 30% to 50%). Most treatment-related deaths were from pulmonary
complications, similar to observations in allogeneic transplants for
Hodgkin's disease.32 This high incidence of pulmonary
complications may be related to the use of busulfan or TBI. Chronic
GVHD, though common, was a rare cause of death.
In conclusion, this analysis establishes the potential of allogeneic
transplantation to achieve survival in patients with advanced low-grade
lymphoma. Our data provide a rationale for prospective studies of
allogeneic transplants earlier in the course of the disease.
| |
FOOTNOTES |
Submitted March 10, 1998;
accepted May 1, 1998.
See Appendix for support data.
Address reprint requests to Mary M. Horowitz, MD, MS, IBMTR/ABMTR
Statistical Center, Medical College of Wisconsin, PO Box 26509, 8701 Watertown Plank Rd, Milwaukee, WI 53226.
The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" is accordance with 18 U.S.C. section 1734 solely to indicate this fact.
| |
ACKNOWLEDGMENT |
The authors thank the coordinators and physicians of the participating
teams who provided us with additional data on these patients.
| |
APPENDIX |
Supported by Public Health Service Grant No. P01-CA-40053
from the National Cancer Institute, the National Institute of Allergy and Infectious Diseases, and the National Heart, Lung and Blood Institute, of the US Department of Health and Human Services; and
grants from Alpha Therapeutic Corporation; Amgen, Inc; Anonymous; Astra
Pharmaceutical; Baxter Healthcare Corp; Bayer Corp; Biogen; Blue Cross
and Blue Shield Association; Lynde and Harry Bradley Foundation;
Bristol-Myers Squibb Co; Frank G. Brotz Family Foundation; CellPro,
Inc; Centeon; Center for Advanced Studies in Leukemia; Chimeric
Therapies; Chiron Therapeutics; Charles E. Culpeper Foundation; Eleanor
Naylor Dana Charitable Trust; Eppley Foundation for Research; Genentech, Inc; Glaxo Wellcome Co; Hoechst Marion Roussel, Inc; ICN
Pharmaceuticals; Immunex Corp; Janssen Pharmaceutica; Kettering Family
Foundation; Kirin Brewery Co; Robert J. Kleberg, Jr and Helen C. Kleberg Foundation; Herbert H. Kohl Charities, Inc; Eli Lilly Co
Foundation; Nada and Herbert P. Mahler Charities; MDS Nordian; Milstein
Family Foundation; Milwaukee Foundation/Elsa Schoeneich Research Fund;
Samuel Roberts Noble Foundation; Novartis Pharmaceuticals; Ortho
Biotech Corp; John Oster Family Foundation; Elsa U. Pardee Foundation;
Jane and Lloyd Pettit Foundation; Alirio Pfiffer Bone Marrow Transplant
Support Association; Pfizer, Inc; Pharmacia and Upjohn; Principal
Mutual Life Insurance Co; RGK Foundation; Rockwell-Automation
Allen-Bradley Co; Schering-Plough International; Walter Schroeder
Foundation; Searle; Stackner Family Foundation; Starr Foundation; Joan
and Jack Stein Charities; and Wyeth-Ayerst
Laboratories.
| |
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Abstract
Introduction
Abstract