Background and study aims: Endoscopic submucosal dissection (ESD) may cause excessive duodenogastric reflux
(DGR) in a similar manner to distal gastrectomy, particularly after antral resections.
We aimed to examine the occurrence of DGR after ESD.
Patients and methods: Patients with gastric neoplasm for whom ESD was indicated were categorized according
to lesion site: the antral group (lower [L] stomach, n = 46) and the nonantral group
(upper or middle [U or M] stomach, n = 49). Endoscopy was performed before ESD, the
day after ESD, and 3 months after ESD, and the fasting bile acid concentration (BAC)
in the gastric juice was analyzed.
Results: BAC values showed significant interaction between time point and group, although
this association differed in the antral and nonantral groups. BACs on the day after
ESD were higher in the antral group than in the nonantral group, but not the pre-ESD
and 3 months post-ESD levels. In the antral group only, fasting BACs increased significantly
the day after ESD and decreased to baseline levels 3 months post-ESD. There was also
a correlation between BAC and lesion location in the antral subgroups, with significantly
higher BACs found the day after ESD in patients with lesser curvature lesions.
Conclusions: ESD of lesions in the antral lesser curvature may lead to a transient early increase
in DGR. However, ESD does not result in long-term DGR, a factor that is known to increase
the risk of carcinogenesis following gastrectomy.
References
- 1
Bechi P, Amorosi A, Mazzanti R. et al .
Gastric histology and fasting bile reflux after partial gastrectomy.
Gastroenterology.
1987;
93
335-343
- 2
Orlando 3rd R.
, Welch JP. Carcinoma of the stomach after gastric operation.
Am J Surg.
1981;
141
487-491
- 3
Caygill C P, Hill M J, Kirkham J S, Northfield T C.
Mortality from gastric cancer following gastric surgery for peptic ulcer.
Lancet.
1986;
1
929-931
- 4
Toftgaard C.
Gastric cancer after peptic ulcer surgery. A historic prospective cohort investigation.
Ann Surg.
1989;
210
159-164
- 5
Lundegårdh G, Adami H O, Helmick C. et al .
Stomach cancer after partial gastrectomy for benign ulcer disease.
N Engl J Med.
1988;
319
195-200
- 6
Miwa K, Segawa M, Takano Y. et al .
Induction of oesophageal and forestomach carcinomas in rats by reflux of duodenal
contents.
Br J Cancer.
1994;
70
185-189
- 7
Lacaine F, Houry S, Huguier M.
Stomach cancer after partial gastrectomy for benign ulcer disease. A critical analysis
of epidemiological reports.
Hepatogastroenterology.
1992;
39
4-8
- 8
Dvorak K, Chavarria M, Payne C M. et al .
Activation of the interleukin-6/STAT3 antiapoptotic pathway in esophageal cells by
bile acids and low pH: relevance to Barrett’s esophagus.
Clin Cancer Res.
2007;
13
5305-5313
- 9
Song S, Guha S, Liu K. et al .
COX-2 induction by unconjugated bile acids involves reactive oxygen species-mediated
signalling pathways in Barrett’s oesophagus and oesophageal adenocarcinoma.
Gut.
2007;
56
1512-1521
- 10
Hu Y, Jones C, Gellersen O. et al .
Pathogenesis of Barrett esophagus: deoxycholic acid up-regulates goblet-specific gene
MUC2 in concert with CDX2 in human esophageal cells.
Arch Surg.
2007;
142
540-544
- 11
Dvorak K, Payne C M, Chavarria M. et al .
Bile acids in combination with low pH induce oxidative stress and oxidative DNA damage:
relevance to the pathogenesis of Barrett’s oesophagus.
Gut.
2007;
56
763-771
- 12
Kazumori H, Ishihara S, Rumi M A. et al .
Bile acids directly augment caudal related homeobox gene Cdx2 expression in oesophageal
keratinocytes in Barrett’s epithelium.
Gut.
2006;
55
16-25
- 13
Nishijima K, Miwa K, Miyashita T. et al .
Impact of the biliary diversion procedure on carcinogenesis in Barrett’s esophagus
surgically induced by duodenoesophageal reflux in rats.
Ann Surg.
2004;
240
57-67
- 14
Jang T J, Min S K, Bae J D. et al .
Expression of cyclooxygenase 2, microsomal prostaglandin E synthase 1, and EP receptors
is increased in rat oesophageal squamous cell dysplasia and Barrett’s metaplasia induced
by duodenal contents reflux.
Gut.
2004;
53
27-33
- 15
Zaninotto G, Portale G, Parenti A. et al .
Role of acid and bile reflux in development of specialised intestinal metaplasia in
distal oesophagus.
Dig Liver Dis.
2002;
34
251-257
- 16
Dixon M F, Neville P M, Mapstone N P. et al .
Bile reflux gastritis and Barrett’s oesophagus: further evidence of a role for duodenogastro-oesophageal
reflux?.
Gut.
2001;
49
359-363
- 17
Menges M, Müller M, Zeitz M.
Increased acid and bile reflux in Barrett’s esophagus compared to reflux esophagitis,
and effect of proton pump inhibitor therapy.
Am J Gastroenterol.
2001;
96
331-337
- 18
Miyashita T, Ohta T, Fujimura T. et al .
Duodenal juice stimulates oesophageal stem cells to induce Barrett’s oesophagus and
oesophageal adenocarcinoma in rats.
Oncol Rep.
2006;
15
1469-1475
- 19
Sousa J E, Troncon L E, Andrade J I, Ceneviva R.
Comparison between Henley jejunal interposition and Roux-en-Y anastomosis as concerns
enterogastric biliary reflux levels.
Ann Surg.
1988;
208
597-600
- 20
Morii Y, Arita T, Shimoda K. et al .
Jejunal interposition to prevent postgastrectomy syndromes.
Br J Surg.
2000;
87
1576-1579
- 21
Mathias J R, Fernandez A, Sninsky C A. et al .
Nausea, vomiting, and abdominal pain after Roux-en-Y anastomosis: motility of the
jejunal limb.
Gastroenterology.
1985;
88
101-107
- 22
Woodward A, Sillin L F, Wojtowycz A R, Bortoff A.
Gastric stasis of solids after Roux gastrectomy: is the jejunal transection important?.
J Surg Res.
1993;
55
317-322
- 23
Gotoda T, Yanagisawa A, Sasako M. et al .
Incidence of lymph node metastasis from early gastric cancer: estimation with a large
number of cases at two large centers.
Gastric Cancer.
2000;
3
219-225
- 24
Ono H, Kondo H, Gotoda T. et al .
Endoscopic mucosal resection for treatment of early gastric cancer.
Gut.
2001;
48
225-229
- 25
Ahmad N A, Kochman M L, Long W B. et al .
Efficacy, safety, and clinical outcomes of endoscopic mucosal resection: a study of
101 cases.
Gastrointest Endosc.
2002;
55
390-396
- 26
Inoue H, Takeshita K, Hori H. et al .
Endoscopic mucosal resection with a cap-fitted panendoscope for esophagus, stomach,
and colon mucosal lesions.
Gastrointest Endosc.
1993;
39
58-62
- 27
Torii A, Sakai M, Kajiyama T. et al .
Endoscopic aspiration mucosectomy as curative endoscopic surgery; analysis of 24 cases
of early gastric cancer.
Gastrointest Endosc.
1995;
42
475-479
- 28
Suzuki Y, Hiraishi H, Kanke K. et al .
Treatment of gastric tumors by endoscopic mucosal resection with a ligating device.
Gastrointest Endosc.
1999;
49
192-199
- 29
Tanabe S, Koizumi W, Kokutou M. et al .
Usefulness of endoscopic aspiration mucosectomy as compared with strip biopsy for
the treatment of gastric mucosal cancer.
Gastrointest Endosc.
1999;
50
819-822
- 30
Ono H, Kondo H, Gotoda T. et al .
Endoscopic mucosal resection for treatment of early gastric cancer.
Gut.
2001;
48
225-229
- 31
Gotoda T, Kondo H, Ono H. et al .
A new endoscopic mucosal resection procedure using an insulation-tipped electrosurgical
knife for rectal flat lesions: report of two cases.
Gastrointest Endosc.
1999;
50
560-563
- 32
Yamamoto H, Kawata H, Sunada K. et al .
Successful en-bloc resection of large superficial tumors in the stomach and colon
using sodium hyaluronate and small-caliber-tip transparent hood.
Endoscopy.
2003;
35
690-694
- 33
Oka S, Tanaka S, Kaneko I. et al .
Advantage of endoscopic submucosal dissection compared with EMR for early gastric
cancer.
Gastrointest Endosc.
2006;
64
877-883
- 34
Rösch T, Sarbia M, Schumacher B. et al .
Attempted endoscopic en bloc resection of mucosal and submucosal tumors using insulated-tip
knives: a pilot series.
Endoscopy.
2004;
36
788-801
- 35
The Paris endoscopic classification of superficial neoplastic lesions: esophagus,
stomach, and colon: November 30 to December 1, 2002.
Gastrointest Endosc.
2003;
58
S3-S43
- 36
Schlemper R J, Riddell R H, Kato Y. et al .
The Vienna classification of gastrointestinal epithelial neoplasia.
Gut.
2000;
47
251-255
- 37
Dixon M F.
Gastrointestinal epithelial neoplasia: Vienna revisited.
Gut.
2002;
51
130-131
- 38
Japanese Gastric Cancer Association .
Japanese Classification of Gastric Carcinoma, 2nd English Edition.
Gastric Cancer.
1998;
1
10-24
- 39
Schindlbeck N E, Heinrich C, Stellaard F. et al .
Healthy controls have as much bile reflux as gastric ulcer patients.
Gut.
1987;
28
1577-1583
- 40
Rhodes J, Barnardo D E, Phillips S F. et al .
Increased reflux of bile into the stomach in patients with gastric ulcer.
Gastroenterology.
1969;
57
241-252
- 41
Sobala G M, King R F, Axon A T, Dixon M F.
Reflux gastritis in the intact stomach.
J Clin Pathol.
1990;
43
303-306
- 42
Müller-Lissner S A.
Measurements of bile salt reflux are influenced by the method of collecting gastric
juice.
Gastroenterology.
1985;
89
1338-1341
- 43
Bechi P, Pucciani F, Baldini F. et al .
Long-term ambulatory enterogastric reflux monitoring. Validation of a new fiberoptic
technique.
Dig Dis Sci.
1993;
38
1297-1306
- 44
Caldwell M T, Byrne P J, Brazil N. et al .
An ambulatory bile reflux monitoring system: an in vitro appraisal.
Physiol Meas.
1994;
15
57-65
- 45
Vaezi M F, Lacamera R G, Richter J E.
Validation studies of Bilitec 2000: an ambulatory duodenogastric reflux monitoring
system.
Am J Physiol.
1994;
267
G1050-G1057
- 46
Oda I, Gotoda T, Hamanaka H. et al .
Endoscopic submucosal dissection for early gastric cancer: Technical feasibility,
operation time and complications from a large consecutive series.
Dig Endosc.
2005;
17
54-58
- 47
Heddle R, Collins P J, Dent J. et al .
Motor mechanisms associated with slowing of the gastric emptying of a solid meal by
an intraduodenal lipid infusion.
J Gastroenterol Hepatol.
1989;
4
437-447
- 48
Heddle R, Dent J, Toouli J, Read N W.
Topography and measurement of pyloric pressure waves and tone in humans.
Am J Physiol.
1988;
255
G490-G497
- 49
Schulze-Delrieu K, Wall J P.
Determinants of flow across isolated gastroduodenal junctions of cats and rabbits.
Am J Physiol.
1983;
245
G257-G264
- 50
Byrne J P, Romagnoli R, Bechi P. et al .
Duodenogastric reflux of bile in health: the normal range.
Physiol Meas.
1999;
20
149-158
- 51
Gowen G F.
Spontaneous enterogastric reflux gastritis and esophagitis.
Ann Surg.
1985;
201
170-175
- 52
Black R B, Hole D, Rhodes J.
Bile damage to the gastric mucosal barrier: the influence of pH and bile acid concentration.
Gastroenterology.
1971;
61
178-184
- 53
Gadacz T R, Zuidema G D.
Bile acid composition in patients with and without symptoms of postoperative reflux
gastritis.
Am J Surg.
1978;
135
48-52
- 54
Gillen P, Keeling P, Byrne P J. et al .
Implication of duodenogastric reflux in the pathogenesis of Barrett’s oesophagus.
Br J Surg.
1988;
75
540-543
- 55
Onozato Y, Ishihara H, Iizuka H. et al .
Endoscopic submucosal dissection for early gastric cancers and large flat adenomas.
Endoscopy.
2006;
38
980-986
- 56
Adachi Y, Shiraishi N, Shiromizu A. et al .
Laparoscopy-assisted Billroth I gastrectomy compared with conventional open gastrectomy.
Arch Surg.
2000;
135
806-810
- 57
Kitano S, Shiraishi N, Fujii K. et al .
A randomized controlled trial comparing open vs laparoscopy-assisted distal gastrectomy
for the treatment of early gastric cancer: an interim report.
Surgery.
2002;
131
S306-S311
- 58
Reyes C D, Weber K J, Gagner M, Divino C M.
Laparoscopic vs open gastrectomy. A retrospective review.
Surg Endosc.
2001;
15
928-931
- 59
Shimizu S, Uchiyama A, Mizumoto K. et al .
Laparoscopically assisted distal gastrectomy for early gastric cancer: is it superior
to open surgery?.
Surg Endosc.
2000;
14
27-31
- 60
Yano H, Monden T, Kinuta M. et al .
The usefulness of laparoscopy-assisted distal gastrectomy in comparison with that
of open distal gastrectomy for early gastric cancer.
Gastric Cancer.
2001;
4
93-97
- 61
Hayashi H, Ochiai T, Shimada H, Gunji Y.
Prospective randomized study of open versus laparoscopy-assisted distal gastrectomy
with extraperigastric lymph node dissection for early gastric cancer.
Surg Endosc.
2005;
19
1172-1176
- 62
Adachi Y, Suematsu T, Shiraishi N. et al .
Quality of life after laparoscopy-assisted Billroth I gastrectomy.
Ann Surg.
1999;
229
49-54
K. MiyakeMD PhD
Department of Internal Medicine, Division of Gastroenterology
Nippon Medical School
1-1-5 Sendagi, Bunkyo-ku,
Tokyo 113-8603
Japan
Fax: +81-3-56851793
eMail: km366@nms.ac.jp