Analysis of risk factors for dysphagia in patients after laparoscopic radical gastrectomy

Abstract

BACKGROUND

Gastric cancer is among the most prevalent malignancies worldwide. Despite significant advancements in chemoradiotherapy, targeted therapy, and neoadjuvant therapy, conventional surgical intervention remains the cornerstone of gastric cancer management. Improvements in surgical techniques, coupled with the use of staplers and other advanced instruments, have substantially reduced the incidence of complications and mortality following gastric cancer surgery. However, dysphagia remains a common postoperative complication.

AIM

To retrospectively investigate the potential factors contributing to dysphagia in patients who have undergone laparoscopic radical gastrectomy for gastric cancer and to explore effective strategies for its postoperative management.

METHODS

In this retrospective study, we analyzed data from patients who underwent elective laparoscopic total gastrectomy at Lihuili Hospital, Ningbo University, between January 2018 and May 2022. A total of 115 eligible postoperative patients were included. Postoperatively, patients completed questionnaires and were categorized into two groups based on their responses: The dysphagia group (Eating Assessment Tool-10 score ≥ 3) and the non-dysphagia group (Eating Assessment Tool-10 score < 3). Risk factors associated with dysphagia following total gastrectomy were assessed using χ² tests, Fisher’s exact tests, t-tests, Pearson correlation coefficients, and univariate and multivariate regression analyses.

RESULTS

Multivariate analysis further identified anastomotic style, prolonged intubation time, advanced age, and low albumin (ALB) levels as independent risk factors for postoperative dysphagia. Implementing targeted preventive measures for high-risk groups may significantly enhance postoperative quality of life.

CONCLUSION

Univariate analysis revealed that anastomotic style, low serum ALB levels, advanced age, and prolonged intubation time were significantly associated with postoperative dysphagia in gastric cancer patients. Multivariate analysis further identified anastomotic style, prolonged intubation time, advanced age, and low ALB levels as independent risk factors for postoperative dysphagia. Implementing targeted preventive measures for high-risk groups may significantly enhance postoperative quality of life.

Key Words: Dysphagia; Old age; Surgical anastomosis; Laparoscopic total gastrectomy; Low serum albumin

Core Tip: Dysphagia is a common complication after total gastrectomy, yet research on it is limited. This retrospective study analyzed factors influencing dysphagia in patients undergoing laparoscopic radical gastrectomy for gastric cancer and explored management strategies. Data from 115 patients treated at Li Huili Hospital between January 2018 and May 2022 were reviewed. Post-surgery, patients completed questionnaires and were divided into dysphagia (Eating Assessment Tool-10 score ≥ 3) and non-dysphagia (Eating Assessment Tool-10 score < 3) groups. Risk factors were assessed using χ² test, Fisher’s exact test, t-test, Pearson correlation, and regression analyses.

INTRODUCTION

Gastric cancer is among the most prevalent malignancies worldwide. Despite significant advancements in chemoradiotherapy, targeted therapy, and neoadjuvant therapy[1], conventional surgical intervention remains the cornerstone of gastric cancer management[2,3]. Improvements in surgical techniques, coupled with the use of staplers and other advanced instruments, have substantially reduced the incidence of complications and mortality following gastric cancer surgery. However, dysphagia remains a common postoperative complication[4], significantly affecting patients’ quality of life and prognosis. Despite its clinical relevance, data on the characteristics and management of postoperative dysphagia are limited. In particular, there is a lack of comprehensive studies exploring the factors contributing to dysphagia after laparoscopic total gastrectomy.

Dysphagia is a somewhat subjective condition, typically describing sensations such as food or liquids feeling stuck in the throat or chest during swallowing[5], or experiencing pain, choking, or coughing while swallowing. Accurately quantifying the prevalence of dysphagia poses a challenge[6]. According to reports, the swallowing process is regulated by internal nerves, and dysphagia may occur to varying degrees in patients with abnormal gastrointestinal peristalsis or tissue injury[7]. Common causes of dysphagia following gastric cancer surgery may include anastomotic stenosis and infectious lesions. This study conducted a retrospective analysis to evaluate the impact of various factors, including surgical anastomosis techniques, age, body mass index (BMI), clinical stage, and other relevant variables, on the occurrence of postoperative dysphagia in gastric cancer patients. The primary objective was to identify risk factors associated with postoperative dysphagia, assess medical conditions potentially contributing to its development, and provide a robust foundation for improving postoperative quality of life and clinical outcomes in these patients.

MATERIALS AND METHODS

This study was approved by the Medical Ethics Committee of the Affiliated Lihuili Hospital of Ningbo University and focused on patients who underwent total gastrectomy for gastric cancer at the hospital between January 2018 and May 2022. Written informed consent was obtained from all participants prior to enrollment. All surgical procedures were performed by the same surgeon, utilizing laparoscopic digestive tract reconstruction techniques, including π anastomosis and overlap anastomosis.

Between March and July 2023, patients who underwent total gastrectomy will be contacted via phone starting from the screening phase to preliminarily assess the presence of dysphagia. Detailed information regarding patients with dysphagia will be collected using SurveyMonkey, through the distribution of an electronic questionnaire and follow-up phone calls. The electronic questionnaire primarily aims to evaluate the severity of dysphagia using the Eating Assessment Tool-10 (EAT-10) scoring system. The EAT-10 questionnaire consists of 10 items related to swallowing, as well as the psychological and social aspects associated with swallowing difficulties. Each item is rated on a scale from 0 (no impairment) to 4 (severe impairment). A total score greater than 3 points generally indicates the presence of swallowing dysfunction. The EAT-10 is useful in identifying signs of aspiration and abnormal swallowing patterns.

During the study period, a total of 246 questionnaires were distributed, with 178 successfully retrieved. Preoperative and postoperative data for these 178 patients were systematically collected, including variables such as age, gender, height, weight, BMI, and medical history, including cardiovascular disease and diabetes. After applying the inclusion and exclusion criteria, 115 patients were ultimately included in the retrospective analysis. Detailed patient histories, including information on hypertension, alcohol consumption, smoking habits, routine laboratory test results, and postoperative tumor pathology, were recorded. Baseline demographic characteristics were compared among the enrolled patients to ensure comparability of the patient populations.

None of the patients exhibited dysphagia prior to surgery. All patients presenting with symptomatic dysphagia underwent postoperative upper gastrointestinal endoscopy to evaluate for esophageal and anastomotic strictures, as well as any mucosal changes. However, no significant abnormalities were detected in any of the patients included in this study. This study included individuals aged 18 years and older who underwent surgical treatment for gastric cancer. The inclusion criteria were as follows: (1) Absence of distant metastases; (2) Willingness to participate in long-term follow-up and research post-surgery; and (3) Provision of written informed consent. Exclusion criteria included: (1) Diagnosis of achalasia; (2) Presence of atypical reflux symptoms; (3) History of stroke or neuromuscular disorders; (4) Traumatic brain injury; and (5) Receipt of preoperative radiotherapy and/or chemotherapy. A total of 63 patients were excluded based on these criteria. The detailed inclusion process is depicted in Figure 1.

Figure 1  Incorporate standard flowcharts.

Statistical analysis

The data were analyzed on a per-subject basis, following the recommendations in the literature to initiate a mechanically modified soft diet ≥ 2 weeks post-surgery[8]. Therefore, dysphagia occurring ≥ 2 weeks after surgery was included in the final analysis. Patients with an EAT-10 score ≥ 3 were categorized as the dysphagia group, while those with an EAT-10 score < 3 were classified as the control group (as shown in Table 1). Statistical analyses were performed using SPSS software (IBM SPSS Statistics 27). Preoperative general characteristics, surgical details, and postoperative pathological findings were compared between the two groups. Independent sample t-tests and one-way ANOVA were used for normally distributed data, while Mann-Whitney U tests and Kruskal-Wallis tests were employed for non-normally distributed continuous variables. Paired t-tests were conducted for preoperative and postoperative continuous data, and χ² tests were applied for categorical variables to assess differences between responders and non-responders. A significance level of P ≤ 0.05 was used for all statistical tests.

Table 1 Eating Assessment Tool-10 swallowing screening scale.

Eating Assessment Tool-10 swallowing screening scale	Score
The difficulty in swallowing caused me to lose weight	0	1	2	3	4
The problem of swallowing prevented me from eating out as before	0	1	2	3	4
It takes a lot of energy to drink a drink	0	1	2	3	4
It takes a lot of effort to eat solid food	0	1	2	3	4
It takes a lot of effort to swallow pills	0	1	2	3	4
The process of swallowing causes pain	0	1	2	3	4
The problem of swallowing made it impossible for me to enjoy my meal	0	1	2	3	4
I will feel something stuck in my throat after eating	0	1	2	3	4
Cough while eating	0	1	2	3	4
The process of swallowing makes me nervous	0	1	2	3	4

0 indicates no problem and 4 indicates the most serious problem. A total score of ≥ 3 indicates a possible risk of dysphagia.

RESULTS

Preoperative general condition

The study cohort consisted of 24 females (20.9%) and 91 males (79.1%). The mean age of the participants was 65.42 ± 7.43 years, with a range of 47 to 82 years. The average preoperative BMI was 21.76 ± 3.20 kg/m². All patients underwent radical gastrectomy, and pathological diagnoses confirmed the presence of gastric cancer. As shown in Table 2, preoperative demographic factors, including gender, age, preoperative serum albumin (ALB) levels, smoking history, alcohol consumption, cardiovascular disease, diabetes (fasting blood glucose > 7.1 mmol/L), thyroid disease, bronchitis, and chronic obstructive pulmonary disease (COPD), were categorized based on the presence of dysphagia and analyzed using logistic regression models. The results revealed that age (P = 0.017), preoperative serum ALB levels (P = 0.002), and preoperative bronchitis or COPD (P < 0.001) were statistically significant. Older patients were more likely to experience postoperative dysphagia. Furthermore, patients with preoperative bronchitis or COPD had a significantly higher risk of dysphagia after surgery compared to those without respiratory conditions. In contrast, no significant associations were found between sex, BMI, hypertension, diabetes, coronary heart disease, smoking, alcohol consumption history, and postoperative dysphagia. Although previous studies suggested a potential link between thyroid disease or prior thyroid surgery and postoperative dysphagia following total gastrectomy, our study did not find a significant correlation between a history of thyroid disease and the occurrence of postoperative dysphagia.

Table 2 The general condition of the patient before operation is counted, n (%).

Variable	Patients with dysphagia (n = 18)	Patients without dysphagia (n = 97)	P value
Gender			0.271
Male	16 (88.9)	75 (77.3)	-
Female	2 (11.1)	22 (22.7)	-
Age, years, mean ± SD	69.22 ± 7.030	64.71 ± 8.565	0.017
Preoperative nutritional status
BMI (kg/m²), mean ± SD	20.51 ± 2.86	21.99 ± 3.22	0.071
Serum albumin (g/L), mean ± SD	34.44 ± 4.32	38.99 ± 5.64	0.002
Hypertension	35 (36.1)	7 (38.9)	0.820
Diabetes	4 (22.2)	26 (26.8)	0.684
Coronary heart disease	4 (22.2)	12 (12.4)	0.267
Smoking	10 (55.6)	41 (42.3)	0.297
Alcohol	7 (38.9)	43 (44.3)	0.669
Thyroid disease	1 (5.6)	5 (5.2)	0.944
Chronic bronchitis or COPD	4 (22.2)	6 (6.2)	0.027

BMI: Body mass index; COPD: Chronic obstructive pulmonary disease.

Surgical-related data

Goh et al[4] suggested that patients undergoing total gastrectomy tend to have larger tumor lesions and higher tumor locations, which result in greater surgical trauma compared to proximal or distal gastrectomy, thereby leading to a higher incidence of complications. We hypothesized that the occurrence of postoperative dysphagia might be related to the extent and method of surgical resection. However, since the majority of dysphagia cases in our clinical dataset were observed in patients undergoing total gastrectomy, with only a few cases in those who had distal or proximal gastrectomy, statistical significance was not achieved. As a result, only patients who underwent total gastrectomy were included in this study. To further examine the impact of different anastomotic techniques on postoperative dysphagia, two laparoscopic surgical methods “II anastomosis and overlap anastomosis” were independently compared. The results showed that patients who underwent overlap anastomosis had a lower likelihood of developing postoperative dysphagia. As shown in Table 3, patients with prolonged tracheal intubation times (P < 0.001) demonstrated a significantly higher risk of developing postoperative dysphagia. However, no significant associations were found between intraoperative blood loss (P = 0.754), postoperative complications (P = 0.451), and the occurrence of postoperative dysphagia.

Table 3 Operation related data statistics, n (%).

Variable	Patients with dysphagia (n = 18)	Patients without dysphagia (n = 97)	P value
Surgical method	-	-	0.036
II anastomosis	13 (72.2)	44 (45.4)	-
Overlap anastomosis	5 (27.8)	53 (54.6)	-
Tracheal intubation time, mean ± SD	204.11 ± 7.64	181.75 ± 2.43	< 0.001
Amount of bleeding, mean ± SD	97.22 ± 23.99	103.76 ± 7.80	0.754
Postoperative complications	2 (11.1)	6 (6.2)	0.451

Postoperative pathological condition

As shown in Table 4, the pathological type (P = 0.803), maximum tumor diameter (P = 0.058), primary tumor location (P = 0.925), degree of differentiation (P = 0.117), pathological stage (tumor stage: P = 0.461, node stage: P = 0.087), microsatellite instability status (P = 0.784), and human epidermal growth factor receptor 2 status (P = 0.919) did not demonstrate any statistically significant associations with postoperative dysphagia.

Table 4 Postoperative pathologic data were analyzed, n (%).

Variable	Patients with dysphagia (n = 18)	Patients without dysphagia (n = 97)	P value
Msi	1 (5.6)	4 (4.1)	0.784
Her2+	2 (11.1)	10 (10.3)	0.919
Pathology type of tumor	-	-	0.803
Adenocarcinoma	17 (94.4)	86 (88.7)	-
Signet-ring cell carcinoma	1 (5.6)	6 (6.2)	-
Neuroendocrine tumor	0	1 (1.0)	-
Low adhesion carcinoma	0	4 (4.1)	-
The longest diameter of the tumor (cm) mean ± SD	3.16 ± 1.77	4.40 ± 2.66	0.058
Tumor location			0.925
Upper	2 (11.1)	13 (13.4)	-
Middle	4 (22.2)	24 (24.7)	-
Lower	12 (66.7)	60 (61.9)	-
Tumor differentiation			0.117
Poor	14 (77.8)	75 (77.3)	-
Moderate-poor	2 (11.1)	20 (20.6)	-
Medium	2 (11.1)	2 (2.1)	-
The pT category			0.461
< T2	1 (5.6)	11 (11.3)	-
T2-T4a	17 (94.4)	86 (88.7)	-
The pN category			0.087
0	9 (50.0)	34 (35.1)	-
1	5 (27.8)	11 (11.3)	-
2	3 (16.7)	19 (19.6)	-
3	1 (5.6)	33 (34.0)	-

Msi: Microsatellite instability; Her2+: Human epidermal growth factor receptor 2.

Multivariable logistic regression analysis

As shown in Table 5, multivariate logistic regression analysis (forward method) was performed based on the significant risk factors identified in the previous analysis, including intraoperative anastomosis type, age, serum ALB level, preoperative presence of bronchitis or COPD, and duration of tracheal intubation. The analysis revealed that four variables - serum ALB level, tracheal intubation time, age, and anastomotic method - were retained in the model due to their significant effects. Notably, the presence of bronchitis or COPD prior to surgery was not included in the final model, indicating that it was not significantly associated with postoperative dysphagia.

Table 5 Results of multivariate logistic regression analysis.

Variable	B	SE	Wals	P value	Exp
Age, years	0.86	0.040	4.567	0.033	1.090
Surgical method	1.341	0.722	3.450	0.043	3.822
Serum albumin (g/L)	-0.173	0.064	7.369	0.007	0.841
Chronic bronchitis or COPD	1.445	0.934	2.397	0.122	4.244
Tracheal intubation time	0.030	0.012	6.212	0.013	1.031
Constant	-7.029	4.012	3.069	0.080	0.001

COPD: Chronic obstructive pulmonary disease.

DISCUSSION

Surgery remains a cornerstone in the treatment of gastric cancer; however, dysphagia is a significant postoperative complication, particularly following total gastrectomy[4]. Previous studies on the incidence of dysphagia after total gastrectomy have been limited. The aim of this study was to conduct both univariate and multivariate retrospective analyses to identify potential factors influencing postoperative dysphagia in patients. We excluded patients who experienced immediate postoperative dysphagia, as mild symptoms are commonly observed after total gastrectomy[8], often attributed to transient edema at the anastomosis site, postoperative mucosal inflammation, and fasting. In the present study, the incidence of postoperative dysphagia, excluding symptoms occurring within the first two weeks after surgery, was 15.6%. Among the 18 patients who developed dysphagia, the mean time to onset was 79.31 ± 42.18 days.

Among the study participants, the mean age of patients who developed dysphagia was significantly higher than that of those without symptoms (P = 0.033). Elderly patients experience various physiological changes in swallowing, including reduced neuronal coordination and decreased digestive motility due to diminished connective tissue elasticity[9,10], which makes them more susceptible to dysphagia. Sura et al[11] reported a decline in muscle mass and contractility in older individuals, leading to a reduction in the strength and velocity of digestive tract movements, which further exacerbates postoperative dysphagia. In the logistic regression analysis conducted in this study, low serum ALB levels were identified as an independent risk factor for dysphagia. Low serum ALB is commonly used as an indicator of nutritional status and is often associated with malnutrition[12], which can contribute to swallowing difficulties through its adverse effects on muscles and nerves[13]. These effects include muscle wasting, loss of muscle mass and strength[13,14], and reduced nerve conduction velocity[15]. The coordination between the nervous system and muscle contraction during swallowing is crucial, suggesting an interplay between malnutrition, neuromuscular dysfunction, and dysphagia[16]. Notably, malnutrition can both predispose individuals to dysphagia and result from it.

Additionally, prolonged endotracheal intubation significantly influenced the occurrence of postoperative dysphagia in our study. Hou et al[17] similarly confirmed that the duration of endotracheal intubation was a significant risk factor for dysphagia following intensive care unit extubation. In line with these findings, Hongo et al[18] observed that longer durations of endotracheal intubation were associated with an increased risk of dysphagia after extubation. Prolonged endotracheal intubation may impair laryngeal and pharyngeal muscle function, thereby affecting the coordination and strength of chewing and swallowing movements. Moreover, the positioning of the endotracheal tube may cause damage or compression to the normal anatomy of the larynx and esophagus, potentially resulting in postoperative dysphagia. Univariate analysis[19] also demonstrated a significant association between preoperative bronchitis or COPD and postoperative dysphagia; however, this relationship lost significance in multivariate analyses when accounting for other factors.

For gastrointestinal diseases, surgical resection of lesions is often followed by the need for digestive tract reconstruction. The primary goal of digestive tract reconstruction is to preserve postoperative physiological function as much as possible[20] and to ensure an improved quality of life for patients. The method of digestive tract reconstruction employed can significantly affect patient outcomes. Following total gastrectomy, various reconstruction techniques are available, including tubular anastomosis, linear anastomosis, and manual anastomosis. Manual anastomosis is rarely used due to its high technical demands and steep learning curve. Tubular anastomosis, which is widely applied in surgical practice, provides superior incisal margins and includes techniques such as the reverse puncture method, pouch suture method, and OrVil method, differing in stapler anvil placement. With the growing prevalence of laparoscopic total gastrectomy, linear anastomosis has gained popularity, incorporating techniques such as functional end-to-end anastomosis, overlap anastomosis, and II-type anastomosis.

In this study, we observed that all patients who developed dysphagia following laparoscopic total gastrectomy had undergone π anastomosis during the procedure. II anastomosis, a modification of functional end-to-end anastomosis, involves initially anastomosing the jejunum to the right side of the esophagus before proceeding with stomach resection[21]. While this technique simplifies the surgical procedure and reduces operative time, it is associated with uncertainty regarding the margins of the anastomotic site. Additionally, the higher side of the anastomosis may be subjected to excessive tension and compromised blood supply[22]. Moreover, some researchers have suggested that the π anastomosis creates an angulation between the jejunum and the esophagus, resulting in an anti-peristaltic alignment that deviates from the natural physiological pathway. This anatomical configuration may impede the smooth passage of food and could represent a key factor contributing to postoperative dysphagia. In contrast, overlap anastomosis is currently a widely adopted reconstruction method for total laparoscopic gastrectomy in China. Initially introduced to facilitate peristaltic digestive tract reconstruction, the overlap technique significantly reduces anastomotic tension and the incidence of reflux esophagitis[23]. However, due to the limited access and narrow space for esophagojejunal anastomosis, manual suturing under magnification is often required when closing the common opening[23,24]. This procedure is complex and time-consuming, requiring effective teamwork and posing risks such as Roux limb distortion and retraction of the esophagojejunal anastomosis into the mediastinum. Zhang[25] roposed a novel approach to overlap anastomosis involving delayed separation of the esophagus, using the stomach as a traction point, which may offer an optimal solution for total laparoscopic esophagojejunal anastomosis.

We found that the incidence of postoperative dysphagia was significantly higher in patients who underwent II-shaped anastomosis compared to those who underwent overlap anastomosis. The overlap anastomosis technique aims to reduce the occurrence of postoperative dysphagia, alleviate patients’ eating difficulties and discomfort, shorten both the operative and anastomotic durations, thereby minimizing endotracheal intubation time. This approach helps to reduce laryngeal and esophageal damage, ultimately facilitating faster postoperative recovery. Furthermore, for patients with compromised preoperative nutritional status, we recommend appropriate nutritional supplementation to improve serum ALB levels. Elderly patients should undergo thorough preoperative evaluations to proactively address any potential intraoperative complications.

However, this study has several limitations. First, its retrospective design inherently carries a lower level of evidence compared to prospective studies. Second, dysphagia assessment in clinical practice is subjective, which may introduce inaccuracies in its definition. Additionally, the study’s small sample size and single-center design limit the generalizability of the findings. Therefore, future research should include large-scale, multicenter prospective studies to validate these results. Despite these limitations, this study represents a significant contribution by quantifying the incidence of post-total gastrectomy dysphagia and analyzing potential contributing factors for the first time.

CONCLUSION

Dysphagia has increasingly emerged as a common complication following total gastrectomy, significantly impacting patient mortality and hospital outcomes. Advanced age, low serum ALB levels, prolonged tracheal intubation time, and the use of II anastomosis have been identified as independent risk factors for the development of dysphagia. In light of these findings, we emphasize the importance of employing improved overlap techniques and minimizing intraoperative tracheal intubation duration to reduce the incidence of postoperative dysphagia. Additionally, thorough preoperative assessment is essential for elderly patients and those with preexisting low serum ALB levels. Finally, special attention should be given to preventing postoperative complications in patients diagnosed with dysphagia.

ACKNOWLEDGEMENTS

We extend our sincere gratitude to all the participants and clinical staff involved in this research.