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Abstract

Sarcopenia is thought to be a marker for underlying frailty and malnutrition, contributing to poor functional status and suboptimal healing postoperatively. We aimed to complete an updated systematic review and meta-analysis evaluating the impact of sarcopenia on short- and long-term outcomes following colorectal cancer surgery. We searched MEDLINE, Embase, and CENTRAL up to September 2023. Studies that compared sarcopenic and non-sarcopenic patients’ short- and long-term outcomes following curative intent elective surgery for colorectal cancer were included. The main outcomes included postoperative morbidity, postoperative mortality, and length of stay (LOS), among others. Inverse variance random effects meta-analyses was performed. Risk of bias was assessed with Cochrane tools. Certainty of evidence was assessed with GRADE. After screening 215 studies, we included 40 non-randomized studies, totalling 13,422 patients, of which 5,432 (40.4%) were classified as sarcopenic. Across 27 studies, patients with sarcopenia were more likely to experience 30-day postoperative morbidity (40% vs 33%, RR 1.30, 95% CI 1.12-1.50, P < 0.01, I² 79%). The mean LOS was 1.46 days longer for sarcopenic patients (26 studies, 95% CI 0.85-2.07, P < 0.01, I² 82%). Upon pooling data from 13 studies, sarcopenic patients had increased risk of 30-day postoperative mortality (2.8% vs 1.0%, RR 2.74, 95% CI 1.63-4.62, P < 0.01, I² 0%). The findings from this systematic review suggest with low to very-low certainty evidence that in patients who are undergoing curative intent surgery for colorectal cancer, preoperative sarcopenia is associated with poor postoperative outcomes.

Keywords

colorectal cancer colonic neoplasm rectal neoplasm colorectal surgery sarcopenia meta-analysis

Introduction

Colorectal cancer is the third most common cancer in the world, with 1.9 million cases diagnosed per year worldwide.¹ Despite recent advances in neoadjuvant, endoscopic, and surgical endoluminal therapies, oncologic resection remains the mainstay for definitive care of curative colorectal cancer. Importantly, colorectal cancer is often diagnosed in patients of advanced age (ie, median age of 68 in women and 65 in men)²; therefore, most patients have medical comorbidities at the time of their colorectal cancer surgery.

In addition to comorbidities, an important metric in the oncologic patient population is sarcopenia, which can be an indicator of frailty and malnutrition. Sarcopenia has been defined as a progressive skeletal muscle disorder that is associated with falls, disability, and even mortality.³ Sarcopenia can be diagnosed based on clinical tests of muscle strength (eg, grip strength or chair rise test) or quantitative tests of muscle mass on imaging (eg, computed tomography (CT) and magnetic resonance imaging (MRI)).³ It has been cited that between 12 and 60% of colorectal cancer patients are sarcopenic.⁴ Multiple studies have shown that this is associated with worsened postoperative outcomes,^4-7 which may then cause delay in adjuvant chemotherapy initiation and subsequently worse long-term oncologic outcomes, such as disease-free survival (DFS) and overall survival (OS).^8-12 A recent meta-analysis by Trejo-Avila et al⁹ demonstrated increases in postoperative complications, mortality, and length of stay (LOS) in patients with sarcopenia. Moreover, they demonstrated decreased DFS and OS in patients with sarcopenia following colorectal cancer surgery.⁹

There have been multiple observational studies published since the most up to date data synthesis.^13-17 These studies have added important data regarding surgical outcomes of colorectal cancer patients with sarcopenia. Our aim is to update previous reviews and meta-analyses to compare postoperative complication rates and survival outcomes between patients with and without sarcopenia undergoing surgery for colorectal cancer. We hypothesize that preoperative sarcopenia will be associated with worsened short- and long-term outcomes for these patients.

Methods

This systematic review and meta-analysis is reported in accordance to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) (Appendixes 1-2). The study protocol (CRD42023493416) was registered on the International Prospective Register of Systematic Reviews (PROSPERO) a priori. This study did not require local ethics approval.

Search Strategy

The databases Medline, EMBASE, and Cochrane Central Register of Controlled Trials (CENTRAL) were searched over the period from database inception through September 2023. The search was devised and executed by a medical research librarian with input from study investigators. Search terms included “sarcopenia,” “muscle atrophy,” “colorectal adenocarcinoma,” “colorectal surgery,” and more (complete search strategy available in Appendixes 3 and 4). To ensure all relevant articles were included, the references of studies meeting inclusion criteria were searched manually.

Eligibility Criteria

Articles were eligible for inclusion if they were observational studies comparing adult patients (greater than 18 years of age) with or without sarcopenia undergoing elective colorectal cancer surgery with curative intent. Studies containing data regarding one or more short-term postoperative outcome (ie, 30-day morbidity, 30-day mortality, LOS, specific complications, re-operation, or readmission) were included. Studies were excluded if they evaluated patients undergoing emergency surgery, as when compared to elective surgical patients, this population confers a high risk profile and may add significant heterogeneity. Single-armed, non-comparative studies were also excluded, as well as systematic reviews, editorials, meta-analyses, and any study not reporting primary data.

Study Selection

Four reviewers (SK, VS, MA, and EH) independently evaluated the searched titles and abstracts using a standardized, pilot-tested form on Covidence©. Any discrepancies that arose during title and abstract screening phases were resolved by inclusion of the study. The same four reviewers completed full-text screening. Discrepancies were resolved by consensus between the reviewers during the full-text screening phase. An alternate reviewer was consulted in the case of persisting disagreement.

Data Collection

Four reviewers (SK, VS, MA, and EH) independently conducted data extraction into a data collection form designed a priori and pilot-tested on Microsoft Excel©. The extracted data included study characteristics (eg, author, year of publication, and location of study), patient demographics (eg, age, gender, body mass index [BMI], comorbidities, and sarcopenia status), disease characteristics (eg, colorectal cancer location and stage of colorectal cancer), treatment characteristics (eg, operation type and receipt of neoadjuvant or adjuvant chemotherapy), postoperative complications (eg, 30-day postoperative morbidity, 30-day postoperative mortality, system-specific morbidity, anastomotic leak, and surgical site infection (SSI)), postoperative LOS, reoperation, readmission, and long-term oncologic outcomes (eg, 5-year OS and 5-year DFS),.

Outcomes Assessed

The main outcomes defined a priori included 30-day postoperative mortality, 30-day postoperative morbidity, anastomotic leak, SSI, postoperative LOS, 30-day readmission, 30-day reoperation, 5-year OS, and 5-year DFS. 30-day postoperative mortality was defined as any documented death within 30 days of the index operation. 30-day postoperative morbidity was defined according to each individual study and included any documented deviation from the expected postoperative course. If studies did not report 30-day postoperative morbidity as a pooled outcome, it was reported as missing. Postoperative LOS was defined as the number of days from the index operation to the time the patient left an acute care bed. Anastomotic leak was defined as communication between the intraluminal and extraluminal compartments at the site of surgical anastomosis, which results from defect of the intestinal wall.¹⁸ Surgical site infection was defined according to the Centre for Disease Control and Prevention classification of SSIs.¹⁹ If studies reported overall SSI as a pooled outcome, this was extracted preferentially; studies that reported organ or space SSI, deep incisional SSI, and superficial incisional SSI were extracted and used to represent the event rate. 30-day readmission was defined as readmission to hospital reported by each included study within 30 days of the index surgery. For this review, reoperation rate was defined as any unanticipated return to the operating room following the index procedure and within 30 days of the index surgery. 5-year OS and DFS data were defined as the percentage of patients alive vs alive and without evidence of disease at 5 years following their index surgery, respectively. This data was extracted from tables and text, and in the event that this data was not reported in those forms, they were extracted from estimations of Kaplan-Meier curves.

Risk of Bias Assessment and Certainty of Evidence

Risk of bias for observational studies was assessed using the Risk of Bias in Non-randomized Studies of Interventions (ROBINS-I) assessment tool.²⁰ Four reviewers (SK, VS, MA, and EH) assessed the risk of bias and certainty of evidence independently. Any discrepancies were discussed among the reviewers to reach consensus.

Certainty of evidence for estimates derived from meta-analyses was assessed by Grading of Recommendations, Assessment, Development, and Evaluation (GRADE).²¹ As recommended by the Cochrane Collaborative, the GRADE results were collated in a summary of findings table. The GRADEpro software was used for calculations and organization of results into a summary of findings table.²²

Statistical Analysis

All statistical analyses were performed using Stata version 18 (StataCorp, College, TX) and DataParty (Hamilton, ON, Canada). A meta-analysis was performed using an inverse variance random effects model for all comparative data. The threshold for statistical significance was set a priori at P < 0.05. Pooled effect estimates for binary outcomes were estimated with risk ratios (RRs) along with their respective 95% confidence intervals (CIs). Pooled effect estimates for continuous outcomes were estimated with mean differences (MDs) along with their respective 95% CI. Mean and standard deviation (SD) were estimated for studies that only reported median and range or interquartile range (IQR) using the method described by Wan et al.²³ Any missing SD data were then calculated according to the prognostic method.²⁴ Assessment of the between-study heterogeneity was done using the I² statistic, with I² greater than 40% being considered as a sign of considerable heterogeneity.²⁵ Publication and reporting bias in meta-analyzed outcomes were assessed with funnel plots when data from more than 10 studies were included in the analysis.²⁶ Egger’s test was used to assess for publication bias.²⁷ Heterogeneity was explored through the following a priori subgroup analyses: (1) geographic location; (2) operative approach (ie, more than 50% laparoscopic vs less than 50% laparoscopic); and (3) age (mean age <65, ≥65, or <65 non-sarcopenic, ≥65 sarcopenic). A systematic narrative summary was provided for each outcome.

Results

Study Characteristics

After screening 215 studies, 40 non-randomized studies,^5,7,15,28-64 totalling 13,422 patients were included. Of these patients, 5432 (40.4%) were classified as sarcopenic. A PRISMA flow diagram of the study selection process is illustrated in Figure 1. Included studies were conducted between 2012 and 2023. Detailed demographic data for each of the included studies is shown in Supplemental Table 1.

Figure 1.

PRISMA diagram of included studies From: Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 2021;372:n71. doi: 10.1136/bmj.n71.

Disease Characteristics and Treatment

Features of disease and treatment course including cancer location, stage, neoadjuvant or adjuvant treatment, and surgery type are included in Supplemental Table 2. Regarding operative approach, 12 studies (30%) reported data on procedure performed, of which right hemicolectomy was the most commonly performed procedure (n = 1,518, 38%). Studies varied in their determination of sarcopenia. The majority of studies (36/40, 90%) used smooth muscle index (SMI) measured from the psoas muscle at the level of L3 in preoperative computed topography (CT) scans. Studies chose the SMI value which defines sarcopenia based on lowest quartile or tertile verses pre-set values based on prior literature in all cases except three.^34,40,45

Immediate Postoperative Outcomes

Short-term postoperative outcomes on patients’ courses in hospital after colorectal cancer resection are shown in Table 1. Across 27 studies with data on postoperative morbidity, pooled analysis found that patients with sarcopenia were more likely to experience 30-day postoperative morbidity (40% vs 33%, RR 1.30, 95% CI 1.12-1.50, P < 0.01, I² 79%) as shown in Figure 2. There was an observed subgroup interaction according to geographic study location (X² = 8.56, P = 0.04, I² = 79%) for this outcome, with increased morbidity seen in studies from Asia and “Other” counties including the continents of North America and Australia (Supplemental Figure 1). There was also an observed subgroup interaction according to operative approaches (X² = 6.53, P = 0.01, I² = 84.7%) (Supplemental Figure 2), with increased risk of postoperative morbidity in sarcopenic patients from studies where the majority of patients underwent open operations (RR 1.74, 95% CI 1.23-2.45) as compared to studies where the majority of patients underwent minimally invasive operations (RR 1.04, 95% CI 0.86-1.26). A subgroup analysis for age did not show significant interaction with postoperative morbidity (Supplemental Figure 3, X² = 1.74, P = 0.42, I² = 0.0%).

Table 1.

Short-Term Postoperative Outcomes in Sarcopenic and Non-sarcopenic Patients Following Colorectal Cancer Surgery.

Study	Arm	N per Arm	Mean LOS (SD)	30-day Mortality (%)	Total Morbidity (%)	SSI (%)	Anastomotic Leak (%)	Reoperation (%)
Treager, 2023	Non-sarcopenic	230	6.00 (2.98)	2 (0.8)	157 (68)	-	6 (2.6)	8 (3.5)
Treager, 2023	Sarcopenic	67	8.00 (5.30)	1 (1.5)	57 (85)	-	5 (7.5)	5 (7.5)
Erozkan, 2023	Non-sarcopenic	43	6.33 (0.77)	0 (0)	2 (4.7)	-	-	-
Erozkan, 2023	Sarcopenic	351	6.33 (0.77)	3 (8.6)	11 (31.4)	-	-	-
Batista, 2022	Non-sarcopenic	425	6.17 (3.35)	-	-	-	-	-
Batista, 2022	Sarcopenic	214	6.33 (3.73)	-	-	-	-	-
Bocca, 2022	Non-sarcopenic	48	9.8 (1.82)	-	-	-	-	-
Bocca, 2022	Sarcopenic	28	10.55 (1.9)	-	-	-	-	-
Cujipers, 2022	Non-sarcopenic	96	6.33 (4.47)	-	41 (42.7)	-	-	-
Cujipers, 2022	Sarcopenic	142	6.33 (4.47)	-	55 (38.7)	-	-	-
Uehara, 2022	Non-sarcopenic	213	28.75 (15.42)	0 (0)	63 (29.6)	31 (14.6)	30 (14.1)	-
Uehara, 2022	Sarcopenic	49	28.00 (17.45)	0 (0)	23 (46.9)	8 (16.3)	7 (14.3)	-
Giani, 2022	Non-sarcopenic	129	-	-	43.33 (33.3)	-	8/94 (8.5)^a	8 (6.2)
Giani, 2022	Sarcopenic	129	-	-	43.33 (33.3)	-	8/94 (8.5)^a	8 (6.2)
Takenami, 2022	Non-sarcopenic	123	20.5 (8.95)	-	27 (22)	14 (11.4)	-	-
Takenami, 2022	Sarcopenic	86	31.25 (19.43)	-	13 (15.1)	2 (2.3)	-	-
Yang, 2019	Low SI	120	17 (8.38)	-	37 (30.8)	5 (4.2)	4 (3.3)	-
Yang, 2019	High SI	297	19 (10.93)	-	34 (11.4)	7 (2.4)	6 (2.0)	-
Chen 2018	Non-SC and non-visceral obesity	134	16.00 (7.49)	0 (0)	17 (12.7)	-	3 (2.2)	-
Chen 2018	SC	51	19.00 (15.26)	0 (0)	18 (35.3)	-	1 (2.0)	-
Hanaoka, 2017	Mild MPM	105	-	0 (0)	24 (22.9)	4 (3.8)	4 (3.8)	1 (0.1)
Hanaoka, 2017	Severe MPM	28	-	1 (3.6)	13 (46.4)	5 (17.9)	2 (7.1)	2 (7.1)
Ojima, 2019	Low PMI	35	-	-	-	-	-	-
Ojima, 2019	Normal PMI	107	-	-	-	-	-	-
Malietzis, 2016	No myopenia	320	7.66 (5.21)	2 (0.6)	-	-	26 (8.4)	-
Malietzis, 2016	Myopenia	485	8.00 (5.20)	8 (1.6)	-	-	24 (5.2)	-
Richards, 2020	Non-sarcopenic	235	7.00 (2.98)	1 (0.4)^b	81 (34.5)	-	-	-
Richards, 2020	Sarcopenic	115	13.67 (7.51)	4 (3.5)^b	98 (85.2)	-	-	-
Pereira, 2020	Non-sarcopenic	220	-	14 (6.4)	76 (35.0)	27 (12.4)	16 (7.40)	-
Pereira, 2020	Sarcopenic	52	-	6 (11.5)	17 (33.3)	6 (11.8)	6 (11.8)	-
Aro, 2020	Sarcopenic	208	10.40 (5.43)	8 (3.8)^b	61 (29.3)	-	12 (5.8)	-
Aro, 2020	Non-sarcopenic	140	9.60 (7.96)	2 (1.4)^b	36 (25.7)	-	5 (3.6)	-
Nakanishi, 2018	Non-sarcopenic	196	16.3 (12.0)	-	63 (32)	-	-	-
Nakanishi, 2018	Sarcopenic	298	19.4 (17.8)	-	127 (43)	-	-	-
Takeda, 2018	Low SMM	37	-	-	9 (24.3)	0 (0)	1 (2.7)	-
Takeda, 2018	Non-low SMM	107	-	-	32 (29.9)	4 (3.7)	3 (2.8)	-
Pedziwiatr, 2016	Non-sarcopenic	90	5.9 (5.6)	-	25 (27.8)	2 (2.2)	6 (6.7)	-
Pedziwiatr, 2016	Sarcopenic	34	5.7 (3.4)	-	10 (29.4)	3 (8.8)	1 (2.9)	-
van Vugt, 2018	High SMM	404	7.67 (4.46)	-	187 (46.3)	-	-	-
van Vugt, 2018	Low SMM	412	9.00 (5.21)	-	197 (47.8)	-	-	-
Tamagawa, 2018	Non-sarcopenic	42	12.3 (9.8)	3 (3.7)	35 (42.7)	9 (10.98)	3 (3.7)	-
Tamagawa, 2018	Sarcopenic	40	15.9 (14.2)	3 (3.7)	35 (42.7)	9 (10.98)	3 (3.7)	-
Ouchi, 2016	Non-sarcopenic	40	19.25 (8.58)	-	8 (20)	1 (2.5)	2 (5)	-
Ouchi, 2016	Sarcopenic	20	18.00 (9.10)	-	4 (20)	2 (10)	1 (5)	-
Huang, 2015	Non-sarcopenic	125	13.00 (4.50)	0 (0)	30 (24)	-	-	0 (0)
Huang, 2015	Sarcopenic	17	15.00 (8.49)	0 (0)	10 (59)	-	-	0 (0)
Miyamoto, 2015	Non-sarcopenic	165	-	-	-	-	-	-
Miyamoto, 2015	Sarcopenic	55	-	-	-	-	-	-
Jones, 2015	Non-sarcopenic	85	6.23 (2.92)	0 (0)	31 (36.5)	7 (7)	5 (5)	-
Jones, 2015	Sarcopenic	15	7.69 (5.22)	0 (0)	8 (53.3)	7 (7)	5 (5)	-
Reisinger, 2015	Non-sarcopenic	162	11 (0.6)	1 (0.6)	-	-	24/133 (18.0)^a	-
Reisinger, 2015	Sarcopenic	148	11 (0.6)	11 (7.4)	-	-	13/116 (11.2)^a	-
Xiao, 2020	Normal SMI	926	6 (4.9)	3 (0.3)	278 (30)	-	-	-
Xiao, 2020	Low SMI	704	6.9 (7.9)	14 (2.0)	257 (36.5)	-	-	-
Xie, 2020	Non-sarcopenic	166	14.25 (7.20)	-	27 (9.1)	-	-	-
Xie, 2020	Sarcopenic	132	15.25 (7.74)	-	39 (13.1)	-	-	-
Dolan, 2019	Non-sarcopenic	131	8.67 (4.50)	0 (0)	73 (55.7)	-	-	-
Dolan, 2019	Sarcopenic	32	8.67 (4.66)	1 (3.1)	14 (43.8)	-	-	-
Jochum, 2019	Non-sarcopenic	24	10.6 (7.0)	-	7 (30.4)	3 (12.5)^c	1 (4.3)	7 (29)
Jochum, 2019	Sarcopenic	23	9.42 (6.6)	-	15 (62.5)	2 (8.7)^c	3 (12.5)	6 (26)
Lee, 2021	Non-sarcopenic	1178	-	-	-	-	-	-
Lee, 2021	Sarcopenic	1155	-	-	-	-	-	-
Giani, 2020	Non-sarcopenic	130	-	-	36 (27.7)	-	8 (6.2)	-
Giani, 2020	Sarcopenic	43	-	-	23 (54.8)	-	2 (4.6)	-
Chen, 2020	Non-sarcopenic	227	19.00 (6.71)	-	62 (27.3)	-	9 (2.5)	-
Chen, 2020	Sarcopenic	133	20.00 (7.49)	-	51 (38.3)	-	9 (2.5)	-
Olmez, 2020	Non-sarcopenic	112	10.5 (6)	-	51 (45.4)	26 (23.2)	-	-
Olmez, 2020	Sarcopenic	97	12.3 (8.6)	-	46 (47.4)	20 (20.6)	-	-
Souwer, 2020	Q2-Q4 SMM (non-sarcopenic)	131	-	8 (6)	55 (41.9)	-	9 (6.9)	14 (10.7)
Souwer, 2020	Q1 SMM (sarcopenic)	43	-	2 (5)	13 (30.2)	-	2 (4.7)	5 (11.6)
Tankel, 2020	TPI non-sarcopenic	139	-	-	49 (35)	-	-	-
Tankel, 2020	TPI sarcopenic	46	12 (13.77)	-	14 (30)	-	-	-
Okabe, 2019	Non-sarcopenic	109	19.75 (8.90)	-	-	19 (17)	9 (7)	-
Okabe, 2019	Sarcopenic	159	23.00 (10.91)	-	-	29 (18)	11 (7)	-
Herrod, 2019	Non-sarcopenic	118	7.00 (5.25)	-	-	-	2 ( 2)	2 ( 2)
Herrod, 2019	Sarcopenic	51	9.00 (5.34)	-	-	-	4 (8)	4 (8)
van der Kroft, 2018	Non-sarcopenic	30	-	-	-	-	-	-
van der Kroft, 2018	Sarcopenic	33	-	-	-	-	-	-
Schaffler Schaden, 2020	Non-sarcopenic	53	-	-	15 (28.3)	-	-	-
Schaffler Schaden, 2020	Sarcopenic	32	-	-	6 (18.8)	-	-	-

^aOnly some of the patients in this arm had anastomoses.

^b90-day period, not 30.

^cSuperficial surgical site infection only.

Abbreviations - SI: sarcopenia index. SC: sarcopenic. VO: visceral obesity. MPM: morphologic change of the psoas muscle. SMM: skeletal muscle mass. BMI: body mass index. SMD: skeletal muscle density. SMI: skeletal muscle index. Q: quartile. TPI: total psoas muscle index. OR: odds ratio.

Figure 2.

Postoperative morbidity in sarcopenic vs non-sarcopenic patients. Relative risk (RR) shown.

Twenty-six studies (63%) included data on LOS, with comparisons for both patients with and without sarcopenia. The mean difference (MD) in postoperative LOS was 1.46 days longer for patients with sarcopenia (26 studies, 95% CI 0.85-2.07, P < 0.01, I² 82%)), as shown in Figure 3. There was no significant subgroup interaction according to geographic study location (Supplemental Figure 4, X² = 6.40, P = 0.09, I² = 53.1%). There was no observed subgroup interaction according to operative approach (Supplemental Figure 5, X² = 3.08, P = 0.08, I² = 67.5%) or age (Supplemental Figure 6, X² = 7.03, P = 0.07, I² = 57.4%).

Figure 3.

Length of stay (LOS) postoperatively for sarcopenic vs non-sarcopenic patients. Length of stay with standard deviation (SD), as well as mean difference (MD) shown.

Upon pooling data from 13 studies, patients with sarcopenia had increased risk of 30-day postoperative mortality (2.8% vs 1.0%, RR 2.74, 95% CI 1.63-4.62, P < 0.01, I² 0%), as seen in Figure 4. Pooled data of 19 studies with data on anastomotic leaks showed that there was no difference in risk of anastomotic leak between patients with and without sarcopenia (6.1% vs 6.0%, RR 1.01, 95% CI 0.80-1.31, P = 0.86, I² 5%), as seen in Figure 5. As shown in Figure 6, patients with sarcopenia also were more likely to be readmitted within 30 days of surgery (12 studies, RR 1.63 95% CI 1.07-2.49, P = 0.02, I² 43%),).

Figure 4.

30-day postoperative mortality rates in sarcopenic vs non-sarcopenic patients. Relative risk (RR) shown.

Figure 5.

Anastomotic leak rate in sarcopenic vs non-sarcopenic patients. Relative risk (RR) shown.

Figure 6.

30-day readmission rates in sarcopenic vs non-sarcopenic patients. Relative risk (RR) as shown.

No statistically significant reporting biases were detected using Egger’s test for all of the above outcomes (Supplemental Figure 7).

Long-Term Outcomes

Long-term outcomes including OS and DFS at various intervals are shown in Table 2. Three studies with 5-year OS and four studies with 5-year DFS were included in pooled analyses. Patients with sarcopenia had lower 5-year DFS as seen in Figure 7(a) (4 studies, RR 0.91, 95% CI 0.84-0.98, P = 0.01, I² 56%) compared with those without sarcopenia. However, 5-year OS did not show a significant difference between patients with and without sarcopenia, as seen in Figure 7(b) (3 studies, RR 0.88, 95% CI 0.76-1.03, P = 0.11, I² 72%).

Table 2.

Long-Term Outcomes in Sarcopenic vs Non-sarcopenic Patients Following Colorectal Cancer Surgery.

Study	Arm	N per Arm	Readmission (%)	OS (%)	DFS (%)
Traeger, 2023	Non-sarcopenic	230	13 (5.7)	-	-
Traeger, 2023	Sarcopenic	67	6 (9)	-	-
Bocca, 2022	Non-sarcopenic	48	6 (12.5)	-	-
Bocca, 2022	Sarcopenic	28	2 (7.1)	-	-
Uehara, 2022	Non-sarcopenic	213	-	1 year: 205 (96)	-
Uehara, 2022	Sarcopenic	49	-	1 year: 47 (96)	-
Takenami, 2022	Non-sarcopenic	123	0	3 year: (93.4)	3 year: (89.4)
Takenami, 2022	Sarcopenic	86	4 (4.7)	3 year: (84.4)	3 year: (87.9)
Giani, 2022	Non-sarcopenic	-	-	1 year: (95.7), 3 year: (86.0), 5 year: (76.8)	1 year: (89.4)
					3 year: (80.3)
					5 year: (70.6)
	Sarcopenic	-	-	1 year: (82.4), 3 year: (58.8), 5 year: (40.0)	1 year: (69.2)
					3 year: (46.2)
					5 year: (46.2)
Chen, 2018	Non-sarcopenic, non-obesity	134	0	-	-
Chen, 2018	Sarcopenic	51	1 (2)	-	-
Ojima, 2019	Non-sarcopenic	107	-	5 year: 93 (87)	5 year: 83 (78)
Ojima, 2019	Sarcopenic	35		5 year: 21 (61)	5 year: 18 (51)
Richards, 2020	Non-sarcopenic	235	-	1 year: 233 (99.1)	-
Richards, 2020	Sarcopenic	115	-	1 year: 99 (86.1)	-
Takeda, 2018	Non-sarcopenic	107	-	5 year: 100 (93)	5 year: 85 (79)
Takeda, 2018	Sarcopenic	37	-	5-year: 31 (83.2)	5 year: 22 (60.7)
Pedziwiatr, 2016	Non-sarcopenic	90	5 (5.5)	-	-
Pedziwiatr, 2016	Sarcopenic	34	5 (14.7)	-	-
Van Vugt, 2018	Non-sarcopenic	404	-	-	1 year: (92.4)
					3 year: (84.4)
					5 year: (81.1)
	Sarcopenic	412	-	-	1 year: (89.8)
					3 year: (81.1)
					5 year: (77.1)
Ouchi, 2016	Non-sarcopenic	40	1 (2)	-	-
Ouchi, 2016	Sarcopenic	20	1 (5)	-	-
Huang, 2015	Non-sarcopenic	125	4 (3.20)	-	-
Huang, 2015	Sarcopenic	17	2 (1.18)	-	-
Xiao, 2020	Non-sarcopenic	926	143 (15.4)	-	-
Xiao, 2020	Sarcopenic	704	128 (18.2)	-	-
Dolan, 2019	Non-sarcopenic	131	18 (13.7)	1 year: 124 (94.7)	-
Dolan, 2019	Sarcopenic	32	3 (9.4)	1 year: 27 (84.4)	-
Jochum, 2019	Non-sarcopenic	24	8 (34.8%)	-	-
Jochum, 2019	Sarcopenic	23	6 (25%)	-	-
Lee, 2021	Non-sarcopenic	1178		5 year: (95.8)	5 year: (93.2)
Lee, 2021	Sarcopenic	1155		5 year: (92.1)	5 year: (86.2)
Chen, 2020	Non-sarcopenic	227	2 (0.55)
Chen, 2020	Sarcopenic	133	10 (2.78)
Souwer, 2020	Non-sarcopenic (Q1-3)	131	10 (7.6)
Souwer, 2020	Sarcopenic (Q4)	43	8 (19)

Figure 7.

5-year outcomes in sarcopenic vs non-sarcopenic patients including (a) disease-free survival and (b) overall survival (OS). Relative risk (RR) as shown.

Risk of Bias

Risk of bias for observational studies was assessed using the ROBINS-I. The results of this analysis can be seen in Supplemental Figure 8.

Certainty of Evidence

Certainty of evidence for estimates derived from meta-analyses was assessed by GRADE (see Supplemental Figure 9 for further information).

Discussion

Sarcopenia has been associated with poor postoperative outcomes in many fields, especially as it relates to oncology.⁶⁵ This review and meta-analysis analyzes the postoperative short- and long-term outcomes in patients with sarcopenia compared to those without sarcopenia undergoing surgery for colorectal cancer, expanding and updating on previous reviews.^9,10 Low to very-low certainty evidence demonstrated that there was an increase in 30-day postoperative morbidity (40 vs 33%, RR 1.3, 95% CI 1.12-1.50, P < 0.01) and 30-day postoperative mortality rate (3% vs 1%, RR 2.74, 95% CI 1.63-4.62, P < 0.01), as well as a 1.46 day longer LOS for patients with sarcopenia (26 studies, 95% CI 0.85-2.07, P < 0.01). Patients with sarcopenia also had lower 5-year DFS (4 studies, RR 0.91, 95% CI 0.84-0.98, P = 0.01), but there was no significant difference in 5-year OS (3 studies, RR 0.88, 95% CI 0.76-1.03, P = 0.11).

Previous studies and meta-analyses have shown an association between sarcopenia and adverse postoperative outcomes in gastrointestinal oncology patients,^66-68 and colorectal cancer patients in particular.^9,69,70 Our study further confirms the increase in morbidity and mortality, as well as longer LOS and poorer long-term oncologic outcomes. With the median age of diagnosis of colorectal cancer being 68 in women and 65 in men,² many patients are elderly at the time of surgery. With increasing age naturally comes decreasing muscle mass, and the prevalence of sarcopenia becomes greater. An estimated 5%-13% of those age 60-70 and 11%-50% of those 80 years and older have sarcopenia in the general population.⁷¹ These estimates are likely even higher in the colorectal cancer population, ranging from 12% to 60% depending on the study.¹⁰ Thus, the detrimental impact of sarcopenia on operative outcomes in colorectal cancer is highly pervasive, and it is a preoperative prognostic indicator that clinicians must be increasingly aware of and competent at managing.

In addition to the impact of sarcopenia on surgical outcomes, it may also impact how patients tolerate other aspects of multi-modal care. In rectal cancer in particular, where neoadjuvant therapies are becoming increasingly common,⁷² sarcopenia can increase treatment-related complications.⁷³ Meta-analysis of the colorectal cancer patient population has shown that patients with sarcopenia are more likely to have premature termination of chemotherapy treatment with FOLFOX.⁷³ Specifically, observational data has shown higher rates of multiple systemic complications, such as neutropenia, neuropathy, thrombocytopenia, mucositis, and others in patients with sarcopenia.⁷⁴ Although there are limited data, chemotherapeutic agents are also thought to cause or worsen sarcopenia,⁷⁵ which this and other studies have not accounted for when using pre-treatment CT scans for sarcopenia analysis. Thus, as contemporary neoadjuvant therapies become more ubiquitous in clinical practice, the prevalence and impact of sarcopenia on perioperative outcomes may heighten.

The relationship between sarcopenia and adverse outcomes highlights a need to attempt to modify this risk factor through prehabilitation. Prehabilitation may include a variety of interventions, including exercise, nutrition, patient education, and geriatric specialist assessment.⁷⁶ Randomized studies have shown that prehabilitation can significantly improve objective measures such as peak volume of oxygen consumption,⁷⁷ 6-minute walk test,⁷⁸ and muscle mass⁷⁹ in patients undergoing neoadjuvant therapy before rectal cancer resection when compared to a control group without prehabilitation. A recent RCT of 251 patients with colon or rectal cancer showed that prehabilitation with a three times weekly exercise program, nutritional intervention, psychological support, and smoking cessation led to significant reduction in severe postoperative complications as well as medical complications in colorectal cancer patients.⁸⁰ However, meta-analysis of the many RCTs studying prehabilitation has not yet shown significant decreases in postoperative complications.⁸¹

This review and meta-analysis has strengths such as the number of included studies and patients, the comprehensive risk of bias assessment, and GRADE assessment. However, the study limitations include low to very-low certainty of evidence, inclusion of only non-randomized data, and a heterogeneity of patients, pathologies, and methods of sarcopenia assessment between studies. Although almost all included studies used analysis of psoas muscle at the L3 level on CT imaging to diagnose sarcopenia, there were differences among studies’ choice of cutoff values (pre-determined cutoffs vs quartiles) or methods of psoas analysis (short to long axis ratio vs psoas area). This heterogeneity among studies induces uncertainty in our findings and limited the statistical power of certain data analyses. Regarding long-term outcomes, few studies reported 5-year OS and DFS, limiting our statistical power and decreasing the confidence in our effect estimates. The GRADE assessment of the overall quality of evidence was significantly impacted by indirectness and inconsistency. It may still be difficult to ascertain the degree to which sarcopenia impact short- and long-term colorectal surgery postoperative outcomes given the low to very-low certainty of evidence in this meta-analysis. Nonetheless, an RCT aimed at assessing sarcopenia is not possible, and thus, we will have to rely on these meta-analyses of observational data to inform our clinical practices. Lastly, the observational nature of the included data places these findings at risk of selection and confounding bias.

Overall, the presence of preoperative sarcopenia in patients undergoing surgical resection for colorectal cancer is associated with poorer short- and long-term outcomes, including postoperative morbidity and mortality, as well as long-term oncologic outcomes. These data are in keeping with previous systematic reviews and meta-analyses evaluating sarcopenia in the perioperative period. The significant negative impacts associated with sarcopenia should prompt clinicians to further study, develop, and implement prehabilitation programs aimed at building muscle mass and preventing exacerbation of sarcopenia in the preoperative period.

Supplemental Material

Supplemental Material - The Impact of Sarcopenia on Postoperative Outcomes in Colorectal Cancer Surgery: An Updated Systematic Review and Meta-Analysis

Supplemental Material for The Impact of Sarcopenia on Postoperative Outcomes in Colorectal Cancer Surgery: An Updated Systematic Review and Meta-Analysis by Sara Keshavjee, Tyler Mckechnie, Victoria Shi, Muhammad Abbas, Elena Huang, Nalin Amin, Dennis Hong, and Cagla Eskicioglu in The American Surgeon™.

Supplemental Material

Supplemental Material - The Impact of Sarcopenia on Postoperative Outcomes in Colorectal Cancer Surgery: An Updated Systematic Review and Meta-Analysis

Footnotes

Author’s Contributions

Conception and design of the study: all authors; acquisition of data: Keshavjee, Shi, Abbas, Huang, and McKechnie; analysis and interpretation of data: all authors; drafting and revision of the manuscript: all authors; approval of the final version of the manuscript: all authors; and agreement to be accountable for all aspects of the work: all authors.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Prospero Registration Number

CRD42023493416.

ORCID iD

Sara Keshavjee

Supplemental Material

Supplemental material for this article is available online.

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Supplementary Material

Please find the following supplemental material available below.

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