Smaller-Diameter Circular Stapler Has an Advantage in Billroth I Stapled Anastomosis After Laparoscopy-Assisted Distal Gastrectomy

Abstract

Introduction:

Billroth I gastroduodenostomy using a circular stapler is the most preferred reconstruction method after laparoscopy-assisted distal gastrectomy (LADG). The optimal stapler size for this procedure has not yet been proposed.

Methods:

Sixty-five patients who underwent LADG and stapled anastomosis with a 25-mm stapler (25-mm group) and a 29-mm stapler (29-mm group) were enrolled in this study. Clinical data and gastroscopic findings at 6 and 12 months after surgery were retrospectively reviewed.

Results:

Postoperative complications and postprandial symptoms were similar in both groups. Gastroscopically, food materials remained more frequently in the remnant stomach in the 25-mm group than in the 29-mm group at 6 months after surgery (P=.041). Gastritis and bile reflux were observed more frequently in the 29-mm group than in the 25-mm group (P=.012 and P=.015, respectively). All these differences in the gastroscopic findings between the two groups decreased at 12 months after surgery except for reflux esophagitis, which was observed more frequently in the 29-mm group (P=.002). The length of the incision was smaller in the 25-mm group than in the 29-mm group (4.39 cm versus 4.95 cm, P=.009).

Conclusion:

A small-diameter stapler is a risk factor for gastric stasis in the early postoperative period, whereas a large-diameter stapler is a risk factor for gastritis and bile reflux in the early postoperative period and for esophagitis in the late postoperative period. Thus, a small-diameter circular stapler has more advantages over a large-diameter circular stapler. It also enables a reliable anastomosis through a smaller incision and easy handling of the stapler during anastomosis.

Introduction

Billroth I gastroduodenostomy has been the procedure of choice for distal gastrectomy because it preserves normal bowel integrity and provides a better postoperative physiologic outcome.¹ The procedure is relatively simple in conventional open surgery, especially when circular stapling devices are used. However, it becomes more technically challenging when attempted laparoscopically, and some surgeons have advocated placement of the anvil and the suture extracorporeally after the duodenal stump has been exteriorized via minilaparotomy.

Most surgeons have a tendency to use a large stapler for this procedure because of the possible occurrence of anastomotic stricture or gastric stasis. However, the surgeon has to struggle to push a large stapler through a small incision, especially in the case of obese patients. Using a smaller stapler for this procedure seems to have some inherent advantages such as easy handling of the stapler or a cosmetic benefit, as per the expectations from a minimally invasive surgery.

In esophagectomy and stapled esophagogastrostomy, some reports have suggested that benign anastomotic stricture formation is significantly related to the size of the staple gun used.^2,3 However, the optimal stapler size for laparoscopy-assisted distal gastrectomy (LADG) reconstructed by Billroth I anastomosis has not yet been proposed. Hence, we compared the clinical symptoms and gastroscopic findings after Billroth I LADG on the basis of the stapler size and then evaluated the effect of diameter of the stapler on the clinical outcome of this anastomosis.

Patients and Methods

We retrospectively evaluated 65 patients who underwent Billroth I reconstruction after LADG between January 2007 and September 2009. The patients were classified retrospectively into two groups by the stapler size used for reconstructive procedures: a 25-mm group (14 patients) and a 29-mm group (51 patients). Only those patients with early gastric cancer were included in this study, as the indication for laparoscopic gastrectomy for gastric cancer was clinical stage T1N0 in our institute.

A five-trocar technique was used for laparoscopic procedures. The 11-mm trocar was introduced through an umbilical incision for a camera port, three 5-mm trocars were inserted in the right upper, left upper, and left lower abdomen, and a 12-mm trocar was inserted in right lower abdomen. In the reconstruction phase, a small midline upper abdominal incision 4–5 cm in length was made. The stomach was externalized through the incision, followed by duodenal resection with a purse-string clamp.

Mechanically stapled anastomosis was performed using 25-mm- or 29-mm-sized circular staplers (CDH 25 and 29, respectively; Ethicon Endo-surgery, Johnson & Johnson, Cincinnati, OH) with the anvil head being inserted into the cut end of the duodenum, and a purse-string suture with a 2-0 polypropylene (Prolene^®; Ethicon Endo-surgery) was placed from the cephalad position. The tip of the central rod pierced the greater curvature side of the posterior wall of the remnant stomach and was connected to the anvil head. The body of the circular stapler was inserted into the minilaparotomy incision. If the body of the stapler could not be inserted, an appropriate extension of the skin incision was made. Then, the stapler and anvil were removed after the stapler was fired. The anastomosis was inspected, and the gastric conduit opening was closed using an additional firing of a linear stapler (Autosuture™ Endo GIA™; Covidien, Mansfield, MA) with a seromuscular suture of 3-0 Vicryl^® (Ethicon, Johnson & Johnson, New Brunswick, NJ).

The perioperative clinical outcome of each patient was evaluated retrospectively by collecting data on operative time, time until oral intake, postoperative hospital stay, and anastomotic and general postoperative complications. Patients were followed up at the surgical outpatient clinic at 6 weeks, 3 months, and 6 months after surgery and thereafter at 6-month intervals. All patients were interviewed at 6 and 12 months after the surgery and were asked to answer questions about their condition, such as postprandial discomfort (stomach fullness, nausea, regurgitation). We analyzed the upper gastrointestinal endoscopic findings at 6 months and 1 year after surgery and evaluated the status of the remnant stomach regarding the development of esophagitis, gastritis, bile reflux, and residual food. These were not detected on the preoperative gastroscopy in all patients. As for the positive endoscopic findings correlated with stapler size, their relationship with clinicopathologic factors, such as age, sex, extent of lymph node dissection, stapler size, operative time, body mass index, and number of dissected lymph nodes, was assessed to verify whether some other contributory factors existed in addition to the stapler size.

The unpaired Student's t test was used for statistical analysis of the data. The chi-squared test was used to compare the parameters. Differences between the two groups with a P value of <.05 were considered statistically significant.

Results

Sixty-five consecutive patients (mean age, 58.7 years; range, 30–83 years) were offered LADG with Billroth I anastomosis using a circular stapler between January 2007 and September 2009. Demographic data, clinical characteristics, and pathologic staging are shown in Table 1. Median operative time was 263.1 minutes (range, 140–420 minutes). Proximal and distal margins were negative in all patients. The median number of lymph nodes dissected from each specimen was 28.2 (range, 4–74). No intraoperative technical failures of the anastomosis or deaths occurred. The median hospital stay was 11.4 days (range, 6–39 days).

Table 1.

Demographic and Clinicopathologic Characteristics of the 65 Patients with Early Gastric Cancer

Characteristic
Number of patients	65
Age (years)	58.7±13.4 (30–83)
Sex (men/women)	43/22
BMI (kg/m²)	23.2±3.1 (16.6–30.9)
Operative time (minutes)	263.1±74.5 (140–420)
Postoperative progress
Water permit (days)	3.9±0.9 (2–7)
Liquid diet (days)	4.7±0.9 (2–8)
Hospital stay (day)	11.35±4.9 (6–39)
Incision length (cm)	4.48±0.45 (4–6)
Stapler size
25-mm	14 (21.5%)
29-mm	51 (78.5%)
Anastomotic complications
Bleeding	2 (3.08%)
Tumor size (cm)	2.4±1.3 (0.2–6)
Number of retrieved lymph nodes	28.2±14.4 (4–74)
Depth of invasion
T1a	33 (46.5%)
T1b	21 (29.6%)
T2a	7 (9.9%)
LN metastasis
N0	57 (90.5%)
N1	6 (9.5%)
TNM stage
Ia	50 (76.9%)
Ib	11 (16.9%)
II	1 (1.5%)

BMI, body mass index.

The characteristics of the patients in the 25-mm and 29-mm groups are shown in Table 2. There were no significant differences in sex, age, body mass index, operative time, tumor size, tumor stage, and postoperative hospital stay. However, the length of the incision for minilaparotomy was significantly shorter in the 25-mm group than in the 29-mm group (4.39±0.4 cm versus 4.95±0.7 cm, P=.009). There was no anastomotic leakage or stricture that required surgical or interventional treatment. Two cases of anastomotic bleeding developed in the 29-mm group only and were managed nonoperatively.

Table 2.

Clinicopathologic Characteristics on the Basis of the Stapler Size

	Stapler size
	25-mm	29-mm	P value
Age (years)	58.64±13.4	58.67±13.5	.995
Sex (men/women)	9/5	34/17	1.000
BMI (kg/m²)	21.92±2.7	23.60±3.1	.074
Operative time (minutes)	250.93±72.7	266.47±75.4	.494
Tumor size (cm)	2.67±1.4	2.31±1.3	.398
Incision length (cm)	4.39±0.4	4.95±0.7	.009
T stage			.328
T1a	13	43
T1b, T2a	0	7
N stage			1.000
N0	12	46
N1	1	5
TNM stage			.431
Ia	12	39
Ib, II	1	11
LN dissection			.104
D1+α	2	19
D1+β, D2	12	32
Anastomotic bleeding	0/14	2/51	.613
Hospital stay (days)	10.6±4.0	11.6±5.1	.516

Patients interviewed were asked about postprandial discomfort; no significant differences were revealed between the 25-mm and 29-mm groups (35.7% versus 16.0%, P=.105; Table 3).

Table 3.

Postoperative Gastroscopic Findings on the Basis of the Stapler Size (25-mm Versus 29-mm)

	Stapler size
After surgery	25-mm	29-mm	P value
At 6 months
Postprandial discomfort	5/14 (35.7%)	8/50 (16.0%)	.105
Esophagitis	3/14 (21.4%)	19/50 (38.0%)	.249
Gastritis	2/14 (14.3%)	26/50 (52.0%)	.012
Bile reflux	0/14 (0.0%)	16/50 (32.0%)	.015
Food retention	9/14 (64.3%)	17/50 (34.0%)	.041
At 12 months
Postprandial discomfort	0/12 (0.0%)	6/49 (12.2%)	.202
Esophagitis	1/12 (8.3%)	28/48 (58.3%)	.002
Gastritis	2/12 (16.7%)	23/48 (47.9%)	.050
Bile reflux	3/12 (25.0%)	10/48 (20.8%)	0.754
Food retention	3/12 (25.0%)	10/48 (20.8%)	0.754

When the the remnant stomach was evaluated on the basis of the gastroscopic findings, the 25-mm group was associated with a significantly higher incidence of residual food compared with the 29-mm group at 6 months after surgery (P=.041). A significant difference was seen in the incidence of remnant gastritis and bile reflux between the two groups, resulting in the preference for the 25-mm stapler at 6 months after surgery; the incidence of gastritis was 14.3% versus 52.0% (P=.012), and the incidence of bile reflux was 0.0% versus 32.0% (P=.015) in the 25-mm and 29-mm groups, respectively. As a prolonged outcome, the amount of differences in the gastroscopic findings between the two groups decreased in most of the parameters at 12 months after surgery. Still, remnant gastritis was frequently observed in the 29-mm group (16.7% versus 47.9%, P=.050), and several new cases of esophagitis were detected in the 29-mm group (8.3% versus 58.3%, P=.002).

There were no patients who required hospitalization or conversion surgery to Roux-en-Y revision due to these problems.

According to our investigation about some of the clinicopathologic factors that can influence the postoperative gastroscopic findings, bile reflux was related to age and a more advanced cancer stage at 6 months after surgery (P=.027 and P=.033, respectively; Table 4). Otherwise, stapler size was the only significant factor affecting the postoperative gastroscopic findings.

Table 4.

Factors Influencing the Postoperative Gastroscopic Findings

	Food retention (6 months)			Gastritis (6 months)			Bile reflux (6 months)			Esophagitis (12 months)
	Yes	No	P value	Yes	No	P value	Yes	No	P value	Yes	No	P value
Age (years)	60.2±11.4	56.8±13.2	.407	60.3±11.8	56.7±14.1	.277	64.3±11.9	56.3±13.0	.033	58.7±12.9	56.4±12.8	.486
Sex (women/men)	11/15	10/28	.181	6/22	15/21	.087	5/11	16/32	.878	10/19	10/21	.855
BMI (kg/m²)	22.7±3.4	23.5±2.9	.423	23.9±2.9	22.9±3.2	.225	23.0±3.6	23.4±2.9	.645	23.5±3.3	23.3±2.9	.814
Stage (Ia/Ib, II)	21/5	31/7	.935	22/6	30/6	.628	10/6	42/6	.027	22/7	26/5	.438
Lymph node dissection
>D1+β or not	20/6	24/14	.243	20/8	24/12	.683	9/7	35/13	.213	20/9	21/10	.919
Number	29.1±10.2	28.2±16.9	.334	29.3±14.5	28.1±14.6	.747	25.8±12.6	29.6±15.0	.367	29.6±15.2	26.9±14.3	.487
Stapler size (25-mm/29-mm)	9/17	5/33	.041	2/26	12/24	.012	0/16	14/34	.015	1/28	11/20	.002

Discussion

In this study, we evaluated the results of the 25-mm- and 29-mm-sized mechanical staplers used for gastroduodenostomy procedures in patients undergoing LADG for early gastric cancer. We found that the clinical outcomes, including the prevalence of anastomotic problems, were also equal in both groups. An evaluation of the postoperative remnant gastric status revealed that there was a significantly higher incidence of residual food, but a lower incidence of gastritis or bile reflux, at 6 months after surgery and a lower incidence of esophagitis at 12 months after surgery in the 25-mm group compared with the 29-mm group.

In esophagogastric anastomosis, Griffin et al.⁴ reported a significantly higher stricture rate with the EEA25 stapler compared with the EEA28 according to chi-squared test (P<.001). Although this procedure is not performed for malignancy, in gastrojejunostomy in laparoscopic Roux-en-Y gastric bypass using a circular stapler, Nguyen et al.⁵ showed a significant drop in stricture rate with the use of a 25-mm circular stapler instead of a 21-mm circular stapler (from 26.8% to 8.8%) in a nonrandomized study. As for Billroth I reconstruction with distal gastrectomy, Takahashi et al.⁶ retrospectively compared the clinical outcomes of mechanically stapled anastomosis and hand-sutured anastomosis techniques; the study showed equivalent quality between mechanically stapled anastomosis and hand-sutured anastomosis procedures, with comparable anastomotic complications and status of the remnant stomach. However, to the best of our knowledge, regarding the stapler size for Billroth I gastroduodenostomy, no study has been performed to compare the clinical outcomes for each stapler size.

On endoscopy at 6 months, the patients in whom the anastomosis was performed using a 25-mm stapler had a larger amount of residual food in the remnant stomach. However, on endoscopy at 1 year, most of these patients did not have more residual food in the remnant stomach. Physiological gastric emptying and motility of the digestive system are complex processes that are controlled and regulated by complicated physiological mechanisms. Tonic contractions of the proximal stomach are important for the transfer of liquid food from the stomach to the duodenum,⁷ whereas peristaltic contractions of the distal stomach are of primary importance for reducing the size of the solid food particles and for the transfer of solid food to the duodenum.⁸ Consequently, as in another study on gastric stasis after distal gastrectomy, gastric emptying of the liquid diet was significantly faster in the patients who had undergone distal gastrectomy compared with that in control subjects, and, for the semisolid diet, the gastric emptying rate in patients who had undergone distal gastrectomy was significantly slower than that in the control group.⁹

Food stasis associated with Billroth I stapled anastomosis is associated with several factors, including gastric motility and the location of the anastomosis, creating a sharp angle between the remnant stomach and the duodenum. Gastric motility after gastrectomy is associated with the length of preserved duodenum (preservation of the duodenal pacemaker, which is located 0.5–1 cm distally from the pylorus)¹⁰ or pacemaker in the gastric remnant (size of remnant stomach) and preservation of the celiac branch of the vagus nerve.¹¹ In this study, even though these factors were not checked by a measurable tool, they were almost completely controlled because the study was conducted by a single surgeon. We tentatively add the stapler size as a temporary contributing factor to gastric stasis after stapled distal gastrectomy.

Slow emptying of a semisolid diet in patients after distal gastrectomy is thought to contribute to the sensation of epigastric fullness after meals, and fast gastric emptying of a liquid diet in these patients may be related to the early dumping syndrome. We only checked for gross discomfort in patients after surgery. However, a detailed questionnaire and description of symptoms such as changes in appetite, gastric fullness, symptoms of reflux esophagitis (heartburn, dyspepsia, regurgitation, dysphagia), symptoms of early dumping syndrome (palpation, dizziness, weakness, flushing, diaphoresis, nausea, abdominal pain, bloating, diarrhea), and changes in body weight would provide us with a better understanding specifically on whether delayed emptying, early dumping syndrome, or esophagogastritis is predominant in such cases.

Looking into the issue of anastomotic stricture, reported in a circular stapled gastrojejunostomy, some factors like Helicobacter pylori, bile salts, higher number of stapler rows, and tissue injury^12,13 have been linked with an increasing stricture rate, although there was no episode of development of anastomotic stricture in this study.

Delayed gastric emptying is mostly a self-limited entity, if it is not accompanied by severe anastomotic stenosis. The reoperation rate in patients experiencing delayed gastric emptying as a postoperative complication is extremely low.¹⁴ Gastric emptying recovers gradually during a period of weeks to months, and it mostly recovered within 1 year in this study, and only a minority of cases sustained prolonged clinical symptoms postoperatively.

As might be expected, the degree of residual gastritis was significantly lower in the 25-mm group than that in the 29-mm group, probably owing to the reduced reflux of duodenal juice. Kojima et al.¹⁵ reported that, in LADG, Roux-en-Y reconstruction seems superior to Billroth I reconstruction for preventing both postoperative complications and bile reflux into the gastric remnant, and the duodenogastric reflux is considered the main cause of various symptoms after gastrectomy that adversely affect quality of life for patients, even if Billroth I reconstruction has been applied after LADG as the standard in Japan. Thus, anastomosis using smaller-sized staplers in LADG with Billroth I reconstruction might reduce these drawbacks.

The reflux of bile or pancreatic juice into the gastric remnant may increase the risk of carcinogenesis through remnant mucosal cell damage or acceleration of cell proliferation in the gastric mucosa.^16,17 In this respect, a larger-sized anastomosis may engender a higher prevalence rate for secondary gastric cancer after a long period than a smaller-sized anastomosis. However, this issue should be considered from various viewpoints, and further studies on this issue are needed.

In this study, we investigated the endoscopic findings at 6 months and 1 year after surgery and attempted to elucidate not only their temporal condition, but also their time trends. In the endoscopic findings at 1 year, increased incidence of esophagitis in the 29-mm group caught our attention. Reflux of duodenal contents into the esophagus was thought to be strongly associated with the genesis of esophagitis. The antireflux function at the gastroesophageal junction has been shown to be deteriorated by anatomic changes and denervation caused by distal gastrectomy and lymph node dissection.¹⁸ It is interesting that the difference in the amount of the reflux into the esophagus was not caused by the patency of the esophagogastric junction, but was mostly caused by the difference in the amount of reflux into the gastric remnant.¹⁹

Endoscopic findings had been evaluated after distal gastrectomy with respect to their relationship with the reconstruction method or suture technique used before.^15,20 However, there are no known influencing clinicopathologic factors related to endoscopic findings in a fixed anastomosis method. We found that at 6 months after surgery, bile reflux correlated not only with stapler size but also with advanced age and cancer stage. Because bile reflux is related to personal diet-related behavior, we thought that in cases where the diet contains even a modest amount of fat or exercise after eating, advanced age might be an influencing factor. Concerning the cancer stage, we routinely perform more intensive lymph node dissection in patients with advanced gastric cancer. Although in this study no relationship between endoscopic findings and extent of lymph node dissection was revealed, because we studied patients in the preoperative clinical stage T1N0, it is likely that a comparison between advanced and early gastric cancer may show some difference on endoscopic findings based on lymph node dissection. Similarly, Nunobe et al.²¹ reported that preservation of vagus nerve and infrapyloric blood flow induces less stasis in laparoscopy-assisted pylorus-preserving gastrectomy. However, because these factors (i.e., advanced age and cancer stage) showed no correlation or continuity with later or the other endoscopic findings, we think that the stapler size is the most important factor with an influence on the residual stomach after laparoscopic stapled gastroduodenostomy.

Handling of small-sized staplers is easy, and smaller-sized Billroth I anastomosis results in lower incidence of bile reflux and gastritis in the remnant stomach. Because we consider laparoscopic surgery as a surgical technique with cosmetic advantages, a possible smaller incision with the 25-mm stapler is definitely an advantage. Furthermore, we confirmed that there was no increase in the stricture rate with the 25-mm-sized stapler used in this study. We also confirmed from previous reports that a diameter of 25 mm is sufficient for Billroth I anastomosis.²² However, food stasis in the early postoperative period was distinct in the 25-mm group in this study. Hence, further studies on food intake and nutritional parameters (body weight, serum albumin, total cholesterol) should be performed in this postoperative period. The role of some prokinetic agents, whether preventive or therapeutic, in the management of delayed gastric emptying and food stasis in this condition remains controversial. We may consider that some medications like erythromycin, the only regimen studied inside the scope of randomized controlled trials, might aid to improve the stasis, the only drawback of the smaller-sized stapling technique for Billroth I anastomosis.²³

This study had some limitations such as a small sample size, short follow-up period, and a lack of some other tools to visualize the measurable time for gastric emptying such as the radioisotope method or acetaminophen method. We need to follow up these patients for a longer postoperative period (of 2 years or more) and compare those results with the results of this study.

In conclusion, our data suggest that the smaller-diameter circular stapler has advantages over the larger-diameter circular stapler in Billroth I stapled anastomosis. Further studies are necessary to reveal the real advantages and disadvantages of these two stapling tools. Further detailed studies on these patients will enable the development of more rational surgical techniques and provide benefit to the patients undergoing surgery for gastric cancer.

Footnotes

Disclosure Statement

No competing financial interests exist.

References

Loffeld

. Prevalence of upper abdominal complaints in patients who have undergone partial gastrectomy. Can J Gastroenterol, 2000; 14:681–684.

Dresner

, Lamb

, Wayman

, Hayes

, Griffin

. Benign anastomotic stricture following transthoracic subtotal oesophagectomy and stapled oesophago-gastrostomy: risk factors and management. Br J Surg, 2000; 87:362–373.

Berrisford

, Page

, Donnelly

. Stapler design and strictures at the esophagogastric anastomosis. J Thorac Cardiovasc Surg, 1996; 111:142–146.

Griffin

, Woods

, Chan

, Chung

, Li

. Early and late surgical complications of subtotal oesophagectomy for squamous carcinoma of the oesophagus. J R Coll Surg Edinb, 1991; 36:170–173.

Nguyen

, Stevens

, Wolfe

. Incidence and outcome of anastomotic stricture after laparoscopic gastric bypass. J Gastrointest Surg, 2003; 7:997–1003discussion 1003.

Takahashi

, Saikawa

, Yoshida

, Otani

, Kubota

, Kumai

, Kitajima

. Mechanical-stapled versus hand-sutured anastomoses in Billroth-I reconstruction with distal gastrectomy. Surg Today, 2007; 37:122–126.

Azpiroz

. Control of gastric emptying by gastric tone. Dig Dis Sci, 1994; 39,12 Suppl:18S–19S.

Haba

, Sarna

. Regulation of gastroduodenal emptying of solids by gastropyloroduodenal contractions. Am J Physiol, 1993; 264:G261–G271.

Tomita

, Fujisaki

, Tanjoh

. Pathophysiological studies on the relationship between postgastrectomy syndrome and gastric emptying function at 5 years after pylorus-preserving distal gastrectomy for early gastric cancer. World J Surg, 2003; 27:725–733.

10.

Tanaka

, Sarr

. Total duodenectomy: Effect on canine gastrointestinal motility. J Surg Res, 1987; 42:483–493.

11.

Ando

, Tsuji

. Surgical technique of vagus nerve-preserving gastrectomy with D2 lymphadenectomy for gastric cancer. A N Z J Surg, 2008; 78:172–176.

12.

Kaplan

. Gastrointestinal management of the bariatric surgery patient. Gastroenterol Clin North Am, 2005; 34:105–125.

13.

Pope

, Goodney

, Burchard

, Proia

, Olafsson

, Lacy

, Burrows

. Peptic ulcer/stricture after gastric bypass: A comparison of technique and acid suppression variables. Obes Surg, 2002; 12:30–33.

14.

Jimenez

, Fernandez-del Castillo

, Rattner

, Chang

, Warshaw

. Outcome of pancreaticoduodenectomy with pylorus preservation or with antrectomy in the treatment of chronic pancreatitis. Ann Surg, 2000; 231:293–300.

15.

Kojima

, Yamada

, Inokuchi

, Kawano

, Sugihara

. A comparison of Roux-en-Y and Billroth-I reconstruction after laparoscopy-assisted distal gastrectomy. Ann Surg, 2008; 247:962–967.

16.

Byrne

, Attwood

. Duodenogastric reflux and cancer. Hepatogastroenterology, 1999; 46:74–85.

17.

Sugiyama

, Sohma

, Ozawa

, Hada

, Mikami

, Konn

, Ono

. Regurgitant bile acids and mucosal injury of the gastric remnant after partial gastrectomy. Am J Surg, 1987; 153:399–403.

18.

Abe

. [Experimental and clinical studies on lower esophageal sphincter motor function with special reference to the influence of vagal denervation] J Smooth Muscle Res, 1994; 30:97–110.

19.

Fukuhara

, Osugi

, Takada

, Takemura

, Higashino

, Kinoshita

. Reconstructive procedure after distal gastrectomy for gastric cancer that best prevents duodenogastroesophageal reflux. World J Surg, 2002; 26:1452–1457.

20.

Nagano

, Ohyama

, Sakamoto

, Ohta

, Yamaguchi

, Muto

, Yamaguchi

. The endoscopic evaluation of gastritis, gastric remnant residue, and the incidence of secondary cancer after pylorus-preserving and transverse gas-trectomies. Gastric Cancer, 2004; 7:54–59.

21.

Nunobe

, Hiki

, Fukunaga

, Tokunaga

, Ohyama

, Seto

, Yamaguchi

. Laparoscopy-assisted pylorus-preserving gastrectomy: Preservation of vagus nerve and infrapyloric blood flow induces less stasis. World J Surg, 2007; 31:2335–1240.

22.

Kobayashi O

. Billroth I method reconstruction surgery by use of instruments after pyloric side gastrectomy. Shujutsu, 1997; 50:1337–1344.

23.

Yeo

, Barry

, Sauter

, Sostre

, Lillemoe

, Pitt

, Cameron

. Erythromycin accelerates gastric emptying after pancreaticoduodenectomy. A prospective, randomized, placebo-controlled trial. Ann Surg, 1993; 218:229–237discussion 237–238.