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. 2024 Nov 3;38(6):2827–2835. doi: 10.21873/invivo.13763

Sarcopenia’s Impact Defined by Grip Strength and Muscle Mass on Post-hepatectomy Outcomes: A Multicenter Analysis

SOTARO FUKUHARA 1, TSUYOSHI KOBAYASHI 1, MICHINORI HAMAOKA 2, HONMYO NARUHIKO 1,3, KOICHI OISHI 4, YOSUKE NAMBA 1, KO OSHITA 1, KEISO MATSUBARA 1, DAISUKE TAKEI 1, RYOSUKE NAKANO 1, HIROSHI SAKAI 1, SHINTARO KURODA 1, HIROYUKI TAHARA 1, MASAHIRO OHIRA 1, HIDEKI OHDAN 1
PMCID: PMC11535901  PMID: 39477404

Abstract

Background/Aim

Sarcopenia is diagnosed based on grip strength and skeletal muscle mass. Although decreased skeletal muscle mass has been reported to be associated with poor outcomes after hepatectomy, a few studies have included data on grip strength in hepatectomy candidates. This multicenter study investigated the clinical factors and postoperative complications associated with sarcopenia by assessing the grip strength and skeletal muscle mass in patients undergoing hepatectomy for hepatocellular carcinoma (HCC).

Patients and Methods

Data from patients who underwent hepatectomy for HCC between January 2020 and March 2022 were retrospectively collected from multi-institutional databases. Sarcopenia was defined as reduced grip strength and skeletal muscle mass. The patients were categorized into the sarcopenia and non-sarcopenia groups, and baseline characteristics and short term outcomes were compared between the two groups.

Results

Overall, 253 patients were included, among which 36 (14.2%) had sarcopenia. The sarcopenia group was significantly associated with older age, low body mass index, comorbid heart or chronic pulmonary disease, cerebrovascular accident history, and overall and major postoperative complications compared to the non-sarcopenia group. Among major postoperative complications [Clavien-Dindo classification (CDC) ≥Ⅲ], the incidence of bile leakage and intra-abdominal abscess were higher in the sarcopenia group than in the non-sarcopenia group. Multivariate analysis revealed that sarcopenia was an independent risk factor for overall and major postoperative complications (CDC ≥Ⅲ).

Conclusion

Sarcopenia, defined by grip strength and skeletal muscle mass, is a predictor of overall and major complications after hepatectomy for HCC.

Keywords: Sarcopenia, hepatocellular carcinoma, hepatectomy, complications, grip strength

Liver cancer is the sixth most common cancer and the third leading cause of cancer-related deaths worldwide (1). Although advances in multimodal therapies have improved the survival rate of patients with liver cancer (2), hepatectomy remains the primary treatment option. Postoperative complications are strongly related to poor long-term outcomes of hepatocellular carcinoma (HCC) (3). Therefore, identifying the risk factors for complications after hepatectomy for HCC is essential.

In hepatology, the assessment of the nutritional and functional status of patients synchronized with the evaluation of sarcopenia has gained considerable interest (4-6). Sarcopenia is a highly prevalent comorbidity in patients with liver disease (7), and it has been reported to affect the postoperative outcomes of liver cancer (5,8-10). However, most previous studies have assessed sarcopenia solely based on the skeletal muscle mass and have lacked data on grip strength (5,8-10), although assessing both the skeletal muscle mass and grip strength is essential for diagnosing sarcopenia (11,12). Since grip strength has been reported to be a better predictor of adverse outcomes than skeletal muscle mass (11,13), assessing both measures is crucial for predicting poor therapeutic outcomes. Consequently, further investigation of the effect of sarcopenia on the outcomes after hepatectomy for liver cancer is required based on the assessment of both the grip strength and skeletal muscle mass.

To the best of our knowledge, no multicenter studies have examined the association between sarcopenia, assessed based on grip strength and skeletal muscle mass, and short-term outcomes after HCC resection. In this study, we assessed sarcopenia using grip strength and skeletal muscle mass and retrospectively investigated the clinical characteristics of patients with sarcopenia, as well as the impact of sarcopenia on short-term outcomes of patients undergoing hepatectomy for HCC in a multicenter cohort using a multicenter database. This study aimed to examine the clinical factors associated with sarcopenia and the impact of sarcopenia on the short-term outcomes of patients undergoing HCC resection.

Patients and Methods

Patients. This retrospective multicenter study included patients who underwent hepatectomy for HCC at four facilities affiliated with the Hiroshima Surgical Study Group of Clinical Oncology between January 2020 and March 2022. The study protocol was approved by the Ethics Committee of our hospital (Permit Number: E2057) and was conducted in accordance with the Declaration of Helsinki and its later amendments. All patients provided informed consent for the procedures and data usage. We excluded patients with missing data on grip strength or skeletal muscle mass.

Data collection. Data on the baseline characteristics and perioperative outcomes were extracted from the Hiroshima Surgical Study Group of Clinical Oncology database. Baseline characteristics included age, sex, body mass index (BMI), American Society of Anesthesiologists Physical Status classification (ASA-PS), grip strength, skeletal muscle mass index (SMI), hepatitis B surface antigen, hepatitis C virus antibody, comorbidities, Child-Pugh classification, preoperative general blood biochemistry data, indocyanine green retention (ICGR) 15, tumor markers, such as alpha-fetoprotein and des-γ-carboxy prothrombin, tumor size, tumor number, tumor differentiation, microvascular invasion (mvi), and TNM stage. TNM stage was classified according to the Liver Cancer Study Group of Japan (14). Comorbidities comprised liver cirrhosis, hypertension, diabetes mellitus, heart disease (congestive heart failure, history of ischemic heart disease, and arrhythmia), chronic pulmonary disease (chronic obstructive pulmonary disease and interstitial pneumonia), cerebrovascular accident history, and chronic renal failure. Perioperative outcomes included type of surgical procedure (open/laparoscopic, anatomical/non-anatomical, and initial/repeat hepatectomy), Pringle maneuver, liver resection volume, operative time, blood loss, blood transfusion, postoperative complications, 30-day mortality, postoperative hospital stay, and death at one year.

Definition of sarcopenia. Sarcopenia was defined as a decrease in both grip strength and skeletal muscle mass regardless of age, according to the Japan Society of Hepatology criteria (15). Reduced muscle strength was defined as grip strength of ≤28 kg and ≤18 kg for males and females, respectively (12,15). Grip strength was measured using a Smedley-type grip dynamometer according to the Japanese Ministry of Education’s guidelines for strength testing (15). Reduced skeletal muscle mass was defined as SMI of <42 cm2/m2 and <38 cm2/m2 for males and females, respectively (15). Skeletal muscle mass was measured using computed tomography as the cross-sectional area of the skeletal muscle at the level of the third lumbar spine (L3). This variable was calculated using SYNAPSE VINCENT software (Fujifilm Co., Tokyo, Japan) and quantified within the Hounsfield unit (HU) range of -29 to +150 HU (8,11). Patients were categorized into the sarcopenia and non-sarcopenia groups based on the above definitions.

Treatment and patient follow-up. To evaluate sarcopenia, grip strength and SMI were measured within one month preoperatively. The hepatectomy procedure was decided after assessing liver function, the tumor size, tumor number, tumor location, and patient status. Hepatectomy and liver function were classified according to the General Rules for the Clinical and Pathological Study of Primary Liver Cancer (14). The Pringle maneuver was applied during hepatectomy, except when the tumor was on the liver surface or there was severe adhesion around the hepatoduodenal mesentery. An intraoperative ultrasound was performed to confirm the location of the tumor and vascular structures. Cavitron ultrasonic surgical aspirator [Clarity Ultrasonic Surgical Aspirator System (CUSA®, Integra LifeSciences Corporation, Plainsboro, NJ, USA) or WaterJet® (ERBE Elektromedizin, Tübingen, Germany)] was used to dissect the liver parenchyma. Regarding postoperative complications, complications within 30 days postoperatively were assessed using the Clavien-Dindo classification (CDC) (16). CDC ≥Ⅲ was defined as a major complication. We also calculated the comprehensive complication index (17). Post hepatectomy liver failure and bile leakage were defined according to the definitions of the International Study Group of Liver Surgery (18,19).

Statistical analysis. Patient baseline characteristics and perioperative outcomes were compared between the sarcopenia and non sarcopenia groups. Categorical variables were compared using Pearson’s chi-square test and are presented as numbers and percentages. Continuous variables were compared using the Mann-Whitney U-test and are presented as medians and interquartile ranges (IQRs). Multigroup comparisons were performed using the Kruskal-Wallis test. Univariate and multivariate logistic regression analyses were conducted to identify the risk factors for postoperative complications. All variables in the univariate analysis were included in the multivariate models, and variables with a p-value >0.05 were used to exclude covariates through backward elimination. All statistical analyses were two-sided, with a significance level set at p<0.05. Statistical analyses were performed using JMP version 14 (SAS Institute, Cary, NC, USA).

Results

Patients. Overall, 253 patients who underwent hepatectomy for HCC were included in this study. The median age of the patients was 74 years (IQR=69-78 years), with 191 (75.5%) being male. Sarcopenia was present in 36 (14.2%) patients, who were classified into the sarcopenia group, whereas the remaining 217 (85.8%) were included in the non-sarcopenia group. Among postoperative complications, major complications occurred in 30 (11.9%) patients.

Sarcopenia and baseline characteristics. A comparison of the baseline characteristics of patients between the two groups is presented in Table I. Patients in the sarcopenia group were significantly older (p=0.003), had a higher proportion of females (p=0.009), lower BMI (p<0.001), and serum cholinesterase level (p=0.031) than those in the non-sarcopenia group. The Child-Pugh score was significantly higher in the sarcopenia group than in the non-sarcopenia group (p=0.016). Regarding comorbidities, the sarcopenia group had a significantly higher prevalence of comorbid heart disease (p=0.024), chronic pulmonary disease (p=0.028), and history of cerebrovascular disease (p=0.028) than the non-sarcopenia group. No significant differences were found between the two groups regarding ASA-PS, underlying liver disease, tumor markers, tumor size, tumor number, tumor differentiation, mvi, and stage.

Table I. Comparison of baseline characteristics of patients between the sarcopenia and non-sarcopenia groups.

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BMI: Body mass index; ASA-PS: American Society of Anesthesiologists Physical Status; SMI: skeletal muscle mass index; HBV: hepatitis B virus; HCV: hepatitis C virus; NBNC: non-B non-C; AST: aspartate aminotransferase; ALT: alanine aminotransferase; ICGR 15: indocyanine green retention 15; AFP: alpha-fetoprotein; DCP: des-γ-carboxy prothrombin; mvi: micro vascular invasion. Values are expressed as median (interquartile range) or numbers (percentages).

Sarcopenia and perioperative outcomes. A comparison of the perioperative outcomes between the two groups is shown in Table II. No significant differences were observed in the type of surgical procedure, Pringle maneuver, liver resection volume, operative time, blood loss, and blood transfusion. The sarcopenia group experienced a significantly higher incidence of overall postoperative complications than the non-sarcopenia group (p=0.037). The incidence of major complications was also significantly higher in the sarcopenia group than in the non-sarcopenia group (p=0.008). Moreover, the comprehensive complication index was significantly higher in the sarcopenia group than in the non-sarcopenia group (p=0.028). The postoperative hospital stay length was significantly longer in the sarcopenia group than in the non-sarcopenia group (p=0.011). No significant differences were observed in other postoperative outcomes between the two groups.

Table II. Comparison of perioperative outcomes between the sarcopenia and non-sarcopenia groups.

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PHLF: Post-hepatectomy liver failure; CDC: Clavien-Dindo classification; ICU: intensive care unit. Values are expressed as median (interquartile range) or number (percentage).

We also investigated major complications after hepatectomy for HCC in the two groups (Table III). Among the major complications, the incidence of bile leakage ≥ grade B was significantly higher in the sarcopenia group than in the non-sarcopenia group (p<0.001). Additionally, intra abdominal abscesses tended to be more frequent in the sarcopenia group than in the non-sarcopenia group (p=0.056).

Table III. Major complications after hepatectomy for hepatocellular carcinoma in the sarcopenia and non-sarcopenia groups.

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SSI: Surgical site infection. Major complications were defined as postoperative complications with Clavien-Dindo ≥III. There are some overlapping data. Values are expressed as numbers (percentages).

Risk factors for postoperative complications. The risk factors for overall postoperative complications are shown in Table IV. Sarcopenia, low hemoglobin levels, high serum aspartate aminotransferase levels, low serum cholinesterase levels, high ICGR 15 levels, liver cirrhosis, multiple tumors, long operative time, and large amounts of blood loss were significantly associated with the development of postoperative complications in the univariate analysis. The results of the multivariate analysis indicated that sarcopenia (p=0.044), low hemoglobin levels (p=0.002), high ICGR 15 levels (p=0.012), and a large amount of blood loss (p<0.001) were the independent risk factors for overall postoperative complications.

Table IV. Risk factors for overall postoperative complications in patients with hepatocellular carcinoma after hepatectomy.

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CI: Confidence interval; BMI: body mass index; NBNC: non-B non-C; ASA-PS: American Society of Anesthesiologists Physical Status; AST: aspartate aminotransferase; ALT: alanine aminotransferase; ICGR 15: indocyanine green retention 15; AFP: alpha-fetoprotein; DCP: des-γ-carboxy prothrombin.

The risk factors for major postoperative complications were also analyzed (Table V). Univariate analysis showed that female sex, sarcopenia, low serum cholinesterase level, liver cirrhosis, and multiple tumors were significantly associated with the development of major complications. In multivariate analysis, sarcopenia (p=0.009) and multiple tumors (p=0.008) were the independent risk factors for major complications.

Table V. Risk factors for major postoperative complications in patients with hepatocellular carcinoma after hepatectomy.

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CI: Confidence interval; BMI: body mass index; NBNC: non-B non-C; ASA-PS: American Society of Anesthesiologists Physical Status; AST: aspartate aminotransferase; ALT: alanine aminotransferase; ICGR 15: indocyanine green retention 15; AFP: alpha-fetoprotein; DCP: des-γ-carboxy prothrombin. Major complications were defined as postoperative complications with Clavien-Dindo ≥ΙΙΙ.

Based on the above results, sarcopenia was an independent risk factor for both overall and major postoperative complications.

Discussion

This study assessed sarcopenia by measuring the grip strength and skeletal muscle mass in patients undergoing hepatectomy for HCC in a multicenter setting. To the best of our knowledge, this is the first multicenter study of the association between short-term outcomes after hepatectomy for HCC and sarcopenia, evaluated using both grip strength and skeletal muscle mass. The clinical factors associated with sarcopenia were older age, low BMI, comorbidities of heart disease, chronic pulmonary disease, and cerebrovascular accident history. Sarcopenia, defined by grip strength and skeletal muscle mass, was found to be an independent risk factor for postoperative complications. Especially, sarcopenia, defined by grip strength and skeletal muscle mass, can predict major complications after hepatectomy for HCC.

The causes of sarcopenia are related to age, activity, disease, and nutrition (18). A previous study reported that the incidence of sarcopenia was approximately 30% in patients with chronic hepatitis and 40% in those with liver cirrhosis in Japan (19). In patients who underwent hepatectomy for HCC, the preoperative incidence of sarcopenia in this study was 14.2%, which is similar to its frequency in a previous study (13). Regarding comorbidities, the results showed that patients with sarcopenia had higher Child-Pugh scores and higher prevalence rates of heart, pulmonary, and cerebrovascular diseases. These diseases have been reported to be associated with a high incidence of sarcopenia (20-22). Thus, these data suggest that patients with HCC who have concomitant sarcopenia have impaired liver function, along with various functional impairments, such as cardiac, pulmonary, and neurological impairments.

Decreased skeletal muscle mass has been reported to be associated with poor long-term outcomes after surgery for malignant tumors (23,24). Several studies have also revealed that decreased skeletal muscle mass was associated with poor short-term outcomes after hepatectomy for malignant tumors (5,9,25,26). Although these findings are important for elucidating the effects of skeletal muscle mass on short-term outcomes after hepatectomy, the abovementioned studies lacked data on grip strength. Grip strength is reportedly an important factor for predicting poor outcomes in patients with liver disease, as grip strength has been shown to be an adverse predictor of mortality in patients with chronic liver disease (27). Furthermore, a previous study indicated that patients with low grip strength and skeletal muscle mass had worse short-term outcomes after hepatectomy than those with either low grip strength or skeletal muscle mass only (13,28). Therefore, it is recommended that both grip strength and skeletal muscle mass be assessed before treatment to predict the outcomes of liver disease. Although a few studies have evaluated sarcopenia based on both grip strength and skeletal muscle mass in patients undergoing hepatectomy, they were conducted either in non uniform populations or were single-center studies (13,28). Therefore, we conducted a multicenter study that included only patients with HCC to reduce bias owing to patient background factors. Consequently, in patients with HCC undergoing hepatectomy, sarcopenia was associated with a high incidence of post hepatectomy complications and elevated comprehensive complication index. Sarcopenia, defined as reduced grip strength and skeletal muscle mass, was found to be an independent risk factor for overall complications and major complications after hepatectomy. Preoperative assessment of muscle strength and mass may help clinicians identify patients at high risk of experiencing complications after hepatectomy for HCC. Previous reports have suggested that maintenance of gut microbiota and dietary supplementation could improve muscle strength and mass and alter short-term outcomes after cancer surgery (29,30). Early detection and comprehensive management strategies for sarcopenia are important for improving outcomes in patients with cancer (31). Because muscle mass and strength can be improved preoperatively, clinicians can reduce the risk of complications after hepatectomy by addressing sarcopenia preoperatively.

This study suggests that sarcopenia is associated with the development of biliary leakage and intra-abdominal abscesses after hepatectomy. Regarding the relationship between sarcopenia and postoperative bile leakage, sarcopenic obesity, defined as the visceral fat area/SMI ratio, was reported to be an independent risk factor for developing bile leakage after hepatectomy for HCC (32). Previous studies have suggested that the catabolic and inflammatory conditions associated with sarcopenia impede tissue healing capacity (33,34). Accordingly, the negative impact of sarcopenia on the healing capacity may influence the occurrence of post hepatectomy complications. Since postoperative bile leakage has been reported to be associated with poor overall survival after hepatectomy (3,35), identifying its risk factors is important for predicting the prognosis after resection of liver cancer. Because of the small number of patients with postoperative bile leakage in this study, it could not be determined whether sarcopenia is an independent risk factor for postoperative bile leakage. Nevertheless, our results can help to elucidate the relationship between sarcopenia and postoperative bile leakage.

Study limitations. Since it is a retrospective study, prospective studies are necessary to better assess the relationship between sarcopenia and short-term outcomes after hepatectomy for HCC. This study examined whether sarcopenia, with reduced grip strength and skeletal muscle mass, affects short-term outcomes after hepatectomy for HCC. In the future, the effects of sarcopenia, defined as decreased grip strength and skeletal muscle mass, should also be investigated on the long-term outcomes after hepatectomy for HCC.

Conclusion

In conclusion, this multicenter study evaluated sarcopenia based on grip strength and skeletal muscle mass and identified clinical features associated with sarcopenia in patients with HCC after hepatectomy. Additionally, sarcopenia was found to be a predictor of overall and major complications after hepatectomy for HCC. Thus, preoperative assessment of grip strength and skeletal muscle mass may help to improve the perioperative management of patients.

Funding

This work was supported by AMED (Grant Number JP24fk0210108). The funders played no role in the study design, data collection, data analysis, or manuscript preparation.

Conflicts of Interest

The Authors declare no conflicts of interest in relation to this study.

Authors’ Contributions

Sotaro Fukuhara, Tsuyoshi Kobayashi, and Hideki Ohdan conceived and designed the study. Michinori Hamaoka, Naruhiko Honmyo, Koichi Oishi, Yosuke Namba, Ko Oshita, Keiso Matsubara, Daisuke Takei, Ryosuke Nakano and Hiroshi Sakai acquired the data. Sotaro Fukuhara and Tsuyoshi Kobayashi analyzed and interpreted the data and drafted the manuscript. Shintaro Kuroda, Hiroyuki Tahara, Masahiro Ohira, and Hideki Ohdan critically revised the article. All Authors approve of this manuscript for submission, and publication.

Acknowledgements

The Authors would like to thank Editage (www.editage.jp) for English language editing.

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