The Prognostic Role of Sarcopenia in Long-term Outcomes of Colorectal Cancer Pathological Stage III Cases: A Propensity Score-matched Analysis

doi:10.21203/rs.3.rs-3863855/v1

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The Prognostic Role of Sarcopenia in Long-term Outcomes of Colorectal Cancer Pathological Stage III Cases: A Propensity Score-matched Analysis

https://doi.org/10.21203/rs.3.rs-3863855/v1

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Background

The prognostic role of sarcopenia for colorectal cancer (CRC) surgery remains controversial. We evaluated the prognostic role of sarcopenia in patients with pathological Stage III (pStage III) CRC.

Methods

We retrospectively examined 113 patients with pStage III CRC who underwent curative resection. We assessed sarcopenia based on a decrease in muscle mass; specifically, the cross-sectional area of the skeletal muscle at the level of the third lumbar vertebra was measured using computed tomography, and low values were defined as sarcopenia. The effects of sarcopenia on overall survival (OS) and recurrence-free survival (RFS) were investigated. The propensity score matching method was used to adjust for patient background.

Results

Of the 113 cases, 10 were excluded owing to lack of information, and 103 cases were analyzed. Of 103 patients, 67 (65.0%) had sarcopenia. Patients in the sarcopenia group were predominantly female and had a high number of right-sided lesions. Using propensity score matching, the sarcopenia and control groups were matched in 33 patients, and sex and tumor location were almost equal between the groups. Postoperative hospital stay was significantly longer in the sarcopenia group than in the non-sarcopenia group (median, 15 days vs. 10 days; p = 0.020). The sarcopenia group had significantly worse OS (5-year: 64.0% vs. 90.9%; hazard ratio, 4.870; 95% confidence interval, 1.371–17.306; p = 0.007) and RFS (5-year: 52.1% vs. 78.8%; hazard ratio, 2.654; 95% confidence interval, 1.078–6.537; p = 0.027) than the non-sarcopenia group.

Conclusions

Sarcopenia is a poor prognostic factor for both OS and RFS in patients with pStage III CRC.

sarcopenia

colorectal cancer

skeletal muscle index

propensity score matching

Sarcopenia is defined as the loss of skeletal muscle mass and strength [1, 2]. Sarcopenia affects the survival of patients with various diseases, including cardiovascular, pulmonary, and inflammatory bowel diseases [3–6]. The impact of sarcopenia on the short- and long-term outcomes of colorectal cancer remains uncertain and controversial [7]. Some reports have suggested that sarcopenia is a significant negative prognostic factor for overall survival (OS) [8–12], whereas others disagree [13]. The influence of sarcopenia on recurrence-free survival (RFS) and disease-free survival remains controversial [9–11, 13].

This study aimed to clarify the effects of sarcopenia on the survival of patients with colorectal cancer. The survival of patients with colorectal cancer greatly depends on the presence or absence of lymph node and distant metastases. Therefore, to investigate the effect of sarcopenia on the long-term survival of patients with colorectal cancer, we focused on patients with lymph node metastasis and without distant metastasis, defined as pathological Stage III (pStage III) in the TNM classification, according to the 8th edition of the American Joint Committee on Cancer staging [14].

Patients

Patients with pStage III colorectal adenocarcinoma admitted to the Shiga University of Medical Science Hospital who underwent primary tumor resection between January 2014 and December 2018 were enrolled. Abdominal computed tomography (CT) was performed within 2 months of surgery. The following data were collected retrospectively: demographic data (age, sex, height, weight, body mass index, American Society of Anesthesiologists physical status), laboratory data (albumin, number of lymphocytes, C-reactive protein, carcinoembryonic antigen, carbohydrate antigen 19 − 9), operative findings (operative time, amount of bleeding, laparoscopic surgery or open surgery), tumor-specific data (tumor location, size, histology, tumor depth, number of lymph node metastases), and postoperative course (postoperative complication, postoperative hospital stay, adjuvant chemotherapy [AC], recurrence, survival). RFS was defined as the period between the date of surgery and the date of confirmation of survival without cancer recurrence. OS was defined as the period between the date of surgery and the date of survival confirmation.

Assessment of muscle

In this study, we assessed sarcopenia based on a decrease in muscle mass. Specifically, the cross-sectional area of the skeletal muscles at the L3 level was measured on CT images using image analysis software (OsiriX MD version 13.0.1, Pixmeo, Geneva, Switzerland). Skeletal muscle was identified as Hounsfield units (HUs) of -29 to + 100 HU (Fig. 1). The muscles at L3 included the psoas, erector spinae, quadratus lumborum, transversus abdominis, internal oblique, external oblique, and rectus abdominis. Sarcopenia was determined by the skeletal muscle index (L3 skeletal muscle area divided by height squared) using the skeletal muscle index cutoff values for identifying sarcopenia in liver disease of 42 cm²/m² for men and 38 cm²/m² for women, as proposed by the Japan Society of Hepatology and widely used as an indicator of sarcopenia among the Japanese people [15].

Statistical analysis

Continuous variables are expressed as medians (interquartile ranges). The χ2 test, Fisher’s exact test, and Mann–Whitney U test were used as appropriate. Survival curves were estimated using the Kaplan–Meier (KP) method and analyzed using the log-rank test to determine statistical differences between the groups. Cox regression analysis was performed to estimate the risks of OS and RFS. Statistical significance was set at p < 0.05. All statistical analyses were performed using the SPSS version 25 software (IBM Corp., Armonk, New York, USA). We used PSM to balance the baseline characteristics of the sarcopenia and non-sarcopenia groups. PSM was performed in a 1:1 ratio without replacement using a caliper of 0.08.

Patients

Of 113 consecutive patients with pStage III colorectal adenocarcinoma who underwent resection of primary lesions in Shiga University of Medical Science Hospital during the specified period, 9 patients without appropriate CT images and 1 patient without physical data were excluded; therefore, a total of 103 patients were enrolled in this study (Fig. 2). The median (interquartile range) follow-up period was 60 (44–69) months. During follow-up, 29 patients (28.2%) developed recurrence and 23 patients (22.3%) died.

Comparison of clinical background, characteristics, and postoperative outcome between sarcopenia and non-sarcopenia groups

Of the 103 patients, 67 (65.0%) belonged to the sarcopenia group, and 36 (35%) belonged to the non-sarcopenia group. Table 1 shows the clinical background and characteristics of the patients in both groups. The sarcopenia group comprised predominantly females, short in stature, and light in weight. In addition, patients in the sarcopenia group tended to be older and had longer postoperative hospital stays than those in the non-sarcopenia group. Furthermore, patients in the sarcopenia group had more right-sided lesions than those in the non-sarcopenia group.

Comparison of clinical background, characteristics, and postoperative outcome between sarcopenia and non-sarcopenia groups after PSM

To match the background factors, PSM was performed using age, sex, tumor location, and N factor according to the TNM classification of the 8th edition of the American Joint Committee on Cancer staging (the number of lymph node metastases 1–3 for N1 and ≥ 4 for N2 [14]) as covariates. Table 2 shows the clinical background and characteristics of both groups after PSM. Sex and tumor location were almost equal between the groups, and differences in the N factor were alleviated. Oncological factors, such as albumin, lymphocytes, C-reactive protein, carcinoembryonic antigen, and carbohydrate antigen 19 − 9, showed no significant differences between the groups. In addition, there was no significant difference in postoperative complications and surgical site infection. Postoperative hospital stay was longer in the sarcopenia group (median, 15 [10-22.5] days vs. 10 [9-13.5] days; p = 0.020) than in the non-sarcopenia group. The proportion of patients who received AC was lower in the sarcopenia group than in the non-sarcopenia group; however, the difference was not statistically significant (60.6% vs. 78.8%; p = 0.108). Among patients administered AC, the rate of oxaliplatin (OX)-containing regimens did not differ between the groups (45.0% vs. 50.0%). The AC completion rate in patients who were administered AC tended to be lower in the sarcopenia group than in the non-sarcopenia group (62.5% vs. 84.6%, p = 0.116). Among all patients in each group, fewer patients completed AC in the sarcopenia group than in the non-sarcopenia group (39.3% [13 out of 33 patients] vs. 66.7% [22 out of 33 patients], p = 0.011).

Long-term survival after surgery

Figure 3(a) shows the KP curves for OS between the sarcopenia and non-sarcopenia groups before PSM. The log-rank test showed poor OS in the sarcopenia group (5-year OS rate: sarcopenia vs. non-sarcopenia, 72.2% vs. 88.6%; hazard ratio [HR], 3.046; 95% confidence interval [CI], 1.034–8.972; p = 0.034). Figure 3(b) shows the KP curves for RFS between the sarcopenia and non-sarcopenia groups before PSM. No significant difference in RFS was observed between the sarcopenia and non-sarcopenia groups in the log-rank test (5-year RFS, 65.6% vs. 79.8%; HR, 1.824; 95% CI, 0.774–4.295; p = 0.163).

Figure 4(a) shows the KP curves for OS between the sarcopenia and non-sarcopenia groups after PSM. The log-rank test showed poor OS in the sarcopenia group (5-year OS rate, 64.0% vs. 90.9%; HR, 4.870; 95% CI, 1.371–17.306; p = 0.007). The difference between the two groups was greater than that before PSM. Figure 4(b) shows the KP curves for RFS between the sarcopenia and non-sarcopenia groups after PSM. Unlike before PSM, the log-rank test showed significantly poorer RFS in the sarcopenia group than in the non-sarcopenia group after PSM (5-year RFS, 52.1% vs. 78.8%; HR, 2.654; 95% CI, 1.078–6.537; p = 0.027).

This study revealed that sarcopenia was not associated with postoperative complications or surgical site infection; however, sarcopenia was associated with a long postoperative hospital stay in the short-term outcome. After equalizing the background factors with PSM, the sarcopenia group had worse long-term survival in terms of OS and RFS than the non-sarcopenia group.

Sarcopenia, first proposed by Rosenberg, is characterized by decreased muscle mass and function [1, 2]. Although sarcopenia has been reported to be a negative prognostic factor for the development of physical disability and mortality in various diseases, such as cardiovascular, pulmonary, and inflammatory bowel diseases [3–6], the effect of sarcopenia on postoperative outcomes and long-term prognosis of patients with colorectal cancer remains controversial [7].

Regarding postoperative outcomes, some reports have indicated that sarcopenia is associated with long hospital stays [8, 13, 16, 17]. In terms of postoperative complications, whether sarcopenia is a significant risk factor [13, 16, 18] or not [8, 19, 20] remains controversial. In our study, sarcopenia did not affect postoperative complications or surgical site infections. Pędziwiatr et al. pointed out that the introduction of laparoscopic surgery and enhanced recovery after surgery protocol may offset the negative impact of sarcopenia on postoperative complications [19]. To the best of our knowledge, there have been no reports indicating that preoperative nutritional therapy and pre-rehabilitation intervention trials improve sarcopenia and reduce postoperative complications. It is the next research topic for future investigation.

Regarding the long-term prognosis of patients with postoperative colorectal cancer, some reports have suggested that sarcopenia is a significant negative prognostic factor for OS [8–12], whereas others have reported the opposite [13]. In terms of RFS and disease-free survival, some reports have indicated that sarcopenia is a negative prognostic factor [10, 11], whereas others have not [9, 13]. In the present study, the sarcopenia group had significantly worse prognoses than the non-sarcopenia group in terms of OS and RFS.

The AC of fluoropyrimidine administered after curative resection for patients with pStage III colorectal cancer improves their prognosis when they are in good general condition, have preserved major organ function, and have no serious comorbidities [21]. Adding OX to fluoropyrimidine increases side effects such as peripheral neuropathy, but further improvement in prognosis can be expected [22]. However, the effects of OX in older patients have not been well established [23]. In this study, the adaptation rate of the OX-containing regimen in patients who were administered AC was almost the same in the sarcopenia and non-sarcopenia groups (45.0% vs. 50.0%). In contrast, the proportion of patients who received AC (60.6% vs. 78.8%, p = 0.108) and the completion rate of AC (62.5% vs. 84.6%, p = 0.116) tended to be lower in the sarcopenia group than in the non-sarcopenia group, and fewer patients completed AC in the sarcopenia group than in the non-sarcopenia group (39.3% vs. 66.7%, p = 0.011), which may have influenced the poor prognosis.

Loss of muscle mass in sarcopenia is often defined as less than 2 standard deviations in a young healthy adult [24]. However, which muscle mass should be measured and what population should be selected as the control have not been determined; therefore, the muscles to be examined and the threshold for sarcopenia vary among studies [7]. Although it may be difficult to set a uniform threshold for sarcopenia because the physique and nutritional status differ among races, a consensus is necessary.

It is speculated that lifestyle habits, such as decreased physical activity and reduced food intake, lead to sarcopenia in older people. Various molecular mechanisms underlying sarcopenia have been proposed. Sex hormones, such as testosterone and estrogen, have been suggested to be involved in the mechanisms leading to sarcopenia. Muscle catabolism progresses when these are reduced [25]. Insulin prevents muscle catabolism. Therefore, increased insulin resistance with aging leads to increased muscle catabolism and sarcopenia [26]. Elucidating the molecular mechanisms underlying sarcopenia may lead to the development of drugs that directly target sarcopenia.

This study had some limitations. First, this was a retrospective study conducted at a single institution, and the number of patients was limited. Prospective multicenter studies with a large number of patients are needed to confirm our results. Second, the study population was Japanese. The Japanese people are generally small and thin compared with those in Western countries. Therefore, it is necessary to consider whether these results can be generalized to other populations. Third, our study was limited to patients with pStage III colorectal cancer. Whether sarcopenia affects the outcomes of colorectal cancer at other stages is a topic for future investigation.

In conclusion,, sarcopenia is a poor prognostic factor for both OS and RFS in patients with pStage III CRC.

Ethical Considerations

This retrospective, single-center study was approved by the ethics committee of Shiga University of Medical Science (R2019-331). The need for consent was waived, and an opt-out policy was implemented. Clinical data were collected from the medical records and anonymized for analysis.

Conflict of Interest Disclosure Statement

The authors declare that they have no competing interests.

Author Contributions

MK carried out the design of the study, collected the clinical data, and drafted the manuscript. All authors participated in the manuscript’s design and coordination and helped to draft the manuscript. All authors have read the draft, revised it critically, and approved the final manuscript.

Acknowledgement

We thank Jun Matsubayashi at the Center for Clinical Research and Advanced Medicine, Shiga University of Medical Science, for his advice on the statistical analysis.

Data Availability Statement

The datasets supporting the conclusions of this article are included within the article.

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TABLE 1. Clinical Background and Characteristics of the Patients before PSM
Patients (N=102)	Sarcopenia (N=67 )	Non-Sarcopenia (N=36 )	P
Age (years)	71 (65-77)	66 (57.5-74.5)	0.084
Male/female	36/31	28/8	0.016
Hight (cm)	159.7 (151.8-164.4)	161.7 (157.8-167.3)	0.047
Body weight (kg)	52.0 (47.4-59.9)	64.5 (55.9-73.6)	<0.001
Body mass index (kg/m2)	20.6 (19.3-23.3)	24.4 (20.8-27.0)	<0.001
ASA-PS 1/2/3	6/24/4	13/44/8	0.953
Tumor location (Right side/Left side)	22/44	5/29	0.047
Tumor histology (muc, por, sig/ others)	5/62	2/33	0.547
Tumor invasion depth (T1/T2/T3/T4)	2/5/43/17	2/5/24/5	0.413
Lymph node metastases (N1/N2)	40/27	27/9	0.121
Albumin (g/dL)	3.85 (3.50-4.10)	3.90 (3.60-4.20)	0.131
Lymphocyte (/μL)	1350 (1025-1625)	1205 (1038-1714)	0.926
CRP (mg/dL)	0.11 (0.05-0.36)	0.11 (0.06-0.22)	0.546
CEA　(ng/mL)	5.6 (2.9-8.7)	4.2 (2.3-11.1)	0.646
CA19-9 (U/mL)	18.5 (10.0-32.8)	15.0 (9.0-28.0)	0.320
Skeletal muscle index (cm2/m2)	31.9 (26.5-36.8)	46.1 (42.9-49.8)	<0.001
Complication CD grade ≧3 (yes/no)	6/61	4/32	0.487
Surgical site infection (yes/no)	8/59	4/32	0.587
Laparoscopic/Open surgery	63/4	35/1	0.426
Operation time (min)	269 (207-362)	261 (204.8-326.5)	0.777
Amount of bleeding (g)	50 (0-229)	50 (0-142.5)	0.497
Postoperative hospital stay (days)	11 (10-20)	10 (9-13.8)	0.080
Adjuvant chemotherapy (yes/no)	48/18	29/7	0.380
OX containing regimen / oral FP	26/22	15/14	0.835
Completion / incompletion†	32/14	25/4	0.084

Values are shown as the median (IQR) or as the number of patients.

Abbreviations: PSM, Propensity score matching; CRP, C-reactive protein; CEA, Carcinoembryonic antigen; CA 19-9; Carbohydrate antigen 19-9, CD, Clavien-Dindo classification; OX, Oxaliplatin; FP, fluoropyrimidine.

†Two patients details unknown due to transfer.

TABLE 2. Clinical Background and Characteristics of the Patients after PSM
Patients (N=66)	Sarcopenia (N=33)	Non-Sarcopenia (N=33 )	P
Age (years)	72.0 (66.5-80.0)	66 (57.5-74.5)	0.076
Male/female	24/9	25/8	0.500
Hight (cm)	162.0 (154.2-168.6)	161.4 (157.2-167.7)	0.644
Body weight (kg)	53.9 (48.9-63.4)	64.5 (56.1-73.1)	<0.001
Body mass index (kg/m2)	21.4 (19.8-23.3)	24.6 (22.7-26.6)	<0.001
ASA-PS 1/2/3	6/23/4	5/24/4	0.945
Tumor location (Right side/Left side)	6/27	5/28	0.500
Tumor histology (muc, por, sig/ others)	3/30	2/31	0.500
Tumor invasion depth (T1/T2/T3/T4)	1/1/22/9	1/4/23/5	0.397
Lymph node metastases (N1/N2)	26/7	24/9	0.387
Albumin (g/dL)	3.8 (3.4-4.1)	3.8 (3.6-4.2)	0.224
Lymphocyte (/μL)	1356 (1012-1630)	1206 (1049-1684)	0.763
CRP (mg/dL)	0.1 (0.05-0.30)	0.11 (0.06-0.21)	0.793
CEA　(ng/mL)	5.0 (2.4-8.6)	3.9 (2.4-10.8)	0.995
CA19-9 (U/mL)	15.0 (8.0-29.0)	14.0 (9.0-31.0)	0.904
Skeletal muscle index (cm2/m2)	32.05 (27.60-38.18)	46.02 (42.94-49.72)	<0.001
Complication CD grade ≧3 (yes/no)	3/30	4/29	0.500
Surgical site infection (yes/no)	6/27	3/30	0.238
Laparoscopic/Open surgery	32/1	32/1	0.754
Operation time (min)	285 (232-398)	248 (197-325)	0.082
Amount of bleeding (g)	148 (0-316)	45 (0-120)	0.064
Postoperative hospital stay (days)	15 (10-22.5)	10 (9-13.5)	0.020
Adjuvant chemotherapy (yes/no)	20/13	26/7	0.108
OX containing regimen / oral FP	9/11	13/13	0.485
Completion / incompletion†	13/7	22/4	0.116

Values are shown as the median (IQR) or as the number of patients.

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The Prognostic Role of Sarcopenia in Long-term Outcomes of Colorectal Cancer Pathological Stage III Cases: A Propensity Score-matched Analysis

Status:

Version 1

Abstract

Background

Methods

Results

Conclusions

Figures

Introduction

Patients and methods

Patients

Assessment of muscle

Statistical analysis

Results

Patients

Comparison of clinical background, characteristics, and postoperative outcome between sarcopenia and non-sarcopenia groups

Comparison of clinical background, characteristics, and postoperative outcome between sarcopenia and non-sarcopenia groups after PSM

Long-term survival after surgery

Discussion

Declarations

Ethical Considerations

Conflict of Interest Disclosure Statement

Author Contributions

Acknowledgement

Data Availability Statement

References

Tables

Status:

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