Impact of visceral fat distribution on postoperative complications in high-aged patients undergoing gastric cancer surgery: A cross-sectional study

Abstract

BACKGROUND

The annual incidence of gastric cancer in elderly patients is increasing. Despite the continuous progress in treatment methods, the prognosis of elderly patients remains poor, and postoperative complications are frequent. Obesity is believed to be associated with the risk of gastric cancer and postoperative prognosis; however, the effect of visceral fat distribution on postoperative complications of gastric cancer in elderly patients remains unclear.

AIM

To explore the effect of visceral fat distribution on postoperative complications of gastric cancer in elderly patients.

METHODS

A total of 163 elderly patients treated at the Affiliated Longyan First Hospital of Fujian Medical University after radical gastrectomy between January 2021 and January 2024 were enrolled. The patients' visceral and subcutaneous fat distributions were measured and divided into a high visceral fat area (VFA-H) group and a low visceral fat area (VFA-L) group, with a critical value of 100 cm². The t-test and χ² test were used to calculate and analyze the relationship between visceral fat area (VFA) and complications. Independent risk factors for postoperative complications were analyzed using binary logistic regression analysis.

RESULTS

Compared with the VFA-L group, the incidence of postoperative complications was higher in the VFA-H group (27.8% vs 6.4%, P < 0.001), and the operation time was longer (268.55 ± 63.41 vs 224.31 ± 51.89, P < 0.001). The amount of blood loss was more (163.77 ± 105.27 mL vs 127.93 ± 98.26 mL, P < 0.001). Logistic regression analysis showed that VFA [odds ratio (OR): 2.597, 95%CI: 1.479-4.853, P = 0.004], total fat area (OR: 1.655, 95%CI: 1.076-4.040, P = 0.013), and the visceral subcutaneous fat area ratio (OR: 2.046, 95%CI: 1.196-5.640, P = 0.008) were independent risk factors for postoperative complications.

CONCLUSION

This study showed that postoperative complications are closely related to fat distribution in elderly patients with gastric cancer undergoing gastrectomy. A high VFA is associated by a high incidence of postoperative complications.

Key Words: Visceral fat distribution; Gastric cancer; Complications; Risk factor; Cross-sectional study

Core Tip: Postoperative complications were closely related to visceral fat content in elderly patients with gastric cancer who underwent gastrectomy. High visceral fat area results in increased intraoperative blood loss, longer operation time, and a higher incidence of postoperative complications. Clinicians should pay close attention to the relevant indicators before surgery and improve the nutritional status of patients to minimize the risk of postoperative complications and improve prognosis.

INTRODUCTION

Gastric cancer is the fifth most common malignant tumor worldwide, the third leading cause of cancer-related deaths, and one of the major health problems facing mankind[1]. Its incidence is closely related to age, with about 65% of new cases in the United Kingdom occurring in patients over the age of 70[2]. Gastrectomy remains the definitive treatment for patients with potentially curable gastric cancer. However, the survival rate of elderly patients after surgery is also a concern. Recent studies have shown that the mortality rate within 30 days after radical surgery in elderly patients with gastric cancer remains very high, ranging from 4.1% to 7.4% in recent studies[3,4], and the 5-year overall and disease-specific survival rates after radical surgery are 51.5% and 58.3%, respectively[5]. Therefore, improving the prognosis of elderly patients is a priority. Moreover, reducing the incidence of complications in elderly patients with gastric cancer is crucial for improving short- and long-term outcomes[6].

As living standards have improved over the past few decades, the global prevalence of obesity has increased. The global average body mass index (BMI) increased by 0.4 kg/m² per decade for men and 0.5 kg/m² for women[7]. Surgeons have gradually recognized that extreme systemic obesity is a potential risk factor for various malignant tumors, surgical morbidity, and mortality[8]. A meta-analysis[9] showed that obesity is associated with an increased risk of stomach cancer, and the strength of this association increases with increasing BMI. However, other epidemiological studies on the association between excess body weight and cancer risk have yielded conflicting results[10,11]. Therefore, obesity alone is unlikely to fully explain the risk or distribution of stomach cancer. Adipose tissue is divided into visceral adipose tissue (VAT) and subcutaneous adipose tissue (SAT)[12]. Different fat distribution patterns may reflect a unique metabolic environment associated with disease development. Compared with SAT, VAT has more cells and blood vessels, accumulation of adipokines and immune cells that produce inflammatory mediators, and increased endocrine and metabolic activities, all of which cause chronic low-grade systemic inflammation[13]. A study has found that increased VAT is associated with reduced cancer survival in malignant melanoma[14], endometrial cancer[15], colorectal cancer[16], and postmenopausal breast cancer[17]. In addition, studies have found that visceral obesity is also associated with multiple hormones, such as insulin-like growth factor and adiponectin, which are known to affect cell division, cell death, and healing. Therefore, visceral obesity may alter the risk of cancer through these mechanisms[18].

Few studies have evaluated the association between the distribution of visceral obesity and postoperative complications of gastric cancer in older patients. Therefore, this study aimed to explore the effect of visceral fat distribution on postoperative complications in elderly patients with gastric cancer, and provide new ideas for improving the prognosis of patients with gastric cancer.

MATERIALS AND METHODS

Research participants

A total of 163 elderly patients treated in the Affiliated Longyan First Hospital of Fujian Medical University after radical gastrectomy from January 2021 to January 2024 were collected. The patients' visceral and subcutaneous fat distributions were measured and divided into a high visceral fat area (VFA-H) group and a low visceral fat area (VFA-L) group, with a critical value of 100 cm². The t-test and χ² test were used to calculate and analyze the relationship between VFA and complications. The independent risk factors for postoperative complications were analyzed using binary logistic regression analysis.

The inclusion criteria: (1) Age ≥ 60 years; (2) Patients undergoing laparoscopic total gastrectomy (LTG) combined with D2 Lymph node dissection for gastric adenocarcinoma confirmed by preoperative endoscopic biopsy or postoperative pathology, and undergoing postoperative pathological diagnosis confirming R0 resection; (3) The tumor stage was T₁N₀M₀-T_4aN₀M₀; (4) No other primary malignant tumor; and (5) Consented to participate in the trial and gave written informed consent.

The exclusion criteria: (1) Patients receiving neoadjuvant chemotherapy or radiotherapy that might affect the efficacy assessment; (2) Patients unable to undergo radical surgery for gastric cancer; (3) Patients with other malignant tumors or other organ failure; and (4) Patients who withdrew participation in the trial after signing the informed consent form. Based on the inclusion and exclusion criteria, 163 patients were included in the study.

This study was a retrospective cohort study. According to the previous literature investigation and clinical experience of the research team, the probability of postoperative complications was estimated, and the incidence was about 35%. The results were input into PASS 15 for sample size estimation, α was 0.05 (bilateral), and the sample loss rate of 10% was considered. Finally, n = 135 cases were identified. The general rule of logistic regression requires the ratio of the number of items to the sample size to be between 1:5 and 1:10. Therefore, the sample size of the participants in this study was 179 cases. There were 17 cases of loss to follow-up, and the final statistics included 163 cases. Written informed consent was obtained from all patients.

General information questionnaire

The general information questionnaire included demographic data (such as age, sex, and BMI) and clinical data, including whether there was a combination of hypertension, diabetes, hyperlipidemia, American Society of Anesthesiologists (ASA) score, visceral fat area (VFA), subcutaneous fat area (SFA), and blood pressure. SFA, muscle fat content, total fat area (TFA), relative VFA (rVFA), etc.

Quantitative computed tomography was used to determine fat distribution

Quantitative computed tomography (QCT) combined with low-dose chest computed tomography (CT) can accurately measure the area and content of subcutaneous fat, visceral fat, and muscle fat without increasing the amount of radiation. Adipose tissue was determined using the Lightspeed VCT 64-row CT scanner (General Electric, United States) in accordance with conventional low-dose chest CT scanning specifications by setting attenuation levels in the range of -190 to -30 Hounsfield units. The scanning parameters were as follows: Tube voltage, set at 120 kV; tube current, 100 mA; scanning field of view 500 mm × 500 mm, layer thickness, 5 mm; and pitch, 0.984. The scanned images were uploaded to a QCT Pro workstation for image analysis using QCT Pro Version 6.1 software. The abdominal fat area was measured at the central level of the L2 vertebra using the "Tissue Composition" module, and the abdominal fat tissue was divided into subcutaneous fat and visceral fat using the blue threshold semi-automatic segmentation. The abdominal area of interest was mapped semi-automatically to identify the areas of subcutaneous and visceral fat. The "Measure Muscle Fat" module was used to measure the percentage of paravertebral muscle fat of the subjects. The regions with a relatively homogeneous central density of the psoas major muscle on both sides were selected in the horizontal cross-section of the endplate of the L2 vertebral body, and the areas of interest with each selected area of approximately 90-110 mm were measured. Finally, the mean values of the two were taken as the measurement results. Total fat area (TFA = VFA + SFA) and the visceral subcutaneous fat area ratio (VSR = VFA/SFA). In addition, patients were divided into two groups according to the VFA threshold recommended by the Japanese Association for the Study of Obesity[19]: VFA-L group, VFA < 100 cm²; and VFA-H group, VFA ≥ 100 cm². The measurement method is shown in Figure 1.

Figure 1 Measurement image of abdominal fat distribution. The red, blue, and yellow areas indicate muscle, subcutaneous, and visceral fat, respectively. The software automatically identifies visceral and subcutaneous fat according to the selected area boundary and fat density range and completes the measurement of fat volume and average density, allowing the observer to correct the boundary.

Controlling nutritional status

The controlling nutritional status (CONUT score) was calculated using the latest preoperative results of serum albumin (ALB) level, serum total cholesterol (TC), and total lymphocyte count[20] (Table 1).

Table 1 The controlling nutritional status.

Parameter	Malnutritional status
	Normal	Mild	Moderate	Severe
ALB (g/dL)	3.5-4.5	3.0-3.49	2.5-2.9	< 2.5
Score	0	2	4	6
Total lymphocytes (/mm3)	≥ 1600	1200-1599	800-1199	< 800
Score	0	1	2	3
Cholesterol (mg/dL)	≥ 180	140-180	100-139	< 100
Score	0	1	2	3
Total	0-1	2-4	5-8	9-12

ALB: Albumin.

Observation index

Operative time, intraoperative blood loss, first exhaust time, oral recovery time, postoperative hospital stay, and postoperative complications were recorded as surgical outcomes. Serological indices mainly recorded ALB, hemoglobin, C-reactive protein (CRP), triglycerides (TG), TC, white blood cells, red blood cell, and total lymphocyte counts. Postoperative complications included anastomotic lesions (anastomotic fistula, anastomotic stenosis, and anastomotic hemorrhage), surgical incision infection or fat liquefaction, pulmonary infection, abdominal infection, intestinal obstruction, and others including pancreatic fistula, bacteremia, deep vein thrombosis, pulmonary embolism, and arrhythmia.

Statistical analysis

The results of each scale were input into the computer for score conversion, and SPSS 26 (IBM SPSS, United States) was used for statistical analysis. The measurement data were represented by mean and standard deviation, and the counting data were represented by frequency and percentage. The t-test and χ² test were used for statistical analysis between groups. After collinearity diagnosis, the independent risk factors of postoperative complications and infection were analyzed using binary logistic regression analysis, and P < 0.05 was considered statistically significant.

RESULTS

Baseline data

The baseline characteristics of the patients are shown in Table 2. A total of 163 patients were included in this study, 22 of whom experienced postoperative complications. The mean age of the group without complications was 68.23 ± 7.94, and that of the group with complications was 69.12 ± 7.45. There were no significant differences in age, sex, history of hypertension, location of the primary tumor, or tumor-node-metastasis stage between the two groups (P > 0.05); however, there were significant differences in BMI, history of diabetes, history of hyperlipidemia, ASA score, VFA, SFA, TFA, and VSR between the two groups (P < 0.05).

Table 2 Comparison of the baseline characteristics of patients, n (%).

Item	Without complication	With complication	t/χ2	P value
Age	68.23 ± 7.94	69.12 ± 7.45	-0.892	0.419
Sex
Male	92 (65.2)	15 (68.2)	0.073	0.788
Female	49 (34.8)	7 (31.8)
BMI (kg/m2)	25.87 ± 5.19	29.14 ± 3.28	8.091	0.000
Combined hypertension
Yes	34 (24.1)	5 (22.7)	0.020	0.887
No	107 (75.9)	17 (77.3)
Combined diabetes
Yes	21 (14.9)	9 (42.9)	9.472	0.002
No	120 (85.1)	12 (57.1)
Combined hyperlipidemia
Yes	16 (11.3)	6 (27.3)	4.134	0.042
No	125 (88.7)	16 (72.7)
ASA score
I	61 (43.3)	3 (13.6)	7.004	0.008
II	80 (56.7)	19 (86.4)
Primary tumor site
Esophagogastric junction	55 (39.0)	9 (40.9)	0.123	0.940
Proximal stomach	49 (34.8)	8 (36.4)
Distal stomach	37 (26.2)	5 (22.7)
TNM stage
I stage	38 (27.0)	5 (22.7)	0.175	0.676
II stage	103 (73.0)	17 (77.3)
VFA	105.28 ± 37.61	151.98 ± 45.33	5.872	0.000
SFA	213.60 ± 57.18	247.35 ± 79.35	2.523	0.013
TFA	318.88 ± 47.40	399.33 ± 62.34	9.108	0.000
VSR	0.79 ± 0.41	1.07 ± 0.56	6.129	0.000

BMI: Body mass index; ASA: American Society of Anesthesiologists; VFA: Visceral fat area; SFA: Subcutaneous fat area; TFA: Total fat area; VSR: Visceral to subcutaneous fat area ratio; TNM: Tumor-node-metastasis.

Relationship between postoperative complications and VFA

Patients were divided into two groups based on the VFA cutoff values: 109 in the VFA-L group and 54 in the VFA-H group. There were 7 and 15 complications in the VFA-L and VFA-H groups, respectively. There were statistically significant differences in the incidence of anastomotic lesions, surgical incision infection or fat liquefaction, and total complications between the two groups (P < 0.05), as shown in Table 3.

Table 3 Relationship between postoperative complications and visceral fat area, n (%).

Item	Anastomotic lesions	Surgical incision infection or fat liquefaction	Lung infection	Abdominal infection	Intestinal obstruction	Other	With complication
VFA-L	1 (0.9)	2 (1.8)	1 (0.9)	1 (0.9)	1 (0.9)	2 (1.8)	7 (6.4)
VFA-H	4 (7.4)	5 (9.3)	2 (3.7)	2 (3.7)	1 (1.9)	3 (5.6)	15 (27.8)
χ2	5.115	4.843	1.552	1.552	0.260	1.681	14.106
P value	0.024	0.028	0.213	0.213	0.610	0.195	0.000

VFA-L: Low visceral fat area; VFA-H: High visceral fat area.

Analysis of postoperative related conditions and VFA

The postoperative recovery indicators of patients in the VFA-H group included operation time (268.55 ± 63.41 minutes vs 224.31 ± 51.89 minutes) and intraoperative blood loss (163.77 ± 105.27 mL vs 127.93 ± 98.26 mL) were significantly greater than those in the VFA-L group (P < 0.05), as shown in Table 4.

Table 4 Analysis of postoperative related conditions and visceral fat area.

Item	Operation time (minute)	Intraoperative blood loss (mL)	First exhaust time (day)	Postoperative hospital stay (day)
VFA-L	224.31 ± 51.89	127.93 ± 98.26	2.89 ± 1.13	10.13 ± 4.75
VFA-H	268.55 ± 63.41	163.77 ± 105.27	3.02 ± 1.88	11.28 ± 7.32
t	6.064	8.719	2.981	5.174
P value	0.000	0.000	0.109	0.552

VFA-L: Low visceral fat area; VFA-H: High visceral fat area.

Analysis of serological indicators and VFA

The t test showed that the ALB level in VFA-H group was significantly lower than that in the VFA-L group (33.12 ± 4.67 g/L vs 28.53 ± 3.92 g/L). CRP (6.14 ± 2.47 mg/L vs 13.58 ± 4.36 mg/L), TC (6.33 ± 2.35 mmol/L vs 4.71 ± 1.24 mmol/L), TG (2.78 ± 1.76 mmol/L vs 1.99 ± 1.01 mmol/L), and white blood cell (16.73 ± 5.27 × 10⁹/L vs 11.89 ± 3.44 × 10⁹/L) levels were significantly higher in the VFA-H group than in the VFA-L group (P < 0.05), and there was a significant difference in CONUT scores between the two groups (P < 0.001), as shown in Table 5 and Figure 2.

Figure 2 Comparison of controlling nutritional status between the two groups. This column depicts the distribution of the number of patients in each of the four categories of the controlling nutritional status score for the two groups: Low visceral fat area and high visceral fat area. COUNT: Controlling nutritional status; VFA-L: Low visceral fat area; VFA-H: High visceral fat area.

Table 5 Analysis of serological indicators and visceral fat area.

Item	ALB (g/L)	Hb (g/L)	CRP (mg/L)	TC (mmol/ L)	TG (mmol/L)	WBC (109/L)
VFA-L	33.12 ± 4.67	118.29 ± 39.61	6.14 ± 2.47	4.71 ± 1.24	1.99 ± 1.01	13.89 ± 3.44
VFA-H	28.53 ± 3.92	115.99 ± 41.23	13.58 ± 4.36	6.33 ± 2.35	2.78 ± 1.76	16.73 ± 5.27
t	-3.378	-0.276	4.416	2.434	2.136	3.192
P value	0.452	0.735	0.0007	0.031	0.045	0.057

VFA-L: Low visceral fat area; VFA-H: High visceral fat area; ALB: Albumin; Hb: Hemoglobin; CRP: C-reactive protein; TG: Triglycerides; TC: Total cholesterol; WBC: White blood cell.

Risk factors of complication analyzed by binary logistic regression models

The binary logistic regression analysis showed that BMI, combined history of diabetes, ASA score, VFA, TFA, and VSR were independent risk factors for complications in elderly patients after gastric cancer surgery, as shown in Table 6 and Figure 3.

Figure 3 Forest plot of complication risk factors. The forest plot presents six independent risk factors identified by binary logistic regression analysis as influencing the occurrence of complications in elderly patients after gastric cancer surgery. BMI: Body mass index; ASA: American Society of Anesthesiologists; VFA: Visceral fat area; TFA: Total fat area; VSR: Visceral to subcutaneous fat area ratio; OR: Odds ratio.

Table 6 Risk factors of complication analyzed by binary logistic regression models.

Item	B	SE	Wald	P value	OR	95%CI
						Upper	Lower
BMI (kg/m2)	0.827	0.366	5.624	0.019	1.952	3.624	1.183
Combined diabetes	0.688	0.313	3.705	0.035	1.672	3.185	1.079
Combined hyperlipidemia	0.455	0.241	1.545	0.217	1.544	3.103	0.844
ASA score	0.040	0.019	4.635	0.031	1.041	1.080	1.004
VFA	0.951	0.342	8.531	0.004	2.597	4.853	1.479
SFA	-0.341	0.169	2.121	0.142	0.773	1.074	0.529
TFA	0.857	0.306	6.133	0.013	1.655	4.040	1.076
VSR	0.868	0.325	7.879	0.008	2.046	5.640	1.196

ASA: American Society of Anesthesiologists; VFA: Visceral fat area; SFA: Subcutaneous fat area; TFA: Total fat area; VSR: Visceral subcutaneous fat area ratio; OR: Odds ratio; BMI: Body mass index.

DISCUSSION

Some previous retrospective studies have discussed the effect of visceral fat distribution on postoperative gastric cancer[21,22], mostly due to excessive abdominal fat affecting the surgical outcome; however, few studies have further defined the effect of visceral fat distribution on postoperative complications. Gastrectomy combined with D2 Lymphadenectomy is widely performed in East Asia. Due to the complexity and difficulty of radical surgery for gastric cancer (D2 lymph node dissection), a previous multicenter clinical study involving 17 Chinese medical centers reported that the incidence of serious complications after LTG was as high as 10.3%[23]. According to the results of high-quality RCTs in Japan and South Korea, the incidence of postoperative complications after gastrectomy ranges between 10%-30%[24,25]. Therefore, it is important to identify the complications as early as possible to improve the quality of life and prognosis of patients after surgery. This study retrospectively analyzed the distribution of visceral and subcutaneous fats to provide a relatively high level of evidence clarifying the influence of obesity on postoperative complications in elderly patients undergoing LTG.

A previous study showed that the incidence of postoperative complications in patients with a higher VFA was higher than that in patients with a lower VFA[22], and the results were approximately the same as those in this study. Tokunaga et al[26] found that the proportion of abdominal infections after gastrectomy was 9.6%, which was closely related to the VFA and total fat area. It has been suggested that patients with a high visceral fat content are more likely to develop abdominal infections after gastrectomy. These results were roughly the same as those of the present study, and there were statistically significant differences in the incidence of anastomotic lesions, surgical incision infection, fat liquefaction, and the incidence of total complications. This may be because malignant tumors alter glucose metabolism and induce peripheral insulin resistance due to long-term exposure to proinflammatory molecules[27]. Visceral and subcutaneous fat were independently and positively correlated with peripheral insulin resistance[28]. Diabetes has been proven to be highly associated with anastomotic fistula, infections, and other related conditions[29]. There is also evidence that visceral fat, unlike subcutaneous fat, may contribute to carcinogenesis by secreting pro-inflammatory cytokines and free fatty acids, especially in obese individuals[30,31]. Study has also found that pro-inflammatory cytokines are associated with tumor growth, immune escape and metastasis[32]. In conclusion, fat distribution may influence the occurrence of postoperative complications by affecting blood glucose levels and promoting tumor cell growth. However, this study also found that the operative time and intraoperative blood loss were significantly higher in the VFA-H group than in the VFA-L group. This may be because the excess visceral fat tissue makes the narrow cavity more crowded, increasing the difficulty of laparoscopically assisted gastrectomy. The regression results of this study confirm the above conclusions. In clinical practice, attention should be paid to assessing the fat distribution and nutritional status of patients and providing corresponding management measures to help reduce the occurrence of postoperative complications.

This study also found significant differences in the CONUT scores between the two groups. Lin et al[33] found that in elderly patients with gastric cancer after laparoscopic-assisted radical gastrectomy, the CONUT score is an independent risk factor for overall postoperative complications and can be used as a reliable indicator to judge short-term prognosis. The lower CONUT scores of patients in the VFA-L group may be due to lower ALB levels, as demonstrated in this study. However, whether this is related to the loss of muscle mass needs to be confirmed through further research. In addition, studies have shown that there is a shift in the distribution of VAT and an imbalance of pro-inflammatory adipocytokines in susceptible individuals. Visceral and intramuscular fat have been shown to secrete a large amount of pro-inflammatory cytokines[34], leading to the accumulation of pro-inflammatory immune cells, and the association between obesity and CRP is stronger[35,36]. A positive correlation between the VFA and CRP levels was also observed in this study.

In conclusion, visceral fat distribution has a significant effect on the occurrence of postoperative complications. Therefore, in clinical practice, VFA should be accurately evaluated by CT/magnetic resonance imaging before surgery. In Asian populations, with VFA ≥ 100 cm² as the high-risk threshold, metabolic intervention (such as high-protein diet, etc.) combined with aerobic resistance exercise is recommended to reduce VFA to a safe range within 3-6 months before surgery, while optimizing blood glucose and blood pressure. For patients undergoing short-term surgery, a low-calorie diet can be used to rapidly lose fat; however, branched-chain amino acids and vitamin D supplementation are required to maintain muscle mass. The intraoperative pneumoperitoneum pressure was controlled, and early enteral nutrition was provided after surgery. Finally, multidisciplinary collaboration can achieve simultaneous optimization of metabolism, nutrition, and muscle function to reduce the risk of complications.

Finally, this study has several limitations. First, because this was a retrospective, single-center, cross-sectional study, it was not possible to determine the causal relationship between visceral fat distribution and postoperative complications in gastric cancer. Second, the study population consisted of elderly patients who underwent radical gastrectomy at a single center; therefore, there was sampling bias. In the future, multi-center randomized controlled trials should be conducted to clarify the causal relationship between visceral fat distribution and postoperative complications of gastric cancer, reduce selection bias, and make the results more generalizable.

CONCLUSION

The results of this study show that postoperative complications are closely related to fat distribution in elderly patients with gastric cancer undergoing gastrectomy. A high VFA is characterized by large intraoperative blood loss, long operation time, and a high incidence of postoperative complications. Clinicians should pay close attention to relevant indicators before surgery to improve the nutritional status of patients to minimize the risk of postoperative complications and promote prognosis.

ACKNOWLEDGEMENTS

We would like to express our sincere gratitude to all those who contributed to the successful completion of this study. First, we would like to thank the patients who participated in this study, as well as their families, for their cooperation and trust. Without their willingness to participate, this research would not have been possible. We are deeply grateful to our colleagues at the Department of Gastrointestinal and Anus Surgery, The Affiliated Longyan First Hospital of Fujian Medical University, for their support and assistance throughout the research process. This work was supported by the resources and facilities provided by The Affiliated Longyan First Hospital of Fujian Medical University, Longyan, Fujian Province, China. Finally, we would like to thank the peer reviewers for their insightful feedback, which helped improve the quality of this manuscript.