Skip to main content

Advertisement

SpringerLink
Log in

Exercise-Based Interventions to Counteract Skeletal Muscle Mass Loss in People with Cancer: Can We Overcome the Odds?

  • Review Article
  • Published:
Sports Medicine Aims and scope Submit manuscript

Abstract

Addressing skeletal muscle mass loss is an important focus in oncology research to improve clinical outcomes, including cancer treatment tolerability and survival. Exercise is likely a necessary component of muscle-mass-preserving interventions for people with cancer. However, randomized controlled trials with exercise that include people with cancer with increased susceptibility to more rapid and severe muscle mass loss are limited. The aim of the current review is to highlight features of cancer-related skeletal muscle mass loss, discuss the impact in patients most at risk, and describe the possible role of exercise as a management strategy. We present current gaps within the exercise oncology literature and offer several recommendations for future studies to support research translation, including (1) utilizing accurate and reliable body composition techniques to assess changes in skeletal muscle mass, (2) incorporating comprehensive assessments of patient health status to allow personalized exercise prescription, (3) coupling exercise with robust nutritional recommendations to maximize the impact on skeletal muscle outcomes, and (4) considering key exercise intervention features that may improve exercise efficacy and adherence. Ultimately, the driving forces behind skeletal muscle mass loss are complex and may impede exercise tolerability and efficacy. Our recommendations are intended to foster the design of high-quality patient-centred research studies to determine whether exercise can counteract muscle mass loss in people with cancer and, as such, improve knowledge on this topic.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Ryan AM, Prado CM, Sullivan ES, Power DG, Daly LE. Effects of weight loss and sarcopenia on response to chemotherapy, quality of life, and survival. Nutrition. 2019;67–68:110539.

    Article  PubMed  Google Scholar 

  2. Shachar SS, Williams GR, Muss HB, Nishijima TF. Prognostic value of sarcopenia in adults with solid tumours: a meta-analysis and systematic review. Eur J Cancer. 2016;57:58–67.

    Article  PubMed  Google Scholar 

  3. Pamoukdjian F, Bouillet T, Levy V, Soussan M, Zelek L, Paillaud E. Prevalence and predictive value of pre-therapeutic sarcopenia in cancer patients: a systematic review. Clin Nutr. 2018;37(4):1101–13.

    Article  PubMed  Google Scholar 

  4. Gibson DJ, Burden ST, Strauss BJ, Todd C, Lal S. The role of computed tomography in evaluating body composition and the influence of reduced muscle mass on clinical outcome in abdominal malignancy: a systematic review. Eur J Clin Nutr. 2015;69(10):1079–86.

    Article  CAS  PubMed  Google Scholar 

  5. Kazemi-Bajestani SM, Mazurak VC, Baracos V. Computed tomography-defined muscle and fat wasting are associated with cancer clinical outcomes. Semin Cell Dev Biol. 2016;54:2–10.

    Article  PubMed  Google Scholar 

  6. Blauwhoff-Buskermolen S, Versteeg KS, de van der Schueren MA, den Braver NR, Berkhof J, Langius JA, et al. Loss of muscle mass during chemotherapy is predictive for poor survival of patients with metastatic colorectal cancer. J Clin Oncol. 2016;34(12):1339–44.

    Article  CAS  PubMed  Google Scholar 

  7. Awad S, Tan BH, Cui H, Bhalla A, Fearon KC, Parsons SL, et al. Marked changes in body composition following neoadjuvant chemotherapy for oesophagogastric cancer. Clin Nutr. 2012;31(1):74–7.

    Article  PubMed  Google Scholar 

  8. Brown JC, Caan BJ, Meyerhardt JA, Weltzien E, Xiao J, Cespedes Feliciano EM, et al. The deterioration of muscle mass and radiodensity is prognostic of poor survival in stage I–III colorectal cancer: a population-based cohort study (C-SCANS). J Cachexia Sarcopenia Muscle. 2018;9(4):664–72.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Daly LE, Ni Bhuachalla EB, Power DG, Cushen SJ, James K, Ryan AM. Loss of skeletal muscle during systemic chemotherapy is prognostic of poor survival in patients with foregut cancer. J Cachexia Sarcopenia Muscle. 2018;9(2):315–25.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Dewys WD, Begg C, Lavin PT, Band PR, Bennett JM, Bertino JR, et al. Prognostic effect of weight loss prior to chemotherapy in cancer patients. Eastern Cooperative Oncology Group. Am J Med. 1980;69(4):491–7.

    Article  CAS  PubMed  Google Scholar 

  11. Martin L, Birdsell L, Macdonald N, Reiman T, Clandinin MT, McCargar LJ, et al. Cancer cachexia in the age of obesity: skeletal muscle depletion is a powerful prognostic factor, independent of body mass index. J Clin Oncol. 2013;31(12):1539–47.

    Article  PubMed  Google Scholar 

  12. Prado CM, Lieffers JR, McCargar LJ, Reiman T, Sawyer MB, Martin L, et al. Prevalence and clinical implications of sarcopenic obesity in patients with solid tumours of the respiratory and gastrointestinal tracts: a population-based study. Lancet Oncol. 2008;9(7):629–35.

    Article  PubMed  Google Scholar 

  13. Caan BJ, Meyerhardt JA, Kroenke CH, Alexeeff S, Xiao J, Weltzien E, et al. Explaining the obesity paradox: the association between body composition and colorectal cancer survival (C-SCANS Study). Cancer Epidemiol Biomarkers Prev. 2017;26(7):1008–15.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Antoun S, Borget I, Lanoy E. Impact of sarcopenia on the prognosis and treatment toxicities in patients diagnosed with cancer. Curr Opin Support Palliat Care. 2013;7(4):383–9.

    Article  PubMed  Google Scholar 

  15. Alexandre J, Rey E, Girre V, Grabar S, Tran A, Montheil V, et al. Relationship between cytochrome 3A activity, inflammatory status and the risk of docetaxel-induced febrile neutropenia: a prospective study. Ann Oncol. 2007;18(1):168–72.

    Article  CAS  PubMed  Google Scholar 

  16. Prado CM, Baracos VE, McCargar LJ, Reiman T, Mourtzakis M, Tonkin K, et al. Sarcopenia as a determinant of chemotherapy toxicity and time to tumor progression in metastatic breast cancer patients receiving capecitabine treatment. Clin Cancer Res. 2009;15(8):2920–6.

    Article  CAS  PubMed  Google Scholar 

  17. Feliciano EMC, Kroenke CH, Meyerhardt JA, Prado CM, Bradshaw PT, Kwan ML, et al. Association of systemic inflammation and sarcopenia with survival in nonmetastatic colorectal cancer: results from the C SCANS study. JAMA Oncol. 2017;3(12):e172319.

    Article  PubMed  Google Scholar 

  18. Clark BC, Manini TM. Functional consequences of sarcopenia and dynapenia in the elderly. Curr Opin Clin Nutr Metab Care. 2010;13(3):271–6.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Naito T, Okayama T, Aoyama T, Ohashi T, Masuda Y, Kimura M, et al. Skeletal muscle depletion during chemotherapy has a large impact on physical function in elderly Japanese patients with advanced non-small-cell lung cancer. BMC Cancer. 2017;17(1):571.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Wheelwright S, Darlington A-S, Hopkinson JB, Fitzsimmons D, White A, Johnson CD. A systematic review of health-related quality of life instruments in patients with cancer cachexia. Support Care Cancer. 2013;21(9):2625–36.

    Article  PubMed  Google Scholar 

  21. Gill TM. Hospitalization, restricted activity, and the development of disability among older persons. JAMA. 2004;292(17):2115.

    Article  CAS  PubMed  Google Scholar 

  22. Ligthart-Melis GC, Luiking YC, Kakourou A, Cederholm T, Maier AB, De Van Der Schueren MAE. Frailty, sarcopenia, and malnutrition frequently (co-)occur in hospitalized older adults: a systematic review and meta-analysis. J Am Med Dir Assoc. 2020;21(9):1216–28.

    Article  PubMed  Google Scholar 

  23. Scott D, Hayes A, Sanders KM, Aitken D, Ebeling PR, Jones G. Operational definitions of sarcopenia and their associations with 5-year changes in falls risk in community-dwelling middle-aged and older adults. Osteoporos Int. 2014;25(1):187–93.

    Article  CAS  PubMed  Google Scholar 

  24. Janssen I, Heymsfield SB, Ross R. Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatr Soc. 2002;50(5):889–96.

    Article  PubMed  Google Scholar 

  25. Joglekar S, Nau PN, Mezhir JJ. The impact of sarcopenia on survival and complications in surgical oncology: a review of the current literature. J Surg Oncol. 2015;112(5):503–9.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Khandelwal D, Goel A, Kumar U, Gulati V, Narang R, Dey AB. Frailty is associated with longer hospital stay and increased mortality in hospitalized older patients. J Nutr Health Aging. 2012;16(8):732–5.

    Article  CAS  PubMed  Google Scholar 

  27. Du Y, Karvellas CJ, Baracos V, Williams DC, Khadaroo RG. Sarcopenia is a predictor of outcomes in very elderly patients undergoing emergency surgery. Surgery. 2014;156(3):521–7.

    Article  PubMed  Google Scholar 

  28. Sobestiansky S, Michaelsson K, Cederholm T. Sarcopenia prevalence and associations with mortality and hospitalisation by various sarcopenia definitions in 85–89 year old community-dwelling men: a report from the ULSAM study. BMC Geriatr. 2019;19(1):318.

    Article  PubMed  PubMed Central  Google Scholar 

  29. McLean RR, Shardell MD, Alley DE, Cawthon PM, Fragala MS, Harris TB, et al. Criteria for clinically relevant weakness and low lean mass and their longitudinal association with incident mobility impairment and mortality: the foundation for the National Institutes of Health (FNIH) sarcopenia project. J Gerontol A Biol Sci Med Sci. 2014;69(5):576–83.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Prado CM, Purcell SA, Laviano A. Nutrition interventions to treat low muscle mass in cancer. J Cachexia Sarcopenia Muscle. 2020;11(2):366–80.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Advani SM, Advani PG, VonVille HM, Jafri SH. Pharmacological management of cachexia in adult cancer patients: a systematic review of clinical trials. BMC Cancer. 2018;18(1):1174.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Campbell KL, Winters-Stone KM, Wiskemann J, May AM, Schwartz AL, Courneya KS, et al. Exercise guidelines for cancer survivors: consensus statement from international multidisciplinary roundtable. Med Sci Sports Exerc. 2019;51(11):2375–90.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Cormie P, Zopf EM, Zhang X, Schmitz KH. The impact of exercise on cancer mortality, recurrence, and treatment-related adverse effects. Epidemiol Rev. 2017;39(1):71–92.

    Article  PubMed  Google Scholar 

  34. Hawley JA, Hargreaves M, Joyner MJ, Zierath JR. Integrative biology of exercise. Cell. 2014;159(4):738–49.

    Article  CAS  PubMed  Google Scholar 

  35. Fragala MS, Cadore EL, Dorgo S, Izquierdo M, Kraemer WJ, Peterson MD, et al. Resistance training for older adults: position statement from the national strength and conditioning association. J Strength Cond Res. 2019;33(8):2019–52.

    Article  PubMed  Google Scholar 

  36. American College of Sports Medicine. American College of Sports Medicine position stand. Progression models in resistance training for healthy adults. Med Sci Sports Exerc. 2009;41(3):687–708.

    Article  Google Scholar 

  37. Schiaffino S, Dyar KA, Ciciliot S, Blaauw B, Sandri M. Mechanisms regulating skeletal muscle growth and atrophy. FEBS J. 2013;280(17):4294–314.

    Article  CAS  PubMed  Google Scholar 

  38. Peterson MD, Sen A, Gordon PM. Influence of resistance exercise on lean body mass in aging adults: a meta-analysis. Med Sci Sports Exerc. 2011;43(2):249–58.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Koeppel M, Mathis K, Schmitz KH, Wiskemann J. Muscle hypertrophy in cancer patients and survivors via strength training A meta-analysis and meta-regression. Crit Rev Oncol Hematol. 2021;163:103371. https://doi.org/10.1016/j.critrevonc.2021.103371.

    Article  PubMed  Google Scholar 

  40. Hanson ED, Wagoner CW, Anderson T, Battaglini CL. The independent effects of strength training in cancer survivors: a systematic review. Curr Oncol Rep. 2016;18(5):31.

    Article  PubMed  Google Scholar 

  41. Albanes D, Blair A, Taylor PR. Physical activity and risk of cancer in the NHANES I population. Am J Public Health. 1989;79(6):744–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. De Groef A, Geraerts I, Demeyer H, Van der Gucht E, Dams L, de Kinkelder C, et al. Physical activity levels after treatment for breast cancer: two-year follow-up. Breast. 2018;40:23–8.

    Article  PubMed  Google Scholar 

  43. Irwin ML, Crumley D, McTiernan A, Bernstein L, Baumgartner R, Gilliland FD, et al. Physical activity levels before and after a diagnosis of breast carcinoma: the Health, Eating, Activity, and Lifestyle (HEAL) study. Cancer. 2003;97(7):1746–57.

    Article  PubMed  Google Scholar 

  44. Howlader NA, Krapcho M, Miller D, Brest A, Yu M, Ruhl J, Tatalovich Z, Mariotto A, Lewis DR, Chen HS, Feuer EJ, Cronin KA, editors. SEER cancer statistics review. Bethesda: National Cancer Institute; 1975–2017.

  45. Walston JD. Sarcopenia in older adults. Curr Opin Rheumatol. 2012;24(6):623–7.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyere O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48(1):16–31.

    Article  PubMed  Google Scholar 

  47. Papadopoulou SK, Tsintavis P, Potsaki G, Papandreou D. Differences in the prevalence of sarcopenia in community-dwelling, nursing home and hospitalized individuals. A systematic review and meta-analysis. J Nutr Health Aging. 2020;24(1):83–90.

    Article  CAS  PubMed  Google Scholar 

  48. Hughes VA, Frontera WR, Roubenoff R, Evans WJ, Singh MA. Longitudinal changes in body composition in older men and women: role of body weight change and physical activity. Am J Clin Nutr. 2002;76(2):473–81.

    Article  CAS  PubMed  Google Scholar 

  49. Williams GR, Chen Y, Kenzik KM, McDonald A, Shachar SS, Klepin HD, et al. Assessment of sarcopenia measures, survival, and disability in older adults before and after diagnosis with cancer. JAMA Netw Open. 2020;3(5):e204783.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Van Londen GJ, Levy ME, Perera S, Nelson JB, Greenspan SL. Body composition changes during androgen deprivation therapy for prostate cancer: a 2-year prospective study. Crit Rev Oncol Hematol. 2008;68(2):172–7.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Smith MR, Finkelstein JS, McGovern FJ, Zietman AL, Fallon MA, Schoenfeld DA, et al. Changes in body composition during androgen deprivation therapy for prostate cancer. J Clin Endocrinol Metab. 2002;87(2):599–603.

    Article  CAS  PubMed  Google Scholar 

  52. Antoun S, Birdsell L, Sawyer MB, Venner P, Escudier B, Baracos VE. Association of skeletal muscle wasting with treatment with sorafenib in patients with advanced renal cell carcinoma: results from a placebo-controlled study. J Clin Oncol. 2010;28(6):1054–60.

    Article  CAS  PubMed  Google Scholar 

  53. Broughman JR, Williams GR, Deal AM, Yu H, Nyrop KA, Alston SM, et al. Prevalence of sarcopenia in older patients with colorectal cancer. J Geriatr Oncol. 2015;6(6):442–5.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Shahrokni A, Wu AJ, Carter J, Lichtman SM. Long-term toxicity of cancer treatment in older patients. Clin Geriatr Med. 2016;32(1):63–80.

    Article  PubMed  Google Scholar 

  55. Van Abbema D, Van Vuuren A, Van Den Berkmortel F, Van Den Akker M, Deckx L, Buntinx F, et al. Functional status decline in older patients with breast and colorectal cancer after cancer treatment: a prospective cohort study. J Geriatr Oncol. 2017;8(3):176–84.

    Article  PubMed  Google Scholar 

  56. Ariën F, Baitar A, Perkisas S, Vandewoude M, De Cock A-M. The association between muscle mass and the degree of myosteatosis of the psoas muscle and mortality in older patients with cancer. J Geriatr Oncol. 2021;12(1):85–90.

    Article  PubMed  Google Scholar 

  57. Forbes CC, Swan F, Greenley SL, Lind M, Johnson MJ. Physical activity and nutrition interventions for older adults with cancer: a systematic review. J Cancer Surviv. 2020;14(5):689–711.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Mikkelsen MK, Juhl CB, Lund CM, Jarden M, Vinther A, Nielsen DL. The effect of exercise-based interventions on health-related quality of life and physical function in older patients with cancer receiving medical antineoplastic treatments: a systematic review. Eur Rev Aging Phys Act. 2020. https://doi.org/10.1186/s11556-020-00250-w.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Chin A, Paw MJM, Van Uffelen JGZ, Riphagen I, Van Mechelen W. The functional effects of physical exercise training in frail older people. Sports Med. 2008;38(9):781–93.

    Article  Google Scholar 

  60. Loh KP, Kleckner IR, Lin PJ, Mohile SG, Canin BE, Flannery MA, et al. Effects of a home-based exercise program on anxiety and mood disturbances in older adults with cancer receiving chemotherapy. J Am Geriatr Soc. 2019;67(5):1005–11.

    Article  PubMed  PubMed Central  Google Scholar 

  61. Bourke L, Gilbert S, Hooper R, Steed LA, Joshi M, Catto JW, et al. Lifestyle changes for improving disease-specific quality of life in sedentary men on long-term androgen-deprivation therapy for advanced prostate cancer: a randomised controlled trial. Eur Urol. 2014;65(5):865–72.

    Article  PubMed  Google Scholar 

  62. Galvao DA, Spry N, Denham J, Taaffe DR, Cormie P, Joseph D, et al. A multicentre year-long randomised controlled trial of exercise training targeting physical functioning in men with prostate cancer previously treated with androgen suppression and radiation from TROG 03.04 RADAR. Eur Urol. 2014;65(5):856–64.

    Article  PubMed  Google Scholar 

  63. Winters-Stone KM, Dobek J, Bennett JA, Nail LM, Leo MC, Schwartz A. The effect of resistance training on muscle strength and physical function in older, postmenopausal breast cancer survivors: a randomized controlled trial. J Cancer Surviv. 2012;6(2):189–99.

    Article  PubMed  Google Scholar 

  64. Alberga AS, Segal RJ, Reid RD, Scott CG, Sigal RJ, Khandwala F, et al. Age and androgen-deprivation therapy on exercise outcomes in men with prostate cancer. Support Care Cancer. 2012;20(5):971–81.

    Article  PubMed  Google Scholar 

  65. Marechal R, Fontvieille A, Parent-Roberge H, Fulop T, Riesco E, Pavic M, et al. Effect of a mixed-exercise program on physical capacity and sedentary behavior in older adults during cancer treatments. Aging Clin Exp Res. 2019;31(11):1583–9.

    Article  PubMed  Google Scholar 

  66. Mikkelsen MK, Lund CM, Vinther A, Tolver A, Johansen JS, Chen I, et al. Effects of a 12-week multimodal exercise intervention among older patients with advanced cancer: results from a randomized controlled trial. Oncologist. 2021. https://doi.org/10.1002/onco.13970 (online ahead of print).

    Article  Google Scholar 

  67. Solheim TS, Blum D, Fayers PM, Hjermstad MJ, Stene GB, Strasser F, et al. Weight loss, appetite loss and food intake in cancer patients with cancer cachexia: three peas in a pod?—analysis from a multicenter cross sectional study. Acta Oncol. 2014;53(4):539–46.

    Article  CAS  PubMed  Google Scholar 

  68. de Pinho NB, Martucci RB, Rodrigues VD, D’Almeida CA, Thuler LCS, Saunders C, et al. Malnutrition associated with nutrition impact symptoms and localization of the disease: results of a multicentric research on oncological nutrition. Clin Nutr. 2019;38(3):1274–9.

    Article  PubMed  Google Scholar 

  69. Marshall KM, Loeliger J, Nolte L, Kelaart A, Kiss NK. Prevalence of malnutrition and impact on clinical outcomes in cancer services: a comparison of two time points. Clin Nutr. 2019;38(2):644–51.

    Article  PubMed  Google Scholar 

  70. Hébuterne X, Lemarié E, Michallet M, De Montreuil CB, Schneider SM, Goldwasser F. Prevalence of malnutrition and current use of nutrition support in patients with cancer. JPEN J Parenter Enteral Nutr. 2014;38(2):196–204.

    Article  PubMed  Google Scholar 

  71. Ryan AM, Healy LA, Power DG, Rowley SP, Reynolds JV. Short-term nutritional implications of total gastrectomy for malignancy, and the impact of parenteral nutritional support. Clin Nutr. 2007;26(6):718–27.

    Article  PubMed  Google Scholar 

  72. Haverkort EB, Binnekade JM, Busch OR, van Berge Henegouwen MI, de Haan RJ, Gouma DJ. Presence and persistence of nutrition-related symptoms during the first year following esophagectomy with gastric tube reconstruction in clinically disease-free patients. World J Surg. 2010;34(12):2844–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Spotten LE, Corish CA, Lorton CM, Ui Dhuibhir PM, O’Donoghue NC, O’Connor B, et al. Subjective and objective taste and smell changes in cancer. Ann Oncol. 2017;28(5):969–84.

    Article  CAS  PubMed  Google Scholar 

  74. Bye A, Jordhoy MS, Skjegstad G, Ledsaak O, Iversen PO, Hjermstad MJ. Symptoms in advanced pancreatic cancer are of importance for energy intake. Support Care Cancer. 2013;21(1):219–27.

    Article  PubMed  Google Scholar 

  75. Cao Y, Lu Q, Zhuang B, Zhang L, Wang Y, Jin S, et al. The prevalence of sarcopenia and relationships between dietary intake and muscle mass in head and neck cancer patients undergoing radiotherapy: a longitudinal study. Eur J Oncol Nurs. 2021;53:101943.

    Article  PubMed  Google Scholar 

  76. Hopanci Bicakli D, Ozkaya Akagunduz O, Meseri Dalak R, Esassolak M, Uslu R, Uyar M. The effects of compliance with nutritional counselling on body composition parameters in head and neck cancer patients under radiotherapy. J Nutr Metab. 2017;2017:8631945.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Churchward-Venne TA, Burd NA, Phillips SM. Nutritional regulation of muscle protein synthesis with resistance exercise: strategies to enhance anabolism. Nutr Metab (Lond). 2012;9(1):40.

    Article  CAS  PubMed Central  Google Scholar 

  78. Nicholson BD, Hamilton W, O’Sullivan J, Aveyard P, Hobbs FR. Weight loss as a predictor of cancer in primary care: a systematic review and meta-analysis. Br J Gen Pract. 2018;68(670):e311–22.

    Article  PubMed  PubMed Central  Google Scholar 

  79. Ryan AM, Power DG, Daly L, Cushen SJ, Ni Bhuachalla E, Prado CM. Cancer-associated malnutrition, cachexia and sarcopenia: the skeleton in the hospital closet 40 years later. Proc Nutr Soc. 2016;75(2):199–211.

    Article  PubMed  Google Scholar 

  80. Kubrak C, Olson K, Jha N, Jensen L, McCargar L, Seikaly H, et al. Nutrition impact symptoms: key determinants of reduced dietary intake, weight loss, and reduced functional capacity of patients with head and neck cancer before treatment. Head Neck. 2009;32(3):290–300.

    Google Scholar 

  81. Arends J, Bachmann P, Baracos V, Barthelemy N, Bertz H, Bozzetti F, et al. ESPEN guidelines on nutrition in cancer patients. Clin Nutr. 2017;36(1):11–48.

    Article  PubMed  Google Scholar 

  82. Rinninella E, Cintoni M, Raoul P, Pozzo C, Strippoli A, Bria E, et al. Effects of nutritional interventions on nutritional status in patients with gastric cancer: a systematic review and meta-analysis of randomized controlled trials. Clin Nutr ESPEN. 2020;38:28–42.

    Article  PubMed  Google Scholar 

  83. Hamaker ME, Oosterlaan F, Van Huis LH, Thielen N, Vondeling A, Van Den Bos F. Nutritional status and interventions for patients with cancer—a systematic review. J Geriatr Oncol. 2021;12(1):6–21.

    Article  PubMed  Google Scholar 

  84. Baldwin C, Spiro A, Ahern R, Emery PW. Oral nutritional interventions in malnourished patients with cancer: a systematic review and meta-analysis. J Natl Cancer Inst. 2012;104(5):371–85.

    Article  PubMed  Google Scholar 

  85. Burden ST, Gibson DJ, Lal S, Hill J, Pilling M, Soop M, et al. Pre-operative oral nutritional supplementation with dietary advice versus dietary advice alone in weight-losing patients with colorectal cancer: single-blind randomized controlled trial. J Cachexia Sarcopenia Muscle. 2017;8(3):437–46.

    Article  PubMed  PubMed Central  Google Scholar 

  86. Kim SH, Lee SM, Jeung HC, Lee IJ, Park JS, Song M, et al. The effect of nutrition intervention with oral nutritional supplements on pancreatic and bile duct cancer patients undergoing chemotherapy. Nutrients. 2019;11(5):1145.

    Article  CAS  PubMed Central  Google Scholar 

  87. van der Werf A, Langius JAE, Beeker A, Ten Tije AJ, Vulink AJ, Haringhuizen A, et al. The effect of nutritional counseling on muscle mass and treatment outcome in patients with metastatic colorectal cancer undergoing chemotherapy: a randomized controlled trial. Clin Nutr. 2020;39(10):3005–13.

    Article  CAS  PubMed  Google Scholar 

  88. Breitkreutz R, Tesdal K, Jentschura D, Haas O, Leweling H, Holm E. Effects of a high-fat diet on body composition in cancer patients receiving chemotherapy: a randomized controlled study. Wien Klin Wochenschr. 2005;117(19–20):685–92.

    Article  CAS  PubMed  Google Scholar 

  89. Grote M, Maihofer C, Weigl M, Davies-Knorr P, Belka C. Progressive resistance training in cachectic head and neck cancer patients undergoing radiotherapy: a randomized controlled pilot feasibility trial. Radiat Oncol. 2018;13(1):215.

    Article  PubMed  PubMed Central  Google Scholar 

  90. Lønbro S, Dalgas U, Primdahl H, Johansen J, Nielsen JL, Aagaard P, et al. Progressive resistance training rebuilds lean body mass in head and neck cancer patients after radiotherapy—results from the randomized DAHANCA 25B trial. Radiother Oncol. 2013;108(2):314–9.

    Article  PubMed  Google Scholar 

  91. Yen CJ, Hung CH, Kao CL, Tsai WM, Chan SH, Cheng HC, et al. Multimodal exercise ameliorates exercise responses and body composition in head and neck cancer patients receiving chemotherapy. Support Care Cancer. 2019;27(12):4687–95.

    Article  PubMed  Google Scholar 

  92. Zhao SG, Alexander NB, Djuric Z, Zhou J, Tao Y, Schipper M, et al. Maintaining physical activity during head and neck cancer treatment: results of a pilot controlled trial. Head Neck. 2016;38(Suppl 1):E1086-1096.

    Article  PubMed  Google Scholar 

  93. Lønbro S, Dalgas U, Primdahl H, Overgaard J, Overgaard K. Feasibility and efficacy of progressive resistance training and dietary supplements in radiotherapy treated head and neck cancer patients—the DAHANCA 25A study. Acta Oncol. 2013;52(2):310–8.

    Article  CAS  PubMed  Google Scholar 

  94. Sandmael JA, Bye A, Solheim TS, Stene GB, Thorsen L, Kaasa S, et al. Feasibility and preliminary effects of resistance training and nutritional supplements during versus after radiotherapy in patients with head and neck cancer: a pilot randomized trial. Cancer. 2017;123(22):4440–8.

    Article  PubMed  Google Scholar 

  95. Edvardsen E, Skjonsberg OH, Holme I, Nordsletten L, Borchsenius F, Anderssen SA. High-intensity training following lung cancer surgery: a randomised controlled trial. Thorax. 2015;70(3):244–50.

    Article  CAS  PubMed  Google Scholar 

  96. Quist M, Langer SW, Lillelund C, Winther L, Laursen JH, Christensen KB et al. Effects of an exercise intervention for patients with advanced inoperable lung cancer undergoing chemotherapy: a randomized clinical trial. Lung Cancer. 2020;145:76–82.

    Article  PubMed  Google Scholar 

  97. Fearon K, Strasser F, Anker SD, Bosaeus I, Bruera E, Fainsinger RL, et al. Definition and classification of cancer cachexia: an international consensus. Lancet Oncol. 2011;12(5):489–95.

    Article  PubMed  Google Scholar 

  98. Anker MS, Holcomb R, Muscaritoli M, von Haehling S, Haverkamp W, Jatoi A, et al. Orphan disease status of cancer cachexia in the USA and in the European Union: a systematic review. J Cachexia Sarcopenia Muscle. 2019;10(1):22–34.

    Article  PubMed  PubMed Central  Google Scholar 

  99. von Haehling S, Anker SD. Prevalence, incidence and clinical impact of cachexia: facts and numbers-update 2014. J Cachexia Sarcopenia Muscle. 2014;5(4):261–3.

    Article  Google Scholar 

  100. Fearon K, Arends J, Baracos V. Understanding the mechanisms and treatment options in cancer cachexia. Nat Rev Clin Oncol. 2013;10(2):90–9.

    Article  CAS  PubMed  Google Scholar 

  101. Purcell SA, Wallengren O, Baracos VE, Lundholm K, Iresjo BM, Chu QSC, et al. Determinants of change in resting energy expenditure in patients with stage III/IV colorectal cancer. Clin Nutr. 2020;39(1):134–40.

    Article  PubMed  Google Scholar 

  102. Cao DX, Wu GH, Zhang B, Quan YJ, Wei J, Jin H, et al. Resting energy expenditure and body composition in patients with newly detected cancer. Clin Nutr. 2010;29(1):72–7.

    Article  PubMed  Google Scholar 

  103. Jouinot A, Vazeille C, Durand JP, Huillard O, Boudou-Rouquette P, Coriat R, et al. Resting energy expenditure in the risk assessment of anticancer treatments. Clin Nutr. 2018;37(2):558–65.

    Article  CAS  PubMed  Google Scholar 

  104. Vazeille C, Jouinot A, Durand JP, Neveux N, Boudou-Rouquette P, Huillard O, et al. Relation between hypermetabolism, cachexia, and survival in cancer patients: a prospective study in 390 cancer patients before initiation of anticancer therapy. Am J Clin Nutr. 2017;105(5):1139–47.

    Article  CAS  PubMed  Google Scholar 

  105. Dijk DPJ, Horstman AMH, Smeets JSJ, Dulk M, Grabsch HI, Dejong CHC, et al. Tumour-specific and organ-specific protein synthesis rates in patients with pancreatic cancer. J Cachexia Sarcopenia Muscle. 2019;10(3):549–56.

    Article  PubMed  PubMed Central  Google Scholar 

  106. Horstman A, Olde Damink S, Schols A, Van Loon L. Is cancer cachexia attributed to impairments in basal or postprandial muscle protein metabolism? Nutrients. 2016;8(8):499.

    Article  CAS  PubMed Central  Google Scholar 

  107. Argiles JM, Lopez-Soriano FJ, Busquets S. Mediators of cachexia in cancer patients. Nutrition. 2019;66:11–5.

    Article  CAS  PubMed  Google Scholar 

  108. Aoyagi T, Terracina KP, Raza A, Matsubara H, Takabe K. Cancer cachexia, mechanism and treatment. World J Gastrointest Oncol. 2015;7:17–29.

    Article  PubMed  PubMed Central  Google Scholar 

  109. Looijaard S, Te Lintel Hekkert ML, Wust RCI, Otten RHJ, Meskers CGM, Maier AB. Pathophysiological mechanisms explaining poor clinical outcome of older cancer patients with low skeletal muscle mass. Acta Physiol (Oxf). 2020;231(1):e13516. https://doi.org/10.1111/apha.13516.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Dolly A, Dumas JF, Servais S. Cancer cachexia and skeletal muscle atrophy in clinical studies: what do we really know? J Cachexia Sarcopenia Muscle. 2020;11(6):1413–28.

    Article  PubMed  PubMed Central  Google Scholar 

  111. Wu J, Huang C, Xiao H, Tang Q, Cai W. Weight loss and resting energy expenditure in male patients with newly diagnosed esophageal cancer. Nutrition. 2013;29(11–12):1310–4.

    Article  PubMed  Google Scholar 

  112. Roeland EJ, Bohlke K, Baracos VE, Bruera E, Del Fabbro E, Dixon S, et al. Management of cancer cachexia: ASCO guideline. J Clin Oncol. 2020;38(21):2438–53.

    Article  CAS  PubMed  Google Scholar 

  113. de van der Schueren MAE, Laviano A, Blanchard H, Jourdan M, Arends J, Baracos VE. Systematic review and meta-analysis of the evidence for oral nutritional intervention on nutritional and clinical outcomes during chemo(radio)therapy: current evidence and guidance for design of future trials. Ann Oncol. 2018;29(5):1141–53.

    Article  Google Scholar 

  114. Zanetti M, Gortan Cappellari G, Barazzoni R, Sanson G. The impact of protein supplementation targeted at improving muscle mass on strength in cancer patients: a scoping review. Nutrients. 2020;12(7):2099.

    Article  CAS  PubMed Central  Google Scholar 

  115. Balstad TR, Solheim TS, Strasser F, Kaasa S, Bye A. Dietary treatment of weight loss in patients with advanced cancer and cachexia: a systematic literature review. Crit Rev Oncol Hematol. 2014;91(2):210–21.

    Article  PubMed  Google Scholar 

  116. Niels T, Tomanek A, Freitag N, Schumann M. Can exercise counteract cancer cachexia? A systematic literature review and meta-analysis. Integr Cancer Ther. 2020;19:153473542094041.

    Article  Google Scholar 

  117. Argilés JM, Busquets S, López-Soriano FJ, Costelli P, Penna F. Are there any benefits of exercise training in cancer cachexia? J Cachexia Sarcopenia Muscle. 2012;3(2):73–6.

    Article  PubMed  PubMed Central  Google Scholar 

  118. Wiskemann J, Clauss D, Tjaden C, Hackert T, Schneider L, Ulrich CM, et al. Progressive resistance training to impact physical fitness and body weight in pancreatic cancer patients: a randomized controlled trial. Pancreas. 2019;48(2):257–66.

    Article  PubMed  Google Scholar 

  119. Solheim TS, Laird BJA, Balstad TR, Stene GB, Bye A, Johns N, et al. A randomized phase II feasibility trial of a multimodal intervention for the management of cachexia in lung and pancreatic cancer. J Cachexia Sarcopenia Muscle. 2017;8(5):778–88.

    Article  PubMed  PubMed Central  Google Scholar 

  120. Solheim TS, Laird BJA, Balstad TR, Bye A, Stene G, Baracos V, et al. Cancer cachexia: rationale for the MENAC (Multimodal-Exercise, Nutrition and Anti-inflammatory medication for Cachexia) trial. BMJ Support Palliat Care. 2018;8(3):258–65.

    Article  PubMed  Google Scholar 

  121. Aleixo GFP, Shachar SS, Nyrop KA, Muss HB, Battaglini CL, Williams GR. Bioelectrical impedance analysis for the assessment of sarcopenia in patients with cancer: a systematic review. Oncologist. 2020;25(2):170–82.

    Article  PubMed  Google Scholar 

  122. Sheean P, Gonzalez MC, Prado CM, McKeever L, Hall AM, Braunschweig CA. American Society for Parenteral and Enteral Nutrition Clinical Guidelines: the validity of body composition assessment in clinical populations. JPEN J Parenter Enteral Nutr. 2020;44(1):12–43.

    Article  PubMed  Google Scholar 

  123. Yip C, Dinkel C, Mahajan A, Siddique M, Cook GJR, Goh V. Imaging body composition in cancer patients: visceral obesity, sarcopenia and sarcopenic obesity may impact on clinical outcome. Insights Imaging. 2015;6(4):489–97.

    Article  PubMed  PubMed Central  Google Scholar 

  124. Lee H, Troschel FM, Tajmir S, Fuchs G, Mario J, Fintelmann FJ, et al. Pixel-level deep segmentation: artificial intelligence quantifies muscle on computed tomography for body morphometric analysis. J Digit Imaging. 2017;30(4):487–98.

    Article  PubMed  PubMed Central  Google Scholar 

  125. Blake GM, Naeem M, Boutros M. Comparison of effective dose to children and adults from dual X-ray absorptiometry examinations. Bone. 2006;38(6):935–42.

    Article  PubMed  Google Scholar 

  126. Mettler FA Jr, Huda W, Yoshizumi TT, Mahesh M. Effective doses in radiology and diagnostic nuclear medicine: a catalog. Radiology. 2008;248(1):254–63.

    Article  PubMed  Google Scholar 

  127. Haun CT, Vann CG, Roberts BM, Vigotsky AD, Schoenfeld BJ, Roberts MD. A critical evaluation of the biological construct skeletal muscle hypertrophy: size matters but so does the measurement. Front Physiol. 2019;10:247.

    Article  PubMed  PubMed Central  Google Scholar 

  128. Kasper AM, Langan-Evans C, Hudson JF, Brownlee TE, Harper LD, Naughton RJ, et al. Come back skinfolds, all is forgiven: a narrative review of the efficacy of common body composition methods in applied sports practice. Nutrients. 2021;13(4):1075.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Nana A, Slater GJ, Hopkins WG, Burke LM. Effects of daily activities on dual-energy X-ray absorptiometry measurements of body composition in active people. Med Sci Sports Exerc. 2012;44(1):180–9.

    Article  PubMed  Google Scholar 

  130. Nana A, Slater GJ, Hopkins WG, Burke LM. Effects of exercise sessions on DXA measurements of body composition in active people. Med Sci Sports Exerc. 2013;45(1):178–85.

    Article  PubMed  Google Scholar 

  131. Nana A, Slater GJ, Stewart AD, Burke LM. Methodology review: using dual-energy X-ray absorptiometry (DXA) for the assessment of body composition in athletes and active people. Int J Sport Nutr Exerc Metab. 2015;25(2):198–215.

    Article  PubMed  Google Scholar 

  132. Shepherd JA, Ng BK, Sommer MJ, Heymsfield SB. Body composition by DXA. Bone. 2017;104:101–5.

    Article  PubMed  PubMed Central  Google Scholar 

  133. Wells JC, Fewtrell MS. Measuring body composition. Arch Dis Child. 2006;91(7):612–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Stringer HJ, Wilson D. The role of ultrasound as a diagnostic tool for sarcopenia. J Frailty Aging. 2018;7(4):258–61.

    CAS  PubMed  PubMed Central  Google Scholar 

  135. Nijholt W, Scafoglieri A, Jager-Wittenaar H, Hobbelen JSM, Van Der Schans CP. The reliability and validity of ultrasound to quantify muscles in older adults: a systematic review. J Cachexia Sarcopenia Muscle. 2017;8(5):702–12.

    Article  PubMed  PubMed Central  Google Scholar 

  136. Tillquist M, Kutsogiannis DJ, Wischmeyer PE, Kummerlen C, Leung R, Stollery D, et al. Bedside ultrasound is a practical and reliable measurement tool for assessing quadriceps muscle layer thickness. JPEN J Parenter Enteral Nutr. 2014;38(7):886–90.

    Article  PubMed  Google Scholar 

  137. Almada-Correia I, Neves PM, Mäkitie A, Ravasco P. Body composition evaluation in head and neck cancer patients: a review. Front Oncol. 2019;9:1112.

    Article  PubMed  PubMed Central  Google Scholar 

  138. Cotogni P, Monge T, Fadda M, De Francesco A. Bioelectrical impedance analysis for monitoring cancer patients receiving chemotherapy and home parenteral nutrition. BMC Cancer. 2018;18(1):990.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Barreira TV, Tseh W. The effects of acute water ingestion on body composition analyses via dual-energy X-ray absorptiometry. Clin Nutr. 2020;39(12):3836–8.

    Article  CAS  PubMed  Google Scholar 

  140. Hui D, Dev R, Bruera E. The last days of life: symptom burden and impact on nutrition and hydration in cancer patients. Curr Opin Support Palliat Care. 2015;9(4):346–54.

    Article  PubMed  PubMed Central  Google Scholar 

  141. Price KA. Hydration in cancer patients. Curr Opin Support Palliat Care. 2010;4(4):276–80.

    Article  PubMed  Google Scholar 

  142. Clark RV, Walker AC, Miller RR, O’Connor-Semmes RL, Ravussin E, Cefalu WT. Creatine (methyl-d3) dilution in urine for estimation of total body skeletal muscle mass: accuracy and variability vs. MRI and DXA. J Appl Physiol (1985). 2018;124(1):1–9.

    Article  CAS  Google Scholar 

  143. Stimpson SA, Leonard MS, Clifton LG, Poole JC, Turner SM, Shearer TW, et al. Longitudinal changes in total body creatine pool size and skeletal muscle mass using the D 3-creatine dilution method. J Cachexia Sarcopenia Muscle. 2013;4(3):217–23.

    Article  PubMed Central  Google Scholar 

  144. Evans WJ, Scottoline B, Imam F, Hellerstein M, Garton K, Czerwieniec G, et al. D3-creatine dilution for the noninvasive measurement of skeletal muscle mass in premature infants. Pediatr Res. 2021;89(6):1508–14.

    Article  CAS  PubMed  Google Scholar 

  145. Cawthon PM, Orwoll ES, Peters KE, Ensrud KE, Cauley JA, Kado DM, et al. Strong relation between muscle mass determined by D3-creatine dilution, physical performance, and incidence of falls and mobility limitations in a prospective cohort of older men. J Gerontol A Biol Sci Med Sci. 2019;74(6):844–52.

    Article  PubMed  Google Scholar 

  146. Cawthon PM, Blackwell T, Cummings SR, Orwoll ES, Duchowny KA, Kado DM, et al. Muscle mass assessed by the D3-creatine dilution method and incident self-reported disability and mortality in a prospective observational study of community-dwelling older men. J Gerontol A Biol Sci Med Sci. 2021;76(1):123–30.

    Article  CAS  PubMed  Google Scholar 

  147. Nana A, Slater GJ, Hopkins WG, Halson SL, Martin DT, West NP, et al. Importance of standardized DXA protocol for assessing physique changes in athletes. Int J Sport Nutr Exerc Metab. 2016;26(3):259–67.

    Article  PubMed  Google Scholar 

  148. Schag CC, Heinrich RL, Ganz PA. Karnofsky performance status revisited: reliability, validity, and guidelines. J Clin Oncol. 1984;2(3):187–93.

    Article  CAS  PubMed  Google Scholar 

  149. Aaronson NK, Ahmedzai S, Bergman B, Bullinger M, Cull A, Duez NJ, et al. The European Organization for Research and Treatment of Cancer QLQ-C30: a quality-of-life instrument for use in international clinical trials in oncology. J Natl Cancer Inst. 1993;85(5):365–76.

    Article  CAS  PubMed  Google Scholar 

  150. Oken MM, Creech RH, Tormey DC, Horton J, Davis TE, McFadden ET, et al. Toxicity and response criteria of the Eastern Cooperative Oncology Group. Am J Clin Oncol. 1982;5(6):649–56.

    Article  CAS  PubMed  Google Scholar 

  151. Craig CL, Marshall AL, Sjostrom M, Bauman AE, Booth ML, Ainsworth BE, et al. International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc. 2003;35(8):1381–95.

    Article  PubMed  Google Scholar 

  152. Godin G. The Godin-Shephard leisure-time physical activity questionnaire. Health Fit J Canada. 2011;4(1):18–22.

    Google Scholar 

  153. Troiano RP. A timely meeting: objective measurement of physical activity. Med Sci Sports Exerc. 2005;37(11 Suppl):S487-489.

    Article  PubMed  Google Scholar 

  154. Beaudart C, Rolland Y, Cruz-Jentoft AJ, Bauer JM, Sieber C, Cooper C, et al. Assessment of Muscle Function and Physical Performance in Daily Clinical Practice: A position paper endorsed by the European Society for Clinical and Economic Aspects of Osteoporosis, Osteoarthritis and Musculoskeletal Diseases (ESCEO). Calcif Tissue Int. 2019;105(1):1–14.

    Article  CAS  PubMed  Google Scholar 

  155. Den Ouden MEM, Schuurmans MJ, Arts IEMA, Van Der Schouw YT. Physical performance characteristics related to disability in older persons: a systematic review. Maturitas. 2011;69(3):208–19.

    Article  Google Scholar 

  156. Wang C-Y, Chen L-Y. Grip strength in older adults: test-retest reliability and cutoff for subjective weakness of using the hands in heavy tasks. Arch Phys Med Rehabil. 2010;91(11):1747–51.

    Article  PubMed  Google Scholar 

  157. Liguori G, American College of Sports Medicine. ACSM's guidelines for exercise testing and prescription: Lippincott: Williams & Wilkins; 2020.

  158. Dos Santos WDN, Siqueira GDJ, Martins WR, Vieira A, Schincaglia RM, Gentil P, et al. Reliability and agreement of the 10-repetition maximum test in breast cancer survivors. Front Oncol. 2019;9:918.

    Article  PubMed  PubMed Central  Google Scholar 

  159. Isenring E, Elia M. Which screening method is appropriate for older cancer patients at risk for malnutrition? Nutrition. 2015;31(4):594–7.

    Article  PubMed  Google Scholar 

  160. da Silva FJ, de Mello PD, de Mello ED. Subjective global assessment of nutritional status—a systematic review of the literature. Clin Nutr. 2015;34(5):785–92.

    Article  Google Scholar 

  161. Bauer J, Capra S, Ferguson M. Use of the scored Patient-Generated Subjective Global Assessment (PG-SGA) as a nutrition assessment tool in patients with cancer. Eur J Clin Nutr. 2002;56(8):779–85.

    Article  CAS  PubMed  Google Scholar 

  162. Read JA, Crockett N, Volker DH, MacLennan P, Boris Choy ST, Beale P, et al. Nutritional Assessment in Cancer: Comparing the Mini-Nutritional Assessment (MNA) with the Scored Patient-Generated Subjective Global Assessment (PGSGA). Nutr Cancer. 2005;53(1):51–6.

  163. Clifford BK, Mizrahi D, Sandler CX, Barry BK, Simar D, Wakefield CE, et al. Barriers and facilitators of exercise experienced by cancer survivors: a mixed methods systematic review. Support Care Cancer. 2018;26(3):685–700.

    Article  PubMed  Google Scholar 

  164. Mikkelsen MK, Nielsen DL, Vinther A, Lund CM, Jarden M. Attitudes towards physical activity and exercise in older patients with advanced cancer during oncological treatment—a qualitative interview study. Eur J Oncol Nurs. 2019;41:16–23.

    Article  PubMed  Google Scholar 

  165. Kirkham AA, Bonsignore A, Bland KA, McKenzie DC, Gelmon KA, Van Patten CL, et al. Exercise prescription and adherence for breast cancer: one size does not FITT all. Med Sci Sports Exerc. 2018;50(2):177–86.

    Article  PubMed  Google Scholar 

  166. Fairman CM, Nilsen TS, Newton RU, Taaffe DR, Spry N, Joseph D, et al. Reporting of resistance training dose, adherence, and tolerance in exercise oncology. Med Sci Sports Exerc. 2020;52(2):315–22.

    Article  PubMed  Google Scholar 

  167. Scott JM, Iyengar NM, Nilsen TS, Michalski M, Thomas SM, Herndon J 2nd, et al. Feasibility, safety, and efficacy of aerobic training in pretreated patients with metastatic breast cancer: a randomized controlled trial. Cancer. 2018;124(12):2552–60.

    Article  CAS  PubMed  Google Scholar 

  168. Zhou T, Yang K, Thapa S, Liu H, Wang B, Yu S. Differences in symptom burden among cancer patients with different stages of cachexia. J Pain Symptom Manag. 2017;53(5):919–26.

    Article  Google Scholar 

  169. Blum D, Stene GB, Solheim TS, Fayers P, Hjermstad MJ, Baracos VE, et al. Validation of the Consensus-Definition for Cancer Cachexia and evaluation of a classification model-a study based on data from an international multicentre project (EPCRC-CSA). Ann Oncol. 2014;25(8):1635–42.

    Article  CAS  PubMed  Google Scholar 

  170. Strasser F. Diagnostic criteria of cachexia and their assessment: decreased muscle strength and fatigue. Curr Opin Clin Nutr Metab Care. 2008;11(4):417–21.

    Article  PubMed  Google Scholar 

  171. Kirkova J, Davis MP, Walsh D, Tiernan E, O’Leary N, LeGrand SB, et al. Cancer symptom assessment instruments: a systematic review. J Clin Oncol. 2006;24(9):1459–73.

    Article  PubMed  Google Scholar 

  172. Liao C-D, Tsauo J-Y, Wu Y-T, Cheng C-P, Chen H-C, Huang Y-C, et al. Effects of protein supplementation combined with resistance exercise on body composition and physical function in older adults: a systematic review and meta-analysis. Am J Clin Nutr. 2017;106(4):1078–91.

    Article  CAS  PubMed  Google Scholar 

  173. Capitão C, Coutinho D, Neves PM, Capelas ML, Pimenta NM, Santos T, et al. Protein intake and muscle mass maintenance in patients with cancer types with high prevalence of sarcopenia: a systematic review. Support Care Cancer. 2021. https://doi.org/10.1007/s00520-021-06633-8.

    Article  PubMed  Google Scholar 

  174. Deutz NEP, Bauer JM, Barazzoni R, Biolo G, Boirie Y, Bosy-Westphal A, et al. Protein intake and exercise for optimal muscle function with aging: Recommendations from the ESPEN Expert Group. Clin Nutr. 2014;33(6):929–36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Hanson ED, Nelson AR, West DW, Violet JA, O’Keefe L, Phillips SM, et al. Attenuation of resting but not load-mediated protein synthesis in prostate cancer patients on androgen deprivation. J Clin Endocrinol Metab. 2017;102(3):1076–83.

    PubMed  Google Scholar 

  176. Van Dijk DPJ, Van De Poll MCG, Moses AGW, Preston T, Olde Damink SWM, Rensen SS, et al. Effects of oral meal feeding on whole body protein breakdown and protein synthesis in cachectic pancreatic cancer patients. J Cachexia Sarcopenia Muscle. 2015;6(3):212–21.

    Article  PubMed  PubMed Central  Google Scholar 

  177. Williams JP, Phillips BE, Smith K, Atherton PJ, Rankin D, Selby AL, et al. Effect of tumor burden and subsequent surgical resection on skeletal muscle mass and protein turnover in colorectal cancer patients. Am J Clin Nutr. 2012;96(5):1064–70.

    Article  CAS  PubMed  Google Scholar 

  178. Haran PH, Rivas DA, Fielding RA. Role and potential mechanisms of anabolic resistance in sarcopenia. J Cachexia Sarcopenia Muscle. 2012;3(3):157–62.

    Article  PubMed  PubMed Central  Google Scholar 

  179. Moore DR, Churchward-Venne TA, Witard O, Breen L, Burd NA, Tipton KD, et al. Protein ingestion to stimulate myofibrillar protein synthesis requires greater relative protein intakes in healthy older versus younger men. J Gerontol A Biol Sci Med Sci. 2015;70(1):57–62.

    Article  CAS  PubMed  Google Scholar 

  180. Yang Y, Breen L, Burd NA, Hector AJ, Churchward-Venne TA, Josse AR, et al. Resistance exercise enhances myofibrillar protein synthesis with graded intakes of whey protein in older men. Br J Nutr. 2012;108(10):1780–8.

    Article  CAS  PubMed  Google Scholar 

  181. Pennings B, Groen B, de Lange A, Gijsen AP, Zorenc AH, Senden JM, et al. Amino acid absorption and subsequent muscle protein accretion following graded intakes of whey protein in elderly men. Am J Physiol Endocrinol Metab. 2012;302(8):E992-999.

    Article  CAS  PubMed  Google Scholar 

  182. Antoun S, Raynard B. Muscle protein anabolism in advanced cancer patients: response to protein and amino acids support, and to physical activity. Ann Oncol. 2018; 29(suppl_2):ii10–17.

  183. Dijxhoorn DN, van den Berg MGA, Kievit W, Korzilius J, Drenth JPH, Wanten GJA. A novel in-hospital meal service improves protein and energy intake. Clin Nutr. 2017;37(6 Pt A):2238–45.

  184. Stelten S, Dekker IM, Ronday EM, Thijs A, Boelsma E, Peppelenbos HW, et al. Protein-enriched “regular products” and their effect on protein intake in acute hospitalized older adults; a randomized controlled trial. Clin Nutr. 2015;34(3):409–14.

    Article  CAS  PubMed  Google Scholar 

  185. Beelen J, Vasse E, Janssen N, Janse A, de Roos NM, de Groot L. Protein-enriched familiar foods and drinks improve protein intake of hospitalized older patients: a randomized controlled trial. Clin Nutr. 2017;37(4):1186–92.

    Article  CAS  PubMed  Google Scholar 

  186. Bourdel-Marchasson I, Barateau M, Rondeau V, Dequae-Merchadou L, Salles-Montaudon N, Emeriau JP, et al. A multi-center trial of the effects of oral nutritional supplementation in critically ill older inpatients. GAGE Group. Groupe Aquitain Geriatrique d’Evaluation. Nutrition. 2000;16(1):1–5.

    Article  CAS  PubMed  Google Scholar 

  187. Cawood AL, Elia M, Stratton RJ. Systematic review and meta-analysis of the effects of high protein oral nutritional supplements. Ageing Res Rev. 2012;11(2):278–96.

    Article  CAS  PubMed  Google Scholar 

  188. Milne AC, Avenell A, Potter J. Meta-analysis: protein and energy supplementation in older people. Ann Intern Med. 2006;144(1):37–48.

    Article  CAS  PubMed  Google Scholar 

  189. Kumar V, Atherton P, Smith K, Rennie MJ. Human muscle protein synthesis and breakdown during and after exercise. J Appl Physiol (1985). 2009;106(6):2026–39.

    Article  CAS  Google Scholar 

  190. Phillips SM, Tipton KD, Aarsland A, Wolf SE, Wolfe RR. Mixed muscle protein synthesis and breakdown after resistance exercise in humans. Am J Physiol. 1997;273(1 Pt 1):E99-107.

    CAS  PubMed  Google Scholar 

  191. Madzima TA, Ormsbee MJ, Schleicher EA, Moffatt RJ, Panton LB. Effects of resistance training and protein supplementation in breast cancer survivors. Med Sci Sports Exerc. 2017;49(7):1283–92.

    Article  CAS  PubMed  Google Scholar 

  192. Dawson JK, Dorff TB, Todd Schroeder E, Lane CJ, Gross ME, Dieli-Conwright CM. Impact of resistance training on body composition and metabolic syndrome variables during androgen deprivation therapy for prostate cancer: a pilot randomized controlled trial. BMC Cancer. 2018;18(1):368.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  193. Fairman CM, Hyde PN, Focht BC. Resistance training interventions across the cancer control continuum: a systematic review of the implementation of resistance training principles. Br J Sports Med. 2017;51(8):677–85.

    Article  CAS  PubMed  Google Scholar 

  194. Bland KA, Neil-Sztramko SE, Zadravec K, Medysky ME, Kong J, Winters-Stone KM, et al. Attention to principles of exercise training: an updated systematic review of randomized controlled trials in cancers other than breast and prostate. BMC Cancer. 2021;21(1):1179.

    Article  PubMed  PubMed Central  Google Scholar 

  195. Sweegers MG, Altenburg TM, Brug J, May AM, van Vulpen JK, Aaronson NK, et al. Effects and moderators of exercise on muscle strength, muscle function and aerobic fitness in patients with cancer: a meta-analysis of individual patient data. Br J Sports Med. 2018;53(13):812.

    Article  PubMed  Google Scholar 

  196. Bland KA, Bigaran A, Campbell KL, Trevaskis M, Zopf EM. Exercising in isolation? The role of telehealth in exercise oncology during the COVID-19 pandemic and beyond. Phys Ther. 2020;100(10):1713–6.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Mary MacKillop Institute for Health Research, Australian Catholic University, Melbourne, VIC, Australia

    Kelcey A. Bland, Luc J. C. van Loon & Eva M. Zopf

  2. The Szalmuk Family Department of Medical Oncology, Cabrini Cancer Institute, Cabrini Health, Melbourne, VIC, Australia

    Kelcey A. Bland & Eva M. Zopf

  3. Intensive Care Unit, Royal Adelaide Hospital, Adelaide, SA, Australia

    Imre W. K. Kouw

  4. Centre of Research Excellence in Translating Nutritional Science To Good Health, The University of Adelaide, Adelaide, SA, Australia

    Imre W. K. Kouw

  5. Adelaide Medical School, Faculty of Health and Medical Sciences, The University of Adelaide, Adelaide, SA, Australia

    Imre W. K. Kouw

  6. Department of Human Biology, NUTRIM School for Nutrition and Translational Research in Metabolism, Maastricht University, Maastricht, The Netherlands

    Luc J. C. van Loon

  7. Exercise Science Department, Arnold School of Public Health, University of South Carolina, 921 Assembly Street, PHRC 220, Columbia, SC, 29208, USA

    Ciaran M. Fairman

Authors
  1. Kelcey A. Bland
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Imre W. K. Kouw
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Luc J. C. van Loon
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eva M. Zopf
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ciaran M. Fairman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ciaran M. Fairman.

Ethics declarations

Funding

No sources of funding were used to assist in the preparation of this article.

Conflict of interest

Luc van Loon has received research grants, consulting fees, and speaking honoraria, or a combination of these, from Kenniscentrum Suiker & Voeding and PepsiCo. Kelcey Bland, Imre Kouw, Eva Zopf, and Ciaran Fairman have no conflicts of interest of potential relevance to the content of this review.

Availability of data and material

Not applicable.

Code availability

Not applicable.

Author contributions

Kelcey Bland and Ciaran Fairman conceived the manuscript idea and wrote the first draft of the manuscript. All authors critically revised the manuscript and contributed intellectual content. All authors read and approved the final manuscript.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bland, K.A., Kouw, I.W.K., van Loon, L.J.C. et al. Exercise-Based Interventions to Counteract Skeletal Muscle Mass Loss in People with Cancer: Can We Overcome the Odds?. Sports Med 52, 1009–1027 (2022). https://doi.org/10.1007/s40279-021-01638-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40279-021-01638-z

Search

Navigation