Abstract
The purpose of this study was to conduct an exploratory analysis of the START examining the effects of resistance exercise training (RET) and aerobic exercise training (AET) on sarcopenia, dynapenia, and associated quality of life (QoL) changes in breast cancer (BC) patients receiving adjuvant chemotherapy. Participants were randomized to usual care (UC) (n = 70), AET (n = 64), or RET (n = 66) for the duration of chemotherapy. Measures of sarcopenia [skeletal muscle index (SMI)] and dynapenia [upper extremity (UE) and lower extremity (LE) muscle dysfunction (MD)] were normalized relative to age-/sex-based clinical cut-points. QoL was assessed by the Functional Assessment of Cancer Therapy-Anemia (FACT-An) scales. At baseline, 25.5 % of BC patients were sarcopenic and 54.5 % were dynapenic with both conditions associated with poorer QoL. ANCOVAs showed significant differences favoring RET over UC for SMI (0.32 kg/m2; p = 0.017), UE-MD (0.12 kg/kg; p < 0.001), and LE-MD (0.27 kg/kg; p < 0.001). Chi-square analyses revealed significant effects of RET, compared to UC/AET combined, on reversing sarcopenia (p = 0.039) and dynapenia (p = 0.019). The reversal of sarcopenia was associated with clinically relevant improvements in the FACT-An (11.7 points [95 % confidence interval (CI) −4.2 to 27.6]), the Trial Outcome Index-Anemia (10.0 points [95 % CI −4.0 to 24.1]), and fatigue (5.3 points [95 % CI −1.5 to 12.1]). Early-stage BC patients initiating adjuvant chemotherapy have higher than expected rates of sarcopenia and dynapenia which are associated with poorer QoL. RET during adjuvant chemotherapy resulted in the reversal of both sarcopenia and dynapenia; however, only the reversal of sarcopenia was associated with clinically meaningful improvements in QoL.
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Abbreviations
- 1-RM:
-
One repetition maximum
- AET:
-
Aerobic exercise training
- BC:
-
Breast cancer
- CI:
-
Confidence interval
- DXA:
-
Dual X-ray absorptiometry
- FACT-An:
-
Functional Assessment of Cancer Therapy-Anemia
- HR:
-
Hazard ratio
- LBM:
-
Lean body mass
- LE:
-
Lower extremity
- MD:
-
Muscle dysfunction
- QoL:
-
Quality of life
- RET:
-
Resistance exercise training
- SMI:
-
Skeletal muscle index
- START:
-
Supervised Trial of Aerobic and Resistance Training
- TOI-An:
-
Trial Outcome Index-Anemia
- UC:
-
Usual care
- UE:
-
Upper extremity
- VO2peak :
-
Peak oxygen uptake
References
Shapiro CL, Recht A (2001) Side effects of adjuvant treatment of breast cancer. New Engl J Med 344(26):1997–2008. doi:10.1056/NEJM200106283442607
Griggs JJ, Mangu PB, Anderson H, Balaban EP, Dignam JJ, Hryniuk WM, Morrison VA, Pini TM, Runowicz CD, Rosner GL, Shayne M, Sparreboom A, Sucheston LE, Lyman GH, American Society of Clinical Oncology (2012) Appropriate chemotherapy dosing for obese adult patients with cancer: American Society of Clinical Oncology clinical practice guideline. J Clin Oncol 30(13):1553–1561. doi:10.1200/JCO.2011.39.9436
Griggs JJ, Sorbero ME, Lyman GH (2005) Undertreatment of obese women receiving breast cancer chemotherapy. Arch Intern Med 165(11):1267–1273. doi:10.1001/archinte.165.11.1267
Madarnas Y, Sawka CA, Franssen E, Bjarnason GA (2001) Are medical oncologists biased in their treatment of the large woman with breast cancer? Breast Cancer Res Treat 66(2):123–133
Kaidar-Person O, Bar-Sela G, Person B (2011) The two major epidemics of the twenty-first century: obesity and cancer. Obes Surg 21(11):1792–1797. doi:10.1007/s11695-011-0490-2
Parekh N, Chandran U, Bandera EV (2012) Obesity in cancer survival. Annu Rev Nutr 32:311–342. doi:10.1146/annurev-nutr-071811-150713
Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ (2003) Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. New Engl J Med 348(17):1625–1638. doi:10.1056/NEJMoa021423
Cao Y, Ma J (2011) Body mass index, prostate cancer-specific mortality, and biochemical recurrence: a systematic review and meta-analysis. Cancer Prev Res 4(4):486–501. doi:10.1158/1940-6207.CAPR-10-0229
James FR, Wootton S, Jackson A, Wiseman M, Copson ER, Cutress RI (2015) Obesity in breast cancer—what is the risk factor? Eur J Cancer 51(6):705–720. doi:10.1016/j.ejca.2015.01.057
Prado CM, Baracos VE, McCargar LJ, Reiman T, Mourtzakis M, Tonkin K, Mackey JR, Koski S, Pituskin E, Sawyer MB (2009) Sarcopenia as a determinant of chemotherapy toxicity and time to tumor progression in metastatic breast cancer patients receiving capecitabine treatment. Clin Cancer Res 15(8):2920–2926. doi:10.1158/1078-0432.CCR-08-2242
Villaseñor A, Ballard-Barbash R, Baumgartner KB, Baumgartner RN, Bernstein L, McTiernan A, Neuhouser ML (2012) Prevalence and prognostic effect of sarcopenia in breast cancer survivors: the HEAL Study. J Cancer Surviv 6(4):398–406
Dodson RM, Firoozmand A, Hyder O, Tacher V, Cosgrove DP, Bhagat N, Herman JM, Wolfgang CL, Geschwind J-FH, Kamel IR (2013) Impact of sarcopenia on outcomes following intra-arterial therapy of hepatic malignancies. J Gastrointest Surg 17(12):2123–2132
Prado CM, Lieffers JR, McCargar LJ, Reiman T, Sawyer MB, Martin L, Baracos VE (2008) Prevalence and clinical implications of sarcopenic obesity in patients with solid tumours of the respiratory and gastrointestinal tracts: a population-based study. Lancet Oncol 9(7):629–635. doi:10.1016/S1470-2045(08)70153-0
Tan BH, Birdsell LA, Martin L, Baracos VE, Fearon KC (2009) Sarcopenia in an overweight or obese patient is an adverse prognostic factor in pancreatic cancer. Clin Cancer Res 15(22):6973–6979. doi:10.1158/1078-0432.CCR-09-1525
Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel J-P, Rolland Y, Schneider SM, Topinková E, Vandewoude M, Zamboni M (2010) Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on Sarcopenia in Older People. Age Ageing 39(4):412–423. doi:10.1093/ageing/afq034
Batsis JA, Mackenzie TA, Barre LK, Lopez-Jimenez F, Bartels SJ (2014) Sarcopenia, sarcopenic obesity and mortality in older adults: results from the National Health and Nutrition Examination Survey III. Eur J Clin Nutr 68(9):1001–1007. doi:10.1038/ejcn.2014.117
Muller MJ, Geisler C, Pourhassan M, Gluer CC, Bosy-Westphal A (2014) Assessment and definition of lean body mass deficiency in the elderly. Eur J Clin Nutr 68(11):1220–1227. doi:10.1038/ejcn.2014.169
Courneya KS, Crawford JJ, Adams SC (2015) Physical activity and exercise interventions in cancer survivors. In: Holland JC, Breitbart WS, Jacobsen PB, Lederberg MS, Loscalzo MJ, McCorkle R (eds) Psycho-oncology, 3rd edn. Oxford University Press, New York, pp 515–520
Goodpaster BH, Park SW, Harris TB, Kritchevsky SB, Nevitt M, Schwartz AV, Simonsick EM, Tylavsky FA, Visser M, Newman AB (2006) The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci 61(10):1059–1064
Janssen I, Heymsfield SB, Ross R (2002) Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatr Soc 50(5):889–896. doi:10.1046/j.1532-5415.2002.50216.x
Heymsfield SB, Gallagher D, Mayer L, Beetsch J, Pietrobelli A (2007) Scaling of human body composition to stature: new insights into body mass index. Am J Clin Nutr 86(1):82–91
Jaric S (2002) Muscle strength testing. Sports Med 32(10):615–631
da Silva Alexandre T, De Oliveira Duarte YA, Ferreira Santos JL, Wong R, Lebrão ML (2014) Sarcopenia according to the European Working Group on Sarcopenia in Older People (EWGSOP) versus dynapenia as a risk factor for mortality in the elderly. J Nutr Health Aging 18(8):751–756
Davies MJ, Dalsky GP (1997) Normalizing strength for body size differences in older adults. Med Sci Sports Exerc 29(5):713–717. doi:10.1097/00005768-199705000-00020
Courneya KS, Segal RJ, Mackey JR, Gelmon K, Reid RD, Friedenreich CM, Ladha AB, Proulx C, Vallance JK, Lane K, Yasui Y, McKenzie DC (2007) Effects of aerobic and resistance exercise in breast cancer patients receiving adjuvant chemotherapy: a multicenter randomized controlled trial. J Clin Oncol 25(28):4396–4404. doi:10.1200/JCO.2006.08.2024
Cella D, Eton DT, Lai J, Peterman AH, Merkel DE (2002) Combining anchor and distribution-based methods to derive minimal clinically important differences on the Functional Assessment of Cancer Therapy (FACT) anemia and fatigue scales. J Pain Symptom Manage 24(6):547–561
Lander J (1985) Maximum based on reps. NSCA J 6:60–61
Kelly TL, Wilson KE, Heymsfield SB (2009) Dual energy X-ray absorptiometry body composition reference values from NHANES. PLoS One 4(9):e7038
Brown DA, Miller WC (1998) Normative data for strength and flexibility of women throughout life. Eur J Appl Physiol 78(1):77–82. doi:10.1007/s004210050390
Hollander DB, Kraemer RR, Kilpatrick MW, Ramadan ZG, Reeves GV, Francois M, Hebert EP, Tryniecki JL (2007) Maximal eccentric and concentric strength discrepancies between young men and women for dynamic resistance exercise. J Strength Cond Res 21(1):34–40
Clark BC, Manini TM (2008) Special article “Green Banana”—Sarcopenia not equal dynapenia. J Gerontol A Biol Sci Med Sci 63(8):829–834
Baumgartner RN (2000) Body composition in healthy aging. Ann N Y Acad Sci 904(1):437–448
Morley JE, Baumgartner RN, Roubenoff R, Mayer J, Nair KS (2001) Sarcopenia. J Lab Clin Med 137(4):231–243. doi:10.1067/mlc.2001.113504
da Silva Alexandre T, De Oliveira Duarte YA, Ferreira Santos JL, Wong R, Lebrão ML (2014) Sarcopenia according to the European Working Group on Sarcopenia in older people (EWGSOP) versus dynapenia as a risk factor for disability in the elderly. J Nutr Health Aging 18(5):547–553. doi:10.1007/s12603-014-0465-9
Courneya KS, Segal RJ, McKenzie DC, Dong H, Gelmon K, Friedenreich CM, Yasui Y, Reid RD, Crawford JJ, Mackey JR (2014) Effects of exercise during adjuvant chemotherapy on breast cancer outcomes. Med Sci Sports Exerc 46(9):1744–1751
Ruiz JR, Sui X, Lobelo F, Morrow JR Jr, Jackson AW, Sjostrom M, Blair SN (2008) Association between muscular strength and mortality in men: prospective cohort study. BMJ 337:a439. doi:10.1136/bmj.a439
Ruiz JR, Sui XM, Lobelo F, Lee DC, Morrow JR, Jackson AW, Hebert JR, Matthews CE, Sjostrom M, Blair SN (2009) Muscular strength and adiposity as predictors of adulthood cancer mortality in men. Cancer Epidemiol Biomarkers Prev 18(5):1468–1476. doi:10.1158/1055-9965.EPI-08-1075
Kalantar-Zadeh K, Horwich TB, Oreopoulos A, Kovesdy CP, Younessi H, Anker SD, Morley JE (2007) Risk factor paradox in wasting diseases. Curr Opin Clin Nutr Metab Care 10(4):433–442. doi:10.1097/MCO.0b013e3281a30594
Acknowledgments
The START was supported by a grant from the Canadian Breast Cancer Research Alliance. JRV was supported by a Fredrick Banting and Charles Best Canada Graduate Scholarship from the Canadian Institutes of Health Research. CMF was supported by a Health Senior Scholar Award from Alberta Innovates-Health Solutions and the Alberta Cancer Foundation Weekend to End Women’s Cancers Breast Cancer Chair. KSC was supported by the Canada Research Chairs Program.
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Adams, S.C., Segal, R.J., McKenzie, D.C. et al. Impact of resistance and aerobic exercise on sarcopenia and dynapenia in breast cancer patients receiving adjuvant chemotherapy: a multicenter randomized controlled trial. Breast Cancer Res Treat 158, 497–507 (2016). https://doi.org/10.1007/s10549-016-3900-2
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DOI: https://doi.org/10.1007/s10549-016-3900-2