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© 1999 American Society for Clinical Oncology Health-Related Quality of Life 1 Year After Allogeneic or Autologous Stem-Cell Transplantation: A Prospective StudyFrom the Norwegian Cancer Society, Department of Oncology, Norwegian Radium Hospital, and Medical Department A, National Hospital, Oslo, Norway; Palliative Medicine Unit, Department of Oncology, Trondheim University Hospital, and Norwegian University of Science and Technology, Faculty of Medicine, Unit for Applied Clinical Research, Trondheim, Norway; and Medical Research Council Cancer Trials Office, Cambridge, United Kingdom. Address reprint requests to Marianne Jensen Hjermstad, RN, MPH, Department of Oncology, The Norwegian Radium Hospital, Montebello, N-0310 Oslo, Norway; email mlhjerm{at}online.no
PURPOSE: To evaluate health-related quality of life (HRQOL) in adults treated with high-dose chemotherapy followed by allogeneic (SCT) and autologous (ASCT) stem-cell transplantation 1 year after transplantation, using data from concurrent lymphoma patients receiving combination chemotherapy (CT) as a reference. MATERIALS AND METHODS: Forty-one leukemia patients (SCT group), 51 lymphoma patients (ASCT group), and 85 CT patients completed the European Organization for Research and Treatment of Cancer QLQ-C30 questionnaire at baseline and after 1 year.
RESULTS: The SCT group (median age, 36 years) had better functioning scores and less symptomatology at baseline compared with the ASCT (median age, 41 years) and CT (median age, 37 years) groups. Statistically significant differences of 10 or more points on the 0 to 100 scales were found for 10 of 15 scales and items (P Patterns of change in HRQOL scores were different between groups during follow-up. A great improvement was found in the ASCT group (P < .01 for emotional and role function, fatigue, appetite, and constipation), whereas no significant changes were observed for the SCT group. CONCLUSION: Prospective studies with extended follow-up periods are necessary to separate a slow recovery process from more permanently reduced HRQOL after transplantation and to examine the late side effects from previous treatment.
HIGH-DOSE CHEMOTHERAPY (HDC) followed by allogeneic stem-cell transplantation (SCT) or autologous stem-cell transplantation (ASCT) is frequently used as a treatment modality for a number of malignant diseases.1 SCT is regarded as curative treatment for adult cancer patients with chronic myelogenous leukemia (CML) and acute myeloid leukemia (AML) who fail induction therapy.2 Long-term disease-free survival may be achieved in adults with high-risk acute lymphoblastic leukemia and myelodysplastic syndrome.2 ASCT is now regarded as standard treatment in relapsed high-grade non–Hodgkin's lymphoma (H-NHL) and relapsed Hodgkin's disease (HD) after chemotherapy.2 Additionally, ASCT is widely used in treating breast and testicular cancer.2 It is well known that these treatment modalities carry significant morbidity and mortality, and the acute and late side effects are well documented.3,4 Data on health-related quality of life (HRQOL), including the frequency and severity of late side effects and psychosocial sequelae, might aid in the follow-up and information on the steadily increasing numbers of long-term transplant survivors. Although this research is constantly progressing, most studies in bone marrow transplant recipients are small sized and retrospective or cross-sectional.5 Direct comparisons between studies are difficult because of differences in design and methods of definition and assessment of HRQOL. Many transplantation survivors seem to have good physical functioning and HRQOL 1 year after transplantation, although there seems to be a subgroup of patients for whom readjustment may take longer.6-17 The most frequently reported difficulties are related to inability to resume social roles, worry about the future, work-related problems, infertility, fear of relapse, and anxiety and depression, varying in severity and frequency, depending on time of assessment and methodology used.6-16,18-27 Prospective studies have been initiated to assess specific problems in SCT or ASCT patients, such as neurobehavioral difficulties,24 sexual functioning,28 and anxiety and depression.21,23 However, we identified only five prospective studies measuring HRQOL beyond the immediate posttransplantation period in patients with hematologic malignancies. Chao et al8 evaluated 58 ASCT patients every 90 days during the first year posttransplantation by a 14-item ad hoc questionnaire, including a linear analog scale for assessment of global quality of life (QOL). Patients were asked to evaluate their situation in three domains of HRQOL after 1 year, compared with pretransplantation. The large majority was satisfied with their appearance (98%) and sexual activity (64%), and 78% had returned to work. Global QOL was rated as good to excellent in 88%. Syrjala et al10 showed that 68% of 23 long-term allogeneic transplant recipients had returned to full-time employment with normal physical and psychologic functioning after 2 years, as assessed by several questionnaires, including the Sickness Impact Profile. Andrykowski et al19 assessed 24 SCT patients and four ASCT patients before and 12 to 16 months after transplantation by standardized questionnaires, including the Sickness Impact Profile and the Functional Living Index-Cancer. There was little change in scores over time, but reduced status after 1 year compared with baseline was associated with male sex and higher age at transplantation. Wettergren et al,29 using the European Organization for Research and Treatment of Cancer (EORTC) QLQ-C30 questionnaire, studied a small sample of 12 ASCT patients. The patients perceived their HRQOL and physical and psychosocial functioning 8 to 12 months posttransplantation to be as good as before transplantation. In a fifth prospective study, 86 patients with breast cancer or hematologic malignancies were assessed four times from pretransplantation through 1 year posttransplantation by the Functional Assessment of Cancer Therapy Bone Marrow Transplant Scale.30 Quality of life was significantly impaired during treatment but improved at the 1-year assessment for the 42 patients who completed the questionnaire at each assessment. We report a Norwegian prospective study, evaluating HRQOL by the EORTC QLQ-C30 questionnaire in 92 adults treated with HDC followed by SCT for leukemia or ASCT for malignant lymphoma. This article examines the study hypothesis that this high-intensity treatment does not in itself lead to impaired HRQOL, as assessed 1 year posttransplantation. The main objective is to compare the patients' HRQOL at baseline and after 1 year. Results from the SCT and ASCT groups are compared with results from a concurrent sample of lymphoma patients (CT group) receiving combination chemotherapy.
Patients Inclusion criteria required a hematolymphoproliferative malignancy, age above 16 years, fluency in oral and written Norwegian, cognitive capability of filling in the questionnaires, no present psychiatric disorder, and no prior history of cancer.
Transplantation patients. The inclusion period lasted 3 years from April 1993. All consecutive patients who were admitted for HDC and who met the eligibility criteria were invited to participate in the study. Over the 3-year period, 161 patients were approached, 76 at the National Hospital and 85 at the Norwegian Radium Hospital (Fig 1). The population in this report consists of all patients with completed questionnaires at baseline and after 1 year (41 in the SCT group and 51 in the ASCT group). The diagnoses in the SCT group encompassed 25 patients (61%) with CML, 12 patients (29%) with AML, and four patients (10%) with acute lymphoblastic leukemia. The disease distribution in the ASCT group was 11 (21%) with HD, 30 (59%) with H-NHL, and 10 (20%) with low-grade non–Hodgkin's lymphoma (L-NHL) according to the Kiel classification.31
Chemotherapy patients.
Data Collection
Methods
Data Analysis
Forty-one of the 42 SCT patients (98%) who remained in the study after 1 year completed the questionnaires (Fig 1). One patient failed to answer. Three patients who had withdrawn previously did not give any reasons on the statement coupons. The questionnaire package was completed after 1 year by 51 of the 52 (98%) remaining subjects in the ASCT group (Fig 1). One patient withdrew without giving any reason on the statement coupon. Three patients had previously declined further participation owing to relapse. Compliance among the CT patients who remained in the study after 12 months was 94% (85 of 90 patients) (Fig 1). Five patients failed to return the questionnaires. Five patients had withdrawn during follow-up. Four gave no reason, and one found the study irrelevant because treatment was completed. No statistically significant differences were found between the three groups with respect to age and sociodemographic variables (Table 1).
The distribution of lymphoma diagnoses was significantly different (P < .0001) when the ASCT and CT groups were compared, as expected because of the different indications for each treatment (Table 1). The median interval in months from diagnosis to transplantation was significantly longer (17 v 11; P = .006) in the ASCT group than in the SCT group (Table 2). All ASCT patients had received combination chemotherapy before transplantation, compared with only 16 (39%) of the SCT patients. The SCT group had spent significantly more days in protective isolation compared with the ASCT group (P < .0001), with a median of 31 days versus 21 days (Table 2). None of the SCT patients had undergone total-body irradiation (TBI), as opposed to 34 (67%) of the ASCT patients (13 Gy in 10 fractions). Twelve SCT patients (29%) had received stem cells from a matched unrelated donor. Radiotherapy had not been used in the SCT group as part of the primary treatment but was given to 13 ASCT patients (29%), with mantle field and mediastinal fields in three and four patients, respectively. Radiotherapy after transplantation was given to four ASCT patients (8%). Eleven SCT patients (27%) had developed chronic graft-versus-host disease (GVHD), two with extensive disease. Two SCT patients (5%) and nine ASCT patients (18%) relapsed within 1 year after transplantation. Sixty-nine percent of those who had been working or studying before transplantation had resumed these activities.
All patients in the CT group had received chemotherapy according to standard treatment protocols, depending on the underlying disease (data not tabulated). Twenty-five patients were treated with combination chemotherapy, using multiple agents in various cycles. Cyclophosphamide, hydroxydaunorubicin, vincristine, and prednisone was the most frequently used regimen in H-NHL (35%), representing the treatment of choice, and was given to 27 (61%) of these patients. Epirubicin, bleomycin, vinblastine, and prednisone was the most frequent regimen for HD patients and was given to 14 of these patients (35%). Radiotherapy subsequent to chemotherapy was given to 23 HD patients and 12 patients with H-NHL, most frequently as mantle fields alone (11 HD patients [28%]). Seventy-three percent of patients in the CT group (n = 62) were in complete remission after 1 year, whereas 17 patients (20%) were in partial remission, and six (7%) had relapsed. Sixty-five percent of those who were working or attending school before diagnosis had resumed these activities after 1 year. Overall, the SCT and ASCT patients had few clinical toxicity symptoms, according to World Health Organization toxicity criteria,35 at the 1-year medical examination. The majority of SCT patients (68% to 98%) had no signs of toxicity (grade 0) on the different items, compared with 70% to 100% in the ASCT group. Grade 4 toxicity was noted in two SCT patients (low hemoglobin and peripheral neurotoxicity) and in two ASCT patients (low platelet count and allergic reaction to medication). Four SCT patients (10%) had slightly reduced lung function (grade 1). One had received medication for persisting lung infections. Impaired lung function was found in 13 ASCT patients: grade 1 in six patients (12%) and grade 2 in seven patients (14%). Seven patients had received TBI (one with additional mediastinal fields after ASCT), one had not received any radiation treatment, whereas five had received radiotherapy as part of their primary treatment (mantle field, three patients; inverted Y field, one patient; head-and-neck, one patient). Recurrent pneumonias, Pneumocystis carinii pneumonia, heart failure, and impaired ventilatory capacity had been clinically diagnosed and treated in four individual ASCT patients.
EORTC QLQ-C30
Baseline (T1)
Mean scores at T1 for those who completed the questionnaire at T1 but did not remain in the study until T2 are listed in Table 3 (21 SCT patients, 18 ASCT patients, and 38 CT patients). The differences in mean scores between compliers and noncompliers at T1 in the SCT group were in the direction of poorer status among the noncompliers. Differences were 10 points or more and statistically significant for role function, nausea and vomiting, and sleep disturbances (P < .01). In the ASCT group, mean scores of the noncompliers were fairly similar to those of the compliers at T1, and no statistically significant differences were found in the CT group. Regarding sociodemographic characteristics, no statistically significant differences between compliers and noncompliers were found in any of the groups.
After 1 Year (T2)
Development from T1 to T2
Total-Body Irradiation
Graft-Versus-Host Disease
Relapse
Multivariate Approach
Patient group was significantly associated with global QOL, fatigue, and sleep disturbances, in the direction of better scores in the SCT group (P values from .006 to < .0001). Lower age was significantly associated with better global QOL (P = .01). There was significantly more dyspnea (P = .002) among those who were single compared with those who were married or living with a partner (Table 4). Relapse was added to the model at T2 and was significantly associated with all outcome variables except physical function and global QOL, in the direction of reduced function and more symptoms with relapsed disease (Table 4). Living situation was significantly associated with dyspnea (P = .01). Patient group showed no statistically significant association with any of the outcome variables at T2. The baseline values of the different variables were entered into the analyses to examine the relationship between scores at T1 and T2 (data not tabulated). The baseline values were significantly associated (P < .0001) with the scores at T2 for all variables except dyspnea in the direction that higher scores at T1 predicted higher scores at T2. Relapse was still significantly associated with all variables except physical and social function (P values from < .002 to .01). A separate regression analysis was performed for the SCT and ASCT groups at T1, including the same background variables as the other regression analysis. A dichotomous variable regarding stage of disease at transplantation (1, first remission or CML chronic phase; 2, second remission or later, second relapse or later; see Table 2) was added to the model to examine the extent of previous cytotoxic treatment as a possible predictor of the great baseline differences across these two groups. This was considered as an indicator of prior treatment encompassing the stage of disease, its duration, and the length, intensity, and number of previous chemotherapy cycles. Transplantation at a later stage was significantly associated with more dyspnea (P = .001), as was living alone (P = .004). No significant associations were found with social function. Treatment group (SCT v ASCT) was significantly associated with the other outcome variables (P values from .002 to < .0001) in the direction of better scores in the SCT group (data not tabulated), as in the other regression analysis. For clinicians, the individual change in mean scores from T1 to T2 is interesting, because the situation might change substantially for some patients in either direction, whereas it remains fairly stable for others. Thus, patients were categorized as "improvers" or "nonimprovers" (those who improved or reduced their baseline scores from T1 to T2 by 10 points or more, respectively), consistent with our definition of clinically significant changes. Physical function and global QOL were selected as dependent variables because of their relationship with both physical and sociodemographic variables. Logistic regression was used to look at the relationship between improvers or nonimprovers with the same background variables as in the multiple regression analyses. Relapse was significantly related to being a nonimprover in physical function (P = .003) and global QOL (P = .007), whereas higher baseline scores in physical function and global QOL were associated with being an improver (P < .0001). Belonging to the SCT group was inversely related to being a nonimprover with regard to global QOL (P < .0001).
This study revealed major differences in HRQOL scores among the SCT, ASCT, and CT groups at baseline. The SCT group reported better functional scores and less symptomatology than the other two groups. Smaller differences across groups were seen at the second assessment. The results at T2 contradicted our clinically based hypothesis of a better 1-year outcome in the ASCT group compared with the SCT group, owing to shorter time in protective isolation, fewer treatment-related side effects, and no risk of GVHD. However, the literature is ambiguous on this point, and many HRQOL studies fail to analyze the groups separately. A uniform ranking of SCT patients lower than ASCT patients lower than CT patients was reported from a retrospective assessment of HRQOL by the EORTC QLQ-C30 in an AML clinical trial.27 Increased physical problems and symptomatology were reported in SCT patients compared with ASCT patients,27,41 but some investigators report the opposite24 or no significant differences.14,21,22 Heterogeneity with respect to diagnoses and prior treatment in these studies might explain these variations. The change in scores from T1 to T2 was different across groups. No significant changes were found in the SCT group over the year of follow-up. We failed to find significant differences regarding chronic GVHD at T2. Some researchers have reported that the presence of GVHD is associated with poor outcome posttransplantation,10,11,20,22 whereas no such relationship has been found in other studies.15,18,21,41 Only two patients in our study had extensive GVHD. Such small numbers, however, imply that chance findings cannot be ruled out. The change in the ASCT and CT groups from T1 to T2 was in the direction of better functional status and less symptomatology. The changes in scores from T1 to T2 described in this report were considerably larger than those found by Andrykowski et al19 and yield more information about the patients' HRQOL than a comparison of the group mean scores only. The reason for improvement in HRQOL from T1 to T2 in the ASCT group might be that these patients were sicker than the SCT patients at baseline, or that they had undergone more chemotherapy of higher intensity over a longer period of time. This is supported by findings that the difference between groups in median time from diagnosis to transplantation was significant (P = .006), that 61% of the SCT group were CML patients who had been treated with a comparatively mild regimen consisting of hydroxyurea alone or in combination with interferon, and that more ASCT patients were in second or later remission at transplantation com-pared with SCT patients (80% v 19%; P < .0001). Dyspnea was a major problem in the ASCT group at both assessments. Eleven of the 17 ASCT patients who had not received TBI were previously treated with radiotherapy, involving the lungs in seven cases. This, together with smaller fractions than commonly used (13 Gy in 10 fractions), could partly explain why our anticipation of more problems among those who had gone through TBI was not borne out. Similar results have also been reported elsewhere.9 The reason for the positive change from T1 to T2 in the CT group, especially regarding role, social and emotional function, pain, and fatigue, is probably that these patients were newly diagnosed with malignant lymphoma at T1, were clinically ill, and were about to start chemotherapy. Most patients seemed to have recovered reasonably well after 1 year, judging from the functioning scales in particular, with mean scores ranging from 75 to 89 on the 0- to 100-point scales. Furthermore, two thirds of the patients in all three groups were back to work or school. The Karnofsky performance scores of the two transplantation groups after 1 year were high (median, 90%), indicating ability to carry on normal activity.34 These results correspond well with those of other published studies using the EORTC QLQ-C30.15,27,29 However, recovery might take longer for some individuals, consistent with prior prospective reports.8,10,19,29,30,42 Regardless of patient group, the multivariate approach showed that relapse was associated with HRQOL at T2 with regard to changes in individual and group mean scores. The definition of 10 points as a clinically significant change in scores in the logistic regression analyses does not mean that smaller differences are not perceptible for patients. The hope for cure is extremely small when relapse occurs after transplantation, and this still represents the major obstacle for success in ASCT patients. A clinical implication of this observation could be the offering of special support programs, which might be beneficial to these patients. What should be kept in mind when interpreting the results is the magnitude of the difference in scores on the EORTC QLQ-C30 and their clinical significance. The magnitude of comparisons performed between subgroups imposes restrictions regarding generalizability. Although the groups were small in some of the analyses, we assume that the differences greater than 10 points were clinically significant and that these were unlikely to be chance findings if supported by P values lower than .01. One limitation of this study is related to the variability and impact of the patients' pretransplantation treatment experiences, which are difficult to assess. In the multiple regression analysis encompassing all groups, treatment group was significantly associated with HRQOL at baseline, but it had little impact at T2. As a consequence, a separate regression analysis, in which stage of disease at transplantation was included, was performed to assess the history of pretransplantation treatment. However, this analysis yielded little new information, with treatment group still being significantly associated with four of six outcome variables. We also attempted to quantify prior treatment by giving the patients a score from 1 to 3 (light, medium, and high), based on an evaluation of the number and agents of previous cycles of chemotherapy, duration and intensity of treatment, and previous radiotherapy. The scores were assigned by three independent clinicians. When the stage-of-disease variable was replaced by this variable in the regression model, almost identical results were obtained. The advantages of the stage-of-disease variable over the variable that implies weighting of the treatment are that it is a less arbitrary and more objective way of trying to quantify pretransplantation treatment and that the subgroups involved in the analyses do not become too small. It might be that the baseline differences between the SCT and ASCT groups are due to factors related to the leukemia and lymphoma diagnoses, respectively, and not only to previous treatment or other patient characteristics that we have not been able to quantify. A second limitation of this study is that the differences between the two transplantation groups, on the one hand, and the CT group, on the other, might in fact be greater than reported here. Among those who failed to respond, there were more patients with progressive disease in the two transplantation groups than in the CT group. Some of the nonrespondents in the CT group stated upon request that they were living normal lives and found the study irrelevant. Consequently, a healthier subset of the transplantation patients might have complied, whereas the opposite could have happened in the CT group. This implies that the CT group should be regarded only as a reference group, not as a comparison group. Although the underlying diagnoses were similar to those in the ASCT group (lymphoid malignancies), the patients were distinctly different from the SCT and ASCT patients with respect to important medical variables that are known to influence HRQOL, such as prior treatment experience and prognosis. Withdrawal of patients in prospective studies can introduce a selection bias. An underestimation of problems may occur if only those with good performance status comply. This does not seem to be a major problem in our study, because significant differences in mean scores between compliers and noncompliers at T1 were found only in the SCT group, and no differences were found regarding the sociodemographic characteristics. A third limitation is the short duration of follow-up. Long-term side effects caused by previous cytotoxic treatment or the preparative regimens might not become manifest until years after transplantation, as evidenced in a study of fatigue among HD survivors.42 Such long-term side effects are not properly assessed with only 1 year of follow-up. Furthermore, these side effects might lead to greater differences between groups as time goes by. The strength of this study is related to its prospective design and the use of a well-validated cancer-specific HRQOL questionnaire. The analyses of the change of scores over time within patient groups should be of great importance for clinical practice. It has led to an extended follow-up of the patients in this study so that the different development across groups during the first year of follow-up can be investigated further. The prospective design of this study revealed distinct baseline differences between patient groups, as reflected in the regression analyses, whereas patient group was less important after 1 year. This shows the importance of undertaking prospective studies and demonstrates why cross-sectional studies might be biased. Our results were consistent with previous reports in that most patients seemed to do reasonably well 1 year after transplantation, particularly in the physical domains. Extended follow-up periods are nevertheless required to differentiate a slow process of recovery in some patients from a more permanent reduction of HRQOL posttransplantation and to assess the long-term side effects of previous treatment.
Supported by grant no. 93094 from the Norwegian Cancer Society. We greatly appreciate the sincere interest and valuable help received from Harald Holte and Lorentz Brinch. We give special thanks to Bente Moldaunet, Eldbjørg Hanslien, and Siri Hjerpeset for data management. We also thank Grethe Lauvvang, Eldbjørg Vorkinn, Elisabeth Normannvik, Anne Kristine Lilja, and Hilde Beate Vik for follow-up of patients.
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Copyright © 1999 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
.01) between the SCT and ASCT groups. Global quality of life (79 v 58, P < .0001), role function (83 v 65, P = .001), sleep disturbances (6 v 28, P < .0001), and fatigue (25 v 44, P = .0001) deviated most. The differences were 10 or more points for seven of 15 scales and items comparing the SCT and CT groups, with sleep disturbances (6 v 35, P < .0001) and pain (11 v 29, P < .01) deviating most. Differences across groups were smaller after 1 year; cognitive function was the only scale with a statistically significant difference (ASCT 80 v CT 89; P = .002). 
2 tests (nominal categorical variables), Wilcoxon's test for independent and paired samples (scale and item scores), and Kruskal-Wallis analyses of variance where appropriate. A conservative P value of .01 was taken to indicate statistical significance with all tests, because of multiple comparisons. Patients were not omitted from analyses because of partially incomplete data, and missing values were imputed by the techniques advocated in the EORTC manual.
