Advertisement
Browse Subject Areas
?

Click through the PLOS taxonomy to find articles in your field.

For more information about PLOS Subject Areas, click here.

  • Loading metrics

Open Access

Peer-reviewed

Research Article

Predictive role of preoperative sarcopenia for long-term survival in rectal cancer patients: A meta-analysis

  • Qiutong Su ,

    Roles Conceptualization, Data curation, Software, Writing – original draft

    ss5323001@163.com

    Affiliation Department of Gastroenterology and Hepatology, West China Hospital, Sichuan University/West China School of Nursing, Sichuan University, Chengdu, China

    ⨯
  • Jia Shen

    Roles Data curation, Formal analysis, Writing – review & editing

    Affiliation Department of Critical Care Medicine, West China Hospital, Sichuan University/West China School of Nursing, Sichuan University, Chengdu, China

    ⨯

Abstract

Purpose

To identify the predictive role of sarcopenia in long-term survival among rectal cancer patients who underwent surgery based on available evidence.

Methods

The Medline, EMBASE and Web of Science databases were searched up to October 20, 2023, for relevant studies. Overall survival (OS), disease-free survival (DFS) and cancer-specific survival (CSS) were the endpoints. Hazard ratios (HRs) and 95% confidence intervals (CIs) were combined to evaluate the association between sarcopenia and survival.

Results

Fifteen studies with 4283 patients were included. The pooled results demonstrated that preoperative sarcopenia significantly predicted poorer OS (HR = 2.07, 95% CI = 1.67–2.57, P<0.001), DFS (HR = 1.85, 95% CI = 1.39–2.48, P<0.001) and CSS (HR = 1.83, 95% CI = 1.31–2.56, P<0.001). Furthermore, subgroup analysis based on neoadjuvant therapy indicated that sarcopenia was a risk factor for worse OS and DFS in patients who received (OS: HR = 2.44, P<0.001; DFS: HR = 2.16, P<0.001) but not in those who did not receive (OS: HR = 2.44, P<0.001; DDFS: HR = 1.86, P = 0.002) neoadjuvant chemoradiotherapy. In addition, subgroup analysis based on sample size and ethnicity showed similar results.

Conclusion

Preoperative sarcopenia is significantly related to poor survival in surgical rectal cancer patients and could serve as a novel and valuable predictor of long-term prognosis in these patients.

Citation: Su Q, Shen J (2024) Predictive role of preoperative sarcopenia for long-term survival in rectal cancer patients: A meta-analysis. PLoS ONE 19(5): e0303494. https://doi.org/10.1371/journal.pone.0303494

Editor: Zubing Mei, Shuguang Hospital, CHINA

Received: November 22, 2023; Accepted: April 25, 2024; Published: May 21, 2024

Copyright: © 2024 Su, Shen. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All data generated or analyzed during this study are included in this published article.

Funding: The author(s) received no specific funding for this work.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Colorectal cancer is one of the most common malignant tumors of the digestive system in China [1, 2]. According to reports, in 2015, there were 387,600 new cases of colorectal cancer in China, ranking fourth in incidence among all malignant tumors. Colorectal cancer accounts for 8.01% of all cancer deaths in China, ranking fifth in the spectrum of cancer deaths and making it one of the leading causes of malignant tumor-related deaths in the country [3]. Compared to those in foreign countries, colorectal cancer in China is more commonly located in the rectum [4]. Generally, surgery is the primary treatment for rectal cancer patients. However, accurately predicting postoperative survival has always been a challenging issue in clinical practice.

Malnutrition is a common issue among cancer patients, and many tumor patients inevitably experience weight loss, which has adverse effects on cancer treatment and prognosis [5, 6]. Weight loss may result from reduced nutritional intake, such as anorexia, or from tumor-related consumption. Additionally, the side effects of antitumor treatments can exacerbate this condition [7, 8]. Sarcopenia refers to a progressive and generalized skeletal muscle disorder associated with increased risks of adverse outcomes such as falls, fractures, physical disability, and mortality. Research has confirmed a close association between sarcopenia and various chronic diseases, including chronic obstructive pulmonary disease (COPD), chronic heart failure, and chronic kidney disease [9, 10]. The diagnosis of sarcopenia primarily involves assessing muscle mass, muscle strength, and physical performance. The final confirmation is made by determining the presence of low muscle mass. Furthermore, studies indicate that preexisting sarcopenia is prevalent among cancer patients and can adversely affect their prognosis. It has been reported that sarcopenia can lead to poor prognosis in several types of cancers, such as lung cancer, esophageal cancer and gastric cancer [11–13]. However, for now, the association between sarcopenia and long-term prognosis in rectal cancer patients who underwent surgery has not been determined.

Therefore, the aim of this meta-analysis was to further clarify the predictive role of preoperative sarcopenia for long-term survival among surgical rectal cancer patients.

Materials and methods

This meta-analysis was conducted according to the Preferred Reporting Items for Systematic Review and Meta-Analyses 2020 [14].

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. For this type of study, formal consent is not needed.

Literature search

The Medline, EMBASE and Web of Science databases were searched from inception to October 20, 2023. In this meta-analysis, the following terms were used during the search: sarcopenia, rectal, rectum, cancer, tumor, neoplasm, carcinoma, surgery, resection, preoperative, prognosis, prognostic and survival. MeSH terms and free texts were applied. The specific search strategies used for each database are presented in S1 File.

Inclusion criteria

Studies that met the following criteria were included in our meta-analysis: 1) patients were diagnosed with primary rectal cancer and received surgical therapy; 2) sarcopenia was defined according to the skeletal muscle index (SMI), psoas muscle mass index (PMI) or other similar indicators before surgery; 3) patients were divided into sarcopenia and nonsarcopenia groups, and overall survival (OS), disease-free survival (DFS) and (or) cancer-specific survival (CSS) were compared between groups; 4) hazard ratios (HRs) with 95% confidence intervals (CIs) for OS, DFS and CSS were reported; and 5) studies were published in English.

Exclusion criteria

The exclusion criteria for studies were as follows: 1) insufficient, duplicated or overlapped data; 2) editorials, animal trials, case reports or reviews; and 3) studies that did not report HRs with 95% CIs for survival, including studies providing Kaplan–Meier survival curves because of significant bias in the calculation of HRs with 95% CIs from Kaplan–Meier survival curves.

Data collection

We collected the following information from each included study: the first author, publication year, sample size, country, TNM stage, history of neoadjuvant therapy and adjuvant therapy, definition of sarcopenia, endpoint, follow-up period, HR with corresponding 95% CI and source of HRs (multivariate analysis or univariate analysis).

Quality assessment

All included studies were cohort studies; thus, the methodological quality was evaluated according to the Newcastle–Ottawa Scale (NOS) score, and studies with NOS scores >5 were defined as high-quality studies [15].

Statistical analysis

All analyses were performed with STATA version 15.0 software. The heterogeneity between studies was calculated by I2 statistics and the Q test. If significant heterogeneity was detected, represented by I2 > 50% and/or P < 0.1, the random effects model was applied; otherwise, the fixed effects model was applied [16]. The HRs with 95% CIs from multiple regression models were applied whenever available. The hazard ratio (HR) and 95% confidence interval (CI) were combined to evaluate the relationship between preoperative survival and survival. Subgroup analysis based on the history of neoadjuvant therapy, sample size and ethnicity was performed. Sensitivity analysis was performed to detect the sources of heterogeneity and assess the stability of the pooled results. In addition, Begg’s funnel plot and Egger’s test were conducted to detect publication bias, and significant publication bias was defined as P < 0.05 [17, 18]. If obvious publication bias was detected, then the fill-and-trim method was applied to identify potentially unpublished studies [19].

Results

Literature search

As shown in Fig 1, 214 records were found in these three databases (PubMed: n = 54, EMBASE: n = 77 and Web of Science: n = 83), and 39 duplicated records were removed. After reviewing the titles, 126 records were excluded. Then, 26 additional publications were excluded after reviewing the abstracts. After carefully reviewing the full texts, 15 studies were eventually included in this meta-analysis [20–34].

thumbnail
Download:
Fig 1. Prisma flow diagram of this meta-analysis.

https://doi.org/10.1371/journal.pone.0303494.g001

Basic characteristics of the included studies

Detailed information about the included studies is presented in Table 1. All included studies were retrospective. A total of 4283 patients were enrolled, and the sample size ranged from 46 to 1384 patients. Most related studies were from Asian countries, including China, Korea, South Korea and Japan, and sarcopenia was evaluated according to the SMI in most studies. In addition, all included studies were high-quality studies with an NOS score ≥6.

thumbnail
Download:
Table 1. Basic characteristics of included studies.

https://doi.org/10.1371/journal.pone.0303494.t001

Predictive role of preoperative sarcopenia for OS in rectal cancer patients

Thirteen studies explored the relationship between sarcopenia and OS among surgical rectal cancer patients [20–29, 31, 32, 34]. The pooled results demonstrated that the presence of preoperative sarcopenia was significantly related to poor OS (hazard ratio (HR) = 2.07, 95% CI = 1.67–2.57, P<0.001; I2 = 39.5%, P = 0.071) (Fig 2). Subgroup analysis stratified by history of neoadjuvant therapy revealed that both patients with (HR = 2.44, 95% CI = 1.54–3.87, P<0.001; I2 = 0.0%, P = 0.432) [20, 23, 28, 32] and without (HR = 2.44, 95% CI = 1.74–3.42, P<0.001; I2 = 0.0%, P = 0.561) [22, 27, 29] neoadjuvant chemoradiotherapy-related sarcopenia had worse OS. In addition, subgroup analyses based on sample size (<200 vs. ≥200) and ethnicity (Asian vs. non-Asian) showed similar results (Table 2).

thumbnail
Download:
Fig 2. Predictive role of preoperative sarcopenia for overall survival in rectal cancer patients.

https://doi.org/10.1371/journal.pone.0303494.g002

thumbnail
Download:
Table 2. Results of pooled analysis.

https://doi.org/10.1371/journal.pone.0303494.t002

Predictive role of preoperative sarcopenia for DFS in rectal cancer patients

Twelve studies reported the association between sarcopenia and DFS in surgical rectal cancer patients [20–22, 24, 26, 27, 29–34]. The pooled results indicated that preoperative sarcopenia significantly predicted poor DFS (hazard ratio (HR) = 1.85, 95% CI = 1.39–2.48, P<0.001; I2 = 58.5%, P = 0.005) (Fig 3). Moreover, subgroup analysis based on the history of neoadjuvant therapy revealed similar results (patients who received neoadjuvant chemoradiotherapy: HR = 2.16, 95% CI = 1.42–3.31, P<0.001; I2 = 0.0%, P = 0.485 [20, 30, 32, 33]; patients who did not receive neoadjuvant chemoradiotherapy: HR = 1.86, 95% CI = 1.25–2.75, P = 0.002; I2 = 30.8%, P = 0.236 [22, 27, 29]). In addition, subgroup analyses based on sample size (<150 vs. ≥150) and ethnicity (Asian vs. non-Asian) produced similar results (Table 2).

thumbnail
Download:
Fig 3. Predictive role of preoperative sarcopenia for disease-free survival in rectal cancer patients.

https://doi.org/10.1371/journal.pone.0303494.g003

Predictive role of preoperative sarcopenia for CSS in rectal cancer patients

Only four studies have explored the association between sarcopenia and postoperative CSS in rectal cancer patients [22, 25, 29, 31]. The pooled results verified that preoperative sarcopenia also predicted worse CSS (hazard ratio (HR) = 1.83, 95% CI = 1.31–2.56, P<0.001; I2 = 0.0%, P = 0.514) (Fig 4).

thumbnail
Download:
Fig 4. Predictive role of preoperative sarcopenia for cancer-specific survival in rectal cancer patients.

https://doi.org/10.1371/journal.pone.0303494.g004

Sensitivity analysis

Sensitivity analysis of the relationship between preoperative sarcopenia incidence and OS and DFS was performed. According to Fig 5A and 5B, the pooled results of this meta-analysis were stable and reliable, and none of the included studies caused an obvious impact on the overall results.

thumbnail
Download:
Fig 5. Sensitivity analysis for the association of preoperative sarcopenia with overall survival (A) and disease-free survival (B) in rectal cancer patients.

https://doi.org/10.1371/journal.pone.0303494.g005

Publication bias

According to Begg’s funnel plots (Fig 6A and 6B) and Egger’s test (P = 0.001 and P = 0.003) for the associations between preoperative sarcopenia and OS and DFS, significant publication bias was detected. Thus, the fill-and-trim method was applied, and five (Fig 6C) and four (Fig 6D) potentially unpublished studies were found. However, five (OS: filled HR = 1.66, 95% CI = 1.31–2.10, P<0.001) and four (DFS: filled HR = 1.56, 95% CI = 1.19–2.03, P = 0.001) “unpublished studies” did not affect the overall conclusions.

thumbnail
Download:
Fig 6. Begg’s and filled funnel plots for the association of preoperative sarcopenia with overall survival (A and B) and disease-free survival (C and D) in rectal cancer patients.

https://doi.org/10.1371/journal.pone.0303494.g006

Discussion

In this meta-analysis, we demonstrated that sarcopenia was significantly associated with long-term survival among rectal cancer patients who received surgical therapy and that patients with sarcopenia had poorer survival. Furthermore, a history of neoadjuvant therapy did not significantly affect the association between sarcopenia and poor prognosis. Thus, sarcopenia could serve as a valuable prognostic factor in surgical-related rectal cancer patients. However, additional high-quality studies are still needed to further verify the above findings. Zhu et al. conducted a meta-analysis to determine the prognostic role of sarcopenia in rectal cancer patients [35]. These authors included seven studies with 2377 patients and reported that sarcopenia predicted poor OS (HR = 2.37, 95% CI = 1.13–4.98, P = 0.02) [35]. However, their findings are relatively limited. In this meta-analysis, 15 studies were included, and patients who underwent surgery were the focus. In addition, the associations of sarcopenia with postoperative DFS and CSS were also assessed, and subgroup analysis based on neoadjuvant chemoradiotherapy was further conducted. Therefore, this meta-analysis provides additional high-quality evidence about the prognostic role of sarcopenia in surgically treated rectal cancer patients.

The impact of muscle loss on the prognosis of cancer patients involves various factors. First, a reduction in muscle mass may lead to a decreased ability for postoperative recovery, resulting in reduced surgical tolerance. Surgery is a primary modality for treating many tumors, and a patient’s postoperative recovery directly correlates with prognosis. Second, muscle loss can influence the functionality of the immune system. The immune system plays a crucial role in combating tumor cells and preventing infections. When immune function decreases, patients are more susceptible to complications such as infections, thus affecting prognosis [36, 37]. Additionally, muscle loss may result in decreased tolerance to chemotherapy and radiation therapy. These treatments impose a significant burden on the body, and patients with weakened physical constitutions may struggle to endure side effects, impacting treatment completion and efficacy [11, 38]. Moreover, there is an association between muscle loss and systemic inflammation. Inflammation may play a role in the development of tumors and is related to systemic complications associated with malignancies, further influencing patient prognosis [39, 40]. Finally, muscle loss is often associated with malnutrition. Maintaining good nutritional status is crucial for a patient’s recovery and treatment outcomes. Muscle loss may signify insufficient nutritional support, exacerbating malnutrition.

Our meta-analysis confirmed that sarcopenia is a risk factor affecting the prognosis of rectal cancer patients. Therefore, appropriate and reasonable interventions for sarcopenia may help improve the prognosis of rectal cancer patients. Currently, there are three main treatment options for sarcopenia: nutritional supplementation, exercise intervention, and drug therapy. Current research evidence indicates that nutritional therapy is beneficial for improving muscle mass, strength, and muscle function [41]. Key nutritional components include protein supplementation, creatine, vitamins, and omega-3 polyunsaturated fatty acids, among others, with protein supplementation being crucial for improving nutritional status [41]. In addition, proper physical exercise can increase muscle mass, strength, and endurance, thereby improving muscle wasting [42, 43]. It is currently believed that combining exercise with protein and energy intake is key to preventing and treating sarcopenia [42, 43]. Treatment for sarcopenia primarily includes testosterone, selective androgen receptor modulators, growth hormone analogs, etc. [44, 45]. However, there is a lack of standardized international guidelines for the systematic treatment of sarcopenia. Many intervention measures are still in the early exploration stage, so further research is needed to provide additional high-quality evidence-based support.

There are several limitations in our meta-analysis that should be noted. First, the overall sample size was relatively small, and all the studies were retrospective. Second, several confounding factors, such as the definition of sarcopenia, including the cutoff values of SMI, PMV and PMI and adjuvant therapy, were included in this meta-analysis, and we were unable to conduct a more detailed analysis due to the lack of original data. Third, most of the included studies were from Asian countries, which might affect the generalizability of our findings. Fourth, due to the lack of relevant data, we failed to explore the association between sarcopenia and postoperative short-term outcomes. Fifth, significant publication bias was detected in our meta-analysis. Although the results of the fill-and-trim method indicated that “unpublished studies” did not affect the overall findings, additional high-quality studies are still needed to verify our conclusions.

Conclusion

Preoperative sarcopenia is significantly associated with poor survival among surgical rectal cancer patients and could serve as a novel and valuable predictor of long-term prognosis in these patients.

Supporting information

S1 File. Literature search strategies in each database.

https://doi.org/10.1371/journal.pone.0303494.s001

(DOCX)

S1 Checklist. PRISMA 2020 checklist.

https://doi.org/10.1371/journal.pone.0303494.s002

(DOCX)

References

  1. 1. Siegel RL, Wagle NS, Cercek A, Smith RA, Jemal A: Colorectal cancer statistics, 2023. CA Cancer J Clin 2023, 73(3):233–254.
  2. 2. Zheng RS, Zhang SW, Sun KX, Chen R, Wang SM, Li L, et al: [Cancer statistics in China, 2016]. Zhonghua Zhong Liu Za Zhi 2023, 45(3):212–220. pmid:36944542
  3. 3. Zheng Y, Wu C: [Prevalence and trend of gastrointestinal malignant tumors in the elderly over 75 years old in China]. Zhonghua Wei Chang Wai Ke Za Zhi 2016, 19(5):481–485. pmid:27215509
  4. 4. Xia C, Dong X, Li H, Cao M, Sun D, He S, et al: Cancer statistics in China and United States, 2022: profiles, trends, and determinants. Chin Med J (Engl) 2022, 135(5):584–590. pmid:35143424
  5. 5. Almasaudi AS: An investigation of the clinical nutritional practices of oncologists and the management of cancer-related malnutrition in inpatient care. Eur Rev Med Pharmacol Sci 2023, 27(20):9928–9936. pmid:37916362
  6. 6. Shen N, Wen J, Chen C, Chen X, Zhang W, Garijo PD, et al: The relationship between GLIM-malnutrition, post-operative complications and long-term prognosis in elderly patients undergoing colorectal cancer surgery. J Gastrointest Oncol 2023, 14(5):2134–2145. pmid:37969837
  7. 7. Al-Shahethi AH, Mahdi FA, Al-Shameri EA, Abol Gaith FM: Factors Associated With Malnutrition in Hospitalized Cancer Patients in a National Oncology Center in Conflict-Affected Settings in Sana’a, Yemen: An Institution-Based Cross-Sectional Study. Cureus 2023, 15(9):e45411. pmid:37859884
  8. 8. Nakamura Y, Kawase M, Kawabata Y, Kanto S, Yamaura T, Kinjo Y, et al: Impact of malnutrition on cancer recurrence, colorectal cancer-specific death, and non-colorectal cancer-related death in patients with colorectal cancer who underwent curative surgery. J Surg Oncol 2023. pmid:37846204
  9. 9. Wu JF, Jia J, Chen P, Wang XF, Yang FX, Liu Y, et al: Sarcopenia and its clinical correlation in elderly chronic obstructive pulmonary disease: a prospective cohort study. Eur Rev Med Pharmacol Sci 2023, 27(20):9762–9772. pmid:37916340
  10. 10. Xu R, Ma LL, Cui S, Chen L, Xu H: Bioinformatics and Systems Biology Approach to Identify the Pathogenetic Link between Heart Failure and Sarcopenia. Arq Bras Cardiol 2023, 120(10):e20220874.
  11. 11. Jensen S, Bloch Z, Quist M, Hansen TTD, Johansen C, Pappot H, et al: Sarcopenia and loss of muscle mass in patients with lung cancer undergoing chemotherapy treatment: a systematic review and meta-analysis. Acta oncologica (Stockholm, Sweden) 2023, 62(3):318–328. pmid:37051865
  12. 12. Park A, Orlandini MF, Szor DJ, Junior UR, Tustumi F: The impact of sarcopenia on esophagectomy for cancer: a systematic review and meta-analysis. BMC Surg 2023, 23(1):240. pmid:37592262
  13. 13. Meyer HJ, Wienke A, Surov A: Sarcopenia as a Prognostic Marker for Survival in Gastric Cancer Patients Undergoing Palliative Chemotherapy. A Systematic Review and Meta Analysis. Nutr Cancer 2022, 74(10):3518–3526. pmid:35603926
  14. 14. 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 (Clinical research ed) 2021, 372:n71. pmid:33782057
  15. 15. Wang Y, Li J, Chang S, Dong Y, Che G: Risk and Influencing Factors for Subsequent Primary Lung Cancer After Treatment of Breast Cancer: A Systematic Review and Two Meta-Analyses Based on Four Million Cases. Journal of thoracic oncology: official publication of the International Association for the Study of Lung Cancer 2021, 16(11):1893–1908. pmid:34256110
  16. 16. Li J, Wang Y, Li J, Cao S, Che G: Meta-analysis of Lobectomy and Sublobar Resection for Stage I Non-small Cell Lung Cancer With Spread Through Air Spaces. Clinical lung cancer 2022, 23(3):208–213. pmid:34799251
  17. 17. Begg CB, Mazumdar M: Operating characteristics of a rank correlation test for publication bias. Biometrics 1994, 50(4):1088–1101. pmid:7786990
  18. 18. Egger M, Davey Smith G, Schneider M, Minder C: Bias in meta-analysis detected by a simple, graphical test. BMJ (Clinical research ed) 1997, 315(7109):629–634. pmid:9310563
  19. 19. Shi L, Lin L: The trim-and-fill method for publication bias: practical guidelines and recommendations based on a large database of meta-analyses. Medicine (Baltimore) 2019, 98(23):e15987. pmid:31169736
  20. 20. Choi MH, Oh SN, Lee IK, Oh ST, Won DD: Sarcopenia is negatively associated with long-term outcomes in locally advanced rectal cancer. Journal of Cachexia Sarcopenia and Muscle 2018, 9(1):53–59. pmid:28849630
  21. 21. Park SE, Hwang IG, Choi CH, Kang H, Kim BG, Park BK, et al: Sarcopenia is poor prognostic factor in older patients with locally advanced rectal cancer who received preoperative or postoperative chemoradiotherapy. Medicine 2018, 97(48). pmid:30508928
  22. 22. Hopkins JJ, Reif RL, Bigam DL, Baracos VE, Eurich DT, Sawyer MB: The Impact of Muscle and Adipose Tissue on Long-term Survival in Patients With Stage I to III Colorectal Cancer. Diseases of the Colon & Rectum 2019, 62(5):549–560.
  23. 23. Chung E, Lee HS, Cho E-S, Park EJ, Baik SH, Lee KY, et al: Prognostic significance of sarcopenia and skeletal muscle mass change during preoperative chemoradiotherapy in locally advanced rectal cancer. Clinical Nutrition 2020, 39(3):820–828. pmid:30928250
  24. 24. Han JS, Ryu H, Park IJ, Kim KW, Shin Y, Kim SO, et al: Association of Body Composition with Long-Term Survival in Non-metastatic Rectal Cancer Patients. Cancer Research and Treatment 2020, 52(2):563–572. pmid:31801316
  25. 25. Shirdel M, Andersson F, Myte R, Axelsson J, Rutegård M, Blomqvist L, et al: Body composition measured by computed tomography is associated with colorectal cancer survival, also in early-stage disease. Acta oncologica (Stockholm, Sweden) 2020, 59(7):799–808. pmid:32228271
  26. 26. Wang S, Xie H, Gong Y, Kuang J, Yan L, Ruan G, et al: The value of L3 skeletal muscle index in evaluating preoperative nutritional risk and long-term prognosis in colorectal cancer patients. Scientific Reports 2020, 10(1). pmid:32424167
  27. 27. Xie H, Gong Y, Kuang J, Yan L, Ruan G, Tang S, et al: Computed Tomography-Determined Sarcopenia Is a Useful Imaging Biomarker for Predicting Postoperative Outcomes in Elderly Colorectal Cancer Patients. Cancer Research and Treatment 2020, 52(3):957–972. pmid:32311863
  28. 28. Abe S, Nozawa H, Kawai K, Sasaki K, Murono K, Emoto S, et al: Poor nutrition and sarcopenia are related to systemic inflammatory response in patients with rectal cancer undergoing preoperative chemoradiotherapy. International Journal of Colorectal Disease 2022, 37(1):189–200. pmid:34633498
  29. 29. Giani A, Famularo S, Fogliati A, Riva L, Tamini N, Ippolito D, et al: Skeletal muscle wasting and long-term prognosis in patients undergoing rectal cancer surgery without neoadjuvant therapy. World Journal of Surgical Oncology 2022, 20(1). pmid:35216606
  30. 30. Horie K, Matsuda T, Yamashita K, Hasegawa H, Utsumi M, Urakawa N, et al: Sarcopenia assessed by skeletal muscle mass volume is a prognostic factor for oncological outcomes of rectal cancer patients undergoing neoadjuvant chemoradiotherapy followed by surgery. Ejso 2022, 48(4):850–856. pmid:34756762
  31. 31. Abe S, Nozawa H, Sasaki K, Murono K, Emoto S, Yokoyama Y, et al: Sarcopenia is Associated With Oncological Prognosis and the Incidence of Secondary Cancer in Patients With Middle/Lower Rectal Cancer. Clinical Colorectal Cancer 2023, 22(1):143–152. pmid:36418196
  32. 32. Gartrell R, Qiao J, Kiss N, Faragher I, Chan S, Baird PN, et al: Can sarcopenia predict survival in locally advanced rectal cancer patients? ANZ J Surg 2023, 93(9):2166–2171. pmid:37209307
  33. 33. Mallet-Boutboul L, Basile D, Gallois C, Roblot V, Cazelles A, Labiad C, et al: Impact of sarcopenia and visceral fat on postoperative morbidity and survival after rectal cancer surgery in patients treated with neoadjuvant chemoradiotherapy. Surgery Open Digestive Advance 2023, 10 (no pagination)(100083).
  34. 34. Portale G, Zuin M, Spolverato YC, Bartolotta P, Gregori D, Rettore C, et al: Prognostic effect of sarcopenia in patients undergoing laparoscopic rectal cancer resection. Anz Journal of Surgery 2023, 93(6):1631–1637.
  35. 35. Zhu Y, Guo X, Zhang Q, Yang Y: Prognostic value of sarcopenia in patients with rectal cancer: A meta-analysis. PloS one 2022, 17(6):e0270332. pmid:35749415
  36. 36. Abdelrahman Z, Wang X, Wang D, Zhang T, Zhang Y, Wang X, et al: Identification of novel pathways and immune profiles related to sarcopenia. Front Med (Lausanne) 2023, 10:928285. pmid:37138756
  37. 37. Lin TY, Chen YF, Wu WT, Han DS, Tsai IC, Chang KV, et al: Impact of sarcopenia on the prognosis and treatment of lung cancer: an umbrella review. Discov Oncol 2022, 13(1):115. pmid:36307591
  38. 38. Harada T, Tsuji T, Ueno J, Hijikata N, Ishikawa A, Kotani D, et al: Association of sarcopenia with relative dose intensity of neoadjuvant chemotherapy in older patients with locally advanced esophageal cancer: A retrospective cohort study. J Geriatr Oncol 2023, 14(7):101580. pmid:37478514
  39. 39. Merchant RA, Chan YH, Anbarasan D, Aprahamian I: Association of Motoric Cognitive Risk Syndrome with Sarcopenia and Systemic Inflammation in Pre-Frail Older Adults. Brain Sci 2023, 13(6). pmid:37371414
  40. 40. Schmeusser BN, Ali AA, Fintelmann FJ, Garcia JM, Williams GR, Master VA, et al: Imaging Techniques to Determine Degree of Sarcopenia and Systemic Inflammation in Advanced Renal Cell Carcinoma. Curr Urol Rep 2023, 24(7):317–334. pmid:37036632
  41. 41. Chen LK, Woo J, Assantachai P, Auyeung TW, Chou MY, Iijima K, et al: Asian Working Group for Sarcopenia: 2019 Consensus Update on Sarcopenia Diagnosis and Treatment. J Am Med Dir Assoc 2020, 21(3):300–307.e302.
  42. 42. Bilski J, Pierzchalski P, Szczepanik M, Bonior J, Zoladz JA: Multifactorial Mechanism of Sarcopenia and Sarcopenic Obesity. Role of Physical Exercise, Microbiota and Myokines. Cells 2022, 11(1).
  43. 43. Dhillon RJ, Hasni S: Pathogenesis and Management of Sarcopenia. Clin Geriatr Med 2017, 33(1):17–26. pmid:27886695
  44. 44. Shin MJ, Jeon YK, Kim IJ: Testosterone and Sarcopenia. World J Mens Health 2018, 36(3):192–198. pmid:29756416
  45. 45. Rolland Y, Dray C, Vellas B, Barreto PS: Current and investigational medications for the treatment of sarcopenia. Metabolism 2023, 149:155597. pmid:37348598