Abstract
Purpose
Sarcopenia is increasingly recognized as a risk factor for postoperative complications in gastrointestinal cancer surgery. This study aimed to assess the association between sarcopenia and postoperative complications following laparoscopic radical resection of non-metastatic colorectal cancer (CRC).
Methods
In this retrospective study, 387 non-metastatic CRC patients undergoing laparoscopic radical resection were categorized into a sarcopenic group and a non-sarcopenic group based on preoperative skeletal muscle index (SMI, cm2/m2). Logistic regression analysis was performed to identify independent predictors for postoperative complications.
Results
Sarcopenia was present in 156 (40.31%) patients. The incidence of postoperative complications was 32.3%, with a serious complication (Clavien-Dindo III–V) rate of 12.1%. Compared with non-sarcopenic patients, sarcopenic patients had significantly higher incidences of total complications (P < 0.001) and severe complications (P = 0.026). Multivariable analysis identified sarcopenia as an independent risk factor for total postoperative complications (OR = 3.42, 95%CI 1.85–6.31). Further analysis of specific types of postoperative complications revealed that anastomotic leakage (P = 0.001), surgical site infection (P = 0.002), and surgical site adverse events (P = 0.001) rates were higher in sarcopenic patients. In multivariable analysis, sarcopenia was independently associated with anastomotic leakage (OR = 3.36, 95%CI = 1.12–10.12) and surgical site adverse events (OR = 3.02, 95%CI = 1.55–5.90).
Conclusions
Preoperative CT-derived sarcopenia can predict postoperative complications in patients with non-metastatic CRC undergoing laparoscopic radical resection, particularly anastomotic leakage and surgical site adverse events.
Supplementary Information
The online version contains supplementary material available at 10.1007/s00384-025-04932-8.
Keywords: Colorectal cancer, Sarcopenia, Postoperative complications, Computed tomography
Introduction
Colorectal cancer (CRC) is the third leading cause of cancer death worldwide and the second leading cause of cancer-related mortality [1]. Radical resection is regarded as the primary treatment modality for non-metastatic CRC [2]. With the advancement of laparoscopic and robotic techniques, the effectiveness and safety of CRC surgery continue to improve progressively, yet the risk of postoperative complications remains [3, 4]. Postoperative complications may hinder patient recovery, prolong hospitalization, and increase mortality [5]. Therefore, it is important to investigate risk factors predicting postoperative complications to identify patients that may benefit more from radical resection of CRC.
At present, most studies on the postoperative complications of CRC focus on the tumor itself [6, 7]. However, tumor characteristics are not the only factors influencing postoperative complications. Host-related factors also play an important role in the postoperative complications of CRC patients. In recent years, an increasing number of studies have reported that sarcopenia is a risk factor for postoperative complications in patients with many malignant tumors [8–10]. Sarcopenia is an age-related syndrome characterized by progressive generalized loss of muscle mass [11]. Patients with gastrointestinal tumors are most likely to have sarcopenia due to impaired digestion and absorption [12]. A meta-analysis revealed that sarcopenia was associated with an increased risk of total postoperative complications after tumor resection across a wide range of gastrointestinal cancers [13]. However, previous studies have mainly included patients undergoing open resection and those with metastatic tumors, with limited research focusing on patients with non-metastatic CRC after laparoscopic colorectal surgery [14–16]. Moreover, the effect of sarcopenia on postoperative complications in patients with non-metastatic CRC undergoing laparoscopic radical resection remains controversial. Some studies have suggested that sarcopenia was not associated with postoperative complications in CRC patients [17, 18].
The identification of sarcopenia involves three key elements: low muscle strength, low muscle mass, and low physical performance. Muscle quantity or muscle mass can be determined by several techniques, with computed tomography (CT) being recognized as the gold standard for non-invasive muscle mass assessment [19]. The most commonly used approach involves calculating the total skeletal muscle area at the level of the third lumbar vertebra. Since CT is a routinely used for the clinical staging of cancer patients, CT-derived sarcopenia is expected to be an economical and convenient method for predicting postoperative complications of CRC.
In this study, we aimed to determine whether CT-derived sarcopenia serves as a negative prognostic predictor for postoperative outcomes in patients with non-metastatic CRC undergoing laparoscopic surgery.
Materials and methods
Patient selection
We retrospectively investigated 387 patients with histologically confirmed CRC who underwent laparoscopic radical resection at our institution from January 2016 to December 2020. The exclusion criteria comprised (1) patients younger than 18 or older than 80 years; (2) patients with distant metastases; (3) patients undergoing non-laparoscopic surgery; (4) patients receiving neoadjuvant chemoradiotherapy; (5) patients with coexisting other malignant tumors; (6) patients with inadequate clinical or imaging data; and (7) patients with severe pre-existing health conditions. After applying the exclusion criteria, the final sample size was obtained (Fig. 1).
Fig. 1.
Flowchart depicting the patient selection process
This study was conducted in accordance with the principles of the Declaration of Helsinki and was approved by the Ethics Committee of Shantou University Medical College (No. B-2022–234) [20]. Given the retrospective nature of this study, the requirement for informed consent was waived.
Data collection
For each patient, the following parameters were collected: (1) patient characteristics, including age, gender, and body mass index (BMI). (2) Nutritional Risk Score (NRS) 2002 score and preoperative laboratory markers, including serum albumin, neutrophil, hemoglobin, platelet, lymphocyte, and carcinoma embryonic antigen (CEA) concentration, along with the calculated neutrophil-to-lymphocyte ratio (NLR), lymphocyte-to-monocyte ratio (LMR), and platelet-to-lymphocyte ratio (PLR) which served as indicators of inflammation [21]. (3) Surgery details, including American Society of Anesthesiologists (ASA) grade, tumor location, and surgical duration. Tumors in the cecum, right-sided, and transverse colon were classified as right-sided; those in the left colon and rectum were classified as left-sided. (4) Postoperative outcome assessment, including length of hospital stay, hospitalization costs, and postoperative complications. Postoperative complications were defined as symptoms meeting the Clavien-Dindo (CD) classification criteria between the date of operation and the date of hospital discharge, with serious complications defined as a score of ≥ 3 [22]. This study specifically investigated six key postoperative complications: incisional hernia, surgical site infection, anastomotic leakage, anastomotic bleeding, abdominal infection, and intestinal obstruction. For analytical purposes, incisional hernia and surgical site infection were categorized as surgical site adverse events. (5) Postoperative pathological tumor node metastasis (TNM) stage (8th edition of American Joint Committee on Cancer Staging Manual) [23].
Assessment of skeletal muscle mass and definition of sarcopenia
Abdominal CT examination was performed 2 weeks before surgery to assess preoperative cancer staging. As the gold standard for body composition assessment, CT enables muscle mass quantification using third lumbar vertebra cross-sectional images with visible transverse processes [19]. Skeletal musculature at this level consists of the psoas muscle, quadratus lumborum, erector spinae, transversus abdominis muscle, internal and external oblique muscles, and rectus abdominis. Skeletal muscle area was measured by manually outlining the CT images using the commercially available system (Advantage Windows Workstation 4.4, GE Healthcare, Milwaukee, Wisconsin, USA), as shown in Fig. 2. Skeletal muscle was identified based on Hounsfield Unit thresholds ranging from − 29 to + 150, as previously described. The skeletal muscle area was normalized by square height (m2) to derive the lumbar skeletal muscle index (SMI, cm2/m2). Sarcopenia was defined in this study using sex-specific SMI cutoff values of less than 40.8 cm2/m2 for males and less than 34.9 cm2/m2 for females, based on the study of Zhuang et al., which was reported to be optimal SMI cutoff values for sarcopenia of Chinese [24].
Fig. 2.
CT scan image analysis method of skeletal muscle at the third lumbar spine vertebra level
Statistical analysis
Continuous variables were presented as means ± standard deviations (SD), while categorical variables were presented as numbers and percentages. The Student t-test was used for continuous parameters, and Chi-square tests and/or Fisher precision tests were used for categorical parameters to compare baseline characteristics between sarcopenic and non-sarcopenic groups. Logistic regression analyses, both univariate and multivariate, were conducted to identify factors associated with an increased risk of postoperative complications. The degree of association was estimated using corresponding odds ratios (OR) and their 95% confidence intervals (CI). All tests conducted in this study were two-sided, with a P-value of less than 0.05 deemed statistically significant. Variables with P < 0.1 in the univariate analysis were entered in a multivariate logistic regression analysis. The statistical analyses were carried out using the commercial statistics software SPSS (version 26.0, IBM, Armonk, NY, USA).
Results
Baseline demographic and clinicopathological characteristics
A total of 387 patients were enrolled in this study and 156 (40.31%) patients had preoperative sarcopenia. Patients with sarcopenia were older than those with non-sarcopenia (median age ± SD: 62.9 ± 10.0 vs 60.6 ± 9.9, P = 0.024). Sarcopenic patients were more likely to have a lower BMI and an NRS 2002 score ≥ 3 than non-sarcopenic patients (P < 0.001). Regarding preoperative blood parameters, patients with sarcopenia had lower serum albumin (P < 0.001), hemoglobin (P = 0.001) levels, and higher NLR (P = 0.002), PLR (P = 0.038) levels than those with non-sarcopenia. There was no difference in LMR (P = 0.250) and CEA level (P = 0.863) between the two groups. The tumor locations in patients with sarcopenia were more common in right-sided (P < 0.001). There was no significant difference in pTNM stage (P = 0.447) between the two groups. All descriptive data are summarized in Table 1.
Table 1.
Comparison of basic characteristics between the sarcopenic group and the non-sarcopenic group
| Characteristic | Overall (n = 387) | Sarcopenia (n = 156) | Non-sarcopenia(n = 231) | P-value |
|---|---|---|---|---|
| Age (years) | 61.5 ± 10.0 | 62.9 ± 10.0 | 60.6 ± 9.9 | 0.024* |
| Sex, n (%) | 0.548 | |||
| Male | 218 (56.3) | 85 (54.5) | 133 (57.6) | |
| Female | 169 (43.7) | 71 (45.5) | 98 (42.4) | |
| BMI (kg/m2) | 22.2 ± 3.4 | 20.6 ± 2.8 | 23.3 ± 3.3 | < 0.001* |
| NRS 2002 score, n (%) | < 0.001* | |||
| ≥ 3 score | 178 (46.0) | 135 (86.5) | 43 (18.6) | |
| < 3 score | 209 (54.0) | 21 (13.5) | 188 (81.4) | |
| ASA grade, n (%) | 0.211 | |||
| 1 | 23 (5.9) | 8 (5.1) | 15 (6.5) | |
| 2 | 320 (82.7) | 125 (80.1) | 195 (84.4) | |
| 3 | 44 (11.4) | 23 (14.7) | 21 (9.1) | |
| Preoperative blood results | ||||
| Serum albumin (g/L) | 36.4 ± 4.6 | 35.2 ± 4.7 | 37.1 ± 4.3 | < 0.001* |
| Hemoglobin (g/L) | 120.3 ± 22.6 | 115.8 ± 22.7 | 123.3 ± 22.1 | 0.001* |
| NLR | 2.7 ± 2.0 | 3.0 ± 2.1 | 2.5 ± 1.9 | 0.002* |
| LMR | 4.0 ± 1.9 | 3.9 ± 1.7 | 4.2 ± 2.0 | 0.250 |
| PLR | 160.9 ± 86.9 | 175.3 ± 100.8 | 151.1 ± 74.8 | 0.038* |
| CEA (µg/L) | 12.9 ± 29.7 | 13.3 ± 34.8 | 12.6 ± 25.8 | 0.863 |
| Tumor location, n (%) | < 0.001* | |||
| Left-sided | 315 (81.4) | 113 (72.4) | 202 (87.4) | |
| Right-sided | 72 (18.6) | 43 (27.6) | 29 (12.6) | |
| pTNM stage, n (%) | 0.477 | |||
| I | 58 (15.0) | 19 (12.2) | 39 (16.9) | |
| II | 178 (46.0) | 72 (46.2) | 106 (45.9) | |
| III | 151 (39.0) | 65 (41.7) | 86 (37.2) |
BMI, body mass index; NRS 2002, Nutritional Risk Screening 2002; ASA, American Society of Anesthesiology; NLR, neutrophil-to-lymphocyte ratio; LMR, lymphocyte-to-monocyte ratio; PLR, platelet-to-lymphocyte ratio; CEA, carcinoembryonic antigen; TNM, tumor node metastasis
*P-value of < 0.05 was considered to indicate statistical significance
Postoperative outcome
According to the CD system classification, postoperative complications were observed in 125 patients (32.3%), of which 47 patients (12.1%) were classified as severe (CD III–V). Among the six specific types of postoperative complications in this study, surgical site infection emerged as the most prevalent complication, affecting 32 patients (8.3%), followed by anastomotic leak (7.5%), abdominal infection (6.2%), incisional hernia (3.1%), anastomotic bleeding (2.1%), and intestinal obstruction (1.6%). Table 2 summarized postoperative outcomes and complications. Patients with sarcopenia were significantly more likely to experience any complication (73/156, 46.8%). Additionally, these patients demonstrated a significantly higher incidence of severe postoperative complications (33/156, 21.2%). Anastomotic leakage occurred in 20 (12.8%) patients with sarcopenia and 9 (3.9%) patients with non-sarcopenia, and the difference was significant (P = 0.001). Surgical site infection occurred in 21 (13.5%) patients with sarcopenia and 11 (4.8%) patients with non-sarcopenia, with a significant difference (P = 0.002). Surgical site adverse events occurred in 28 (17.9%) patients with sarcopenia and 15 (6.5%) patients with non-sarcopenia, and the difference was significant (P = 0.001). There was no difference in incisional hernia (P = 0.111), anastomotic bleeding (P = 0.841), abdominal infection (P = 0.889), and intestinal obstruction (P = 0.946) between the two groups. Patients with sarcopenia had a significantly longer length of hospital stay and higher hospitalization costs compared to those with non-sarcopenia (P < 0.001). There was no significant difference in surgical duration (P = 0.801) between the two groups.
Table 2.
Comparison of clinical outcomes between the sarcopenia group and non-sarcopenia group
| Total (n = 387) |
Sarcopenia (n = 156) |
Non-sarcopenia (n = 231) |
P-value | |
|---|---|---|---|---|
| Overall complications, n (%) | 125 (32.3) | 73 (46.8) | 52 (22.5) | < 0.001* |
| Serious complication, n (%) (CDC ≥ III grade) | 47 (12.1) | 33 (21.2) | 14 (6.1) | 0.026* |
| Incisional hernia, n (%) | 12 (3.1) | 8 (5.1) | 4 (1.7) | 0.111 |
| Anastomotic leakage, n (%) | 29 (7.5) | 20 (12.8) | 9 (3.9) | 0.001* |
| Anastomotic bleeding, n (%) | 8 (2.1) | 4 (2.6) | 4 (1.7) | 0.841 |
| Surgical site infection, n (%) | 32 (8.3) | 21 (13.5) | 11 (4.8) | 0.002* |
| Abdominal infection, n (%) | 24 (6.2) | 10 (6.4) | 14 (6.1) | 0.889 |
| Intestinal obstruction, n (%) | 6 (1.6) | 3 (1.9) | 3 (1.9) | 0.946 |
| Surgical site adverse events, n (%) | 43 (11.1) | 28 (17.9) | 15 (6.5) | 0.001* |
| Surgical duration (min) | 199.7 ± 61.5 | 197.4 ± 53.2 | 201.3 ± 66.6 | 0.801 |
| Length of hospital stay (days) | 20.5 ± 8.6 | 23.0 ± 8.9 | 18.9 ± 8.0 | < 0.001* |
| Hospitalization costs (yuan) | 49,397.1 ± 13,274.0 | 52,226.7 ± 14,312.7 | 47,486.2 ± 12,188.5 | < 0.001* |
*P-value of < 0.05 was considered to indicate statistical significance
Risk factors for postoperative complications after CRC resection
The univariate analysis revealed that sarcopenia (OR = 3.03, 95%CI = 1.95–4.07) and NRS 2002 score ≥ 3 (OR = 1.91, 95%CI = 1.24–2.93) were significant risk factors for total postoperative complications. Multivariate analysis identified sarcopenia as an independent significant predictor for total postoperative complications (OR = 3.42, 95%CI = 1.85–6.31), detailed in Table 3. When specific types of postoperative complications were assessed, sarcopenia alone remained a significant independent predictor of postoperative anastomotic leakage (OR = 3.36, 95%CI = 1.12–10.12) and surgical site adverse events (OR = 3.02, 95%CI = 1.55–5.90), detailed in Table 4.
Table 3.
Uni- and multivariate analyses of predictive factors for postoperative complications
| Factors | Univariate analysis | Multivariate analysis | ||
|---|---|---|---|---|
| OR (95% CI) | P-value | OR (95% CI) | P-value | |
| Age (years) | 1.01 (0.99–1.03) | 0.515 | ||
| Sex (male/female) | 0.73 (0.47–1.12) | 0.149 | ||
| Charlson Comorbidity Index | 1.06 (0.91–1.23) | 0.477 | ||
| Sarcopenia, yes | 3.03 (1.95–4.07) | < 0.001# | 3.42 (1.85–6.31) | < 0.001* |
| BMI (kg/m2) | 0.99 (0.93–1.06) | 0.750 | ||
| NRS 2002 score, ≥ 3 | 1.91 (1.24–2.93) | 0.003# | 0.84 (0.45–1.54) | 0.570 |
| Serum albumin (g/L) | 1.00 (0.99–1.01) | 0.850 | ||
| Hemoglobin (g/L) | 0.96 (0.92–1.01) | 0.102 | ||
| ASA grade, < 3 | 0.59 (0.31–1.12) | 0.104 | ||
| Tumor location, right | 1.06 (0.62–1.83) | 0.835 | ||
| Surgical duration (min) | 1.00 (1.00–1.01) | 0.222 | ||
| TNM stage, < 3 grade | 1.34 (0.87–2.06) | 0.188 | ||
| NLR | 1.00 (0.90–1.11) | 0.997 | ||
| LMR | 0.97 (0.86–1.08) | 0.546 | ||
| PLR | 1.00 (1.00–1.00) | 0.372 | ||
OR, odds ratios; CI, confidence intervals; BMI, body mass index; NRS 2002, Nutritional Risk Screening 2002; ASA, American Society of Anesthesiology; TNM, tumor node metastasis; NLR, neutrophil-to-lymphocyte ratio; LMR, lymphocyte-to-monocyte ratio; PLR, platelet-to-lymphocyte ratio
#P-value of < 0.1 was considered to indicate statistical significance
*P-value of < 0.05 was considered to indicate statistical significance
Table 4.
Uni- and multivariate analyses of predictive factors for anastomotic leakage and surgical site adverse events
| Factors | Anastomotic Leakage | Surgical site adverse events | ||||
|---|---|---|---|---|---|---|
| Univariate analysis | Multivariable analysis | Univariate analysis | Multivariable analysis | |||
| P-value | OR (95%CI) | P-value | P-value | OR (95%CI) | P-value | |
| Age (years) | 0.487 | 0.285 | ||||
| Sex (male/female) | 0.796 | 0.800 | ||||
| Charlson Comorbidity Index | 0.260 | 0.386 | ||||
| Sarcopenia, yes | 0.002# | 3.36 (1.12–10.12) | 0.031* | 0.001# | 3.02 (1.55–5.90) | 0.001* |
| BMI (kg/m2) | 0.765 | 0.795 | ||||
| NRS 2002 score, ≥ 3 | 0.032# | 0.97 (0.33–2.86) | 0.962 | 0.173 | ||
| Serum albumin (g/L) | 0.731 | 0.507 | ||||
| Hemoglobin (g/L) | 0.070# | 0.95 (0.88–1.04) | 0.247 | 0.849 | ||
| ASA grade, < 3 | 0.305 | 0.041# | 0.48 (0.21–1.11) | 0.086 | ||
| Tumor location, right | 0.111 | 0.408 | ||||
| Surgical duration (min) | 0.790 | 0.118 | ||||
| TNM stage, < 3 grade | 0.950 | 0.635 | ||||
| NLR | 0.956 | 0.581 | ||||
| LMR | 0.583 | 0.699 | ||||
| PLR | 0.836 | 0.588 | ||||
OR, odds ratios; CI, confidence intervals; BMI, body mass index; NRS 2002, nutritional risk screening 2002; ASA, American Society of Anesthesiology; TNM, tumor node metastasis; NLR, neutrophil-to-lymphocyte ratio; LMR, lymphocyte-to-monocyte ratio; PLR, platelet-to-lymphocyte ratio
#P-value of < 0.1 was considered to indicate statistical significance
*P-value of < 0.05 was considered to indicate statistical significance
Discussion
This study confirmed that sarcopenia was significantly associated with an increased incidence of postoperative complications following laparoscopic radical resection for non-metastatic CRC. Furthermore, we demonstrated that sarcopenia served as an independent predictor of anastomotic leakage and surgical site adverse events in patients undergoing CRC surgery.
Sarcopenia is a progressive and generalized skeletal muscle disorder characterized by a pathological decline in muscle strength, quantity, and quality [11]. Some organizations worldwide, including those in Europe and Asia, have established their own diagnostic guidelines for sarcopenia [25, 26]. Although the definition of sarcopenia should include muscle strength and function as well as muscle mass, cancer-associated sarcopenia research has predominantly relied on CT-determined muscle mass as a diagnostic criterion, given its widespread use in cancer staging and surveillance [27–29]. For CRC patients, abdominal CT scan is routinely performed as part of the preoperative examination. CT-based assessment offers higher accuracy in measuring skeletal muscle mass, making it an economical, convenient, and reliable method for diagnosing sarcopenia in this population. Nevertheless, existing studies have primarily established cutoff values for the SMI based on Western populations, with limited data available for Asian cohorts [30–32]. Since all the patients in our study were Chinese, we adopted the sex-specific SMI cutoff values derived from Zhuang et al.’s study, which were reported to be optimal SMI cutoff values for Chinese [24]. Based on these SMI cutoff values, the morbidity of sarcopenia in our cohort was 40.31%, which was similar to that reported in a recent meta-analysis [33, 34].
In recent years, sarcopenia has been found to have a negative impact on the outcomes in CRC patients. Our findings align with previous studies, confirming that sarcopenic CRC patients exhibit higher rates of total and serious postoperative complications, prolonged hospitalization, and increased healthcare costs[14, 15]. However, most prior studies have predominantly focused on open resection or included patients with metastasis, rarely exploring the association between sarcopenia and postoperative complications following laparoscopic non-metastatic CRC resection [14–16]. Laparoscopic technology has become an important approach for the radical resection of non-metastatic CRC, offering advantages such as shortening hospital stay and promoting rapid recovery [35, 36]. However, this technique presents inherent challenges, especially in mid-low rectal surgeries, where the narrow pelvic space and restricted operating angles increase surgical difficulty and risk [37, 38]. Consequently, postoperative complications remain a critical concern in laparoscopic radical resection of CRC. Our findings indicated that sarcopenia was associated with an increased risk of postoperative complications in patients undergoing laparoscopic radical resection for non-metastatic CRC. Importantly, multivariable analysis identified sarcopenia as an independent risk factor for postoperative complications.
Furthermore, we conducted a detailed analysis of the association between sarcopenia and specific types of postoperative complications. While a previous study evaluating the clinical impact of sarcopenia in colon cancer patients undergoing laparoscopic surgery found it associated with overall postoperative complications but not specific types [39], our findings demonstrated that anastomotic fistula, surgical site infection, and surgical site adverse events were more frequently observed in sarcopenic CRC patients. Multivariable regression analysis showed that sarcopenia independently predicted both anastomotic fistula and surgical site adverse events undergoing laparoscopic radical resection for non-metastatic CRC.
The mechanism of sarcopenia is multifactorial, and it can alter systemic inflammatory response, endocrine function, nutritional status, and insulin resistance [40]. These mechanisms may contribute to increased incidence of postoperative complications. Systemic inflammatory response is recognized as a key factor in the occurrence and development of sarcopenia [41]. High inflammatory response is often observed in patients with sarcopenia. In our research, it can also be seen that the inflammation indicators such as NLR and PLR were higher in the sarcopenic group. Moreover, Zhou et al.’s research demonstrated that postoperative inflammatory indicator levels in sarcopenic patients were significantly elevated compared to preoperative baseline values [42]. Additionally, previous studies, including our present study, found sarcopenia was associated with malnutrition such as lower BMI, decreased hemoglobin levels, serum albumin, and lower NRS 2002 scores. Malnutrition may also lead to a pro-inflammatory state [43, 44]. Hyperinflammatory state resulting from these factors can hamper the healing capacity of intestinal tissues and wounds. This can explain why sarcopenia is associated with anastomotic leakage and surgical site adverse events after CRC surgery.
By analyzing the odds ratio (OR = 3.42), this study indicated that a threefold increased risk of postoperative complications for CRC patients undergoing laparoscopic radical resection once sarcopenia occurred. These findings suggested that sarcopenia might be a potential therapeutic point for surgeons during the perioperative period in the future. Several current studies have demonstrated that resistance training and supplementation of supportive proteins can increase or prevent further loss of muscle mass of patients with CRC [45]. However, as a retrospective study, our research could not evaluate whether such physical and nutritional interventions might reduce the incidence of postoperative complications in patients with CRC. This requires further verification through future clinical trials. Additionally, emerging surgical techniques may offer additional benefits for sarcopenic patients. Previous studies have demonstrated that natural orifice specimen extraction surgery (NOSES) for CRC, which was less invasive than laparoscopic surgery with auxiliary incisions, can avoid auxiliary incisions in the abdomen and reduce the incidence of postoperative incisional hernia and incisional infection [46, 47]. Therefore, NOSES could represent a preferable surgical approach for CRC patients with sarcopenia, provided that radical surgical specimens are suitable for natural orifice extraction. This requires further investigation in future studies.
While this study provides valuable insights, it is essential to acknowledge its limitations. Firstly, as a single-center study, the bias on the different population may be inevitable. Large-scale and multi-center studies are warranted to verify our conclusion. Secondly, the further long-term outcome regarding the prognosis of sarcopenic patients with CRC was not present in this study, and it remains to be investigated through further long-term follow-up.
Conclusion
In conclusion, our study demonstrated that in patients with laparoscopic radical resection of non-metastatic CRC, preoperative CT-derived sarcopenia was an independent predictor for postoperative complications, particularly anastomotic leakage and surgical site adverse events.
Supplementary Information
Below is the link to the electronic supplementary material.
Acknowledgements
We sincerely thank Dr. Caiyu Zhuang for the English language polishing.
Author contribution
SSY, LXX and HRB were involved in study concepts and design. CZL, HLP and XYB were responsible for imaging data measurement. YFJ and HXJ contributed to clinical data collection. LZJ, CYK and ZZQ focused on data analysis and interpretation. SSY, LZJ and CZL wrote the manuscript. HRB and LXX served as the corresponding author, overseeing the review of the article and providing guidance. All authors have approved the final manuscript.
Funding
This work was supported by the 2023 Guangdong Province Medical Research Fund Projects (A2023264) and the Guangdong Basic and Applied Basic Research Foundation (2024A1515220098).
Data availability
No datasets were generated or analysed during the current study.
Declarations
Ethical approval
This study was approved by the Ethics Committee of Shantou University Medical College (No. B-2022–234) and performed in accordance with the Declaration of Helsinki.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Shuyan Su, Zejia Lin, and Zelong Cai have contributed equally to this work.
Contributor Information
Xinxin Li, Email: xxli2023@163.com.
Ruibin Huang, Email: rbhuang1@stu.edu.cn.
References
- 1.Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F (2021) Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71:209–249. 10.3322/caac.21660 [DOI] [PubMed] [Google Scholar]
- 2.Dekker E, Tanis PJ, Vleugels J, Kasi PM, Wallace MB (2019) Colorectal cancer. LANCE-T 394:1467–1480. 10.1016/S0140-6736(19)32319-0 [DOI] [PubMed] [Google Scholar]
- 3.Wang W, Liu J, Wang J, Li L, Kong D, Wang J (2024) Comparative study of robotic-assisted vs. laparoscopic surgery for colorectal cancer: a single-center experience. FRONT ONC-OL 14:1507323. 10.3389/fonc.2024.1507323 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Vilsan J, Maddineni SA, Ahsan N, Mathew M, Chilakuri N, Yadav N, Munoz EJ, Nadee-m MA, Abbas K, Razzaq W et al (2023) Open, laparoscopic, and robotic approaches to treat colorectal cancer: a comprehensive review of literature. Cureus 15:e38956. 10.7759/cureus.38956 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.McSorley ST, Horgan PG, McMillan DC (2016) The impact of the type and severity of postoperative complications on long-term outcomes following surgery for colorectal cancer: a systematic review and meta-analysis. Crit Rev Oncol Hematol 97:168–177. 10.1016/j.critrevonc.2015.08.013 [DOI] [PubMed] [Google Scholar]
- 6.Micu BV, Vesa SC, Pop TR, Micu CM (2020) Evaluation of prognostic factors for 5 yearsurvival after surgery for colorectal cancer. ANN ITAL CHIR 91:41–48 [PubMed] [Google Scholar]
- 7.Luo YH, Yan ZC, Liu JY, Li XY, Yang M, Fan J, Huang B, Ma CG, Chang XN, Nie X (2024) Association of tumor budding with clinicopathological features and prognostic value in stage III-IV colorectal cancer. World J Gastroenterol 30:158–169. 10.3748/wjg.v30.i2.158 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Fang P, Zhou J, Xiao X, Yang Y, Luan S, Liang Z, Li X, Zhang H, Shang Q, Zeng X et al (2023) The prognostic value of sarcopenia in oesophageal cancer: a systematic review and meta-analysis. J Cachexia Sarcopenia Muscle 14:3–16. 10.1002/jcsm.13126 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Chen F, Chi J, Liu Y, Fan L, Hu K (2022) Impact of preoperative sarcopenia on postoperative complications and prognosis of gastric cancer resection: a meta-analysis of cohort studies. Arch Gerontol Geriatr 98:104534. 10.1016/j.archger.2021.104534 [DOI] [PubMed] [Google Scholar]
- 10.Liu C, An L, Zhang S, Deng S, Wang N, Tang H (2024) Association between preoperative sarcopenia and prognosis of pancreatic cancer after curative intent surgery: a updated systematic review and meta-analysis. WORLD J SURG ONCOL 22:38. 10.1186/s12957-024-03310-y [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Cruz-Jentoft AJ, Sayer AA (2019) Sarcopenia. LANCET 393:2636–2646. 10.1016/S0140-6736(19)31138-9 [DOI] [PubMed] [Google Scholar]
- 12.Zhang FM, Wu HF, Shi HP, Yu Z, Zhuang CL (2023) Sarcopenia and malignancies: epidemiology, clinical classification and implications. AGEING RES REV 91:102057. 10.1016/j.arr.2023.102057 [DOI] [PubMed] [Google Scholar]
- 13.Simonsen C, de Heer P, Bjerre ED, Suetta C, Hojman P, Pedersen BK, Svendsen LB, C-hristensen JF (2018) Sarcopenia and postoperative complication risk in gastrointestinal surgical oncology: a meta-analysis. ANN SURG 268:58–69. 10.1097/SLA.0000000000002679 [DOI] [PubMed] [Google Scholar]
- 14.Chai VW, Chia M, Cocco A, Bhamidipaty M, D’Souza B (2021) Sarcopenia is a strong predictive factor of clinical and oncological outcomes following curative colorectal cancer resection. ANZ J SURG 91:E292–E297. 10.1111/ans.16706 [DOI] [PubMed] [Google Scholar]
- 15.Nakanishi R, Oki E, Sasaki S, Hirose K, Jogo T, Edahiro K, Korehisa S, Taniguchi D, Kudo K, Kurashige J et al (2018) Sarcopenia is an independent predictor of complications after colorectal cancer surgery. SURG TODAY 48:151–157. 10.1007/s00595-017-1564-0 [DOI] [PubMed] [Google Scholar]
- 16.Bajric T, Kornprat P, Faschinger F, Werkgartner G, Mischinger HJ, Wagner D (2022) Sar-copenia and primary tumor location influence patients outcome after liver resection for colorectal liver metastases. Eur J Surg Oncol 48:615–620. 10.1016/j.ejso.2021.09.010 [DOI] [PubMed] [Google Scholar]
- 17.Portale G, Spolverato YC, Bartolotta P, Gregori D, Mazzeo A, Rettore C, Cancian L, Fiscon V (2023) Skeletal muscle mass and surgical morbidity after laparoscopic rectal cancer resection. J Laparoendosc Adv Surg Tech A 33:570–578. 10.1089/lap.2023.0068 [DOI] [PubMed] [Google Scholar]
- 18.Kemper M, Melling N, Krause L, Kuhn K, Grass JK, Izbicki JR, Gerdes L, Adam G, Y-amamura J, Molwitz I (2023) Muscle quality, not quantity, is associated with outcome after colorectal cancer surgery. Eur J Surg Oncol 49:107098. 10.1016/j.ejso.2023.107098 [DOI] [PubMed] [Google Scholar]
- 19.Tagliafico AS, Bignotti B, Torri L, Rossi F (2022) Sarcopenia: how to measure, when and why. RADIOL MED 127:228–237. 10.1007/s11547-022-01450-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.World Medical Association Declaration (2025) World Medical Association Declaration of Helsinki: ethical principles for medical research involving human participants. JAMA 333:71–74. 10.1001/jama.2024.21972 [DOI] [PubMed] [Google Scholar]
- 21.Kondrup J, Allison SP, Elia M, Vellas B, Plauth M (2003) ESPEN guidelines for nutrition screening 2002. CLIN NUTR 22:415–421. 10.1016/s0261-5614(03)00098-0 [DOI] [PubMed] [Google Scholar]
- 22.Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. ANN SURG 240:205–213. 10.1097/01.sla.0000133083.54934.ae [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Amin MB, Edge SB, Greene FL, et al (2016) AJCC cancer staging manual. 8th ed. New York, NY: Springer, 779–85.
- 24.Zhuang CL, Huang DD, Pang WY, Zhou CJ, Wang SL, Lou N, Ma LL, Yu Z, Shen X (2016) 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. 10.1097/MD.0000000000003164 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyere O, Cederholm T, Cooper C, Landi- F, Rolland Y, Sayer AA et al (2019) Sarcopenia: revised European consensus on definition and diagnosis. AGE AGEING 48:16–31. 10.1093/ageing/afy169 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Chen LK, Woo J, Assantachai P, Auyeung TW, Chou MY, Iijima K, Jang HC, Kang L, Kim M, Kim S et al (2020) Asian Working Group for Sarcopenia: 2019 consensus update on sarcopenia diagnosis and treatment. J AM MED DIR ASSOC 21:300–307. 10.1016/j.jamda.2019.12.012 [DOI] [PubMed] [Google Scholar]
- 27.Kim EY, Kim YS, Park I, Ahn HK, Cho EK, Jeong YM (2015) Prognostic significance of CT-determined sarcopenia in patients with small-cell lung cancer. J THORAC ONCOL 10:1795–1799. 10.1097/JTO.0000000000000690 [DOI] [PubMed] [Google Scholar]
- 28.Liu T, Yi X, Ge J, Zhang J, Tan F, Song K, Liu H, Tang M (2022) Preoperative computed tomography-determined sarcopenia is a reliable prognostic factor in patients with gastric cancer after radical gastrectomy: a sex-specific analysis. Front Nutr 9:884586. 10.3389/fnut.2022.884586 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Su H, Ruan J, Chen T, Lin E, Shi L (2019) CT-assessed sarcopenia is a predictive factor for both long-term and short-term outcomes in gastrointestinal oncology patients: a systematic review and meta-analysis. Cancer Imaging 19:82. 10.1186/s40644-019-0270-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Xiong J, Wu Y, Hu H, Kang W, Li Y, Jin P, Shao X, Li W, Tian Y (2022) Prognostic significance of preoperative sarcopenia in patients with gastric cancer liver metastases receiving hepatectomy. Front Nutr 9:878791. 10.3389/fnut.2022.878791 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Yang J, Zhang T, Feng D, Dai X, Lv T, Wang X, Gong J, Zhu W, Li J (2019) A new diagnostic index for sarcopenia and its association with short-term postoperative complications in patients undergoing surgery for colorectal cancer. COLORECTAL DIS 21:538–547. 10.1111/codi.14558 [DOI] [PubMed] [Google Scholar]
- 32.Choi MH, Oh SN, Lee IK, Oh ST, Won DD (2018) Sarcopenia is negatively associated with long-term outcomes in locally advanced rectal cancer. J Cachexia Sarcopenia Muscle 9:53–59. 10.1002/jcsm.12234 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.He J, Luo W, Huang Y, Song L, Mei Y (2023) Sarcopenia as a prognostic indicator in colorectal cancer: an updated meta-analysis. FRONT ONCOL 13:1247341. 10.3389/fonc.2023.1247341 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Lin WL, Nguyen TH, Huang WT, Guo HR, Wu LM (2024) Sarcopenia and survival in c-olorectal cancer without distant metastasis: a systematic review and meta-analysis. J Gastroenterol Hepatol 39:2250–2259. 10.1111/jgh.16681 [DOI] [PubMed] [Google Scholar]
- 35.Veldkamp R, Kuhry E, Hop WC, Jeekel J, Kazemier G, Bonjer HJ, Haglind E, Pahlman L, Cuesta MA, Msika S et al (2005) Laparoscopic surgery versus open surgery for colon cancer: short-term outcomes of a randomised trial. LANCET ONCOL 6:477–484. 10.1016/S1470-2045(05)70221-7 [DOI] [PubMed] [Google Scholar]
- 36.Kong M, Chen H, Shan K, Sheng H, Li L (2022) Comparison of survival among adults with rectal cancer who have undergone laparoscopic vs open surgery: a meta-analysis. JAMA Netw Open 5:e2210861. 10.1001/jamanetworkopen.2022.10861 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Yao Q, Sun QN, Ren J, Wang LH, Wang DR (2023) Comparison of robotic-assisted vers-us conventional laparoscopic surgery for mid-low rectal cancer: a systematic review and meta analysis. J Cancer Res Clin Oncol 149:15207–15217. 10.1007/s00432-023-05228-6 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38.Zhu XM, Bai X, Wang HQ, Dai DQ (2025) Comparison of efficacy and safety between robotic-assisted versus laparoscopic surgery for locally advanced mid-low rectal cancer following neoadjuvant chemoradiotherapy: a systematic review and meta-analysis. INT J SURG 111:1154–1166. 10.1097/JS9.0000000000001854 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39.Oh RK, Ko HM, Lee JE, Lee KH, Kim JY, Kim JS (2020) Clinical impact of sarcopenia in patients with colon cancer undergoing laparoscopic surgery. ANN SURG TREAT RES 99:153–160. 10.4174/astr.2020.99.3.153 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Nishikawa H, Fukunishi S, Asai A, Yokohama K, Nishiguchi S, Higuchi K (2021) Pathophysiology and mechanisms of primary sarcopenia (review). INT J MOL MED 48:156. 10.3892/ijmm.2021.4989 [DOI] [PubMed] [Google Scholar]
- 41.Liang Z, Zhang T, Liu H, Li Z, Peng L, Wang C, Wang T (2022) Inflammaging: the ground for sarcopenia? EXP GERONTOL 168:111931. 10.1016/j.exger.2022.111931 [DOI] [PubMed] [Google Scholar]
- 42.Zhou S, Wang K, Yuan Q, Liu L, Miao J, Wang H, Ding C, Guan W (2024) The role of sarcopenia in pre- and postoperative inflammation: implications of outcomes in patients with colorectal cancer. J GASTROINTEST SURG 28:1791–1798. 10.1016/j.gassur.2024.08.015 [DOI] [PubMed] [Google Scholar]
- 43.Benedek Z, Todor-Boer S, Kocsis L, Bauer O, Suciu N, Coros MF (2021) Psoas muscle index defined by computer tomography predicts the presence of postoperative complications in colorectal cancer surgery. Medicina (Kaunas) 57:472. 10.3390/medicina57050472 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44.Traeger L, Bedrikovetski S, Nguyen TM, Kwan YX, Lewis M, Moore JW, Sammour T (2023) The impact of preoperative sarcopenia on postoperative ileus following colorectal cancer surgery. TECH COLOPROCTOL 27:1265–1274. 10.1007/s10151-023-02812-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45.Burke D, Brown M, O’Neill C, Coleman HG, Kuhn T, Schlesinger S, Prue G, Coyle V (2025) The effect of lifestyle interventions on sarcopenia in advanced colorectal cancer: a systematic review. J GERIATR ONCOL 16:102143. 10.1016/j.jgo.2024.102143 [DOI] [PubMed] [Google Scholar]
- 46.Xu S, Liu K, Chen X, Yao H (2022) The safety and efficacy of laparoscopic surgery ver-sus laparoscopic NOSE for sigmoid and rectal cancer. SURG ENDOSC 36:222–235. 10.1007/s00464-020-08260-6 [DOI] [PubMed] [Google Scholar]
- 47.Wang S, Tang J, Sun W, Yao H, Li Z (2022) The natural orifice specimen extraction surgery compared with conventional laparoscopy for colorectal cancer: a meta-analysis of efficacy and long-term oncological outcomes. INT J SURG 97:106196. 10.1016/j.ijsu.2021.106196 [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Data Availability Statement
No datasets were generated or analysed during the current study.