Skip to main content

Impact of resistance and aerobic exercise on sarcopenia and dynapenia in breast cancer patients receiving adjuvant chemotherapy: a multicenter randomized controlled trial

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

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

  1. 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

    CAS  Article  PubMed  Google Scholar 

  2. 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

    Article  PubMed  Google Scholar 

  3. 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

    Article  PubMed  Google Scholar 

  4. 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

    CAS  Article  PubMed  Google Scholar 

  5. 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

    Article  PubMed  Google Scholar 

  6. Parekh N, Chandran U, Bandera EV (2012) Obesity in cancer survival. Annu Rev Nutr 32:311–342. doi:10.1146/annurev-nutr-071811-150713

    CAS  Article  PubMed  Google Scholar 

  7. 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

    Article  PubMed  Google Scholar 

  8. 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

    CAS  Article  Google Scholar 

  9. 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

    CAS  Article  PubMed  Google Scholar 

  10. 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

    CAS  Article  PubMed  Google Scholar 

  11. 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

    Article  PubMed  PubMed Central  Google Scholar 

  12. 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

    Article  PubMed  PubMed Central  Google Scholar 

  13. 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

    Article  PubMed  Google Scholar 

  14. 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

    CAS  Article  PubMed  Google Scholar 

  15. 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

    Article  PubMed  PubMed Central  Google Scholar 

  16. 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

    CAS  Article  PubMed  Google Scholar 

  17. 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

    CAS  Article  PubMed  Google Scholar 

  18. 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

    Google Scholar 

  19. 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

    Article  PubMed  Google Scholar 

  20. 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

    Article  PubMed  Google Scholar 

  21. 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

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Jaric S (2002) Muscle strength testing. Sports Med 32(10):615–631

    Article  PubMed  Google Scholar 

  23. 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

    Article  Google Scholar 

  24. 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

    CAS  Article  PubMed  Google Scholar 

  25. 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

    Article  PubMed  Google Scholar 

  26. 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

    Article  PubMed  Google Scholar 

  27. Lander J (1985) Maximum based on reps. NSCA J 6:60–61

    Google Scholar 

  28. Kelly TL, Wilson KE, Heymsfield SB (2009) Dual energy X-ray absorptiometry body composition reference values from NHANES. PLoS One 4(9):e7038

    Article  PubMed  PubMed Central  Google Scholar 

  29. 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

    CAS  Article  Google Scholar 

  30. 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

    Article  PubMed  Google Scholar 

  31. Clark BC, Manini TM (2008) Special article “Green Banana”—Sarcopenia not equal dynapenia. J Gerontol A Biol Sci Med Sci 63(8):829–834

    Article  PubMed  Google Scholar 

  32. Baumgartner RN (2000) Body composition in healthy aging. Ann N Y Acad Sci 904(1):437–448

    CAS  Article  PubMed  Google Scholar 

  33. 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

    CAS  Article  PubMed  Google Scholar 

  34. 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

    Article  Google Scholar 

  35. 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

    CAS  Article  PubMed  Google Scholar 

  36. 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

    Article  PubMed  PubMed Central  Google Scholar 

  37. 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

    Article  PubMed  PubMed Central  Google Scholar 

  38. 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

    Article  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kerry S. Courneya.

Ethics declarations

Conflict of Interest

None.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10549-016-3900-2

Keywords

  • Body composition
  • Resistance exercise
  • Skeletal muscle index
  • Muscle dysfunction
  • Quality of life