Myosteatosis predicts prognosis after radical gastrectomy for gastric cancer: A propensity score–matched analysis from a large-scale cohort

doi:10.1016/j.surg.2019.03.020

Surgery

Volume 166, Issue 3, September 2019, Pages 297-304

https://doi.org/10.1016/j.surg.2019.03.020 Get rights and content

Abstract

Background

Increasing evidence has suggested that sarcopenia is linked with cancer prognosis, but only limited data have focused on the impact of myosteatosis on cancer outcomes. This study evaluates the influence of myosteatosis on postoperative complications and survival in those patients who underwent radical resection of gastric carcinoma.

Methods

Patients who underwent elective radical gastrectomy for gastric cancer and had computed tomographic images available were identified from a prospectively collected database between 2008 and 2013. Myosteatosis was diagnosed by the cutoff values obtained from the method of optimum stratification. To obtain 2 well-balanced cohorts for available variables influencing clinical outcomes, the myosteatosis group was matched 1:1 with nonmyosteatosis group by using a propensity score match.

Results

Of 973 patients, 584 were matched for analyses. Compared with the nonmyosteatosis group, the myosteatosis group manifested significantly higher severe postoperative complications rates, shorter overall survival, and disease-free survival. Before matching, multivariate analyses identified that myosteatosis was an independent risk factor for severe postoperative complications, and Cox proportions hazards model showed that myosteatosis was an independent predictor for shorter overall survival and disease-free survival. In addition, subgroup analyses of each muscle phenotype showed that patients with both sarcopenia and myosteatosis had a poorer overall survival and disease-free survival than other patients.

Conclusion

Myosteatosis in gastric cancer is associated with poor prognosis. Classifying the skeletal muscle into subranges of radio density is a promising strategy to understand the impact of skeletal muscle on unfavorable surgical outcomes in gastric cancer patients.

Section snippets

Patients

From a prospectively collected database, consecutive patients with primary gastric cancer undergoing radical gastrectomy at Wenzhou Medical University between December 2008 and August 2013 were identified. Exclusion criteria included cancer metastasis confirmed preoperatively or during surgery, a diagnosis of double cancer or emergency surgery. Subsequently, patients with no preoperative abdominal computed tomography (CT) or incomplete data were excluded. The study was approved by the WENZHOU

Population

From December 2008 to August 2013, a total of 1,314 patients were analyzed and 341 were excluded. Thus, the total sample size included 973 patients who received radical surgery for gastric cancer. An overview of patient selection process is shown in Fig 1. There were 460 deaths; the median follow-up time was 80 months. Patients’ demographic and clinicopathologic characteristics are listed in Table I.

The sex-specific cutoff values for L3 mean muscle attenuation associated with OS were 38.5 HU

Discussion

Muscle depletion is characterized by reduced muscle size (termed sarcopenia¹⁸) and declined muscle quality (termed myosteatosis⁸), which is distinct from ordinary weight loss or cachexia and can occur in patients in any weight category, from underweight to obese.16, 19 These pathologic phenomena usually are associated with physical disability and impaired survival in cancer patients.20, 21 The predictive role of muscle mass is well established; however, less is known about the relationship

Conflicts of interest

The authors have indicated that they have no conflict of interest regarding the content of this article.

References (36)

G. Malietzis et al.
The role of body composition evaluation by computerized tomography in determining colorectal cancer treatment outcomes: a systematic review
Eur J Surg Oncol
(2015)
C.M. Prado 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)
E. von Elm et al.
The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies
Lancet
(2007)
V.E. Baracos 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)
D.E. Kelley et al.
Skeletal muscle density: effects of obesity and non-insulin-dependent diabetes mellitus
Am J Clin Nutr
(1991)
N. Mitsiopoulos et al.
Cadaver validation of skeletal muscle measurement by magnetic resonance imaging and computerized tomography
J Appl Physiol
(1998)
K.W. Reisinger et al.
Functional compromise reflected by sarcopenia, frailty, and nutritional depletion predicts adverse postoperative outcome after colorectal cancer surgery
Ann Surg
(2015)
T. Voron et al.
Sarcopenia impacts on short- and long-term results of hepatectomy for hepatocellular carcinoma
Ann Surg
(2015)
C. Simonsen et al.
Sarcopenia and postoperative complication risk in gastrointestinal surgical oncology: a meta-analysis
Ann Surg
(2018)
S.L. Wang et al.
Sarcopenia adversely impacts postoperative clinical outcomes following gastrectomy in patients with gastric cancer: a prospective study
Ann Surg Oncol
(2016)

C.L. Zhuang 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

(2016)

I. Miljkovic et al.

Epidemiology of myosteatosis

Curr Opin Clin Nutr Metab Care

(2010)

O. Addison et al.

Intermuscular fat: a review of the consequences and causes

Int J Endocrinol

(2014)

K.F. Petersen et al.

Mitochondrial dysfunction in the elderly: possible role in insulin resistance

Science

(2003)

M. Visser et al.

Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well-functioning older persons

J Gerontol A Biol Sci Med Sci

(2005)

F. Bray et al.

Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries

CA Cancer J Clin

(2018)

C. Lepage et al.

Operative mortality after gastric cancer resection and long-term survival differences across Europe

Br J Sug

(2010)

W.A. Papenfuss et al.

Morbidity and mortality associated with gastrectomy for gastric cancer

Ann Surg Oncol

(2014)

Cited by (58)

Muscle attenuation, not skeletal muscle index, is an independent prognostic factor for survival in gastric cancer patients with overweight and obesity
2024, Nutrition
Skeletal muscle index (SMI) is insufficient for evaluating muscle in obesity, and muscle attenuation (MA) may be a preferred indicator. This study aimed to investigate whether MA has greater prognostic value than SMI in gastric cancer patients with overweight and obesity.
Clinical parameters of 1312 patients with gastric cancer who underwent radical gastrectomy were prospectively collected between 2013 and 2019. MA and SMI were analyzed by computed tomography scan. Overweight/obesity was defined as body mass index (BMI) ≥24 kg/m². The hazard ratio (HR) for death was calculated using Cox regression analysis.
Among all patients, 405 were identified as overweight and obese, and 907 were identified as normal and underweight. MA was inversely associated with BMI and visceral fat area. Among the 405 patients with overweight and obesity, 212 patients (52%) were diagnosed with low MA. In the overweight/obese group, MA was an independent predictor for overall survival (HR, 1.610; P = 0.021) in multivariate Cox regression analyses, whereas SMI did not remain in the model. In the normal/underweight group, both low MA (HR, 1.283; P = 0.039) and low SMI (HR, 1.369; P = 0.008) were independent factors of overall survival. Additionally, 318 patients were identified as having visceral obesity in the overweight/obese group, and low MA was also an independent prognostic factor for survival in these patients (HR, 1.765; P = 0.013).
MA had a higher prognostic value than SMI in overweight and obese patients with gastric cancer after radical gastrectomy.
Phase angle - A screening tool for malnutrition, sarcopenia, and complications in gastric cancer
2024, Clinical Nutrition ESPEN
Patients with gastric cancer (GC) are more likely to experience malnutrition and muscle wasting. This study aims to investigate the potential of phase angle (PhA) as a screening tool for identifying malnutrition and sarcopenia in GC patients, as well as its association with short-term outcomes after radical gastrectomy.
This cross-sectional study enrolled patients diagnosed with GC at The Affiliated People's Hospital of Jiangsu University from October 2021 to September 2022. PhA was measured using bioelectrical impedance analysis. Computed tomography scan images were analyzed for body composition at the level of the third lumbar vertebra. Malnutrition was diagnosed using Global Leadership Initiative on Malnutrition (GLIM) criteria. Sarcopenia diagnosis was based on the Asian Working Group for Sarcopenia (AWGS) 2019 criteria.
A total of 248 patients with GC were analyzed, including 188 patients who underwent radical gastrectomy. Of these, 71.4 % (n = 177) were male and 28.6 % (n = 71) were female and the median overall age was 68 years (IQR: 61–72 years). According to GLIM criteria, 49.2 % (n = 122) of patients were malnourished and 19.8 % (n = 49) had sarcopenia based on AWGS criteria. A one-degree decrease in PhA was significantly associated with GLIM malnutrition (Odds Ratio [OR] = 8.108, 95 % CI:3.181–20.665) and sarcopenia (OR = 2.903, 95 % CI:1.170–7.206). PhA exhibited fair to good diagnostic accuracy in identifying GLIM malnutrition (male: AUC = 0.797; female: AUC = 0.816) and sarcopenia (male: AUC = 0.814; female: AUC = 0.710). Low PhA (OR = 3.632, 95 % CI: 1.686–7.824) and operation time (OR = 2.434, 95 % CI:1.120–5.293) were independently associated with the risk of postoperative complications.
PhA can serve as a reliable screening tool for identifying patients at risk of malnutrition, sarcopenia, and postoperative complications in GC.
Sarcopenia predicts postoperative complications and survival in colorectal cancer patients with GLIM-defined malnutrition: Analysis from a prospective cohort study
2024, European Journal of Surgical Oncology
To investigate whether sarcopenia could predict postoperative outcomes in patients with colorectal cancer with Global Leadership Initiative on Malnutrition (GLIM)-defined malnutrition.
Clinical data of patients who underwent radical resection for colorectal cancer were prospectively collected. Sarcopenia was diagnosed by the combination of low handgrip strength and low muscle quantity or quality as measured by abdominal computed tomography (CT) images. Logistic regression analysis and Cox proportional hazards regression analysis were performed to identify independent predictors for postoperative complications and survival, respectively.
A total of 310 patients with colorectal cancer with GLIM-defined malnutrition were included, of which 145 (46.77%) were identified with sarcopenia. Malnutritional patients with sarcopenia had significantly higher incidences of total complications (34.5% versus 15.8%), severe complications (9.7% versus 1.8%), longer lengths of postoperative hospital stay (median, 14 days versus 12 days), and more costs (median, 56,257 RMB versus 49,024 RMB) than those without sarcopenia. Sarcopenia was an independent predictive factor for postoperative complications (OR 2.531, 95% CI 1.451–4.415), overall survival (HR 1.519, 95% CI 1.026–2.248), and disease-free survival (HR 1.847, 95% CI 1.324–2.576). Patients with severe sarcopenia had a higher incidence of severe complications but not total complications or survival than those with not-severe sarcopenia. Moreover, the predictive value of sarcopenia for postoperative complications was attributed to muscle strength and quality but not muscle quantity.
Sarcopenia predicts postoperative complications and survival in patients with colorectal cancer with GLIM-defined malnutrition. Preoperative assessment of sarcopenia is still necessary when nutritional assessment has been well performed.
The association between skeletal muscle mass index (SMI) and survival after gastrectomy: A systematic review and meta-analysis of cohort studies
2023, European Journal of Surgical Oncology
Low skeletal muscle mass index (SMI) is frequently identified in gastric cancer patients but its association with patient survival rate is not clear. This systematic review and meta-analysis aimed to clarify the association between SMI and overall survival in gastric cancer patients after gastrectomy.
PubMed, Scopus, and Web of Science were searched from database inception until July 2021. Studies were eligible if they included gastric cancer patients, measured the SMI level, reported SMI before gastrectomy, defined sarcopenia according to SMI, and had a cohort or case-control design. Primary outcome was cancer survival rate. The risk of bias of individual studies was assessed using the Newcastle – Ottawa Scale.
Overall, 22 cohort studies including 7,203 participants were included. The quality of the included studies was moderate to high. A higher overall survival rate was associated with a higher SMI (RR = 1.62, 95% CI: 1.42–1.85). Subgroup analysis suggested a stronger association in overweight or obese patients (RR = 2.39, 95% CI: 1.13–5.09; I² = 77%; heterogeneity P < 0.01). But no significant differences in the association based on the surgery type (curative surgery vs radical surgery) or the type of gastrectomy (total gastrectomy vs sub-total gastrectomy) were observed.
It is suggested that SMI can be a prognostic indicator for overall survival in gastric cancer patients, especially in overweight and obese patients.
Efficacy of supervised exercise prehabilitation programs to improve major abdominal surgery outcomes: A systematic review and meta-analysis
2023, Journal of Clinical Anesthesia
The optimal package of components for a prehabilitation intervention remains unclear. The aim was to determine the efficacy of supervised exercise prehabilitation programs to enhance patient fitness and improve surgical outcomes. The protocol was preregistered (PROSPERO: CRD42020180693). PubMed, MEDLINE, CINAHL, AMED, CENTRAL, PeDro, ClinicalTrials.gov and the WHO International Clinical Trials Registry were searched. Randomized controlled trials (RCTs) of supervised prehabilitation programs before major abdominal surgery were included. Physical function, cardiorespiratory capacity and surgical outcomes were the primary outcomes measures. Risk of bias was assessed according to the Cochrane Risk of Bias 1.0 tool for RCTs. Data are summarized narratively, and where possible, quantitavely. Meta-analyses results are reported as risk ratios (RR), mean difference of changes between baseline and follow-up time points or mean difference between groups and 95% confidence interval (CI). Twenty RCTs were included in the analysis with a total of 1258 patients. The average 6-min walking distance change was +33 m in the prehabilitation group compared to the usual care (UC) group after prehabilitation (95% CI: [13, 53], P < 0.01). Only in studies with more than one supervised session per week changes in 6-min-walk distance were significantly higher in the prehabilitation group compared to the UC group after prehabiliatation (Mean difference: 47 m, 95% [CI]: [20–75], P < 0.01). The change in peak volume of oxygen uptake during a maximum cardiopulmonary test was +1.47 mL·kg⁻¹·min⁻¹ in the prehabilitation group compared to the UC group (95% CI: [0.68, 2.25], P < 0.01). There was no significant difference in the change in oxygen uptake at anaerobic threshold between groups (Mean differences: 0.47, 95% CI: [−0.16, 1.10], P:0.14). Post-operative complications incidence was similar between groups (RR: 0.80, 95% CI: [0.61, 1.05], P:0.11), irrespective of the frequency of supervised session per week (RR: 0.67, 95% CI: [0.43, 1.03], P:0.07). In conclusion, prehabilitation programmes with more than one supervised session per week improved physical function but did not enhance surgical outcomes.
Prognostic values of myosteatosis for overall survival in patients with gastric cancers: A meta-analysis with trial sequential analysis
2023, Nutrition
Gastric cancer is among the most common and lethal cancers worldwide. Recently, studies have reported that myosteatosis is a prognosticator for adverse survival outcomes in patients with gastric cancer, but with inconsistent conclusions. Therefore, this meta-analysis aimed to systematically quantify the predictive power of myosteatosis for overall survival in the gastric cancer setting.
A systematic literature earch was conducted based on three databases (PubMed/Medline, EMBASE, and Web of Science) from inception until November 30, 2021. This meta-analysis pooled the hazard ratios and their 95% confidence intervals of mortality risk in patients with gastric cancer with myosteatosis versus nonmyosteatosis using a fixed-effects model.
Twelve studies of 5904 patients were included. Myosteatosis was associated with higher mortality risk (hazard ratio: 1.46; 95% confidence interval, 1.32–1.61; P < 0.001; I² = 23.8%) in the gastric cancer setting. The results of the subgroup analysis revealed that patients with myosteatosis undergoing surgery had significantly shortened overall survival. Overall, the results of this meta-analysis are robust to sensitivity and trial sequential analyses.
Myosteatosis was identified as a strong predictor of reduced overall survival in the gastric cancer population.

View all citing articles on Scopus

: Supported by the National Natural Science Foundation of China (No. 81800795,81770884), Shanghai Science and Technology Committee (No. 16411954200), Shanghai Municipal Commission of Health and Family Planning (No. 20184Y0301), Fundamental Research Funds for the Central Universities (No. 22120180051).

: Cheng-Le Zhuang and Xian Shen contributed equally to this work.

View full text

StomachMyosteatosis predicts prognosis after radical gastrectomy for gastric cancer: A propensity score–matched analysis from a large-scale cohort

Abstract

Background

Methods

Results

Conclusion

Section snippets

Patients

Population

Discussion

Conflicts of interest

Eur J Surg Oncol

Lancet Oncol

Lancet

Am J Clin Nutr

Am J Clin Nutr

Cadaver validation of skeletal muscle measurement by magnetic resonance imaging and computerized tomography

J Appl Physiol

Functional compromise reflected by sarcopenia, frailty, and nutritional depletion predicts adverse postoperative outcome after colorectal cancer surgery

Ann Surg

Sarcopenia impacts on short- and long-term results of hepatectomy for hepatocellular carcinoma

Ann Surg

Sarcopenia and postoperative complication risk in gastrointestinal surgical oncology: a meta-analysis

Ann Surg

Sarcopenia adversely impacts postoperative clinical outcomes following gastrectomy in patients with gastric cancer: a prospective study

Ann Surg Oncol

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

Epidemiology of myosteatosis

Curr Opin Clin Nutr Metab Care

Intermuscular fat: a review of the consequences and causes

Int J Endocrinol

Mitochondrial dysfunction in the elderly: possible role in insulin resistance

Science

Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well-functioning older persons

J Gerontol A Biol Sci Med Sci

Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries

CA Cancer J Clin

Operative mortality after gastric cancer resection and long-term survival differences across Europe

Br J Sug

Morbidity and mortality associated with gastrectomy for gastric cancer

Ann Surg Oncol

Stomach
Myosteatosis predicts prognosis after radical gastrectomy for gastric cancer: A propensity score–matched analysis from a large-scale cohort