CT-based muscle and adipose measurements predict prognosis in patients with digestive system malignancy.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
06 06 2024
Historique:
received: 02 02 2024
accepted: 03 06 2024
medline: 7 6 2024
pubmed: 7 6 2024
entrez: 6 6 2024
Statut: epublish

Résumé

The role of skeletal muscle and adipose tissue in the progression of cancer has been gradually discussed, but it needs further exploration. The objective of this study was to provide an in-depth analysis of skeletal muscle and fat in digestive malignancies and to construct novel predictors for clinical management. This is a retrospective study that includes data from Cancer Center, the First Hospital of Jilin University. Basic characteristic information was analyzed by T tests. Correlation matrices were drawn to explore the relationship between CT-related indicators and other indicators. Cox risk regression analyses were performed to analyze the association between the overall survivals (OS) and various types of indicators. A new indicator body composition score (BCS) was then created and a time-dependent receiver operating characteristic curve was plotted to analyze the efficacy of the BCS. Finally, a nomogram was produced to develop a scored-CT system based on BCS and other indicators. C-index and calibration curve analyses were performed to validate the predictive accuracy of the scored-CT system. A total of 575 participants were enrolled in the study. Cox risk regression model revealed that VFD, L3 SMI and VFA/SFA were associated with prognosis of cancer patients. After adjustment, BCS index based on CT was significantly associated with prognosis, both in all study population and in subgroup analysis according to tumor types (all study population: HR 2.036, P < 0.001; colorectal cancer: HR 2.693, P < 0.001; hepatocellular carcinoma: HR 4.863, P < 0.001; esophageal cancer: HR 4.431, P = 0.008; pancreatic cancer: HR 1.905, P = 0.016; biliary system malignancies: HR 23.829, P = 0.035). The scored-CT system was constructed according to tumor type, stage, KPS, PG-SGA and BCS index, and it was of great predictive validity. This study identified VFD, L3 SMI and VFA/SFA associated with digestive malignancies outcomes. BCS was created and the scored-CT system was established to predict the OS of cancer patients.

Identifiants

pubmed: 38844600
doi: 10.1038/s41598-024-63806-1
pii: 10.1038/s41598-024-63806-1
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

13036

Subventions

Organisme : National Key R&amp;D Program of China
ID : 2016YFC1303804

Informations de copyright

© 2024. The Author(s).

Références

Sung, H. et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 71(3), 209–249 (2021).
pubmed: 33538338 doi: 10.3322/caac.21660
Song, M., Garrett, W. S. & Chan, A. T. Nutrients, foods, and colorectal cancer prevention. Gastroenterology 148(6), 1244–60 e16 (2015).
pubmed: 25575572 doi: 10.1053/j.gastro.2014.12.035
Anand, P. et al. Cancer is a preventable disease that requires major lifestyle changes. Pharm Res 25(9), 2097–2116 (2008).
pubmed: 18626751 pmcid: 2515569 doi: 10.1007/s11095-008-9661-9
Matrone, A. et al. Potential impact of BMI on the aggressiveness of presentation and clinical outcome of differentiated thyroid cancer. J. Clin. Endocrinol. Metab. 105(4), e1124–e1134 (2020).
doi: 10.1210/clinem/dgz312
Cantini, L. et al. Body mass index and hormone receptor status influence recurrence risk in HER2-positive early breast cancer patients. Clin. Breast Cancer 20(1), e89–e98 (2020).
pubmed: 31378534 doi: 10.1016/j.clbc.2019.06.008
Greenlee, H. et al. Association between body mass index and cancer survival in a pooled analysis of 22 clinical trials. Cancer Epidemiol. Biomark. Prev. 26(1), 21–29 (2017).
doi: 10.1158/1055-9965.EPI-15-1336
Cruz-Jentoft, A. J. et al. Sarcopenia: Revised European consensus on definition and diagnosis. Age Ageing 48(4), 601 (2019).
pubmed: 31081853 pmcid: 6593317 doi: 10.1093/ageing/afz046
Kim, J. M. et al. Impact of subcutaneous and visceral fat adiposity in patients with colorectal cancer. Clin. Nutr. 40(11), 5631–5638 (2021).
pubmed: 34662848 doi: 10.1016/j.clnu.2021.10.001
Lee, J. S. et al. Subcutaneous fat distribution is a prognostic biomarker for men with castration resistant prostate cancer. J. Urol. 200(1), 114–120 (2018).
pubmed: 29366641 doi: 10.1016/j.juro.2018.01.069
Wada, M. et al. Visceral-to-subcutaneous fat ratio is a possible prognostic factor for type 1 endometrial cancer. Int. J. Clin. Oncol. 27(2), 434–440 (2022).
pubmed: 34716844 doi: 10.1007/s10147-021-02060-1
Fischer, A. et al. Prevalence of low muscle mass in the computed tomography at the third lumbar vertebra level depends on chosen cut-off in 200 hospitalised patients: A prospective observational trial. Nutrients 14(16), 3446 (2022).
pubmed: 36014952 pmcid: 9413680 doi: 10.3390/nu14163446
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. 56(8), 779–785 (2002).
pubmed: 12122555 doi: 10.1038/sj.ejcn.1601412
Brundage, M. et al. Patterns of reporting health-related quality of life outcomes in randomized clinical trials: Implications for clinicians and quality of life researchers. Qual. Life Res. 20(5), 653–664 (2011).
pubmed: 21110123 doi: 10.1007/s11136-010-9793-3
Kang, Z. et al. Correlation between L3 skeletal muscle index and prognosis of patients with stage IV gastric cancer. J. Gastrointest. Oncol. 12(5), 2073–2081 (2021).
pubmed: 34790375 pmcid: 8576239 doi: 10.21037/jgo-21-556
Kim, H. K. et al. Age-related changes in muscle quality and development of diagnostic cutoff points for myosteatosis in lumbar skeletal muscles measured by CT scan. Clin. Nutr. 40(6), 4022–4028 (2021).
pubmed: 34144412 doi: 10.1016/j.clnu.2021.04.017
Aubrey, J. et al. Measurement of skeletal muscle radiation attenuation and basis of its biological variation. Acta Physiol. (Oxf.) 210(3), 489–497 (2014).
pubmed: 24393306 doi: 10.1111/apha.12224
Martin, L. et al. Assessment of computed tomography (CT)-defined muscle and adipose tissue features in relation to short-term outcomes after elective surgery for colorectal cancer: A multicenter approach. Ann. Surg. Oncol. 25(9), 2669–2680 (2018).
pubmed: 30006691 doi: 10.1245/s10434-018-6652-x
Camp, R. L., Dolled-Filhart, M. & Rimm, D. L. X-tile: A new bio-informatics tool for biomarker assessment and outcome-based cut-point optimization. Clin. Cancer Res. 10(21), 7252–7259 (2004).
pubmed: 15534099 doi: 10.1158/1078-0432.CCR-04-0713
Hagens, E. R. C. et al. Influence of body composition and muscle strength on outcomes after multimodal oesophageal cancer treatment. J. Cachexia Sarcopenia Muscle 11(3), 756–767 (2020).
pubmed: 32096923 pmcid: 7296271 doi: 10.1002/jcsm.12540
Zhang, Y. et al. Impact of body composition on clinical outcomes in people with gastric cancer undergoing radical gastrectomy after neoadjuvant treatment. Nutrition 85, 111135 (2021).
pubmed: 33556785 doi: 10.1016/j.nut.2020.111135
Blüher, M. Metabolically healthy obesity. Endocr. Rev. 41(3), bnaa004 (2020).
pubmed: 32128581 pmcid: 7098708 doi: 10.1210/endrev/bnaa004
Baracos, V. E. & Arribas, L. Sarcopenic obesity: Hidden muscle wasting and its impact for survival and complications of cancer therapy. Ann. Oncol. 29, ii1–ii9 (2018).
pubmed: 29506228 doi: 10.1093/annonc/mdx810
Looijaard, S. et al. Pathophysiological mechanisms explaining poor clinical outcome of older cancer patients with low skeletal muscle mass. Acta Physiol. (Oxf.) 231(1), e13516 (2021).
pubmed: 32478975 doi: 10.1111/apha.13516
Bichels, A. V. et al. Muscle mass assessed by computed tomography at the third lumbar vertebra predicts patient survival in chronic kidney disease. J. Ren. Nutr. 31(4), 342–350 (2021).
pubmed: 33257228 doi: 10.1053/j.jrn.2020.05.007
Liu, X. et al. The correlation between skeletal muscle index of the L3 vertebral body and malnutrition in patients with advanced lung cancer. BMC Cancer 21(1), 1148 (2021).
pubmed: 34702196 pmcid: 8549206 doi: 10.1186/s12885-021-08876-4
Argiles, J. M. et al. Cancer cachexia: Understanding the molecular basis. Nat. Rev. Cancer 14(11), 754–762 (2014).
pubmed: 25291291 doi: 10.1038/nrc3829
Wendrich, A. W. et al. Low skeletal muscle mass is a predictive factor for chemotherapy dose-limiting toxicity in patients with locally advanced head and neck cancer. Oral Oncol. 71, 26–33 (2017).
pubmed: 28688687 doi: 10.1016/j.oraloncology.2017.05.012
Zhuang, C. L. 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) 95(13), e3164 (2016).
pubmed: 27043677 doi: 10.1097/MD.0000000000003164
Chen, F. et al. Impact of preoperative sarcopenia on postoperative complications and prognosis of gastric cancer resection: A meta-analysis of cohort studies. Arch. Gerontol. Geriatr. 98, 104534 (2022).
pubmed: 34601314 doi: 10.1016/j.archger.2021.104534
Halvorsen, T. O. et al. Associations between muscle measures, survival, and toxicity in patients with limited stage small cell lung cancer. J. Cachexia Sarcopenia Muscle 11(5), 1283–1290 (2020).
pubmed: 32725772 pmcid: 7567150 doi: 10.1002/jcsm.12583
Park, J. et al. Obesity and cancer–mechanisms underlying tumour progression and recurrence. Nat. Rev. Endocrinol. 10(8), 455–465 (2014).
pubmed: 24935119 pmcid: 4374431 doi: 10.1038/nrendo.2014.94
Stefan, N. Causes, consequences, and treatment of metabolically unhealthy fat distribution. Lancet Diabetes Endocrinol. 8(7), 616–627 (2020).
pubmed: 32559477 doi: 10.1016/S2213-8587(20)30110-8
Bluher, S. & Schwarz, P. Metabolically healthy obesity from childhood to adulthood: Does weight status alone matter?. Metabolism 63(9), 1084–1092 (2014).
pubmed: 25038727 doi: 10.1016/j.metabol.2014.06.009
Chen, G. C. et al. Association between regional body fat and cardiovascular disease risk among postmenopausal women with normal body mass index. Eur. Heart J. 40(34), 2849–2855 (2019).
pubmed: 31256194 pmcid: 6933870 doi: 10.1093/eurheartj/ehz391
Fukuda, T. et al. Sarcopenic obesity assessed using dual energy X-ray absorptiometry (DXA) can predict cardiovascular disease in patients with type 2 diabetes: A retrospective observational study. Cardiovasc. Diabetol. 17(1), 55 (2018).
pubmed: 29636045 pmcid: 5891961 doi: 10.1186/s12933-018-0700-5
Hyun, Y. Y. et al. Chronic kidney disease and high eGFR according to body composition phenotype in adults with normal BMI. Nutr. Metab. Cardiovasc. Dis. 26(12), 1088–1095 (2016).
pubmed: 27776918 doi: 10.1016/j.numecd.2016.09.003
Godziuk, K. et al. The impact of sarcopenic obesity on knee and hip osteoarthritis: A scoping review. BMC Musculoskelet. Disord. 19(1), 271 (2018).
pubmed: 30055599 pmcid: 6064616 doi: 10.1186/s12891-018-2175-7
Correa, L. H., Heyn, G. S. & Magalhaes, K. G. The impact of the adipose organ plasticity on inflammation and cancer progression. Cells 8(7), 662 (2019).
pubmed: 31262098 pmcid: 6679170 doi: 10.3390/cells8070662
Booth, A. et al. Adipose tissue: An endocrine organ playing a role in metabolic regulation. Horm. Mol. Biol. Clin. Investig. 26(1), 25–42 (2016).
pubmed: 26910750 doi: 10.1515/hmbci-2015-0073
Baracos, V. E. & Arribas, L. Sarcopenic obesity: Hidden muscle wasting and its impact for survival and complications of cancer therapy. Ann. Oncol. 29(suppl_2), ii1–ii9 (2018).
pubmed: 29506228 doi: 10.1093/annonc/mdx810
Jung, G. H., Kim, J. H. & Chung, M. S. Changes in weight, body composition, and physical activity among patients with breast cancer under adjuvant chemotherapy. Eur. J. Oncol. Nurs. 44, 101680 (2020).
pubmed: 31756674 doi: 10.1016/j.ejon.2019.101680
Cederholm, T. et al. GLIM criteria for the diagnosis of malnutrition: A consensus report from the global clinical nutrition community. Clin. Nutr. 38(1), 1–9 (2019).
pubmed: 30181091 doi: 10.1016/j.clnu.2018.08.002
D’Almeida, C. A. et al. Prevalence of malnutrition in older hospitalized cancer patients: A multicenter and multiregional study. J. Nutr. Health Aging 24(2), 166–171 (2020).
pubmed: 32003406 doi: 10.1007/s12603-020-1309-4
Brown, D. et al. Relationship between global leadership initiative on malnutrition (GLIM) defined malnutrition and survival, length of stay and post-operative complications in people with cancer: A systematic review. Clin. Nutr. 42(3), 255–268 (2023).
pubmed: 36716618 doi: 10.1016/j.clnu.2023.01.012
Wei, K. et al. Association of frailty and malnutrition with long-term functional and mortality outcomes among community-dwelling older adults: Results from the Singapore longitudinal aging study 1. JAMA Netw. Open 1(3), e180650 (2018).
pubmed: 30646023 pmcid: 6324309 doi: 10.1001/jamanetworkopen.2018.0650
Scott, J. M. et al. Exercise therapy and cardiovascular toxicity in cancer. Circulation 137(11), 1176–1191 (2018).
pubmed: 29530893 pmcid: 6028047 doi: 10.1161/CIRCULATIONAHA.117.024671
Fyfe, J. J., Hamilton, D. L. & Daly, R. M. Minimal-dose resistance training for improving muscle mass, strength, and function: A narrative review of current evidence and practical considerations. Sports Med. 52(3), 463–479 (2022).
pubmed: 34822137 doi: 10.1007/s40279-021-01605-8
Bland, K. A. et al. Exercise-based interventions to counteract skeletal muscle mass loss in people with cancer: Can we overcome the odds?. Sports Med. 52(5), 1009–1027 (2022).
pubmed: 35118634 doi: 10.1007/s40279-021-01638-z
Wedell-Neergaard, A. S. et al. Exercise-induced changes in visceral adipose tissue mass are regulated by IL-6 signaling: A randomized controlled trial. Cell Metab. 29(4), 844-855.e3 (2019).
pubmed: 30595477 doi: 10.1016/j.cmet.2018.12.007

Auteurs

Kaiwen Zheng (K)

Cancer Center, The First Hospital of Jilin University, Xinmin St No 126, Changchun, 130021, Jilin, China.

Xiangliang Liu (X)

Cancer Center, The First Hospital of Jilin University, Xinmin St No 126, Changchun, 130021, Jilin, China.

Yuguang Li (Y)

College of Instrumentation and Electrical Engineering, Jilin University, Changchun, Jilin, China.

Jiuwei Cui (J)

Cancer Center, The First Hospital of Jilin University, Xinmin St No 126, Changchun, 130021, Jilin, China. cuijw@jlu.edu.cn.

Wei Li (W)

Cancer Center, The First Hospital of Jilin University, Xinmin St No 126, Changchun, 130021, Jilin, China. liwei66@jlu.edu.cn.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH