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Exercise for women receiving adjuvant therapy of breast-cancer [Elektronische Ressource] : a systematic review / vorgelegt von Martina Markes

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238 pages
Exercise for women receiving adjuvant therapy of breast-cancer: a systematic review Vorgelegt von Diplom-Biologin Martina Markes aus Köln an der Technischen Universität Berlin Fakultät VII – Wirtschaft und Management zur Erlangung des akademischen Grades Doktorin der Gesundheitswissenschaften / Public Health Dr. P.H. Genehmigte Dissertation Promotionsausschuss: Vorsitzender: Prof. Dr. med. Reinhard Busse Gutachterin: Prof. Dr. phil. Ulrike Maschewsky-Schneider Gutachter: Prof. Dr. med. Karl-Ludwig Resch Tag der wissenschaftlichen Aussprache: 9.12.2010 Berlin 2011 D 83 Abstract Abstract Exercise has become an integral part of breast cancer rehabilitation. A growing body of evidence shows health benefits such as increased physical fitness and reduced fatigue through exercise, not only after breast cancer treatment has finished, but during treatment as well. The aim of this systematic review was to determine the effectiveness of aerobic and resistance exercise interventions during adjuvant treatment of breast can-cer with respect to physical functioning and health-related physical fitness, among other important health outcomes. The findings of controlled trial stud-ies of aerobic, strength, and combined exercise interventions among women undergoing adjuvant treatment of breast cancer were critically evaluated and summarised.
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Exercise for women receiving adjuvant therapy
of breast-cancer: a systematic review





Vorgelegt von
Diplom-Biologin
Martina Markes
aus Köln




an der Technischen Universität Berlin
Fakultät VII – Wirtschaft und Management
zur Erlangung des akademischen Grades
Doktorin der Gesundheitswissenschaften / Public Health
Dr. P.H.

Genehmigte Dissertation





Promotionsausschuss:

Vorsitzender: Prof. Dr. med. Reinhard Busse
Gutachterin: Prof. Dr. phil. Ulrike Maschewsky-Schneider
Gutachter: Prof. Dr. med. Karl-Ludwig Resch

Tag der wissenschaftlichen Aussprache: 9.12.2010




Berlin 2011

D 83
Abstract
Abstract
Exercise has become an integral part of breast cancer rehabilitation. A growing
body of evidence shows health benefits such as increased physical fitness and
reduced fatigue through exercise, not only after breast cancer treatment has
finished, but during treatment as well.
The aim of this systematic review was to determine the effectiveness of aerobic
and resistance exercise interventions during adjuvant treatment of breast can-
cer with respect to physical functioning and health-related physical fitness,
among other important health outcomes. The findings of controlled trial stud-
ies of aerobic, strength, and combined exercise interventions among women
undergoing adjuvant treatment of breast cancer were critically evaluated and
summarised. The potential harm associated with exercise in this vulnerable
period was also examined and discussed. This review was conducted in co-
operation with the Cochrane Breast Cancer Group, and followed the rigorous
review methodology of the Cochrane Collaboration.
Results indeed indicate that important physical and mental health outcomes,
such as health-related physical fitness, fatigue, anxiety, and depression, can be
improved through regular exercise training. There is no evidence currently in
the literature showing an association of moderate physical exercise training
during adjuvant treatment of breast cancer with increased risk of injuries, lym-
phedema, or other harm. Thus, the results of this systematic review support
recommending and encouraging women undergoing adjuvant treatment of
breast cancer to exercise.
If the benefits of participation in exercise programmes are to be preserved over
the course of cancer survivorship, sustained physical exercise is essential. Exer-
cise adherence thus plays a vital role in maintaining the benefits associated with
exercise. The review concludes that understanding the determinants of exercise
adherence and the barriers to participation is important. Applying strategies for
behaviour change to individual situations can help in developing and maintain-
ing the habits associated with a healthy lifestyle. Besides developing the evi-
dence base through further research, it is recommended that further activities
should focus as well on how research findings can be translated in to public
health practice.
Table of contents
Table of Contents
List of figures _______________________________________________IV
List of tables ________________________________________________ V
List of abbreviations, acronyms and units of measurement___________VI
Executive Summary ___________________________________________ 1
1 Introduction _____________________________________________ 5
2 Setting the context ________________________________________ 8
2.1 Logic model of the review__________________________________ 8
2.2 Breast cancer treatment 12
2.3 Rationale for exercise interventions ________________________ 13
2.3.1 Health-related physical fitness 13
2.3.2 Treatment-related symptoms ___________________________________ 19
2.3.3 Biological and physiological problems ___________________________ 21
2.3.4 Mental health_______________________________________________ 23
2.3.5 Health-related quality of life 23
2.3.6 Recurrence and survival ______________________________________ 26
2.3.7 Prevalence of treatment-related adverse effects ____________________ 26
2.4 The intervention: exercise ________________________________ 27
2.4.1 Exercise patterns in breast cancer patients ________________________ 27
2.4.2 Behaviour change theories for program planning ___________________ 28
2.4.3 Exercise adherence __________________________________________ 30
2.4.4 se prescription _________________________________________ 32
2.4.5 Exercise Testing ____________________________________________ 33
2.5 Potential harm associated with exercise _____________________ 34
2.6 Previous research _______________________________________ 36
2.7 Preliminary work: rehabilitation sport in Germany ___________ 37
3 Methods _______________________________________________ 39
3.1 The role of systematic reviews in evidence based medicine______ 40
3.2 Execution of the review___________________________________ 41
3.2.1 Review protocol ____________________________________________ 41
3.2.2 Identification of research______________________________________ 41
3.2.3 Search updates within duration of review implementation ____________ 44
3.2.4 Selection of studies __________________________________________ 45
3.2.5 Data extraction _____________________________________________ 47
3.2.6 Study quality assessment 49
3.2.7 Meta-analysis 55
3.3 Methods for the assessment of harm ________________________ 60
4 Results: Identification and description of studies_______________ 63
4.1 Studies of benefit ________________________________________ 63
4.1.1 Process of retrieval of included trials in basic search ________________ 66
4.1.2 Process of retrieval of ongoing trials_____________________________ 67
4.1.3 Characteristics of excluded studies ______________________________ 68
4.1.4 Characteristics of included studies 70
4.2 Studies of harm _________________________________________ 86

I Table of contents
5 Results: Evidence synthesis ________________________________ 89
5.1 Physical health effects____________________________________ 89
5.1.1 Physical functioning _________________________________________ 89
5.1.2 Health-related physical fitness__________________________________ 90
5.1.3 Treatment-related symptoms ___________________________________ 92
5.1.4 Biological and physiological effects _____________________________ 93
5.2 Mental health effects_____________________________________ 95
5.2.1 Emotional distress ___________________________________________ 95
5.2.2 Positive psychological function_________________________________ 95
5.3 Quality of life effects 96
5.3.1 Cancer- and cancer-site-specific quality of life _____________________ 96
5.3.2 Generic health-related quality of life_____________________________ 96
5.4 Adherence and contamination 96
5.5 Forest plots for immediate post-intervention effects __________ 100
5.6 Sustainability of effects__________________________________ 106
5.6.1 Exercise behaviour _________________________________________ 106
5.6.2 Long-term intervention effects ________________________________ 107
5.6.3 Recurrence and survival _____________________________________ 108
5.6.4 Forest plots for long-term intervention outcomes __________________ 109
5.7 Harm from exercise interventions _________________________ 111
5.8 Perception of exercise during breast cancer treatment ________ 112
6 Discussion_____________________________________________ 113
6.1 Summary of main results ________________________________ 113
6.2 Applicability and overall completeness of evidence ___________ 115
6.3 Strengths and limitations of included studies________________ 116
6.3.1 Inconsistencies of effects across studies _________________________ 117
6.3.2 Replicability of the intervention and mediational pathways __________ 118
6.4 Potential biases in the review process ______________________ 120
6.5 Agreements with other reviews ___________________________ 121
7 Conclusions and forecast_________________________________ 122
7.1 Implications for research ________________________________ 122
7.2 Implications for practice 123
7.2.1 Setting up exercise classes____________________________________ 123
8 Bibliography___________________________________________ 126
9 Appendices ____________________________________________ 138
9.1 Appendix 1 – Protocol___________________________________ 138
9.2 Appendix 2 – Search Activities ___________________________ 149
9.2.1 Journals handsearched_______________________________________ 149
9.2.2 Conference proceedings searched ______________________________ 149
9.2.3 Study registers searched _____________________________________ 150
9.2.4 Experts contacted __________________________________________ 150
9.2.5 Search strategy for electronic databases _________________________ 151
9.3 Appendix 3 – Study eligibility form________________________ 154


II Table of contents
9.4 Appendix 4 – Data extraction forms _______________________ 155
9.4.1 Data extraction of study descriptors ____________________________ 155
9.4.2 Instructions for extraction of study descriptors ____________________ 156
9.4.3 Effect size data coding_______________________________________ 158
9.5 Appendix 5 – Study quality forms _________________________ 159
9.5.1 Methodological quality form__________________________________ 159
9.5.2 Code of practice for implementing methodological quality criteria ____ 160
9.5.3 Intervention quality form_____________________________________ 162
9.6 Appendix 6 – Identification/critical appraisal of studies of harm 163
9.6.1 Medline search strategy for studies of harm (WinSPIRS 5.0)_________ 163
9.6.2 Data extraction form for studies of harm_________________________ 164
9.6.3 Quality assessment form for studies of harm _____________________ 165
9.7 Appendix 7 – Reference list of excluded studies of benefit _____ 166
9.8 Appendix 8 – Included studies of benefit ___________________ 168
9.8.1 Study descriptors and effect size statistics________________________ 168
9.8.2 Intervention quality _________________________________________ 214
9.9 Appendix 9 – Characteristics of studies adressing harm_______ 215
9.9.1 Reference list of included studies of harm _______________________ 215
9.9.2 Reference list of excluded studies of harm 215
9.9.3 Quality of studies of harm ____________________________________ 216
9.9.4 Study descriptors and effect size data of studies of harm ____________ 217
9.10 Appendix 10 – Outcome assessment instruments_____________ 219
9.11 Appendix 11 – Effect size calculation: inputs into meta-analyses 221
9.12 Appendix 12 – Forest plots _______________________________ 222
9.12.1 Immediate post-intervention outcomes________________________ 222
9.12.2 Long-term outcomes______________________________________ 225

III Table of contents
List of figures
Figure 1: Logic model for evaluation of exercise interventions..........................11
Figure 2: Breast cancer treatment overview...........................................................14
Figure 3: A functional performance framework....................................................15
Figure 4: Work breakdown structure ......................................................................42
Figure 5: Process flow of review steps....................................................................48
Figure 6: Flow diagram of study selection process ...............................................64
Figure 7: Meta-analysis for cardiorespiratory fitness ..........................................100
Figure 8: Meta-analysis for strength ......................................................................101
Figure 9: Meta-analysis for strength with resistance exercise training studies 101
Figure 10: Meta-analysis for body composition ..................................................102
Figure 11: Meta-analysis for cancer-related fatigue.............................................103
Figure 12: Meta-analysis for cancer-related depression......................................104
Figure 13: Meta-analysis for anxiety ......................................................................104
Figure 14: Meta-analysis for cancer-site-specific quality of life.........................105
Figure 15: Meta-analysis for physical activity.......................................................109
Figure 16: Meta-analysis for long-term effect on fatigue ...................................109
Figure 17: Meta-analysis for long-term effect on depression ............................110
Figure 18: Meta-analysis for long-term effect on cancer-specific quality of life
....................................................................................................110

IV Table of contents
List of tables
Table 1: Inclusion criteria for reviewing benefits of exercise..............................46
Table 2: Quality criteria assessed with the vanTulder scale .................................51
Table 3: Criteria for assessing quality of aerobic endurance training .................53
Table 4: Criteria for assessing quality of muscular endurance training ..............54
Table 5: Inclusion criteria for reviewing harm associated with exercise............61
Table 6: Reference list of included studies .............................................................65
Table 7: Identification of included studies per database in the basic search.....67
Table 8: Origin of reports of included trials in the basic search .........................67
Table 9: Origin of ongoing trials..............................................................................68
Table 10: Characteristics of excluded studies.........................................................68
Table 11: Description of interventions and study characteristics .......................73
Table 12: Outcomes reported ..................................................................................78
Table 13: Quality criteria met by studies.................................................................81
Table 14: Number of studies meeting individual quality criteria .......................82
Table 15: Characteristics of included studies .........................................................83
Table 16: Characteristics of studies of harm..........................................................88
Table 17: Summary of findings: immediate post-intervention effects ..............99
Table 18: Summary of findings: long-term effects..............................................108
Table 19: Summary of findings: harm...................................................................112
V Table of contents
List of abbreviations, acronyms and units of measurement
ACSM American College of Sports Medicine
AET Aerobic exercise training
ANOVA Analysis of variance
BDI Beck Depression Inventory
%BF Body fat percentage
BMD Bone mineral density
CACE Complier-Average Causal Effect
CBCG Cochrane Breast Cancer Group
CES-D Center for Epidemiological Studies – Depression Scale
CBCSR Cochrane Breast Cancer Group Specialised Register
CDSR Cochrane Database of Systematic Reviews
CI Confidence interval
CINAHL Cumulative Index to Nursing and Allied Health Literature
CONFSCI Conference Papers Index
CONSORT CONsolidated Standards of Reporting Trials
DBS German Federation for Disabled Sports,
Deutscher Behindertensportverband
df Degrees of freedom
DOSB German Sports Federation, Deutscher Olympischer Sportbund
FACT Functional Assessment of Cancer Therapy instrument
FACT–An Functional assessment of cancer therapy – Anemia scale
FACT–B erapy – Breast cancer scale
FACT–ES cancer therapy – Endocrine symptom
scale
FACT–F Functional assessment of cancer therapy – Fatigue
FACT–G erapy – General scale
g Hedge’s g
HR Maximum heart rate max
HR Heart rate reserve reserve
ICC Intra-class correlation coefficient
2 I Degree of inconsistency across studies in meta-analysis
IQR Interquartile range
LBM Lean body mass
M Mean
Min minutes
12 MWT 12-minute walk test
Mo months
NA Negative affects
NCCN National Comprehensive Cancer Network
NKCA Natural Killer Cytotoxic Activity
PFS Piper Fatigue Scale
VI Table of contents
POMS Profile of mood states
PA Positive affects
PANAS Positive and Negative Affect Schedule
PSQI Pittsburgh Sleep Quality Index
Q Cochran’s Q
RCT Randomised controlled trial
RET Resistance exercise training
RevMan RevMan Analyses (Computer Programme)
1-RM One repetition maximum
RPE Rating of Perceived Exertion
r-PFS Revised Piper Fatigue Scale
RR Relative Risk
SAS Symptom assessment scale
SD Standard deviation Self-directed exercise training
SE m -m1 2 Standard error of the difference in means
SF-36 Medical Outcomes Study 36-Item Short Form
SGB IX Book 9 of the German social code, Sozialgesetzbuch
SIGLE System for Information on Grey Literature
SMD Standardised mean difference
SPSS Statistical Product and Service Solutions
STAI Spielberger State Anxiety Inventory
SU Supervised exercise training
TMD Total mood disturbance
TNM Tumour node metastasis system
VAS Visual analogue scale
VO max Maximal oxygen consumption 2
WHO World Health Organization
WHOQOL World Health Organization Quality of Life project
Wk weeks
WISE Women International Space Simulation for Exploration
WMD Weighted mean difference
Yr years

VII Executive Summary
Executive Summary
Breast cancer remains an important public health problem in Europe and the ageing of the
European population will cause cancer incidence data to continue to increase. The principal
treatments for breast cancer are surgery, chemotherapy, radiotherapy, and hormonal therapy, and
evidence suggests that these are very effective at improving disease-free and overall survival.
However, these therapies can compromise women’s physical, mental, or social health. Evidence
continues to accumulate on the positive impact of exercise on women’s physical or mental health
and on quality of life improvements during treatment. The literature suggests, however, that
many women who exercised prior to being diagnosed with breast cancer do not continue to
exercise during their treatment. Over time, prolonged inactivity leads to decreased muscle
strength, progressive loss of physical functioning and a decreased ability to perform the activities
of daily living. Women, clinicians, and health policy makers need reliable, up-to-date information
from controlled trials on the benefits and potential harm from exercise during adjuvant cancer
treatment, to make evidence-based decisions about interventions. At present, a diverse range of
primary studies exists in the scientific literature regarding the role of exercise during treatment for
breast cancer, and this systematic review seeks to summarise this evidence to date.
Methods of the systematic review
This review was conducted in co-operation with the Cochrane Breast Cancer Group, and fol-
lowed the rigorous review methodology of the Cochrane Collaboration. The research question is:
should women undergoing adjuvant treatment of breast cancer be encouraged to exercise? Study
identification was based on a comprehensive search strategy with a variety of commonly used
electronic databases and manual search methods. Inclusion and exclusion criteria were developed
in accordance with the review question, and were defined in terms of the population, interven-
tions, outcomes, and the study designs of interest. Trials were included that reported on women
receiving adjuvant treatment (chemotherapy, hormonal therapy, or radiotherapy) for breast can-
cer. Breast cancer was restricted to stages 0-III, and trials which included women with stage IV
breast cancer (i.e., with distant metastasis) were excluded from the review. Trials that included
women who had completed adjuvant cancer treatment, or who were being treated for other can-
cers were excluded. Trials with an intervention consisting of aerobic or resistance exercise were
included, but those that examined complex exercise interventions (e.g., a program of exercise and
diet, or a program of exercise and behavioural therapy) were excluded. Trials in which exercise
interventions were restricted to selected body functions only (e.g., arm mobility) were also ex-
cluded. Trials were included that employed at least one of the following outcome measures:
physical functioning, health-related physical fitness, symptom experience, biological or physio-
logical outcomes, mental health, health-related quality of life and harm. Both randomised con-
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