Abstract
Aging and smoking are known to promote atrophic gastritis (AG) and intestinal metaplasia (IM). This study investigated the relationship between Helicobacter pylori (Hp) infection, aging, smoking, and AG/IM. Ninety-six Hp-negative and 231 Hp-positive subjects were divided according to age; (≤39 years, 40–59 years, and ≥60 years) and smoking history (never smoked, or currently smoking). Histologic grading was performed according to the updated Sydney system. Fasting pH, total bile acid (TBA) concentration, and ammonia (NH3) concentration in gastric juice were measured. Comparisons were made based on Hp status, age, and smoking. Independent relative risks for severe AG and IM were calculated. Grades of atrophy and IM were significantly higher in Hp-positive subjects, and these increased with age. Within Hp-positive subjects, grades of atrophy and IM were higher in smokers and in the middle and upper age groups. Within Hp-positive subjects, gastric pH and TBA were similarly higher in smokers and older subjects. An increased risk of severe AG/IM was statistically associated with smoking (OR 9.31, 3.85–22.50/OR 4.91, 1.90–12.68) and high TBA concentrations (OR 2.92, 1.19–7.17/OR 3.28, 1.25–8.62). Both Hp infection and aging are closely related to the development of AG and IM. Cigarette use and high TBA concentrations may play a role in the progression of AG and IM in Hp-positive subjects.
Similar content being viewed by others
REFERENCES
Blaser MJ: Gastric Campylobacter-like organisms, gastritis, and peptic ulcer disease. Gastroenterology 93:371–383, 1987
Dixon MF: Campylobacter pylori and chronic gastritis. In Campylobacter pylori and Gastroduodenal Disease. BJ Rathbone, RV Heatley, (eds). London, Blackwell Scientific Publications, 1992, pp 106–116
Correa P: Is gastric carcinoma an infectious disease? N Engl J Med 17:1170–1171, 1991
Satoh K, Kimura K, Taniguchi Y, Yoshida Y, Kihara K, Takimoto T, Kawata H, Saifuku K, Ido K, Takemoto T, Ota Y, Tada M, Karita M, Sakaki N, Hoshihara Y: Distribution of inflammation and atrophy in the stomach of Helicobacter pylori-positive and negative patients with chronic gastritis. Am J Gastroenterol 91:963–969, 1996
Genta RM, Lew GM, Graham DY: Changes in the gastric mucosa following eradiation of Helicobacter pylori. Modern Pathol 6:281–289, 1993
Kimura K: Chronological transition of the fundic pyloric border determined by stepwise biopsy of the lesser curvatures of the stomach. Gastroentelogy 63:584–592, 1972
Webb PM, Bates CJ, Palli D, Forman D: Gastric cancer, gastritis and plasma vitamin C: results from an international correlation and cross-sectional study. The Eurogast Study Group. Int J Cancer 73:684–689, 1997
Sipponen P, Hyvarinen H, Seppala K, Blaser MJ: Pathogenesis of the transformation from gastritis to malignancy. Aliment Pharmacol Ther 12(suppl 1):61–71, 1998
Jedrychowski W, Wahrendorf J, Popiela T, Rachtan J: Effect of Helicobacter pylori infection, smoking and dietary habits on the occurrence of antral intestinal metaplasia. Clinico-epidemiological study in Polanad. Pol J Pathol 50:289–295, 1999
Fonthan E, Ruiz B, Perez A, Hunter F, Correa P: Determination of Helicobacter pylori infection and chronic gastritis. Am J Gastroenterol 90:1094–1101, 1995
Stemmermann G, Nomura A, Chyou P, Hankin J: Impact of diet and smoking on risk of developing intestinal metaplasia of the stomach. Dig Dis Sci 35:433–438, 1990
Ozasa K, Kurata JH, Higashi A, Hayashi K, Inokuchi H, Miki K, Tada M, Kawai K, Watanabe Y: Helicobacter pylori infection and atrophic gastritis: A nested case-control study in rural town in Japan Dig Dis Sci 44:253–256, 1999
Shousha S, Barrison IG, EI Sayeed W, Kahn S, Parkins RA: A study of incidence and relationship of intestinal metaplasia of gastric antrum and gastric metaplasia of gastric antrum and gastric metaplasia of the duodenum in patients with non ulcer dyspepsia. Dig Dis Sci 29:311–316, 1984
Kneller RW, You WC, Chang YS, Liu WD, Zhang L, Zhao L, Xu GW, Fraumeni JF Jr, Blot WJ: Cigarette smoking and other risk factors for progression of precancerous stomach lesions. J Natl Cancer Inst 84:1261–1266, 1992
Paxton D, Michael FD, David J: Bile reflux and degree of gastritis in patients with gastric ulcer, before and after operation. J Surg Res 37:277–284, 1984
Watt PCH, Sloan JM, Donaldson JD, Patterson CC, Kennedy TL: Relationship between histology and gastric juice pH and nitrite in the stomach after operation for duodenal ulcer. Gut 25:246–252, 1984
Houghton PWJ, Mortensen NJMC, Thomas WEG, Cooper MJ, Morgan AP, Davies ER: Gastric juice bile acids and scintigraphy in the assessment of duodenogastric reflux. Gut 25:1183, (abstract) 1984
Muller-Lissner SA: Bile reflux is increased in cigarette smokers. Gastroenterology 90:1205–1209, 1986
Haruma K, Fujimura J, Hata J, Yoshihara M, Yamanaka H, Machino H, Kajiyama G: Effect of cigarette smoking on antroduodenal motility. Gastroenterology 102:457, (abstract) 1992
Mashige F, Tanaka N, Maki A, Kamei S, Yamanaka M: Direct spectrophotometry of total bile acids in serum. Clin Chem 27:1352–1356, 1981
Okuda H, Fujii S: Determination of the concentration of ammonia in plasma by means of direct color reaction method. Saishin-Igaku 21:622–627, 1966 (in Japanese)
McNulty CAM: Detection of Helicobacter pylori by the biopsy urease test. In Helicobacter pylori and Gastroduodenal Disease. BJ Rathbone, RV Heatley, (eds). Oxford: Blackwell Scientific Publications, 1992, pp 58–63
Misiewicz JJ, Price AB, Tytgat GNJ, Goodwin CS, Strickland RG, Sipponen P: The Sydney system. A new classification of gastritis. J Gastroenterol Hepatol 6:207–252, 1991
Glassman MS, Dallal S, Berezin SH, Bostwick HE, Newman LJ, Perez GI, Blaser MJ: Helicobacter pylori-related gastroduodenal disease in children. Diagnostic utility of enzyme-linked immunosorbent assay. Dig Dis Sci 35:993–997, 1990
Morson BC: Carcinoma arising from areas of intestinal metaplasia in gastric mucosa. Br J Cancer 9:377–385, 1955
Correa P: A human model of gastric carcinogenesis. Cancer Res 48:1319–1326, 1988
Mirvish SS: The etiology of gastric cancer. J Natl Cancer Inst 71:629–647, 1983
Komoto K, Haruma K, Kamada T, Tanaka S, Yoshihara M, Sumii K, Kajiyama G, Talley NJ: Helicobacter pylori infection and gastric neoplasia: Correlations with histological gastritis and tumor histology. Am J Gastroenterol 93:1271–1276, 1998
Asaka M, Kimura T, Kudo M, Takeda H, Mitani S, Miyazaki T, Miki K, Graham DY: Relationship of Helicobacter pylori to serum pepsinogens in an asymptomatic Japanese population. Gastroenterology 102:760–766, 1992
Nomura A, Stemmermann G, Chyou PH, Hankin J. Helicobacter pylori infection and gastric carcinoma among Japanese Americans in Hawaii. N Engl J Med 325:1132–1136, 1991
Kawaguchi H, Haruma K, Komoto K, Yoshihara M, Sumii K, Kajiyama G: Helicobacter pylori infection is the major risk factor for atrophic gastritis. Am J Gastroenterol 91:959–962, 1996
Fonthan E, Zavala D, Correa P, Rodriguez E, Hunter F, Haenszel W, Tannenbaum SR: Diet and chronic atrophic gastritis: A case-control study. J Natl Cancer Inst 76:621–627, 1986
Tatsuta M, Iishi H, Okuda S: Effect of cigarette smoking on extent of acid-secreting area and in the stomach. Dig Dis Sci 33:23–29, 1988
Endoh K, Leung FW: Effects of smoking and nicotine on gastric mucosa: A review of clinical and experimental evidence. Gastroenterology 107:864–878, 1994
Sobala GM, O'Connor HJ, Dixon MF, Dewar EP, King RFG, Axon ATR: Bile reflux and intestinal metaplasia in gastric mucosa. J Clin Pathol 46:235–240, 1993
Nakamura M, Haruma K, Kamada T, Mihara M, Yoshihara M, Imagawa M, Kajiyama G: Duodenogastric reflux is closely associated with antral metaplastic gastritis. Gastrointest Endosc 53:53–59, 2001
Mukawa K, Nakamura T, Nakao G, Nagamachi Y: Histopathogenesis of intestinal metaplasia: Minute lesions of intestinal metaplasia in ulcerated stomachs. J Clin Pathol 40:13–18, 1987
Oohara T, Yohma H, Aono G, Ukawa S, Kondo Y: Intestinal metaplasia of the regenerative epithelia in 549 gastric ulcers. Hum Pathol 14:1066–1071, 1983
Silva S, Filipe MI, Pinho A: Variants of intestinal metaplasia in the evolution of chronic atrophic gastritis and gastric ulcer. A follow-up study. Gut 31:1097–1104, 1990
Wyatt JI, Rathbone BJ, Sobala GM, Shallcross T, Heatley RV, Axon ATR: Gastric epithelium in the duodenum. Its association with Helicobacter pylori and inflammation. J Clin Pathol 43:981–986, 1990
Ladas SD, Katsogridakis J, Malamou H, Giannopoulou H, Kesse-Elia M, Raptis SA: Helicobacter pylori may induce bile reflux: Link between H. pylori and bile induced injury to gastric epithelium. Gut 38:15–18, 1996
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Nakamura, M., Haruma, K., Kamada, T. et al. Cigarette Smoking Promotes Atrophic Gastritis in Helicobacter pylori-Positive Subjects. Dig Dis Sci 47, 675–681 (2002). https://doi.org/10.1023/A:1017901110580
Issue Date:
DOI: https://doi.org/10.1023/A:1017901110580