Analysis of Cell Proliferation in Endoscopically Biopsied Specimens of Stomal Mucosa of the Gastric Remnant

Abstract: Carcinoma of the gastric remnant is thought to occur more commonly in the stomal than in the other areas, particularly following Billroth II surgery (BII). An attempt was made to determine the status of cell kinetics in the gastric remnant using endoscopically biopsied specimens, with assay of ornithine decarboxylase (ODC) activity and flow cytometric analysis of the cell cycle parameters. Fifty-two partially gastrectomized patients were studied. Significantly higher ODC activity was recognized in the stomal mucosa than in the greater curvature; this difference was especially pronounced for the group of BII patients. The S-phase cell percentage was also significantly higher in the stomal area than in the greater curvature; this was particularly so in the patients who had undergone BII 5 or more years prior to this study. Our results suggest that activation of cell proliferation is present in the stomal area of the gastric remnant following BII surgery. This activation increased with time following surgery. Activation of cell proliferation occurred in association with histological changes in the stomal glands, and may play a role in carcinogenesis within the gastric remnant.     

A Histologic Study of Endoscopic Biopsies of the Gastric Remnant Mucosa Following Subtotal Gastrectomy,with Special Reference to Changes of the Stomal Mucosa

Abstract: Endoscopic biopsy specimens of the remnant gastric mucosa (and of the stomal mucosa in particular) were investigated in 219 patients who had received subtotal gastrectomy for gastric cancer. Dilated glandular lumina (glandular dilatation) and curved ducts (irregular glandular structure) were detected significantly more freguently in the group gastrectomized long before, or by Billroth II resection, than in those treated recently, or by Billroth I resection. DNA histograms showed a distribution of epithelial cells from the remnant gastric mucosa which was somewhat different from the normal histogram. The occurrence rates of polyploid cells were significantly higher than normal, and tended to increase in the same individuals with advancing time after gastrectomy. These observations suggested that the pavticulav environments of the gastric remnant might have nonphvsiologic influences upon the gastric mucosa, although further studies are essential for the clarification of the possible relationship of these environments to oncogenesis in the remnant stomach.     

Proliferation assay of human gastric remnant by bromodeoxyuridine and flow cytometry.

The cell kinetics of gastric epithelium were studied by bromodeoxyuridine (BrdU) and flow cytometry in seven patients with remnant stomachs reconstructed with a Billroth type II procedure and in 25 patients with whole stomachs. Each patient received an intravenous injection of BrdU (200 mg/m2) 6 hours before surgery. Fresh specimens obtained from the lesser curvature, greater curvature, and stomal areas in the cases of remnant stomachs and from the antrum and fundus in the case of whole stomachs were studied. The BrdU labeling index was higher in the stomal area of the gastric remnant than in other areas, and DNA synthesis time was shortened in the stomal area of the gastric remnant (P less than 0.01) but not in other areas. The turnover time of the mucosa in the stomal area was 4.1 +/- 1.2 days, significantly shorter (P less than 0.01) than in other areas (7.6 +/- 2.3 to 8.2 +/- 1.2 days). The present study showed that the cell proliferation was extremely rapid in the stomal area of the gastric remnant, suggesting that this enhanced turnover of epithelial cells may assist in promoting carcinogenesis in the stomal area of the gastric remnant.     

Effects of bile reflux and intragastric microflora changes on lesions of remnant gastric mucosa after gastric operation

AIM: To investigate the effects of bile reflux and intragastric microflora changes on lesions of remnant gastric mucosa after gastric operation. METHODS: Concentration of bile acid and total bacterial counts (TBC) in gastric juice were measured in 49 patients with peptic ulcer before and after gastrectomy. One year after the operation, sample of gastric mucosa taken from all the patients were used for histological examination. RESULTS: The concentration of gastric bile acid was significantly increased in group B-I, or B-II and SV+A than that in group HSV (P<0.05-0.01). The abnormal histological changes in the remnant gastric mucosa were more common in the first 2 groups than in the last group. CONCLUSION: The type of gastrectomy can affect bile reflux. The abnormal histological changes in the remnant gastric mucosa are closely related to the elevation of bile acid concentration and increase of TBC in gastric juice. HSV can effectively prevent bile reflux and keep the gastric physiological functions stable.     

Influence of bile reflux and Helicobacter pylori infection on gastritis in the remnant gastric mucosa after distal gastrectomy

Background Two main pathogenic factors, bile reflux and Helicobacter pylori infection, have been identified in the remnant stomach, but it is still unclear which factor is important in the pathogenesis of gastritis in the remnant stomach after distal gastrectomy.Methods In 184 patients who had had distal gastrectomy performed using the Billroth-I procedure (B-I; n-106), Billroth-II procedure (B-II; n-36), and jejunal interposition (J-I; n-42) we examined the severity of remnant gastritis endoscopically and carried out examinations for H. pylori infection and histological examination.Results The endoscopic severity of remnant gastritis was grade 1 or more in 101 of the 106 B-I patients (95.3%) and in all 36 B-II patients (100%). But, of the 42 J-I patients, the grade was 0 in 33 (78.6%). The endoscopic severity of remnant gastritis was significantly milder for J-I than for B-I (P < 0.001) and B-II (P < 0.001). H. pylori infection was confirmed in 59 of the 106 B-I patients (55.6%), 21 of the 36 B-II patients (58.3%), and 32 of the 42 J-I patients (76.1%). The rate of H. pylori infection was higher for J-I patients than for B-I (P < 0.05), but not for B-II patients (P = 0.1495). The severity of chronic and active inflammatory cellular infiltration tended to be inverse proportional relation with the endoscopic severity of the remnant gastritis. Furthermore, the histological inflammation and activity scores of H. pylori-positive patients were higher than those of H. pylori-negative patients, without regard to the endoscopic grade of gastritis.Conclusions Reconstruction techniques play an important role in the prevention of bile reflux, and we found that endoscopically more severe remnant gastritis was associated with a lower rate of H. pylori infection and with a lower degree of inflammatory cellular infiltration.     

Decrease in Ornithine Decarboxylase Activity after Eradication of Helicobacter pylori

Objective: Our aim was to determine whether gastric mucosal ODC activity is altered after successful eradication of HP. Recent reports have suggested that Helicobacter pylori (HP) infection of the stomach is associated with the development of gastric cancer. Gastrointestinal cancers usually do not arise de novo; a series of mucosal changes leading to neoplastic transformation and degrees of dysplasia are believed to precede the development of cancer. These conditions are associated with increased cellular proliferation. Ornithine decarboxylase (ODC) activity is induced by factors that stimulate cellular proliferation, and has been shown to be elevated in gastrointestinal neoplasia, including gastric cancer. Methods: Gastric antral and body biopsies were obtained from 17 HP-positive patients at endoscopy, for ODC activity and histology (including Warthin Starry stain) before and 4–6 wk after successful triple therapy. Results: Patients included 12 males and five females, with a mean age of 55 yr (27–73 yr). Mean ODC activity (in pmol CO₂/mg protein/h) was significantly decreased after eradication of HP, compared with pretreatment levels in antral (147 ± 26 vs . 80 ± 15) and body mucosa (76 ± 21 vs . 20 ± 5) ( p < 0.05). Conclusion: Successful eradication of HP decreases mucosal proliferative activity, as reflected by decreased ODC activity. We speculate that by decreasing mucosal proliferative activity, HP eradication may help decrease the subsequent risk of gastric cancer.     

Induction of gastric ornithine decarboxylase in early weaning rats.

BACKGROUND/AIMS: Early weaning has been shown to induce intestinal ornithine decarboxylase (ODC) activities and cell proliferation in rats. No information is available about the effect of early weaning on ODC activity in the stomach. METHODS: Suckling rats were prematurely weaned on postnatal day 15 and followed through day 21. Oxyntic gland mucosa of stomach was obtained on postnatal days 15, 16, 18 and 21 (days 0, 1, 3 and 6 after early weaning) and assayed for ODC activity, DNA, protein and pepsinogen activity. alpha-Difluoromethyl ornithine (DFMO), a specific ODC inhibitor, was given orally to early-weaned pups and its resultant effects were assessed on days 1 and 6 after early weaning. RESULTS: Stomach mucosal wet weight, DNA, protein and pepsinogen activities significantly increased on day 6 after early weaning. ODC activity increased on days 1, 3, and 6 after early weaning, with the highest increase (3-fold) on day 1 when compared to controls. The increases of ODC activity, DNA and protein contents as induced by early weaning were significantly suppressed when pups were exposed to DFMO. However, no suppression of pepsinogen activity was observed. CONCLUSIONS: Our study shows that early weaning induces ODC activity and functional growth in the stomach. Gastric ODC activity is essential in gastric mucosal growth processes but not in differentiation. The induction of stomach ODC may act as an early marker in the growth of stomach mucosa induced by early weaning in rats.     

Histopathologic study on development and extension of atrophic change in the gastric mucosa

A histopathologic study was carried out on 30 resected stomachs with various gastric or duodenal diseases. Both the pyloric gland cells and the parietal cells were counted in serial sections of the surgically resected stomach. A good correlation (p less than 0.001) was found between the number of pyloric gland cells and parietal cells. The number of both glandular cells was greatest on the greater curvature and fewest at the part closer to the antrofundic mucosal border on the lesser curvature. In addition, a fairly uniform pattern was observed in the distribution of the parietal cells. The maximum density area of parietal cells was centered on the greater curvature of the stomach body, and this density decreased concentrically in proportion to the distance from the center. This uniform pattern was seen in almost all specimens, with or without atrophic change in the gastric mucosa. These results suggest that atrophic change does not develop in a particular part of the stomach but wholly and equally in the gastric mucosa.     

Cytology of the gastric mucosa in the development of chronic gastritis

Cellular changes were studied in specimens of the gastric mucosa from 131 patients with gastric biopsies from the normal mucosa and from those with various forms of chronic gastritis. The normal gastric mucosa was associated with moderate cell exfoliation and with normal cell structures. In cases of superficial gastritis and interstitial gastritis, the cellular material was more abundant than in smears from the normal stomach. The cells encountered were of surface mucosal and often also of glandular origin and were found together with numerous inflammatory cells. Cases with preatrophic and atrophic gastritis and with gastritis of the stomach remnant presented evidence of cellular metaplasia and nuclear and cytoplasmic alterations in surface mucosal cells. The results from study of gastric cellular changes in smears have led to further clarification of the diagnostic role of cytology which reflects the histologic alterations of gastric disorders and also often complements gastric biopsy findings.     

Inhibitory remnant stomach motility by duodenal distention after B-I gastrectomy

BACKGROUND/AIMS: Although control of gastric motility is a highly regulated process, B-I gastrectomy causes accelerated gastric emptying. We found few reports so far concerned with the mechanical effect of balloon distention of the duodenum on the remnant stomach in B-I dogs. METHODOLOGY: Four weeks after conventional distal gastrectomy with B-I reconstruction procedure, a balloon was inserted into the duodenum, and strain gauge force transducers (SGTs) were sutured onto the wall of the gastric remnant and duodenal serosa in beagles. After a two-week postoperative recovery period, gastro-duodenal motility was measured with SGTs prior to distention, during distention, and after evacuation of the balloon. The motility index (MI) was calculated every 30 minutes. RESULTS: Upon duodenal distention with 4 mL of water, motility of gastric remnant was significantly inhibited, however, no reduction in duodenal MI was observed. The response was maintained for as long as duodenal distension continued. Ninety minutes after evacuation of the balloon, MI returned to predistension levels. Increased plasma levels of cholecystokinin (CCK) were observed upon distention of the duodenal balloon. CONCLUSIONS: Motility of the remnant stomach in B-I dogs was inhibited by duodenal distension. Increased levels of plasma CCK during distention might play a role in this feedback mechanism.     

Gastric lipase: localization in the human stomach

The aim of this study was to determine the range of activity and the location of lipase in the human stomach. The range of lipase activity in gastric mucosa of surgical specimens from the fundic area of 22 subjects was 594 to 3350 mU [mean, 1598 +/- 144 mU tri[3H]olein, (1 mU-1 nmol [3H]oleic acid released from tri[3H]olein per minute per milligram protein)]. For localization of activity, pinch biopsy specimens of gastric mucosa from 6 subjects were taken from the greater and lesser curvatures within 2 cm of the gastroesophageal junction (upper greater curvature and upper lesser curvature) and within 2 cm of the pylorus (lower greater curvature and lower lesser curvature). Lipase activity was higher in the upper greater curvature (405 +/- 92 mU) than in the upper lesser curvature (32 +/- 13 mU) and lowest in the antral area (16 +/- 9 mU in the lower lesser curvature and 10 +/- 2 mU in the lower greater curvature). The data show that in the human, lipase activity is localized primarily in the fundic area of the stomach. Comparison of the lipase activity levels in the gastric mucosa with lingual lipase activity levels in specimens of lingual serous glands indicates that in humans, gastric lipase is the main lipase active in the stomach.     

Increase in apoptosis and decrease in ornithine decarboxylase activity of the gastric mucosa in patients with atrophic gastritis and gastric ulcer after successful eradication of Helicobacter pylori

OBJECTIVE: Recent reports have shown that patients infected with Helicobacter pylori (H. pylori) have a higher risk of gastric cancer. However, the mechanism of this increased risk is still unclear. In the gastric mucosa, the size of a continuously renewed population of cells is determined by the rates of cell production and of cell loss. Ornithine decarboxylase (ODC) activity is elevated in various gastrointestinal cancers and serves as a marker of mucosal proliferative activity. Apoptosis occurs throughout the gut and is associated with cell loss. Both cell proliferation and cell loss have important roles in H. pylori-associated gastric carcinogenesis. Therefore, we investigated the effect of H. pylori eradication on ODC activity and apoptosis in the gastric mucosa of patients with atrophic gastritis and gastric ulcers. METHODS: Biopsy specimens of the gastric antrum were obtained at endoscopy from 17 H. pylori-positive gastric ulcers patients and 15 H. pylori-positive gastritis patients before and 4 wk after eradication therapy with amoxicillin, omeprazole, and a new anti-ulcer agent, ecabet sodium, and from 10 gastric ulcer patients in whom ulcer healed but H. pylori was left untreated. ODC activity and induction of apoptosis were determined immunohistochemically. RESULTS: H. pylori was successfully eradicated with the triple therapy in 12 (80%) of 15 gastritis patients and 13 (76%) of 17 gastric ulcer patients. ODC activity was present in the gastric mucosa in 21 (84%) patients before eradication but in only four (16%) patients after successful eradication (p = 0.0005). The apoptotic index increased significantly (p = 0.0006) from 4.2% +/- 0.4% before treatment to 7.4% +/- 0.5% after successful eradication. CONCLUSIONS: Successful eradication of H. pylori decreases mucosal ODC activity and increases apoptosis in the gastric mucosa. These findings indicate that by decreasing mucosal cell proliferation and increasing epithelial cell loss, H. pylori eradication may help decrease the subsequent risk of gastric cancer.     

Spatial heterogeneity of mucosal blood flow during ischemia-reperfusion injury of rat stomach investigated by laser Doppler perfusion imaging

Spatial alterations in blood flow during the development of mucosal injury induced by ischemia-reperfusion in rats were determined with a two-dimensional laser Doppler tissue perfusion imager. The rats were anesthetized with pentobarbital, and the stomach was exteriorized on a stage; the mucosa was then sequentially scanned. The mucosa was constantly superfused with 0.1N HCl in physiological saline. Systemic arterial pressure was continuously monitored and blood was stepwisely withdrawn from the femoral artery by 20-mmHg stage and then maintained at 20 mmHg for 20 min. The shed blood was reinfused and the stomach was removed 30 min later. Under control conditions, the average perfusion of the forestomach was usually greater than that in the glandular stomach. When systemic blood pressure was stepwisely decreased, the extent of decrease in the mucosal blood perfusion unit was always greater than that in systemic blood pressure, but mucosal perfusion appeared to be uniformly decreased throughout the stomach. Ten min after reperfusion, a hypoperfused area began to appear in the corpus near the greater curvature, and this area subsequently increased. The area of ulcer formation corresponded with the hypoperfused area in the gastric mucosa 30 min after reperfusion. Pretreatment with CV-6209, a platelet-activating factor antagonist, significantly attenuated the hypoperfusion induced by reperfusion and also prevented gastric mucosal damage. Our results suggest that hypoperfusion in the mucosal microcirculation is indeed an important factor contributing to the localized occurrence of gastric mucosal lesions and that the laser Doppler perfusion imager is useful for the detection of local hypoperfused areas in the gastric mucosa.     

Duodenogastric reflux sustains Helicobacter pylori infection in the gastric stump

BACKGROUND: Duodenogastric reflux (DGR) and Helicobacter pylori infection have been suspected of being contributing agents to the genesis of gastritis and subsequent cancer, but compelling, conclusive data about the exact relationship have been lacking. METHODS: We investigated the effect of DGR on H. pylori infection in 95 gastrectomized subjects divided into four groups according to type of reconstruction: the jejunal pouch interposition group (JPI, n = 36); the Roux-en-Y group (RY, n = 17); the Billroth I group (B-I, n = 20); and the Billroth II group (B-II, n = 22). The following items were examined for each group: the duration of DGR; the prevalence of H. pylori infection; other bacterial identification and quantity; and the severity of gastritis. RESULTS: The percent of total time of DGR was lower in the JPI (7%) and RY groups (28%) than in the B-I (59%) and B-II groups (88%) (P < 0.02). The prevalence of H. pylori infection was lower in the JPI (28%) and RY groups (29%) than in the B-I (60%) and B-II groups (73%) (P < 0.02). Inversely, the JPI and the RY groups had a higher quantity of other bacteria than the B-I group (P = 0.02). For all four groups, the stomachs infected with H. pylori were fewer than those tested negative for the organism (P < 0.0001). Inflammation scores were lower in both the JPI and RY groups than in the B-I and B-II groups (P < 0.05, respectively). CONCLUSIONS: Duodenogastric reflux facilitates the survival of H. pylori in the gastric stump after a distal gastrectomy.     

长期胆汁反流对大鼠胃黏膜的影响

目的研究长期胆汁反流对大鼠胃黏膜的影响.方法反流组大鼠91只,于胆总管开口水平以下横断十二指肠,并将前胃与空肠吻合,建立胆汁反流大鼠模型,对照组大鼠12只未手术,1年后予胃部病理检查.结果反流组大鼠13只存活满1年.大鼠前胃鳞状上皮基底细胞增生,黏膜下血管增多、扩张、充血,黏膜基底部和黏膜下中、重度慢性炎症,呈轻度活动性.腺胃胃体小凹增生,泌酸腺底部扩张,黏膜表层轻度慢性炎症,无活动性,黏膜基底部和黏膜下轻度慢性炎症,活动性为轻度.胃窦小凹增生,1只大鼠呈轻度不典型增生,1只有高分化管状腺癌伴黏膜下层骨化生,黏膜基底部和黏膜下轻度慢性炎症,无活动性.结论长期胆汁反流能导致腺胃柱状上皮和前胃鳞状上皮增生,并逐渐加重,终具有致癌作用.     

Direct observation of microcirculation of the basal region of rat gastric mucosa

We modified and improved techniques for the intravital microscopic observation of the rat gastric microcirculation. The stomach of anesthetized rats was cut along the greater curvature, and the posterior wall of the glandular stomach was fixed in a chamber with the serosal side up and perfused with warmed Tyrode's solution. A portion of the muscularis externa was resected with the serosa to make an observation window. Vascular casts were studied histologically after the injection of Monastral blue B gelatin solution. Vascular casts revealed that most of the microvasculature observed in the window was not located in the submucosa, but in the basal part of the mucosa. Microscopic observation showed that the basal mucosal arterioles branched to form the mucosal capillaries, and the collecting venules from the mucosal surface were seen in cross-sections to drain into the venules located in the basal mucosa, without penetrating the muscularis mucosae. Topical application of acetylcholine (0.03–10μM) to the window dilated the arterioles, and topical application of epinephrine (0.03–3μM) constricted them dose-dependently without affecting the collecting venules and the venules. This method made possible the direct observation of the microvasculature in the basal mucosa of the stomach, in which common microvessel characteristics were shown.     

Ornithine decarboxylase as a marker for premalignancy in the stomach.

Assessment of mucosal ornithine decarboxylase (ODC) activity in the human large bowel may be of value as a marker of potential malignant risk. Its value as a marker of premalignancy in the upper gastrointestinal tract is less clear. Using a [14C]-ornithine bioassay, gastric mucosal ODC activity was measured in 32 normal subjects and 22 patients with confirmed gastric cancer. These results were compared with 47 patients at increased risk of upper gastrointestinal malignancy, (32 patients with partial gastric resection, 15 patients with familial adenomatous polyposis). Median ODC activity in normal subjects was 371 pmol/mg protein/h, (interquartile range (IQR), 230-617). There was no variation with age or sex and no relation to Helicobacter pylori status. Normal subjects had significantly lower ODC activity than patients with a gastric resection or confirmed gastric cancer, but similar to patients with familial adenomatous polyposis. Furthermore, no difference in activity was identified between patients with a gastric resection and established gastric cancer. ODC activity was, however, significantly increased in areas of gastric atrophy or intestinal metaplasia, regardless of the clinical group from which the samples were obtained. It is concluded that measurement of mucosal ODC activity does not provide additional predictive information of malignant risk in the stomach and investigation of other potential biomarkers of malignancy is warranted.     

A study of ornithine decarboxylase activity in tumor tissue and rectal mucosa in patients with colorectal cancer or adenoma

Rectal mucosa from normal controls (n = 25) and tumor tissue and rectal mucosa from patients with colorectal cancer (n = 38) and adenoma (n = 35) were biopsied via colonoscopy. Ornithine decarboxylase (ODC) activity was determined in order to study the role of promoters in the process of colorectal carcinogenesis. ODC activity of cancer tissue was significantly higher than that of adenoma tissue. Normal mucosal ODC activity in rectum and sigmoid colon was 2 to 4 times higher than that in the proximal colon. Moreover, rectal mucosal ODC activity was significantly higher in patients with cancer or adenoma than that in normal controls. When ODC activity is regarded as an index of promoter, the possibility is suggested that cancer and adenoma developed in similar mucosa of the large bowel. Furthermore, ODC activity in colon cancer was significantly higher than that in rectal cancer. This suggests the possibility that TPA type promoter assumes a greater role in the process of carcinogenesis of colon cancer than that of rectal cancer.     

Lymph node dissection in surgical treatment for remnant stomach cancer

BACKGROUND/AIMS: Lymphatic flow and the incidence of lymph node metastasis in remnant stomach cancer after distal gastrectomy are obscure. There is consequent controversy about appropriate lymph node dissection in such cases. METHODOLOGY: Thirty-three consecutive patients with remnant stomach cancer and 44 consecutive patients primary gastric cancer in the upper third of the stomach were investigated retrospectively about lymphatic flow by injection of activated carbon particles, and about the incidence of lymph node metastasis. RESULTS: Lymphatic flow and the incidence of lymph node metastasis in remnant stomach cancer after distal gastrectomy without lymph node dissection were the same as those in primary gastric cancer in the upper third of the stomach. Lymphatic flow after distal gastrectomy with lymph node dissection frequently streamed toward the para-aortic lymph nodes through the lymph nodes along the greater curvature and the suprapancreatic lymph nodes. Lymphatic flow toward the jejunal and colonic mesentery was observed regardless of the method of reconstruction. This lymphogenesis was clearly observed, especially in patients with tumors invading the anastomosis site of Billroth-II reconstruction. Station Nos. 110 (lower paraesophageal) and 111 (supradiaphragmatic) lymph nodes were also stained, despite being considered sites of distant metastasis irrespective of the method of reconstruction. CONCLUSIONS: On the basis of the evidence of altered lymphatic flow and the incidence of lymph node metastases in remnant stomach cancer, left upper abdominal evisceration with para-aortic lymph node dissection should be performed in advanced remnant stomach cancer.     

Intestinal-type tumour in resected gastric remnant cancer

Lauren's intestinal type of gastric cancer was proposed to be dependent on long-term environmental factors and is always preceded by chronic premalignant change. A cohort study was performed and demonstrated an increased cancer risk of gastric remnant after gastric surgery for benign disease. It is generally believed that after gastrectomy the residual stomach has an environmental change and, thus, enters a neoplastic process. Based on the carcinogenic theory of intestinal-type tumour, it would be of interest to know whether the intestinal-type tumour is more common in gastric remnant cancer. Forty patients with gastric remnant cancer had gastrectomy in the Veterans General Hospital-Taipei. Another 683 patients with primary gastric carcinoma underwent resection and were used as controls. The clinical characteristics, tumour stage and intestinal-type tumour were analysed in gastric remnant cancer and were compared with the various portions of primary gastric carcinoma. Although the overall distribution of intestinal-type carcinoma in gastric remnant (45%) was no different to that of any other portion of stomach cancer, intestinal-type carcinoma was more common in the early stage of gastric remnant (73%) and distal stomach (73%), but not in the proximal stomach (50%), which was supposed to have the same characteristics as the gastric remnant because of identical anatomic location. More than expected, intestinal-type carcinoma in early gastric remnant cancer together with a long incubation interval between primary surgery and later tumour occurrence were compatible with the theory of carcinogenesis of intestinal-type carcinoma.