Effects of supervised exercise during adjuvant endocrine therapy in overweight or obese patients with breast cancer: The I-MOVE study

Harm L Ormel, Carolina P Schröder, Gabriela G F van der Schoot, Nico-Derk L Westerink, Annette W G van der Velden, Boelo Poppema, Aline H Vrieling, Jourik A Gietema, Annemiek M E Walenkamp, Anna K L Reyners, Harm L Ormel, Carolina P Schröder, Gabriela G F van der Schoot, Nico-Derk L Westerink, Annette W G van der Velden, Boelo Poppema, Aline H Vrieling, Jourik A Gietema, Annemiek M E Walenkamp, Anna K L Reyners

Abstract

Background: Adjuvant endocrine therapy (ET) in patients with breast cancer (BC) increases the risk of becoming less physically active. Physical inactivity is associated with a higher risk of treatment-related side effects and mortality. This study investigated whether supervised exercise increased the proportion of patients adhering to the national physical activity (PA) guideline during adjuvant ET in overweight or obese BC patients.

Methods: This multicentre single-arm clinical trial included patients with BC participating in a 12-week supervised exercise intervention. An accelerometer measured moderate to vigorous PA (MVPA) at baseline (T0), after 12 (T1) and 26 weeks (T2). The primary endpoint was change in the proportion of patients with weekly ≥150 min of MVPA at T1 compared to T0. Secondary endpoints were adherence to PA guideline at T2, metabolic syndrome (MetS), body composition, health-related quality of life (HRQoL) and BC-specific functioning and symptoms, self-reported PA, self-efficacy, exercise motivation and satisfaction with life.

Results: 141 patients with a median age of 61 years and a mean BMI of 31.3 participated. Adherence to the PA guideline increased from 38.3% at T0, to 40.4% at T1 (p = .112) and 44.7% at T2 (p = .003). MetS, body composition, HRQoL, BC-specific functioning and symptoms (i.e. fatigue, dyspnoea), self-reported PA, self-efficacy, exercise motivation and satisfaction with life improved significantly over time.

Conclusions: Supervised exercise increased the proportion of BC patients adhering to the PA guideline over time. Furthermore, MetS, body composition, HRQoL and symptoms improved. Our findings highlight the clinical relevance of supervised exercise during ET in overweight BC patients.

Clinical trial information: (NCT02424292).

Keywords: Breast cancer; Endocrine therapy; Exercise; Oncologic rehabilitation; Physical activity.

Conflict of interest statement

Declaration of competing interest All authors have nothing to disclose.

Copyright © 2021 The Authors. Published by Elsevier Ltd.. All rights reserved.

Figures

Fig. 1
Fig. 1
CONSORT diagram of the I-MOVE study. PS, performance score; BMI, body mass index; CVD, cardiovascular disease; T0, baseline; T1, post-intervention (12 weeks); T2, follow-up (26 weeks).
Fig. 2
Fig. 2
Alluvial diagram of proportion of patients adhering to the PA guideline. Flows between the blocks represent changes in clusters of patients that adhere or do not adhere to the PA guideline over time. PA, physical activity; T0, baseline; T1, post-intervention (12 weeks); T2, follow-up (26 weeks).
Fig. 3
Fig. 3
Overall change from baseline. (A) EORTC QLQ-C30: QoL and functional scales; EORTC QLQ-BR23: functional scales. (B) EORTC QLQ-C30: QoL and symptom scales; EORTC QLQ-BR23: symptom scales. EORTC, European Organization for Research and Treatment of Cancer; QLQ-C30; Quality of Life Questionnaire Core 30; QLQ-BR23, Quality of Life Questionnaire breast cancer module; HRQoL, health-related quality of life; CI, confidence interval; T0-T1, change from baseline to post-intervention (week 12); T0-T2, change from baseline to follow-up (week 26). Asterisks denote that the change from baseline was statistically significant with two-sided p values (∗, p ≤ .05; ∗∗, p ≤ .01). aThe sample sizes for the ‘sexual enjoyment’ functional scale and ‘Upset by hair loss’ symptom scale were smaller than other scales.

References

    1. Bray F., Ferlay J., Soerjomataram I., Siegel R.L., Torre L.A., Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA A Cancer J Clin. 2018;68:394–424. doi: 10.3322/caac.21492.
    1. Avgerinos K.I., Spyrou N., Mantzoros C.S., Dalamaga M. Obesity and cancer risk: emerging biological mechanisms and perspectives. Metabolism. 2019;92:121–135. doi: 10.1016/j.metabol.2018.11.001.
    1. van Gemert W.A., Lanting C.I., Goldbohm R.A., van den Brandt P.A., Grooters H.G., Kampman E. The proportion of postmenopausal breast cancer cases in The Netherlands attributable to lifestyle-related risk factors. Breast Canc Res Treat. 2015;152:155–162. doi: 10.1007/s10549-015-3447-7.
    1. Schmidt M.E., Chang-Claude J., Vrieling A., Seibold P., Heinz J., Obi N. Association of pre-diagnosis physical activity with recurrence and mortality among women with breast cancer. Int J Canc. 2013;133:1431–1440. doi: 10.1002/ijc.28130.
    1. Foucaut A.-M., Berthouze S.E., Touillaud M., Morelle M., Bourne-Branchu V., Kempf-Lépine A.-S. Deterioration of physical activity level and metabolic risk factors after early-stage breast cancer diagnosis. Cancer Nurs. 2015;38:E1–E9. doi: 10.1097/NCC.0000000000000187.
    1. De Groef A., Geraerts I., Demeyer H., Van der Gucht E., Dams L., de Kinkelder C. Physical activity levels after treatment for breast cancer: two-year follow-up. Breast. 2018;40:23–28. doi: 10.1016/j.breast.2018.04.009.
    1. Irwin M.L., Cartmel B., Gross C.P., Ercolano E., Li F., Yao X. Randomized exercise trial of aromatase inhibitor-induced arthralgia in breast cancer survivors. J Clin Oncol. 2015;33:1104–1111. doi: 10.1200/JCO.2014.57.1547.
    1. Sadim M., Xu Y., Selig K., Paulus J., Uthe R., Agarwl S. A prospective evaluation of clinical and genetic predictors of weight changes in breast cancer survivors. Cancer. 2017;123:2413–2421. doi: 10.1002/cncr.30628.
    1. Baglia M.L., Lin I.H., Cartmel B., Sanft T., Ligibel J., Hershman D.L. Endocrine-related quality of life in a randomized trial of exercise on aromatase inhibitor-induced arthralgias in breast cancer survivors. Cancer. 2019;125(13):2262–2271. doi: 10.1002/cncr.32051.
    1. Gal R., Monninkhof E.M., Peeters P.H.M., van Gils C.H., van den Bongard D.H.J.G., Wendel-Vos G.C.W. Physical activity levels of women with breast cancer during and after treatment, a comparison with the Dutch female population. Acta Oncol (Madr) 2019:1–9. doi: 10.1080/0284186X.2018.1563712.
    1. Weggemans R.M., Backx F.J.G., Borghouts L., Chinapaw M., Hopman M.T.E., Koster A. The 2017 Dutch physical activity guidelines. Int J Behav Nutr Phys Activ. 2018;15:1–12. doi: 10.1186/s12966-018-0661-9.
    1. Schermers D.P., Jongert D.M.W.A., Chorus D.I.A.M.J., Verheijden D.I.M.W. Inleiding bij de KNGF standaarden Inhoudsopgave. TNO-Rapport. 2008;32
    1. Mok A., Khaw K.-T., Luben R., Wareham N., Brage S. Physical activity trajectories and mortality: population based cohort study. BMJ. 2019:l2323. doi: 10.1136/bmj.l2323.
    1. Dieli-Conwright C.M., Courneya K.S., Demark-Wahnefried W., Sami N., Lee K., Sweeney F.C. Aerobic and resistance exercise improves physical fitness, bone health, and quality of life in overweight and obese breast cancer survivors: a randomized controlled trial. Breast Cancer Res. 2018;20:1–10. doi: 10.1186/s13058-018-1051-6.
    1. Perry R.J., Shulman G.I. Mechanistic links between obesity, insulin, and cancer. Trends in Cancer. 2020;6:75–78. doi: 10.1016/j.trecan.2019.12.003.
    1. Schmitz K.H., Courneya K.S., Matthews C., Demark-Wahnefried W., Galvão D.A., Pinto B.M. American college of sports medicine roundtable on exercise guidelines for cancer survivors. Med Sci Sports Exerc. 2010;42:1409–1426. doi: 10.1249/MSS.0b013e3181e0c112.
    1. Karvonen J., Vuorimaa T. Heart rate and exercise intensity during sports activities. Sports Med. 1988;5:303–312. doi: 10.2165/00007256-198805050-00002.
    1. Bandura A. Prentice-Hall, Inc; Englewood Cliffs, NJ, US: 1986. Social foundations of thought and action: a social cognitive theory.
    1. Migueles J.H., Rowlands A.V., Huber F., Sabia S., van Hees V.T. GGIR: a research community–driven open source R package for generating physical activity and sleep outcomes from multi-day raw accelerometer data. J Meas Phys Behav. 2019;2:188–196. doi: 10.1123/jmpb.2018-0063.
    1. Migueles J.H., Cadenas-Sanchez C., Rowlands A.V., Henriksson P., Shiroma E.J., Acosta F.M. Comparability of accelerometer signal aggregation metrics across placements and dominant wrist cut points for the assessment of physical activity in adults. Sci Rep. 2019;9:1–12. doi: 10.1038/s41598-019-54267-y.
    1. Hildebrand M., Van Hees V.T., Hansen B.H., Ekelund U. Age group comparability of raw accelerometer output from wrist-and hip-worn monitors. Med Sci Sports Exerc. 2014;46:1816–1824. doi: 10.1249/MSS.0000000000000289.
    1. Scott J.J., Rowlands A.V., Cliff D.P., Morgan P.J., Plotnikoff R.C., Lubans D.R. Comparability and feasibility of wrist- and hip-worn accelerometers in free-living adolescents. J Sci Med Sport. 2017;20:1101–1106. doi: 10.1016/j.jsams.2017.04.017.
    1. Alberti K.G.M.M., Eckel R.H., Grundy S.M., Zimmet P.Z., Cleeman J.I., Donato K.A. Harmonizing the metabolic syndrome. Circulation. 2009;120:1640–1645. doi: 10.1161/CIRCULATIONAHA.109.192644.
    1. Bateman L.A., Slentz C.A., Willis L.H., Shields A.T., Piner L.W., Bales C.W. Comparison of aerobic versus resistance exercise training effects on metabolic syndrome (from the studies of a targeted risk reduction intervention through defined exercise - STRRIDE-AT/RT) Am J Cardiol. 2011;108:838–844. doi: 10.1016/j.amjcard.2011.04.037.
    1. Durnin JVGA, Womersley J. Its estimation from skinfold thickness: measurements on. Br J Nutr. 1973;32:77–97. doi: 10.1079/BJN19740060.
    1. Groenvold M., Klee M.C., Sprangers M.A.G., Aaronson N.K. Validation of the EORTC QLQ-C30 quality of life questionnaire through combined qualitative and quantitative assessment of patient-observer agreement. J Clin Epidemiol. 1997;50:441–450. doi: 10.1016/S0895-4356(96)00428-3.
    1. Sprangers M.A., Groenvold M., Arraras J.I., Franklin J., te Velde A., Muller M. The European Organization for Research and Treatment of Cancer breast cancer-specific quality-of-life questionnaire module: first results from a three-country field study. J Clin Oncol. 1996;14:2756–2768. doi: 10.1200/JCO.1996.14.10.2756.
    1. Washburn R.A., McAuley E., Katula J., Mihalko S.L., Boileau R.A. The physical activity scale for the elderly (PASE) J Clin Epidemiol. 1999;52:643–651. doi: 10.1016/S0895-4356(99)00049-9.
    1. Bosscher R., Smit J.H., Kempen G.I.J.M. Algemene competentieverwachtingen bij ouderen: een onderzoek naar de psychometrische kenmerken van de Algemene Competentieschaal (ALCOS) Ned Tijdschr Voor Psychol. 1997;52:239–248.
    1. Marcus B.H., Selby V.C., Niaura R.S., Rossi J.S. Self-efficacy and the stages of exercise behavior change. Res Q Exerc Sport. 1992;63:60–66.
    1. Rogers L.Q., Hopkins-Price P., Vicari S., Pamenter R., Courneya K.S., Markwell S. A randomized trial to increase physical activity in breast cancer survivors. Med Sci Sports Exerc. 2009;41:935–946. doi: 10.1249/MSS.0b013e31818e0e1b.
    1. Beasley J.M., Kwan M.L., Chen W.Y., Weltzien E.K., Kroenke C.H., Lu W. Meeting the physical activity guidelines and survival after breast cancer: findings from the after breast cancer pooling project. Breast Canc Res Treat. 2012;131:637–643. doi: 10.1007/s10549-011-1770-1.
    1. Andre F., Ismaila N., Henry N.L., Somerfield M.R., Bast R.C., Barlow W. Use of biomarkers to guide decisions on adjuvant systemic therapy for women with early-stage invasive breast cancer: ASCO clinical practice guideline update-integration of results from TAILORx. J Clin Oncol. 2019;37:1956–1964. doi: 10.1200/JCO.19.00945.
    1. World Health Organization (WHO) European health information gateway . Switz; Geneva: 2016. Prevalence of obesity among adult women in The Netherlands. Accessed April 2021.
    1. An K.-Y., Kang D.-W., Morielli A.R., Friedenreich C.M., Reid R.D., McKenzie D.C. Patterns and predictors of exercise behavior during 24 months of follow-up after a supervised exercise program during breast cancer chemotherapy. Int J Behav Nutr Phys Activ. 2020;17:23. doi: 10.1186/s12966-020-00924-9.
    1. Kampshoff C.S., Jansen F., van Mechelen W., May A.M., Brug J., Chinapaw M.J.M. Determinants of exercise adherence and maintenance among cancer survivors: a systematic review. Int J Behav Nutr Phys Activ. 2014;11:80. doi: 10.1186/1479-5868-11-80.
    1. Ormel H.L., van der Schoot G.G.F., Westerink N.-D.L., Sluiter W.J., Gietema J.A., Walenkamp A.M.E. Self-monitoring physical activity with a smartphone application in cancer patients: a randomized feasibility study (SMART-trial) Support Care Canc. 2018;26:3915–3923. doi: 10.1007/s00520-018-4263-5.
    1. Wong J.N., McAuley E., Trinh L. Physical activity programming and counseling preferences among cancer survivors: a systematic review. Int J Behav Nutr Phys Activ. 2018;15 doi: 10.1186/s12966-018-0680-6.
    1. Rogers L.Q., Courneya K.S., Anton P.M., Hopkins-Price P., Verhulst S., Vicari S.K. Effects of the BEAT Cancer physical activity behavior change intervention on physical activity, aerobic fitness, and quality of life in breast cancer survivors: a multicenter randomized controlled trial. Breast Canc Res Treat. 2015;149:109–119. doi: 10.1007/s10549-014-3216-z.
    1. Derksen J.W.G., Beijer S., Koopman M., Verkooijen H.M., van de Poll-Franse L.V., May A.M. Monitoring potentially modifiable lifestyle factors in cancer survivors: a narrative review on currently available methodologies and innovations for large-scale surveillance. Eur J Canc. 2018;103:327–340. doi: 10.1016/j.ejca.2018.06.017.
    1. Cocks K., King M.T., Velikova G., St-James M.M., Fayers P.M., Brown J.M. Evidence-based guidelines for determination of sample size and interpretation of the European organisation for the research and treatment of cancer quality of life questionnaire core 30. J Clin Oncol. 2011;29:89–96. doi: 10.1200/JCO.2010.28.0107.
    1. Levett-Jones T., Jones M. Physical activity for women diagnosed with breast cancer after adjuvant therapy: a Cochrane review summary. Int J Nurs Stud. 2018 doi: 10.1016/j.ijnurstu.2018.12.002.
    1. Dieli-Conwright C.M., Courneya K.S., Demark-Wahnefried W., Sami N., Lee K., Buchanan T.A. Effects of aerobic and resistance exercise on metabolic syndrome, sarcopenic obesity, and circulating biomarkers in overweight or obese survivors of breast cancer: a randomized controlled trial. J Clin Oncol. 2018;36:875–883. doi: 10.1200/JCO.2017.75.7526.
    1. Ormel H.L., van der Schoot G.G.F., Sluiter W.J., Jalving M., Gietema J.A., Walenkamp A.M.E. Predictors of adherence to exercise interventions during and after cancer treatment: a systematic review. Psycho Oncol. 2018;27:713–724. doi: 10.1002/pon.4612.
    1. Janni W., Rack B.K., Friedl T.W., Müller V., Lorenz R., Rezai M. Lifestyle intervention and effect on disease-free survival in early breast cancer pts: interim analysis from the randomized SUCCESS C study. Cancer Res. 2019;79 doi: 10.1158/1538-7445.SABCS18-GS5-03. Abstract nr GS5-03.
    1. Ligibel J.A., Barry W.T., Alfano C., Hershman D.L., Irwin M., Neuhouser M. Randomized phase III trial evaluating the role of weight loss in adjuvant treatment of overweight and obese women with early breast cancer (Alliance A011401): study design. NPJ Breast Cancer. 2017;3:37. doi: 10.1038/s41523-017-0040-8.
    1. Younge J.O., Kouwenhoven-Pasmooij T.A., Freak-Poli R., Roos-Hesselink J.W., Hunink M.M. Randomized study designs for lifestyle interventions: a tutorial. Int J Epidemiol. 2015;44:2006–2019. doi: 10.1093/ije/dyv183.
    1. Migueles J.H., Cadenas-Sanchez C., Tudor-Locke C., Löf M., Esteban-Cornejo I., Molina-Garcia P. Comparability of published cut-points for the assessment of physical activity: implications for data harmonization. Scand J Med Sci Sports. 2019;29:566–574. doi: 10.1111/sms.13356.
    1. Gal R., May A.M., van Overmeeren E.J., Simons M., Monninkhof E.M. The effect of physical activity interventions comprising wearables and smartphone applications on physical activity: a systematic review and meta-analysis. Sport Med Open. 2018;4:42. doi: 10.1186/s40798-018-0157-9.
    1. Schmitz K.H., Campbell A.M., Stuiver M.M., Pinto B.M., Schwartz A.L., Morris G.S. Exercise is medicine in oncology: engaging clinicians to help patients move through cancer. CA A Cancer J Clin. 2019;69:468–484. doi: 10.3322/caac.21579.

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