Exercise and psychosocial interventions to improve quality of life in patients with
cancer
Kalter, J.
2018
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citation for published version (APA)
Kalter, J. (2018). Exercise and psychosocial interventions to improve quality of life in patients with cancer:
Secondary and individual patient data analyses evaluating intervention moderators and mediators.
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Current exercise and psychosocial interventi ons are typically off ered to a heterogeneous group of pati ents with cancer and are not targeted to specifi c pati ents. Such a ‘one-size-fi ts all’ approach may explain the modest eff ects of these interventi ons that have been reported. Therefore, these interventi ons should be bett er targeted and tailored to specifi c characteristi cs of pati ents. To be able to shift from this ‘one-size-fi ts-all’ approach to more personalized exercise and psychosocial interventi ons, it is important to identi fy which subgroups of pati ents respond best to these interventi ons. Furthermore, to improve the eff ecti veness of exercise and psychosocial interventi ons on quality of life (QoL) among pati ents with cancer, insights into the working mechanisms of an interventi on are needed. Therefore, this thesis aimed to investi gate the eff ects of exercise and psychosocial interventi ons on QoL in pati ents with cancer during and aft er cancer treatment, and to identi fy demographic, clinical, personal and interventi on-related moderators of these interventi on eff ects. Further, this thesis investi gated some possible mechanisms underlying the eff ects of exercise interventi ons on QoL. Finally, this thesis aimed to build a fl exible data harmonizati on platf orm that facilitates harmonizing raw individual pati ent data (IPD) of original studies for meta-analyses purposes, where such harmonizati on already starts during collecti on of the data from the original studies. The Predicti ng Opti maL Cancer RehabIlitati on and Supporti ve care (POLARIS) study used this platf orm. POLARIS included IPD from 57 randomized controlled trials (RCTs) that evaluated the eff ects of exercise interventi ons and/or psychosocial interventi ons on QoL compared to a wait-list, usual care or att enti on control group in adult pati ents with cancer. Aft er briefl y summarizing and discussing the main fi ndings of this thesis, the methodological considerati ons are discussed. This is followed by implicati ons for clinical practi ce, recommendati ons for future research, and a general conclusion.
Main fi ndings
Eff ects and moderators of exercise and psychosocial interventi ons on QoL in pa-ti ents with cancer
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The single study described in Chapter 2 suggests that the eff ects of a group-based exercise interventi on on global QoL in pati ents aft er cancer treatment were larger for pati ents who received radiotherapy, and in parti cular, in those who received a combinati on of chemotherapy and radiotherapy, and in pati ents with higher levels of fati gue at baseline (i.e. prior to the exercise interventi on). No moderator eff ects were found for age, sex, educati on level, marital status, employment status, ti me since treatment, presence of comorbidity, self-effi cacy, depression, and anxiety. This study was a fi rst step in identi fying pati ents who may benefi t most from exercise interventi ons to improve QoL [1]. However, single studies are generally not powered to analyze moderators of interventi on eff ects and to conduct subsequent strati fi ed analysis [1]. Therefore, the POLARIS study was launched allowing to set up and conduct meta-analyses of IPD.
Results of the POLARIS IPD meta-analysis of 34 RCTs (n=4,519 pati ents) evaluati ng the eff ects and demographic, clinical, interventi on- and exercise-related moderators of exercise on QoL and physical functi on in pati ents with cancer, demonstrated that exercise interventi ons signifi cantly improved QoL and physical functi on, with small overall eff ects (Chapter 6). These fi ndings are consistent with those reported in previous meta-analyses based on aggregate data [2-4]. Furthermore, the results presented in this thesis showed that the eff ects of exercise interventi ons in which (part of) the weekly exercise sessions were supervised, were twice as large as those of exercise interventi ons in which sessions were unsupervised and conducted at or from home. No signifi cant moderator eff ects were found for age, sex, educati on level, marital status, body mass index, cancer type, the presence of distant metastasis, and type of cancer treatment. Besides, exercise interventi ons during and aft er cancer treatment were found to be equally benefi cial for QoL and physical functi on. Results of earlier RCTs that evaluated whether or not demographic and clinical characteristi cs moderated the exercise interventi on eff ects on QoL and physical functi on were inconsistent [5-9]. Findings from this thesis suggests that targeti ng exercise interventi ons based on these demographic and clinical characteristi cs may not be useful for further improving QoL and physical functi on.
8
cancer types. However, it may be that the moderati ng eff ect of cancer type on the psychotherapy eff ects on QoL was coincidental due to the small sample size of some other cancer types included in the analyses. Therefore, future studies are needed to confi rm whether pati ents with diff erent cancer types indeed respond diff erently to psychosocial interventi ons. Overall, this IPD meta-analysis stresses the need for developing a coping skills training tailored to the specifi c needs of elderly pati ents, and it highlights the importance of targeti ng psychosocial interventi ons to pati ents with distress.
Mechanisms underlying exercise interventi on eff ects on QoL
The second aim of this thesis was to investi gate the mechanisms underlying the eff ects of exercise interventi ons on QoL.
Research into the mechanisms underlying psychosocial interventi on eff ects on QoL were beyond the scope of the current thesis. However, data collected in the POLARIS study will allow to explore which factors may mediate the eff ect of psychosocial interventi ons on QoL.
A fl exible data harmonizati on pla� orm that facilitates harmonizing data during data collecti on
The third aim of this thesis was to build a fl exible data harmonizati on platf orm for use in IPD meta-analyses that facilitates harmonizati on of IPD already during the process of data collecti on. Chapter 5 describes the development and use of this platf orm. This platf orm is the fi rst data harmonizati on platf orm that allows starti ng data harmonizati on already during data collecti on, which is ti me effi cient, especially when the number of studies is large. Furthermore, the data harmonizati on platf orm allows to store, prepare, and harmonize IPD within one transparent platf orm. The harmonizati on process is facilitated by transparent interfaces, which makes the platf orm easy in use. Finally, the data harmonizati on platf orm has the ability to export harmonized IPD and corresponding data dicti onary to the stati sti cal program SPSS [30] for further analysis.
Methodological considerations
When interpreti ng the main fi ndings of this thesis, it is important to take into ac-count methodological considerati ons related to stati sti cal power, study design, pri-mary outcome, potenti al sources of bias in IPD meta-analyses, and generalizability. These considerati ons are discussed below.
Stati sti cal power
8
cancer (n= 209), the sample size was small for studying interventi on moderators. In fact, the results of the presented power analyses showed that the sample size should be at least 395 to be able to adequately conduct strati fi ed analyses with a power of 80%. Consequently, the analyses of the moderator eff ects described in this study should be interpreted as exploratory (hypothesis generati ng) analyses [1]. To confi rm fi ndings from single studies or to identi fy new interventi on moderators, a meta-analysis using IPD has been suggested as the preferred method [31, 32]. The large number of raw data points in an IPD meta-analysis facilitates testi ng of interacti ons at the pati ent level, conducti ng subsequent strati fi ed analyses, and standardizing analyti c techniques across the included studies [31, 32]. With over 4,500 pati ents included in the IPD meta-analyses that studied the moderators of exercise on QoL and physical functi on (Chapter 6) and over 4,200 pati ents included in the IPD meta-analyses that studied moderators of psychosocial interventi on on QoL, emoti onal functi on and social functi on (Chapter 7), there was suffi cient power to test potenti al moderators of interventi on eff ects, and conduct subsequent strati fi ed analyses accordingly. To the best of our knowledge, the POLARIS study is currently the largest IPD meta-analysis study in this fi eld of research. However, the search was conducted in September 2012, and, despite maintaining contact with principal investi gators of identi fi ed ongoing trials, not all relevant studies published since September 2012 were included in the POLARIS database as used in the present thesis.
Study design
the mediator can precede the changes in the outcome QoL [5].
On the contrary, RCTs with pre-and post-interventi on measurements are suitable for studying possible moderators of interventi on eff ects. The use of meta-analyses in which IPD of multi ple RCTs are pooled (as used for the studies presented in Chapter 6 and 7) is the best way to study whether the eff ects of an interventi on diff er across subgroups of pati ents, as the large sample sizes provide suffi cient stati sti cal power to detect moderators of interventi on eff ects and conduct subsequent strati fi ed analyses [31, 32].
Primary outcome
The primary outcome of the studies in this thesis was QoL, which is typically assessed with pati ent-reported outcomes (e.g. cancer-specifi c QoL questi onnaires such as the Functi onal Assessment of Cancer Therapy [35] and the European Organizati on for Research and Treatment of Cancer Quality of Life Questi onnaire-Core 30 questi onnaire [36], and the generic QoL questi onnaire Short Form-36 [37]). Although these questi onnaires are well-known, widely used, reliable and valid instruments to measure QoL [35-37], they have limitati ons. QoL may, for instance, be suscepti ble to ‘response shift ’, i.e. a recalibrati on of a parti cipant’s internal standard used to judge one’s current QoL experience [38, 39]. This internal standard of QoL percepti on may change throughout the cancer conti nuum [40]. Therefore, ‘response shift ’ should be taken into account when evaluati ng the exercise and psychosocial interventi on eff ect on QoL in a longitudinal study design.
Potenti al sources of bias in IPD meta-analyses
Despite advantages of IPD meta-analyses, such as the ability to use consistent stati sti cal methods across studies, obtain results for unpublished or poorly reported outcomes, and increase power to detect diff erenti al subgroup eff ects, there may be biases. These biases include publicati on bias and data availability bias (i.e. if the collected studies are a biased subset of all eligible studies [41]), which may hamper the validity of IPD meta-analyses.
8
signifi cant or clinically favorable results) are more likely to be published than other studies [42, 43]. This can generally lead to an overesti mati on of interventi on eff ects [44]. In the POLARIS study that evaluated the eff ects of exercise interventi ons on QoL (Chapter 6) evidence was found for a signifi cant publicati on bias for all eligible RCTs reporti ng on QoL, which overesti mated the interventi on eff ects by 28%. However, the RCTs included in the IPD meta-analysis were a representati ve sample of all published studies. No evidence for publicati on bias was found in the IPD meta-analysis that investi gated the eff ects of psychosocial interventi ons on QoL (Chapter 7).
Data availability bias may occur when investi gators of eligible studies are not willing or able to share the data of their study for an IPD meta-analysis. This situati on leads to a set of available studies that may not refl ect the enti re evidence base [45]. For POLARIS, 49% of the eligible RCTs on exercise and 36% of the eligible RCTs on psychosocial interventi ons were included in the IPD meta-analyses, which may limit the generalizability of the results [46]. However, no signifi cant diff erences in eff ect sizes were found between studies that were included in the IPD meta-analysis and those not included. This indicates that the studies included for both the analyses on exercise interventi ons as well as psychosocial interventi ons were a representati ve sample of the published studies, at least in terms of eff ects found in these studies.
Generalizability
demographic (age, sex) and clinical characteristi cs (cancer type) [48]. Besides, most RCTs that examined psychosocial interventi on eff ects included parti cipants that were more likely highly educated, wealthier, and Caucasian pati ents with cancer [52]. Furthermore, the majority of studies evaluati ng the eff ects of exercise and psychosocial interventi ons have been conducted in pati ents with breast cancer or prostate cancer who were treated with curati ve intent [53, 54]. Due to diff erences in disease and treatment trajectories, results may not be generalizable to other (less common) cancer pati ent populati ons, such as pati ents with glioma, esophageal, head and neck and ovarian cancer, and pati ents with metastati c disease.
Clinical implications
The results of the POLARIS study showed that exercise interventi ons, and parti cularly those that are (partly) supervised, have signifi cant benefi cial eff ects on QoL and physical functi on in various subgroups of pati ents with cancer with diff erent demographic and clinical characteristi cs, both during and aft er treatment. These fi ndings support and strengthen the evidence base for current nati onal and internati onal exercise recommendati ons that all pati ents with cancer should be physically acti ve during and aft er cancer treatment [54-61]. The results of the POLARIS study also suggest that psychosocial interventi ons are eff ecti ve for improving QoL, emoti onal functi on, and social functi on in pati ents with cancer, both during and post treatment.
Although the fi ndings presented in this thesis identi fi ed only a few moderators of interventi on eff ects that would enable bett er targeti ng of interventi ons, it is and remains important to target exercise and psychosocial interventi ons to pati ents with cancer most in need for support. Some pati ents may be much bett er able to self-manage the consequences of cancer and its treatment (e.g. physical problems such as lower physical fi tness, and psychological problems such as increased fati gue, anxiety, distress), while other pati ents may have a stronger need for referral to a monodisciplinary healthcare provider (e.g. physiotherapist, psychologist) or to multi disciplinary cancer rehabilitati on [58, 62].
8
possible, pati ents are recommended to exercise at least 150 minutes per week and include strength training exercises at least two days per week [54]. For pati ents who require supervision or who may need guidance on safe procedures, referral to a physiotherapist or exercise specialist may help [54]. The Dutch evidence-based guideline ‘Medical specialist oncological rehabilitati on’, published in 2017 [58] recommends that pati ents with multi ple related functi onal problems or with serious functi onal disorders with permanent disability should be referred to multi disciplinary cancer rehabilitati on. In the case of a single problem, pati ent should be referred to a monodisciplinary healthcare provider. For example, pati ents with reduced physical functi on or psychological distress may go to a physiotherapist or a psychologist, respecti vely. As recommended by the guideline [58] these interventi ons should opti mally fi t the pati ent’s characteristi cs, health state, needs, preferences, capabiliti es and opportuniti es. It is therefore important to know which existi ng programs works best, and for whom (that is, to identi fy important moderators of interventi on eff ects). This thesis aimed to provide evidence on which moderati ng factors are of importance. Evidence from the studies conducted so far of which data were included in the POLARIS study (i.e. for pati ents with breast or prostate cancer who were treated with curati ve intent), indicates that targeti ng exercise interventi ons based on the studied demographic and clinical characteristi cs may not be useful for further improving QoL and physical functi on (Chapter 6). Therefore, exercise interventi ons can be off ered in routi ne clinical cancer care for various subgroups of pati ents with cancer with diff erent demographic and clinical characteristi cs, both during and aft er treatment. However, more research is needed to obtain insight into (possibly other) factors to improve individual pati ent care.
characteristi cs, health state, needs, preferences, capabiliti es and opportuniti es. Based on the evidence from this thesis, targeti ng pati ents by screening for distress (e.g. depression, fati gue, cogniti ve problems, menopausal symptoms) is indeed important and likely results in higher eff ect sizes of psychosocial interventi ons (Chapter 7). In additi on, coping skills training interventi ons may help to improve QoL for younger pati ents and for pati ents treated with chemotherapy. However, this thesis also showed that current coping skills training interventi ons may not address the needs of older pati ents. The supporti ve care needs of elderly pati ents should be identi fi ed and eff ecti ve coping skills training interventi ons targeti ng this populati on should be developed.
Recommendations for future research
To further improve the eff ecti veness of exercise and psychosocial interventi ons for pati ents with cancer, interventi ons should be targeted to specifi c cancer populati ons with the highest needs, or tailored to specifi c characteristi cs of pati ent groups. This requires more knowledge of (I) the eff ects of exercise and psychosocial interventi ons in less common cancer populati ons, (II) opti mal prescripti ons for exercise and psychosocial interventi on, (III) mediators of exercise and psychosocial interventi on eff ects, (IV) strategies to opti mize adopti on, implementati on and maintenance of exercise and psychosocial care at the pati ent as well as care giver levels, and (V) strategies to opti mize data sharing and secondary analysis of harmonized single studies as a means to understand and predict interventi on eff ects, inform policy makers, and maximize the benefi ts of exercise and psychosocial interventi ons for the individual pati ents with cancer [67-70].
Eff ects of exercise and psychosocial interventi ons in less common cancer populati ons
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Opti mal prescripti ons for exercise and psychosocial interventi ons
In order to opti mize exercise prescripti ons to improve QoL and physical functi on, more insight into the opti mal exercise-related characteristi cs (i.e. frequency, intensity, type and ti me or durati on of exercise) for pati ents with cancer is required. No diff erences in eff ects between types of exercise were found in this thesis, which is consistent with a previous meta-analysis on aggregate data that contains 32 more studies than our IPD meta-analyses [80]. Larger eff ects of supervised compared to unsupervised exercise interventi ons were found in this thesis and may be explained by a more demanding exercise prescripti on, a higher compliance to the prescribed exercise interventi on, access to bett er equipment with more adjustment and performance feedback, the att enti on and support of the exercise physiologist delivering the interventi on, and possibly social interacti on with other parti cipants [81]. The lack of signifi cant diff erences in exercise eff ects across exercise-related characteristi cs in the current thesis might have resulted from litt le variati on in these characteristi cs across studies that assessed supervised exercise interventi ons, as most of these studies investi gated the eff ect of at least moderate-vigorous-intensity aerobic exercise with or without resistance exercise. However, there is some evidence that the eff ects of exercise vary by exercise frequency, intensity, type and durati on [9, 82, 83]. Previous head-to-head comparisons of exercise-related characteristi cs indicated a dose response eff ect of aerobic exercise on physical functi on but not on QoL during treatment in pati ents with breast cancer [83],
larger eff ects of resistance exercise than aerobic exercise compared with usual care on QoL in pati ents with prostate cancer [82], and larger eff ects of high intensity compared to low-moderate intensity exercise post treatment in a populati on with mixed cancer types [9]. Therefore, more adequately powered, high quality RCTs that directly compare exercise-related characteristi cs are warranted to defi ne opti mal exercise prescripti ons on a given outcome, for a given cancer type, and in a parti cular phase of the cancer trajectory (e.g. during treatment, aft er treatment, end of life [84]).
8
cancer is required [85]. A previous RCT in pati ents with advanced cancer and their caregivers that investi gated the opti mal dose of a psychosocial interventi on, found no diff erences in eff ects on QoL, emoti onal functi on and social functi on between a brief psychosocial program (that consisted of three contacts) and an extensive psychosocial program (that consisted of six contacts) [86]. However, the RCT also suggest that the opti mal interventi on dose may depend on which outcome is targeted for change. In additi on, a previous RCT that examined the effi cacy of Internet-based cogniti ve behavioral therapy for severe fati gue in pati ents with breast cancer [87], found that the eff ecti veness on severe fati gue was not signifi cantly diff erent from face-to-face cogniti ve behavioral therapy [88, 89]. More head-to-head comparisons of psychosocial interventi on-related characteristi cs and techniques are needed to personalize psychosocial interventi ons on a given outcome.
Mediators of exercise and psychosocial interventi on eff ects
domains of QoL.
In additi on to psychosocial mediators, biological factors may mediate the eff ect of exercise on fati gue and QoL [97]. The associati on between elevated concentrati ons of C-reacti ve protein [98] and pro-infl ammatory cytokines [99, 100] and cancer-related fati gue has been suggested in earlier studies. Exercise may lower these concentrati ons [101-104], and thereby reducing fati gue, and improve QoL. Future studies among pati ents with cancer should further explore anti -infl ammatory eff ects of exercise and their mediati ng role on reducing fati gue and improve QoL, and focus how exercise can improve clinical outcomes such as tumour growth and (disease-free) survival as this would likely help adopti ng exercise as standard clinical practi ce [105].
Opti mizing adopti on, implementati on and suffi cient maintenance of exercise and psychosocial care
8
may improve when exercise interventi ons are focused on intrinsic moti vati on, social support, self-effi cacy, perceived benefi ts (in the long term), and perceived barriers [49, 50, 115, 116]. In order to improve the opportuniti es for parti cipati on in exercise and psychosocial interventi ons, interventi ons should be off ered in a convenient manner to pati ents with cancer and supported by well-informed and trained health professionals.
Furthermore, for opti mal implementati on of exercise and psychosocial interventi ons in cancer care it is important to get insight in the cost-eff ecti veness of these interventi ons. Given the shortage of healthcare resources and the increasingly ti ght funding of healthcare systems, it is vital that exercise and psychosocial interventi ons be evaluated not only in terms of effi cacy in symptom reducti on and improving QoL (which evidence has been shown in the current thesis), but in economic terms as well [117]. Earlier studies suggest that off ering exercise and psychosocial interventi on to pati ents with cancer can be cost-eff ecti ve [9, 116, 118-121]. However, as studies diff ered regarding types of exercise and psychosocial care and pati ent populati ons, future studies should provide more clear informati on as to which types of exercise and psychosocial inventi ons are most likely to be cost-eff ecti ve and for whom.
Opti mal data sharing
8
interventi ons on QoL in pati ents with cancer, and to identi fy moderators of interventi on eff ects. However, the reusability of datasets was limited to the 42% of all identi fi ed datasets to which access was granted. Therefore, diff erent approaches should be investi gated in the future how to encourage principal investi gators to share their dataset for IPD meta-analysis. Principal investi gators should publish an open and freely accessible study protocol for easily retrieving metadata from their study such as types of variables, age groups under study, study design, measurement instruments used, and ti me frame. Besides, principal investi gators should be clear which IPD will be made (openly) available for interested researchers, legal and ethical issues should be resolved, and IPD should be clearly stored aft er fi nalizing their study. The POLARIS study applies to these FAIR data principles, as publicati ons from the POLARIS study can be fi nd through search approaches (‘Findability’). It is possible to retrieve the metadata from these datasets on the types of variables, age groups under study, study design, measurement instruments used, and ti me frame (‘Accessibility’). The IPD available in the POLARIS study use a consistent data format and classifi cati on for knowledge representati on (‘Interoperable’), and IPD are made available to other researchers (‘Reusability’). Complying to the FAIR principles will help the reusability of relevant IPD. This will help future research to understand and predict interventi on eff ects, inform policy makers, and maximize the benefi ts of exercise and psychosocial interventi ons for the individual pati ents with cancer.
Conclusion
psychotherapy compared to coping skills training and informati on provision. The eff ects of coping skills training were moderated by age, treatment type, and targeted interventi ons. Eff ects of psychotherapy on emoti onal functi on may be moderated by cancer type, but these analyses were based on two RCTs with small sample sizes of some cancer types. Fourth, benefi cial eff ects of exercise on global QoL and physical functi on in pati ents with cancer were mediated by increased cardiorespiratory fi tness, and subsequent reducti ons in fati gue. Finally, IPD meta-analyses benefi ts from a fl exible data harmonizati on platf orm that facilitates harmonizing data during data collecti on, especially when the number of studies and variables is large.
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