Skip to main content
Download PDF

Correlation between sarcopenia and esophageal cancer: a narrative review

World Journal of Surgical Oncology volume 22, Article number: 27 (2024) Cite this article

Abstract

Background

In recent years, the research on the relationship between sarcopenia before and after the treatment of esophageal cancer, as well as its impact on prognosis of esophageal cancer, has increased rapidly, which has aroused people’s attention to the disease of patients with esophageal cancer complicated with sarcopenia. This review examines the prevalence of sarcopenia in patients with esophageal cancer, as well as the relationship between sarcopenia (before and after surgery or chemotherapy) and prognosis in patients with esophageal cancer. Moreover, we summarized the potential pathogenesis of sarcopenia and pharmacologic and non-pharmacologic therapies.

Methods

A narrative review was performed in PubMed and Web of Science using the keywords (“esophageal cancer” or “esophageal neoplasm” or “neoplasm, esophageal” or “esophagus neoplasm” or “esophagus neoplasms” or “neoplasm, esophagus” or “neoplasms, esophagus” or “neoplasms, esophageal” or “cancer of esophagus” or “cancer of the esophagus” or “esophagus cancer” or “cancer, esophagus” or “cancers, esophagus” or “esophagus cancers” or “esophageal cancer” or “cancer, esophageal” or “cancers, esophageal” or “esophageal cancers”) and (“sarcopenia” or “muscular atrophy” or “aging” or “senescence” or “biological aging” or “aging, biological” or “atrophies, muscular” or “atrophy, muscular” or “muscular atrophies” or “atrophy, muscle” or “atrophies, muscle” or “muscle atrophies”). Studies reporting relationship between sarcopenia and esophageal cancer were analyzed.

Results

The results of the review suggest that the average prevalence of sarcopenia in esophageal cancer was 46.3% ± 19.6% ranging from 14.4 to 81% and sarcopenia can be an important predictor of poor prognosis in patients with esophageal cancer. Patients with esophageal cancer can suffer from sarcopenia due to their nutritional deficiencies, reduced physical activity, chemotherapy, and the effects of certain inflammatory factors and pathways. When classic diagnostic values for sarcopenia such as skeletal muscle index (SMI) are not available clinically, it is also feasible to predict esophageal cancer prognosis using simpler metrics, such as calf circumference (CC), five-count sit-up test (5-CST), and six-minute walk distance (6MWD).

Conclusions

Identifying the potential mechanism of sarcopenia in patients with esophageal cancer and implementing appropriate interventions may hold the key to improving the prognosis of these patients.

Introduction

According to the latest data from the Global Cancer Observatory (GLOBOCAN) database, esophageal cancer (EC) ranks as the eighth most frequently diagnosed cancer and the sixth leading cause of cancer-related death in 2020 [1]. Moreover, the incidence of esophageal cancer has been steadily increasing in recent years. Currently, surgical resection, radiotherapy, and chemotherapy are important means of treating esophageal cancer [2]. For patients with resectable esophageal cancer, according to TNM staging, resectable patients with limited disease of cT1-T2, cN0M0 can be directly treated with surgical resection, whereas patients with locally advanced resectable patients with staging cT3-4 or cN1-3M0 need neoadjuvant chemoradiotherapy or definitive chemoradiotherapy or perioperative chemotherapy before surgery [3]. Esophageal cancer is histologically classified as squamous cell carcinoma (SCC) or adenocarcinoma, with different etiology, pathology, tumor location, treatment, and prognosis [4]. Worldwide, > 85% of all esophageal cancer cases are esophageal squamous cell carcinoma (ESCC) [5]. Alcohol consumption and smoking are responsible for the majority of ESCC cases worldwide, whereas the main risk factors for EAC are gastroesophageal reflux disease (GERD), abdominal obesity, and smoking [4, 5]. ESCC is usually located at or above the tracheal bifurcation, has a tendency for early lymphatic spread, has a poor prognosis, and is the most common histologic type in Eastern Europe, Asia, and Africa, whereas esophageal adenocarcinoma usually involves the lower and middle esophagus and is most common in North America and Western Europe [4, 6]. In addition to this, ESCC is mainly treated with chemoradiotherapy (CRT) with or without surgery. Adenocarcinoma (AC), on the other hand, is usually treated with induction therapy and surgical resection, although the optimal induction regimen is controversial [7]. Unfortunately, since most patients with esophageal cancer are diagnosed at an advanced stage, the overall 5-year survival rate for esophageal cancer remains disappointingly low, with less than 20% of patients surviving beyond this timeframe despite advances in treatment. Therefore, understanding the risk factors associated with esophageal cancer is of paramount importance for public health and clinical decision-making, particularly in terms of risk stratification, screening, and prevention [5].

The concept of muscle function was initially introduced through six consensus definitions in 2010, while the diagnosis of sarcopenia was officially established by the International Classification of Diseases-10 in 2016 [8]. In 2010, the European Working Group on Sarcopenia in Older People (EWGSOP) reported a practical definition of sarcopenia [9]. A similar approach was adopted by the Asian Working Group on Sarcopenia (AWGS) [10]. According to these definitions, sarcopenia is characterized by low muscle mass along with poor muscle function. AWGS demonstrated that sarcopenia should be described as low muscle mass plus low muscle strength and/or low physical performance, and they also recommend outcome indicators for further researches, as well as the conditions that sarcopenia should be assessed. Moreover, they also recommend cutoff values for muscle mass measurements (7.0 kg/m2 for men and 5.4 kg/m2 for women by using dual X-ray absorptiometry and 7.0 kg/m2 for men and 5.7 kg/m2 for women by using bioimpedance analysis), handgrip strength (< 26 kg for men and < 18 kg for women), and usual gait speed (< 0.8 m/s). In 2018, EWGSOP revised the consensus and proposed a new definition of sarcopenia, EWGSOP-2 [11]. In this updated definition, EWGSOP-2 includes muscle strength as an important factor and recommends specific cut-off points for the components of sarcopenia. According to EWGSOP-2, sarcopenia is defined by low levels of measures for three parameters: (1) muscle strength, (2) muscle quantity/quality, and (3) physical performance as an indicator of severity [11].

Sarcopenia is characterized as a progressive and generalized skeletal muscle disorder, involving the accelerated loss of muscle mass and function. Notably, sarcopenia has been identified as a prognostic factor for certain cancer types and has been associated with an increased risk of adverse outcomes, including falls, decreased function, frailty, physical disability, and mortality [8, 11]. In the realm of human health, sarcopenia not only heightens the risk of falls and fractures but also impacts activities of daily living, mobility, and has been linked to heart disease, respiratory disease, and cognitive impairment, thereby leading to movement disorders and a diminished quality of life [11]. Recently, sarcopenia has garnered significant attention in the field of oncology and has emerged as a crucial predictor of long-term prognosis in patients with esophageal cancer [12,13,14]. Given the rising number of elderly patients diagnosed with esophageal cancer, it is worth noting that these individuals often experience cancer-related malnutrition, which contributes to the development of sarcopenia [15]. Additionally, it has been observed that geriatric syndromes such as sarcopenia can impede recovery from esophageal cancer [16].

In this comprehensive review, we delve into various aspects related to sarcopenia in patients with esophageal cancer, including its incidence, prognostic value, the interplay between chemotherapy and sarcopenia, the underlying mechanisms of sarcopenia, therapeutic approaches, and alternative methods for predicting sarcopenia. Our aim is to critically evaluate the combined prognostic impact of factors associated with esophageal cancer and sarcopenia, drawing practical conclusions to support the multidisciplinary management of patients with esophageal cancer and offering fresh insights for the development of therapeutic regimens targeting this disease.

Prevalence of sarcopenia in esophageal cancer

The prevalence of sarcopenia exhibited considerable variation, depending on the definitions, diagnostic methods, classifications, and cut-off points employed [17]. Notably, several investigations have highlighted disparities in the prevalence of sarcopenia across different regions and age groups [18]. Specifically, sarcopenia affects 5–13% of people aged 60 to 70 and up to 50% of people over 80 [19]. Furthermore, it has been observed that sarcopenia is a prevalent condition within the field of oncology, affecting approximately 35.3% of patients [20]. In a study conducted by Haiducu et al. [21], it was demonstrated that sarcopenia is highly prevalent (43.68%) among individuals with gastrointestinal tumors, with esophageal cancer exhibiting the highest prevalence (70.4%) due to the frequently associated symptom of dysphagia. Additionally, a meta-analysis conducted by Jogiat et al. [13], which encompassed 21 studies and 3966 patients, identified sarcopenia in 1940 individuals, reflecting a prevalence rate of 48.1%. Among the included studies (Table 1), the average prevalence of sarcopenia in esophageal cancer was found to be 46.3% ± 19.6%. However, the prevalence of sarcopenia in patients with esophageal cancer varies considerably due to differences in study populations, age, diagnostic methods, and criteria, and the criteria used to determine the prevalence of sarcopenia varied among the studies in this review, as shown in Table 1, with prevalence rates ranging from 14.4 to 81%. For instance, Tan et al. [22] employed computed tomography (CT) data to retrospectively diagnose sarcopenia in esophageal cancer patients, revealing a sarcopenia prevalence of 75.9%. Conversely, Yoshida et al. [23] conducted a prospective study involving 71 patients with esophageal cancer, utilizing the bioelectrical impedance analysis (BIA) method to diagnose sarcopenia, and reported a sarcopenia prevalence of 40.8% in this cohort. Despite discrepancies in diagnostic criteria and methods, sarcopenia was frequently diagnosed during preoperative examinations in patients with esophageal cancer. Given that esophageal cancer exhibits the highest prevalence of sarcopenia among gastrointestinal tumors, it is imperative to allocate greater attention to this condition in esophageal cancer patients.

Table 1 Prediction effect of preoperative sarcopenia on prognosis of esophageal cancer
Full size table

The role of sarcopenia in the prognosis of surgical treatment of esophageal cancer

Relationship between preoperative muscle loss and prognosis in esophageal cancer

Sarcopenia, a condition characterized by the loss of muscle mass, has a significant impact on the postoperative prognosis of esophageal cancer. Numerous studies have demonstrated that preoperative sarcopenia not only increases the risk of complications such as pulmonary issues and mortality in older adults, but also leads to extended hospital stays and reduced survival rates. In a retrospective study by Elliott et al. [25], it was discovered that preoperative sarcopenia independently predicted an increase in the Charlson Comorbidity Index (CCI), prolonged length of hospital stay, major postoperative complications, postoperative pulmonary complications (PPC), pneumonia, and prolonged intubation time. Similarly, a retrospective study conducted by Fehrenbach et al. [29] revealed that esophageal cancer patients with comorbid sarcopenia faced a higher risk of major complications and prolonged hospitalization, while obese patients with sarcopenia were significantly more likely to experience pneumonia and extended hospital stays. Nakashima et al. [24] conducted a study on elderly patients with esophageal cancer and found that sarcopenia in this demographic was associated with a higher incidence of anastomotic fistulae and in-hospital death. Another prospective study by Makiura et al. [27] demonstrated that patients with skeletal sarcopenia had a significantly higher rate of unplanned 90-day readmission, with sarcopenia itself being an independent predictor of this outcome according to multivariate logistic regression analysis.

Apart from its impact on surgical complications, preoperative sarcopenia has also been linked to long-term prognosis. Makiura et al. [27] found that sarcopenia reduced overall survival (OS) according to log-rank tests. Another retrospective study [44] identified sarcopenia as an independent prognostic factor affecting both OS and disease-free survival (DFS). Sugimura et al. [38] conducted a study involving 363 patients who underwent esophagectomy and discovered that low preoperative skeletal muscle index (SMI) was associated with poor long-term survival. Additionally, Takahashi et al. [37] observed that preoperative sarcopenia decreased postoperative OS and recurrence-free survival (RFS). Given its implications for postoperative complications and prognosis in esophageal cancer, sarcopenia has emerged as a crucial prognostic factor. The studies listed in Table 1 provide evidence of sarcopenia’s association with complications and prognosis in esophageal cancer. Consequently, the routine evaluation and accurate diagnosis of sarcopenia in esophageal cancer patients can assist clinicians in tailoring treatment plans, providing timely nutritional support, and ultimately improving short-term and long-term patient outcomes, as well as the overall prognosis of esophageal cancer.

Relationship between postoperative muscle loss and prognosis in esophageal cancer carcinoma

Previous investigations have primarily focused on examining the consequences of preoperative sarcopenia on postoperative complications and prognosis. However, the impact of diminished skeletal muscle mass following esophagectomy in individuals with esophageal cancer on long-term postoperative prognosis remains insufficiently explored [48]. The loss of skeletal muscle mass in the acute phase after surgery may serve as a novel prognostic indicator for long-term outcomes, particularly in highly invasive procedures like ESCC surgery. Notably, it was observed that the 3-year overall survival rate was notably lower in the group with severely reduced total psoas mass index (TPI) compared to the group with mildly reduced TPI [49]. A study by Takahashi et al. [50] found that substantial skeletal muscle loss in esophageal cancer patients after 3 months postoperatively was associated with poorer OS and RFS. Additionally, another study revealed a significant correlation between reduced SMI and a worsened prognosis following esophageal cancer resection [51]. Kudou et al.’s study [52] demonstrated that the development of postoperative sarcopenia in patients with adenocarcinoma of the esophagogastric junction (AEG) and upper gastric cancer (UGC) independently predicted poor overall survival in multivariate analysis. Furthermore, the progression of sarcopenia was found to be indicative of unfavorable recurrence-free survival in patients with AEG and UGC. Another retrospective study [53] indicated that a greater decline in PMI after neoadjuvant chemoradiation therapy (NACRT) and esophagectomy constituted a significant risk factor for overall survival and recurrence-free survival. The prognosis of postoperative muscle loss in esophageal cancer has received limited attention and the timing of postoperative detection of sarcopenia varies considerably across studies, but each of these studies consistently demonstrates a substantial association between postoperative muscle loss or reduced skeletal muscle mass and poor prognosis, and more prospective cohort studies are needed to demonstrate this association.

Chemotherapy and sarcopenia

Chemotherapy-induced sarcopenia

Multimodal neoadjuvant concurrent chemoradiotherapy (CCRT) has gained traction in the treatment of esophageal cancer, specifically in cases of ESCC and esophageal adenocarcinoma [54]. The incidence of sarcopenia can rise by 17% from neoadjuvant chemotherapy until the completion of treatment in individuals with tumors [55]. A particular study [56] underscored the negative impact of chemotherapy-related adverse events, such as fatigue, loss of appetite, nausea, vomiting, and diarrhea, on food intake, physical activity, and ultimately, the severe loss of muscle mass. In a retrospective cohort study conducted by Halliday et al. [57], significant reductions in body weight, BMI, skeletal muscle (SM) area, skeletal muscle index (SMI), visceral adipose tissue (VAT), and total adipose tissue (TAT) were observed following neoadjuvant therapy. Fujihata et al. [58] investigated esophageal cancer-related skeletal muscle wasting (SMW) during neoadjuvant chemotherapy (NAC) and discovered a declining trend in SMI and body weight among patients with esophageal cancer during NAC treatment. Furthermore, decreasing SMI was found to be associated with a higher incidence of postoperative anastomotic fistula. In another retrospective study [59], it was determined that the mean change in total psoas area (TPA) of patients before and after neoadjuvant chemotherapy was 7.3% (6.8%). During neoadjuvant therapy, 43 (81.1%) patients experienced some degree of psoas loss. The target population in certain studies extends beyond patients with esophageal cancer. For instance, Oflazoglu et al. [60] included a substantial number of patients with primary tumors and assessed various indicators of sarcopenia before chemotherapy, as well as at the third and sixth months following chemotherapy. Their findings indicated a continuous rise in the prevalence of sarcopenia during chemotherapy. The study by Jogiat et al. [61] also corroborated this point. They observed that the prevalence of sarcopenia in patients with esophageal cancer increased from 17.0% before chemotherapy to 38.1% after chemotherapy, nearly doubling the incidence of sarcopenia in this specific patient group.

Sarcopenia leads to increased chemotherapy-related toxicity

Due to the narrow therapeutic range of chemotherapeutic agents used for esophageal cancer, it becomes crucial to identify factors that can predict individual variances in chemotherapy toxicity and effectiveness [62]. A retrospective study [63] discovered a significantly higher occurrence of grade 3–4 toxicity among the 184 ESCC patients included, who also had sarcopenia. The major treatment-related toxicities observed in grades 3–4 were leukopenia, neutropenia, esophagitis, and anorexia. Several other studies [64, 65] have yielded similar findings. Furthermore, additional studies [66, 67] have demonstrated that sarcopenia increases the likelihood of dose-limiting toxicity (DLT) and serves as a significant predictor of DLT. Tan et al. [66] conducted a retrospective study specifically focusing on the impact of sarcopenia on dose-limiting toxicity of neoadjuvant chemotherapy in patients with esophagogastric cancer. The study revealed a significant correlation between sarcopenia and DLT, highlighting the necessity of employing various methods to assess skeletal muscle mass in order to predict toxicity and customize chemotherapy dosage. Another retrospective study conducted by Ota et al. [62] also identified sarcopenia as an independent predictor of poor pathological response.

Table 2 lists the studies related to the effect of sarcopenia on chemotherapy in esophageal cancer. Based on the aforementioned studies, it is evident that sarcopenia independently indicates reduced overall survival [14, 63, 68,69,70], disease-free survival [40, 71], and recurrence-free survival [14] in patients with esophageal cancer who undergo chemotherapy. Furthermore, sarcopenia increases the incidence of toxic reactions [66, 67], mucositis, fever [71], and lymphopenia [70], consequently leading to perioperative complications [68, 72], an elevated risk of postoperative recurrence rates [40], and postoperative mortality [73]. Early implementation of appropriate nutritional intervention prior to treatment may improve prognosis [74].

Table 2 Predictive effect of pre-chemotherapy sarcopenia on chemotherapy toxicity
Full size table

Potential mechanisms of esophageal cancer-associated sarcopenia

In individuals afflicted with EC, sarcopenia may arise as a result of nutritional deficiencies caused by dysphagia, pain, systemic inflammation, and an augmented metabolic rate [63].

Malnutrition

Malnutrition is a condition characterized by changes in body composition and cellular mass resulting from inadequate nutrient intake or absorption. This deficiency leads to compromised physical and mental abilities, with involuntary weight loss being one of its prominent manifestations [78]. Moreover, malnutrition has been linked to the mechanisms of sarcopenia [79]. The development of malnutrition-induced sarcopenia is influenced by various factors, including abnormal protein and energy metabolism in tumor cells, inflammation, impaired immunity, and cancer-related symptoms such as fatigue, pain, cough, and loss of appetite [14]. Gastrointestinal cancers, such as esophageal and gastric cancer, often exhibit reduced gastrointestinal function, particularly affecting swallowing and digestion in esophageal cancer. Consequently, protein intake is adversely affected. Among all types of cancer, esophageal cancer has one of the highest prevalence rates of increased nutritional risk, exceeding 60% [79].

Lack of exercise lifestyle

Lack of physical activity is widely acknowledged as the primary risk factor for sarcopenia [19]. The decline in skeletal muscle mass and strength becomes apparent around the age of 40, and the incidence of sarcopenia increases with age. Furthermore, the loss of muscle mass and strength accelerates as individuals grow older [80]. Sedentary individuals experience a more significant decline in muscle fiber and strength compared to those who are physically active [19]. There is often a decrease in physical activity after esophagectomy [81]. Therefore, patients with esophageal cancer should also pay attention to sarcopenia due to reduced physical activity.

Inflammation

Inflammation is a response triggered by tissue dysfunction or disturbances in the body’s balance, and it is believed to underlie various physiological and pathological processes [82]. Inflammatory cells and mediators are present in the microenvironment of most tumors [83]. Pro-inflammatory cytokines, including interleukin-1 (IL-1), IL-6, and tumor necrosis factor-α (TNF-α), have been identified as mediators of anorexia and the breakdown of skeletal muscle protein, which are crucial components of cancer malignant stroma [12]. These cytokines contribute to muscle deterioration by promoting the infiltration of inflammatory cells through NF-κB [84], esophageal cancer has been shown to activate NF-κB [73], and this activation of the NF-κB pathway is paralleled by a simultaneous increase in IL-1, IL-6, and TNF-α [85]. TNF-α exacerbates catabolism (protein loss, insulin resistance), impairs muscle contraction, disrupts myogenesis, and ultimately leads to muscle weakness [86]. The chronic inflammatory response not only diminishes skeletal muscle function but also triggers a vicious cycle by inducing skeletal muscle tissue dysfunction, thus accelerating the progression of sarcopenia [82].

Chemotherapy causes sarcopenia

A multicenter study demonstrated that neoadjuvant chemoradiation in esophageal cancer patients increased the percentage of sarcopenia [64], and another study found that 32.5% of esophageal cancer patients had body composition changes during NAC (patients with ≥ 3% increase in visceral fat mass (VFM) and ≥ 3% decrease in PMI) [87]. In addition, a systematic review noted that esophageal cancer patients receiving chemotherapy are at risk for severe loss of skeletal muscle mass [88]. Several adverse effects of chemotherapy, such as fatigue, loss of appetite, nausea, vomiting, diarrhea, taste disturbances, anorexia, mucositis, and dysphagia, can negatively impact food intake, physical activity, and ultimately result in significant muscle mass loss [89]. Insulin-like growth factor-1 (IGF-1) is a well-studied activator of muscle hypertrophy, and its receptor, IGF-1 R, mediates protein synthesis activation [90]. The IGF 1-PI3K-Akt/PKB-mTOR pathway positively regulates muscle growth [91]. However, certain chemotherapeutic agents, such as cisplatin, one of the commonly used drugs in chemotherapy for esophageal cancer, can reduce IGF-1 protein levels by approximately 85% and inhibit IGF-1/PI3K/Akt signaling in skeletal muscle [92]. Consequently, the downregulation of IGF-1 expression in skeletal muscle during chemotherapy may be a significant factor contributing to the development of muscle weakness in cancer patients [92]. Chemotherapeutic drugs such as cisplatin and irinotecan directly induce muscle loss by activating the transcription factor NF-κB, which upregulates ubiquitin and the proteasome, leading to increased protein breakdown and the release of inflammatory cytokines (IL-1 β, IL-6, and TNF-α). These inflammatory cytokines further enhance the activity of E3 ligase (atrogin-1) and promote ubiquitin-mediated protein degradation [86].

Other signaling pathways

mTOR is a crucial regulator of skeletal muscle mass [90], and the IGF1-PI3K-Akt/PKB-mTOR pathway positively regulates muscle growth [91]. mTOR also plays a significant role in mitochondrial metabolism, protein synthesis enhancement, and the promotion of mitochondrial biosynthesis and adipogenesis. The tumor suppressors liver kinase B1 (LKB1) and AMPK regulate cell growth in response to changes in environmental nutrient levels and generally downregulate the mTOR pathway, resulting in reduced protein synthesis and the development of sarcopenia [93].

Predicting esophageal cancer prognosis with a simple indicator in the diagnosis of sarcopenia

In addition to employing SMI values to define sarcopenia and determine esophageal cancer prognosis in most studies, numerous researchers have utilized alternative methods as prognostic indicators for esophageal cancer. For instance, several studies have showcased the predictive role of skeletal muscle mass loss in determining esophageal cancer prognosis [51, 87, 88, 94]. Moreover, measurements of the total psoas major area (TPA) [59] and the psoas muscle index [53] have been utilized as surrogate markers of sarcopenia to predict postoperative complications, overall survival (OS), and recurrence-free survival (RFS) in esophageal cancer patients. Furthermore, Kurita conducted several studies [95,96,97] employing hand grip strength (HGS) and the five-count sit-up test as predictors of esophageal cancer prognosis, revealing that HGS and 5-CST can significantly predict complications such as postoperative pneumonia. A retrospective study by Zhou et al. [98] also identified low subcutaneous fat as a risk factor for increased mortality. Additionally, the sarcopenia index, specifically the serum creatinine/cystatin C ratio, has been employed to predict prognosis in esophageal cancer patients and has been associated with postoperative complications and long-term survival [99]. This index has also demonstrated similar associations in other types of cancer [100,101,102,103]. Alongside grip strength and 5-CST, gait speed (GS) and six-minute walk distance, which are diagnostic criteria for sarcopenia, can be utilized to determine a patient’s prognosis. A prospective study analyzing 922 elderly men revealed that slow gait speed increased the risk of death in elderly male cancer patients [104]. Multiple other studies have demonstrated that GS and 6MWD can predict survival [105, 106] and complications [107, 108]. Additionally, some studies have proposed the use of calf circumference (CC) as a diagnostic indicator for sarcopenia to enhance diagnostic accuracy [109]. A prospective study by Sousa et al., which included 250 patients, discovered that a low CC predicted the risk of death in cancer patients [110]. Several other studies have also indicated that CC can serve as a simpler, faster, and cost-effective measurement to rapidly screen patients at risk of death [111,112,113].

Besides assessing the presence of sarcopenia according to diagnostic criteria and gauging its prognostic significance, researchers have been particularly intrigued by the extent of skeletal muscle mass reduction during treatment or post-surgery. In instances where standardized tests fail to meet the criteria for diagnosing sarcopenia, employing alternative, efficient methods like HGS, 5-SCT, GS, 6MWD, and CC to predict prognosis is highly desirable (Table 3).

Table 3 A simpler way replaces sarcopenia to predict esophageal cancer prognosis
Full size table

Treatment of sarcopenia

Non-pharmacological treatment

A comprehensive assessment has concluded that the implementation of suitable physical activity, strength training, and nutritional interventions, coupled with a stable biological clock, holds the potential to enhance skeletal muscle growth, decelerate skeletal muscle deterioration, and ameliorate symptoms associated with sarcopenia [119].

The absence of physical activity has been linked to a decline in muscle strength and mass. Hence, exercise programs are considered the fundamental element in the treatment of sarcopenia, as they can mitigate muscle loss by reducing the activation of NF-κB [120]. Short-term resistance exercise has demonstrated the ability to enhance the synthesis of proteins in skeletal muscle, bolstering its ability and capacity [19]. Long-term resistance training, on the other hand, has proven to enhance both muscle strength and mass [121]. A systematic review has revealed that resistance training, as well as a combination of resistance training with other exercises, can enhance muscle strength and gait speed (GS) [122]. Furthermore, specific strength exercises contribute to the amelioration of muscle function and neuromuscular adaptations [119]. In a cohort study conducted by Ziegler et al. [121], subjects were randomly assigned to either a 1-year heavy resistance training (HRT) group or a control group (CON). After 12 months of training, the HRT group exhibited significantly higher isometric and dynamic muscle strength compared to the control group.

Certain nutritional interventions, such as the consumption of high-protein or essential amino acids like leucine, in conjunction with resistance training, have the potential to delay skeletal muscle loss observed in sarcopenia [119]. Specific dietary patterns, including the consumption of adequate protein such as leucine-containing protein supplements or whey protein, vitamin D, antioxidant nutrients, and long-chain polyunsaturated fatty acids, have proven beneficial in the prevention and improvement of sarcopenia [18]. Esophageal cancer patients undergoing esophagectomy require careful postoperative nutritional monitoring due to fasting requirements. Studies have indicated that more than half of the patients exhibited inadequate oral intake upon discharge [123]. Therefore, for patients with esophageal cancer, enteral nutrition is a preferred option to meet internal nutritional requirements, while parenteral nutrition can be considered if enteral nutrition is insufficient or undesirable [124]. It has been observed that patients receiving nutritional management exhibited higher serum total protein and albumin levels, fewer postoperative adverse events, and lower hospitalization costs compared to those following a conventional diet [125]. Additionally, declines in weight, BMI, and appendicular skeletal muscle mass index (ASMI) were significantly reduced, leading to improvements in patients’ quality of life and fatigue status [74]. Another retrospective study [126] noted that adults who received early nutritional support during neoadjuvant therapy experienced less weight loss at 12 months after esophagectomy compared to those who received oral nutritional support after surgery. Therefore, providing appropriate nutritional support at the correct time is of utmost importance for patients with esophageal cancer.

Skeletal muscle, as a peripheral organ, is regulated by the biological clock [127], a mechanism that fosters skeletal muscle growth and maintains homeostasis within the body [119]. A review encompassing numerous studies on genetic strategies involving targeted gene failure in mice specifically related to skeletal muscle has revealed that many circadian mutants exhibit muscle defects [127]. A deeper understanding of the molecular clock of skeletal muscle and its relationship with muscle-skeletal interactions could yield valuable insights into sarcopenia. Consequently, more effective intervention strategies (e.g., exercise and dietary restrictions) can be developed based on the biological clock [128]. This, in turn, could help prevent muscle loss during aging or in chronic diseases that may lead to sarcopenia by preserving and promoting the proper functioning of intrinsic muscle clock mechanisms [129].

Pharmacologic treatment

Currently, there are no FDA-approved treatments available for sarcopenia [19]. However, a comprehensive review has revealed the existence of several recommended agents with varying degrees of effectiveness. These include growth hormone, anabolic or androgenic steroids, selective androgen receptor modulators, protein anabolic agents, appetite stimulants, myostatin inhibitors, activating II receptor drugs, β-receptor blockers, angiotensin-converting enzyme inhibitors, and troponin activators [18].

In a study conducted by Hirani et al. [130], it was discovered that low levels of vitamin D were significantly associated with the occurrence of sarcopenia. Therefore, maintaining adequate vitamin D levels may reduce the incidence of this condition. Another cross-sectional study found a correlation between growth hormone (GH) and insulin-like growth factor (IGF-1) with sarcopenia in older adults. This suggests that the use of IGF-1 and GH may potentially increase skeletal muscle mass [131]. Additionally, it was observed that individuals taking metformin [132] or statins [133] had a lower risk of developing sarcopenia compared to those not taking these medications. This demonstrates the potential protective effect of metformin against sarcopenia. Furthermore, it appears that statins may also prevent the development of sarcopenia, with higher doses showing a more pronounced preventive effect. A prospective study involving 740 older adults revealed a significant positive correlation between calcium intake and appendicular lean mass (ALM) [134]. Animal studies have also suggested that losartan may slow down muscle degeneration, promote clinical benefits, and provide protection for patients with sarcopenia [135, 136].

Despite the existence of studies showcasing the positive effects of the aforementioned drugs in sarcopenia patients, their efficacy remains a subject of controversy. Furthermore, the optimal dosage and potential side effects of these drugs require further investigation through additional studies. The pharmacological treatment of sarcopenia necessitates more extensive exploration and clinical trials to scientifically evaluate the efficacy of these drugs.

Conclusions and future perspectives

To date, the majority of studies investigating sarcopenia in esophageal cancer patients have primarily relied on retrospective approaches, severely constraining their ability to comprehensively depict patient populations. Consequently, our understanding of the underlying mechanisms linked to heightened adverse outcomes remains limited [137]. Hence, it is imperative to conduct more prospective evaluations on sarcopenia in individuals afflicted with esophageal cancer. These evaluations will enable us to establish a more profound comprehension of the correlation between sarcopenia, characterized by the depletion of skeletal muscle mass or strength, and adverse outcomes or post-treatment complications. Furthermore, they will facilitate the development of precise and personalized interventions based on the findings, thereby enhancing outcomes in high-risk populations [137]. By performing requisite assessments of sarcopenia in esophageal cancer patients, we can devise optimal treatment strategies that rectify the sarcopenic condition prior to surgery or chemotherapy through nutritional support and exercise, adjuvant therapy, and meticulous postoperative monitoring [138]. This comprehensive approach aims to augment the quality of life for patients with esophageal cancer while simultaneously alleviating the healthcare burden on society.

Availability of data and materials

Not applicable.

Abbreviations

CC:

Calf circumference

5-CST:

Five-count sit-up test

6MWD:

Six-minute walk distance

GLOBOCAN:

Global cancer observatory

EC:

Esophageal carcinoma

SCC:

Squamous cell carcinoma

ESCC:

Esophageal squamous cell carcinoma

GERD:

Gastroesophageal reflux disease

CRT:

Chemoradiotherapy

AC:

Adenocarcinoma

EWGSOP:

European working group on sarcopenia in older people

AWGS:

Asian working group on sarcopenia

CT:

Computed tomography

BIA:

Bioelectrical impedance analysis

CCI:

Charlson comorbidity index

PPC:

Postoperative pulmonary complications

OS:

Overall survival

DFS:

Disease-free survival

SMI:

Skeletal muscle mass index

RFS:

Recurrence-free survival

BMI:

Body mass index

PMI:

Psoas muscle index

IQR:

Interquartile range

HGS:

Hand grip strength

ASM:

Appendicular skeletal muscle mass

LAEC:

Locally advanced esophageal cancer

PFS:

Progress-free survival

GEC:

Gastroesophageal cancer

GS:

Gait speed

LOS:

Length of stay

EGJC:

Esophagogastric junction carcinoma

UGC:

Upper gastric cancer

MEC:

Metastatic esophageal cancer

NA:

No available

TPI:

Total psoas mass index

AEG:

Adenocarcinoma of esophagogastric junction

UGC:

Upper gastric cancer

NACRT:

Neoadjuvant chemoradiation therapy

CCRT:

Concurrent chemoradiotherapy

SM:

Skeletal muscle

VAT:

Visceral adipose tissue

TAT:

Total adipose tissue

SMW:

Skeletal muscle wasting

NAC:

Neoadjuvant chemotherapy

TPA:

Total psoas area

DLT:

Dose-limiting toxicity

GC:

Gastric cancer

GEJC:

Gastro-esophageal junction cancer

RDI:

Relative dose intensity

OGC:

Oesophago-gastric cancer

FN:

Febrile neutropenia

PP:

Postoperative pneumonia

IL-1:

Interleukin-1

TNF-α:

Tumor necrosis factor-α

VFM:

Visceral fat mass

IGF-1:

Insulin-like growth factor-1

LKB1:

Liver kinase B1

CL:

Chyle leak

SI:

Sarcopenia index

HRT:

Heavy resistance training

CON:

Control group

ASMI:

Appendicular skeletal muscle mass index

GH:

Growth hormone

ALM:

Appendicular lean mass

References

  1. Morgan E, Soerjomataram I, Rumgay H, Coleman HG, Thrift AP, Vignat J, Laversanne M, Ferlay J, Arnold M. The global landscape of esophageal squamous cell carcinoma and esophageal adenocarcinoma incidence and mortality in 2020 and projections to 2040: new estimates from GLOBOCAN 2020. Gastroenterology. 2022;163:649-658.e642.

    Article  PubMed  Google Scholar 

  2. Zheng Y, Li Y, Liu X, Zhang R, Wang Z, Sun H, Liu S. Neoadjuvant chemotherapy followed by minimally invasive esophagectomy versus primary surgery for management of esophageal carcinoma: a retrospective study. J Cancer. 2019;10:1097–102.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Lordick F, Mariette C, Haustermans K, Obermannová R, Arnold D. Oesophageal cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2016;27:v50–7.

    Article  CAS  PubMed  Google Scholar 

  4. Ajani JA, D’Amico TA, Bentrem DJ, Cooke D, Corvera C, Das P, Enzinger PC, Enzler T, Farjah F, Gerdes H, et al. Esophageal and esophagogastric junction cancers, version 2.2023, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw. 2023;21:393–422.

    Article  PubMed  Google Scholar 

  5. Thrift AP. Global burden and epidemiology of Barrett oesophagus and oesophageal cancer. Nat Rev Gastroenterol Hepatol. 2021;18:432–43.

    Article  PubMed  Google Scholar 

  6. Yang YM, Hong P, Xu WW, He QY, Li B. Advances in targeted therapy for esophageal cancer. Signal Transduct Target Ther. 2020;5:229.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Egyud MR, Tseng JF, Suzuki K. Multidisciplinary therapy of esophageal cancer. Surg Clin North Am. 2019;99:419–37.

    Article  PubMed  Google Scholar 

  8. Cruz-Jentoft AJ, Sayer AA. Sarcopenia. Lancet. 2019;393:2636–46.

    Article  PubMed  Google Scholar 

  9. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel JP, Rolland Y, Schneider SM, et al. Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on Sarcopenia in Older People. Age Ageing. 2010;39:412–23.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Chen LK, Liu LK, Woo J, Assantachai P, Auyeung TW, Bahyah KS, Chou MY, Chen LY, Hsu PS, Krairit O, et al. Sarcopenia in Asia: consensus report of the Asian Working Group for Sarcopenia. J Am Med Dir Assoc. 2014;15:95–101.

    Article  PubMed  Google Scholar 

  11. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, Cooper C, Landi F, Rolland Y, Sayer AA, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48:16–31.

    Article  PubMed  Google Scholar 

  12. Matsunaga T, Miyata H, Sugimura K, Motoori M, Asukai KEI, Yanagimoto Y, Takahashi Y, Tomokuni A, Yamamoto K, Akita H, et al. Prognostic significance of sarcopenia and systemic inflammatory response in patients with esophageal cancer. Anticancer Res. 2018;39:449–58.

    Article  Google Scholar 

  13. Jogiat UM, Sasewich H, Turner SR, Baracos V, Eurich DT, Filafilo H, Bédard ELR. Sarcopenia determined by skeletal muscle index predicts overall survival, disease-free survival, and postoperative complications in resectable esophageal cancer: a systematic review and meta-analysis. Ann Surg. 2022;276:e311–8.

    Article  PubMed  Google Scholar 

  14. Qian J, Si Y, Zhou K, Tian Y, Guo Q, Zhao K, et al. Sarcopenia is associated with prognosis in patients with esophageal squamous cell cancer after radiotherapy or chemoradiotherapy. BMC Gastroenterol. 2022;22:211.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Kemper M, Molwitz I, Krause L, Reeh M, Burdelski C, Kluge S, Yamamura J, Izbicki JR, de Heer G. Are muscle parameters obtained by computed tomography associated with outcome after esophagectomy for cancer? Clin Nutr. 2021;40:3729–40.

    Article  PubMed  Google Scholar 

  16. Makiura D, Ono R, Inoue J, Kashiwa M, Oshikiri T, Nakamura T, Kakeji Y, Sakai Y, Miura Y. Preoperative sarcopenia is a predictor of postoperative pulmonary complications in esophageal cancer following esophagectomy: a retrospective cohort study. J Geriatric Oncol. 2016;7:430–6.

    Article  Google Scholar 

  17. Petermann-Rocha F, Balntzi V, Gray SR, Lara J, Ho FK, Pell JP, Celis-Morales C. Global prevalence of sarcopenia and severe sarcopenia: a systematic review and meta-analysis. J Cachexia Sarcopenia Muscle. 2021;13:86–99.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Cho M-R, Lee S, Song S-K. A review of sarcopenia pathophysiology, diagnosis, treatment and future direction. J Korean Med Sci. 2022;37:e146.

  19. Dhillon RJS, Hasni S. Pathogenesis and management of sarcopenia. Clin Geriatr Med. 2017;33:17–26.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Surov A, Wienke A. Prevalence of sarcopenia in patients with solid tumors: a meta-analysis based on 81,814 patients. J Parenter Enter Nutr. 2022;46:1761–8.

    Article  CAS  Google Scholar 

  21. Haiducu C, Buzea A, Mirea LE, Dan GA. The prevalence and the impact of sarcopenia in digestive cancers. A systematic review. Roman J Int Med. 2021;59:328–44.

    Google Scholar 

  22. Tan X, Peng H, Gu P, Chen M, Wang Y. Prognostic significance of the L3 skeletal muscle index and advanced lung cancer inflammation index in elderly patients with esophageal cancer. Cancer Manag Res. 2021;13:3133–43.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Yoshida S, Nishigori T, Tsunoda S, Tanaka E, Okabe H, Kobayashi A, Nobori Y, Obama K, Hisamori S, Shide K, et al. Chronological changes in skeletal muscle mass two years after minimally invasive esophagectomy: a prospective cohort study. Surg Endosc. 2021;36:1527–35.

    Article  PubMed  Google Scholar 

  24. Nakashima Y, Saeki H, Nakanishi R, Sugiyama M, Kurashige J, Oki E, Maehara Y. Assessment of sarcopenia as a predictor of poor outcomes after esophagectomy in elderly patients with esophageal cancer. Ann Surg. 2018;267:1100–4.

    Article  PubMed  Google Scholar 

  25. Elliott JA, Doyle SL, Murphy CF, King S, Guinan EM, Beddy P, Ravi N, Reynolds JV. Sarcopenia: prevalence, and impact on operative and oncologic outcomes in the multimodal management of locally advanced esophageal cancer. Ann Surg. 2017;266:822–30.

    Article  PubMed  Google Scholar 

  26. Ida S, Watanabe M, Yoshida N, Baba Y, Umezaki N, Harada K, Karashima R, Imamura Y, Iwagami S, Baba H. Sarcopenia is a predictor of postoperative respiratory complications in patients with esophageal cancer. Ann Surg Oncol. 2015;22:4432–7.

    Article  PubMed  Google Scholar 

  27. Makiura D, Ono R, Inoue J, Fukuta A, Kashiwa M, Miura Y, Oshikiri T, Nakamura T, Kakeji Y, Sakai Y. Impact of sarcopenia on unplanned readmission and survival after esophagectomy in patients with esophageal cancer. Ann Surg Oncol. 2017;25:456–64.

    Article  PubMed  Google Scholar 

  28. Wang P-y, Chen X-k. Liu Q, Yu Y-k, Xu L, Liu X-b, Zhang R-x, Wang Z-f, Li Y: Highlighting sarcopenia management for promoting surgical outcomes in esophageal cancers: evidence from a prospective cohort study. Int J Surg. 2020;83:206–15.

    Article  PubMed  Google Scholar 

  29. Fehrenbach U, Wuensch T, Gabriel P, Segger L, Yamaguchi T, Auer TA, et al. CT body composition of sarcopenia and sarcopenic obesity: predictors of postoperative complications and survival in patients with locally advanced esophageal adenocarcinoma. Cancers. 2021;13:2921.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Sakai M, Sohda M, Saito H, Ubukata Y, Nakazawa N, Kuriyama K, Hara K, Sano A, Ogata K, Yokobori T, et al. Impact of combined assessment of systemic inflammation and presarcopenia on survival for surgically resected esophageal cancer. Am J Surg. 2021;221:149–54.

    Article  PubMed  Google Scholar 

  31. Xu J, Zheng B, Zhang S, Zeng T, Chen H, Zheng W, Chen C. Effects of preoperative sarcopenia on postoperative complications of minimally invasive oesophagectomy for oesophageal squamous cell carcinoma. J Thorac Dis. 2019;11:2535–45.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Soma D, Kawamura YI, Yamashita S, Wake H, Nohara K, Yamada K, et al. Sarcopenia, the depletion of muscle mass, an independent predictor of respiratory complications after oncological esophagectomy. Dis Esophagus. 2018;32:doy092.

  33. Fukushima T, Watanabe N, Okita Y, Yokota S, Matsuoka A, Kojima K, Kurita D, Ishiyama K, Oguma J, Kawai A, Daiko H. The evaluation of the association between preoperative sarcopenia and postoperative pneumonia and factors for preoperative sarcopenia in patients undergoing thoracoscopic-laparoscopic esophagectomy for esophageal cancer. Surg Today. 2023;53:782–90.

    Article  PubMed  Google Scholar 

  34. Cossu A, Palumbo D, Battaglia S, Parise P, De Pascale S, Gualtierotti M, Vecchiato M, Scotti GM, Gritti C, Bettinelli A, et al. Sarcopenia and patient’s body composition: new morphometric tools to predict clinical outcome after Ivor Lewis esophagectomy: a multicenter study. J Gastrointest Surg. 2023;27:1047–54.

    Article  PubMed  Google Scholar 

  35. Benadon B, Servagi-Vernat S, Quero L, Cattan P, Guillerm S, Hennequin V, Aparicio T, Lourenço N, Bouché O, Hennequin C. Sarcopenia: an important prognostic factor for males treated for a locally advanced esophageal carcinoma. Dig Liver Dis. 2020;52:1047–52.

    Article  PubMed  Google Scholar 

  36. Kudou K, Saeki H, Nakashima Y, Edahiro K, Korehisa S, Taniguchi D, Tsutsumi R, Nishimura S, Nakaji Y, Akiyama S, et al. Prognostic significance of sarcopenia in patients with esophagogastric junction cancer or upper gastric cancer. Ann Surg Oncol. 2017;24:1804–10.

    Article  PubMed  Google Scholar 

  37. Takahashi K, Nishikawa K, Furukawa K, Tanishima Y, Ishikawa Y, Kurogochi T, Yuda M, Tanaka Y, Matsumoto A, Mitsumori N, Ikegami T. Prognostic significance of preoperative osteopenia in patients undergoing esophagectomy for esophageal cancer. World J Surg. 2021;45:3119–28.

    Article  PubMed  Google Scholar 

  38. Sugimura K, Miyata H, Kanemura T, Takeoka T, Shinnno N, Yamamoto K, Omori T, Motoori M, Ohue M, Yano M. Impact of preoperative skeletal muscle mass and physical performance on short-term and long-term postoperative outcomes in patients with esophageal cancer after esophagectomy. Ann Gastroenterol Surg. 2022;6:623–32.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Nakayama T, Furuya S, Kawaguchi Y, Shoda K, Akaike H, Hosomura N, et al. Prognostic value of preoperative psoas muscle index as a measure of nutritional status in patients with esophageal cancer receiving neoadjuvant therapy. Nutrition. 2021;90:111232.

  40. Ozawa Y, Nakano T, Taniyama Y, Sakurai T, Onodera Y, Kamiya K, Hikage M, Sato C, Takaya K, Konno T, et al. Evaluation of the impact of psoas muscle index, a parameter of sarcopenia, in patients with esophageal squamous cell carcinoma receiving neoadjuvant therapy. Esophagus. 2019;16:345–51.

    Article  PubMed  Google Scholar 

  41. Peng H, Tan X. The prognostic significance of sarcopenia and the neutrophil-to-lymphocyte ratio in elderly patients with esophageal squamous cell carcinoma. Cancer Manage Res. 2021;13:3209–18.

    Article  CAS  Google Scholar 

  42. Wakefield CJ, Hamati F, Karush JM, Arndt AT, Geissen N, Liptay MJ, Borgia JA, Basu S, Seder CW. Sarcopenia after induction therapy is associated with reduced survival in patients undergoing esophagectomy for locally-advanced esophageal cancer. J Thorac Dis. 2021;13:861–9.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Srpcic M, Jordan T, Popuri K, Sok M. Sarcopenia and myosteatosis at presentation adversely affect survival after esophagectomy for esophageal cancer. Radiol Oncol. 2020;54:237–46.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Oguma J, Ozawa S, Kazuno A, Yamamoto M, Ninomiya Y, Yatabe K. Prognostic significance of sarcopenia in patients undergoing esophagectomy for superficial esophageal squamous cell carcinoma. Dis Esophagus. 2019;32:doy104.

  45. Zeuge U, Fares AF, Soriano J, Hueniken K, Bajwa J, Wang W, Schmid S, Rudolph-Naiberg S, Brown MC, Yeung J, et al. Differential prognostic significance of sarcopenia in metastatic esophageal squamous and adenocarcinoma. Esophagus. 2023;20:557–66.

    Article  PubMed  Google Scholar 

  46. Yamamoto M, Ozawa S, Koyanagi K, Kazuno A, Ninomiya Y, Yatabe K, Higuchi T, Kanamori K, Tajima K. Usefulness of skeletal muscle measurement by computed tomography in patients with esophageal cancer: changes in skeletal muscle mass due to neoadjuvant therapy and the effect on the prognosis. Surg Today. 2023;53:692–701.

    Article  PubMed  Google Scholar 

  47. Hinzpeter R, Mirshahvalad SA, Kulanthaivelu R, Murad V, Ortega C, Metser U, et al. Prognostic value of sarcopenia and metabolic parameters of (18)F-FDG-PET/CT in patients with advanced gastroesophageal cancer. Diagnostics (Basel). 2023;13:838.

    Article  CAS  PubMed  Google Scholar 

  48. Nakashima Y, Mori M. ASO author reflections: significance of skeletal muscle loss after esophagectomy for esophageal cancer. Ann Surg Oncol. 2019;27:499–499.

    Article  PubMed  Google Scholar 

  49. Maeda N, Shirakawa Y, Tanabe S, Sakurama K, Noma K, Fujiwara T. Skeletal muscle loss in the postoperative acute phase after esophageal cancer surgery as a new prognostic factor. World J Surg Oncol. 2020;18:1–10.

    Article  Google Scholar 

  50. Takahashi K, Watanabe M, Kozuki R, Toihata T, Okamura A, Imamura Y, Mine S, Ishizuka N. Prognostic significance of skeletal muscle loss during early postoperative period in elderly patients with esophageal cancer. Ann Surg Oncol. 2019;26:3727–35.

    Article  PubMed  Google Scholar 

  51. Nakashima Y, Saeki H, Hu Q, Tsuda Y, Zaitsu Y, Hisamatsu Y, Ando K, Kimura Y, Oki E, Mori M. Skeletal muscle loss after esophagectomy is an independent risk factor for patients with esophageal cancer. Ann Surg Oncol. 2019;27:492–8.

    Article  PubMed  Google Scholar 

  52. Kudou K, Saeki H, Nakashima Y, Sasaki S, Jogo T, Hirose K, Hu Q, Tsuda Y, Kimura K, Nakanishi R, et al. Postoperative development of sarcopenia is a strong predictor of a poor prognosis in patients with adenocarcinoma of the esophagogastric junction and upper gastric cancer. Am J Surg. 2019;217:757–63.

    Article  PubMed  Google Scholar 

  53. Kawakita Y, Motoyama S, Sato Y, Wakita A, Nagaki Y, Imai K, Minamiya Y. Decreases in the psoas muscle index correlate more strongly with survival than other prognostic markers in esophageal cancer after neoadjuvant chemoradiotherapy plus esophagectomy. World J Surg. 2020;44:1559–68.

    Article  PubMed  Google Scholar 

  54. Huang FL, Yu SJ. Esophageal cancer: risk factors, genetic association, and treatment. Asian J Surg. 2018;41:210–5.

    Article  PubMed  Google Scholar 

  55. Yip C, Goh V, Davies A, Gossage J, Mitchell-Hay R, Hynes O, Maisey N, Ross P, Gaya A, Landau DB, et al. Assessment of sarcopenia and changes in body composition after neoadjuvant chemotherapy and associations with clinical outcomes in oesophageal cancer. Eur Radiol. 2014;24:998–1005.

    Article  PubMed  Google Scholar 

  56. Kakinuma K, Tsuruoka H, Morikawa K, Furuya N, Inoue T, Miyazawa T, Mineshita M. Differences in skeletal muscle loss caused by cytotoxic chemotherapy and molecular targeted therapy in patients with advanced non-small cell lung cancer. Thoracic Cancer. 2018;9:99–104.

    Article  CAS  PubMed  Google Scholar 

  57. Halliday LJ, Boshier PR, Doganay E, Wynter-Blyth V, Buckley JP, Moorthy K. The effects of prehabilitation on body composition in patients undergoing multimodal therapy for esophageal cancer. Dis Esophagus. 2023;36:doac046.

  58. Fujihata S, Ogawa R, Nakaya S, Hayakawa S, Okubo T, Sagawa H, Tanaka T, Takahashi H, Matsuo Y, Takiguchi S. The impact of skeletal muscle wasting during neoadjuvant chemotherapy on postoperative anastomotic leakage in patients with esophageal cancer. Esophagus. 2020;18:258–66.

    Article  PubMed  Google Scholar 

  59. Yassaie SS, Keane C, French SJH, Al-Herz FAJ, Young MK, Gordon AC. Decreased total psoas muscle area after neoadjuvant therapy is a predictor of increased mortality in patients undergoing oesophageal cancer resection. ANZ J Surg. 2019;89:515–9.

    Article  PubMed  Google Scholar 

  60. Oflazoglu U, Alacacioglu A, Varol U, Kucukzeybek Y, Salman T, Taskaynatan H, Yildiz Y, Saray S, Tarhan MO. Chemotherapy-induced sarcopenia in newly diagnosed cancer patients: Izmir Oncology Group (IZOG) study. Support Care Cancer. 2020;28:2899–910.

    Article  PubMed  Google Scholar 

  61. Jogiat UM, Baracos V, Turner SR, Eurich D, Filafilo H, Rouhi A, et al. Changes in sarcopenia status predict survival among patients with resectable esophageal cancer. Ann Surg Oncol. 2023;30:7412–21.

    Article  PubMed  Google Scholar 

  62. Ota T, Ishikawa T, Endo Y, Matsumura S, Yoshida J, Yasuda T, et al. Skeletal muscle mass as a predictor of the response to neo-adjuvant chemotherapy in locally advanced esophageal cancer. Med Oncol. 2019;36:1–7.

    Article  Google Scholar 

  63. Xu Y-Y, Zhou X-L, Yu C-H, Wang W-W, Ji F-Z, He D-C, et al. Association of sarcopenia with toxicity and survival in postoperative recurrent esophageal squamous cell carcinoma patients receiving chemoradiotherapy. Front Oncol. 2021;11:655071.

  64. Panje CM, Höng L, Hayoz S, Baracos VE, Herrmann E, Garcia Schüler H, et al. Skeletal muscle mass correlates with increased toxicity during neoadjuvant radiochemotherapy in locally advanced esophageal cancer: a SAKK 75/08 substudy. Radiat Oncol. 2019;14:1–7.

    Article  Google Scholar 

  65. Murimwa GZ, Venkat PS, Jin W, Leuthold S, Latifi K, Almhanna K, Pimiento JM, Fontaine J-P, Hoffe SE, Frakes JM. Impact of sarcopenia on outcomes of locally advanced esophageal cancer patients treated with neoadjuvant chemoradiation followed by surgery. J Gastrointest Oncol. 2017;8:808–15.

    Article  PubMed  PubMed Central  Google Scholar 

  66. Tan BHL, Brammer K, Randhawa N, Welch NT, Parsons SL, James EJ, Catton JA. Sarcopenia is associated with toxicity in patients undergoing neo-adjuvant chemotherapy for oesophago-gastric cancer. Eur J Surg Oncol (EJSO). 2015;41:333–8.

    Article  CAS  PubMed  Google Scholar 

  67. Anandavadivelan P, Brismar TB, Nilsson M, Johar AM, Martin L. Sarcopenic obesity: a probable risk factor for dose limiting toxicity during neo-adjuvant chemotherapy in oesophageal cancer patients. Clin Nutr. 2016;35:724–30.

    Article  CAS  PubMed  Google Scholar 

  68. De Mello RA, Koch C, Reitz C, Schreckenbach T, Eichler K, Filmann N, et al. Sarcopenia as a prognostic factor for survival in patients with locally advanced gastroesophageal adenocarcinoma. Plos One. 2019;14:e0223613.

  69. Mallet R, Modzelewski R, Lequesne J, Mihailescu S, Decazes P, Auvray H, et al. Prognostic value of sarcopenia in patients treated by radiochemotherapy for locally advanced oesophageal cancer. Radiat Oncol. 2020;15:1–9.

    Article  Google Scholar 

  70. McSweeney DM, Raby S, Radhakrishna G, Weaver J, Green A, Bromiley PA, van Herk M, McWilliam A. Low muscle mass measured at T12 is a prognostic biomarker in unresectable oesophageal cancers receiving chemoradiotherapy. Radiother Oncol. 2023;186: 109764.

    Article  CAS  PubMed  Google Scholar 

  71. Huang C-H, Lue K-H, Hsieh T-C, Liu S-H, Wang T-F, Peng T-C. Association between sarcopenia and clinical outcomes in patients with esophageal cancer under neoadjuvant therapy. Anticancer Res. 2020;40:1175–81.

    Article  PubMed  Google Scholar 

  72. Nishi S, Miki Y, Imai T, Nambara M, Miyamoto H, Tamura T, et al. The evaluation of sarcopenia before neoadjuvant chemotherapy is important for predicting postoperative pneumonia in patients with esophageal cancer. Dig Surg. 2023;40:153–60.

    Article  CAS  PubMed  Google Scholar 

  73. Yang L, Francois F, Pei Z. Molecular pathways: pathogenesis and clinical implications of microbiome alteration in esophagitis and Barrett esophagus. Clin Cancer Res. 2012;18:2138–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Liu K, Ji S, Xu Y, Diao Q, Shao C, Luo J, et al. Safety, feasibility, and effect of an enhanced nutritional support pathway including extended preoperative and home enteral nutrition in patients undergoing enhanced recovery after esophagectomy: a pilot randomized clinical trial. Dis Esophagus. 2020;33:doz030.

  75. Reisinger KW, Bosmans JWAM, Uittenbogaart M, Alsoumali A, Poeze M, Sosef MN, Derikx JPM. Loss of skeletal muscle mass during neoadjuvant chemoradiotherapy predicts postoperative mortality in esophageal cancer surgery. Ann Surg Oncol. 2015;22:4445–52.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Nara K, Yamamoto T, Sato Y, Yagi K, Kawasaki K, Toriumi T, Takada T, Seto Y, Suzuki H. Low pretherapy skeletal muscle mass index is associated with an increased risk of febrile neutropenia in patients with esophageal cancer receiving docetaxel + cisplatin + 5-fluorouracil (DCF) therapy. Support Care Cancer. 2023;31:150.

    Article  PubMed  PubMed Central  Google Scholar 

  77. Harada T, Tsuji T, Ueno J, Hijikata N, Ishikawa A, Kotani D, Kojima T, Fujita T. 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: 101580.

    Article  CAS  PubMed  Google Scholar 

  78. Meza-Valderrama D, Marco E, Dávalos-Yerovi V, Muns MD, Tejero-Sánchez M, Duarte E, et al. Sarcopenia, malnutrition, and cachexia: adapting definitions and terminology of nutritional disorders in older people with cancer. Nutrients. 2021;13:761.

    Article  PubMed  PubMed Central  Google Scholar 

  79. Bossi P, Delrio P, Mascheroni A, Zanetti M. The spectrum of malnutrition/cachexia/sarcopenia in oncology according to different cancer types and settings: a narrative review. Nutrients. 2021;13:1980.

    Article  PubMed  PubMed Central  Google Scholar 

  80. Sieber CC. Malnutrition and sarcopenia. Aging Clin Exp Res. 2019;31:793–8.

    Article  PubMed  Google Scholar 

  81. Chang YL, Tsai YF, Hsu CL, Chao YK, Hsu CC, Lin KC. The effectiveness of a nurse-led exercise and health education informatics program on exercise capacity and quality of life among cancer survivors after esophagectomy: a randomized controlled trial. Int J Nurs Stud. 2020;101: 103418.

    Article  PubMed  Google Scholar 

  82. Pan L, Xie W, Fu X, Lu W, Jin H, Lai J, Zhang A, Yu Y, Li Y, Xiao W. Inflammation and sarcopenia: a focus on circulating inflammatory cytokines. Exp Gerontol. 2021;154: 111544.

    Article  CAS  PubMed  Google Scholar 

  83. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature. 2008;454:436–44.

    Article  CAS  PubMed  Google Scholar 

  84. Jimenez-Gutierrez GE, Martínez-Gómez LE, Martínez-Armenta C, Pineda C, Martínez-Nava GA, Lopez-Reyes A. Molecular mechanisms of inflammation in sarcopenia: diagnosis and therapeutic update. Cells. 2022;11:2359.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Sharma T, Gupta A, Chauhan R, Bhat AA, Nisar S, Hashem S, Akhtar S, Ahmad A, Haris M, Singh M, Uddin S. Cross-talk between the microbiome and chronic inflammation in esophageal cancer: potential driver of oncogenesis. Cancer Metastasis Rev. 2022;41:281–99.

    Article  PubMed  PubMed Central  Google Scholar 

  86. Davis MP, Panikkar R. Sarcopenia associated with chemotherapy and targeted agents for cancer therapy. Ann Palliative Med. 2019;8:86–101.

    Article  Google Scholar 

  87. Onishi S, Tajika M, Tanaka T, Yamada K, Kamiya T, Abe T, et al. Effect of body composition change during neoadjuvant chemotherapy for esophageal squamous cell carcinoma. J Clin Med. 2022;11:508.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Jang MK, Park C, Hong S, Li H, Rhee E, Doorenbos AZ. Skeletal muscle mass change during chemotherapy: a systematic review and meta-analysis. Anticancer Res. 2020;40:2409–18.

    Article  CAS  PubMed  Google Scholar 

  89. Bozzetti F. Chemotherapy-induced sarcopenia. Curr Treat Options Oncol. 2020;21:1–18.

    Article  Google Scholar 

  90. Gumucio JP, Mendias CL. Atrogin-1, MuRF-1, and sarcopenia. Endocrine. 2012;43:12–21.

    Article  PubMed  PubMed Central  Google Scholar 

  91. Schiaffino S, Dyar KA, Ciciliot S, Blaauw B, Sandri M. Mechanisms regulating skeletal muscle growth and atrophy. FEBS J. 2013;280:4294–314.

    Article  CAS  PubMed  Google Scholar 

  92. Sakai H, Asami M, Naito H, Kitora S, Suzuki Y, Miyauchi Y, Tachinooka R, Yoshida S, Kon R, Ikarashi N, et al. Exogenous insulin-like growth factor 1 attenuates cisplatin-induced muscle atrophy in mice. J Cachexia Sarcopenia Muscle. 2021;12:1570–81.

    Article  PubMed  PubMed Central  Google Scholar 

  93. Buono R, Longo VD. Starvation, stress resistance, and cancer. Trends Endocrinol Metab. 2018;29:271–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Boshier PR, Klevebro F, Jenq W, Puccetti F, Muthuswamy K, Hanna GB, et al. Long-term variation in skeletal muscle and adiposity in patients undergoing esophagectomy. Dis Esophagus. 2021;34:doab016.

  95. Kurita D, Oguma J, Ishiyama K, Hirano Y, Kanamori J, Daiko H. Handgrip strength predicts postoperative pneumonia after thoracoscopic–laparoscopic esophagectomy for patients with esophageal cancer. Ann Surg Oncol. 2020;27:3173–81.

    Article  PubMed  Google Scholar 

  96. Kurita D, Utsunomiya D, Kubo K, Fujii Y, Kanematsu K, Ishiyama K, Oguma J, Daiko H. Handgrip strength predicts early postoperative dysphagia after thoracoscopic-laparoscopic esophagectomy in male patients with esophageal cancer. Esophagus. 2022;19:586–95.

    Article  PubMed  Google Scholar 

  97. Kurita D, Sakurai T, Utsunomiya D, Kubo K, Fujii Y, Kanematsu K, Ishiyama K, Oguma J, Daiko H. Predictive ability of the five-time chair stand test for postoperative pneumonia after minimally invasive esophagectomy for esophageal cancer. Ann Surg Oncol. 2022;29:7462–70.

    Article  PubMed  Google Scholar 

  98. Zhou MJ, Tseng L, Guo X, Jin Z, Bentley-Hibbert S, Shen S, Araujo JL, Spinelli CF, Altorki NK, Sonett JR, et al. Low subcutaneous adiposity and mortality in esophageal cancer. Cancer Epidemiol Biomark Prev. 2021;30:114–22.

    Article  Google Scholar 

  99. Zheng C, Wang E, Li J-S, Xie K, Luo C, Ge Q-Y, et al. Serum creatinine/cystatin C ratio as a screening tool for sarcopenia and prognostic indicator for patients with esophageal cancer. BMC Geriatr. 2022;22:207.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Jung CY, Kim HW, Han SH, Yoo TH, Kang SW, Park JT. Creatinine-cystatin C ratio and mortality in cancer patients: a retrospective cohort study. J Cachexia Sarcopenia Muscle. 2022;13:2064–72.

    Article  PubMed  PubMed Central  Google Scholar 

  101. Tang T, Xie L, Hu S, Tan L, Lei X, Luo X, Yang L, Yang M. Serum creatinine and cystatin C-based diagnostic indices for sarcopenia in advanced non-small cell lung cancer. J Cachexia Sarcopenia Muscle. 2022;13:1800–10.

    Article  PubMed  PubMed Central  Google Scholar 

  102. Sun J, Yang H, Cai W, Zheng J, Shen N, Yang X, Pan B, Zhang W, Chen X, Shen X. Serum creatinine/cystatin C ratio as a surrogate marker for sarcopenia in patients with gastric cancer. BMC Gastroenterol. 2022;22:26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Gao S, Xie H, Wei L, Liu M, Liang Y, Wang Q, Tang S, Gan J. Serum creatinine/cystatin C ratio as a prognostic indicator for patients with colorectal cancer. Front Oncol. 2023;13:1155520.

    Article  PubMed  PubMed Central  Google Scholar 

  104. Dociak-Salazar E, Barrueto-Deza JL, Urrunaga-Pastor D, Runzer-Colmenares FM, Parodi JF. Gait speed as a predictor of mortality in older men with cancer: a longitudinal study in Peru. Heliyon. 2022;8: e08862.

    Article  PubMed  PubMed Central  Google Scholar 

  105. Hantel A, DuMontier C, Odejide OO, Luskin MR, Sperling AS, Hshieh T, Chen R, Soiffer R, Driver JA, Abel GA. Gait speed, survival, and recommended treatment intensity in older adults with blood cancer requiring treatment. Cancer. 2021;127:875–83.

    Article  PubMed  Google Scholar 

  106. Kondo S, Inoue T, Yoshida T, Saito T, Inoue S, Nishino T, Goto M, Sato N, Ono R, Tangoku A, Katoh S. Impact of preoperative 6-minute walk distance on long-term prognosis after esophagectomy in patients with esophageal cancer. Esophagus. 2022;19:95–104.

    Article  PubMed  Google Scholar 

  107. Chandoo A, Chi CH, Ji W, Huang Y, Chen XD, Zhang WT, Wu RS, Shen X. Gait speed predicts post-operative medical complications in elderly gastric cancer patients undergoing gastrectomy. ANZ J Surg. 2018;88:723–6.

    Article  PubMed  Google Scholar 

  108. Inoue T, Ito S, Kanda M, Niwa Y, Nagaya M, Nishida Y, et al. Preoperative six-minute walk distance as a predictor of postoperative complication in patients with esophageal cancer. Dis Esophagus. 2020;33:doz050.

  109. Wu SE, Chen WL. Calf circumference refines sarcopenia in correlating with mortality risk. Age Ageing. 2022;51:afab239.

  110. Sousa IM, Bielemann RM, Gonzalez MC, da Rocha IMG, Barbalho ER, de Carvalho ALM, Dantas MAM, de Medeiros GOC, Silva FM, Fayh APT. Low calf circumference is an independent predictor of mortality in cancer patients: a prospective cohort study. Nutrition. 2020;79–80: 110816.

    Article  PubMed  Google Scholar 

  111. Real GG, Frühauf IR, Sedrez JHK, Dall’Aqua EJF, Gonzalez MC. Calf circumference: a marker of muscle mass as a predictor of hospital readmission. JPEN J Parenter Enteral Nutr. 2018;42:1272–9.

    Article  CAS  PubMed  Google Scholar 

  112. Srinivasaraghavan N, Venketeswaran MV, Balakrishnan K, Ramasamy T, Ramakrishnan A, Agarwal A, Krishnamurthy A. Comparison of nutrition screening tools and calf circumference in estimating the preoperative prevalence of malnutrition among patients with aerodigestive tract cancers-a prospective observational cohort study. Support Care Cancer. 2022;30:6603–12.

    Article  PubMed  Google Scholar 

  113. Zhang XY, Zhang XL, Zhu YX, Tao J, Zhang Z, Zhang Y, Wang YY, Ke YY, Ren CX, Xu J, Zhong Y. Low calf circumference predicts nutritional risks in hospitalized patients aged more than 80 years. Biomed Environ Sci. 2019;32:571–7.

    PubMed  Google Scholar 

  114. Halle-Smith JM, Siddaiah-Subramanya M, Ghoneim A, Almonib A, Tan BHL. Influence of body composition measures on chyle leak after oesophagectomy. J Thorac Dis. 2022;14:877–83.

    Article  PubMed  PubMed Central  Google Scholar 

  115. Qiu J, Yang J, Yu Y, Wang Z, Lin H, Ke D, Zheng H, Li J, Yao Q. Prognostic value of pre-therapeutic nutritional risk factors in elderly patients with locally advanced esophageal squamous cell carcinoma receiving definitive chemoradiotherapy or radiotherapy. BMC Cancer. 2023;23:597.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Liu J, Hu G, Zhai C, Wang J, Xu W, Xie J, Zhu W, Jiang P, Liu D. Predictive value of nutritional indicators with regard to the survival outcomes in patients with metastatic esophageal squamous cell carcinoma treated with camrelizumab. Oncol Lett. 2023;25:198.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Townsend AN, Denton A, Gohel N, Lozano J. Rodriguez de la Vega P, Castro G, Seetharamaiah R: An association between comorbidities and postsurgical complications in adults who underwent esophagectomy. Cureus. 2023;15.

    PubMed  PubMed Central  Google Scholar 

  118. Sugimura K, Miyata H, Kanemura T, Takeoka T, Shinnno N, Yamamoto K, Omori T, Motoori M, Ohue M, Yano M. Impact of preoperative skeletal muscle mass and physical performance on short-term and long-term postoperative outcomes in patients with esophageal cancer after esophagectomy. Ann Gastroenterol Surg. 2022;6:623–32.

    Article  PubMed  PubMed Central  Google Scholar 

  119. Pascual-Fernández J, Fernández-Montero A, Córdova-Martínez A, Pastor D, Martínez-Rodríguez A, Roche E. Sarcopenia: molecular pathways and potential targets for intervention. Int J Mol Sci. 2020;21:8844.

    Article  PubMed  PubMed Central  Google Scholar 

  120. Liu HW, Chang SJ. Moderate exercise suppresses NF-κB signaling and activates the SIRT1-AMPK-PGC1α axis to attenuate muscle loss in diabetic db/db mice. Front Physiol. 2018;9:636.

    Article  PubMed  PubMed Central  Google Scholar 

  121. Ziegler AK, Jensen SM, Schjerling P, Mackey AL, Andersen JL, Kjaer M. The effect of resistance exercise upon age-related systemic and local skeletal muscle inflammation. Exp Gerontol. 2019;121:19–32.

    Article  CAS  PubMed  Google Scholar 

  122. Lu L, Mao L, Feng Y, Ainsworth BE, Liu Y, Chen N. Effects of different exercise training modes on muscle strength and physical performance in older people with sarcopenia: a systematic review and meta-analysis. BMC Geriatr. 2021;21:708.

    Article  PubMed  PubMed Central  Google Scholar 

  123. Niihara M, Tsubosa Y, Yamashita A, Mori K, Tsumaki H, Onozawa Y, Fukuda H. Supplemental enteral tube feeding nutrition after hospital discharge of esophageal cancer patients who have undergone esophagectomy. Esophagus. 2021;18:504–12.

    Article  PubMed  PubMed Central  Google Scholar 

  124. Steenhagen E, van Vulpen JK, van Hillegersberg R, May AM, Siersema PD. Nutrition in peri-operative esophageal cancer management. Expert Rev Gastroenterol Hepatol. 2017;11:663–72.

    Article  CAS  PubMed  Google Scholar 

  125. Chen J, Luo A-L, Yang L, Wang W, Zhou X, Yang M. Nutrition management by a multidisciplinary team for prevention of nutritional deficits and morbidity following esophagectomy. Brazil J Med Biol Res. 2023;56:e12421.

  126. Davies SJ, West MA, Rahman SA, Underwood TJ, Marino LV. Oesophageal cancer: the effect of early nutrition support on clinical outcomes. Clin Nutrition ESPEN. 2021;42:117–23.

    Article  CAS  Google Scholar 

  127. Mayeuf-Louchart A, Staels B, Duez H. Skeletal muscle functions around the clock. Diabetes Obes Metab. 2015;17(Suppl 1):39–46.

    Article  CAS  PubMed  Google Scholar 

  128. Riley LA, Esser KA. The role of the molecular clock in skeletal muscle and what it is teaching us about muscle-bone crosstalk. Curr Osteoporos Rep. 2017;15:222–30.

    Article  PubMed  PubMed Central  Google Scholar 

  129. Vitale J, Bonato M, La Torre A, Banfi G. The role of the molecular clock in promoting skeletal muscle growth and protecting against sarcopenia. Int J Mol Sci. 2019;20:4318.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Hirani V, Cumming RG, Naganathan V, Blyth F, Le Couteur DG, Hsu B, Handelsman DJ, Waite LM, Seibel MJ. Longitudinal associations between vitamin D metabolites and sarcopenia in older Australian men: the Concord Health and Aging in Men Project. J Gerontol A Biol Sci Med Sci. 2017;73:131–8.

    Article  PubMed  Google Scholar 

  131. Bian A, Ma Y, Zhou X, Guo Y, Wang W, Zhang Y, et al. Association between sarcopenia and levels of growth hormone and insulin-like growth factor-1 in the elderly. BMC Musculoskelet Disord. 2020;21:1–9.

    Article  Google Scholar 

  132. Chen F, Xu S, Wang Y, Chen F, Cao L, Liu T, Huang T, Wei Q, Ma G, Zhao Y, Wang D. Risk factors for sarcopenia in the elderly with type 2 diabetes mellitus and the effect of metformin. J Diabetes Res. 2020;2020:3950404.

    Article  PubMed  PubMed Central  Google Scholar 

  133. Lin MH, Chiu SY, Chang PH, Lai YL, Chen PC, Ho WC. Hyperlipidemia and statins use for the risk of new diagnosed sarcopenia in patients with chronic kidney: a population-based study. Int J Environ Res Public Health. 2020;17:1494.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Scott D, Blizzard L, Fell J, Giles G, Jones G. Associations between dietary nutrient intake and muscle mass and strength in community-dwelling older adults: the Tasmanian Older Adult Cohort Study. J Am Geriatr Soc. 2010;58:2129–34.

    Article  PubMed  Google Scholar 

  135. Kang D, Park K, Kim D. Study of therapeutic effects of losartan for sarcopenia based on the F344xBN rat aging model. In Vivo. 2022;36:2740–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Burks TN, Andres-Mateos E, Marx R, Mejias R, Van Erp C, Simmers JL, et al. Losartan restores skeletal muscle remodeling and protects against disuse atrophy in sarcopenia. Sci Transl Med. 2011;3:82ra37.

  137. Williams GR, Rier HN, McDonald A, Shachar SS. Sarcopenia & aging in cancer. J Geriatric Oncol. 2019;10:374–7.

    Article  Google Scholar 

  138. Deng HY, Hou L, Zha P. Sarcopenia: an unneglectable nutritional status in oncological esophagectomy. Dis Esophagus. 2019;32:doy108.

Download references

Acknowledgements

Not applicable.

Funding

This work was supported by the Natural Science Foundation General Program of Hunan Province (2022JJ40830), Natural Science Foundation General Program of Changsha City (kq2014290), and National Multidisciplinary Cooperative Diagnosis and Treatment Capacity Building Project for Major Diseases (Lung Cancer, grant number: z027002).

Author information

Authors and Affiliations

  1. Department of Pharmacy, Xiangya Hospital, Central South University, Changsha, 410008, China

    Shenglan Li, Kaiqiang Xie & Mimi Tang

  2. National Clinical Research Center for Geriatric Disorders, Xiangya Hospital, Central South University, Changsha, Hunan, China

    Shenglan Li, Kaiqiang Xie, Xiaoxiong Xiao, Mimi Tang & Dai Li

  3. The Hunan Institute of Pharmacy Practice and Clinical Research, Changsha, 410008, China

    Shenglan Li, Kaiqiang Xie & Mimi Tang

  4. Institute of Hospital Pharmacy, Central South University, Changsha, 410008, China

    Shenglan Li, Kaiqiang Xie & Mimi Tang

  5. Department of Thoracic Surgery, Xiangya Hospital, Central South University, Changsha, Hunan, China

    Xiaoxiong Xiao

  6. Xiangya Lung Cancer Center, Xiangya Hospital, Central South University, Changsha, Hunan, China

    Xiaoxiong Xiao

  7. Phase I Clinical Trial Center, Xiangya Hospital, Central South University, Changsha, 410008, China

    Pingsheng Xu & Dai Li

Authors
  1. Shenglan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kaiqiang Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiaoxiong Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pingsheng Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mimi Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dai Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

TM developed ideas, conceptualized the article and contributed significantly to the revision of the first draft, LS conducted the literature search and conceptualized the article and was a major contributor to the writing and revision of the manuscript. XK contributed significantly to the writing and revision of the manuscript. LD, XX and XP conducted the literature search and data collection. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Mimi Tang or Dai Li.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Additional file 1.

 This supplement describes the various parts of the manuscript in detail according to the major sections and topics required by the PRISMA guidelines.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, S., Xie, K., Xiao, X. et al. Correlation between sarcopenia and esophageal cancer: a narrative review. World J Surg Onc 22, 27 (2024). https://doi.org/10.1186/s12957-024-03304-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12957-024-03304-w

Keywords

World Journal of Surgical Oncology

ISSN: 1477-7819

Contact us