Impact of sarcopenia on postoperative pulmonary complications after gastric cancer surgery: A retrospective cohort study

Background: Few studies have investigated the relationship between sarcopenia and postoperative pulmonary complications (PPCs) after gastric cancer surgery. This study aimed to explore the impact of sarcopenia on PPCs in patients who had undergone gastric cancer surgery.

Methods: We included patients who underwent a transabdominal radical gastrectomy between June 2016 and October 2020. Patients were divided into two groups according to the median prevalence rate of lumbar triplane skeletal muscle index (L3 SMI): sarcopenia group (≤37.5% percentile in male and female group) and non-sarcopenia group (>37.5% percentile in male and female group). Baseline characteristics, intraoperative and postoperative conditions, pulmonary complications, and overall complications were compared between the two groups. The primary outcome was the incidence of PPCs. The secondary outcomes were overall postoperative complications and length of stay (LOS).

Results: Among the 143 patients included, 50 had sarcopenia and 93 had not. Compared to the non-sarcopenia group, the sarcopenia group had a higher the incidence of PPCs (22.0% vs. 8.6%, P = 0.024). The incidence of overall postoperative complications in the sarcopenia group was higher than that in the non-sarcopenia group (36.00% vs. 20.43%, P = 0.043). There was no significant difference in the LOS between the two groups.

Conclusions: Our research indicates that sarcopenia, preoperative comorbidities, and longer duration of intraoperative oxygen saturation <95% were risk factors for PPCs. Sarcopenia is an independent risk factor for postoperative complications. Given that our results provided a correlation rather than causation, future prospective randomized trials are needed to confirm the relationship between sarcopenia and prognosis.

Introduction

Sarcopenia is a complex age-related syndrome characterized by progressive and generalized loss of skeletal muscle mass and function (1, 2), with the potential for physical disability, loss of independence, and adverse consequences, such as death (3, 4). The etiology of sarcopenia may be related to skeletal muscle disuse, endocrine changes, chronic wasting disease, systemic inflammatory responses, insulin resistance, and malnutrition (5, 6). Excessive inflammatory responses and chronic wasting disease largely contribute to sarcopenia, especially in patients with cancer (7). Thus, sarcopenia and cancer are causally related. Patients with gastric cancer usually have a certain degree of anorexia and underlying metabolic changes such as increased energy consumption, catabolism, and inflammation. These direct effects are exacerbated by the combined effects of chemotherapy and major gastrectomy, resulting in decreased nutrient intake. Decreased nutritional intake in patients with gastric cancer can further aggravate the occurrence and development of sarcopenia (8, 9).

Gastric cancer is the fifth most common cancer and third leading cause of cancer-related deaths worldwide (10). Studies have shown that sarcopenia is an independent factor for postoperative complications and overall survival in patients with gastric cancer (11). Studies have shown that sarcopenia is very common in older people, with a prevalence of 5%–13% in people aged 60–70 years and 11%–50% in those aged >80 years of age. Large differences in prevalence are related to differences in the measurements and cutoffs used to define sarcopenia (12). The prevalence of sarcopenia among community residents in China was 4.8% among women and 13.2% among men aged ≥70 years (13). The prevalence of sarcopenia in patients with cancer has significantly increased by approximately 35.7% (14). With further aggravation of population aging, the number of older patients with gastric cancer will gradually increase (15). Surgery remains the most important treatment for gastric cancer (16). However, the high incidence of postoperative complications and low survival rate in such patients have always been a concern for clinicians (17, 18). Postoperative complications have been shown to affect overall survival (19). Predicting the risk of postoperative complications and how to better intervene in order to reduce postoperative complications have become the focus of attention. Previous studies have shown that patients with sarcopenia have a higher risk of postoperative complications, longer length of stay (LOS), and higher hospital costs than patients without sarcopenia (20). Among the postoperative complications, anastomotic leakage and pulmonary complications have the greatest influence on postoperative mortality and prolonged LOS (21). Anastomotic leakage has decreased with improvements in surgical techniques. Pneumonia or lung-related complications are the most common postoperative complications in individuals under 80 years of age (22). Accurately predicting the risk of complications and actively preventing and doing everything possible to reduce the occurrence of postoperative pulmonary complications (PPCs) have become the focus of surgeons and anesthesiologists. However, few studies have investigated the relationship between sarcopenia and PPCs after gastric cancer surgery. In this study, we aimed to investigate the impact of sarcopenia on PPCs in patients undergoing gastric cancer surgery and to identify other risk factors for post-operative pneumonia.

Materials and methods

Study design and patients

This single-center, retrospective cohort study used data obtained from the discharge medical records of patients undergoing gastrointestinal surgery from June 2016 to October 2020 in the Department of Gastrointestinal Surgery, West China Hospital, Sichuan University, Chengdu, China. This study was approved by the Biomedical Research Ethics Committee of West China Hospital, Sichuan University, and was registered at www.chictr.org.cn (ChiCTR1900026578).

Inclusion and exclusion criteria

The inclusion criteria were as follows: age 18–75 years; American Society of Anesthesiologists (ASA) I–III, and plan to undergo transabdominal radical gastrectomy for clinical stage I-III gastric cancer. Patients were excluded if their medical records were incomplete or inaccurate, if they had missing abdominal computed tomography (CT), or if they had a history of radical gastric resection or preoperative chemotherapy. Proximal (PG), distal (DG), or total gastrectomy (TG) was performed by specialized surgeons, according to the Japanese Gastric Cancer Treatment Guidelines (23).

Data collection

For each patient, the data were collected by trained surgeons, radiologists, and anesthesiologists. The surgeons were trained by experienced surgeons until they were sufficiently skilled and precise in data collection (as judged by an experienced surgeon).

The basic information was as follows: patient sociodemographic characteristics, clinical characteristics, surgical procedures, and outcomes. The intraoperative parameters examined were as follows: the types of resection, anesthesia method, operation time (min), mechanical ventilation time (min), respiratory parameters (tidal volume [ml/kg], positive end expiratory pressure [PEEP], airway pressure, end-tidal carbon dioxide), circulation (systolic and diastolic blood pressure, heart rate, intraoperative vasoactive drug use), intraoperative pulse oximetry (SPO₂) < 95% duration, intraoperative infusion volume (colloid volume, crystalloid volume), urine volume, and medication data.

After surgery, we monitored: the time of removing the tracheal tube after surgery (min), days of hospitalization after surgery (days), hospitalization expenses (yuan), time of removing gastric tube after surgery (days), postoperative complications, and pulmonary complications within 15 days after surgery (24), postoperative destination, whether patient-controlled analgesia was used, postoperative pathological diagnosis, histological type, TNM stage, and readmission within 30 days of discharge.

For primary outcomes, we measured PPCs and for secondary outcome measures, we considered the severity classification of PPCs, other postoperative complications, and intra-abdominal infections.

Diagnosis of sarcopenia

Sarcopenia was defined as low muscle mass, strength, and/or physical performance. Previous studies have shown that lumbar triplane skeletal muscle index (L3 SMI) on CT is the gold standard for estimating muscle quality (25). After professional training, imaging physicians identified and measured the muscle area of the L3 plane and divided it by the height squared (m²) to obtain the skeletal muscle index of L3 SMI (cm²/m²) on the syngo Multimodality Workplace software (Siemens Medical Solutions, Forchheim, Germany).

Studies have shown that the median prevalence of sarcopenia in patients with gastric cancer is approximately 35.7% (14). Therefore, in this study, we used a median of 35.7% for grouping. In all the medical records collected,  ≤ 35.7% of both sexes were classified as the sarcopenia group and >35.7% as the non-sarcopenia group. A data collection flowchart is presented in Figure 1.

FIGURE 1

Figure 1. .

Complications definition

PPCs were defined as any of the following postoperative conditions within 15 days after operation: initial ventilation support for >48 h, re-intubation due to respiratory failure or pneumonia, respiratory infection, respiratory failure, bronchospasm, atelectasis, pleural effusion, pneumothorax, or aspiration pneumonia (26). The severity of PPCs was classified as 0–5, in which 0 indicates that PPCs have no symptoms or signals, 1–4 indicates gradual deterioration of complications, and 5 indicates death before discharge (27). A grade of at least 2 was defined as severe PPCs. Postoperative complications were defined as any deviation from the normal postoperative course and were graded according to the Clavien-Dindo classification (28).

Statistical analysis

The Shapiro–Wilk test was used to test the normality of continuous variables. The Student's t-test was used for quantitative data of normal and approximately normal distribution, and the mean±standard deviation was used for quantitative data of severely skewed distributions. For such distributions, the rank sum test was used and the data were expressed as median (25% quantile, 75% quantile). Categorical variables were analyzed using the chi-squared or Fisher's exact test, and classified variable data were expressed as numbers and percentages. Univariate logistic regression analysis was used for the univariate analysis. Variables with significant trends and known prognostic values, such as age, were selected as potential parameters in the univariate analysis. Forward stepwise variable selection was used to establish a multivariate logistic regression. All tests were bilateral (except for logistic regression analysis) and were considered statistically significant at P < 0.05. The IBM SPSS statistical software version 23.0 (SPSS Inc., Chicago, IL) was used for the statistical analysis.

Results

Comparison of baseline characteristics

A total of 143 patients met the inclusion criteria and were included in the study. The basic patient information is summarized in Tables 1, 2. They were divided into sarcopenia and non-sarcopenia groups according to the abdominal CT-guided L3 SMI, and the median prevalence rate was 35.7%.

TABLE 1

Table 1. Baseline characteristics of sarcopenia vs. non-sarcopenia groups.

TABLE 2

Table 2. Perioperative management of sarcopenia vs. non-sarcopenia groups.

Compared with those in the non-sarcopenia group, the patients in the sarcopenia group had lower body weight (kg) (P < 0.001), BMI (kg/m²) (P < 0.001), and preoperative blood albumin (P = 0.001). In addition, serum prealbumin (mg/L) (P = 0.029), T-BIL (μM) (P = 0.001), and ALT (IU/L) (P = 0.006) levels were also lower. The intraoperative small dose of remifentanil (µg/h) was lower (P = 0.041). The intraoperative tidal volume (ml/kg) of kilogram body weight (ml/kg) in the sarcopenia group was larger than that in the non-sarcopenia group (P < 0.001). As for the types of surgical resection, most distal gastrectomies were performed in the two groups, accounting for >50% in each group, while there was no proximal gastrectomy in the sarcopenia group (P = 0.003). The postoperative use of an intravenous analgesia pump was lower in the sarcopenia group than in the non-sarcopenia group (P = 0.037). In terms of pathological diagnosis, adenocarcinoma was lower in the sarcopenia group than in the non-sarcopenia group (P = 0.007). Other preoperative and intraoperative factors were not significantly different between the two groups.

Comparison of short-term outcomes

Compared with the non-sarcopenia group, the sarcopenia group had worse outcomes for the incidence of the PPCs (P = 0.024). Moreover, the incidence of postoperative complications was higher in the sarcopenia group than in the non-sarcopenia group (P = 0.043). A total of three patients were then re-admitted within 30 days after discharge (one case in the sarcopenia group and two cases in the non-sarcopenia group). There were no significant differences in hospitalization cost, LOS, postoperative gastric tube extubation time, or postoperative endotracheal tube extubation time (Table 3).

TABLE 3

Table 3. Outcomes of sarcopenia vs. non-sarcopenia groups.

Risk factors of PPCs and postoperative complications

In the univariate analysis, age, sarcopenia, preoperative comorbidities, SPO₂ < 95% when inhaling air under air, and duration of intraoperative SPO₂ < 95% were risk factors for the PPCs. In the multivariate analysis that included these factors, sarcopenia (odds ratio [OR] 3.79, 95% confidence interval [CI] 1.27–11.34, P = 0.017), preoperative comorbidities (OR 2.86, 95% CI 1.01–8.15, P = 0.049), and duration of intraoperative SPO₂ < 95% (OR 1.14, 95% CI 1.04–1.24. P = 0.005) may be risk factors for PPCs. Univariate analysis also revealed that age, sarcopenia, preoperative comorbidities, and the duration of intraoperative SPO₂ < 95% were risk factors for severe PPCs. Multivariate regression analysis showed that sarcopenia (OR 5.10, 95% CI 1.63–16.00, P = 0.005) and the duration of intraoperative SPO₂ < 95% (OR 1.12; 95% CI 1.02–1.22, P = 0.016) were independent risk factors for severe PPCs in patients after gastric cancer surgery (Table 4).

TABLE 4

Table 4. Univariate and multivariate analysis of factors associated with PPCs.

Univariate analyses also found that sarcopenia was the risk factor for postoperative complications. Multivariate regression analysis with age using binary logistic regression showed that sarcopenia (OR 2.19, 95% CI 1.02–4.72, P = 0.045) was an independent risk factor for postoperative complications after gastric cancer surgery (Table 5).

TABLE 5

Table 5. Univariate and multivariate analysis of factors associated with postoperative complications.

Discussion

We performed a single-center cohort study to investigate the effect of sarcopenia on PPCs in patients after gastric cancer surgery. We found that sarcopenia was associated with a higher incidence of postoperative complications and PPCs, compared to non-sarcopenia, in patients undergoing gastric cancer surgery. Multivariate regression analysis showed that sarcopenia, preoperative comorbidities, and the duration of intraoperative SPO₂ <95% were the risk factors for PPCs in patients undergoing radical gastrectomy. Sarcopenia and intraoperative SPO₂<95% were still the risk factors for severe PPCs. In addition, sarcopenia was an independent risk factor for postoperative complications after gastrectomy.

Some studies have investigated the relationship between sarcopenia and postoperative complications following gastric cancer surgery (29–31). Patients with sarcopenia have a higher risk of postoperative complications and longer LOS. Zhou et al. indicated that sarcopenia is a strong independent risk factor for postoperative complications in older patients with gastric cancer (32). This is consistent with the results of our studies. The mechanism of sarcopenia leading to the increased risk of postoperative complications, especially pulmonary complications, remains unclear, and it is speculated that it may be related to the following possible mechanisms. Respiratory and swallowing muscles are affected by sarcopenia, which can lead to damage to the lungs and swallowing function. Impaired respiratory muscle function and swallowing function may lead to postoperative difficulty in expectoration, aspiration, postoperative pneumonia, and atelectasis (33, 34). Second, sarcopenia is associated with increased insulin resistance and increased circulation of proinflammatory cytokines, which may lead to the risk of postoperative acute lung injury (35). It has been reported that sarcopenia is associated with an increased inflammatory response to surgery (36). Increased inflammatory activity may also lead to pulmonary complications. Muscle fibers produce cytokines and other peptides such as interleukin-6, which affect the immune response by inhibiting the production of tumor necrosis factor-α and insulin resistance (37, 38). Sarcopenia may lead to immune senescence, which is characterized by impaired cellular immune function and increased inflammatory activity (39).

These factors may lead to PPCs. Fortunately, preoperative exercise through inspiratory muscle training, nutritional support, and other preoperative interventions may improve muscle function in patients with sarcopenia and effectively reduce the incidence of PPCs (25, 40). Further prospective studies are required to verify this finding. Sarcopenia can be diagnosed using a questionnaire, action ability test, or L3 SMI on CT. In the future, more attention should be paid to the diagnosis of sarcopenia in different regions, races, and populations, and the relationship between sarcopenia and prognosis should be further explored.

Our study also showed that the longer the duration of SPO₂ < 95%, the higher the incidence of PPCs, especially the severe PPCs. Previous studies also found that a low SPO₂ was associated with increased mortality and mortality caused by pulmonary diseases (41). The duration of intraoperative SPO₂ < 95% may be related to the changes in pulmonary ventilation function caused by lung disease, mechanical ventilation lung injury, operation, and other inflammatory stimulations, which are currently recognized as indicators closely related to PPCs. This study indicated that the management of intraoperative mechanical ventilation could be further improved.

Interestingly, we found that tidal volume was larger in the sarcopenia group (P < 0.001) than in the non-sarcopenia group. In clinical practice, the tidal volume is often set according to the patient's body weight and pulmonary function. Compared to the non-sarcopenia group, the sarcopenia group had a smaller body weight but a larger tidal volume. Studies have shown that mechanical ventilation itself can induce inflammation and cooperate with surgery-induced responses. This magnifying inflammatory cascade reaction leads to lung injury and systemic multiple-organ failure.

Sarcopenia negatively affects the prognosis of patients who require mechanical ventilation, increasing all-cause mortality in these patients (42). This may be related to nutritional status, chronic inflammatory reaction, changes in hormone levels, and lack of physical activity in sarcopenia. Some studies have shown that low tidal volume can reduce pulmonary and systemic inflammatory responses compared with conventional tidal volume (43, 44). Mechanical ventilation with a high tidal volume may cause injury in healthy lungs (45, 46). Although the tidal volume of the two groups in this study did not exceed 10 ml/kg, it was higher in the sarcopenia group than in the non-sarcopenia group. There was no significant difference in the average value of PEEP between the two groups (the average value was approximately 2.8–2.9). Some studies have shown that the use of lower levels of PEEP may make the small airways open and close repeatedly, resulting in atelectasis and accelerating the development of pulmonary complications (47, 48). Multifaceted lung-protective ventilation strategies for high-risk patients, combined with low tidal volume, reopening of collapsed alveoli, and moderate levels of PEEP, can prevent further collapse (49). This would help reduce the incidence of postoperative atelectasis, improve clinical results, and reduce the consumption of medical resources. Whether the existing lung-protective ventilation strategy is the best perioperative ventilation management mode for patients with sarcopenia, and how to individualize PEEP and tidal volume to reduce the increase in PPCs caused by mechanical ventilation remain open questions.

Given the adverse effects of sarcopenia on mortality and hospital outcomes, sarcopenia is often considered a treatable indicator in adult respiratory medical treatment (50). It also shows that the prognosis of patients with sarcopenia can be improved through clinical intervention. Previous studies have shown that rehabilitation exercises, nutritional support, and growth hormone supplementation can improve the muscle mass and prognosis of patients with mechanical ventilation (51–53). However, to date, accurate intervention for sarcopenia has been the focus of attention in patients with oligomyopathy. These findings suggest that doctors should pay more attention to the perioperative respiratory system, intraoperative ventilation management, and postoperative lung rehabilitation. It is not limited to the preoperative evaluation and intraoperative management of anesthesiologists, but also includes early identification and intervention by surgeons, rehabilitation doctors, and nurses to reduce its effect on the poor prognosis of patients with sarcopenia. Therefore, it is necessary to carry out a unified standard diagnostic method, larger sample sizes, and multicenter prospective studies on sarcopenia intervention.

Our study bears several limitations. First, this was a single-center retrospective study with incomplete or, in limited cases, absent medical records, and a small sample size. The conclusions of this study need to be verified in additional multicenter prospective studies, involving larger samples. Second, the definitions of sarcopenia were different. In this study, CT-guided L3 SMI was directly used as an index to evaluate sarcopenia, but it was not diagnosed using a muscle strength test. Since this was a retrospective study, we could not comprehensively evaluate skeletal muscle function. Additionally, the cutoff value was not used in this study because of disease type and other factors. The cutoff value depends on measurement techniques, reference studies, and population availability. Moreover, the definition of sarcopenia is greatly influenced by race, population, sex, and other factors. Currently, considerable controversy remains. Therefore, we used the median prevalence rate of patients with gastric cancer to divide the patients into sarcopenia and non-sarcopenia groups. Because some patients visited the local hospital for revisit after surgery, the relevant data for a long time after surgery could not be accurately collected; therefore the long-term prognosis of the patients was not analyzed in this study.

Conclusions

Our study demonstrates that the duration of intraoperative SPO₂ <95%, sarcopenia, and preoperative comorbidities were the risk factors for PPCs, especially severe PPCs. Furthermore, sarcopenia was an independent risk factor for postoperative complications. Future large randomized controlled trials and long-term follow-ups are needed to confirm the relationship between sarcopenia and prognosis.

Data availability statement

The original contributions presented in the study are included in the article/Supplementary Material, further inquiries can be directed to the corresponding author/s.

Ethics statement

The studies involving human participants were reviewed and approved by The Biomedical Research Ethics Committee of West China Hospital of Sichuan University. Written informed consent for participation was not required for this study in accordance with the national legislation and the institutional requirements.

Author contributions

Conception and design: XZ, CD and XW; Provision of study materials or patients: XZ, CD and LH; Collection and assembly of data: XZ, CD and XW; Data analysis and interpretation: XZ, CD and RZ; Manuscript writing: XZ, CD and XW. All authors contributed to the article and approved the submitted version.

Acknowledgments

We would like to thank Editage (www.editage.cn) for English language editing.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher's note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

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