Elevated risk of recurrent colorectal neoplasia with Helicobacter pylori‑associated chronic atrophic gastritis: 
A follow‑up study of patients with endoscopically resected colorectal neoplasia

Inoue,Izumi; Kato,Jun; Yoshimura,Noriko; Maeda,Yoshimasa; Moribata,Kosaku; Shingaki,Naoki; Deguchi,Hisanobu; Enomoto,Shotaro; Maekita,Takao; Ueda,Kazuki; Iguchi,Mikitaka; Tamai,Hideyuki; Fujishiro,Mitsuhiro; Yamamichi,Nobutake; Takeshita,Tatsuya; Ichinose,Masao

doi:10.3892/mco.2012.22

Elevated risk of recurrent colorectal neoplasia with Helicobacter pylori‑associated chronic atrophic gastritis: A follow‑up study of patients with endoscopically resected colorectal neoplasia

Authors:
- Izumi Inoue
- Jun Kato
- Noriko Yoshimura
- Yoshimasa Maeda
- Kosaku Moribata
- Naoki Shingaki
- Hisanobu Deguchi
- Shotaro Enomoto
- Takao Maekita
- Kazuki Ueda
- Mikitaka Iguchi
- Hideyuki Tamai
- Mitsuhiro Fujishiro
- Nobutake Yamamichi
- Tatsuya Takeshita
- Masao Ichinose
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Affiliations: Department of Gastroenterology, School of Medicine, Wakayama Medical University, Wakayama 641-0012, Japan, Department of Joint Disease Research, Graduate School of Medicine, The University of Tokyo, Tokyo 113‑8655, Japan, Department of Gastroenterology, Graduate School of Medicine, The University of Tokyo, Tokyo 113‑8655, Japan, Department of Public Health, School of Medicine, Wakayama Medical University, Wakayama 641-0012, Japan
Published online on: September 11, 2012 https://doi.org/10.3892/mco.2012.22
Pages: 75-82

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Abstract

In a previous population-based case-control study, we demonstrated an elevated risk of colorectal neoplasia with Helicobacter pylori (H. pylori) infection. The present study investigated the effects of H. pylori-associated chronic gastritis on the development of colorectal neoplasia by analyzing the recurrence of colorectal neoplasia subsequent to endoscopic resection. Ninety-nine patients who had undergone endoscopic resection of colorectal neoplasia were monitored under colonoscopy, and the recurrence of colorectal neoplasia was prospectively investigated. The stage of H. pylori-associated chronic gastritis in each subject was evaluated using a combination of two serum tests: H. pylori antibody and pepsinogen. In the present cohort, colorectal neoplasia recurred at a rate of 15,296/100,000 person-years during the study period. After adjusting for the confounding factors, chronic atrophic gastritis (CAG) was identified as an independent risk factor [adjusted hazard ratio (HR), 2.72; 95% confidence interval, 1.33-5.57], while H. pylori-infected non-atrophic gastritis was not identified as an independent risk factor for recurrent colorectal neoplasia. Colorectal neoplasia recurred earlier and was significantly more frequent in patients with CAG (22,573/100,000 person-years) compared to patients without CAG (11,089/100,000 person-years; P=0.029, log‑rank test). Patients with more extensive CAG showed a higher risk of recurrence. These results demonstrated a significant elevation of the risk of recurrent colorectal neoplasia with the establishment and progression of CAG, indicating the involvement of H. pylori infection in the development of colorectal neoplasia. The two serum tests were useful clinical markers for non-invasively evaluating the risk of each individual for recurrent colorectal neoplasia subsequent to endoscopic resection.

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1.	Lee JH, Bae JS, Ryu KW, et al: Gastric cancer patients at high-risk of having synchronous cancer. World J Gastroenterol. 12:2588–2592. 2006.
2.	Ciccotosto GD, McLeish A, Hardy KJ and Shulkes A: Expression, processing, and secretion of gastrin in patients with colorectal carcinoma. Gastroenterology. 109:1142–1153. 1995.
3.	Hollande F, Imdahl A, Mantamadiotis T, Ciccotosto GD, Shulkes A and Baldwin GS: Glycine-extended gastrin acts as an autocrine growth factor in a nontransformed colon cell line. Gastroenterology. 113:1576–1588. 1997.
4.	Brown D, Yallampalli U, Owlia A and Singh P: pp60c-Src kinase mediates growth effects of the full-length precursor progastrin1-80 peptide on rat intestinal epithelial cells, in vitro. Endocrinology. 144:201–211. 2003.
5.	Koh TJ: Extragastric effects of gastrin gene knock-out mice. Pharmacol Toxicol. 91:368–374. 2002.
6.	Kanno T, Matsuki T, Oka M, et al: Gastric acid reduction leads to an alteration in lower intestinal microflora. Biochem Biophys Res Commun. 381:666–670. 2009.
7.	Inoue I, Mukoubayashi C, Yoshimura N, et al: Elevated risk of colorectal adenoma with Helicobacter pylori-related chronic gastritis: a population-based case-control study. Int J Cancer. 129:2704–2711. 2011.
8.	Saini SD, Kim HM and Schoenfeld P: Incidence of advanced adenomas at surveillance colonoscopy in patients with a personal history of colon adenomas: a meta-analysis and systematic review. Gastrointest Endosc. 64:614–626. 2006.
9.	Lin OS: Clinical update: postpolypectomy colonoscopy surveillance. Lancet. 370:1674–1676. 2007.
10.	Martinez EM, Baron AJ, Lieberman AD, et al: A pooled analysis of advanced colorectal neoplasia diagnoses after colonoscopic polypectomy. Gastroenterology. 136:832–841. 2009.
11.	Kikuchi S and Miwa H: Efficacy of the ELISA test ‘E Plate Eiken H. pylori antibody’ for the diagnosis of Helicobacter pylori infection. Jpn J Med Pharm Sci. 43:581–586. 2000.(In Japanese).
12.	Ichinose M, Miki K, Furihata C, et al: Radioimmunoassay of serum group I and group II pepsinogens in normal controls and patients with various disorders. Clin Chim Acta. 126:183–191. 1982.
13.	Ichinose M, Yahagi N, Oka M, Ikeda H, Miki K and Omata M: Screening for gastric cancer in Japan. Cancer Screening. Wu GY and Aziz K: Humana Press; Totowa, NJ: pp. 255–268. 2001
14.	Yanaoka K, Oka M, Mukoubayashi C, et al: Cancer high-risk subjects identified by serum pepsinogen tests: outcomes after 10-year follow-up in asymptomatic middle-aged males. Cancer Epidemiol Biomarkers Prev. 17:838–845. 2008.
15.	Komine M: Megaloblastic anemia. Int J Hematol. 71:82000.
16.	Ohata H, Kitauchi S, Yoshimura N, et al: Progression of chronic atrophic gastritis associated with Helicobacter pylori infection increases risk of gastric cancer. Int J Cancer. 109:138–143. 2004.
17.	Takeda M, Iwachika C, Demura H, Shiratori K and Watanabe S: Experimental and clinical investigation of gastrin RIA kit α. Horumon To Rinsho. 31:1123–1128. 1983.(In Japanese).
18.	Harewood GC and Lawlor GO: Incident rates of colonic neoplasia according to age and gender. J Clin Gastroenterol. 39:894–899. 2005.
19.	Laiyemo AO, Murphy G, Albert PS, et al: Postpolypectomy surveillance guidelines: predictive accuracy for advanced adenoma at 4 years. Ann Intern Med. 148:419–426. 2008.
20.	Boolchand V, Olds G, Singh P, Chak A and Cooper GS: Colorectal screening after polypectomy: a national survey study of primary care physicians. Ann Intern Med. 145:654–659. 2006.
21.	Correa P: Human gastric carcinogenesis: a multistep and multi-factorial process - First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res. 52:6735–6740. 1992.
22.	Meucci G, Tatarella M, Vecchi M, et al: High prevalence of Helicobacter pylori infection in patients with colonic adenomas and carcinomas. J Clin Gastroenterol. 25:605–607. 1997.
23.	Breuer-Katschinski B, Nemes K, Marr A, Rump B, Leiendecker B, Breuer N and Goebell H: Helicobacter pylori and the risk of colonic adenomas. Colorectal Adenoma Study Group Digestion. 60:210–215. 1999.
24.	Mizuno S, Morita Y, Inui T, et al: Helicobacter pylori infection is associated with colon adenomatous polyps detected by high-resolution colonoscopy. Int J Cancer. 117:1058–1059. 2005.
25.	Fireman Z, Trost L, Kopelman Y, Segal A and Sternberg A: Helicobacter pylori: seroprevalence and colorectal cancer. Isr Med Assoc J. 2:6–9. 2000.
26.	Shmuely H, Passaro D, Figer A, et al: Relationship between Helicobacter pylori CagA status and colorectal cancer. Am J Gastroenterol. 96:3406–3410. 2001.
27.	Fujimori S, Kishida T, Kobayashi T, et al: Helicobacter pylori infection increases the risk of colorectal adenoma and adenocarcinoma, especially in women. J Gastroenterol. 40:887–893. 2005.
28.	Jones M, Helliwell P, Pritchard C, Tharakan J and Mathew J: Helicobacter pylori in colorectal neoplasms: is there an aetiological relationship? World J Surg Oncol. 5:512007.
29.	Machida-Montani A, Sasazuki S, Inoue M, et al: Atrophic gastritis, Helicobacter pylori, and colorectal cancer risk: a case-control study. Helicobacter. 12:328–332. 2007.
30.	Laiyemo AO, Kamanger F, Marcus PM, Taylor PR, Virtamo J, Albanes D and Stolzenberg-Solomon RZ: Atrophic gastritis and the risk of incident colorectal cancer. Cancer Causes Control. 21:163–170. 2010.
31.	Imperiale TF, Glowinski EA, Lin-Cooper C, Larkin GN, Rogge JD and Ransohoff DF: Five-year risk of colorectal neoplasia after negative screening colonoscopy. N Engl J Med. 359:1218–1224. 2008.
32.	Georgopoulos SD, Polymeros D, Triantafyllou K, Spiliadi C, Mentis A, Karamanolis DG and Ladas SD: Hypergastrinemia is associated with increased risk of distal colon adenomas. Digestion. 74:42–46. 2006.
33.	Penman ID, el-Omar E, Ardill JES, McGregor JR, Galloway DJ, O’Dwyer PJ and McColl KE: Plasma gastrin concentrations are normal in patients with colorectal neoplasia and unaltered following tumor resection. Gastroenterology. 106:1263–1270. 1994.
34.	Kado S, Uchida K, Funabashi H, et al: Intestinal microflora are necessary for development of spontaneous adenocarcinoma of the large intestine in T-cell receptor β chain and p53 double-knockout mice. Cancer Res. 61:2395–2398. 2001.
35.	Howden CW and Hunt RH: Relationship between gastric secretion and infection. Gut. 28:96–107. 1987.
36.	Drasar BS, Shiner M and McLeod GM: Studies on the intestinal flora: I. The bacterial flora of the gastrointestinal tract in healthy and achlorhydric persons. Gastroenterology. 56:71–79. 1969.
37.	Thorens J, Froehlich F, Schwizer W, et al: Bacterial overgrowth during treatment with omeprazole compared with cimetidine: a prospective randomized double blind study. Gut. 39:54–59. 1996.
38.	Evenepoel P, Claus D, Geypens B, Maes B, Hiele M, Rutgeerts P and Ghoos Y: Evidence for impaired assimilation and increased colonic fermentation of protein, related to gastric acid suppression therapy. Aliment Pharmacol Ther. 12:1011–1019. 1998.
39.	Visek WJ: Diet and cell growth modulation by ammonia. Am J Clin Nutr. 31:216–220. 1978.
40.	LeVeen HH, LeVeen EG and LeVeen RF: Awakenings to the pathogenicity of urease and the requirement for continuous long-term therapy. Biomed Pharmacother. 48:157–166. 1994.
41.	Clinton SK, Bostwick DG, Olson LM, Mangian HJ and Visek WJ: Effects of ammonium acetate and sodium cholate on N-methyl-N-nitro-N-nitrosoguanidine-induced colon carcinogenesis of rats. Cancer Res. 48:3035–3039. 1988.
42.	Martinez ME, Sampliner R, Marshall JR, Bhattacharyya AK, Reid ME and Alberts DS: Adenoma characteristics as risk factors for recurrence of advanced adenomas. Gastroenterology. 120:1077–1083. 2001.
43.	Iacopetta B: Are there two sides to colorectal cancer? Int J Cancer. 101:403–408. 2002.
44.	Nakajima T, Enomoto S and Ushijima T: DNA methylation: a marker for carcinogen exposure and cancer risk. Environ Health Prev Med. 13:8–15. 2008.
45.	Giovannucci E, Colditz GA and Stampfer MJ: A meta-analysis of cholecystectomy and risk of colorectal cancer. Gastroenterology. 105:130–141. 1993.
46.	Pereira MA, Wang W, Kramer PM and Tao L: DNA hypomethylation induced by non-genotoxic carcinogens in mouse and rat colons. Cancer Lett. 212:145–151. 2004.
47.	Bernstein H, Bernstein C, Payne CM, Dvorakova K and Garewal H: Bile acids as carcinogens in human gastrointestinal cancers. Mutat Res. 589:47–65. 2005.
48.	Rex DK, Cutler CS, Lemmel GT, et al: Colonoscopic miss rates of adenomas determined by back-to-back colonoscopies. Gastroenterology. 112:24–28. 1997.
49.	Hixson LJ, Fennerty MB, Sampliner RE and Garewal HS: Prospective blinded trial of the colonoscopy miss-rate of large colorectal polyps. Gastrointest Endosc. 37:125–127. 1991.
50.	Robertson DJ, Greenberg ER, Beach M, et al: Colorectal cancer in patients under close colonoscopic surveillance. Gastroenterology. 129:34–41. 2005.