Sarcopenia: a new predictor of postoperative complications for elderly gastric cancer patients who underwent radical gastrectomy

doi:10.1016/j.jss.2016.12.014

Journal of Surgical Research

Volume 211, 1 May 2017, Pages 137-146

https://doi.org/10.1016/j.jss.2016.12.014 Get rights and content

Abstract

Background

A geriatric assessment is needed to identify high-risk elderly patients with gastric cancer. However, the current geriatric assessment has been considered to be either time-consuming or subjective. The present study aimed to investigate the predictive effect of sarcopenia on the postoperative complications for elderly patients who underwent radical gastrectomy.

Materials and methods

We conducted a prospective study of patients who underwent radical gastrectomy from August 2014 to December 2015. Computed tomography–assessed lumbar skeletal muscle, handgrip strength, and gait speed were measured to define sarcopenia.

Results

Sarcopenia was present in 69 of 240 patients (28.8%) and was associated with lower body mass index, lower serum albumin, lower hemoglobin, and higher nutritional risk screening 2002 scores. Postoperative complications significantly increased in the sarcopenic patients (49.3% versus 24.6%, P < 0.001), compared with nonsarcopenic patients. The multivariate analysis demonstrated that sarcopenia (odds ratio: 2.959, 95% CI: 1.629-5.373, P < 0.001) and the Charlson comorbidity index ≥2 (odds ratio: 3.357, 95% CI: 1.144-9.848, P = 0.027) were independent risk factors for postoperative complications.

Conclusions

Sarcopenia, presented as a new geriatric assessment factor, was a strong and independent risk factor for postoperative complications of elderly patients with gastric cancer.

Introduction

Gastric cancer is the fourth most common malignancy and the third leading cause of death worldwide.¹ As the world population ages and lifespans increase, the number of elderly patients with gastric cancer has been increasing significantly.² Surgical resection remains the most effective therapy for potentially curable gastric cancer.³ However, surgeons sometimes hesitate to perform surgery on elderly patients due to the high frequency of complications and poor survival rates associated with aging.4, 5 Recently, some reviews confirmed that chronological age alone was not an independent predictor of postoperative complications and highlighted the importance of geriatric assessment to identify high-risk patients.6, 7

The American Geriatrics Society published a practice guideline for optimal preoperative assessment of geriatric surgical patients, including cognitive/behavioral disorders, cardiac evaluation, pulmonary evaluation, functional/performance status, frailty, nutritional status, medication management, patient counseling, and preoperative testing.⁸ However, this assessment seems time-consuming and may be infeasible in a busy surgical practice.⁶ Specific items such as deficiencies in activities of daily living, depression, decreased cognition, and frailty were believed to be the most robust predictors of postoperative complications among the surgical oncology population.⁶ Regrettably, these items were considered to be subjective and relatively cumbersome.9, 10

Sarcopenia, is an age-related syndrome, characterized by progressive and generalized loss of skeletal muscle mass and strength.¹¹ In recent years, sarcopenia has been gradually recognized to be associated with a negative prognosis after colorectal,¹² pancreatic,¹³ hepatic,¹⁴ and gastric surgery.¹⁵ However, most of these studies defined sarcopenia as reduced skeletal muscle mass alone, ignoring the importance of skeletal muscle function.¹⁶ Moreover, patients of all ages were included in these studies. It seems more meaningful to explore the predictive effect of sarcopenia among elderly patients undergoing oncological surgery, as sarcopenia is an age-related syndrome.

In this prospective study, we assessed both skeletal muscle mass and function to define sarcopenia, aiming to investigate the predictive effect of sarcopenia on the postoperative complications for elderly patients who underwent radical gastrectomy.

Section snippets

Patients

From August 2014 to December 2015, all patients who underwent gastric cancer surgery at our department were included in this prospective study. The inclusion criteria included patients who were aged ≥65 y, had American society of anesthesiology (ASA) grade ≤ III, planned to receive elective radical gastrectomy for gastric cancer, and had preoperative abdominal computed tomography (CT) scans available for review. Exclusion criteria included those patients with a physical deformity, who were

Clinicopathologic characteristics

From August 2014 to December 2015, a total of 240 patients met the inclusion criteria and were included in this study. The patients’ clinicopathologic characteristics are summarized in Table 1. Based on the diagnostic criteria for sarcopenia, 69 patients (28.8%) were diagnosed with sarcopenia and the remaining 171 patients (71.3%) with no sarcopenia. There were no significant differences in gender, ASA grade, Charlson comorbidity index, and previous abdominal surgery between sarcopenic and

Discussion

Although the advances in surgical techniques and perioperative treatment have reduced postoperative complications, these complications remain substantial in elderly patients due to the increasing prevalence of frailty, comorbidities, and the decline of functional reserve associated with aging.5, 24 Therefore, a preoperative assessment for the elderly surgical oncology population is needed to identify high-risk patients. To date, commonly used geriatric assessment factors are considered to be

Conclusions

The present study demonstrates that sarcopenia, which can reflect both physical function and nutritional status of elderly patients, was a strong and independent risk factor for postoperative complications of these patients with gastric cancer. This objective, convenient, relatively comprehensive, and preoperatively modifiable predictive factor should be considered as part of comprehensive geriatric assessment in the future.

Acknowledgment

This work was supported by the foundation of the Health Department of Zhejiang Province (2016139771), and the Shanghai Science and Technology Committee (16411954200). Chen-Ping Huang, Department of Public Health, Wenzhou Medical University, contributed to the optimization of the statistical methods of this study.

Authors' contributions: X.X.C. and C.L.Z. contributed to the study design. F.M.Z., F.Y.Z., and X.L.C. collected the data. C.J.Z. and F.M.Z. analyzed and interpreted the data. C.J.Z. and

References (35)

C.J. Zhou et al.
Feasibility of radical gastrectomy for elderly patients with gastric cancer
Eur J Surg Oncol
(2016)
M.A. Feng et al.
Geriatric assessment in surgical oncology: a systematic review
J Surg Res
(2015)
S. Mohanty et al.
Optimal perioperative management of the geriatric patient: a best practices guideline from the American College of Surgeons NSQIP and the American Geriatrics Society
J Am Coll Surgeons
(2016)
P. Peng et al.
Impact of sarcopenia on outcomes following resection of pancreatic adenocarcinoma
J Gastrointest Surg
(2012)
M.E. Charlson et al.
A new method of classifying prognostic comorbidity in longitudinal studies: development and validation
J Chronic Dis
(1987)
J. Yu et al.
Risk factors for postoperative fatigue after gastrointestinal surgery
J Surg Res
(2015)
L.K. Chen et al.
Sarcopenia in Asia: consensus report of the Asian working group for sarcopenia
J Am Med Directors Assoc
(2014)
S.M. Phillips
Nutritional supplements in support of resistance exercise to counter age-related sarcopenia
Adv Nutr (Bethesda, Md.)
(2015)
J.C. Hall
Nutritional assessment of surgery patients
J Am Coll Surg
(2006)
L.A. Torre et al.
Global cancer statistics, 2012
CA Cancer J Clin
(2015)

T. Marugame et al.

Comparison of time trends in stomach cancer incidence (1973-1997) in East Asia, Europe and USA, from cancer incidence in five continents Vol. Iv-viii

Jpn J Clin Oncol

(2007)

S.G. Thrumurthy et al.

The diagnosis and management of gastric cancer

BMJ

(2013)

H. Takeshita et al.

Surgical outcomes of gastrectomy for elderly patients with gastric cancer

World J Surg

(2013)

B. Korc-Grodzicki et al.

Surgical considerations in older adults with cancer

J Clin Oncol

(2014)

Y.H. Hsu et al.

Association of cognitive impairment, depressive symptoms and sarcopenia among healthy older men in the veterans retirement community in southern Taiwan: a cross-sectional study

Geriatr Gerontol Int

(2014)

D. Wagner et al.

Clinical and morphometric parameters of frailty for prediction of mortality following hepatopancreaticobiliary surgery in the elderly

Br J Surg

(2016)

A.J. Cruz-Jentoft et al.

Sarcopenia: European consensus on definition and diagnosis: report of the European working group on sarcopenia in older people

Age Ageing

(2010)

Cited by (57)

Sarcopenia measured by tomography as a predictor of morbidity and mortality in thoracic surgery, a cohort retrospective
2024, Revista Espanola de Anestesiologia y Reanimacion
La sarcopenia se ha identificado como factor de riesgo para eventos adversos perioperatorios. Varios estudios han demostrado que la valoración tomográfica de la masa muscular puede ser un indicador apropiado de sarcopenia asociado a morbimortalidad. El objetivo del estudio fue determinar la asociación entre el área de los músculos pectorales y erectores de la espina ajustados por talla de los músculos pectorales y de los músculos erectores de la espina (AaMP y AaMEE) y morbimortalidad perioperatoria en cirugía torácica.
Estudio de cohortes retrospectivo. Se realizó medición de áreas musculares mediante tomografía. Los desenlaces fueron mortalidad a 30 días y morbilidad posoperatoria. Se evaluó la capacidad discriminativa de las áreas musculares con un análisis de curvas receiver operating characteristic (ROC) y se empleó el índice de Youden para establecer un punto de corte. Se determinó el riesgo de morbimortalidad crudo y ajustado por potenciales confusores.
Se incluyeron 509 pacientes llevados a cirugía torácica. La incidencia de mortalidad a 30 días fue del 7,3%. Se encontró una asociación entre las áreas musculares y mortalidad a 30 días y neumonía, con una capacidad discriminativa adecuada para mortalidad (área bajo la curva [AUC] 0,68 para AaMP y 0,67 para AaMEE). Se identificó un AaMP menor a 10 y AaMEE menor a 8,5 cm²/m² como factor de riesgo para mortalidad a 30 días con un Odds Ratio (OR) ajustado de 2,34 (intervalo de confianza [IC] 95% 1,03 – 5,15) y 2,22 (IC 95% 1,10 – 6,04), respectivamente.
La sarcopenia, definida como una baja área muscular en los músculos pectorales y erectores de la espina, se asocia a mayor morbimortalidad en los pacientes sometidos a cirugía torácica.
Sarcopenia has been identified as a risk factor for perioperative adverse events. Several studies have shown that tomographic assessment of muscle mass can be an appropriate indicator of sarcopenia associated with morbidity and mortality. The aim of the study was to determine the association between height-adjusted area of the pectoral and erector spinae muscles (haPMA and haESA) and perioperative morbidity and mortality in thoracic surgery.
Retrospective cohort study. Measurement of muscle areas was performed by tomography. The outcomes were 30-day mortality and postoperative morbidity. The discriminative capacity of the muscle areas was evaluated with an analysis of ROC curves and the Youden index was used to establish a cut-off point. The raw morbidity and mortality risk was determined and adjusted for potential confounders.
A total of 509 patients taken to thoracic surgery were included. The incidence of 30-day mortality was 7.3%. An association was found between muscle areas and 30-day mortality and pneumonia, with adequate discriminative power for mortality (AUC 0.68 for haPMA and 0.67 for haESA). An haPMA less than 10 and haESA less than 8.5 cm2/m2 were identified as a risk factor for 30-day mortality with an adjusted OR of 2.34 (95%CI 1.03 – 5.15) and 2.22 (95%CI 1.10 – 6.04) respectively.
Sarcopenia, defined as low muscle area in the pectoral and erector spinae muscles, is associated with increased morbidity and mortality in patients undergoing thoracic surgery.
Association between preoperative skeletal muscle mass depletion and poor relapse-free survival in patients with gastrointestinal stromal tumors after complete resection
2022, Nutrition
The aim of this study was to investigate the predictive effects of skeletal muscle mass (SMM) depletion on relapse risk in patients who had undergone complete surgical resection for primary resectable gastrointestinal stromal tumors (GISTs).
This retrospective study comprised 445 enrolled patients with primary resectable GISTs who had undergone surgical treatment between January 2013 and January 2021. The lumbar skeletal muscle index (SMI) was assessed using abdominal computed tomography images taken within 7 d preoperatively. Univariate and multivariate Cox regression analyses were performed to identify independent risk factors for nomogram construction. Predictive accuracy and discriminative ability were measured using the concordance index (C-index).
Three- and 5-y relapse-free survival (RFS) rates for patients in the low SMI group were significantly worse than those in the high SMI group (81.3 and 75.4% versus 92.3 and 91.6%, respectively; P < 0.001). In stratification analysis using modified National Institutes of Health criteria, high-risk patients with low SMI showed significantly shorter RFS (P = 0.001). Multivariate analysis indicated that tumor size, tumor location, mitotic rates, the platelet-to-lymphocyte ratio, the prognostic nutritional index, and SMM depletion were independent prognostic factors for RFS (P < 0.05). These six variables were selected for nomogram construction, which showed superior discrimination with a C-index of 0.82.
There was a significant association between preoperative SMM depletion and a high risk for relapse in patients who had undergone complete resection for primary resectable GISTs, especially in patients with high-risk GIST. Our simple, practical, novel nomogram intuitively predicted RFS in these patients.
Effects of Sarcopenia on Postoperative Outcomes in Patients Who Underwent Gastrectomy for Gastric Cancer
2022, Journal of Surgical Research
Citation Excerpt :
In addition to diagnosing sarcopenia, questions such as how it can be dealt with and how clinical outcomes can be improved also need to be addressed. In the present study, impairment in nutrition-related parameters in sarcopenic patients demonstrated a close relationship between sarcopenia and poor nutritional status.11 It may therefore be suggested that providing adequate preoperative energy-protein support may exert a positive effect on clinical outcomes.40
The relationship between sarcopenia and postoperative outcomes in patients with gastric cancer remains controversial. This study aimed to investigate the impact of sarcopenia on short-term outcomes after surgery for gastric cancer.
Patients who underwent surgical treatment for gastric cancer were evaluated in this prospective observational study. Muscle strength, muscle mass, and physical performance were measured before surgery. Diagnosis of sarcopenia was based on the revised European Working Group on Sarcopenia criteria. Postoperative 30-day outcomes, including complications, reoperation, readmission, and operative mortality, were recorded.
Sarcopenia was observed in 31 out of 146 patients (21.2%). The overall complication incidence was 31.5%. The postoperative complication rate was higher in the sarcopenic patients compared to the nonsarcopenic patients (54.8% versus 25.2%, P = 0.003). There was no statistically significant difference in terms of surgical complication rates (25.8% versus 14.8%, P = 0.239), although the sarcopenic group had a significantly higher systemic complication rate (38.7% versus 13%, P = 0.003). No statistically significant difference was observed in terms of major complications (3.2% versus 5.2%, P = 1.000). Muscle strength, muscle mass, and physical performance were not identified as independent factors when tested alone at adjusted multivariable analysis. Sarcopenia (Odds ratio: 2.73, 95% CI 1.02-7.52, P = 0.047) and severe sarcopenia (Odds ratio: 4.44, 95% CI 1.57-13.34, P = 0.006) were identified as independent prognostic factors for postoperative complications.
Sarcopenia was associated with postoperative complications after gastrectomy for gastric cancer. Severe sarcopenia may serve as a more robust prognostic indicator. The variation in the complication rates between sarcopenic and nonsarcopenic patients was mainly due to difference in systemic complications rather than surgical complications.
Evolving concepts on perioperative nutrition of sarcopenic cancer patients
2022, European Journal of Surgical Oncology
The recent recognition of the association of sarcopenia with an increased risk of complications after a surgical procedure calls for rethinking the proper approach of the perioperative care in cancer patients.
Sarcopenia is broadly considered in literature according to three different definitions: loss of muscle mass, loss of muscle mass plus reduced muscle function and myosteatosis.
The aim of this short review on this issue is to define the excess of risk by type of primary and of surgical procedure, depending on the definition of sarcopenia, to speculate on this association (casual versus causal) and to examine the current therapeutical approaches.
The analysis of the data shows that sarcopenia, defined as loss of muscle mass plus reduced muscle function, has the higher predictive power for the occurrence of postoperative complications than the two other definitions, and any definition of sarcopenia works better than the usual indexes or scores of surgical risk.
Our analysis supports the concept that: a) sarcopenia is frequently associated with inflammation, but inflammation cannot be considered the only or the absolute cause for sarcopenia, b) sarcopenia is not a simple marker of risk but can have a direct role in the increase of risk.
Data on perioperative care of sarcopenic cancer patients are scanty but a correct approach cannot rely on nutritional support alone but on a combined approach of optimized nutrition and exercise, hopefully associated with an anti-inflammatory treatment. This strategy should be applied proactively in keeping with the recent recommendations of the American Society of Clinical Oncology for the medical treatment of advanced cancer patients even if a clear demonstration of effectiveness is still lacking.
Sarcopenia among older patients with cancer: A scoping review of the literature
2022, Journal of Geriatric Oncology
Citation Excerpt :
Table 2 reveals the characteristics of eligible articles in this scoping review. Over 90% (n = 36) were published since 2016 [8,10,12–45]. Of the 39 included studies, 28.2% were conducted in Japan (n = 11) [8,13,21,23,25,28–30,34,35,44], 20.5% in China (n = 8) [18,33,36,38–41,45] and 10.3% in USA (n = 4) [31,32,46,47].
In the older patients with cancer, the combination of aging and cancer makes sarcopenia more likely to occur. However, previous studies paid less attention to the sarcopenia of older patients with cancer. To address these gaps, we conducted a scoped review of the prevalence, measurement, prognostic value, and clinical interventions of sarcopenia in this population.
A comprehensive search of PubMed, Cumulative Index to Nursing and Allied Health Literature (CINAHL), Web of Science, Embase, China National Knowledge Infrastructure (CNKI) and Wangfang electronic databases was conducted according to the Preferred Reporting Items for Systematic Reviews and Meta-Analysis Extension for Scoping Reviews. Two independent reviewers screened all abstracts and full-text studies for inclusion.
We identified 10,850 studies, and 39 met the inclusion criteria. Two reviewers extracted data on study characteristics, study design, measuring tools and main outcomes. This review included works from 11 countries. All studies were quantitative and most used a cross-sectional (n = 17) or retrospective (n = 16) design. The prevalence of sarcopenia in elderly cancer survivors ranged from 18.5% to 83%, and skeletal muscle mass index (SMI) by computed tomography (CT) scan at lumbar 3 (L3) was the most commonly used way to define sarcopenia. Meanwhile, pre-therapeutic sarcopenia was significantly related to postoperative complications, lower overall survival and impaired physical function.
This review emphasizes sarcopenia is highly prevalent in older patients with cancer, which leads to poor outcomes and urgently needs attention from nutritionists, surgeons, oncologists, psychologists and nurses.
Impact of preoperative sarcopenia on postoperative complications and prognosis of gastric cancer resection: A meta-analysis of cohort studies
2022, Archives of Gerontology and Geriatrics
Background The effect of preoperative sarcopenia on postoperative complications and prognosis in patients undergoing gastrectomy for gastric cancer has been controversial. The purpose of this study was to explore the effect of preoperative sarcopenia on postoperative complications and prognosis of patients with gastric cancer through meta-analysis method, providing new ideas for the prognosis study of patients undergoing gastrectomy for gastric cancer.
Methods From databases establishment to April 2021, we systematically searched PubMed, Embase, Web of Science, the Cochrane Library, China National Knowledge Infrastructure (CNKI), VIP, WanFang Data, and Chinese Biomedical Literature Database (CBM) to collect cohort studies on the effect of sarcopenia on postoperative complications or prognosis of gastric cancer. Based on the inclusion and exclusion criteria, two researchers independently screened the literature and extracted the data. The Newcastle-Ottawa Scale was used to evaluate the quality of the included studies and Revman 5.3 software was used for the meta-analysis.
Result A total of 20 studies (11 prospective cohort studies and 9 retrospective cohort studies) involving 7615 patients were finally included. Meta-analysis showed that: 1) preoperative sarcopenia significantly increased the risk of overall complications (risk ratio[RR] =2.89, 95% confidence interval[CI]: 1.86, 4.49; P < 0.000 01), serious complications (Clavien-Dindo grade ≥ III, RR = 3.01, 95% CI: 1.73, 5.23; P < 0.000 01), pneumonia (RR =2.64, 95% CI: 1.71, 4.09; P < 0.0001), and obstruction (RR = 3.96, 95% CI: 2.27, 6.90; P < 0.000 01), but did not increase the risk of postoperative delayed gastric emptying (RR = 1.44, 95% CI: 0.63, 3.25; P = 0.38), intra-abdominal infection (RR =2.09, 95% CI: 0.88, 5.00; P = 0.10), and anastomotic leakage (RR = 1.26, 95% CI: 0.69, 2.32; P = 0.45); 2) preoperative sarcopenia reduced the overall survival rate (HR = 1.71, 95% CI: 1.53, 1.91; P < 0.00001).
Conclusion Preoperative sarcopenia increased the risk of postoperative complications and reduced the overall survival rate of patients undergoing gastrectomy for gastric cancer. Therefore, for patients with gastric cancer, preoperative risk assessment and active intervention for sarcopenia are necessary to reduce the risk of postoperative complications and improve poor prognosis. Future studies should focus on the effect of preoperative sarcopenia on the quality of life after gastrectomy for gastric cancer.

View all citing articles on Scopus

¹: These authors contributed equally to this work.

View full text

GastrointestinalSarcopenia: a new predictor of postoperative complications for elderly gastric cancer patients who underwent radical gastrectomy

Abstract

Background

Materials and methods

Results

Conclusions

Introduction

Section snippets

Patients

Clinicopathologic characteristics

Discussion

Conclusions

Acknowledgment

Eur J Surg Oncol

J Surg Res

J Am Coll Surgeons

J Gastrointest Surg

J Chronic Dis

J Surg Res

J Am Med Directors Assoc

Adv Nutr (Bethesda, Md.)

J Am Coll Surg

Global cancer statistics, 2012

CA Cancer J Clin

Comparison of time trends in stomach cancer incidence (1973-1997) in East Asia, Europe and USA, from cancer incidence in five continents Vol. Iv-viii

Jpn J Clin Oncol

The diagnosis and management of gastric cancer

BMJ

Surgical outcomes of gastrectomy for elderly patients with gastric cancer

World J Surg

Surgical considerations in older adults with cancer

J Clin Oncol

Association of cognitive impairment, depressive symptoms and sarcopenia among healthy older men in the veterans retirement community in southern Taiwan: a cross-sectional study

Geriatr Gerontol Int

Clinical and morphometric parameters of frailty for prediction of mortality following hepatopancreaticobiliary surgery in the elderly

Br J Surg

Sarcopenia: European consensus on definition and diagnosis: report of the European working group on sarcopenia in older people

Age Ageing

Gastrointestinal
Sarcopenia: a new predictor of postoperative complications for elderly gastric cancer patients who underwent radical gastrectomy