Skip to main content

Advertisement

SpringerLink
Log in

Gastric Cancer with Sarcopenia: an Area Worth Focusing On

  • Published:
Current Treatment Options in Oncology Aims and scope Submit manuscript

Opinion statement

Gastric cancer (GC) is the fifth most common cancer and the third leading cause of cancer death worldwide, which seriously endangers human health. A number of studies have shown that sarcopenia occurs more frequently in patients with gastric cancer than in the general population and can significantly affect the disease status and survival of patients, which is of great significance in predicting the prognosis of gastric cancer. Patients with gastric cancer may suffer sarcopenia no matter before or after surgery, and the pathogenesis is complex. Abnormal nutrient metabolism and reduced exercise are the leading causes. In addition, surgical treatment and chemotherapy for gastric cancer might participate in the physiological and pathological mechanism of sarcopenia. Generally speaking, exercise and nutritional therapy are the main prevention and treatment methods for sarcopenia. But more prospective evidence is needed to establish reasonable interventions, and other drug treatments are in their infancy. For the diagnostic criteria of sarcopenia, the cut-off values of the skeletal muscle mass index obtained from CT images vary widely and need to be standardized and unified. We also need to explore simple predictors to facilitate sarcopenia risk assessment. More research is needed to formulate more appropriate treatments for gastric cancer patients with sarcopenia.

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

Similar content being viewed by others

References and Recommended Reading

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Smyth EC, Nilsson M, Grabsch HI, van Grieken NC, Lordick F. Gastric cancer. Lancet. 2020;396(10251):635–48.

    Article  CAS  PubMed  Google Scholar 

  2. Ongaro E, Buoro V, Cinausero M, Caccialanza R, Turri A, Fanotto V, et al. Sarcopenia in gastric cancer: when the loss costs too much. Gastric Cancer. 2017;20(4):563–72.

    Article  PubMed  Google Scholar 

  3. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, et al. Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing. 2010;39(4):412–23.

    Article  PubMed  PubMed Central  Google Scholar 

  4. •• Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48(1):16–31. The European Working Group on Sarcopenia in Older People has held its second meeting to update diagnostic criteria for the condition.

    Article  PubMed  Google Scholar 

  5. 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 

  6. Xia L, Zhao R, Wan Q, Wu Y, Zhou Y, Wang Y, et al. Sarcopenia and adverse health-related outcomes: An umbrella review of meta-analyses of observational studies. Cancer Med. 2020;9(21):7964–78.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Mayhew AJ, Amog K, Phillips S, Parise G, McNicholas PD, de Souza RJ, et al. The prevalence of sarcopenia in community-dwelling older adults, an exploration of differences between studies and within definitions: a systematic review and meta-analyses. Age Ageing. 2019;48(1):48–56.

    Article  CAS  PubMed  Google Scholar 

  8. von Haehling S, Morley JE, Anker SD. An overview of sarcopenia: facts and numbers on prevalence and clinical impact. J Cachexia Sarcopenia Muscle. 2010;1(2):129–33.

    Article  Google Scholar 

  9. Hopancı Bıçaklı D, Çehreli R, Özveren A, Meseri R, Uslu R, Karabulut B, et al. Evaluation of sarcopenia, sarcopenic obesity, and phase angle in geriatric gastrointestinal cancer patients: before and after chemotherapy. Turk J Med Sci. 2019;49(2):583–8.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Haiducu C, Buzea A, Mirea LE, Dan GA. The prevalence and the impact of sarcopenia in digestive cancers. A systematic review. Rom J Intern Med. 2021;59(4):328–44.

    PubMed  Google Scholar 

  11. Zhuang CL, Shen X, Zou HB, Dong QT, Cai HY, Chen XL, et al. EWGSOP2 versus EWGSOP1 for sarcopenia to predict prognosis in patients with gastric cancer after radical gastrectomy: analysis from a large-scale prospective study. Clin Nutr. 2020;39(7):2301–10.

    Article  PubMed  Google Scholar 

  12. Zhuang CL, Huang DD, Pang WY, Zhou CJ, Wang SL, Lou N, et al. Sarcopenia is an independent predictor of severe postoperative complications and long-term survival after radical gastrectomy for gastric cancer: analysis from a large-scale cohort. Medicine (Baltimore). 2016;95(13): e3164.

    Article  PubMed  Google Scholar 

  13. Fukuda Y, Yamamoto K, Hirao M, Nishikawa K, Nagatsuma Y, Nakayama T, et al. Sarcopenia is associated with severe postoperative complications in elderly gastric cancer patients undergoing gastrectomy. Gastric Cancer. 2016;19(3):986–93.

    Article  PubMed  Google Scholar 

  14. Wang SL, Zhuang CL, Huang DD, Pang WY, Lou N, Chen FF, et al. Sarcopenia adversely impacts postoperative clinical outcomes following gastrectomy in patients with gastric cancer: a prospective study. Ann Surg Oncol. 2016;23(2):556–64.

    Article  PubMed  Google Scholar 

  15. Huang DD, Chen XX, Chen XY, Wang SL, Shen X, Chen XL, et al. Sarcopenia predicts 1-year mortality in elderly patients undergoing curative gastrectomy for gastric cancer: a prospective study. J Cancer Res Clin Oncol. 2016;142(11):2347–56.

    Article  CAS  PubMed  Google Scholar 

  16. Huang DD, Zhou CJ, Wang SL, Mao ST, Zhou XY, Lou N, et al. Impact of different sarcopenia stages on the postoperative outcomes after radical gastrectomy for gastric cancer. Surgery. 2017;161(3):680–93.

    Article  PubMed  Google Scholar 

  17. Zhou CJ, Zhang FM, Zhang FY, Yu Z, Chen XL, Shen X, et al. Sarcopenia: a new predictor of postoperative complications for elderly gastric cancer patients who underwent radical gastrectomy. J Surg Res. 2017;211:137–46.

    Article  PubMed  Google Scholar 

  18. Lou N, Chi CH, Chen XD, Zhou CJ, Wang SL, Zhuang CL, et al. Sarcopenia in overweight and obese patients is a predictive factor for postoperative complication in gastric cancer: a prospective study. Eur J Surg Oncol. 2017;43(1):188–95.

    Article  CAS  PubMed  Google Scholar 

  19. Kawamura T, Makuuchi R, Tokunaga M, Tanizawa Y, Bando E, Yasui H, et al. Long-term outcomes of gastric cancer patients with preoperative sarcopenia. Ann Surg Oncol. 2018;25(6):1625–32.

    Article  PubMed  Google Scholar 

  20. Yamamoto K, Hirao M, Nishikawa K, Omori T, Yanagimoto Y, Shinno N, et al. sarcopenia is associated with impaired overall survival after gastrectomy for elderly gastric cancer. Anticancer Res. 2019;39(8):4297–303.

    Article  PubMed  Google Scholar 

  21. Chen XY, Li B, Ma BW, Zhang XZ, Chen WZ, Lu LS, et al. Sarcopenia is an effective prognostic indicator of postoperative outcomes in laparoscopic-assisted gastrectomy. Eur J Surg Oncol. 2019;45(6):1092–8.

    Article  PubMed  Google Scholar 

  22. Yu JI, Choi C, Lee J, Kang WK, Park SH, Kim ST, et al. Effect of baseline sarcopenia on adjuvant treatment for D2 dissected gastric cancer: analysis of the ARTIST phase III trial. Radiother Oncol. 2020;152:19–25.

    Article  CAS  PubMed  Google Scholar 

  23. Huang DD, Cai HY, Chen XY, Dong WX, Wangchuk D, Yan JY, et al. Value of sarcopenia defined by the new EWGSOP2 consensus for the prediction of postoperative complications and long-term survival after radical gastrectomy for gastric cancer: a comparison with four common nutritional screening tools. J Cancer. 2020;11(19):5852–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Sun X, Xu J, Chen X, Zhang W, Chen W, Zhu C, et al. Sarcopenia in patients with normal body mass index is an independent predictor for postoperative complication and long-term survival in gastric cancer. Clin Transl Sci. 2021;14(3):837–46.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Huang DD, Cai HY, Wang WB, Song HN, Luo X, Dong WX, et al. Measurement of muscle quantity/quality has additional predictive value for postoperative complications and long-term survival after gastrectomy for gastric cancer in patients with probable sarcopenia as defined by the new EWGSOP2 consensus: Analysis from a large-scale prospective study. Nutrition. 2021;86: 111156.

    Article  PubMed  Google Scholar 

  26. Wu WY, Dong JJ, Huang XC, Chen ZJ, Chen XL, Dong QT, et al. AWGS2019 vs EWGSOP2 for diagnosing sarcopenia to predict long-term prognosis in Chinese patients with gastric cancer after radical gastrectomy. World J Clin Cases. 2021;9(18):4668–80.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Tamandl D, Paireder M, Asari R, Baltzer PA, Schoppmann SF, Ba-Ssalamah A. Markers of sarcopenia quantified by computed tomography predict adverse long-term outcome in patients with resected oesophageal or gastro-oesophageal junction cancer. Eur Radiol. 2016;26(5):1359–67.

    Article  PubMed  Google Scholar 

  28. Nishigori T, Tsunoda S, Okabe H, Tanaka E, Hisamori S, Hosogi H, et al. Impact of sarcopenic obesity on surgical site infection after laparoscopic total gastrectomy. Ann Surg Oncol. 2016;23(Suppl 4):524–31.

    Article  PubMed  Google Scholar 

  29. Kudou K, Saeki H, Nakashima Y, Edahiro K, Korehisa S, Taniguchi D, et al. Prognostic significance of sarcopenia in patients with esophagogastric junction cancer or upper gastric cancer. Ann Surg Oncol. 2017;24(7):1804–10.

    Article  PubMed  Google Scholar 

  30. Zheng ZF, Lu J, Zheng CH, Li P, Xie JW, Wang JB, et al. A novel prognostic scoring system based on preoperative sarcopenia predicts the long-term outcome for patients after R0 resection for gastric cancer: experiences of a high-volume center. Ann Surg Oncol. 2017;24(7):1795–803.

    Article  PubMed  Google Scholar 

  31. Kuwada K, Kuroda S, Kikuchi S, Yoshida R, Nishizaki M, Kagawa S, et al. Sarcopenia and comorbidity in gastric cancer surgery as a useful combined factor to predict eventual death from other causes. Ann Surg Oncol. 2018;25(5):1160–6.

    Article  PubMed  PubMed Central  Google Scholar 

  32. O’Brien S, Twomey M, Moloney F, Kavanagh RG, Carey BW, Power D, et al. Sarcopenia and post-operative morbidity and mortality in patients with gastric cancer. J Gastric Cancer. 2018;18(3):242–52.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Beuran M, Tache C, Ciubotaru C, Vartic M, Hostiuc S, Prodan A, et al. Sarcopenia is a predictive factor for postoperative morbidity and mortality in patients having radical gastrectomy for cancer. Chirurgia (Bucur). 2018;113(5):678–86.

    Article  PubMed  Google Scholar 

  34. Tamura T, Sakurai K, Nambara M, Miki Y, Toyokawa T, Kubo N, et al. Adverse effects of preoperative sarcopenia on postoperative complications of patients with gastric cancer. Anticancer Res. 2019;39(2):987–92.

    Article  CAS  PubMed  Google Scholar 

  35. Lin JX, Lin JP, Xie JW, Wang JB, Lu J, Chen QY, et al. Prognostic value and association of sarcopenia and systemic inflammation for patients with gastric cancer following radical gastrectomy. Oncologist. 2019;24(11):e1091–101.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Sierzega M, Chrzan R, Wiktorowicz M, Kolodziejczyk P, Richter P. Prognostic and predictive implications of sarcopenia in Western patients undergoing gastric resections for carcinoma of the stomach. J Surg Oncol. 2019;120(3):473–82.

    Article  PubMed  Google Scholar 

  37. Wang JB, Xue Z, Lu J, He QL, Zheng ZF, Xu BB, et al. Effect of sarcopenia on short- and long-term outcomes in patients with gastric neuroendocrine neoplasms after radical gastrectomy: results from a large, two-institution series. BMC Cancer. 2020;20(1):1002.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Kim EY, Jun KH, Kim SY, Chin HM. Body mass index and skeletal muscle index are useful prognostic factors for overall survival after gastrectomy for gastric cancer: retrospective cohort study. Medicine (Baltimore). 2020;99(47): e23363.

    Article  PubMed  Google Scholar 

  39. Olmez T, Gulmez S, Karakose E, Ofluoglu CB, Senger AS, Bozkurt H, et al. Relation between sarcopenia and surgical site infection in patients undergoing gastric cancer surgery. Surg Infect (Larchmt). 2021;22(5):551–5.

    Article  PubMed  Google Scholar 

  40. •• Lee JK, Park YS, Lee K, Youn SI, Won Y, Min SH, et al. Prognostic significance of surgery-induced sarcopenia in the survival of gastric cancer patients: a sex-specific analysis. J Cachexia Sarcopenia Muscle. 2021;12(6):1897–907. A retrospective cohort analysis of the effects of postoperative muscle loss and surgery-induced sarcopenia on the prognosis of patients with gastric cancer.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Takahashi S, Shimizu S, Nagai S, Watanabe H, Nishitani Y, Kurisu Y. Characteristics of sarcopenia after distal gastrectomy in elderly patients. PLoS ONE. 2019;14(9): e0222412.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Matsunaga T, Satio H, Miyauchi W, Shishido Y, Miyatani K, Murakami Y, et al. Impact of skeletal muscle mass in patients with recurrent gastric cancer. World J Surg Oncol. 2021;19(1):170.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Kouzu K, Tsujimoto H, Sugasawa H, Ishibashi Y, Itazaki Y, Tsuchiya S, et al. Impact of postoperative reduced skeletal muscle on prognosis after recurrence in gastric cancer. Mol Clin Oncol. 2021;14(1):3.

    PubMed  Google Scholar 

  44. Kudou K, Saeki H, Nakashima Y, Sasaki S, Jogo T, Hirose K, et al. Postoperative development of sarcopenia is a strong predictor of a poor prognosis in patients with adenocarcinoma of the esophagogastric junction and upper gastric cancer. Am J Surg. 2019;217(4):757–63.

    Article  PubMed  Google Scholar 

  45. Lee C, Park IJ, Kim KW, Shin Y, Lim SB, Kim CW, et al. Influence of postoperative changes in sarcopenia on long-term survival in non-metastatic colorectal cancer patients. Cancers (Basel). 2021;13(10):2410.

    Article  PubMed  PubMed Central  Google Scholar 

  46. 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):203–4.

    Article  PubMed  Google Scholar 

  47. Yamaoka Y, Fujitani K, Tsujinaka T, Yamamoto K, Hirao M, Sekimoto M. Skeletal muscle loss after total gastrectomy, exacerbated by adjuvant chemotherapy. Gastric Cancer. 2015;18(2):382–9.

    Article  CAS  PubMed  Google Scholar 

  48. Rinninella E, Strippoli A, Cintoni M, Raoul P, Vivolo R, Di Salvatore M, et al. Body composition changes in gastric cancer patients during preoperative FLOT therapy: preliminary results of an Italian cohort study. Nutrients. 2021;13(3):960.

  49. VanderVeen BN, Cardaci TD, Madero SS, McDonald SJ, Bullard BM, Price RL, et al. 5-Fluorouracil disrupts skeletal muscle immune cells and impairs skeletal muscle repair and remodeling. J Appl Physiol (1985). 2022;133(4):834–49.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. 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.

    Article  CAS  PubMed  Google Scholar 

  51. Jang MK, Park S, Park C, Doorenbos AZ, Go J, Kim S. Does neoadjuvant chemotherapy regimen affect sarcopenia status in patients with breast cancer? Breast. 2022;66:1–7.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Gorini S, De Angelis A, Berrino L, Malara N, Rosano G, Ferraro E. Chemotherapeutic drugs and mitochondrial dysfunction: focus on doxorubicin, trastuzumab, and sunitinib. Oxid Med Cell Longev. 2018;2018:7582730.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Moryoussef F, Dhooge M, Volet J, Barbe C, Brezault C, Hoeffel C, et al. Reversible sarcopenia in patients with gastrointestinal stromal tumor treated with imatinib. J Cachexia Sarcopenia Muscle. 2015;6(4):343–50.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Quan-Jun Y, Yan H, Yong-Long H, Li-Li W, Jie L, Jin-Lu H, et al. Selumetinib attenuates skeletal muscle wasting in murine cachexia model through ERK inhibition and AKT activation. Mol Cancer Ther. 2017;16(2):334–43.

    Article  PubMed  Google Scholar 

  55. Pamoukdjian F, Bouillet T, Lévy 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 

  56. Botsen D, Ordan MA, Barbe C, Mazza C, Perrier M, Moreau J, et al. Dynapenia could predict chemotherapy-induced dose-limiting neurotoxicity in digestive cancer patients. BMC Cancer. 2018;18(1):955.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Tan BH, Brammer K, Randhawa N, Welch NT, Parsons SL, James EJ, et al. Sarcopenia is associated with toxicity in patients undergoing neo-adjuvant chemotherapy for oesophago-gastric cancer. Eur J Surg Oncol. 2015;41(3):333–8.

    Article  CAS  PubMed  Google Scholar 

  58. Matsunaga T, Saito H, Miyauchi W, Shishido Y, Miyatani K, Morimoto M, et al. Impact of skeletal muscle mass in patients with unresectable gastric cancer who received palliative first-line chemotherapy based on 5-fluorouracil. BMC Cancer. 2021;21(1):1219.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Hashimoto T, Kurokawa Y, Takahashi T, Saito T, Yamashita K, Tanaka K, et al. What is the most useful body composition parameter for predicting toxicities of preoperative chemotherapy for gastric cancer? Surg Today. 2020;50(5):509–15.

    Article  CAS  PubMed  Google Scholar 

  60. Kano M, Hihara J, Tokumoto N, Kohashi T, Hara T, Shimbara K, 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):523–31.

    Article  CAS  PubMed  Google Scholar 

  61. •• Takenaka Y, Oya R, Takemoto N, Inohara H. Predictive impact of sarcopenia in solid cancers treated with immune checkpoint inhibitors: a meta-analysis. J Cachexia Sarcopenia Muscle. 2021;12(5):1122–35. This meta-analysis demonstrated a negative correlation between sarcopenia and efficacy of immune checkpoint inhibitors.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Kim YY, Lee J, Jeong WK, Kim ST, Kim JH, Hong JY, et al. Prognostic significance of sarcopenia in microsatellite-stable gastric cancer patients treated with programmed death-1 inhibitors. Gastric Cancer. 2021;24(2):457–66.

    Article  CAS  PubMed  Google Scholar 

  63. Mirkin KA, Luke FE, Gangi A, Pimiento JM, Jeong D, Hollenbeak CS, et al. Sarcopenia related to neoadjuvant chemotherapy and perioperative outcomes in resected gastric cancer: a multi-institutional analysis. J Gastrointest Oncol. 2017;8(3):589–95.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Lee JS, Kim YS, Kim EY, Jin W. Prognostic significance of CT-determined sarcopenia in patients with advanced gastric cancer. PLoS ONE. 2018;13(8): e0202700.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Sugiyama K, Narita Y, Mitani S, Honda K, Masuishi T, Taniguchi H, et al. Baseline sarcopenia and skeletal muscle loss during chemotherapy affect survival outcomes in metastatic gastric cancer. Anticancer Res. 2018;38(10):5859–66.

    Article  CAS  PubMed  Google Scholar 

  66. Matsuura N, Motoori M, Fujitani K, Nishizawa Y, Komatsu H, Miyazaki Y, et al. Correlation between skeletal muscle mass and adverse events of neoadjuvant chemotherapy in patients with gastric cancer. Oncology. 2020;98(1):29–34.

    Article  PubMed  Google Scholar 

  67. Cruz-Jentoft AJ, Kiesswetter E, Drey M, Sieber CC. Nutrition, frailty, and sarcopenia. Aging Clin Exp Res. 2017;29(1):43–8.

    Article  PubMed  Google Scholar 

  68. Gonçalves EM, Salomão EM, Gomes-Marcondes MC. Leucine modulates the effect of Walker factor, a proteolysis-inducing factor-like protein from Walker tumours, on gene expression and cellular activity in C2C12 myotubes. Cytokine. 2013;64(1):343–50.

    Article  PubMed  Google Scholar 

  69. Ma DW, Cho Y, Jeon MJ, Kim JH, Lee IJ, Youn YH, et al. Relationship between sarcopenia and prognosis in patient with concurrent chemo-radiation therapy for esophageal cancer. Front Oncol. 2019;9:366.

    Article  PubMed  PubMed Central  Google Scholar 

  70. Hyatt H, Deminice R, Yoshihara T, Powers SK. Mitochondrial dysfunction induces muscle atrophy during prolonged inactivity: a review of the causes and effects. Arch Biochem Biophys. 2019;662:49–60.

    Article  CAS  PubMed  Google Scholar 

  71. Kortebein P, Ferrando A, Lombeida J, Wolfe R, Evans WJ. Effect of 10 days of bed rest on skeletal muscle in healthy older adults. JAMA. 2007;297(16):1772–4.

    Article  CAS  PubMed  Google Scholar 

  72. Abrigo J, Simon F, Cabrera D, Vilos C, Cabello-Verrugio C. Mitochondrial dysfunction in skeletal muscle pathologies. Curr Protein Pept Sci. 2019;20(6):536–46.

    Article  CAS  PubMed  Google Scholar 

  73. Julienne CM, Dumas JF, Goupille C, Pinault M, Berri C, Collin A, et al. Cancer cachexia is associated with a decrease in skeletal muscle mitochondrial oxidative capacities without alteration of ATP production efficiency. J Cachexia Sarcopenia Muscle. 2012;3(4):265–75.

    Article  PubMed  PubMed Central  Google Scholar 

  74. • Zhang Y, Wang J, Wang X, Gao T, Tian H, Zhou D, et al. The autophagic-lysosomal and ubiquitin proteasome systems are simultaneously activated in the skeletal muscle of gastric cancer patients with cachexia. Am J Clin Nutr. 2020;111(3):570–9. The autophagic-lysosomal and ubiquitin proteasome systems of muscle cells are simultaneously activated in rectus abdominis muscle biopsy specimens of gastric cancer patients.

    Article  PubMed  Google Scholar 

  75. Oflazoglu U, Alacacioglu A, Varol U, Kucukzeybek Y, Salman T, Onal HT, et al. The role of inflammation in adjuvant chemotherapy-induced sarcopenia (Izmir Oncology Group (IZOG) study). Support Care Cancer. 2020;28(8):3965–77.

    Article  PubMed  Google Scholar 

  76. White JP, Puppa MJ, Sato S, Gao S, Price RL, Baynes JW, et al. IL-6 regulation on skeletal muscle mitochondrial remodeling during cancer cachexia in the ApcMin/+ mouse. Skelet Muscle. 2012;2:14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Bozzetti F. Chemotherapy-induced Sarcopenia. Curr Treat Options Oncol. 2020;21(1):7.

    Article  PubMed  Google Scholar 

  78. Chen JA, Splenser A, Guillory B, Luo J, Mendiratta M, Belinova B, et al. Ghrelin prevents tumour- and cisplatin-induced muscle wasting: characterization of multiple mechanisms involved. J Cachexia Sarcopenia Muscle. 2015;6(2):132–43.

    Article  PubMed  PubMed Central  Google Scholar 

  79. Chen JL, Colgan TD, Walton KL, Gregorevic P, Harrison CA. The TGF-β signalling network in muscle development, adaptation and disease. Adv Exp Med Biol. 2016;900:97–131.

    Article  CAS  PubMed  Google Scholar 

  80. Barreto R, Waning DL, Gao H, Liu Y, Zimmers TA, Bonetto A. Chemotherapy-related cachexia is associated with mitochondrial depletion and the activation of ERK1/2 and p38 MAPKs. Oncotarget. 2016;7(28):43442–60.

    Article  PubMed  PubMed Central  Google Scholar 

  81. Machlowska J, Baj J, Sitarz M, Maciejewski R, Sitarz R. Gastric cancer: epidemiology, risk factors, classification, genomic characteristics and treatment strategies. Int J Mol Sci. 2020;21(11):4012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Gungor O, Ulu S, Hasbal NB, Anker SD, Kalantar-Zadeh K. Effects of hormonal changes on sarcopenia in chronic kidney disease: where are we now and what can we do? J Cachexia Sarcopenia Muscle. 2021;12(6):1380–92.

    Article  PubMed  PubMed Central  Google Scholar 

  83. Giresi PG, Stevenson EJ, Theilhaber J, Koncarevic A, Parkington J, Fielding RA, et al. Identification of a molecular signature of sarcopenia. Physiol Genomics. 2005;21(2):253–63.

    Article  CAS  PubMed  Google Scholar 

  84. Zhou D, Zhang Y, Mamtawla G, Wan S, Gao X, Zhang L, et al. Iron overload is related to muscle wasting in patients with cachexia of gastric cancer: using quantitative proteome analysis. Med Oncol. 2020;37(12):113.

    Article  CAS  PubMed  Google Scholar 

  85. • Huang Y, Wu B, Shen D, Chen J, Yu Z, Chen C. Ferroptosis in a sarcopenia model of senescence accelerated mouse prone 8 (SAMP8). Int J Biol Sci. 2021;17(1):151–62. The study revealed the iron-p53-SLC7A11 signaling pathway for ferroptosis in sarcopenia.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Uchida T, Sekine R, Matsuo K, Kigawa G, Umemoto T, Tanaka K. Benefit of laparoscopic compared to standard open gastric cancer surgery for sarcopenic patients: a propensity score-matching analysis. Surg Endosc. 2022;36(12):9244–53.

    Article  PubMed  Google Scholar 

  87. Yamada M, Nishiguchi S, Fukutani N, Aoyama T, Arai H. Mail-Based intervention for sarcopenia prevention increased anabolic hormone and skeletal muscle mass in community-dwelling Japanese older adults: the INE (Intervention by nutrition and exercise) study. J Am Med Dir Assoc. 2015;16(8):654–60.

    Article  PubMed  Google Scholar 

  88. Aoyama T, Nakazono M, Nagasawa S, Segami K. Clinical impact of a perioperative exercise program for sarcopenia and overweight/obesity gastric cancer. In Vivo. 2021;35(2):707–12.

    Article  PubMed  PubMed Central  Google Scholar 

  89. Yamamoto K, Nagatsuma Y, Fukuda Y, Hirao M, Nishikawa K, Miyamoto A, et al. Effectiveness of a preoperative exercise and nutritional support program for elderly sarcopenic patients with gastric cancer. Gastric Cancer. 2017;20(5):913–8.

    Article  PubMed  Google Scholar 

  90. Dieli-Conwright CM, Courneya KS, Demark-Wahnefried W, Sami N, Lee K, Buchanan TA, et al. Effects of aerobic and resistance exercise on metabolic syndrome, sarcopenic obesity, and circulating biomarkers in overweight or obese survivors of breast cancer: a randomized controlled trial. J Clin Oncol. 2018;36(9):875–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. D’Amico D, Andreux PA, Valdés P, Singh A, Rinsch C, Auwerx J. Impact of the natural compound urolithin a on health, disease, and aging. Trends Mol Med. 2021;27(7):687–99.

    Article  CAS  PubMed  Google Scholar 

  92. Chang YC, Chen YT, Liu HW, Chan YC, Liu MY, Hu SH, et al. Oligonol alleviates sarcopenia by regulation of signaling pathways involved in protein turnover and mitochondrial quality. Mol Nutr Food Res. 2019;63(10): e1801102.

    Article  PubMed  Google Scholar 

  93. Gutierrez-Salmean G, Ciaraldi TP, Nogueira L, Barboza J, Taub PR, Hogan MC, et al. Effects of (-)-epicatechin on molecular modulators of skeletal muscle growth and differentiation. J Nutr Biochem. 2014;25(1):91–4.

    Article  CAS  PubMed  Google Scholar 

  94. Mori H, Tokuda Y. Effect of whey protein supplementation after resistance exercise on the muscle mass and physical function of healthy older women: a randomized controlled trial. Geriatr Gerontol Int. 2018;18(9):1398–404.

    Article  PubMed  Google Scholar 

  95. Takeuchi I, Yoshimura Y, Shimazu S, Jeong S, Yamaga M, Koga H. Effects of branched-chain amino acids and vitamin D supplementation on physical function, muscle mass and strength, and nutritional status in sarcopenic older adults undergoing hospital-based rehabilitation: a multicenter randomized controlled trial. Geriatr Gerontol Int. 2019;19(1):12–7.

    Article  PubMed  Google Scholar 

  96. Bauer JM, Verlaan S, Bautmans I, Brandt K, Donini LM, Maggio M, et al. Effects of a vitamin D and leucine-enriched whey protein nutritional supplement on measures of sarcopenia in older adults, the PROVIDE study: a randomized, double-blind, placebo-controlled trial. J Am Med Dir Assoc. 2015;16(9):740–7.

    Article  PubMed  Google Scholar 

  97. El Hajj C, Fares S, Chardigny JM, Boirie Y, Walrand S. Vitamin D supplementation and muscle strength in pre-sarcopenic elderly Lebanese people: a randomized controlled trial. Arch Osteoporos. 2018;14(1):4.

    Article  PubMed  Google Scholar 

  98. Smith GI, Atherton P, Reeds DN, Mohammed BS, Rankin D, Rennie MJ, et al. Dietary omega-3 fatty acid supplementation increases the rate of muscle protein synthesis in older adults: a randomized controlled trial. Am J Clin Nutr. 2011;93(2):402–12.

    Article  CAS  PubMed  Google Scholar 

  99. Smith GI, Julliand S, Reeds DN, Sinacore DR, Klein S, Mittendorfer B. Fish oil-derived n-3 PUFA therapy increases muscle mass and function in healthy older adults. Am J Clin Nutr. 2015;102(1):115–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Morley JE, Argiles JM, Evans WJ, Bhasin S, Cella D, Deutz NE, et al. Nutritional recommendations for the management of sarcopenia. J Am Med Dir Assoc. 2010;11(6):391–6.

    Article  PubMed  PubMed Central  Google Scholar 

  101. Rieu I, Balage M, Sornet C, Giraudet C, Pujos E, Grizard J, et al. Leucine supplementation improves muscle protein synthesis in elderly men independently of hyperaminoacidaemia. J Physiol. 2006;575(Pt 1):305–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Meng Q, Tan S, Jiang Y, Han J, Xi Q, Zhuang Q, et al. Post-discharge oral nutritional supplements with dietary advice in patients at nutritional risk after surgery for gastric cancer: a randomized clinical trial. Clin Nutr. 2021;40(1):40–6.

    Article  CAS  PubMed  Google Scholar 

  103. Urban RJ, Dillon EL, Choudhary S, Zhao Y, Horstman AM, Tilton RG, et al. Translational studies in older men using testosterone to treat sarcopenia. Trans Am Clin Climatol Assoc. 2014;125:27–44.

    PubMed  PubMed Central  Google Scholar 

  104. Tanner SB, Harwell SA. More than healthy bones: a review of vitamin D in muscle health. Ther Adv Musculoskelet Dis. 2015;7(4):152–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Rejnmark L. Effects of vitamin d on muscle function and performance: a review of evidence from randomized controlled trials. Ther Adv Chronic Dis. 2011;2(1):25–37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Colldén G, Tschöp MH, Müller TD. Therapeutic potential of targeting the ghrelin pathway. Int J Mol Sci. 2017;18(4):798.

    Article  PubMed  PubMed Central  Google Scholar 

  107. •• Miyake M, Hori S, Itami Y, Oda Y, Owari T, Fujii T, et al. Supplementary oral anamorelin mitigates anorexia and skeletal muscle atrophy induced by gemcitabine plus cisplatin systemic chemotherapy in a mouse model. Cancers (Basel). 2020;12(7):1942. An animal experiment to search for potential preventive interventions for chemotherapy-induced adverse effects.

  108. Walton RG, Dungan CM, Long DE, Tuggle SC, Kosmac K, Peck BD, et al. Metformin blunts muscle hypertrophy in response to progressive resistance exercise training in older adults: a randomized, double-blind, placebo-controlled, multicenter trial: the MASTERS trial. Aging Cell. 2019;18(6): e13039.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Pilmark NS, Oberholzer L, Halling JF, Kristensen JM, Bønding CP, Elkjær I, et al. Skeletal muscle adaptations to exercise are not influenced by metformin treatment in humans: secondary analyses of 2 randomized, clinical trials. Appl Physiol Nutr Metab. 2022;47(3):309–20.

    Article  CAS  PubMed  Google Scholar 

  110. Adams SC, Segal RJ, McKenzie DC, Vallerand JR, Morielli AR, Mackey JR, et al. Impact of resistance and aerobic exercise on sarcopenia and dynapenia in breast cancer patients receiving adjuvant chemotherapy: a multicenter randomized controlled trial. Breast Cancer Res Treat. 2016;158(3):497–507.

    Article  CAS  PubMed  Google Scholar 

  111. Mazzuca F, Roberto M, Arrivi G, Sarfati E, Schipilliti FM, Crimini E, et al. Clinical impact of highly purified, whey proteins in patients affected with colorectal cancer undergoing chemotherapy: preliminary results of a placebo-controlled study. Integr Cancer Ther. 2019;18:1534735419866920.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. 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  PubMed  Google Scholar 

  113. Moug SJ, Barry SJE, Maguire S, Johns N, Dolan D, Steele RJC, et al. Does prehabilitation modify muscle mass in patients with rectal cancer undergoing neoadjuvant therapy? A subanalysis from the REx randomised controlled trial. Tech Coloproctol. 2020;24(9):959–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. •• Tan S, Meng Q, Jiang Y, Zhuang Q, Xi Q, Xu J, et al. Impact of oral nutritional supplements in post-discharge patients at nutritional risk following colorectal cancer surgery: a randomised clinical trial. Clin Nutr. 2021;40(1):47–53. ()

    Article  CAS  PubMed  Google Scholar 

  115. Kim EY, Kim K, Kim YS, Ahn HK, Jeong YM, Kim JH, et al. Prevalence of and factors associated with sarcopenia in Korean cancer survivors: based on data obtained by the Korea National Health and Nutrition Examination Survey (KNHANES) 2008–2011. Nutr Cancer. 2017;69(3):394–401.

    Article  PubMed  Google Scholar 

  116. Miyoshi K, Shimoda M, Udo R, Oshiro Y, Suzuki S. Urinary titin N-terminal fragment concentration is an indicator of preoperative sarcopenia and nutritional status in patients with gastrointestinal tract and hepatobiliary pancreatic malignancies. Nutrition. 2020;79–80: 110957.

    Article  PubMed  Google Scholar 

  117. Lin J, Zhang W, Huang Y, Chen W, Wu R, Chen X, et al. Sarcopenia is associated with the neutrophil/lymphocyte and platelet/lymphocyte ratios in operable gastric cancer patients: a prospective study. Cancer Manag Res. 2018;10:4935–44.

    Article  PubMed  PubMed Central  Google Scholar 

  118. Fielding RA, Vellas B, Evans WJ, Bhasin S, Morley JE, Newman AB, et al. Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J Am Med Dir Assoc. 2011;12(4):249–56.

    Article  PubMed  Google Scholar 

  119. Beaudart C, McCloskey E, Bruyère O, Cesari M, Rolland Y, Rizzoli R, et al. Sarcopenia in daily practice: assessment and management. BMC Geriatr. 2016;16(1):170.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pharmacy, Xiangya Hospital, Central South University, Changsha, 410008, China

    Kaiqiang Xie MMed, Tingyu Zhao MMed, Ting Liu MMed & Mimi Tang MD

  2. National Clinical Research Center for Geriatric Disorders, Xiangya Hospital, Central South University, Changsha, 410008, Hunan, China

    Kaiqiang Xie MMed, Tingyu Zhao MMed, Ting Liu MMed & Mimi Tang MD

  3. The Hunan Institute of Pharmacy Practice and Clinical Research, Changsha, 410008, China

    Kaiqiang Xie MMed, Tingyu Zhao MMed, Ting Liu MMed & Mimi Tang MD

  4. Institute of Hospital Pharmacy, Central South University, Changsha, 410008, China

    Kaiqiang Xie MMed, Tingyu Zhao MMed, Ting Liu MMed & Mimi Tang MD

  5. Xiangya School of Pharmaceutical Sciences, Central South University, Changsha, 410008, China

    Danling He BMed

Authors
  1. Kaiqiang Xie MMed
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Danling He BMed
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tingyu Zhao MMed
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ting Liu MMed
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mimi Tang MD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mimi Tang MD.

Ethics declarations

Conflict of Interest

The authors declare no competing interests.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Kaiqiang Xie is the first author.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xie, K., He, D., Zhao, T. et al. Gastric Cancer with Sarcopenia: an Area Worth Focusing On. Curr. Treat. Options in Oncol. 24, 1305–1327 (2023). https://doi.org/10.1007/s11864-023-01122-y

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11864-023-01122-y

Keywords

Search

Navigation