Wang DE, Qin XF, Yang W. Correlation between sarcopenia diagnosed by C3SMI criteria and prognosis in esophageal cancer patients after radiotherapy. World J Gastrointest Oncol 2025; 17(9): 107626 [DOI: 10.4251/wjgo.v17.i9.107626]
Corresponding Author of This Article
Wei Yang, MM, Associate Chief Physician, Department of Ultrasound Medicine, The Affiliated Huaian No. 1 People’s Hospital of Nanjing Medical University, No. 1 Huanghe West Road, Huaiyin District, Huai’an 223300, Jiangsu Province, China. yangwei110501@163.com
Research Domain of This Article
Oncology
Article-Type of This Article
Retrospective Study
Open-Access Policy of This Article
This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
De-En Wang, Department of Geriatrics, The Affiliated Huaian No. 1 People’s Hospital of Nanjing Medical University, Huai’an 223300, Jiangsu Province, China
Xiao-Fang Qin, Wei Yang, Department of Ultrasound Medicine, The Affiliated Huaian No. 1 People’s Hospital of Nanjing Medical University, Huai’an 223300, Jiangsu Province, China
Author contributions: Wang DE and Yang W designed the research study; Wang DE and Qin XF performed the research and collected the data; Wang DE and Yang W analyzed the data and wrote the manuscript; All authors have read and approve the final manuscript.
Institutional review board statement: The study was reviewed and approved by the Institutional Review Board of The Affiliated Huaian No. 1 People’s Hospital of Nanjing Medical University (Approval Number: KY-2024-242-01).
Informed consent statement: The data used in this study did not involve identifiable patient information; thus, the requirement for informed consent was waived by the Institutional Review Board of The Affiliated Huaian No. 1 People’s Hospital of Nanjing Medical University. All patient data were obtained, recorded, and managed exclusively for this study, with strict confidentiality maintained, ensuring no harm to the patients.
Conflict-of-interest statement: All the authors report no relevant conflicts of interest for this article.
Data sharing statement: No additional data are available.
Open Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Wei Yang, MM, Associate Chief Physician, Department of Ultrasound Medicine, The Affiliated Huaian No. 1 People’s Hospital of Nanjing Medical University, No. 1 Huanghe West Road, Huaiyin District, Huai’an 223300, Jiangsu Province, China. yangwei110501@163.com
Received: April 22, 2025 Revised: May 25, 2025 Accepted: July 30, 2025 Published online: September 15, 2025 Processing time: 145 Days and 16.5 Hours
Abstract
BACKGROUND
Esophageal cancer is a common malignancy with high mortality. Radiotherapy is an important treatment. Sarcopenia affects patients' physical function and prognosis. However, the relationship between sarcopenia diagnosed by Chun-Hou Chen method for sarcopenia measurement and index (C3SMI) criteria and esophageal cancer prognosis after radiotherapy is unclear.
AIM
To explore the correlation between sarcopenia (SA) diagnosed based on C3SMI criteria and the prognosis of patients with esophageal cancer following radiotherapy.
METHODS
A retrospective analysis was conducted on the general clinical data of 131 esophageal cancer patients who received radiotherapy in the Affiliated Huaian No. 1 People’s Hospital of Nanjing Medical University from March 2021 to July 2024. Based on the presence of SA, the patients were assigned into two groups - the SA group and the non-SA group. Logistic regression analysis was used for investigating the risk factors influencing SA in esophageal cancer patients. Additionally, the patients were followed up, with their prognosis recorded. As per their prognostic outcomes, the patients were allocated into a good prognosis group and a poor prognosis group. The data of the two groups were compared. Using logistic regression analysis, the risk factors that may influence the prognosis of these patients were analyzed. SPSS 26.0 statistical software was introduced for analyzing the study data. Comparisons were made between groups using t-tests or χ2 tests based on the data type.
RESULTS
As revealed through logistic regression analysis, age [odds ratio (OR) = 2.898, P = 0.038], body mass index (OR = 5.983, P = 0.006), prealbumin (OR = 6.253, P = 0.003), and Karnofsky performance status score (OR = 3.854, P = 0.010) were independent risk factors impacting SA for esophageal cancer patients (P < 0.05). Logistic regression analysis also found that age (OR = 3.823, P = 0.030), differentiation degree (OR = 4.802, P = 0.028), American Joint Committee on Cancer clinical staging (OR = 3.732, P = 0.013), alpha-fetoprotein level (OR = 3.508, P = 0.018), thrombospondin-1 level (OR = 5.749, P = 0.006), carcinoembryonic antigen level (OR = 3.873, P = 0.030), and SA (OR = 3.593, P = 0.017) were independent risk factors that may influence esophageal cancer patients' prognosis (P < 0.05).
CONCLUSION
The presence of SA has a significant relation to the poor prognosis of esophageal cancer patients, which highlights the importance of assessing and intervening in SA in clinical management so as to improve patient prognosis.
Core Tip: This study highlights the significant correlation between sarcopenia (SA) (diagnosed using Chun-Hou Chen method for SA measurement and index criteria) and poor prognosis in esophageal cancer patients undergoing radiotherapy. Key findings reveal that age, body mass index, prealbumin levels, and Karnofsky performance status score are independent risk factors for SA, while SA itself, along with tumor differentiation, American Joint Committee on Cancer staging, and serum markers (alpha-fetoprotein, thrombospondin-1, carcinoembryonic antigen), adversely impacts prognosis. These results underscore the importance of early SA assessment and nutritional intervention in clinical management to improve patient outcomes.
Citation: Wang DE, Qin XF, Yang W. Correlation between sarcopenia diagnosed by C3SMI criteria and prognosis in esophageal cancer patients after radiotherapy. World J Gastrointest Oncol 2025; 17(9): 107626
Sarcopenia (SA) is a syndrome characterized by age-associated muscle mass and strength reduction, increasingly gaining widespread attention in the medical field[1]. In accordance with Chun-Hou Chen method for SA measurement and index (C3SMI) criteria, SA should be diagnosed with comprehensive consideration of multiple indicators, such as muscle mass, strength, and function[2]. The criteria aim to improve the identification of SA, particularly in high-risk populations such as cancer patients[3]. Research has unraveled that SA impacts physiological function and is inextricably associated with the prognosis of various diseases, including cardiovascular diseases, diabetes, and cancer[4]. Among cancer patients, the prevalence of SA is significantly higher and is strongly correlated with tumor type, stage, and treatment modalities[5]. Therefore, it will provide critical insights for the management and treatment of cancer patients to effectively assess SA levels according to C3SMI criteria.
Esophageal cancer, a prevalent malignancy in the digestive system, has witnessed rising incidence and mortality rates across the globe. Treatment methods for esophageal cancer include surgery, radiotherapy, and chemotherapy, among which radiotherapy is widely utilized due to its effective control of local tumor progression[6]. However, radiotherapy is often accompanied by a range of side effects, such as radiation esophagitis, dysphagia, and malnutrition, all of which can contribute to weight loss and reduced muscle mass in patients[7]. Studies have suggested that post-radiotherapy patients often face a significantly increased risk of muscle loss due to reduced intake and augmented metabolism, leading to SA[8].
Clinical research has shown that the presence of SA lowers patients' quality of life, impairs treatment tolerance, and heightens the incidence of postoperative complications[9]. Moreover, SA may also exert a negative impact on patients' survival by triggering systemic inflammatory responses or influencing drug metabolism[10]. Thus, a deep probe into the SA status in post-radiotherapy esophageal cancer patients and its impact on prognosis is particularly important. This study seeks to systematically analyze the correlation between SA, as defined by C3SMI criteria, and the prognosis of esophageal cancer patients undergoing radiotherapy. By doing so, it intends to provide a more precise risk assessment tool for clinical practice, thereby facilitating the implementation of related care and treatment strategies.
MATERIALS AND METHODS
General information
The general clinical data of 131 esophageal cancer patients receiving radiotherapy in the Affiliated Huaian No. 1 People’s Hospital of Nanjing Medical University from March 2021 to July 2024 were subjected to a retrospective analysis.
Inclusion criteria: (1) All meeting the relevant diagnostic criteria for esophageal cancer[11]; (2) All patients underwent computed tomography (CT) examinations of the mandible, tongue, and oropharynx before surgery; (3) Patients who were unable to undergo surgical resection and received concurrent radiotherapy (cisplatin + fluorouracil) in the Affiliated Huaian No. 1 People’s Hospital of Nanjing Medical University; and (4) Patients with an estimated survival of over 6 months.
Exclusion criteria: (1) Other concomitant malignancies; (2) History of surgery, chemotherapy, or radiotherapy; (3) Concomitant immune diseases or chronic inflammatory diseases; or (4) Women who were pregnant or lactating.
This study was conducted in accordance with the relevant diagnostic criteria outlined in the Declaration of Helsinki.
Diagnostic criteria for SA
Analyze the CT images of the mandible, tongue, and oropharynx taken from the patient before surgery. Select the imaging of the third cervical intervertebral disc plane and capture two consecutive images at the C3 plane. Set the threshold region where the values for the muscle area range from -29 to +150 HU. Outline the C3 skeletal muscles (sternocleidomastoid muscle and paravertebral muscles), measure the cross-sectional area (CSA) of the muscles, and calculate the average value. The formula is CSA at L3 (m2) = 24.078 + 2.789 × CSA at C3 (m2). The CSA of the skeletal muscles at the L3 vertebral level can be calculated based on that at the C3 vertebral level. The skeletal muscle mass index at L3 is calculated as the ratio of the CSA of the L3 skeletal muscles to the patient's height. If the index is less than 38.5 cm²/m² in females or less than 52.4 cm²/m² in males, the patient is diagnosed with SA; otherwise, the patient is classified as non-SA. Divide the patients into the SA group and the non-SA group according to whether they have SA[12].
Radiotherapy and chemotherapy
Three-dimensional conformal radiotherapy: The patient, placed in the supine position, underwent CT simulation for localization. The images were uploaded to the radiotherapy technology station, where the planning target volume, clinical target volume (CTV), gross tumor volume (GTV), and organs at risk were delineated. The Elekta 6 MV X-ray linear accelerator was adopted for radical radiotherapy using 6 MV photon beams. A total dose of 63 Gy was set for the GTV, delivered at 3.1 Gy per fraction, while a dose of 54 Gy was prescribed to the CTV at 1.8 Gy per fraction. Treatment was administered 5 times per week and completed within 6 weeks.
Concurrent chemotherapy: Intravenous drip of 80 mg/m2 cisplatin injection (produced by Jiangsu Hansoh Pharmaceutical Group Co., Ltd., National Medicine Approval No. H20010743, injection, 6 mL: 30 mg × 5 vials) and fluorouracil injection [Approval No.: National Medicine Approval No. H20253343, produced by Jinyao Heping (Tianjin) Pharmaceutical Co., Ltd., 10 mL: 0.25 g]. One cycle lasts for 21 days, with a total of 6 cycles. Symptomatic treatments such as routine fluid replacement and anti-vomiting were given before drug administration.
Prognostic assessment
Patients were assessed for treatment response 4 weeks post-therapy. A prognostic assessment was conducted based on the literature[13]. Complete response (CR): Lesions were nearly resolved, with no new lesions observed, and tumor markers returned to normal levels, sustained for more than 4 weeks. Partial response (PR): The sum of the longest diameters of tumors decreased by 30% or more, sustained for at least 4 weeks. Stable disease (SD): The sum of the longest diameters of tumors decreased by less than 30% or increased by less than 20%. Progressive disease (PD): The sum of the longest diameters of tumors increased by 20% or more, or new lesions appeared. CR and PR were regarded as good prognosis, whereas SD and PD were considered poor prognosis. As per the prognostic outcome, the patients were allocated into the good prognosis group and the poor prognosis group.
General data
The patients' general clinical data were collected, including age, sex, body mass index (BMI), hypertension, hyperlipidemia, coronary heart disease (CHD), diabetes mellitus (DM), tumor type, differentiation degree, American Joint Committee on Cancer (AJCC) clinical staging, pathogenic site, lymph node metastasis, number of lesions, tumor diameter, dissection method, American Society of Anesthesiologists (ASA) classification, human serum albumin (HSA), platelet to lymphocyte ratio (PLR), alpha fetal protein (AFP), thrombospondin-1 (TSP-1), hemoglobin (Hb), plasma albumin (ALB), prealbumin (PA), total cholesterol (TC), triglyceride (TG), Karnofsky performance status (KPS) score, and carcinoembryonic antigen (CEA).
Statistical analysis
SPSS 26.0 software and R 4.4 were employed for processing and picture plotting of the study data. Unordered categorical data were analyzed via the χ2 test. Measurement data were represented as mean ± SD and subjected to independent-samples t-tests. Multivariate analysis was performed using logistic regression analysis. A P value of less than 0.05 was considered statistically significant.
RESULTS
Single factors influencing SA in esophageal cancer patients
The general data were compared between the SA group and the non-SA group. As a result, no substantial differences were noted between the two groups in terms of sex, hypertension, hyperlipidemia, CHD, DM, tumor type, differentiation degree, AJCC clinical staging, pathogenic site, lymph node metastasis, number of lesions, tumor diameter, dissection method, ASA classification, HSA, PLR, AFP, TSP-1, Hb, ALB, TC, or TG (P > 0.05). Nevertheless, we found significant differences between the two groups in age, BMI, PA, and KPS score (P < 0.05; Table 1).
Table 1 Single factors influencing sarcopenia in esophageal cancer patients.
Analysis of risk factors influencing SA in esophageal cancer patients
The factors that showed differences in the above single factor analysis - age, BMI, PA, and KPS score - were incorporated into the logistic regression equation. The analysis revealed that age, BMI, PA, and KPS score were independent risk factors influencing SA in patients with esophageal cancer (P < 0.05; Table 2 and Figure 1A).
Figure 1 Odds ratio value forest map.
A: Forest plot of multivariate risk factors affecting sarcopenia in patients with esophageal cancer; B: Forest plot of multivariate risk factors affecting the prognosis of patients with esophageal cancer. BMI: Body mass index; PA: Prealbumin; KPS: Karnofsky performance status; AJCC: American Joint Committee on Cancer; AFP: Alpha fetal protein; TSP-1: Thrombospondin-1; CEA: Carcinoembryonic antigen.
Table 2 Analysis of risk factors influencing sarcopenia in esophageal cancer patients.
Single factors influencing the prognosis of esophageal cancer patients
Through an analysis of the general data on esophageal cancer patients with different prognostic outcomes, we observed no substantial differences between the good prognosis group and the poor prognosis group in several indicators (P > 0.05). These indicators encompassed sex, BMI, hypertension, hyperlipidemia, CHD, DM, tumor type, pathogenic site, lymph node metastasis, number of lesions, tumor diameter, dissection method, ASA classification, HSA, PLR, Hb, ALB, PA, TC, TG, and KPS score. However, significant variances were found in age, differentiation degree, SA, AJCC clinical staging, AFP, TSP-1, and CEA levels between the two groups (P < 0.05; Table 3).
Table 3 Single factors influencing the prognosis of esophageal cancer patients.
Risk factors influencing the prognosis of esophageal cancer patients
The single factors mentioned in Table 3 were incorporated into the logistic regression equation. The results unveiled that age, differentiation degree, AJCC clinical staging, AFP, TSP-1, CEA, and SA were all independent risk factors that impacted the prognosis of patients with esophageal cancer (P < 0.05; Table 4 and Figure 1B).
Table 4 Risk factors influencing the prognosis of esophageal cancer patients.
Over the past years, SA has been gaining attention, particularly among the cancer patient population. SA is considered an independent risk factor that causes a decline in patient survival rates, impacting tolerance and recovery[14]. With an increase in the incidence of esophageal cancer, relevant studies have been gradually enriched, and most of them are focused on physiological changes in patients following radiotherapy. Esophageal cancer patients usually are in the face of issues like malnutrition and weight loss, while SA tends to exacerbate such vicious conditions[15]. However, the impact of SA on the prognostic outcomes of esophageal cancer patients has not been analyzed yet.
In this study, we discovered age is an independent risk factor that impacts SA occurring in esophageal cancer patients. Analysis revealed that with age increases, human bodies may present with a decline in physiological functions, such as reduced muscle mass and strength. The elderly are more susceptible to such SA, which may occur in esophageal cancer patients during treatment more easily[16]. The basal metabolic rate in older adults is generally lower, leading to a reduction in muscle synthesis capacity. Additionally, the efficiency of nutrient absorption and utilization in the elderly may also be impaired, which can negatively impact muscle maintenance and repair[17]. BMI serves as an indicator adopted to assess the relationship between an individual's weight and height, reflecting their nutritional status. Our study confirmed that BMI levels may impact SA in esophageal cancer patients. This is mainly attributed to the correlation between low BMI levels and malnutrition in these patients, which may result in decreased muscle mass and augmented SA risks. Patients with esophageal cancer often experience cancer-associated wasting syndromes, including loss of appetite, nausea, and dysphagia, contributing to insufficient nutrient intake, leading to lowered BMI and nutritional deficiencies, which further contribute to the development of SA[18]. PA, another independent risk factor for SA in esophageal cancer patients, can reflect the short-term nutritional status of the body. Low PA levels are usually correlated with malnutrition. Esophageal cancer patients are prone to developing SA due to tumor-caused dysphagia and inadequate nutrient intake, and low PA levels can suggest the degree of malnutrition. Esophageal cancer patients often experience systemic inflammation, which affects the synthesis of PA due to its dependence on liver function and inflammatory status. Inflammatory-induced metabolic changes may accelerate sarcolysis, hence heightening the risk of SA[19]. The levels of PA are associated with the survival rates and prognosis of cancer patients. Low PA levels typically indicate poor overall nutritional status and reduced muscle reserves, further elevating the risk of SA[20]. The KPS score is also an independent risk factor for SA in esophageal cancer patients. This may be because the KPS score assesses patients' ability to perform daily activities, and patients with poorer functional status typically demonstrate lower levels of physical activity. Reduced activity levels can lead to muscle atrophy and disruptions in energy metabolism, thus stepping up the risk of SA[21]. Patients with lower KPS scores often experience malnutrition, as inadequate or imbalanced dietary intake results in insufficient protein and essential nutrient uptake, accelerating muscle loss. Additionally, malignant tumors frequently induce metabolic alterations that exacerbate sarcolysis[22].
Independent risk factors for the prognosis of patients with esophageal cancer were analyzed in our study. As indicated by the results, in addition to age and tumor-associated indicators (such as differentiation degree, staging, and serum tumor markers), SA also acts as an independent risk factor for the prognosis of esophageal cancer patients. As age increases, the body's immune function gradually declines, and cellular repair capacity weakens, leading to an elevated risk of cancer progression. This is particularly evident in patients undergoing radiotherapy and chemotherapy, whose tolerance to treatment is relatively poorer, thereby affecting prognosis[23]. Among tumor-correlated indicators, the degree of differentiation refers to the maturity of tumor cells and their resemblance to normal tissue. Well-differentiated tumor cells closely resemble normal cells in morphology and exhibit slower proliferation rates, whereas poorly differentiated tumor cells grow more rapidly and are more invasive[24]. This makes early detection and treatment more challenging. Similarly, the AJCC clinical staging provides clinical guidance by reflecting the biological behavior of tumors, which is associated with survival outcomes[25]. Additionally, serum tumor markers such as AFP, CEA, and TSP-1 are commonly employed to assess disease severity and survival prognosis. Elevated AFP levels often indicate stronger proliferation capacity and greater invasiveness of tumor cells, hence impacting patient survival[26,27]. TSP-1 modulates the tumor microenvironment, influencing tumor cell proliferation and invasion. It can dampen angiogenesis, attenuate tumor blood supply, and consequently limit tumor growth and metastasis[28]. CEA expression has a close correlation with the regulation of tumor-related inflammation and angiogenesis, impacting tumor cell proliferation, migration, and metastasis, and further influencing patient prognosis[29].
The aforementioned influencing factors are not uncommon in clinical research, they are often combined with other indicators to comprehensively predict adverse outcomes in cancer patients. Given the high prevalence of SA in the elderly population, the study team integrated these indicators with SA to assess the prognosis of esophageal cancer patients undergoing radiotherapy and chemotherapy. The findings unraveled that SA is also a significant factor influencing the outcomes of such treatments. Epidemiological studies on chronic diseases in the elderly population have shown that the global prevalence of SA in individuals aged 60 or 65 and above is approximately 10%[30]. Adverse events triggered by SA, such as falls, disability, and reduced quality of life, consume considerable medical resources. This is particularly impactful in countries/regions experiencing population aging, placing a substantial economic burden on both society and families. Moreover, common chronic diseases threatening the elderly population encompass not only cardiovascular and cerebrovascular diseases but also malignancies. A cross-sectional study conducted in Jiangsu Province revealed that the estimated incidence and mortality rates of newly diagnosed malignant tumors among the elderly population in the region were 1080.18 per 100000 and 1050.50 per 100000, respectively, and the incidence of malignant tumors showed a significant upward trend[31]. Under the combined influence of systemic inflammatory responses, metabolic abnormalities, malnutrition, and treatment side effects, the prevalence of concomitant SA has also increased, particularly in gastrointestinal tumors. This may be attributed to the association of SA with malnutrition, leading to insufficient energy and protein intake before surgery and during postoperative recovery, thereby affecting overall rehabilitation. In addition, the loss of skeletal muscle mass leads to insufficient metabolic reserve. Active mediators (such as branched - chain amino acids) abnormally released during muscle catabolism accelerate tumor progression by activating pro - proliferative signaling pathways such as mTORC1 and induce treatment resistance. Meanwhile, the decline in the body's functional reserve directly limits the intensity and tolerance of anti-tumor treatments (such as radiotherapy/chemotherapy), thus affecting the prognosis[32].
CONCLUSION
In conclusion, independent risk factors that may influence SA comprise age, BMI, PA, and KPS score. Further analysis has demonstrated that age, differentiation degree, AJCC clinical staging, AFP, TSP-1, CEA, and SA themselves are also independent risk factors for patient prognosis. Therefore, the combination of common assessment indicators in clinical settings with SA in the elderly is of significant value for analyzing influencing factors for prognosis following tumor radiotherapy and chemotherapy. Such combination also offers important references for clinical management. Nevertheless, it should be noted that there are limitations in this study, which is a retrospective analysis predominantly relying on existing data, leading to limited generalizability of the results.
Footnotes
Provenance and peer review: Unsolicited article; Externally peer reviewed.
Peer-review model: Single blind
Specialty type: Oncology
Country of origin: China
Peer-review report’s classification
Scientific Quality: Grade B, Grade C
Novelty: Grade B, Grade C
Creativity or Innovation: Grade B, Grade B
Scientific Significance: Grade C, Grade C
P-Reviewer: Kawanishi S, Chief Physician, Japan; Wang GF, MD, Chief Physician, Japan S-Editor: Li L L-Editor: A P-Editor: Wang WB
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