Moderators of Exercise Effects on Cancer-related Fatigue: A Meta-analysis of Individual Patient Data

Jonna K. Van Vulpen; Maike G. Sweegers; Petra H.M. Peeters; Kerry S. Courneya; Robert U. Newton; Neil K. Aaronson; Paul B. Jacobsen; Daniel A. Galvaõ; Mai J. Chinapaw; Karen Steindorf; Melinda L. Irwin; Martijn M. Stuiver; Sandi Hayes; Kathleen A. Griffith; Ilse Mesters; Hans Knoop; Martine M. Goedendorp; Nanette Mutrie; Amanda J. Daley; Alex McConnachie; Martin Bohus; Lene Thorsen; Karl Heinz Schulz; Camille E. Short; Erica L. James; Ronald C. Plotnikoff; Martina E. Schmidt; Cornelia M. Ulrich; Marc Van Beurden; Hester S. Oldenburg; Gabe S. Sonke; Wim H. Van Harten; Kathryn H. Schmitz; Kerri M. Winters-Stone; Miranda J. Velthuis; Dennis R. Taaffe; Willem Van Mechelen; Marie José Kersten; Frans Nollet; Jennifer Wenzel; Joachim Wiskemann; Irma M. Verdonck-De Leeuw; Johannes Brug; Anne M. May; Laurien M. Buffart

doi:10.1249/MSS.0000000000002154

Moderators of Exercise Effects on Cancer-related Fatigue: A Meta-analysis of Individual Patient Data

Jonna K. Van Vulpen, Maike G. Sweegers, Petra H.M. Peeters, Kerry S. Courneya, Robert U. Newton, Neil K. Aaronson, Paul B. Jacobsen, Daniel A. Galvaõ, Mai J. Chinapaw, Karen Steindorf, Melinda L. Irwin, Martijn M. Stuiver, Sandi Hayes, Kathleen A. Griffith, Ilse Mesters, Hans Knoop, Martine M. Goedendorp, Nanette Mutrie, Amanda J. Daley, Alex McConnachieMartin Bohus, Lene Thorsen, Karl Heinz Schulz, Camille E. Short, Erica L. James, Ronald C. Plotnikoff, Martina E. Schmidt, Cornelia M. Ulrich, Marc Van Beurden, Hester S. Oldenburg, Gabe S. Sonke, Wim H. Van Harten, Kathryn H. Schmitz, Kerri M. Winters-Stone, Miranda J. Velthuis, Dennis R. Taaffe, Willem Van Mechelen, Marie José Kersten, Frans Nollet, Jennifer Wenzel, Joachim Wiskemann, Irma M. Verdonck-De Leeuw, Johannes Brug, Anne M. May, Laurien M. Buffart^*

^*Corresponding author for this work

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Abstract

Purpose Fatigue is a common and potentially disabling symptom in patients with cancer. It can often be effectively reduced by exercise. Yet, effects of exercise interventions might differ across subgroups. We conducted a meta-analysis using individual patient data of randomized controlled trials (RCT) to investigate moderators of exercise intervention effects on cancer-related fatigue. Methods We used individual patient data from 31 exercise RCT worldwide, representing 4366 patients, of whom 3846 had complete fatigue data. We performed a one-step individual patient data meta-analysis, using linear mixed-effect models to analyze the effects of exercise interventions on fatigue (z score) and to identify demographic, clinical, intervention- A nd exercise-related moderators. Models were adjusted for baseline fatigue and included a random intercept on study level to account for clustering of patients within studies. We identified potential moderators by testing their interaction with group allocation, using a likelihood ratio test. Results Exercise interventions had statistically significant beneficial effects on fatigue (β =-0.17; 95% confidence interval [CI],-0.22 to-0.12). There was no evidence of moderation by demographic or clinical characteristics. Supervised exercise interventions had significantly larger effects on fatigue than unsupervised exercise interventions (β_difference =-0.18; 95% CI-0.28 to-0.08). Supervised interventions with a duration ≤12 wk showed larger effects on fatigue (β =-0.29; 95% CI,-0.39 to-0.20) than supervised interventions with a longer duration. Conclusions In this individual patient data meta-analysis, we found statistically significant beneficial effects of exercise interventions on fatigue, irrespective of demographic and clinical characteristics. These findings support a role for exercise, preferably supervised exercise interventions, in clinical practice. Reasons for differential effects in duration require further exploration.

Original language	English
Pages (from-to)	303-314
Number of pages	12
Journal	Medicine and Science in Sports and Exercise
Volume	52
Issue number	2
DOIs	https://doi.org/10.1249/MSS.0000000000002154
Publication status	Published - Feb 2020

Funding

The content is solely the responsibility of the authors and does not necessarily represent the official views of the (U.S.) National Institutes of Health. In conclusion, we found that exercise has statistically significant beneficial effects on fatigue in patients with cancer. These benefits are consistent across subgroups formed on the basis of demographic and clinical characteristics. The effect of exercise interventions on fatigue is significantly larger when performed under supervision. Differential effects of duration and potential roles of adherence and contamination in these findings need further exploration. Our results support implementation of exercise, preferably supervised exercise interventions, in clinical practice. The results of the study are presented clearly, honestly, and without fabrication, falsification, or inappropriate data manipulation, and results of the present study do not constitute endorsement by ACSM. Conflicts of interest: None declared. Source of funding: The POLARIS study is supported by the Bas Mulder Award, granted to L. M. Buffart by the Alpe d’HuZes foundation/Dutch Cancer Society (VU2011–5045). The contribution of J. K. van Vulpen is financially supported by the World Cancer Research Fund The Netherlands (WCRF NL, project number 2013/997). Disclaimer: The content is solely the responsibility of the authors and does not necessarily represent the official views of the (U.S.) National Institutes of Health.

Funders	Funder number
foundation/Dutch Cancer Society	VU2011–5045
National Institutes of Health
National Center for Advancing Translational Sciences	UL1TR001863
World Cancer Research Fund
Wereld Kanker Onderzoek Fonds	2013/997

Keywords

Cancer
Exercise
Fatigue
Individual Patient Data Meta-Analysis

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1249/MSS.0000000000002154

Moderators of Exercise Effects on Cancer-related FatigueFinal published version, 353 KBLicence: Article 25fa Dutch Copyright Act

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Van Vulpen, J. K., Sweegers, M. G., Peeters, P. H. M., Courneya, K. S., Newton, R. U., Aaronson, N. K., Jacobsen, P. B., Galvaõ, D. A., Chinapaw, M. J., Steindorf, K., Irwin, M. L., Stuiver, M. M., Hayes, S., Griffith, K. A., Mesters, I., Knoop, H., Goedendorp, M. M., Mutrie, N., Daley, A. J., ... Buffart, L. M. (2020). Moderators of Exercise Effects on Cancer-related Fatigue: A Meta-analysis of Individual Patient Data. Medicine and Science in Sports and Exercise, 52(2), 303-314. https://doi.org/10.1249/MSS.0000000000002154

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abstract = "Purpose Fatigue is a common and potentially disabling symptom in patients with cancer. It can often be effectively reduced by exercise. Yet, effects of exercise interventions might differ across subgroups. We conducted a meta-analysis using individual patient data of randomized controlled trials (RCT) to investigate moderators of exercise intervention effects on cancer-related fatigue. Methods We used individual patient data from 31 exercise RCT worldwide, representing 4366 patients, of whom 3846 had complete fatigue data. We performed a one-step individual patient data meta-analysis, using linear mixed-effect models to analyze the effects of exercise interventions on fatigue (z score) and to identify demographic, clinical, intervention- A nd exercise-related moderators. Models were adjusted for baseline fatigue and included a random intercept on study level to account for clustering of patients within studies. We identified potential moderators by testing their interaction with group allocation, using a likelihood ratio test. Results Exercise interventions had statistically significant beneficial effects on fatigue (β =-0.17; 95% confidence interval [CI],-0.22 to-0.12). There was no evidence of moderation by demographic or clinical characteristics. Supervised exercise interventions had significantly larger effects on fatigue than unsupervised exercise interventions (βdifference =-0.18; 95% CI-0.28 to-0.08). Supervised interventions with a duration ≤12 wk showed larger effects on fatigue (β =-0.29; 95% CI,-0.39 to-0.20) than supervised interventions with a longer duration. Conclusions In this individual patient data meta-analysis, we found statistically significant beneficial effects of exercise interventions on fatigue, irrespective of demographic and clinical characteristics. These findings support a role for exercise, preferably supervised exercise interventions, in clinical practice. Reasons for differential effects in duration require further exploration.",

keywords = "Cancer, Exercise, Fatigue, Individual Patient Data Meta-Analysis",

author = "{Van Vulpen}, {Jonna K.} and Sweegers, {Maike G.} and Peeters, {Petra H.M.} and Courneya, {Kerry S.} and Newton, {Robert U.} and Aaronson, {Neil K.} and Jacobsen, {Paul B.} and Galva{\~o}, {Daniel A.} and Chinapaw, {Mai J.} and Karen Steindorf and Irwin, {Melinda L.} and Stuiver, {Martijn M.} and Sandi Hayes and Griffith, {Kathleen A.} and Ilse Mesters and Hans Knoop and Goedendorp, {Martine M.} and Nanette Mutrie and Daley, {Amanda J.} and Alex McConnachie and Martin Bohus and Lene Thorsen and Schulz, {Karl Heinz} and Short, {Camille E.} and James, {Erica L.} and Plotnikoff, {Ronald C.} and Schmidt, {Martina E.} and Ulrich, {Cornelia M.} and {Van Beurden}, Marc and Oldenburg, {Hester S.} and Sonke, {Gabe S.} and {Van Harten}, {Wim H.} and Schmitz, {Kathryn H.} and Winters-Stone, {Kerri M.} and Velthuis, {Miranda J.} and Taaffe, {Dennis R.} and {Van Mechelen}, Willem and Kersten, {Marie Jos{\'e}} and Frans Nollet and Jennifer Wenzel and Joachim Wiskemann and {Verdonck-De Leeuw}, {Irma M.} and Johannes Brug and May, {Anne M.} and Buffart, {Laurien M.}",

year = "2020",

month = feb,

doi = "10.1249/MSS.0000000000002154",

language = "English",

volume = "52",

pages = "303--314",

journal = "Medicine and Science in Sports and Exercise",

issn = "0195-9131",

publisher = "Lippincott Williams and Wilkins",

number = "2",

}

Van Vulpen, JK, Sweegers, MG, Peeters, PHM, Courneya, KS, Newton, RU, Aaronson, NK, Jacobsen, PB, Galvaõ, DA, Chinapaw, MJ, Steindorf, K, Irwin, ML, Stuiver, MM, Hayes, S, Griffith, KA, Mesters, I, Knoop, H, Goedendorp, MM, Mutrie, N, Daley, AJ, McConnachie, A, Bohus, M, Thorsen, L, Schulz, KH, Short, CE, James, EL, Plotnikoff, RC, Schmidt, ME, Ulrich, CM, Van Beurden, M, Oldenburg, HS, Sonke, GS, Van Harten, WH, Schmitz, KH, Winters-Stone, KM, Velthuis, MJ, Taaffe, DR, Van Mechelen, W, Kersten, MJ, Nollet, F, Wenzel, J, Wiskemann, J, Verdonck-De Leeuw, IM, Brug, J, May, AM & Buffart, LM 2020, 'Moderators of Exercise Effects on Cancer-related Fatigue: A Meta-analysis of Individual Patient Data', Medicine and Science in Sports and Exercise, vol. 52, no. 2, pp. 303-314. https://doi.org/10.1249/MSS.0000000000002154

TY - JOUR

T1 - Moderators of Exercise Effects on Cancer-related Fatigue

T2 - A Meta-analysis of Individual Patient Data

AU - Van Vulpen, Jonna K.

AU - Sweegers, Maike G.

AU - Peeters, Petra H.M.

AU - Courneya, Kerry S.

AU - Newton, Robert U.

AU - Aaronson, Neil K.

AU - Jacobsen, Paul B.

AU - Galvaõ, Daniel A.

AU - Chinapaw, Mai J.

AU - Steindorf, Karen

AU - Irwin, Melinda L.

AU - Stuiver, Martijn M.

AU - Hayes, Sandi

AU - Griffith, Kathleen A.

AU - Mesters, Ilse

AU - Knoop, Hans

AU - Goedendorp, Martine M.

AU - Mutrie, Nanette

AU - Daley, Amanda J.

AU - McConnachie, Alex

AU - Bohus, Martin

AU - Thorsen, Lene

AU - Schulz, Karl Heinz

AU - Short, Camille E.

AU - James, Erica L.

AU - Plotnikoff, Ronald C.

AU - Schmidt, Martina E.

AU - Ulrich, Cornelia M.

AU - Van Beurden, Marc

AU - Oldenburg, Hester S.

AU - Sonke, Gabe S.

AU - Van Harten, Wim H.

AU - Schmitz, Kathryn H.

AU - Winters-Stone, Kerri M.

AU - Velthuis, Miranda J.

AU - Taaffe, Dennis R.

AU - Van Mechelen, Willem

AU - Kersten, Marie José

AU - Nollet, Frans

AU - Wenzel, Jennifer

AU - Wiskemann, Joachim

AU - Verdonck-De Leeuw, Irma M.

AU - Brug, Johannes

AU - May, Anne M.

AU - Buffart, Laurien M.

PY - 2020/2

Y1 - 2020/2

N2 - Purpose Fatigue is a common and potentially disabling symptom in patients with cancer. It can often be effectively reduced by exercise. Yet, effects of exercise interventions might differ across subgroups. We conducted a meta-analysis using individual patient data of randomized controlled trials (RCT) to investigate moderators of exercise intervention effects on cancer-related fatigue. Methods We used individual patient data from 31 exercise RCT worldwide, representing 4366 patients, of whom 3846 had complete fatigue data. We performed a one-step individual patient data meta-analysis, using linear mixed-effect models to analyze the effects of exercise interventions on fatigue (z score) and to identify demographic, clinical, intervention- A nd exercise-related moderators. Models were adjusted for baseline fatigue and included a random intercept on study level to account for clustering of patients within studies. We identified potential moderators by testing their interaction with group allocation, using a likelihood ratio test. Results Exercise interventions had statistically significant beneficial effects on fatigue (β =-0.17; 95% confidence interval [CI],-0.22 to-0.12). There was no evidence of moderation by demographic or clinical characteristics. Supervised exercise interventions had significantly larger effects on fatigue than unsupervised exercise interventions (βdifference =-0.18; 95% CI-0.28 to-0.08). Supervised interventions with a duration ≤12 wk showed larger effects on fatigue (β =-0.29; 95% CI,-0.39 to-0.20) than supervised interventions with a longer duration. Conclusions In this individual patient data meta-analysis, we found statistically significant beneficial effects of exercise interventions on fatigue, irrespective of demographic and clinical characteristics. These findings support a role for exercise, preferably supervised exercise interventions, in clinical practice. Reasons for differential effects in duration require further exploration.

AB - Purpose Fatigue is a common and potentially disabling symptom in patients with cancer. It can often be effectively reduced by exercise. Yet, effects of exercise interventions might differ across subgroups. We conducted a meta-analysis using individual patient data of randomized controlled trials (RCT) to investigate moderators of exercise intervention effects on cancer-related fatigue. Methods We used individual patient data from 31 exercise RCT worldwide, representing 4366 patients, of whom 3846 had complete fatigue data. We performed a one-step individual patient data meta-analysis, using linear mixed-effect models to analyze the effects of exercise interventions on fatigue (z score) and to identify demographic, clinical, intervention- A nd exercise-related moderators. Models were adjusted for baseline fatigue and included a random intercept on study level to account for clustering of patients within studies. We identified potential moderators by testing their interaction with group allocation, using a likelihood ratio test. Results Exercise interventions had statistically significant beneficial effects on fatigue (β =-0.17; 95% confidence interval [CI],-0.22 to-0.12). There was no evidence of moderation by demographic or clinical characteristics. Supervised exercise interventions had significantly larger effects on fatigue than unsupervised exercise interventions (βdifference =-0.18; 95% CI-0.28 to-0.08). Supervised interventions with a duration ≤12 wk showed larger effects on fatigue (β =-0.29; 95% CI,-0.39 to-0.20) than supervised interventions with a longer duration. Conclusions In this individual patient data meta-analysis, we found statistically significant beneficial effects of exercise interventions on fatigue, irrespective of demographic and clinical characteristics. These findings support a role for exercise, preferably supervised exercise interventions, in clinical practice. Reasons for differential effects in duration require further exploration.

KW - Cancer

KW - Exercise

KW - Fatigue

KW - Individual Patient Data Meta-Analysis

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UR - http://www.scopus.com/inward/citedby.url?scp=85074763027&partnerID=8YFLogxK

U2 - 10.1249/MSS.0000000000002154

DO - 10.1249/MSS.0000000000002154

M3 - Article

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AN - SCOPUS:85074763027

SN - 0195-9131

VL - 52

SP - 303

EP - 314

JO - Medicine and Science in Sports and Exercise

JF - Medicine and Science in Sports and Exercise

IS - 2

ER -

Moderators of Exercise Effects on Cancer-related Fatigue: A Meta-analysis of Individual Patient Data

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