Research ArticleClinical Studies

Clinical Impact of Surgical Sarcopenia on Long-term Survival

KEISUKE KOMORI, KAZUKI KANO, TORU AOYAMA, KENTARO HARA, SHINSUKE NAGASAWA, MASATO NAKAZONO, YOTA SHIMODA, YUKIO MAEZAWA, YUTA KUMAZU, TAIICHI KAWABE, MASAKATSU NUMATA, TSUTOMU HAYASHI, TAKANOBU YAMADA, HIROSHI TAMAGAWA, TSUTOMU SATO, HARUHIKO CHO, NORIO YUKAWA, YASUSHI RINO, TAKAKI YOSHIKAWA, TAKASHI OGATA and TAKASHI OSHIMA
Anticancer Research September 2022, 42 (9) 4545-4552; DOI: https://doi.org/10.21873/anticanres.15957

Abstract

Background/Aim: Preoperative sarcopenia is associated with various cancers and affects the long-term prognosis of patients. After gastrectomy for gastric cancer, dynamic changes in body composition occur, and sarcopenia becomes more apparent after surgery than before surgery. However, the relationship between sarcopenia in the early postoperative period and long-term survival is not fully understood. The aim of this study was to determine the effects of surgical sarcopenia on long-term outcomes of patents with gastric cancer. Patients and Methods: We included 408 patients who underwent curative gastrectomy (distal or total gastrectomy) for gastric cancer at the Kanagawa Cancer Center from December 2013 to November 2017. Sarcopenia was defined using the skeletal muscle index (SMI), using computed tomography (CT) one month after gastrectomy. We compared the long-term outcomes between patients with and without sarcopenia. Results: The 5-year overall survival (OS) rates were 83.2% and 91.4% in the surgical and non-surgical sarcopenia groups, respectively. The hazard ratio (HR) of surgical sarcopenia for OS was 2.410 (95% confidence interval (CI)=1.321-4.396). In addition, surgical sarcopenia was associated with non-cancer-related deaths and deaths from other cancers. Conclusion: Patients with surgical sarcopenia after gastrectomy should be carefully monitored not only for gastric cancer recurrence but also for the occurrence of other diseases, including other cancers.

Key Words:

Gastric cancer has the third highest prevalence among cancers worldwide, and is the second most frequent cause of cancer-related deaths (1). Gastrectomy with perioperative adjuvant treatment is necessary for locally advanced gastric cancer (2); however, gastrectomy with perioperative treatment leads to perioperative changes in the body composition (3, 4), which affects both the short- and long-term oncological outcomes (5, 6) of patients with gastric cancer.

Sarcopenia is characterized by a decrease in muscle mass and function (7). Sarcopenia has been reported to be associated with various cancers and long-term prognosis recently (8-15). The prevalence of sarcopenia in gastric cancer patients is reported to be as high as 38% (16). Sarcopenia may be attributed to the effects of either gastric cancer alone, called “cancer-related malnutrition” and results in appetite loss and lean body mass loss (17), or gastrectomy, which is the second leading frequent cause of sarcopenia in patients with gastric cancer. Despite being indispensable for gastric cancer treatment, gastrectomy alone can cause sarcopenia as it results in a decrease in food intake, exercise capacity, and muscle mass after surgery (18).

Skeletal muscle loss up to 2 months after surgery was reported to be related to a worse OS in pancreatic cancer (19), and skeletal muscle loss up to 3 or 7 days after surgery was reported to be related to a worse OS in esophageal cancer (20, 21); similar results were obtained for gastric cancer.

In this study, we investigated whether sarcopenia one month after surgery for gastric cancer affects the long-term outcomes of patients and analyzed prognostic factors for long-term survival.

Patients and Methods

Patients. A total of 540 patients were selected from 703 consecutive patients who underwent gastrectomy for gastric cancer at the Kanagawa Cancer Center from December 2013 to November 2017. The eligibility criteria were the following: (i) gastric cancer proven by histological diagnosis; (ii) total or distal gastrectomy that achieved R0 resection as initial treatment for gastric cancer; (iii) aged ≥20 years; and (iv) Eastern Cooperative Oncology Group (ECOG) performance status of 0-2. The exclusion criterion was the following: (i) simultaneous surgery for diseases other than gastric cancer (excluding cholecystectomy for benign gallbladder disease); (ii) presence of infectious diseases with systemic treatments; and (iii) presence of multiple active cancers.

Surgical procedure and adjuvant treatment. This study was conducted as per the gastric cancer treatment guidelines (2). D1-plus and D2 dissection were performed for T1 and ≥T2 cases, respectively. Adjuvant chemotherapy was administered as a single agent to stage II gastric cancer patients and as a combination of two agents to stage III gastric cancer patients.

Perioperative care. Patients were treated with the Enhanced Recovery After Surgery (ERAS) protocol after gastrectomy (22). The patient was allowed to eat until midnight the day before surgery. By 3 hours before surgery, the patient had to drink 1,000 ml of hydration solution. The nasogastric tube was removed immediately after surgery, and oral intake was started from water and oral dietary supplements on the second day after surgery. On postoperative day 3, solid food was gradually introduced starting with rice porridge until postoperative day 7 when regular solid food was tolerated. Patients were discharged provided that they have recovered their diet and activities of daily living, have been able to control their pain, and have no abnormalities on blood and X-rays on the 7th postoperative day.

Evaluation of sarcopenia. We investigated the relationship between sarcopenia 1 month after surgery and OS, disease-specific survival, cancer-specific survival (CSS), and other CSS. The SMI was determined from the skeletal muscle area of L3, as measured by CT. The skeletal muscle area of L3 was determined on a single-slice plain abdominal CT image using SliceOmatic (Tomovision, Montreal, Canada) and was derived using radiation density measurements in Hounsfield units (HU). We defined the HU values of skeletal muscle from −29 to +150. Sarcopenia was present when the SMI was less than the sex-specific quartile in men (<41.5 cm2/m2) and women (<32.6 cm2/m2).

Statistical analysis and follow-up. The EZR software (Jichi Medical University, Saitama, Japan) was used for all analyses (version 3.4.3) (23). Overall survival was defined as the period from the date of surgery to the last day the patient was alive. CSS pertained to gastric cancer-related deaths. Disease-specific survival was defined as the period from the date of surgery to the date of death due to gastric cancer. Other CSS pertained to survival from other cancers aside from gastric cancer.

Univariate and multivariate analyses were used for prognostic factor analysis, and the log-rank test was used to analyze long-term survival. Continuous variables were evaluated by the t-test, whereas categorical and binary variables were evaluated by the Fisher’s exact test and Chi-square test. This study was approved by the institutional review board of Kanagawa Cancer Center (25. epidemiologic study-20).

Results

Patient background. A total of 540 patients met the inclusion criteria. Consort diagram is shown in Figure 1. The median follow-up period was 54.8 months (range=5.2-80.6 months). The median preoperative SMI for men, as measured by CT, was 46.3 (range=32.2-67.3), and the quartile was 41.5. One month after surgery, the median SMI in men was 42.2 (range=23.5-60.5). For women, the median preoperative SMI was 36.2 (range=20.8-53.1) and the quartile was 32.6. One month after surgery, the median SMI in women was 35.3 (range=16.9-46.3). The number of patients with sarcopenia before and one month after surgery was 101 (24.8%) and 161 (39.5%), respectively. This indicated that men and women with an SMI <41.5 and <32.6, respectively, had sarcopenia.

Figure 1.
Figure 1.

Consort diagram of patients enrolled in the study.

The patient backgrounds are summarized in Table I Compared to the non-sarcopenia group, the sarcopenia group was older (71 years old vs. 67 years old, p<0.001), had more males (72.0% vs. 60.7%, p=0.020), underwent total gastrectomy more often (30.4% vs. 19.8%, p=0.018), and had a higher incidence of intestinal type (57.8% vs. 47.4%, p=0.043).

View this table:
Table I.

Patients’ characteristics and pathological outcomes.

Survival. Long-term survival was compared between the sarcopenia group (group A: n=161) and the non-sarcopenia group (group B: n=247) (Figure 2). The 5-year overall survival rates in groups A and B were 83.2% and 91.4%, respectively, and the overall survival rate was significantly worse in group A (p=0.003). An analysis for prognostic factors for OS was performed (Table II). The univariate analysis for OS extracted age, T-factor, N-factor, lymphovascular invasion, and sarcopenia as prognostic factors. In addition, multivariate analysis was performed for the factors that showed significant differences in the univariate analysis. In the multivariate analysis, age, N-factor, lymphovascular invasion, and sarcopenia (HR=2.073, 95% CI=1.129-3.805, p=0.019) were identified as prognostic factors for OS.

Figure 2.
Figure 2.

Overall survival rates between sarcopenia and non-sarcopenia group a month after gastrectomy.

View this table:
Table II.

The univariate and multivariate Cox proportional hazards analysis of clinicopathological factors for overall survival.

The 5-year survival rates for gastric CSS in groups A and B were 91.8% and 94.9%, respectively, which was not significantly different between the groups (p=0.138) (Figure 3). For CSS, univariate analysis did not show sarcopenia as a prognostic factor (HR=1.839; 95% CI=0.812-4.169, p=0.144).

Figure 3.
Figure 3.

Cancer-specific survival rates between sarcopenia and non-sarcopenia group a month after gastrectomy.

The 5-year other disease-specific survival rate in group A (93.4%) was significantly worse than that in group B (98.4%) (p=0.009) (Figure 4). For other disease-specific survival, sarcopenia was identified as a prognostic factor in the univariate (HR=4.861, 95% CI=1.316-17.96, p=0.018) and multivariate analyses (HR=3.786, 95% CI=1.021-14.04, p=0.046).

Figure 4.
Figure 4.

Other disease-specific survival rates between sarcopenia and non-sarcopenia group a month after gastrectomy.

The 5-year other CSS rate in group A (83.2%) was significantly worse than that in group B (91.4%) (p=0.003) (Figure 5). For other CSS, sarcopenia was not identified as a prognostic factor in the univariate analysis (HR=6.932, 95% CI=0.773-62.18, p=0.084).

Figure 5.
Figure 5.

Other cancer-specific survival rates between sarcopenia and non-sarcopenia group a month after gastrectomy.

Comparison of the sites of recurrence between the sarcopenia and non-sarcopenia groups are shown in Table III. No significant difference was observed between the two groups in any of the recurrence sites of peritoneal recurrence, lymph node recurrence, and hematological recurrence.

View this table:
Table III.

Comparison of the sites of recurrence between the sarcopenia and non-sarcopenia groups.

Discussion

The goal of the present study was to clarify whether sarcopenia one month after gastrectomy for gastric cancer impacts the long-term prognosis of patients with gastric cancer. An important observation from the present study was that within one month, sarcopenia had an impact on OS and other disease-specific survival. In addition, sarcopenia one month after gastrectomy was an independent prognostic factor for OS and other disease-specific survival.

In the present study, the 5-year OS and CSS rates in the surgical sarcopenia and non-sarcopenia groups were 83.2% and 91.8%, and 91.4% and 94.9%, respectively. In addition, the HR of surgical sarcopenia for OS and CSS were 2.410 (95% CI=1.321-4.396) and 1.839 (95% CI=0.812-4.169), respectively. Similar results have been observed in reports on esophageal cancer (20, 21).

Matsui et al. evaluated the clinical impact of sarcopenia a week after surgery in 152 patients with esophageal cancer who underwent curative esophagectomy (20). The study participants were divided into a total psoas muscle area (TPA) non-decreasing group (no change or increase on postoperative day 7, n=100) and a TPA-decreasing group (decrease on postoperative day 7, n=52), with the TPA in both groups compared to the preoperative TPA. They demonstrated that decreased TPA early after surgery was an independent predictor of the 5-year OS in patients with esophageal cancer. The OS rates were 81.3% and 58.7% in the non-decreasing and decreasing groups, respectively (p=0.003). Moreover, decreased TPA was an independent prognostic factor for OS (HR=2.130; 95% CI=1.061-4.274; p=0.033). They concluded that decreased TPA within a week after esophagectomy was a predictive factor for OS in patients with esophageal cancer.

Maeda et al. clarified the clinical impact of sarcopenia 3 days after surgery in 72 patients with esophageal cancer who underwent radical esophagectomy (21). In this study, the total psoas major muscle mass index (TPI) was defined as the cross-sectional area of the bilateral psoas major muscles for height (cm2/m2) on CT 3 days after surgery. The median TPI reduction rate (−4.4%) from the baseline TPI was defined as the cutoff value to divide patients into the mild reduction group (n=36) and severe reduction group (n=36). They reported that OS was significantly worse in the severe reduction group (p=0.013), and multivariate analysis for OS revealed that the TPI reduction rate was an independent prognostic factor in patients with esophageal cancer (HR=4.38; 95% CI=1.15-20.06, p=0.030). Surgical sarcopenia is a promising prognostic factor in patients with esophageal cancer. Similarly, the evaluation of surgical sarcopenia using the SMI score a month after gastrectomy may be a useful tool for patients with gastric cancer.

We further discussed the clinical impact of surgical sarcopenia on deaths from other causes. In the present study, the 5-year other disease-specific survival rates in the surgical sarcopenia group (93.4%) was significantly worse than that in the non-sarcopenia (98.4%) (p=0.009). In addition, the HR of surgical sarcopenia for other disease-specific survival rates was 3.786 (95% CI=1.021-14.04) from the multivariate analysis.

Few studies have reported the relationship between non-cancer-related deaths and sarcopenia. Kuwada et al. evaluated the clinical impact of preoperative sarcopenia in 491 patients with gastric cancer who underwent gastrectomy. The SMA was divided by the body surface area (BSA) to compute the SMA/BSA index (cm2/m2) on preoperative CT (24). Sarcopenia was defined as an SMA/BSA value less than the sex-specific quartile of SMA/BSA; in their study, the cutoff values for men and women were 69.7 and 54.2 cm2/m2, respectively. The study participants were divided into preoperative sarcopenia (n=123) and non-sarcopenia (n=368) groups. Kaplan–Meier survival analysis showed that sarcopenic patients with preoperative comorbidities had more non-gastric cancer-related deaths than those without sarcopenia (p<0.001). Additionally, preoperative sarcopenia with comorbidity was an independent prognostic factor for non-cancer-related deaths after surgery (HR=1.84; 95% CI=1.31-3.61, p=0.031). It was concluded that preoperative sarcopenia combined with comorbidities is a risk factor for non-gastric cancer-related death after gastrectomy.

Meanwhile, several reports regarding sarcopenia and mortality exist (25, 26). Arango-Lopera et al. explained the association between sarcopenia and mortality in an elderly Mexican group (25). In their study, 345 elderly subjects were recruited from Mexico City and followed-up for three years. To define sarcopenia, the European Working Group on Sarcopenia in Older People (EWGSOP) algorithm was adapted with gait speed, calf perimeter, and grip strength (7). They reported that 116 subjects (33.6%) had sarcopenia, and the adjusted HR for sarcopenia was 2.39 (95% CI=1.05-5.43, p=0.037). Similarly, Landi et al. clarified the relationship between sarcopenia and mortality in elderly people over 70 years of age living in a nursing home in Italy according to the EWGSOP (n=122) (26). They reported that 40 residents (32.8%) had sarcopenia, and the adjusted HR for sarcopenia was 2.34 (95% CI=1.04-5.24).

In this study, it is possible that the high proportion of elderly people in the sarcopenia group may have contributed to the deterioration of other disease-specific survival in the sarcopenia group. In fact, the age was a strong prognostic factor for other disease-specific survival (HR=11.62, 95% CI=1.491-90.50, p=0.019) from the multivariate analysis. However, since sarcopenia a month after gastrectomy was also detected as a prognostic factor, the age is not confounding factor. This result is consistent with the previous two reports.

Lastly, we determined the clinical impact of surgical sarcopenia on death from other cancers. In the present study, the 5-year other CSS rate in the surgical sarcopenia group (83.2%) was significantly worse than that in the non-sarcopenia group (91.4%) (p=0.003). The HR of surgical sarcopenia for other CSS was 6.932 (95% CI=0.773-62.18) based on the univariate analysis. In our study, no reports of death from other cancers after gastrectomy were found.

Some reports have shown that pre-treatment sarcopenia in patients with non-gastric cancers affects OS after treatment. A meta-analysis and systematic review of 7,843 patients assessed the prognostic impact of pre-treatment SMI on clinical outcomes in patients with non-hematological solid tumors, Shachar et al. showed that a low SMI was significantly associated with poorer OS (HR=1.437; 95% CI=1.321-1.563, p<0.001) than a high SMI (27).

Several reviews have reported the relationship between poor OS with preoperative sarcopenia and non-gastric other cancers, such as breast (9), ovarian (10), hepatocellular (11), biliary tract (12), pancreatic (13), colorectal (14), and pulmonary cancer (15). In non-gastric cancers, secondary sarcopenia associated with gastrectomy may result in a poor OS. Japanese gastric cancer treatment guidelines recommend that a CT scan be performed at least once a year until 5 years after gastrectomy (2). In CT examination of patients with sarcopenia a month after gastrectomy, it is necessary to carefully diagnose not only the recurrence of gastric cancer but also the morbidity of other cancers.

This study has certain limitations. First, it was a single-center retrospective study. Second, the SMI in this study was obtained from CT a month after gastrectomy; this is usually not performed during a normal postoperative course. Third, sarcopenia was defined by the sex-specific SMI quartile and did not include muscle strength measurement, as recommended by the EWGSOP (7). Lastly, many patients with stage I gastric cancer (68.6%, n=280) were included in this study. In patients with stage II/III gastric cancer who underwent D2 gastrectomy, body weight loss at a month after gastrectomy was reported to be the most important risk factor for adherence to adjuvant chemotherapy with S-1 (28). Analyzing the cohort focused on stage II/III may yield different results.

In conclusion, it was demonstrated that sarcopenia after gastrectomy affects OS, other disease-specific survival, and other CSS. In addition, sarcopenia after gastrectomy was an independent prognostic factor for OS and other disease-specific survival. Therefore, our study suggests that patients with perioperative sarcopenia after gastrectomy should be carefully monitored not only for gastric cancer recurrence, but also for the occurrence of other diseases, including other cancers.

Acknowledgements

The Authors express their sincere gratitude to Ms. Rika Takahashi for the excellent data management.

Footnotes

  • ↵* These Authors contributed equally to this study.

  • Authors’ Contributions

    KKo wrote the article. KKo, KKa, and TA contributed to the study conception and design. KKo, KKa, TA, KT, SN, MN, YS, YM, YK, TK, MN, TH, TY, HT, YS, HC, NY, YR, TY, TOg, and TOs contributed to the data collection. All authors contributed to data acquisition, interpretation of the analyzed data, and critical revision of the manuscript. All the authors have read and approved the final manuscript.

  • Conflicts of Interest

    The Authors declare no conflicts of interest

  • Received April 30, 2022.
  • Revision received May 26, 2022.
  • Accepted June 5, 2022.

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Clinical Impact of Surgical Sarcopenia on Long-term Survival
KEISUKE KOMORI, KAZUKI KANO, TORU AOYAMA, KENTARO HARA, SHINSUKE NAGASAWA, MASATO NAKAZONO, YOTA SHIMODA, YUKIO MAEZAWA, YUTA KUMAZU, TAIICHI KAWABE, MASAKATSU NUMATA, TSUTOMU HAYASHI, TAKANOBU YAMADA, HIROSHI TAMAGAWA, TSUTOMU SATO, HARUHIKO CHO, NORIO YUKAWA, YASUSHI RINO, TAKAKI YOSHIKAWA, TAKASHI OGATA, TAKASHI OSHIMA
Anticancer Research Sep 2022, 42 (9) 4545-4552; DOI: 10.21873/anticanres.15957
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