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CC BY-NC-ND 4.0 · Endosc Int Open 2021; 09(03): E297-E305
DOI: 10.1055/a-1314-6626
Original article

Factors associated with the progression of gastric intestinal metaplasia: a multicenter, prospective cohort study

S. A. V. Nieuwenburg
 1   Departments of Gastroenterology and Hepatology, Erasmus University Medical Centre, Rotterdam, The Netherlands
,
M. C. Mommersteeg‡
 1   Departments of Gastroenterology and Hepatology, Erasmus University Medical Centre, Rotterdam, The Netherlands
,
E. L. Eikenboom‡
 1   Departments of Gastroenterology and Hepatology, Erasmus University Medical Centre, Rotterdam, The Netherlands
,
B. Yu
 1   Departments of Gastroenterology and Hepatology, Erasmus University Medical Centre, Rotterdam, The Netherlands
,
W. J. den Hollander
 2   Leiden University Medical Centre, Leiden, The Netherlands
,
I. Lisanne Holster
 1   Departments of Gastroenterology and Hepatology, Erasmus University Medical Centre, Rotterdam, The Netherlands
,
Caroline M. den Hoed
 1   Departments of Gastroenterology and Hepatology, Erasmus University Medical Centre, Rotterdam, The Netherlands
,
L. G Capelle
 3   Meander Medical Centre, Amersfoort, the Netherlands
,
Thjon J. Tang
 4   IJsselland Hospital, Capelle aan den IJssel, The Netherlands
,
Marie-Paule Anten
 5   Sint Franciscus Hospital, Rotterdam, The Netherlands
,
I. Prytz-Berset
 6   More and Romsdal Trust Ålesund, Ålesund, Norway
,
E. M. Witteman
 7   Canisius-Wilhelmina Hospital, Nijmegen, The Netherlands
,
F. ter Borg
 8   Deventer Hospital, Deventer, The Netherlands
,
Jordy P. W. Burger
 9   Department of Gastroenterology and Hepatology, Rijnstate, Arnhem, The Netherlands
,
Marco J. Bruno
 1   Departments of Gastroenterology and Hepatology, Erasmus University Medical Centre, Rotterdam, The Netherlands
,
G. M. Fuhler
 1   Departments of Gastroenterology and Hepatology, Erasmus University Medical Centre, Rotterdam, The Netherlands
,
Maikel P. Peppelenbosch
 1   Departments of Gastroenterology and Hepatology, Erasmus University Medical Centre, Rotterdam, The Netherlands
,
Michael Doukas
10   Department of Pathology, Erasmus University Medical Centre, Rotterdam, The Netherlands
,
Ernst J. Kuipers
 1   Departments of Gastroenterology and Hepatology, Erasmus University Medical Centre, Rotterdam, The Netherlands
,
Manon C.W. Spaander
 1   Departments of Gastroenterology and Hepatology, Erasmus University Medical Centre, Rotterdam, The Netherlands
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Abstract

Background and study aims Gastric cancer (GC) is usually preceded by premalignant gastric lesions (GPLs) such as gastric intestinal metaplasia (GIM). Information on risk factors associated with neoplastic progression of GIM are scarce. This study aimed to identify predictors for progression of GIM in areas with low GC incidence.

Patients and methods The Progression and Regression of Precancerous Gastric Lesions (PROREGAL) study includes patients with GPL. Patients underwent at least two upper endoscopies with random biopsy sampling. Progression of GIM means an increase in severity according to OLGIM (operative link on gastric intestinal metaplasia) during follow-up (FU). Family history and lifestyle factors were determined through questionnaires. Serum Helicobacter pylori infection, pepsinogens (PG), gastrin-17 and GC-associated single nucleotide polymorphisms (SNPs) were determined. Cox regression was performed for risk analysis and a chi-squared test for analysis of single nucleotide polymorphisms.

Results Three hundred and eight patients (median age at inclusion 61 years, interquartile range (IQR: 17; male 48.4 %; median FU 48 months, IQR: 24) were included. During FU, 116 patients (37.7 %) showed progression of IM and six patients (1.9 %) developed high-grade dysplasia or GC. The minor allele (C) on TLR4 (rs11536889) was inversely associated with progression of GIM (OR 0.6; 95 %CI 0.4–1.0). Family history (HR 1.5; 95 %CI 0.9–2.4) and smoking (HR 1.6; 95 %CI 0.9–2.7) showed trends towards progression of GIM. Alcohol use, body mass index, history of H. pylori infection, and serological markers were not associated with progression.

Conclusions Family history and smoking appear to be related to an increased risk of GIM progression in low GC incidence countries. TLR4 (rs11536889) showed a significant inverse association, suggesting that genetic information may play a role in GIM progression.

Supplementary material



Publication History

Received: 28 May 2020
Received: 22 September 2020

Article published online:
18 February 2021

© 2021. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commecial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/)

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  • References

  • 1 IARC Working Group. Schistosomes, liver flukes and Helicobacter pylori. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Lyon, 7–14 June 1994. IARC Monogr Eval Carcinog Risks Hum 1994; 61: 1-241
    PubMedGoogle Scholar
  • 2 Plummer M, Franceschi S, Vignat J. et al. Global burden of gastric cancer attributable to Helicobacter pylori. Int J Cancer 2015; 136: 487-490
    CrossrefPubMedGoogle Scholar
  • 3 Fock KM, Talley N, Moayyedi P. et al. Asia-Pacific consensus guidelines on gastric cancer prevention. J Gastroenterol Hepatol 2008; 23: 351-365
    CrossrefPubMedGoogle Scholar
  • 4 Dinis-Ribeiro M, Areia M, de Vries AC. et al. Management of precancerous conditions and lesions in the stomach (MAPS): guideline from the European Society of Gastrointestinal Endoscopy (ESGE), European Helicobacter Study Group (EHSG), European Society of Pathology (ESP), and the Sociedade Portuguesa de Endoscopia Digestiva (SPED). Endoscopy 2012; 44: 74-94
    Article in Thieme ConnectPubMedGoogle Scholar
  • 5 Trieu JA, Bilal M, Saraireh H. et al. Update on the diagnosis and management of gastric intestinal metaplasia in the USA. Dig Dis Sci 2019; 64: 1079-1088
    CrossrefPubMedGoogle Scholar
  • 6 Banks M, Graham D, Jansen M. et al. British Society of Gastroenterology guidelines on the diagnosis and management of patients at risk of gastric adenocarcinoma. Gut 2019; 68: 1545-1575
    CrossrefPubMedGoogle Scholar
  • 7 Evans JA, Chandrasekhara V. ASGE Standard of Practice Committee. et al. The role of endoscopy in the management of premalignant and malignant conditions of the stomach. Gastrointest Endosc 2015; 82: 1-8
    CrossrefPubMedGoogle Scholar
  • 8 Gupta S, Li D, El Serag HB. et al. AGA Clinical Practice Guidelines on Management of Gastric Intestinal Metaplasia. Gastroenterology 2020; 158: 693-702
    CrossrefPubMedGoogle Scholar
  • 9 Pimentel-Nunes P, Libanio D, Marcos-Pinto R. et al. Management of epithelial precancerous conditions and lesions in the stomach (MAPS II): European Society of Gastrointestinal Endoscopy (ESGE), European Helicobacter and Microbiota Study Group (EHMSG), European Society of Pathology (ESP), and Sociedade Portuguesa de Endoscopia Digestiva (SPED) guideline update 2019. Endoscopy 2019; 51: 365-388
    Article in Thieme ConnectPubMedGoogle Scholar
  • 10 Oliveira C, Pinheiro H, Figueiredo J. et al. Familial gastric cancer: genetic susceptibility, pathology, and implications for management. Lancet Oncol 2015; 16: e60-70
    CrossrefPubMedGoogle Scholar
  • 11 Yaghoobi M, Bijarchi R, Narod SA. Family history and the risk of gastric cancer. Br J Cancer 2010; 102: 237-242
    CrossrefPubMedGoogle Scholar
  • 12 Safaee A, Moghimi-Dehkordi B, Fatemi SR. et al. Family history of cancer and risk of gastric cancer in Iran. Asian Pac J Cancer Prev 2011; 12: 3117-3120
    PubMedGoogle Scholar
  • 13 Castano-Rodriguez N, Kaakoush NO, Goh KL. et al. The role of TLR2, TLR4 and CD14 genetic polymorphisms in gastric carcinogenesis: a case-control study and meta-analysis. PLoS One 2013; 8: e60327
    CrossrefPubMedGoogle Scholar
  • 14 Castano-Rodriguez N, Kaakoush NO, Pardo AL. et al. Genetic polymorphisms in the Toll-like receptor signalling pathway in Helicobacter pylori infection and related gastric cancer. Hum Immunol 2014; 75: 808-815
    CrossrefPubMedGoogle Scholar
  • 15 Castano-Rodriguez N, Kaakoush NO, Goh KL. et al. Autophagy in Helicobacter pylori infection and related gastric cancer. Helicobacter 2015; 20: 353-369
    CrossrefPubMedGoogle Scholar
  • 16 Leung WK, Lin SR, Ching JY. et al. Factors predicting progression of gastric intestinal metaplasia: results of a randomised trial on Helicobacter pylori eradication. Gut 2004; 53: 1244-1249
    CrossrefPubMedGoogle Scholar
  • 17 Rota M, Pelucchi C, Bertuccio P. et al. Alcohol consumption and gastric cancer risk-A pooled analysis within the StoP project consortium. Int J Cancer 2017; 141: 1950-1962
    CrossrefPubMedGoogle Scholar
  • 18 Huang YK, Yu JC, Kang WM. et al. Significance of serum pepsinogens as a biomarker for gastric cancer and atrophic gastritis screening: a systematic review and Meta-Analysis. PLoS One 2015; 10: e0142080
    CrossrefPubMedGoogle Scholar
  • 19 Hunt RH, Camilleri M, Crowe SE. et al. The stomach in health and disease. Gut 2015; 64: 1650-1668
    CrossrefPubMedGoogle Scholar
  • 20 den Hollander WJ, Holster IL, den Hoed CM. et al. Surveillance of premalignant gastric lesions: a multicentre prospective cohort study from low incidence regions. Gut 2018; 68: 585-593
    CrossrefPubMedGoogle Scholar
  • 21 Yue H, Shan L, Bin L. The significance of OLGA and OLGIM staging systems in the risk assessment of gastric cancer: a systematic review and meta-analysis. Gastric Cancer 2018; 21: 579-587
    CrossrefPubMedGoogle Scholar
  • 22 Tang FB, Li ZX, Wang YM. et al. Toll-like receptor 1 and 10 polymorphisms, Helicobacter pylori susceptibility and risk of gastric lesions in a high-risk Chinese population. Infect Genet Evol 2015; 31: 263-269
    CrossrefPubMedGoogle Scholar
  • 23 Zhang K, Zhou B, Wang Y. et al. The TLR4 gene polymorphisms and susceptibility to cancer: a systematic review and meta-analysis. Eur J Cancer 2013; 49: 946-954
    CrossrefPubMedGoogle Scholar
  • 24 Ryan BM, Zanetti KA, Robles AI. et al. Germline variation in NCF4, an innate immunity gene, is associated with an increased risk of colorectal cancer. Int J Cancer 2014; 134: 1399-1407
    CrossrefPubMedGoogle Scholar
  • 25 Burada F, Ciurea ME, Nicoli R. et al. ATG16L1 T300A polymorphism is correlated with gastric cancer susceptibility. Pathol Oncol Res 2016; 22: 317-322
    CrossrefPubMedGoogle Scholar
  • 26 Ikram MA, Brusselle GGO, Murad SD. et al. The Rotterdam Study: 2018 update on objectives, design and main results. Eur J Epidemiol 2017; 32: 807-850
    CrossrefPubMedGoogle Scholar
  • 27 Peduzzi P, Concato J, Feinstein AR. et al. Importance of events per independent variable in proportional hazards regression analysis. II. Accuracy and precision of regression estimates. J Clin Epidemiol 1995; 48: 1503-1510
    CrossrefPubMedGoogle Scholar
  • 28 Zagari RM, Rabitti S, Greenwood DC. et al. Systematic review with meta-analysis: diagnostic performance of the combination of pepsinogen, gastrin-17 and anti-Helicobacter pylori antibodies serum assays for the diagnosis of atrophic gastritis. Aliment Pharmacol Ther 2017; 46: 657-667
    CrossrefPubMedGoogle Scholar
  • 29 Wong BC, Lam SK, Wong WM. et al. Helicobacter pylori eradication to prevent gastric cancer in a high-risk region of China: a randomized controlled trial. Jama 2004; 291: 187-194
    CrossrefPubMedGoogle Scholar
  • 30 Ma JL, Zhang L, Brown LM. et al. Fifteen-year effects of Helicobacter pylori, garlic, and vitamin treatments on gastric cancer incidence and mortality. J Natl Cancer Inst 2012; 104: 488-492
    CrossrefPubMedGoogle Scholar
  • 31 Lin XJ, Wang CP, Liu XD. et al. Body mass index and risk of gastric cancer: a meta-analysis. Jpn J Clin Oncol 2014; 44: 783-791
    CrossrefPubMedGoogle Scholar
  • 32 Kneller RW, You WC, Chang YS. et al. Cigarette smoking and other risk factors for progression of precancerous stomach lesions. J Natl Cancer Inst 1992; 84: 1261-1266
    CrossrefPubMedGoogle Scholar
  • 33 Okada E, Ukawa S, Nakamura K. et al. Demographic and lifestyle factors and survival among patients with esophageal and gastric cancer: The Biobank Japan Project. J Epidemiol 2017; 27: S29-S35
    CrossrefPubMedGoogle Scholar
  • 34 Tramacere I, Negri E, Pelucchi C. et al. A meta-analysis on alcohol drinking and gastric cancer risk. Ann Oncol 2012; 23: 28-36
    CrossrefPubMedGoogle Scholar
  • 35 Kim K, Chang Y, Ahn J. et al. Smoking and urinary cotinine levels are predictors of increased risk for gastric intestinal metaplasia. Cancer Res 2019; 79: 676-684
    CrossrefPubMedGoogle Scholar
  • 36 Nieminen AA, Kontto J, Puolakkainen P. et al. Long-term gastric cancer risk in male smokers with atrophic corpus gastritis. Scand J Gastroenterol 2019; 54: 145-151
    CrossrefPubMedGoogle Scholar
  • 37 Altayar O, Davitkov P, Shah SC. et al. AGA technical review on gastric intestinal metaplasia-epidemiology and risk factors. Gastroenterology 2020; 158: 732-744 e716
    CrossrefPubMedGoogle Scholar
  • 38 Leja M, Kupcinskas L, Funka K. et al. Value of gastrin-17 in detecting antral atrophy. Adv Med Sci 2011; 56: 145-150
    CrossrefPubMedGoogle Scholar
  • 39 Lahner E, Esposito G, Pilozzi E. et al. Occurrence of gastric cancer and carcinoids in atrophic gastritis during prospective long-term follow up. Scand J Gastroenterol 2015; 50: 856-865
    CrossrefPubMedGoogle Scholar
  • 40 Reddy KM, Chang JI, Shi JM. et al. Risk of gastric cancer among patients with intestinal metaplasia of the stomach in a US integrated health care system. Clin Gastroenterol Hepatol 2016; 14: 1420-1425
    CrossrefPubMedGoogle Scholar
  • 41 Cooney R, Baker J, Brain O. et al. NOD2 stimulation induces autophagy in dendritic cells influencing bacterial handling and antigen presentation. Nat Med 2010; 16: 90-97
    CrossrefPubMedGoogle Scholar
  • 42 Mommersteeg MC, Yu J, Peppelenbosch MP. et al. Genetic host factors in Helicobacter pylori-induced carcinogenesis: Emerging new paradigms. Biochim Biophys Acta Rev Cancer 2018; 1869: 42-52
    CrossrefPubMedGoogle Scholar
  • 43 Mayerle J, den Hoed CM, Schurmann C. et al. Identification of genetic loci associated with Helicobacter pylori serologic status. JAMA 2013; 309: 1912-1920
    CrossrefPubMedGoogle Scholar
  • 44 Dargiene G, Streleckiene G, Skieceviciene J. et al. TLR1 and PRKAA1 gene polymorphisms in the development of atrophic gastritis and gastric cancer. J Gastrointestin Liver Dis 2018; 27: 363-369
    CrossrefPubMedGoogle Scholar
  • 45 Loh M, Koh KX, Yeo BH. et al. Meta-analysis of genetic polymorphisms and gastric cancer risk: variability in associations according to race. Eur J Cancer 2009; 45: 2562-2568
    CrossrefPubMedGoogle Scholar
  • 46 Lu B, Chen MT, Fan YH. et al. Effects of Helicobacter pylori eradication on atrophic gastritis and intestinal metaplasia: a 3-year follow-up study. World J Gastroenterol 2005; 11: 6518-6520
    CrossrefPubMedGoogle Scholar
  • 47 Sung JJ, Lin SR, Ching JY. et al. Atrophy and intestinal metaplasia one year after cure of H. pylori infection: a prospective, randomized study. Gastroenterology 2000; 119: 7-14
    CrossrefPubMedGoogle Scholar