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The effect of resistance training on muscle strength and physical function in older, postmenopausal breast cancer survivors: a randomized controlled trial
Open accessAbstract
Introduction Older breast cancer survivors (BCS) report more falls and functional limitations than women with no cancer history. Exercise training could reduce risk factors for future falls and disability.Methods We conducted a randomized, controlled trial in 106 early-stage, postmenopausal BCS who were ≥50 years old at diagnosis and post-treatment. Women were randomly assigned to a 1-year resistance + impact exercise program or a stretching placebo program. Endpoints were one repetition maximum bench press and leg press strength, timed five chair stands, 4 m usual walk speed, timed stance tests, handgrip strength, self-report physical function, and fatigue. We also examined the influence of age, adjuvant hormone therapy use, and exercise adherence on study outcomes.Results Women in the resistance + impact training program significantly improved maximal leg (p <0 .02) and bench (p <0 .02) press strength compared to the stretching group. Women who attended 50% or more of prescribed resistance training sessions had significantly better changes in maximal strength measures compared to less adherent women.Conclusions Resistance + impact exercise is superior to stretching at improving maximal muscle strength and exercise adherence contributes to the degree of improvement.Implications for cancer survivors Older BCS can safely engage in resistance exercise that improves lower and upper body strength, thereby reducing a risk factor for falls and future disability. However, the ability of resistance training to shift other indices of fall and disability risk, i.e., balance and function, is unclear. Strategies to promote adherence to resistance training could lead to greater improvements in strength.
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“Breast cancer was the most investigated cancer type (n = 6) [25–30, 32], followed by prostate cancer (n = 2) [28, 31], and one trial included diverse types of cancer [24].”
From Effects of Supervised Multimodal Exercise Interventions on Cancer-Related Fatigue: Systematic Review and Meta-Analysis of Randomized Controlled Trials (2015) · cites this paper as [31]
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“Regarding cancer treatment stage, most studies were performed during current treatment [24, 25, 28–31]; the most common treatment was chemotherapy (n = 522).”
From Effects of Supervised Multimodal Exercise Interventions on Cancer-Related Fatigue: Systematic Review and Meta-Analysis of Randomized Controlled Trials (2015) · cites this paper as [31]
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“However, the evidence base for comparison of our results is sparse, with only one study having tested the effect of PRT on fatigue in 65 older post-menopausal women with BC, finding no effect of the intervention [27].”
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“We have shown that resistance training is acceptable, safe, and beneficial for cancer survivors when delivered in a supervised, group setting [10, 11].”
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“Other studies have reported mild to strong associations between CRF and physical fitness level in various cancer populations in cross-sectional analyses but none of them focused on change data during intervention trials (Winters-Stone et al., 2008; Kilgour et al., 2010; Wiskemann et al., 2011).”
BackgroundWinters‐Stone, K. M., Laudermilk, M., Woo, K. M., Brown, J. C., & Schmitz, K. H. (2014) · Journal of Cancer Survivorship · doi:10.1007/s11764-013-0337-z · Cited by 44
“and is now being explored as a strategy to reverse bone and muscle loss and functional declines related to cancer treatment [15–20].”
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“Cut-off values for stratification variables were selected on the basis of the known measurement error 1-RM testing (27, 44, 45) and DXA (46).”
MethodSelf-citationSchmidt, M. E., Wiskemann, J., Krakowski‐Roosen, H., Knicker, A. J., Habermann, N., Schneeweiß, A., Ulrich, C. M., & Steindorf, K. (2012) · Contemporary Clinical Trials · doi:10.1016/j.cct.2012.10.006 · Cited by 43
“To our knowledge, only seven randomized studies with endpoints CRF investigated a pure resistance training in patients with various cancer types [11,48–53], of which two studies included only prostate cancer patients [48,49] and two others were underpowered (n=22 and 38) [52,53].”
BackgroundPudkasam, S., Feehan, J., Talevski, J., Vingrys, K., Polman, R. C. J., Chinlumprasert, N., Stojanovska, L., & Apostolopoulos, V. (2021) · Maturitas · doi:10.1016/j.maturitas.2021.06.008 · Cited by 51
Santagnello, S. B., Martins, F. M., Júnior, G. N. D. O., de Sousa, J. D. F. R., Nomelini, R. S., Murta, E. F. C., & Orsatti, F. L. (2020) · Supportive Care in Cancer · doi:10.1007/s00520-020-05429-6 · Cited by 40
“[21], as the researchers did not find any significant differences for LBM gain after a 12-month RE protocol when compared with the control group; this was because of the control group that performed only stretching exercises who also obtained LBM gains.”
BackgroundA randomized study to prevent lymphedema in women treated for breast cancer: CALGB 70305 (Alliance)
Paskett, E. D., Le‐Rademacher, J. G., Oliveri, J. M., Liu, H., Seisler, D. K., Sloan, J. A., Armer, J. M., Naughton, M. J., Hock, K., Schwartz, M., et al. (2020) · Cancer · doi:10.1002/cncr.33183 · Cited by 48
“Age, y, median (range) 59 (24-83) 58 (27-88) 58 (24-88) Race, n (%) Missing 3 6 9 Black 38 (15.”
Abrahams, H. J. G., Gielissen, M. F. M., Goedendorp, M. M., Berends, T., Peters, M. E. W. J., Poort, H., Verhagen, C. A. H. H. V. M., & Knoop, H. (2015) · BMC Cancer · doi:10.1186/s12885-015-1787-7 · Cited by 42
Lee, J. (2021) · Journal of sport and health science/Journal of Sport and Health Science · doi:10.1016/j.jshs.2021.02.002 · Cited by 45
Bioelectrical Phase Angle in Patients with Breast Cancer: A Systematic Review
Morlino, D., Cioffi, I., Marra, M., Vincenzo, O. D., Scalfi, L., & Pasanisi, F. (2022) · Cancers · doi:10.3390/cancers14082002 · Cited by 38
Exercise for reducing falls in people living with and beyond cancer
Williams, A. D., Bird, M., Hardcastle, S., Kirschbaum, M., Ogden, K., & Walters, J. A. (2018) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd011687.pub2 · Cited by 37
“[DOI: 10.1186/s12885-016-2805-0] Winters-Stone 2012b {published data only} Winters-Stone KM, Li F, Horak F, Luoh S-W, Bennett JA, Nail L, et al. Comparison of tai chi vs. strength training for fall prevention among female cancer survivors: study protocol for the GET FIT trial.”
BackgroundMethodInfluentialEffects of Resistance Training and Protein Supplementation in Breast Cancer Survivors
Madzima, T. A., Ormsbee, M. J., Schleicher, E. A., Moffatt, R. J., & Panton, L. B. (2017) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000001250 · Cited by 38
“The improvements in muscular strength in the present study are similar to other RT studies in BCS (32,38); however, the RT did not affect adiponectin and CRP.”
ResultRogers, B. H., Brown, J. C., Gater, D. R., & Schmitz, K. H. (2016) · Archives of Physical Medicine and Rehabilitation · doi:10.1016/j.apmr.2016.07.017 · Cited by 36
“Additional criteria included: (5) body mass index (BMI) ≤50 kg/m2; (6) no future plans for surgery during the study; (7) no history of bilateral lymph node removal; (8) no weight lifting in the previous year; and (9) stable body weight while not attempting to lose weight.”
Resistance exercise interventions during and following cancer treatment: a systematic review
Focht, B. C., Clinton, S. K., Devor, S. T., Garver, M. J., Lucas, A. R., Thomas‐Ahner, J. M., & Grainer, E. (2013) · The Journal of Supportive Oncology · doi:10.12788/j.suponc.0002 · Cited by 48
“terventions involving a combination of supervised and unsupervised RE.(23,25,26,32) The RE intervention charac-”
BackgroundInfluentialLee, K.-J., & An, K.-O. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph19095463 · Cited by 36
“[49] reported that RE increased upper and lower body strength in FBCSs over 50 years of age.”
BackgroundExercise is more effective than health education in reducing fatigue in fatigued cancer survivors
Sheehan, P., Denieffe, S., Murphy, N. M., & Harrison, M. (2020) · Supportive Care in Cancer · doi:10.1007/s00520-020-05328-w · Cited by 31
Martins, A., Oliveira, R., Brito, J., Costa, T., Ramalho, F., Pimenta, N., & Santos-Rocha, R. (2021) · Physiology and Behavior · doi:10.1016/j.physbeh.2021.113400 · Cited by 25
Winters‐Stone, K. M., Leo, M. C., & Schwartz, A. L. (2012) · Archives of Osteoporosis · doi:10.1007/s11657-012-0071-6 · Cited by 29
“POWIR improved lower extremity muscle strength in older BCS regardless of age [18], lowering a top risk factor for falls.”
BackgroundSelf-citationMeneses-Echavez, J. F., González‐Jiménez, E., Correa‐Bautista, J. E., Schmidt‐RioValle, J., & Ramírez‐Vélez, R. (2015) · Cadernos de Saúde Pública · doi:10.1590/0102-311x00114414 · Cited by 29
Exercise for managing cancer- and treatment-related side effects in older adults
Loh, K. P., Lin, P., Uth, J., Quist, M., Klepin, H. D., & Mustian, K. M. (2018) · Journal of Geriatric Oncology · doi:10.1016/j.jgo.2018.03.003 · Cited by 29
Wang, L., Shi, Y. X., Wang, T. T., Chen, K., & Shang, S. M. (2022) · Journal of Clinical Nursing · doi:10.1111/jocn.16437 · Cited by 32
Winters‐Stone, K. M., Li, F., Horak, F. B., Luoh, S., Bennett, J. A., Nail, L. M., & Dieckmann, N. F. (2012) · BMC Cancer · doi:10.1186/1471-2407-12-577 · Cited by 29
Self-citationHagstrom, A. D., Shorter, K. A., & Marshall, P. W. (2017) · The Journal of Strength and Conditioning Research · doi:10.1519/jsc.0000000000001890 · Cited by 29
Effects of Exercise Training on Physical Fitness and Biomarker Levels in Breast Cancer Survivors
Kim, T. H., Chang, J. S., & Kong, I. D. (2017) · Journal of Lifestyle Medicine · doi:10.15280/jlm.2017.7.2.55 · Cited by 26
“[18] (2011) Stage I‐IIIa 1 yr after treatment.”
Latihan bodyweight dengan total-body resistance exercise (TRX) dapat meningkatkan kekuatan otot
Nasrulloh, A., & Wicaksono, I. S. (2020) · Jurnal Keolahragaan · doi:10.21831/jk.v8i1.31208 · Cited by 26
“Winters-Stone et al. (2012) mengatakan bahwa wanita yang menghadiri 50% atau lebih dari sesi pelatihan resistensi yang terprogram memiliki perubahan signifikan yang lebih baik dalam ukuran kekuatan maksimal dibandingkan Copyright © 2020, Jurnal Keolahragaan, ISSN 2339-0662 (print), ISSN 2461-0259…”
BackgroundStudien zu körperlichem Training bei onkologischen Patienten: Empfehlungen zu den Erhebungsmethoden
Scharhag‐Rosenberger, F., Becker, T., Streckmann, F., Schmidt, K., & al, E. (2014) · German Journal of Sports Medicine · doi:10.5960/dzsm.2014.148 · Cited by 27
Charati, F. G., Shojaee, L., Haghighat, S., Esmaeili, R., Madani, Z., Charati, J. Y., Hosseini, S. H., & Shafipour, V. (2022) · Clinical Breast Cancer · doi:10.1016/j.clbc.2022.07.009 · Cited by 25
Effects of Resistance Exercise Training on Doxorubicin-Induced Cardiotoxicity
Pfannenstiel, K., & Hayward, R. (2018) · Journal of Cardiovascular Pharmacology · doi:10.1097/fjc.0000000000000574 · Cited by 25
“Currently, cancer rehabilitation programs have begun to incorporate RT due to the fact that this type of training can result in significant improvements in muscular strength, aerobic capacity, and quality of life (Schwartz & WintersStone, 2009; Segal et al., 2003; Winters-Stone et al., 2012).”
BackgroundLiu, X., Xu, X., Cheung, D. S. T., Chau, P. H., Ho, M., Takemura, N., & Lin, C. (2023) · Journal of Cancer Survivorship · doi:10.1007/s11764-023-01396-z · Cited by 26
“) [24, 32], and the remaining studies used single exercise (RE [16, 22, 25, 30, 31, 35] or AE [25, 36] or mind–body exercise [17, 35]).”
InfluentialLee, C. E., Warden, S. J., Szuck, B., & Lau, Y. K. J. (2016) · American Journal of Physical Medicine & Rehabilitation · doi:10.1097/phm.0000000000000440 · Cited by 24
Cancer‐driven changes link T cell frequency to muscle strength in people with cancer: a pilot study
Narsale, A. A., Moya, R., Ma, J., Anderson, L. J., Wu, D. Y., Garcia, J. M., & Davies, J. D. (2019) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12424 · Cited by 22
Musculoskeletal changes after 1 year of exercise in older breast cancer survivors
Dobek, J., Winters‐Stone, K. M., Bennett, J. A., & Nail, L. M. (2013) · Journal of Cancer Survivorship · doi:10.1007/s11764-013-0313-7 · Cited by 24
Self-citationReliability and Agreement of the 10-Repetition Maximum Test in Breast Cancer Survivors
dos Santos, W. D. N., Siqueira, G., Martins, W. R., Vieira, A., Schincaglia, R. M., Gentil, P., & Vieira, C. A. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.00918 · Cited by 21
Evaluation of an Exercise-Based Phase Program as Part of a Standard Care Model for Cancer Survivors
Brown, J. M., Shackelford, D. Y. K., Hipp, M. L., & Hayward, R. (2019) · Translational Journal of the American College of Sports Medicine · doi:10.1249/tjx.0000000000000082 · Cited by 21
“Of note, strength gains were only observed in those who attended 50% or more of the prescribed exercise sessions, and withdrawal from the program occurred primarily in those closest to treatment (38).”
BackgroundPostactivation Potentiation Biases Maximal Isometric Strength Assessment
de Lima, L. C. R., de Oliveira, F. B. D., de Oliveira, T. P., Assumpção, C. D. O., Greco, C. C., Cardozo, A. C., & Denadai, B. S. (2014) · BioMed Research International · doi:10.1155/2014/126961 · Cited by 21
Adult Inflammatory Bowel Disease, Physical Rehabilitation, and Structured Exercise
Elia, J. R., & Kane, S. V. (2018) · Inflammatory Bowel Diseases · doi:10.1093/ibd/izy199 · Cited by 20
Conejo, I., Pajares, B., Alba, E., & Cuesta‐Vargas, A. (2018) · BMC Complementary and Alternative Medicine · doi:10.1186/s12906-018-2236-3 · Cited by 19
“01) compared to a stretching placebo program [65].”
BackgroundWinters‐Stone, K. M., Lyons, K. S., Dieckmann, N. F., Lee, C. S., Mitri, Z. I., & Beer, T. M. (2021) · Trials · doi:10.1186/s13063-021-05548-3 · Cited by 20
Self-citationBland, K. A., Kouw, I. W. K., van Loon, L. J. C., Zopf, E. M., & Fairman, C. M. (2022) · Sports Medicine · doi:10.1007/s40279-021-01638-z · Cited by 19
“[63] reported that supervised resistance exercise training plus impact exercises improved muscular strength compared with a stretching control group in post-menopausal women aged ≥ 50 years with breast cancer (n = 106).”
BackgroundAminnasab, A., Mohammadi, S., Zareinezhad, M., Chatrrouz, T., Mirghafari, S. B., & Rahmani, S. (2018) · PubMed Central · Cited by 19
Winters‐Stone, K. M., Li, F., Horak, F. B., Dieckmann, N. F., Hung, A., Amling, C. L., & Beer, T. M. (2021) · Trials · doi:10.1186/s13063-021-05687-7 · Cited by 19
“CHAMPS is a frequently used, highly reliable [58] measure of physical activity in older adults, including studies in cancer survivors performed by our team [29, 42, 59, 60].”
BackgroundResultSelf-citationReliability of the 1 RM bench press and squat in young women
Augustsson, S. R., & Svantesson, U. M. (2013) · European Journal of Physiotherapy · doi:10.3109/21679169.2013.810305 · Cited by 19
Management of bone disease in women after breast cancer
Milat, F., & Vincent, A. J. (2015) · Climacteric · doi:10.3109/13697137.2015.1100383 · Cited by 18
Metadata
- Authors
- Winters-Stone, K. M., Dobek, J., Bennett, J. A., Nail, L. M., Leo, M. C., & Schwartz, A.
- Affiliations
- Oregon Health & Science University (US)
- Idaho State University (US)
- Venue
- Journal of Cancer Survivorship
- Published
- 2011-12-23
- Volume
- 6
- Issue
- 2
- Pages
- 189-199
- ISSN
- 1932-2259 (ISSN-L)
- 1932-2267
- PMC
- PMC3488606
- OpenAlex
- W2045462605
- Cited by
- 211
- References
- 81
- Citations by year
- 2026: 12 · 2025: 8 · 2024: 17 · 2023: 9 · 2022: 16 · 2021: 17 · 2020: 15 · 2019: 14 · 2018: 16 · 2017: 22 · 2016: 16 · 2015: 17 · 2014: 16 · 2013: 11 · 2012: 5
- FWCI
- 5.03
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Journal of Cancer Survivorship (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Susan G. Komen
- Institut National de la Santé et de la Recherche Médicale
- National Institutes of Health (UL1TR000128)
- Oregon Clinical and Translational Research Institute
- National Cancer Institute (R01CA120123)
- National Center for Research Resources (UL1RR024140)
- National Center for Advancing Translational Sciences
- Topics
- Health Sciences › Medicine › Oncology › Cancer survivorship and care
- Health Sciences › Medicine › Physiology (medical) › Nutrition and Health in Aging
- Health Sciences › Medicine › Oncology › Cancer-related cognitive impairment studies
- Keywords
- resistance training, impact exercise, breast cancer survivors, postmenopausal women, older adults, muscle strength, physical function, exercise adherence, fall risk, balance, grip strength, walking speed, fatigue, stretching, adjuvant endocrine therapy
- MeSH terms
- Aged, Aged, 80 and over, Breast Neoplasms, Exercise Therapy, Female, Humans, Middle Aged, Neoplasm Staging, Prognosis, Single-Blind Method, Postmenopause, Survivors, Hand Strength, Muscle Strength, Resistance Training
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