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Association of Depressive Syndrome and Early Deaths Among Patients After Stem-Cell Transplantation for Malignant Diseases

From the Health Policy Institute and the Department of Medicine, Hematology and Oncology, Bone Marrow Transplantation Program, Medical College of Wisconsin, Milwaukee, WI; and the Department of Adult Oncology, Dana-Farber Cancer Institute, Boston, MA.

Address reprint requests to Fausto R. Loberiza, Jr, MD, MS, International Bone Marrow Transplant Registry Health Policy Institute, Medical College of Wisconsin, 8701 Watertown Plank Rd, Milwaukee, WI 53224; email: faustol{at}mcw.edu

	ABSTRACT

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PURPOSE: The association of depression and increased mortality in the general population, and also various medical conditions, is well documented. However, depression is not well studied in the setting of hematopoietic stem-cell transplantation (HSCT). We examined the association between depressive syndrome and survival after HSCT.

PATIENTS AND METHODS: A total of 193 patients who received autologous or allogeneic HSCT from Brigham and Women’s Hospital or Dana-Farber Cancer Institute were evaluated prospectively. The self-rated Likert-scaled symptom checklist, the SF-36, and the Spitzer Quality of Life Index Scale were administered. Outcomes evaluated included survival and quality of life.

RESULTS: Sixty-seven patients (35%) satisfied the criteria for depressive syndrome. The 1-year probability of survival for the depressed and nondepressed patients was 85% (95% confidence interval [CI], 74% to 92%) and 94% (95% CI, 89% to 97%), respectively (P = .04). In multivariable modeling, depressed patients have a three-fold greater risk of dying than nondepressed patients (95% CI, 1.07 to 8.30; P = .04) between 6 and 12 months after HSCT after adjusting for other prognostic factors. Global inferiority in quality of life was observed in the depressed cohort when last measured at 24 months after transplantation.

CONCLUSION: Depressive syndrome after HSCT is associated with decreased survival, at least from 6 to 12 months after transplantation. Persistence of this association after controlling for possible confounding factors suggests that depression may be more than simply a marker for concurrent ill health. This study raises an interesting hypothesis as to whether psychological or pharmacologic intervention for depression after HSCT can improve survival and/or quality of life.

	INTRODUCTION

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THE ASSOCIATION of depression and increased mortality in the general population is well documented.^1-8 A meta-analysis using a pooled sample representing 19,000 people showed individuals with depression had excess mortality from infectious, respiratory, nervous, and circulatory disorders compared with the general population.⁹ Similarly, depression and reduced survival have been linked in patient populations with various medical conditions such as heart disease, cancer, and solid organ transplantation.^10-14 Nevertheless, it remains controversial whether depression (or any psychological deficit) contributes directly to the increased mortality or is simply a marker for the severity of underlying chronic illness.

The association of depression and survival is not well addressed in the setting of hematopoietic stem-cell transplantation (HSCT). Only one study has examined the relationship between depressed mood and subsequent survival. Colon et al¹⁵ found that patients with depressed mood as documented before HSCT had lower survival rates. Although this study involved a relatively homogenous population and adjusted for patient age, type of acute leukemia, stage of disease, and year of transplantation, other physical and mental patient characteristics were not measured to allow adjustment for concurrent health status. Thus, this study could not address whether depression simply reflects poor health and is consequently a marker for poor outcome, or is a primary contributor to poor outcome.

Both depression and anxiety are common after HSCT,^15-23 with the prevalence of depressive symptoms among transplant recipients estimated to be at least 18%.¹⁸ Clinical depression is a major impediment to high levels of perceived health, affecting patients’ quality of life and, possibly, interfering with complete recovery.¹⁷ Longitudinal studies show that despite steady increases in return to normal functioning with 75% of HSCT recipi-ents returning to baseline levels at the end of 2 years, 37% have at least mild depression at the end of the first year after transplantation.¹⁹

The biopsychosocial mechanism of how depression may alter survival independent of physical status is largely speculative. Randomized studies of pharmacologic interventions with or without psychotherapy in cancer patients with depression provide conflicting evidence for benefit, further fueling the controversy.^24-27 The purpose of this observational study is to identify the association, if any, between depression and survival after HSCT after controlling for other potential prognostic factors. Evidence suggesting an association could prompt further studies aimed at identifying possible mechanisms and developing and testing interventions. Even if survival is not directly affected, proper treatment of depression after transplantation could improve patients’ quality of life and return to normal function.

	PATIENTS AND METHODS

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Study Population
Patients scheduled for autologous or allogeneic HSCT were prospectively recruited from either the Brigham and Women’s Hospital (BWH) or Dana-Farber Cancer Institute (DFCI). Recruitment began at BWH in August 1996 and at DFCI in January 1997. Eligible patients were required to be at least 18 years of age and scheduled for either autologous or allogeneic HSCT within 1 week to 3 months of enrollment. Excluded were patients who (1) did not speak or read English, (2) declined participation, (3) did not return baseline questionnaires, or (4) could not be contacted before admission for transplantation because of logistic reasons. Initial contact of the potential study patient was made by one of the authors (S.J.L.) to describe the study. Subsequently, mailed questionnaires, consent forms, and a self-addressed, stamped envelope were sent to the potential study participants. Follow-up questionnaires were mailed to surviving participants at 6, 12, and 24 months after HSCT. Results reported here describe data collected before May 1, 2001, although data collection continues. The specific transplantation regimens and protocols have been described in detail elsewhere.²⁸ Only patients who returned their 6-month posttransplant surveys are included in this report (n = 193). The study protocol was reviewed and approved by the institutional review boards of BWH and DFCI.

Data Collection
Patients were surveyed before transplantation and at 6, 12, and 24 months after HSCT using both validated and constructed items. Constructed items and a symptom checklist were developed after a review of the literature and input from transplant physicians, nurses, and patients. The survey was then tested to gauge clarity and ease of completion on a pilot group of posttransplant patients. The general description of the population is provided in two previous publications.^28,29 Baseline questionnaires elicited information on sociodemographics (age, sex, marital status, race, education, and work status) and general health status (excellent, very good, good, fair, or poor). Follow-up surveys collected information on return to work; physician visits; medication use; and prevalence and severity of symptoms such as depression, fatigue, anxiety, concentration ability, feelings of isolation, and memory loss. These symptoms were rated on a five-point scale labeled as "I do not have this symptom," "not bothered at all," "bothered a little," "bothered a lot," or "extremely bothered." All three follow-up surveys were identical and addressed recovery issues. Overall survival of the cohort was calculated as of May 1, 2001, using data from the BWH/DFCI clinical database.

In order to verify the constellation of symptoms representing depression, a chart review was conducted by a blinded assessor to determine clinician documentation of depressive symptoms and prescription of antidepressants. Information was abstracted from notes in the medical record dated within 4 weeks of the 6-month survey completion. This chart review was considered the "gold standard" for calculating test characteristics for our definition of depressive syndrome.

Measures and Outcome
Because no standardized measure of depression was collected, depressive syndrome was operationally defined as being present in any person who reported being bothered by depression and who had four or more diagnostic symptoms (anxiety, difficulty concentrating, feelings of isolation, fatigue, or memory loss). Individuals with three symptoms but who reported being "extremely bothered" by depression were likewise considered as having depressive syndrome. Patients were classified as to the presence or absence of depressive syndrome on the basis of their 6-month posttransplant questionnaire. Patients fulfilling the above definition are referred to in this study as "depressed" to distinguish them from the "nondepressed." Two validated quality-of-life instruments, the SF-36^30,31 and the Spitzer Quality of Life Index,^32,33 were administered before transplantation and 6, 12, and 24 months after transplantation. The defined measure of depressive syndrome was correlated with the measure of composite mental health from the SF-36 (r = .65) to establish convergent validity. The outcome of interest is survival defined as time to death. Patients were censored at time of last follow-up.

Statistical Analysis
Patient-, disease-, and transplantation-related characteristics between patients with or without depressive syndrome were compared using ² test or Wilcoxon rank sum test for categorical and continuous variables, respectively. Baseline quality-of-life domains from the SF-36 and the Spitzer Quality of Life Index were compared between the two groups using similar tests.

Data were analyzed using a Cox proportional hazards model. Because the main focus of the study was to determine whether there was a survival difference after the diagnosis of depressive syndrome (which was first assessed by the 6-month survey); only patients surviving longer than 6 months and completing surveys were analyzed. The method built a single model with time to death as the dependent variable and age, sex, race, religion, marital status, disease type, disease stage (early, intermediate, advanced),²⁹ type of transplantation (autologous, related, unrelated), use of total-body irradiation, and T-cell depletion as explanatory variables. A main effect term for the presence or absence of depressive syndrome was forced into the model. The proportional hazards assumption for all variables was examined using time-varying covariate and graphical approaches.³⁴ Construction of stratified proportional hazards models or time-dependent covariates was used whenever nonproportional variables were identified. Interactions between presence or absence of depressive syndrome and all explanatory variables were examined. The final model included all patient, disease, and transplantation factors found prognostic of the outcome plus a term for depressive syndrome. We then evaluated the effect of chronic graft-versus-host disease, physical and mental composite scores of the SF-36 at 6 months, state of health score in the Spitzer Quality of Life Index at 6 months, and relapse on the association between depressive syndrome and survival by forcing each into the final model described above. Using the prognostic factors identified, an adjusted Kaplan-Meier curve comparing the depressed and nondepressed groups was plotted. Type I error was set at an alpha of less than .05, but values greater than .01 should be interpreted with caution, given the multiple comparisons. All tests were performed using SAS Version 8.0 (SAS Institute, Inc, Cary, NC) for Unix.

	RESULTS

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Patient Characteristics
A total of 313 (68%) of the 458 mailed baseline questionnaire were completed before transplantation. Comparison of the 313 responders with the 145 nonresponders with the initial mailed survey at baseline showed that the study participants were more likely to have good prognosis and to undergo allogeneic transplantation, and to be white, female, and older.²⁹ Of the 313 patients returning questionnaires, 86 (27%) died within 6 months and 34 (11%) failed to respond to the 6-month follow-up questionnaire, leaving 193 (62%) patients included in the study. Patients who failed to respond to the 6-month questionnaire had more advanced disease (20% v 3%; P < .001), lower baseline physical composite scores (SF-36) and lower overall states of health (Spitzer Quality of Life Index), and a lower probability of surviving to 1 year (56% v 90%; P = .001) than those who were included in the study. Other patient-, disease-, and transplantation-related characteristics were similar between responders and nonresponders. Response rates of the study population over time are summarized in Fig 1.

View larger version (15K): [in this window] [in a new window]   Fig 1. Response rates of study participants over time.

Multivariate and Adjusted Models Predicting Survival
Table 4 shows the multivariate model for survival. The relative risk of death between the depressed and nondepressed patients varied before and after 12 months after transplantation. In multivariable modeling, depressed patients were found to have a three-fold greater risk of dying than nondepressed patients (95% confidence interval [CI], 1.07 to 8.30; P = .04) between 6 and 12 months after transplantation. There were 17 patients in the cohort who died during this time period. Fifteen (88%) of these patients received allogeneic HSCT; 10 (67%) were classified as depressed. No difference was seen between the two cohorts in their risk of dying after 12 months. Other patient-, disease-, and transplantation-related variables associated with survival included age at transplantation, disease stage at transplantation, and type of disease. Adjusted Kaplan-Meier survival curves of the depressed and nondepressed cohorts are shown in Fig 2. The 1-year probabilities of survival for depressed and nondepressed patients are 85% (95% CI, 74% to 92%) and 94% (95% CI, 89% to 97%), respectively (P = .04). The effects of forcing factors potentially altering the relationship between depression and survival outcome into the final model are shown in Table 5. The same overall relationship between depression and increased risk of death existed when the model was adjusted separately for (1) chronic graft-versus-host disease, (2) the physical and mental composite scores of the SF-36 at 6 months, (3) the state of health score in the Spitzer Quality of Life Index at 6 months, and (4) relapse.

View larger version (9K): [in this window] [in a new window]   Fig 2. Adjusted Kaplan-Meier plot of survival probability between depressed and nondepressed patients.

At 12 months after HSCT, depressed patients were more likely to be taking medications related to the transplantation (83% v 58%; P = .02), less likely to be working full-time or part-time (39% v 55%; P = .03), less likely to agree with the statement that life has returned to normal (37% v 70%; P < .001), less likely to report "very good to excellent" perception of their overall health (23% v 53%; P = .03), and more likely to report depressive symptoms (72% v 17%; P < .001) than the nondepressed cohort. Frequencies of physician visits as self-reported by patients were the same for the two cohorts.

	DISCUSSION

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We found that 35% of patients surviving at least 6 months after HSCT reported symptoms characteristic for depressive syndrome. These patients had poorer quality of life and a three-fold higher risk for death in the subsequent 6 months compared with nondepressed patients, even after controlling for all known potential confounders.

Depression is frequent in cancer patients sometime in the course of their illness.^35-37 The natural evolution of cancer and its treatment from anticipation, diagnosis, treatment, remission, and exacerbation are intuitively sources of psychic assault. In HSCT, the additional stress of rigorous pretransplantation chemotherapy, the intense posttransplant prophylaxis and monitoring, and the constant prospect of death may lead to depression or may exacerbate depressive symptoms. Clinicians may consider depression as a natural response to a stressful situation and an unfortunate by-product of an aggressive curative attempt. Although true, according to our data, depressive syndrome is associated with a global decrease in physical and mental functioning and is associated with decreased survival in the subsequent 6 months. In the palliative care model, where a premium is placed on life with quality and dignity, there is little doubt that depression should be diagnosed and treated.

Our data also suggest that a component causative role of depression in early deaths may be possible because a statistical association persisted despite adjustment for multiple possible confounders including type of transplantation, chronic graft-versus-host disease, mental and physical functioning as measured on validated instruments, and relapse. However, allogeneic patients were overrepresented in the depressed cohort. We have tested for an interaction between type of transplantation and depression and found no evidence that the risk of death associated with depression varies. However, because we remain concerned about potentially important unmeasured clinical variables associated with autologous and allogeneic transplantation, and there is an intrinsic difference in the risk of death, all multivariate models were stratified according to type of transplantation.

No study in stem-cell transplantation has evaluated pharmacologic and/or psychological interventions among patients with comorbid depression. Our results suggest active intervention should be evaluated because both quality of life and possibly survival could be improved. Such a study must consider that standard pharmacologic approaches with antidepressants, although useful in other settings, may not be as easily applied here because of possible interactions with multiple other drugs. Effective clinical doses may be higher or lower than standard doses. Combination with active psychological intervention, such as cognitive-behavioral therapy, may be more effective.

This study has several limitations. The instrument used to operationally define depression is not a standard one, although the criteria used to define depressive syndrome have content validity, and, when satisfied, should prompt further psychological evaluation. We recognize that the somatic elements of depression used in our definition (anxiety, difficulty concentrating, feeling isolated, fatigue, or memory loss) may not be as specific for the diagnosis of depression in this population. Nevertheless, the sensitivity and specificity we attained for our system of classifying depressive syndrome is comparable to validation studies of depression scales such as the Beck’s Depression Inventory, Hamilton Anxiety and Depression scale, Zung Self Rating scale, and the Center for Epidemiologic Studies Depression scale.^38-42 We used chart review as the gold standard for these calculations. It is quite possible that this measure underestimates clinical depression, and that patient report is actually a more accurate reflection of depressive syndrome. If so, then the appropriate response to a positive predictive value of 29% is not to raise the threshold of the instrument, but rather to implement greater efforts in routine clinical care to identify depressive syndrome.

Another limiting factor is the potential effect of the nonresponders on the association of depression with survival. Our data, however, suggest that the nonresponders may even be more depressed and have lower quality-of-life scores, as they were much more likely to die or relapse than responders. If so, then inclusion of these patients might have increased the observed association between depression and mortality.

Our study instrument was not designed to look at depressive symptoms before transplantation or before 6 months after transplantation. Prospectively collected data on other aspects of mental health, physical health, social support, and prognostic expectations before transplantation suggest that the two groups started out with similar physical characteristics. However, patients who will subsequently report depressive symptoms at 6 months are more likely to have pretransplant deficits in mental health and outlook. This observation suggests that patients at risk for depressive syndrome might be identified by pretransplant screening, thereby allowing more active monitoring and earlier intervention. By 6 months, the depressed and nondepressed groups were clearly distinguishable on all quality-of-life domains, and these changes were maintained at 12 and 24 months. Although the survival difference was seen only in the first 12 months after transplantation, the small number of events in the two cohorts after 12 months may limit our ability to detect a difference in the two groups beyond this time.

Finally, we did not collect any data that could address potential mediating mechanisms for depression’s effects, such as health behaviors (threshold for seeking medical evaluation for symptoms, compliance with treatment), availability of tangible social support, and physiologic parameters such as susceptibility to infection.

In summary, we find support that depressive symptoms among patients who have undergone stem-cell transplantation are associated with higher mortality, at least in the period from 6 to 12 months after transplantation, after controlling for other patient-, disease-, and transplantation-related prognostic factors. Although our study is not definitive, we believe our data provide compelling support for future studies to evaluate the role of pharmacologic and psychological intervention for depression in improving quality of life and possibly survival.

	ACKNOWLEDGMENTS

 
Supported in part by grant no. CA75267-03 from the National Institutes of Health, Bethesda, MD, and the Amy Strelzer-Manasevit Scholars Program, Minneapolis, MN.

We thank Christina Caron and Samantha Bennett for their help with study coordination and Sandy Sobotka for administrative assistance.

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Submitted October 30, 2001; accepted January 16, 2002.

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This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Save to my personal folders Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Loberiza, F. R. Articles by Lee, S. J. Search for Related Content PubMed PubMed Citation Articles by Loberiza, F. R., Jr Articles by Lee, S. J.