Vol 18, No 5 (2022)
Review paper
Published online: 2021-07-15

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Dual impact from coincide potential complications of cancer therapy and sarcopenia: a narrative review

Anmar Al-Taie1, Aygül Koseoğlu2
Oncol Clin Pract 2022;18(5):302-325.

Abstract

Sarcopenia is a disorder of progressive loss of skeletal muscle mass and strength that is linked with multiple complications, decreased physical activity, lower quality of life and accelerated mortality rate. It is more common among cancer patients and identified with reduced tolerance by the toxic effects from cancer therapy, negative outcomes, lowered response and overall survival rate. This narrative review aims to demonstrate the dual impact from the co-occurrence of cancer therapy; chemotherapy, radiotherapy, immunotherapy, and sarcopenia alongside the potential complications from their coincide effects on cancer prognosis. By searching through data sets, all articles that focused on sarcopenia and cancer therapy were collected in the indexed journals between the years 2000 and 2021 that could provide findings for the potential complications from the coinciding effects of cancer therapy and sarcopenia in cancer patients receiving chemo-radio- and immunotherapy. Outcome measures were the rate of studies showing potential complications from the co-occurrence of cancer therapies and sarcopenia. A total of hundred-two cohort studies were enrolled. The majority were about chemotherapy and sarcopenia (45%). About 56.9% of the studies designed as retrospective analysis, and a high proportion were about chemotherapy and sarcopenia (21.6%). About 63.7% of the studies reported skeletal muscle index as the primary marker. Lower than half of the reviewed studies revealed a significant increase in the rate of sarcopenia (47%). The direct toxic effects of chemotherapy on skeletal muscle were reported in 13.7% of the studies. Studies that reported the impact of sarcopenia on a reduction in chemotherapy cycles were about 10.8%. About 11.8% and 14.7% of the studies showed lowered overall survival by the coinciding impact of chemotherapy/radiotherapy and sarcopenia, respectively. In conclusion, the evaluation of sarcopenia in cancer patients should be considered a primary part of oncological care in cancer patients as there are potential complications and poor survival from the co-occurrence of sarcopenia and different cancer therapies.

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References

  1. Santilli V. Clinical definition of sarcopenia. Clinical Cases in Mineral and Bone Metabolism. 2014.
  2. Rosenberg IH, Rosenberg IH. Sarcopenia: origins and clinical relevance. J Nutr. 1997; 127(5 Suppl): 990S–991S.
  3. Muscaritoli M, Anker SD, Argilés J, et al. Consensus definition of sarcopenia, cachexia and pre-cachexia: joint document elaborated by Special Interest Groups (SIG) "cachexia-anorexia in chronic wasting diseases" and "nutrition in geriatrics". Clin Nutr. 2010; 29(2): 154–159.
  4. Kenis C, Decoster L, Van Puyvelde K, et al. Performance of two geriatric screening tools in older patients with cancer. J Clin Oncol. 2014; 32(1): 19–26.
  5. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, et al. European Working Group on Sarcopenia in Older People. Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing. 2010; 39(4): 412–423.
  6. Kwan P, Kwan P. Sarcopenia, a neurogenic syndrome? J Aging Res. 2013; 2013: 791679.
  7. Pedersen BK, Febbraio MA. Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat Rev Endocrinol. 2012; 8(8): 457–465.
  8. Quinn LS. Interleukin-15: a muscle-derived cytokine regulating fat-to-lean body composition. J Anim Sci. 2008; 86(14 Suppl): E75–E83.
  9. Lutz CT, Quinn LS. Sarcopenia, obesity, and natural killer cell immune senescence in aging: altered cytokine levels as a common mechanism. Aging (Albany NY). 2012; 4(8): 535–546.
  10. Roy P, Chowdhury S, Roy HK. Exercise-induced myokines as emerging therapeutic agents in colorectal cancer prevention and treatment. Future Oncol. 2018; 14(4): 309–312.
  11. Steensberg A, Fischer CP, Keller C, et al. IL-6 enhances plasma IL-1ra, IL-10, and cortisol in humans. Am J Physiol Endocrinol Metab. 2003; 285(2): E433–E437.
  12. Lin JX, Lin JP, Xie JW, et al. Prognostic Value and Association of Sarcopenia and Systemic Inflammation for Patients with Gastric Cancer Following Radical Gastrectomy. Oncologist. 2019; 24(11): e1091–e1101.
  13. Patel HJ, Patel BM. TNF-α and cancer cachexia: Molecular insights and clinical implications. Life Sci. 2017; 170: 56–63.
  14. Janssen I, Shepard DS, Katzmarzyk PT, et al. The healthcare costs of sarcopenia in the United States. J Am Geriatr Soc. 2004; 52(1): 80–85.
  15. Gale CR, Martyn CN, Cooper C, et al. Grip strength, body composition, and mortality. Int J Epidemiol. 2007; 36(1): 228–235.
  16. Zargar H, Almassi N, Kovac E, et al. Change in Psoas Muscle Volume as a Predictor of Outcomes in Patients Treated with Chemotherapy and Radical Cystectomy for Muscle-Invasive Bladder Cancer. Bladder Cancer. 2017; 3(1): 57–63.
  17. 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.
  18. Levolger S, van Vugt JLA, de Bruin RWF, et al. Systematic review of sarcopenia in patients operated on for gastrointestinal and hepatopancreatobiliary malignancies. Br J Surg. 2015; 102(12): 1448–1458.
  19. Kawamura T, Makuuchi R, Tokunaga M, et al. Long-Term Outcomes of Gastric Cancer Patients with Preoperative Sarcopenia. Ann Surg Oncol. 2018; 25(6): 1625–1632.
  20. Blauwhoff-Buskermolen S, Versteeg KS, de van der Schueren MAE, 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): 1339–1344.
  21. Liu J, Motoyama S, Sato Y, et al. Decreased Skeletal Muscle Mass After Neoadjuvant Therapy Correlates with Poor Prognosis in Patients with Esophageal Cancer. Anticancer Res. 2016; 36(12): 6677–6685.
  22. Ma DW, Cho Y, Jeon MJ, et al. Relationship Between Sarcopenia and Prognosis in Patient With Concurrent Chemo-Radiation Therapy for Esophageal Cancer. Front Oncol. 2019; 9: 366.
  23. Paireder M, Asari R, Kristo I, et al. Impact of sarcopenia on outcome in patients with esophageal resection following neoadjuvant chemotherapy for esophageal cancer. Eur J Surg Oncol. 2017; 43(2): 478–484.
  24. Järvinen T, Ilonen I, Kauppi J, et al. Loss of skeletal muscle mass during neoadjuvant treatments correlates with worse prognosis in esophageal cancer: a retrospective cohort study. World J Surg Oncol. 2018; 16(1): 27.
  25. Choi Y, Oh DY, Kim TY, et al. Skeletal Muscle Depletion Predicts the Prognosis of Patients with Advanced Pancreatic Cancer Undergoing Palliative Chemotherapy, Independent of Body Mass Index. PLoS One. 2015; 10(10): e0139749.
  26. Jung HW, Kim JW, Kim JY, et al. Effect of muscle mass on toxicity and survival in patients with colon cancer undergoing adjuvant chemotherapy. Support Care Cancer. 2015; 23(3): 687–694.
  27. Miyamoto Y, Baba Y, Sakamoto Y, et al. Negative Impact of Skeletal Muscle Loss after Systemic Chemotherapy in Patients with Unresectable Colorectal Cancer. PLoS One. 2015; 10(6): e0129742.
  28. Derksen JWG, Kurk SA, Oskam MJ, et al. Factors Contributing to Cancer-Related Muscle Wasting During First-Line Systemic Treatment for Metastatic Colorectal Cancer. JNCI Cancer Spectr. 2019; 3(2): pkz014.
  29. Go SI, Park MiJ, Song HN, et al. Sarcopenia and inflammation are independent predictors of survival in male patients newly diagnosed with small cell lung cancer. Support Care Cancer. 2016; 24(5): 2075–2084.
  30. Prado CMM, 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(8): 2920–2926.
  31. Rutten IJG, van Dijk DPJ, Kruitwagen RF, et al. Loss of skeletal muscle during neoadjuvant chemotherapy is related to decreased survival in ovarian cancer patients. J Cachexia Sarcopenia Muscle. 2016; 7(4): 458–466.
  32. Awad S, Tan BH, Cui H, et al. Marked changes in body composition following neoadjuvant chemotherapy for oesophagogastric cancer. Clin Nutr. 2012; 31(1): 74–77.
  33. Yip C, Goh V, Davies A, et al. Assessment of sarcopenia and changes in body composition after neoadjuvant chemotherapy and associations with clinical outcomes in oesophageal cancer. Eur Radiol. 2014; 24(5): 998–1005.
  34. Daly LE, Ní Bhuachalla ÉB, Power DG, et al. Loss of skeletal muscle during systemic chemotherapy is prognostic of poor survival in patients with foregut cancer. J Cachexia Sarcopenia Muscle. 2018; 9(2): 315–325.
  35. Guinan EM, Doyle SL, Bennett AE, et al. Sarcopenia during neoadjuvant therapy for oesophageal cancer: characterising the impact on muscle strength and physical performance. Support Care Cancer. 2018; 26(5): 1569–1576.
  36. Cooper AB, Slack R, Fogelman D, et al. Characterization of Anthropometric Changes that Occur During Neoadjuvant Therapy for Potentially Resectable Pancreatic Cancer. Ann Surg Oncol. 2015; 22(7): 2416–2423.
  37. Benjamin AJ, Buschmann MM, Zhang SQ, et al. The impact of changes in radiographic sarcopenia on overall survival in older adults undergoing different treatment pathways for pancreatic cancer. J Geriatr Oncol. 2018; 9(4): 367–372.
  38. Sandini M, Patino M, Ferrone CR, et al. Association Between Changes in Body Composition and Neoadjuvant Treatment for Pancreatic Cancer. JAMA Surg. 2018; 153(9): 809–815.
  39. Poterucha T, Burnette B, Jatoi A. A decline in weight and attrition of muscle in colorectal cancer patients receiving chemotherapy with bevacizumab. Med Oncol. 2012; 29(2): 1005–1009.
  40. Eriksson S, Nilsson JH, Strandberg Holka P, et al. The impact of neoadjuvant chemotherapy on skeletal muscle depletion and preoperative sarcopenia in patients with resectable colorectal liver metastases. HPB (Oxford). 2017; 19(4): 331–337.
  41. Nattenmüller J, Wochner R, Muley T, et al. Prognostic Impact of CT-Quantified Muscle and Fat Distribution before and after First-Line-Chemotherapy in Lung Cancer Patients. PLoS One. 2017; 12(1): e0169136.
  42. Goncalves MD, Taylor S, Halpenny DF, et al. Imaging skeletal muscle volume, density, and FDG uptake before and after induction therapy for non-small cell lung cancer. Clin Radiol. 2018; 73(5): 505.e1–505.e8.
  43. Zargar H, Almassi N, Kovac E, et al. Change in Psoas Muscle Volume as a Predictor of Outcomes in Patients Treated with Chemotherapy and Radical Cystectomy for Muscle-Invasive Bladder Cancer. Bladder Cancer. 2017; 3(1): 57–63.
  44. Rimar KJ, Glaser AP, Kundu S, et al. Changes in Lean Muscle Mass Associated with Neoadjuvant Platinum-Based Chemotherapy in Patients with Muscle Invasive Bladder Cancer. Bladder Cancer. 2018; 4(4): 411–418.
  45. Prado CMM, 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(7): 629–635.
  46. Stene GB, Helbostad JL, Amundsen T, et al. Changes in skeletal muscle mass during palliative chemotherapy in patients with advanced lung cancer. Acta Oncol. 2015; 54(3): 340–348.
  47. Englesbe MJ, Patel SP, He K, et al. Sarcopenia and mortality after liver transplantation. J Am Coll Surg. 2010; 211(2): 271–278.
  48. Garcia JM, Scherer T, Chen Ja, et al. Inhibition of cisplatin-induced lipid catabolism and weight loss by ghrelin in male mice. Endocrinology. 2013; 154(9): 3118–3129.
  49. Rier HN, Jager A, Sleijfer S, et al. Changes in body composition and muscle attenuation during taxane-based chemotherapy in patients with metastatic breast cancer. Breast Cancer Res Treat. 2018; 168(1): 95–105.
  50. Chen JA, Splenser A, Guillory B, et al. Ghrelin prevents tumour- and cisplatin-induced muscle wasting: characterization of multiple mechanisms involved. J Cachexia Sarcopenia Muscle. 2015; 6(2): 132–143.
  51. Gilliam LAA, St Clair DK. Chemotherapy-induced weakness and fatigue in skeletal muscle: the role of oxidative stress. Antioxid Redox Signal. 2011; 15(9): 2543–2563.
  52. Barreto R, Waning DL, Gao H, et al. Chemotherapy-related cachexia is associated with mitochondrial depletion and the activation of ERK1/2 and p38 MAPKs. Oncotarget. 2016; 7(28): 43442–43460.
  53. Chen JL, Colgan TD, Walton KL, et al. The TGF-β Signalling Network in Muscle Development, Adaptation and Disease. Adv Exp Med Biol. 2016; 900: 97–131.
  54. Ali R, Baracos VE, Sawyer MB, et al. Lean body mass as an independent determinant of dose-limiting toxicity and neuropathy in patients with colon cancer treated with FOLFOX regimens. Cancer Med. 2016; 5(4): 607–616.
  55. Palmela C, Velho S, Agostinho L, et al. Body Composition as a Prognostic Factor of Neoadjuvant Chemotherapy Toxicity and Outcome in Patients with Locally Advanced Gastric Cancer. J Gastric Cancer. 2017; 17(1): 74–87.
  56. Prado CMM, Baracos VE, McCargar LJ, et al. Body composition as an independent determinant of 5-fluorouracil-based chemotherapy toxicity. Clin Cancer Res. 2007; 13(11): 3264–3268.
  57. Barret M, Antoun S, Dalban C, et al. Sarcopenia is linked to treatment toxicity in patients with metastatic colorectal cancer. Nutr Cancer. 2014; 66(4): 583–589.
  58. Kurk S, Peeters P, Stellato R, et al. Skeletal muscle mass loss and dose-limiting toxicities in metastatic colorectal cancer patients. J Cachexia Sarcopenia Muscle. 2019; 10(4): 803–813.
  59. Prado CMM, Lima ISF, Baracos VE, et al. An exploratory study of body composition as a determinant of epirubicin pharmacokinetics and toxicity. Cancer Chemother Pharmacol. 2011; 67(1): 93–101.
  60. Mazzuca F, Onesti CE, Roberto M, et al. Lean body mass wasting and toxicity in early breast cancer patients receiving anthracyclines. Oncotarget. 2018; 9(39): 25714–25722.
  61. Kodera Y. More than 6 months of postoperative adjuvant chemotherapy results in loss of skeletal muscle: a challenge to the current standard of care. Gastric Cancer. 2015; 18(2): 203–204.
  62. Pin F, Barreto R, Couch ME, et al. Cachexia induced by cancer and chemotherapy yield distinct perturbations to energy metabolism. J Cachexia Sarcopenia Muscle. 2019; 10(1): 140–154.
  63. Moreira-Pais A, Ferreira R, Gil da Costa R. Platinum-induced muscle wasting in cancer chemotherapy: Mechanisms and potential targets for therapeutic intervention. Life Sci. 2018; 208: 1–9.
  64. Nissinen TA, Degerman J, Räsänen M, et al. Systemic blockade of ACVR2B ligands prevents chemotherapy-induced muscle wasting by restoring muscle protein synthesis without affecting oxidative capacity or atrogenes. Sci Rep. 2016; 6: 32695.
  65. Van Gammeren D, Damrauer JS, Jackman RW, et al. The IkappaB kinases IKKalpha and IKKbeta are necessary and sufficient for skeletal muscle atrophy. FASEB J. 2009; 23(2): 362–370.
  66. Hiensch AE, Bolam KA, Mijwel S, et al. Doxorubicin-induced skeletal muscle atrophy: Elucidating the underlying molecular pathways. Acta Physiol (Oxf). 2020; 229(2): e13400.
  67. Denekamp J, Rojas A. Cell kinetics and radiation pathology. Experientia. 1989; 45(1): 33–41.
  68. Lefaix JL, Delanian S, Leplat JJ, et al. [Radiation-induced cutaneo-muscular fibrosis (III): major therapeutic efficacy of liposomal Cu/Zn superoxide dismutase]. Bull Cancer. 1993; 80(9): 799–807.
  69. Al-Taie A, Al-Shohani AD, Albasry Z, et al. Current topical trends and novel therapeutic approaches and delivery systems for oral mucositis management. J Pharm Bioallied Sci. 2020; 12(2): 94–101.
  70. Sroussi HY, Epstein JB, Bensadoun RJ, et al. Common oral complications of head and neck cancer radiation therapy: mucositis, infections, saliva change, fibrosis, sensory dysfunctions, dental caries, periodontal disease, and osteoradionecrosis. Cancer Med. 2017; 6(12): 2918–2931.
  71. Arribas L, Hurtós L, Taberna M, et al. Nutritional changes in patients with locally advanced head and neck cancer during treatment. Oral Oncol. 2017; 71: 67–74.
  72. Alshadwi A, Nadershah M, Carlson ER, et al. Nutritional considerations for head and neck cancer patients: a review of the literature. J Oral Maxillofac Surg. 2013; 71(11): 1853–1860.
  73. Ganju RG, Morse R, Hoover A, et al. The impact of sarcopenia on tolerance of radiation and outcome in patients with head and neck cancer receiving chemoradiation. Radiother Oncol. 2019; 137: 117–124.
  74. Forastiere AA, Goepfert H, Maor M, et al. Concurrent chemotherapy and radiotherapy for organ preservation in advanced laryngeal cancer. N Engl J Med. 2003; 349(22): 2091–2098.
  75. Li G, Jiang XY, Qiu Bo, et al. Vicious circle of acute radiation toxicities and weight loss predicts poor prognosis for nasopharyngeal carcinoma patients receiving intensity modulated radiotherapy. J Cancer. 2017; 8(5): 832–838.
  76. Panje CM, Höng L, Hayoz S, et al. Swiss Group for Clinical Cancer Research (SAKK). Skeletal muscle mass correlates with increased toxicity during neoadjuvant radiochemotherapy in locally advanced esophageal cancer: A SAKK 75/08 substudy. Radiat Oncol. 2019; 14(1): 166.
  77. Lønbro S, Petersen GB, Andersen JR, et al. Prediction of critical weight loss during radiation treatment in head and neck cancer patients is dependent on BMI. Support Care Cancer. 2016; 24(5): 2101–2109.
  78. Ghadjar P, Hayoz S, Zimmermann F, et al. Swiss Group for Clinical Cancer Research (SAKK). Impact of weight loss on survival after chemoradiation for locally advanced head and neck cancer: secondary results of a randomized phase III trial (SAKK 10/94). Radiat Oncol. 2015; 10: 21.
  79. Chargi N, Bril SI, de Jong PA, et al. Sarcopenia is a prognostic factor for overall survival in elderly patients with head-and-neck cancer. Eur Arch Otorhinolaryngol. 2019; 276(5): 1475–1486.
  80. Cho Y, Kim JW, Keum KiC, et al. Prognostic Significance of Sarcopenia With Inflammation in Patients With Head and Neck Cancer Who Underwent Definitive Chemoradiotherapy. Front Oncol. 2018; 8: 457.
  81. Mallet R, Modzelewski R, Lequesne J, et al. Prognostic value of sarcopenia in patients treated by Radiochemotherapy for locally advanced oesophageal cancer. Radiat Oncol. 2020; 15(1): 116.
  82. van Rijn-Dekker MI, van den Bosch L, van den Hoek JGM, et al. Impact of sarcopenia on survival and late toxicity in head and neck cancer patients treated with radiotherapy. Radiother Oncol. 2020; 147: 103–110.
  83. Thureau S, Lebret L, Lequesne J, et al. Prospective Evaluation of Sarcopenia in Head and Neck Cancer Patients Treated with Radiotherapy or Radiochemotherapy. Cancers (Basel). 2021; 13(4).
  84. Sanders KJC, Hendriks LE, Troost EGC, et al. Early Weight Loss during Chemoradiotherapy Has a Detrimental Impact on Outcome in NSCLC. J Thorac Oncol. 2016; 11(6): 873–879.
  85. Shen LJ, Chen C, Li BF, et al. High weight loss during radiation treatment changes the prognosis in under-/normal weight nasopharyngeal carcinoma patients for the worse: a retrospective analysis of 2433 cases. PLoS One. 2013; 8(7): e68660.
  86. Olson B, Edwards J, Stone L, et al. Association of Sarcopenia With Oncologic Outcomes of Primary Surgery or Definitive Radiotherapy Among Patients With Localized Oropharyngeal Squamous Cell Carcinoma. JAMA Otolaryngol Head Neck Surg. 2020; 146(8): 714–722.
  87. Ma DW, Cho Y, Jeon MJ, et al. Relationship Between Sarcopenia and Prognosis in Patient With Concurrent Chemo-Radiation Therapy for Esophageal Cancer. Front Oncol. 2019; 9: 366.
  88. Yoon HG, Oh D, Ahn YC, et al. Prognostic Impact of Sarcopenia and Skeletal Muscle Loss During Neoadjuvant Chemoradiotherapy in Esophageal Cancer. Cancers (Basel). 2020; 12(4).
  89. Liang H, Peng H, Chen L. Prognostic Value of Sarcopenia and Systemic Inflammation Markers in Patients Undergoing Definitive Radiotherapy for Esophageal Cancer. Cancer Manag Res. 2021; 13: 181–192.
  90. Lee J, Cho Y, Park S, et al. Skeletal Muscle Depletion Predicts the Prognosis of Patients With Hepatocellular Carcinoma Treated With Radiotherapy. Front Oncol. 2019; 9: 1075.
  91. Lin J, Peng J, Qdaisat A, et al. Severe weight loss during preoperative chemoradiotherapy compromises survival outcome for patients with locally advanced rectal cancer. J Cancer Res Clin Oncol. 2016; 142(12): 2551–2560.
  92. Park SEe, Hwang InG, Choi CH, et al. Sarcopenia is poor prognostic factor in older patients with locally advanced rectal cancer who received preoperative or postoperative chemoradiotherapy. Medicine (Baltimore). 2018; 97(48): e13363.
  93. Kiyotoki T, Nakamura K, Haraga J, et al. Sarcopenia Is an Important Prognostic Factor in Patients With Cervical Cancer Undergoing Concurrent Chemoradiotherapy. Int J Gynecol Cancer. 2018; 28(1): 168–175.
  94. Pielkenrood BJ, van Urk PR, van der Velden JM, et al. Impact of body fat distribution and sarcopenia on the overall survival in patients with spinal metastases receiving radiotherapy treatment: a prospective cohort study. Acta Oncol. 2020; 59(3): 291–297.
  95. Langendijk JA, Doornaert P, Verdonck-de Leeuw IM, et al. Impact of late treatment-related toxicity on quality of life among patients with head and neck cancer treated with radiotherapy. J Clin Oncol. 2008; 26(22): 3770–3776.
  96. Tsekoura M, Kastrinis A, Katsoulaki M, et al. Sarcopenia and Its Impact on Quality of Life. Adv Exp Med Biol. 2017; 987: 213–218.
  97. Elias R, Hartshorn K, Rahma O, et al. Aging, immune senescence, and immunotherapy: A comprehensive review. Semin Oncol. 2018; 45(4): 187–200.
  98. Pawelec G, Derhovanessian E, Larbi A. Immunosenescence and cancer. Crit Rev Oncol/Hematol. 2010; 75(2): 165–172.
  99. Pedersen BK. Muscles and their myokines. J Exp Biol. 2011; 214(Pt 2): 337–346.
  100. Nagaraj S, Gabrilovich DI. Myeloid-derived suppressor cells in human cancer. Cancer J. 2010; 16(4): 348–353.
  101. Verschoor CP, Johnstone J, Millar J, et al. Blood CD33(+)HLA-DR(-) myeloid-derived suppressor cells are increased with age and a history of cancer. J Leukoc Biol. 2013; 93(4): 633–637.
  102. Londhe P, Guttridge DC. Inflammation induced loss of skeletal muscle. Bone. 2015; 80: 131–142.
  103. Tsukamoto H, Fujieda K, Miyashita A, et al. Combined Blockade of IL6 and PD-1/PD-L1 Signaling Abrogates Mutual Regulation of Their Immunosuppressive Effects in the Tumor Microenvironment. Cancer Res. 2018; 78(17): 5011–5022.
  104. Kim EY, Lee HY, Kim YS, et al. Prognostic Significance of CT-Determined Sarcopenia in Patients with Small-Cell Lung Cancer. J Thorac Oncol. 2015; 10(12): 1795–1799.
  105. Ábrigo J, Campos F, Simon F, et al. TGF-β requires the activation of canonical and non-canonical signalling pathways to induce skeletal muscle atrophy. Biol Chem. 2018; 399(3): 253–264.
  106. Mariathasan S, Turley SJ, Nickles D, et al. TGFβ attenuates tumour response to PD-L1 blockade by contributing to exclusion of T cells. Nature. 2018; 554(7693): 544–548.
  107. Suzuki Y, Okamoto T, Fujishita T, et al. Clinical implications of sarcopenia in patients undergoing complete resection for early non-small cell lung cancer. Lung Cancer. 2016; 101: 92–97.
  108. Wherry EJ. T cell exhaustion. Nat Immunol. 2011; 12(6): 492–499.
  109. 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(5): e37563.
  110. Nishioka N, Uchino J, Hirai S, et al. Association of Sarcopenia with and Efficacy of Anti-PD-1/PD-L1 Therapy in Non-Small-Cell Lung Cancer. J Clin Med. 2019; 8(4).
  111. Heidelberger V, Goldwasser F, Kramkimel N, et al. Sarcopenic overweight is associated with early acute limiting toxicity of anti-PD1 checkpoint inhibitors in melanoma patients. Invest New Drugs. 2017; 35(4): 436–441.
  112. Daly LE, Power DG, O'Reilly Á, et al. The impact of body composition parameters on ipilimumab toxicity and survival in patients with metastatic melanoma. Br J Cancer. 2017; 116(3): 310–317.
  113. Revel MP, Raynard B, Pigneur F, et al. Sarcopenia and toxicity of the anti-PD1 inhibitors in real-life lung cancer patients: Results from the French Nationwide SCAN study. J Clin Oncol. 2018; 36(15_suppl): e21066–e21066.
  114. Heidelberger V, Kramkimel N, Huillard O, et al. Sarcopenia associated with a body mass index (BMI) > 25 kg/m2 predicts severe acute toxicity of nivolumab and pembrolizumab in melanoma patients. Ann Oncol. 2016; 27: vi387.
  115. 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(6): 2401–2408.
  116. Veasey-Rodrigues H, Parsons HA, Janku F, et al. A pilot study of temsirolimus and body composition. J Cachexia Sarcopenia Muscle. 2013; 4(4): 259–265.
  117. Bozzetti F. Chemotherapy-Induced Sarcopenia. Curr Treat Options Oncol. 2020; 21(1): 7.
  118. Cortellini A, Verna L, Porzio G, et al. Predictive value of skeletal muscle mass for immunotherapy with nivolumab in non-small cell lung cancer patients: A "hypothesis-generator" preliminary report. Thorac Cancer. 2019; 10(2): 347–351.
  119. Shiroyama T, Nagatomo I, Koyama S, et al. Impact of sarcopenia in patients with advanced non-small cell lung cancer treated with PD-1 inhibitors: A preliminary retrospective study. Sci Rep. 2019; 9(1): 2447.
  120. Kano M, Hihara J, Tokumoto N, et al. Association between skeletal muscle loss and the response to nivolumab immunotherapy in advanced gastric cancer patients. Int J Clin Oncol. 2021; 26(3): 523–531.
  121. Reisinger KW, Bosmans JW, Uittenbogaart M, et al. Loss of Skeletal Muscle Mass During Neoadjuvant Chemoradiotherapy Predicts Postoperative Mortality in Esophageal Cancer Surgery. Ann Surg Oncol. 2015; 22(13): 4445–4452.
  122. Elliott JA, Doyle SL, Murphy CF, et al. Sarcopenia: Prevalence, and Impact on Operative and Oncologic Outcomes in the Multimodal Management of Locally Advanced Esophageal Cancer. Ann Surg. 2017; 266(5): 822–830.
  123. Paireder M, Asari R, Kristo I, et al. Impact of sarcopenia on outcome in patients with esophageal resection following neoadjuvant chemotherapy for esophageal cancer. Eur J Surg Oncol. 2017; 43(2): 478–484.
  124. Dijksterhuis WPM, Pruijt MJ, van der Woude SO, et al. Association between body composition, survival, and toxicity in advanced esophagogastric cancer patients receiving palliative chemotherapy. J Cachexia Sarcopenia Muscle. 2019; 10(1): 199–206.
  125. Ota T, Ishikawa T, Endo Y, et al. Skeletal muscle mass as a predictor of the response to neo-adjuvant chemotherapy in locally advanced esophageal cancer. Med Oncol. 2019; 36(2): 15.
  126. Voisinet M, Venkatasamy A, Alratrout H, et al. How to Prevent Sarcopenia Occurrence during Neoadjuvant Chemotherapy for Oesogastric Adenocarcinoma? Nutr Cancer. 2021; 73(5): 802–808.
  127. Dalal S, Hui D, Bidaut L, et al. Relationships among body mass index, longitudinal body composition alterations, and survival in patients with locally advanced pancreatic cancer receiving chemoradiation: a pilot study. J Pain Symptom Manage. 2012; 44(2): 181–191.
  128. Fogelman DR, Holmes H, Mohammed K, et al. Does IGFR1 inhibition result in increased muscle mass loss in patients undergoing treatment for pancreatic cancer? J Cachexia Sarcopenia Muscle. 2014; 5(4): 307–313.
  129. Antoun S, Bayar MA, Dyevre V, et al. No evidence for changes in skeletal muscle mass or weight during first-line chemotherapy for metastatic colorectal cancer. BMC Cancer. 2019; 19(1): 847.
  130. Kobayashi T, Kawai H, Nakano O, et al. Rapidly declining skeletal muscle mass predicts poor prognosis of hepatocellular carcinoma treated with transcatheter intra-arterial therapies. BMC Cancer. 2018; 18(1): 756.
  131. Atlan P, Bayar MA, Lanoy E, et al. Factors which modulate the rates of skeletal muscle mass loss in non-small cell lung cancer patients: a pilot study. Support Care Cancer. 2017; 25(11): 3365–3373.
  132. Kakinuma K, Tsuruoka H, Morikawa K, et al. Differences in skeletal muscle loss caused by cytotoxic chemotherapy and molecular targeted therapy in patients with advanced non-small cell lung cancer. Thorac Cancer. 2018; 9(1): 99–104.
  133. Xiao DY, Luo S, O'Brian K, et al. Longitudinal Body Composition Changes in Diffuse Large B-cell Lymphoma Survivors: A Retrospective Cohort Study of United States Veterans. J Natl Cancer Inst. 2016; 108(11).
  134. Grossberg AJ, Chamchod S, Fuller CD, et al. Association of Body Composition With Survival and Locoregional Control of Radiotherapy-Treated Head and Neck Squamous Cell Carcinoma. JAMA Oncol. 2016; 2(6): 782–789.
  135. Chauhan NS, Samuel SR, Meenar N, et al. Sarcopenia in male patients with head and neck cancer receiving chemoradiotherapy: a longitudinal pilot study. PeerJ. 2020; 8: e8617.
  136. Op den Kamp CMH, De Ruysscher DKM, van den Heuvel M, et al. Early body weight loss during concurrent chemo-radiotherapy for non-small cell lung cancer. J Cachexia Sarcopenia Muscle. 2014; 5(2): 127–137.
  137. Kiss N, Beraldo J, Everitt S. Early Skeletal Muscle Loss in Non-Small Cell Lung Cancer Patients Receiving Chemoradiation and Relationship to Survival. Support Care Cancer. 2019; 27(7): 2657–2664.
  138. Murimwa GZ, Venkat PS, Jin W, et al. Impact of sarcopenia on outcomes of locally advanced esophageal cancer patients treated with neoadjuvant chemoradiation followed by surgery. J Gastrointest Oncol. 2017; 8(5): 808–815.
  139. Shiba S, Shibuya K, Katoh H, et al. No Deterioration in Clinical Outcomes of Carbon Ion Radiotherapy for Sarcopenia Patients with Hepatocellular Carcinoma. Anticancer Res. 2018; 38(6): 3579–3586.
  140. Matsubara Y, Nakamura K, Matsuoka H, et al. Sarcopenia Is Not a Prognostic Factor of Outcome in Patients With Cervical Cancer Undergoing Concurrent Chemoradiotherapy or Radiotherapy. Anticancer Res. 2019; 39(2): 933–939.
  141. Couderc AL, Muracciole X, Nouguerede E, et al. HoSAGE: Sarcopenia in Older Patients before and after Treatment with Androgen Deprivation Therapy and Radiotherapy for Prostate Cancer. J Nutr Health Aging. 2020; 24(2): 205–209.
  142. Ferini G, Cacciola A, Parisi S, et al. Curative Radiotherapy in Elderly Patients With Muscle Invasive Bladder Cancer: The Prognostic Role of Sarcopenia. In Vivo. 2021; 35(1): 571–578.
  143. Zhang G, Li X, Sui C, et al. Incidence and risk factor analysis for sarcopenia in patients with cancer. Oncol Lett. 2016; 11(2): 1230–1234.
  144. Magri V, Gottfried T, Di Segni M, et al. Correlation of body composition by computerized tomography and metabolic parameters with survival of nivolumab-treated lung cancer patients. Cancer Manag Res. 2019; 11: 8201–8207.
  145. Popinat G, Cousse S, Goldfarb L, et al. Sub-cutaneous Fat Mass measured on multislice computed tomography of pretreatment PET/CT is a prognostic factor of stage IV non-small cell lung cancer treated by nivolumab. Oncoimmunology. 2019; 8(5): e1580128.
  146. Cortellini A, Bozzetti F, Palumbo P, et al. Weighing the role of skeletal muscle mass and muscle density in cancer patients receiving PD-1/PD-L1 checkpoint inhibitors: a multicenter real-life study. Sci Rep. 2020; 10(1): 1456.
  147. Roch B, Coffy A, Jean-Baptiste S, et al. Cachexia - sarcopenia as a determinant of disease control rate and survival in non-small lung cancer patients receiving immune-checkpoint inhibitors. Lung Cancer. 2020; 143: 19–26.
  148. Petrova MP, Donev IS, Radanova MA, et al. Sarcopenia and high NLR are associated with the development of hyperprogressive disease after second-line pembrolizumab in patients with non-small-cell lung cancer. Clin Exp Immunol. 2020; 202(3): 353–362.
  149. Ichihara E, Harada D, Inoue K, et al. The impact of body mass index on the efficacy of anti-PD-1/PD-L1 antibodies in patients with non-small cell lung cancer. Lung Cancer. 2020; 139: 140–145.
  150. Minami S, Ihara S, Tanaka T, et al. Sarcopenia and Visceral Adiposity Did Not Affect Efficacy of Immune-Checkpoint Inhibitor Monotherapy for Pretreated Patients With Advanced Non-Small Cell Lung Cancer. World J Oncol. 2020; 11(1): 9–22.
  151. Katayama Y, Shimamoto T, Yamada T, et al. Retrospective Efficacy Analysis of Immune Checkpoint Inhibitor Rechallenge in Patients with Non-Small Cell Lung Cancer. J Clin Med. 2019; 9(1).
  152. Tsukagoshi M, Yokobori T, Yajima T, et al. Skeletal muscle mass predicts the outcome of nivolumab treatment for non-small cell lung cancer. Medicine (Baltimore). 2020; 99(7): e19059.
  153. Takada K, Yoneshima Y, Tanaka K, et al. Clinical impact of skeletal muscle area in patients with non-small cell lung cancer treated with anti-PD-1 inhibitors. J Cancer Res Clin Oncol. 2020; 146(5): 1217–1225.
  154. Kichenadasse G, Miners JO, Mangoni AA, et al. Association Between Body Mass Index and Overall Survival With Immune Checkpoint Inhibitor Therapy for Advanced Non-Small Cell Lung Cancer. JAMA Oncol. 2020; 6(4): 512–518.
  155. Kim YY, Lee J, Jeong WK, et al. Prognostic significance of sarcopenia in microsatellite-stable gastric cancer patients treated with programmed death-1 inhibitors. Gastric Cancer. 2021; 24(2): 457–466.
  156. Qayyum A, Bhosale P, Aslam R, et al. Effect of sarcopenia on systemic targeted therapy response in patients with advanced hepatocellular carcinoma. Abdom Radiol (NY). 2021; 46(3): 1008–1015.
  157. Akce M, Liu Y, Zakka K, et al. Impact of Sarcopenia, BMI, and Inflammatory Biomarkers on Survival in Advanced Hepatocellular Carcinoma Treated With Anti-PD-1 Antibody. Am J Clin Oncol. 2021; 44(2): 74–81.
  158. Hu JB, Ravichandran S, Rushing C, et al. Higher BMI, But Not Sarcopenia, Is Associated With Pembrolizumab-related Toxicity in Patients With Advanced Melanoma. Anticancer Res. 2020; 40(9): 5245–5254.
  159. Shimizu T, Miyake M, Hori S, et al. Clinical Impact of Sarcopenia and Inflammatory/Nutritional Markers in Patients with Unresectable Metastatic Urothelial Carcinoma Treated with Pembrolizumab. Diagnostics (Basel). 2020; 10(5).
  160. Fukushima H, Fukuda S, Moriyama S, et al. Impact of sarcopenia on the efficacy of pembrolizumab in patients with advanced urothelial carcinoma: a preliminary report. Anticancer Drugs. 2020; 31(8): 866–871.
  161. Gyawali B, Shimokata T, Honda K, et al. Muscle wasting associated with the long-term use of mTOR inhibitors. Mol Clin Oncol. 2016; 5(5): 641–646.