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© 2003 American Society for Clinical Oncology Trends in Survival Rates After Allogeneic Hematopoietic Stem-Cell Transplantation for Acute and Chronic Leukemia by Ethnicity in the United States and Canada
From the International Bone Marrow Transplant Registry, Division of Biostatistics, Health Policy Institute, and Division of Neoplastic Diseases and Related Disorders, Department of Internal Medicine, Medical College of Wisconsin, Milwaukee, WI; Center for Outcomes and Policy Research, Dana-Farber Cancer Institute, Boston, MA; and Pediatric Blood and Marrow Transplant Program, University of Minnesota, Minneapolis, MN. Address reprint requests to Fausto R. Loberiza Jr, MD, MS, International Bone Marrow Transplant Registry, Medical College of Wisconsin, 8701 Watertown Plank Road, Milwaukee, WI 53226; e-mail: faustol{at}mcw.edu.
Purpose: Differences in survival among ethnic groups in the United States are reported in numerous diseases and treatment strategies. Whether survival after allogeneic hematopoietic stem-cell transplantation (HSCT) differs by ethnicity is uncertain. Patients and Methods: Patients (n = 6,443) receiving HLA-identical sibling HSCT for acute or chronic leukemia in the United States or Canada between 1985 and 1999 and reported to the International Bone Marrow Transplant Registry were included. The survival of recipients reported as white, black, Hispanic, or Asian was compared using Cox proportional hazards regression adjusting for other clinical factors. Three 5-year periods were studied to evaluate changes over time. Results: Hispanics compared with whites had lower 1-year (53% v 65%; P < .001) and 3-year adjusted survival rates (38% v 53%; P < .001) between 1995 and 1999, the most recent period studied. We failed to find significant differences in survival rates comparing whites with blacks or with Asians in any of the time periods. Overall survival for the entire cohort improved over time, from 56% to 63% at 1 year and from 43% to 51% at 3 years, with greater improvements noted among blacks (45% to 61% at 1 year and 34% to 48% at 3 years). Conclusion: Disparities remain in survival rates between whites and Hispanics despite adjustment for clinical factors. Factors not accounted for in this analysis, such as comorbid disease, socioeconomic status, healthcare access and delivery, and psychosocial and cultural variables, require further prospective study.
THERE ARE documented differences in healthcare access, use, and clinical outcome among racial and ethnic groups for a wide variety of medical and surgical settings in the United States. For instance, blacks are less likely to undergo some medical procedures,1–5 including bone marrow transplantation,6 and have lower long-term survival than whites for many types of cancer,7–9 including the leukemias.10,11 Poorer prognosis of ethnic minorities has been correlated with factors both intrinsic and extrinsic to the patient. Implicated factors include age at onset, cancer cell biology, disease stage at diagnosis, comorbid medical conditions, patient socioeconomic status (SES), healthcare access (insurance coverage, geographic barriers, and time from diagnosis to treatment) and delivery (compliance and treatment options received), and psychosocial and cultural factors.9,12–14 Adjusting for these characteristics can sometimes remove apparent disparities attributed to ethnicity.3,9,14–16 A recent review of survival trends after a diagnosis of cancer shows that there is only a modest cancer-specific mortality difference between blacks and whites treated for similar-stage cancer, suggesting that gaps in survival between blacks and whites are only modestly explained by cancer cell biology.17 Less research about other ethnic or racial groups has been conducted. The same factors affecting the healthcare experience of blacks may extend to other populations such as Hispanics or Asians.2 High-dose chemotherapy with or without radiotherapy followed by allogeneic hematopoietic stem-cell transplantation (HSCT) is widely used to treat a variety of malignant and nonmalignant diseases.18–21 Standard indications include leukemia, lymphoma, multiple myeloma, aplastic anemia, and congenital immune deficiencies. Procedure volume has increased rapidly during the last few decades, with approximately 40,000 HSCTs performed worldwide in 2000.22 Although HSCT has the potential to increase survival for many diseases, it is an intensive, costly, and technically sophisticated procedure with substantial risk of early morbidity and mortality. Complications include infection, bleeding, mucositis, graft failure, graft-versus-host disease (GVHD), and major organ toxicity. Transplantation-related mortality ranges from 3% to more than 50%, depending on factors related to the patient (age, sex, comorbid diseases), the disease (stage, extent of involvement, and intrinsic disease characteristics), or the transplantation procedure (time from diagnosis to transplantation, type of graft, and HLA compatibility of the donor).19,23 We sought to examine whether ethnicity is associated with survival outcome once patients decide to undergo HSCT. This high-risk procedure requires intensive pretransplantation and posttransplantation care that may involve many disciplines, is expensive, and is technologically sophisticated. Patients undergoing stem-cell transplantation have already overcome many perceived barriers to access to care that may contribute to poorer outcomes in other diseases. Conversely, the rigors of HSCT and degree of patient involvement in posttransplantation care might accentuate ethnic differences in outcomes. The study cohorts are referred to as ethnic groups rather than racial groups because Hispanics and Asians in most studies are a mix of different races. We hypothesized that ethnicity would remain a significant factor associated with survival outcome after adjusting for patient-, disease-, and transplantation-related characteristics of patients receiving HLA-identical sibling transplantation for leukemia.
Data Source The International Bone Marrow Transplant Registry (IBMTR) is a voluntary working group of more than 400 transplantation centers worldwide that contribute detailed data on consecutive allogeneic HSCT to the Statistical Center at the Health Policy Institute of the Medical College of Wisconsin in Milwaukee (Milwaukee, WI). Approximately 40% of allogeneic transplantations worldwide are registered with the IBMTR; 45% to 50% are from the United States and Canada. Participating centers are required to report all consecutive transplantations and compliance is monitored with on-site audits. Patients are observed longitudinally with yearly follow-up.
Patient Selection Additional information analyzed included age, sex, disease type, disease stage at transplantation, stem-cell source, conditioning regimen, GVHD prophylaxis, interval from diagnosis to transplantation, and geographic location of transplantation centers. Disease stage at transplantation was grouped as early, intermediate, or advanced. First chronic phase of CML and first complete remission of acute leukemia were classified as early disease stage. Second or greater chronic phase and accelerated phase CML and second or subsequent complete remission of acute leukemia were classified as intermediate disease stage. Advanced disease stage included acute leukemia in relapse or never in remission and blast phase CML. We limited the analyses to patients receiving a single transplant with methotrexate and cyclosporine with or without other drugs for GVHD prophylaxis. Likewise, only patients who received predominantly cyclophosphamide with total-body irradiation or cyclophosphamide with busulfan (with or without other drugs) were included in the analysis. None of the patients received reduced-intensity conditioning regimens. Because transplantation technology has changed over time, we first evaluated trends in patient-, disease- and transplantation-related characteristics over time among recipients of HLA-identical sibling transplantation by the year of transplantation divided into three 5-year groups: 1985 to 1989, 1990 to 1994, and 1995 to 1999. Hispanics were excluded from the analysis for the time period 1985 to 1989 because of insufficient numbers (n = 10). Overall survival was the primary outcome studied and was defined as the interval between transplantation and death from any cause. Surviving patients were censored at the date of last contact.
Statistical Analysis Variables considered in multivariate analysis were age, sex, disease type, disease stage, stem-cell source, conditioning regimen, GVHD prophylaxis, interval from diagnosis to transplantation, and transplantation center geographic location. We tested the proportional hazards assumption for each factor in the Cox model using time-dependent covariates. All covariates met criteria for proportional hazards. Interactions between the main effect term (ethnicity) and all covariates were tested before stepwise modeling. The final multivariate model was built using a forward stepwise model selection approach with each model containing the main effect variable. Only factors significantly associated with survival at a 5% level were kept in the final model. First-order interactions were again examined between ethnicity and all significant prognostic factors. Because the population distribution of ethnic groups by geographic regions varied significantly, models were stratified by the geographic location of their transplantation center. Stem-cell source was only considered in the models for the time period 1995 to 1999 because widespread usage of peripheral-blood stem cells did not begin until 1994. Adjusted probabilities of survival were generated from the final Cox models per time period stratified by ethnicity. The predicted survival probabilities were calculated for each cohort according to unique combinations of significant prognostic covariates. A weighted average of the above-predicted survival probabilities was then calculated with weights proportional to the number of individuals at each level of covariates from the pooled sample.24 Estimates and 95% time-specific CIs for differences in survival were obtained by computing estimates of survival for each ethnicity separately at each time period using the regression coefficients from the pooled sample. For all analyses, a P value less than .05 was considered statistically significant. Analyses were performed using SAS Unix Version 8 (SAS Institute, Cary, NC).
A total of 6,443 patients who met our selection criteria were registered with the IBMTR. Of these, 5,301 (82%) were classified as white, 460 (7%) as black, 423 (6%) as Hispanic, and 259 (5%) as Asian. Figure 1  shows the increase in the number of transplantations done in the three time periods by ethnic group. Noticeable is the greater increase in the number of transplantations performed among blacks, Asians, and Hispanics compared with whites between 1990 to 1994 and 1995 to 1999. Characteristics of the cohort by ethnic groups and time period are presented in Table 1. Hispanics undergoing transplantation from 1985 to 1989 were excluded from all analyses because of insufficient numbers (n = 10). In general, Hispanics and Asians underwent transplantation at younger ages than whites and blacks. AML was the most common indication for transplantation among whites, CML was the most common indication among blacks, and ALL was the most common indication among Hispanics. No differences in disease stage at transplantation were noted between whites and blacks or between whites and Asians. Hispanics tended to undergo transplantation more often at an intermediate disease stage but less often at an early or advanced disease stage compared with whites. The proportion of ethnic minorities receiving transplantation more than 1 year after diagnosis was higher than that in whites. As expected, minorities constituted a greater percentage of the population undergoing transplantation in certain geographic regions.
Table 1  shows the changes over time in the patient-, disease- and transplantation-related characteristics of the patients by ethnicity. Tests for trend show variation over time among the different ethnic groups according to age at transplantation, type of disease, conditioning regimen, time interval from diagnosis to transplantation, and transplantation center location.
Table 2
Figures 2 and 3 show the survival probabilities at 1 and 3 years for each time period according to ethnicity after adjusting for statistically significant covariates identified and listed in Table 2. The adjusted 1- and 3-year survival rates for all patients improved from 56% to 63% and 43% to 51%, respectively, from the 1980s to the 1990s. Improved survival from the 1980s to 1999 was observed in whites and blacks, with a greater improvement observed among blacks (1-year survival rate increase of 8% for whites and 16% for blacks when comparing 1985 to 1989 with 1995 to 1999). In the time period 1985 to 1989, blacks had lower adjusted survival rates than whites at 1 year (45% v 57%) and 3 years (34% v 47%) after HSCT. In 1990 to 1994 and 1995 to 1999, no statistically significant differences in survival rates were noted between blacks and whites at 1 and 3 years. Conversely, adjusted 1- and 3-year survival rates decreased over time for Hispanics. One- and 3-year adjusted survival rates for Hispanics were similar to those for whites in 1990 to 1994, but lower than those for whites in 1995 to 1999 (53% v 65% at 1 year and 38% v 53% at 3 years). Asians were not statistically different from those of whites for any time period. Unadjusted survival rates showed essentially the same findings (data not shown).
Although survival rates varied across time periods by ethnicity, no noticeable differences in reported causes of death were observed between whites and other ethnicities (data not shown). Deaths as a result of disease recurrence, infections, and GVHD ranked as the three most common causes of death by ethnicity across time periods.
Our study shows that the survival rates for Hispanics, which were not different from those of whites between 1990 and 1994, have decreased and are most recently (1995 to 1999) significantly lower than for those whites. Survival rates for blacks, which were lower in 1985 to 1989, are most recently similar to those for whites. We did not find any statistically significant differences between whites and Asians in any study period. Significant differences persisted for Hispanics in the multivariate analysis after controlling for age at transplantation, disease type, and disease stage at transplantation. One possible explanation for our results is that imbalances in patient characteristics may account for the worse outcome of Hispanics during 1995 to 1999. However, we do not believe these imbalances caused the survival differences because we did not detect any significant interactions between ethnicity and any of the significant covariates (age, disease, and disease stage) found to be imbalanced in the cohorts, and conclusions were identical when the analysis was limited to the more homogeneous subgroup with chronic phase CML (n = 1,698). Conversely, if imbalances or unmeasured disease factors are the cause of our findings, then this too is of interest. Our analysis included all patients registered to the IBMTR who met the eligibility criteria. The imbalances in the characteristics of the patients are therefore a reflection of actual practice. If Hispanics are undergoing transplantation with more advanced, poorer prognosis diseases than are patients from other ethnic groups, when Hispanics could have undergone transplantation earlier, this also is a problem that may be associated with ethnicity. Alternatively, our finding that survival differences between whites and Hispanics persist after adjustment for statistically significant clinical variables supports the hypothesis that there are other unmeasured factors (perhaps SES, structure of the healthcare system, compliance, or psychosocial and cultural elements related to ethnicity) that may explain the disparities in HSCT survival outcome. For example, optimal posttransplantation care is intensive and requires vigilance for complications, compliance with a large number of critical medications, and a high degree of family support. Ethnic minorities are well documented to have generally lower SES and less medical insurance coverage. This may have affected the Hispanics in our study in their ability to obtain adequate posttransplantation care. Lower SES is associated with lower overall healthcare usage, fewer surveillance tests, and lower quality ambulatory and hospital care.2 A significantly larger percentage of Hispanics lack adequate medical insurance compared with whites, blacks, and Asians.25 Other barriers to access and delivery of health care observed among minority groups, such as skepticism toward efficacy of treatment,26 lower satisfaction with received health care,27 and language barriers,28 could also potentially affect survival. Previous studies have shown that minority children, including blacks and Hispanics, make fewer physician visits compared with white children.29 After HSCT, a wide variety of psychosocial and cultural elements could differentially affect the behavior of patients. Ethnic differences in reacting to and coping with a new state of health and well-being are not well understood in HSCT, but have been linked with survival among patients with breast cancer.30 We believe that some or all of these factors could explain our findings. Many of these variables are difficult to quantify and require patient-reported information necessitating prospectively designed studies. Additional conclusions regarding any link between ethnicity and survival are limited by our inability to explore several factors in this data set. Socioeconomic variables such as education, income, and insurance were not analyzed. These variables are often independent predictors of usage and outcome in other procedures and diseases.2,9 IBMTR collects only limited data on SES, thus restricting our ability to examine this issue further. Comorbid diseases (for example, diabetes mellitus and cardiovascular disease), not characterized in this study, are disproportionately present in ethnic minorities,31–34 and have been shown to increase cancer mortality.35 The prevalence of risk factors such as high cholesterol, diabetes, hypertension, obesity, poor diet, sedentary lifestyle, and smoking are also more common in people of lower SES12,36–38 and varies among ethnic groups.39,40 An additional limitation of this study is that we are only able to characterize the experience of patients who received HSCT. Patients without insurance or with restricted insurance plans may face limited access to HSCT in the first place.6 Our manner of classifying ethnicity may not be biologically homogenous and is not the same as racial grouping. For instance, outcome between Chinese and Japanese people may be different, but small numbers prevented subgroup analyses. Perhaps most importantly, unmeasured biologic patient or leukemia characteristics that unequally affect ethnic groups may exist and account for our findings.10 However, the fact that disparities were only seen in the later study period points to a factor that changes over time, leading us to believe that it is likely not biology that causes this disparity between whites and Hispanics. In addition, it is interesting to study whether nonbiologic factors (SES, culture, or health insurance) interact with the biology of the disease, or whether these nonbiologic factors affect treatment compliance. In summary, in 1995 to 1999, Hispanics had significantly reduced survival after HLA-identical sibling HSCT for AML, ALL, and CML than whites, even after adjusting for age, disease type, and disease stage at transplantation. Survival rates between whites and blacks and between whites and Asians were not statistically different over the study period. Although considerable research has focused on the factors that influence outcomes for blacks in the medical setting, the factors causing discrepancies in survival among Hispanics after HSCT remain unclear. It is interesting to note that the number of transplantations performed over the years among ethnic minorities is much lower when compared with the number performed on whites, suggesting the possibility of differential access to health care. It is possible that factors before transplantation, such as patients’ choice of treatment or beliefs and trust in the medical system, may vary among ethnicities and lead to differences in use of stem-cell transplantation. However, it is not possible to address these hypotheses with IBMTR data because information is collected only on patients who undergo transplantation. Our study suggests that more research is needed to clarify these factors, perhaps first focusing on socioeconomic, psychosocial, and cultural issues in the Hispanic population. Strategies for better collection of these types of data also should be explored.
The authors indicated no potential conflicts of interest.
Supported by Public Health Service Grant U24-CA76518 from the National Cancer Institute, the National Institute of Allergy and Infectious Diseases, and the National Heart, Lung and Blood Institute; and grants from Allianz Life/Life Trac; American Cancer Society; American Red Cross; American Society of Clinical Oncology; Amgen Inc; anonymous; Aventis Pharmaceuticals; Baxter Healthcare Corp; Baxter Oncology; Berlex Laboratories Inc; Blue Cross and Blue Shield Association; The Lynde and Harry Bradley Foundation; Bristol Myers Squibb Oncology; Cedarlane Laboratories Ltd; Cell Pathways; CelMed Biosciences; Centocor Inc.; Cubist Pharmaceuticals; Darwin Medical Communications Ltd; Dynal Biotech ASA; Edwards Lifesciences RMI; Endo Pharmaceuticals Inc; Enzon Pharmaceuticals Inc; Excess Inc; Fujisawa Healthcare Inc; Gambro BCT Inc; GlaxoSmithKline Inc; Human Genome Sciences; ICN Pharmaceuticals Inc; ILEX Oncology; The Kettering Family Foundation; Kirin Brewery Co; Ligand Pharmaceuticals Inc; Eli Lilly and Company; Nada and Herbert P. Mahler Charities; Merck & Co; Millennium Pharmaceuticals; Miller Pharmacal Group; Milliman USA Inc; Miltenyi Biotec; Irving I. Moskowitz Foundation; National Marrow Donor Program; NeoRx Corp; Novartis Pharmaceuticals Inc; Novo Nordisk Pharmaceuticals; Orphan Medical Inc; Ortho Biotech Inc; Osiris Therapeutics Inc; PacifiCare Health Systems; Pall Medical; Pfizer U.S. Pharmaceuticals; Pharmacia Corp; Pharmametrics; Pharmion Corp; Protein Design Labs; Roche Laboratories; SangStat Medical; Schering AG; StemCyte Inc; StemCell Technologies Inc; Stemco Biomedical; StemSoft Software Inc; SuperGen Inc; Sysmex; THERAKOS, a Johnson & Johnson Co; Unicare Life & Health Insurance; University of Colorado Cord Blood Bank; ViaCell Inc; ViaCor Biotechnologies; WB Saunders Mosby Churchill; and Zymogenetics Inc.
Presented orally during the 44th American Society of Hematology Annual Meeting in Philadelphia, PA, December 6–10, 2002. The contents of this article are solely the responsibility of the authors and do not necessarily represent the official views of the National Cancer Institute.
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Copyright © 2003 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
2 test for categorical variables and the Kruskal-Wallis test for continuous variables to compare patient, disease, and transplantation-related characteristics among the four improvised ethnic cohorts. Test for trends across time periods among the four ethnicities were also tested. The risk of death after HSCT was evaluated in multivariate analyses using Cox proportional hazards regression techniques to compare the relative risk of mortality among ethnicities (with whites used as the reference group) while adjusting for other potentially confounding differences between the cohorts. Because the main focus of the study was to look for differences in survival among ethnicities at different time periods, separate models were constructed for the years 1985 to 1989, 1990 to 1994, and 1995 to 1999. 
