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Psychosomatics 45:378-385, October 2004
© 2004 The Academy of Psychosomatic Medicine

Predictors of 1-Year Survival Assessed at the Time of Bone Marrow Transplantation

Grace Chang, M.D., M.P.H., E. John Orav, Ph.D., Mei-Yee Tong, M.S., and Joseph H. Antin, M.D.

Received May 22, 2003; revision received Nov. 17, 2003; accepted Dec. 16, 2003. From Brigham and Women's Hospital; the Department of Psychiatry, the Department of Medicine, and the Department of Medicine (Biostatistics), Harvard Medical School, Boston; and the Dana Farber Cancer Institute, Boston. Address correspondence to Dr. Chang, Brigham and Women's Hospital, 221 Longwood Ave., Boston, MA 02115; Gchang{at}partners.org (e-mail).


  ABSTRACT

 
TOP
 ABSTRACT
INTRODUCTION
 METHOD
 RESULTS
 DISCUSSION
 REFERENCES
 
The purpose of this prospective cohort study was to identify pretransplant and transplant predictors of 1-year survival after allogeneic hematopoietic stem cell transplantation (HSCT) for chronic myelogenous leukemia. Psychosocial and behavioral variables such as alcohol abuse and cigarette smoking were systematically assessed at the time of HSCT with structured diagnostic instruments. A total of 114 patients participated, with an overall 1-year survival rate of 66%. Lifetime alcohol and other substance use, cigarette smoking, depression, and quality of life prior to transplant were not found to affect 1-year survival. However, other clinical variables prior to transplant and once transplant occurred were found to predict survival.


  INTRODUCTION

 
TOP
 ABSTRACT
 INTRODUCTION
METHOD
 RESULTS
 DISCUSSION
 REFERENCES
 
Chronic myelogenous leukemia is a malignant clonal disorder of hematopoietic stem cells that results in increased myeloid cells, erythroid cells, and platelets in peripheral blood and marked myeloid hyperplasia in bone marrow.1–3 Accounting for approximately 15% of all cases of leukemia in the United States, chronic myelogenous leukemia is caused by the inadvertent activation of Abelson tyrosine kinase.1 The disease is slightly more prevalent in men than in women and occurs at any age, with a median age at onset of 55–60 years and a median survival of 4 to 5 years.2

Treatment strategies for this disease include an Abelson tyrosine kinase inhibitor (STI-571 or Gleevec), interferon alpha, busulfan, hydroxyurea, and allogeneic hematopoietic stem cell transplantation (HSCT), the only proven curative therapy.3–7 More popularly known as a bone marrow transplant, HSCT is the second most frequent major organ transplant in the United States and has the potential for substantial growth and therapeutic application to a variety of other diseases. There is no particular constraint imposed by a limited supply of donor organs.

Allogeneic HSCT is associated with mortality rates estimated to range from 10% to 20% in the first 100 days following transplant for chronic myelogenous leukemia in the ideal candidate with a fully HLA-matched sibling donor.8 Prognostic factors to predict outcome have been studied. For example, disease phase (stable), patient age (younger), and the length of time between diagnosis and transplant (shorter) have all been found to influence survival.3,9–11 On the other hand, splenomegaly and a preparative regimen with interferon alpha have no apparent effect.12 Equivalent outcomes for phenotypically matched related and unrelated donors have been well documented, although unrelated donor HSCT has a higher death rate.13–15

Whereas the clinical variables impacting survival have been studied, much less is known about the psychosocial and behavioral factors that may affect HSCT outcome.16 A retrospective study of 100 patients undergoing bone marrow transplantation reported that pretransplant depressed mood was predictive of shorter survival time. The depressed mood was established by retrospective chart review of psychiatric evaluations completed by residents and attending staff. This study did not use standardized measures of depression or control for disease or treatment variables.17 A prospective study of 42 patients with acute and chronic leukemias undergoing allogeneic bone marrow transplantation, given standard measures of mood, anxiety, and quality of life, found that better quality of life trended with increased survival. Quality of life, however, was not associated with any disease, demographic, or treatment variables.18 Another prospective study of 123 consecutive patients undergoing autologous and allogeneic bone marrow transplantation who completed six self-report questionnaires found that none of the psychological variables assessed before transplant were associated with survival. The questionnaires measured functional limitations, general health, psychological symptoms, locus of control, self-esteem, and general quality of life.19

Moreover, in contrast to liver transplants, where the impact of alcohol abuse and other substance use disorders has been well considered from medical and ethical viewpoints, the role of substance abuse in bone marrow transplant outcome has not been prospectively studied.20–23 A retrospective case-control study of 34 patients matched for disease and stage, type of transplant, pretransplant conditioning regimen, and age—but only half of whom had substance abuse diagnoses—found reduced survival times for the patients with substance abuse (p=0.0022). The difference in survival persisted even after stratifying for type of transplant and cigarette smoking.24

Despite these intriguing studies, the role of psychosocial and behavioral variables, including alcohol and substance use diagnoses, in HSCT outcome is difficult to assess.16 Impediments may stem from limitations of study design such as 1) small sample sizes; 2) lack of standardized measures to assess mood longitudinally; or 3) inadequate consideration of medical variables, such as donor-recipient match quality or the inclusion of both hematologic and solid organ cancers or both autologous and allogeneic transplants without statistically adjusting for their nonequivalence in terms of morbidity or mortality.17–19,24

The purpose of this prospective cohort study was to identify the predictors of 1-year survival after allogeneic hematopoietic stem cell transplantation (HSCT) for chronic myelogenous leukemia. The predictors to be examined include not only baseline and pretransplant demographic and clinical variables (such as age and interval between diagnosis and transplant) but also psychosocial and behavioral variables such as alcohol and drug use, cigarette smoking, functional quality of life, and depression. These are the variables that might be considered when the decision to proceed with transplantation is made. The specific hypothesis tested was that psychosocial and behavioral variables such as alcohol abuse and cigarette smoking would have an adverse impact on survival. Finally, transplant variables such as medical complications were examined as predictors of survival.


  METHOD

 
TOP
 ABSTRACT
 INTRODUCTION
 METHOD
RESULTS
 DISCUSSION
 REFERENCES
 
Patients with chronic myelogenous leukemia admitted for allogeneic transplantation were invited to participate in this prospective cohort study within the first week of admission. In the first 12 months of the study beginning in July 1997, recruitment was limited to subjects receiving related donor transplants. However, in subsequent months, recruitment was broadened to include patients receiving transplants from unrelated donors, since equivalent outcomes with unrelated donors were demonstrated in 1998.13–15

Participants consented to an initial diagnostic interview, with follow-up interviews 6 and 12 months after transplant, and review of their medical records. Participants were given a $50.00 honorarium for completion of the initial interview and honoraria of $25.00 for each follow-up interview completed. This study was reviewed and approved by the institutional review board of Brigham and Women's Hospital, Boston.

The initial diagnostic interview included: 1) the Functional Living Index–Cancer,25 the original 22-item measure of the overall functional quality of the patient's day-to-day life with four items referring to "today," seven items referring to the past "2 weeks," and one item referring to the "past month;" 2) the QL-Index,26 a 5-item measure of quality of life over the past week; 3) Beck Depression Inventory–Revised Edition,27 a 21-item measure for depressive symptoms; 4) the alcohol and drug abuse modules from the Structured Clinical Interview for DSM-IV28 to generate lifetime and current alcohol and substance use diagnoses; 5) the Timeline Followback technique29 to provide data on the quantity and frequency of alcohol consumption in the 180 days preceding study enrollment or hospital admission; and 6) a structured series of questions about the use of tobacco products, age at first and last use, quantity, and frequency. The occupation of each participant was coded according to Treiman's Standard International Occupational Prestige Scale,30 as a measure of socioeconomic status in a group for whom income may be adversely impacted by illness.

Medical records were abstracted 12 months after transplant using an abstraction form for pretransplant and transplant information. Pretransplant information included medical history prior to transplantation and clinical data at the time of diagnosis, such as white cell and platelet count. Transplant variables included transplant admission and discharge liver function test results, complications during transplant, and transplant outcome. Cause of death was ascertained from autopsy and death certificate data.31

Data Analysis
All analyses were carried out by using the SAS statistical package (Version 8.01, SAS Institute, Inc, Cary, NC). Simple descriptive statistics were calculated and are reported as percentages, means, and standard deviations. Survival times were calculated from the date of admission to the date of 12-month follow-up or death, whichever came first. Potential predictor variables of survival were tested individually using either the log-rank test for discrete variables or the Cox proportional hazards model for continuous variables. Age was tested as a continuous variable and in groups divided by quartile (first quartile=38 years; second quartile=46 years; third quartile=52 years), similar to groupings in other investigations.10,13 Variables found to be associated with survival at p<0.10 were then tested in one of two multivariate Cox proportional hazards models using forward selection, with alpha=0.05 as the criterion for statistical significance. The first model included only pretransplant variables. The second model included transplant variables. In the event that no psychosocial variables would be included, two representative psychosocial variables (lifetime alcohol diagnoses and cigarette pack-years) would be individually forced into the two multivariate models in order to test them.


  RESULTS

 
TOP
 ABSTRACT
 INTRODUCTION
 METHOD
 RESULTS
DISCUSSION
 REFERENCES
 
Of 122 patients with chronic myelogenous leukemia admitted for allogeneic HSCT between July 1997 and January 2001, 114 (93.4%) agreed to participate in this study. Three individuals declined (2.5%), and five (4.1%) were ineligible because they were not English speaking. No survivors refused to complete the 6-month interview (N=80). Only two of 75 surviving participants (2.7%) declined to complete any part of their 12-month follow-up interview, and one participant (1.3%) provided partial 12-month follow-up data.

The median age of participants was 46 years (mean= 44, SD=9, range=22–64). There were somewhat more male subjects (60%). Most participants were married (70%). The ethnic background was 93% Caucasian, 1.7% Asian, 2.6% African American or black, 1.7% Hispanic, and 1% Native American. The mean occupational scale score was 47 (SD=13, range=16–78). Examples of occupations with a score of 47 include sales representatives from the manufacturing industries and wholesale trade, building managers and superintendents, and agriculture and biological technicians.

Subjects' functional quality of life at admission was assessed by the self-administered Functional Living Index–Cancer scale and the physician-administered Q-L Index. The mean Functional Living Index–Cancer score was 99 (SD=11, range 71–126). A high score on this scale (maximum=154) is consistent with a higher quality of life. The mean Q-L score was 9 (SD=1.4, range=2–10). As with the Functional Living Index–Cancer scale, a higher Q-L score (maximum=10) is consistent with higher quality of life. The two scores were highly correlated (r=0.46, df=112, p<0.0001). Subjects were assessed for depression with the Beck Depression Inventory, which yields summary scores that range from 0 to 63. The mean score on the Beck Depression Inventory was 10 (SD=7, range=7–37). In psychiatric patients, scores of 10 to 18 suggest mild to moderate depression, but in others, scores greater than 15 suggest depression.32

Thirty-eight percent of subjects satisfied DSM-IV criteria for lifetime alcohol abuse or dependence, but none satisfied criteria for current diagnoses. Participants had an average of 1.6 standard drinks (SD=1.7) per drinking day on 40% of the 180 days preceding admission. Subjects also satisfied DSM-IV criteria for lifetime cannabis abuse or dependence (8%), current cannabis abuse or dependence (3%), lifetime stimulant abuse or dependence (1%), lifetime opioid abuse or dependence (1%), lifetime cocaine abuse or dependence (5%), and lifetime polysubstance abuse or dependence (1%). Sixty-two percent were lifetime cigarette smokers with a mean of 12 (SD=20) pack-years. Sixty of the 71 (84%) smokers stopped their use of cigarettes at least 3 months before transplant admission.

At the time of admission, 97 patients (85%) had stable phase chronic myelogenous leukemia, nine (8%) were in the accelerated phase, seven were in blast crisis (6%), and the disease stage of one subject (1%) was not classified. One hundred seven (94%) were admitted for a myeloablative HSCT, and seven (6%) had a T-cell depleted HSCT. Donors were unrelated (51%), related siblings (46%), and related nonsiblings (3%). Most donor matches were 6/6 (84%), and the rest were 5/6 (16%). Table 1 summarizes additional clinical information.


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TABLE 1. Clinical Characteristics of 114 Patients With Chronic Myelogenous Leukemia Who Underwent Allogeneic Hematopoietic Stem Cell Transplantation



The overall 1-year survival rate was 66%. Median survival among those who died was 69 days. Most frequent causes of death were pulmonary failure (N=10, 26%), sepsis (N=7, 18%), graft versus host disease (N=7, 18%), and multiple organ system failure (N=7, 18%). Other causes of death (N=8, 21%) included renal failure, veno-occlusive disease, hemorrhage, and gastrointestinal complications.

Table 2 summarizes the univariate analyses of pretransplant and transplant clinical variables as predictors of survival. Disease phase, age group, recipient CMV status, and interval between diagnosis and transplant were pretransplant variables related to outcome (all p<0.05). Twelve transplant variables, such as measures of liver function at discharge or complications, were identified to be individual predictors of survival (all p<0.05). Of note, none of the psychosocial or behavioral variables was statistically significantly related to transplant outcome (p>0.05).


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TABLE 2. Univariate Predictors of Survival in 114 Patients With Chronic Myelogenous Leukemia Who Underwent Allogeneic Hematopoietic Stem Cell Transplantation



Table 3 summarizes the multivariate survival models. Three pretransplant clinical variables were found to increase the risk of death. Chronic myelogenous leukemia disease phase other than stable phase and being older than 39 each increased the risk of death approximately threefold. Admission aspartate aminotransferase (ALT) values increased the risk of death by 2% for each unit increase in ALT. Five transplant variables were found to increase the risk of death. Development of CNS complications (e.g., delirium), veno-occlusive disease, and infection each increased the risk of death by a factor of about 3. Elevated lactate dehydrogenase (LDH) and total bilirubin at discharge increased the risk of death by 0.2% and 6%, per unit increase in LDH and total bilirubin, respectively.


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TABLE 3. Multivariate Survival Models



Neither lifetime alcohol diagnoses nor cigarette pack-years increased the risk of death in either the pretransplant or transplant variable models. The hazard ratio for lifetime alcohol diagnoses as a univariate predictor was 0.529 (Table 2) and was 0.537 in the multivariate model (Table 3). A possible trend is that lifetime alcohol diagnoses have a protective effect on survival. It was not possible to evaluate the impact of current substance abuse or dependence, including alcohol and cigarette use, because of their relative infrequency.


  DISCUSSION

 
TOP
 ABSTRACT
 INTRODUCTION
 METHOD
 RESULTS
 DISCUSSION
REFERENCES
 
The main finding of this study was that when psychosocial, behavioral, and medical variables were systematically evaluated in a cohort of 114 patients undergoing allogeneic HSCT for chronic myelogenous leukemia, different clinical variables predicted 1-year survival prior to transplant and once transplant occurs. Pretransplant variables found to have an adverse impact on survival were age greater than 39, chronic myelogenous leukemia phase other than stable, and having higher ALT at admission. Transplant variables found to have an adverse impact on survival were the development of CNS complications, veno-occlusive disease, infection, and elevated total bilirubin and LDH at discharge. When systematically evaluated with standard instruments, lifetime alcohol and other substance use, cigarette smoking, depression, and quality of life prior to transplantation were not found to affect survival outcome.

However, the high prevalence rate of cigarette smoking (62%) and lifetime alcohol diagnoses (38%) in this sample is noteworthy. The overall prevalence of cigarette use by American adults is approximately 25%.33 The estimated lifetime prevalence of alcohol abuse and dependence disorders is 23.5% (or 9.4% and 14.1%, respectively).34 Few participants reported current cigarette smoking and alcohol consumption, but it may be possible that many subjects modified their smoking and drinking behaviors prior to admission or once their diagnosis of chronic myelogenous leukemia was made. A Danish randomized trial found that just 1 month of preoperative abstinence from alcohol significantly reduced postoperative morbidity in a group of 42 "alcohol misusers."35

While neither cigarette smoking nor alcohol diagnoses had a direct effect on survival in this study, it seems possible that these practices may have been contributory to the subjects' ill health in other ways. Although speculative, they could account for the observation that the median age of participants was nearly one decade less than the usual age of chronic myelogenous leukemia onset. Some have proposed a link between smoking and the hematolympho-proliferative cancers, and alcohol's role as a carcinogen has been documented.36–42 Chronic alcohol abuse has been associated with increased mortality in seriously ill patients because of the increased risk of developing acute respiratory distress syndrome in adults.43 Pulmonary failure accounted for 26% of the deaths in this sample.

Potential limitations to this study's findings include reliance on patients with one type of cancer undergoing allogeneic HSCT at one center. However, inclusion of patients with disparate types of cancers undergoing autologous and allogeneic transplantation would have been problematic without statistical adjustment, given their widely different morbidity, mortality, and treatment indication and success rates. The median age of the study participants was younger than the median age typically associated with chronic myelogenous leukemia onset. This may be explained by the fact that younger patients are more likely to be candidates for HSCT, as reflected in other studies of HSCT for chronic myelogenous leukemia.10,13 Another possible limitation is that subjects were not forthcoming about their use of alcohol and substances or that they modified their customary practices, resulting in few subjects satisfying criteria for current diagnoses. The use of standardized diagnostic instruments generally reduces the potential for ascertainment bias in research volunteers.44 Finally, this study did not assess the impact of alcohol or cigarette use in the 12-month period following transplant, since its purpose was to evaluate the impact of pre-transplant and transplant variables on 1-year survival.

In this comprehensive evaluation of clinical, psychosocial, and behavioral variables, different clinical variables were found to predict 1-year survival prior to transplant and once transplant had occurred. Prior to HSCT, younger age and stable phase of disease were associated with improved survival, and so early diagnosis is clearly beneficial. After HSCT, acute transplant-related complications may exert greater influence than psychosocial or behavioral variables in moderating outcomes in the first year after the procedure. Future investigations might include longer follow-up periods to evaluate more fully the impact of behavioral variables. The results of this prospective cohort study support the American Medical Association's criteria for patient selection for organ transplantation,45 in that perceived obstacles to treatment (such as substance abuse or the patient's contribution to his medical condition) are unacceptable exclusion criteria because they do not appear to affect outcome in this sample of patients.


  ACKNOWLEDGMENTS

 
This study was supported by grants from the Alcoholic Beverage Medical Research Foundation (GC) and the NIH/National Institute on Alcohol Abuse and Alcoholism (K2400289, GC).

The authors wish to thank Arti Gehani and Elizabeth Berger who were research assistants for this project; Rodney C. Haring and Gregory Brass who assisted as interns from the Four Directions Summer Research Program at Harvard Medical School; and the patients who participated in this study.


  REFERENCES

 
TOP
 ABSTRACT
 INTRODUCTION
 METHOD
 RESULTS
 DISCUSSION
 REFERENCES
 

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