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Rofo 2024; 196(07): 699-706
DOI: 10.1055/a-2213-2320
Review

Prognostic role of the skeletal musculature in oncology: significance, coherences and clinical implications

Article in several languages: English | deutsch
Alexey Surov
1   Department of Radiology, Neuroradiology and Nuclear Medicine, Johannes Wesling Medical Center, Ruhr University Bochum, Germany
,
Andreas Wienke
2   Institute of Medical Epidemiology, Biostatistics, and Informatics, Martin Luther University Halle Wittenberg, Halle, Germany
,
Ralf Gutzmer
3   Department of Dermatology, Johannes Wesling Medical Center, Ruhr University Bochum, Germany
,
Jan Borggrefe
1   Department of Radiology, Neuroradiology and Nuclear Medicine, Johannes Wesling Medical Center, Ruhr University Bochum, Germany
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Abstract

Background

Sarcopenia is defined as a loss of muscle mass and strength as well as decreased physical performance.

Method

The present study provides a systematic overview of the current literature in regard to the prognostic role of sarcopenia in oncology.

Conclusion

In oncologic patients, sarcopenia occurs in 39.6 % of cases in a curative setting and in 49.2 % in a palliative setting. Sarcopenia is associated with dose-limiting toxicity. Furthermore, sarcopenia is associated with the occurrence of postoperative complications. Also, reduced muscle mass limits overall survival in most tumors both in a curative and a palliative setting. Therefore, analysis of the skeletal musculature on staging CT should be implemented in the clinical routine in oncology.

Key Points

  • In oncologic patients, the prevalence of sarcopenia is 39.6 % in a curative setting and 49.2 % in a palliative setting.

  • Sarcopenia is associated with dose-limiting toxicity and treatment response.

  • Sarcopenia predicts overall survival in oncologic patients.

Citation Format

  • Surov A, Wienke A, Gutzmer R et al. Prognostic role of the skeletal musculature in oncology: significance, coherences and clinical implications. Fortschr Röntgenstr 2024; 196: 699 – 706

Key words

sarcopenia - cancer - survival


Publication History

Received: 10 July 2023

Accepted: 02 November 2023

Article published online:
22 December 2023

© 2023. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Cruz-Jentoft AJ, Bahat G, Bauer J. et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 2019; 48: 16-31
    CrossrefPubMedSearch in Google Scholar
  • 2 Ali S, Garcia JM. Sarcopenia, Cachexia and Aging: Diagnosis, Mechanisms and Therapeutic Options – A Mini-Review. Gerontology 2014; 60: 294-230
    CrossrefPubMedSearch in Google Scholar
  • 3 Rier HN, Jager A, Sleijfer S. et al. The Prevalence and Prognostic Value of Low Muscle Mass in Cancer Patients: A Review of the Literature. Oncologist 2016; 21 (11) 1396-1409
    CrossrefPubMedSearch in Google Scholar
  • 4 Buettner S, Wagner D, Kim Y. et al. Inclusion of Sarcopenia Outperforms the Modified Frailty Index in Predicting 1-Year Mortality among 1326 Patients Undergoing Gastrointestinal Surgery for a Malignant Indication. J Am Coll Surg 2016; 222: 397-407
    CrossrefPubMedSearch in Google Scholar
  • 5 Simonsen C, de Heer P, Bjerre ED. et al. Sarcopenia and Postoperative Complication Risk in Gastrointestinal Surgical Oncology: A Meta-analysis. Ann Surg 2018; 268 (01) 58-69
    CrossrefPubMedSearch in Google Scholar
  • 6 Surov A, Pech M, Gessner D. et al. Low skeletal muscle mass is a predictor of treatment related toxicity in oncologic patients. A meta-analysis. Clin Nutr 2021; 40 (10) 5298-5310
    CrossrefPubMedSearch in Google Scholar
  • 7 Prado CM, Lieffers JR, McCargar LJ. 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 (07) 629-635
    CrossrefPubMedSearch in Google Scholar
  • 8 Shachar SS, Williams GR, Muss HB. et al. Prognostic value of sarcopenia in adults with solid tumours: A meta-analysis and systematic review. Eur J Cancer 2016; 57: 58-67
    CrossrefPubMedSearch in Google Scholar
  • 9 Martin L, Birdsell L, Macdonald N. 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) 1539-1547
    CrossrefPubMedSearch in Google Scholar
  • 10 Baracos VE, Reiman T, Mourtzakis M. et al. Body composition in patients with non-small cell lung cancer: A contemporary view of cancer cachexia with the use of computed tomography image analysis. Am J Clin Nutr 2010; 91: 1133S-1137S
    CrossrefPubMedSearch in Google Scholar
  • 11 van Vledder MG, Levolger S, Ayez N. et al. Body composition and outcome in patients undergoing resection of colorectal liver metastases. Br J Surg 2012; 99: 550-557
    CrossrefPubMedSearch in Google Scholar
  • 12 Camus V, Lanic H, Kraut J. et al. Prognostic impact of fat tissue loss and cachexia assessed by computed tomography scan in elderly patients with diffuse large B-cell lymphoma treated with immunochemotherapy. Eur J Haematol 2014; 93: 9-18
    CrossrefPubMedSearch in Google Scholar
  • 13 Surov A, Wienke A. Prevalence of sarcopenia in patients with solid tumors: A meta-analysis based on 81,814 patients. JPEN J Parenter Enteral Nutr 2022; 46 (08) 1761-1768
    CrossrefPubMedSearch in Google Scholar
  • 14 Surov A, Strobel A, Borggrefe J. et al. Low skeletal muscle mass predicts treatment response in oncology: a meta-analysis. Eur Radiol 2023; 33 (09) 6426-6437
    CrossrefPubMedSearch in Google Scholar
  • 15 Surov A, Wienke A, Gutzmer R. et al. Time to include sarcopenia into the oncological routine. Eur J Cancer 2023; 190: 112939
    CrossrefPubMedSearch in Google Scholar
  • 16 Williams GR, Dunne RF, Giri S. et al. Sarcopenia in the Older Adult With Cancer. J Clin Oncol 2021; 39 (19) 2068-2078
    CrossrefPubMedSearch in Google Scholar
  • 17 Hilmi M, Jouinot A, Burns R. et al. Body composition and sarcopenia: The next-generation of personalized oncology and pharmacology?. Pharmacol Ther 2019; 196: 135-159
    CrossrefPubMedSearch in Google Scholar
  • 18 van der Meij BS, Teleni L, McCarthy AL. et al. Cancer cachexia: an overview of diagnostic criteria and therapeutic approaches for the accredited practicing dietitian. J Hum Nutr Diet 2021; 34 (01) 243-254
    CrossrefPubMedSearch in Google Scholar
  • 19 Cohen S, Nathan JA, Goldberg AL. Muscle wasting in disease: molecular mechanisms and promising therapies. Nat Rev Drug Discov 2015; 14 (01) 58-74
    CrossrefPubMedSearch in Google Scholar
  • 20 Armstrong VS, Fitzgerald LW, Bathe OF. Armstrong Cancer-Associated Muscle Wasting-Candidate Mechanisms and Molecular Pathways. Int J Mol Sci 2020; 21 (23) 9268
    CrossrefPubMedSearch in Google Scholar
  • 21 Sakai H, Asami M, Naito H. et al. Exogenous insulin-like growth factor 1 attenuates cisplatin-induced muscle atrophy in mice. J Cachexia Sarcopenia Muscle 2021; 16
    CrossrefPubMedSearch in Google Scholar
  • 22 Prado CM, Maia YL, Ormsbee M. et al. Assessment of nutritional status in cancer-the relationship between body composition and pharmacokinetics. Anticancer Agents Med Chem 2013; 13 (08) 1197-1203
    CrossrefPubMedSearch in Google Scholar
  • 23 Hopkins JJ, Sawyer MB. A review of body composition and pharmacokinetics in oncology. Expert Rev Clin Pharmacol 2017; 10 (09) 947-956
    CrossrefPubMedSearch in Google Scholar
  • 24 Hopkins JJ, Sawyer MB. Interactions of lean soft-tissue and chemotherapy toxicities in patients receiving anti-cancer treatments. Cancer Chemother Pharmacol 2018; 82 (01) 1-29
    CrossrefPubMedSearch in Google Scholar
  • 25 Prado CMM, Baracos VE, McCargar LJ. et al. Body composition as an independent determinant of 5-fluorouracil-based chemotherapy toxicity. Clinical Cancer Research 2007; 13 (11) 3264-3268
    CrossrefPubMedSearch in Google Scholar
  • 26 Mourtzakis M, Prado CM, Lieffers JR. et al. A practical and precise approach to quantification of body composition in cancer patients using computed tomography images acquired during routine care. Appl Physiol Nutr Metab 2008; 33: 997-1006
    CrossrefPubMedSearch in Google Scholar
  • 27 Sjøblom B, Grønberg BH, Benth JŠ. et al. Low muscle mass is associated with chemotherapy-induced haematological toxicity in advanced non-small cell lung cancer. Lung Cancer 2015; 90 (01) 85-91
    CrossrefPubMedSearch in Google Scholar
  • 28 Prado CM, Baracos VE, McCargar LJ. 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 (08) 2920-2926
    CrossrefPubMedSearch in Google Scholar
  • 29 Mir O, Coriat R, Blanchet B. et al. Sarcopenia predicts early dose-limiting toxicities and pharmacokinetics of sorafenib in patients with hepatocellular carcinoma. PLoS One 2012; 7 (05) e37563
    CrossrefPubMedSearch in Google Scholar
  • 30 Massicotte MH, Borget I, Broutin S. et al. Body composition variation and impact of low skeletal muscle mass in patients with advanced medullary thyroid carcinoma treated with vandetanib: results from a placebo-controlled study. J Clin Endocrinol Metab 2013; 98 (06) 2401-2408
    CrossrefPubMedSearch in Google Scholar
  • 31 Williams GR, Deal AM, Shachar SS. et al. The impact of skeletal muscle on the pharmacokinetics and toxicity of 5-fluorouracil in colorectal cancer. Cancer Chemother Pharmacol 2018; 81 (02) 413-417
    CrossrefPubMedSearch in Google Scholar
  • 32 Cespedes Feliciano EM, Chen WY, Lee V. et al. Body Composition, Adherence to Anthracycline and Taxane-Based Chemotherapy, and Survival After Nonmetastatic Breast Cancer. JAMA Oncol 2020; 6 (02) 264-270
    CrossrefPubMedSearch in Google Scholar
  • 33 Cvan Trobec K, Kerec Kos M, Trontelj J. et al. Influence of cancer cachexia on drug liver metabolism and renal elimination in rats. J Cachexia Sarcopenia Muscle 2015; 6 (01) 45-52
    CrossrefPubMedSearch in Google Scholar
  • 34 Kitano Y, Yamashita YI, Saito Y. et al. Sarcopenia Affects Systemic and Local Immune System and Impacts Postoperative Outcome in Patients with Extrahepatic Cholangiocarcinoma. World J Surg 2019; 43 (09) 2271-2280
    CrossrefPubMedSearch in Google Scholar
  • 35 Afzali AM, Müntefering T, Wiendl H. et al. Skeletal muscle cells actively shape (auto)immune responses. Autoimmun Rev 2018; 17 (05) 518-529
    CrossrefPubMedSearch in Google Scholar
  • 36 Nelke C, Dziewas R, Minnerup J. et al. Skeletal muscle as potential central link between sarcopenia and immune senescence. EBioMedicine 2019; 49: 381-388
    CrossrefPubMedSearch in Google Scholar
  • 37 Conlon KC, Lugli E, Welles HC. et al. Redistribution, hyperproliferation, activation of natural killer cells and CD8 T cells, and cytokine production during first-in-human clinical trial of recombinant human interleukin-15 in patients with cancer. J Clin Oncol 2015; 33: 74-82
    CrossrefPubMedSearch in Google Scholar
  • 38 Dubois SP, Miljkovic MD, Fleisher TA. et al. Short-course IL-15 given as a continuous infusion led to a massive expansion of effective NK cells: implications for combination therapy with antitumor antibodies. J Immunother Cancer 2021; 9 (04) e002193
    CrossrefPubMedSearch in Google Scholar
  • 39 Yu P, Steel JC, Zhang M. et al. Simultaneous blockade of multiple immune system inhibitory checkpoints enhances antitumor activity mediated by interleukin-15 in a murine metastatic colon carcinoma model. Clin Cancer Res 2010; 16: 6019-6028
    CrossrefPubMedSearch in Google Scholar
  • 40 Yamamoto K, Nagatsuma Y, Fukuda Y. et al. Effectiveness of a preoperative exercise and nutritional support program for elderly sarcopenic patients with gastric cancer. Gastric Cancer 2017; 20: 913-918
    CrossrefPubMedSearch in Google Scholar
  • 41 Nowak S, Kloth C, Theis M. et al. Deep learning-based assessment of CT markers of sarcopenia and myosteatosis for outcome assessment in patients with advanced pancreatic cancer after high-intensity focused ultrasound treatment. Eur Radiol 2023;
    CrossrefPubMedSearch in Google Scholar
  • 42 Aleixo GFP, Shachar SS, Nyrop KA. et al. Myosteatosis and prognosis in cancer: Systematic review and meta-analysis. Crit Rev Oncol Hematol 2020; 145: 102839
    CrossrefPubMedSearch in Google Scholar
  • 43 Fang T, Gong Y, Wang Y. Prognostic values of myosteatosis for overall survival in patients with gastric cancers: A meta-analysis with trial sequential analysis. Nutrition 2023; 105: 111866
    CrossrefPubMedSearch in Google Scholar
  • 44 Feng S, Mu H, Hou R. et al. Prognostic value of myosteatosis in patients with lung cancer: a systematic review and meta-analysis. Int J Clin Oncol 2022; 27 (07) 1127-1138
    CrossrefPubMedSearch in Google Scholar
  • 45 Lee CM, Kang J. Prognostic impact of myosteatosis in patients with colorectal cancer: a systematic review and meta-analysis. J Cachexia Sarcopenia Muscle 2020; 11 (05) 1270-1282
    CrossrefPubMedSearch in Google Scholar
  • 46 Iwashita K, Kubota H, Nishioka R. et al. Prognostic Value of Radiomics Analysis of Skeletal Muscle After Radical Irradiation of Esophageal Cancer. Anticancer Res 2023; 43 (04) 1749-1760
    CrossrefPubMedSearch in Google Scholar
  • 47 Saalfeld S, Kreher R, Hille G. et al. Prognostic role of radiomics-based body composition analysis for the 1-year survival for hepatocellular carcinoma patients. J Cachexia Sarcopenia Muscle 2023;
    CrossrefPubMedSearch in Google Scholar