We examined the course and the prevalence of a high fear of cancer recurrence (FCR) in patients undergoing allogeneic PBSC transplantation (hematopoietic SCT (HSCT)) before HSCT (N=239), 100 days after (n=150, and 12 months after allogeneic HSCT (n=102). The Fear of Progression Questionnaire-Short Form (FoP-Q-SF), the EORTC Quality of Life Questionnaire, and the Hospital Anxiety and Depression Scale were used. Pre-HSCT 36% of patients, 100 days after HSCT 24% of patients, and 1 year after HSCT 23% of patients fulfilled the criteria for high FCR (FoP-Q-SF cutoff=34). Being married (b=2.76, P=0.026), female gender (b=4.45, P<0.001) and depression (b=4.44, P<0.001) were significantly associated with FCR at baseline. One hundred days after HSCT, depression significantly predicted FCR (b=6.46, P<0.001). One year following HSCT, female gender (b=6.61, P=0.008) and higher depression were (b=4.88, P=0.004) significant predictors for FCR. Over the three assessment points, patients with high FCR had a significantly lower quality of life compared to patients with low FCR in physical functioning (P=0.019), role functioning (P=0.003), emotional functioning (P<0.001), cognitive functioning (P=0.003), social functioning (P<0.001) and global quality of life (P<0.001). Our data provide evidence that FCR is a prevalent problem in patients with hematological malignancies and has a significant adverse impact on health-related quality of life.
According to the World Health Organization (WHO), more than 7.6 million people died as a result of a malignant disease worldwide in 20081 and the WHO expects a significant increase in cancer deaths by an estimated 60% in 2030 from 7.4 million (2004) to 11.8 million2 due to the worldwide increase in life expectancy. However, due to rapid developments in early diagnosis and tumor therapies, survival probabilities have increased significantly in the last 20 years. Today, multimodal cancer treatments have enabled a large number of patients to be successfully treated and to survive longer than before. Nevertheless, the fact remains that many of those treatments are associated with significant physical and psychological side effects, symptom burden and co-morbidity for patients.
A highly prevalent psychological consequence of the disease and cancer treatments is fear of cancer recurrence (FCR). FCR is defined as the fear or worry that cancer will return, progress or metastasize.3, 4, 5, 6, 7 FCR is often conceptualized as a multidimensional phenomenon, including emotional components of anxiety and fear, and a cognitive dimension, including worry, preoccupation and intrusive thoughts.3,8,9
Prevalence estimates of FCR range between 22 and 99% among cancer survivors and FCR is considered to be one of the most distressing psychological consequences of cancer.3,9 The results of a systematic review indicate FCR to be significantly associated with younger age, maladaptive coping responses and poorer quality of life.3 Moderate evidence was found for the association with FCR and individual beliefs (for example, perceptions of vulnerability), as well as with demographic factors such as ethnicity and having younger children.3 No associations were found for cancer-related factors such as cancer type, stage and treatment type, socio-demographic factors including gender, education, employment, as well as social resources such as family support.3
Although FCR describes an appropriate and rational response to the real threat of a cancer diagnosis and invasive treatments,10 higher levels of FCR may become dysfunctional, causing concentration problems, sleep disturbances, anxiety symptoms such as panic attacks and rumination, and can affect well-being and quality of life.10 Cancer survivors who reported higher FCR used more health-care services, including outpatient and emergency room visits, and consumed more medication compared to patients with lower FCR.11 A recently published study indicated that FCR levels were highest in the peri-operative period, but remained stable throughout cancer treatments.12
Most studies about FCR were, however, conducted in breast cancer patients.13, 14, 15 Therefore, studies in patients with hematological malignancies treated with blood SCT (hematopoietic SCT (HSCT)) are still lacking. Taking into account that FCR is highly prevalent in cancer patients and higher levels of FCR may become dysfunctional, the identification of high-risk patients for FCR is warranted. Prospective studies are necessary to investigate the long-term course of FCR and the impact on health-related quality of life (HRQoL) in patients undergoing allogeneic HSCT. The objectives and research questions of this prospective study are as follows: (a) Which cutoff value on the Fear of Progression Questionnaire (FoP-Q-SF) is best suited to identify hematological cancer patients with high FCR? (b) How many hematological patients suffer from high FCR before conditioning (T0), 100 days (T1) after and 12 months after allogeneic HSCT? (c) Does FCR significantly change over time in hematological cancer patients undergoing allogeneic HSCT? (d) Which demographic, cancer and treatment-related factors predict high FCR at baseline and follow-up? (e) How is the course of HRQoL in hematological cancer patients with high and low FCR?
Patients and methods
Our research was part of a prospective multicenter trial investigating cognitive functioning in cancer patients treated with allogeneic HSCT including three assessment points.16 Patients were recruited from six German university medical centers in Hamburg, Hannover, Dresden, Kiel, Essen and Munich and were assessed before conditioning/at admission (pre-HSCT), 100 ± 20 days after allogeneic HSCT (100 days after HSCT) and 12 ± 1 months after HSCT (1 year following HSCT). Data were collected over a 3-year period from June 2005 to July 2008. Study approval was obtained from the local ethics committees or the institutional review boards. All patients provided written informed consent prior to participation. Eligible patients were ⩾18 years of age, diagnosed with a hematologic disease and scheduled for allogeneic HSCT. All patients who agreed to participate completed a set of standardized self-report questionnaires. For both follow-up assessment points, the study questionnaires were sent out by mail. All patients completed the set of questionnaires at home and brought them to the scheduled oncology follow-up appointment at the Department of Stem Cell Transplantation, where also the neuropsychological assessment was performed (data published elsewhere).16
Sociodemographic data including age, gender and marital status were assessed via patient’s self-report questionnaire. Medical information such as cancer diagnosis and clinical characteristics were collected at baseline and follow-up assessments though medical charts.
Fear of cancer recurrence was measured using the short version of the FoP-Q-SF,17 a validated self-report instrument to assess fear of recurrence in patients with both active and chronic disease.17 The FoP-Q-SF consists of 12 items and scores on a 5-point Likert scale ranging from 1 (‘never’) to 5 (‘very often’). Higher values indicate higher levels of FCR. A valid external criterion for the categorization of low, middle and high FCR is absent.
The EORTC Quality of Life Questionnaire (EORTC QLQ-C30)18 was used to assess HRQoL. This questionnaire is composed of five functioning scales (physical, social, role, cognitive and emotional functioning), a scale for global quality of life, three nine-symptom scales and a number of single items assessing additional symptoms. Each scale and single-item measure is linearly transformed to scores from 0 to 100. On the function scales and global quality of life scale, a score of 100 represents maximum functioning.
Anxiety and depression was measured using the Hospital Anxiety and Depression Scale (HADS). The HADS is a widely validated self-assessment instrument used in somatically ill patients, divided into two subscales measuring anxiety (A) and depression (D). Each scale has seven items that are scored on a 4-point Likert scale (range 0–3).19 Higher scores indicate higher levels of anxiety or depression. A score of 0–7 is categorized as normal, a score of 8–10 is considered to indicate a possible anxiety or depressive disorder, and a score of ⩾11 is considered to indicate a probable anxiety or depressive disorder.
Patient-, cancer- and treatment-related factors at baseline and at follow-up assessments were reported. At first, a receiver operating characteristic analysis was performed in order to establish the cutoff score for high FCR measured by the FoP-Q-SF using the HADS anxiety subscale cutoff score >10 for detecting cases of moderate to severe FCR (probable anxiety disorder). We used a descriptive analysis for the frequencies of high FCR before conditioning/at admission (pre-HSCT), 100 days after HSCT and 1 year following HSCT. We further described the course of FCR over time for answering the research question whether FCR changes significantly between the three assessment points. Since we had a substantial percentage of missing values 100 days after HSCT and 1 year following HSCT we used a random intercept model with time as a fixed factor at the three levels pre-HSCT, 100 days after HSCT and 1 year following HSCT. Assuming compound symmetry accounts for possible correlations arising from assessing the FCR score for each patient several times.
We identified key predictors of FCR among HSCT survivors before conditioning (pre-HSCT), 100 days after, and 1 year after allogeneic HSCT. Therefore, a multiple linear regression analysis was calculated with the baseline predictors gender, age, marital status (married vs others), education (> or <9 years), cancer entity (AML vs others), pretreatment (‘yes’ vs ‘no’), time since diagnosis and depression (HADS subscale score). We further analyzed the course of HRQoL between three measuring points for the five functioning scales of the EORTC QLQ-C30, and the scale for global quality of life separated for patients with low and high FCR. Therefore, we use a random intercept model with time as a fixed factor at the three levels pre-HSCT, 100 days after HSCT and 1 year following HSCT and high FCR (‘yes’ or ‘no’) as between-subject factor.
We examined the relationship between FCR and HRQoL over the course of treatment. Bivariate associations between HRQoL and FCR were calculated using Pearson’s product-moment correlation coefficient for all functioning scales.
All tests and confidence intervals were two-sided, and the level of significance was α=0.05. A statistical analysis was performed by using SAS 9.3, and SPSS Statistics, version 19.0 (IBM SPSS, Chicago, IL, USA).
Patient-, cancer- and treatment-related characteristics at baseline are summarized in Table 1. Two hundred and thirty-nine patients were assessed at baseline, 150 patients 100 days after HSCT and 102 patients at 1 year following HSCT. Forty-three percent of the patients were assessed at all measurement times. Among the 239 patients included at baseline, the most common disease was AML (44%). Mean age was 50 years (range 18–71), and the majority of patients were men (62%). Pretreatments most often included chemotherapy (70%).
The subgroup of serially assessed patients with pretreatments had received a mean number (M) of 5.17 chemotherapy cycles (n = 64, range = 1–16) and 1.32 autologous SCTs (n = 19, range = 1–3) prior to HSCT. Ninety-seven patients (95%) were treated with PBSC transplantation and 5 patients (5%) with BM transplantation. The conditioning intensity was reduced in the majority of patients (n=60, 59%); 42 patients (41%) received standard conditioning intensity. Thirty percent of the patients (n=31) underwent a TBI 100 days after HSCT, 57 patients (56%) suffered from acute GVHD and 60 patients from chronic GVHD at T2 (60%). At 1 year following HSCT, n=88 patients had CR and n=3 patients had PR. Ten patients had developed a cancer recurrence and one patient was diagnosed with a new cancer (bladder cancer).
FoP-Q-SF cutoff value
Receiver operating characteristic curve analysis showed that the best suited cutoff point for high FCR was 34, with a sensitivity of 77.4% and a specificity of 69.1% (area under the curve 0.793, 95% confidence interval 0.72–0.90, P<0.001).
Frequency and course of FCR recurrence
The total mean score (M) on the FoP-Q-SF was 30.9 (s.d.=8.4) before conditioning. At 100 days after HSCT, the total mean score was 27.8 (s.d.=8.4) and at 1 year following HSCT 26.9 (s.d.=8.6). At baseline, 87 patients (36%) were classified as having high FCR. At 100 days after HSCT, 36 patients (24%) suffered from high FCR and at 1 year following HSCT 23 patients (23%) were classified as having high FCR. At 100 days after HSCT, the patients completed the questionnaires at an average of 21 days before (range 1–31 days) the patient follow-up visit by a physician. One year after HSCT, the time frame for answering the FCR questionnaire was an average of 15 days before (range 1–19 days) an outpatient follow-up visit. FCR significantly declined over the three assessment times (F2,245)=19.23, P<0.0001).
We found a significant decrease in FCR between pre-HSCT and 100 days after HSCT (t=−4.64, df=245, P<0.0001) and between pre-HSCT and 1 year following HSCT (t=−5.64, df=245, P<0.0001). However, there was no significant decrease in FCR between 100 days after HSCT and 1 year following HSCT (t=−1.55, df=245, P=0.123).
Predictors of FCR
A multiple linear regression analysis was performed to identify those risk factors that predicted FCR (FCR score measured by the FoP-Q-SF) at admission, 100 days after HSCT and 1 year after HSCT. The results of the multiple regression analysis are shown in Table 2. At admission (pre-HSCT), being married significantly predicted FCR compared to being single, divorced or widowed (b=2.76, P=0.026). Female gender (b=4.45, P<0.001) and higher depression (b=4.44, P<0.001) were significantly associated with FCR at baseline.
One hundred days after allogeneic HSCT, again higher depression at baseline predicted FCR (b=6.46, P<0.001). The results of regression model 3 showed that female gender (b=6.61, P=0.008) and higher depression (b=4.88, P=0.004) were significant predictors for FCR 1 year after HSCT. The other factors had no significant influence on FCR.
Course of HRQoL in patients with high and low FCR
Over the three assessment points, patients with high FCR had a significantly lower quality of life compared to patients with low FCR in physical functioning (F1,401=5.46, P=0.019), role functioning (F1,400=9.03, P=0.003), emotional functioning (F1,402=62.51, P<0.001), cognitive functioning (F1,402=8.94, P=0.003), social functioning (F1,400)=13.15, P<0.001) and global quality of life (F1,401=12.21, P<0.001). The random intercept model showed a significant effect of time in physical functioning (F2,401=6.64, P=0.002), role functioning (F2,400=6.08, P=0.003), emotional functioning (F2,401=5.83, P=0.003), social functioning (F2,400=13.0, P<0.001) and global quality of life (F2,401=9.11, P<0.001).
Patients with low and high FCR had a significantly different course in the quality-of-life subscales role functioning (F2,400=4.73, P=0.009), emotional functioning (F2,402=5.74, P=0.004) and global quality of life (F2,401=4.30, P=0.014) over the three assessment points. In role functioning, patients with low FCR declined between baseline (pre-HSCT) and 100 days after HSCT (t=−3.35, df=400, P<0.001) and improved significantly between 100 days after HSCT and 1 year after HSCT (t=2.77, df=400, P=0.006). Patients with low FCR reached approximately their initial level in role functioning 1 year following HSCT.
In contrast, patients with high FCR showed a low initial level (pre-HSCT) in role functioning, and showed a continuous improvement across all three time points. Patients with high FCR improved in role functioning significantly between 100 days SCT and 1 year after HSCT (t=2.24, df=400, P=0.026) and between pre-HSCT and 1 year after HSCT (t=3.17, df=400, P=0.002). In emotional functioning, patients with low FCR showed higher emotional functioning prior to therapy (pre-HSCT), with a constant profile over all three time points. In contrast, patients with high FCR showed a low initial level in emotional functioning and improved significantly between baseline (pre-HSCT) and 100 days after HSCT (t=2.72, df=402, P=0.007), and between pre-HSCT and 1 year after HSCT (t=4.03, df=402, P<0.001). In global quality of life, patients with low FCR showed higher values at baseline (pre-HSCT) compared to patients with high FCR. One year after HSCT patients with low FCR had significantly higher global quality-of-life values compared to 100 days after HSCT (t=2.48, df=401, P=0.014). Patients with high FCR showed a low initial global quality-of-life level, but improved significantly between pre-HSCT and 100 days after HSCT (t=2.26, df=401, P=0.025) and between pre-HSCT and 1 year after HCST (t=4.14, df=401, P<0.001). The results of the random intercept model are shown in Figure 1.
FCR and HRQoL
The analysis of the association between FCR and HRQoL at baseline, 100 days after HSCT and 1 year following HSCT shows a significant bivariate correlation for all functioning scales (P<0.01) and is shown in Table 3.
The FoP-Q-SF is a validated brief questionnaire measuring FCR. Nevertheless, the question regarding an optimal cutoff score by which to define high FCR remained unanswered so far in patients with hematological cancers. For use in clinical practice, we recommend considering a cutoff value of ⩾34 for high FCR on the basis of receiver operating characteristic analyses using the HADS anxiety subscale cutoff values as standard instrument. This cutoff provided the best discriminatory properties for separating low from high FCR with sufficient sensitivity and specificity compared with other cutoff scores.
In our study, between 23% and 36% of patients were classified as having high levels of FCR; similar high baseline levels of FCR were also found in other cancer populations.10,12,20,21 To the best of our knowledge, this is the first study demonstrating a decline in FCR in hematological cancer patients 100 days and 12 months after HSCT compared to pre-HSCT. Previous studies in other cancer populations in contrast have shown stable levels of FCR.12,20,21
The present study contributes to our understanding of the experience of FCR in patients during and after HSCT. The high baseline FCR can be explained by the perceived threat and uncertainty before the invasive anti-cancer therapy including blood SCT. Our study suggests that FCR is likely to decline 100 days and 12 months after HSCT when patients respond successfully to the treatment. Moreover, the cancer diagnosis and the information about necessary treatments are associated with high psychological stress, which again is significantly correlated with FCR.12,22 However, corresponding to previous repeatedly replicated findings, we did not found a significant association between FCR and cancer diagnosis.3,4,22, 23, 24, 25
A further aim of this study was to identify high-risk baseline predictors for FCR before and after allogeneic PBSC transplantation. We examined the cumulative effects of baseline clinical risk factors on FCR. Our results show that married patients had a significantly higher risk of developing FCR as compared to unmarried patients at baseline. Higher depression symptoms predicted significantly FCR. Possibly married patients suffer from higher FCR because they often have children, and this was associated in many studies with FCR.26, 27, 28 In contrast to another very recently published study, we found no association between age and FCR.29
Different hypotheses have been proposed to explain the association of having children with psychological well-being. In particular, some authors showed that concerns for the future welfare of the children, responding to children’s needs and grief related to potential loss of opportunities to engage in the children’s upbringing were reported as major concerns.6,30
The risk for high FCR through subclinical anxiety and depressive symptoms before the beginning of the therapy shows similarity to the concept of subsyndromal symptomatic depression, which has been defined as minimal depressive symptoms beneath the diagnostic threshold for minor, dysthymic or major depressive disorders.31,32 Subsyndromal symptomatic depression is very commonly observed in patients with unipolar major depressive disorder33 and is an integral component of the symptomatic course of illness.32,34 A similar concept exists for subclinical depressive symptoms, which are highly associated with interferon-associated depression during antiviral treatment.35,36
In accordance with previous studies, we found FCR to be significantly associated with HRQoL.10,20,24,37 We observed that patients with high FCR had significantly lower HRQoL compared to patients with low FCR because of significant differences in the subscales emotional functioning, social functioning, global quality of life, physical functioning and role functioning. Our finding suggests that health-care professionals should be aware of FCR as an important factor adversely influencing HRQoL.
Our study has some limitations. There is a high dropout rate after HSCT, including death and post-transplant complications, suggesting that our follow-up sample is biased towards patients with a better health status and treatment response, which might partially explain the decrease in FCR over time. Patients who dropped out of the study were significantly older, less educated and less often treated with TBI. Hence, another sample bias towards younger age, better education and cancer treatments not associated with TBI has to be considered. Nevertheless, systematic differences between dropouts and participants were small in view of the relatively large sample size. The investigated study sample consisted of a very heterogeneous sample of patients in terms of cancer diagnosis, duration of disease, comorbidity and pretreatments, which limits the generalizability of our findings.
In conclusion, our study shows that FCR significantly decreases in patients with hematological malignancies treated with PBSC transplantation over time. Nevertheless, FCR has a significant influence on HRQoL. We were able to demonstrate that pre-existing subclinical depressive symptoms significantly increase the risk for high FCR. Pre-treatment evaluation of subclinical depressive symptoms may help to detect patients at risk who might benefit from interventions tailored to specific problems such as FCR.7,38
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This study was supported by grants from the German José Carreras Leukemia Foundation (grant nos. DJCLS R 04/29pf and DJCLS R 07/37pf).
The authors declare no conflict of interest.
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Sarkar, S., Scherwath, A., Schirmer, L. et al. Fear of recurrence and its impact on quality of life in patients with hematological cancers in the course of allogeneic hematopoietic SCT. Bone Marrow Transplant 49, 1217–1222 (2014). https://doi.org/10.1038/bmt.2014.139
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