Open Access

Impact of postoperative reduced skeletal muscle on prognosis after recurrence in gastric cancer

  • Authors:
    • Keita Kouzu
    • Hironori Tsujimoto
    • Hidekazu Sugasawa
    • Yusuke Ishibashi
    • Yujiro Itazaki
    • Satoshi Tsuchiya
    • Yoji Kishi
    • Hideki Ueno
  • View Affiliations

  • Published online on: October 30, 2020     https://doi.org/10.3892/mco.2020.2165
  • Article Number: 3
  • Copyright: © Kouzu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Little is known about the association between sarcopenia development after gastrectomy and gastric cancer prognosis after recurrence. The present study retrospectively examined the effects of decreased psoas muscle index (PMI) on post‑recurrence prognosis after gastrectomy. A total of 67 patients with gastric cancer recurrence were included in the present study. PMI at pre‑operation and recurrence were calculated, and 25 patients whose PMI reduction rate value was lower than the cutoff values (male=0.766 and female=0.704) were classified into the sarcopenia group and 42 patients into the non‑sarcopenia group. There were no significant differences between the groups regarding age, sex, pathological stage, and nutrition and inflammation indices at the time of recurrence. Post‑recurrence overall survival (OS) was significantly shorter in the sarcopenia group compared with the non‑sarcopenia group (P<0.001). The post‑recurrence survival rate was significantly worse in the sarcopenia group compared with the non‑sarcopenia group (P<0.001). In multivariate analysis, sarcopenia (HR=5.04) and the total courses of chemotherapy after recurrence (HR=3.88) were independent unfavorable prognostic factors. In conclusion, sarcopenia and fewer total courses of post‑recurrence chemotherapy were poor prognostic factors after gastric cancer recurrence. To improve prognosis, preventing sarcopenia development after gastrectomy is required.

Introduction

Despite ongoing advances in diagnostics, operative technique, and treatment strategy for the decades, gastric cancer remains one of the most common cancers in the world and a lethal disease (1). Gastrectomy for gastric cancer is essential for improving the survival rate, it may cause persistent functional disorders such as reduced amount of oral intake, insulin resistance, increased protein catabolism, and metabolic changes, leading to weight loss and the development of sarcopenia (2). It is reported that preoperative sarcopenia has been associated with long-term prognosis as well as short-term outcomes such as the development of postoperative pneumonia, poor activities of daily living, longer hospital stay, and the incidence of postoperative complications (3-10), which may restrict the following treatment options (11). Treatment option for patient with recurrence of gastric cancer after gastrectomy is limited to chemotherapy or best supportive care. It is known that sarcopenia could influence on pharmacokinetics of chemotherapy which could be associated with adverse effects of chemotherapy in several cancers (4). However, little is known about the effects of reduced skeletal muscle volume after gastrectomy on prognosis and treatment strategy after the recurrence of gastric cancer. In the present study, we investigated the effects of reduced skeletal muscle volume after gastrectomy on the treatment and prognosis in patients with recurrent gastric cancer.

Materials and methods

Patients

The study protocol was approved by the Institutional Review Board of National Defense Medical College (Saitama, Japan). Of the 553 patients who underwent radical gastrectomy for gastric cancer at the National Defense Medical College between 2011 and 2016, 67 patients who had gastric cancer recurrence were included in this study. We retrospectively evaluated the clinicopathological findings, serum albumin levels, C-reactive protein (CRP), total cholesterol, and neutrophil and lymphocyte counts at the time of preoperative and recurrence of gastric cancer. In addition, the neutrophil-lymphocyte ratio (NLR), the CRP-albumin ratio (CAR), the controlling nutrition status (CONUT) score, the prognostic nutritional index (PNI), and the modified Glasgow prognostic (mGPS) score were calculated as markers of nutrition or inflammation.

The tumor pathological findings were recorded in accordance with the third English edition of the Japanese Classification of Gastric Carcinoma, edited by the Japanese Gastric Cancer Association (12). All patients were followed-up using an oncologically appropriate plan on a per-patient basis. For patients with stage II or III disease, postoperative adjuvant chemotherapy with S-1 (80 mg/m²/day) was recommended for 1 year. In 45 cases of pathological stage II or III gastric cancer patients, 26 cases (57.8%) received adjuvant chemotherapy. There was no significant correlation between age and receiving adjuvant chemotherapy.

Definition of sarcopenia

The psoas muscle index (PMI: cm2/m2) was calculated from CT images (Aquilion 64; Toshiba Medical Systems) and the psoas muscle cross-sectional area at the third lumbar vertebra (L3) normalized length preoperatively and at the recurrence of gastric cancer by a physician who was blinded to the clinicopathological characteristics of the patients (Fig. 1) (13,14). The reduction rate of PMI from the preoperative value to that at the recurrence of gastric cancer was calculated. The patients were divided into two groups by the cutoff value using area under the receiver operating characteristic curves (ROC); the sarcopenia group (n=25 patients) had less than the cutoff value of the reduction rate of PMI (male=0.766 and female=0.704), and the non-sarcopenia group (n=42 patients) had more than the cutoff value (Fig. 2). The median value of the total cohort was 0.793.

Statistical analyses

All statistical analyses were performed using the JMP® Pro 14.0.0 software package (SAS Institute Inc.). The Student's t-test and Pearson's Chi-square test were performed, as appropriate. A receiver operating characteristics (ROC) curve was constructed to estimate the optimal cutoff value of the reduction of PMI. Survival rates were obtained by the Kaplan-Meier method, and the statistical significance was determined by the log-rank test.

Univariate and multivariate analyses were performed using the Cox proportional hazards regression model. The data are expressed as mean ± standard deviation. A P-value of <0.05 was considered statistically significant.

Results

Patient characteristics

Patients' clinical factors at the recurrence of gastric cancer and pathological factors diagnosed from resected specimens are shown in Table I. There were no significant differences in age, sex, Charlson Comorbidity Index score, and surgical procedure including reconstruction methods between the two groups. The sarcopenia group had a higher body weight and body mass index (BMI) than did the non-sarcopenia group. In addition, the reduction rates of body weight and BMI due to the recurrence of gastric cancer in the sarcopenia group were higher than those of the non-sarcopenia group. There was no significant difference in the pathological factors between the two groups except for tumor depth. The NLR, CAR, CONUT score, PNI, and mGPS at the recurrence of gastric cancer were not significantly different between the two groups (Table II). There was no significant difference in the time between gastrectomy and recurrence, the number of patients who received adjuvant chemotherapy and chemotherapy after the recurrence, the number of discontinued chemotherapies due to adverse effect, the number of chemotherapy regimens after recurrence, the kind of basic chemotherapy after recurrence, and the total courses of chemotherapies between the two groups. The sarcopenia group had a significantly shorter OS from recurrence than did the non-sarcopenia group (median survival time, interquartile range: 118, 43.5-180.5 vs. 300, 133.8-636.3 days, P<0.001).

Table I

Patient's clinicopathological factors.

Table I

Patient's clinicopathological factors.

CharacteristicSarcopenia (n=25, 37.3%)Non-Sarcopenia (n=42, 62.7%)Total (n=67)P-value
Age72.1±7.870.0±8.670.8±8.30.393
Sex   0.718
     Male203252 
     Female51015 
Body weight (kg)    
     Preoperatively55.4±8.959.5±9.857.9±9.60.082
     At the time of recurrence46.2±8.151.2±7.949.3±8.30.014a
     Recurrence/preoperatively0.8±0.10.9±0.10.9±0.1 0.422b
Body mass index (kg/m2)    
     Preoperatively21.3±2.922.6±3.222.1±3.10.071
     At the time of recurrence17.7±2.219.5±2.618.8±2.60.010a
     Recurrence/preoperatively0.8±0.10.9±0.10.9±0.10.338
Psoas muscle index    
     Preoperatively3.9±0.93.7±1.13.8±1.00.223
     At the time of recurrence2.5±0.83.2±1.03.0±1.00.005a
     Recurrence/Preoperatively0.6±0.10.9±0.10.8±0.2 <0.001a
CCI score 2≤   0.630
     Yes6814 
     No193453 
Tumor location U/M/L   0.579
     U111526 
     M91221 
     L51520 
Histology int/dif/other   0.210
     Int141832 
     Dif82230 
     Other325 
Tumor depth   0.418
     pT14 (16.0%)3 (7.1%)7 (10.5%) 
     pT23 (12.0%)3 (7.1%)6 (9.0%) 
     pT37 (28.0%)19 (45.2%)26 (38.8%) 
     pT411 (44.0%)17 (40.5%)28 (41.8%) 
Lymph node metastasis   0.978
     pN05 (20.0%)8 (19.1%)13 (19.4%) 
     pN14 (16.0%)8 (19.1%)12 (17.9%) 
     pN26 (24.0%)11 (26.2%)17 (25.4%) 
     pN310 (40.0%)15 (35.7%)25 (37.3%) 
Pathological cancer stage   0.267
     pStageI3 (12.0%)3 (7.2%)6 (9.1%) 
     pStageII6 (24.0%)12 (28.6%)18 (27.3%) 
     pStageIII16 (64.0%)27 (64.3%)43 (63.6%) 
Lymphatic invasion   0.613
     Ly0257 
     Ly1233760 
Venous invasion   0.429
     V0448 
     V1213859 
DG/TG/other   0.161
     DG61925 
     TG172239 
     Other213 
Open/laparoscopy   0.161
     Open182341 
     Laparoscopy71926 
Billroth-I/Roux-en-Y/other   0.130
     Billroth-I61521 
     Roux-en-Y22744 
     Other1702 
Recurrence pattern   0.455
     Peritoneal9 (36.0%)9 (7.1%)18 (26.9%) 
     Hematogenous6 (24.0%)17 (7.1%)23 (34.3%) 
     Lymph node6 (24.0%)11 (7.1%)17 (25.4%) 
     Local2 (8.0%)1 (7.1%)3 (4.5%) 
     Other2 (8.0%)4 (45.2%)6 (8.9%) 

[i] U, upper third; M, middle third; L, lower third; Int, intestinal type; Dif, diffuse type; DG, Distal gastrectomy; TG, Total gastrectomy; CCI, Charlson comorbidity index;

[ii] aP<0.05. Data are expressed as the mean ± standard deviation.

Table II

Patient's characteristics at the time of recurrence of gastric cancer.

Table II

Patient's characteristics at the time of recurrence of gastric cancer.

CharacteristicSarcopenia (n=25, 37.3%)Non-Sarcopenia (n=42, 62.7%)Total (n=67)P-value
Neutrophil lymphocyte ratio    
     Preoperatively3.0±2.43.5±2.83.3±2.60.828
     At the time of recurrence4.2±3.14.6±4.74.5±4.10.589
CAR    
     Preoperatively0.3±0.40.1±0.20.2±0.30.213
     At the time of recurrence0.7±1.00.5±0.60.6±0.80.474
CONUT score    
     Preoperatively2.3±1.12.5±1.32.4±1.20.597
     At the time of recurrence4.8±2.83.0±1.73.9±2.50.062
Prognostic nutritional index    
     Preoperatively37.2±9.535.9±13.336.4±11.70.746
     At the time of recurrence39.7±7.543.7±9.042.1±8.60.114
Modified GPS score    
     Preoperatively0.4±0.70.5±0.70.5±0.70.927
     At the time of recurrence1.2±0.71.0±0.61.1±0.70.180
Adjuvant chemotherapy   0.874
     Yes81624 
     No172643 
Discontinued adjuvant chemotherapy due to adverse effect6 (75.0%)10 (62.5%)16 (66.7%)0.540
Duration from gastrectomy to recurrence (day)572.9±513.2444.8±331.0492.6±409.50.484
Chemotherapy after recurrence   0.729
     Yes122234 
     No132033 
1st line regimen after recurrence   0.100
     Pyrimidine fluoride82028 
     Taxane224 
     Other202 
Number of chemotherapy regimens after recurrence1.6±0.81.7±1.01.7±0.90.855
Total courses of chemotherapy after recurrence3.7±2.47.5±5.66.3±5.10.092
Discontinued chemotherapy due to adverse effect6 (50.0%)7 (31.8%)13 (38.2%)0.297
Overall survival from the recurrence of gastric cancer (day)169.0±52.8492.9±83.4372.0±58.8<0.001

[i] CAR, C-reactive protein Albumin ratio; CONUT, controlling nutrition status; GPS, Glasgow Prognostic Score. Data are expressed as the mean ± standard deviation.

Prognostic factors

The survival rate from the time of recurrence in the sarcopenia group was significantly worse than that in the non-sarcopenia group (3-year OS 6.0% vs. 21.0%, P<0.001; Fig. 3). Univariate and multivariate analyses that might affect the survival rate from the time of the recurrence of gastric cancer were shown in Table III. Univariate analysis demonstrated that the total courses of chemotherapy after recurrence <5 [hazard ratio (HR)=3.82], sarcopenia (HR=2.66), NLR ≥3.0 (HR=2.63), and PNI ≤40 (HR=2.59) were significantly associated with the prognosis after recurrence. The sarcopenia group more frequently had peritoneal recurrence, which didn't affect prognosis.

Table III

Prognostic factor for the overall survival from the time at recurrence.

Table III

Prognostic factor for the overall survival from the time at recurrence.

 Univariate analysisMultivariate analysis
CharacteristicHR95% CIP-valueHR95% CIP-value
Age1.690.91-3.220.096   
     ≥70 years old      
Body weight reduction rate1.240.67-2.280.490   
     ≥Median      
Body mass index reduction rate1.210.65-2.230.530   
     ≥Median      
CCI score0.900.37-1.920.802   
     ≥2      
Tumor depth0.710.35-1.660.404   
     ≥pT3      
Lymph node metastasis1.650.88-3.240.117   
     ≥pN2      
Lymphatic invasion0.990.45-2.620.984   
     Ly1      
Venous invasion0.950.43-2.520.908   
     V1      
Neutro Lymph ratio2.631.28-5.530.008a1.480.40-5.010.544
     ≥3.0      
CONUT score2.260.90-6.200.084   
     ≥4      
Prognostic Nutritional Index2.591.23-5.500.012a1.250.33-5.010.746
     ≤40      
modified GPS score1.910.90-4.700.097   
     ≥1      
Sarcopenia4.182.17-8.07 <0.001a5.041.28-22.610.021a
     Yes      
Adjuvant chemotherapy1.050.58-1.930.872   
     No      
Recurrence site1.490.75-2.800.246   
     Peritoneal      
Chemotherapy after recurrence1.320.71-2.430.376   
     No      
Chemotherapy regimen after recurrence0.450.16-1.590.192   
     Pyrimidine fluoride      
Number of regimens after recurrence1.130.50-2.580.762   
     <2      
Total courses of chemotherapy after recurrence3.821.33-11.420.013a3.881.19-13.690.025a
     <5      

[i] HR, hazard ratio; CI, confidence interval; CRP, C-reactive protein; CONUT, controlling nutrition status; GPS, Glasgow Prognostic Score; CCI, Charlson comorbidity index.

[ii] aP<0.05.

Multivariate analysis revealed that sarcopenia at the recurrence (HR=5.04) and the total courses of chemotherapy after recurrence (HR=3.88) were independent unfavorable prognostic factors.

Table IV shows univariate and multivariate analysis for the OS from the time at recurrence among the difference time of sarcopenia. Sarcopenia at the recurrence and the reduction rate of PMI from surgery to the recurrence were selected as the independent poor prognostic factors via multivariate analysis, but preoperative sarcopenia was not.

Table IV

Univariate and multivariate analysis for the overall survival from the time at recurrence among the difference time of sarcopenia.

Table IV

Univariate and multivariate analysis for the overall survival from the time at recurrence among the difference time of sarcopenia.

 Univariate analysisMultivariate analysis
  HR95% CIP-valueHR95% CIP-value
Sarcopenia by skeletal muscle mass reduction rateYes4.182.17-8.07 <0.001a3.051.44-6.480.004a
Preoperative sarcopeniaYes0.930.51-1.730.8130.800.39-1.670.551
Sarcopenia at the time of recurrenceYes3.581.78-7.42 <0.001a3.051.30-7.310.010a

[i] HR, hazard ratio; CI, confidence interval.

[ii] aP<0.05.

Discussion

In the present study, we demonstrated that the high reduction rate of PMI from the preoperative value to that at the recurrence of gastric cancer and the fewer courses of chemotherapy performed after recurrence were independently associated with poor prognosis after the recurrence.

Since Rosenberg has reported the concept of sarcopenia in 1997, and many studies have evaluated the associations between sarcopenia and clinical factors, such as poor quality of life, aspiration pneumonia, osteoporosis, swallowing function, and respiratory function (15). In patients with malignancies, sarcopenia is more likely to be developed due to increased protein catabolism, inflammatory reactions, metabolic abnormalities, and poor oral intake and may be associated with cancer cachexia. Many recent studies have shown that the frequency of serious postoperative complications was high and the long-term prognosis was poor in gastric cancer patients with preoperative sarcopenia (5-7,9,10). In addition, postoperative loss of the muscle mass affects the continuation rate of postoperative adjuvant chemotherapy, especially in the elderly, because of increased severe adverse events (16,17). However, no study has evaluated the relationship between prognosis after the recurrence and the reduction of skeletal muscle mass after gastrectomy. This study indicated that the reduction of PMI was a risk factor of poor OS after the recurrence of gastric cancer, which is consistent with a previous report that skeletal muscle loss during postoperative adjuvant chemotherapy is associated with poor prognosis (18).

We also demonstrated that patients who failed to continue chemotherapy more than five courses after the recurrence of gastric cancer had a poor prognosis. There are several factors affecting the continuity of chemotherapy after the recurrence, i.e., adverse events, age, performance status, the amounts of oral intakes, economic problem, and other social circumstances (19). Physicians can intervene the continuity of chemotherapy by providing appropriate nutritional management and preventing loss of skeletal muscle mass at the time of recurrence, which may be associated with longer survival after the recurrence of gastric cancer.

Preoperative exercises and nutritional support programs were effective for increasing total caloric intake, protein, and grip strength, maintaining skeletal muscle volume and improving postoperative outcomes in patients with gastric cancer (19,20). However, there were few reports on the effects of postoperative nutritional supports on the postoperative development of sarcopenia and outcome. In addition, it has been reported that subtotal gastrectomy for the upper third of gastric cancer had advantages over total gastrectomy in terms of maintaining weight and nutritional status (20,21). Thus, it will be essential to ensure thorough nutritional management after surgery, as well as surgical procedures, for maintaining skeletal muscle volume and nutritional status at the recurrence of gastric cancer.

In the present study, we also evaluated the NLR, CAR, PNI, CONUT, and mGPS at the recurrence of gastric cancer, which were well known to be preoperative prognostic markers in various malignancies (22-26). We demonstrated that these markers were not associated with prognosis when the values at the recurrence were used, indicating the importance of preoperative value but not at the recurrence.

We compared the clinical importance of the sarcopenia preoperatively, at the recurrence, and the reduction rate of PMI from surgery to the recurrence. Sarcopenia at the recurrence and the reduction rate of PMI from surgery to the recurrence were selected as the independent poor prognostic factors by multivariate analysis.

This study has several potential limitations. The retrospective design of the study and relatively small number of patients in this study may have resulted in bias. In addition, we did not evaluate the relation of amounts of oral intake and the exercise after gastrectomy to the occurrence of gastric cancer, which made it difficult to determine whether skeletal muscle loss was caused by eating disorder after gastrectomy or with the progression of cancer.

In conclusion, fewer total courses of chemotherapy after recurrence and sarcopenia were poor prognostic factors for patients with gastric cancer recurrence. Our data suggested that prospective interventional study to prevent the reduction of skeletal muscle volume should be promising for improving survival after the recurrence of gastric cancer.

Acknowledgements

Not applicable.

Funding

No funding was received.

Availability of data and materials

The datasets used and/or analyzed during the present study are available from the corresponding author on reasonable request.

Authors contributions

KK, HT, HS, YIt, YIs, ST, YK and HU contributed to the study conception and design. Material preparation and data collection and analysis were performed by KK. The first draft of the manuscript was written by KK and HT, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Ethics approval and consent to participate

All procedures followed were in accordance with the Helsinki Declaration of 1964 and later versions. The study protocol was approved by the Institutional Review Board of the National Defense Medical College, and written informed consent was obtained from every patient.

Patient consent for publication

Informed consent for publication was obtained from every patient.

Competing interests

The authors declare that they have no competing interests.

References

1 

Siegel RL, Miller KD and Jemal A: Cancer statistics, 2020. CA Cancer J Clin. 70:7–30. 2020.PubMed/NCBI View Article : Google Scholar

2 

Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel JP, Rolland Y, Schneider SM, et al: Sarcopenia: European consensus on definition and diagnosis: Report of the European working group on sarcopenia in older people. Age Ageing. 39:412–423. 2010.PubMed/NCBI View Article : Google Scholar

3 

Nagata K, Tsujimoto H, Nagata H, Harada M, Ito N, Kanematsu K, Nomura S, Horiguchi H, Hiraki S, Hase K, et al: Impact of reduced skeletal muscle volume on clinical outcome after esophagectomy for esophageal cancer: A retrospective study. Medicine (Baltimore). 97(e11450)2018.PubMed/NCBI View Article : Google Scholar

4 

Antoun S, Borget I and Lanoy E: Impact of sarcopenia on the prognosis and treatment toxicities in patients diagnosed with cancer. Curr Opin Support Palliat Care. 7:383–389. 2013.PubMed/NCBI View Article : Google Scholar

5 

Fukuda Y, Yamamoto K, Hirao M, Nishikawa K, Nagatsuma Y, Nakayama T, Tanikawa S, Maeda S, Uemura M, Miyake M, et al: Sarcopenia is associated with severe postoperative complications in elderly gastric cancer patients undergoing gastrectomy. Gastric Cancer. 19:986–993. 2016.PubMed/NCBI View Article : Google Scholar

6 

Huang DD, Chen XX, Chen XY, Wang SL, Shen X, Chen XL, Yu Z and Zhuang CL: Sarcopenia predicts 1-year mortality in elderly patients undergoing curative gastrectomy for gastric cancer: A prospective study. J Cancer Res Clin Oncol. 142:2347–2356. 2016.PubMed/NCBI View Article : Google Scholar

7 

Kawamura T, Makuuchi R, Tokunaga M, Tanizawa Y, Bando E, Yasui H, Aoyama T, Inano T and Terashima M: Long-term outcomes of gastric cancer patients with preoperative sarcopenia. Ann Surg Oncol. 25:1625–1632. 2018.PubMed/NCBI View Article : Google Scholar

8 

Ongaro E, Buoro V, Cinausero M, Caccialanza R, Turri A, Fanotto V, Basile D, Vitale MG, Ermacora P, Cardellino GG, et al: Sarcopenia in gastric cancer: When the loss costs too much. Gastric Cancer. 20:563–572. 2017.PubMed/NCBI View Article : Google Scholar

9 

Wang SL, Zhuang CL, Huang DD, Pang WY, Lou N, Chen FF, Zhou CJ, Shen X and Yu Z: Sarcopenia adversely impacts postoperative clinical outcomes following gastrectomy in patients with gastric cancer: A prospective study. Ann Surg Oncol. 23:556–564. 2016.PubMed/NCBI View Article : Google Scholar

10 

Zhuang CL, Huang DD, Pang WY, Zhou CJ, Wang SL, Lou N, Ma LL, Yu Z and Shen X: 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(e3164)2016.PubMed/NCBI View Article : Google Scholar

11 

Gosney MA: Clinical assessment of elderly people with cancer. Lancet Oncol. 6:790–797. 2005.PubMed/NCBI View Article : Google Scholar

12 

Japanese Gastric Cancer Association. Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer. 14:101–112. 2011.PubMed/NCBI View Article : Google Scholar

13 

Hamaguchi Y, Kaido T, Okumura S, Kobayashi A, Hammad A, Tamai Y, Inagaki N and Uemoto S: Proposal for new diagnostic criteria for low skeletal muscle mass based on computed tomography imaging in Asian adults. Nutrition. 32:1200–1205. 2016.PubMed/NCBI View Article : Google Scholar

14 

Mourtzakis M, Prado CM, Lieffers JR, Reiman T, McCargar LJ and Baracos VE: A practical and precise approach to quantification of body composition in cancer patients using computed tomography images acquired during routine care. Appl Physiol Nutr Metab. 33:997–1006. 2008.PubMed/NCBI View Article : Google Scholar

15 

Rosenberg IH: Sarcopenia: Origins and clinical relevance. J Nutr. 127 (5 Suppl):990S–991S. 1997.PubMed/NCBI View Article : Google Scholar

16 

Aoyama T, Kawabe T, Fujikawa H, Hayashi T, Yamada T, Tsuchida K, Yukawa N, Oshima T, Rino Y, Masuda M, et al: Loss of lean body mass as an independent risk factor for continuation of S-1 adjuvant chemotherapy for gastric cancer. Ann Surg Oncol. 22:2560–2566. 2015.PubMed/NCBI View Article : Google Scholar

17 

Shen Y, Hao Q, Zhou J and Dong B: The impact of frailty and sarcopenia on postoperative outcomes in older patients undergoing gastrectomy surgery: A systematic review and meta-analysis. BMC Geriatr. 17(188)2017.PubMed/NCBI View Article : Google Scholar

18 

Sugiyama K, Narita Y, Mitani S, Honda K, Masuishi T, Taniguchi H, Kadowaki S, Ura T, Ando M, Tajika M and Muro K: Baseline sarcopenia and skeletal muscle loss during chemotherapy affect survival outcomes in metastatic gastric cancer. Anticancer Res. 38:5859–5866. 2018.PubMed/NCBI View Article : Google Scholar

19 

Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2014 (ver. 4). Gastric Cancer. 20:1–19. 2017.PubMed/NCBI View Article : Google Scholar

20 

Yamamoto K, Nagatsuma Y, Fukuda Y, Hirao M, Nishikawa K, Miyamoto A, Ikeda M, Nakamori S, Sekimoto M, Fujitani K and Tsujinaka T: Effectiveness of a preoperative exercise and nutritional support program for elderly sarcopenic patients with gastric cancer. Gastric Cancer. 20:913–918. 2017.PubMed/NCBI View Article : Google Scholar

21 

Kosuga T, Hiki N, Nunobe S, Noma H, Honda M, Tanimura S, Sano T and Yamaguchi T: Feasibility and nutritional impact of laparoscopy-assisted subtotal gastrectomy for early gastric cancer in the upper stomach. Ann Surg Oncol. 21:2028–2035. 2014.PubMed/NCBI View Article : Google Scholar

22 

Ishibashi Y, Tsujimoto H, Hiraki S, Kumano I, Yaguchi Y, Horiguchi H, Nomura S, Ito N, Shinto E, Aosasa S, et al: Prognostic value of preoperative systemic immunoinflammatory measures in patients with esophageal cancer. Ann Surg Oncol. 25:3288–3299. 2018.PubMed/NCBI View Article : Google Scholar

23 

Forrest LM, McMillan DC, McArdle CS, Angerson WJ and Dunlop DJ: Evaluation of cumulative prognostic scores based on the systemic inflammatory response in patients with inoperable non-small-cell lung cancer. Br J Cancer. 89:1028–1030. 2003.PubMed/NCBI View Article : Google Scholar

24 

Ishibashi Y, Tsujimoto H, Yaguchi Y, Kishi Y and Ueno H: Prognostic significance of systemic inflammatory markers in esophageal cancer: Systematic review and meta-analysis. Ann Gastroenterol Surg. 4:56–63. 2019.PubMed/NCBI View Article : Google Scholar

25 

Ignacio de Ulíbarri J, González-Madroño A, de Villar NG, González P, González B, Mancha A, Rodríguez F and Fernández G: CONUT: A tool for controlling nutritional status. First validation in a hospital population. Nutr Hosp. 20:38–45. 2005.PubMed/NCBI

26 

Toyokawa T, Kubo N, Tamura T, Sakurai K, Amano R, Tanaka H, Muguruma K, Yashiro M, Hirakawa K and Ohira M: The pretreatment controlling nutritional status (CONUT) score is an independent prognostic factor in patients with resectable thoracic esophageal squamous cell carcinoma: Results from a retrospective study. BMC Cancer. 16(722)2016.PubMed/NCBI View Article : Google Scholar

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Kouzu K, Tsujimoto H, Sugasawa H, Ishibashi Y, Itazaki Y, Tsuchiya S, Kishi Y and Ueno H: Impact of postoperative reduced skeletal muscle on prognosis after recurrence in gastric cancer. Mol Clin Oncol 14: 3, 2021.
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Kouzu, K., Tsujimoto, H., Sugasawa, H., Ishibashi, Y., Itazaki, Y., Tsuchiya, S. ... Ueno, H. (2021). Impact of postoperative reduced skeletal muscle on prognosis after recurrence in gastric cancer. Molecular and Clinical Oncology, 14, 3. https://doi.org/10.3892/mco.2020.2165
MLA
Kouzu, K., Tsujimoto, H., Sugasawa, H., Ishibashi, Y., Itazaki, Y., Tsuchiya, S., Kishi, Y., Ueno, H."Impact of postoperative reduced skeletal muscle on prognosis after recurrence in gastric cancer". Molecular and Clinical Oncology 14.1 (2021): 3.
Chicago
Kouzu, K., Tsujimoto, H., Sugasawa, H., Ishibashi, Y., Itazaki, Y., Tsuchiya, S., Kishi, Y., Ueno, H."Impact of postoperative reduced skeletal muscle on prognosis after recurrence in gastric cancer". Molecular and Clinical Oncology 14, no. 1 (2021): 3. https://doi.org/10.3892/mco.2020.2165