Effects of anastomotic techniques in laparoscopic distal gastrectomy with Billroth I method on remnant stomach motor functions and postoperative quality of life

Abstract

Laparoscopic distal gastrectomy with Billroth I reconstruction (LDGBI) is a standard procedure for early-stage gastric cancer. Although both Delta-shaped (Delta) and circular stapler (CS) techniques are commonly used for anastomosis, their long-term effects on remnant gastric motility and postoperative quality of life (QOL) remain insufficiently defined. This retrospective study analyzed 43 patients who underwent LDGBI at least one year prior, divided into CS (n=22) and Delta (n=21) groups. Gastric emptying was evaluated using the ¹³C-acetate breath test, focusing on residual reservoir capacity (RR5) and half-emptying time (T1/2). Postgastrectomy symptoms and living status were assessed via structured questionnaires. The Delta group demonstrated significantly lower RR5 (40.5% vs. 56.1%, P=0.033) and shorter T1/2 (4.8 vs. 8.5 min, P=0.033), indicating diminished reservoir function and accelerated gastric emptying. These alterations correlated with a higher incidence of early dumping abdominal symptoms (66.7% vs. 27.3%, P=0.015), as well as trends toward increased early dumping general symptoms and greater body weight loss. The Delta method is associated with enhanced gastric emptying and more frequent postgastrectomy symptoms, likely due to a wider anastomotic stoma. Tailoring the stoma size or selecting alternative reconstruction methods based on remnant gastric volume may help mitigate adverse outcomes and improve patients’ quality of life following LDGBI.

Introduction

The advent of laparoscopic gastrectomy has revolutionized gastric cancer treatment, providing minimally invasive options that improve short- and long-term outcomes (1,2,3). Compared to traditional open surgery, laparoscopic techniques offer reduced intraoperative blood loss, faster recovery, and fewer complications, making them a preferred choice for early stage gastric cancer (1,2,3).

Among distal gastrectomy procedures, Billroth-I reconstruction (LDGBI) has gained widespread acceptance (4, 5). This procedure involves remnant gastroduodenal anastomosis, with evolving techniques such as the circular stapler (CS) and Delta-shaped (Delta) methods offering distinct advantages. The CS method, traditionally performed via a small laparotomy, has been widely used, while the Delta method, performed entirely endoscopically, represents a more recent innovation.

While short-term outcomes, including reduced postoperative pain and shorter hospital stays, have been extensively reported (6,7,8), the long-term effects of these anastomotic techniques on remnant stomach motor function and quality of life (QOL) remain underexplored. Understanding these outcomes is increasingly important as advances in early detection and treatment have led to higher survival rates and a growing focus on postoperative QOL.

This study aims to evaluate the differential impacts of the CS and Delta anastomotic techniques on remnant stomach motor function, postgastrectomy symptoms, and living status. By addressing these factors, the study seeks to optimize long-term patient outcomes.

Methods

Study design and participants

This retrospective study included 43 patients diagnosed with gastric cancer who underwent LDGBI at least one year prior to evaluation. The cohort was divided into two groups based on the anastomotic technique employed: the CS group (n=22) and the Delta group (n=21). All patients were classified as clinical stage IA or IB and had not received adjuvant chemotherapy.

Surgical procedures

At our institution, the anastomotic technique for LDGBI underwent a temporal evolution, shifting from the CS method (Fig. 1A), which required a small laparotomy, to the totally laparoscopic Delta method (Fig. 1B). Accordingly, the CS and Delta groups were not created through randomization or simultaneous allocation but instead represent temporally distinct cohorts shaped by an institutional shift in surgical strategy. The extent of resection included approximately two-thirds of the distal stomach, with D1+ or D2 lymph node dissection performed in all cases. In the CS group, a small laparotomy (4–5 cm) was utilized for hemi-double stapling anastomosis using a 28 or 29 mm circular stapler (9). Conversely, the Delta group underwent entirely endoscopic reconstruction as reported by Kanaya et al. (10).

Fig. 1.

A. Circular stapler (CS) method, B. Delta method.

The hatched area indicates the cross-sectional lumen of the anastomosis, representing the anastomotic opening.

Assessment of remnant stomach motor function

Gastric emptying was evaluated using the ¹³C-acetate breath test, which is performed according to a standardized protocol widely adopted in Japan (11). Patients consumed a test meal comprising 100 mg of ¹³C-labeled sodium acetate mixed with 200 kcal of liquid meal (Racol, Otsuka Pharmaceutical Co., Ltd., Tokyo, Japan). Breath samples were collected before ingestion and at 0, 5, 10, 15, 20, 30, 40, 50, 60, 75, 90, 105, 120, 135, 150, 165, and 180 min after intake. The exhaled ¹³CO₂/¹²CO₂ ratio was measured using infrared spectrometer, UbiT-IR 300^® or POCone^® (Otsuka Electronics Co., Ltd., Osaka, Japan), and the data were analyzed using Wagner–Nelson analysis (12) to calculate gastric retention rates over time. In accordance with prior studies (13, 14), RR5 (defined as the retention rate at 5 min) was employed as an indicator of remnant gastric reservoir capacity, while T1/2 (half-emptying time) was used as a measure of gastric emptying efficiency. These parameters, derived from the ¹³C-acetate breath test using the Wagner–Nelson analytical approach, have been validated and show a strong correlation with scintigraphy, the current gold standard (12).

Questionnaire-based symptom and living status evaluation

Participants completed a structured questionnaire addressing two domains: (1) Postgastrectomy Symptoms: esophageal reflux, nausea, abdominal pain, early satiation, diarrhea, early dumping general symptoms (cold sweat, palpitations, dizziness, numbness, fainting, facial flushing, facial pallor, feeling hot, fatigue or weakness, lassitude, drowsiness, headache, heaviness of the head, tightness in the chest), early dumping abdominal symptoms (borborygmi*, abdominal cramps*, diarrhoea*, nausea, vomiting, bloating, abdominal discomfort; * except after drinking milk), and late dumping (cold sweat, palpitations, dizziness, headache, fainting, fatigue or weakness, lassitude, languor, shakiness, hunger, shortness of breath). (2) Living Status: body weight change, the amount of food consumed per meal (expressed as the proportion of food intake per meal compared to preoperative intake, as subjectively estimated by the patient), and meal frequency per day.

Statistical analysis

Intergroup comparisons were conducted using Fisher’s exact test, the independent t test, or Pearson’s correlation coefficient, as appropriate. A P-value <0.05 was considered statistically significant. Statistical analyses were performed using JMP 12.0.1 software (SAS Institute Inc., Cary, NC, USA).

Ethical considerations

The study was conducted in accordance with the principles of the Declaration of Helsinki. The study protocol was reviewed and approved by the Ethics Committee of the Jikei University School of Medicine (approval no. 18-199[4861]), and written informed consent was obtained from all participants prior to their inclusion.

Results

Patients’ characteristics

The baseline characteristics of the patients are summarized in Table 1. The mean age of patients was marginally higher in the Delta group compared to the CS group (68.7 ± 9.1 vs. 63.2 ± 10.6 years; P=0.078). The postoperative period was marginally shorter in the Delta group than in the CS group (16.6 ± 4.0 vs. 22.8 ± 15.1 months; P=0.075).

Table 1. Comparison of patients’ characteristics, symptoms, living status, and remnant gastric motility between CS and Delta anastomotic methods.

		Anastomotic method
		CS (n=22)		Delta (n=21)		P-value
Patients’ characteristics
	Sex [M/F (%)]	15/7 (68)		14/7 (67)		1.000†
	Age* (years)	63.2	10.6	68.7	9.1	0.078‡
	Postoperative period* (months)	22.8	15.1	16.6	4.0	0.075‡
Remnant gastric motility
	RR5* (%)	56.1	25.5	40.5	20.6	0.033‡
	T1/2* (minutes)	8.5	7.4	4.8	2.2	0.033‡
Symptoms
	Esophageal reflux [Y/N (%)]	2/20 (9.1)		2/19 (9.5)		1.000†
	Nausea [Y/N (%)]	2/20 (9.1)		5/16 (23.8)		0.240†
	Abdominal pain [Y/N (%)]	7/15 (31.8)		6/15 (28.6)		1.000†
	Early satiation [Y/N (%)]	3/19 (13.6)		3/18 (14.3)		1.000†
	Diarrhea [Y/N (%)]	6/16 (27.3)		7/14 (33.3)		0.747†
	Early-dumping general symptoms [Y/N (%)]	2/20 (9.1)		7/14 (33.3)		0.069†
	Early-dumping abdominal symptoms [Y/N (%)]	6/16 (27.3)		14/7 (66.7)		0.015†
	Late-dumping symptoms [Y/N (%)]	2/20 (9.1)		6/15 (28.6)		0.132†
Living status
	Change in body weight* (%)	−7.9	6.3	−12.2	8.3	0.063‡
	Food intake per meal* (%)	66.8	13.2	62.9	21.5	0.469‡
	Frequency of meals per day* (times)	5.2	1.9	6.0	1.7	0.148‡

*Mean ± SD; ^†Fisher’s exact test; ^‡unpaired t test; RR5=retention rate at 5 min; T1/2=half-emptying time. CS: circular stapler.

Remnant stomach motor function

The ¹³C-acetate breath test results revealed significant differences in remnant stomach motor function between the two groups. The RR5 was smaller in the Delta group compared to the CS group (40.5% ± 20.6% vs. 56.1% ± 25.5%; P=0.033), indicating reduced reservoir capacity (Table 1). Similarly, T1/2 was significantly shorter in the Delta group (4.8 ± 2.2 min vs. 8.5 ± 7.4 min; P=0.033), suggesting accelerated gastric emptying (Table 1).

Postgastrectomy symptoms

The frequency of postgastrectomy symptoms is detailed in Table 1. Patients in the Delta group reported significantly higher incidences of early dumping abdominal symptoms (66.7% vs. 27.3%; P=0.015) and marginally higher rates of early dumping general symptoms (33.3% vs. 9.1%; P=0.069). Body weight loss was marginally greater in the Delta group compared to the CS group (−12.2% ± 8.3% vs. −7.9% ± 6.3%; P=0.063).

Relationships between remnant stomach motor function and symptoms

Table 2 illustrates the relationship between remnant stomach motor function and postgastrectomy symptoms. Patients with early dumping abdominal symptoms exhibited significantly reduced RR5 (40.2% ± 21.7% vs. 55.7% ± 24.6%; P=0.035) and significantly shorter T1/2 (4.6 ± 1.7 min vs. 8.5 ± 7.3 min; P=0.027) compared to those without such symptoms.

Table 2. Comparison of reservoir capacity (RR5) and gastric emptying (T1/2) between patients with and without each symptom.

		RR5 (%)					T1/2 (min)
		With symptom		Without symptom		P-value*	With symptom		Without symptom		P-value*
		Mean	SD	Mean	SD		Mean	SD	Mean	SD
Symptoms
	Esophageal reflux	46.7	29.8	48.8	23.8	0.846	5.1	2.4	6.9	6.1	0.475
	Nausea	36.3	17.7	50.9	24.9	0.149	4.1	1.1	7.2	6.2	0.203
	Abdominal pain	50.8	27.0	48.3	24.4	0.847	5.1	1.8	6.8	6.0	0.570
	Early satiation	54.4	23.7	45.9	24.5	0.302	7.1	4.6	6.5	6.3	0.767
	Diarrhea	52.4	23.7	46.8	24.8	0.489	7.7	8.5	6.2	4.3	0.469
	Early-dumping general symptoms	40.0	10.4	50.7	26.5	0.245	4.2	0.7	7.3	6.4	0.160
	Early-dumping abdominal symptoms	40.2	21.7	55.7	24.6	0.035	4.6	1.7	8.5	7.3	0.027
	Late-dumping symptoms	39.0	14.2	50.7	25.7	0.224	4.4	1.3	7.2	6.3	0.226

*unpaired t test; RR5=retention rate at 5 min; T1/2=half-emptying time.

Relationships between remnant stomach motor function and living status

The correlation between remnant stomach motor function and living status is summarized in Table 3. The frequency of meals per day was inversely correlated with RR5 (r=−0.357; P=0.019) and T1/2 (r=−0.388; P=0.010), indicating that reduced reservoir capacity and accelerated gastric emptying were associated with an increased meal frequency.

Table 3. Correlations between remnant gastric motility and living status.

		RR5		T1/2
		r	P-value	r	P-value
Living status
	Change in body weight (%)	0.126	0.420	−0.020	0.897
	Food intake per meal (%)	0.022	0.890	0.032	0.839
	Frequency of meal per day (times)	−0.357	0.019	−0.388	0.010

r=Pearson’s product-moment correlation coefficient; RR5=retention rate at 5 min; T1/2=half-emptying time.

Discussion

This study is the first to demonstrate that differences in anastomotic techniques in LDGBI significantly affect remnant stomach motor function and postoperative QOL. Specifically, the Delta group exhibited significantly reduced reservoir capacity and accelerated gastric emptying compared to the CS group, leading to a higher incidence of early dumping symptoms and a trend toward greater weight loss. These findings highlight the critical role of anastomotic technique selection in optimizing long-term outcomes for patients undergoing LDGBI.

Advances in early gastric cancer detection and minimally invasive surgery have improved survival rates (15) and short-term outcomes (1,2,3), shifting the focus toward postoperative QOL. Laparoscopic distal gastrectomy with Billroth-I reconstruction is widely performed (4, 5), with anastomotic techniques evolving from the conventional CS method to the fully laparoscopic Delta method (5). While meta-analyses have demonstrated superior short-term outcomes with the Delta technique, such as reduced postoperative pain and shorter hospitalization (7), its long-term effects on remnant stomach function and patients’ daily life remain largely unexplored. Considering that differences in anastomotic techniques may significantly impact postoperative symptoms and daily living, this study aimed to clarify the functional and QOL differences between the CS and Delta methods in LDGBI.

The radioisotope method has long been regarded as the gold standard for directly and quantitatively assessing gastric emptying (16). However, its clinical application is limited by the requirement for specialized facilities, radiation exposure, and high costs. In contrast, the ¹³C breath test is a noninvasive, safe, reliable, and cost-effective alternative that indirectly evaluates gastric emptying and is easy to administer (11). Sanaka et al. applied Wagner–Nelson analysis and demonstrated that the gastric emptying rate obtained through the ¹³C breath test using this analytical approach closely correlates with that measured by the radioisotope method (12). Recently, the ¹³C breath test has been utilized to assess gastric emptying in postgastrectomy patients (13, 14, 17, 18). Furthermore, by applying Wagner–Nelson analysis, it is possible to quantitatively evaluate various aspects of gastric motility, including residual reservoir capacity (RR5) and gastric emptying function (T1/2) (13, 14).

Gastric emptying following gastrectomy varies depending on the type of surgical procedure. It has been reported that total gastrectomy results in the most rapid gastric emptying, followed sequentially by distal gastrectomy, proximal gastrectomy, and pylorus-preserving gastrectomy (PPG) (17). Compared to healthy individuals, distal gastrectomy leads to significantly accelerated gastric emptying, whereas local resection maintains gastric emptying rates comparable to those of healthy controls (13). In contrast, PPG has been reported to result in significantly delayed gastric emptying (18).

The impact of gastric motility on symptoms and quality of life (QOL) in postgastrectomy patients has also been investigated. Hayami et al. reported that greater acceleration of gastric emptying is associated with increased symptom severity (17). Additionally, Konishi et al. demonstrated that a reduction in residual reservoir capacity and an acceleration of gastric emptying are significantly associated with the occurrence of diarrhea and dumping symptoms (14). Moreover, these factors exhibit a trend toward certain correlation with a decrease in meal volume per sitting and an increased frequency of daily meals (14).

Our findings demonstrate that patients undergoing the Delta method exhibited significantly reduced gastric reservoir capacity (lower RR5) and faster gastric emptying (shorter T1/2) compared to the CS method. These physiological changes correlated with a higher incidence of early dumping symptoms, particularly abdominal symptoms, a tendency for greater weight loss, and an increased frequency of daily meals, and our findings are consistent with previous study (14).

The accelerated gastric emptying observed in the Delta group is likely due to two primary factors. First, the complete resection of the pyloric sphincter during distal gastrectomy removes a key regulatory mechanism responsible for modulating gastric emptying (19). Second, the Delta method creates a wider anastomotic stoma compared to the CS method (Fig. 1A, 1B), thereby decreasing outflow resistance and promoting more rapid transit of gastric contents into the duodenum (8, 19). Furthermore, in cases where the remnant stomach volume is small, intragastric pressure increases with a smaller amount of food intake, thereby amplifying the acceleration of gastric emptying (19).

Unlike differences in gastric emptying rates observed among various gastrectomy types—where the presence or absence of the pyloric sphincter is a primary determinant—our findings demonstrate that even after pyloric sphincter removal, variations in anastomotic technique significantly influence gastric motility and symptomatology within the same surgical procedure (LDGBI). This highlights the important role of anastomotic stoma size as an additional factor contributing to postoperative gastric emptying dynamics. As demonstrated in this study and previous reports (8, 14), such enhanced gastric emptying may result in the development of dumping symptoms and diarrhea. Among these, dumping symptoms are particularly prevalent among postgastrectomy patients and occur with considerable frequency (20). They are widely recognized as the most detrimental postoperative symptoms affecting quality of life (21), underscoring the critical need for preventive strategies to mitigate their impact.

In light of the observed correlation between the Delta method and accelerated gastric emptying, surgical modifications should be considered to mitigate these effects. One potential approach is to reduce the anastomotic stoma size to maintain a degree of outflow resistance while preserving the minimally invasive advantages of the Delta method. Alternatively, in patients with small remnant gastric volumes, Roux-en-Y reconstruction could be considered to prevent rapid gastric emptying. Furthermore, tailored postoperative dietary guidance and proactive symptom management strategies may improve long-term outcomes for patients undergoing Delta anastomosis.

This study offers critical insights into the long-term physiological outcomes associated with varying anastomotic techniques in LDGBI. However, several limitations must be acknowledged. First, the retrospective design and relatively small sample size limit the generalizability of our findings. Although our study was able to detect significant differences in key outcomes, the limited number of patients may affect the statistical power, and future prospective studies with larger cohorts are warranted to validate these findings. Second, the questionnaire utilized in this study was originally developed and has been routinely applied at our institution to assess outcomes after gastrectomy. Although formal validation has not been conducted, previous research (14) employing this instrument has revealed significant correlations between its items and objective measures of gastric function, thereby supporting its clinical relevance and applicability.

This study underscores the significant impact of anastomotic techniques on remnant stomach motor function and QOL following LDGBI. While the Delta method provides advantages in minimally invasive surgery, its association with accelerated gastric emptying and increased dumping symptoms highlights the need for careful patient selection and potential surgical modifications. Future studies should aim to refine anastomotic techniques that optimize both short-term recovery and long-term functional outcomes, ensuring improved postoperative QOL for patients undergoing gastrectomy.

Data Availability

All data are included in this published article.

Funding

This work was supported in part by grants from the High Technology Research Center Project for Private University and from Grants-in-Aid for Scientific Research (nos. 17590476 and 19590572) from the Ministry of Education, Culture, Sports, Science and Technology of Japan.

Conflict of Interest

The authors declare that they have no conflict of interest in association with the present study.