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Recovery After Stem-Cell Transplantation for Hematologic Diseases

From the Department of Adult Oncology and Department of Pediatric Oncology, Dana-Farber Cancer Institute, Boston, MA; and American Medical Center Cancer Research Center, Denver, CO.

Address reprint requests to Stephanie Lee, MD MPH, Center for Outcomes and Policy Research, Dana-Farber Cancer Institute, 44 Binney Street, Boston, MA 02115; email stephanie_lee{at}dfci .harvard.edu.

	ABSTRACT

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
PURPOSE: Although the number of autologous and allogeneic stem-cell transplantations (SCT) is increasing, relatively little information about recovery after transplantation is available. Quantitative information appropriate for patient counseling is difficult to discern from the literature. We sought to suggest reasonable expectations for recovery and symptoms after SCT for hematologic malignancies and other disorders using the following measures: (1) objective measures of health status, such as frequency of clinic visits, need for rehospitalization, medication usage, work status, and overall and event-free survival; (2) qualitative assessment of quality of life, such as returning to a normal life, resumption of normal activities, satisfaction with appearance, and whether recovery has occurred; and (3) quantification of specific bothersome symptoms.

PATIENTS AND METHODS: Autologous and allogeneic SCT recipients at a tertiary-care transplant center participated in the prospective, longitudinal questionnaire study.

RESULTS: Three hundred twenty patients were studied. Questionnaire response rates at 6, 12, and 24 months range from 85% to 88% among survivors. Although autologous patients had better event-free and overall survival, fewer symptoms, and more complete recovery at 6 months, these advantages had largely equalized by 12 months. Specific bothersome symptoms were reported by less than 24% of patients after transplantation, except for fatigue and financial and sexual difficulties, which were more prevalent.

CONCLUSION: These findings may help counsel patients considering transplantation and educate them about reasonable expectations for recovery. Overall, the low level of bothersome symptoms and continued recovery through the first year after transplantation are encouraging.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
ALTHOUGH STEM-CELL transplantation (SCT) is able to cure a variety of malignant and nonmalignant hematologic diseases, the procedure is still associated with significant morbidity and mortality. The high doses of chemotherapy, frequently combined with total-body irradiation (TBI), cause extended hospitalizations and prolonged recovery periods. Informed consent discussions about the risks and benefits of SCT likely cover the procedure itself and the probability of disease-free survival. However, it is not clear how patients are informed about potential long-term morbidity because concrete estimates of symptom prevalence after transplantation and reasonable expectations for recovery are difficult to discern from the literature.

Many patients considering transplantation rely on their physicians or anecdotal personal accounts from other patients who have undergone SCT to learn about the process. We sought to generate more reliable data on their likely short- and long-term outcomes by surveying the full population. In particular, we wanted to pose questions and provide qualitative and quantitative answers about recovery after transplantation that would be meaningful to future patients considering these procedures. We specifically tried to capture summary information in ways understandable to patients, such as the percentage of patients bothered by certain symptoms, or who rate their health as excellent, or who report that life has returned to normal and they are back to work. Some patients may factor these considerations into their decision to undergo transplantation. Others may gain reassurance from this information; it may help them to envision life after transplantation and conserve their resources accordingly.

Transplantations are broadly divided into autologous (from the patient) or allogeneic (donated by another individual) procedures depending on the source of repopulating stem cells. In general, autologous transplantations are thought to be less dangerous, but to entail a greater risk of relapse, than allogeneic procedures. In most cases, a clear recommendation between autologous and allogeneic transplantation can be made after consideration of a patient’s disease, stage, and donor availability. A few patients (such as those with acute myelogenous leukemia, non-Hodgkin’s lymphoma, multiple myeloma, and chronic lymphocytic leukemia) may consider either autologous or allogeneic transplantation and might benefit from comparative data. Because our program has an active interest in both types of transplantation, we had the opportunity to observe a large cohort of patients prospectively. Data collected before transplantation and at 6, 12, and 24 months after transplantation form the basis for this report.

	PATIENTS AND METHODS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Study Population
All patients scheduled for autologous or allogeneic transplantation at the Brigham and Women’s Hospital or Dana-Farber Cancer Institute were eligible for participation. Enrollment began at the Brigham and Women’s Hospital in August 1996 and at the Dana-Farber Cancer Institute in January 1997. Patients who were older than 18 years of age and scheduled for either autologous or allogeneic transplantation within 1 week to 3 months of baseline survey completion were eligible. Patients were contacted by the principal investigator (S.J.L) to describe the study, then mailed questionnaires and a self-addressed, stamped envelope. Patients who could not be contacted before admission for transplantation because of logistic reasons or who did not speak or read English were not eligible for the study. Patients who elected not to participate in the study or did not return baseline questionnaires also were not enrolled. Surviving participants were mailed follow-up questionnaires at 6, 12, and 24 months. Results reported here describe data collected before May 1, 2000, although data collection continues.

Patients undergoing any type of allogeneic transplantation were pooled for analysis. This group included patients receiving transplants from related or unrelated donors. They could be HLA-matched or mismatched. T-cell depletion (TCD) or methotrexate/cyclosporine (MTX/CSA) was used for graft-versus-host disease (GVHD) prophylaxis. The five patients undergoing syngeneic transplantations were grouped with the autologous patients for analysis.

Patients were treated on a variety of protocols according to attending physician or patient preference. Broadly, they could receive autologous purged^1,2 or nonpurged SCTs and related- or unrelated-donor, matched or mismatched grafts. Most of the allogeneic recipients received cyclophosphamide and TBI as a preparative regimen unless contraindicated by prior irradiation, in which case they received busulfan/cyclophosphamide. Autologous patients received either cyclo-phosphamide/TBI,³ melphalan/TBI, or cyclophosphamide/etoposide/carmustine.⁴ GVHD prophylactic regimens included MTX/CSA +/- corticosteroids, tacrolimus, cyclosporine/prednisone, or TCD using an anti-CD6 antibody and complement.⁵ Specific details of the transplantation regimens have been published previously.^1-5

Medical care after transplantation was dictated by the patient’s transplant physician. In general, autologous patients remained off work, limited their public exposure, took medications to prevent pneumocystic pneumonia, and wore mask and gloves in public for 2 to 6 months, whereas allogeneic patients were placed on such restrictions for 4 to 12 months.

Data Collection
Patients were surveyed by mail at baseline, 6, 12, and 24 months using both standardized and constructed items. This report includes qualitative information on symptoms and feelings about the transplantation process. These data were collected using items constructed specifically for this study because standardized assessment tools were not available. Questions were formulated and the symptom list developed after a review of the literature and input from transplant physicians, nurses, and patients. The survey was then pilot tested on a limited number of posttransplantation patients for clarity and ease of completion. These measures yielded the following three types of information on recovery after transplantation: (1) objective measures of health status such as frequency of clinic visits, need for rehospitalization, medication usage, work status, and overall and event-event free survival; (2) qualitative assessment of quality of life, for example whether life has returned to normal, whether normal activities were resumed, satisfaction with appearance, and whether recovery has occurred; and (3) elicitation of specific bothersome symptoms. Results of the standardized portion of the survey will be reported separately because they generate numerical summary scores that we feel are less useful for patient education and decision-making.

The following specific data were collected and included in this report: Baseline questionnaires elicited information on sociodemographics (age, sex, marital status, race, education, and work status) and general health status (excellent, very good, good, fair, and poor). Follow-up surveys collected information on return to work, physician visits, hospital admissions, medication use, agreement with qualitative statements ("Life has returned to normal," and "I feel back to my old self") using a scale from strongly disagree to strongly agree, and prevalence and severity of symptoms such as fatigue, anxiety, and pain, rated as I do not have this symptom, not bothered at all, bothered a little, bothered a lot, extremely bothered. All three follow-up surveys were identical and addressed recovery issues. (A copy of the survey may be obtained by contacting the corresponding author.) Overall and event-free survival of the cohort were calculated as of May 1, 2000, using data from our clinical database.

Statistical Methods
Demographics. Descriptive statistics are reported for autologous (including syngeneic recipients) and allogeneic study participants. Populations were compared using the ² or Fisher’s exact test for categorical or binary variables, and the Mantel-Haenszel trend test for ordered categorical variables. The Wilcoxon rank sum test was used for continuous variables. Logistic regression was used to investigate whether the study population differed from the entire population of patients undergoing transplantation during the study period. Explanatory variables included age, sex, race (white v other), disease stage, and type of transplantation (autologous v allogeneic). In separate regressions limited to allogeneic patients, type of GVHD prophylaxis (TCD v immunosuppressive therapy), degree of matching, and donor type were also included as independent variables. A P value less than .05 was considered significant.

Survival. Overall and event-free survival of the cohort as of May 1, 2000 were calculated from the date of transplantation using the Kaplan-Meier method. For event-free survival, relapses and deaths were considered events.

Measures of recovery. Patient responses regarding symptoms and quality of life after transplantation measured on Likert Scales were dichotomized into bothered a lot or extremely bothered versus not having the symptom, not bothered at all, or bothered a little, and somewhat or strongly agree versus neutral or disagree. Recovery at 6, 12, and 24 months are reported both as absolute and conditional rates. The absolute probabilities use the entire cohort of patients enrolled before transplantation as the denominator, whereas conditional probabilities only consider the cohort of surviving patients who return surveys. The absolute percentages answer the following question: what are my chances of being alive and in good health at 1 year? The conditional probabilities, alternatively, address the following question: if I survive at least 1 year, what are my chances of being in good health? Note that the absolute percentages incorporate both mortality and morbidity (shown in Figs 1 and 2), whereas the conditional probabilities reflect morbidity only (Tables 1, 2, and 3). For consistency and to allow comparison with other results from cross-sectional studies reported in the literature, the text refers to conditional probabilities unless otherwise noted.

View larger version (50K): [in this window] [in a new window]   Fig 1. Absolute proportion of patients at 6, 12, and 24 months experiencing the listed good outcomes.

View larger version (62K): [in this window] [in a new window]   Fig 2. Absolute proportion of patients at 6, 12 and 24 months somewhat or strongly agreeing with the listed statements or indicating very good or excellent health.

Association of baseline patient characteristics with measures of recovery. Selected outcomes at 1 year (return to work, school, or homemaking, bothersome fatigue or sexual difficulties, and agreement with the statement "I have recovered from my transplant") were modeled using logistic regression. These outcomes were selected for modeling on the basis of prior reports in the literature, their frequency in our study population, or relevance as a summary measure of recovery. Possible exploratory variables included age, sex, disease stage, education (college or postgraduate degree v other), and type of transplantation. In separate regressions limited to allogeneic patients, we also included type of GVHD prophylaxis (TCD v immunosuppressive therapy) and donor type. A P value less than .05 was considered significant. We were not able to evaluate the effects of TBI or use of a mismatched donor.

	RESULTS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Patient Characteristics
During the time period of this study, 728 patients underwent transplantation; 320 (44%) were enrolled onto the study, 138 (19%) were sent surveys but did not complete baseline assessments, and 270 (37%) were not offered enrollment either because they could not be contacted by phone before admission, they did not speak English, or the investigators were not aware of their admission. No patient was purposefully excluded from the study. Of those patients sent baseline surveys, 320 (70%) of 458 agreed to participate and are included in this analysis (114 autologous, five syngeneic, and 201 allogeneic [113 related-donor and 88 unrelated-donor] patients. Figure 3 shows the number of patients completing surveys at each time point and the reasons for missing data.

View larger version (24K): [in this window] [in a new window]   Fig 3. Enrollment and follow-up of the cohort.

Table 4 summarizes the characteristics of patients included in the study. At baseline, autologous and allogeneic patients were similar demographically and in reported overall health. There were no differences in terms of sex, marital situation, race, education, percentage employed at diagnosis or at time of survey completion, or the percentage reporting excellent, very good, good, fair, or poor health. However, the autologous patients were significantly older than the allogeneic recipients, were more likely to have intermediate than early stage disease, were less likely to receive TBI, and represented a different spectrum of diseases. Preliminary evaluation showed that outcomes were similar for 59 TCD (29%) and 142 MTX/CSA patients (71%), and these groups were pooled for analysis.

Objective Measures of Recovery
Objective measures of recovery included overall survival, event-free survival, frequency of clinic visits, readmission to the hospital, need for medications, and return to school, work, or homemaking activities as listed in Table 1 and Fig 1. At 6 months, surviving autologous patients were more likely than surviving allogeneic patients to report returning to clinic once per month or less (92% v 58%, respectively), to report being off medications, and, for those working, in school, or homemaking before transplantation, to have resumed those activities (46% v 29%, respectively). Rehospitalization was common in both groups, with 26% of autologous and 51% of allogeneic patients requiring readmission. Autologous patients, compared with allogeneic patients, had superior overall survival (89% v 64%, respectively) and event-free survival (86% v 60%, respectively). Thus, at 6 months, autologous patients showed better recovery than allogeneic patients on these measures regardless of whether conditional (analyzing only survivors) or absolute (including all transplanted patients regardless of survival status) probabilities were considered (see Results, under "Measures of recovery").

By 1 year, more than 80% of survivors in both groups saw a physician once per month or less and the majority had returned to work, school, or homemaking (61% of autologous patients and 58% of allogeneic patients). Forty-three percent of autologous and 25% of allogeneic patients were off all transplant-related medications by 1 year. At 2 years, further improvements were seen for both groups. Frequency of physician visits (97% of autologous patients and 86% of allogeneic patients seeing a physician once per month or less), medication usage (56% autologous and 44% allogeneic patients off medications) and return to work, school, or homemaking (70% autologous v 67% allogeneic patients) were stable or improved among survivors. Overall survival was still better for the autologous than allogeneic patients (78% v 48%, respectively), but the higher relapse rate caused the event-free survival to be similar (54% v 39%, respectively).

The percentages reported in Table 1 represent conditional probabilities reflecting the experiences of surviving patients who return surveys. Note that 5% to 13% of data are missing at each time point, and no assumptions were made about the recovery of these patients. Figure 1 shows the absolute probabilities that include all patients who undergo transplantation and are eligible for inclusion in the analysis regardless of whether they survive or return surveys. For both autologous and allogeneic patients, the frequency of clinic visits, ability to discontinue medications, and return to school, work, or homemaking do improve with time, although the absolute probabilities of the good outcomes are often considerably lower than the corresponding conditional probabilities. Note also that interpretation of the smallest cohort, autologous patients transplanted more than 2 years before the time of the analysis, must be made cautiously because they actually had a lower mortality rate than those transplanted more recently.

Qualitative Statements About Recovery
Patients indicated their agreement or disagreement with a number of qualitative statements about recovery as listed in Table 2. Overall, the difference between autologous and allogeneic patients was most striking at 6 months when both absolute and conditional probabilities suggested better recovery in the autologous patients. However, for almost all categories, less than 60% of patients indicated recovery, and on most items, it was closer to a third. The low conditional probabilities suggest that both groups of patients perceived their recovery was just beginning. Only two measures showed substantial recovery by 6 months in autologous patients; three-fourths reported satisfaction with appearance and enjoying social activities.

Figure 2 shows selected absolute probabilities for qualitative assessments of good outcomes, such as life returning to normal, recovery from transplantation, and very good or excellent health. When both mortality and failure to return surveys are considered, less than 50% of patients achieved the good outcomes.

Symptoms
Patients were presented with a list of 12 symptoms and asked to indicate how bothered they were on a five-point Likert scale, ranging from I do not have this symptom to extremely bothered. Table 3 shows the percentage of autologous and allogeneic patients reporting being bothered a lot or extremely bothered at 6, 12, and 24 months. Overall, patients were most likely to be bothered by fatigue, financial problems, and sexual difficulties. The prevalence of other symptoms (anxiety, depression, pain, difficulty concentrating, feeling isolated, mouth sores, painful joints, skin changes, and memory loss) was generally less than 20%. Even if the 5% to 13% of patients with missing data at each time point were assumed to be symptomatic, the prevalence of these rarer symptoms would be less than 30%. Autologous and allogeneic patients reported surprisingly similar symptomatology at most time points.

Association of Baseline Patient Characteristics With Measures of Recovery
Of all patients working, in school, or homemaking before transplantation, younger patients were more likely to return to these activities after transplantation. No baseline patient or transplantation characteristics were associated with bothersome fatigue, bothersome sexual difficulties, and agreement with the statement "I have recovered from my transplant" at 1 year.

	DISCUSSION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
We report measures of recovery at 6, 12, and 24 months after transplantation for our patients undergoing autologous and allogeneic SCT for hematologic diseases. Overall, we found that autologous patients began their recuperation sooner than allogeneic patients did, with detectable differences seen at 6 months. However, global measures of recovery continued to improve and were roughly equal at 1 year, by which point the majority of patients had recovered substantially. Between 1 and 2 years, little further recovery was detected. Our finding that approximately 60% of survivors return to work by 1 year is comparable with the conditional probabilities reported by others (50% to 70%).^6-10 Encouragingly, the prevalence of specific bothersome symptoms was low and less than 24%, except for fatigue, sexual difficulties, and financial concerns, which were much more frequent. Thus, patients may be counseled that although autologous patients begin their recovery sooner than allogeneic recipients, allogeneic patients catch up and report similar rates of recovery by 1 year. Approximately 60% of patients report return to some aspects of a normal lifestyle, although 40% continue to have some deficits.

We have chosen to report both absolute and conditional probabilities. Which is better to present when counseling patients? Although they sound very similar, the statement "your chances of surviving to 1 year and returning to work are X%" is very different from "if you survive, your chance of returning to work at 1 year are Y%." The absolute probability (X%) will be a much lower figure because it is the conditional probability (Y%) multiplied by the survival percentage at 1 year. For example, the conditional probability of returning to work at 1 year is 64% for surviving autologous patients and 59% for allogeneic patients. However, the chance of being alive and back to work at one year is 43% versus 26%, respectively, once mortality is taken into account. We have provided conditional probabilities in the tables, but illustrated our absolute probabilities in the figures so that clinicians and patients can choose the format that is preferable. Whether patients have a better understanding of or preference for absolute or conditional probabilities is unclear. Both can communicate realistic expectations as long as mortality and morbidity are clearly addressed.

Most studies of quality of life and recovery after SCT use a cross-sectional design.^6-9,11-33 Although response rates are generally excellent, only the conditional probabilities of the outcome for responders have been reported, a figure which excludes patients who are deceased or choose not to return the survey. In addition, because patients complete surveys at various times in their recovery process, the ability to report reasonable expectations for recovery by certain time points is limited. Nevertheless, the general message of the cross-sectional studies supports our results; although certain bothersome symptoms persist, overall quality of life, ability to return to work and other normal activities, and global measures of recovery are quite good. A few prospective, longitudinal studies have assessed patients before transplantation or very early after transplantation, then observed them for at least 1 year.^10,34-40 These studies report various rates of recovery and symptomatology but also support the conclusions of cross-sectional studies.

Because patients in our study were surveyed about a wide variety of symptoms and perceptions of recovery at standardized intervals after transplantation, we are able to comment on a broad range of measures and the tempo of recovery. We found that the low prevalence of specific symptoms at the time points 6, 12, and 24 months was similar, although perceptions of recovery improved between 6 and 12 months. Our finding that fatigue,^27,33 sexual dissatisfaction^13,20,26 and financial concerns¹⁰ are common in transplant patients confirms the reports of others. We can also add that fatigue and sexual difficulties do not seem to resolve with greater time from transplantation. Some evidence suggests that these concerns are common in the general population^28,41,42 and other patient groups,^6,22 so the high prevalence we observed must be taken in this context.

We present comparisons between autologous and allogeneic patients because it is generally believed that autologous procedures are safer and have less impact on quality of life. Much of our counseling and many of our activity restrictions are based on this perception. In addition, although most patients will receive a clear recommendation to undergo autologous and allogeneic transplantation based on considerations of event-free survival and donor availability, a few patients will have a choice between these procedures. The mortality among the allogeneic patients in our cohort was higher through at least 2 years after transplantation. However, the similarity in the conditional probabilities of other outcomes by 12 months suggests that the impact on quality of life may be more comparable than commonly believed. Attempts to find associations between selected outcomes at 1-year and baseline patient or transplantation characteristics were generally unsuccessful, implying that it may be difficult to identify large patient subsets at risk for poor recovery as we measured it.

These results represent data collection at a single institution, although the spectrum of diseases and transplantation protocols are generally similar to those at other large centers. We were able to collect data on 46% of all patients transplanted at our institution during this time period and have achieved 85% to 88% follow-up for surviving patients. We were not able to contact 32% of patients before admission, and 30% of those contacted failed to return their baseline surveys and are thus not included in this study. We know that patients who participated in our study were more likely to have good prognosis diseases, to undergo allogeneic transplantation, and be white, female, and older. Although our report reflects the experiences of only half of our total population, its prospective design allows us to calculate both the absolute and conditional probabilities for achieving the desired quality of life by specific time points. Our data suggest that patients who do not return follow-up surveys are more likely to have relapsed or be ill. Thus, nonresponders must be handled carefully or conclusions may be biased by loss of a population with the poorest health. We were careful to delineate the potential impact of patients who fail to return surveys and kept 6-, 12-, and 24-month responses separate to aid interpretability.

As transplantation becomes safer and greater numbers of patients survive the acute mortality risk, posttransplantation quality of life will become increasingly important to discuss as part of fully informed consent for the procedure.⁴³ Continued efforts to measure recovery after transplantation will allow future patients to understand and incorporate this knowledge into their own planning and decision making.

	ACKNOWLEDGMENTS

 
Supported in part by National Institutes of Health grant no. CA75267-01 and the Amy Strelzer-Manasevit Scholars Program.

We thank Taiye Odedosu for her help with study coordination, Richard Gelber, ScD, for helpful discussions, and our patients for sharing their experiences. Carol McGarigle, RN, Deborah Doss, RN, and Caroline Kuhlman, MS, RNCS, assisted with patient enrollment.

	REFERENCES

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
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Submitted January 25, 2000; accepted August 8, 2000.

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