Recent research has shown that patients undergoing hematopoietic SCT (HSCT) experience multiple symptoms that can affect the sleep quality adversely. This study investigated the sleep quality of patient in the acute course of HSCT, and measured the impact of sociodemographic, medical, physical and psychological factors. Fifty patients were assessed before admission, 44 participated during inpatient treatment and 32 on day 100 (±20) post-transplantation. Measuring instruments included the Pittsburgh Sleep Quality Index (PSQI) and a sleep diary (sleep quality), the European Organization for Research and Treatment of Cancer Quality of Life Questionnaire—Core 30 (health-related quality of life), the Hospital Anxiety and Depression Scale—German version (anxiety/depression) and the German version of the Cancer and Treatment Distress Scale (treatment-specific distress). The prevalence of sleep disturbances was 32% before admission, 77% during the hospital stay and 28% after discharge. Difficulty in maintaining sleep was the most intense sleep problem during the inpatient phase. This was mainly caused by disturbing noises and need to use the bathroom frequently. Sleep problems were significantly worse during the hospital stay compared with the other measurement points in time (P<0.001). A significant interaction was seen between the time course of sleep disturbances and the type of transplantation (P=0.001). The findings suggest that sleep disturbances after HSCT are particularly associated with physical functioning, fatigue and treatment-specific distress, and factors that contribute to sleep difficulties in the general population seem to be less important.
Intensive high-dose chemotherapy followed by PBSCT or BMT is increasingly used as a potentially curative treatment for different cancers and hematological diseases. Patients undergoing these procedures still experience a series of physical, social and psychological distress (for example, pain, fatigue and anxiety). Thereby, sleep disturbances are probably part of a symptom cluster co-occuring with pain, fatigue and depression.1, 2, 3 Sleep disturbances are a common concern in the general population. The prevalence of sleep difficulties in a representative German-speaking population sample is 32.1%.4 Reported prevalence rates among cancer patients range from 31 to 75%, due to a variety of clinical populations, care settings and measurement methods.5 Nevertheless, the existing literature on sleep quality of BMT/PBSCT-patients is sparse. In the majority of cases sleep quality is only marginally discussed and assessed by a single or a few items, for example in studies that deal with quality of life. Furthermore, most studies include patients in the post-transplant period and not during the acute course of treatment. Nonetheless, it is highly likely that sleep quality decreases during a hospital stay because of physical, psychosocial strains and environmental factors, such as noises coming from monitors, pump alarms or care frequently delivered by the nursing team. In addition, the fact of sharing the room with other persons might also weaken the quality of sleep.
Of the few studies dealing with sleep quality of patients during the acute course of BMT/PBSCT, none focuses exclusively on this topic. In sum, the results of these studies show that disturbed sleep is one of the most prominent concerns among patients; sleep difficulties occur frequently and are worst during the inpatient treatment.6, 7, 8, 9, 10, 11
Anderson et al.6 assessed the symptom burden in 100 patients undergoing autologous SCT during their hospital stay. They identified sleep disturbance as one of the most pronounced symptoms. According to their records, sleep difficulties were worst at nadir, when 39% of the patients described disturbed sleep as moderate or severe. Zittoun et al.11 studied the quality of life during intensive chemotherapy or BMT. They found that sleep difficulties are worst during cytotoxic treatment.
The largest part of the studies show that during the course of the first year post-transplantation and in the further follow-up period sleep disturbances diminish. The studies note that the proportion of patients with good sleep varies about 55–80%, but that observed sleep difficulties are significantly worse compared with a healthy comparison group.12, 13, 14
Andrykowski et al.15 analyzed the sleep quality of patients who received BMT 12–124 months ago. They found that approximately half of the participants had mild sleep difficulties. These were particularly nocturnal and early morning awakening, which were mainly attributed to ‘having to get up to use the bathroom’. In all, 17% of the participants were taking sleep medications and 48% considered their sleep quality to be worse than before their cancer diagnosis. Patients aged >40 years at BMT, females and those having received TBI during pre-BMT conditioning were more likely to report sleep difficulties.
This study investigates the prevalence, nature and causes of sleep difficulties of patients in the acute course of HSCT. In addition, we examine the impact of sociodemographic, medical, physical and psychological factors on sleep quality. On the basis of the literature we hypothesize that: (a) the highest prevalence rate of sleep disturbances occurs during hospital stay, (b) women and older patients report a poorer sleep quality than men and younger patients, (c) patients who received an allogeneic transplant report a poorer sleep quality than those who received an autologous transplant and (d) that a decrease in physical functioning and an increase of fatigue, treatment-specific distress, anxiety and depression are accompanied by a decrease of sleep quality.
Patients and methods
Study design and patients
The study is based on a prospective longitudinal design including patients receiving an allogeneic or autologous BMT/PBSCT at the Bone Marrow Transplantation Unit of the University Medical Center Hamburg-Eppendorf. Eligible patients were at least 18 years of age and spoke German fluently. Before admission they received an information letter explaining the procedures and aims of the study. Written informed consent was obtained according to institutional guidelines. Patients completed assessment measures shortly before admission (T1), daily during their hospital stay (T2), shortly before discharge (T3) and 100 days (range: 80–120 days) after transplant (T4). The exclusion criterion during hospital stay was a relocation to an intensive care unit for more than two nights.
During the study period from July to December 2006, 50 of the 57 eligible patients (87.7%) agreed to participate. During the hospital stay five patients were relocated to an intensive care unit and therefore excluded from the study. In addition, one patient declined. Between discharge and 100 (±20) days post-transplant five patients died. Of the 39 remaining patients five stayed at an intensive care unit or a peripheral hospital and two withdrew. Overall, 32 patients (71.7%) participated during the entire length of the study.
Sociodemographic and medical data were collected from the patients’ records. Study self-report measures comprised domains including sleep quality, health-related quality of life, anxiety/depression and treatment-specific distress. Sleep quality was measured at each time point, whereas the other domains were assessed only before admission and on day 100 post-transplantation. It was decided not to use actigraphy as it tends to overestimate sleep efficiency by misinterpretation of quiet wakefulness as sleep.16
Sleep quality before hospital admission, before discharge and 100 days post-transplantation was assessed using the German version of the Pittsburgh Sleep Quality Index (PSQI).17 This validated 19-item instrument measures subjective sleep quality, sleep latency, sleep duration, sleep efficiency, sleep disturbances, use of sleep medication and daytime dysfunction retrospectively over a 1-month period, resulting in a sum score that corresponds to global subjective sleep quality (range: 0-21; higher scores represent poorer sleep quality). In clinical populations PSQI sum scores greater than eight indicate a poor sleep quality or sleep disturbance.18 The overall internal consistency is Cronbach's α=0.83.17 The German version of the PSQI has been validated in patients with primary insomnia and shows a sensitivity of 98.7%, a specificity of 84.4%, a test–retest reliability of 0.87 and Cronbach's α=0.85.19
To evaluate sleep quality during hospital stay we developed a brief, easily understood sleep diary, which the participants completed every morning. Sleep diaries have been frequently used and are reliable and valid measuring methods in sleep research.20, 21 Owing to the daily assessment and a partly weak condition of the participants, we tried to create an instrument that could be filled out easily and therefore improve the patients’ compliance and the validity of the data. Thereby, typical parameters that had turned out to be important elements of sleep quality in former studies were selected. The diary measures non-restorative sleep, difficulties in falling asleep, difficulties in maintaining sleep, difficulties in falling back to sleep once awake and early morning awakening on a four-point Likert scale. Symptoms were categorized as follows: 0=none, 1=mild, 2=moderate, 3=severe. The sleep diary also asks for the use of sleeping medication (no vs yes). The daily sum score can range between 0 and 18; higher scores reflect more complaints. To analyze changes during the inpatient treatment, mean scores were computed for the following three periods: admission to night before transplantation, night after transplantation to night before engraftment, night after engraftment to discharge. To compare results from the sleep diaries with the PSQI the sleep diary was also completed at T1 and T4.
Assessment of sleep quality during hospital stay was completed by a short, semi-structured interview with self-developed questions dealing with issues such as reasons and temporal courses of sleep difficulties. This could be administered in about 15 min and contained questions like ‘Have there been periods during your hospital stay in which sleep disturbances were worse?’ or ‘What did you or the staff do if sleep disturbances occurred?’.
Health-related quality of life was assessed using the European Organization for Research and Treatment of Cancer Quality of Life Questionnaire—Core 30 (EORTC QLQ-C30), a well-validated instrument.22 It comprises 30 items that are grouped to a global health status scale, five functional scales, three symptom scales and six single items. Scores range from 0 to 100 with higher scores in global health and functional scales reflecting better functioning and higher scores in symptom scales and items representing a greater amount of complaints. For this study the functional scale physical functioning and the symptom scale fatigue were particularly relevant.
Anxiety and depression were assessed using the Hospital Anxiety and Depression Scale—German version (HADS-D).23, 24 It includes 14 items rated on a four point Likert-scale—seven items measure depression and seven anxiety. Sum scores on both subscales can range between 0=no symptoms and 21=severe symptoms. The German version is validated.25
Treatment-specific distress was estimated using the questionnaire Belastungen hämato-onkologischer Erkrankung und Therapie (BHET), that is, the German version of the Cancer and Treatment Distress (CTXD) scale26 (translated with permission from the authors). It assesses specific potential stressors in BMT/PBSCT, such as nausea, alopecia and pain. The version Acute measures treatment-specific distress before treatment. It consists of 32 items which are scaled from 0=no distress to 3=severe distress. These are added to seven subscales (uncertainty, family strain, appearance and sexuality, health burden, managing medical system, finances and acute symptoms before treatment) and one sum score. The version Follow-up is an abbreviated instrument, which excludes the subscale acute symptoms before treatment. It was administered on day 100 post-transplant. Overall internal consistency is Cronbach's α=0.93.26 For statistical analyses the mean sum scores of the two versions were used.
Data analysis were carried out using the Statistical Package for the Social Sciences (SPSS), version 12.0. Descriptive statistics were calculated to present demographic and medical characteristics of the sample as well as prevalence rates of sleep disturbances at each measurement point in time. The Kolmogorov–Smirnov test was used to verify the assumption of normal distribution. For parameters not following the normal distribution, non-parametric tests were conducted. Differences in the prevalence of sleep disturbances between participants and a representative population sample were tested with χ2-tests. McNemar tests were used to measure differences in prevalence of sleep disturbances over time. To evaluate changes in sleep quality during hospital stay (T2), inpatient treatment was categorized into three time intervals as follows: (1) admission to night before transplantation, (2) night after transplantation to night before engraftment, (3) night after engraftment to discharge. Repeated-measures analysis of variance (rmANOVA) with a priori contrasts was calculated for those individuals who participated during the entire length of hospital stay (n=44).
Furthermore, rmANOVA was computed to measure differences in sleep quality over time regarding age (young vs old), gender and type of transplant (autologous vs allogeneic) as the between-subjects factors (n=32). The within-subjects factor time included the time points before admission (T1), shortly before discharge (T3) and 100 days post-transplantation (T4). When significant main or interaction effects occurred, post-hoc t-tests for independent samples were carried out to compare groups at each time point. Spearman's rank correlation coefficients were calculated to examine relationships between changes in physical and psychological variables on the one hand and changes in subjective sleep quality on the other hand (n=32). Therefore, we composited difference scores by subtracting the mean scores of each variable pre-admission from the mean scores 100 days post-transplantation. In addition, Spearman's rank correlation coefficients were computed to compare results of the sleep diaries with the PSQI. A significance level of P⩽0.05 was chosen. To adjust for multiple comparisons Bonferroni corrections were applied.
Table 1 represents demographic and disease-related characteristics of the patients before admission (T1) and 100 days post-transplantation (T4).
At T1 the mean age of the 50 patients was 53.3 years (range: 21–70 years); 74% were male. Educational levels were equally distributed; most of the patients lived together with a spouse. More than one-third was diagnosed with acute myeloid leukemia, 22% with multiple myeloma and 14% with non-Hodgkin's lymphoma. Nearly all participants received PBSCs. The largest part of the sample achieved an allogeneic transplantation—one-third from related donors. Most of the participants were treated with BMT/PBSCT for the first time, whereas 22% had already received a BMT/PBSCT in the past.
Prevalence of sleep disturbances
The prevalence of sleep difficulties was 32% before admission (n=50), 77.3% during hospital stay (n=44) and 28.1% 100 days post-transplantation (n=32). During hospital stay sleep quality was significantly worse compared with a representative German-speaking population sample, with a prevalence of sleep difficulties of 32.1% (χ2(1, n=44)=41.194, P<0.001).4 Sleep problems are also reflected by the outcome in sleep latency, sleep duration, sleep efficiency and use of sleep medications reported by the patients at the different time points. Results are summarized in Table 2.
For those patients who participated during the entire length of the study (n=32), sleep quality in the course of hospital stay was significantly worse than before admission (χ2(1, n=32)=0.199, P<0.001) and 100 days post-transplantation (χ2(1, n=32)=1.951, P<0.001).
Sleep quality during hospital stay
Findings regarding sleep quality during hospital stay were from the sleep diaries, which were completed every day by those patients who participated during the entire length of inpatient treatment (n=44). They show that sleep difficulties are most prominent during the phase between transplantation and engraftment. Repeated-measures ANOVA shows sleep quality to be significantly worse than in the phase between admission and transplantation (F(1)=4.585, P=0.038). During the entire hospital stay the predominant sleep problem was difficulty in maintaining sleep: 81.8% of the participants characterized this complaint to be moderate or severe, whereas 18.2% reported this problem to be not present or only of mild nature. In comparison, 61.4% of the patients described non-restorative sleep, 52.3% difficulties in falling asleep, 47.7% difficulties in falling back to sleep once awake and 20.5% early morning awakening to be moderate or severe. Findings of the interview show a number of reasons for sleep difficulties during hospital stay: 77.3% of the participants attributed disturbed sleep to noises of monitors and pumps, 75% to the need to use the bathroom and 68.2% to agitation/stress. Furthermore, 54.5% of the patients ascribed sleep difficulties to frequently delivered care by the nursing staff during the night.
Spearman's rank correlations show that results of the sleep diaries that were additionally completed at T1 and T4 are significantly associated with the results of the PSQI (T1: r=0.756, P<0.001; T4: r=0.772, P<0.001).
Sleep quality and sociodemographic variables
The sample was divided into the groups young and old by median-split (Md=56.5 years). Repeated-measures ANOVA with the within-subjects factor time and the between-subjects factors age and gender were used to evaluate changes of sleep quality depending on age and gender. Except for the significant main effect for the repeated-measures factor time (F(2)=28.071, P<0.001), results showed no significant main effects or interactions. Therefore, there were no differences in sleep quality and its temporal course between men and women, or younger and older patients.
Sleep quality and type of transplant (autologous vs allogeneic)
Once again, rmANOVA showed the significant main effect of the within-subjects factor time (F(2)=18.940, P<0.001). In addition, there was a significant interaction between time and type of transplant, which indicates different temporal courses of sleep quality between autologous and allogeneic transplanted patients (F(2)=10.093, P<0.001). These are illustrated in Figure 1.
The main effect of the between-subjects factor type of transplant was not significant. However, Figure 1 shows that the sleep quality of patients who received an autologous transplant was worse before admission and better during hospital stay compared with patients who received an allogeneic transplantation. Post-hoc t-tests for independent samples evidenced these differences to be significant (T1: t(30)=2.413, P=0.022; T3: t(30)=−2.480, P=0.019), even when Bonferroni correction (α′=0.025) was applied.
Sleep quality and self-rated physical and psychological variables
Spearman's rank correlation coefficients were used to examine relationships between changes in self-rated physical/psychological distress on the one hand and changes in subjective sleep quality on the other. These changes refer to the results measured at the time points pre-admission (T1) and 100 days post-transplantation (T4) (n=32).
We chose the subscales fatigue and physical functioning of the EORTC QLQ-C30 as physical variables. As psychological variables the subscales anxiety and depression of the HADS-D and the mean sum score of the BHET (treatment-specific distress) were selected. The subjective sleep quality was represented by the PSQI sum score. The variables used for correlational analysis are shown in Table 3.
Results indicated that an increase in fatigue and a decrease in physical functioning significantly correlate with an increase in sleep disturbances (fatigue: r=0.450, P=0.005; physical functioning: r=−0.469, P=0.003). Regarding the psychological variables we observed a significant correlation between an increase in treatment-specific distress and an increase in sleep disturbances (r=0.507, P=0.002). Findings did not show a significant relationship between changes in anxiety/depression and changes in sleep quality. All correlations remained statistically significant after Bonferroni correction (α′=0.01).
This study focused on the subjective sleep quality of patients in the acute course of hematopoietic SCT. Patients were assessed before admission, during their hospital stay and 100 days post-transplantation. In all, 87.7% of the patients approached agreed to participate (n=50) and 32 patients completed all assessments. High response rates may refer to the importance of the topic sleep disturbances. In sum, findings show a substantial percentage of patients suffering from sleep difficulties, especially during their hospital stay. Disturbed sleep is associated with a variety of physical, emotional and environmental stressors.
Corresponding to our first hypothesis, the highest prevalence rate of sleep disturbances occurred during hospital stay. Our result is consistent with findings from other studies that measure sleep disturbances at least one time during inpatient treatment.6, 7, 8, 9 In line with our outcome, Hacker and Ferrans8 showed that sleep difficulties are significantly worse during hospital stay compared with time points before admission and two weeks after discharge. At six weeks after discharge sleep problems were a little less pronounced than before admission.
Only during inpatient treatment was the prevalence of disturbed sleep significantly higher compared with a representative German-speaking population sample. Regarding this result, one has to consider that the comparative study shows a relatively high prevalence of sleep disturbances (32.1%)—other studies show lower prevalences of sleep difficulties among the population 18.8 or 25%.27, 28 Nonetheless, we used this norm population because of use of the same questionnaire. Furthermore, it has to be kept in mind that the authors of the comparative study used a cut-off score greater than five to indicate sleep disturbances—we applied a score of >8, which is recommended for clinical populations. If we had used the first cut-off score, the prevalence of disturbed sleep would have been 44% (T1), 88.6% (T3) and 43.8% (T4). Therefore, results at all time points would have been significantly higher than among the population sample. The prevalence rates among cancer patients range from 31 to 75%.5 Compared with this the prevalence of sleep disturbances during hospital stay among our participants reached the upper range, whereas the prevalence rates before admission and 100 days post transplantation were in the lower range.
Findings of the interview show that the main causes of sleep difficulties during inpatient treatment belong to physical, psychological and environmental factors. This is consistent with a multifactorial etiology of sleep disturbances. Patients ascribed disturbed sleep most frequently to noises of monitors/pumps, the need to use the bathroom and agitation/stress. For a couple of patients the need to use the bathroom can be attributed to diuretic therapy. In addition, about half of the patients attributed sleep disturbances to care delivered by the nursing staff. During the phase of aplasia vital signs were monitored every 4 h. Even healthy individuals could develop sleep difficulties if they were woken up so frequently. These disturbing factors are also shown to be important in other studies. There is only one study that examines the causes of disturbed sleep during the hospital stay for HSCT. According to this study sleep difficulties are most frequently attributed to environmental factors (noises, care delivered by the nursing staff, illumination), anxiety, depression and nervousness.29 Our findings are also consistent with the results from Andrykowski et al.,15 who examined the sleep quality of BMT-survivors 12–124 months post-transplantation. They show sleep disturbances to be most often caused by the need to use the bathroom.
During the entire length of hospital stay the most prominent sleep problems were difficulties in maintaining sleep. As mentioned above, sleep disturbances were especially ascribed to noises, care delivered by the nursing team and the need to use the bathroom. These are typical causes that can lead to nocturnal awakening. It has to be considered that nocturnal awakenings represent a severe problem for patients who cannot fall asleep without delay afterwards; for those who fall asleep immediately multiple awakenings are less disturbing. There is no published study that deals with the sleep quality of BMT/PBSCT patients during hospital stay and distinguishes between different types of sleep difficulties. Studies in the long-term follow-up or studies among other populations show the importance of difficulties in maintaining sleep. Andrykowski et al.15 describe multiple awakenings as the most frequently complained sleep difficulty. However, the authors ask for difficulties in maintaining sleep only in correspondence with early awakening. Most of the studies that examine different types of sleep problems among cancer patients demonstrate difficulties in maintaining sleep as the most prominent concern.30, 31 For the general population the same fact has been shown by Ohayon and Roth.32
Our results show that disturbed sleep is most pronounced during the phase between transplantation and engraftment. This is the phase of aplasia — a time that is known for its strong physical and emotional distress. Our findings correspond to the results from Anderson et al.6 At nadir, 39% of the patients describe sleep disturbances as moderate or severe. This is the maximum during the acute course of treatment. In contrast, Zittoun et al.11 showed the highest frequency of severe sleep difficulty during conditioning therapy.
Neither age nor gender had a significant impact on the sleep quality. This was not consistent with our hypothesis that older and female patients would complain about more severe sleep difficulties than younger and male ones. These assumptions arose from the fact that the largest part of studies on sleep quality among the general population describes sleep difficulties to be more pronounced among women and to increase with age.27, 33 Disturbed sleep among older patients is mainly attributed to increased physical complaints and depression—these differences were not present in our study. At T1 the physical functioning of older participants was even better. Studies that deal with sleep quality of BMT/PBSCT patients and distinguish between young and old patients describe different results: some show a better sleep quality in younger patients,13, 15 whereas others show no significant differences of sleep quality regarding age.6, 34, 35, 36 Sleep disturbances of women within the general population are mainly ascribed to a higher frequency of anxiety/depression and to hormonal changes during menstrual cycle, pregnancy and post-menopause.37, 38 In our study, female patients did not differ significantly from males regarding anxiety and/or depression. The literature is inconsistent regarding this issue: some studies show a better sleep quality of men,15, 39 whereas others describe no differences regarding concerning gender.6, 36, 40
Our results indicate different temporal courses of sleep quality regarding the type of transplant. Sleep difficulties of participants receiving an allogeneic transplant were less pronounced before admission and worse during the inpatient treatment compared with patients who received an autologous transplant. The findings from two studies of Hjermstad et al.35, 41 who measured sleep quality before admission are comparable.
According to our assumption, correlational analysis showed that a worsening of self-rated physical functioning and an increase of fatigue and treatment-specific distress between pre-admission and 100 days post transplantation was associated with an increase in sleep disturbances. This corresponds to other studies.15, 30, 42, 43 However, the directions of these relationships are not known; it seems to be likely that sleep quality and the selected physical/psychological variables reciprocally influence each other and are co-occurring, respectively. Our study showed no significant associations between changes in anxiety and depression and changes in sleep quality, which are present in the general population.44, 45, 46 This result is in line with findings from two other studies.6, 36
In summary, it can be stated that sleep disturbances of BMT/PBSCT-patients might particularly be associated with subjective physical functioning, fatigue and treatment-specific distress. Factors that are shown to enhance sleep difficulties in the general population (for example, age, gender, depression) are supposed to be less important.
However, results have to be considered with some caution. First of all, it has to be kept in mind that the meaning of good sleep is different between individuals, as an objective size of optimal sleep duration does not exist. The study was limited by its small sample size, resulting in lack of power. There is an essential need for replication with a larger sample. Moreover, patients with different treatment histories were included and premorbid levels of sleep quality before diagnosis are not known. However, no participant has been diagnosed with sleep disturbances. Furthermore, we documented the usage of sleep medications only, not their types or dose. Differences in type or dose of sleep medication or other medications with hypnotic side effects may have directly influenced sleep quality. Five patients in the 100 days post-transplant group could not be included because of health-related reasons. It is possible that these patients had also more sleep difficulties and therefore the prevalence rate of sleep disturbances might be underestimated. In addition, the comparability of results is limited because of differences in design and methods as most studies only used a single or a few items to assess sleep disturbances.
Our findings show the importance of sleep disturbances among patients in the acute course of BMT/PBSCT and have fundamental implications for health professionals. Results confirm our concern that a substantial percentage of patients suffer from sleep difficulties, mainly during the course of inpatient treatment, and indicate the need for action. The type and amount of adequate professional support should be investigated in further studies. The direction of the relationship between physical/psychological variables and sleep quality as well as the correlation between subjective and objective sleep quality should also be a main topic of future research. We recommend an adequate documentation of sleep medication use within this research. Patients could benefit from additional treatments, not only regarding their sleep difficulties, but also with regard to the overall quality of life. In addition to well-established treatments like pharmacotherapy and behavior therapy, technical and organizational approaches to reduce environmental causes of disturbed sleep also have to be considered.
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Rischer, J., Scherwath, A., Zander, A. et al. Sleep disturbances and emotional distress in the acute course of hematopoietic stem cell transplantation. Bone Marrow Transplant 44, 121–128 (2009). https://doi.org/10.1038/bmt.2008.430
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